Tau-induced traffic jams reflect organelles accumulation at points of microtubule polar mismatching

Traffic

Volumn 9, Issue 4, 2008, Pages 458-471

  Shemesh, Or A ^a   Erez, Hadas ^a   Ginzburg, Irith ^b   Spira, Micha E ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

Alzheimer's disease; Aplysia; Axonal transport; Microtubule polarity; Microtubules; Tau; Tauopathy

Indexed keywords

MEMBRANE PROTEIN; MICROTUBULE PROTEIN; TAU PROTEIN;

AMINO ACID SEQUENCE; ANIMAL CELL; APLYSIA; ARTICLE; CELL ORGANELLE; CONTROLLED STUDY; DEPOLYMERIZATION; GENE OVEREXPRESSION; MICROTUBULE ASSEMBLY; MOLECULAR MECHANICS; NERVE CELL CULTURE; NERVE DEGENERATION; NERVE FIBER TRANSPORT; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENESIS; POLARIZATION; PRIORITY JOURNAL; PROTEIN DOMAIN; RETROGRADE NERVE FIBER TRANSPORT;

ANIMALS; APLYSIA; BIOLOGICAL TRANSPORT; CELLS, CULTURED; HUMANS; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; MOLECULAR SEQUENCE DATA; NEURONS; ORGANELLES; PHENOTYPE; RECOMBINANT FUSION PROTEINS; TAU PROTEINS;

EID: 40449093880     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2007.00695.x     Document Type: Article

References (55)

1. Baas PW, Qiang L. Neuronal microtubules: When the MAP is the roadblock. Trends Cell Biol 2005; 15: 183-187.
2. Goedert M, Jakes R. Mutations causing neurodegenerative tauopathies. Biochim Biophys Acta 2005; 1739: 240-250.
3. Buee L, Bussiere T, Buee-Scherrer V, Delacourte A, Hof PR. Tau protein isoforms, phosphorylation and role in neurodegenerative disorders. Brain Res Brain Res Rev 2000; 33: 95-130.
4. Feinstein SC, Wilson L. Inability of tau to properly regulate neuronal microtubule dynamics: A loss-of-function mechanism by which tau might mediate neuronal cell death. Biochim Biophys Acta 2005; 1739: 268-279.
5. Thies E, Mandelkow EM. Missorting of tau in neurons causes degeneration of synapses that can be rescued by the kinase MARK2/Par-1. J Neurosci 2007; 27: 2896-2907.
6. Ballatore C, Lee VM, Trojanowski JQ. Tau-mediated neurodegeneration in Alzheimer's disease and related disorders. Nat Rev Neurosci 2007; 8: 663-672.
7. Shaw LM, Korecka M, Clark CM, Lee VM, Trojanowski JQ. Biomarkers of neurodegeneration for diagnosis and monitoring therapeutics. Nat Rev Drug Discov 2007; 6: 295-303.
8. Gotz J, Deters N, Doldissen A, Bokhari L, Ke Y, Wiesner A, Schonrock N, Ittner LM. A decade of tau transgenic animal models and beyond. Brain Pathol 2007; 17: 91-103.
9. Seitz A, Kojima H, Oiwa K, Mandelkow EM, Song YH, Mandelkow E. Single-molecule investigation of the interference between kinesin, tau and MAP2c. EMBO J 2002; 21: 4896-4905.
10. McNally KP, Buster D, McNally FJ. Katanin-mediated microtubule severing can be regulated by multiple mechanisms. Cell Motil Cytoskeleton 2002; 53: 337-349.
11. Ahmad FJ, Yu W, McNally FJ, Baas PW. An essential role for katanin in severing microtubules in the neuron. J Cell Biol 1999; 145: 305-315.
12. Quarmby L. Cellular Samurai: Katanin and the severing of microtubules. J Cell Sci 2000; 113: 2821-2827.
13. Evans KJ, Gomes ER, Reisenweber SM, Gundersen GG, Lauring BP. Linking axonal degeneration to microtubule remodeling by Spastin-mediated microtubule severing. J Cell Biol 2005; 168: 599-606.
14. Qiang L, Yu W, Andreadis A, Luo M, Baas PW. Tau protects microtubules in the axon from severing by katanin. J Neurosci 2006; 26: 3120-3129.
15. Mandelkow EM, Mandelkow E. Tau in Alzheimer's disease. Trends Cell Biol 1998; 8: 425-427.
16. Ebneth A, Godemann R, Stamer K, Illenberger S, Trinczek B, Mandelkow E. 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.
17. Mandelkow EM, Stamer K, Vogel R, Thies E, Mandelkow E. Clogging of axons by tau, inhibition of axonal traffic and starvation of synapses. Neurobiol Aging 2003; 24: 1079-1085.
18. Stamer K, Vogel R, Thies E, Mandelkow E, Mandelkow EM. Tau blocks traffic of organelles, neurofilaments, and APP vesicles in neurons and enhances oxidative stress. J Cell Biol 2002; 156: 1051-1063.
19. Wittmann CW, Wszolek MF, Shulman JM, Salvaterra PM, Lewis J, Hutton M, Feany MB. Tauopathy in Drosophila: Neurodegeneration without neurofibrillary tangles. Science 2001; 293: 711-714.
20. Moroz LL, Edwards JR, Puthanveettil SV, Kohn AB, Ha T, Heyland A, Knudsen B, Sahni A, Yu F, Liu L, Jezzini S, Lovell P, Iannucculli W, Chen M, Nguyen T et al. Neuronal transcriptome of Aplysia: Neuronal compartments and circuitry. Cell 2006; 127: 1453-1467.
21. Cambiazo V, Gonzalez M, Maccioni RB. DMAP-85: A tau-like protein from Drosophila melanogaster larvae. J Neurochem 1995; 64: 1288-1297.
22. Goedert M, Baur CP, Ahringer J, Jakes R, Hasegawa M, Spillantini MG, Smith MJ, Hill F. PTL-1, a microtubule-associated protein with tau-like repeats from the nematode Caenorhabditis elegans. J Cell Sci 1996; 109: 2661-2672.
23. Dehmelt L, Halpain S. The MAP2/Tau family of microtubule-associated proteins. Genome Biol 2005; 6: 204.
24. Akhmanova A, Hoogenraad CC. Microtubule plus-end-tracking proteins: mechanisms and functions. Curr Opin Cell Biol 2005; 17: 47-54.
25. Stepanova T, Slemmer J, Hoogenraad CC, Lansbergen G, Dortland B, De Zeeuw CI, Grosveld F, van Cappellen G, Akhmanova A, Galjart N. Visualization of microtubule growth in cultured neurons via the use of EB3-GFP (end-binding protein 3-green fluorescent protein). J Neurosci 2003; 23: 2655-2664.
26. Ahmad FJ, He Y, Myers KA, Hasaka TP, Francis F, Black MM, Baas PW. Effects of dynactin disruption and dynein depletion on axonal microtubules. Traffic 2006; 7: 524-537.
27. Spira ME, Oren R, Dormann A, Gitler D. Critical calpain-dependent ultrastructural alterations underlie the transformation of an axonal segment into a growth cone after axotomy of cultured Aplysia neurons. J Comp Neurol 2003; 457: 293-312.
28. Sahly I, Khoutorsky A, Erez H, Prager-Khoutorsky M, Spira ME. On-line confocal imaging of the events leading to structural dedifferentiation of an axonal segment into a growth cone after axotomy. J Comp Neurol 2006; 494: 705-720.
29. Teng H, Cole JC, Roberts RL, Wilkinson RS. Endocytic active zones: Hot spots for endocytosis in vertebrate neuromuscular terminals. J Neurosci 1999; 19: 4855-4866.
30. Shaner NC, Campbell RE, Steinbach PA, Giepmans BN, Palmer AE, Tsien RY. Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat Biotechnol 2004; 22: 1567-1572.
31. Oyler GA, Higgins GA, Hart RA, Battenberg E, Billingsley M, Bloom FE, Wilson MC. The identification of a novel synaptosomal-associated protein, SNAP-25, differentially expressed by neuronal subpopulations. J Cell Biol 1989; 109: 3039-3052.
32. Kimura K, Mizoguchi A, Ide C. Regulation of growth cone extension by SNARE proteins. J Histochem Cytochem 2003; 51: 429-433.
33. Sankaranarayanan S, De Angelis D, Rothman JE, Ryan TA. The use of pHluorins for optical measurements of presynaptic activity. Biophys J 2000; 79: 2199-2208.
34. Erez H, Malkinson G, Prager-Khoutorsky M, De Zeeuw CI, Hoogenraad CC, Spira ME. Formation of microtubule-based traps controls the sorting and concentration of vesicles to restricted sites of regenerating neurons after axotomy. J Cell Biol 2007; 176: 497-507.
35. Kraemer BC, Zhang B, Leverenz JB, Thomas JH, Trojanowski JQ, Schellenberg GD. Neurodegeneration and defective neurotransmission in a Caenorhabditis elegans model of tauopathy. Proc Natl Acad Sci U S A 2003; 100: 9980-9985.
36. Jackson GR, Wiedau-Pazos M, Sang TK, Wagle N, Brown CA, Massachi S, Geschwind DH. Human wild-type tau interacts with wingless pathway components and produces neurofibrillary pathology in Drosophila. Neuron 2002; 34: 509-519.
37. Drechsel DN, Hyman AA, Cobb MH, Kirschner MW. Modulation of the dynamic instability of tubulin assembly by the microtubule-associated protein tau. Mol Biol Cell 1992; 3: 1141-1154.
38. Kanai Y, Chen J, Hirokawa N. Microtubule bundling by tau proteins in vivo: Analysis of functional domains. EMBO J 1992;11: 3953-3961.
39. Panda D, Miller HP, Wilson L. Rapid treadmilling of brain microtubules free of microtubule-associated proteins in vitro and its suppression by tau. Proc Natl Acad Sci U S A 1999; 96: 12459-12464.
40. Brandt R, Leger J, Lee G. Interaction of tau with the neural plasma membrane mediated by tau's amino-terminal projection domain. J Cell Biol 1995; 131: 1327-1340.
41. Lee G, Newman ST, Gard DL, Band H, Panchamoorthy G. Tau interacts with src-family non-receptor tyrosine kinases. J Cell Sci 1998; 111: 3167-3177.
42. Cytrynbaum EN, Rodionov V, Mogilner A. Nonlocal mechanism of self-organization and centering of microtubule asters. Bull Math Biol 2006; 68: 1053-1072.
43. Malikov V, Cytrynbaum EN, Kashina A, Mogilner A, Rodionov V. Centering of a radial microtubule array by translocation along microtubules spontaneously nucleated in the cytoplasm. Nat Cell Biol 2005; 7: 1113-1118.
44. Stokin GB, Lillo C, Falzone TL, Brusch RG, Rockenstein E, Mount SL, Raman R, Davies P, Masliah E, Williams DS, Goldstein LS. Axonopathy and transport deficits early in the pathogenesis of Alzheimer's disease. Science 2005; 307: 1282-1288.
45. Schacher S, Proshansky E. Neurite regeneration by Aplysia neurons in dissociated cell culture: Modulation by Aplysia hemolymph and the presence of the initial axonal segment. J Neurosci 1983; 3: 2403-2413.
46. Spira ME, Dormann A, Ashery U, Gabso M, Gitler D, Benbassat D, Oren R, Ziv NE. Use of Aplysia neurons for the study of cellular alterations and the resealing of transected axons in vitro. J Neurosci Methods 1996; 69: 91-102.
47. Sahly I, Erez H, Khoutorsky A, Shapira E, Spira ME. Effective expression of the green fluorescent fusion proteins in cultured Aplysia neurons. J Neurosci Methods 2003; 126: 111-117.
48. Nakagawa H, Koyama K, Murata Y, Morito M, Akiyama T, Nakamura Y. EB3, a novel member of the EB1 family preferentially expressed in the central nervous system, binds to a CNS-specific APC homologue. Oncogene 2000; 19: 210-216.
49. Rizzini C, Goedert M, Hodges JR, Smith MJ, Jakes R, Hills R, Xuereb JH, Crowther RA, Spillantini MG. Tau gene mutation K257T causes a tauopathy similar to Pick's disease. J Neuropathol Exp Neurol 2000; 59: 990-1001.
50. Goedert M, Jakes R, Crowther RA. Effects of frontotemporal dementia FTDP-17 mutations on heparin-induced assembly of tau filaments. FEBS Lett 1999; 450: 306-311.
51. Bugiani O, Murrell JR, Giaccone G, Hasegawa M, Ghigo G, Tabaton M, Morbin M, Primavera A, Carella F, Solaro C, Grisoli M, Savoiardo M, Spillantini MG, Tagliavini F, Goedert M et al. Frontotemporal dementia and corticobasal degeneration in a family with a P301S mutation in tau. J Neuropathol Exp Neurol 1999; 58: 667-677.
52. Weingarten MD, Lockwood AH, Hwo SY, Kirschner MW. A protein factor essential for microtubule assembly. Proc Natl Acad Sci U S A 1975; 72: 1858-1862.
53. Kim H, Binder LI, Rosenbaum JL. The periodic association of MAP2 with brain microtubules in vitro. J Cell Biol 1979; 80: 266-276.
54. Gitler D, Spira ME. Real time imaging of calcium-induced localized proteolytic activity after axotomy and its relation to growth cone formation. Neuron 1998; 20: 1123-1135.
55. Malkinson G, Fridman ZM, Kamber D, Dormann A, Shapira E, Spira ME. Calcium-induced exocytosis from actomyosin-driven, motile varicosities formed by dynamic clusters of organelles. Brain Cell Biol 2006; 35: 57-73.