A novel form of melanoma apoptosis resistance: Melanogenesis up-regulation in apoptotic B16-F0 cells delays ursolic acid-triggered cell death

Experimental Cell Research

Volumn 317, Issue 12, 2011, Pages 1669-1676

  Pinon, Aline ^a   Limami, Youness ^a   Micallef, Ludovic ^a   Cook Moreau, Jeanne ^a   Liagre, Bertrand ^a   Delage, Christiane ^a   Duval, Raphaël Emmanuel ^b   Simon, Alain ^a  

^a UNIVERSITÉ DE LIMOGES   (France)

^b NANCY UNIVERSITÉ   (France)

Author keywords

Apoptosis resistance; B16 F0 mouse melanoma; Melanogenesis; Tyrosinase; Tyrosinase related protein; Ursolic acid

Indexed keywords

MELANIN; TYROSINASE RELATED PROTEIN 1; TYROSINASE RELATED PROTEIN 2; URSOLIC ACID;

APOPTOSIS; ARTICLE; CANCER CHEMOTHERAPY; CELL DEATH; CONTROLLED STUDY; HUMAN; HUMAN CELL; MELANOGENESIS; MELANOMA B16; MELANOMA CELL; PRIORITY JOURNAL; UPREGULATION;

EID: 79958786624     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2011.04.014     Document Type: Article

References (54)

1. Miller A.J., Mihm M.C. Melanoma. N. Engl. J. Med. 2006, 355:51-65.
2. Giblin A.V., Thomas J.M. Incidence, mortality and survival in cutaneous melanoma. J. Plast. Reconstr. Aesthet. Surg. 2007, 60:32-40.
3. Lens M.B., Dawes M. Global perspectives of contemporary epidemiological trends of cutaneous malignant melanoma. Br. J. Dermatol. 2004, 150:179-185.
4. Hearing V.J., Tsukamoto K. Enzymatic control of pigmentation in mammals. FASEB J. 1991, 5:2902-2909.
5. Hearing V.J. Biogenesis of pigment granules: a sensitive way to regulate melanocyte function. J. Dermatol. Sci. 2005, 37:3-14.
6. Slominski A., Tobin D.J., Shibahara S., Wortsman J. Melanin pigmentation in mammalian skin and its hormonal regulation. Physiol. Rev. 2004, 84:1155-1228.
7. Yaar M., Gilchrest B.A. Melanocyte biology: before, during, and after the Fitzpatrick era. J. Invest. Dermatol. 2004, 122:27-29.
8. Ivry G.B., Ogle C.A., Shim E.K. Role of sun exposure in melanoma. Dermatol. Surg. 2006, 32:481-492.
9. Jhappan C., Noonan F.P., Merlino G. Ultraviolet radiation and cutaneous malignant melanoma. Oncogene 2003, 22:3099-3112.
10. Abdel-Malek Z.A., Kadekaro A.L., Swope V.B. Stepping up melanocytes to the challenge of UV exposure. Pigment Cell Melanoma Res. 2010, 23:171-186.
11. Eller M.S., Ostrom K., Gilchrest B.A. DNA damage enhances melanogenesis. Proc. Natl Acad. Sci. U. S. A. 1996, 93:1087-1092.
12. Kadekaro A.L., Kavanagh R.J., Wakamatsu K., Ito S., Pipitone M.A., Abdel-Malek Z.A. Cutaneous photobiology. The melanocyte vs. the sun: who will win the final round?. Pigment Cell Res. 2003, 16:434-447.
13. Miyamura Y., Coelho S.G., Wolber R., Miller S.A., Wakamatsu K., Zmudzka B.Z., Ito S., Smuda C., Passeron T., Choi W., Batzer J., Yamaguchi Y., Beer J.Z., Hearing V.J. Regulation of human skin pigmentation and responses to ultraviolet radiation. Pigment Cell Res. 2007, 20:2-13.
14. Brenner M., Hearing V.J. The protective role of melanin against UV damage in human skin. Photochem. Photobiol. 2008, 84:539-549.
15. Ortonne J.P. Photoprotective properties of skin melanin. Br. J. Dermatol. 2002, 146(Suppl 61):7-10.
16. Gilchrest B.A., Eller M.S., Geller A.C., Yaar M. The pathogenesis of melanoma induced by ultraviolet radiation. N. Engl. J. Med. 1999, 340:1341-1348.
17. Soengas M.S., Lowe S.W. Apoptosis and melanoma chemoresistance. Oncogene 2003, 22:3138-3151.
18. Grossman D., McNiff J.M., Li F., Altieri D.C. Expression and targeting of the apoptosis inhibitor, survivin, in human melanoma. J. Invest. Dermatol. 1999, 113:1076-1081.
19. Grossman D., Altieri D.C. Drug resistance in melanoma: mechanisms, apoptosis, and new potential therapeutic targets. Cancer Metastasis Rev. 2001, 20:3-11.
20. Chu W., Pak B.J., Bani M.R., Kapoor M., Lu S.J., Tamir A., Kerbel R.S., Ben-David Y. Tyrosinase-related protein 2 as a mediator of melanoma specific resistance to cis-diamminedichloroplatinum(II): therapeutic implications. Oncogene 2000, 19:395-402.
21. Pak B.J., Lee J., Thai B.L., Fuchs S.Y., Shaked Y., Ronai Z., Kerbel R.S., Ben-David Y. Radiation resistance of human melanoma analysed by retroviral insertional mutagenesis reveals a possible role for dopachrome tautomerase. Oncogene 2004, 23:30-38.
22. Jiang S., Liu X.M., Dai X., Zhou Q., Lei T.C., Beermann F., Wakamatsu K., Xu S.Z. Regulation of DHICA-mediated antioxidation by dopachrome tautomerase: implication for skin photoprotection against UVA radiation. Free Radic. Biol. Med. 2010, 48:1144-1151.
23. Liu J. Pharmacology of oleanolic acid and ursolic acid. J. Ethnopharmacol. 1995, 49:57-68.
24. Novotny L., Vachalkova A., Biggs D. Ursolic acid: an anti-tumorigenic and chemopreventive activity. Minireview. Neoplasma 2001, 48:241-246.
25. Aggarwal B.B., Shishodia S. Molecular targets of dietary agents for prevention and therapy of cancer. Biochem. Pharmacol. 2006, 71:1397-1421.
26. Dorai T., Aggarwal B.B. Role of chemopreventive agents in cancer therapy. Cancer Lett. 2004, 215:129-140.
27. Harmand P.O., Duval R., Liagre B., Jayat-Vignoles C., Beneytout J.L., Delage C., Simon A. Ursolic acid induces apoptosis through caspase-3 activation and cell cycle arrest in HaCat cells. Int. J. Oncol. 2003, 23:105-112.
28. Harmand P.O., Duval R., Delage C., Simon A. Ursolic acid induces apoptosis through mitochondrial intrinsic pathway and caspase-3 activation in M4Beu melanoma cells. Int. J. Cancer 2005, 114:1-11.
29. Manu K.A., Kuttan G. Ursolic acid induces apoptosis by activating p53 and caspase-3 gene expressions and suppressing NF-kappaB mediated activation of bcl-2 in B16F-10 melanoma cells. Int. Immunopharmacol. 2008, 8:974-981.
30. Agar N., Young A.R. Melanogenesis: a photoprotective response to DNA damage?. Mutat. Res. 2005, 571:121-132.
31. Chen K.G., Valencia J.C., Lai B., Zhang G., Paterson J.K., Rouzaud F., Berens W., Wincovitch S.M., Garfield S.H., Leapman R.D., Hearing V.J., Gottesman M.M. Melanosomal sequestration of cytotoxic drugs contributes to the intractability of malignant melanomas. Proc. Natl Acad. Sci. U. S. A. 2006, 103:9903-9907.
32. Chen K.G., Valencia J.C., Gillet J.P., Hearing V.J., Gottesman M.M. Involvement of ABC transporters in melanogenesis and the development of multidrug resistance of melanoma. Pigment Cell Melanoma Res. 2009, 22:740-749.
33. Khlgatian M.K., Hadshiew I.M., Asawanonda P., Yaar M., Eller M.S., Fujita M., Norris D.A., Gilchrest B.A. Tyrosinase gene expression is regulated by p53. J. Invest. Dermatol. 2002, 118:126-132.
34. Olszewska-Slonina D.M., Styczynski J., Czajkowski R., Drewa T.A., Musialkiewicz D. Cell cycle, melanin contents and apoptosis processes in B16 and Cloudman S91 mouse melanoma cells after exposure to cytostatic drugs. Acta Pol. Pharm. 2007, 64:469-478.
35. Koo J.H., Kim H.T., Yoon H.Y., Kwon K.B., Choi I.W., Jung S.H., Kim H.U., Park B.H., Park J.W. Effect of xanthohumol on melanogenesis in B16 melanoma cells. Exp. Mol. Med. 2008, 40:313-319.
36. Prince S., Wiggins T., Hulley P.A., Kidson S.H. Stimulation of melanogenesis by tetradecanoylphorbol 13-acetate (TPA) in mouse melanocytes and neural crest cells. Pigment Cell Res. 2003, 16:26-34.
37. Yang J.Y., Koo J.H., Song Y.G., Kwon K.B., Lee J.H., Sohn H.S., Park B.H., Jhee E.C., Park J.W. Stimulation of melanogenesis by scoparone in B16 melanoma cells. Acta Pharmacol. Sin. 2006, 27:1467-1473.
38. Sato K., Toriyama M. Effect of pyrroloquinoline quinone (PQQ) on melanogenic protein expression in murine B16 melanoma. J. Dermatol. Sci. 2009, 53:140-145.
39. Costin G.E., Hearing V.J. Human skin pigmentation: melanocytes modulate skin color in response to stress. FASEB J. 2007, 21:976-994.
40. Korytowski W., Sarna T. Bleaching of melanin pigments. Role of copper ions and hydrogen peroxide in autooxidation and photooxidation of synthetic dopa-melanin. J. Biol. Chem. 1990, 265:12410-12416.
41. Brozyna A.A., VanMiddlesworth L., Slominski A.T. Inhibition of melanogenesis as a radiation sensitizer for melanoma therapy. Int. J. Cancer 2008, 123:1448-1456.
42. Ott M., Gogvadze V., Orrenius S., Zhivotovsky B. Mitochondria, oxidative stress and cell death. Apoptosis 2007, 12:913-922.
43. Kakkar P., Singh B.K. Mitochondria: a hub of redox activities and cellular distress control. Mol. Cell. Biochem. 2007, 305:235-253.
44. Achiwa Y., Hasegawa K., Komiya T., Udagawa Y. Ursolic acid induces Bax-dependent apoptosis through the caspase-3 pathway in endometrial cancer SNG-II cells. Oncol. Rep. 2005, 13:51-57.
45. Shyu M.H., Kao T.C., Yen G.C. Oleanolic acid and ursolic acid induce apoptosis in HuH7 human hepatocellular carcinoma cells through a mitochondrial-dependent pathway and downregulation of XIAP. J. Agric. Food Chem. 2010, 58:6110-6118.
46. Kassi E., Sourlingas T.G., Spiliotaki M., Papoutsi Z., Pratsinis H., Aligiannis N., Moutsatsou P. Ursolic acid triggers apoptosis and Bcl-2 downregulation in MCF-7 breast cancer cells. Cancer Invest. 2009, 27:723-733.
47. Newmeyer D.D., Ferguson-Miller S. Mitochondria: releasing power for life and unleashing the machineries of death. Cell 2003, 112:481-490.
48. Bayir H., Kagan V.E. Bench-to-bedside review: mitochondrial injury, oxidative stress and apoptosis - there is nothing more practical than a good theory. Crit. Care 2008, 12:206-216.
49. Orrenius S. Reactive oxygen species in mitochondria-mediated cell death. Drug Metab. Rev. 2007, 39:443-455.
50. Rad H.H., Yamashita T., Jin H.Y., Hirosaki K., Wakamatsu K., Ito S., Jimbow K. Tyrosinase-related proteins suppress tyrosinase-mediated cell death of melanocytes and melanoma cells. Exp. Cell Res. 2004, 298:317-328.
51. Riley P.A. Melanogenesis and melanoma. Pigment Cell Res. 2003, 16:548-552.
52. Pak B.J., Li Q., Kerbel R.S., Ben-David Y. TYRP2-mediated resistance to cis-diamminedichloroplatinum (II) in human melanoma cells is independent of tyrosinase and TYRP1 expression and melanin content. Melanoma Res. 2000, 10:499-505.
53. Pak B.J., Chu W., Lu S.J., Kerbel R.S., Ben-David Y. Lineage-specific mechanism of drug and radiation resistance in melanoma mediated by tyrosinase-related protein 2. Cancer Metastasis Rev. 2001, 20:27-32.
54. Nishioka E., Funasaka Y., Kondoh H., Chakraborty A.K., Mishima Y., Ichihashi M. Expression of tyrosinase, TRP-1 and TRP-2 in ultraviolet-irradiated human melanomas and melanocytes: TRP-2 protects melanoma cells from ultraviolet B induced apoptosis. Melanoma Res. 1999, 9:433-443.