The atomic structure of the HIV-1 gp41 transmembrane domain and its connection to the immunogenic membrane-proximal external region

Journal of Biological Chemistry

Volumn 290, Issue 21, 2015, Pages 12999-13015

  Apellániz, Beatriz ^a   Rujas, Edurne ^a,b   Serrano, Soraya ^c   Morante, Koldo ^b   Tsumoto, Kouhei ^b   Caaveiro, Jose M M ^b   Jiménez, M Ángeles ^c,d   Nieva, José L ^a,e  

^a CSIC UPV Unidad de Biofisica UBF   (Spain)

^b UNIVERSITY OF TOKYO   (Japan)

^c CSIC   (Spain)

^d INSTITUTO DE QUÍMICA FÍSICA ROCASOLANO   (Spain)

^e UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATION ANALYSIS; CELL MEMBRANES; PEPTIDES; VACCINES;

ANTIBODY BINDING; C-TERMINAL SEGMENTS; ENVELOPE GLYCOPROTEINS; IMMUNE RECOGNITION; ISOTHERMAL TITRATION CALORIMETRY; MOLECULAR DYNAMICS SIMULATIONS; TRANS-MEMBRANE DOMAINS; TRANSMEMBRANE DOMAIN;

MOLECULAR DYNAMICS;

GLYCOPROTEIN GP 41; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY; PEPTIDE FRAGMENT;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ANTIGEN BINDING; ANTIGEN RECOGNITION; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ENERGY TRANSFER; HUMAN; HUMAN CELL; HUMORAL IMMUNITY; ISOTHERMAL TITRATION CALORIMETRY; MEMBRANE PROXIMAL EXTERNAL REGION; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN STRUCTURE; TRANSMEMBRANE DOMAIN; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; CIRCULAR DICHROISM; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOLOGY; MEMBRANE FUSION; METABOLISM; MOLECULAR GENETICS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PHYSIOLOGY; PROTEIN SECONDARY STRUCTURE; RABBIT; VIROLOGY; VIRUS ENTRY; X RAY CRYSTALLOGRAPHY;

HUMAN IMMUNODEFICIENCY VIRUS 1; ORYCTOLAGUS CUNICULUS;

AMINO ACID SEQUENCE; ANIMALS; CIRCULAR DICHROISM; CRYSTALLOGRAPHY, X-RAY; HIV ANTIBODIES; HIV ENVELOPE PROTEIN GP41; HIV INFECTIONS; HIV-1; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; MEMBRANE FUSION; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; PROTEIN STRUCTURE, SECONDARY; RABBITS; VIRUS INTERNALIZATION;

EID: 84930011701     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.644351     Document Type: Article

References (78)

1. Wyatt, R., and Sodroski, J. (1998) The HIV-1 envelope glycoproteins: fusogens, antigens, and immunogens. Science 280, 1884-1888
2. Melikyan, G. B. (2011) Membrane fusion mediated by human immunodeficiency virus envelope glycoprotein. Curr. Top. Membr. 68, 81-106
3. Blumenthal, R., Durell, S., and Viard, M. (2012) HIV entry and envelope glycoprotein-mediated fusion. J. Biol. Chem. 287, 40841-40849
4. Eckert, D. M., and Kim, P. S. (2001) Mechanisms of viral membrane fusion and its inhibition. Annu. Rev. Biochem. 70, 777-810
5. Julien, J. P., Cupo, A., Sok, D., Stanfield, R. L., Lyumkis, D., Deller, M. C., Klasse, P. J., Burton, D. R., Sanders, R. W., Moore, J. P., Ward, A. B., and Wilson, I. A. (2013) Crystal structure of a soluble cleaved HIV-1 envelope trimer. Science 342, 1477-1483
6. Lyumkis, D., Julien, J. P., de Val, N., Cupo, A., Potter, C. S., Klasse, P. J., Burton, D. R., Sanders, R. W., Moore, J. P., Carragher, B., Wilson, I. A., and Ward, A. B. (2013) Cryo-EM structure of a fully glycosylated soluble cleaved HIV-1 envelope trimer. Science 342, 1484-1490
7. Pancera, M., Zhou, T., Druz, A., Georgiev, I. S., Soto, C., Gorman, J., Huang, J., Acharya, P., Chuang, G. Y., Ofek, G., Stewart-Jones, G. B., Stuckey, J., Bailer, R. T., Joyce, M. G., Louder, M. K., et al. (2014) Structure and immune recognition of trimeric pre-fusion HIV-1 Env. Nature 514, 455-461
8. Haffar, O. K., Dowbenko, D. J., and Berman, P. W. (1988) Topogenic analysis of the human immunodeficiency virus type 1 envelope glycoprotein, gp160, in microsomal membranes. J. Cell Biol. 107, 1677-1687
9. Helseth, E., Olshevsky, U., Gabuzda, D., Ardman, B., Haseltine, W., and Sodroski, J. (1990) Changes in the transmembrane region of the human immunodeficiency virus type 1 gp41 envelope glycoprotein affect membrane fusion. J. Virol. 64, 6314-6318
10. Yue, L., Shang, L., and Hunter, E. (2009) Truncation of the membranespanning domain of human immunodeficiency virus type 1 envelope glycoprotein defines elements required for fusion, incorporation, and infectivity. J. Virol. 83, 11588-11598
11. Liu, S., Kondo, N., Long, Y., Xiao, D., Iwamoto, A., and Matsuda, Z. (2010) Membrane topology analysis of HIV-1 envelope glycoprotein gp41. Retrovirology 7, 100
12. Kim, J. H., Hartley, T. L., Curran, A. R., and Engelman, D. M. (2009) Molecular dynamics studies of the transmembrane domain of gp41 from HIV-1. Biochim. Biophys. Acta 1788, 1804-1812
13. Montero, M., Gulzar, N., Klaric, K. A., Donald, J. E., Lepik, C., Wu, S., Tsai, S., Julien, J. P., Hessell, A. J., Wang, S., Lu, S., Burton, D. R., Pai, E. F., Degrado, W. F., and Scott, J. K. (2012) Neutralizing epitopes in the mem-brane-proximal external region of HIV-1 gp41 are influenced by the transmembrane domain and the plasma membrane. J. Virol. 86, 2930-2941
14. Gangupomu, V. K., and Abrams, C. F. (2010) All-atom models of the membrane-spanning domain of HIV-1 gp41 from metadynamics. Biophys. J. 99, 3438-3444
15. Baker, M. K., Gangupomu, V. K., and Abrams, C. F. (2014) Characterization of the water defect at the HIV-1 gp41 membrane spanning domain in bilayers with and without cholesterol using molecular simulations. Biochim. Biophys. Acta 1838, 1396-1405
16. Owens, R. J., Burke, C., and Rose, J. K. (1994) Mutations in the membranespanning domain of the human immunodeficiency virus envelope glycoprotein that affect fusion activity. J. Virol. 68, 570-574
17. Miyauchi, K., Komano, J., Yokomaku, Y., Sugiura, W., Yamamoto, N., and Matsuda, Z. (2005) Role of the specific amino acid sequence of the mem-brane-spanning domain of human immunodeficiency virus type 1 in membrane fusion. J. Virol. 79, 4720-4729
18. Shang, L., Yue, L., and Hunter, E. (2008) Role of the membrane-spanning domain of human immunodeficiency virus type 1 envelope glycoprotein in cell-cell fusion and virus infection. J. Virol. 82, 5417-5428
19. Zwick, M. B. (2005) The membrane-proximal external region of HIV-1 gp41: a vaccine target worth exploring. AIDS 19, 1725-1737
20. Montero, M., van Houten, N. E., Wang, X., and Scott, J. K. (2008) The membrane-proximal external region of the human immunodeficiency virus type 1 envelope: dominant site of antibody neutralization and target for vaccine design. Microbiol. Mol. Biol. Rev. 72, 54-84
21. Kwong, P. D., and Mascola, J. R. (2012) Human antibodies that neutralize HIV-1: identification, structures, and B cell ontogenies. Immunity 37, 412-425
22. Cardoso, R. M., Brunel, F. M., Ferguson, S., Zwick, M., Burton, D. R., Dawson, P. E., and Wilson, I. A. (2007) Structural basis of enhanced binding of extended and helically constrained peptide epitopes of the broadly neutralizing HIV-1 antibody 4E10. J. Mol. Biol. 365, 1533-1544
23. Huang, J., Ofek, G., Laub, L., Louder, M. K., Doria-Rose, N. A., Longo, N. S., Imamichi, H., Bailer, R. T., Chakrabarti, B., Sharma, S. K., Alam, S. M., Wang, T., Yang, Y., Zhang, B., Migueles, S. A., et al. (2012) Broad and potent neutralization of HIV-1 by a gp41-specific human antibody. Nature 491, 406-412
24. Schibli, D. J., Montelaro, R. C., and Vogel, H. J. (2001) The membraneproximal tryptophan-rich region of the HIV glycoprotein, gp41, forms a well defined helix in dodecylphosphocholine micelles. Biochemistry 40, 9570-9578
25. Sáez-Cirión, A., Nir, S., Lorizate, M., Agirre, A., Cruz, A., Pérez-Gil, J., and Nieva, J. L. (2002) Sphingomyelin and cholesterol promote HIV-1 gp41 pretransmembrane sequence surface aggregation and membrane restructuring. J. Biol. Chem. 277, 21776-21785
26. Sun, Z. Y., Oh, K. J., Kim, M., Yu, J., Brusic, V., Song, L., Qiao, Z., Wang, J. H., Wagner, G., and Reinherz, E. L. (2008) HIV-1 broadly neutralizing antibody extracts its epitope from a kinked gp41 ectodomain region on the viral membrane. Immunity 28, 52-63
27. Huarte, N., Lorizate, M., Maeso, R., Kunert, R., Arranz, R., Valpuesta, J. M., and Nieva, J. L. (2008) The broadly neutralizing anti-human immunodeficiency virus type 1 4E10 monoclonal antibody is better adapted to mem-brane-bound epitope recognition and blocking than 2F5. J. Virol. 82, 8986-8996
28. Dennison, S. M., Stewart, S. M., Stempel, K. C., Liao, H. X., Haynes, B. F., and Alam, S. M. (2009) Stable docking of neutralizing human immunodeficiency virus type 1 gp41 membrane-proximal external region monoclonal antibodies 2F5 and 4E10 is dependent on the membrane immersion depth of their epitope regions. J. Virol. 83, 10211-10223
29. Reardon, P. N., Sage, H., Dennison, S. M., Martin, J. W., Donald, B. R., Alam, S. M., Haynes, B. F., and Spicer, L. D. (2014) Structure of an HIV-1-neutralizing antibody target, the lipid-bound gp41 envelope membrane proximal region trimer. Proc. Natl. Acad. Sci. U.S.A. 111, 1391-1396
30. Cohen, T., Cohen, S. J., Antonovsky, N., Cohen, I. R., and Shai, Y. (2010) HIV-1 gp41 and TCRα trans-membrane domains share a motif exploited by the HIV virus to modulate T-cell proliferation. PLoS Pathog. 6, e1001085
31. Ashkenazi, A., Faingold, O., and Shai, Y. (2013) HIV-1 fusion protein exerts complex immunosuppressive effects. Trends Biochem. Sci. 38, 345-349
32. Reuven, E. M., Ali, M., Rotem, E., Schwarzter, R., Gramatica, A., Futerman, A. H., and Shai, Y. (2014) The HIV-1 envelope transmembrane domain binds TLR2 through a distinct dimerization motif and inhibits TLR2-mediated responses. PLoS Pathog. 10, e1004248
33. Sun, Z. Y., Cheng, Y., Kim, M., Song, L., Choi, J., Kudahl, U. J., Brusic, V., Chowdhury, B., Yu, L., Seaman, M. S., Bellot, G., Shih, W. M., Wagner, G., and Reinherz, E. L. (2014) Disruption of helix-capping residues 671 and 674 reveals a role in HIV-1 entry for a specialized hinge segment of the membrane proximal external region of gp41. J. Mol. Biol. 426, 1095-1108
34. Serrano, S., Araujo, A., Apellániz, B., Bryson, S., Carravilla, P., de la Arada, I., Huarte, N., Rujas, E., Pai, E. F., Arrondo, J. L., Domene, C., Jiménez, M. A., and Nieva, J. L. (2014) Structure and immunogenicity of a peptide vaccine, including the complete HIV-1 gp41 2F5 epitope: implications for antibody recognition mechanism and immunogen design. J. Biol. Chem. 289, 6565-6580
35. Apellániz, B., Nir, S., and Nieva, J. L. (2009) Distinct mechanisms of lipid bilayer perturbation induced by peptides derived from the mem-brane-proximal external region of HIV-1 gp41. Biochemistry 48, 5320-5331
36. Apellániz, B., Rujas, E., Carravilla, P., Requejo-Isidro, J., Huarte, N., Domene, C., and Nieva, J. L. (2014) Cholesterol-dependent membrane fusion induced by the gp41 membrane-proximal external region-transmembrane domain connection suggests a mechanism for broad HIV-1 neutralization. J. Virol. 88, 13367-13377
37. Julien, J. P., Huarte, N., Maeso, R., Taneva, S. G., Cunningham, A., Nieva, J. L., and Pai, E. F. (2010) Ablation of the complementarity-determining region H3 apex of the anti-HIV-1 broadly neutralizing antibody 2F5 abrogates neutralizing capacity without affecting core epitope binding. J. Virol. 84, 4136-4147
38. Markley, J. L., Bax, A., Arata, Y., Hilbers, C. W., Kaptein, R., Sykes, B. D., Wright, P. E., and Wüthrich, K. (1998) Recommendations for the presentation of NMR structures of proteins and nucleic acids. J. Mol. Biol. 280, 933-952
39. Mirassou, Y., Santiveri, C. M., Perez de Vega, M. J., Gonzalez-Muniz, R., and Jimenez, M. A. (2009) Disulfide bonds versus TrpTrp pairs in irregular β-hairpins: NMR structure of vammin loop 3-derived peptides as a case study. Chembiochem 10, 902-910
40. Cornilescu, G., Delaglio, F., and Bax, A. (1999) Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J. Biomol. NMR 13, 289-302
41. Güntert, P., Mumenthaler, C., and Wüthrich, K. (1997) Torsion angle dynamics for NMR structure calculation with the new program DYANA. J. Mol. Biol. 273, 283-298
42. Güntert, P. (2004) Automated NMR structure calculation with CYANA. Methods Mol. Biol. 278, 353-378
43. Laskowski, R. A., Rullmannn, J. A., MacArthur, M. W., Kaptein, R., and Thornton, J. M. (1996) AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR 8, 477-486
44. Koradi, R., Billeter, M., and Wüthrich, K. (1996) MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graph. 14, 51-55
45. Guex, N., and Peitsch, M. C. (1997) SWISS-MODEL and the Swiss-Pdb-Viewer: an environment for comparative protein modeling. Electrophoresis 18, 2714-2723
46. Evans, P. (2006) Scaling and assessment of data quality. Acta Crystallogr.D Biol. Crystallogr. 62, 72-82
47. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674
48. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255
49. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501
50. Laskowski, R. A., MacArthur, M. W., Moss, D. S., and Thornton, J. M. (1993) PROCHECK-a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26, 283-291
51. Yethon, J. A., Epand, R. F., Leber, B., Epand, R. M., and Andrews, D. W. (2003) Interaction with a membrane surface triggers a reversible conformational change in Bax normally associated with induction of apoptosis. J. Biol. Chem. 278, 48935-48941
52. Dreesman, G. R., Sanchez, Y., Ionescu-Matiu, I., Sparrow, J. T., Six, H. R., Peterson, D. L., Hollinger, F. B., and Melnick, J. L. (1982) Antibody to hepatitis B surface antigen after a single inoculation of uncoupled synthetic HBsAg peptides. Nature 295, 158-160
53. Maeso, R., Huarte, N., Julien, J. P., Kunert, R., Pai, E. F., and Nieva, J. L. (2011) Interaction of anti-HIV type 1 antibody 2F5 with phospholipid bilayers and its relevance for the mechanism of virus neutralization. AIDS Res. Hum. Retroviruses 27, 863-876
54. Alving, C. R., Rao, M., Steers, N. J., Matyas, G. R., and Mayorov, A. V. (2012) Liposomes containing lipid A: an effective, safe, generic adjuvant system for synthetic vaccines. Expert Rev. Vaccines 11, 733-744
55. Suárez, T., Gallaher, W. R., Agirre, A., Goñi, F. M., and Nieva, J. L. (2000) Membrane interface-interacting sequences within the ectodomain of the human immunodeficiency virus type 1 envelope glycoprotein: putative role during viral fusion. J. Virol. 74, 8038-8047
56. Sáez-Cirión, A., Arrondo, J. L., Gómara, M. J., Lorizate, M., Iloro, I., Melikyan, G., and Nieva, J. L. (2003) Structural and functional roles of HIV-1 gp41 pretransmembrane sequence segmentation. Biophys. J. 85, 3769-3780
57. Litowski, J. R., and Hodges, R. S. (2002) Designing heterodimeric twostranded α-helical coiled-coils. Effects of hydrophobicity and α-helical propensity on protein folding, stability, and specificity. J. Biol. Chem. 277, 37272-37279
58. Sreerama, N., and Woody, R. W. (2000) Estimation of protein secondary structure from circular dichroism spectra: comparison of CONTIN, SELCON, and CDSSTR methods with an expanded reference set. Anal. Biochem. 287, 252-260
59. Wüthrich, K., Billeter, M., and Braun, W. (1984) Polypeptide secondary structure determination by nuclear magnetic resonance observation of short proton-proton distances. J. Mol. Biol. 180, 715-740
60. Wuthrich, K. (1986) NMR of Proteins and Nucleic Acids, John Wiley & Sons, Inc., New York
61. Wishart, D. S., Sykes, B. D., and Richards, F. M. (1991) Relationship between nuclear magnetic resonance chemical shift and protein secondary structure. J. Mol. Biol. 222, 311-333
62. Vila, R., Ponte, I., Jiménez, M. A., Rico, M., and Suau, P. (2000) A helix-turn motif in the C-terminal domain of histone H1. Protein Sci. 9, 627-636
63. Aurora, R., and Rose, G. D. (1998) Helix capping. Protein Sci. 7, 21-38
64. Salzwedel, K., West, J. T., and Hunter, E. (1999) A conserved tryptophanrich motif in the membrane-proximal region of the human immunodeficiency virus type 1 gp41 ectodomain is important for Env-mediated fusion and virus infectivity. J. Virol. 73, 2469-2480
65. Correia, B. E., Ban, Y. E., Holmes, M. A., Xu, H., Ellingson, K., Kraft, Z., Carrico, C., Boni, E., Sather, D. N., Zenobia, C., Burke, K. Y., Bradley-Hewitt, T., Bruhn-Johannsen, J. F., Kalyuzhniy, O., Baker, D., et al. (2010) Computational design of epitope-scaffolds allows induction of antibodies specific for a poorly immunogenic HIV vaccine epitope. Structure 18, 1116-1126
66. Bird, G. H., Irimia, A., Ofek, G., Kwong, P. D., Wilson, I. A., and Walensky, L. D. (2014) Stapled HIV-1 peptides recapitulate antigenic structures and engage broadly neutralizing antibodies. Nat. Struct. Mol. Biol. 21, 1058-1067
67. Sanders, R. W., and Moore, J. P. (2014) HIV: A stamp on the envelope. Nature 514, 437-438
68. Khayat, R., Lee, J. H., Julien, J. P., Cupo, A., Klasse, P. J., Sanders, R. W., Moore, J. P., Wilson, I. A., and Ward, A. B. (2013) Structural characterization of cleaved, soluble HIV-1 envelope glycoprotein trimers. J. Virol. 87, 9865-9872
69. Klasse, P. J., Depetris, R. S., Pejchal, R., Julien, J. P., Khayat, R., Lee, J. H., Marozsan, A. J., Cupo, A., Cocco, N., Korzun, J., Yasmeen, A., Ward, A. B., Wilson, I. A., Sanders, R. W., and Moore, J. P. (2013) Influences on trimerization and aggregation of soluble, cleaved HIV-1 SOSIP envelope glycoprotein. J. Virol. 87, 9873-9885
70. Reuven, E. M., Dadon, Y., Viard, M., Manukovsky, N., Blumenthal, R., and Shai, Y. (2012) HIV-1 gp41 transmembrane domain interacts with the fusion peptide: implication in lipid mixing and inhibition of virus-cell fusion. Biochemistry 51, 2867-2878
71. van Gils, M. J., and Sanders, R. W. (2014) In vivo protection by broadly neutralizing HIV antibodies. Trends Microbiol. 22, 550-551
72. Trkola, A., Kuster, H., Rusert, P., von Wyl, V., Leemann, C., Weber, R., Stiegler, G., Katinger, H., Joos, B., and Günthard, H. F. (2008) In vivo efficacy of human immunodeficiency virus neutralizing antibodies: estimates for protective titers. J. Virol. 82, 1591-1599
73. Dennison, S. M., Sutherland, L. L., Jaeger, F. H., Anasti, K. M., Parks, R., Stewart, S., Bowman, C., Xia, S. M., Zhang, R., Shen, X., Scearce, R. M., Ofek, G., Yang, Y., Kwong, P. D., Santra, S., et al. (2011) Induction of antibodies in rhesus macaques that recognize a fusion-intermediate conformation of HIV-1 gp41. PLoS One 6, e27824
74. Kim,M., Song, L., Moon, J., Sun, Z. Y., Bershteyn, A., Hanson, M., Cain, D., Goka, S., Kelsoe, G., Wagner, G., Irvine, D., and Reinherz, E. L. (2013) Immunogenicity of membrane-bound HIV-1 gp41 membraneproximal external region (MPER) segments is dominated by residue accessibility and modulated by stereochemistry. J. Biol. Chem. 288, 31888-31901
75. Venditto, V. J., Watson, D. S., Motion, M., Montefiori, D., and Szoka, F. C., Jr. (2013) Rational design of membrane proximal external region lipopeptides containing chemical modifications for HIV-1 vaccination. Clin. Vaccine Immunol. 20, 39-45
76. Mao, Y., Wang, L., Gu, C., Herschhorn, A., Désormeaux, A., Finzi, A., Xiang, S.-H., and Sodroski, J. G. (2013) Molecular architecture of the uncleaved HIV-1 envelope glycoprotein trimer. Proc. Natl. Acad. Sci. U.S.A. 110, 12438-12443
77. de la Vega, M., Marin, M., Kondo, N., Miyauchi, K., Kim, Y., Epand, R. F., Epand, R. M., and Melikyan, G. B. (2011) Inhibition of HIV-1 endocytosis allows lipid mixing at the plasma membrane, but not complete fusion. Retrovirology 8, 99
78. Wishart, D. S., Bigam, C. G., Holm, A., Hodges, R. S., and Sykes, B. D. (1995) 1H, 13C and 15N random coil NMR chemical shifts of the common amino acids. I. Investigations of nearest-neighbor effects. J. Biomol. NMR 5, 67-81