194
Views
9
CrossRef citations to date
0
Altmetric
Research Article

Chronic low dose UV exposure and p53 mutation: Tilting the odds in early epidermal preneoplasia?

&
Pages 682-687 | Received 27 Feb 2012, Accepted 30 May 2012, Published online: 23 Aug 2012

References

  • Allen TD, Potten CS. 1974. Fine-structural identification and organization of the epidermal proliferative unit. Journal of Cell Science 15:291–319.
  • Allen TD, Potten CS. 1976. Ultrastructural site variations in mouse epidermal organization. Journal of Cell Science 21:341–359.
  • Berg RJ, van Kranen HJ, Rebel HG, de Vries A, van Vloten WA, Van Kreijl CF, van der Leun JC, de Gruijl FR. 1996. Early p53 alterations in mouse skin carcinogenesis by UVB radiation: Immunohistochemical detection of mutant p53 protein in clusters of preneoplastic epidermal cells. Proceedings of the National Academy of Sciences of the USA 93:274–278.
  • Brash D, Cairns J. 2009. The mysterious steps in carcinogenesis: Addendum. British Journal of Cancer 101:1490.
  • Brash DE, Rudolph JA, Simon JA, Lin A, McKenna GJ, Baden HP, Halperin AJ, Ponten J. 1991. A role for sunlight in skin cancer: UV-induced p53 mutations in squamous cell carcinoma. Proceedings of the National Academy of Sciences of the USA 88:10124–10128.
  • Braun KM, Watt FM. 2004. Epidermal label-retaining cells: Background and recent applications. Journal of Investigative Dermatology Symposium Proceedings 9:196–201.
  • Braun KM, Niemann C, Jensen UB, Sundberg JP, Silva-Vargas V, Watt FM. 2003. Manipulation of stem cell proliferation and lineage commitment: Visualisation of label-retaining cells in wholemounts of mouse epidermis. Development 130:5241–5255.
  • Cairns J. 1975. Mutation selection and the natural history of cancer. Nature 255:197–200.
  • Caulin C, Nguyen T, Lang GA, Goepfert TM, Brinkley BR, Cai WW, Lozano G, Roop DR. 2007. An inducible mouse model for skin cancer reveals distinct roles for gain- and loss-of-function p53 mutations. Journal of Clinical Investigation 117:1893–1901.
  • Chao DL, Eck JT, Brash DE, Maley CC, Luebeck EG. 2008. Preneoplastic lesion growth driven by the death of adjacent normal stem cells. Proceedings of the National Academy of Sciences of the USA 105:15034–15039.
  • Clayton E, Doupe DP, Klein AM, Winton DJ, Simons BD, Jones PH. 2007. A single type of progenitor cell maintains normal epidermis. Nature 446:185–189.
  • de Gruijl FR. 2008. UV-induced immunosuppression in the balance. Photochemistry and Photobiology 84:2–9.
  • de Gruijl FR, Rebel H. 2008. Early events in UV carcinogenesis – DNA damage, target cells and mutant p53 foci. Photochemistry and Photobiology 84:382–387.
  • Doherty VR, Brewster DH, Jensen S, Gorman D. 2010. Trends in skin cancer incidence by socioeconomic position in Scotland, 1978–2004. British Journal of Cancer 102:1661–1664.
  • Doupe D, Jones PH. 2012. Interfollicular homeostasis: Dicing with differentiation. Experimental Dermatology 21:249–253.
  • Doupe DP, Klein AM, Simons BD, Jones PH. 2010. The ordered architecture of murine ear epidermis is maintained by progenitor cells with random fate. Developmental Cell 18:317–323.
  • Ghazizadeh S, Taichman LB. 2001. Multiple classes of stem cells in cutaneous epithelium: A lineage analysis of adult mouse skin. The EMBO Journal 20:1215–1222.
  • Goh AM, Coffill CR, Lane DP. 2011. The role of mutant p53 in human cancer. Journal of Pathology 223:116–126.
  • Gonzalez KD, Noltner KA, Buzin CH, Gu D, Wen-Fong CY, Nguyen VQ, Han JH, Lowstuter K, Longmate J, Sommer SS, . 2009. Beyond Li Fraumeni Syndrome: Clinical characteristics of families with p53 germline mutations. Journal of Clinical Oncology 27:1250–1256.
  • Greaves M, Maley CC. 2012. Clonal evolution in cancer. Nature 481: 306–313.
  • Honda H, Tanemura M, Imayama S. 1996. Spontaneous architectural organization of mammalian epidermis from random cell packing. Journal of Investigative Dermatology 106:312–315.
  • Ito M, Liu Y, Yang Z, Nguyen J, Liang F, Morris RJ, Cotsarelis G. 2005. Stem cells in the hair follicle bulge contribute to wound repair but not to homeostasis of the epidermis. Nature Medicine 11: 1351–1354.
  • Jiang W, Ananthaswamy HN, Muller HK, Kripke ML. 1999. p53 protects against skin cancer induction by UV-B radiation. Oncogene 18:4247–4253.
  • 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. Proceedings of the National Academy of Sciences of the USA 93:14025–14029.
  • Jones P, Simons BD. 2008. Epidermal homeostasis: Do committed progenitors work while stem cells sleep?Nature Reviews Molecular and Cell Biology 9:82–88.
  • Jones PH, Simons BD, Watt FM. 2007. Sic Transit Gloria: Farewell to the epidermal transit amplifying cell?Cell Stem Cell 1:371–381.
  • Kameda T, Nakata A, Mizutani T, Terada K, Iba H, Sugiyama T. 2003. Analysis of the cellular heterogeneity in the basal layer of mouse ear epidermis: An approach from partial decomposition in vitro and retroviral cell marking in vivo. Experimental Cell Research 283: 167–183.
  • Klein AM, Simons BD. 2011. Universal patterns of stem cell fate in cycling adult tissues. Development 138:3103–3111.
  • Klein AM, Doupe DP, Jones PH, Simons BD. 2007. Kinetics of cell division in epidermal maintenance. Physical Review E Statistical Nonlinear and Soft Matter Physics 76:021910.
  • Klein AM, Doupe DP, Jones PH, Simons BD. 2008. Mechanism of murine epidermal maintenance: Cell division and the voter model. Physical Review E Statistical Nonlinear and Soft Matter Physics 77:031907.
  • Klein AM, Brash DE, Jones PH, Simons BD. 2010. Stochastic fate of p53-mutant epidermal progenitor cells is tilted toward proliferation by UV B during preneoplasia. Proceedings of the National Academy of Sciences of the USA 107:270–275.
  • Levy V, Lindon C, Harfe BD, Morgan BA. 2005. Distinct stem cell populations regenerate the follicle and interfollicular epidermis. Developmental Cell 9:855–861.
  • Ling G, Persson A, Berne B, Uhlen M, Lundeberg J, Ponten F. 2001. Persistent p53 mutations in single cells from normal human skin. American Journal of Pathology 159:1247–1253.
  • Mackenzie IC. 1970. Relationship between mitosis and the ordered structure of the stratum corneum in mouse epidermis. Nature 226:653–655.
  • Marin MC, Jost CA, Brooks LA, Irwin MS, O’Nions J, Tidy JA, James N, McGregor JM, Harwood CA, Yulug IG, . 2000. A common polymorphism acts as an intragenic modifier of mutant p53 behaviour. Nature Genetics 25:47–54.
  • Menton DN. 1976a. A liquid film model of tetrakaidecahedral packing to account for the establishment of epidermal cell columns. Journal of Investigative Dermatology 66:283–291.
  • Menton DN. 1976b. A minimum-surface mechanism to account for the organization of cells into columns in the mammalian epidermis. American Journal of Anatomy 145:1–22.
  • Moles JP, Theillet C, Basset-Seguin N, Guilhou JJ. 1993. Mutation of the tumor suppressor gene TP53 is not detected in psoriatic skin. Journal of Investigative Dermatology 101:100–102.
  • Mosterd K, Krekels GA, Nieman FH, Ostertag JU, Essers BA, Dirksen CD, Steijlen PM, Vermeulen A, Neumann H, Kelleners-Smeets NW. 2008. Surgical excision versus Mohs’ micrographic surgery for primary and recurrent basal-cell carcinoma of the face: A prospective randomised controlled trial with 5-years’ follow-up. Lancet Oncology 9:1149–1156.
  • Nowell PC. 1976. The clonal evolution of tumor cell populations. Science 194:23–28.
  • Petitjean A, Achatz MI, Borresen-Dale AL, Hainaut P, Olivier M. 2007. TP53 mutations in human cancers: Functional selection and impact on cancer prognosis and outcomes. Oncogene 26:2157–2165.
  • Pfeifer GP, Besaratinia A. 2009. Mutational spectra of human cancer. Human Genetics 125:493–506.
  • Pierceall WE, Mukhopadhyay T, Goldberg LH, Ananthaswamy HN. 1991. Mutations in the p53 tumor suppressor gene in human cutaneous squamous cell carcinomas. Molecular Carcinogenesis 4:445–449.
  • Potten CS. 1974. The epidermal proliferative unit: The possible role of the central basal cell. Cell and Tissue Kinetics 7:77–88.
  • Potten CS. 1981. Cell replacement in epidermis (keratopoiesis) via discrete units of proliferation. International Review of Cytology 69:271–318.
  • Ratushny V, Gober MD, Hick R, Ridky TW, Seykora JT. 2012. From keratinocyte to cancer: The pathogenesis and modeling of cutaneous squamous cell carcinoma. Journal of Clinical Investigation 122: 464–472.
  • Rebel H, Kram N, Westerman A, Banus S, van Kranen HJ, de Gruijl FR. 2005. Relationship between UV-induced mutant p53 patches and skin tumours, analysed by mutation spectra and by induction kinetics in various DNA-repair-deficient mice. Carcinogenesis 26: 2123–2130.
  • Rebel H, Mosnier LO, Berg RJ, Westerman-de Vries A, van Steeg H, van Kranen HJ, de Gruijl FR. 2001. Early p53-positive foci as indicators of tumor risk in ultraviolet-exposed hairless mice: Kinetics of induction, effects of DNA repair deficiency, and p53 heterozygosity. Cancer Research 61:977–983.
  • Rebel HG, Bodmann CA, van de Glind GC, de Gruijl FR. 2012. UV-induced ablation of the epidermal basal layer including p53-mutant clones resets UV carcinogenesis showing squamous cell carcinomas to originate from interfollicular epidermis. Carcinogenesis 33:714–720.
  • Remenyik E, Wikonkal NM, Zhang W, Paliwal V, Brash DE. 2003. Antigen-specific immunity does not mediate acute regression of UVB-induced p53-mutant clones. Oncogene 22:6369–6376.
  • Ren ZP, Hedrum A, Ponten F, Nister M, Ahmadian A, Lundeberg J, Uhlen M, Ponten J. 1996. Human epidermal cancer and accompanying precursors have identical p53 mutations different from p53 mutations in adjacent areas of clonally expanded non-neoplastic keratinocytes. Oncogene 12:765–773.
  • Ren ZP, Ahmadian A, Ponten F, Nister M, Berg C, Lundeberg J, Uhlen M, Ponten J. 1997. Benign clonal keratinocyte patches with p53 mutations show no genetic link to synchronous squamous cell precancer or cancer in human skin. American Journal of Pathology 150:1791–1803.
  • Ro S, Rannala B. 2004. A stop-EGFP transgenic mouse to detect clonal cell lineages generated by mutation. EMBO Reports 5: 914–920.
  • Ro S, Rannala B. 2005. Evidence from the stop-EGFP mouse supports a niche-sharing model of epidermal proliferative units. Experimental Dermatology 14:838–843.
  • Schmidt GH, Blount MA, Ponder BA 1987. Immunochemical demonstration of the clonal organization of chimaeric mouse epidermis. Development 100:535–541.
  • Stahl PL, Stranneheim H, Asplund A, Berglund L, Ponten F, Lundeberg J. 2011. Sun-induced nonsynonymous p53 mutations are extensively accumulated and tolerated in normal appearing human skin. Journal of Investigative Dermatology 131:504–508.
  • Stang A, Stausberg J, Boedeker W, Kerek-Bodden H, Jockel KH. 2008. Nationwide hospitalization costs of skin melanoma and non- melanoma skin cancer in Germany. Journal of the European Academy of Dermatology and Venereology 22:65–72.
  • Stout GJ, Westdijk D, Calkhoven DM, Pijper O, Backendorf CM, Willemze R, Mullenders LH, de Gruijl FR 2005. Epidermal transit of replication-arrested, undifferentiated keratinocytes in UV-exposed XPC mice: An alternative to in situ apoptosis. Proceedings of the National Academy of Sciences of the USA 102:18980–18985.
  • Torchia EC, Caulin C, Acin S, Terzian T, Kubick BJ, Box NF, Roop DR. 2012. Myc, Aurora Kinase A, and mutant p53(R172H) co-operate in a mouse model of metastatic skin carcinoma. Oncogene 31: 2680–2690.
  • Wijnhoven SW, Speksnijder EN, Liu X, Zwart E, vanOostrom CT, Beems RB, Hoogervorst EM, Schaap MM, Attardi LD, Jacks T, . 2007. Dominant-negative but not gain-of-function effects of a p53.R270H mutation in mouse epithelium tissue after DNA damage. Cancer Research 67:4648–4656.
  • Zhang W, Remenyik E, Zelterman D, Brash DE, Wikonkal NM. 2001. Escaping the stem cell compartment: Sustained UVB exposure allows p53-mutant keratinocytes to colonize adjacent epidermal proliferating units without incurring additional mutations. Proceedings of the National Academy of Sciences of the USA 98:13948–13953.
  • Zhang W, Hanks AN, Boucher K, Florell SR, Allen SM, Alexander A, Brash DE, Grossman D. 2005. UVB-induced apoptosis drives clonal expansion during skin tumor development. Carcinogenesis 26:249–257.
  • Ziegler A, Jonason AS, Leffell DJ, Simon JA, Sharma HW, Kimmelman J, Remington L, Jacks T, Brash DE. 1994. Sunburn and p53 in the onset of skin cancer. Nature 372:773–776.
  • Ziegler A, Leffell DJ, Kunala S, Sharma HW, Gailani M, Simon JA, Halperin AJ, Baden HP, Shapiro PE, Bale AE, . 1993. Mutation hotspots due to sunlight in the p53 gene of nonmelanoma skin cancers. Proceedings of the National Academy of Sciences of the USA 90:4216–4220.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.