Intestinal double-positive CD4+CD8+ T cells of neonatal rhesus macaques are proliferating, activated memory cells and primary targets for SIVMAC251 infection

Blood

Volumn 112, Issue 13, 2008, Pages 4981-4990

  Wang, Xiaolei ^a   Das, Arpita ^a   Lackner, Andrew A ^a   Veazey, Ronald S ^a   Pahar, Bapi ^a  

^a TULANE NATIONAL PRIMATE RESEARCH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD28 ANTIGEN; CD45RA ANTIGEN; CHEMOKINE RECEPTOR CCR5; FAS LIGAND; L SELECTIN; CYTOKINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4 CD8 T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL FUNCTION; CELL MATURATION; CELL PROLIFERATION; CELLULAR IMMUNITY; COMPARATIVE STUDY; CONTROLLED STUDY; FEMALE; IMMUNOPHENOTYPING; LYMPHOCYTE; LYMPHOCYTE PROLIFERATION; MALE; MEMORY CELL; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RHESUS MONKEY; SIMIAN IMMUNODEFICIENCY VIRUS; THYMUS; VIRUS INFECTION; ANIMAL; BIOSYNTHESIS; CELL DIFFERENTIATION; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; INTESTINE; MACACA; MONKEY DISEASE; PATHOLOGY; VIROLOGY;

ANIMALS; ANIMALS, NEWBORN; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; CELL PROLIFERATION; CYTOKINES; IMMUNOLOGIC MEMORY; INTESTINES; MACACA MULATTA; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME;

EID: 58149390134     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2008-05-160077     Document Type: Article

References (44)

1. Veazey RS, Mansfield KG, Tham IC, et al. Dynamics of CCR5 expression by CD4( + ) T cells in lymphoid tissues during simian immunodeficiency virus infection. J Virol. 2000;74:11001-11007.
2. Pahar B, Lackner AA, Veazey RS. Intestinal double-positive CD4+CD8+ T cells are highly activated memory cells with an increased capacity to produce cytokines. Eur J Immunol. 2006;36: 583-592.
3. Sala P, Tonutti E, Feruglio C, Florian F Colombatti A. Persistent expansions of CD4+ CD8+ peripheral blood T cells. Blood. 1993;82: 1546-1552.
4. Ortolani C, Forti E, Radin E, Cibin R, Cossarizza A. Cytofluorimetric identification of two populations of double positive (CD4+,CD8+)T lymphocytes in human peripheral blood. Biochem Bio-phys Res Commun. 1993;191:601-609.
5. Weiss L, RouxA, Garcia S, et al. Persistent expansion, in a human immunodeficiency virus-infected person, of V beta-restricted CD4+CD8 + T lymphocytes that express cytotoxicity-associated molecules and are committed to produce inter-feron-gamma and tumor necrosis factor-alpha. J Infect Dis. 1998;178:1158-1162.
6. Takahashi M, Ido E, UesakaH, et al. Comparison of susceptibility to SIVmac239 infection between CD4(+) and CD4( + )8(+) T cells. Arch Virol. 2005;150:1517-1528.
7. Akari H, Nam KH, Mori K, et al. Effects of SIVmac infection on peripheral blood CD4+CD8+ T lymphocytes in cynomolgus macaques. Clin Immunol. 1999;91:321-329.
8. Scott CS, Wheeler R, Ford P, Bynoe AG, Roberts BE. T lymphocyte subpopulations in idiopathic thrombocytopenic purpura (ITP). Scand J Haematol. 1983;30:401-406.
9. Matsui M, Fukuyama H, Akiguchi I, Kameyama M. Circulating CD4+CD8+ cells in myasthenia gravis: supplementary immunological parameter for long-term prognosis. J Neurol. 1989;236:329-335.
10. Airo P, Rossi G, Facchetti F, et al. Monoclonal expansion of large granular lymphocytes with a CD4+ CD8dim+/- phenotype associated with hairy cell leukemia. Haematologica. 1995;80:146-149.
11. Bagot M, Echchakir H, Mami-Chouaib F, et al. Isolation of tumor-specific cytotoxic CD4+ and CD4+CD8dim+ T-cell clones infiltrating a cutaneous T-cell lymphoma. Blood. 1998;91:4331-4341.
12. Parel Y, Aurrand-Lions M, SchejaA, Dayer JM, Roosnek E, Chizzolini C. Presence of CD4+CD8+ double-positive T cells with very high interleukin-4 production potential in lesional skin of patients with systemic sclerosis. Arthritis Rheum. 2007;56:3459-3467.
13. Jimenez E, Sacedon R, Vicente A, Hernandez-Lopez C, Zapata AG, Varas A. Rat peripheral CD4+CD8+ T lymphocytes are partially immunocompetent thymus-derived cells that undergo postthymic maturation to become functionally mature CD4+ T lymphocytes. J Immunol. 2002;168:5005-5013.
14. Nascimbeni M, Shin EC, Chiriboga L, Kleiner DE, Rehermann B. Peripheral CD4(+)CD8(+) T cells are differentiated effector memory cells with antiviral functions. Blood. 2004;104:478-486.
15. Periwal SB, Cebra JJ. Respiratory mucosal immunization with reovirus serotype 1/L stimulates virus-specific humoral and cellular immune responses, including double-positive (CD4+/ CD8+) T cells. J Virol. 1999;73:7633-7640.
16. Zuckermann FA, Husmann RJ. Functional and phenotypic analysis of porcine peripheral blood CD4/CD8 double-positive T cells. Immunology. 1996;87:500-512.
17. Veazey RS, DeMaria M, Chalifoux LV, et al. Gastrointestinal tract as a major site of CD4+ T cell depletion and viral replication in SIV infection. Science. 1998;280:427-431.
18. Wang X, Rasmussen T, Pahar B, et al. Massive infection and loss of CD4+ T cells occurs in the intestinal tract of neonatal rhesus macaques in acute SIV infection. Blood. 2007;109:1174-1181.
19. Brenchley JM, Schacker TW, Ruff LE, et al. CD4+ Tcell depletion during all stages of HIV disease occurs predominantly in the gastrointestinal tract. J Exp Med. 2004;200:749-759.
20. Veazey RS, Lifson JD, Pandrea I, Purcell J, Piatak M, Jr., Lackner AA. Simian immunodeficiency virus infection in neonatal macaques. J Virol. 2003;77:8783-8792.
21. Veazey RS, Rosenzweig M, Shvetz DE, et al. Characterization of gut-associated lymphoid tissue (GALT) of normal rhesus macaques. Clin Immunol Immunopathol. 1997;82:230-242.
22. Pahar B, Li J, RourkeT, Miller CJ, McChesney MB. Detection of antigen-specific T cell interferon gamma expression by ELISPOT and cytokine flow cytometry assays in rhesus macaques. J Immunol Methods. 2003;282:103-115.
23. Waldrop SL, Pitcher CJ, Peterson DM, Maino VC, Picker LJ. Determination of antigen-specific memory/effector CD4+ Tcell frequencies by flow cytometry: evidence for a novel, antigen-specific homeostatic mechanism in HIV-associated immunodeficiency. J Clin Invest. 1997;99:1739-1750.
24. OkoyeA, Meier-Schellersheim M, Brenchley JM, et al. Progressive CD4+ central memory Tcell decline results in CD4+ effector memory insufficiency and overt disease in chronic SIV infection. J Exp Med. 2007;204:2171-2185.
25. Pitcher CJ, Hagen SI, Walker JM, et al. Development and homeostasis of T cell memory in rhesus macaque. J Immunol. 2002;168:29-43.
26. Ivetic A, Ridley AJ. The telling tail of L-selectin. Biochem Soc Trans. 2004;32:1118-1121.
27. Gosling J, Dairaghi DJ, Wang Y, et al. Cutting edge: identification of a novel chemokine receptor that binds dendritic cell- and T cell-active chemo-kines including ELC, SLC, and TECK. J Immunol. 2000;164:2851-2856.
28. Pier GB, Geri H, Mody C, Preston M. T-cell maturation and activation. Washington, DC: ASM Press;2004.
29. Vanhecke D, Leclercq G, Plum J, Vandekerckhove B. Characterization of distinct stages during the differentiation of human CD69+CD3+ thymocytes and identification of thymic emigrants. J Immunol. 1995;155:1862-1872.
30. Ley K, Kansas GS. Selectins in T-cell recruitment to non-lymphoid tissues and sites of inflammation. Nat Rev Immunol. 2004;4:325-335.
31. Naito T, Shiohara T, Hibi T, Suematsu M, Ishikawa H. RORyt is dispensable for the development of intestinal mucosal T cells. Mucosal Immunol. 2008;1:198-207.
32. Suzuki K, Oida T, Hamada H, et al. Gut cryptopatches: direct evidence of extrathymic anatomical sites for intestinal T lymphopoiesis. Immunity. 2000;13:691-702.
33. Saito H, Kanamori Y, TakemoriT, et al. Generation of intestinal T cells from progenitors residing in gut cryptopatches. Science. 1998;280:275-278.
34. Hayday A, Theodoridis E, Ramsburg E, Shires J. Intraepithelial lymphocytes: exploring the Third Way in immunology. Nat Immunol. 2001;2:997-1003.
35. Howie D, Spencer J, DeLord D, et al. Extrathymic T cell differentiation in the human intestine early in life. J Immunol. 1998;161:5862-5872.
36. Spencer J, MacDonald TT, Finn T, Isaacson PG. The development of gut associated lymphoid tissue in the terminal ileum of fetal human intestine. Clin Exp Immunol. 1986;64:536-543.
37. Zaitseva MB, Lee S, Rabin RL, et al. CXCR4 and CCR5 on human thymocytes: biological function and role in HIV-1 infection. J Immunol. 1998;161: 3103-3113.
38. Pedroza-Martins L, Boscardin WJ, Anisman-Posner DJ, Schols D, Bryson YJ, Uittenbogaart CH. Impact of cytokines on replication in the thymus of primary human immunodeficiency virus type 1 isolates from infants. J Virol. 2002;76: 6929-6943.
39. 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;434:1093-1097.
40. Veazey RS, Marx PA, Lackner AA. The mucosal immune system: primary target for HIV infection and AIDS. Trends Immunol. 2001;22:626-633.
41. Li Q, Duan L, Estes JD, et al. Peak SIV replication in resting memory CD4+ T cells depletes gut lamina propria CD4+ T cells. Nature. 2005;434: 1148-1152.
42. Suni MA, Ghanekar SA, Houck DW, et al. CD4(+)CD8(dim) T lymphocytes exhibit enhanced cytokine expression, proliferation and cytotoxic activity in response to HCMV and HIV-1 antigens. Eur J Immunol. 2001;31:2512-2520.
43. ZlozaA, Sullivan YB, Connick E, Landay AL, Al-Harthi L. CD8+ T cells that express CD4 on their surface (CD4dimCD8bright T cells) recognize an antigen-specific target, are detected in vivo, and can be productively infected by T-tropic HIV. Blood. 2003;102:2156-2164.
44. De Boer RJ, Mohri H, Ho DD, Perelson AS. Turnover rates of B cells, T cells, and NK cells in simian immunodeficiency virus-infected and uninfected rhesus macaques. J Immunol. 2003;170: 2479-2487.