Tau protects microtubules in the axon from severing by katanin

Journal of Neuroscience

Volumn 26, Issue 12, 2006, Pages 3120-3129

  Qiang, Liang ^a   Yu, Wenqian ^a   Andreadis, Athena ^b   Luo, Minhua ^b   Baas, Peter W ^a  

^a DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

Axon; Katanin; MAP1b; Microtubule; Neuron; Tau

Indexed keywords

MICROTUBULE ASSOCIATED PROTEIN 1; MICROTUBULE ASSOCIATED PROTEIN 2; PACLITAXEL; SMALL INTERFERING RNA; TAU PROTEIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DRUG STABILITY; FIBROBLAST; GENETIC TRANSFECTION; MICROTUBULE; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; RAT;

ADENOSINE TRIPHOSPHATASES; ANIMALS; ANTINEOPLASTIC AGENTS, PHYTOGENIC; AXONS; CELL LINE; CELL SHAPE; CELLS, CULTURED; DOWN-REGULATION; FIBROBLASTS; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; NEURONAL PLASTICITY; PACLITAXEL; RATS; RNA INTERFERENCE; TAU PROTEINS; TAUOPATHIES;

EID: 33645221487     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5392-05.2006     Document Type: Article

References (54)

1. Ahmad FJ, Yu W, McNally FJ, Baas PW (1999) An essential role for katanin in severing microtubules in the neuron. J Cell Biol 14:305-315.
2. Baas PW, Ahmad FJ (2001) Force generation by cytoskeletal motor proteins as a regulator of axonal elongation and retraction. Trends Cell Biol 11:244-249.
3. Baas PW, Qiang L (2005) Neuronal microtubules: when the MAP is the roadblock. Trends Cell Biol 15:183-187.
4. Brugg B, Reddy D, Matus A (1993) Attenuation of microtubule-associated protein 1B expression by antisense oligodeoxynucleotides inhibits initiation of neurite outgrowth. Neuroscience 52:489-496.
5. Caceres A, Kosik KS (1990) Inhibition of neurite polarity by tau antisense oligonucleotides in primary cerebellar neurons. Nature 343:461-463.
6. Caceres A, Potrebic S, Kosik KS (1991) The effect of tau antisense oligonucleotides on neurite formation of cultured cerebellar macroneurons. J Neurosci 11:1515-1523.
7. Caceres A, Mautino J, Kosik KS (1992) Supression of MAP2 in cultured cerebellar macroneurons inhibits minor neurite formation. Neuron 9:607-618.
8. Cairns NJ, Lee VM, Trojanowski JQ (2005) The cytoskeleton in neurodegenerative diseases. J Pathol 204:438-449.
9. Chang W, Gruber D, Chari S, Kitazawa H, Hamazumi Y, Hisanaga S, Bulinski JC (2001) Phosphorylation of MAP4 affects microtubule properties and cell cycle progression. J Cell Sci 114:2879-2887.
10. Chapin SJ, Bulinski JC (1991) Non-neuronal 210 x 10(3) Mr microtubule associated-protein (MAP4) contains a domain homologous to the microtubule-binding domains of neuronal MAP2 and tau. J Cell Sci 98:27-36.
11. Chapin SJ, Lue CM, Yu MT, Bulinski JC (1995) Differential expression of alternatively spliced forms of MAP4: a repertoire of structurally different microtubule-binding domains. Biochemistry 34:2289-2301.
12. Dawson HN, Ferreira A, Eyster MV, Ghoshal N, Binder LI, Vitek MP (2001) Inhibition of neuronal maturation in primary hippocampal neurons from tau deficient mice. J Cell Sci 114:179-1187.
13. Dehmelt L, Halpain S (2004) Actin and microtubules in neurite initiation: are MAPs the missing link? J Neurobiol 58:18-33.
14. Dent EW, Callaway JL, Szebenyi G, Baas PW, Kalil K (1999) Reorganization and movement of microtubules in growth cones and developing interstitial branches. J Neurosci 9:8894-8904.
15. DiTella MC, Feiguin F, Carri N, Kosik KS, Caceres A (1996) MAP1B/TAU functional redundancy during laminin-enhanced axonal growth. J Cell Sci 109:467-477.
16. Errico A, Ballabio A, Rugarli EI (2002) Spastin, the protein mutated in autosomal dominant hereditary spastic paraplegia, is involved in microtubule dynamics. Hum Mol Genet 11:153-163.
17. Evans KJ, Gomes ER, Reisenweber SM, Gundersen GG, Lauring BP (2005) Linking axonal degeneration to microtubule remodeling by Spastin-mediated microtubule severing. J Cell Biol 14:599-606.
18. Ferreira A, Busciglio J, Caceres A (1987) An immunocytochemical analysis of the ontogeny of the microtubule-associated proteins MAP-2 and Tau in the nervous system of the rat. Brain Res 431:9-31.
19. Francis F, Koulakoff A, Boucher D, Chafey P, Schaar B, Vinet MC, Friocourt G, McDonnell N, Reiner O, Kahn A, McConnell SK, Berwald-Netter Y, Denoulet P, Chelly J (1999) Doublecortin is a developmentally regulated, microtubule-associated protein expressed in migrating and differentiating neurons. Neuron 23:247-256.
20. Gamblin TC, Nachmanoff K, Halpain S, Williams Jr RC (1996) Recombinant microtubule-associated protein 2c reduces the dynamic instability of individual microtubules. Biochemistry 35:12576-12586.
21. Gonzalez-Billault C, Engelke M, Jimenez-Mateos EM, Wandosell F, Caceres A, Avila J (2002) Participation of structural microtubule-associated proteins (MAPs) in the development of neuronal polarity. J Neurosci Res 67:713-719.
22. Goold RG, Gordon-Weeks PR (2005) The MAP kinase pathway is upstream of the activation of GSK3beta that enables it to phosphorylate MAP1B and contributes to the stimulation of axon growth. Mol Cell Neurosci 28:524-534.
23. Gordon-Weeks PR, Fischer I (2000) MAP1B expression and microtubule stability in growing and regenerating axons. Microsc Res Tech 48:63-74.
24. Hall GF, Yao J, Lee G (1997) Human tau becomes phosphorylated and forms filamentous deposits when overexpressed in lamprey central neurons in situ. Proc Natl Acad Sci USA 94:4733-4738.
25. Harada A, Teng J, Takei Y, Oguchi K, Hirokawa N (2002) MAP2 is required for dendrite elongation, PKA anchoring, and proper PKA signal transduction. J Cell Biol 158:541-549.
26. He Y, Francis F, Myers KA, Yu W, Black MM, Baas PW (2005) Role of cytoplasmic dynein in the axonal transport of microtubules and neurofilaments. J Cell Biol 168:697-703.
27. Johnson GV, Stoothoff WH (2004) Tau phosphorylation in neuronal cell function and dysfunction. J Cell Sci 117:5721-5729.
28. Karabay A, Yu W, Solowska JM, Baird DH, Baas PW (2004) Axonal growth is sensitive to the levels of katanin, a protein that severs microtubules. J Neurosci 24:5778-5788.
29. Kawauchi T, Chihama K, Nishimura YV, Nabeshima Y, Hoshino M (2005) MAP1B phosphorylation is differentially regulated by Cdk5/p35, Cdk5/ p25, and JNK. Biochem Biophys Res Commun 331:50-55.
30. Krichevsky A, Kosik K (2002) RNAi functions in cultured mammalian neurons. Proc Natl Acad Sci USA 99:11926-11929.
31. Lee G, Rook SL (1992) Expression of tau protein in non-neuronal cells: microtubule binding and stabilization. J Cell Sci 102:227-237.
32. Leger JG, Brandt R, Lee G (1994) Identification of tau protein regions required for process formation in PC12 cells. J Cell Sci 107:3403-3412.
33. Lu M, Kosik KS (2001) Competition for microtubule-binding with dual expression of tau missense and splice isoforms. Mol Biol Cell 12:171-184.
34. Luo MH, Tse SW, Memmott J, Andreadis A (2004) Novel isoforms of tau that lack the microtubule-binding domain. J Neurochem 90:340-351.
35. Mandelkow EM, Thies E, Trinczek B, Biernat J, Mandelkow E (2004) MAPK/PAR kinase is a regulator of microtubule-dependent transport in axons. J Cell Biol 167:99-110.
36. Mandell JW, Banker GA (1996) A spatial gradient of tau protein phosphorylation in nascent axons. J Neurosci 16:5727-5740.
37. McNally FJ, Vale RD (1993) Identification of katanin, an ATPase that severs and disassembles stable microtubules. Cell 75:419-429.
38. McNally KP, Bazirgan OA, McNally FJ (2000) Two domains of p80 katanin regulate microtubule severing and spindle pole targeting by p60 katanin. J Cell Sci 113:1623-1633.
39. McNally KP, Buster D, McNally FJ (2002) Katanin-mediated microtubule severing can be regulated by multiple mechanisms. Cell Motil Cytoskeleton 53:337-349.
40. Meichsner M, Doll T, Reddy D, Weisshaar B, Matus A (1993) The low molecular weight form of microtubule-associated protein 2 is transported into both axons and dendrites. Neuroscience 54:8738-8780.
41. Peng I, Binder LI, Black MM (1986) Biochemical and immunological analyses of cytoskeletal domains of neurons. J Cell Biol 102:252-262.
42. Roll-Mecak A, Vale R (2005) The Drosophila homologue of the hereditary spastic paraplegia protein, spastin, severs and disassembles microtubules. Curr Biol 15:650-655.
43. Rossi J, Eckstein F (2003) RNAi impacts the world of antisense. Oligonucleotides 13:279-280.
44. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning. A Laboratory Manual, Ed 2 (Janssen K, ed), pp 18.47-18.71. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
45. Seitz A, Kojima H, Oiwa K, Mandelkow EM, Song YH, Mandelow E (2002) Single-molecule investigation of the interference between kinesin, tau, and MAP2c. EMBO J 21:4896-4905.
46. Slaughter T, Black MM (2003) STOP (stable-tubule-only-polypeptide) is preferentially associated with the stable domain of axonal microtubules. J Neurocytol 32:399-413.
47. Stoothoff WH, Johnson GV (2005) Tau phosphorylation: physiological and pathological consequences. Biochim Biophys Acta 1739:280-297.
48. Takemura R, Okabe S, Umeyama T, Kanai Y, Cowan NJ, Hirokawa N (1992) Increased microtubule stability and alpha tubulin acetylation in cells transfected with microtubule-associated proteins MAP1B, MAP2 or tau. J Cell Sci 103:953-964.
49. Teng J, Takei J, Nakata T, Chen J, Hirokawa N (2001) Synergistic effects of MAP2 and MAP1b knockout in neuronal migration, dendritic outgrowth, and microtubule organization. J Cell Biol 155:65-76.
50. Tint I, Slaughter T, Fischer I, Black MM (1998) Acute inactivation of tau has no effect on dynamics of microtubules in growing axons of cultured sympathetic neurons. J Neurosci 18:8660-8673.
51. Vale RD (1991) Severing of stable microtubules by a mitotically activated protein in Xenopus egg extracts. Cell 64:827-839.
52. Wang L, Brown A (2002) Rapid movement of microtubules in axons. Curr Biol 12:1496-1501.
53. Yu W, Baas PW (1994) Changes in microtubule number and length during axon differentiation. J Neurosci 14:2818-2829.
54. Yu W, Solowska JM, Qiang L, Karabay A, Baird D, Baas PW (2005) Regulation of microtubule severing by katanin subunits during neuronal development. J Neurosci 25:5573-5583.