{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,1]],"date-time":"2026-10-01T06:01:59Z","timestamp":1790834519267,"version":"4.1.0"},"reference-count":51,"publisher":"Elsevier BV","content-domain":{"domain":["elsevier.com","sciencedirect.com"],"crossmark-restriction":true},"short-container-title":["Neurobiology of Disease"],"published-print":{"date-parts":[[2013,8]]},"DOI":"10.1016\/j.nbd.2013.03.009","type":"journal-article","created":{"date-parts":[[2013,3,28]],"date-time":"2013-03-28T00:49:45Z","timestamp":1364431785000},"page":"34-46","update-policy":"https:\/\/doi.org\/10.1016\/elsevier_cm_policy","source":"Crossref","is-referenced-by-count":111,"special_numbering":"C","title":["Calpains mediate axonal cytoskeleton disintegration during Wallerian degeneration"],"prefix":"10.1016","volume":"56","author":[{"given":"Marek","family":"Ma","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Toby A.","family":"Ferguson","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kathleen M.","family":"Schoch","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jian","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yaping","family":"Qian","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Frances S.","family":"Shofer","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kathryn E.","family":"Saatman","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Robert W.","family":"Neumar","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"78","reference":[{"key":"10.1016\/j.nbd.2013.03.009_bb0005","doi-asserted-by":"crossref","first-page":"960","DOI":"10.1089\/neu.2006.0224","article-title":"Calpain inhibitor MDL-28170 reduces the functional and structural deterioration of corpus callosum following fluid percussion injury","volume":"24","author":"Ai","year":"2007","journal-title":"J. Neurotrauma"},{"key":"10.1016\/j.nbd.2013.03.009_bb0010","first-page":"e3606","article-title":"Reproducible mouse sciatic nerve crush and subsequent assessment of regeneration by whole mount muscle analysis","volume":"60","author":"Bauder","year":"2012","journal-title":"J. Vis. Exp."},{"key":"10.1016\/j.nbd.2013.03.009_bb0015","doi-asserted-by":"crossref","first-page":"455","DOI":"10.1097\/NEN.0b013e3181da84db","article-title":"Mechanisms of axonal spheroid formation in central nervous system Wallerian degeneration","volume":"69","author":"Beirowski","year":"2010","journal-title":"J. Neuropathol. Exp. Neurol."},{"key":"10.1016\/j.nbd.2013.03.009_bb0020","doi-asserted-by":"crossref","first-page":"537","DOI":"10.1097\/00005072-198109000-00005","article-title":"The fate of axonal debris in Wallerian degeneration of rat optic and sciatic nerves. Electron microscopy and immunofluorescence studies with neurofilament antisera","volume":"40","author":"Bignami","year":"1981","journal-title":"J. Neuropathol. Exp. Neurol."},{"key":"10.1016\/j.nbd.2013.03.009_bb0025","doi-asserted-by":"crossref","first-page":"565","DOI":"10.1089\/neu.1995.12.565","article-title":"Topography of axonal injury as defined by amyloid precursor protein and the sector scoring method in mild and severe closed head injury","volume":"12","author":"Blumbergs","year":"1995","journal-title":"J. Neurotrauma"},{"key":"10.1016\/j.nbd.2013.03.009_bb0030","doi-asserted-by":"crossref","first-page":"889","DOI":"10.1038\/nrn1788","article-title":"Axon degeneration mechanisms: commonality amid diversity","volume":"6","author":"Coleman","year":"2005","journal-title":"Nat. Rev. Neurosci."},{"key":"10.1016\/j.nbd.2013.03.009_bb0035","doi-asserted-by":"crossref","first-page":"410","DOI":"10.1002\/jnr.20170","article-title":"Calpain inhibitor 2 prevents axonal degeneration of opossum optic nerve fibers","volume":"77","author":"Couto","year":"2004","journal-title":"J. Neurosci. Res."},{"key":"10.1016\/j.nbd.2013.03.009_bb0040","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1016\/S1044-7431(02)00037-4","article-title":"Intraocular elevation of cyclic AMP potentiates ciliary neurotrophic factor-induced regeneration of adult rat retinal ganglion cell axons","volume":"22","author":"Cui","year":"2003","journal-title":"Mol. Cell. Neurosci."},{"key":"10.1016\/j.nbd.2013.03.009_bb0045","doi-asserted-by":"crossref","first-page":"1333","DOI":"10.1523\/JNEUROSCI.20-04-01333.2000","article-title":"Evidence that Wallerian degeneration and localized axon degeneration induced by local neurotrophin deprivation do not involve caspases","volume":"20","author":"Finn","year":"2000","journal-title":"J. Neurosci."},{"key":"10.1016\/j.nbd.2013.03.009_bb0055","doi-asserted-by":"crossref","first-page":"225","DOI":"10.1006\/exnr.1994.1164","article-title":"Delayed macrophage responses and myelin clearance during Wallerian degeneration in the central nervous system: the dorsal radiculotomy model","volume":"129","author":"George","year":"1994","journal-title":"Exp. Neurol."},{"key":"10.1016\/j.nbd.2013.03.009_bb0050","doi-asserted-by":"crossref","first-page":"6445","DOI":"10.1523\/JNEUROSCI.15-10-06445.1995","article-title":"Axotomy-induced axonal degeneration is mediated by calcium influx through ion-specific channels","volume":"15","author":"George","year":"1995","journal-title":"J. Neurosci."},{"key":"10.1016\/j.nbd.2013.03.009_bb0060","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1016\/j.jns.2004.03.010","article-title":"Wallerian degeneration as a window to peripheral neuropathy","volume":"220","author":"Glass","year":"2004","journal-title":"J. Neurol. Sci."},{"key":"10.1016\/j.nbd.2013.03.009_bb0065","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1016\/S0022-510X(02)00013-8","article-title":"Very early activation of m-calpain in peripheral nerve during Wallerian degeneration","volume":"196","author":"Glass","year":"2002","journal-title":"J. Neurol. Sci."},{"key":"10.1016\/j.nbd.2013.03.009_bb0070","doi-asserted-by":"crossref","first-page":"731","DOI":"10.1152\/physrev.00029.2002","article-title":"The calpain system","volume":"83","author":"Goll","year":"2003","journal-title":"Physiol. Rev."},{"key":"10.1016\/j.nbd.2013.03.009_bb0075","doi-asserted-by":"crossref","first-page":"379","DOI":"10.1111\/j.1699-0463.1988.tb05320.x","article-title":"Some new, simple and efficient stereological methods and their use in pathological research and diagnosis","volume":"96","author":"Gundersen","year":"1988","journal-title":"APMIS"},{"key":"10.1016\/j.nbd.2013.03.009_bb0080","doi-asserted-by":"crossref","first-page":"2101","DOI":"10.1046\/j.1471-4159.2000.0742101.x","article-title":"Calpain inhibitors confer biochemical, but not electrophysiological, protection against anoxia in rat optic nerves","volume":"74","author":"Jiang","year":"2000","journal-title":"J. Neurochem."},{"key":"10.1016\/j.nbd.2013.03.009_bb0085","doi-asserted-by":"crossref","first-page":"1023","DOI":"10.1111\/j.1460-9568.2005.04279.x","article-title":"Up-regulation of lysosomal cathepsin L and autophagy during neuronal death induced by reduced serum and potassium","volume":"22","author":"Kaasik","year":"2005","journal-title":"Eur. J. Neurosci."},{"key":"10.1016\/j.nbd.2013.03.009_bb0090","doi-asserted-by":"crossref","first-page":"6064","DOI":"10.1073\/pnas.0909794107","article-title":"Mechanisms of acute axonal degeneration in the optic nerve in vivo","volume":"107","author":"Kn\u00f6ferle","year":"2010","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"10.1016\/j.nbd.2013.03.009_bb0095","doi-asserted-by":"crossref","first-page":"9694","DOI":"10.1167\/iovs.11-7869","article-title":"Quantitative analysis of retinal ganglion cell survival with Rbpms immunolabeling in animal models of optic neuropathies","volume":"52","author":"Kwong","year":"2011","journal-title":"Invest. Ophthalmol. Vis. Sci."},{"key":"10.1016\/j.nbd.2013.03.009_bb0100","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1016\/j.expneurol.2008.09.024","article-title":"Immediate short-duration hypothermia provides long-term protection in an in vivo model of traumatic axonal injury","volume":"215","author":"Ma","year":"2009","journal-title":"Exp. Neurol."},{"key":"10.1016\/j.nbd.2013.03.009_bb0105","doi-asserted-by":"crossref","first-page":"1199","DOI":"10.1038\/nn770","article-title":"Wallerian degeneration of injured axons and synapses is delayed by a Ube4b\/Nmnat chimeric gene","volume":"4","author":"Mack","year":"2001","journal-title":"Nat. Neurosci."},{"key":"10.1016\/j.nbd.2013.03.009_bb0110","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/S0006-8993(02)03834-9","article-title":"Participation of neurofilament proteins in axonal dark degeneration of rat's optic nerves","volume":"969","author":"Marques","year":"2003","journal-title":"Brain Res."},{"key":"10.1016\/j.nbd.2013.03.009_bb0115","doi-asserted-by":"crossref","first-page":"1944","DOI":"10.1093\/brain\/awq119","article-title":"Anti-GD1a antibodies activate complement and calpain to injure distal motor nodes of Ranvier in mice","volume":"133","author":"McGonigal","year":"2010","journal-title":"Brain"},{"key":"10.1016\/j.nbd.2013.03.009_bb0120","doi-asserted-by":"crossref","first-page":"515","DOI":"10.1093\/brain\/awg061","article-title":"Axonal damage: a key predictor of outcome in human CNS diseases","volume":"126","author":"Medana","year":"2003","journal-title":"Brain"},{"key":"10.1016\/j.nbd.2013.03.009_bb0125","doi-asserted-by":"crossref","first-page":"507","DOI":"10.1113\/jphysiol.1970.sp009076","article-title":"On the degeneration of rat neuromuscular junctions after nerve section","volume":"207","author":"Miledi","year":"1970","journal-title":"J. Physiol."},{"key":"10.1016\/j.nbd.2013.03.009_bb0130","doi-asserted-by":"crossref","first-page":"511","DOI":"10.1093\/brain\/awn332","article-title":"Motor axon excitability during Wallerian degeneration","volume":"132","author":"Moldovan","year":"2009","journal-title":"Brain"},{"key":"10.1016\/j.nbd.2013.03.009_bb0135","doi-asserted-by":"crossref","first-page":"231","DOI":"10.1590\/S0001-37652001000200008","article-title":"Watery and dark axons in Wallerian degeneration of the opossum's optic nerve: different patterns of cytoskeletal breakdown?","volume":"73","author":"Narciso","year":"2001","journal-title":"An. Acad. Bras. Cienc."},{"key":"10.1016\/j.nbd.2013.03.009_bb0140","doi-asserted-by":"crossref","first-page":"2497","DOI":"10.1093\/brain\/awg254","article-title":"Calpain inhibitors protect against axonal degeneration in a model of anti-ganglioside antibody-mediated motor nerve terminal injury","volume":"126","author":"O'Hanlon","year":"2003","journal-title":"Brain"},{"key":"10.1016\/j.nbd.2013.03.009_bb0145","first-page":"25","article-title":"Abnormalities of the sciatic nerves of dystrophic mice, with reference to nerve counts and mean area of axons","volume":"22","author":"Okada","year":"1975","journal-title":"Bull. Tokyo Med. Dent. Univ."},{"key":"10.1016\/j.nbd.2013.03.009_bb0150","doi-asserted-by":"crossref","first-page":"70","DOI":"10.1085\/jgp.53.1.70","article-title":"Motor nerve terminals as the site of initial functional changes after denervation","volume":"53","author":"Okamoto","year":"1969","journal-title":"J. Gen. Physiol."},{"key":"10.1016\/j.nbd.2013.03.009_bb0155","doi-asserted-by":"crossref","first-page":"481","DOI":"10.1126\/science.1223899","article-title":"dSarm\/Sarm1 is required for activation of an injury-induced axon death pathway","volume":"337","author":"Osterloh","year":"2012","journal-title":"Science"},{"key":"10.1016\/j.nbd.2013.03.009_bb0160","doi-asserted-by":"crossref","first-page":"610","DOI":"10.1002\/mus.21284","article-title":"Noninvasive model of sciatic nerve conduction in healthy and septic mice: reliability and normative data","volume":"40","author":"Osuchowski","year":"2009","journal-title":"Muscle Nerve"},{"key":"10.1016\/j.nbd.2013.03.009_bb0165","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1016\/j.expneurol.2006.09.012","article-title":"Heavy neurofilament accumulation and \u03b1-spectrin degradation accompany cerebellar white matter functional deficits following forebrain fluid percussion injury","volume":"204","author":"Park","year":"2007","journal-title":"Exp. Neurol."},{"key":"10.1016\/j.nbd.2013.03.009_bb0170","doi-asserted-by":"crossref","first-page":"270","DOI":"10.2174\/156802610790725489","article-title":"Calpains: attractive targets for the development of synthetic inhibitors","volume":"10","author":"Pietsch","year":"2010","journal-title":"Curr. Top. Med. Chem."},{"key":"10.1016\/j.nbd.2013.03.009_bb0175","doi-asserted-by":"crossref","first-page":"3428","DOI":"10.1073\/pnas.93.8.3428","article-title":"Calpain inhibitor AK295 attenuates motor and cognitive deficits following experimental brain injury in the rat","volume":"93","author":"Saatman","year":"1996","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"10.1016\/j.nbd.2013.03.009_bb0180","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1016\/j.nurt.2009.11.002","article-title":"Calpain as a therapeutic target in traumatic brain injury","volume":"7","author":"Saatman","year":"2010","journal-title":"Neurotherapeutics"},{"key":"10.1016\/j.nbd.2013.03.009_bb0185","doi-asserted-by":"crossref","first-page":"174","DOI":"10.1016\/j.pneurobio.2007.07.007","article-title":"Mechanisms of axon degeneration: from development to disease","volume":"83","author":"Saxena","year":"2007","journal-title":"Prog. Neurobiol."},{"key":"10.1016\/j.nbd.2013.03.009_bb0190","doi-asserted-by":"crossref","DOI":"10.1111\/jnc.12144","article-title":"Brain injury-induced proteolysis is reduced in a novel calpastatin-overexpressing transgenic mouse","author":"Schoch","year":"2013","journal-title":"J. Neurochem"},{"key":"10.1016\/j.nbd.2013.03.009_bb0195","doi-asserted-by":"crossref","first-page":"110","DOI":"10.1016\/S1474-4422(02)00042-X","article-title":"Hereditary motor and sensory neuropathies: a biological perspective","volume":"1","author":"Shy","year":"2002","journal-title":"Lancet Neurol."},{"key":"10.1016\/j.nbd.2013.03.009_bb0200","doi-asserted-by":"crossref","first-page":"150","DOI":"10.1016\/S0304-3940(02)00469-X","article-title":"Calpain-dependent neurofilament breakdown in anoxic and ischemic rat central axons","volume":"328","author":"Stys","year":"2002","journal-title":"Neurosci. Lett."},{"key":"10.1016\/j.nbd.2013.03.009_bb0205","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1016\/j.expneurol.2011.12.020","article-title":"Calcium dependence of damage to mouse motor nerve terminals following oxygen\/glucose deprivation","volume":"234","author":"Talbot","year":"2012","journal-title":"Exp. Neurol."},{"key":"10.1016\/j.nbd.2013.03.009_bb0210","doi-asserted-by":"crossref","first-page":"2796","DOI":"10.1172\/JCI34254","article-title":"Inhibition of calpains improves memory and synaptic transmission in a mouse model of Alzheimer disease","volume":"118","author":"Trinchese","year":"2008","journal-title":"J. Clin. Invest."},{"key":"10.1016\/j.nbd.2013.03.009_bb0215","doi-asserted-by":"crossref","first-page":"153","DOI":"10.1146\/annurev.neuro.30.051606.094354","article-title":"Why is Wallerian degeneration in the CNS so slow?","volume":"30","author":"Vargas","year":"2007","journal-title":"Annu. Rev. Neurosci."},{"key":"10.1016\/j.nbd.2013.03.009_bb0220","doi-asserted-by":"crossref","first-page":"423","DOI":"10.1098\/rstl.1850.0021","article-title":"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","volume":"140","author":"Waller","year":"1850","journal-title":"Philos. Trans. R. Soc. London"},{"key":"10.1016\/j.nbd.2013.03.009_bb0230","doi-asserted-by":"crossref","first-page":"599","DOI":"10.1093\/jnen\/59.7.599","article-title":"Pathogenesis of axonal degeneration: parallels between Wallerian degeneration and vincristine neuropathy","volume":"59","author":"Wang","year":"2000","journal-title":"J. Neuropathol. Exp. Neurol."},{"key":"10.1016\/j.nbd.2013.03.009_bb0235","doi-asserted-by":"crossref","first-page":"671","DOI":"10.1093\/brain\/awh078","article-title":"Calpain inhibition protects against taxol-induced sensory neuropathy","volume":"127","author":"Wang","year":"2004","journal-title":"Brain"},{"key":"10.1016\/j.nbd.2013.03.009_bb0225","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1083\/jcb.201108111","article-title":"Axon degeneration: molecular mechanisms of a self-destruction pathway","volume":"196","author":"Wang","year":"2012","journal-title":"J. Cell Biol."},{"key":"10.1016\/j.nbd.2013.03.009_bb0240","doi-asserted-by":"crossref","first-page":"260","DOI":"10.1038\/sj.cdd.4401147","article-title":"The proapoptotic proteins Bax and Bak are not involved in Wallerian degeneration","volume":"10","author":"Whitmore","year":"2003","journal-title":"Cell Death Differ."},{"key":"10.1016\/j.nbd.2013.03.009_bb0245","doi-asserted-by":"crossref","first-page":"2979","DOI":"10.1111\/j.1460-9568.2007.05914.x","article-title":"Induction of autophagy in neurite degeneration of mouse superior cervical ganglion neurons","volume":"26","author":"Yang","year":"2007","journal-title":"Eur. J. Neurosci."},{"key":"10.1016\/j.nbd.2013.03.009_bb0250","doi-asserted-by":"crossref","first-page":"217","DOI":"10.1016\/S0896-6273(03)00429-X","article-title":"Involvement of the ubiquitin\u2013proteasome system in the early stages of Wallerian degeneration","volume":"39","author":"Zhai","year":"2003","journal-title":"Neuron"},{"key":"10.1016\/j.nbd.2013.03.009_bb0255","doi-asserted-by":"crossref","first-page":"3977","DOI":"10.1021\/bi00260a012","article-title":"Characterization of a brain calcium-activated protease that degrades neurofilament proteins","volume":"21","author":"Zimmerman","year":"1982","journal-title":"Biochemistry"}],"container-title":["Neurobiology of Disease"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0969996113000971?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0969996113000971?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"}],"deposited":{"date-parts":[[2019,7,11]],"date-time":"2019-07-11T08:53:35Z","timestamp":1562835215000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S0969996113000971"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2013,8]]},"references-count":51,"alternative-id":["S0969996113000971"],"URL":"https:\/\/doi.org\/10.1016\/j.nbd.2013.03.009","relation":{},"ISSN":["0969-9961"],"issn-type":[{"value":"0969-9961","type":"print"}],"subject":[],"published":{"date-parts":[[2013,8]]},"assertion":[{"value":"Elsevier","name":"publisher","label":"This article is maintained by"},{"value":"Calpains mediate axonal cytoskeleton disintegration during Wallerian degeneration","name":"articletitle","label":"Article Title"},{"value":"Neurobiology of Disease","name":"journaltitle","label":"Journal Title"},{"value":"https:\/\/doi.org\/10.1016\/j.nbd.2013.03.009","name":"articlelink","label":"CrossRef DOI link to publisher maintained version"},{"value":"article","name":"content_type","label":"Content Type"},{"value":"Copyright \u00a9 2013 Elsevier Inc. All rights reserved.","name":"copyright","label":"Copyright"}]}}