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Regeneration in the Podarcis bocagei model organism: a comprehensive immune-/histochemical analysis of the tail

  • Carla LuísEmail author
  • Ilda Rodrigues
  • Susana G. Guerreiro
  • Rúben Fernandes
  • Raquel Soares
Original Paper

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.

Keywords

Tail regeneration Histology Lizards Podarcis bocagei Regenerative medicine 

Notes

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).

Compliance with ethical standards

Conflict of interest

There is no conflict of interests.

References

  1. Alibardi L (1995) Development of the axial cartilaginous skeleton in the regenerating tail of lizards. Bull Assoc Anat 79:3–9Google Scholar
  2. 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 CrossRefGoogle Scholar
  3. 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 CrossRefGoogle Scholar
  4. 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 CrossRefGoogle Scholar
  5. 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 CrossRefGoogle Scholar
  6. 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 CrossRefGoogle Scholar
  7. Bellairs A, Bryant SV (1985) Autotomy and regeneration in reptiles. Biol Reptil 15:301–410Google Scholar
  8. 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 CrossRefGoogle Scholar
  9. 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 CrossRefGoogle Scholar
  10. 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 CrossRefGoogle Scholar
  11. 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 CrossRefGoogle Scholar
  12. 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 CrossRefGoogle Scholar
  13. 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 CrossRefGoogle Scholar
  14. 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 CrossRefGoogle Scholar
  15. 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 CrossRefGoogle Scholar
  16. 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 CrossRefGoogle Scholar
  17. Hopwood D (1977) Histopathologic technic and practical histochemistry (4th edition). Biochem Soc Trans.  https://doi.org/10.1042/bst0050558a Google Scholar
  18. 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 CrossRefGoogle Scholar
  19. 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 CrossRefGoogle Scholar
  20. 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 CrossRefGoogle Scholar
  21. 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 CrossRefGoogle Scholar
  22. 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 CrossRefGoogle Scholar
  23. 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 CrossRefGoogle Scholar
  24. 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 CrossRefGoogle Scholar
  25. Reinke JM, Sorg H (2012) Wound repair and regeneration. Eur Surg Res 49:35–43.  https://doi.org/10.1159/000339613 CrossRefGoogle Scholar
  26. 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 CrossRefGoogle Scholar
  27. Schindelin J, Rueden CT, Hiner MC, Eliceiri KW (2015) The ImageJ ecosystem: an open platform for biomedical image analysis. Mol Reprod Dev 82:518–529CrossRefGoogle Scholar
  28. 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 CrossRefGoogle Scholar
  29. 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 Google Scholar
  30. 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 CrossRefGoogle Scholar
  31. 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 CrossRefGoogle Scholar
  32. 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 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.School of HealthPolytechnic of Porto (ESS/P.PORTO)PortoPortugal
  2. 2.Biochemistry Unit, Department of Biomedicine, Faculty of MedicineUniversity of Porto (FMUP)PortoPortugal
  3. 3.Instituto de Investigação e Inovação em Saúde (I3S), Metabolism, Nutrition and Endocrinology GroupUniversity of PortoPortoPortugal
  4. 4.Institute of Molecular Pathology and ImmunologyUniversity of Porto (IPATIMUP)PortoPortugal
  5. 5.Faculty of Nutrition and Food ScienceUniversity of PortoPortoPortugal

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