Microtubule-severing ATPase spastin in glioblastoma: Increased expression in human glioblastoma cell lines and inverse roles in cell motility and proliferation

Journal of Neuropathology and Experimental Neurology

Volumn 70, Issue 9, 2011, Pages 811-826

  Dráberová, Eduarda ^a   Vinopal, Stanislav ^a   Morfini, Gerardo ^g   Liu, Pei S ^c   Sládková, Vladimíra ^a   Sulimenko, Tetyana ^a   Burns, Matthew R ^g   Solowska, Joanna ^c   Kulandaivel, Kandan ^c   De Chadarévian, Jean Pierre ^d,e   Legido, Agustin ^c,e   Mörk, Sverre J ^h   Janáček, Jiří ^b   Baas, Peter W ^c   Dráber, Pavel ^a   Katsetos, Christos D ^c,d,e,f  

^a INSTITUTE OF MOLECULAR GENETICS   (Czech Republic)

^b INSTITUTE OF PHYSIOLOGY   (Czech Republic)

^c Department of Neurology ^*  (United States)

^d Laboratory Medicine   (United States)

^e ST CHRISTOPHER'S HOSPITAL FOR CHILDREN   (United States)

^f HAHNEMANN UNIVERSITY HOSPITAL   (United States)

^g UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^h UNIVERSITY OF BERGEN   (Norway)

Author keywords

Astrocyte; Brain tumor; Cell motility; Glioblastoma; Glioma; Microtubule severing; Spastin

Indexed keywords

ISOPROTEIN; MESSENGER RNA; SPASTIN; SPASTIN M1 ISOPROTEIN; SPASTIN M87 ISOPROTEIN; UNCLASSIFIED DRUG;

ARTICLE; ASTROCYTOMA; BRAIN LEVEL; CELL MOTILITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM; DENDRITE; GLIA; GLIOBLASTOMA; GLIOMA CELL; HUMAN; HUMAN CELL; IMMUNOBLOTTING; INTERPHASE; MICROFILAMENT; MICROTUBULE; MITOSIS SPINDLE; NERVE CELL; NEUROPIL; NUCLEOTIDE SEQUENCE; PERIKARYON; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PURKINJE CELL; REAL TIME POLYMERASE CHAIN REACTION; SYNAPSE; TUMOR GROWTH;

ADENOSINE TRIPHOSPHATASES; AGE FACTORS; BRAIN; BRAIN NEOPLASMS; CELL COUNT; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; CHILD; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GLIOBLASTOMA; HUMANS; INFANT; MALE; MICROTUBULES; MIDDLE AGED; RNA, MESSENGER; YOUNG ADULT;

EID: 80052150163     PISSN: 00223069     EISSN: 15546578     Source Type: Journal    
DOI: 10.1097/NEN.0b013e31822c256d     Document Type: Article

References (60)

1. Ohgaki H, Kleihues P. Population-based studies on incidence, survival rates, and genetic alterations in astrocytic and oligodendroglial gliomas. J Neuropathol Exp Neurol 2005;64:479-89 (Pubitemid 40781150)
2. Jordan MA, Wilson L. Microtubules and actin filaments: Dynamic targets for cancer chemotherapy. Curr Opin Cell Biol 1998;10:123-30 (Pubitemid 28066130)
3. Pasquier E, Kavallaris M. Microtubules: A dynamic target in cancer therapy. IUBMB Life 2008;60:165-70
4. Dumontet C, Jordan MA. Microtubule-binding agents: A dynamic field of cancer therapeutics. Nat Rev Drug Discov 2010;9:790-803
5. Baas PW, Karabay A, Qiang L. Microtubules cut and run. Trends Cell Biol 2005;15:518-24 (Pubitemid 41396433)
6. Whipple RA, Cheung AM, Martin SS. Detyrosinated microtubule protrusions in suspended mammary epithelial cells promote reattachment. Exp Cell Res 2007;313:1326-36 (Pubitemid 46509778)
7. Schoumacher M, Goldman RD, Louvard D, et al. Actin, microtubules, and vimentin intermediate filaments cooperate for elongation of invadopodia. J Cell Biol 2010;189:541-56
8. Liaw TY, Chang MH, Kavallaris M. The cytoskeleton as a therapeutic target in childhood acute leukemia: Obstacles and opportunities. Curr Drug Targets 2007;8:739-49 (Pubitemid 47603403)
9. Ferlini C, Raspaglio G, Cicchillitti L, et al. Looking at drug resistance mechanisms for microtubule interacting drugs: Does TUBB3 work? Curr Cancer Drug Targets 2007;7:704-12
10. Katsetos CD, Draberova E, Legido A, et al. Tubulin targets in the pathobiology and therapy of glioblastoma multiforme. I. Class III A-tubulin. J Cell Physiol 2009;221:505-13
11. Kavallaris M. Microtubules and resistance to tubulin-binding agents. Nat Rev Cancer 2010;10:194-204
12. Regina A, Demeule M, Che C, et al. Antitumour activity of ANG1005, a conjugate between paclitaxel and the new brain delivery vector Angiopep-2. Br J Pharmacol 2008;155:185-97
13. Mielke S, Sparreboom A, Mross K. Peripheral neuropathy: A persisting challenge in paclitaxel-based regimes. Eur J Cancer 2006;42:24-30 (Pubitemid 41814529)
14. Richter-Landsberg C. The cytoskeleton in oligodendrocytes. Microtubule dynamics in health and disease. J Mol Neurosci 2008;35:55-63
15. Shi J, Orth JD, Mitchison T. Cell type variation in responses to antimitotic drugs that target microtubules and kinesin-5. Cancer Res 2008;68: 3269-76
16. Hornick JE, Karanjeet K, Collins ES, et al. Kinesins to the core: The role of microtubule-based motor proteins in building the mitotic spindle midzone. Semin Cell Dev Biol 2010;21:290-99
17. Baas PW, Sudo H. More microtubule severing proteins: More microtubules. Cell Cycle 2010;9:2271-74
18. Claudiani P, Riano E, Errico A, et al. Spastin subcellular localization is regulated through usage of different translation start sites and active export from the nucleus. Exp Cell Res 2005;309:358-69 (Pubitemid 41317359)
19. White SR, Evans KJ, Lary J, et al. Recognition of C-terminal amino acids in tubulin by pore loops in Spastin is important for microtubule severing. J Cell Biol 2007;176:995-1005 (Pubitemid 46506972)
20. Svenson IK, Ashley-Koch AE, Gaskell PC, et al. Identification and expression analysis of spastin gene mutations in hereditary spastic paraplegia. Am J Hum Genet 2001;68:1077-85 (Pubitemid 32424406)
21. Salinas S, Carazo-Salas RE, Proukakis C, et al. Human spastin has multiple microtubule-related functions. J Neurochem 2005;95:1411-20 (Pubitemid 41779265)
22. Solowska JM, Morfini G, Falnikar A, et al. Quantitative and functional analyses of spastin in the nervous system: Implications for hereditary spastic paraplegia. J Neurosci 2008;28:2147-57 (Pubitemid 351317638)
23. Hazan J, Fonknechten N, Mavel D, et al. Spastin, a new AAA protein, is altered in the most frequent form of autosomal dominant spastic paraplegia. Nat Genet 1999;23:296-303 (Pubitemid 29526426)
24. Wharton SB, McDermott CJ, Grierson AJ, et al. The cellular and molecular pathology of the motor system in hereditary spastic paraparesis due to mutation of the spastin gene. J Neuropathol Exp Neurol 2003; 62:1166-77 (Pubitemid 37413827)
25. Ma DL, Chia SC, Tang YC, et al. Spastin in the human and mouse central nervous system with special reference to its expression in the hippocampus of mouse pilocarpine model of status epilepticus and temporal lobe epilepsy. Neurochem Int 2006;49:651-64 (Pubitemid 44572567)
26. Encinas M, Iglesias M, Liu Y, et al. Sequential treatment of SH-SY5Y cells with retinoic acid and brain-derived neurotrophic factor gives rise to fully differentiated, neurotrophic factorYdependent, human neuron-like cells. J Neurochem 2000;75:991-1003 (Pubitemid 30660487)
27. Draberova E, Del Valle L, Gordon J, et al. Class III A-tubulin is constitutively coexpressed with glial fibrillary acidic protein and nestin in midgestational human fetal astrocytes: Implications for phenotypic identity. J Neuropathol Exp Neurol 2008;67:341-54 (Pubitemid 351507489)
28. Viklick] V, Draber P, Haxek J, et al. Production and characterization of a monoclonal antitubulin antibody. Cell Biol Int Rep 1982;6:725-31 (Pubitemid 13200897)
29. Draber P, Draberova E, Zicconi D, et al. Heterogeneity of microtubules recognized by monoclonal antibodies to α-tubulin. Eur J Cell Biol 1986; 41:82-88
30. Draber P, Draberova E, Viklick] V. Immunostaining of human spermatozoa with tubulin domain-specific monoclonal antibodies. Recognition of a unique A-tubulin epitope in the sperm head. Histochemistry 1991;95: 519-24
31. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970;227:680-85
32. Draber P, Lagunowich LA, Draberova E, et al. Heterogeneity of tubulin epitopes in mouse fetal tissues. Histochemistry 1988;89:485-92
33. Draberova E, Draber P. A microtubule-interacting protein involved in coalignment of vimentin intermediate filaments with microtubules. J Cell Sci 1993;106:1263-73 (Pubitemid 24018411)
34. Soile P. Morphological Image Analysis. 2nd ed. Berlin, Germany: Springer, 2003
35. Katsetos CD, Del Valle L, Geddes JF, et al. Aberrant localization of the neuronal class III A-tubulin in astrocytomas. Arch Pathol Lab Med 2001;125:613-24
36. Katsetos CD, Reddy G, Draberova E, et al. Altered cellular distribution and subcellular sorting of F-tubulin in diffuse astrocytic gliomas and human glioblastoma cell lines. J Neuropathol Exp Neurol 2006;65:465-77 (Pubitemid 44297268)
37. Katsetos CD, Draberova E, wmejkalova B, et al. Class III A-tubulin and F-tubulin are co-expressed and form complexes in human glioblastoma cells. Neurochem Res 2007;32:1387-98 (Pubitemid 46988201)
38. Louis DN, Ohgaki H, Wiestler OD, et al. The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol 2007; 114:97-109 (Pubitemid 47103521)
39. Fleiss JG. Statistical Methods for Rates and Proportions. New York, NY: Wiley, 1981:225-32
40. Landis JR, Koch GG. The measurement of observer agreement for categorical data. Biometrics 1977;33:159-74 (Pubitemid 8054849)
41. Trotta N, Orso G, Rossetto MG, et al. The hereditary spastic paraplegia gene, spastin, regulates microtubule stability to modulate synaptic structure and function. Curr Biol 2004;14:1135-47 (Pubitemid 38893976)
42. Quick Q, Skalli O. α-Actinin 1 and α-actinin 4: Contrasting roles in the survival, motility, and RhoA signaling of astrocytoma cells. Exp Cell Res 2010;316:1137-47
43. Pan Y, Jing R, Pitre A, et al. Intermediate filament protein synemin contributes to the migratory properties of astrocytoma cells by influencing the dynamics of the actin cytoskeleton. FASEB J 2008;22:3196-206
44. Berens ME, Beaudry C. Radial monolayer cell migration assay. Methods Mol Med 2004;88:219-24
45. Zhang D, Grode KD, Stewman SF, et al. Drosophila katanin is a microtubule depolymerase that regulates cortical-microtubule plus-end interactions and cell migration. Nat Cell Biol 2011;13:361-70
46. Giese A, Bjerkvig R, Berens ME, et al. Cost of migration: Invasion of malignant gliomas and implications for treatment. J Clin Oncol 2003; 21:1624-36 (Pubitemid 46594118)
47. Berens ME, Giese A. "Ithose left behind." Biology and oncology of invasive glioma cells. Neoplasia 1999;1:208-19
48. Nigg EA. Centrosome aberrations: Cause or consequence of cancer progression? Nat Rev Cancer 2002;2:815-25 (Pubitemid 37328900)
49. Ahmad FJ, Yu W, McNally FJ, et al. An essential role for katanin in severing microtubules in the neuron. J Cell Biol 1999;145:305-15 (Pubitemid 29198303)
50. Yu W, Ahmad FJ, Baas PW. Microtubule fragmentation and partitioning in the axon during collateral branch formation. J Neurosci 1994;14:5872-84 (Pubitemid 24307784)
51. Dent EW, Callaway JL, Szebenyi G, et al. Reorganization and movement of microtubules in axonal growth cones and developing interstitial branches. J Neurosci 1999;19:8894-908 (Pubitemid 30226711)
52. Errico A, Claudiani P, D'Addio M, et al. Spastin interacts with the centrosomal protein NA14, and is enriched in the spindle pole, the midbody and the distal axon. Hum Mol Genet 2004;13:2121-32 (Pubitemid 39377834)
53. Roll-Mecak A, Vale RD. Making more microtubules by severing: A common theme of noncentrosomal microtubule arrays? J Cell Biol 2006; 175:849-51 (Pubitemid 44969190)
54. Roll-Mecak A, McNally FJ. Microtubule-severing enzymes. Curr Opin Cell Biol 2010;22:96-103
55. Katsetos CD, Draberova E, Legido A, et al. Tubulin targets in the pathobiology and therapy of glioblastoma multiforme. II. F-Tubulin. J Cell Physiol 2009;221:514-20
56. Cho EH, Whipple RA, Matrone MA, et al. Delocalization of F-tubulin due to increased solubility in human breast cancer cell lines. Cancer Biol Ther 2010;9:66-76
57. Joshi HC, Palacios MJ, McNamara L, et al. F-Tubulin is a centrosomal protein required for cell cycleYdependent microtubule nucleation. Nature 1992;356:80-83
58. Zheng Y, Wong ML, Alberts B, et al. Nucleation of microtubule assembly by a F-tubulinYcontaining ring complex. Nature 1995;378:578-83
59. Chabin-Brion K, Marceiller J, Perez F, et al. The Golgi complex is a microtubule-organizing organelle. Mol Biol Cell 2001;12:2047-60 (Pubitemid 33049698)
60. Macurek L, Draberova E, Richterova V, et al. Regulation of microtubule nucleation in differentiating embryonal carcinoma cells by complexes of membrane-bound F-tubulin with Fyn kinase and phosphoinositide 3-kinase. Biochem J 2008;416:421-0