Deer antlers - A model of mammalian appendage regeneration: An extensive review

Gerontology

Volumn 57, Issue 1, 2010, Pages 53-65

  Kierdorf, Uwe ^a   Kierdorf, Horst ^a  

^a UNIVERSITY OF HILDESHEIM   (Germany)

Author keywords

Antlers; Epimorphic regeneration; Periosteum; Regenerative medicine; Stem cells

Indexed keywords

ANTIANDROGEN; BETA CATENIN; CD9 ANTIGEN; ESTROGEN; FIBROBLAST GROWTH FACTOR; OCTAMER TRANSCRIPTION FACTOR 4; RETINOIC ACID; SOMATOMEDIN C; TESTOSTERONE; TRANSCRIPTION FACTOR NANOG;

AMPHIBIA; ANIMAL ANATOMY; ANTIANDROGEN THERAPY; APPENDAGE; BONE TUMOR; CARCINOGENESIS; CASTRATION; DEER; EPIDERMIS; EXPERIMENTAL MODEL; GROWTH RATE; HISTOGENESIS; HORN; MALIGNANT TRANSFORMATION; MAMMAL; MORPHOGENESIS; NERVE FIBER REGENERATION; NONHUMAN; PERIOSTEUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGENERATION; REGENERATIVE MEDICINE; REVIEW; SCAR FORMATION; SIGNAL TRANSDUCTION; SKIN INJURY; SMOOTH MUSCLE FIBER; STEM CELL; WOUND HEALING; ZEBRA FISH;

ADULT STEM CELLS; ANIMALS; ANTLERS; DEER; FEMALE; HUMANS; MALE; MODELS, BIOLOGICAL; NEOPLASMS; REGENERATION; REGENERATIVE MEDICINE; SPECIES SPECIFICITY; WOUND HEALING;

EID: 78651089161     PISSN: 0304324X     EISSN: None     Source Type: Journal    
DOI: 10.1159/000300565     Document Type: Review

References (81)

1. Stocum DL: Regenerative Biology and Medicine. Amsterdam, Elsevier Academic Press, 2006.
2. Carlson BM: Principles of Regenerative Biology. Amsterdam, Elsevier Academic Press, 2007.
3. Gardiner DM, Bryant SV: Tetrapod limb regeneration; in Hall BK (ed): Fins into Limbs: Evolution, Development, and Transformation. Chicago, University of Chicago Press, 2007, pp 163-182.
4. Yakushiji N, Yokoyama H, Tamura K: Repatterning in amphibian limb regeneration: a model for study of genetic and epigenetic control of organ regeneration. Semin Cell Dev Biol 2009; 20: 565-574.
5. Tseng AS, Levin M: Tail regeneration in Xenopus laevis as a model for understanding tissue repair. J Dent Res 2008; 87: 806-816.
6. Gardiner DM: Ontogenetic decline of regenerative ability and the stimulation of human regeneration. Rejuvenation Res 2005; 8: 141-153.
7. Han M, Yang X, Lee J, Allan CH, Muneoka K: Development and regeneration of the neonatal digit tip in mice. Dev Biol 2008; 315: 125-135.
8. Goss RJ: Deer Antlers: Regeneration, Function, and Evolution. New York, Academic Press, 1983.
9. Goss RJ: Epimorphic regeneration in mammals; in Hunt TK, Heppenstall RB, Pines E, Rovee D (eds): Soft and Hard Tissue Repair. New York, Praeger, 1984, pp 554-573.
10. Goss RJ: Prospects for regeneration in man. Clin Orthop Relat Res 1980; 151: 270-282.
11. Price J, Faucheux C, Allen S: Deer antlers as a model of mammalian regeneration. Curr Top Dev Biol 2005; 67: 1-48.
12. Price JS, Allen S, Faucheux C, Althnaian T, Mount JG: Deer antlers: a zoological curiosity or the key to understanding organ regeneration in mammals? J Anat 2005; 207: 603-618.
13. Kierdorf U, Kierdorf H, Szuwart T: Deer antler regeneration: cells, concepts, and controversies. J Morphol 2007; 268: 726-738.
14. Kierdorf U, Li C, Price J: Improbable appendages: deer antler renewal as a unique case of mammalian regeneration. Semin Cell Dev Biol 2009; 20: 535-542.
15. 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: 237-251.
16. Kierdorf U, Kierdorf H: Pedicle and first antler formation in deer: anatomical, histological, and developmental aspects. Z Jagdwiss 2002; 48: 22-34.
17. Bubenik GA: The endocrine control of the antler cycle; in Brown RD (ed): Antler Development in Cervidae. Kingsville, Caesar Kleberg Wildlife Research Institute, 1983, pp 73-107.
18. Suttie JM, Lincoln GA, Kay RNB: Endocrine control of antler growth in red deer stags. J Reprod Fertil 1984; 71: 7-15.
19. Goss RJ: Problems of antlerogenesis. Clin Orthop Relat Res 1970; 69: 227-238.
20. Li C, Stanton JL, Robertson TM, Suttie JM, Sheard PW, Harris AJ, Clark DE: Nerve growth factor mRNA expression in the regenerating antler tip of red deer (Cervus elaphus) . PLoS One 2007; 2:e148.
21. Hartwig H, Schrudde J: Experimentelle Untersuchungen zur Bildung der primären Stirnauswüchse beim Reh ( Capreolus capreolus L.). Z Jagdwiss 1974; 20: 1-13.
22. Goss RJ, Powel RS: Induction of deer antlers by transplanted periosteum. I. Graft size and shape. J Exp Zool 1985; 235: 359-373.
23. Kierdorf H, Kierdorf U: The role of the antlerogenic periosteum for pedicle and antler formation in deer; in Sim JS, Sunwoo HH, Hudson RJ, Jeon BT (eds): Antler Science and Product Technology. Edmonton, ASPTRC, 2001, pp 33-51.
24. Goss RJ: Induction of deer antlers by transplanted periosteum. II. Regional competence for velvet transformation in ectopic skin. J Exp Zool 1987; 244: 101-111.
25. Goss RJ: Induction of deer antlers by transplanted periosteum. III. Orientation. J Exp Zool 1991; 259: 246-251.
26. Jiang XB, Iseki S, Maxson RE, Sucov HM, Morriss-Kay GM: Tissue origins and interactions in the mammalian skull vault. Dev Biol 2002; 241: 106-116.
27. Kierdorf H, Kierdorf U, Szuwart T, Gath U, Clemen G: Light microscopic observations on the ossification process in the early developing pedicle of fallow deer (Dama dama) . Ann Anat 1994; 176: 243-249. (Pubitemid 24185362)
28. Li C, Suttie JM: Light microscopic studies of pedicle and early first antler development in red deer (Cervus elaphus) . Anat Rec 1994; 239: 198-215.
29. Berg DK, Li C, Asher G, Wells DN, Oback B: Red deer cloned from antler stem cells and their differentiated progeny. Biol Reprod 2007; 77: 384-394.
30. Goss RJ: Of antlers and embryos; in Bubenik GA, Bubenik AB (eds): Horns, Pronghorns, and Antlers. New York, Springer, 1990, pp 298-312.
31. Li C, Yuang 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 Zool (Mol Dev Evol) 2008; 310B:267-277.
32. Li C, Gao X, Yang F, Martin SK, Haines SR, Deng X, Schofield J, Stanton JL: Development of a nude mouse model for the study of antlerogenesis -mechanism of tissue interactions and ossification pathway. J Exp Zool (Mol Dev Evol) 2009; 312B:118-135.
33. Gruber GB: Morphobiologische Untersuchungen am Cerviden-Geweih. Werden, Wechsel und Wesen des Rehgehörns. Nachr Ges Wiss Göttingen Math Phys Kl NF Fachgr VI 1937; 3: 9-63.
34. 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.
35. Waldo CM, Wislocki GB, Fawcett DW: Observations on the blood supply of growing antlers. Am J Anat 1949; 84: 27-61.
36. Rolf HJ, Enderle A: Hard fallow deer antler: a living bone till antler casting? Anat Rec 1999; 255: 68-77.
37. Kierdorf U, Schultz M, Fischer K: Effects of an antiandrogen treatment on the antler cycle of male fallow deer ( Dama dama L.). J Exp Zool 1993; 266: 195-205.
38. Goss RJ: Inhibition of growth and shedding of antlers by sex hormones. Nature 1968; 220: 83-85.
39. Goss RJ, Van Praagh A, Brewer P: The mechanism of antler casting in the fallow deer. J Exp Zool 1992; 264: 429-436.
40. Kierdorf U, Kierdorf H: Der Doppelkopf, ein für das Verständnis der Folgegeweih-Bildung aufschlussreiches Naturexperiment. Z Jagdwiss 1992; 38: 244-251.
41. 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 A 2003; 273A:741-751.
42. Li C, Suttie JM, Clark DE: Histological examination of antler regeneration in red deer (Cervus elaphus) . Anat Rec A 2005; 282A: 163-174.
43. Kierdorf H, Kierdorf U: State of determination of the antlerogenic tissues with special reference to double-head formation; in Brown RD (ed): The Biology of Deer. New York, Springer, 1992, pp 525-531.
44. Stoick-Cooper CL, Moon RT, Weidinger G: Advances in signaling in vertebrate regeneration as a prelude to regenerative medicine. Genes Dev 2007; 21: 1292-1315.
45. Goss RJ: Wound healing and antler regeneration; in Maibach HI, Rovee DT (eds): Epidermal Wound Healing. Chicago, Year Book Medical Publishers, 1972, pp 219-228.
46. Harty M, Neff AW, King MW, Mescher AL: Regeneration or scarring: an immunologic perspective. Dev Dyn 2003; 226: 268-279.
47. Goss RJ: Future directions in antler research. Anat Rec 1995; 241: 291-302.
48. Clark RAF: Wound repair. Overview and general considerations; in Clark RAF (ed): The Molecular and Cellular Biology of Wound Repair, ed 2. New York, Plenum Press, 1996, pp 3-50.
49. Ito M, Yang Z, Andl T, Cui C, Kim N, Millar SE, Cotsarelis G: Wnt-dependent de novo hair follicle regeneration in adult mouse skin after wounding. Nature 2007; 447: 316-320.
50. Ferguson MWJ, O'Kane S: Scar-free healing: from embryonic mechanisms to adult therapeutic intervention. Phil Trans R Soc Lond B 2004; 359: 839-850.
51. Eming SA, Hammerschmidt M, Krieg T, Roers A: Interrelation of immunity and tissue repair or regeneration. Semin Cell Dev Biol 2009; 20: 517-527.
52. Akimenko MA, Smith A: Paired fin repair and regeneration; in Hall BK (ed): Fins into Limbs: Evolution, Development, and Transformation. Chicago, University of Chicago Press, 2007, pp 152-162.
53. Mescher AL: The cellular basis of limb regeneration in urodeles. Int J Dev Biol 1996; 40: 785-795.
54. Gyurján I, Molnár A, Borsy A, Stéger V, Hackler L, Zomborsky Z, Papp P, Duda E, Deák F, Lakatos P, Puskás LG, Orosz L: Gene expression dynamics in deer antler: mesenchymal differentiation towards chondrogenesis. Mol Genet Genomics 2007; 277: 221-235.
55. 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 Zool 2007; 307A:95-105.
56. Kierdorf U, Kierdorf H, Schultz M: The macroscopic and microscopic structure of double-head antlers and pedicle bone of Cervidae (Mammalia, Artiodactyla). Ann Anat 1994; 176: 251-257.
57. Li C, Mackintosh CG, Martin SK, Clark DE: Identification of key tissue type for antler regeneration through pedicle periosteum deletion.
58. Cell Tissue Res 2007; 328: 65-75.
59. Kragl M, Knapp D, Nacu E, Khattak S, Maden M, Epperlein HH, Tanaka EM: Cells keep a memory of their tissue origin during axolotl limb regeneration. Nature 2009; 460: 60-65.
60. Morrison JI, Lööf S, He P, Simon A: Salamander limb regeneration involves the activation of a multipotent skeletal muscle satellite cell population. J Cell Biol 2006; 172: 433-440.
61. Echeverri K, Clarke JDW, Tanaka EM: In vivo imaging indicates muscle fiber dedifferentiation is a major contributor to the regenerating tail blastema. Dev Biol 2001; 236: 151-164.
62. Gargioli C, Slack JWM: Cell lineage tracing during Xenopus tail regeneration. Development 2004; 131: 2669-2679.
63. Nechiporuk A, Keating MT: A proliferation gradient between proximal and msxb -expressing distal blastema directs zebrafish fin regeneration. Development 2002; 129: 2607-2617.
64. 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.
65. Mount JG, Muzylak M, Allen S, Okushima S, Althnaian T, McGonnell IM, Price JS: Antlers may regenerate from persistent neural crestlike stem cells; in Bartoš L, Dušek A, Kotrba R, Bartošová- Víchová J (eds): Advances in Deer Biology. Proc 5th Int Deer Biol Congress, Prague, 2006, p 161.
66. Price JS, Faucheux C: Exploring the molecular mechanisms of antler regeneration; in Sim JS, Sunwoo HH, Hudson RJ, Jeon BT (eds): Antler Science and Product Technology. Edmonton, ASPTRC, 2001, pp 53-67.
67. Banks WJ, Newbrey JW: Light microscopic studies of the ossification process in developing antlers; in Brown RD (ed): Antler Development in Cervidae. Kingsville, Caesar Kleberg Wildlife Research Institute, 1983, pp 231-260.
68. Colitti M, Allen SP, Price JS: Programmed cell death in the regenerating deer antler. J Anat 2005; 207: 339-351.
69. Kierdorf H, Kierdorf U, Szuwart T, Clemen G: A light microscopic study of primary antler development in fallow deer (Dama dama) . Ann Anat 1995; 177: 525-532.
70. Kierdorf U, Kierdorf H, Schultz M, Rolf HJ: Histological structure of antlers in castrated male fallow deer (Dama dama) . Anat Rec A 2004; 281A:1352-1362.
71. Mount JG, Muzylak M, Allen S, Althnaian T, McGonnell IM, Price JS: Evidence that the canonical Wnt signalling pathway regulates deer antler regeneration. Dev Dyn 2006; 235: 1390-1399.
72. Allen SP, Maden M, Price JS: A role for retinoic acid in regulating the regeneration of deer antlers. Dev Biol 2002; 251: 409-423.
73. Kierdorf U, Bartoš L: Treatment of the growing pedicle with retinoic acid increased the size of first antlers in fallow deer ( Dama dama L.). Comp Biochem Physiol C 1999; 124: 7-9.
74. Kierdorf U, Kierdorf H: Effects of retinoic acid on pedicle and first antler growth in a fallow buck ( Dama dama L.). Ann Anat 1998; 180: 373-375.
75. Suttie JM, Fennessy PF: Regrowth of amputated velvet antlers with and without innervation. J Exp Zool 1985; 234: 359-366.
76. Bubenik GA: The role of the nervous system in the growth of antlers; in Bubenik GA, Bubenik AB (eds): Horns, Pronghorns, and Antlers. New York, Springer, 1990, pp 339-358.
77. Steinwedel M: Histologische und histogenetische Studien über das Geweih von Cervus elaphus , von Cervus capreolus und Rangifer tarandus ; zugleich ein Beitrag zur Kenntnis des Verknöcherungs-Vorganges; doctoral thesis, Tierärztliche Hochschule Berlin, 1929, pp 1-81.
78. Kierdorf H, Kierdorf U: Knochengeschwulst an Damhirschstange. Z Jagdwiss 1985; 31; 52-55.
79. Oviedo NJ, Beane WS: Regeneration: the origin of cancer or a possible cure? Semin Cell Dev Biol 2009; 20: 557-564.
80. Prehn RT: Regeneration versus neoplastic growth. Carcinogenesis 1997; 18: 1439-1444.
81. Goss RJ: Tumor-like growth of antlers in castrated fallow deer: an electron microscopic study. Scanning Microsc 1990; 4: 715-721.