Resistance to antibody neutralization in HIV-2 infection occurs in late stage disease and is associated with X4 tropism

AIDS

Volumn 26, Issue 18, 2012, Pages 2275-2284

  Marcelino, José M ^a,c   Borrego, Pedro ^b,c   Nilsson, Charlotta ^d   Família, Carlos ^b   Barroso, Helena ^b,c   Maltez, Fernando ^e   Doroana, Manuela ^f   Antunes, Francisco ^f   Quintas, Alexandre ^b   Taveira, Nuno ^b,c  

^a INSTITUTO DE HIGIENE E MEDICINA TROPICAL   (Portugal)

^b INSTITUTO SUPERIOR DE CIÊNCIAS DA SAÚDE EGAS MONIZ   (Portugal)

^c RESEARCH INSTITUTE FOR MEDICINES IMED ULISBOA   (Portugal)

^d KAROLINSKA INSTITUTE   (Sweden)

^e HOSPITAL CURRY CABRAL   (Portugal)

^f HOSPITAL DE SANTA MARIA   (Portugal)

Author keywords

C2V3C3 neutralizing domains; HIV 2 infection; neutralizing antibodies and disease progression; X4 tropism and resistance to neutralizing antibodies

Indexed keywords

IMMUNOGLOBULIN G; IMMUNOGLOBULIN G ANTIBODY; NEUTRALIZING ANTIBODY;

ADULT; ANTIBODY RESPONSE; ARTICLE; CLINICAL ARTICLE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 2 INFECTION; IMMUNOGLOBULIN BLOOD LEVEL; PATHOGENESIS; PRIORITY JOURNAL; VIRAL TROPISM; VIRUS ISOLATION;

ADULT; ANTIBODIES, NEUTRALIZING; CD4 LYMPHOCYTE COUNT; DISEASE PROGRESSION; FEMALE; HIV ANTIBODIES; HIV ENVELOPE PROTEIN GP120; HIV INFECTIONS; HIV-2; HUMANS; MALE; NEUTRALIZATION TESTS; PORTUGAL; RECEPTORS, CXCR4; VIRAL TROPISM;

EID: 84870192423     PISSN: 02699370     EISSN: 14735571     Source Type: Journal    
DOI: 10.1097/QAD.0b013e328359a89d     Document Type: Article

References (60)

1. Berry N, Ariyoshi K, Jaffar S, Sabally S, Corrah T, Tedder R, Whittle H. Low peripheral blood viral HIV-2 RNA in individuals with high CD4 percentage differentiates HIV-2 from HIV-1 infection. J Hum Virol 1998;1:457-468. (Pubitemid 128543591)
2. Soares R, Foxall R, Albuquerque A, Cortesao C, Garcia M, Victorino RM, Sousa AE. Increased frequency of circulating CCR5RCD4RT cells in human immunodeficiency virus type 2 infection. J Virol 2006;80:12425-12429. (Pubitemid 44904396)
3. Marlink R, Kanki P, Thior I, Travers K, Eisen G, Siby T, et al. Reduced rate of disease development after HIV-2 infection as compared to HIV-1. Science 1994;265:1587-1590. (Pubitemid 24308975)
4. Drylewicz J, Matheron S, Lazaro E, Damond F, Bonnet F, Simon F, et al. Comparison of viro-immunological marker changes between HIV-1 and HIV-2-infected patients in France. AIDS 2008;22:457-468. (Pubitemid 351317287)
5. Cavaleiro R, Sousa AE, Loureiro A, Victorino RM. Marked immunosuppressive effects of the HIV-2 envelope protein in spite of the lower HIV-2 pathogenicity. AIDS 2000;14:2679-2686. (Pubitemid 32118721)
6. Cavaleiro R, Brunn GJ, Albuquerque AS, Victorino RM, Platt JL, Sousa AE. Monocyte-mediated T cell suppression by HIV-2 envelope proteins. Eur J Immunol 2007;37:3435-3444.
7. Grossman Z, Meier-Schellersheim M, Sousa AE, Victorino RM, Paul WE. CD4RT-cell depletion in HIV infection: are we closer to understanding the cause? Nat Med 2002;8:319-323. (Pubitemid 34407019)
8. Cavaleiro R, Baptista AP, Soares RS, Tendeiro R, Foxall RB, Gomes P, et al. Major depletion of plasmacytoid dendritic cells in HIV-2 infection: an attenuated form of HIV disease. PLoS Pathog 2009;5:e1000667.
9. Leligdowicz A, Rowland-Jones S. Tenets of protection from progression to AIDS: lessons from the immune responses to HIV-2 infection. Expert Rev Vaccines 2008;7:319-331. (Pubitemid 351520020)
10. Duvall MG, Jaye A, Dong T, Brenchley JM, Alabi AS, Jeffries DJ, et al. Maintenance of HIV-specific CD4R T cell help distinguishes HIV-2 from HIV-1 infection. J Immunol 2006;176:6973-6981. (Pubitemid 43787877)
11. Ozkaya Sahin G, Holmgren B, da Silva Z, Nielsen J, Nowroozalizadeh S, Esbjornsson J, et al. Potent intratype neutralizing activity distinguishes human immunodeficiency virus type 2 (HIV-2) from HIV-1. J Virol 2012;86:961-971.
12. Kong R, Li H, Bibollet-Ruche F, Decker JM, Zheng NN, Gottlieb GS, et al. Broad and potent neutralizing antibody responses elicited in natural HIV-2 infection. J Virol 2012;86:947-960.
13. de Silva TI, Aasa-Chapman M, Cotten M, Hue S, Robinson J, Bibollet-Ruche F, et al. Potent autologous and heterologous neutralizing antibody responses occur in HIV-2 infection across a broad range of infection outcomes. J Virol 2012;86:930-946.
14. Rodriguez SK, Sarr AD, MacNeil A, Thakore-Meloni S, Gueye-Ndiaye A, Traore I, et al. Comparison of heterologous neutralizing antibody responses of human immunodeficiency virus type 1 (HIV-1) - and HIV-2-infected Senegalese patients: distinct patterns of breadth and magnitude distinguish HIV-1 and HIV-2 infections. J Virol 2007;81:5331-5338. (Pubitemid 46744442)
15. Bjorling E, Scarlatti G, von Gegerfelt A, Albert J, Biberfeld G, Chiodi F, et al. Autologous neutralizing antibodies prevail in HIV-2 but not in HIV-1 infection. Virology 1993;193:528-530.
16. Shi Y, Brandin E, Vincic E, Jansson M, Blaxhult A, Gyllensten K, et al. Evolution of human immunodeficiency virus type 2 coreceptor usage, autologous neutralization, envelope sequence and glycosylation. J Gen Virol 2005;86:3385-3396. (Pubitemid 41685173)
17. Matsushita S, Matsumi S, Yoshimura K, Morikita T, Murakami T, Takatsuki K. Neutralizing monoclonal antibodies against human immunodeficiency virus type 2 gp120. J Virol 1995;69:3333-3340.
18. Bjorling E, Chiodi F, Utter G, Norrby E. Two neutralizing domains in the V3 region in the envelope glycoprotein gp125 of HIV type 2. J Immunol 1994;152:1952-1959. (Pubitemid 24075729)
19. Bjorling E, Broliden K, Bernardi D, Utter G, Thorstensson R, Chiodi F, Norrby E. Hyperimmune antisera against synthetic peptides representing the glycoprotein of human immunodeficiency virus type 2 can mediate neutralization and antibodydependent cytotoxic activity. Proc Natl Acad Sci U S A 1991;88:6082-6086. (Pubitemid 21914890)
20. Bottiger B, Karlsson A, Andreasson PA, Naucler A, Costa CM, Norrby E, Biberfeld G. Envelope cross-reactivity between human immunodeficiency virus types 1 and 2 detected by different serological methods: correlation between crossneutralization and reactivity against the main neutralizing site. J Virol 1990;64:3492-3499. (Pubitemid 20219555)
21. Robert-Guroff M, Aldrich K, Muldoon R, Stern TL, Bansal GP, Matthews TJ, et al. Cross-neutralization of human immunodeficiency virus type 1 and 2 and simian immunodeficiency virus isolates. J Virol 1992;66:3602-3608.
22. McKnight A, Shotton C, Cordell J, Jones I, Simmons G, Clapham PR. Location, exposure, and conservation of neutralizing and nonneutralizing epitopes on human immunodeficiency virus type 2 SU glycoprotein. J Virol 1996;70:4598-4606. (Pubitemid 26187456)
23. Marcelino JM, Borrego P, Rocha C, Barroso H, Quintas A, Novo C, Taveira N. Potent and broadly reactive HIV-2 neutralizing antibodies elicited by a vaccinia virus vector prime-C2V3C3 polypeptide boost immunization strategy. J Virol 2010;84:12429-12436.
24. Gomes P, Taveira NC, Pereira JM, Antunes F, Ferreira MO, Lourenco MH. Quantitation of human immunodeficiency virus type 2 DNA in peripheral blood mononuclear cells by using a quantitative-competitive PCR assay. J Clin Microbiol 1999;37:453-456. (Pubitemid 29056428)
25. Cavaco-Silva P, Taveira NC, Rosado L, Lourenco MH, Moniz-Pereira J, Douglas NW, et al. Virological and molecular demonstration of human immunodeficiency virus type 2 vertical transmission. J Virol 1998;72:3418-3422. (Pubitemid 28175591)
26. Thorstensson R, Walther L, Putkonen P, Albert J, Biberfeld G. A capture enzyme immunoassay for detection of HIV-2/SIV antigen. J Acquir Immune Defic Syndr 1991;4:374-379.
27. Borrego P, Calado R, Marcelino JM, Bartolo I, Rocha C, Cavaco-Silva P, et al. Baseline susceptibility of primary HIV-2 to entry inhibitors. Antivir Ther 2012;17:565-570.
28. Montefiori DC. Measuring HIV neutralization in a luciferase reporter gene assay. Methods Mol Biol 2009;485:395-405.
29. Wei X, Decker JM, Wang S, Hui H, Kappes JC, Wu X, et al. Antibody neutralization and escape by HIV-1. Nature 2003;422:307-312. (Pubitemid 36378357)
30. Arnold K, Bordoli L, Kopp J, Schwede T. The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 2006;22:195-201. (Pubitemid 43205406)
31. Kiefer F, Arnold K, Kunzli M, Bordoli L, Schwede T. The SWISSMODEL repository and associated resources. Nucleic Acids Res 2009;37:D387-392.
32. Peitsch MC, Wells TN, Stampf DR, Sussman JL. The Swiss-3DImage collection and PDB-Browser on the World-Wide Web. Trends Biochem Sci 1995;20:82-84.
33. Chen B, Vogan EM, Gong H, Skehel JJ, Wiley DC, Harrison SC. Structure of an unliganded simian immunodeficiency virus gp120 core. Nature 2005;433:834-841. (Pubitemid 40314887)
34. Kabsch W, Sander C. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 1983;22:2577-2637.
35. Joosten RP, te Beek TA, Krieger E, Hekkelman ML, Hooft RW, Schneider R, et al. A series of PDB related databases for everyday needs. Nucleic Acids Res 2010;39:D411-419.
36. Marcelino JM, Nilsson C, Barroso H, Gomes P, Borrego P, Maltez F, et al. Envelope-specific antibody response in HIV-2 infection: C2V3C3-specific IgG response is associated with disease progression. AIDS 2008;22:2257-2265.
37. Borrego P, Marcelino JM, Rocha C, Doroana M, Antunes F, Maltez F, et al. The role of the humoral immune response in the molecular evolution of the envelope C2, V3 and C3 regions in chronically HIV-2 infected patients. Retrovirology 2008;5:78.
38. Blaak H, Boers PH, Gruters RA, Schuitemaker H, van der Ende ME, Osterhaus AD. CCR5, GPR15, and CXCR6 are major coreceptors of human immunodeficiency virus type 2 variants isolated from individuals with and without plasma viremia. J Virol 2005;79:1686-1700. (Pubitemid 40459115)
39. Doria-Rose NA, Klein RM, Daniels MG, O'Dell S, Nason M, Lapedes A, et al. Breadth of human immunodeficiency virusspecific neutralizing activity in sera: clustering analysis and association with clinical variables. J Virol 2010;84:1631-1636.
40. McMichael AJ, Borrow P, Tomaras GD, Goonetilleke N, Haynes BF. The immune response during acute HIV-1 infection: clues for vaccine development. Nat Rev Immunol 2010;10:11-23.
41. Mascola JR, Montefiori DC. The role of antibodies in HIV vaccines. Annu Rev Immunol 2010;28:413-444.
42. van Gils MJ, Euler Z, Schweighardt B, Wrin T, Schuitemaker H. Prevalence of cross-reactive HIV-1-neutralizing activity in HIV-1-infected patients with rapid or slow disease progression. AIDS 2009;23:2405-2414.
43. van Gils MJ, Edo-Matas D, Schweighardt B, Wrin T, Schuitemaker H. High prevalence of neutralizing activity against multiple unrelated human immunodeficiency virus type 1 (HIV-1) subtype B variants in sera from HIV-1 subtype B-infected individuals: evidence for subtype-specific rather than strain-specific neutralizing activity. J Gen Virol 2010;91:250-258.
44. Foxall RB, Albuquerque AS, Soares RS, Baptista AP, Cavaleiro R, Tendeiro R, et al. Memory and naive-like regulatory CD4R T cells expand during HIV-2 infection in direct association with CD4R T-cell depletion irrespectively of viremia. AIDS 2011;25:1961-1970.
45. Lim HW, Hillsamer P, Banham AH, Kim CH. Cutting edge: direct suppression of B cells by CD4R CD25R regulatory T cells. J Immunol 2005;175:4180-4183. (Pubitemid 41361949)
46. Wollenberg I, Agua-Doce A, Hernandez A, Almeida C, Oliveira VG, Faro J, Graca L. Regulation of the germinal center reaction by foxp3R follicular regulatory T cells. J Immunol 2011;187:4553-4560.
47. Linterman MA, Pierson W, Lee SK, Kallies A, Kawamoto S, Rayner TF, et al. Foxp3Rfollicular regulatory T cells control the germinal center response. Nat Med 2011;17:975-982.
48. Richman DD, Wrin T, Little SJ, Petropoulos CJ. Rapid evolution of the neutralizing antibody response to HIV type 1 infection. Proc Natl Acad Sci U S A 2003;100:4144-4149. (Pubitemid 36418171)
49. Bunnik EM, Pisas L, van Nuenen AC, Schuitemaker H. Autologous neutralizing humoral immunity and evolution of the viral envelope in the course of subtype B human immunodeficiency virus type 1 infection. J Virol 2008;82:7932-7941.
50. Bosch KA, Rainwater S, Jaoko W, Overbaugh J. Temporal analysis of HIV envelope sequence evolution and antibody escape in a subtype A-infected individual with a broad neutralizing antibody response. Virology 2010;398:115-124.
51. Montefiori DC, Collman RG, Fouts TR, Zhou JY, Bilska M, Hoxie JA, et al. Evidence that antibody-mediated neutralization of human immunodeficiency virus type 1 by sera from infected individuals is independent of coreceptor usage. J Virol 1998;72:1886-1893. (Pubitemid 28100740)
52. Naganawa S, Yokoyama M, Shiino T, Suzuki T, Ishigatsubo Y, Ueda A, et al. Net positive charge of HIV-1 CRF01-AE V3 sequence regulates viral sensitivity to humoral immunity. PLoS One 2008;3:e3206.
53. Lusso P, Earl PL, Sironi F, Santoro F, Ripamonti C, Scarlatti G, et al. Cryptic nature of a conserved, CD4-inducible V3 loop neutralization epitope in the native envelope glycoprotein oligomer of CCR5-restricted, but not CXCR4-using, primary human immunodeficiency virus type 1 strains. J Virol 2005;79:6957-6968. (Pubitemid 40677327)
54. McKnight A, Clapham PR. Immune escape and tropism of HIV. Trends Microbiol 1995;3:356-361.
55. McKnight A, Weiss RA, Shotton C, Takeuchi Y, Hoshino H, Clapham PR. Change in tropism upon immune escape by human immunodeficiency virus. J Virol 1995;69:3167-3170.
56. Polonis VR, de Souza MS, Darden JM, Chantakulkij S, Chuenchitra T, Nitayaphan S, et al. Human immunodeficiency virus type 1 primary isolate neutralization resistance is associated with the syncytium-inducing phenotype and lower CD4 cell counts in subtype CRF01-AE-infected patients. J Virol 2003;77:8570-8576. (Pubitemid 36871486)
57. Blaak H, van der Ende ME, Boers PH, Schuitemaker H, Osterhaus AD. In vitro replication capacity of HIV-2 variants from long-term aviremic individuals. Virology 2006;353:144-154. (Pubitemid 44291787)
58. Visseaux B, Hurtado-Nedelec M, Charpentier C, Collin G, Storto A, Matheron S, et al. Molecular determinants of HIV-2 R5-X4 tropism in the V3 loop: development of a new genotypic tool. J Infect Dis 2011;205:111-120.
59. Sharon M, Kessler N, Levy R, Zolla-Pazner S, Gorlach M, Anglister J. Alternative conformations of HIV-1 V3 loops mimic beta hairpins in chemokines, suggesting a mechanism for coreceptor selectivity. Structure 2003;11:225-236. (Pubitemid 36183646)
60. Stanfield RL, Gorny MK, Williams C, Zolla-Pazner S, Wilson IA. Structural rationale for the broad neutralization of HIV-1 by human monoclonal antibody 447-52D. Structure 2004;12:193-204. (Pubitemid 38224543)