Fibroblast growth factor 13 regulates glioma cell invasion and is important for bevacizumab-induced glioma invasion

Oncogene

Volumn 37, Issue 6, 2018, Pages 777-786

  Otani, Y ^a   Ichikawa, T ^a   Kurozumi, K ^a   Inoue, S ^b   Ishida, J ^a   Oka, T ^a   Shimizu, T ^a   Tomita, Y ^a   Hattori, Y ^a   Uneda, A ^a   Matsumoto, Y ^a   Michiue, H ^a   Date, I ^a  

^a OKAYAMA UNIVERSITY   (Japan)

^b Okayama Citizens Hospital   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BEVACIZUMAB; FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 13; TUBULIN; UNCLASSIFIED DRUG; TUMOR MARKER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CARCINOGENESIS; CELL INFILTRATION; CELL MIGRATION; CELL VIABILITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; GENE EXPRESSION; GLIOMA CELL LINE; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; J3T 1 CELL LINE; J3T 2 CELL LINE; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; OVERALL SURVIVAL; PRIORITY JOURNAL; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR INVASION; WESTERN BLOTTING; ANIMAL; APOPTOSIS; BRAIN TUMOR; CANCER STEM CELL; CELL MOTION; CELL PROLIFERATION; DRUG EFFECT; DRUG SCREENING; FEMALE; FOLLOW UP; GENE EXPRESSION REGULATION; GENETICS; GLIOBLASTOMA; METABOLISM; PATHOLOGY; PROGNOSIS; SCID MOUSE; TUMOR CELL CULTURE;

ANIMALS; APOPTOSIS; BEVACIZUMAB; BIOMARKERS, TUMOR; BRAIN NEOPLASMS; CELL MOVEMENT; CELL PROLIFERATION; FEMALE; FIBROBLAST GROWTH FACTORS; FOLLOW-UP STUDIES; GENE EXPRESSION REGULATION, NEOPLASTIC; GLIOBLASTOMA; HUMANS; MICE; MICE, SCID; NEOPLASM INVASIVENESS; NEOPLASTIC STEM CELLS; PROGNOSIS; TUMOR CELLS, CULTURED; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 85041497955     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2017.373     Document Type: Article

References (44)

1. Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 2005; 352: 987-996.
2. Chinot OL, Wick W, Mason W, Henriksson R, Saran F, Nishikawa R et al. Bevacizumab plus radiotherapy-temozolomide for newly diagnosed glioblastoma. N Engl J Med 2014; 370: 709-722.
3. Gilbert MR, Dignam JJ, Armstrong TS, Wefel JS, Blumenthal DT, Vogelbaum MA et al. A randomized trial of bevacizumab for newly diagnosed glioblastoma. N Engl J Med 2014; 370: 699-708.
4. Piao Y, Liang J, Holmes L, Zurita AJ, Henry V, Heymach JV et al. Glioblastoma resistance to anti-VEGF therapy is associated with myeloid cell infiltration, stem cell accumulation, and a mesenchymal phenotype. Neuro Oncol 2012; 14: 1379-1392.
5. Onishi M, Ichikawa T, Kurozumi K, Fujii K, Yoshida K, Inoue S et al. Bimodal antiglioma mechanisms of cilengitide demonstrated by novel invasive glioma models. Neuropathology 2013; 33: 162-174.
6. Ishida J, Onishi M, Kurozumi K, Ichikawa T, Fujii K, Shimazu Y et al. Integrin inhibitor suppresses bevacizumab-induced glioma invasion. Transl Oncol 2014; 7: e1.
7. Scherer HJ. A critical review: the pathology of cerebral gliomas. J Neurol Psychiatry 1940; 3: 147-177.
8. Inoue S, Ichikawa T, Kurozumi K, Maruo T, Onishi M, Yoshida K et al. Novel animal glioma models that separately exhibit two different invasive and angiogenic phenotypes of human glioblastomas. World Neurosurg 2012; 78: 670-682.
9. Maruo T, Ichikawa T, Kanzaki H, Inoue S, Kurozumi K, Onishi M et al. Proteomicsbased analysis of invasion-related proteins in malignant gliomas. Neuropathology 2013; 33: 264-275.
10. Onishi M, Ichikawa T, Kurozumi K, Date I. Angiogenesis and invasion in glioma. Brain Tumor Pathol 2011; 28: 13-24.
11. Onishi M, Ichikawa T, Kurozumi K, Inoue S, Maruo T, Otani Y et al. Annexin A2 regulates angiogenesis and invasion phenotypes of malignant glioma. Brain Tumor Pathol 2015; 32: 184-194.
12. Smallwood PM, Munoz-Sanjuan I, Tong P, Macke JP, Hendry SH, Gilbert DJ et al. Fibroblast growth factor (FGF) homologous factors: new members of the FGF family implicated in nervous system development. Proc Natl Acad Sci USA 1996; 93: 9850-9857.
13. Nishimoto S, Nishida E. Fibroblast growth factor 13 is essential for neural differentiation in Xenopus early embryonic development. J Biol Chem 2007; 282: 24255-24261.
14. Wu QF, Yang L, Li S, Wang Q, Yuan XB, Gao X et al. Fibroblast growth factor 13 is a microtubule-stabilizing protein regulating neuronal polarization and migration. Cell 2012; 149: 1549-1564.
15. Fujimura A, Michiue H, Cheng Y, Uneda A, Tani Y, Nishiki T et al. Cyclin G2 promotes hypoxia-driven local invasion of glioblastoma by orchestrating cytoskeletal dynamics. Neoplasia 2013; 15: 1272-1281.
16. 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.
17. Katsetos CD, Reginato MJ, Baas PW, D'Agostino L, Legido A, Tuszyn Ski JA et al. Emerging microtubule targets in glioma therapy. Semin Pediatr Neurol 2015; 22: 49-72.
18. Wakimoto H, Mohapatra G, Kanai R, Curry WT Jr., Yip S, Nitta M et al. Maintenance of primary tumor phenotype and genotype in glioblastoma stem cells. Neuro Oncol 2012; 14: 132-144.
19. DeLay M, Jahangiri A, Carbonell WS, Hu YL, Tsao S, Tom MW et al. Microarray analysis verifies two distinct phenotypes of glioblastomas resistant to antiangiogenic therapy. Clin Cancer Res 2012; 18: 2930-2942.
20. Wang F, Yang L, Shi L, Li Q, Zhang G, Wu J et al. Nuclear translocation of fibroblast growth factor-2 (FGF2) is regulated by Karyopherin-beta2 and Ran GTPase in human glioblastoma cells. Oncotarget 2015; 6: 21468-21478.
21. Okada T, Murata K, Hirose R, Matsuda C, Komatsu T, Ikekita M et al. Upregulated expression of FGF13/FHF2 mediates resistance to platinum drugs in cervical cancer cells. Sci Rep 2013; 3: 2899.
22. Yu L, Toriseva M, Tuomala M, Seikkula H, Elo T, Tuomela J et al. Increased expression of fibroblast growth factor 13 in prostate cancer is associated with shortened time to biochemical recurrence after radical prostatectomy. Int J Cancer 2016; 139: 140-152.
23. Saito N, Fu J, Zheng S, Yao J, Wang S, Liu DD et al. A high Notch pathway activation predicts response to gamma secretase inhibitors in proneural subtype of glioma tumor-initiating cells. Stem Cells 2014; 32: 301-312.
24. Fang X, Yoon JG, Li L, Yu W, Shao J, Hua D et al. The SOX2 response program in glioblastoma multiforme: an integrated ChIP-seq, expression microarray, and microRNA analysis. BMC Genomics 2011; 12: 11.
25. Berezovsky AD, Poisson LM, Cherba D, Webb CP, Transou AD, Lemke NW et al. Sox2 promotes malignancy in glioblastoma by regulating plasticity and astrocytic differentiation. Neoplasia 2014; 16: e19-e25.
26. Hayashi K, Michiue H, Yamada H, Takata K, Nakayama H, Wei FY et al. Fluvoxamine, an anti-depressant, inhibits human glioblastoma invasion by disrupting actin polymerization. Sci Rep 2016; 6: 23372.
27. Fife CM, McCarroll JA, Kavallaris M. Movers and shakers: cell cytoskeleton in cancer metastasis. Br J Pharmacol 2014; 171: 5507-5523.
28. Draberova E, Vinopal S, Morfini G, Liu PS, Sladkova V, Sulimenko T 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: 811-826.
29. Song Y, Mu L, Han X, Liu X, Fu S. siRNA targeting stathmin inhibits invasion and enhances chemotherapy sensitivity of stem cells derived from glioma cell lines. Acta Biochim Biophys Sin (Shanghai) 2014; 46: 1034-1040.
30. Oehler C, Frei K, Rushing EJ, McSheehy PM, Weber D, Allegrini PR et al. Patupilone (epothilone B) for recurrent glioblastoma: clinical outcome and translational analysis of a single-institution phase I/II trial. Oncology 2012; 83: 1-9.
31. Barker CA, Bishop AJ, Chang M, Beal K, Chan TA. Valproic acid use during radiation therapy for glioblastoma associated with improved survival. Int J Radiat Oncol Biol Phys 2013; 86: 504-509.
32. Stupp R, Taillibert S, Kanner AA, Kesari S, Steinberg DM, Toms SA et al. Maintenance therapy with tumor-treating fields plus temozolomide vs temozolomide alone for glioblastoma: a randomized clinical trial. JAMA 2015; 314: 2535-2543.
33. Nagai S, Moreno O, Smith CA, Ivanchuk S, Romagnuolo R, Golbourn B et al. Role of the cofilin activity cycle in astrocytoma migration and invasion. Genes Cancer 2011; 2: 859-869.
34. Wittmack EK, Rush AM, Craner MJ, Goldfarb M, Waxman SG, Dib-Hajj SD. Fibroblast growth factor homologous factor 2B: association with Nav1.6 and selective colocalization at nodes of Ranvier of dorsal root axons. J Neurosci 2004; 24: 6765-6775.
35. Ichikawa T, Otani Y, Kurozumi K, Date I. Phenotypic transition as a survival strategy of glioma. Neurol Med Chir (Tokyo) 2016; 56: 387-395.
36. Lu KV, Chang JP, Parachoniak CA, Pandika MM, Aghi MK, Meyronet D et al. VEGF inhibits tumor cell invasion and mesenchymal transition through a MET/VEGFR2 complex. Cancer Cell 2012; 22: 21-35.
37. Keunen O, Johansson M, Oudin A, Sanzey M, Rahim SA, Fack F et al. Anti-VEGF treatment reduces blood supply and increases tumor cell invasion in glioblastoma. Proc Natl Acad Sci USA 2011; 108: 3749-3754.
38. Piao Y, Park SY, Henry V, Smith BD, Tiao N, Flynn DL et al. Novel MET/TIE2/VEGFR2 inhibitor altiratinib inhibits tumor growth and invasiveness in bevacizumabresistant glioblastoma mouse models. Neuro Oncol 2016; 18: 1230-1241.
39. Hampl JA, Camp SM, Mydlarz WK, Hampl M, Ichikawa T, Chiocca EA et al. Potentiated gene delivery to tumors using herpes simplex virus/Epstein-Barr virus/RV tribrid amplicon vectors. Hum Gene Ther 2003; 14: 611-626.
40. Berens ME, Bjotvedt G, Levesque DC, Rief MD, Shapiro JR, Coons SW. Tumorigenic, invasive, karyotypic, and immunocytochemical characteristics of clonal cell lines derived from a spontaneous canine anaplastic astrocytoma. In Vitro Cell Dev Biol Anim 1993; 29a: 310-318.
41. Ichikawa T, Hogemann D, Saeki Y, Tyminski E, Terada K, Weissleder R et al. MRI of transgene expression: correlation to therapeutic gene expression. Neoplasia 2002; 4: 523-530.
42. Wakimoto H, Kesari S, Farrell CJ, Curry WT Jr., Zaupa C, Aghi M et al. Human glioblastoma-derived cancer stem cells: establishment of invasive glioma models and treatment with oncolytic herpes simplex virus vectors. Cancer Res 2009; 69: 3472-3481.
43. Huang, da W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009; 4: 44-57.
44. Oka T, Kurozumi K, Shimazu Y, Ichikawa T, Ishida J, Otani Y et al. A super gene expression system enhances the anti-glioma effects of adenovirus-mediated REIC/Dkk-3 gene therapy. Sci Rep 2016; 6: 33319.