Inhibition of autophagy causes tau proteolysis by activating calpain in rat brain

Journal of Alzheimer's Disease

Volumn 16, Issue 1, 2009, Pages 39-47

  Zhang, Jia Yu ^a   Peng, Caixia ^a   Shi, Hairong ^a   Wang, Shaohui ^a   Wang, Qun ^a   Wang, Jian Zhi ^a,b  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

Autophagy; Calpain; Degradation; Tau

Indexed keywords

3 METHYLADENINE; BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; CALPAIN; CHLOROQUINE; PROTEASOME; PROTEINASE; RAPAMYCIN; TAU PROTEIN;

ANIMAL TISSUE; ARTICLE; AUTOPHAGY; BRAIN; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME MECHANISM; ENZYME REPRESSION; HIPPOCAMPUS; LATERAL BRAIN VENTRICLE; LYSOSOME; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; RAT; WESTERN BLOTTING;

EID: 58849106655     PISSN: 13872877     EISSN: None     Source Type: Journal    
DOI: 10.3233/JAD-2009-0908     Document Type: Article

References (42)

1. Alonso A, Grundke-Iqbal I, Barra HS, Iqbal K (1997) Abnormal phosphorylation of tau and the mechanism of Alzheimer neurofibrillary degeneration: sequestration of microtubule-associated proteins 1 and 2 and the disassembly of microtubules by the abnormal tau. Proc Natl Acad Sci USA 94, 298-303.
2. Avila J, Lucas J, Perez M, Hernandez F (2004) Role of tau protein in both physiological and pathological conditions. Physiol Rev 54, 361-384.
3. Bednarski E, Lynch G (1996) Cytosolic proteolysis of tau by cathepsin D in hippocampus following suppression of cathepsins B and L. J Neurochem 67, 1846-1855.
4. Bennett E, Bence N, Jayakumar R, Kopito R (2005) Global impairment of the ubiquitin-proteasome system by nuclear or cytoplasmic protein aggregates precedes inclusion body formation. Mol Cell 17, 351-365.
5. Berger Z, Ravikumar B, Menzies FM, Oroz LG, Underwood BR, Pangalos MN, Schmitt I, Wullner U, Evert BO, O'Kane CJ, Rubinsztein DC (2006) Rapamycin alleviates toxicity of different aggregate-prone proteins. Hum Mol Genet 15, 433-442.
6. Bi X, Zhou J, Lynch G (1999) Lysosomal protease inhibitors induce meganeurites and tangle-like structures in entorhino-hippocampal regions vulnerable to Alzheimer's disease. Exp Neurol 158, 312-327.
7. Brown MR, Bondada V, Keller JN, Thorpe J, Geddes JW (2005) Proteasome or calpain inhibition does not alter cellular tau levels in neuroblastoma cells or primary neurons. J Alzheimers Dis 7, 15-24.
8. Cataldo AM, Barnett JL, Berman SA, Li J, Quarless S, Bursztajn S, Lippa C, Nixon RA (1995) Gene expression and cellular content of cathepsin D in Alzheimer's disease brain: evidence for early upregulation of the endosomal/lysosomal system. Neuron 14, 671-680.
9. Cataldo AM, Hamilton DJ, Barnett JL, Paskevich PA, Nixon RA (1996) Properties of the endosomal-lysosomal system in the human central nervous system: disturbances mark most neurons in populations at risk to degenerate in Alzheimer's disease. J Neurosci 16, 186-199.
10. Cataldo AM, Paskevich PA, Kominami E, Nixon RA (1991) Lysosomal hydrolases of different classes are abnormally distributed in brains of patients with Alzheimer disease. Proc Natl Acad Sci USA 88, 10998-11002.
11. Cuervo AM (2004) Autophagy: in sickness and in health. Trends Cell Biol 14, 70-77.
12. Demarchi F, Bertoli C, Copetti T, Tanida I, Brancolini C, Eskelinen EL, Schneider C (2006) Calpain is required for macroautophagy in mammalian cells. J Cell Biol 175, 595-605.
13. Goedert M, Ghetti B, Spillantini MG (2000) Tau gene mutations in frontotemporal dementia and parkinsonism linked to chromosome 17 (FTDP-17). Their relevance for understanding the neurodegenerative process. Ann N Y Acad Sci 920, 74-78.
14. Grundke-Iqbal I, Iqbal K, Quinlan M, Tung YC, Zaidi MS, Wisniewski HM (1986) Microtubule-associated protein tau: A component of Alzheimer paired helical filaments. J Biol Chem 261, 6084-6089.
15. Hara T, Nakamura K, Matsui M, Yamamoto A, Nakahara Y, Suzuki-Migishima R, Yokoyama M, Mishima K, Saito I, Okano H, Mizushima N (2006) Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature 441, 885-889.
16. Hartford CM, Ratain MJ (2007) Rapamycin: something old, something new, sometimes borrowed and now renewed. Clin Pharmacol Ther 82, 381-388.
17. Hegde AN, Upadhya SC (2007) The ubiquitin-proteasome pathway in health and disease of the nervous system. Trends Neurosci 30, 587-595.
18. Hutton M, Lendon CL, Rizzu P, Baker M, Froelich S, Houlden H, Pickering-Brown S, Chakraverty S, Isaacs A, Grover A, Hackett J, Adamson J, Lincoln S, Dickson D, Davies P, Petersen RC, Stevens M, de Graaff E, Wauters E, van Baren J, Hillebrand M, Joosse M, Kwon JM, Nowotny P, Che LK, Norton J, Morris JC, Reed LA, Trojanowski J, Basun H, Lannfelt L, Neystat M, Fahn S, Dark F, Tannenberg T, Dodd PR, Hayward N, Kwok JB, Schofield PR, Andreadis A, Snowden J, Craufurd D, Neary D, Owen F, Oostra BA, Hardy J, Goate A, van Swieten J, Mann D, Lynch T, Heutink P (1998) Association of missense and 50-splice-site mutations in tau with the inherited dementia FTDP-17. Nature 393, 702-705.
19. Iqbal K, Grundke-Iqbal I, Smith AJ, George L, Tung YC, Zaidi T (1989) Identification and localization of a tau peptide to paired helical filaments of Alzheimer disease. Proc Natl Acad Sci USA 86, 5646-5650.
20. Kabashi E, Agar JN, Taylor DM, Minotti S, Durham HD (2004) Focal dysfunction of the proteasome: a pathogenic factor in a mouse model of amyotrophic lateral sclerosis. J Neurochem 89, 1325-1335.
21. Ravikumar B, Vacher C, Berger Z, Davies JE, Luo S, Oroz LG, Scaravilli F, Easton DF, Duden R, O'Kane CJ, Rubinsztein DC (2004) Inhibition of mTOR induces autophagy and reduces toxicity of polyglutamine expansions in fly and mouse models of Huntington disease. Nat Genet 36, 585-595.
22. Keck S, Nitsch R, Grune T, Ullrich O (2003) Proteasome inhibition by paired helical filament-tau in brains of patients with Alzheimer's disease. J Neurochem 85, 115-122.
23. Kenessey A, Nacharaju P, Ko LW, Yen SH (1997) Degradation of tau by lysosomal enzyme cathepsin D: implication for Alzheimer neurofibrillary degeneration. J Neurochem 69, 2026-2038.
24. Kohli V, Gao W, Camargo CA Jr., Clavien PA (1997) Calpain is a mediator of preservation-reperfusion injury in rat liver transplantation. Proc Natl Acad Sci USA 94, 9354-9359.
25. Komatsu M, Waguri S, Chiba T, Murata S, Iwata J, Tanida I, Ueno T, Koike M, Uchiyama Y, Kominami E, Tanaka K (2006) Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature 441, 880-884.
26. Lee MS, Kwon YT, Li M, Peng J, Friedlander RM, Tsai LH (2000) Neurotoxicity induces cleavage of p35 to p25 by calpain. Nature 405, 360-364.
27. Liu YH, Wei W, Yin J, Liu GP, Wang Q, Cao FY, Wang JZ (2008) Proteasome inhibition increases tau accumulation independent of phosphorylation, Neurobiol Aging (2008), in press.
28. Mizushima N (2007) Autophagy: process and function. Genes Dev 21, 2861-2873.
29. Murakami N, Oyama F, Gu Y, McLennan IS, Nonaka I, Ihara Y (1998) Accumulation of tau in autophagic vacuoles in chloroquine myopathy. J Neuropathol Exp Neurol 57, 664-673.
30. Nixon RA, Cataldo AM (1993) The lysosomal system in neuronal cell death: a review. Ann NY Acad Sci 679, 87-109.
31. Nixon RA, Wegiel J, Kumar A, Yu WH, Peterhoff C, Cataldo A, Cuervo AM (2005) Extensive involvement of autophagy in Alzheimer disease: an immuno-electron microscopy study. J Neuropathol Exp Neurol 64, 113-122.
32. Qin ZH, Wang Y, Kegel KB, Kazantsev A, Apostol BL, Thompson LM, Yoder J, Aronin N, DiFiglia M (2003) Autophagy regulates the processing of amino terminal huntingtin fragments. Hum Mol Genet 12, 3231-3244.
33. Ravikumar B, Duden R, Rubinsztein DC (2002) Aggregate-prone proteins with polyglutamine and polyalanine expansions are degraded by autophagy. Hum Mol Genet 11, 1107-1117.
34. Rubinsztein DC, Gestwicki JE, Murphy LO, Klionsky DJ (2007) Potential therapeutic applications of autophagy. Nat Rev Drug Discov 6, 304-312.
35. Schwagerl AL, Mohan PS, Cataldo AM, Vonsattel JP, Kowall NW, Nixon RA (1995) Elevated levels of the endosomal-lysosomal proteinase cathepsin D in cerebrospinal fluid in Alzheimer disease. J Neurochem 64, 443-446.
36. Seglen PO, Gordon PB (1982) 3-Methyladenine: specific inhibitor of autophagic/lysosomal protein degradation in isolated rat hepatocytes. Proc Natl Acad Sci USA 79, 1889-1892.
37. Takeuchi IK, Takeuchi YK (2001) Transient accumulation of Gallyas-Braak- positive and phosphorylated tau-immunopositive substances in neuronal lipofuscin granules in the amygdala, hippocampus and entorhinal cortex of rats during long-term chloroquine intoxication. Acta Neuropathol (Berl) 102, 191-194.
38. Taniguchi S, Fujita Y, Hayashi S, Kakita A, Takahashi H, Murayama S, Saido TC, Hisanaga S, Iwatsubo T, Hasegawa M (2001) Calpain-mediated degradation of p35 to p25 in post-mortem human and rat brains. FEBS Lett 489, 46-50.
39. Wang CW, Klionsky DJ (2003) The molecular mechanism of autophagy. Mol Med 9, 65-76.
40. Wei W, Fareed MU, Evenson A, Menconi MJ, Yang H, Petkova V, Hasselgren PO (2005) Sepsis stimulates calpain activity in skeletal muscle by decreasing calpastatin activity but does not activate caspase-3. Am J Physiol Regul Integr Comp Physiol 288, R580-R590.
41. Wibo M, Poole B (1974) Protein degradation in cultured cells. II. The uptake of chloroquine by rat fibroblasts and the inhibition of cellular protein degradation and cathepsin B1. J Cell Biol 63, 430-440.
42. Yang LS, Ksiezak-Reding H (1995) Calpain-induced proteolysis of normal human tau and tau associated with paired helical filaments. Eur J Biochem 233, 9-17.