Host defense mechanisms in secondary syphilitic lesions: A role for IFN-γ-/IL-17-producing CD8+ T cells?

American Journal of Pathology

Volumn 177, Issue 5, 2010, Pages 2421-2432

  Stary, Georg ^a   Klein, Irene ^a   Brüggen, Marie Charlotte ^a   Kohlhofer, Sabine ^a   Brunner, Patrick M ^a   Spazierer, Daniel ^a   Müllauer, Leonhard ^b   Petzelbauer, Peter ^a   Stingl, Georg ^a  

^a Universitatsklinik fur Dermatologie   (Austria)

^b MEDICAL UNIVERSITY OF VIENNA   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 17;

ADULT; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; HISTOPATHOLOGY; HOST RESISTANCE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; IMMUNOREGULATION; INFLAMMATORY CELL; INFLAMMATORY INFILTRATE; LANGERHANS CELL; MACROPHAGE; MALE; NEUTROPHIL; NUCLEOTIDE SEQUENCE; PLASMA CELL; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SYPHILIS; T LYMPHOCYTE; TREPONEMA PALLIDUM;

EID: 78149304382     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2010.100277     Document Type: Article

References (46)

1. Rockwell DH, Yobs AR, Moore MB Jr: The Tuskegee Study of Untreated Syphilis; the 30th Year of Observation. Arch Intern Med 1964, 114:792-798
2. Baker-Zander SA, Fohn MJ, Lukehart SA: Development of cellular immunity to individual soluble antigens of Treponema pallidum during experimental syphilis. J Immunol 1988, 141:4363-4369
3. Arroll TW, Centurion-Lara A, Lukehart SA, Van Voorhis WC: T-Cell responses to Treponema pallidum subsp. pallidum antigens during the course of experimental syphilis infection. Infect Immun 1999, 67:4757-4763
4. Lukehart SA, Baker-Zander SA, Lloyd RM, Sell S: Characterization of lymphocyte responsiveness in early experimental syphilis. II. Nature of cellular infiltration and Treponema pallidum distribution in testicular lesions. J Immunol 1980, 124:461-467
5. Sell S, Baker-Zander S, Powell HC: Experimental syphilitic orchitis in rabbits: ultrastructural appearance of Treponema pallidum during phagocytosis and dissolution by macrophages in vivo. Lab Invest 1982, 46:355-364
6. van Voorhis WC, Barrett LK, Nasio JM, Plummer FA, Lukehart SA: Lesions of primary and secondary syphilis contain activated cytolytic T-cells. Infect Immun 1996, 64:1048-1050
7. Van Voorhis WC, Barrett LK, Koelle DM, Nasio JM, Plummer FA, Lukehart SA: Primary and secondary syphilis lesions contain mRNA for Th1 cytokines. J Infect Dis 1996, 173:491-495
8. Lukehart SA: Activation of macrophages by products of lymphocytes from normal and syphilitic rabbits. Infect Immun 1982, 37:64-69
9. Baker-Zander SA, Lukehart SA: Macrophage-mediated killing of opsonized Treponema pallidum. J Infect Dis 1992, 165:69-74
10. Lukehart SA, Miller JN: Demonstration of the in vitro phagocytosis of Treponema pallidum by rabbit peritoneal macrophages. J Immunol 1978, 121:2014-2024
11. McBroom RL, Styles AR, Chiu MJ, Clegg C, Cockerell CJ, Radolf JD: Secondary syphilis in persons infected with and not infected with HIV-1: a comparative immunohistologic study. Am J Dermatopathol 1999, 21:432-441
12. Salazar JC, Cruz AR, Pope CD, Valderrama L, Trujillo R, Saravia NG, Radolf JD: Treponema pallidum elicits innate and adaptive cellular immune responses in skin and blood during secondary syphilis: a flow-cytometric analysis. J Infect Dis 2007, 195:879-887
13. Sellati TJ, Waldrop SL, Salazar JC, Bergstresser PR, Picker LJ, Radolf JD: The cutaneous response in humans to Treponema pallidum lipoprotein analogues involves cellular elements of both innate and adaptive immunity. J Immunol 2001, 166:4131-4140
14. Brightbill HD, Libraty DH, Krutzik SR, Yang RB, Belisle JT, Bleharski JR, Maitland M, Norgard MV, Plevy SE, Smale ST, Brennan PJ, Bloom BR, Godowski PJ, Modlin RL: Host defense mechanisms triggered by microbial lipoproteins through toll-like receptors. Science 1999, 285:732-736
15. Stary G, Bangert C, Tauber M, Strohal R, Kopp T, Stingl G: Tumoricidal activity of TLR7/8-activated inflammatory dendritic cells. J Exp Med 2007, 204:1441-1451
16. Pavia CS, Folds JD, Baseman JB: Depression of lymphocyte response to concanavalin A in rabbits infected with Treponema pallidum (Nichols strain). Infect Immun 1976, 14:320-322
17. Hanff PA, Bishop NH, Miller JN, Lovett MA: Humoral immune response in experimental syphilis to polypeptides of Treponema pallidum. J Immunol 1983, 131:1973-1977
18. Pavia CS, Niederbuhl CJ: Acquired resistance and expression of a protective humoral immune response in guinea pigs infected with Treponema pallidum Nichols. Infect Immun 1985, 50:66-72
19. Leader BT, Godornes C, VanVoorhis WC, Lukehart SA: CD4+ lymphocytes and gamma interferon predominate in local immune responses in early experimental syphilis. Infect Immun 2007, 75: 3021-3026
20. Sell S, Gamboa D, Baker-Zander SA, Lukehart SA, Miller JN: Host response to Treponema pallidum in intradermally-infected rabbits: evidence for persistence of infection at local and distant sites. J Invest Dermatol 1980, 75:470-475
21. Engelkens HJ, ten Kate FJ, Judanarso J, Vuzevski VD, van Lier JB, Godschalk JC, van der Sluis JJ, Stolz E: The localisation of treponemes and characterisation of the inflammatory infiltrate in skin biopsies from patients with primary or secondary syphilis, or early infectious yaws. Genitourin Med 1993, 69:102-107
22. Tosca A, Lehou J, Hatjivasiliou M, Varelzidis A, Stratigos JD: Infiltrate of syphilitic lesions before and after treatment. Genitourin Med 1988, 64:289-293
23. Jepsen OB, Hougen KH, Birch-Andersen A: Electron microscopy of treponema pallidum Nichols. Acta Pathol Microbiol Scand 1968, 74:241-258
24. Louten J, Boniface K, de Waal Malefyt R: Development and function of TH17 cells in health and disease. J Allergy Clin Immunol 2009, 123:1004-1011
25. Ortega C, Fernandez AS, Carrillo JM, Romero P, Molina IJ, Moreno JC, Santamaria M: IL-17-producing CD8+ T lymphocytes from psoriasis skin plaques are cytotoxic effector cells that secrete Th17-related cytokines. J Leukoc Biol 2009, 86:435-443
26. He D, Wu L, Kim HK, Li H, Elmets CA, Xu H: IL-17 and IFN-gamma mediate the elicitation of contact hypersensitivity responses by different mechanisms and both are required for optimal responses. J Immunol 2009, 183:1463-1470
27. Kish DD, Li X, Fairchild RL: CD8 T-cells producing IL-17 and IFN-gamma initiate the innate immune response required for responses to antigen skin challenge. J Immunol 2009, 182:5949-5959
28. Hinrichs CS, Kaiser A, Paulos CM, Cassard L, Sanchez-Perez L, Heemskerk B, Wrzesinski C, Borman ZA, Muranski P, Restifo NP: Type 17 CD8+ T-cells display enhanced anti-tumor immunity. Blood 2009, 114:596-599
29. Zhao Y, Balato A, Fishelevich R, Chapoval A, Mann DL, Gaspari AA: Th17/Tc17 infiltration and associated cytokine gene expression in elicitation phase of allergic contact dermatitis. Br J Dermatol 2009, 161:1301-1306
30. Billerbeck E, Kang YH, Walker L, Lockstone H, Grafmueller S, Fleming V, Flint J, Willberg CB, Bengsch B, Seigel B, Ramamurthy N, Zitzmann N, Barnes EJ, Thevanayagam J, Bhagwanani A, Leslie A, Oo YH, Kollnberger S, Bowness P, Drognitz O, Adams DH, Blum HE, Thimme R, Klenerman P: Analysis of CD161 expression on human CD8+ T cells defines a distinct functional subset with tissue-homing properties. Proc Natl Acad Sci USA 2010, 107:3006-3011
31. He D, Wu L, Kim HK, Li H, Elmets CA, Xu H: CD8+ IL-17-producing T cells are important in effector functions for the elicitation of contact hypersensitivity responses. J Immunol 2006, 177:6852-6858
32. Schöfer H, Imhof M, Thoma-Greber E, Brockmeyer NH, Hartmann M, Gerken G, Pees HW, Rasokat H, Hartmann H, Sadri I, Emminger C, Stellbrink HJ, Baumgarten R, Plettenberg A: Active syphilis in HIV infection: a multicentre retrospective survey. The German AIDS Study Group (GASG) Genitourin Med 1996, 72:176-181
33. Don PC, Rubinstein R, Christie S: Malignant syphilis (lues maligna) and concurrent infection with HIV. Int J Dermatol 1995, 34:403-407
34. Gregory N, Sanchez M, Buchness MR: The spectrum of syphilis in patients with human immunodeficiency virus infection. J Am Acad Dermatol 1990, 22:1061-1067
35. Lee SM, Joo YD, Seo SK: Expression and function of TLR2 on CD4 versus CD8 T cells. Immune Netw 2009, 9:127-132
36. Farhi D, Benhaddou N, Grange P, Zizi N, Deleuze J, Morini JP, Gerhardt P, Krivine A, Avril MF, Dupin N: Clinical and serologic baseline and follow-up features of syphilis according to HIV status in the post-HAART era. Medicine (Baltimore) 2009, 88:331-340
37. Rolfs RT, Joesoef MR, Hendershot EF, Rompalo AM, Augenbraun MH, Chiu M, Bolan G, Johnson SC, French P, Steen E, Radolf JD, Larsen S: A randomized trial of enhanced therapy for early syphilis in patients with and without human immunodeficiency virus infection. The Syphilis and HIV Study Group N Engl J Med 1997, 337:307-314
38. Barber DL, Wherry EJ, Masopust D, Zhu B, Allison JP, Sharpe AH, Freeman GJ, Ahmed R: Restoring function in exhausted CD8 T cells during chronic viral infection. Nature 2006, 439:682-687
39. Kaufmann DE, Walker BD: PD-1 and CTLA-4 inhibitory cosignaling pathways in HIV infection and the potential for therapeutic intervention. J Immunol 2009, 182:5891-5897
40. Miossec P: IL-17 and Th17 cells in human inflammatory diseases. Microbes Infect 2009, 11:625-630
41. Nograles KE, Zaba LC, Guttman-Yassky E, Fuentes-Duculan J, Suarez-Farinas M, Cardinale I, Khatcherian A, Gonzalez J, Pierson KC, White TR, Pensabene C, Coats I, Novitskaya I, Lowes MA, Krueger JG: Th17 cytokines interleukin (IL)-17 and IL-22 modulate distinct inflammatory and keratinocyte-response pathways. Br J Dermatol 2008, 159:1092-1102
42. Kleinschek MA, Boniface K, Sadekova S, Grein J, Murphy EE, Turner SP, Raskin L, Desai B, Faubion WA, de Waal Malefyt R, Pierce RH, McClanahan T, Kastelein RA: Circulating and gut-resident human Th17 cells express CD161 and promote intestinal inflammation. J Exp Med 2009, 206:525-534
43. Jiao Y, Fu J, Xing S, Fu B, Zhang Z, Shi M, Wang X, Zhang J, Jin L, Kang F, Wu H, Wang FS: The decrease of regulatory T-cells correlates with excessive activation and apoptosis of CD8+ T-cells in HIV-1-infected typical progressors, but not in long-term non-progressors. Immunology 2009, 128:e366-e375
44. Tschachler E, Groh V, Popovic M, Mann DL, Konrad K, Safai B, Eron L, DiMarzo Veronese F, Wolff K, Stingl G: Epidermal Langerhans cells-a target for HTLV-III/LAV infection. J Invest Dermatol 1987, 88:233-237
45. Romani N, Ebner S, Tripp CH, Flacher V, Koch F, Stoitzner P: Epidermal Langerhans cells-changing views on their function in vivo. Immunol Lett 2006, 106:119-125
46. Liu J, Hamrouni A, Wolowiec D, Coiteux V, Kuliczkowski K, Hetuin D, Saudemont A, Quesnel B: Plasma cells from multiple myeloma patients express B7-H1 (PD-L1) and increase expression after stimulation with IFN-gamma and TLR ligands via a MyD88- TRAF6-, and MEK-dependent pathway Blood 2007, 110:296-304