Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Animal Production Science Animal Production Science Society
Food, fibre and pharmaceuticals from animals
REVIEW

Deer antler: a unique model for studying mammalian organ morphogenesis

Zhao Haiping A , Chu Wenhui A , Liu Zhen A and Li Chunyi A B
+ Author Affiliations
- Author Affiliations

A State Key Laboratory for Molecular Biology of Special Economic Animals, Institute of Special Wild Economic Animals and Plants, Chinese Academy of Agricultural Sciences, Changchun, 130112, China.

B Corresponding author. Email: lichunyi1959@163.com

Animal Production Science 56(6) 946-952 https://doi.org/10.1071/AN14902
Submitted: 24 October 2014  Accepted: 10 March 2015   Published: 16 June 2015

Abstract

It is now widely accepted that organ morphogenesis in the lower animals, such as amphibians, is encoded by bioelectricity. Whether this finding applies to mammals is not known, a situation which is at least partially caused by the lack of suitable models. Deer antlers are complex mammalian organs, and their morphogenetic information resides in a primordium, the periosteum overlying the frontal crest of a prepubertal deer. The present paper reviews (1) the influence of morphogenetic information on antler formation and regeneration, and proposes that antlers are an appropriate organ for studying mammalian organ morphogenesis and (2) the storage, duplication and transferring pathways of morphogenetic information for deer antlers, and outlines a preliminary idea about how to understand the morphogenesis of mammalian organs through an involvement of bioelectricity. We believe that findings made using the deer antler model will benefit human health and wellbeing.

Additional keywords: antlerogenic periosteum, bioelectric code, pedicle periosteum, regeneration.


References

Adams DS, Levin M (2012a) Measuring resting membrane potential using the fluorescent voltage peporters DiBAC 4(3) and CC2-DMPE. Cold Spring Harbor Protocols 1, 459–464.

Adams DS, Levin M (2012b) General principles for measuring resting membrane potential and ion concentration using fluorescent bioelectricity reporters. Cold Spring Harbor Protocols 1, 385–397.

Adams DS, Levin M (2013) Endogenous voltage gradients as mediators of cell–cell communication: strategies for investigating bioelectrical signals during pattern formation. Cell and Tissue Research 352, 95–122.
Endogenous voltage gradients as mediators of cell–cell communication: strategies for investigating bioelectrical signals during pattern formation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXksFent74%3D&md5=b0aba75725c51b9df5c6ada533135db7CAS | 22350846PubMed |

Bartos L, Bubenik GA, Kuzmova E (2012) Endocrine relationships between rank-related behavior and antler growth in deer. Frontiers in Bioscience E4, 1111–1126.
Endocrine relationships between rank-related behavior and antler growth in deer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFShtr%2FL&md5=4fe80574b6d6ba5353255fa9df3a68bdCAS |

Beane WS, Morokuma J, Adams DS, Levin M (2011) A chemical genetics approach reveals H,K-ATPase-mediated membrane voltage is required for planarian head regeneration. Chemistry & Biology 18, 77–89.
A chemical genetics approach reveals H,K-ATPase-mediated membrane voltage is required for planarian head regeneration.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlarsLo%3D&md5=0707d800f1d9be5a4c98a4350b7e0ad1CAS |

Borgens RB (1999) Electrically-mediated regeneration and guidance of adult mammalian spinal axons into polymeric channels. Neuroscience 91, 251–264.
Electrically-mediated regeneration and guidance of adult mammalian spinal axons into polymeric channels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXisFKhs7w%3D&md5=1e3286e7bdf5c76621f4fc6611bce2fdCAS | 10336075PubMed |

Borgens RB, Jaffe LF, Cohen MJ (1980) Large and persistent electrical currents enter the transected lamprey spinal cord. Proceedings of the National Academy of Sciences, USA 77, 1209–1213.
Large and persistent electrical currents enter the transected lamprey spinal cord.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXhs1Wnurs%3D&md5=f6d45b62509a824eba1ab8c5041ad342CAS |

Borgens RB, Jaffe LF, Cohen MJ (1981) Enhanced spinal cord regeneration in lamprey by applied electric fields. Science 213, 611–617.
Enhanced spinal cord regeneration in lamprey by applied electric fields.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL3M3kvFWiug%3D%3D&md5=09b96ff8c6100a0ea169089d2cdc21d6CAS | 7256258PubMed |

Borgens RB, Blight AR, McGinnis ME (1987) Behavioral recovery induced by applied electric fields after spinal cord hemisection in guinea pig. Science 238, 366–369.
Behavioral recovery induced by applied electric fields after spinal cord hemisection in guinea pig.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1c%2FhvVShsg%3D%3D&md5=6953f4d6d9b03efa4606b30ca6cb44baCAS | 3659920PubMed |

Bubenik AB, Pavlansky R (1965) Trophic responses to trauma in growing antlers. The Journal of Experimental Zoology 159, 289–302.
Trophic responses to trauma in growing antlers.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaF287jvV2qsw%3D%3D&md5=a02153c61b0f2c5e188e5bbaad669fb5CAS | 5883952PubMed |

Dai L, Wu YQ, Zhu J, Wang Y, Zhou G, Liang J, Miao L (2002) An epidemiological investigation of perinatal teratomas in China. Journal of West China University of Medical Sciences 33, 111–114.

Gao X, Yang F, Zhao H, Wang W, Li C (2010) Antler transformation is advanced by inversion of antlerogenic periosteum implants in sika deer (Cervus nippon). Anatomical Record 293, 1787–1796.
Antler transformation is advanced by inversion of antlerogenic periosteum implants in sika deer (Cervus nippon).Crossref | GoogleScholarGoogle Scholar |

Gao Z, Yang F, McMahon C, Li C (2012) Mapping the morphogenetic potential of antler fields through deleting and transplanting subregions of antlerogenic periosteum in sika deer (Cervus nippon). Journal of Anatomy 220, 131–143.
Mapping the morphogenetic potential of antler fields through deleting and transplanting subregions of antlerogenic periosteum in sika deer (Cervus nippon).Crossref | GoogleScholarGoogle Scholar | 22122063PubMed |

Goss RJ (1980) Is antler asymmetry in reindeer and caribou genetically determined? Proceedings of the Reindeer/Caribou Symposium 2, 364–372.

Goss RJ (1983) ‘Deer antlers, regeneration, function and evolution.’ (Academic Press: New York)

Goss RJ (1987) Induction of deer antlers by transplanted periosteum II: regional competence for velvet transformation in ectopic skin. The Journal of Experimental Zoology 244, 101–111.
Induction of deer antlers by transplanted periosteum II: regional competence for velvet transformation in ectopic skin.Crossref | GoogleScholarGoogle Scholar |

Goss RJ (1990) ‘Horns, pronghorns, and antlers: Of antlers and embryos.’ (Springer-Verlag: New York)

Goss RJ (1991) Induction of deer antlers by transplanted periosteum III: orientation. The Journal of Experimental Zoology 259, 246–251.
Induction of deer antlers by transplanted periosteum III: orientation.Crossref | GoogleScholarGoogle Scholar |

Goss RJ (1995) Future directions in antler research. Anatomy and Embryology 241, 291–302.

Goss RJ, Powel RS (1985) Induction of deer antlers by transplanted periosteum I. Graft size and shape. The Journal of Experimental Zoology 235, 359–373.
Induction of deer antlers by transplanted periosteum I. Graft size and shape.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL28%2Fjs1SgsA%3D%3D&md5=b376a79acc25ca888c6cb05750acbbccCAS | 4056697PubMed |

Hartwig H, Schrudde J (1974) Experimentelle Untersuchungen zur Bildung der primaren Stirnauswuchse beim Reh (CAPreolus cAPreolus L.). Zeitschrift fur Jagdwissenschaft 20, 1–13.

Jaczewski Z, Doboszynska T, Krzywinski A (1976) The induction of antler growth by amputation of the pedicle in red deer (Cervus elaphus L.) males castrated before puberty. Folia Biologica 24, 299–307.

Kieny M (1968) Variation de la capacite inductrice du mesoderme et de la comptence de l’ectoderme au cours de l’induction primaire du bourgeon de membre chez l’embryon de poulet. Archrves d’anatomie microscopique et de morphologie experimentale 57, 401–418.

Kierdorf U, Kierdorf H, Szuwart T (2007) Deer antler regeneration: cells, concepts, and controversies. Journal of Morphology 268, 726–738.
Deer antler regeneration: cells, concepts, and controversies.Crossref | GoogleScholarGoogle Scholar | 17538973PubMed |

Levin M (2011) The wisdom of the body: future techniques and approaches to morphogenetic fields in regenerative medicine, developmental biology and cancer. Regenerative Medicine 6, 667–673.
The wisdom of the body: future techniques and approaches to morphogenetic fields in regenerative medicine, developmental biology and cancer.Crossref | GoogleScholarGoogle Scholar | 22050517PubMed |

Levin M (2012a) Molecular bioelectricity in developmental biology: new tools and recent discoveries: control of cell behavior and pattern formation by transmembrane potential gradients. BioEssays 34, 205–217.
Molecular bioelectricity in developmental biology: new tools and recent discoveries: control of cell behavior and pattern formation by transmembrane potential gradients.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xit1Sku7Y%3D&md5=fbb3a93a121063488abac7009414d2fdCAS | 22237730PubMed |

Levin M (2012b) Morphogenetic fields in embryogenesis, regeneration, and cancer: non-local control of complex patterning. Bio Systems 109, 243–261.
Morphogenetic fields in embryogenesis, regeneration, and cancer: non-local control of complex patterning.Crossref | GoogleScholarGoogle Scholar | 22542702PubMed |

Levin M, Stevenson CG (2012) Regulation of cell behavior and tissue patterning by bioelectrical signals: challenges and opportunities for biomedical engineering. Annual Review of Biomedical Engineering 14, 295–323.
Regulation of cell behavior and tissue patterning by bioelectrical signals: challenges and opportunities for biomedical engineering.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1Oks7rO&md5=6dbcc37a2a77ed516f6804413195c026CAS | 22809139PubMed |

Li C, Suttie JM (1994) Light microscopic studies of pedicle and early first antler development in red deer (Cervus elaphus). The Anatomical Record 239, 198–215.
Light microscopic studies of pedicle and early first antler development in red deer (Cervus elaphus).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2czjsl2qtg%3D%3D&md5=7fad0811665763245acaa15a3029b77bCAS | 8059982PubMed |

Li C, Suttie JM (2001a) Deer antler generation: a process from permanent to deciduous. In ‘1st international symposium on antler science and product technology’. (Eds JS Sim, HH Sunwoo, RJ Hudson, BT Jeon) pp. 15–31. (Banff, Canada)

Li C, Suttie JM (2001b) Deer antlerogenic periosteum: a piece of postnatally retained embryonic tissue? Anatomy and Embryology 204, 375–388.
Deer antlerogenic periosteum: a piece of postnatally retained embryonic tissue?Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38%2FmtlKitA%3D%3D&md5=7bc95dfc5e650e08d3ea70a30caf14abCAS | 11789985PubMed |

Li C, Suttie JM (2012) Morphogenetic aspects of deer antler development. Frontiers in Bioscience E4, 1836–1842.
Morphogenetic aspects of deer antler development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFOhsb7J&md5=d11cdbcd844769faf3845b1e3238b89bCAS |

Li C, Zhao S, Wang W (1988) ‘Deer antler.’ (China Agricultural Science and Technology Press: Beijing)

Li C, Harris AJ, Suttie JM (2001) Tissue interactions and antlerogenesis: new findings revealed by a xenograft Approach. The Journal of Experimental Zoology 290, 18–30.
Tissue interactions and antlerogenesis: new findings revealed by a xenograft Approach.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MzntFGrtA%3D%3D&md5=27a5e82b75dd7b9763e5480e95a0b358CAS | 11429760PubMed |

Li C, Littlejohn RP, Corson ID, Suttie JM (2003) 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 131, 21–31.
Effects of testosterone on pedicle formation and its transformation to antler in castrated male, freemartin and normal female red deer (Cervus elaphus).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhs1KgsL4%3D&md5=494dcb1aa43e2e4add4577471406f37dCAS | 12620243PubMed |

Li C, Suttie JM, Clark DE (2004) Morphological observation of antler regeneration in red deer (Cervus elaphus). Journal of Morphology 262, 731–740.
Morphological observation of antler regeneration in red deer (Cervus elaphus).Crossref | GoogleScholarGoogle Scholar | 15487018PubMed |

Li C, Mackintosh CG, Martin SK, Dawn C (2007a) Identification of key tissue type for antler regeneration through pedicle periosteum deletion. Cell and Tissue Research 328, 65–75.
Identification of key tissue type for antler regeneration through pedicle periosteum deletion.Crossref | GoogleScholarGoogle Scholar | 17120051PubMed |

Li C, Yang F, Li G, Gao X, Xing X, Wei H, Deng X, Clark DE (2007b) Antler regeneration: a dependent process of stem tissue primed via interaction with its enveloping skin. The Journal of Experimental Zoology 307A, 95–105.
Antler regeneration: a dependent process of stem tissue primed via interaction with its enveloping skin.Crossref | GoogleScholarGoogle Scholar |

Li C, Gao X, Yang F, Martin SK, Haines SR, Deng X, Schofield J, Stanton JA (2009) Development of a nude mouse model for the study of antlerogenesis–mechanism of tissue interactions and ossification pathway. The Journal of Experimental Zoology 312B, 118–135.
Development of a nude mouse model for the study of antlerogenesis–mechanism of tissue interactions and ossification pathway.Crossref | GoogleScholarGoogle Scholar |

Pai VP, Aw S, Shomrat T, Lemire JM, Levin M (2012) Transmembrane voltage potential controls embryonic eye patterning in Xenopus laevis. Development 139, 313–323.
Transmembrane voltage potential controls embryonic eye patterning in Xenopus laevis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xjt1Git7c%3D&md5=a15e411f475a7bc49065b33960f4ae04CAS | 22159581PubMed |

Pineda RH, Svoboda KR, Wright MA, Taylor AD, Novak AE, Gamse JT, Eisen JS, Ribera AB (2006) Knockdown of Nav1.6a Na+ channels affects zebrafish motoneuron development. Development 133, 3827–3836.
Knockdown of Nav1.6a Na+ channels affects zebrafish motoneuron development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFyms7%2FO&md5=dbf204e89e75f79ca67178dd9bb32296CAS | 16943272PubMed |

Pocock RI (1933) The homologies between the branches of the antlers of the Cervidse based on the theory of dichotomous growth. Zoology 103, 377–406.
The homologies between the branches of the antlers of the Cervidse based on the theory of dichotomous growth.Crossref | GoogleScholarGoogle Scholar |

Sheldrake R (1981) ‘A new science of life: the hypothesis of formative causation.’ (J. P. Tarcher Incorporated: Los Angeles, CA)

Suttie JM, Fennessy PF, Lapwood KR, Corson ID (1995) Role of steroids in antler growth of red deer stags. The Journal of Experimental Zoology 271, 120–130.
Role of steroids in antler growth of red deer stags.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXkslaju78%3D&md5=9403afc188419460617d972f45a2528fCAS | 7884386PubMed |

Thompson DW (1917). ‘On growth and form.’ (Cambridge University Press: Cambridge, UK)

Todt W, Fallon J (1984) Development of the apical ectodermal ridge in the chick wing bud. Journal of Embryology and Exerimental Morphology 80, 21–41.

Tseng A, Levin M (2013) Cracking the bioelectric code: probing endogenous ionic controls of pattern formation. Communicative & Integrative Biology 6, e22595
Cracking the bioelectric code: probing endogenous ionic controls of pattern formation.Crossref | GoogleScholarGoogle Scholar |

Tseng AS, Beane WS, Lemire JM, Masi A, Levin M (2010) Induction of vertebrate regeneration by a transient sodium current. The Journal of Neuroscience 30, 13192–13200.
Induction of vertebrate regeneration by a transient sodium current.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1KisLbN&md5=778fd07e4fed400537f56fd260be44b7CAS | 20881138PubMed |

Vandenberg LN, Morrie RD, Adams DS (2011) V-ATPase-dependent ectodermal voltage and pH regionalization are required for craniofacial morphogenesis. Developmental Dynamics 240, 1889–1904.
V-ATPase-dependent ectodermal voltage and pH regionalization are required for craniofacial morphogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXovFGjtL8%3D&md5=cb584b8366a49841251103f71483feaeCAS | 21761475PubMed |