β-Endorphin expression in the mouse retina

Journal of Comparative Neurology

Volumn 518, Issue 15, 2010, Pages 3130-3148

  Gallagher, Shannon K ^a   Witkovsky, Paul ^b   Roux, Michel J ^c   Low, Malcolm J ^d   Otero Corchon, Veronica ^d   Hentges, Shane T ^a   Vigh, Jozsef ^a  

^a Department of Environmental and Radiological Health Sciences   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITÉ DE STRASBOURG   (France)

^d UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

endorphin; POMC; retina; starburst amacrine cell

Indexed keywords

BETA ENDORPHIN; GLUTAMATE DECARBOXYLASE 67; OPIATE PEPTIDE; PROOPIOMELANOCORTIN; RED FLUORESCENT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHOLINERGIC SYSTEM; CONTROLLED STUDY; FLUORESCENCE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; REGULATORY MECHANISM; RETINA; RETINA AMACRINE CELL; TRANSGENIC MOUSE;

ADRENOCORTICOTROPIC HORMONE; ALPHA-MSH; AMACRINE CELLS; ANIMALS; ANTIBODY SPECIFICITY; BETA-ENDORPHIN; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; CHOLINE O-ACETYLTRANSFERASE; GLUTAMATE DECARBOXYLASE; GLYCINE PLASMA MEMBRANE TRANSPORT PROTEINS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; LUMINESCENT PROTEINS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROSCOPY, CONFOCAL; PARASYMPATHETIC NERVOUS SYSTEM; PITUITARY GLAND; PRO-OPIOMELANOCORTIN; RETINA;

EID: 77954570609     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.22387     Document Type: Article

References (79)

1. Altschuler RA, Mosinger JL, Hoffman DW, Parakkal MH. 1982. Immunocytochemical localization of enkephalin-like immu-noreactivity in the retina of the guinea pig. Proc Natl Acad Sci USA 79:2398-2400.
2. Andrade da Costa BL, Hokoc JN. 2003. Coexistence of GAD-65 and GAD-67 with tyrosine hydroxylase and nitric oxide synthase in amacrine and interplexiform cells of the primate, Cebus apella. Vis Neurosci 20:153-163.
3. Bicknell AB. 2008. The tissue-specific processing of pro-opio- melanocortin. J Neuroendocrinol 20:692-699.
4. Borbe HO, Wollert U, Muller WE. 1982. Stereospecific [3H]nal-oxone binding associated with opiate receptors in bovine retina. Exp Eye Res 34:539-544.
5. Brecha NC. 2003. Peptide and peptide receptor expression and function in the vertebrate retina. In: Chalupa, Werner, editors. The visual neurosciences. Cambridge, MA: MIT Press. p 334-354.
6. Brecha NC, Johnson J, Kui B, Anton B, Keith D, Evans C, Ster-nini C. 1995. Mu opioid receptor immunoreactivity is expressed in the retina and retina recipient nuclei. Analgesia 1:331-334.
7. Brunelli G, Spano P, Barlati S, Guarneri B, Barbon A, Bresciani R, Pizzi M. 2005. Glutamatergic reinnervation through peripheral nerve graft dictates assembly of glutamatergic synapses at rat skeletal muscle. Proc Natl Acad Sci USA 102:8752-8757.
8. Campbell RE, Tour O, Palmer AE, Steinbach PA, Baird GS, Zacharias DA, Tsien RY. 2002. A monomeric red fluorescent protein. Proc Natl Acad Sci USA 99:7877-7882.
9. Caputi A, Rozov A, Blatow M, Monyer H. 2009. Two calretinin-positive GABAergic cell types in layer 2/3 of the mouse neocortex provide different forms of inhibition. Cereb Cortex 19:1345-1359.
10. Casini G, Brecha NC. 1992. Colocalization of vasoactive intestinal polypeptide and GABA immunoreactivities in a population of wide-field amacrine cells in the rabbit retina. Vis Neurosci 8:373-378.
11. Chang YC, Gottlieb DI. 1988. Characterization of the proteins purified with monoclonal antibodies to glutamic acid decar-boxylase. J Neurosci 8:2123-2130.
12. Chen P, Williams SM, Grove KL, Smith MS. 2004. Melanocor-tin 4 receptor-mediated hyperphagia and activation of neu-ropeptide Y expression in the dorsomedial hypothalamus during lactation. J Neurosci 24:5091-6100.
13. Choi JH, Lee CH, Yoo KY, Hwang IK, Lee IS, Lee YL, Shin HC, Won MH. 2010. Age-related changes in calbindin-D28k, parvalbumin, and calretinin immunoreactivity in the dog main olfactory bulb. Cell Mol Neurobiol 30:1-12.
14. Cuenca N, Kolb H. 1998. Circuitry and role of substance P-im-munoreactive neurons in the primate retina. J Comp Neurol 393:439-456.
15. de Melo J, Du G, Fonseca M, Gillespie LA, Turk WJ, Ruben-stein JL, Eisenstat DD. 2005. Dlx1 and Dlx2 function is necessary for terminal differentiation and survival of late-born retinal ganglion cells in the developing mouse retina. Development 132:311-322.
16. de Souza FS, Santangelo AM, Bumaschny V, Avale ME, Smart JL, Low MJ, Rubinstein M. 2005. Identification of neuronal enhancers of the proopiomelanocortin gene by transgenic mouse analysis and phylogenetic footprinting. Mol Cell Biol 25:3076-3086.
17. Djamgoz MB, Stell WK, Chin CA, Lam DM. 1981. An opiate system in the goldfish retina. Nature 292:620-623.
18. Dkhissi O, Julien JF, Wasowicz M, il-Thiney N, Nguyen-Legros J, Versaux-Botteri C. 2001. Differential expression of GAD(65) and GAD(67) during the development of the rat retina. Brain Res 919:242-249.
19. Eglen SJ, Raven MA, Tamrazian E, Reese BE. 2003. Dopami-nergic amacrine cells in the inner nuclear layer and ganglion cell layer comprise a single functional retinal mosaic. J Comp Neurol 466:343-355.
20. Ehinger B. 1982. Neurotransmitter systems in the retina. Retina 2:305-221.
21. Elias CF, Saper CB, Maratos-Flier E, Tritos NA, Lee C, Kelly J, Tatro JB, Hoffman GE, Ollmann MM, Barsh GS, Sakurai T, Yanagisawa M, Elmquist JK. 1998. Chemically defined projections linking the mediobasal hypothalamus and the lateral hypothalamic area. J Comp Neurol 402:442-459.
22. Fischer AJ, Seltner RL, Stell WK. 1998. Opiate and N-methyl-D-aspartate receptors in form-deprivation myopia. Vis Neu-rosci 15:1089-10896.
23. Gábriel R, Volgyi B, Pollak E. 1998. Calretinin-immunoreactive elements in the retina and optic tectum of the frog, Rana esculenta. Brain Res 782:53-62.
24. Ghosh KK, Bujan S, Haverkamp S, Feigenspan A, Ẅassle H. 2004. Types of bipolar cells in the mouse retina. J Comp Neurol 469:70-82.
25. Hamano K, Kiyama H, Emson PC, Manabe R, Nakauchi M, Tohyama M. 1990. Localization of two calcium binding proteins, calbindin (28 kD) and parvalbumin (12 kD), in the vertebrate retina. J Comp Neurol 302:417-424.
26. Hannibal J, Moller M, Ottersen OP, Fahrenkrug J. 2000. PACAP and glutamate are co-stored in the retinohypothalamic tract. J Comp Neurol 418:147-155.
27. Haverkamp S, Ẅassle H. 2000. Immunocytochemical analysis of the mouse retina. J Comp Neurol 424:1-23.
28. Haverkamp S, Inta D, Monyer H, Ẅassle H. 2009. Expression analysis of green fluorescent protein in retinal neurons of four transgenic mouse lines. Neuroscience 160:126-139.
29. Hentges ST, Otero-Corchon V, Pennock RL, King CM, Low MJ. 2009. Proopiomelanocortin expression in both GABA and glutamate neurons. J Neurosci 29:13684-13690.
30. Hokfelt T, Broberger C, Xu ZQ, Sergeyev V, Ubink R, Diez M. 2000. Neuropeptides-an overview. Neuropharmacology 39:1337-1356.
31. Howells RD, Groth J, Hiller JM, Simon EJ. 1980. Opiate binding sites in the retina: properties and distribution. J Pharmacol Exp Ther 215:60-64.
32. Husain S, Potter DE, Crosson CE. 2009. Opioid receptor-activation: retina protected from ischemic injury. Invest Oph-thalmol Vis Sci 50:3853-3859.
33. Jackson IM, Bolaffi JL, Guillemin R. 1980. Presence of immu-noreactive beta-endorphin and enkephalin-like material in the retina and other tissues of the frog, Rana pipiens. Gen Comp Endocrinol 42:505-508.
34. Jeon CJ, Strettoi E, Masland RH. 1998. The major cell populations of the mouse retina. J Neurosci 18:8936-8946.
35. Kang TH, Ryu YH, Kim IB, Oh GT, Chun MH. 2004. Comparative study of cholinergic cells in retinas of various mouse strains. Cell Tissue Res 317:109-115.
36. Khalap A, Bagrosky B, Lecaude S, Youson J, Danielson P, Dores RM. 2005. Trends in the evolution of the proenke-phalin and prodynorphin genes in gnathostomes. Ann NY Acad Sci 1040:22-37.
37. Kieffer BL. 1995. Recent advances in molecular recognition and signal transduction of active peptides: receptors for opioid peptides. Cell Mol Neurobiol 15:615-635.
38. Kielczewski JL, Pease ME, Quigley HA. 2005. The effect of experimental glaucoma and optic nerve transection on ama-crine cells in the rat retina. Invest Ophthalmol Vis Sci 46: 3188-3196.
39. Kong JH, Fish DR, Rockhill RL, Masland RH. 2005. Diversity of ganglion cells in the mouse retina: unsupervised morphological classification and its limits. J Comp Neurol 489:293-310.
40. Lam TT, Takahashi K, Tso MO. 1994. The effects of naloxone on retinal ischemia in rats. J Ocul Pharmacol 10:481-492.
41. MacNeil MA, Masland RH. 1998. Extreme diversity among amacrine cells: implications for function. Neuron 20: 971-982.
42. Marc RE, Murry RF, Fisher SK, Linberg KA, Lewis GP, Kallonia-tis M. 1998. Amino acid signatures in the normal cat retina. Invest Ophthalmol Vis Sci 39:1685-1693.
43. Masland RH, Mills JW. 1979. Autoradiographic identification of acetylcholine in the rabbit retina. J Cell Biol 83:159-178.
44. Matilla A, Gorbea C, Einum DD, Townsend J, Michalik A, van BC, Jensen CC, Murphy KJ, Ptacek LJ, Fu YH. 2001. Association of ataxin-7 with the proteasome subunit S4 of the 19S regulatory complex. Hum Mol Genet 10:2821-2831.
45. May CA, Nakamura K, Fujiyama F, Yanagawa Y. 2008. Quantification and characterization of GABA-ergic amacrine cells in the retina of GAD67-GFP knock-in mice. Acta Ophthal-mol 86:395-400.
46. Medzihradsky F. 1976. Stereospecific binding of etorphine in isolated neural cells and in retina, determined by a sensitive microassay. Brain Res 108:212-219.
47. Millington GW. 2007. The role of proopiomelanocortin (POMC) neurones in feeding behaviour. Nutr Metab (Lond) 4:18.
48. Moon JI, Kim IB, Gwon JS, Park MH, Kang TH, Lim EJ, Choi KR, Chun MH. 2005. Changes in retinal neuronal populations in the DBA/2J mouse. Cell Tissue Res 320:51-59.
49. Neal MJ, Paterson SJ, Cunningham JR. 1994. Enhancement of retinal acetylcholine release by DAMGO: possibly a direct opioid receptor-mediated excitatory effect. Br J Pharmacol 113:789-794.
50. Oliva AA Jr, Jiang M, Lam T, Smith KL, Swann JW. 2000. Novel hippocampal interneuronal subtypes identified using trans-genic mice that express green fluorescent protein in GABAergic interneurons. J Neurosci 20:3354-3368.
51. Overstreet LS, Hentges ST, Bumaschny VF, de Souza FS, Smart JL, Santangelo AM, Low MJ, Westbrook GL, Rubinstein M. 2004. A transgenic marker for newly born granule cells in dentate gyrus. J Neurosci 24:3251-3259.
52. Peng PH, Huang HS, Lee YJ, Chen YS, Ma MC. 2009. Novel role for the delta-opioid receptor in hypoxic preconditioning in rat retinas. J Neurochem 108:741-754.
53. Pow DV. 1998. Transport is the primary determinant of gly-cine content in retinal neurons. J Neurochem 70:2628-2636.
54. Raymond ID, Vila A, Huynh UC, Brecha NC. 2008. Cyan fluorescent protein expression in ganglion and amacrine cells in a thy1-CFP transgenic mouse retina. Mol Vis 14:1559-1574.
55. Sarthy V, Hoshi H, Mills S, Dudley VJ. 2007. Characterization of green fluorescent protein-expressing retinal cells in CD 44-transgenic mice. Neuroscience 144:1087-1093.
56. Seltner RL, Rohrer B, Grant V, Stell WK. 1997. Endogenous opiates in the chick retina and their role in form-deprivation myopia. Vis Neurosci 14:801-809.
57. Slaughter MM, Mattler JA, Gottlieb DI. 1985. Opiate binding sites in the chick, rabbit and goldfish retina. Brain Res 339:39-47.
58. Smart JL, Tolle V, Low MJ. 2006. Glucocorticoids exacerbate obesity and insulin resistance in neuron-specific proopio-melanocortin-deficient mice. J Clin Invest 116:495-505.
59. Storch KF, Paz C, Signorovitch J, Raviola E, Pawlyk B, Li T, Weitz CJ. 2007. Intrinsic circadian clock of the mammalian retina: importance for retinal processing of visual information. Cell 130:730-741.
60. Su YY, Watt CB, Lam DM. 1985. Opioid pathways in an avian retina. I. The content, biosynthesis, and release of Met5-enkephalin. J Neurosci 5:851-856.
61. Tamamaki N, Yanagawa Y, Tomioka R, Miyazaki J, Obata K, Kaneko T. 2003. Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatosta-tin in the GAD67-GFP knock-in mouse. J Comp Neurol 467:60-79.
62. Vaney DI, Whitington GE, Young HM. 1989. The morphology and topographic distribution of substance-P-like immunore-active amacrine cells in the cat retina. Proc R Soc Lond B Biol Sci 237:471-488.
63. Vaney DI, Nelson JC, Pow DV. 1998. Neurotransmitter coupling through gap junctions in the retina. J Neurosci 18: 10594-10602.
64. Vardi N, Auerbach P. 1995. Specific cell types in cat retina express different forms of glutamic acid decarboxylase. J Comp Neurol 351:374-384.
65. Vitanova L, Popova E, Kupenova P, Kosteljanetz N, Belcheva S. 1990. Comparative studies on the effects of some en-kephalin agonists on the ERG of frog and turtle. Comp Bio-chem Physiol C 97:93-98.
66. Voigt T. 1986. Cholinergic amacrine cells in the rat retina. J Comp Neurol 248:19-35.
67. von Engelhardt J, Eliava M, Meyer AH, Rozov A, Monyer H. 2007. Functional characterization of intrinsic cholinergic interneurons in the cortex. J Neurosci 27:5633-5642.
68. Wamsley JK, Palacios JM, Kuhar MJ. 1981. Autoradiographic localization of opioid receptors in the mammalian retina. Neurosci Lett 27:19-24.
69. Wässle H, Riemann HJ. 1978. The mosaic of nerve cells in the mammalian retina. Proc R Soc Lond B Biol Sci 200: 441-461.
70. Watt CB, Su YY, Lam DM. 1984. Interactions between enkephalin and GABA in avian retina. Nature 311: 761-763.
71. Watt CB, Li T, Lam DM, Wu SM. 1988. Quantitative studies of enkephalin's coexistence with gamma-aminobutyric acid, glycine and neurotensin in amacrine cells of the chicken retina. Brain Res 444:366-370.
72. Whitney IE, Keeley PW, Raven MA, Reese BE. 2008. Spatial patterning of cholinergic amacrine cells in the mouse retina. J Comp Neurol 508:1-12.
73. Yamamoto T, Yamato E, Tashiro F, Sato T, Noso S, Ikegami H, Tamura S, Yanagawa Y, Miyazaki JI. 2004. Development of autoimmune diabetes in glutamic acid decarboxylase 65 (GAD65) knockout NOD mice. Diabetologia 47:221-224.
74. Yamasaki EN, Barbosa VD, De Mello FG, Hokoc JN. 1999. GABAergic system in the developing mammalian retina: dual sources of GABA at early stages of postnatal development. Int J Dev Neurosci 17:201-213.
75. Yang DS, Boelen MK, Morgan IG. 1997. Development of the enkephalin-, neurotensin-and somatostatin-like (ENSLI) amacrine cells in the chicken retina. Brain Res Dev Brain Res 101:57-65.
76. Zafra F, Aragon C, Olivares L, Danbolt NC, Gimenez C, Storm-Mathisen J. 1995. Glycine transporters are differentially expressed among CNS cells. J Neurosci 15(5 Pt 2): 3952-3969.
77. Zalutsky RA, Miller RF. 1990a. The physiology of somatostatin in the rabbit retina. J Neurosci 10:383-393.
78. Zalutsky RA, Miller RF. 1990b. The physiology of substance P in the rabbit retina. J Neurosci 10:394-402.
79. Zhou ZJ, Lee S. 2008. Synaptic physiology of direction selectivity in the retina. J Physiol 586(Pt 18): 4371-4376.