Neurotoxic calcium transfer from endoplasmic reticulum to mitochondria is regulated by cyclin-dependent kinase 5-dependent phosphorylation of tau

Journal of Neuroscience

Volumn 25, Issue 16, 2005, Pages 4159-4168

  Darios, Frédéric ^a,b   Muriel, Marie Paule ^a   Khondiker, Myriam Escobar ^a   Brice, Alexis ^a   Ruberg, Merle ^a  

^a PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^b MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

Apoptosis; Centrosome; Clustering; Microtubule; Phosphorylation; Tau

Indexed keywords

ALANINE; CALCIUM; CERAMIDE; CYCLIN DEPENDENT KINASE 5; CYCLIN DEPENDENT KINASE INHIBITOR; PROTEIN BCL 2; PROTEIN BID; ROSCOVITINE; TAU PROTEIN; THREONINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; CELL CULTURE; CELL DEATH; CELL ORGANELLE; CELL STRAIN; CENTROSOME; CONTROLLED STUDY; ELECTRON MICROSCOPY; EMBRYO; ENDOPLASMIC RETICULUM; FEMALE; FLUORESCENCE; IMMUNOCYTOCHEMISTRY; MICROTUBULE; MITOCHONDRION; NERVE CELL; NEUROTOXICITY; NONHUMAN; PHOSPHORYLATION; PRIORITY JOURNAL; RAT;

ANALYSIS OF VARIANCE; ANIMALS; BLOTTING, WESTERN; CALCIUM; CELL COUNT; CELL DEATH; CELLS, CULTURED; CERAMIDES; CLONING, MOLECULAR; CYCLIN-DEPENDENT KINASE 5; CYTOCHALASIN D; DRUG INTERACTIONS; EMBRYO; ENDOPLASMIC RETICULUM; ENZYME ACTIVATION; ENZYME INHIBITORS; FEMALE; GENE EXPRESSION REGULATION; HETEROCYCLIC COMPOUNDS, 3-RING; IMMUNOHISTOCHEMISTRY; MALE; MESENCEPHALON; MICROSCOPY, ELECTRON, TRANSMISSION; MITOCHONDRIA; NEURONS; NOCODAZOLE; PHOSPHORYLATION; PREGNANCY; PURINES; RATS; RATS, WISTAR; TAU PROTEINS; TIME FACTORS; TRANSFECTION; TUBULIN;

EID: 17644397819     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0060-05.2005     Document Type: Article

References (54)

1. Ahlijanian MK, Barrezueta NX, Williams RD, Jakowski A, Kowsz KP, McCarthy S, Coskran T, Carlo A, Seymour PA, Burkhardt JE, Nelson RB, McNeish JD (2000) Hyperphosphorylated tau and neurofilament and cytoskeletal disruptions in mice overexpressing human p25, an activator of cdk5. Proc Natl Acad Sci USA 97:2910-2915.
2. Baumann K, Mandelkow EM, Biernat J, Piwnica-Worms H, Mandelkow E (1993) Abnormal Alzheimer-like phosphorylation of tau-protein by cyclin-dependent kinases cdk2 and cdk5. FEBS Lett 336:417-424.
3. Biernat J, Wu YZ, Timm T, Zheng-Fischhofer Q, Mandelkow E, Meijer L, Mandelkow EM (2002) Protein kinase MARK/PAR-1 is required for neurite outgrowth and establishment of neuronal polarity. Mol Biol Cell 13:4013-4028.
4. Brugg B, Michel PP, Agid Y, Ruberg M (1996) Ceramide induces apoptosis in cultured mesencephalic neurons. J Neurochem 66:733-739.
5. Buee L, Bussiere T, Buee-Scherrer V, Delacourte A, Hof PR (2000) Tau protein isoforms, phosphorylation and role in neurodegenerative disorders. Brain Res Brain Res Rev 33:95-130.
6. Cho JH, Johnson GV (2004) Primed phosphorylation of tau at Thr231 by glycogen synthase kinase 3beta (GSK3beta) plays a critical role in regulating tau's ability to bind and stabilize microtubules. J Neurochem 88:349-358.
7. Csordas G, Thomas AP, Hajnoczky G (1999) Quasi-synaptic calcium signal transmission between endoplasmic reticulum and mitochondria. EMBO J 18:96-108.
8. 2+ permeation through the outer mitochondrial membrane. EMBO J 21:2198-2206.
9. Darios F, Lambeng N, Troadec JD, Michel PP, Ruberg M (2003) Ceramide increases mitochondrial free calcium levels via caspase 8 and Bid: role in initiation of cell death. J Neurochem 84:643-654.
10. Delobel P, Mailliot C, Hamdane M, Sambo AV, Begard S, Violleau A, Delacourte A, Buee L (2003) Stable-tau overexpression in human neuroblastoma cells: an open door for explaining neuronal death in tauopathies. Ann NY Acad Sci 1010:623-634.
11. Drechsel DN, Hyman AA, Cobb MH, Kirschner MW (1992) Modulation of the dynamic instability of tubulin assembly by the microtubule-associated protein tau. Mol Biol Cell 3:1141-1154.
12. Duchen MR (2000) Mitochondria and calcium: from cell signalling to cell death. J Physiol (Lond) 529:57-68.
13. Ebneth A, Godemann R, Stamer K, Illenberger S, Trinczek B, Mandelkow E (1998) Overexpression of tau protein inhibits kinesin-dependent trafficking of vesicles, mitochondria, and endoplasmic reticulum: implications for Alzheimer's disease. J Cell Biol 143:777-794.
14. Eskes R, Desagher S, Antonsson B, Martinou JC (2000) Bid induces the oligomerization and insertion of Bax into the outer mitochondrial membrane. Mol Cell Biol 20:929-935.
15. Hajnoczky G, Robb-Gaspers LD, Seitz MB, Thomas AP (1995) Decoding of cytosolic calcium oscillations in the mitochondria. Cell 82:415-424.
16. 2+ signalling between sarco-endoplasmic reticulum and mitochondria. J Physiol (Lond) 529:69-81.
17. Hamdane M, Sambo AV, Delobel P, Begard S, Violleau A, Delacourte A, Bertrand P, Benavides J, Buee L (2003) Mitotic-like tau phosphorylation by p25-Cdk5 kinase complex. J Biol Chem 278:34026-34034.
18. Hetman M, Cavanaugh JE, Kimelman D, Xia Z (2000) Role of glycogen synthase kinase-3beta in neuronal apoptosis induced by trophic withdrawal. J Neurosci 20:2567-2574.
19. Illenberger S, Zheng-Fischhofer Q, Preuss U, Stamer K, Baumann K, Trinczek B, Biernat J, Godemann R, Mandelkow EM, Mandelkow E (1998) The endogenous and cell cycle-dependent phosphorylation of tau protein in living cells: implications for Alzheimer's disease. Mol Biol Cell 9:1495-1512.
20. Mandelkow EM, Thies E, Trinczek B, Biernat J, Mandelkow E (2004) MARK/PAR1 kinase is a regulator of microtubule-dependent transport in axons. J Cell Biol 167:99-110.
21. Muriel MP, Lambeng N, Darios F, Michel PP, Hirsch EC, Agid Y, Ruberg M (2000) Mitochondrial free calcium levels (Rhod-2 fluorescence) and ultrastructural alterations in neuronally differentiated PC12 cells during ceramide-dependent cell death. J Comp Neurol 426:297-315.
22. Niethammer M, Smith DS, Ayala R, Peng J, Ko J, Lee MS, Morabito M, Tsai LH (2000) NUDEL is a novel Cdk5 substrate that associates with LIS1 and cytoplasmic dynein. Neuron 28:697-711.
23. Nikolic M, Dudek H, Kwon YT, Ramos YF, Tsai LH (1996) The cdk5/p35 kinase is essential for neurite outgrowth during neuronal differentiation. Genes Dev 10:816-825.
24. 2+ stores. J Biol Chem 277:9219-9225.
25. 2+mobilization promotes cytochrome c release during apoptosis. J Biol Chem 277:20301-20308.
26. Pacher P, Csordas P, Schneider T, Hajnoczky G (2000) Quantification of calcium signal transmission from sarco-endoplasmic reticulum to the mitochondria. J Physiol (Lond) 529:553-564.
27. Paschen W (2003) Mechanisms of neuronal cell death: diverse roles of calcium in the various subcellular compartments. Cell Calcium 34:305-310.
28. Patrick GN, Zukerberg L, Nikolic M, de la Monte S, Dikkes P, Tsai LH (1999) Conversion of p35 to p25 deregulates Cdk5 activity and promotes neurodegeneration. Nature 402:615-622.
29. 2+ concentration of the endoplasmic reticulum is a key determinant of ceramide-induced apoptosis: significance for the molecular mechanism of Bcl-2 action. EMBO J 20:2690-2701.
30. 2+ microdomains to mitochondria. J Cell Biol 159:613-624.
31. Reynolds IJ, Rintoul GL (2004) Mitochondrial stop and go: signals that regulate organelle movement. Sci STKE 2004:PE46.
32. Rintoul GL, Filiano AJ, Brocard JB, Kress GJ, Reynolds IJ (2003) Glutamate decreases mitochondrial size and movement in primary forebrain neurons. J Neurosci 23:7881-7888.
33. 2+ close to IP3-sensitive channels that are sensed by neighboring mitochondria. Science 262:744-747.
34. 2+ responses. Science 280:1763-1766.
35. Sasaki S, Shionoya A, Ishida M, Gambello MJ, Yingling J, Wynshaw-Boris A, Hirotsune S (2000) A LIS1/NUDEL/cytoplasmic dynein heavy chain complex in the developing and adult nervous system. Neuron 28:681-696.
36. Sato-Harada R, Okabe S, Umeyama T, Kanai Y, Hirokawa N (1996) Microtubule-associated proteins regulate microtubule function as the track for intracellular membrane organelle transports. Cell Struct Funct 21:283-295.
37. Sengupta A, Kabat J, Novak M, Wu Q, Grundke-Iqbal I, Iqbal K (1998) Phosphorylation of tau at both Thr 231 and Ser 262 is required for maximal inhibition of its binding to microtubules. Arch Biochem Biophys 357:299-309.
38. Sergeant N, Delacourte A, Buee L (2005) Tau protein as a differential biomarker of tauopathies. Biochim Biophys Acta 1739:179-197.
39. Simmen T, Asian JE, Blagoveshchenskaya AD, Thomas L, Wan L, Xiang Y, Feliciangeli SF, Hung CH, Crump CM, Thomas G (2005) PACS-2 controls endoplasmic reticulum-mitochondria communication and Bidmediated apoptosis. EMBO J 24:717-729.
40. 2+ entry. EMBO J 21:622-630.
41. Sperber BR, Leight S, Goedert M, Lee VM (1995) Glycogen synthase kinase-3 beta phosphorylates tau protein at multiple sites in intact cells. Neurosci Lett 197:149-153.
42. Stamer K, Vogel R, Thies E, Mandelkow E, Mandelkow EM (2002) Tau blocks traffic of organelles, neurofilaments, and APP vesicles in neurons and enhances oxidative stress. J Cell Biol 156:1051-1063.
43. Stout AK, Raphael HM, Kanterewicz BI, Klann E, Reynolds IJ (1998) Glutamate-induced neuron death requires mitochondrial calcium uptake. Nat Neurosci 1:366-373.
44. Szalai G, Krishnamurthy R, Hajnoczky G (1999) Apoptosis driven by IP(3)-linked mitochondrial calcium signals. EMBO J 18:6349-6361.
45. Takahashi S, Saito T, Hisanaga S, Pant HC, Kulkarni AB (2003) Tau phosphorylation by cyclin-dependent kinase 5/p39 during brain development reduces its affinity for microtubules. J Biol Chem 278:10506-10515.
46. Trinczek B, Ebneth A, Mandelkow EM, Mandelkow E (1999) Tau regulates the attachment/detachment but not the speed of motors in microtubule-dependent transport of single vesicles and organelles. J Cell Sci 112:2355-2367.
47. Tsai LH, Delalle I, Caviness Jr VS, Chae T, Harlow E (1994) p35 is a neural-specific regulatory subunit of cyclin-dependent kinase 5. Nature 371:419-423.
48. 2+ homeostasis and neuronal death. J Cell Mol Med 7:351-361.
49. Wada Y, Ishiguro K, Itoh TJ, Uchida T, Hotani H, Saito T, Kishimoto T, Hisanaga S (1998) Microtubule-stimulated phosphorylation of tau at Ser202 and Thr205 by cdk5 decreases its microtubule nucleation activity. J Biochem (Tokyo) 124:738-746.
50. Wang HJ, Guay G, Pogan L, Sauve R, Nabi IR (2000) Calcium regulates the association between mitochondria and a smooth subdomain of the endoplasmic reticulum. J Cell Biol 150:1489-1498.
51. Wei MC, Lindsten T, Mootha VK, Weiler S, Gross A, Ashiya M, Thompson CB, Korsmeyer SJ (2000) tBID, a membrane-targeted death ligand, oligomerizes BAK to release cytochrome c. Genes Dev 14:2060-2071.
52. Weishaupt JH, Kussmaul L, Grotsch P, Heckel A, Rohde G, Romig H, Bahr M, Gillardon F (2003) Inhibition of CDK5 is protective in necrotic and apoptotic paradigms of neuronal cell death and prevents mitochondrial dysfunction. Mol Cell Neurosci 24:489-502.
53. Yi M, Weaver D, Hajnoczky G (2004) Control of mitochondrial motility and distribution by the calcium signal: a homeostatic circuit. J Cell Biol 167:661-672.
54. Zheng YL, Kesavapany S, Gravell M, Hamilton RS, Schubert M, Amin N, Albers W, Grant P, Pant HC (2005) A Cdk5 inhibitory peptide reduces tau hyperphosphorylation and apoptosis in neurons. EMBO J 24:209-220.