Akt2, a Novel Functional Link between p38 Mitogen-Activated Protein Kinase and Phosphatidylinositol 3-Kinase Pathways in Myogenesis

REFERENCES

• Alessi, D. R., and Cohen P.. 1998. Mechanism of activation and function of protein kinase B. Curr. Opin. Genet. Dev. 8:55–62.
   PubMed Web of Science ®Google Scholar
• Alessi, D. R., Deak M., Casamayor A., Caudwell F. B., Morrice N., Norman D. G., Gaffney P., Reese C. B., MacDougall C. N., Harbison D., Ashworth A., and Bownes B.. 1997. 3-Phosphoinositide-dependent kinase 1 (PDK1): structural and functional homology with the Drosophila DSTPK61 kinase. Curr. Biol. 7:776–789.
   PubMed Web of Science ®Google Scholar
• Alessi, D. R., Caudwell F. B., Andjelkovic M., Hemmings B. A., and Cohen P.. 1996. Molecular basis for substrate specificity of protein kinase B: comparison with MAPKAP kinase-1 and p70 S6 kinase. FEBS Lett. 399:333–338.
   PubMed Web of Science ®Google Scholar
• Alessi, D. R., Andjelkovic M., Caudwell B., Cron P., Morrice N., Cohen P., and Hemmings B. A.. 1996. Mechanism of activation of protein kinase B by insulin and IGF-I. EMBO J. 15:6541–6551.
   PubMed Web of Science ®Google Scholar
• Allen, M., Svensson L., Roach M., Hambar J., McNeish J., and Gabel G. A.. 2000. Deficiency of the stress kinase p38α results in embryonic lethality: characterization of the kinase dependence of stress responses of enzyme-deficient embryonic stem cells. J. Exp. Med. 191:859–869.
   PubMed Web of Science ®Google Scholar
• Alonso, G., Ambrosino C., Jones M., and Nebrada A. R.. 2000. Differential activation of p38 mitogen-activated protein kinase isoforms depending on signal strength. J. Biol. Chem. 275:40641–40648.
   PubMedGoogle Scholar
• Altomare, D. A., Lyons G. E., Mitsuuchi Y., Cheng J. Q., and Testa J. R.. 1998. Akt2 mRNA is highly expressed in embryonic brown fat and the Akt2 kinase is activated by insulin. Oncogene 16:2407–2411.
   PubMedGoogle Scholar
• Andjelkovic, M., Alessi D. R., Meier R., Fernandez A., Lamb N. J. C., Frech M., Cron P., Cohen P., Lucocq J. M., and Hemmings B. A.. 1997. Role of translocation in the activation and function of protein kinase B. J. Biol. Chem. 272:31515–31524.
   PubMed Web of Science ®Google Scholar
• Baudhuin, L. M., Kristina K. L., Lu J., and Xu Y.. 2002. Akt activation induced by lysophosphatidic acid and sphingosine-1-phosphate requires both mitogen-activated protein kinase kinase and p38 mitogen-activated protein kinase and is cell-line specific. Mol. Pharmacol. 62:660–672.
   PubMedGoogle Scholar
• Belham, C., Comb M. J., and Avruch J.. 2001. Identification of the NIMA family kinases NEK6/7 as regulators of the p70 ribosomal S6 kinase. Curr. Biol. 11:1155–1167.
   PubMedGoogle Scholar
• Bergstrom, D. A., Penn B. H., Strand A., Perry R. L. S., Rudnicki M. A., and Tapscott S. J.. 2002. Promoter-specific regulation of MyoD binding and signal transduction cooperate to pattern gene expression. Mol. Cell 9:587–600.
   PubMed Web of Science ®Google Scholar
• Calera, M., and Pilch P. F.. 1998. Induction of Akt2 correlates with differentiation in Sol8 muscle cells. Biochem. Biophys. Res. Commun. 251:835–841.
   PubMedGoogle Scholar
• Casanovas, O., Miro F., Estanyol J. M., Itarte E., Agell N., and Bachs O.. 2000. Osmotic stress regulated the stability of cyclin D1 in a p38SAPK2-dependent manner. J. Biol. Chem. 275:35091–35097.
   PubMed Web of Science ®Google Scholar
• Chen, W. S., Xu P.-Y., Gottlob K., Chen M.-L., Sokol K., Shiyanova T., Roninson I., Weng W., Suzuki R., Tobe K., Kadwaki T., and Hay N.. 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
• Cho, H., Thorvaldson J. L., Chu Q., Feng F., and Birnbaum M. J.. 2001. Akt1/PKBα is required for normal growth but dispensable for maintenance of glucose homeostasis in mice. J. Biol. Chem. 276:38349–38352.
   PubMed Web of Science ®Google Scholar
• Cho, H., Mu J., Kim J. K., Thorvaldsen J. L., Chu Q., Crenshaw III E. B., Kaestner K. H., Bartolmei M. S., Shulman G. I., and Birnbaum M. J.. 2001. Insulin resistance and a diabetes mellitus-like syndrome in mice lacking the protein kinase Akt2 (PKBβ). Science 292:1728–1731.
   PubMed Web of Science ®Google Scholar
• Chun, Y. K., Kim J., Kwon S., Choi S. H., Hong F., Moon K., Kim J. M., Choi S. L., Kim B. S., Ha J., and Kim S. S.. 2000. Phosphatidylinositol 3-kinase stimulates muscle differentiation by activating p38 mitogen-activated protein kinase. Biochem. Biophys. Res. Commun. 276:502–507.
   PubMedGoogle Scholar
• Coolican, S. A., Samuel D. S., Ewton D. Z., McWade F. J., and Florini J. R.. 1997. The mitogenic and myogenic actions of the insulin-like growth factors utilize distinct signalling pathways. J. Biol. Chem. 272:6653–6662.
   PubMed Web of Science ®Google Scholar
• Cuenda, C., and Cohen P.. 1999. Stress-activated protein kinase-2/p38 and a rapamycin-sensitive pathway are required for C2 myogenesis. J. Biol. Chem. 274:4341–4346.
   PubMed Web of Science ®Google Scholar
• Delcommenne, M., Tan C., Gray V., Rue L., Woogett J., and Dedhar S.. 1998. Phosphoinositide-3-OH kinase-dependent regulation of glycogen synthase kinase 3 and protein kinase B/Akt by the integrin-linked kinase. Proc. Natl. Acad. Sci. USA 95:11211–11216.
   PubMed Web of Science ®Google Scholar
• Frech, M., Andjelkovic M., Ingley E., Reddy K. K., Falck J. R., and Hemmings B. A.. 1997. High affinity binding of inositol phosphates and phosphoinositides to the pleckstrin homology domain of RAC/protein kinase B and their influence on kinase activity. J. Biol. Chem. 272:8474–8481.
   PubMed Web of Science ®Google Scholar
• Fujio, Y., Guo K., Mano T., Mitsuuchi Y., Testa J. R., and Walsh K.. 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., Mitsuuchi Y., Testa J. R., and Walsh K.. 2001. Activation of Akt2 inhibits anoikis and apoptosis induced by myogenic differentiation. Cell Death Differ. 8:1207–1212.
   PubMedGoogle Scholar
• Galbiati, F., Volonte D., Engelman J. A., Scherer P. E., and Lisanti M. P.. 1999. Targeted down-regulation of caveolin-3 is sufficient to inhibit myotube formation in differentiating C2 myoblasts. Transient activation of p38 mitogen-activated protein kinase is required for induction of caveolin-3 expression and subsequent myotube formation. J. Biol. Chem. 274:30315–30321.
   PubMedGoogle Scholar
• Han, J., Lee J.-D., Bibbs L., and Ulevitch R. J.. 1994. A MAP kinase targeted by endotoxin and hyperosmolarity in mammalian cells. Science 265:808–811.
   PubMed Web of Science ®Google Scholar
• Jiang, B.-H., Zheng J. Z., and Vogt P. K.. 1998. An essential role of phosphatidylinositol 3-kinase in myogenic differentiation. Proc. Natl. Acad. Sci. USA 95:14179–14183.
   PubMed Web of Science ®Google Scholar
• Jiang, B.-H., Aoki M., Zheng J. Z., Li J., and Vogt P. K.. 1999. Myogenic signalling of phosphatidylinositol 3-kinase requires the serine-threonine kinase Akt/protein kinase B. Proc. Natl. Acad. Sci. USA 96:2077–2081.
   PubMed Web of Science ®Google Scholar
• Kaliman, P., Viñals F., Tester X., Palacin M., and Zorzano A.. 1996. Phosphatidylinositol 3-kinase inhibitors block differentiation of skeletal muscle cells. J. Biol. Chem. 271:19146–19151.
   PubMed Web of Science ®Google Scholar
• Kaliman, P., Canicio J., Shepher P. R., Beeton C. A., Testar X., Palacin M., and Zorzano A.. 1998. Insulin-like growth factors require phosphatidylinositol 3-kinase to signal myogenesis: dominant negative p85 expression blocks differentiation of L6E9 muscle cells. Mol. Endocrinol. 12:66–77.
   PubMedGoogle Scholar
• Kaneko, S., Feldman R. I., Yu L., Wu Z., Gritsko T., Shelley S. A., Nicosia S. V., Nobori T., and Cheng J. Q.. 2002. Positive feedback regulation between Akt2 and MyoD during muscle differentiation: cloning of the Akt2 promoter. J. Biol. Chem. 277:23230–23235.
   PubMedGoogle Scholar
• Kotlyarov, A., Yannoni Y., Fritz S., Laass K., Teliez J.-B., Pitman D., and Gaestel M.. 2002. Distinct cellular function of MK2. Mol. Cell. Biol. 22:4827–4835.
   PubMed Web of Science ®Google Scholar
• Lali, F. V., Hunt A. E., Turner S. J., and Foxwell B. M. J.. 2000. The pyridinyl imidazole inhibitor SB203580 blocks phosphoinositide-dependent protein kinase activity, protein kinase B phosphorylation, and retinoblastoma hyperphosphorylation in interleukin-2-stimulated T cells independently of p38 mitogen-activated protein kinase. J. Biol. Chem. 275:7395–7402.
   PubMed Web of Science ®Google Scholar
• Langley, B., Thomas M., Bishop A., Sharma M., Gilmour S., and Kambadur R.. 2002. Myostatin inhibits myoblast differentiation by down-regulating MyoD expression. J. Biol. Chem. 277:49831–49840.
   PubMed Web of Science ®Google Scholar
• Laprise, P., Chailler P., Houde M., Beaulieu J.-F., Boucher M.-J., and Rivard N.. 2002. Phosphatidylinositol-3-kinase controls human intestinal epithelial cell differentiation by promoting adherens junction assembly and p38 MAPK activation. J. Biol. Chem. 277:8226–8234.
   PubMed Web of Science ®Google Scholar
• Lawlor, M. A., and Rotwein P.. 2000. Insulin-like growth factor-mediated muscle cell survival: central roles for Akt and cyclin-dependent kinase inhibitor p21. Mol. Cell. Biol. 20:8983–8995.
   PubMedGoogle Scholar
• Lawlor, M. A., Feng X., Everding D. R., Sieger K., Stewart C. E. H., and Rotwein P.. 2000. Dual control of muscle cell survival by distinct growth factor-regulated signaling pathways. Mol. Cell. Biol. 20:3256–3265.
   PubMed Web of Science ®Google Scholar
• Lechner, C., Zahalka M. A., Giot J.-F., Moller N. P. H., and Ulrich A.. 1996. ERK6, a mitogen-activated protein kinase involved in C2 myoblast differentiation. J. Biol. Chem. 93:4355–4359.
   Google Scholar
• Lee, J. C., Laydon J. T., McDonnell P. C., Gallagher T. F., Kumar S., Green D., McNulty D., Blumenthal M. J., Hayes R. J., Landvatter S. W., Strickler J. E., McLaughlin M. M., Siemens I., Fisher S., Livi G. P., White J. R., Adams J. L., and Young P. R.. 1994. Identification and characterization of a novel protein kinase involved in regulation of inflammatory cytokine biosynthesis. Nature 372:739–746.
   PubMed Web of Science ®Google Scholar
• Li, Y., Jiang B.-H., Ensign W. Y., Vogt P. K., and Han J.. 2000. Myogenic differentiation requires signalling through both phosphatidylinositol 3-kinase and p38 MAP kinase. Cell. Signal. 12:751–757.
   PubMed Web of Science ®Google Scholar
• Meier, R., Alessi D. R., Cron P., Andjelkovic M., and Hemmings B. A.. 1997. Mitogenic activation, phosphorylation, and nuclear translocation of protein kinase Bβ. J. Biol. Chem. 272:30491–30497.
   PubMed Web of Science ®Google Scholar
• Ming, X.-F., Stoeklin G., Lu M., Looser R., and Moroni C.. 2001. Parallel and independent regulation of interleukin-3 mRNA turnover by phosphatidylinositol 3-kinase and p38 mitogen-activated protein kinase. Mol. Cell. Biol. 21:5778–5789.
   PubMed Web of Science ®Google Scholar
• Nebrada, A. R., and Porras A.. 2000. p38 MAP kinases: beyond the stress response. Trends Biochem. Sci. 25:257–260.
   PubMedGoogle Scholar
• Peng, X., Xu P.-Z., Chen M.-L., Hahn-Windgassen A., Skeen J., Jacobs J., Sundararajan D., Chen W. S., Crawford S. E., Coleman K., and Hay N.. 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.
   PubMed Web of Science ®Google Scholar
• Perry, R. L. S., and M. A. Rudnicki. 2000. Molecular mechanisms regulating myogenic determination and differentiation. Front. Biosci. 5:750–767.
   PubMed Web of Science ®Google Scholar
• Persad, S., Attwell S., Gray V., Mawji N., Deng J. T., Leung D., Yan J., Sanghera J., Walsh M. P., and Dedhar S.. 2001. Regulation of protein kinase B/Akt-serine 473 phosphorylation by integrin-linked kinase: critical roles for kinase and amino acids arginine 211 and serine 343. J. Biol. Chem. 276:27462–27469.
   PubMed Web of Science ®Google Scholar
• Puri, P. L., Wu Z., Xhang P., Wood L. D., Bhakta K. S., Han J., Feramisco J. R., Karin M., and Wang J. Y. J.. 2000. Induction of terminal differentiation by constitutive activation of p38 MAP kinase in human rhabdomyosarcoma cells. Genes Dev. 14:574–584.
   PubMed Web of Science ®Google Scholar
• Rane, M. J., Coxon P. Y., Powell D. W., Webster R., Klein J. B., Pierce W., Ping P., and McLeish K. R.. 2001. p38 kinase-dependent MAPKAPK-2 activation functions as 3-phosphoinositide-dependent kinase-2 for Akt in human neutrophils. J. Biol. Chem. 276:3517–3523.
   PubMed Web of Science ®Google Scholar
• Rössig, L., A. S. Jadidi, C. Urbich, C. Badorff, A. M. Zeiher, and S. Dimmeler. 2001. Akt-dependent phosphorylation of p21CIP1 regulates PCNA binding and proliferation of endothelial cells. Mol. Cell. Biol. 21:5644–5657.
   PubMed Web of Science ®Google Scholar
• Scheid, M. P., Marignani P. A., and Woodgett J. R.. 2002. Multiple phosphoinositide 3-kinase-dependent steps in activation of protein kinase B. Mol. Cell. Biol. 22:6247–6260.
   PubMed Web of Science ®Google Scholar
• Shaw, M., Cohen P., and Alessi D. R.. 1998. The activation of protein kinase B by H2O2 or heat shock is mediated by phosphoinositide-3-kinase and not by mitogen-activated protein kinase-activated protein kinase-2. Biochem. J. 336:241–246.
   PubMed Web of Science ®Google Scholar
• Stokoe, D., Stephens L. R., Copeland T., Gaffney P. R., Reese C. B., Painter G. F., Holmes A. B., McCormick F., and Hawkins P. T.. 1997. Dual role of phosphatidylinositol-3,4,5-trisphosphate in the activation of protein kinase B. Science 277:567–570.
   PubMed Web of Science ®Google Scholar
• Tamir, Y., and Bengal E.. 2000. Phosphoinositide 3-kinase induces the transcriptional activity of MEF2 proteins during muscle differentiation. J. Biol. Chem. 275:34424–34432.
   PubMedGoogle Scholar
• Tamura, K., Sudo T., Senttleben U., Dadak A., Johnson R., and Karin M.. 2000. Requirement of p38α in erythropoietin expression: a role for stress kinases in erythropoiesis. Cell 102:221–231.
   PubMed Web of Science ®Google Scholar
• Tang, Y., Yu J., and Field J.. 1999. Signals from Ras, Rac, and Rho GTPases converge on the Pak protein kinase in Rat-1 fibroblasts. Mol. Cell. Biol. 19:1881–1891.
   PubMedGoogle Scholar
• Troussard, A. A., Mawji N. M., Ong C., Mui A., St. Arnaud R., and Dedhar S.. 2003. Conditional knock-out of integrin-linked kinase demonstrates an essential role in protein kinase B/Akt activation. J. Biol. Chem. 278:22374–22378.
   PubMed Web of Science ®Google Scholar
• Tureckova, J., Wilson E. M., Cappalonga J. L., and Rotwein P.. 2001. Insulin-like growth factor-mediated muscle differentiation. J. Biol. Chem. 276:39264–39270.
   PubMed Web of Science ®Google Scholar
• Vandromme, M., Roche A., Meier R., Carnac G., Besser D., Hemmings B. A., Fernandez A., and Lamb N. J. C.. 2001. Protein kinase Bβ/Akt2 plays a specific role in muscle differentiation. J. Biol. Chem. 276:8173–8179.
   PubMedGoogle Scholar
• Wang, S., Nath N., Minden A., and Chellappan S.. 1999. Regulation of Rb and E2F by signal transduction cascades: divergent effects of JNK1 and p38 kinases. EMBO J. 18:1559–1570.
   PubMedGoogle Scholar
• Williams, M. R., Arthur J. S., Balendran A., van der Kaay J., Poli V., Cohen P., and Alessi D. R.. 2000. The role of 3-phosphoinositide-dependent protein kinase 1 in activating AGC kinases defined in embryonic stem cells. Curr. Biol. 10:439–448.
   PubMed Web of Science ®Google Scholar
• Wu, Z., Woodring P. J., Bhakta K. S., Tamura K., Wen F., Feramisco J. R., Karin M., Wang J. Y. J., and Puri P. L.. 2000. p38 and extracellular signal-related kinases regulate the myogenic program at multiple stages. Mol. Cell. Biol. 20:3951–3964.
   PubMed Web of Science ®Google Scholar
• Xu, Q., and Wu Z.. 2000. The insulin-like growth factor-phosphatidylinositol 3-kinase-Akt signalling pathway regulates myogenin expression in normal myogenic cells but not in rhabdomyosarcoma-derived RD cells. J. Biol. Chem. 275:36750–36757.
   PubMed Web of Science ®Google Scholar
• Yaffe, M. B., Leparc G. G., Lai J., Obata T., Volinia S., and Cantley L. C.. 2001. A motif-based profile scanning approach for genome-wide prediction of signalling pathways. Nat. Biotechnol. 19:348–353.
   PubMed Web of Science ®Google Scholar
• Yang, S.-H., Galamis A., and Sharrocks A. D.. 1999. Targeting of p38 mitogen-activated protein kinase to MEF2 transcription factors. Mol. Cell. Biol. 19:4028–4038.
   PubMedGoogle Scholar
• Yun, K., and Wold B.. 1996. Skeletal muscle determination and differentiation: story of a core regulatory network and its context. Curr. Opin. Cell Biol. 8:877–889.
   PubMed Web of Science ®Google Scholar
• Zetser, A., Gredinger E., and Bengal E.. 1999. p38 mitogen-activated protein kinase pathway promotes skeletal muscle differentiation: participation of the MEF2C transcription factor. J. Biol. Chem. 274:5193–5200.
   PubMed Web of Science ®Google Scholar
• Zhao, M., New L., Kravchenko V. V., Kato Y., Gram H., di Padova F., Olsen E. N., Ulevitch R. J., and Han J.. 1999. Regulation of MEF2 transcription factor family by p38. Mol. Cell. Biol. 19:21–30.
   PubMedGoogle Scholar
• Zhou, B. P., Liao Y., Xia W., Spohn B., Lee M.-H., and Hung M.-C.. 2001. Cytoplasmic localization of p21Cip1/WAF1 by Akt-induced phosphorylation in HER-2/neu-overexpressing cells. Nat. Cell Biol. 3:245–252.
   PubMed Web of Science ®Google Scholar