Association of progressive CD4+ T cell decline in SIV infection with the induction of autoreactive Antibodies

PLoS Pathogens

Volumn 5, Issue 4, 2009, Pages

  Kuwata, Takeo ^a,b   Nishimura, Yoshiaki ^b   Whitted, Sonya ^b   Ourmanov, Ilnour ^b   Brown, Charles R ^b   Dang, Que ^b   Buckler White, Alicia ^b   Iyengar, Ranjini ^b   Brenchley, Jason M ^b   Hirsch, Vanessa M ^b  

^a KUMAMOTO UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIBODY; DNA ANTIBODY; GLYCOPROTEIN IIIA ANTIBODY; IMMUNOGLOBULIN G; PHOSPHOLIPID ANTIBODY; THROMBOCYTE ANTIBODY; UNCLASSIFIED DRUG;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY BLOOD LEVEL; ANTIBODY RESPONSE; ARTICLE; AUTOIMMUNE DISEASE; B LYMPHOCYTE ACTIVATION; BIOLOGICAL TRAIT; BLOOD; CD4+ T LYMPHOCYTE; CLINICAL FEATURE; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE COURSE; INOCULATION; MEMORY T LYMPHOCYTE; NONHUMAN; PATHOGENESIS; PHENOTYPE; RHESUS MONKEY; SIMIAN IMMUNODEFICIENCY VIRUS; T CELL DEPLETION; T LYMPHOCYTE SUBPOPULATION; TERMINAL DISEASE; THROMBOCYTOPENIA; THROMBOSIS; TISSUE; VIRUS INFECTION; VIRUS LOAD; ANIMAL; IMMUNOLOGY; MACACA; MONKEY DISEASE;

HUMAN IMMUNODEFICIENCY VIRUS; MACACA; MACACA MULATTA; SIMIAN IMMUNODEFICIENCY VIRUS;

ANIMALS; AUTOANTIBODIES; CD4-POSITIVE T-LYMPHOCYTES; MACACA MULATTA; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; T-LYMPHOCYTE SUBSETS; VIRAL LOAD;

EID: 66349134152     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000372     Document Type: Article

References (68)

1. Hazenberg MD, Otto SA, van Benthem BH, Roos MT, Coutinho RA, et al. (2003) Persistent immune activation in HIV-1 infection is associated with progression to AIDS. AIDS 17: 1881-1888.
2. Roederer M, Dubs JG, Anderson MT, Raju PA, Herzenberg LA, et al. (1995) CD8 naive T cell counts decrease progressively in HIV-infected adults. J Clin Invest 95: 2061-2066.
3. Ullum H, Lepri AC, Victor J, Skinhoj P, Phillips AN, et al. (1997) Increased losses of CD4+CD45RA+ cells in late stages of HIV infection is related to increased risk of death: evidence from a cohort of 347 HIV-infected individuals. Aids 11: 1479-1485.
4. Ho Tsong Fang R, Khatissian E, Monceaux V, Cumont MC, Beq S, et al. (2005) Disease progression in macaques with low SIV replication levels: on the relevance of TREC counts. AIDS 19: 663-673.
5. Mattapallil JJ, Letvin NL, Roederer M (2004) T-cell dynamics during acute SIV infection. AIDS 18: 13-23.
6. Nishimura Y, Igarashi T, Buckler-White A, Buckler C, Imamichi H, et al. (2007) Loss of naive cells accompanies memory CD4+ T-cell depletion during longterm progression to AIDS in Simian immunodeficiency virus-infected macaques. J Virol 81: 893-902.
7. Li Q, Duan L, Estes JD, Ma ZM, Rourke T, et al. (2005) Peak SIV replication in resting memory CD4+ T cells depletes gut lamina propria CD4+ T cells. Nature 434: 1148-1152.
8. Mattapallil JJ, Douek DC, Hill B, Nishimura Y, Martin M, et al. (2005) Massive infection and loss of memory CD4+ T cells in multiple tissues during acute SIV infection. Nature 434: 1093-1097.
9. Brenchley JM, Schacker TW, Ruff LE, Price DA, Taylor JH, et al. (2004) CD4+ T cell depletion during all stages of HIV disease occurs predominantly in the gastrointestinal tract. J Exp Med 200: 749-759.
10. Mehandru S, Poles MA, Tenner-Racz K, Horowitz A, Hurley A, et al. (2004) Primary HIV-1 infection is associated with preferential depletion of CD4+ T lymphocytes from effector sites in the gastrointestinal tract. J Exp Med 200: 761-770.
11. Nishimura Y, Brown CR, Mattapallil JJ, Igarashi T, Buckler-White A, et al. (2005) Resting naive CD4+ T cells are massively infected and eliminated by X4- tropic simian-human immunodeficiency viruses in macaques. Proc Natl Acad Sci U S A 102: 8000-8005.
12. Veazey RS, DeMaria M, Chalifoux LV, Shvetz DE, Pauley DR, et al. (1998) Gastrointestinal tract as a major site of CD4+ T cell depletion and viral replication in SIV infection. Science 280: 427-431.
13. Gordon SN, Klatt NR, Bosinger SE, Brenchley JM, Milush JM, et al. (2007) Severe depletion of mucosal CD4+ T cells in AIDS-free simian immunodeficiency virus-infected sooty mangabeys. J Immunol 179: 3026-3034.
14. Pandrea IV, Gautam R, Ribeiro RM, Brenchley JM, Butler IF, et al. (2007) Acute loss of intestinal CD4+ T cells is not predictive of simian immunodeficiency virus virulence. J Immunol 179: 3035-3046.
15. Douek DC, Picker LJ, Koup RA (2003) T cell dynamics in HIV-1 infection. Annu Rev Immunol 21: 265-304.
16. Groux H, Torpier G, Monte D, Mouton Y, Capron A, et al. (1992) Activationinduced death by apoptosis in CD4+ T cells from human immunodeficiency virus-infected asymptomatic individuals. J Exp Med 175: 331-340.
17. Margolick JB, Munoz A, Donnenberg AD, Park LP, Galai N, et al. (1995) Failure of T-cell homeostasis preceding AIDS in HIV-1 infection. The Multicenter AIDS Cohort Study. Nat Med 1: 674-680.
18. Schacker TW, Brenchley JM, Beilman GJ, Reilly C, Pambuccian SE, et al. (2006) Lymphatic Tissue Fibrosis Is Associated with Reduced Numbers of Naive CD4+ T Cells in Human Immunodeficiency Virus Type 1 Infection. Clin Vaccine Immunol 13: 556-560.
19. Brenchley JM, Price DA, Schacker TW, Asher TE, Silvestri G, et al. (2006) Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med 12: 1365-1371.
20. Hunt PW, Brenchley J, Sinclair E, McCune JM, Roland M, et al. (2008) Relationship between T cell activation and CD4+ T cell count in HIVseropositive individuals with undetectable plasma HIV RNA levels in the absence of therapy. J Infect Dis 197: 126-133.
21. Moir S, Fauci AS (2008) Pathogenic mechanisms of B-lymphocyte dysfunction in HIV disease. J Allergy Clin Immunol 122: 12-19. Quiz 20-11.
22. Lane HC, Masur H, Edgar LC, Whalen G, Rook AH, et al. (1983) Abnormalities of B-cell activation and immunoregulation in patients with the acquired immunodeficiency syndrome. N Engl J Med 309: 453-458.
23. Silvestri G, Sodora DL, Koup RA, Paiardini M, O'Neil SP, et al. (2003) Nonpathogenic SIV infection of sooty mangabeys is characterized by limited bystander immunopathology despite chronic high-level viremia. Immunity 18: 441-452.
24. Pandrea I, Gaufin T, Brenchley JM, Gautam R, Monjure C, et al. (2008) Cutting edge: Experimentally induced immune activation in natural hosts of simian immunodeficiency virus induces significant increases in viral replication and CD4+ T cell depletion. J Immunol 181: 6687-6691.
25. Brown CR, Czapiga M, Kabat J, Dang Q, Ourmanov I, et al. (2007) Unique pathology in simian immunodeficiency virus-infected rapid progressor macaques is consistent with a pathogenesis distinct from that of classical AIDS. J Virol 81: 5594-5606.
26. Dehghani H, Puffer BA, Doms RW, Hirsch VM (2003) Unique pattern of convergent envelope evolution in simian immunodeficiency virus-infected rapid progressor macaques: association with CD4-independent usage of CCR5. J Virol 77: 6405-6418.
27. Kuwata T, Byrum R, Whitted S, Goeken R, Buckler-White A, et al. (2007) A rapid progressor-specific variant clone of simian immunodeficiency virus replicates efficiently in vivo only in the absence of immune responses. J Virol 81: 8891-8904.
28. Kuwata T, Dehghani H, Brown CR, Plishka R, Buckler-White A, et al. (2006) Infectious molecular clones from a simian immunodeficiency virus-infected rapid-progressor (RP) macaque: evidence of differential selection of RP-specific envelope mutations in vitro and in vivo. J Virol 80: 1463-1475.
29. Picker LJ, Hagen SI, Lum R, Reed-Inderbitzin EF, Daly LM, et al. (2004) Insufficient production and tissue delivery of CD4+ memory T cells in rapidly progressive simian immunodeficiency virus infection. J Exp Med 200: 1299-1314.
30. Hirsch VM, Santra S, Goldstein S, Plishka R, Buckler-White A, et al. (2004) Immune failure in the absence of profound CD4+ T-lymphocyte depletion in simian immunodeficiency virus-infected rapid progressor macaques. J Virol 78: 275-284.
31. Karpatkin S (2004) Autoimmune thrombocytopenias. Autoimmunity 37: 363-368.
32. Zandman-Goddard G, Shoenfeld Y (2002) HIV and autoimmunity. Autoimmun Rev 1: 329-337.
33. Dittmer U, Coulibaly C, Sauermann U, Stahl-Hennig C, Petry H, et al. (1994) Autoantibody-mediated platelet phagocytosis in SIV-infected macaques. Aids 8: 1509.
34. McClure HM, Anderson DC, Ansari AA, Fultz PN, Klumpp SA, et al. (1990) Nonhuman primate models for evaluation of AIDS therapy. Ann N Y Acad Sci 616: 287-298.
35. Saif MW, Greenberg B (2001) HIV and thrombosis: a review. AIDS Patient Care STDS 15: 15-24.
36. Kodama T, Mori K, Kawahara T, Ringler DJ, Desrosiers RC (1993) Analysis of simian immunodeficiency virus sequence variation in tissues of rhesus macaques with simian AIDS. J Virol 67: 6522-6534.
37. Milush JM, Reeves JD, Gordon SN, Zhou D, Muthukumar A, et al. (2007) Virally induced CD4+ T cell depletion is not sufficient to induce AIDS in a natural host. J Immunol 179: 3047-3056.
38. Massabki PS, Accetturi C, Nishie IA, da Silva NP, Sato EI, et al. (1997) Clinical implications of autoantibodies in HIV infection. AIDS 11: 1845-1850.
39. Hillyer CD, Brodie AR, Ansari AA, Anderson DC, McClure HM (1991) Severe autoimmune hemolytic anemia in SIVsmm9-infected Macaca mulatta. J Med Primatol 20: 156-158.
40. Ansari AA, Pereira LE, Mayne AE, Onlamoon N, Pattanapanyasat K, et al. (2007) The role of disease stage, plasma viral load and regulatory T cells (Tregs) on autoantibody production in SIV-infected non-human primates. J Autoimmun 28: 152-159.
41. Root-Bernstein R, Rallo A (2004) Antigenic complementarity resulting in idiotype-antiidiotype immune complexes: possible contributor to AIDS pathogenesis and autoimmunity. Autoimmunity 37: 203-210.
42. Silvestris F, Williams RC Jr, Dammacco F (1995) Autoreactivity in HIV-1 infection: the role of molecular mimicry. Clin Immunol Immunopathol 75: 197-205.
43. Haynes BF, Fleming J, St. Clair EW, Katinger H, Stiegler G, et al. (2005) Cardiolipin polyspecific autoreactivity in two broadly neutralizing HIV-1 antibodies. Science 308: 1906-1908.
44. Dorsett B, Cronin W, Chuma V, Ioachim HL (1985) Anti-lymphocyte antibodies in patients with the acquired immune deficiency syndrome. Am J Med 78: 621-626.
45. Stricker RB, McHugh TM, Moody DJ, Morrow WJ, Stites DP, et al. (1987) An AIDS-related cytotoxic autoantibody reacts with a specific antigen on stimulated CD4+ T cells. Nature 327: 710-713.
46. Fultz PN, Stricker RB, McClure HM, Anderson DC, Switzer WM, et al. (1990) Humoral response to SIV/SMM infection in macaque and mangabey monkeys. J Acquir Immune Defic Syndr 3: 319-329.
47. Daniel V, Sadeghi M, Naujokat C, Weimer R, Huth-Kuhne A, et al. (2004) Evidence for autoantibody-induced CD4 depletion mediated by apoptotic and non-apoptotic mechanisms in HIV-positive long-term surviving haemophilia patients. Clin Exp Immunol 135: 94-104.
48. Muller C, Kukel S, Bauer R (1993) Relationship of antibodies against CD4+ T cells in HIV-infected patients to markers of activation and progression: autoantibodies are closely associated with CD4 cell depletion. Immunology 79: 248-254.
49. Ardman B, Mayer K, Bristol J, Ryan M, Settles M, et al. (1990) Surface immunoglobulin-positive T lymphocytes in HIV-1 infection: relationship to CD4+ lymphocyte depletion. Clin Immunol Immunopathol 56: 249-258.
50. Wang Z, Horowitz HW, Orlikowsky T, Hahn BI, Trejo V, et al. (1999) Polyspecific self-reactive antibodies in individuals infected with human immunodeficiency virus facilitate T cell deletion and inhibit costimulatory accessory cell function. J Infect Dis 180: 1072-1079.
51. Dion ML, Bordi R, Zeidan J, Asaad R, Boulassel MR, et al. (2007) Slow disease progression and robust therapy-mediated CD4+ T-cell recovery are associated with efficient thymopoiesis during HIV-1 infection. Blood 109: 2912-2920.
52. Paiardini M, Cervasi B, Engram JC, Gordon SN, Klatt NR, et al. (2009) Bone marrow-based homeostatic proliferation of mature T-cells in non-human primates: implications for AIDS pathogenesis. Blood 113: 612-621.
53. Okoye A, Meier-Schellersheim M, Brenchley JM, Hagen SI, Walker JM, et al. (2007) Progressive CD4+ central memory T cell decline results in CD4+ effector memory insufficiency and overt disease in chronic SIV infection. J Exp Med 204: 2171-2185.
54. Rawson PM, Molette C, Videtta M, Altieri L, Franceschini D, et al. (2007) Cross-presentation of caspase-cleaved apoptotic self antigens in HIV infection. Nat Med 13: 1431-1439.
55. Fernando MM, Stevens CR, Walsh EC, De Jager PL, Goyette P, et al. (2008) Defining the role of the MHC in autoimmunity: a review and pooled analysis. PLoS Genet 4: e1000024. doi:10.1371/journal.pgen.1000024.
56. Baba M, Nishimura O, Kanzaki N, Okamoto M, Sawada H, et al. (1999) A small-molecule, nonpeptide CCR5 antagonist with highly potent and selective anti-HIV-1 activity. Proc Natl Acad Sci U S A 96: 5698-5703.
57. Bridger GJ, Skerlj RT, Thornton D, Padmanabhan S, Martellucci SA, et al. (1995) Synthesis and structure-activity relationships of phenylenebis(methylene) - linked bis-tetraazamacrocycles that inhibit HIV replication. Effects of macrocyclic ring size and substituents on the aromatic linker. J Med Chem 38: 366-378.
58. De Clercq E, Yamamoto N, Pauwels R, Balzarini J, Witvrouw M, et al. (1994) Highly potent and selective inhibition of human immunodeficiency virus by the bicyclam derivative JM3100. Antimicrob Agents Chemother 38: 668-674.
59. Dragic T, Trkola A, Thompson DA, Cormier EG, Kajumo FA, et al. (2000) A binding pocket for a small molecule inhibitor of HIV-1 entry within the transmembrane helices of CCR5. Proc Natl Acad Sci U S A 97: 5639-5644.
60. Hendrix CW, Flexner C, MacFarland RT, Giandomenico C, Fuchs EJ, et al. (2000) Pharmacokinetics and safety of AMD-3100, a novel antagonist of the CXCR-4 chemokine receptor, in human volunteers. Antimicrob Agents Chemother 44: 1667-1673.
61. Wei X, Decker JM, Wang S, Hui H, Kappes JC, et al. (2003) Antibody neutralization and escape by HIV-1. Nature 422: 307-312.
62. Wei X, Decker JM, Liu H, Zhang Z, Arani RB, et al. (2002) Emergence of resistant human immunodeficiency virus type 1 in patients receiving fusion inhibitor (T-20) monotherapy. Antimicrob Agents Chemother 46: 1896-1905.
63. Derdeyn CA, Decker JM, Sfakianos JN, Wu X, O'Brien WA, et al. (2000) Sensitivity of human immunodeficiency virus type 1 to the fusion inhibitor T-20 is modulated by coreceptor specificity defined by the V3 loop of gp120. J Virol 74: 8358-8367.
64. Platt EJ, Wehrly K, Kuhmann SE, Chesebro B, Kabat D (1998) Effects of CCR5 and CD4 cell surface concentrations on infections by macrophagetropic isolates of human immunodeficiency virus type 1. J Virol 72: 2855-2864.
65. Overton WR (1988) Modified histogram subtraction technique for analysis of flow cytometry data. Cytometry 9: 619-626.
66. Brenchley JM, Hill BJ, Ambrozak DR, Price DA, Guenaga FJ, et al. (2004) Tcell subsets that harbor human immunodeficiency virus (HIV) in vivo: implications for HIV pathogenesis. J Virol 78: 1160-1168.
67. Douek DC, Brenchley JM, Betts MR, Ambrozak DR, Hill BJ, et al. (2002) HIV preferentially infects HIV-specific CD4+ T cells. Nature 417: 95-98.
68. Igarashi T, Brown CR, Byrum RA, Nishimura Y, Endo Y, et al. (2002) Rapid and irreversible CD4+ T-cell depletion induced by the highly pathogenic simian/human immunodeficiency virus SHIV(DH12R) is systemic and synchronous. J Virol 76: 379-391.