O 2 regulates skeletal muscle progenitor differentiation through phosphatidylinositol 3-kinase/AKT signaling

Molecular and Cellular Biology

Volumn 32, Issue 1, 2012, Pages 36-49

  Majmundar, Amar J ^a,b   Skuli, Nicolas ^a,b   Mesquita, Rickson C ^c   Kim, Meeri N ^c   Yodh, Arjun G ^c   Nguyen Mccarty, Michelle ^a,b   Celeste Simon, M ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; OXYGEN; PHOSPHATIDYLINOSITOL 3 KINASE;

ANIMAL CELL; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CONTROLLED STUDY; ENZYME ACTIVITY; HYPOXIA; IN VITRO STUDY; IN VIVO STUDY; ISCHEMIA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; STEM CELL; TISSUE REPAIR;

ANIMALS; CELL DIFFERENTIATION; CELL HYPOXIA; CELL LINE; CELLS, CULTURED; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MICE; MICE, INBRED C57BL; MYOBLASTS; OXYGEN; PHOSPHATIDYLINOSITOL 3-KINASE; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES;

EID: 84863011381     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.05857-11     Document Type: Article

References (64)

1. Alvarez-Tejado M, et al. 2001. Hypoxia induces the activation of the phosphatidylinositol 3-kinase/Akt cell survival pathway in PC12 cells. J. Biol. Chem. 276:22368-22374.
2. Amé J-C, Spenlehauer C, de Murcia G. 2004. The PARP superfamily. Bioessays 26:882-893.
3. Arsham AM, Howell JJ, Simon MC. 2003. A novel hypoxia-inducible factor-independent hypoxic response regulating mammalian target of rapamycin and its targets. J. Biol. Chem. 278:29655-29660.
4. Beckman JA, Creager MA, Libby P. 2002. Diabetes and atherosclerosis. JAMA 287:2570-2581.
5. Bertout JA, et al. 2009. Heterozygosity for hypoxia inducible factor 1α decreases the incidence of thymic lymphomas in a p53 mutant mouse model. Cancer Res. 69:3213-3220.
6. Bobrovnikova-Marjon E, et al. 2008. PERK-dependent regulation of lipogenesis during mouse mammary gland development and adipocyte differentiation. Proc. Natl. Acad. Sci. U. S. A. 105:16314-16319.
7. Borselli C, et al. 2010. Functional muscle regeneration with combined delivery of angiogenesis and myogenesis factors. Proc. Natl. Acad. Sci. U. S. A. 107:3287-3292.
8. Bosch-Marce M, et al. 2007. Effects of aging and hypoxia-inducible factor-1 activity on angiogenic cell mobilization and recovery of perfusion after limb ischemia. Circ. Res. 101:1310-1318.
9. Buas MF, Kabak S, Kadesch T. 2010. The Notch effector Hey1 associates with myogenic target genes to repress myogenesis. J. Biol. Chem. 285:1249-1258.
10. Bushby K, et al. 2010. Diagnosis and management of Duchenne muscular dystrophy, part 1: diagnosis, and pharmacological and psychosocial management. Lancet Neurol. 9:77-93.
11. Cantley LC. 2002. The phosphoinositide 3-kinase pathway. Science 296:1655-1657.
12. Chen C-H, et al. 2011. ER stress inhibits mTORC2 and Akt signaling through GSK-3β-mediated phosphorylation of Rictor. Sci. Signal. 4:ra10.
13. Conejo R, Valverde AM, Benito M, Lorenzo M. 2001. Insulin produces myogenesis in C2C12 myoblasts by induction of NF-κB and downregulation of AP-1 activities. J. Cell. Physiol. 186:82-94.
14. Coolican SA, Samuel DS, Ewton DZ, McWade FJ, Florini JR. 1997. The mitogenic and myogenic actions of insulin-like growth factors utilize distinct signaling pathways. J. Biol. Chem. 272:6653-6662.
15. Di Carlo A, et al. 2004. Hypoxia inhibits myogenic differentiation through accelerated MyoD degradation. J. Biol. Chem. 279:16332-16338.
16. Doetzlhofer A, et al. 2009. Hey2 regulation by FGF provides a Notchindependent mechanism for maintaining pillar cell fate in the organ of Corti. Dev. Cell 16:58-69.
17. Erbay E, Park I-H, Nuzzi PD, Schoenherr CJ, Chen J. 2003. IGF-II transcription in skeletal myogenesis is controlled bymTORand nutrients. J. Cell Biol. 163:931-936.
18. Florina J, Ewton D, Coolican S. 1996. Growth hormone and the insulinlike growth factor system in myogenesis. Endocrine Rev. 17:481-517.
19. Fu J, Taubman MB. 2010. Prolyl hydroxylase EGLN3 regulates skeletal myoblast differentiation through an NF-κB-dependent pathway. J. Biol. Chem. 285:8927-8935.
20. Fulco M, et al. 2008. Glucose restriction inhibits skeletal myoblast differentiation by activating SIRT1 through AMPK-mediated regulation of Nampt. Dev. Cell 14:661-673.
21. Gan X, Wang J, Su B, Wu D. 2011. Evidence for direct activation of mTORC2 kinase activity by phosphatidylinositol 3,4,5-triphosphate. J. Biol. Chem. 286:10998-11002.
22. Glass D, Roubenoff R. 2010. Recent advances in the biology and therapy of muscle wasting. Ann. N. Y. Acad. Sci. 1211:25-36.
23. Gordan JD, Bertout JA, Hu C-J, Diehl JA, Simon MC. 2007. HIF-2α promotes hypoxic cell proliferation by enhancing c-Myc transcriptional activity. Cancer Cell 11:335-347.
24. Greco S, et al. 2009. Common micro-RNA signature in skeletal muscle damage and regeneration induced by Duchenne muscular dystrophy and acute ischemia. FASEB J. 23:3335-3346.
25. Gustafsson MV, et al. 2005. Hypoxia requires Notch signaling to maintain the undifferentiated cell state. Dev. Cell 9:617-628.
26. Hiatt WR. 2001. Medical treatment of peripheral arterial disease and claudication. N. Engl. J. Med. 344:1608-1621.
27. Iso T, Kedes L, Hamamori Y. 2003. HES and HERP families: multiple effectors of the notch signaling pathway. J. Cell. Physiol. 194:237-255.
28. Jiang B-H, Aoki M, Zheng JZ, Li J, Vogt PK. 1999. Myogenic signaling of phosphatidylinositol 3-kinase requires the serine-threonine kinase Akt/protein kinase B. Proc. Natl. Acad. Sci. U. S. A. 96:2077-2081.
29. Jiang B-H, Zheng JZ, Vogt PK. 1998. An essential role of phosphatidylinositol 3-kinase in myogenic differentiation. Proc. Natl. Acad. Sci. U. S. A. 95:14179-14183.
30. Jorissen E, De Strooper B. 2010. γ-Secretase and the intramembrane proteolysis of Notch, p. 201-230. InR Kopan (ed.), Notch signaling. Academic Press, San Diego, CA.
31. Kolch W. 2005. Coordinating ERK/MAPK signalling through scaffolds and inhibitors. Nat. Rev. Mol. Cell Biol. 6:827-837.
32. Kuang S, Gillespie MA, Rudnicki MA. 2008. Niche regulation of muscle satellite cell self-renewal and differentiation. Cell Stem Cell 2:22-31.
33. Lau JF, Weinberg MD, Olin JW. 2011. Peripheral artery disease. Part 1: clinical evaluation and noninvasive diagnosis. Nat. Rev. Cardiol. 8:429-441.
34. Le Grand F, Rudnicki MA. 2007. Skeletal muscle satellite cells and adult myogenesis. Curr. Opin. Cell Biol. 19:628-633.
35. Lindsell CE, Shawber CJ, Boulter J, Weinmaster G. 1995. Jagged: a mammalian ligand that activates Notch1. Cell 80:909-917.
36. Liu J-P, Baker J, Perkins AS, Robertson EJ, Efstratiadis A. 1993. Mice carrying null mutations of the genes encoding insulin-like growth factor I (Igf-1) and type 1 IGF receptor (Igf1r). Cell 75:59-72.
37. Majmundar AJ, Wong WJ, Simon MC. 2010. Hypoxia-inducible factors and the response to hypoxic stress. Mol. Cell 40:294-309.
38. Manning BD, Cantley LC. 2007. AKT/PKB signaling: navigating downstream. Cell 129:1261-1274.
39. Mansfield KD, et al. 2005. Mitochondrial dysfunction resulting from loss of cytochrome c impairs cellular oxygen sensing and hypoxic HIF-α activation. Cell. Metab. 1:393-399.
40. Mesquita RC, et al. 2010. Hemodynamic and metabolic diffuse optical monitoring in a mouse model of hindlimb ischemia. Biomed. Opt. Express 1:1173-1187.
41. Milasincic D, Calera M, Farmer S, Pilch P. 1996. Stimulation of C2C12 myoblast growth by basic fibroblast growth factor and insulin-like growth factor 1 can occur via mitogen-activated protein kinase-dependent and -independent pathways. Mol. Cell. Biol. 16:5964-5973.
42. Özcan U, et al. 2004. Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science 306:457-461.
43. Ozcan U, et al. 2008. Loss of the tuberous sclerosis complex tumor suppressors triggers the unfolded protein response to regulate insulin signaling and apoptosis. Mol. Cell 29:541-551.
44. Pallafacchina G, Calabria E, Serrano AL, Kalhovde JM, Schiaffino S. 2002. A protein kinase B-dependent and rapamycin-sensitive pathway controls skeletal muscle growth but not fiber type specification. Proc. Natl. Acad. Sci. U. S. A. 99:9213-9218.
45. Paoni NF, et al. 2002. Time course of skeletal muscle repair and gene expression following acute hind limb ischemia in mice. Physiol. Genomics 11:263-272.
46. Pearce LR, Komander D, Alessi DR. 2010. The nuts and bolts of AGC protein kinases. Nat. Rev. Mol. Cell Biol. 11:9-22.
47. Peng XD, et al. 2003. Dwarfism, impaired skin development, skeletal muscle atrophy, delayed bone development, and impeded adipogenesis in mice lacking Akt1 and Akt2. Genes Dev. 17:1352-1365.
48. Philippou A, Halapas A, Maridaki M, Koutsilieris M. 2007. Type I insulin-like growth factor receptor signaling in skeletal muscle regeneration and hypertrophy. J. Musculoskel. Neuron Interact. 7:208-218.
49. Provot S, et al. 2007. Hif-1α regulates differentiation of limb bud mesenchyme and joint development. J. Cell Biol. 177:451-464.
50. Relaix F, Rocancourt D, Mansouri A, Buckingham M. 2005. A Pax3/Pax7-dependent population of skeletal muscle progenitor cells. Nature 435:948-953.
51. Ren H, Accili D, Duan C. 2010. Hypoxia converts the myogenic action of insulin-like growth factors into mitogenic action by differentially regulating multiple signaling pathways. Proc. Natl. Acad. Sci. U. S. A. 107:5857-5862.
52. Sarbassov DD, et al. 2006. Prolonged rapamycin treatment inhibits mTORC2 assembly and Akt/PKB. Mol. Cell 22:159-168.
53. Sengupta S, Peterson TR, Sabatini DM. 2010. Regulation of the mTOR complex 1 pathway by nutrients, growth factors, and stress. Mol. Cell 40:310-322.
54. Shu L, Houghton PJ. 2009. The mTORC2 complex regulates terminal differentiation of C2C12 myoblasts. Mol. Cell. Biol. 29:4691-4700.
55. Simon MC, Keith B. 2008. The role of oxygen availability in embryonic development and stem cell function. Nat. Rev. Mol. Cell Biol. 9:285-296.
56. Springer ML, Rando TA, Blau HM. 2001. Gene delivery to muscle. John Wiley & Sons, Inc., Hoboken, NJ.
57. Tedesco FS, Dellavalle A, Diaz-Manera J, Messina G, Cossu G. 2010. Repairing skeletal muscle: regenerative potential of skeletal muscle stem cells. J. Clin. Invest. 120:11-19.
58. Thoreen CC, et al. 2009. An ATP-competitive mammalian target of rapamycin inhibitor reveals rapamycin-resistant functions of mTORC1. J. Biol. Chem. 284:8023-8032.
59. Tureckova J, Wilson EM, Cappalonga JL, Rotwein P. 2001. Insulin-like growth factor-mediated muscle differentiation. J. Biol. Chem. 276:39264-39270.
60. Wilson EM, Hsieh MM, Rotwein P. 2003. Autocrine growth factor signaling by insulin-like growth factor-II mediates MyoD-stimulated myocyte maturation. J. Biol. Chem. 278:41109-41113.
61. Wilson EM, Rotwein P. 2006. Control of MyoD function during initiation of muscle differentiation by an autocrine signaling pathway activated by insulin-like growth factor-II. J. Biol. Chem. 281:29962-29971.
62. Wilson EM, Rotwein P. 2007. Selective control of skeletal muscle differentiation by Akt1. J. Biol. Chem. 282:5106-5110.
63. Wouters BG, Koritzinsky M. 2008. Hypoxia signalling through mTOR and the unfolded protein response in cancer. Nat. Rev. Cancer 8:851-864.
64. Yun Z, Lin Q, Giaccia AJ. 2005. Adaptive myogenesis under hypoxia. Mol. Cell. Biol. 25:3040-3055.