Stable isotope labeling methods for protein NMR spectroscopy

Progress in Nuclear Magnetic Resonance Spectroscopy

Volumn 53, Issue 4, 2008, Pages 208-226

  Ohki, Shin ya ^a   Kainosho, Masatsune ^b,c  

^a JAPAN ADVANCED INSTITUTE OF SCIENCE AND TECHNOLOGY   (Japan)

^b Japan Science and Technology Agency   (Japan)

^c NAGOYA UNIVERSITY   (Japan)

Author keywords

Protein structure; SAIL; Segmental labeling; Stable isotope aided NMR method; TROSY

Indexed keywords

ISOTOPES; LABELING; NUCLEAR MAGNETIC RESONANCE;

NMR SPECTROS COPY; PROTEIN STRUCTURE; SAIL; SAMPLE PREPARATION METHODS; SEGMENTAL LABELING; STABLE-ISOTOPE LABELING; STABLE-ISOTOPE-AIDED NMR METHOD; TROSY;

NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY;

ELONGATION; ISOTOPES; LABELING; NUCLEAR MAGNETIC RESONANCE; PROTEINS; RELAXATION;

EID: 50249161939     PISSN: 00796565     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pnmrs.2008.01.003     Document Type: Review

References (132)

1. Jardetzky O., and Roberts G.C.K. NMR in Molecular Biology (1981), Academic Press, New York
2. Wüthrich K. NMR of Proteins and Nucleic Acids (1986), John Wiley and Sons, New York
3. Cavanagh J., Fairbother W.J., Palmer III A.G., and Skelton N.J. Protein NMR Spectroscopy (1996), Academic Press, San Diego
4. Wüthrich K. Nat. Struct. Biol. 5 Suppl. (1998) 492-495
5. Kay L.E. J. Magn. Reson. 173 (2005) 193-207
6. Vuister G.W., Tessari M., Karimi-Nejad Y., and Whitehead B. In: Krishna N.R., and Berliner L.J. (Eds). Biological Magnetic Resonance vol. 16 (1999), Kluwer Academic/Publishers, Dordrecht 195-257
7. Grzesiek S., Cordier F., Jaravine V., and Barfield M. Prog. Nucl. Magn. Reson. Spectrosc. 45 (2005) 275-300
8. Blackledge M. Prog. Nucl. Magn. Reson. Spectrosc. 46 (2005) 23-61
9. Bax A., and Pochapsky S.S. J. Magn. Reson. 99 (1992) 638-643
10. Yokoyama S., Hirota H., Kigawa T., Yabuki T., Terada T., Ito Y., Matsuo Y., Kuroda Y., Nishimura Y., Kyogoku Y., Miki K., Masui R., and Kuramitsu S. Nat. Struct. Biol. 7 Suppl. (2000) 943-945
11. Montelione G.T., Zheng D., Huang Y.J., Gunsalus K.C., and Szyperski T. Nat. Struct. Biol. 7 Suppl. (2000) 982-985
12. Yee A., Pardee K., Christendat D., Savchenko A., Edwards A.M., and Arrowsmith C.H. Acc. Chem. Res. 36 (2003) 183-189
13. Staunton D., Owen J., and Campbell I.D. Acc. Chem. Res. 36 (2003) 207-214
14. Crespi H.L., Rosenberg R.M., and Katz J.J. Science 161 (1968) 795-796
15. Markley J.L., Putter I., and Jardetzky O. Science 161 (1968) 1249-1251
16. Kalbitzer H.R., Leberman R., and Wittinghofer A. FEBS Lett. 180 (1985) 40-42
17. LeMaster D.M., and Richards F.M. Biochemistry 27 (1988) 142-150
18. Torchia D.A., Sparks S.W., and Bax A. J. Am. Chem. Soc. 110 (1988) 2320-2321
19. Seeholzer S.H., Cohn M., Putkey J.A., Means A.R., and Crespi H.L. Proc. Natl. Acad. Sci. USA 83 (1986) 6570-6579
20. Griesinger C., Sorensen O.W., and Ernst R.R. J. Magn. Reson. 73 (1987) 574-580
21. Griesinger C., Sorensen O.W., and Ernst R.R. J. Am. Chem. Soc. 109 (1987) 7227-7228
22. Oschkinat H., Cieslar C., Holak T.A., Clore G.M., and Gronenborn A.M. J. Magn. Reson. 83 (1989) 450-472
23. Fesik S.W., and Zuiderweg E.R.P. J. Magn. Reson. 78 (1988) 588-593
24. Marion D., Kay L.E., Sparks S.W., Torchia D.A., and Bax A. Am. Chem. Soc. 111 (1989) 1515-1517
25. Cavanagh J., Palmer A.G., Wright P.E., and Rance M. J. Magn. Reson. 91 (1991) 429-436
26. Palmer A.G., Cavanagh J., Wright P.E., and Rance M. J. Magn. Reson 93 (1991) 151-170
27. Palmer A.G., Cavanagh J., Byrd R.A., and Rance M. J. Magn. Reson. 96 (1992) 416-424
28. Cavanagh J., and Rance M. Annu. Rep. NMR Spectrosc. 27 (1993) 1-58
29. Akke M., Carr P.A., and Palmer A.G. J. Magn. Reson. 104B (1994) 298-302
30. Kay L.E., Keifer P., and Saarinen T. J. Am. Chem. Soc. 114 (1992) 10663-10665
31. Vuister G.W., and Bax A. J. Am. Chem. Soc. 115 (1993) 7772-7777
32. Kubaniwa H., Grzesiek S., Delaglio F., and Bax A. J. Biomol. NMR 6 (1994) 871-878
33. Brünger A.T. X-PLOR: A System for X-ray Crystallography and NMR (1992), Yale University Press, New Haven and London
34. Kainosho M., and Tsuji T. Biochemistry 21 (1982) 6273-6279
35. Kay L.E., Ikura M., Tschudin R., and Bax A. J. Magn. Reson. 89 (1990) 496-514
36. Ikura M., Kay L.E., and Bax A. Biochemistry 29 (1990) 4659-4667
37. Grzesiek S., and Bax A. J. Am. Chem. Soc. 114 (1992) 6291-6293
38. Wittekind M., and Muller L. J. Magn. Reson. 101B (1993) 201-205
39. Grzesiek S., and Bax A. J. Magn. Reson. 99 (1992) 201-207
40. Bax A., Clore G.M., and Gronenbonre A.M. J. Magn. Reson. 88 (1990) 425-431
41. Olejniczak E.T., Xu R.X., and Fesik S.W. J. Biomol. NMR 2 (1992) 655-659
42. Ikura M., and Bax A. J. Am. Chem. Soc. 114 (1992) 2433-2440
43. Lee W., Revington M.J., Arrowsmith C., and Kay L.E. FEBS Lett. 350 (1994) 87-90
44. Folmer R.H.A., Hilbers C.W., Konings R.N.H., and Hallenga K. J. Biomol. NMR 5 (1995) 427-432
45. Ogura K., Terasawa H., and Inagaki F. J. Biomol. NMR 8 (1996) 492-498
46. Zwahlen C., Legault P., Vincent S.J.F., Greenblatt J., Konrat R., and Kay L.E. J. Am. Chem. Soc. 119 (1997) 6711-6721
47. Melacini G. J. Am. Chem. Soc. 122 (2000) 9735-9738
48. Zangger K., Oberer M., Keller W., and Sterk H. J. Magn. Reson. 160 (2003) 97-106
49. O'Donoghue S.I., and Nilges M. In: Krishna N.R., and Berliner L.J. (Eds). Biological Magnetic Resonance vol. 17 (1999), Kluwer Academic/Publishers, Dordrecht 131-161
50. Wu H., Finger D., and Feigon J. Methods Enzymol. 394 (2005) 525-545
51. Hirata R., Ohsumi Y., Nakano A., Kawasaki H., Suzuki K., and Anraku Y. J. Biol. Chem. 265 (1990) 6726-6733
52. Kane P.M., Yamashiro C.T., Wolczyck D.F., Neff N., Goebl M., and Stevens T.H. Science 250 (1990) 651-657
53. Duan X., Gimble F.S., and Quiocho F.A. Cell 89 (1997) 555-564
54. Klabunde T., Sharma S., Telenti A., Jacobs W.R., and Sacchettini J.C. Nat. Struct. Biol. 5 (1998) 31-36
55. Yamazaki T., Otomo T., Oda N., Kyogoku Y., Uegaki K., Ito N., Ishino Y., and Nakamura H. J. Am. Chem. Soc. 120 (1998) 5591-5592
56. Otomo T., Teruya K., Uegaki K., Yamazaki T., and Kyogoku Y. J. Biomol. NMR 14 (1999) 105-114
57. Otomo T., Ito N., Kyogoku Y., and Yamazaki T. Biochemistry 38 (1999) 16040-16044
58. Yagi H., Tsujimoto T., Yamazaki T., Yoshida M., and Akutsu H. J. Am. Chem. Soc. 126 (2004) 16632-16638
59. Xu R., Ayers B., Cowburn D., and Muir T.W. Proc. Natl. Acad. Sci. USA 96 (1999) 388-393
60. Züger S., and Iwai H. Nat. Biotech. 23 (2005) 736-740
61. Iwai H., and Plückthun A. FEBS Lett. 459 (1999) 166-172
62. Williams N.K., Prosselkov P., Liepinsh E., Line I., Shapiro A., Littler D.R., Curmi P.M., Otting G., and Dixon N.E. J. Biol. Chem. 277 (2002) 7790-7798
63. Romanelli A., Shekhtman A., Cowburn D., and Muir T. Proc. Natl. Acad. Sci. USA 101 (2004) 6397-6402
64. Williams N.K., Liepinsh E., Watt S.J., Prosselkov P., Matthews J.M., Attard P., Beck J.L., Dixon N.E., and Otting G. J. Mol. Biol. 346 (2005) 1095-1108
65. Vuister G.W., Kim S.J., Wu C., and Bax A. J. Am. Chem. Soc. 116 (1994) 9206-9210
66. Aghazadeh B., Zhu K., Kubiseski T.J., Liu G.A., Pawson T., Zheng Y., and Rosen M.K. Nat. Struct. Biol. 5 (1998) 1098-1107
67. Wang H., Janowick D.A., Schkeryantz J.M., Liu X., and Fesik S.W. J. Am. Chem. Soc. 121 (1999) 1611-1612
68. Medek A., Olejniczak E.T., Meadows R.P., and Fesik S.W. J. Biomol. NMR 18 (2000) 229-238
69. Pervushin K., Riek R., Wider G., and Wüthrich K. Proc. Natl. Acad. Sci. USA 94 (1997) 12366-12371
70. Pervushin K., Riek R., Wider G., and Wüthrich K. J. Am. Chem. Soc. 120 (1998) 6394-6400
71. Salzmann M., Pervusin K., Wider G., Senn H., and Wüthrich K. Proc. Natl. Acad. Sci. USA 95 (1998) 13585-13590
72. Grzesiek S., Anglister J., Ren H., and Bax A. J. Am. Chem. Soc. 115 (1993) 4369-4370
73. Yamazaki T., Lee W., Arrowsmith C.H., Muhandiram D.R., and Kay L.E. J. Am. Chem. Soc. 116 (1994) 11655-11666
74. Shan X., Gardner K.H., Muhandiram D.R., Rao N.S., Arrowsmith C.H., and Kay L.E. J. Am. Chem. Soc. 118 (1996) 6570-6579
75. Garrett D.S., Seok Y.J., Liao D.I., Peterkofsky A., Gronenborn A.M., and Clore G.M. Biochemistry 36 (1997) 2517-2530
76. Flaux J., Bertelsen E.B., Horwich A.L., and Wüthrich K. Nature 418 (2002) 207-211
77. Ishima R., Louis J.M., and Torchia D.A. J. Biomol. NMR 21 (2001) 167-171
78. Pervushin K., and Eletsky A. J. Biomol. NMR 25 (2003) 147-152
79. Bertini I., Duma L., Felli I.C., Fey M., Luchinat C., Pierattelli R., and Vasos P.R. Angew. Chem., Int. Ed. 43 (2004) 2257-2259
80. Bertini I., Felli I.C., Kümmerle R., Moskau D., and Pierattelli R. J. Am. Chem. Soc. 126 (2004) 464-465
81. Bertini I., Felli I.C., Kümmerle R., Luchinat C., and Pierattelli R. J. Biomol. NMR 30 (2004) 245-251
82. Bermel W., Bertini I., Duma L., Emsley L., Felli I.C., Pierattelli R., and Vasos P.R. Angew. Chem. 44 (2005) 3089-3092
83. Bermel W., Bertini I., Felli I.C., Pierattelli R., and Vasos P.R. J. Magn. Reson. 172 (2005) 324-328
84. Bermel W., Bertini I., Felli I.C., Kümmerle R., and Pierattelli R. J. Magn. Reson. 177 (2005) 404-412
85. Bermel W., Bertini I., Felli I.C., Lee Y.M., Luchinat C., and Pierattelli R. J. Am. Chem. Soc. 128 (2006) 3918-3919
86. Machonkin T.E., Westler W.M., and Markley J.L. J. Am. Chem. Soc. 124 (2002) 9054-9055
87. Arnesano F., Banci L., Bertini I., Felli I.C., Kümmerle R., and Pierattelli R. J. Am. Chem. Soc. 125 (2003) 7200-7208
88. Takahashi H., Nakanishi T., Kami K., Arata Y., and Shimada I. Nat. Struct. Biol. 7 (2000) 220-223
89. Yamazaki T., Tochio H., Furui J., Aimoto S., and Kyogoku Y. J. Am. Chem. Soc. 119 (1997) 872-880
90. Coughlin P.E., Anderson F.E., Oliver E.J., Brown J.M., Homans S.W., Pollak S., and Lustbader J.W. J. Am. Chem. Soc. 121 (1999) 11871-11874
91. Ding K., and Gronenborn A.M. J. Magn. Reson. 167 (2004) 253-258
92. Santoro J., and King G.C. J. Magn. Reson. 97 (1992) 202-207
93. Matsuo H., Kupce E., Li H.J., and Wagner G. J. Magn. Reson. 113B (1996) 91-96
94. Matsuo H., Kupce E., and Wagner G. J. Magn. Reson. 113B (1996) 190-194
95. Metzler W.J., Wittekind M., Goldfarb V., Mueller L., and Farmer II B.T. J. Am. Chem. Soc. 118 (1996) 6800-6801
96. Smith B.O., Ito Y., Raine A., Teichmann S., Ben-Tovim L., Nietlispach D., Broadhurst R.W., Terada T., Kelly M., Oshkinat H., Shibata T., Yokoyama S., and Laue E.D. J. Biomol. NMR 8 (1996) 360-368
97. Rajesh S., Nietlispach D., Nakayama H., Takio K., Laue E.D., Shibata T., and Ito Y. J. Biomol. NMR 27 (2003) 81-86
98. Rosen M.K., Gardner K.H., Willis R.C., Parris W.E., Pawson T., and Kay L.E. J. Mol. Biol. 263 (1996) 627-636
99. Gardner K.H., and Kay L.E. J. Am. Chem. Soc. 119 (1997) 7599-7600
100. Goto N.K., Gardner K.H., Mueller G.A., Willis R.C., and Kay L.E. J. Biomol. NMR 13 (1999) 369-374
101. Gardner K.H., Zhang X.C., Gehring K., and Kay L.E. J. Am. Chem. Soc. 120 (1998) 11738-11748
102. Tugarinov V., Choy W.Y., Orekhov V.Y., and Kay L.E. Proc. Natl. Acad. Sci. USA 102 (2005) 622-627
103. Sprangers R., and Kay L.E. Nature 445 (2007) 618-622
104. Neri D., Szyperski T., Otting G., Senn H., and Wüthrich K. Biochemistry 28 (1989) 7510-7516
105. Atreya H.S., and Chary K.V.R. J. Biomol. NMR 19 (2001) 267-272
106. Tate S., Ushioda T., Utsunomiya N., Shibuya K., Ohyama Y., Nakano Y., Kaji H., Inagaki F., Samejima T., and Kainosho M. Biochemistry 34 (1995) 14637-14648
107. Ohki S., Eto M., Kariya E., Hayano T., Hayashi Y., Yazawa M., Brautigan D., and Kainosho M. J. Mol. Biol. 314 (2001) 839-849
108. Ostler G., Soteriou A., Moody C.M., Khan J.A., Birdsall B., Carr M.D., Young D.W., and Feeney J. FEBS Lett. 318 (1993) 177-180
109. LeMaster D.M., LaIuppa J.C., and Kushlan D.M. J. Biomol. NMR 4 (1994) 863-870
110. Kainosho M., Torizawa T., Iwashita Y., Terauchi T., Ono A.M., and Güntert P. Nature 440 (2006) 52-57
111. Available from: .
112. Oba M., Kobayashi M., Oikawa F., Nishiyama K., and Kainosho M. J. Org. Chem. 66 (2001) 5919-5922
113. Oba M., Terauchi T., Miyazawa A., Kamo H., and Nishiyama K. Tetrahedron Lett. 39 (1998) 1595-1598
114. Oba M., Terauchi T., Miyazawa A., and Nishiyama K. Tetrahedron Asymmetry 10 (1999) 937-945
115. Terauchi T., Ohki S., and Kainosho M. PNE (Tankakushitsu Kakusan Koso) 47 (1998) 1045-1051
116. Torizawa T., Shimizu M., Taoka M., Miyano H., and Kainosho M. J. Biomol. NMR 30 (2004) 311-325
117. Torizawa T., Ono A.M., Terauchi T., and Kainosho M. J. Am. Chem. Soc. 127 (2005) 12620-12626
118. Yamazaki T., Forman-Kay J.D., and Kay L.E. J. Am. Chem. Soc. 115 (1993) 11054-11055
119. Ikeya T., Terauchi T., Güntert P., and Kainosho M. Magn. Reson. Chem. 44 (2006) 152-157
120. Fiaux J., Bertelsen E.B., Horwich A.L., and Wüthrich K. J. Biomol. NMR 29 (2004) 289-297
121. Waugh D.S. J. Biomol. NMR 8 (1996) 184-192
122. Wood M.J., and Komives E.A. J. Biomol. NMR 13 (1999) 149-159
123. Massou S., Puech V., Talmont F., Demange P., Lindley N.D., Tropis M., and Milon A. J. Biomol. NMR 14 (1999) 231-239
124. Hansen A.P., Petros A.M., Mazar A.P., Pederson T.M., Rueter A., and Fesik S.W. Biochemistry 31 (1992) 12713-12718
125. Strauss A., Bitsch F., Cutting B., Fendrich G., Graff P., Liebetanz J., Zurini M., and Jahnke W. J. Biomol. NMR 26 (2003) 367-372
126. Spirin A.S., Baranov V.I., Ryabova L.A., Ovodov S.Y., and Alakhov Y.B. Science 242 (1988) 1162-1164
127. Kramer G., Kudlicki W., and Hardesty B. In: Higgins S.J., and Harmes B.D. (Eds). Protein Expression (1999), Oxford University Press, New York 201-223
128. Kigawa T., Muto Y., and Yokoyama S. J. Biomol. NMR 6 (1995) 129-134
129. Ozawa K., Headlam M.J., Schaeffer P.M., Henderson B.R., Dixon N.E., and Otting G. Eur. J. Biochem. 271 (2004) 4084-4093
130. Morita E.H., Shimizu M., Ogasawara T., Endo Y., Tanaka R., and Kohno T. J. Biomol. NMR 30 (2004) 37-45
131. Berrier C., Park K.H., Abes S., Bibonne A., Betton J.M., and Ghazi A. Biochemistry 43 (2004) 12585-12591
132. Rothschild K.J., and Gite S. Curr. Opin. Biotechnol. 10 (1999) 64-70