Transcriptional profiling identifies an interferon-associated host immune response in invasive squamous cell carcinoma of the skin

International Journal of Cancer

Volumn 123, Issue 11, 2008, Pages 2605-2615

  Wenzel, Joerg ^a   Tomiuk, Stefan ^b   Zahn, Sabine ^a   Küsters, Daniel ^b   Vahsen, Anja ^a   Wiechert, Andreas ^a   Mikus, Sandra ^a   Birth, Michael ^b   Scheler, Marina ^a   Von Bubnoff, Dagmar ^a   Baron, Jens M ^c   Merk, Hans F ^c   Mauch, Cornelia ^d   Krieg, Thomas ^d   Bieber, Thomas ^a   Bosio, Andreas ^b   Hofmann, Kay ^b   Tüting, Thomas ^a   Peters, Bettina ^b  

^a UNIVERSITY OF BONN   (Germany)

^b MILTENYI BIOTEC GMBH   (Germany)

^c UNIVERSITY HOSPITAL RWTH AACHEN   (Germany)

^d UNIVERSITY OF COLOGNE   (Germany)

Author keywords

Cancer; Chemokine; Immunosurveillance; Interferon; Lupus; Skin; SLE

Indexed keywords

CHEMOKINE RECEPTOR CXCR3; CXCL9 CHEMOKINE; CYTOKERATIN; INTERFERON; INTERFERON REGULATORY FACTOR 1;

ADULT; AGED; ARTICLE; CANCER PATIENT; CELL PROLIFERATION; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; GENE; GENE EXPRESSION PROFILING; GRAFT REJECTION; HUMAN; HUMAN TISSUE; IFI27 GENE; IFI30 GENE; IMMUNE RESPONSE; IMMUNOHISTOLOGY; IMMUNOSURVEILLANCE; MALE; MX1 GENE; PRIORITY JOURNAL; SKIN CARCINOMA; SQUAMOUS CELL CARCINOMA; UPREGULATION;

AGED; AGED, 80 AND OVER; CARCINOMA, SQUAMOUS CELL; CELL DIFFERENTIATION; CELL PROLIFERATION; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOHISTOCHEMISTRY; INTERFERONS; KERATINS; MALE; MIDDLE AGED; NEOPLASM INVASIVENESS; NEOPLASMS, BASAL CELL; SKIN NEOPLASMS; TRANSCRIPTION, GENETIC;

EID: 57349159200     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.23799     Document Type: Article

References (58)

1. Pipitone M, Robinson JK, Camara C, Chittineni B, Fisher SG. Skin cancer awareness in suburban employees: a Hispanic perspective. J Am Acad Dermatol 2002;47:118-23.
2. Rubin AI, Chen EH, Ratner D. Basal-cell carcinoma. N Engl J Med 2005;353:2262-9.
3. Alam M, Ratner D. Cutaneous squamous-cell carcinoma. N Engl J Med 2001;344:975-83.
4. Pacifico A, Leone G. Role of p53 and CDKN2A inactivation in human squamous cell carcinomas. J Biomed Biotechnol 2007;2007:43418.
5. Nindl I, Dang C, Forschner T, Kuban RJ, Meyer T, Sterry W, Stockfleth E. Identification of differentially expressed genes in cutaneous squamous cell carcinoma by microarray expression profiling. Mol Cancer 2006;5:30.
6. Rowe DE, Carroll RJ, Day CL, Jr. Prognostic factors for local recurrence, metastasis, and survival rates in squamous cell carcinoma of the skin, ear, and lip. Implications for treatment modality selection. J Am Acad Dermatol 1992;26:976-90.
7. Kruger K, Blume-Peytavi U, Orfanos CE. Basal cell carcinoma possibly originates from the outer root sheath and/or the bulge region of the vellus hair follicle. Arch Dermatol Res 1999;291:253-9.
8. Adolphe C, Hetherington R, Ellis T, Wainwright B. Patched1 functions as a gatekeeper by promoting cell cycle progression. Cancer Res 2006;66:2081-8.
9. O'Driscoll L, McMorrow J, Doolan P, McKiernan E, Mehta JP, Ryan E, Gammell P, Joyce H, O'Donovan N, Walsh N, Clynes M. Investigation of the molecular profile of basal cell carcinoma using whole genome microarrays. Mol Cancer 2006;5:74.
10. Quackenbush J. Microarray analysis and tumor classification. N Engl J Med 2006;354:2463-72.
11. Micke P, Kappert K, Ohshima M, Sundquist C, Scheidl S, Lindahl P, Heldin CH, Botling J, Ponten F, Ostman A. In situ identification of genes regulated specifically in fibroblasts of human basal cell carcinoma. J Invest Dermatol 2007;127:1516-23.
12. Buss K, Bosio A. Expression profiling using SAGE and cDNA arrays. Handbook of Toxicogenomics. Weinheim: Wiley-VCH Verlag Gmbh & Co. KGaA 2005;9-25.
13. Wenzel J, Peters B, Zahn S, Birth M, Hofmann K, Küsters D, Baron J, Merk H, Mauch C, Krieg T, Bieber T, Tüting T, et al. Gene expression profiling of lichen planus reflects CXCL91 mediated inflammation and distinguishes this disease from atopic dermatitis and psoriasis. J Invest Dermatol 2008;128:67-78.
14. Pennartz S, Belvindrah R, Tomiuk S, Zimmer C, Hofmann K, Conradt M, Bosio A, Cremer H. Purification of neuronal precursors from the adult mouse brain: comprehensive gene expression analysis provides new insights into the control of cell migration, differentiation, and homeostasis. Mol Cell Neurosci 2004;25:692-706.
15. Saeed AI, Sharov V, White J, Li J, Liang W, Bhagabati N, Braisted J, Klapa M, Currier T, Thiagarajan M, Sturn A, Snuffin M, et al. TM4: a free, open-source system for microarray data management and analysis. Biotechniques 2003;34:374-8.
16. Appay V, Bosio A, Lokan S,Wiencek Y, Biervert C, Kusters D, Devevre E, Speiser D, Romero P, Rufer N, Leyvraz S. Sensitive gene expression profiling of human T cell subsets reveals parallel post-thymic differentiation for CD4+ and CD8+ lineages. J Immunol 2007;179:7406-14.
17. Christoph T, Bahrenberg G, De Vry J, Englberger W, Erdmann VA, Frech M, Kogel B, Rohl T, Schiene K, Schroder W, Seibler J, Kurreck J. Investigation of TRPV1 loss-of-function phenotypes in transgenic shRNA expressing and knockout mice. Mol Cell Neurosci 2008;37:579-89.
18. Dennis G, Jr, Sherman BT, Hosack DA, Yang J, Gao W, Lane HC, Lempicki RA. DAVID: database for annotation, visualization, and integrated discovery. Genome Biol 2003;4:P3.
19. Wenzel J, Worenkamper E, Freutel S, Henze S, Haller O, Bieber T, Tuting T. Enhanced type I interferon signalling promotes Th1-biased inflammation in cutaneous lupus erythematosus. J Pathol 2005;205:435-42.
20. Baechler EC, Batliwalla FM, Karypis G, Gaffney PM, Ortmann WA, Espe KJ, Shark KB, Grande WJ, Hughes KM, Kapur V, Gregersen PK, Behrens TW. Interferon-inducible gene expression signature in peripheral blood cells of patients with severe lupus. Proc Natl Acad Sci USA 2003;100:2610-15.
21. Bennett L, Palucka AK, Arce E, Cantrell V, Borvak J, Banchereau J, Pascual V. Interferon and granulopoiesis signatures in systemic lupus erythematosus blood. J Exp Med 2003;197:711-23.
22. Dunn GP, Koebel CM, Schreiber RD. Interferons, immunity and cancer immunoediting. Nat Rev Immunol 2006;6:836-48.
23. Leigh IM, Purkis PE, Markey A, Collins P, Neill S, Proby C, Glover M, Lane EB. Keratinocyte alterations in skin tumour development. Recent Results Cancer Res 1993;128:179-91.
24. Sigel JE, Skacel M, Bergfeld WF, House NS, Rabkin MS, Goldblum JR. The utility of cytokeratin 5/6 in the recognition of cutaneous spindle cell squamous cell carcinoma. J Cutan Pathol 2001;28:520-4.
25. Chu PG, Lyda MH, Weiss LM. Cytokeratin 14 expression in epithelial neoplasms: a survey of 435 cases with emphasis on its value in differentiating squamous cell carcinomas from other epithelial tumours. Histopathology 2001;39:9-16.
26. Markey AC, Lane EB, Macdonald DM, Leigh IM. Keratin expression in basal cell carcinomas. Br J Dermatol 1992;126:154-60.
27. Jih DM, Lyle S, Elenitsas R, Elder DE, Cotsarelis G. Cytokeratin 15 expression in trichoepitheliomas and a subset of basal cell carcinomas suggests they originate from hair follicle stem cells. J Cutan Pathol 1999;26:113-18.
28. Billings SD, Southall MD, Li T, Cook PW, Baldridge L, Moores WB, Spandau DF, Foley JG, Travers JB. Amphiregulin overexpression results in rapidly growing keratinocytic tumors: an in vivo xenograft model of keratoacanthoma. Am J Pathol 2003;163:2451-8.
29. Engl T, Relja B, Blumenberg C, Muller I, Ringel EM, Beecken WD, Jonas D, Blaheta RA. Prostate tumor CXC-chemokine profile correlates with cell adhesion to endothelium and extracellular matrix. Life Sci 2006;78:1784-93.
30. Shintani S, Ishikawa T, Nonaka T, Li C, Nakashiro K, Wong DT, Hamakawa H. Growth-regulated oncogene-1 expression is associated with angiogenesis and lymph node metastasis in human oral cancer. Oncology 2004;66:316-22.
31. Pellegrini G, Dellambra E, Golisano O, Martinelli E, Fantozzi I, Bondanza S, Ponzin D, McKeon F, De Luca M. p63 identifies keratinocyte stem cells. Proc Natl Acad Sci USA 2001;98:3156-61.
32. Wilker EW, van Vugt MA, Artim SA, Huang PH, Petersen CP, Reinhardt HC, Feng Y, Sharp PA, Sonenberg N, White FM, Yaffe MB. 14-3-3sigma controls mitotic translation to facilitate cytokinesis. Nature 2007;446:329-32.
33. Becker B, Vogt T, Landthaler M, Stolz W. Detection of differentially regulated genes in keratinocytes by cDNA array hybridization: hsp27 and other novel players in response to artificial ultraviolet radiation. J Invest Dermatol 2001;116:983-8.
34. Hell-Pourmojib M, Neuner P, Fischer H, Rezaie S, Kindas-Mugge I, Knobler R, Trautinger F. Differential expression of a novel gene in response to hsp27 and cell differentiation in human keratinocytes. J Invest Dermatol 2002;119:154-9.
35. Freier K, Flechtenmacher C, Devens F, Hartschuh W, Hofele C, Lichter P, Joos S. Recurrent NMYC copy number gain and high protein expression in basal cell carcinoma. Oncol Rep 2006;15: 1141-5.
36. Xie J, Aszterbaum M, Zhang X, Bonifas JM, Zachary C, Epstein E, McCormick F. A role of PDGFRa in basal cell carcinoma proliferation. Proc Natl Acad Sci USA 2001;98:9255-9.
37. Shiratsuchi T, Ishibashi H, Shirasuna K. Inhibition of epidermal growth factor-induced invasion by dexamethasone and AP-1 decoy in human squamous cell carcinoma cell lines. J Cell Physiol 2002;193: 340-8.
38. Kusukawa J, Sasaguri Y, Morimatsu M, Kameyama T. Expression of matrix metalloproteinase-3 in stage I and II squamous cell carcinoma of the oral cavity. J Oral Maxillofac Surg 1995;53:530-4.
39. Kerkela E, Saarialho-Kere U. Matrix metalloproteinases in tumor progression: focus on basal and squamous cell skin cancer. Exp Dermatol 2003;12:109-25.
40. Kerkela E, Ala-Aho R, Jeskanen L, Rechardt O, Grenman R, Shapiro SD, Kahari VM, Saarialho-Kere U. Expression of human macrophage metalloelastase (MMP-12) by tumor cells in skin cancer. J Invest Dermatol 2000;114:1113-9.
41. Thewes M, Worret WI, Engst R, Ring J. Stromelysin-3 (ST-3): immunohistochemical characterization of the matrix metalloproteinase (MMP)-11 in benign and malignant skin tumours and other skin disorders. Clin Exp Dermatol 1999;24:122-6.
42. Chen IF, Ou-Yang F, Hung JY, Liu JC, Wang H, Wang SC, Hou MF, Hortobagyi GN, Hung MC. AIM2 suppresses human breast cancer cell proliferation in vitro and mammary tumor growth in a mouse model. Mol Cancer Ther 2006;5:1-7.
43. Lengyel P. Tumor-suppressor genes: news about the interferon connection. Proc Natl Acad Sci USA 1993;90:5893-5.
44. Yang G, Xu Y, Chen X, Hu G. IFITM1 plays an essential role in the antiproliferative action of interferon-γ. Oncogene 2007;26:594-603.
45. Andersen JB, Hassel BA. The interferon regulated ubiquitin-like protein. ISG15, in tumorigenesis: friend or foe? Cytokine Growth Factor Rev 2006;17:411-21.
46. Walser TC, Ma X, Kundu N, Dorsey R, Goloubeva O, Fulton AM. Immune-mediated modulation of breast cancer growth and metastasis by the chemokine Mig (CXCL9) in a murine model. J Immunother 2007;30:490-8.
47. Bose A, Baral R. IFNα2b stimulated release of IFNγ differentially regulates T cell and NK cell mediated tumor cell cytotoxicity. Immunol Lett 2007;108:68-77.
48. Kaporis HG, Guttman-Yassky E, Lowes MA, Haider AS, Fuentes-Duculan J, Darabi K, Whynot-Ertelt J, Khatcherian A, Cardinale I, Novitskaya I, Krueger JG, Carucci JA. Human basal cell carcinoma is associated with Foxp3(+) T cells in a Th2 dominant microenvironment. J Invest Dermatol 2007;127:2391-8.
49. Hussein MR, Ahmed RA. Analysis of the mononuclear inflammatory cell infiltrate in the non-tumorigenic, pre-tumorigenic and tumorigenic keratinocytic hyperproliferative lesions of the skin. Cancer Biol Ther 2005;4:819-21.
50. Black AP, Bailey A, Jones L, Turner RJ, Hollowood K, Ogg GS. p53-specific CD8+ T-cell responses in individuals with cutaneous squamous cell carcinoma. Br J Dermatol 2005;153:987-91.
51. Barnetson RS, Halliday GM. Regression in skin tumours: a common phenomenon. Australas J Dermatol 1997;38(Suppl 1):S63-S65.
52. Ulrich C, Schmook T, Nindl I, Meyer T, Sterry W, Stockfleth E. Cutaneous precancers in organ transplant recipients: an old enemy in a new surrounding. Br J Dermatol 2003;149(Suppl 66):40-2.
53. Vanbuskirk A, Oberyszyn TM, Kusewitt DF. Depletion of CD8+ or CD4+ lymphocytes enhances susceptibility to transplantable ultraviolet radiation-induced skin tumours. Anticancer Res 2005;25:1963-7.
54. Galon J, Costes A, Sanchez-Cabo F, Kirilovsky A, Mlecnik B, Lagorce-Pages C, Tosolini M, Camus M, Berger A, Wind P, Zinzindohoue F, Bruneval P, et al. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 2006;313:1960-4.
55. Stasko T, Brown MD, Carucci JA, Euvrard S, Johnson TM, Sengelmann RD, Stockfleth E, Tope WD. Guidelines for the management of squamous cell carcinoma in organ transplant recipients. Dermatol Surg 2004;30:642-50.
56. Dunn GP, Bruce AT, Sheehan KC, Shankaran V, Uppaluri R, Bui JD, Diamond MS, Koebel CM, Arthur C, White JM, Schreiber RD. A critical function for type I interferons in cancer immunoediting. Nat Immunol 2005;6:722-9.
57. Sheehan KC, Lai KS, Dunn GP, Bruce AT, Diamond MS, Heutel JD, Dungo-Arthur C, Carrero JA, White JM, Hertzog PJ, Schreiber RD. Blocking monoclonal antibodies specific for mouse IFN-α/β receptor subunit 1 (IFNAR-1) from mice immunized by in vivo hydrodynamic transfection. J Interferon Cytokine Res 2006;26:804-19.
58. Gasser S, Raulet DH. The DNA damage response arouses the immune system. Cancer Res 2006;66:3959-62.