Cross-species identification of genomic drivers of squamous cell carcinoma development across preneoplastic intermediates

Nature Communications

Volumn 7, Issue , 2016, Pages

  Chitsazzadeh, Vida ^a   Coarfa, Cristian ^b   Drummond, Jennifer A ^b   Nguyen, Tri ^c   Joseph, Aaron ^d   Chilukuri, Suneel ^e   Charpiot, Elizabeth ^e   Adelmann, Charles H ^a   Ching, Grace ^a   Nguyen, Tran N ^a   Nicholas, Courtney ^a   Thomas, Valencia D ^a   Migden, Michael ^a   MacFarlane, Deborah ^a   Thompson, Erika ^a   Shen, Jianjun ^a   Takata, Yoko ^a   McNiece, Kayla ^f   Polansky, Maxim A ^f   Abbas, Hussein A ^a   Rajapakshe, Kimal ^b   Gower, Adam ^g   Spira, Avrum ^g   Covington, Kyle R ^b   Xiao, Weimin ^h   Gunaratne, Preethi ^h   Pickering, Curtis ^a   Frederick, Mitchell ^a   Myers, Jeffrey N ^a   Shen, Li ^a   Yao, Hui ^a   Su, Xiaoping ^a   Rapini, Ronald P ^a,f   Wheeler, David A ^b   Hawk, Ernest T ^a   Flores, Elsa R ^a   Tsai, Kenneth Y ^a   more..

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c Northwest Diagnostic Clinic Mohs and Dermatology Associ   (United States)

^d Skin and Laser Surgery Associates   (United States)

^e Bellaire Dermatology Associates   (United States)

^f UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^g BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^h University of Houston   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARCINOGEN; MICRORNA; ANTINEOPLASTIC AGENT;

CANCER; CELLS AND CELL COMPONENTS; EXPERIMENTAL STUDY; GENETIC ANALYSIS; GENOME; IDENTIFICATION METHOD; RODENT; SKIN DISORDER; ULTRAVIOLET RADIATION;

ACTINIC KERATOSIS; ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; EXOME; FEMALE; GENETIC ANALYSIS; GENETIC TRANSCRIPTION; GENOMICS; HAIRLESS MOUSE; HUMAN; HUMAN TISSUE; MALE; MIDDLE AGED; MOUSE; MUTATIONAL ANALYSIS; NONHUMAN; PRECANCER; RNA SEQUENCE; SKIN CARCINOMA; SOLAR RADIATION; TRANSCRIPTOMICS; ULTRAVIOLET RADIATION; VERY ELDERLY; ANIMAL; CARCINOGENESIS; DISEASE EXACERBATION; DNA MUTATIONAL ANALYSIS; GENE EXPRESSION PROFILING; GENETICS; HIGH THROUGHPUT SEQUENCING; MOLECULARLY TARGETED THERAPY; PATHOLOGY; PROCEDURES; SEQUENCE ANALYSIS; SKIN; SKIN TUMOR; SQUAMOUS CELL CARCINOMA; WHOLE EXOME SEQUENCING;

UNITED STATES;

ANIMALS; ANTINEOPLASTIC AGENTS; CARCINOGENESIS; CARCINOMA, SQUAMOUS CELL; DISEASE PROGRESSION; DNA MUTATIONAL ANALYSIS; FEMALE; GENE EXPRESSION PROFILING; GENOMICS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; KERATOSIS, ACTINIC; MICE; MICE, HAIRLESS; MOLECULAR TARGETED THERAPY; PRECANCEROUS CONDITIONS; SEQUENCE ANALYSIS, RNA; SKIN; SKIN NEOPLASMS; ULTRAVIOLET RAYS; WHOLE EXOME SEQUENCING;

EID: 84984904359     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms12601     Document Type: Article

References (80)

1. Rosen, T. & Lebwohl, M. G. Prevalence and awareness of actinic keratosis: barriers and opportunities. J. Am. Acad. Dermatol. 68, S2-S9 (2013).
2. Warino, L. et al. Frequency and cost of actinic keratosis treatment. Dermatol. Surg. 32, 1045-1049 (2006).
3. Criscione, V. D. et al. Actinic keratoses: natural history and risk of malignant transformation in the Veterans Affairs Topical Tretinoin Chemoprevention Trial. Cancer 115, 2523-2530 (2009).
4. Karia, P. S., Han, J. & Schmults, C. D. Cutaneous squamous cell carcinoma: estimated incidence of disease, nodal metastasis, and deaths from disease in the United States, 2012. J. Am. Acad. Dermatol. 68, 957-966 (2013).
5. Neidecker, M. V., Davis-Ajami, M. L., Balkrishnan, R. & Feldman, S. R. Pharmacoeconomic considerations in treating actinic keratosis. Pharmacoeconomics 27, 451-464 (2009).
6. Zaravinos, A., Kanellou, P. & Spandidos, D. A. Viral DNA detection and RAS mutations in actinic keratosis and nonmelanoma skin cancers. Br. J. Dermatol. 162, 325-331 (2010).
7. Kanellou, P. et al. Genomic instability, mutations and expression analysis of the tumour suppressor genes p14(ARF), p15(INK4b), p16(INK4a) and p53 in actinic keratosis. Cancer. Lett. 264, 145-161 (2008).
8. Pacifico, A. et al. Loss of CDKN2A and p14ARF expression occurs frequently in human nonmelanoma skin cancers. Br. J. Dermatol. 158, 291-297 (2008).
9. Rehman, I., Takata, M., Wu, Y. Y. & Rees, J. L. Genetic change in actinic keratoses. Oncogene 12, 2483-2490 (1996).
10. Toll, A. et al. Epidermal growth factor receptor gene numerical aberrations are frequent events in actinic keratoses and invasive cutaneous squamous cell carcinomas. Exp. Dermatol. 19, 151-153 (2010).
11. Toll, A. et al. MYC gene numerical aberrations in actinic keratosis and cutaneous squamous cell carcinoma. Br. J. Dermatol. 161, 1112-1118 (2009).
12. Salgado, R. et al. CKS1B amplification is a frequent event in cutaneous squamous cell carcinoma with aggressive clinical behaviour. Genes Chromosomes Cancer 49, 1054-1061 (2010).
13. Sekulic, A. et al. Loss of inositol polyphosphate 5-phosphatase is an early event in development of cutaneous squamous cell carcinoma. Cancer Prev. Res. (Phila.) 3, 1277-1283 (2010).
14. Padilla, R. S., Sebastian, S., Jiang, Z., Nindl, I. & Larson, R. Gene expression patterns of normal human skin, actinic keratosis, and squamous cell carcinoma: a spectrum of disease progression. Arch. Dermatol. 146, 288-293 (2010).
15. Nindl, I. et al. Identification of differentially expressed genes in cutaneous squamous cell carcinoma by microarray expression profiling. Mol. Cancer 5, 30 (2006).
16. Hameetman, L. et al. Molecular profiling of cutaneous squamous cell carcinomas and actinic keratoses from organ transplant recipients. BMC Cancer 13, 58 (2013).
17. Dooley, T. P., Reddy, S. P., Wilborn, T. W. & Davis, R. L. 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 (2003).
18. Haider, A. S. et al. 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, 869-881 (2006).
19. Kathpalia, V. P. et al. Genome-wide transcriptional profiling in human squamous cell carcinoma of the skin identifies unique tumor-associated signatures. J. Dermatol. 33, 309-318 (2006).
20. Ra, S. H., Li, X. & Binder, S. Molecular discrimination of cutaneous squamous cell carcinoma from actinic keratosis and normal skin. Mod. Pathol. 24, 963-973 (2011).
21. Hudson, L. G. et al. Microarray analysis of cutaneous squamous cell carcinomas reveals enhanced expression of epidermal differentiation complex genes. Mol. Carcinog. 49, 619-629 (2010).
22. Harbig, J., Sprinkle, R. & Enkemann, S. A. A sequence-based identification of the genes detected by probesets on the Affymetrix U133 plus 2.0 array. Nucleic Acids Res. 33, e31 (2005).
23. Benavides, F., Oberyszyn, T. M., VanBuskirk, A. M., Reeve, V. E. & Kusewitt, D. F. The hairless mouse in skin research. J. Dermatol. Sci. 53, 10-18 (2009).
24. Vin, H. et al. BRAF inhibitors suppress apoptosis through off-target inhibition of JNK signaling. Elife 2, e00969 (2013).
25. van Kranen, H. J. et al. Frequent p53 alterations but low incidence of ras mutations in UV-B-induced skin tumors of hairless mice. Carcinogenesis 16, 1141-1147 (1995).
26. Khan, S. G. et al. Mutations in ras oncogenes: rare events in ultraviolet B radiation-induced mouse skin tumorigenesis. Mol. Carcinog. 15, 96-103 (1996).
27. Soufir, N. et al. INK4a-ARF mutations in skin carcinomas from UV irradiated hairless mice. Mol. Carcinog. 39, 195-198 (2004).
28. Ashton, K. J., Weinstein, S. R., Maguire, D. J. & Griffiths, L. R. Chromosomal aberrations in squamous cell carcinoma and solar keratoses revealed by comparative genomic hybridization. Arch. Dermatol. 139, 876-882 (2003).
29. Popp, S. et al. Genetic characterization of a human skin carcinoma progression model: from primary tumor to metastasis. J. Invest. Dermatol. 115, 1095-1103 (2000).
30. Dworkin, A. M. et al. Chromosomal aberrations in UVB-induced tumors of immunosuppressed mice. Genes Chromosomes Cancer 48, 490-501 (2009).
31. Rundhaug, J. E. et al. SAGE profiling of UV-induced mouse skin squamous cell carcinomas, comparison with acute UV irradiation effects. Mol. Carcinog. 42, 40-52 (2005).
32. South, A. P. et al. NOTCH1 mutations occur early during cutaneous squamous cell carcinogenesis. J. Invest. Dermatol. 134, 2630-2638 (2014).
33. Wang, N. J. et al. Loss-of-function mutations in Notch receptors in cutaneous and lung squamous cell carcinoma. Proc. Natl Acad. Sci. USA 108, 17761-17766 (2011).
34. Pickering, C. R. et al. Mutational landscape of aggressive cutaneous squamous cell carcinoma. Clin. Cancer Res. 20, 6582-6592 (2014).
35. Li, Y. Y. et al. Genomic analysis of metastatic cutaneous squamous cell carcinoma. Clin. Cancer Res. 21, 1447-1456 (2015).
36. Martincorena, I. et al. Tumor evolution. High burden and pervasive positive selection of somatic mutations in normal human skin. Science 348, 880-886 (2015).
37. Jonason, A. S. et al. Frequent clones of p53-mutated keratinocytes in normal human skin. Proc. Natl Acad. Sci. USA 93, 14025-14029 (1996).
38. Brash, D. E. UV signature mutations. Photochem. Photobiol. 91, 15-26 (2015).
39. Covington, K. R., Shinbrot, E. & Wheeler, D. A. Mutation signatures reveal biological processes in human cancer, bioRxiv. http://dx.doi.org/10.1101/036541 (2016).
40. Lee, C. S. et al. Recurrent point mutations in the kinetochore gene KNSTRN in cutaneous squamous cell carcinoma. Nat. Genet. 46, 1060-1062 (2014).
41. Ziegler, A. et al. Mutation hotspots due to sunlight in the p53 gene of nonmelanoma skin cancers. Proc. Natl Acad. Sci. USA 90, 4216-4220 (1993).
42. Carter, S. L., Eklund, A. C., Kohane, I. S., Harris, L. N. & Szallasi, Z. A signature of chromosomal instability inferred from gene expression profiles predicts clinical outcome in multiple human cancers. Nat. Genet. 38, 1043-1048 (2006).
43. Kar, A. & Gutierrez-Hartmann, A. Molecular mechanisms of ETS transcription factor-mediated tumorigenesis. Crit. Rev. Biochem. Mol. Biol. 48, 522-543 (2013).
44. Einspahr, J. G. et al. Functional protein pathway activation mapping of the progression of normal skin to squamous cell carcinoma. Cancer Prev. Res. (Phila.) 5, 403-413 (2012).
45. Su, F. et al. RAS mutations in cutaneous squamous-cell carcinomas in patients treated with BRAF inhibitors. N. Engl. J. Med. 366, 207-215 (2012).
46. Kumar, A. P. & Butler, A. P. Enhanced Sp1 DNA-binding activity in murine keratinocyte cell lines and epidermal tumors. Cancer Lett. 137, 159-165 (1999).
47. Miao, Q. et al. Tcf3 promotes cell migration and wound repair through regulation of lipocalin 2. Nat. Commun. 5, 4088 (2014).
48. Bhatia, N. & Spiegelman, V. S. Activation of Wnt/beta-catenin/Tcf signaling in mouse skin carcinogenesis. Mol. Carcinog. 42, 213-221 (2005).
49. Mammucari, C. et al. Integration of Notch 1 and calcineurin/NFAT signaling pathways in keratinocyte growth and differentiation control. Dev. Cell. 8, 665-676 (2005).
50. Eckert, R. L. et al. AP1 transcription factors in epidermal differentiation and skin cancer. J. Skin Cancer 2013, 537028 (2013).
51. Wang, Q. S., Kong, P. Z., Li, X. Q., Yang, F. & Feng, Y. M. FOXF2 deficiency promotes epithelial-mesenchymal transition and metastasis of basal-like breast cancer. Breast Cancer Res. 17, 30 (2015).
52. Ooi, A. T. et al. Molecular profiling of premalignant lesions in lung squamous cell carcinomas identifies mechanisms involved in stepwise carcinogenesis. Cancer Prev. Res. (Phila) 7, 487-495 (2014).
53. Chang, J. T. & Nevins, J. R. GATHER: a systems approach to interpreting genomic signatures. Bioinformatics 22, 2926-2933 (2006).
54. Gunaratne, P. H., Coarfa, C., Soibam, B. & Tandon, A. miRNA data analysis: next-gen sequencing. Methods Mol. Biol. 822, 273-288 (2012).
55. Bruegger, C. et al. MicroRNA expression differs in cutaneous squamous cell carcinomas and healthy skin of immunocompetent individuals. Exp. Dermatol. 22, 426-428 (2013).
56. Dziunycz, P. et al. Squamous cell carcinoma of the skin shows a distinct microRNA profile modulated by UV radiation. J. Invest. Dermatol. 130, 2686-2689 (2010).
57. Wang, A. et al. MicroRNA-31 is overexpressed in cutaneous squamous cell carcinoma and regulates cell motility and colony formation ability of tumor cells. PLoS One 9, e103206 (2014).
58. Akilesh, S. et al. Arhgap24 inactivates Rac1 in mouse podocytes, and a mutant form is associated with familial focal segmental glomerulosclerosis. J. Clin. Invest. 121, 4127-4137 (2011).
59. Wang, W. et al. PTPN14 is required for the density-dependent control of YAP1. Genes Dev. 26, 1959-1971 (2012).
60. Kasem, K. et al. JK1 (FAM134B) represses cell migration in colon cancer: a functional study of a novel gene. Exp. Mol. Pathol. 97, 99-104 (2014).
61. Stransky, N. et al. The mutational landscape of head and neck squamous cell carcinoma. Science 333, 1157-1160 (2011).
62. Agrawal, N. et al. Exome sequencing of head and neck squamous cell carcinoma reveals inactivating mutations in NOTCH1. Science 333, 1154-1157 (2011).
63. Cancer Genome Atlas, N. Comprehensive genomic characterization of head and neck squamous cell carcinomas. Nature 517, 576-582 (2015).
64. Hammerman, P. S. et al. Comprehensive genomic characterization of squamous cell lung cancers. Nature 489, 519-525 (2012).
65. Lin, D. C. et al. Genomic and molecular characterization of esophageal squamous cell carcinoma. Nat. Genet. 46, 467-473 (2014).
66. Bass, A. J. et al. SOX2 is an amplified lineage-survival oncogene in lung and esophageal squamous cell carcinomas. Nat. Genet. 41, 1238-1242 (2009).
67. Arron, S. T., Ruby, J. G., Dybbro, E., Ganem, D. & Derisi, J. L. Transcriptome sequencing demonstrates that human papillomavirus is not active in cutaneous squamous cell carcinoma. J. Invest. Dermatol. 131, 1745-1753 (2011).
68. Ross-Innes, C. S. et al. Whole-genome sequencing provides new insights into the clonal architecture of Barrett's esophagus and esophageal adenocarcinoma. Nat. Genet. 47, 1038-1046 (2015).
69. Stachler, M. D. et al. Paired exome analysis of Barrett's esophagus and adenocarcinoma. Nat. Genet. 47, 1047-1055 (2015).
70. Nassar, D., Latil, M., Boeckx, B., Lambrechts, D. & Blanpain, C. Genomic landscape of carcinogen-induced and genetically induced mouse skin squamous cell carcinoma. Nat. Med. 21, 946-954 (2015).
71. Nghiem, D. X., Walterscheid, J. P., Kazimi, N. & Ullrich, S. E. Ultraviolet radiation-induced immunosuppression of delayed-type hypersensitivity in mice. Methods 28, 25-33 (2002).
72. Alexandrov, L. B. et al. Signatures of mutational processes in human cancer. Nature 500, 415-421 (2013).
73. Lee, W. P. et al. MOSAIK: a hash-based algorithm for accurate next-generation sequencing short-read mapping. PLoS One 9, e90581 (2014).
74. Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).
75. Chen, Y. et al. VirusSeq: software to identify viruses and their integration sites using next-generation sequencing of human cancer tissue. Bioinformatics. 29, 266-267 (2013).
76. Kozomara, A. & Griffiths-Jones, S. miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res. 42, D68-D73 (2014).
77. Johnson, W. E., Li, C. & Rabinovic, A. Adjusting batch effects in microarray expression data using empirical Bayes methods. Biostatistics 8, 118-127 (2007).
78. Agarwal, V., Bell, G. W., Nam, J. W. & Bartel, D. P. Predicting effective microRNA target sites in mammalian mRNAs. Elife 4, 1-38 doi:10.7554/eLife.05005 (2015).
79. Subramanian, A. et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl Acad. Sci. USA 102, 15545-15550 (2005).
80. Krzywinski, M. et al. Circos: an information aesthetic for comparative genomics. Genome Res. 19, 1639-1645 (2009).