Prostaglandin F2α stimulates PI3K/ERK/mTOR signaling and skeletal myotube hypertrophy

American Journal of Physiology - Cell Physiology

Volumn 300, Issue 3, 2011, Pages

  Markworth, James F ^a   Cameron Smith, David ^a  

^a DEAKIN UNIVERSITY   (Australia)

Author keywords

C2C12; Cyclooxygenase; F prostanoid receptor; Muscle growth; Nonsteroidal anti inflammatory drugs

Indexed keywords

11 FLUORO 9,15 DIHYDROXY 15 (2 INDANYL) 16,17,18,19,20 PENTANORPROSTA 5,13 DIENOIC ACID; 2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 2 MORPHOLINO 8 PHENYLCHROMONE; ARACHIDONIC ACID; FLUPROSTENOL; INITIATION FACTOR 4G; MAMMALIAN TARGET OF RAPAMYCIN; MAMMALIAN TARGET OF RAPAMYCIN INHIBITOR; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHOSPHATIDYLINOSITOL 3 KINASE; PROSTAGLANDIN; PROSTAGLANDIN F2 ALPHA; PROSTAGLANDIN RECEPTOR BLOCKING AGENT; PROSTAGLANDIN SYNTHASE; PROSTANOID RECEPTOR; PROTEIN KINASE B; UNCLASSIFIED DRUG; MITOGEN ACTIVATED PROTEIN KINASE; MTOR PROTEIN, MOUSE; TARGET OF RAPAMYCIN KINASE;

ANIMAL TISSUE; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; MOUSE; MUSCLE GROWTH; MUSCLE HYPERTROPHY; MUSCLE REGENERATION; MYOTUBE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; ANIMAL; CELL DIFFERENTIATION; CELL LINE; CELL MOTION; ENZYMOLOGY; HYPERTROPHY; METABOLISM; MYOBLAST; PATHOLOGY; PHYSIOLOGY;

EUKARYOTA; MAMMALIA;

ANIMALS; CELL DIFFERENTIATION; CELL LINE; CELL MOVEMENT; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HYPERTROPHY; MAP KINASE SIGNALING SYSTEM; MICE; MUSCLE FIBERS, SKELETAL; MUSCLE, SKELETAL; MYOBLASTS; PHOSPHATIDYLINOSITOL 3-KINASES; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES;

EID: 79952173258     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00549.2009     Document Type: Article

References (63)

1. Abbott KL, Friday BB, Thaloor D, Murphy TJ, Pavlath GK. Activation and cellular localization of the cyclosporine A-sensitive transcription factor NF-AT in skeletal muscle cells. Mol Biol Cell 9: 2905-2916, 1998. (Pubitemid 28473668)
2. Adams JW, Migita DS, Yu MK, Young R, Hellickson MS, Castro-Vargas FE, Domingo JD, Lee PH, Bui JS, Henderson SA. Prostaglandin F2 alpha stimulates hypertrophic growth of cultured neonatal rat ventricular myocytes. J Biol Chem 271: 1179-1186, 1996.
3. Arvisais EW, Romanelli A, Hou X, Davis JS. AKT-independent phosphorylation of TSC2 and activation of mTOR and ribosomal protein S6 kinase signaling by prostaglandin F2alpha. J Biol Chem 281: 26904-26913, 2006. (Pubitemid 44401719)
4. Avruch J, Long X, Ortiz-Vega S, Rapley J, Papageorgiou A, Dai N. Amino acid regulation of TOR complex 1. Am J Physiol Endocrinol Metab 296: E592-E602, 2009.
5. Bodine SC, Stitt TN, Gonzalez M, Kline WO, Stover GL, Bauerlein R, Zlotchenko E, Scrimgeour A, Lawrence JC, Glass D. J, Yancopoulos GD. Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nature Cell Biol 3: 1014-1019, 2001. (Pubitemid 34428747)
6. Bolster DR, Vary TC, Kimball SR, Jefferson LS. Leucine regulates translation initiation in rat skeletal muscle via enhanced eIF4G phosphorylation. J Nutr 134: 1704-1710, 2004. (Pubitemid 38886558)
7. Bondesen BA, Mills ST, Kegley KM, Pavlath GK. The COX-2 pathway is essential during early stages of skeletal muscle regeneration. Am J Physiol Cell Physiol 287: C475-C483, 2004. (Pubitemid 38955239)
8. Bondesen BA, Mills ST, Pavlath GK. The COX-2 pathway regulates growth of atrophied muscle via multiple mechanisms. Am J Physiol Cell Physiol 290: C1651-C1659, 2006. (Pubitemid 43830805)
9. Brunn GJ, Williams J, Sabers C, Wiederrecht G, Lawrence JC, Jr., Abraham RT. Direct inhibition of the signaling functions of the mammalian target of rapamycin by the phosphoinositide 3-kinase inhibitors, wortmannin and LY294002. EMBO J 15: 5256-5267, 1996. (Pubitemid 26336209)
10. Clemmons DR. Role of IGF-I in skeletal muscle mass maintenance. Trends Endocrinol Metab 20: 349-356, 2009.
11. Davies P, Bailey PJ, Goldenberg MM, Ford-Hutchinson AW. The role of arachidonic acid oxygenation products in pain and inflammation. Annual Rev Immunol 2: 335-357, 1984.
12. Dorn GW, 2nd, Becker MW, Davis MG. Dissociation of the contractile and hypertrophic effects of vasoconstrictor prostanoids in vascular smooth muscle. J Biol Chem 267: 24897-24905, 1992.
13. Erbay E, Chen J. The mammalian target of rapamycin regulates C2C12 myogenesis via a kinase-independent mechanism. J Biol Chem 276: 36079-36082, 2001.
14. Erbay E, Park I-H, Nuzzi PD, Schoenherr CJ, Chen J. IGF-II transcription in skeletal myogenesis is controlled by mTOR and nutrients. J Cell Biol 163: 931-936, 2003. (Pubitemid 37541870)
15. Fluckey JD, Knox M, Smith L, Dupont-Versteegden EE, Gaddy D, Tesch PA, Peterson CA. Insulin-facilitated increase of muscle protein synthesis after resistance exercise involves a MAP kinase pathway. Am J Physiol Endocrinol Metab 290: E1205-E1211, 2006. (Pubitemid 43847905)
16. Frost RA, Lang CH. Protein kinase B/Akt: a nexus of growth factor and cytokine signaling in determining muscle mass. J Appl Physiol 103: 378-387, 2007.
17. Fukuyama K, Ichiki T, Ono H, Tokunou T, Iino N, Masuda S, Ohtsubo H, Takeshita A. cAMP-response element-binding protein mediates prostaglandin F2alpha-induced hypertrophy of vascular smooth muscle cells. Biochem Biophys Res Commun 338: 910-918, 2005. (Pubitemid 41597728)
18. Griffin BW, Klimko P, Crider JY, Sharif NA. AL-8810: a novel prostaglandin F2 alpha analog with selective antagonist effects at the prostaglandin F2 alpha (FP) receptor. J Pharmacol Exper Therap 290: 1278-1284, 1999. (Pubitemid 29400270)
19. Haddad F, Adams GR. Inhibition of MAP/ERK kinase prevents IGF-Iinduced hypertrophy in rat muscles. J Appl Physiol 96: 203-210, 2004. (Pubitemid 38032002)
20. Hornberger TA, Stuppard R, Conley KE, Fedele MJ, Fiorotto ML, Chin ER, Esser KA. Mechanical stimuli regulate rapamycin-sensitive signalling by a phosphoinositide 3-kinase-, protein kinase B- and growth factor-independent mechanism. Biochem J 380: 795-804, 2004. (Pubitemid 38850521)
21. Hornberger TA, Sukhija KB, Chien S. Regulation of mTOR by mechanically induced signaling events in skeletal muscle. Cell Cycle 5: 1391-1396, 2006. (Pubitemid 44153645)
22. Horsley V, Friday BB, Matteson S, Kegley KM, Gephart J, Pavlath GK. Regulation of the growth of multinucleated muscle cells by an NFATC2-dependent pathway. J Cell Biol 153: 329-338, 2001. (Pubitemid 34280219)
23. Horsley V, Pavlath GK. Prostaglandin F2(alpha) stimulates growth of skeletal muscle cells via an NFATC2-dependent pathway. J Cell Biol 161: 111-118, 2003. (Pubitemid 36459084)
24. Iijima Y, Laser M, Shiraishi H, Willey CD, Sundaravadivel B, Xu L, McDermott PJ, Kuppuswamy D. c-Raf/MEK/ERK pathway controls protein kinase C-mediated p70S6K activation in adult cardiac muscle cells. J Biol Chem 277: 23065-23075, 2002. (Pubitemid 34967293)
25. Jansen KM, Pavlath GK. Prostaglandin F2alpha promotes muscle cell survival and growth through upregulation of the inhibitor of apoptosis protein BRUCE. Cell Death Different 15: 1619-1628, 2008.
26. Katsuyama M, Fan C, Yabe-Nishimura C. NADPH oxidase is involved in prostaglandin F2alpha-induced hypertrophy of vascular smooth muscle cells: induction of NOX1 by PGF2alpha. J Biol Chem 277: 13438-13442, 2002. (Pubitemid 34967938)
27. Kimball SR. Interaction between the AMP-activated protein kinase and mTOR signaling pathways. Med Sci Sports Exer 38: 1958-1964, 2006.
28. Kimball SR, Horetsky RL, Jefferson LS. Signal transduction pathways involved in the regulation of protein synthesis by insulin in L6 myoblasts. Am J Physiol Cell Physiol 274: C221-C228, 1998.
29. Kunapuli P, Lawson JA, Rokach JA, Meinkoth JL, FitzGerald GA. Prostaglandin F2alpha (PGF2alpha) and the isoprostane, 8, 12-iso-isoprostane F2alpha-III, induce cardiomyocyte hypertrophy. Differential activation of downstream signaling pathways. J Biol Chem 273: 22442-22452, 1998.
30. Lai J, Jin H, Yang R, Winer J, Li W, Yen R, King KL, Zeigler F, Ko A, Cheng J, Bunting S, Paoni NF. Prostaglandin F2 alpha induces cardiac myocyte hypertrophy in vitro and cardiac growth in vivo. Am J Physiol Heart Circ Physiol 271: H2197-H2208, 1996.
31. Mendias CL, Tatsumi R, Allen RE. Role of cyclooxygenase-1 and -2 in satellite cell proliferation, differentiation, and fusion. Muscle Nerve 30: 497-500, 2004. (Pubitemid 39288155)
32. Mitchell PO, Pavlath GK. A muscle precursor cell-dependent pathway contributes to muscle growth after atrophy. Am J Physiol Cell Physiol 281: C1706-C1715, 2001.
33. Novak ML, Billich W, Smith SM, Sukhija KB, McLoughlin TJ, Hornberger TA, Koh TJ. COX-2 inhibitor reduces skeletal muscle hypertrophy in mice. Am J Physiol Regul Integr Comp Physiol 296: R1132-R1139, 2009.
34. Ocklind A, Lake S, Krook K, Hallin I, Nistér M, Westermark B. Localization of the prostaglandin F2 alpha receptor in rat tissues. Prostaglandins Leukot Essent Fatty Acids 57: 527-532, 1997. (Pubitemid 27522495)
35. Park I-H, Chen J. Mammalian target of rapamycin (mTOR) signaling is required for a late-stage fusion process during skeletal myotube maturation. J Biol Chem 280: 32009-32017, 2005. (Pubitemid 41291952)
36. Park I-H, Erbay E, Nuzzi P, Chen J. Skeletal myocyte hypertrophy requires mTOR kinase activity and S6K1. Exp Cell Res 309: 211-219, 2005. (Pubitemid 41199876)
37. Pavlath GK, Horsley V. Cell fusion in skeletal muscle- central role of NFATC2 in regulating muscle cell size. Cell Cycle 2: 420-423, 2003.
38. Plaisance I, Morandi C, Murigande C, Brink M. TNF-alpha increases protein content in C2C12 and primary myotubes by enhancing protein translation via the TNF-R1, PI3K, and MEK. Am J Physiol Endocrinol Metab 294: E241-E250, 2008. (Pubitemid 351231450)
39. Rao GN, Madamanchi NR, Lele M, Gadiparthi L, Gingras AC, Eling TE, Sonenberg N. A potential role for extracellular signal-regulated kinases in prostaglandin F2alpha-induced protein synthesis in smooth muscle cells. J Biol Chem 274: 12925-12932, 1999.
40. Rennie MJ. Exercise- and nutrient-controlled mechanisms involved in maintenance of the musculoskeletal mass. Biochem Soc Trans 35: 1302-1305, 2007. (Pubitemid 350206485)
41. Rice KM, Uddemarri S, Desai DH, Morrison RG, Harris R, Wright GL, Blough ER. PGF2alpha-associated vascular smooth muscle hypertrophy is ROS dependent and involves the activation of mTOR, p70S6k, and PTEN. Prostaglandins Other Lipid Mediat 85: 49-57, 2008.
42. Rodemann HP, Goldberg AL. Arachidonic acid, prostaglandin E2 and F2 alpha influence rates of protein turnover in skeletal and cardiac muscle. J Biol Chem 257: 1632-1638, 1982. (Pubitemid 12157112)
43. Rommel C, Bodine SC, Clarke BA, Rossman R, Nunez L, Stitt TN, Yancopoulos GD, Glass DJ. Mediation of IGF-1-induced skeletal myotube hypertrophy by PI(3)K/Akt/mTOR and PI(3)K/Akt/GSK3 pathways. Nature Cell Biol 3: 1009-1013, 2001. (Pubitemid 34428746)
44. Roux PP, Ballif BA, Anjum R, Gygi SP, Blenis J. Tumor-promoting phorbol esters and activated Ras inactivate the tuberous sclerosis tumor suppressor complex via p90 ribosomal S6 kinase. Proc Natl Acad Sci USA 101: 13489-13494, 2004. (Pubitemid 39238430)
45. Roux PP, Shahbazian D, Vu H, Holz MK, Cohen MS, Taunton J, Sonenberg N, Blenis J. RAS/ERK signaling promotes site-specific ribosomal protein S6 phosphorylation via RSK and stimulates cap-dependent translation. J Biol Chem 282: 14056-14064, 2007. (Pubitemid 47100467)
46. Shen W, Li Y, Tang Y, Cummins J, Huard J. NS-398, a cyclooxygenase-2- specific inhibitor, delays skeletal muscle healing by decreasing regeneration and promoting fibrosis. Am J Pathol 167: 1105-1117, 2005. (Pubitemid 41416261)
47. Shen W, Li Y, Zhu J, Schwendener R, Huard J. Interaction between macrophages, TGF-beta1, and the COX-2 pathway during the inflammatory phase of skeletal muscle healing after injury. J Cell Physiol 214: 405-412, 2008. (Pubitemid 350308997)
48. Shen W, Prisk V, Li Y, Foster W, Huard J. Inhibited skeletal muscle healing in cyclooxygenase-2 gene-deficient mice: the role of PGE2 and PGF2alpha. J Appl Physiol 101: 1215-1221, 2006. (Pubitemid 44497566)
49. Shi H, Scheffler JM, Zeng C, Pleitner JM, Hannon KM, Grant AL, Gerrard DE. Mitogen-activated protein kinase signaling is necessary for the maintenance of skeletal muscle mass. Am J Physiol Cell Physiol 296: C1040-C1048, 2009.
50. Shi H, Zeng C, Ricome A, Hannon KM, Grant AL, Gerrard DE. Extracellular signal-regulated kinase pathway is differentially involved in β-agonist-induced hypertrophy in slow and fast muscles. Am J Physiol Cell Physiol 292: C1681-C1689, 2007. (Pubitemid 47080548)
51. Shu L, Zhang X, Houghton PJ. Myogenic differentiation is dependent on both the kinase function and the N-terminal sequence of mammalian target of rapamycin. J Biol Chem 277: 16726-16732, 2002. (Pubitemid 34967693)
52. Soltow QA, Betters JL, Sellman JE, Lira VA, Long JH, Criswell DS. Ibuprofen inhibits skeletal muscle hypertrophy in rats. Med Sci Sports Exer 38: 840-846, 2006.
53. Suleyman H, Demircan B, Karagoz Y. Anti-inflammatory and side effects of cyclooxygenase inhibitors. Pharmacology 59: 247-258, 2007. (Pubitemid 47299726)
54. Trappe TA, Fluckey JD, White F, Lambert CP, Evans WJ. Skeletal muscle PGF(2)(alpha) and PGE(2) in response to eccentric resistance exercise: influence of ibuprofen acetaminophen. J Clin Endocrinol Metab 86: 5067-5070, 2001. (Pubitemid 33020565)
55. Trappe TA, White F, Lambert CP, Cesar D, Hellerstein M, Evans WJ. Effect of ibuprofen and acetaminophen on postexercise muscle protein synthesis. Am J Physiol Endocrinol Metab 282: E551-E556, 2002. (Pubitemid 34654769)
56. Tsuboi K, Sugimoto Y, Ichikawa A. Prostanoid receptor subtypes. Prostaglandins Other Lipid Med 68-69: 535-556, 2002. (Pubitemid 35247419)
57. Vandenburgh HH, Hatfaludy S, Sohar I, Shansky J. Stretch-induced prostaglandins and protein turnover in cultured skeletal muscle. Am J Physiol Cell Physiol 259: C232-C240, 1990. (Pubitemid 20254466)
58. Vane JR. Inhibition of prostaglandin synthesis as a mechanism of action for aspirin-like drugs. Nature New Biol 231: 232-235, 1971.
59. Vary TC, Anthony JC, Jefferson LS, Kimball SR, Lynch CJ. Rapamycin blunts nutrient stimulation of eIF4G, but not PKCepsilon phosphorylation, in skeletal muscle. Am J Physiol Endocrinol Metab 293: E188-E196, 2007. (Pubitemid 47105932)
60. Wackerhage H, Ratkevicius A. Signal transduction pathways that regulate muscle growth. Essays Biochem 44: 99-108, 2008.
61. Willett M, Cowan JL, Vlasak M, Coldwell MJ, Morley SJ. Inhibition of mammalian target of rapamycin (mTOR) signalling in C2C12 myoblasts prevents myogenic differentiation without affecting the hyperphosphorylation of 4E-BP1. Cell Signal 21: 1504-1512, 2009.
62. Williams R, Berndt A, Miller S, Hon W-C, Zhang X. Form and flexibility in phosphoinositide 3-kinases. Biochem Soc Trans 37: 615-626, 2009.
63. Xu W, Chou CL, Sun H, Fujino H, Chen M, Regan JW. FP prostanoid receptor-mediated induction of the expression of early growth response factor-1 by activation of a Ras/Raf/mitogen-activated protein kinase signaling cascade. Mol Pharmacol 73: 111-118, 2008. (Pubitemid 350294202)