Role of Phosphoinositide 3-OH Kinase p110β in Skeletal Myogenesis

REFERENCES

• Karalaki M, Fili S, Philippou A, Koutsilieris M. 2009. Muscle regeneration: cellular and molecular events. In Vivo 23:779–796.
   PubMed Web of Science ®Google Scholar
• Kuang S, Rudnicki MA. 2008. The emerging biology of satellite cells and their therapeutic potential. Trends Mol Med 14:82–91. http://dx.doi.org/10.1016/j.molmed.2007.12.004.
   PubMed Web of Science ®Google Scholar
• Schultz E, Gibson MC, Champion T. 1978. Satellite cells are mitotically quiescent in mature mouse muscle: an EM and radioautographic study. J Exp Zool 206:451–456. http://dx.doi.org/10.1002/jez.1402060314.
   PubMedGoogle Scholar
• Mauro A. 1961. Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 9:493–495. http://dx.doi.org/10.1083/jcb.9.2.493.
   PubMed Web of Science ®Google Scholar
• Andres V, Walsh K. 1996. Myogenin expression, cell cycle withdrawal, and phenotypic differentiation are temporally separable events that precede cell fusion upon myogenesis. J Cell Biol 132:657–666. http://dx.doi.org/10.1083/jcb.132.4.657.
   PubMedGoogle Scholar
• Tamir Y, Bengal E. 2000. Phosphoinositide 3-kinase induces the transcriptional activity of MEF2 proteins during muscle differentiation. J Biol Chem 275:34424–34432. http://dx.doi.org/10.1074/jbc.M005815200.
   PubMedGoogle Scholar
• Yoshida N, Yoshida S, Koishi K, Masuda K, Nabeshima Y. 1998. Cell heterogeneity upon myogenic differentiation: down-regulation of MyoD and Myf-5 generates ‘reserve cells.’ J Cell Sci 111(Pt 6):769–779.
   PubMedGoogle Scholar
• Charge SB, Rudnicki MA. 2004. Cellular and molecular regulation of muscle regeneration. Physiol Rev 84:209–238. http://dx.doi.org/10.1152/physrev.00019.2003.
   PubMed Web of Science ®Google Scholar
• Walsh K, Perlman H. 1997. Cell cycle exit upon myogenic differentiation. Curr Opin Genet Dev 7:597–602. http://dx.doi.org/10.1016/S0959-437X(97)80005-6.
   PubMed Web of Science ®Google Scholar
• Shi X, Garry DJ. 2006. Muscle stem cells in development, regeneration, and disease. Genes Dev 20:1692–1708. http://dx.doi.org/10.1101/gad.1419406.
   PubMed Web of Science ®Google Scholar
• Halevy O, Cantley LC. 2004. Differential regulation of the phosphoinositide 3-kinase and MAP kinase pathways by hepatocyte growth factor versus. insulin-like growth factor-I in myogenic cells. Exp Cell Res 297:224–234. http://dx.doi.org/10.1016/j.yexcr.2004.03.024.
   PubMed Web of Science ®Google Scholar
• Jiang BH, 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. http://dx.doi.org/10.1073/pnas.95.24.14179.
   PubMed Web of Science ®Google Scholar
• Kaliman P, Vinals F, Testar X, Palacin M, Zorzano A. 1996. Phosphatidylinositol 3-kinase inhibitors block differentiation of skeletal muscle cells. J Biol Chem 271:19146–19151. http://dx.doi.org/10.1074/jbc.271.32.19146.
   PubMed Web of Science ®Google Scholar
• Hirsch E, Costa C, Ciraolo E. 2007. Phosphoinositide 3-kinases as a common platform for multi-hormone signaling. J Endocrinol 194:243–256. http://dx.doi.org/10.1677/JOE-07-0097.
   PubMed Web of Science ®Google Scholar
• Geering B, Cutillas PR, Nock G, Gharbi SI, Vanhaesebroeck B. 2007. Class IA phosphoinositide 3-kinases are obligate p85-p110 heterodimers. Proc Natl Acad Sci U S A 104:7809–7814. http://dx.doi.org/10.1073/pnas.0700373104.
   PubMed Web of Science ®Google Scholar
• Zhao JJ, Cheng H, Jia S, Wang L, Gjoerup OV, Mikami A, Roberts TM. 2006. The p110alpha isoform of PI3K is essential for proper growth factor signaling and oncogenic transformation. Proc Natl Acad Sci U S A 103:16296–16300. http://dx.doi.org/10.1073/pnas.0607899103.
   PubMed Web of Science ®Google Scholar
• Samuels Y, Wang Z, Bardelli A, Silliman N, Ptak J, Szabo S, Yan H, Gazdar A, Powell SM, Riggins GJ, Willson JK, Markowitz S, Kinzler KW, Vogelstein B, Velculescu VE. 2004. High frequency of mutations of the PIK3CA gene in human cancers. Science 304:554. http://dx.doi.org/10.1126/science.1096502.
   PubMed Web of Science ®Google Scholar
• Vogt PK, Gymnopoulos M, Hart JR. 2009. PI 3-kinase and cancer: changing accents. Curr Opin Genet Dev 19:12–17. http://dx.doi.org/10.1016/j.gde.2008.11.011.
   PubMed Web of Science ®Google Scholar
• Ciraolo E, Iezzi M, Marone R, Marengo S, Curcio C, Costa C, Azzolino O, Gonella C, Rubinetto C, Wu H, Dastru W, Martin EL, Silengo L, Altruda F, Turco E, Lanzetti L, Musiani P, Ruckle T, Rommel C, Backer JM, Forni G, Wymann MP, Hirsch E. 2008. Phosphoinositide 3-kinase p110beta activity: key role in metabolism and mammary gland cancer but not development. Sci Signal 1:ra3. http://dx.doi.org/10.1126/scisignal.1161577.
   PubMed Web of Science ®Google Scholar
• Guillermet-Guibert J, Bjorklof K, Salpekar A, Gonella C, Ramadani F, Bilancio A, Meek S, Smith AJ, Okkenhaug K, Vanhaesebroeck B. 2008. The p110beta isoform of phosphoinositide 3-kinase signals downstream of G protein-coupled receptors and is functionally redundant with p110gamma. Proc Natl Acad Sci U S A 105:8292–8297. http://dx.doi.org/10.1073/pnas.0707761105.
   PubMed Web of Science ®Google Scholar
• Jia S, Liu Z, Zhang S, Liu P, Zhang L, Lee SH, Zhang J, Signoretti S, Loda M, Roberts TM, Zhao JJ. 2008. Essential roles of PI(3)K-p110beta in cell growth, metabolism and tumorigenesis. Nature 454:776–779. http://dx.doi.org/10.1038/nature07091.
   PubMed Web of Science ®Google Scholar
• Marques M, Kumar A, Cortes I, Gonzalez-Garcia A, Hernandez C, Moreno-Ortiz MC, Carrera AC. 2008. Phosphoinositide 3-kinases p110alpha and p110beta regulate cell cycle entry, exhibiting distinct activation kinetics in G1 phase. Mol Cell Biol 28:2803–2814. http://dx.doi.org/10.1128/MCB.01786-07.
   PubMed Web of Science ®Google Scholar
• Foukas LC, Claret M, Pearce W, Okkenhaug K, Meek S, Peskett E, Sancho S, Smith AJ, Withers DJ, Vanhaesebroeck B. 2006. Critical role for the p110alpha phosphoinositide-3-OH kinase in growth and metabolic regulation. Nature 441:366–370. http://dx.doi.org/10.1038/nature04694.
   PubMed Web of Science ®Google Scholar
• Matheny RW, Jr, Adamo ML. 2010. PI3K p110 alpha and p110 beta have differential effects on Akt activation and protection against oxidative stress-induced apoptosis in myoblasts. Cell Death Differ 17:677–688. http://dx.doi.org/10.1038/cdd.2009.150.
   PubMedGoogle Scholar
• Knight ZA, Gonzalez B, Feldman ME, Zunder ER, Goldenberg DD, Williams O, Loewith R, Stokoe D, Balla A, Toth B, Balla T, Weiss WA, Williams RL, Shokat KM. 2006. A pharmacological map of the PI3-K family defines a role for p110alpha in insulin signaling. Cell 125:733–747. http://dx.doi.org/10.1016/j.cell.2006.03.035.
   PubMed Web of Science ®Google Scholar
• Matheny RW, Jr, Lynch CM, Leandry LA. 2012. Enhanced Akt phosphorylation and myogenic differentiation in PI3K p110beta-deficient myoblasts is mediated by PI3K p110alpha and mTORC2. Growth Factors 30:367–384. http://dx.doi.org/10.3109/08977194.2012.734507.
   PubMed Web of Science ®Google Scholar
• Hayakawa M, Kaizawa H, Moritomo H, Koizumi T, Ohishi T, Okada M, Ohta M, Tsukamoto S, Parker P, Workman P, Waterfield M. 2006. Synthesis and biological evaluation of 4-morpholino-2-phenylquinazolines and related derivatives as novel PI3 kinase p110alpha inhibitors. Bioorg Med Chem 14:6847–6858. http://dx.doi.org/10.1016/j.bmc.2006.06.046.
   PubMed Web of Science ®Google Scholar
• Matheny RW, Jr, Adamo ML. 2009. Effects of PI3K catalytic subunit and Akt isoform deficiency on mTOR and p70S6K activation in myoblasts. Biochem Biophys Res Commun 390:252–257. http://dx.doi.org/10.1016/j.bbrc.2009.09.100.
   PubMedGoogle Scholar
• Huwiler KG, Machleidt T, Chase L, Hanson B, Robers MB. 2009. Characterization of serotonin 5-hydroxytryptamine-1A receptor activation using a phospho-extracellular-signal regulated kinase 2 sensor. Anal Biochem 393:95–104. http://dx.doi.org/10.1016/j.ab.2009.06.018.
   PubMed Web of Science ®Google Scholar
• Kost TA, Condreay JP, Ames RS, Rees S, Romanos MA. 2007. Implementation of BacMam virus gene delivery technology in a drug discovery setting. Drug Discov Today 12:396–403. http://dx.doi.org/10.1016/j.drudis.2007.02.017.
   PubMed Web of Science ®Google Scholar
• Ames R, Fornwald J, Nuthulaganti P, Trill J, Foley J, Buckley P, Kost T, Wu Z, Romanos M. 2004. BacMam recombinant baculoviruses in G protein-coupled receptor drug discovery. Receptors Channels 10:99–107. http://dx.doi.org/10.1080/10606820490514969.
   PubMedGoogle Scholar
• Tallquist MD, Weismann KE, Hellstrom M, Soriano P. 2000. Early myotome specification regulates PDGFA expression and axial skeleton development. Development 127:5059–5070.
   PubMed Web of Science ®Google Scholar
• Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. http://dx.doi.org/10.1016/0003-2697(76)90527-3.
   PubMed Web of Science ®Google Scholar
• Jackson SP, Schoenwaelder SM, Goncalves I, Nesbitt WS, Yap CL, Wright CE, Kenche V, Anderson KE, Dopheide SM, Yuan Y, Sturgeon SA, Prabaharan H, Thompson PE, Smith GD, Shepherd PR, Daniele N, Kulkarni S, Abbott B, Saylik D, Jones C, Lu L, Giuliano S, Hughan SC, Angus JA, Robertson AD, Salem HH. 2005. PI 3-kinase p110beta: a new target for antithrombotic therapy. Nat Med 11:507–514. http://dx.doi.org/10.1038/nm1232.
   PubMed Web of Science ®Google Scholar
• Lynch CM, Leandry LA, Matheny RW, Jr. 2013. Lysophosphatidic acid-stimulated phosphorylation of PKD2 is mediated by PI3K p110beta and PKCdelta in myoblasts. J Recept Signal Transduct Res 33:41–48. http://dx.doi.org/10.3109/10799893.2012.752005.
   PubMed Web of Science ®Google Scholar
• Skapek SX, Rhee J, Spicer DB, Lassar AB. 1995. Inhibition of myogenic differentiation in proliferating myoblasts by cyclin D1-dependent kinase. Science 267:1022–1024. http://dx.doi.org/10.1126/science.7863328.
   PubMed Web of Science ®Google Scholar
• Rao SS, Chu C, Kohtz DS. 1994. Ectopic expression of cyclin D1 prevents activation of gene transcription by myogenic basic helix-loop-helix regulators. Mol Cell Biol 14:5259–5267.
   PubMedGoogle Scholar
• Bader D, Masaki T, Fischman DA. 1982. Immunochemical analysis of myosin heavy chain during avian myogenesis in vivo and in vitro. J Cell Biol 95:763–770. http://dx.doi.org/10.1083/jcb.95.3.763.
   PubMed Web of Science ®Google Scholar
• Sumitani S, Goya K, Testa JR, Kouhara H, Kasayama S. 2002. Akt1 and Akt2 differently regulate muscle creatine kinase and myogenin gene transcription in insulin-induced differentiation of C2C12 myoblasts. Endocrinology 143:820–828. http://dx.doi.org/10.1210/endo.143.3.8687.
   PubMed Web of Science ®Google Scholar
• Beylkin DH, Allen DL, Leinwand LA. 2006. MyoD, Myf5, and the calcineurin pathway activate the developmental myosin heavy chain genes. Dev Biol 294:541–553. http://dx.doi.org/10.1016/j.ydbio.2006.02.049.
   PubMedGoogle Scholar
• Utermark T, Rao T, Cheng H, Wang Q, Lee SH, Wang ZC, Iglehart JD, Roberts TM, Muller WJ, Zhao JJ. 2012. The p110alpha and p110beta isoforms of PI3K play divergent roles in mammary gland development and tumorigenesis. Genes Dev 26:1573–1586. http://dx.doi.org/10.1101/gad.191973.112.
   PubMed Web of Science ®Google Scholar
• Jiang BH, 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. http://dx.doi.org/10.1073/pnas.96.5.2077.
   PubMed Web of Science ®Google Scholar
• Rotwein P, Wilson EM. 2009. Distinct actions of Akt1 and Akt2 in skeletal muscle differentiation. J Cell Physiol 219:503–511. http://dx.doi.org/10.1002/jcp.21692.
   PubMedGoogle Scholar
• Vandromme M, Rochat A, Meier R, Carnac G, Besser D, Hemmings BA, Fernandez A, Lamb NJ. 2001. Protein kinase B beta/Akt2 plays a specific role in muscle differentiation. J Biol Chem 276:8173–8179. http://dx.doi.org/10.1074/jbc.M005587200.
   PubMedGoogle Scholar
• Foukas LC, Berenjeno IM, Gray A, Khwaja A, Vanhaesebroeck B. 2010. Activity of any class IA PI3K isoform can sustain cell proliferation and survival. Proc Natl Acad Sci U S A 107:11381–11386. http://dx.doi.org/10.1073/pnas.0906461107.
   PubMed Web of Science ®Google Scholar
• Chaussade C, Rewcastle GW, Kendall JD, Denny WA, Cho K, Gronning LM, Chong ML, Anagnostou SH, Jackson SP, Daniele N, Shepherd PR. 2007. Evidence for functional redundancy of class IA PI3K isoforms in insulin signalling. Biochem J 404:449–458. http://dx.doi.org/10.1042/BJ20070003.
   PubMedGoogle Scholar
• Wang M, Amano SU, Flach RJ, Chawla A, Aouadi M, Czech MP. 2013. Identification of Map4k4 as a novel suppressor of skeletal muscle differentiation. Mol Cell Biol 33:678–687. http://dx.doi.org/10.1128/MCB.00618-12.
   PubMedGoogle Scholar
• Sopasakis VR, Liu P, Suzuki R, Kondo T, Winnay J, Tran TT, Asano T, Smyth G, Sajan MP, Farese RV, Kahn CR, Zhao JJ. 2010. Specific roles of the p110alpha isoform of phosphatidylinositol 3-kinase in hepatic insulin signaling and metabolic regulation. Cell Metab 11:220–230. http://dx.doi.org/10.1016/j.cmet.2010.02.002.
   PubMedGoogle Scholar
• McMullen JR, Shioi T, Huang WY, Zhang L, Tarnavski O, Bisping E, Schinke M, Kong S, Sherwood MC, Brown J, Riggi L, Kang PM, Izumo S. 2004. The insulin-like growth factor 1 receptor induces physiological heart growth via the phosphoinositide 3-kinase(p110alpha) pathway. J Biol Chem 279:4782–4793. http://dx.doi.org/10.1074/jbc.M310405200.
   PubMed Web of Science ®Google Scholar
• Hill K, Welti S, Yu J, Murray JT, Yip SC, Condeelis JS, Segall JE, Backer JM. 2000. Specific requirement for the p85-p110alpha phosphatidylinositol 3-kinase during epidermal growth factor-stimulated actin nucleation in breast cancer cells. J Biol Chem 275:3741–3744. http://dx.doi.org/10.1074/jbc.275.6.3741.
   PubMed Web of Science ®Google Scholar
• Jia S, Roberts TM, Zhao JJ. 2009. Should individual PI3 kinase isoforms be targeted in cancer? Curr Opin Cell Biol 21:199–208. http://dx.doi.org/10.1016/j.ceb.2008.12.007.
   PubMed Web of Science ®Google Scholar
• Smith GC, Ong WK, Rewcastle GW, Kendall JD, Han W, Shepherd PR. 2012. Effects of acutely inhibiting PI3K isoforms and mTOR on regulation of glucose metabolism in vivo. Biochem J 442:161–169. http://dx.doi.org/10.1042/BJ20111913.
   PubMedGoogle Scholar
• Leiter EH, Premdas F, Harrison DE, Lipson LG. 1988. Aging and glucose homeostasis in C57BL/6J male mice. FASEB J 2:2807–2811.
   PubMed Web of Science ®Google Scholar
• Foukas LC, Bilanges B, Bettedi L, Pearce W, Ali K, Sancho S, Withers DJ, Vanhaesebroeck B. 2013. Long-term p110alpha PI3K inactivation exerts a beneficial effect on metabolism. EMBO Mol Med 5:563–571. http://dx.doi.org/10.1002/emmm.201201953.
   PubMed Web of Science ®Google Scholar
• Lai KM, Gonzalez M, Poueymirou WT, Kline WO, Na E, Zlotchenko E, Stitt TN, Economides AN, Yancopoulos GD, Glass DJ. 2004. Conditional activation of Akt in adult skeletal muscle induces rapid hypertrophy. Mol Cell Biol 24:9295–9304. http://dx.doi.org/10.1128/MCB.24.21.9295-9304.2004.
   PubMed Web of Science ®Google Scholar
• Izumiya Y, Hopkins T, Morris C, Sato K, Zeng L, Viereck J, Hamilton JA, Ouchi N, LeBrasseur NK, Walsh K. 2008. Fast/glycolytic muscle fiber growth reduces fat mass and improves metabolic parameters in obese mice. Cell Metab 7:159–172. http://dx.doi.org/10.1016/j.cmet.2007.11.003.
   PubMed Web of Science ®Google Scholar
• Bodine SC, Stitt TN, Gonzalez M, Kline WO, Stover GL, Bauerlein R, Zlotchenko E, Scrimgeour A, Lawrence JC, Glass DJ, Yancopoulos GD. 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. http://dx.doi.org/10.1038/ncb1101-1014.
   PubMed Web of Science ®Google Scholar
• Juss JK, Hayhoe RP, Owen CE, Bruce I, Walmsley SR, Cowburn AS, Kulkarni S, Boyle KB, Stephens L, Hawkins PT, Chilvers ER, Condliffe AM. 2012. Functional redundancy of class I phosphoinositide 3-kinase (PI3K) isoforms in signaling growth factor-mediated human neutrophil survival. PLoS One 7:e45933. http://dx.doi.org/10.1371/journal.pone.0045933.
   PubMedGoogle Scholar
• Beeton CA, Chance EM, Foukas LC, Shepherd PR. 2000. Comparison of the kinetic properties of the lipid- and protein-kinase activities of the p110alpha and p110beta catalytic subunits of class-Ia phosphoinositide 3-kinases. Biochem J 350(Pt 2):353–359. http://dx.doi.org/10.1042/0264-6021:3500353.
   PubMedGoogle Scholar
• Buchanan CM, Dickson JM, Lee WJ, Guthridge MA, Kendall JD, Shepherd PR. 2013. Oncogenic mutations of p110alpha isoform of PI 3-kinase upregulate its protein kinase activity. PLoS One 8:e71337. http://dx.doi.org/10.1371/journal.pone.0071337.
   PubMedGoogle Scholar