Differential calcium signaling mediated by voltage-gated calcium channels in rat retinal ganglion cells and their unmyelinated axons

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Sargoy, Allison ^a   Sun, Xiaoping ^a   Barnes, Steven ^a,b,c   Brecha, Nicholas C ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b VA GREATER LOS ANGELES HEALTHCARE SYSTEM   (United States)

^c DALHOUSIE UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CALCIUM CHANNEL BLOCKING AGENT; CALCIUM CHANNEL L TYPE; CALCIUM CHANNEL L TYPE ALPHA1C SUBUNIT; CALCIUM CHANNEL L TYPE ALPHA1D SUBUNIT; CALCIUM CHANNEL N TYPE; CALCIUM CHANNEL N TYPE ALPHA1B SUBUNIT; CALCIUM CHANNEL P TYPE; CALCIUM CHANNEL P TYPE ALPHA1A SUBUNIT; CALCIUM CHANNEL Q TYPE; CALCIUM CHANNEL Q TYPE ALPHA1A SUBUNIT; CALCIUM CHANNEL T TYPE; UNCLASSIFIED DRUG; VOLTAGE GATED CALCIUM CHANNEL;

ADULT; ANIMAL CELL; ARTICLE; CALCIUM SIGNALING; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DEPOLARIZATION; FEMALE; IMMUNOREACTIVITY; MALE; NONHUMAN; NONMYELINATED NERVE; PATCH CLAMP TECHNIQUE; PERIKARYON; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; RETINA GANGLION CELL;

ACTION POTENTIALS; AMINO ACID SEQUENCE; ANIMALS; AXONS; CALCIUM CHANNELS; CALCIUM SIGNALING; GENE EXPRESSION REGULATION; MOLECULAR SEQUENCE DATA; NERVE FIBERS, UNMYELINATED; PROTEIN TRANSPORT; RATS; RETINAL GANGLION CELLS; TIME FACTORS;

EID: 84897146724     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0084507     Document Type: Article

References (65)

1. Berridge MJ (1998) Neuronal calcium signalling. Neuron 21: 13-26.
2. Berridge MJ (2006) Calcium microdomains: Organization and function. Cell Calcium 40: 405-412.
3. Marambaud P, Dreses-Werringloer U, Vingtdeux V (2009) Calcium signalling in neurodegeneration. Mol Neurodegener 4: 20.
4. Prilloff S, Noblejas MI, Chedhomme V, Sabel BA (2007) Two faces of calcium activation after optic nerve trauma: life or death of retinal ganglion cells in vivo depends on calcium dynamics. Eur J Neurosci 25: 3339-3346. (Pubitemid 46872759)
5. Dolphin A (2009) Calcium channel diversity: multiple roles of calcium channel subunits. Curr Opin Neurobiol 19: 237-244.
6. Richards MW, Butcher AJ, Dolphin AC (2004) Calcium channel beta subunits: structural insights AID our understanding. Trends Pharm Sci 25: 626-632. (Pubitemid 39458168)
7. Davies A, Hendrich J, Van Minh AT, Wratten J, Douglas L, Dolphin AC (2007) Functional biology of the alpha(2)delta subunits of voltage-gated calcium channels. Trends Pharmacol Sci 28: 220-228. (Pubitemid 46661004)
8. Bauer CS, Tran-Van-Minh A, Kadurin I, Dolphin AC (2010) A new look at calcium channel a2d subunits. Curr Opin Neurobiol 20: 563-571.
9. Dolphin AC (2012) Calcium channel auxiliary α2δ and γ subunits: trafficking and one step beyond. Nat Rev Neurosci. 13: 542-555.
10. Karschin A, Lipton SA (1989) Calcium channels in solitary retinal ganglion cells from post-natal rat. J Physiol 418: 379-96. (Pubitemid 19276940)
11. Guenther E, Rothe T, Taschenberger H, Grantyn R (1994) Separation of calcium currents in retinal ganglion cells from postnatal rat. Brain Res 633: 223-235. (Pubitemid 24021265)
12. 2+ channels mediate glutamatergic synaptic responses to activation of single Thy-1-immunolabeled rat retinal ganglion neurons. J Neurosci 15: 2240-2254.
13. 2+ currents in rat retinal ganglion cells. Neuroreport 7: 677-81.
14. Farrell SR, Raymond I, Foote M, Brecha NC, Barnes S (2010) Modulation of voltage-gated ion channels in mammalian retinal ganglion cells mediated by somatostatin receptor subtype 4. J Neurophysiol 104: 1347-54.
15. van Wyk M, Wässle H, Taylor WR (2009) Receptive field properties of ON- and OFF-ganglion cells in the mouse retina. Vis Neurosci 26: 297-308.
16. Margolis DJ, Gartland AJ, Euler T, Detwiler PB (2010) Dendritic calcium signaling in ON and OFF mouse retinal ganglion cells. J Neurosci 30: 7127-38.
17. Mark MD, Maejima T, Kuckelsberg D, Yoo JW, Hyde RA, et al. (2011) Delayed postnatal loss of P/Q-type calcium channels recapitulates the absence epilepsy, Dyskinesia, and Ataxia phenotypes of genomic Cacna1A mutations. J Neurosci 31: 4311-4326.
18. Witkovsky P, Shen C, McRory J (2006) Differential distribution of voltage-gated calcium channels in dopaminergic neurons of the rat retina. J Comp Neurol 497: 384-396. (Pubitemid 43865792)
19. Crossman DJ, Ruygrok PR, Soeller C, Cannell MB (2011) Changes in the organization of excitation-contraction coupling structures in failing human heart. PLoS ONE 6: e17901. doi: 10.1371/journal.pone.0017901.
20. Hell JW, Westenbroek RE, Warner C, Ahlijanian MK, Prystay W, et al. (1993) Identification and differential subcellular localization of the neuronal class C and class D L-type calcium channel α1 subunits. J Cell Biol 4: 949-962. (Pubitemid 23333582)
21. Kwong JMK, Quan A, Kyung H, Piri N, Caprioli J (2011) Quantitative analysis of retinal ganglion cell survival with RBPMS immunolabeling in animal models of optic neuropathies. Invest Ophthal Vis Sci 52: 9694-9702.
22. Rodriguez AR, Pérez de Sevilla Müller L, Brecha NC (2013) The RNA binding protein, RBPMS, is an exclusive marker of ganglion cells in the mammalian retina. J Comp Neurol (Submitted).
23. Firth SI, Morgan IG, Boelen MK, and Morgans CW (2001) Localization of voltage-sensitive L-type calcium channels in the chicken retina. Clin Exper Ophthal 29: 183-187. (Pubitemid 32618987)
24. Perry VH, Walker M (1980) Amacrine cells, displaced amacrine cells and interplexiform cells in the retina of the rat. Proc R Soc Lond B Biol Sci 208: 415-431.
25. Pérez De Sevilla Müller L, Shelley J, Weiler R (2007) Displaced amacrine cells of the mouse retina. J Comp Neurol 505: 177-89. (Pubitemid 350013041)
26. Fliegner KH, Liem RKH (1991) Int Rev Cytol 131: 109-167.
27. Kong WC, Cho EYP (1999) Antibodies against neurofilament subunits label retinal ganglion cells but not displaced amacrine cells of hamsters. Life Sci 64: 1773-1778. (Pubitemid 29185536)
28. Karnas D, Mordel J, Bonnet D, Pévet P, Hicks D, et al. (2013) Heterogeneity of intrinsically photosensitive retinal ganglion cells in the mouse revealed by molecular phenotyping. J Comp Neurol 521: 912-932.
29. Hille B (2001) Ion Channels of Excitable Membranes (3rd ed.). Sunderland, MA: Sinauer.
30. Zhang CL, Wilson JA, Williams J, Chiu SY (2006) Action potentials induce uniform calcium influx in mammalian myelinated optic nerves. J Neurophysiol 96: 695-709. (Pubitemid 44155210)
31. Ishida AT, Bindokas VP, Nuccitelli R (1991) Calcium ion levels in resting and depolarized goldfish retinal ganglion cell somata and growth cones. J Neurophysiol 65: 968-979.
32. Jeon CJ, Strettoi E, and Masland RH (1998) The major cell populations of the mouse retina. J Neurosci 18: 8936-8946. (Pubitemid 28491758)
33. Xu H, Zhao J, Yang X (2002) Expression of voltage-dependent calcium channel subunits in the rat retina. Neurosci Lett 329: 297-300. (Pubitemid 35245346)
34. Xu HP, Zhao JW, Yang XL (2003) Cholinergic and dopaminergic amacrine cells differentially express calcium channel subunits in the rat retina. Neuroscience 118: 763-8. (Pubitemid 36506963)
35. Habermann CJ, O'Brien BJ, Wässle H, Protti DA (2003). AII amacrine cells express L-type calcium channels at their output synapses. J Neurosci 23: 6904-6913. (Pubitemid 36951219)
36. LoGiudice L, Henry D, Matthews G (2007) Identification of calcium channel α1 subunit mRNA expressed in retinal bipolar neurons Mol Vis; 12: 184-189.
37. Schmid S, Guenther E (1999). The voltage-activated calcium currents in rat retinal ganglion cells in situ: Changes during prenatal and postnatal development. J Neurosci 19: 3486-3494. (Pubitemid 29203128)
38. de la Villa P, Vaquero CF, Kaneko A (1998) Two types of calcium currents of the mouse bipolar cells recorded in the retinal slice preparation. Eur J Neurosci 10: 317-323.
39. Hartveit E (1999) Reciprocal synaptic interactions between rod bipolar cells and amacrine cells in the rat retina. J Neurophys 81: 2923-2936.
40. Pan ZH (2000) Differential expression of high- and two types of low voltage-activated calcium currents in rod and cone bipolar cells of the rat retina. J Neurophys 83: 513-527. (Pubitemid 30039319)
41. 2+ channels mediate neurotransmitter release in retinal bipolar cells. Neuron 32: 89-98.
42. Hu C, Bi A, Pan ZH (2009) Differential expression of three T-type calcium channels in retinal bipolar cells in rats. Vis Neurosci 26: 177-187.
43. Knöferle J, Koch JC, Ostendorf T, Michel U, Planchamp V, et al. (2010) Mechanisms of acute axonal degeneration in the optic nerve in vivo. Proc Nat Acad Sci 107: 6064-9.
44. B receptors in axons of neonatal rat optic nerve. J Neurosci 19: 5185-5194.
45. Verkhratsky A, Rodriguez JJ, Parpura V (2012) Calcium signalling in astroglia. Mol. Cell Endocrinol 353: 45-56.
46. 2+ signals and calcium channels in axons of developing rat cerebellar interneurones. J Physiol 527: 33-48.
47. 2+ channels influence action potential generation and timing. Neuron 61: 259-71.
48. Viana F, Van den Bosch L, Missiaen L, Vandenberghe W, Droogmans G, et al. (1997) Mibefradil (Ro 40-5967) blocks multiple types of voltage-gated calcium channels in cultured rat spinal motoneurones. Cell Calcium 22: 299-311. (Pubitemid 27490309)
49. Eller P, Berjukov S, Wanner S, Huber I, Hering S, et al. (2000) High affinity interaction of mibefradil with voltage-gated calcium and sodium channels. Br J Pharmacol 130: 669-77. (Pubitemid 30332987)
50. McNulty MM, Hanck DA (2004) State-dependent mibefradil block of Na+ channels. Mol Pharmacol. 66: 1652-61.
51. La Morgia C, Ross-Cisneros FN, Sadun AA, Hannibal J, Munarini A, et al. (2010) Melanopsin retinal ganglion cells are resistant to neurodegeneration in mitochondrial optic neuropathies. Brain 133: 2426-2438.
52. Quigley HA (1998) Neuronal death in glaucoma. Ret Eye Res 18: 39-57.
53. Nakano N, Ikeda HO, Hangai M, Muraoka Y, Toda Y, et al. (2011) Model of glaucoma induced N-Methyl-D-Aspartate. Glaucoma 52: 8754-8762.
54. Hartwick ATE, Hamilton CM, Baldridge WH (2008) Glutamatergic calcium dynamics and deregulation of rat retinal ganglion cells. J Physiol 586: 3425-46. (Pubitemid 352003875)
55. Kong GYX, Van Bergen NJ, Trounce IA, Crowston JG (2009) Mitochondrial dysfunction and glaucoma. J Glaucoma 18: 93-100.
56. Kawasaki A, Otori Y, Barnstable C (2000) Müller cell protection of rat retinal ganglion cells from glutamate and nitric oxide neurotoxicity. Invest Ophthal Vis Sci 41: 3444-3450.
57. Ryskamp DA, Witkovsky P, Barabas P, Huang W, Koehler C, et al. (2011) The polymodal ion channel transient receptor potential vanilloid 4 modulates calcium flux, spiking rate, and apoptosis of mouse retinal ganglion cells. J Neurosci 31: 7089-7101.
58. Staal JA, Dickson TC, Gasperini R, Liu Y, Foa L, et al. (2010) Initial calcium release from intracellular stores followed by calcium dysregulation is linked to secondary axotomy following transient axonal stretch injury. J Neurochem 112: 1147-1155.
59. Weber JT, Rzigalinski BA, Ellis EF (2001) Traumatic injury of cortical neurons causes changes in intracellular calcium stores and capacitative calcium influx. J Biol Chem 276: 1800-1807. (Pubitemid 32109653)
60. Karim Z, Sawada A, Kawakami H, Yamamoto T, Taniguchi T (2006) A new calcium channel antagonist, lomerizine, alleviates secondary retinal ganglion cell death after optic nerve injury in the rat. Curr Eye Res 31: 273-83. (Pubitemid 43379198)
61. Fitzgerald M, Payne SC, Bartlett CA, Evill L, Harvey AR, et al. (2009) Secondary retinal ganglion cell death and the neuroprotective effects of the calcium channel blocker lomerizine. Invest Ophthal Vis Sci 50: 5456-5462.
62. Raff MC, Whitmore AV, Finn JT (2002) Axonal self-destruction and neurodegeneration. Science 296: 868-871.
63. Coleman MP, Perry VH (2002) Axon pathology in neurological disease: a neglected therapeutic target. Trends Neurosci 25: 532-537. (Pubitemid 35246324)
64. Zhai O, Wang J, Kim A, Liu Q, Watts R, et al. (2003) Involvement of the ubiquitin-proteasome system in the early stages of Wallerian degeneration. Neuron 39: 217-225. (Pubitemid 36897545)
65. Crish SD, Calkins DJ (2011) Neurodegeneration in glaucoma: progression and calcium-dependent intracellular mechanisms. Neuroscience 176: 1-11.