Advertisement

Genetics and Regeneration in Vertebrates

  • Elizabeth D. Hutchins
  • Kenro KusumiEmail author
Chapter
First Online:

Abstract

Regeneration is a common trait in vertebrates, with regrowth of entire appendages carried out by a number of groups including teleost fish, amphibians, and squamate reptiles. While humans are also vertebrates, we have very limited ability to regenerate as adults. Cellular and molecular studies in zebrafish, Xenopus frog, axolotl, and green anole lizard model systems have identified components of genetic programs for regeneration that include both developmental and adult repair mechanisms shared with mammals. Regeneration in vertebrates involves the genetic regulation of wound epithelium formation, modulation of the immune response, remodeling of the extracellular matrix, patterning of the regrowing appendage, and activation of Wnt/β-catenin and FGF signaling pathways. By understanding the mechanisms by which vertebrates are able to regenerate their appendages, we can translate these processes to develop clinically relevant regenerative therapies.

Keywords

Vertebrate Tetrapods Non-tetrapod vertebrate Teleost fish Amphibians Squamate reptiles Zebrafish Xenopus frog Axolotl Ambystoma mexicanum Mammals Inflammation Immune response Extracellular matrix Regeneration 
This is a preview of subscription content, log in to check access.

Notes

Acknowledgments

The authors would like to acknowledge Jeanne Wilson-Rawls, Matt Huentelman, Alan Rawls, Dale DeNardo, Rebecca Fisher, Stephen Pratt, Joshua Ho, and members of the Kusumi Lab at Arizona State University for helpful discussions. We thank Joel Robertson for his photograph of the green anole.

References

  1. Agata K, Inoue T (2012) Survey of the differences between regenerative and non-regenerative animals. Dev Growth Differ 54(2):143–152. doi: 10.1111/j.1440-169X.2011.01323.x PubMedCrossRefGoogle Scholar
  2. Alföldi J, Di Palma F, Grabherr M et al (2011) The genome of the green anole lizard and a comparative analysis with birds and mammals. Nature 477(7366):587–591. doi: 10.1038/nature10390 PubMedPubMedCentralCrossRefGoogle Scholar
  3. Alibardi L (1995a) Development of the axial cartilaginous skeleton in the regenerating tail of lizards. Bull Assoc Anat (Nancy) 79(244):3–9Google Scholar
  4. Alibardi L (1995b) Muscle differentiation and morphogenesis in the regenerating tail of lizards. J Anat 186(Pt 1):143–151PubMedPubMedCentralGoogle Scholar
  5. Alibardi L (2010a) Morphological and cellular aspects of tail and limb regeneration in lizards. A model system with implications for tissue regeneration in mammals. Adv Anat Embryol Cell Biol 207:iii–v–x– 1–109Google Scholar
  6. Alibardi L (2010b) Ultrastructural features of the process of wound healing after tail and limb amputation in lizard. Acta Zool 91(3):306–318. doi: 10.1111/j.1463-6395.2009.00409.x Google Scholar
  7. Alibardi L (2014a) Observations on lumbar spinal cord recovery after lesion in lizards indicates regeneration of a cellular and fibrous bridge reconnecting the injured cord. J Dev Biol 2(4):210–229. doi: 10.3390/jdb2040210 CrossRefGoogle Scholar
  8. Alibardi L (2014b) Ultrastructural observations on lumbar spinal cord recovery after lesion in lizard indicates axonal regeneration and neurogenesis. Int J Biol 7(1). doi: 10.5539/ijb.v7n1p122
  9. Alibardi L, Celeghin A, Valle LD (2012) Wounding in lizards results in the release of beta-defensins at the wound site and formation of an antimicrobial barrier. Dev Comp Immunol 36(3):557–565. doi: 10.1016/j.dci.2011.09.012 PubMedCrossRefGoogle Scholar
  10. Barron L, Wynn TA (2011) Macrophage activation governs schistosomiasis-induced inflammation and fibrosis. Eur J Immunol 41(9):2509–2514. doi: 10.1002/eji.201141869 PubMedPubMedCentralCrossRefGoogle Scholar
  11. Beck CW, Christen B, Slack JMW (2003) Molecular pathways needed for regeneration of spinal cord and muscle in a vertebrate. Dev Cell 5(3):429–439PubMedCrossRefGoogle Scholar
  12. Beck CW, Izpisúa Belmonte JC, Christen B (2009) Beyond early development: Xenopus as an emerging model for the study of regenerative mechanisms. Dev Dyn 238(6):1226–1248. doi: 10.1002/dvdy.21890 PubMedCrossRefGoogle Scholar
  13. Becker T, Wullimann MF, Becker CG et al (1997) Axonal regrowth after spinal cord transection in adult zebrafish. J Comp Neurol 377(4):577–595PubMedCrossRefGoogle Scholar
  14. Bellairs AD, Bryant SV (1985) Autotomy and regeneration in reptiles. In: Gans C, Billet F (eds) Biology of the reptilia. Wiley, New York, pp 301–409Google Scholar
  15. Bely AE, Nyberg KG (2010) Evolution of animal regeneration: re-emergence of a field. Trends Ecol Evol 25(3):161–170. doi: 10.1016/j.tree.2009.08.005 PubMedCrossRefGoogle Scholar
  16. Benders KEM, van Weeren PR, Badylak SF et al (2013) Extracellular matrix scaffolds for cartilage and bone regeneration. Trends Biotechnol 31:171–178. doi: 10.1016/j.tibtech.2012.12.004 CrossRefGoogle Scholar
  17. Borgens RB (1982) Mice regrow the tips of their foretoes. Science 217(4561):747–750PubMedCrossRefGoogle Scholar
  18. Bosco L (1979) Expression of regenerative capacity of caudal spinal cord during the larval development of Xenopus laevis. Acta Embryol Exp 3:275–285Google Scholar
  19. Brockes JP, Kumar A (2008) Comparative aspects of animal regeneration. Annu Rev Cell Dev Biol 24(1):525–549. doi: 10.1146/annurev.cellbio.24.110707.175336 PubMedCrossRefGoogle Scholar
  20. Bryant SV, Endo T, Gardiner DM (2002) Vertebrate limb regeneration and the origin of limb stem cells. Int J Dev Biol 46(7):887–896PubMedGoogle Scholar
  21. Butler EG, O’Brien JP (1942) Effects of localized X radiation on regeneration of the urodele limb. Anat Rec (Hoboken) 84(4):407–413. doi: 10.1002/ar.1090840408 CrossRefGoogle Scholar
  22. Cameron DA (2000) Cellular proliferation and neurogenesis in the injured retina of adult zebrafish. Vis Neurosci 17(5):789–797PubMedCrossRefGoogle Scholar
  23. Campbell LJ, Crews CM (2008) Molecular and cellular basis of regeneration and tissue repair. Cell Mol Life Sci 65(1):54–63. doi: 10.1007/s00018-007-7431-1 CrossRefGoogle Scholar
  24. Cañestro C, Yokoi H, Postlethwait JH (2007) Evolutionary developmental biology and genomics. Nat Rev Genet 8:932–942. doi: 10.1038/nrg2226 PubMedCrossRefGoogle Scholar
  25. Carlson MR, Bryant SV, Gardiner DM (1998) Expression of Msx-2 during development, regeneration, and wound healing in axolotl limbs. J Exp Zool 282(6):715–723PubMedCrossRefGoogle Scholar
  26. Chadwick RB, Bu L, Yu H et al (2007) Digit tip regrowth and differential gene expression in MRL/Mpj, DBA/2, and C57BL/6 mice. Wound Repair Regen 15(2):275–284. doi: 10.1111/j.1524-475X.2007.00216.x PubMedCrossRefGoogle Scholar
  27. Chlebowski JS, Przbylski RJ, Cox PG (1973) Ultrastructural studies of lizard (I) myogenesis in vitro. Dev Biol 33(1):80–99PubMedCrossRefGoogle Scholar
  28. Christensen RN, Tassava RA (2000) Apical epithelial cap morphology and fibronectin gene expression in regenerating axolotl limbs. Dev Dyn 217(2):216–224. doi: 10.1002/(SICI)1097-0177(200002)217:2<216::AID-DVDY8>3.0.CO;2-8 PubMedCrossRefGoogle Scholar
  29. Christensen RN, Weinstein M, Tassava RA (2002) Expression of fibroblast growth factors 4, 8, and 10 in limbs, flanks, and blastemas of Ambystoma. Dev Dyn 223(2):193–203. doi: 10.1002/dvdy.10049 PubMedCrossRefGoogle Scholar
  30. Cox PG (1968) In vitro myogenesis of promuscle cells from the regenerating tail of the lizard, Anolis carolinensis. J Morphol 126(1):1–18. doi: 10.1002/jmor.1051260102 PubMedCrossRefGoogle Scholar
  31. Cox PG (1969) Some aspects of tail regeneration in the lizard, Anolis carolinensis. I. A description based on histology and autoradiography. J Exp Zool 171(2):127–149. doi: 10.1002/jez.1401710202 CrossRefGoogle Scholar
  32. da Silva SM, Gates PB, Brockes JP (2002) The newt ortholog of CD59 is implicated in proximodistal identity during amphibian limb regeneration. Dev Cell 3(4):547–555PubMedCrossRefGoogle Scholar
  33. Delavary BM, van der Veer WM, van Egmond M (2011) Macrophages in skin injury and repair. Immunobiology 216(7):753–762. doi: 10.1016/j.imbio.2011.01.001 CrossRefGoogle Scholar
  34. Delorme SL, Lungu IM, Vickaryous MK (2012) Scar-free wound healing and regeneration following tail loss in the leopard gecko, Eublepharis macularius. Anat Rec (Hoboken) 295(10):1575–1595. doi: 10.1002/ar.22490 CrossRefGoogle Scholar
  35. Dent JN (1962) Limb regeneration in larvae and metamorphosing individuals of the South African clawed toad. J Morphol 110:61–77. doi: 10.1002/jmor.1051100105 PubMedCrossRefGoogle Scholar
  36. Dial BE, Fitzpatrick LC (1983) Lizard tail autotomy: function and energetics of postautotomy tail movement in Scincella lateralis. Science 219(4583):391–393. doi: 10.1126/science.219.4583.391 PubMedCrossRefGoogle Scholar
  37. Donoghue PCJ, Benton MJ (2007) Rocks and clocks: calibrating the Tree of Life using fossils and molecules. Trends Ecol Evol 22(8):424–431PubMedCrossRefGoogle Scholar
  38. Douglas BS (1972) Conservative management of guillotine amputation of the finger in children. Aust Paediatr J 8(2):86–89PubMedGoogle Scholar
  39. Duffy MT, Simpson SB Jr, Liebich DR et al (1990) Origin of spinal cord axons in the lizard regenerated tail: supernormal projections from local spinal neurons. J Comp Neurol 293(2):208–222. doi: 10.1002/cne.902930205 PubMedCrossRefGoogle Scholar
  40. Echeverri K, Tanaka EM (2002) Ectoderm to mesoderm lineage switching during axolotl tail regeneration. Science 298(5600):1993–1996. doi: 10.1126/science.1077804 PubMedCrossRefGoogle Scholar
  41. Eckalbar WL, Lasku E, Infante CR et al (2012) Somitogenesis in the anole lizard and alligator reveals evolutionary convergence and divergence in the amniote segmentation clock. Dev Biol 363(1):308–319. doi: 10.1016/j.ydbio.2011.11.021 PubMedCrossRefGoogle Scholar
  42. Eckalbar WL, Hutchins ED, Markov GJ et al (2013) Genome reannotation of the lizard Anolis carolinensis based on 14 adult and embryonic deep transcriptomes. BMC Genomics 14:49. doi: 10.1186/1471-2164-14-49 PubMedPubMedCentralCrossRefGoogle Scholar
  43. Egar M, Simpson SB Jr, Singer M (1970) The growth and differentiation of the regenerating spinal cord of the lizard, Anolis carolinensis. J Morphol 131(2):131–151. doi: 10.1002/jmor.1051310202 PubMedCrossRefGoogle Scholar
  44. Endo T, Tamura K, Ide H (2000) Analysis of gene expressions during Xenopus forelimb regeneration. Dev Biol 220(2):296–306. doi: 10.1006/dbio.2000.9641 PubMedCrossRefGoogle Scholar
  45. Fahmy GH, Sicard RE (2002) A role for effectors of cellular immunity in epimorphic regeneration of amphibian limbs. In Vivo 16(3):179–184PubMedGoogle Scholar
  46. Fernando WA, Leininger E, Simkin J et al (2011) Wound healing and blastema formation in regenerating digit tips of adult mice. Dev Biol 350(2):301–310. doi: 10.1016/j.ydbio.2010.11.035 PubMedPubMedCentralCrossRefGoogle Scholar
  47. Filoni S, Paglialunga L (1990) Effect of denervation on hindlimb regeneration in Xenopus laevis larvae. Differentiation 43(1):10–19PubMedCrossRefGoogle Scholar
  48. Fisher RE, Geiger LA, Stroik LK et al (2012) A histological comparison of the original and regenerated tail in the green anole, Anolis carolinensis. Anat Rec (Hoboken) 295(10):1609–1619. doi: 10.1002/ar.22537 CrossRefGoogle Scholar
  49. Gaete M, Muñoz R, Sánchez N et al (2012) Spinal cord regeneration in Xenopus tadpoles proceeds through activation of Sox2-positive cells. Neural Dev 7:13. doi: 10.1186/1749-8104-7-13 PubMedPubMedCentralCrossRefGoogle Scholar
  50. Galliera E, Tacchini L, Corsi Romanelli MM (2015) Matrix metalloproteinases as biomarkers of disease: updates and new insights. Clin Chem Lab Med 53(3):349–355. doi: 10.1515/cclm-2014-0520 PubMedCrossRefGoogle Scholar
  51. Gargioli C, Slack JMW (2004) Cell lineage tracing during Xenopus tail regeneration. Development 131(11):2669–2679. doi: 10.1242/dev.01155 PubMedCrossRefGoogle Scholar
  52. Gemberling M, Bailey TJ, Hyde DR et al (2013) The zebrafish as a model for complex tissue regeneration. Trends Genet 29(11):611–620. doi: 10.1016/j.tig.2013.07.003 PubMedCrossRefGoogle Scholar
  53. Géraudie J, Singer M (1992) The fish fin regenerate. Monogr Dev Biol 23:62–72PubMedGoogle Scholar
  54. Ghosh S, Roy S, Séguin C et al (2008) Analysis of the expression and function of Wnt-5a and Wnt-5b in developing and regenerating axolotl (Ambystoma mexicanum) limbs. Dev Growth Differ 50(4):289–297. doi: 10.1111/j.1440-169X.2008.01000.x PubMedCrossRefGoogle Scholar
  55. Gilbert EAB, Payne SL, Vickaryous MK (2013a) The anatomy and histology of caudal autotomy and regeneration in lizards. Physiol Biochem Zool 86(6):631–644. doi: 10.1086/673889 PubMedCrossRefGoogle Scholar
  56. Gilbert RWD, Vickaryous MK, Viloria-Petit AM (2013b) Characterization of TGFβ signaling during tail regeneration in the leopard gecko (Eublepharis macularius). Dev Dyn 242(7):886–896. doi: 10.1002/dvdy.23977 PubMedCrossRefGoogle Scholar
  57. Godwin JW, Brockes JP (2006) Regeneration, tissue injury and the immune response. J Anat 209(4):423–432. doi: 10.1111/j.1469-7580.2006.00626.x PubMedPubMedCentralCrossRefGoogle Scholar
  58. Godwin JW, Rosenthal N (2014) Scar-free wound healing and regeneration in amphibians: immunological influences on regenerative success. Differentiation 87(1–2):66–75. doi: 10.1016/j.diff.2014.02.002 PubMedCrossRefGoogle Scholar
  59. Godwin JW, Pinto AR, Rosenthal NA (2013) Macrophages are required for adult salamander limb regeneration. Proc Natl Acad Sci U S A 110(23):9415–9420. doi: 10.1073/pnas.1300290110 PubMedPubMedCentralCrossRefGoogle Scholar
  60. Godwin J, Kuraitis D, Rosenthal N (2014) Extracellular matrix considerations for scar-free repair and regeneration: insights from regenerative diversity among vertebrates. Int J Biochem Cell Biol 56:47–55. doi: 10.1016/j.biocel.2014.10.011 PubMedCrossRefGoogle Scholar
  61. Gross J, Lapiere CM (1962) Collagenolytic activity in amphibian tissues: a tissue culture assay. Proc Natl Acad Sci U S A 48:1014–1022PubMedPubMedCentralCrossRefGoogle Scholar
  62. Haas HJ (1962) Studies on mechanisms of joint and bone formation in the skeleton rays of fish fins. Dev Biol 5:1–34PubMedCrossRefGoogle Scholar
  63. Halim S, Stone CA, Devaraj VS (1998) The Hyphecan cap: a biological fingertip dressing. Injury 29(4):261–263PubMedCrossRefGoogle Scholar
  64. Han MJ, An JY, Kim WS (2001) Expression patterns of Fgf-8 during development and limb regeneration of the axolotl. Dev Dyn 220(1):40–48. doi: 10.1002/1097-0177(2000)9999:9999<::AID-DVDY1085>3.0.CO;2-8 PubMedCrossRefGoogle Scholar
  65. Han M, Yang X, Taylor G et al (2005) Limb regeneration in higher vertebrates: developing a roadmap. Anat Rec B New Anat 287(1):14–24. doi: 10.1002/ar.b.20082 PubMedCrossRefGoogle Scholar
  66. Han M, Yang X, Lee J et al (2008) Development and regeneration of the neonatal digit tip in mice. Dev Biol 315(1):125–135. doi: 10.1016/j.ydbio.2007.12.025 PubMedPubMedCentralCrossRefGoogle Scholar
  67. Hardy S, Legagneux V, Audic Y et al (2012) Reverse genetics in eukaryotes. Biol Cell 102:561–580. doi: 10.1042/BC20100038 CrossRefGoogle Scholar
  68. Harty M, Neff AW, King MW et al (2003) Regeneration or scarring: an immunologic perspective. Dev Dyn 226(2):268–279. doi: 10.1002/dvdy.10239 PubMedCrossRefGoogle Scholar
  69. Hay ED, Fischman DA (1961) Origin of the blastema in regenerating limbs of the newt Triturus viridescens. An autoradiographic study using tritiated thymidine to follow cell proliferation and migration. Dev Biol 3:26–59PubMedCrossRefGoogle Scholar
  70. Hellsten U, Harland RM, Gilchrist MJ et al (2010) The genome of the Western clawed frog Xenopus tropicalis. Science 328(5978):633–636. doi: 10.1126/science.1183670 PubMedPubMedCentralCrossRefGoogle Scholar
  71. Hughes A, New D (1959) Tail regeneration in the geckonid lizard, Sphaerodactylus. J Embryol Exp Morphol 7:281–302PubMedGoogle Scholar
  72. Hui SP, Sengupta D, Lee SGP et al (2014) Genome wide expression profiling during spinal cord regeneration identifies comprehensive cellular responses in zebrafish. PLoS One 9(1), e84212. doi: 10.1371/journal.pone.0084212 PubMedPubMedCentralCrossRefGoogle Scholar
  73. Hutchins ED, Markov GJ, Eckalbar WL et al (2014) Transcriptomic analysis of tail regeneration in the lizard anolis carolinensis reveals activation of conserved vertebrate developmental and repair mechanisms. PLoS One 9, e105004. doi: 10.1371/journal.pone.0105004.s014 PubMedPubMedCentralCrossRefGoogle Scholar
  74. Hutchison C, Pilote M, Roy S (2007) The axolotl limb: a model for bone development, regeneration and fracture healing. Bone 40(1):45–56. doi: 10.1016/j.bone.2006.07.005 PubMedCrossRefGoogle Scholar
  75. Illingworth CM (1974) Trapped fingers and amputated finger tips in children. J Pediatr Surg 9(6):853–858PubMedCrossRefGoogle Scholar
  76. Iten LE, Bryant SV (1973) Forelimb regeneration from different levels of amputation in the newt, Notophthalmus viridescens: length, rate, and stages. Wilhelm Roux Arch Entwickl Mech Org 173(4):263–282. doi: 10.1007/BF00575834 CrossRefGoogle Scholar
  77. Kahn EB, Simpson SB Jr (1974) Satellite cells in mature, uninjured skeletal muscle of the lizard tail. Dev Biol 37(1):219–223PubMedCrossRefGoogle Scholar
  78. Kamrin RP, Singer M (1955) The influence of the spinal cord in regeneration of the tail of the lizard, Anolis carolinensis. J Exp Zool 128:611–627CrossRefGoogle Scholar
  79. Kato T, Miyazaki K, Shimizu-Nishikawa K et al (2003) Unique expression patterns of matrix metalloproteinases in regenerating newt limbs. Dev Dyn 226(2):366–376. doi: 10.1002/dvdy.10247 PubMedCrossRefGoogle Scholar
  80. Kawakami Y, Rodriguez Esteban C, Raya M et al (2006) Wnt/beta-catenin signaling regulates vertebrate limb regeneration. Genes Dev 20(23):3232–3237. doi: 10.1101/gad.1475106 PubMedPubMedCentralCrossRefGoogle Scholar
  81. Kim J, Kim J, Kim DW et al (2010) Wnt5a induces endothelial inflammation via -catenin-independent signaling. J Immunol 185:1274–1282. doi: 10.4049/jimmunol.1000181 PubMedCrossRefGoogle Scholar
  82. King MW, Neff AW, Mescher AL (2012) The developing Xenopus limb as a model for studies on the balance between inflammation and regeneration. Anat Rec (Hoboken) 295(10):1552–1561. doi: 10.1002/ar.22443 CrossRefGoogle Scholar
  83. Kizil C, Kaslin J, Kroehne V et al (2012) Adult neurogenesis and brain regeneration in zebrafish. Dev Neurobiol 72(3):429–461. doi: 10.1002/dneu.20918 PubMedCrossRefGoogle Scholar
  84. Knapp D, Schulz H, Rascon CA et al (2013) Comparative transcriptional profiling of the axolotl limb identifies a tripartite regeneration-specific gene program. PLoS One 8(5), e61352. doi: 10.1371/journal.pone.0061352.s011 PubMedPubMedCentralCrossRefGoogle Scholar
  85. Knopf F, Hammond C, Chekuru A et al (2011) Bone regenerates via dedifferentiation of osteoblasts in the zebrafish fin. Dev Cell 20(5):713–724. doi: 10.1016/j.devcel.2011.04.014 PubMedCrossRefGoogle Scholar
  86. Korneluk RG, Anderson MJ (1982) Stage dependency of forelimb regeneration on nerves in postmetamorphic froglets of Xenopus laevis. J Exp Zool 220(3):331–342CrossRefGoogle Scholar
  87. Korneluk RG, Liversage RA (1984) Tissue regeneration in the amputated forelimb of Xenopus laevis froglets. Can J Zool 62(12):2383–2391. doi: 10.1139/z84-351 CrossRefGoogle Scholar
  88. Kostakopoulou K, Vogel A, Brickell P et al (1996) “Regeneration” of wing bud stumps of chick embryos and reactivation of Msx-1 and Shh expression in response to FGF-4 and ridge signals. Mech Dev 55(2):119–131PubMedCrossRefGoogle Scholar
  89. Kragl M, Knapp D, Nacu E et al (2009) Cells keep a memory of their tissue origin during axolotl limb regeneration. Nature 460(7251):60–65. doi: 10.1038/nature08152 PubMedCrossRefGoogle Scholar
  90. Kumar A, Brockes JP (2012) Nerve dependence in tissue, organ, and appendage regeneration. Trends Neurosci 35(11):691–699. doi: 10.1016/j.tins.2012.08.003 PubMedCrossRefGoogle Scholar
  91. Kusumi K, Kulathinal RJ, Abzhanov A et al (2011) Developing a community-based genetic nomenclature for anole lizards. BMC Genomics 12(1):554. doi: 10.1186/1471-2164-12-554 PubMedPubMedCentralCrossRefGoogle Scholar
  92. Lander ES, Linton LM, Birren B et al (2001) Initial sequencing and analysis of the human genome. Nature 409:860–921. doi: 10.1038/35057062 PubMedCrossRefGoogle Scholar
  93. Lee L, Lau P, Chan C (1995) A simple and efficient treatment for fingertip injuries. J Hand Surg (Br) 20(1):63–71. doi: 10.1016/S0266-7681(05)80019-1 CrossRefGoogle Scholar
  94. Lee Y, Grill S, Sanchez A et al (2005) Fgf signaling instructs position-dependent growth rate during zebrafish fin regeneration. Development 132:5173–5183PubMedCrossRefGoogle Scholar
  95. Lee Y, Hami D, De Val S et al (2009) Maintenance of blastemal proliferation by functionally diverse epidermis in regenerating zebrafish fins. Dev Biol 331(2):270–280. doi: 10.1016/j.ydbio.2009.05.545 PubMedPubMedCentralCrossRefGoogle Scholar
  96. Lehoczky JA, Robert B, Tabin CJ (2011) Mouse digit tip regeneration is mediated by fate-restricted progenitor cells. Proc Natl Acad Sci U S A 108(51):20609–20614. doi: 10.1073/pnas.1118017108 PubMedPubMedCentralCrossRefGoogle Scholar
  97. Lin G, Chen Y, Slack JMW (2013) Imparting regenerative capacity to limbs by progenitor cell transplantation. Dev Cell 24(1):41–51. doi: 10.1016/j.devcel.2012.11.017 PubMedPubMedCentralCrossRefGoogle Scholar
  98. Looso M, Preussner J, Sousounis K et al (2013) A de novo assembly of the newt transcriptome combined with proteomic validation identifies new protein families expressed during tissue regeneration. Genome Biol 14:R16. doi: 10.1186/gb-2013-14-2-r16 PubMedPubMedCentralCrossRefGoogle Scholar
  99. Love NR, Chen Y, Bonev B et al (2011) Genome-wide analysis of gene expression during Xenopus tropicalis tadpole tail regeneration. BMC Dev Biol 11(1):70. doi: 10.1186/1471-213X-11-70 PubMedPubMedCentralCrossRefGoogle Scholar
  100. Lovern MB, Wade J (2003) Yolk testosterone varies with sex in eggs of the lizard, Anolis carolinensis. J Exp Zool A Comp Exp Biol 295(2):206–210. doi: 10.1002/jez.a.10225 PubMedCrossRefGoogle Scholar
  101. Lozito TP, Tuan RS (2015) Lizard tail regeneration: regulation of two distinct cartilage regions by Indian hedgehog. Dev Biol 399(2):249–262. doi: 10.1016/j.ydbio.2014.12.036 PubMedCrossRefGoogle Scholar
  102. Lucas T, Waisman A, Ranjan R et al (2010) Differential roles of macrophages in diverse phases of skin repair. J Immunol 184(7):3964–3977. doi: 10.4049/jimmunol.0903356 PubMedCrossRefGoogle Scholar
  103. Maden M, Manwell LA, Ormerod BK (2013) Proliferation zones in the axolotl brain and regeneration of the telencephalon. Neural Dev 8(1):1. doi: 10.1186/1749-8104-8-1 PubMedPubMedCentralCrossRefGoogle Scholar
  104. Maderson PF, Licht P (1968) Factors influencing rates of tail regeneration in the lizard Anolis carolinensis. Experientia 24(10):1083–1086PubMedCrossRefGoogle Scholar
  105. Makanae A, Mitogawa K, Satoh A (2014) Co-operative Bmp- and Fgf-signaling inputs convert skin wound healing to limb formation in urodele amphibians. Dev Biol 396(1):57–66. doi: 10.1016/j.ydbio.2014.09.021 PubMedCrossRefGoogle Scholar
  106. Makino S, Whitehead GG, Lien CL et al (2005) Heat-shock protein 60 is required for blastema formation and maintenance during regeneration. Proc Natl Acad Sci U S A 102(41):14599–14604. doi: 10.1073/pnas.0507408102 PubMedPubMedCentralCrossRefGoogle Scholar
  107. Martini R, Fischer S, López-Vales R et al (2008) Interactions between Schwann cells and macrophages in injury and inherited demyelinating disease. Glia 56(14):1566–1577. doi: 10.1002/glia.20766 PubMedCrossRefGoogle Scholar
  108. McLean KE, Vickaryous MK (2011) A novel amniote model of epimorphic regeneration: the leopard gecko, Eublepharis macularius. BMC Dev Biol 11(1):50. doi: 10.1186/1471-213X-11-50 PubMedPubMedCentralCrossRefGoogle Scholar
  109. Mercer SE, Cheng C-H, Atkinson DL et al (2012) Multi-tissue microarray analysis identifies a molecular signature of regeneration. PLoS One 7(12), e52375. doi: 10.1371/journal.pone.0052375 PubMedPubMedCentralCrossRefGoogle Scholar
  110. Mercola M (2012) Cardiovascular biology: a boost for heart regeneration. Nature 492(7429):360–362. doi: 10.1038/nature11763 PubMedCrossRefGoogle Scholar
  111. Mescher AL (1996) The cellular basis of limb regeneration in urodeles. Int J Dev Biol 40(4):785–795PubMedGoogle Scholar
  112. Mescher AL, Neff AW (2006) Limb regeneration in amphibians: immunological considerations. Sci World J 6(Suppl 1):1–11. doi: 10.1100/tsw.2006.323 CrossRefGoogle Scholar
  113. Mihaylova Y, Aboobaker AA (2013) What is it about ‘eye of newt’? Genome Biol 14:106. doi: 10.1186/1741-7007-10-103 PubMedPubMedCentralCrossRefGoogle Scholar
  114. Mohammad KS, Neufeld DA (2000) Denervation retards but does not prevent toetip regeneration. Wound Repair Regen 8(4):277–281PubMedCrossRefGoogle Scholar
  115. Mohammad KS, Day FA, Neufeld DA (1999) Bone growth is induced by nail transplantation in amputated proximal phalanges. Calcif Tissue Int 65(5):408–410PubMedCrossRefGoogle Scholar
  116. Monaghan JR, Epp LG, Putta S et al (2009) Microarray and cDNA sequence analysis of transcription during nerve-dependent limb regeneration. BMC Biol 7(1):1. doi: 10.1186/1741-7007-7-1 PubMedPubMedCentralCrossRefGoogle Scholar
  117. Monaghan JR, Athippozhy A, Seifert AW et al (2012) Gene expression patterns specific to the regenerating limb of the Mexican axolotl. Biol Open 1(10):937–948. doi: 10.1242/bio.20121594 PubMedPubMedCentralCrossRefGoogle Scholar
  118. Montuelle SJ, Herrel A, Libourel P-A et al (2009) Locomotor-feeding coupling during prey capture in a lizard (Gerrhosaurus major): effects of prehension mode. J Exp Biol 212(Pt 6):768–777. doi: 10.1242/jeb.026617 PubMedCrossRefGoogle Scholar
  119. Morrison JI, Lööf S, He P et al (2006) Salamander limb regeneration involves the activation of a multipotent skeletal muscle satellite cell population. J Cell Biol 172(3):433–440. doi: 10.1083/jcb.200509011 PubMedPubMedCentralCrossRefGoogle Scholar
  120. Morrison JI, Borg P, Simon A (2010) Plasticity and recovery of skeletal muscle satellite cells during limb regeneration. FASEB J 24(3):750–756. doi: 10.1096/fj.09-134825 PubMedCrossRefGoogle Scholar
  121. Muneoka K, Bryant SV (1982) Evidence that patterning mechanisms in developing and regenerating limbs are the same. Nature 298(5872):369–371PubMedCrossRefGoogle Scholar
  122. Muneoka K, Allan CH, Yang X et al (2008) Mammalian regeneration and regenerative medicine. Birth Defects Res C Embryo Today 84(4):265–280. doi: 10.1002/bdrc.20137 PubMedCrossRefGoogle Scholar
  123. Murawala P, Tanaka EM, Currie JD (2012) Regeneration: the ultimate example of wound healing. Semin Cell Dev Biol 23(9):954–962. doi: 10.1016/j.semcdb.2012.09.013 PubMedCrossRefGoogle Scholar
  124. Nabrit SM (1929) The rôle of the fin rays in the regeneration in the tail-fins of fishes in fundulus and goldfish. Biol Bull 56(4):235–266CrossRefGoogle Scholar
  125. Nacu E, Tanaka EM (2011) Limb regeneration: a new development? Annu Rev Cell Dev Biol 27(1):409–440. doi: 10.1146/annurev-cellbio-092910-154115 PubMedCrossRefGoogle Scholar
  126. Nambiar VV, Bhatt IY, Deshmukh PA et al (2008) Assessment of extracellular matrix remodeling during tail regeneration in the lizard Hemidactylus flaviviridis. J Endocrinol 12(2):67–72Google Scholar
  127. Namenwirth M (1974) The inheritance of cell differentiation during limb regeneration in the axolotl. Dev Biol 41(1):42–56PubMedCrossRefGoogle Scholar
  128. Neale DB, Wegrzyn JL, Stevens KA et al (2014) Decoding the massive genome of loblolly pine using haploid DNA and novel assembly strategies. Genome Biol 15(3):R59. doi: 10.1186/gb-2014-15-3-r59 PubMedPubMedCentralCrossRefGoogle Scholar
  129. Nechiporuk A, Poss KD, Johnson SL et al (2003) Positional cloning of a temperature-sensitive mutant emmental reveals a role for sly1 during cell proliferation in zebrafish fin regeneration. Dev Biol 258(2):291–306PubMedCrossRefGoogle Scholar
  130. Neufeld DA, Zhao W (1995) Bone regrowth after digit tip amputation in mice is equivalent in adults and neonates. Wound Repair Regen 3(4):461–466. doi: 10.1046/j.1524-475X.1995.30410.x PubMedCrossRefGoogle Scholar
  131. Nucera S, Biziato D, De Palma M (2011) The interplay between macrophages and angiogenesis in development, tissue injury and regeneration. Int J Dev Biol 55(4–5):495–503. doi: 10.1387/ijdb.103227sn PubMedCrossRefGoogle Scholar
  132. Ogai K, Nakatani K, Hisano S et al (2014) Function of Sox2 in ependymal cells of lesioned spinal cords in adult zebrafish. Neurosci Res 88:84–87. doi: 10.1016/j.neures.2014.07.010 PubMedCrossRefGoogle Scholar
  133. Ohgo S, Itoh A, Suzuki M et al (2010) Analysis of hoxa11 and hoxa13 expression during patternless limb regeneration in Xenopus. Dev Biol 338(2):148–157. doi: 10.1016/j.ydbio.2009.11.026 PubMedCrossRefGoogle Scholar
  134. Otteson DC, Hitchcock PF (2003) Stem cells in the teleost retina: persistent neurogenesis and injury-induced regeneration. Vision Res 43(8):927–936PubMedCrossRefGoogle Scholar
  135. Paiva KBS, Granjeiro JM (2014) Bone tissue remodeling and development: focus on matrix metalloproteinase functions. Arch Biochem Biophys 561:74–87. doi: 10.1016/j.abb.2014.07.034 PubMedCrossRefGoogle Scholar
  136. Park JE, Barbul A (2004) Understanding the role of immune regulation in wound healing. Am J Surg 187(5A):11S–16S. doi: 10.1016/S0002-9610(03)00296-4 PubMedCrossRefGoogle Scholar
  137. Peadon AM, Singer M (1966) The blood vessels of the regenerating limb of the adult newt, Triturus. J Morphol 118(1):79–89. doi: 10.1002/jmor.1051180106 PubMedCrossRefGoogle Scholar
  138. Poss KD, Shen J, Nechiporuk A et al (2000) Roles for Fgf signaling during zebrafish fin regeneration. Dev Biol 222(2):347–358. doi: 10.1006/dbio.2000.9722 PubMedCrossRefGoogle Scholar
  139. Poss KD, Wilson LG, Keating MT (2002) Heart regeneration in zebrafish. Science 298(5601):2188–2190. doi: 10.1126/science.1077857 PubMedCrossRefGoogle Scholar
  140. Pyron RA (2010) A likelihood method for assessing molecular divergence time estimates and the placement of fossil calibrations. Syst Biol 59:185–194. doi: 10.1093/sysbio/syp090 PubMedCrossRefGoogle Scholar
  141. Reimer MM, Sörensen I, Kuscha V (2008) Motor neuron regeneration in adult zebrafish. J Neurosci 28(34):8510–8516. doi: 10.1523/JNEUROSCI.1189-08.2008 PubMedCrossRefGoogle Scholar
  142. Revardel JL, Chebouki F (1987) Étude de la réponse l’amputation des phalanges chez la souris: rôle morphogénétique des épithéliums, stimulation de la chondrogense. Can J Zool 65(12):3166–3176CrossRefGoogle Scholar
  143. Rinkevich Y, Lindau P, Ueno H et al (2011) Germ-layer and lineage-restricted stem/progenitors regenerate the mouse digit tip. Nature 476(7361):409–413. doi: 10.1038/nature10346 PubMedCrossRefGoogle Scholar
  144. Ritzman TB, Stroik LK, Julik E et al (2012) The gross anatomy of the original and regenerated tail in the green anole (Anolis carolinensis). Anat Rec (Hoboken) 295(10):1596–1608. doi: 10.1002/ar.22524 CrossRefGoogle Scholar
  145. Roy S, Gardiner DM (2002) Cyclopamine induces digit loss in regenerating axolotl limbs. J Exp Zool 293(2):186–190. doi: 10.1002/jez.10110 PubMedCrossRefGoogle Scholar
  146. Roy S, Gardiner DM, Bryant SV (2000) Vaccinia as a tool for functional analysis in regenerating limbs: ectopic expression of Shh. Dev Biol 218(2):199–205. doi: 10.1006/dbio.1999.9556 PubMedCrossRefGoogle Scholar
  147. Ruffell D, Mourkioti F, Gambardella A et al (2009) A CREB-C/EBPbeta cascade induces M2 macrophage-specific gene expression and promotes muscle injury repair. Proc Natl Acad Sci U S A 106(41):17475–17480. doi: 10.1073/pnas.0908641106 PubMedPubMedCentralCrossRefGoogle Scholar
  148. Ryffel GU (2003) Tagging muscle cell lineages in development and tail regeneration using Cre recombinase in transgenic Xenopus. Nucleic Acids Res 31(8):44e–44. doi: 10.1093/nar/gng044 CrossRefGoogle Scholar
  149. Said S, Parke W, Neufeld DA (2004) Vascular supplies differ in regenerating and nonregenerating amputated rodent digits. Anat Rec A: Discov Mol Cell Evol Biol 278(1):443–449. doi: 10.1002/ar.a.20034 CrossRefGoogle Scholar
  150. Sandoval-Guzmán T, Wang H, Khattak S et al (2014) Fundamental differences in dedifferentiation and stem cell recruitment during skeletal muscle regeneration in two salamander species. Cell Stem Cell 14(2):174–187. doi: 10.1016/j.stem.2013.11.007 PubMedCrossRefGoogle Scholar
  151. Sanger TJ, Losos JB, Gibson-Brown JJ (2008) A developmental staging series for the lizard genus Anolis: a new system for the integration of evolution, development, and ecology. J Morphol 269:129–137. doi: 10.1002/jmor.10563 PubMedCrossRefGoogle Scholar
  152. Santamaría JA, Becerra J (1991) Tail fin regeneration in teleosts: cell-extracellular matrix interaction in blastemal differentiation. J Anat 176:9–21PubMedPubMedCentralGoogle Scholar
  153. Satoh A, Ide H, Tamura K (2005) Muscle formation in regenerating Xenopus froglet limb. Dev Dyn 233(2):337–346. doi: 10.1002/dvdy.20349 PubMedCrossRefGoogle Scholar
  154. Satoh A, Endo T, Abe M et al (2006) Characterization of Xenopus digits and regenerated limbs of the froglet. Dev Dyn 235(12):3316–3326. doi: 10.1002/dvdy.20985 PubMedCrossRefGoogle Scholar
  155. Satoh A, Graham GMC, Bryant SV et al (2008) Neurotrophic regulation of epidermal dedifferentiation during wound healing and limb regeneration in the axolotl (Ambystoma mexicanum). Dev Biol 319(2):321–335. doi: 10.1016/j.ydbio.2008.04.030 PubMedCrossRefGoogle Scholar
  156. Satoh A, James MA, Gardiner DM (2009) The role of nerve signaling in limb genesis and agenesis during axolotl limb regeneration. J Bone Joint Surg Am 91(Suppl 4):90–98. doi: 10.2106/JBJS.I.00159 PubMedCrossRefGoogle Scholar
  157. Satoh A, Makanae A, Hirata A et al (2011) Blastema induction in aneurogenic state and Prrx-1 regulation by MMPs and FGFs in Ambystoma mexicanum limb regeneration. Dev Biol 355(2):263–274. doi: 10.1016/j.ydbio.2011.04.017 PubMedCrossRefGoogle Scholar
  158. Satoh A, Bryant SV, Gardiner DM (2012) Nerve signaling regulates basal keratinocyte proliferation in the blastema apical epithelial cap in the axolotl (Ambystoma mexicanum). Dev Biol 366(2):374–381. doi: 10.1016/j.ydbio.2012.03.022 PubMedCrossRefGoogle Scholar
  159. Seifert AW, Kiama SG, Seifert MG et al (2012) Skin shedding and tissue regeneration in African spiny mice (Acomys). Nature 489(7417):561–565. doi: 10.1038/nature11499 PubMedPubMedCentralCrossRefGoogle Scholar
  160. Shedlock AM, Edwards SV (2009) Amniotes (Amniota). In: Hedges SB, Kumar S (eds) The timetree of life. Oxford University Press, Oxford, pp 375–379Google Scholar
  161. Simpson SB Jr (1964) Analysis of tail regeneration in the lizard Lygosoma laterale. i. Initiation of regeneration and cartilage differentiation: the role of ependyma. J Morphol 114:425–435. doi: 10.1002/jmor.1051140305 PubMedCrossRefGoogle Scholar
  162. Simpson SB Jr (1968) Morphology of the regenerated spinal cord in the lizard, Anolis carolinensis. J Comp Neurol 134(2):193–210. doi: 10.1002/cne.901340207 PubMedCrossRefGoogle Scholar
  163. Simpson SB Jr (1970) Studies on regeneration of the lizard’s tail. Am Zool 10:157–165PubMedCrossRefGoogle Scholar
  164. Singer M (1974) Trophic functions of the neuron. VI. Other trophic systems. Neurotrophic control of limb regeneration in the newt. Ann N Y Acad Sci 228:308–322PubMedCrossRefGoogle Scholar
  165. Singer M, Weckesser EC, Géraudie J et al (1987) Open finger tip healing and replacement after distal amputation in rhesus monkey with comparison to limb regeneration in lower vertebrates. Anat Embryol 177(1):29–36PubMedCrossRefGoogle Scholar
  166. Singh SP, Holdway JE, Poss KD (2012) Regeneration of amputated zebrafish fin rays from de novo osteoblasts. Dev Cell 22(4):879–886. doi: 10.1016/j.devcel.2012.03.006 PubMedPubMedCentralCrossRefGoogle Scholar
  167. Slack JMW, Lin G, Chen Y (2007) Molecular and cellular basis of regeneration and tissue repair. Cell Mol Life Sci 65(1):54–63. doi: 10.1007/s00018-007-7431-1 CrossRefGoogle Scholar
  168. Smith AR, Wolpert L (1975) Nerves and angiogenesis in amphibian limb regeneration. Nature 257(5523):224–225PubMedCrossRefGoogle Scholar
  169. Sousa S, Afonso N, Bensimon-Brito A et al (2011) Differentiated skeletal cells contribute to blastema formation during zebrafish fin regeneration. Development 138(18):3897–3905. doi: 10.1242/dev.064717 PubMedCrossRefGoogle Scholar
  170. Stefater JA, Ren S, Lang RA et al (2011) Metchnikoff’s policemen: macrophages in development, homeostasis and regeneration. Trends Mol Med 17(12):743–752. doi: 10.1016/j.molmed.2011.07.009 PubMedPubMedCentralCrossRefGoogle Scholar
  171. Stewart S, Stankunas K (2012) Limited dedifferentiation provides replacement tissue during zebrafish fin regeneration. Dev Biol 365(2):339–349. doi: 10.1016/j.ydbio.2012.02.031 PubMedPubMedCentralCrossRefGoogle Scholar
  172. Stewart R, Rascon CA, Tian S et al (2013) Comparative RNA-seq analysis in the unsequenced axolotl: the oncogene burst highlights early gene expression in the blastema. PLoS Comput Biol 9(3), e1002936. doi: 10.1371/journal.pcbi.1002936 PubMedPubMedCentralCrossRefGoogle Scholar
  173. Stocum DL, Cameron JA (2011) Looking proximally and distally: 100 years of limb regeneration and beyond. Dev Dyn 240(5):943–968. doi: 10.1002/dvdy.22553 PubMedCrossRefGoogle Scholar
  174. Stoick-Cooper CL, Weidinger G, Riehle KJ et al (2006) Distinct Wnt signaling pathways have opposing roles in appendage regeneration. Development 134(3):479–489. doi: 10.1242/dev.001123 PubMedCrossRefGoogle Scholar
  175. Sugiura T, Tazaki A, Ueno N (2009) Xenopus Wnt-5a induces an ectopic larval tail at injured site, suggesting a crucial role for noncanonical Wnt signal in tail regeneration. Mech Dev 126(1–2):56–67. doi: 10.1016/j.mod.2008.10.002 PubMedCrossRefGoogle Scholar
  176. Suzuki M, Satoh A, Ide H et al (2005) Nerve-dependent and -independent events in blastema formation during Xenopus froglet limb regeneration. Dev Biol 286(1):361–375. doi: 10.1016/j.ydbio.2005.08.021 PubMedCrossRefGoogle Scholar
  177. Takeo M, Chou WC, Sun Q et al (2013) Wnt activation in nail epithelium couples nail growth to digit regeneration. Nature 499(7457):228–232. doi: 10.1038/nature12214 PubMedPubMedCentralCrossRefGoogle Scholar
  178. Takeo M, Lee W, Ito M (2015) Wound healing and skin regeneration. Cold Spring Harb Perspect Med 5(1):a023267. doi: 10.1101/cshperspect.a023267 PubMedCrossRefGoogle Scholar
  179. Tanaka EM, Reddien PW (2011) The cellular basis for animal regeneration. Dev Cell 21(1):172–185. doi: 10.1016/j.devcel.2011.06.016 PubMedPubMedCentralCrossRefGoogle Scholar
  180. Thornton CS (1938) The histogenesis of the regenerating fore limb of larval Ambystoma after exarticulation of the humerus. J Morphol 62(2):219–241. doi: 10.1002/jmor.1050620204 CrossRefGoogle Scholar
  181. Tidball JG, Wehling-Henricks M (2007) Macrophages promote muscle membrane repair and muscle fibre growth and regeneration during modified muscle loading in mice in vivo. J Physiol 578(Pt 1):327–336. doi: 10.1113/jphysiol.2006.118265 PubMedPubMedCentralCrossRefGoogle Scholar
  182. Tollis M, Boissinot S (2014) Genetic variation in the green anole lizard (Anolis carolinensis) reveals island refugia and a fragmented Florida during the quaternary. Genetica 142(1):59–72. doi: 10.1007/s10709-013-9754-1 PubMedPubMedCentralCrossRefGoogle Scholar
  183. Tollis M, Hutchins ED, Kusumi K (2015) Reptile genomes open the frontier for comparative analysis of amniote development and regeneration. Int J Dev Biol (in press)Google Scholar
  184. Torok MA, Gardiner DM, Shubin NH et al (1998) Expression of HoxD genes in developing and regenerating axolotl limbs. Dev Biol 200(2):225–233. doi: 10.1006/dbio.1998.8956 PubMedCrossRefGoogle Scholar
  185. Tu S, Johnson SL (2011) Fate restriction in the growing and regenerating zebrafish fin. Dev Cell 20:725–732. doi: 10.1016/j.devcel.2011.04.013 PubMedPubMedCentralCrossRefGoogle Scholar
  186. Turner JE, Singer M (1973) Some morphological and ultrastructural changes in the ependyma of the amputation stump during early regeneration of the tail in the lizard, Anolis carolinensis. J Morphol 140(3):257–269. doi: 10.1002/jmor.1051400302 CrossRefGoogle Scholar
  187. Vidal P, Dickson MG (1993) Regeneration of the distal phalanx. A case report. J Hand Surg Eur 18(2):230–233CrossRefGoogle Scholar
  188. Vinarsky V, Atkinson DL, Stevenson TJ et al (2005) Normal newt limb regeneration requires matrix metalloproteinase function. Dev Biol 279(1):86–98. doi: 10.1016/j.ydbio.2004.12.003 PubMedCrossRefGoogle Scholar
  189. Wade J (2012) Sculpting reproductive circuits: relationships among hormones, morphology and behavior in anole lizards. Gen Comp Endocrinol 176(3):456–460. doi: 10.1016/j.ygcen.2011.12.011 PubMedCrossRefGoogle Scholar
  190. Wallace BM, Wallace H (1973) Participation of grafted nerves in amphibian limb regeneration. J Embryol Exp Morphol 29(3):559–570PubMedGoogle Scholar
  191. Wallis JW, Aerts J, Groenen M et al (2004) A physical map of the chicken genome. Nature 432:761–764PubMedCrossRefGoogle Scholar
  192. Wang Y, Wang R, Jiang S et al (2011) Gecko CD59 is implicated in proximodistal identity during tail regeneration. PLoS One 6(3), e17878. doi: 10.1371/journal.pone.0017878.g008 PubMedPubMedCentralCrossRefGoogle Scholar
  193. Wehner D, Cizelsky W, Vasudevaro MD et al (2014) Wnt/b-catenin signaling defines organizing centers that orchestrate growth and differentiation of the regenerating zebrafish caudal fin. Cell Rep 6(3):467–481. doi: 10.1016/j.celrep.2013.12.036 PubMedCrossRefGoogle Scholar
  194. Whimster IW (1978) Nerve supply as a stimulator of the growth of tissues including skin. Clin Exp Dermatol 3(4):389–410PubMedCrossRefGoogle Scholar
  195. Whitehead GG, Makino S, Lien C-L et al (2005) fgf20 is essential for initiating zebrafish fin regeneration. Science 310(5756):1957–1960. doi: 10.1126/science.1117637 PubMedCrossRefGoogle Scholar
  196. Wordley C, Slate J, Stapley J (2011) Mining online genomic resources in Anolis carolinensis facilitates rapid and inexpensive development of cross-species microsatellite markers for the Anolis lizard genus. Mol Ecol Resour 11(1):126–133. doi: 10.1111/j.1755-0998.2010.02863.x PubMedCrossRefGoogle Scholar
  197. Wu C-H, Tsai M-H, Ho C-C et al (2013) De novo transcriptome sequencing of axolotl blastema for identification of differentially expressed genes during limb regeneration. BMC Genomics 14(1):1–1. doi: 10.1186/1471-2164-14-434 CrossRefGoogle Scholar
  198. Yakushiji N, Suzuki M, Satoh A et al (2007) Correlation between Shh expression and DNA methylation status of the limb-specific Shh enhancer region during limb regeneration in amphibians. Dev Biol 312(1):171–182. doi: 10.1016/j.ydbio.2007.09.022 PubMedCrossRefGoogle Scholar
  199. Yang EV, Bryant SV (1994) Developmental regulation of a matrix metalloproteinase during regeneration of axolotl appendages. Dev Biol 166(2):696–703PubMedCrossRefGoogle Scholar
  200. Yang EV, Gardiner DM, Carlson MR et al (1999) Expression of Mmp-9 and related matrix metalloproteinase genes during axolotl limb regeneration. Dev Dyn 216(1):2–9. doi: 10.1002/(SICI)1097-0177(199909)216:1<2::AID-DVDY2>3.0.CO;2-P PubMedCrossRefGoogle Scholar
  201. Yokoyama H (2008) Initiation of limb regeneration: the critical steps for regenerative capacity. Dev Growth Differ 50(1):13–22. doi: 10.1111/j.1440-169X.2007.00973.x PubMedCrossRefGoogle Scholar
  202. Yokoyama H, Ogino H, Stoick-Cooper CL et al (2007) Wnt/β-catenin signaling has an essential role in the initiation of limb regeneration. Dev Biol 306(1):170–178. doi: 10.1016/j.ydbio.2007.03.014 PubMedPubMedCentralCrossRefGoogle Scholar
  203. Yokoyama H, Maruoka T, Ochi H et al (2011) Different requirement for Wnt/β-catenin signaling in limb regeneration of larval and adult Xenopus. PLoS One 6(7), e21721. doi: 10.1371/journal.pone.0021721 PubMedPubMedCentralCrossRefGoogle Scholar
  204. Zhang Q, Sakamoto K, Wagner K-U (2014) D-type cyclins are important downstream effectors of cytokine signaling that regulate the proliferation of normal and neoplastic mammary epithelial cells. Mol Cell Endocrinol 382(1):583–592. doi: 10.1016/j.mce.2013.03.016 PubMedCrossRefGoogle Scholar
  205. Zika JM (1969) A histological study of the regenerative response in a lizard, Anolis carolinensis. J Exp Zool 172(1):1–8. doi: 10.1002/jez.1401720102 PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.School of Life SciencesArizona State UniversityTempeUSA

Personalised recommendations

Cite chapter

Buy options