Applications of NMR spectroscopy to systems biochemistry

Progress in Nuclear Magnetic Resonance Spectroscopy

Volumn 92-93, Issue , 2016, Pages 18-53

  Fan, Teresa W M ^a   Lane, Andrew N ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

Author keywords

Hyperpolarization; In vivo NMR; Metabolic network and flux; Stable isotope resolved metabolomics; Stable isotope tracers

Indexed keywords

BIOCHEMISTRY; ISOMERS; MASS SPECTROMETRY; METABOLISM; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY;

HYPERPOLARIZATION; IN-VIVO; METABOLIC NETWORK; METABOLOMICS; STABLE ISOTOPE TRACERS;

ISOTOPES;

CARBON;

ANIMAL; CHEMISTRY; HUMAN; ISOTOPE LABELING; METABOLISM; MOUSE; NUCLEAR MAGNETIC RESONANCE; NUCLEAR MAGNETIC RESONANCE IMAGING; PROCEDURES; RAT; SYSTEMS BIOLOGY;

ANIMALS; CARBON ISOTOPES; HUMANS; ISOTOPE LABELING; MAGNETIC RESONANCE IMAGING; METABOLIC NETWORKS AND PATHWAYS; MICE; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; RATS; SYSTEMS BIOLOGY;

EID: 84958981814     PISSN: 00796565     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pnmrs.2016.01.005     Document Type: Review

References (386)

1. E. Purcell, H. Torrey, and R. Pound Resonance absorption by nuclear magnetic moments in a solid Phys. Rev. 69 1946 37 38
2. F. Bloch Nuclear induction Phys. Rev. 70 1946 460 474
3. T.W.M. Fan, R.M. Higashi, A.N. Lane, and O. Jardetzky Combined use of proton NMR and gas chromatography-mass spectra for metabolite monitoring and in vivo proton NMR assignments Biochim. Biophys. Acta 882 1986 154 167
4. W.T. Evanochko, T.T. Sakai, T.C. Ng, N.R. Krishna, H.D. Kim, R.B. Zeidler, V.K. Ghanta, R.W. Brockman, L.M. Schiffer, and et al. NMR study of in-vivo Rif-1 tumors analysis of perchloric-acid extracts and identification of proton phosphorus-31 and carbon-13 resonances Biochim. Biophys. Acta 805 1984 104 116
5. J.R. Bales, D.P. Higham, I. Howe, J.K. Nicholson, and P.J. Sadler Use of high-resolution proton nuclear magnetic resonance spectroscopy for rapid multi-component analysis of urine Clin. Chem. 30 1984 426 432
6. J.K. Nicholson, M.J. Buckingham, and P.J. Sadler High-resolution H-1-NMR studies of vertebrate blood and plasma Biochem. J. 211 1983 605 615
7. C. Chen, F.J. Gonzalez, and J.R. Idle LC-MS-based metabolomics in drug metabolism Drug Metab. Rev. 39 2007 581 597
8. T.O. Metz, Q. Zhang, J.S. Page, Y. Shen, S.J. Callister, J.M. Jacobs, and R.D. Smith The future of liquid chromatography-mass spectrometry (LC-MS) in metabolic profiling and metabolomic studies for biomarker discovery Biomark Med. 1 2007 159 185
9. G.A. Theodoridis, H.G. Gika, E.J. Want, and I.D. Wilson Liquid chromatography-mass spectrometry based global metabolite profiling: a review Anal. Chim. Acta 711 2012 7 16
10. L.W. Sumner, and M. Bedair Current and emerging mass-spectrometry technologies for metabolomics TRAC - Trends Anal. Chem. 27 2008 238 250
11. T.W. Fan, P.K. Lorkiewicz, K. Sellers, H.N. Moseley, R.M. Higashi, and A.N. Lane Stable isotope-resolved metabolomics and applications for drug development Pharmacol. Ther. 133 2012 366 391
12. J.K.M. Sanders, and B.K. Hunter Modern NMR Spectroscopy. A Guide for Chemists 1987 Oxford University Press Oxford, UK
13. K. Wüthrich NMR of Proteins and Nucleic Acids 1986 Wiley New York
14. B.J. Dewar, K. Keshari, R. Jeffries, P. Dzeja, L.M. Graves, and J.M. Macdonald Metabolic assessment of a novel chronic myelogenous leukemic cell line and an imatinib resistant subline by H-1 NMR spectroscopy Metabolomics 6 2010 439 450
15. J.M. Posma, I. Garcia-Perez, M. De Iorio, J.C. Lindon, P. Elliott, E. Holmes, T.M.D. Ebbels, and J.K. Nicholson Subset optimization by reference matching (STORM): an optimized statistical approach for recovery of metabolic biomarker structural information from H-1 NMR spectra of biofluids Anal. Chem. 84 2012 10694 10701
16. H. Der-Torossian, S.A. Asher, J.H. Winnike, A. Wysong, X.Y. Yin, M.S. Willis, T.M. O'Connell, and M.E. Couch Cancer cachexia's metabolic signature in a murine model confirms a distinct entity Metabolomics 9 2013 730 739
17. S.L. Robinette, J.C. Lindon, and J.K. Nicholson Statistical spectroscopic tools for biomarker discovery and systems medicine Anal. Chem. 85 2013 5297 5303
18. C. Chen, L.L. Deng, S.W. Wei, G.A.N. Gowda, H.W. Gu, E.G. Chiorean, M. Abu Zaid, M.L. Harrison, J.F. Pekny, P.J. Loehrer, D.B. Zhang, M. Zhang, and D. Raftery Exploring metabolic profile differences between colorectal polyp patients and controls using seemingly unrelated regression J. Proteome Res. 14 2015 2492 2499
19. A.H. Emwas, C. Luchinat, P. Turano, L. Tenori, R. Roy, R.M. Salek, D. Ryan, J.S. Merzaban, R. Kaddurah-Daouk, A.C. Zeri, G.A.N. Gowda, D. Raftery, Y.L. Wang, L. Brennan, and D.S. Wishart Standardizing the experimental conditions for using urine in NMR-based metabolomic studies with a particular focus on diagnostic studies: a review Metabolomics 11 2015 872 894
20. R. Kaddurah-Daouk, and R. Weinshilboum Metabolomic signatures for drug response phenotypes: pharmacometabolomics enables precision medicine Clin. Pharmacol. Ther. 98 2015 71 75 (N. Pharmacometabolomics Res)
21. T.W.-M. Fan, P. Lorkiewicz, K. Sellers, H.N.B. Moseley, R.M. Higashi, and A.N. Lane Stable isotope-resolved metabolomics and applications to drug development Pharmacol. Ther. 133 2012 366 391
22. T.W.-M. Fan, and A.N. Lane Structure-based profiling of metabolites and isotopomers by NMR Progr. NMR Spectrosc. 52 2008 69 117
23. T.W.-M. Fan Metabolite profiling by one- and two-dimensional NMR analysis of complex mixtures Prog. Nucl. Magn. Reson. Spectrosc. 28 1996 161 219
24. K. Bingol, D.-W. Li, L. Bruschweiler-Li, O.A. Cabrera, T. Megraw, F. Zhang, and R. Brueschweiler Unified and isomer-specific NMR metabolomics database for the accurate analysis of C-13-H-1 HSQC spectra ACS Chem. Biol. 10 2015 452 459
25. K. Bingol, and R. Brueschweiler NMR/MS translator for the enhanced simultaneous analysis of metabolomics mixtures by NMR spectroscopy and mass spectrometry: application to human urine J. Proteome Res. 14 2015 2642 2648
26. T.W.-M. Fan, and A.N. Lane Assignment strategies for NMR resonances in metabolomics research N. Lutz, J.V. Sweedler, R.A. Weevers, Methodologies for Metabolomics: Experimental Strategies and Techniques 2013 Cambridge University Press Cambridge
27. A.M. Weljie, J. Newton, P. Mercier, E. Carlson, and C.M. Slupsky Targeted profiling: quantitative analysis of H-1 NMR metabolomics data Anal. Chem. 78 2006 4430 4442
28. A.N. Lane NMR applications in metabolomics T.W.-M. Fan, A.N. Lane, R.M. Higashi, Handbook of Metabolomics 2012 Humana
29. T.W.-M. Fan, and A.N. Lane Assignment strategies for NMR resonances in metabolomics research N. Lutz, J.V. Sweedler, R.A. Weevers, Methodologies for Metabolomics: Experimental Strategies and Techniques 2012 Cambridge University Press Cambridge
30. R.M. Horak, P.S. Steyn, and R. Vleggaar Carbon-carbon coupling-constants derived from biosynthetic-studies Magn. Reson. Chem. 23 1985 995 1039
31. A.N. Lane, S. Arumugam, P.K. Lorkiewicz, R.M. Higashi, S. Laulhe, M.H. Nantz, H.N.B. Moseley, and T.W.M. Fan Chemoselective detection and discrimination of carbonyl-containing compounds in metabolite mixtures by H-1-detected N-15 nuclear magnetic resonance Magn. Reson. Chem. 53 2015 337 343
32. M.J. Gradwell, T.W.M. Fan, and A.N. Lane Analysis of phosphorylated metabolites in crayfish extracts by two-dimensional H-1-P-31 NMR heteronuclear total correlation spectroscopy (HeteroTOCSY) Anal. Biochem. 263 1998 139 149
33. 15N-cholamine - a smart isotope tag for combining NMR- and MS-based metabolite profiling Anal. Chem. 85 2013 8715 8721
34. 15N tag for sensitive and high-resolution nuclear magnetic resonance profiling of the carboxyl-containing metabolome Anal. Chem. 81 2009 4882 4888
35. S.S. Gori, P.K. Lorkiewicz, D.S. Ehringer, A.C. Belshoff, R.M. Higashi, T.W.-M. Fan, and M.H. Nantz Profiling thiol metabolites and quantification of cellular glutathione using FT-ICR-MS spectrometry Anal. Bioanal. Chem. 406 2014 4371 4379
36. M. Bousamra 2nd, E. Schumer, M. Li, R. Knipp, M.H. Nantz, and V.F.X. van Berkel Quantitative analysis of exhaled carbonyl compounds distinguishes benign from malignant pulmonary disease J. Thorac. Cardiovasc. Surg. 148 2014 1074 1080
37. S.J. Mattingly, T. Xu, M.H. Nantz, R.M. Higashi, and T.W.M. Fan A carbonyl capture approach for profiling oxidized metabolites in cell extracts Metabolomics 8 2012 989 996
38. R.A. Shaykhutdinov, G.D. MacInnis, R. Dowlatabadi, A.M. Weljie, and H.J. Vogel Quantitative analysis of metabolite concentrations in human urine samples using C-13{H-1} NMR spectroscopy Metabolomics 5 2009 307 317
39. C.S. Clendinen, B. Lee-McMullen, C.M. Williams, G.S. Stupp, K. Vandenborne, D.A. Hahn, G.A. Walter, and A.S. Edison C-13 NMR metabolomics: applications at natural abundance Anal. Chem. 86 2014 9242 9250
40. K. Bingol, and R. Brueschweiler Multidimensional approaches to NMR-based metabolomics Anal. Chem. 86 2014 47 57
41. K. Bingol, L. Bruschweiler-Li, D.-W. Li, and R. Brueschweiler Customized metabolomics database for the analysis of NMR H-1-H-1 TOCSY and C-13-H-1 HSQC-TOCSY spectra of complex mixtures Anal. Chem. 86 2014 5494 5501
42. C.S. Clendinen, C. Pasquel, R. Ajredini, and A.S. Edison C-13 NMR metabolomics: INADEQUATE network analysis Anal. Chem. 87 2015 5698 5706
43. A.D. Hegeman, C.F. Schulte, Q. Cui, I.A. Lewis, E.L. Huttlin, H. Eghbalnia, A.C. Harms, E.L. Ulrich, J.L. Markley, and M.R. Sussman Stable isotope assisted assignment of elemental compositions for metabolomics Anal. Chem. 79 2007 6912 6921
44. F.A. de Jong, and C. Beecher Addressing the current bottlenecks of metabolomics: isotopic ratio outlier analysis (TM), an isotopic-labeling technique for accurate biochemical profiling Bioanalysis 4 2012 2303 2314
45. G.S. Stupp, C.S. Clendinen, R. Ajredini, M.A. Szewc, T. Garret, R.F. Menger, R.A. Yost, C. Beecher, and A.S. Edison Isotopic ratio outlier analysis global metabolomics of Caenorhabditis elegans Anal. Chem. 85 2013 11858 11865
46. M. Barfield DFT/FPT studies of the structural dependencies of long-range H-1, H-1 coupling over four bonds (4)J(H,H′) in propanic and allylic systems Magn. Reson. Chem. 41 2003 344 358
47. M. Barfield, A.J. Dingley, J. Feigon, and S. Grzesiek A DFT study of the interresidue dependencies of scalar J-coupling and magnetic shielding in the hydrogen-bonding regions of a DNA tripler J. Am. Chem. Soc. 123 2001 4014 4022
48. Y.Y. Rusakov, and L.B. Krivdin Four-component relativistic DFT calculations of Se-77 NMR chemical shifts: a gateway to a reliable computational scheme for the medium-sized organoselenium molecules J. Comput. Chem. 36 2015 1756 1762
49. A.C. Dona, B. Jimenez, H. Schaefer, E. Humpfer, M. Spraul, M.R. Lewis, J.T.M. Pearce, E. Holmes, J.C. Lindon, and J.K. Nicholson Precision high-throughput proton NMR spectroscopy of human urine, serum, and plasma for large-scale metabolic phenotyping Anal. Chem. 86 2014 9887 9894
50. T. Bally, and P.R. Rablen Quantum-chemical simulation of H-1 NMR spectra. 2. Comparison of DFT-based procedures for computing proton-proton coupling constants in organic molecules J. Org. Chem. 76 2011 4818 4830
51. C. Choi, S.K. Ganji, R.J. DeBerardinis, K.J. Hatanpaa, D. Rakheja, Z. Kovacs, X.L. Yang, T. Mashimo, J.M. Raisanen, I. Marin-Valencia, J.M. Pascual, C.J. Madden, B.E. Mickey, C.R. Malloy, R.M. Bachoo, and E.A. Maher 2-Hydroxyglutarate detection by magnetic resonance spectroscopy in subjects with IDH-mutated gliomas Nat. Med. 18 2012 624 629
52. L. Dang, D.W. White, S. Gross, B.D. Bennett, M.A. Bittinger, E.M. Driggers, V.R. Fantin, H.G. Jang, S. Jin, M.C. Keenan, K.M. Marks, R.M. Prins, P.S. Ward, K.E. Yen, L.M. Liau, J.D. Rabinowitz, L.C. Cantley, C.B. Thompson, M.G.V. Heiden, and S.M. Su Cancer-associated IDH1 mutations produce 2-hydroxyglutarate Nature 462 2009 U739 U752
53. Y. Achouri, G. NoëL, D. Vertommen, M.H. Rider, M. Veiga-Da-Cunha, and E. van Schaftingen Identification of a dehydrogenase acting on d-2-hydroxyglutarate Biochem. J. 381 2004 35 42
54. M. Kranendijk, E.A. Struys, G.S. Salomons, M.S. Van der Knaap, and C. Jakobs Progress in understanding 2-hydroxyglutaric acidurias J. Inherit. Metab. Dis. 35 2012 571 587
55. R. Rzem, M.F. Vincent, E. Van Schaftingen, and M. Veiga-da-Cunha l-2-Hydroxyglutaric aciduria, a defect of metabolite repair J. Inherit. Metab. Dis. 30 2007 681 689
56. E.A. Struys, G.S. Salomons, Y. Achouri, E. Van Schaftingen, S. Grosso, W.J. Craigen, N.M. Verhoeven, and C. Jakobs Mutations in the d-2-hydroxyglutarate dehydrogenase gene cause d-2-hydroxyglutaric aciduria Am. J. Hum. Genet. 76 2005 358 360
57. A.N. Lane, T.W. Fan, and R.M. Higashi Isotopomer-based metabolomic analysis by NMR and mass spectrometry Biophys. Tools Biol. 84 2008 541 588
58. M. Fasano, S. Curry, E. Terreno, M. Galliano, G. Fanali, P. Narciso, S. Notari, and P. Ascenzi The extraordinary ligand binding properties of human serum albumin IUMBM Life 57 2005 787 796
59. J.B. Henry, R.A. McPherson, and M.R. Pincus Henry's Clinical Diagnosis and Management by Laboratory Methods 22nd ed. 2011 Elsevier/Saunders Philadelphia
60. M. Jupin, P.J. Michiels, F.C. Girard, M. Spraul, and S.S. Wijmenga NMR identification of endogenous metabolites interacting with fatted and non-fatted human serum albumin in blood plasma: fatty acids influence the HSA-metabolite interaction J. Magn. Reson. 228 2013 81 94
61. M. Jupin, P.J. Michiels, F.C. Girard, M. Spraul, and S.S. Wijmenga NMR metabolomics profiling of blood plasma mimics shows that medium- and long-chain fatty acids differently release metabolites from human serum albumin J. Magn. Reson. 239 2014 34 43
62. S. Akoka, L. Barantin, and M. Trierweiler Concentration measurement by proton NMR using the ERETIC method Anal. Chem. 71 1999 2554 2557
63. G.A.N. Gowda, and D. Raftery Quantitating metabolites in protein precipitated serum using NMR spectroscopy Anal. Chem. 86 2014 5433 5440
64. G.A.N. Gowda, Y.N. Gowda, and D. Raftery Expanding the limits of human blood metabolite quantitation using NMR spectroscopy Anal. Chem. 87 2015 706 715
65. T.W.-M. Fan Sample preparation for metabolomics investigation T.W.-M. Fan, A.N. Lane, R.M. Higashi, The Handbook of Metabolomics: Pathway and Flux Analysis, Methods in Pharmacology and Toxicology 2012 Springer Science New York 7 27 10.1007/978-1-61779-618-0-11
66. J.C. Lindon, J.K. Nicholson, and J.R. Everett NMR spectroscopy of biofluids Annual Reports on NMR Spectroscopy vol. 38 1999 Academic Press Inc. San Diego 1 88
67. J.K. Nicholson, P.J.D. Foxall, M. Spraul, R.D. Farrant, and J.C. Lindon 750-MHz H-1 and H-1-C-13 NMR-spectroscopy of human blood-plasma Anal. Chem. 67 1995 793 811
68. K. Sellers, M.P. Fox, M. Bousamra, S. Slone, R.M. Higashi, D.M. Miller, Y. Wang, J. Yan, M.O. Yuneva, R. Deshpande, A.N. Lane, and T.W.-M. Fan Pyruvate carboxylase is critical for non-small-cell lung cancer proliferation J. Clin. Invest. 125 2015 687 698
69. I.A. Lewis, S.C. Schommer, B. Hodis, K.A. Robb, M. Tonelli, W.M. Westler, M.R. Suissman, and J.L. Markley Method for determining molar concentrations of metabolites in complex solutions from two-dimensional H-1-C-13 NMR spectra Anal. Chem. 79 2007 9385 9390
70. I.A. Lewis, M.R. Shortreed, A.D. Hegeman, and J.L. Markley Novel NMR and MS approaches to metabolomics T.W.-M. Fan, A.N. Lane, R.M. Higashi, The Handbook of Metabolomics 2012 Humana New York 199 230
71. K. Hu, J.J. Ellinger, R.A. Chylla, and J.L. Markley Measurement of absolute concentrations of individual compounds in metabolite mixtures by gradient-selective time-zero H-1-C-13 HSQC with two concentration references and fast maximum likelihood reconstruction analysis Anal. Chem. 83 2011 9352 9360
72. 1H TOCSY Metabolomics 3 2007 79 86
73. T.W. Fan, and A.N. Lane Structure-based profiling of metabolites and isotopomers by NMR Progr. NMR Spectrosc. 52 2008 69 117
74. A. Le, A.N. Lane, M. Hamaker, S. Bose, J. Barbi, T. Tsukamoto, C.J. Rojas, B.S. Slusher, H. Zhang, L.J. Zimmerman, D.C. Liebler, R.J.C. Slebos, P.K. Lorkiewicz, R.M. Higashi, T.W.-M. Fan, and C.V. Dang Myc induction of hypoxic glutamine metabolism and a glucose-independent TCA cycle in human B lymphocytes Cell Metab. 15 2012 110 121
75. D.I. Hoult, and R.E. Richards The signal-to-noise ratio of the nuclear magnetic resonance experiment J. Magn. Reson. 24 1969 71 85
76. V. Ramaswamy, J.W. Hooker, R.S. Withers, R.E. Nast, W.W. Brey, and A.S. Edison Development of a C-13-optimized 1.5-mm high temperature superconducting NMR probe J. Magn. Reson. 235 2013 58 65
77. W.W. Brey, A.E. Edison, R.E. Nast, J.R. Rocca, S. Saha, and R.S. Withers Design, construction, and validation of a 1-mm triple-resonance high-temperature-superconducting probe for NMR J. Magn. Res. 179 2006 290 293
78. E.B. Henry Osmolarity of human serum and of chemical solutions of biologic importance Clin. Chem. 7 1961 156 164
79. A.N. Lane The stability of intramolecular DNA quadruplexes compared with other macromolecules Biochimie 2011 10.1016/j.biochi.2011.08.004
80. A.N. Lane, and S. Arumugam Improving NMR sensitivity in room temperature and cooled probes with dipolar ions J. Magn. Reson. 173 2005 339 343
81. T.W.M. Fan, R.M. Higashi, T.A. Frenkiel, and A.N. Lane Anaerobic nitrate and ammonium metabolism in flood-tolerant rice coleoptiles J. Exp. Bot. 48 1997 1655 1666
82. J. Ippel, S. Wijmenga, B. de Jong, H. Heus, C. Hilbers, E. Vroom, C. van de Marel, and J. van Boom Heteronuclear scalar couplings in the bases and sugar rings of nucleic acids: their determination and application in assignment and conformational analysis Magn. Reson. Chem. 34 1996 S156 S176
83. A.N. Lane, S. Arumugam, P.K. Lorkiewicz, R.M. Higashi, S. Laulhe, M.H. Nantz, H.N.B. Moseley, and T.W.-M. Fan Chemoselective detection of carbonyl compounds in metabolite mixtures by NMR Magn. Res. Chem. 2015
84. T.W.-M. Fan, and A.N. Lane NMR-based stable isotope resolved metabolomics in systems biochemistry J. Biomol. NMR 49 2011 267 280
85. C.R. Malloy, E. Maher, I. Marin-Valenica, B. Mickey, R.J. DeBerardinis, and A.D. Sherry Carbon-13 nuclear magnetic resonance for analysis of metabolic pathways N. Lutz, J.V. Sweedler, R.A. Weevers, Methodologies for Metabolomics: Experimental Strategies and Techniques 2013 Cambridge University Press Cambridge 415 445
86. R.T. Williamson, A.V. Buevich, and G.E. Martin Using LR-HSQMBC to observe long-range H-1-N-15 correlations Tetrahedron Lett. 55 2014 3365 3366
87. G.E. Martin, K.A. Blinov, and R.T. Williamson HMBC-1,n-ADEQUATE spectra calculated from HMBC and 1,n-ADEQUATE spectra Magn. Reson. Chem. 51 2013 299 307
88. D. Mueller, and E. Heinzle Stable isotope-assisted metabolomics to detect metabolic flux changes in mammalian cell cultures Curr. Opin. Biotechnol. 24 2013 54 59
89. W. Wiechert, and K. Noh Isotopically non-stationary metabolic flux analysis: complex yet highly informative Curr. Opin. Biotechnol. 24 2013 979 986
90. H.N.B. Moseley, A.N. Lane, A.C. Belshoff, R.M. Higashi, and T.W.-M. Fan Non-steady state modeling of UDP-GlcNAc biosynthesis is enabled by stable isotope resolved metabolomics (SIRM) BMC Biol. 9 2011 37
91. T.H. Yang Metabolic flux analysis T.W. Fan, A.N. Lane, R.M. Higashi, The Handbook of Metabolomics 2012 Humana Totoya 231 277
92. K.M. Brindle Imaging metabolism with hyperpolarized C-13-labeled cell substrates J. Am. Chem. Soc. 137 2015 6418 6427
93. S. Niedenfuhr, W. Wiechert, and K. Noh How to measure metabolic fluxes: a taxonomic guide for (13)C fluxomics Curr. Opin. Biotechnol. 34 2015 82 90
94. J.M. Buescher, M.R. Antoniewicz, L.G. Boros, S.C. Burgess, H. Brunengraber, C.B. Clish, R.J. DeBerardinis, O. Feron, C. Frezza, B. Ghesquiere, E. Gottlieb, K. Hiller, R.G. Jones, J.J. Kamphorst, R.G. Kibbey, A.C. Kimmelman, J.W. Locasale, S.Y. Lunt, O.D. Maddocks, C. Malloy, C.M. Metallo, E.J. Meuillet, J. Munger, K. Noh, J.D. Rabinowitz, M. Ralser, U. Sauer, G. Stephanopoulos, J. St-Pierre, D.A. Tennant, C. Wittmann, M.G. Vander Heiden, A. Vazquez, K. Vousden, J.D. Young, N. Zamboni, and S.-M. Fendt A roadmap for interpreting (13)C metabolite labeling patterns from cells Curr. Opin. Biotechnol. 34 2015 189 201
95. S.-M. Fendt, E.L. Bell, M.A. Keibler, B.A. Olenchock, J.R. Mayers, T.M. Wasylenko, N.I. Vokes, L. Guarente, M.G. Vander Heiden, and G. Stephanopoulos Reductive glutamine metabolism is a function of the alpha-ketoglutarate to citrate ratio in cells Nat. Commun. 4 2013
96. T.W.M. Fan, A.N. Lane, and R.M. Higashi In vivo and in vitro metabolomic analysis of anaerobic rice coleoptiles revealed unexpected pathways Russ. J. Plant Physiol. 50 2003 787 793
97. T.W. Fan, A.N. Lane, R.M. Higashi, M.A. Farag, H. Gao, M. Bousamra, and D.M. Miller Altered regulation of metabolic pathways in human lung cancer discerned by (13)C stable isotope-resolved metabolomics (SIRM) Mol. Cancer 8 2009 41
98. A. Le, A.N. Lane, M. Hamaker, S. Bose, A. Gouw, J. Barbi, T. Tsukamoto, C.J. Rojas, B.S. Slusher, H. Zhang, L.J. Zimmerman, D.C. Liebler, R.J. Slebos, P.K. Lorkiewicz, R.M. Higashi, T.W. Fan, and C.V. Dang Glucose-independent glutamine metabolism via TCA cycling for proliferation and survival in B cells Cell Metab. 15 2012 110 121
99. W. Liu, A. Le, C. Hancock, A.N. Lane, C.V. Dang, T.W. Fan, and J.M. Phang Reprogramming of proline and glutamine metabolism contributes to the proliferative and metabolic responses regulated by oncogenic transcription factor c-MYC Proc. Natl. Acad. Sci. U.S.A. 109 2012 8983 8988
100. Y. Yang, A.N. Lane, C.J. Ricketts, C. Sourbier, M.H. Wei, B. Shuch, L. Pike, M. Wu, T.A. Rouault, L.G. Boros, T.W. Fan, and W.M. Linehan Metabolic reprogramming for producing energy and reducing power in fumarate hydratase null cells from hereditary leiomyomatosis renal cell carcinoma PLoS ONE 8 2013 e72179
101. H. Xie, J.I. Hanai, J.G. Ren, L. Kats, K. Burgess, P. Bhargava, S. Signoretti, J. Billiard, K.J. Duffy, A. Grant, X. Wang, P.K. Lorkiewicz, S. Schatzman, M. Bousamra 2nd, A.N. Lane, R.M. Higashi, T.W. Fan, P.P. Pandolfi, V.P. Sukhatme, and P. Seth Targeting lactate dehydrogenase-A inhibits tumorigenesis and tumor progression in mouse models of lung cancer and impacts tumor-initiating cells Cell Metab. 19 2014 1 15
102. C. Dong, T. Yuan, Y. Wu, Y. Wang, T.W. Fan, S. Miriyala, Y. Lin, J. Yao, J. Shi, T. Kang, P. Lorkiewicz, D. St Clair, M.C. Hung, B.M. Evers, and B.P. Zhou Loss of FBP1 by snail-mediated repression provides metabolic advantages in basal-like breast cancer Cancer Cell 23 2013 316 331
103. J.G. Ren, P. Seth, C.B. Clish, P.K. Lorkiewicz, R.M. Higashi, A.N. Lane, T.W. Fan, and V.P. Sukhatme Knockdown of malic enzyme 2 suppresses lung tumor growth, induces differentiation and impacts PI3K/AKT signaling Sci. Rep. 4 2014 5414
104. S. Guin, C. Pollard, Y. Ru, C. Ritterson Lew, J.E. Duex, G. Dancik, C. Owens, A. Spencer, S. Knight, H. Holemon, S. Gupta, D. Hansel, M. Hellerstein, P. Lorkiewicz, A.N. Lane, T.W. Fan, and D. Theodorescu Role in tumor growth of a glycogen debranching enzyme lost in glycogen storage disease J. Natl Cancer Inst. 106 2014
105. T.W. Fan, A.N. Lane, R.M. Higashi, and J. Yan Stable isotope resolved metabolomics of lung cancer in a SCID mouse model Metabolomics 7 2011 257 269
106. T.W. Fan, P. Yuan, A.N. Lane, R.M. Higashi, Y. Wang, A.B. Hamidi, R. Zhou, X. Guitart, G. Chen, H.K. Manji, and R. Kaddurah-Daouk Stable isotope-resolved metabolomic analysis of lithium effects on glial-neuronal metabolism and interactions Metabolomics 6 2010 165 179
107. K. Sellers, M.P. Fox, M. Bousamra II, S.P. Slone, R.M. Higashi, D.M. Miller, Y. Wang, J. Yan, M.O. Yuneva, R. Deshpande, A.N. Lane, and T.W.M. Fan Pyruvate carboxylase is critical for non-small-cell lung cancer proliferation J. Clin. Invest. 125 2015 687 698
108. T. Fan, L. Bandura, R. Higashi, and A. Lane Metabolomics-edited transcriptomics analysis of Se anticancer action in human lung cancer cells Metabolomics 1 2005 325 339
109. K. Chang, and J.K.M. Roberts Quantitation of rates of transport, metabolic fluxes, and cytoplasmic levels of inorganic carbon in maize root tips during potassium ion uptake Plant Physiol. (Rockville) 99 1992 291 297
110. 13C nuclear magnetic resonance studies of glucose metabolism in Escherichia coli Proc. Natl. Acad. Sci. 75 1978 3742 3746
111. 13C NMR isotopomer analysis reveals a connection between pyruvate cycling and glucose-stimulated insulin secretion (GSIS) Proc. Natl. Acad. Sci. U.S.A. 99 2002 2708 2713
112. 13C NMR spectroscopy studies of forest soil microbial activity: glucose uptake and fatty acid biosynthesis Soil Biol. Biochem. 33 2001 621 632
113. 13C NMR, MS and metabolic flux balancing in biotechnology research Quart. Rev. Biophys. 31 1998 41 106
114. 13C)glucose incubation Eur. J. Biochem. 217 1993 457 468
115. K.J.M. Liu, R. Kleps, T. Henderson, and L. Nyhus C-13 NMR-study of hepatic pyruvate-carboxylase activity in tumor rats Biochem. Biophys. Res. Commun. 179 1991 366 371
116. 13C NMR spectroscopy NMR Biomed. 16 2003 424 429
117. C. Yang, A. Richardson, A. Osterman, and J. Smith Profiling of central metabolism in human cancer cells by two-dimensional NMR, GC-MS analysis, and isotopomer modeling Metabolomics 2008
118. 1H NMR analysis of the lactate methyl signal Magn. Reson. Med. 51 2004 1283 1286
119. 13C NMR labeling kinetics in perfused EMT6 mouse mammary tumor cells and betaHC9 mouse insulinomas Biotechnol. Bioeng. 87 2004 835 848
120. 13C-NMR evidence of bacteriochlorophyll a formation by the C5 pathway in Chromatium Arch. Biochem. Biophys. 246 1986 192 198
121. J.G. Jones, M.A. Solomon, S.M. Cole, A.D. Sherry, and C.R. Malloy An integrated (2)H and (13)C NMR study of gluconeogenesis and TCA cycle flux in humans Am. J. Physiol. Endocrinol. Metab. 281 2001 E848 E856
122. 13C NMR measurements of liver glycogen in vivo Magn. Reson. Med. 31 1994 583 588
123. 13C NMR spectroscopy NMR Biomed. 11 1998 395 404
124. 31P NMR study Magn. Reson. Med. 32 1994 303 309
125. 13C NMR spectroscopy of the brain NMR Biomed. 16 2003 313 338
126. 13C NMR assessment of brain glycogen concentration and turnover in the awake rat Neurochem. Int. 43 2003 317 322
127. 13C NMR measurements of muscle glycogen during low-intensity exercise J. Appl. Physiol. 70 1991 1836 1844
128. A. Mancuso, S.T. Sharfstein, S.N. Tucker, D.S. Clark, and H.W. Blanch Examination of primary metabolic pathways in a murine hybridoma with carbon-13 nuclear magnetic resonance spectroscopy Biotechnol. Bioeng. 44 1994 563 585
129. R.J. DeBerardinis, A. Mancuso, E. Daikhin, I. Nissim, M. Yudkoff, S. Wehrli, and C.B. Thompson Beyond aerobic glycolysis: transformed cells can engage in glutamine metabolism that exceeds the requirement for protein and nucleotide synthesis Proc. Natl. Acad. Sci. U.S.A. 104 2007 19345 19350
130. 13C] NMR spectroscopy in vivo. A practical guide NMR Biomed. 24 2011 958 972
131. 13C MRS studies of neuroenergetics and neurotransmitter cycling in humans NMR Biomed. 24 2011 943 957
132. 13C nuclear magnetic resonance: applications and current limitations for noninvasive assessment of fatty acid status Lipids 31 1996 S127 S130
133. 13C]glucose metabolites J. Biol. Chem. 269 1994 27198 27208
134. 13C)-glucose metabolism in tumors by heteronuclear cross polarization Magn. Reson. Med. 33 1995 151 155
135. O. Kaplan, M. Firon, A. Vivi, G. Navon, and I. Tsarfaty HGF/SF activates glycolysis and oxidative phosphorylation in DA3 murine mammary cancer cells Neoplasia 2 2000 365 377
136. 2+](o) Am. J. Physiol. - Heart Circul. Physiol. 287 2004 H889 H895
137. R.L. Dobbins, and C.R. Malloy Measuring in-vivo metabolism using nuclear magnetic resonance Curr. Opin. Clin. Nutr. Metab. Care 6 2003 501 509
138. E.S. Jin, J.G. Jones, S.C. Burgess, M.E. Merritt, A.D. Sherry, and C.R. Malloy Comparison of [3,4-C-13(2)]glucose to [6,6-H-2(2)]glucose as a tracer for glucose turnover by nuclear magnetic resonance Magn. Reson. Med. 53 2005 1479 1483
139. A.D. Sherry, F.M.H. Jeffrey, and C.R. Malloy Analytical solutions for C-13 isotopomer analysis of complex metabolic conditions: substrate oxidation, multiple pyruvate cycles, and gluconeogenesis Metab. Eng. 6 2004 12 24
140. E.S. Jin, J.G. Jones, M. Merritt, S.C. Burgess, C.R. Malloy, and A.D. Sherry Glucose production, gluconeogenesis, and hepatic tricarboxylic acid cycle fluxes measured by nuclear magnetic resonance analysis of a single glucose derivative Anal. Biochem. 327 2004 149 155
141. A.N. Lane, T.W. Fan, Z. Xie, H.N. Moseley, and R.M. Higashi Isotopomer analysis of lipid biosynthesis by high resolution mass spectrometry and NMR Anal. Chim. Acta 651 2009 201 208
142. 15N nuclear magnetic resonance Magn. Reson. Chem. 53 2015 337 343
143. G.M. Clore, and A.M. Gronenborn NMR structure determination of proteins and protein complexes larger than 20 kDa Curr. Opin. Chem. Biol. 2 1998 564 570
144. A. Bax Multidimensional nuclear-magnetic-resonance methods for protein studies Curr. Opin. Struct. Biol. 4 1994 738 744
145. M. Ikura, and A. Bax Isotope-filtered 2d NMR of a protein peptide complex - study of a skeletal-muscle myosin light chain kinase fragment bound to calmodulin J. Am. Chem. Soc. 114 1992 2433 2440
146. G. Otting, and K. Wüthrich Heteronuclear filters in 2-dimensional H-1, H-1 NMR-spectroscopy - combined use with isotope labeling for studies of macromolecular conformation and intermolecular interactions Q. Rev. Biophys. 23 1990 39 96
147. L.P. McIntosh, and F.W. Dahlquist Biosynthetic incorporation of N-15 and C-13 for assignment and interpretation of nuclear-magnetic-resonance spectra of proteins Q. Rev. Biophys. 23 1990 1 38
148. S.W. Fesik, and E.R.P. Zuiderweg Heteronuclear 3-dimensional NMR-spectroscopy of isotopically labeled biological macromolecules Q. Rev. Biophys. 23 1990 97 131
149. H. Senn, G. Otting, and K. Wüthrich Protein-structure and interactions by combined use of sequential NMR assignments and isotope labeling J. Am. Chem. Soc. 109 1987 1090 1092
150. K.H. Gardner, and L.E. Kay The use of H-2, C-13, N-15 multidimensional NMR to study the structure and dynamics of proteins Annu. Rev. Biophys. Biomol. Struct. 27 1998 357 406
151. J. Qin, G.M. Clore, and A.M. Gronenborn Ionization equilibria for side-chain carboxyl groups in oxidized and reduced human thioredoxin and in the complex with its target peptide from the transcription factor NF kappa B Biochemistry 35 1996 7 13
152. M.F. Jeng, and H.J. Dyson Direct measurement of the aspartic acid 26 pK(a) for reduced Escherichia coli thioredoxin by C-13 NMR Biochemistry 35 1996 1 6
153. M.H. Levitt, and R.R. Ernst Improvement of pulse performance in N.M.R. coherence transfer experiments Mol. Phys. 50 1983 1109 1124
154. J.C. Hoch, M.W. Maciejewski, M. Mobli, A.D. Schuyler, and A.S. Stern Nonuniform sampling and maximum entropy reconstruction in multidimensional NMR Acc. Chem. Res. 47 2014 708 717
155. R. Freeman, and E. Kupče Distant echoes of the accordion: reduced dimensionality, GFT-NMR, and projection-reconstruction of multidimensional spectra Conc. Magn. Reson. A 23A 2004 63 75
156. T. Szyperski, and H.S. Atreya Principles and applications of GFT projection NMR spectroscopy Magn. Reson. Chem. 44 2006 S51 S60
157. R.A. Carvalho, F.M.H. Jeffrey, A.D. Sherry, and C.R. Malloy C-13 isotopomer analysis of glutamate by heteronuclear multiple quantum coherence total correlation spectroscopy (HMQC-TOCSY) FEBS Lett. 440 1998 382 386
158. R.H. Lenox, G.J. Kant, and J.L. Meyerhoff Rapid enzyme inactivation A. Lajtha, Handbook of Neurochemistry 1982 Plenum Press New York 77 102
159. A. Wollenberger, O. Ristau, and G. Schoffa Eine einfache Technik der extrem schnellen Abkühlung größerer Gewebestücke Pflügers Arch. 270 1960 399 412
160. G. Lazzarino, M. Nuutinen, B. Tavazzi, D. Di Pierro, and B. Giardina A method for preparing freeze-clamped tissue samples for metabolite analyses Anal. Biochem. 181 1989 239 241
161. Q. Teng, W. Huang, T. Collette, D. Ekman, and C. Tan A direct cell quenching method for cell-culture based metabolomics Metabolomics 5 2009 199 208
162. W. de Koning, and K. van Dam A method for the determination of changes of glycolytic metabolites in yeast on a subsecond time scale using extraction at neutral pH Anal. Biochem. 204 1992 118 123
163. C.L. Winder, W.B. Dunn, S. Schuler, D. Broadhurst, R. Jarvis, G.M. Stephens, and R. Goodacre Global metabolic profiling of Escherichia coli cultures: an evaluation of methods for quenching and extraction of intracellular metabolites Anal. Chem. 80 2008 2939 2948
164. C.A. Sellick, R. Hansen, A.R. Maqsood, W.B. Dunn, G.M. Stephens, R. Goodacre, and A.J. Dickson Effective quenching processes for physiologically valid metabolite profiling of suspension cultured mammalian cells Anal. Chem. 81 2009 174 183
165. S.G. Villas-Bôas, and P. Bruheim Cold glycerol-saline: the promising quenching solution for accurate intracellular metabolite analysis of microbial cells Anal. Biochem. 370 2007 87 97
166. A. Buchholz, J. Hurlebaus, C. Wandrey, and R. Takors Metabolomics: quantification of intracellular metabolite dynamics Biomol. Eng. 19 2002 5 15
167. C.J. Bolten, P. Kiefer, F. Letisse, J.C. Portais, and C. Wittmann Sampling for metabolome analysis of microorganisms Anal. Chem. 79 2007 3843 3849
168. H. Link, B. Anselment, and D. Weuster-Botz Leakage of adenylates during cold methanol/glycerol quenching of Escherichia coli Metabolomics 4 2008 240 247
169. 1H NMR metabolite fingerprinting and metabolomic analysis of perchloric acid extracts from plant tissues Nat. Protoc. 3 2008 1001 1012
170. A. Moreno, and C. Arus Quantitative and qualitative characterization of H-1 NMR spectra of colon tumors, normal mucosa and their perchloric acid extracts: decreased levels of myo-inositol in tumours can be detected in intact biopsies NMR Biomed. 9 1996 33 45
171. U. Flogel, W. Willker, J. Engelmann, T. Niendorf, and D. Leibfritz Adaptation of cellular metabolism to anisosmotic conditions in a glial cell line, as assessed by C-13-NMR spectroscopy Dev. Neurosci. 18 1996 449 459
172. M.C. Martinez-Bisbal, L. Marti-Bonmati, J. Piquer, A. Revert, P. Ferrer, J.L. Llacer, M. Piotto, O. Assemat, and B. Celda H-1 and C-13 HR-MAS spectroscopy of intact biopsy samples ex vivo and in vivo H-1 MRS study of human high grade gliomas NMR Biomed. 17 2004 191 205
173. 13C-isotopic enrichment of malonyl-coenzyme A by gas chromatography-mass spectrometry Anal. Biochem. 298 2001 69 75
174. 31P NMR and HPLC studies of mouse L1210 Leukemia cell extracts: the effect of Au(I) and Cu(I) diphosphine complexes on the cell metabolism Magn. Reson. Med. 18 1991 142 158
175. M. Faijes, A. Mars, and E. Smid Comparison of quenching and extraction methodologies for metabolome analysis of Lactobacillus plantarum Microb. Cell Fact. 6 2007 27
176. R.M. Higashi, T.W.M. Fan, and J.M. Macdonald Monitoring of metabolic responses of intact haliotis (abalones) under salinity stress by P-31 surface probe localized NMR J. Exp. Zool. 249 1989 350 356
177. T.W. Fan, M. Kucia, K. Jankowski, R.M. Higashi, J. Ratajczak, M.Z. Ratajczak, and A.N. Lane Rhabdomyosarcoma cells show an energy producing anabolic metabolic phenotype compared with primary myocytes Mol. Cancer 7 2008 79
178. T.W.-M. Fan, J.L. Tan, M.M. McKinney, and A.N. Lane Stable isotope resolved metabolomics analysis of ribonucleotide and RNA metabolism in human lung cancer cells Metabolomics 8 2012 517 527
179. P. Lorkiewicz, R.M. Higashi, A.N. Lane, and T.W. Fan High information throughput analysis of nucleotides and their isotopically enriched isotopologues by direct-infusion FTICR-MS Metab.: Off. J. Metab. Soc. 8 2012 930 939
180. H.N. Moseley, A.N. Lane, A.C. Belshoff, R.M. Higashi, and T.W. Fan A novel deconvolution method for modeling UDP-N-acetyl-d-glucosamine biosynthetic pathways based on (13)C mass isotopologue profiles under non-steady-state conditions BMC Biol. 9 2011 37
181. J.J. Sloth, E.H. Larsen, and K. Julshamn Determination of organoarsenic species in marine samples using gradient elution cation exchange HPLC-ICP-MS J. Anal. At. Spectrom. 18 2003 452 459
182. S.G. Villas-Bôas, J. Hojer-Pedersen, M. Akesson, J. Smedsgaard, and J. Nielsen Global metabolite analysis of yeast: evaluation of sample preparation methods Yeast 22 2005 1155 1169
183. L. Yang, T. Kasumov, L. Yu, K.A. Jobbins, F. David, S.F. Previs, J.K. Kelleher, and H. Brunengraber Metabolomic assays of the concentration and mass isotopomer distribution of gluconeogenic and citric acid cycle intermediates Metabolomics 2 2006 1573 3882
184. E.J. Want, G. O'Maille, C.A. Smith, T.R. Brandon, W. Uritboonthai, C. Qin, S.A. Trauger, and G. Siuzdak Solvent-dependent metabolite distribution, clustering, and protein extraction for serum profiling with mass spectrometry Anal. Chem. 78 2006 743 752
185. C. Wittmann, J.O. Kromer, P. Kiefer, T. Binz, and E. Heinzle Impact of the cold shock phenomenon on quantification of intracellular metabolites in bacteria Anal. Biochem. 327 2004 135 139
186. C.L. Winder, W.B. Dunn, S. Schuler, D. Broadhurst, R. Jarvis, G.M. Stephens, and R. Goodacre Global metabolic profiling of Escherichia coli cultures: an evaluation of methods for quenching and extraction of intracellular metabolites Anal. Chem. 80 2008 2939 2948
187. R.C. De Vos, S. Moco, A. Lommen, J.J. Keurentjes, R.J. Bino, and R.D. Hall Untargeted large-scale plant metabolomics using liquid chromatography coupled to mass spectrometry Nat. Protoc. 2 2007 778 791
188. J.D. Rabinowitz, and E. Kimball Acidic acetonitrile for cellular metabolome extraction from Escherichia coli Anal. Chem. 79 2007 6167 6173
189. E. Kimball, and J.D. Rabinowitz Identifying decomposition products in extracts of cellular metabolites Anal. Biochem. 358 2006 273 280
190. J.B. Ritter, Y. Genzel, and U. Reichl Simultaneous extraction of several metabolites of energy metabolism and related substances in mammalian cells: optimization using experimental design Anal. Biochem. 373 2008 349 369
191. C. Wittmann, J.O. Kromer, P. Kiefer, T. Binz, and E. Heinzle Impact of the cold shock phenomenon on quantification of intracellular metabolites in bacteria Anal. Biochem. 327 2004 135 139
192. G. Paglia, M. Magnusdottir, S. Thorlacius, O.E. Sigurjonsson, S. Guethmundsson, B.O. Palsson, and I. Thiele Intracellular metabolite profiling of platelets: evaluation of extraction processes and chromatographic strategies J. Chromatogr. B: Anal. Technol. Biomed. Life Sci. 898 2012 111 120
193. Y. Yang, C. Cruickshank, M. Armstrong, S. Mahaffey, R. Reisdorph, and N. Reisdorph New sample preparation approach for mass spectrometry-based profiling of plasma results in improved coverage of metabolome J. Chromatogr. A 1300 2013 217 226
194. V. Matyash, G. Liebisch, T.V. Kurzchalia, A. Shevchenko, and D. Schwudke Lipid extraction by methyl-tert-butyl ether for high-throughput lipidomics J. Lipid Res. 49 2008 1137 1146
195. S.K. Abbott, A.M. Jenner, T.W. Mitchell, S.H. Brown, G.M. Halliday, and B. Garner An improved high-throughput lipid extraction method for the analysis of human brain lipids Lipids 48 2013 307 318
196. A. Reis, A. Rudnitskaya, G.J. Blackburn, N.M. Fauzi, A.R. Pitt, and C.M. Spickett A comparison of five lipid extraction solvent systems for lipidomic studies of human LDL J. Lipid Res. 54 2013 1812 1824
197. J. Folch, M. Lees, and G.H. Sloane Stanley A simple method for the isolation and purification of total lipides from animal tissues J. Biol. Chem. 226 1957 497 509
198. 15N tag for sensitive and high-resolution nuclear magnetic resonance profiling of the carboxyl-containing metabolome Anal. Chem. 81 2009 4882 4888
199. 15N-cholamine - a smart isotope tag for combining NMR- and MS-based metabolite profiling Anal. Chem. 85 2013 8715 8721
200. G.A. Gowda, F. Tayyari, T. Ye, Y. Suryani, S. Wei, N. Shanaiah, and D. Raftery Quantitative analysis of blood plasma metabolites using isotope enhanced NMR methods Anal. Chem. 2010
201. S.S. Gori, P. Lorkiewicz, D.S. Ehringer, A.C. Belshoff, R.M. Higashi, T.W. Fan, and M.H. Nantz Profiling thiol metabolites and quantification of cellular glutathione using FT-ICR-MS spectrometry Anal. Bioanal. Chem. 406 2014 4371 4379
202. S. Moestue, B. Sitter, T. Bathen, M. Tessem, and I. Gribbestad HR MAS MR spectroscopy in metabolic characterization of cancer Curr. Top. Med. Chem. 11 2011 2 26
203. J.L. Griffin, C. Blenkiron, P.K. Valonen, C. Caldas, and R.A. Kauppinen High-resolution magic angle spinning H-1 NMR spectroscopy and reverse transcription-PCR analysis of apoptosis in a rat glioma Anal. Chem. 78 2006 1546 1552
204. A. Imperiale, F.-M. Moussallieh, P. Roche, S. Battini, A.E. Cicek, F. Sebag, L. Brunaud, A. Barlier, K. Elbayed, A. Loundou, P. Bachellier, B. Goichot, C.A. Stratakis, K. Pacak, I.-J. Namer, and d. Taieb Metabolome profiling by HRMAS NMR spectroscopy of pheochromocytomas and paragangliomas detects SDH deficiency: clinical and pathophysiological implications Neoplasia 17 2015 55 65
205. A. Solinas, M. Chessa, N. Culeddu, M.C. Porcu, G. Virgilio, F. Arcadu, A. Deplano, S. Cossu, D. Scanu, and V. Migaleddu High resolution-magic angle spinning (HR-MAS) NMR-based metabolomic fingerprinting of early and recurrent hepatocellular carcinoma Metabolomics 10 2014 616 626
206. M.A. Benahmed, K. Elbayed, F. Daubeuf, N. Santelmo, N. Frossard, and I.J. Namer NMR HRMAS spectroscopy of lung biopsy samples: comparison study between human, pig, rat, and mouse metabolomics Magn. Reson. Med. 71 2014 35 43
207. B.S. Somashekar, A.G. Amin, C.D. Rithner, J. Troudt, R. Basaraba, A. Izzo, D.C. Crick, and D. Chatterjee Metabolic profiling of lung granuloma in mycobacterium tuberculosis infected guinea pigs: ex vivo H-1 magic angle spinning NMR studies J. Proteome Res. 10 2011 4186 4195
208. G. Simon, N. Kervarec, and S. Cerantola HRMAS NMR analysis of algae and identification of molecules of interest via conventional 1D and 2D NMR: sample preparation and optimization of experimental conditions Methods Mol. Biol. (Clifton, N.J.) 1308 2015 191 205
209. M. Palomino-Schaetzlein, M. Micaela Molina-Navarro, M. Tormos-Perez, S. Rodriguez-Navarro, and A. Pineda-Lucena Optimised protocols for the metabolic profiling of S. cerevisiae by H-1-NMR and HRMAS spectroscopy Anal. Bioanal. Chem. 405 2013 8431 8441
210. M. Valentini, M. Ritota, C. Cafiero, S. Cozzolino, L. Leita, and P. Sequi The HRMAS-NMR tool in foodstuff characterisation Magn. Reson. Chem. 49 2011 S121 S125
211. C.M. Rocha, A.S. Barros, A.M. Gil, B.J. Goodfellow, E. Humpfer, M. Spraul, I.M. Carreira, J.B. Melo, J. Bernardo, A. Gomes, V. Sousa, L. Carvalho, and I.F. Duarte Metabolic profiling of human lung cancer tissue by H-1 high resolution magic angle spinning (HRMAS) NMR spectroscopy J. Proteome Res. 9 2010 319 332
212. B.J. Blaise, J. Giacomotto, M.N. Triba, P. Toulhoat, M. Piotto, L. Emsley, L. Segalat, M.-E. Dumas, and B. Elena Metabolic profiling strategy of Caenorhabditis elegans by whole-organism nuclear magnetic resonance J. Proteome Res. 8 2009 2542 2550
213. M. Coen, E. Holmes, J.C. Lindon, and J.K. Nicholson NMR-based metabolic profiling and metabonomic approaches to problems in molecular toxicology Chem. Res. Toxicol. 21 2008 9 27
214. A.D. Maher, J.C. Lindon, and J.K. Nicholson H-1 NMR-based metabonomics for investigating diabetes Fut. Med. Chem. 1 2009 737 747
215. A. Smolinska, L. Blanchet, L.M.C. Buydens, and S.S. Wijmenga NMR and pattern recognition methods in metabolomics: from data acquisition to biomarker discovery: a review Anal. Chim. Acta 750 2012 82 97
216. A.H.M. Emwas, R.M. Salek, J.L. Griffin, and J. Merzaban NMR-based metabolomics in human disease diagnosis: applications, limitations, and recommendations Metabolomics 9 2013 1048 1072
217. D. Rolin, C. Deborde, M. Maucourt, C. Cabasson, F. Fauvelle, D. Jacob, C. Canlet, A. Moing, High-resolution H-1-NMR spectroscopy and beyond to explore plant metabolome, in: D. Rolin (Ed.), Metabolomics Coming of Age with Its Technological Diversity, 2013, pp. 1-66.
218. L. Brennan NMR-based metabolomics: from sample preparation to applications in nutrition research Prog. Nucl. Magn. Reson. Spectrosc. 83 2014 42 49
219. C. Simmler, J.G. Napolitano, J.B. McAlpine, S.N. Chen, and G.F. Pauli Universal quantitative NMR analysis of complex natural samples Curr. Opin. Biotechnol. 25 2014 51 59
220. C.K. Larive, G.A. Barding, and M.M. Dinges NMR spectroscopy for metabolomics and metabolic profiling Anal. Chem. 87 2015 133 146
221. A.P. Sobolev, L. Mannina, N. Proietti, S. Carradori, M. Daglia, A.M. Giusti, R. Antiochia, and D. Capitani Untargeted NMR-based methodology in the study of fruit metabolites Molecules 20 2015 4088 4108
222. L.C. Tavares, I. Jarak, F.N. Nogueira, P.J. Oliveira, and R.A. Carvalho Metabolic evaluations of cancer metabolism by NMR-based stable isotope tracer methodologies Eur. J. Clin. Invest. 45 2015 37 43
223. K. Sellers, M.P. Fox, M. Bousamra II, S.P. Slone, R.M. Higashi, D.M. Miller, Y. Wang, J. Yan, M.O. Yuneva, R. Deshpande, A.N. Lane, and T.W.M. Fan Pyruvate carboxylase is critical for non-small-cell lung cancer proliferation J. Clin. Invest. 125 2015 687 698
224. T.W. Fan Considerations of sample preparation for metabolomics investigation Handb. Metab. 17 2012
225. A.N. Lane, and T.W.-M. Fan Regulation of mammalian nucleotide metabolism and biosynthesis Nucleic Acids Res. 43 2015 2466 2485
226. E.O. Weinman, E.H. Strisower, and I.L. Chaikoff Conversion of fatty acids to carbohydrate; application of isotopes to this problem and role of the Krebs cycle as a synthetic pathway Physiol. Rev. 37 1957 252 272
227. E.H. Strisower, G.D. Kohler, and I.L. Chaikoff Incorporation of acetate carbon into glucose by liver slices from normal and alloxan-diabetic rats J. Biol. Chem. 198 1952 115 126
228. D. Rittenberg, and R. Schoenheimer Deuterium as an indicator in study of intermediatory metabolism. VIII. Hydrogenation of fatty acids in the animals organism J. Biol. Chem. 117 1937 485 490
229. N. Tjandra, J.G. Omichinski, A.M. Gronenborn, G.M. Clore, and A. Bax Use of dipolar H-1-N-15 and H-1-C-13 couplings in the structure determination of magnetically oriented macromolecules in solution Nat. Struct. Biol. 4 1997 732 738
230. G.M. Clore, and J. Potts Recent Developments in Biomolecular NMR 2012 RSC Publishing
231. G. Barbato, M. Ikura, L.E. Kay, R.W. Pastor, and A. Bax Backbone dynamics of calmodulin studied by N-15 relaxation using inverse detected 2-dimensional NMR-spectroscopy - the central helix is flexible Biochemistry 31 1992 5269 5278
232. E. Kupče, and R. Freeman Fast multidimensional NMR: radial sampling of evolution space J. Magn. Reson. 173 2005 317 321
233. K. Pervushin, A. Ono, C. Fernandez, T. Szyperski, M. Kainosho, and K. Wüthrich NMR scaler couplings across Watson-Crick base pair hydrogen bonds in DNA observed by transverse relaxation optimized spectroscopy Proc. Natl. Acad. Sci. U.S.A. 95 1998 14147 14151
234. H.P.J. Bonarius, A. Ozemre, B. Timmerarends, P. Skrabal, J. Tramper, G. Schmid, and E. Heinzle Metabolic-flux analysis of continuously cultured hybridoma cells using (CO2)-C-13 mass spectrometry in combination with C-13-lactate nuclear magnetic resonance spectroscopy and metabolite balancing Biotechnol. Bioeng. 74 2001 528 538
235. 13C NMR isotopomer analysis of anaplerotic pathways in INS-1 cells J. Biol. Chem. 279 2004 44370 44375
236. C. Zwingmann, and D. Leibfritz Regulation of glial metabolism studied by C-13-NMR NMR Biomed. 16 2003 370 399
237. S.A. Wahl, M. Dauner, and W. Wiechert New tools for mass isotopomer data evaluation in C-13 flux analysis: mass isotope correction, data consistency checking, and precursor relationships Biotechnol. Bioeng. 85 2004 259 268
238. R.A. Carvalho, P. Zhao, C.B. Wiegers, F.M. Jeffrey, C.R. Malloy, and A.D. Sherry TCA cycle kinetics in the rat heart by analysis of (13)C isotopomers using indirect (1)H Am. J. Physiol. Heart Circ. Physiol. 281 2001 H1413 H1421
239. G.M. Chowdhury, M. Banasr, R.A. de Graaf, D.L. Rothman, K.L. Behar, and G. Sanacora Chronic riluzole treatment increases glucose metabolism in rat prefrontal cortex and hippocampus J. Cereb. Blood Flow Metab. 28 2008 1892 1897
240. M.O. Yuneva, T.W. Fan, T.D. Allen, R.M. Higashi, D.V. Ferraris, T. Tsukamoto, J.M. Mates, F.J. Alonso, C. Wang, Y. Seo, X. Chen, and J.M. Bishop The metabolic profile of tumors depends on both the responsible genetic lesion and tissue type Cell Metab. 15 2012 157 170
241. O. Warburg Is the respiration of cancer cells normal? Biochem. Zeitschr. 51 1924
242. 13C]glucose in human brain tumors in vivo NMR Biomed. 25 2012 1234 1244
243. K.M. Brindle NMR methods for measuring enzyme kinetics in vivo Prog. Nucl. Magn. Reson. Spectrosc. 20 1988 257 293
244. P. Selenko, and G. Wagner Looking into live cells with in-cell NMR spectroscopy J. Struct. Biol. 158 2007 244 253
245. J.-P. Grivet, and A.-M. Delort NMR for microbiology: in vivo and in situ applications Prog. Nucl. Magn. Reson. Spectrosc. 54 2009 1 53
246. D. Weuster-Botz, and A.A. de Graaf Reaction engineering methods to study intracellular metabolite concentrations Adv. Biochem. Eng. Biotechnol. 54 1996 75 108
247. 13C nuclear magnetic resonance studies of glucose metabolism in Escherichia coli Proc. Natl. Acad. Sci. U.S.A. 75 1978 3742 3746
248. 13C nuclear magnetic resonance studies of anaerobic glycolysis in suspensions of yeast cells Proc. Natl. Acad. Sci. U.S.A. 76 1979 6096 6100
249. A. Hartbrich, G. Schmitz, D. Weuster-Botz, A.A. de Graaf, and C. Wandrey Development and application of a membrane cyclone reactor for in vivo NMR spectroscopy with high microbial cell densities Biotechnol. Bioeng. 51 1996 624 635
250. J.L. Tholozan, J.P. Touzel, E. Samain, J.P. Grivet, G. Prensier, and G. Albagnac Clostridium neopropionicum sp. nov., a strict anaerobic bacterium fermenting ethanol to propionate through acrylate pathway Arch. Microbiol. 157 1992 249 257
251. P.D. Majors, J.S. McLean, G.E. Pinchuk, J.K. Fredrickson, Y.A. Gorby, K.R. Minard, and R.A. Wind NMR methods for in situ biofilm metabolism studies J. Microbiol. Methods 62 2005 337 344
252. 31P-NMR studies of human colon cancer in-vitro and in-vivo Surg. Oncol. 2 1993 7 18
253. Y. Shachar-Hill, P.E. Pfeffer, D. Douds, S.F. Osman, L.W. Doner, and R.G. Ratcliffe Partitioning of intermediary carbon metabolism in vesicular-arbuscular mycorrhizal leek Plant Physiol. (Rockville) 108 1995 7 15
254. T.W.M. Fan, A.N. Lane, and R.M. Higashi An electrophoretic profiling method for thiol-rich phytochelatins and metallothioneins Phytochem. Anal. 15 2004 175 183
255. S.C. Burgess, E.E. Babcock, F.M. Jeffrey, A.D. Sherry, and C.R. Malloy NMR indirect detection of glutamate to measure citric acid cycle flux in the isolated perfused mouse heart FEBS Lett. 505 2001 163 167
256. 13C-NMR J. Mol. Cell. Cardiol. 26 1994 1197 1210
257. N. Anousis, R.A. Carvalho, P. Zhao, C.R. Malloy, and A.D. Sherry Compartmentation of glycolysis and glycogenolysis in the perfused rat heart NMR Biomed. 17 2004 51 59
258. 31P NMR spectroscopy NMR Biomed. 10 1997 18 24
259. I. Marin-Valencia, S.K. Cho, D. Rakheja, K.J. Hatanpaa, P. Kapur, T. Mashimo, A. Jindal, V. Vemireddy, L.B. Good, J. Raisanen, X. Sun, B. Mickey, C. Choi, M. Takahashi, O. Togao, J.M. Pascual, R.J. Deberardinis, E.A. Maher, C.R. Malloy, and R.M. Bachoo Glucose metabolism via the pentose phosphate pathway, glycolysis and Krebs cycle in an orthotopic mouse model of human brain tumors NMR Biomed. 25 2012 1177 1186
260. P. Meric, G. Autret, B.T. Doan, B. Gillet, C. Sebrie, and J.C. Beloeil In vivo 2D magnetic resonance spectroscopy of small animals MAGMA 17 2004 317 338
261. 13C]-glucose and its metabolic products Magn. Reson. Med. 30 1993 544 551
262. 13C MRS studies of neuroenergetics and neurotransmitter cycling in humans NMR Biomed. 24 2011 943 957
263. 13C NMR for the assessment of human brain glucose metabolism in vivo Biochemistry 30 1991 6362 6366
264. 13C MRS in vivo NMR Biomed. 16 2003 358 369
265. G.F. Mason, K.F. Petersen, R.A. de Graaf, G.I. Shulman, and D.L. Rothman Measurements of the anaplerotic rate in the human cerebral cortex using C-13 magnetic resonance spectroscopy and [1-C-13] and [2-C-13] glucose J. Neurochem. 100 2007 73 86
266. 13C glucose in human brain tumors in vivo NMR Biomed. 25 2012 1234 1244
267. G.F. Mason, K.F. Petersen, R.A. de Graaf, T. Kanamatsu, T. Otsuki, and D.L. Rothman A comparison of C-13 NMR measurements of the rates of glutamine synthesis and the tricarboxylic acid cycle during oral and intravenous administration of 1-C-13 glucose (vol 10, pg 181, 2003) Brain Res. Protoc. 11 2003 143
268. K. Golman, R. in't Zandt, and M. Thaning Real-time metabolic imaging Proc. Natl. Acad. Sci. U.S.A. 103 2006 11270 11275
269. K. Golman, R. in't Zandt, M. Lerche, R. Pehrson, and J.H. Ardenkjaer-Larsen Metabolic imaging by hyperpolarized C-13 magnetic resonance imaging for in vivo tumor diagnosis Cancer Res. 66 2006 10855 10860
270. K. Golman, J.S. Petersson, P. Magnusson, E. Johansson, P. Akeson, C.M. Chai, G. Hansson, and S. Mansson Cardiac metabolism measured noninvasively by hyperpolarized C-13 MRI Magn. Reson. Med. 59 2008 1005 1013
271. K.R. Keshari, R. Sriram, B.L. Koelsch, M. Van Criekinge, D.M. Wilson, J. Kurhanewicz, and Z.J. Wang Hyperpolarized C-13-pyruvate magnetic resonance reveals rapid lactate export in metastatic renal cell carcinomas Cancer Res. 73 2013 529 538
272. J. Kurhanewicz, D.B. Vigneron, K. Brindle, E.Y. Chekmenev, A. Comment, C.H. Cunningham, R.J. DeBerardinis, G.G. Green, M.O. Leach, S.S. Rajan, R.R. Rizi, B.D. Ross, W.S. Warren, and C.R. Malloy Analysis of cancer metabolism by imaging hyperpolarized nuclei: prospects for translation to clinical research Neoplasia 13 2011 81 97
273. S. Hu, A. Balakrishnan, R.A. Bok, B. Anderton, P.E. Larson, S.J. Nelson, J. Kurhanewicz, D.B. Vigneron, and A. Goga (13)C-pyruvate imaging reveals alterations in glycolysis that precede c-Myc-induced tumor formation and regression Cell Metab. 14 2011 131 142
274. D.M. Wilson, K.R. Keshari, P.E.Z. Larson, A.P. Chen, S. Hu, M. Van Criekinge, R. Bok, S.J. Nelson, J.M. Macdonald, D.B. Vigneron, and J. Kurhanewicz Multi-compound polarization by DNP allows simultaneous assessment of multiple enzymatic activities in vivo J. Magn. Reson. 205 2010 141 147
275. M.R. Clatworthy, M.I. Kettunen, D.E. Hu, R.J. Mathews, T.H. Witney, B.W.C. Kennedy, S.E. Bohndiek, F.A. Gallagher, L.B. Jarvis, K.G.C. Smith, and K.M. Brindle Magnetic resonance imaging with hyperpolarized 1,4-C-13(2) fumarate allows detection of early renal acute tubular necrosis Proc. Natl. Acad. Sci. U.S.A. 109 2012 13374 13379
276. T.H. Witney, M.I. Kettunen, and K.M. Brindle Kinetic modeling of hyperpolarized C-13 label exchange between pyruvate and lactate in tumor cells J. Biol. Chem. 286 2011 24572 24580
277. T.B. Rodrigues, E.M. Serrao, B.W.C. Kennedy, D.E. Hu, M.I. Kettunen, and K.M. Brindle Magnetic resonance imaging of tumor glycolysis using hyperpolarized C-13-labeled glucose Nat. Med. 20 2014 93
278. B.W.C. Kennedy, M.I. Kettunen, D.E. Hu, and K.M. Brindle Probing lactate dehydrogenase activity in tumors by measuring hydrogen/deuterium exchange in hyperpolarized L-1-C-13, U-H-2 lactate J. Am. Chem. Soc. 134 2012 4969 4977
279. F.A. Gallagher, M.I. Kettunen, S.E. Day, D.E. Hu, M. Karlsson, A. Gisselsson, M.H. Lerche, and K.M. Brindle Detection of tumor glutamate metabolism in vivo using C-13 magnetic resonance spectroscopy and hyperpolarized 1-C-13 glutamate Magn. Reson. Med. 66 2011 18 23
280. F.A. Gallagher, M.I. Kettunen, and K.M. Brindle Imaging pH with hyperpolarized C-13 NMR Biomed. 24 2011 1006 1015
281. S.E. Bohndiek, M.I. Kettunen, D.E. Hu, B.W.C. Kennedy, J. Boren, F.A. Gallagher, and K.M. Brindle Hyperpolarized 1-C-13-ascorbic and dehydroascorbic acid: vitamin C as a probe for imaging redox status in vivo J. Am. Chem. Soc. 133 2011 11795 11801
282. F.A. Gallagher, M.I. Kettunen, D.E. Hu, P.R. Jensen, R. in't Zandt, M. Karlsson, A. Gisselsson, S.K. Nelson, T.H. Witney, S.E. Bohndiek, G. Hansson, T. Peitersen, M.H. Lerche, and K.M. Brindle Production of hyperpolarized 1,4-C-13(2) malate from 1,4-C-13(2) fumarate is a marker of cell necrosis and treatment response in tumors Proc. Natl. Acad. Sci. U.S.A. 106 2009 19801 19806
283. F.A. Gallagher, M.I. Kettunen, S.E. Day, D.E. Hu, J.H. Ardenkjaer-Larsen, R. in't Zandt, P.R. Jensen, M. Karlsson, K. Golman, M.H. Lerche, and K.M. Brindle Magnetic resonance imaging of pH in vivo using hyperpolarized (13)C-labelled bicarbonate Nature 453 2008 U940 U973
284. M.H. Lerche, P.R. Jensen, M. Karlsson, and S. Meier NMR insights into the inner workings of living cells Anal. Chem. 87 2015 119 132
285. P.R. Jensen, S.C. Serra, L. Miragoli, M. Karlsson, C. Cabella, L. Poggi, L. Venturi, F. Tedoldi, and M.H. Lerche Hyperpolarized 1,3-C-13(2) ethyl acetoacetate is a novel diagnostic metabolic marker of liver cancer Int. J. Cancer 136 2015 E117 E126
286. C. Canape, G. Catanzaro, E. Terreno, M. Karlsson, M.H. Lerche, and P.R. Jensen Probing treatment response of glutaminolytic prostate cancer cells to natural drugs with hyperpolarized 5-C-13 glutamine Magn. Reson. Med. 73 2015 2296 2305
287. C.E. Christensen, M. Karlsson, J.R. Winther, P.R. Jensen, and M.H. Lerche Non-invasive in-cell determination of free cytosolic NAD(+)/NADH ratios using hyperpolarized glucose show large variations in metabolic phenotypes J. Biol. Chem. 289 2014 2344 2352
288. P.R. Jensen, T. Peitersen, M. Karlsson, R. in't Zandt, A. Gisselsson, G. Hansson, S. Meier, and M.H. Lerche Tissue-specific short chain fatty acid metabolism and slow metabolic recovery after ischemia from hyperpolarized NMR in vivo J. Biol. Chem. 284 2009 36077 36082
289. K.M. Brindle New approaches for imaging tumour responses to treatment Nat. Rev. Cancer 8 2008 94 107
290. A. Comment, and M.E. Merritt Hyperpolarized magnetic resonance as a sensitive detector of metabolic function Biochemistry 53 2014 7333 7357
291. A. Abragam, and M. Goldman Principles of dynamic nuclear polarisation Rep. Prog. Phys. 41 1978 395 467
292. J.H. Ardenkjaer-Larsen, B. Fridlund, A. Gram, G. Hansson, L. Hansson, M.H. Lerche, R. Servin, M. Thaning, and K. Golman Increase in signal-to-noise ratio of >10,000 times in liquid-state NMR Proc. Natl. Acad. Sci. U.S.A. 100 2003 10158 10163
293. K.R. Albe, M.H. Butler, and B.E. Wright Cellular concentrations of enzymes and their substrates J. Theor. Biol. 143 1990 163 195
294. D.W. Maughan, J.A. Henkin, and J.O. Vigoreaux Concentrations of glycolytic enzymes and other cytosolic proteins in the diffusible fraction of a vertebrate muscle proteome Mol. Cell. Proteomics 4 2005 1541 1549
295. N.S. Madhukar, M.O. Warmoes, and J.W. Locasale Organization of enzyme concentration across the metabolic network in cancer cells PLoS ONE 10 2015 e0117131
296. A. Fersht Structure and Mechanism in Protein Science 1999 W.H. Freeman & Co. New York
297. P. Bhattacharya, E.Y. Chekmenev, W.F. Reynolds, S. Wagner, N. Zacharias, H.R. Chan, R. Bunger, and B.D. Ross Parahydrogen-induced polarization (PHIP) hyperpolarized MR receptor imaging in vivo: a pilot study of C-13 imaging of atheroma in mice NMR Biomed. 24 2011 1023 1028
298. C. Cai, A.M. Coffey, R.V. Shchepin, E.Y. Chekmenev, and K.W. Waddell Efficient transformation of parahydrogen spin order into heteronuclear magnetization J. Phys. Chem. B 117 2013 1219 1224
299. E.Y. Chekmenev, J. Hovener, V.A. Norton, K. Harris, L.S. Batchelder, P. Bhattacharya, B.D. Ross, and D.P. Weitekamp PASADENA hyperpolarization of succinic acid for MRI and NMR spectroscopy J. Am. Chem. Soc. 130 2008 4212
300. J.B. Hovener, E.Y. Chekmenev, K.C. Harris, W.H. Perman, L.W. Robertson, B.D. Ross, and P. Bhattacharya PASADENA hyperpolarization of C-13 biomolecules: equipment design and installation Magn. Reson. Mater. Phys., Biol. Med. 22 2009 111 121
301. J. Natterer, and J. Bargon Parahydrogen induced polarization Prog. Nucl. Magn. Reson. Spectrosc. 31 1997 293 315
302. M. Goldman, H. Johannesson, O. Axelsson, and M. Karlsson Design and implementation of C-13 hyperpolarization from para-hydrogen, for new MRI contrast agents C.R. Chim. 9 2006 357 363
303. 13C diethyl succinate J. Am. Chem. Soc. 134 2012 934 943
304. F. Reineri, T. Boi, and S. Aime ParaHydrogen induced polarization of C-13 carboxylate resonance in acetate and pyruvate Nat. Commun. 6 2015
305. F. Reineri, S. Bouguet-Bonnet, and D. Canet Creation and evolution of net proton hyperpolarization arising from para-hydrogenation J. Magn. Reson. 210 2011 107 112
306. R.V. Shchepin, A.M. Coffey, K.W. Waddell, and E.Y. Chekmenev PASADENA hyperpolarized C-13 phospholactate J. Am. Chem. Soc. 134 2012 3957 3960
307. S.E. Day, M.I. Kettunen, F.A. Gallagher, D.E. Hu, M. Lerche, J. Wolber, K. Golman, J.H. Ardenkjaer-Larsen, and K.M. Brindle Detecting tumor response to treatment using hyperpolarized C-13 magnetic resonance imaging and spectroscopy Nat. Med. 13 2007 1382 1387
308. O. Warburg Versuche an überlebendem Carcinomgewebe (Methoden) Biochem. Zeitschr. 142 1923 317 333
309. O. Warburg On the origin of cancer cells Science 123 1956 309 314
310. K. Garber Energy boost: the Warburg effect returns in a new theory of cancer J. Natl. Cancer Inst. 96 2004 1805 1806
311. H. Xie, J. Hanai, J.-G. Ren, L. Kats, K. Burgess, P. Bhargava, S. Signoretti, J. Billiard, K.J. Duffy, A. Grant, X. Wang, P.K. Lorkiewicz, S. Schatzman, M. Bousamra II, A.N. Lane, R.M. Higashi, T.W.-M. Fan, P.P.P. Pandolfi, V.P. Sukhatme, and P. Seth Targeting lactate dehydrogenase-A (LDH-A) inhibits tumorigenesis and tumor progression in mouse models of lung cancer and impacts tumor initiating cells Cell Metab. 19 2014 795 809
312. B.A. Webb, M. Chimenti, M.P. Jacobson, and D.L. Barber Dysregulated pH: a perfect storm for cancer progression Nat. Rev. Cancer 11 2011 671 677
313. M.V. Shirmanova, I.N. Druzhkova, M.M. Lukina, M.E. Matlashov, V.V. Belousov, L.B. Snopova, N.N. Prodanetz, V.V. Dudenkova, S.A. Lukyanov, and E.V. Zagaynova Intracellular pH imaging in cancer cells in vitro and tumors in vivo using the new genetically encoded sensor SypHer2 Biochim. Biophys. Acta - Gen. Subj. 2015 1850 1905 1911
314. M.T. Hakala, A.J. Glaid, and G.W. Schwert Lactic dehydrogenase. II. Variation of kinetics and equilibrium constants with temperature J. Biol. Chem. 221 1956 191 210
315. S. Lin, and L. Guarente Nicotinamide adenine dinucleotide, a metabolic regulator of transcription, longevity and disease" Curr. Opin. Cell Biol. 15 2003 241 246
316. R.L. Veech, L.V. Eggleston, and H.A. Krebs The redox state of free nicotinamide-adenine dinucleotide phosphate in the cytoplasm of rat liver Biochem. J. 115 4 1969 609 619
317. S.-M. Jeon, N.S. Chandel, and N. Hay AMPK regulates NADPH homeostasis to promote tumour cell survival during energy stress Nature 485 2012 661
318. J. Fan, J.B. Ye, J.J. Kamphorst, T. Shlomi, C.B. Thompson, and J.D. Rabinowitz Quantitative flux analysis reveals folate-dependent NADPH production Nature 510 2014 298
319. M.W. Dzierlenga, D. Antoniou, and S.D. Schwartz Another look at the mechanisms of hydride transfer enzymes with quantum and classical transition path sampling J. Phys. Chem. Lett. 6 2015 117 1181
320. P.J. Berti, and K.S.E. Tanaka Transition state analysis using multiple kinetic isotope effects: mechanisms of enzymatic and non-enzymatic glycoside hydrolysis and transfer Adv. Phys. Org. Chem. 37 2002 239 314
321. J.M. Poulo, T. Elston, A.N. Lane, J.M. Macdonald, and M. Cascante Introduction to metabolic control analysis (MCA) T.W.-M. Fan, R.M. Higashi, A.N. Lane, Handbook of Metabolomics 2012 Humana Press
322. I.A. Rose The use of kinetic isotope effects in the study of metabolic control J. Biol. Chem. 236 1961 603 609
323. S. Meier, P.R. Jensen, and J.O. Duus Real-time detection of central carbon metabolism in living Escherichia coli and its response to perturbations FEBS Lett. 585 2012 3133 3138
324. S. Hu, H.A.I. Yoshihara, R. Bok, J. Zhou, M.H. Zhu, J. Kurhanewicz, and D.B. Vigneron Use of hyperpolarized 1-C-13 pyruvate and 2-C-13 pyruvate to probe the effects of the anticancer agent dichloroacetate on mitochondrial metabolism in vivo in the normal rat Magn. Reson. Imaging 30 2012 1367 1372
325. A.L. Harzstark, V.K. Weinberg, K. Grycz, R.E. Hurd, J.H. Ardenkjaer-Larsen, J. Murray, A. Chen, M. Ferrone, I. Park, G. Reed, P.N. Munster, E.J. Small, L.E. Carvajal, M.E. VanCriekinge, P.E. Larson, J. Chang, R.A. Bok, S.J. Nelson, D.B. Vigneron, and J.V. Kurhanewicz A first-in-human phase I imaging study using hyperpolarized (1)C-13 pyruvate (h-Py) in patients (pts) with localized prostate cancer (I-PCa) J. Clin. Oncol. 30 2012
326. A.P. Chen, R.E. Hurd, M.A. Schroeder, A.Z. Lau, Y.P. Gu, W.W. Lam, J. Barry, J. Tropp, and C.H. Cunningham Simultaneous investigation of cardiac pyruvate dehydrogenase flux, Krebs cycle metabolism and pH, using hyperpolarized 1,2-C-13(2) pyruvate in vivo NMR Biomed. 25 2012 305 311
327. P. Seth, A. Grant, J. Tang, E. Vinogradov, X. Wang, R. Lenkinski, and V.P. Sukhatme On-target inhibition of tumor fermentative glycolysis as visualized by hyperpolarized pyruvate Neoplasia 13 2011 60 71
328. S. Hu, A. Balakrishnan, R.A. Bok, B. Anderton, P.E.Z. Larson, S.J. Nelson, J. Kurhanewicz, D.B. Vigneron, and A. Goga (13)C-pyruvate imaging reveals alterations in glycolysis that precede c-Myc-induced tumor formation and regression Cell Metab. 14 2011 131 142
329. J.A.M. Bastiaansen, H.A.I. Yoshihara, Y. Takado, R. Gruetter, and A. Comment Hyperpolarized C-13 lactate as a substrate for in vivo metabolic studies in skeletal muscle Metabolomics 10 2014 986 994
330. M.A. Schroeder, H.J. Atherton, D.R. Ball, M.A. Cole, L.C. Heather, J.L. Griffin, K. Clarke, G.K. Radda, and D.J. Tyler Real-time assessment of Krebs cycle metabolism using hyperpolarized C-13 magnetic resonance spectroscopy Faseb J. 23 2009 2529 2538
331. M.A. Schroeder, H.J. Atherton, L.C. Heather, J.L. Griffin, K. Clarke, G.K. Radda, and D.J. Tyler Determining the in vivo regulation of cardiac pyruvate dehydrogenase based on label flux from hyperpolarised 1-C-13 pyruvate NMR Biomed. 24 2011 980 987
332. S. Jitrapakdee, M. St Maurice, I. Rayment, W.W. Cleland, J.C. Wallace, and P.V. Attwood Structure, mechanism and regulation of pyruvate carboxylase Biochem. J. 413 2008 369 387
333. P. Dzien, M.I. Kettunen, I. Marco-Rius, E.M. Serrao, T.B. Rodrigues, T.J. Larkin, K.N. Timm, and K.M. Brindle C-13 magnetic resonance spectroscopic imaging of hyperpolarized 1-C-13, U-H-2(5) ethanol oxidation can be used to assess aldehyde dehydrogenase activity in vivo Magn. Reson. Med. 73 2015 1733 1740
334. 13C hyperpolarized magnetic resonance using dynamic nuclear polarization Chem. Soc. Rev. 43 2014 1627 1659
335. S. Meier, P.R. Jensen, M. Karlsson, and M.H. Lerche Hyperpolarized NMR probes for biological assays Sensors 14 2014 1576 1597
336. T. Harris, H. Degani, and L. Frydman Hyperpolarized C-13 NMR studies of glucose metabolism in living breast cancer cell cultures NMR Biomed. 26 2013 1831 1843
337. K.X. Moreno, S. Satapati, R.J. DeBerardinis, S.C. Burgess, C.R. Malloy, and M.E. Merritt Real-time detection of hepatic gluconeogenic and glycogenolytic states using hyperpolarized 2-C-13 dihydroxyacetone J. Biol. Chem. 289 2014 35859 35867
338. 13C]glucose reports on glycolytic and pentose phosphate pathway activity in EL4 tumors and glycolytic activity in yeast cells Magn. Reson. Med. 2014
339. F.A. Gallagher, M.I. Kettunen, S.E. Day, M. Lerche, and K.M. Brindle C-13 MR spectroscopy measurements of glutaminase activity in human hepatocellular carcinoma cells using hyperpolarized C-13-labeled glutamine Magn. Reson. Med. 60 2008 253 257
340. E. Ochoa-Ruiz, and R. Diaz-Ruiz Anaplerosis in cancer: another step beyond the warburg effect Am. J. Mol. Biol. 2 2012 291 303
341. S. Mazurek, and E. Eigenbrodt The tumor metabolome Anticancer Res. 23 2003 1149 1154
342. 13C ketoisocaproate Int. J. Cancer 127 2010 729 736
343. C. von Morze, R.A. Bok, G.D. Reed, J.H. Ardenkjaer-Larsen, J. Kurhanewicz, and D.B. Vigneron Simultaneous multiagent hyperpolarized (13)C perfusion imaging Magn. Reson. Med. 72 2014 1599 1609
344. 13C magnetic resonance study Circ. Cardiovasc. Imaging 5 2012 201 209
345. O.J. Rider, and D.J. Tyler Clinical implications of cardiac hyperpolarized magnetic resonance imaging J. Cardiovasc. Magn. Reson. 15 2013 93
346. A.N. Lane, T.W. Fan, and R.M. Higashi Isotopomer-based metabolomic analysis by NMR and mass spectrometry Methods Cell Biol. 84 2008 541 588
347. K. Schmidt, M. Carlsen, J. Nielsen, and J. Villadsen Modeling isotopomer distributions in biochemical networks using isotopomer mapping matrices Biotechnol. Bioeng. 55 1997 831 840
348. C. Wittmann, and E. Heinzle Modeling and experimental design for metabolic flux analysis of lysine-producing Corynebacteria by mass spectrometry Metab. Eng. 3 2001 173 191
349. C. Zupke, and G. Stephanopoulos Modeling of isotope distributions and intracellular fluxes in metabolic networks using atom mapping matrices Biotechnol. Prog. 10 1994 489 498
350. J. Yuan, B.D. Bennett, and J.D. Rabinowitz Kinetic flux profiling for quantitation of cellular metabolic fluxes Nat. Protoc. 3 2008 1328 1340
351. V. Selivanov, P. Vizan, F. Mollinedo, T. Fan, P. Lee, and M. Cascante Edelfosine-induced metabolic changes in cancer cells that precede the overproduction of reactive oxygen species and apoptosis BMC Syst. Biol. 4 2010 135
352. G.F. Mason, and D.L. Rothman Basic principles of metabolic modeling of NMR (13)C isotopic turnover to determine rates of brain metabolism in vivo Metab. Eng. 6 2004 75 84
353. S. Noack, K. Noh, M. Moch, M. Oldiges, and W. Wiechert Stationary versus non-stationary (13)C-MFA: a comparison using a consistent dataset J. Biotechnol. 154 2011 179 190
354. 13C metabolic flux analysis in complex systems Curr. Opin. Biotechnol. 22 2011 103 108
355. N. Jamshidi, J.S. Edwards, T. Fahland, G.M. Church, and B.O. Palsson Dynamic simulation of the human red blood cell metabolic network Bioinformatics 17 2001 286 287
356. 13C fluxomics Curr. Opin. Biotechnol. 34 2015 82 90
357. D.W. Schryer, P. Peterson, T. Paalme, and M. Vendelin Bidirectionality and compartmentation of metabolic fluxes are revealed in the dynamics of isotopomer networks Int. J. Mol. Sci. 10 2009 1697 1718
358. A.D. Maher, P.W. Kuchel, F. Ortega, P. de Atauri, J. Centelles, and M. Cascante Mathematical modelling of the urea cycle - a numerical investigation into substrate channelling Eur. J. Biochem. 270 2003 3953 3961
359. Z. Luo, A.K. Saha, X. Xiang, and N.B. Ruderman AMPK, the metabolic syndrome and cancer Trends Pharmacol. Sci. 26 2005 69 76
360. J.H. Ardenkjaer-Larsen, G.S. Boebinger, A. Comment, S. Duckett, A.S. Edison, F. Engelke, C. Griesinger, R.G. Griffin, C. Hilty, H. Maeda, G. Parigi, T. Prisner, E. Ravera, J. van Bentum, S. Vega, A. Webb, C. Luchinat, H. Schwalbe, and L. Frydman Facing and overcoming sensitivity challenges in biomolecular NMR spectroscopy Angew. Chem. - Int. Ed. 54 2015 9162 9185
361. A. Bhattacharya Chemistry: breaking the billion-hertz barrier Nature 463 2010 605 606
362. J. Bascunan, S. Hahn, D.K. Park, and Y. Iwasa A 1.3-GHz LTS/HTS NMR magnet- a progress report IEEE Trans. Appl. Supercond. 21 2011 2092 2095
363. W.W. Brey, A.S. Edison, R.E. Nast, J.R. Rocca, S. Saha, and R.S. Withers Design, construction, and validation of a 1-mm triple-resonance high-temperature-superconducting probe for NMR J. Magn. Reson. 179 2006 290 293
364. M. Takeda, K. Hallenga, M. Shigezane, M. Waelchli, F. Loehr, J.L. Markley, and M. Kainosho Construction and performance of an NMR tube with a sample cavity formed within magnetic susceptibility-matched glass J. Magn. Reson. 209 2011 167 173
365. M. Mobli, M.W. Maciejewski, M.R. Gryk, and J.C. Hoch Automatic maximum entropy spectral reconstruction in NMR J. Biomol. NMR 39 2007 133 139
366. E. Kupče, and R. Freeman Fast multi-dimensional Hadamard spectroscopy J. Magn. Reson. 163 2003 56 63
367. R. Freeman, and E. Kupče New ways to record multidimensional NMR spectra Curr. Anal. Chem. 2 2006 101 105
368. E. Kupče NMR with multiple receivers Top. Curr. Chem. 335 2013 71 96
369. S.M. Pudakalakatti, A. Dubey, G. Jaipuria, U. Shubhashree, S.K. Adiga, D. Moskau, and H.S. Atreya A fast NMR method for resonance assignments: application to metabolomics J. Biomol. NMR 58 2014 165 173
370. B. Shapira, K. Shetty, W.W. Brey, Z. Gan, and L. Frydman Single-scan 2D NMR spectroscopy on a 25 T bitter magnet Chem. Phys. Lett. 442 2007 478 482
371. P. Giraudeau, and L. Frydman Ultrafast 2D NMR: an emerging tool in analytical spectroscopy Annu. Rev. Anal. Chem. 7 2014 129 161
372. P. Giraudeau, and E. Baguet Improvement of the inverse-gated-decoupling sequence for a faster quantitative analysis of various samples by C-13 NMR spectroscopy J. Magn. Reson. 180 2006 110 117
373. L. Rouger, B. Charrier, M. Pathan, S. Akoka, and P. Giraudeau Processing strategies to obtain clean interleaved ultrafast 2D NMR spectra J. Magn. Reson. 238 2014 87 93
374. A. Le Guennec, P. Giraudeau, and S. Caldarelli Evaluation of fast 2D NMR for metabolomics Anal. Chem. 86 2014 5946 5954
375. M. Foroozandeh, P. Giraudeau, and D. Jeannerat A toolbox of HSQC experiments for small molecules at high C-13-enrichment. Artifact-free, fully C-13-homodecoupled and J(CC)-encoding pulse sequences Magn. Reson. Chem. 51 2013 808 814
376. R. Boisseau, B. Charrier, S. Massou, J.-C. Portais, S. Akoka, and P. Giraudeau Fast spatially encoded 3D NMR strategies for C-13-based metabolic flux analysis Anal. Chem. 85 2013 9751 9757
377. S. Akoka, and P. Giraudeau Fast hybrid multi-dimensional NMR methods based on ultrafast 2D NMR Magn. Reson. Chem. 2015 10.1002/mrc.4237
378. P. Schanda, E. Kupče, and B. Brutscher SOFAST-HMQC experiments for recording two-dimensional heteronuclear correlation spectra of proteins within a few seconds J. Biomol. NMR 33 2005 199 211
379. E. Kupče, and R. Freeman Fast multidimensional NMR by polarization sharing Magn. Reson. Chem. 45 2007 2 4
380. F.X. Theillet, A. Binolfi, S. Liokatis, S. Verzini, and P. Selenko Paramagnetic relaxation enhancement to improve sensitivity of fast NMR methods: application to intrinsically disordered proteins J. Biomol. NMR 51 2011 487 495
381. 13C dynamic nuclear polarization with a radical mixture J. Am. Chem. Soc. 135 2013 2935 2938
382. G.D. Reed, P.E.Z. Larson, C. von Morze, R. Bok, M. Lustig, A.B. Kerr, J.M. Pauly, J. Kurhanewicz, and D.B. Vigneron A method for simultaneous echo planar imaging of hyperpolarized C-13 pyruvate and C-13 lactate J. Magn. Reson. 217 2012 41 47
383. S.J. Nelson, J. Kurhanewicz, D.B. Vigneron, P.E.Z. Larson, A.L. Harzstark, M. Ferrone, M. van Criekinge, J.W. Chang, R. Bok, I. Park, G. Reed, L. Carvajal, E.J. Small, P. Munster, V.K. Weinberg, J.H. Ardenkjaer-Larsen, A.P. Chen, R.E. Hurd, L.-I. Odegardstuen, F.J. Robb, J. Tropp, and J.A. Murray Metabolic imaging of patients with prostate cancer using hyperpolarized 1-C-13 pyruvate Sci. Transl. Med. 5 2013
384. T.W. Fan Considerations of sample preparation for metabolomics investigation T.W. Fan, A.N. Lane, R.M. Hiagshi, Handbook of Metabolomics 2012 Humana Totoya
385. A. Wollenberger, O. Ristau, and G. Schoffa A simple technique for extremely rapid freezing of large pieces of tissue Pfiugers Arch. Ges. Physiol. 270 1960 399 412
386. T.W.M. Fan, R.M. Higashi, and A.N. Lane Integrating metabolomics and transcriptomics for probing Se anticancer mechanisms Drug Metab. Rev. 38 2006 707 732