Morphological Studies on the Inhibitory Effects of Photoaging Skin of Fermented Red Ginseng in Hairless Mice

발효홍삼의 광노화 피부 억제효과에 대한 형태학적 연구

  • Lee, Chang Hyun (College of Korean Medicine, Woosuk University) ;
  • Kim, Ho Il (College of Korean Medicine, Woosuk University) ;
  • Kim, Jong Seok (Department of Rehabilitation Studies, Woosuk University) ;
  • Oh, Mi Jin (Department of Food & Biotechnology, Woosuk University) ;
  • Kim, Sun Woong (Department of Food & Biotechnology, Woosuk University) ;
  • Ma, Sang Yong (Department of Alternative Medicine, Woosuk University) ;
  • Kim, Myoung Soon (Department of Alternative Medicine, Woosuk University) ;
  • Kwon, Jin (Department of Prosthetics and Orthotics, Korea National College of Welfare) ;
  • Jeong, Han Sol (Division of Applied Medicine, School of Korean Medicine, Pusan National University) ;
  • Oh, Chan Ho (Department of Food & Biotechnology, Woosuk University)
  • 이창현 (우석대학교 한의과대학) ;
  • 김호일 (우석대학교 한의과대학) ;
  • 김종석 (우석대학교 재활학과) ;
  • 오미진 (우석대학교 식품생명공학과) ;
  • 김선웅 (우석대학교 식품생명공학과) ;
  • 마상용 (우석대학교 대체의학과) ;
  • 김명순 (우석대학교 대체의학과) ;
  • 권진 (한국복지대학교 의료보장구과) ;
  • 정한솔 (부산대학교 한의학전문대학원 응용의학부) ;
  • 오찬호 (우석대학교 식품생명공학과)
  • Received : 2014.01.02
  • Accepted : 2014.02.07
  • Published : 2014.04.25

Abstract

To investigate the anti-photoaging effect of fermented Red Ginseng(RG) in SKH-1 mice. We examined the effects of extracts of non-fermented RG(NRG group), fermented RG(FRG group) and fortified fermented RG(FFRG group) on skin wrinkles formation, histological changes related to the number of epidermal cell layers, epidermal thickness, neutrophil infiltration into dermis, degradation of collagen fibers, and the number of mast cells, and immunohistochemical changes related to cytokines and enzymes in photoaging skin caused by UVB irradiation of SKH-1 mice. The oral administration(300 mg/Kg B.W./day) and topical application($100{\mu}{\ell}/mouse/day$) of extracts of NRG, FRG and FFRG inhibited increases in epidermal thickness and wrinkle formation compared to control group in dorsal skin induced by UVB irradiation. We observed more increased stainability of acid fuschin and aniline blue in dermis of FFRG group than those of other groups. Furthermore, NRG, FRG and FFRG prevented the disruption of collagen fibers within papillary layer of dermis, and decreased number of mast cells in the dorsal skins induced by UVB irradiation. We observed fine wrinkle formation in FFRG group. Treatment with NRG, FRG and FFRG decreased immunohistochemical density of myeloperoxidase related to inflammation in the photoaging skin. We observed more decreased immunohistochemical density of myeloperoxidase in FFRG group than those of other groups. Immunohistochemical density of PCNA and Ki-67 in FFRG group was more decreased than those of other groups. Our study suggests that fermented red ginseng extracts participates in inhibitory effects in the morphological processes related to photoaging skin on UVB irradiated SKH-1 mice.

Keywords

References

  1. Meinhard, W., Iiana, T.B., Lale, N., Wenjian, M., Lars, A.S., Ziba, R.W., Jutta, S., Karin, S.K. Solar UV irradiation and dermal photoaging. J Photochem Photobiol 63: 41-51, 2001. https://doi.org/10.1016/S1011-1344(01)00201-9
  2. Lavker, R.M. Structural alterations in exposed and unexposed aged skin. J Invest Dermatol 73: 59-66, 1979. https://doi.org/10.1111/1523-1747.ep12532763
  3. Gilchrest, B.A. Skin aging and photoaging: an overview. J Am Acad Dermatol 989(21): 610-613, 1989.
  4. Griffiths, C.E.M. The clinical identification and quantification of photodamage. Br J Dermatol 127(Suppl. 41):37-42, 1992.
  5. Kligman, A.M., Grove, G.L., Hirose, R., Leyden, J.J. Topical tretinoin for photoaged skin. J Am Acad Dermatol 15: 836-859, 1986. https://doi.org/10.1016/S0190-9622(86)70242-9
  6. Chung, J.H., Seo, J.Y., Choi, H.R., Lee, M.K., Youn, C.S., Rhie, G., Cho, K.H., Kim, K.H., Park, K.C., Eun, H.C. Modulation of skin collagen metabolism in aged and photoaged human skin in vivo. J Invest Dermatol 117: 1218-1224, 2001. https://doi.org/10.1046/j.0022-202x.2001.01544.x
  7. Gilchrest, B.A. A review of skin ageing and its medical therapy. Br J Dermatol 135: 867-875, 1996. https://doi.org/10.1046/j.1365-2133.1996.d01-1088.x
  8. Quan, T., Qin, Z., Xia W., Shao, Y., Voorhees, J.J., Fisher, G.J. Matrix-degrading Metalloproteinases in Photoaging. J Investig Dermatol Symp Proc. 14(1):20-24, 2009. https://doi.org/10.1038/jidsymp.2009.8
  9. 박창민, 이순영, 정민석, 최종완. 3-O-cetyl-L-ascorbic acid의 주름 개선 효과. 대한화장품학회지 34(4):303-309, 2008.
  10. Wyss, R. Chromatographic and electrophoretic analysis of biomedically important retinoids. J Chromatogr B, Biomed Sci Appl 671: 381-425, 1995. https://doi.org/10.1016/0378-4347(95)00154-B
  11. Weiss, J.S., Ellis, C.N., Headington, J.T., Voorhees, J.J. Topical tretinoin in the treatment of aging skin. J Am Acad Dermatol 19: 169-175, 1988. https://doi.org/10.1016/S0190-9622(88)70161-9
  12. Gary, J.F., Kang, S.W., Varani, J., Zsuzsanna, B.C., Wan, Y., Datta, S., Voorhees, J.J. Mechanisms of photoaging and chronological skin aging. Arch Dermatol 138: 1462-1470, 2002.
  13. Kim, Y.G., Sumiyoshi, M., Sakanaka, M., Kimura, Y. Effects of ginseng saponins isolated from red ginseng on ultraviolet B-induced skin aging in hairless mice. Eur J Pharm 602: 148-156, 2009. https://doi.org/10.1016/j.ejphar.2008.11.021
  14. Lee, S.J., Cho, S.W., Kwon, Y.Y., Kwon, H.S., Shin, W.C. Inhibitory effects of ethanol extracts from Nuruk on oxidative stress, melanogenesis, and photo-aging. Mycobiology 40(2):117-123, 2012. https://doi.org/10.5941/MYCO.2012.40.2.117
  15. 김명자, 강상모. 홍삼식이가 여성의 목 피부 홍반과 탄력 개선에 미치는 효과. 한국미용학회지 18(3):661-669, 2012
  16. Choi, Y.K., Su, J.U., Park, S.K., Yu, S.N., Kim, S.H., Rhee, M.S., Ahn, S.C., Shin, M.S. Research trends of fermented medicinal herbs - Based on their clinical efficacy and safety assessment. J Life Science 22: 1729-1739, 2012. https://doi.org/10.5352/JLS.2012.22.12.1729
  17. 이지해, 이병석, 양미숙, 변범선, 김완기, 김배환, 이상준. Hairless mice에서의 대두 홍삼 혼합분말(APB-03)의 경구 반복 투여 시 피부 주름 생성 예방 효과. 한국식품과학회지 37(6):989-996, 2005.
  18. Kang, T.H., Park, H.M., Kim, Y.B., Kim, H.A., Kim, N.M., Do, J.H., Kang, C.H., Cho, Y.H., Kim, S.Y. Effects of red ginseng extract on UVB irradiation-induced skin aging in hairless mice. J Ethnopharmacol 123: 446-451, 2009. https://doi.org/10.1016/j.jep.2009.03.022
  19. Lee, M.J., Won, C.H., Lee, S.R., Kim, J.S., Oh, I.G., Hwang, E.I., Kim, N.M., Kang, B.C., Chung, J.H. Oral administration of KTNG0345 prepared from red ginseng extracts reduces UVB-induced skin wrinkle formation in hairless mice. J Ginseng Res 32(1):48-56, 2008. https://doi.org/10.5142/JGR.2008.32.1.048
  20. Jeong, D.W., Hong, J.W., Shin, W.J., Park, Y.M., Jung, J.H., Kim, C.H., Min, I.K., Park, S.U., Jung, W.S., Park, J.M., Go, C.N., Cho, K.H., Moon, S.K. Effects of Korean ginseng, Korean red ginseng and fermented Korean red ginseng on cerebral blood flow, cerebrovascular reactivity, systemic blood pressure and pulse rate in humans. J Korean Orient Med 27: 38-50, 2006.
  21. Bancroft, J.D., Stevens, A., Turne,r D.R. Theory and practice of histological techniques. 4th ed. Newyork: Churchil Livingstone, pp 127-128, 1996.
  22. Hsu, S.M., Raine, L., Fanger, H. Use of avidinbiotin- peroxidase complex(ABC) in immunoperoxidase techniques: A comparison between ABC and unlabeled antibody(PAP) procedures. J Histochem Cytochem 29: 577-580, 1981. https://doi.org/10.1177/29.4.6166661
  23. Placzec, M., Kerkmann, U., Bell, S., Koepke, P., Przybilla, B. Tobacco smoke is phototoxic. Br J Dermatol 150: 991-993, 2004. https://doi.org/10.1111/j.1365-2133.2004.05818.x
  24. Fisher, G.J., Kan, S., Varani, J., Bata-Csorgo, Z., Wan, Y., Datta, S., Voorhees, J.J. Mechanisms of photoaging and chronological skin aging. Arch Dermatol 138: 1462-1470, 2002.
  25. Landau, M. Exogenous factors in skin aging. Curr Probl Dermatol 35: 1-13, 2007.
  26. 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
  27. Sander, C.S., Chang, H., Salzmann, S., Müller, C.S., Ekanayake-Mudiyanselage, S., Elsner, P., Thiele, J.J. Photoaging is associated with protein oxidation in human skin in vivo. J Invest Dermatol 118(4):618-625, 2002. https://doi.org/10.1046/j.1523-1747.2002.01708.x
  28. Kiss, I., Chen, S., Tramposch, K.M. The effect of high and low ultraviolet-B dose exposure on the degree of hairless mouse skin wrinkling. Photochem Photobiol 53: 109-112, 1991. https://doi.org/10.1111/j.1751-1097.1991.tb08474.x
  29. 김동현. 인삼과 건강. 효일, 2005.
  30. 안덕균. 기미론에서 본 인삼의 효능. 본초분과학회지 7(1): 27-32, 1992.
  31. 허 준. 동의보감. 탕액편.
  32. 노승현. 인삼의 효능. 본초분과학회지 7(1):53-60, 1992.
  33. 상해과학기술출판사. 중약대사전 (김창민, 신민교, 안덕균, 이 경순 외 번역). 정담, 1997.
  34. 주영승. 운곡본초학. 서림재, 2004.
  35. 김은혜, 이동권. 고려인삼이 항스트레스에 미치는 영향. 식품 저장과 가공산업 8(2): 13-18, 2009.
  36. 김대한, 송호준, 정종길, 심영섭, 신민교. 인삼 saponin 장내 Glc-PPT 및 PPT가 면역계에 미치는 영향에 관한 연구. 대한본초학회지 19(4):105-115, 2004.
  37. 이인선, 이승욱, 이인자. Streptozotocin-유도 당뇨모델을 이 용한 배양인삼 분말의 혈당 강하 및 지질대사의 개선효과. 한국식품과학회지 35(2):280-285, 2003.
  38. 임창진, 박은희, 이동원, 이송재, 홍순근. 흰쥐의 혈청 콜레스테롤 및 중성지방 수준에 미치는 인삼 총 사포닌의 영향. 한국생화학회지 14(3): 188-198, 1981.
  39. 정영호, 황영수, 주충노, 백용기. 콜레스티폴과 인삼사포닌이 생쥐의 콜레스테롤 대사에 미치는 영향. 한국지질학회지 2(1):16-23, 1992.
  40. 이산명, 안병철, 이윤호. 인삼, 녹용 및 목향수침이 흰쥐의 체 중 및 소화관 호르몬 분비에 미치는 영향. 대한침구학회지 5(1):1-13, 1988.
  41. 김낙두, 김인철. 인삼성분의 혈압강하기전에 관한 연구. 생약학회지 9(1):41-47, 1978.
  42. 주일우, 성경화, 박정민, 류재환, 오한진. 홍삼이 정상 흰쥐의 혈압 및 대동맥 조직 소견 변화에 미치는 영향. 고려인삼학회지 32(4):324-331, 2008.
  43. 최형기, 김영찬, 홍영권, 신재섭, 강명서, 성도환. 남성 갱년기 성기능 장애에서 홍삼이 성기능과 혈중 지질농도에 미치는 효과. 고려인삼학회지 20(2):125-132, 1996.
  44. Kong, B.M., Park, M.J., Min, J.W., Kim, H.B., Kim, SH., Kim, S.Y., Yang, D.C. Physico-chemical characteristics of white fermented and red ginseng extracts. J Ginseng Res 32: 238-243, 2008. https://doi.org/10.5142/JGR.2008.32.3.238
  45. 신용서. CKDHC 0801과 CKDHC 0802 균주를 이용한 홍삼발효. 한국식품조리과학회지 26: 469-474, 2010.
  46. Odani, T., Tanizawa, H. Takino, Y. Studies on the absorption, distribution, excretion and metabolism of ginseng saponins. II. The absorption, distribution and excretion of ginsenoside Rg1 in the rat. Chem Pharm Bull 31: 292-298, 1983. https://doi.org/10.1248/cpb.31.292
  47. Oikarinen, A. Aging of the skin connective tissue: how to measure the biochemical and mechanical properties of aging dermis. Photodermatol Photoimmunol Photomed 10: 47-52, 1994.
  48. Braverman, I.M., Fonferko, E. Studies in cutaneous aging. I. The elastic fiber network. J Invest Dermatol 78: 434-443, 1982. https://doi.org/10.1111/1523-1747.ep12507866
  49. Uitto, J. Connective tissue biochemistry of the aging dermis. Age-related alterations in collagen and elastin. Dermatol Clin 4: 433-446, 1986.
  50. Varani, J., Spearman, D., Perone, P., Fligiel, S.E.G., Datta, S.C., Wang, Z.Q., Shao, Y., Kang, S., Fisher, G.J., Voorhees, J.J. Inhibition of type I procollagen synthesis by damaged collagen in photoaged skin and by collagenase-degraded collagen in vitro. Am J Pathol 158: 931-942, 2001. https://doi.org/10.1016/S0002-9440(10)64040-0
  51. Kim, Y.G., Sumiyoshi, M., Kawahira, K., Sakanaka, M., Kimura, Y. Effects of red ginseng extract on ultraviolet B-irradiated skin change in C57BL mice. Phytother Res 22: 1423-1427, 2008. https://doi.org/10.1002/ptr.2339
  52. Gilchrest, B.A., Soter, N.A., Stoff, J.S., Mihm, M.C. The human sunburn reaction: histologic and biochemical studies. J Am Acad Dermatol 5: 411-422, 1981. https://doi.org/10.1016/S0190-9622(81)70103-8
  53. Hart, P.H., Grimbaldeston, M.A., Finlay-Jones, J.J. Mast cells in UV-B-induced immunosuppression. J Photochem Photobiol B: Biol 55: 81-87, 2000. https://doi.org/10.1016/S1011-1344(00)00032-4
  54. Pentland, A.P., Mahoney, M., Jacobs, S.C., Holtzman, M.J. Enhanced prostaglandin synthesis after ultraviolet injury is mediated by endogenous histamine stimulation. A mechanism for irradiation erythema. J Clin Invest 86: 566-574, 1990. https://doi.org/10.1172/JCI114746
  55. Hart, P.H., Grimbaldeston, M.A., Swift, C.J., Jaksic, A., Noonan, F.P., Finlay-Jones, J.J. Dermal mast cells determine susceptibility to ultraviolet B-induced systemic suppression of contact hypersensitivity responses in mice. J Exp Med 187: 2045-2053, 1998. https://doi.org/10.1084/jem.187.12.2045
  56. Walsh, L.J. Ultraviolet B irradiation of skin induces mast cell degranulation and release of tumour necrosis factor-$\alpha$. Immunol Cell Biol 73: 226-233, 1995. https://doi.org/10.1038/icb.1995.37
  57. Moodycliffe, A.M., Kimber, I., Norval, M. Role of tumour necrosis factor-$\alpha$ in ultraviolet B light-induced dendritic cell migration and suppression of contact hypersensitivity. Immunology 81: 79-84, 1994.
  58. Laberge, S., Cruikshank, W.W., Kornfield, H., Center, D.M. Histamine induced secretion of lymphocyte chemoattractant factor from CD8q T cells is independent of transcription and translation. Evidence for constitutive protein synthesis and storage. J Immunol 155: 2902-2910, 1995.
  59. Lagier, B., Lebel, B., Bousquet, J., Pene, J. Different modulation by histamine of IL-4 and interferon-gamma (IFN-$\gamma$) release according to the phenotype of human Th0, Th1 and Th2 clones, Clin Exp Immunol 108: 545-551, 1997. https://doi.org/10.1046/j.1365-2249.1997.3791276.x
  60. Chaloob, M.K., Ali, H.H., Qasim, B.J., Mohammed, A.S. Immunohistochemical expression of Ki-67, PCNA and CD34 in astrocytomas: A clinicopathological study. Oman Med J 27(5):368-374, 2012. https://doi.org/10.5001/omj.2012.93
  61. Syed, D.N., Malik, A., Hadi, N., Sarfaraz, S., Afaq, F., Mukhtar, H. Photochemopreventive effect of pomegranate fruit extract on UVA-mediated activation of cellular pathways in normal human epidermal keratinocytes. Photochem Photobiol. 82(2):398-405, 2006. https://doi.org/10.1562/2005-06-23-RA-589
  62. Sundaresan, M., Yu, ZX., Ferrans, V.J., Irani, K., Finker, T. Requirement for generation of H2O2 for platelet-derived growth factor signal transduction. Science (Washington DC), 270: 296-299, 1995. https://doi.org/10.1126/science.270.5234.296
  63. Lu, Y.P., Lou, T.R., Yen, P., Mitchell, D., Huang, M.T, Conney, A.H. Time course for early adaptive responses to ultraviolet B light in the epidermis of SKH-1 mice. Cancer Res 59: 4591-4602, 1999.
  64. Oberyszyn, T.M., Tober, K.L., Ross, M.S., Robertson, F.M. Inhibitory effects of pentoxifylline on ultraviolet B light-induced cutaneous inflammation. Mol Carcinog 22: 16-258, 1998. https://doi.org/10.1002/(SICI)1098-2744(199805)22:1<16::AID-MC3>3.0.CO;2-J