Epigenetic silencing of Id4 identifies a glioblastoma subgroup with a better prognosis as a consequence of an inhibition of angiogenesis

Cancer

Volumn 119, Issue 5, 2013, Pages 1004-1012

  Martini, Maurizio ^a   Cenci, Tonia ^a   D'Alessandris, Giorgio Quintino ^a   Cesarini, Valeriana ^a   Cocomazzi, Alessandra ^a   Ricci Vitiani, Lucia ^b   De Maria, Ruggero ^c   Pallini, Roberto ^a   Larocca, Luigi Maria ^a  

^a CATHOLIC UNIVERSITY   (Italy)

^b ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^c REGINA ELENA NATIONAL CANCER INSTITUTE   (Italy)

Author keywords

adjuvant radiotherapy; glioblastoma; Id4; temozolomide.; vascular endothelial growth factor

Indexed keywords

MESSENGER RNA; OSTEOCALCIN; PROTEIN ID4; TEMOZOLOMIDE; TRANSCRIPTION FACTOR; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG; VASCULOTROPIN; VON WILLEBRAND FACTOR;

ADULT; AGED; ANTIANGIOGENIC ACTIVITY; ARTICLE; CANCER PROGNOSIS; CAPILLARY DENSITY; CELL DENSITY; CONTROLLED STUDY; EPIGENETICS; FEMALE; GENE SILENCING; GENETIC IDENTIFICATION; GLIOBLASTOMA; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; ID4 GENE; MAJOR CLINICAL STUDY; MALE; MOLECULAR CLONING; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN METHYLATION; REAL TIME POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; TUMOR GENE;

ADULT; AGED; AGED, 80 AND OVER; BRAIN NEOPLASMS; DNA METHYLATION; GLIOBLASTOMA; HUMANS; INHIBITOR OF DIFFERENTIATION PROTEINS; MIDDLE AGED; NEOVASCULARIZATION, PATHOLOGIC; PROGNOSIS; VASCULAR ENDOTHELIAL GROWTH FACTOR A; YOUNG ADULT;

EID: 84874256901     PISSN: 0008543X     EISSN: 10970142     Source Type: Journal    
DOI: 10.1002/cncr.27821     Document Type: Article

References (33)

1. Wen PY, Kesari S,. Malignant gliomas in adults. N Engl J Med. 2008; 359: 492-507.
2. Khasraw M, Lassman AB,. Advances in the treatment of malignant gliomas. Curr Oncol Rep. 2010; 12: 26-33.
3. Onishi M, Ichikawa T, Kurozumi K, Date I,. Angiogenesis and invasion in glioma. Brain Tumor Pathol. 2011; 28: 13-24.
4. Dell'Orso S, Ganci F, Strano S, Blandino G, Fontemaggi G,. ID4: a new player in the cancer arena. Oncotarget. 2010; 1: 48-58.
5. Takano S,. Glioblastoma angiogenesis: VEGF resistance solutions and new strategies based on molecular mechanisms of tumor vessel formation. Brain Tumor Pathol. 2012; 29: 73-86.
6. Kuzontkoski PM, Mulligan-Kehoe MJ, Harris BT, Israel MA,. Inhibitor of DNA binding-4 promotes angiogenesis and growth of glioblastoma multiforme by elevating matrix GLA levels. Oncogene. 2010; 29: 3793-3802.
7. Boström K, Zebboudj AF, Yao Y, Lin TS, Torres A,. Matrix GLA protein stimulates VEGF expression through increased transforming growth factor-beta1 activity in endothelial cells. J Biol Chem. 2004; 279: 52904-52913.
8. Benezra R, Davis RL, Lockshon D, Turner DL, Weintraub H,. The protein Id: a negative regulator of helix-loop-helix DNA binding proteins. Cell. 1990; 61: 49-59.
9. Massari ME, Murre C,. Helix-loop-helix proteins: regulators of transcription in eucaryotic organisms. Mol Cell Biol. 2000; 20: 429-440.
10. Ruzinova MB, Benezra R,. Id proteins in development, cell cycle and cancer. Trends Cell Biol. 2003; 13: 410-418.
11. Yun K, Mantani A, Garel S, Rubenstein J, Israel MA,. Id4 regulates neural progenitor proliferation and differentiation in vivo. Development. 2004; 131: 5441-5448.
12. Iavarone A, Lasorella A,. ID proteins as targets in cancer and tools in neurobiology. Trends Mol Med. 2006; 12: 588-594.
13. Umetani N, Takeuchi H, Fujimoto A, Shinozaki M, Bilchik AJ, Hoon DS,. Epigenetic inactivation of ID4 in colorectal carcinomas correlates with poor differentiation and unfavorable prognosis. Clin Cancer Res. 2004; 10: 7475-7483.
14. Noetzel E, Veeck J, Niederacher D, et al. Promoter methylation-associated loss of ID4 expression is a marker of tumour recurrence in human breast cancer. BMC Cancer. 2008; 8: 154.
15. Chan AS, Tsui WY, Chen X, et al. Downregulation of ID4 by promoter hypermethylation in gastric adenocarcinoma. Oncogene. 2003; 22: 6946-6953.
16. Chen SS, Claus R, Lucas DM, et al. Silencing of the inhibitor of DNA binding protein 4 (ID4) contributes to the pathogenesis of mouse and human CLL. Blood. 2011; 117: 862-871.
17. Andres-Barquin PJ, Hernandez MC, Israel MA,. Id4 expression induces apoptosis in astrocytic cultures and is down-regulated by activation of the cAMP-dependent signal transduction pathway. Exp Cell Res. 1999; 247: 347-355.
18. Bedford L, Walker R, Kondo T, van Crüchten I, King ER, Sablitzky F,. Id4 is required for the correct timing of neural differentiation. Dev Biol. 2005; 280: 386-395.
19. Jeon HM, Jin X, Lee JS, et al. Inhibitor of differentiation 4 drives brain tumor-initiating cell genesis through cyclin E and notch signaling. Genes Dev. 2008; 22: 2028-2033.
20. Jeon HM, Sohn YW, Oh SY, et al. ID4 imparts chemoresistance and cancer stemness to glioma cells by derepressing miR-9*-mediated suppression of SOX2. Cancer Res. 2011; 71: 3410-3421.
21. Louis DN, Ohgaki H, Wiestler OD, Cavenee CW,. World Health Organization Classification of the Nervous System. 4th ed. Lyon, France: IARC Press; 2007: 33-49.
22. Pallini R, Ricci-Vitiani L, Banna GL, et al. Cancer stem cell analysis and clinical outcome in patients with glioblastoma multiforme. Clin Cancer Res. 2008; 14: 8205-8212.
23. Martini M, Pallini R, Luongo G, Cenci T, Lucantoni C, Larocca LM,. Prognostic relevance of SOCS3 hypermethylation in patients with glioblastoma multiforme. Int J Cancer. 2008; 123: 2955-2960.
24. Zeng W, Rushing EJ, Hartmann DP, Azumi N,. Increased inhibitor of differentiation 4 (id4) expression in glioblastoma: a tissue microarray study. J Cancer. 2010; 1: 1-5.
25. Leon SP, Folkerth RD, Black PM,. Microvessel density is a prognostic indicator for patients with astroglial brain tumors. Cancer. 1996; 77: 362-372.
26. Norden AD, Young GS, Setayesh K, et al. Bevacizumab for recurrent malignant gliomas: efficacy, toxicity, and patterns of recurrence. Neurology. 2008; 70: 779-787.
27. Ferrari G, Pintucci G, Seghezzi G, Hyman K, Galloway AC, Mignatti P,. VEGF, a prosurvival factor, acts in concert with TGF-beta1 to induce endothelial cell apoptosis. Proc Natl Acad Sci U S A. 2006; 103: 17260-17265.
28. van den Boom J, Wolter M, Kuick R, et al. Characterization of gene expression profiles associated with glioma progression using oligonucleotide-based microarray analysis and real-time reverse transcription-polymerase chain reaction. Am J Pathol. 2003; 163: 1033-1043.
29. Kjellman C, Olofsson SP, Hansson O, et al. Expression of TGF-beta isoforms, TGF-beta receptors, and SMAD molecules at different stages of human glioma. Int J Cancer. 2000; 89: 251-258.
30. Bello L, Giussani C, Carrabba G, Pluderi M, Costa F, Bikfalvi A,. Angiogenesis and invasion in gliomas. Cancer Treat Res. 2004; 117: 263-284.
31. Ricci-Vitiani L, Pallini R, Biffoni M, et al. Tumour vascularization via endothelial differentiation of glioblastoma stem-like cells. Nature. 2010; 468: 824-828.
32. Wang R, Chadalavada K, Wilshire J, et al. Glioblastoma stem-like cells give rise to tumour endothelium. Nature. 2010; 468: 829-833.
33. Linkous AG, Yazlovitskaya EM,. Angiogenesis in glioblastoma multiforme: navigating the maze. Anticancer Agents Med Chem. 2011; 11: 712-718.