End-binding 1 protein overexpression correlates with glioblastoma progression and sensitizes to Vinca-alkaloids in vitro and in vivo

Oncotarget

Volumn 5, Issue 24, 2014, Pages 12769-12787

  Berges, Raphael ^a   Baeza Kallee, Nathalie ^a   Tabouret, Emeline ^a,b   Chinot, Olivier ^a,b   Petit, Marie ^a,b   Kruczynski, Anna ^c   Figarella Branger, Dominique ^a,b   Honore, Stephane ^a,b   Braguer, Diane ^a,b  

^a University of the Mediterranean Aix Marseille II   (France)

^b TIMONE HOSPITAL   (France)

^c INSTITUT DE RECHERCHE PIERRE FABRE   (France)

Author keywords

Biomarker; EB1; Glioblastoma; Microtubules; Vinca alkaloid

Indexed keywords

BINDING PROTEIN; END BINDING 1 PROTEIN; TEMOZOLOMIDE; UNCLASSIFIED DRUG; VINCRISTINE; VINFLUNINE; MAPRE1 PROTEIN, HUMAN; MICROTUBULE ASSOCIATED PROTEIN; VINBLASTINE; VINCA ALKALOID;

ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CANCER PROGNOSIS; CANCER SURVIVAL; CARCINOGENICITY; CELL PROLIFERATION; CHEMOSENSITIZATION; CONTROLLED STUDY; DRUG RESPONSE; FEMALE; GLIOBLASTOMA; GROWTH RATE; HUMAN; HUMAN CELL; IMMUNOHISTOLOGY; IN VITRO STUDY; IN VIVO STUDY; MAJOR CLINICAL STUDY; MALE; MIGRATION INHIBITION; MITOSIS INHIBITION; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; OVERALL SURVIVAL; PROGRESSION FREE SURVIVAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; ANALOGS AND DERIVATIVES; ANIMAL; BIOSYNTHESIS; BRAIN NEOPLASMS; CELL MOTION; DISEASE COURSE; DISEASE FREE SURVIVAL; DRUG EFFECTS; DRUG SCREENING; GENETICS; METABOLISM; NUDE MOUSE; PATHOLOGY; TUMOR CELL LINE;

ANIMALS; BRAIN NEOPLASMS; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; DISEASE PROGRESSION; DISEASE-FREE SURVIVAL; FEMALE; GLIOBLASTOMA; HUMANS; IN VITRO TECHNIQUES; MICE; MICE, NUDE; MICROTUBULE-ASSOCIATED PROTEINS; VINBLASTINE; VINCA ALKALOIDS; VINCRISTINE; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84921415603     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.2646     Document Type: Article

References (49)

1. Akhmanova A, Steinmetz MO. Microtubule +TIPs at a glance. J Cell Sci. 2010; 123:3415-3419.
2. Morrison EE. Action and interactions at microtubule ends. Cell Mol Life Sci. 2007; 64:307-317.
3. Su LK, Qi Y. Characterization of human MAPRE genes and their proteins. Genomics. 2001; 71:142-149.
4. Panopoulos A, Howell M, Fotedar R, Margolis RL. Gliobla stoma motility occurs in the absence of actin polymer. Mol Biol Cell. 2011; 22:2212-2220.
5. Pagano A, Honore S, Mohan R, Berges R, Akhmanova A, Braguer D. Epothilone B inhibits migration of glioblastoma cells by inducing microtubule catastrophes and affecting EB1 accumulation at microtubule plus ends. Biochem Pharmacol. 2012; 84:432-443.
6. Rovini A, Gauthier G, Berges R, Kruczynski A, Braguer D, Honore S. Anti-Migratory Effect of Vinflunine in Endothelial and Glioblastoma Cells Is Associated with Changes in EB1 C-Terminal Detyrosinated/Tyrosinated Status. PLoS One. 2013; 8:e65694.
7. Mohan R, Katrukha EA, Doodhi H, Smal I, Meijering E, Kapitein LC, Steinmetz MO, Akhmanova A. Endbinding proteins sensitize microtubules to the action of microtubule-targeting agents. Proc Natl Acad Sci U S A. 2013; 110:8900-8905.
8. Dong X, Liu F, Sun L, Liu M, Li D, Su D, Zhu Z, Dong JT, Fu L, Zhou J. Oncogenic function of microtubule end-binding protein 1 in breast cancer. J Pathol. 2010; 220:361-369.
9. Wang Y, Zhou X, Zhu H, Liu S, Zhou C, Zhang G, Xue L, Lu N, Quan L, Bai J, Zhan Q, Xu N. Overexpression of EB1 in human esophageal squamous cell carcinoma (ESCC) may promote cellular growth by activating betacatenin/ TCF pathway. Oncogene. 2005; 24:6637-6645.
10. Nishigaki R, Osaki M, Hiratsuka M, Toda T, Murakami K, Jeang KT, Ito H, Inoue T, Oshimura M. Proteomic identification of differentiallyexpressed genes in human gastric carcinomas. Proteomics. 2005; 5:3205-3213.
11. Sugihara Y, Taniguchi H, Kushima R, Tsuda H, Kubota D, Ichikawa H, Sakamoto K, Nakamura Y, Tomonaga T, Fujita S, Kondo T. Proteomic-based identification of the APC-binding protein EB1 as a candidate of novel tissue biomarker and therapeutic target for colorectal cancer. J Proteomics. 2012; 75:5342-5355.
12. Fujii K, Kondo T, Yokoo H, Yamada T, Iwatsuki K, Hirohashi S. Proteomic study of human hepatocellular carcinoma using two-dimensional difference gel electrophoresis with saturation cysteine dye. Proteomics. 2012; 5:1411-1422.
13. Orimo T, Ojima H, Hiraoka N, Saito S, Kosuge T, Kakisaka T, Yokoo H, Nakanishi K, Kamiyama T, Todo S, Hirohashi S, Kondo T. Proteomic profiling reveals the prognostic value of adenomatous polyposis coli-endbinding protein 1 in hepatocellular carcinoma. Hepatology. 2008; 48:1851-1863.
14. Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, Belanger K, Brandes AA, Marosi C, Bogdahn U, Curschmann J, Janzer RC, Ludwin SK, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med. 2005; 352:987-996.
15. van den Bent MJ, Brandes AA, Taphoorn MJ, Kros JM, Kouwenhoven MC, Delattre JY, Bernsen HJ, Frenay M, Tijssen CC, Grisold W, Sipos L, Enting RH, FrenchPJ, et al. Adjuvant procarbazine, lomustine, and vincristine chemotherapy in newly diagnosed anaplastic oligodendroglioma: long-term follow-up of EORTC brain tumor group study 26951. J Clin Oncol. 2013; 31:344-350.
16. Tchoghandjian A, Baeza N, Colin C, Cayre M, Metellus P, Beclin C, Ouafik L, Figarella-Branger D. A2B5 cells from human glioblastoma have cancer stem cell properties. Brain Pathol. 2010; 20:211-221.
17. Tchoghandjian A, Baeza-Kallee N, Beclin C, Metellus P, Colin C, Ducray F, Adelaide J, Rougon G, Figarella-Branger D. Cortical and subventricular zone glioblastoma-derived stem-like cells display different molecular profiles and differential in vitro and in vivo properties. Ann Surg Oncol. 2012; 19 :S608-619.
18. Hartmann C, Meyer J, Balss J, Capper D, Mueller W, Christians A, Felsberg J, Wolter M, Mawrin C, Wick W, Weller M, Herold-Mende C, Unterberg A. Type and frequency of IDH1 and IDH2 mutations are related to astrocytic and oligodendroglial differentiation and age: a study of 1,010 diffuse gliomas. Acta Neuropathol. 2009; 118:469-74.
19. Capper D, Weissert S, Balss J, Habel A, Meyer J, Jäger D, Ackermann U, Tessmer C, Korshunov A, Zentgraf H, Hartmann C, von Deimling A, et al. Characterization of R132H mutation-specific IDH1 antibody binding in brain tumors. Brain Pathol. 2010; 20:245-54.
20. Parsons DW, Jones S, Zhang X, Lin JC, Leary RJ, Angenendt P, Mankoo P, Carter H, Siu IM, Gallia GL, Olivi A, McLendon R, Rasheed BA, et al. An integrated genomic analysis of human glioblastoma multiforme. Science. 2008; 321:1807-12.
21. Gorlia T, van den Bent MJ, Hegi ME, Mirimanoff RO, Weller M, Cairncross JG, Eisenhauer E, Belanger K, Brandes AA, Allgeier A, Lacombe D, Stupp R. Nomograms for predicting survival of patients with newly diagnosed glioblastoma: prognostic factor analysis of EORTC and NCIC trial 26981-22981/CE.3. Lancet Oncol. 2008; 9:29-38.
22. Rivera AL, Pelloski CE, Gilbert MR, Colman H, De La Cruz C, Sulman EP, Bekele BN, Aldape KD. MGMT promoter methylation is predictive of response to radiotherapy and prognostic in the absence of adjuvant alkylating chemotherapy for glioblastoma. Neuro Oncol. 2010; 12:116-21.
23. Wen Y, Eng CH, Schmoranzer J, Cabrera-Poch N, Morris EJ, Chen M, Wallar BJ, Alberts AS, Gundersen GG. EB1 and APC bind to mDia to stabilize microtubules downstream of Rho and promote cell migration. Nat Cell Biol. 2004; 6:820-830.
24. Zaoui K, Benseddik K, Daou P, Salaun D, Badache A. ErbB2 receptor controls microtubule capture by recruiting ACF7 to the plasma membrane of migrating cells. Proc Natl Acad Sci U S A. 2010; 107:18517-18522.
25. Zaoui K, Honore S, Isnardon D, Braguer D, Badache A. Memo-RhoA-mDia1 signaling controls microtubules, the actin network, and adhesion site formation in migrating cells. J Cell Biol. 2008; 183: 401-408.
26. Liu M, Yang S, Wang Y, Zhu H, Yan S, Zhang W, Quan L, Bai J, Xu N. EB1 acts as an oncogene via activating beta-catenin/TCF pathway to promote cellular growth and inhibit apoptosis. Mol Carcinog. 2009; 48:212-219.
27. Zeng WF, Navaratne K, Prayson RA, Weil RJ. Aurora B expression correlates with aggressive behaviour in glioblastoma multiforme. J Clin Pathol. 2007; 60:218-221.
28. Katsetos CD, Dráberová E, Smejkalová B, Reddy G, Bertrand L, de Chadarévian JP, Legido A, Nissanov J, Baas PW, Dráber P. Class III beta-tubulin and gamma-tubulin are co-expressed and form complexes in human glioblastoma cells. Neurochem Res. 2007; 32:1387-98.
29. Dráberová E, Vinopal S, Morfini G, Liu PS, Sládková V, Sulimenko T, Burns MR, Solowska J, Kulandaivel K, de Chadarévian JP, Legido A, Mörk SJ, Janácek J, et al. Microtubule-severing ATPase spastin in glioblastoma: increased expression in human glioblastoma cell lines and inverse roles in cell motility and proliferation. J Neuropathol Exp Neurol. 2011; 70:811-26.
30. Bouissou A, Vérollet C, de Forges H, Haren L, Bellaïche Y, Perez F, Merdes A, Raynaud-Messina B. Gamma-Tubulin Ring Complexes and EB1 play antagonistic roles in microtubule dynamics and spindle positioning. EMBO J. 2014; 33:114-28.
31. Maurer SP, Cade NI, Bohner G, Gustafsson N, Boutant E, Surrey T. EB1 accelerates two conformational transitions important for microtubule maturation and dynamics. Curr Biol. 2014; 24:372-84.
32. Rovini A, Gauthier G, Bergès R, Kruczynski A, Braguer D, Honoré S. Anti-migratory effect of vinflunine in endothelial and glioblastoma cells is associated with changes in EB1 C-terminal detyrosinated/tyrosinated status. PLoS One. 2013; 4:8.
33. Le Grand M, Rovini A, Bourgarel-Rey V, Honore S, Bastonero S, Braguer D, Carre M. ROS-mediated EB1 phosphorylation through Akt/GSK3β pathway: implication in cancer cell response to microtubule-targeting agents. Oncotarget.2014; 30;5:3408-23.
34. Sun L, Gao J, Dong X, Liu M, Li D, Shi X, Dong JT, Lu X, Liu C, Zhou J. EB1 promotes Aurora-B kinase activity through blocking its inactivation by protein phosphatase 2A. Proc Natl Acad Sci U S A. 2008; 105:7153-8.
35. Mialhe A, Lafanechere L, Treilleux I, Peloux N, Dumontet C, Bremond A, Panh MH, Payan R, Wehland J, Margolis RL, Job D. Tubulin detyrosination is a frequent occurrence in breast cancers of poor prognosis. Cancer Res. 2001; 61:5024-5027.
36. Bieling P, Kandels-Lewis S, Telley IA, van Dijk J, Janke C, Surrey T. CLIP-170 tracks growing microtubule ends by dynamically recognizing composite EB1/tubulin-binding sites. J Cell Biol. 2008; 183:1223-1233.
37. Calligaris D, Manatschal C, Marcellin M, Villard C, Monsarrat B, Burlet-Schiltz O, Steinmetz MO, Braguer D, Lafitte D, Verdier-Pinard P. Tyrosine-dependent capture of CAP-Gly domain-containing proteins in complex mixture by EB1 C-terminal peptidic probes. J Proteomics. 2012; 75:3605-3616.
38. Peris L, Thery M, Faure J, Saoudi Y, Lafanechere L, Chilton JK, Gordon-Weeks P, Galjart N, Bornens M, Wordeman L, Wehland J, Andrieux A, Job D. Tubulin tyrosination is a major factor affecting the recruitment of CAP-Gly proteins at microtubule plus ends. J Cell Biol. 2006; 174:839-849.
39. Kleihues P, Sobin LH. World Health Organization classification of tumors. Cancer. 2000; 88:2887.
40. Colin C, Voutsinos-Porche B, Nanni I, Fina F, Metellus P, Intagliata D, Baeza N, Bouvier C, Delfino C, Loundou A, Chinot O, Lah T, Kos J, et al. High expression of cathepsin B and plasminogen activator inhibitor type-1 are strong predictors of survival in glioblastomas. Acta Neuropathol. 2009; 118:745-754.
41. Ducray F, de Reynies A, Chinot O, Idbaih A, Figarella-Branger D, Colin C, Karayan-Tapon L, Chneiweiss H, Wager M, Vallette F, Marie Y, Rickman D, Thomas E, et al. An ANOCEF genomic and transcriptomic microarray study of the response to radiotherapy or to alkylating first-line chemotherapy in glioblastoma patients. Mol Cancer. 2010; 9:234.
42. Macdonald DR, Cascino TL, Schold SC, Jr., Cairncross JG. Response criteria for phase II studies of supratentorial malignant glioma. J Clin Oncol. 1990; 8:1277-1280.
43. Baeza N, Weller M, Yonekawa Y, Kleihues P, Ohgaki H. PTEN methylation and expression in glioblastomas. Acta Neuropathol. 2003; 106:479-485.
44. Berges R, Balzeau J, Peterson AC, Eyer J. A tubulin binding peptide targets glioma cells disrupting their microtubules, blocking migration, and inducing apoptosis. Mol Ther. 2012; 20:1367-1377.
45. Vichai V, Kirtikara K. Sulforhodamine B colorimetric assay for cytotoxicity screening. Nat Protoc. 2006; 1:1112-1116.
46. Jiang F, Zhang X, Kalkanis SN, Zhang Z, Yang H, Katakowski M, Hong X, Zheng X, Zhu Z, Chopp M. Combination therapy with antiangiogenic treatment and photodynamic therapy for the nude mouse bearing U87 glioblastoma. Photochem Photobiol. 2008; 84:128-137.
47. Kruczynski A, Poli M, Dossi R, Chazottes E, Berrichon G, Ricome C, Giavazzi R, Hill BT, Taraboletti G. Antiangiogenic, vascular-disrupting and anti-metastatic activities of vinflunine, the latest vinca alkaloid in clinical development. Eur J Cancer. 2006; 42:2821-2832.
48. Redgate ES, Deutsch M, Boggs SS. Time of death of CNS tumor-bearing rats can be reliably predicted by body weight-loss patterns. Lab Anim Sci. 1991; 41:269-273.
49. Applegate KT, Besson S, Matov A, Bagonis MH, Jaqaman K, Danuser G. Plus Tip Tracker: Quantitative image analysis software for the measurement of microtubule dynamics. J Struct Biol. 2011; 176:168-84.