Reversing resistance to vascular-disrupting agents by blocking late mobilization of circulating endothelial progenitor cells

Cancer Discovery

Volumn 2, Issue 5, 2012, Pages 434-449

  Taylor, Melissa ^a,b   Billiot, Fanny ^a   Marty, Virginie ^a   Rouffiac, Valérie ^b   Cohen, Patrick ^d   Tournay, Elodie ^b   Opolon, Paule ^b   Louache, Fawzia ^c   Vassal, Gilles ^b   Laplace Builhé, Corinne ^a   Vielh, Philippe ^a   Soria, Jean Charles ^a,b   Farace, Françoise ^a,b  

^a INSTITUT GUSTAVE ROUSSY   (France)

^b UNIVERSITÉ PARIS SACLAY   (France)

^c INSERM   (France)

^d SANOFI   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENESIS INHIBITOR; BEVACIZUMAB; CARBONATE DEHYDRATASE IX; CD34 ANTIGEN; CISPLATIN; COMBRETASTATIN A4 PHOSPHATE; GELATINASE B; GRANULOCYTE COLONY STIMULATING FACTOR; MONOCLONAL ANTIBODY DC101; OMBRABULIN; STROMAL CELL DERIVED FACTOR 1; SUNITINIB; VASCULAR TARGETING AGENT; VASCULOTROPIN;

ANIMAL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; C57BL MOUSE; CANCER INFILTRATION; CANCER INHIBITION; CLINICAL ARTICLE; CLINICAL TRIAL; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOLOGY; DRUG DOSE ESCALATION; DRUG EFFECT; DRUG EFFICACY; DRUG RESISTANCE; DRUG SCREENING; ENDOTHELIAL PROGENITOR CELL; ENDOTHELIUM CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HUMAN; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; LOW DRUG DOSE; MALE; MICROVASCULATURE; MOUSE; NECROSIS; NEOPLASM; NONHUMAN; NUDE MOUSE; PATHOLOGY; PHASE 1 CLINICAL TRIAL; PROTEIN EXPRESSION; REVASCULARIZATION; SINGLE DRUG DOSE; STEM CELL; STEM CELL MOBILIZATION; TUMOR CELL LINE; TUMOR RESISTANCE; TUMOR VOLUME;

ANGIOGENESIS INHIBITORS; ANIMALS; CELL LINE, TUMOR; DRUG RESISTANCE, NEOPLASM; ENDOTHELIAL CELLS; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, NUDE; NEOPLASMS; STEM CELLS; TUMOR BURDEN; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84866335646     PISSN: 21598274     EISSN: 21598290     Source Type: Journal    
DOI: 10.1158/2159-8290.CD-11-0171     Document Type: Article

References (55)

1. Horsman MR, Siemann DW. Pathophysiologic effects of vasculartargeting agents and the implications for combination with conventional therapies. Cancer Res 2006;66:11520-39.
2. Tozer GM, Kanthou C, Baguley BC. Disrupting tumour blood vessels. Nat Rev Cancer 2005;5:423-35.
3. Kim JJ, Tannock IF. Repopulation of cancer cells during therapy: an important cause of treatment failure. Nat Rev Cancer 2005;5:516-25.
4. Lara PN Jr, Douillard JY, Nakagawa K, von Pawel J, McKeage MJ, Albert I, et al. Randomized phase III placebo-controlled trial of carboplatin and paclitaxel with or without the vascular disrupting agent vadimezan (ASA404) in advanced non-small-cell lung cancer. J Clin Oncol 2011;29:2965-71.
5. Siemann DW, Chaplin DJ, Horsman MR. Vascular-targeting therapies for treatment of malignant disease. Cancer 2004;100:2491-9.
6. Neri D, Bicknell R. Tumour vascular targeting. Nat Rev Cancer 2005;5:436-46.
7. Tozer GM, Prise VE, Wilson J, Cemazar M, Shan S, Dewhirst MW, et al. Mechanisms associated with tumor vascular shut-down induced by combretastatin A-4 phosphate: intravital microscopy and measurement of vascular permeability. Cancer Res 2001;61:6413-22.
8. Grosios K, Loadman PM, Swaine DJ, Pettit GR, Bibby MC. Combination chemotherapy with combretastatin A-4 phosphate and 5-fluorouracil in an experimental murine colon adenocarcinoma. Anticancer Res 2000;20:229-33.
9. Ng QS, Goh V, Carnell D, Meer K, Padhani AR, Saunders MI, et al. Tumor antivascular effects of radiotherapy combined with combretastatin a4 phosphate in human non-small-cell lung cancer. Int J Radiat Oncol Biol Phys 2007;67:1375-80.
10. Daenen LG, Shaked Y, Man S, Xu P, Voest EE, Hoffman RM, et al. Low-dose metronomic cyclophosphamide combined with vascular disrupting therapy induces potent antitumor activity in preclinical human tumor xenograft models. Mol Cancer Ther 2009;8:2872-81.
11. Chaplin DJ, Horsman MR, Siemann DW. Current development status of small-molecule vascular disrupting agents. Curr Opin Investig Drugs 2006;7:522-8.
12. Rustin GJ, Shreeves G, Nathan PD, Gaya A, Ganesan TS, Wang D, et al. A Phase Ib trial of CA4P (combretastatin A-4 phosphate), carboplatin, and paclitaxel in patients with advanced cancer. Br J Cancer 2010;102:1355-60.
13. Farace F, Bidart JM. Circulating endothelial cells: biomarkers for monitoring activity of antiangiogenic therapy [in French]. Bull Cancer 2007;94 Spec No:S254-9.
14. Siemann DW, Shi W. Dual targeting of tumor vasculature: combining Avastin and vascular disrupting agents (CA4P or OXi4503). Anticancer Res 2008;28:2027-31.
15. Siemann DW, Shi W. Efficacy of combined antiangiogenic and vascular disrupting agents in treatment of solid tumors. Int J Radiat Oncol Biol Phys 2004;60:1233-40.
16. Shaked Y, Ciarrocchi A, Franco M, Lee CR, Man S, Cheung AM, et al. Therapy-induced acute recruitment of circulating endothelial progenitor cells to tumors. Science 2006;313:1785-7.
17. Nathan PD, Judson I, Padhani A, Harris A, Carden CP, Smythe J, et al. A phase I study of combretastatin A-4 phosphate (CA4P) and bevacizumab in subjects with advanced solid tumors. J Clin Oncol 2008;26:(suppl; abstr 3550).
18. Martinelli M, Bonezzi K, Riccardi E, Kuhn E, Frapolli R, Zucchetti M, et al. Sequence dependent antitumour efficacy of the vascular disrupting agent ZD6126 in combination with paclitaxel. Br J Cancer 2007;97:888-94.
19. Asahara T, Murohara T, Sullivan A, Silver M, van der Zee R, Li T, et al. Isolation of putative progenitor endothelial cells for angiogenesis. Science 1997;275:964-7.
20. Asahara T, Masuda H, Takahashi T, Kalka C, Pastore C, Silver M, et al. Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ Res 1999;85:221-8.
21. Rafii S, Heissig B, Hattori K. Efficient mobilization and recruitment of marrow-derived endothelial and hematopoietic stem cells by adenoviral vectors expressing angiogenic factors. Gene Ther 2002;9:631-41.
22. Iwami Y, Masuda H, Asahara T. Endothelial progenitor cells: past, state of the art, and future. J Cell Mol Med 2004;8:488-97.
23. Bertolini F, Shaked Y, Mancuso P, Kerbel RS. The multifaceted circulating endothelial cell in cancer: towards marker and target identification. Nat Rev Cancer 2006;6:835-45.
24. Jain RK, Duda DG. Role of bone marrow-derived cells in tumor angiogenesis and treatment. Cancer Cell 2003;3:515-6.
25. Lyden D, Hattori K, Dias S, Costa C, Blaikie P, Butros L, et al. Impaired recruitment of bone-marrow-derived endothelial and hematopoietic precursor cells blocks tumor angiogenesis and growth. Nat Med 2001;7:1194-201.
26. Nolan DJ, Ciarrocchi A, Mellick AS, Jaggi JS, Bambino K, Gupta S, et al. Bone marrow-derived endothelial progenitor cells are a major determinant of nascent tumor neovascularization. Genes Dev 2007;21:1546-58.
27. Ruzinova MB, Schoer RA, Gerald W, Egan JE, Pandolfi PP, Rafii S, et al. Effect of angiogenesis inhibition by Id loss and the contribution of bone-marrow-derived endothelial cells in spontaneous murine tumors. Cancer Cell 2003;4:277-89.
28. De Palma M, Venneri MA, Roca C, Naldini L. Targeting exogenous genes to tumor angiogenesis by transplantation of genetically modified hematopoietic stem cells. Nat Med 2003;9:789-95.
29. De Palma M, Venneri MA, Galli R, Sergi Sergi L, Politi LS, Sampaolesi M, et al. Tie2 identifies a hematopoietic lineage of proangiogenic monocytes required for tumor vessel formation and a mesenchymal population of pericyte progenitors. Cancer Cell 2005;8:211-26.
30. Purhonen S, Palm J, Rossi D, Kaskenpää N, Rajantie I, Ylä-Herttuala S, et al. Bone marrow-derived circulating endothelial precursors do not contribute to vascular endothelium and are not needed for tumor growth. Proc Natl Acad Sci U S A 2008;105:6620-5.
31. Madlambayan GJ, Butler JM, Hosaka K, Jorgensen M, Fu D, Guthrie SM, Shenoy AK, et al. Bone marrow stem and progenitor cell contribution to neovasculogenesis is dependent on model system with SDF-1 as a permissive trigger. Blood 2009;114:4310-9.
32. Gothert JR, Gustin SE, van Eekelen JA, Schmidt U, Hall MA, Jane SM, et al. Genetically tagging endothelial cells in vivo: bone marrow-derived cells do not contribute to tumor endothelium. Blood 2004;104:1769-77.
33. Gao D, Nolan DJ, Mellick AS, Bambino K, McDonnell K, Mittal V. Endothelial progenitor cells control the angiogenic switch in mouse lung metastasis. Science 2008;319:195-8.
34. Blann AD, Woywodt A, Bertolini F, Bull TM, Buyon JP, Clancy RM, et al. Circulating endothelial cells. Biomarker of vascular disease. Thromb Haemost 2005;93:228-35.
35. Dignat-George F, Sampol J. Circulating endothelial cells in vascular disorders: new insights into an old concept. Eur J Haematol 2000;65:215-20.
36. Dignat-George F, Sampol J, Lip G, Blann AD. Circulating endothelial cells: realities and promises in vascular disorders. Pathophysiol Haemost Thromb 2003;33:495-9.
37. Farace F, Massard C, Borghi E, Bidart JM, Soria JC. Vascular disrupting therapy-induced mobilization of circulating endothelial progenitor cells. Ann Oncol 2007;18:1421-2.
38. Beerepoot LV, Radema SA, Witteveen EO, Thomas T, Wheeler C, Kempin S, et al. Phase I clinical evaluation of weekly administration of the novel vascular-targeting agent, ZD6126, in patients with solid tumors. J Clin Oncol 2006;24:1491-8.
39. Dark GG, Hill SA, Prise VE, Tozer GM, Pettit GR, Chaplin DJ. Combretastatin A-4, an agent that displays potent and selective toxicity toward tumor vasculature. Cancer Res 1997;57:1829-34.
40. Jacques N, Vimond N, Conforti R, Griscelli F, Lecluse Y, Laplanche A, et al. Quantification of circulating mature endothelial cells using a whole blood four-color flow cytometric assay. J Immunol Methods 2008;337:132-43.
41. Taylor M, Rossler J, Geoerger B, Laplanche A, Hartmann O, Vassal G, et al. High levels of circulating VEGFR2+ Bone marrow-derived progenitor cells correlate with metastatic disease in patients with pediatric solid malignancies. Clin Cancer Res 2009;15:4561-71.
42. Yang J, Ii M, Kamei N, Alev C, Kwon SM, Kawamoto A, et al. CD34 cells represent highly functional endothelial progenitor cells in murine bone marrow. PLoS One 2011;6:e20219.
43. Shaked Y, Henke E, Roodhart JM, Mancuso P, Langenberg MH, Colleoni M, et al. Rapid chemotherapy-induced acute endothelial progenitor cell mobilization: implications for antiangiogenic drugs as chemosensitizing agents. Cancer Cell 2008;14:263-73.
44. Guerin O, Formento P, Lo Nigro C, Hofman P, Fischel JL, Etienne-Grimaldi MC, et al. Supra-additive antitumor effect of sunitinib malate (SU11248, Sutent) combined with docetaxel. A new therapeutic perspective in hormone refractory prostate cancer. J Cancer Res Clin Oncol 2008;134:51-7.
45. Li H, Gerald WL, Benezra R. Utilization of bone marrow-derived endothelial cell precursors in spontaneous prostate tumors varies with tumor grade. Cancer Res 2004;64:6137-43.
46. Shaked Y, Tang T, Woloszynek J, Daenen LG, Man S, Xu P, Cai SR, et al. Contribution of granulocyte colony-stimulating factor to the acute mobilization of endothelial precursor cells by vascular disrupting agents. Cancer Res 2009;69:7524-8.
47. Welford AF, Biziato D, Coffelt SB, Nucera S, Fisher M, Pucci F, et al. TIE2-expressing macrophages limit the therapeutic efficacy of the vascular-disrupting agent combretastatin A4 phosphate in mice. J Clin Invest 2011;121:1969-73.
48. Heissig B, Hattori K, Dias S, Friedrich M, Ferris B, Hackett NR, et al. Recruitment of stem and progenitor cells from the bone marrow niche requires MMP-9 mediated release of kit-ligand. Cell 2002;109:625-37.
49. Du R, Lu KV, Petritsch C, Liu P, Ganss R, Passegué E, et al. HIF1alpha induces the recruitment of bone marrow-derived vascular modulatory cells to regulate tumor angiogenesis and invasion. Cancer Cell 2008;13:206-20.
50. Seandel M, Butler J, Lyden D, Rafii S. A catalytic role for proangiogenic marrow-derived cells in tumor neovascularization. Cancer Cell 2008;13:181-3.
51. Yang L, DeBusk LM, Fukuda K, Fingleton B, Green-Jarvis B, Shyr Y, et al. Expansion of myeloid immune suppressor Gr+CD11b+ cells in tumor-bearing host directly promotes tumor angiogenesis. Cancer Cell 2004;6:409-21.
52. Condeelis J, Pollard JW. Macrophages: obligate partners for tumor cell migration, invasion, and metastasis. Cell 2006;124:263-6.
53. Shintani S, Murohara T, Ikeda H, Ueno T, Honma T, Katoh A, et al. Mobilization of endothelial progenitor cells in patients with acute myocardial infarction. Circulation 2001;103:2776-9.
54. Kalka C, Tehrani H, Laudenberg B, Vale PR, Isner JM, Asahara T, et al. VEGF gene transfer mobilizes endothelial progenitor cells in patients with inoperable coronary disease. Ann Thorac Surg 2000;70:829-34.
55. Strijbos MH, Gratama JW, Kraan J, Lamers CH, den Bakker MA, Sleijfer S. Circulating endothelial cells in oncology: pitfalls and promises. Br J Cancer 2008;98:1731-5.