Cdkn2a suppresses metastasis in squamous cell carcinomas induced by the gain-of-function mutant p53R172H

Journal of Pathology

Volumn 240, Issue 2, 2016, Pages 224-234

  Li, Zhongyou ^a   Gonzalez, Cassandra L ^a   Wang, Bingbing ^a   Zhang, Yuanyuan ^a   Mejia, Olga ^a   Katsonis, Panagiotis ^b   Lichtarge, Olivier ^b   Myers, Jeffrey N ^a   El Naggar, Adel K ^a   Caulin, Carlos ^a  

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

^b BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Cdkn2a; metastasis; p53; squamous cell carcinoma

Indexed keywords

CYCLIN D1; CYCLIN DEPENDENT KINASE INHIBITOR 2A; MESSENGER RNA; PROTEIN P19;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER PATIENT; CANCER SURVIVAL; CDKN2A GENE; CONTROLLED STUDY; GAIN OF FUNCTION MUTATION; GENE; GENE DELETION; HEAD AND NECK SQUAMOUS CELL CARCINOMA; HIGH RISK PATIENT; IMMUNOHISTOCHEMISTRY; METASTASIS INHIBITION; MOUSE; NONHUMAN; OUTCOME ASSESSMENT; PRIORITY JOURNAL; SKIN CARCINOMA; SQUAMOUS CELL CARCINOMA; TUMOR MODEL; TUMOR SUPPRESSOR GENE; WILD TYPE;

EID: 84988624562     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.4770     Document Type: Article

References (45)

1. Agrawal N, Frederick MJ, Pickering CR, et al. Exome sequencing of head and neck squamous cell carcinoma reveals inactivating mutations in NOTCH1. Science 2011; 333: 1154–1157.
2. Stransky N, Egloff AM, Tward AD, et al. The mutational landscape of head and neck squamous cell carcinoma. Science 2011; 333: 1157-1160.
3. The Cancer Genome Atlas Network. Comprehensive genomic characterization of head and neck squamous cell carcinomas. Nature 2015; 517: 576-582.
4. Pickering CR, Zhou JH, Lee JJ, et al. Mutational landscape of aggressive cutaneous squamous cell carcinoma. Clin Cancer Res 2014; 20: 6582-6592.
5. Li YY, Hanna GJ, Laga AC, et al. Genomic analysis of metastatic cutaneous squamous cell carcinoma. Clin Cancer Res 2015; 21: 1447-1456.
6. Dittmer D, Pati S, Zambetti G, et al. Gain of function mutations in p53. Nature Genet 1993; 4: 42-46.
7. Zhou G, Wang J, Zhao M, et al. Gain-of-function mutant p53 promotes cell growth and cancer cell metabolism via inhibition of AMPK activation. Mol Cell 2014; 54: 960-974.
8. Brosh R, Rotter V. When mutants gain new powers: news from the mutant p53 field. Nature Rev Cancer 2009; 9: 701-713.
9. Lang GA, Iwakuma T, Suh YA, et al. Gain of function of a p53 hot spot mutation in a mouse model of Li–Fraumeni syndrome. Cell 2004; 119: 861-872.
10. Hanel W, Marchenko N, Xu S, et al. Two hot spot mutant p53 mouse models display differential gain of function in tumorigenesis. Cell Death Differ 2013; 20: 898-909.
11. Xu J, Qian J, Hu Y, et al. Heterogeneity of Li–Fraumeni syndrome links to unequal gain-of-function effects of p53 mutations. Sci Rep 2014; 4: 4223.
12. Poeta ML, Manola J, Goldwasser MA, et al. TP53 mutations and survival in squamous-cell carcinoma of the head and neck. N Engl J Med 2007; 357: 2552-2561.
13. Neskey DM, Osman AA, Ow TJ, et al. Evolutionary action score of TP53 identifies high-risk mutations associated with decreased survival and increased distant metastases in head and neck cancer. Cancer Res 2015; 75: 1527-1536.
14. Caulin C, Nguyen T, Lang GA, et al. An inducible mouse model for skin cancer reveals distinct roles for gain- and loss-of-function p53 mutations. J Clin Invest 2007; 117: 1893-1901.
15. Acin S, Li Z, Mejia O, et al. Gain-of-function mutant p53 but not p53 deletion promotes head and neck cancer progression in response to oncogenic K-ras. J Pathol 2011; 225: 479-489.
16. Serrano M, Hannon GJ, Beach D. A new regulatory motif in cell-cycle control causing specific inhibition of cyclin D/CDK4. Nature 1993; 366: 704-707.
17. Quelle DE, Zindy F, Ashmun RA, et al. Alternative reading frames of the INK4a tumor suppressor gene encode two unrelated proteins capable of inducing cell cycle arrest. Cell 1995; 83: 993-1000.
18. Sharpless NE. INK4a/ARF: a multifunctional tumor suppressor locus. Mutat Res 2005; 576: 22-38.
19. Serrano M, Lee H, Chin L. Role of the INK4a locus in tumor suppression and cell mortality. Cell 1996; 85: 27-37.
20. Kamijo T, Zindy F, Roussel MF, et al. Tumor suppression at the mouse INK4a locus mediated by the alternative reading frame product p19ARF. Cell 1997; 91: 649-659.
21. Arf predisposes mice to tumorigenesis. Nature 2001; 413: 86-91.
22. Hodges A, Smoller BR. Immunohistochemical comparison of p16 expression in actinic keratoses and squamous cell carcinomas of the skin. Mod Pathol 2002; 15: 1121-1125.
23. INK4a expression and infiltrative behavior. Mod Pathol 2004; 17: 1464-1474.
24. Jonkers J, Meuwissen R, van der Gulden H, et al. Synergistic tumor suppressor activity of BRCA2 and p53 in a conditional mouse model for breast cancer. Nature Genet 2001; 29: 418-425.
25. Aguirre AJ, Bardeesy N, Sinha M, et al. Activated Kras and Ink4a/Arf deficiency cooperate to produce metastatic pancreatic ductal adenocarcinoma. Genes Dev 2003; 17: 3112-3126.
26. Zhou Z, Wang D, Wang XJ, et al. In utero activation of K5.CrePR1 induces gene deletion. Genesis 2002; 32: 191-192.
27. Tang KW, Alaei-Mahabadi B, Samuelsson T, et al. The landscape of viral expression and host gene fusion and adaptation in human cancer. Nature Commun 2013; 4: 2513.
28. Campbell C, Quinn AG, Ro YS, et al. p53 mutations are common and early events that precede tumor invasion in squamous cell neoplasia of the skin. J Invest Dermatol 1993; 100: 746-748.
29. Ziegler A, Jonason AS, Leffell DJ, et al. Sunburn and p53 in the onset of skin cancer. Nature 1994; 372: 773-776.
30. Nakazawa H, English D, Randell PL, et al. UV and skin cancer: specific p53 gene mutation in normal skin as a biologically relevant exposure measurement. Proc Natl Acad Sci U S A 1994; 91: 360-364.
31. Jonason AS, Kunala S, Price GJ, et al. Frequent clones of p53-mutated keratinocytes in normal human skin. Proc Natl Acad Sci U S A 1996; 93: 14025-14029.
32. Ren ZP, Hedrum A, Ponten F, et al. Human epidermal cancer and accompanying precursors have identical p53 mutations different from p53 mutations in adjacent areas of clonally expanded non-neoplastic keratinocytes. Oncogene 1996; 12: 765-773.
33. Klein-Szanto AJ, Larcher F, Bonfil RD, et al. Multistage chemical carcinogenesis protocols produce spindle cell carcinomas of the mouse skin. Carcinogenesis 1989; 10: 2169-2172.
34. Wijnhoven SW, Speksnijder EN, Liu X, et al. Dominant-negative but not gain-of-function effects of a p53.R270H mutation in mouse epithelium tissue after DNA damage. Cancer Res 2007; 67: 4648-4656.
35. Jayasurya R, Sathyan KM, Lakshminarayanan K, et al. Phenotypic alterations in Rb pathway have more prognostic influence than p53 pathway proteins in oral carcinoma. Mod Pathol 2005; 18: 1056-1066.
36. Nakahara Y, Shintani S, Mihara M, et al. Alterations of Rb, p16(INK4A) and cyclin D1 in the tumorigenesis of oral squamous cell carcinomas. Cancer Lett 2000; 160: 3-8.
37. Wong CE, Yu JS, Quigley DA, et al. Inflammation and Hras signaling control epithelial–mesenchymal transition during skin tumor progression. Genes Dev 2013; 27: 670-682.
38. Song IY, Balmain A. Cellular reprogramming in skin cancer. Semin Cancer Biol 2014.
39. INK4b in undifferentiated mouse skin tumors. Cancer Res 1995; 55: 5168-5172.
40. Pons M, Cigudosa JC, Rodriguez-Perales S, et al. Chromosomal instability and phenotypic plasticity during the squamous–spindle carcinoma transition: association of a specific T(14;15) with malignant progression. Oncogene 2005; 24: 7608-7618.
41. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006; 126: 663-676.
42. Li H, Collado M, Villasante A, et al. The Ink4/Arf locus is a barrier for iPS cell reprogramming. Nature 2009; 460: 1136-1139.
43. Thiery JP. Epithelial–mesenchymal transitions in tumour progression. Nature Rev Cancer 2002; 2: 442-454.
44. Hollmig ST, Sachdev R, Cockerell CJ, et al. Spindle cell neoplasms encountered in dermatologic surgery: a review. Dermatol Surg 2012; 38: 825-850.
45. Küsters-Vandevelde HVN, Van Leeuwen A, Verdijk MAJ, et al. CDKN2A but not TP53 mutations nor HPV presence predict poor outcome in metastatic squamous cell carcinoma of the skin. Int J Cancer 2010; 126: 2123-2132.