Rational design of membrane proximal external region lipopeptides containing chemical modifications for HIV-1 vaccination

Clinical and Vaccine Immunology

Volumn 20, Issue 1, 2013, Pages 39-45

  Venditto, Vincent J ^a   Watson, Douglas S ^a,c   Motion, Michael ^a   Montefiori, David ^b   Szoka, Francis C ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

^c MERCK RESEARCH LABORATORIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; IMMUNOGLOBULIN G ANTIBODY; LIPOPEPTIDE; LIPOSOME; MEMBRANE PROXIMAL EXTERNAL REGION LIPOPEPTIDE; MONOCLONAL ANTIBODY 2F5; MONOCLONAL ANTIBODY 4E10; NEUTRALIZING ANTIBODY; NITRATE; PHOSPHATE; PHOSPHOLIPID; THREONINE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; BINDING AFFINITY; CHEMICAL MODIFICATION; CIRCULAR DICHROISM; CONTROLLED STUDY; DRUG DESIGN; DRUG SCREENING; DRUG STRUCTURE; DRUG SYNTHESIS; HYDROPHILICITY; IMMUNOGENICITY; NONHUMAN; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN SECONDARY STRUCTURE; RABBIT; SURFACE PLASMON RESONANCE; VIRUS NEUTRALIZATION;

EID: 84872234727     PISSN: 15566811     EISSN: 1556679X     Source Type: Journal    
DOI: 10.1128/CVI.00615-12     Document Type: Article

References (63)

1. Liu J, O'Brien K, Lynch D, Simmons N, La Porte A, Riggs A, Abbink P, Coffey R, Grandpre L, Seaman M, Landucci G, Forthal D, Montefiori DC, Carville A, Mansfield K, Havenga M, Pau M, Goudsmit J, Barouch D. 2009. Immune control of an SIV challange by a T-cell-based vaccine in rhesus monkeys. Nature 457:87-91.
2. Montefiori DC, Karnasuta C, Huang Y, Ahmed H, Gilbert P, de Souza MS, McLinden R, Tovanabutra S, Laurence-Chenine A, Sanders-Buell E, Moody MA, Bonsignori M, Ochsenbauer C, Kappes J, Tang H, Greene K, Gao H, LaBranche CC, Andrews C, Polonis VR, Rerks-Ngarm S, Pitisuttithum P, Nitayaphan S, Kaewkungwal J, Self SG, Berman PW, Francis D, Sinangil F, Lee C, Tartaglia J, Robb ML, Haynes BF, Michael NL, Kim JH. 2012. Magnitude and breadth of the neutralizing antibody response in the RV144 and Vax003 HIV-1 vaccine efficacy trials. J. Infect. Dis. 206:431-441.
3. Walker B, Burton DR. 2008. Toward an AIDS vaccine. Science 320:760-764.
4. Fauci AS. 2007. The release of new data from the HVTN 502 (STEP) HIV vaccine study. In National Institutes of Health (NIH) news, 7 November. National Institutes of Health, Bethesda, MD.
5. 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, Francis DP, Stablein D, Birx DL, Chunsuttiwat S, Khamboonruang C, Thongcharoen P, Robb ML, Michael NL, Kunasol P, Kim JH, Investigators MOPH-TAVEG. 2009. Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand. N. Engl. J. Med. 361:2209-2220.
6. Bianchi E, Joyce JG, Miller MD, Finnefrock AC, Liang X, Finotto M, Ingallinella P, McKenna P, Citron M, Ottinger E, Hepler RW, Hrin R, Nahas D, Wu C, Montefiori DC, Shiver JW, Pessi A, Kim PS. 2010. Vaccination with peptide mimetics of the gp41 prehairpin fusion intermediate yields neutralizing antisera against HIV-1 isolates. Proc. Natl. Acad. Sci. U. S. A. 107:10655-10660.
7. Corti D, Langedjik JP, Hinz A, Seaman MS, Vanzetta F, Fernandez-Rodriguez BM, Silacci C, Pinna D, Jarrossay D, Balla-Jhagjhoorsingh S, Willems B, Zekveld MJ, Dreja H, O'Sullivan E, Prade C, Orkin C, Jeffs SA, Montefiori DC, Davis D, Weissenhorn W, McKnight A, Heeney JL, Sallusto F, Sattentau QJ, Weiss RA, Lanzavecchia A. 2010. Analysis of memory B cell responses and isolation of novel monoclonal antibodies with neutralizing breadth from HIV-1 infected individuals. PLoS One 5:e8805. doi:10.1371/journal.pone.0008805.
8. Karlsson Hedestam G, Fouchier R, Phogat S, Burton D, Sodroski J, Wyatt R. 2008. The challenges of eliciting neutralizing antibodies to HIV-1 and to influenza virus. Nat. Rev. Microbiol. 6:143-155.
9. Scheid JF, Mouquet H, Ueberheide B, Diskin R, Klein F, Oliviera TYK, Pietzsch J, Fenyo D, Abadir A, Velinzon K, Hurley A, Myung S, Boulard F, Poignard P, Burton DR, Pereyra F, Ho DD, Walker BD, Seaman MS, Bjorkman PJ, Chait BT, Nussenzweig MC. 2011. Sequence and structural convergence of broad and potent HIV antibodies that mimic CD4 binding. Science 333:1633-1637.
10. Walker LM, Phogat SK, Chan-Hui PY, Wagner D, Phung P, Gross JL, Wrin T, Simek MD, Fling S, Mitcham JL, Lehrman JK, Priddy FH, Olsen OA, Frey SM, Hammond PW, Kaminsky S, Zamb T, Moyle M, Koff WC, Poignard P, Burton DR. 2009. Broad and potent neutralizing antibodies from an African donor reveal a new HIV-1 vaccine target. Science 326:285-289.
11. Wu X, Yang ZY, Li Y, Hogerkorp CM, Schief WR, Seaman MS, Zhou T, Schmidt SD, Wu L, Xu L, Longo NS, McKee K, O'Dell S, Louder MK, Wycuff DL, Feng Y, Nason M, Doria-Rose N, Connors M, Kwong PD, Roederer M, Wyatt RT, Nabel GJ, Mascola JR. 2010. Rational design of envelope identifies broadly neutralizing human monoclonal antibodies to HIV-1. Science 329:856-861.
12. Zhu Z, Qin HR, Chen W, Zhao Q, Shen X, Schutte R, Wang Y, Ofek G, Streaker E, Prabakaran P, Fouda GG, Liao HX, Owens J, Louder M, Yang Y, Klaric KA, Moody MA, Mascola JR, Scott JK, Kwong PD, Montefiori D, Haynes BF, Tomaras GD, Dimitrov DS. 2011. Crossreactive HIV-1 neutralizing human monoclonal antibodies identified from a patient with 2F5-like antibodies. J. Virol. 85:11401-11408.
13. Montero M, van Houten N, Wang X, Scott JK. 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. 72:54-85.
14. Manrique A, Rusert P, Joos B, Fischer M, Kuster H, Leemann C, Niederost B, Weber R, Stiegler G, Katinger H, Gunthard H, Trkola A. 2007. In vivo and in vitro escape from neutralizing antibodies 2G12, 2F5, and 4E10. J. Virol. 81:8793-8808.
15. Salzwedel K, Johnston P, Roberts S, Dubay J, Hunter E. 1999. A conserved tryptophan-rich 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.
16. Zwick MB, Labrijn AF, Wang M, Spenlehauer C, Saphire EO, Binley JM, Moore JP, Steigler G, Katinger H, Burton DR, Parren PW. 2001. Broadly neutralizing antibodies targeted to the membrane-proximal external region of human immunodeficiency virus type 1 glycoprotein gp41. J. Virol. 75:10892-10905.
17. Arnold G, Velasco P, Holmes A, Wrin T, Geisler S, Phung P, Tian Y, Resnick D, Ma X, Mariano T, Petropoulos C, Taylor J, Katinger H, Arnold E. 2009. Broad neutralization of HIV-1 elicited from human rhinoviruses that display the HIV-1 gp41 ELDKWA epitope. J. Virol. 83:5087-5100.
18. Matyas GR, Wieczorek L, Beck Z, Ochsenbauer-Jambor C, Kappes JC, Michael NL, Polonis VR, Alving CR. 2009. Neutralizing antibodies induced by liposomal HIV-1 glycoprotein 41 peptide simultaneously bind to both the 2F5 or 4E10 epitope and lipid epitopes. AIDS 23:2069-2075.
19. Ye L, Wen Z, Dong K, Wang X, Bu Z, Zhang H, Compans RW, Yang C. 2011. Induction of HIV neutralizing antibodies against the MPER of the HIV envelope protein by HA/gp41 chimeric protein-based DNA and VLP vaccines. PLoS One 6:e14813. doi:10.1371/journal.pone.0014813.
20. Kim M, Qiao L, Yu J, Montefiori DC, Reinherz EL. 2007. Immunogenicity of recombinant human immunodeficiency virus type 1-like particles expressing gp41 derivatives in a pre-fusion state. Vaccine 25:5102-5114.
21. Law M, Cardoso RM, Wilson IA, Burton DR. 2007. Antigenic and immunogenic study of membrane-proximal external region-grafted gp120 antigens by a DNA prime-protein boost immunization strategy. J. Virol. 81:4272-4285.
22. Li Y, Svehla K, Louder M, Wycuff D, Phogat S, Tang M, Migueles S, Wu X, Phogat X, Shaw GM, Connors M, Hoxie J, Mascola J, Wyatt R. 2009. Analysis of neutralization specificities in polyclonal sera derived from human immunodeficiency virus type 1-infected individuals. J. Virol. 83:1045-1059.
23. Haynes BF, Alam SM. 2008. HIV-1 hides an Achilles' heel in virion lipids. Immunity 28:10-12.
24. Zwick M. 2005. The membrane-proximal external region of HIV-1 gp41: a vaccine target worth exploring. AIDS 19:1725-1737.
25. Alam SM, Morelli M, Dennison SM, Liao HX, Zhang R, Xia SM, Rits-Volloch S, Sun L, Harrison SC, Haynes BF, Chen B. 2009. Role of HIV membrane in neutralization by two broadly neutralizing antibodies. Proc. Natl. Acad. Sci. U. S. A. 106:20234-20239.
26. Brown BK, Karasavvas N, Beck Z, Matyas GR, Birx DL, Polonis VR, Alving CR. 2007. Monoclonal antibodies to phosphatidylinositol phosphate neutralize human immunodeficiency virus type 1: role of phosphate-binding subsites. J. Virol. 81:2087-2091.
27. Haynes BF, Fleming J, St Clair E, Katinger H, Stiegler G, Kunert R, Robinson J, Scearce RM, Plonk K, Staats HF, Ortel TL, Liao HX, Alam SM. 2005. Cardiolipin polyspecific autoreactivity in two broadly neutralizing HIV-1 antibodies. Science 208:1906-1908.
28. Matyas G, Beck Z, Karasavvas N, Alving CR. 2008. Lipid binding properties of 4E10, 2F5, and WR304 monoclonal antibodies that neutralize HIV-1. Biochim. Biophys. Acta 1788:660-665.
29. Ofek G, McKee K, Yang Y, Yang ZY, Skinner J, Guenaga FJ, Wyatt R, Zwick MB, Nabel GJ, Mascola JR, Kwong PD. 2010. Relationship between antibody 2F5 neutralization of HIV-1 and hydrophobicity of its heavy chain third complementarity-determining region. J. Virol. 84:2955-2962.
30. Meffre E, Milili M, Blanco-Betancourt C, Antunes H, Nussenzweig M, Schiff C. 2001. Immunoglobulin heavy chain expression shapes the B cell receptor repertoire in human B cell development. J. Clin. Invest. 108:879-886.
31. Armbruster C, Stiegler GM, Vcelar BA, Jager W, Michael NL, Vetter N, Kattinger HW. 2002. A phase I trial with two human monoclonal antibodies (hMAb 2F5, 2G12) against HIV-1. AIDS 16:227-233.
32. Armbruster C, Stiegler GM, Vcelar BA, Jager W, Koller U, Jilch R, Ammann CG, Pruenster M, Stoiber H, Katinger HW. 2004. Passive immunization with the anti-HIV-1 human monoclonal antibody (hMAb) 4E10 and the hMAb combination 4E10/2F5/2G12. J. Antimicrob. Chemother. 54:915-920.
33. Hessell AJ, Rakasz EG, Tahrani DM, Huber M, Weisgrau KL, Landucci G, Forthal DN, Koff WC, Poignard P, Watkins DI, Burton DR. 2010. Broadly neutralizing monoclonal antibodies 2F5 and 4E10 directed against the human immunodeficiency virus type 1 gp41 membrane-proximal external region protect against mucosal challenge by simian-human immunodeficiency virus SHIVBa-L. J. Virol. 84:1302-1313.
34. Joos B, Trkola A, Kuster H, Aceto L, Fischer M, Steigler G, Armbruster C, Vcelar B, Katinger H, Gunthard HF. 2006. Long-term multiple dose pharmacokinetics of human monoclonal antibodies (MAbs) against human immunodeficiency virus type 1 envelope gp120 (MAb 2G12) and gp41 (MAbs 4E10 and 2F5). Antimicrob. Agents Chemother. 50:1773-1779.
35. Mehandru S, Vcelar B, Wrin T, Steigler G, Joos B, Mohri H, Boden D, Galovich J, Tenner-Racz K, Racz P, Carrington M, Petropoulos C, Katinger H, Markowitz M. 2007. Adjunctive passive immunotherapy in human immunodeficiency virus type 1-infected individuals treated with antiviral therapy during acute and early infection. J. Virol. 81:11016-11031.
36. Vcelar B, Steigler G, Wolf HM, Muntean W, Leschnik B, Mehandru S, Markowitz M, Armbruster C, Kunert R, Eibl MM, Katinger H. 2007. Reassessment of autoreactivity of the broadly neutralizing HIV antibodies 4E10 and 2F5 and retrospective analysis of clinical safety data. AIDS 21:2161-2170.
37. Apellaniz B, Garcia-Saez AJ, Huarte N, Kunert R, Vorauer-Uhl K, Katinger H, Schwille P, Nieva JL. 2010. Confocal microscopy of giant vesicles supports the absence of HIV-1 neutralizing 2F5 antibody reactivity to plasma membrane phospholipids. FEBS Lett. 584:1591-1596.
38. Xu J, Gorny MK, Palker T, Karwowska S, Zolla-Pazner S. 1991. Epitope mapping of two immunodominant domains of gp41, the transmembrane protein of human immunodeficiency virus type 1, using ten human monoclonal antibodies. J. Virol. 65:4832-4838.
39. Chan DC, Kim PS. 1998. HIV entry and its inhibition. Cell 93:681-684.
40. Alam SM, Scearce RM, Parks RJ, Plonk K, Plonk SG, Sutherland LL, Gorny MK, Zolla-Pazner S, Vanleeuwen S, Moody MA, Xia SM, Montefiori DC, Tomaras GD, Weinhold JK, Karim SA, Hicks CB, Liao HX, Robinson J, Shaw GM, Haynes BF. 2008. Human immunodeficiency virus type 1 gp41 antibodies that mask the membrane proximal region epitopes: antibody binding kinetics, induction, and potential for regulation in acute infection. J. Virol. 82:115-125.
41. Xiao X, Chen W, Feng Y, Zhu Z, Prabakaran P, Wang Y, Zhang MY, Longo NS, Dimitrov DS. 2009. Germline-like predecessors of broadly neutralizing antibodies lack measurable binding to HIV-1 envelope glycoproteins: implications for evasion of immune responses and design of vaccine immunogens. Biochem. Biophys. Res. Commun. 390:404-409.
42. Pietzsch J, Scheid JF, Mouquet H, Seaman MS, Broder CC, Nussenzweig MC. 2010. Anti-gp41 antibodies cloned from HIV-infected patients with broadly neutralizing serologic activity. J. Virol. 84:5032-5042.
43. Ofek G, Tang M, Sambor A, Katinger H, Mascola JR, Wyatt R, Kwong PD. 2004. Structure and mechanistic analysis of the anti-human immunodeficiency virus type 1 antibody 2F5 in complex with its gp41 epitope. J. Virol. 78:10724-10737.
44. Anderton S. 2004. Post-translational modifications of self antigens: implications for autoimmunity. Curr. Opin. Immunol. 16:753-758.
45. Dhiman M, Estrada-Franco JG, Pando JM, Ramirez-Aguilar FJ, Spratt H, Vazquez-Corzo S, Perez-Molina G, Gallegos-Sandoval R, Moreno R, Garg NJ. 2009. Increased myeloperoxidase activity and protein nitration are indicators of inflammation in patients with Chagas' disease. Clin. Vaccine Immunol. 16:660-666.
46. Doyle H, Mamula M. 2001. Post-translational protein modifications in antigen recognition and autoimmunity. Trends Immunol. 22:443-449.
47. Ohmori H, Oka M, Nishikawa Y, Shigemitsu H, Takeuchi M, Magari M, Kanayama N. 2005. Immunogenicity of autologous IgG bearing the inflammation-associated marker 3-nitrotyrosine. Immunol. Lett. 96:47-54.
48. Semballa S, Geffard M, Daulouede S, Malvy D, Veyret B, Lemesre J, Holzmuller P, Mnaimneh S, Vincendeau P. 2004. Antibodies directed against nitrosylated neoepitopes in sera of patients with human African trypanosomiasis. Trop. Med. Int. Health 9:1104-1110.
49. Wegner N, Lundberg K, Kinloch A, Fischer B, Malmstrom V, Feldmann M, Venables PJ. 2010. Autoimmunity to specific citrullinated proteins gives the first clues to the etiology of rheumatoid arthritis. Immunol. Rev. 233:34-54.
50. Watson DS, Platt VM, Cao L, Venditto VJ, Szoka FC. 2011. Antibody response in mice to polyhistidine-tagged peptide and protein antigens attached to liposomes via lipid-linked nitrilotriacetic acid. Clin. Vaccine Immunol. 18:289-297.
51. Watson D, Szoka FC. 2009. Role of lipid structure in the humoral immune response in mice to covalent lipid-peptides from the membrane proximal region of HIV-1 gp41. Vaccine 27:4672-4683.
52. Taylor J, Kaiser E. 1987. Structure-function analysis of proteins through the design, synthesis and study of peptide models. Methods Enzymol. 154:473-498.
53. Muderwha JM, Matyas GR, Spitler LE, Alving CR. 1999. Oil-in-water liposomal emulsions: characterization and potential use in vaccine delivery. J. Pharm. Sci. 88:1332-1339.
54. Li M, Gao F, Mascola JR, Stamatatos L, Polonis VR, Koutsoukos M, Voss G, Goepfert P, Gilbert P, Greene KM, Bilska M, Kothe DL, Salazar-Gonzalez JF, Wei X, Decker JM, Hahn BM, Montefiori DC. 2005. Human immunodeficiency virus type 1 env clones from acute and early subtype B infections for standardized assessments of vaccine-elicited neutralizing antibodies. J. Virol. 79:10108-10125.
55. Edmonds TG, Ding H, Yuan X, Conway JA, Smith K, West J, Montefiori DC, Kappes JC, Ochsenbauer C. 2010. Replication competent molecular clones of HIV-1 expressing Renilla luciferase facilitate the analysis of antibody inhibition in PBMC. Virology 408:1-13.
56. Marusic C, Rizza P, Lattanzi L, Mancini C, Spada M, Belardelli F, Benvenuto E, Capone I. 2001. Chimeric plant virus particles as immunogens for inducing murine and human immune responses against human immunodeficiency virus type 1. J. Virol. 75:8434-8439.
57. Muster T, Guinea R, Trkola A, Purtscher M, Klima A, Steindl F, Palese P, Katinger H. 1994. Cross-neutralizing activity against divergent human immunodeficiency virus type 1 isolates induced by the gp41 sequence ELDKWAS. J. Virol. 68:4031-4034.
58. Cardoso RM, Brunel FM, Ferguson S, Zwick M, Burton DR, Dawson PE, Wilson IA. 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.
59. Alam SM, McAdams M, Boren D, Rak M, Scearce RM, Gao F, Camacho ZT, Gewirth D, Kelsoe G, Chen P, Haynes BF. 2007. The role of antibody polyspecificity and lipid reactivity in binding of broadly neutralizing anti-HIV-1-envelope human monoclonal antibodies 2F5 and 4E10 to glycoprotein 41 membrane proximal envelope epitopes. J. Immunol. 178:4424-4435.
60. Cardoso RMF, Zwick MB, Stanfield RL, Kunert R, Binley JM, Katinger H, Burton DR, Wilson IA. 2005. Broadly neutralizing anti-HIV antibody 4E10 recognizes a helical conformation of a highly conserved fusion-associated motif in gp41. Immunity 22:163-173.
61. Ingale S, Gach JS, Zwick MB, Dawson PE. 2010. Synthesis and analysis of the membrane proximal external region epitopes of HIV-1. J. Pept. Sci. 16:716-722.
62. Kim M, Sun ZY, Rand KD, Shi X, Song L, Cheng Y, Fahmy AF, Majumdar S, Ofek G, Yang Y, Kwong PD, Wang JH, Engen JR, Wagner G, Reinherz EL. 2011. Antibody mechanics on a membrane-bound HIV segment essential for GP41-targeted viral neutralization. Nat. Struct. Mol. Biol. 18:1235-1243.
63. Gauba V, Grunewald J, Gourney V, Deaton LM, Kang M, Bursulaya B, Ou W, Lerner RA, Schmedt C, Geierstanger BH, Schultz PG, Ramirez-Montagut T. 2011. Loss of CD4 T-cell-dependent tolerance to proteins with modified amino acids. Proc. Natl. Acad. Sci. U. S. A. 108:12821-12826.