The upregulation of α2δ-1 subunit modulates activity-dependent Ca2+ signals in sensory neurons

Journal of Neuroscience

Volumn 35, Issue 15, 2015, Pages 5891-5903

  D’Arco, Marianna ^a   Margas, Wojciech ^a   Cassidy, John S ^a   Dolphin, Annette C ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA2 DELTA SUBUNIT 1 PROTEIN; BETA TUBULIN; COMPLEMENTARY DNA; MEMBRANE PROTEIN; NIFEDIPINE; OMEGA CONOTOXIN GVIA; POLYCLONAL ANTIBODY; UNCLASSIFIED DRUG; VOLTAGE GATED CALCIUM CHANNEL; VOLTAGE GATED SODIUM CHANNEL; YELLOW FLUORESCENT PROTEIN; ANTIMYCIN A1; BETA3 TUBULIN, MOUSE; CACNA1B PROTEIN, RAT; CALCIUM; CALCIUM CHANNEL BLOCKING AGENT; CALCIUM CHANNEL N TYPE; CITRININ; CYCLOPIAZONIC ACID; ENZYME INHIBITOR; INDOLE DERIVATIVE; POTASSIUM CHLORIDE; TUBULIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CALCIUM DEPLETION; CALCIUM TRANSPORT; CONTROLLED STUDY; ELECTROSTIMULATION; ENDOPLASMIC RETICULUM; EVOKED RESPONSE; FEMALE; GENE; GENE MUTATION; GENE OVEREXPRESSION; IMMUNOCYTOCHEMISTRY; INTRACELLULAR SIGNALING; MALE; MEMBRANE DEPOLARIZATION; MIDAS MOTIF GENE; MITOCHONDRIAL MEMBRANE POTENTIAL; NERVE CELL CULTURE; NERVE CELL GROWTH; NEURITE; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; SENSORY NERVE CELL; SPINAL GANGLION; TIME LAPSE IMAGING; TRANSCELLULAR CELL MIGRATION; TRANSIENT TRANSFECTION; UPREGULATION; VOLTAGE CLAMP TECHNIQUE; WESTERN BLOTTING; WHOLE CELL PATCH CLAMP; ANALOGS AND DERIVATIVES; ANIMAL; CALCIUM SIGNALING; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; GENETICS; MEMBRANE POTENTIAL; METABOLISM; NEWBORN; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; ANIMALS, NEWBORN; ANTIMYCIN A; CALCIUM; CALCIUM CHANNEL BLOCKERS; CALCIUM CHANNELS, N-TYPE; CALCIUM SIGNALING; CELLS, CULTURED; ENZYME INHIBITORS; FEMALE; GANGLIA, SPINAL; INDOLES; MALE; MEMBRANE POTENTIALS; NIFEDIPINE; OMEGA-CONOTOXIN GVIA; POTASSIUM CHLORIDE; RATS; RATS, SPRAGUE-DAWLEY; SENSORY RECEPTOR CELLS; TUBULIN; UP-REGULATION;

EID: 84929231287     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3997-14.2015     Document Type: Article

References (46)

1. Akimzhanov AM, Boehning D (2011) Monitoring dynamic changes in mitochondrial calcium levels during apoptosis using A genetically encoded calcium sensor. J Vis Exp 50:2579. CrossRef Medline
2. Basbaum AI, Bautista DM, Scherrer G, Julius D (2009) Cellular and molecular mechanisms of pain. Cell 139:267-284. CrossRef Medline
3. Bauer CS, Nieto-Rostro M, Rahman W, Tran-Van-Minh A, Ferron L, Douglas L, Kadurin I, Sri Ranjan Y, Fernandez-Alacid L, Millar NS, Dickenson AH, Lujan R, Dolphin AC (2009) The increased trafficking of the calcium channel subunit alpha2delta-1 to presynaptic terminals in neuropathic pain is inhibited by the alpha2delta ligand pregabalin. J Neurosci 29:4076-4088. CrossRef Medline
4. Bauer CS, Tran-Van-Minh A, Kadurin I, Dolphin AC (2010) A new look at calcium channel a2ð subunits. Curr Opin Neurobiol 20:563-571. CrossRef Medline
5. Bell TJ, Thaler C, Castiglioni AJ, Helton TD, Lipscombe D (2004) Cell-specific alternative splicing increases calcium channel current density in the pain pathway. Neuron 41:127-138. CrossRef Medline
6. Berridge MJ (1998) Neuronal calcium signaling. Neuron 21:13-26. CrossRef Medline
7. Berridge MJ, Bootman MD, Roderick HL (2003) Calcium signalling: dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol 4:517-529. CrossRef Medline
8. Billups B, Forsythe ID (2002) Presynaptic mitochondrial calcium sequestration influences transmission at mammalian central synapses. J Neurosci 22:5840-5847. Medline
9. Campbell JN, Meyer RA (2006) Mechanisms of neuropathic pain. Neuron 52:77-92. CrossRef Medline
10. Cantí C, Nieto-Rostro M, Foucault I, Heblich F, Wratten J, Richards MW, Hendrich J, Douglas L, Page KM, Davies A, Dolphin AC (2005) The metal-ion-dependent adhesion site in the von Willebrand factor-A domain of alpha2delta subunits is key to trafficking voltage-gated Ca2 + channels. Proc Natl Acad Sci U S A 102:11230-11235. CrossRef Medline
11. Cassidy JS, Ferron L, Kadurin I, Pratt WS, Dolphin AC (2014) Functional exofacially tagged N-type calcium channels elucidate the interaction with auxiliary α2δ-l subunits. Proc Natl Acad Sci USA 111:8979-8984. CrossRef Medline
12. Colegrove SL, Albrecht MA, Friel DD (2000) Dissection of mitochondrial Ca2+ uptake and release fluxes in situ after depolarization-evoked [Ca2 + ] (i) elevations in sympathetic neurons. J Gen Physiol 115:351-370. CrossRef Medline
13. De Stefani D, Raffaello A, Teardo E, Szabò I, Rizzuto R (2011) A forty-kilodalton protein of the inner membrane is the mitochondrial calcium uniporter. Nature 476:336-340. CrossRef Medline
14. Dolphin AC (2012) Calcium channel auxiliary a2δ and β subunits: trafficking and one step beyond. Nat Rev Neurosci 13:542-555. CrossRef Medline
15. Fernyhough P, Calcutt NA (2010) Abnormal calcium homeostasis in peripheral neuropathies. Cell Calcium 47:130-139. CrossRef Medline
16. Friel DD (2000) Mitochondria as regulators of stimulus-evoked calcium signals in neurons. Cell Calcium 28:307-316. CrossRef Medline
17. Fuchs A, Rigaud M, Hogan QH (2007) Painful nerve injury shortens the intracellular Ca2 + signal in axotomized sensory neurons of rats. Anesthesiology 107:106-116. CrossRef Medline
18. Hoppa MB, Lana B, Margas W, Dolphin AC, Ryan TA (2012) a2δ Expression sets presynaptic calcium channel abundance and release probability. Nature 486:122-125. CrossRef Medline
19. Julius D, Basbaum AI (2001) Molecular mechanisms of nociception. Nature 413:203-210. CrossRef Medline
20. Kadurin I, Alvarez-Laviada A, Ng SF, Walker-Gray R, D’Arco M, Fadel MG, Pratt WS, Dolphin AC (2012) Calcium currents are enhanced by α2δ-1 lacking its membrane anchor. J Biol Chem 287:33554-33566. CrossRef Medline
21. Karra D, Dahm R (2010) Transfection techniques for neuronal cells. J Neurosci 30:6171-6177. CrossRef Medline
22. Li CY, Zhang XL, Matthews EA, Li KW, Kurwa A, Boroujerdi A, Gross J, Gold MS, Dickenson AH, Feng G, Luo ZD (2006) Calcium channel alpha2deltal subunit mediates spinal hyperexcitability in pain modulation. Pain 125:20-34. CrossRef Medline
23. Lu SG, Gold MS (2008) Inflammation-induced increase in evoked calcium transients in subpopulations of rat dorsal root ganglion neurons. Neuroscience 153:279-288. CrossRef Medline
24. Lu SG, Zhang X, Gold MS (2006) Intracellular calcium regulation among subpopulations of rat dorsal root ganglion neurons. J Physiol 577:169-190. CrossRef Medline
25. MacAskill AF, Kittler JT (2010) Control of mitochondrial transport and localization in neurons. Trends Cell Biol 20:102-112. CrossRef Medline
26. Macaskill AF, Rinholm JE, Twelvetrees AE, Arancibia-Carcamo IL, Muir J, Fransson A, Aspenstrom P, Attwell D, Kittler JT (2009) Mirol is a calcium sensor for glutamate receptor-dependent localization of mitochondria at synapses. Neuron 61:541-555. CrossRef Medline
27. Medvedeva YV, Kim MS, Usachev YM (2008) Mechanisms of prolonged presynaptic Ca2+ signaling and glutamate release induced by TRPV1 activation in rat sensory neurons. J Neurosci 28:5295-5311. CrossRef Medline
28. Meijering E, Jacob M, Sarria JC, Steiner P, Hirling H, Unser M (2004) Design and validation of a tool for neurite tracing and analysis in fluorescence microscopy images. Cytometry A 58:167-176. CrossRef Medline
29. Nagai T, Sawano A, Park ES, Miyawaki A (2001) Circularly permuted green fluorescent proteins engineered to sense Ca2 +. Proc Natl Acad Sci U S A 98:3197-3202. CrossRef Medline
30. Page KM, Heblich F, Margas W, Pratt WS, Nieto-Rostro M, Chaggar K, Sandhu K, Davies A, Dolphin AC (2010) N terminus is key to the dominant negative suppression of Ca(V)2 calcium channels: implications for episodic ataxia type 2. J Biol Chem 285:835-844. CrossRef Medline
31. Patel R, Bauer CS, Nieto-Rostro M, Margas W, Ferron L, Chaggar K, Crews K, Ramirez JD, Bennett DL, Schwartz A, Dickenson AH, Dolphin AC (2013) a2δ-1 Gene deletion affects somatosensory neuron function and delays mechanical hypersensitivity in response to peripheral nerve damage. J Neurosci 33:16412-16426. CrossRef Medline
32. Perkins GA, Tjong J, Brown JM, Poquiz PH, Scott RT, Kolson DR, Ellisman MH, Spirou GA (2010) The micro-architecture of mitochondria at active zones: electron tomography reveals novel anchoring scaffolds and cristae structured for high-rate metabolism. J Neurosci 30:1015-1026. CrossRef Medline
33. Raffaello A, De Stefani D, Sabbadin D, Teardo E, Merli G, Picard A, Checchetto V, Moro S, Szabò I, Rizzuto R (2013) The mitochondrial calcium uniporter is a multimer that can include a dominant-negative poreforming subunit. EMBO J 32:2362-2376. CrossRef Medline
34. Raghib A, Bertaso F, Davies A, Page KM, Meir A, Bogdanov Y, Dolphin AC (2001) Dominant-negative synthesis suppression of voltage-gated calcium channel Cav2.2 induced by truncated constructs. J Neurosci 21: 8495-8504. Medline
35. Rizzuto R, De Stefani D, Raffaello A, Mammucari C (2012) Mitochondria as sensors and regulators of calcium signalling. Nat Rev Mol Cell Biol 13: 566-578. CrossRef Medline
36. Scroggs RS, Fox AP (1992) Calcium current variation between acutely isolated adult rat dorsal root ganglion neurons of different size. J Physiol 445:639-658. CrossRef Medline
37. Sheng ZH, Cai Q (2012) Mitochondrial transport in neurons: impact on synaptic homeostasis and neurodegeneration. Nat Rev Neurosci 13:77-93. CrossRef Medline
38. Shmigol A, Verkhratsky A, Isenberg G (1995) Calcium-induced calcium release in rat sensory neurons. J Physiol 489:627-636. CrossRef Medline
39. Shutov LP, Kim MS, Houlihan PR, Medvedeva YV, Usachev YM (2013) Mitochondria and plasma membrane Ca2 +-ATPase control presynaptic Ca2+ clearance in capsaicin-sensitive rat sensory neurons. J Physiol 591: 2443-2462. CrossRef Medline
40. Tinker A, Jan YN, Jan LY (1996) Regions responsible for the assembly of inwardly rectifying potassium channels. Cell 87:857-868. CrossRef Medline
41. Usachev YM, Thayer SA (1997) All-or-none Ca2+ release from intracellular stores triggered by Ca2 + influx through voltage-gated Ca2 + channels in rat sensory neurons. J Neurosci 17:7404-7414. Medline
42. Wang X, Schwarz TL (2009) The mechanism of Ca2+-dependent regulation of kinesin-mediated mitochondrial motility. Cell 136:163-174. CrossRef Medline
43. Werth JL, Thayer SA (1994) Mitochondria buffer physiological calcium loads in cultured rat dorsal root ganglion neurons. J Neurosci 14:348-356. Medline
44. Wheeler DG, Groth RD, Ma H, Barrett CF, Owen SF, Safa P, Tsien RW (2012) Ca(V)l and Ca(V)2 channels engage distinct modes of Ca(2+) signaling to control CREB-dependent gene expression. Cell 149:1112-1124. CrossRef Medline
45. Wood JN, Winter J, James IF, Rang HP, Yeats J, Bevan S (1988) Capsaicin-induced ion fluxes in dorsal root ganglion cells in culture. J Neurosci 8:3208-3220. Medline
46. Xiao HS, Huang QH, Zhang FX, Bao L, Lu YJ, Guo C, Yang L, Huang WJ, Fu G, Xu SH, Cheng XP, Yan Q, Zhu ZD, Zhang X, Chen Z, Han ZG, Zhang X (2002) Identification of gene expression profile of dorsal root ganglion in the rat peripheral axotomy model of neuropathic pain. Proc Natl Acad Sci U S A 99:8360-8365. CrossRef Medline