Sodium and potassium currents influence wallerian degeneration of injured Drosophila axons

Journal of Neuroscience

Volumn 33, Issue 48, 2013, Pages 18728-18739

  Mishra, Bibhudatta ^a   Carson, Ross ^a   Hume, Richard I ^a   Collins, Catherine A ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

POTASSIUM CHANNEL; VOLTAGE GATED SODIUM CHANNEL; CALCIUM; SHAKER POTASSIUM CHANNEL; SODIUM CHANNEL; SODIUM CHANNEL BLOCKING AGENT; TETRODOTOXIN;

ACTION POTENTIAL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DROSOPHILA; ELECTROPHYSIOLOGY; EXCITATORY JUNCTION POTENTIAL; GENETIC MANIPULATION; IMMUNOCYTOCHEMISTRY; MALE; MEMBRANE POTENTIAL; MOTONEURON; NERVE CELL EXCITABILITY; NERVE CRUSH; NERVE FIBER DEGENERATION; NEUROMUSCULAR SYNAPSE; NONHUMAN; POTASSIUM CURRENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; SODIUM CURRENT; WALLERIAN DEGENERATION; ANIMAL; CONFOCAL MICROSCOPY; GENETICS; IMMUNOHISTOCHEMISTRY; METABOLISM; NERVE FIBER; PATHOPHYSIOLOGY; PHYSIOLOGY; SYNAPSE; TEMPERATURE;

ACTION POTENTIALS; ANIMALS; AXONS; CALCIUM; DROSOPHILA; ELECTROPHYSIOLOGICAL PROCESSES; IMMUNOHISTOCHEMISTRY; MICROSCOPY, CONFOCAL; NERVE CRUSH; NEUROMUSCULAR JUNCTION; POTASSIUM CHANNELS; SHAKER SUPERFAMILY OF POTASSIUM CHANNELS; SODIUM CHANNEL BLOCKERS; SODIUM CHANNELS; SYNAPSES; TEMPERATURE; TETRODOTOXIN; WALLERIAN DEGENERATION;

EID: 84888225361     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1007-13.2013     Document Type: Article

References (74)

1. AbeggMH (2007) Rhythmic synaptic activity induced by mechanical injury of rat CA3 hippocampal area. J Neurotrauma 24:1536-1542. CrossRef Medline
2. Aberle H, Haghighi AP, Fetter RD, McCabe BD, Magãlhaes TR, Goodman CS (2002) Wishful thinking encodes a BMP type II receptor that regulates synaptic growth in Drosophila. Neuron 33:545-558. CrossRef Medline
3. Adalbert R, Morreale G, Paizs M, Conforti L, Walker SA, Roderick HL, Bootman MD, Siklós L, Coleman MP (2012) Intra-axonal calcium changes after axotomy in wild-type and slow Wallerian degeneration axons. Neuroscience 225:44-54.
4. Ambron RT, Walters ET (1996) Priming events and retrograde injury signals: a new perspective on the cellular and molecular biology of nerve regeneration. Mol Neurobiol 13:61-79. CrossRef Medline
5. 2+ buffering. Curr Biol 22:596-600. CrossRef Medline
6. Babetto E, Beirowski B, Russler EV, Milbrandt J, DiAntonio A (2013) The Phr1 ubiquitin ligase promotes injury-induced axon self-destruction. Cell Rep 3:1422-1429. CrossRef Medline
7. Baines RA, Uhler JP, Thompson A, Sweeney ST, Bate M (2001) Altered electrical properties in Drosophila neurons developing without synaptic transmission. J Neurosci 21:1523-1531. Medline
8. Bainton RJ, Tsai LT, Schwabe T, DeSalvo M, Gaul U, Heberlein U (2005) moody encodes two GPCRs that regulate cocaine behaviors and blood-brain barrier permeability in Drosophila. Cell 123:145-156. CrossRef Medline
9. Barrientos SA, Martinez NW, Yoo S, Jara JS, Zamorano S, Hetz C, Twiss JL, Alvarez J, Court FA (2011) Axonal degeneration is mediated by the mitochondrial permeability transition pore. J Neurosci 31:966-978. CrossRef Medline
10. Bechtold DA, Yue X, Evans RM, Davies M, Gregson NA, Smith KJ (2005) Axonal protection in experimental autoimmune neuritis by the sodium channel blocking agent flecainide. Brain 128:18-28. CrossRef Medline
11. Birks R, Katz B, Miledi R (1960) Physiological and structural changes at the amphibian myoneural junction, in the course of nerve degeneration. J Physiol 150:145-168. Medline
12. Bittner GD (1991) Long-term survival of anucleate axons and its implications for nerve regeneration. Trends Neurosci 14:188-193. CrossRef Medline
13. Budnik V, Gorczyca M, Prokop A (2006) Selected methods for the anatomical study of Drosophila embryonic and larval neuromuscular junctions. Int Rev Neurobiol 75:323-365. CrossRef Medline
14. Chaudhry V, Cornblath DR (1992) Wallerian degeneration in human nerves: serial electrophysiological studies. Muscle Nerve 15:687-693. CrossRef Medline
15. ColemanM (2005) Axon degeneration mechanisms: commonality amid diversity. Nat Rev Neurosci 6:889-898. CrossRef Medline
16. Coleman MP, Freeman MR (2010) Wallerian degeneration, wld(s), and nmnat. Annu Rev Neurosci 33:245-267. CrossRef Medline
17. Eddleman CS, Ballinger ML, Smyers ME, Fishman HM, Bittner GD (1998) Endocytotic formation of vesicles and other membranous structures induced by Ca2+ and axolemmal injury. J Neurosci 18:4029-4041. Medline
18. Ganetzky B, Wu CF (1982) Drosophila mutants with opposing effects on nerve excitability: genetic and spatial interactions in repetitive firing. J Neurophysiol 47:501-514. Medline
19. Ganetzky B, Wu CF (1983) Neurogenetic analysis of potassium currents in Drosophila: synergistic effects on neuromuscular transmission in double mutants. J Neurogenet 1:17-28. CrossRef Medline
20. Ganetzky B, Loughney K, Wu CF (1986) Analysis of mutations affecting sodium channels in Drosophila. AnnN Y Acad Sci 479:325-337. CrossRef Medline
21. George EB, Glass JD, Griffin JW (1995) Axotomy-induced axonal degeneration is mediated by calcium influx through ion-specific channels. J Neurosci 15:6445-6452. Medline
22. Gilley J, Coleman MP (2010) Endogenous Nmnat2 is an essential survival factor for maintenance of healthy axons. PLoS Biol 8:e1000300. CrossRef Medline
23. Gillingwater TH, Haley JE, Ribchester RR, Horsburgh K (2004) Neuroprotection after transient global cerebral ischemia in Wld(s) mutant mice. J Cereb Blood Flow Metab 24:62-66. CrossRef Medline
24. Glass JD, Schryer BL, Griffin JW (1994) Calcium-mediated degeneration of the axonal cytoskeleton in the Ola mouse. J Neurochem 62:2472-2475. Medline
25. Hodge JJ (2009) Ion channels to inactivate neurons in Drosophila. Front Mol Neurosci 2:13. CrossRef Medline
26. Hummel T, Krukkert K, Roos J, Davis G, Klämbt C (2000) Drosophila Futsch/22C10 is a MAP1B-like protein required for dendritic and axonal development. Neuron 26:357-370. CrossRef Medline
27. Hunt CC, Nelson PG (1965) Structural and functional changes in the frog sympathetic ganglion following cutting of the presynaptic nerve fibres. J Physiol 177:1-20. Medline
28. Jan YN, Jan LY, Dennis MJ (1977) Two mutations of synaptic transmission in Drosophila. Proc R Soc Lond B Biol Sci 198:87-108. CrossRef Medline
29. Johns DC, Marx R, Mains RE, O'Rourke B, Marbán E (1999) Inducible genetic suppression of neuronal excitability. J Neurosci 19:1691-1697. Medline
30. Kaneko S, Wang J, Kaneko M, Yiu G, Hurrell JM, Chitnis T, Khoury SJ, He Z (2006) Protecting axonal degeneration by increasing nicotinamide adenine dinucleotide levels in experimental autoimmune encephalomyelitis models. J Neurosci 26:9794-9804. CrossRef Medline
31. 3H]-tetrodotoxin binding in the napts paralytic mutant of Drosophila. Mol Gen Genet 187:172-173. CrossRef Medline
32. Keshishian H, Broadie K, Chiba A, Bate M (1996) The drosophila neuromuscular junction: a model system for studying synaptic development and function. Annu Rev Neurosci 19:545-575. CrossRef Medline
33. Knöferle J, Koch JC, Ostendorf T, Michel U, Planchamp V, Vutova P, Tönges L, Stadelmann C, Brück W, Bähr M, Lingor P (2010) Mechanisms of acute axonal degeneration in the optic nerve in vivo. Proc Natl Acad Sci U S A 107:6064-6069. CrossRef Medline
34. Kuwada JY, Wine JJ (1981) Transient, axotomy-induced changes in the membrane properties of crayfish central neurones. J Physiol 317:435-461. Medline
35. Lo Pachin RM Jr, LoPachin VR, Saubermann AJ (1990) Effects of axotomy on distribution and concentration of elements in rat sciatic nerve. J Neurochem 54:320-332. CrossRef Medline
36. Loughney K, Kreber R, Ganetzky B (1989) Molecular analysis of the para locus, a sodium channel gene in Drosophila. Cell 58:1143-1154. CrossRef Medline
37. Lubińska L (1977) Early course of Wallerian degeneration in myelinated fibres of the rat phrenic nerve. Brain Res 130:47-63. CrossRef Medline
38. Luttges MW, Kelly PT, Gerren RA (1976) Degenerative changes in mouse sciatic nerves: electrophoretic and electrophysiologic characterizations. Exp Neurol 50:706-733. CrossRef Medline
39. Mata M, Staple J, Fink DJ (1986) Changes in intra-axonal calcium distribution following nerve crush. J Neurobiol 17:449-467. CrossRef Medline
40. McDonald WI (1972) The time course of conduction failure during degeneration of a central tract. Exp Brain Res 14:550-556. Medline
41. Miledi R, Slater CR (1970) On the degeneration of rat neuromuscular junctions after nerve section. J Physiol 207:507-528. Medline
42. Miller BR, Press C, Daniels RW, Sasaki Y, Milbrandt J, DiAntonio A (2009) A dual leucine kinase-dependent axon self-destruction program promotes Wallerian degeneration. Nat Neurosci 12:387-389. CrossRef Medline
43. Moldovan M, Alvarez S, Krarup C (2009) Motor axon excitability during Wallerian degeneration. Brain 132:511-523. CrossRef Medline
44. Mosca TJ, Carrillo RA, White BH, Keshishian H (2005) Dissection of synaptic excitability phenotypes by using a dominant-negative shaker K+ channel subunit. Proc Natl Acad Sci U S A 102:3477-3482. CrossRef Medline
45. Nelson JC, Wyman RJ (1990) Examination of paralysis in Drosophila temperature-sensitive paralytic mutations affecting sodium channels: a proposed mechanism of paralysis. J Neurobiol 21:453-469. CrossRef Medline
46. Nitabach MN, Blau J, Holmes TC (2002) Electrical silencing of Drosophila pacemaker neurons stops the free-running circadian clock. Cell 109:485-495. CrossRef Medline
47. O'Dowd DK, Germeraad SE, Aldrich RW (1989) Alterations in the expression and gating of Drosophila sodium channels by mutations in the para gene. Neuron 2:1301-1311. CrossRef Medline
48. Osterloh JM, Yang J, Rooney TM, Fox AN, Adalbert R, Powell EH, Sheehan AE, Avery MA, Hackett R, Logan MA, MacDonald JM, Ziegenfuss JS, Milde S, Hou YJ, Nathan C, Ding A, Brown RH Jr, Conforti L, Coleman M, Tessier-Lavigne M, Züchner S, et al. (2012) dSarm/Sarm1 is required for activation of an injury-induced axon death pathway. Science 337:481-484. CrossRef Medline
49. Press C, Milbrandt J (2008) Nmnat delays axonal degeneration caused by mitochondrial and oxidative stress. J Neurosci 28:4861-4871. CrossRef Medline
50. Ritzenthaler S, Suzuki E, Chiba A (2000) Postsynaptic filopodia in muscle cells interact with innervating motoneuron axons. Nat Neurosci 3:1012-1017. CrossRef Medline
51. Roos J, Hummel T, Ng N, Klämbt C, Davis GW (2000) Drosophila Futsch regulates synaptic microtubule organization and is necessary for synaptic growth. Neuron 26:371-382. CrossRef Medline
52. Schlaepfer WW, Bunge RP (1973) Effects of calcium ion concentration on the degeneration of amputated axons in tissue culture. J Cell Biol 59:456-470. CrossRef Medline
53. Schwabe T, Bainton RJ, Fetter RD, Heberlein U, Gaul U (2005) GPCR signaling is required for blood-brain barrier formation in drosophila. Cell 123:133-144. CrossRef Medline
54. Shen H, Hyrc KL, Goldberg MP (2013) Maintaining energy homeostasis is an essential component of Wld-mediated axon protection. Neurobiol Dis 59:69-79. CrossRef Medline
55. Siddiqi O, Benzer S (1976) Neurophysiological defects in temperaturesensitive paralytic mutants of Drosophila melanogaster. Proc Natl Acad Sci U S A 73:3253-3257. CrossRef Medline
56. Stern M, Kreber R, Ganetzky B (1990) Dosage effects of a Drosophila sodium channel gene on behavior and axonal excitability. Genetics 124:133-143. Medline
57. Stewart BA, Atwood HL, Renger JJ, Wang J, Wu CF (1994) Improved stability of Drosophila larval neuromuscular preparations in haemolymphlike physiological solutions. J Comp Physiol A 175:179-191. CrossRef Medline
58. Stys PK (2005) General mechanisms of axonal damage and its prevention. J Neurol Sci 233:3-13. CrossRef Medline
59. Stys PK, Waxman SG, Ransom BR (1992) Ionic mechanisms of anoxic injury in mammalian CNS white matter: role of Na+channels and Na(+)-Ca2+ exchanger. J Neurosci 12:430-439. Medline
60. Suzuki DT, Grigliatti T, Williamson R (1971) Temperature-sensitive mutations in Drosophila melanogaster: VII. A mutation (para-ts) causing reversible adult paralysis. Proc Natl Acad Sci U S A 68:890-893. CrossRef Medline
61. Tanouye MA, Ferrus A, Fujita SC (1981) Abnormal action potentials associated with the shaker complex locus of Drosophila. Proc Natl Acad Sci U S A 78:6548-6552. CrossRef Medline
62. Tian L, Hires SA, Mao T, Huber D, Chiappe ME, Chalasani SH, Petreanu L, Akerboom J, McKinney SA, Schreiter ER, Bargmann CI, Jayaraman V, Svoboda K, Looger LL (2009) Imaging neural activity in worms, flies and mice with improvedGCaMPcalcium indicators. Nat Methods 6:875-881. CrossRef Medline
63. Titmus MJ, Faber DS (1990) Axotomy-induced alterations in the electrophysiological characteristics of neurons. Prog Neurobiol 35:1-51. CrossRef Medline
64. Tsao JW, George EB, Griffin JW (1999) Temperature modulation reveals three distinct stages of Wallerian degeneration. J Neurosci 19:4718-4726. Medline
65. Walters ET, Alizadeh H, Castro GA (1991) Similar neuronal alterations induced by axonal injury and learning in Aplysia. Science 253:797-799. CrossRef Medline
66. Wang JT, Medress ZA, Barres BA (2012) Axon degeneration: molecular mechanisms of a self-destruction pathway. J Cell Biol 196:7-18. CrossRef Medline
67. Waxman SG (2006) Axonal conduction and injury in multiple sclerosis: the role of sodium channels. Nat Rev Neurosci 7:932-941. CrossRef Medline
68. WuCF, Ganetzky B (1980) Genetic alteration of nerve membrane excitability in temperature-sensitive paralytic mutants of Drosophila melanogaster. Nature 286:814-816. CrossRef Medline
69. Xiong X, Collins CA (2012) A conditioning lesion protects axons from degeneration via the Wallenda/DLK MAP kinase signaling cascade. J Neurosci 32:610-615. CrossRef Medline
70. Xiong X, Wang X, Ewanek R, Bhat P, Diantonio A, Collins CA (2010) Protein turnover of the Wallenda/DLK kinase regulates a retrograde response to axonal injury. J Cell Biol 191:211-223. CrossRef Medline
71. Xiong X, Hao Y, Sun K, Li J, Li X, Mishra B, Soppina P, Wu C, Hume RI, Collins CA (2012) The highwire ubiquitin ligase promotes axonal degeneration by tuning levels of nmnat protein. PLoS Biol 10:e1001440. CrossRef Medline
72. Zhang B, Stewart B (2010) Electrophysiological recording from Drosophila larval body-wall muscles. Cold Spring Harb Protoc 2010:pdb. prot5487. CrossRef Medline
73. Ziv NE, Spira ME (1993) Spatiotemporal distribution of Ca2+ following axotomy and throughout the recovery process of cultured Aplysia neurons. Eur J Neurosci 5:657-668. CrossRef Medline
74. Ziv NE, Spira ME (1995) Axotomy induces a transient and localized elevation of the free intracellular calcium concentration to the millimolar range. J Neurophysiol 74:2625-2637. Medline