Microtubule stabilization by peloruside A and paclitaxel rescues degenerating neurons from okadaic acid-induced tau phosphorylation

European Journal of Neuroscience

Volumn 35, Issue 11, 2012, Pages 1705-1717

  Das, Viswanath ^a   Miller, John H ^a  

^a VICTORIA UNIVERSITY OF WELLINGTON   (New Zealand)

Author keywords

Acetylated tubulin; Alzheimer's disease; Growth cone; Growth associated protein 43; Sprague Dawley rat

Indexed keywords

ANTINEOPLASTIC AGENT; BETA TUBULIN; MICROTUBULE STABILIZING DRUG; NEUROMODULIN; OKADAIC ACID; PACLITAXEL; PELORUSIDE A; TAU PROTEIN; UNCLASSIFIED DRUG;

ACETYLATION; ANIMAL CELL; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; GROWTH CONE; MICROTUBULE; NERVE CELL CULTURE; NERVE CELL DEGENERATION; NERVE FIBER GROWTH; NEWBORN; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT;

ANIMALS; ANIMALS, NEWBORN; BICYCLO COMPOUNDS, HETEROCYCLIC; FEMALE; LACTONES; MALE; MICROTUBULES; NERVE DEGENERATION; NEUROPROTECTIVE AGENTS; PACLITAXEL; PHOSPHORYLATION; PRIMARY CELL CULTURE; RATS; RATS, SPRAGUE-DAWLEY; TAU PROTEINS; TUBULIN MODULATORS;

EID: 84861906161     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2012.08084.x     Document Type: Article

References (45)

1. Arendt, T., Holzer, M., Brückner, M.K., Janke, C. & Gärtner, U. (1998) The use of okadaic acid in vivo and the induction of molecular changes typical for Alzheimer's disease. Neuroscience, 85, 1337-1340.
2. Arias, C., Sharma, N., Davies, P. & Shafit-Zagardo, B. (1993) Okadaic acid induces early changes in microtubule-associated protein-2 and tau phosphorylation prior to neurodegeneration in cultured cortical neurons. J. Neurochem., 61, 673-682.
3. Black, M.M., Baas, P.W. & Humphries, S. (1989) Dynamics of α-tubulin deacetylation in intact neurons. J. Neurosci., 9, 358-368.
4. Brunden, K.R., Zhang, B., Carroll, J., Yao, Y., Potuzak, J.S., Hogan, A.M.L., Iba, M., James, M.J., Xie, S.X., Ballatore, C., Smith, A.B., Lee, V.M.Y. & Trojanowski, J.Q. (2010) Epothilone D improves microtubule density, axonal integrity, and cognition in a transgenic mouse model of tauopathy. J. Neurosci., 30, 13861-13866.
5. Brunden, K.R., Yao, Y., Potuzak, J.S., Ferrer, N.I., Ballatore, C., James, M.J., Hogan, A.M., Trojanowski, J.Q., Smith, A.B. & Lee, V.M. (2011) The characterization of microtubule-stabilizing drugs as possible therapeutic agents for Alzheimer's disease and related tauopathies. Pharmacol. Res., 63, 341-351.
6. +-induced neurodegeneration. J. Neurochem., 115, 247-258.
7. Chan, A., Andreae, P.M., Northcote, P.T. & Miller, J.H. (2011) Peloruside A inhibits microtubule dynamics in a breast cancer cell line MCF7. Invest. New Drugs, 29, 615-626.
8. Crume, K.P., O'Sullivan, D., Miller, J.H., Northcote, P.T. & La Flamme, A.C. (2009) Delaying the onset of experimental autoimmune encephalomyelitis with the microtubule-stabilizing compounds, paclitaxel and peloruside A. J. Leukoc. Biol., 86, 949-958.
9. Denny, J.B. (2006) Molecular mechanisms, biological actions, and neuropharmacology of the growth-associated protein GAP-43. Curr. Neuropharmacol., 4, 293-304.
10. Derry, W.B., Wilson, L. & Jordan, M.A. (1995) Substoichiometric binding of taxol suppresses microtubule dynamics. Biochemistry, 34, 2203-2211.
11. Doster, S.K., Lozano, A.M., Aguayo, A.J. & Willard, M.B. (1991) Expression of the growth-associated protein GAP-43 in adult rat retinal ganglion cells following axon injury. Neuron, 6, 635-647.
12. Feinstein, S.C. & Wilson, L. (2005) 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, 1739, 268-279.
13. Gaitanos, T.N., Buey, R.M., Díaz, J.F., Northcote, P.T., Teesdale-Spittle, P., Andreu, J.M. & Miller, J.H. (2004) Peloruside A does not bind to the taxoid site on beta-tubulin and retains its activity in multidrug-resistant cell lines. Cancer Res., 64, 5063-5067.
14. 53 acetylation. Cell Death Differ., 17, 1392-1408.
15. Gong, C.X. & Iqbal, K. (2008) Hyperphosphorylation of microtubule-associated protein tau: a promising therapeutic target for Alzheimer's disease. Curr. Med. Chem., 15, 2321-2328.
16. Hellal, F., Hurtado, A., Ruschel, J., Flynn, K.C., Laskowski, C.J., Umlauf, M., Kapitein, L.C., Strikis, D., Lemmon, V., Bixby, J., Hoogenraad, C.C. & Bradke, F. (2011) Microtubule stabilization reduces scarring and causes axon regeneration after spinal cord injury. Science, 331, 928-931.
17. Hilgenberg, L.G. & Smith, M.A. (2007) Preparation of dissociated mouse cortical neuron cultures. J. Vis. Exp., 10, 562.
18. Hood, K.A., West, L.M., Rouwé, B., Northcote, P.T., Berridge, M.V., Wakefield, S.J. & Miller, J.H. (2002) Peloruside A, a novel antimitotic agent with paclitaxel-like microtubule-stabilizing activity. Cancer Res., 62, 3356-3360.
19. Huzil, J.T., Chik, J.K., Slysz, G.W., Freedman, H., Tuszynski, J., Taylor, R.E., Sackett, D.L. & Schriemer, D.C. (2008) A unique mode of microtubule stabilization induced by Peloruside A. J. Mol. Biol., 378, 1016-1030.
20. Jacobson, R.D., Virag, I. & Skene, J.H.P. (1986) A protein associated with axon growth, GAP-43, is widely distributed and developmentally regulated in rat CNS. J. Neurosci., 6, 1843-1855.
21. Kar, S., Florence, G.J., Paterson, I. & Amos, L.A. (2003) Discodermolide interferes with the binding of tau protein to microtubules. FEBS Lett., 539, 34-36.
22. Kivell, B.M., McDonald, F.J. & Miller, J.H. (2001) Method for serum-free culture of late fetal and early postnatal rat brainstem neurons. Brain Res. Brain Res. Protoc., 6, 91-99.
23. Kunze, A., Meissner, R., Brando, S. & Renaud, P. (2011) Co-pathological connected primary neurons in a microfluidic device for Alzheimer studies. Biotechnol. Bioeng., 108, 2241-2245.
24. Marcus, A.I., Zhou, J., O'Brate, A., Hamel, E., Wong, J., Nivens, M., El-Naggar, A., Yao, T.P., Khuri, F.R. & Giannakakou, P. (2005) The synergistic combination of the farnesyl transferase inhibitor lonafarnib and paclitaxel enhances tubulin acetylation and requires a functional tubulin deacetylase. Cancer Res., 65, 3883-3893.
25. Merrick, S.E., Trojanowski, J.Q. & Lee, V.M. (1997) Selective destruction of stable microtubules and axons by inhibitors of protein serine/threonine phosphatases in cultured human neurons. J. Neurosci., 17, 5726-5737.
26. Meyer, C., Ferguson, D., Krauth, M., Wick, M. & Northcote, P. (2006) RTA 301 (Peloruside): a novel microtubule stabilizer with potent in vivo activity against lung cancer and resistant breast cancer. Eur. J. Cancer Suppl., 4, 192-193. 18th EORTC-NCI-AACR Symposium on Molecular Targets and Cancer Therapeutics. Prague, Czech Republic, (for pdf, see:).
27. Nakayama, T., Goshima, Y., Misu, Y. & Kato, T. (1999) Role of cdk5 and tau phosphorylation in heterotrimeric G protein-mediated retinal growth cone collapse. J. Neurobiol., 41, 326-339.
28. Piperno, G., Le Dizet, M. & Chang, X.J. (1987) Microtubules containing acetylated alpha-tubulin in mammalian cells in culture. J. Cell Biol., 104, 289-302.
29. Qiang, L., Yu, W., Liu, M., Solowska, J.M. & Baas, P.W. (2010) Basic fibroblast growth factor elicits formation of interstitial axonal branches via enhanced severing of microtubules. Mol. Biol. Cell, 21, 334-344.
30. Reed, N.A., Cai, D., Blasius, T.L., Jih, G.T., Meyhofer, E., Gaertig, J. & Verhey, K.J. (2006) Microtubule acetylation promotes kinesin-1 binding and transport. Curr. Biol., 16, 2166-2172.
31. Schaechter, J.D. & Benowitz, L.I. (1993) Activation of protein kinase C by arachidonic acid selectively enhances the phosphorylation of GAP-43 in nerve terminal membranes. J. Neurosci., 13, 4361-4371.
32. Schmidt, H. & Rathjen, F.G. (2010) Signaling mechanisms regulating axonal branching in vivo. BioEssays, 37, 977-985.
33. Sengottuvel, V., Leibinger, M., Pfreimer, M., Andreadaki, A. & Fischer, D. (2011) Taxol facilitates axon regeneration in the mature CNS. J. Neurosci., 31, 2688-2699.
34. Shemesh, A. & Spira, M.E. (2011) Rescue of neurons from undergoing hallmark tau-induced Alzheimer's disease cell pathologies by the antimitotic drug paclitaxel. Neurobiol. Dis., 43, 163-175.
35. Shen, Y., Mani, S., Donovan, S.L., Schwob, J.E. & Meiri, K.F. (2002) Growth-associated protein-43 is required for commissural axon guidance in the developing vertebrate nervous system. J. Neurosci., 22, 239-247.
36. Strittmatter, S.M., Fankhauser, C., Huang, P.L., Mashimo, H. & Fishman, M.C. (1995) Neuronal pathfinding is abnormal in mice lacking the neuronal growth cone protein GAP-43. Cell, 80, 445-452.
37. Sudo, H. & Baas, P.W. (2010) Acetylation of microtubules influences their sensitivity to severing by katanin in neurons and fibroblasts. J. Neurosci., 30, 7215-7226.
38. Tran, A.A.D., Marmo, T.P., Salam, A.A., Che, S., Finkelstein, E., Kabarriti, R., Xenias, H.S., Mazitschek, R., Hubbert, C., Kawaguchi, Y., Sheetz, M.P., Yao, T.P. & Bulinski, J.C. (2007) HDAC6 deacetylation of tubulin modulates dynamics of cellular adhesions. J. Cell Sci., 120, 1469-1479.
39. Wang, J.Z., Tung, Y.C., Wang, Y., Li, X.T., Iqbal, K. & Iqbal, I.G. (2001) Hyperphosphorylation and accumulation of neurofilament proteins in Alzheimer's disease brain and in okadaic acid-treated SY5Y cells. FEBS Lett., 507, 81-87.
40. West, L.M., Northcote, P.T. & Battershill, C.N. (2000) Peloruside A: a potent cytotoxic macrolide isolated from the New Zealand marine sponge Mycale sp. J. Org. Chem., 65, 445-449.
41. Wilmes, A., Bargh, K., Kelly, C., Northcote, P.T. & Miller, J.H. (2007) Peloruside A synergizes with other microtubule stabilizing agents in cultured cancer cell lines. Mol. Pharm., 4, 269-280.
42. Wilmes, A., O'Sullivan, D., Chan, A., Chandrahasen, C., Paterson, I., Northcote, P.T., La Flamme, A.C. & Miller, J.H. (2011) Synergistic interactions between peloruside A and other microtubule-stabilizing and destabilizing agents in cultured human ovarian carcinoma cells and murine T cells. Cancer Chemother. Pharmacol., 68, 117-126.
43. Witte, H., Neukirchen, D. & Bradke, F. (2008) Microtubule stabilization specifies initial neuronal polarization. J. Cell Biol., 180, 619-632.
44. Xu, Y.F., Zhang, Y.J., Zhang, A.H., Zhang, Q., Wu, T. & Wang, J.Z. (2004) Attenuation of okadaic acid-induced hyperphosphorylation of cytoskeletal proteins by heat preconditioning and its possible underlying mechanisms. Cell Stress Chaperones, 9, 304-312.
45. Zhang, B., Maiti, A., Shively, S., Lakhani, F., McDonald-Jones, G., Bruce, J., Lee, E.B., Xie, S.X., Joyce, S., Li, C., Toleikis, P.M., Lee, V.M.Y. & Trojanowski, J.Q. (2005) Microtubule-binding drugs offset tau sequestration by stabilizing microtubules and reversing fast axonal transport deficits in a tauopathy model. Proc. Natl Acad. Sci. USA, 102, 227-231.