Implicating calpain in tau-mediated toxicity In Vivo

PLoS ONE

Volumn 6, Issue 8, 2011, Pages

  Reinecke, James B ^a   DeVos, Sarah L ^a   McGrath, James P ^a   Shepard, Amanda M ^a   Goncharoff, Dustin K ^a   Tait, Don N ^a   Fleming, Samantha R ^a   Vincent, Michael P ^a   Steinhilb, Michelle L ^a  

^a CENTRAL MICHIGAN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALPAIN; CALPAIN A; CALPAIN B; TAU PROTEIN; UNCLASSIFIED DRUG; CALPAIN A, DROSOPHILA; CALPB PROTEIN, DROSOPHILA; DROSOPHILA PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEGENERATIVE DISEASE; DROSOPHILA; GENOMIC FRAGMENT; IN VIVO STUDY; MUTATIONAL ANALYSIS; NEUROTOXICITY; NONHUMAN; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; RETINA; SIGNAL TRANSDUCTION; TAUOPATHY; ANIMAL; CELL CULTURE; DISEASE MODEL; EYE; GENETICS; METABOLISM; MUTATION; NERVE CELL; PATHOLOGY; SCANNING ELECTRON MICROSCOPY; TRANSGENIC ANIMAL; ULTRASTRUCTURE; WESTERN BLOTTING;

ANIMALIA;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BLOTTING, WESTERN; CALPAIN; CELLS, CULTURED; DISEASE MODELS, ANIMAL; DROSOPHILA PROTEINS; EYE; MICROSCOPY, ELECTRON, SCANNING; MUTATION; NEURODEGENERATIVE DISEASES; NEURONS; TAU PROTEINS; TAUOPATHIES;

EID: 80051766151     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0023865     Document Type: Article

References (63)

1. Hong M, Zhukareva V, Vogelsberg-Ragaglia V, Wszolek Z, Reed L, et al. (1998) Mutation-specific functional impairments in distinct tau isoforms of hereditary FTDP-17. Science 282: 1914-1917.
2. Poorkaj P, Bird TD, Wijsman E, Nemens E, Garruto RM, et al. (1998) Tau is a candidate gene for chromosome 17 frontotemporal dementia. Ann Neurol 43: 815-825.
3. Hutton M, Lendon CL, Rizzu P, Baker M, Froelich S, et al. (1998) Association of missense and 5′-splice-site mutations in tau with the inherited dementia FTDP-17. Nature 393: 702-705.
4. Spillantini MG, Murrell JR, Goedert M, Farlow MR, Klug A, et al. (1998) Mutation in the tau gene in familial multiple system tauopathy with presenile dementia. Proc Natl Acad Sci U S A 95: 7737-7741.
5. Wittmann CW, Wszolek MF, Shulman JM, Salvaterra PM, Lewis J, et al. (2001) Tauopathy in Drosophila: neurodegeneration without neurofibrillary tangles. Science 293: 711-714.
6. Shulman JM, Feany MB, (2003) Genetic modifiers of tauopathy in Drosophila. Genetics 165: 1233-1242.
7. Adamec E, Mohan PS, Cataldo AM, Vonsattel JP, Nixon RA, (2000) Up-regulation of the lysosomal system in experimental models of neuronal injury: implications for Alzheimer's disease. Neuroscience 100: 663-675.
8. Delobel P, Leroy O, Hamdane M, Sambo AV, Delacourte A, et al. (2005) Proteasome inhibition and Tau proteolysis: an unexpected regulation. FEBS Lett 579: 1-5.
9. Oddo S, Billings L, Kesslak JP, Cribbs DH, LaFerla FM, (2004) Abeta immunotherapy leads to clearance of early, but not late, hyperphosphorylated tau aggregates via the proteasome. Neuron 43: 321-332.
10. Siman R, McIntosh TK, Soltesz KM, Chen Z, Neumar RW, et al. (2004) Proteins released from degenerating neurons are surrogate markers for acute brain damage. Neurobiol Dis 16: 311-320.
11. Canu N, Dus L, Barbato C, Ciotti MT, Brancolini C, et al. (1998) Tau cleavage and dephosphorylation in cerebellar granule neurons undergoing apoptosis. J Neurosci 18: 7061-7074.
12. Park SY, Ferreira A, (2005) The generation of a 17 kDa neurotoxic fragment: an alternative mechanism by which tau mediates beta-amyloid-induced neurodegeneration. J Neurosci 25: 5365-5375.
13. Reifert J, Hartung-Cranston D, Feinstein SC, (2011) Amyloid beta mediated cell death of cultured hippocampal neurons reveals extensive tau fragmentation without increased full-length tau phosphorylation. J Biol Chem doi:10.1074/jbc.M111.234674.
14. Ferreira A, Bigio EH, (2011) Calpain-mediated tau cleavage: a mechanism leading to neurodegeneration shared by multiple tauopathies. Mol Med doi:10.2119/molmed.2010.00220.
15. Xie H, Johnson GV, (1997) Ceramide selectively decreases tau levels in differentiated PC12 cells through modulation of calpain I. J Neurochem 69: 1020-1030.
16. Xie HQ, Johnson GV, (1998) Calcineurin inhibition prevents calpain-mediated proteolysis of tau in differentiated PC12 cells. J Neurosci Res 53: 153-164.
17. Lee MS, Kwon YT, Li M, Peng J, Friedlander RM, et al. (2000) Neurotoxicity induces cleavage of p35 to p25 by calpain. Nature 405: 360-364.
18. Liang B, Duan BY, Zhou XP, Gong JX, Luo ZG, (2010) Calpain activation promotes BACE1 expression, amyloid precursor protein processing, and amyloid plaque formation in a transgenic mouse model of Alzheimer disease. J Biol Chem 285: 27737-27744.
19. Nixon RA, (2003) The calpains in aging and aging-related diseases. Ageing Res Rev 2: 407-418.
20. Friedrich P, Tompa P, Farkas A, (2004) The calpain-system of Drosophila melanogaster: coming of age. Bioessays 26: 1088-1096.
21. Gafni J, Hermel E, Young JE, Wellington CL, Hayden MR, et al. (2004) Inhibition of calpain cleavage of huntingtin reduces toxicity: accumulation of calpain/caspase fragments in the nucleus. J Biol Chem 279: 20211-20220.
22. Ratovitski T, Chighladze E, Waldron E, Hirschhorn RR, Ross CA, (2011) Cysteine Proteases Bleomycin Hydrolase and Cathepsin Z Mediate N-terminal Proteolysis and Toxicity of Mutant Huntingtin. J Biol Chem 286: 12578-12589.
23. Dufty BM, Warner LR, Hou ST, Jiang SX, Gomez-Isla T, et al. (2007) Calpain-cleavage of alpha-synuclein: connecting proteolytic processing to disease-linked aggregation. Am J Pathol 170: 1725-1738.
24. Delobel P, Mailliot C, Hamdane M, Sambo AV, Begard S, et al. (2003) Stable-tau overexpression in human neuroblastoma cells: an open door for explaining neuronal death in tauopathies. Ann N Y Acad Sci 1010: 623-634.
25. Khlistunova I, Biernat J, Wang Y, Pickhardt M, von Bergen M, et al. (2006) Inducible expression of Tau repeat domain in cell models of tauopathy: aggregation is toxic to cells but can be reversed by inhibitor drugs. J Biol Chem 281: 1205-1214.
26. Wang YP, Biernat J, Pickhardt M, Mandelkow E, Mandelkow EM, (2007) Stepwise proteolysis liberates tau fragments that nucleate the Alzheimer-like aggregation of full-length tau in a neuronal cell model. Proc Natl Acad Sci U S A 104: 10252-10257.
27. Bandyopadhyay B, Li G, Yin H, Kuret J, (2007) Tau aggregation and toxicity in a cell culture model of tauopathy. J Biol Chem 282: 16454-16464.
28. Garg S, Timm T, Mandelkow EM, Mandelkow E, Wang Y, (2011) Cleavage of Tau by calpain in Alzheimer's disease: the quest for the toxic 17 kD fragment. Neurobiol Aging 32: 1-14.
29. Farkas A, Nardai G, Csermely P, Tompa P, Friedrich P, (2004) DUK114, the Drosophila orthologue of bovine brain calpain activator protein, is a molecular chaperone. Biochem J 383: 165-170.
30. 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.
31. Cuerrier D, Moldoveanu T, Davies PL, (2005) Determination of peptide substrate specificity for mu-calpain by a peptide library-based approach: the importance of primed side interactions. J Biol Chem 280: 40632-40641.
32. Tompa P, Buzder-Lantos P, Tantos A, Farkas A, Szilagyi A, et al. (2004) On the sequential determinants of calpain cleavage. J Biol Chem 279: 20775-20785.
33. Nicholson AM, Methner DN, Ferreira A, (2011) Membrane cholesterol modulates {beta}-amyloid-dependent tau cleavage by inducing changes in the membrane content and localization of N-methyl-D-aspartic acid receptors. J Biol Chem 286: 976-986.
34. Nicholson AM, Ferreira A, (2009) Increased membrane cholesterol might render mature hippocampal neurons more susceptible to beta-amyloid-induced calpain activation and tau toxicity. J Neurosci 29: 4640-4651.
35. Park SY, Tournell C, Sinjoanu RC, Ferreira A, (2007) Caspase-3- and calpain-mediated tau cleavage are differentially prevented by estrogen and testosterone in beta-amyloid-treated hippocampal neurons. Neuroscience 144: 119-127.
36. Schilling B, Gafni J, Torcassi C, Cong X, Row RH, et al. (2006) Huntingtin phosphorylation sites mapped by mass spectrometry. Modulation of cleavage and toxicity. J Biol Chem 281: 23686-23697.
37. Adamec E, Mohan P, Vonsattel JP, Nixon RA, (2002) Calpain activation in neurodegenerative diseases: confocal immunofluorescence study with antibodies specifically recognizing the active form of calpain 2. Acta Neuropathol (Berl) 104: 92-104.
38. Peterson C, Goldman JE, (1986) Alterations in calcium content and biochemical processes in cultured skin fibroblasts from aged and Alzheimer donors. Proc Natl Acad Sci U S A 83: 2758-2762.
39. Adamec E, Murrell JR, Takao M, Hobbs W, Nixon RA, et al. (2002) P301L tauopathy: confocal immunofluorescence study of perinuclear aggregation of the mutated protein. J Neurol Sci 200: 85-93.
40. Hung KS, Hwang SL, Liang CL, Chen YJ, Lee TH, et al. (2005) Calpain inhibitor inhibits p35-p25-Cdk5 activation, decreases tau hyperphosphorylation, and improves neurological function after spinal cord hemisection in rats. J Neuropathol Exp Neurol 64: 15-26.
41. Sinjoanu RC, Kleinschmidt S, Bitner RS, Brioni JD, Moeller A, et al. (2008) The novel calpain inhibitor A-705253 potently inhibits oligomeric beta-amyloid-induced dynamin 1 and tau cleavage in hippocampal neurons. Neurochem Int 53: 79-88.
42. Veeranna, Kaji T, Boland B, Odrljin T, Mohan P, et al. (2004) Calpain mediates calcium-induced activation of the erk1,2 MAPK pathway and cytoskeletal phosphorylation in neurons: relevance to Alzheimer's disease. Am J Pathol 165: 795-805.
43. Rao MV, Mohan PS, Peterhoff CM, Yang DS, Schmidt SD, et al. (2008) Marked calpastatin (CAST) depletion in Alzheimer's disease accelerates cytoskeleton disruption and neurodegeneration: neuroprotection by CAST overexpression. J Neurosci 28: 12241-12254.
44. Li PA, Howlett W, He QP, Miyashita H, Siddiqui M, et al. (1998) Postischemic treatment with calpain inhibitor MDL 28170 ameliorates brain damage in a gerbil model of global ischemia. Neurosci Lett 247: 17-20.
45. Noble W, Olm V, Takata K, Casey E, Mary O, et al. (2003) Cdk5 is a key factor in tau aggregation and tangle formation in vivo. Neuron 38: 555-565.
46. Monaco EA 3rd, (2004) Recent evidence regarding a role for Cdk5 dysregulation in Alzheimer's disease. Curr Alzheimer Res 1: 33-38.
47. Amadoro G, Ciotti MT, Costanzi M, Cestari V, Calissano P, et al. (2006) NMDA receptor mediates tau-induced neurotoxicity by calpain and ERK/MAPK activation. Proc Natl Acad Sci U S A 103: 2892-2897.
48. Amadoro G, Pieri M, Ciotti MT, Carunchio I, Canu N, et al. (2007) Substance P provides neuroprotection in cerebellar granule cells through Akt and MAPK/Erk activation: evidence for the involvement of the delayed rectifier potassium current. Neuropharmacology 52: 1366-1377.
49. Loewen CA, Feany MB, (2010) The unfolded protein response protects from tau neurotoxicity in vivo. PLoS One 5.
50. Khurana V, Elson-Schwab I, Fulga TA, Sharp KA, Loewen CA, et al. (2010) Lysosomal dysfunction promotes cleavage and neurotoxicity of tau in vivo. PLoS Genet 6: e1001026.
51. Dermaut B, Norga KK, Kania A, Verstreken P, Pan H, et al. (2005) Aberrant lysosomal carbohydrate storage accompanies endocytic defects and neurodegeneration in Drosophila benchwarmer. J Cell Biol 170: 127-139.
52. Fulga TA, Elson-Schwab I, Khurana V, Steinhilb ML, Spires TL, et al. (2007) Abnormal bundling and accumulation of F-actin mediates tau-induced neuronal degeneration in vivo. Nat Cell Biol 9: 139-148.
53. Blard O, Feuillette S, Bou J, Chaumette B, Frebourg T, et al. (2007) Cytoskeleton proteins are modulators of mutant tau-induced neurodegeneration in Drosophila. Hum Mol Genet 16: 555-566.
54. Feuillette S, Deramecourt V, Laquerriere A, Duyckaerts C, Delisle MB, et al. (2010) Filamin-A and Myosin VI colocalize with fibrillary Tau protein in Alzheimer's disease and FTDP-17 brains. Brain Res 1345: 182-189.
55. Dias-Santagata D, Fulga TA, Duttaroy A, Feany MB, (2007) Oxidative stress mediates tau-induced neurodegeneration in Drosophila. J Clin Invest 117: 236-245.
56. Steinhilb ML, Dias-Santagata D, Fulga TA, Felch DL, Feany MB, (2007) Tau phosphorylation sites work in concert to promote neurotoxicity in vivo. Mol Biol Cell 18: 5060-5068.
57. Steinhilb ML, Dias-Santagata D, Mulkearns EE, Shulman JM, Biernat J, et al. (2007) S/P and T/P phosphorylation is critical for tau neurotoxicity in Drosophila. J Neurosci Res 85: 1271-1278.
58. Feuillette S, Miguel L, Frebourg T, Campion D, Lecourtois M, (2010) Drosophila models of human tauopathies indicate that Tau protein toxicity in vivo is mediated by soluble cytosolic phosphorylated forms of the protein. J Neurochem 113: 895-903.
59. Iijima-Ando K, Zhao L, Gatt A, Shenton C, Iijima K, (2010) A DNA damage-activated checkpoint kinase phosphorylates tau and enhances tau-induced neurodegeneration. Hum Mol Genet 19: 1930-1938.
60. Mittoo S, Sundstrom LE, Bradley M, (2003) Synthesis and evaluation of fluorescent probes for the detection of calpain activity. Anal Biochem 319: 234-238.
61. Augustinack JC, Schneider A, Mandelkow EM, Hyman BT, (2002) Specific tau phosphorylation sites correlate with severity of neuronal cytopathology in Alzheimer's disease. Acta Neuropathol (Berl) 103: 26-35.
62. Dickson DW, Crystal HA, Bevona C, Honer W, Vincent I, et al. (1995) Correlations of synaptic and pathological markers with cognition of the elderly. Neurobiol Aging 16: 285-298; discussion 298-304.
63. Kraft R, Levine RB, Restifo LL, (1998) The steroid hormone 20-hydroxyecdysone enhances neurite growth of Drosophila mushroom body neurons isolated during metamorphosis. J Neurosci 18: 8886-8899.