Cellular reprogramming in skin cancer

Seminars in Cancer Biology

Volumn 32, Issue , 2015, Pages 32-39

  Song, Ihn Young ^a   Balmain, Allan ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cell of origin; Inflammation; Malignant potential; P53; Reprogramming; Skin cancer; Stem cell hierarchy

Indexed keywords

PROTEIN P53;

CANCER CLASSIFICATION; HUMAN; INFLAMMATION; MALIGNANT TRANSFORMATION; NONHUMAN; NUCLEAR REPROGRAMMING; PROTEIN FUNCTION; REVIEW; SKIN CANCER; SKIN CARCINOGENESIS; STEM CELL NICHE; TUMOR MICROENVIRONMENT; TUMOR PROMOTION; ANIMAL; CANCER STEM CELL; CARCINOGENESIS; CELL DIFFERENTIATION; CELL TRANSFORMATION; GENETICS; MOUSE; ONCOGENE; SKIN TUMOR;

ANIMALS; CARCINOGENESIS; CELL DIFFERENTIATION; CELL TRANSFORMATION, NEOPLASTIC; CELLULAR REPROGRAMMING; HUMANS; INFLAMMATION; MICE; NEOPLASTIC STEM CELLS; ONCOGENES; SKIN NEOPLASMS;

EID: 84929954368     PISSN: 1044579X     EISSN: 10963650     Source Type: Journal    
DOI: 10.1016/j.semcancer.2014.03.006     Document Type: Review

References (85)

1. Perez-Losada J., Balmain A. Stem-cell hierarchy in skin cancer. Nat Rev Cancer 2003, 434-443.
2. Takahashi K., Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006, 663-676.
3. Egli D., Birkhoff G., Eggan K. Mediators of reprogramming: transcription factors and transitions through mitosis. Nat Rev Mol Cell Biol 2008, 505-516.
4. Hanna J., Carey B.W., Jaenisch R. Reprogramming of somatic cell identity. Cold Spring Harb Symp Quant Biol 2008, 147-155.
5. Buczacki S.J.A., Zecchini H.I., Nicholson A.M., Russell R., Vermeulen L., Kemp R., et al. Intestinal label-retaining cells are secretory precursors expressing Lgr5. Nature 2013, 65-69.
6. Yan K.S., Chia L.A., Li X., Ootani A., Su J., Lee J.Y., et al. The intestinal stem cell markers Bmi1 and Lgr5 identify two functionally distinct populations. Proc Natl Acad Sci U S A 2012, 466-471.
7. Tata P.R., Mou H., Pardo-Saganta A., Zhao R., Prabhu M., Law B.M., et al. Dedifferentiation of committed epithelial cells into stem cells in vivo. Nature 2013, 218-223.
8. Schwitalla S., Fingerle A.A., Cammareri P., Nebelsiek T., Göktuna S.I., Ziegler P.K., et al. Intestinal tumorigenesis initiated by dedifferentiation and acquisition of stem-cell-like properties. Cell 2013, 25-38.
9. Friedmann-Morvinski D., Bushong E.A., Ke E., Soda Y., Marumoto T., Singer O., et al. Dedifferentiation of neurons and astrocytes by oncogenes can induce gliomas in mice. Science 2012, 1080-1084.
10. Brown K., Strathdee D., Bryson S., Lambie W., Balmain A. The malignant capacity of skin tumours induced by expression of a mutant H-ras transgene depends on the cell type targeted. Curr Biol 1998, 516-524.
11. Wong C.E., Yu J.S., Quigley D.A., To M.D., Jen K.-Y., Huang P.Y., et al. Inflammation and Hras signaling control epithelial-mesenchymal transition during skin tumor progression. Genes Dev 2013, 670-682.
12. Hanahan D., Weinberg R.A. Hallmarks of cancer: the next generation. Cell 2011, 646-674.
13. Colotta F., Allavena P., Sica A., Garlanda C., Mantovani A. Cancer-related inflammation, the seventh hallmark of cancer: links to genetic instability. Carcinogenesis 2009, 1073-1081.
14. Virchow R. An address on the value of pathological experiments. Br Med J 1881, 198-203.
15. Elinav E., Nowarski R., Thaiss C.A., Hu B., Jin C., Flavell R.A. Inflammation-induced cancer: crosstalk between tumours, immune cells and microorganisms 2013, 759-771. Nature Publishing Group.
16. Balkwill F.R., Mantovani A. Cancer-related inflammation: common themes and therapeutic opportunities. Semin Cancer Biol 2012, 33-40.
17. Gonda T.A., Tu S., Wang T.C. Chronic inflammation, the tumor microenvironment and carcinogenesis. Cell Cycle 2009, 2005-2013.
18. Mantovani A., Allavena P., Sica A., Balkwill F. Cancer-related inflammation. Nature 2008, 436-444.
19. Klein-Szanto A.J., Larcher F., Bonfil R.D., Conti C.J. Multistage chemical carcinogenesis protocols produce spindle cell carcinomas of the mouse skin. Carcinogenesis 1989, 2169-2172.
20. Quintanilla M., Brown K., Ramsden M., Balmain A. Carcinogen-specific mutation and amplification of Ha-ras during mouse skin carcinogenesis. Nature 1986, 78-80.
21. Balmain A., Ramsden M., Bowden G.T., Smith J. Activation of the mouse cellular Harvey-ras gene in chemically induced benign skin papillomas. Nature 1984, 658-660.
22. Balmain A., Pragnell I.B. Mouse skin carcinomas induced in vivo by chemical carcinogens have a transforming Harvey-ras oncogene. Nature 1983, 72-74.
23. Viaje A., Slaga T.J., Wigler M., Weinstein I.B. Effects of antiinflammatory agents on mouse skin tumor promotion, epidermal DNA synthesis, phorbol ester-induced cellular proliferation, and production of plasminogen activator. Cancer Res 1977, 1530-1536.
24. Verma A.K., Boutwell R.K. Effects of dose and duration of treatment with the tumor-promoting agent, 12-O-tetradecanoylphorbol-13-acetate on mouse skin carcinogenesis. Carcinogenesis 1980, 271-276.
25. Hensler S., Mueller M.M. Inflammation and skin cancer: old pals telling new stories. Cancer J 2013, 517-524.
26. Hansen L.A., Monteiro-Riviere N.A., Smart R.C. Differential down-regulation of epidermal protein kinase C by 12-O-tetradecanoylphorbol-13-acetate and diacylglycerol: association with epidermal hyperplasia and tumor promotion. Cancer Res 1990, 5740-5745.
27. Fournier A., Murray A.W. Application of phorbol ester to mouse skin causes a rapid and sustained loss of protein kinase C. Nature 1987, 767-769.
28. Castagna M., Takai Y., Kaibuchi K., Sano K., Kikkawa U., Nishizuka Y. Direct activation of calcium-activated, phospholipid-dependent protein kinase by tumor-promoting phorbol esters. J Biol Chem 1982, 7847-7851.
29. Akhurst R.J., FEE F., Balmain A. Localized production of TGF-beta mRNA in tumour promoter-stimulated mouse epidermis. Nature 1988, 363-365.
30. Fürstenberger G., Rogers M., Schnapke R., Bauer G., Höfler P., Marks F. Stimulatory role of transforming growth factors in multistage skin carcinogenesis: possible explanation for the tumor-inducing effect of wounding in initiated NMRI mouse skin. Int J Cancer 1989, 915-921.
31. Fürstenberger G., Richter H., Argyris T.S., Marks F. Effects of the phorbol ester 4-O-methyl-12-O-tetradecanoylphorbol-13-acetate on mouse skin in vivo: evidence for its uselessness as a negative control compound in studies on the biological effects of phorbol ester tumor promoters. Cancer Res 1982, 342-348.
32. Yamasaki H., Aguelon-Pegouries A.M., Enomoto T., Martel N., Furstenberger G., Marks F. Comparative effects of a complete tumor promoter, TPA, and a second-stage tumor promoter, RPA, on intercellular communication, cell differentiation and cell transformation. Carcinogenesis 1985, 1173-1179.
33. Prat A., Parker J.S., Karginova O., Fan C., Livasy C., Herschkowitz J.I., et al. Phenotypic and molecular characterization of the claudin-low intrinsic subtype of breast cancer. Breast Cancer Res 2010, pR68.
34. De Craene B., Berx G. Regulatory networks defining EMT during cancer initiation and progression. Nat Rev Cancer 2013, 97-110.
35. Li H., Collado M., Villasante A., Strati K., Ortega S., Cañamero M., et al. The Ink4/Arf locus is a barrier for iPS cell reprogramming. Nature 2009, 1136-1139.
36. Molofsky A.V., Pardal R., Iwashita T., Park I.-K., Clarke M.F., Morrison S.J. Bmi-1 dependence distinguishes neural stem cell self-renewal from progenitor proliferation. Nature 2003, 962-967.
37. Park I.-K., Qian D., Kiel M., Becker M.W., Pihalja M., Weissman I.L., et al. Bmi-1 is required for maintenance of adult self-renewing haematopoietic stem cells. Nature 2003, 302-305.
38. Hennings H., Shores R., Mitchell P., Spangler E.F., Yuspa S.H. Induction of papillomas with a high probability of conversion to malignancy. Carcinogenesis 1985, 1607-1610.
39. Bailleul B., Surani M.A., White S., Barton S.C., Brown K., Blessing M., et al. Skin hyperkeratosis and papilloma formation in transgenic mice expressing a ras oncogene from a suprabasal keratin promoter. Cell 1990, 697-708.
40. Greenhalgh D.A., Rothnagel J.A., Quintanilla M.I., Orengo C.C., Gagne T.A., Bundman D.S., et al. Induction of epidermal hyperplasia, hyperkeratosis, and papillomas in transgenic mice by a targeted v-Ha-ras oncogene. Mol Carcinog 1993, 99-110.
41. Caulin C., Nguyen T., Longley M.A., Zhou Z., Wang X.-J., Roop D.R. Inducible activation of oncogenic K-ras results in tumor formation in the oral cavity. Cancer Res 2004, 5054-5058.
42. Caulin C., Nguyen T., Lang G.A., Goepfert T.M., Brinkley B.R., Cai W.-W., et al. An inducible mouse model for skin cancer reveals distinct roles for gain- and loss-of-function p53 mutations. J Clin Investig 2007, 1893-1901.
43. White A.C., Tran K., Khuu J., Dang C., Cui Y., Binder S.W., et al. Defining the origins of Ras/p53-mediated squamous cell carcinoma. Proc Natl Acad Sci U S A 2011, 7425-7430.
44. Lapouge G., Youssef K.K., Vokaer B., Achouri Y., Michaux C., Sotiropoulou P.A., et al. Identifying the cellular origin of squamous skin tumors. Proc Natl Acad Sci U S A 2011, 7431-7436.
45. Page M.E., Lombard P., Ng F., Göttgens B., Jensen K.B. The epidermis comprises autonomous compartments maintained by distinct stem cell populations. Cell Stem Cell 2013, 471-482.
46. Wang G.Y., Wang J., Mancianti M.-L., Epstein E.H. Basal cell carcinomas arise from hair follicle stem cells in Ptch1(+/-) mice. Cancer Cell 2011, 114-124.
47. Youssef K.K., Van Keymeulen A., Lapouge G., Beck B., Michaux C., Achouri Y., et al. Identification of the cell lineage at the origin of basal cell carcinoma. Nat Cell Biol 2010, 299-305.
48. Grachtchouk M., Pero J., Yang S.H., Ermilov A.N., Michael L.E., Wang A., et al. Basal cell carcinomas in mice arise from hair follicle stem cells and multiple epithelial progenitor populations. J Clin Investig 2011, 1768-1781.
49. Dejosez M., Ura H., Brandt V.L., Zwaka T.P. Safeguards for cell cooperation in mouse embryogenesis shown by genome-wide cheater screen. Science 2013, 1511-1514.
50. Bondar T., Medzhitov R. p53-mediated hematopoietic stem and progenitor cell competition. Cell Stem Cell 2010, 309-322.
51. Vermeulen L., Morrissey E., van der Heijden M., Nicholson A.M., Sottoriva A., Buczacki S., et al. Defining stem cell dynamics in models of intestinal tumor initiation. Science 2013, 995-998.
52. Li S., Park H., Trempus C.S., Gordon D., Liu Y., Cotsarelis G., et al. A keratin 15 containing stem cell population from the hair follicle contributes to squamous papilloma development in the mouse. Mol Carcinog 2013, 751-759.
53. Andl T., Reddy S.T., Gaddapara T., Millar S.E. WNT signals are required for the initiation of hair follicle development. Dev Cell 2002, 643-653.
54. Watt F.M., Jensen K.B. Epidermal stem cell diversity and quiescence. EMBO Mol Med 2009, 260-267.
55. Zhang Y., Andl T., Yang S.H., Teta M., Liu F., Seykora J.T., et al. Activation of beta-catenin signaling programs embryonic epidermis to hair follicle fate. Development 2008, 2161-2172.
56. Richardson G.D., Bazzi H., Fantauzzo K.A., Waters J.M., Crawford H., Hynd P., et al. KGF and EGF signalling block hair follicle induction and promote interfollicular epidermal fate in developing mouse skin. Development 2009, 2153-2164.
57. Davidson E.H. Emerging properties of animal gene regulatory networks. Nature 2010, 911-920.
58. Varjosalo M., Taipale J. Hedgehog: functions and mechanisms. Genes Dev 2008, 2454-2472.
59. Nitzki F., Becker M., Frommhold A., Schulz-Schaeffer W., Hahn H. Patched knockout mouse models of Basal cell carcinoma. J Skin Cancer 2012, p907543.
60. Wakabayashi Y., Mao J.-H., Brown K., Girardi M., Balmain A. Promotion of Hras-induced squamous carcinomas by a polymorphic variant of the Patched gene in FVB mice. Nature 2007, 761-765.
61. Kang H.C., Wakabayashi Y., Jen K.-Y., Mao J.-H., Zoumpourlis V., Del Rosario R., et al. Ptch1 overexpression drives skin carcinogenesis and developmental defects in K14Ptch(FVB) mice. J Invest Dermatol 2012.
62. Vicente-Dueñas C., Romero-Camarero I., Cobaleda C., Sánchez-García I. Function of oncogenes in cancer development: a changing paradigm. EMBO J 2013, 1502-1513.
63. Bremner R., Balmain A. Genetic changes in skin tumor progression: correlation between presence of a mutant ras gene and loss of heterozygosity on mouse chromosome 7. Cell 1990, 407-417.
64. Kemp C.J., Donehower L.A., Bradley A., Balmain A. Reduction of p53 gene dosage does not increase initiation or promotion but enhances malignant progression of chemically induced skin tumors. Cell 1993, 813-822.
65. Meletis K., Wirta V., Hede S.-M., Nistér M., Lundeberg J., Frisén J. p53 suppresses the self-renewal of adult neural stem cells. Development 2006, 363-369.
66. Tao L., Roberts A.L., Dunphy K.A., Bigelow C., Yan H., Jerry D.J. Repression of mammary stem/progenitor cells by p53 is mediated by Notch and separable from apoptotic activity. Stem Cell 2011, 119-127.
67. Cicalese A., Bonizzi G., Pasi C.E., Faretta M., Ronzoni S., Giulini B., et al. The tumor suppressor p53 regulates polarity of self-renewing divisions in mammary stem cells. Cell 2009, 1083-1095.
68. Zhao Z., Zuber J., Diaz-Flores E., Lintault L., Kogan S.C., Shannon K., et al. p53 loss promotes acute myeloid leukemia by enabling aberrant self-renewal. Genes Dev 2010, 1389-1402.
69. Lin T., Chao C., Saito S.i., Mazur S.J., Murphy M.E., Appella E., et al. p53 induces differentiation of mouse embryonic stem cells by suppressing Nanog expression. Nat Cell Biol 2005, 165-171.
70. Morrison S.J., Kimble J. Asymmetric and symmetric stem-cell divisions in development and cancer. Nature 2006, 1068-1074.
71. Kawamura T., Suzuki J., Wang Y.V., Menendez S., Morera L.B., Raya A., et al. Linking the p53 tumour suppressor pathway to somatic cell reprogramming. Nature 2009, 1140-1144.
72. Marión R.M., Strati K., Li H., Murga M., Blanco R., Ortega S., et al. A p53-mediated DNA damage response limits reprogramming to ensure iPS cell genomic integrity. Nature 2009, 1149-1153.
73. Tanabe K., Nakamura M., Narita M., Takahashi K., Yamanaka S. Maturation, not initiation, is the major roadblock during reprogramming toward pluripotency from human fibroblasts. Proc Natl Acad Sci U S A 2013, 12172-12179.
74. Hong H., Takahashi K., Ichisaka T., Aoi T., Kanagawa O., Nakagawa M., et al. Suppression of induced pluripotent stem cell generation by the p53-p21 pathway. Nature 2009, 1132-1135.
75. Hünten S., Siemens H., Kaller M., Hermeking H. The p53/microRNA network in cancer: experimental and bioinformatics approaches. Adv Exp Med Biol 2013, 77-101.
76. Lin C.-P., Choi Y.J., Hicks G.G., He L. The emerging functions of the p53-miRNA network in stem cell biology. Cell Cycle 2012, 2063-2072.
77. Choi Y.J., Lin C.-P., Ho J.J., He X., Okada N., Bu P., et al. miR-34 miRNAs provide a barrier for somatic cell reprogramming. Nat Cell Biol 2011, 1353-1360.
78. Chang T.-C., Wentzel E.A., Kent O.A., Ramachandran K., Mullendore M., Lee K.H., et al. Transactivation of miR-34a by p53 broadly influences gene expression and promotes apoptosis. Mol Cell 2007, 745-752.
79. Kim N.H., Kim H.S., Kim N.-G., Lee I., Choi H.-S., Li X.-Y., et al. p53 and microRNA-34 are suppressors of canonical Wnt signaling. Sci Signal 2011, pra71.
80. Fiucci G., Beaucourt S., Duflaut D., Lespagnol A., Stumptner-Cuvelette P., Géant A., et al. Siah-1b is a direct transcriptional target of p53: identification of the functional p53 responsive element in the siah-1b promoter. Proc Natl Acad Sci U S A 2004, 3510-3515.
81. Iwai A., Marusawa H., Matsuzawa S.-i., Fukushima T., Hijikata M., Reed J.C., et al. Siah-1L, a novel transcript variant belonging to the human Siah family of proteins, regulates beta-catenin activity in a p53-dependent manner. Oncogene 2004, 7593-7600.
82. Lee K.-H., Li M., Michalowski A.M., Zhang X., Liao H., Chen L., et al. A genomewide study identifies the Wnt signaling pathway as a major target of p53 in murine embryonic stem cells. Proc Natl Acad Sci U S A 2010, 69-74.
83. He X.C., Zhang J., Tong W.-G., Tawfik O., Ross J., Scoville D.H., et al. BMP signaling inhibits intestinal stem cell self-renewal through suppression of Wnt-beta-catenin signaling. Nat Genet 2004, 1117-1121.
84. Reya T., Duncan A.W., Ailles L., Domen J., Scherer D.C., Willert K., et al. A role for Wnt signalling in self-renewal of haematopoietic stem cells. Nature 2003, 409-414.
85. Lapouge G., Beck B., Nassar D., Dubois C., Dekoninck S., Blanpain C. Skin squamous cell carcinoma propagating cells increase with tumour progression and invasiveness. EMBO J 2012, 4563-4575.