Ontogenetic expression of the vanilloid receptors TRPV1 and TRPV2 in the rat retina

International Journal of Developmental Neuroscience

Volumn 27, Issue 7, 2009, Pages 709-718

  Leonelli, Mauro ^a   Martins, Daniel O ^a   Kihara, Alexandre H ^b   Britto, Luiz R G ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b Universidade Federal   (Brazil)

Author keywords

Calcium; Development; Rat retina; Transient receptor potential channels; Vanilloid receptors

Indexed keywords

RNA; VANILLOID RECEPTOR 1; VANILLOID RECEPTOR 2;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BLOOD VESSEL; CONTROLLED STUDY; EMBRYO; GENE EXPRESSION; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; MICROGLIA; NEUROBLAST; NEWBORN; NONHUMAN; ONTOGENY; PERIKARYON; PERINATAL PERIOD; PIGMENT EPITHELIUM; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; RETINA BIPOLAR GANGLION CELL; RETINA DEVELOPMENT; RETINA GANGLION CELL; RETINA INNER PLEXIFORM LAYER; RNA ANALYSIS; SYNAPSE; VISION;

ANIMALS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; RATS; RETINA; TRPV CATION CHANNELS;

RATTUS;

EID: 70349311268     PISSN: 07365748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijdevneu.2009.07.003     Document Type: Article

References (72)

1. Agopyan N., Head J., Yu S., and Simon S.A. TRPV1 receptors mediate particulate matter-induced apoptosis. Am. J. Physiol. Lung Cell. Mol. Physiol. 286 (2004) L563-L572
2. Akerman S., Kaube H., and Goadsby P.J. Anandamide acts as a vasodilator of dural blood vessels in vivo by activating TRPV1 receptors. Br. J. Pharmacol. 142 (2004) 1354-1360
3. Alter B.J., and Gereau R.W.T. Hotheaded: TRPV1 as mediator of hippocampal synaptic plasticity. Neuron 57 (2008) 629-631
4. Amantini C., Mosca M., Nabissi M., Lucciarini R., Caprodossi S., Arcella A., Giangaspero F., and Santoni G. Capsaicin-induced apoptosis of glioma cells is mediated by TRPV1 vanilloid receptor and requires p38 MAPK activation. J. Neurochem. 102 (2007) 977-990
5. Bae Y.C., Oh J.M., Hwang S.J., Shigenaga Y., and Valtschanoff J.G. Expression of vanilloid receptor TRPV1 in the rat trigentinal sensory nuclei. J. Comp. Neurol. 478 (2004) 62-71
6. Bang S., Kim K.Y., Yoo S., Lee S.H., and Hwang S.W. Transient receptor potential V2 expressed in sensory neurons is activated by probenecid. Neurosci. Lett. 425 (2007) 120-125
7. Bisogno T., Delton-Vandenbroucke I., Milone A., Lagarde M., and Di Marzo V. Biosynthesis and inactivation of N-arachidonoylethanolamine (anandamide) and N-docosahexaenoylethanolamine in bovine retina. Arch. Biochem. Biophys. 370 (1999) 300-307
8. Burnstock G., and Knight G.E. Cellular distribution and functions of P2 receptor subtypes in different systems. Int. Rev. Cytol. 240 (2004) 31-304
9. Caterina M.J., Rosen T.A., Tominaga M., Brake A.J., and Julius D. A capsaicin-receptor homologue with a high threshold for noxious heat. Nature 398 (1999) 436-441
10. Caterina M.J., Schumacher M.A., Tominaga M., Rosen T.A., Levine J.D., and Julius D. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389 (1997) 816-824
11. Cellerino A., Bahr M., and Isenmann S. Apoptosis in the developing visual system. Cell Tissue Res. 301 (2000) 53-69
12. Chen J., Matias I., Dinh T., Lu T., Venezia S., Nieves A., Woodward D.F., and Di Marzo V. Finding of endocannabinoids in human eye tissues: implications for glaucoma. Biochem. Biophys. Res. Commun. 330 (2005) 1062-1067
13. Di Marzo V., Bisogno T., and De Petrocellis L. Anandamide: some like it hot. Trends Pharmacol. Sci. 22 (2001) 346-349
14. Di Marzo V., Blumberg P.M., and Szallasi A. Endovanilloid signaling in pain. Curr. Opin. Neurobiol. 12 (2002) 372-379
15. Dixon R.G., and Eng L.F. Glial fibrillary acidic protein in the retina of the developing albino rat: an immunoperoxidase study of paraffin-embedded tissue. J. Comp. Neurol. 195 (1980) 305-321
16. Doly S., Fischer J., Salio C., and Conrath M. The vanilloid receptor-1 is expressed in rat spinal dorsal horn astrocytes. Neurosci. Lett. 357 (2004) 123-126
17. Drager U.C., Edwards D.L., and Barnstable C.J. Antibodies against filamentous components in discrete cell types of the mouse retina. J. Neurosci. 4 (1984) 2025-2042
18. Feigenspan A., Bormann J., and Wassle H. Organotypic slice culture of the mammalian retina. Vis. Neurosci. 10 (1993) 203-217
19. Ferriero D.M., and Sagar S.M. Development of somatostatin immunoreactive neurons in rat retina. Brain Res. 431 (1987) 207-214
20. Ferrini F., Salio C., Vergnano A.M., and Merighi A. Vanilloid receptor-1 (TRPV1)-dependent activation of inhibitory neurotransmission in spinal substantia gelatinosa neurons of mouse. Pain 129 (2007) 195-209
21. Frade J.M., Bovolenta P., and Rodriguez-Tebar A. Neurotrophins and other growth factors in the generation of retinal neurons. Microsc. Res. Tech. 45 (1999) 243-251
22. Glaser S.T., Kaczocha M., and Deutsch D.G. Anandamide transport: a critical review. Life Sci. 77 (2005) 1584-1604
23. Goswami C., Dreger M., Jahnel R., Bogen O., Gillen C., and Hucho F. Identification and characterization of a Ca2+ -sensitive interaction of the vanilloid receptor TRPV1 with tubulin. J. Neurochem. 91 (2004) 1092-1103
24. Gunthorpe M.J., Benham C.D., Randall A., and Davis J.B. The diversity in the vanilloid (TRPV) receptor family of ion channels. Trends Pharmacol. Sci. 23 (2002) 183-191
25. Heidinger V., Dreyfus H., Sahel J., Christen Y., and Hicks D. Excitotoxic damage of retinal glial cells depends upon normal neuron-glial interactions. Glia 23 (1998) 146-155
26. Hu H.Z., Gu Q., Wang C., Colton C.K., Tang J., Kinoshita-Kawada M., Lee L.Y., Wood J.D., and Zhu M.X. 2-aminoethoxydiphenyl borate is a common activator of TRPV1, TRPV2, and TRPV3. J. Biol. Chem. 279 (2004) 35741-35748
27. Iwasaki Y., Saito O., Tanabe M., Inayoshi K., Kobata K., Uno S., Morita A., and Watanabe T. Monoacylglycerols activate capsaicin receptor, TRPV1. Lipids 43 (2008) 471-483
28. Ji R.R., Samad T.A., Jin S.X., Schmoll R., and Woolf C.J. p38 MAPK activation by NGF in primary sensory neurons after inflammation increases TRPV1 levels and maintains heat hyperalgesia. Neuron 36 (2002) 57-68
29. Kihara A.H., Mantovani de Castro L., Belmonte M.A., Yan C.Y., Moriscot A.S., and Hamassaki D.E. Expression of connexins 36, 43 and 45 during postnatal development of the mouse retina. J. Neurobiol. 66 (2006) 1397-1410
30. Kihara A.H., Paschon V., Akamine P.S., Saito K.C., Leonelli M., Jiang J.X., Hamassaki D.E., and Britto L.R. Differential expression of connexins during histogenesis of the chick retina. Dev. Neurobiol. 68 (2008) 1287-1302
31. Lam P.M., Hainsworth A.H., Smith G.D., Owen D.E., Davies J., and Lambert D.G. Activation of recombinant human TRPV1 receptors expressed in SH-SY5Y human neuroblastoma cells increases [Ca(2+)](i), initiates neurotransmitter release and promotes delayed cell death. J. Neurochem. 102 (2007) 801-811
32. Leonelli M., Torrao A.S., and Britto L.R. Unconventional neurotransmitters, neurodegeneration and neuroprotection. Braz. J. Med. Biol. Res. 42 (2009) 68-75
33. Li D.P., Chen S.R., and Pan H.L. VR1 receptor activation induces glutamate release and postsynaptic firing in the paraventricular nucleus. J. Neurophysiol. 92 (2004) 1807-1816
34. Linden R., Martins R.A., and Silveira M.S. Control of programmed cell death by neurotransmitters and neuropeptides in the developing mammalian retina. Prog. Retin. Eye Res. 24 (2005) 457-491
35. Maccarrone M., Lorenzon T., Bari M., Melino G., and Finazzi-Agro A. Anandamide induces apoptosis in human cells via vanilloid receptors. Evidence for a protective role of cannabinoid receptors. J. Biol. Chem. 275 (2000) 31938-31945
36. Mandell J.W., Townes-Anderson E., Czernik A.J., Cameron R., Greengard P., and De Camilli P. Synapsins in the vertebrate retina: absence from ribbon synapses and heterogeneous distribution among conventional synapses. Neuron 5 (1990) 19-33
37. Matsuda S., Kanemitsu N., Nakamura A., Mimura Y., Ueda N., Kurahashi Y., and Yamamoto S. Metabolism of anandamide, an endogenous cannabinoid receptor ligand, in porcine ocular tissues. Exp. Eye Res. 64 (1997) 707-711
38. Medhurst A.D., Harrison D.C., Read S.J., Campbell C.A., Robbins M.J., and Pangalos M.N. The use of TaqMan RT-PCR assays for semiquantitative analysis of gene expression in CNS tissues and disease models. J. Neurosci. Methods 98 (2000) 9-20
39. Medvedeva Y.V., Kim M.S., and Usachev Y.M. Mechanisms of prolonged presynaptic Ca2+ signaling and glutamate release induced by TRPV1 activation in rat sensory neurons. J. Neurosci. 28 (2008) 5295-5311
40. Metea M.R., and Newman E.A. Glial cells dilate and constrict blood vessels: a mechanism of neurovascular coupling. J. Neurosci. 26 (2006) 2862-2870
41. Metea M.R., and Newman E.A. Signalling within the neurovascular unit in the mammalian retina. Exp. Physiol. 92 (2007) 635-640
42. Nucci C., Gasperi V., Tartaglione R., Cerulli A., Terrinoni A., Bari M., De Simone C., Agro A.F., Morrone L.A., Corasaniti M.T., Bagetta G., and Maccarrone M. Involvement of the endocannabinoid system in retinal damage after high intraocular pressure-induced ischemia in rats. Invest. Ophthalmol. Vis. Sci. 48 (2007) 2997-3004
43. Pareek T.K., Keller J., Kesavapany S., Agarwal N., Kuner R., Pant H.C., Iadarola M.J., Brady R.O., and Kulkarni A.B. Cyclin-dependent signaling through transient receptor kinase 5 modulates nociceptive direct phosphorylation of potential vanilloid 1. Proc. Natl. Acad. Sci. U.S.A. 104 (2007) 660-665
44. Pedersen S.F., Owsianik G., and Nilius B. TRP channels: an overview. Cell Calcium 38 (2005) 233-252
45. Poblete I.M., Orliac M.L., Briones R., Adler-Graschinsky E., and Huidobro-Toro J.P. Anandamide elicits an acute release of nitric oxide through endothelial TRPV1 receptor activation in the rat arterial mesenteric bed. J. Physiol. 568 (2005) 539-551
46. Puntambekar P., Mukherjea D., Jajoo S., and Ramkumar V. Essential role of Rac1/NADPH oxidase in nerve growth factor induction of TRPV1 expression. J. Neurochem. 95 (2005) 1689-1703
47. Ritter S., and Dinh T.T. Capsaicin-induced neuronal degeneration in the brain and retina of preweanling rats. J. Comp. Neurol. 296 (1990) 447-461
48. Ritter S., and Dinh T.T. Prior optic nerve transection reduces capsaicin-induced degeneration in rat subcortical visual structures. J. Comp. Neurol. 308 (1991) 79-90
49. Ritter S., and Dinh T.T. Age-related changes in capsaicin-induced degeneration in rat brain. J. Comp. Neurol. 318 (1992) 103-116
50. Sanchez A.M., Sanchez M.G., Malagarie-Cazenave S., Olea N., and Diaz-Laviada I. Induction of apoptosis in prostate tumor PC-3 cells and inhibition of xenograft prostate tumor growth by the vanilloid capsaicin. Apoptosis 11 (2006) 89-99
51. Sanchez J.F., Krause J.E., and Cortright D.N. The distribution and regulation of vanilloid receptor VR1 and VR1 5′ splice variant RNA expression in rat. Neuroscience 107 (2001) 373-381
52. Sappington R.M., and Calkins D.J. Contribution of TRPV1 to microglia-derived IL-6 and NFkappaB translocation with elevated hydrostatic pressure. Invest. Ophthalmol. Vis. Sci. 49 (2008) 3004-3017
53. Sappington R.M., Chan M., and Calkins D.J. Interleukin-6 protects retinal ganglion cells from pressure-induced death. Invest. Ophthalmol. Vis. Sci. 47 (2006) 2932-2942
54. Sappington R.M., Sidorova T., Long D.J., and Calkins D.J. TRPV1: contribution to retinal ganglion cell apoptosis and increased intracellular Ca2+ with exposure to hydrostatic pressure. Invest. Ophthalmol. Vis. Sci. 50 (2009) 717-728
55. Shirakawa H., Yamaoka T., Sanpei K., Sasaoka H., Nakagawa T., and Kaneko S. TRPV1 stimulation triggers apoptotic cell death of rat cortical neurons. Biochem. Biophys. Res. Commun. 377 (2008) 1211-1215
56. Stokes A.J., Shimoda L.M., Koblan-Huberson M., Adra C.N., and Turner H. A TRPV2-PKA signaling module for transduction of physical stimuli in mast cells. J. Exp. Med. 200 (2004) 137-147
57. Straiker A., Stella N., Piomelli D., Mackie K., Karten H.J., and Maguire G. Cannabinoid CB1 receptors and ligands in vertebrate retina: localization and function of an endogenous signaling system. Proc. Natl. Acad. Sci. U.S.A. 96 (1999) 14565-14570
58. Straiker A., and Sullivan J.M. Cannabinoid receptor activation differentially modulates ion channels in photoreceptors of the tiger salamander. J. Neurophysiol. 89 (2003) 2647-2654
59. Straiker A.J., Maguire G., Mackie K., and Lindsey J. Localization of cannabinoid CB1 receptors in the human anterior eye and retina. Invest. Ophthalmol. Vis. Sci. 40 (1999) 2442-2448
60. Szolcsanyi J. Forty years in capsaicin research for sensory pharmacology and physiology. Neuropeptides 38 (2004) 377-384
61. Tohda C., Sasaki M., Konemura T., Sasamura T., Itoh M., and Kuraishi Y. Axonal transport of VR1 capsaicin receptor mRNA in primary afferents and its participation in inflammation-induced increase in capsaicin sensitivity. J. Neurochem. 76 (2001) 1628-1635
62. Toth A., Boczan J., Kedei N., Lizanecz E., Bagi Z., Papp Z., Edes I., Csiba L., and Blumberg P.M. Expression and distribution of vanilloid receptor 1 (TRPV1) in the adult rat brain. Brain Res. Mol. Brain Res. 135 (2005) 162-168
63. Tulapurkar M.E., Laubinger W., Nahum V., Fischer B., and Reiser G. Subtype specific internalization of P2Y1 and P2Y2 receptors induced by novel adenosine 5′-O-(1-boranotriphosphate) derivatives. Br. J. Pharmacol. 142 (2004) 869-878
64. Voilley N., de Weille J., Mamet J., and Lazdunski M. Nonsteroid anti-inflammatory drugs inhibit both the activity and the inflammation-induced expression of acid-sensing ion channels in nociceptors. J. Neurosci. 21 (2001) 8026-8033
65. Von Kriegstein K., Schmitz F., Link E., and Sudhof T.C. Distribution of synaptic vesicle proteins in the mammalian retina identifies obligatory and facultative components of ribbon synapses. Eur. J. Neurosci. 11 (1999) 1335-1348
66. Wang L.H., Luo M., Wang Y., Galligan J.J., and Wang D.H. Impaired vasodilation in response to perivascular nerve stimulation in mesenteric arteries of TRPV1-null mutant mice. J. Hypertens. 24 (2006) 2399-2408
67. Waning J., Vriens J., Owsianik G., Stuwe L., Mally S., Fabian A., Frippiat C., Nilius B., and Schwab A. A novel function of capsaicin-sensitive TRPV1 channels: involvement in cell migration. Cell Calcium 42 (2007) 17-25
68. Yazulla S., and Studholme K.M. Vanilloid receptor like 1 (VRL1) immunoreactivity in mammalian retina: colocalization with somatostatin and purinergic P2X1 receptors. J. Comp. Neurol. 474 (2004) 407-418
69. Yazulla S., Studholme K.M., McIntosh H.H., and Deutsch D.G. Immunocytochemical localization of cannabinoid CB1 receptor and fatty acid amide hydrolase in rat retina. J. Comp. Neurol. 415 (1999) 80-90
70. Zhang C., and Tso M.O. Characterization of activated retinal microglia following optic axotomy. J. Neurosci. Res. 73 (2003) 840-845
71. Zimov S., and Yazulla S. Localization of vanilloid receptor 1 (TRPV1/VR1)-like immunoreactivity in goldfish and zebrafish retinas: restriction to photoreceptor synaptic ribbons. J. Neurocytol. 33 (2004) 441-452
72. Zimov S., and Yazulla S. Vanilloid receptor 1 (TRPV1/VR1) co-localizes with fatty acid amide hydrolase (FAAH) in retinal amacrine cells. Vis. Neurosci. 24 (2007) 581-591