UVB stimulates the expression of endothelin B receptor in human melanocytes via a sequential activation of the p38/MSK1/CREB/MITF pathway which can be interrupted by a French maritime pine bark extract through a direct inactivation of MSK1

PLoS ONE

Volumn 10, Issue 6, 2015, Pages

  Tagashira, Hideki ^a   Miyamoto, Aki ^a   Kitamura, Sei Ichi ^a   Tsubata, Masahito ^a   Yamaguchi, Kazuya ^a   Takagaki, Kinya ^a   Imokawa, Genji ^b  

^a Toyo Shinyaku Co Ltd   (Japan)

^b CHUBU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; ENDOTHELIN B RECEPTOR; FRENCH MARITIME PINE BARK EXTRACT; MICROPHTHALMIA ASSOCIATED TRANSCRIPTION FACTOR; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; MSK1 PROTEIN; N [2 (4 BROMOCINNAMYLAMINO)ETHYL] 5 ISOQUINOLINESULFONAMIDE; PLANT EXTRACT; PROTEIN SERINE THREONINE KINASE; S6 KINASE; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG; CREB1 PROTEIN, HUMAN; EDNRB PROTEIN, HUMAN; ENDOTHELIN; MELANIN; MITF PROTEIN, HUMAN; MITOGEN AND STRESS-ACTIVATED PROTEIN KINASE 1;

ARTICLE; CELL STIMULATION; DOWN REGULATION; DRUG EFFECT; ENZYME ACTIVATION; ENZYME INACTIVATION; ENZYME PHOSPHORYLATION; GENE EXPRESSION; HUMAN; HUMAN CELL; MELANOCYTE; NORMAL HUMAN; PROTEIN EXPRESSION; ULTRAVIOLET B RADIATION; ADVERSE EFFECTS; BARK; CELL CULTURE; CHEMISTRY; DRUG EFFECTS; GENETICS; KERATINOCYTE; METABOLISM; PHOSPHORYLATION; PIGMENTATION; PINE; SIGNAL TRANSDUCTION; SKIN; ULTRAVIOLET RADIATION; UPREGULATION;

PINUS PINASTER;

CELLS, CULTURED; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; ENDOTHELINS; GENE EXPRESSION; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; KERATINOCYTES; MELANINS; MELANOCYTES; MICROPHTHALMIA-ASSOCIATED TRANSCRIPTION FACTOR; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; PIGMENTATION; PINUS; PLANT BARK; PLANT EXTRACTS; RECEPTOR, ENDOTHELIN B; RIBOSOMAL PROTEIN S6 KINASES, 90-KDA; SIGNAL TRANSDUCTION; SKIN; ULTRAVIOLET RAYS; UP-REGULATION;

EID: 84935019626     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0128678     Document Type: Article

References (68)

1. Imokawa G, Yada Y, Miyagishi M. Endothelins secreted from human keratinocytes are intrinsic mitogens for human melanocytes. J Biol Chem. 1992; 267: 24675-24680. PMID: 1280264
2. Tada A, Suzuki I, Im S, Davis MB, Cornelius J, Babcock G, et al. Endothelin-1 is a paracrine growth factor that modulates melanogenesis of human melanocytes and participates in their responses to ultraviolet radiation. Cell Growth Differ. 1998; 9: 575-584. PMID: 9690625
3. Yohn JJ, Morelli JG, Walchak SJ, Rundell KB, Norris DA, Zamora MR. Cultured human keratinocytes synthesize and secrete endothelin-1. J Invest Dermatol. 1993; 100: 23-26. PMID: 8423387
4. Yada Y, Higuchi K, Imokawa G. Effects of endothelins on signal transduction and proliferation in human melanocytes. J Biol Chem (1991) 266: 18352-18357. PMID: 1917960
5. Imokawa G, Yada Y, Kimura M. Signaling mechanisms of endothelin-induced mitogenesis and melanogenesis in human melanocytes. Biochem J. 1996; 314: 305-312. PMID: 8660299
6. Tada A, Pereira E, Beitner-Johnson D, Kavanagh R, Abdel-Malek ZA. Mitogen- and ultraviolet-B-induced signaling pathways in normal human melanocytes. J Invest Dermatol. 2002; 118: 316-322. PMID: 11841550
7. Mizutani Y, Hayashi N, Kawashima M, Imokawa GA. single UVB exposure increases the expression of functional KIT in human melanocytes by up-regulating MITF expression through the phosphorylation of p38/CREB. Arch Dermatol Res. 2010; 302: 283-294. doi: 10.1007/s00403-009-1007-x PMID: 19937254
8. Hou L, Panthier JJ, Arnheiter H. Signaling and transcriptional regulation in the neural crest-derived melanocyte lineage: interactions between KIT and MITF. Development. 2000; 127: 5379-5389. PMID: 11076759
9. Hou L, Arnheiter H, Pavan WJ. Interspecies difference in the regulation of melanocyte development by SOX10 and MITF. Proc Natl Acad Sci U S A. 2006; 103: 9081-9085. PMID: 16757562
10. Yang R, Zheng Y, Li L, Liu S, Burrows M, Wei Z, et al. Direct conversion of mouse and human fibroblasts to functional melanocytes by defined factors. Nat Commun. 2014; 5: 5807. doi: 10.1038/ncomms6807 PMID: 25510211
11. Carreira S, Liu B, Goding CR. The gene encoding the T-box factor Tbx2 is a target for the microphthalmia-associated transcription factor in melanocytes. J Biol Chem. 2000; 275: 21920-21927. PMID: 10770922
12. Vance KW, Carreira S, Brosch G, Goding CR. Tbx2 is overexpressed and plays an important role in maintaining proliferation and suppression of senescence in melanomas. Cancer Res. 2005; 65: 2260-2268. PMID: 15781639
13. Du J, Widlund HR, Horstmann MA, Ramaswamy S, Ross K, Huber WE, et al. Critical role of CDK2 for melanoma growth linked to its melanocyte-specific transcriptional regulation by MITF. Cancer Cell. 2004; 6: 565-576. PMID: 15607961
14. Carreira S, Goodall J, Aksan I, La Rocca SA, Galibert MD, Denat L, et al. Mitf cooperates with Rb1 and activates p21Cip1 expression to regulate cell cycle progression. Nature. 2005; 433: 764-769. PMID: 15716956
15. McGill GG, Horstmann M, Widlund HR, Du J, Motyckova G, Nishimura EK, et al. Bcl2 regulation by the melanocyte master regulator Mitf modulates lineage survival and melanoma cell viability. Cell. 2002; 109: 707-718. PMID: 12086670
16. Hornyak TJ, Jiang S, Guzmán EA, Scissors BN, Tuchinda C, He H, et al. Mitf dosage as a primary determinant of melanocyte survival after ultraviolet irradiation. Pigment Cell Melanoma Res. 2009; 22: 307-318. doi: 10.1111/j.1755-148X.2009.00551.x PMID: 19192212
17. Ganss R, Schütz G, Beermann F. The mouse tyrosinase gene. Promoter modulation by positive and negative regulatory elements. J Biol Chem. 1994; 269: 29808-29816. PMID: 7961973
18. Yasumoto K, Yokoyama K, Shibata K, Tomita Y, Shibahara S. Microphthalmia-associated transcription factor as a regulator for melanocyte-specific transcription of the human tyrosinase gene. Mol Cell Biol. 1994; 14: 8058-8070. PMID: 7969144
19. Vachtenheim J, Borovanský J. "Transcription physiology" of pigment formation in melanocytes: central role of MITF. Exp Dermatol. 2010; 19: 617-627. doi: 10.1111/j.1600-0625.2009.01053.x PMID: 20201954
20. 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. PMID: 7615973
21. 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. PMID: 9263329
22. Hyter S, Coleman DJ, Ganguli-Indra G, Merrill GF, Ma S, Yanagisawa M, et al. Endothelin-1 is a transcriptional target of p53 in epidermal keratinocytes and regulates ultraviolet-induced melanocyte homeostasis. Pigment Cell Melanoma Res. 2013; 26: 247-258. doi: 10.1111/pcmr.12063 PMID: 23279852
23. Yanagisawa M, Kurihara H, Kimura S, Tomobe Y, Kobayashi M, Mitsui Y, et al. A novel potent vasoconstrictor peptide produced by vascular endothelial cells. Nature. 1988; 332: 411-415. PMID: 2451132
24. Hachiya A, Kobayashi T, Takema Y, Imokawa G. Biochemical characterization of endothlein-converting enzyme-1alpha in cultured skin-derived cells and its postulated role in the stimulation of melanogenesis in human epidermis. J Biol Chem. 2002; 277: 5395-5403. doi: 10.1074/jbc.M105874200 PMID: 11723113
25. Sakurai T, Yanagisawa M, Takuwa Y, Miyazaki H, Kimura S, Goto K, et al. Cloning of a cDNA encoding a non-isopeptide-selective subtype of the endothelin receptor. Nature. 1990; 348: 732-735. PMID: 2175397
26. Read AP, Newton VE. Waardenburg syndrome. J Med Genet. 1997; 34: 656-665. PMID: 9279758
27. Brenner M, Coelho SG, Beer JZ, Miller SA, Wolber R, Smuda C, et al. Long-lasting molecular changes in human skin after repetitive in situ UV irradiation. J Invest Dermatol. 2009; 129: 1002-1011. doi: 10.1038/jid.2008.325 PMID: 18946495
28. Choi W, Miyamura Y, Wolber R, Smuda C, Reinhold W, Liu H, et al. Regulation of human skin pigmentation in situ by repetitive UV exposure: molecular characterization of responses to UVA and/or UVB. J Invest Dermatol. 2010; 130: 1685-1696. doi: 10.1038/jid.2010.5 PMID: 20147966
29. 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. PMID: 15579452
30. Kadono S, Manaka 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. PMID: 11286625
31. Sato-Jin K, Nishimura EK, Akasaka E, Huber W, Nakano H, Miller A, et al. Epistatic connections between microphthalmia-associated transcription factor and endothelin signaling in Waardenburg syndrome and other pigmentary disorders. FASEB J. 2008; 22: 1155-1168. PMID: 18039926
32. Smit N, Vicanova J, Pavel S. The hunt for natural skin whitening agents. Int J Mol Sci. 2009; 10: 5326-5349. doi: 10.3390/ijms10125326 PMID: 20054473
33. Li EPH, Hyun JM, Belk RW, Kimura J, Bahl S. Skin lightening and beauty in four asian cultures. Adv Consum Res. 2008; 35: 444-449.
34. Shimada T, Tokuhara D, Tsubata M, Kamiya T, Kamiya-Sameshima M, Nagamine R, et al. Flavangenol (pine bark extract) and its major component procyanidin B1 enhance fatty acid oxidation in fatloaded models. Eur J Pharmacol. 2012; 677: 147-153. doi: 10.1016/j.ejphar.2011.12.034 PMID: 22227333
35. Ohkita M, Kiso Y, Matsumura Y. Pharmacology in health foods: improvement of vascular endothelial function by French maritime pine bark extract (Flavangenol). J Pharmacol Sci. 2011; 115: 461-465. PMID: 21436602
36. Yoshida A, Yoshino F, Tsubata M, Ikeguchi M, Nakamura T, Lee MC. Direct assessment by electron spin resonance spectroscopy of the antioxidant effects of French maritime pine bark extract in the maxillofacial region of hairless mice. J Clin Biochem Nutr. 2011; 49: 79-86. doi: 10.3164/jcbn.10-103 PMID: 21980222
37. Rohdewald P. A review of the French maritime pine bark extract (Pycnogenol), a herbal medication with a diverse clinical pharmacology. Int J Clin Pharmacol Ther. 2002; 40: 158-168. PMID: 11996210
38. Maimoona A, Naeem I, Saddiqe Z, Jameel K. A review on biological, nutraceutical and clinical aspects of French maritime pine bark extract. J Ethnopharmacol. 2011; 133: 261-277. doi: 10.1016/j.jep.2010.10.041 PMID: 21044675
39. Packer L, Rimbach G, Virgili F. Antioxidant activity and biologic properties of a procyanidin-rich extract from pine (Pinus maritima) bark, pycnogenol. Free Radic Biol Med. 1999; 27: 704-724. PMID: 10490291
40. Nelson AB, Lau BH, Ide N, Rong Y. Pycnogenol inhibits macrophage oxidative burst, lipoprotein oxidation, and hydroxyl radical-induced DNA damage. Drug Dev Ind Pharm. 1998; 24: 139-144. PMID: 15605443
41. Kim YJ, Kang KS, Yokozawa T. The anti-melanogenic effect of pycnogenol by its anti-oxidative actions. Food Chem Toxicol. 2008; 46: 2466-2471. doi: 10.1016/j.fct.2008.04.002 PMID: 18482785
42. Saliou C, Rimbach G, Moini H, McLaughlin L, Hosseini S, Lee J, et al. Solar ultraviolet-induced erythema in human skin and nuclear factor-kappa-B-dependent gene expression in keratinocytes are modulated by a French maritime pine bark extract. Free Radic Biol Med. 2001; 30: 154-160. PMID: 11163532
43. Furumura M, Sato N, Kusaba N, Takagaki K, Nakayama J. Oral administration of French maritime pine bark extract (Flavangenol) improves clinical symptoms in photoaged facial skin. Clin Interv Aging. 2012; 7: 275-286. doi: 10.2147/CIA.S33165 PMID: 22956863
44. Terazawa S, Nakajima H, Shingo M, 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. doi: 10.1111/j.1600-0625.2012.01496.x PMID: 22626465
45. Zhu W, Gao J. The use of botanical extracts as topical skin-lightening agents for the improvement of skin pigmentation disorders J Invest Dermatol Symp Proc. 2008; 13: 20-24.
46. Smit N, Vicanova J, Pavel S. The hunt for natural skin whitening agents. Int J Mol Sci. 2009; 10: 5326-5349. doi: 10.3390/ijms10125326 PMID: 20054473
47. Chida M, Suzuki K, Nakanishi-Ueda T, Ueda T, Yasuhara H, Koide R, et al. In vitro testing of antioxidants and biochemical end-points in bovine retinal tissue. Ophthalmic Res. 1999; 31: 407-415. PMID: 10474069
48. Redmond RW, Kochevar IE. Spatially resolved cellular responses to singlet oxygen. Photochem Photobiol. 2006; 82: 1178-1186. PMID: 16740059
49. Muthusamy V, Piva TJ. UVB-stimulated TNFα release from human melanocyte and melanoma cells is mediated by p38 MAPK. Int J Mol Sci. 2013; 14: 17029-17054. doi: 10.3390/ijms140817029 PMID: 23965971
50. Abdel-Malek ZA, Kadekaro AL, Swope VB. Stepping up melanocytes to the challenge of UV exposure. Pigment Cell Melanoma Res. 2010; 23: 171-186. doi: 10.1111/j.1755-148X.2010.00679.x PMID: 20128873
51. Liu J, Yang D, Minemoto Y, Leitges M, Rosner MR, Lin A. NF-jB is required for UV induced JNK activation via induction of PKCd. Mol Cell. 2006; 21: 467-480. PMID: 16483929
52. Yanase H, Ando H, Horikawa M, Watanabe M, Mori T, Matsuda N. Possible involvement of ERK1/2 in UVA-induced melanogenesis in cultured normal human epidermal melanocytes. Pigment Cell Res. 2001; 14: 103-109. PMID: 11310789
53. Tada A, Pereira E, Beitner-Johnson D, Kavanagh R, Abdel-Malek ZA. Mitogen- and ultraviolet-B-induced signaling pathways in normal human melanocytes. J Invest Dermatol. 2002; 118: 316-322. PMID: 11841550
54. Matsuzawa A, Ichijo H. Redox control of cell fate by MAP kinase: physiological roles of ASK1-MAP kinase pathway in stress signaling. Biochim Biophys Acta. 2008; 1780: 1325-1336. doi: 10.1016/j.bbagen.2007.12.011 PMID: 18206122
55. Lee SJ, Bai SK, Lee KS, Namkoong S, Na HJ, Ha KS, et al. Astaxanthin inhibits nitric oxide production and inflammatory gene expression by suppressing I(kappa)B kinase-dependent NF-kappaB activation. Mol Cell. 2003; 16, 97-105.
56. Suzuki Y, Ohgami K, Shiratori K, Jin X, Ilieva I, Koyama Y, et al. Suppressive effects of astaxanthin against rat endotoxin-induced uveitis by inhibiting the NF-kappaB signaling pathway. Exp Eye Res. 2006; 82, 275-281. PMID: 16126197
57. Hur S, Lee YS, Yoo H, Yang JH, Kim TY. Homoisoflavanone inhibits UVB-induced skin inflammation through reduced cyclooxygenase-2 expression and NF-kappaB nuclear localization. J Dermatol Sci. 2010; 59: 163-169. doi: 10.1016/j.jdermsci.2010.07.001 PMID: 20724116
58. Afaq F, Adhami VM, Ahmad N, Mukhtar H. Inhibition of ultraviolet B-mediated activation of nuclear factor kB in normal human epidermal keratinocytes by green tea Constituent (-)-epigallocatechin-3-gallate. Oncogene. 2003; 22: 1035-1044. PMID: 12592390
59. Vicentini FT, He T, Shao Y, Fonseca MJ, Verri WA Jr, Fisher GJ, et al. Quercetin inhibits UV irradiation-induced inflammatory cytokine production in primary human keratinocytes by suppressing NF-κB pathway. J Dermatol Sci. 2011; 61: 162-168. doi: 10.1016/j.jdermsci.2011.01.002 PMID: 21282043
60. Adhami VM, Afaq F, Ahmad N. Suppression of Ultraviolet B exposure-mediated activation of NF-KB in normal human keratinocytes by resveratrol. Neoplasia 5: 74-82. PMID: 12659672
61. 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. doi: 10.1007/s11010-011-0823-4 PMID: 21519923
62. Potterf SB, Furumura M, Dunn KJ, Arnheiter H, Pavan WJ. Transcription factor hierarchy in Waardenburg syndrome: regulation of MITF expression by SOX10 and PAX3. Hum Genet. 2000; 107: 1-6. PMID: 10982026
63. Kim DS, Kim SY, Lee JE, Kwon SB, Joo YH, Youn SW, et al. Sphingosine-1-phosphate-induced ERK activation protects human melanocytes from UVB-induced apoptosis. Arch Pharm Res. 2003; 26:739-746. PMID: 14560924
64. Deak M, Clifton AD, Lucocq LM, Alessi DR. Mitogen- and stress-activated protein kinase-1 (MSK1) is directly activated by MAPK and SAPK2/p38, and may mediate activation of CREB. EMBO J. 1998; 17: 4426-4441. PMID: 9687510
65. Wiggin GR, Soloaga A, Foster JM, Murray-Tait V, Cohen P, Arthur JS. MSK1 and MSK2 are required for the mitogen- and stress-induced phosphorylation of CREB and ATF1 in fibroblasts. Mol Cell Biol. 2002; 22: 2871-2881. PMID: 11909979
66. McCoy CE, Campbell DG, Deak M, Bloomberg GB, Arthur JSE. MSK1 activity is controlled by multiple phosphorylation sites. Biochem J. 2005; 387: 507-517. PMID: 15568999
67. McCoy CE, Macdonald A, Morrice NA, Campbell DG, Deak M, Toth R, et al. Identification of novel phosphorylation sites in MSK1 by precursor on scanning MS. Biochem J. 2007; 402: 491-501. PMID: 17117922
68. Cheresternsen CA, Sturgill TW. Characterization of the p90 ribosomal S6 kinase carboxyl-terminal domain as a protein kinase. J Biol Chem. 2002; 277: 27733-27741. PMID: 12016217