Bacterial toxins fuel disease progression in cutaneous T-cell lymphoma

Andreas Willerslev-Olsen, Thorbjørn Krejsgaard, Lise M Lindahl, Charlotte Menne Bonefeld, Mariusz A Wasik, Sergei B Koralov, Carsten Geisler, Mogens Kilian, Lars Iversen, Anders Woetmann, Niels Odum, Andreas Willerslev-Olsen, Thorbjørn Krejsgaard, Lise M Lindahl, Charlotte Menne Bonefeld, Mariusz A Wasik, Sergei B Koralov, Carsten Geisler, Mogens Kilian, Lars Iversen, Anders Woetmann, Niels Odum

Abstract

In patients with cutaneous T-cell lymphoma (CTCL) bacterial infections constitute a major clinical problem caused by compromised skin barrier and a progressive immunodeficiency. Indeed, the majority of patients with advanced disease die from infections with bacteria, e.g., Staphylococcus aureus. Bacterial toxins such as staphylococcal enterotoxins (SE) have long been suspected to be involved in the pathogenesis in CTCL. Here, we review links between bacterial infections and CTCL with focus on earlier studies addressing a direct role of SE on malignant T cells and recent data indicating novel indirect mechanisms involving SE- and cytokine-driven cross-talk between malignant- and non-malignant T cells.

Figures

Figure 1
Figure 1
Schematic illustration of the antigen presenting cells (APC) antigen presentation and cytokine release together with the subsequent induction of different lymphocyte helper subsets. (1) The APC delivers three signals required for successful lymphocyte activation; antigen presentation, co-stimulation and cytokine release with cytokines being the major determinant of lymphocyte subset induction; (2) Additionally dendritic cells DC are able to induce a regulatory phenotype either by the absence of co-stimulation (immature DC’s lack CD80/86) or by activation of lymphocytes in a regulatory cytokine environment (tolerogenic DC’s).
Figure 2
Figure 2
Schematic illustration of the transition from a state of tumor equilibrium to a state of tumor immune privilege. The tumor equilibrium state (1) is characterized by T cell- and cytokine-mediated control of tumor progression. Conversely, the state of tumor immune privilege (2) is predominated by regulatory signals and cytokines allowing for immune evasion and tumor progression and metastasis. (Yellow: DC; blue: nonmalignant T cell; red: malignant T cell).
Figure 3
Figure 3
Schematic illustration of SE-mediated cross-talk between malignant and non-malignant T cells. Malignant T cells often display deficient expression and function of the TCR/CD3 complex and may not respond directly to bacterial superantigens such as staphylococcal enterotoxins (SE). Instead, malignant T cells often express MHC class II molecules, which are high-affinity receptors for SE (1). Non-malignant T cells with the appropriate Vb TCR respond to SE presented by malignant T cells (2, 3) or by antigen presenting cells (APC) (not shown). SE-mediated cross-talk between malignant and non-malignant T cells triggers cell-to-cell contact and production of growth factors, which in turn promote proliferation of malignant T cells (3) [104].

References

    1. Girardi M., Heald P.W., Wilson L.D. The pathogenesis of mycosis fungoides. N. Engl. J. Med. 2004;350:1978–1988. doi: 10.1056/NEJMra032810.
    1. Hwang S.T., Janik J.E., Jaffe E.S., Wilson W.H. Mycosis fungoides and sezary syndrome. Lancet. 2008;371:945–957. doi: 10.1016/S0140-6736(08)60420-1.
    1. Weinstock M.A., Gardstein B. Twenty-year trends in the reported incidence of mycosis fungoides and associated mortality. Am. J. Public Health. 1999;89:1240–1244. doi: 10.2105/AJPH.89.8.1240.
    1. Willemze R., Jaffe E.S., Burg G., Cerroni L., Berti E., Swerdlow S.H., Ralfkiaer E., Chimenti S., Diaz-Perez J.L., Duncan L.M., et al. Who-eortc classification for cutaneous lymphomas. Blood. 2005;105:3768–3785. doi: 10.1182/blood-2004-09-3502.
    1. Willemze R., Meijer C.J. Classification of cutaneous t-cell lymphoma: From alibert to who-eortc. J. Cutan. Pathol. 2006;33:18–26. doi: 10.1111/j.0303-6987.2006.00494.x.
    1. Wong H.K., Mishra A., Hake T., Porcu P. Evolving insights in the pathogenesis and therapy of cutaneous t-cell lymphoma (mycosis fungoides and sezary syndrome) Br. J. Haematol. 2011;155:150–166. doi: 10.1111/j.1365-2141.2011.08852.x.
    1. Ralfkiaer U., Hagedorn P.H., Bangsgaard N., Lovendorf M.B., Ahler C.B., Svensson L., Kopp K.L., Vennegaard M.T., Lauenborg B., Zibert J.R., et al. Diagnostic microrna profiling in cutaneous t-cell lymphoma (ctcl) Blood. 2011;118:5891–5900. doi: 10.1182/blood-2011-06-358382.
    1. Marstrand T., Ahler C.B., Ralfkiaer U., Clemmensen A., Kopp K.L., Sibbesen N.A., Krejsgaard T., Litman T., Wasik M.A., Bonefeld C.M., et al. Validation of a diagnostic mirna classifier in cutaneous t-cell lymphomas. Leuk. Lymphoma. 2013 doi: 10.3109/10428194.2013.815352.
    1. Krejsgaard T., Odum N., Geisler C., Wasik M.A., Woetmann A. Regulatory t cells and immunodeficiency in mycosis fungoides and sezary syndrome. Leukemia. 2012;26:424–432. doi: 10.1038/leu.2011.237.
    1. Kim E.J., Hess S., Richardson S.K., Newton S., Showe L.C., Benoit B.M., Ubriani R., Vittorio C.C., Junkins-Hopkins J.M., Wysocka M., et al. Immunopathogenesis and therapy of cutaneous t cell lymphoma. J. Clin. Investig. 2005;115:798–812.
    1. Izban K.F., Ergin M., Qin J.Z., Martinez R.L., Pooley R.J., Saeed S., Alkan S. Constitutive expression of nf-kappa b is a characteristic feature of mycosis fungoides: Implications for apoptosis resistance and pathogenesis. Hum. Pathol. 2000;31:1482–1490. doi: 10.1053/hupa.2000.20370.
    1. Mao X., Orchard G., Mitchell T.J., Oyama N., Russell-Jones R., Vermeer M.H., Willemze R., van Doorn R., Tensen C.P., Young B.D., et al. A genomic and expression study of ap-1 in primary cutaneous t-cell lymphoma: Evidence for dysregulated expression of junb and jund in mf and ss. J. Cutan. Pathol. 2008;35:899–910.
    1. Van Kester M.S., Borg M.K., Zoutman W.H., Out-Luiting J.J., Jansen P.M., Dreef E.J., Vermeer M.H., van Doorn R., Willemze R., Tensen C.P. A meta-analysis of gene expression data identifies a molecular signature characteristic for tumor-stage mycosis fungoides. J. Investig. Dermatol. 2012;132:2050–2059. doi: 10.1038/jid.2012.117.
    1. Tuyp E., Burgoyne A., Aitchison T., MacKie R. A case-control study of possible causative factors in mycosis fungoides. Arch. Dermatol. 1987;123:196–200. doi: 10.1001/archderm.1987.01660260066015.
    1. Lynge E., Afonso N., Kaerlev L., Olsen J., Sabroe S., Ahrens W., Eriksson M., Guenel P., Merletti F., Stengrevics A., et al. European multi-centre case-control study on risk factors for rare cancers of unknown aetiology. Eur. J. Cancer. 2005;41:601–612. doi: 10.1016/j.ejca.2004.12.016.
    1. Morales-Suarez-Varela M.M., Olsen J., Johansen P., Kaerlev L., Guenel P., Arveux P., Wingren G., Hardell L., Ahrens W., Stang A., et al. Occupational risk factors for mycosis fungoides: A European multicenter case-control study. J. Occup. Environ. Med. 2004;46:205–211. doi: 10.1097/01.jom.0000116819.01813.8c.
    1. Jahan-Tigh R.R., Huen A.O., Lee G.L., Pozadzides J.V., Liu P., Duvic M. Hydrochlorothiazide and cutaneous t cell lymphoma: Prospective analysis and case series. Cancer. 2013;119:825–831. doi: 10.1002/cncr.27740.
    1. Hodak E., Klein T., Gabay B., Ben-Amitai D., Bergman R., Gdalevich M., Feinmesser M., Maron L., David M. Familial mycosis fungoides: Report of 6 kindreds and a study of the hla system. J. Am. Acad. Dermatol. 2005;52:393–402. doi: 10.1016/j.jaad.2003.12.052.
    1. Jackow C.M., McHam J.B., Friss A., Alvear J., Reveille J.R., Duvic M. Hla-dr5 and dqb1*03 class ii alleles are associated with cutaneous t-cell lymphoma. J. Investig. Dermatol. 1996;107:373–376.
    1. Bonin S., Tothova S.M., Barbazza R., Brunetti D., Stanta G., Trevisan G. Evidence of multiple infectious agents in mycosis fungoides lesions. Exp. Mol. Pathol. 2010;89:46–50. doi: 10.1016/j.yexmp.2010.05.001.
    1. Axelrod P.I., Lorber B., Vonderheid E.C. Infections complicating mycosis fungoides and sezary syndrome. JAMA. 1992;267:1354–1358. doi: 10.1001/jama.1992.03480100060031.
    1. Mirvish E.D., Pomerantz R.G., Geskin L.J. Infectious agents in cutaneous t-cell lymphoma. J. Am. Acad. Dermatol. 2011;64:423–431. doi: 10.1016/j.jaad.2009.11.692.
    1. Posner L.E., Fossieck B.E., Jr., Eddy J.L., Bunn P.A., Jr. Septicemic complications of the cutaneous t-cell lymphomas. Am. J. Med. 1981;71:210–216. doi: 10.1016/0002-9343(81)90107-8.
    1. Li J.Y., Horwitz S., Moskowitz A., Myskowski P.L., Pulitzer M., Querfeld C. Management of cutaneous t cell lymphoma: New and emerging targets and treatment options. Cancer Manag. Res. 2012;4:75–89.
    1. Vermeer M.H., van Doorn R., Dukers D., Bekkenk M.W., Meijer C.J., Willemze R. Cd8+ t cells in cutaneous t-cell lymphoma: Expression of cytotoxic proteins, fas ligand, and killing inhibitory receptors and their relationship with clinical behavior. J. Clin. Oncol. Off. J. Am. Soc. Clin. Oncol. 2001;19:4322–4329.
    1. Rook A.H., Kuzel T.M., Olsen E.A. Cytokine therapy of cutaneous t-cell lymphoma: Interferons, interleukin-12, and interleukin-2. Hematol. Oncol. Clin. North Am. 2003;17:1435–1448. doi: 10.1016/S0889-8588(03)00109-6.
    1. Munir S., Andersen G.H., Woetmann A., Odum N., Becker J.C., Andersen M.H. Cutaneous T cell lymphoma cells are targets for immune checkpoint ligand pd-l1-specific, cytotoxic T cells. Leukemia. 2013 doi: 10.1038/leu.2013.118.
    1. Larsen S., Munir S., Woetmann A., Frøsig T., Odum N., Svane I., Becker J.C., Andersen M.H. Functional characterization of Foxp3-specific spontaneous immune responses. Leukemi. 2013 doi: 10.1038/leu.2013.1.
    1. Zackheim H.S., Koo J., LeBoit P.E., McCalmont T.H., Bowman P.H., Kashani-Sabet M., Jones C., Zehnder J. Psoriasiform mycosis fungoides with fatal outcome after treatment with cyclosporine. J. Am. Acad. Dermatol. 2002;47:155–157. doi: 10.1067/mjd.2002.120571.
    1. Pielop J.A., Jones D., Duvic M. Transient cd30+ nodal transformation of cutaneous t-cell lymphoma associated with cyclosporine treatment. Int. J. Dermatol. 2001;40:505–511. doi: 10.1046/j.1365-4362.2001.01256.x.
    1. Leroy S., Dubois S., Tenaud I., Chebassier N., Godard A., Jacques Y., Dreno B. Interleukin-15 expression in cutaneous t-cell lymphoma (mycosis fungoides and sezary syndrome) Br. J. Dermatol. 2001;144:1016–1023. doi: 10.1046/j.1365-2133.2001.04192.x.
    1. Guenova E., Watanabe R., Teague J.E., Desimone J.A., Jiang Y., Dowlatshahi M., Schlapbach C., Schaekel K., Rook A.H., Tawa M., et al. Th2 cytokines from malignant cells suppress th1 responses and enforce a global th2 bias in leukemic cutaneous t-cell lymphoma. Clin. Cancer Res. 2013 doi: 10.1158/1078-0432.CCR-12-3488.
    1. Krejsgaard T., Vetter-Kauczok C.S., Woetmann A., Lovato P., Labuda T., Eriksen K.W., Zhang Q., Becker J.C., Odum N. Jak3- and jnk-dependent vascular endothelial growth factor expression in cutaneous t-cell lymphoma. Leukemia. 2006;20:1759–1766. doi: 10.1038/sj.leu.2404350.
    1. Pedersen I.H., Willerslev-Olsen A., Vetter-Kauczok C., Krejsgaard T., Lauenborg B., Kopp K.L., Geisler C., Bonefeld C.M., Zhang Q., Wasik M.A., et al. Vascular endothelial growth factor receptor-3 expression in mycosis fungoides. Leuk. Lymphoma. 2013;54:819–826. doi: 10.3109/10428194.2012.726720.
    1. Nielsen M., Nissen M.H., Gerwien J., Zocca M.B., Rasmussen H.M., Nakajima K., Ropke C., Geisler C., Kaltoft K., Odum N. Spontaneous interleukin-5 production in cutaneous t-cell lymphoma lines is mediated by constitutively activated stat3. Blood. 2002;99:973–977. doi: 10.1182/blood.V99.3.973.
    1. Sommer V.H., Clemmensen O.J., Nielsen O., Wasik M., Lovato P., Brender C., Eriksen K.W., Woetmann A., Kaestel C.G., Nissen M.H., et al. In vivo activation of stat3 in cutaneous t-cell lymphoma. Evidence for an antiapoptotic function of stat3. Leukemia. 2004;18:1288–1295. doi: 10.1038/sj.leu.2403385.
    1. Kopp K.L., Ralfkiaer U., Gjerdrum L.M., Helvad R., Pedersen I.H., Litman T., Jonson L., Hagedorn P.H., Krejsgaard T., Gniadecki R., et al. Stat5-mediated expression of oncogenic mir-155 in cutaneous t-cell lymphoma. Cell Cycle. 2013;12:1939–1937. doi: 10.4161/cc.24987.
    1. Krejsgaard T., Vetter-Kauczok C.S., Woetmann A., Kneitz H., Eriksen K.W., Lovato P., Zhang Q., Wasik M.A., Geisler C., Ralfkiaer E., et al. Ectopic expression of b-lymphoid kinase in cutaneous t-cell lymphoma. Blood. 2009;113:5896–5904. doi: 10.1182/blood-2008-09-181024.
    1. Kopp K.L., Kauczok C.S., Lauenborg B., Krejsgaard T., Eriksen K.W., Zhang Q., Wasik M.A., Geisler C., Ralfkiaer E., Becker J.C., et al. Cox-2-dependent pge(2) acts as a growth factor in mycosis fungoides (mf) Leukemia. 2010;24:1179–1185. doi: 10.1038/leu.2010.66.
    1. Brender C., Nielsen M., Kaltoft K., Mikkelsen G., Zhang Q., Wasik M., Billestrup N., Odum N. Stat3-mediated constitutive expression of socs-3 in cutaneous t-cell lymphoma. Blood. 2001;97:1056–1062. doi: 10.1182/blood.V97.4.1056.
    1. Brender C., Lovato P., Sommer V.H., Woetmann A., Mathiesen A.M., Geisler C., Wasik M., Odum N. Constitutive socs-3 expression protects t-cell lymphoma against growth inhibition by ifnalpha. Leukemia. 2005;19:209–213. doi: 10.1038/sj.leu.2403610.
    1. Gjerdrum L.M., Woetmann A., Odum N., Burton C.M., Rossen K., Skovgaard G.L., Ryder L.P., Ralfkiaer E. Foxp3+ regulatory t cells in cutaneous t-cell lymphomas: Association with disease stage and survival. Leukemia. 2007;21:2512–2518. doi: 10.1038/sj.leu.2404913.
    1. Hallermann C., Niermann C., Schulze H.J. Regulatory t-cell phenotype in association with large cell transformation of mycosis fungoides. Eur. J. Haematol. 2007;78:260–263. doi: 10.1111/j.1600-0609.2006.00809.x.
    1. Kasprzycka M., Zhang Q., Witkiewicz A., Marzec M., Potoczek M., Liu X., Wang H.Y., Milone M., Basu S., Mauger J., et al. Gamma c-signaling cytokines induce a regulatory t cell phenotype in malignant cd4+ t lymphocytes. J. Immunol. 2008;181:2506–2512.
    1. Krejsgaard T., Gjerdrum L.M., Ralfkiaer E., Lauenborg B., Eriksen K.W., Mathiesen A.M., Bovin L.F., Gniadecki R., Geisler C., Ryder L.P., et al. Malignant tregs express low molecular splice forms of foxp3 in sezary syndrome. Leukemia. 2008;22:2230–2239. doi: 10.1038/leu.2008.224.
    1. Wong H.K., Wilson A.J., Gibson H.M., Hafner M.S., Hedgcock C.J., Berger C.L., Edelson R.L., Lim H.W. Increased expression of ctla-4 in malignant t-cells from patients with mycosis fungoides—Cutaneous t cell lymphoma. J. Investig. Dermatol. 2006;126:212–219. doi: 10.1038/sj.jid.5700029.
    1. Samimi S., Benoit B., Evans K., Wherry E.J., Showe L., Wysocka M., Rook A.H. Increased programmed death-1 expression on cd4+ t cells in cutaneous t-cell lymphoma: Implications for immune suppression. Arch. Dermatol. 2010;146:1382–1388. doi: 10.1001/archdermatol.2010.200.
    1. Kantekure K., Yang Y., Raghunath P., Schaffer A., Woetmann A., Zhang Q., Odum N., Wasik M. Expression patterns of the immunosuppressive proteins pd-1/cd279 and pd-l1/cd274 at different stages of cutaneous t-cell lymphoma/mycosis fungoides. Am. J. Dermatopathol. 2012;34:126–128. doi: 10.1097/DAD.0b013e31821c35cb.
    1. Abraham R.M., Zhang Q., Odum N., Wasik M.A. The role of cytokine signaling in the pathogenesis of cutaneous t-cell lymphoma. Cancer Biol. Therapy. 2011;12:1019–1022. doi: 10.4161/cbt.12.12.18144.
    1. Berger C.L., Tigelaar R., Cohen J., Mariwalla K., Trinh J., Wang N., Edelson R.L. Cutaneous t-cell lymphoma: Malignant proliferation of t-regulatory cells. Blood. 2005;105:1640–1647. doi: 10.1182/blood-2004-06-2181.
    1. Berger C.L., Hanlon D., Kanada D., Dhodapkar M., Lombillo V., Wang N., Christensen I., Howe G., Crouch J., El-Fishawy P., et al. The growth of cutaneous t-cell lymphoma is stimulated by immature dendritic cells. Blood. 2002;99:2929–2939.
    1. Hofmann B., Odum N., Platz P., Ryder L.P., Svejgaard A., Neilsen J.O. Immunological studies in acquired immunodeficiency syndrome. Functional studies of lymphocyte subpopulations. Scand. J. Immunol. 1985;21:235–243. doi: 10.1111/j.1365-3083.1985.tb01426.x.
    1. Gardner J.M., Evans K.G., Musiek A., Rook A.H., Kim E.J. Update on treatment of cutaneous t-cell lymphoma. Curr. Opin. Oncol. 2009;21:131–137. doi: 10.1097/CCO.0b013e3283253190.
    1. Ciree A., Michel L., Camilleri-Broet S., Jean Louis F., Oster M., Flageul B., Senet P., Fossiez F., Fridman W.H., Bachelez H., et al. Expression and activity of il-17 in cutaneous t-cell lymphomas (mycosis fungoides and sezary syndrome) Int. J. Cancer. 2004;112:113–120. doi: 10.1002/ijc.20373.
    1. Krejsgaard T., Litvinov I.V., Wang Y., Xia L., Willerslev-Olsen A., Koralov S.B., Kopp K.L., Bonefeld C.M., Wasik M.A., Geisler C., et al. Elucidating the role of interleukin-17f in cutaneous t-cell lymphoma. Blood. 2013 doi: 10.1182/blood-2013-01-480889.
    1. Krejsgaard T., Ralfkiaer U., Clasen-Linde E., Eriksen K.W., Kopp K.L., Bonefeld C.M., Geisler C., Dabelsteen S., Wasik M.A., Ralfkiaer E., et al. Malignant cutaneous t-cell lymphoma cells express il-17 utilizing the jak3/stat3 signaling pathway. J. Investig. Dermatol. 2011;131:1331–1338. doi: 10.1038/jid.2011.27.
    1. MacKie R.M. Initial event in mycosis fungoides of the skin is viral infection of epidermal langerhans cells. Lancet. 1981;2:283–285. doi: 10.1016/S0140-6736(81)90529-8.
    1. van der Loo E.M., van Muijen G.N., van Vloten W.A., Beens W., Scheffer E., Meijer C.J. C-type virus-like particles specifically localized in langerhans cells and related cells of skin and lymph nodes of patients with mycosis fungoides and sezary’s syndrome. A morphological and biochemical study. Virchows Arch. B Cell Pathol. Incl. Mol. Pathol. 1979;31:193–203. doi: 10.1007/BF02889936.
    1. Potoczna N., Boehncke W.H., Nestle F.O., Kuenzlen C., Sterry W., Burg G., Dummer R. T-cell receptor beta variable region (v beta) usage in cutaneous t-cell lymphomas (ctcl) in comparison to normal and eczematous skin. J. Cutan. Pathol. 1996;23:298–305. doi: 10.1111/j.1600-0560.1996.tb01301.x.
    1. Yawalkar N., Ferenczi K., Jones D.A., Yamanaka K., Suh K.Y., Sadat S., Kupper T.S. Profound loss of t-cell receptor repertoire complexity in cutaneous t-cell lymphoma. Blood. 2003;102:4059–4066. doi: 10.1182/blood-2003-04-1044.
    1. Cornberg M., Chen A.T., Wilkinson L.A., Brehm M.A., Kim S.K., Calcagno C., Ghersi D., Puzone R., Celada F., Welsh R.M., et al. Narrowed tcr repertoire and viral escape as a consequence of heterologous immunity. J. Clin. Investig. 2006;116:1443–1456. doi: 10.1172/JCI27804.
    1. Poiesz B.J., Ruscetti F.W., Gazdar A.F., Bunn P.A., Minna J.D., Gallo R.C. Detection and isolation of type c retrovirus particles from fresh and cultured lymphocytes of a patient with cutaneous t-cell lymphoma. Proc. Natl. Acad. Sci. USA. 1980;77:7415–7419. doi: 10.1073/pnas.77.12.7415.
    1. Yoshida M., Miyoshi I., Hinuma Y. Isolation and characterization of retrovirus from cell lines of human adult t-cell leukemia and its implication in the disease. Proc. Natl. Acad. Sci. USA. 1982;79:2031–2035. doi: 10.1073/pnas.79.6.2031.
    1. Barre-Sinoussi F., Chermann J.C., Rey F., Nugeyre M.T., Chamaret S., Gruest J., Dauguet C., Axler-Blin C., Vezinet-Brun F., Rouzioux C., et al. Isolation of a t-lymphotropic retrovirus from a patient at risk for acquired immune deficiency syndrome (aids) Science. 1983;220:868–871.
    1. Zucker-Franklin D., Pancake B.A. The role of human t-cell lymphotropic viruses (htlv-i and ii) in cutaneous t-cell lymphomas. Semin. Dermatol. 1994;13:160–165.
    1. Pancake B.A., Zucker-Franklin D., Coutavas E.E. The cutaneous T cell lymphoma, mycosis fungoides, is a human T cell lymphotropic virus-associated disease. A study of 50 patients. J. Clin. Investig. 1995;95:547–554. doi: 10.1172/JCI117697.
    1. Lessin S.R., Rook A.H., Li G., Wood G.S. Htlv-i and ctcl: The link is missing. J. Investig. Dermatol. 1996;107:783–784.
    1. Wood G.S., Salvekar A., Schaffer J., Crooks C.F., Henghold W., Fivenson D.P., Kim Y.H., Smoller B.R. Evidence against a role for human t-cell lymphotrophic virus type i (htlv-i) in the pathogenesis of American cutaneous t-cell lymphoma. J. Investig. Dermatol. 1996;107:301–307.
    1. Bazarbachi A., Soriano V., Pawson R., Vallejo A., Moudgil T., Matutes E., Peries J., Molina A., de The H., Schulz T.F., et al. Mycosis fungoides and sezary syndrome are not associated with htlv-i infection: An international study. Br. J. Haematol. 1997;98:927–933. doi: 10.1046/j.1365-2141.1997.3213138.x.
    1. Erkek E., Sahin S., Atakan N., Kocagoz T., Olut A., Gokoz A. Examination of mycosis fungoides for the presence of epstein-barr virus and human herpesvirus-6 by polymerase chain reaction. J. Eur. Acad. Dermatol. Venereol. 2001;15:422–426. doi: 10.1046/j.1468-3083.2001.00309.x.
    1. Kreuter A., Bischoff S., Skrygan M., Wieland U., Brockmeyer N.H., Stucker M., Altmeyer P., Gambichler T. High association of human herpesvirus 8 in large-plaque parapsoriasis and mycosis fungoides. Arch. Dermatol. 2008;144:1011–1016. doi: 10.1001/archderm.144.8.1011.
    1. Gupta R.K., Ramble J., Tong C.Y., Whittaker S., MacMahon E. Cytomegalovirus seroprevalence is not higher in patients with mycosis fungoides/sezary syndrome. Blood. 2006;107:1241–1242.
    1. Herne K.L., Talpur R., Breuer-McHam J., Champlin R., Duvic M. Cytomegalovirus seropositivity is significantly associated with mycosis fungoides and sezary syndrome. Blood. 2003;101:2132–2136. doi: 10.1182/blood-2002-07-2247.
    1. Nagore E., Ledesma E., Collado C., Oliver V., Perez-Perez A., Aliaga A. Detection of epstein-barr virus and human herpesvirus 7 and 8 genomes in primary cutaneous t- and b-cell lymphomas. Br. J. Dermatol. 2000;143:320–323. doi: 10.1046/j.1365-2133.2000.03657.x.
    1. Abrams J.T., Vonderheid E.C., Kolbe S., Appelt D.M., Arking E.J., Balin B.J. Sezary t-cell activating factor is a chlamydia pneumoniae-associated protein. Clin. Diagn. Lab. Immunol. 1999;6:895–905.
    1. Abrams J.T., Balin B.J., Vonderheid E.C. Association between sezary T cell-activating factor, chlamydia pneumoniae, and cutaneous T cell lymphoma. Ann. N.Y. Acad. Sci. 2001;941:69–85.
    1. Tothova S.M., Bonin S., Trevisan G., Stanta G. Mycosis fungoides: Is it a borrelia burgdorferi-associated disease? Br. J. Cancer. 2006;94:879–883. doi: 10.1038/sj.bjc.6602997.
    1. Rossler M.J., Rappl G., Muche M., Hasselmann D.O., Sterry W., Tilgen W., Reinhold U. No evidence of skin infection with chlamydia pneumoniae in patients with cutaneous T cell lymphoma. Clin. Microbiol. Infect. Off. Public. Eur. Soc. Clin. Microbiol. Infect. Dis. 2003;9:721–723.
    1. Ponzoni M., Ferreri A.J., Mappa S., Pasini E., Govi S., Facchetti F., Fanoni D., Tucci A., Vino A., Doglioni C., et al. Prevalence of borrelia burgdorferi infection in a series of 98 primary cutaneous lymphomas. Oncologist. 2011;16:1582–1588. doi: 10.1634/theoncologist.2011-0108.
    1. Hotz C., Ingen-Housz-Oro S., tran van Nhieu J., Charlier C., Foulet F., Rahmouni A., Zegai B., Duong T.A., Wolkenstein P., Bagot M., et al. Pulmonary cryptococcoma in a patient with sezary syndrome treated with alemtuzumab. Eur. J. Dermatol. 2011;21:1018–1020.
    1. Poonawalla T., Diwan H., Duvic M. Mycosis fungoides with coccidioidomycosis. Clin. Lymphoma Myeloma. 2006;7:148–150. doi: 10.3816/CLM.2006.n.054.
    1. Duvic M., Feasel A.M., Schwartz C.A., Cather J.C. Enterococcal eschars in cutaneous t-cell lymphoma tumors: A distinct clinical entity. Clin. Lymphoma. 2000;1:141–145. doi: 10.3816/CLM.2000.n.012.
    1. Jackow C.M., Cather J.C., Hearne V., Asano A.T., Musser J.M., Duvic M. Association of erythrodermic cutaneous t-cell lymphoma, superantigen-positive staphylococcus aureus, and oligoclonal t-cell receptor v beta gene expansion. Blood. 1997;89:32–40.
    1. Baser S., Onn A., Lin E., Morice R.C., Duvic M. Pulmonary manifestations in patients with cutaneous t-cell lymphomas. Cancer. 2007;109:1550–1555. doi: 10.1002/cncr.22567.
    1. Ortega E., Abriouel H., Lucas R., Galvez A. Multiple roles of staphylococcus aureus enterotoxins: Pathogenicity, superantigenic activity, and correlation to antibiotic resistance. Toxins. 2010;2:2117–2131. doi: 10.3390/toxins2082117.
    1. Pinchuk I.V., Beswick E.J., Reyes V.E. Staphylococcal enterotoxins. Toxins. 2010;2:2177–2197. doi: 10.3390/toxins2082177.
    1. Tokura Y., Heald P.W., Yan S.L., Edelson R.L. Stimulation of cutaneous t-cell lymphoma cells with superantigenic staphylococcal toxins. J. Investig. Dermatol. 1992;98:33–37.
    1. Irwin M.J., Hudson K.R., Ames K.T., Fraser J.D., Gascoigne N.R. T-cell receptor beta-chain binding to enterotoxin superantigens. Immunol. Rev. 1993;131:61–78. doi: 10.1111/j.1600-065X.1993.tb01530.x.
    1. Linnemann T., Gellrich S., Lukowsky A., Mielke A., Audring H., Sterry W., Walden P. Polyclonal expansion of T cells with the tcr v beta type of the tumour cell in lesions of cutaneous t-cell lymphoma: Evidence for possible superantigen involvement. Br. J. Dermatol. 2004;150:1013–1017. doi: 10.1111/j.1365-2133.2004.05970.x.
    1. McCormack J.E., Callahan J.E., Kappler J., Marrack P.C. Profound deletion of mature T cells in vivo by chronic exposure to exogenous superantigen. J. Immunol. 1993;150:3785–3792.
    1. Vonderheid E.C., Boselli C.M., Conroy M., Casaus L., Espinoza L.C., Venkataramani P., Bigler R.D., Hou J.S. Evidence for restricted vbeta usage in the leukemic phase of cutaneous T cell lymphoma. J. Investig. Dermatol. 2005;124:651–661. doi: 10.1111/j.0022-202X.2004.23586.x.
    1. Van der Fits L., Sandberg Y., Darzentas N., Zoutman W.H., Tielemans D., Wolvers-Tettero I.L., Vermeer M.H., Langerak A.W. A restricted clonal t-cell receptor alphabeta repertoire in sezary syndrome is indicative of superantigenic stimulation. Br. J. Dermatol. 2011;165:78–84. doi: 10.1111/j.1365-2133.2011.10308.x.
    1. Ni X., Hazarika P., Zhang C., Talpur R., Duvic M. Fas ligand expression by neoplastic t lymphocytes mediates elimination of cd8+ cytotoxic t lymphocytes in mycosis fungoides: A potential mechanism of tumor immune escape? Clin. Cancer Res. 2001;7:2682–2692.
    1. Wu J., Nihal M., Siddiqui J., Vonderheid E.C., Wood G.S. Low fas/cd95 expression by ctcl correlates with reduced sensitivity to apoptosis that can be restored by fas upregulation. J. Investig. Dermatol. 2009;129:1165–1173. doi: 10.1038/jid.2008.309.
    1. Lauenborg B., Kopp K., Krejsgaard T., Eriksen K.W., Geisler C., Dabelsteen S., Gniadecki R., Zhang Q., Wasik M.A., Woetmann A., et al. Programmed cell death-10 enhances proliferation and protects malignant T cells from apoptosis. APMIS. 2010;118:719–728. doi: 10.1111/j.1600-0463.2010.02669.x.
    1. Nielsen M., Kaestel C.G., Eriksen K.W., Woetmann A., Stokkedal T., Kaltoft K., Geisler C., Ropke C., Odum N. Inhibition of constitutively activated stat3 correlates with altered bcl-2/bax expression and induction of apoptosis in mycosis fungoides tumor cells. Leukemia. 1999;13:735–738. doi: 10.1038/sj.leu.2401415.
    1. Thurber S.E., Zhang B., Kim Y.H., Schrijver I., Zehnder J., Kohler S. T-cell clonality analysis in biopsy specimens from two different skin sites shows high specificity in the diagnosis of patients with suggested mycosis fungoides. J. Am. Acad. Dermatol. 2007;57:782–790. doi: 10.1016/j.jaad.2007.06.004.
    1. Gorochov G., Bachelez H., Cayuela J.M., Legac E., Laroche L., Dubertret L., Sigaux F. Expression of v beta gene segments by sezary cells. J. Investig. Dermatol. 1995;105:56–61.
    1. Longley J., Tyrrell L., Lu S.Z., Farrell J., Ding T.G., Yan S., Sallee D., Heald P., Berger C., Tigelaar R., et al. Malignant and normal T cells show random use of t-cell receptor alpha chain variable regions in patients with cutaneous t-cell lymphoma. J. Investig. Dermatol. 1995;105:62–64. doi: 10.1038/jid.1995.13.
    1. Morgan S.M., Hodges E., Mitchell T.J., Harris S., Whittaker S.J., Smith J.L. Molecular analysis of t-cell receptor beta genes in cutaneous t-cell lymphoma reveals jbeta1 bias. J. Investig. Dermatol. 2006;126:1893–1899. doi: 10.1038/sj.jid.5700304.
    1. Klemke C.D., Brenner D., Weiss E.M., Schmidt M., Leverkus M., Gulow K., Krammer P.H. Lack of t-cell receptor-induced signaling is crucial for cd95 ligand up-regulation and protects cutaneous t-cell lymphoma cells from activation-induced cell death. Cancer Res. 2009;69:4175–4183. doi: 10.1158/0008-5472.CAN-08-4631.
    1. Edelman J., Meyerson H.J. Diminished cd3 expression is useful for detecting and enumerating sezary cells. Am. J. Clin. Pathol. 2000;114:467–477.
    1. Morice W.G., Katzmann J.A., Pittelkow M.R., El-Azhary R.A., Gibson L.E., Hanson C.A. A comparison of morphologic features, flow cytometry, tcr-vbeta analysis, and tcr-pcr in qualitative and quantitative assessment of peripheral blood involvement by sezary syndrome. Am. J. Clin. Pathol. 2006;125:364–374.
    1. Woetmann A., Lovato P., Eriksen K.W., Krejsgaard T., Labuda T., Zhang Q., Mathiesen A.M., Geisler C., Svejgaard A., Wasik M.A., et al. Nonmalignant T cells stimulate growth of t-cell lymphoma cells in the presence of bacterial toxins. Blood. 2007;109:3325–3332. doi: 10.1182/blood-2006-04-017863.
    1. Fraser J.D., Proft T. The bacterial superantigen and superantigen-like proteins. Immunol. Rev. 2008;225:226–243. doi: 10.1111/j.1600-065X.2008.00681.x.
    1. Odum N., Ledbetter J.A., Martin P., Geraghty D., Tsu T., Hansen J.A., Gladstone P. Homotypic aggregation of human cell lines by hla class ii-, class ia- and hla-g-specific monoclonal antibodies. Eur. J. Immunol. 1991;21:2121–2131. doi: 10.1002/eji.1830210921.
    1. Nielsen M., Odum N., Bendtzen K., Ryder L.P., Jakobsen B.K., Svejgaard A. Mhc class ii molecules regulate growth in human T cells. Exp. Clin. Immunogenet. 1994;11:23–32.
    1. Odum N., Kanner S.B., Ledbetter J.A., Svejgaard A. Mhc class ii molecules deliver costimulatory signals in human T cells through a functional linkage with il-2-receptors. J. Immunol. 1993;150:5289–5298.
    1. Odum N., Martin P.J., Schieven G.L., Hansen J.A., Ledbetter J.A. Signal transduction by hla class ii antigens expressed on activated T cells. Eur. J. Immunol. 1991;21:123–129. doi: 10.1002/eji.1830210119.
    1. Kanner S.B., Grosmaire L.S., Blake J., Schieven G.L., Masewicz S., Odum N., Ledbetter J.A. Zap-70 and p72syk are signaling response elements through mhc class ii molecules. Tissue Antigens. 1995;46:145–154. doi: 10.1111/j.1399-0039.1995.tb03113.x.
    1. Kanner S.B., Odum N., Grosmaire L., Masewicz S., Svejgaard A., Ledbetter J.A. Superantigen and hla-dr ligation induce phospholipase-c gamma 1 activation in class ii+ T cells. J. Immunol. 1992;149:3482–3488.
    1. Odum N., Martin P.J., Schieven G.L., Norris N.A., Grosmaire L.S., Hansen J.A., Ledbetter J.A. Signal transduction by hla-dr is mediated by tyrosine kinase(s) and regulated by cd45 in activated T cells. Hum. Immunol. 1991;32:85–94.
    1. Odum N., Martin P.J., Schieven G.L., Masewicz S., Hansen J.A., Ledbetter J.A. Hla-dr molecules enhance signal transduction through the cd3/ti complex in activated T cells. Tissue Antigens. 1991;38:72–77. doi: 10.1111/j.1399-0039.1991.tb01883.x.
    1. Daniel D., Meyer-Morse N., Bergsland E.K., Dehne K., Coussens L.M., Hanahan D. Immune enhancement of skin carcinogenesis by cd4+ T cells. J. Exp. Med. 2003;197:1017–1028. doi: 10.1084/jem.20021047.
    1. Talpur R., Bassett R., Duvic M. Prevalence and treatment of Staphylococcus aureus colonization in patients with mycosis fungoides and sezary syndrome. Br. J. Dermatol. 2008;159:105–112. doi: 10.1111/j.1365-2133.2008.08612.x.
    1. Tokura Y., Yagi H., Ohshima A., Kurokawa S., Wakita H., Yokote R., Shirahama S., Furukawa F., Takigawa M. Cutaneous colonization with Staphylococci influences the disease activity of sezary syndrome: A potential role for bacterial superantigens. Br. J. Dermatol. 1995;133:6–12.

Source: PubMed

Sponsors en medewerkers

Medische omstandigheden

Geneesmiddelinterventies

3
Abonneren