Progeny of Lgr5-expressing hair follicle stem cell contributes to papillomavirus-induced tumor development in epidermis

Oncogene

Volumn 32, Issue 32, 2013, Pages 3732-3743

  Da Silva Diz, V ^a   Sole Sanchez S ^a   Valdes Gutierrez A ^a   Urpi M ^a   Riba Artes D ^a   Penin, R M ^b   Pascual, G ^c   Gonzalez Suarez E ^a   Casanovas, O ^d   Vinals F ^d,e   Paramio, J M ^f   Batlle, E ^g   Munoz P ^a  

^a BELLVITGE BIOMEDICAL RESEARCH INSTITUTE IDIBELL   (Spain)

^b HOSPITAL UNIVERSITARI DE BELLVITGE   (Spain)

^c Barcelona Biomedical Research Park   (Spain)

^d CATALAN INSTITUTE OF ONCOLOGY   (Spain)

^e UNIVERSITY OF BARCELONA   (Spain)

^f Molecular Oncology Unit   (Spain)

^g INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Spain)

Author keywords

carcinogenesis mouse models; cell lineage tracing; hair follicle stem cells; papillomavirus; squamous cell carcinoma

Indexed keywords

CYTOKERATIN 15; G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR 5; P CADHERIN; PROTEIN E6; PROTEIN E7; TRANSCRIPTION FACTOR 7 LIKE 1; TRANSCRIPTION FACTOR SOX9; UNCLASSIFIED DRUG;

ARTICLE; CELL LINEAGE; CONTROLLED STUDY; EPIDERMIS; HAIR FOLLICLE; HUMAN PAPILLOMAVIRUS TYPE 16; IMMOBILIZED CELL; KERATINOCYTE; MOUSE; NONHUMAN; PAPILLOMA VIRUS; PRIORITY JOURNAL; PROGENY; SKIN CARCINOGENESIS; SKIN CARCINOMA; SQUAMOUS CELL CARCINOMA; STEM CELL;

ANIMALS; ANTIGENS, CD34; CARCINOMA, SQUAMOUS CELL; CELL MOVEMENT; EPIDERMIS; HAIR FOLLICLE; KERATIN-15; MICE; ONCOGENE PROTEINS, VIRAL; PAPILLOMAVIRIDAE; PAPILLOMAVIRUS E7 PROTEINS; RECEPTORS, G-PROTEIN-COUPLED; REPRESSOR PROTEINS; SKIN NEOPLASMS; STEM CELLS;

HUMAN PAPILLOMAVIRUS; HUMAN PAPILLOMAVIRUS - 16; HUMAN PAPILLOMAVIRUS TYPE 16; PAPILLOMAVIRIDAE;

EID: 84881476621     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2012.375     Document Type: Article

References (57)

1. Blanpain C, Fuchs E. Epidermal homeostasis: a balancing act of stem cells in the skin. Nat Rev Mol Cell Biol 2009; 10: 207-217.
2. Watt FM, Jensen KB. Epidermal stem cell diversity and quiescence. EMBO Mol Med 2009; 1: 260-267.
3. Petersson M, Brylka H, Kraus A, John S, Rappl G, Schettina P et al. TCF/Lef1 activity controls establishment of diverse stem and progenitor cell compartments in mouse epidermis. Embo J 2011; 30: 3004-3018.
4. Merrill BJ, Gat U, DasGupta R, Fuchs E. Tcf3 and Lef1 regulate lineage differentiation of multipotent stem cells in skin. Genes Dev 2001; 15: 1688-1705.
5. Trempus CS, Morris RJ, Bortner CD, Cotsarelis G, Faircloth RS, Reece JM et al. Enrichment for living murine keratinocytes from the hair follicle bulge with the cell surface marker CD34. J Invest Dermatol 2003; 120: 501-511.
6. Morris RJ, Liu Y, Marles L, Yang Z, Trempus C, Li S et al. Capturing and profiling adult hair follicle stem cells. Nat Biotechnol 2004; 22: 411-417.
7. Rhee H, Polak L, Fuchs E. Lhx2 maintains stem cell character in hair follicles. Science 2006; 312: 1946-1949.
8. Nowak JA, Polak L, Pasolli HA, Fuchs E. Hair follicle stem cells are specified and function in early skin morphogenesis. Cell Stem Cell 2008; 3: 33-43.
9. Jaks V, Barker N, Kasper M, van Es JH, Snippert HJ, Clevers H et al. Lgr5 marks cycling, yet long-lived, hair follicle stem cells. Nat Genet 2008; 40: 1291-1299.
10. Hsu YC, Pasolli HA, Fuchs E. Dynamics between stem cells, niche, and progeny in the hair follicle. Cell 2011; 144: 92-105.
11. Muller-Rover S, Tokura Y, Welker P, Furukawa F, Wakita H, Takigawa M et al. E-and P-cadherin expression during murine hair follicle morphogenesis and cycling. Exp Dermatol 1999; 8: 237-246.
12. Greco V, Chen T, Rendl M, Schober M, Pasolli HA, Stokes N et al. A two-step mechanism for stem cell activation during hair regeneration. Cell Stem Cell 2009; 4: 155-169.
13. Ito M, Liu Y, Yang Z, Nguyen J, Liang F, Morris RJ et al. Stem cells in the hair follicle bulge contribute to wound repair but not to homeostasis of the epidermis. Nat Med 2005; 11: 1351-1354.
14. Alam M, Ratner D. Cutaneous squamous-cell carcinoma. N Engl J Med 2001; 344: 975-983.
15. Schaper ID, Marcuzzi GP, Weissenborn SJ, Kasper HU, Dries V, Smyth N et al. Development of skin tumors in mice transgenic for early genes of human papillomavirus type 8. Cancer Res 2005; 65: 1394-1400.
16. Karagas MR, Nelson HH, Sehr P, Waterboer T, Stukel TA, Andrew A et al. Human papillomavirus infection and incidence of squamous cell and basal cell carcinomas of the skin. J Natl Cancer Inst 2006; 98: 389-395.
17. Ghittoni R, Accardi R, Hasan U, Gheit T, Sylla B, Tommasino M. The biological properties of E6 and E7 oncoproteins from human papillomaviruses. Virus Genes 2010; 40: 1-13.
18. zur Hausen H. Papillomaviruses in the causation of human cancers-a brief historical account. Virology 2009; 384: 260-265.
19. Hama N, Ohtsuka T, Yamazaki S. Detection of mucosal human papilloma virus DNA in bowenoid papulosis, Bowen's disease and squamous cell carcinoma of the skin. J Dermatol 2006; 33: 331-337.
20. Gormley RH, Groft CM, Miller CJ, Kovarik CL. Digital squamous cell carcinoma and association with diverse high-risk human papillomavirus types. J Am Acad Dermatol 2011; 64: 981-985.
21. Moody CA, Laimins LA. Human papillomavirus oncoproteins: pathways to transformation. Nat Rev Cancer 2010; 10: 550-560.
22. Arbeit JM, Munger K, Howley PM, Hanahan D. Progressive squamous epithelial neoplasia in K14-human papillomavirus type 16 transgenic mice. J Virol 1994; 68: 4358-4368.
23. Coussens LM, Hanahan D, Arbeit JM. Genetic predisposition and parameters of malignant progression in K14-HPV16 transgenic mice. Am J Pathol 1996; 149: 1899-1917.
24. Boccardo E, Lepique AP, Villa LL. The role of inflammation in HPV carcinogenesis. Carcinogenesis 2010; 31: 1905-1912.
25. Lapouge G, Youssef KK, Vokaer B, Achouri Y, Michaux C, Sotiropoulou PA et al. Identifying the cellular origin of squamous skin tumors. Proc Natl Acad Sci USA 2011; 108: 7431-7436.
26. White AC, Tran K, Khuu J, Dang C, Cui Y, Binder SW et al. Defining the origins of Ras/p53-mediated squamous cell carcinoma. Proc Natl Acad Sci USA 2011; 108: 7425-7430.
27. Boxman IL, Hogewoning A, Mulder LH, Bouwes Bavinck JN, ter Schegget J. Detection of human papillomavirus types 6 and 11 in pubic and perianal hair from patients with genital warts. J Clin Microbiol 1999; 37: 2270-2273.
28. Jensen KB, Collins CA, Nascimento E, Tan DW, Frye M, Itami S et al. Lrig1 expression defines a distinct multipotent stem cell population in mammalian epidermis. Cell Stem Cell 2009; 4: 427-439.
29. Snippert HJ, Haegebarth A, Kasper M, Jaks V, van Es JH, Barker N et al. Lgr6 marks stem cells in the hair follicle that generate all cell lineages of the skin. Science 2010; 327: 1385-1389.
30. Lowry WE, Blanpain C, Nowak JA, Guasch G, Lewis L, Fuchs E. Defining the impact of beta-catenin/Tcf transactivation on epithelial stem cells. Genes Dev 2005; 19: 1596-1611.
31. Jho EH, Zhang T, Domon C, Joo CK, Freund JN, Costantini F. Wnt/beta-catenin/Tcf signaling induces the transcription of Axin2, a negative regulator of the signaling pathway. Mol Cell Biol 2002; 22: 1172-1183.
32. Van der Flier LG, Sabates-Bellver J, Oving I, Haegebarth A, De Palo M, Anti M et al. The intestinal Wnt/TCF signature. Gastroenterology 2007; 132: 628-632.
33. Malanchi I, Peinado H, Kassen D, Hussenet T, Metzger D, Chambon P et al. Cutaneous cancer stem cell maintenance is dependent on beta-catenin signalling. Nature 2008; 452: 650-653.
34. Arwert EN, Lal R, Quist S, Rosewell I, van Rooijen N, Watt FM. Tumor formation initiated by nondividing epidermal cells via an inflammatory infiltrate. Proc Natl Acad Sci USA 2010; 107: 19903-19908.
35. Youssef KK, 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; 12: 299-305.
36. Wong SY, Reiter JF. Wounding mobilizes hair follicle stem cells to form tumors. Proc Natl Acad Sci USA 2011; 108: 4093-4098.
37. Meletis K, Wirta V, Hede SM, Nister M, Lundeberg J, Frisen J. p53 suppresses the self-renewal of adult neural stem cells. Development 2006; 133: 363-369.
38. Liu Y, Elf SE, Miyata Y, Sashida G, Liu Y, Huang G et al. p53 regulates hematopoietic stem cell quiescence. Cell Stem Cell 2009; 4: 37-48.
39. Cicalese A, Bonizzi G, Pasi CE, Faretta M, Ronzoni S, Giulini B et al. The tumor suppressor p53 regulates polarity of self-renewing divisions in mammary stem cells. Cell 2009; 138: 1083-1095.
40. Lorz C, Garcia-Escudero R, Segrelles C, Garin MI, Ariza JM, Santos M et al. A functional role of RB-dependent pathway in the control of quiescence in adult epidermal stem cells revealed by genomic profiling. Stem Cell Rev 2010; 6: 162-177.
41. Ruiz S, Santos M, Segrelles C, Leis H, Jorcano JL, Berns A et al. Unique and overlapping functions of pRb and p107 in the control of proliferation and differentiation in epidermis. Development 2004; 131: 2737-2748.
42. Martinez-Cruz AB, Santos M, Lara MF, Segrelles C, Ruiz S, Moral M et al. Spontaneous squamous cell carcinoma induced by the somatic inactivation of retinoblastoma and Trp53 tumor suppressors. Cancer Res 2008; 68: 683-692.
43. Huelsken J, Vogel R, Erdmann B, Cotsarelis G, Birchmeier W. Beta-catenin controls hair follicle morphogenesis and stem cell differentiation in the skin. Cell 2001; 105: 533-545.
44. Vidal VP, Chaboissier MC, Lutzkendorf S, Cotsarelis G, Mill P, Hui CC et al. Sox9 is essential for outer root sheath differentiation and the formation of the hair stem cell compartment. Curr Biol 2005; 15: 1340-1351.
45. Nguyen H, Rendl M, Fuchs E. Tcf3 governs stem cell features and represses cell fate determination in skin. Cell 2006; 127: 171-183.
46. McLaughlin-Drubin ME, Munger K. Oncogenic activities of human papillomaviruses. Virus Res 2009; 143: 195-208.
47. Schober M, Fuchs E. Tumor-initiating stem cells of squamous cell carcinomas and their control by TGF-beta and integrin/focal adhesion kinase (FAK) signaling. Proc Natl Acad Sci USA 2011; 108: 10544-10549.
48. Visvader JE, Lindeman GJ. Cancer stem cells: current status and evolving complexities. Cell Stem Cell 2012; 10: 717-728.
49. Kasper M, Jaks V, Are A, Bergstrom A, Schwager A, Barker N et al. Wounding enhances epidermal tumorigenesis by recruiting hair follicle keratinocytes. Proc Natl Acad Sci USA 2011; 108: 4099-4104.
50. Thomas M, Narayan N, Pim D, Tomaic V, Massimi P, Nagasaka K et al. Human papillomaviruses, cervical cancer and cell polarity. Oncogene 2008; 27: 7018-7030.
51. de Visser KE, Korets LV, Coussens LM. De novo carcinogenesis promoted by chronic inflammation is B lymphocyte dependent. Cancer Cell 2005; 7: 411-423.
52. Shinohara A, Yokoyama Y, Wan X, Takahashi Y, Mori Y, Takami T et al. Cytoplasmic/nuclear expression without mutation of exon 3 of the beta-catenin gene is frequent in the development of the neoplasm of the uterine cervix. Gynecol Oncol 2001; 82: 450-455.
53. Rodriguez-Sastre MA, Gonzalez-Maya L, Delgado R, Lizano M, Tsubaki G, Mohar A et al. Abnormal distribution of E-cadherin and beta-catenin in different histologic types of cancer of the uterine cervix. Gynecol Oncol 2005; 97: 330-336.
54. Bulut G, Fallen S, Beauchamp EM, Drebing LE, Sun J, Berry DL et al. Beta-catenin accelerates human papilloma virus type-16 mediated cervical carcinogenesis in transgenic mice. PLoS One 2011; 6: e27243.
55. Muñ oz P, Blanco R, Flores JM, Blasco MA. XPF nuclease-dependent telomere loss and increased DNA damage in mice overexpressing TRF2 result in premature aging and cancer. Nat Genet 2005; 37: 1063-1071.
56. Blanco R, Munoz P, Flores JM, Klatt P, Blasco MA. Telomerase abrogation dramatically accelerates TRF2-induced epithelial carcinogenesis. Genes Dev 2007; 21: 206-220.
57. Arbeit JM, Munger K, Howley PM, Hanahan D. Neuroepithelial carcinomas in mice transgenic with human papillomavirus type 16 E6/E7 ORFs. Am J Pathol 1993; 142: 1187-1197.