A simple one-step method for the preparation of HIV-1 envelope glycoprotein immunogens based on a CD4 mimic peptide

Virology

Volumn 381, Issue 2, 2008, Pages 241-250

  Martin, Grégoire ^a   Sun, Yide ^b   Heyd, Bernadette ^a   Combes, Olivier ^a   Ulmer, Jeffrey B ^b   Descours, Anne ^a   Barnett, Susan W ^b   Srivastava, Indresh K ^b   Martin, Loïc ^a  

^a SERVICE DE CHIMIE BIOORGANIQUE ET DE MARQUAGE   (France)

^b Novartis Vaccines and Diagnostics Corporation   (United States)

Author keywords

Affinity chromatography; AIDS vaccine; CD4 mimic; HIV 1; Monomer; Trimer

Indexed keywords

CD4 ANTIGEN; CHEMOKINE RECEPTOR CCR5; GLYCOPROTEIN GP 120; GLYCOPROTEIN GP 140; HUMAN IMMUNODEFICIENCY VIRUS ANTIGEN; LIGAND; MONOCLONAL ANTIBODY;

AFFINITY CHROMATOGRAPHY; ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN RECOGNITION; ARTICLE; CONTROLLED STUDY; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMORAL IMMUNITY; IMMUNOGENICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN PURIFICATION; RAT; RECEPTOR BINDING; SUPERNATANT; VIRUS ENVELOPE;

ANIMALS; ANTIGENS, CD4; CHO CELLS; CHROMATOGRAPHY, AFFINITY; CRICETINAE; CRICETULUS; HIV ANTIBODIES; HIV ENVELOPE PROTEIN GP120; HIV-1; PEPTIDES; PROTEIN BINDING; PROTEIN MULTIMERIZATION; RATS; RATS, WISTAR; RECEPTORS, CCR5; RECOMBINANT PROTEINS;

HUMAN IMMUNODEFICIENCY VIRUS 1; RATTUS;

EID: 54549093550     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2008.08.039     Document Type: Article

References (53)

1. Barnett S.W., Srivastava I.K., Kan E., Zhou F., Goodsell A., Cristillo A.D., Ferrai M.G., Weiss D.E., Letvin N.L., Montefiori D., Pal R., and Vajdy M. Protection of macaques against vaginal SHIV challenge by systemic or mucosal and systemic vaccinations with HIV-envelope. AIDS 22 3 (2008) 339-348
2. Berman P.W., Gregory T.J., Riddle L., Nakamura G.R., Champe M.A., Porter J.P., Wurm F.M., Hershberg R.D., Cobb E.K., and Eichberg J.W. Protection of chimpanzees from infection by HIV-1 after vaccination with recombinant glycoprotein gp120 but not gp160. Nature 345 6276 (1990) 622-625
3. Binley J.M., Sanders R.W., Clas B., Schuelke N., Master A., Guo Y., Kajumo F., Anselma D.J., Maddon P.J., Olson W.C., and Moore J.P. A recombinant human immunodeficiency virus type 1 envelope glycoprotein complex stabilized by an intermolecular disulfide bond between the gp120 and gp41 subunits is an antigenic mimic of the trimeric virion-associated structure. J. Virol. 74 2 (2000) 627-643
4. Binley J.M., Wrin T., Korber B., Zwick M.B., Wang M., Chappey C., Stiegler G., Kunert R., Zolla-Pazner S., Katinger H., Petropoulos C.J., and Burton D.R. Comprehensive cross-clade neutralization analysis of a panel of anti-human immunodeficiency virus type 1 monoclonal antibodies. J. Virol. 78 23 (2004) 13232-13252
5. Broder C.C., Earl P.L., Long D., Abedon S.T., Moss B., and Doms R.W. Antigenic implications of human immunodeficiency virus type 1 envelope quaternary structure: oligomer-specific and -sensitive monoclonal antibodies. Proc. Natl. Acad. Sci. U. S. A. 91 24 (1994) 11699-11703
6. Burton D.R., and Parren P.W. Vaccines and the induction of functional antibodies: time to look beyond the molecules of natural infection?. Nat. Med. 6 2 (2000) 123-125
7. Cefai D., Debre P., Kaczorek M., Idziorek T., Autran B., and Bismuth G. Human immunodeficiency virus-1 glycoproteins gp120 and gp160 specifically inhibit the CD3/T cell-antigen receptor phosphoinositide transduction pathway. J. Clin. Invest. 86 6 (1990) 2117-2124
8. Chapman B.S., Thayer R.M., Vincent K.A., and Haigwood N.L. Effect of intron A from human cytomegalovirus (Towne) immediate early gene on heterologous expression in mammalian cells. Nucleic Acids Res. 19 14 (1991) 3979-3986
9. Drakopoulou E., Zinn-Justin S., Guenneugues M., Gilquin B., Menez A., and Vita C. Changing the structural context of a functional beta-hairpin. Synthesis and characterization of a chimera containing the curaremimetic loop of a snake toxin in the scorpion alpha/beta scaffold. J. Biol. Chem. 271 20 (1996) 11979-11987
10. Fouts T.R., Trkola A., Fung M.S., and Moore J.P. Interactions of polyclonal and monoclonal anti-glycoprotein 120 antibodies with oligomeric glycoprotein 120-glycoprotein 41 complexes of a primary HIV type 1 isolate: relationship to neutralization. AIDS Res. Hum. Retrovir. 14 7 (1998) 591-597
11. Gallo R.C. The end or the beginning of the drive to an HIV-preventive vaccine: a view from over 20 years. Lancet 366 9500 (2005) 1894-1898
12. Girard M., Meignier B., Barré-Sinoussi F., Kieny M.P., Matthews T., Muchmore E., Nara P.L., Wei Q., Rimsky L., Weinhold K., et al. Vaccine-induced protection of chimpanzees against infection by a heterologous human immunodeficiency virus type 1. J. Virol. 69 10 (1995) 6239-6248
13. Girard M., Yue L., Barré-Sinoussi F., van der Ryst E., Meignier B., Muchmore E., and Fultz P.N. Failure of a human immunodeficiency virus type 1 (HIV-1) subtype B-derived vaccine to prevent infection of chimpanzees by an HIV-1 subtype E strain. J. Virol. 70 11 (1996) 8229-8233
14. Girard M.P., Osmanov S.K., and Kieny M.P. A review of vaccine research and development: the human immunodeficiency virus (HIV). Vaccine 24 19 (2006) 4062-4081
15. Graham B.S. Clinical trials of HIV vaccines. Annu. Rev. Med. 53 (2002) 207-221
16. Graham B.S., and Wright P.F. Candidate AIDS vaccines. N. Engl. J. Med. 333 20 (1995) 1331-1339
17. Graham B.S., and Mascola J.R. Lessons from failure-preparing for future HIV-1 vaccine efficacy trials. J. Infect. Dis. 191 5 (2005) 647-649
18. Huang C.C., Stricher F., Martin L., Decker J.M., Majeed S., Barthe P., Hendrickson W.A., Robinson J., Roumestand C., Sodroski J., Wyatt R., Shaw G.M., Vita C., and Kwong P.D. Scorpion-toxin mimics of CD4 in complex with human immunodeficiency virus gp120 crystal structures, molecular mimicry, and neutralization breadth. Structure 13 5 (2005) 755-768
19. Jeffs S.A., Goriup S., Kebble B., Crane D., Bolgiano B., Sattentau Q., Jones S., and Holmes H. Expression and characterization of recombinant oligomeric envelope glycoproteins derived from primary isolates of HIV-1. Vaccine 22 8 (2004) 1032-1046
20. Joint United Nations programme on HIV/.AIDS (UNAIDS)/World Health Organization (WHO), 2007. AIDS epidemic update, Genewa Switzerland, December 2007.
21. Jones D.H., McBride B.W., Roff M.A., and Farrar G.H. Efficient purification and rigorous characterisation of a recombinant gp120 for HIV vaccine studies. Vaccine 13 11 (1995) 991-999
22. Kalyanaraman V.S., Rodriguez V., Veronese F., Rahman R., Lusso P., DeVico A.L., Copeland T., Oroszlan S., Gallo R.C., and Sarngadharan M.G. Characterization of the secreted native gp120 and gp160 of the human immunodeficiency virus type 1. AIDS Res. Hum. Retrovir. 6 3 (1990) 371-380
23. Kieny M.P., Lathe R., Rivière Y., Dott K., Schmitt D., Girard M., Montagnier L., and Lecocq J. Improved antigenicity of the HIV env protein by cleavage site removal. Protein Eng. 2 3 (1988) 219-225
24. Kwong P.D., Wyatt R., Desjardins E., Robinson J., Culp J.S., Hellmig B.D., Sweet R.W., Sodroski J., and Hendrickson W.A. Probability analysis of variational crystallization and its application to gp120, the exterior envelope glycoprotein of type 1 human immunodeficiency virus (HIV-1). J. Biol. Chem. 274 7 (1999) 4115-4123
25. Martin L., Stricher F., Misse D., Sironi F., Pugniere M., Barthe P., Prado-Gotor R., Freulon I., Magne X., Roumestand C., Menez A., Lusso P., Veas F., and Vita C. Rational design of a CD4 mimic that inhibits HIV-1 entry and exposes cryptic neutralization epitopes. Nat. Biotechnol. 21 1 (2003) 71-76
26. Mascola J.R., Snyder S.W., Weislow O.S., Belay S.M., Belshe R.B., Schwartz D.H., Clements M.L., Dolin R., Graham B.S., Gorse G.J., Keefer M.C., McElrath M.J., Walker M.C., Wagner K.F., McNeil J.G., McCutchan F.E., and Burke D.S. Immunization with envelope subunit vaccine products elicits neutralizing antibodies against laboratory-adapted but not primary isolates of human immunodeficiency virus type 1. The National Institute of Allergy and Infectious Diseases AIDS Vaccine Evaluation Group. J. Infect. Dis. 173 2 (1996) 340-348
27. McCune J.M., Rabin L.B., Feinberg M.B., Lieberman M., Kosek J.C., Reyes G.R., and Weissman I.L. Endoproteolytic cleavage of gp160 is required for the activation of human immunodeficiency virus. Cell 53 1 (1988) 55-67
28. Mechulam A., Cerutti M., Pugniere M., Misse D., Gajardo J., Roquet F., Robinson J., and Veas F. Highly conserved beta16/beta17 beta-hairpin structure in human immunodeficiency virus type 1 YU2 gp120 is critical for CCR5 binding. J. Mol. Med. 83 7 (2005) 542-552
29. Misse D., Cerutti M., Schmidt I., Jansen A., Devauchelle G., Jansen F., and Veas F. Dissociation of the CD4 and CXCR4 binding properties of human immunodeficiency virus type 1 gp120 by deletion of the first putative alpha-helical conserved structure. J. Virol. 72 9 (1998) 7280-7288
30. Moore J.P., Cao Y., Qing L., Sattentau Q.J., Pyati J., Koduri R., Robinson J., Barbas III C.F., Burton D.R., and Ho D.D. Primary isolates of human immunodeficiency virus type 1 are relatively resistant to neutralization by monoclonal antibodies to gp120, and their neutralization is not predicted by studies with monomeric gp120. J. Virol. 69 1 (1995) 101-109
31. Parren P.W., Ditzel H.J., Gulizia R.J., Binley J.M., Barbas III C.F., Burton D.R., and Mosier D.E. Protection against HIV-1 infection in hu-PBL-SCID mice by passive immunization with a neutralizing human monoclonal antibody against the gp120 CD4-binding site. AIDS 9 6 (1995) F1-F6
32. Parren P.W., Mondor I., Naniche D., Ditzel H.J., Klasse P.J., Burton D.R., and Sattentau Q.J. Neutralization of human immunodeficiency virus type 1 by antibody to gp120 is determined primarily by occupancy of sites on the virion irrespective of epitope specificity. J. Virol. 72 5 (1998) 3512-3519
33. Parren P.W., Marx P.A., Hessell A.J., Luckay A., Harouse J., Cheng-Mayer C., Moore J.P., and Burton D.R. Antibody protects macaques against vaginal challenge with a pathogenic R5 simian/human immunodeficiency virus at serum levels giving complete neutralization in vitro. J. Virol. 75 17 (2001) 8340-8347
34. Phogat S., and Wyatt R. Rational modifications of HIV-1 envelope glycoproteins for immunogen design. Curr. Pharm. Des. 13 2 (2007) 213-227
35. Rhodes A.D., Spitali M., Hutchinson G., Rud E.W., and Stephens P.E. Expression, characterization and purification of simian immunodeficiency virus soluble, oligomerized gp160 from mammalian cells. J. Gen. Virol. 75 Pt 1 (1994) 207-213
36. Ruprecht R.M., Ferrantelli F., Kitabwalla M., Xu W., and McClure H.M. Antibody protection: passive immunization of neonates against oral AIDS virus challenge. Vaccine 21 24 (2003) 3370-3373
37. Samson M., Labbe O., Mollereau C., Vassart G., and Parmentier M. Molecular cloning and functional expression of a new human CC-chemokine receptor gene. Biochemistry 35 11 (1996) 3362-3367
38. Sanders R.W., Vesanen M., Schuelke N., Master A., Schiffner L., Kalyanaraman R., Paluch M., Berkhout B., Maddon P.J., Olson W.C., Lu M., and Moore J.P. Stabilization of the soluble, cleaved, trimeric form of the envelope glycoprotein complex of human immunodeficiency virus type 1. J. Virol. 76 17 (2002) 8875-8889
39. Sattentau Q.J., and Moore J.P. Human immunodeficiency virus type 1 neutralization is determined by epitope exposure on the gp120 oligomer. J. Exp. Med. 182 1 (1995) 185-196
40. Srivastava I.K., Stamatatos L., Legg H., Kan E., Fong A., Coates S.R., Leung L., Wininger M., Donnelly J.J., Ulmer J.B., and Barnett S.W. Purification and characterization of oligomeric envelope glycoprotein from a primary R5 subtype B human immunodeficiency virus. J. Virol. 76 6 (2002) 2835-2847
41. Srivastava I.K., Stamatatos L., Kan E., Vajdy M., Lian Y., Hilt S., Martin L., Vita C., Zhu P., Roux K.H., Vojtech L.C., Montefiori D., Donnelly J., Ulmer J.B., and Barnett S.W. Purification, characterization, and immunogenicity of a soluble trimeric envelope protein containing a partial deletion of the V2 loop derived from SF162, an R5-tropic human immunodeficiency virus type 1 isolate. J. Virol. 77 20 (2003) 11244-11259
42. Srivastava I.K., Kan E., Sun Y., Sharma V.A., Cisto J., Burke B., Lian Y., Hilt S., Biron Z., Hartog K., Stamatatos L., Cheng R.H., Ulmer J.B., and Barnett S.W. Comparative evaluation of trimeric envelope glycoproteins derived from subtype C and B HIV-1 R5 isolates. Virology 372 2 (2008) 273-290
43. Stott E.J., Almond N., Kent K., Walker B., Hull R., Rose J., Silvera P., Sangster R., Corcoran T., Lines J., Silvera K., Luciw P., Murphy-Corb M., Momin P., and Bruck C. Evaluation of a candidate human immunodeficiency virus type 1 (HIV-1) vaccine in macaques: effect of vaccination with HIV-1 gp120 on subsequent challenge with heterologous simian immunodeficiency virus-HIV-1 chimeric virus. J. Gen. Virol. 79 Pt 3 (1998) 423-432
44. Stricher F., Martin L., Barthe P., Pogenberg V., Mechulam A., Menez A., Roumestand C., Veas F., Royer C., and Vita C. A high-throughput fluorescence polarization assay specific to the CD4 binding site of HIV-1 glycoproteins based on a fluorescein-labelled CD4 mimic. Biochem. J. 390 Pt 1 (2005) 29-39
45. Stricher F., Huang C.C., Descours A., Duquesnoy S., Combes O., Decker J.M., Do Kwon Y., Lusso P., Shaw G.M., Vita C., Kwong P.D., and Martin L. Combinatorial optimization of a CD4-mimetic miniprotein and cocrystal structures with HIV-1 gp120 envelope glycoprotein. J. Mol. Biol. 382 2 (2008) 510-524
46. Van Herrewege Y., Morellato L., Descours A., Aerts L., Michiels J., Heyndrickx L., Martin L., and Vanham G. CD4 mimetic miniproteins: a new class of potent anti-HIV compounds with promising activity as microbicides. J. Antimicrob. Chemother. 61 4 (2008) 818-826
47. VanCott T.C., Veit S.C., Kalyanaraman V., Earl P., and Birx D.L. Characterization of a soluble, oligomeric HIV-1 gp160 protein as a potential immunogen. J. Immunol. Methods 183 1 (1995) 103-117
48. Veazey R.S., Shattock R.J., Pope M., Kirijan J.C., Jones J., Hu Q., Ketas T., Marx P.A., Klasse P.J., Burton D.R., and Moore J.P. Prevention of virus transmission to macaque monkeys by a vaginally applied monoclonal antibody to HIV-1 gp120. Nat. Med. 9 3 (2003) 343-346
49. Vita C., Drakopoulou E., Vizzavona J., Rochette S., Martin L., Menez A., Roumestand C., Yang Y.S., Ylisastigui L., Benjouad A., and Gluckman J.C. Rational engineering of a mini-protein that reproduces the core of the CD4 site interacting with HIV-1 envelope glycoprotein. Proc. Natl. Acad. Sci. U. S. A. 96 23 (1999) 13091-13096
50. Wrin T., and Nunberg J.H. HIV-1MN recombinant gp120 vaccine serum, which fails to neutralize primary isolates of HIV-1, does not antagonize neutralization by antibodies from infected individuals. AIDS 8 11 (1994) 1622-1623
51. Wyatt R., and Sodroski J. The HIV-1 envelope glycoproteins: fusogens, antigens, and immunogens. Science 280 5371 (1998) 1884-1888
52. Zhang P.F., Cham F., Dong M., Choudhary A., Bouma P., Zhang Z., Shao Y., Feng Y.R., Wang L., Mathy N., Voss G., Broder C.C., and Quinnan Jr. G.V. Extensively cross-reactive anti-HIV-1 neutralizing antibodies induced by gp140 immunization. Proc. Natl. Acad. Sci. U. S. A. 104 24 (2007) 10193-10198
53. Zhou T., Xu L., Dey B., Hessell A.J., Van Ryk D., Xiang S.H., Yang X., Zhang M.Y., Zwick M.B., Arthos J., Burton D.R., Dimitrov D.S., Sodroski J., Wyatt R., Nabel G.J., and Kwong P.D. Structural definition of a conserved neutralization epitope on HIV-1 gp120. Nature 445 7129 (2007) 732-737