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RESEARCH ARTICLE
Contents Vol 73(3)

A Theoretical Assessment of the Structure Determination of Multi-Span Membrane Proteins by Oriented Sample Solid-State NMR Spectroscopy

Daniel K. Weber https://orcid.org/0000-0001-8400-767X A C and Gianluigi Veglia A B
+ Author Affiliations
- Author Affiliations

A Department of Biochemistry, Molecular Biology, and Biophysics, University of Minnesota, Minneapolis, MN 55455, USA.

B Department of Chemistry, University of Minnesota, Minneapolis, MN 55455, USA.

C Corresponding author. Email: dweber@umn.edu

Australian Journal of Chemistry 73(3) 246-251 https://doi.org/10.1071/CH19307
Submitted: 6 July 2019  Accepted: 17 August 2019   Published: 20 September 2019

Abstract

Oriented sample solid-state NMR (OS-ssNMR) spectroscopy allows the direct determination of the structure and topology of membrane proteins reconstituted into aligned lipid bilayers. Although OS-ssNMR theoretically has no upper size limit, its application to multi-span membrane proteins has not been established because most studies have been restricted to single- or dual-span proteins and peptides. Here, we present a critical assessment of the application of this method to multi-span membrane proteins. We used molecular dynamics simulations to back-calculate [15N-1H] separated local field (SLF) spectra from a G protein-coupled receptor (GPCR) and show that fully resolved spectra can be obtained theoretically for a multi-span membrane protein with currently achievable resonance linewidths.


References

[1]  C. Chipot, F. Dehez, J. R. Schnell, N. Zitzmann, E. Pebay-Peyroula, L. J. Catoire, B. Miroux, E. R. S. Kunji, G. Veglia, T. A. Cross, P. Schanda, Chem. Rev. 2018, 118, 3559.
         | Crossref | GoogleScholarGoogle Scholar | 29488756PubMed |

[2]  V. Ladizhansky, Biochim. Biophys. Acta 2017, 1865, 1577.
         | Crossref | GoogleScholarGoogle Scholar |

[3]  J. Radoicic, G. J. Lu, S. J. Opella, Q. Rev. Biophys. 2014, 47, 249.
         | Crossref | GoogleScholarGoogle Scholar | 25032938PubMed |

[4]  P. C. A. van der Wel, Emerg. Top. Life Sci. 2018, 2, 57.
         | Crossref | GoogleScholarGoogle Scholar |

[5]  B. J. Wylie, H. Q. Do, C. G. Borcik, E. P. Hardy, Mol. Phys. 2016, 114, 3598.
         | Crossref | GoogleScholarGoogle Scholar |

[6]  S. J. Opella, Biomed. Spectrosc. Imaging 2014, 3, 81.
         | Crossref | GoogleScholarGoogle Scholar | 26069880PubMed |

[7]  C. R. Sanders, G. C. Landis, Biochemistry 1995, 34, 4030.
         | Crossref | GoogleScholarGoogle Scholar | 7696269PubMed |

[8]  S. H. Park, S. Berkamp, G. A. Cook, M. K. Chan, H. Viadiu, S. J. Opella, Biochemistry 2011, 50, 8983.
         | Crossref | GoogleScholarGoogle Scholar | 21936505PubMed |

[9]  J. Radoicic, S. H. Park, S. J. Opella, Biophys. J. 2018, 115, 22.
         | Crossref | GoogleScholarGoogle Scholar | 29914645PubMed |

[10]  H. Saitô, I. Ando, A. Ramamoorthy, Prog. Nucl. Magn. Reson. Spectrosc. 2010, 57, 181.
         | Crossref | GoogleScholarGoogle Scholar | 20633363PubMed |

[11]  B. A. Cornell, F. Separovic, A. J. Baldassi, R. Smith, Biophys. J. 1988, 53, 67.
         | Crossref | GoogleScholarGoogle Scholar | 19431717PubMed |

[12]  B. A. Cornell, L. E. Weir, F. Separovic, Eur. Biophys. J. 1988, 16, 113.
         | Crossref | GoogleScholarGoogle Scholar | 2463153PubMed |

[13]  R. Smith, D. E. Thomas, F. Separovic, A. R. Atkins, B. A. Cornell, Biophys. J. 1989, 56, 307.
         | Crossref | GoogleScholarGoogle Scholar | 2476189PubMed |

[14]  R. Ketchem, W. Hu, T. Cross, Science 1993, 261, 1457.
         | Crossref | GoogleScholarGoogle Scholar | 7690158PubMed |

[15]  R. R. Ketchem, B. Roux, T. A. Cross, Structure 1997, 5, 1655.
         | Crossref | GoogleScholarGoogle Scholar |

[16]  C. H. Wu, A. Ramamoorthy, S. J. Opella, J. Magn. Reson. A 1994, 109, 270.
         | Crossref | GoogleScholarGoogle Scholar |

[17]  A. A. Nevzorov, S. J. Opella, J. Magn. Reson. 2003, 164, 182.
         | Crossref | GoogleScholarGoogle Scholar | 12932472PubMed |

[18]  A. A. Nevzorov, S. J. Opella, J. Magn. Reson. 2007, 185, 59.
         | Crossref | GoogleScholarGoogle Scholar | 17074522PubMed |

[19]  F. M. Marassi, J. J. Gesell, A. P. Valente, Y. Kim, M. Oblatt-Montal, M. Montal, S. J. Opella, J. Biomol. NMR 1999, 14, 141.
         | Crossref | GoogleScholarGoogle Scholar | 10427741PubMed |

[20]  K. R. Mote, T. Gopinath, N. J. Traaseth, J. Kitchen, P. L. Gor’kov, W. W. Brey, G. Veglia, J. Biomol. NMR 2011, 51, 339.
         | Crossref | GoogleScholarGoogle Scholar | 21976256PubMed |

[21]  T. Gopinath, K. R. Mote, G. Veglia, Prog. Nucl. Magn. Reson. Spectrosc. 2013, 75, 50.
         | Crossref | GoogleScholarGoogle Scholar | 24160761PubMed |

[22]  T. Gopinath, G. Veglia, J. Am. Chem. Soc. 2009, 131, 5754.
         | Crossref | GoogleScholarGoogle Scholar | 19351170PubMed |

[23]  T. Gopinath, K. R. Mote, G. Veglia, J. Biomol. NMR 2015, 62, 53.
         | Crossref | GoogleScholarGoogle Scholar | 25749871PubMed |

[24]  P. L. Gor’kov, E. Y. Chekmenev, C. Li, M. Cotten, J. J. Buffy, N. J. Traaseth, G. Veglia, W. W. Brey, J. Magn. Reson. 2007, 185, 77.
         | Crossref | GoogleScholarGoogle Scholar | 17174130PubMed |

[25]  S. Wang, T. Gopinath, G. Veglia, Methods 2018, 138–139, 54.
         | Crossref | GoogleScholarGoogle Scholar | 29274874PubMed |

[26]  A. De Simone, K. R. Mote, G. Veglia, Biophys. J. 2014, 106, 2566.
         | Crossref | GoogleScholarGoogle Scholar | 24940774PubMed |

[27]  J. K. Denny, J. Wang, T. A. Cross, J. R. Quine, J. Magn. Reson. 2001, 152, 217.
         | Crossref | GoogleScholarGoogle Scholar | 11567575PubMed |

[28]  J. Lapin, A. A. Nevzorov, J. Magn. Reson. 2018, 293, 104.
         | Crossref | GoogleScholarGoogle Scholar | 29920407PubMed |

[29]  J. Lapin, A. A. Nevzorov, J. Biomol. NMR 2019, 73, 229.
         | Crossref | GoogleScholarGoogle Scholar | 31076969PubMed |

[30]  F. M. Marassi, S. J. Opella, J. Magn. Reson. 2000, 144, 150.
         | Crossref | GoogleScholarGoogle Scholar | 10783285PubMed |

[31]  A. Mascioni, B. L. Eggimann, G. Veglia, Chem. Phys. Lipids 2004, 132, 133.
         | Crossref | GoogleScholarGoogle Scholar | 15530454PubMed |

[32]  A. A. Nevzorov, S. J. Opella, J. Magn. Reson. 2003, 160, 33.
         | Crossref | GoogleScholarGoogle Scholar | 12565046PubMed |

[33]  L. Shi, N. J. Traaseth, R. Verardi, A. Cembran, J. Gao, G. Veglia, J. Biomol. NMR 2009, 44, 195.
         | Crossref | GoogleScholarGoogle Scholar | 19597943PubMed |

[34]  Z. Gan, I. Hung, X. Wang, J. Paulino, G. Wu, I. M. Litvak, P. L. Gor’kov, W. W. Brey, P. Lendi, J. L. Schiano, M. D. Bird, I. R. Dixon, J. Toth, G. S. Boebinger, T. A. Cross, J. Magn. Reson. 2017, 284, 125.
         | Crossref | GoogleScholarGoogle Scholar | 28890288PubMed |

[35]  B. Bechinger, eMagRes 2018, 7, 25.
         | Crossref | GoogleScholarGoogle Scholar |

[36]  E. Salnikov, M. Rosay, S. Pawsey, O. Ouari, P. Tordo, B. Bechinger, J. Am. Chem. Soc. 2010, 132, 5940.
         | Crossref | GoogleScholarGoogle Scholar | 20392100PubMed |

[37]  E. S. Salnikov, S. Abel, G. Karthikeyan, H. Karoui, F. Aussenac, P. Tordo, B. Bechinger, O. Ouari, ChemPhysChem 2017, 18, 2103.
         | Crossref | GoogleScholarGoogle Scholar | 28574169PubMed |

[38]  E. S. Salnikov, H. Sarrouj, C. Reiter, C. Aisenbrey, A. Purea, F. Aussenac, O. Ouari, P. Tordo, I. Fedotenko, F. Engelke, B. Bechinger, J. Phys. Chem. B 2015, 119, 14574.
         | Crossref | GoogleScholarGoogle Scholar | 26487390PubMed |

[39]  S. J. Opella, F. M. Marassi, J. J. Gesell, A. P. Valente, Y. Kim, M. Oblatt-Montal, M. Montal, Nat. Struct. Biol. 1999, 6, 374.
         | Crossref | GoogleScholarGoogle Scholar | 10201407PubMed |

[40]  A. C. Zeri, M. F. Mesleh, A. A. Nevzorov, S. J. Opella, Proc. Natl. Acad. Sci. USA 2003, 100, 6458.
         | Crossref | GoogleScholarGoogle Scholar | 12750469PubMed |

[41]  S. H. Park, A. A. De Angelis, A. A. Nevzorov, C. H. Wu, S. J. Opella, Biophys. J. 2006, 91, 3032.
         | Crossref | GoogleScholarGoogle Scholar | 16861273PubMed |

[42]  S. H. Park, A. A. Mrse, A. A. Nevzorov, M. F. Mesleh, M. Oblatt-Montal, M. Montal, S. J. Opella, J. Mol. Biol. 2003, 333, 409.
         | Crossref | GoogleScholarGoogle Scholar | 14529626PubMed |

[43]  B. B. Das, H. J. Nothnagel, G. J. Lu, W. S. Son, Y. Tian, F. M. Marassi, S. J. Opella, J. Am. Chem. Soc. 2012, 134, 2047.
         | Crossref | GoogleScholarGoogle Scholar | 22217388PubMed |

[44]  A. A. De Angelis, S. C. Howell, A. A. Nevzorov, S. J. Opella, J. Am. Chem. Soc. 2006, 128, 12256.
         | Crossref | GoogleScholarGoogle Scholar | 16967977PubMed |

[45]  Y. Tian, G. J. Lu, F. M. Marassi, S. J. Opella, J. Biomol. NMR 2014, 60, 67.
         | Crossref | GoogleScholarGoogle Scholar | 25103921PubMed |

[46]  M. Sharma, M. Yi, H. Dong, H. Qin, E. Peterson, D. D. Busath, H. X. Zhou, T. A. Cross, Science 2010, 330, 509.
         | Crossref | GoogleScholarGoogle Scholar | 20966252PubMed |

[47]  R. Mahalakshmi, F. M. Marassi, Biochemistry 2008, 47, 6531.
         | Crossref | GoogleScholarGoogle Scholar | 18512961PubMed |

[48]  U. H. N. Dürr, L. Waskell, A. Ramamoorthy, Biochim. Biophys. Acta 2007, 1768, 3235.
         | Crossref | GoogleScholarGoogle Scholar |

[49]  N. J. Traaseth, L. Shi, R. Verardi, D. G. Mullen, G. Barany, G. Veglia, Proc. Natl. Acad. Sci. USA 2009, 106, 10165.
         | Crossref | GoogleScholarGoogle Scholar | 19509339PubMed |

[50]  R. Verardi, L. Shi, N. J. Traaseth, N. Walsh, G. Veglia, Proc. Natl. Acad. Sci. USA 2011, 108, 9101.
         | Crossref | GoogleScholarGoogle Scholar | 21576492PubMed |

[51]  N. Das, J. Dai, I. Hung, M. Rajagopalan, H.-X. Zhou, T. A. Cross, Proc. Natl. Acad. Sci. USA 2015, 112, E119.
         | Crossref | GoogleScholarGoogle Scholar | 25548160PubMed |

[52]  C. Aisenbrey, E. S. Salnikov, B. Bechinger, J. Membr. Biol. 2019, in press
         | Crossref | GoogleScholarGoogle Scholar | 31187155PubMed |

[53]  E. S. Salnikov, C. Aisenbrey, G. M. Anantharamaiah, B. Bechinger, Chem. Phys. Lipids 2019, 219, 58.
         | Crossref | GoogleScholarGoogle Scholar | 30711343PubMed |

[54]  C. Aisenbrey, P. Kemayo-Koumkoua, E. S. Salnikov, E. Glattard, B. Bechinger, Biochemistry 2019, 58, 2782.
         | Crossref | GoogleScholarGoogle Scholar | 31120242PubMed |

[55]  M. Michalek, E. S. Salnikov, B. Bechinger, Biophys. J. 2013, 105, 699.
         | Crossref | GoogleScholarGoogle Scholar | 23931318PubMed |

[56]  C. Douat, C. Aisenbrey, S. Antunes, M. Decossas, O. Lambert, B. Bechinger, A. Kichler, G. Guichard, Angew. Chem. Int. Ed. 2015, 54, 11133.
         | Crossref | GoogleScholarGoogle Scholar |

[57]  J. Wolf, C. Aisenbrey, N. Harmouche, J. Raya, P. Bertani, N. Voievoda, R. Süss, B. Bechinger, Biophys. J. 2017, 113, 1290.
         | Crossref | GoogleScholarGoogle Scholar | 28734478PubMed |

[58]  A. Gayen, M. Leninger, N. J. Traaseth, Nat. Chem. Biol. 2016, 12, 141.
         | Crossref | GoogleScholarGoogle Scholar | 26751516PubMed |

[59]  S. G. F. Rasmussen, H. J. Choi, J. J. Fung, E. Pardon, P. Casarosa, P. S. Chae, B. T. Devree, D. M. Rosenbaum, F. S. Thian, T. S. Kobilka, A. Schnapp, I. Konetzki, R. K. Sunahara, S. H. Gellman, A. Pautsch, J. Steyaert, W. I. Weis, B. K. Kobilka, Nature 2011, 469, 175.
         | Crossref | GoogleScholarGoogle Scholar |

[60]  D. K. Weber, M. A. Sani, M. T. Downton, F. Separovic, F. R. Keene, J. G. Collins, J. Am. Chem. Soc. 2016, 138, 15267.
         | Crossref | GoogleScholarGoogle Scholar | 27786471PubMed |

[61]  J. Wang, J. Denny, C. Tian, S. Kim, Y. Mo, F. Kovacs, Z. Song, K. Nishimura, Z. Gan, R. Fu, J. R. Quine, T. A. Cross, J. Magn. Reson. 2000, 144, 162.
         | Crossref | GoogleScholarGoogle Scholar | 10783287PubMed |

[62]  D. T. Murray, I. Hung, T. A. Cross, J. Magn. Reson. 2014, 240, 34.
         | Crossref | GoogleScholarGoogle Scholar | 24509383PubMed |

[63]  E. Salnikov, P. Bertani, J. Raap, B. Bechinger, J. Biomol. NMR 2009, 45, 373.
         | Crossref | GoogleScholarGoogle Scholar | 19823773PubMed |

[64]  P. Bertani, J. Raya, B. Bechinger, Solid State Nucl. Magn. Reson. 2014, 61–62, 15.
         | Crossref | GoogleScholarGoogle Scholar | 24746715PubMed |

[65]  A. Holt, L. Rougier, V. Réat, F. Jolibois, O. Saurel, J. Czaplicki, J. Antoinette Killian, A. Milon, Biophys. J. 2010, 98, 1864.
         | Crossref | GoogleScholarGoogle Scholar | 20441750PubMed |

[66]  F. Separovic, R. Pax, B. Cornell, Mol. Phys. 1993, 78, 357.
         | Crossref | GoogleScholarGoogle Scholar |

[67]  S. Esteban-Martín, E. Strandberg, G. Fuertes, A. S. Ulrich, J. Salgado, Biophys. J. 2009, 96, 3233.
         | Crossref | GoogleScholarGoogle Scholar | 19383467PubMed |

[68]  T. R. Molugu, X. Xu, A. Leftin, S. Lope-Piedrafita, G. V. Martinez, H. I. Petrache, M. F. Brown, in Modern Magnetic Resonance (Ed. G. A. Webb) 2018, pp. 581–603 (Springer International Publishing: Cham).

[69]  W. Humphrey, A. Dalke, K. Schulten, J. Mol. Graph. 1996, 14, 33.
         | Crossref | GoogleScholarGoogle Scholar | 8744570PubMed |

[70]  W. Lee, M. Tonelli, J. L. Markley, Bioinformatics 2015, 31, 1325.
         | Crossref | GoogleScholarGoogle Scholar | 25505092PubMed |

[71]  L. Shi, A. Cembran, J. Gao, G. Veglia, Biophys. J. 2009, 96, 3648.
         | Crossref | GoogleScholarGoogle Scholar | 19413970PubMed |

[72]  S. Jo, T. Kim, V. G. Iyer, W. Im, J. Comput. Chem. 2008, 29, 1859.
         | Crossref | GoogleScholarGoogle Scholar | 18351591PubMed |

[73]  E. L. Wu, X. Cheng, S. Jo, H. Rui, K. C. Song, E. M. Davila-Contreras, Y. Qi, J. Lee, V. Monje-Galvan, R. M. Venable, J. B. Klauda, W. Im, J. Comput. Chem. 2014, 35, 1997.
         | Crossref | GoogleScholarGoogle Scholar | 25130509PubMed |

[74]  J. Huang, A. D. MacKerell, J. Comput. Chem. 2013, 34, 2135.
         | Crossref | GoogleScholarGoogle Scholar | 23832629PubMed |

[75]  J. B. Klauda, R. M. Venable, J. A. Freites, J. W. O’Connor, D. J. Tobias, C. Mondragon-Ramirez, I. Vorobyov, A. D. MacKerell, R. W. Pastor, J. Phys. Chem. B 2010, 114, 7830.
         | Crossref | GoogleScholarGoogle Scholar | 20496934PubMed |

[76]  J. C. Phillips, R. Braun, W. Wang, J. Gumbart, E. Tajkhorshid, E. Villa, C. Chipot, R. D. Skeel, L. Kalé, K. Schulten, J. Comput. Chem. 2005, 26, 1781.
         | Crossref | GoogleScholarGoogle Scholar | 16222654PubMed |

[77]  K. R. Mote, T. Gopinath, G. Veglia, J. Biomol. NMR 2013, 57, 91.
         | Crossref | GoogleScholarGoogle Scholar | 23963722PubMed |

[78]  A. Mascioni, C. Karim, G. Barany, D. D. Thomas, G. Veglia, Biochemistry 2002, 41, 475.
         | Crossref | GoogleScholarGoogle Scholar | 11781085PubMed |

[79]  D. M. Rosenbaum, C. Zhang, J. A. Lyons, R. Holl, D. Aragao, D. H. Arlow, S. G. F. Rasmussen, H. J. Choi, B. T. Devree, R. K. Sunahara, P. S. Chae, S. H. Gellman, R. O. Dror, D. E. Shaw, W. I. Weis, M. Caffrey, P. Gmeiner, B. K. Kobilka, Nature 2011, 469, 236.
         | Crossref | GoogleScholarGoogle Scholar | 21228876PubMed |

[80]  R. O. Dror, D. H. Arlow, P. Maragakis, T. J. Mildorf, A. C. Pan, H. Xu, D. W. Borhani, D. E. Shaw, Proc. Natl. Acad. Sci. USA 2011, 108, 18684.
         | Crossref | GoogleScholarGoogle Scholar | 22031696PubMed |

[81]  J. J. Helmus, C. P. Jaroniec, J. Biomol. NMR 2013, 55, 355.
         | Crossref | GoogleScholarGoogle Scholar | 23456039PubMed |

[82]  A. Itkin, E. S. Salnikov, C. Aisenbrey, J. Raya, E. Glattard, V. Raussens, J.-M. Ruysschaert, B. Bechinger, ACS Omega 2017, 2, 6525.
         | Crossref | GoogleScholarGoogle Scholar | 31457253PubMed |

[83]  J. R. Quine, S. Achuthan, T. Asbury, R. Bertram, M. S. Chapman, J. Hu, T. A. Cross, J. Magn. Reson. 2006, 179, 190.
         | Crossref | GoogleScholarGoogle Scholar | 16413215PubMed |

[84]  D. P. Staus, R. T. Strachan, A. Manglik, B. Pani, A. W. Kahsai, T. H. Kim, L. M. Wingler, S. Ahn, A. Chatterjee, A. Masoudi, A. C. Kruse, E. Pardon, J. Steyaert, W. I. Weis, R. S. Prosser, B. K. Kobilka, T. Costa, R. J. Lefkowitz, Nature 2016, 535, 448.
         | Crossref | GoogleScholarGoogle Scholar | 27409812PubMed |

[85]  D. Lacabanne, B. H. Meier, A. Böckmann, J. Biomol. NMR 2018, 71, 141.
         | Crossref | GoogleScholarGoogle Scholar | 29197975PubMed |

[86]  R. Verardi, N. J. Traaseth, L. R. Masterson, V. V. Vostrikov, G. Veglia, in Isotope Labeling in Biomolecular NMR (Ed. H. S. Atreya) 2012, Vol. 992, pp. 35–62 (Springer Netherlands: Dordrecht).

[87]  R. S. Prosser, S. A. Hunt, J. A. DiNatale, R. R. Vold, J. Am. Chem. Soc. 1996, 118, 269.
         | Crossref | GoogleScholarGoogle Scholar |

[88]  S. H. Park, A. A. Mrse, A. A. Nevzorov, A. A. De Angelis, S. J. Opella, J. Magn. Reson. 2006, 178, 162.
         | Crossref | GoogleScholarGoogle Scholar | 16213759PubMed |

[89]  D. M. Tesch, Z. Pourmoazzen, E. O. Awosanya, A. A. Nevzorov, Appl. Magn. Reson. 2018, 49, 1335.
         | Crossref | GoogleScholarGoogle Scholar |

[90]  J. J. Buffy, N. J. Traaseth, A. Mascioni, P. L. Gor’kov, E. Y. Chekmenev, W. W. Brey, G. Veglia, Biochemistry 2006, 45, 10939.
         | Crossref | GoogleScholarGoogle Scholar | 16953579PubMed |

[91]  S. Kim, T. A. Cross, Biophys. J. 2002, 83, 2084.
         | Crossref | GoogleScholarGoogle Scholar | 12324426PubMed |

[92]  T. Ravula, N. Z. Hardin, S. K. Ramadugu, S. J. Cox, A. Ramamoorthy, Angew. Chem. Int. Ed. 2018, 57, 1342.
         | Crossref | GoogleScholarGoogle Scholar |

[93]  T. Ravula, N. Z. Hardin, A. Ramamoorthy, Chem. Phys. Lipids 2019, 219, 45.
         | Crossref | GoogleScholarGoogle Scholar | 30707909PubMed |

[94]  N. Harmouche, B. Bechinger, Biophys. J. 2018, 115, 1033.
         | Crossref | GoogleScholarGoogle Scholar | 30195937PubMed |