Recent applications of isotopic labeling for protein NMR in drug discovery

Expert Opinion on Drug Discovery

Volumn 8, Issue 5, 2013, Pages 523-536

  Hiroaki, Hidekazu ^a  

^a NAGOYA UNIVERSITY   (Japan)

Author keywords

Amino acid type selective labeling; Fragment based approach; In cell NMR; Inverse labeling; Protein based method; SAIL method

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; BACTERIAL PROTEIN; DRUG ANTIBODY; PHOSPHOPROTEIN PHOSPHATASE INHIBITOR; PROTEINASE; TACROLIMUS;

AATS LABELING; AMINO ACID SELECTIVE UNLABELING; BREVIBACILLUS; BREVIBACILLUS CHOSHINENSIS; CARBON NUCLEAR MAGNETIC RESONANCE; CELL FREE SYSTEM; COMBINATORIAL AATS LABELING; COMBINATORIAL CHEMISTRY; DISULFIDE BOND; DRUG DELIVERY SYSTEM; DRUG DEVELOPMENT; FOURIER TRANSFORMATION; GENE EXPRESSION; GENE EXPRESSION SYSTEM; GENETIC ANALYSIS; GROWTH RATE; HETERONUCLEAR SINGLE QUANTUM COHERENCE; INSECT CELL; ISOTOPE LABELING; KLUYVEROMYCES LACTIS; LIGAND BINDING; MAMMAL CELL; METABOLIC FRACTIONAL LABELING; MOIETY SPECIFIC LABELING; MOLECULAR PATHOLOGY; MOLECULAR WEIGHT; NITROGEN NUCLEAR MAGNETIC RESONANCE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OOCYTE; PICHIA PASTORIS; PLANT CELL; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; PROTON NUCLEAR MAGNETIC RESONANCE; REVIEW; SAIL METHOD; SEGMENTAL LABELING; XENOPUS;

ANIMALS; DRUG DISCOVERY; HUMANS; ISOTOPE LABELING; MAGNETIC RESONANCE SPECTROSCOPY; PROTEINS;

EID: 84876779164     PISSN: 17460441     EISSN: 1746045X     Source Type: Journal    
DOI: 10.1517/17460441.2013.779665     Document Type: Review

References (99)

1. Pellecchia M, Sem DS, Wüthrich K. NMR in drug discovery. Nat Rev Drug Discov 2002;1(3):211-19
2. Pellecchia M, Bertini I, Cowburn D, et al. Perspectives on NMR in drug discovery: a technique comes of age. Nat Rev Drug Discov 2008;7(9):738-45
3. Heller M, Kessler H. NMR spectroscopy in drug design. Pure Appl Chem 2001;73(9):1429-36
4. Orita M, Warizaya M, Amano Y, et al. Advances in fragment-based drug discovery platforms. Expert Opin Drug Discov 2009;4(11):1125-44
5. Ni F. Recent developments in transferred noe methods. Prog Nucl Magn Reson Spectrosc 1994;26:517-606
6. Fejzo J, Lepre CA, Peng JW, et al. The SHAPES strategy: an NMR-based approach for lead generation in drug discovery. Chem Biol 1999;6(10):755-69
7. Antalek B. Using pulsed gradient spin echo NMR for chemical mixture analysis: how to obtain optimum results. Concepts Magn Reson 2002;14(4):225-58
8. Chen A, Shapiro MJ. Affinity NMR. Analyt Chem 1999;71(19):669A-75A
9. Bhunia A, Bhattacharjya S, Chatterjee S. Applications of saturation transfer difference NMR in biological systems. Drug Discov Today 2012;17(9-10):505-13
10. Dalvit C, Pevarello P, Tatò M, et al. Identification of compounds with binding affinity to proteins via magnetization transfer from bulk water. J Biomol NMR 2000;18(1):65-8 . A paper describing WATERLOGSY.
11. Becattini B, Culmsee C, Leone M, et al. Structure-activity relationships by interligand NOE-based design and synthesis of antiapoptotic compounds targeting Bid. Proc Nat Acad Sci USA 2006;103:33:12602-6
12. Sánchez-Pedregal VM, Reese M, Meiler J, et al. The INPHARMA Method: protein-Mediated Interligand NOEs for pharmacophore mapping. Angew Chem 2005;117(27):4244-7
13. Shuker SB, Hajduk PJ, Meadows RP, Fesik SW. Discovering high-affinity ligands for proteins: SAR by NMR. Science 1996;274(5292):1531-4
14. Hajduk PJ, Sheppard G, Nettesheim DG, et al. Discovery of Potent Nonpeptide Inhibitors of Stromelysin Using SAR by NMR. J Am Chem Soc 1997;119(25):5818-27
15. Petros AM, Huth JR, Oost T, et al. Discovery of a potent and selective Bcl-2 inhibitor using SAR by NMR. Bioorg Med Chem lett 2010;20(22):6587-91
16. Cai M, Huang Y, Sakaguchi K, et al. An efficient and cost-effective isotope labeling protocol for proteins expressed in Escherichia coli. J Biomol NMR 1998;11(1):97-102
17. Hewitt L, McDonnell JM. Screening and optimizing protein production in E. coli. Methods Mol Biol 2004;278:1-16
18. Studier FW, Rosenberg AH, Dunn JJ, Dubendorff JW. Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol 1990;185:60-89
19. Qing G, Ma L-C, Khorchid A, et al. Cold-shock induced high-yield protein production in Escherichia coli. Nat Biotechnol 2004;22(7):877-82
20. Yashiro K, Lowenthal JW, O'Neil TE, et al. High-level production of recombinant chicken interferon-gamma by Brevibacillus choshinensis. Protein Expr Purif 2001;23(1):113-20
21. Udaka S, Yamagata H. High-level secretion of heterologous proteins by Bacillus brevis. Methods Enzymol 1993;217:23-33
22. Tanio M, Tanaka T, Kohno T. 15N isotope labeling of a protein secreted by Brevibacillus choshinensis for NMR study. Anal Biochem 2008;373(1):164-6
23. Tanio M, Tanaka R, Tanaka T, Kohno T. Amino acid-selective isotope labeling of proteins for nuclear magnetic resonance study: proteins secreted by Brevibacillus choshinensis. Anal Biochem 2009;386(2):156-60
24. Takahashi H, Shimada I. Production of isotopically labeled heterologous proteins in non-E. coli prokaryotic and eukaryotic cells. J Biomol NMR 2010;46(1):3-10
25. Kamiya Y, Yamamoto S, Chiba Y, et al. Overexpression of a homogeneous oligosaccharide with 13C labeling by genetically engineered yeast strain. J Biomol NMR 2011;50(4):397-401
26. Takegawa K, Tohda H, Sasaki M, et al. Production of heterologous proteins using the fission-yeast (Schizosaccharomyces pombe) expression system. Biotechnol Appl Biochem 2009;53(Pt 4):227-35 . An industrial scale expression system using fission yeast.
27. Antuch W, Gu?ntert P, Wu?thrich K. Ancestral beta gamma-crystallin precursor structure in a yeast killer toxin. Nat Struct Biol 1996;3(8):662-5
28. Pickford AR, O'Leary JM. Isotopic labeling of recombinant proteins from the methylotrophic yeast Pichia pastoris. Methods Mol Biol 2004;278:17-33
29. Rodriguez E, Krishna NR. An economical method for (15)N/(13)C isotopic labeling of proteins expressed in Pichia pastoris. J Biochem 2001;130(1):19-22
30. Sugiki T, Shimada I, Takahashi H. Stable isotope labeling of protein by Kluyveromyces lactis for NMR study. J Biomol NMR 2008;42(3):159-62
31. Sugiki T, Ichikawa O, Miyazawa-Onami M, et al. Isotopic labeling of heterologous proteins in the yeast Pichia pastoris and Kluyveromyces lactis. Methods Mol Biol 2012;831:19-36
32. Colussi PA, Taron CH. Kluyveromyces lactis LAC4 promoter variants that lack function in bacteria but retain full function in K. lactis. Appl Environ Microbiol 2005;71(11):7092-8
33. Strauss A, Bitsch F, Cutting B, et al. Amino-acid-type selective isotope labeling of proteins expressed in Baculovirus-infected insect cells useful for NMR studies. J Biomol NMR 2003;26(4):367-72
34. Strauss A, Bitsch F, Fendrich G, et al. Efficient uniform isotope labeling of Abl kinase expressed in Baculovirus-infected insect cells. J Biomol NMR 2005;31(4):343-9
35. Gossert AD, Hinniger A, Gutmann S, et al. A simple protocol for amino acid type selective isotope labeling in insect cells with improved yields and high reproducibility. J Biomol NMR 2011;51(4):449-56
36. Ohki S, Dohi K, Tamai A, et al. Stable-isotope labeling using an inducible viral infection system in suspension-cultured plant cells. J Biomol NMR 2008;42(4):271-7
37. Kato K, Yamaguchi Y, Arata Y. Stable-isotope-assisted NMR approaches to glycoproteins using immunoglobulin G as a model system. Prog Nucl Magn Reson Spectrosc 2010;56(4):346-59
38. Sastry M, Xu L, Georgiev IS, et al. Mammalian production of an isotopically enriched outer domain of the HIV-1 gp120 glycoprotein for NMR spectroscopy. J Biomol NMR 2011;50(3):197-207
39. Takeda M, Kainosho M. Cell-free protein production for NMR studies. Methods Mol Biol 2012;831:71-84
40. Kainosho M, Torizawa T, Iwashita Y, et al. Optimal isotope labelling for NMR protein structure determinations. Nature 2006;440(7080):52-7
41. Goto NK, Kay LE. New developments in isotope labeling strategies for protein solution NMR spectroscopy. Curr Opin Struct Biol 2000;10(5):585-92
42. Chen C-Y, Cheng C-H, Chen Y-C, et al. Preparation of amino-acid-type selective isotope labeling of protein expressed in Pichia pastoris. Proteins 2006;62(1):279-87
43. Brüggert M, Rehm T, Shanker S, et al. A novel medium for expression of proteins selectively labeled with 15N-amino acids in Spodoptera frugiperda (Sf9) insect cells. J Biomol NMR 2003;25(4):335-48
44. Lin MT, Sperling LJ, Frericks Schmidt HL, et al. A rapid and robust method for selective isotope labeling of proteins. Methods 2011;55(4):370-8
45. O'Grady C, Rempel BL, Sokaribo A, et al. One-step amino acid selective isotope labeling of proteins in prototrophic Escherichia coli strains. Anal Biochem 2012;426(2):126-8
46. Yokoyama J, Matsuda T, Koshiba S, et al. A practical method for cell-free protein synthesis to avoid stable isotope scrambling and dilution. Anal Biochem 2011;411(2):223-9
47. Shortle D. Assignment of amino acid type in 1H-15N correlation spectra by labeling with 14N-amino acids. J Magn Reson B 1994;105(1):88-90
48. Hiroaki H, Umetsu Y, Nabeshima Y, et al. A simplified recipe for assigning amide NMR signals using combinatorial 14N amino acid inverse-labeling. J Struct Funct Genomics 2011;12(3):167-74
49. Krishnarjuna B, Jaipuria G, Thakur A, et al. Amino acid selective unlabeling for sequence specific resonance assignments in proteins. J Biomol NMR 2011;49(1):39-51
50. Kohno T. NMR assignment method for amide signals with cell-free protein synthesis system. Methods Mol Biol 2010;607:113-26
51. Iwai H, Zuger S. Protein ligation: applications in NMR studies of proteins. Biotechnology & genetic engineering reviews 2007;24:129-45 . A review for protein ligation and segmental isotope labeling.
52. Yamazaki T, Otomo T, Oda N, et al. Segmental isotope labeling for protein NMR using peptide splicing. J Am Chem Soc 1998;120(22):5591-2
53. Kobayashi H, Swapna GVT, Wu K-P, et al. Segmental isotope labeling of proteins for NMR structural study using a protein S tag for higher expression and solubility. J Biomol NMR 2012;52(4):303-13
54. Senn H, Werner B, Messerle BA, et al. Stereospecific assignment of the methyl 1H NMR lines of valine and leucine in polypeptides by nonrandom 13C labelling. FEBS Lett 1989;249(1):113-18
55. Teilum K, Brath U, Lundstrom P, Akke M. Biosynthetic 13C labeling of aromatic side chains in proteins for NMR relaxation measurements. J Am Chem Soc 2006;128(8):2506-7
56. Lundstrom P, Teilum K, Carstensen T, et al. Fractional 13C enrichment of isolated carbons using [1-13C]- or [2- 13C]-glucose facilitates the accurate measurement of dynamics at backbone Calpha and side-chain methyl positions in proteins. J Biomol NMR 2007;38(3):199-212
57. LeMaster DM, Kushlan DM. Dynamical mapping of E. coli thioredoxin via 13C NMR relaxation analysis. J Am Chem Soc 1996;118(39):9255-64
58. Takeuchi K, Sun Z-YJ, Wagner G. Alternate 13C-12C labeling for complete mainchain resonance assignments using C alpha direct-detection with applicability toward fast relaxing protein systems. J Am Chem Soc 2008;130(51):17210-11
59. Szyperski T. Biosynthetically directed fractional 13C-labeling of proteinogenic amino acids. An efficient analytical tool to investigate intermediary metabolism. Eur J Biochem FEBS 1995;232(2):433-48
60. Szyperski T, Neri D, Leiting B, et al. Support of 1H NMR assignments in proteins by biosynthetically directed fractional 13C-labeling. J Biomol NMR 1992;2(4):323-34
61. Iwai H, Fiaux J. Use of biosynthetic fractional 13C-labeling for backbone NMR assignment of proteins. J Biomol NMR 2007;37(3):187-93
62. Goto NK, Gardner KH, Mueller GA, et al. A robust and cost-effective method for the production of Val, Leu, Ile (delta 1) methyl-protonated 15N-, 13C-, 2H-labeled proteins. J Biomol NMR 1999;13(4):369-74
63. Takeuchi K, Frueh DP, Sun Z-YJ, et al. CACA-TOCSY with alternate 13C-12C labeling: a 13Calpha direct detection experiment for mainchain resonance assignment, dihedral angle information, and amino acid type identification. J Biomol NMR 2010;47(1):55-63
64. Abraham SJ, Hoheisel S, Gaponenko V. Detection of protein-ligand interactions by NMR using reductive methylation of lysine residues. J Biomol NMR 2008;42(2):143-8 . Chemical 13C-methyl labeling on lysin residues.
65. Kobayashi M, Kubota M, Matsuura Y. Crystallization and improvement of crystal quality for x-ray diffraction of maltooligosyl trehalose synthase by reductive methylation of lysine residues. Acta crystallogr D Biol Crystallogr 1999;55(Pt 4):931-3
66. Walter TS, Meier C, Assenberg R, et al. Lysine methylation as a routine rescue strategy for protein crystallization. Structure 2006;14(11):1617-22
67. Sledz P, Zheng H, Murzyn K, et al. New surface contacts formed upon reductive lysine methylation: improving the probability of protein crystallization. Protein sci 2010;19(7):1395-404
68. Oba M, Kobayashi M, Oikawa F, et al. Synthesis of 13 C/D doubly labeled l - leucines: probes for conformational analysis of the leucine side-chain. J Org Chem 2001;66(17):5919-22
69. Oba M, Miyakawa A, Nishiyama K, et al. Stereodivergent Synthesis of (2S, 3S, 4R, 5R) - and (2S, 3S, 4R, 5S) - [3,4,5-D 3]Proline Depending on the Substituent of the g-Lactam Ring. J Org Chem 1999;64(25):9275-8
70. Oba M, Terauchi T, Miyakawa A, et al. Stereoselective deuterium-labelling of diastereotopic methyl and methylene protons of L-leucine. Tetrahedron Lett 1998;39(12):1595-8
71. Takeda M, Sugimori N, Torizawa T, et al. Structure of the putative 32 kDa myrosinase-binding protein from Arabidopsis (At3g16450.1) determined by SAIL-NMR. FEBS J 2008;275(23):5873-84
72. Takeda M, Chang C, Ikeya T, et al. Solution structure of the c-terminal dimerization domain of SARS coronavirus nucleocapsid protein solved by the SAIL-NMR method. J Mol Biol 2008;380(4):608-22
73. Ito Y, Selenko P. Cellular structural biology. Curr Opin Struct Biol 2010;20(5):640-8
74. Serber Z, Selenko P, Ha?nsel R, et al. Investigating macromolecules inside cultured and injected cells by in-cell NMR spectroscopy. Nat Protoc 2006;1(6):2701-9
75. Serber Z, Ledwidge R, Miller SM, Dotsch V. Evaluation of parameters critical to observing proteins inside living Escherichia coli by in-cell NMR spectroscopy. J Am Chem Soc 2001;123(37):8895-901
76. Serber Z, Dotsch V. In-cell NMR spectroscopy. Biochemistry 2001;40(48):14317-23
77. Gronenborn AM, Clore GM. Rapid screening for structural integrity of expressed proteins by heteronuclear NMR spectroscopy. Protein Sci 1996;5(1):174-7 . In situ HSQC experiment of isotopically labeled nonpurified proteins.
78. Sakakibara D, Sasaki A, Ikeya T, et al. Protein structure determination in living cells by in-cell NMR spectroscopy. Nature 2009;458(7234):102-5
79. Ikeya T, Sasaki A, Sakakibara D, et al. NMR protein structure determination in living E. coli cells using nonlinear sampling. Nat Protoc 2010;5(6):1051-60
80. Xie J, Thapa R, Reverdatto S, et al. Screening of small molecule interactor library by using in-cell NMR spectroscopy (SMILI-NMR). J Med Chem 2009;52(11):3516-22
81. Burz DS, Dutta K, Cowburn D, Shekhtman A. In-cell NMR for protein-protein interactions (STINTNMR). Nat Protoc 2006;1(1):146-52
82. Burz DS, Dutta K, Cowburn D, Shekhtman A. Mapping structural interactions using in-cell NMR spectroscopy (STINT-NMR). Nat Methods 2006;3(2):91-3
83. Sakai T, Tochio H, Tenno T, et al. In-cell NMR spectroscopy of proteins inside Xenopus laevis oocytes. J Biomol NMR 2006;36(3):179-88
84. Bodart J-F, Wieruszeski J-M, Amniai L, et al. NMR observation of Tau in Xenopus oocytes. J Mag Reson 2008;192(2):252-7
85. Hansel R, Foldynová-Trantírková S, Lohr F, et al. Evaluation of parameters critical for observing nucleic acids inside living Xenopus laevis oocytes by in-cell NMR spectroscopy. J Am Chem Soc 2009;131(43):15761-8
86. Dascal N. The use of xenopus oocytes for the study of ion channel. Crit Rev Biochem Mol Biol 1987;22(4):317-87
87. Preston GM, Carroll TP, Guggino WB, Agre P. Appearance of water channels in xenopus oocytes expressing red cell CHIP28 protein. Science 1992;256(5055):385-7
88. Pehl U, Leisgen C, Gampe K, Guenther E. Automated higher-throughput compound screening on ion channel targets based on the xenopus laevis oocyte expression system. Assay Drug Dev Technol 2004;2(5):515-24
89. Sakai T, Tochio H, Inomata K, et al. Fluoroscopic assessment of protein leakage during Xenopus oocytes in-cell NMR experiment by co-injected EGFP. Anal Biochem 2007;371(2):247-9
90. Inomata K, Ohno A, Tochio H, et al. High-resolution multi-dimensional NMR spectroscopy of proteins in human cells. Nature 2009;458(7234):106-9
91. Ogino S, Kubo S, Umemoto R, et al. Observation of NMR signals from proteins introduced into living mammalian cells by reversible membrane permeabilization using a pore-forming toxin, streptolysin O. J Am Chem Soc 2009;131(31):10834-5
92. Vives E. A Truncated HIV-1 tat protein basic domain rapidly translocates through the plasma membrane and accumulates in the cell nucleus. J Biol Chem 1997;272(25):16010-17
93. Derossi D, Joliot AH, Chassaing G, Prochiantz A. The third helix of the Antennapedia homeodomain translocates through biological membranes. J Biol Chem 1994;269(14):10444-50
94. Wender PA, Mitchell DJ, Pattabiraman K, et al. The design, synthesis, and evaluation of molecules that enable or enhance cellular uptake: peptoid molecular transporters. Proc Nat Acad Sci 2000;97(24):13003-8
95. Takeuchi T, Kosuge M, Tadokoro A, et al. Direct and rapid cytosolic delivery using cell-penetrating peptides mediated by pyrenebutyrate. ACS Chem Biol 2006;1(5):299-303
96. Montelione GT. The protein structure initiative: achievements and visions for the future. F1000 Biol Rep 2012;4:7
97. Bonvin AMJJ, Rosato A, Wassenaar TA. The eNMR platform for structural biology. J Struct Funct Genomics 2010;11(1):1-8
98. Schanda P, Kupce E, Brutscher B. SOFAST-HMQC experiments for recording two-dimensional heteronuclear correlation spectra of proteins within a few seconds. J Biomol NMR 2005;33(4):199-211
99. Schanda P, Van Melckebeke H, Brutscher B. Speeding up three-dimensional protein NMR experiments to a few minutes. J Am Chem Soc 2006;128(28):9042-3