The role of voltage-gated calcium channels in neurotransmitter phenotype specification: Coexpression and functional analysis in Xenopus laevis

Journal of Comparative Neurology

Volumn 522, Issue 11, 2014, Pages 2518-2531

  Lewis, Brittany B ^a,b   Miller, Lauren E ^a,c   Herbst, Wendy A ^a   Saha, Margaret S ^a  

^a The College of William and Mary   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c EMORY UNIVERSITY   (United States)

Author keywords

Calcium activity; Development; Embryo; GABA; Glutamate

Indexed keywords

4 AMINOBUTYRIC ACID; NEUROTRANSMITTER; UNCLASSIFIED DRUG; VESICULAR GLUTAMATE TRANSPORTER 1; VESICULAR INHIBITORY AMINO ACID TRANSPORTER; VOLTAGE GATED CALCIUM CHANNEL; VOLTAGE GATED CALCIUM CHANNEL ALPHA 1 SUBUNIT; VOLTAGE GATED CALCIUM CHANNEL CAV2.1; VOLTAGE GATED CALCIUM CHANNEL CAV2.2; 4 AMINOBUTYRIC ACID RECEPTOR; AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; CALCIUM; CALCIUM CHANNEL; CALCIUM CHANNEL N TYPE; CAV2.1 PROTEIN, XENOPUS; CAV2.2 PROTEIN, XENOPUS; GLUTAMIC ACID; VGLUT1 PROTEIN, XENOPUS; VIAAT PROTEIN, XENOPUS; XENOPUS PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CRANIAL NERVE; EMBRYO; FLUORESCENCE IN SITU HYBRIDIZATION; LONG TERM EXPOSURE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; RHOMBENCEPHALON; SIGNAL TRANSDUCTION; SPINAL CORD; TADPOLE; XENOPUS LAEVIS; ACTION POTENTIAL; ANIMAL; BRAIN; CELL CULTURE; DRUG EFFECTS; METABOLISM; NERVE CELL; PHYSIOLOGY; RETINA;

ACTION POTENTIALS; ANIMALS; BRAIN; CALCIUM; CALCIUM CHANNELS; CALCIUM CHANNELS, N-TYPE; CELLS, CULTURED; CRANIAL NERVES; GABAERGIC NEURONS; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; IN SITU HYBRIDIZATION, FLUORESCENCE; NEURONS; NEUROTRANSMITTER AGENTS; RETINA; SPINAL CORD; VESICULAR GLUTAMATE TRANSPORT PROTEIN 1; VESICULAR INHIBITORY AMINO ACID TRANSPORT PROTEINS; XENOPUS LAEVIS; XENOPUS PROTEINS;

EID: 84901677676     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23547     Document Type: Article

References (64)

1. Barbado M, Fablet K, Ronjat M, De Waard M. 2009. Gene regulation by voltage-dependent calcium channels. Biochim Biophys Acta 1793:1096-1104.
2. Borodinsky LN, Root CM, Cronin JA, Sann SB, Gu X, Spitzer NC. 2004. Activity-dependent homeostatic specification of transmitter expression in embryonic neurons. Nature 429:523-530.
3. Borodinsky LN, Belgacem YH, Swapna I, Sequerra EB. 2014. Dynamic regulation of neurotransmitter specification: relevance to nervous system homeostasis. Neuropharmacology 78:75-80.
4. 2+ channels by benzothiazepines and phenylalkylamines: class-specific pharmacology and underlying molecular determinants. Mol Pharmacol 51:872-881.
5. Catterall WA. 2011. Voltage-gated calcium channels. Cold Spring Harb Perspect Biol 3:a003947.
6. Catterall WA, Leal K, Nanou E. 2013. Calcium channels and short-term synaptic plasticity. J Biol Chem 288:10742-10749.
7. Chang LW, Spitzer NC. 2009. Spontaneous calcium spike activity in embryonic spinal neurons is regulated by developmental expression of the Na+, K+-ATPase beta3 subunit. J Neurosci 29:7877-7885.
8. Davidson LA, Keller RE. 1999. Neural tube closure in Xenopus laevis involves medial migration, directed protrusive activity, cell intercalation and convergent extension. Development 126:4547-4556.
9. De Paoli P, Cerbai E, Koidl B, Kirchengast M, Sartiani L, Mugelli A. 2002. Selectivity of different calcium antagonists on T- and L-type calcium currents in guinea-pig ventricular myocytes. Pharmacol Res 46:491-497.
10. Dolmetsch RE, Pajvani U, Fife K, Spotts JM, Greenberg ME. 2001. Signaling to the nucleus by an L-type calcium channel-calmodulin complex through the MAP kinase pathway. Science 294:333-339.
11. Dulcis D, Spitzer NC. 2008. Illumination controls differentiation of dopamine neurons regulating behaviour. Nature 456:195-201.
12. Dullin JP, Locker M, Robach M, Henningfeld KA, Parain K, Afelik S, Pieler T, Perron M. 2007. Ptf1a triggers GABAergic neuronal cell fates in the retina. BMC Dev Biol 7:110.
13. 2+ entry and embryonic rat neural stem cell proliferation. J Neurosci 25:2687-2701.
14. v2.2 identified in presynaptic membrane by mass spectrometric analysis. Channels (Austin) 4:58-62.
15. Glaser T, Resende RR, Ulrich H. 2013. Implications of purinergic receptor-mediated intracellular calcium transients in neural differentiation. Cell Commun Signal 11:12.
16. Gleason KK, Dondeti VR, Hsia HL, Cochran ER, Gumulak-Smith J, Saha MS. 2003. The vesicular glutamate transporter 1 (xVGlut1) is expressed in discrete regions of the developing Xenopus laevis nervous system. Gene Expr Patterns 3:503-507.
17. Gu X, Olson EC, Spitzer NC. 1994. Spontaneous neuronal calcium spikes and waves during early differentiation. J Neurosci 14:6325-6335.
18. Gutiérrez R. 2002. Activity-dependent expression of simultaneous glutamatergic and GABAergic neurotransmission from the mossy fibers in vitro. J Neurophysiol 87:2562-2570.
19. Guzman JN, Sánchez-Padilla J, Chan CS, Surmeier DJ. 2009. Robust pacemaking in substantia nigra dopaminergic neurons. J Neurosci 29:11011-11019.
20. Hashimoto K, Tsujita M, Miyazaki T, Kitamura K, Yamazaki M, Shin HS, Watanabe M, Sakimura K, Kano M. 2011. Postsynaptic P/Q-type Ca2+ channel in Purkinje cell mediates synaptic competition and elimination in developing cerebellum. Proc Natl Acad Sci U S A 108:9987-9992.
21. v1.3 calcium channels are required for normal development of the auditory brainstem. J Neurosci 31:8280-8294.
22. 2+ that enhances neurite outgrowth in PC12 cells via activation of 5-HT3 receptors and voltage-gated calcium channels. J Neurosci Res 84:316-325.
23. v1.2 in pioneer axons during pathfinding in the developing rat forebrain. J Comp Neurol 520:3650-3672.
24. Jun K, Piedras-Rentería ES, Smith SM, Wheeler DB, Lee SB, Lee TG, Chin H, Adams ME, Scheller RH, Tsien RW, Shin HS. 1999. Ablation of P/Q-type Ca(2+) channel currents, altered synaptic transmission, and progressive ataxia in mice lacking the alpha(1A)-subunit. Proc Natl Acad Sci U S A 96:15245-15250.
25. Kasyanov AM, Safiulina VF, Voronin LL, Cherubini E. 2004. GABA-mediated giant depolarizing potentials as coincidence detectors for enhancing synaptic efficacy in the developing hippocampus. Proc Natl Acad Sci U S A 101:3967-3972.
26. Kerstein PC, Jacques-Fricke BT, Rengifo J, Mogen BJ, Williams JC, Gottlieb PA, Sachs F, Gomez TM. 2013. Mechanosensitive TRPC1 channels promote calpain proteolysis of talin to regulate spinal axon outgrowth. J Neurosci 33:273-285.
27. Leclerc C, Néant I, Moreau M. 2011. Early neural development in vertebrates is also a matter of calcium. Biochimie 93:2102-2111.
28. Lee KW, Moreau M, Néant I, Bibonne A, Leclerc C. 2009. FGF-activated calcium channels control neural gene expression in Xenopus. Biochim Biophys Acta 1793:1033-1040.
29. Lepski G, Jannes CE, Nikkhah G, Bischofberger J. 2013. cAMP promotes the differentiation of neural progenitor cells in vitro via modulation of voltage-gated calcium channels. Front Cell Neurosci 7:155.
30. Lewis BB, Wester MR, Miller LE, Nagarkar MD, Johnson MB, Saha MS. 2009. Cloning and characterization of voltage-gated calcium channel alpha1 subunits in Xenopus laevis during development. Dev Dyn 238:2891-2902.
31. Li M, Sipe CW, Hoke K, August LL, Wright MA, Saha MS. 2006. The role of early lineage in GABAergic and glutamatergic cell fate determination in Xenopus laevis. J Comp Neurol 495:645-657.
32. Lipscombe D, Andrade A, Allen SE. 2013. Alternative splicing: functional diversity among voltage-gated calcium channels and behavioral consequences. Biochim Biophys Acta 1828:1522-1529.
33. Lu CB, Fu W, Xu X, Mattson MP. 2009. Numb-mediated neurite outgrowth is isoform-dependent, and requires activation of voltage-dependent calcium channels. Neuroscience 161:403-412.
34. Marek KW, Kurtz LM, Spitzer NC. 2010. cJun integrates calcium activity and tlx3 expression to regulate neurotransmitter specification. Nat Neurosci 13:944-950.
35. Massé K, Dale N. 2012. Purines as potential morphogens during embryonic development. Purinergic Signal 8:503-521.
36. McDonough MJ, Allen CE, Ng-Sui-Hing NK, Rabe BA, Lewis BB, Saha MS. 2012. Dissection, culture, and analysis of Xenopus laevis embryonic retinal tissue. J Vis Exp 70.
37. 2+ sensor proteins mediates short-term synaptic plasticity. Neuron 57:210-216.
38. Moreau M, Leclerc C, Gualandris-Parisot L, Duprat AM. 1994. Increased internal Ca2+ mediates neural induction in the amphibian embryo. Proc Natl Acad Sci U S A 91:12639-12643.
39. Morton RA, Norlin MS, Vollmer CC, Valenzuela CF. 2013. Characterization of L-type voltage-gated Ca(2+) channel expression and function in developing CA3 pyramidal neurons. Neuroscience 238:59-70.
40. Nieuwkoop P, Faber J. 1994. Normal table of Xenopus laevis (Daudin). New York: Garland Publishing.
41. Nishiyama M, Togashi K, von Schimmelmann MJ, Lim CS, Maeda S, Yamashita N, Goshima Y, Ishii S, Hong K. 2011. Semaphorin 3A induces Cav2.3 channel-dependent conversion of axons to dendrites. Nat Cell Biol 13:676-685.
42. Papanayotou C, De Almeida I, Liao P, Oliveira NM, Lu SQ, Kougioumtzidou E, Zhu L, Shaw A, Sheng G, Streit A, Yu D, Wah Soong T, Stern CD. 2013. Calfacilitin is a calcium channel modulator essential for initiation of neural plate development. Nat Commun 4:1837.
43. Rajapaksha WR, Wang D, Davies JN, Chen L, Zamponi GW, Fisher TE. 2008. Novel splice variants of rat Cav2.1 that lack much of the synaptic protein interaction site are expressed in neuroendocrine cells. J Biol Chem 283:15997-16003.
44. Roberts A, Li WC, Soffe SR. 2012. A functional scaffold of CNS neurons for the vertebrates: the developing Xenopus laevis spinal cord. Dev Neurobiol 72:575-584.
45. Rosenberg SS, Spitzer NC. 2011. Calcium signaling in neuronal development. Cold Spring Harb Perspect Biol 3:a004259.
46. Sagala FS, Harnack D, Bobrov E, Sohr R, Gertler C, James Surmeier D, Kupsch A. 2012. Neurochemical characterization of the striatum and the nucleus accumbens in L-type Ca(v)1.3 channels knockout mice. Neurochem Int 60:229-232.
47. Sambrook J, Russell D. 2001. Molecular cloning, 3rd ed. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
48. Sanhueza D, Montoya A, Sierralta J, Kukuljan M. 2009. Expression of voltage-activated calcium channels in the early zebrafish embryo. Zygote 17:131-135.
49. Shim S, Goh EL, Ge S, Sailor K, Yuan JP, Roderick HL, Bootman MD, Worley PF, Song H, Ming GL. 2005. XTRPC1-dependent chemotropic guidance of neuronal growth cones. Nat Neurosci 8:730-735.
50. Sive H, Grainger R, Harland R. 2000. Early development of Xenopus laevis: a laboratory manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
51. Spitzer NC. 2012. Activity-dependent neurotransmitter respecification. Nat Rev Neurosci 13:94-106.
52. Spitzer NC, Kingston PA, Manning TJ, Conklin MW. 2002. Outside and in: development of neuronal excitability. Curr Opin Neurobiol 12:315-323.
53. Spitzer NC, Borodinsky LN, Root CM. 2005. Homeostatic activity-dependent paradigm for neurotransmitter specification. Cell Calcium 37:417-423.
54. Takahashi H, Magee JC. 2009. Pathway interactions and synaptic plasticity in the dendritic tuft regions of CA1 pyramidal neurons. Neuron 62:102-111.
55. 2(+) signaling mechanisms and cell motility in presumptive ectodermal cells during amphibian gastrulation. Dev Growth Differ 53:37-47.
56. Tan GM, Yu D, Wang J, Soong TW. 2012. Alternative splicing at C terminus of Ca(V)1.4 calcium channel modulates calcium-dependent inactivation, activation potential, and current density. J Biol Chem 287:832-847.
57. Tuluc P, Flucher BE. 2011. Divergent biophysical properties, gating mechanisms, and possible functions of the two skeletal muscle Ca(V)1.1 calcium channel splice variants. J Muscle Res Cell Motil 32:249-256.
58. Turner RW, Anderson D, Zamponi GW. 2011. Signaling complexes of voltage-gated calcium channels. Channels (Austin) 5:440-448.
59. Vandael DH, Mahapatra S, Calorio C, Marcantoni A, Carbone E. 2013. Cav1.3 and Cav1.2 channels of adrenal chromaffin cells: emerging views on cAMP/cGMP-mediated phosphorylation and role in pacemaking. Biochim Biophys Acta 1828:1608-1618.
60. 2+ transients upregulate GAD 67 transcripts in embryonic spinal neurons. Mol Cell Neurosci 16:376-387.
61. Wester MR, Teasley DC, Byers SL, Saha MS. 2008. Expression patterns of glycine transporters (xGlyT1, xGlyT2, and xVIAAT) in Xenopus laevis during early development. Gene Expr Patterns 8:261-270.
62. Wheeler DG, Barrett CF, Groth RD, Safa P, Tsien RW. 2008. CaMKII locally encodes L-type channel activity to signal to nuclear CREB in excitation-transcription coupling. J Cell Biol 183:849-863.
63. Zhang HY, Liao P, Wang JJ, Yu dJ, Soong TW. 2010. Alternative splicing modulates diltiazem sensitivity of cardiac and vascular smooth muscle Ca(v)1.2 calcium channels. Br J Pharmacol 160:1631-1640.
64. Zhou W, Horstick EJ, Hirata H, Kuwada JY. 2008. Identification and expression of voltage-gated calcium channel beta subunits in zebrafish. Dev Dyn 237:3842-3852.