Volume 40 Issue 5
Sep.  2019
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Lorenzo Alibardi. Immunodetection of ephrin receptors in the regenerating tail of the lizard Podarcis muralis suggests stimulation of differentiation and muscle segmentation. Zoological Research, 2019, 40(5): 416-426. doi: 10.24272/j.issn.2095-8137.2019.046
Citation: Lorenzo Alibardi. Immunodetection of ephrin receptors in the regenerating tail of the lizard Podarcis muralis suggests stimulation of differentiation and muscle segmentation. Zoological Research, 2019, 40(5): 416-426. doi: 10.24272/j.issn.2095-8137.2019.046

Immunodetection of ephrin receptors in the regenerating tail of the lizard Podarcis muralis suggests stimulation of differentiation and muscle segmentation

doi: 10.24272/j.issn.2095-8137.2019.046
Funds:  This study was mainly supported by the Comparative Histolab Padova and University of Bologna
More Information
  • Corresponding author: Lorenzo Alibardi
  • Received Date: 2019-01-13
  • Publish Date: 2019-09-18
  • Ephrin receptors are the most common tyrosine kinase effectors operating during development. Ephrin receptor genes are reported to be up-regulated in the regenerating tail of the Podarcis muralis lizard. Thus, in the current study, we investigated immunolocalization of ephrin receptors in the Podarcis muralis tail during regeneration. Weak immunolabelled bands for ephrin receptors were detected at 15–17 kDa, with a stronger band also detected at 60–65 kDa. Labelled cells and nuclei were seen in the basal layer of the apical wound epidermis and ependyma, two key tissues stimulating tail regeneration. Strong nuclear and cytoplasmic labelling were present in the segmental muscles of the regenerating tail, sparse blood vessels, and perichondrium of regenerating cartilage. The immunolocalization of ephrin receptors in muscle that gives rise to large portions of new tail tissue was correlated with their segmentation. This study suggests that the high localization of ephrin receptors in differentiating epidermis, ependyma, muscle, and cartilaginous cells is connected to the regulation of cell proliferation through the activation of programs for cell differentiation in the proximal regions of the regenerating tail. The lower immunolabelling of ephrin receptors in the apical blastema, where signaling proteins stimulating cell proliferation are instead present, helps maintain the continuous growth of this region.
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  • [1]
    null Alibardi L . 1994. Fine autoradiographical study on scale morphogenesis in the regenerating tail of lizards. Histology and Histopathology, 9: 119–134.
    null Alibardi L . 1995. Muscle differentiation and morphogenesis in the regenerating tail of lizards. Journal of Anatomy, 186: 143–151.
    null Alibardi L . 2014. Histochemical, biochemical and cell biological aspects of tail regeneration in lizard, an amniote model for studies on tissue regeneration. Progress in Histochemistry and Cytochemistry, 48(4): 143–244.
    null Alibardi L . 2015. Immunolocalization of FGF7 (KGF) in the regenerating tail of lizard suggests it is involved in the differentiation of the epidermis. Acta Histochemica, 117(8): 718–724.
    null Alibardi L . 2016. Immunolocalization of a p53/p63-like protein in the regenerating tail of the wall lizard (Podarcis muralis) suggests it is involved in the differentiation of the epidermis. Acta Zoologica, 97(4): 395–406.
    null Alibardi L . 2017a. Review: Biological and molecular differences between tail regeneration and limb scarring in lizard: an inspiring model addressing limb regeneration in amniotes. Journal of Experimental Zoology, 328B(6): 493–514.
    null Alibardi L . 2017b. Hyaluronate likely contributes to the immunesuppression of the regenerating tail blastema in lizards: implications for organ regeneration in amniotes. Acta Zoologica, 99(4): 321–330.
    null Alibardi L . 2017c. Review: Hyaluronic acid in the tail and limb of amphibians and lizards recreates permissive embryonic conditions for regeneration due to its hygroscopic and immuno-suppressive properties. Journal of Experimental Zoology, 328B(8): 760–771.
    null Alibardi L . 2017d. Wnt-1 immunodetection in the regenerating tail of lizard suggests it is involved in the proliferation and distal growth of the blastema. Acta Histochemica, 119(3): 211–219.
    null Alibardi L . 2018. Tail regeneration reduction in lizards after repetitive amputation or cauterization reflects an increase of immune cells in blastemas. Zoological Research, 39(6): 413–423.
    null Alibardi L , Meyer-Rochow VB . 1989. Comparative fine structure of the axial skeleton inside the regenerated tail of some lizard species and the tuatara (Sphenodon punctatus). Gegembaurs Morphologisches Jahrbuch (Leipzig), 135(5): 705–716.
    null Alibardi L , Miolo V . 1990. Fine observation on nerves colonizing the regenerating tail of the lizard Podarcis sicula . Histology and Histophathology, 5: 387–396.
    null Bellairs AA , Bryant SV . 1985. Autotomy and regeneration in reptiles. In: Gans C, Billet F, Maderson PFA. Biology of the Reptilia, vol 15B
    null NY, USA: John Wiley & Sons, 302–410.
    null Bong YS , Lee HS , Carim-Todd L , Mood K , Nishanian TG , Tessarollo L , Daar IO . 2007. EphrinB1 signals from the cell surface to the nucleus by recruitment of STAT3. Proceedings of the National Academy of Sciences of the United States of America, 104(44): 17305–17310.
    null Compagni A , Logan M , Klein R , Adams RH . 2003. Control of skeletal patterning by ephrinB1-EphB interactions. Developmental Cell, 5(2): 217–230.
    null Cox PG . 1969. Some aspects of tail regeneration in the lizard, Anolis carolinensis . I. A description based on histology and autoradiography. Journal of Experimental Zoology, 171(2): 127–150.
    null Cristino L , Pica A , Della Corte F , Bentivoglio M . 2000a. Plastic changes and nitric oxide synthase induction in neurons that innervate the regenerated tail of the lizard Gekko gecko: I. Response of spinal motoneurons to tail amputation and regeneration. Journal of Comparative Neurology, 417(1): 60–72.
    null Cristino L , Pica A , Della Corte F , Bentivoglio M . 2000b. Plastic changes and nitric oxide synthase induction in neurons that innervate the regenerated tail of the lizard Gekko gecko . II. The response of dorsal root ganglion cells to tail amputation and regeneration. Brain Research, 871(1): 83–93.
    null Davy A , Aubin J , Soriano P . 2004. Ephrin-B1 forward and reverse signaling are required during mouse development. Genes & Development, 18(5): 572–583.
    null Durbin L , Brennan C , Shiomi K , Cooke J , Barriors A , Shanmugalingam S , Guthrie B , Lindberg R , Holder N . 1998. Eph signaling is required for segmentation and differentiation of the somites. Genes & Development, 12(19): 3096–3109.
    null Fisher RE , Geiger LA , Stroik LK , Hutchins ED , George RM , DeNardo DF , Kosumi K , Rawls JA , Wilson-Rawls J . 2012. A histological comparison of the original and regenerated tail in the green anole, Anolis carolinensis . Anatomical Record, 295(10): 1609–1619.
    null Gilbert EAB , Delorme SL , Vickaryous MK . 2015. The regeneration blastema of lizards: an amniote model for the study of appendage replacement. Regeneration, 2(2): 45–53.
    null Henkemeyer M , Mcglade J , Holmyard D , Marengere LEM , Olivier JP , Conlon RA , Letwin KC , Pawson T . 1994. Immunolocalization of the Nuk receptor tyrosine kinase suggests roles in segmental patterning of the brain and axonogenesis. Oncogene, 9(4): 1001–1014.
    null Hughes A , New D . 1959. Tail regeneration in the geckonid lizard, Sphaerodactylus . Development, 7: 281–302.
    null Hutchins ED , Markov GJ , Eckalbar WL , Gorge RM , King JM , Tokuyama MA , Geiger LA , Emmert N , Ammar MJ , Allen AP , Siniard AL , Corneveaux JJ , Fisher RE , Wade J , DeNardo DF , Rawls JA , Huentelman MJ , Wilson-Rawls J , Kosumi K . 2014. Transcriptomic analysis of tail regeneration in the lizard Anolis carolinensis reveals activation of conserved vertebrate developmental and repair mechanisms. PLoS One, 9(8): e105004.
    null Klein R . 2012. Eph/ephrin signalling during development. Development, 139: 4105–4109.
    null Lin KT , Wang B , Getsios S . 2012. Eph/ephrin signaling in epidermal differentiation and disease. Seminars in Cell Developmental Biology, 23(1): 92–101.
    null Liu Y , Zhou O , Wang Y , Luo L , Yang J , Yang L , Liu M , Li Y , Qian YT , Zheng Y , Li M , Li J , Gu Y , Han Z , Xu M , Wang Y , Zhu C , Yu B , Yang Y , Ding F , Jiand J , Yang H , Gu X . 2015. Gekko japonicus genome reveals evolution of adhesive toe pads and tail regeneration. Nature Communications, 6: 10033..
    null Lozito TP , Tuan RS . 2015. Lizard tail regeneration: regulation of two distinct cartilage regions by indian hedgehog. Developmental Biology, 399(2): 249–262.
    null Lozito TP , Tuan RS . 2016. Lizard tail skeletal regeneration combines aspects of fracture healing and blastema-based regeneration. Development, 143: 2946–2957.
    null Nunan R , Campbell J , Mori R , Pitulescu ME , Jiang WG , Harding KG , Adams RH , Nobes CD , Martin P . 2015. Ephrin-Bs drive junctional downregulation and actin stress fiber disassembly to enable wound re-epithelialization. Cell Reports, 13(7): 1380–1395.
    null Palmer A , Klein R . 2003. Multiple roles of ephrins in morphogenesis, neuronal networking, and brain function. Genes Development, 17: 1429–1450.
    null Park I , Lee HS . 2015. EphB/ephrinB signaling in cell adhesion and migration. Molecular and Cell, 38(1): 14–19.
    null Pasquale EB . 2010. Eph receptors and ephrins in cancer: bidirectional signalling and beyond. Nature Review in Cancer, 10: 165–180.
    null Perez-White BE , Getsios S . 2014. Eph receptor and ephrin function in breast, gut, and skin epithelia. Cell Adhesion and Migration, 8(4): 327–338.
    null Poliakov A , Cotrina M , Wilkinson DG . 2004. Diverse roles of eph receptors and ephrins in the regulation of cell migration and tissue assembly. Developmental Cell, 7(4): 465–480.
    null Simpson SB , Duffy MT . 1994. The lizard spinal cord: a model system for the study of spinal cord injury and repair. Progress in Brain Research, 103: 229–241.
    null Stark DA , Karvas RM , Siegel AL , Cornelison DDW . 2011. Eph/ephrin interactions modulate muscle satellite cell motility and patterning. Development, 138(24): 5279–5289.
    null Tomita T , Tanaka S , Morohashi Y , Iwatsubo T . 2006. Presenilin-dependent intramembrane cleavage of ephrin-B1. Molecular Neurodegeneration, 1: 1.
    null Vitulo N , Dalla Valle L , Skobo T , Valle G , Alibardi L . 2017a. Transcriptome analysis of the regenerating tail vs. the scarring limb in lizard reveals pathways leading to successful vs. unsuccessful organ regeneration in amniotes. Developmental Dynamics, 246(2): 116–134.
    null Vitulo N , Dalla Valle L , Skobo T , Valle G , Alibardi L . 2017b. Down-regulation of lizard immuno-genes in the regenerating tail and myogenes in the scarring limb suggests that tail regeneration occurs in an immuno-privileged organ. Protoplasma, 254(6): 2127–2141.
    null Wada N , Tanaks H , Ide H , Nohno T . 2003. Ephrin-A2 regulates position-specific cell affinity and is involved in cartilage morphogenesis in the chick limb bud. Developmental Biology, 264(2): 550–563.
    null Wu P , Alibardi L , Chuong CM . 2014. Lizard scale regeneration and development: a model system to analyze mechanisms of skin appendages morphogenesis in amniotes. Regeneration, 1: 15–26.
    null Yang HB , Song W , Chen LY , Li QF , Shi SL , Kong HY , Chen P . 2014. Differential expression and regulation of prohibitin during curcumin-induced apoptosis of immortalized human epidermal HaCaT cells. International Journal of Molecular Medicine, 33(3): 507–514.
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