Withaferin A abolishes the stem cell factor-stimulated pigmentation of human epidermal equivalents by interrupting the auto-phosphorylation of c-KIT in human melanocytes

Archives of Dermatological Research

Volumn 307, Issue 1, 2014, Pages 73-88

  Terazawa, Shuko ^a   Nakajima, Hiroaki ^b   Fukasawa, Katsunori ^b   Imokawa, Genji ^a  

^a CHUBU UNIVERSITY   (Japan)

^b TOKYO UNIVERSITY OF TECHNOLOGY   (Japan)

Author keywords

Anti pigmentation; Human epidermal equivalents; Intracellular signaling; Melanocytes; Stem cell factor; Tyrosinase

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; DITHIOTHREITOL; DOPACHROME TAUTOMERASE; ENZYME; EUMELANIN; MELANIN; MELANOCYTE PROTEIN PMEL 17; MICROPHTHALMIA ASSOCIATED TRANSCRIPTION FACTOR; MITOGEN ACTIVATED PROTEIN KINASE; MONOPHENOL MONOOXYGENASE; PROTEIN SHC; RAF PROTEIN; STEM CELL FACTOR; TYROSINASE RELATED PROTEIN 1; WITHAFERIN A; WITHANIA SOMNIFERA EXTRACT; DEPIGMENTING AGENT; PROTEIN BINDING; STEM CELL FACTOR RECEPTOR; WITHANOLIDE;

ALKYLATION; ARTICLE; CELL LYSATE; CELL VIABILITY; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; EPIDERMIS; GENE EXPRESSION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; HUMAN EPIDERMAL EQUIVALENT; INTRACELLULAR SIGNALING; MELANOCYTE; MICHAEL ADDITION; MTT ASSAY; NORMAL HUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; SKIN PIGMENTATION; THIOALKYLATION; UPREGULATION; WESTERN BLOTTING; BIOSYNTHESIS; CELL CULTURE; COCULTURE; CYTOLOGY; DOSE RESPONSE; DRUG EFFECTS; ENZYME ACTIVATION; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHOSPHORYLATION; SIGNAL TRANSDUCTION; TIME;

CELLS, CULTURED; COCULTURE TECHNIQUES; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME ACTIVATION; EPIDERMIS; GENE EXPRESSION REGULATION; HUMANS; MELANINS; MELANOCYTES; MONOPHENOL MONOOXYGENASE; PHOSPHORYLATION; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS C-KIT; SIGNAL TRANSDUCTION; SKIN LIGHTENING PREPARATIONS; SKIN PIGMENTATION; STEM CELL FACTOR; TIME FACTORS; WITHANOLIDES;

EID: 84924698529     PISSN: 03403696     EISSN: 1432069X     Source Type: Journal    
DOI: 10.1007/s00403-014-1518-y     Document Type: Article

References (73)

1. Abdel-Malek Z, Swope VB, Suzuki I, Akcali C, Harriger MD, Boyce ST, Urabe K, Hearing VJ (1995) Mitogenic and melanogenic stimulation of normal human melanocytes by melanotropic peptides. Proc Natl Acad Sci USA 92:1789-1793
2. Adams JD Jr, Yang J, Mishra LC, Singh BB (2002) Effects of Ashwagandha in a rat model of stroke. Altern Ther Health Med 8:18-19
3. An SM, Koh JS, Boo YC (2010) p-Coumaric acid not only inhibits human tyrosinase activity in vitro but also melanogenesis in cells exposed to UVB. Phytother Res 24:1175-1180
4. Ando H, Funasaka Y, Oka M, Ohashi A, Furumura M, Matsunaga J, Matsunaga N, Hearing VJ, Ichihashi M (1999) Possible involvement of proteolytic degradation of tyrosinase in the regulatory effect of fatty acids on melanogenesis. J Lipid Res 40:1312-1316
5. Bentley NJ, Eisen T, Goding CR (1994) Melanocyte-specific expression of the human tyrosinase promoter: activation by the microphthalmia gene product and role of the initiator. Mol Cell Biol 14:7996-8006
6. Bernier M, Kwon YK, Pandey SK, Zhu TN, Zhao RJ, Maciuk A, He HJ, Decabo R, Kole S (2006) Binding of manumycin A inhibits IkappaB kinase beta activity. J Biol Chem 281:2551-2561
7. Bertolotto C, Buscà R, Abbe P, Bille K, Aberdam E, Ortonne JP, Ballotti R (1998) Different cis-acting elements are involved in the regulation of TRP1 and TRP2 promoter activities by cyclic AMP: pivotal role of M boxes (GTCATGTGCT) and of microphthalmia. Mol Cell Biol 18:694-702
8. Blume-Jensen P, Claesson-Welsh L, Siegbahn A, Zsebo KM, Westermark B, Heldin CH (1991) Activation of the human c-kit product by ligand-induced dimerization mediates circular actin reorganization and chemotaxis. EMBO J 10:4121-4128
9. Cha SH, Ko SC, Kim D, Jeon YJ (2011) Screening of marine algae for potential tyrosinase inhibitor: those inhibitors reduced tyrosinase activity and melanin synthesis in zebrafish. J Dermatol 38:354-363
10. Chi H, Barry SP, Roth RJ, Wu JJ, Jones EA, Bennett AM, Flavell RA (2006) Dynamic regulation of pro-and anti-inflammatory cytokines by MAPK phosphatase 1 (MKP-1) in innate immune responses. Proc Natl Acad Sci USA 103:2274-2279
11. Chung KW, Park YJ, Choi YJ, Park MH, Ha YM, Uehara Y, Yoon JH, Chun P, Moon HR, Chung HY (2012) Evaluation of in vitro and in vivo anti-melanogenic activity of a newly synthesized strong tyrosinase inhibitor (E)-3-(2,4 dihydroxybenzylidene) pyrrolidine-2,5-dione (3-DBP). Biochim Biophys Acta 1820:962-969
12. Codreanu SG, Adams DG, Dawson ES, Wadzinski BE, Liebler DC (2006) Inhibition of protein phosphatase 2A activity by selective electrophile alkylation damage. Biochemistry 45:10020-10029
13. Cutler RL, Liu L, Damen JE, Krystal G (1993) Multiple cytokines induce the tyrosine phosphorylation of Shc and its association with Grb2 in hemopoietic cells. J Biol Chem 268:21463-21465
14. Du J, Miller AJ, Widlund HR, Horstmann MA, Ramaswamy S, Fisher DE (2003) MLANA/MART1and SILV/PMEL17/GP100 are transcriptionally regulated by MITF in melanocytes and melanoma. Am J Pathol 163:333-343
15. Emami S, Hosseinimehr SJ, Shahrbandi K, Enayati AA, Esmaeeli Z (2012) Synthesis and evaluation of 2(3H)-thiazole thiones as tyrosinase inhibitors. Arch Pharm 345:629-637
16. 2sensitivity of the major constitutive MAPK phosphatase from rat brain. Biochem Biophys Res Commun 315:568-574
17. Green H (1978) Cyclic AMP in relation to proliferation of the epidermal cell: new view. Cell 15:801-811
18. Hachiya A, Kobayashi A, Ohuchi A, Takema Y, Imokawa G (2001) The paracrine role of stem cell factor/c-kit signaling in the activation of human melanocytes in ultraviolet-B-induced pigmentation. J Invest Dermatol 116:578-586
19. Hachiya A, Kobayashi A, Yoshida Y, Kitahara T, Takema Y, Imokawa G (2004) Biphasic expression of two paracrine melanogenic cytokines, stem cell factor and endothelin-1, in ultraviolet B-induced human melanogenesis. Am J Pathol 165:2099-2109
20. Hattori H, Kawashima M, Ichikawa Y, Imokawa G (2004) The epidermal stem cell factor is over-expressed in lentigo senilis: implication for the mechanism of hyperpigmentation. J Invest Dermatol 122:1256-1265
21. Hehner SP, Hofmann TG, Dröge W, Schmitz ML (1999) The antiinflammatory sesquiterpene lactone parthenolide inhibits NFkappa B by targeting the I kappa B kinase complex. J Immunol 163:5617-5623
22. Hemesath TJ, Price ER, Takemoto C, Badalian T, Fisher DE (1998) MAP kinase links the transcription factor Microphthalmia to c-Kit signalling in melanocytes. Nature 391:298-301
23. Humphries KM, Deal MS, Taylor SS (2005) Enhanced dephosphorylation of cAMP-dependent protein kinase by oxidation and thiol modification. J Biol Chem 280:2750-2758
24. Imokawa G, Yada Y, Miyagishi M (1992) Endothelins secreted from human keratinocytes are intrinsic mitogens for human melanocytes. J Biol Chem 267:24675-24680
25. Imokawa G, Miyagishi M, Yada Y (1995) Endothelin-1 as a new melanogen: coordinated expression of its gene and the tyrosinase gene in UVB-exposed human epidermis. J Invest Dermatol 105:32-37
26. Imokawa G, Yada Y, Kimura M (1996) Signalling mechanisms of endothelin-induced mitogenesis and melanogenesis in human melanocytes. Biochem J 314:305-312
27. Imokawa G, Kobayashi T, Miyagishi M, Higashi K, Yada Y (1997) The role of endothelin-1 in epidermal hyperpigmentation and signaling mechanisms of mitogenesis and melanogenesis. Pigment Cell Res 10:218-228
28. Imokawa G, Kobayasi T, Miyagishi M (2000) Intracellular signaling mechanisms leading to synergistic effects of endothelin-1 and stem cell factor on proliferation of cultured human melanocytes. Cross-talk via trans-activation of the tyrosine kinase c-kit receptor. J Biol Chem 275:33321-33328
29. Ito S, Nakanishi Y, Valenzuela RK, Brilliant MH, Kolbe L, Wakamatsu K (2011) Usefulness of alkaline hydrogen peroxide oxidation to analyze eumelanin and pheomelanin in various tissue samples: application to chemical analysis of human hair melanins. Pigment Cell Mel Res 24:605-613
30. Kadono S, Manak I, Kawashima M, Kobayashi T, Imokawa G (2001) The role of the epidermal endothelin cascade in the hyperpigmentation mechanism of lentigo senilis. J Invest Dermatol 116:571-577
31. Kaileh M, Vanden BW, Heyerick A, Horion J, Piette J, Libert C, De Keukeleire D, Essawi T, Haegeman G (2007) Withaferin A strongly elicits IkappaB kinase beta hyperphosphorylation concomitant with potent inhibition of its kinase activity. J Biol Chem 282:4253-4264
32. Koduru S, Kumar R, Srinivasan S, Evers MB, Damodaran C (2010) Notch-1 inhibition by Withaferin-A: a therapeutic target against colon carcinogenesis. Mol Cancer Ther 9:202-210
33. Kray AE, Carter RS, Pennington KN, Gomez RJ, Sanders LE, Llanes JM, Llanes JM, Khan WN, Ballard DW, Wadzinski BE (2005) Positive regulation of IkappaB kinase signaling by protein serine/threonine phosphatase 2A. J Biol Chem 280:35974-35982
34. Lavie D, Glotter E, Shvo Y (1965) Constituents of withania somnifera. Dun. III. The side chain of withaferin A. J Org Chem 30:1774-1778
35. Lennartsson J, Blume-Jensen P, Hermanson M, Pontén E, Carlberg M, Rönnstrand L (1999) Phosphorylation of Shc by Src family kinases is necessary for stem cell factor receptor/c-kit mediated activation of the Ras/MAP kinase pathway and c-fos induction. Oncogene 18:5546-5553
36. Liang MC, Bardhan S, Li C, Pace EA, Porco JA Jr, Gilmore TD (2003) Jesterone dimer, a synthetic derivative of the fungal metabolite jesterone, blocks activation of transcription factor nuclear factor kappaB by inhibiting the inhibitor of kappaB kinase. Mol Pharmacol 64:123-131
37. Liang MC, Bardhan S, Pace EA, Rosman D, Beutler JA, Porco JA Jr, Gilmore TD (2006) Inhibition of transcription factor NFkappaB signaling proteins IKKbeta and p65 through specific cysteine residues by epoxyquinone A monomer: correlation with its anti-cancer cell growth activity. Biochem Pharmacol 71:634-645
38. Liu L, Damen JE, Cutler RL, Krystal G (1994) Multiple cytokines stimulate the binding of a common 145-kilodalton protein to Shc at the Grb2 recognition site of Shc. Mol Cell Biol 14:6926-6935
39. Malik F, Singh J, Khajuria A, Suri KA, Satti NK, Singh S, Kaul MK, Kumar A, Bhatia A, Qazi GN (2007) A standardized root extract of Withania somnifera and its major constituent withanolide-A elicit humoral and cell-mediated immune responses by up regulation of Th1-dominant polarization in BALB/c mice. Life Sci 8:1525-1538
40. Mohan R, Hammers HJ, Bargagna-Mohan P, Zhan XH, Herbstritt CJ, Ruiz A, Zhang L, Hanson AD, Conner BP, Rougas J, Pribluda VS (2004) Withaferin A is a potent inhibitor of angiogenesis. Angiogenesisn 7:115-122
41. Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 6:55-63
42. Na HK, Surh YJ (2006) Transcriptional regulation via cysteine thiol modification: a novel molecular strategy for chemoprevention and cytoprotection. Mol Carcinog 45:368-380
43. Nakajima H, Wakabayashi Y, Wakamatsu K, Imokawa G (2011) An extract of Melia toosendan attenuates endothelin-1-stimulated pigmentation in human epidermal equivalents through the interruption of PKC activity within melanocytes. Arch Dermatol Res 303:263-276
44. Nakajima H, Wakabayashi Y, Wakamatsu K, Imokawa G (2011) An extract of Withania somnifera attenuates endothelin-1-stimulated pigmentation in human epidermal equivalents through the interruption of PKC activity within melanocytes. Phytother Res 25:1398-1411
45. Nakajima H, Fukazawa K, Wakabayashi Y, Wakamatsu K, Imokawa G (2012) Withania somnifera extract attenuates stem cell factor-stimulated pigmentation in human epidermal equivalents through interruption of ERK phosphorylation within melanocytes. J Nat Med 66:435-446
46. Nakajima H, Fukazawa K, Wakabayashi Y, Wakamatsu K, Senda K, Imokawa G (2012) Abrogating effect of a xanthophyll carotenoid astaxanthin on the stem cell factor-induced stimulation of human epidermal pigmentation. Arch Dermatol Res 304:803-816
47. Noh JM, Kwak SY, Kim DH, Lee YS (2007) Kojic acid-tripeptide amide as a new tyrosinase inhibitor. Biopolymers 88:300-307
48. Paine C, Sharlow E, Liebel F, Eisinger M, Shapiro S, Seiberg M (2001) An alternative approach to depigmentation by soybean extracts via inhibition of the PAR-2 pathway. J Invest Dermatol 116:587-595
49. Peyregne VP, Kar S, Ham SW, Wang M, Wang Z, Carr BI (2005) Novel hydroxyl naphthoquinones with potent Cdc25 antagonizing and growth inhibitory properties. Mol Cancer Ther 4:595-602
50. Potterf SB, Furumura M, Dunn KJ, Arnheiter H, Pavan WJ (2000) Transcription factor hierarchy in Waardenburg syndrome: regulation of MITF expression by SOX10 and PAX3. Hum Genet 107:1-6
51. Prajapati S, Verma U, Yamamoto Y, Kwak YT, Gaynor RB (2004) Protein phosphatase 2Cbeta association with the IkappaB kinase complex is involved in regulating NF-kappaB activity. J Biol Chem 279:1739-1746
52. Prasanna KS, Shilpa P, Salimath BP (2009) Withaferin A suppresses the expression of vascular endothelial growth factor in Ehrlich ascites tumor cells via Sp1 transcription factor. Curr Trends Biotech Pharm 3:138-148
53. Rahmouni S, Cerignoli F, Alonso A, Tsutji T, Henkens R, Zhu C, Louis-dit-Sully C, Moutschen M, Jiang W, Mustelin T (2006) Loss of the VHR dual-specific phosphatase causes cell-cycle arrest and senescence. Nat Cell Biol 8:524-531
54. Reynaert NL, van der Vliet A, Guala AS, McGovern T, Hristova M, Pantano C, Heintz NH, Heim J, Ho YS, Matthews DE, Wouters EF, Janssen-Heininger YM (2006) Dynamic redox control of NF-kappaB through glutaredoxin-regulated S-glutathionylation of inhibitory kappaB kinase beta. Proc Natl Acad Sci USA 103:13086-13091
55. Rheinwald JG, Green H (1975) Serial cultivation of strains of human epidermal keratinocytes: the formation of keratinizing colonies from single cells. Cell 6:331-344
56. Rosazza JP, Nicholas AW, Gustafson ME (1978) Microbial transformations of natural antitumor agents. 7. 14-alpha-Hydroxylation of withaferin-A by Cunninghamella elegans (NRRL 1393). Steroids 31:671-679
57. Samadi AK, Cohen SM, Mukerji R, Chaguturu V, Zhang X, Timmermann BN, Cohen MS, Person EA (2012) Natural withanolide withaferin A induces apoptosis in uveal melanoma cells by suppression of Akt and c-MET activation. Tumour Biol 33:1179-1189
58. Salojin KV, Owusu IB, Millerchip KA, Potter M, Platt KA, Oravecz T (2006) Essential role of MAPK phosphatase-1 in the negative control of innate immune responses. J Immunol 176:1899-1907
59. Sato-Jin K, Nishimura EK, Akasaka E, Huber W, Nakano H, Miller A, Du J, Wu M, Hanada K, Sawamura D, Fisher DE, Imokawa G (2008) Epistatic connections between MITF and endothelin signaling in Waardenburg syndrome and other pigmentary disorders. FASEB J 22:1155-1168
60. Seth D, Rudolph J (2006) Redox regulation of MAP kinase phosphatase 3. Biochemistry 45:8476-8487
61. Shin HM, Lee YR, Chang YS, Lee JY, Kim BH, Min KR, Kim Y (2006) Suppression of interleukin-6 production in macrophages by furonaphthoquinone NFD-37. Int Immunopharmacol 6:916-923
62. Srinivasan S, Ranga RS, Burikhanov R, Han SS, Chendil D (2007) Par-4-dependent apoptosis by the dietary compound withaferin A in prostate cancer cells. Cancer Res 67:246-253
63. Suzuki I, Cone RD, Im S, Nordlund J, Abdel-Malek ZA (1996) Binding of melanotropic hormones to the melanocortin receptor MC1R on human melanocytes stimulates proliferation and melanogenesis. Endocrinology 137:1627-1633
64. Troppmair J, Bruder JT, App H, Cai H, Liptak L, Szeberényi J (1992) Ras controls coupling of growth factor receptors and protein kinase C in the membrane to Raf-1 and B-Raf protein serine kinases in the cytosol. Oncogene 7:1867-1873
65. Ueda K, Usui T, Nakayama H, Ueki M, Takio K, Ubukata M, Osada H (2002) 4-Isoavenaciolide covalently binds and inhibits VHR, a dual-specificity phosphatase. FEBS Lett 525:48-52
66. Vasudevan SA, Skoko J, Wang K, Burlingame SM, Patel PN, Lazo JS, Nuchtern JG, Yang J (2005) MKP-8, a novel MAPK phosphatase that inhibits p38 kinase. Biochem Biophys Res Commun 330:511-518
67. Vontzalidou A, Zoidis G, Chaita E, Makropoulou M, Aligiannis N, Lambrinidis G, Mikros E, Skaltsounis AL (2012) Design, synthesis and molecular simulation studies of dihydrostilbene derivatives as potent tyrosinase inhibitors. Bioorg Med Chem Lett 22:5523-5526
68. Wan P, Hu Y, He L (2011) Regulation of melanocyte pivotal transcription factor MITF by some other transcription factors. Mol Cell Biochem 354:241-246
69. Winder AJ, Harris H (1991) New assays for the tyrosine hydroxylase and dopa oxidase activities of tyrosinase. Eur J Biochem 198:317-326
70. Wood KW, Sarnecki C, Roberts TM, Blenis J (1992) Ras mediates nerve growth factor receptor modulation of three signaltransducing protein kinases: MAP kinase, Raf-1, and RSK. Cell 68:1041-1050
71. Yada Y, Higuchi K, Imokawa G (1991) Effects of endothelins on signal transduction and proliferation in human melanocytes. J Biol Chem 266:18352-18357
72. Yang H, Shi G, Dou QP (2007) The tumor proteasome is a primary target for the natural anticancer compound Withaferin A isolated from ''Indian winter cherry. Mol Pharmacol 71:426-437
73. Yokota Y, Bargagna-Mohan P, Ravindranath PP, Kim KB, Mohan R (2006) Development of withaferin A analogs as probes of angiogenesis. Bioorg Med Chem Lett 16:2603-2607