Cilengitide inhibits progression of experimental breast cancer bone metastases as imaged noninvasively using VCT, MRI and DCE-MRI in a longitudinal in vivo study

International Journal of Cancer

Volumn 128, Issue 10, 2011, Pages 2453-2462

  Bäuerle, Tobias ^a   Komljenovic, Dorde ^a   Merz, Maximilian ^a   Berger, Martin R ^a   Goodman, Simon L ^b   Semmler, Wolfhard ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b Merck Serono GmbH   (Germany)

Author keywords

bone metastases; dynamic contrast enhanced MRI; integrins; osteolysis; volumetric computed tomography

Indexed keywords

ALPHAVBETA5 INTEGRIN; CILENGITIDE; COLLAGEN TYPE 4; SMOOTH MUSCLE ACTIN; VITRONECTIN RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ANTIRESORPTIVE ACTIVITY; ARTICLE; BLOOD VESSEL PERMEABILITY; BLOOD VOLUME; BONE METASTASIS; BREAST CANCER; CANCER INHIBITION; CONE BEAM COMPUTED TOMOGRAPHY; CONTRAST ENHANCEMENT; CONTROLLED STUDY; DRUG ACTIVITY; EXPERIMENTAL NEOPLASM; FUNCTIONAL ASSESSMENT; HUMAN; HUMAN CELL; IMMUNOPATHOLOGY; IN VITRO STUDY; IN VIVO STUDY; LONGITUDINAL STUDY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; OSTEOLYSIS; PRIORITY JOURNAL; RAT; SOFT TISSUE; TUMOR VASCULARIZATION; TUMOR VOLUME;

ANIMALS; BONE NEOPLASMS; BREAST NEOPLASMS; CELL LINE, TUMOR; DISEASE PROGRESSION; FEMALE; HUMANS; INTEGRIN ALPHAVBETA3; MAGNETIC RESONANCE IMAGING; MAMMARY NEOPLASMS, EXPERIMENTAL; RATS; RATS, NUDE; RECEPTORS, VITRONECTIN; SNAKE VENOMS; TOMOGRAPHY, X-RAY COMPUTED;

EID: 79952748179     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.25563     Document Type: Article

References (51)

1. Guise TA,. Breaking down bone: new insight into site-specific mechanisms of breast cancer osteolysis mediated by metalloproteinases. Genes Dev 2009; 23: 2117-23.
2. Schwartz MA,. Integrin signaling revisited. Trends. Cell Biol 2001; 11: 466-70.
3. Varner JA, Brooks PC, Cheresh DA,. The integrin alpha V beta 3: angiogenesis and apoptosis. Cell Adhes Commun 1995; 3: 367-74.
4. Hynes RO,. Integrins: bidirectional, allosteric signaling machines. Cell 2002; 110: 673-87. (Pubitemid 35283958)
5. Max R, Gerritsen RR, Nooijen PT, Goodman SL, Sutter A, Keilholz U, Ruiter DJ, De Waal RM,. Immunohistochemical analysis of integrin alpha v beta3 expression on tumor-associated vessels of human carcinomas. Int J Cancer 1997; 71: 320-4. (Pubitemid 27224290)
6. Nemeth JA, Nakada MT, Trikha M, Lang Z, Gordon MS, Jayson GC, Corringham R, Prabhakar U, Davis HM, Beckman RA,. Alpha-v integrins as therapeutic targets in oncology. Cancer Invest 2007; 25: 632-46. (Pubitemid 350135743)
7. Mulder WJ, Castermans K, van Beijnum JR, Oude Egbrink MG, Chin PT, Fayad ZA, Löwik CW, Kaijzel EL, Que I, Storm G, Strijkers GJ, Griffioen AW, et al. Molecular imaging of tumor angiogenesis using alphavbeta3-integrin targeted multimodal quantum dots. Angiogenesis 2009; 12: 17-24.
8. Nemeth JA, Cher ML, Zhou Z, Mullins C, Bhagat S, Trikha M,. Inhibition of alpha(v)beta3 integrin reduces angiogenesis, bone turnover, and tumor cell proliferation in experimental prostate cancer bone metastases. Clin Exp Metastasis 2003; 20: 413-20. (Pubitemid 37108427)
9. Pecheur I, Peyruchaud O, Serre CM, Guglielmi J, Voland C, Bourre F, Margue C, Cohen-Solal M, Buffet A, Kieffer N, Clezardin P,. Integrin alpha(v)beta3 expression confers on tumor cells a greater propensity to metastasize to bone. FASEB J 2002; 16: 1266-8.
10. Sloan EK, Pouliot N, Stanley KL, Chia J, Moseley JM, Hards DK, Anderson RL,. Tumor-specific expression of alphavbeta3 integrin promotes spontaneous metastasis of breast cancer to bone. Breast Cancer Res 2006; 8: R20.
11. Silvestri I, Longanesi Cattani I, Franco P, Pirozzi G, Botti G, Stoppelli MP, Carriero MV,. Engaged urokinase receptors enhance tumor breast cell migration and invasion by upregulating alpha(v)beta5 vitronectin receptor cell surface expression. Int J Cancer 2002; 102: 562-71. (Pubitemid 35334462)
12. Inoue M, Ross FP, Erdmann JM, Abu-Amer Y, Wei S, Teitelbaum SL,. Tumor necrosis factor alpha regulates alpha(v)beta5 integrin expression by osteoclast precursors in vitro and in vivo. Endocrinology 2000; 141: 284-90. (Pubitemid 32260369)
13. Reardon DA, Nabors LB, Stupp R, Mikkelsen T,. Cilengitide: an integrin-targeting arginine-glycine-aspartic acid peptide with promising activity for glioblastoma multiforme. Expert Opin Investig Drugs 2008; 17: 1225-35.
14. Dechantsreiter MA, Planker E, Matha B, Lohof E, Holzemann G, Jonczyk A, Goodman SL, Kessler H,. N-Methylated cyclic RGD peptides as highly active and selective alpha(v)beta(3) integrin antagonists. J Med Chem 1999; 42: 3033-40. (Pubitemid 29384038)
15. Nisato RE, Tille JC, Jonczyk A, Goodman SL, Pepper MS,. Alpha v beta 3 and alphav beta 5 integrin antagonists inhibit angiogenesis in vitro. Angiogenesis 2003; 6: 105-19. (Pubitemid 38173862)
16. Patsenker E, Popov Y, Sickel F, Schneider V, Ledermann M, Sägesser H, Niedobitek G, Goodman SL, Schuppan D,. Pharmacological inhibition of integrin alphavbeta3 aggravates experimental liver fibrosis and suppresses hepatic angiogenesis. Hepatology 2009; 50: 1501-11.
17. Xiong JP, Stehle T, Zhang R, Joachimiak A, Frech M, Goodman SL, Arnaout MA,. Crystal structure of the extracellular segment of integrin alpha V beta3 in complex with an Arg-Gly-Asp ligand. Science 2002; 296: 151-5. (Pubitemid 34280076)
18. Reardon DA, Fink KL, Mikkelsen T, Cloughesy TF, O'Neill A, Plotkin S, Glantz M, Ravin P, Raizer JJ, Rich KM, Schiff D, Shapiro WR, 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.
19. Buerkle MA, Pahernik SA, Sutter A, Jonczyk A, Messmer K, Dellian M,. Inhibition of the alpha-nu integrins with a cyclic RGD peptide impairs angiogenesis, growth and metastasis of solid tumours in vivo. Br J Cancer 2002; 86: 788-95. (Pubitemid 34250824)
20. Strieth S, Eichhorn ME, Sutter A, Jonczyk A, Berghaus A, Dellian M,. Antiangiogenic combination tumor therapy blocking alpha(v)-integrins and VEGF-receptor-2 increases therapeutic effects in vivo. Int J Cancer 2006; 119: 423-31.
21. Hodivala-Dilke K,. Alphavbeta3 integrin and angiogenesis: a moody integrin in a changing environment. Curr Opin Cell Biol 2008; 20: 514-9.
22. Taverna D, Moher H, Crowley D, Borsig L, Varki A, Hynes RO,. Increased primary tumor growth in mice null for beta3- or beta3/beta5-integrins or selectins. Proc Natl Acad Sci USA 2004; 101: 763-8. (Pubitemid 38121032)
23. Bäuerle T, Bartling S, Berger M, Schmitt-Gräff A, Hilbig H, Kauczor HU, Delorme S, Kiessling F,. Imaging anti-angiogenic treatment response with DCE-VCT, DCE-MRI and DWI in an animal model of breast cancer bone metastasis. Eur J Radiol 2010; 73: 280-7.
24. Bäuerle T, Hilbig H, Bartling S, Kiessling F, Kersten A, Schmitt-Gräff A, Kauczor HU, Delorme S, Berger MR,. Bevacizumab inhibits breast cancer-induced osteolysis, surrounding soft tissue metastasis, and angiogenesis in rats as visualized by VCT and MRI. Neoplasia 2008; 10: 511-20. (Pubitemid 351657393)
25. Mitjans F, Sander D, Adan J, Sutter A, Martinez JM, Jaggle CS, Moyano JM, Kreysch HG, Piulats J, Goodman SL,. An anti-alpha v-integrin antibody that blocks integrin function inhibits the development of a human melanoma in nude mice. J Cell Sci 1995; 108 (Pt 8): 2825-38.
26. Cheresh DA, Spiro RC,. Biosynthetic and functional properties of an Arg-Gly-Asp-directed receptor involved in human melanoma cell attachment to vitronectin, fibrinogen, and von Willebrand factor. J Biol Chem 1987; 262: 17703-11. (Pubitemid 18032258)
27. Weinacker A, Chen A, Agrez M, Cone RI, Nishimura S, Wayner E, Pytela R, Sheppard D,. Role of the integrin alpha v beta 6 in cell attachment to fibronectin. Heterologous expression of intact and secreted forms of the receptor. J Biol Chem 1994; 269: 6940-8.
28. Bäuerle T, Adwan H, Kiessling F, Hilbig H, Armbruster FP, Berger MR,. Characterization of a rat model with site-specific bone metastasis induced by MDA-MB-231 breast cancer cells and its application to the effects of an antibody against bone sialoprotein. Int J Cancer 2005; 115: 177-86. (Pubitemid 40586725)
29. Yamada S, Bu XY, Khankaldyyan V, Gonzales-Gomez I, McComb JG, Laug WE,. Effect of the angiogenesis inhibitor cilengitide (EMD 121974) on glioblastoma growth in nude mice. Neurosurgery 2006; 59: 1304-12. (Pubitemid 44949775)
30. Brix G, Semmler W, Port R, Schad LR, Layer G, Lorenz WJ,. Pharmacokinetic parameters in CNS Gd-DTPA enhanced MR imaging. J Comput Assist Tomogr 1991; 15: 621-8.
31. Harms JF, Welch DR, Samant RS, Shevde LA, Miele ME, Babu GR, Goldberg SF, Gilman VR, Sosnowski DM, Campo DA, Gay CV, Budgeon LR, et al. A small molecule antagonist of the alpha(v)beta3 integrin suppresses MDA-MB-435 skeletal metastasis. Clin Exp Metastasis 2004; 21: 119-28. (Pubitemid 38988085)
32. Zhao Y, Bachelier R, Treilleux I, Pujuguet P, Peyruchaud O, Baron R, Clement-Lacroix P, Clezardin P,. Tumor alphavbeta3 integrin is a therapeutic target for breast cancer bone metastases. Cancer Res 2007; 67: 5821-30. (Pubitemid 46985016)
33. Eliceiri BP, Puente XS, Hood JD, Stupack DG, Schlaepfer DD, Huang XZ, Sheppard D, Cheresh DA,. Src-mediated coupling of focal adhesion kinase to integrin alpha (v) beta5 in vascular endothelial growth factor signaling. J Cell Biol 2002; 157: 149-60.
34. Duong LT, Rodan GA,. Integrin-mediated signaling in the regulation of osteoclast adhesion and activation. Front Biosci 1998; 3: d757-d768.
35. Nakamura I, Duong le T, Rodan SB, Rodan GA,. Involvement of alpha(v) beta3 integrins in osteoclast function. J Bone Miner Metab 2007; 25: 337-44. (Pubitemid 350063834)
36. Andersen TL, Sondergaard TE, Skorzynska KE, Dagnaes-Hansen F, Plesner TL, Hauge EM, Plesner T, Delaisse JM,. A physical mechanism for coupling bone resorption and formation in adult human bone. Am J Pathol 2009; 174: 239-47.
37. Hamaoka T, Madewell JE, Podoloff DA, Hortobagyi GN, Ueno NT,. Bone imaging in metastatic breast cancer. J Clin Oncol 2004; 22: 2942-53. (Pubitemid 41079914)
38. Lai CF, Cheng SL,. Alphavbeta integrins play an essential role in BMP-2 induction of osteoblast differentiation. J Bone Miner Res 2005; 20: 330-40.
39. Bäuerle T, Peterschmitt J, Hilbig H, Kiessling F, Armbruster FP, Berger MR,. Treatment of bone metastasis induced by MDA-MB-231 breast cancer cells with an antibody against bone sialoprotein. Int J Oncol 2006; 28: 573-83.
40. Karadag A, Ogbureke KU, Fedarko NS, Fisher LW,. Bone sialoprotein, matrix metalloproteinase 2, and alpha(v)beta3 integrin in osteotropic cancer cell invasion. J Natl Cancer Inst 2004; 96: 956-65. (Pubitemid 38868142)
41. Mitjans F, Meyer T, Fittschen C, Goodman S, Jonczyk A, Marshall JF, Reyes G, Piulats J,. In vivo therapy of malignant melanoma by means of antagonists of alphav integrins. Int J Cancer 2000; 87: 716-23. (Pubitemid 30620415)
42. MacDonald TJ, Taga T, Shimada H, Tabrizi P, Zlokovic BV, Cheresh DA, Laug WE,. Preferential susceptibility of brain tumors to the antiangiogenic effects of an alpha(v) integrin antagonist. Neurosurgery 2001; 48: 151-7. (Pubitemid 32039837)
43. Chen Q, Manning AD, Millar H, McCabe FL, Ferrante C, Sharp C, Shahied-Arruda L, Doshi P, Nakada MT, Anderson GM,. CNTO 95, a fully human anti αv integrin antibody, inhibits cell signalin, migration, invasion, and spontaneous metastasis of human breast cancer cells. Clin Exp Metastasis 2008; 25: 139-48.
44. Patsenker E, Popov Y, Stickel F, Schneider V, Ledermann M, Sagesser H, Niedobitek G, Goodman SL, Schuppan D,. Pharmacological inhibition of integrin alphavbeta3 aggravates experimental liver fibrosis and suppresses hepatic angiogenesis. Hepatology 2009; 50: 1501-11.
45. Brooks PC, Montgomery AM, Rosenfeld M, Reisfeld RA, Hu T, Klier G, Cheresh DA,. Integrin alpha v beta 3 antagonists promote tumor regression by inducing apoptosis of angiogenic blood vessels. Cell 1994; 79: 1157-64.
46. Alghisi GC, Ponsonnet L, Ruegg C,. The integrin antagonist cilengitide activates alphaVbeta3, disrupts VE-cadherin localization at cell junctions and enhances permeability in endothelial cells. PLoS One 2009; 4: e4449.
47. Abdollahi A, Griggs DW, Zieher H, Roth A, Lipson KE, Saffrich R, Gröne HJ, Hallahan DE, Reisfeld RA, Debus J, Niethammer AG, Huber PE,. Inhibition of alpha(v) beta3 integrin survival signaling enhances antiangiogenic and antitumor effects of radiotherapy. Clin Cancer Res 2005; 11: 6270-9. (Pubitemid 41262958)
48. Mikkelsen T, Brodie C, Finniss S, Berens ME, Rennert JL, Nelson K, Lemke N, Brown SL, Hahn D, Neuteboom B, Goodman SL,. Radiation sensitization of glioblastoma by cilengitide has unanticipated schedule-dependency. Int J Cancer 2009; 124: 2719-27.
49. Albert JM, Cao C, Geng L, Leavitt L, Hallahan DE, Lu B,. Integrin alpha v beta 3 antagonist cilengitide enhances efficacy of radiotherapy in endothelial cell and non-small-cell lung cancer models. Int J Radiat Oncol Biol Phys 2006; 65: 1536-43. (Pubitemid 44425239)
50. Reynolds LE, Wyder L, Lively JC, Taverna D, Robinson SD, Huang X, Sheppard D, Hynes RO, Hodivala-Dilke KM,. Enhanced pathological angiogenesis in mice lacking beta3 integrin or beta3 and beta5 integrins. Nat Med 2002; 8: 27-34. (Pubitemid 34101725)
51. Reynolds AR, Hart IR, Watson AR, Welti JC, Silva RG, Robinson SD, Da Violante G, Gourlaouen M, Salih M, Jones MC, Jones DT, Saunders G, et al. Stimulation of tumor growth and angiogenesis by low concentrations of RGD-mimetic integrin inhibitors. Nat Med 2009; 15: 392-400.