The microtubule-stabilizing drug Epothilone D increases axonal sprouting following transection injury in vitro

Molecular and Cellular Neuroscience

Volumn 66, Issue PB, 2015, Pages 129-140

  Brizuela, Mariana ^a   Blizzard, Catherine A ^a   Chuckowree, Jyoti A ^a   Dawkins, Edgar ^a   Gasperini, Robert J ^a   Young, Kaylene M ^a   Dickson, Tracey C ^a  

^a UNIVERSITY OF TASMANIA   (Australia)

Author keywords

Axotomy; Epothilone D; Microtubule stabilizing drug; Microtubules; Traumatic brain injury

Indexed keywords

EPOTHILONE D; DESOXYEPOTHILONE B; EPOTHILONE DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AXONAL INJURY; BRAIN INJURY; BRAIN NERVE CELL; CELL COUNT; CELL FUNCTION; CELL POPULATION; CONTROLLED STUDY; DISEASE ASSOCIATION; DOSE RESPONSE; DRUG EFFECT; DRUG MECHANISM; DRUG RESPONSE; FEMALE; IN VITRO STUDY; MICROTUBULE; MOLECULAR DYNAMICS; NERVE CELL DIFFERENTIATION; NERVE FIBER; NERVE FIBER REGENERATION; NERVE SPROUTING; NONHUMAN; PRIORITY JOURNAL; ANIMAL; BRAIN; BRAIN INJURIES; C57BL MOUSE; CYTOLOGY; DRUG EFFECTS; METABOLISM; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; TRANSGENIC MOUSE;

ANIMALIA;

ANIMALS; AXONS; BRAIN; BRAIN INJURIES; EPOTHILONES; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROTUBULES; NEUROGENESIS; NEURONS;

EID: 84937973158     PISSN: 10447431     EISSN: 10959327     Source Type: Journal    
DOI: 10.1016/j.mcn.2015.02.006     Document Type: Article

References (68)

1. Andrieux A., Salin P., Schweitzer A., Begou M., Pachoud B., Brun P., Gory-Faure S., Kujala P., Suaud-Chagny M.F., Hofle G., Job D. Microtubule stabilizer ameliorates synaptic function and behavior in a mouse model for schizophrenia. Biol. Psychiatry 2006, 60:1224-1230. (Epub 2006 Jun 27).
2. Baas P.W., Ahmad F.J. Beyond taxol: microtubule-based treatment of disease and injury of the nervous system. Brain 2013, 136:2937-2951. (Epub 2013 Jun 27). 10.1093/brain/awt153.
3. Bareyre F.M., Kerschensteiner M., Raineteau O., Mettenleiter T.C., Weinmann O., Schwab M.E. The injured spinal cord spontaneously forms a new intraspinal circuit in adult rats. Nat. Neurosci. 2004, 7:269-277.
4. Barten D.M., Fanara P., Andorfer C., Hoque N., Wong P.Y., Husted K.H., Cadelina G.W., Decarr L.B., Yang L., Liu V., Fessler C., Protassio J., Riff T., Turner H., Janus C.G., Sankaranarayanan S., Polson C., Meredith J.E., Gray G., Hanna A., Olson R.E., Kim S.H., Vite G.D., Lee F.Y., Albright C.F. Hyperdynamic microtubules, cognitive deficits, and pathology are improved in tau transgenic mice with low doses of the microtubule-stabilizing agent BMS-241027. J. Neurosci. 2012, 32:7137-7145.
5. Beer T.M., Higano C.S., Saleh M., Dreicer R., Hudes G., Picus J., Rarick M., Fehrenbacher L., Hannah A.L. Phase II study of KOS-862 in patients with metastatic androgen independent prostate cancer previously treated with docetaxel. Investig. New Drugs 2007, 25:565-570.
6. Blizzard C.A., Haas M.A., Vickers J.C., Dickson T.C. Cellular dynamics underlying regeneration of damaged axons differs from initial axon development. Eur. J. Neurosci. 2007, 26:1100-1108.
7. Blizzard C.A., Chuckowree J.A., King A.E., Hosie K.A., McCormack G.H., Chapman J.A., Vickers J.C., Dickson T.C. Focal damage to the adult rat neocortex induces wound healing accompanied by axonal sprouting and dendritic structural plasticity. Cereb. Cortex 2011, 21:281-291.
8. Blizzard C.A., King A.E., Vickers J., Dickson T. Cortical murine neurons lacking the neurofilament light chain protein have an attenuated response to injury in vitro. J. Neurotrauma 2013, 30:1908-1918. 10.1089/neu.2013.2850.
9. Bradke F., Fawcett J.W., Spira M.E. Assembly of a new growth cone after axotomy: the precursor to axon regeneration. Nat. Rev. Neurosci. 2012, 13:183-193. 10.1038/nrn3176.
10. Brunden K.R., Zhang B., Carroll J., Yao Y., Potuzak J.S., Hogan A.M., Iba M., James M.J., Xie S.X., Ballatore C., Smith A.B., Lee V.M., Trojanowski J.Q. Epothilone D improves microtubule density, axonal integrity, and cognition in a transgenic mouse model of tauopathy. J. Neurosci. 2010, 30:13861-13866.
11. 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. The characterization of microtubule-stabilizing drugs as possible therapeutic agents for Alzheimer's disease and related tauopathies. Pharmacol. Res. 2011, 63:341-351. (Epub 2010 Dec 14). 10.1016/j.phrs.2010.12.002.
12. Brunden K.R., Ballatore C., Lee V.M., Smith A.B., Trojanowski J.Q. Brain-penetrant microtubule-stabilizing compounds as potential therapeutic agents for tauopathies. Biochem. Soc. Trans. 2012, 40:661-666. 10.1042/BST20120010.
13. Cafferty W.B., McGee A.W., Strittmatter S.M. Axonal growth therapeutics: regeneration or sprouting or plasticity?. Trends Neurosci. 2008, 31:215-220.
14. Canty A.J., Huang L., Jackson J.S., Little G.E., Knott G., Maco B., De Paola V. In-vivo single neuron axotomy triggers axon regeneration to restore synaptic density in specific cortical circuits. Nat. Commun. 2013, 4.
15. Carmichael S.T. Plasticity of cortical projections after stroke. Neuroscientist 2003, 9:64-75.
16. Cartelli D., Casagrande F., Busceti C.L., Bucci D., Molinaro G., Traficante A., Passarella D., Giavini E., Pezzoli G., Battaglia G., Cappelletti G. Microtubule alterations occur early in experimental Parkinsonism and the microtubule stabilizer epothilone D is neuroprotective. Sci. Rep. 2013, 3:1837. 10.1038/srep01837.
17. Cengiz N., Ozturk G., Erdogan E., Him A., Oguz E.K. Consequences of neurite transection in vitro. J. Neurotrauma 2012, 29:2465-2474.
18. Chen R., Cohen L.G., Hallett M. Nervous system reorganization following injury. Neuroscience 2002, 111:761-773.
19. Cheng K.L., Bradley T., Budman D.R. Novel microtubule-targeting agents - the epothilones. Biologics 2008, 2:789-811.
20. Chuckowree J., Vickers J.C. Cytoskeletal and morphological alterations underlying axonal sprouting after localized transection of cortical neuron axons in vitro. J. Neurosci. 2003, 23:3715.
21. Chuckowree J.A., Dickson T.C., Vickers J.C. Intrinsic regenerative ability of mature CNS neurons. Neuroscientist 2004, 10:280-285.
22. Chung R.S., Vickers J.C., Chuah M.I., Eckhardt B.L., West A.K. Metallothionein-III inhibits initial neurite formation in developing neurons as well as postinjury, regenerative neurite sprouting. Exp. Neurol. 2002, 178:1-12.
23. Clarke L.E., Young K.M., Hamilton N.B., Li H., Richardson W.D., Attwell D. Properties and fate of oligodendrocyte progenitor cells in the corpus callosum, motor cortex, and piriform cortex of the mouse. J. Neurosci. 2012, 32:8173-8185.
24. Conde C., Caceres A. Microtubule assembly, organization and dynamics in axons and dendrites. Nat. Rev. Neurosci. 2009, 10:319-332.
25. Cortes J., Baselga J. Targeting the microtubules in breast cancer beyond taxanes: the epothilones. Oncologist 2007, 12:271-280.
26. De Lima A.D., Merten M.D.P., Voigt T. Neuritic differentiation and synaptogenesis in serum-free neuronal cultures of the rat cerebral cortex. J. Comp. Neurol. 1997, 382:230-246.
27. Dichter M.A. Rat cortical neurons in cell culture: culture methods, cell morphology, electrophysiology, and synapse formation. Brain Res. 1978, 149:279-293.
28. Dickey C.A., Ash P., Klosak N., Lee W.C., Petrucelli L., Hutton M., Eckman C.B. Pharmacologic reductions of total tau levels; implications for the role of microtubule dynamics in regulating tau expression. Mol. Neurodegener. 2006, 1:6.
29. Dickson T.C., Adlard P.A., Vickers J.C. Sequence of cellular changes following localized axotomy to cortical neurons in glia-free culture. J. Neurotrauma 2000, 17:1095-1103.
30. Dotti C.G., Sullivan C.A., Banker G.A. The establishment of polarity by hippocampal neurons in culture. J. Neurosci. 1988, 8:1454-1468.
31. Drechsel D.N., Hyman A.A., Cobb M.H., Kirschner M.W. Modulation of the dynamic instability of tubulin assembly by the microtubule-associated protein tau. Mol. Biol. Cell 1992, 3:1141-1154.
32. Erturk A., Hellal F., Enes J., Bradke F. Disorganized microtubules underlie the formation of retraction bulbs and the failure of axonal regeneration. J. Neurosci. 2007, 27:9169-9180.
33. Farkas O., Povlishock J.T. Cellular and subcellular change evoked by diffuse traumatic brain injury: a complex web of change extending far beyond focal damage. Prog. Brain Res. 2007, 161:43-59.
34. Fournet V., de Lavilleon G., Schweitzer A., Giros B., Andrieux A., Martres M.P. Both chronic treatments by epothilone D and fluoxetine increase the short-term memory and differentially alter the mood status of STOP/MAP6 KO mice. J. Neurochem. 2012, 123:982-996.
35. Gomis-Ruth S., Wierenga C.J., Bradke F. Plasticity of polarization: changing dendrites into axons in neurons integrated in neuronal circuits. Curr. Biol. 2008, 18:992-1000.
36. Goodin S., Kane M.P., Rubin E.H. Epothilones: mechanism of action and biologic activity. J. Clin. Oncol. 2004, 22:2015-2025.
37. Hanell A., Greer J., McGinn M., Povlishock J. Traumatic Brain Injury-Induced Axonal Phenotypes React Differently to Treatment 2014, D - 0412041, (T - aheadofprint).
38. 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. Microtubule stabilization reduces scarring and causes axon regeneration after spinal cord injury. Science 2011, 331:928-931.
39. Hunt R.F., Boychuk J.A., Smith B.N. Neural circuit mechanisms of post-traumatic epilepsy. Front. Cell. Neurosci. 2013, 7.
40. Janke C., Kneussel M. Tubulin post-translational modifications: encoding functions on the neuronal microtubule cytoskeleton. Trends Neurosci. 2010, 33:362-372.
41. Johnson V.E., Stewart W., Smith D.H. Axonal pathology in traumatic brain injury. Exp. Neurol. 2012, 246:35-43.
42. Kar S., Fan J., Smith M.J., Goedert M., Amos L.A. Repeat motifs of tau bind to the insides of microtubules in the absence of taxol. EMBO J. 2003, 22:70-77.
43. King C.E., Adlard P.A., Dickson T.C., Vickers J.C. Neuronal response to physical injury and its relationship to the pathology of Alzheimer's disease. Clin. Exp. Pharmacol. Physiol. 2000, 27:548-552.
44. King A.E., Chung R.S., Vickers J.C., Dickson T.C. Localization of glutamate receptors in developing cortical neurons in culture and relationship to susceptibility to excitotoxicity. J. Comp. Neurol. 2006, 498:277-294.
45. Kolman A. Activity of epothilones. Curr. Opin. Investig. Drugs 2005, 6:616-622.
46. Loov C., Shevchenko G., Nadadhur A.G., Clausen F., Hillered L., Wetterhall M., Erlandsson A. Identification of injury specific proteins in a cell culture model of traumatic brain injury. PLoS One 2013, 8:e55983.
47. Lou K., Yao Y., Hoye A.T., James M.J., Cornec A.-S., Hyde E., Gay B., Lee V.M.Y., Trojanowski J.Q., Smith A.B., Brunden K.R., Ballatore C. Brain-penetrant, orally bioavailable microtubule-stabilizing small molecules Are potential candidate therapeutics for Alzheimer' Äôs disease and related tauopathies. J. Med. Chem. 2014, 57:6116-6127.
48. Mainen Z.F., Sejnowski T.J. Influence of dendritic structure on firing pattern in model neocortical neurons. Nature 1996, 382:363-366.
49. Maxwell W. Microtubular changes in axons after stretch injury. J. Neurotrauma 1995, 12:363.
50. McKinney R.A., Debanne D., Gahwiler B.H., Thompson S.M. Lesion-induced axonal sprouting and hyperexcitability in the hippocampus in vitro: implications for the genesis of posttraumatic epilepsy. Nat. Med. 1997, 3:990-996.
51. McKinney R.A., Luthi A., Bandtlow C.E., Gähwiler B.H., Thompson S.M. Selective glutamate receptor antagonists can induce or prevent axonal sprouting in rat hippocampal slice cultures. Proc. Natl. Acad. Sci. 1999, 96:11631-11636.
52. Meythaler J.M., Peduzzi J.D., Eleftheriou E., Novack T.A. Current concepts: diffuse axonal injury-associated traumatic brain injury. Arch. Phys. Med. Rehabil. 2001, 82:1461-1471.
53. Picken Bahrey H.L., Moody W.J. Early development of voltage-gated ion currents and firing properties in neurons of the mouse cerebral cortex. J. Neurophysiol. 2003, 89:1761-1773. (Epub 2002 Dec 11).
54. Prince D.A., Parada I., Scalise K., Graber K., Jin X., Shen F. Epilepsy following cortical injury: cellular and molecular mechanisms as targets for potential prophylaxis. Epilepsia 2009, 2:30-40.
55. Rampersad S.N. Multiple applications of Alamar Blue as an indicator of metabolic function and cellular health in cell viability bioassays. Sensors (Basel) 2012, 12:12347-12360. (Epub 2012 Sep 10). 10.3390/s120912347.
56. Rossignol S., Drew T., Brustein E., Jiang W. Locomotor performance and adaptation after partial or complete spinal cord lesions in the cat. Prog. Brain Res. 1999, 123:349-365.
57. Sengottuvel V., Fischer D. Facilitating axon regeneration in the injured CNS by microtubules stabilization. Commun. Integr. Biol. 2011, 4:391-393. (Epub 2011 Jul 1). 10.4161/cib.4.4.15552.
58. Sengottuvel V., Leibinger M., Pfreimer M., Andreadaki A., Fischer D. Taxol facilitates axon regeneration in the mature CNS. J. Neurosci. 2011, 31:2688-2699.
59. Smith D.H., Wolf J.A., Lusardi T.A., Lee V.M., Meaney D.F. High tolerance and delayed elastic response of cultured axons to dynamic stretch injury. J. Neurosci. 1999, 19:4263-4269.
60. Smith D.H., Hicks R., Povlishock J.T. Therapy development for diffuse axonal injury. J. Neurotrauma 2013, 30:307-323.
61. Tang-Schomer M.D., Patel A.R., Baas P.W., Smith D.H. Mechanical breaking of microtubules in axons during dynamic stretch injury underlies delayed elasticity, microtubule disassembly, and axon degeneration. FASEB J. 2010, 24:1401-1410.
62. Tang-Schomer M.D., Johnson V.E., Baas P.W., Stewart W., Smith D.H. Partial interruption of axonal transport due to microtubule breakage accounts for the formation of periodic varicosities after traumatic axonal injury. Exp. Neurol. 2012, 233:364-372. (Epub 2011 Nov 4). 10.1016/j.expneurol.2011.10.030.
63. Thiel G. Synapsin I, synapsin II, and synaptophysin: marker proteins of synaptic vesicles. Brain Pathol. 1993, 3:87-95.
64. Tytell M., Brady S.T., Lasek R.J. Axonal transport of a subclass of tau proteins: evidence for the regional differentiation of microtubules in neurons. Proc. Natl. Acad. Sci. U. S. A. 1984, 81:1570-1574.
65. Wang H., Wang Z., Wang S., Li M., Nan L., Rhie J.K., Covey J.M., Zhang R., Hill D.L. Preclinical pharmacology of epothilone D, a novel tubulin-stabilizing antitumor agent. Cancer Chemother. Pharmacol. 2005, 56:255-260. (Epub 2005 May 3).
66. Wang H., Wang Z., Wang S., Li M., Nan L., Rhie J., Covey J., Zhang R., Hill D. Preclinical Pharmacology of Epothilone D, A Novel Tubulin-Stabilizing Antitumor 2005.
67. Weidner N., Ner A., Salimi N., Tuszynski M.H. Spontaneous corticospinal axonal plasticity and functional recovery after adult central nervous system injury. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:3513-3518.
68. Wieloch T., Nikolich K. Mechanisms of neural plasticity following brain injury. Curr. Opin. Neurobiol. 2006, 16:258-264.