DOI QR코드

DOI QR Code

3,4-Dihydroxytoluene suppresses UVB-induced wrinkle formation by inhibiting Raf-1

  • Park, Sang-Hee (School of Food Science and Biotechnology, Kyungpook National University) ;
  • Kang, Nam Joo (School of Food Science and Biotechnology, Kyungpook National University)
  • Received : 2020.07.01
  • Accepted : 2020.07.07
  • Published : 2020.08.31

Abstract

This study examined the effect of 3,4-dihydroxytoluene (DHT) on UVB-induced photoaging and determined its molecular mechanisms, using HaCaT human keratinocytes and SKH-1 hairless mice. DHT suppressed UVB-induced matrix metalloproteinase-1 (MMP-1) expression in HaCaT cells. In vivo data from mouse skin supported that DHT decreased UVB-induced wrinkle formation, epidermal thickness, and matrix metalloproteinase-13 (MMP-13) expression. DHT appeared to exert its anti-aging effects by suppressing UVB-induced Raf-1 kinase activity and subsequent attenuation of UVB-induced phosphorylation of MEK, ERK, and p90RSK in HaCaT cells. In vitro and in vivo pull-down assays revealed that DHT bound with Raf-1 in ATP-noncompetitive manner. Overall, DHT appears to anti-photoaging effects in vitro and in vivo through the suppression of Raf-1 kinase activity and may have potential as a treatment for the prevention of skin aging.

Keywords

References

  1. Afaq F, Adhami VM, Mukhtar H. Photochemoprevention of ultraviolet b signaling and photocarcinogenesis. Mutat. Res. 571: 153-173 (2005) https://doi.org/10.1016/j.mrfmmm.2004.07.019
  2. Arjumand W, Seth A, Sultana S. Rutin attenuates cisplatin induced renal inflammation and apoptosis by reducing nfkappab, tnf-alpha and caspase-3 expression in wistar rats. Food Chem. Toxicol. 49: 2013-2021 (2011) https://doi.org/10.1016/j.fct.2011.05.012
  3. Baba S, Furuta T, Horie M, Nakagawa H. Studies on drug metabolism by use of isotopes xxvi: Determination of urinary metabolites of rutin in humans. J. Pharm. Sci. 70: 780-782 (1981) https://doi.org/10.1002/jps.2600700717
  4. Berneburg M, Plettenberg H, Krutmann J. Photoaging of human skin. Photodermatol. Photoimmunol. Photomed. 16: 239-244 (2000) https://doi.org/10.1034/j.1600-0781.2000.160601.x
  5. Bhattacharyya TK, Pathria M, Mathison C, Vargas M, Thomas JR. Cosmeceutical effect on skin surface profiles and epidermis in uv-b-irradiated mice. JAMA Facial Plast. Surg. 16: 253-260 (2014) https://doi.org/10.1001/jamafacial.2013.2582
  6. Bokkenheuser VD, Shackleton CH, Winter J. Hydrolysis of dietary flavonoid glycosides by strains of intestinal bacteroides from humans. Biochem. J. 248: 953-956 (1987) https://doi.org/10.1042/bj2480953
  7. Braune A, Gutschow M, Engst W, Blaut M. Degradation of quercetin and luteolin by eubacterium ramulus. Appl. Environ. Microbiol. 67: 5558-5567 (2001) https://doi.org/10.1128/AEM.67.12.5558-5567.2001
  8. Brennan M, Bhatti H, Nerusu KC, Bhagavathula N, Kang S, Fisher GJ, Varani J, Voorhees JJ. Matrix metalloproteinase-1 is the major collagenolytic enzyme responsible for collagen damage in uv-irradiated human skin. Photochem. Photobiol. 78: 43-48 (2003) https://doi.org/10.1562/0031-8655(2003)078<0043:MMITMC>2.0.CO;2
  9. Bryce GF, Bogdan NJ, Brown CC. Retinoic acids promote the repair of the dermal damage and the effacement of wrinkles in the uvb-irradiated hairless mouse. J. Invest. Dermatol. 91: 175-180 (1988) https://doi.org/10.1111/1523-1747.ep12464445
  10. Chaquour B, Seite S, Coutant K, Fourtanier A, Borel JP, Bellon G. Chronic uvb- and all-trans retinoic-acid-induced qualitative and quantitative changes in hairless mouse skin. J. Photochem. Photobiol. B-Biol. 28: 125-135 (1995) https://doi.org/10.1016/1011-1344(94)07080-8
  11. Chen TJ, Jeng JY, Lin CW, Wu CY, Chen YC. Quercetin inhibition of ros-dependent and -independent apoptosis in rat glioma c6 cells. Toxicology 223: 113-126 (2006) https://doi.org/10.1016/j.tox.2006.03.007
  12. Cho HJ, Kang JH, Kwak JY, Lee TS, Lee IS, Park NG, Nakajima H, Magae J, Chang YC. Ascofuranone suppresses pma-mediated matrix metalloproteinase-9 gene activation through the ras/raf/mek/erk- and ap1-dependent mechanisms. Carcinogenesis 28: 1104-1110 (2007) https://doi.org/10.1093/carcin/bgl217
  13. Chung JH. Photoaging in asians. Photodermatol. Photoimmunol. Photomed. 19: 109-121 (2003) https://doi.org/10.1034/j.1600-0781.2003.00027.x
  14. Chung JH, Yano K, Lee MK, Youn CS, Seo JY, Kim KH, Cho KH, Eun HC, Detmar M. Differential effects of photoaging vs intrinsic aging on the vascularization of human skin. Arch. Dermatol. : 1437-1442 (2002)
  15. D'Orazio J, Jarrett S, Amaro-Ortiz A, Scott T. Uv radiation and the skin. Int. J. Mol. Sci., 14: 12222-12248 (2013) https://doi.org/10.3390/ijms140612222
  16. Dall'Agnol R, Ferraz A, Bernardi AP, Albring D, Nor C, Sarmento L, Lamb L, Hass M, von Poser G, Schapoval EES. Antimicrobial activity of some hypericum species. Phytomedicine, 10(6-7): 511-516 (2003) https://doi.org/10.1078/094471103322331476
  17. Fisher GJ, Kang S, Varani J, Bata-Csorgo Z, Wan Y, Datta S, Voorhees JJ. Mechanisms of photoaging and chronological skin aging. Arch. Dermatol., 138: 1462-1470 (2002)
  18. Fisher GJ, Wang ZQ, Datta SC, Varani J, Kang S, Voorhees JJ. Pathophysiology of premature skin aging induced by ultraviolet light. N. Engl. J. Med., 337: 1419-1428 (1997) https://doi.org/10.1056/NEJM199711133372003
  19. Gao K, Xu A, Krul C, Venema K, Liu Y, Niu Y, Lu J, Bensoussan L, Seeram NP, Heber D, Henning SM. Of the major phenolic acids formed during human microbial fermentation of tea, citrus, and soy flavonoid supplements, only 3,4-dihydroxyphenylacetic acid has antiproliferative activity. J. Nutr. 136: 52-57 (2006) https://doi.org/10.1093/jn/136.1.52
  20. Gelse K, Poschl E, Aigner T. Collagens--structure, function, and biosynthesis. Adv. Drug Deliv. Rev. 55: 1531-1546 (2003) https://doi.org/10.1016/j.addr.2003.08.002
  21. Gilchrest BA. Skin aging and photoaging: An overview. J. Am. Acad. Dermatol. 21: 610-613 (1989) https://doi.org/10.1016/S0190-9622(89)70227-9
  22. Goihman-Yahr M. Skin aging and photoaging: An outlook. Clin. Dermatol. 14: 153-160 (1996) https://doi.org/10.1016/0738-081X(95)00150-E
  23. Griffiths LA, Barrow A. Metabolism of flavonoid compounds in germ-free rats. Biochem. J. 130: 1161-1162 (1972) https://doi.org/10.1042/bj1301161
  24. Guardia T, Rotelli AE, Juarez AO, Pelzer LE. Anti-inflammatory properties of plant flavonoids. Effects of rutin, quercetin and hesperidin on adjuvant arthritis in rat. Farmaco 56: 683-687 (2001) https://doi.org/10.1016/S0014-827X(01)01111-9
  25. Han Y. Rutin has therapeutic effect on septic arthritis caused by candida albicans. Int. Immunopharmacol. 9: 207-211 (2009) https://doi.org/10.1016/j.intimp.2008.11.002
  26. Holasova M, Fiedlerova V, Smrcinova H, Orsak M, Lachman J, Vavreinova S. Buckwheat-the source of antioxidant activity in functional foods. Food Res. Int. 35: 207-211 (2002) https://doi.org/10.1016/S0963-9969(01)00185-5
  27. Hollman PC, Katan MB. Absorption, metabolism and health effects of dietary flavonoids in man. Biomed. Pharmacother. 51: 305-310 (1997) https://doi.org/10.1016/S0753-3322(97)88045-6
  28. Hwang E, Sun ZW, Lee TH, Shin HS, Park SY, Lee DG, Cho BG, Sohn H, Kwon OW, Kim SY, Yi TH. Enzyme-processed korean red ginseng extracts protects against skin damage induced by uvb irradiation in hairless mice. J. Ginseng Res. 37: 425-434 (2013) https://doi.org/10.5142/jgr.2013.37.425
  29. Jaganath IB, Mullen W, Lean ME, Edwards CA, Crozier A. In vitro catabolism of rutin by human fecal bacteria and the antioxidant capacity of its catabolites. Free Radic. Biol. Med. 47: 1180-1189 (2009) https://doi.org/10.1016/j.freeradbiomed.2009.07.031
  30. Jung CH, Lee JY, Cho CH, Kim CJ. Anti-asthmatic action of quercetin and rutin in conscious guinea-pigs challenged with aerosolized ovalbumin. Arch. Pharm. Res. 30: 1599-1607 (2007) https://doi.org/10.1007/BF02977330
  31. Jung SK, Lee KW, Kim HY, Oh MH, Byun S, Lim SH, Heo YS, Kang NJ, Bode AM, Dong Z, Lee HJ. Myricetin suppresses uvb-induced wrinkle formation and mmp-9 expression by inhibiting raf. Biochem. Pharmacol. 79: 1455-1461 (2010) https://doi.org/10.1016/j.bcp.2010.01.004
  32. Kang NJ, Shin SH, Lee HJ, Lee KW. Polyphenols as small molecular inhibitors of signaling cascades in carcinogenesis. Pharmacol. Ther. 130: 310-324 (2011) https://doi.org/10.1016/j.pharmthera.2011.02.004
  33. Lee WS, Lim JH, Sung MS, Lee EG, Oh YJ, Yoo WH. Ethyl acetate fraction from angelica sinensis inhibits il-1beta-induced rheumatoid synovial fibroblast proliferation and cox-2, pge2, and mmps production. Biol. Res. 47: 41 (2014) https://doi.org/10.1186/0717-6287-47-41
  34. Lim SH, Jung SK, Byun S, Lee EJ, Hwang JA, Seo SG, Kim YA, Yu JG, Lee KW, Lee HJ. Luteolin suppresses uvb-induced photoageing by targeting jnk1 and p90 rsk2. J. Cell. Mol. Med. 17: 672-680 (2013) https://doi.org/10.1111/jcmm.12050
  35. Lin JP, Yang JS, Lu CC, Chiang JH, Wu CL, Lin JJ, Lin HL, Yang MD, Liu KC, Chiu TH, Chung JG. Rutin inhibits the proliferation of murine leukemia wehi-3 cells in vivo and promotes immune response in vivo. Leuk. Res. 33: 823-828 (2009) https://doi.org/10.1016/j.leukres.2008.09.032
  36. Manach C, Morand C, Texier O, Favier ML, Agullo G, Demigne C, Regerat F, Remesy C. Quercetin metabolites in plasma of rats fed diets containing rutin or quercetin. J. Nutr. 125: 1911-1922 (1995) https://doi.org/10.1093/jn/125.7.1911
  37. Moelling K, Heimann B, Beimling P, Rapp UR, Sander T. Serine- and threonine-specific protein kinase activities of purified gag-mil and gag-raf proteins. Nature 312: 558-561 (1984) https://doi.org/10.1038/312558a0
  38. Olthof MR, Hollman PC, Buijsman MN, van Amelsvoort JM, Katan MB. Chlorogenic acid, quercetin-3-rutinoside and black tea phenols are extensively metabolized in humans. J. Nutr., 133(6): 1806-1814 (2003) https://doi.org/10.1093/jn/133.6.1806
  39. Pashikanti S, de Alba DR, Boissonneault GA, Cervantes-Laurean D. Rutin metabolites: Novel inhibitors of nonoxidative advanced glycation end products. Free Radic. Biol. Med., 48(5): 656-663 (2010) https://doi.org/10.1016/j.freeradbiomed.2009.11.019
  40. Pastore S, Potapovich A, Kostyuk V, Mariani V, Lulli D, De Luca C, Korkina L. Plant polyphenols effectively protect hacat cells from ultraviolet c-triggered necrosis and suppress inflammatory chemokine expression. Ann. N.Y. Acad. Sci. 1171: 305-313 (2009) https://doi.org/10.1111/j.1749-6632.2009.04684.x
  41. Pyun HB, Kim M, Park J, Sakai Y, Numata N, Shin JY, Shin HJ, Kim DU, Hwang JK. Effects of collagen tripeptide supplement on photoaging and epidermal skin barrier in uvb-exposed hairless mice. Prev. Nutr. Food Sci. 17: 245-253 (2012) https://doi.org/10.3746/pnf.2012.17.4.245
  42. Ramanathan R, Das N, Tan C. Inhibitory effects of 2-hydroxy chalcone and other flavonoids on human cancer cell-proliferation. Int. J. Oncol. 3: 115-119 (1993)
  43. Ren W, Qiao Z, Wang H, Zhu L, Zhang L. Flavonoids: Promising anticancer agents. Med. Res. Rev. 23: 519-534 (2003) https://doi.org/10.1002/med.10033
  44. Rittie L, Fisher GJ. Uv-light-induced signal cascades and skin aging. Ageing Res. Rev. 1: 705-720 (2002) https://doi.org/10.1016/S1568-1637(02)00024-7
  45. Schneider H, Simmering R, Hartmann L, Pforte H, Blaut M. Degradation of quercetin-3-glucoside in gnotobiotic rats associated with human intestinal bacteria. J. Appl. Microbiol. 89: 1027-1037 (2000) https://doi.org/10.1046/j.1365-2672.2000.01209.x
  46. Shen SC, Lee WR, Lin HY, Huang HC, Ko CH, Yang LL, Chen YC. In vitro and in vivo inhibitory activities of rutin, wogonin, and quercetin on lipopolysaccharide-induced nitric oxide and prostaglandin e(2) production. Eur. J. Pharmacol. 446: 187-194 (2002) https://doi.org/10.1016/S0014-2999(02)01792-2
  47. Van Puyvelde K, Mets T, Njemini R, Beyer I, Bautmans I. Effect of advanced glycation end product intake on inflammation and aging: A systematic review. Nutr. Rev. 72: 638-650 (2014) https://doi.org/10.1111/nure.12141
  48. Wang Y, Chen H, Wang W, Wang R, Liu ZL, Zhu W, Lian S. N-terminal 5-mer peptide analog p165 of amyloid precursor protein inhibits uva-induced mmp-1 expression by suppressing the mapk pathway in human dermal fibroblasts. Eur. J. Pharmacol. 734: 1-8 (2014) https://doi.org/10.1016/j.ejphar.2014.03.028
  49. Watanabe H, Shimizu T, Nishihira J, Abe R, Nakayama T, Taniguchi M, Sabe H, Ishibashi T, Shimizu H. Ultraviolet a-induced production of matrix metalloproteinase-1 is mediated by macrophage migration inhibitory factor (mif) in human dermal fibroblasts. J. Biol. Chem. 279: 1676-1683 (2004) https://doi.org/10.1074/jbc.M303650200
  50. Watanabe M, Ohshita Y, Tsushida T. Antioxidant compounds from buckwheat (fagopyrum esculentum moench) hulls. J. Agric. Food Chem. 45: 1039-1044 (1997) https://doi.org/10.1021/jf9605557
  51. Winter J, Moore LH, Dowell VR, Jr., Bokkenheuser VD. C-ring cleavage of flavonoids by human intestinal bacteria. Appl. Environ. Microbiol. 55: 1203-1208 (1989) https://doi.org/10.1128/AEM.55.5.1203-1208.1989
  52. Yang J, Guo J, Yuan J. In vitro antioxidant properties of rutin. LWT-Food Sci. Technol. 41: 1060-1066 (2008) https://doi.org/10.1016/j.lwt.2007.06.010
  53. Yang K, Lamprecht SA, Liu Y, Shinozaki H, Fan K, Leung D, Newmark H, Steele VE, Kelloff GJ, Lipkin M. Chemoprevention studies of the flavonoids quercetin and rutin in normal and azoxymethane-treated mouse colon. Carcinogenesis 21: 1655-1660 (2000) https://doi.org/10.1093/carcin/21.9.1655
  54. Yang YC, Lin HY, Su KY, Chen CH, Yu YL, Lin CC, Yu SL, Yan HY, Su KJ, Chen YL. Rutin, a flavonoid that is a main component of saussurea involucrata, attenuates the senescence effect in d-galactose aging mouse model. Evid.-based Complement Altern. Med. 2012: 980276 (2012)
  55. Yu YS, Hsu CL, Yen GC. Anti-inflammatory effects of the roots of alpinia pricei hayata and its phenolic compounds. J. Agric. Food Chem. 57: 7673-7680 (2009) https://doi.org/10.1021/jf901327g