O(6)-methylguanine-DNA methyltransferase is a novel negative effector of invasion in glioblastoma multiforme

Molecular Cancer Therapeutics

Volumn 11, Issue 11, 2012, Pages 2440-2450

  Chahal, Manik ^a   Abdulkarim, Bassam ^a,c   Xu, Yaoxian ^a,c   Guiot, Marie Christine ^d   Easaw, Jacob C ^b   Stifani, Nicolas ^c   Sabri, Siham ^a,c  

^a UNIVERSITY OF ALBERTA   (Canada)

^b TOM BAKER CANCER CENTRE   (Canada)

^c MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^d MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

FOCAL ADHESION KINASE; METHYLATED DNA PROTEIN CYSTEINE METHYLTRANSFERASE; OSTEONECTIN; PARAFFIN; SHORT HAIRPIN RNA; VERY LATE ACTIVATION ANTIGEN 5; SMALL INTERFERING RNA;

ANGIOGENESIS; ARTICLE; CANCER CELL CULTURE; CANCER INVASION; CELL MIGRATION; CELL SIZE; CELL STRUCTURE; CONTROLLED STUDY; DNA METHYLATION; GENE EXPRESSION; GENE SILENCING; GLIOBLASTOMA; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; SPINDLE CELL; BRAIN TUMOR; CELL MOTION; CELL SHAPE; ENZYME ACTIVATION; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY; PHENOTYPE; TUMOR CELL LINE;

BRAIN NEOPLASMS; CELL LINE, TUMOR; CELL MOVEMENT; CELL SHAPE; ENZYME ACTIVATION; FOCAL ADHESION PROTEIN-TYROSINE KINASES; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKDOWN TECHNIQUES; GLIOBLASTOMA; HUMANS; IMMUNOHISTOCHEMISTRY; NEOPLASM INVASIVENESS; O(6)-METHYLGUANINE-DNA METHYLTRANSFERASE; OSTEONECTIN; PHENOTYPE; RNA, SMALL INTERFERING;

EID: 84869237270     PISSN: 15357163     EISSN: 15388514     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-11-0977     Document Type: Article

References (49)

1. Giese A, Bjerkvig R, Berens ME, Westphal M. Cost of migration: invasion of malignant gliomas and implications for treatment. J Clin Oncol 2003;21:1624-36. (Pubitemid 46594118)
2. 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;352:987-96. (Pubitemid 40349501)
3. Nakada M, Okada Y, Yamashita J. The role of matrix metalloproteinases in glioma invasion. Front Biosci 2003;8:e261-9.
4. Rich JN, Hans C, Jones B, Iversen ES, McLendon RE, Rasheed BK, et al. Gene expression profiling and genetic markers in glioblastoma survival. Cancer Res 2005;65:4051-8. (Pubitemid 40775641)
5. Johnston AL, Lun X, Rahn JJ, Liacini A, Wang L, Hamilton MG, et al. The p75 neurotrophin receptor is a central regulator of glioma invasion. PLoS Biol 2007;5:e212.
6. Carro MS, Lim WK, Alvarez MJ, Bollo RJ, Zhao X, Snyder EY, et al. The transcriptional network for mesenchymal transformation of brain tumours. Nature 2010;463:318-25.
7. Tabatabai G, Stupp R, van den Bent MJ, Hegi ME, Tonn JC, Wick W, et al. Molecular diagnostics of gliomas: the clinical perspective. Acta Neuropathol 2010;120:585-92.
8. Esteller M, Garcia-Foncillas J, Andion E, Goodman SN, Hidalgo OF, Vanaclocha V, et al. Inactivation of the DNA-repair gene MGMT and the clinical response of gliomas to alkylating agents. N Engl J Med 2000;343:1350-4.
9. Hegi ME, Diserens AC, Gorlia T, Hamou MF, de Tribolet N, Weller M, et al. MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med 2005;352:997-1003. (Pubitemid 40349502)
10. Kreth S, Thon N, Eigenbrod S, Lutz J, Ledderose C, Egensperger R, et al. O-Methylguanine-DNA methyltransferase (MGMT) mRNA expression predicts outcome in malignant glioma independent of MGMT promoter methylation. PLoS One 2011;6:e17156.
11. Network TCGAR. Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 2008;455:1061-8.
12. Takeshita A, Inoshita N, Taguchi M, Okuda C, Fukuhara N, Oyama K, et al. High incidence of low O(6)-methylguanine DNA methyltransferase expression in invasive macroadenomas of Cushing's disease. Eur J Endocrinol 2009;161:553-9.
13. Park TJ, Han SU, Cho YK, Paik WK, Kim YB, Lim IK. Methylation of O (6)-methylguanine-DNA methyltransferase gene is associated significantly with K-ras mutation, lymph node invasion, tumor staging, and disease free survival in patients with gastric carcinoma. Cancer 2001;92:2760-8. (Pubitemid 33091912)
14. Brandes AA, Tosoni A, Franceschi E, Sotti G, Frezza G, Amista P, et al. Recurrence pattern after temozolomide concomitant with and adjuvant to radiotherapy in newly diagnosed patients with glioblastoma: correlation With MGMT promoter methylation status. J Clin Oncol 2009;27:1275-9.
15. Chahal M, Xu Y, Lesniak D, Graham K, Famulski K, Christensen JG, et al. MGMT modulates glioblastoma angiogenesis and response to the tyrosine kinase inhibitor sunitinib. Neuro Oncol 2010;12:822-33.
16. Vajkoczy P, Goldbrunner R, Farhadi M, Vince G, Schilling L, Tonn JC, et al. Glioma cell migration is associated with glioma-induced angiogenesis in vivo. Int J Dev Neurosci 1999;17:557-63. (Pubitemid 29421842)
17. Eccles SA. Parallels in invasion and angiogenesis provide pivotal points for therapeutic intervention. Int J Dev Biol 2004;48:583-98. (Pubitemid 39360409)
18. Onishi M, Ichikawa T, Kurozumi K, Date I. Angiogenesis and invasion in glioma. Brain Tumor Pathol 2011;28:13-24.
19. Schultz C, Lemke N, Ge S, Golembieski WA, Rempel SA. Secreted protein acidic and rich in cysteine promotes glioma invasion and delays tumor growth in vivo. Cancer Res 2002;62:6270-7. (Pubitemid 35244481)
20. Thomas SL, Alam R, Lemke N, Schultz LR, Gutierrez JA, Rempel SA. PTEN augments SPARC suppression of proliferation and inhibits SPARC-induced migration by suppressing SHC-RAF-ERK and AKT signaling. Neuro Oncol 2010;12:941-55.
21. Aghi M, Rabkin S, Martuza RL. Effect of chemotherapy-induced DNA repair on oncolytic herpes simplex viral replication. J Natl Cancer Inst 2006;98:38-50. (Pubitemid 43057091)
22. Hamilton MG, Roldan G, Magliocco A, McIntyre JB, Parney I, Easaw JC. Determination of the methylation status of MGMT in different regions within glioblastoma multiforme. J Neurooncol 2010;102:255-60.
23. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, et al. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 2000;25:25-9. (Pubitemid 30257031)
24. Kanzawa T, Germano IM, Kondo Y, Ito H, Kyo S, Kondo S. Inhibition of telomerase activity in malignant glioma cells correlates with their sensitivity to temozolomide. Br J Cancer 2003;89:922-9. (Pubitemid 37175817)
25. D'Abaco GM, Kaye AH. Integrins: molecular determinants of glioma invasion. J Clin Neurosci 2007;14:1041-8. (Pubitemid 47588943)
26. Gu J, Isaji T, Sato Y, Kariya Y, Fukuda T. Importance of N-glycosylation on alpha5beta1 integrin for its biological functions. Biol Pharm Bull 2009;32:780-5.
27. Gladson CL. The extracellular matrix of gliomas: modulation of cell function. J Neuropathol Exp Neurol 1999;58:1029-40. (Pubitemid 29468264)
28. Ulrich TA, de Juan Pardo EM, Kumar S. The mechanical rigidity of the extracellular matrix regulates the structure, motility, and proliferation of glioma cells. Cancer Res 2009;69:4167-74.
29. Demuth T, Berens ME. Molecular mechanisms of glioma cell migration and invasion. J Neurooncol 2004;70:217-28. (Pubitemid 39545733)
30. Zhong J, Paul A, Kellie SJ, O'Neill GM. Mesenchymal migration as a therapeutic target in glioblastoma. J Oncol 2010;2010:430142.
31. Natarajan M, Hecker TP, Gladson CL. FAK signaling in anaplastic astrocytoma and glioblastoma tumors. Cancer J 2003;9:126-33.
32. Dolan ME, Moschel RC, Pegg AE. Depletion of mammalian O6-alkylguanine-DNA alkyltransferase activity by O6-benzylguanine provides a means to evaluate the role of this protein in protection against carcinogenic and therapeutic alkylating agents. Proc Natl Acad Sci U S A 1990;87:5368-72.
33. Arnold SA, Brekken RA. SPARC: a matricellular regulator of tumorigenesis. J Cell Commun Signal 2009;3:255-73.
34. Weller M, Stupp R, Reifenberger G, Brandes AA, van den Bent MJ, Wick W, et al. MGMT promoter methylation in malignant gliomas: ready for personalized medicine? Nat Rev Neurol 2010;6:39-51.
35. Cao VT, Jung TY, Jung S, Jin SG, Moon KS, Kim IY, et al. The correlation and prognostic significance of MGMT promoter methylation and MGMT protein in glioblastomas. Neurosurgery 2009;65:866-75; discussion 75.
36. Yamazaki D, Kurisu S, Takenawa T. Involvement of Rac and Rho signaling in cancer cell motility in 3D substrates. Oncogene 2009;28:1570-83.
37. Carragher NO, Walker SM, Scott Carragher LA, Harris F, Sawyer TK, Brunton VG, et al. Calpain 2 and Src dependence distinguishes mesenchymal and amoeboid modes of tumour cell invasion: a link to integrin function. Oncogene 2006;25:5726-40. (Pubitemid 44435250)
38. Nie J, Chang B, Traktuev DO, Sun J, March K, Chan L, et al. IFATS collection: combinatorial peptides identify alpha5beta1 integrin as a receptor for the matricellular protein SPARC on adipose stromal cells. Stem Cells 2008;26:2735-45.
39. Weaver MS, Workman G, Sage EH. The copper binding domain of SPARC mediates cell survival in vitro via interaction with integrin beta1 and activation of integrin-linked kinase. J Biol Chem 2008;283:22826-37.
40. Barker TH, Baneyx G, Cardo-Vila M, Workman GA, Weaver M, Menon PM, et al. SPARC regulates extracellular matrix organization through its modulation of integrin-linked kinase activity. J Biol Chem 2005;280:36483-93. (Pubitemid 41633922)
41. Shi Q, Bao S, Song L, Wu Q, Bigner DD, Hjelmeland AB, et al. Targeting SPARC expression decreases glioma cellular survival and invasion associated with reduced activities of FAK and ILK kinases. Oncogene 2007;26:4084-94. (Pubitemid 46920166)
42. Preusser M, Charles Janzer R, Felsberg J, Reifenberger G, Hamou MF, Diserens AC, et al. Anti-O6-methylguanine-methyltransferase (MGMT) immunohistochemistry in glioblastoma multiforme: observer variability and lack of association with patient survival impede its use as clinical biomarker. Brain Pathol 2008;18:520-32.
43. Capper D, Mittelbronn M, Meyermann R, Schittenhelm J. Pitfalls in the assessment of MGMT expression and in its correlation with survival in diffuse astrocytomas: proposal of a feasible immunohistochemical approach. Acta Neuropathol 2008;115:249-59.
44. Della Puppa A, Persano L, Masi G, Rampazzo E, Sinigaglia A, Pistollato F, et al. MGMT expression and promoter methylation status may depend on the site of surgical sample collection within glioblastoma: a possible pitfall in stratification of patients? J Neurooncol 2011;106:33-41.
45. Hoelzinger DB, Mariani L, Weis J, Woyke T, Berens TJ, McDonough WS, et al. Gene expression profile of glioblastoma multiforme invasive phenotype points to new therapeutic targets. Neoplasia 2005;7:7-16. (Pubitemid 40209466)
46. Glas M, Rath BH, Simon M, Reinartz R, Schramme A, Trageser D, et al. Residual tumor cells are unique cellular targets in glioblastoma. Ann Neurol 2010;68:264-9.
47. Su Y, Liu R, Sheng J, Liu H, Wang Y, Pan E, et al. Malignant progression in O(6)-methylguanine-DNA methyltransferase-deficient esophageal cancer cells is associated with Ezrin protein. DNA Cell Biol 2011;31:856-66.
48. Teo AK, Oh HK, Ali RB, Li BF. The modified human DNA repair enzyme O(6)-methylguanine-DNA methyltransferase is a negative regulator of estrogen receptor-mediated transcription upon alkylation DNA damage. Mol Cell Biol 2001;21:7105-14. (Pubitemid 32911269)
49. Wu J, Vallenius T, Ovaska K, Westermarck J, Makela TP, Hautaniemi S. Integrated network analysis platform for protein-protein interactions. Nat Methods 2009;6:75-7.