Deficient cutaneous antibacterial competence in cutaneous T-cell lymphomas: Role of Th2-mediated biased Th17 function

Clinical Cancer Research

Volumn 20, Issue 21, 2014, Pages 5507-5516

  Wolk, Kerstin ^a   Mitsui, Hiroshi ^b   Witte, Katrin ^a   Gellrich, Sylke ^a,d   Gulati, Nicholas ^b   Humme, Daniel ^a   Witte, Ellen ^a   Gonsior, Melanie ^a   Beyer, Marc ^a   Kadin, Marshall E ^c   Volk, Hans Dieter ^a   Krueger, James G ^b   Sterry, Wolfram ^a   Sabat, Robert ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b ROCKEFELLER UNIVERSITY   (United States)

^c ROGER WILLIAMS MEDICAL CENTER   (United States)

^d MD   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BETA DEFENSIN; CALGRANULIN B; GAMMA INTERFERON; INTERLEUKIN 13; INTERLEUKIN 14; INTERLEUKIN 14 RECEPTOR ALPHA; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 22; INTERLEUKIN 26; INTERSTITIAL COLLAGENASE; MESSENGER RNA; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN; PSORIASIN; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT; INTERLEUKIN DERIVATIVE; MMP1 PROTEIN, HUMAN;

ARTICLE; ATOPIC DERMATITIS; BACTERIAL SKIN DISEASE; CELL PROLIFERATION; CELL REGENERATION; CONTROLLED STUDY; CUTANEOUS T CELL LYMPHOMA; CYTOKINE PRODUCTION; DISEASE PREDISPOSITION; DOWN REGULATION; HUMAN; HUMAN CELL; INFECTION RISK; KERATINOCYTE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PSORIASIS; T LYMPHOCYTE SUBPOPULATION; UPREGULATION; AGED; CELL CULTURE; EPIDERMIS; FEMALE; IMMUNOLOGY; MALE; MIDDLE AGED; SKIN TUMOR; TH17 CELL; TH2 CELL; VERY ELDERLY;

AGED; AGED, 80 AND OVER; ANTI-BACTERIAL AGENTS; CELLS, CULTURED; DERMATITIS, ATOPIC; EPIDERMIS; FEMALE; HUMANS; INTERLEUKINS; KERATINOCYTES; LYMPHOMA, T-CELL, CUTANEOUS; MALE; MATRIX METALLOPROTEINASE 1; MIDDLE AGED; PSORIASIS; SKIN NEOPLASMS; TH17 CELLS; TH2 CELLS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84909606453     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-14-0707     Document Type: Article

References (50)

1. Bradford PT, Devesa SS, Anderson WF, Toro JR. Cutaneous lymphoma incidence patterns in the United States: a population-based study of 3884 cases. Blood 2009;113:5064-73.
2. Girardi M, Heald PW, Wilson LD. The pathogenesis of mycosis fungoides. N Engl J Med 2004;350:1978-88.
3. Wong HK, 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;155:150-66.
4. Bieber T. Atopic dermatitis. N Engl J Med 2008;358:1483-94.
5. Schon MP, Boehncke WH. Psoriasis. N Engl J Med 2005;352:1899-912.
6. Beyer M, Mobs M, Humme D, Sterry W. Pathogenesis of Mycosis fungoides. J Dtsch Dermatol Ges 2011;9:594-8.
7. Burg G, Dummer R, Haeffner A, Kempf W, Kadin M. From inflammation to neoplasia: mycosis fungoides evolves from reactive inflammatory conditions (lymphoid infiltrates) transforming into neoplastic plaques and tumors. Arch Dermatol 2001;137:949-52.
8. 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;159:105-12.
9. Tokura Y, Yagi H, Ohshima A, Kurokawa S, Wakita H, Yokote R, et al. Cutaneous colonization with staphylococci influences the disease activity of Sezary syndrome: a potential role for bacterial superantigens. Br J Dermatol 1995;133:6-12.
10. Jackow CM, Cather JC, Hearne V, Asano AT, Musser JM, 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.
11. Willerslev-Olsen A, Krejsgaard T, Lindahl LM, BonefeldCM, Wasik MA, Koralov SB, et al. Bacterial toxins fuel disease progression in cutaneous T-cell lymphoma. Toxins (Basel) 2013;5:1402-21.
12. Posner LE, Fossieck BE Jr, Eddy JL, Bunn PA Jr. Septicemic complications of the cutaneous T-cell lymphomas.AmJ Med 1981;71:210-6.
13. Tsambiras PE, Patel S, Greene JN, Sandin RL, Vincent AL. Infectious complications of cutaneous t-cell lymphoma. Cancer Control 2001;8:185-8.
14. Grice K, Sattar H, Baker H, Sharratt M. The relationship of transepidermal water loss to skin temperature in psoriasis and eczema. J Invest Dermatol 1975;64:313-5.
15. Segre JA. Epidermal barrier formation and recovery in skin disorders. J Clin Invest 2006;116:1150-8.
16. Ong PY, Ohtake T, Brandt C, Strickland I, Boguniewicz M, Ganz T, et al. Endogenous antimicrobial peptides and skin infections in atopic dermatitis. N Engl J Med 2002;347:1151-60.
17. Harder J, Schroder JM. Psoriatic scales: a promising source for the isolation of human skin-derived antimicrobial proteins. J Leukoc Biol 2005;77:476-86.
18. Wolk K, Kunz S, Witte E, Friedrich M, Asadullah K, Sabat R. IL-22 increases the innate immunity of tissues. Immunity 2004;21:241-54.
19. Liang SC, Tan XY, Luxenberg DP, Karim R, Dunussi-Joannopoulos K, Collins M, et al. Interleukin (IL)-22 and IL-17 are coexpressed by Th17 cells and cooperatively enhance expression of antimicrobial peptides. J Exp Med 2006;203:2271-9.
20. Glaser R, Harder J, Lange H, Bartels J, Christophers E, Schroder JM. Antimicrobial psoriasin (S100A7) protects human skin from Escherichia coli infection. Nat Immunol 2005;6:57-64.
21. Garcia JR, Jaumann F, Schulz S, Krause A, Rodriguez-Jimenez J, Forssmann U, et al. Identification of a novel, multifunctional beta-defensin (human beta-defensin 3) with specific antimicrobial activity. Its interaction with plasma membranes of Xenopus oocytes and the induction of macrophage chemoattraction. Cell Tissue Res 2001;306:257-64.
22. Liu AY, Destoumieux D, Wong AV, Park CH, Valore EV, Liu L, et al. Human beta-defensin-2 production in keratinocytes is regulated by interleukin-1, bacteria, and the state of differentiation. J Invest Dermatol 2002;118:275-81.
23. Howell MD, Boguniewicz M, Pastore S, Novak N, Bieber T, Girolomoni G, et al. Mechanism of HBD-3 deficiency in atopic dermatitis. Clin Immunol 2006;121:332-8.
24. Nomura I, Goleva E, Howell MD, Hamid QA, Ong PY, Hall CF, et al. Cytokine milieu of atopic dermatitis, as compared to psoriasis, skin prevents induction of innate immune response genes. J Immunol 2003;171:3262-9.
25. Wolk K, Witte E, Warszawska K, Schulze-Tanzil G, Witte K, Philipp S, et al. The Th17 cytokine IL-22 induces IL-20 production in keratinocytes: a novel immunological cascade with potential relevance in psoriasis. Eur J Immunol 2009;39:3570-81.
26. WolkK,Witte K, Witte E, Raftery M, KokolakisG, Philipp S, et al. IL-29 is produced by T(H)17 cells and mediates the cutaneous antiviral competence in psoriasis. Sci Transl Med 2013;5:204ra129.
27. Wolk K, Witte E, Reineke U, Witte K, Friedrich M, Sterry W, et al. Is there an interaction between interleukin-10 and interleukin-22? Genes Immun 2005;6:8-18.
28. Kunz S, Wolk K, Witte E, Witte K, Doecke WD, Volk HD, et al. Interleukin (IL)-19, IL-20 and IL-24 are produced by and act on keratinocytes and are distinct from classical ILs. Exp Dermatol 2006;15:991-1004.
29. Wolk K, Haugen HS, Xu W, Witte E, Waggie K, Anderson M, et al. IL-22 and IL-20 are key mediators of the epidermal alterations in psoriasis while IL-17 and IFN-gamma are not. J Mol Med 2009;87:523-36.
30. Wolk K, Witte E, Wallace E, Docke WD, Kunz S, Asadullah K, et al. IL-22 regulates the expression of genes responsible for antimicrobial defense, cellular differentiation, and mobility in keratinocytes: a potential role in psoriasis. Eur J Immunol 2006;36:1309-23.
31. Miyagaki T, Sugaya M, Suga H, Kamata M, Ohmatsu H, Fujita H, et al. IL-22, but not IL-17, dominant environment in cutaneous T-cell lymphoma. Clin Cancer Res 2011;17:7529-38.
32. Vowels BR, Lessin SR, Cassin M, Jaworsky C, Benoit B, Wolfe JT, et al. Th2 cytokine mRNA expression in skin in cutaneous T-cell lymphoma. J Invest Dermatol 1994;103:669-73.
33. Newcomb DC, Zhou W, Moore ML, Goleniewska K, Hershey GK, Kolls JK, et al. A functional IL-13 receptor is expressed on polarized murine CD4+ Th17 cells and IL-13 signaling attenuates Th17 cytokine production. J Immunol 2009;182:5317-21.
34. Wolk K, Witte K, Sabat R. Interleukin-28 and interleukin-29: novel regulators of skin biology. J Interferon Cytokine Res 2010;30:617-28.
35. Gallo RL, Hooper LV. Epithelial antimicrobial defence of the skin and intestine. Nat Rev Immunol 2012;12:503-16.
36. Wolk K, Warszawska K, Hoeflich C,Witte E, Schneider-Burrus S,Witte K, et al. Deficiency of IL-22 contributes to a chronic inflammatory disease: pathogenetic mechanisms in acne inversa. J Immunol 2011;186:1228-39.
37. Guttman-Yassky E, Lowes MA, Fuentes-Duculan J, Zaba LC, Cardinale I, Nograles KE, et al. Low expression of the IL-23/Th17 pathway in atopic dermatitis compared to psoriasis. J Immunol 2008;181:7420-7.
38. Litvinov IV, Jones DA, Sasseville D, Kupper TS. Transcriptional profiles predict disease outcome in patients with cutaneous T-cell lymphoma. Clin Cancer Res 2010;16:2106-14.
39. Krejsgaard T, Ralfkiaer U, Clasen-Linde E, Eriksen KW, Kopp KL, Bonefeld CM, et al. Malignant cutaneous T-cell lymphoma cells express IL-17 utilizing the Jak3/Stat3 signaling pathway. J Invest Dermatol 2011;131:1331-8.
40. Berger CL, Hanlon D, Kanada D, Dhodapkar M, Lombillo V, Wang N, et al. The growth of cutaneous T-cell lymphoma is stimulated by immature dendritic cells. Blood 2002;99:2929-39.
41. McCusker ME, Garifallou M, Bogen SA. Sezary lineage cells can be induced to proliferate via CD28-mediated costimulation. J Immunol 1997;158:4984-91.
42. Tokura Y, Heald PW, Yan SL, Edelson RL. Stimulation of cutaneous T-cell lymphoma cells with superantigenic staphylococcal toxins. J Invest Dermatol 1992;98:33-7.
43. Marzec M, Halasa K, Kasprzycka M, Wysocka M, Liu X, Tobias JW, et al. Differential effects of interleukin-2 and interleukin-15 versus interleukin-21 on CD4+ cutaneous T-cell lymphoma cells. Cancer Res 2008;68:1083-91.
44. Woetmann A, Lovato P, Eriksen KW, Krejsgaard T, Labuda T, Zhang Q, et al. Nonmalignant T cells stimulate growth of T-cell lymphoma cells in the presence of bacterial toxins. Blood 2007;109:3325-32.
45. Suga H, Sugaya M, Miyagaki T, Kawaguchi M, Fujita H, Asano Y, et al. The Role of IL-32 in Cutaneous T-Cell Lymphoma. J Invest Dermatol 2014;134:1428-35.
46. Yamanaka K, Clark R, Rich B, Dowgiert R, Hirahara K, Hurwitz D, et al. Skin-derived interleukin-7 contributes to the proliferation of lymphocytes in cutaneous T-cell lymphoma. Blood 2006;107:2440-5.
47. Hoogeboom R, van Kessel KP, Hochstenbach F, Wormhoudt TA, Reinten RJ, Wagner K, et al. A mutated B cell chronic lymphocytic leukemia subset that recognizes and responds to fungi. J Exp Med 2013;210:59-70.
48. Bagot M, Wechsler J, Lescs MC, Revuz J, Farcet JP, Gaulard P. Intraepidermal localization of the clone in cutaneous T-cell lymphoma. J Am Acad Dermatol 1992;27:589-93.
49. Gellrich S, Lukowsky A, Schilling T, Rutz S, Muche JM, Jahn S, et al. Microanatomical compartments of clonal and reactive T cells in mycosis fungoides: molecular demonstration by single cell polymerase chain reaction of T cell receptor gene rearrangements. J Invest Dermatol 2000;115:620-4.
50. Sabat R, Ouyang W, Wolk K. Therapeutic opportunities of the IL-22-IL-22R1 system. Nat Rev Drug Discov 2013;13:21-38.