Peptide neuroprotection through specific interaction with brain tubulin

Journal of Neurochemistry

Volumn 98, Issue 3, 2006, Pages 973-984

  Divinski, Inna ^a   Holtser Cochav, Miri ^a   Vulih Schultzman, Inna ^a   Steingart, Ruth A ^a   Gozes, Illana ^a  

^a TEL AVIV UNIVERSITY   (Israel)

Author keywords

III tubulin; Activity dependent neuroprotective protein; Microtubules; NAP; Taxol

Indexed keywords

ASPARAGINYLALANYLPROLYLVALYLSERYLISOLEUCYLPROLYLGLUTAMINE; BETA TUBULIN; PACLITAXEL; PEPTIDE; TUBULIN; UNCLASSIFIED DRUG; ZINC CHLORIDE;

AFFINITY CHROMATOGRAPHY; ANIMAL CELL; ARTICLE; BINDING AFFINITY; BRAIN CELL; CELL FUNCTION; CELL PROTECTION; CELL SURVIVAL; FIBROBLAST; MICROTUBULE; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PHEOCHROMOCYTOMA CELL; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RAT;

ANIMALS; BRAIN; CELLS, CULTURED; MICE; NEUROPROTECTIVE AGENTS; NIH 3T3 CELLS; OLIGOPEPTIDES; PC12 CELLS; PEPTIDES; RATS; TUBULIN;

EID: 33745916443     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2006.03936.x     Document Type: Article

References (57)

1. Alcalay R. N., Giladi E., Pick C. G. and Gozes I. (2004) Intranasal administration of NAP, a neuroprotective peptide, decreases anxiety-like behavior in aging mice in the elevated plus maze. Neurosci. Lett. 361, 128-131.
2. Banerjee A., Roach M. C., Trcka P. and Luduena R. F. (1990) Increased microtubule assembly in bovine brain tubulin lacking the type III isotype of β-tubulin. J. Biol. Chem. 265, 1794-1799.
3. Bassan M., Zamostiano R., Davidson A. et al. (1999) Complete sequence of a novel protein containing a femtomolar-activity-dependent neuroprotective peptide. J. Neurochem. 72, 1283-1293.
4. Baulieu E. E., Robel P., Fellous A., Duchossoy Y., Fontaine-Lenoir V. and David S. (2004) MAPREG: toward a novel approach of neuroprotection and treatment of Alzheimer's disease. J. Mol. Neurosci. 24, 63-65.
5. Beni-Adani L., Gozes I., Cohen Y., Assaf Y., Steingart R. A., Brenneman, D. E., Eizenberg O., Trembolver V. and Shohami E. (2001) A peptide derived from activity-dependent neuroprotective protein (ADNP) ameliorates injury response in closed head injury in mice. J. Pharmacol. Exp. Ther. 296, 57-63.
6. Benitez-King G., Ramirez-Rodriguez G., Ortiz L. and Meza I. (2004) The neuronal cytoskeleton as a potential therapeutical target in neurodegenerative diseases and schizophrenia. Curr. Drug Targets CNS Neurol. Disord. 3, 515-533.
7. Boss B. D., Gozes I. and Cowan W. M. (1987) The survival of dentate gyrus neurons in dissociated culture. Brain Res. 433, 199-218.
8. Divinski I., Mittelman L. and Gozes I. (2004) A femtomolar acting octapeptide interacts with tubulin and protects astrocytes against zinc intoxication. J. Biol. Chem. 279, 28 531-28 538.
9. Don S., Verrills N. M., Liaw T., Liu M., Norris M. D., Haber M. and Kavallaris M. (2004) Neuronal-associated microtubule proteins class III β-tubulin and MAP2c neuroblastoma: role in resistance to microtubule-targeted drugs. Mol. Cancer Ther. 3, 1137-1146.
10. Ferlini C., Raspaglio G., Mozzetti S., Cicchillitti L., Filippetti F., Gallo D., Fattourusso C., Campiani G. and Scambia G. (2005) The secotaxane IDN5390 is able to target class III β-tubulin and to overcome paclitaxel resistance. Cancer Res. 65, 2397-2405.
11. Furman S., Steingart R. A., Mandel S., Hauser J. M., Brenneman D. E. and Gozes I. (2004) Subcellular localization and secretion of activity-dependent neuroprotective protein in astrocytes. Neuron Glia Biol. 1, 193-199.
12. Giant B., Wang C., Ravelli R. B., Roussi F., Steinmetz M. O., Curmi P. A., Sobel A. and Knossow M. (2005) Structural basis for the regulation of tubulin by vinblastine. Nature 435, 519-522.
13. Gozes I. and Barnstable C. J. (1982) Monoclonal antibodies that recognize discrete forms of tubulin. Proc. Natl Acad. Sci. USA 79, 2579-2583.
14. Gozes I. and Divinski I. (2004) The femtomolar-acting NAP interacts with microtubules: novel aspects of astrocyte protection. J. Alzheimers Dis. 6, S37-S41.
15. Gozes I. and Littauer U. Z. (1978) Tubulin microheterogeneity increases with rat brain maturation. Nature 276, 411-413.
16. Gozes I. and Littauer U. Z. (1979) The α-subunit of tubulin is preferentially associated with brain presynaptic membrnae. FEBS Lett. 99, 86-90.
17. Gozes I. and Littauer U. Z. (1982) Microtubule protein: tubulin. Scand. J. Immunol. Suppl. 9, 299-316.
18. Gozes I. and Richter-Landsberg C. (1978) Identification of tubulin associated with rat brain myelin. FEBS Lett. 95, 169-172.
19. Gozes I. and Sweadner K. J. (1981) Multiple tubulin forms are expressed by a single neurone. Nature 294, 477-480.
20. Gozes I., Littauer U. Z., Geiger B. and Fuchs S. (1977) Immunochemical determination of tubulin. FEBS Lett. 73, 109-114.
21. Gottlieb P., Beretz A. and Fridkin M. (1982) Tuftsin analogs for probing its specific receptor site on phagocytic cells. Eur. J. Biochem. 125, 631-638.
22. Gozes I., Giladi E., Pinhasov A., Bardea A. and Brenneman D. E. (2000) Activity-dependent neurotrophic factor: intranasal administration of femtomolar-acting peptides improve performance in a water maze. J. Pharmacol. Exp. Ther. 293, 1091-1098.
23. Gozes I., Alcalay R., Giladi E., Pinhasov A., Furman S. and Brenneman D. E. (2002) NAP accelerates the performance of normal rats in the water maze. J. Mol. Neurosci. 19, 167-170.
24. Gozes I., Divinsky I., Pilzer I., Fridkin M., Brenneman D. E. and Spier A. D. (2003) From vasoactive intestinal peptide (VIP) through activity-dependent neuroprotective protein (ADNP) to NAP: a view of neuroprotection and cell division. J. Mol. Neurosci. 20, 315-322.
25. Gozes I., Steingart R. A. and Spier A. D. (2004) NAP mechanisms of neuroprotection. J. Mol. Neurosci. 24, 67-72.
26. Hamel E. and Covell D. G. (2002) Anti-mitotic peptides and depsipeptides. Curr. Med. Chem. - Anti-Cancer Agents 2, 19-53.
27. Joshi H. C. and Cleveland D. W. (1989) Differential utilization of β-tubulin isotypes in differentiating neurites. J. Cell Biol. 109, 663-673.
28. Joshi H. C. and Cleveland D. W. (1990) Diversity among tubulin subunits: toward what functional end? Cell Motil. Cytoskeleton 16, 159-163.
29. Katsetos C. D., Legido A., Perentes E. and Mork S. J. (2003) Class III β-tubulin isotype: a key cytoskeletal protein at the crossroads of developmental neurobiology and tumor neuropathology. J. Child Neurol. 18, 851-867.
30. Lagrèze W. A., Pielen A., Steingart R. A., Schlunck G., Hofmann H.-D., Gozes I. and Kirsch M. (2005) The peptides ADNF-9 and NAP increase survival and neurite outgrowth of rat retinal ganglion cells in vitro. Invest. Ophthalmol. Visual Sci. 46, 933-938.
31. Leker R. R., Teichner A., Grigoriadis N., Ovadia H., Brenneman D. E., Fridkin M., Giladi E., Romano J. and Gozes I. (2002) NAP, a femtomolar-acting peptide, protects the brain against ischemic injury by reducing apoptotic death. Stroke 33, 1085-1092.
32. Li Y., Edsall R. Jr, Jagtap P. G., Kingston D. G. and Bane S. (2000) Equilibrium studies of a flurescent paclitaxel derivative binding to microtubules. Biochemistry 39, 616-623.
33. Lowe J., Li H., Downing K. H. and Nogales E. (2001) Refined structure of αβ-tubulin at 3.5A resolution. J. Mol. Biol. 313, 1045-1057.
34. Luduena R. F. (1998) Multiple forms of tubulin: different gene products and covalent modifications. Int. Rev. Cytol. 178, 207-275.
35. Michaelis M. L., Ansar S., Chen Y., Reiff E. R., Seyb K. I., Himes R. H., Audus K. L. and Georg G. I. (2005) β-Amyloid-induced neurodegeneration and protection by structurally diverse microtubule-stabilizing agents. J. Pharmacol. Exp. Ther. 312, 659-668.
36. 2+ release. J. Biol. Chem. 280, 715-721.
37. Mitra A. and Sept D. (2004) Localization of the anti-mitotic peptide and depsipeptide binding site on β-tubulin. Biochemistry 43, 13 955-13 962.
38. Moolman D. L., Vitolo O. V., Vonsattel J. P. and Shelanski M. L. (2004) Dendrite and dendritic spine alterations in Alzheimer models. J. Neurocytol. 33, 377-387.
39. Mozzetti S., Ferlini C., Concolino P. et al. (2005) Class III β-tubulin overexpression is a prominent mechanism of paclitaxel resistance in ovarian cancer patients. Clin. Cancer Res. 11, 298-305.
40. Offen D., Sherki Y., Melamed E., Fridkin M., Brenneman D. E. and Gozes I. (2000) Vasoactive intestinal peptide (VIP) prevents neurotoxicity in neuronal cultures: relevance to neuroprotection in Parkinson's disease. Brain Res. 854, 257-262.
41. Panda D., Miller H. P., Banerjee A., Luduena R. F. and Wilson L. (1994) Microtubule dynamics in vitro are regulated by the tubulin isotype composition. Proc. Natl Acad. Sci. USA 91, 11 358-11 362.
42. Peng I., Binder L. I. and Black M. M. (1986) Biochemical and immunological analyses of cytoskeletal domains of neurons. J. Cell Biol. 102, 252-262.
43. Pinhasov A., Mandel S., Torchinsky A., Giladi E., Pittel Z., Goldsweig A. M., Servoss S. J., Brenneman D. E. and Gozes I. (2003) Activity-dependent neuroprotective protein: a novel gene essential for brain formation. Brain Res. Dev. Brain Res. 144, 83-90.
44. Roy S., Zhang B., Lee V. M. and Trojanowski J. Q. (2005) Axonal transport defects: a common theme in neurodegenerative diseases. Acta Neuropathol. (Berl.) 109, 5-13.
45. Smith-Swintosky V. L., Gozes I., Brenneman D. E., D'Andrea M. R. and Plata-Salaman C. R. (2005) Activity-dependent neurotrophic factor-9 and NAP promote neurite outgrowth in rat hippocampal and cortical cultures. J. Mol. Neurosci. 25, 225-238.
46. Spong C. Y., Abebe D. T., Gozes I., Brenneman D. E. and Hill J. M. (2001) Prevention of fetal demise and growth restriction in a mouse model of fetal alcohol syndrome. J. Pharmacol. Exp. Ther. 297, 774-779.
47. Steingart R. A., Solomon B., Brenneman D. E., Fridkin M. and Gozes, I. (2000). VIP and peptides related to activity-dependent neurotrophic factor protect PC12 cells against oxidative stress. J. Mol. Neurosci. 15, 137-145.
48. Terry R. D. (1998) The cytoskeleton in Alzheimer disease. J. Neural Transm. Suppl. 53, 141-145.
49. Visochek L., Steingart R. A., Vulih-Shultzman I., Klein R., Priel E., Gozes I. and Armon-Cohen M. (2005) PolyADP-ribosylation is involved in neurotrophic activity. J. Neurosci. 25, 7420-7428.
50. Wise D. O., Krahe R. and Oakley B. R. (2000) The γ-tubulin gene family in humans. Genomics 67, 164-170.
51. Xu G., Pierson C. R., Murakawa Y. and Sima A. A. (2002) Altered tubulin and neurofilament expression and impaired axonal growth in diabetic nerve regeneration. J. Neuropathol. Exp. Neurol. 61, 164-175.
52. Zaltzman R., Alexandrovich A., Beni S. M., Trembovler V., Shohami E. and Gozes I. (2004) Brain injury-dependent expression of activity-dependent neuroprotective protein. J. Mol. Neurosci. 24, 181-187.
53. Zambito A. M., Knipling L. and Wolff J. (2002) Charge variants of tubulin, tubulin S, membrane-bound and palmitoylated tubulin from brain and pheochromocytoma cells. Biochim. Biophys. Acta 1601, 200-207.
54. Zamostiano R., Pinhasov A., Gelber E. et al. (2001) Cloning and characterization of the human activity-dependent neuroprotective protein. J. Biol. Chem. 276, 708-714.
55. Zemlyak I., Furman S., Brenneman D. E. and Gozes I. (2000) A novel peptide prevents death in enriched neuronal cultures. Regul. Pept. 96, 39-43.
56. Zhang B., Maiti A., Shively S. et al. (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.
57. Zisapel N., Levi M. and Gozes I. (1980) Tubulin: an integral protein of mammalian synaptic vesicle membranes. J. Neurochem. 34, 26-32.