Differentiation Markers of Retinal Cell Types in Studies on Vertebrate Eye Development and Regeneration

Data on the use of various immunochemical markers specifically indicating cell types of the neural retina and pigment epithelium are reviewed. It is demonstrated how this approach can be applied to the analysis of specific features of vertebrate retinal development, including the order and timing of differentiation of the main cell types, their interdependence in the course of this process, and factors controlling the latter. Problems concerning the state of differentiation and its change in the cells of retinal pigment epithelium and glial cells are discussed in respect to their analysis with the aid of specific protein markers. The current state of retina regeneration research involving the use of labeled cell sources and regenerated cells in lower vertebrates is analyzed. Problems in the search for new markers of retinal photoreceptor, macroglial, and microglial cells and their use in experiments are addressed.

[1]  T. Reh.  Cell-specific regulation of neuronal production in the larval frog retina , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[2]  K. Palczewski,et al.  Turned on by Ca2+! The physiology and pathology of Ca2+-binding proteins in the retina , 1996, Trends in Neurosciences.

[3]  S. McLoon,et al.  Immediate differentiation of ganglion cells following mitosis in the developing retina , 1995, Neuron.

[4]  E. Harris,et al.  A developmentally regulated microsomal protein specific for the pigment epithelium of the vertebrate retina , 1993, Journal of neuroscience research.

[5]  R. Wetts,et al.  Multipotent precursors can give rise to all major cell types of the frog retina. , 1988, Science.

[6]  P. Raymond,et al.  Selective regeneration of photoreceptors in goldfish retina. , 1994, Development.

[7]  A. Kahn.  An autoradiographic analysis of the time of appearance of neurons in the developing chick neural retina. , 1974, Developmental biology.

[8]  P. Raymond,et al.  Retinal regeneration , 1992, Trends in Neurosciences.

[9]  J. Voyvodic,et al.  Differentiation and morphogenesis in pellet cultures of developing rat retinal cells , 1996, The Journal of comparative neurology.

[10]  P. Mobbs,et al.  Connexin α1 and Cell Proliferation in the Developing Chick Retina , 1999, Experimental Neurology.

[11]  W. Harris,et al.  Regulation of neuronal diversity in the Xenopus retina by Delta signalling , 1997, Nature.

[12]  J. Wye-Dvorak,et al.  GABA-like immunoreactive neurons in the retina of Bufo marinus: evidence for the presence of GABA-containing ganglion cells , 1992, Brain Research.

[13]  V. Mitashov.  Retinal regeneration in amphibians. , 1997, The International journal of developmental biology.

[14]  V. N. Ivanov,et al.  IMMUNOHISTOCHEMICAL STUDIES OF S‐100 PROTEIN DURING POSTNATAL ONTOGENESIS OF THE BRAIN OF TWO STRAINS OF RATS , 1972, Journal of neurochemistry.

[15]  H. Kolb,et al.  Circuitry and role of substance P‐immunoreactive neurons in the primate retina , 1998, The Journal of comparative neurology.

[16]  C. Hamel,et al.  Molecular cloning and expression of RPE65, a novel retinal pigment epithelium-specific microsomal protein that is post-transcriptionally regulated in vitro. , 1993, The Journal of biological chemistry.

[17]  L. Chun,et al.  Developmental study of Müller cells in the rat retina using a new monoclonal antibody, RT10F7 , 1998, Neuroscience.

[18]  C. Cepko,et al.  Two Phases of Rod Photoreceptor Differentiation during Rat Retinal Development , 1998, The Journal of Neuroscience.

[19]  M. Raff,et al.  Diffusible rod-promoting signals in the developing rat retina. , 1992, Development.

[20]  J B Hurley,et al.  Recoverin: a calcium sensitive activator of retinal rod guanylate cyclase , 1991, Science.

[21]  K. Negishi,et al.  Dopamine cells and rod bipolar cells contain protein kinase C-like immunoreactivity in some vertebrate retinas , 1988, Neuroscience Letters.

[22]  C. Barnstable,et al.  Expression of the cell surface antigens RET-PE2 and N-CAM by rat retinal pigment epithelial cells during development and in tissue culture. , 1990, Experimental eye research.

[23]  Y. Courtois,et al.  Suppression of fibroblast growth factor 2 expression by antisense oligonucleotides inhibits embryonic chick neural retina cell differentiation and survival in vivo , 1998, Developmental dynamics : an official publication of the American Association of Anatomists.

[24]  P. Koulen.  Localization of synapse‐associated proteins during postnatal development of the rat retina , 1999, The European journal of neuroscience.

[25]  H. Richer,et al.  Search for High Frequency Optical Variability in X-Ray Sources , 1972 .

[26]  P. R. Johns.  Growth of the adult goldfish eye. III. Source of the new retinal cells , 1977, The Journal of comparative neurology.

[27]  C. Spilker,et al.  Calcium- and myristoyl-dependent subcellular localization of the neuronal calcium-binding protein VILIP in transfected PC12 cells , 1997, Neuroscience Letters.

[28]  T. Reh,et al.  A possible role for the vascular membrane in retinal regeneration in Rana catesbienna tadpoles. , 1987, Developmental biology.

[29]  W. Eldred,et al.  Neuropeptide Y‐immunoreactive amacrine cells in the retina of the turtle Pseudemys scripta elegans , 1988, The Journal of comparative neurology.

[30]  H. Wässle,et al.  Diversity of glutamate receptors in the mammalian retina , 1998, Vision Research.

[31]  I. Grierson,et al.  Retinal pigment epithelial cells in epiretinal membranes: an immunohistochemical study. , 1984, The British journal of ophthalmology.

[32]  A. F. Wiechmann,et al.  Early expression of recoverin in a unique population of neurons in the human retina , 1996, Anatomy and Embryology.

[33]  Don H. Anderson,et al.  Changes in the expression of specific Müller cell proteins during long-term retinal detachment. , 1989, Experimental eye research.

[34]  Y. Kaneko,et al.  Study of the regenerating newt retina by electrophysiology and immunohistochemistry (bipolar- and cone-specific antigen localization). , 1994, The Journal of experimental zoology.

[35]  N. Dünker.  Serotonergic neurons and processes in the adult and developing retina of Ichthyophis kohtaoensis (Amphibia; Gymnophiona) , 1999, Anatomy and Embryology.

[36]  C. Guérin,et al.  Effects of the neurotrophin brain-derived neurotrophic factor in an experimental model of retinal detachment. , 1999, Investigative ophthalmology & visual science.

[37]  W. Eldred,et al.  Immunocytochemical localization of glycine in the retina of the turtle (Pseudemys scripta) , 1989, Visual Neuroscience.

[38]  Y. Sasai,et al.  Regulation of neural induction by the Chd and Bmp-4 antagonistic patterning signals in Xenopus , 1995, Nature.

[39]  B. Reese,et al.  Mosaics of Islet-1-Expressing Amacrine Cells Assembled by Short-Range Cellular Interactions , 1997, The Journal of Neuroscience.

[40]  C. Barnstable.  Chapter 3 Molecular aspects of development of mammalian optic cup and formation of retinal cell types , 1991 .

[41]  S. Nawy,et al.  Role of the low-affinity NGF receptor (p75) in survival of retinal bipolar cells , 1998, Visual Neuroscience.

[42]  S. Hatakenaka,et al.  Immunohistochemical localization of chick retinal 24 kdalton protein (visinin) in various vertebrate retinae , 1985, Brain Research.

[43]  G. Ramı́rez,et al.  Spatial and Temporal Patterns of Neurogenesis in the Chick Retina , 1991, The European journal of neuroscience.

[44]  M. Kelley,et al.  Retinoic acid promotes differentiation of photoreceptors in vitro. , 1994, Development.

[45]  H. Sagara,et al.  Monoclonal antibodies which recognize endoplasmic reticulum in the retinal pigment epithelium. , 1991, Experimental eye research.

[46]  Diurnal expression of recoverin in the rat retina. , 1997, Brain research. Molecular brain research.

[47]  J. Schnitzer,et al.  Horizontal cells of the mouse retina contain glutamic acid decarboxylase-like immunoreactivity during early developmental stages , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[48]  R. Dacheux,et al.  Antigenic changes of rabbit retinal Müller cells in culture. , 1998, Investigative ophthalmology & visual science.

[49]  H. Wolburg,et al.  Müller glia endfeet, a basal lamina and the polarity of retinal layers form properly in vitro only in the presence of marginal pigmented epithelium , 1991, Cell and Tissue Research.

[50]  G. Wistow,et al.  The cDNA RPE1 and monoclonal antibody HMB-50 define gene products preferentially expressed in retinal pigment epithelium. , 1992, Experimental eye research.

[51]  Y. Kaneko,et al.  Regeneration of the newt retina: Order of appearance of photoreceptors and ganglion cells , 1998, The Journal of comparative neurology.

[52]  Keun-Young Kim,et al.  Double-labeling techniques demonstrate that rod bipolar cells are under GABAergic control in the inner plexiform layer of the rat retina , 1998, Cell and Tissue Research.

[53]  P. Layer,et al.  Pigmented epithelium induces complete retinal reconstitution from dispersed embryonic chick retinae in reaggregation culture , 1997, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[54]  C. Holt,et al.  A role for the fibroblast growth factor receptor in cell fate decisions in the developing vertebrate retina. , 1998, Development.

[55]  W. Harris,et al.  Molecular recapitulation: the growth of the vertebrate retina. , 1998, The International journal of developmental biology.

[56]  B. Völgyi,et al.  Calretinin-immunoreactive elements in the retina and optic tectum of the frog, Rana esculenta , 1998, Brain Research.

[57]  M. Takeichi,et al.  The cadherins: cell-cell adhesion molecules controlling animal morphogenesis. , 1988, Development.

[58]  C. Cepko,et al.  Cell fate determination in the vertebrate retina. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[59]  H. Wässle,et al.  Immunocytochemical labelling of horizontal cells in mammalian retina using antibodies against calcium-binding proteins , 1987, Neuroscience Letters.

[60]  P. Raymond,et al.  Retinal regeneration in teleost fish. , 1991, Ciba Foundation symposium.

[61]  H. Kolb,et al.  Endothelial nitric oxide synthase (eNOS) is localized to Müller cells in all vertebrate retinas , 1999, Vision Research.

[62]  R. Weiler,et al.  Co-localization of neurotensin-like immunoreactivity and 3H-glycine uptake system in sustained amacrine cells of turtle retina , 1984, Nature.

[63]  Anton Hj,et al.  [The appearance and distribution of the NF-200 neurofilament protein in transdifferentiating cells of the pigment epithelium and in other eye cells during retinal regeneration in tritons]. , 1993 .

[64]  H. Wässle,et al.  Organotypic slice culture of the mammalian retina , 1993, Visual Neuroscience.

[65]  Mitashov Vi.  Autoradiographic study of the retinal regeneration in the newt (Triturus cristatus) , 1968 .

[66]  T. Wiesel,et al.  Immunolabelling by a newt retinal pigment epithelium antibody during retinal development and regeneration , 1990, The Journal of comparative neurology.

[67]  J. Hollyfield.  Differential addition of cells to the retina in Rana pipiens tadpoles. , 1968, Developmental biology.

[68]  R. Pochet,et al.  Recoverin and hippocalcin distribution in the lamprey (Lampreta fluviatilis) retina , 1998, Neuroscience Letters.

[69]  C. Holt,et al.  Cellular determination in the xenopus retina is independent of lineage and birth date , 1988, Neuron.

[70]  A. Gown,et al.  Anti-melanoma monoclonal antibody HMB45 identifies an oncofetal glycoconjugate associated with immature melanosomes. , 1992, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[71]  P. Wilson,et al.  Induction of epidermis and inhibition of neural fate by Bmp-4 , 1995, Nature.

[72]  J. Coulombre,et al.  Regeneration of neural retina from the pigmented epithelium in the chick embryo. , 1965, Developmental biology.

[73]  H. Karten,et al.  Chapter 7 Identification and localization of biologically active peptides in the vertebrate retina , 1984 .

[74]  V. Mitashov,et al.  Remodeling processes during neural retinal regeneration in adult urodeles: an immunohistochemical survey. , 1995, The International journal of developmental biology.

[75]  C. Redies,et al.  N‐ and R‐cadherin expression in the optic nerve of the chicken embryo , 1993, Glia.

[76]  J. Keefe.  An analysis of urodelian retinal regeneration. I. Studies of the cellular source of retinal regeneration in Notophthalmus viridescens utilizing 3 H-thymidine and colchicine. , 1973, The Journal of experimental zoology.

[77]  D. Morse,et al.  Neuroectoderm of the early embryonic rat eye. Scanning electron microscopy. , 1984, Investigative ophthalmology & visual science.

[78]  U. Hellman,et al.  The retinal pigment epithelial membrane receptor for plasma retinol-binding protein. Isolation and cDNA cloning of the 63-kDa protein. , 1993, The Journal of biological chemistry.

[79]  P. Layer,et al.  Müller glia cells and their possible roles during retina differentiation in vivo and in vitro. , 1998, Histology and histopathology.

[80]  J. Keefe,et al.  An analysis of urodelian retinal regeneration. II. Ultrastructural features of retinal regeneration in Notophthalmus viridescens. , 1973, The Journal of experimental zoology.

[81]  R. Wetts,et al.  Cell lineage analysis reveals multipotent precursors in the ciliary margin of the frog retina. , 1989, Developmental biology.

[82]  J. Janssen,et al.  4145 Characterization of monoclonal antibodies recognizing retinal pigment epithelial antigens , 1995, Vision Research.

[83]  M. Kelley,et al.  Retinoic acid promotes rod photoreceptor differentiation in rat retina in vivo. , 1999, Neuroreport.

[84]  P. Witkovsky,et al.  Serotonin-like immunoreactivity in the retina of the clawed frogXenopus laevis , 1990, Journal of neurocytology.

[85]  T. Kivelä.  Parvalbumin, a horizontal cell-associated calcium-binding protein in retinoblastoma eyes. , 1998, Investigative ophthalmology & visual science.

[86]  Viazovaia Ea,et al.  [Content of neurospecific protein S-100 in the brain of mice of different inbred lines]. , 1975 .

[87]  H. Wolburg,et al.  Regeneration of the goldfish retina after exposure to different doses of ouabain , 1979, Cell and Tissue Research.

[88]  Naomasa Miki,et al.  Expression of gicerin, a cell adhesion molecule, in the abnormal retina in silver plumage color mutation of Japanese quail (Coturnix japonica) , 1999, Neuroscience Letters.

[89]  T. Reh,et al.  Age of differentiation determines rat retinal germinal cell phenotype: induction of differentiation by dissociation , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[90]  E. Henderson,et al.  Isolation and Characterization of Glial Cell Lines from Xenopus Neuroepithelium and Retinal Pigment Epithelium , 1993 .

[91]  V. Mitashov.  [Autoradiographic study of the retinal regeneration in the newt (Triturus cristatus)]. , 1968, Doklady Akademii nauk SSSR.

[92]  Constance L. Cepko,et al.  A common progenitor for neurons and glia persists in rat retina late in development , 1987, Nature.

[93]  S. Matsuda,et al.  Functional expression and characterization of frog photoreceptor-specific calcium-binding proteins. , 1997, Biochemical and biophysical research communications.

[94]  M. Oguni,et al.  Calbindin-D 28 kD and parvalbumin in the horizontal cells of rat retina during development. , 1998, Current eye research.

[95]  Grigorian En,et al.  An analysis of keratin expression in the cells of the retinal pigment epithelium during transdifferentiation in newts , 1995 .

[96]  A. Milam,et al.  Guanylate-cyclase-inhibitory protein is a frog retinal Ca2+-binding protein related to mammalian guanylate-cyclase-activating proteins. , 1998, European Journal of Biochemistry.

[97]  P. Sterling,et al.  Identification of a G-protein in depolarizing rod bipolar cells , 1993, Visual Neuroscience.

[98]  E. Kicliter,et al.  Two groups of TH-like immunoreactive neurons in the frog (Rana pipiens) retina , 1999, Brain Research.

[99]  W. Thoreson,et al.  In vitro analysis of a mammalian retinal progenitor that gives rise to neurons and glia , 1999, Brain Research.

[100]  K. Goto,et al.  Visinin: A novel calcium binding protein expressed in retinal cone cells , 1990, Neuron.

[101]  R. Weiler,et al.  Immunocytochemical localization of serotonin in intracellularly analyzed and dye-injected ganglion cells of the turtle retina , 1986, Neuroscience Letters.

[102]  J. Nakajima,et al.  Monoamine oxidase-A-positive retinal ganglion cells projecting to the superior colliculus and dorsolateral geniculate nucleus of the rat brain. , 1998, Experimental eye research.

[103]  J. Jeanny,et al.  Analysis of opsin mRNA and protein expression in adult and regenerating newt retina by immunology and hybridization , 1992, Journal of neurocytology.

[104]  Rui,et al.  Synthesis of , 2001, Angewandte Chemie.

[105]  T. Belecky-Adams,et al.  Activin family members in the developing chick retina: expression patterns, protein distribution, and in vitro effects. , 1999, Developmental biology.

[106]  J. Dowling,et al.  Colocalization of immunoreactive substance P and neurotensin in amacrine cells of the goldfish retina , 1986, Brain Research.

[107]  C. Straznicky,et al.  Morphology and distribution of serotonin-like immunoreactive amacrine cells in the retina of Bufo marinus , 1990, Visual Neuroscience.

[108]  W. Harris,et al.  Xotch inhibits cell differentiation in the xenopus retina , 1995, Neuron.

[109]  M. D. Murphy,et al.  S-laminin expression in adult and developing retinae: A potential cue for photoreceptor morphogenesis , 1992, Neuron.

[110]  K. Negishi,et al.  An immunohistochemical study of regenerating newt retinas. , 1992, Brain research. Developmental brain research.

[111]  U. Wolfrum,et al.  Expression of centrin isoforms in the mammalian retina. , 1998, Experimental cell research.

[112]  Juliette Johnson,et al.  Expression of the somatostatin subtype 2A receptor in the rabbit retina , 1998, The Journal of comparative neurology.

[113]  W. Franklin,et al.  CD68 antigen expression by human retinal pigment epithelial cells. , 1992, Experimental eye research.

[114]  S. Easter,et al.  Retinal neurogenesis: the formation of the initial central patch of postmitotic cells. , 1999, Developmental biology.

[115]  C. Watt,et al.  Localization of serotoninlike‐immunoreactive amacrine cells in the larval tiger salamander retina , 1989, The Journal of comparative neurology.

[116]  S. Ying,et al.  Immunohistochemical localization of inhibin in the retinal interphotoreceptor matrix. , 1995, Experimental eye research.

[117]  P. Bovolenta,et al.  Neurotrophins and other growth factors in the generation of retinal neurons , 1999, Microscopy research and technique.

[118]  C. Barnstable,et al.  RET-PE10: a 61 kD polypeptide epitope expressed late during vertebrate RPE maturation. , 1993, Investigative ophthalmology & visual science.

[119]  Y. de Kozak,et al.  Retinal S antigen identified as the 48K protein regulating light-dependent phosphodiesterase in rods. , 1985, Science.

[120]  G. Ramı́rez,et al.  Spatial and Temporal Patterns of Neurogenesis in the Chick Retina. , 1991, The European journal of neuroscience.

[121]  C. Lillo,et al.  Enzyme histochemical identification of microglial cells in the retina of a fish (Tinca tinca) , 1999, Neuroscience Letters.

[122]  R. Adler,et al.  Differentiation of retinal precursor cells born in vitro. , 1992, Developmental biology.

[123]  W. Eldred,et al.  Synaptic microcircuitry of bipolar and amacrine cells with serotonin-like immunoreactivity in the retina of the turtle, Pseudemys scripta elegans , 1993, Visual Neuroscience.

[124]  S. Yazulla,et al.  GABA-like immunoreactivity in the vertebrate retina: a species comparison. , 1986, Experimental eye research.

[125]  M. Lee,et al.  Expression of CNTF in Müller cells of the rat retina after pressure-induced ischemia. , 1999, Neuroreport.

[126]  K. Negishi,et al.  Immunohistochemical and autoradiographic studies on retinal regeneration in teleost fish. , 1988, Neuroscience research. Supplement : the official journal of the Japan Neuroscience Society.

[127]  D. Herbert,et al.  Evidence that Müller cells can phagocytize egg-lecithin-coated silicone particles. , 1993, Tissue & cell.

[128]  F S Werblin,et al.  Amacrine cells in the tiger salamander retina: Morphology, physiology, and neurotransmitter identification , 1991, The Journal of comparative neurology.

[129]  R. M. Gaze,et al.  The growth of the retina in Xenopus laevis: an autoradiographic study. , 1971, Journal of embryology and experimental morphology.

[130]  J. Hollyfield,et al.  Serotoninergic neurons in the retina of Xenopus laevis: Selective staining, identification, development, and content , 1989, The Journal of comparative neurology.

[131]  K. Kunert,et al.  Microglia increase as photoreceptors decrease in the aging avian retina. , 1999, Current eye research.

[132]  R. Hunt,et al.  Altered expression of keratin and vimentin in human retinal pigment epithelial cells in vivo and in vitro , 1990, Journal of cellular physiology.

[133]  D. Altshuler,et al.  A temporally regulated, diffusible activity is required for rod photoreceptor development in vitro. , 1992, Development.

[134]  M. Lavail,et al.  Continuous exposure to bright light upregulates bFGF and CNTF expression in the rat retina. , 1998, Current eye research.

[135]  C. Barnstable,et al.  Differentiation and transdifferentiation of the retinal pigment epithelium. , 1997, International review of cytology.

[136]  C. Chiba.  Appearance of glutamate-like immunoreactivity during retinal regeneration in the adult newt , 1998, Brain Research.

[137]  C. Watt.  A double-label study demonstrating that all serotonin-like immunoreactive amacrine cells in the larval tiger salamander retina express GABA-like immunoreactivity , 1992, Brain Research.

[138]  T. Tully,et al.  Regulation of tyrosine hydroxylase-containing amacrine cell number in larval frog retina. , 1986, Developmental biology.

[139]  M. Hasegawa.  RESTITUTION OF THE EYE AFTER REMOVAL OF THE RETINA AND LENS IN THE NEWT, TRITVRUS PYRRHOGASTER* , 1958 .

[140]  Y. Sasai,et al.  Regulation of neural induction by the Chd and Bmp-4 antagonistic patterning signals in Xenopus , 1995, Nature.

[141]  W. Harris,et al.  Sequential genesis and determination of cone and rod photoreceptors in Xenopus. , 1998, Journal of neurobiology.

[142]  R. Adler,et al.  Plasticity and differentiation of embryonic retinal cells after terminal mitosis. , 1989, Science.