Murine double minute-2 expression is required for capillary maintenance and exercise-induced angiogenesis in skeletal muscle

FASEB Journal

Volumn 26, Issue 11, 2012, Pages 4530-4539

  Roudier, Emilie ^a,b   Forn, Paul ^c   Perry, Mary Ellen ^a   Birot, Olivier ^a,b,d  

^a YORK UNIVERSITY   (Canada)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

^c NATIONAL CANCER INSTITUTE   (United States)

^d York University   (Canada)

Author keywords

Endothelial cell; P53; Physiology; VEGF A

Indexed keywords

COLLAGEN; PROTEIN MDM2; PROTEIN P53; VASCULOTROPIN A;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CAPILLARIZATION; CAPILLARY; CONTROLLED STUDY; ENDOTHELIUM CELL; EXERCISE; FEMALE; GEL; MOUSE; MUSCLE BIOPSY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RUNNING; SKELETAL MUSCLE; VASCULARIZATION;

ANIMALS; CAPILLARIES; FEMALE; GENE EXPRESSION REGULATION; MALE; MICE; MUSCLE, SKELETAL; NEOVASCULARIZATION, PHYSIOLOGIC; OBESITY; PHYSICAL CONDITIONING, ANIMAL; PROTO-ONCOGENE PROTEINS C-MDM2; RATS; RATS, SPRAGUE-DAWLEY; RATS, ZUCKER; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

ANIMALIA; MURINAE; MUS; RATTUS;

EID: 84868268447     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.12-212720     Document Type: Article

References (54)

1. Hudlicka, O., Brown, M., and Egginton, S. (1992) Angiogenesis in skeletal and cardiac muscle. Physiol. Rev. 72, 369-417
2. Bloor, C. M. (2005) Angiogenesis during exercise and training. Angiogenesis 8, 263-271
3. Egginton, S. (2009) Invited review: activity-induced angiogenesis. Pflügers Arch. 457, 963-977
4. Carmeliet, P., and Jain, R. K. (2011) Molecular mechanisms and clinical implications of angiogenesis. Nature 473, 298-307
5. Hiatt, W. R., Regensteiner, J. G., Hargarten, M. E., Wolfel, E. E., and Brass, E. P. (1990) Benefit of exercise conditioning for patients with peripheral arterial disease. Circulation 81, 602-609
6. Gustafsson, T., and Kraus, W. E. (2001) Exercise-induced angiogenesis-related growth and transcription factors in skeletal muscle, and their modification in muscle pathology. Front. Biosci. 6, 75-89
7. Yang, H. T., Prior, B. M., Lloyd, P. G., Taylor, J. C., Li, Z., Laughlin, M. H., and Terjung, R. L. (2008) Training-induced vascular adaptations to ischemic muscle. J. Physiol. Pharmacol. 59, 57-70
8. Lee, S., Chen, T. T., Barber, C. L., Jordan, M. C., Murdock, J., Desai, S., Ferrara, N., Nagy, A., Roos, K. P., and Iruela-Arispe, M. L. (2007) Autocrine VEGF signaling is required for vascular homeostasis. Cell 130, 691-703
9. Shangary, S., and Wang, S. (2008) Targeting the MDM2-p53 interaction for cancer therapy. Clin. Cancer Res. 14, 5318-5324
10. Bouvet, M., Ellis, L. M., Nishizaki, M., Fujiwara, T., Liu, W., Bucana, C. D., Fang, B., Lee, J. J., and Roth, J. A. (1998) Adenovirus-mediated wild-type p53 gene transfer down-regulates vascular endothelial growth factor expression and inhibits angiogenesis in human colon cancer. Cancer Res. 58, 2288-2292
11. Zhang, L., Yu, D., Hu, M., Xiong, S., Lang, A., Ellis, L. M., and Pollock, R. E. (2000) Wild-type p53 suppresses angiogenesis in human leiomyosarcoma and synovial sarcoma by transcriptional suppression of vascular endothelial growth factor expression. Cancer Res. 60, 3655-3661
12. Qin, G., Kishore, R., Dolan, C. M., Silver, M., Wecker, A., Luedemann, C. N., Thorne, T., Hanley, A., Curry, C., Heyd, L., Dinesh, D., Kearney, M., Martelli, F., Murayama, T., Goukassian, D. A., Zhu, Y., and Losordo, D. W. (2006) Cell cycle regulator E2F1 modulates angiogenesis via p53-dependent transcriptional control of VEGF. Proc. Natl. Acad. Sci. U. S. A. 103, 11015-11020
13. Yoshioka, Y., Shimizu, S., Ito, T., Taniguchi, M., Nomura, M., Nishida, T., and Sawa, Y. (2012) p53 inhibits vascular endothelial growth factor expression in solid tumor. J. Surg. Res. 174, 291-297
14. Prives, C. (1998) Signaling to p53: breaking the Mdm2-p53 circuit. Cell 95, 5-8
15. Manfredi, J. J. (2010) The Mdm2-p53 relationship evolves: Mdm2 swings both ways as an oncogene and a tumor suppressor. Genes Dev. 24, 1580-1589
16. Jones, S. N., Hancock, A. R., Vogel, H., Donehower, L. A., and Bradley, A. (1998) Overexpression of Mdm2 in mice reveals a p53-independent role for Mdm2 in tumorigenesis. Proc. Natl. Acad. Sci. U. S. A. 95, 15608-15612
17. Skinner, H. D., Zheng, J. Z., Fang, J., Agani, F., and Jiang, B. H. (2004) Vascular endothelial growth factor transcriptional activation is mediated by hypoxia-inducible factor 1-, HDM2, and p70S6K1 in response to phosphatidylinositol 3-kinase/AKT signaling. J. Biol. Chem. 279, 45643-45651
18. Carroll, V. A., and Ashcroft, M. (2008) Regulation of angiogenic factors by HDM2 in renal cell carcinoma. Cancer Res. 68, 545-552
19. Bardos, J. I., Chau, N. M., and Ashcroft, M. (2004) Growth factor-mediated induction of HDM2 positively regulates hypoxia-inducible factor 1-expression. Mol. Cell. Biol. 24, 2905-2914
20. Nieminen, A. L., Qanungo, S., Schneider, E. A., Jiang, B. H., and Agani, F. H. (2005) Mdm2 and HIF-1-interaction in tumor cells during hypoxia. J. Cell. Physiol. 204, 364-369
21. LaRusch, G. A., Jackson, M. W., Dunbar, J. D., Warren, R. S., Donner, D. B., and Mayo, L. D. (2007) Nutlin-3 blocks vascular endothelial growth factor induction by preventing the interaction between hypoxia inducible factor 1-And Hdm2. Cancer Res. 67, 450-454
22. Lee, Y. M., Lim, J. H., Chun, Y. S., Moon, H. E., Lee, M. K., Huang, L. E., and Park, J. W. (2009) Nutlin-3, an Hdm2 antagonist, inhibits tumor adaptation to hypoxia by stimulating the FIH-mediated inactivation of HIF-1+. Carcinogenesis 30, 1768-1775
23. Park, J. H., Lee, J. Y., Shin, D. H., Jang, K. S., Kim, H. J., and Kong, G. (2011) Loss of Mel-18 induces tumor angiogenesis through enhancing the activity and expression of HIF-1-mediated by the PTEN/PI3K/Akt pathway. Oncogene 30, 4578-4589
24. Secchiero, P., Corallini, F., Gonelli, A., Dell'Eva, R., Vitale, M., Capitani, S., Albini, A., and Zauli, G. (2007) Antiangiogenic activity of the MDM2 antagonist nutlin-3. Circ. Res. 100, 61-69
25. Vassilev, L. T. (2007) MDM2 inhibitors for cancer therapy. Trends Mol. Med. 13, 23-31
26. Millard, M., Pathania, D., Grande, F., Xu, S., and Neamati, N. (2011) Small-molecule inhibitors of p53-MDM2 interaction: the 2006-2010 update. Curr. Pharm. Des. 17, 536-559
27. Mendrysa, S. M., McElwee, M. K., Michalowski, J., O'Leary, K. A., Young, K. M., and Perry, M. E. (2003) Mdm2 is critical for inhibition of p53 during lymphopoiesis and the response to ionizing radiation. Mol. Cell. Biol. 23, 462-473
28. Birot, O., Koulmann, N., Peinnequin, A., and Bigard, X. A. (2003) Exercise-induced expression of vascular endothelial growth factor mRNA in rat skeletal muscle is dependent on fibre type. J. Physiol. 552, 213-221
29. Roudier, E., Chapados, N., Decary, S., Gineste, C., Le Bel, C., Lavoie, J. M., Bergeron, R., and Birot, O. (2009) Angiomotin p80/p130 ratio: a new indicator of exercise-induced angiogenic activity in skeletal muscles from obese and non-obese rats? J. Physiol. 587, 4105-4119
30. Roudier, E., Gineste, C., Wazna, A., Dehghan, K., Desplanches, D., and Birot, O. (2010) Angio-Adaptation in unloaded skeletal muscle: new insights into an early and muscle type-specific dynamic process. J. Physiol. 588, 4579-4591
31. Milkiewicz, M., Roudier, E., Doyle, J. L., Trifonova, A., Birot, O., and Haas, T. L. (2011) Identification of a mechanism underlying regulation of the anti-Angiogenic forkhead transcription factor FoxO1 in cultured endothelial cells and ischemic muscle. Am. J. Pathol. 178, 935-944
32. Chen, J., Marechal, V., and Levine, A. J. (1993) Mapping of the p53 and mdm-2 interaction domains. Mol. Cell. Biol. 13, 4107-4114
33. Uguccioni, G., and Hood, D. A. (2011) The importance of PGC-1-in contractile activity-induced mitochondrial adaptations. Am. J. Physiol. Endocrinol. Metab. 300, 361-371
34. Teodoro, J. G., Evans, S. K., and Green, M. R. (2007) Inhibition of tumor angiogenesis by p53: a new role for the guardian of the genome. J. Mol. Med. 85, 1175-1186
35. Assadian, S., and Teodoro, J. G. (2008) Regulation of collagenderived antiangiogenic factors by p53. Expert Opin. Biol. Ther. 8, 941-950
36. Malek, M. H., and Olfert, I. M. (2009) Global deletion of thrombospondin-1 increases cardiac and skeletal muscle capillarity and exercise capacity in mice. Exp. Physiol. 94, 749-760
37. Dameron, K. M., Volpert, O. V., Tainsky, M. A., and Bouck, N. (1994) Control of angiogenesis in fibroblasts by p53 regulation of thrombospondin-1. Science 265, 1582-1584
38. Su, F., Pascal, L. E., Xiao, W., and Wang, Z. (2010) Tumor suppressor U19/EAF2 regulates thrombospondin-1 expression via p53. Oncogene 29, 421-431
39. Park, J. Y., Wang, P. Y., Matsumoto, T., Sung, H. J., Ma, W., Choi, J. W., Anderson, S. A., Leary, S. C., Balaban, R. S., Kang, J. G., and Hwang, P. M. (2009) p53 improves aerobic exercise capacity and augments skeletal muscle mitochondrial DNA content. Circ. Res. 105, 705-712
40. Olfert, I. M., Howlett, R. A., Tang, K., Dalton, N. D., Gu, Y., Peterson, K. L., Wagner, P. D., and Breen, E. C. (2009) Muscle-specific VEGF deficiency greatly reduces exercise endurance in mice. J. Physiol. 587, 1755-1767
41. Olfert, I. M., Howlett, R. A., Wagner, P. D., and Breen, E. C. (2010) Myocyte vascular endothelial growth factor is required for exercise-induced skeletal muscle angiogenesis. Am. J. Physiol. 299, 1059-1067
42. Perry, M. E. (2010) The regulation of the p53-mediated stress response by Mdm2 and Mdm4. Cold Spring Harb. Perspect. Biol. 2, a000968
43. Alam, H., Weck, J., Maizels, E., Park, Y., Lee, E. J., Ashcroft, M., and Hunzicker-Dunn, M. (2009) Role of the phosphatidylinositol-3-kinase and extracellular regulated kinase pathways in the induction of hypoxia-inducible factor (HIF)-1 activity and the HIF-1 target vascular endothelial growth factor in ovarian granulosa cells in response to follicle-stimulating hormone. Endocrinology 150, 915-928
44. Paik, J. H., Kollipara, R., Chu, G., Ji, H., Xiao, Y., Ding, Z., Miao, L., Tothova, Z., Horner, J. W., Carrasco, D. R., Jiang, S., Gilliland, D. G., Chin, L., Wong, W. H., Castrillon, D. H., and DePinho, R. A. (2007) FoxOs are lineage-restricted redundant tumor suppressors and regulate endothelial cell homeostasis. Cell 128, 309-323
45. Ganguli, G., and Wasylyk, B. (2003) p53-independent functions of MDM2. Mol. Cancer Res. 1, 1027-1035
46. Marine, J. C., and Lozano, G. (2010) Mdm2-mediated ubiquitylation: p53 and beyond. Cell Death Differ. 17, 93-102
47. Ravi, R., Mookerjee, B., Bhujwalla, Z. M., Sutter, C. H., Artemov, D., Zeng, Q., Dillehay, L. E., Madan, A., Semenza, G. L., and Bedi, A. (2000) Regulation of tumor angiogenesis by p53-induced degradation of hypoxia-inducible factor 1-. Genes Dev. 14, 34-44
48. Zhou, S., Gu, L., He, J., Zhang, H., and Zhou, M. (2011) MDM2 regulates vascular endothelial growth factor mRNA stabilization in hypoxia. Mol. Cell. Biol. 31, 4928-4937
49. Zhang, X., Kazerounian, S., Duquette, M., Perruzzi, C., Nagy, J. A., Dvorak, H., and Lawler, J. (2009) Thrombospondin-1 modulates vascular endothelial growth factor activity at the receptor level. FASEB J. 23, 3368-3376
50. Fu, W., Ma, Q., Chen, L., Li, P., Zhang, M., Ramamoorthy, S., Nawaz, Z., Shimojima, T., Wang, H., Yang, Y., Shen, Z., Zhang, Y., Zhang, X., Nicosia, S. V., Zhang, Y., Pledger, J. W., Chen, J., and Bai, W. (2009) MDM2 acts downstream of p53 as an E3 ligase to promote FOXO ubiquitination and degradation. J. Biol. Chem. 284, 13987-14000
51. Hohberg, M., Knockel, J., Hoffmann, C. J., Chlench, S., Wunderlich, W., Alter, A., Maroski, J., Vorderwulbecke, B. J., Da Silva-Azevedo, L., Knudsen, R., Lehmann, R., Fiedorowicz, K., Bongrazio, M., Nitsche, B., Hoepfner, M., Styp-Rekowska, B., Pries, A. R., and Zakrzewicz, A. (2011) Expression of ADAMTS1 in endothelial cells is induced by shear stress and suppressed in sprouting capillaries. J. Cell. Physiol. 226, 350-361
52. Lee, N. V., Sato, M., Annis, D. S., Loo, J. A., Wu, L., Mosher, D. F., and Iruela-Arispe, M. L. (2006) ADAMTS1 mediates the release of anti-Angiogenic polypeptides from TSP-1 and 2. EMBO J. 25, 5270-5283
53. Wang, Z., and Li, B. (2010) Mdm2 links genotoxic stress and metabolism to p53. Protein Cell 1, 1063-1072
54. Feng, J., Tamaskovic, R., Yang, Z., Brazil, D. P., Merlo, A., Hess, D., and Hemmings, B. A. (2004) Stabilization of Mdm2 via decreased ubiquitination is mediated by protein kinase B/Aktdependent phosphorylation. J. Biol. Chem. 279, 35510-35517