Overabundance of putative cancer stem cells in human skin keratinocyte cells malignantly transformed by arsenic

Toxicological Sciences

Volumn 125, Issue 1, 2012, Pages 20-29

  Sun, Yang ^a   Tokar, Erik J ^a   Waalkes, Michael P ^a  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

Author keywords

Arsenic; Cancer stem cell; Skin cancer

Indexed keywords

ARSENIC; CARCINOGEN; CD34 ANTIGEN; K 13; NOTCH1 RECEPTOR; PROTEIN P63; RAC1 PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN EXPRESSION; ARTICLE; CANCER STEM CELL; CELL ISOLATION; CELL POPULATION; CELL TRANSFORMATION; COLONY FORMATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; KERATINOCYTE; MOUSE; NONHUMAN; PHENOTYPE;

MUS;

EID: 84555189064     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfr282     Document Type: Article

References (48)

1. Barrandon, Y., and Green, H. (1987). Three clonal types of keratinocyte with different capacities for multiplication. Proc. Natl. Acad. Sci. U.S.A. 84, 2302-2306.
2. Benbrahim-Tallaa, L., Tokar, E. J., Diwan, B. A., Dill, A. L., Coppin, J. F., and Waalkes, M. P. (2009). Cadmium malignantly transforms normal human breast epithelial cells into a basal-like phenotype. Environ. Health Perspect. 117, 1847-1852.
3. Benitah, S. A., Frye, M., Glogauer, M., and Watt, F. M. (2005). Stem cell depletion through epidermal deletion of rac1. Science 309, 933-935.
4. Bernhard, E. J., Gruber, S. B., and Muschel, R. J. (1994). Direct evidence linking expression of matrix metalloproteinase 9 (92-kDa gelatinase/ collagenase) to the metastatic phenotype in transformed rat embryo cells. Proc. Natl. Acad. Sci. U.S.A. 91, 4293-4297.
5. Boukamp, P., Petrussevska, R. T., Breitkreutz, D., Hornung, J., Markham, A., and Fusenig, N. E. (1988). Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line. J. Cell Biol. 106, 761-771.
6. Claudinot, S., Nicolas, M., Oshima, H., Rochat, A., and Barrandon, Y. (2005). Long-term renewal of hair follicles from clonogenic multipotent stem cells. Proc. Natl. Acad. Sci. U.S.A. 102, 14677-14682.
7. Commandeur, S., de Gruijl, F. R., Willemze, R., Tensen, C. P., and El Ghalbzouri, A. (2009). An in vitro three-dimensional model of primary human cutaneous squamous cell carcinoma. Exp. Dermatol. 18, 849-856.
8. Di Cristofano, A., and Pandolfi, P. P. (2000). The multiple roles of PTEN in tumor suppression. Cell 100, 387-390.
9. Dontu, G., Abdallah, W. M., Foley, J. M., Jackson, K. W., Clarke, M. F., Kawamura, M. J., and Wicha, M. S. (2003). In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes Dev. 17, 1253-1270.
10. Fuchs, E. (2008). Skin stem cells: Rising to the surface. J. Cell Biol. 180, 273-284.
11. Gerdes, M. J., and Yuspa, S. H. (2005). The contribution of epidermal stem cells to skin cancer. Stem Cell Rev. 1, 225-231.
12. Germolec, D. R., Spalding, J., Boorman, G. A., Wilmer, J. L., Yoshida, T., Simeonova, P. P., Bruccoleri, A., Kayama, F., Gaido, K., Tennant, R., et al. (1997). Arsenic can mediate skin neoplasia by chronic stimulation of keratinocyte-derived growth factors. Mutat. Res. 386, 209-218.
13. Germolec, D. R., Spalding, J., Yu, H. S., Chen, G. S., Simeonova, P. P., Humble, M. C., Bruccoleri, A., Boorman, G. A., Foley, J. F., Yoshida, T., et al. (1998). Arsenic enhancement of skin neoplasia by chronic stimulation of growth factors. Am. J. Pathol. 153, 1775-1785.
14. He, Y. Y., Pi, J., Huang, J. L., Diwan, B. A., Waalkes, M. P., and Chignell, C. F. (2006). Chronic UVA irradiation of human HaCaT keratinocytes induces malignant transformation associated with acquired apoptotic resistance. Oncogene 25, 3680-3688.
15. International Agency for Research on Cancer (IARC). (2004). Arsenic in Drinking Water. International Agency for Research on Cancer Monographs on the Evaluation of Carcinogenic Risk to Humans. Some Drinking Water Disinfectants and Contaminants, Including Arsenic, pp. 269-477. IARC, Lyon, France.
16. Kangsamaksin, T., Park, H. J., Trempus, C. S., and Morris, R. J. (2007). A perspective on murine keratinocyte stem cells as targets of chemically induced skin cancer. Mol. Carcinog. 46, 579-584.
17. Kanitakis, J., Bourchany, D., Faure, M., and Claudy, A. (1999). Expression of the hair stem cell-specific keratin 15 in pilar tumors of the skin. Eur. J. Dermatol. 9, 363-365.
18. Kwei, K. A., Finch, J. S., Ranger-Moore, J., and Bowden, G. T. (2006). The role of Rac1 in maintaining malignant phenotype of mouse skin tumor cells. Cancer 231, 326-338.
19. Li, H., Chen, X., Calhoun-Davis, T., Claypool, K., and Tang, D. G. (2008). PC3 human prostate carcinoma cell holoclones contain self-renewing tumorinitiating cells. Cancer Res. 68, 1820-1825.
20. Liu, Y., Lyle, S., Yang, Z., and Cotsarelis, G. (2003). Keratin 15 promoter targets putative epithelial stem cells in the hair follicle bulge. J. Invest. Dermatol. 121, 963-968.
21. Lyle, S., Christofidou-Solomidou, M., Liu, Y., Elder, D. E., Albelda, S., and Cotsarelis, G. (1998). The C8/144B monoclonal antibody recognizes cytokeratin 15 and defines the location of human hair follicle stem cells. J. Cell Sci. 111(Pt 21), 3179-3188.
22. Malanchi, I., Peinado, H., Kassen, D., Hussenet, T., Metzger, D., Chambon, P., Huber, M., Hohl, D., Cano, A., Birchmeier, W., et al. (2008). Cutaneous cancer stem cell maintenance is dependent on beta-catenin signalling. Nature 452, 650-653.
23. Mazur, P. K., Grüner, B. M., Nakhai, H., Sipos, B., Zimber-Strobl, U., Strobl, L. J., Radtke, F., Schmid, R. M., and Siveke, J. T. (2010). Identification of epidermal Pdx1 expression discloses different roles of Notch1 and Notch2 in murine Kras(G12D)-induced skin carcinogenesis in vivo. PLoS One 5, e13578.
24. Mimeault, M., and Batra, S. K. (2006). Concise review: Recent advances on the significance of stem cells in tissue regeneration and cancer therapies. Stem Cells 24, 2319-2345.
25. Panelos, J., and Massi, D. (2009). Emerging role of Notch signaling in epidermal differentiation and skin cancer. Cancer Biol. Ther. 8, 1986-1993.
26. Pardal, R., Clarke, M. F., and Morrison, S. J. (2003). Applying the principles of stem-cell biology to cancer. Nat. Rev. Cancer 3, 895-902.
27. Patterson, T. J., Reznikova, T. V., Phillips, M. A., and Rice, R. H. (2005). Arsenite maintains germinative state in cultured human epidermal cells. Toxicol. Appl. Pharmacol. 207, 69-77.
28. Patterson, T. J., and Rice, R. H. (2007). Arsenite and insulin exhibit opposing effects on epidermal growth factor receptor and keratinocyte proliferative potential. Toxicol. Appl. Pharmacol. 221, 119-128.
29. Pellegrini, G., Dellambra, E., Golisano, O., Martinelli, E., Fantozzi, I., Bondanza, S., Ponzin, D., McKeon, F., and De Luca, M. (2001). p63 identifies keratinocyte stem cells. Proc. Natl. Acad. Sci. U.S.A. 98, 3156-3161.
30. Pi, J., Diwan, B. A., Sun, Y., Liu, J., Qu, W., He, Y., Stýblo, M., and Waalkes, M. P. (2008). Arsenic-induced malignant transformation of human keratinocytes: Involvement of Nrf2. Free Radic. Biol. Med. 45, 651-658.
31. Prado, E., Wurtz, T., Ferbus, D., Shabana, el-H., Forest, N., and Berdal, A. (2011). Sodium fluoride influences the expression of keratins in cultured keratinocytes. Cell Biol. Toxicol. 27, 69-81.
32. Rossman, T. G., Uddin, A. N., Burns, F. J., and Bosland, M. C. (2001). Arsenite is a cocarcinogen with solar ultraviolet radiation for mouse skin: An animal model for arsenic carcinogenesis. Toxicol. Appl. Pharmacol. 176, 64-71.
33. Rossman, T. G., Uddin, A. N., Burns, F. J., and Bosland, M. C. (2002). Arsenite cocarcinogenesis: An animal model derived from genetic toxicology studies. Environ. Health Perspect. 110(Suppl. 5), 749-752.
34. Schwartz, R. A. (1996). Premalignant keratinocytic neoplasms. J. Am. Acad. Dermatol. 35, 223-242.
35. Sell, S. (2004). Stem cell origin of cancer and differentiation therapy. Crit. Rev. Oncol. Hematol. 51, 1-28.
36. Signoretti, S., and Loda, M. (2007). Prostate stem cells: From development to cancer. Semin. Cancer Biol. 17, 219-224.
37. Stambolic, V., Suzuki, A., de la Pompa, J. L., Brothers, G. M., Mirtsos, C., Sasaki, T., Ruland, J., Penninger, J. M., Siderovski, D. P., and Mak, T. W. (1998). Negative regulation of PKB/Akt-dependent cell survival by the tumor suppressor PTEN. Cell 95, 29-39.
38. Straif, K., Benbrahim-Tallaa, L., Baan, R., Grosse, Y., Secretan, B., El Ghissassi, F., Bouvard, V., Guha, N., Freeman, C., Galichet, L., et al. (2009). A review of human carcinogens-Part C: Metals, arsenic, dusts, and fibres. Lancet Oncol. 10, 453-454.
39. Sun, Y., Pi, J., Wang, X., Tokar, E. J., Liu, J., and Waalkes, M. P. (2009). Aberrant cytokeratin expression during arsenic-induced acquired malignant phenotype in human HaCaT keratinocytes consistent with epidermal carcinogenesis. Toxicology 262, 162-170.
40. Tokar, E. J., Diwan, B. A., and Waalkes, M. P. (2010a). Arsenic exposure transforms human epithelial stem/progenitor cells into a cancer stem-like phenotype. Environ. Health Perspect. 118, 108-115.
41. Tokar, E. J., Diwan, B. A., Ward, J. M., Delker, D. A., and Waalkes, M. P. (2011). Carcinogenic effects of "whole-life" exposure to inorganic arsenic in CD1 mice. Toxicol. Sci. 119, 73-83.
42. Tokar, E. J., Qu, W., Liu, J., Liu, W., Webber, M. M., Phang, J. M., and Waalkes, M. P. (2010b). Arsenic-specific stem cell selection during malignant transformation. J. Natl. Cancer Inst. 102, 638-649.
43. Trempus, C. S., Morris, R. J., Bortner, C. D., Cotsarelis, G., Faircloth, R. S., Reece, J. M., and Tennant, R. W. (2003). Enrichment for living murine keratinocytes from the hair follicle bulge with the cell surface marker CD34. J. Invest. Dermatol. 120, 501-511.
44. Trempus, C. S., Morris, R. J., Ehinger, M., Elmore, A., Bortner, C. D., Ito, M., Cotsarelis, G., Nijhof, J. G., Peckham, J., Flagler, N., et al. (2007). CD34 expression by hair follicle stem cells is required for skin tumor development in mice. Cancer Res. 67, 4173-4181.
45. Waalkes, M. P., Liu, J., Germolec, D. R., Trempus, C. S., Cannon, R. E., Tokar, E. J., Tennant, R. W., Ward, J. M., and Diwan, B. A. (2008). Arsenic exposure in utero exacerbates skin cancer response in adulthood with contemporaneous distortion of tumor stem cell dynamics. Cancer Res. 68, 8278-8285.
46. Warren, B. S., Naylor, M. F., Winberg, L. D., Yoshimi, N., Volpe, J. P., Gimenez-Conti, I., and Slaga, T. J. (1993). Induction and inhibition of tumor progression. Proc. Soc. Exp. Biol. Med. 202, 9-15.
47. Wicha, M. S., Liu, S., and Dontu, G. (2006). Cancer stem cells: An old idea-a paradigm shift. Cancer Res. 66, 1883-1890.
48. Yu, H. S., Lee, C. H., Jee, S. H., Ho, C. K., and Guo, Y. L. (2001). Environmental and occupational skin diseases in Taiwan. J. Dermatol. 28, 628-631.