Skip to main content

Advertisement

SpringerLink
Log in

Ontogeny of the conus papillaris of the lizard Gallotia galloti and cellular response following transection of the optic nerve: an immunohistochemical and ultrastructural study

  • Regular Article
  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

Spontaneous regrowth of the axons of retinal ganglion cells (RGC) occurs after unilateral optic nerve transection (ONT) in the lizard Gallotia galloti. We have performed an immunohistochemical and ultrastructural study of the conus papillaris (CP) of this lizard during ontogeny and after ONT in order to characterize its cell subpopulations, innervation and putative blood-brain barrier (BBB) and to evaluate changes occurring throughout regeneration. Proliferating PCNA+ cells were abundant between embryonic stage 33 (E33) and hatching. From E33, we observed Pax2+/GS+ glial cells in the primitive CP, which became increasingly pigmented and vascularised from E35. Conal astrocytes coexpressing Pax2 with vimentin and/or GFAP were identified from E37-E38. GluT-1+/LEA+/Pax2- endothelial cells (ECs) formed a continuous endothelium with tight junctions and luminal and abluminal microfolds. In adults, the peripheral blood vessels showed a thinner calibre, stronger GluT-1 staining and more abundant microfolds than those of the central CP indicating the higher specialization involved during transport within the former. Occasional pericytes, abundant Pax2+ pigment cells, LEA+ microglia/macrophages, unmyelinated Tuj1+ nerve fibres and SV2+ synaptic vesicles were also observed in the perivascular zone. After ONT, the expression of GluT-1 and p75NTR persisted in ECs, suggesting the preservation/early recovery of the BBB. Relevant ultrastructural alterations were observed at 0.5 months postlesion, although, by 3 months, the CP had recovered the ultrastructure of controls indicating tissue recovery. Abnormal newly formed blood vessels had developed in the CP-optic nerve junction. Thus, the CP is a central nervous system structure whose regenerating capacity might be key for the nutritional support of regenerating RGCs in G. galloti.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

Abbreviations

BBB:

Blood-brain barrier

CNS:

Central nervous system

CP:

Conus papillaris

ECs:

Endothelial cells

GFAP:

Glial fibrillary acidic protein

GluT-1:

Glucose transporter-1

GS:

Glutamine synthetase

iR:

Inner region

LEA:

Tomato lectin (Lycopersicon esculentum agglutinin)

MCs:

Mast cells

nPCs:

Non-pigmented cells

ON:

Optic nerve

ONH:

Optic nerve head

ONJ:

Optic nerve junction

ONT:

Optic nerve transection

oR:

Outer region

PCs:

Pigmented cells

PCNA:

Proliferating cell nuclear antigen

p75NTR :

p75 Neurotrophin receptor

RER:

Rough endoplasmic reticulum

RGCs:

Retinal ganglion cells

SV2:

Synaptic vesicle marker

TJs:

Tight junctions

Tuj1:

Anti-beta-III tubulin antibody

Vim:

Vimentin

References

  • Abbot NJ (2002) Astrocyte-endothelial interactions and blood-brain barrier permeability. J Anat 200:629–638

    Article  Google Scholar 

  • Abramsson A, Lindblom P, Betsholtz C (2003) Endothelial and nonendothelial sources of PDGF-B regulate pericytes recruitment and influence vascular pattern formation in tumors. J Clin Invest 112:1142–1151

    PubMed  CAS  Google Scholar 

  • Acarín L, Vela JM, González B, Castellano B (1994) Demonstration of poly-N-acetyl lactosamine residues in ameboid and ramified microglial cells in rat brain by tomato lectin binding. J Histochem Cytochem 42:1033–1041

    Article  PubMed  Google Scholar 

  • Allt G, Lawrenson JG (1997) Is the pial microvessel a good model for blood-brain barrier studies? Brain Res Brain Res Rev 24:67–76

    Article  PubMed  CAS  Google Scholar 

  • Barlow HB, Ostwald TJ (1972) Pecten of the pigeon´s eye as an inter-ocular eye shade. Nat New Biol 236:88–90

    PubMed  CAS  Google Scholar 

  • Bawa SR, Yash Roy RC (1974) Structure and function of vulture pecten. Acta Anat 89:473–480

    Article  PubMed  CAS  Google Scholar 

  • Beazley LD, Tennant M, Dunlop SA (1996) The effect of a chronic breakdown of the blood-optic nerve barrier on the severed optic nerve in adult rat. Restor Neurol Neurosci 10:95–101

    PubMed  CAS  Google Scholar 

  • Bergmann M, Grabs D, Rager G (2000) Expression of presynaptic proteins is closely correlated with the chronotopic pattern of axons in the retinotectal system of the chick. J Comp Neurol 418:361–372

    Article  PubMed  CAS  Google Scholar 

  • Bischoff W (1982) Die innerartliche Gliederung von Gallotia galloti (Dumeril & Bibron, 1839) (Reptilia, Sauria: Lacertidae) auf Teneriffa, Kanarische Inseln. Bonn Zool Beitr 33:363–381

    Google Scholar 

  • Brach V (1976) Structure and function of the ocular conus papillaris in Anolis equestris (Sauria:Iguanidae). Copeia 3:552–558

    Article  Google Scholar 

  • Brach V (1977) The functional significance of the avian pecten: a review. The Condor 79:321–327

    Article  Google Scholar 

  • Braekevelt CR (1984) Electron microscopic observations on the pecten of the nighthawk (Cordieles minor). Ophthalmologica 189:211–220

    Article  PubMed  CAS  Google Scholar 

  • Braekevelt CR (1986) Fine structure of the pecten oculi of the common loon (Gavia immer). Can J Zool 64:2181–2186

    Article  Google Scholar 

  • Braekevelt CR (1988) Fine structure of the pecten oculi of the pigeon (Columbia livia). Opthalmologica 196:151–159

    Article  CAS  Google Scholar 

  • Braekevelt CR (1989) Fine structure of the conus papillaris in the bobtail goanna (Tiliqua rugosa). Histol Histopathol 4:287–293

    PubMed  CAS  Google Scholar 

  • Braekevelt CR (1991) Electron microscopic observations on the pecten of the great blue heron (Ardea herodias). Histol Histopathol 6:345–351

    PubMed  CAS  Google Scholar 

  • Braekevelt CR (1993) Fine structure of the pecten oculi of the mallard (Anas platyrhynchos). Can J Zool 68:427–432

    Article  Google Scholar 

  • Braekevelt CR (1994) Fine structure of the pecten oculi in the American crow (Corvus brachyrhynchos). Anat Histol Embryol 23:357–366

    Article  PubMed  CAS  Google Scholar 

  • Braekevelt CR (1996) Fine structure of the pecten oculi in the Australian galah (Eolophus roseicapillus). Histol Histopathol 11:565–571

    PubMed  CAS  Google Scholar 

  • Bravo R, McDonald-Bravo H (1987) Existence of two populations of cyclin/proliferating cell nuclear antigen during the cell cycle. Association with DNA replication sites. J Cell Biol 105:1549–1554

    Article  PubMed  CAS  Google Scholar 

  • Buckley K, Kelly RB (1985) Identification of a transmembrane glycoprotein specific for secretory vesicles of neural and endocrine cells. J Cell Biol 100:1284–1294

    Article  PubMed  CAS  Google Scholar 

  • Calvo JL, Carbonell AL, Boya J (1991) Co-expression of glial fibrillary acidic protein and vimentin in reactive astrocytes following brain injury in rats. Brain Res 566:333–336

    Article  PubMed  CAS  Google Scholar 

  • Carbonell AL, Boya J, Calvo JL, Marin JF (1991) Ultrastructural study of the neuroglial and macrophagic reaction in Wallerian degeneration of the adult rat optic nerve. Histol Histopathol 6:443–451

    PubMed  CAS  Google Scholar 

  • Casaccia-Bonnefil P, Gu C, Khursigara G, Chao MV (1999) p75 neurotrophin receptor as a modulator of survival and death decisions. Microsc Res Tech 45:217–224

    Article  PubMed  CAS  Google Scholar 

  • Casañas N (2005) Proliferación y diversidad de las células astrogliales durante la ontogenia del sistema visual de Gallotia galloti. Doctoral thesis, Facultad de Biología, Universidad de La Laguna, Spain

  • Cerveró F (1998) Definiendo el papel de la sustancia P en el dolor. Rev Soc Esp Dolor 5:269–270

    Google Scholar 

  • Chan-Ling T, Chu Y, Baxter L, Weible Ii M, Hughes S (2009) In vivo characterization of astrocyte precursor cells (APCs) and astrocytes in developing rat retinae: differentiation, proliferation, and apoptosis. Glia 57:39–53

    Article  PubMed  Google Scholar 

  • Chu Y, Hughes S, Chan-Ling T (2001) Differentiation and migration of astrocyte precursor cells and astrocytes in human fetal retina: relevance to optic nerve coloboma. FASEB J 15:2013–2015

    PubMed  CAS  Google Scholar 

  • Cohen MP, Frank RN, Khalifa AA (1980) Collagen production by cultured retinal capillary pericytes. Invest Ophthalmol Vis Sci 19:90–94

    PubMed  CAS  Google Scholar 

  • Confaloni A, Lyckman W, Moya KL (1997) Developmental shift of synaptic vesicle protein 2 from axons to terminals in the primary visual projection of the hamster. Neuroscience 77:1225–1236

    Article  PubMed  CAS  Google Scholar 

  • Copray S, Kust B, Emmer B, Young LM, Liem R, Amor S, De Vries H, Floris S, Boddeke EJ (2004) Deficient p75 low-affinity neurotrophin receptor expression exacerbates experimental allergic encephalomyelitis in C57/BL6 mice. J Neuroimmunol 148:41–53

    Article  PubMed  CAS  Google Scholar 

  • Cragnolini AB, Friedman WJ (2008) The function of p75NTR in glia. Trends Neurosci 31:99–104

    Article  PubMed  CAS  Google Scholar 

  • Dávila JC, Guirado S, de la Calle A, Marín-Girón F (1987) The intra-ocular portion of the optic nerve in the turtle Mauremys caspita. J Anat 151:189–198

    PubMed  Google Scholar 

  • De Stefano ME, Mugnaini E (1997) Fine structure of the choroidal coat of the avian eye. II. Vascularization, supporting tissue and innervation. Anat Embryol 195:393–418

    Article  PubMed  Google Scholar 

  • Dieterich CE, Dieterich HJ (1975a) Comparative electron microscopic studies on the capillary endothelium of the conus papillaris of lizards (Sauria). Verh Anat Ges 59:643–650

    Google Scholar 

  • Dieterich CE, Dieterich HJ (1975b) Comparative electron microscopic studies on the pecten oculi of bird and the conus papillaris of reptiles. Verh Anat Ges 69:635–652

    PubMed  CAS  Google Scholar 

  • Dieterich CE, Dieterich HJ (1977) Fine structure of the conus papillaris in the eye of Chalcides chalcides L. (Lacertilia, Scincidae). Zoomorphology 87:103–121

    Article  Google Scholar 

  • Dieterich CE, Dieterich HJ, Hildebrand R (1976) Comparative electron microscopic studies on the conus papillaris and its relationship to the retina in night and day active geckos. Graefes Arch Klin Exp Ophthalmol 200:279–292

    Article  CAS  Google Scholar 

  • Dore-Duffy P (2008) Pericytes: pluripotent cells of the blood-brain barrier. Curr Pharm Des 14:1581–1593

    Article  PubMed  CAS  Google Scholar 

  • Dufaure JP, Hubert J (1961) Table de dévelopment du lizard viviparae (Lacerta vivipara jacquin). Arch Anat Microsc Morphol Exp 50:309–327

    Google Scholar 

  • Ehinger B (1967) Adrenergic nerves in the avian eye and ciliary ganglion. Z Zellforsch Mikrosk Anat 82:577–588

    Article  PubMed  CAS  Google Scholar 

  • Fischer AJ (2005) Neural regeneration in the chick retina. Prog Retin Eye Res 24:161–182

    Article  PubMed  Google Scholar 

  • Fisher M (2009) Pericytes signalling in the neovascular unit. Stroke 40:13–15

    Article  CAS  Google Scholar 

  • Flügel A, Bradl M, Kreutzberg GW, Graeber MB (2001) Transformation of donor-derived bone marrow precursors into host microglia during autoimmune CNS inflamammation and during the retrograde response to axotomy. J Neurosci Res 66:74–82

    Article  PubMed  Google Scholar 

  • Gerhardt H, Betsholtz C (2003) Endothelial-pericyte interactions in angiogenesis. Cell Tissue Res 314:15–23

    Article  PubMed  Google Scholar 

  • Gerhardt H, Liebner S, Wolburg H (1996) The pecten oculi of the chicken as a new in vivo model of the blood-brain barrier. Cell Tissue Res 285:91–100

    Article  PubMed  CAS  Google Scholar 

  • Gerhardt H, Liebner S, Redies C, Wolburg H (1999a) N-cadherin expression in endothelial cells during early angiogenesis in the eye and brain of chicken: relation to blood-retina and blood-brain barrier development. Eur J Neurosci 11:1191–1201

    Article  PubMed  CAS  Google Scholar 

  • Gerhardt H, Schuck J, Wolburg H (1999b) Differentiation of a unique macroglial cell type in the pecten oculi of the chicken. Glia 28:201–214

    Article  PubMed  CAS  Google Scholar 

  • Gorio A, Vergani L, Ferro L, Prino G, Di Giulio AM (1996) Glycosaminoglycans in nerve injury. II. Effects on transganglionic degeneration and on the expression of neurotrophic factors. J Neurosci Res 46:572–580

    Article  PubMed  CAS  Google Scholar 

  • Gschwendtner A, Liu Z, Hucho T, Bohatschek M, Kalla R, Dechant G, Raivich G (2003) Regulation, cellular localization, and function of the p75 neurotrophin receptor (p75NTR) during the regeneration of facial motoneurons. Mol Cell Neurosci 24:307–322

    Article  PubMed  CAS  Google Scholar 

  • Hirase H, Creso J, Singleton M, Barthó P, Buzsáki G (2004) Two-photon imaging of brain pericytes in vivo using dextran-conjugated dyes. Glia 46:95–100

    Article  PubMed  Google Scholar 

  • Hjelmeland LM, Harvey AK (1988) Growth factors: soluble mediators of wound repair and ocular fibrosis. Birth Defects Orig Artic Ser 24:87–102

    PubMed  CAS  Google Scholar 

  • Jasinski A (1977) Fine structure of capillaries in the conus papillaris of the limbless lizard, Ophisaurus apodus (Anguidae, Lacertilia). Cell Tissue Res 182:421–424

    Article  PubMed  CAS  Google Scholar 

  • Jeon GS, Kang TC, Park SW, Kim DW, Seo JH, Cho SS (2004) Microglial responses in the avascular quail retina following transection of the optic nerve. Brain Res 1023:15–23

    Article  PubMed  CAS  Google Scholar 

  • Jones MP, Pierce KE, Ward D (2007) Avian vision: a review of form and function with special consideration to birds of prey. J Exotic Pet Med 16:69–87

    Article  Google Scholar 

  • Joo F (1987) Current aspects of the development of blood-brain barrier. Int J Dev Neurosci 5:369–372

    Article  PubMed  CAS  Google Scholar 

  • Kenny TP, Shivers RR (1974) The blood-brain barrier in a reptile, Anolis carolinensis. Tissue Cell 6:319–333

    Article  PubMed  CAS  Google Scholar 

  • Kiama SG, Maina JN, Bhattacharjee J, Mwangi DK, Macharia RG, Weyrauch KD (2006) The morphology of the pecten oculi of the ostrich, Struthio camelus. Ann Anat 188:519–528

    Article  PubMed  CAS  Google Scholar 

  • Kiernan JA, Contestabile A (1981) Vascular permeability associated with axonal regeneration in the optic system of the goldfish. Acta Neuropathol 51:39–45

    Article  Google Scholar 

  • Krauss A, Guerra-Bautista G, Espinoza G, Barojas E, Quiroz-Mercado H, Sánchez-Echeverri G, Alarcón-Segovia D (1991) Defects of the retinal pigment epithelium in scleroderma. Br J Rheumatol 30:112–114

    Article  Google Scholar 

  • Krueger M, Bechmann I (2010) CNS pericytes: concepts, misconceptions, and a way out. Glia 58:1–10

    Article  PubMed  Google Scholar 

  • Lang DM, Monzón-Mayor M, Bandtlow CE, Stuermer CA (1998) Retinal axon regeneration in the lizard Gallotia galloti in the presence of CNS myelin and oligodendrocytes. Glia 23:61–74

    Article  PubMed  CAS  Google Scholar 

  • Lang DM, Romero-Alemán MM, Arbelo-Galvan JF, Stuermer CA, Monzón-Mayor M (2002) Regeneration of retinal axons in the lizard Gallotia galloti is not linked to generation of new retinal ganglion cells. J Neurobiol 52:322–335

    Article  PubMed  Google Scholar 

  • Latker CH, Beebe DC (1984) Developmental changes in the blood-ocular barrier in the chicken embryos. Exp Eye Res 39:401–414

    Article  PubMed  CAS  Google Scholar 

  • Liebner S, Gerhardt H, Wolburg H (1997) Maturation of the blood-retina barrier in the developing pecten oculi of the chicken. Dev Brain Res 100:205–219

    Article  CAS  Google Scholar 

  • Lillo C, Velasco A, Jimeno D, Cid E, Lara JM, Aijón J (2002) The glial design of a teleost optic nerve head supporting continuous growth. J Histochem Cytochem 50:1289–1302

    Article  PubMed  CAS  Google Scholar 

  • Lozada A, Maegele M, Stark H, Neugebauer EM, Panula P (2005) Traumatic brain injury results in mast cell increase and changes in regulation of the central histamine receptors. Neuropathol Appl Neurobiol 31:150–162

    Article  PubMed  CAS  Google Scholar 

  • Lu X, Richardson PM (1991) Inflamation near the nerve cell body enhances axonal regeneration. J Neurosci 11:972–978

    PubMed  CAS  Google Scholar 

  • Mandarino LJ, Sundarraj N, Finlayson J, Hassell HR (1993) Regulation of fibronectin and laminin synthesis by retinal capillary endothelial cells and pericytes in vitro. Exp Eye Res 57:609–621

    Article  PubMed  CAS  Google Scholar 

  • Marín-Teva JL, Almendros A, Calvente R, Cuadros MA, Navascués J (1998) Tangential migration of ameboid microglia in the developing quail retina: mechanism of migration and migratory behavior. Glia 22:31–52

    Article  PubMed  Google Scholar 

  • Meyer DB (1977) The avian eye and its adaptations. In: Crescitelli F (ed) Handbook of sensory physiology, vol VII/5. The visual system in vertebrates. Springer, Berlin, pp 549–612

    Google Scholar 

  • Mi H, Barres BA (1999) Purification and characterization of astrocyte precursor cells in the developing rat optic nerve. J Neurosci 19:1049–1061

    PubMed  CAS  Google Scholar 

  • Monzón-Mayor M, Yanes C, James JL, Sturrock RR (1990a) An ultrastructural study of the development of astrocytes in the midbrain of the lizard. J Anat 170:33–41

    PubMed  Google Scholar 

  • Monzón-Mayor M, Yanes C, James JL, Sturrock RR (1990b) An ultrastructural study of the development of oligodendrocytes in the midbrain of the lizard. J Anat 170:43–49

    PubMed  Google Scholar 

  • Moody SA, Quigg MS, Frankfurter A (1989) Development of the peripheral trigeminal system in the chick revealed by an isotype–specific anti-beta-tubulin monoclonal antibody. J Comp Neurol 279:567–580

    Article  PubMed  CAS  Google Scholar 

  • Navascués J, Moujahid A, Almendros A, Marín-Teva JL, Cuadros MA (1995) Origin of microglia in the quail retina: central-to-peripheral and vitreal-to-scleral migration of microglial precursors during development. J Comp Neurol 354:209–228

    Article  PubMed  Google Scholar 

  • Nguyen J (1969) The conus papillaris of reptiles. I. Ultrastructure in the slow-worm (Anguis fragilis, Anguides). Z Mikrosk Anat Forsch 81:96–110

    Google Scholar 

  • Nguyen-Legros J (1978) Innervation of the conus papillaris in the eyes of lacertilians. Graefes Arch Klin Exp Ophthalmol. 208:169–175

    Article  CAS  Google Scholar 

  • Nico B, Mangieri D, De Luca A, Corsi P, Benagiano V, Tamma R, Annese T, Longo V, Crivellato E, Ribatti D (2009) Nerve growth factor and its receptors TrkA and p75 are upregulated in the brain of mdx dystrophic mouse. Neuroscience 161:1057–1066

    Article  PubMed  CAS  Google Scholar 

  • Nordell VL, Lewis DK, Bake Sh, Sohrabji F (2005) The neurotrophin receptor p75NTR mediates early anti-inflammatory effects of estrogen in the forebrain of young adult rats. BMC Neurosci 6:58, doi:10.1186/1471-2202-6-58

    Article  PubMed  CAS  Google Scholar 

  • Oderfeld-Nowak B, Orzylowska-Sliwinska O, Soltys Z, Zaremba M, Januszewski S, Janeczko K, Mossakowski M (2003) Concomitant up-regulation of astroglial high and low affinity nerve growth factor receptors in the CA1 hippocampal area following global transient cerebral ischemia in rat. Neuroscience 120:31–40

    Article  PubMed  CAS  Google Scholar 

  • Okada M, Erickson A, Hendrickson A (1994) Light and electron-microscopic analysis of synaptic development in Macaca monkey retina as detected in immunocytochemical labelling for the synaptic vesicle protein SV2. J Comp Neurol 339:535–558

    Article  PubMed  CAS  Google Scholar 

  • Parrilla M, Lillo C, Herrero-Turrión M, Arévalo R, Lara J, Aijón J, Velasco A (2009) Pax2 in the optic nerve of the goldfish, a model of continuous growth. Brain Res 1255:75–88

    Article  PubMed  CAS  Google Scholar 

  • Peters A (2004) A fourth type of neuroglial cell in the adult central nervous system. J Neurocytol 33:345–357

    Article  PubMed  Google Scholar 

  • Pettigrew JD, Wallman J, Wildsoet CF (1990) Saccadic oscillations facilitate ocular perfusion from the avian pecten. Nature 343:362–363

    Article  PubMed  CAS  Google Scholar 

  • Püschel AW, Westerfield M, Dressler GR (1992) Comparative analysis of Pax-2 protein distributions during neurulation in mice and zebrafish. Mech Dev 38:197–208

    Article  PubMed  Google Scholar 

  • Quesada A, Prada FA, Aguilera Y, Espinar A, Carmona A, Prada C (2004) Peripapillary glial cells in the chick retina: a special glial cell type expressing astrocyte, radial glia, neuron, and oligodendrocyte markers throughout development. Glia 46:346–355

    Article  PubMed  Google Scholar 

  • Rankin S, Guy C, Rahimtula M, Mearow K (2008) Neurotrophin-induced upregulation of p75NTR via protein kinase C-delta-dependent mechanism. Brain Res 1217:10–24

    Article  PubMed  CAS  Google Scholar 

  • Reijerkerk A, Kooij G, Pol SMA van der, Khazen S, Dijkstra C, Vries HE de (2006) Diapedesis of monocytes is associated with MMP-mediated occluding disappearance in brain endothelial cells. FASEB J 20:1901–1909

    Article  CAS  Google Scholar 

  • Ribatti D, Nico B, Maxia C, Longo V, Murtas D, Mangieri D, Perra MT, De Giorgis M, Piras F, Crivellato E, Sirigu P (2007) Neovascularization and mast cells with tryptase activity increase simultaneously in human pterygium. J Cell Mol Med 11:585–589

    Article  PubMed  Google Scholar 

  • Risau W, Esser S, Engelhardt B (1998) Differentiation of blood-brain barrier endothelial cells. Pathol Biol 46:171–175

    PubMed  CAS  Google Scholar 

  • Rodríguez-Peralta LA (1975) Hematic and fluid barriers of the retina and vitreous body. J Comp Neurol 132:109–124

    Article  Google Scholar 

  • Romero-Alemán MM, Monzón-Mayor M, Yanes C, Arbelo-Galván JF, Lang D, Renau-Piqueras J, Negrín-Martínez C (2003) S100 immunoreactive glial cells in the forebrain and midbrain of the lizard Gallotia galloti during ontogeny. J Neurobiol 57:54–66

    Article  CAS  Google Scholar 

  • Romero-Alemán MM, Monzón-Mayor M, Yanes C, Lang D (2004) Radial glial cells, proliferating periventricular cells, and microglia might contribute to successful structural repair in the cerebral cortex of the lizard Gallotia galloti. Exp Neurol 188:74–85

    Article  PubMed  CAS  Google Scholar 

  • Romero-Alemán MM, Monzón-Mayor M, Santos E, Yanes C (2010) Expression of neuronal markers, synaptic proteins and glutamine synthetase in the control and regenerating lizard visual system. J Comp Neurol 518:4067–4087

    Article  PubMed  CAS  Google Scholar 

  • Rouget C (1873) Mémorie sur le développment, la structure et les proprietés physiologiques des capillaires sanguins et lymphatiques. Arch Physiol Norm Pathol 5:603–663

    Google Scholar 

  • Santos E (2008) Estudio de las neurotrofinas NT-3 y BDNF, mielinización y diferenciación macroglial durante la ontogenia y la regeneración de la vía óptica de Gallotia galloti. Doctoral thesis, Facultad de Biología. Universidad de La Laguna, Spain

  • Santos E, Monzón-Mayor M, Romero-Alemán M, Yanes C (2008) Distribution of neurotrophin-3 during ontogeny and regeneration of the lizard (Gallotia galloti) visual system. Dev Neurobiol 68:31–44

    Article  PubMed  CAS  Google Scholar 

  • Schuck J, Gerhardt H, Wolburg H (2000) The peripapillary glia of the optic nerve head in the chicken retina. Anat Rec 259:263–275

    Article  PubMed  CAS  Google Scholar 

  • Schweigerer L, Neufeld G, Friedman J, Abraham JA, Fiddes JC, Gospodarowicz D (1987) Capillary endothelial cells express basic fibroblast growth factor, a mitogen that promotes their own growth. Nature 325:257–259

    Article  PubMed  CAS  Google Scholar 

  • Shivers RR (1979) The effect of hyperglycemia on brain capillary permeability in the lizard, Anolis carolinensis. A freeze fracture analysis of blood-brain barrier pathology. Brain Res 170:509–522

    Article  PubMed  CAS  Google Scholar 

  • Smith BJ, Smith SA, Braekevelt CR (1996) Fine structure of the pecten oculi of the barred owl (Strix varia). Histol Histopathol 11:89–96

    PubMed  CAS  Google Scholar 

  • Snow RL, Robson JA (1995) Migration and differentiation of neurons in the retina and optic tectum of the chick. Exp Neurol 134:13–24

    Article  PubMed  CAS  Google Scholar 

  • Soukkarieh C, Agius E, Soula C, Cochard P (2007) Pax2 regulates neuronal-glial cell fate choice in the embryonic optic nerve. Dev Biol 303:800–813

    Article  PubMed  CAS  Google Scholar 

  • Stanke J, Moose HE, El-Hodiri HM, Fischer AJ (2010) Comparative study of Pax2 expression in glial cells in the retina and optic nerve of birds and mammals. J Comp Neurol 518:2316–2333

    Article  PubMed  CAS  Google Scholar 

  • Streit WJ (2001) Microglia and macrophages in the developing CNS. Neurotoxicology 22:619–624

    Article  PubMed  CAS  Google Scholar 

  • Sundberg C, Ivarsson M, Gerdin B, Rubin K (1996) Pericytes as collagen producing cells in excessive dermal scarring. Lab Invest 74:452–466

    PubMed  CAS  Google Scholar 

  • Taniuchi M, Clark HB, Schweitzer JB, JR JEM (1988) Expression of nerve growth factor receptor by Schwann cells of axotomized peripheral nerves: ultrastructural location suppression by axonal contact, and binding properties. J Neurosci 8:664–681

    PubMed  CAS  Google Scholar 

  • Tennant M, Beazley LD (1992) A breakdown of the blood-brain barrier is associated with optic nerve regeneration in the frog. Vis Neurosci 9:149–155

    Article  PubMed  CAS  Google Scholar 

  • Tennant M, Moore SR, Beazley LD (1993) Transient neovascularisation of the frog retina during optic nerve regeneration. J Comp Neurol 336:605–612

    Article  PubMed  CAS  Google Scholar 

  • Theoharides TC (1990) Mast cells: the immune gate to the brain. Life Sci 46:607–617

    Article  PubMed  CAS  Google Scholar 

  • Tout S, Chang-Ling T, Hollander H, Stone J (1993) The role of Müller cells in the formation of the blood-retinal barrier. Neuroscience 55:291–301

    Article  PubMed  CAS  Google Scholar 

  • Triviño A, Ramírez JM, Salazar JJ, Ramírez AI, García-Sánchez J (1996) Immunohistochemical study of the human optic nerve head astroglia. Vis Res 36:2015–2028

    Article  PubMed  Google Scholar 

  • Viñoly R (2005) Inmunohistoquímica de las células GS y lectina positivas durante la ontogenia del sistema visual de Gallotia galloti. Doctoral thesis, Facultad de Biología, Universidad de La Laguna, Spain

  • Wingstrand KG, Munk O (1965) The pecten oculi of the pigeon with particular regard to its function. Biol Skr Dan Vid Selsk 14:1–64

    Google Scholar 

  • Wolburg H, Bäuerle C (1993) Astrocytes in the lamina cribrosa of the rat optic nerve: are their morphological peculiarities involved in an altered blood-brain barrier? J Hirnforsch 34:445–459

    PubMed  CAS  Google Scholar 

  • Wolburg H, Liebner S, Reichenbach A, Gerhardt H (1999) The pecten oculi of the chicken: a model system for vascular differentiation and barrier maturation. Int Rev Cytol 187:111–159

    Article  PubMed  CAS  Google Scholar 

  • Yanes C, Monzón-Mayor M, Ghandour MS, Barry J de, Gombos G (1990) Radial glia and astrocytes in developing and adult telencephalon of the lizard Gallotia galloti as revealed by immunohistochemistry with anti-GFAP and anti-vimentin antibodies. J Comp Neurol 295:559–568

    Article  PubMed  CAS  Google Scholar 

  • Yang Hy, Lieska N, Shao D, Kriho V, Pappas GD (1994) Proteins of the intermediate filament cytoskeleton as markers for astrocytes and human astrocytomas. Mol Chem Neuropathol 21:155–176

    Article  PubMed  CAS  Google Scholar 

  • Zhou XF, Rush RA, McLachlan EM (1996) Differential expression of the p75 nerve growth factor receptor in glia and neurons of the rat dorsal root ganglia after peripheral nerve transection. J Neurosci 16:2901–2911

    PubMed  CAS  Google Scholar 

Download references

Acknowledgements

The authors are grateful to Dr. Nualart for his kind gift of some commercial antibodies and they express their appreciation to Agustín Fernández from the Cytometry and Microscopy Centre of the University Complutense of Madrid (UCM) for technical assistance, to the Electron Microscopy Services of the University of La Laguna (ULL) and to the University of Las Palmas of Gran Canaria (ULPGC).

Author information

Authors and Affiliations

  1. Department of Cellular Biology, Faculty of Biology, University of La Laguna, Avda. Fco. Sánchez s/n, 38206, La Laguna, Tenerife, Canary Islands, Spain

    M. C. Alfayate, E. Santos, C. Yanes, N. Casañas & R. Viñoly

  2. Department of Morphology (Cellular Biology), Faculty of Health Sciences, University of Las Palmas of Gran Canaria, C/ Dr. Pasteur s/n. A.C. 550, 35016, Las Palmas, Canary Islands, Spain

    E. Santos, Maria del Mar Romero-Alemán & Maximina Monzón-Mayor

Authors
  1. M. C. Alfayate
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. E. Santos
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. C. Yanes
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. N. Casañas
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. R. Viñoly
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Maria del Mar Romero-Alemán
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Maximina Monzón-Mayor
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Maximina Monzón-Mayor.

Additional information

This work was supported by the Spanish Ministry of Education (Research Project BFU2007-67139) and the Regional Canary Islands Government (ACIISI, Research Project SolSubC200801000281; Project ULPAPD-08/01-4).

Electronic supplementary materials

Below is the link to the electronic supplementary material.

Fig. S1

Immunofluorescence labelling for PCNA, Vim and Pax2/GFAP and electron micrograph in the developing or regenerating CP. Asterisks in this figure indicate CP-ONJ, for orientation. The CP tip is located at the top and the base at the bottom in all images. a, b Abundant PCNA+ cells were detected in the developing CP, being more numerous at E35 than at E33 due to the CP growth. c Labelling for PCNA at 1 month postlesion, showing proliferating cells (arrows) in different regions of the CP. d Vimentin staining was abundant in the entire adult CP. Note the stained endothelial cells (arrows). Cell nuclei are stained with Dapi. e GFAP staining in postnatals is intense in the inner CP (arrow) whereas is absent in peripheral capillaries. Cell nuclei are stained with Dapi. f Lower-power image corresponding to the Fig 2k, k´showing abundant reactive Pax2+/GFAP+ astrocytes (arrowheads) in the ONH and CP base at 1 month postlesion. Note, in addition, scarce Pax2+/GFAP- cells in the CP. g Electron micrograph of a reactive astrocyte at the CP base (arrows in inset g´) at 1 month postlesion, showing a cytoplasm filled with gliofilaments (top-left inset) and lipid droplet (arrow). Overlapping cell processes are closely located (arrowhead). Bars 50 μm (a-f) 10 μm (inset in g) 1 μm (g) (GIF 647 kb)

High resolution image (TIFF 21791 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Alfayate, M.C., Santos, E., Yanes, C. et al. Ontogeny of the conus papillaris of the lizard Gallotia galloti and cellular response following transection of the optic nerve: an immunohistochemical and ultrastructural study. Cell Tissue Res 344, 63–83 (2011). https://doi.org/10.1007/s00441-011-1128-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-011-1128-3

Keywords

Search

Navigation