Key differences identified between actinic keratosis and cutaneous squamous cell carcinoma by transcriptome profiling

British Journal of Cancer

Volumn 110, Issue 2, 2014, Pages 520-529

  Lambert, S R ^a   Mladkova, N ^a   Gulati, A ^a   Hamoudi, R ^b   Purdie, K ^a   Cerio, R ^a   Leigh, I ^a,c   Proby, C ^a,c   Harwood, C A ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

actinic keratosis; cutaneous squamous cell carcinoma; differentiation status; expression microarray profiling; MAPK pathway; skin cancer

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; TRANSCRIPTOME;

ACTINIC KERATOSIS; ANGIOGENESIS; ARTICLE; CANCER PATIENT; CANCER PREVENTION; CELL CYCLE REGULATION; CELL DIFFERENTIATION; CELL METABOLISM; CELL MIGRATION; FEMALE; GENE EXPRESSION PROFILING; HUMAN; HUMAN TISSUE; IMMUNOCOMPROMISED PATIENT; LASER CAPTURE MICRODISSECTION; MALE; MICROARRAY ANALYSIS; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; RNA EXTRACTION; SKIN CARCINOMA; SQUAMOUS CELL CARCINOMA; ADULT; AGED; CLINICAL ARTICLE; CONTROLLED STUDY; DIFFERENTIALLY EXPRESSED GENE; ENZYME ACTIVITY; GENE; GENE FUNCTION; GENE IDENTIFICATION; HISTOPATHOLOGY; KERATINOCYTE; MALIGNANT TRANSFORMATION; MICROARRAY KIT; SIGNAL TRANSDUCTION; SKIN CARCINOGENESIS; TRANSCRIPTOMICS;

ADULT; AGED; AGED, 80 AND OVER; CARCINOMA, SQUAMOUS CELL; CELL ADHESION; CELL CYCLE; CELL DIFFERENTIATION; CELL MOVEMENT; CELL PROLIFERATION; DISEASE PROGRESSION; EPIDERMIS; FEMALE; GENE EXPRESSION PROFILING; HUMANS; KERATOSIS, ACTINIC; MALE; MIDDLE AGED; MITOGEN-ACTIVATED PROTEIN KINASES; NEOVASCULARIZATION, PATHOLOGIC; SKIN NEOPLASMS; TRANSCRIPTOME;

EID: 84892928428     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/bjc.2013.760     Document Type: Article

References (51)

1. Arnault JP, Mateus C, Escudier B, Tomasic G, Wechsler J, Hollville E, Soria JC, Malka D, Sarasin A, Larcher M, Andre J, Kamsu-Kom N, Boussemart L, Lacroix L, Spatz A, Eggermont AM, Druillennec S, Vagner S, Eychene A, Dumaz N, Robert C (2012) Skin tumors induced by sorafenib; paradoxic RAS-RAF pathway activation and oncogenic mutations of HRAS, TP53, and TGFBR1. Clin Cancer Res 18(1): 263-272.
2. Ashton KJ, Weinstein SR, Maguire DJ, Griffiths LR (2003) Chromosomal aberrations in squamous cell carcinoma and solar keratoses revealed by comparative genomic hybridization. Arch Dermatol 139(7): 876-882.
3. Breuninger H, Brantsch K, Eigentler T, Hafner HM (2012) Comparison and evaluation of the current staging of cutaneous carcinomas. J Dtsch Dermatol Ges 10(8): 579-586.
4. Brown VL, Harwood CA, Crook T, Cronin JG, Kelsell DP, Proby CM (2004) p16INK4a and p14ARF tumor suppressor genes are commonly inactivated in cutaneous squamous cell carcinoma. J Invest Dermatol 122(5): 1284-1292.
5. Clausen OP, Aass HC, Beigi M, Purdie KJ, Proby CM, Brown VL, Mattingsdal M, Micci F, Kolvraa S, Bolund L, Deangelis PM (2006) Are keratoacanthomas variants of squamous cell carcinomas? A comparison of chromosomal aberrations by comparative genomic hybridization. J Invest Dermatol 126(10): 2308-2315.
6. Criscione VD, Weinstock MA, Naylor MF, Luque C, Eide MJ, Bingham SF (2009) Actinic keratoses: natural history and risk of malignant transformation in the Veterans Affairs Topical Tretinoin Chemoprevention Trial. Cancer 115(11): 2523-2530.
7. de Vries E, van de Poll-Franse LV, Louwman WJ, de Gruijl FR, Coebergh JW (2005) Predictions of skin cancer incidence in the Netherlands up to 2015.Br J Dermatol 152(3): 481-488.
8. Dhillon AS, Hagan S, Rath O, Kolch W (2007) MAP kinase signalling pathways in cancer. Oncogene 26(22): 3279-3290.
9. Durinck S, Ho C, Wang NJ, LiaoW, Jakkula LR, Collisson EA, Pons J, Chan SW, Lam ET, Chu C, Park K, Hong SW, Hur JS, Huh N, Neuhaus IM, Yu SS, Grekin RC, Mauro TM, Cleaver JE, Kwok PY, LeBoit PE,GetzG,Cibulskis K, Aster JC, Huang H, Purdom E, Li J, Bolund L, Arron ST, Gray JW, Spellman PT, Cho RJ (2011) Temporal dissection of tumorigenesis in primary cancers. Cancer Discov 1(2): 137-143.
10. Einspahr JG, Calvert V, Alberts DS, Curiel-Lewandrowski C, Warneke J, Krouse R, Stratton SP, Liotta L, Longo C, Pellacani G, Prasad A, Sagerman P, Bermudez Y, Deng J, Bowden GT, Petricoin 3rd EF (2012) Functional protein pathway activation mapping of the progression of normal skin to squamous cell carcinoma. Cancer Prev Res (Phila) 5(3): 403-413.
11. Euvrard S, Kanitakis J, Claudy A (2003) Skin cancers after organ transplantation. N Engl J Med 348(17): 1681-1691.
12. Skin Care Foundation (2010) Skin Cancer Foundation Vol. 2010. Skin Care Foundation: New York.
13. Frost C, Williams G, Green A (2000) High incidence and regression rates of solar keratoses in a queensland community. J Invest Dermatol 115(2): 273-277.
14. Gialeli C, Theocharis AD, Karamanos NK (2011) Roles of matrix metalloproteinases in cancer progression and their pharmacological targeting. FEBS J 278(1): 16-27.
15. Tumor Analysis Best Practices Working Group (2004) Expression profiling-best practices for data generation and interpretation in clinical trials. Nat Rev Genet 5(3): 229-237.
16. Haider AS, Peters SB, Kaporis H, Cardinale I, Fei J, Ott J, Blumenberg M, Bowcock AM, Krueger JG, Carucci JA (2006) Genomic analysis defines a cancer-specific gene expression signature for human squamous cell carcinoma and distinguishes malignant hyperproliferation from benign hyperplasia. J Invest Dermatol 126(4): 869-881.
17. Hameetman L, Commandeur S, Bavinck JN, Wisgerhof HC, de Gruijl FR, Willemze R, Mullenders L, Tensen CP, Vrieling H (2013) Molecular profiling of cutaneous squamous cell carcinomas and actinic keratoses from organ transplant recipients. BMC Cancer 13: 58.
18. Hamoudi RA, Appert A, Ye H, Ruskone-Fourmestraux A, Streubel B, Chott A, Raderer M, Gong L, Wlodarska I, De Wolf-Peeters C, MacLennan KA, de Leval L, Isaacson PG, Du MQ (2010) Differential expression of NF-kappaB target genes in MALT lymphoma with and without chromosome translocation: insights into molecular mechanism. Leukemia 24(8): 1487-1497.
19. Harwood CA, Mesher D, McGregor JM, Mitchell L, Leedham-Green M, Raftery M, Cerio R, Leigh IM, Sasieni P, Proby CM (2013) A surveillance model for skin cancer in organ transplant recipients: a 22-year prospective study in an ethnically diverse population. Am J Transplant 13(1): 119-129.
20. Harwood CA, Proby CM, McGregor JM, Sheaff MT, Leigh IM, Cerio R (2006) Clinicopathologic features of skin cancer in organ transplant recipients: a retrospective case-control series. J Am Acad Dermatol 54(2): 290-300.
21. Hatzivassiliou G, Song K, Yen I, Brandhuber BJ, Anderson DJ, Alvarado R, Ludlam MJ, Stokoe D, Gloor SL, Vigers G, Morales T, Aliagas I, Liu B, Sideris S, Hoeflich KP, Jaiswal BS, Seshagiri S, Koeppen H, Belvin M, Friedman LS, Malek S (2010) RAF inhibitors prime wild-type RAF to activate the MAPK pathway and enhance growth. Nature 464(7287): 431-435.
22. Heidorn SJ, Milagre C, Whittaker S, Nourry A, Niculescu-Duvas I, Dhomen N, Hussain J, Reis-Filho JS, Springer CJ, Pritchard C, Marais R (2010) Kinasedead BRAF and oncogenic RAS cooperate to drive tumor progression through CRAF. Cell 140(2): 209-221.
23. Jambusaria-Pahlajani A, Kanetsky PA, Karia PS, Hwang WT, Gelfand JM, Whalen FM, Elenitsas R, Xu X, Schmults CD (2013) Evaluation of AJCC Tumor Staging for cutaneous squamous cell carcinoma and a proposed alternative tumor staging system. JAMA Dermatol 149(4): 402-410.
24. Jonason AS, Kunala S, Price GJ, Restifo RJ, Spinelli HM, Persing JA, Leffell DJ, Tarone RE, Brash DE (1996) Frequent clones of p53-mutated keratinocytes in normal human skin. Proc Natl Acad Sci USA 93(24): 14025-14029.
25. Kathpalia VP, Mussak EN, Chow SS, Lam PH, Skelley N, Time M, Markelewicz Jr RJ, Kanduc D, Lomas L, Xiang Z, Sinha AA (2006) Genome-wide transcriptional profiling in human squamous cell carcinoma of the skin identifies unique tumor-associated signatures. J Dermatol 33(5): 309-318.
26. Kraus DH, Carew JF, Harrison LB (1998) Regional lymph node metastasis from cutaneous squamous cell carcinoma. Arch Otolaryngol Head Neck Surg 124(5): 582-587.
27. Lambert SR, Harwood CA, Purdie KJ, Gulati A, Matin RN, Romanowska M, Cerio R, Kelsell DP, Leigh IM, Proby CM (2012) Metastatic cutaneous squamous cell carcinoma shows frequent deletion in the protein tyrosine phosphatase receptor Type D gene. Int J Cancer 131(3): E216-E226.
28. Lo Muzio L, Staibano S, Pannone G, Mignogna MD, Mariggio A, Salvatore G, Chieffi P, Tramontano D, De Rosa G, Altieri DC (2001) Expression of the apoptosis inhibitor survivin in aggressive squamous cell carcinoma. Exp Mol Pathol 70(3): 249-254.
29. Madan V, Lear JT, Szeimies RM (2010) Non-melanoma skin cancer. Lancet 375(9715): 673-685.
30. Memon AA, Tomenson JA, Bothwell J, Friedmann PS (2000) Prevalence of solar damage and actinic keratosis in a Merseyside population. Br J Dermatol 142(6): 1154-1159.
31. Mourouzis C, Boynton A, Grant J, Umar T, Wilson A, Macpheson D, Pratt C (2009) Cutaneous head and neck SCCs and risk of nodal metastasis-UK experience. J Craniomaxillofacial Surg 37(8): 443-447.
32. Nindl I, Dang C, Forschner T, Kuban RJ, Meyer T, Sterry W, Stockfleth E (2006) Identification of differentially expressed genes in cutaneous squamous cell carcinoma by microarray expression profiling. Mol Cancer 5: 30.
33. Overall CM, Kleifeld O (2006) Tumour microenvironment-opinion: validating matrix metalloproteinases as drug targets and anti-targets for cancer therapy. Nat Rev Cancer 6(3): 227-239.
34. Padilla RS, Sebastian S, Jiang Z, Nindl I, Larson R (2010) Gene expression patterns of normal human skin, actinic keratosis, and squamous cell carcinoma: a spectrum of disease progression. Arch Dermatol 146(3): 288-293.
35. Popp S, Waltering S, Herbst C, Moll I, Boukamp P (2002) UV-B-type mutations and chromosomal imbalances indicate common pathways for the development of Merkel and skin squamous cell carcinomas. Int J Cancer 99(3): 352-360.
36. Poulikakos PI, Zhang C, Bollag G, Shokat KM, Rosen N (2010) RAF inhibitors transactivate RAF dimers and ERK signalling in cells with wild-type BRAF. Nature 464(7287): 427-430.
37. Purdie KJ, Harwood CA, Gulati A, Chaplin T, Lambert SR, Cerio R, Kelly GP, Cazier JB, Young BD, Leigh IM, Proby CM (2009) Single nucleotide polymorphism array analysis defines a specific genetic fingerprint for well-differentiated cutaneous SCCs. J Invest Dermatol 129(6): 1562-1568.
38. Purdie KJ, Lambert SR, Teh MT, Chaplin T, Molloy G, Raghavan M, Kelsell DP, Leigh IM, Harwood CA, Proby CM, Young BD (2007) Allelic imbalances and microdeletions affecting the PTPRD gene in cutaneous squamous cell carcinomas detected using single nucleotide polymorphism microarray analysis. Genes Chromosomes Cancer 46(7): 661-669.
39. Quinn AG, Sikkink S, Rees JL (1994) Basal cell carcinomas and squamous cell carcinomas of human skin show distinct patterns of chromosome loss. Cancer Res 54(17): 4756-4759.
40. Ra SH, Li X, Binder S (2011) Molecular discrimination of cutaneous squamous cell carcinoma from actinic keratosis and normal skin. Mod Pathol 24(7): 963-973.
41. Ribas A, Flaherty KT (2011) BRAF targeted therapy changes the treatment paradigm in melanoma. Nat Rev Clin Oncol 8(7): 426-433.
42. Rogers HW,Weinstock MA, Harris AR, Hinckley MR, Feldman SR, Fleischer AB, Coldiron BM (2010) Incidence estimate of nonmelanoma skin cancer in the United States, 2006. Arch Dermatol 146(3): 283-287.
43. Rowe DE, Carroll RJ, Day Jr. CL (1992) 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 26(6): 976-990.
44. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, Mesirov JP (2005) Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA 102(43): 15545-15550.
45. Tam CW, Liu VW, Leung WY, Yao KM, Shiu SY (2008) The autocrine human secreted PDZ domain-containing protein 2 (sPDZD2) induces senescence or quiescence of prostate, breast and liver cancer cells via transcriptional activation of p53. Cancer Lett 271(1): 64-80.
46. Tanemura A, Nagasawa T, Inui S, Itami S (2005) LRIG-1 provides a novel prognostic predictor in squamous cell carcinoma of the skin: immunohistochemical analysis for 38 cases. Dermatol Surg 31(4): 423-430.
47. Tu WH, Zhu C, Clark C, Christensen JG, Sun Z (2010) Efficacy of c-Met inhibitor for advanced prostate cancer. BMC cancer 10: 556.
48. Van Haren R, Feldman D, Sinha AA (2009) Systematic comparison of nonmelanoma skin cancer microarray datasets reveals lack of consensus genes. Br J Dermatol 161(6): 1278-1287.
49. Wang NJ, Sanborn Z, Arnett KL, Bayston LJ, Liao W, Proby CM, Leigh IM, Collisson EA, Gordon PB, Jakkula L, Pennypacker S, Zou Y, Sharma M, North JP, Vemula SS, Mauro TM, Neuhaus IM, Leboit PE, Hur JS, Park K, Huh N, Kwok PY, Arron ST, Massion PP, Bale AE, Haussler D, Cleaver JE, Gray JW, Spellman PT, South AP, Aster JC, Blacklow SC, Cho RJ (2011) Loss-of-function mutations in Notch receptors in cutaneous and lung squamous cell carcinoma. Proc Natl Acad Sci USA 108(43): 17761-17766.
50. Wang Y, Solt LA, Kojetin DJ, Burris TP (2012) Regulation of p53 stability and apoptosis by a ROR agonist. PLoS One 7(4): e34921.
51. Yip PY, Kench JG, Rasiah KK, Benito RP, Lee CS, Stricker PD, Henshall SM, Sutherland RL, Horvath LG (2011) Low AZGP1 expression predicts for recurrence in margin-positive, localized prostate cancer. Prostate 71(15): 1638-1645.