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Preservation of a specialized phenotype of dermal papilla cells of a human hair follicle under cultivation conditions

  • Cell Biology
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Abstract

Possible ways to extend cultivation of dermal papilla cells without the loss of expression of their specific markers were studied. The effect of extracellular matrix components, as well as valproic acid, on the maintenance of the phenotype of dermal papilla cells was studied for the first time. Two ways of cultivation (in a monolayer culture and in spheroids) were used. It was established that a short-term positive effect is reached during the addition of the BMP6 growth factor and vitamin D3 in the monolayer culture, while cultivation in spheroids or in the presence of valproic acid allows us to preserve most efficiently the initial phenotype of these cells in vitro. The significance of the results obtained for tissue engineering and for the study of regeneration processes is discussed.

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References

  • Aoi, N., Inoue, K., Chikanishi, T., Fujiki, R., Yamamoto, H., Kato, H., Eto, H., Doi, K., Itami, S., Kato, S., and Yoshimura, K., 1a,25-Dihydroxyvitamin D3 modulates the hair-inductive capacity of dermal papilla cells: therapeutic potential for hair regeneration, Stem Cells Transl. Med., 2012, vol. 1, pp. 615–626.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baeg, G.H. and Perrimon, N., Functional binding of secreted molecules to heparan sulfate proteoglycans in Drosophila, Curr. Opin. Cell Biol., 2000, vol. 12, pp. 575–580.

    Article  CAS  PubMed  Google Scholar 

  • Béchard, D., Gentina, T., Delehedde, M., Scherpereel, A., Lyon, M., Aumercier, M., Vazeux, R., Richet, C., Degand, P., Jude, B., Janin, A., Fernig, D.G., Tonnel, A.B., and Lassalle, P., Endocan is a novel chondroitin sulfate/ dermatan sulfate proteoglycan that promotes hepatocyte growth factor/scatter factor mitogenic activity, J. Biol. Chem., 2001, vol. 276, pp. 48341–48349.

    Article  PubMed  Google Scholar 

  • Benelli, R. and Albini, A., In vitro models of angiogenesis: the use of matrigel, Int. J. Biol. Markers, 1999, vol. 14, pp. 234–246.

    Google Scholar 

  • Bobis, S., Jarocha, D., and Majka, M., Mesenchymal stem cells: characteristics and clinical applications, Folia Histochem. Cytobiol., 2006, vol. 44, pp. 215–230.

    CAS  PubMed  Google Scholar 

  • Botchkarev, V.A. and Paus, R., Molecular biology of hair morphogenesis: development and cycling, J. Exp. Zool. B. Mol. Dev. Evol., 2003, vol. 298, pp. 164–180.

    Article  PubMed  Google Scholar 

  • Chermnykh, E.S., Vorotelyak, E.A., Gnedeva, K.Y., Moldaver, M.V., Yegorov, Y.E., Vasiliev, A.V., and Terskikh, V.V., Dermal papilla cells induce keratinocyte tubulogenesis in culture, Histochem. Cell Biol., 2010, vol. 133, pp. 567–576.

    Article  CAS  PubMed  Google Scholar 

  • Chueh, S.C., Lin, S.J., Chen, C.C., Lei, M., Wang, L.M., Widelitz, R., Hughes, M.W., Jiang, T.X., and Chuong, C.M., Therapeutic strategy for hair regeneration: hair cycle activation, niche environment modulation, wound-induced follicle neogenesis, and stem cell engineering, Expert Opin. Biol. Ther., 2013, vol. 13, pp. 377–391.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harel, S., Higgins, C.A., Cerise, J.E., Dai, Z., Chen, J.C., Clynes, R., and Christiano, A.M., Pharmacologic inhibition of JAK–STAT signaling promotes hair growth, Sci. Adv., 2015, vol. 1, p. e1500973.

    Article  PubMed  PubMed Central  Google Scholar 

  • Higgins, C.A., Richardson, G.D., Ferdinando, D., Westgate, G.E., and Jahoda, C.A., Modelling the hair follicle dermal papilla using spheroid cell cultures, Exp. Dermatol., 2010, vol. 19, pp. 546–548.

    Article  PubMed  Google Scholar 

  • Higgins, C.A., Chen, J.C., Cerise, J.E., Jahoda, C.A.B., and Christiano, A.M., Microenvironmental reprogramming by three-dimensional culture enables dermal papilla cells to induce de novo human hair-follicle growth, Proc. Natl. Acad. Sci. U. S. A., 2013, vol. 110, pp. 19679–19688.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hsieh, J.C., Sisk, J.M., Jurutka, P.W., Haussler, C.A., Slater, S.A., Haussler, M.R., and Thompson, C.C., Physical and functional interaction between the vitamin D receptor and hairless corepressor, two proteins required for hair cycling, J. Biol. Chem., 2003, vol. 278, pp. 38665–38674.

    Article  CAS  PubMed  Google Scholar 

  • Hsieh, J.C., Estess, R.C., Kaneko, I., Whitfield, G.K., Jurutka, P.W., and Haussler, M.R., Vitamin D receptormediated control of soggy, wise, and hairless gene expression in keratinocytes, J. Cell Mol. Med., 2009, vol. 13, pp. 4643–4656.

    Article  Google Scholar 

  • Huang, Y.C., Chan, C.C., Lin, W.T., Chiu, H.Y., Tsai, R.Y., Tsai, T.H., Chan, J.Y., and Lin, S.J., Scalable production of controllable dermal papilla spheroids on PVA surfaces and the effects of spheroid size on hair follicle regeneration, Biomaterials, 2013, vol. 34, pp. 442–451.

    Article  CAS  PubMed  Google Scholar 

  • Hwang, N.S., Varghese, S., and Elisseeff, J., Cartilage tissue engineering: directed differentiation of embryonic stem cells in three-dimensional hydrogel culture, Meth. Mol. Biol., 2007, vol. 407, pp. 351–373.

    Article  CAS  Google Scholar 

  • Huang, C.F., Chang, Y.J., Hsueh, Y.Y., Huang, C.W., Wang, D.H., Huang, T.C., Wu, Y.T., Su, F.C., Hughes, M., Chuong, C.M., and Wu, C.C., Assembling composite dermal papilla spheres with adipose-derived stem cells to enhance hair follicle induction, Sci. Rep., 2016, vol. 6, p. 26436.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Inoue, K., Kato, H., Sato, T., Osada, A., Aoi, N., Suga, H., Eto, H., Gonda, K., and Yoshimura, K., Evaluation of animal models for the hair-inducing capacity of cultured human dermal papilla cells, Cells Tiss. Organs, 2009, vol. 190, pp. 102–110.

    Article  Google Scholar 

  • Jo, S.J., Choi, S.J., Yoon, S.Y., Lee, J.Y., Park, W.S., Park, P.J., Kim, K.H., Eun, H.C., and Kwon, O., Valproic acid promotes human hair growth in vitro culture model, J. Dermatol. Sci., 2013, vol. 72, pp. 16–24.

    Article  CAS  PubMed  Google Scholar 

  • Katsuoka, K., Schell, H., Wessel, B., and Hornstein, O.P., Effects of epidermal growth factor, fibroblast growth factor, minoxidil and hydrocortisone on growth kinetics in human hair bulb papilla cells and root sheath fibroblasts cultured in vitro, Arch. Dermatol. Res., 1987, vol. 279, pp. 247–250.

    Article  CAS  PubMed  Google Scholar 

  • Lee, S.H., Yoon, J., Shin, S.H., Zahoor, M., Kim, H.J., Park, P.J., Park, W.S., Min, S., Kim, H.Y., and Choi, K.Y., Valproic acid induces hair regeneration in murine model and activates alkaline phosphatase activity in human dermal papilla cells, PLoS One, 2012, vol. 7, p. 34152.

    Article  Google Scholar 

  • Lee, J. and Tumbar, T., Hairy tale of signaling in hair follicle development and cycling, Semin. Cell Dev. Biol., 2012, vol. 23, pp. 906–916.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin, B., Miao, Y., Wang, J., Fan, Z., Du, L., Su, Y., Liu, B., Hu, Z., and Xing, M., Surface tension guided hangingdrop: producing controllable 3D spheroid of high-passaged human dermal papilla cells and forming inductive microtissues for hair-follicle regeneration, ACS Appl. Mater. Interfaces, 2016, vol. 8, pp. 5906–5916.

    Article  CAS  PubMed  Google Scholar 

  • Lorenz, K., Sicker, M., Schmelzer, E., Rupf, T., Salvetter, J., Schulz-Siegmund, M., and Bader, A., Multilineage differentiation potential of human dermal skin-derived fibroblasts, Exp. Dermatol., 2008, vol. 17, pp. 925–932.

    Article  CAS  PubMed  Google Scholar 

  • Malgouries, S., Thibaut, S., and Bernard, B.A., Proteoglycan expression patterns in human hair follicle, Br. J. Dermatol., 2008, vol. 158, pp. 234–242.

    Article  CAS  PubMed  Google Scholar 

  • Ohyama, M., Kobayashi, T., Sasaki, T., Shimizu, A., and Amagai, M., Restoration of the intrinsic properties of human dermal papilla in vitro, J. Cell Sci., 2012, vol. 125, pp. 4114–4125.

    Article  CAS  PubMed  Google Scholar 

  • Paine-Saunders, S., Viviano, B.L., Economides, A.N., and Saunders, S., Heparan sulfate proteoglycans retain noggin at the cell surface: a potential mechanism for shaping bone morphogenetic protein gradients, J. Biol. Chem., 2002, vol. 277, pp. 2089–2096.

    Article  CAS  PubMed  Google Scholar 

  • Rendl, M., Polak, L., and Fuchs, E., BMP signaling in dermal papilla cells is required for their hair follicle-inductive properties, Genes Dev., 2008, vol. 22, pp. 543–557.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rocha-Azevedo, B. and Grinnell, F., Fibroblast morphogenesis on 3D collagen matrices: the balance between cell clustering and cell migration, Exp. Cell Res., 2013, vol. 319, pp. 2440–2446.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ross, F.P. and Christiano, A.M., Nothing but skin and bone, J. Clin. Invest., 2006, vol. 116, pp. 1140–1149.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schneider, M.R., Schmidt-Ullrich, R., and Paus, R., The hair follicle as a dynamic miniorgan, Curr. Biol., 2009, vol. 19, pp. R132–R142.

    Article  CAS  PubMed  Google Scholar 

  • Sennett, R. and Rendl, M., Mesenchymal-epithelial interactions during hair follicle morphogenesis and cycling, Semin. Cell Dev. Biol., 2012, vol. 23, pp. 917–927.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsang, K.Y., Cheung, M.C., Chan, D., and Cheah, K.S., The developmental roles of the extracellular matrix: beyond structure to regulation, Cell Tiss. Res., 2010, vol. 339, pp. 93–110.

    Article  CAS  Google Scholar 

  • Wu, J.J., Liu, R.Q., Lu, Y.G., Zhu, T.Y., Cheng, B., and Men, X., Enzyme digestion to isolate and culture human scalp dermal papilla cells: a more efficient method, Arch. Dermatol. Res., 2005, vol. 297, pp. 60–67.

    Article  PubMed  Google Scholar 

  • Yang, Y., Li, Y., Wang, Y., Wu, J., Yang, G., Yang, T., Gao, Y., and Lu, Y., Versican gene: regulation by the ß-catenin signaling pathway plays a significant role in dermal papilla cell aggregative growth, J. Dermatol. Sci., 2012, vol. 68, pp. 157–163.

    Article  CAS  PubMed  Google Scholar 

  • Yoo, E.J., Chung, J.J., Choe, S.S., Kim, K.H., and Kim, J.B., Down-regulation of histone deacetylases stimulates adipocyte differentiation, J. Biol. Chem., 2006, vol. 281, pp. 6608–6615.

    Article  CAS  PubMed  Google Scholar 

  • Young, T.H., Tu, H.R., Chan, C.C., Huang, Y.C., Yen, M.H., Cheng, N.C., Chiu, H.C., and Lin, S.J., The enhancement of dermal papilla cell aggregation by extracellular matrix proteins through effects on cell-substratum adhesivity and cell motility, Biomaterials, 2009, vol. 30, pp. 5031–5040.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, X., Wang, Y., Gao, Y., Liu, X., Bai, T., Li, M., Li, L., Chi, G., Xu, H., Liu, F., Liu, J.Y., and Li, Y., Maintenance of high proliferation and multipotent potential of human hair follicle-derived mesenchymal stem cells by growth factors, Int. J. Mol. Med., 2013, vol. 31, pp. 913–921.

    CAS  PubMed  Google Scholar 

  • Zhang, H., Nan, W., Wang, S., Zhang, T., Si, H., Wang, D., and Yang, F., Li, Y. epidermal growth factor promotes proliferation of dermal papilla cells via Notch signaling pathway, Biochimie, 2016, vol. S0300, pp. 30068–30072.

    Google Scholar 

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Authors and Affiliations

  1. Koltzov Institute of Developmental Biology, Russian Academy of Sciences, ul. Vavilova 26, Moscow, 119334, Russia

    E. P. Kalabusheva, E. S. Chermnykh, V. V. Terskikh & E. A. Vorotelyak

  2. Pirogov Russian National Research Medical University, Ministry of Health of the Russian Federation, ul. Ostrovityanova 1, Moscow, 117997, Russia

    E. P. Kalabusheva, E. S. Chermnykh & E. A. Vorotelyak

  3. Faculty of Biology, Moscow State University, Moscow, 119234, Russia

    E. A. Vorotelyak

Authors
  1. E. P. Kalabusheva
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  2. E. S. Chermnykh
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  3. V. V. Terskikh
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  4. E. A. Vorotelyak
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Correspondence to E. P. Kalabusheva.

Additional information

Original Russian Text © E.P. Kalabusheva, E.S. Chermnykh, V.V. Terskikh, E.A. Vorotelyak, 2017, published in Izvestiya Akademii Nauk, Seriya Biologicheskaya, 2017, No. 4, pp. 360–369.

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Kalabusheva, E.P., Chermnykh, E.S., Terskikh, V.V. et al. Preservation of a specialized phenotype of dermal papilla cells of a human hair follicle under cultivation conditions. Biol Bull Russ Acad Sci 44, 363–371 (2017). https://doi.org/10.1134/S1062359017040069

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  • DOI: https://doi.org/10.1134/S1062359017040069

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