About this Journal Submit a Manuscript Table of Contents
BioMed Research International
Volume 2013 (2013), Article ID 643601, 21 pages
http://dx.doi.org/10.1155/2013/643601
Review Article

Morphogenetic Mechanisms in the Cyclic Regeneration of Hair Follicles and Deer Antlers from Stem Cells

1AgResearch Invermay Agricultural Centre, Private Bag 50034, Mosgiel 9053, New Zealand
2State Key Laboratory for Molecular Biology of Special Economic Animals, Chinese Academy of Agricultural Sciences, Changchun, Jilin 130112, China
3AgResearch Ruakura Agricultural Centre, Private Bag 3123, Hamilton 3240, New Zealand

Received 14 May 2013; Accepted 1 October 2013

Academic Editor: Andre Van Wijnen

Copyright © 2013 Chunyi Li et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. G. Cotsarelis, “The hair follicle: dying for attention,” The American Journal of Pathology, vol. 151, no. 6, pp. 1505–1509, 1997. View at Scopus
  2. R. J. Goss, Deer Antlers. Regeneration, Function and Evolution, Academic Press, New York, NY, USA, 1983.
  3. M. R. Schneider, R. Schmidt-Ullrich, and R. Paus, “The hair follicle as a dynamic miniorgan,” Current Biology, vol. 19, no. 3, pp. R132–R142, 2009. View at Publisher · View at Google Scholar · View at Scopus
  4. G. Cotsarelis, T.-T. Sun, and R. M. Lavker, “Label-retaining cells reside in the bulge area of pilosebaceous unit: implications for follicular stem cells, hair cycle, and skin carcinogenesis,” Cell, vol. 61, no. 7, pp. 1329–1337, 1990. View at Publisher · View at Google Scholar · View at Scopus
  5. R. Paus, S. Müller-Röver, C. Van Der Veen et al., “A comprehensive guide for the recognition and classification of distinct stages of hair follicle morphogenesis,” Journal of Investigative Dermatology, vol. 113, no. 4, pp. 523–532, 1999. View at Publisher · View at Google Scholar · View at Scopus
  6. C. Niemann and F. M. Watt, “Designer skin: lineage commitment in postnatal epidermis,” Trends in Cell Biology, vol. 12, no. 4, pp. 185–192, 2002. View at Publisher · View at Google Scholar · View at Scopus
  7. C. A. B. Jahoda and A. J. Reynolds, “Hair follicle dermal sheath cells: unsung participants in wound healing,” The Lancet, vol. 358, no. 9291, pp. 1445–1448, 2001. View at Publisher · View at Google Scholar · View at Scopus
  8. H. Kierdorf, U. Kierdorf, T. Szuwart, U. Gath, and G. Clemen, “Light microscopic observations on the ossification process in the early developing pedicle of fallow deer (Dama dama),” Annals of Anatomy, vol. 176, no. 3, pp. 243–249, 1994. View at Scopus
  9. C. Li and J. M. Suttie, “Light microscopic studies of pedicle and early first antler development in red deer (Cervus elaphus),” Anatomical Record, vol. 239, no. 2, pp. 198–215, 1994. View at Publisher · View at Google Scholar · View at Scopus
  10. C. Li, C. G. Mackintosh, S. K. Martin, and D. E. Clark, “Identification of key tissue type for antler regeneration through pedicle periosteum deletion,” Cell and Tissue Research, vol. 328, no. 1, pp. 65–75, 2007. View at Publisher · View at Google Scholar · View at Scopus
  11. W. J. Banks and J. W. Newbrey, “Light microscopic studies of the ossification process in developing antlers,” in Antler Development in Cervidae, pp. 231–260, 1982.
  12. C. Li, D. E. Clark, E. A. Lord, J.-A. L. Stanton, and J. M. Suttie, “Sampling technique to discriminate the different tissue layers of growing antler tips for gene discovery,” Anatomical Record, vol. 268, no. 2, pp. 125–130, 2002. View at Publisher · View at Google Scholar · View at Scopus
  13. G. B. Wislocki, “Studies on the growth of deer antlers. I. On the structure and histogenesis of the antlers of the Virginia deer (Odocoileus virginianus borealis),” American Journal of Anatomy, vol. 71, pp. 371–451, 1942.
  14. C. Blanpain and E. Fuchs, “Epidermal stem cells of the skin,” Annual Review of Cell and Developmental Biology, vol. 22, pp. 339–373, 2006. View at Publisher · View at Google Scholar · View at Scopus
  15. C. Li, R. P. Littlejohn, I. D. Corson, and J. M. Suttie, “Effects of testosterone on pedicle formation and its transformation to antler in castrated male, freemartin and normal female red deer (Cervus elaphus),” General and Comparative Endocrinology, vol. 131, no. 1, pp. 21–31, 2003. View at Publisher · View at Google Scholar · View at Scopus
  16. J. M. Suttie, P. F. Fennessy, I. D. Corson, B. A. Veenvliet, R. P. Littlejohn, and K. R. Lapwood, “Seasonal pattern of luteinizing hormone and testosterone pulsatile secretion in young adult red deer stags (Cervus elaphus) and its association with the antler cycle,” Journal of Reproduction and Fertility, vol. 95, no. 3, pp. 925–933, 1992. View at Scopus
  17. C. Li and J. Suttie, “Histological studies of pedicle skin formation and its transformation to antler velvet in red deer (Cervus elaphus),” The Anatomical Record, vol. 260, pp. 62–71, 2000.
  18. H. Oshima, A. Rochat, C. Kedzia, K. Kobayashi, and Y. Barrandon, “Morphogenesis and renewal of hair follicles from adult multipotent stem cells,” Cell, vol. 104, no. 2, pp. 233–245, 2001. View at Publisher · View at Google Scholar · View at Scopus
  19. C. Li and J. M. Suttie, “Deer antlerogenic periosteum: a piece of postnatally retained embryonic tissue?” Anatomy and Embryology, vol. 204, no. 5, pp. 375–388, 2001. View at Publisher · View at Google Scholar · View at Scopus
  20. V. Greco and S. Guo, “Compartmentalized organization: a common and required feature of stem cell niches?” Development, vol. 137, no. 10, pp. 1586–1594, 2010.
  21. A. J. Reynolds and C. A. B. Jahoda, “Cultured dermal papilla cells induce follicle formation and hair growth by transdifferentiation of an adult epidermis,” Development, vol. 115, no. 2, pp. 587–593, 1992. View at Scopus
  22. C. Li, F. Yang, X. Xing et al., “Role of heterotypic tissue interactions in deer pedicle and first antler formation—revealed via a membrane insertion approach,” Journal of Experimental Zoology Part B, vol. 310, no. 3, pp. 267–277, 2008. View at Publisher · View at Google Scholar · View at Scopus
  23. W. Montagna, H. B. Chase, and H. P. Melaragno, “The skin of hairless mice. I. The formation of cysts and the distribution of lipids,” The Journal of Investigative Dermatology, vol. 19, no. 1, pp. 83–94, 1952. View at Publisher · View at Google Scholar
  24. K. Kobayashi, A. Rochat, and Y. Barrandon, “Segregation of keratinocyte colony-forming cells in the bulge of the rat vibrissa,” Proceedings of the National Academy of Sciences of the United States of America, vol. 90, no. 15, pp. 7391–7395, 1993. View at Scopus
  25. C. Li, J. M. Suttie, and D. E. Clark, “Morphological observation of antler regeneration in red deer (Cervus elaphus),” Journal of Morphology, vol. 262, no. 3, pp. 731–740, 2004. View at Publisher · View at Google Scholar · View at Scopus
  26. C. Li, X. Gao, F. Yang et al., “Development of a nude mouse model for the study of antlerogenesis-mechanism of tissue interactions and ossification pathway,” Journal of Experimental Zoology Part B, vol. 312, no. 2, pp. 118–135, 2009. View at Publisher · View at Google Scholar · View at Scopus
  27. A. M. Kligman, “Pathologic dynamics of human hair loss. I. Telogen effuvium,” Archives of Dermatology, vol. 83, pp. 175–198, 1961. View at Scopus
  28. Y. Milner, J. Sudnik, M. Filippi, M. Kizoulis, M. Kashgarian, and K. Stenn, “Exogen, shedding phase of the hair growth cycle: characterization of a mouse model,” Journal of Investigative Dermatology, vol. 119, no. 3, pp. 639–644, 2002. View at Publisher · View at Google Scholar · View at Scopus
  29. S. Müller-Röver, B. Handjiski, C. Van Der Veen et al., “A comprehensive guide for the accurate classification of murine hair follicles in distinct hair cycle stages,” Journal of Investigative Dermatology, vol. 117, no. 1, pp. 3–15, 2001. View at Publisher · View at Google Scholar · View at Scopus
  30. E. J. Vanscott, T. M. Ekel, and R. Auerbach, “Determinants of rate and kinetics of cell division in scalp hair,” The Journal of Investigative Dermatology, vol. 41, pp. 269–273, 1963. View at Scopus
  31. U. Kierdorf, E. Stoffels, D. Stoffels, H. Kierdorf, T. Szuwart, and G. Clemen, “Histological studies of bone formation during pedicle restoration and early antler regeneration in roe deer and fallow deer,” Anatomical Record A, vol. 273, no. 2, pp. 741–751, 2003. View at Scopus
  32. C. Li, J. M. Suttie, and D. E. Clark, “Histological examination of antler regeneration in red deer (Cervus elaphus),” Anatomical Record A, vol. 282, no. 2, pp. 163–174, 2005. View at Publisher · View at Google Scholar · View at Scopus
  33. J. M. Suttie, G. A. Lincoln, and R. N. B. Kay, “Endocrine control of antler growth in red deer stags,” Journal of Reproduction and Fertility, vol. 71, no. 1, pp. 7–15, 1984. View at Scopus
  34. P. F. Fennessy and J. M. Suttie, “Antler growth: nutritional and endocrine factors,” in Biology of Deer Production, P. F. Fennessy and K. R. Drew, Eds., pp. 239–250, Royal Society of New Zealand, Wellington, New Zealand, 1985.
  35. T. Abbas-Terki, W. Blanco-Bose, N. Déglon, W. Pralong, and P. Aebischer, “Lentiviral-mediated RNA interference,” Human Gene Therapy, vol. 13, no. 18, pp. 2197–2201, 2002. View at Publisher · View at Google Scholar · View at Scopus
  36. R. F. Oliver, “Whisker growth after removal of the dermal papilla and lengths of follicle in the hooded rat,” Journal of Embryology and Experimental Morphology, vol. 15, no. 3, pp. 331–347, 1966. View at Scopus
  37. C. Blanpain, W. E. Lowry, A. Geoghegan, L. Polak, and E. Fuchs, “Self-renewal, multipotency, and the existence of two cell populations within an epithelial stem cell niche,” Cell, vol. 118, no. 5, pp. 635–648, 2004. View at Publisher · View at Google Scholar · View at Scopus
  38. S. Claudinot, M. Nicolas, H. Oshima, A. Rochat, and Y. Barrandon, “Long-term renewal of hair follicles from clonogenic multipotent stem cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 41, pp. 14677–14682, 2005. View at Publisher · View at Google Scholar · View at Scopus
  39. Y. Sasahara, Y. Yoshikawa, T. Morinaga et al., “Human keratinocytes derived from the bulge region of hair follicles are refractory to differentiation,” International Journal of Oncology, vol. 34, no. 5, pp. 1191–1199, 2009. View at Publisher · View at Google Scholar · View at Scopus
  40. H. Yu, D. Fang, S. M. Kumar et al., “Isolation of a novel population of multipotent adult stem cells from human hair follicles,” American Journal of Pathology, vol. 168, no. 6, pp. 1879–1888, 2006. View at Publisher · View at Google Scholar · View at Scopus
  41. J. A. Nowak, L. Polak, H. A. Pasolli, and E. Fuchs, “Hair follicle stem cells are specified and function in early skin morphogenesis,” Cell Stem Cell, vol. 3, no. 1, pp. 33–43, 2008. View at Publisher · View at Google Scholar · View at Scopus
  42. R. J. Goss and R. S. Powel, “Induction of deer antlers by transplanted periosteum I. Graft size and shape,” Journal of Experimental Zoology, vol. 235, no. 3, pp. 359–373, 1985. View at Scopus
  43. C. Li, “Development of deer antler model for biomedical research,” Advances and Research Updates, vol. 4, pp. 256–274, 2003.
  44. H. Hartwig and J. Schrudde, “Experimentelle Untersuchungen zur Bildung der primären Stirnauswüchse beim Reh (Capreolus capreolus L.),” Zeitschrift für Jagdwissenschaft, vol. 20, no. 1, pp. 1–13, 1974. View at Publisher · View at Google Scholar · View at Scopus
  45. C. Li, F. Yang, and A. Sheppard, “Adult stem cells and mammalian epimorphic regeneration-insights from studying annual renewal of deer antlers,” Current Stem Cell Research and Therapy, vol. 4, no. 3, pp. 237–251, 2009. View at Scopus
  46. R. J. Goss, “Induction of deer antlers by transplanted periosteum. II. Regional competence for velvet transformation in ectopic skin,” Journal of Experimental Zoology, vol. 244, pp. 101–111, 1987.
  47. C. Li, F. Yang, S. Haines et al., “Stem cells responsible for deer antler regeneration are unable to recapitulate the process of first antler development-revealed through intradermal and subcutaneous tissue transplantation,” Journal of Experimental Zoology Part B, vol. 314, no. 7, pp. 552–570, 2010. View at Publisher · View at Google Scholar · View at Scopus
  48. C. Li, A. Harper, J. Puddick, W. Wang, and C. McMahon, “Proteomes and signalling pathways of antler stem cells,” PLoS ONE, vol. 7, no. 1, Article ID e30026, 2012. View at Publisher · View at Google Scholar · View at Scopus
  49. D. Gancz, T. Lengil, and L. Gilboa, “Coordinated regulation of niche and stem cell precursors by hormonal signaling,” PLoS Biology, vol. 9, no. 11, Article ID e1001202, 2011. View at Publisher · View at Google Scholar · View at Scopus
  50. J. M. Suttie, P. F. Fennessy, K. R. Lapwood, and I. D. Corson, “Role of steroids in antler growth of red deer stags,” Journal of Experimental Zoology, vol. 271, no. 2, pp. 120–130, 1995. View at Scopus
  51. R. J. Goss, “Of antlers and embryos,” in Horns, Pronghorns, and Antlers, G. Bubenik and A. Bubenik, Eds., pp. 299–312, Springer, New York, NY, USA, 1990.
  52. C. Li, “Exploration of the mechanism underlying neogenesis and regeneration of postnatal mammalian skin—deer antler velvet,” in International Journal of Medical and Biological Frontiers, vol. 16, pp. 1–19, 2010.
  53. R. F. Oliver, “The experimental induction of whisker growth in the hooded rat by implantation of dermal papillae,” Journal of Embryology and Experimental Morphology, vol. 18, no. 1, pp. 43–51, 1967. View at Scopus
  54. F. Yang, W. Wang, J. Li, S. Haines, G. Asher, and C. Li, “Antler development was inhibited or stimulated by cryosurgery to periosteum or skin in a central antlerogenic region respectively,” Journal of Experimental Zoology Part B, vol. 316, no. 5, pp. 359–370, 2011. View at Publisher · View at Google Scholar · View at Scopus
  55. C. A. B. Jahoda, R. F. Oliver, A. J. Reynolds et al., “Trans-species hair growth induction by human hair follicle dermal papillae,” Experimental Dermatology, vol. 10, no. 4, pp. 229–237, 2001. View at Publisher · View at Google Scholar · View at Scopus
  56. C. Li, F. Yang, G. Li et al., “Antler regeneration: a dependent process of stem tissue primed via interaction with its enveloping skin,” Journal of Experimental Zoology Part A, vol. 307, no. 2, pp. 95–105, 2007. View at Publisher · View at Google Scholar · View at Scopus
  57. H. B. Chase, “Growth of the hair,” Physiological Reviews, vol. 34, no. 1, pp. 113–126, 1954. View at Scopus
  58. W. Montagna, H. B. Chase, and W. C. Lobitz Jr., “Histology and cytochemistry of human skin. II. The distribution of glycogen in the epidermis, hair follicles, sebaceous glands and eccrine sweat glands,” The Anatomical Record, vol. 114, no. 2, pp. 231–247, 1952. View at Scopus
  59. G. B. Wislocki, “Antlers in female deer, with a report of three cases in Odocoileus,” Journal of Mammalogy, vol. 35, pp. 486–495, 1954.
  60. Z. Jaczewski, The Artificial Induction of Antler Growth in Deer, 1982.
  61. U. Kierdorf, H. Kierdorf, and S. Knuth, “Effects of castration on antler growth in fallow deer (Dama dama L.),” Journal of Experimental Zoology, vol. 273, no. 1, pp. 33–43, 1995. View at Scopus
  62. J. R. Couchman and W. T. Gibson, “Expression of basement membrane components through morphological changes in the hair growth cycle,” Developmental Biology, vol. 108, no. 2, pp. 290–298, 1985. View at Scopus
  63. V. Puccinelli, R. Caputo, and B. Ceccarelli, “Changes in the basement membrane of the papilla and wall of the human hair follicle,” Archiv fur Klinische und Experimentelle Dermatologie, vol. 233, no. 2, pp. 172–183, 1968. View at Publisher · View at Google Scholar · View at Scopus
  64. V. A. Randall, “Androgens and hair growth,” Dermatology and Therapy, vol. 21, pp. 314–328, 2008.
  65. R. J. Goss, “Future directions in antler research,” Anatomical Record, vol. 241, no. 3, pp. 291–302, 1995. View at Publisher · View at Google Scholar · View at Scopus
  66. R. M. Lavker, S. Miller, C. Wilson et al., “Hair follicle stem cells: their location, role in hair cycle, and involvement in skin tumor formation,” Journal of Investigative Dermatology, vol. 101, no. 1, supplement, pp. 16S–26S, 1993. View at Scopus
  67. R. E. Link, R. Paus, K. S. Stenn, E. Kuklinska, and G. Moellmann, “Epithelial growth by rat vibrissae follicles in vitro requires mesenchymal contact via native extracellular matrix,” Journal of Investigative Dermatology, vol. 95, no. 2, pp. 202–207, 1990. View at Scopus
  68. A. J. Craven, A. J. Nixon, M. G. Ashby et al., “Prolactin delays hair regrowth in mice,” Journal of Endocrinology, vol. 191, no. 2, pp. 415–425, 2006. View at Publisher · View at Google Scholar · View at Scopus
  69. G. B. Wislocki, J. C. Aub, and C. M. Waldo, “The effects of gonadectomy and the administration of testosterone propionate on the growth of antlers in male and female deer,” Endocrinology, vol. 40, pp. 202–224, 1947.
  70. L. Martinet, D. Allain, and C. Weiner, “Role of prolactin in the photoperiodic control of moulting in the mink (Mustela vison),” Journal of Endocrinology, vol. 103, no. 1, pp. 9–15, 1984. View at Scopus
  71. R. Goss, “Control of deer antler cycles by the photoperiod,” in Antler Development in Cervidae, pp. 1–13, 1982.
  72. F. J. G. Ebling, “The hair cycle and its regulation,” Clinics in Dermatology, vol. 6, no. 4, pp. 67–73, 1988. View at Scopus
  73. G. A. Lincoln, H. M. Fraser, and T. J. Fletcher, “Induction of early rutting in male red deer (Cervus elaphus) by melatonin and its dependence on LHRH,” Journal of Reproduction and Fertility, vol. 72, no. 2, pp. 339–343, 1984. View at Scopus
  74. J. M. Suttie, B. H. Breier, P. D. Gluckman, R. P. LittleJohn, and J. R. Webster, “Effects of melatonin implants on insulin-like growth factor 1 in male red deer (Cervus elaphus),” General and Comparative Endocrinology, vol. 87, no. 1, pp. 111–119, 1992. View at Publisher · View at Google Scholar · View at Scopus
  75. V. A. Randall, M. J. Thornton, K. Hamada, and A. G. Messenger, “Androgen action in cultured dermal papilla cells from human hair follicles,” Skin Pharmacology, vol. 7, no. 1-2, pp. 20–26, 1994. View at Scopus
  76. J. M. Suttie, P. F. Fennessy, S. F. Crosbie et al., “Temporal changes in LH and testosterone and their relationship with the first antler in red deer (Cervus elaphus) stags from 3 to 15 months of age,” Journal of Endocrinology, vol. 131, no. 3, pp. 467–474, 1991. View at Scopus
  77. D. I. Chapman, “Antlers-bones of contention,” Mammal Review, vol. 5, pp. 121–172, 1975.
  78. M. Chieffi, “Effect of testosterone administration on the beard growth of elderly males,” Journals of Gerontology, vol. 4, pp. 200–204, 1949.
  79. J. Griffin and J. Wilson, “The resistance syndromes: 5a-reductase deficiency, testicular feminisation and related disorders,” in The Metabolic Basis of Inherited Disease, C. R. Scriver, A. Baudct, W. Sly, and D. Valle, Eds., pp. 1919–1944, McGraw-Hill, New York, NY, USA, 1989.
  80. V. A. Randall, M. J. Thornton, K. Hamada et al., “Androgens and the hair follicle: cultured human dermal papilla cells as a model system,” Annals of the New York Academy of Sciences, vol. 642, pp. 355–375, 1991. View at Scopus
  81. J. B. Hamilton, H. Terada, and G. E. Mestler, “Studies of growth throughout the life span in Japanese. II. Beard growth in relation to age, sex, heredity, and other factors,” Journal of Gerontology, vol. 13, no. 3, pp. 269–281, 1958. View at Scopus
  82. S. V. Seago and F. J. G. Ebling, “The hair cycle on the human thigh and upper arm,” British Journal of Dermatology, vol. 113, no. 1, pp. 9–16, 1985. View at Scopus
  83. G. A. Lincoln, F. Guinness, and R. V. Short, “The way in which testosterone controls the social and sexual behavior of the red deer stag (Cervus elaphus),” Hormones and Behavior, vol. 3, no. 4, pp. 375–396, 1972. View at Scopus
  84. G. A. Lincoln, “The seasonal reproductive changes in the red deer stag (Cervus elaphus),” Journal of Zoology, vol. 163, pp. 105–123, 1971.
  85. G. A. Bubenik, “Endocrine regulation of the antler cycle,” in Antler Development in Cervidae, pp. 73–107, 1982.
  86. K. Elliott, T. J. Stephenson, and A. G. Messenger, “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,” Journal of Investigative Dermatology, vol. 113, no. 6, pp. 873–877, 1999. View at Publisher · View at Google Scholar · View at Scopus
  87. M. J. Thornton, N. A. Hibberts, T. Street, B. R. Brinklow, A. I. Loudon, and V. A. Randall, “Androgen receptors are only present in mesenchyme-derived dermal papilla cells of red deer (Cervus elaphus) neck follicles when raised androgens induce a mane in the breeding season,” Journal of Endocrinology, vol. 168, no. 3, pp. 401–408, 2001. View at Publisher · View at Google Scholar · View at Scopus
  88. C. Li, S. Zhao, and J. Song, “Cytosol testosterone receptor in antler tissue of sika deer: an assay based on isoelectric focusing in polyacrylamide gel,” Chinese Journal of Zoology, vol. 22, pp. 23–25, 1987.
  89. C. Li, W. Wang, T. Manley, and J. M. Suttie, “No direct mitogenic effect of sex hormones on antlerogenic cells detected in vitro,” General and Comparative Endocrinology, vol. 124, no. 1, pp. 75–81, 2001. View at Publisher · View at Google Scholar · View at Scopus
  90. V. A. Randall, M. J. Thornton, A. G. Messenger, N. A. Hibberts, A. S. I. Loudon, and B. R. Brinklow, “Hormones and hair growth: variations in androgen receptor content of dermal papilla cells cultured from human and red deer (Cervus elaphus) hair follicles,” Journal of Investigative Dermatology, vol. 101, no. 1, supplement, pp. 114S–120S, 1993. View at Scopus
  91. C. Li, R. P. Littlejohn, and J. M. Suttie, “Effects of insulin-like growth factor 1 and testosterone on the proliferation of antlerogenic cells in vitro,” Journal of Experimental Zoology, vol. 284, pp. 82–90, 1999.
  92. M. P. Philpott, D. A. Sanders, and T. Kealey, “Effects of insulin and insulin-like growth factors on cultured human hair follicles: IGF-I at physiologic concentrations is an important regulator of hair follicle growth in vitro,” Journal of Investigative Dermatology, vol. 102, no. 6, pp. 857–861, 1994. View at Scopus
  93. V. A. Randall, N. A. Hibberts, M. J. Thornton et al., “Do androgens influence hair growth by altering the paracrine factors secreted by dermal papilla cells?” European Journal of Dermatology, vol. 11, no. 4, pp. 315–320, 2001. View at Scopus
  94. N. Oshimori and E. Fuchs, “Paracrine TGF-β signaling counterbalances BMP-mediated repression in hair follicle stem cell activation,” Cell Stem Cell, vol. 10, no. 1, pp. 63–75, 2012. View at Publisher · View at Google Scholar · View at Scopus
  95. T. Andl, S. T. Reddy, T. Gaddapara, and S. E. Millar, “WNT signals are required for the initiation of hair follicle development,” Developmental Cell, vol. 2, no. 5, pp. 643–653, 2002. View at Publisher · View at Google Scholar · View at Scopus
  96. J. Huelsken, R. Vogel, B. Erdmann, G. Cotsarelis, and W. Birchmeier, “β-Catenin controls hair follicle morphogenesis and stem cell differentiation in the skin,” Cell, vol. 105, no. 4, pp. 533–545, 2001. View at Publisher · View at Google Scholar · View at Scopus
  97. K. Närhi, E. Järvinen, W. Birchmeier, M. M. Taketo, M. L. Mikkola, and I. Thesleff, “Sustained epithelial β-catenin activity induces precocious hair development but disrupts hair follicle down-growth and hair shaft formation,” Development, vol. 135, no. 6, pp. 1019–1028, 2008. View at Publisher · View at Google Scholar · View at Scopus
  98. Y. Zhang, T. Andl, S. H. Yang et al., “Activation of β-catenin signaling programs embryonic epidermis to hair follicle fate,” Development, vol. 135, no. 12, pp. 2161–2172, 2008. View at Publisher · View at Google Scholar · View at Scopus
  99. J. G. Mount, M. Muzylak, S. Allen, T. Althnaian, I. M. McGonnell, and J. S. Price, “Evidence that the canonical Wnt signalling pathway regulates deer antler regeneration,” Developmental Dynamics, vol. 235, no. 5, pp. 1390–1399, 2006. View at Publisher · View at Google Scholar · View at Scopus
  100. C. Chiang, R. Z. Swan, M. Grachtchouk et al., “Essential role for Sonic hedgehog during hair follicle morphogenesis,” Developmental Biology, vol. 205, no. 1, pp. 1–9, 1999. View at Publisher · View at Google Scholar · View at Scopus
  101. M. Ashery, “FGF8 in deer antler,” “Physiology”, 1999.
  102. A. de Alwis, J. L. Stanton, J. Gray, J. M. Suttie, and A. J. Harris, “Androgen-induced growth factor expression in deer antlers,” Proceedings of the University of Otago Medical School, vol. 74, no. 3, p. 34, 1996.
  103. N. A. Hibberts, A. G. Messenger, and V. A. Randall, “Dermal papilla cells derived from beard hair follicles secrete more stem cell factor (SCF) in culture than scalp cells or dermal fibroblasts,” Biochemical and Biophysical Research Communications, vol. 222, no. 2, pp. 401–405, 1996. View at Publisher · View at Google Scholar · View at Scopus
  104. S. Lachgar, H. Moukadiri, F. Jonca et al., “Vascular endothelial growth factor is an autocrine growth factor for hair dermal papilla cells,” Journal of Investigative Dermatology, vol. 106, no. 1, pp. 17–23, 1996. View at Scopus
  105. D. E. Clark, E. A. Lord, and J. M. Suttie, “Expression of VEGF and pleiotrophin in deer antler,” Anatomical Record A, vol. 288, no. 12, pp. 1281–1293, 2006. View at Publisher · View at Google Scholar · View at Scopus
  106. F. M. Watt, M. Frye, and S. A. Benitah, “MYC in mammalian epidermis: how can an oncogene stimulate differentiation?” Nature Reviews Cancer, vol. 8, no. 3, pp. 234–242, 2008. View at Publisher · View at Google Scholar · View at Scopus
  107. M. Ito and K. Kizawa, “Expression of calcium-binding S100 proteins A4 and A6 in regions of the epithelial sac associated with the onset of hair follicle regeneration,” Journal of Investigative Dermatology, vol. 116, no. 6, pp. 956–963, 2001. View at Publisher · View at Google Scholar · View at Scopus
  108. G. Bubenik and A. Bubenik, “Horns, Pronghorns, and Antlers,” 1990.
  109. U. Kierdorf, C. Li, and J. S. Price, “Improbable appendages: deer antler renewal as a unique case of mammalian regeneration,” Seminars in Cell and Developmental Biology, vol. 20, no. 5, pp. 535–542, 2009. View at Publisher · View at Google Scholar · View at Scopus
  110. J. L. Woods, D. P. Harland, J. A. Vernon, G. L. Krsinic, and R. J. Walls, “Morphology and ultrastructure of antler velvet hair and body hair from red deer (Cervus elaphus),” Journal of Morphology, vol. 272, no. 1, pp. 34–49, 2011. View at Publisher · View at Google Scholar · View at Scopus
  111. C. Li, A. John Harris, and J. M. Suttie, “Tissue interactions and antlerogenesis: new findings revealed by a xenograft approach,” Journal of Experimental Zoology, vol. 290, no. 1, pp. 18–30, 2001. View at Publisher · View at Google Scholar · View at Scopus
  112. G. Cotsarelis, “Epithelial stem cells: a folliculocentric view,” Journal of Investigative Dermatology, vol. 126, no. 7, pp. 1459–1468, 2006. View at Publisher · View at Google Scholar · View at Scopus
  113. R. Paus and K. Foitzik, “In search of the “hair cycle clock”: a guided tour,” Differentiation, vol. 72, no. 9-10, pp. 489–511, 2004. View at Publisher · View at Google Scholar · View at Scopus
  114. M. Rendl, L. Lewis, and E. Fuchs, “Molecular dissection of mesenchymal-epithelial interactions in the hair follicle,” PLoS Biology, vol. 3, no. 11, article e331, 2005. View at Scopus
  115. K. S. Stenn and R. Paus, “Controls of hair follicle cycling,” Physiological Reviews, vol. 81, no. 1, pp. 449–494, 2001. View at Scopus
  116. Y.-C. Hsu, H. A. Pasolli, and E. Fuchs, “Dynamics between stem cells, niche, and progeny in the hair follicle,” Cell, vol. 144, no. 1, pp. 92–105, 2011. View at Publisher · View at Google Scholar · View at Scopus
  117. P. A. Sotiropoulou, A. Candi, G. Mascré et al., “Bcl-2 and accelerated DNA repair mediates resistance of hair follicle bulge stem cells to DNA-damage-induced cell death,” Nature Cell Biology, vol. 12, no. 6, pp. 572–582, 2010. View at Publisher · View at Google Scholar · View at Scopus
  118. M. Colitti, S. P. Allen, and J. S. Price, “Programmed cell death in the regenerating deer antler,” Journal of Anatomy, vol. 207, no. 4, pp. 339–351, 2005. View at Publisher · View at Google Scholar · View at Scopus
  119. M. V. Plikus, J. A. Mayer, D. De La Cruz et al., “Cyclic dermal BMP signalling regulates stem cell activation during hair regeneration,” Nature, vol. 451, no. 7176, pp. 340–344, 2008. View at Publisher · View at Google Scholar · View at Scopus
  120. M. R. Schneider, S. Werner, R. Paus, and E. Wolf, “Beyond wavy hairs: the epidermal growth factor receptor and its ligands in skin biology and pathology,” American Journal of Pathology, vol. 173, no. 1, pp. 14–24, 2008. View at Publisher · View at Google Scholar · View at Scopus
  121. B. N. Nagorcka and J. R. Mooney, “The role of a reaction-diffusion system in the initiation of primary hair follicles,” Journal of Theoretical Biology, vol. 114, no. 2, pp. 243–272, 1985. View at Scopus
  122. R. E. Billingham, R. Mangold, and W. K. Silvers, “The neogenesis of skin in the antlers of deer,” Annals of the New York Academy of Sciences, vol. 83, pp. 491–498, 1959. View at Scopus
  123. G. A. Bubenik, “Morphological differences in the antler velvet of cervidae,” Deer of China, pp. 56–64, 1993.
  124. D. Frances and C. Niemann, “Stem cell dynamics in sebaceous gland morphogenesis in mouse skin,” Developmental Biology, vol. 363, no. 1, pp. 138–146, 2012. View at Publisher · View at Google Scholar · View at Scopus