Astaxanthin and withaferin A block paracrine cytokine interactions between UVB-exposed human keratinocytes and human melanocytes via the attenuation of endothelin-1 secretion and its downstream intracellular signaling

Cytokine

Volumn 73, Issue 2, 2015, Pages 184-197

  Niwano, Takao ^a,b   Terazawa, Shuko ^c   Nakajima, Hiroaki ^b   Wakabayashi, Yuki ^b   Imokawa, Genji ^b,c  

^a Mitsui Eng Shipbuilding Co Ltd   (Japan)

^b TOKYO UNIVERSITY OF TECHNOLOGY   (Japan)

^c CHUBU UNIVERSITY   (Japan)

Author keywords

Endothelin 1; Keratinocytes; Melanocytes; Paracrine interaction; Tyrosinase

Indexed keywords

ALPHA INTERMEDIN; ASTAXANTHIN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; ENDOTHELIN 1; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 1ALPHA; INTERLEUKIN 6; INTERLEUKIN 8; MICROPHTHALMIA ASSOCIATED TRANSCRIPTION FACTOR; MITOGEN ACTIVATED PROTEIN KINASE; MONOPHENOL MONOOXYGENASE; PROTEIN KINASE C; RAF PROTEIN; TYROSINASE RELATED PROTEIN 1; WITHAFERIN A; ANTIBODY; CALCIUM; CYTOKINE; DITHIOTHREITOL; WITHANOLIDE; XANTHOPHYLL;

ARTICLE; BINDING SITE; CATALYSIS; CELL CULTURE; CONTROLLED STUDY; CYTOKINE RELEASE; DOWN REGULATION; DRUG MECHANISM; DRUG PROTEIN BINDING; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE ACTIVITY; GENE EXPRESSION REGULATION; GENE REPRESSION; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; KERATINOCYTE; MELANOCYTE; MICROPHTHALMIA ASSOCIATED TRANSCRIPTION FACTOR GENE; PARACRINE SIGNALING; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RADIATION EXPOSURE; REAL TIME POLYMERASE CHAIN REACTION; TYROSINASE GENE; TYROSINASE RELATED PROTEIN 1 GENE; UPREGULATION; WESTERN BLOTTING; COCULTURE; CYTOLOGY; DRUG EFFECTS; INTRACELLULAR SPACE; MELANOMA; METABOLISM; PATHOLOGY; PHOSPHORYLATION; RADIATION RESPONSE; SECRETION (PROCESS); SIGNAL TRANSDUCTION; TUMOR CELL LINE; ULTRAVIOLET RADIATION;

ANTIBODIES; CALCIUM; CELL LINE, TUMOR; COCULTURE TECHNIQUES; CYTOKINES; DITHIOTHREITOL; ENDOTHELIN-1; GENE EXPRESSION REGULATION; HUMANS; INTRACELLULAR SPACE; KERATINOCYTES; MELANOCYTES; MELANOMA; MONOPHENOL MONOOXYGENASE; PARACRINE COMMUNICATION; PHOSPHORYLATION; SIGNAL TRANSDUCTION; ULTRAVIOLET RAYS; WITHANOLIDES; XANTHOPHYLLS;

EID: 84924676684     PISSN: 10434666     EISSN: 10960023     Source Type: Journal    
DOI: 10.1016/j.cyto.2015.02.006     Document Type: Article

References (73)

1. Terazawa S., Nakajima H., Mori S., Niwano T., Imokawa G. Astaxanthin attenuates the UVB-induced secretion of prostaglandin E2 and interleukin-8 in human keratinocytes by interrupting MSK1 phosphorylation in a ROS depletion-independent manner. Exp Dermatol 2012, 21(Suppl. 1):11-17.
2. Imokawa G., Yada Y., Miyagishi M. Endothelins secreted from human keratinocytes are intrinsic mitogens for human melanocytes. J Biol Chem 1992, 267:24675-24680.
3. Imokawa G., Miyagishi M., Yada Y. Endothelin-1 as a new melanogen: coordinated expression of its gene and the tyrosinase gene in UVB-exposed human epidermis. J Invest Dermatol 1995, 105:32-37.
4. Imokawa G., Kobayashi T., Miyagishi M., Higashi K., Yada Y. The role of endothelin-1 in epidermal hyperpigmentation and signaling mechanisms of mitogenesis and melanogenesis. Pigment Cell Res 1997, 10:218-228.
5. Hachiya A., Kobayashi A., Yoshida Y., Kitahara T., Takema Y., Imokawa G. Biphasic expression of two paracrine melanogenic cytokines, stem cell factor and endothelin-1, in ultraviolet B-induced human melanogenesis. Am J Pathol 2004, 165:2099-2109.
6. Hachiya A., Kobayashi A., Ohuchi A., Takema Y., Imokawa G. The paracrine role of stem cell factor/c-kit signaling in the activation of human melanocytes in ultraviolet-B-induced pigmentation. J Invest Dermatol 2001, 116:578-586.
7. Abdel-Malek Z., Swope V.B., Suzuki I., Akcali C., Harriger M.D., Boyce S.T., Urabe K., Hearing V.J. Mitogenic and melanogenic stimulation of normal human melanocytes by melanotropic peptides. Proc Natl Acad Sci USA 1995, 92:1789-1793.
8. Suzuki I., Cone R.D., Im S., Nordlund J., Abdel-Malek Z.A. Binding of melanotropic hormones to the melanocortin receptor MC1R on human melanocytes stimulates proliferation and melanogenesis. Endocrinology 1996, 137:1627-1633.
9. Imokawa G., Yada Y., Morisaki N., Kimura M. Granulocyte/macrophage-colony-stimulatory factor is an intrinsic keratinocyte-derived growth factor for human melanocytes in UVA-induced melanosis. Biochem J 1996, 313:625-631.
10. Kadono S., Manak I., Kawashima M., Kobayashi T., Imokawa G. The role of the epidermal endothelin cascade in the hyperpigmentation mechanism of lentigo senilis. J Invest Dermatol 2001, 116:571-577.
11. Hattori H., Kawashima M., Ichikawa Y., Imokawa G. The epidermal stem cell factor is over-expressed in lentigo senilis: implication for the mechanism of hyperpigmentation. J Invest Dermatol 2004, 122:1256-1265.
12. Kang H.Y., Hwang J.S., Lee J.Y., Ahn J.H., Kim J.Y., Lee E.S., Kang W.H. The dermal stem cell factor and c-kit are overexpressed in melasma. Br J Dermatol 2006, 154:1094-1099.
13. Chung K.W., Park Y.J., Choi Y.J., Park M.H., Ha Y.M., Uehara Y., Yoon J.H., Chun P., Moon H.R., Chung H.Y. 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 2012, 1820:962-969.
14. Vontzalidou A., Zoidis G., Chaita E., Makropoulou M., Aligiannis N., Lambrinidis G., Mikros E., Skaltsounis A.L. Design, synthesis and molecular simulation studies of dihydrostilbene derivatives as potent tyrosinase inhibitors. Bioorg Med Chem Lett 2012, 22:5523-5526.
15. Emami S., Hosseinimehr S.J., Shahrbandi K., Enayati A.A., Esmaeeli Z. Synthesis and evaluation of 2(3H)-thiazole thiones as tyrosinase inhibitors. Arch Pharm 2012, 345:629-637.
16. Cha S.H., Ko S.C., Kim D., Jeon Y.J. Screening of marine algae for potential tyrosinase inhibitor: those inhibitors reduced tyrosinase activity and melanin synthesis in zebrafish. J Dermatol 2011, 38:354-363.
17. An S.M., Koh J.S., Boo Y.C. p-Coumaric acid not only inhibits human tyrosinase activity in vitro but also melanogenesis in cells exposed to UVB. Phytother Res 2010, 24:1175-1180.
18. Noh J.M., Kwak S.Y., Kim D.H., Lee Y.S. Kojic acid-tripeptide amide as a new tyrosinase inhibitor. Biopolymers 2007, 88:300-307.
19. Ando H., Funasaka Y., Oka M., Ohashi A., Furumura M., Matsunaga J., Matsunaga N., Hearing V.J., Ichihashi M. Possible involvement of proteolytic degradation of tyrosinase in the regulatory effect of fatty acids on melanogenesis. J Lipid Res 1999, 40:1312-1316.
20. Paine C., Sharlow E., Liebel F., Eisinger M., Shapiro S., Seiberg M. An alternative approach to depigmentation by soybean extracts via inhibition of the PAR-2 pathway. J Invest Dermatol 2001, 116:587-595.
21. Lavie D., Glotter E., Shvo Y. Constituents of Withania somnifera. Dun. III. The side chain of withaferin A. J Org Chem 1965, 30:1774-1778.
22. Samadi A.K., Cohen S.M., Mukerji R., Chaguturu V., Zhang X., Timmermann B.N., Cohen M.S., Person E.A. Natural withanolide withaferin A induces apoptosis in uveal melanoma cells by suppression of Akt and c-MET activation. Tumour Biol 2012, 33:1179-1189.
23. Yang H., Shi G., Dou Q.P. The tumor proteasome is a primary target for the natural anticancer compound Withaferin A isolated from "Indian winter cherry". Mol Pharmacol 2007, 71:426-437.
24. Adams J.D., Yang J., Mishra L.C., Singh B.B. Effects of ashwagandha in a rat model of stroke. Altern Ther Health Med 2002, 8:18-19.
25. Malik F., Singh J., Khajuria A., Suri K.A., Satti N.K., Singh S., Kaul M.K., Kumar A., Bhatia A., Qazi G.N. 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 2007, 8:1525-1538.
26. Srinivasan S., Ranga R.S., Burikhanov R., Han S.S., Chendil D. Par-4-dependent apoptosis by the dietary compound withaferin A in prostate cancer cells. Cancer Res 2007, 67:246-253.
27. Koduru S., Kumar R., Srinivasan S., Evers M.B., Damodaran C. Notch-1 inhibition by Withaferin-A: a therapeutic target against colon carcinogenesis. Mol Cancer Ther 2010, 9:202-210.
28. Mohan R., Hammers H.J., Bargagna-Mohan P., Zhan X.H., Herbstritt C.J., Ruiz A., Zhang L., Hanson A.D., Conner B.P., Rougas J., Pribluda V.S. Withaferin A is a potent inhibitor of angiogenesis. Angiogenesis 2004, 7:115-122.
29. Prasanna K.S., Shilpa P., Salimath B.P. Withaferin A suppresses the expression of vascular endothelial growth factor in Ehrlich ascites tumor cells via Sp1 transcription factor. Curr Trends Biotechnol Pharm 2009, 3:138-148.
30. Kaileh M., Vanden B.W., Heyerick A., Horion J., Piette J., Libert C., De Keukeleire D., Essawi T., Haegeman G. Withaferin A strongly elicits IkappaB kinase beta hyperphosphorylation concomitant with potent inhibition of its kinase activity. J Biol Chem 2007, 282:4253-4264.
31. Kurashige M., Okimasu E., Inoue M., Utsumi K. Inhibition of oxidative injury of biological membranes by astaxanthin. Physiol Chem Phys Med NMR 1990, 22:27-38.
32. Miki W. Biological functions and activities of animal carotenoids. Pure Appl Chem 1991, 63:141-146.
33. Hussein G., Sankawa N., Goto H., Matsumoto K., Watanabe H. Astaxanthin, a carotenoid with potential in human health and nutrition. J Nat Prod 2006, 69:443-449.
34. Palozza P., Krinsky N.I. Astaxanthin and canthaxanthin are potent antioxidants in a membrane mode. Arch Biochem Biophys 1992, 297:291-295.
35. Mortensen A., Skibsted L., Sampson J., Rice-Evance C., Everett S.A. Comparative mechanisms and rates of free radical scavenging by carotenoid antioxidants. FEBS Lett 1997, 418:91-97.
36. Suganuma K., Nakajima H., Otsuki M., Imokawa G. Astaxanthin attenuates the UVA-induced up-regulation of matrix-metalloproteinase-1 and skin fibroblast elastase in human dermal fibroblasts. J Dermatol Sci 2010, 58:136-142.
37. Nakajima H., Ezaki Y., Nagai T., Yoshioka R., Imokawa G. Epithelial-mesenchymal interaction during UVB-induced up-regulation of neutral endopeptidase. Biochem J 2012, 443:297-305.
38. Sato-Jin K., Nishimura E.K., Akasaka E., Huber W., Nakano H., Miller A., Du J., Wu M., Hanada K., Sawamura D., Fisher D.E., Imokawa G. Epistatic connections between MITF and endothelin signaling in Waardenburg syndrome and other pigmentary disorders. FASEB J 2008, 22:1155-1168.
39. Nakajima H., Wakabayashi Y., Wakamatsu K., Imokawa G. An extract of Withania somnifera attenuates endothelin-1-stimulated pigmentation in human epidermal equivalents through the interruption of PKC activity within melanocytes. Phytother Res 2011, 25:1398-1411.
40. Terazawa S., Nakajima H., Fukasawa K., Imokawa G. Withaferin A abolishes the stem cell factor-stimulated pigmentation of human epidermal equivalents by interrupting the autophosphorylation of c-KIT in human melanocytes. Arch Dermatol Res 2015, 307:73-88.
41. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Meth 1983, 65:55-63.
42. Nakajima H., Fukazawa K., Wakabayashi Y., Wakamatsu K., Imokawa G. Withania somnifera extract attenuates stem cell factor-stimulated pigmentation in human epidermal equivalent through interruption of ERK phosphorylation within melanocytes. J Nat Med 2012, 66:435-446.
43. Winder A.J., Harris H. New assays for the tyrosine hydroxylase and dopa oxidase activities of tyrosinase. Eur J Biochem 1991, 198:317-326.
44. Nakajima H., Fukazawa K., Wakabayashi Y., Wakamatsu K., Senda K., Imokawa G. Abrogating effect of a xanthophyll carotenoid astaxanthin on the stem cell factor-induced stimulation of human epidermal pigmentation. Arch Dermatol Res 2012, 304:803-816.
45. Nakajima H., Wakabayashi Y., Wakamatsu K., Imokawa G. 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 2011, 303:263-276.
46. Yada Y., Higuchi K., Imokawa G. Effects of endothelins on signal transduction and proliferation in human melanocytes. J Biol Chem 1991, 266:18352-18357.
47. Yokota Y., Bargagna-Mohan P., Ravindranath P.P., Kim K.B., Mohan R. Development of withaferin A analogs as probes of angiogenesis. Bioorg Med Chem Lett 2006, 16:2603-2607.
48. Rosazza J.P., Nicholas A.W., Gustafson M.E. Microbial transformations of natural antitumor agents. 7. 14-alpha-Hydroxylation of withaferin-A by Cunninghamella elegans (NRRL 1393). Steroids 1978, 31:671-679.
49. Shishido E., Kadono S., Manaka I., Kawashima M., Imokawa G. The mechanism of epidermal hyperpigmentation in dermatofibroma is associated with stem cell factor and hepatocyte growth factor expression. J Invest Dermatol 2001, 117:627-633.
50. Okazaki M., Yoshimura K., Suzuki Y., Uchid G., Kitano Y., Harii K., Imokawa G. The mechanism of epidermal hyperpigmentation in Café-Au-Lait Macules of neurofibromatosis type-1 (von Recklinghausen's Disease) may be associated with dermal fibroblast-derived stem cell factor and hepatocyte growth factor. Br J Dermatol 2003, 148:689-697.
51. Imokawa G., Yada Y., Kimura M. Signalling mechanisms of endothelin-induced mitogenesis and melanogenesis in human melanocytes. Biochem J 1996, 314:305-312.
52. Kolch W., Heidecker G., Kochs G., Hummel R., Vahidi H., Mischak H., Finkenzeller G., Marme D., Rapp U.R. Protein kinase Cα activates RAF-1 by direct phosphorylation. Nature 1993, 364:249-252.
53. Schonwasser D.C., Marais R.M., Marshall C.J., Parker P.J. Activation of the mitogen-activated protein kinase/extracellular signal-regulated kinase pathway by conventional, novel, and atypical protein kinase C isotypes. Mol Cell Biol 1998, 18:790-798.
54. Mason C.S., Springer C.J., Cooper R.G., Superti-Furga G., Marshall C.J., Marais R. Serine and tyrosine phosphorylations cooperate in Raf-1, but not B-Raf activation. EMBO J 1999, 18:2137-2148.
55. Marais R., Light Y., Mason C., Paterson H., Olson M.F., Marshall C.J. Requirement of Ras-GTP-Raf complexes for activation of Raf-1 by protein kinase C. Science 1998, 280:109-112.
56. Imokawa G., Kobayasi T., Miyagishi M. 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 2000, 275:33321-33328.
57. Wan P., Hu Y., He L. Regulation of melanocyte pivotal transcription factor MITF by some other transcription factors. Mol Cell Biochem 2011, 354:241-246.
58. Potterf S.B., Furumura M., Dunn K.J., Arnheiter H., Pavan W.J. Transcription factor hierarchy in Waardenburg syndrome: regulation of MITF expression by SOX10 and PAX3. Hum Genet 2000, 107:1-6.
59. Hemesath T.J., Price E.R., Takemoto C., Badalian T., Fisher D.E. MAP kinase links the transcription factor Microphthalmia to c-Kit signalling in melanocytes. Nature 1998, 391:298-301.
60. Shin H.M., Lee Y.R., Chang Y.S., Lee J.Y., Kim B.H., Min K.R., Kim Y. Suppression of interleukin-6 production in macrophages by furonaphthoquinone NFD-37. Int Immunopharmacol 2006, 6:916-923.
61. Ueda K., Usui T., Nakayama H., Ueki M., Takio K., Ubukata M., Osada H. 4-Isoavenaciolide covalently binds and inhibits VHR, a dual-specificity phosphatase. FEBS Lett 2002, 525:48-52.
62. Rahmouni S., Cerignoli F., Alonso A., Tsutji T., Henkens R., Zhu C., Louis-dit-Sully C., Moutschen M., Jiang W., Mustelin T. Loss of the VHR dual-specific phosphatase causes cell-cycle arrest and senescence. Nat Cell Biol 2006, 8:524-531.
63. Vasudevan S.A., Skoko J., Wang K., Burlingame S.M., Patel P.N., Lazo J.S., Nuchtern J.G., Yang J. MKP-8, a novel MAPK phosphatase that inhibits p38 kinase. Biochem Biophys Res Commun 2005, 330:511-518.
64. Peyregne V.P., Kar S., Ham S.W., Wang M., Wang Z., Carr B.I. Novel hydroxyl naphthoquinones with potent Cdc25 antagonizing and growth inhibitory properties. Mol Cancer Ther 2005, 4:595-602.
65. 2 sensitivity of the major constitutive MAPK phosphatase from rat brain. Biochem Biophys Res Commun 2004, 315:568-574.
66. Prajapati S., Verma U., Yamamoto Y., Kwak Y.T., Gaynor R.B. Protein phosphatase 2Cbeta association with the IkappaB kinase complex is involved in regulating NF-kappaB activity. J Biol Chem 2004, 279:1739-1746.
67. Reynaert N.L., van der Vliet A., Guala A.S., McGovern T., Hristova M., Pantano C., Heintz N.H., Heim J., Ho Y.S., Matthews D.E., Wouters E.F., Janssen-Heininger Y.M. Dynamic redox control of NF-kappaB through glutaredoxin-regulated S-glutathionylation of inhibitory kappaB kinase beta. Proc Natl Acad Sci USA 2006, 103:13086-13091.
68. Codreanu S.G., Adams D.G., Dawson E.S., Wadzinski B.E., Liebler D.C. Inhibition of protein phosphatase 2A activity by selective electrophile alkylation damage. Biochemistry 2006, 45:10020-10029.
69. Humphries K.M., Deal M.S., Taylor S.S. Enhanced dephosphorylation of cAMP-dependent protein kinase by oxidation and thiol modification. J Biol Chem 2005, 280:2750-2758.
70. Seth D., Rudolph J. Redox regulation of MAP kinase phosphatase 3. Biochemistry 2006, 45:8476-8487.
71. Chi H., Barry S.P., Roth R.J., Wu J.J., Jones E.A., Bennett A.M., Flavell R.A. Dynamic regulation of pro- and anti-inflammatory cytokines by MAPK phosphatase 1 (MKP-1) in innate immune responses. Proc Natl Acad Sci USA 2006, 103:2274-2279.
72. Salojin K.V., Owusu I.B., Millerchip K.A., Potter M., Platt K.A., Oravecz T. Essential role of MAPK phosphatase-1 in the negative control of innate immune responses. J Immunol 2006, 176:1899-1907.
73. Kray A.E., Carter R.S., Pennington K.N., Gomez R.J., Sanders L.E., Llanes J.M., Khan W.N., Ballard D.W., Wadzinski B.E. Positive regulation of IkappaB kinase signaling by protein serine/threonine phosphatase 2A. J Biol Chem 2005, 280:35974-35982.