Huntingtin is degraded to small fragments by calpain after ischemic injury

Experimental Neurology

Volumn 183, Issue 1, 2003, Pages 109-115

  Kim, Manho ^a   Roh, Jae Kyu ^a   Yoon, Byung Woo ^a   Kang, Lami ^a   Kim, Yun J ^b   Aronin, Neil ^c   DiFiglia, Marian ^a,b  

^a Seoul National University Hospital   (South Korea)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c UMASS MEMORIAL MEDICAL CENTER   (United States)

Author keywords

Calpain; Huntingtin proteolysis; Huntington's disease; Ischemia; N terminal huntingtin; Neurodegeneration

Indexed keywords

BRAIN EXTRACT; CALCIUM; CALPAIN; HUNTINGTIN; PROTEINASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN INFARCTION; BRAIN ISCHEMIA; CONTROLLED STUDY; CORPUS STRIATUM; ENZYME ACTIVATION; EXTRACTION; HUNTINGTON CHOREA; MALE; MOLECULAR WEIGHT; NERVE DEGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; RAT; STRIATE CORTEX; WESTERN BLOTTING;

EID: 0042190049     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0014-4886(03)00132-8     Document Type: Article

References (49)

1. Aronin N., Chase K., Young C., Sapp E., Schwarz C., Matta N., Kornreich R., Landwehrmeyer B., Bird E., Beal M.F., Vonsattel J.-P., Smith T., Carraway R., Boyce F.M., Young A.B., Penney J.B., DiFiglia M. CAG expansion affects the expression of mutant huntingtin in the Huntington's disease brain. Neuron. 15:1995;1193-1201.
2. Bhide P.G., Day M., Sapp E., Schwarz C., Sheth A., Kim J., Young A.B., Penney J., Golden J., Aronin N., DiFiglia M. Expression of normal and mutant huntingtin in the developing brain. J. Neurosci. 16:1996;5523-5535.
3. Block-Gallarza J., Chase K.O., Sapp E., Vaughn D.T., Vallee R.B., DiFiglia M., Aronin N. Fast transport and retrograde movement of huntingtin and HAP 1 in axons. NeuroReport. 8:1997;2247-2251.
4. Blomgren K., Ahu C., Wang X., Karlsson J.-O., Leverin A.-L., Bahr B.A., Hagberg H. Synergistic activation of caspase-3 by m-calpain after neonatal hypoxia-ischemia. J. Biol. Chem. 276:2001;10191-10198.
5. Castejon M.S., Culver D.G., Glass J.D. Generation of spectrin breakdown products in peripheral nerves by addition of M-calpain. Muscle Nerve. 22:1999;905-909.
6. Chan S.L., Mattson M.P. Caspase and calpain substrates roles in synaptic plasticity and cell death . J. Neurosci. Res. 58:1999;167-190.
7. Chen N., Luo T., Wellington C., Metzler M., McCutcheon D., Hayden M.R., Raymond L.A. Subtype-specific enhancement of NMDA receptor currents by mutant huntingtin. J. Neurochem. 72:1999;1890-1898.
8. Davies S.W., Turmaine M., Cozens B.A., DiFiglia M., Sharp A.H., Ross C.A., Scherzinger E., Wanker E.E., Mangiarini L., Bates G.P. Formation of neuronal intranuclear inclusions underlies the neurological dysfunction in mice transgenic for the HD mutation. Cell. 90:1997;537-548.
9. DiFiglia M. Excitotoxic injury of the neostriatum. A model for Huntington's disease. TINS. 13:1990;286-289.
10. DiFiglia M., Sapp E., Chase K., Schwarz C., Meloni A., Young C., Martin E., Vonsattel J.-P., Carraway R., Reeves S.A., Boyce F.M., Aronin N. Huntingtin is a cytoplasmic protein associated with vesicles in human and rat brain neurons. Neuron. 14:1995;1075-1081.
11. DiFiglia M., Sapp E., Chase K.O., Davies S.W., Bates G.F., Vonsattel J.-P., Aronin N. Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neurites in brain. Science. 277:1997;1990-1993.
12. duBois M., Bowman P.D., Goldstein G.W. Cell proliferation after ischemic injury in gerbil brain. An immunocytochemical and autoradiographic study. Cell Tissue Res. 242:1985;17-23.
13. Dyer R.B., McMurray C.T. Mutant protein in Huntington disease is resistant to proteolysis in affected brain. Nat. Genet. 29:2001;270-278.
14. Faddis B.T., Hasbani J., Goldberg M.P. Calpain activation contributes to dendritic remodeling after brief excitotoxic injury in vitro. J. Neurosci. 17:1997;951-959.
15. Gafni J., Ellerby L.M. Calpain activation in Huntington's disease. J. Neurosci. 22:2002;4842-4849.
16. Goffredo, D., Rigamonti, D., Tartari, M., DeMicheli, A., Verderio, C., Matteoli, M., Zuccato, C., Cattaneo, E., 2002. Calcium-dependent cleavage of endogenous wild-type huntingtin in primary cortical neurons. J Biol. Chem. 277, 39594-39598.
17. Grynspan F., Griffin W.B., Mohan P.S., Shea T.B., Nixon R.A. Calpains and calpastatin in SH-SY5Y neuroblastoma cells during retinoic acid-induced differentiation and neurite outgrowth comparison with the human brain calpain system . J. Neurosci. Res. 48:1997;181-191.
18. Hackam A., Singaraja T., Wellington C.L., Metzler M., McCutcheon K., Zhang T., Kalchaman M., Hayden M.R. The influence of huntingtin protein size on nuclear localization and cellular toxicity. J. Cell Biol. 141:1998;1097-1105.
19. Hewitt K.E., Lesiuk H.J., Tauskela J.S., Morley P., Durkin J.P. Selective coupling of μ-calpain activation with the NMDA receptor is independent of translocation and autolysis in primary cortical neurons. J. Neurosci. Res. 54:1998;223-232.
20. Hong S.C., Goto Y., Lanzino G., Sloeau S., Kassell N.F., Lee K.S. Neuroprotection with a calpain inhibitor in a model of focal cerebral ischemia. Stroke. 25:1994;663-669.
21. A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. Cell. 72:1993;971-983.
22. Katchanov J., Gertz K., Dirmagl U., Veh R.W., Endres M. Loss of striatal spiny projection neurons but not interneurons following mild focal brain ischemia. Soc. Neurosci. Abstr. 27:2001;1163.
23. Kim Y.J., Yi Y., Sapp E., Wang Y., Cuiffo B., Kegel K.B., Qin Z.-H., Aronin N., DiFiglia M. Caspase 3 cleaved N-terminal fragments of wt and mutant huntingtin are present in normal and Huntington's disease brains, associate with membranes, and undergo calpain-dependent proteolysis. Proc. Natl. Acad. Sci. USA. 98:2001;12784-12789.
24. Laforet G., Sapp E., Chase K., McIntyre C., Boyce F.M., Campbell M., Cadigan B.A., Warzecki L., Tagle D.A., Reddy H., Cepeda C., Calvert C.R., Jokel E.S., Klapstein G.J., Ariano M.A., Levine M., DiFiglia M., Aronin N. Changes in cortical and striatal neurons predict behavioral and electrophysiological abnormalities in a transgenic murine model of Huntington's disease. J. Neurosci. 21:2001;9112-9123.
25. Leist M., Volbracht C., Rava E., Nicotera P. 1-Methyl-4-phenylpyridinium induces autocrine excitotoxicity, protease activation, and neuronal apoptosis. Mol. Pharmacol. 54:1998;789-801.
26. Liebetrau M., Staufer B., Auerswald E.A., Gabrijelcic-Geiger D., Fritz H., Zimmermann C., Pfefferkorn T., Hamann G.F. Increased intracellular calpain detection in experimental focal cerebral ischemia. NeuroReport. 10:1999;529-534.
27. Longa E.Z., Weinstein P.R., Carlson S., Cummins R. Reversible middle cerebral artery occlusion without craniectomy in rats. Stroke. 20:1989;84-91.
28. Lunkes, A., Lindenberg, K.S., L., Ben-Haiem, L., Weber, C., Devys, D., Landewehrmeyer, G.B., J.L., Trottier, Y., 2002. Proteases acting on mutant huntingtin generate cleaved products that differentially build up cytoplasmic and nuclear inclusions. Mol. Cell 10;259-269.
29. Meade C.A., Figueredo-Cardenas G., Fusco F., Nowak T.S. Jr., Pulsinelli W.A., Reiner A. Transient global ischemia in rats yields striatal projection neurons and interneuron loss resembling that in Huntington's disease. Exp. Neurol. 166:2000;307-322.
30. Mende-Mueller L.M., Toneff T., Hwang S.-R., Chesselet M.-F., Hood V.Y.H. Tissue-specific proteolysis of huntingtin (htt) in human brain evidence of enhanced levels of N- and C-terminal htt fragments in Huntington's disease striatum . J. Neurosci. 2:2001;1830-1837.
31. 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. 170:2001;27-35.
32. Pettigrew L.C., Holtz M.L., Craddock S.D., Minger S.L., Hall N., Geddes W. Microtubular proteolysis in focal cerebral ischemia. J. Cereb. Blood Flow Metab. 16:1996;1189-1202.
33. Pike B.R., Zhao X., Newcomb J.K., Glenn C.C., Anderson D.K., Hayes R.L. Stretch injury causes calpain and caspase-3 activation and necrotic and apoptotic cell death in septo-hippocampal cell cultures. J. Neurotrauma. 17:2000;283-298.
34. Rami A., Agarwal R., Botez G., Winckler J. mu-Calpain activation, DNA fragmentation, and synergistic effects of caspase and calpain inhibitors in protecting hippocampal neurons from ischemic damage. Brain Res. 866:2000;299-312.
35. Roberts-Lewis J.M., Savage M.J., Marcy V.R., Pinsker L.R., Siman R. Immunolocalization of calpain 1-mediated spectrin degradation to vulnerable neurons in the ischemic gerbil brain. J. Neurosci. 14:1994;3934-3944.
36. Ruan Y.W., Zhang J.L., Ling G.Y., Xu Z.C. Both necrosis and apoptosis occur in the striatum following transient global ischemia. Soc. Neurosci. Abstr. 27:2001;547.
37. Saatman K.E., Bozyczko-Coyne D., Siman M.V., McIntosh T.K. Prolonged calpain-mediated spectrin breakdown occurs regionally following experimental brain injury in the rat. J. Neuropathol. Exp. Neurol. 55:1996;850-860.
38. Saito K.-I., Elce J.S., Hamos J.E., Nixon R.A. 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. 90:1993;2628-2632.
39. Saito Y., Saido T.C., Sano K., Kawashima S. The calpain-calpastatin system is regulated differently during human neuroblastoma cell differentiation to Schwannian and neuronal cells. FEBS Lett. 353:1994;327-331.
40. Saudou F., Finkbeiner S., Devys D., Greenberg M.E. Huntingtin acts in the nucleus to induce apoptosis but death does not correlate with the formation of intranuclear inclusions. Cell. 95:1998;55-66.
41. Scherzinger E., Lurz R., Turmaine M., Mangiarini L., Hollenbach B., Hasenbank R., Bates G.P., Davies S.W., Lehrach H., Wanker E.E. Huntingtin-encoded polyglutamine expansions form amyloid-like protein aggregates in vitro and in vivo. Cell. 90:1997;549-558.
42. Schumacher P.S., Siman R.G., Fehlings M.G. Pretreatment with calpain inhibitor CEP-4143 inhibits calpain I activation and cytoskeletal degradation, improves neurological function, and enhances axonal survival after traumatic spinal cord injury. J. Neurochem. 74:2000;1646-1655.
43. Sun Y., Savanenin A., Reddy P.H., Liu Y.F. Polyglutamine-expanded huntingtin promotes sensitization of N-methyl-D-aspartate receptors via post-synaptic density 95. J. Biol. Chem. 276:2001;24713-24718.
44. Vanderklish P.W., Bahr B.A. The pathogenic activation of calpain a marker and mediator of cellular toxicity and disease states . Int. J. Exp. Pathol. 81:2000;323-339.
45. Wang K.K.W. Calpain and caspase can you tell the difference? Trends Neurosci. 23:2000;20-26.
46. Wellington C.L., Ellerby L.M., Hackam A.S., Margolis R.L., Trifiro M.A., Singaraja R., McCutcheon K., Salvesen G.S., Propp S.S., Bromm M., Rowland K.J., Zhang T., Rasper D., Roy S., Thornberry N., Pinsky L., Kakizuka A., Ross C.A., Nicholson D.W., Bredesen D.E., Hayden M.R. Caspase cleavage of gene products associated with triplet expansion disorders generates truncated fragments containing the polyglutamine tract. J. Biol. Chem. 273:1998;9158-9167.
47. Wellington C.L., Singaraja R., Ellerby L., Savill J., Roy S., Leavitt B., Cattaneo E., Hackam A., Sharp A., Thornberry N., Nicholson D.W., Bredesen D.E., Hayden M.R. Inhibiting caspase cleavage of huntingtin reduces toxicity and aggregate formation in neuronal and nonneuronal cells. J. Biol. Chem. 275:2000;19831-19838.
48. Yamashima T. Implication of cysteine proteases calpain, cathepsin and caspase in ischemic neuronal death of primates. Prog. Neurobiol. 62:2000;273-295.
49. Zeron M.M., Chen N., Moshaver A., Lee T.-C., Wellington C.L., Hayden M.R., Raymond L.A. Mutant huntingtin enhances excitotoxic cell death. Mol. Cell. Neurosci. 17:2001;41-53.