Fibroblast growth factor 9 imparts hierarchy and vasoreactivity to the microcirculation of renal tumors and suppresses metastases

Journal of Biological Chemistry

Volumn 290, Issue 36, 2015, Pages 22127-22142

  Yin, Hao ^a   Frontini, Matthew J ^a,b   Arpino, John Michael ^a,b   Nong, Zengxuan ^a   O'Neil, Caroline ^a   Xu, Yiwen ^a,b   Balint, Brittany ^a,b   Ward, Aaron D ^b   Chakrabarti, Subrata ^b   Ellis, Christopher G ^b   Gros, Robert ^a,b   Pickering, J Geoffrey ^a,b,c  

^a ROBARTS RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF WESTERN ONTARIO   (Canada)

^c LONDON HEALTH SCIENCES CENTRE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD VESSELS; CELL CULTURE; FIBROBLASTS; MICROCIRCULATION; PATHOLOGY;

BLOOD FLOW; FIBROBLAST GROWTH FACTOR-9; MICROVASCULAR; MICROVESSELS; RENAL TUMORS; STROMAL CELLS; TUMOR HYPOXIA; VASOREACTIVITY;

TUMORS;

ALPHA ACTIN; CD31 ANTIGEN; FIBROBLAST GROWTH FACTOR 9; KI 67 ANTIGEN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; VASCULOTROPIN A; FGF9 PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERIOLE; ARTICLE; BASEMENT MEMBRANE; BLOOD VESSEL PARAMETERS; CAPILLARY; CELL ACTIVATION; CELL DIFFERENTIATION; CELL DIVISION; CELL MIGRATION; COLLAGEN FORTIFIED BASEMENT MEMBRANE; CONTROLLED STUDY; DRUG MECHANISM; EMBRYO; ENZYME ACTIVATION; FEMALE; HIERARCHICAL VESSEL NETWORK; HISTOPATHOLOGY; HYPOXIA; KIDNEY BLOOD FLOW; KIDNEY TUMOR; LUNG METASTASIS; MESENCHYMAL STROMA CELL; METASTASIS INHIBITION; MICROCIRCULATION; MOUSE; NONHUMAN; PERICYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RENAL CANCER CELL LINE; RENCA CELL LINE; SMOOTH MUSCLE FIBER; TUMOR HYPOXIA; TUMOR MICROCIRCULATION; TUMOR VASCULARIZATION; VASOCONSTRICTION; VASODILATATION; VASOREACTIVITY; VENULE; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; CELL CULTURE; CELL LINE; GENE EXPRESSION REGULATION; GENETICS; HUMAN; IMMUNOBLOTTING; LUNG TUMOR; METABOLISM; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SECONDARY; TRANSGENE; TUMOR CELL LINE; VASCULARIZATION;

ANIMALS; CELL LINE; CELL LINE, TUMOR; CELLS, CULTURED; FEMALE; FIBROBLAST GROWTH FACTOR 9; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOBLOTTING; KIDNEY NEOPLASMS; LUNG NEOPLASMS; MICE, INBRED BALB C; MICE, INBRED C57BL; MICROCIRCULATION; RECEPTOR, PLATELET-DERIVED GROWTH FACTOR BETA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSGENES; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84941343675     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.652222     Document Type: Article

References (49)

1. Folkman, J. (1971) Tumor angiogenesis: Therapeutic implications. N. Engl. J. Med. 285, 1182-1186.
2. Chung, A. S., Lee, J., and Ferrara, N. (2010) Targeting the tumour vasculature: insights from physiological angiogenesis. Nat. Rev. Cancer 10, 505-514.
3. Ebos, J. M., and Kerbel, R. S. (2011) Antiangiogenic therapy: impact on invasion, disease progression, and metastasis. Nat. Rev. Clin. Oncol. 8, 210-221.
4. Jain, R. K. (2005) Normalization of tumor vasculature: An emerging concept in antiangiogenic therapy. Science 307, 58-62.
5. Nagy, J. A., Chang, S. H., Dvorak, A. M., and Dvorak, H. F. (2009) Why are tumour blood vessels abnormal and why is it important to know? Br. J. Cancer 100, 865-869.
6. Fukumura, D., Duda, D. G., Munn, L. L., and Jain, R. K. (2010) Tumor microvasculature and microenvironment: Novel insights through intravital imaging in pre-clinical models. Microcirculation 17, 206-225.
7. De Bock, K., Mazzone, M., and Carmeliet, P. (2011) Antiangiogenic therapy, hypoxia, and metastasis: Risky liaisons, or not? Nat. Rev. Clin. Oncol. 8, 393-404.
8. Goel, S., Duda, D. G., Xu, L., Munn, L. L., Boucher, Y., Fukumura, D., and Jain, R. K. (2011) Normalization of the vasculature for treatment of cancer and other diseases. Physiol. Rev. 91, 1071-1121.
9. Pàez-Ribes, M., Allen, E., Hudock, J., Takeda, T., Okuyama, H., Viñals, F., Inoue, M., Bergers, G., Hanahan, D., and Casanovas, O. (2009) Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell 15, 220-231.
10. Ebos, J. M., Lee, C. R., Cruz-Munoz, W., Bjarnason, G. A., Christensen, J. G., and Kerbel, R. S. (2009) Accelerated metastasis after short-term treatment with a potent inhibitor of tumor angiogenesis. Cancer Cell 15, 232-239.
11. Tong, R. T., Boucher, Y., Kozin, S. V., Winkler, F., Hicklin, D. J., and Jain, R. K. (2004) Vascular normalization by vascular endothelial growth factor receptor 2 blockade induces a pressure gradient across the vasculature and improves drug penetration in tumors. Cancer Res. 64, 3731-3736.
12. Mazzone, M., Dettori, D., Leite de Oliveira, R., Loges, S., Schmidt, T., Jonckx, B., Tian, Y. M., Lanahan, A. A., Pollard, P., Ruiz de Almodovar, C., De Smet, F., Vinckier, S., Aragonés, J., Debackere, K., Luttun, A., Wyns, S., Jordan, B., Pisacane, A., Gallez, B., Lampugnani, M. G., Dejana, E., Simons, M., Ratcliffe, P., Maxwell, P., and Carmeliet, P. (2009) Heterozygous defi- ciency of PHD2 restores tumor oxygenation and inhibits metastasis via endothelial normalization. Cell 136, 839-851.
13. Maes, H., Kuchnio, A., Peric, A., Moens, S., Nys, K., De Bock, K., Quaegebeur, A., Schoors, S., Georgiadou, M., Wouters, J., Vinckier, S., Vankelecom, H., Garmyn, M., Vion, A. C., Radtke, F., Boulanger, C., Gerhardt, H., Dejana, E., Dewerchin, M., Ghesquière, B., Annaert, W., Agostinis, P., and Carmeliet, P. (2014) Tumor vessel normalization by chloroquine independent of autophagy. Cancer Cell 26, 190-206.
14. Jain, R. K. (1988) Determinants of tumor blood flow: A review. Cancer Res. 48, 2641-2658.
15. Less, J. R., Skalak, T. C., Sevick, E. M., and Jain, R. K. (1991) Microvascular architecture in a mammary carcinoma: branching patterns and vessel dimensions. Cancer Res. 51, 265-273.
16. Baum, O., Vieregge, M., Koch, P., Gül, S., Hahn, S., Huber-Abel, F. A., Pries, A. R., and Hoppeler, H. (2013) Phenotype of capillaries in skeletal muscle of nNOS-knockout mice. Am. J. Physiol. Regul. Integr. Comp. Physiol. 304, R1175-R1182.
17. Colvin, J. S., White, A. C., Pratt, S. J., and Ornitz, D. M. (2001) Lung hypoplasia and neonatal death in Fgf9-null mice identify this gene as an essential regulator of lung mesenchyme. Development 128, 2095-2106.
18. Lavine, K. J., White, A. C., Park, C., Smith, C. S., Choi, K., Long, F., Hui, C. C., and Ornitz, D. M. (2006) Fibroblast growth factor signals regulate a wave of Hedgehog activation that is essential for coronary vascular development. Genes Dev. 20, 1651-1666.
19. Geske, M. J., Zhang, X., Patel, K. K., Ornitz, D. M., and Stappenbeck, T. S. (2008) Fgf9 signaling regulates small intestinal elongation and mesenchymal development. Development 135, 2959-2968.
20. Lin, Y., Chen, L., Lin, C., Luo, Y., Tsai, R. Y., and Wang, F. (2009) Neuron-derived FGF9 is essential for scaffold formation of Bergmann radial fibers and migration of granule neurons in the cerebellum. Dev. Biol. 329, 44 -54.
21. Frontini, M. J., Nong, Z., Gros, R., Drangova, M., O'Neil, C., Rahman, M. N., Akawi, O., Yin, H., Ellis, C. G., and Pickering, J. G. (2011) Fibroblast growth factor 9 delivery during angiogenesis produces durable, vasoresponsive microvessels wrapped by smooth muscle cells. Nat. Biotechnol. 29, 421-427.
22. Vafaie, F., Yin, H., O'Neil, C., Nong, Z., Watson, A., Arpino, J. M., Chu, M. W., Wayne Holdsworth, D., Gros, R., and Pickering, J. G. (2014) Collagenase- resistant collagen promotes mouse aging and vascular cell senescence. Aging Cell 13, 121-130.
23. Salup, R. R., Herberman, R. B., and Wiltrout, R. H. (1985) Role of natural killer activity in development of spontaneous metastases in murine renal cancer. J. Urol. 134, 1236-1241.
24. Fera, E., O'Neil, C., Lee, W., Li, S., and Pickering, J. G. (2004) Fibroblast growth factor-2 and remodeled type I collagen control membrane protrusion in human vascular smooth muscle cells: biphasic activation of Rac1. J. Biol. Chem. 279, 35573-35582.
25. Yin, H., van der Veer, E., Frontini, M. J., Thibert, V., O'Neil, C., Watson, A., Szasz, P., Chu, M. W., and Pickering, J. G. (2012) Intrinsic directionality of migrating vascular smooth muscle cells is regulated by NAD- biosynthesis. J. Cell Sci. 125, 5770-5780.
26. Small, T. W., Bolender, Z., Bueno, C., O'Neil, C., Nong, Z., Rushlow, W., Rajakumar, N., Kandel, C., Strong, J., Madrenas, J., and Pickering, J. G. (2006) Wilms' tumor 1-associating protein regulates the proliferation of vascular smooth muscle cells. Circ. Res. 99, 1338-1346.
27. Peña-Llopis, S., Vega-Rubín-de-Celis, S., Liao, A., Leng, N., Pavía-Jiménez, A., Wang, S., Yamasaki, T., Zhrebker, L., Sivanand, S., Spence, P., Kinch, L., Hambuch, T., Jain, S., Lotan, Y., Margulis, V., Sagalowsky, A. I., Summerour, P. B., Kabbani, W., Wong, S. W., Grishin, N., Laurent, M., Xie, X. J., Haudenschild, C. D., Ross, M. T., Bentley, D. R., Kapur, P., and Brugarolas, J. (2012) BAP1 loss defines a new class of renal cell carcinoma. Nat. Genet. 44, 751-759.
28. Sato, Y., Yoshizato, T., Shiraishi, Y., Maekawa, S., Okuno, Y., Kamura, T., Shimamura, T., Sato-Otsubo, A., Nagae, G., Suzuki, H., Nagata, Y., Yoshida, K., Kon, A., Suzuki, Y., Chiba, K., Tanaka, H., Niida, A., Fujimoto, A., Tsunoda, T., Morikawa, T., Maeda, D., Kume, H., Sugano, S., Fukayama, M., Aburatani, H., Sanada, M., Miyano, S., Homma, Y., and Ogawa, S. (2013) Integrated molecular analysis of clear-cell renal cell carcinoma. Nat. Genet. 45, 860-867.
29. Zhang, X., Ibrahimi, O. A., Olsen, S. K., Umemori, H., Mohammadi, M., and Ornitz, D. M. (2006) Receptor specificity of the fibroblast growth factor family: The complete mammalian FGF family. J. Biol. Chem. 281, 15694-15700.
30. White, A. C., Xu, J., Yin, Y., Smith, C., Schmid, G., and Ornitz, D. M. (2006) FGF9 and SHH signaling coordinate lung growth and development through regulation of distinct mesenchymal domains. Development 133, 1507-1517.
31. 2 gradients in solid tumors in vivo: high-resolution measurements reveal a lack of correlation. Nat. Med. 3, 177-182.
32. Gaengel, K., Genové, G., Armulik, A., and Betsholtz, C. (2009) Endothelial- mural cell signaling in vascular development and angiogenesis. Arterioscler. Thromb. Vasc. Biol. 29, 630-638.
33. Crisan, M., Yap, S., Casteilla, L., Chen, C. W., Corselli, M., Park, T. S., Andriolo, G., Sun, B., Zheng, B., Zhang, L., Norotte, C., Teng, P. N., Traas, J., Schugar, R., Deasy, B. M., Badylak, S., Buhring, H. J., Giacobino, J. P., Lazzari, L., Huard, J., and Péault, B. (2008) A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 3, 301-313.
34. Kim, K. J., Li, B., Winer, J., Armanini, M., Gillett, N., Phillips, H. S., and Ferrara, N. (1993) Inhibition of vascular endothelial growth factor-induced angiogenesis suppresses tumour growth in vivo. Nature 362, 841-844.
35. Yuan, F., Chen, Y., Dellian, M., Safabakhsh, N., Ferrara, N., and Jain, R. K. (1996) Time-dependent vascular regression and permeability changes in established human tumor xenografts induced by an anti-vascular endothelial growth factor/vascular permeability factor antibody. Proc. Natl. Acad. Sci. U.S.A. 93, 14765-14770.
36. Greenberg, J. I., Shields, D. J., Barillas, S. G., Acevedo, L. M., Murphy, E., Huang, J., Scheppke, L., Stockmann, C., Johnson, R. S., Angle, N., and Cheresh, D. A. (2008) A role for VEGF as a negative regulator of pericyte function and vessel maturation. Nature 456, 809-813.
37. Carmeliet, P., and Jain, R. K. (2011) Molecular mechanisms and clinical applications of angiogenesis. Nature 473, 298-307.
38. Emblem, K. E., Mouridsen, K., Bjornerud, A., Farrar, C. T., Jennings, D., Borra, R. J., Wen, P. Y., Ivy, P., Batchelor, T. T., Rosen, B. R., Jain, R. K., and Sorensen, A. G. (2013) Vessel architectural imaging identifies cancer patient responders to anti-angiogenic therapy. Nat. Med. 19, 1178 -1183.
39. Chauhan, V. P., Stylianopoulos, T., Martin, J. D., Popović, Z., Chen, O., Kamoun, W. S., Bawendi, M. G., Fukumura, D., and Jain, R. K. (2012) Normalization of tumour blood vessels improves the delivery of nanomedicines in a size-dependent manner. Nat. Nanotechnol. 7, 383-388.
40. Wang, Q., Kocaoglu, O. P., Cense, B., Bruestle, J., Jonnal, R. S., Gao, W., and Miller, D. T. (2011) Imaging retinal capillaries using ultrahigh-resolution optical coherence tomography and adaptive optics. Invest. Ophthalmol. Vis. Sci. 52, 6292-6299.
41. Segal, S. S. (2005) Regulation of blood flow in the microcirculation. Microcirculation 12, 33-45.
42. Clifford, P. S. (2011) Local control of blood flow. Adv. Physiol. Educ. 35, 5-15.
43. Andrae, J., Gallini, R., and Betsholtz, C. (2008) Role of platelet-derived growth factors in physiology and medicine. Genes Dev. 22, 1276-1312.
44. Wu, X., Jin, C., Wang, F., Yu, C., and McKeehan, W. L. (2003) Stromal cell heterogeneity in fibroblast growth factor-mediated stromal-epithelial cell cross-talk in premalignant prostate tumors. Cancer Res. 63, 4936-4944.
45. Jin, C., Wang, F., Wu, X., Yu, C., Luo, Y., and McKeehan, W. L. (2004) Directionally specific paracrine communication mediated by epithelial FGF9 to stromal FGFR3 in two-compartment premalignant prostate tumors. Cancer Res. 64, 4555-4562.
46. Agrawal, V., Maharjan, S., Kim, K., Kim, N. J., Son, J., Lee, K., Choi, H. J., Rho, S. S., Ahn, S., Won, M. H., Ha, S. J., Koh, G. Y., Kim, Y. M., Suh, Y. G., and Kwon, Y. G. (2014) Direct endothelial junction restoration results in significant tumor vascular normalization and metastasis inhibition in mice. Oncotarget 5, 2761-2777.
47. Xian, X., Håkansson, J., Ståhlberg, A., Lindblom, P., Betsholtz, C., Gerhardt, H., and Semb, H. (2006) Pericytes limit tumor cell metastasis. J. Clin. Invest. 116, 642-651.
48. Pickering, J. G., Ford, C. M., Tang, B., and Chow, L. H. (1997) Coordinated effects of fibroblast growth factor-2 on expression of fibrillar collagens, matrix metalloproteinases, and tissue inhibitors of matrix metalloproteinases by human vascular smooth muscle cells. Evidence for repressed collagen production and activated degradative capacity. Arterioscler. Thromb. Vasc. Biol. 17, 475-482.
49. Yin, Y., Betsuyaku, T., Garbow, J. R., Miao, J., Govindan, R., and Ornitz, D. M. (2013) Rapid induction of lung adenocarcinoma by fibroblast growth factor 9 signaling through FGF receptor 3. Cancer Res. 73, 5730-5741.