Forskolin attenuates the action of insulin on the Akt-mTOR pathway in human skeletal muscle

Applied Physiology, Nutrition and Metabolism

Volumn 34, Issue 5, 2009, Pages 916-925

  Richmond, Scott R ^a   Touchberry, Chad D ^a   Gallagher, Philip M ^a  

^a UNIVERSITY OF KANSAS   (United States)

Author keywords

4EBP1l; CAMP; Insulin; P70 ribosomal protein S6 kinase 1 (S6K1); Protein kinase B (PKB)

Indexed keywords

EIF4EBP1 PROTEIN, HUMAN; FORSKOLIN; INSULIN; MAMMALIAN TARGET OF RAPAMYCIN; PHOSPHOPROTEIN; PROTEIN KINASE; PROTEIN KINASE B; S6 KINASE; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ADULT; ARTICLE; GENETICS; HUMAN; MALE; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; SKELETAL MUSCLE; TISSUE CULTURE TECHNIQUE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; FORSKOLIN; HUMANS; INSULIN; MALE; MUSCLE, SKELETAL; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN KINASES; PROTO-ONCOGENE PROTEINS C-AKT; RIBOSOMAL PROTEIN S6 KINASES, 90-KDA; TISSUE CULTURE TECHNIQUES; YOUNG ADULT;

EID: 73649093768     PISSN: 17155312     EISSN: None     Source Type: Journal    
DOI: 10.1139/H09-096     Document Type: Article

References (50)

1. Adnot, S., Desmier, M., Ferry, N., Hanoune, J., and Sevenet, T. 1982. Forskolin (a powerful inhibitor of human platelet aggregation). Biochem. Pharmacol. 31(24): 4071-4074. doi:10.1016/0006-2952(82)90659-1. PMID:6818975.
2. Baum, J.I., O'Connor, J.C., Seyler, J.E., Anthony, T.G., Freund, G.G., and Layman, D.K. 2005. Leucine reduces the duration of insulin-induced PI 3-kinase activity in rat skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 288(1): E86-E91. doi:10.1152/ajpendo.00272.2004. PMID:15339747.
3. Bodine, S.C., Stitt, T.N., Gonzalez, M., Kline, W.O., Stover, G.L., Bauerlein, R., et al. 2001. Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat. Cell Biol. 3(11): 1014-1019. doi:10.1038/ncb1101-1014. PMID:11715023.
4. Bolster, D.R., Jefferson, L.S., and Kimball, S.R. 2004. Regulation of protein synthesis associated with skeletal muscle hypertrophy by insulin-, amino acid- and exercise-induced signalling. Proc. Nutr. Soc. 63(2): 351-356. doi:10.1079/PNS2004355. PMID: 15294054.
5. Bristow, M.R., Ginsburg, R., Strosberg, A., Montgomery, W., and Minobe, W. 1984. Pharmacology and inotropic potential of forskolin in the human heart. J. Clin. Invest. 74(1): 212-223. doi:10.1172/JCI111404. PMID:6330174.
6. Brozinick, J.T., Jr., and Birnbaum, M.J. 1998. Insulin, but not contraction, activates Akt/PKB in isolated rat skeletal muscle. J. Biol. Chem. 273(24): 14679-14682. doi:10.1074/jbc.273.24.14679. PMID:9614064.
7. Carini, R., Grazia De Cesaris, M., Splendore, R., Baldanzi, G., Nitti, M.P., Alchera, E., et al. 2004. Role of phosphatidylinositol 3-kinase in the development of hepatocyte preconditioning. Gastroenterology, 127(3): 914-923. doi:10.1053/j.gastro.2004.06.018. PMID:15362046.
8. Cass, L.A., Summers, S.A., Prendergast, G.V., Backer, J.M., Birnbaum, M.J., and Meinkoth, J.L. 1999. Protein kinase A-dependent and independent signaling pathways contribute to cyclic AMP-stimulated proliferation. Mol. Cell. Biol. 19(9): 5882-5891. PMID:10454535.
9. Deldicque, L., Theisen, D., and Francaux, M. 2005. Regulation of mTOR by amino acids and resistance exercise in skeletal muscle. Eur. J. Appl. Physiol. 94(1-2): 1-10. doi:10.1007/s00421-004-1255-6. PMID:15702344.
10. Filippa, N., Sable, C.L., Filloux, C., Hemmings, B., and Van Obberghen, E. 1999. Mechanism of protein kinase B activation by cyclic AMP-dependent protein kinase. Mol. Cell. Biol. 19(7): 4989-5000. PMID:10373549.
11. Foulstone, E., Prince, S., Zaccheo, O., Burns, J.L., Harper, J., Jacobs, C., et al. 2005. Insulin-like growth factor ligands, receptors, and binding proteins in cancer. J. Pathol. 205(2): 145-153. doi:10.1002/path.1712. PMID:15641016.
12. Gesta, S., Lolméde, K., Daviaud, D., Berlan, M., Bouloumié, A., Lafontan, M., et al. 2003. Culture of human adipose tissue explants leads to profound alteration of adipocyte gene expression. Horm. Metab. Res. 35(3): 158-163. doi:10.1055/s-2003-39070. PMID:12734776.
13. Godard, M.P., Johnson, B.A., and Richmond, S.R. 2005. Body composition and hormonal adaptations associated with forskolin consumption in overweight and obese men. Obes. Res. 13(8): 1335-1343. doi:10.1038/oby.2005.162. PMID:16129715.
14. Godinho, R.O., and Costa, V.L., Jr. 2003. Regulation of intracellular cyclic AMP in skeletal muscle cells involves the efflux of cyclic nucleotide to the extracellular compartment. Br. J. Pharmacol. 138: 995-1003. doi:10.1038/sj.bjp.0705130. PMID: 12642402.
15. González, A., Aranda, E., Mezzano, D., and Garrido, J. 1983. Effects of diterpene forskolin on the release reaction and protein phosphorylation of human platelets. Cell Biochem. Funct. 1(3): 179-185. doi:10.1002/cbf.290010311. PMID:6088107.
16. Graves, L.M., Bornfeldt, K.E., Argast, G.M., Krebs, E.G., Kong, X., Lin, T.A., and Lawrence, J.C., Jr. 1995. cAMP- and rapamycin-sensitive regulation of the association of eukaryotic initiation factor 4E and the translational regulator PHAS-I in aortic smooth muscle cells. Proc. Natl. Acad. Sci. U.S.A. 92(16): 7222-7226. doi:10.1073/pnas.92.16.7222. PMID:7638171.
17. Hahn-Windgassen, A., Nogueira, V., Chen, C.C., Skeen, J.E., Sonenberg, N., and Hay, N. 2005. Akt activates the mammalian target of rapamycin by regulating cellular ATP level and AMPK activity. J. Biol. Chem. 280(37): 32081-32089. doi:10.1074/jbc. M502876200. PMID:16027121.
18. Iijima, Y., Laser, M., Shiraishi, H., Willey, C.D., Sundaravadivel, B., Xu, L., et al. 2002. c-Raf/MEK/ERK pathway controls protein kinase C-mediated p70S6K activation in adult cardiac muscle cells. J. Biol. Chem. 277(25): 23065-23075. doi:10.1074/jbc.M200328200. PMID:11940578.
19. Kim, S., Jee, K., Kim, D., Koh, H., and Chung, J. 2001. Cyclic AMP inhibits Akt activity by blocking the membrane localization of PDK1. J. Biol. Chem. 276(16): 12864-12870. doi:10.1074/jbc.M001492200. PMID:11278269.
20. Kimball, S.R., and Jefferson, L.S. 2004. Molecular mechanisms through which amino acids mediate signaling through the mammalian target of rapamycin. Curr. Opin. Clin. Nutr. Metab. Care, 7(1): 39-44. doi:10.1097/00075197-200401000-00008. PMID: 15090902.
21. Kohn, A.D., Summers, S.A., Birnbaum, M.J., and Roth, R.A. 1996. Expression of a constitutively active Akt Ser/Thr kinase in 3T3-L1 adipocytes stimulates glucose uptake and glucose transporter 4 translocation. J. Biol. Chem. 271(49): 31372-31378. doi:10.1074/jbc.271.49.31372. PMID:8940145.
22. Kwon, G., Marshall, C.A., Pappan, K.L., Remedi, M.S., and McDaniel, M.L. 2004. Signaling elements involved in the metabolic regulation of mTOR by nutrients, incretins, and growth factors in islets. Diabetes, 53(Suppl. 3): S225-S232. doi:10.2337/diabetes.53.suppl_3.S225. PMID:15561916.
23. Latres, E., Amini, A.R., Amini, A.A., Griffiths, J., Martin, F.J., Wei, Y., et al. 2005. Insulin-like growth factor-1 (IGF-1) inversely regulates atrophy-induced genes via the phosphatidylinositol 3-kinase/Akt/mammalian target of rapamycin (PI3K/Akt/mTOR) pathway. J. Biol. Chem. 280(4): 2737-2744. doi:10.1074/jbc.M407517200. PMID:15550386.
24. Lawrence, J.C., Jr. 2001. mTOR-dependent control of skeletal muscle protein synthesis. Int. J. Sport Nutr. Exerc. Metab. 11(Suppl): S177-S185. PMID:11915918.
25. Lécureuil, C., Tesseraud, S., Kara, E., Martinat, N., Sow, A., Fontaine, I., et al. 2005. Follicle-stimulating hormone activates p70 ribosomal protein S6 kinase by protein kinase A-mediated dephosphorylation of Thr 421/Ser 424 in primary Sertoli cells. Mol. Endocrinol. 19(7): 1812-1820. doi:10.1210/me.2004-0289. PMID:15774499.
26. Li, Z., Dong, X., Wang, Z., Liu, W., Deng, N., Ding, N., et al. 2005. Regulation of PTEN by Rho small GTPases. Nat. Cell Biol. 7(4): 399-404. doi:10.1038/ncb1236. PMID:15793569.
27. Litosch, I., Hudson, T.H., Mills, I., Li, S.Y., and Fain, J.N. 1982. Forskolin as an activator of cyclic AMP accumulation and lipolysis in rat adipocytes. Mol. Pharmacol. 22(1): 109-115. PMID: 6289066.
28. Machida, K., Inoue, H., Matsumoto, K., Tsuda, M., Fukuyama, S., Koto, H., et al. 2005. Activation of PI3K-Akt pathway mediates antiapoptotic effects of beta-adrenergic agonist in airway eosinophils. Am. J. Physiol. Lung Cell. Mol. Physiol. 288(5): L860-L867. doi:10.1152/ajplung.00131.2004. PMID:15618457.
29. Mei, F.C., Qiao, J., Tsygankova, O.M., Meinkoth, J.L., Quilliam, L.A., and Cheng, X. 2002. Differential signaling of cyclic AMP: opposing effects of exchange protein directly activated by cyclic AMP and cAMP-dependent protein kinase on protein kinase B activation. J. Biol. Chem. 277(13): 11497-11504. doi:10.1074/jbc.M110856200. PMID:11801596.
30. Meriane, M., Roux, P., Primig, M., Fort, P., and Gauthier-Rouviére, C. 2000. Critical activities of Rac1 and Cdc42Hs in skeletal myogenesis: antagonistic effects of JNK and p38 pathways. Mol. Biol. Cell, 11(8): 2513-2528. PMID:10930450.
31. Metzger, H., and Lindner, E. 1981. The positive inotropic-acting forskolin, a potent adenylate cyclase activator. Arzneimittelforschung, 31(8): 1248-1250. PMID:7197529.
32. Morisco, C., Condorelli, G., Trimarco, V., Bellis, A., Marrone, C., Condorelli, G., et al. 2005. Akt mediates the cross-talk between beta-adrenergic and insulin receptors in neonatal cardiomyocytes. Circ. Res. 96(2): 180-188. doi:10.1161/01.RES.0000152968.71868.c3. PMID:15591229.
33. Parkington, J.D., Siebert, A.P., LeBrasseur, N.K., and Fielding, R.A. 2003. Differential activation of mTOR signaling by contractile activity in skeletal muscle. Am. J. Physiol. Regul. Integr. Comp. Physiol. 285(5): R1086-R1090. PMID:12881204.
34. Perez, V., Bouschet, T., Fernandez, C., Bockaert, J., and Journot, L. 2005. Dynamic reorganization of the astrocyte actin cytoskeleton elicited by cAMP and PACAP: a role for phosphatidylInositol 3-kinase inhibition. Eur. J. Neurosci. 21(1): 26-32. doi:10.1111/j.1460-9568.2004.03845.x. PMID:15654840.
35. Pieske, B., Trost, S., Schütt, K., Minami, K., Just, H., and Hasenfuss, G. 1998. Influence of forskolin on the forcefrequency behavior in nonfailing and end-stage failing human myocardium. Basic Res. Cardiol. 93(Suppl. 1): 66-75. doi:10.1007/s003950050222. PMID:9833133.
36. Reuveny, M., Heller, H., and Bengal, E. 2004. RhoA controls myoblast survival by inducing the phosphatidylinositol 3-kinase-Akt signaling pathway. FEBS Lett. 569(1-3): 129-134. doi:10.1016/j.febslet.2004.05.035. PMID:15225621.
37. Roberts, S.J., and Summers, R.J. 1998. Cyclic AMP accumulation in rat soleus muscle: stimulation by beta2- but not beta3-adrenoceptors. Eur. J. Pharmacol. 348(1): 53-60. doi:10.1016/S0014-2999(98)00021-1. PMID:9650831.
38. Rommel, C., Bodine, S.C., Clarke, B.A., Rossman, R., Nunez, L., Stitt, T.N., et al. 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(11): 1009-1013. doi:10.1038/ncb1101-1009. PMID:11715022.
39. Sable, C.L., Filippa, N., Hemmings, B., and Van Obberghen, E. 1997. cAMP stimulates protein kinase B in a Wortmannin-insensitive manner. FEBS Lett. 409(2): 253-257. doi:10.1016/S0014-5793(97)00518-8. PMID:9202156.
40. Sakamoto, K., Hirshman, M.F., Aschenbach, W.G., and Goodyear, L.J. 2002. Contraction regulation of Akt in rat skeletal muscle. J. Biol. Chem. 277(14): 11910-11917. doi:10.1074/jbc.M112410200. PMID:11809761.
41. Seamon, K.B., Padgett, W., and Daly, J.W. 1981. Forskolin: unique diterpene activator of adenylate cyclase in membranes and in intact cells. Proc. Natl. Acad. Sci. U.S.A. 78(6): 3363-3367. doi:10.1073/pnas.78.6.3363. PMID:6267587.
42. Sonenberg, N., and Gingras, A.C. 1998. The mRNA 5' cap-binding protein eIF4E and control of cell growth. Curr. Opin. Cell Biol. 10(2): 268-275. doi:10.1016/S0955-0674(98)80150-6. PMID: 9561852.
43. Song, Y.H., Godard, M., Li, Y., Richmond, S.R., Rosenthal, N., and Delafontaine, P. 2005. Insulin-like growth factor I-mediated skeletal muscle hypertrophy is characterized by increased mTOR-p70S6K signaling without increased Akt phosphorylation. J. Investig. Med. 53(3): 135-142. doi:10.2310/6650.2005.00309. PMID:15921033.
44. Stitt, T.N., Drujan, D., Clarke, B.A., Panaro, F., Timofeyva, Y., Kline, W.O., et al. 2004. The IGF-1/PI3K/Akt pathway prevents expression of muscle atrophy-induced ubiquitin ligases by inhibiting FOXO transcription factors. Mol. Cell, 14(3): 395-403. doi:10.1016/S1097-2765(04)00211-4. PMID:15125842.
45. Takai, Y., Sasaki, T., and Matozaki, T. 2001. Small GTP-binding proteins. Physiol. Rev. 81(1): 153-208. PMID:11152757. Tokunaga, C., Yoshino, K., and Yonezawa, K. 2004. mTOR integrates amino acid- and energy-sensing pathways. Biochem. Biophys. Res. Commun. 313(2): 443-446. doi:10.1016/j.bbrc.2003. 07.019. PMID:14684182.
46. Tokunaga, C., Yoshino, K., and Yonezawa, K. 2004. mTOR integrates amino acid- and energy-sensing pathways. Biochem. Biophys. Res. Commun. 313(2): 443-446. doi:10.1016/j.bbrc.2003.07.019. PMID:14684182.
47. Vanhaesebroeck, B., and Alessi, D.R. 2000. The PI3K-PDK1 connection: more than just a road to PKB. Biochem. J. 346(Pt. 3): 561-576. doi:10.1042/0264-6021:3460561. PMID:10698680.
48. Williamson, D.L., Kubica, N., Kimball, S.R., and Jefferson, L.S. 2006. Exercise-induced alterations in extracellular signal-regulated kinase 1/2 and mammalian target of rapamycin (mTOR) signalling to regulatory mechanisms of mRNA translation in mouse muscle. J. Physiol. 573(Pt. 2): 497-510. doi:10.1113/jphysiol.2005.103481. PMID:16543272.
49. Yarasheski, K.E. 2003. Exercise, aging, and muscle protein metabolism. J. Gerontol. A Biol. Sci. Med. Sci. 58(10): M918-M922. PMID:14570859.
50. Zhou, B., Li, F., Chen, H., and Song, J. 2005. The modulation of apoptosis by cyclic AMP involves Akt and epidermal growth factor receptor. Int. J. Biochem. Cell Biol. 37(7): 1483-1495. doi:10.1016/j.biocel.2005.02.012. PMID:15833279.