RNAi targeting μ-calpain increases neuron survival and preserves hippocampal function after global brain ischemia

Experimental Neurology

Volumn 224, Issue 1, 2010, Pages 170-177

  Bevers, Matthew B ^a   Ingleton, Lori P ^a   Che, Dongfang ^a   Cole, Jeffrey T ^a   Li, Luchuan ^a   Da, Tong ^a   Kopil, Catherine M ^a   Cohen, Akiva S ^a   Neumar, Robert W ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Adeno associated virus; Calpain; Hippocampus; Ischemia; RNA interference

Indexed keywords

CALPAIN; CALPAIN 1; CALPAIN 2; CYSTEINE PROTEINASE; PARVOVIRUS VECTOR; SHORT HAIRPIN RNA; ISOPROTEIN; SMALL INTERFERING RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; BRAIN FUNCTION; BRAIN INJURY; BRAIN ISCHEMIA; BRAIN PROTECTION; CELL DEATH; CELL SURVIVAL; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; FOREBRAIN; GENE EXPRESSION; GENE TARGETING; HIPPOCAMPUS; IN VIVO STUDY; NERVE CELL; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN FUNCTION; PYRAMIDAL NERVE CELL; RAT; RNA INTERFERENCE; SURVIVAL TIME; VIRAL GENE DELIVERY SYSTEM; ADENO ASSOCIATED VIRUS; ANALYSIS OF VARIANCE; ANIMAL; CELL CULTURE; CYTOLOGY; ELECTROPHYSIOLOGY; FLUORESCENT ANTIBODY TECHNIQUE; GENE VECTOR; GENETICS; MALE; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANALYSIS OF VARIANCE; ANIMALS; BRAIN ISCHEMIA; CALPAIN; CELL SURVIVAL; CELLS, CULTURED; DEPENDOVIRUS; ELECTROPHYSIOLOGY; FLUORESCENT ANTIBODY TECHNIQUE; GENETIC VECTORS; HIPPOCAMPUS; MALE; NEURONS; PROTEIN ISOFORMS; RATS; RNA INTERFERENCE; RNA, SMALL INTERFERING;

EID: 77953719968     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2010.03.007     Document Type: Article

References (42)

1. Azam M., Andrabi S.S., Sahr K.E., Kamath L., Kuliopulos A., Chishti A.H. Disruption of the mouse mu-calpain gene reveals an essential role in platelet function. Mol. Cell. Biol. 2001, 21:2213-2220.
2. Bano D., Young K.W., Guerin C.J., Lefeuvre R., Rothwell N.J., Naldini L., Rizzuto R., Carafoli E., Nicotera P. Cleavage of the plasma membrane Na+/Ca2+ exchanger in excitotoxicity. Cell 2005, 120:275-285.
3. Bartus R.T., Baker K.L., Heiser A.D., Sawyer S.D., Dean R.L., Elliott P.J., Straub J.A. Postischemic administration of AK275, a calpain inhibitor, provides substantial protection against focal ischemic brain damage. J. Cereb. Blood Flow Metab. 1994, 14:537-544.
4. Bartus R.T., Hayward N.J., Elliott P.J., Sawyer S.D., Baker K.L., Dean R.L., Akiyama A., Straub J.A., Harbeson S.L., Li Z. Calpain inhibitor AK295 protects neurons from focal brain ischemia. Effects of postocclusion intra-arterial administration. Stroke 1994, 25:2265-2270.
5. Bartus R.T., Dean R.L., Cavanaugh K., Eveleth D., Carriero D.L., Lynch G. Time-related neuronal changes following middle cerebral artery occlusion: implications for therapeutic intervention and the role of calpain. J. Cereb. Blood Flow Metab. 1995, 15:969-979.
6. Bartus R.T., Dean R.L., Mennerick S., Eveleth D., Lynch G. Temporal ordering of pathogenic events following transient global ischemia. Brain Res. 1998, 790:1-13.
7. Bevers M.B., Neumar R.W. Mechanistic role of calpains in postischemic neurodegeneration. J. Cereb. Blood Flow Metab. 2008, 28:655-673.
8. Bevers M.B., Lawrence E., Maronski M., Starr N., Amesquita M., Neumar R.W. Knockdown of m-calpain increases survival of primary hippocampal neurons following NMDA excitotoxicity. J. Neurochem. 2008, 108:1237-1250.
9. Cao G., Xing J., Xiao X., Liou A.K., Gao Y., Yin X.M., Clark R.S., Graham S.H., Chen J. Critical role of calpain I in mitochondrial release of apoptosis-inducing factor in ischemic neuronal injury. J. Neurosci. 2007, 27:9278-9293.
10. Colbourne F., Sutherland G.R., Auer R.N. An automated system for regulating brain temperature in awake and freely moving rodents. J. Neurosci. Methods 1996, 67:185-190.
11. D'Cruz B.J., Fertig K.C., Filiano A.J., Hicks S.D., DeFranco D.B., Callaway C.W. Hypothermic reperfusion after cardiac arrest augments brain-derived neurotrophic factor activation. J. Cereb. Blood Flow Metab. 2002, 22(7):843-851.
12. Dutt P., Croall D.E., Arthur S.C., De Veyra T., Williams K., Elce J.S., Greer P.A. m-Calpain is required for preimplantation embryonic development in mice. BMC Dev. Biol. 2006, 6:3.
13. Fisher K.J., Jooss K., Alston J., Yang Y., Haecker S.E., High K., Pathak R., Raper S.E., Wilson J.M. Recombinant adeno-associated virus for muscle directed gene therapy. Nat. Med. 1997, 3:306-312.
14. Frederick J.R., Chen Z., Bevers M.B., Ingleton L.P., Ma M., Neumar R.W. Neuroprotection with delayed calpain inhibition after transient forebrain ischemia. Crit. Care Med. 2008, 36:S481-S485.
15. Garcia M., Bondada V., Geddes J.W. Mitochondrial localization of mu-calpain. Biochem. Biophys. Res. Commun. 2005, 338:1241-1247.
16. Goll D.E., Thompson V.F., Li H., Wei W., Cong J. The calpain system. Physiol. Rev. 2003, 83:731-801.
17. Hicks S.D., DeFranco D.B., Callaway C.W. Hypothermia during reperfusion after asphyxial cardiac arrest improves functional recovery and selectively alters stress-induced protein expression. J. Cereb. Blood Flow Metab. 2000, 20:520-530.
18. Honda S., Marumoto T., Hirota T., Nitta M., Arima Y., Ogawa M., Saya H. Activation of m-calpain is required for chromosome alignment on the metaphase plate during mitosis. J. Biol. Chem. 2004, 279:10615-10623.
19. Hong S.C., Lanzino G., Goto Y., Kang S.K., Schottler F., Kassell N.F., Lee K.S. Calcium-activated proteolysis in rat neocortex induced by transient focal ischemia. Brain Res. 1994, 661:43-50.
20. Hou S.T., Jiang S.X., Desbois A., Huang D., Kelly J., Tessier L., Karchewski L., Kappler J. Calpain-cleaved collapsin response mediator protein-3 induces neuronal death after glutamate toxicity and cerebral ischemia. J. Neurosci. 2006, 26:2241-2249.
21. Jiang S.X., Kappler J., Zurakowski B., Desbois A., Aylsworth A., Hou S.T. Calpain cleavage of collapsin response mediator proteins in ischemic mouse brain. Eur. J. Neurosci. 2007, 26:801-809.
22. Joshi A., Bondada V., Geddes J.W. Mitochondrial mu-calpain is not involved in the processing of apoptosis-inducing factor. Exp Neuro. 2009, 218(2):221-227.
23. Lee K.S., Frank S., Vanderklish P., Arai A., Lynch G. Inhibition of proteolysis protects hippocampal neurons from ischemia. Proc. Natl. Acad. Sci. U. S. A. 1991, 88:7233-7237.
24. Li P.A., Howlett W., He Q.P., Miyashita H., Siddiqui M., Shuaib A. Postischemic treatment with calpain inhibitor MDL 28170 ameliorates brain damage in a gerbil model of global ischemia. Neurosci. Lett. 1998, 247:17-20.
25. Li Y., Bondada V., Joshi A., Geddes J. Calpain 1 and Calpastatin expression is developmentally regulated in rat brain. Exp. Neurol. 2009, 220(2):316-319. Online.
26. Markgraf C.G., Velayo N.L., Johnson M.P., McCarty D.R., Medhi S., Koehl J.R., Chmielewski P.A., Linnik M.D. Six-hour window of opportunity for calpain inhibition in focal cerebral ischemia in rats. Stroke 1998, 29:152-158.
27. Neumar R.W., Hagle S.M., DeGracia D.J., Krause G.S., White B.C. Brain mu-calpain autolysis during global cerebral ischemia. J. Neurochem. 1996, 66:421-424.
28. Neumar R.W., Meng F.H., Mills A.M., Xu Y.A., Zhang C., Welsh F.A., Siman R. Calpain activity in the rat brain after transient forebrain ischemia. Exp. Neurol. 2001, 170:27-35.
29. O'Hare M.J., Kushwaha N., Zhang Y., Aleyasin H., Callaghan S.M., Slack R.S., Albert P.R., Vincent I., Park D.S. Differential roles of nuclear and cytoplasmic cyclin-dependent kinase 5 in apoptotic and excitotoxic neuronal death. J. Neurosci. 2005, 25:8954-8966.
30. Polster B.M., Basañez G., Etxebarria A., Hardwick J.M., Nicholls D.G. Calpain I induces cleavage and release of apoptosis-inducing factor from isolated mitochondria. J. Biol. Chem. 2005, 280:6447-6454.
31. Rami A., Krieglstein J. Protective effects of calpain inhibitors against neuronal damage caused by cytotoxic hypoxia in vitro and ischemia in vivo. Brain Res. 1993, 609:67-70.
32. Roberts-Lewis J.M., Savage M.J., Marcy V.R., Pinsker L.R., Siman R. Immunolocalization of calpain I-mediated spectrin degradation to vulnerable neurons in the ischemic gerbil brain. J. Neurosci. 1994, 14:3934-3944.
33. Saido T.C., Yokota M., Nagao S., Yamaura I., Tani E., Tsuchiya T., Suzuki K., Kawashima S. Spatial resolution of fodrin proteolysis in postischemic brain. J. Biol. Chem. 1993, 268:25239-25243.
34. Saito T., Konno T., Hosokawa T., Asada A., Ishiguro K., Hisanaga S.I. p25/Cyclin-dependent kinase 5 promotes the progression of cell death in nucleus of endoplasmic reticulum-stressed neurons. J. Neurochem. 2007, 102:133-140.
35. Takano E., Masatoshi M., Yuen P. Structure of calpastatin and its inhibitory control of calpain. Calpain: Pharmacology and Toxicology of Calcium-Dependent Protease 1999, 25-50. Taylor &Francis, Philadelphia, PA. K.K.W. Wang (Ed.).
36. Wang Y., White M.G., Akay C., et al. Activation of cyclin-dependent kinase 5 by calpains contributes to human immunodeficiency virus-induced neurotoxicity. J. Neurochem. 2007, 103:439-455.
37. Wang, Y., Kim, N.S., Li, X., Greer, P.A., Koehler, R.C., Dawson, V.L., Dawson, T.M., 2009. Calpain activation is not required for AIF translocation in PARP-1-dependent cell death (Parthanatos). J. Neurochem. Published online June 2009.
38. Wu H.Y., Tomizawa K., Oda Y., Wei F.Y., Lu Y.F., Matsushita M., Li S.T., Moriwaki A., Matsui H. Critical role of calpain-mediated cleavage of calcineurin in excitotoxic neurodegeneration. J. Biol. Chem. 2004, 279:4929-4940.
39. Xu W., Wong T.P., Chery N., Gaertner T., Wang Y.T., Baudry M. Calpain-mediated mGluR1alpha truncation: a key step in excitotoxicity. Neuron 2007, 53:399-412.
40. Yamashima T., Saido T.C., Takita M., et al. Transient brain ischaemia provokes Ca2+, PIP2 and calpain responses prior to delayed neuronal death in monkeys. Eur. J. Neurosci. 1996, 8:1932-1944.
41. Yokota M., Tani E., Tsubuki S., Yamaura I., Nakagaki I., Hori S., Saido T.C. Calpain inhibitor entrapped in liposome rescues ischemic neuronal damage. Brain Res. 1999, 819:8-14.
42. Zhang Z., Ottens A.K., Sadasivan S., Kobeissy F.H., Fang T., Hayes R.L., Wang K.K. Calpain-mediated collapsin response mediator protein-1, -2, and -4 proteolysis after neurotoxic and traumatic brain injury. J. Neurotrauma 2007, 24:460-472.