Müller cells express the cannabinoid CB2 receptor in the vervet monkey retina

Journal of Comparative Neurology

Volumn 521, Issue 11, 2013, Pages 2399-2415

  Bouskila, Joseph ^a   Javadi, Pasha ^a   Casanova, Christian ^a   Ptito, Maurice ^a,b   Bouchard, Jean François ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

CB1R; CB2R; Confocal microscopy; Endocannabinoids; Immunofluorescence; Retinal glia

Indexed keywords

CALBINDIN; CANNABINOID 1 RECEPTOR; CANNABINOID 2 RECEPTOR; GLUTAMATE AMMONIA LIGASE; IMMUNOGLOBULIN G; MONOCLONAL ANTIBODY; PARVALBUMIN; PROTEIN KINASE C; SYNTAXIN; TRANSCRIPTION FACTOR POU4F1;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL MEMBRANE; CELLULAR DISTRIBUTION; CHLOROCEBUS; CONFOCAL MICROSCOPY; GLIA CELL; IMMUNOHISTOCHEMISTRY; MUELLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RETINA; RETINA NERVE CELL;

AMACRINE CELLS; ANIMALS; ANTIBODIES; BLOTTING, WESTERN; CANNABINOID RECEPTOR ANTAGONISTS; CERCOPITHECUS AETHIOPS; EPENDYMOGLIAL CELLS; EXCITATORY POSTSYNAPTIC POTENTIALS; IMMUNOHISTOCHEMISTRY; MICROSCOPY, CONFOCAL; NERVE TISSUE PROTEINS; NEURONS; RECEPTOR, CANNABINOID, CB1; RECEPTOR, CANNABINOID, CB2; RETINA; RETINAL BIPOLAR CELLS; RETINAL CONE PHOTORECEPTOR CELLS; RETINAL GANGLION CELLS; RETINAL HORIZONTAL CELLS;

EID: 84878627548     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23333     Document Type: Article

References (74)

1. Argaw A, Duff G, Cherif H, Cécyre B, Tea N, Bouchard J-F. 2011. Cannabinoid receptor CB2 modulates axon guidance. Abstract B045, 8th IBRO World Congress on Neuroscience, Firenze, Italy.
2. Atwood BK, Mackie K. 2010. CB2: a cannabinoid receptor with an identity crisis. Br J Pharmacol 160: 467-479.
3. Barnstable CJ, Hofstein R, Akagawa K. 1985. A marker of early amacrine cell development in rat retina. Brain Res 352: 286-290.
4. Bolognini D, Costa B, Maione S, Comelli F, Marini P, Di Marzo V, Parolaro D, Ross RA, Gauson LA, Cascio MG, Pertwee RG. 2010. The plant cannabinoid delta9-tetrahydrocannabivarin can decrease signs of inflammation and inflammatory pain in mice. Br J Pharmacol 160: 677-687.
5. Bordt A, Hoshi H, Yamada E, Perryman Stout W, Marshak D. 2006. Synaptic input to Off parasol ganglion cells in macaque retina. J Comp Neurol 498: 46-57.
6. Bouskila J, Burke MW, Zabouri N, Casanova C, Ptito M, Bouchard JF. 2012. Expression and localization of the cannabinoid receptor type 1 and the enzyme fatty acid amide hydrolase in the retina of vervet monkeys. Neuroscience 202: 117-130.
7. 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.
8. 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.
9. Burke M, Zangenehpour S, Bouskila J, Boire D, Ptito M. 2009. The gateway to the brain: dissecting the primate eye. J Vis Exp e1261.
10. Cabral GA, Raborn ES, Griffin L, Dennis J, Marciano-Cabral F. 2008. CB2 receptors in the brain: role in central immune function. Br J Pharmacol 153: 240-251.
11. Carrier EJ, Kearn CS, Barkmeier AJ, Breese NM, Yang W, Nithipatikom K, Pfister SL, Campbell WB, Hillard CJ. 2004. Cultured rat microglial cells synthesize the endocannabinoid 2-arachidonylglycerol, which increases proliferation via a CB2 receptor-dependent mechanism. Mol Pharmacol 65: 999-1007.
12. Chen J, Matias I, Dinh T, Lu T, Venezia S, Nieves A, Woodward DF, Di Marzo V. 2005. Finding of endocannabinoids in human eye tissues: implications for glaucoma. Biochem Biophys Res Commun 330: 1062-1067.
13. Chiquet C, Dkhissi-Benyahya O, Chounlamountri N, Szel A, Degrip WJ, Cooper HM. 2002. Characterization of calbindin-positive cones in primates. Neuroscience 115: 1323-1333.
14. 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.
15. Cuenca N, Herrero MT, Angulo A, de Juan E, Martínez-Navarrete GC, López S, Barcia C, Martín-Nieto J. 2005. Morphological impairments in retinal neurons of the scotopic visual pathway in a monkey model of Parkinson's disease. J Comp Neurol 493: 261-273.
16. Devane WA, Hanus L, Breuer A, Pertwee RG, Stevenson LA, Griffin G, Gibson D, Mandelbaum A, Etinger A, Mechoulam R. 1992. Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science 258: 1946-1949.
17. Di Marzo V, Bisogno T, De Petrocellis L. 2007. Endocannabinoids and related compounds: walking back and forth between plant natural products and animal physiology. Chem Biol 14: 741-756.
18. Dinh TP, Carpenter D, Leslie FM, Freund TF, Katona I, Sensi SL, Kathuria S, Piomelli D. 2002. Brain monoglyceride lipase participating in endocannabinoid inactivation. Proc Natl Acad Sci U S A 99: 10819-10824.
19. Distler C, Dreher Z. 1996. Glia cells of the monkey retina-II. Müller cells. Vis Res 36: 2381-2394.
20. Eljaschewitsch E, Witting A, Mawrin C, Lee T, Schmidt P, Wolf S, Hoertnagl H, Raine C, Schneider Stock R, Nitsch R, Ullrich O. 2006. The endocannabinoid anandamide protects neurons during CNS inflammation by induction of MKP-1 in microglial cells. Neuron 49: 67-79.
21. Ellert-Miklaszewska A, Grajkowska W, Gabrusiewicz K, Kaminska B, Konarska L. 2007. Distinctive pattern of cannabinoid receptor type II (CB2) expression in adult and pediatric brain tumors. Brain Res 1137: 161-169.
22. Fischer AJ, Hendrickson A, Reh TA. 2001. Immunocytochemical characterization of cysts in the peripheral retina and pars plana of the adult primate. Invest Ophthalmol Vis Sci 42: 3256-3263.
23. Galiègue S, Mary S, Marchand J, Dussossoy D, Carrière D, Carayon P, Bouaboula M, Shire D, Le Fur G, Casellas P. 1995. Expression of central and peripheral cannabinoid receptors in human immune tissues and leukocyte subpopulations. Eur J Biochem 232: 54-61.
24. Griffin G, Tao Q, Abood ME. 2000. Cloning and pharmacological characterization of the rat CB2 cannabinoid receptor. J Pharmacol Exp Ther 292: 886-894.
25. Howlett AC, Barth F, Bonner TI, Cabral G, Casellas P, Devane WA, Felder CC, Herkenham M, Mackie K, Martin BR, Mechoulam R, Pertwee RG. 2002. International Union of Pharmacology. XXVII. Classification of cannabinoid receptors. Pharmacol Rev 54: 161-202.
26. 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.
27. Ishii M, Horio Y, Tada Y, Hibino H, Inanobe A, Ito M, Yamada M, Gotow T, Uchiyama Y, Kurachi Y. 1997. Expression and clustered distribution of an inwardly rectifying potassium channel, KAB-2/Kir4.1, on mammalian retinal Müller cell membrane: their regulation by insulin and laminin signals. J Neurosci 17: 7725-7735.
28. Kline RP, Ripps H, Dowling JE. 1985. Light-induced potassium fluxes in the skate retina. Neuroscience 14: 225-235.
29. Kolb H, Zhang L, Dekorver L, Cuenca N. 2002. A new look at calretinin-immunoreactive amacrine cell types in the monkey retina. J Comp Neurol 453: 168-184.
30. Kozak KR, Rowlinson SW, Marnett LJ. 2000. Oxygenation of the endocannabinoid, 2-arachidonylglycerol, to glyceryl prostaglandins by cyclooxygenase-2. J Biol Chem 275: 33744-33749.
31. Krishnan G, Chatterjee N. 2012. Endocannabinoids alleviate proinflammatory conditions by modulating innate immune response in Müller glia during inflammation. Glia 60: 1629-1645.
32. Li L, Head V, Timpe LC. 2001. Identification of an inward rectifier potassium channel gene expressed in mouse cortical astrocytes. Glia 33: 57-71.
33. López EM, Tagliaferro P, Onaivi ES, López-Costa JJ. 2011. Distribution of CB2 cannabinoid receptor in adult rat retina. Synapse 65: 388-392.
34. Lu Q, Straiker A, Maguire G. 2000. Expression of CB2 cannabinoid receptor mRNA in adult rat retina. Vis Neurosci 17: 91-95.
35. + channel, ROMK2 (kir1.2). Am J Physiol 275: F415-F422.
36. Mackie K. 2008. Cannabinoid receptors: where they are and what they do. J Neuroendocrinol 20(Suppl 1): 10-14.
37. Martínez-Navarrete GC, Martín-Nieto J, Esteve-Rudd J, Angulo A, Cuenca N. 2007. Alpha synuclein gene expression profile in the retina of vertebrates. Mol Vis 13: 949-961.
38. Martínez-Navarrete GC, Angulo A, Martín-Nieto J, Cuenca N. 2008. Gradual morphogenesis of retinal neurons in the peripheral retinal margin of adult monkeys and humans. J Comp Neurol 511: 557-580.
39. McPartland JM, Norris RW, Kilpatrick CW. 2007. Coevolution between cannabinoid receptors and endocannabinoid ligands. Gene 397: 126-135.
40. Mechoulam R, Ben Shabat S, Hanus L, Ligumsky M, Kaminski NE, Schatz AR, Gopher A, Almog S, Martin BR, Compton DR. 1995. Identification of an endogenous 2-monoglyceride, present in canine gut, that binds to cannabinoid receptors. Biochem Pharmacol 50: 83-90.
41. Miller RF, Dowling JE. 1970. Intracellular responses of the Müller (glial) cells of mudpuppy retina: their relation to b-wave of the electroretinogram. J Neurophysiol 33: 323-341.
42. Mills SL, Massey SC. 1999. AII amacrine cells limit scotopic acuity in central macaque retina: a confocal analysis of calretinin labeling. J Comp Neurol 411: 19-34.
43. Mukherjee S, Adams M, Whiteaker K, Daza A, Kage K, Cassar S, Meyer M, Yao BB. 2004. Species comparison and pharmacological characterization of rat and human CB2 cannabinoid receptors. Eur J Pharmacol 505: 1-9.
44. Munro S, Thomas KL, Abu-Shaar M. 1993. Molecular characterization of a peripheral receptor for cannabinoids. Nature 365: 61-65.
45. Nadal-Nicolás FM, Jiménez-López M, Sobrado-Calvo P, Nieto-López L, Cánovas-Martínez I, Salinas-Navarro M, Vidal-Sanz M, Agudo M. 2009. Brn3a as a marker of retinal ganglion cells: qualitative and quantitative time course studies in naïve and optic nerve-injured retinas. Invest Ophthalmol Vis Sci 50: 3860-3868.
46. Nag TC, Wadhwa S. 2001. Differential expression of syntaxin-1 and synaptophysin in the developing and adult human retina. J Biosci 26: 179-191.
47. Newman E, Reichenbach A. 1996. The Müller cell: a functional element of the retina. Trends Neurosci 19: 307-312.
48. + siphoning. Science 225: 1174-1175.
49. Nishikawa S, Tamai M. 2001. Müller cells in the human foveal region. Curr Eye Res 22: 34-41.
50. Onaivi E, Ishiguro H, Gu S, Liu Q-R. 2012. CNS effects of CB2 cannabinoid receptors: beyond neuro-immuno-cannabinoid activity. J Psychopharmacol 26: 92-103.
51. Pacher P, Mechoulam R. 2011. Is lipid signaling through cannabinoid 2 receptors part of a protective system? Prog Lipid Res 50: 193-211.
52. Piomelli D. 2003. The molecular logic of endocannabinoid signalling. Nat Rev Neurosci 4: 873-884.
53. Placzek EA, Okamoto Y, Ueda N, Barker EL. 2008. Mechanisms for recycling and biosynthesis of endogenous cannabinoids anandamide and 2-arachidonylglycerol. J Neurochem 107: 987-1000.
54. Porcella A, Casellas P, Gessa GL, Pani L. 1998. Cannabinoid receptor CB1 mRNA is highly expressed in the rat ciliary body: implications for the antiglaucoma properties of marihuana. Brain Res Mol Brain Res 58: 240-245.
55. 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.
56. Qi H-X, Gharbawie OA, Wong P, Kaas JH. 2011. Cell-poor septa separate representations of digits in the ventroposterior nucleus of the thalamus in monkeys and prosimian galagos. J Comp Neurol 519: 738-758.
57. Ramírez BG, Blázquez C, del Pulgar TG, Guzmán M, de Ceballos ML. 2005. Prevention of Alzheimer's disease pathology by cannabinoids: neuroprotection mediated by blockade of microglial activation. J Neurosci 25: 1904-1913.
58. Riepe RE, Norenburg MD. 1977. Müller cell localisation of glutamine synthetase in rat retina. Nature 268: 654-655.
59. Röhrenbeck J, Wässle H, Heizmann CW. 1987. Immunocytochemical labelling of horizontal cells in mammalian retina using antibodies against calcium-binding proteins. Neurosci Lett 77: 255-260.
60. Shire D, Calandra B, Rinaldi-Carmona M, Oustric D, Pessègue B, Bonnin-Cabanne O, Le Fur G, Caput D, Ferrara P. 1996. Molecular cloning, expression and function of the murine CB2 peripheral cannabinoid receptor. Biochim Biophys Acta 1307: 132-136.
61. Stella N. 2009. Endocannabinoid signaling in microglial cells. Neuropharmacology 56(Suppl 1): 244-253.
62. Stockton RA, Slaughter MM. 1989. B-wave of the electroretinogram. A reflection of ON bipolar cell activity. J Gen Physiol 93: 101-122.
63. 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.
64. Sugiura T, Kondo S, Sukagawa A, Nakane S, Shinoda A, Itoh K, Yamashita A, Waku K. 1995. 2-Arachidonoylglycerol: a possible endogenous cannabinoid receptor ligand in brain. Biochem Biophys Res Commun 215: 89-97.
65. Wässle H, Dacey DM, Haun T, Haverkamp S, Grunert U, Boycott BB. 2000. The mosaic of horizontal cells in the macaque monkey retina: with a comment on biplexiform ganglion cells. Vis Neurosci 17: 591-608.
66. Wei Y, Wang X, Wang L. 2009. Presence and regulation of cannabinoid receptors in human retinal pigment epithelial cells. Mol Vis 15: 1243-1251.
67. +-evoked Müller cell depolarization generates b-wave of electroretinogram in toad retina. Proc Natl Acad Sci U S A 87: 2117-2121.
68. Xiang M, Zhou L, Macke JP, Yoshioka T, Hendry SH, Eddy RL, Shows TB, Nathans J. 1995. The Brn-3 family of POU-domain factors: primary structure, binding specificity, and expression in subsets of retinal ganglion cells and somatosensory neurons. J Neurosci 15: 4762-4785.
69. Yazulla S. 2008. Endocannabinoids in the retina: from marijuana to neuroprotection. Prog Ret Eye Res 27: 501-526.
70. 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 415: 80-90.
71. Zabouri N, Bouchard JF, Casanova C. 2011a. Cannabinoid receptor type 1 expression during postnatal development of the rat retina. J Comp Neurol 519: 1258-1280.
72. Zabouri N, Ptito M, Casanova C, Bouchard JF. 2011b. Fatty acid amide hydrolase expression during retinal postnatal development in rats. Neuroscience 195: 145-165.
73. Zhong L, Geng L, Njie Y, Feng W, Song Z-H. 2005. CB2 cannabinoid receptors in trabecular meshwork cells mediate JWH015-induced enhancement of aqueous humor outflow facility. Invest Ophthalmol Vis Sci 46: 1988-1992.
74. Zurolo E, Iyer AM, Spliet WGM, Van Rijen PC, Troost D, Gorter JA, Aronica E. 2010. CB1 and CB2 cannabinoid receptor expression during development and in epileptogenic developmental pathologies. Neuroscience 170: 28-41.