Skip to main content

Solid-State NMR Spectroscopy of Proteins

  • Chapter
  • First Online:

Part of the book series: Topics in Current Chemistry ((TOPCURRCHEM,volume 335))

Abstract

Solid-state NMR spectroscopy proved to be a versatile tool for characterization of structure and dynamics of complex biochemical systems. In particular, magic angle spinning (MAS) solid-state NMR came to maturity for application towards structural elucidation of biological macromolecules. Current challenges in applying solid-state NMR as well as progress achieved recently will be discussed in the following chapter focusing on conceptual aspects important for structural elucidation of proteins.

To my father Werner Heise (1944–2013)

This is a preview of subscription content, log in via an institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

Abbreviations

APP:

Amyloid precursor protein

ASR:

Anabaena sensory rhodopsin

CE:

Cross-effect

CRAMPS:

Combined rotation and multiple pulse spectroscopy

CW:

Continuous wave

DARR:

Dipolar assisted rotational resonance

DNP:

Dynamic nuclear polarization

EPR:

Electron paramagnetic resonance

FSLG:

Frequency-switched Lee-Goldburg

GPCR:

G protein-coupled receptor

HORROR:

Homonuclear rotary resonance

INEPT:

Insensitive nuclei enhanced by polarization transfer

MAS:

Magic angle spinning

PDSD:

Proton-driven spin diffusion

PMLG:

Phase-modulated Lee-Goldburg

PRE:

Paramagnetic relaxation enhancement

REDOR:

Rotational echo double resonance

SE:

Solid effect

TEDOR:

Transferred echo double resonance

TM:

Transmembrane helix

References

  1. Opella SJ, Marassi FM (2004) Chem Rev 104:3587

    CAS  Google Scholar 

  2. Andrew ER, Bradbury A, Eades RG (1958) Nature 182:1659

    CAS  Google Scholar 

  3. Heise H (2008) Chembiochem 9:179

    CAS  Google Scholar 

  4. McDermott A (2009) Annu Rev Biophys 38:385

    CAS  Google Scholar 

  5. Wylie BJ, Rienstra CM (2008) J Chem Phys 128:052207

    Google Scholar 

  6. Higman VA, Flinders J, Hiller M, Jehle S, Markovic S, Fiedler S, van Rossum BJ, Oschkinat H (2009) J Biomol NMR 44:245

    CAS  Google Scholar 

  7. Böckmann A (2008) Angew Chem Int Ed Engl 47:6110

    Google Scholar 

  8. Guo C, Geng C, Tugarinov V (2009) J Biomol NMR 44:167

    CAS  Google Scholar 

  9. Lundstrom P, Teilum K, Carstensen T, Bezsonova I, Wiesner S, Hansen DF, Religa TL, Akke M, Kay LE (2007) J Biomol NMR 38:199

    Google Scholar 

  10. Boer E, Steinborn G, Kunze G, Gellissen G (2007) Appl Microbiol Biotechnol 77:513

    Google Scholar 

  11. Madden DR, Safferling M (2007) Methods Mol Biol 363:39

    CAS  Google Scholar 

  12. Armstrong N, Sun Y, Chen GQ, Gouaux E (1998) Nature 395:913

    CAS  Google Scholar 

  13. Waugh DS (1996) J Biomol NMR 8:184

    CAS  Google Scholar 

  14. Hong M, Jakes K (1999) J Biomol NMR 14:71

    CAS  Google Scholar 

  15. Whittaker JW (2007) Methods Mol Biol 389:175

    CAS  Google Scholar 

  16. Blanco FJ, Hess S, Pannell LK, Rizzo NW, Tycko R (2001) J Mol Biol 313:845

    CAS  Google Scholar 

  17. LeMaster DM, Kushlan DM (1996) J Am Chem Soc 118:9255

    Google Scholar 

  18. Lee AL, Urbauer JL, Wand AJ (1997) J Biomol NMR 9:437

    CAS  Google Scholar 

  19. Kigawa T, Muto Y, Yokoyama S (1995) J Biomol NMR 6:129

    CAS  Google Scholar 

  20. Noren CJ, Anthonycahill SJ, Griffith MC, Schultz PG (1989) Science 244:182

    CAS  Google Scholar 

  21. Young TS, Schultz PG (2010) J Biol Chem 285:11039

    CAS  Google Scholar 

  22. Tugarinov V, Kanelis V, Kay LE (2006) Nat Protoc 1:749

    CAS  Google Scholar 

  23. Gardner KH, Kay LE (1998) Annu Rev Biophys Biomol Struct 27:357

    CAS  Google Scholar 

  24. Chevelkov V, Rehbein K, Diehl A, Reif B (2006) Angew Chem Int Ed Engl 45:3878

    CAS  Google Scholar 

  25. del Amo JM, Fink U, Reif B (2010) J Biomol NMR 48:203

    CAS  Google Scholar 

  26. Asami S, Schmieder P, Reif B (2010) J Am Chem Soc 132:15133

    CAS  Google Scholar 

  27. Zhou DH, Shah G, Cormos M, Mullen C, Sandoz D, Rienstra CM (2007) J Am Chem Soc 129: 11791

    CAS  Google Scholar 

  28. Etzkorn M, Böckmann A, Lange A, Baldus M (2004) J Am Chem Soc 126:14746

    CAS  Google Scholar 

  29. Mao L, Vaiphei ST, Shimazu T, Schneider WM, Tang Y, Mani R, Roth MJ, Montelione GT, Inouye M (2010) J Struct Funct Genomics 11:81

    CAS  Google Scholar 

  30. Havlin RH, Tycko R (2005) Proc Natl Acad Sci USA 102:3284

    CAS  Google Scholar 

  31. Heise H, Luca S, de Groot BL, Grubmüller H, Baldus M (2005) Biophys J 89:2113

    CAS  Google Scholar 

  32. Karpinar DP, Balija MB, Kugler S, Opazo F, Rezaei-Ghaleh N, Wender N, Kim HY, Taschenberger G, Falkenburger BH, Heise H, Kumar A, Riedel D, Fichtner L, Voigt A, Braus GH, Giller K, Becker S, Herzig A, Baldus M, Jackle H, Eimer S, Schulz JB, Griesinger C, Zweckstetter M (2009) EMBO J 28:3256

    CAS  Google Scholar 

  33. Sakellariou D, Brown SP, Lesage A, Hediger S, Bardet M, Meriles CA, Pines A, Emsley L (2003) J Am Chem Soc 125:4376

    CAS  Google Scholar 

  34. Mainz A, Jehle S, van Rossum BJ, Oschkinat H, Reif B (2009) J Am Chem Soc 131:15968

    CAS  Google Scholar 

  35. Bertini I, Luchinat C, Parigi G, Ravera E, Reif B, Turano P (2011) Proc Natl Acad Sci 108: 10396

    CAS  Google Scholar 

  36. Tycko R (2011) Annu Rev Phys Chem 62:279

    CAS  Google Scholar 

  37. Tycko R (2006) Q Rev Biophys 39:1

    CAS  Google Scholar 

  38. Goldbourt A, Gross BJ, Day LA, McDermott AE (2007) J Am Chem Soc 129:2338

    CAS  Google Scholar 

  39. Goldbourt A, Day LA, McDermott AE (2010) J Biol Chem 285:37051

    CAS  Google Scholar 

  40. Loquet A, Sgourakis NG, Gupta R, Giller K, Riedel D, Goosmann C, Griesinger C, Kolbe M, Baker D, Becker S, Lange A (2012) Nature 486:276

    CAS  Google Scholar 

  41. Hoyer W, Antony T, Cherny D, Heim G, Jovin TM, Subramaniam V (2002) J Mol Biol 322: 383

    CAS  Google Scholar 

  42. Petkova AT, Leapman RD, Guo Z, Yau W-M, Mattson MP, Tycko R (2005) Science 307:262

    CAS  Google Scholar 

  43. Paravastu AK, Leapman RD, Yau WM, Tycko R (2008) Proc Natl Acad Sci USA 105:18349

    CAS  Google Scholar 

  44. Qiang W, Yau WM, Tycko R (2011) J Am Chem Soc 133:4018

    CAS  Google Scholar 

  45. Paravastu AK, Qahwash I, Leapman RD, Meredith SC, Tycko R (2009) Proc Natl Acad Sci USA 106:7443

    CAS  Google Scholar 

  46. Kryndushkin DS, Wickner RB, Tycko R (2011) J Mol Biol 409:263

    CAS  Google Scholar 

  47. Cross TA, Sharma M, Yi M, Zhou HX (2011) Trends Biochem Sci 36:117

    CAS  Google Scholar 

  48. De Angelis AA, Opella SJ (2007) Nat Protoc 2:2332

    Google Scholar 

  49. Diller A, Loudet C, Aussenac F, Raffard G, Fournier S, Laguerre M, Grelard A, Opella SJ, Marassi FM, Dufourc EJ (2009) Biochimie 91:744

    CAS  Google Scholar 

  50. Cho HS, Dominick JL, Spence MM (2010) J Phys Chem B 114:9238

    CAS  Google Scholar 

  51. Grelard A, Loudet C, Diller A, Dufourc EJ (2010) Methods Mol Biol 654:341

    CAS  Google Scholar 

  52. Bayburt TH, Carlson JW, Sligar SG (1998) J Struct Biol 123:37

    CAS  Google Scholar 

  53. Li Y, Kijac AZ, Sligar SG, Rienstra CM (2006) Biophys J 91:3819

    CAS  Google Scholar 

  54. Kijac AZ, Li Y, Sligar SG, Rienstra CM (2007) Biochemistry 46:13696

    CAS  Google Scholar 

  55. Kijac A, Shih AY, Nieuwkoop AJ, Schulten K, Sligar SG, Rienstra CM (2010) Biochemistry 49:9190

    CAS  Google Scholar 

  56. Maricq MM, Waugh JS (1979) J Chem Phys 70:3300

    CAS  Google Scholar 

  57. Bajaj VS, van der Wel PC, Griffin RG (2009) J Am Chem Soc 131:118

    CAS  Google Scholar 

  58. Franks WT, Zhou DH, Wylie BJ, Money BG, Graesser DT, Frericks HL, Sahota G, Rienstra CM (2005) J Am Chem Soc 127:12291

    CAS  Google Scholar 

  59. Linden A, Franks W, Akbey Ü, Lange S, van Rossum B-J, Oschkinat H (2011) J Biomol NMR 51:283

    CAS  Google Scholar 

  60. Thurber KR, Tycko R (2008) J Magn Reson 195:179

    CAS  Google Scholar 

  61. Bertini I, Emsley L, Lelli M, Luchinat C, Mao J, Pintacuda G (2010) J Am Chem Soc 132: 5558

    CAS  Google Scholar 

  62. Laage S, Sachleben JR, Steuernagel S, Pierattelli R, Pintacuda G, Emsley L (2009) J Magn Reson 196:133

    CAS  Google Scholar 

  63. Lee M, Goldburg I (1965) Phys Rev 140:A1261

    Google Scholar 

  64. Dvinskikh SV, Zimmermann H, Maliniak A, Sandstrom D (2005) J Chem Phys 122:44512

    Google Scholar 

  65. Vinogradov E, Madhu PK, Vega S (1999) Chem Phys Lett 314:443

    CAS  Google Scholar 

  66. Sakellariou D, Lesage A, Hodgkinson P, Emsley L (2000) Chem Phys Lett 319:253

    CAS  Google Scholar 

  67. Haeberlen U, Waugh JS (1968) Phys Rev 175:453

    CAS  Google Scholar 

  68. Gerstein BC, Pembleton RG, Wilson RC, Ryan LM (1977) J Chem Phys 66:361

    CAS  Google Scholar 

  69. Vinogradov E, Madhu PK, Vega S (2002) Chem Phys Lett 354:193

    CAS  Google Scholar 

  70. Lesage A, Sakellariou D, Hediger S, Elena B, Charmont P, Steuernagel S, Emsley L (2003) J Magn Reson 163:105

    CAS  Google Scholar 

  71. Schaefer J, Stejskal EO (1976) J Am Chem Soc 98:1031

    CAS  Google Scholar 

  72. Bennett AE, Rienstra CM, Auger M, Lakshmi KV, Griffin RG (1995) J Chem Phys 103:6951

    CAS  Google Scholar 

  73. Detken A, Hardy EH, Ernst M, Meier BH (2002) Chem Phys Lett 356:298

    CAS  Google Scholar 

  74. Fung BM, Khitrin AK, Ermolaev K (2000) J Magn Reson 142:97

    CAS  Google Scholar 

  75. Ernst M, Samoson A, Meier BH (2001) Chem Phys Lett 348:293

    CAS  Google Scholar 

  76. Ladizhansky V (2009) Solid State Nucl Magn Reson 36:119

    CAS  Google Scholar 

  77. De Paëpe G (2012) Annu Rev Phys Chem 63:661

    Google Scholar 

  78. Gullion T, Schaefer J (1989) J Magn Reson 81:196

    CAS  Google Scholar 

  79. Hing AW, Vega S, Schaefer J (1992) J Magn Reson 96:205

    CAS  Google Scholar 

  80. Jaroniec CP, Tounge BA, Herzfeld J, Griffin RG (2001) J Am Chem Soc 123:3507

    CAS  Google Scholar 

  81. Baldus M, Petkova AT, Herzfeld J, Griffin RG (1998) Mol Phys 95:1197

    CAS  Google Scholar 

  82. Schütz A, Wasmer C, Habenstein B, Verel R, Greenwald J, Riek R, Böckmann A, Meier BH (2010) Chembiochem 11:1543

    Google Scholar 

  83. Andrew ER, Clough S, Farnell LF, Gledhill TD, Roberts I (1966) Phys Lett 21:505

    CAS  Google Scholar 

  84. Raleigh DP, Levitt MH, Griffin RG (1988) Chem Phys Lett 146:71

    CAS  Google Scholar 

  85. Levitt MH, Oas TG, Griffin RG (1988) Isr J Chem 28:271

    Google Scholar 

  86. Nielsen NC, Bildsoe H, Jakobsen HJ, Levitt MH (1994) J Chem Phys 101:1805

    CAS  Google Scholar 

  87. Levitt MH (2002) In: Harris RK (ed) Encyclopedia of nuclear magnetic resonance: supplementary volume. Wiley, Chichester, p 165

    Google Scholar 

  88. Hohwy M, Rienstra CM, Griffin RG (2002) J Chem Phys 117:4973

    CAS  Google Scholar 

  89. Bayro MJ, Huber M, Ramachandran R, Davenport TC, Meier BH, Ernst M, Griffin RG (2009) J Chem Phys 130:114506

    Google Scholar 

  90. Hohwy M, Rienstra CM, Jaroniec CP, Griffin RG (1999) J Chem Phys 110:7983

    CAS  Google Scholar 

  91. Bayro MJ, Maly T, Birkett NR, Dobson CM, Griffin RG (2009) Angew Chem Int Ed 48:5708

    CAS  Google Scholar 

  92. Caravatti P, Neuenschwander P, Ernst RR (1985) Macromolecules 18:119

    CAS  Google Scholar 

  93. Brus J, Petrickova H, Dybal J (2003) Solid State Nucl Magn Reson 23:183

    CAS  Google Scholar 

  94. Brown SP (2007) Prog Nucl Magn Reson Spectrosc 50:199

    CAS  Google Scholar 

  95. Zhang S, Meier BH, Ernst RR (1992) Phys Rev Lett 69:2149

    CAS  Google Scholar 

  96. Lange A, Luca S, Baldus M (2002) J Am Chem Soc 124:9704

    CAS  Google Scholar 

  97. Grommek A, Meier BH, Ernst M (2006) Chem Phys Lett 427:404

    CAS  Google Scholar 

  98. Castellani F, van Rossum B, Diehl A, Schubert M, Rehbein K, Oschkinat H (2002) Nature 420:98

    CAS  Google Scholar 

  99. Manolikas T, Herrmann T, Meier BH (2008) J Am Chem Soc 130:3959

    CAS  Google Scholar 

  100. Takegoshi K, Nakamura S, Terao T (2001) Chem Phys Lett 344:631

    CAS  Google Scholar 

  101. Takegoshi K, Nakamura S, Terao T (2003) J Chem Phys 118:2325

    CAS  Google Scholar 

  102. Morcombe CR, Gaponenko V, Byrd RA, Zilm KW (2004) J Am Chem Soc 126:7196

    CAS  Google Scholar 

  103. Weingarth M, Demco DE, Bodenhausen G, Tekely P (2009) Chem Phys Lett 469:342

    CAS  Google Scholar 

  104. Scholz I, Huber M, Manolikas T, Meier BH, Ernst M (2008) Chem Phys Lett 460:278

    CAS  Google Scholar 

  105. De Paepe G, Lewandowski JR, Loquet A, Bockmann A, Griffin RG (2008) J Chem Phys 129: 245101

    Google Scholar 

  106. Lewandowski JR, De Paepe G, Griffin RG (2007) J Am Chem Soc 129:728

    CAS  Google Scholar 

  107. Morris GA, Freeman R (1979) J Am Chem Soc 101:760

    CAS  Google Scholar 

  108. Andronesi OC, Becker S, Seidel K, Heise H, Young HS, Baldus M (2005) J Am Chem Soc 127:12965

    CAS  Google Scholar 

  109. Siemer AB, Arnold AA, Ritter C, Westfeld T, Ernst M, Riek R, Meier BH (2006) J Am Chem Soc 128:13224

    CAS  Google Scholar 

  110. Heise H, Hoyer W, Becker S, Andronesi OC, Riedel D, Baldus M (2005) Proc Natl Acad Sci USA 102:15871

    CAS  Google Scholar 

  111. Helmus JJ, Surewicz K, Surewicz WK, Jaroniec CP (2010) J Am Chem Soc 132:2393

    CAS  Google Scholar 

  112. Munowitz MG, Griffin RG, Bodenhausen G, Huang TH (1981) J Am Chem Soc 103:2529

    CAS  Google Scholar 

  113. Heise H, Celej MS, Becker S, Riede D, Pelah A, Kumar A, Jovin TM, Baldus M (2008) J Mol Biol 380:444

    CAS  Google Scholar 

  114. Helmus JJ, Surewicz K, Nadaud PS, Surewicz WK, Jaroniec CP (2008) Proc Natl Acad Sci USA 105:6284

    CAS  Google Scholar 

  115. Böckmann A, Meier B (2010) Prion 4:72

    Google Scholar 

  116. Glenner GG, Wong CW (1984) Biochem Biophys Res Commun 120:885

    CAS  Google Scholar 

  117. Kang J, Lemaire H-G, Unterbeck A, Salbaum JM, Masters CL, Grzeschik K-H, Multhaup G, Beyreuther K, Muller-Hill B (1987) Nature 325:733

    CAS  Google Scholar 

  118. Tycko R, Sciarretta KL, Orgel JP, Meredith SC (2009) Biochemistry 48:6072

    CAS  Google Scholar 

  119. Lopez del Amo JM, Schmidt M, Fink U, Dasari M, Fändrich M, Reif B (2012) Angew Chem Int Ed 51:6136

    Google Scholar 

  120. Bertini I, Gonnelli L, Luchinat C, Mao J, Nesi A (2011) J Am Chem Soc 133:16013

    CAS  Google Scholar 

  121. Chimon S, Shaibat MA, Jones CR, Calero DC, Aizezi B, Ishii Y (2007) Nat Struct Mol Biol 14:1157

    CAS  Google Scholar 

  122. Ahmed M, Davis J, Aucoin D, Sato T, Ahuja S, Aimoto S, Elliott JI, Van Nostrand WE, Smith SO (2010) Nat Struct Mol Biol 17:561

    CAS  Google Scholar 

  123. Scheidt HA, Morgado I, Rothemund S, Huster D, Fandrich M (2011) Angew Chem Int Ed Engl 50:2837

    CAS  Google Scholar 

  124. Scheidt HA, Morgado I, Huster D (2012) J Biol Chem 287:22822

    CAS  Google Scholar 

  125. Spillantini MG, Schmidt ML, Lee VMY, Trojanowski JQ, Jakes R, Goedert M (1997) Nature 388:839

    CAS  Google Scholar 

  126. Kruger R, Kuhn W, Muller T, Woitalla D, Graeber M, Kosel S, Przuntek H, Epplen JT, Schols L, Riess O (1998) Nat Genet 18:106

    CAS  Google Scholar 

  127. Polymeropoulos MH, Lavedan C, Leroy E, Ide SE, Dehejia A, Dutra A, Pike B, Root H, Rubenstein J, Boyer R, Stenroos ES, Chandrasekharappa S, Athanassiadou A, Papapetropoulos T, Johnson WG, Lazzarini AM, Duvoisin RC, DiIorio G, Golbe LI, Nussbaum RL (1997) Science 276:2045

    CAS  Google Scholar 

  128. Zarranz JJ, Alegre J, Gomez-Esteban JC, Lezcano E, Ros R, Ampuero I, Vidal L, Hoenicka J, Rodriguez O, Atares B, Llorens V, Tortosa EG, del Ser T, Munoz DG, de Yebenes JG (2004) Ann Neurol 55:164

    CAS  Google Scholar 

  129. Kloepper KD, Woods WS, Winter KA, George JM, Rienstra CM (2006) Protein Expr Purif 48:112

    CAS  Google Scholar 

  130. Kloepper K, Zhou D, Li Y, Winter K, George J, Rienstra C (2007) J Biomol NMR 39:197

    CAS  Google Scholar 

  131. Kloepper KD, Hartman KL, Ladror DT, Rienstra CM (2007) J Phys Chem B 111:13353

    CAS  Google Scholar 

  132. Vilar M, Chou HT, Luhrs T, Maji SK, Riek-Loher D, Verel R, Manning G, Stahlberg H, Riek R (2008) Proc Natl Acad Sci USA 105:8637

    CAS  Google Scholar 

  133. Loquet A, Giller K, Becker S, Lange A (2010) J Am Chem Soc 132:15164

    CAS  Google Scholar 

  134. Gath J, Habenstein B, Bousset L, Melki R, Meier B, Böckmann A (2012) Biomol NMR Assign 6:51

    CAS  Google Scholar 

  135. Chen M, Margittai M, Chen J, Langen R (2007) J Biol Chem 282:24970

    CAS  Google Scholar 

  136. Lemkau LR, Comellas G, Kloepper KD, Woods WS, George JM, Rienstra CM (2012) J Biol Chem 287:11526

    CAS  Google Scholar 

  137. Comellas G, Lemkau LR, Nieuwkoop AJ, Kloepper KD, Ladror DT, Ebisu R, Woods WS, Lipton AS, George JM, Rienstra CM (2011) J Mol Biol 411:881

    CAS  Google Scholar 

  138. Saibil HR, Seybert A, Habermann A, Winkler J, Eltsov M, Perkovic M, Castaño-Diez D, Scheffer MP, Haselmann U, Chlanda P, Lindquist S, Tyedmers J, Frangakis AS (2012) Proc Natl Acad Sci USA 109:14906

    Google Scholar 

  139. Wickner RB (1994) Science 264:566

    CAS  Google Scholar 

  140. Suzuki G, Shimazu N, Tanaka M (2012) Science 336:355

    CAS  Google Scholar 

  141. Shewmaker F, Wickner RB, Tycko R (2006) Proc Natl Acad Sci USA 103:19754

    CAS  Google Scholar 

  142. Baxa U, Wickner RB, Steven AC, Anderson DE, Marekov LN, Yau WM, Tycko R (2007) Biochemistry 46:13149

    CAS  Google Scholar 

  143. Wickner RB, Dyda F, Tycko R (2008) Proc Natl Acad Sci USA 105:2403

    CAS  Google Scholar 

  144. Shewmaker F, Kryndushkin D, Chen B, Tycko R, Wickner RB (2009) Biochemistry 48:5074

    CAS  Google Scholar 

  145. Chan JCC, Oyler NA, Yau WM, Tycko R (2005) Biochemistry 44:10669

    CAS  Google Scholar 

  146. Goncalves JA, Ahuja S, Erfani S, Eilers M, Smith SO (2010) Prog Nucl Magn Reson Spectrosc 57:159

    CAS  Google Scholar 

  147. Stouffer AL, Acharya R, Salom D, Levine AS, Di Costanzo L, Soto CS, Tereshko V, Nanda V, Stayrook S, DeGrado WF (2008) Nature 451:596

    CAS  Google Scholar 

  148. van der Wel PCA, Lewandowski JR, Griffin RG (2007) J Am Chem Soc 129:5117

    Google Scholar 

  149. Lewandowski JR, van der Wel PCA, Rigney M, Grigorieff N, Griffin RG (2011) J Am Chem Soc 133:14686

    CAS  Google Scholar 

  150. Loquet A, Bousset L, Gardiennet C, Sourigues Y, Wasmer C, Habenstein B, Schütz A, Meier BH, Melki R, Böckmann A (2009) J Mol Biol 394:108

    CAS  Google Scholar 

  151. Ritter C, Maddelein ML, Siemer AB, Luhrs T, Ernst M, Meier BH, Saupe SJ, Riek R (2005) Nature 435:844

    CAS  Google Scholar 

  152. Wasmer C, Lange A, Van Melckebeke H, Siemer AB, Riek R, Meier BH (2008) Science 319: 1523

    CAS  Google Scholar 

  153. Van Melckebeke H, Wasmer C, Lange A, Ab E, Loquet A, Böckmann A, Meier BH (2010) J Am Chem Soc 132:13765

    Google Scholar 

  154. Wasmer C, Schütz A, Loquet A, Buhtz C, Greenwald J, Riek R, Böckmann A, Meier BH (2009) J Mol Biol 394:119

    CAS  Google Scholar 

  155. Schütz AK, Soragni A, Hornemann S, Aguzzi A, Ernst M, Böckmann A, Meier BH (2011) Angew Chem Int Ed 50:5956

    Google Scholar 

  156. Hong M, Zhang Y, Hu FH (2012) Annu Rev Phys Chem 63:1

    Google Scholar 

  157. Smith SO (2010) Annu Rev Biophys 39:309

    Google Scholar 

  158. Schnell JR, Chou JJ (2008) Nature 451:591

    CAS  Google Scholar 

  159. Cady SD, Hong M (2008) Proc Natl Acad Sci USA 105:1483

    CAS  Google Scholar 

  160. Cady SD, Mishanina TV, Hong MJ (2009) Mol Biol 385:1127

    CAS  Google Scholar 

  161. Cady SD, Schmidt-Rohr K, Wang J, Soto CS, DeGrado WF, Hong M (2010) Nature 463:689

    CAS  Google Scholar 

  162. Cady S, Wang T, Hong M (2011) J Am Chem Soc 133:11572

    CAS  Google Scholar 

  163. Miao Y, Qin H, Fu R, Sharma M, Can TV, Hung I, Luca S, Gor'kov PL, Brey WW, Cross TA (2012) Angew Chem Int Ed 51:8383

    CAS  Google Scholar 

  164. Hu FH, Luo WB, Hong M (2010) Science 330:505

    CAS  Google Scholar 

  165. Hong M, Fritzsching KJ, Williams JK (2012) J Am Chem Soc 134:14753

    CAS  Google Scholar 

  166. Luo W, Hong M (2010) J Am Chem Soc 132:2378

    CAS  Google Scholar 

  167. Andreas LB, Eddy MT, Chou JJ, Griffin RG (2012) J Am Chem Soc 134:7215

    CAS  Google Scholar 

  168. Oesterhelt D, Stoeckenius W (1971) Nature 233:149

    CAS  Google Scholar 

  169. Béjà O, Aravind L, Koonin EV, Suzuki MT, Hadd A, Nguyen LP, Jovanovich SB, Gates CM, Feldman RA, Spudich JL, Spudich EN, DeLong EF (2000) Science 289:1902

    Google Scholar 

  170. Gordeliy VI, Labahn J, Moukhametzianov R, Efremov R, Granzin J, Schlesinger R, Buldt G, Savopol T, Scheidig AJ, Klare JP, Engelhard M (2002) Nature 419:484

    CAS  Google Scholar 

  171. Gautier A, Mott HR, Bostock MJ, Kirkpatrick JP, Nietlispach D (2010) Nat Struct Mol Biol 17:768

    CAS  Google Scholar 

  172. Reckel S, Gottstein D, Stehle J, Löhr F, Verhoefen M-K, Takeda M, Silvers R, Kainosho M, Glaubitz C, Wachtveitl J, Bernhard F, Schwalbe H, Güntert P, Dötsch V (2011) Angew Chem Int Ed 50:11942

    CAS  Google Scholar 

  173. Klare JP, Bordignon E, Doebber M, Fitter J, Kriegsmann J, Chizhov I, Steinhoff HJ, Engelhard M (2006) J Mol Biol 356:1207

    CAS  Google Scholar 

  174. Moukhametzianov R, Klare JP, Efremov R, Baeken C, Goppner A, Labahn J, Engelhard M, Buldt G, Gordeliy VI (2006) Nature 440:115

    CAS  Google Scholar 

  175. Etzkorn M, Seidel K, Li L, Martell S, Geyer M, Engelhard M, Baldus M (2010) Structure 18:293

    CAS  Google Scholar 

  176. Bajaj VS, Mak-Jurkauskas ML, Belenky M, Herzfeld J, Griffin RG (2009) Proc Natl Acad Sci USA 106:9244

    CAS  Google Scholar 

  177. Mak-Jurkauskas ML, Bajaj VS, Hornstein MK, Belenky M, Griffin RG, Herzfeld J (2008) Proc Natl Acad Sci USA 105:883

    CAS  Google Scholar 

  178. Harbison GS, Smith SO, Pardoen JA, Winkel C, Lugtenburg J, Herzfeld J, Mathies R, Griffin RG (1984) Proc Natl Acad Sci USA 81:1706

    CAS  Google Scholar 

  179. Jaroniec CP, Lansing JC, Tounge BA, Belenky M, Herzfeld J, Griffin RG (2001) J Am Chem Soc 123:12929

    CAS  Google Scholar 

  180. Higman VA, Varga K, Aslimovska L, Judge PJ, Sperling LJ, Rienstra CM, Watts A (2011) Angew Chem Int Ed Engl 50(36):8432

    CAS  Google Scholar 

  181. Shi L, Ahmed MAM, Zhang W, Whited G, Brown LS, Ladizhansky V (2009) J Mol Biol 386:1078

    CAS  Google Scholar 

  182. Shi L, Kawamura I, Jung K-H, Brown LS, Ladizhansky V (2011) Angew Chem Int Ed 50:1302

    CAS  Google Scholar 

  183. Wang S, Shi L, Okitsu T, Wada A, Brown LS, Ladizhansky V (2012) Biomol NMR Assign

    Google Scholar 

  184. Pfleger N, Worner AC, Yang J, Shastri S, Hellmich UA, Aslimovska L, Maier MS, Glaubitz C (2009) Biochim Biophys Acta 1787:697

    CAS  Google Scholar 

  185. Yang J, Aslimovska L, Glaubitz C (2011) J Am Chem Soc 133:4874

    CAS  Google Scholar 

  186. Pfleger N, Lorch M, Woerner AC, Shastri S, Glaubitz C (2008) J Biomol NMR 40:15

    CAS  Google Scholar 

  187. Ward ME, Shi L, Lake E, Krishnamurthy S, Hutchins H, Brown LS, Ladizhansky VJ (2011) J Am Chem Soc 133:17434

    CAS  Google Scholar 

  188. Hempelmann F, Holper S, Verhoefen MK, Woerner AC, Kohler T, Fiedler SA, Pfleger N, Wachtveitl J, Glaubitz C (2011) J Am Chem Soc 133:4645

    CAS  Google Scholar 

  189. Wang S, Munro RA, Kim SY, Jung KH, Brown LS, Ladizhansky V (2012) J Am Chem Soc 134:16995

    CAS  Google Scholar 

  190. Hopkins AL, Groom CR (2002) Nat Rev Drug Discov 1:727

    CAS  Google Scholar 

  191. Jacoby E, Bouhelal R, Gerspacher M, Seuwen K (2006) ChemMedChem 1:761

    Google Scholar 

  192. Klabunde T, Hessler G (2002) Chembiochem 3:928

    CAS  Google Scholar 

  193. Rosenbaum DM, Rasmussen SG, Kobilka BK (2009) Nature 459:356

    CAS  Google Scholar 

  194. Zhao Q, Wu BL (2012) Acta Pharmacol Sin 33:324

    CAS  Google Scholar 

  195. Katritch V, Cherezov V, Stevens RC (2013) Annu Rev Pharmacol Toxicol 53:531

    Google Scholar 

  196. Kobilka B, Schertler GFX (2008) Trends Pharmacol Sci 29:79

    CAS  Google Scholar 

  197. Tapaneeyakorn S, Goddard AD, Oates J, Willis CL, Watts A (2011) Biochim Biophys Acta 1808:1462

    CAS  Google Scholar 

  198. Ahuja S, Hornak V, Yan ECY, Syrett N, Goncalves JA, Hirshfeld A, Ziliox M, Sakmar TP, Sheves M, Reeves PJ, Smith SO, Eilers M (2009) Nat Struct Mol Biol 16:168

    CAS  Google Scholar 

  199. Park SH, Prytulla S, De Angelis AA, Brown JM, Kiefer H, Opella SJ (2006) J Am Chem Soc 128:7402

    CAS  Google Scholar 

  200. Goncalves JA, South K, Ahuja S, Zaitseva E, Opefi CA, Eilers M, Vogel R, Reeves PJ, Smith SO (2010) Proc Natl Acad Sci USA 107:19861

    CAS  Google Scholar 

  201. Struts AV, Salgado GF, Martinez-Mayorga K, Brown MF (2011) Nat Struct Mol Biol 18:392

    CAS  Google Scholar 

  202. Mertz B, Struts AV, Feller SE, Brown MF (2012) Biochim Biophys Acta 1818:241

    CAS  Google Scholar 

  203. Overhauser AW (1953) Phys Rev 92:411

    CAS  Google Scholar 

  204. Carver TR, Slichter CP (1953) Phys Rev 92:212

    CAS  Google Scholar 

  205. Carver TR, Slichter CP (1956) Phys Rev 102:975

    CAS  Google Scholar 

  206. Hu KN, Debelouchina GT, Smith AA, Griffin RG (2011) J Chem Phys 134:125105

    Google Scholar 

  207. Smith AA, Corzilius B, Barnes AB, Maly T, Griffin RG (2012) J Chem Phys 136:015101

    Google Scholar 

  208. Wind RA, Duijvestijn MJ, Vanderlugt C, Manenschijn A, Vriend J (1985) Prog Nucl Magn Reson Spectrosc 17:33

    CAS  Google Scholar 

  209. Wollan DS (1976) Phys Rev B 13:3671

    CAS  Google Scholar 

  210. Maly T, Debelouchina GT, Bajaj VS, Hu KN, Joo CG, Mak-Jurkauskas ML, Sirigiri JR, van der Wel PCA, Herzfeld J, Temkin RJ, Griffin RG (2008) J Chem Phys 128:052211

    Google Scholar 

  211. Felch KL, Danly BG, Jory HR, Kreischer KE, Lawson W, Levush B, Temkin RJ (1999) Proc IEEE 87:752

    Google Scholar 

  212. Becerra LR, Gerfen GJ, Temkin RJ, Singel DJ, Griffin RG (1993) Phys Rev Lett 71:3561

    CAS  Google Scholar 

  213. Becerra LR, Gerfen GJ, Bellew BF, Bryant JA, Hall DA, Inati SJ, Weber RT, Un S, Prisner TF, McDermott AE, Fishbein KW, Kreischer KE, Temkin RJ, Singel DJ, Griffin RG (1995) J Magn Reson Ser A 117:28

    CAS  Google Scholar 

  214. Haze O, Corzilius B, Smith AA, Griffin RG, Swager TM (2012) J Am Chem Soc 134:14287

    CAS  Google Scholar 

  215. Hu KN, Yu HH, Swager TM, Griffin RG (2004) J Am Chem Soc 126:10844

    CAS  Google Scholar 

  216. Song CS, Hu KN, Joo CG, Swager TM, Griffin RG (2006) J Am Chem Soc 128:11385

    CAS  Google Scholar 

  217. Matsuki Y, Maly T, Ouari O, Karoui H, Le Moigne F, Rizzato E, Lyubenova S, Herzfeld J, Prisner T, Tordo P, Griffin RG (2009) Angew Chem Int Ed Engl 48:4996

    CAS  Google Scholar 

  218. Matsuki Y, Takahashi H, Ueda K, Idehara T, Ogawa I, Toda M, Akutsu H, Fujiwara T (2010) Phys Chem Chem Phys 12:5799

    CAS  Google Scholar 

  219. Hall DA, Maus DC, Gerfen GJ, Inati SJ, Becerra LR, Dahlquist FW, Griffin RG (1997) Science 276:930

    CAS  Google Scholar 

  220. Rosay M, Zeri AC, Astrof NS, Opella SJ, Herzfeld J, Griffin RG (2001) J Am Chem Soc 123:1010

    CAS  Google Scholar 

  221. vanderWel PCA, Hu KN, Lewandowski J, Griffin RG (2006) J Am Chem Soc 128:10840

    CAS  Google Scholar 

  222. Bajaj VS, Mak-Jurkauskas ML, Belenky M, Herzfeld J, Griffin RG (2010) J Magn Reson 202:9

    CAS  Google Scholar 

  223. Akbey U, Linden AH, Oschkinat H (2012) Appl Magn Reson 43:81

    CAS  Google Scholar 

  224. Barnes AB, Corzilius B, Mak-Jurkauskas ML, Andreas LB, Bajaj VS, Matsuki Y, Belenky ML, Lugtenburg J, Sirigiri JR, Temkin RJ, Herzfeld J, Griffin RG (2010) Phys Chem Chem Phys 12: 5861

    CAS  Google Scholar 

  225. Lange S, Linden AH, Akbey Ü, Trent Franks W, Loening NM, Rossum B-J, Oschkinat H (2012) J Magn Reson 216:209

    CAS  Google Scholar 

  226. Debelouchina GT, Bayro MJ, van der Wel PCA, Caporini MA, Barnes AB, Rosay M, Maas WE, Griffin RG (2010) Phys Chem Chem Phys 12:5911

    CAS  Google Scholar 

  227. Bayro MJ, Debelouchina GT, Eddy MT, Birkett NR, MacPhee CE, Rosay M, Maas WE, Dobson CM, Griffin RG (2011) J Am Chem Soc 133:13967

    CAS  Google Scholar 

  228. Sergeyev IV, Day LA, Goldbourt A, McDermott AE (2011) J Am Chem Soc 133:20208

    CAS  Google Scholar 

  229. Reggie L, Lopez JJ, Collinson I, Glaubitz C, Lorch M (2011) J Am Chem Soc 133:19084

    CAS  Google Scholar 

  230. Linden AH, Lange S, Franks WT, Akbey Ü, Specker E, van Rossum B-J, Oschkinat H (2011) J Am Chem Soc 133:19266

    CAS  Google Scholar 

  231. Krabben L, van Rossurn BJ, Jehle S, Bocharov E, Lyukmanova EN, Schulga AA, Arseniev A, Hucho F, Oschkinat H (2009) J Mol Biol 390:662

    CAS  Google Scholar 

  232. Jacso T, Franks WT, Rose H, Fink U, Broecker J, Keller S, Oschkinat H, Reif B (2012) Angew Chem Int Ed 51:432

    CAS  Google Scholar 

  233. Renault M, Pawsey S, Bos MP, Koers EJ, Nand D, Tommassen-van Boxtel R, Rosay M, Tommassen J, Maas WE, Baldus M (2012) Angew Chem Int Ed 51:2998

    CAS  Google Scholar 

  234. Maly T, Cui DT, Griffin RG, Miller AF (2012) J Phys Chem B 116:7055

    CAS  Google Scholar 

  235. Corzilius B, Smith AA, Barnes AB, Luchinat C, Bertini I, Griffin RG (2011) J Am Chem Soc 133:5648

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Henrike Heise .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2013 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Müller, H., Etzkorn, M., Heise, H. (2013). Solid-State NMR Spectroscopy of Proteins. In: Heise, H., Matthews, S. (eds) Modern NMR Methodology. Topics in Current Chemistry, vol 335. Springer, Berlin, Heidelberg. https://doi.org/10.1007/128_2012_417

Download citation

Publish with us

Policies and ethics