DOI QR코드

DOI QR Code

Hair-Loss Preventing Effect of Grateloupia elliptica

  • Kang, Jung-Il (Department of Medicine, School of Medicine, Institute of Medical Sciences, Jeju National University) ;
  • Kim, Sang-Cheol (Department of Medicine, School of Medicine, Institute of Medical Sciences, Jeju National University) ;
  • Han, Sang-Chul (Department of Medicine, School of Medicine, Institute of Medical Sciences, Jeju National University) ;
  • Hong, Hye-Jin (Department of Medicine, School of Medicine, Institute of Medical Sciences, Jeju National University) ;
  • Jeon, You-Jin (Aqua Green Technology Co.) ;
  • Kim, Bo-Ra (Enprani Co., Ltd. R&D Center of Skin Science and Cosmetics) ;
  • Koh, Young-Sang (Department of Medicine, School of Medicine, Institute of Medical Sciences, Jeju National University) ;
  • Yoo, Eun-Sook (Department of Medicine, School of Medicine, Institute of Medical Sciences, Jeju National University) ;
  • Kang, Hee-Kyoung (Department of Medicine, School of Medicine, Institute of Medical Sciences, Jeju National University)
  • Received : 2011.07.06
  • Accepted : 2011.11.29
  • Published : 2012.01.31

Abstract

This study was conducted to evaluate the effect of Grateloupia elliptica, a seaweed native to Jeju Island, Korea, on the prevention of hair loss. When immortalized rat vibrissa dermal papilla cells were treated with extract of G. elliptica, the proliferation of dermal papilla cells significantly increased. In addition, the G. elliptica extract significantly inhibited the activity of $5{\alpha}$-reductase, which converts testosterone to dihydrotestosterone (DHT), a main cause of androgenetic alopecia. On the other hand, the G. elliptica extract promoted $PGE_2$ production in HaCaT cells in a dose-dependent manner. The G. elliptica extract exhibited particularly high inhibitory effect on LPS-stimulated IL-12, IL-6, and TNF-${\alpha}$ production in lipopolysaccharide (LPS)-stimulated bone marrow-derived dendritic cells. The G. elliptica extract also showed inhibitory activity against Pityrosporum ovale, a main cause of dandruff. These results suggest that G. elliptica extract has the potential to treat alopecia via the proliferation of dermal papilla, $5{\alpha}$-reductase inhibition, increase of $PGE_2$ production, decrease of LPS-stimulated pro-inflammatory cytokines and inhibitory activity against Pityrosporum ovale.

Keywords

References

  1. Alkhalifah, A., Alsantali, A., Wang, E., McElwee, K. J. and Shapiro, J. (2010) Alopecia areata update: part I. Clinical picture, histopathology, and pathogenesis. J. Am. Acad. Dermatol. 62, 177-188, quiz 189-190. https://doi.org/10.1016/j.jaad.2009.10.032
  2. Anesini, C. and Perez, C. (1993) Screening of plants used in Argentine folk medicine for antimicrobial activity. J. Ethnopharmacol. 39, 119-128. https://doi.org/10.1016/0378-8741(93)90027-3
  3. Bernard, B. A. (2008) Factors affecting PGE2 production in seaweed gracilaria tenuistipitata. J. Food Drug Anal. 59, 59-65.
  4. Burton, J. L. and Marshall, A. (1979) Hypertrichosis due to minoxidil. Br. J. Dermatol. 101, 593-595. https://doi.org/10.1111/j.1365-2133.1979.tb11892.x
  5. Carmichael, J., DeGraff, W. G., Gazdar, A. F., Minna, J. D. and Mitchell, J. B. (1987) Evaluation of a tetrazolium-based semiautomated colorimetric assay: assessment of chemosensitivity testing. Cancer Res. 47, 936-942.
  6. Coleman, R. A., Grix, S. P., Head, S. A., Louttit, J. B., Mallett, A. and Sheldrick, R. L. (1994a) A novel inhibitory prostanoid receptor in piglet saphenous vein. Prostaglandins. 47, 151-168.
  7. Coleman, R. A., Smith, W. L. and Narumiya, S. (1994b) International Union of Pharmacology classifi cation of prostanoid receptors: properties, distribution, and structure of the receptors and their subtypes. Pharmacol. Rev. 46, 205-229.
  8. Colombe, L., Michelet, J. F. and Bernard, B. A. (2008) Prostanoid receptors in anagen human hair follicles. Exp. Dermatol. 17, 63-72.
  9. Colombe, L., Vindrios, A., Michelet, J. F. and Bernard, B. A. (2007) Prostaglandin metabolism in human hair follicle. Exp. Dermatol. 16, 762-769. https://doi.org/10.1111/j.1600-0625.2007.00586.x
  10. Elliott, K., Stephenson, T. J. and Messenger, A. G. (1999) Differences in hair follicle dermal papilla volume are due to extracellular matrix volume and cell number: implications for the control of hair follicle size and androgen responses. J. Invest. Dermatol. 113, 873-877. https://doi.org/10.1046/j.1523-1747.1999.00797.x
  11. Filsell, W., Little, J. C., Stones, A. J., Granger, S. P. and Bayley, S. A. (1994) Transfection of rat dermal papilla cells with a gene encoding a temperature-sensitive polyomavirus large T antigen generates cell lines retaining a differentiated phenotype. J. Cell. Sci. 107 (Pt 7), 1761-1772.
  12. Gately, M. K., Renzetti, L. M., Magram, J., Stern, A. S., Adorini, L., Gubler, U. and Presky, D. H. (1998) The interleukin-12/interleukin-12-receptor system: role in normal and pathologic immune responses. Annu. Rev. Immunol. 16, 495-521. https://doi.org/10.1146/annurev.immunol.16.1.495
  13. Gilhar, A. and Kalish, R. S. (2006) Alopecia areata: a tissue specifi c autoimmune disease of the hair follicle. Autoimmun. Rev. 5, 64-69. https://doi.org/10.1016/j.autrev.2005.07.001
  14. Gormley, G. J. (1995) Finasteride: a clinical review. Biomed. Pharmacother. 49, 319-324. https://doi.org/10.1016/0753-3322(96)82658-8
  15. Hamaoka, H., Minakuchi, K., Miyoshi, H., Arase, S., Chen, C. H. and Nakaya, Y. (1997) Effect of K+ channel openers on K+ channel in cultured human dermal papilla cells. J. Med. Invest. 44, 73-77.
  16. Han, J. H., Kwon, O. S., Chung, J. H., Cho, K. H., Eun, H. C. and Kim, K. H. (2004) Effect of minoxidil on proliferation and apoptosis in dermal papilla cells of human hair follicle. J. Dermatol. Sci. 34, 91-98. https://doi.org/10.1016/j.jdermsci.2004.01.002
  17. Hibino, T., Nishiyama, T. (2004) Role of TGF-beta2 in the human hair cycle. J. Dermatol. Sci. 35, 9-18. https://doi.org/10.1016/j.jdermsci.2003.12.003
  18. Hirosumi, J., Nakayama, O., Fagan, T., Sawada, K., Chida, N., Inami, M., Takahashi, S., Kojo, H., Notsu, Y. and Okuhara, M. (1995) FK143, a novel nonsteroidal inhibitor of steroid 5 alpha-reductase: (1) In vitro effects on human and animal prostatic enzymes. J. Steroid Biochem. Mol. Biol. 52, 357-363. https://doi.org/10.1016/0960-0760(94)00187-Q
  19. Horsley, V., Aliprantis, A. O., Polak, L., Glimcher, L. H. and Fuchs, E. (2008) NFATc1 balances quiescence and proliferation of skin stem cells. Cell 132, 299-310. https://doi.org/10.1016/j.cell.2007.11.047
  20. Inui, S., Fukuzato, Y., Nakajima, T., Yohikawa, K., Itami, S. (2002) Androgen-inducible TGF-beta1 from balding dermal papilla cells inhibits epithelial cell growth: a clue to understand paradoxical effects of androgen on human hair growth. J. Investig. Dermatol. Symp. Proc. 16, 1967-1969.
  21. Itami, S., Kurata, S. and Takayasu, S. (1995) Androgen induction of follicular epithelial cell growth is mediated via insulin-like growth factor-I from dermal papilla cells. Biochem. Biophys. Res. Commun. 212, 988-994. https://doi.org/10.1006/bbrc.1995.2067
  22. Jahoda, C. A., Horne, K. A. and Oliver, R. F. (1984) Induction of hair growth by implantation of cultured dermal papilla cells. Nature 311, 560-562. https://doi.org/10.1038/311560a0
  23. Johnstone, M. A. and Albert, D. M. (2002) Prostaglandin-induced hair growth. Surv. Ophthalmol. 47 Suppl 1, S185-202. https://doi.org/10.1016/S0039-6257(02)00307-7
  24. Kaufman, K. D., (1996) Androgen metabolism as it affects hair growth in androgenetic alopecia. Dermatol. Clin. 14, 697-711. https://doi.org/10.1016/S0733-8635(05)70396-X
  25. Kaufman, K. D., Girman, C. J., Round, E. M., Johnson-Levonas, A. O., Shah, A. K. and Rotonda, J. (2008) Progression of hair loss in men with androgenetic alopecia (male pattern hair loss): long-term (5-year) controlled observational data in placebo-treated patients. Eur. J. Dermatol. 18, 407-411.
  26. Kaufman, K. D., Olsen, E. A., Whiting, D., Savin, R., DeVillez, R., Bergfeld, W., Price, V. H., Van Neste, D., Roberts, J. L., Hordinsky, M., Shapiro, J., Binkowitz, B. and Gormley, G. J. (1998) Finasteride in the treatment of men with androgenetic alopecia. Finasteride Male Pattern Hair Loss Study Group. J. Am. Acad. Dermatol. 39, 578-589. https://doi.org/10.1016/S0190-9622(98)70007-6
  27. Kaufman, K. D., Rotonda, J., Shah, A. K. and Meehan, A. G. (2008) Long-term treatment with fi nasteride 1 mg decreases the likelihood of developing further visible hair loss in men with androgenetic alopecia (male pattern hair loss). Eur. J. Dermatol. 18, 400-406.
  28. Kim, K. Y., Nam, K. A., Kurihara, H. and Kim, S. M. (2008) Potent alpha-glucosidase inhibitors purifi ed from the red alga Grateloupia elliptica. Phytochemistry 69, 2820-2825. https://doi.org/10.1016/j.phytochem.2008.09.007
  29. Koh, Y. S., Koo, J. E., Biswas, A. and Kobayashi, K. S. (2010) MyD88-dependent signaling contributes to host defense against ehrlichial infection. PLoS One. 5, e11758. https://doi.org/10.1371/journal.pone.0011758
  30. Kwack, M. H., Sung, Y. K., Chung, E. J., Im, S. U., Ahn, J. S., Kim, M. K., Kim, J. C. (2008) Dihydrotestosterone-inducible dickkopf 1 from balding dermal papilla cells causes apoptosis in follicular keratinocytes. J. Invest. Dermatol. 128, 262-269.
  31. Kwack, M. H., Kang, B. M., Kim, M. K., Kim, J. C. and Sung, Y. K. (2011). Minoxidil activates beta-catenin pathway in human dermal papilla cells: A possible explanation for its anagen prolongation effect. J. Dermatol. Sci. 62, 154-159. https://doi.org/10.1016/j.jdermsci.2011.01.013
  32. Lachgar, S., Charveron, M., Gall, Y. and Bonafe, J. L. (1998) Minoxidil upregulates the expression of vascular endothelial growth factor in human hair dermal papilla cells. Br. J. Dermatol. 138, 407-411. https://doi.org/10.1046/j.1365-2133.1998.02115.x
  33. Lachgar, S., Moukadiri, H., Jonca, F., Charveron, M., Bouhaddioui, N., Gall, Y., Bonafe, J. L. and Plouet, J. (1996) Vascular endothelial growth factor is an autocrine growth factor for hair dermal papilla cells. J. Invest. Dermatol. 106, 17-23. https://doi.org/10.1111/1523-1747.ep12326964
  34. Messenger, A. G. and Rundegren, J. (2004) Minoxidil: mechanisms of action on hair growth. Br. J. Dermatol. 150, 186-194. https://doi.org/10.1111/j.1365-2133.2004.05785.x
  35. Nematian, J., Ravaghi, M., Gholamrezanezhad, A. and Nematian, E. (2006) Increased hair shedding may be associated with the presence of Pityrosporum ovale. Am. J. Clin. Dermatol. 7, 263-266. https://doi.org/10.2165/00128071-200607040-00008
  36. Pierard-Franchimont, C., Xhaufl aire-Uhoda, E., Loussouarn, G., Saint Leger, D. and Pierard, G. E. (2006) Dandruff-associated smouldering alopecia: a chronobiological assessment over 5 years. Clin. Exp. Dermatol. 31, 23-26. https://doi.org/10.1111/j.1365-2230.2005.02026.x
  37. Shimaoka, S., Imai, R. and Ogawa, H. (1994) Dermal papilla cells express hepatocyte growth factor. J. Dermatol. Sci. 7 Suppl, S79-83. https://doi.org/10.1016/0923-1811(94)90038-8
  38. Shorter, K., Farjo, N. P., Picksley, S. M. and Randall, V. A. (2008) Human hair follicles contain two forms of ATP-sensitive potassium channels, only one of which is sensitive to minoxidil. FASEB. J. 22, 1725-1736. https://doi.org/10.1096/fj.07-099424
  39. Sinclair, R. (1998) Male pattern androgenetic alopecia. BMJ. 317, 865-869. https://doi.org/10.1136/bmj.317.7162.865
  40. Soma, T., Dohrmann, C. E., Hibino, T. and Raftery, L. A. (2003) Profile of transforming growth factor-beta responses during the murine hair cycle. J. Invest. Dermatol. 121, 969-975. https://doi.org/10.1046/j.1523-1747.2003.12516.x
  41. Soma, T., Tsuji, Y. and Hibino, T. (2002) Involvement of transforming growth factor-beta2 in catagen induction during the human hair cycle. J. Invest. Dermatol. 118, 993-997. https://doi.org/10.1046/j.1523-1747.2002.01746.x
  42. Taki, S., Sato, T., Ogasawara, K., Fukuda, T., Sato, M., Hida, S., Suzuki, G., Mitsuyama, M., Shin, E. H., Kojima, S., Taniguchi, T. and Asano, Y. (1997) Multistage regulation of Th1-type immune responses by the transcription factor IRF-1. Immunity 6, 673-679. https://doi.org/10.1016/S1074-7613(00)80443-4
  43. Tong, X., Coulombe, P. A. (2006) Keratin 17 modulates hair follicle cycling in a TNFalpha-dependent fashion. Genes Dev. 20, 1353-1364. https://doi.org/10.1101/gad.1387406
  44. Uno, H., Zimbric, M. L., Albert, D. M. and Stjernschantz, J. (2002) Effect of latanoprost on hair growth in the bald scalp of the stumptailed macacque: a pilot study. Acta Derm. Venereol. 82, 7-12. https://doi.org/10.1080/000155502753600803
  45. Van Neste, D., Fuh, V., Sanchez-Pedreno, P., Lopez-Bran, E., Wolff, H., Whiting, D., Roberts, J., Kopera, D., Stene, J. J., Calvieri, S., Tosti, A., Prens, E., Guarrera, M., Kanojia, P., He, W. and Kaufman, K. D. (2000) Finasteride increases anagen hair in men with androgenetic alopecia. Br. J. Dermatol. 143, 804-810. https://doi.org/10.1046/j.1365-2133.2000.03780.x
  46. Whiting, D. A., Waldstreicher, J., Sanchez, M. and Kaufman, K. D. (1999) Measuring reversal of hair miniaturization in androgenetic alopecia by follicular counts in horizontal sections of serial scalp biopsies: results of fi nasteride 1 mg treatment of men and postmenopausal women. J. Investig. Dermatol. Symp. Proc. 4, 282-284. https://doi.org/10.1038/sj.jidsp.5640230
  47. Yamamoto, S. and Kato, R. (1994) Hair growth-stimulating effects of cyclosporin A and FK506, potent immunosuppressants. J. Dermatol. Sci. 7 Suppl, S47-54. https://doi.org/10.1016/0923-1811(94)90035-3
  48. Yang, E. J., Moon, J. Y., Kim, M. J., Kim, D. S., Kim, C. S., Lee, W. J., Lee, N. H. and Hyun, C. G. (2010) Inhibitory effect of Jeju endemic seaweeds on the production of pro-infl ammatory mediators in mouse macrophage cell line RAW 264.7. J. Zhejiang Univ. Sci. B. 11, 315-322.

Cited by

  1. Anti-Inflammatory Effect of Ethanol Extract from Grateloupia elliptica Holmes on Lipopolysaccharide-Induced Inflammatory Responses in RAW 264.7 Cells and Mice Ears vol.44, pp.8, 2015, https://doi.org/10.3746/jkfn.2015.44.8.1128
  2. Sphingosine 1-phosphate induced anti-atherogenic and atheroprotective M2 macrophage polarization through IL-4 vol.26, pp.10, 2014, https://doi.org/10.1016/j.cellsig.2014.07.009
  3. Comparison of Saccharina japonica–Undaria pinnatifida Mixture and Minoxidil on Hair Growth Promoting Effect in Mice vol.43, pp.6, 2016, https://doi.org/10.5999/aps.2016.43.6.498
  4. Therapeutic Effects of S-Petasin on Disease Models of Asthma and Peritonitis vol.23, pp.1, 2015, https://doi.org/10.4062/biomolther.2014.069
  5. Identification of a novel anti-inflammatory compound, α-cubebenoate from Schisandra chinensis vol.153, pp.1, 2014, https://doi.org/10.1016/j.jep.2014.02.027
  6. Hair growth effect of traditional Chinese medicine BeauTop on androgenetic alopecia patients: A randomized double-blind placebo-controlled clinical trial vol.13, pp.1, 2017, https://doi.org/10.3892/etm.2016.3935
  7. Seaweeds as Source of Bioactive Substances and Skin Care Therapy—Cosmeceuticals, Algotheraphy, and Thalassotherapy vol.5, pp.4, 2018, https://doi.org/10.3390/cosmetics5040068
  8. screening model for hair growth vol.40, pp.5, 2018, https://doi.org/10.1111/ics.12489
  9. Melandrium firmumExtract Promotes Hair Growth by Modulating 5α-Reductase Activity and Gene Expression in C57BL/6J Mice vol.31, pp.5, 2012, https://doi.org/10.5021/ad.2019.31.5.502
  10. Monoterpenoid Loliolide Regulates Hair Follicle Inductivity of Human Dermal Papilla Cells by Activating the AKT/β-Catenin Signaling Pathway vol.29, pp.11, 2012, https://doi.org/10.4014/jmb.1908.08018
  11. Stimulating hair growth via hormesis: Experimental foundations and clinical implications vol.152, pp.None, 2012, https://doi.org/10.1016/j.phrs.2019.104599
  12. 흑효모를 이용한 참도박 발효 추출물의 항산화 효과와 티로시나제 및 콜라게나제 저해효과 vol.46, pp.1, 2020, https://doi.org/10.15230/scsk.2020.46.1.1
  13. Kinetic Cytokine Secretion Profile of LPS-Induced Inflammation in the Human Skin Organ Culture vol.12, pp.4, 2012, https://doi.org/10.3390/pharmaceutics12040299
  14. Effects of Ethanol Extracts from Grateloupia elliptica, a Red Seaweed, and Its Chlorophyll Derivative on 3T3-L1 Adipocytes: Suppression of Lipid Accumulation through Downregulation of Adipogenic Prote vol.19, pp.2, 2021, https://doi.org/10.3390/md19020091