FAK regulates platelet extravasation and tumor growth after antiangiogenic therapy withdrawal

Journal of Clinical Investigation

Volumn 126, Issue 5, 2016, Pages 1885-1896

  Haemmerle, Monika ^a   Bottsford Miller, Justin ^a   Pradeep, Sunila ^a   Taylor, Morgan L ^a   Choi, Hyun Jin ^a   Hansen, Jean M ^a   Dalton, Heather J ^a   Stone, Rebecca L ^a   Cho, Min Soon ^a   Nick, Alpa M ^a   Nagaraja, Archana S ^a   Gutschner, Tony ^a   Gharpure, Kshipra M ^a   Mangala, Lingegowda S ^a   Rupaimoole, Rajesha ^a   Han, Hee Dong ^a,d   Zand, Behrouz ^a   Armaiz Pena, Guillermo N ^a   Wu, Sherry Y ^a   Pecot, Chad V ^b   Burns, Alan R ^c   Lopez Berestein, Gabriel ^a   Afshar Kharghan, Vahid ^a   Sood, Anil K ^a   more..

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF HOUSTON   (United States)

^d Konkuk University School of Medicine   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE; BEVACIZUMAB; FOCAL ADHESION KINASE; FOCAL ADHESION KINASE INHIBITOR; GSK 2256098; PAZOPANIB; UNCLASSIFIED DRUG; VASCULOTROPIN ANTIBODY; ANTINEOPLASTIC AGENT; CANCER ANTIBODY; FOCAL ADHESION KINASE 1; PTK2 PROTEIN, HUMAN; PTK2 PROTEIN, MOUSE; PYRIMIDINE DERIVATIVE; SULFONAMIDE; TUMOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC THERAPY; ARTICLE; CANCER INHIBITION; COMPARATIVE STUDY; CONTROLLED STUDY; EXTRAVASATION; FEMALE; HUMAN; HUMAN CELL; HYPOXIA; MOUSE; MOUSE MODEL; NONHUMAN; OVARY CANCER; PLATELET EXTRAVASATION; PLATELET INFILTRATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; THROMBOCYTE COUNT; THROMBOCYTE FUNCTION; TREATMENT WITHDRAWAL; TUMOR MICROENVIRONMENT; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL HYPOXIA; DRUG EFFECTS; DRUG SCREENING; ENZYMOLOGY; GENETICS; KNOCKOUT MOUSE; METABOLISM; NEOVASCULARIZATION, PATHOLOGIC; OVARIAN NEOPLASMS; PATHOLOGY; THROMBOCYTE; TUMOR CELL LINE;

ADENOSINE DIPHOSPHATE; ANIMALS; ANTIBODIES, NEOPLASM; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; BEVACIZUMAB; BLOOD PLATELETS; CELL HYPOXIA; CELL LINE, TUMOR; FEMALE; FOCAL ADHESION KINASE 1; HUMANS; MICE; MICE, KNOCKOUT; NEOPLASM PROTEINS; NEOVASCULARIZATION, PATHOLOGIC; OVARIAN NEOPLASMS; PYRIMIDINES; SULFONAMIDES; TUMOR MICROENVIRONMENT; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84988489941     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI85086     Document Type: Article

References (62)

1. Folkman J. Tumor angiogenesis: therapeutic implications. N Engl J Med. 1971;285(21):1182-1186.
2. Blagosklonny MV. Antiangiogenic therapy and tumor progression. Cancer Cell. 2004;5(1):13-17.
3. Choi HJ, Armaiz Pena GN, Pradeep S, Cho MS, Coleman RL, Sood AK. Anti-vascular therapies in ovarian cancer: moving beyond anti-VEGF approaches. Cancer Metastasis Rev. 2015;34(1):19-40.
4. Hurwitz H, et al. Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer. N Engl J Med. 2004;350(23):2335-2342.
5. Miller K, et al. Paclitaxel plus bevacizumab versus paclitaxel alone for metastatic breast cancer. N Engl J Med. 2007;357(26):2666-2676.
6. Loges S, Mazzone M, Hohensinner P, Carmeliet P. Silencing or fueling metastasis with VEGF inhibitors: antiangiogenesis revisited. Cancer Cell. 2009;15(3):167-170.
7. Welti J, Loges S, Dimmeler S, Carmeliet P. Recent molecular discoveries in angiogenesis and antiangiogenic therapies in cancer. J Clin Invest. 2013;123(8):3190-3200.
8. Perren TJ, et al. A phase 3 trial of bevacizumab in ovarian cancer. N Engl J Med. 2011;365(26):2484-2496.
9. Oza AM, et al. Standard chemotherapy with or without bevacizumab for women with newly diagnosed ovarian cancer (ICON7): overall survival results of a phase 3 randomised trial. Lancet Oncol. 2015;16(8):928-936.
10. Burger RA, et al. Incorporation of bevacizumab in the primary treatment of ovarian cancer. N Engl J Med. 2011;365(26):2473-2483.
11. Griffioen AW, et al. Rapid angiogenesis onset after discontinuation of sunitinib treatment of renal cell carcinoma patients. Clin Cancer Res. 2012;18(14):3961-3971.
12. Mancuso MR, et al. Rapid vascular regrowth in tumors after reversal of VEGF inhibition. J Clin Invest. 2006;116(10):2610-2621.
13. Sharpe K, et al. The effect of VEGF-targeted therapy on biomarker expression in sequential tissue from patients with metastatic clear cell renal cancer. Clin Cancer Res. 2013;19(24):6924-6934.
14. Ebos JM, Lee CR, Cruz-Munoz W, Bjarnason GA, Christensen JG, Kerbel RS. Accelerated metastasis after short-term treatment with a potent inhibitor of tumor angiogenesis. Cancer Cell. 2009;15(3):232-239.
15. Rubenstein JL, et al. Anti-VEGF antibody treat-ment of glioblastoma prolongs survival but results in increased vascular cooption. Neoplasia. 2000;2(4):306-314.
16. Paez-Ribes M, et al. Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell. 2009;15(3):220-231.
17. Riess L. Zur pathologischen Anatomie des Blutes. Arch Anat Physiol Wissensch Med. 1872;39:237-249.
18. Trousseau ABV, Cormack J. Lectures On Clinical Medicine, Delivered At The Hôtel-Dieu, Paris. London, United Kingdom: R Hardwicke; 1867.
19. Cho MS, et al. Platelets increase the proliferation of ovarian cancer cells. Blood. 2012;120(24):4869-4872.
20. Bottsford-Miller J, et al. Differential platelet levels affect response to taxane-based therapy in ovarian cancer. Clin Cancer Res. 2015;21(3):602-610.
21. Labelle M, Begum S, Hynes RO. Direct signaling between platelets and cancer cells induces an epithelial-mesenchymal-like transition and promotes metastasis. Cancer Cell. 2011;20(5):576-590.
22. Labelle M, Begum S, Hynes RO. Platelets guide the formation of early metastatic niches. Proc Natl Acad Sci U S A. 2014;111(30):E3053-E3061.
23. Stone RL, et al. Paraneoplastic thrombocytosis in ovarian cancer. N Engl J Med. 2012;366(7):610-618.
24. Klement GL, et al. Platelets actively sequester angiogenesis regulators. Blood. 2009;113(12):2835-2842.
25. Pinedo HM, Verheul HM, D'Amato RJ, Folkman J. Involvement of platelets in tumour angiogenesis? Lancet. 1998;352(9142):1775-1777.
26. Stone R, et al. Unraveling the century-old mystery of paraneoplastic thrombocytosis in ovarian cancer. Gynecol Oncol. 2012;127(1 suppl):S2.
27. Noto T, et al. Temporal and topographic profiles of tissue hypoxia following transient focal cerebral ischemia in rats. J Vet Med Sci. 2006;68(8):803-807.
28. Serebrovskaya TV, Nikolsky IS, Nikolska VV, Mallet RT, Ishchuk VA. Intermittent hypoxia mobilizes hematopoietic progenitors and augments cellular and humoral elements of innate immunity in adult men. High Alt Med Biol. 2011;12(3):243-252.
29. Oga T, et al. Effects of obstructive sleep apnea with intermittent hypoxia on platelet aggregability. J Atheroscler Thromb. 2009;16(6):862-869.
30. Raju NC, Eikelboom JW, Hirsh J. Platelet ADPreceptor antagonists for cardiovascular disease: past, present and future. Nat Clin Pract Cardiovasc Med. 2008;5(12):766-780.
31. Bastida E, Ordinas A, Giardina SL, Jamieson GA. Differentiation of platelet-aggregating effects of human tumor cell lines based on inhibition studies with apyrase, hirudin, and phospholipase. Cancer Res. 1982;42(11):4348-4352.
32. Egan K, et al. Platelet adhesion and degranulation induce pro-survival and pro-angiogenic signalling in ovarian cancer cells. PLoS One. 2011;6(10):e26125.
33. Hitchcock IS, Fox NE, Prevost N, Sear K, Shattil SJ, Kaushansky K. Roles of focal adhesion kinase (FAK) in megakaryopoiesis and platelet function: studies using a megakaryocyte lineage specific FAK knockout. Blood. 2008;111(2):596-604.
34. Thanapprapa D, et al. PTEN expression as a predictor of response to focal adhesion kinase inhibition in uterine cancer. Mol Cancer Ther. 2015;14(6):1466-1475.
35. Stone RL, et al. Focal adhesion kinase: an alternative focus for anti-angiogenesis therapy in ovarian cancer. Cancer Biol Ther. 2014;15(7):919-929.
36. Schultze A, Fiedler W. Clinical importance and potential use of small molecule inhibitors of focal adhesion kinase. Anticancer Agents Med Chem. 2011;11(7):593-599.
37. Zhang J, He DH, Zajac-Kaye M, Hochwald SN. A small molecule FAK kinase inhibitor, GSK2256098, inhibits growth and survival of pancreatic ductal adenocarcinoma cells. Cell Cycle. 2014;13(19):3143-3149.
38. Pujade-Lauraine E, et al. Bevacizumab combined with chemotherapy for platinum-resistant recurrent ovarian cancer: The AURELIA openlabel randomized phase III trial. J Clin Oncol. 2014;32(13):1302-1308.
39. Stockler MR, et al. Patient-reported outcome results from the open-label phase III AURELIA trial evaluating bevacizumab-containing therapy for platinum-resistant ovarian cancer. J Clin Oncol. 2014;32(13):1309-1316.
40. Tomao F, Tomao S, Benedetti Panici P. Combination of bevacizumab and chemotherapy for platinum-resistant recurrent ovarian cancer: some observations about the AURELIA trial. J Clin Oncol. 2014;32(31):3580.
41. Katsumata N, et al. Dose-dense paclitaxel once a week in combination with carboplatin every 3 weeks for advanced ovarian cancer: a phase 3, open-label, randomised controlled trial. Lancet. 2009;374(9698):1331-1338.
42. McGuire WP, et al. Cyclophosphamide and cisplatin compared with paclitaxel and cisplatin in patients with stage III and stage IV ovarian cancer. N Engl J Med. 1996;334(1):1-6.
43. Bennouna J, et al. Continuation of bevacizumab after first progression in metastatic colorectal cancer (ML18147): a randomised phase 3 trial. Lancet Oncol. 2013;14(1):29-37.
44. von Minckwitz G, et al. Bevacizumab plus chemotherapy versus chemotherapy alone as second-line treatment for patients with HER2-negative locally recurrent or metastatic breast cancer after firstline treatment with bevacizumab plus chemotherapy (TANIA): an open-label, randomised phase 3 trial. Lancet Oncol. 2014;15(11):1269-1278.
45. De Bock K, Mazzone M, Carmeliet P. Antiangiogenic therapy, hypoxia, and metastasis: risky liaisons, or not? Nat Rev Clin Oncol. 2011;8(7):393-404.
46. Bagri A, et al. Effects of anti-VEGF treatment duration on tumor growth, tumor regrowth, and treatment efficacy. Clin Cancer Res. 2010;16(15):3887-3900.
47. Fidler IJ. Angiogenic heterogeneity: regulation of neoplastic angiogenesis by the organ microenvironment. J Natl Cancer Inst. 2001;93(14):1040-1041.
48. Jain RK. Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science. 2005;307(5706):58-62.
49. Nagy JA, Chang SH, Shih SC, Dvorak AM, Dvorak HF. Heterogeneity of the tumor vasculature. Semin Thromb Hemost. 2010;36(3):321-331.
50. Casanovas O, Hicklin DJ, Bergers G, Hanahan D. Drug resistance by evasion of antiangiogenic targeting of VEGF signaling in late-stage pancreatic islet tumors. Cancer Cell. 2005;8(4):299-309.
51. Fernando NT, et al. Tumor escape from endogenous, extracellular matrix-associated angiogenesis inhibitors by up-regulation of multiple proangiogenic factors. Clin Cancer Res. 2008;14(5):1529-1539.
52. Franco M, et al. Targeted anti-vascular endothelial growth factor receptor-2 therapy leads to short-term and long-term impairment of vascular function and increase in tumor hypoxia. Cancer Res. 2006;66(7):3639-3648.
53. Levin J, Conley CL. Thrombocytosis associated with malignant disease. Arch Intern Med. 1964;114:497-500.
54. Borsig L. The role of platelet activation in tumor metastasis. Expert Rev Anticancer Ther. 2008;8(8):1247-1255.
55. Noto T, et al. Tacrolimus (FK506) limits accumulation of granulocytes and platelets and protects against brain damage after transient focal cerebral ischemia in rat. Biol Pharm Bull. 2007;30(2):313-317.
56. Qi C, et al. P-Selectin-mediated adhesion between platelets and tumor cells promotes intestinal tumorigenesis in Apc(Min/+) mice. Int J Biol Sci. 2015;11(6):679-687.
57. Pertuy F, et al. Broader expression of the mouse platelet factor 4-cre transgene beyond the megakaryocyte lineage. J Thromb Haemost. 2015;13(1):115-125.
58. Thijs T, Deckmyn H, Broos K. Model systems of genetically modified platelets. Blood. 2012;119(7):1634-1642.
59. Auger KR, et al. 387 The focal adhesion kinase inhibitor GSK2256098: a potent and selective inhibitor for the treatment of cancer. Eur J Cancer. 2012;48:118.
60. Golubovskaya VM. Focal adhesion kinase as a cancer therapy target. Anti-cancer agents in medicinal chemistry. 2010;10(10):735-741.
61. Rupaimoole R, et al. Hypoxia-mediated downregulation of miRNA biogenesis promotes tumour progression. Nat Commun. 2014;5:5202.
62. Lu C, et al. Regulation of tumor angiogenesis by EZH2. Cancer Cell. 2010;18(2):185-197.