Calpains mediate axonal cytoskeleton disintegration during Wallerian degeneration

Neurobiology of Disease

Volumn 56, Issue , 2013, Pages 34-46

  Ma, Marek ^a,b   Ferguson, Toby A ^c   Schoch, Kathleen M ^d   Li, Jian ^a   Qian, Yaping ^c   Shofer, Frances S ^a   Saatman, Kathryn E ^d   Neumar, Robert W ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c TEMPLE UNIVERSITY   (United States)

^d UNIVERSITY OF KENTUCKY   (United States)

Author keywords

Axon; Calpain; Calpastatin; Neurofilament; Neuromuscular junction; Wallerian degeneration

Indexed keywords

CALPAIN; CALPASTATIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOSKELETON; IN VIVO STUDY; MOUSE; MUSCLE ACTION POTENTIAL; NERVE FIBER; NERVE TRANSECTION; NEUROFILAMENT; NEUROMUSCULAR SYNAPSE; NONHUMAN; OPTIC NERVE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; SCIATIC NERVE; SYNAPSE; TRANSGENIC MOUSE; WALLERIAN DEGENERATION; WILD TYPE;

ANIMALS; AXONS; CALCIUM-BINDING PROTEINS; CALPAIN; CEREBRAL CORTEX; CYTOSKELETON; ELECTROMYOGRAPHY; ELECTROPHYSIOLOGICAL PROCESSES; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; MICE; MICE, TRANSGENIC; NEUROFILAMENT PROTEINS; NEUROMUSCULAR JUNCTION; OPTIC NERVE; RETINA; SCIATIC NERVE; WALLERIAN DEGENERATION;

EID: 84877315278     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2013.03.009     Document Type: Article

References (51)

1. Ai J., Liu E., Wang J., Chen Y., Yu J., Baker A.J. Calpain inhibitor MDL-28170 reduces the functional and structural deterioration of corpus callosum following fluid percussion injury. J. Neurotrauma 2007, 24:960-978.
2. Bauder A.R., Ferguson T.A. Reproducible mouse sciatic nerve crush and subsequent assessment of regeneration by whole mount muscle analysis. J. Vis. Exp. 2012, 60:e3606.
3. Beirowski B., Nógrádi A., Babetto E., Garcia-Alias G., Coleman M.P. Mechanisms of axonal spheroid formation in central nervous system Wallerian degeneration. J. Neuropathol. Exp. Neurol. 2010, 69:455-472.
4. Bignami A., Dahl D., Nguyen B.T., Crosby C.J. The fate of axonal debris in Wallerian degeneration of rat optic and sciatic nerves. Electron microscopy and immunofluorescence studies with neurofilament antisera. J. Neuropathol. Exp. Neurol. 1981, 40:537-550.
5. Blumbergs P.C., Scott G., Manavis J., Wainwright H., Simpson D.A., McLean A.J. Topography of axonal injury as defined by amyloid precursor protein and the sector scoring method in mild and severe closed head injury. J. Neurotrauma 1995, 12:565-572.
6. Coleman M. Axon degeneration mechanisms: commonality amid diversity. Nat. Rev. Neurosci. 2005, 6:889-898.
7. Couto L.A., Narciso M.S., Hokoç J.N., Martinez A.M.B. Calpain inhibitor 2 prevents axonal degeneration of opossum optic nerve fibers. J. Neurosci. Res. 2004, 77:410-419.
8. Cui Q., Yip H.K., Zhao R.C.H., So K.-F., Harvey A.R. Intraocular elevation of cyclic AMP potentiates ciliary neurotrophic factor-induced regeneration of adult rat retinal ganglion cell axons. Mol. Cell. Neurosci. 2003, 22:49-61.
9. Finn J.T., Weil M., Archer F., Siman R., Srinivasan A., Raff M.C. Evidence that Wallerian degeneration and localized axon degeneration induced by local neurotrophin deprivation do not involve caspases. J. Neurosci. 2000, 20:1333-1341.
10. George R., Griffin J.W. Delayed macrophage responses and myelin clearance during Wallerian degeneration in the central nervous system: the dorsal radiculotomy model. Exp. Neurol. 1994, 129:225-236.
11. George E.B., Glass J.D., Griffin J.W. Axotomy-induced axonal degeneration is mediated by calcium influx through ion-specific channels. J. Neurosci. 1995, 15:6445-6452.
12. Glass J.D. Wallerian degeneration as a window to peripheral neuropathy. J. Neurol. Sci. 2004, 220:123-124.
13. Glass J.D., Culver D.G., Levey A.I., Nash N.R. Very early activation of m-calpain in peripheral nerve during Wallerian degeneration. J. Neurol. Sci. 2002, 196:9-20.
14. Goll D.E., Thompson V.F., Li H., Wei W., Cong J. The calpain system. Physiol. Rev. 2003, 83:731-801.
15. Gundersen H.J.G., Bendtsen T.F., Korbo L., Marcussen N., Møller A., Nielsen K., et al. Some new, simple and efficient stereological methods and their use in pathological research and diagnosis. APMIS 1988, 96:379-394.
16. Jiang Q., Stys P.K. Calpain inhibitors confer biochemical, but not electrophysiological, protection against anoxia in rat optic nerves. J. Neurochem. 2000, 74:2101-2107.
17. Kaasik A., Rikk T., Piirsoo A., Zharkovsky T., Zharkovsky A. Up-regulation of lysosomal cathepsin L and autophagy during neuronal death induced by reduced serum and potassium. Eur. J. Neurosci. 2005, 22:1023-1031.
18. Knöferle J., Koch J.C., Ostendorf T., Michel U., Planchamp V., Vutova P., et al. Mechanisms of acute axonal degeneration in the optic nerve in vivo. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:6064-6069.
19. Kwong J.M.K., Quan A., Kyung H., Piri N., Caprioli J. Quantitative analysis of retinal ganglion cell survival with Rbpms immunolabeling in animal models of optic neuropathies. Invest. Ophthalmol. Vis. Sci. 2011, 52:9694-9702.
20. Ma M., Matthews B.T., Lampe J.W., Meaney D.F., Shofer F.S., Neumar R.W. Immediate short-duration hypothermia provides long-term protection in an in vivo model of traumatic axonal injury. Exp. Neurol. 2009, 215:119-127.
21. Mack T.G.A., Reiner M., Beirowski B., Mi W., Emanuelli M., Wagner D., Thomson D., et al. Wallerian degeneration of injured axons and synapses is delayed by a Ube4b/Nmnat chimeric gene. Nat. Neurosci. 2001, 4:1199-1206.
22. Marques S.A., Taffarel M., Martinez A.M.B. Participation of neurofilament proteins in axonal dark degeneration of rat's optic nerves. Brain Res. 2003, 969:1-13.
23. McGonigal R., Rowan E.G., Greenshields K.N., Halstead S.K., Humphreys P.D., Rother R.P., et al. Anti-GD1a antibodies activate complement and calpain to injure distal motor nodes of Ranvier in mice. Brain 2010, 133:1944-1960.
24. Medana I.M., Esiri M.M. Axonal damage: a key predictor of outcome in human CNS diseases. Brain 2003, 126:515-530.
25. Miledi R., Slater C.R. On the degeneration of rat neuromuscular junctions after nerve section. J. Physiol. 1970, 207:507-528.
26. Moldovan M., Alvarez S., Krarup C. Motor axon excitability during Wallerian degeneration. Brain 2009, 132:511-523.
27. Narciso M.S., Hokoç J.N., Martinez A.M.B. Watery and dark axons in Wallerian degeneration of the opossum's optic nerve: different patterns of cytoskeletal breakdown?. An. Acad. Bras. Cienc. 2001, 73:231-243.
28. O'Hanlon G.M., Humphreys P.D., Goldman R.S., Halstead S.K., Bullens R.W.M., Plomp J.J., et al. Calpain inhibitors protect against axonal degeneration in a model of anti-ganglioside antibody-mediated motor nerve terminal injury. Brain 2003, 126:2497-2509.
29. Okada E., Mizuhira V., Nakamura H. Abnormalities of the sciatic nerves of dystrophic mice, with reference to nerve counts and mean area of axons. Bull. Tokyo Med. Dent. Univ. 1975, 22:25-43.
30. Okamoto M., Riker W.F. Motor nerve terminals as the site of initial functional changes after denervation. J. Gen. Physiol. 1969, 53:70-80.
31. Osterloh J.M., Yang J., Rooney T.M., Fox A.N., Adalbert R., Powell E.H., et al. dSarm/Sarm1 is required for activation of an injury-induced axon death pathway. Science 2012, 337:481-484.
32. Osuchowski M.F., Teener J., Remick D. Noninvasive model of sciatic nerve conduction in healthy and septic mice: reliability and normative data. Muscle Nerve 2009, 40:610-616.
33. Park E., Liu E., Shek M., Park A., Baker A.J. Heavy neurofilament accumulation and α-spectrin degradation accompany cerebellar white matter functional deficits following forebrain fluid percussion injury. Exp. Neurol. 2007, 204:49-57.
34. Pietsch M., Chua K.C.H., Abell A.D. Calpains: attractive targets for the development of synthetic inhibitors. Curr. Top. Med. Chem. 2010, 10:270-293.
35. Saatman K.E., Murai H., Bartus R.T., Smith D.H., Hayward N.J., Perri B.R., et al. Calpain inhibitor AK295 attenuates motor and cognitive deficits following experimental brain injury in the rat. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:3428-3433.
36. Saatman K.E., Creed J., Raghupathi R. Calpain as a therapeutic target in traumatic brain injury. Neurotherapeutics 2010, 7:31-42.
37. Saxena S., Caroni P. Mechanisms of axon degeneration: from development to disease. Prog. Neurobiol. 2007, 83:174-191.
38. Schoch K.M., von Reyn C.R., Bian J., Telling G.C., Meaney D.F., Saatman K.E. Brain injury-induced proteolysis is reduced in a novel calpastatin-overexpressing transgenic mouse. J. Neurochem 2013, (Jan 10 [Epub ahead of print]) (in press). 10.1111/jnc.12144.
39. Shy M.E., Garbern J.Y., Kamholz J. Hereditary motor and sensory neuropathies: a biological perspective. Lancet Neurol. 2002, 1:110-118.
40. Stys P.K., Jiang Q. Calpain-dependent neurofilament breakdown in anoxic and ischemic rat central axons. Neurosci. Lett. 2002, 328:150-154.
41. Talbot J.D., David G., Barrett E.F., Barrett J.N. Calcium dependence of damage to mouse motor nerve terminals following oxygen/glucose deprivation. Exp. Neurol. 2012, 234:95-104.
42. Trinchese F., Fa' M., Liu S., Zhang H., Hidalgo A., Schmidt S.D., et al. Inhibition of calpains improves memory and synaptic transmission in a mouse model of Alzheimer disease. J. Clin. Invest. 2008, 118:2796-2807.
43. Vargas M.E., Barres B.A. Why is Wallerian degeneration in the CNS so slow?. Annu. Rev. Neurosci. 2007, 30:153-179.
44. Waller A. Experiments on the section of the glossopharyngeal and hypoglossal nerves of the frog, and observations of the alterations produced thereby in the structure of their primitive fibres. Philos. Trans. R. Soc. London 1850, 140:423-429.
45. Wang M.-S., Wu Y., Culver D.G., Glass J.D. Pathogenesis of axonal degeneration: parallels between Wallerian degeneration and vincristine neuropathy. J. Neuropathol. Exp. Neurol. 2000, 59:599-606.
46. Wang M.S., Davis A.A., Culver D.G., Wang Q., Powers J.C., Glass J.D. Calpain inhibition protects against taxol-induced sensory neuropathy. Brain 2004, 127:671-679.
47. Wang J.T., Medress Z.A., Barres B.A. Axon degeneration: molecular mechanisms of a self-destruction pathway. J. Cell Biol. 2012, 196:7-18.
48. Whitmore A.V., Lindsten T., Raff M.C., Thompson C.B. The proapoptotic proteins Bax and Bak are not involved in Wallerian degeneration. Cell Death Differ. 2003, 10:260-261.
49. Yang Y., Fukui K., Koike T., Zheng X. Induction of autophagy in neurite degeneration of mouse superior cervical ganglion neurons. Eur. J. Neurosci. 2007, 26:2979-2988.
50. Zhai Q., Wang J., Kim A., Liu Q., Watts R., Hoopfer E., et al. Involvement of the ubiquitin-proteasome system in the early stages of Wallerian degeneration. Neuron 2003, 39:217-225.
51. Zimmerman U.-J.P., Schlaepfer W.W. Characterization of a brain calcium-activated protease that degrades neurofilament proteins. Biochemistry 1982, 21:3977-3983.