Changes in T cell phenotype and activated MAPKs are correlated to impaired cellular responses to antigens and glucocorticoids during HTLV-I infection

Journal of Neuroimmunology

Volumn 216, Issue 1-2, 2009, Pages 76-84

  Pillat, Micheli M ^a   Correa, Bruna L ^a   da Rocha, Cláudio F K ^a   Müller, Guilherme C ^a   Lopes, Rodrigo P ^a,d   Lampert, Simone S ^a   Teixeira, Antônio L ^c   Menna Barreto, Márcio ^b   Bauer, Moisés E ^a  

^a PONTIFICAL CATHOLIC UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

^b Secretaria Municipal de Saude de Porto Alegre   (Brazil)

^c FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^d BD Biosciences   (Brazil)

Author keywords

Glucocorticoids; HTLV I; MAPK; Proliferation

Indexed keywords

DEXAMETHASONE; INTERLEUKIN 10; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 5; IONOMYCIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; PHORBOL 12 ACETATE 13 MYRISTATE; PHYTOHEMAGGLUTININ; TUMOR NECROSIS FACTOR ALPHA;

ADOLESCENT; ADULT; AGED; ARTICLE; CD4+ CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; HUMAN; HUMAN CELL; HUMAN T CELL LEUKEMIA VIRUS 1; HUMAN T CELL LEUKEMIA VIRUS INFECTION; IMMUNOMODULATION; LYMPHOCYTE PROLIFERATION; MALE; PERIPHERAL BLOOD MONONUCLEAR CELL; PHENOTYPIC VARIATION; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SPASTIC PARAPLEGIA; SPINAL CORD DISEASE; T LYMPHOCYTE ACTIVATION;

ADOLESCENT; ADULT; AGED; ANTIGEN PRESENTATION; BIOLOGICAL MARKERS; CELL DIFFERENTIATION; CELLS, CULTURED; DEXAMETHASONE; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; FLOW CYTOMETRY; GLUCOCORTICOIDS; HTLV-I INFECTIONS; HUMANS; IMMUNE TOLERANCE; IMMUNOSUPPRESSIVE AGENTS; LYMPHOCYTE ACTIVATION; MALE; MAP KINASE SIGNALING SYSTEM; MIDDLE AGED; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHENOTYPE; T-LYMPHOCYTES; UP-REGULATION; YOUNG ADULT;

EID: 72049127785     PISSN: 01655728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jneuroim.2009.08.016     Document Type: Article

References (62)

1. Adler H.S., Kubsch S., Graulich E., Ludwig S., Knop J., and Steinbrink K. Activation of MAP kinase p38 is critical for the cell-cycle-controlled suppressor function of regulatory T cells. Blood 109 (2007) 4351-4359
2. Al-Fahim A., Cabre P., Kastrukoff L., Dorovini-Zis K., and Oger J. Blood mononuclear cells in patients with HTLV-I-associated myelopathy: lymphocytes are highly activated and adhesion to endothelial cells is increased. Cell. Immunol. 198 (1999) 1-10
3. Aye M.M., Matsuoka E., Moritoyo T., Umehara F., Suehara M., Hokezu Y., Yamanaka H., Isashiki Y., Osame M., and Izumo S. Histopathological analysis of four autopsy cases of HTLV-I-associated myelopathy/tropical spastic paraparesis: inflammatory changes occur simultaneously in the entire central nervous system. Acta Neuropathol. (Berl) 100 (2000) 245-252
4. Balashov K.E., Khoury S.J., Hafler D.A., and Weiner H.L. Inhibition of T cell responses by activated human CD8+ T cells is mediated by interferon-gamma and is defective in chronic progressive multiple sclerosis. J. Clin. Invest. 95 (1995) 2711-2719
5. Brito-Melo G.E., Martins-Filho O.A., Carneiro-Proietti A.B., Catalan-Soares B., Ribas J.G., Thorum G.W., and Barbosa-Stancioli E.F. Phenotypic study of peripheral blood leucocytes in HTLV-I-infected individuals from Minas Gerais, Brazil. Scand. J. Immunol. 55 (2002) 621-628
6. Brito-Melo G.E., Souza J.G., Barbosa-Stancioli E.F., Carneiro-Proietti A.B., Catalan-Soares B., Ribas J.G., Thorum G.W., Rocha R.D., and Martins-Filho O.A. Establishing phenotypic features associated with morbidity in human T-cell lymphotropic virus type 1 infection. Clin. Diagn. Lab. Immunol. 11 (2004) 1105-1110
7. Brunetti M., Colasante A., Mascetra N., Piantelli M., Musiani P., and Aiello F.B. IL-10 synergizes with dexamethasone in inhibiting human T cell proliferation. J. Pharmacol. Exp. Ther. 285 (1998) 915-919
8. Chang C.C., Ciubotariu R., Manavalan J.S., Yuan J., Colovai A.I., Piazza F., Lederman S., Colonna M., Cortesini R., Dalla-Favera R., and Suciu-Foca N. Tolerization of dendritic cells by T(S) cells: the crucial role of inhibitory receptors ILT3 and ILT4. Nat. Immunol. 3 (2002) 237-243
9. Chow S., Patel H., and Hedley D.W. Measurement of MAP kinase activation by flow cytometry using phospho-specific antibodies to MEK and ERK: potential for pharmacodynamic monitoring of signal transduction inhibitors. Cytometry 46 (2001) 72-78
10. Croda M.G., de Oliveira A.C., Vergara M.P., Bonasser F., Smid J., Duarte A.J., and Casseb J. Corticosteroid therapy in TSP/HAM patients: the results from a 10 years open cohort. J. Neurol. Sci. 269 (2008) 133-137
11. Dong C., Yang D.D., Tournier C., Whitmarsh A.J., Xu J., Davis R.J., and Flavell R.A. JNK is required for effector T-cell function but not for T-cell activation. Nature 405 (2000) 91-94
12. Duma D., Jewell C.M., and Cidlowski J.A. Multiple glucocorticoid receptor isoforms and mechanisms of post-translational modification. J. Steroid Biochem. Mol. Biol. 102 (2006) 11-21
13. Edlich R.F., Arnette J.A., and Williams F.M. Global epidemic of human T-cell lymphotropic virus type-I (HTLV-I). J. Emerg. Med. 18 (2000) 109-119
14. Effros R.B., Allsopp R., Chiu C.P., Hausner M.A., Hirji K., Wang L., Harley C.B., Villeponteau B., West M.D., and Giorgi J.V. Shortened telomeres in the expanded CD28-CD8+ cell subset in HIV disease implicate replicative senescence in HIV pathogenesis. Aids 10 (1996) F17-F22
15. Fenoglio D., Ferrera F., Fravega M., Balestra P., Battaglia F., Proietti M., Andrei C., Olive D., Antonio L.C., Indiveri F., and Filaci G. Advancements on phenotypic and functional characterization of non-antigen-specific CD8+CD28- regulatory T cells. Hum. Immunol. 69 (2008) 745-750
16. Filaci G., Fravega M., Fenoglio D., Rizzi M., Negrini S., Viggiani R., and Indiveri F. Non-antigen specific CD8+ T suppressor lymphocytes. Clin. Exp. Med. 4 (2004) 86-92
17. Filaci G., Fravega M., Negrini S., Procopio F., Fenoglio D., Rizzi M., Brenci S., Contini P., Olive D., Ghio M., Setti M., Accolla R.S., Puppo F., and Indiveri F. Nonantigen specific CD8+ T suppressor lymphocytes originate from CD8+CD28- T cells and inhibit both T-cell proliferation and CTL function. Hum. Immunol. 65 (2004) 142-156
18. Filaci G., Fenoglio D., Fravega M., Ansaldo G., Borgonovo G., Traverso P., Villaggio B., Ferrera A., Kunkl A., Rizzi M., Ferrera F., Balestra P., Ghio M., Contini P., Setti M., Olive D., Azzarone B., Carmignani G., Ravetti J.L., Torre G., and Indiveri F. CD8+ CD28- T regulatory lymphocytes inhibiting T cell proliferative and cytotoxic functions infiltrate human cancers. J. Immunol. 179 (2007) 4323-4334
19. Fiorentino S., Dalod M., Olive D., Guillet J.G., and Gomard E. Predominant involvement of CD8+CD28- lymphocytes in human immunodeficiency virus-specific cytotoxic activity. J. Virol. 70 (1996) 2022-2026
20. Franceschi C., Bonafe M., and Valensin S. Human immunosenescence: the prevailing of innate immunity, the failing of clonotypic immunity, and the filling of immunological space. Vaccine 18 (2000) 1717-1720
21. Fukushima N., Nishiura Y., Nakamura T., Yamada Y., Kohno S., and Eguchi K. Involvement of p38 MAPK signaling pathway in IFN-gamma and HTLV-I expression in patients with HTLV-I-associated myelopathy/tropical spastic paraparesis. J. Neuroimmunol. 159 (2005) 196-202
22. Hayashi D., Kubota R., Takenouchi N., Tanaka Y., Hirano R., Takashima H., Osame M., Izumo S., and Arimura K. Reduced Foxp3 expression with increased cytomegalovirus-specific CTL in HTLV-I-associated myelopathy. J. Neuroimmunol. 200 (2008) 115-124
23. Hazzan M., Labalette M., Noel C., Lelievre G., and Dessaint J.P. Recall response to cytomegalovirus in allograft recipients: mobilization of CD57+, CD28+ cells before expansion of CD57+, CD28- cells within the CD8+ T lymphocyte compartment. Transplantation 63 (1997) 693-698
24. Hittelman A.B., Burakov D., Iniguez-Lluhi J.A., Freedman L.P., and Garabedian M.J. Differential regulation of glucocorticoid receptor transcriptional activation via AF-1-associated proteins. EMBO J. 18 (1999) 5380-5388
25. Ijichi S., Eiraku N., Osame M., Izumo S., Kubota R., Maruyama I., Matsumoto M., Niimura T., and Sonoda S. Activated T lymphocytes in cerebrospinal fluid of patients with HTLV-I-associated myelopathy (HAM/TSP). J. Neuroimmunol. 25 (1989) 251-254
26. Itoyama Y., Minato S., Kira J., Goto I., Sato H., Okochi K., and Yamamoto N. Spontaneous proliferation of peripheral blood lymphocytes increased in patients with HTLV-I-associated myelopathy. Neurology 38 (1988) 1302-1307
27. Jamieson C.A., and Yamamoto K.R. Crosstalk pathway for inhibition of glucocorticoid-induced apoptosis by T cell receptor signaling. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 7319-7324
28. Kam J.C., Szefler S.J., Surs W., Sher E.R., and Leung D.Y. Combination IL-2 and IL-4 reduces glucocorticoid receptor-binding affinity and T cell response to glucocorticoids. J. Immunol. 151 (1993) 3460-3466
29. Kaplan J.E., Osame M., Kubota H., Igata A., Nishitani H., Maeda Y., Khabbaz R.F., and Janssen R.S. The risk of development of HTLV-I-associated myelopathy/tropical spastic paraparesis among persons infected with HTLV-I. J. Acquir. Immune. Defic. Syndr. 3 (1990) 1096-1101
30. Katsuki T., Katsuki K., Imai J., and Hinuma Y. Immune suppression in healthy carriers of adult T-cell leukemia retrovirus (HTLV-I): impairment of T-cell control of Epstein-Barr virus-infected B-cells. Jpn. J. Cancer Res. 78 (1987) 639-642
31. Klatt T., Ouyang Q., Flad T., Koetter I., Buhring H.J., Kalbacher H., Pawelec G., and Muller C.A. Expansion of peripheral CD8+ CD28- T cells in response to Epstein-Barr virus in patients with rheumatoid arthritis. J. Rheumatol. 32 (2005) 239-251
32. Kogkopoulou O., Tzakos E., Mavrothalassitis G., Baldari C.T., Paliogianni F., Young H.A., and Thyphronitis G. Conditional up-regulation of IL-2 production by p38 MAPK inactivation is mediated by increased Erk1/2 activity. J. Leukoc. Biol. 79 (2006) 1052-1060
33. Kohno T., Yamada Y., Akamatsu N., Kamihira S., Imaizumi Y., Tomonaga M., and Matsuyama T. Possible origin of adult T-cell leukemia/lymphoma cells from human T lymphotropic virus type-1-infected regulatory T cells. Cancer Sci. 96 (2005) 527-533
34. Krstic M.D., Rogatsky I., Yamamoto K.R., and Garabedian M.J. Mitogen-activated and cyclin-dependent protein kinases selectively and differentially modulate transcriptional enhancement by the glucocorticoid receptor. Mol. Cell. Biol. 17 (1997) 3947-3954
35. Kubota R., Kawanishi T., Matsubara H., Manns A., and Jacobson S. Demonstration of human T lymphotropic virus type I (HTLV-I) tax-specific CD8+ lymphocytes directly in peripheral blood of HTLV-I-associated myelopathy/tropical spastic paraparesis patients by intracellular cytokine detection. J. Immunol. 161 (1998) 482-488
36. Lee C.H., Chen R.F., Liu J.W., Yeh W.T., and Yang K.D. Altered p38 mitogen-activated protein kinase expression in different leukocytes with increment of immunosuppressive mediators in patients with severe acute respiratory syndrome. J. Immunol. (2004) 7841-7847
37. Li Y.Q., Hii C.S., Der C.J., and Ferrante A. Direct evidence that ERK regulates the production/secretion of interleukin-2 in PHA/PMA-stimulated T lymphocytes. Immunology 96 (1999) 524-528
38. Lopes R.P., Menna-Barreto M., and Bauer M.E. Spontaneous cell proliferation is associated with poor sensitivity to glucocorticoids in patients infected with HTLV. Cell Prolif. 40 (2007) 64-74
39. Luz C., Collaziol D., Preissler T., da Cruz I.M., Glock L., and Bauer M.E. Healthy aging is associated with unaltered production of immunoreactive growth hormone but impaired neuroimmunomodulation. Neuroimmunomodulation 13 (2006) 160-169
40. Miller A.L., Webb M.S., Copik A.J., Wang Y., Johnson B.H., Kumar R., and Thompson E.B. p38 Mitogen-activated protein kinase (MAPK) is a key mediator in glucocorticoid-induced apoptosis of lymphoid cells: correlation between p38 MAPK activation and site-specific phosphorylation of the human glucocorticoid receptor at serine 211. Mol. Endocrinol. 19 (2005) 1569-1583
41. Miller A.L., Garza A.S., Johnson B.H., and Thompson E.B. Pathway interactions between MAPKs, mTOR, PKA, and the glucocorticoid receptor in lymphoid cells. Cancer Cell Int. 7 (2007) 3
42. Oh U., Grant C., Griffith C., Fugo K., Takenouchi N., and Jacobson S. Reduced Foxp3 protein expression is associated with inflammatory disease during human t lymphotropic virus type 1 Infection. J. Infect. Dis. 193 (2006) 1557-1566
43. Ohkusu-Tsukada K., Tominaga N., Udono H., and Yui K. Regulation of the maintenance of peripheral T-cell anergy by TAB1-mediated p38 alpha activation. Mol. Cell. Biol. 24 (2004) 6957-6966
44. Osame M. Review of WHO Kagoshima meeting and diagnostic guidelines for HAM/TSP (1990), Raven Press
45. Osborne B.A. Apoptosis and the maintenance of homoeostasis in the immune system. Curr. Opin. Immunol. 8 (1996) 245-254
46. Ouyang Q., Wagner W.M., Wikby A., Walter S., Aubert G., Dodi A.I., Travers P., and Pawelec G. Large numbers of dysfunctional CD8+ T lymphocytes bearing receptors for a single dominant CMV epitope in the very old. J. Clin. Immunol. 23 (2003) 247-257
47. Roos M.T., van Lier R.A., Hamann D., Knol G.J., Verhoofstad I., van Baarle D., Miedema F., and Schellekens P.T. Changes in the composition of circulating CD8+ T cell subsets during acute Epstein-Barr and human immunodeficiency virus infections in humans. J. Infect. Dis. 182 (2000) 451-458
48. Sakaguchi S., Yamaguchi T., Nomura T., and Ono M. Regulatory T cells and immune tolerance. Cell 133 (2008) 775-787
49. Sakai J.A., Nagai M., Brennan M.B., Mora C.A., and Jacobson S. In vitro spontaneous lymphoproliferation in patients with human T-cell lymphotropic virus type I-associated neurologic disease: predominant expansion of CD8+ T cells. Blood 98 (2001) 1506-1511
50. Simone R., Zicca A., and Saverino D. The frequency of regulatory CD3+CD8+CD28-CD25+ T lymphocytes in human peripheral blood increases with age. J. Leukoc. Biol. 84 (2008) 1454-1461
51. Sloan D.D., and Jerome K.R. Herpes simplex virus remodels T-cell receptor signaling, resulting in p38-dependent selective synthesis of interleukin-10. J. Virol. 81 (2007) 12504-12514
52. Tachibana N., Okayama A., Ishizaki J., Yokota T., Shishime E., Murai K., Shioiri S., Tsuda K., Essex M., and Mueller N. Suppression of tuberculin skin reaction in healthy HTLV-I carriers from Japan. Int. J. Cancer 42 (1988) 829-831
53. Thompson E.B. Stepping stones in the path of glucocorticoid-driven apoptosis of lymphoid cells. Acta Biochim. Biophys. Sin. (Shanghai) 40 (2008) 595-600
54. Toulza F., Heaps A., Tanaka Y., Taylor G.P., and Bangham C.R. High frequency of CD4+FoxP3+ cells in HTLV-1 infection: inverse correlation with HTLV-1-specific CTL response. Blood 111 (2008) 5047-5053
55. Trimble L.A., Kam L.W., Friedman R.S., Xu Z., and Lieberman J. CD3 and CD28 down-modulation on CD8T cells during viral infection. Immunobiology 96 (2000)
56. Tsitoura D.C., and Rothman P.B. Enhancement of MEK/ERK signaling promotes glucocorticoid resistance in CD4+ T cells. J. Clin. Invest. 113 (2004) 619-627
57. Veiopoulou C., Kogopoulou O., Tzakos E., Mavrothalassitis G., Mitsias D., Karafoulidou A., Paliogianni F., Moutsopoulos H.M., and Thyphronitis G. IL-2 and IL-10 production by human CD4+ T cells is differentially regulated by p38: mode of stimulation-dependent regulation of IL-2. Neuroimmunomodulation 11 (2004) 199-208
58. Wang Z., Frederick J., and Garabedian M.J. Deciphering the phosphorylation "code" of the glucocorticoid receptor in vivo. J. Biol. Chem. 277 (2002) 26573-26580
59. Weekes M.P., Carmichael A.J., Wills M.R., Mynard K., and Sissons J.G. Human CD28-CD8+ T cells contain greatly expanded functional virus-specific memory CTL clones. J. Immunol. 162 (1999) 7569-7577
60. Xystrakis E., Kusumakar S., Boswell S., Peek E., Urry Z., Richards D.F., Adikibi T., Pridgeon C., Dallman M., Loke T.K., Robinson D.S., Barrat F.J., O'Garra A., Lavender P., Lee T.H., Corrigan C., and Hawrylowicz C.M. Reversing the defective induction of IL-10-secreting regulatory T cells in glucocorticoid-resistant asthma patients. J. Clin. Invest. 116 (2006) 146-155
61. Yamano Y., Takenouchi N., Li H.C., Tomaru U., Yao K., Grant C.W., Maric D.A., and Jacobson S. Virus-induced dysfunction of CD4+CD25+ T cells in patients with HTLV-I-associated neuroimmunological disease. J. Clin. Invest. 115 (2005) 1361-1368
62. Yang D.D., Conze D., Whitmarsh A.J., Barrett T., Davis R.J., Rincon M., and Flavell R.A. Differentiation of CD4+ T cells to Th1 cells requires MAP kinase JNK2. Immunity 9 (1998) 575-585