Expression profile of skin papillomas with high cancer risk displays a unique genetic signature that clusters with squamous cell carcinomas and predicts risk for malignant conversion

Oncogene

Volumn 26, Issue 48, 2007, Pages 6885-6895

  Darwiche, N ^a   Ryscavage, A ^b   Perez Lorenzo, R ^c   Wright, L ^b   Bae, D S ^b,d   Hennings, H ^b   Yuspa, S H ^b   Glick, A B ^c  

^a AMERICAN UNIVERSITY OF BEIRUT   (Lebanon)

^b NATIONAL CANCER INSTITUTE   (United States)

^c PENNSYLVANIA STATE UNIVERSITY   (United States)

^d GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

Author keywords

Microarray; Skin carcinogenesis; Squamous cell carcinoma; Tumor immunology

Indexed keywords

KERATIN; TUMOR MARKER;

ADAPTIVE IMMUNITY; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BENIGN TUMOR; CANCER RISK; COMPARATIVE STUDY; CONTROLLED STUDY; DIAGNOSTIC VALUE; FEMALE; GENE CLUSTER; GENE EXPRESSION PROFILING; GENETIC IDENTIFICATION; IMMUNOHISTOCHEMISTRY; LYMPHOCYTE COUNT; MALIGNANT TRANSFORMATION; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PRECANCER; PRIORITY JOURNAL; PROGNOSIS; SKIN PAPILLOMA; SQUAMOUS CELL CARCINOMA; T LYMPHOCYTE; TUMOR GROWTH;

9,10-DIMETHYL-1,2-BENZANTHRACENE; ANIMALS; CARCINOGENS; CARCINOMA, SQUAMOUS CELL; CELL TRANSFORMATION, NEOPLASTIC; FEMALE; GENE EXPRESSION PROFILING; IMMUNITY, CELLULAR; IMMUNOPHENOTYPING; MICE; MICE, INBRED SENCAR; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PAPILLOMA; PREDICTIVE VALUE OF TESTS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RISK FACTORS; RNA, MESSENGER; SKIN; SKIN NEOPLASMS; TETRADECANOYLPHORBOL ACETATE; TUMOR MARKERS, BIOLOGICAL;

MURINAE;

EID: 34547878575     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/sj.onc.1210491     Document Type: Article

References (38)

1. Balkwill F, Mantovani A. (2001). Inflammation and cancer: back to Virchow? Lancet 357: 539-545.
2. Brown K, Strathdee D, Bryson S, Lambie W, Balmain A. (1998). The malignant capacity of skin tumours induced by expression of a mutant H-ras transgene depends on the cell type targeted. Curr Biol 8: 516-524.
3. Callen JP, Bickers DR, Moy RL. (1997). Actinic keratoses. J Am Acad Dermatol 36: 650-653.
4. Coussens LM, Raymond WW, Bergers G, Laig-Webster M, Behrendtsen O, Werb Z et al. (1999). Inflammatory mast cells up-regulate angiogenesis during squamous epithelial carcinogenesis. Genes Dev 13: 1382-1397.
5. Coussens LM, Werb Z. (2002). Inflammation and cancer. Nature 420: 860-867.
6. Ha oncogene and high risk for premalignant progression. Cancer Res 56: 4942-4959.
7. de Visser KE, Korets LV, Coussens LM. (2005). De novo carcinogenesis promoted by chronic inflammation is B lymphocyte dependent. Cancer Cell 7: 411-423.
8. Dighe AS, Richards E, Old LJ, Schreiber RD. (1994). Enhanced in vivo growth and resistance to rejection of tumor cells expressing dominant negative IFN gamma receptors. Immunity 1: 447-456.
9. Dong G, Loukinova E, Smith CW, Chen Z, Van Waes C. (1997). Genes differentially expressed with malignant transformation and metastatic tumor progression of murine squamous cell carcinoma. J Cell Biochem Suppl 28-29: 90-100.
10. Dooley TP, Reddy SP, Wilborn TW, Davis RL. (2003). Biomarkers of human cutaneous squamous cell carcinoma from tissues and cell lines identified by DNA microarrays and qRT-PCR. Biochem Biophys Res Commun 306: 1026-1036.
11. Dumitriu IE, Baruah P, Manfredi AA, Bianchi ME, Rovere-Querini P. (2005). HMGB1: guiding immunity from within. Trends Immunol 26: 381-387.
12. Girardi M, Glusac E, Filler RB, Roberts SJ, Propperova I, Lewis J et al. (2003). The distinct contributions of murine T cell receptor (TCR)gammadelta+ and TCRalphabeta+ T cells to different stages of chemically induced skin cancer. J Exp Med 198: 747-755.
13. Girardi M, Oppenheim DE, Steele CR, Lewis JM, Glusac E, Filler R et al. (2001). Regulation of cutaneous malignancy by gammadelta T cells. Science 294: 605-609.
14. Glick AB, Kulkarni AB, Tennenbaum T, Hennings H, Flanders KC, O'Reilly M et al. (1993). Loss of expression of transforming growth factor β in skin and skin tumors is associated with hyperproliferation and a high risk for malignant conversion. Proc Natl Acad Sci USA 90: 6076-6080.
15. Glinsky GV, Glinskii AB, Stephenson AJ, Hoffman RM, Gerald WL. (2004). Gene expression profiling predicts clinical outcome of prostate cancer. J Clin Invest 113: 913-923.
16. Hennings H, Shores R, Mitchell P, Spangler EF, Yuspa SH. (1985). Induction of papillomas with a high probability of conversion to malignancy. Carcinogenesis 6: 1607-1610.
17. Hummerich L, Muller R, Hess J, Kokocinski F, Hahn M, Furstenberger G et al. (2006). Identification of novel tumour-associated genes differentially expressed in the process of squamous cell cancer development. Oncogene 25: 111-121.
18. Juric D, Sale S, Hromas RA, Yu R, Wang Y, Duran GE et al. (2005). Gene expression profiling differentiates germ cell tumors from other cancers and defines subtype-specific signatures. Proc Natl Acad Sci USA 102: 17763-17768.
19. Kaplan DH, Shankaran V, Dighe AS, Stockert E, Aguet M, Old LJ et al. (1998). Demonstration of an interferon gamma-dependent tumor surveillance system in immunocompetent mice. Proc Natl Acad Sci USA 95: 7556-7561.
20. Larcher F, Bauluz C, Diaz-Guerra M, Quintanilla M, Conti CJ, Ballestin C et al. (1992). Aberrant expression of the simple epithelial type II keratin 8 by mouse skin carcinomas but not papillomas. Mol Carcinog 6: 112-121.
21. Lossos IS, Czerwinski DK, Alizadeh AA, Wechser MA, Tibshirani R, Botstein D et al. (2004). Prediction of survival in diffuse large-B-cell lymphoma based on the expression of six genes. N Engl J Med 350: 1828-1837.
22. Ma C, Staudt LM. (1996). LAF-4 encodes a lymphoid nuclear protein with transactivation potential that is homologous to AF-4, the gene fused to MLL in t(4;11) leukemias. Blood 87: 734-745.
23. Morris RJ, Coulter K, Tryson K, Steinberg SR. (1997). Evidence that cutaneous carcinogen-initiated epithelial cells from mice are quiescent rather than actively cycling. Cancer Res 57: 3436-3443.
24. Morris RJ, Tryson KA, Wu KQ. (2000). Evidence that the epidermal targets of carcinogen action are found in the interfollicular epidermis of infundibulum as well as in the hair follicles. Cancer Res 60: 226-229.
25. Nambiar PR, Nakanishi M, Gupta R, Cheung E, Firouzi A, Ma XJ et al. (2004). Genetic signatures of high- and low-risk aberrant crypt foci in a mouse model of sporadic colon cancer. Cancer Res 64: 6394-6401.
26. Nishimura H, Washizu J, Nakamura N, Enomoto A, Yoshikai Y. (1998). Translational efficiency is up-regulated by alternative exon in murine IL-15 mRNA. J Immunol 160: 936-942.
27. Nishimura H, Yajima T, Naiki Y, Tsunobuchi H, Umemura M, Itano K et al. (2000). Differential roles of interleukin 15 mRNA isoforms generated by alternative splicing in immune responses in vivo. J Exp Med 191: 157-170.
28. Ozaki K, Inoue K, Sato H, Iida A, Ohnishi Y, Sekine A et al. (2004). Functional variation in LGALS2 confers risk of myocardial infarction and regulates lymphotoxin-alpha secretion in vitro. Nature 429: 72-75.
29. Perez-Losada J, Balmain A. (2003). Stem-cell hierarchy in skin cancer. Nat Rev Cancer 3: 434-443.
30. Peyssonnaux C, Zinkernagel AS, Datta V, Lauth X, Johnson RS, Nizet V. (2006). TLR-4 dependent hepcidin expression by myeloid cells in response to bacterial pathogens. Blood 107: 3727-3732.
31. Rhodes DR, Yu J, Shanker K, Deshpande N, Varambally R, Ghosh D et al. (2004). ONCOMINE: a cancer microarray database and integrated data-mining platform. Neoplasia 6: 1-6.
32. Ridd K, Zhang SD, Edwards RE, Davies R, Greaves P, Wolfreys A et al. (2006). Association of gene expression with sequential proliferation, differentiation and tumor formation in murine skin. Carcinogenesis 27: 1556-1566.
33. Schlingemann J, Hess J, Wrobel G, Breitenbach U, Gebhardt C, Steinlein P et al. (2003). Profile of gene expression induced by the tumour promotor TPA in murine epithelial cells. Int J Cancer 104: 699-708.
34. Serewko MM, Popa C, Dahler AL, Smith L, Strutton GM, Coman W et al. (2002). Alterations in gene expression and activity during squamous cell carcinoma development. Cancer Res 62: 3759-3765.
35. Smyth MJ, Thia KY, Street SE, MacGregor D, Godfrey DI, Trapani JA. (2000). Perforin-mediated cytotoxicity is critical for surveillance of spontaneous lymphoma. J Exp Med 192: 755-760.
36. Tennenbaum T, Weiner AK, Belanger AJ, Glick AB, Hennings H, Yuspa SH. (1993). The suprabasal expression of α6β4 integrin is associated with a high risk for malignant progression in mouse skin carcinogenesis. Cancer Res 53: 4803-4810.
37. Tibshirani R, Hastie T, Narasimhan B, Chu G. (2002). Diagnosis of multiple cancer types by shrunken centroids of gene expression 2. Proc Natl Acad Sci USA 99: 6567-6572.
38. Yuspa SH. (1998). The pathogenesis of squamous cell cancer: lessons learned from studies of skin carcinogenesis. J Dermatol Sci 17: 1-7.