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Red ginseng oil promotes hair growth and protects skin against UVC radiation

  • Truong, Van-Long (Department of Food and Life Sciences, College of BNIT, Inje University) ;
  • Keum, Young-Sam (College of Pharmacy and Integrated Research Institute for Drug Development, Dongguk University) ;
  • Jeong, Woo-Sik (Department of Food and Life Sciences, College of BNIT, Inje University)
  • Received : 2020.07.20
  • Accepted : 2020.12.31
  • Published : 2021.07.01

Abstract

Background: A wide range of environmental factors, such as diseases, nutritional deficiencies, ageing, hormonal imbalances, stress, and ultraviolet (UV) radiation, may affect the structure and function of the skin that covers the entire surface of the human body. In this study, we investigated roles of red ginseng oil (RGO) in enhancing skin functions, including hair growth and skin protection, using mouse models. Methods: For hair growth experiment, shaved dorsal skins of C57BL/6 mice were topically applied with vehicle, RGO, RGO's major compounds, or minoxidil for consecutive 21 days and skin tissues were examined the hair growth promoting capacity. For skin protection experiment, SKH-1 hairless mice were topically applied with vehicle or RGO twice a day for three days prior to exposure to UVC radiation at 20 kJ/cm2. Skin tissues were collected to evaluate skin protective effects of RGO. Results: Topical application of RGO to C57BL/6 mice effectively promoted hair regeneration by inducing early telogen-to-anagen transition and significantly increasing the density and bulb diameter of hair follicles. Major compounds, including linoleic acids and β-sitosterol, contributed to RGO-promoted hair growth. Treatment with RGO as well as its major components upregulated expression of hair growth-related proteins. Furthermore, in SKH-1 hairless mice, RGO had a protective effect against UVC-induced skin damage by inhibiting inflammation and apoptosis, as well as inducing cytoprotective systems. Conclusion: These data suggest that RGO may be a potent agent for improving skin health and thereby preventing and/or treating hair loss and protecting skin against UV radiation.

Keywords

Acknowledgement

We are grateful to the Korea Ginseng Corporation for the preparation of RGO. This work was supported by the National Research Foundation of Korea (NRF) grants funded by the Korea government (MSIT) (NRF- 2014R1A2A1A11050006, 2020R1F1A1073595, and 2021R1A2C2006745).

References

  1. Montagna W, Parakkal PF. An introduction to skin. In: The structure & function of skin. ed. Academic Press; 1974. p. 1-17.
  2. Lin T-K, Zhong L, Santiago JL. Anti-inflammatory and skin barrier repair effects of topical application of some plant oils. Int J Mol Sci 2018;19:70. https://doi.org/10.3390/ijms19010070
  3. Bak M-J, Jun M, Jeong W-S. Antioxidant and hepatoprotective effects of the red ginseng essential oil in H(2)O(2)-treated HepG2 cells and CCl(4)-treated mice. Int J Mol Sci 2012;13:2314-30. https://doi.org/10.3390/ijms13022314
  4. Bak MJ, Truong V-L, Ko S-Y, Nguyen XNG, Jun M, Hong S-G, Lee J-W, Jeong W-S. Induction of Nrf2/ARE-mediated cytoprotective genes by red ginseng oil through ASK1-MKK4/7-JNK and p38 MAPK signaling pathways in HepG2 cells. J Ginseng Res 2016;40:423-30. https://doi.org/10.1016/j.jgr.2016.07.003
  5. Bak M-J, Hong S-G, Lee J-W, Jeong W-S. Red ginseng marc oil inhibits iNOS and COX-2 via NFkB and p38 pathways in LPS-stimulated RAW 264.7 macrophages. Molecules 2012;17:13769. https://doi.org/10.3390/molecules171213769
  6. Van-Long T, Ng KA, Woo-Sik J. Red ginseng oil inhibits TPA-induced transformation of skin epidermal JB6 cells. J Med Food 2018;21:380-9. https://doi.org/10.1089/jmf.2017.4082
  7. Truong V-L, Bak MJ, Lee C, Jun M, Jeong W-S. Hair regenerative mechanisms of red ginseng oil and its major components in the testosterone-induced delay of anagen entry in C57BL/6 mice. Molecules 2017;22:1505. https://doi.org/10.3390/molecules22091505
  8. Bak M-J, Kim K-B, Jun M, Jeong W-S. Safety of red ginseng oil for single oral administration in SpragueeDawley rats. J Ginseng Res 2014;38:78-81. https://doi.org/10.1016/j.jgr.2013.11.009
  9. Choi J-S, Jeon M-H, Moon W-S, Moon J-N, Cheon EJ, Kim J-W, Jung SK, Ji Y-H, Son SW, Kim M-R. In vivo hair growth-promoting effect of rice bran extract prepared by supercritical carbon dioxide fluid. Biol Pharm Bull 2014;37: 44-53. https://doi.org/10.1248/bpb.b13-00528
  10. Sahena F, Zaidul ISM, Jinap S, Karim AA, Abbas KA, Norulaini NAN, Omar AKM. Application of supercritical CO2 in lipid extraction - a review. J Food Eng 2009;95:240-53. https://doi.org/10.1016/j.jfoodeng.2009.06.026
  11. Seo HW, Suh JH, So S-H, Kyung J-S, Kim Y-S, Han C-K. Subacute oral toxicity and bacterial mutagenicity study of Korean Red Ginseng oil. J Ginseng Res 2017;41:595-601. https://doi.org/10.1016/j.jgr.2017.01.009
  12. Park HJ, Lee JH, Song YB, Park KH. Effects of dietary supplementation of lipophilic fraction from Panax ginseng on cGMP and cAMP in rat platelets and on blood coagulation. Biol Pharm Bull 1996;19:1434-9. https://doi.org/10.1248/bpb.19.1434
  13. Lee DG, Lee J, Kim K-T, Lee S-W, Kim Y-O, Cho I-H, Kim H-J, Park C-G, Lee S. High-performance liquid chromatography analysis of phytosterols in Panax ginseng root grown under different conditions. J Ginseng Res 2018;42:16-20. https://doi.org/10.1016/j.jgr.2016.10.004
  14. Matsumura Y, Ananthaswamy HN. Toxic effects of ultraviolet radiation on the skin. Toxicol Appl Pharmacol 2004;195:298-308. https://doi.org/10.1016/j.taap.2003.08.019
  15. D'Orazio J, Jarrett S, Amaro-Ortiz A, Scott T. UV radiation and the skin. Int J Mol Sci 2013;14:12222-48. https://doi.org/10.3390/ijms140612222
  16. Schneider MR, Schmidt-Ullrich R, Paus R. The hair follicle as a dynamic miniorgan. Curr Biol 2009;19:132-42.
  17. Cotsarelis G, Millar SE. Towards a molecular understanding of hair loss and its treatment. Trends Mol Med 2001;7:293-301. https://doi.org/10.1016/S1471-4914(01)02027-5
  18. Choi YS, Zhang Y, Xu M, Yang Y, Ito M, Peng T, Cui Z, Nagy A, Hadjantonakis A-K, Lang RA, et al. Distinct functions for Wnt/β-catenin in hair follicle stem cell proliferation and survival and interfollicular epidermal homeostasis. Cell Stem Cell 2013;13:720-33. https://doi.org/10.1016/j.stem.2013.10.003
  19. Huelsken J, Vogel R, Erdmann B, Cotsarelis G, Birchmeier W. β-Catenin controls hair follicle morphogenesis and stem cell differentiation in the skin. Cell 2001;105:533-45. https://doi.org/10.1016/S0092-8674(01)00336-1
  20. Li Y-H, Zhang K, Yang K, Ye J-X, Xing Y-Z, Guo H-Y, Deng F, Lian X-H, Yang T. Adenovirus-mediated Wnt10b overexpression induces hair follicle regeneration. J Invest Dermatol 2013;133:42-8. https://doi.org/10.1038/jid.2012.235
  21. Gat U, DasGupta R, Degenstein L, Fuchs E. De novo hair follicle morphogenesis and hair tumors in mice expressing a truncated beta-catenin in skin. Cell 1998;95:605-14. https://doi.org/10.1016/S0092-8674(00)81631-1
  22. Celso CL, Prowse DM, Watt FM. Transient activation of β-catenin signalling in adult mouse epidermis is sufficient to induce new hair follicles but continuous activation is required to maintain hair follicle tumours. Development 2004;131:1787. https://doi.org/10.1242/dev.01052
  23. Van Genderen C, Okamura RM, Farinas I, Quo RG, Parslow TG, Bruhn L, Grosschedl R. Development of several organs that require inductive epithelialmesenchymal interactions is impaired in LEF-1-deficient mice. Genes Dev 1994;8:2691-703. https://doi.org/10.1101/gad.8.22.2691
  24. Lu G-Q, Wu Z-B, Chu X-Y, Bi Z-G, Fan W-X. An investigation of crosstalk between Wnt/β-catenin and transforming growth factor-β signaling in androgenetic alopecia. Medicine 2016;95:e4297. https://doi.org/10.1097/MD.0000000000004297
  25. Enshell-Seijffers D, Lindon C, Kashiwagi M, Morgan BA. β-catenin activity in the dermal papilla regulates morphogenesis and regeneration of hair. Dev Cell 2010;18:633-42. https://doi.org/10.1016/j.devcel.2010.01.016
  26. Rishikaysh P, Dev K, Diaz D, Qureshi WMS, Filip S, Mokry J. Signaling involved in hair follicle morphogenesis and development. Int. J. Mol. Sci. 2014;15: 1647-70. https://doi.org/10.3390/ijms15011647
  27. Chiang C, Swan RZ, Grachtchouk M, Bolinger M, Litingtung Y, Robertson EK, Cooper MK, Gaffield W, Westphal H, Beachy PA, et al. Essential role for sonic hedgehog during hair follicle morphogenesis. Dev Biol 1999;205:1-9. https://doi.org/10.1006/dbio.1998.9103
  28. Sato N, Leopold PL, Crystal RG. Effect of adenovirus-mediated expression of Sonic hedgehog gene on hair regrowth in mice with chemotherapy-induced alopecia. J Natl Cancer Inst 2001;93:1858-64. https://doi.org/10.1093/jnci/93.24.1858
  29. St-Jacques B, Dassule HR, Karavanova I, Botchkarev VA, Li J, Danielian PS, McMahon JA, Lewis PM, Paus R, McMahon AP. Sonic hedgehog signaling is essential for hair development. Curr Biol 1998;8:1058-69. https://doi.org/10.1016/S0960-9822(98)70443-9
  30. Oro AE, Higgins K. Hair cycle regulation of Hedgehog signal reception. Dev Biol 2003;255:238-48. https://doi.org/10.1016/S0012-1606(02)00042-8
  31. Peus D, Pittelkow MR. Growth factors in hair organ development and the hair growth cycle. Dermatol Clin 1996;14:559-72. https://doi.org/10.1016/S0733-8635(05)70384-3
  32. Stenn KS, Paus R. Controls of hair follicle cycling. Physiol Rev 2001;81: 449-94. https://doi.org/10.1152/physrev.2001.81.1.449
  33. Yano K, Brown LF, Detmar M. Control of hair growth and follicle size by VEGF-mediated angiogenesis. J Clin Invest 2001;107:409-17. https://doi.org/10.1172/JCI11317
  34. Weger N, Schlake T. IGF-I signalling controls the hair growth cycle and the differentiation of hair shafts. J Invest Dermatol 2005;125:873-82. https://doi.org/10.1111/j.0022-202X.2005.23946.x
  35. Li J, Yang Z, Li Z, Gu L, Wang Y, Sung C. Exogenous IGF-1 promotes hair growth by stimulating cell proliferation and down regulating TGF-β1 in C57BL/6 mice in vivo. Growth Horm IGF Res 2014;24:89-94. https://doi.org/10.1016/j.ghir.2014.03.004
  36. Panchaprateep R, Asawanonda P. Insulin-like growth factor-1: roles in androgenetic alopecia. Exp Dermatol 2014;23:216-8. https://doi.org/10.1111/exd.12339
  37. Trueb RM. Further clinical evidence for the effect of IGF-1 on hair growth and alopecia. Skin Appendage Disord 2018;4:90-5. https://doi.org/10.1159/000479333
  38. Buonanno M, Stanislauskas M, Ponnaiya B, Bigelow AW, Randers-Pehrson G, Xu Y, Shuryak I, Smilenov L, Owens DM, Brenner DJ. 207-nm UV light-a promising tool for safe low-cost reduction of surgical site infections. II: in-vivo safety studies. PLOS ONE 2016;11. e0138418. https://doi.org/10.1371/journal.pone.0138418
  39. Tripp CS, Blomme EAG, Chinn KS, Hardy MM, LaCelle P, Pentland AP. Epidermal COX-2 induction following ultraviolet irradiation: suggested mechanism for the role of COX-2 inhibition in photoprotection. J Invest Dermatol 2003;121:853-61. https://doi.org/10.1046/j.1523-1747.2003.12495.x
  40. Rundhaug JE, Fischer SM. Cyclo-oxygenase-2 plays a critical role in UV-induced skin carcinogenesisy. Photochem Photobiol 2008;84:322-9. https://doi.org/10.1111/j.1751-1097.2007.00261.x
  41. Lee JL, Mukhtar H, Bickers DR, Kopelovich L, Athar M. Cyclooxygenases in the skin: pharmacological and toxicological implications. Toxicol Appl Pharmacol 2003;192:294-306. https://doi.org/10.1016/S0041-008X(03)00301-6
  42. Wu N-L, Fang J-Y, Chen M, Wu C-J, Huang C-C, Hung C-F. Chrysin protects epidermal keratinocytes from UVA- and UVB-induced damage. J Agric Food Chem 2011;59:8391-400. https://doi.org/10.1021/jf200931t
  43. Lee C-H, Wu S-B, Hong C-H, Yu H-S, Wei Y-H. Molecular mechanisms of UV-induced apoptosis and its effects on skin residential cells: the implication in UV-based phototherapy. Int J Mol Sci 2013;14:6414-35. https://doi.org/10.3390/ijms14036414
  44. Cory S, Adams JM. The Bcl2 family: regulators of the cellular life-or-death switch. Nat Rev Cancer 2002;2:647-56. https://doi.org/10.1038/nrc883
  45. Green DR, Reed JC. Mitochondria and apoptosis. Science 1998;281:1309. https://doi.org/10.1126/science.281.5381.1309
  46. Shin SW, Jung E, Kim S, Kim J-H, Kim E-G, Lee J, Park D. Antagonizing effects and mechanisms of afzelin against UVB-induced cell damage. PLOS ONE 2013;8. e61971. https://doi.org/10.1371/journal.pone.0061971
  47. Ola MS, Nawaz M, Ahsan H. Role of Bcl-2 family proteins and caspases in the regulation of apoptosis. Mol Cell Biochem 2011;351:41-58. https://doi.org/10.1007/s11010-010-0709-x
  48. Porter AG, Janicke RU. Emerging roles of caspase-3 in apoptosis. Cell Death Differ 1999;6:99-104. https://doi.org/10.1038/sj.cdd.4400476
  49. Yoshihisa Y, Mu Rehman, Shimizu T. Astaxanthin, a xanthophyll carotenoid, inhibits ultraviolet-induced apoptosis in keratinocytes. Exp. Dermatol. 2014;23:178-83. https://doi.org/10.1111/exd.12347
  50. Huang C, Li J, Ding M, Leonard SS, Wang L, Castranova V, Vallyathan V, Shi X. UV induces phosphorylation of protein kinase B (Akt) at ser-473 and thr-308 in mouse epidermal Cl 41 cells through hydrogen peroxide. J Biol Chem 2001;276:40234-40. https://doi.org/10.1074/jbc.M103684200
  51. Bode AM, Dong Z. Mitogen-activated protein kinase activation in UV-induced signal transduction. Sci STKE 2003;2003:re2.
  52. Oliveira MM, Ratti BA, Dare RG, Silva SO, Truiti MdCT, Ueda-Nakamura T, Auzely-Velty R, Nakamura CV. Dihydrocaffeic acid prevents UVB-induced oxidative stress leading to the inhibition of apoptosis and MMP-1 expression via p38 signaling pathway. Oxid Med Cell Longev 2019;2019:1-14.
  53. Dong Z, Huang C, Ma W-Y, Malewicz B, Baumann WJ, Kiss Z. Increased synthesis of phosphocholine is required for UV-induced AP-1 activation. Oncogene 1998;17:1845. https://doi.org/10.1038/sj.onc.1202084
  54. Ma WY, Huang C, Dong Z. Inhibition of ultraviolet C irradiation-induced AP-1 activity by aspirin is through inhibition of JNKs but not erks or P38 MAP kinase. Int J Oncol 1998;12:565-73.
  55. Halliday GM. Inflammation, gene mutation and photoimmunosuppression in response to UVR-induced oxidative damage contributes to photocarcinogenesis. Mutat Res 2005;571:107-20. https://doi.org/10.1016/j.mrfmmm.2004.09.013
  56. Truong V-L, Jun M, Jeong W-S. Role of resveratrol in regulation of cellular defense systems against oxidative stress. BioFactors 2018;44:36-49. https://doi.org/10.1002/biof.1399
  57. Lin Q, Weis S, Yang G, Weng Y-H, Helston R, Rish K, Smith A, Bordner J, Polte T, Gaunitz F, et al. Heme oxygenase-1 protein localizes to the nucleus and activates transcription factors important in oxidative stress. J Biol Chem 2007;282:20621-33. https://doi.org/10.1074/jbc.M607954200

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