Melanogenesis stimulation in B16-F10 melanoma cells induces cell cycle alterations, increased ROS levels and a differential expression of proteins as revealed by proteomic analysis

Experimental Cell Research

Volumn 318, Issue 15, 2012, Pages 1913-1925

  Cunha, Elizabeth S ^a   Kawahara, Rebeca ^a   Kadowaki, Marina K ^b   Amstalden, Hudson G ^a   Noleto, Guilhermina R ^a   Cadena, Silvia Maria S C ^a   Winnischofer, Sheila M B ^a   Martinez, Glaucia R ^a  

^a FEDERAL UNIVERSITY OF PARANÁ   (Brazil)

^b UNIVERSIDADE ESTADUAL DO OESTE DO PARANÁ   (Brazil)

Author keywords

Cell cycle; Melanin; Melanogenesis; Melanoma; ROS

Indexed keywords

FRUCTOSE BIPHOSPHATE ALDOLASE A; HEAT SHOCK PROTEIN 70; LACTATE DEHYDROGENASE; MELANIN; MESSENGER RNA; PROTEIN; PROTEIN P21; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; PYRUVATE KINASE M2; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL AGING; CELL CYCLE; CELL PROLIFERATION; CELL VIABILITY; DOWN REGULATION; ENZYME ACTIVITY; IN VITRO STUDY; MELANOGENESIS; MELANOMA CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; PROTEOMICS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION;

EID: 84863775741     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2012.05.019     Document Type: Article

References (57)

1. Maresca V., Flori E., Briganti S., Mastrofrancesco A., Fabbri C., Mileo A.M., Paggi M.G., Picardo M. Correlation between melanogenic and catalase activity in in vitro human melanocytes: a synergic strategy against oxidative stress. Pigment Cell Melanoma Res. 2008, 21:200-205.
2. Korytowski W., Pilas B., Sarna T., Kalyanaraman B. Photoinduced generation of hydrogen peroxide and hydroxyl radicals in melanin. Photochem. Photobiol. 1987, 45:185-190.
3. Suzukawa A.A., Vieira A., Winnischofer S.M.B., Scalfo A.C., Di Mascio P., Ferreira A.M.d.C., Ravanat J.-L., Martins D.d.L., Rocha M.E.M., Martinez G.R. Novel properties of melanins include promotion of DNA strand breaks, impairment of repair, and reduced ability to damage DNA after quenching of singlet oxygen. Free Radic. Biol. Med. 2012, 52:1945-1953.
4. Hoshino T., Matsuda M., Yamashita Y., Takehara M., Fukuya M., Mineda K., Maji D., Ihn H., Adachi H., Sobue G., Funasaka Y., Mizushima T. Suppression of melanin production by expression of HSP70. J. Biol. Chem. 2010, 285:13254-13263.
5. Snyder J.R., Hall A., Ni-Komatsu L., Khersonsky S.M., Chang Y.-T., Orlow S.J. Dissection of Melanogenesis with Small Molecules Identifies Prohibitin as a Regulator. Chem. Biol. 2005, 12:477-484.
6. Nawarak J., Huang-Liu R., Kao S.-H., Liao H.-H., Sinchaikul S., Chen S.-T., Cheng S.-L. Proteomics analysis of kojic acid treated A375 human malignant melanoma cells. J. Proteome Res. 2008, 7:3737-3746.
7. Pinon A., Limami Y., Micallef L., Cook-Moreau J., Liagre B., Delage C., Duval R.E., Simon A. A novel form of melanoma apoptosis resistance: melanogenesis up-regulation in apoptotic B16-F0 cells delays ursolic acid-triggered cell death. Exp. Cell Res. 2011, 317:1669-1676.
8. Borovanský J., Mirejovský P., Riley P.A. Possible relationship between abnormal melanosomestructure and cytotoxic phenomena in malignant melanoma. Neoplasma 1991, 38:393-400.
9. Nappi A.J., Vass E. Hydrogen peroxide generation associated with the oxidation of theeumelanogenic precursor 5,6-dihydroxyndole and 5,6 dihydroxyindole-2-carboxylic acid. Melanoma Res. 1996, 6:341-349.
10. Kvam E., Tyrrell R.M. The role of melanin in the induction of oxidative DNA base damage by ultraviolet A irradiation of DNA or melanoma cells 1999, 113:209-213.
11. 2+. Exp. Cell Res. 2004, 294:60-67.
12. Wang J., Bao N., Paris L.L., Geahlen R.L., Lu C. Total internal reflection fluorescence flow cytometry. Anal. Chem. 2008, 80:9840-9844.
13. Reilly T.P., Bellevue Iii F.H., Woster P.M., Svensson C.K. Comparison of the in vitro cytotoxicity of hydroxylamine metabolites of sulfamethoxazole and dapsone. Biochem. Pharmacol. 1998, 55:803-810.
14. Gillies R.J., Didier N., Denton M. Determination of cell number in monolayer cultures. Anal. Biochem. 1986, 159:109-113.
15. Debacq-Chainiaux F., Erusalimsky J.D., Campisi J., Toussaint O. Protocols to detect senescence-associated beta-galactosidase (SA-[beta]gal) activity, a biomarker of senescent cells in culture and in vivo. Nat. Protocols 2009, 4:1798-1806.
16. Vandesompele J., De Preter K., Pattyn F., Poppe B., Van Roy N., De Paepe A., Speleman F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 2002, 3. research0034.0031 - research0034.0011.
17. Shapiro H.M. Flow cytometric estimation of DNA and RNA content in intact cells stained with hoechst 33342 and pyronin Y. Cytometry 1981, 2:143-150.
18. Williams K.R., Stone K.L. Enzymatic cleavage and HPLC peptide mapping of proteins. Mol. Biotechnol. 1997, 8:155-167.
19. Keiding R., Hörder M., Denmark W.G., Pitkänen E., Tenhunen R., Strömme J.H., Theodorsen L., Waldenström J., Tryding N., Westlund L. Recommended Methods for the Determination of Four Enzymes in Blood. Scand. J. Clin. Lab. Invest. 1974, 33:291-306.
20. Pavel S., van Nieuwpoort F., van der Meulen H., Out C., Pizinger K., Cetkovská P., Smit N.P.M., Koerten H.K. Disturbed melanin synthesis and chronic oxidative stress in dysplastic naevi. Eur. J. Cancer 2004, 40:1423-1430.
21. Szatrowski T.P., Nathan C.F. Production of large amounts of hydrogen peroxide by human tumor cells. Cancer Res. 1991, 51:794-798.
22. Haddad M.M., Xu W., Schwahn D.J., Liao F., Medrano E.E. Activation of a cAMP Pathway and Induction of Melanogenesis Correlate with Association of p16INK4 and p27KIP1 to CDKs, Loss of E2F-Binding Activity, and Premature Senescence of Human Melanocytes. Exp. Cell Res. 1999, 253:561-572.
23. Stein G.H., Drullinger L.F., Soulard A., Dulić V. Differential roles for cyclin-dependent kinase inhibitors p21 and p16 in the mechanisms of senescence and differentiation in human fibroblasts. Mol. Cell Biol. 1999, 19:2109-2117.
24. Collado M., Serrano M. The power and the promise of oncogene-induced senescence markers. Nat. Rev. Cancer 2006, 6:472-476.
25. CDKN1A impairs entry to quiescence and activates a DNA damage response in normal fibroblasts induced to quiescence. Cell Cycle 2009, 8:105-114.
26. Rastogi S., Joshi B., Dasgupta P., Morris M., Wright K., Chellappan S. Prohibitin facilitates cellular senescence by recruiting specific corepressors to inhibit E2F target genes. Mol. Cell Biol. 2006, 26:4161-4171.
27. Wang F., Osawa T., Tsuchida R., Yuasa Y., Shibuya M. Downregulation of receptor for activated C-kinase 1 (RACK1) suppresses tumor growth by inhibiting tumor cell proliferation and tumor-associated angiogenesis. Cancer Sci. 2011, 102:2007-2013.
28. Cho Y.-Y., Tang F., Yao K., Lu C., Zhu F., Zheng D., Pugliese A., Bode A.M., Dong Z. Cyclin-dependent kinase-3-mediated c-jun phosphorylation at Ser63 and Ser73 enhances cell transformation. Cancer Res 2009, 69:272-281.
29. Caraglia M., Abbruzzese A., Leardi A., Pepe S., Budillon A., Baldassare G., Selleri C., Lorenzo S.D, Fabbrocini A., Giuberti G., Vitale G., Lupoli G., Bianco A.R., Tagliaferri P. Interferon-alpha induces apoptosis in human KB cells through a stress-dependent mitogen activated protein kinase pathway that is antagonized by epidermal growth factor. Cell Death Differ. 1999, 6:773-780.
30. Noiva R., Lennarz W.J. Protein disulfide isomerase. A multifunctional protein resident in the lumen of the endoplasmic reticulum. J. Biol. Chem. 1992, 267:3553-3556.
31. Morimoto R.I., Santoro M.G. Stress-inducible responses and heat shock proteins: new pharmacologic targets for cytoprotection. Nat. Biotech. 1998, 16:833-838.
32. Lei T., He Q.-Y., Cai Z., Zhou Y., Wang Y.-L., Si L.-S., Cai Z., Chiu J.-F. Proteomic analysis of chromium cytotoxicity in cultured rat lung epithelial cells. Proteomics 2008, 8:2420-2429.
33. Prensner J.R., Chinnaiyan A.M. Metabolism unhinged: IDH mutations in cancer. Nat. Med. 2011, 17:291-293.
34. Fantin V.R., St-Pierre J., Leder P. Attenuation of LDH-A expression uncovers a link between glycolysis, mitochondrial physiology, and tumor maintenance. Cancer Cell 2006, 9:425-434.
35. Suzuki A., Iizuka A., Komiyama M., Takikawa M., Kume A., Tai S., Ohshita C., Kurusu A., Nakamura Y., Yamamoto A., Yamazaki N., Yoshikawa S., Kiyohara Y., Akiyama Y. Identification of melanoma antigens using a Serological Proteome Approach (SERPA). Cancer Genomics-Proteomics 2010, 7:17-23.
36. 2. Biochem. Biophys. Res. Commun. 2004, 325:1412-1417.
37. Sarosi L.A.G., Rieber M.S., Rieber M. Hydrogen peroxide increases a 55-kDa tyrosinase concomitantly with induction of p53-dependent p21 waf1 expression and a greater Bax/Bcl-2 ratio in pigmented melanoma. Biochem. Biophys. Res. Commun. 2003, 312:355-359.
38. Spencer J.D., Gibbons N.C.J., Rokos H., Peters E.M.J., Wood J.M., Schallreuter K.U. Oxidative stress via hydrogen peroxide affects proopiomelanocortin peptides directly in the epidermis of patients with vitiligo. J. Invest. Dermatol. 2006, 127:411-420.
39. Brown J.P., Wei W., Sedivy J.M. Bybass of senescence after disruption of p21CIP1/WAF1 gene in normal diploid human fibroblasts. Science 1997, 277:831-834.
40. Zheng Q.H., Ma L.W., Zhu W.G., Zhang Z.Y., Tong T.J. p21Waf1/Cip1 plays a critical role in modulating senescence through changes of DNA methylation. J. Cell Biochem. 2006, 98:1230-1248.
41. Laporte D., Lebaudy A., Sahin A., Pinson B., Ceschin J., Daignan-Fornier B., Sagot I. Metabolic status rather than cell cycle signals control quiescence entry and exit. J. Cell Biol. 2011, 192:949-957.
42. Tian J.Q., Quaroni A. Involvement of p21(WAF1/Cip1) and p27(Kip1) in intestinal epithelial cell differentiation. Am. J. Physiol.-Cell Physiol. 1999, 276:C1245-C1258.
43. Kwon Y.H., Jovanovic A., Serfas M.S., Kiyokawa H., Tyner A.L. p21 Functions to Maintain Quiescence of p27-deficient Hepatocytes. J. Biol. Chem. 2002, 277:41417-41422.
44. Neckers L. Heat shock protein 90: The cancer chaperone. J. Biosci. 2007, 32:517-530.
45. Meyerson G.H.E.M, Wu C L, Su L K, Gorka C, Nelson C, Harlow E, Tsai L H A family of human cdc2-related protein kinases. Embo. J. 1992, 11:2909-2917.
46. Braun K., Holzl G., Soucek T., Geisen C., Moroy T., Hengstschlager M. Investigation of the cell cycle regulation of cdk3-associated kinase activity and the role of cdk3 in proliferation and transformation. Oncogene 1998, 17:2259-2269.
47. van den Heuvel S., Harlow E. Distinct roles for cyclin-dependent kinases in cell cycle control. Science 1993, 262:2050-2054.
48. Liu Y., He J., Ji S., Wang Q., Pu H., Jiang T., Meng L., Yang X., Ji J. Comparative studies of early liver dysfunction in senescence-accelerated mouse using mitochondrial proteomics approaches. Mol. Cell. Proteomics 2008, 7:1737-1747.
49. Christofk H.R., Vander Heiden M.G., Harris M.H., Ramanathan A., Gerszten R.E., Wei R., Fleming M.D., Schreiber S.L., Cantley L.C. The M2 splice isoform of pyruvate kinase is important for cancer metabolism and tumour growth. Nature 2008, 452:230-233.
50. Perl A., Hanczko R., Telarico T., Oaks Z., Landas S. Oxidative stress, inflammation and carcinogenesis are controlled through the pentose phosphate pathway by transaldolase. Trends Mol. Med. 2011, 17:395-403.
51. Rosanna S.C.Cedrola, La Porta Caterina A.M. Effect of glucose stress conditions in BL6T murine melanoma cells. Melanoma Res. 2004, 14:345-351.
52. Wang N., Stamenovic D. Mechanics of vimentin intermediate filaments. J. Muscle Res. Cell Motil. 2002, 23:535-540.
53. Paron I., D'Elia A., D'Ambrosio C., Scaloni A., D'Aurizio F., Prescott A., Damante G., Tell G. A proteomic approach to identify early molecular targets of oxidative stress in human epithelial lens cells. Biochem. J. 2004, 378:929-937.
54. Yang X., Wang J., Liu C., Grizzle W.E., Yu S., Zhang S., Barnes S., Koopman W.J., Mountz J.D., Kimberly R.P., Zhang H.-G. Cleavage of p53-vimentin complex enhances tumor necrosis factor-related apoptosis-inducing ligand-mediated apoptosis of rheumatoid arthritis synovial fibroblasts. Am. J. Pathol. 2005, 167:705-719.
55. Sheikh M.S., Fornace A.J. Death and decoy receptors and p53-mediated apoptosis. Leukemia 2000, 14:1509-1513.
56. Cuezva J., Sánchez-Aragó M., Sala S., Blanco-Rivero A., Ortega Á. A message emerging from development: the repression of mitochondrial Β-F1-ATPase expression in cancer. J. Bioenerg. Biomembr. 2007, 39:259-265.
57. 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. Pigm. Cell Melanoma Res. 2009, 22:740-749.