Characterization of Ca v 1.4 complexes (α 1 1.4, β 2 , and α 2 δ 4 ) in HEK293T cells and in the retina

Journal of Biological Chemistry

Volumn 290, Issue 3, 2015, Pages 1505-1521

  Lee, Amy ^a   Wang, Shiyi ^a   Williams, Brittany ^a   Hagen, Jussara ^a   Scheetz, Todd E ^a   Haeseleer, Franҫoise ^b  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; ELECTROPHYSIOLOGY; VISION;

CHANNEL COMPLEX; ELECTROPHYSIOLOGICAL RECORDINGS; FUNCTIONAL PROPERTIES; HIGH VOLTAGE-ACTIVATED; PORE FORMING; SYNAPTIC TERMINALS; VISUAL STIMULUS; WHOLE CELL PATCH CLAMP;

CYTOLOGY;

UNCLASSIFIED DRUG; VOLTAGE GATED CALCIUM CHANNEL; VOLTAGE GATED CALCIUM CHANNEL CAV1.4 ALPHA1 SUBUNIT; VOLTAGE GATED CALCIUM CHANNEL CAV1.4 ALPHA2DELTA4 SUBUNIT; VOLTAGE GATED CALCIUM CHANNEL CAV1.4 BETA2 SUBUNIT; CACNA1F PROTEIN, HUMAN; CACNA1F PROTEIN, MOUSE; CALCIUM CHANNEL; CALCIUM CHANNEL L TYPE;

ADULT; AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALCIUM SIGNALING; COMPLEX FORMATION; CONTROLLED STUDY; EXON; HEK293 CELL LINE; HUMAN; HUMAN CELL; HUMAN TISSUE; MOLECULAR CLONING; MOUSE; NEUROMODULATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHOTORECEPTOR; PROTEIN EXPRESSION; RETINA; RETINA OUTER PLEXIFORM LAYER; RNA SEQUENCE; SEQUENCE ALIGNMENT; SYNAPTOSOME; ANIMAL; C57BL MOUSE; CELL LINE; GENE EXPRESSION REGULATION; IMMUNOHISTOCHEMISTRY; METABOLISM; MOLECULAR GENETICS; PATCH CLAMP TECHNIQUE; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; ANIMALS; CALCIUM CHANNELS; CALCIUM CHANNELS, L-TYPE; CELL LINE; CLONING, MOLECULAR; GENE EXPRESSION REGULATION; HEK293 CELLS; HUMANS; IMMUNOHISTOCHEMISTRY; MICE; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; PATCH-CLAMP TECHNIQUES; RETINA; SEQUENCE ANALYSIS, RNA; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84961288765     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.607465     Document Type: Article

References (71)

1. 2+ channels. Physiol. Rev. 90, 1461-1506
2. Dolphin, A. C. (2012) Calcium channel auxiliary α2δ and β subunits: trafficking and one step beyond. Nat. Rev. Neurosci. 13, 542-555
3. Dolphin, A. C. (2013) The α2δ subunits of voltage-gated calcium channels. Biochim. Biophys. Acta 1828, 1541-1549
4. Simms, B. A., and Zamponi, G. W. (2014) Neuronal voltage-gated calcium channels: structure, function, and dysfunction. Neuron 82, 24-45
5. 2+ channels. Annu. Rev. Cell Dev. Biol. 16, 521-555
6. Catterall, W. A., Perez-Reyes, E., Snutch, T. P., and Striessnig, J. (2005) International Union of Pharmacology. XLVIII. Nomenclature and structure-function relationships of voltage-gated calcium channels. Pharmacol. Rev. 57, 411-425
7. Lipscombe, D., Andrade, A., and Allen, S. E. (2013) Alternative splicing: functional diversity among voltage-gated calcium channels and behavioral consequences. Biochim. Biophys. Acta 1828, 1522-1529
8. Matthews, G., and Fuchs, P. (2010) The diverse roles of ribbon synapses in sensory neurotransmission. Nat. Rev. Neurosci. 11, 812-822
9. Krizaj, D., and Copenhagen, D. R. (2002) Calcium regulation in photoreceptors. Front. Biosci. 7, d2023-d2044
10. Barnes, S., and Kelly, M. E. M. (2002) Calcium channels at the photoreceptor synapse. Adv. Exp. Med. Biol. 514, 465-476
11. Berntson, A., Taylor, W. R., and Morgans, C. W. (2003) Molecular identity, synaptic localization, and physiology of calcium channels in retinal bipolar cells. J. Neurosc. Res. 71, 146-151
12. Morgans, C. W. (2001) Localization of the α(1F) calcium channel subunit in the rat retina. Invest. Ophthalmol. Vis. Sci. 42, 2414-2418
13. Liu, X., Kerov, V., Haeseleer, F., Majumder, A., Artemyev, N., Baker, S. A., and Lee, A. (2013) Dysregulation of Ca(v)1.4 channels disrupts the maturation of photoreceptor synaptic ribbons in congenital stationary night blindness type 2. Channels 7, 514-523
14. Knoflach, D., Kerov, V., Sartori, S. B., Obermair, G. J., Schmuckermair, C., Liu, X., Sothilingam, V., Garrido, M. G., Baker, S. A., Glösmann, M., Schicker, K., Seeliger, M., Lee, A., and Koschak, A. (2013) Cav1.4 IT mouse as model for vision impairment in human congenital stationary night blindness type 2. Channels 7, 503-513
15. Mansergh, F., Orton, N. C., Vessey, J. P., Lalonde, M. R., Stell, W. K., Tremblay, F., Barnes, S., Rancourt, D. E., and Bech-Hansen, N. T. (2005) Mutation of the calcium channel gene Cacna1f disrupts calcium signaling, synaptic transmission and cellular organization in mouse retina. Hum. Mol. Genet. 14, 3035-3046
16. Zabouri, N., and Haverkamp, S. (2013) Calcium channel-dependent molecular maturation of photoreceptor synapses. PLoS One 8, e63853
17. Strom, T. M., Nyakatura, G., Apfelstedt-Sylla, E., Hellebrand, H., Lorenz, B., Weber, B. H. F., Wutz, K., Gutwillinger, N., Rüther, K., Drescher, B., Sauer, C., Zrenner, E., Meitinger, T., Rosenthal, A., and Meindl, A. (1998) An L-type calcium-channel gene mutated in incomplete X-linked congenital stationary night blindness. Nat. Genet. 19, 260-263
18. Wutz, K., Sauer, C., Zrenner, E., Lorenz, B., Alitalo, T., Broghammer, M., Hergersberg, M., de la Chapelle, A., Weber, B. H. F., Wissinger, B., Meindl, A., and Pusch, C. M. (2002) Thirty distinct CACNA1F mutations in 33 families with incomplete type of XLCSNB and Cacna1f expression profiling in mouse retina. Eur. J. Hum. Genet. 10, 449-456
19. Bech-Hansen, N. T., Naylor, M. J., Maybaum, T. A., Pearce, W. G., Koop, B., Fishman, G. A., Mets, M., Musarella, M. A., and Boycott, K. M. (1998) Loss-of-function mutations in a calcium-channel α(1)-subunit gene in Xp11.23 cause incomplete X-linked congenital stationary night blindness. Nat. Genet. 19, 264-267
20. Boycott, K. M., Maybaum, T. A., Naylor, M. J., Weleber, R. G., Robitaille, J., Miyake, Y., Bergen, A. A., Pierpont, M. E., Pearce, W. G., and Bech-Hansen, N. T. (2001) A summary of 20 CACNA1F mutations identified in 36 families with incomplete X-linked congenital stationary night blindness, and characterization of splice variants. Hum. Genet. 108, 91-97
21. Taylor, W. R., and Morgans, C. (1998) Localization and properties of voltage-gated calcium channels in cone photoreceptors of Tupaia belangeri. Vis. Neurosci. 15, 541-552
22. Morgans, C. W. (1999) Calcium channel heterogeneity among cone photoreceptors in the tree shrew retina. Eur. J. Neurosc. 11, 2989-2993
23. Ko, M. L., Liu, Y., Dryer, S. E., and Ko, G. Y. P. (2007) The expression of L-type voltage-gated calcium channels in retinal photoreceptors is under circadian control. J. Neurochem. 103, 784-792
24. 2+ channels modulate depression-like behaviour in mice independent of deaf phenotype. Int. J. Neuropsychopharmacol. 13, 499-513
25. Ball, S. L., Powers, P. A., Shin, H. S., Morgans, C. W., Peachey, N. S., and Gregg, R. G. (2002) Role of the β(2) subunit of voltage-dependent calcium channels in the retinal outer plexiform layer. Invest. Ophthalmol. Vis. Sci. 43, 1595-1603
26. Wycisk, K. A., Budde, B., Feil, S., Skosyrski, S., Buzzi, F., Neidhardt, J., Glaus, E., Nürnberg, P., Ruether, K., and Berger, W. (2006) Structural and functional abnormalities of retinal ribbon synapses due to Cacna2d4 mutation. Invest. Ophthalmol. Vis. Sci. 47, 3523-3530
27. Doering, C. J., Hamid, J., Simms, B., McRory, J. E., and Zamponi, G. W. (2005) Ca(v)1.4 encodes a calcium channel with low open probability and unitary conductance. Biophys. J. 89, 3042-3048
28. 2+ -binding protein 4, a Ca(v)1.4 channel regulator, in photoreceptor synaptic function. Nat. Neurosci. 7, 1079-1087
29. 2+ -dependent inactivation. J. Neurosci. 23, 6041-6049
30. Peloquin, J. B., Doering, C. J., Rehak, R., and McRory, J. E. (2008) Temperature dependence of Ca-v 1.4 calcium channel gating. Neuroscience 151, 1066-1083
31. 2+ channel Cav1.4α1 from mouse retina. Invest. Ophthalmol. Vis. Sci. 45, 708-713
32. McRory, J. E., Hamid, J., Doering, C. J., Garcia, E., Parker, R., Hamming, K., Chen, L., Hildebrand, M., Beedle, A. M., Feldcamp, L., Zamponi, G. W., and Snutch, T. P. (2004) The CACNA1F gene encodes an L-type calcium channel with unique biophysical properties and tissue distribution. J. Neurosci. 24, 1707-1718
33. Specht, D., Wu, S. B., Turner, P., Dearden, P., Koentgen, F., Wolfrum, U., Maw, M., Brandstätter, J. H., and tom Dieck, S. (2009) Effects of presynaptic mutations on a postsynaptic Cacna1s calcium channel colocalized with mGluR6 at mouse photoreceptor ribbon synapses. Invest. Ophthalmol. Vis. Sci. 50, 505-515
34. Livak, K. J., and Schmittgen, T. D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-ΔΔC(T)) method. Methods 25, 402-408
35. Whitmore, S. S., Wagner, A. H., DeLuca, A. P., Drack, A. V., Stone, E. M., Tucker, B. A., Zeng, S., Braun, T. A., Mullins, R. F., and Scheetz, T. E. (2014) Transcriptomic analysis across nasal, temporal, and macular regions of human neural retina and RPE/choroid by RNA-Seq. Exp. Eye Res. 129C, 93-126
36. Trapnell, C., Roberts, A., Goff, L., Pertea, G., Kim, D., Kelley, D. R., Pimentel, H., Salzberg, S. L., Rinn, J. L., and Pachter, L. (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protoc. 7, 562-578
37. Thorvaldsdóttir, H., Robinson, J. T., and Mesirov, J. P. (2013) Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform. 14, 178-192
38. 2+ channels in auditory hair cells. J. Physiol. 585, 791-803
39. Davies, A., Kadurin, I., Alvarez-Laviada, A., Douglas, L., Nieto-Rostro, M., Bauer, C. S., Pratt, W. S., and Dolphin, A. C. (2010) The α2δ subunits of voltage-gated calcium channels form GPI-anchored proteins, a posttranslational modification essential for function. Proc. Natl. Acad. Sci. U.S.A. 107, 1654-1659
40. Bolte, S., and Cordelières, F. P. (2006) A guided tour into subcellular colocalization analysis in light microscopy. J. Microsc. 224, 213-232
41. Lyford, G. L., Strege, P. R., Shepard, A., Ou, Y., Ermilov, L., Miller, S. M., Gibbons, S. J., Rae, J. L., Szurszewski, J. H., and Farrugia, G. (2002) α(1C) (Ca(V)1.2) L-type calcium channel mediates mechanosensitive calcium regulation. Am. J. Physiol. Cell Physiol. 283, C1001-C1008
42. 2+ -binding protein 4 (CaBP4). J. Biol. Chem. 287, 36312-36321
43. Qin, N., Yagel, S., Momplaisir, M. L., Codd, E. E., and D'Andrea, M. R. (2002) Molecular cloning and characterization of the human voltagegated calcium channel α(2)δ-4 subunit. Mol. Pharmacol. 62, 485-496
44. 2+ channels. Nat. Neurosci. 9, 1108-1116
45. Wahl-Schott, C., Baumann, L., Cuny, H., Eckert, C., Griessmeier, K., and Biel, M. (2006) Switching off calcium-dependent inactivation in L-type calcium channels by an autoinhibitory domain. Proc. Natl. Acad. Sci. U.S.A. 103, 15657-15662
46. Chaudhuri, D., Issa, J. B., and Yue, D. T. (2007) Elementary mechanisms producing facilitation of Cav2.1 (P/Q-type) channels. J. Gen. Physiol. 129, 385-401
47. Stea, A., Tomlinson, W. J., Soong, T. W., Bourinet, E., Dubel, S. J., Vincent, S. R., and Snutch, T. P. (1994) Localization and functional properties of a rat brain α 1A calcium channel reflect similarities to neuronal Q- and P-type channels. Proc. Natl. Acad. Sci. U.S.A. 91, 10576-10580
48. 2+ channels. Biophys. J. 93, 834-845
49. Richards, M. W., Leroy, J., Pratt, W. S., and Dolphin, A. C. (2007) The HOOK-domain between the SH3 and the GK domains of Cavβ subunits contains key determinants controlling calcium channel inactivation. Channels 1, 92-101
50. Schlick, B., Flucher, B. E., and Obermair, G. J. (2010) Voltage-activated calcium channel expression profiles in mouse brain and cultured hippocampal neurons. Neuroscience 167, 786-798
51. Ball, S. L., McEnery, M. W., Yunker, A. M., Shin, H. S., and Gregg, R. G. (2011) Distribution of voltage gated calcium channel β subunits in the mouse retina. Brain Res. 1412, 1-8
52. Mercer, A. J., Chen, M., and Thoreson, W. B. (2011) Lateral mobility of presynaptic L-type calcium channels at photoreceptor ribbon synapses. J. Neurosci. 31, 4397-4406
53. De Sevilla Müller, L. P., Liu, J., Solomon, A., Rodriguez, A., and Brecha, N. C. (2013) Expression of voltage-gated calcium channel α(2)δ(4) subunits in the mouse and rat retina. J. Comp. Neurol. 521, 2486-2501
54. Wycisk, K. A., Zeitz, C., Feil, S., Wittmer, M., Forster, U., Neidhardt, J., Wissinger, B., Zrenner, E., Wilke, R., Kohl, S., and Berger, W. (2006) Mutation in the auxiliary calcium-channel subunit CACNA2D4 causes autosomal recessive cone dystrophy. Am. J. Hum. Genet. 79, 973-977
55. 2+ channels. Biochim. Biophys. Acta 1828, 1530-1540
56. Perez-Reyes, E., Castellano, A., Kim, H. S., Bertrand, P., Baggstrom, E., Lacerda, A. E., Wei, X. Y., and Birnbaumer, L. (1992) Cloning and expression of a cardiac/brain β subunit of the L-type calcium channel. J. Biol. Chem. 267, 1792-1797
57. Chien, A. J., Carr, K. M., Shirokov, R. E., Rios, E., and Hosey, M. M. (1996) Identification of palmitoylation sites within the L-type calcium channel β2a subunit and effects on channel function. J. Biol. Chem. 271, 26465-26468
58. Chu, P. J., Larsen, J. K., Chen, C. C., and Best, P. M. (2004) Distribution and relative expression levels of calcium channel β subunits within the chambers of the rat heart. J. Mol. Cell Cardiol. 36, 423-434
59. Yasuda, T., Chen, L., Barr, W., McRory, J. E., Lewis, R. J., Adams, D. J., and Zamponi, G. W. (2004) Auxiliary subunit regulation of high-voltage activated calcium channels expressed in mammalian cells. Eur. J. Neurosci. 20, 1-13
60. Ebert, A. M., McAnelly, C. A., Srinivasan, A., Mueller, R. L., Garrity, D. B., and Garrity, D. M. (2008) The calcium channel β2 (CACNB2) subunit repertoire in teleosts. BMC Mol. Biol. 9, 38
61. Roberts-Crowley, M. L., and Rittenhouse, A. R. (2009) Arachidonic acid inhibition of L-type calcium (CaV1.3b) channels varies with accessory CaVβ subunits. J. Gen. Physiol. 133, 387-403
62. 2+ current in salamander photoreceptors by polyunsaturated fatty acids and retinoids. J. Physiol. 529, 333-344
63. Bernstein, G. M., and Jones, O. T. (2007) Kinetics of internalization and degradation of N-type voltage-gated calcium channels: role of the α2/δ subunit. Cell Calcium 41, 27-40
64. 2+ channels. Proc. Natl. Acad. Sci. U.S.A. 102, 11230-11235
65. 2+ channel α 2 δ subunit in current stimulation and subunit interaction. Neuron 16, 431-440
66. 2+ channels. FEBS Lett. 576, 21-26
67. 2+ channel α2δ subunit. J. Neurosci. 17, 6884-6891
68. Ferreira, G., Yi, J., Ríos, E., and Shirokov, R. (1997) Ion-dependent inactivation of barium current through L-type calcium channels. J. Gen. Physiol. 109, 449-461
69. Hoppa, M. B., Lana, B., Margas, W., Dolphin, A. C., and Ryan, T. A. (2012) α2δ expression sets presynaptic calcium channel abundance and release probability. Nature 486, 122-125
70. Eroglu, C., Allen, N. J., Susman, M. W., O'Rourke, N. A., Park, C. Y., Ozkan, E., Chakraborty, C., Mulinyawe, S. B., Annis, D. S., Huberman, A. D., Green, E. M., Lawler, J., Dolmetsch, R., Garcia, K. C., Smith, S. J., Luo, Z. D., Rosenthal, A., Mosher, D. F., and Barres, B. A. (2009) Gabapentin receptor alpha2delta-1 is a neuronal thrombospondin receptor responsible for excitatory CNS synaptogenesis. Cell 139, 380-392
71. 2+ -channel functions. Nat. Neurosci. 12, 1415-1423