Real-time NMR monitoring of biological activities in complex physiological environments

Current Opinion in Structural Biology

Volumn 32, Issue , 2015, Pages 39-47

  Smith, Matthew J ^a   Marshall, Christopher B ^a   Theillet, Francois Xavier ^b   Binolfi, Andres ^b   Selenko, Philipp ^b   Ikura, Mitsuhiko ^a,c  

^a Ontario Cancer Institute   (Canada)

^b LEIBNIZ INSTITUT FÜR MOLEKULARE PHARMAKOLOGIE   (Germany)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

GUANOSINE TRIPHOSPHATASE; PROLINE; PROTEIN;

BIOLOGICAL ACTIVITY; BIOLOGICAL MONITORING; CELL METABOLISM; CONFORMATIONAL TRANSITION; ENZYME ACTIVITY; ENZYME REGULATION; HUMAN; ISOMERIZATION; ISOTOPE LABELING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; QUANTITATIVE ANALYSIS; REAL TIME NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; REVIEW; ANIMAL; BIOCATALYSIS; CHEMISTRY; DEVICES; EQUIPMENT DESIGN; METABOLISM; NUCLEAR MAGNETIC RESONANCE; PROCEDURES;

ANIMALS; BIOCATALYSIS; EQUIPMENT DESIGN; GTP PHOSPHOHYDROLASES; HUMANS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEINS;

EID: 84923559957     PISSN: 0959440X     EISSN: 1879033X     Source Type: Journal    
DOI: 10.1016/j.sbi.2015.02.003     Document Type: Review

References (50)

1. Purvis J.E., Lahav G. Encoding and decoding cellular information through signaling dynamics. Cell 2013, 152:945-956.
2. Eicher J.J., Snoep J.L., Rohwer J.M. Determining enzyme kinetics for systems biology with nuclear magnetic resonance spectroscopy. Metabolites 2012, 2:818-843.
3. Hall H., Cuellar-Baena S., Denisov V., Kirik D. Development of NMR spectroscopic methods for dynamic detection of acetylcholine synthesis by choline acetyltransferase in hippocampal tissue. J Neurochem 2013, 124:336-346.
4. Lerche M.H., Jensen P.R., Karlsson M., Meier S. NMR insights into the inner workings of living cells. Anal Chem 2015, 87:119-132. 10.1021/ac501467x.
5. 13C NMR studies of glucose metabolism in living breast cancer cell cultures. NMR Biomed 2013, 26:1831-1843.
6. Chaumeil M.M., Larson P.E., Yoshihara H.A., Danforth O.M., Vigneron D.B., Nelson S.J., Pieper R.O., Phillips J.J., Ronen S.M. Non-invasive in vivo assessment of IDH1 mutational status in glioma. Nat Commun 2013, 4:2429.
7. Venkatesh H.S., Chaumeil M.M., Ward C.S., Haas-Kogan D.A., James C.D., Ronen S.M. Reduced phosphocholine and hyperpolarized lactate provide magnetic resonance biomarkers of PI3K/Akt/mTOR inhibition in glioblastoma. Neuro Oncol 2012, 14:315-325.
8. Lodi A., Woods S.M., Ronen S.M. Treatment with the MEK inhibitor U0126 induces decreased hyperpolarized pyruvate to lactate conversion in breast, but not prostate, cancer cells. NMR Biomed 2013, 26:299-306.
9. 1H NMR spectroscopy profiling of metabolic reprogramming of Chinese hamster ovary cells upon a temperature shift during culture. PLoS ONE 2013, 8:e77195. 10.1371/journal.pone.0077195.
10. Xue J., Isern N.G., Ewing R.J., Liyu A.V., Sears J.A., Knapp H., Iversen J., Sisk D.R., Ahring B.K., Majors P.D. New generation NMR bioreactor coupled with high-resolution NMR spectroscopy leads to novel discoveries in Moorella thermoacetica metabolic profiles. Appl Microbiol Biotechnol 2014, 98:8367-8375.
11. Jensen P.R., Karlsson M., Lerche M.H., Meier S. Real-time DNP NMR observations of acetic acid uptake, intracellular acidification, and of consequences for glycolysis and alcoholic fermentation in yeast. Chemistry 2013, 19:13288-13293.
12. Theillet F.X., Smet-Nocca C., Liokatis S., Thongwichian R., Kosten J., Yoon M.K., Kriwacki R.W., Landrieu I., Lippens G., Selenko P. Cell signaling, post-translational protein modifications and NMR spectroscopy. J Biomol NMR 2012, 54:217-236.
13. Theillet F.-X., Rose H.M., Liokatis S., Binolfi A., Thongwichian R., Stuiver M., Selenko P. Site-specific NMR mapping and time-resolved monitoring of serine and threonine phosphorylation in reconstituted kinase reactions and mammalian cell extracts. Nat Protoc 2013, 8:1416-1432.
14. Liokatis S., Stützer A., Elsässer S.J., Theillet F.-X., Klingberg R., van Rossum B., Schwarzer D., Allis C.D., Fischle W., Selenko P. Phosphorylation of histone H3 Ser10 establishes a hierarchy for subsequent intramolecular modification events. Nat Struct Mol Biol 2012, 19:819-823.
15. Rose H.M., Stuiver M., Thongwichian R., Theillet F.-X., Feller S.M., Selenko P. Quantitative NMR analysis of Erk activity and inhibition by U0126 in a panel of patient-derived colorectal cancer cell lines. BBA Protein Proteom 2013, 1834:1396-1401.
16. Cordier F., Chaffotte A., Terrien E., Préhaud C., Theillet O.-X., Delepierre M., Lafon M., Buc H., Wolf N. Ordered phosphorylation events in two independent cascades of the PTEN C-tail revealed by NMR. J Am Chem Soc 2012, 134:20533-20543.
17. Kosten J., Binolfi A., Stuiver M., Verzini S., Theillet F.X., Bekei B., van Rossum M., Selenko P. Efficient modification of alpha-synuclein serine 129 by protein kinase CK1 requires phosphorylation of tyrosine 125 as a priming event. ACS Chem Neurosci 2014, 5:1203-1208. 10.1021/cn5002254.
18. Borcherds W., Theillet F.X., Katzer A., Finzel A., Mishall K.M., Powell A.T., Wu H., Manieri W., Dieterich C., Selenko P., et al. Disorder and residual helicity alter p53-Mdm2 binding affinity and signaling in cells. Nat Chem Biol 2014, 10:1000-1002.
19. Amata I., Maffei M., Igea A., Gay M., Vilaseca M., Nebreda A.R., Pons M. Multi-phosphorylation of the intrinsically disordered unique domain of c-Src studied by in-cell and real-time NMR spectroscopy. ChemBioChem 2013, 14:1820-1827.
20. Selenko P., Frueh D.P., Elsaesser S.J., Haas W., Gygi S.P., Wagner G. In situ observation of protein phosphorylation by high-resolution NMR spectroscopy. Nat Struct Mol Biol 2008, 15:321-329.
21. Mayzel M., Rosenlöw J., Isaksson L., Orekhov V.Y. Time-resolved multidimensional NMR with non-uniform sampling. J Biomol NMR 2014, 58:129-139.
22. Liokatis S., Dose A., Schwarzer D., Selenko P. Simultaneous detection of protein phosphorylation and acetylation by high-resolution NMR spectroscopy. J Am Chem Soc 2010, 132:14704-14705.
23. Theillet F.-X., Liokatis S., Jost J.O., Bekei B., Rose H.M., Binolfi A., Schwarzer D., Selenko P. Site-specific mapping and time-resolved monitoring of lysine methylation by high-resolution NMR spectroscopy. J Am Chem Soc 2012, 134:7616-7619.
24. Maltsev A.S., Chen J., Levine R.L., Bax A. Site-specific interaction between α-synuclein and membranes probed by NMR-observed methionine oxidation rates. J Am Chem Soc 2013, 135:2943-2946.
25. Miotto M.C., Rodriguez E.E., Valiente-gabioud A.A., Torres-monserrat V., Quintanar L., Zweckstetter M., Griesinger C., Ferna C.O. Site-specific copper-catalyzed oxidation of α-synuclein: tightening the link between metal binding and protein oxidative damage in Parkinson's disease. Inorg Chem 2014, 53:4350-4358.
26. Marshall C.B., Ho J., Buerger C., Plevin M.J., Li G.-Y., Li Z., Ikura M., Stambolic V. Characterization of the intrinsic and TSC2-GAP-regulated GTPase activity of Rheb by real-time NMR. Sci Signal 2009, 2:ra3. 10.1126/scisignal.2000029.
27. Gasmi-Seabrook G.M.C., Marshall C.B., Cheung M., Kim B., Wang F., Jang Y.J., Mak T.W., Stambolic V., Ikura M. Real-time NMR study of guanine nucleotide exchange and activation of RhoA by PDZ-RhoGEF. J Biol Chem 2010, 285:5137-5145.
28. Buosi V., Placial J.-P., Leroy J.-L., Cherfils J., Guittet É., van Heijenoort C. Insight into the role of dynamics in the conformational switch of the small GTP-binding protein Arf1. J Biol Chem 2010, 285:37987-37994.
29. Hellmich U.a., Haase W., Velamakanni S., van Veen H.W., Glaubitz C. Caught in the act: ATP hydrolysis of an ABC-multidrug transporter followed by real-time magic angle spinning NMR. FEBS Lett 2008, 582:3557-3562.
30. Smith M.J., Neel B.G., Ikura M. NMR-based functional profiling of RASopathies and oncogenic RAS mutations. Proc Natl Acad Sci USA 2013, 110.
31. Smith M.J., Ikura M. Integrated RAS signaling defined by parallel NMR detection of effectors and regulators. Nat Chem Biol 2014, 10:223-230.
32. Findlay G.M., Smith M.J., Lanner F., Hsiung M.S., Gish G.D., Petsalaki E., Cockburn K., Kaneko T., Huang H., Bagshaw R.D., et al. Interaction domains of Sos1/Grb2 are finely tuned for cooperative control of embryonic stem cell fate. Cell 2013, 152:1008-1020.
33. Organ S.L., Hai J., Radulovich N., Marshall C.B., Leung L., Sasazuki T., Shirasawa S., Zhu C.-Q., Navab R., Ikura M., et al. p120RasGAP is a mediator of Rho pathway activation and tumorigenicity in the DLD1 colorectal cancer cell line. PLoS ONE 2014, 9:e86103. 10.1371/journal.pone.0086103.
34. Meiri D., Marshall C.B., Greeve Ma, Kim B., Balan M., Suarez F., Bakal C., Wu C., Larose J., Fine N., et al. Mechanistic insight into the microtubule and actin cytoskeleton coupling through dynein-dependent RhoGEF inhibition. Mol Cell 2012, 45:642-655.
35. Meiri D., Marshall C.B., Mokady D., LaRose J., Mullin M., Gingras A.-C., Ikura M., Rottapel R. Mechanistic insight into GPCR-mediated activation of the microtubule-associated RhoA exchange factor GEF-H1. Nat Commun 2014, 5:4857. 10.1038/ncomms5857.
36. Denisov I.G., Grinkova Y.V., Lazarides A.A., Sligar S.G. Directed self-assembly of monodisperse phospholipid bilayer Nanodiscs with controlled size. J Am Chem Soc 2004, 126:3477-3487.
37. Mazhab-Jafari M.T., Marshall C.B., Stathopulos P.B., Kobashigawa Y., Stambolic V., Kay L.E., Inagaki F., Ikura M. Membrane-dependent modulation of the mTOR activator Rheb: NMR observations of a GTPase tethered to a lipid-bilayer nanodisc. J Am Chem Soc 2013, 135:3367-3370.
38. Hoffmann-Thoms S., Weininger U., Eckert B., Jakob R.P., Koch J.R., Balbach J., Schmid F.X. Initiation of phage infection by partial unfolding and prolyl isomerization. J Biol Chem 2013, 288:12979-12991.
39. Kumar A., Balbach J. Real-time protein NMR spectroscopy and investigation of assisted protein folding. Biochim Biophys Acta 2014, 9:1242-1250.
40. Rennella E., Brutscher B. Fast real-time NMR methods for characterizing short-lived molecular states. ChemPhysChem 2013, 14:3059-3070.
41. Marsh E.N.G., Suzuki Y. Using F-19 NMR to probe biological interactions of proteins and peptides. ACS Chem Biol 2014, 9:1242-1250.
42. Shekhawat S.S., Pham G.H., Prabakaran J., Strieter E.R. Simultaneous detection of distinct ubiquitin chain topologies by 19F NMR. ACS Chem Biol 2014, 9:2229-2236.
43. Li H.L., Frieden C. Observation of sequential steps in the folding of intestinal fatty acid binding protein using a slow folding mutant and F-19 NMR. Proc Natl Acad Sci USA 2007, 104:11993-11998.
44. Suzuki Y., Brender J.R., Hartman K., Ramamoorthy A., Marsh E.N.G. Alternative pathways of human islet amyloid polypeptide aggregation distinguished by F-19 nuclear magnetic resonance-detected kinetics of monomer consumption. Biochemistry 2012, 51:8154-8162.
45. Suzuki Y., Brender J.R., Soper M.T., Krishnamoorthy J., Zhou Y.L., Ruotolo B.T., Kotov N.A., Ramamoorthy A., Marsh E.N.G. Resolution of oligomeric species during the aggregation of A beta(1-40) using F-19 NMR. Biochemistry 2013, 52:1903-1912.
46. Schlepckow K., Schwalbe H. Molecular mechanism of prion protein oligomerization at atomic resolution. Angew Chem (International ed. in English) 2013, 52:10002-10005.
47. Binolfi A., Rodriguez E.E., Valensin D., D'Amelio N., Ippoliti E., Obal G., Duran R., Magistrato A., Pritsch O., Zweckstetter M., et al. Bioinorganic chemistry of Parkinson's disease: structural determinants for the copper-mediated amyloid formation of alpha-synuclein. Inorg Chem 2010, 49:10668-10679.
48. Inomata K., Ohno A., Tochio H., Isogai S., Tenno T., Nakase I., Takeuchi T., Futaki S., Ito Y., Hiroaki H., et al. High-resolution multi-dimensional NMR spectroscopy of proteins in human cells. Nature 2009, 458:106-109.
49. Hamatsu J., O'Donovan D., Tanaka T., Shirai T., Hourai Y., Mikawa T., Ikeya T., Mishima M., Boucher W., Smith B.O., et al. High-resolution heteronuclear multidimensional NMR of proteins in living insect cells using a baculovirus protein expression system. J Am Chem Soc 2013, 135:1688-1691.
50. Banci L., Barbieri L., Bertini I., Luchinat E., Secci E., Zhao Y., Aricescu aR. Atomic-resolution monitoring of protein maturation in live human cells by NMR. Nat Chem Biol 2013, 9:297-299.