Integrin control of the transforming growth factor-β pathway in glioblastoma

Brain

Volumn 136, Issue 2, 2013, Pages 564-576

  Roth, Patrick ^a   Silginer, Manuela ^a   Goodman, Simon L ^b   Hasenbach, Kathy ^a,c   Thies, Svenja ^d   Maurer, Gabriele ^c   Schraml, Peter ^d   Tabatabai, Ghazaleh ^a,c   Moch, Holger ^d   Tritschler, Isabel ^a,c   Weller, Michael ^a,c  

^a UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^b MERCK KGAA   (Germany)

^c UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^d UNIVERSITY HOSPITAL ZURICH   (Switzerland)

Author keywords

cilengitide; glioma; integrin; TGF

Indexed keywords

ALPHAVBETA5 INTEGRIN; ALPHAVBETA8 INTEGRIN; CILENGITIDE; INTEGRIN; MESSENGER RNA; NEUTRALIZING ANTIBODY; SMAD2 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; VITRONECTIN RECEPTOR;

ARTICLE; BRAIN BLOOD VESSEL; CONTROLLED STUDY; GENE SILENCING; GENETIC TRANSCRIPTION; GLIOBLASTOMA; GLIOMA CELL; HUMAN; HUMAN CELL; IN VIVO STUDY; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; REPORTER GENE; RNA INTERFERENCE;

EID: 84874318559     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/aws351     Document Type: Article

References (40)

1. Abe M, Harpel JG, Metz CN, Nunes I, Loskutoff DJ, Rifkin DB. An assay for transforming growth factor-beta using cells transfected with a plasminogen activator inhibitor-1 promoter-luciferase construct. Anal Biochem 1994; 216: 276-84.
2. Alghisi GC, Ruegg C. Vascular integrins in tumor angiogenesis: mediators and therapeutic targets. Endothelium 2006; 13: 113-35.
3. Anido J, Saez-Borderias A, Gonzalez-Junca A, Rodon L, Folch G, Carmona MA, et al. TGF-beta receptor inhibitors target the CD44(high)/Id1(high) glioma-initiating cell population in human glioblastoma. Cancer Cell 2010; 18: 655-68.
4. Annes JP, Munger JS, Rifkin DB. Making sense of latent TGFbeta activation. J Cell Sci 2003; 116: 217-24.
5. Azaro A, Baselga J, Sepú lveda JM, Seoane J, Ahnert JR, Brana I, et al. The oral transforming growth factor-beta (TGF-ß) receptor I kinase inhibitor LY2157299 plus lomustine in patients with treatment-refractory malignant glioma: the first human dose study. J Clin Oncol 2012; 30(suppl; abstr 2042).
6. Batchelor TT, Duda DG, di Tomaso E, Ancukiewicz M, Plotkin SR, Gerstner E, et al. Phase II study of cediranib, an oral pan-vascular endothelial growth factor receptor tyrosine kinase inhibitor, in patients with recurrent glioblastoma. J Clin Oncol 2010; 28: 2817-23.
7. Beisner J, Buck MB, Fritz P, Dippon J, Schwab M, Brauch H, et al. A novel functional polymorphism in the transforming growth factor-beta2 gene promoter and tumor progression in breast cancer. Cancer Res 2006; 66: 7554-61.
8. Bogdahn U, Hau P, Stockhammer G, Venkataramana NK, Mahapatra AK, Suri A, et al. Targeted therapy for high-grade glioma with the TGF-beta2 inhibitor trabedersen: results of a randomized and controlled phase IIb study. Neuro Oncol 2011; 13: 132-42.
9. Bruna A, Darken RS, Rojo F, Ocana A, Penuelas S, Arias A, et al. High TGFbeta-Smad activity confers poor prognosis in glioma patients and promotes cell proliferation depending on the methylation of the PDGF-B gene. Cancer Cell 2007; 11: 147-60.
10. Cambier S, Gline S, Mu D, Collins R, Araya J, Dolganov G, et al. Integrin alpha(v)beta8-mediated activation of transforming growth factor-beta by perivascular astrocytes: an angiogenic control switch. Am J Pathol 2005; 166: 1883-94.
11. Carraro G, Albertin G, Forneris M, Nussdorfer GG. Similar sequence-free amplification of human glyceraldehyde-3-phosphate dehydrogenase for real time RT-PCR applications. Mol Cell Probes 2005; 19: 181-6.
12. Desgrosellier JS, Cheresh DA. Integrins in cancer: biological implications and therapeutic opportunities. Nat Rev Cancer 2010; 10: 9-22.
13. Friese MA, Wischhusen J, Wick W, Weiler M, Eisele G, Steinle A, et al. RNA interference targeting transforming growth factor-beta enhances NKG2D-mediated antiglioma immune response, inhibits glioma cell migration and invasiveness, and abrogates tumorigenicity in vivo. Cancer Res 2004; 64: 7596-603.
14. Goodman SL, Grote HJ, Wilm C. Matched rabbit monoclonal antibodies against v-series integrins reveal a novel v 3-LIBS epitope, and permit routine staining of archival paraffin samples of human tumors. Biol Open 2012; 1 (4): 329-40.
15. Gunther HS, Schmidt NO, Phillips HS, Kemming D, Kharbanda S, Soriano R, et al. Glioblastoma-derived stem cell-enriched cultures form distinct subgroups according to molecular and phenotypic criteria. Oncogene 2008; 27: 2897-909.
16. Hanahan D, Folkman J. Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 1996; 86: 353-64.
17. Kononen J, Bubendorf L, Kallioniemi A, Barlund M, Schraml P, Leighton S, et al. Tissue microarrays for high-throughput molecular profiling of tumor specimens. Nat Med 1998; 4: 844-7.
18. Leitlein J, Aulwurm S, Waltereit R, Naumann U, Wagenknecht B, Garten W, et al. Processing of immunosuppressive pro-TGF-beta 1,2 by human glioblastoma cells involves cytoplasmic and secreted furin-like proteases. J Immunol 2001; 166: 7238-43.
19. Ludbrook SB, Barry ST, Delves CJ, Horgan CM. The integrin alphavbeta3 is a receptor for the latency-associated peptides of transforming growth factors beta1 and beta3. Biochem J 2003; 369: 311-8.
20. Mas-Moruno C, Rechenmacher F, Kessler H. Cilengitide: the first anti-angiogenic small molecule drug candidate design, synthesis and clinical evaluation. Anticancer Agents Med Chem 2010; 10: 753-68.
21. Maurer GD, Tritschler I, Adams B, Tabatabai G, Wick W, Stupp R, et al. Cilengitide modulates attachment and viability of human glioma cells, but not sensitivity to irradiation or temozolomide in vitro. Neuro Oncol 2009; 11: 747-56.
22. Miyazono K, Olofsson A, Colosetti P, Heldin CH. A role of the latent TGF-beta 1-binding protein in the assembly and secretion of TGF-beta 1. Embo J 1991; 10: 1091-101.
23. Mu D, Cambier S, Fjellbirkeland L, Baron JL, Munger JS, Kawakatsu H, et al. The integrin alpha(v)beta8 mediates epithelial homeostasis through MT1-MMP-dependent activation of TGF-beta1. J Cell Biol 2002; 157: 493-507.
24. Munger JS, Huang X, Kawakatsu H, Griffiths MJ, Dalton SL, Wu J, et al. The integrin alpha v beta 6 binds and activates latent TGF beta 1: a mechanism for regulating pulmonary inflammation and fibrosis. Cell 1999; 96: 319-28.
25. Ortega-Velazquez R, Diez-Marques ML, Ruiz-Torres MP, Gonzalez-Rubio M, Rodriguez-Puyol M, Rodriguez Puyol D. Arg-Gly-Asp-Ser (RGDS) peptide stimulates transforming growth factor beta1 transcription and secretion through integrin activation. FASEB J 2003; 17: 1529-31.
26. Penuelas S, Anido J, Prieto-Sanchez RM, Folch G, Barba I, Cuartas I, et al. TGF-beta increases glioma-initiating cell self-renewal through the induction of LIF in human glioblastoma. Cancer Cell 2009; 15: 315-27.
27. Preusser M, de Ribaupierre S, Wohrer A, Erridge SC, Hegi M, Weller M, et al. Current concepts and management of glioblastoma. Ann Neurol 2011; 70: 9-21.
28. Reardon DA, Fink KL, Mikkelsen T, Cloughesy TF, O'Neill A, Plotkin S, et al. Randomized phase ii study of cilengitide, an integrin-targeting arginine-glycine-aspartic acid peptide, in recurrent glioblastoma multiforme. J Clin Oncol 2008; 26: 5610-7.
29. Schnell O, Krebs B, Carlsen J, Miederer I, Goetz C, Goldbrunner RH, et al. Imaging of integrin alpha(v)beta(3) expression in patients with malignant glioma by [18F] Galacto-RGD positron emission tomography. Neuro Oncol 2009; 11: 861-70.
30. Sheppard D. Integrin-mediated activation of latent transforming growth factor beta. Cancer Metastasis Rev 2005; 24: 395-402.
31. Stupp R, Hegi ME, Neyns B, Goldbrunner R, Schlegel U, Clement PM, et al. Phase I/IIa study of cilengitide and temozolomide with concomitant radiotherapy followed by cilengitide and temozolomide maintenance therapy in patients with newly diagnosed glioblastoma. J Clin Oncol 2010; 28: 2712-8.
32. 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.
33. Uhl M, Aulwurm S, Wischhusen J, Weiler M, Ma JY, Almirez R, et al. SD-208, a novel transforming growth factor beta receptor I kinase inhibitor, inhibits growth and invasiveness and enhances immunogenicity of murine and human glioma cells in vitro and in vivo. Cancer Res 2004; 64: 7954-61.
34. Vredenburgh JJ, Desjardins A, Herndon JE II, Marcello J, Reardon DA, Quinn JA, et al. Bevacizumab plus irinotecan in recurrent glioblastoma multiforme. J Clin Oncol 2007; 25: 4722-9.
35. Weigert C, Brodbeck K, Klopfer K, Haring HU, Schleicher ED Angiotensin II induces human TGF-beta 1 promoter activation: similarity to hyperglycaemia. Diabetologia 2002 45.890-8.
36. Weigert C, Brodbeck K, Sawadogo M, Haring HU, Schleicher ED Upstream stimulatory factor (USF) proteins induce human TGF-beta1 gene activation via the glucose-response element-1013/-1002 in mesangial cells: up-regulation of USF activity by the hexosamine biosynthetic pathway. J Biol Chem 2004,279.15908-15.
37. Wick W, Naumann U, Weller M. Transforming growth factor-beta: a molecular target for the future therapy of glioblastoma. Curr Pharm Des 2006; 12: 341-9.
38. Wipff PJ, Hinz B. Integrins and the activation of latent transforming growth factor beta1-an intimate relationship. Eur J Cell Biol 2008; 87: 601-15.
39. Zawel L, Dai JL, Buckhaults P, Zhou S, Kinzler KW, Vogelstein B, et al. Human Smad3 and Smad4 are sequence-specific transcription activators. Mol Cell 1998; 1: 611-7.
40. Zhang M, Kleber S, Rohrich M, Timke C, Han N, Tuettenberg J, et al. Blockade of TGF-beta signaling by the TGFbetaR-I kinase inhibitor LY2109761 enhances radiation response and prolongs survival in glioblastoma. Cancer Res 2011; 71: 7155-67.