Myogenic Akt Signaling Regulates Blood Vessel Recruitment during Myofiber Growth

REFERENCES

• Alessi, D. R., M. Andjelkovic, B. Caudwell, P. Cron, N. Morrice, P. Cohen, and B. A. Hemmings. 1996. Mechanism of activation of protein kinase B by insulin and IGF-1. EMBO J. 15: 6541–6551.
   PubMed Web of Science ®Google Scholar
• Altomare, D. A., K. Guo, J. Q. Cheng, G. Sonoda, K. Walsh, and J. R. Testa. 1995. Cloning, chromosomal localization and expression analysis of the mouse Akt2 oncogene. Oncogene 11: 1055–1060.
   PubMed Web of Science ®Google Scholar
• Altomare, D. A., G. E. Lyons, Y. Mitsuuchi, J. Q. Cheng, and J. R. Testa. 1998. Akt2 mRNA is highly expressed in embryonic brown fat and AKT2 kinase is activated by insulin. Oncogene 16: 2407–2411.
   PubMedGoogle Scholar
• Barton-Davis, E. R., D. I. Shoturma, A. Musaro, N. Rosenthal, and H. L. Sweeney. 1998. Viral mediated expression of insulin-like growth factor I blocks the aging-related loss of skeletal muscle function. Proc. Natl. Acad. Sci. USA 95: 15603–15607.
   PubMed Web of Science ®Google Scholar
• Baumgartner, I., A. Pieczek, O. Manor, R. Blair, M. Kearney, K. Walsh, and J. M. Isner. 1998. Constitutive expression of phVEGF165 after intramuscular gene transfer promotes collateral vessel development in patients with critical limb ischemia. Circulation 97: 1114–1123.
   PubMed Web of Science ®Google Scholar
• Bodine, S. C., T. N. Stitt, M. Gonzalez, W. O. Kline, G. L. Stover, R. Bauerlein, E. Zlotchenko, A. Scrimgeour, J. C. Lawrence, D. J. Glass, and G. D. Yancopoulos. 2001. Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat. Cell Biol. 3: 1014–1019.
   PubMed Web of Science ®Google Scholar
• Carmeliet, P., V. Ferreira, G. Breier, S. Pollefeyt, L. Kieckens, M. Gertsenstein, M. Fahrig, A. Vandenhoeck, K. Harpal, C. Eberhardt, C. Declercq, J. Pawling, L. Moons, D. Collen, W. Risau, and A. Nagy. 1996. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 380: 435–439.
   PubMed Web of Science ®Google Scholar
• Carpenter, S., and G. Karpati. 1982. Necrosis of capillaries in denervation atrophy of human skeletal muscle. Muscle Nerve 5: 250–254.
   PubMedGoogle Scholar
• Chen, W. S., P. Z. Xu, K. Gottlob, M. L. Chen, K. Sokol, T. Shiyanova, I. Roninson, W. Weng, R. Suzuki, K. Tobe, T. Kadowaki, and N. Hay. 2001. Growth retardation and increased apoptosis in mice with homozygous disruption of the Akt1 gene. Genes Dev. 15: 2203–2208.
   PubMed Web of Science ®Google Scholar
• Chou, M. M., W. Hou, J. Johnson, L. K. Graham, M. H. Lee, C. S. Chen, A. C. Newton, B. S. Schaffhausen, and A. Toker. 1998. Regulation of protein kinase C zeta by PI 3-kinase and PDK-1. Curr. Biol. 8: 1069–1077.
   PubMed Web of Science ®Google Scholar
• Claffey, K. P., W. O. Wilkison, and B. M. Spiegelman. 1992. Vascular endothelial growth factor. Regulation by cell differentiation and activated second messenger pathways. J. Biol. Chem. 267: 16317–16322.
   PubMed Web of Science ®Google Scholar
• Dai, Y., E. M. Schwarz, D. Gu, W.-W. Zhang, N. Sarvetnick, and I. M. Verma. 1995. Cellular and humoral immune responses to adenoviral vectors containing factor IX gene: tolerization of factor IX and vector antigens allows for long-term expression. Proc. Natl. Acad. Sci. USA 92: 1401–1405.
   PubMed Web of Science ®Google Scholar
• Datta, S. R., A. Brunet, and M. E. Greenberg. 1999. Cellular survival: a play in three Akts. Genes Dev. 13: 2905–2927.
   PubMed Web of Science ®Google Scholar
• Degens, H., Z. Turek, L. J. C. Hoofd, M. A. Van't Hof, and R. A. Binkhorst. 1992. The relationship between capillarisation and fibre types during compensatory hypertrophy of the plantaris muscle in the rat. J. Anat. 180: 455–463.
   PubMedGoogle Scholar
• Degens, H., J. H. Veerkamp, H. T. B. van Moerkerk, Z. Turek, L. J. C. Hoofd, and R. A. Binkhorst. 1993. Metabolic capacity, fibre type area and capillarization of rat plantaris muscle. Effects of age, overload and training and relationship with fatigue resistance. Int. J. Biochem. 25: 1141–1148.
   PubMedGoogle Scholar
• Diaz, R., E. A. Paolasso, L. S. Piegas, C. D. Tajer, M. G. Moreno, R. Corvalan, J. E. Isea, G. Romero, et al. 1998. Metabolic modulation of acute myocardial infarction. Circulation 98: 2227–2234.
   PubMed Web of Science ®Google Scholar
• Doornbos, R. P., M. Theelen, P. C. van der Hoeven, W. J. van Blitterswijk, A. J. Verkleij, and P. M. van Bergen en Henegouwen. 1999. Protein kinase Czeta is a negative regulator of protein kinase B activity. J. Biol. Chem. 274: 8589–8596.
   PubMedGoogle Scholar
• Ferrara, N. 1999. Molecular and biological properties of vascular endothelial growth factor. J. Mol. Med. 77: 527–543.
   PubMed Web of Science ®Google Scholar
• Florini, J. R., K. A. Magri, D. Z. Ewton, P. L. James, K. Grindstaff, and P. S. Rotwein. 1991. “Spontaneous” differentiation of skeletal myoblasts is dependent upon autocrine secretion of insulin-like growth factor-II. J. Biol. Chem. 266: 15917–15923.
   PubMed Web of Science ®Google Scholar
• Franzini-Armstrong, C., and D. A. Fischman. 1994. Morphogenesis of skeletal muscle fibers, p. 74–96. In A. G. Engel and C. Franzini-Armstrong (ed.), Myology: basic and clinical, 2nd ed., vol. 1. McGraw-Hill Book Co., Inc., New York, N.Y.
   Google Scholar
• Fujio, Y., K. Guo, T. Mano, Y. Mitsuuchi, J. R. Testa, and K. Walsh. 1999. Cell cycle withdrawal promotes myogenic induction of Akt, a positive modulator of myocyte survival. Mol. Cell. Biol. 19: 5073–5082.
   PubMedGoogle Scholar
• Fujio, Y., Y. Mitsuuchi, J. R. Testa, and K. Walsh. 2001. Activation of Akt2 inhibits anoikis and apoptosis induced by myogenic differentiation. Cell Death Differ. 8: 1207–1212.
   PubMedGoogle Scholar
• Fujio, Y., T. Nguyen, D. Wencker, R. N. Kitsis, and K. Walsh. 2000. Akt promotes survival of cardiomyocytes in vitro and protects against ischemia-reperfusion injury in mouse heart. Circulation 101: 660–667.
   PubMed Web of Science ®Google Scholar
• Fujio, Y., and K. Walsh. 1999. Akt mediates cytoprotection of endothelial cells by vascular endothelial growth factor in an anchorage-dependent manner. J. Biol. Chem. 274: 16349–16354.
   PubMed Web of Science ®Google Scholar
• Gille, J., R. A. Swerlick, and S. W. Caughman. 1997. Transforming growth factor-alpha-induced transcriptional activation of the vascular permeability factor (VPF/VEGF) gene requires AP-2-dependent DNA binding and transactivation. EMBO J. 16: 750–759.
   PubMed Web of Science ®Google Scholar
• Han, V. K. M., A. J. D'Ercole, and P. K. Lund. 1987. Cellular localization of somatomedin (insulin-like growth factor) messenger RNA in the human fetus. Science 236: 193–197.
   PubMed Web of Science ®Google Scholar
• Hixon, M. L., C. Muro-Cacho, M. W. Wagner, C. Obejero-Paz, E. Millie, Y. Fujio, Y. Kureishi, T. Hassold, K. Walsh, and A. Gualberto. 2000. Akt1/PKB upregulation leads to vascular smooth muscle cell hypertrophy and polyploidization. J. Clin. Investig. 106: 1011–1020.
   PubMed Web of Science ®Google Scholar
• Hudlicka, O. 1990. The response of muscle to enhanced and reduced activity, p. 417–439. In J. B. Harris and D. M. Turnbull (ed.), Bailliere's clinical endocrinology and metabolism, vol. 4. Bailliere-Tindal, Toronto, Ontario, Canada.
   PubMedGoogle Scholar
• Ikeda, E., M. G. Achen, G. Breier, and W. Risau. 1995. Hypoxia-induced transcriptional activation and increased mRNA stability of vascular endothelial growth factor in C6 glioma cells. J. Biol. Chem. 270: 19761–19766.
   PubMed Web of Science ®Google Scholar
• Ingjer, F. 1979. Capillary supply and mitochondrial content of different skeletal muscle fiber types in untrained and endurance-trained men. A histochemical and ultrastructural study. Eur. J. Appl. Physiol. Occup. Physiol. 40: 197–209.
   PubMed Web of Science ®Google Scholar
• Isner, J. M., A. Pieczek, R. Schainfeld, R. Blair, L. haley, T. Asahara, K. Rosenfield, S. Razvi, K. Walsh, and J. F. Symes. 1996. Clinical evidence of angiogenesis after arterial gene transfer of phVEGF165 in patient with ischaemic limb. Lancet 348: 370–374.
   PubMed Web of Science ®Google Scholar
• Jerusalem, F. 1994. The microcirculation of muscle, p. 361–374. In A. G. Engel and C. Franzini-Armstrong (ed.), Myology: basic and clinical, 2nd ed., vol. 1. McGraw-Hill Book Co., Inc., New York, N.Y.
   Google Scholar
• Jiang, B. H., J. Z. Zheng, M. Aoki, and P. K. Vogt. 2000. Phosphatidylinositol 3-kinase signaling mediates angiogenesis and expression of vascular endothelial growth factor in endothelial cells. Proc. Natl. Acad. Sci. USA 97: 1749–1753.
   PubMed Web of Science ®Google Scholar
• Kano, Y., S. Shimegi, K. Masuda, H. Ohmori, and S. Katsuta. 1997. Morphological adaptation of capillary network in compensatory hypertrophied rat plantaris muscle. Eur. J. Appl. Physiol. Occup. Physiol. 75: 97–101.
   PubMedGoogle Scholar
• Laham, R. J., A. Mannam, M. J. Post, and F. Sellke. 2001. Gene transfer to induce angiogenesis in myocardial and limb ischaemia. Expert Opin. Biol. Ther. 1: 985–994.
   PubMed Web of Science ®Google Scholar
• Lawlor, M. A., and P. Rotwein. 2000. Coordinate control of muscle cell survival by distinct insulin-like growth factor activated signaling pathways. J. Cell Biol. 151: 1131–1140.
   PubMed Web of Science ®Google Scholar
• Lee, R. J., M. L. Springer, W. E. Blanco-Bose, R. Shaw, P. C. Ursell, and H. M. Blau. 2000. VEGF gene delivery to myocardium: deleterious effects of unregulated expression. Circulation 102: 898–901.
   PubMed Web of Science ®Google Scholar
• Le Good, J. A., W. H. Ziegler, D. B. Parekh, D. R. Alessi, P. Cohen, and P. J. Parker. 1998. Protein kinase C isotypes controlled by phosphoinositide 3-kinase through the protein kinase PDK1. Science 281: 2042–2045.
   PubMed Web of Science ®Google Scholar
• Mazure, N. M., E. Y. Chen, K. R. Laderoute, and A. J. Giaccia. 1997. Induction of vascular endothelial growth factor by hypoxia is modulated by a phosphatidylinositol 3-kinase/Akt signaling pathway in Ha-ras-transformed cells through a hypoxia inducible factor-1 transcriptional element. Blood 90: 3322–3331.
   PubMed Web of Science ®Google Scholar
• Miao, W., Z. Luo, R. N. Kitsis, and K. Walsh. 2000. Intracoronary, adenovirus-mediated Akt gene transfer in heart limits infarct size following ischemia-reperfusion injury in vivo. J. Mol. Cell. Cardiol. 32: 2397–2402.
   PubMed Web of Science ®Google Scholar
• Milanini, J., F. Vinals, J. Pouyssegur, and G. Pages. 1998. p42/p44 MAP kinase module plays a key role in the transcriptional regulation of the vascular endothelial growth factor gene in fibroblasts. J. Biol. Chem. 273: 18165–18172.
   PubMed Web of Science ®Google Scholar
• Mukhopadhyay, D., B. Knebelmann, H. T. Cohen, S. Ananth, and V. P. Sukhatme. 1997. The von Hippel-Lindau tumor suppressor gene product interacts with Sp1 to repress vascular endothelial growth factor promoter activity. Mol. Cell. Biol. 17: 5629–5639.
   PubMed Web of Science ®Google Scholar
• Musarò, A., K. J. A. McCullagh, F. J. Naya, E. N. Olson, and N. Rosenthal. 1999. IGF-1 induces skeletal myocyte hypertrophy through calcineurin in association with GATA-2 and NF-ATc1. Nature 400: 581–585.
   PubMed Web of Science ®Google Scholar
• Oosthuyse, B., L. Moons, E. Storkebaum, H. Beck, D. Nuyens, K. Brusselmans, J. Van Dorpe, P. Hellings, M. Gorselink, S. Heymans, G. Theilmeier, M. Dewerchin, V. Laudenbach, P. Vermylen, H. Raat, T. Acker, V. Vleminckx, L. Van den Bosch, N. Cashman, H. Fujisawa, M. R. Drost, R. Sciot, F. Bruyninckx, D. Hicklin, C. Ince, P. Gressens, F. Lupu, K. H. Plate, W. Robberecht, J. M. Herbert, D. Collen, and P. Carmeliet. 2001. Deletion of the hypoxia-response element in the vascular endothelial growth factor promoter causes motor neuron degeneration. Nat. Genet. 28: 131–138.
   PubMed Web of Science ®Google Scholar
• Pal, S., K. Datta, R. Khosravi-Far, and D. Mukhopadhyay. 2001. Role of protein kinase Czeta in Ras-mediated transcriptional activation of vascular permeability factor/vascular endothelial growth factor expression. J. Biol. Chem. 276: 2395–2403.
   PubMed Web of Science ®Google Scholar
• Pal, S., K. Datta, and D. Mukhopadhyay. 2001. Central role of p53 on regulation of vascular permeability factor/vascular endothelial growth factor (VPF/VEGF) expression in mammary carcinoma. Cancer Res. 61: 6952–6957.
   PubMed Web of Science ®Google Scholar
• Plyley, M. J., B. J. Olmstead, and E. G. Noble. 1998. Time course of changes in capillarization in hypertrophied rat plantaris muscle. J. Appl. Physiol. 84: 902–907.
   PubMedGoogle Scholar
• Proud, C. G., and R. M. Denton. 1997. Molecular mechanisms for the control of translation by insulin. Biochem. J. 328: 329–341.
   PubMedGoogle Scholar
• Pu, L. Q., A. D. Sniderman, Z. Arekat, A. M. Graham, R. Brassard, and J. F. Symes. 1993. Angiogenic growth factor and revascularization of the ischemic limb: evaluation in a rabbit model. J. Surg. Res. 54: 575–583.
   PubMed Web of Science ®Google Scholar
• Regensteiner, J. G., E. E. Wolfel, E. P. Brass, M. R. Carry, S. P. Ringel, M. E. Hargarten, E. R. Stamm, and W. R. Hiatt. 1993. Chronic changes in skeletal muscle histology and function in peripheral arterial disease. Circulation 87: 413–421.
   PubMed Web of Science ®Google Scholar
• Rommel, C., S. C. Bodine, B. A. Clarke, R. Rossman, L. Nunez, T. N. Stitt, G. D. Yancopoulos, and D. J. Glass. 2001. Mediation of IGF-1-induced skeletal myotube hypertrophy by PI(3)K/Akt/mTOR and PI(3)K/Akt/GSK3 pathways. Nat. Cell Biol. 3: 1009–1013.
   PubMed Web of Science ®Google Scholar
• Rommel, C., B. A. Clarke, S. Zimmermann, L. Nunez, R. Rossman, K. Reid, K. Moelling, G. D. Yancopoulos, and D. J. Glass. 1999. Differentiation stage-specific inhibition of the Raf-MEK-ERK pathway by Akt. Science 286: 1738–1741.
   PubMed Web of Science ®Google Scholar
• Rosen, K. M., B. M. Wentworth, N. Rosenthal, and L. Villa-Komaroff. 1993. Specific, temporally regulated expression of the insulin-like growth factor II gene during muscle cell differentiation. Endocrinology 133: 474–481.
   PubMedGoogle Scholar
• Ryuto, M., M. Ono, H. Izumi, S. Yoshida, H. A. Weich, K. Kohno, and M. Kuwano. 1996. Induction of vascular endothelial growth factor by tumor necrosis factor alpha in human glioma cells. Possible roles of SP-1. J. Biol. Chem. 271: 28220–28228.
   PubMed Web of Science ®Google Scholar
• Sakuta, T., K. Matsushita, N. Yamaguchi, T. Oyama, R. Motani, T. Koga, S. Nagaoka, K. Abeyama, I. Maruyama, H. Takada, and M. Torii. 2001. Enhanced production of vascular endothelial growth factor by human monocytic cells stimulated with endotoxin through transcription factor SP-1. J. Med. Microbiol. 50: 233–237.
   PubMedGoogle Scholar
• Schwarz, E. R., M. T. Speakman, M. Patterson, S. S. Hale, J. M. Isner, L. H. Kedes, and R. A. Kloner. 2000. Evaluation of the effects of intramyocardial injection of DNA expressing vascular endothelial growth factor (VEGF) in a myocardial infarction model in the rat—angiogenesis and angioma formation. J. Am. Coll. Cardiol. 35: 1323–1330.
   PubMed Web of Science ®Google Scholar
• Semenza, G. L. 2000. HIF-1 and human disease: one highly involved factor. Genes Dev. 14: 1983–1991.
   PubMed Web of Science ®Google Scholar
• Semsarian, C., M. J. Wu, Y. K. Ju, T. Marciniec, T. Yeoh, D. G. Allen, R. P. Harvey, and R. M. Graham. 1999. Skeletal muscle hypertrophy is mediated by a Ca2+-dependent calcineurin signalling pathway. Nature 400: 576–581.
   PubMed Web of Science ®Google Scholar
• Shah, O. J., J. C. Anthony, S. R. Kimball, and L. S. Jefferson. 2000. 4E-BP1 and S6K1: translational integration sites for nutritional and hormonal information in muscle. Am. J. Physiol. Endocrinol. Metab. 279: E715–E729.
   PubMed Web of Science ®Google Scholar
• Shi, Q., X. Le, J. L. Abbruzzese, Z. Peng, C. N. Qian, H. Tang, Q. Xiong, B. Wang, X. C. Li, and K. Xie. 2001. Constitutive Sp1 activity is essential for differential constitutive expression of vascular endothelial growth factor in human pancreatic adenocarcinoma. Cancer Res. 61: 4143–4154.
   PubMed Web of Science ®Google Scholar
• Shioi, T., P. M. Kang, P. S. Douglas, J. Hampe, C. M. Yballe, J. Lawitts, L. C. Cantley, and S. Izumo. 2000. The conserved phosphoinositide 3-kinase pathway determines heart size in mice. EMBO J. 19: 2537–2548.
   PubMed Web of Science ®Google Scholar
• Smith, R. C., D. Branellec, D. H. Gorski, K. Guo, H. Perlman, J.-F. Dedieu, C. Pastore, A. Mahfoudi, P. Denèfle, J. M. Isner, and K. Walsh. 1997. p21CIP1-mediated inhibition of cell proliferation by overexpression of the gax homeodomain gene. Genes Dev. 11: 1674–1689.
   PubMed Web of Science ®Google Scholar
• Springer, M. L., A. S. Chen, P. E. Kraft, M. Bednarski, and H. M. Blau. 1998. VEGF gene delivery to muscle: potential role for vasculogenesis in adults. Mol. Cell 2: 549–558.
   PubMed Web of Science ®Google Scholar
• Stein, I., A. Itin, P. Einat, R. Skaliter, Z. Grossman, and E. Keshet. 1998. Translation of vascular endothelial growth factor mRNA by internal ribosome entry: implications for translation under hypoxia. Mol. Cell. Biol. 18: 3112–3119.
   PubMed Web of Science ®Google Scholar
• Stoner, M., F. Wang, M. Wormke, T. Nguyen, I. Samudio, C. Vyhlidal, D. Marme, G. Finkenzeller, and S. Safe. 2000. Inhibition of vascular endothelial growth factor expression in HEC1A endometrial cancer cells through interactions of estrogen receptor alpha and Sp3 proteins. J. Biol. Chem. 275: 22769–22779.
   PubMedGoogle Scholar
• Tanaka, T., H. Kanai, K. Sekiguchi, Y. Aihara, T. Yokoyama, M. Arai, T. Kanda, R. Nagai, and M. Kurabayashi. 2000. Induction of VEGF gene transcription by IL-1 beta is mediated through stress-activated MAP kinases and Sp1 sites in cardiac myocytes. J. Mol. Cell. Cardiol. 32: 1955–1967.
   PubMedGoogle Scholar
• Toker, A., and A. C. Newton. 2000. Akt/Protein Kinase B is regulated by autophosphorylation at the hypothetical PDK-2 site. J. Biol. Chem. 275: 8271–8274.
   PubMed Web of Science ®Google Scholar
• Tollefsen, S. E., J. L. Sadow, and P. Rotwein. 1989. Coordinate expression of insulin-like growth factor II and its receptor during muscle differentiation. Proc. Natl. Acad. Sci. USA 86: 1543–1547.
   PubMedGoogle Scholar
• Ueki, K., R. Yamamoto-Honda, Y. Kaburagi, T. Yamauchi, K. Tobe, B. M. Burgering, P. J. Coffer, I. Komuro, Y. Akanuma, Y. Yazaki, and T. Kadowaki. 1998. Potential role of protein kinase B in insulin-induced glucose transport, glycogen synthesis, and protein synthesis. J. Biol. Chem. 273: 5315–5322.
   PubMed Web of Science ®Google Scholar
• Ushio-Fukai, M., R. W. Alexander, M. Akers, Q. Yin, Y. Fujio, K. Walsh, and K. K. Griendling. 1999. Reactive oxygen species mediate the activation of Akt/protein kinase B by angiotensin II in vascular smooth muscle cells. J. Biol. Chem. 274: 22699–22704.
   PubMed Web of Science ®Google Scholar
• Verdu, J., M. A. Buratovich, E. L. Wilder, and M. J. Birnbaum. 1999. Cell-autonomous regulation of cell and organ growth in Drosophila by Akt/PKB. Nat. Cell Biol. 1: 500–506.
   PubMed Web of Science ®Google Scholar
• Vincent, K. A., K. G. Shyu, Y. Luo, M. Magner, R. A. Tio, C. Jiang, M. A. Goldberg, G. Y. Akita, R. J. Gregory, and J. M. Isner. 2000. Angiogenesis is induced in a rabbit model of hindlimb ischemia by naked DNA encoding an H1F-1alpha/VP16 hybrid transcription factor. Circulation 102: 2255–2261.
   PubMed Web of Science ®Google Scholar
• Zundel, W., C. Schindler, D. Haas-Kogan, A. Koong, F. Kaper, E. Chen, A. R. Gottschalk, H. E. Ryan, R. S. Johnson, A. B. Jefferson, D. Stokoe, and A. J. Giaccia. 2000. Loss of PTEN facilitates HIF-1-mediated gene expression. Genes Dev. 14: 391–396.
   PubMed Web of Science ®Google Scholar