Abstract
Regeneration is the process of regrowth of an injured/missing tissue/organ from the residual tissue. One outstanding example is the regeneration of tail in lizards in which they can completely regenerate without the formation of scaring or fibrotic tissue. This study presents an analysis of the main differences between a mature regenerated tail and the original tail of the lizard Podarcis bocagei by comparing histological biomarkers for support structures, morphology and pigmentation, vasculature and energy storage. Matured regenerated and original tails were studied with different histological staining’s and immunohistochemistry to highlight the various tissue components. We found differences in the morphological features scalation pattern and pigmentation, as well as in the support structures: muscle organization, collagen and calcification. Vasculature was remodeled. Energy storage was restored with regeneration maintaining therefore the main metabolic function. We demonstrate that the regenerated tail does not lose its main functions like locomotion and energy metabolism. The present findings may open a new window of research with implications in regenerative medicine.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Alibardi L (1995) Development of the axial cartilaginous skeleton in the regenerating tail of lizards. Bull Assoc Anat 79:3–9
Alibardi L (2014) Histochemical, Biochemical and Cell Biological aspects of tail regeneration in lizard, an amniote model for studies on tissue regeneration. Prog Histochem Cytochem 48(4):143–244. https://doi.org/10.1016/j.proghi.2013.12.001
Alibardi L (2015) Regeneration of articular cartilage in lizard knee from resident stem/progenitor cells. Int J Mol Sci 16:20731–20747. https://doi.org/10.3390/ijms160920731
Alibardi L, Lovicu FJ (2010) Immunolocalization of FGF1 and FGF2 in the regenerating tail of the lizard Lampropholis guichenoti: implications for FGFs as trophic factors in lizard tail regeneration. Acta Histochem 112:459–473. https://doi.org/10.1016/j.acthis.2009.05.006
Alibardi L, Toni M (2005) Wound keratins in the regenerating epidermis of lizard suggest that the wound reaction is similar in the tail and limb. J Exp Zool Part A Comp Exp Biol 303:845–860. https://doi.org/10.1002/jez.a.213
Beazley LD, Sheard PW, Tennant M et al (1997) Optic nerve regenerates but does not restore topographic projections in the lizard Ctenophorus ornatus. J Comp Neurol 120:105–120. https://doi.org/10.1002/(SICI)1096-9861(19970106)377:1%3c105:AID-CNE10%3e3.0.CO;2-P
Bellairs A, Bryant SV (1985) Autotomy and regeneration in reptiles. Biol Reptil 15:301–410
Boozalis TS, LaSalle LT, Davis JR (2012) Morphological and biochemical analyses of original and regenerated lizard tails reveal variation in protein and lipid composition. Comp Biochem Physiol A Mol Integr Physiol 161:77–82. https://doi.org/10.1016/j.cbpa.2011.09.004
Carpenter AE, Jones TR, Lamprecht MR et al (2006) Cell profiler: image analysis software for identifying and quantifying cell phenotypes. Genome Biol 7:R100. https://doi.org/10.1186/gb-2006-7-10-r100
Cox PG (1969) Some aspects of tail regeneration in the lizard, Anolis carolinensis I. A description based on histology and autoradiography. J Exp Zool 171:127–149. https://doi.org/10.1002/jez.1401710202
Delorme SL, Lungu IM, Vickaryous MK (2012) Scar-free wound healing and regeneration following tail loss in the leopard gecko, Eublepharis macularius. Anat Rec 295:1575–1595. https://doi.org/10.1002/ar.22490
Egar M, Simpson SB, Singer M (1970) The growth and differentiation of the regenerating spinal cord of the lizard, Anolis carolinensis. J Morphol 131:131–151. https://doi.org/10.1002/jmor.1051310202
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 295:1609–1619. https://doi.org/10.1002/ar.22537
Font E, García-Verdugo JM, Alcántara S, López-García C (1991) Neuron regeneration reverses 3-acetylpyridine-induced cell loss in the cerebral cortex of adult lizards. Brain Res 551:230–235. https://doi.org/10.1016/0006-8993(91)90937-Q
Font E, Desfilis E, Pérez-Cañellas M et al (1997) 3-Acetylpyridine-induced degeneration and regeneration in the adult lizard brain: a qualitative and quantitative analysis. Brain Res 754:245–259. https://doi.org/10.1016/S0006-8993(97)00085-1
Golub EE, Boesze-Battaglia K (2007) The role of alkaline phosphatase in mineralization. Curr Opin Orthop 18:444–448. https://doi.org/10.1097/BCO.0b013e3282630851
Hopwood D (1977) Histopathologic technic and practical histochemistry (4th edition). Biochem Soc Trans. https://doi.org/10.1042/bst0050558a
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. https://doi.org/10.1371/journal.pone.0105004
Jacyniak K, McDonald RP, Vickaryous MK (2017) Tail regeneration and other phenomena of wound healing and tissue restoration in lizards. J Exp Biol 220:2858–2869. https://doi.org/10.1242/jeb.126862
Lozito TP, Tuan RS (2016) Lizard tail skeletal regeneration combines aspects of fracture healing and blastema-based regeneration. Development 143:2946–2957. https://doi.org/10.1242/dev.129585
Lozito TP, Tuan RS (2017) Lizard tail regeneration as an instructive model of enhanced healing capabilities in an adult amniote. Connect Tissue Res 58:145–154. https://doi.org/10.1080/03008207.2016.1215444
Maginnis TL (2006) The costs of autotomy and regeneration in animals: a review and framework for future research. Behav Ecol 17:857–872. https://doi.org/10.1093/beheco/arl010
Noble GK, Bradley HT (1933) The effect of temperature on the scale form of regenerated lizard skin. J Exp Zool 65:1–16. https://doi.org/10.1002/jez.1400650102
Peacock HM, Gilbert EAB, Vickaryous MK (2015) Scar-free cutaneous wound healing in the leopard gecko, Eublepharis macularius. J Anat 227:596–610. https://doi.org/10.1111/joa.12368
Reinke JM, Sorg H (2012) Wound repair and regeneration. Eur Surg Res 49:35–43. https://doi.org/10.1159/000339613
Rodriguez-Carballo E, Gámez B, Sedó-Cabezón L et al (2014) The p38α MAPK function in osteoprecursors is required for bone formation and bone homeostasis in adult mice. PLoS One 9:e102032. https://doi.org/10.1371/journal.pone.0102032
Schindelin J, Rueden CT, Hiner MC, Eliceiri KW (2015) The ImageJ ecosystem: an open platform for biomedical image analysis. Mol Reprod Dev 82:518–529
Simpson SB (1968) Morphology of the regenerated spinal cord in the lizard, Anolis carolinensis. J Comp Neurol 134:193–209. https://doi.org/10.1002/cne.901340207
Simpson SB (1970) Studies on regeneration of the lizard’s tail. Integr Comp Biol 10:157–165. https://doi.org/10.1093/icb/10.2.157
Tokuyama MA, Xu C, Fisher RE et al (2018) Developmental and adult-specific processes contribute to de novo neuromuscular regeneration in the lizard tail. Dev Biol 433:287–296. https://doi.org/10.1016/j.ydbio.2017.10.003
Tseng AS, Adams DS, Qiu D et al (2007) Apoptosis is required during early stages of tail regeneration in Xenopus laevis. Dev Biol 301:62–69. https://doi.org/10.1016/j.ydbio.2006.10.048
Wu P, Alibardi L, Chuong C-M (2014) Regeneration of reptilian scales after wounding: neogenesis, regional difference, and molecular modules. Regeneration 1:15–26. https://doi.org/10.1002/reg2.9
Acknowledgements
The authors would like to thank Catarina Pinho and Antigoni Kaliontzopoulou from CIBIO-InBIO, Research Center in Biodiversity and Genetic Resources, Portugal, for providing samples of original and regenerative tails of P. bocagei. This work was supported by FCT—Fundação para a Ciência e Tecnologia (REF UID/BIM/04293/2013); by the project (NORTE-01-0145-FEDER-000012) funded by COMPETE and Fundo Social Europeu; and by a scholarship (Ref. SAICT2016/FEDER/BIO4DIA/BTI).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
There is no conflict of interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Luís, C., Rodrigues, I., Guerreiro, S.G. et al. Regeneration in the Podarcis bocagei model organism: a comprehensive immune-/histochemical analysis of the tail. Zoomorphology 138, 399–407 (2019). https://doi.org/10.1007/s00435-019-00452-6
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00435-019-00452-6