Evolution of broadly cross-reactive HIV-1-neutralizing activity: Therapy-associated decline, positive association with detectable viremia, and partial restoration of B-cell subpopulations

Journal of Virology

Volumn 87, Issue 22, 2013, Pages 12227-12236

  Ferreira, Carolina B ^a,b   Merino Mansilla, Alberto ^a,b   Llano, Anuska ^b,c   Pérez, Ignacio ^d   Crespo, Isabel ^a   Llinas, Laia ^a   Garcia, Felipe ^b,d   Gatell, Jose M ^b,d   Yuste, Eloisa ^a,b   Sanchez Merino, Victor ^a,b  

^a INSTITUT D INVESTIGACIONS BIOMÈDIQUES AUGUST PI I SUNYER IDIBAPS   (Spain)

^b HIVACAT   (Spain)

^c HOSPITAL UNIVERSITARI GERMANS TRIAS I PUJOL   (Spain)

^d HOSPITAL CLÍNIC   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIRETROVIRUS AGENT; CD19 ANTIGEN; CD27 ANTIGEN; COMMON ACUTE LYMPHOBLASTIC LEUKEMIA ANTIGEN; COMPLEMENT COMPONENT C3D RECEPTOR; IMMUNOGLOBULIN G; NEUTRALIZING ANTIBODY; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY;

ADULT; ANTIBODY TITER; ARTICLE; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CROSS REACTION; DISEASE ASSOCIATION; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IMMUNE RESPONSE; LYMPHOCYTE SUBPOPULATION; MAJOR CLINICAL STUDY; MEMORY CELL; NONHUMAN; PRIORITY JOURNAL; TREATMENT DURATION; VIREMIA; VIRUS INHIBITION; VIRUS LOAD; VIRUS NEUTRALIZATION; VIRUS RECOMBINANT; BLOOD; CASE CONTROL STUDY; COMPARATIVE STUDY; CROSS-SECTIONAL STUDY; EVOLUTION; FEMALE; GENETICS; HIV INFECTIONS; IMMUNOLOGY; MALE; MIDDLE AGED; SERODIAGNOSIS; VIROLOGY;

HUMAN IMMUNODEFICIENCY VIRUS 1;

ADULT; ANTIBODIES, NEUTRALIZING; B-LYMPHOCYTES; BIOLOGICAL EVOLUTION; CASE-CONTROL STUDIES; CROSS REACTIONS; CROSS-SECTIONAL STUDIES; FEMALE; FLOW CYTOMETRY; HIV ANTIBODIES; HIV INFECTIONS; HIV-1; HUMANS; MALE; MIDDLE AGED; NEUTRALIZATION TESTS; VIRAL LOAD; VIREMIA;

EID: 84886303941     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02155-13     Document Type: Article

References (40)

1. Klasse PJ, Sanders RW, Cerutti A, Moore JP. 2012. How can HIV-type-1-Env immunogenicity be improved to facilitate antibody-based vaccine development? AIDS Res. Hum. Retroviruses 28:1-15.
2. Reitter JN, Means RE, Desrosiers RC. 1998. A role for carbohydrates in immune evasion in AIDS. Nat. Med. 4:679-684.
3. Zhu P, Chertova E, Bess J, Jr, Lifson JD, Arthur LO, Liu J, et al. 2003. Electron tomography analysis of envelope glycoprotein trimers on HIV and simian immunodeficiency virus virions. Proc. Natl. Acad. Sci. U. S. A. 100:15812-15817.
4. Poignard P, Moulard M, Golez E, Vivona V, Franti M, Venturini S, et al. 2003. Heterogeneity of envelope molecules expressed on primary human immunodeficiency virus type 1 particles as probed by the binding of neutralizing and nonneutralizing antibodies. J. Virol. 77:353-365.
5. Sather DN, Armann J, Ching LK, Mavrantoni A, Sellhorn G, Caldwell Z, et al. 2009. Factors associated with the development of cross-reactive neutralizing antibodies during human immunodeficiency virus type 1 infection. J. Virol. 83:757-769.
6. Binley JM, Lybarger EA, Crooks ET, Seaman MS, Gray E, Davis KL, et al. 2008. Profiling the specificity of neutralizing antibodies in a large panel of plasmas from patients chronically infected with human immunodeficiency virus type 1 subtypes B and C. J. Virol. 82:11651-11668.
7. Gray ES, Taylor N, WycuffD, Moore PL, Tomaras GD, Wibmer CK, et al. 2009. Antibody specificities associated with neutralization breadth in plasma from human immunodeficiency virus type 1 subtype C-infected blood donors. J. Virol. 83:8925-8937.
8. Li Y, Migueles SA, Welcher B, Svehla K, Phogat A, Louder MK, et al. 2007. Broad HIV-1 neutralization mediated by CD4-binding site antibodies. Nat. Med. 13:1032-1034.
9. Doria-Rose NA, Klein RM, Daniels MG, O'Dell S, Nason M, Lapedes A, et al. 2010. Breadth of human immunodeficiency virus-specific neutralizing activity in sera: clustering analysis and association with clinical variables. J. Virol. 84:1631-1636.
10. Tomaras GD, Yates NL, Liu P, Qin L, Fouda GG, Chavez LL, et al. 2008. Initial B-cell responses to transmitted human immunodeficiency virus type 1: virion-binding immunoglobulinM(IgM) and IgG antibodies followed by plasma anti-gp41 antibodies with ineffective control of initial viremia. J. Virol. 82:12449-12463.
11. Rong R, Li B, Lynch RM, Haaland RE, Murphy MK, Mulenga J, et al. 2009. Escape from autologous neutralizing antibodies in acute/early subtype C HIV-1 infection requires multiple pathways. PLoS Pathog. 5:e1000594. doi:10.1371/journal.ppat.1000594.
12. Richman DD, Wrin T, Little SJ, Petropoulos CJ. 2003. Rapid evolution of the neutralizing antibody response to HIV type 1 infection. Proc. Natl. Acad. Sci. U. S. A. 100:4144-4149.
13. Mikell I, Sather DN, Kalams SA, Altfeld M, Alter G, Stamatatos L. 2011. Characteristics of the earliest cross-neutralizing antibody response to HIV-1. PLoS Pathog. 7:e1001251. doi:10.1371/journal.ppat.1001251.
14. Sajadi MM, Guan Y, DeVico AL, Seaman MS, Hossain M, Lewis GK, et al. 2011. Correlation between circulating HIV-1 RNA and broad HIV-1 neutralizing antibody activity. J. Acquir. Immune Defic. Syndr. 57:9-15.
15. Medina-Ramirez M, Sanchez-Merino V, Sanchez-Palomino S, Merino-Mansilla A, Ferreira CB, Perez I, et al. 2011. Broadly cross-neutralizing antibodies in HIV-1 patients with undetectable viremia. J. Virol. 85:5804-5813.
16. Euler Z, van den Kerkhof TL, van Gils MJ, Burger JA, Edo-Matas D, Phung P, et al. 2012. Longitudinal analysis of early HIV-1-specific neutralizing activity in an elite neutralizer and in five patients who developed cross-reactive neutralizing activity. J. Virol. 86:2045-2055.
17. Gray ES, Madiga MC, Hermanus T, Moore PL, Wibmer CK, Tumba NL, et al. 2011. The neutralization breadth of HIV-1 develops incrementally over four years and is associated with CD4+ T cell decline and high viral load during acute infection. J. Virol. 85:4828-4840.
18. Moir S, Malaspina A, Ogwaro KM, Donoghue ET, Hallahan CW, Ehler LA, et al. 2001. HIV-1 induces phenotypic and functional perturbations of B cells in chronically infected individuals. Proc. Natl. Acad. Sci. U. S. A. 98:10362-10367.
19. Notermans DW, de Jong JJ, Goudsmit J, Bakker M, Roos MT, Nijholt L, et al. 2001. Potent antiretroviral therapy initiates normalization of hypergammaglobulinemia and a decline in HIV type 1-specific antibody responses. AIDS Res. Hum. Retroviruses 17:1003-1008.
20. Shirai A, Cosentino M, Leitman-Klinman SF, Klinman DM. 1992. Human immunodeficiency virus infection induces both polyclonal and virus-specific B cell activation. J. Clin. Invest. 89:561-566.
21. Kovacs JA, Lempicki RA, Sidorov IA, Adelsberger JW, Herpin B, Metcalf JA, et al. 2001. Identification of dynamically distinct subpopulations of T lymphocytes that are differentially affected by HIV. J. Exp. Med. 194:1731-1741.
22. Martinez-Maza O, Crabb E, Mitsuyasu RT, Fahey JL, Giorgi JV. 1987. Infection with the human immunodeficiency virus (HIV) is associated with an in vivo increase in B lymphocyte activation and immaturity. J. Immunol. 138:3720-3724.
23. De Milito A, Nilsson A, Titanji K, Thorstensson R, Reizenstein E, Narita M, et al. 2004. Mechanisms of hypergammaglobulinemia and impaired antigen-specific humoral immunity in HIV-1 infection. Blood 103:2180-2186.
24. Conge AM, Tarte K, Reynes J, Segondy M, Gerfaux J, Zembala M, et al. 1998. Impairment of B-lymphocyte differentiation induced by dual triggering of the B-cell antigen receptor and CD40 in advanced HIV-1-disease. AIDS 12:1437-1449.
25. Scherer EM, Zwick MB, Teyton L, Burton DR. 2007. Difficulties in eliciting broadly neutralizing anti-HIV antibodies are not explained by cardiolipin autoreactivity. AIDS 21:2131-2139.
26. Moir S, Fauci AS. 2009. B cells in HIV infection and disease. Nat. Rev. Immunol. 9:235-245.
27. De Roos AJ, Mirick DK, Edlefsen KL, LaCroix AZ, Kopecky KJ, Madeleine MM, et al. 2012. Markers of B-cell activation in relation to risk of non-Hodgkin lymphoma. Cancer Res. 72:4733-4743.
28. Moir S, Malaspina A, Ho J, Wang W, Dipoto AC, O'Shea MA, et al. 2008. Normalization of B cell counts and subpopulations after antiretroviral therapy in chronic HIV disease. J. Infect. Dis. 197:572-579.
29. Newman RM, Hall L, Connole M, Chen GL, Sato S, Yuste E, et al. 2006. Balancing selection and the evolution of functional polymorphism in Old World monkey TRIM5alpha. Proc. Natl. Acad. Sci. U. S. A. 103:19134-19139.
30. Doria-Rose NA, Klein RM, Manion MM, O'Dell S, Phogat A, Chakrabarti B, et al. 2009. Frequency and phenotype of human immunodeficiency virus envelope-specific B cells from patients with broadly cross-neutralizing antibodies. J. Virol. 83:188-199.
31. Euler Z, van Gils MJ, Bunnik EM, Phung P, Schweighardt B, Wrin T, et al. 2010. Cross-reactive neutralizing humoral immunity does not protect from HIV type 1 disease progression. J. Infect. Dis. 201:1045-1053.
32. Simek MD, Rida W, Priddy FH, Pung P, Carrow E, Laufer DS, et al. 2009. Human immunodeficiency virus type 1 elite neutralizers: individuals with broad and potent neutralizing activity identified by using a highthroughput neutralization assay together with an analytical selection algorithm. J. Virol. 83:7337-7348.
33. Euler Z, van Gils MJ, Boeser-Nunnink BD, Schuitemaker H, van Manen D. 2013. Genome-wide association study on the development of crossreactive neutralizing antibodies in HIV-1 infected individuals. PLoS One 8:e54684. doi:10.1371/journal.pone.0054684.
34. Lafeuillade A, Chollet L, Hittinger G, Profizi N, Costes O, Poggi C. 1998. Residual human immunodeficiency virus type 1 RNA in lymphoid tissue of patients with sustained plasmaRNA of < 200 copies/mL. J. Infect. Dis. 177:235-238.
35. Moir S, Buckner CM, Ho J, Wang W, Chen J, Waldner AJ, et al. 2010. B cells in early and chronic HIV infection: evidence for preservation of immune function associated with early initiation of antiretroviral therapy. Blood 116:5571-5579.
36. Caraux A, Klein B, Paiva B, Bret C, Schmitz A, Fuhler GM, et al. 2010. Circulating human B and plasma cells. Age-associated changes in counts and detailed characterization of circulating normal C. Haematologica 95: 1016-1020.
37. Moir S, Ho J, Malaspina A, Wang W, Dipoto AC, O'Shea MA, et al. 2008. Evidence for HIV-associated B cell exhaustion in a dysfunctional memory B cell compartment in HIV-infected viremic individuals. J. Exp. Med. 205:1797-1805.
38. Ogg GS, Jin X, Bonhoeffer S, Moss P, Nowak MA, Monard S, et al. 1999. Decay kinetics of human immunodeficiency virus-specific effector cytotoxic T lymphocytes after combination antiretroviral therapy. J. Virol. 73:797-800.
39. Kalams SA, Goulder PJ, Shea AK, Jones NG, Trocha AK, Ogg GS, et al. 1999. Levels of human immunodeficiency virus type 1-specific cytotoxic T-lymphocyte effector and memory responses decline after suppression of viremia with highly active antiretroviral therapy. J. Virol. 73:6721-6728.
40. Nagase H, Agematsu K, Kitano K, Takamoto M, Okubo Y, Komiyama A, et al. 2001. Mechanism of hypergammaglobulinemia by HIV infection: circulating memory B-cell reduction with plasmacytosis. Clin. Immunol. 100:250-259.