Postischemic reperfusion induces α-fodrin proteolysis by m-calpain in the synaptosome and nucleus in rat brain

Journal of Neurochemistry

Volumn 70, Issue 6, 1998, Pages 2526-2532

  Fukuda, Shiro ^a   Harada, Kazuki ^a   Kunimatsu, Mitoshi ^b   Sakabe, Takefumi ^a   Yoshida, Ken Ichi ^a,c  

^a YAMAGUCHI UNIVERSITY   (Japan)

^b NAGOYA CITY UNIV MEDICAL SCHOOL   (Japan)

^c YAMAGUCHI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Calpain; Fodrin; Ischemia; Rat brain; Reperfusion

Indexed keywords

ACETYLLEUCYLLEUCYLNORLEUCINAL; ALPHA FODRIN; CALCIUM ION; CALPAIN; CALPASTATIN; FODRIN; M CALPAIN; MU CALPAIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN ISCHEMIA; CALCIUM TRANSPORT; CELL FRACTIONATION; CONTROLLED STUDY; ENZYME BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; RAT; REPERFUSION;

ANIMALIA;

EID: 0031776915     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.1998.70062526.x     Document Type: Article

References (52)

1. Bartus R. T., Baker K. L., Heiser A. D., Sawyer S. D., Dean R. L., Elliott P. J., and Straub J. A. (1994a) Postischemic administration of AK275, a calpain inhibitor, provides substantial protection against focal ischemic brain damage. J. Cereb. Blood Flow Metab. 14, 537-544.
2. 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., and Powers J. (1994b) Calpain inhibitor AK295 protects neurons from focal ischemic brain ischemia. Stroke 25, 2265-2270.
3. Bennett V. and Lambert S. (1991) The spectrin skeleton: from red cells to brain. J. Clin. Invest. 87, 1483-1489.
4. Bradford M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
5. Burgoyne R. D. and Cheek T. R. (1987) Role of fodrin in secretion. Nature 326, 448.
6. DeMartino G. N., Huff C. A., and Croall D. E. (1986) Autoproteolysis of the small subunit of calcium-dependent protease 11 activates and regulates protease activity. J. Biol. Chem. 261, 12047-12052.
7. Dietrich W. D., Halley M., Valdes I., and Busto R. (1991) Interrelationships between increased vascular permeability and acute neuronal damage following temperature-controlled brain ischemia in rats. Acta Neuropathol. (Berl.) 81, 615-625.
8. Dunkley P. B., Jarvie P. E., Heath J. W., Kidd G. J., and Rostas J. A. P. (1986) A rapid method for isolation of synaptosomes on Percoll gradients. Brain Res. 372, 115-129.
9. Elvira M., Díez J. A., Wang K. K. W., and Villalobo A. (1993) Phosphorylation of connexin-32 by protein kinase C prevents its proteolysis by μ-calpain and m-calpain. J. Biol. Chem. 268, 14294-14300.
10. Fagnou D. D. and Tuchek J. M. (1995) The biochemistry of learning and memory. Mol. Cell. Biochem. 149/150, 279-286.
11. Gray E. G. and Whittaker V. P. (1962) The isolation of nerve endings from brain: an electron-microscopic study of cell fragments derived by homogenization and centrifugation. J. Anal. 96, 79-88.
12. Harada K., Fukuda S., Kunimoto M., and Yoshida K. (1997) Distribution of ankyrin isoforms and their proteolysis after ischemia and reperfusion in rat brain. J. Neurochem. 69, 371-376.
13. Hong S.-C., Goto Y., Lanzino G., Soleau S., Kassel N. F., and Lee K. S. (1994) Neuroprotection with a calpain inhibitor in a model of focal cerebral ischemia. Stroke 25, 663-669.
14. Iga M., Inui M., and Sobue K. (1997) Characterization of the interaction between synapsin I and calspectin (brain spectrin or fodrin). Biochem. Biophys. Res. Commun. 231, 852-855.
15. Inuzuka T., Tamura A., Sato S., Kirino T., Toyoshima I., and Miyatake T. (1990) Suppressive effect of E-64c on ischemic degradation of cerebral proteins following occlusion of the middle cerebral artery in rats. Brain Res. 526, 177-179.
16. Kawashima S., Hayashi M., Saito Y., Kasai Y., and Imahori K. (1988) Tissue distribution of calcium-activated neutral protein-ases in rat. Biochim. Biophys. Acta 965, 130-135.
17. Laemmli U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
18. Lee K. S., Frank S., Vanderklish P., Arai A., and Lynch G. (1991) Inhibition of proteolysis protects hippocampal neurons from ischemia. Proc. Natl. Acad. Sci. USA 88, 7233-7237.
19. Lowry O. H., Rosebrough N. J., Farr A. L., and Randall R. J. (1951) Protein measurement with the Polin phenol reagent. J. Biol. Chem. 193, 265-275.
20. Mellgren R. L., Song K., and Mericle M. T. (1993) m-Calpain requires DNA for activity on nuclear proteins at low calcium concentrations. J. Biol. Chem. 268, 653-657.
21. Mizukami Y. and Yoshida K. (1997) Mitogen-activated protein kinase translocates to the nucleus during ischaemia and is activated during reperfusion. Biochem. J. 323, 785-790.
22. Mizukami Y., Hirata T., and Yoshida K. (1997a) Nuclear translocation of PKCξ during ischemia and its inhibition by wortmannin, an inhibitor of phosphatidylinositol 3-kinase. FEBS Lett. 401, 247-251.
23. Mizukami Y., Yoshioka K., Morimoto S., and Yoshida K. (1997b) A novel mechanism of JNK1 activation: nuclear translocation and activation of JNK1 during ischemia and reperfusion. J. Biol. Chem. 272, 16657-16662.
24. Moon R. T. and McMahon A. P. (1987) Composition and expression of spectrin-based membrane skeletons in non-erythroid cell. Bioessays 7, 159-164.
25. 1-adrenergic stimulation and reperfusion of ischaemic rat heart. J. Mol. Cell Cardiol. 23, 841-850.
26. Neumar R. W., DeGracia D. J., White B. C., McDermott P. J., Evans D. R., and Krause G. S. (1995) Eukaryotic initiation factor 4E degradation during brain ischemia. J. Neurochem. 65, 1391-1394.
27. +) ATPase and implications for the organization of membrane domains in polarized cells. Nature 328, 533-536.
28. Pontén U., Ratcheson R. A., Salford L. G., and Siesjö B. K. (1973) Optimal freezing conditions for cerebral metabolites in rats. J. Neurochem. 21, 1127-1138.
29. Rami A. and Krieglstein J. (1993) Protective effects of calpain inhibitors against neuronal damage caused by cytotoxic hypoxia in vitro and ischemia in vivo. Brain Res. 609, 67-70.
30. Raser K. J., Posner A., and Wang K. K. W. (1995) Casein zymography: a method of study of μ-calpain, m-calpain, and their inhibitory agents. Arch. Biochem. Biophys. 319, 211-216.
31. Riederer B. M., Zagon I. S., and Goodman S. R. (1986) Brain spectrin (240/235) and brain spectrin (240/235E): two distinct spectrin subtypes with different locations within mammalian neural cells. J. Cell Biol. 102, 2088-2097.
32. Saido T. C., Shibata M., Takenawa T., Murofushi H., and Suzuki K. (1992) Positive regulation of μ-calpain action by polyphosphoinositides. J. Biol. Chem. 267, 24585-24590.
33. Saido T. C., Yokota M., Nagano S., Yamamura I., Tani E., Tsuchiya T., Suzuki K., and Kawashima S. (1993) Spatial resolution of fodrin proteolysis in postischemic brain. J. Biol. Chem. 268, 25239-25243.
34. Saido T. C., Sorimachi H., and Suzuki K. (1994) Calpain: new perspectives in molecular diversity and physiological-pathological involvement. FASEB J. 8, 814-822.
35. Salamino F., Tullio R. D., Michetti M., Mengotti P., Melloni E., and Pontremoli S. (1994) Modulation of calpastatin specificity in rat tissues by reversible phosphorylation and dephosphorylation. Biochem. Biophys. Res. Commun. 199, 1326-1332.
36. Sano T., Patel P. M., Drummond J. C., and Cole D. J. (1993) A comparison of the cerebral protective effects of etomidate, thiopental, and isoflurane in a model of forebrain ischemia in the rat. Anesth. Analg. 76, 990-997.
37. Seubert P. and Lynch G. (1990) Plasticity to pathology: brain calpains as modifiers of synaptic structure, in Intracellular Calcium-Dependent Proteolysis (Mellgren R. L. and Murachi T., eds), pp. 251-263. CRC Press, Boca Raton, Florida.
38. 2+/calmodulin-dependent protein kinase II following spinal cord ischemia. J. Neurochem. 61, 738-747.
39. Shiba E., Ariyoshi H., Yano Y., Kawasaki T., Sakon M., Kambayashi J., and Mori T. (1992) Purification and characterization of a calpain activator from human platelets. Biochem. Biophys. Res. Commun. 182, 461-465.
40. Siesjö B. K., Zhao Q., Pahlmark K., Siesjö P., Katsura K., and Folbergrová J. (1995) Glutamate, calcium, and free radicals as mediators of ischemic brain damage. Ann. Thorac. Surg. 59, 1316-1320.
41. Smith M.-L., Bendek G., Dahlgren N., Rosén I., Wieloch T., and Siesjö B. K. (1984) Models for studying long-term recovery following forebrain ischemia in the rat. 2. A 2-vessel occlusion model. Acta Neurol. Scand. 69, 385-401.
42. Sorimachi Y., Harada K., and Yoshida K. (1996) Involvement of calpain in postmortem proteolysis in the rat brain. Forensic Sci. Int. 81, 165-174.
43. Sorimachi Y., Harada K., Saido T. C., Ono T., Kawashima S., and Yoshida K. (1997) Downregulation of calpastatin in rat heart after brief ischemia and reperfusion. J. Biochem. (Tokyo) 122, 743-748.
44. Takeuchi K. H., Saito K.-I., and Nixon R. A. (1992) Immunoassay and activity of calcium-activated neutral proteinase (mCANP): distribution in soluble and membrane-associated fractions in human and mouse brain. J. Neurochem. 58, 1526-1532.
45. Towbin H., Staehelin T., and Gordon J. (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA 76, 4350-4354.
46. Wang K. K. W. and Yuen P.-W. (1994) Calpain inhibition: an overview of its therapeutic potential. Trends Pharmacol. Sci. 15, 412-419.
47. Wieloch T., Cardell M., Bingren H., Zivin J., and Saitoh T. (1991) Changes in the activity of protein kinase C and the differential subcellular redistribution of its isozymes in the rat striatum during and following transient forebrain ischemia. J. Neurochem. 56, 1227-1235.
48. Yoshida K., Yamasaki Y., and Kawashima S. (1993) Calpain activity alters in rat myocardial subfractions after ischemia and reperfusion. Biochim. Biophys. Acta 1182, 215-220.
49. Yoshida K., Sorimachi Y., Fujiwara M., and Hironaka K. (1995a) Calpain is implicated in rat myocardial injury after ischemia or reperfusion. Jpn. Circ. J. 59, 40-48.
50. Yoshida K., Inui M., Harada K., Saido T. C., Sorimachi Y., Ishihara T., Kawashima S., and Sobue K. (1995b) Reperfusion of rat heart after brief ischemia induces proteolysis of calspectin (non-erythroid spectrin or fodrin) by calpain. Circ. Res. 77, 603-610.
51. Yoshida K., Hirata T., Akita Y., Mizukami Y., Yamaguchi K., Sorimachi Y., Ishihara T., and Kawashima S. (1996) Translocation of protein kinase C-α, δ and ∈ isoforms in ischemie rat heart. Biochim. Biophys. Acta 1317, 36-44.
52. Yoshizawa T., Sorimachi H., Tomioka S., Ishiura S., and Suzuki K. (1995) Calpain dissociates into subunits in the presence of calcium ions. Biochem. Biophys. Res. Commun. 208, 376-383.