Expression of CD8α identifies a distinct subset of effector memory CD4+ T lymphocytes

Immunology

Volumn 119, Issue 2, 2006, Pages 232-242

  Macchia, Iole ^a,b   Gauduin, Marie Claire ^a   Kaur, Amitinder ^a   Johnson, R Paul ^a,c  

^a HARVARD MEDICAL SCHOOL   (United States)

^b ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Animal models studies: primates; Helper T cells (Th cells, Th0, Th1, Th2, Th3); Memory cells; Simian immunodeficiency virus

Indexed keywords

CD8ALPHA ANTIGEN; CYTOKINE; GRANZYME B; HLA DR ANTIGEN; HOMODIMER; CD8 ANTIGEN; VIRUS ANTIGEN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN EXPRESSION; ARTICLE; BLOOD; CD4 CD8 RATIO; CD4+ T LYMPHOCYTE; CELL POPULATION; CONTROLLED STUDY; CYTOMEGALOVIRUS; MACACA; MEMORY T LYMPHOCYTE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RHESUS MONKEY; SIMIAN IMMUNODEFICIENCY VIRUS; WILD TYPE; ANIMAL; BIOSYNTHESIS; FLOW CYTOMETRY; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; IMMUNOPHENOTYPING; LYMPHOCYTE ACTIVATION; METHODOLOGY; MONKEY DISEASE; T LYMPHOCYTE RECEPTOR GENE; T LYMPHOCYTE SUBPOPULATION;

ANIMALS; ANTIGENS, CD8; ANTIGENS, VIRAL; CD4-POSITIVE T-LYMPHOCYTES; CYTOKINES; FLOW CYTOMETRY; GENES, T-CELL RECEPTOR; IMMUNOLOGIC MEMORY; IMMUNOPHENOTYPING; LYMPHOCYTE ACTIVATION; MACACA MULATTA; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; T-LYMPHOCYTE SUBSETS;

EID: 33748740886     PISSN: 00192805     EISSN: 13652567     Source Type: Journal    
DOI: 10.1111/j.1365-2567.2006.02428.x     Document Type: Article

References (68)

1. Blue ML, Daley JF, Levine H, Schlossman SF. Co-expression of T4 and T8 on peripheral blood T cells demonstrated by two-color fluorescence flow cytometry. J Immunol 1985; 134:228-34.
2. Lanier LL, Phillips JH. Evidence for three types of human cytotoxic lymphocytes. Immunol Today 1986; 7:132-4.
3. +) T lymphocytes in human peripheral blood. Biochem Biophys Res Commun 1993; 191:601-9.
4. Colombatti A, Doliana R, Schiappacassi M, Argentini C, Tonutti E, Feruglio C, Sala P. Age-related persistent clonal expansions of CD28(-) cells: phenotypic and molecular TCR analysis reveals both CD4(+) and CD4(+) CD8(+) cells with identical CDR3 sequences. Clin Immunol Immunopathol 1998; 89:61-70.
5. Prince H, Golding J, York J. Characterization of circulating CD4+ CD8+ lymphocytes in healthy individuals prompted by identification of a blood donor with a markedly elevated level of CD4+ CD8+ lymphocytes. Clin Diagn Lab Immunol 1994; 1:597-605.
6. Sala P, Tonutti E, Feruglio C, Florian F, Colombatti A. Persistent expansions of CD4+ CD8+ peripheral blood T cells. Blood 1993; 1:1546-52.
7. Tonutti E, Sala P, Feruglio C, Yin Z, Colombatti A. Phenotypic heterogeneity of persistent expansions of CD4+ CD8+ T cells. Clin Immunol Immunopathol 1994; 73:312-20.
8. 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; 91:4331-41.
9. Mizuki M, Tagawa S, Machii T et al. Phenotypical heterogeneity of CD4+ CD8+ double-positive chronic T lymphoid leukemia. Leukemia 1998; 12:499-504.
10. 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; 236:329-35.
11. Weiss L, Roux A, Garcia S, Demouchy C, Haeffner-Cavaillon N, Kazatchkine MD, Gougeon ML. Persistent expansion, in human immunodeficiency virus-infected person, of V beta-restricted CD4+ CD8+ T lymphocytes that express cytotoxicity-associated molecules and are committed to produce interferon-gamma and tumor necrosis factor-alpha. J Infect Dis 1998; 178:1158-62.
12. Suni MA, Ghanekar SA, Houck DW, Maecker HT, Wormsley SB, Picker LJ, Moss RB, Maino VC. 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; 31:2512-20.
13. Sullivan YB, Landay AL, Zack JA, Kitchen SG, Al-Harthi L. Upregulation of CD4 on CD8+ T cells: CD4dim CD8bright T cells constitute an activated phenotype of CD8+ T cells. Immunology 2001; 103:270-80.
14. Sasahara T, Tamauchi H, Ikewaki N, Kubota K. Unique properties of a cytotoxic CD4+ CD8+ intraepithelial T-cell line established from the mouse intestinal epithelium. Microbiol Immunol 1994; 38:191-9.
15. Kenny E, Mason D, Pombo A, Ramirez F. Phenotypic analysis of peripheral CD4+ CD8+ T cells in the rat. Immunology 2000; 101:178-84.
16. Zuckermann FA, Husmann RJ. Functional and phenotypic analysis of porcine peripheral blood CD4/CD8 double-positive T cells. Immunology 1996; 87:500-12.
17. Akari H, Terao K, Murayama Y, Nam KH, Yoshikawa Y. Peripheral blood CD4+ CD8+ lymphocytes in cynomolgus monkeys are of resting memory T lineage. Int Immunol 1997; 9:591-7.
18. Pescovitz MD, Sakopoulos AG, Gaddy JA, Husmann RJ, Zuckermann FA. Porcine peripheral blood CD4+ CD8+ dual expressing T-cells. Vet Immunol Immunopathol 1994; 43:53-62.
19. Bonomo A, Kehn PJ, Shevach EM. Premature escape of double-positive thymocytes to the periphery of young mice. Possible role in autoimmunity. J Immunol 1994; 152:1509-14.
20. Res P, Blom B, Hori T, Weijer K, Spits H. Downregulation of CD1 marks acquisition of functional maturation of human thymocytes and defines a control point in late stages of human T cell development. J Exp Med 1997; 185:141-51.
21. Watanabe N, DeRosa SC, Cmelak A, Hoppe R, Herzenberg LA, Herzenberg LA, Roederer M. Long-term depletion of naive T cells in patients treated for Hodgkin's disease. Blood 1997; 90:3662-72.
22. Paliard X, Malefijt RW, de Vries JE, Spits H. Interleukin-4 mediates CD8 induction on human CD4+ T-cell clones. Nature 1988; 335:642-4.
23. Zuckermann FA. Extrathymic CD4/CD8 double positive T cells. Vet Immunol Immunopathol 1999; 72:55-66.
24. Flamand L, Crowley RW, Lusso P, Columbini-Hatch S, Margolis DM, Gallo RC. Activation of CD8+ T lymphocytes through the T cell receptor turns on CD4 gene expression: implications for HIV pathogenesis. Proc Natl Acad Sci USA 1998; 95:3111-16.
25. Kestler HW III, Ringler DJ, Mori K, Panicali DL, Sehgal PK, Daniel MD, Desrosiers RC. Importance of the nef gene for maintenance of high virus loads and for development of AIDS. Cell 1991; 65:651-62.
26. Wyand MS, Manson KH, Garcia-Moll M, Montefiori D, Desrosiers RC. Vaccine protection by a triple deletion mutant of simian immunodeficiency virus. J Virol 1996; 70:3724-33.
27. Kaur A, Hale CL, Noren B, Kassis N, Simon MA, Johnson RP. Decreased frequency of cytomegalovirus (CMV) -specific CD4+ T lymphocytes in simian immunodeficiency virus-infected rhesus macaques: inverse relationship with CMV viremia. J Virol 2002; 76:3646-58.
28. Anonymous. The Institute of Laboratory Animal Resources, National. Research Council, Guide for the Care and Use of Laboratory Animals. Washington, DC: National Institutes of Health, 1996:86-123.
29. DiSanto JP, Knowles RW, Flomenberg N. The human Lyt-3 molecule requires CD8 for cell surface expression. Embo J 1988; 7:3465-70.
30. Norment AM, Littman DR. A second subunit of CD8 is expressed in human T cells. EMBO J 1988; 7:3433-9.
31. Roederer M. Spectral compensation for flow cytometry. Visualization artifacts, limitations, and caveats. Cytometry 2001; 45:194-205.
32. Gauduin M-C, Kaur A, Ahmad S, Yilma T, Lifson JD, Johnson RP. Optimization of intracellular cytokine staining for the quantitation of antigen-specific CD4+ T cell responses in rhesus macaques. J Immunol Meth 2004; 288:61-79.
33. Pitcher CJ, Hagen SI, Walker JM, Lum R, Mitchell BL, Maino VC, Axthelm MK, Picker LJ. Development and homeostasis of T cell memory in rhesus macaque. J Immunol 2002; 168:29-43.
34. Douek DC, McFarland RD, Keiser PH et al. Changes in thymic function with age and during the treatment of HIV infection. Nature 1998; 396:690-5.
35. Sodora DL, Douek DC, Silvestri G et al. Quantification of thymic function by measuring T cell receptor excision circles within peripheral blood and lymphoid tissues in monkeys. Eur J Immunol 2000; 30:1145-53.
36. Chakrabarti LA, Lewin SR, Zhang L et al. Normal T-cell turnover in sooty mangabeys harboring active simian immunodeficiency virus infection. J Virol 2000; 74:1209-23.
37. Macchi B, Graziani G, Zhang J, Mastino A. Emergence of double-positive CD4/CD8 cells from adult peripheral blood mononuclear cells infected with human T cell leukemia virus type I (HTLV-1). Cell Immunol 1993; 149:376-89.
38. Aandahl EM, Sandberg JK, Beckerman KP, Tasken K, Moretto WJ, Nixon DF. CD7 is a differentiation marker that identifies multiple CD8 T cell effector subsets. J Immunol 2003; 170:2349-55.
39. Nam KH, Akari H, Terao K, Shibata H, Kawamura S, Yoshikawa Y. Peripheral blood extrathymic CD4(+) CD8(+) T cells with high cytotoxic activity are from the same lineage as CD4(+) CD8(-) T cells in cynomolgus monkeys. Int Immunol 2000; 12:1095-103.
40. Nascimbeni M, Shin E-C, Chiriboga L, Kleiner DE, Rehermann B. Peripheral CD4+ CD8+ T cells are differentiated effector memory cells with antiviral functions. Blood 2004; 104:478-86.
41. bright double-positive T-lymphocytes have a phenotype of granzyme B+ CD8+ memory T-lymphocytes. Nephrol Dial Transplant 1999; 14:1430-4.
42. Gerdes J, Lemke H, Baisch H, Wacker HH, Schwab U, Stein H. Cell cycle analysis of a cell proliferation-associated human nuclear antigen defined by the monoclonal antibody Ki-67. J Immunol 1984; 133:1710-15.
43. Chen Z, Zhou P, Ho DD, Landau NR, Marx PA. Genetically divergent strains of simian immunodeficiency virus use CCR5 as a coreceptor for entry. J Virol 1997; 71:2705-14.
44. Veazey RS, Tham IC, Mansfield KG et al. Identifying the target cell in primary simian immunodeficiency virus (SIV) infection: highly activated memory CD4+ T cells are rapidly eliminated in early SIV infection in vivo. J Virol 2000; 74:57-64.
45. Gauduin M-C, Glickman RL, Ahmad S, Yilma T, Johnson RP. Immunization with live attenuated simian immunodeficiency virus induces strong type 1 T helper responses and β-chemokine production. Proc Natl Acad Sci USA 1999; 96:14031-6.
46. Kong F, Chen CH, Cooper MD. Thymic function can be accurately monitored by the level of recent T cell emigrants in the circulation. Immunity 1998; 8:97-104.
47. Parel Y, Chizzolini C. CD4+ CD8+ double positive (DP) T cells in health and disease. Autoimmun Rev 2004; 3:215-20.
48. Schmitz JE, Forman MA, Lifton MA et al. Expression of the CD8αβ-heterodimer on CD8(+) T lymphocytes in peripheral blood lymphocytes of human immunodeficiency virus- and human immunodeficiency virus+ individuals. Blood 1998; 92:198-206.
49. Graham MB, Braciale VL, Braciale TJ. Influenza virus-specific CD4+ T helper type 2 T lymphocytes do not promote recovery from experimental virus infection. J Exp Med 1994; 180:1273-82.
50. Christensen JP, Cardin RD, Branum KC, Doherty PC. CD4(+) T cell-mediated control of a gamma-herpesvirus in B cell-deficient mice is mediated by IFN-gamma. Proc Natl Acad Sci USA 1999; 96:5135-40.
51. Iwashiro M, Peterson K, Messer RJ, Stromnes IM, Hasenkrug KJ. CD4(+) T cells and gamma interferon in the long-term control of persistent friend retrovirus infection. J Virol 2001; 75:52-60.
52. Norris PJ, Sumaroka M, Brander C et al. Multiple effector functions mediated by human immunodeficiency virus-specific CD4(+) T-cell clones. J Virol 2001; 75:9771-9.
53. Zaunders JJ, Dyer WB, Wang B et al. Identification of circulating antigen-specific CD4+ T lymphocytes with a CCR5+, cytotoxic phenotype in an HIV-1 long-term nonprogressor and in CMV infection. Blood 2004; 103:2238-47.
54. Appay V, Zaunders JJ, Papagno L et al. Characterization of CD4+ CTLs ex vivo. J Immunol 2002; 168:5954-8.
55. Veazey RS, Mansfield KG, Tham IC, Carville AC, Shvetz DE, Forand AE, Lackner AA. Dynamics of CCR5 expression by CD4+ T cells in lymphoid tissues during simian immunodeficiency virus infection. J Virol 2000; 74:11001-7.
56. Mattapallil JJ, Douek DC, Hill BJ, Nishimura Y, Martin M, Roederer M. Massive infection and loss of memory CD4+ T cells in multiple tissues during acute SIV infection. Nature 2005; 434:1093-7.
57. Akari H, Nam KH, Mori K, Otani I, Shibata H, Adachi A, Terao K, Yoshikawa Y. Effects of SIVmac infection on peripheral blood CD4+ CD8+ T lymphocytes in cynomolgus macaques. Clin Immunol 1999; 91:321-9.
58. Brenchley JM, Schacker TW, Ruff LE et al. CD4+ T cell depletion during all stages of HIV disease occurs predominantly in the gastrointestinal tract. J Exp Med 2004; 200:749-59.
59. Lackner A. Pathology of simian immunodeficiency virus induced disease. Curr Top Microbiol Immunol 1994; 188:35-59.
60. Schmitz JE, Kuroda MJ, Santra S et al. Control of viremia in simian immunodeficiency virus infection by CD8+ lymphocytes. Science 1999; 283:857-60.
61. Jin X, Bauer DE, Tuttleton SE et al. Dramatic rise in plasma viremia after CD8(+) T cell depletion in simian immunodeficiency virus-infected macaques. J Exp Med 1999; 189:991-8.
62. Webster RL, Johnson RP. Delineation of multiple subpopulations of natural killer cells in rhesus macaques. Immunology 2005; 115:206-14.
63. Gangadharan D, Cheroutre H. The CD8 isoform CD8αα is not a functional homologue of the TCR co-receptor CD8αβ. Curr Opin Immunol 2004; 16:264-70.
64. Salter RD, Benjamin RJ, Wesley PK et al. A binding site for the T-cell co-receptor CD8 on the alpha 3 domain of HLA-A2. Nature 1990; 345:41-6.
65. Hoeveler A, Malissen B. The cysteine residues in the cytoplasmic tail of CD8 alpha are required for its coreceptor function. Mol Immunol 1993; 30:755-64.
66. Wong JS, Wang X, Witte T, Nie L, Carvou N, Kern P, Chang HC. Stalk region of beta-chain enhances the coreceptor function of CD8. J Immunol 2003; 171:867-74.
67. Arcaro A, Gregoire C, Boucheron N, Stotz S, Palmer E, Malissen B, Luescher IF. Essential role of CD8 palmitoylation in CD8 coreceptor function. J Immunol 2000; 165:2068-76.
68. Gao MH, Walz M, Kavathas PB. Post-transcriptional regulation associated with control of human CD8 alpha expression of CD4+ T cells. Immunogenetics 1996; 45:130-5.