Brain injury-induced proteolysis is reduced in a novel calpastatin- overexpressing transgenic mouse

Journal of Neurochemistry

Volumn 125, Issue 6, 2013, Pages 909-920

  Schoch, Kathleen M ^a   Von Reyn, Catherine R ^b,c   Bian, Jifeng ^d   Telling, Glenn C ^d   Meaney, David F ^b   Saatman, Kathryn E ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^d Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

calcium; calpain; CRMP 2; protease; sodium channel; spectrin

Indexed keywords

CALPAIN; CALPAIN 1; CALPAIN 2; CALPASTATIN; CASPASE 3; COLLAPSIN RESPONSE MEDIATOR PROTEIN 2; FODRIN; SODIUM CHANNEL NAV1.2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN HOMOGENATE; BRAIN INJURY; CELL FUNCTION; CELL SURVIVAL; CONTROLLED STUDY; ENZYME INHIBITION; ENZYME SUBSTRATE; FEMALE; GENE OVEREXPRESSION; IN VITRO STUDY; INTRACELLULAR SIGNALING; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; TRANSGENIC MOUSE;

ANIMALS; BRAIN INJURIES; CALCIUM-BINDING PROTEINS; FEMALE; FOUNDER EFFECT; HIPPOCAMPUS; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MICE; MICE, TRANSGENIC; NAV1.2 VOLTAGE-GATED SODIUM CHANNEL; NERVE DEGENERATION; NERVE TISSUE PROTEINS; PRIONS; PROMOTER REGIONS, GENETIC; PROTEOLYSIS; SPECTRIN;

MUS MUSCULUS;

EID: 84878757431     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.12144     Document Type: Article

References (48)

1. Anagli J., Han Y., Stewart L., Yang D., Movsisyan A., Abounit K., and, Seyfried D., (2009) A novel calpastatin-based inhibitor improves postischemic neurological recovery. Biochem. Biophys. Res. Commun. 385, 94-99.
2. Angers R. C., Seward T. S., Napier D., Green M., Hoover E., Spraker T., O'Rourke K., Balachandran A., and, Telling G. C., (2009) Chronic wasting disease prions in elk antler velvet. Emerg. Infect. Dis. 15, 696-703.
3. Barmada S., Piccardo P., Yamaguchi K., Ghetti B., and, Harris D. A., (2004) GFP-tagged prion protein is correctly localized and functionally active in the brains of transgenic mice. Neurobiol. Dis. 16, 527-537.
4. Borchelt D. R., Davis J., Fischer M., et al,. (1996) A vector for expressing foreign genes in the brains and hearts of transgenic mice. Genet. Anal. 13, 159-163.
5. Bretin S., Rogemond V., Marin P., Maus M., Torrens Y., Honnorat J., Glowinski J., Premont J., and, Gauchy C., (2006) Calpain product of WT-CRMP2 reduces the amount of surface NR2B NMDA receptor subunit. J. Neurochem. 98, 1252-1265.
6. Brittain J. M., Piekarz A. D., Wang Y., Kondo T., Cummins T. R., and, Khanna R., (2009) An atypical role for collapsin response mediator protein 2 (CRMP-2) in neurotransmitter release via interaction with presynaptic voltage-gated calcium channels. J. Biol. Chem. 284, 31375-31390.
7. Brittain J. M., Chen L., Wilson S. M., et al,. (2011) Neuroprotection against traumatic brain injury by a peptide derived from the collapsin response mediator protein 2 (CRMP2). J. Biol. Chem. 286, 37778-37792.
8. Camins A., Verdaguer E., Folch J., and, Pallas M., (2006) Involvement of calpain activation in neurodegenerative processes. CNS Drug Rev. 12, 135-148.
9. Carragher N. O., (2006) Calpain inhibition: a therapeutic strategy targeting multiple disease states. Curr. Pharm. Des. 12, 615-638.
10. Deng Y., Thompson B. M., Gao X., and, Hall E. D., (2007) Temporal relationship of peroxynitrite-induced oxidative damage, calpain-mediated cytoskeletal degradation and neurodegeneration after traumatic brain injury. Exp. Neurol. 205, 154-165.
11. Fukata Y., Itoh T. J., Kimura T., et al,. (2002) CRMP-2 binds to tubulin heterodimers to promote microtubule assembly. Nat. Cell Biol. 4, 583-591.
12. Goll D. E., Thompson V. F., Li H., Wei W., and, Cong J., (2003) The calpain system. Physiol. Rev. 83, 731-801.
13. Higuchi M., Tomioka M., Takano J., Shirotani K., Iwata N., Masumoto H., Maki M., Itohara S., and, Saido T. C., (2005) Distinct mechanistic roles of calpain and caspase activation in neurodegeneration as revealed in mice overexpressing their specific inhibitors. J. Biol. Chem. 280, 15229-15237.
14. Institute of Laboratory Animal Resources (US). 2011 Committee on Care and Use of Laboratory Animals. Guide for the care and use of laboratory animals. NIH publication, p v. U.S. Dept. of Health and Human Services, Public Health Service, Bethesda, Md.
15. Iwata A., Stys P. K., Wolf J. A., Chen X. H., Taylor A. G., Meaney D. F., and, Smith D. H., (2004) Traumatic axonal injury induces proteolytic cleavage of the voltage-gated sodium channels modulated by tetrodotoxin and protease inhibitors. J. Neurosci. 24, 4605-4613.
16. Kampfl A., Posmantur R., Nixon R., Grynspan F., Zhao X., Liu S. J., Newcomb J. K., Clifton G. L., and, Hayes R. L., (1996) mu-calpain activation and calpain-mediated cytoskeletal proteolysis following traumatic brain injury. J. Neurochem. 67, 1575-1583.
17. Kupina N. C., Nath R., Bernath E. E., Inoue J., Mitsuyoshi A., Yuen P. W., Wang K. K., and, Hall E. D., (2001) The novel calpain inhibitor SJA6017 improves functional outcome after delayed administration in a mouse model of diffuse brain injury. J. Neurotrauma 18, 1229-1240.
18. Li A., Christensen H. M., Stewart L. R., Roth K. A., Chiesa R., and, Harris D. A., (2007) Neonatal lethality in transgenic mice expressing prion protein with a deletion of residues 105-125. EMBO J. 26, 548-558.
19. Maki M., Takano E., Mori H., Sato A., Murachi T., and, Hatanaka M., (1987) All four internally repetitive domains of pig calpastatin possess inhibitory activities against calpains I and II. FEBS Lett. 223, 174-180.
20. McCollum A. T., Jafarifar F., Lynn B. C., Agu R. U., Stinchcomb A. L., Wang S., Chen Q., and, Guttmann R. P., (2006) Inhibition of calpain-mediated cell death by a novel peptide inhibitor. Exp. Neurol. 202, 506-513.
21. Moldoveanu T., Gehring K., and, Green D. R., (2008) Concerted multi-pronged attack by calpastatin to occlude the catalytic cleft of heterodimeric calpains. Nature 456, 404-408.
22. Mondello S., Robicsek S. A., Gabrielli A., et al,. (2010) alphaII-spectrin breakdown products (SBDPs): diagnosis and outcome in severe traumatic brain injury patients. J. Neurotrauma 27, 1203-1213.
23. Paxinos G., and, Franklin K. B. J., (2001) The mouse brain in stereotaxic coordinates. Academic Press, San Diego.
24. Pike B. R., Zhao X., Newcomb J. K., Posmantur R. M., Wang K. K., and, Hayes R. L., (1998) Regional calpain and caspase-3 proteolysis of alpha-spectrin after traumatic brain injury. NeuroReport 9, 2437-2442.
25. Pike B. R., Flint J., Dutta S., Johnson E., Wang K. K., and, Hayes R. L., (2001) Accumulation of non-erythroid alpha II-spectrin and calpain-cleaved alpha II-spectrin breakdown products in cerebrospinal fluid after traumatic brain injury in rats. J. Neurochem. 78, 1297-1306.
26. Pleasant J. M., Carlson S. W., Mao H., Scheff S. W., Yang K. H., and, Saatman K. E., (2011) Rate of neurodegeneration in the mouse controlled cortical impact model is influenced by impactor tip shape: implications for mechanistic and therapeutic studies. J. Neurotrauma 28, 2245-2262.
27. Posmantur R., Kampfl A., Siman R., Liu J., Zhao X., Clifton G. L., and, Hayes R. L., (1997) A calpain inhibitor attenuates cortical cytoskeletal protein loss after experimental traumatic brain injury in the rat. Neuroscience 77, 875-888.
28. Quinn C. C., Gray G. E., and, Hockfield S., (1999) A family of proteins implicated in axon guidance and outgrowth. J. Neurobiol. 41, 158-164.
29. Quinn C. C., Chen E., Kinjo T. G., Kelly G., Bell A. W., Elliott R. C., McPherson P. S., and, Hockfield S., (2003) TUC-4b, a novel TUC family variant, regulates neurite outgrowth and associates with vesicles in the growth cone. J. Neurosci. 23, 2815-2823.
30. Rahajeng J., Giridharan S. S., Naslavsky N., and, Caplan S., (2010) Collapsin response mediator protein-2 (Crmp2) regulates trafficking by linking endocytic regulatory proteins to dynein motors. J. Biol. Chem. 285, 31918-31922.
31. Rao M. V., Mohan P. S., Peterhoff C. M., et al,. (2008) Marked calpastatin (CAST) depletion in Alzheimer's disease accelerates cytoskeleton disruption and neurodegeneration: neuroprotection by CAST overexpression. J. Neurosci. 28, 12241-12254.
32. von Reyn C. R., Spaethling J. M., Mesfin M. N., Ma M., Neumar R. W., Smith D. H., Siman R., and, Meaney D. F., (2009) Calpain mediates proteolysis of the voltage-gated sodium channel alpha-subunit. J. Neurosci. 29, 10350-10356.
33. von Reyn C. R., Mott R. E., Siman R., Smith D. H., and, Meaney D. F., (2012) Mechanisms of calpain mediated proteolysis of voltage gated sodium channel alpha-subunits following in vitro dynamic stretch injury. J. Neurochem. 121, 793-805.
34. Ringger N. C., O'Steen B. E., Brabham J. G., Silver X., Pineda J., Wang K. K., Hayes R. L., and, Papa L., (2004) A novel marker for traumatic brain injury: CSF alphaII-spectrin breakdown product levels. J. Neurotrauma 21, 1443-1456.
35. Saatman K. E., Bozyczko-Coyne D., Marcy V., Siman R., and, McIntosh T. K., (1996) Prolonged calpain-mediated spectrin breakdown occurs regionally following experimental brain injury in the rat. J. Neuropathol. Exp. Neurol. 55, 850-860.
36. Saatman K. E., Zhang C., Bartus R. T., and, McIntosh T. K., (2000) Behavioral efficacy of posttraumatic calpain inhibition is not accompanied by reduced spectrin proteolysis, cortical lesion, or apoptosis. J. Cereb. Blood Flow Metab. 20, 66-73.
37. Saatman K. E., Creed J., and, Raghupathi R., (2010) Calpain as a therapeutic target in traumatic brain injury. Neurotherapeutics 7, 31-42.
38. Sato K., Minegishi S., Takano J., Plattner F., Saito T., Asada A., Kawahara H., Iwata N., Saido T. C., and, Hisanaga S., (2011) Calpastatin, an endogenous calpain-inhibitor protein, regulates the cleavage of the Cdk5 activator p35 to p25. J. Neurochem. 117, 504-515.
39. Schoch K. M., Evans H. N., Brelsfoard J. M., Madathil S. K., Takano J., Saido T. C., and, Saatman K. E., (2012) Calpastatin overexpression limits calpain-mediated proteolysis and behavioral deficits following traumatic brain injury. Exp. Neurol. 236, 371-382.
40. Sorimachi H., Hata S., and, Ono Y., (2011) Calpain chronicle-an enzyme family under multidisciplinary characterization. Proc. Jpn. Acad., Ser. B, Phys. Biol. Sci. 87, 287-327.
41. Taghian K., Lee J. Y., and, Petratos S., (2012) Phosphorylation and cleavage of the family of collapsin response mediator proteins may play a central role in neurodegeneration after CNS trauma. J. Neurotrauma 29, 1728-1735.
42. Thompson S. N., Carrico K. M., Mustafa A. G., Bains M., and, Hall E. D., (2010) A pharmacological analysis of the neuroprotective efficacy of the brain- and cell-permeable calpain inhibitor MDL-28170 in the mouse controlled cortical impact traumatic brain injury model. J. Neurotrauma 27, 2233-2243.
43. Touma E., Kato S., Fukui K., and, Koike T., (2007) Calpain-mediated cleavage of collapsin response mediator protein(CRMP)-2 during neurite degeneration in mice. Eur. J. Neurosci. 26, 3368-3381.
44. Westenbroek R. E., Merrick D. K., and, Catterall W. A., (1989) Differential subcellular localization of the RI and RII Na+ channel subtypes in central neurons. Neuron 3, 695-704.
45. Wilson S. M., Xiong W., Wang Y., Ping X., Head J. D., Brittain J. M., Gagare P. D., Ramachandran P. V., Jin X., and, Khanna R., (2012) Prevention of posttraumatic axon sprouting by blocking collapsin response mediator protein 2-mediated neurite outgrowth and tubulin polymerization. Neuroscience 210, 451-466.
46. Yuen T. J., Browne K. D., Iwata A., and, Smith D. H., (2009) Sodium channelopathy induced by mild axonal trauma worsens outcome after a repeat injury. J. Neurosci. Res. 87, 3620-3625.
47. Zhang Z., Ottens A. K., Sadasivan S., Kobeissy F. H., Fang T., Hayes R. L., and, Wang K. K., (2007) Calpain-mediated collapsin response mediator protein-1, -2, and -4 proteolysis after neurotoxic and traumatic brain injury. J. Neurotrauma 24, 460-472.
48. Zhang Z., Larner S. F., Liu M. C., Zheng W., Hayes R. L., and, Wang K. K., (2009) Multiple alphaII-spectrin breakdown products distinguish calpain and caspase dominated necrotic and apoptotic cell death pathways. Apoptosis 14, 1289-1298.