Differential infection patterns of CD4+ T cells and lymphoid tissue viral burden distinguish progressive and nonprogressive lentiviral infections

Blood

Volumn 120, Issue 20, 2012, Pages 4172-4181

  Brenchley, Jason M ^a   Vinton, Carol ^a   Tabb, Brian ^b   Hao, Xing Pei ^b   Connick, Elizabeth ^c   Paiardini, Mirko ^d   Lifson, Jeffrey D ^b   Silvestri, Guido ^d   Estes, Jacob D ^b  

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

^b SAIC FREDERICK INC   (United States)

^c UNIVERSITY OF COLORADO   (United States)

^d EMORY UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD28 ANTIGEN; CD4 ANTIGEN; CHEMOKINE RECEPTOR CCR7; FAS ANTIGEN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CERCOCEBUS; CLINICAL ARTICLE; COHORT ANALYSIS; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; FOLLICULAR DENDRITIC CELL; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; LENTIVIRUS INFECTION; LYMPHOID TISSUE; MALE; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; RHESUS MONKEY; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; T LYMPHOCYTE SUBPOPULATION; TARGET CELL; VIREMIA;

EID: 84869814713     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2012-06-437608     Document Type: Article

References (54)

1. Hahn BH, Shaw GM, De Cock KM, Sharp PM. AIDS as a zoonosis: scientific and public health implications. Science. 2000;287(5453):607-614. (Pubitemid 30070900)
2. Pandrea I, Sodora DL, Silvestri G, Apetrei C. Into the wild: simian immunodeficiency virus (SIV) infection in natural hosts. Trends Immunol. 2008;29(9):419-428.
3. Silvestri G, Paiardini M, Pandrea I, Lederman MM, Sodora DL. Understanding the benign nature of SIV infection in natural hosts. J Clin Invest. 2007;117(11):3148-3154. (Pubitemid 350096967)
4. Goldstein S, Brown CR, Ourmanov I, et al. Comparison of simian immunodeficiency virus SIVagmVer replication and CD4+ T-cell dynamics in vervet and sabaeus African green monkeys. J Virol. 2006;80(10):4868-4877.
5. Pandrea I, Apetrei C, Dufour J, et al. Simian immunodeficiency virus SIVagm.sab infection of Caribbean African green monkeys: a new model for the study of SIV pathogenesis in natural hosts. J Virol. 2006;80(10):4858-4867.
6. Silvestri G, Sodora DL, Koup RA, et al. Nonpathogenic SIV infection of sooty mangabeys is characterized by limited bystander immunopathology despite chronic high-level viremia. Immunity. 2003;18(3):441-452. (Pubitemid 36351522)
7. Barry AP, Silvestri G, Safrit JT, et al. Depletion of CD8+ cells in sooty mangabey monkeys naturally infected with simian immunodeficiency virus reveals limited role for immune control of virus replication in a natural host species. J Immunol. 2007;178(12):8002-8012. (Pubitemid 46898071)
8. Dunham R, Pagliardini P, Gordon S, et al. The AIDS resistance of naturally SIV-infected sooty mangabeys is independent of cellular immunity to the virus. Blood. 2006;108(1):209-217. (Pubitemid 43990631)
9. Li B, Stefano-Cole K, Kuhrt DM, et al. Nonpathogenic simian immunodeficiency virus infection of sooty mangabeys is not associated with high levels of autologous neutralizing antibodies. J Virol. 2010;84(12):6248-6253.
10. Klatt NR, Villinger F, Bostik P, et al. Availability of activated CD4+ T cells dictates the level of viremia in naturally SIV-infected sooty mangabeys. J Clin Invest. 2008;118(6):2039-2049. (Pubitemid 351872324)
11. Pandrea I, Onanga R, Souquiere S, et al. Paucity of CD4+ CCR5+ T cells may prevent transmission of simian immunodeficiency virus in natural nonhuman primate hosts by breast-feeding. J Virol. 2008;82(11):5501-5509.
12. Gordon SN, Dunham RM, Engram JC, et al. Short-lived infected cells support virus replication in sooty mangabeys naturally infected with simian immunodeficiency virus: implications for AIDS pathogenesis. J Virol. 2008;82(7):3725-3735. (Pubitemid 351429948)
13. Goldstein S, Ourmanov I, Brown CR, et al. Plateau levels of viremia correlate with the degree of CD4+-T-cell loss in simian immunodeficiency virus SIVagm-infected pigtailed macaques: variable pathogenicity of natural SIVagm isolates. J Virol. 2005;79(8):5153-5162. (Pubitemid 40464264)
14. Watson A, Ranchalis J, Travis B, et al. Plasma viremia in macaques infected with simian immunodeficiency virus: plasma viral load early in infection predicts survival. J Virol. 1997;71(1):284-290. (Pubitemid 26412290)
15. Hirsch V, Adger-Johnson D, Campbell B, et al. A molecularly cloned, pathogenic, neutralization-resistant simian immunodeficiency virus, SIVsmE543-3. J Virol. 1997;71(2):1608-1620. (Pubitemid 27030338)
16. Li Y, Hui H, Burgess CJ, et al. Complete nucleotide sequence, genome organization, and biological properties of human immunodeficiency virus type 1 in vivo: evidence for limited defectiveness and complementation. J Virol. 1992;66(11):6587-6600.
17. Okoye A, Meier-Schellersheim M, Brenchley JM, et al. Progressive CD4+ central memory T cell decline results in CD4+ effector memory insufficiency and overt disease in chronic SIV infection. J Exp Med. 2007;204(9):2171-2185. (Pubitemid 47360877)
18. Okoye AA, Rohankhedkar M, Abana C, et al. Naive T cells are dispensable for memory CD4+ T cell homeostasis in progressive simian immunodeficiency virus infection. J Exp Med. 2012;209(4):641-651.
19. Beaumier CM, Harris LD, Goldstein S, et al. CD4 downregulation by memory CD4+ T cells in vivo renders African green monkeys resistant to progressive SIVagm infection. Nat Med. 2009;15(8):879-885.
20. Pandrea I, Apetrei C, Gordon S, et al. Paucity of CD4+CCR5+ T cells is a typical feature of natural SIV hosts. Blood. 2007;109(3):1069-1076. (Pubitemid 46220653)
21. Paiardini M, Cervasi B, Reyes-Aviles E, et al. Low levels of SIV infection in sooty mangabey central memory CD4(+) T cells are associated with limited CCR5 expression. Nat Med. 2011;17(7):830-836.
22. Klatt NR, Harris LD, Vinton CL, et al. Compromised gastrointestinal integrity in pigtail macaques is associated with increased microbial translocation, immune activation, and IL-17 production in the absence of SIV infection. Mucosal Immunol. 2010;3(4):387-398.
23. Folkvord JM, McCarter MD, Ryder J, Meditz AL, Forster JE, Connick E. α-defensins 1, 2, and 3 are expressed by granulocytes in lymphoid tissues of HIV-1-seropositive and -seronegative individuals. J Acquir Immune Defic Syndr. 2006;42(5):529-536. (Pubitemid 44162420)
24. Campbell TB, Staskus KA, Folkvord J, et al. Persistence of Kaposi sarcoma-associated herpesvirus (KSHV)-infected cells in KSHV/HIV-1-coinfected subjects without KSHV-associated diseases. J Infect Dis. 2005;191(3):367-371. (Pubitemid 40139761)
25. Folkvord JM, Anderson DM, Arya J, MaWhinney S, Connick E. Microanatomic relationships between CD8+ cells and HIV-1-producing cells in human lymphoid tissue in vivo. J Acquir Immune Defic Syndr. 2003;32(5):469-476. (Pubitemid 36423116)
26. Campbell TB, Schneider K,Wrin T, Petropoulos CJ, Connick E. Relationship between in vitro human immunodeficiency virus type 1 replication rate and virus load in plasma. J Virol. 2003;77(22):12105-12112. (Pubitemid 37339863)
27. Folkvord JM, Armon C, Connick E. Lymphoid follicles are sites of heightened human immunodeficiency virus type 1 (HIV-1) replication and reduced antiretroviral effector mechanisms. AIDS Res Hum Retroviruses. 2005;21(5):363-370. (Pubitemid 40800452)
28. Mattapallil JJ, Douek DC, Hill B, Nishimura Y, Martin M, Roederer M. Massive infection and loss of memory CD4+ T cells in multiple tissues during acute SIV infection. Nature. 2005;434(7037):1093-1097. (Pubitemid 40663481)
29. Haase AT, Henry K, Zupancic M, et al. Quantitative image analysis of HIV-1 infection in lymphoid tissue. Science. 1996;274:985-989. (Pubitemid 26398421)
30. Cavert W, Notermans D, Staskus K, et al. Kinetics of response in lymphoid tissues to antiretroviral therapy of HIV-1 infection. Science. 1997;276:960-964. (Pubitemid 27209096)
31. Hirsch VM, Olmsted RA, Murphey-Corb M, Purcell RH, Johnson PR. An African primate lentivirus (SIVsm) closely related to HIV-2. Nature. 1989;339(6223):389-392. (Pubitemid 19144229)
32. Ortiz AM, Klatt NR, Li B, et al. Depletion of CD4+ T cells abrogates post-peak decline of viremia in SIV-infected rhesus macaques. J Clin Invest. 2011;121(11):4433-4445.
33. Kent KA, Gritz L, Stallard G, et al. Production and of monoclonal antibodies to simian immunodeficiency virus envelope glycoproteins. AIDS. 1991;5(7):829-836.
34. Chahroudi A, Bosinger SE, Vanderford TH, Paiardini M, Silvestri G. Natural SIV hosts: showing AIDS the door. Science. 2012;335(6073):1188-1193.
35. Beer B, Scherer J, zur Megede J, Norley S, Baier M, Kurth R. Lack of dichotomy between virus load of peripheral blood and lymph nodes during long-term simian immunodeficiency virus infection of African green monkeys. Virology. 1996;219(2):367-375. (Pubitemid 26188387)
36. Meythaler M, Wang Z, Martinot A, et al. Early induction of polyfunctional simian immunodeficiency virus (SIV)-specific T lymphocytes and rapid disappearance of SIV from lymph nodes of sooty mangabeys during primary infection. J Immunol. 2011;186(9):5151-5161.
37. Rey-Cuillé MA, Berthier JL, Bomsel-Demontoy MC, et al. Simian immunodeficiency virus replicates to high levels in sooty mangabeys without inducing disease. J Virol. 1998;72(5):3872-3886. (Pubitemid 28188688)
38. Diop OM, Gueye A, Dias-Tavares M, et al. High levels of viral replication during primary simian immunodeficiency virus SIVagm infection are rapidly and strongly controlled in African green monkeys. J Virol. 2000;74(16):7538-7547. (Pubitemid 30613099)
39. Broussard SR, Staprans SI, White R, Whitehead EM, Feinberg MB, Allan JS. Simian immunodeficiency virus replicates to high levels in naturally infected African green monkeys without inducing immunologic or neurologic disease. J Virol. 2001;75(5):2262-2275. (Pubitemid 32147565)
40. Brenchley JM, Knox KK, Asher AI, et al. High frequencies of polyfunctional HIV-specific T cells are associated with preservation of mucosal CD4 T cells in bronchoalveolar lavage. Mucosal Immunol. 2008;1:49-58.
41. Betts MR, Nason MC, West SM, et al. HIV nonprogressors preferentially maintain highly functional HIV-specific CD8+ T cells. Blood. 2006;107(12):4781-4789. (Pubitemid 43882629)
42. Brenchley JM, Paiardini M, Knox KS, et al. Differential Th17 CD4 T-cell depletion in pathogenic and nonpathogenic lentiviral infections. Blood. 2008;112(7):2826-2835.
43. Cecchinato V, Trindade C, Laurence A, et al. Altered balance between Th17 and Th1 cells at mucosal sites predicts AIDS progression in simian immunodeficienty virus-infected macaques. Mucosal Immunol. 2008;1(4):279-288. (Pubitemid 351850534)
44. Favre D, Lederer S, Kanwar B, et al. Critical loss of the balance between Th17 and T regulatory cell populations in pathogenic SIV infection. PLoS Pathog. 2009;5(2):e1000295.
45. Dunham RM, Cervasi B, Brenchley JM, et al. CD127 and CD25 expression defines CD4+ T-cell subsets that are differentially depleted during HIV infection. J Immunol. 2008;180(8):5582-5592.
46. Shaw JM, Hunt PW, Critchfield JW, et al. Increased frequency of regulatory T cells accompanies increased immune activation in rectal mucosae of HIV-positive noncontrollers. J Virol. 2012;85(21):11422-11434.
47. Klatt NR, Vinton CL, Lynch RM, et al. SIV infection of rhesus macaques results in dysfunctional T- and B-cell responses to neo and recall Leishmania major vaccination. Blood. 2011;118(22):5803-5812.
48. Moir S, Fauci AS. B cells in HIV infection and disease. Nat Rev Immunol. 2009;9(4):235-245.
49. Moir S, Ho J, Malaspina A, et al. Evidence for HIV-associated B cell exhaustion in a dysfunctional memory B cell compartment in HIV-infected viremic individuals. J Exp Med. 2008;205(8):1797-1805.
50. Vinton C, Klatt NR, Harris LD, et al. CD4-like immunological function by CD4- T cells in multiple natural hosts of simian immunodeficiency virus. J Virol. 2011;85(17):8702-8708.
51. Gattinoni L, Lugli E, Ji Y, et al. A human memory T-cell subset with stem cell-like properties. Nat Med. 2011;17(10):1290-1297.
52. Hufert FT, van Lunzen J, Janossy G, et al. Germinal centre CD4+ T cells are an important site of HIV replication in vivo. AIDS. 1997;11(7):849-857. (Pubitemid 27226407)
53. Burton GF, Keele BF, Estes JD, Thacker TC, Gartner S. Follicular dendritic cell contributions to HIV pathogenesis. Semin Immunol. 2002;14(4):275-284. (Pubitemid 34969896)
54. Vinuesa CG, Cyster JG. How T cells earn the follicular rite of passage. Immunity. 2011;35(5):671-680.