Paclitaxel induces axonal microtubules polar reconfiguration and impaired organelle transport: Implications for the pathogenesis of paclitaxel-induced polyneuropathy

Acta Neuropathologica

Volumn 119, Issue 2, 2010, Pages 235-248

  Shemesh, Or A ^a   Spira, Micha E ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

Aplysia; Axoplasmic transport; Microtubules; Paclitaxel; Peripheral neuropathy; Plus ends binding proteins

Indexed keywords

ANTINEOPLASTIC AGENT; PACLITAXEL;

ANIMAL CELL; APLYSIA; ARTICLE; CONTROLLED STUDY; MICROTUBULE; NERVE CELL DEGENERATION; NERVE CELL DIFFERENTIATION; NERVE FIBER; NERVE FIBER TRANSPORT; NONHUMAN; PATHOGENESIS; POLYNEUROPATHY; PRIORITY JOURNAL; ANIMAL; CELL ORGANELLE; CHEMICALLY INDUCED DISORDER; CONFOCAL MICROSCOPY; DRUG EFFECT; IMAGE PROCESSING; METABOLISM; PATHOLOGY; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; ANTINEOPLASTIC AGENTS, PHYTOGENIC; APLYSIA; AXONS; BIOLOGICAL TRANSPORT; IMAGE PROCESSING, COMPUTER-ASSISTED; MICROSCOPY, CONFOCAL; MICROTUBULES; ORGANELLES; PACLITAXEL; POLYNEUROPATHIES;

EID: 77449107515     PISSN: 00016322     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00401-009-0586-0     Document Type: Article

References (63)

1. AA Argyriou M Koltzenburg P Polychronopoulos S Papapetropoulos HP Kalofonos 2008 Peripheral nerve damage associated with administration of taxanes in patients with cancer Crit Rev Oncol Hematol 66 218 228 10.1016/j.critrevonc. 2008.01.008 18329278
2. PW Baas MM Black GA Banker 1989 Changes in microtubule polarity orientation during the development of hippocampal neurons in culture J Cell Biol 109 3085 3094 10.1083/jcb.109.6.3085 1:STN:280:DyaK3c%2FnvVensw%3D%3D 2592416 (Pubitemid 20011932)
3. PW Baas A Karabay L Qiang 2005 Microtubules cut and run Trends Cell Biol 15 518 524 10.1016/j.tcb.2005.08.004 1:CAS:528:DC%2BD2MXhtVynu7bM 16126385 (Pubitemid 41396433)
4. PR Burton 1988 Dendrites of mitral cell neurons contain microtubules of opposite polarity Brain Res 473 107 115 10.1016/0006-8993(88)90321-6 1:STN:280:DyaL1M%2FovFWntA%3D%3D 3264743 (Pubitemid 19008217)
5. PR Burton JL Paige 1981 Polarity of axoplasmic microtubules in the olfactory nerve of the frog Proc Natl Acad Sci USA 78 3269 3273 10.1073/pnas.78.5.3269 1:STN:280:DyaL3M3kslClsQ%3D%3D 6973153 (Pubitemid 11033011)
6. N Callizot E Andriambeloson J Glass, et al. 2008 Interleukin-6 protects against paclitaxel, cisplatin and vincristine-induced neuropathies without impairing chemotherapeutic activity Cancer Chemother Pharmacol 62 995 1007 10.1007/s00280-008-0689-7 1:CAS:528:DC%2BD1cXhtFaju77E 18270703
7. C Conde A Caceres 2009 Microtubule assembly, organization and dynamics in axons and dendrites Nat Rev Neurosci 10 319 332 10.1038/nrn2631 1:CAS:528:DC%2BD1MXks12ktbk%3D 19377501
8. EN Cytrynbaum V Rodionov A Mogilner 2004 Computational model of dynein-dependent self-organization of microtubule asters J Cell Sci 117 1381 1397 10.1242/jcs.00919 1:CAS:528:DC%2BD2cXjs12hsbo%3D 14996905 (Pubitemid 38559815)
9. EN Cytrynbaum V Rodionov A Mogilner 2006 Nonlocal mechanism of self-organization and centering of microtubule asters Bull Math Biol 68 1053 1072 10.1007/s11538-006-9092-x 1:CAS:528:DC%2BD28XosFait7o%3D 16832739 (Pubitemid 44195539)
10. M De Brabander G Geuens R Nuydens R Willebrords J De Mey 1981 Taxol induces the assembly of free microtubules in living cells and blocks the organizing capacity of the centrosomes and kinetochores Proc Natl Acad Sci USA 78 5608 5612 10.1073/pnas.78.9.5608 6117858
11. KJ De Vos AJ Grierson S Ackerley CC Miller 2008 Role of axonal transport in neurodegenerative diseases Annu Rev Neurosci 31 151 173 10.1146/annurev. neuro.31.061307.090711 18558852
12. L Dehmelt P Nalbant W Steffen S Halpain 2006 A microtubule-based, dynein-dependent force induces local cell protrusions: implications for neurite initiation Brain Cell Biol 35 39 56 10.1007/s11068-006-9001-0 1:STN:280:DC%2BD2snhs1Ogtw%3D%3D 17940912 (Pubitemid 47012539)
13. H Erez G Malkinson M Prager-Khoutorsky, et al. 2007 Formation of microtubule-based traps controls the sorting and concentration of vesicles to restricted sites of regenerating neurons after axotomy J Cell Biol 176 497 507 10.1083/jcb.200607098 1:CAS:528:DC%2BD2sXhvFCqtr0%3D 17283182 (Pubitemid 46257276)
14. Erez H, Spira ME (2008) Local self-assembly mechanisms underlie the differential transformation of the proximal and distal cut axonal ends into functional and aberrant growth cones. J Comp Neurol 507:spc1
15. Falnikar A, Baas PW (2009) Critical roles for microtubules in axonal development and disease. Results Probl Cell Differ. doi: 10.1007/400-2009-2
16. R Fazio A Quattrini A Bolognesi, et al. 1999 Docetaxel neuropathy: a distal axonopathy Acta Neuropathol 98 651 653 10.1007/s004010051132 1:STN:280:DC%2BD3c%2FmvVeksw%3D%3D 10603043
17. SJ Flatters GJ Bennett 2006 Studies of peripheral sensory nerves in paclitaxel-induced painful peripheral neuropathy: evidence for mitochondrial dysfunction Pain 122 245 257 10.1016/j.pain.2006.01.037 1:CAS:528: DC%2BD28XkvVCqsbg%3D 16530964 (Pubitemid 43729476)
18. M Foss BW Wilcox GB Alsop D Zhang 2008 Taxol crystals can masquerade as stabilized microtubules PLoS ONE 3 e1476 10.1371/journal.pone.0001476 18213384 (Pubitemid 351803439)
19. N Galjart 2005 CLIPs and CLASPs and cellular dynamics Nat Rev Mol Cell Biol 6 487 498 10.1038/nrm1664 1:CAS:528:DC%2BD2MXks1Gmtbk%3D 15928712 (Pubitemid 40780560)
20. D Gitler ME Spira 1998 Real time imaging of calcium-induced localized proteolytic activity after axotomy and its relation to growth cone formation Neuron 20 1123 1135 10.1016/S0896-6273(00)80494-8 1:CAS:528:DyaK1cXktFOksrc%3D 9655501 (Pubitemid 28293130)
21. K Hayashi R Kawai-Hirai K Ishikawa K Takata 2002 Reversal of neuronal polarity characterized by conversion of dendrites into axons in neonatal rat cortical neurons in vitro Neuroscience 110 7 17 10.1016/S0306-4522(01)00592-9 1:CAS:528:DC%2BD38XhslSktbo%3D 11882368 (Pubitemid 34214755)
22. M Hendricks S Jesuthasan 2009 PHR regulates growth cone pausing at intermediate targets through microtubule disassembly J Neurosci 29 6593 6598 10.1523/JNEUROSCI.1115-09.2009 1:CAS:528:DC%2BD1MXmsFent7o%3D 19458229
23. J Jaworski CC Hoogenraad A Akhmanova 2008 Microtubule plus-end tracking proteins in differentiated mammalian cells Int J Biochem Cell Biol 40 619 637 1:CAS:528:DC%2BD1cXivVOmtbk%3D 18023603
24. J Jaworski LC Kapitein SM Gouveia, et al. 2009 Dynamic microtubules regulate dendritic spine morphology and synaptic plasticity Neuron 61 85 100 10.1016/j.neuron.2008.11.013 1:CAS:528:DC%2BD1MXhtlCnu78%3D 19146815
25. MA Jordan K Kamath 2007 How do microtubule-targeted drugs work? An overview Curr Cancer Drug Targets 7 730 742 10.2174/156800907783220417 1:CAS:528:DC%2BD1cXhsFOnsbg%3D 18220533
26. MA Jordan K Wendell S Gardiner, et al. 1996 Mitotic block induced in HeLa cells by low concentrations of paclitaxel (Taxol) results in abnormal mitotic exit and apoptotic cell death Cancer Res 56 816 825 1:CAS:528:DyaK28XhtVClsbo%3D 8631019
27. S Kar J Fan MJ Smith M Goedert LA Amos 2003 Repeat motifs of tau bind to the insides of microtubules in the absence of taxol Embo J 22 70 77 10.1093/emboj/cdg001 1:CAS:528:DC%2BD3sXovFaksQ%3D%3D 12505985 (Pubitemid 36091270)
28. T Kim S Chang 2006 Quantitative evaluation of the mode of microtubule transport in Xenopus neurons Mol Cells 21 76 81 1:CAS:528:DC%2BD28XislSltr4%3D 16511349
29. Y Komarova CO De Groot I Grigoriev, et al. 2009 Mammalian end binding proteins control persistent microtubule growth J Cell Biol 184 691 706 10.1083/jcb.200807179 1:CAS:528:DC%2BD1MXjt12qt7k%3D 19255245
30. JJ Lee SM Swain 2006 Peripheral neuropathy induced by microtubule-stabilizing agents J Clin Oncol 24 1633 1642 10.1200/JCO.2005.04. 0543 1:CAS:528:DC%2BD28XjvFyktLs%3D 16575015 (Pubitemid 46638788)
31. PC Letourneau AH Ressler 1984 Inhibition of neurite initiation and growth by taxol J Cell Biol 98 1355 1362 10.1083/jcb.98.4.1355 1:CAS:528: DyaL2cXhslansro%3D 6143759
32. JW Lewcock N Genoud K Lettieri SL Pfaff 2007 The ubiquitin ligase Phr1 regulates axon outgrowth through modulation of microtubule dynamics Neuron 56 604 620 10.1016/j.neuron.2007.09.009 1:CAS:528:DC%2BD2sXhsVahsbzO 18031680 (Pubitemid 350102027)
33. Lodish H, Berk A, Zipursky L et al (2000) Molecular cell biology, 4th edn. W. H. Freeman, New York
34. Y Ma D Shakiryanova I Vardya SV Popov 2004 Quantitative analysis of microtubule transport in growing nerve processes Curr Biol 14 725 730 10.1016/j.cub.2004.03.061 1:CAS:528:DC%2BD2cXjt1Cmtr8%3D 15084289 (Pubitemid 38503611)
35. EB Masurovsky ER Peterson SM Crain SB Horwitz 1981 Microtubule arrays in taxol-treated mouse dorsal root ganglion-spinal cord cultures Brain Res 217 392 398 10.1016/0006-8993(81)90017-2 1:STN:280:DyaL3M3jsVSjsA%3D%3D 6113880 (Pubitemid 11067811)
36. S Mielke A Sparreboom K Mross 2006 Peripheral neuropathy: a persisting challenge in paclitaxel-based regimes Eur J Cancer 42 24 30 10.1016/j.ejca.2005. 06.030 1:CAS:528:DC%2BD2MXhtlCktLzF 16293411 (Pubitemid 41814529)
37. H Nakagawa K Koyama Y Murata, et al. 2000 EB3, a novel member of the EB1 family preferentially expressed in the central nervous system, binds to a CNS-specific APC homologue Oncogene 19 210 216 10.1038/sj.onc.1203308 1:CAS:528:DC%2BD3cXhtVSitLw%3D 10644998
38. T Nakata H Yorifuji 1999 Morphological evidence of the inhibitory effect of taxol on the fast axonal transport Neurosci Res 35 113 122 10.1016/S0168-0102(99)00074-7 1:CAS:528:DyaK1MXntVChtrc%3D 10616915 (Pubitemid 29518402)
39. F Perez GS Diamantopoulos R Stalder TE Kreis 1999 CLIP-170 highlights growing microtubule ends in vivo Cell 96 517 527 10.1016/S0092-8674(00)80656-X 1:CAS:528:DyaK1MXhsFygtbk%3D 10052454
40. S Pignata S De Placido R Biamonte, et al. 2006 Residual neurotoxicity in ovarian cancer patients in clinical remission after first-line chemotherapy with carboplatin and paclitaxel: the Multicenter Italian Trial in Ovarian cancer (MITO-4) retrospective study BMC Cancer 6 5 10.1186/1471-2407-6-5 16398939 (Pubitemid 43085338)
41. TJ Postma JB Vermorken AJ Liefting HM Pinedo JJ Heimans 1995 Paclitaxel-induced neuropathy Ann Oncol 6 489 494 1:STN:280:DyaK2MzpvFegtQ%3D%3D 7669713
42. AM Rajnicek LE Foubister CD McCaig 2006 Growth cone steering by a physiological electric field requires dynamic microtubules, microfilaments and Rac-mediated filopodial asymmetry J Cell Sci 119 1736 1745 10.1242/jcs.02897 1:CAS:528:DC%2BD28XlsVOnu7c%3D 16595545 (Pubitemid 43811000)
43. G Ruthel PJ Hollenbeck 2003 Response of mitochondrial traffic to axon determination and differential branch growth J Neurosci 23 8618 8624 1:CAS:528:DC%2BD3sXns1Srsb0%3D 13679431
44. Z Sahenk R Barohn P New JR Mendell 1994 Taxol neuropathy. Electrodiagnostic and sural nerve biopsy findings Arch Neurol 51 726 729 1:STN:280:DyaK2c3ovVOlsw%3D%3D 7912506
45. I Sahly H Erez A Khoutorsky E Shapira ME Spira 2003 Effective expression of the green fluorescent fusion proteins in cultured Aplysia neurons J Neurosci Methods 126 111 117 10.1016/S0165-0270(03)00072-4 1:CAS:528:DC%2BD3sXks1Wksr4%3D 12814835 (Pubitemid 36694152)
46. I Sahly A Khoutorsky H Erez M Prager-Khoutorsky ME Spira 2006 On-line confocal imaging of the events leading to structural dedifferentiation of an axonal segment into a growth cone after axotomy J Comp Neurol 494 705 720 10.1002/cne.20690 16374810 (Pubitemid 43054221)
47. A Scuteri G Nicolini M Miloso, et al. 2006 Paclitaxel toxicity in post-mitotic dorsal root ganglion (DRG) cells Anticancer Res 26 1065 1070 1:CAS:528:DC%2BD28XktFWms7k%3D 16619507
48. A Seitz H Kojima K Oiwa, et al. 2002 Single-molecule investigation of the interference between kinesin, tau and MAP2c Embo J 21 4896 4905 10.1093/emboj/cdf503 1:CAS:528:DC%2BD38Xnt1Gnt7g%3D 12234929
49. OA Shemesh H Erez I Ginzburg ME Spira 2008 Tau-induced traffic jams reflect organelles accumulation at points of microtubule polar mismatching Traffic 9 458 471 10.1111/j.1600-0854.2007.00695.x 1:CAS:528: DC%2BD1cXkt1ais70%3D 18182010 (Pubitemid 351351608)
50. C Siau W Xiao GJ Bennett 2006 Paclitaxel- and vincristine-evoked painful peripheral neuropathies: loss of epidermal innervation and activation of Langerhans cells Exp Neurol 201 507 514 10.1016/j.expneurol.2006.05.007 1:CAS:528:DC%2BD28XpslSmurY%3D 16797537 (Pubitemid 44344243)
51. ME Spira A Dormann U Ashery, et al. 1996 Use of Aplysia neurons for the study of cellular alterations and the resealing of transected axons in vitro J Neurosci Methods 69 91 102 10.1016/S0165-0270(96)00024-6 1:STN:280: DyaK2s%2FmvF2muw%3D%3D 8912939 (Pubitemid 26354468)
52. T Stepanova J Slemmer CC Hoogenraad, et al. 2003 Visualization of microtubule growth in cultured neurons via the use of EB3-GFP (end-binding protein 3-green fluorescent protein) J Neurosci 23 2655 2664 1:CAS:528:DC%2BD3sXjtFCntrk%3D 12684451
53. D Takahashi W Yu PW Baas R Kawai-Hirai K Hayashi 2007 Rearrangement of microtubule polarity orientation during conversion of dendrites to axons in cultured pyramidal neurons Cell Motil Cytoskeleton 64 347 359 10.1002/cm.20188 17342761 (Pubitemid 46608669)
54. C Theiss K Meller 2000 Taxol impairs anterograde axonal transport of microinjected horseradish peroxidase in dorsal root ganglia neurons in vitro Cell Tissue Res 299 213 224 10.1007/s004410050019 1:CAS:528:DC%2BD3cXitFCgsbY%3D 10741462 (Pubitemid 30103139)
55. P Verstreken CV Ly KJ Venken, et al. 2005 Synaptic mitochondria are critical for mobilization of reserve pool vesicles at Drosophila neuromuscular junctions Neuron 47 365 378 10.1016/j.neuron.2005.06.018 1:CAS:528: DC%2BD2MXovFSjsL0%3D 16055061 (Pubitemid 41073878)
56. T Williamson PR Gordon-Weeks M Schachner J Taylor 1996 Microtubule reorganization is obligatory for growth cone turning Proc Natl Acad Sci USA 93 15221 15226 10.1073/pnas.93.26.15221 1:CAS:528:DyaK2sXntFCj 8986791 (Pubitemid 27009580)
57. EP Winer DA Berry S Woolf, et al. 2004 Failure of higher-dose paclitaxel to improve outcome in patients with metastatic breast cancer: cancer and leukemia group B trial 9342 J Clin Oncol 22 2061 2068 10.1200/JCO.2004.08.048 1:CAS:528:DC%2BD2cXpsVWls7g%3D 15169793 (Pubitemid 41095138)
58. WH Xiao GJ Bennett 2008 C-fiber spontaneous discharge evoked by chronic inflammation is suppressed by a long-term infusion of lidocaine yielding nanogram per milliliter plasma levels Pain 137 218 228 10.1016/j.pain.2008.02. 018 1:CAS:528:DC%2BD1cXnt1Ohsrc%3D 18395983
59. WH Xiao GJ Bennett 2008 Chemotherapy-evoked neuropathic pain: abnormal spontaneous discharge in A-fiber and C-fiber primary afferent neurons and its suppression by acetyl-l-carnitine Pain 135 262 270 10.1016/j.pain.2007.06.001 1:CAS:528:DC%2BD1cXivFyks7w%3D 17659836 (Pubitemid 351330186)
60. W Yu C Cook C Sauter, et al. 2000 Depletion of a microtubule-associated motor protein induces the loss of dendritic identity J Neurosci 20 5782 5791 1:CAS:528:DC%2BD3cXlt1Glurg%3D 10908619
61. C Zhang A Sriratana T Minamikawa P Nagley 1998 Photosensitisation properties of mitochondrially localised green fluorescent protein Biochem Biophys Res Commun 242 390 395 10.1006/bbrc.1997.7970 1:CAS:528: DyaK1cXkslGnug%3D%3D 9446805 (Pubitemid 28412438)
62. Y Zheng J Wildonger B Ye, et al. 2008 Dynein is required for polarized dendritic transport and uniform microtubule orientation in axons Nat Cell Biol 10 1172 1180 10.1038/ncb1777 1:CAS:528:DC%2BD1cXhtFyqurvE 18758451
63. NE Ziv ME Spira 1997 Localized and transient elevations of intracellular Ca2+ induce the dedifferentiation of axonal segments into growth cones J Neurosci 17 3568 3579 1:CAS:528:DyaK2sXjt1Wksbw%3D 9133380