Hyperpolarized 13C spectroscopy and an NMR-compatible bioreactor system for the investigation of real-time cellular metabolism

Magnetic Resonance in Medicine

Volumn 63, Issue 2, 2010, Pages 322-329

  Keshari, Kayvan R ^a,b   Kurhanewicz, John ^a   Jeffries, Rex E ^b   Wilson, David M ^a   Dewar, Brian J ^b   Van Criekinge, Mark ^a   Zierhut, Matthew ^a   Vigneron, Daniel B ^a   Macdonald, Jeffrey M ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

Bioreactor; Carbon; DNP; Flux; Hyperpolarized; Metabolism

Indexed keywords

AMINO ACIDS; BIOCONVERSION; CARBON; CELLS; CYTOLOGY; FLUIDIZATION; FLUXES; METABOLISM; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY;

13C NMR SPECTROSCOPY; ALANINE AMINOTRANSFERASE; CELLULAR METABOLISM; CORRELATION SPECTROSCOPY; HYPERPOLARIZED; HYPERPOLARIZED [1; IMMORTALIZED CELLS; LACTATE DEHYDROGENASE;

BIOREACTORS;

1 PYRUVATE C 13; ALANINE; ALANINE AMINOTRANSFERASE; CARBON 13; CELL EXTRACT; GLUCOSE C 13; LACTATE DEHYDROGENASE; LACTIC ACID; PYRUVIC ACID; RADIOISOTOPE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL MODEL; ARTICLE; BIOREACTOR; CARBON NUCLEAR MAGNETIC RESONANCE; CELL CULTURE; CELL IMMORTALIZATION; CELL METABOLISM; CONTROLLED STUDY; CORRELATIONAL STUDY; GLYCOLYSIS; HEPATOMA CELL; HUMAN; HUMAN CELL; INJECTION; MALE; NONHUMAN; PHOSPHORUS NUCLEAR MAGNETIC RESONANCE; PROTON NUCLEAR MAGNETIC RESONANCE; RAT; TECHNOLOGY;

EID: 75749154392     PISSN: 07403194     EISSN: 15222594     Source Type: Journal    
DOI: 10.1002/mrm.22225     Document Type: Article

References (52)

1. Christofk H, Vander Heiden M, Harris M, Ramanathan A, Gerszten R, Wei R, Fleming M, Schreiber S, Cantley L. The M2 splice isoform of pyruvate kinase is important for cancer metabolism and tumour growth. Nature 2008;452:230-233.
2. DeBerardinis RJ, Lum JJ, Hatzivassiliou G, Thompson CB. The biology of cancer: metabolic reprogramming fuels cell growth and proliferation. Cell Metab 2008;7:11-20.
3. Fan TW, Kucia M, Jankowski K, Higashi RM, Ratajczak J, Ratajczak MZ, Lane AN. Rhabdomyosarcoma cells show an energy producing anabolic metabolic phenotype compared with primary myocytes. Mol Cancer 2008;7:79.
4. Gatenby RA, Gillies RJ. Glycolysis in cancer: a potential target for therapy. Int J Biochem Cell Biol 2007.
5. Hsu PP, Sabatini DM. Cancer cell metabolism: Warburg and beyond. Cell 2008;134:703-707.
6. Munger J, Bennett B, Parikh A, Feng X, Mcardle J, Rabitz H, Shenk T, Rabinowitz J. Systems-level metabolic flux profiling identifies fatty acid synthesis as a target for antiviral therapy. Nat Biotechnol 2008;26:1179-1186.
7. Tessem M, Swanson MG, Keshari KR, Albers MJ, Joun D, Tabatabai ZL, Simko J, Shinohara K, Nelson SJ, Vigneron DB, Gribbestad IS, Kurhanewicz J. Evaluation of lactate and alanine as metabolic biomarkers of prostate cancer using 1H HR-MAS spectroscopy of biopsy tissues. Magn Reson Med 2008;60:510-516.
8. Albers MJ, Bok R, Chen AP, Cunningham CH, Zierhut ML, Zhang VY, Kohler SJ, Tropp J, Hurd RE, Yen YF, Nelson SJ, Vigneron DB, Kurhanewicz J. Hyperpolarized 13C lactate, pyruvate, and alanine: noninvasive biomarkers for prostate cancer detection and grading. Cancer Res 2008;68:8607-8615.
9. Day SE, Kettunen MI, Gallagher FA, Hu DE, Lerche M, Wolber J, Golman K, Ardenkjaer-Larsen JH, Brindle KM. Detecting tumor response to treatment using hyperpolarized 13C magnetic resonance imaging and spectroscopy. Nat Med 2007;13:1382-1387.
10. Ackerstaff E, Glunde K, Bhujwalla ZM. Choline phospholipid metabolism: a target in cancer cells?J Cell Biochem 2003;90: 525-533.
11. Iorio E, Mezzanzanica D, Alberti P, Spadaro F, Ramoni C, D'Ascenzo S, Millimaggi D, Pavan A, Dolo V, Canevari S, Podo F. Alterations of choline phospholipid metabolism in ovarian tumor progression. Cancer Res 2005;65:9369-9376.
12. Bonarius HP, Ozemre A, Timmerarends B, Skrabal P, Tramper J, Schmid G, Heinzle E. Metabolic-flux analysis of continuously cultured hybridoma cells using (13)CO(2) mass spectrometry in combination with (13)C-lactate nuclear magnetic resonance spectroscopy and metabolite balancing. Biotechnol Bioeng 2001;74:528-538.
13. 31P magnetic resonance spectroscopy and high pressure liquid chromatography. NMR Biomed 1992;5:185-192.
14. Thelwall PE, Yemin AY, Gillian TL, Simpson NE, Kasibhatla MS, Rabbani ZN, Macdonald JM, Blackband SJ, Gamcsik MP. Noninvasive in vivo detection of glutathione metabolism in tumors. Cancer Res 2005;65:10149-10153.
15. Gillies RJ, Liu Z, Bhujwalla ZM. 31P-MRS measurements of extracellular pH of tumors using 3-aminopropylphosphonate. Am J Physiol 1994;267(1 pt 1):C195-203.
16. 13C NMR. Magn Reson Med 2002;48:430-439.
17. 13C NMR measurements of hepatocellular tricarboxylic acid cycle flux. J Biol Chem 1998;273: 12187-12194.
18. van Zijl PC, Jones CK, Ren J, Malloy CR, Sherry AD. MRI detection of glycogen in vivo by using chemical exchange saturation transfer imaging (glycoCEST). Proc Natl Acad Sci USA 2007;104: 4359-4364.
19. Mancuso A, Fernandez EJ, Blanch HW, Clark DS. A nuclear magnetic resonance technique for determining hybridoma cell concentration in hollow fiber bioreactors. Biotechnology (NY) 1990;8:1282-1285.
20. Wolfe SP, Hsu E, Reid LM, Macdonald JM. A novel multi-coaxial hollow fiber bioreactor for adherent cell types, part 1: hydrodynamic studies. Biotechnol Bioeng 2002;77:83-90.
21. 13C NMR spectroscopic changes during chemotherapy-induced apoptosis in human glioma cells. Magn Reson Med 2005;54:67-78.
22. 31P-NMR spectroscopic evaluation of immobilized perfused rat Sertoli cells. J Lab Clin Med 1996;128:408-416.
23. Bailey JE, Ollis DF. Biochemical engineering fundamentals. New York: McGraw-Hill; 1986, 928 pp.
24. Beloueche-Babari M, Jackson LE, Al-Saffar NM, Eccles SA, Raynaud FI, Workman P, Leach MO, Ronen SM. Identification of magnetic resonance detectable metabolic changes associated with inhibition of phosphoinositide 3-kinase signaling in human breast cancer cells. Mol Cancer Ther 2006;5:187-196.
25. Gamcsik MP, Millis KK, Colvin OM. Noninvasive detection of elevated glutathione levels in MCF-7 cells resistant to 4-hydroperoxycyclophosphamide. Cancer Res 1995;55:2012-2016.
26. DeBerardinis RJ, Mancuso A, Daikhin E, Nissim I, Yudkoff M, Wehrli S, Thompson CB. Beyond aerobic glycolysis: transformed cells can engage in glutamine metabolism that exceeds the requirement for protein and nucleotide synthesis. Proc Natl Acad Sci USA 2007;104: 19345-19350.
27. Droste P, Weitzel M, Wiechert W. Visual exploration of isotope labeling networks in 3D. Bioprocess Biosyst Eng 2008;31:227-239.
28. Massou S, Nicolas C, Letisse F, Portais JC. NMR-based fluxomics: quantitative 2D NMR methods for isotopomers analysis. Phytochemistry 2007;68:2330-2340.
29. Chowdhury SK, Gemin A, Singh G. High activity of mitochondrial glycerophosphate dehydrogenase and glycerophosphate-dependent ROS production in prostate cancer cell lines. Biochem Biophys Res Commun 2005;333:1139-1145.
30. 13C MR spectroscopic imaging of regionally specific metabolic alterations after experimental stroke. Brain 2008;131(pt 8):2209-2219.
31. 13C2]glucose reveals a heterogeneous metabolism in human leukemia T cells. Biochimie 2006;88:437-448.
32. 13C NMR isotopomer analysis of human urine. Anal Biochem 2003;312:228-234.
33. Stephanopoulos G, Gill RT. Metabolic engineering.Nielsen J, editor. Heidelberg: Springer Berlin; 2001.
34. 1H TOCSY. Metabolomics 2007;3:79-86.
35. Ardenkjaer-Larsen JH, Fridlund B, Gram A, Hansson G, Hansson L, Lerche MH, Servin R, Thaning M, Golman K. Increase in signal-tonoise ratio of > 10,000 times in liquid-state NMR. Proc Natl Acad Sci USA 2003;100:10158-10163.
36. Chen AP, Albers MJ, Cunningham CH, Kohler SJ, Yen YF, Hurd RE, Tropp J, Bok R, Pauly JM, Nelson SJ, Kurhanewicz J, Vigneron DB. Hyperpolarized C-13 spectroscopic imaging of the TRAMP mouse at 3T-initial experience. Magn Reson Med 2007;58:1099-1106.
37. Warburg O. On the origin of cancer cells. Science 1956;123: 309-314.
38. Macdonald JM, Grillo M, Schmidlin O, Tajiri DT, James TL. NMR spectroscopy and MRI investigation of a potential bioartificial liver. NMR Biomed 1998;11:55-66.
39. Maharjan RP, Ferenci T. Global metabolite analysis: the influence of extraction methodology on metabolome profiles of Escherichia coli. Anal Biochem 2003;313:145-154.
40. Tyagi RK, Azrad A, Degani H, Salomon Y. Simultaneous extraction of cellular lipids and water-soluble metabolites: evaluation by NMR spectroscopy. Magn Reson Med 1996;35:194-200.
41. Chandrasekaran P, Seagle C, Rice L, Macdonald JM, Gerber DA. Functional analysis of encapsulated hepatic progenitor cells. Tissue Eng 2006;12:2001-2008.
42. Gamcsik MP, Forder JR, Millis KK, McGovern KA. A versatile oxygenator and perfusion system for magnetic resonance studies. Biotechnol Bioeng 1996;49:348-354.
43. Swanson MG, Keshari KR, Tabatabai ZL, Simko JP, Shinohara K, Carroll PR, Zektzer AS, Kurhanewicz J. Quantification of choline- and ethanolamine- containing metabolites in human prostate tissues using (1)H HR-MAS total correlation spectroscopy. Magn Reson Med 2008; 60:33-40.
44. Karlsson J, Hulten B, Sjodin B. Substrate activation and product inhibition of LDH activity in human skeletal muscle. Acta Physiol Scand 1974;92:21-26.
45. 13C-1-pyruvate. Magn Reson Med 2007;58:65-69.
46. 1H NMR-based metabolomic analysis of liver, serum, and brain following ethanol administration in rats. Chem Res Toxicol 2008;21:408-420.
47. Gamcsik MP, Dubay GR, Cox BR. Increased rate of glutathione synthesis from cystine in drug-resistant MCF-7 cells. Biochem Pharmacol 2002;63:843-851.
48. Balendiran GK, Dabur R, Fraser D. The role of glutathione in cancer. Cell Biochem Funct 2004;22:343-352.
49. 31P MRS. Magn Reson Med 1993;29: 244-248.
50. 31P NMR visibility of ATP in perfused rat liver remains about 90%, unaffected by changes of metabolic state. Biochemistry 1992;31:7488-7493.
51. 31P NMR of mammalian cells encapsulated in alginate gels utilizing a new phosphate-free perfusion medium. NMR Biomed 1990;3:23-26.
52. Gross JD, Constantinidis I, Sambanis A. Modeling of encapsulated cell systems. J Theor Biol 2007;244:500-510.