Paucity of CD4+ natural killer T (NKT) lymphocytes in sooty mangabeys is associated with lack of NKT cell depletion after SIV infection

PLoS ONE

Volumn 5, Issue 3, 2010, Pages

  Rout, Namita ^a   Else, James G ^b   Yue, Simon ^a   Connole, Michelle ^a   Exley, Mark A ^a   Kaur, Amitinder ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b EMORY UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD1D ANTIGEN; CD8 ANTIGEN; INTERLEUKIN 10;

ANIMAL; ARTICLE; BIOSYNTHESIS; CD4+ T LYMPHOCYTE; CERCOCEBUS; CYTOLOGY; DISEASE COURSE; FLOW CYTOMETRY; GENETICS; IMMUNOLOGY; IMMUNOPHENOTYPING; LYMPHOCYTE; METABOLISM; METHODOLOGY; NATURAL KILLER CELL; PHENOTYPE; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; T LYMPHOCYTE; VIROLOGY;

ANIMALS; ANTIGENS, CD1D; ANTIGENS, CD8; CD4-POSITIVE T-LYMPHOCYTES; CERCOCEBUS ATYS; DISEASE PROGRESSION; FLOW CYTOMETRY; IMMUNOPHENOTYPING; INTERLEUKIN-10; KILLER CELLS, NATURAL; LYMPHOCYTES; PHENOTYPE; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; T-LYMPHOCYTES;

EID: 77954683638     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0009787     Document Type: Article

References (84)

1. Chakrabarti LA, Lewin SR, Zhang L, Gettie A, Luckay A, et al. (2000) Normal T-cell turnover in sooty mangabeys harboring active simian immunodeficiency virus infection. J Virol 74: 1209-1223.
2. 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.
3. Kaur A, Di Mascio M, Barabasz A, Rosenzweig M, McClure HM, et al. (2008) Dynamics of T-and B-lymphocyte turnover in a natural host of simian immunodeficiency virus. J Virol 82: 1084-1093.
4. Pandrea I, Sodora DL, Silvestri G, Apetrei C (2008) Into the wild: simian immunodeficiency virus (SIV) infection in natural hosts. Trends Immunol 29: 419-428.
5. Sodora DL, Allan JS, Apetrei C, Brenchley JM, Douek DC, et al. (2009) Toward an AIDS vaccine: lessons from natural simian immunodeficiency virus infections of African nonhuman primate hosts. Nat Med 15: 861-865.
6. 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.
7. 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.
8. Estes JD, Gordon SN, Zeng M, Chahroudi AM, Dunham RM, et al. (2008) Early resolution of acute immune activation and induction of PD-1 in SIVinfected sooty mangabeys distinguishes nonpathogenic from pathogenic infection in rhesus macaques. J Immunol 180: 6798-6807.
9. Meythaler M, Martinot A, Wang Z, Pryputniewicz S, Kasheta M, et al. (2009) Differential CD4+ T-lymphocyte apoptosis and bystander T-cell activation in rhesus macaques and sooty mangabeys during acute simian immunodeficiency virus infection. J Virol 83: 572-583.
10. Lederer S, Favre D, Walters KA, Proll S, Kanwar B, et al. (2009) Transcriptional profiling in pathogenic and non-pathogenic SIV infections reveals significant distinctions in kinetics and tissue compartmentalization. PLoS Pathog 5: e1000296.
11. Kornfeld C, Ploquin MJ, Pandrea I, Faye A, Onanga R, et al. (2005) Antiinflammatory profiles during primary SIV infection in African green monkeys are associated with protection against AIDS. J Clin Invest 115: 1082-1091.
12. 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.
13. Pandrea I, Apetrei C, Gordon S, Barbercheck J, Dufour J, et al. (2007) Paucity of CD4+CCR5+ T cells is a typical feature of natural SIV hosts. Blood 109: 1069-1076.
14. Mandl JN, Barry AP, Vanderford TH, Kozyr N, Chavan R, et al. (2008) Divergent TLR7 and TLR9 signaling and type I interferon production distinguish pathogenic and nonpathogenic AIDS virus infections. Nat Med 14: 1077-1087.
15. Favre D, Lederer S, Kanwar B, Ma ZM, Proll S, et al. (2009) Critical loss of the balance between Th17 and T regulatory cell populations in pathogenic SIV infection. PLoS Pathog 5: e1000295.
16. Brenchley JM, Paiardini M, Knox KS, Asher AI, Cervasi B, et al. (2008) Differential Th17 CD4 T-cell depletion in pathogenic and nonpathogenic lentiviral infections. Blood 112: 2826-2835.
17. Kaur A, Grant RM, Means RE, McClure H, Feinberg M, et al. (1998) Diverse host responses and outcomes following simian immunodeficiency virus SIVmac239 infection in sooty mangabeys and rhesus macaques. J Virol 72: 9597-9611.
18. Wang Z, Metcalf B, Ribeiro RM, McClure H, Kaur A (2006) Th-1-type cytotoxic CD8+ T-lymphocyte responses to simian immunodeficiency virus (SIV) are a consistent feature of natural SIV infection in sooty mangabeys. J Virol 80: 2771-2783.
19. Stacey AR, Norris PJ, Qin L, Haygreen EA, Taylor E, et al. (2009) Induction of a striking systemic cytokine cascade prior to peak viremia in acute human immunodeficiency virus type 1 infection, in contrast to more modest and delayed responses in acute hepatitis B and C virus infections. J Virol 83: 3719-3733.
20. Bendelac A, Savage PB, Teyton L (2007) The biology of NKT cells. Annu Rev Immunol 25: 297-336.
21. Godfrey DI, Kronenberg M (2004) Going both ways: immune regulation via CD1d-dependent NKT cells. J Clin Invest 114: 1379-1388.
22. Koseki H, Asano H, Inaba T, Miyashita N, Moriwaki K, et al. (1991) Dominant expression of a distinctive V14+ T-cell antigen receptor alpha chain in mice. Proc Natl Acad Sci U S A 88: 7518-7522.
23. Porcelli S, Yockey CE, Brenner MB, Balk SP (1993) Analysis of T cell antigen receptor (TCR) expression by human peripheral blood CD4-8-alpha/beta T cells demonstrates preferential use of several V beta genes and an invariant TCR alpha chain. J Exp Med 178: 1-16.
24. Lantz O, Bendelac A (1994) An invariant T cell receptor alpha chain is used by a unique subset of major histocompatibility complex class I-specific CD4+ and CD4-8-T cells in mice and humans. J Exp Med 180: 1097-1106.
25. Coquet JM, Chakravarti S, Kyparissoudis K, McNab FW, Pitt LA, et al. (2008) Diverse cytokine production by NKT cell subsets and identification of an IL-17-producing CD4-NK1.1-NKT cell population. Proc Natl Acad Sci U S A 105: 11287-11292.
26. Matsuda JL, Mallevaey T, Scott-Browne J, Gapin L (2008) CD1d-restricted iNKT cells, the 'Swiss-Army knife' of the immune system. Curr Opin Immunol 20: 358-368.
27. Matsuda JL, Gapin L, Baron JL, Sidobre S, Stetson DB, et al. (2003) Mouse V alpha 14i natural killer T cells are resistant to cytokine polarization in vivo. Proc Natl Acad Sci U S A 100: 8395-8400.
28. Brigl M, Bry L, Kent SC, Gumperz JE, Brenner MB (2003) Mechanism of CD1d-restricted natural killer T cell activation during microbial infection. Nat Immunol 4: 1230-1237.
29. Carnaud C, Lee D, Donnars O, Park SH, Beavis A, et al. (1999) Cutting edge: Cross-talk between cells of the innate immune system: NKT cells rapidly activate NK cells. J Immunol 163: 4647-4650.
30. Hermans IF, Silk JD, Gileadi U, Salio M, Mathew B, et al. (2003) NKT cells enhance CD4+ and CD8+ T cell responses to soluble antigen in vivo through direct interaction with dendritic cells. J Immunol 171: 5140-5147.
31. Galli G, Pittoni P, Tonti E, Malzone C, Uematsu Y, et al. (2007) Invariant NKT cells sustain specific B cell responses and memory. Proc Natl Acad Sci U S A 104: 3984-3989.
32. Crowe NY, Smyth MJ, Godfrey DI (2002) A critical role for natural killer T cells in immunosurveillance of methylcholanthrene-induced sarcomas. J Exp Med 196: 119-127.
33. Ilyinskii PO, Wang R, Balk SP, Exley MA (2006) CD1d mediates T-celldependent resistance to secondary infection with encephalomyocarditis virus (EMCV) in vitro and immune response to EMCV infection in vivo. J Virol 80: 7146-7158.
34. Grubor-Bauk B, Simmons A, Mayrhofer G, Speck PG (2003) Impaired clearance of herpes simplex virus type 1 from mice lacking CD1d or NKT cells expressing the semivariant V alpha 14-J alpha 281 TCR. J Immunol 170: 1430-1434.
35. Ashkar AA, Rosenthal KL (2003) Interleukin-15 and natural killer and NKT cells play a critical role in innate protection against genital herpes simplex virus type 2 infection. J Virol 77: 10168-10171.
36. Johnson TR, Hong S, Van Kaer L, Koezuka Y, Graham BS (2002) NK T cells contribute to expansion of CD8(+) T cells and amplification of antiviral immune responses to respiratory syncytial virus. J Virol 76: 4294-4303.
37. Diana J, Griseri T, Lagaye S, Beaudoin L, Autrusseau E, et al. (2009) NKT cellplasmacytoid dendritic cell cooperation via OX40 controls viral infection in a tissue-specific manner. Immunity 30: 289-299.
38. Kakimi K, Guidotti LG, Koezuka Y, Chisari FV (2000) Natural killer T cell activation inhibits hepatitis B virus replication in vivo. J Exp Med 192: 921-930.
39. Sonoda KH, Faunce DE, Taniguchi M, Exley M, Balk S, et al. (2001) NK T cell-derived IL-10 is essential for the differentiation of antigen-specific T regulatory cells in systemic tolerance. J Immunol 166: 42-50.
40. Watte CM, Nakamura T, Lau CH, Ortaldo JR, Stein-Streilein J (2008) Ly49 C/ I-dependent NKT cell-derived IL-10 is required for corneal graft survival and peripheral tolerance. J Leukoc Biol 83: 928-935.
41. Chen YG, Choisy-Rossi CM, Holl TM, Chapman HD, Besra GS, et al. (2005) Activated NKT cells inhibit autoimmune diabetes through tolerogenic recruitment of dendritic cells to pancreatic lymph nodes. J Immunol 174: 1196-1204.
42. Dieli F, Taniguchi M, Kronenberg M, Sidobre S, Ivanyi J, et al. (2003) An antiinflammatory role for V alpha 14 NK T cells in Mycobacterium bovis bacillus Calmette-Guerin-infected mice. J Immunol 171: 1961-1968.
43. Motsinger A, Haas DW, Stanic AK, Van Kaer L, Joyce S, et al. (2002) CD1drestricted human natural killer T cells are highly susceptible to human immunodeficiency virus 1 infection. J Exp Med 195: 869-879.
44. Fleuridor R, Wilson B, Hou R, Landay A, Kessler H, et al. (2003) CD1drestricted natural killer T cells are potent targets for human immunodeficiency virus infection. Immunology 108: 3-9.
45. Motsinger A, Azimzadeh A, Stanic AK, Johnson RP, Van Kaer L, et al. (2003) Identification and simian immunodeficiency virus infection of CD1d-restricted macaque natural killer T cells. J Virol 77: 8153-8158.
46. Sandberg JK, Fast NM, Palacios EH, Fennelly G, Dobroszycki J, et al. (2002) Selective loss of innate CD4(+) V alpha 24 natural killer T cells in human immunodeficiency virus infection. J Virol 76: 7528-7534.
47. van der Vliet HJ, von Blomberg BM, Hazenberg MD, Nishi N, Otto SA, et al. (2002) Selective decrease in circulating V alpha 24+V beta 11+ NKT cells during HIV type 1 infection. J Immunol 168: 1490-1495.
48. Unutmaz D (2003) NKT cells and HIV infection. Microbes Infect 5: 1041-1047.
49. van der Vliet HJ, van Vonderen MG, Molling JW, Bontkes HJ, Reijm M, et al. (2006) Cutting edge: Rapid recovery of NKT cells upon institution of highly active antiretroviral therapy for HIV-1 infection. J Immunol 177: 5775-5778.
50. Moll M, Snyder-Cappione J, Spotts G, Hecht FM, Sandberg JK, et al. (2006) Expansion of CD1d-restricted NKT cells in patients with primary HIV-1 infection treated with interleukin-2. Blood 107: 3081-3083.
51. Vasan S, Poles MA, Horowitz A, Siladji EE, Markowitz M, et al. (2007) Function of NKT cells, potential anti-HIV effector cells, are improved by beginning HAART during acute HIV-1 infection. Int Immunol 19: 943-951.
52. Yang OO, Wilson SB, Hultin LE, Detels R, Hultin PM, et al. (2007) Delayed reconstitution of CD4+ iNKT cells after effective HIV type 1 therapy. AIDS Res Hum Retroviruses 23: 913-922.
53. Moll M, Kuylenstierna C, Gonzalez VD, Andersson SK, Bosnjak L, et al. (2009) Severe functional impairment and elevated PD-1 expression in CD1d-restricted NKT cells retained during chronic HIV-1 infection. Eur J Immunol 39: 902-911.
54. Fernandez CS, Chan AC, Kyparissoudis K, De Rose R, Godfrey DI, et al. (2009) Peripheral NKT cells in simian immunodeficiency virus-infected macaques. J Virol 83: 1617-1624.
55. Exley MA, Hou R, Shaulov A, Tonti E, Dellabona P, et al. (2008) Selective activation, expansion, and monitoring of human iNKT cells with a monoclonal antibody specific for the TCR alpha-chain CDR3 loop. Eur J Immunol 38: 1756-1766.
56. Benlagha K, Weiss A, Beavis A, Teyton L, Bendelac A (2000) In vivo identification of glycolipid antigen-specific T cells using fluorescent CD1d tetramers. J Exp Med 191: 1895-1903.
57. Liu Y, Goff RD, Zhou D, Mattner J, Sullivan BA, et al. (2006) A modified alphagalactosyl ceramide for staining and stimulating natural killer T cells. J Immunol Methods 312: 34-39.
58. Gadola SD, Dulphy N, Salio M, Cerundolo V (2002) Valpha24-JalphaQindependent, CD1d-restricted recognition of alpha-galactosylceramide by human CD4(+) and CD8alphabeta(+) T lymphocytes. J Immunol 168: 5514-5520.
59. Van Rhijn I, Young DC, Im JS, Levery SB, Illarionov PA, et al. (2004) CD1drestricted T cell activation by nonlipidic small molecules. Proc Natl Acad Sci U S A 101: 13578-13583.
60. Shaulov A, Yue S, Wang R, Joyce RM, Balk SP, et al. (2008) Peripheral blood progenitor cell product contains Th1-biased noninvariant CD1d-reactive natural killer T cells: implications for posttransplant survival. Exp Hematol 36: 464-472.
61. Gumperz JE, Miyake S, Yamamura T, Brenner MB (2002) Functionally distinct subsets of CD1d-restricted natural killer T cells revealed by CD1d tetramer staining. J Exp Med 195: 625-636.
62. Kashiwase K, Kikuchi A, Ando Y, Nicol A, Porcelli SA, et al. (2003) The CD1d natural killer T-cell antigen presentation pathway is highly conserved between humans and rhesus macaques. Immunogenetics 54: 776-781.
63. Gansuvd B, Goodwin J, Asiedu CK, Jiang XL, Jargal U, et al. (2008) Invariant natural killer T cells from rhesus macaque spleen and peripheral blood are phenotypically and functionally distinct populations. J Med Primatol 37: 1-11.
64. Exley M, Porcelli S, Furman M, Garcia J, Balk S (1998) CD161 (NKR-P1A) costimulation of CD1d-dependent activation of human T cells expressing invariant V alpha 24 J alpha Q T cell receptor alpha chains. J Exp Med 188: 867-876.
65. Makino Y, Kanno R, Ito T, Higashino K, Taniguchi M (1995) Predominant expression of invariant V alpha 14+ TCR alpha chain in NK1.1+ T cell populations. Int Immunol 7: 1157-1161.
66. Kim CH, Johnston B, Butcher EC (2002) Trafficking machinery of NKT cells: shared and differential chemokine receptor expression among V alpha 24(+)V beta 11(+) NKT cell subsets with distinct cytokine-producing capacity. Blood 100: 11-16.
67. Exley M, Garcia J, Balk SP, Porcelli S (1997) Requirements for CD1d recognition by human invariant Valpha24+ CD4-CD8-T cells. J Exp Med 186: 109-120.
68. Lee PT, Benlagha K, Teyton L, Bendelac A (2002) Distinct functional lineages of human V(alpha)24 natural killer T cells. J Exp Med 195: 637-641.
69. Campillo-Gimenez L, Cumont MC, Fay M, Kared H, Monceaux V, et al. (2010) AIDS Progression Is Associated with the Emergence of IL-17-Producing Cells Early After Simian Immunodeficiency Virus Infection. J Immunol 184: 984-992.
70. Hammond KJ, Pelikan SB, Crowe NY, Randle-Barrett E, Nakayama T, et al. (1999) NKT cells are phenotypically and functionally diverse. Eur J Immunol 29: 3768-3781.
71. Bendelac A, Lantz O, Quimby ME, Yewdell JW, Bennink JR, et al. (1995) CD1 recognition by mouse NK1+ T lymphocytes. Science 268: 863-865.
72. Loza MJ, Metelitsa LS, Perussia B (2002) NKT and T cells: coordinate regulation of NK-like phenotype and cytokine production. Eur J Immunol 32: 3453-3462.
73. Jamieson AM, Diefenbach A, McMahon CW, Xiong N, Carlyle JR, et al. (2002) The role of the NKG2D immunoreceptor in immune cell activation and natural killing. Immunity 17: 19-29.
74. Vilarinho S, Ogasawara K, Nishimura S, Lanier LL, Baron JL (2007) Blockade of NKG2D on NKT cells prevents hepatitis and the acute immune response to hepatitis B virus. Proc Natl Acad Sci U S A 104: 18187-18192.
75. Thomas SY, Hou R, Boyson JE, Means TK, Hess C, et al. (2003) CD1drestricted NKT cells express a chemokine receptor profile indicative of Th1-type inflammatory homing cells. J Immunol 171: 2571-2580.
76. Liu TY, Uemura Y, Suzuki M, Narita Y, Hirata S, et al. (2008) Distinct subsets of human invariant NKT cells differentially regulate T helper responses via dendritic cells. Eur J Immunol 38: 1012-1023.
77. Gansuvd B, Hubbard WJ, Hutchings A, Thomas FT, Goodwin J, et al. (2003) Phenotypic and functional characterization of long-term cultured rhesus macaque spleen-derived NKT cells. J Immunol 171: 2904-2911.
78. Grubor-Bauk B, Arthur JL, Mayrhofer G (2008) Importance of NKT cells in resistance to herpes simplex virus, fate of virus-infected neurons, and level of latency in mice. J Virol 82: 11073-11083.
79. Liu R, La Cava A, Bai XF, Jee Y, Price M, et al. (2005) Cooperation of invariant NKT cells and CD4+CD25+ T regulatory cells in the prevention of autoimmune myasthenia. J Immunol 175: 7898-7904.
80. Jiang S, Game DS, Davies D, Lombardi G, Lechler RI (2005) Activated CD1drestricted natural killer T cells secrete IL-2: innate help for CD4+CD25+ regulatory T cells? Eur J Immunol 35: 1193-1200.
81. Roelofs-Haarhuis K, Wu X, Gleichmann E (2004) Oral tolerance to nickel requires CD4+ invariant NKT cells for the infectious spread of tolerance and the induction of specific regulatory T cells. J Immunol 173: 1043-1050.
82. Terabe M, Matsui S, Park JM, Mamura M, Noben-Trauth N, et al. (2003) Transforming growth factor-beta production and myeloid cells are an effector mechanism through which CD1d-restricted T cells block cytotoxic T lymphocyte-mediated tumor immunosurveillance: abrogation prevents tumor recurrence. J Exp Med 198: 1741-1752.
83. Exley M, Garcia J, Wilson SB, Spada F, Gerdes D, et al. (2000) CD1d structure and regulation on human thymocytes, peripheral blood T cells, B cells and monocytes. Immunology 100: 37-47.
84. Exley MA, Balk SP, Wilson SB (2003) Isolation and functional use of human NK T cells. Curr Protoc Immunol, Chapter 14: Unit 14 11.