Register      Login
Animal Production Science Animal Production Science Society
Food, fibre and pharmaceuticals from animals
REVIEW

Stem cells, stem cell niche and antler development

Chunyi Li A C , Fuhe Yang B and Jimmy Suttie A
+ Author Affiliations
- Author Affiliations

A AgResearch Invermay Agricultural Centre, Private Bag 50034, Mosgiel, New Zealand.

B Institute of Wild Economic Animals and Plants, Chinese Academy of Agricultural Sciences, Jilin City, Jilin Province, China.

C Corresponding author. Email: chunyi.li@agresearch.co.nz

Animal Production Science 51(4) 267-276 https://doi.org/10.1071/AN10157
Submitted: 25 August 2010  Accepted: 18 November 2010   Published: 8 April 2011

Abstract

Annual full regeneration of deer antlers has been proved to be a stem cell-based process, and antler stem cells (ASC) reside in both antlerogenic periosteum (AP) and pedicle periosteum (PP). In this review, we first put forward a hypothesis that the closely associated skin is the primary component of ASC niche and then provide results testing this hypothesis. Membrane insertion experiments confirmed that interactions between ASC and the associated skin are indispensible for both antler generation and regeneration, and these are achieved through exchanging diffusible molecules. Intradermal AP transplantation study demonstrated that both epidermal and dermal papilla cells are involved in these interactions. Further, the AP inversion experiment indicated that the initial inductive signal originates from the ASC resident in the AP cellular layer, although the AP fibrous layer is naturally adjacent to skin. Experimental manipulation to the niche has profound effects on antler development. We believe that eventual identification of these interactive molecules will not only greatly enhance our knowledge of antler development, but also have significant impacts on regenerative medicine in general.

Additional keyword: pedicle.


References

[1]  Stocum D. Regenerative biology and medicine. New York: Academic Press; 2006.

[2]  Goss RJ. Deer antlers. Regeneration, function and evolution. New York: Academic Press; 1983.

[3]  Li C. Development of deer antler model for biomedical research. Rec Adv Res Updates 2003; 4 256–74.

[4]  Hartwig H, Schrudde J. Experimentelle untersuchungen zur bildung der primaren stirnauswuchse beim Reh (Capreolus capreolus L.). Z Jagdwiss 1974; 20 1–13.
Experimentelle untersuchungen zur bildung der primaren stirnauswuchse beim Reh (Capreolus capreolus L.).Crossref | GoogleScholarGoogle Scholar |

[5]  Goss RJ, Powel RS. Induction of deer antlers by transplanted periosteum. I. Graft size and shape. J Exp Zool 1985; 235 359–73.
Induction of deer antlers by transplanted periosteum. I. Graft size and shape.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL28%2Fjs1SgsA%3D%3D&md5=e78c62f293dec7c4efb47f202345f58cCAS | 4056697PubMed |

[6]  Goss RJ. Of antlers and embryos. In Bubenik G, Bubenik A, editors. Horns, pronghorns, and antlers. New York: Springer-Verlag; 1990. pp. 299–312.

[7]  Li C, Littlejohn RP, Suttie JM. Effects of insulin-like growth factor 1 and testosterone on the proliferation of antlerogenic cells in vitro. J Exp Zool 1999; 284 82–90.
Effects of insulin-like growth factor 1 and testosterone on the proliferation of antlerogenic cells in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjvFKhu78%3D&md5=7514c1809d4e64c94de8bfa6b498bba9CAS | 10368936PubMed |

[8]  Goss RJ. Future directions in antler research. Anat Rec 1995; 241 291–302.
Future directions in antler research.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2M3nsVyjtQ%3D%3D&md5=f8c5dcf0012309bfa54690b04978985fCAS | 7755168PubMed |

[9]  Wislocki GB. Studies on the growth of deer antlers. I. On the structure and histogenesis of the antlers of the Virginia deer (Odocoileus virginianus borealis). Am J Anat 1942; 71 371–415.
Studies on the growth of deer antlers. I. On the structure and histogenesis of the antlers of the Virginia deer (Odocoileus virginianus borealis).Crossref | GoogleScholarGoogle Scholar |

[10]  Kierdorf H, Kierdorf U. State of determination of the antlerogenic tissues with special reference to double-head formation. In Brown R, editor. The biology of deer. New York: Springer-Verlag; 1992. pp. 525–31.

[11]  Kierdorf U, Stoffels E, Stoffels D, Kierdorf H, Szuwart T, Clemen G. Histological studies of bone formation during pedicle restoration and early antler regeneration in roe deer and fallow deer. Anat Rec 2003; 273A 741–51.
Histological studies of bone formation during pedicle restoration and early antler regeneration in roe deer and fallow deer.Crossref | GoogleScholarGoogle Scholar |

[12]  Li C, Suttie JM, Clark DE. Morphological observation of antler regeneration in red deer (Cervus elaphus). J Morphol 2004; 262 731–40.
Morphological observation of antler regeneration in red deer (Cervus elaphus).Crossref | GoogleScholarGoogle Scholar | 15487018PubMed |

[13]  Li C, Suttie JM, Clark DE. Histological examination of antler regeneration in red deer (Cervus elaphus). Anat Rec A Discov Mol Cell Evol Biol 2005; 282 163–74.
| 15641024PubMed |

[14]  Li C, Mackintosh CG, Martin SK, Clark DE. Identification of key tissue type for antler regeneration through pedicle periosteum deletion. Cell Tissue Res 2007; 328 65–75.
Identification of key tissue type for antler regeneration through pedicle periosteum deletion.Crossref | GoogleScholarGoogle Scholar | 17120051PubMed |

[15]  Li C, Suttie JM, Clark DE. Deer antler regeneration: a system which allows the full regeneration of mammalian appendages. In Suttie JM, Haines SR, Li C, editors. Advances in antler science and product technology. Mosgiel, New Zealand: Taieri Print Ltd; 2004. pp. 1–10.

[16]  Harper A, Wang W, Li C. Identifying ligands for S100A4 and galectin 1 in antler stem cells. In Arcus V, editor. 2009 Queenstown Molecular Biology Meetings. Queenstown, New Zealand: The Queenstown Molecular Biology Meeting Society Inc.; 2009. p. Q35.

[17]  Li C, Yang F, Sheppard A. Adult stem cells and mammalian epimorphic regeneration – insights from studying annual renewal of deer antlers. Curr Stem Cell Res Ther 2009; 4 237–51.
| 1:CAS:528:DC%2BD1MXhtVWkt7bK&md5=b0d039ff932bfc038721874cf2d4b5acCAS | 19492976PubMed |

[18]  Rolf HJ, Kierdorf U, Kierdorf H, Schulz J, Seymour N, Schliephake H, Napp J, Niebert S, Wölfel H, Wiese KG. Localization and characterization of STRO-1 cells in the deer pedicle and regenerating antler. PLoS ONE 2008; 3 e2064
Localization and characterization of STRO-1 cells in the deer pedicle and regenerating antler.Crossref | GoogleScholarGoogle Scholar | 18446198PubMed |

[19]  Li C, Suttie J. Histological studies of pedicle skin formation and its transformation to antler velvet in red deer (Cervus elaphus). Anat Rec 2000; 260 62–71.
Histological studies of pedicle skin formation and its transformation to antler velvet in red deer (Cervus elaphus).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3M%2Fhs1Cmtg%3D%3D&md5=21e29d54b26e575e261b9842540f0bc9CAS | 10967537PubMed |

[20]  Li C, Yang F, Xing X, Gao X, Deng X, Mackintosh C, Suttie JM. Role of heterotypic tissue interactions in deer pedicle and first antler formation – revealed via a membrane insertion approach. J Exp Zoolog B Mol Dev Evol 2008; 310 267–77.
Role of heterotypic tissue interactions in deer pedicle and first antler formation – revealed via a membrane insertion approach.Crossref | GoogleScholarGoogle Scholar |

[21]  Li C, Yang F, Li G, Gao X, Xing X, Wei H, Deng X, Clark DE. Antler regeneration: a dependent process of stem tissue primed via interaction with its enveloping skin. J Exp Zoolog A Comp Exp Biol 2007; 307 95–105.

[22]  Goss RJ. Induction of deer antlers by transplanted periosteum. II. Regional competence for velvet transformation in ectopic skin. J Exp Zool 1987; 244 101–11.
Induction of deer antlers by transplanted periosteum. II. Regional competence for velvet transformation in ectopic skin.Crossref | GoogleScholarGoogle Scholar |

[23]  Li C, Gao X, Yang F, Martin SK, Haines SR, Deng X, Schofield J, Stanton J-AL. Development of a nude mouse model for the study of antlerogenesis – mechanism of tissue interactions and ossification pathway. J Exp Zoolog B Mol Dev Evol 2009; 312 118–35.
Development of a nude mouse model for the study of antlerogenesis – mechanism of tissue interactions and ossification pathway.Crossref | GoogleScholarGoogle Scholar |

[24]  Li C, Yang F, Haines S, Zhao H, Wang W, Xing X, Sun H, Chu W, Lu X, Liu L, McMahon C. Stem cells responsible for deer antler regeneration are unable to recapitulate the process of first antler development – revealed through intradermal and subcutaneous tissue transplantation. J Exp Zoolog B Mol Dev Evol 2010; 314 552–70.
Stem cells responsible for deer antler regeneration are unable to recapitulate the process of first antler development – revealed through intradermal and subcutaneous tissue transplantation.Crossref | GoogleScholarGoogle Scholar |

[25]  Gao X, Yang F, Zhao H, Wang W, Li C. Antler transformation is advanced by inversion of antlerogenic periosteum implants in sika deer (Cervus nippon). Anat Rec 2010; 293 1787–96.
Antler transformation is advanced by inversion of antlerogenic periosteum implants in sika deer (Cervus nippon).Crossref | GoogleScholarGoogle Scholar |

[26]  Li C, Suttie JM. Pedicle and antler regeneration following antlerogenic tissue removal in red deer (Cervus elaphus). J Exp Zool 1994; 269 37–44.
Pedicle and antler regeneration following antlerogenic tissue removal in red deer (Cervus elaphus).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2c3msleqtA%3D%3D&md5=5c1cb2b949ee7ffd14033645f0e0ed11CAS | 8207380PubMed |

[27]  Kierdorf U, Kierdorf H. The role of the antlerogenic periosteum for pedicle and antler formation in deer. In Sim JS, Sunwoo HH, Hudson RJ, Jeon BT, editors. Banff, Canada: Antler Science and Product Technology; 2001. pp. 33–52.

[28]  Yang F, Wang W, Li J, Haines S, Asher G, Li C. Antler development was inhibited or stimulated by cryosurgery to periosteum or skin in a central antlerogenic region respectively. J Exp Zoolog B Mol Dev Evol ; in press