Cannabinoid receptor type 1 expression during postnatal development of the rat retina

Journal of Comparative Neurology

Volumn 519, Issue 7, 2011, Pages 1258-1280

  Zabouri, N ^a   Bouchard, J F ^a   Casanova, C ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

CB1R; Endocannabinoids; FAAH; Immunohistochemistry; NAPE PLD; Retinogenesis

Indexed keywords

CANNABINOID 1 RECEPTOR;

AGE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CELL STRUCTURE; CELL TYPE; CONTROLLED STUDY; DEVELOPMENTAL STAGE; IMMUNOHISTOCHEMISTRY; MITOSIS; MUELLER CELL; NEWBORN; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RETINA AMACRINE CELL; RETINA BIPOLAR GANGLION CELL; RETINA CONE; RETINA DEVELOPMENT; RETINA FUNCTION; RETINA GANGLION CELL; RETINA HORIZONTAL NERVE CELL; VISUAL SYSTEM FUNCTION; WESTERN BLOTTING;

ANIMALS; BIOLOGICAL MARKERS; ENDOCANNABINOIDS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEURONS; RATS; RATS, LONG-EVANS; RECEPTOR, CANNABINOID, CB1; RETINA;

EID: 79953139245     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.22534     Document Type: Article

References (144)

1. Acosta ML, Bumsted O'Brien KM, Tan SS, Kalloniatis M. 2008. Emergence of cellular markers and functional ionotropic glutamate receptors on tangentially dispersed cells in the developing mouse retina. J Comp Neurol 506: 506-523.
2. Ade KK, Lovinger DM. 2007. Anandamide regulates postnatal development of long-term synaptic plasticity in the rat dorsolateral striatum. J Neurosci 27: 2403-2409.
3. Aguado T, Monory K, Palazuelos J, Stella N, Cravatt B, Lutz B, Marsicano G, Kokaia Z, Guzman M, Galve-Roperh I. 2005. The endocannabinoid system drives neural progenitor proliferation. FASEB J 19: 1704-1706.
4. Argaw A, Duff G, Ptito M, Bouchard J-F. 2008. Contribution of the endocannabinoid CB1 receptor during axon guidance Program No. 624.1/B38. Neuroscience (2008) Abstracts. Washigton, DC: Society for Neuroscience. Online.
5. Argaw A, Duff G, Tea N, Ptito M, Bouchard J-F. 2009. The endocannabinoid system modulates axon guidance and target selection during development. Program No. 129.8/B29. Neuroscience (2009) Abstracts. Chicago, IL: Society for Neuroscience.
6. Bansal A, Singer JH, Hwang BJ, Xu W, Beaudet A, Feller MB. 2000. Mice lacking specific nicotinic acetylcholine receptor subunits exhibit dramatically altered spontaneous activity patterns and reveal a limited role for retinal waves in forming ON and OFF circuits in the inner retina. J Neurosci 20: 7672-7681.
7. Barker PA, Shooter EM. 1994. Disruption of NGF binding to the low affinity neurotrophin receptor p75LNTR reduces NGF binding to TrkA on PC12 cells. Neuron 13: 203-215.
8. Barnstable CJ, Hofstein R, Akagawa K. 1985. A marker of early amacrine cell development in rat retina. Brain Res 352: 286-290.
9. Barton KM, Levine EM. 2008. Expression patterns and cell cycle profiles of PCNA, MCM6, cyclin D1, cyclin A2, cyclin B1, and phosphorylated histone H3 in the developing mouse retina. Dev Dyn 237: 672-682.
10. Baye LM, Link BA. 2007. Interkinetic nuclear migration and the selection of neurogenic cell divisions during vertebrate retinogenesis. J Neurosci 27: 10143-10152.
11. Baye LM, Link BA. 2008. Nuclear migration during retinal development. Brain Res 1192: 29-36.
12. Begbie J, Doherty P, Graham A. 2004. Cannabinoid receptor, CB1, expression follows neuronal differentiation in the early chick embryo. J Anat 205: 213-218.
13. Belue RC, Howlett AC, Westlake TM, Hutchings DE. 1995. The ontogeny of cannabinoid receptors in the brain of postnatal and aging rats. Neurotoxicol Teratol 17: 25-30.
14. Berghuis P, Dobszay MB, Wang X, Spano S, Ledda F, Sousa KM, Schulte G, Ernfors P, Mackie K, Paratcha G, Hurd YL, Harkany T. 2005. Endocannabinoids regulate interneuron migration and morphogenesis by transactivating the TrkB receptor. Proc Natl Acad Sci U S A 102: 19115-19120.
15. Berghuis P, Rajnicek AM, Morozov YM, Ross RA, Mulder J, Urban GM, Monory K, Marsicano G, Matteoli M, Canty A, Irving AJ, Katona I, Yanagawa Y, Rakic P, Lutz B, Mackie K, Harkany T. 2007. Hardwiring the brain: endocannabinoids shape neuronal connectivity. Science 316: 1212-1216.
16. Bernard C, Milh M, Morozov YM, Ben-Ari Y, Freund TF, Gozlan H. 2005. Altering cannabinoid signaling during development disrupts neuronal activity. Proc Natl Acad Sci U S A 102: 9388-9393.
17. Berrendero F, Sepe N, Ramos JA, Di Marzo V, Fernandez-Ruiz JJ. 1999. Analysis of cannabinoid receptor binding and mRNA expression and endogenous cannabinoid contents in the developing rat brain during late gestation and early postnatal period. Synapse 33: 181-191.
18. Bramblett DE, Pennesi ME, Wu SM, Tsai MJ. 2004. The transcription factor Bhlhb4 is required for rod bipolar cell maturation. Neuron 43: 779-793.
19. Brandon C. 1985. Improved immunocytochemical staining through the use of Fab fragments of primary antibody, Fab-specific second antibody, and Fab-horseradish peroxidase. J Histochem Cytochem 33: 715-719.
20. Buckley NE, Hansson S, Harta G, Mezey E. 1998. Expression of the CB1 and CB2 receptor messenger RNAs during embryonic development in the rat. Neuroscience 82: 1131-1149.
21. Chang ML, Wu CH, Jiang-Shieh YF, Shieh JY, Wen CY. 2007. Reactive changes of retinal astrocytes and Muller glial cells in kainate-induced neuroexcitotoxicity. J Anat 210: 54-65.
22. Cinar O, Semiz O, Can A. 2006. A microscopic survey on the efficiency of well-known routine chemical fixatives on cryosections. Acta Histochem 108: 487-496.
23. Coleman JE, Zhang Y, Brown GA, Semple-Rowland SL. 2004. Cone cell survival and downregulation of GCAP1 protein in the retinas of GC1 knockout mice. Invest Ophthalmol Vis Sci 45: 3397-3403.
24. Cravatt BF, Giang DK, Mayfield SP, Boger DL, Lerner RA, Gilula NB. 1996. Molecular characterization of an enzyme that degrades neuromodulatory fatty-acid amides. Nature 384: 83-87.
25. Cravatt BF, Demarest K, Patricelli MP, Bracey MH, Giang DK, Martin BR, Lichtman AH. 2001. Supersensitivity to anandamide and enhanced endogenous cannabinoid signaling in mice lacking fatty acid amide hydrolase. Proc Natl Acad Sci U S A 98: 9371-9376.
26. Deutsch DG, Chin SA. 1993. Enzymatic synthesis and degradation of anandamide, a cannabinoid receptor agonist. Biochem Pharmacol 46: 791-796.
27. Dhingra NK, Ramamohan Y, Raju TR. 1997. Developmental expression of synaptophysin, synapsin I and syntaxin in the rat retina. Brain Res Dev Brain Res 102: 267-273.
28. Egertova M, Giang DK, Cravatt BF, Elphick MR. 1998. A new perspective on cannabinoid signalling: complementary localization of fatty acid amide hydrolase and the CB1 receptor in rat brain. Proc Biol Sci 265: 2081-2085.
29. Elshatory Y, Deng M, Xie X, Gan L. 2007. Expression of the LIM-homeodomain protein Isl1 in the developing and mature mouse retina. J Comp Neurol 503: 182-197.
30. Fan SF, Yazulla S. 2003. Biphasic modulation of voltage-dependent currents of retinal cones by cannabinoid CB1 receptor agonist WIN 55212-2. Vis Neurosci 20: 177-188.
31. Fan SF, Yazulla S. 2007. Retrograde endocannabinoid inhibition of goldfish retinal cones is mediated by 2-arachidonoyl glycerol. Vis Neurosci 24: 257-267.
32. Fei Y. 2003. Development of the cone photoreceptor mosaic in the mouse retina revealed by fluorescent cones in transgenic mice. Mol Vis 9: 31-42.
33. Feller MB, Wellis DP, Stellwagen D, Werblin FS, Shatz CJ. 1996. Requirement for cholinergic synaptic transmission in the propagation of spontaneous retinal waves. Science 272: 1182-1187.
34. Fletcher EL, Kalloniatis M. 1997. Localisation of amino acid neurotransmitters during postnatal development of the rat retina. J Comp Neurol 380: 449-471.
35. Freund TF, Katona I, Piomelli D. 2003. Role of endogenous cannabinoids in synaptic signaling. Physiol Rev 83: 1017- 1066.
36. Fride E. 2008. Multiple roles for the endocannabinoid system during the earliest stages of life: pre- and postnatal development. J Neuroendocrinol 20(suppl 1): 75-81.
37. Galli-Resta L, Ensini M. 1996. An intrinsic time limit between genesis and death of individual neurons in the developing retinal ganglion cell layer. J Neurosci 16: 2318-2324.
38. Gaillard F, Bonfield S, Gilmour GS, Kuny S, Mema SC, Martin BT, Smale L, Crowder N, Stell WK, Sauve Y. 2008. Retinal anatomy and visual performance in a diurnal cone-rich laboratory rodent, the Nile grass rat (Arvicanthis niloticus). J Comp Neurol 510: 525-538.
39. Galve-Roperh I, Aguado T, Rueda D, Velasco G, Guzman M. 2006. Endocannabinoids: a new family of lipid mediators involved in the regulation of neural cell development. Curr Pharm Des 12: 2319-2325.
40. Gao Y, Vasilyev DV, Goncalves MB, Howell FV, Hobbs C, Reisenberg M, Shen R, Zhang MY, Strassle BW, Lu P, Mark L, Piesla MJ, Deng K, Kouranova EV, Ring RH, Whiteside GT, Bates B, Walsh FS, Williams G, Pangalos MN, Samad TA, Doherty P. 2010. Loss of retrograde endocannabinoid signaling and reduced adult neurogenesis in diacylglycerol lipase knock-out mice. J Neurosci 30: 2017-2024.
41. Gargini C, Terzibasi E, Mazzoni F, Strettoi E. 2007. Retinal organization in the retinal degeneration 10 (rd10) mutant mouse: a morphological and ERG study. J Comp Neurol 500: 222-238.
42. Ghosh KK, Bujan S, Haverkamp S, Feigenspan A, Wassle H. 2004. Types of bipolar cells in the mouse retina. J Comp Neurol 469: 70-82.
43. Gomez M, Hernandez M, Johansson B, de Miguel R, Ramos JA, Fernandez-Ruiz J. 2003. Prenatal cannabinoid and gene expression for neural adhesion molecule L1 in the fetal rat brain. Brain Res Dev Brain Res 147: 201-207.
44. Gomez M, Hernandez M, Fernandez-Ruiz J. 2007. The activation of cannabinoid receptors during early postnatal development reduces the expression of cell adhesion molecule L1 in the rat brain. Brain Res 1145: 48-55.
45. Gomez M, Hernandez M, Fernandez-Ruiz J. 2008a. Cannabinoid signaling system: does it play a function in cell proliferation and migration, neuritic elongation and guidance and synaptogenesis during brain ontogenesis? Cell Adh Migr 2: 246-248.
46. Gomez M, Hernandez ML, Pazos MR, Tolon RM, Romero J, Fernandez-Ruiz J. 2008b. Colocalization of CB1 receptors with L1 and GAP-43 in forebrain white matter regions during fetal rat brain development: evidence for a role of these receptors in axonal growth and guidance. Neuroscience 153: 687-699.
47. Goldenthal KL, Hedman K, Chen JW, August JT, Willingham MC. 1985. Postfixation detergent treatment for immunofluorescence suppresses localization of some integral membrane proteins. J Histochem Cytochem 33: 813-820.
48. Hack I, Koulen P, Peichl L, Brandstatter JH. 2002. Development of glutamatergic synapses in the rat retina: the postnatal expression of ionotropic glutamate receptor subunits. Vis Neurosci 19: 1-13.
49. Haque ME, Thomas KJ, D'Souza C, Callaghan S, Kitada T, Slack RS, Fraser P, Cookson MR, Tandon A, Park DS. 2008. Cytoplasmic Pink1 activity protects neurons from dopaminergic neurotoxin MPTP. Proc Natl Acad Sci U S A 105: 1716-1721.
50. Harkany T, Keimpema E, Barabas K, Mulder J. 2008. Endocannabinoid functions controlling neuronal specification during brain development. Mol Cell Endocrinol 286(suppl 1): S84-90.
51. Haverkamp S, Wässle H. 2000. Immunocytochemical analysis of the mouse retina. J Comp Neurol 424: 1-23.
52. Haverkamp S, Ghosh KK, Hirano AA, Wässle H. 2003. Immunocytochemical description of five bipolar cell types of the mouse retina. J Comp Neurol 455(4): 463-476.
53. Herkenham M. 1991. Characterization and localization of cannabinoid receptors in brain: an in vitro technique using slide-mounted tissue sections. NIDA Res Monogr 112: 129-145.
54. Hill MN, Kambo JS, Sun JC, Gorzalka BB, Galea LA. 2006. Endocannabinoids modulate stress-induced suppression of hippocampal cell proliferation and activation of defensive behaviours. Eur J Neurosci 24: 1845-1849.
55. Hirano AA, Brandstatter JH, Brecha NC. 2005. Cellular distribution and subcellular localization of molecular components of vesicular transmitter release in horizontal cells of rabbit retina. J Comp Neurol 488: 70-81.
56. Hojo M, Ohtsuka T, Hashimoto N, Gradwohl G, Guillemot F, Kageyama R. 2000. Glial cell fate specification modulated by the bHLH gene Hes5 in mouse retina. Development 127: 2515-2522.
57. Ino H, Chiba T. 2000. Expression of proliferating cell nuclear antigen (PCNA) in the adult and developing mouse nervous system. Brain Res Mol Brain Res 78: 163-174.
58. Inoue A, Obata K, Akagawa K. 1992. Cloning and sequence analysis of cDNA for a neuronal cell membrane antigen, HPC-1. J Biol Chem 267: 10613-10619.
59. Johnson PT, Williams RR, Reese BE. 2001. Developmental patterns of protein expression in photoreceptors implicate distinct environmental versus cell-intrinsic mechanisms. Vis Neurosci 18: 157-168.
60. Kanda A, Swaroop A. 2009. A comprehensive analysis of sequence variants and putative disease-causing mutations in photoreceptor-specific nuclear receptor NR2E3. Mol Vis 15: 2174-2184.
61. Kim D, Thayer SA. 2001. Cannabinoids inhibit the formation of new synapses between hippocampal neurons in culture. J Neurosci 21: RC146.
62. Kim DS, Ross SE, Trimarchi JM, Aach J, Greenberg ME, Cepko CL. 2008. Identification of molecular markers of bipolar cells in the murine retina. J Comp Neurol 507: 1795-1810.
63. Kobayashi M, Takezawa S, Hara K, Yu RT, Umesono Y, Agata K, Taniwaki M, Yasuda K, Umesono K. 1999. Identification of a photoreceptor cell-specific nuclear receptor. Proc Natl Acad Sci U S A 96: 4814-4819.
64. Kreitzer AC, Regehr WG. 2002. Retrograde signaling by endocannabinoids. Curr Opin Neurobiol 12: 324-330.
65. Lalonde MR, Jollimore CA, Stevens K, Barnes S, Kelly ME. 2006. Cannabinoid receptor-mediated inhibition of calcium signaling in rat retinal ganglion cells. Mol Vis 12: 1160-1166.
66. Leonelli M, Britto LR, Chaves GP, Torrao AS. 2005. Developmental expression of cannabinoid receptors in the chick retinotectal system. Brain Res Dev Brain Res 156: 176-182.
67. Leu S, Ouyang P. 2006. Spatial and temporal expression profile of pinin during mouse development. Gene Expr Patterns 6: 620-631.
68. Li L, Bender KJ, Drew PJ, Jadhav SP, Sylwestrak E, Feldman DE. 2009. Endocannabinoid signaling is required for development and critical period plasticity of the whisker map in somatosensory cortex. Neuron 64: 537-549.
69. Li S, Mo Z, Yang X, Price SM, Shen MM, Xiang M. 2004. Foxn4 controls the genesis of amacrine and horizontal cells by retinal progenitors. Neuron 43: 795-807.
70. Li Y, Zheng H, Liu PP, Chen YY, She ZJ, Xiao HL, Zhou GM. 2010. The new targets of ouabain in retinal interneurons of Sprague-Dawley rats. Brain Res Bull 81: 617-624.
71. Mailleux P, Parmentier M, Vanderhaeghen JJ. 1992. Distribution of cannabinoid receptor messenger RNA in the human brain: an in situ hybridization histochemistry with oligonucleotides. Neurosci Lett 143: 200-204.
72. Malicki J. 2004. Cell fate decisions and patterning in the vertebrate retina: the importance of timing, asymmetry, polarity and waves. Curr Opin Neurobiol 14: 15-21.
73. Marsicano G, Wotjak CT, Azad SC, Bisogno T, Rammes G, Cascio MG, Hermann H, Tang J, Hofmann C, Zieglgansberger W, Di Marzo V, Lutz B. 2002. The endogenous cannabinoid system controls extinction of aversive memories. Nature 418: 530-534.
74. Masland RH, Mills JW, Hayden SA. 1984. Acetylcholine-synthesizing amacrine cells: identification and selective staining by using radioautography and fluorescent markers. Proc R Soc Lond B 223: 79-100.
75. Mayor S, Maxfield FR. 1995. Insolubility and redistribution of GPI-anchored proteins at the cell surface after detergent treatment. Mol Biol Cell 6: 929-944.
76. McGinnis JF, Stepanik PL, Baehr W, Subbaraya I, Lerious V. 1992a. Cloning and sequencing of the 23 kDa mouse photoreceptor cell-specific protein. FEBS Lett 302: 172-176.
77. McGinnis JF, Whelan JP, Donoso LA. 1992b. Transient, cyclic changes in mouse visual cell gene products during the light-dark cycle. J Neurosci Res 31: 584-590.
78. McGinnis JF, Stepanik PL, Jariangprasert S, Lerious V. 1997. Functional significance of recoverin localization in multiple retina cell types. J Neurosci Res 50: 487-495.
79. McKinney MK, Cravatt BF. 2005. Structure and function of fatty acid amide hydrolase. Annu Rev Biochem 74: 411-432.
80. McLaughlin CR, Abood ME. 1993. Developmental expression of cannabinoid receptor mRNA. Brain Res Dev Brain Res 76: 75-78.
81. McLaughlin T, Torborg CL, Feller MB, O'Leary DD. 2003. Retinotopic map refinement requires spontaneous retinal waves during a brief critical period of development. Neuron 40: 1147-1160.
82. Melan MA, Sluder G. 1992. Redistribution and differential extraction of soluble proteins in permeabilized cultured cells. Implications for immunofluorescence microscopy. J Cell Sci 101: 731-743.
83. Micheva KD, Vallee A, Beaulieu C, Herman IM, Leclerc N. 1998. beta-Actin is confined to structures having high capacity of remodelling in developing and adult rat cerebellum. Eur J Neurosci 10: 3785-3798.
84. Milam AH, Dacey DM, Dizhoor AM. 1993. Recoverin immunoreactivity in mammalian cone bipolar cells. Vis Neurosci 10: 1-12.
85. Mitchell CK, Huang B, Redburn-Johnson DA. 1999. GABA(A) receptor immunoreactivity is transiently expressed in the developing outer retina. Vis Neurosci 16: 1083-1088.
86. Morest DK. 1970. The pattern of neurogenesis in the retina of the rat. Z Anat Entwicklungsgesch 131: 45-67.
87. Morgan JL, Dhingra A, Vardi N, Wong RO. 2006. Axons and dendrites originate from neuroepithelial-like processes of retinal bipolar cells. Nat Neurosci 9: 85-92.
88. Morishita J, Okamoto Y, Tsuboi K, Ueno M, Sakamoto H, Maekawa N, Ueda N. 2005. Regional distribution and age-dependent expression of N-acylphosphatidylethanolamine-hydrolyzing phospholipase D in rat brain. J Neurochem 94: 753-762.
89. Morrow EM, Chen CM, Cepko CL. 2008. Temporal order of bipolar cell genesis in the neural retina. Neural Dev 3: 2.
90. Mulder J, Aguado T, Keimpema E, Barabas K, Ballester Rosado CJ, Nguyen L, Monory K, Marsicano G, Di Marzo V, Hurd YL, Guillemot F, Mackie K, Lutz B, Guzman M, Lu HC, Galve-Roperh I, Harkany T. 2008. Endocannabinoid signaling controls pyramidal cell specification and long-range axon patterning. Proc Natl Acad Sci U S A 105: 8760-8765.
91. Nag TC, Wadhwa S. 2001. Differential expression of syntaxin-1 and synaptophysin in the developing and adult human retina. J Biosci 26: 179-191.
92. Nagar S, Krishnamoorthy V, Cherukuri P, Jain V, Dhingra NK. 2009. Early remodeling in an inducible animal model of retinal degeneration. Neuroscience 160: 517-529.
93. Negishi K, Kato S, Teranishi T. 1988. Dopamine cells and rod bipolar cells contain protein kinase C-like immunoreactivity in some vertebrate retinas. Neurosci Lett 94: 247-252.
94. Nicholson DA, Geinisman Y. 2009. Axospinous synaptic subtype-specific differences in structure, size, ionotropic receptor expression, and connectivity in apical dendritic regions of rat hippocampal CA1 pyramidal neurons. J Comp Neurol 512: 399-418.
95. Nucci C, Gasperi V, Tartaglione R, Cerulli A, Terrinoni A, Bari M, De Simone C, Agro AF, Morrone LA, Corasaniti MT, Bagetta G, Maccarrone M. 2007. Involvement of the endocannabinoid system in retinal damage after high intraocular pressure-induced ischemia in rats. Invest Ophthalmol Vis Sci 48: 2997-3004.
96. Okamoto Y, Morishita J, Tsuboi K, Tonai T, Ueda N. 2004. Molecular characterization of a phospholipase D generating anandamide and its congeners. J Biol Chem 279: 5298-5305.
97. Ono M, Murakami T, Kudo A, Isshiki M, Sawada H, Segawa A. 2001. Quantitative comparison of anti-fading mounting media for confocal laser scanning microscopy. J Histochem Cytochem 49: 305-312.
98. Pan L, Yang Z, Feng L, Gan L. 2005. Functional equivalence of Brn3 POU-domain transcription factors in mouse retinal neurogenesis. Development 132: 703-712.
99. Perry VH, Henderson Z, Linden R. 1983. Postnatal changes in retinal ganglion cell and optic axon populations in the pigmented rat. J Comp Neurol 219: 356-368.
100. Poche RA, Furuta Y, Chaboissier MC, Schedl A, Behringer RR. 2008. Sox9 is expressed in mouse multipotent retinal progenitor cells and functions in Muller glial cell development. J Comp Neurol 510: 237-250.
101. Porcella A, Maxia C, Gessa GL, Pani L. 2000. The human eye expresses high levels of CB1 cannabinoid receptor mRNA and protein. Eur J Neurosci 12: 1123-1127.
102. Quina LA, Pak W, Lanier J, Banwait P, Gratwick K, Liu Y, Velasquez T, O'Leary DD, Goulding M, Turner EE. 2005. Brn3a-expressing retinal ganglion cells project specifically to thalamocortical and collicular visual pathways. J Neurosci 25: 11595-11604.
103. Rapaport DH, Wong LL, Wood ED, Yasumura D, LaVail MM. 2004. Timing and topography of cell genesis in the rat retina. J Comp Neurol 474: 304-324.
104. Raven MA, Orton NC, Nassar H, Williams GA, Stell WK, Jacobs GH, Bech-Hansen NT, Reese BE. 2008. Early afferent signaling in the outer plexiform layer regulates development of horizontal cell morphology. J Comp Neurol 506: 745-758.
105. Rich KA, Zhan Y, Blanks JC. 1997. Migration and synaptogenesis of cone photoreceptors in the developing mouse retina. J Comp Neurol 388: 47-63.
106. Riepe RE, Norenburg MD. 1977. Muller cell localisation of glutamine synthetase in rat retina. Nature 268: 654-655.
107. Riepe RE, Norenberg MD. 1978. Glutamine synthetase in the developing rat retina: an immunohistochemical study. Exp Eye Res 27: 435-444.
108. Rimmerman N, Hughes HV, Bradshaw HB, Pazos MX, Mackie K, Prieto AL, Walker JM. 2008. Compartmentalization of endocannabinoids into lipid rafts in a dorsal root ganglion cell line. Br J Pharmacol 153: 380-389.
109. Rodriguez de Fonseca F, Ramos JA, Bonnin A, Fernandez-Ruiz JJ. 1993. Presence of cannabinoid binding sites in the brain from early postnatal ages. Neuroreport 4: 135-138.
110. Schnitzer J, Rusoff AC. 1984. Horizontal cells of the mouse retina contain glutamic acid decarboxylase-like immunoreactivity during early developmental stages. J Neurosci 4: 2948-2955.
111. Schroeter EH, Wong RO, Gregg RG. 2006. In vivo development of retinal ON-bipolar cell axonal terminals visualized in nyx:: MYFP transgenic zebrafish. Vis Neurosci 23: 833-843.
112. Sernagor E, Eglen SJ, O'Donovan MJ. 2000. Differential effects of acetylcholine and glutamate blockade on the spatiotemporal dynamics of retinal waves. J Neurosci 20: RC56.
113. Sharma RK, O'Leary TE, Fields CM, Johnson DA. 2003. Development of the outer retina in the mouse. Brain Res Dev Brain Res 145: 93-105.
114. Sherry DM, Wang MM, Bates J, Frishman LJ. 2003. Expression of vesicular glutamate transporter 1 in the mouse retina reveals temporal ordering in development of rod vs. cone and ON vs. OFF circuits. J Comp Neurol 465: 480-498.
115. Song ZH, Zhong M. 2000. CB1 cannabinoid receptor-mediated cell migration. J Pharmacol Exp Ther 294: 204-209.
116. Stacy RC, Demas J, Burgess RW, Sanes JR, Wong RO. 2005. Disruption and recovery of patterned retinal activity in the absence of acetylcholine. J Neurosci 25: 9347-9357.
117. Straiker A, Sullivan JM. 2003. Cannabinoid receptor activation differentially modulates ion channels in photoreceptors of the tiger salamander. J Neurophysiol 89: 2647-2654.
118. Straiker A, Stella N, Piomelli D, Mackie K, Karten HJ, Maguire G. 1999. Cannabinoid CB1 receptors and ligands in vertebrate retina: localization and function of an endogenous signaling system. Proc Natl Acad Sci U S A 96: 14565- 14570.
119. Struik ML, Yazulla S, Kamermans M. 2006. Cannabinoid agonist WIN 55212-2 speeds up the cone response to light offset in goldfish retina. Vis Neurosci 23: 285-293.
120. Suarez J, Bermudez-Silva FJ, Mackie K, Ledent C, Zimmer A, Cravatt BF, de Fonseca FR. 2008. Immunohistochemical description of the endogenous cannabinoid system in the rat cerebellum and functionally related nuclei. J Comp Neurol 509: 400-421.
121. Suarez J, Romero-Zerbo SY, Rivera P, Bermudez-Silva FJ, Perez J, De Fonseca FR, Fernandez-Llebrez P. 2010. Endocannabinoid system in the adult rat circumventricular areas: an immunohistochemical study. J Comp Neurol 518: 3065-3085.
122. Syed MM, Lee S, Zheng J, Zhou ZJ. 2004. Stage-dependent dynamics and modulation of spontaneous waves in the developing rabbit retina. J Physiol 560: 533-549.
123. Tauchi M, Masland RH. 1984. The shape and arrangement of the cholinergic neurons in the rabbit retina. Proc R Soc Lond B 223: 101-119.
124. Thomas EA, Cravatt BF, Danielson PE, Gilula NB, Sutcliffe JG. 1997. Fatty acid amide hydrolase, the degradative enzyme for anandamide and oleamide, has selective distribution in neurons within the rat central nervous system. J Neurosci Res 50: 1047-1052.
125. Torborg CL, Feller MB. 2005. Spontaneous patterned retinal activity and the refinement of retinal projections. Prog Neurobiol 76: 213-235.
126. Turu G, Hunyady L. Signal transduction of the CB1 cannabinoid receptor. J Mol Endocrinol 44: 75-85.
127. Voinescu PE, Kay JN, Sanes JR. 2009. Birthdays of retinal amacrine cell subtypes are systematically related to their molecular identity and soma position. J Comp Neurol 517: 737-750.
128. Wang H, Xie H, Sun X, Kingsley PJ, Marnett LJ, Cravatt BF, Dey SK. 2007. Differential regulation of endocannabinoid synthesis and degradation in the uterus during embryo implantation. Prostaglandins Other Lipid Mediat 83: 62-74.
129. Warrier A, Wilson M. 2007. Endocannabinoid signaling regulates spontaneous transmitter release from embryonic retinal amacrine cells. Vis Neurosci 24: 25-35.
130. Waseem NH, Lane DP. 1990. Monoclonal antibody analysis of the proliferating cell nuclear antigen (PCNA). Structural conservation and the detection of a nucleolar form. J Cell Sci 96: 121-129.
131. Weinberger R, Schevzov G, Jeffrey P, Gordon K, Hill M, Gunning P. 1996. The molecular composition of neuronal microfilaments is spatially and temporally regulated. J Neurosci 16: 238-252.
132. Westlake TM, Howlett AC, Bonner TI, Matsuda LA, Herkenham M. 1994. Cannabinoid receptor binding and messenger RNA expression in human brain: an in vitro receptor autoradiography and in situ hybridization histochemistry study of normal aged and Alzheimer's brains. Neuroscience 63: 637-652.
133. Williams EJ, Walsh FS, Doherty P. 2003. The FGF receptor uses the endocannabinoid signaling system to couple to an axonal growth response. J Cell Biol 160: 481-486.
134. Wong WT, Myhr KL, Miller ED, Wong RO. 2000. Developmental changes in the neurotransmitter regulation of correlated spontaneous retinal activity. J Neurosci 20: 351-360.
135. Xue J, Li G, Laabich A, Cooper NG. 2001. Visual-mediated regulation of retinal CaMKII and its GluR1 substrate is age-dependent. Brain Res Mol Brain Res 93: 95-104.
136. Yan XX, Wiechmann AF. 1997. Early expression of recoverin in a unique population of neurons in the human retina. Anat Embryol (Berl) 195: 51-63.
137. Yazulla S. 2008. Endocannabinoids in the retina: from marijuana to neuroprotection. Prog Retin Eye Res 27: 501- 526.
138. Yazulla S, Studholme KM, McIntosh HH, Deutsch DG. 1999. Immunocytochemical localization of cannabinoid CB1 receptor and fatty acid amide hydrolase in rat retina. J Comp Neurol. 1999; 12: 80-90.
139. Yazulla S, Studholme KM, McIntosh HH, Fan SF. 2000. Cannabinoid receptors on goldfish retinal bipolar cells: electron-microscope immunocytochemistry and whole-cell recordings. Vis Neurosci 17: 391-401.
140. Zabouri N, Bouchard J-F, Casanova C. 2007. Expression of the endocannabinoid receptor CB1 and the FAAH enzyme during retinal development in the rat. Program No. 461.23/F39 Neuroscience (2007) Abstracts. San Diego, CA: Society for Neuroscience.
141. Zabouri N, Bouchard J-F, Casanova C. Expression of the NAPE-PLD, CB1 receptors, and FAAH during retinal development. Program No. 723.15/C19. Neuroscience (2008) Abstracts. Washington, DC: Society for Neuroscience.
142. Zheng J, Lee S, Zhou ZJ. 2006. A transient network of intrinsically bursting starburst cells underlies the generation of retinal waves. Nat Neurosci 9: 363-371.
143. Zhou ZJ. 1998. Direct participation of starburst amacrine cells in spontaneous rhythmic activities in the developing mammalian retina. J Neurosci 18: 4155-4165.
144. Zhou ZJ, Zhao D. 2000. Coordinated transitions in neurotransmitter systems for the initiation and propagation of spontaneous retinal waves. J Neurosci 20: 6570-6577.