Immunohistochemical study of calpain-mediated breakdown products to α- spectrin following controlled cortical impact injury in the rat

Journal of Neurotrauma

Volumn 14, Issue 6, 1997, Pages 369-383

  Newcomb, Jennifer K ^a   Kampfl, Andreas ^a,b   Posmantur, Rand M ^a,c   Zhao, Xiurong ^a   Pike, Brian R ^a   Liu, Shi Jie ^a   Clifton, Guy L ^a   Hayes, Ronald L ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF INNSBRUCK   (Austria)

^c PFIZER INC   (United States)

Author keywords

Calpain; Cytoskeleton; Immunohistochemistry; Traumatic brain injury; spectrin

Indexed keywords

CALPAIN; FODRIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CONTUSION; BRAIN CORTEX; BRAIN INJURY; CONTROLLED STUDY; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MALE; NERVE CELL NECROSIS; NONHUMAN; RAT;

EID: 0030872701     PISSN: 08977151     EISSN: None     Source Type: Journal    
DOI: 10.1089/neu.1997.14.369     Document Type: Article

References (82)

1. 2+-mediated degredation of central nervous system (CNS) proteins: Topograhpic and species variation. Metab. Brain Dis. 2, 117-126.
2. BANIK, N.L., HOGAN, E.L., POWERS, J.M., and WHETSTINE, L.J. (1982). Degradation of neurofilaments in spinal cord injury. Neurochem. Res. 7, 1465-1475.
3. BARTUS, R.T., DEAN, R.L., CAVANAUGH, K., EVELETH, D., CARRIERO, D.L., and LYNCH, G. (1995). Time related neuronal changes following middle cerebral artery occlusion: implications for therapeutic intervention and the role of calpain. J. Cereb. Blood Flow Metab. 15, 969-979.
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., and POWERS, J. (1994). Calpain inhibitor AK295 protects neurons from focal brain ischemia: Effects of postocclusion intra-arterial administration. Stroke 25, 2265-2270.
5. BERNHARDT, R., and MATUS, A. (1984). Light and electron microscopic studies of the distribution of microtubule-associated protein 2 in rat brain: A difference between the dendritic and axonal cytoskeletons. J. Comp. Neurol. 226, 203-221.
6. BLOMGREN, K., MCRAE, A., BONA, E., SAIDO, T.C., KARLSSON, J-O., and HAGBERG, H. (1995). Degredation of fodrin and MAP2 after neonatal cerebral hypoxic-ischemia. Brain Res. 684, 136-142.
7. BONNEKOH, P., BARBIER, A., OSCHLIES, U., and HOSSMAN, K.-A. (1990). Selective vulnerability in the gerbil hippocampus: Morphological changes after 5-min ischemia and long survival times. Acta Neuropathologica 80, 18-25.
8. BRIERLEY, J.B. (1976). Cerebral Hypoxia, in: Greenfield's Neuropathology. W. Blackwood and J.A.N. Corsellis (eds), Edward Arnold Publishers: London, p. 56.
9. BRORSON, J.R., MARCUCILLI, C.J., and MILLER, R.J. (1995). Delayed antagonism of calpain reduces excitotoxicity in cultured neurons. Stroke 26, 1259-1267.
10. BRYAN, R.M., CHERIAN, L., and ROBERTSON, C. (1995). Regional cerebral blood flow after controlled cortical impact in rats. Anesth. Analg. 80, 687-695.
11. CHOI, D.W. (1988). Calcium mediated neurotoxicity: relationship to specific channel type and role in ischemic damage. TINS 11, 465-469.
12. COLICOS, M.A., and DASH, P.K. (1996). Apoptotic morphology of dentate gyrus granule cells following experimental cortical impact injury in rats: Possible role in spatial memory deficits. Brain Res. 739, 120-131.
13. COLICOS, M.A., DIXON, E.D., and DASH, P.K. (1996). Delayed, selective neuronal death following experimental cortical impact injury in rats: possible role in memory deficits. Brain Res. 739, 111-119.
14. DHERMY, D. (1991). The spectrin super-family. Biol. of the Cell 71, 249-254.
15. DIXON, C.E., CLIFTON, G.L., LIGHTHALL, J.W., YAGHMAI, A.A., and HAYES, R.L. (1991). A controlled cortical impact model of traumatic brain injury in the rat. J. Neurosci. Methods 39, 253-262.
16. DIXON, C.E., and HAYES, R.L. (1996). Fluid percussion and cortical impact models of traumatic brain injury, in Neurotrauma. R.K. Narayan, J.E. Wilberger, and J.T. Povlishock (eds), McGraw-Hill: NY, pps. 1337-1346.
17. FADEN, A.I., DOGMATIC, P., PANTER, S.S., and VINK, R. (1989). The role of excitatory amino acids and NMDA receptors in traumatic brain injury. Science 244, 798-800.
18. 45Ca autoradiographic study. Brain Res. 624, 94-102.
19. GEORGE, E.B., GLASS, J.D., and GRIFFIN, J.W. (1995). Axotomy induced axonal degeneration is mediated by calcium influx through ion-specific channels. J. Neurosci. 15, 6445-6452.
20. 2+-Dependent Proteinase System, in: Intracellular Calcium-Dependent Proteolysis. Mellgren, R.L., and Murachi, T. (eds), CRC Press: Boca Raton, FL, pps. 3-24.
21. GOODMAN, J.C., CHERIAN, L., BRYAN, JR., R.M., and ROBERTSON, C.S. (1994). Lateral cortical impact injury in rats: Pathologic effects of varying cortical compression and impact velocity. J. Neurotrauma 11, 587-597.
22. GUROFF, G. (1964). A neutral, calcium-activated proteinase from the soluble fraction of rat brain. J. Biol. Chem. 239, 149-155.
23. HAMAKUBO, T., KANNAGI, R., MURACHI, T., and MATUS, A. (1986). Distribution of calpains I and II in rat brain. J. Neurosci. 6, 3103-3111.
24. HAYES, R.L., JENKINS, L.W., and LYETH, B.C. (1992). Neurotransmitter mediated mechanisms of traumatic brain injury. J. Neurotrauma 9, 173-187.
25. HICKS, R.R., SMITH, D.H., and McINTOSH, T.K. (1995). Temporal response and effects of excitatory amino acid antagonism on microtubule-associated protein 2 immunoreactivity following experimental brain injury in rats. Brain Res. 678, 151-160.
26. HONG, S.C., GOTO, Y., LANZINO, G., SOLEAU, S., KASSELL, N.F., and LEE, K.S. (1994). Neuroprotection with a calpain inhibitor in a model of focal cerebral ischemia. Stroke 25, 663-669.
27. 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.
28. JOHNSON, G.V.W., LITERSKY, J.M., and JOPE, R.S. (1991). Degradation of microtubule associated protein 2 and spectrin by calpain: a comparative study. J. Neurochem. 56, 1630-1638.
29. KAKU, Y., YONEKAWA, Y., TSUKAHARA, T., OGATA, N., KIMURA, T., and TANIGUCHI, T. (1993). Alterations of a 200kDa neurofilament in the rat hippocampus after forebrain ischemia. J. Cereb. Blood Flow Metab. 13, 402-408.
30. KAMPFL, A., POSMANTUR, R., NIXON, R., GRYNSPAN, F., ZHAO, X., LIU, S.J., NEWCOMB, J.K., CLIFTON, G.L., and HAYES, R.L. (1996a). μ-Calpain activation and calpain-mediated cytoskeletal proteolysis following traumatic brain injury. J. Neurochem. 67, 1575-1583.
31. KAMPFL, A., POSMANTUR, R.M., ZHAO, X., SCHMUTZHARD, E., CLIFTON, G.L., and HAYES, R.L. (1997). Mechanisms of calpain proteolysis following traumatic brain injury: Implications for pathology and therapy. A review and update. J. Neurotrauma, in press.
32. KAMPFL, A., WHITSON, S.J., ZHAO, X., POSMANTUR, R., CLIFTON, G.L., and HAYES, R.L. (1995). Calpain inhibitors reduce depolarization induced loss of tau protein in primary septo-hippocampal cultures. Neurosci. Lett. 194, 149-152.
33. KAMPFL, A., ZHAO, X., WHITSON, S.J., POSMANTUR, R., DIXON, C.E., YANG, K., CLIFTON, G.L., and HAYES, R.L. (1996b). Calpain inhibitors protect against depolarization induced neurofilament protein loss of septo-hippocampal neurons in culture. Eur. J. Neurosci. 8, 344-352.
34. KARST, H., JOELS, M., and WADMAN, W.J. (1993). Low-threshold calcium currents in dendrites of the adult rat hippocampus. Neurosci. Lett. 164, 154-158.
35. KATAYAMA, Y., BECKER, D.P., TAMURA, T., and HOVDA, D.A. (1990). Massive increases in extracellular potassium and the indiscriminate release of glutamate following concussive brain injury. J. Neurosurg. 73, 889-900.
36. 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.
37. LI, Z., HOGAN, E.L., and BANIK, N.L. (1995). Role of calpain in spinal cord injury: Increased m-calpain immunoreactivity in spinal cord after compression injury in the rat. Neurochem. Int. 27, 425-432.
38. MATESIC, D.F., and LIN, R.C.S. (1994). Microtubule associated protein 2 as an early indicator of ischemia induced neurodegeneration in the gerbil forebrain. J. Neurochem. 63, 1012-1020.
39. McINTOSH, T.K., SMITH, D.H., and GARDE, E. (1996). Therapeutic approaches for the prevention of secondary brain injury. Eur. J. Anes. 13, 291-309.
40. MELLGREN, R.L. (1980). Canine cardiac calcium-dependent proteases: resolution of two forms with different requirements for calcium. FEBS Lett. 109, 129-133.
41. MELLONI, E., and PONTREMOLI, S. (1989). The calpains. TINS 12, 438-444.
42. 45Ca accumulation in rat brain after closed head injury; attenuation by the novel neuroprotective agent HU-211. Brain Res. 685, 1-11.
43. NAKAMURA, M., ARAKI, M., OGURO, K., and MASUZAWA, T. (1992). Differential distribution of 68kD and 200kD neurofilament proteins in gerbil hippocampus and their early distributional changes following transient forebrain ischemia. Exp. Brain Res. 89, 31-39.
44. NEUMAR, R.W., HAGLE, S.M., DEGARCIA, D.J., KRAUSE, G.S., and WHITE, B.C. (1996). Brain μ-calpain autolysis during global cerebral ischemia. J. Neurochem. 66, 421-424.
45. NG, T., GRAHAM, D.I., ADAMS, J.H., and FORD, I. (1989). Changes in the hippocampus and the cerebellum resulting from hypoxic insults: frequency and distribution. Acta Neuropathologica 78, 438-443.
46. 2+ levels following cortical compression contusion trauma in rats. J. Cereb. Blood Flow Metab. 13, 185-192.
47. NIXON, R.A. (1986). Fodrin degredation by calcium-activated neutral proteinase (CANP) in retinal ganglion cell neurons and optic glia: Preferential localization of CANP activities in neurons. J. Neurosci. 6, 1264-1271.
48. NIXON, R.A., CLARKE, J.F., LOGVINENKO, K.B., TAN, M.K.H., HOULT, M., and GRYNSPAN, F. (1990). Aluminium inhibits calpain mediated proteolysis and induces human neurofilament proteins to form protein resistant high molecular weight complexes. J. Neurochem. 55, 1950-1959.
49. PERLMUTTER, L.S., GALL, C., BAUDRY, M., and LYNCH, G. (1990). Distribution of calcium-activated protease calpain in the rat brain. J. Comp. Neurol. 296, 269-276.
50. PETTUS, E.H., CHRISTMAN, C.W., GIEBEL, M.L., and POVLISHOCK, J.T. (1994). Traumatically induced altered membrane permeability: Its relationship to traumatically induced reactive axonal change. J. Neurotrauma 11, 507-521.
51. POSMANTUR, R., HAYES, R.L., DIXON, C.E., and TAFT, W.C. (1994). Neurofilament 68 and neurofilament 200 protein levels decrease after traumatic brain injury. J. Neurotrauma 11, 533-545.
52. POSMANTUR, R.M., KAMPFL, A., LIU, S.J., HECK, K., TAFT, W.C., CLIFTON, G.L., and HAYES, R.L. (1996). Cytoskeletal derangements of cortical neuronal processes three hours after traumatic brain injury in rats: an immunofluorescence study. J. Neuropath. Exp. Neurol. 55, 68-80.
53. POSMANTUR, R.M., KAMPFL, A., SIMAN, R., LIU, S.J., ZHAO, X., CLIFTON, G.L., and HAYES, R.L. (1997). A calpain inhibitor attenuates cortical cytoskeletal protein loss after experimental brain injury in the rat. Neuroscience, in press.
54. POVLISHOCK, J.T., MARMAROU, A., McINTOSH, T., TROJANOWSKI, J.Q., and MOROI, J. (1996). Impact acceleration injury in the rat: evidence for focal axolemmal change and related neurofilament sidearm alteration. J. Neuropath. Exp. Neurol., in press.
55. PULSINELLI, W.A., BRIERLEY, J.B., and PLUM, F. (1982). Temporal profile of neuronal damage in a model of transient forebrain ischemia. Ann. Neurol. 11, 491-498.
56. 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.
57. REGEHR, W.G., and TANK, D.W. (1994). Dendritic calcium dynamics. Curr. Opin. Neurobiol. 4, 373-382.
58. RIEDERER, B., and MATUS, A. (1985). Differential expression of distinct microtubule-associated proteins during development. Proc. Natl. Acad. Sci. USA 82, 6006-6009.
59. ROBERTS-LEWIS, J.M., SAVAGE, M.J., MARCY, V.R., PINSKER, L.R., and SIMAN, R. (1994). Immunolocalization of μ calpain mediated spectrin degradation to vulnerable neurons in ischemic gerbil brain. J. Neurosci. 14, 3934-3944.
60. SAATMAN, K.E., BOZYCZKO-COYNE, D., MARCY, V., SIMAN, R., and MCINTOSH, T.K. (1996a). Prolonged calpain-mediated spectrin breakdown occurs regionally following experimental brain injury in the rat. J. Neuropath. Exp. Neurol. 55, 850-860.
61. SAATMAN, K.E., MURAI, H., BARTUS, R.T., SMITH, D.H., HAYWARD, N.J., PERRI, B.R., and MCINTOSH, T.K. (1996b). Calpain inhibitor AK295 attenuates motor and cognitive deficits following experimental brain injury in the rat. Proc. Natl. Acad. Sci. USA 93, 3428-3433.
62. SAIDO, T.C., SORIMACHI, H., and SUZUKI, K. (1994). Calpain: new perspectives in molecular diversity and physiological-pathological involvement. FASEB J. 8, 814-822.
63. SAIDO, T.C., YOKOTA, M., NAGAO, S., YAMAURA, 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.
64. SAITO, K.I., ELCE, I.S., HAMOS, J.E., and NIXON, R.A. (1993). Widespread activation of calcium-activated neutral proteinase (calpain) in the brain in Alzheimer disease: a potential molecular basis for neuronal degeneration. Proc. Natl. Acad. Sci. USA 90, 2628-2632.
65. SCHLAEPFER, W.W., and ZIMMERMAN, U.J.P. (1985). Calcium-activated proteolysis of intermediate filaments. Ann. N.Y. Acad. Sci. 455, 552-562.
66. SHAPIRA, Y., YADID, G., COTEV, S., and SHOHAMI, E. (1989). Accumulation of calcium in the brain following head trauma. Neurological Res. 11, 169-172.
67. SIESJOE, B.K., and BENGTSSON, F. (1989). Calcium fluxes, calcium antagonists, and calcium related pathology in brain ischemia, hypoglycemia, and spreading depression: a unifying hypothesis. J. Cereb. Blood Flow Metab. 9, 127-140.
68. SIMAN, R., BAUDRY, M., and LYNCH, G. (1984). Brain fodrin: Substrate for calpain I, an endogenous calcium-activated protease. Proc. Natl. Acad. Sci. USA 81, 3572-3576.
69. SIMAN, R., NOSZEK, J.C., and KEGERISE, C. (1989). Calpain I activation is specifically related to excitatory amino acid induction of hippocampal damage. J. Neurosci. 9, 1579-1590.
70. + conductance in rat optic nerve axons. Proc. Natl. Acad. Sci. USA 90, 6976-6980.
71. SUZUKI, K., TSUJI, S., ISHIURA, S., KTMURA, Y., KUBOTA, S., and IMAHORI, K. (1981). Autolysis of calcium-activated neutral protease of chicken skeletal muscle. J. Biochem. 90, 1787-1793.
72. TAFT, W.C., YANG, K., DIXON, C.E., CLIFTON, G.L., and HAYES, R.L. (1993). Hypothermia attenuates the loss of hippocampal microtubule-associated protein 2 (MAP2) following traumatic brain injury. J. Cereb. Blood Flow Metab. 13, 796-802.
73. TAFT, W.C., YANG, K., DIXON, C.E., and HAYES, R.L. (1992). Microtubule associated protein 2 level in hippocampus following traumatic brain injury. J. Neurotrauma 9, 281-290.
74. WANG, K.K.W., and YUEN, P.W. (1994). Calpain inhibition: an oveview of its therapeutic potential. TIPS 15, 412-419.
75. WHITSON, J.S., KAMPFL, A., ZHAO, X., and HAYES, R.L. (1995a). Time course of neurofilament protein loss following depolarization-induced injury in CNS culture. Neurosci. Lett. 197, 159-163.
76. WHITSON, J.S., KAMPFL, A., ZHAO, X., DIXON, C.E., and HAYES, R.L. (1995b). Brief potassium depolarization decreases levels of neurofilament proteins in CNS culture. Brain Res. 694, 213-222.
77. YAGHMAI, A., and POVLISHOCK, J.T. (1992). Traumatically induced reactive change as visualized through the use of monoclonal antibodies targeted to neurofilament subunits, J. Neuropath. Exp. Neurol. 51, 158-176.
78. YAMAKAMI, I., and McINTOSH, T.K. (1991). Alterations in regional cerebral blood flow following brain injury in the rat. J. Cereb. Blood Flow Metab. 11, 655-660.
79. YOKOTA, M., SAIDO, T.C., TANI, E., KAWASHIMA, S., and SUZUKI, K. (1995). Three distinct phases of fodrin proteolysis induced in postischemic hippocampus: Involvement of calpain and unidentified proteases. Stroke 26, 1901-1907.
80. YUSTE, R., GUTNICK, M.J., SAAR, D., DELANEY, K.R., and TANK, D.W. (1994). Calcium accumulations in dendrites of neocortical pyramidal neurons: An apical band and evidence for two functional compartments. Neuron 13, 23-43.
81. ZHAO, X., POSMANTUR, R.M., LIU, J.S., NEWCOMB, J.K., CLIFTON, G.L., and HAYES, R.L. (1996). Time-related calpain I activity analysis following traumatic brain injury in rat using casein zymography. Soc. Neurosci. Abstr 22, 1903.
82. ZIMMERMAN, U.J.P., and SCHLAEPFER, W.W. (1991). Two stage autolysis of the catalytic subunit initiates activation of μ calpain. Biochem. Biophys. Acta. 1078, 192-198.