Stem cell quiescence acts as a tumour suppressor in squamous tumours

Nature Cell Biology

Volumn 16, Issue 1, 2014, Pages 99-107

  White, A C ^a   Khuu, J K ^a   Dang, C Y ^a   Hu, J ^a   Tran, K V ^a   Liu, A ^a   Gomez, S ^a   Zhang, Z ^b   Yi, R ^b   Scumpia, P ^c   Grigorian, M ^a   Lowry, W E ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF COLORADO   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; LGR5 PROTEIN; LGR6 PROTEIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CANCER INHIBITION; CARCINOGENESIS; CELL PROLIFERATION; CONTROLLED STUDY; FEMALE; GENE EXPRESSION PROFILING; HAIR FOLLICLE STEM CELL; HUMAN; HUMAN TISSUE; HYPERPLASIA; MALE; MOUSE; NONHUMAN; ONCOGENE K RAS; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SQUAMOUS CELL CARCINOMA; STEM CELL; STEM CELL QUIESCENCE; TUMOR SUPPRESSOR GENE;

EID: 84891344481     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb2889     Document Type: Article

References (54)

1. Lowry, W. E. Richter, L. Signaling in adult stem cells. Front. Biosci. 12, 3911-3927 (2007).
2. Fuchs, E. The tortoise and the hair: slow-cycling cells in the stem cell race. Cell 137, 811-819 (2009).
3. Lapouge, G. et al. Identifying the cellular origin of squamous skin tumors. Proc. Natl Acad. Sci. USA 108, 7431-7436 (2011).
4. White, A. C. et al. De-ning the origins of Ras/p53-mediated squamous cell carcinoma. Proc. Natl Acad. Sci. USA 108, 7425-7430 (2011).
5. Barker, N. et al. Crypt stem cells as the cells-of-origin of intestinal cancer. Nature 457, 608-611 (2009).
6. Visvader, J. E. Cells of origin in cancer. Nature 469, 314-322 (2011).
7. Paus, R., Muller-Rover, S., Botchkarev, V. A. Chronobiology of the hair follicle: hunting the ̀hair cycle clock'. J. Invest. Dermatol. Symp. Proc. 4, 338-345 (1999).
8. Greco, V. et al. A two-step mechanism for stem cell activation during hair regeneration. Cell Stem Cell 4, 155-169 (2009).
9. Trempus, C. S. et al. CD34 expression by hair follicle stem cells is required for skin tumor development in mice. Cancer Res. 67, 4173-4181 (2007).
10. Finch, J. S., Albino, H. E. Bowden, G. T. Quantitation of early clonal expansion of two mutant 61st codon c-Ha-ras alleles in DMBA/TPA treated mouse skin by nested PCR/RFLP. Carcinogenesis 17, 2551-2557 (1996).
11. Andreasen, E., Borum, K. The in-uence of the mouse hair cycle on 9, 10-dimethyl-1, 2-benzanthracene-induced skin tumors. Acta Pathol. Microbiol. Scand. Suppl. 39, 76-77 (1956).
12. Klinken-Rasmussen, L. Effect of croton oil applied to mouse skin originally painted with suboptimal doses of carcinogen during the growth and resting phases of the hair follicles. Acta Pathol. Microbiol. Scand. Suppl. 39, 78-79 (1956).
13. Miller, S. J. et al. Mouse skin is particularly susceptible to tumor initiation during early anagen of the hair cycle: possible involvement of hair follicle stem cells. J. Invest. Dermatol. 101, 591-594 (1993).
14. Lavker, R. M. et al. Hair follicle stem cells: their location, role in hair cycle, and involvement in skin tumor formation. J. Invest. Dermatol. 101, 16S-26S (1993).
15. Grachtchouk, M. et al. Basal cell carcinomas in mice arise from hair follicle stem cells and multiple epithelial progenitor populations. J. Clin. Invest. 121, 1768-1781 (2011).
16. Mancuso, M. et al. Hair cycle-dependent basal cell carcinoma tumorigenesis in Ptc1neo67/C mice exposed to radiation. Cancer Res. 66, 6606-6614 (2006).
17. Li, S. et al. A keratin 15 containing stem cell population from the hair follicle contributes to squamous papilloma development in the mouse. Mol. Carcinog. 52, 751-759 (2012).
18. Groszer, M. et al. Negative regulation of neural stem/progenitor cell proliferation by the Pten tumor suppressor gene in vivo. Science 294, 2186-2189 (2001).
19. Jaks, V. et al. Lgr5 marks cycling, yet long-lived, hair follicle stem cells. Nature Genet. 40, 1291-1299 (2008).
20. Snippert, H. J. et al. Lgr6 marks stem cells in the hair follicle that generate all cell lineages of the skin. Science 327, 1385-1389 (2010).
21. Zhang, J. et al. BMP signaling inhibits hair follicle anagen induction by restricting epithelial stem/progenitor cell activation and expansion. Stem Cells 24, 2826-2839 (2006).
22. Gu, T. et al. CREB is a novel nuclear target of PTEN phosphatase. Cancer Res. 71, 2821-2825 (2011).
23. Vivanco, I. et al. Identi-cation of the JNK signaling pathway as a functional target of the tumor suppressor PTEN. Cancer Cell 11, 555-569 (2007).
24. Tran, L. M. et al. Determining PTEN functional status by network component deduced transcription factor activities. PLoS ONE 7, e31053 (2012).
25. Rozenberg, J. et al. Inhibition of CREB function in mouse epidermis reduces papilloma formation. Mol. Cancer Res. 7, 654-664 (2009).
26. Ji, J. et al. Elevated coding mutation rate during the reprogramming of human somatic cells into induced pluripotent stem cells. Stem Cells 30, 435-440 (2012).
27. Plikus, M. V. New activators and inhibitors in the hair cycle clock: targeting stem cells' state of competence. J. Invest. Dermatol. 132, 1321-1324 (2012).
28. Ahmed, M. I., Mardaryev, A. N., Lewis, C. J., Sharov, A. A. Botchkareva, N. V. MicroRNA-21 is an important downstream component of BMP signalling in epidermal keratinocytes. J. Cell Sci. 124, 3399-3404 (2011).
29. Wang, T. et al. TGF-beta-induced miR-21 negatively regulates the antiproliferative activity but has no effect on EMT of TGF-beta in HaCaT cells. Int. J. Biochem. Cell Biol. 44, 366-376 (2012).
30. Zhong, X., Chung, A. C., Chen, H. Y., Meng, X. M. Lan, H. Y. Smad3-mediated upregulation of miR-21 promotes renal-brosis. J. Am. Soc. Nephrol. 22, 1668-1681 (2011).
31. Yao, Q. et al. Micro-RNA-21 regulates TGF-beta-induced myo-broblast differen-tiation by targeting PDCD4 in tumor-stroma interaction. Int. J. Cancer 128, 1783-1792 (2011).
32. Kim, Y. J., Hwang, S. J., Bae, Y. C. Jung, J. S. MiR-21 regulates adipogenic differentiation through the modulation of TGF-beta signaling in mesenchymal stem cells derived from human adipose tissue. Stem Cells 27, 3093-3102 (2009).
33. Ma, X. et al. Loss of the miR-21 allele elevates the expression of its target genes and reduces tumorigenesis. Proc. Natl Acad. Sci. USA 108, 10144-10149 (2011).
34. Zhu, H. et al. MicroRNA expression abnormalities in limited cutaneous scleroderma and diffuse cutaneous scleroderma. J. Clin. Immunol. 32, 514-522 (2012).
35. Darido, C. et al. Targeting of the tumor suppressor GRHL3 by a miR-21-dependent proto-oncogenic network results in PTEN loss and tumorigenesis. Cancer Cell 20, 635-648 (2011).
36. Narducci, M. G. et al. MicroRNA pro-ling reveals that miR-21, miR486 and miR-214 are upregulated and involved in cell survival in Sezary syndrome. Cell Death Dis. 2, e151 (2011).
37. Oshimori, N., Fuchs, E. Paracrine TGF-beta signaling counterbalances BMP-mediated repression in hair follicle stem cell activation. Cell Stem Cell 10, 63-75 (2012).
38. Sugawara, K., Schneider, M. R., Dahlhoff, M., Kloepper, J. E. Paus, R. Cutaneous consequences of inhibiting EGF receptor signaling in vivo: normal hair follicle development, but retarded hair cycle induction and inhibition of adipocyte growth in Egfr(Wa5) mice. J. Dermatol. Sci. 57, 155-161 (2010).
39. Lowry, W. E. et al. De-ning the impact of beta-catenin/Tcf transactivation on epithelial stem cells. Genes Dev. 19, 1596-1611 (2005).
40. Kimura-Ueki, M. et al. Hair cycle resting phase is regulated by cyclic epithelial FGF18 signaling. J. Invest. Dermatol. 132, 1338-1345 (2012).
41. Kobielak, K., Stokes, N., de la Cruz, J., Polak, L., Fuchs, E. Loss of a quiescent niche but not follicle stem cells in the absence of bone morphogenetic protein signaling. Proc. Natl Acad. Sci. USA 104, 10063-10068 (2007).
42. Brownstein, M. H., Mehregan, A. H. Bilowski, J. B. Trichilemmomas in Cowden's disease. Jama 238, 26 (1977).
43. Lazarov, M. et al. CDK4 coexpression with Ras generates malignant human epidermal tumorigenesis. Nat. Med. 8, 1105-1114 (2002).
44. Agrawal, N. et al. Exome sequencing of head and neck squamous cell carcinoma reveals inactivating mutations in NOTCH1. Science 333, 1154-1157 (2011).
45. Stransky, N. et al. The mutational landscape of head and neck squamous cell carcinoma. Science 333, 1157-1160 (2011).
46. Kubo, Y., Urano, Y., Hida, Y., Arase, S. Lack of somatic mutation in the PTEN gene in squamous cell carcinomas of human skin. J. Dermatol. Sci. 19, 199-201 (1999).
47. Al-Zaid, T. et al. Trichilemmomas show loss of PTEN in Cowden syndrome but only rarely in sporadic tumors. J. Cutan. Pathol. 39, 493-499 (2012).
48. Kurose, K., Zhou, X. P., Araki, T., Eng, C. Biallelic inactivating mutations and an occult germline mutation of PTEN in primary cervical carcinomas. Genes Chromosom. Cancer 29, 166-172 (2000).
49. Tuveson, D. A. et al. Endogenous oncogenic K-ras(G12D) stimulates proliferation and widespread neoplastic and developmental defects. Cancer Cell 5, 375-387 (2004).
50. Jonkers, J. et al. Synergistic tumor suppressor activity of BRCA2 and p53 in a conditional mouse model for breast cancer. Nature Gen. 29, 418-425 (2001).
51. Jackson, E. L. et al. Analysis of lung tumor initiation and progression using conditional expression of oncogenic K-ras. Genes Dev. 15, 3243-3248 (2001).
52. Horenstein, M. G. Bacheler, C. J. Follicular density and ratios in scarring and nonscarring alopecia. Am. J. Dermatopathol. 35, 818-826 (2013).
53. Chin, M. H., Pellegrini, M., Plath, K., Lowry, W. E. Molecular analyses of human induced pluripotent stem cells and embryonic stem cells. Cell Stem Cell 7, 263-269 (2010).
54. Wang, D. et al. Quantitative functions of Argonaute proteins in mammalian development. Genes Dev. 26, 693-704 (2012).