DOI QR코드

DOI QR Code

Novel Effect of Hyaluronan and Proteoglycan Link Protein 1 (HAPLN1) on Hair Follicle Cells Proliferation and Hair Growth

  • Hae Chan Ha (Department of Environmental & Health Chemistry, College of Pharmacy, Chung-Ang University) ;
  • Dan Zhou (Department of Environmental & Health Chemistry, College of Pharmacy, Chung-Ang University) ;
  • Zhicheng Fu (Department of Environmental & Health Chemistry, College of Pharmacy, Chung-Ang University) ;
  • Moon Jung Back (Department of Environmental & Health Chemistry, College of Pharmacy, Chung-Ang University) ;
  • Ji Min Jang (Department of Environmental & Health Chemistry, College of Pharmacy, Chung-Ang University) ;
  • In Chul Shin (Department of Environmental & Health Chemistry, College of Pharmacy, Chung-Ang University) ;
  • Dae Kyong Kim (Department of Environmental & Health Chemistry, College of Pharmacy, Chung-Ang University)
  • 투고 : 2023.04.04
  • 심사 : 2023.06.23
  • 발행 : 2023.09.01

초록

Hair loss is a common condition that can have a negative impact on an individual's quality of life. The severe side effects and the low efficacy of current hair loss medications create unmet needs in the field of hair loss treatment. Hyaluronan and Proteoglycan Link Protein 1 (HAPLN1), one of the components of the extracellular matrix, has been shown to play a role in maintaining its integrity. HAPLN1 was examined for its ability to impact hair growth with less side effects than existing hair loss treatments. HAPLN1 was predominantly expressed in the anagen phase in three stages of the hair growth cycle in mice and promotes the proliferation of human hair matrix cells. Also, recombinant human HAPLN1 (rhHAPLN1) was shown to selectively increase the levels of transforming growth factor-β receptor II in human hair matrix cells. Furthermore, we observed concomitant activation of the ERK1/2 signaling pathway following treatment with rhHAPLN1. Our results indicate that rhHAPLN1 elicits its cell proliferation effect via the TGF-β2-induced ERK1/2 pathway. The prompt entering of the hair follicles into the anagen phase was observed in the rhHAPLN1-treated group, compared to the vehicle-treated group. Insights into the mechanism underlying such hair growth effects of HAPLN1 will provide a novel potential strategy for treating hair loss with much lower side effects than the current treatments.

키워드

과제정보

This research was supported by the Chung-Ang University Young Scientist Scholarship in 2017, and also supported by a grant from the National Research Foundation of Korea (NRF-2017M3A9D8048414) funded by the Korean government (Ministry of Science and ICT).

참고문헌

  1. Alonso, L. and Fuchs, E. (2006) The hair cycle. J. Cell Sci. 119, 391-393. https://doi.org/10.1242/jcs.02793
  2. Binette, F., Cravens, J., Kahoussi, B., Haudenschild, D. R. and Goetinck, P. F. (1994) Link protein is ubiquitously expressed in non-cartilaginous tissues where it enhances and sta-bilizes the interaction of proteoglycans with hyaluronic acid. J. Biol. Chem. 269, 19116-19122. https://doi.org/10.1016/S0021-9258(17)32282-2
  3. Bourguignon, L. Y., Singleton, P. A., Zhu, H. and Zhou, B. (2002) Hyaluronan promotes signaling interaction between CD44 and the transforming growth factor beta receptor I in metastatic breast tumor cells. J. Biol. Chem. 277, 39703-39712. https://doi.org/10.1074/jbc.M204320200
  4. Buckwalter, J. A., Rosenberg, L. C. and Tang, L. H. (1984) The effect of link protein on proteoglycan aggregate structure. An electron microscopic study of the molecular architecture and dimensions of proteoglycan aggregates reassembled from the proteoglycan monomers and link proteins of bovine fetal epiphyseal cartilage. J. Biol. Chem. 259, 5361-5363. https://doi.org/10.1016/S0021-9258(18)91012-4
  5. Chase, H. B. (1954) Growth of the hair. Physiol. Rev. 34, 113-126. https://doi.org/10.1152/physrev.1954.34.1.113
  6. Campiche, R., Jackson, E., Laurent, G., Roche, M., Gougeon, S., Seroul, P., Strobel, S., Massironi, M. and Gempeler, M. (2019) Skin filling and firming activity of a hyaluronic acid inducing synthetic tripeptide. Int. J. Pept. Res. Ther. 26, 181-189.
  7. Derynck, R. and Zhang, Y. E. (2003) Smad-dependent and Smad-independent pathways in TGF-beta family signalling. Nature 425, 577-584. https://doi.org/10.1038/nature02006
  8. Danielson, B. T., Knudson, C. B. and Knudson, W. (2015) Extracellular processing of the cartilage proteoglycan aggregate and its effect on CD44-mediated internalization of hyaluronan. J. Biol. Chem. 290, 9555-9570. https://doi.org/10.1074/jbc.M115.643171
  9. Foitzik, K., Lindner, G., Mueller-Roever, S., Maurer, M., Botchkareva, N., Botchkarev, V., Handjiski, B., Metz, M., Hibino, T., Soma, T., Dotto, G. P. and Paus, R. (2000) Control of murine hair follicle regression (catagen) by TGF-beta1 in vivo. FASEB J. 14, 752-760. https://doi.org/10.1096/fasebj.14.5.752
  10. Foitzik, K., Paus, R., Doetschman, T. and Dotto, G. P. (1999) The TGFbeta2 isoform is both a required and sufficient inducer of murine hair follicle morphogenesis. Dev. Biol. 212, 278-289. https://doi.org/10.1006/dbio.1999.9325
  11. Govindan, J. and Iovine, M. K. (2014) Hapln1a is required for connexin43-dependent growth and patterning in the regenerating fin skeleton. PLoS One 9, e88574.
  12. Hibino, T. and 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
  13. Huang, F. and Chen, Y. G. (2012) Regulation of TGF-beta receptor activity. Cell Biosci. 2, 9.
  14. Hardingham, T. E. (1979) The role of link-protein in the structure of cartilage proteoglycan aggregates. Biochem. J. 177, 237-247. https://doi.org/10.1042/bj1770237
  15. Harada, H. and Takahashi, M. (2007) CD44-dependent intracellular and extracellular catabolism of hyaluronic acid by hyaluronidase-1 and -2. J. Biol. Chem. 282, 5597-5607. https://doi.org/10.1074/jbc.M608358200
  16. Hua, Q., Knudson, C. B. and Knudson. W. (1993) Internalization of hyaluronan by chondrocytes occurs via receptor-mediated endocytosis. J. Cell Sci. 106, 365-375. https://doi.org/10.1242/jcs.106.1.365
  17. Ito, T., Williams, J. D., Fraser, D. J. and Phillips, A. O. (2004) Hyaluronan regulates transforming growth factor-beta1 receptor compartmentalization. J. Biol. Chem. 279, 25326-25332. https://doi.org/10.1074/jbc.M403135200
  18. Kim, M. J., Seong, K. Y., Kim, D. S., Jeong, J. S., Kim, S. Y., Lee, S., Yang, S. Y. and An, B. S. (2022) Minoxidil-loaded hyaluronic acid dissolving microneedles to alleviate hair loss in an alopecia animal model. Acta Biomater. 143, 189-202. https://doi.org/10.1016/j.actbio.2022.02.011
  19. Kultti, A., Pasonen-Seppanen, S., Jauhiainen, M., Rilla, K. J., Karna, R., Pyoria, E., Tammi, R. H. and Tammi, M. I. (2009) 4-Methylumbelliferone inhibits hyaluronan synthesis by depletion of cellular UDP-glucuronic acid and downregulation of hyaluronan synthase 2 and 3. Exp. Cell Res. 315, 1914-1923. https://doi.org/10.1016/j.yexcr.2009.03.002
  20. Knudson, C. B. and Knudson, W. (1993) Hyaluronan-binding proteins in development, tissue homeostasis, and disease. FASEB J. 7, 1233-1241. https://doi.org/10.1096/fasebj.7.13.7691670
  21. Mori, O., Hachisuka, H. and Sasai, Y. (1996) Effects of transforming growth factor beta 1 in the hair cycle. J. Dermatol. 23, 89-94. https://doi.org/10.1111/j.1346-8138.1996.tb03976.x
  22. Massague, J., Blain, S. W. and Lo, R. S. (2000) TGFbeta signaling in growth control, cancer, and heritable disorders. Cell 103, 295-309. https://doi.org/10.1016/S0092-8674(00)00121-5
  23. Niimori, D., Kawano, R., Felemban, A., Niimori-Kita, K., Tanaka, H., Ihn, H. and Ohta, K. (2012) Tsukushi controls the hair cycle by regulating TGF-β1 signaling. Dev. Biol. 372, 81-87. https://doi.org/10.1016/j.ydbio.2012.08.030
  24. Neuzillet, C., Hammel, P., Tijeras-Raballand, A., Couvelard, A. and Raymond, E. (2013) Targeting the Ras-ERK pathway in pancreatic adenocarcinoma. Cancer Metastasis Rev. 32, 147-162. https://doi.org/10.1007/s10555-012-9396-2
  25. Oshimori, N. and Fuchs, E. (2012) Paracrine TGF-beta signaling counterbalances BMP-mediated repression in hair follicle stem cell activation. Cell Stem Cell 10, 63-75. https://doi.org/10.1016/j.stem.2011.11.005
  26. Philpott, M. P., Green, M. R. and Kealey, T. (1990) Human hair growth in vitro. J. Cell Sci. 97, 463-471. https://doi.org/10.1242/jcs.97.3.463
  27. Papakonstantinou, E., Roth, M. and Karakiulakis, G. (2012) Hyaluronic acid: a key molecule in skin aging. Dermatoendocrinol 4, 253-258. https://doi.org/10.4161/derm.21923
  28. Plikus, M. V. and Chuong, C. M. (2008) Complex hair cycle domain patterns and regenerative hair waves in living rodents. J. Invest. Dermatol. 128, 1071-1080. https://doi.org/10.1038/sj.jid.5701180
  29. Spicer, A. P., Joo, A. and Bowling, R. A., Jr. (2003) A hyaluronan binding link protein gene family whose members are physically linked adjacent to chondroitin sulfate proteoglycan core protein genes: the missing links. J. Biol. Chem. 278, 21083-21091. https://doi.org/10.1074/jbc.M213100200
  30. Sato, N., Leopold, P. L. and Crystal, R. G. (1999) Induction of the hair growth phase in postnatal mice by localized transient expression of Sonic hedgehog. J. Clin. Investig. 104, 855-864. https://doi.org/10.1172/JCI7691
  31. Taghiabadi, E., Nilforoushzadeh, M. A. and Aghdami, N. (2020) Maintaining hair inductivity in human dermal papilla cells: a review of effective methods. Skin Pharmacol. Physiol. 33, 280-292. https://doi.org/10.1159/000510152
  32. Tang, P., Wang, X., Zhang, M., Huang, S., Lin, C., Yan, F., Deng, Y., Zhang, L. and Zhang, L. (2019) Activin B stimulates mouse vibrissae growth and regulates cell proliferation and cell cycle progression of hair matrix cells through ERK signaling. Int. J. Mol. Sci. 20, 853.
  33. Warren, J. P., Miles, D. E., Kapur, N., Wilcox, R. K. and Beales, P. A. (2021) Hydrodynamic mixing tunes the stiffness of proteoglycan-mimicking physical hydrogels. Adv. Healthc. Mater. 10, e2001998.
  34. Xi, J., Ting, Y. L., Xue, L. and Dan, L. (2019) Effect of hyaluronic acid: Mechanistic investigations via topological and functional analysis of its protein interaction network. Trop. J. Pharm. Res. 18, 1919-1925.