FOXP3 expression and frequency of regulatory T cells in healed individuals from Leishmania major infection and the asymptomatic cases

Human Immunology

Volumn 75, Issue 10, 2014, Pages 1026-1033

  Bahrami, Fariborz ^a   Darabi, Haiedeh ^a   Riazi Rad, Farhad ^a   Khaze, Vahid ^a   Ajdary, Soheila ^a   Alimohammadian, Mohammad Hossein ^a  

^a PASTEUR INSTITUTE OF IRAN   (Iran)

Author keywords

Asymptomatic individuals; Cutaneous leishmaniasis; Leishmania major; Regulatory T cell

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 4; RETINOID RELATED ORPHAN RECEPTOR GAMMA; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA; CYTOKINE; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, HUMAN; LEISHMANIN; PARASITE ANTIGEN; RORC PROTEIN, HUMAN;

ADOLESCENT; ADULT; ARTICLE; ASYMPTOMATIC INFECTION; CD4 LYMPHOCYTE PERCENTAGE; CD4+ CD25+ T LYMPHOCYTE; CELLULAR IMMUNITY; CLINICAL ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION ASSAY; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IRAN; LEISHMANIA MAJOR; LYMPHOCYTE COUNT; MALE; PERIPHERAL BLOOD MONONUCLEAR CELL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SKIN LEISHMANIASIS; ASYMPTOMATIC DISEASE; CELL CULTURE; CHILD; GENETICS; HELPER CELL; IMMUNOLOGY; METABOLISM; MIDDLE AGED; SKIN TEST; UPREGULATION; YOUNG ADULT;

ADOLESCENT; ADULT; ANTIGENS, PROTOZOAN; ASYMPTOMATIC DISEASES; CELLS, CULTURED; CHILD; CYTOKINES; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; IRAN; LEISHMANIA MAJOR; LEISHMANIASIS, CUTANEOUS; MALE; MIDDLE AGED; NUCLEAR RECEPTOR SUBFAMILY 1, GROUP F, MEMBER 3; SKIN TESTS; T-LYMPHOCYTES, HELPER-INDUCER; T-LYMPHOCYTES, REGULATORY; UP-REGULATION; YOUNG ADULT;

EID: 84907991749     PISSN: 01988859     EISSN: 18791166     Source Type: Journal    
DOI: 10.1016/j.humimm.2014.08.204     Document Type: Article

References (49)

1. Kaye P., Scott P. Leishmaniasis: complexity at the host-pathogen interface. Nat Rev Microbiol 2011, 9:604.
2. Kedzierski L. Leishmaniasis vaccine: where are we today?. J Glob Infect Dis 2010, 2:177.
3. Neghina R., Neghina A.M. Leishmaniasis, a global concern for travel medicine. Scand J Infect Dis 2010, 42:563.
4. Croft S.L., Vivas L., Brooker S. Recent advances in research and control of malaria, leishmaniasis, trypanosomiasis and schistosomiasis. East Mediterr Health J 2003, 9:518.
5. Desjeux P. Leishmaniasis: current situation and new perspectives. Comp Immunol Microbiol Infect Dis 2004, 27:305.
6. Gramiccia M., Gradoni L. The current status of zoonotic leishmaniases and approaches to disease control. Int J Parasitol 2005, 35:1169.
7. Mahmoudzadeh-Niknam H., Ajdary S., Riazi-Rad F., Mirzadegan E., Rezaeian A., Khaze V., et al. Molecular epidemiology of cutaneous leishmaniasis and heterogeneity of Leishmania major strains in Iran. Trop Med Int Health 2012, 17:1335.
8. Modabber F. Leishmaniasis. In: Tropical disease research. Progress 1975-94, Highlights 1993-1994. Twelfth programme report, UNDP/Word Bank/WHO, Special programme for research & training in tropical disease (TDR). Geneva: World Health Organization; 1995. p. 135-146.
9. Mauel J., Behin R. Leishmaniasis: immunity, immunopathology and immunodiagnosis. Immunology of parasitic infection 1982, 299-314. Blackwell Scientific Publication, Oxford. S. Cohen, K.S. Warren (Eds.).
10. Manson-Bahr P.E.C. Diagnosis. Clinical aspects and control 1987, vol. 2:703-729. Academic Press, London. W. Peters, R. Killick-Kendrick (Eds.).
11. Alimohammadian M.H., Almasi H., Khabiri A.R., Hatam G.R., Karimi A., Mahboudi F., et al. Identification of species and characterization of an outbreak of cutaneous leishmaniasis in a new focus of Iran. Iranian Biomed J 1999, 3:31.
12. Moral L., Rubio E.M., Moya M. A leishmanin skin test survey in the human population of l'Alacanti region (Spain): implications for the epidemiology of Leishmania infantum infection in southern Europe. Trans R Soc Trop Med Hyg 2002, 96:129.
13. Bañuls A.L., Bastien P., Pomares C., Arevalo J., Fisa R., Hide M. Clinical pleiomorphism in human leishmaniases, with special mention of asymptomatic infection. Clin Microbiol Infect 2011, 17:1451.
14. Bacchetta R., Gambineri E., Roncarolo M.G. Role of regulatory T cells and FOXP3 in human diseases. J Allergy Clin Immunol 2007, 120:227.
15. Chen W., Jin W., Hardegen N., Lei K.J., Li L., Marinos N., et al. Conversion of peripheral CD4+CD25- naive T cells to CD4+CD25+ regulatory T cells by TGF-beta induction of transcription factor Foxp3. J Exp Med 2003, 198:1875.
16. Liston A., Gray D.H. Homeostatic control of regulatory T cell diversity. Nat Rev Immunol 2014, 14:154.
17. Campanelli A.P., Roselino A.M., Cavassani K.A., Pereira M.S., Mortara R.A., Brodskyn C.I., et al. CD4+CD25+ T cells in skin lesions of patients with cutaneous leishmaniasis exhibit phenotypic and functional characteristics of natural regulatory T cells. J Infect Dis 2006, 193:1313.
18. Hoseini S.G., Javanmard S.H., Zarkesh S.H., Khamesipour A., Rafiei L., Karbalaie K., et al. Regulatory T-cell profile in early and late lesions of cutaneous leishmaniasis due to Leishmania major. J Res Med Sci 2012, 17:513.
19. Velavan T.P., Ojurongbe O. Regulatory T cells and parasites. J Biomed Biotechnol 2011, 2011:520940.
20. Falcão SC, de Moura T.R., Clarencio J., Brodskyn C., Barral A., de Oliveira C.I. The presence of Tregs does not preclude immunity to reinfection with Leishmania braziliensis. Int J Parasitol 2012, 42:771.
21. Nagase H., Jones K.M., Anderson C.F., Noben-Trauth N. Despite increased CD4+Foxp3+ cells within the infection site, BALB/c IL-4 receptor-deficient mice reveal CD4+Foxp3-negative T cells as a source of IL-10 in Leishmania major susceptibility. J Immunol 2007, 179:2435.
22. Suffia I., Reckling S.K., Salay G., Belkaid Y. A role for CD103 in the retention of CD4+CD25+ Treg and control of Leishmania major infection. J Immunol 2005, 174:5444.
23. Rouse B.T., Suvas S. Regulatory cells and infectious agents: détentes cordiale and contraire. J Immunol 2004, 173:2211.
24. Bourreau E., Ronet C., Darcissac E., Lise M.C., Sainte Marie D., Clity E., et al. Intralesional regulatory T-cell suppressive function during human acute and chronic cutaneous leishmaniasis due to Leishmania guyanensis. Infect Immun 2009, 77:1465.
25. Bourreau E., Ronet C., Darsissac E., Lise M.C., Marie D.S., Clity E., et al. In leishmaniasis due to Leishmania guyanensis infection, distinct intralesional interleukin-10 and Foxp3 mRNA expression are associated with unresponsiveness to treatment. J Infect Dis 2009, 199:576.
26. Rodriguez-Pinto D., Navas A., Blanco V.M., Ramirez L., Garcerant D., Cruz A., et al. Regulatory T cells in the pathogenesis and healing of chronic human dermal leishmaniasis caused by Leishmania (Viannia) species. PLoS Negl Trop Dis 2012, 6:e1627.
27. Alimohammadian M.H., Hakimi H., Nikseresht M.A. The preparation and evaluation of reference leishman from Leishmania major for use in man for diagnostic and experimental purposes. Med J Islamic Republic Iran 1993, 93:23.
28. Alimohammadian M.H., Kivanjah M., Pak F., Gaznavia A., Kharazmi A. Evaluation of the efficacy of Iran leishmanin and comparison with leishmanins from Wellcome (UK) and Roma (Italy) in cured cutaneous leishmaniasis patients. Trans R Soc Trop Med Hyg 1993, 87:550.
29. Sokal J.E. Editorial: measurement of delayed skin-test responses. N Engl J Med 1975, 293:501.
30. Ajdary S., Alimohammadian M.H., Eslami M.B., Kemp K., Kharazmi A. Comparison of the immune profile of nonhealing cutaneous leishmaniasis patients with those with active lesions and those who have recovered from infection. Infect Immun 2000, 68:1760.
31. Salhi A., Rodrigues V., Santoro F., Dessein H., Romano A., Castellano L.R., et al. Immunological and genetic evidence for a crucial role of IL-10 in cutaneous lesions in humans infected with Leishmania braziliensis. J Immun 2008, 180:6139.
32. Costa D.L., Guimaraes L.H., Cardoso T.M., Queiroz A., Lago E., Roselino A.M., et al. Characterization of regulatory T cell (Treg) function in patients infected with Leishmania braziliensis. Hum Immunol 2013, 74:1491.
33. Yokokawa J., Cereda V., Remondo C., Gulley J.L., Arlen P.M., Schlom J., et al. Enhanced functionality of CD4+CD25(high)FoxP3+ regulatory T cells in the peripheral blood of patients with prostate cancer. Clin Cancer Res 2008, 14:1032.
34. Rech A.J., Mick R., Kaplan D.E., Chang K.M., Domchek S.M., Vonderheide R.H. Homeostasis of peripheral FoxP3(+) CD4 (+) regulatory T cells in patients with early and late stage breast cancer. Cancer Immunol Immunother 2010, 59:599.
35. Heinzel F.P., Sadick M.D., Holaday B.J., Coffman R.L., Locksley R.M. Reciprocal expression of interferon gamma or interleukin 4 during the resolution or progression of murine leishmaniasis. Evidence for expansion of distinct helper T cell subsets. J Exp Med 1989, 169:59.
36. Mosmann T.R., Cherwinski H., Bond M.W., Giedlin M.A., Coffman R.L. Two types of murine helper T cell clone. I. Definition according to profiles of lymphokine activities and secreted proteins. J Immunol 1986, 136:2348.
37. Tripathi P., Singh V., Naik S. Immune response to Leishmania: paradox rather than paradigm. FEMS Immunol Med Microbiol 2007, 51:229.
38. Reinhard K., Huber M., Wostl C., Hellhund A., Toboldt A., Abass E., et al. C-Rel promotes type 1 and type 17 immune responses during Leishmania major infection. Eur J Immunol 2011, 41:1388.
39. Nylen S., Gautam S. Immunological perspectives of leishmaniasis. J Glob Infect Dis 2010, 2:135.
40. Kemp M., Hey A.S., Kurtzhals J.A., Christensen C.B., Gaafar A., Mustafa M.D., et al. Dichotomy of the human T cell response to Leishmania antigens. I. Th1-like response to Leishmania major promastigote antigens in individuals recovered from cutaneous leishmaniasis. Clin Exp Immunol 1994, 96:410.
41. Akuffo H.O., Britton S.F. Contribution of non-Leishmania-specific immunity to resistance to Leishmania infection in humans. Clin Exp Immunol 1992, 87:58.
42. Kemp M., Hansen M.B., Theander T.G. Recognition of Leishmania antigens by T lymphocytes from nonexposed individuals. Infect Immun 1992, 60:2246.
43. Belkaid Y., Piccirillo C.A., Mendez S., Shevach E.M., Sacks D.L. CD4+CD25+ regulatory T cells control Leishmania major persistence and immunity. Nature 2002, 420:502.
44. Suffia I.J., Reckling S.K., Piccirillo C.A., Goldszmid R.S., Belkaid Y. Infected site-restricted Foxp3+ natural regulatory T cells are specific for microbial antigens. J Exp Med 2006, 203:777.
45. Brincks E.L., Roberts A.D., Cookenham T., Sell S., Kohlmeier J.E., Blackman M.A., et al. Antigen-specific memory regulatory CD4+Foxp3+ T cells control memory responses to influenza virus infection. J Immunol 2013, 190:3438.
46. Sanchez A.M., Zhu J., Huang X., Yang Y. The development and function of memory regulatory T cells after acute viral infections. J Immunol 2012, 189:2805.
47. Ayyoub M., Deknuydt F., Raimbaud I., Dousset C., Leveque L., Bioley G., et al. Human memory FOXP3+ Tregs secrete IL-17 ex vivo and constitutively express the T(H)17 lineage-specific transcription factor RORgamma t. Proc Natl Acad Sci U S A 2009, 106:8635.
48. Haas J., Hug A., Viehover A., Fritzsching B., Falk C.S., Filser A., et al. Reduced suppressive effect of CD4+CD25 high regulatory T cells on the T cell immune response against myelin oligodendrocyte glycoprotein in patients with multiple sclerosis. Eur J Immunol 2005, 35:3343.
49. Pronio A., Montesani C., Butteroni C., Vecchione S., Mumolo G., Vestri A., et al. Probiotic administration in patients with ileal pouch-anal anastomosis for ulcerative colitis is associated with expansion of mucosal regulatory cells. Inflamm Bowel Dis 2008, 14:662.