Structural and biochemical insights into the V/I505T mutation found in the EIAV gp45 vaccine strain

Retrovirology

Volumn 11, Issue 1, 2014, Pages

  Du, Jiansen ^a   Wang, Xuefeng ^b   Ma, Jing ^a   Wang, Jianxin ^a   Qin, Yuyin ^b   Zhu, Chunhui ^b   Liu, Fang ^a   Shao, Yiming ^c   Zhou, Jianhua ^b   Qiao, Wentao ^a   Liu, Xinqi ^a  

^a NANKAI UNIVERSITY   (China)

^b INSTITUTE OF PLANT PROTECTION   (China)

^c CHINESE CENTER FOR DISEASE CONTROL AND PREVENTION   (China)

Author keywords

Crystal structure; EIAV; gp45; Heptad repeat; Pre fusion conformation; Replication; Stability; Vaccine strain

Indexed keywords

GLYCOPROTEIN GP 41; GLYCOPROTEIN GP 45; UNCLASSIFIED DRUG; VIRUS GLYCOPROTEIN;

ALPHA HELIX; ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; EQUINE INFECTIOUS ANEMIA VIRUS; HYDROPHILICITY; HYDROPHOBICITY; LENTIVIRINAE; NONHUMAN; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN STABILITY; TEMPERATURE DEPENDENCE; VIRUS ATTENUATION; VIRUS INFECTIVITY; VIRUS REPLICATION; VIRUS STRAIN;

ANIMALS; CRYSTALLOGRAPHY, X-RAY; HORSES; INFECTIOUS ANEMIA VIRUS, EQUINE; MUTANT PROTEINS; MUTATION, MISSENSE; PROTEIN CONFORMATION; PROTEIN STABILITY; TEMPERATURE; VIRAL ENVELOPE PROTEINS; VIRAL VACCINES;

EID: 84899081437     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/1742-4690-11-26     Document Type: Article

References (59)

1. Gorry PR, Ancuta P. Coreceptors and HIV-1 pathogenesis. Curr HIV/AIDS Rep 2011, 8:45-53.
2. Campbell EM, Hope TJ. Live cell imaging of the HIV-1 life cycle. Trends Microbiol 2008, 16:580-587. 10.1016/j.tim.2008.09.006, 3209483, 18977142.
3. Citterio P, Rusconi S. Novel inhibitors of the early steps of the HIV-1 life cycle. Expert Opin Investig Drugs 2007, 16:11-23. 10.1517/13543784.16.1.11, 17155850.
4. Cook RF, Leroux C, Issel CJ. Equine infectious anemia and equine infectious anemia virus in 2013A review. Vet Microbiol 2013, 167:181-204. 10.1016/j.vetmic.2013.09.031, 24183747.
5. Nakamura H, Miyazaki N, Hosoya N, Koga M, Odawara T, Kikuchi T, Koibuchi T, Kawana-Tachikawa A, Fujii T, Miura T, Iwamoto A. Long-term successful control of super-multidrug-resistant human immunodeficiency virus type 1 infection by a novel combination therapy of raltegravir, etravirine, and boosted-darunavir. J Infect Chemother 2011, 17:105-110.
6. Rerks-Ngarm S, Pitisuttithum P, Nitayaphan S, Kaewkungwal J, Chiu J, Paris R, Premsri N, Namwat C, de Souza M, Adams E, Benenson M, Gurunathan S, Tartaglia J, McNeil JG, Feancis DP, Stablein D, Biex DL, Chunsuttiwat S, Khamboonruang C, Thongcharoen P, Robb ML, Michael NL, Kunasol P, Kim JH, . Moph-Taveg Investigators Vaccination with ALVAC and AIDSVAX to Prevent HIV-1 Infection in Thailand. New Engl J Med 2009, 361:2209-2220. 10.1056/NEJMoa0908492, 19843557, Moph-Taveg Investigators.
7. de Souza MS, Ratto-Kim S, Chuenarom W, Schuetz A, Chantakulkij S, Nuntapinit B, Valencia-Micolta A, Thelian D, Nitayaphan S, Pitisuttithum P, Paris RM, Kaewkungwal J, Michael NL, Rerks-Ngarm S, Mathieson B, Marovich M, Currier JR, Kim JH, . Minist Publ Hlth Thai AIDS Vaccine The Thai Phase III Trial (RV144) Vaccine Regimen Induces T Cell Responses That Preferentially Target Epitopes within the V2 Region of HIV-1 Envelope. J Immunol 2012, 188:5166-5176. 10.4049/jimmunol.1102756, 3383859, 22529301, Minist Publ Hlth Thai AIDS Vaccine.
8. Harouse JM, Bhat S, Spitalnik SL, Laughlin M, Stefano K, Silberberg DH, Gonzalez-Scarano F. Inhibition of entry of HIV-1 in neural cell lines by antibodies against galactosyl ceramide. Science 1991, 253:320-323. 10.1126/science.1857969, 1857969.
9. Blumenthal R, Durell S, Viard M. HIV entry and envelope glycoprotein-mediated fusion. J Biol Chem 2012, 287:40841-40849. 10.1074/jbc.R112.406272, 3510787, 23043104.
10. Stein BS, Gowda SD, Lifson JD, Penhallow RC, Bensch KG, Engleman EG. pH-independent HIV entry into CD4-positive T cells via virus envelope fusion to the plasma membrane. Cell 1987, 49:659-668. 10.1016/0092-8674(87)90542-3, 3107838.
11. Cai L, Gochin M, Liu K. Biochemistry and biophysics of HIV-1 gp41 - membrane interactions and implications for HIV-1 envelope protein mediated viral-cell fusion and fusion inhibitor design. Curr Top Med Chem 2011, 11:2959-2984. 10.2174/156802611798808497, 3220743, 22044229.
12. Leroux C, Cadore JL, Montelaro RC. Equine Infectious Anemia Virus (EIAV): what has HIV's country cousin got to tell us?. Veterinary Res 2004, 35:485-512.
13. Li HG, Zhang XY, Fan XJ, Shen T, Tong X, Shen RX, Shao YM. A conservative domain shared by HIV gp120 and EIAV gp90: Implications for HIV vaccine design. Aids Res Human Retrov 2005, 21:1057-1059.
14. Berger EA, Murphy PM, Farber JM. Chemokine receptors as HIV-1 coreceptors: Roles in viral entry, tropism, and disease. Ann Rev Immunol 1999, 17:657-700.
15. Greenberg M, Cammack N, Salgo M, Smiley L. HIV fusion and its inhibition in antiretroviral therapy. Rev Med Virol 2004, 14:321-337. 10.1002/rmv.440, 15334539.
16. LaBranche CC, Galasso G, Moore JP, Bolognesi DP, Hirsch MS, Hammer SM. HIV fusion and its inhibition. Antiviral Res 2001, 50:95-115. 10.1016/S0166-3542(01)00130-9, 11369431.
17. Kliger Y, Shai Y. Inhibition of HIV-1 entry before gp41 folds into its fusion-active conformation. J Mol Biol 2000, 295:163-168. 10.1006/jmbi.1999.3368, 10623516.
18. Bar KJ, Decker JM, Ganusov VV, Li H, McLellan JS, Yang Y, Pavlicek JW, Keele BF, Gao F, Perelson AS, Kwong PD, Hahn BH, Shaw GM. Molecular targets and potency of HIV-1 neutralization revealed by dynamic assessment of transmitted/founder virus antibody recognition and escape. Aids Res Human Retrov 2010, 26:A11-A12.
19. Wei XP, Decker JM, Wang SY, Hui HX, Kappes JC, Wu XY, Salazar-Gonzalez JF, Salazar MG, Kilby JM, Saag MS, Komarova NL, Nowak MA, Hahn BH, Kwong PD, Shaw GM. Antibody neutralization and escape by HIV-1. Nature 2003, 422:307-312. 10.1038/nature01470, 12646921.
20. Huang JH, Ofek G, Laub L, Louder MK, Doria-Rose NA, Longo NS, Imamichi H, Bailer RT, Chakrabarti B, Sharma SK, Alam SM, Wang T, Yang YP, Zhang BS, Migueles SA, Wyatt R, Haynes BF, Kwong PD, Mascola JR, Connors M. Broad and potent neutralization of HIV-1 by a gp41-specific human antibody. Nature 2012, 491:406. 10.1038/nature11544, 23151583.
21. Chen Y, Zhang JS, Hwang KK, Bouton-Verville H, Xia SM, Newman A, Ouyang YB, Haynes BF, Verkoczy L. Common tolerance mechanisms, but distinct cross-reactivities associated with gp41 and lipids, limit production of HIV-1 broad neutralizing antibodies 2 F5 and 4E10. J Immunol 2013, 191:1260-1275. 10.4049/jimmunol.1300770, 23825311.
22. Lu L, Pan C, Li Y, Lu H, He W, Jiang S. A bivalent recombinant protein inactivates HIV-1 by targeting the gp41 prehairpin fusion intermediate induced by CD4 D1D2 domains. Retrovirology 2012, 9:104. 10.1186/1742-4690-9-104, 3531269, 23217195.
23. Yang ZN, Mueser TC, Kaufman J, Stahl SJ, Wingfield PT, Hyde CC. The crystal structure of the SIV gp41 ectodomain at 1.47 angstrom resolution. J Struct Biol 1999, 126:131-144. 10.1006/jsbi.1999.4116, 10388624.
24. Malashkevich VN, Chan DC, Chutkowski CT, Kim PS. Crystal structure of the simian immunodeficiency virus (SIV) gp41 core: Conserved helical interactions underlie the broad inhibitory activity of gp41 peptides. Proc Natl Acad Sci USA 1998, 95:9134-9139. 10.1073/pnas.95.16.9134, 21304, 9689046.
25. Weissenhorn W, Dessen A, Harrison SC, Skehel JJ, Wiley DC. Atomic structure of the ectodomain from HIV-1 gp41. Nature 1997, 387:426-430. 10.1038/387426a0, 9163431.
26. Tan K, Liu J, Wang J, Shen S, Lu M. Atomic structure of a thermostable subdomain of HIV-1 gp41. Proc Natl Acad Sci USA 1997, 94:12303-12308. 10.1073/pnas.94.23.12303, 24915, 9356444.
27. Chan DC, Fass D, Berger JM, Kim PS. Core structure of gp41 from the HIV envelope glycoprotein. Cell 1997, 89:263-273. 10.1016/S0092-8674(00)80205-6, 9108481.
28. Maeso R, Huarte N, Julien JP, Kunert R, Pai EF, Nieva JL. Interaction of anti-HIV type 1 antibody 2F5 with phospholipid bilayers and its relevance for the mechanism of virus neutralization. AIDS Res Hum Retrov 2011, 27:863-876.
29. Du J, Xue H, Ma J, Liu F, Zhou J, Shao Y, Qiao W, Liu X. The crystal structure of HIV CRF07 B'/C gp41 reveals a hyper-mutant site in the middle of HR2 heptad repeat. Virology 2013, 446:86-94. 10.1016/j.virol.2013.07.024, 24074570.
30. Buzon V, Natrajan G, Schibli D, Campelo F, Kozlov MM, Weissenhorn W. Crystal structure of HIV-1 gp41 including both fusion peptide and membrane proximal external regions. PLoS Pathog 2010, 6:e1000880. 10.1371/journal.ppat.1000880, 2865522, 20463810.
31. Craigo JK, Montelaro RC. Lessons in AIDS vaccine development learned from studies of equine infectious, anemia virus infection and immunity. Viruses 2013, 5:2963-2976. 10.3390/v5122963, 24316675.
32. Anderson LJ. Respiratory syncytial virus vaccine development. Semin Immunol 2013, 25:160-171. 10.1016/j.smim.2013.04.011, 23778071.
33. Uhl EW, Heaton-Jones TG, Pu R, Yamamoto JK. FIV vaccine development and its importance to veterinary and human medicine: a review FIV vaccine 2002 update and review. Vet Immunol Immunopathol 2002, 90:113-132. 10.1016/S0165-2427(02)00227-1, 12459160.
34. Shen RX, Wang Z. Development and use of an equine infectious anemia donkey leucocyte attenuated vaccine. In: Tashjian RJ, Zarish, D, Equine Infectious Anaemia A National Review of Policies, Programs and Future Objectives 1985, 135-148. American Quarter Horse Association.
35. Craigo JK, Barnes S, Cook SJ, Issel CJ, Montelaro RC. Divergence, not diversity of an attenuated equine lentivirus vaccine strain correlates with protection from disease. Vaccine 2010, 28:8095-8104. 10.1016/j.vaccine.2010.10.003, 2997116, 20955830.
36. Wang X, Wang S, Lin Y, Jiang C, Ma J, Zhao L, Lv X, Wang F, Shen R, Kong X, Zhou J. Genomic comparison between attenuated Chinese equine infectious anemia virus vaccine strains and their parental virulent strains. Arch Virol 2011, 156:353-357. 10.1007/s00705-010-0877-8, 21136127.
37. Liang H, He X, Shen RX, Shen T, Tong X, Ma Y, Xiang WH, Zhang XY, Shao YM. Combined amino acid mutations occurring in the envelope closely correlate with pathogenicity of EIAV. Arch Virol 2006, 151:1387-1403. 10.1007/s00705-005-0718-3, 16502285.
38. Suntoke TR, Chan DC. The fusion activity of HIV-1 gp41 depends on interhelical interactions. J Biolog Chem 2005, 280:19852-19857.
39. Julien JP, Cupo A, Sok D, Stanfield RL, Lyumkis D, Deller MC, Klasse PJ, Burton DR, Sanders RW, Moore JP, Ward AB, Wilson IA. Crystal structure of a soluble cleaved HIV-1 envelope trimer. Science 2013, 342:1477-1483. 10.1126/science.1245625, 24179159.
40. Shen T, Liang H, Tong X, Fan XJ, He X, Ma Y, Xiang WH, Shen RX, Zhang XY, Shao YM. Amino acid mutations of the infectious clone from Chinese EIAV attenuated vaccine resulted in reversion of virulence. Vaccine 2006, 24:738-749. 10.1016/j.vaccine.2005.08.084, 16202485.
41. Gallo SA, Finnegan CM, Viard M, Raviv Y, Dimitrov A, Rawat SS, Puri A, Durell S, Blumenthal R. The HIV Env-mediated fusion reaction. Biochimica Et Biophysica Acta-Biomembranes 2003, 1614:36-50.
42. Cook RF, Cook SJ, Berger SL, Leroux C, Ghabrial NN, Gantz M, Bolin PS, Mousel MR, Montelaro RC, Issel CJ. Enhancement of equine infectious anemia virus virulence by identification and removal of suboptimal nucleotides. Virology 2003, 313:588-603. 10.1016/S0042-6822(03)00351-9, 12954224.
43. Colman PM, Lawrence MC. The structural biology of type I viral membrane fusion. Nat Rev Mol Cell Biol 2003, 4:309-319. 10.1038/nrm1076, 12671653.
44. Peisajovich SG, Epand RF, Pritsker M, Shai Y, Epand RM. The polar region consecutive to the HIV fusion peptide participates in membrane fusion. Biochemistry 2000, 39:1826-1833. 10.1021/bi991887i, 10677233.
45. Sen J, Yan TR, Wang JZ, Rong LJ, Tao L, Caffrey M. Alanine scanning mutagenesis of HIV-1 gp41 heptad repeat 1: insight into the gp120-gp41 interaction. Biochemistry 2010, 49:5057-5065. 10.1021/bi1005267, 20481578.
46. Finzi A, Xiang SH, Pacheco B, Wang LP, Haight J, Kassa A, Danek B, Pancera M, Kwong PD, Sodroski J. Topological layers in the HIV-1 gp120 inner domain regulate gp41 interaction and CD4-triggered conformational transitions. Mol Cell 2010, 37:656-667. 10.1016/j.molcel.2010.02.012, 2854584, 20227370.
47. Rigter A, Widjaja I, Versantvoort H, Coenjaerts FE, van Roosmalen M, Leenhouts K, Rottier PJ, Haijema BJ, de Haan CA. A protective and safe intranasal RSV vaccine based on a recombinant prefusion-like form of the F protein bound to bacterium-like particles. PLoS One 2013, 8:e71072. 10.1371/journal.pone.0071072, 3741363, 23951084.
48. Jiang CG, Ma J, Gao X, Lin YZ, Zhao LP, Hua YP, Liu D, Zhou JH. Effects on in vitro replication of equine infectious anemia virus attenuated vaccine strain with truncated mutation in the transmembrane protein. Prog Biochem Biophys 2010, 37:261-268.
49. Zhang BS, Jin S, Jin J, Li F, Montelaro RC. A tumor necrosis factor receptor family protein serves as a cellular receptor for the macrophage-tropic equine lentivirus. Proc Natl Acad Sci USA 2005, 102:9918-9923. 10.1073/pnas.0501560102, 1174982, 15985554.
50. He J, Chen Y, Farzan M, Choe H, Ohagen A, Gartner S, Busciglio J, Yang X, Hofmann W, Newman W, Mackay CR, Sodroski J, Gabuzda D. CCR3 and CCR5 are co-receptors for HIV-1 infection of microglia. Nature 1997, 385:645-649. 10.1038/385645a0, 9024664.
51. Hoxie JA, LaBranche CC, Endres MJ, Turner JD, Berson JF, Doms RW, Matthews TJ. CD4-independent utilization of the CXCR4 chemokine receptor by HIV-1 and HIV-2. J Reprod Immunol 1998, 41:197-211. 10.1016/S0165-0378(98)00059-X, 10213311.
52. Craigo JK, Montelaro RC. Equine infectious anemia virus infection and immunity: lessons for aids vaccine development. Future Virol 2011, 6:139-142. 10.2217/fvl.10.85, 3107501, 21643555.
53. Craigo JK, Montelaro RC. EIAV envelope diversity: shaping viral persistence and encumbering vaccine efficacy. Curr HIV Res 2010, 8:81-86. 10.2174/157016210790416398, 20210783.
54. Lyumkis D, Julien JP, de Val N, Cupo A, Potter CS, Klasse PJ, Burton DR, Sanders RW, Moore JP, Carragher B, Wilson IA, Ward AB. Cryo-EM structure of a fully glycosylated soluble cleaved HIV-1 envelope trimer. Science 2013, 342:1484-1490. 10.1126/science.1245627, 24179160.
55. WM ZO. Processing of X-ray Diffraction Data Collected in Oscillation Mode. Methods Enzymol 1997, 276:307-326.
56. Winn MD, Ballard CC, Cowtan KD, Dodson EJ, Emsley P, Evans PR, Keegan RM, Krissinel EB, Leslie AGW, McCoy A, McNicholas SJ, Murshudoy GN, Pannu NS, Potterton EA, Powell HR, Read RJ, Vagin A, Wilson KS. Overview of the CCP4 suite and current developments. Acta Crystallographica Sec D-Biolog Crystallog 2011, 67:235-242.
57. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, McCoy AJ, Moriarty NW, Oeffner R, Read RJ, Richardson DC, Richardson JS, Terwilliger TC, Zwart PH. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallographica Sec D-Biolog Crystallog 2010, 66:213-221.
58. Emsley P, Lohkamp B, Scott WG, Cowtan K. Features and development of Coot. Acta Crystallographica Sec D-Biolog Crystallog 2010, 66:486-501.
59. Pozdnyakova I, Regan L. New insights into Fragile X syndrome - Relating genotype to phenotype at the molecular level. Febs J 2005, 272:872-878. 10.1111/j.1742-4658.2004.04527.x, 15670167.