Skip to main content

Advertisement

SpringerLink
Log in

Dermal papilla cells induce keratinocyte tubulogenesis in culture

  • Original Paper
  • Published:
Histochemistry and Cell Biology Aims and scope Submit manuscript

Abstract

The ability of dermal papilla (DP) cells to induce hair growth was reported in many studies. However, early stages of hair follicle development and signals that govern this process are poorly understood. Therefore, an in vitro model may be a convenient system to study epithelial–mesenchymal interactions and early stages of epidermal morphogenesis, especially in humans. To investigate the role of DP cells in epidermal morphogenesis we modified the method of isolation of DP cells from hair follicle of human scalp and developed the three-dimensional model of epidermal morphogenesis. Isolated DP cells were able to differentiate in adipogenic and osteogenic directions and retained activity of alkaline phosphatase (AP) for seven passages in culture. DP cells were able to induce tubule-like structures in three-dimensional model in vitro and to reorganize collagen matrix. Prolonged cultivation of DP cells has been a big problem because of the loss of hair follicle-inducing ability and growth activity after several passages. To solve this problem we immortalized DP cells by the transfection of the human telomerase reverse transcriptase cDNA (hTERT). Immortalized DP-hTERT cells retained AP activity and demonstrated low ability to osteogenic differentiation. The conditioned medium collected from actively proliferated cells as well as DP-hTERT cells themselves were capable to induce tubulogenesis after prolonged keratinocyte cultivation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Almond-Roesler B, Schon M, Schon MP, Blume-Peytavi U, Sommer C, Loster K, Orfanos CE (1997) Cultured dermal papilla cells of the rat vibrissa follicle. Proliferative activity, adhesion properties and reorganization of the extracellular matrix in vitro. Arch Dermatol Res 289:698–704

    Article  CAS  PubMed  Google Scholar 

  • Arase S, Sadamoto Y, Katoh S (1991) Coculture of human hair follicles and dermal papillae in type I collagen gel. Ann NY Acad Sci 642:454–456

    Article  CAS  PubMed  Google Scholar 

  • Bodnar AG, Ouellette M, Frolkis M, Holt SE, Chiu CP, Morin GB, Harley CB, Shay JW, Lichtsteiner S, Wright WE (1998) Extension of life-span by introduction of telomerase into normal human cells. Science 279(5349):349–352

    Article  CAS  PubMed  Google Scholar 

  • Chermnykh ES, Vorotelyak EA, Tkachenko SB, Vasiliev AV, Terskikh VV (2007) Proliferation of keratin-19+ epidermal keratinocytes in vitro. Dokl Biol Sci 416:555–557

    Article  Google Scholar 

  • Chiu HC, Chang CH, Wu YC (1993) An efficient method for isolation of hair papilla and follicle epithelium from human hair specimens. Br J Dermatol 129:350–351

    Article  CAS  PubMed  Google Scholar 

  • Egorov EE, Terekhov SM, KhS Vishniakova, Karachentsev DN, Kazimirchuk EV, Tsvetkova TG, Veĭko NN, Smirnova TD, Makarenkov AS, El’darov MA, IuA Meshcheriakova, Liapunova NA, Zelenin AV (2003) Telomerization as a method of obtaining immortal human cells preserving normal properties. Ontogenez 34:183–192

    CAS  PubMed  Google Scholar 

  • Egorov EE, Moldaver MV, KhS Vishniakova, Terekhov SM, Dashinimaev EB, Cheglakov IB, IIu Toropygin, Iarygin KN, Chumakov PM, Korochkin LI, Antonova GA, EIu Rybalkina, Saburina IN, Burnaevskiĭ NS, Zelenin AV (2007) Enhanced control of proliferation in telomerized cells. Ontogenez 38:105–119

    CAS  PubMed  Google Scholar 

  • Handjiski BK, Eichmüller S, Hofmann U, Czarnetzki BM, Paus R (1994) Alkaline phosphatase activity and localization during the murine hair cycle. Br J Dermatol 131:303–310

    Article  CAS  PubMed  Google Scholar 

  • Hunt DPJ, Morris PN, Sterling J, Anderson JA, Joannides A, Jahoda C, Compston A, Chandran S (2008) A highly enriched niche of precursor cells with neuronal and glial potential within the hair follicle dermal papilla of adult skin. Stem Cells 26:163–172

    Article  CAS  PubMed  Google Scholar 

  • Iida M, Ihara S, Matsuzaki T (2007) Hair cycle-dependent changes of alkaline phosphatase activity in the mesenchyme and epithelium in mouse vibrissal follicles. Dev Growth Differ 49:185–195

    CAS  PubMed  Google Scholar 

  • Jahoda C, Oliver RF (1981) The growth of vibrissa dermal papilla cells in vitro. Br J Dermatol 105:623–627

    Article  CAS  PubMed  Google Scholar 

  • Jahoda CA, Oliver RF (1984) Vibrissa dermal papilla cell aggregative behaviour in vivo and in vitro. J Embryol Exp Morphol 79:211–224

    CAS  PubMed  Google Scholar 

  • Jahoda CAB, Horne KA, Oliver RF (1984) Induction of hair growth by implantation of cultured dermal cells. Nature 311:560–562

    Article  CAS  PubMed  Google Scholar 

  • Jahoda CA, Whitehouse J, Reynolds AJ, Hole N (2005) Hair follicle dermal cells differentiate into adipogenic and osteogenic lineages. Exp Dermatol 12(6):849–859

    Article  Google Scholar 

  • Kiseleva EV, Chermnykh ES, Vorotelyak EA, Volozhin AI, Vasiliev AV, Terskikh VV (2009) Differentiation capacity of stromal fibroblast-like cells from human bone marrow, adipose tissue, hair follicle dermal papilla and derma. Cell Tissue Biol 3:42–49

    Article  Google Scholar 

  • Kishimoto J, Burgeson RE, Morgan BA (2000) Wnt signaling maintains the hair-inducing activity of the dermal papilla. Genes Dev 14:1181–1185

    CAS  PubMed  Google Scholar 

  • Lako M, Armstrong L, Cairns PM, Harris S, Hole N, Jahoda CA (2002) Hair follicle dermal cells repopulate the mouse haematopoietic system. J Cell Sci 115:3967–3974

    Article  CAS  PubMed  Google Scholar 

  • Lichti U, Weinberg WC, Goodman L, Ledbetter S, Dooley T, Morgan D, Yuspa SH (1993) In vivo regulation of murine hair growth: insights from grafting defined cell population onto nude mice. J Invest Dermatol 101:124S–129S

    Article  CAS  PubMed  Google Scholar 

  • McElwee KJ, Kissling S, Wenzel E, Huth A, Hoffman R (2003) Cultured peribulbar dermal sheath cells can induce hair follicle development and contribute to the dermal sheath and dermal papilla. J Invest Dermatol 121:1267–1275

    Article  CAS  PubMed  Google Scholar 

  • Messenger AG (1984) The culture of dermal papilla cells from human hair follicle. Br J Dermatol 110:685–689

    Article  CAS  PubMed  Google Scholar 

  • Messenger AG, Elliott K, Temple A, Randall VA (1991) Expression of basement membrane proteins and interstitial collagens in dermal papillae of human hair follicles. J Invest Dermatol 96:93–97

    Article  CAS  PubMed  Google Scholar 

  • Muller-Rover S, Handjiski B, van der Veen C, Eichmuller S, Foitzik K, McKay IA, Stenn KS, Paus R (2001) A comprehensive guide for the accurate classification of murine hair follicles in distinct hair cycle stages. J Invest Dermatol 117:3–15

    Article  CAS  PubMed  Google Scholar 

  • Oliver RF (1970) The induction of hair follicle formation in the adult hooded rat by vibrissa dermal papillae. J Embryol Exp Morphol 23:219–236

    CAS  PubMed  Google Scholar 

  • Osada A, Iwabuchi T, Kishimoto J, Hamazaki TS, Okochi H (2007) Long-term culture of mouse vibrissal dermal papilla cells and de novo hair follicle induction. Tissue Eng 13:975–982

    Article  CAS  PubMed  Google Scholar 

  • Pontiggia L, Biedermann T, Meuli M, Widmer D, Bottcher-Haberzeth S, Schiestl C, Schneider J, Braziulis E, Montano I, Meuli-Simmen C, Reichmann E (2009) Markers to evaluate the quality and self-renewing potential of engineered human skin substitutes in vitro and after transplantation. J Invest Dermatol 129(2):480–890

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Schmidt-Ullrich R, Paus R (2005) Molecular principles of hair follicle induction and morphogenesis. Bioessays 27:247–261

    Article  CAS  PubMed  Google Scholar 

  • Shinin VV, Chernaia OG, Terskikh VV (2002) Induction of invasion and epithelial tubulogenesis in primary human keratinocyte culture. Izv Akad Nauk Ser Biol 2:133–141

    PubMed  Google Scholar 

  • Stenn KS, Paus R (2001) Controls of hair follicle cycling. Physiol Rev 81:449–494

    CAS  PubMed  Google Scholar 

  • Vaziri H, Benchimol S (1998) Reconstitution of telomerase activity in normal human cells leads to elongation of telomeres and extended replicative life span. Curr Biol 8(5):279–282

    Article  CAS  PubMed  Google Scholar 

  • Warren R, Chestnut MH, Wong TK, Otte TE, Lanners KM, Meili ML (1992) Improved method for the isolation and cultivation of human scalp dermal papilla cells. J Invest Dermatol 98:693–699

    Article  CAS  PubMed  Google Scholar 

  • Wu JJ, Liu RQ, Lu YG, Zhu TY, Cheng B, Men X (2005) Enzyme digestion to isolate and culture human scalp dermal papilla cells: a more efficient method. Arch Dermatol Res 297:60–67

    Article  PubMed  Google Scholar 

  • Yuspa SH, Wang Q, Weinberg WC, Goodman L, Ledbetter S, Dooley T, Lichti U (1993) Regulation of hair follicle development: an in vitro model for hair follicle invasion of dermis and associated connective tissue remodeling. J Invest Dermatol 101:27S–32S

    Article  CAS  PubMed  Google Scholar 

  • Zuk PA, Zhu M, Mizuno H, Huang J, Futrell JW, Katz AJ, Benhaim P, Lorenz HP, Hedrick MH (2001) Multilineage cells from adipose tissue: implication for cell-based therapies. Tissue Eng 7:211–228

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The work was supported by the Russian Foundation for Basic Research (projects 08-04-00611a and 09-04-01071a).

Author information

Authors and Affiliations

  1. Koltzov Institute of Developmental Biology, Russian Academy of Sciences, Moscow, Russia

    Elina S. Chermnykh, Ekaterina A. Vorotelyak, Ksenia Y. Gnedeva, Andrey V. Vasiliev & Vasily V. Terskikh

  2. Engelhardt Institute of Molecular Biology, Russian Academy of Sciences, Moscow, Russia

    Marianna V. Moldaver & Yegor E. Yegorov

Authors
  1. Elina S. Chermnykh
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ekaterina A. Vorotelyak
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ksenia Y. Gnedeva
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Marianna V. Moldaver
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yegor E. Yegorov
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Andrey V. Vasiliev
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Vasily V. Terskikh
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ekaterina A. Vorotelyak.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chermnykh, E.S., Vorotelyak, E.A., Gnedeva, K.Y. et al. Dermal papilla cells induce keratinocyte tubulogenesis in culture. Histochem Cell Biol 133, 567–576 (2010). https://doi.org/10.1007/s00418-010-0691-0

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00418-010-0691-0

Keywords

Search

Navigation