Ca2+ toxicity due to reverse Na+/Ca2+ exchange contributes to degeneration of neurites of DRG neurons induced by a neuropathy-associated Nav1.7 mutation

Journal of Neurophysiology

Volumn 114, Issue 3, 2015, Pages 1554-1564

  Estacion, M ^a,b   Vohra, B P S ^a,b   Liu, S ^a,b   Hoeijmakers, J ^c   Faber, C G ^c   Merkies, I S J ^c,d   Lauria, G ^e   Black, J A ^a,b   Waxman, S G ^a,b  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VA CONNECTICUT HEALTHCARE SYSTEM   (United States)

^c MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

^d Infection and Immunology   (Netherlands)

^e DEPARTMENT OF NEUROSURGERY   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; DEOXYGLUCOSE; MUTANT PROTEIN; POTASSIUM ION; SODIUM CALCIUM EXCHANGE PROTEIN; SODIUM CHANNEL; SODIUM CHANNEL NAV1.7; SODIUM CHANNEL NAV1.8; SODIUM ION; CALCIUM; POTASSIUM; SCN3A PROTEIN, HUMAN; SODIUM; SODIUM CHANNEL NAV1.3;

ADULT; ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CONTROLLED STUDY; DEPOLARIZATION; GENE EXPRESSION; GENE MUTATION; GENETIC TRANSFECTION; HYPERPOLARIZATION; NERVE CELL DEGENERATION; NERVE CELL EXCITABILITY; NEURITE; NONHUMAN; PERIKARYON; PRIORITY JOURNAL; RAT; SMALL FIBER NEUROPATHY; SODIUM CALCIUM EXCHANGE; SODIUM CELL LEVEL; SPINAL CORD NERVE CELL; SPINAL GANGLION; WILD TYPE; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL CULTURE; CYTOLOGY; ERYTHROMELALGIA; GENETICS; HUMAN; METABOLISM; MISSENSE MUTATION; PATHOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; CALCIUM; CELLS, CULTURED; ERYTHROMELALGIA; GANGLIA, SPINAL; HUMANS; MUTATION, MISSENSE; NAV1.3 VOLTAGE-GATED SODIUM CHANNEL; NEURITES; POTASSIUM; RATS; RATS, SPRAGUE-DAWLEY; SODIUM; SODIUM CHANNELS; SODIUM-CALCIUM EXCHANGER;

EID: 84941248150     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00195.2015     Document Type: Article

References (34)

1. Alobuia WM, Xia W, Vohra BP. Axon degeneration is key component of neuronal death in amyloid-β toxicity. Neurochem Int 63: 782-789, 2013.
2. Ames A 3rd, Li YY, Heher EC, Kimble CR. Energy metabolism of rabbit retina as related to function: high cost of Na+ transport. J Neurosci 12: 840-853, 1992.
3. Annunziato L, Pignataro G, Di Renzo GF. Pharmacology of brain Na+/ Ca2+ exchanger: from molecular biology to therapeutic perspectives. Pharmacol Rev 56: 633-654, 2004.
4. Baloh RH, Schmidt RE, Pestronk A, Milbrandt J. Altered axonal mito-chondrial transport in the pathogenesis of Charcot-Marie-Tooth disease from mitofusin 2 mutations. J Neurosci 27: 422-423, 2007.
5. Brustovetsky T, Brittain MK, Sheets PL, Cummins TR, Pinelis V, Brus-tovetsky N. KB-R7943, an inhibitor of the reverse Na+/Ca2+ exchanger, blocks N-methyl-D-aspartate receptor and inhibits mitochondrial complex I. Br J Pharmacol 162: 255-270, 2011.
6. Catterall WA, Goldin AL, Waxman SG. International Union of Pharmacology. XLVII Nomenclature and structure-function relationships of voltage-gated sodium channels. Pharmacol Rev 57: 397-409, 2005.
7. Cummins TR, Howe JR, Waxman SG. Slow closed-state inactivation: a novel mechanism underlying ramp currents in cells expressing the hNE/PN1 sodium channel. J Neurosci 18: 9607-9619, 1998.
8. David G, Barrett JN, Barrett EF. Spatiotemporal gradients of intra-axonal [Na+] after transection and resealing in lizard peripheral myelinated axons. J Physiol 498: 295-307, 1997.
9. Estacion M, Han C, Choi JS, Hoeijmakers JG, Lauria G, Drenth JP, Gerrits MM, Dib-Hajj SD, Faber CG, Merkies IS, Waxman SG. Intra- and interfamily phenotypic diversity in pain syndromes associated with a gain-of-function variant of NaV1.7. Mol Pain 7: 92, 2011.
10. Estacion M, Waxman SG. The response of Nav1.3 sodium channels to ramp stimuli: multiple components and mechanisms. J Neurophysiol 109: 306-314, 2013.
11. Faber CG, Hoeijmakers JG, Ahn HS, Cheng X, Han C, Choi JS, Estacion M, Lauria G, Vanhoutte EK, Gerrits MM, Dib-Hajj S, Drenth JP, Waxman SG, Merkies IS. Gain of function Nav1.7 mutations in idiopathic small fiber neuropathy. Ann Neurol 71: 26-39, 2012.
12. Fleidervish IA, Lasser-Ross N, Gutnick MJ, Ross WN. Na+ imaging reveals little difference in action potential-evoked Na+ influx between axon and soma. Nat Neurosci 13: 852-860, 2010.
13. Han C, Hoeijmakers JG, Liu S, Gerrits MM, te Morsche RH, Lauria G, Dib-Hajj SD, Drenth JP, Faber CG, Merkies IS, Waxman SG. Functional profiles of SCN9A variants in dorsal root ganglion neurons and superior cervical ganglion neurons correlate with autonomic symptoms in small fibre neuropathy. Brain 135: 2613-2628, 2012.
14. Hertz L, Schousboe A. Ion and energy metabolism of the brain at the cellular level. Int Rev Neurobiol 18: 141-211, 1975.
15. Herzog RI, Cummins TR, Ghassemi F, Dib-Hajj SD, Waxman SG. Distinct repriming and closed-state inactivation kinetics of Nav1.6 and Nav1.7 sodium channels in mouse spinal sensory neurons. J Physiol 551: 741-750,2003.
16. Hoeijmakers JG, Faber CG, Lauria G, Merkies IS, Waxman SG. Small-fibre neuropathies-advances in diagnosis, pathophysiology, and management. Nat Rev Neurol 8: 369-379, 2012a.
17. Hoeijmakers JG, Han C, Merkies IS, Macala LJ, Lauria G, Gerrits MM, Dib-Hajjj SD, Faber CG, Waxman SG. Small nerve fibres, small hands, and small feet: a new syndrome of pain, dysautonomia and acromesomelia in a kindred with a novel NaV1.7 mutation. Brain 135: 345-358, 2012b.
18. Lehmann HC, Chen W, Borzan J, Mankowski JL, Hoke A. Mitochondrial dysfunction in distal axons contributes to human immunodeficiency virus sensory neuropathy. Ann Neurol 69: 100-110, 2011.
19. Lehning EJ, Doshi R, Isaksson N, Stys PK, LoPachin RM Jr. Mechanisms of injury-induced calcium entry into peripheral nerve myelinated axons: role of reverse sodium-calcium exchange. J Neurochem 66: 493-500, 1996.
20. Nikolaeva MA, Mukherjee B, Stys PK. Na+-dependent sources of intra-axonal Ca2+ release in rat optic nerve during in vitro chemical ischemia. J Neurosci 25: 9960-9967, 2005.
21. Persson AK, Black JA, Gasser A, Cheng X, Fischer TZ, Waxman SG. Sodium-calcium exchanger and multiple sodium channel isoforms in intra-epidermal nerve terminals. Mol Pain 6: 84, 2010.
22. Persson AK, Kim I, Zhao P, Estacion M, Black JA, Waxman SG. Sodium channels contribute to degeneration of dorsal root ganglion neurites induced by mitochondrial dysfunction in an in vitro model of axonal injury. J Neurosci 33: 19250-19261, 2013a.
23. Persson AK, Liu S, Faber CG, Merkies IS, Black JA, Waxman SG. Neuropathy-associated Nav1.7 variant I228M impairs integrity of dorsal root ganglion neuron axons. Ann Neurol 73: 140-145, 2013b.
24. Rahman M, Inman M, Kiss l Janssen LJ. Reverse-mode NCX current in mouse airway smooth muscle: Na(+) and voltage dependence, contributions to Ca(2+) influx and contraction, and altered expression in a model of allergen-induced hyperresponsiveness. Acta Physiol (Oxf) 205: 279-291, 2012.
25. Ross W, Fleidervish I, Lasser-Ross N. Imaging sodium in axons and dendrites. Cold Spring Harb Protoc 2013: 433-437, 2013.
26. Rush AM, Cummins TR, Waxman SG. Multiple sodium channels and their roles in electrogenesis within dorsal root ganglion neurons. J Physiol 579: 1-14, 2007.
27. Rush AM, Dib-Hajj SD, Liu S, Cummins TR, Black JA, Waxman SG. A single sodium channel mutation produces hyper- or hypoexcitability in different types of neurons. Proc Natl Acad SciUSA 103: 8245-8250, 2006.
28. Sokoloff L. Energetics of functional activation in neural tissues. Neurochem Res 24: 321-329, 1999.
29. Stys PK, Waxman SG, Ransom BR. Ionic mechanisms of anoxic injury in mammalian CNS white matter: role of Na+ channels and Na+-Ca2+ exchanger. J Neurosci 12: 430-439, 1992.
30. Summers DW, DiAntonio A, Milbrandt J. Mitochondrial dysfunction induces sarm1-dependent cell death in sensory neurons. J Neurosci 34: 9338-9350, 2014.
31. Svichar N, Shishkin V, Kostyuk P. Mitochondrial participation in the modulation of calcium transients in DRG neurons. NeuroReport 10: 1257-1261, 1999.
32. Toledo-Aral JJ, Moss BL, He ZJ, Koszowski AG, Whisenand T, Levinson SR, Wolf JJ, Silos-Santiago I, Halegoua S, Mandel G. Identification of PN1, a predominant voltage-dependent sodium channel expressed principally in peripheral neurons. Proc Natl Acad SciUSA 94: 1527-1532, 1997.
33. Vasylyev DV, Han C, Zhao P, Dib-Hajj S, Waxman SG. Dynamic-clamp analysis of wild-type human Nav1.7 and erythromelalgia mutant channel L858H. J Neurophysiol 111: 1429-1443, 2014.
34. Watanabe Y, Koide Y, Kimura J. Topics on the Na+ /Ca2+ exchanger: pharmacological characterization of Na+/Ca2+ exchanger inhibitors. J Pharm Sci 102: 7-16, 2006.