FAK-heterozygous mice display enhanced tumour angiogenesis

Nature Communications

Volumn 4, Issue , 2013, Pages

  Kostourou, Vassiliki ^a,b   Lechertier, Tanguy ^b   Reynolds, Louise E ^b   Lees, Delphine M ^b   Baker, Marianne ^b   Jones, Dylan T ^b   Tavora, Bernardo ^b   Ramjaun, Antoine R ^b   Birdsey, Graeme M ^c   Robinson, Stephen D ^b,e   Parsons, Maddy ^d   Randi, Anna M ^c   Hart, Ian R ^b   Hodivala Dilke, Kairbaan ^b  

^a BIOMEDICAL SCIENCES RESEARCH CENTER ALEXANDER FLEMING   (Greece)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^c HAMMERSMITH HOSPITAL   (United Kingdom)

^d KING'S COLLEGE LONDON   (United Kingdom)

^e UNIVERSITY OF EAST ANGLIA   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; FOCAL ADHESION KINASE; FOCAL ADHESION KINASE 2; FOCAL ADHESION KINASE INHIBITOR; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PF 573228; PROTEIN KINASE B; UNCLASSIFIED DRUG; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2; FOCAL ADHESION KINASE 1; MUTANT PROTEIN; PAXILLIN; PTK2 PROTEIN, MOUSE; TALIN; VINCULIN;

ALLELE; ANGIOGENESIS; ANIMAL CELL; ARTICLE; AUTOPHOSPHORYLATION; CANCER GROWTH; CANCER SIZE; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; HETEROZYGOSITY; IMMUNOFLUORESCENCE; LUNG CARCINOMA; MELANOMA; MICROVASCULATURE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TUMOR VASCULARIZATION; VASCULAR RING; WESTERN BLOTTING; ANIMAL; CELL SEPARATION; ENZYMOLOGY; HETEROZYGOTE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; METABOLISM; NEOPLASM; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; SUBCUTANEOUS TISSUE; TUMOR VOLUME; VASCULARIZATION;

MUS;

ANIMALS; CELL PROLIFERATION; CELL SEPARATION; CELL SURVIVAL; ENDOTHELIAL CELLS; FOCAL ADHESION KINASE 1; HETEROZYGOTE; IMMUNOHISTOCHEMISTRY; MICE; MUTANT PROTEINS; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; PAXILLIN; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; SUBCUTANEOUS TISSUE; TALIN; TUMOR BURDEN; VINCULIN; IN VITRO TECHNIQUES;

EID: 84886101162     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms3020     Document Type: Article

References (52)

1. Mitra, S. K. & Schlaepfer, D. D. Integrin-regulated FAK-Src signaling in normal and cancer cells. Curr. Opin. Cell. Biol. 18, 516-523 (2006).
2. Mitra, S. K., Hanson, D. A. & Schlaepfer, D. D. Focal adhesion kinase: in command and control of cell motility. Nat. Rev. Mol. Cell. Biol. 6, 56-68 (2005).
3. McLean, G. W. et al. The role of focal-adhesion kinase in cancer - a new therapeutic opportunity. Nat. Rev. Cancer. 5, 505-515 (2005).
4. Li, S. & Hua, Z. FAK expression regulation and therapeutic potential. Adv. Cancer. Res. 101, 45-61 (2008).
5. Calalb, M. B., Zhang, X., Polte, T. R. & Hanks, S. K. Focal adhesion kinase tyrosine-861 is a major site of phosphorylation by Src. Biochem. Biophys. Res. Commun. 228, 662-668 (1996).
6. Qi, J. H. & Claesson-Welsh, L. VEGF-induced activation of phosphoinositide 3-kinase is dependent on focal adhesion kinase. Exp. Cell. Res. 263, 173-182 (2001).
7. Abu-Ghazaleh, R., Kabir, J., Jia, H., Lobo, M. & Zachary, I. Src mediates stimulation by vascular endothelial growth factor of the phosphorylation of focal adhesion kinase at tyrosine 861, and migration and anti-apoptosis in endothelial cells. Biochem. J. 360, 255-264 (2001).
8. Sieg, D. J. et al. FAK integrates growth-factor and integrin signals to promote cell migration. Nat. Cell. Biol. 2, 249-256 (2000).
9. Haskell, H. et al. Focal adhesion kinase is expressed in the angiogenic blood vessels of malignant astrocytic tumors in vivo and promotes capillary tube formation of brain microvascular endothelial cells. Clin. Cancer. Res. 9, 2157-2165 (2003).
10. Ilic, D. et al. Focal adhesion kinase is required for blood vessel morphogenesis. Circ. Res. 92, 300-307 (2003).
11. Braren, R. et al. Endothelial FAK is essential for vascular network stability, cell survival, and lamellipodial formation. J. Cell. Biol. 172, 151-162 (2006).
12. Shen, T.-L. et al. Conditional knockout of focal adhesion kinase in endothelial cells reveals its role in angiogenesis and vascular development in late embryogenesis. J. Cell. Biol. 169, 941-952 (2005).
13. Peng, X. et al. Overexpression of focal adhesion kinase in vascular endothelial cells promotes angiogenesis in transgenic mice. Cardiovasc. Res. 64, 421-430 (2004).
14. Weis, S. M. et al. Compensatory role for Pyk2 during angiogenesis in adult mice lacking endothelial cell FAK. J. Cell. Biol. 181, 43-50 (2008).
15. Tavora, B. et al. Endothelial FAK is required for tumour angiogenesis. EMBO. Mol. Med. 2, 516-528 (2010).
16. Sweeney, S. M. et al. Angiogenesis in collagen I requires alpha2beta1 ligation of a GFP∗GER sequence and possibly p38 MAPK activation and focal adhesion disassembly. J. Biol. Chem. 278, 30516-30524 (2003).
17. Nakamura, J. et al. Biphasic function of focal adhesion kinase in endothelial tube formation induced by fibril-forming collagens. Biochem. Biophys. Res. Commun. 374, 699-703 (2008).
18. Lim, S.-T. et al. Nuclear FAK promotes cell proliferation and survival through FERM-enhanced p53 degradation. Mol. Cell. 29, 9-22 (2008).
19. Cai, X. et al. Spatial and temporal regulation of focal adhesion kinase activity in living cells. Mol. Cell. Biol. 28, 201-214 (2008).
20. McLean, G. W. et al. Decreased focal adhesion kinase suppresses papilloma formation during experimental mouse skin carcinogenesis. Cancer. Res. 61, 8385 (2001).
21. Kostourou, V., Robinson, S. P., Cartwright, J. E. & Whitley, G. S. J. Dimethylarginine dimethylaminohydrolase I enhances tumour growth and angiogenesis. Br. J. Cancer. 87, 673-680 (2002).
22. Noguera-Troise, I. et al. Blockade of Dll4 inhibits tumour growth by promoting non-productive angiogenesis. Nature 444, 1032-1037 (2006).
23. Murdoch, C., Muthana, M., Coffelt, S. B. & Lewis, C. E. The role of myeloid cells in the promotion of tumour angiogenesis. Nat. Rev. Cancer 8, 618-631 (2008).
24. Tartour, E. et al. Angiogenesis and immunity: a bidirectional link potentially relevant for the monitoring of antiangiogenic therapy and the development of novel therapeutic combination with immunotherapy. Cancer Metastasis. Rev. 30, 83-95 (2011).
25. Arnaoutova, I. & Kleinman, H. K. In vitro angiogenesis: endothelial cell tube formation on gelled basement membrane extract. Nat. Protoc. 5, 628-635 (2010).
26. Slack-Davis, J. K. et al. Cellular characterization of a novel focal adhesion kinase inhibitor. J. Biol. Chem. 282, 14845-14852 (2007).
27. Wendt, M. K. & Schiemann, W. P. Therapeutic targeting of the focal adhesion complex prevents oncogenic TGF-β signaling and metastasis. Breast Cancer Res. 11, R68 (2009).
28. Roberts, W. G. et al. Antitumor activity and pharmacology of a selective focal adhesion kinase inhibitor, PF-562,271. Cancer Res. 68, 1935-1944 (2008).
29. Slack-Davis, J. K., Hershey, E. D., Theodorescu, D., Frierson, H. F. & Parsons, J. T. Differential requirement for focal adhesion kinase signaling in cancer progression in the transgenic adenocarcinoma of mouse prostate model. Mol. Cancer Ther. 8, 2470-2477 (2009).
30. Luo, M. & Guan, J.-L. Focal adhesion kinase: a prominent determinant in breast cancer initiation, progression and metastasis. Cancer Lett. 289, 127-139 (2010).
31. Schmitz, K. J. et al. High expression of focal adhesion kinase (p125FAK) in node-negative breast cancer is related to overexpression of HER-2/neu and activated Akt kinase but does not predict outcome. Breast Cancer Res. 7, R194-R203 (2005).
32. Furuyama, K. et al. Clinical significance of focal adhesion kinase in resectable pancreatic cancer. World J. Surg. 30, 219-226 (2006).
33. Theocharis, S. E. et al. Focal adhesion kinase expression is not a prognostic predictor in colon adenocarcinoma patients. Eur. J. Surg. Oncol. 29, 571-574 (2003).
34. Ozkal, S. et al. Focal adhesion kinase (FAK) expression in normal and neoplastic lymphoid tissues. Pathol. Res. Pract. 205, 781-788 (2009).
35. Carelli, S. et al. Up-regulation of focal adhesion kinase in non-small cell lung cancer. Lung. Cancer 53, 263-271 (2006).
36. Lahlou, H. et al. Mammary epithelial-specific disruption of the focal adhesion kinase blocks mammary tumor progression. Proc. Natl Acad. Sci. USA 104, 20302-20307 (2007).
37. Brunton, V. G. & Frame, M. C. Src and focal adhesion kinase as therapeutic targets in cancer. Curr. Opin. Pharmacol. 8, 427-432 (2008).
38. Reynolds, A. R. et al. Stimulation of tumor growth and angiogenesis by low concentrations of RGD-mimetic integrin inhibitors. Nat. Med. 15, 392-400 (2009).
39. Lietha, D. et al. Structural basis for the autoinhibition of focal adhesion kinase. Cell 129, 1177-1187 (2007).
40. Lunn, J. A., Jacamo, R. & Rozengurt, E. Preferential phosphorylation of focal adhesion kinase tyrosine 861 is critical for mediating an anti-apoptotic response to hyperosmotic stress. J. Biol. Chem. 282, 10370-10379 (2007).
41. Kuramochi, Y., Guo, X. & Sawyer, D. B. Neuregulin activates erbB2-dependent src/FAK signaling and cytoskeletal remodeling in isolated adult rat cardiac myocytes. J. Mol. Cell. Cardiol. 41, 228-235 (2006).
42. Lim, Y. et al. Phosphorylation of focal adhesion kinase at tyrosine 861 is crucial for Ras transformation of fibroblasts. J. Biol. Chem. 279, 29060-29065 (2004).
43. Ackah, E. et al. Akt1/protein kinase Balpha is critical for ischemic and VEGF-mediated angiogenesis. J. Clin. Invest. 115, 2119-2127 (2005).
44. Phung, T. L. et al. Pathological angiogenesis is induced by sustained Akt signaling and inhibited by rapamycin. Cancer Cell 10, 159-170 (2006).
45. Wang, S. & Basson, M. D. Akt directly regulates focal adhesion kinase through association and serine phosphorylation: implication for pressure-induced colon cancer metastasis. AJP: Cell Physiol. 300, C657-C670 (2011).
46. Zhao, X., Peng, X., Sun, S., Park, A. Y. J. & Guan, J.-L. Role of kinase-independent and -dependent functions of FAK in endothelial cell survival and barrier function during embryonic development. J. Cell. Biol. 189, 955-965 (2010).
47. Golubovskaya, V. & Cance, W. Focal adhesion kinase and p53 signaling in cancer cells. Int. Rev. Cytol. 263, 103-153 (2007).
48. Park, E. K. et al. Cholesterol depletion induces anoikis-like apoptosis via FAK down-regulation and caveolae internalization. J. Pathol. 218, 337-349 (2009).
49. Sandilands, E. et al. Autophagic targeting of Src promotes cancer cell survival following reduced FAK signalling. Nat. Cell. Biol. 14, 51-60 (2011).
50. Reynolds, L. E. & Hodivala-Dilke, K. M. Primary mouse endothelial cell culture for assays of angiogenesis. Methods Mol. Med. 120, 503-509 (2006).
51. Germain, M. et al. Genetic ablation of the alpha 6-integrin subunit in Tie1Cre mice enhances tumour angiogenesis. J. Pathol. 220, 370-381 (2010).
52. Baker, M. et al. Use of the mouse aortic ring assay to study angiogenesis. Nat. Protoc. 7, 89-104 (2011).