Increased association between rough endoplasmic reticulum membranes and mitochondria in transgenic mice that express P301L tau

Journal of Neuropathology and Experimental Neurology

Volumn 68, Issue 5, 2009, Pages 503-514

  Perreault, Sébastien ^a   Bousquet, Olivier ^a   Lauzon, Michel ^a   Paiement, Jacques ^a   Leclerc, Nicole ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Alzheimer disease; Microtubule associated protein tau; Mitochondria; Neurodegeneration; P301L; Rough endoplasmic reticulum

Indexed keywords

RIBOPHORIN I; TAU PROTEIN; TAU PROTEIN P301L; UNCLASSIFIED DRUG; KDEL RECEPTOR; LEUCINE; MICROTUBULE ASSOCIATED PROTEIN; MONOCLONAL ANTIBODY; MTAP2 PROTEIN, MOUSE; PHF 1; PHF-1; PROLINE; RECEPTOR; SYNTAXIN;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ARTICLE; BRAIN; CELL CONTACT; CELL FRACTIONATION; CELL SURFACE; CONTROLLED STUDY; GENE OVEREXPRESSION; IMMUNOGOLD LABELING; MICROSOME; MITOCHONDRION; MOTONEURON; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; ROUGH ENDOPLASMIC RETICULUM; SOMATIC CELL; WILD TYPE; AGED; ANIMAL; FEMALE; GENETICS; HUMAN; IMMUNOELECTRON MICROSCOPY; MALE; METABOLISM; METHODOLOGY; MUTATION; PATHOLOGY; SPINAL CORD; TRANSGENIC MOUSE; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; ANIMALS; ANTIBODIES, MONOCLONAL; BRAIN; ENDOPLASMIC RETICULUM, ROUGH; FEMALE; HUMANS; LEUCINE; MALE; MICE; MICE, TRANSGENIC; MICROSCOPY, ELECTRON, TRANSMISSION; MICROSCOPY, IMMUNOELECTRON; MICROTUBULE-ASSOCIATED PROTEINS; MITOCHONDRIA; MUTATION; PROLINE; QA-SNARE PROTEINS; RECEPTORS, PEPTIDE; SPINAL CORD; SUBCELLULAR FRACTIONS; TAU PROTEINS;

EID: 70149098692     PISSN: 00223069     EISSN: None     Source Type: Journal    
DOI: 10.1097/NEN.0b013e3181a1fc49     Document Type: Article

References (70)

1. Chesselet M. Molecular Mechanisms of Neurodegenerative Diseases. Totowa, NJ: Human Press, 2000
2. Alafuzoff I, Iqbal K, Friden H, et al. Histopathological criteria for progressive dementia disorders: Clinical-pathological correlation and classification by multivariate data analysis. Acta Neuropathol 1987:74; 209-225
3. Arriagada P, Growdon J, Hedley-Whyte ET, et al. Neurofibrillary tangles but not senile plaques parallel duration and severity of Alzheimer's disease. Neurology 1992:42;631-639
4. Bierer L, Hof P, Purohit D, et al. Neocortical neurofibrillary tangles correlate with dementia severity in Alzheimer's disease. Arch Neurol 1995:52;81-88
5. Braak H, Braak E. Neuropathological staging of Alzheimer-related changes. Acta Neuropathol 1991:82;239-259
6. Tomlinson BE, Blessed G, Roth M. Observations on the brains of demented old people. J Neurol Sci 1970:11;205-242
7. Mandell J, Banker G. Microtubule-associated proteins, phosphorylation gradients, and the establishment of neuronal polarity. Perspect Dev Neurobiol 1996:4;125-135
8. Grundke-Iqbal I, Iqbal K, Quinlan M, et al. Microtubule-associated protein tau. A component of Alzheimer paired helical filaments. J Biol Chem 1986:261;6084-6089
9. Lee V, Goedert M, Trojanowski J. Neurodegenerative tauopathies. Annu Rev Neurosci 2001:24;1121-1159
10. Grundke-Iqbal I, Iqbal K, Tung Y, et al. Abnormal phosphorylation of the microtubule-associated protein tau (tau) in Alzheimer cytoskeletal pathology. Proc Natnl Acad Sci U S A 1986:83;4913-4917
11. Cairns NJ, Bigio EH, Mackenzie IR, et al. Neuropathologic diagnostic and nosologic criteria for frontotemporal lobar degeneration: Consensus of the Consortium for Frontotemporal Lobar Degeneration. Acta Neuropathol 2007:114;5-22
12. Hutton M, Lendon CL, Rizzu P, et al. Association of missense and 5′-splice-site mutations in tau with the inherited dementia FTDP-17. Nature 1998:393;702-705
13. Poorkaj P, Bird TD, Wijsman E, et al. Tau is a candidate gene for chromosome 17 frontotemporal dementia. Ann Neurol 1998:43;815-825
14. Duff K, Knight H, Refolo L, et al. Characterization of pathology in transgenic mice over-expressing human genomic and cDNA tau transgenes. Neurobiol Dis 2000:7;87-98
15. Probst A, Götz J, Wiederhold K, et al. Axonopathy and amyotrophy in mice transgenic for human four-repeat tau protein. Acta Neuropathol 2000:99;469-481
16. Spittaels K, Van den Haute C, Van Dorpe J, et al. Prominent axonopathy in the brain and spinal cord of transgenic mice overexpressing four-repeat human tau protein. Am J Pathol 1999:155;2153-2165
17. Ishihara T, Hong M, Zhang B, et al. Age-dependent emergence and progression of a tauopathy in transgenic mice overexpressing the shortest human tau isoform. Neuron 1999:24;751-762
18. Tatebayashi Y, Miyasaka T, Chui DH, et al. Tau filament formation and associative memory deficit in aged mice expressing mutant (R406W) human tau. Proc Natl Acad Sci U S A 2002:99;13896-13901
19. Lewis J, McGowan E, Rockwood J, et al. Neurofibrillary tangles, amyotrophy and progressive motor disturbance in mice expressing mutant (P301L) tau protein. Nat Genet 2000:25;402-405
20. Hutton M. Missense and splice site mutations in tau associated with FTDP-17: Multiple pathogenic mechanisms. Neurology 2001:56; S21-25
21. Papasozomenos S, Binder L. Phosphorylation determines two distinct species of tau in the central nervous system. Cell Motil Cytoskeleton 1987:8;210-226
22. de Ancos J, Avila J. Differential distribution in white and grey matter of tau phosphoisoforms containing four tubulin-binding motifs. Biochem J 1993:296(Pt 2);351-54
23. Farah C, Perreault S, Liazoghli D, et al. Tau interacts with Golgi membranes and mediates their association with microtubules. Cell Motil Cytoskeleton 2006:63;710-724
24. Arendt T, Stieler J, Strijkstra A, et al. Reversible paired helical filament-like phosphorylation of tau is an adaptive process associated with neuronal plasticity in hibernating animals. J Neurosci 2003:23; 6972-6981
25. Gray E, Paula-Barbosa M, Roher A. Alzheimer's disease: Paired helical filaments and cytomembranes. Neuropathol Appl Neurobiol 1987:13; 91-110
26. Stieber A, Mourelatos Z, Gonatas NK. In Alzheimer's disease the Golgi apparatus of a population of neurons without neurofibrillary tangles is fragmented and atrophic. Am J Pathol 1996:148;415-426
27. Metuzals J, Robitaille Y, Houghton S, et al. Paired helical filaments and the cytoplasmic-nuclear interface in Alzheimer's disease. J Neurocytol 1988:17;827-833
28. Liazoghli D, Perreault S, Micheva K, et al. Fragmentation of the Golgi apparatus induced by the overexpression of wild-type and mutant human tau forms in neurons. Am J Pathol 2005:166;1499-1514
29. Yoshiyama Y, Higuchi M, Zhang B, et al. Synapse loss and microglial activation precede tangles in a P301S tauopathy mouse model. Neuron 2007:53;337-351
30. Lin W, Lewis J, Yen S, et al. Ultrastructural neuronal pathology in transgenic mice expressing mutant (P301L) human tau. J Neurocytol 2003:32;1091-1105
31. Hall GF, Chu B, Lee G, et al. Human tau filaments induce microtubule and synapse loss in an in vivo model of neurofibrillary degenerative disease. J Cell Sci 2000:113;1373-1387
32. Wittmann C, Wszolek M, Shulman J, et al. Tauopathy in Drosophila: Neurodegeneration without neurofibrillary tangles. Science 2001:293; 711-714
33. Santacruz K, Lewis J, Spires T, et al. Tau suppression in a neurodegenerative mouse model improves memory function. Science 2005: 309;476-481
34. Alonso Adel C, Li B, Grundke-Iqbal I, et al. Polymerization of hyperphosphorylated tau into filaments eliminates its inhibitory activity. Proc Natl Acad Sci U S A 2006:103;8864-8869
35. Li B, Chohan MO, Grundke-Iqbal I, et al. Disruption of microtubule network by Alzheimer abnormally hyperphosphorylated tau. Acta Neuropathol 2007:113;501-511
36. Micheva K, Vallée A, Beaulieu C, et al. beta-Actin is confined to structures having high capacity of remodelling in developing and adult rat cerebellum. Eur J Neurosci 1998:10;3785-3798
37. Garver TD, Harris KA, Lehman RA, et al. Tau phosphorylation in human, primate, and rat brain: Evidence that a pool of tau is highly phosphorylated in vivo and is rapidly dephosphorylated in vitro. J Neurochem 1994:63;2279-2287
38. Lavoie C, Lanoix J, Kan FW, et al. Cell-free assembly of rough and smooth endoplasmic reticulum. J Cell Sci 1996:109;1415-1425
39. Farah C, Liazoghli D, Perreault S, et al. Interaction of microtubule-associated protein-2 and p63: A new link between microtubules and rough endoplasmic reticulum membranes in neurons. J Biol Chem 2005:280; 9439-9449
40. Baudhuin P, Evrard P, Berthet J. Electron microscopic examination of subcellular fractions. I. The preparation of representative samples from suspensions of particles. J Cell Biol 1967:32;181-191
41. Perkins G, Renken C, Martone ME, et al. Electron tomography of neuronal mitochondria: Three-dimensional structure and organization of cristae and membrane contacts. J Struct Biol 1997:119;260-272
42. Wang HJ, Guay G, Pogan L, et al. Calcium regulates the association between mitochondria and a smooth subdomain of the endoplasmic reticulum. J Cell Biol 2000:150;1489-1498
43. Ebneth A, Godemann R, Stamer K, et al. Overexpression of tau protein inhibits kinesin-dependent trafficking of vesicles, mitochondria and endoplasmic reticulum: Implications for Alzheimer's disease. J Cell Biol 1998:143;777-794
44. David DC, Hauptmann S, Scherping I, et al. Proteomic and functional analyses reveal a mitochondrial dysfunction in P301L tau transgenic mice. J Biol Chem 2005:280;23802-23814
45. Peters A, Palay S, Webster H. The Fine Structure of the Nervous System: The Neurons and Supporting Cells. Philadelphia, PA: Saunders Company, 1976
46. Rambourg A, Clermont Y. Three-dimensional electron microscopy: Structure of the Golgi apparatus. Eur J Cell Biol 1990:51;189-200
47. Marsh B, Mastonarde D, Buttle K, et al. Organellar relationships in the Golgi region of the pancreatic beta cell line, HIT-115, visualized by high resolution electron tomography. Proc Natl Acad Sci U S A 2001:98; 2399-2406
48. Bard F, Mazelin L, Pechoux-Longin C, et al. Src regulates Golgi structure and KDEL receptorYdependent retrograde transport to the endoplasmic reticulum. J Biol Chem 2003:278;46601-46606
49. Iqbal K, Grundke-Iqbal I, Zaidi T, et al. Defective brain microtubule assembly in Alzheimer's disease. Lancet 1986:2;421-426
50. Rizzuto R, Pinton P, Carrington W, et al. Close contacts with the endoplasmic reticulum as determinants of mitochondrial Ca2+ responses. Science 1998:280;1763-1766
51. Goetz JG, Nabi IR. Interaction of the smooth endoplasmic reticulum and mitochondria. Biochem Soc Trans 2006:34;370-373
52. Walter L, Hajnoczky G. Mitochondria and endoplasmic reticulum: The lethal interorganelle cross-talk. J Bioenerg Biomembr 2005:37; 191-206
53. de Brito OM, Scorrano L. Mitofusin 2 tethers endoplasmic reticulum to mitochondria. Nature 2008:456;605-610
54. Zuchner S, Mersiyanova IV, Muglia M, et al. Mutations in the mitochondrial GTPase mitofusin 2 cause Charcot-Marie-Tooth neuropathy type 2A. Nat Genet 2004:36;449-451
55. Vance JE. Phospholipid synthesis in a membrane fraction associated with mitochondria. J Biol Chem 1990:265;7248-7256
56. Hayashi T, Su TP. Sigma-1 receptor chaperones at the ER-mitochondrion interface regulate Ca(2+) signaling and cell survival. Cell 2007:131; 596-610
57. Berridge MJ. The endoplasmic reticulum: A multifunctional signaling organelle. Cell Calcium 2002:32;235-249
58. Mironov S, Ivannikov M, Johansson M. Ca2+i signaling between mitochondria and endoplasmic reticulum in neurons is regulated by microtubules. J Biol Chem 2005:280;715-721
59. Darios F, Muriel MP, Khondiker ME, et al. Neurotoxic calcium transfer from endoplasmic reticulum to mitochondria is regulated by cyclin-dependent kinase 5Ydependent phosphorylation of tau. J Neurosci 2005:25; 4159-4168
60. Karsten SL, Sang TK, Gehman LT, et al. A genomic screen for modifiers of tauopathy identifies puromycin-sensitive aminopeptidase as an inhibitor of tau-induced neurodegeneration. Neuron 2006:51; 549-560
61. Furukawa K, D'Souza I, Crudder CH, et al. Pro-apoptotic effects of tau mutations in chromosome 17 frontotemporal dementia and parkinsonism. Neuroreport 2000:11;57-60
62. Furukawa K, Wang Y, Yao PJ, et al. Alteration in calcium channel properties is responsible for the neurotoxic action of a familial frontotemporal dementia tau mutation. J Neurochem 2003:87;427-436
63. Christensen RA, Shtifman A, Allen PD, et al. Calcium dyshomeostasis in beta-amyloid and tau-bearing skeletal myotubes. J Biol Chem 2004: 279;53524-53532
64. Takuma K, Yan SS, Stern DM, et al. Mitochondrial dysfunction, endoplasmic reticulum stress, and apoptosis in Alzheimer's disease. J Pharmacol Sci 2005:97;312-316
65. Sheffield LG, Miskiewicz HB, Tannenbaum LB, et al. Nuclear pore complex proteins in Alzheimer disease. J Neuropathol Exp Neurol 2006: 65;45-54
66. Kopke E, Tung YC, Shaikh S, et al. Microtubule-associated protein tau. Abnormal phosphorylation of a non-paired helical filament pool in Alzheimer disease. J Biol Chem 1993:268;24374-24384
67. Wang JZ, Grundke-Iqbal I, Iqbal K. Glycosylation of microtubule- associated protein tau: An abnormal posttranslational modification in Alzheimer's disease. Nat Med 1996:2;871-875
68. Luna-Munoz J, Garcia-Sierra F, Falcon V, et al. Regional conformational change involving phosphorylation of tau protein at the Thr231, precedes the structural change detected by Alz-50 antibody in Alzheimer's disease. J Alzheimers Dis 2005:8;29-41
69. Escobar-Khondiker M, Hollerhage M, Muriel MP, et al. Annonacin, a natural mitochondrial complex I inhibitor, causes tau pathology in cultured neurons. J Neurosci 2007:27;7827-7837
70. Moreira PI, Santos MS, Oliveira CR. Alzheimer's disease: A lesson from mitochondrial dysfunction. Antioxid Redox Signal 2007:9; 1621-30