Virus like particle based strategy to elicit HIV-protective antibodies to the alpha-helic regions of gp41

Virology

Volumn 431, Issue 1-2, 2012, Pages 1-11

  Pastori, C ^a   Tudor, D ^b   Diomede, L ^a   Drillet, A S ^b   Jegerlehner, A ^c   Rohn T A ^c,d   Bomsel, M ^b   Lopalco, L ^a  

^a SAN RAFFAELE HOSPITAL   (Italy)

^b INSTITUT COCHIN   (France)

^c CYTOS BIOTECHNOLOGY AG   (Switzerland)

^d NOVARTIS PHARMA AG   (Switzerland)

Author keywords

ADCC; Gp41; HIV; Neutralizing antibodies; VLP

Indexed keywords

AMINO ACID; EPITOPE; GLYCOPROTEIN GP 41; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY; IMMUNOGLOBULIN G; PEPTIDE; PROTEIN AP205; PROTEIN AP205 3 13; PROTEIN AP205 3 17; PROTEIN AP205 3 20; PROTEIN AP205 3 24; PROTEIN AP205 P1; PROTEIN AP205 P8; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTIBODY SPECIFICITY; ANTIBODY TITER; ARTICLE; BACTERIOPHAGE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DRUG CONJUGATION; FEMALE; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; HUMORAL IMMUNITY; IMMUNOGENICITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; VIRUS LIKE AGENT;

AIDS VACCINES; ANIMALS; BACTERIOPHAGES; CYTOTOXICITY TESTS, IMMUNOLOGIC; DRUG CARRIERS; FEMALE; GENETIC VECTORS; HIV ANTIBODIES; HIV ENVELOPE PROTEIN GP41; HIV-1; IMMUNOGLOBULIN G; MICE; MICE, INBRED BALB C; VACCINES, SYNTHETIC; VACCINES, VIROSOME;

HUMAN IMMUNODEFICIENCY VIRUS 1; MUS;

EID: 84862309329     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2012.05.005     Document Type: Article

References (44)

1. Alam S.M., Scearce R.M., Parks R.J., Plonk K., Plonk S.G., Sutherland L.L., Gorny M.K., Zolla-Pazner S., Vanleeuwen S., Moody M.A., Xia S.M., Montefiori D.C., Tomaras G.D., Weinhold K.J., Karim S.A., Hicks C.B., Liao H.X., Robinson J., Shaw G.M., Haynes B.F. Human immunodeficiency virus type 1 gp41 antibodies that mask membrane proximal region epitopes: antibody binding kinetics, induction, and potential for regulation in acute infection. J. Virol. 2008, 82(1):115-125.
2. Bachmann M.F., Zinkernagel R.M. Neutralizing antiviral B cell responses. Annu. Rev. Immunol. 1997, 15:235-270.
3. Bomsel M., Tudor D., Drillet A.S., Alfsen A., Ganor Y., Roger M.G., Mouz N., Amacker M., Chalifour A., Diomede L., Devillier G., Cong Z., Wei Q., Gao H., Qin C., Yang G.B., Zurbriggen R., Lopalco L., Fleury S. Immunization with HIV-1 gp41 subunit virosomes induces mucosal antibodies protecting nonhuman primates against vaginal SHIV challenges. Immunity 2011, 34(2):269-280.
4. Chakrabarti B.K., Walker L.M., Guenaga J.F., Ghobbeh A., Poignard P., Burton D.R., Wyatt R.T. Direct antibody access to the HIV-1 membrane-proximal external region positively correlates with neutralization sensitivity. J. Virol. 2011, 85(16):8217-8226.
5. Cielens I., Ose V., Petrovskis I., Strelnikova A., Renhofa R., Kozlovska T., Pumpens P. Mutilation of RNA phage Qbeta virus-like particles: from icosahedrons to rods. FEBS Lett. 2000, 482(3):261-264.
6. Clerici M., Barassi C., Devito C., Pastori C., Piconi S., Trabattoni D., Longhi R., Hinkula J., Broliden K., Lopalco L. Serum IgA of HIV-exposed uninfected individuals inhibit HIV through recognition of a region within the alpha-helix of gp41. AIDS 2002, 16(13):1731-1741.
7. Diomede L., Nyoka S., Pastori C., Scotti L., Zambon A., Sherman G., Gray C.M., Sarzotti-Kelsoe M., Lopalco L. Passively transmitted gp41 antibodies in babies born from HIV-1 subtype C-seropositive women: correlation between fine specificity and protection. J. Virol. 2012, 86(8):4129-4138.
8. Fehr T., Bachmann M.F., Bucher E., Kalinke U., Di Padova F.E., Lang A.B., Hengartner H., Zinkernagel R.M. Role of repetitive antigen patterns for induction of antibodies against antibodies. J. Exp. Med. 1997, 185(10):1785-1792.
9. Ferrantelli F., Rasmussen R.A., Buckley K.A., Li P.L., Wang T., Montefiori D.C., Katinger H., Stiegler G., Anderson D.C., McClure H.M., Ruprecht R.M. Complete protection of neonatal rhesus macaques against oral exposure to pathogenic simian-human immunodeficiency virus by human anti-HIV monoclonal antibodies. J. Infect. Dis. 2004, 189(12):2167-2173.
10. Gamvrellis A., Leong D., Hanley J.C., Xiang S.D., Mottram P., Plebanski M. Vaccines that facilitate antigen entry into dendritic cells. Immunol. Cell Biol. 2004, 82(5):506-516.
11. Gray E.S., Moore P.L., Choge I.A., Decker J.M., Bibollet-Ruche F., Li H., Leseka N., Treurnicht F., Mlisana K., Shaw G.M., Karim S.S., Williamson C., Morris L. Neutralizing antibody responses in acute human immunodeficiency virus type 1 subtype C infection. J. Virol. 2007, 81(12):6187-6196.
12. Guevara H., Casseb J., Zijenah L.S., Mbizvo M., Oceguera L.F., Hanson C.V., Katzenstein D.A., Hendry R.M. Maternal HIV-1 antibody and vertical transmission in subtype C virus infection. J. Acquir. Immune Defic. Syndr. 2002, 29(5):435-440.
13. Hinton H.J., Jegerlehner A., Bachmann M.F. Pattern recognition by B cells: the role of antigen repetitiveness versus Toll-like receptors. Curr. Top. Microbiol. Immunol. 2008, 319:1-15.
14. Jain S., Patrick A.J., Rosenthal K.L. Multiple tandem copies of conserved gp41 epitopes incorporated in gag virus-like particles elicit systemic and mucosal antibodies in an optimized heterologous vector delivery regimen. Vaccine 2010, 28(43):7070-7080.
15. Jain S., Rosenthal K.L. The gp41 epitope, QARVLAVERY, is highly conserved and a potent inducer of IgA that neutralizes HIV-1 and inhibits viral transcytosis. Mucosal Immunol. 2011, 4(5):539-553.
16. Jegerlehner A., Maurer P., Bessa J., Hinton H.J., Kopf M., Bachmann M.F. TLR9 signaling in B cells determines class switch recombination to IgG2a. J. Immunol. 2007, 178(4):2415-2420.
17. Jennings G.T., Bachmann M.F. The coming of age of virus-like particle vaccines. Biol. Chem. 2008, 389(5):521-536.
18. Kaul R., Plummer F., Clerici M., Bomsel M., Lopalco L., Broliden K. Mucosal IgA in exposed, uninfected subjects: evidence for a role in protection against HIV infection. AIDS 2001, 15(3):431-432.
19. Kirchherr J.L., Hamilton J., Lu X., Gnanakaran S., Muldoon M., Daniels M., Kasongo W., Chalwe V., Mulenga C., Mwananyanda L., Musonda R.M., Yuan X., Montefiori D.C., Korber B.T., Haynes B.F., Gao F. Identification of amino acid substitutions associated with neutralization phenotype in the human immunodeficiency virus type-1 subtype C gp120. Virology 2011, 409(2):163-174.
20. Klovins J., Overbeek G.P., van den Worm S.H., Ackermann H.W., van Duin J. Nucleotide sequence of a ssRNA phage from Acinetobacter: kinship to coliphages. J. Gen. Virol. 2002, 83(Part 6):1523-1533.
21. Koning R., van den Worm S., Plaisier J.R., van Duin J., Pieter Abrahams J., Koerten H. Visualization by cryo-electron microscopy of genomic RNA that binds to the protein capsid inside bacteriophage MS2. J. Mol. Biol. 2003, 332(2):415-422.
22. Kratz P.A., Bottcher B., Nassal M. Native display of complete foreign protein domains on the surface of hepatitis B virus capsids. Proc. Natl. Acad. Sci. USA 1999, 96(5):1915-1920.
23. Lallemant M., Baillou A., Lallemant-Le Coeur S., Nzingoula S., Mampaka M., M'Pele P., Barin F., Essex M. Maternal antibody response at delivery and perinatal transmission of human immunodeficiency virus type 1 in African women. Lancet 1994, 343(8904):1001-1005.
24. Lang R., Winter G., Vogt L., Zurcher A., Dorigo B., Schimmele B. Rational design of a stable, freeze-dried virus-like particle-based vaccine formulation. Drug Dev. Ind. Pharm. 2009, 35(1):83-97.
25. Lynch R.M., Rong R., Boliar S., Sethi A., Li B., Mulenga J., Allen S., Robinson J.E., Gnanakaran S., Derdeyn C.A. The B cell response is redundant and highly focused on V1V2 during early subtype C infection in a Zambian seroconverter. J. Virol. 2011, 85(2):905-915.
26. Ma B.J., Alam S.M., Go E.P., Lu X., Desaire H., Tomaras G.D., Bowman C., Sutherland L.L., Scearce R.M., Santra S., Letvin N.L., Kepler T.B., Liao H.X., Haynes B.F. Envelope deglycosylation enhances antigenicity of HIV-1 gp41 epitopes for both broad neutralizing antibodies and their unmutated ancestor antibodies. PLoS Pathog. 2011, 7(9):e1002200.
27. Moore P.L., Gray E.S., Morris L. Specificity of the autologous neutralizing antibody response. Curr. Opin. HIV AIDS 2009, 4(5):358-363.
28. Moore P.L., Ranchobe N., Lambson B.E., Gray E.S., Cave E., Abrahams M.R., Bandawe G., Mlisana K., Abdool Karim S.S., Williamson C., Morris L. Limited neutralizing antibody specificities drive neutralization escape in early HIV-1 subtype C infection. PLoS Pathog. 2009, 5(9):e1000598.
29. Morris L., Chen X., Alam M., Tomaras G., Zhang R., Marshall D.J., Chen B., Parks R., Foulger A., Jaeger F., Donathan M., Bilska M., Gray E.S., Abdool Karim S.S., Kepler T.B., Whitesides J., Montefiori D., Moody M.A., Liao H.X., Haynes B.F. Isolation of a human anti-HIV gp41 membrane proximal region neutralizing antibody by antigen-specific single B cell sorting. PLoS One 2011, 6(9):e23532.
30. Peabody D.S. Translational repression by bacteriophage MS2 coat protein expressed from a plasmid. A system for genetic analysis of a protein-RNA interaction. J. Biol. Chem. 1990, 265(10):5684-5689.
31. Rohn T.A., Ralvenius W.T., Paul J., Borter P., Hernandez M., Witschi R., Grest P., Zeilhofer H.U., Bachmann M.F., Jennings G.T. A virus-like particle-based anti-nerve growth factor vaccine reduces inflammatory hyperalgesia: potential long-term therapy for chronic pain. J. Immunol. 2011, 186(3):1769-1780.
32. Rong R., Bibollet-Ruche F., Mulenga J., Allen S., Blackwell J.L., Derdeyn C.A. Role of V1V2 and other human immunodeficiency virus type 1 envelope domains in resistance to autologous neutralization during clade C infection. J. Virol. 2007, 81(3):1350-1359.
33. Rong R., Li B., Lynch R.M., Haaland R.E., Murphy M.K., Mulenga J., Allen S.A., Pinter A., Shaw G.M., Hunter E., Robinson J.E., Gnanakaran S., Derdeyn C.A. Escape from autologous neutralizing antibodies in acute/early subtype C HIV-1 infection requires multiple pathways. PLoS Pathog. 2009, 5(9):e1000594.
34. Ruprecht R.M., Hofmann-Lehmann R., Smith-Franklin B.A., Rasmussen R.A., Liska V., Vlasak J., Xu W., Baba T.W., Chenine A.L., Cavacini L.A., Posner M.R., Katinger H., Stiegler G., Bernacky B.J., Rizvi T.A., Schmidt R., Hill L.R., Keeling M.E., Montefiori D.C., McClure H.M. Protection of neonatal macaques against experimental SHIV infection by human neutralizing monoclonal antibodies. Transfus. Clin. Biol. 2001, 8(4):350-358.
35. Spohn G., Jennings G.T., Martina B.E., Keller I., Beck M., Pumpens P., Osterhaus A.D., Bachmann M.F. A VLP-based vaccine targeting domain III of the West Nile virus E protein protects from lethal infection in mice. Virol. J. 2010, 7:146.
36. Spohn G., Schwarz K., Maurer P., Illges H., Rajasekaran N., Choi Y., Jennings G.T., Bachmann M.F. Protection against osteoporosis by active immunization with TRANCE/RANKL displayed on virus-like particles. J. Immunol. 2005, 175(9):6211-6218.
37. Tissot A.C., Maurer P., Nussberger J., Sabat R., Pfister T., Ignatenko S., Volk H.D., Stocker H., Muller P., Jennings G.T., Wagner F., Bachmann M.F. Effect of immunisation against angiotensin II with CYT006-AngQb on ambulatory blood pressure: a double-blind, randomised, placebo-controlled phase IIa study. Lancet 2008, 371(9615):821-827.
38. Tissot A.C., Renhofa R., Schmitz N., Cielens I., Meijerink E., Ose V., Jennings G.T., Saudan P., Pumpens P., Bachmann M.F. Versatile virus-like particle carrier for epitope based vaccines. PLoS One 2010, 5(3):e9809.
39. Tudor D., Bomsel M. The broadly neutralizing HIV-1 IgG 2F5 elicits gp41-specific antibody-dependent cell cytotoxicity in a FcgammaRI-dependent manner. AIDS 2011, 25(6):751-759.
40. Tudor D., Derrien M., Diomede L., Drillet A.S., Houimel M., Moog C., Reynes J.M., Lopalco L., Bomsel M. HIV-1 gp41-specific monoclonal mucosal IgAs derived from highly exposed but IgG-seronegative individuals block HIV-1 epithelial transcytosis and neutralize CD4(+) cell infection: an IgA gene and functional analysis. Mucosal Immunol. 2009, 2(5):412-426.
41. van den Worm S.H., Koning R.I., Warmenhoven H.J., Koerten H.K., van Duin J. Cryo electron microscopy reconstructions of the Leviviridae unveil the densest icosahedral RNA packing possible. J. Mol. Biol. 2006, 363(4):858-865.
42. Zhou M., Kostoula I., Brill B., Panou E., Sakarellos-Daitsiotis M., Dietrich U. Prime boost vaccination approaches with different conjugates of a new HIV-1 gp41 epitope encompassing the membrane proximal external region induce neutralizing antibodies in mice. Vaccine 2012, 30(11):1911-1916.
43. Zhu P., Liu J., Bess J., Chertova E., Lifson J.D., Grise H., Ofek G.A., Taylor K.A., Roux K.H. Distribution and three-dimensional structure of AIDS virus envelope spikes. Nature 2006, 441(7095):847-852.
44. Zwick M.B., Labrijn A.F., Wang M., Spenlehauer C., Saphire E.O., Binley J.M., Moore J.P., Stiegler G., Katinger H., Burton D.R., Parren P.W. Broadly neutralizing antibodies targeted to the membrane-proximal external region of human immunodeficiency virus type 1 glycoprotein gp41. J. Virol. 2001, 75(22):10892-10905.