Ankrd2/ARPP is a novel Akt2 specific substrate and regulates myogenic differentiation upon cellular exposure to H 2O 2

Molecular Biology of the Cell

Volumn 22, Issue 16, 2011, Pages 2946-2956

  Cenni, Vittoria ^a,b   Bavelloni, Alberto ^b   Beretti, Francesca ^c   Tagliavini, Francesca ^b,d   Manzoli, Lucia ^d   Lattanzi, Giovanna ^a   Maraldi, Nadir M ^a,b   Cocco, Lucio ^d   Marmiroli, Sandra ^a,c  

^a CNR   (Italy)

^b RIZZOLI ORTHOPAEDIC INSTITUTE   (Italy)

^c UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

^d UNIVERSITY OF BOLOGNA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANKYRIN; ANKYRIN REPEART DOMAIN PROTEIN 2; ENZYME ANTIBODY; HYDROGEN PEROXIDE; PROTEIN KINASE B; PROTEIN KINASE B BETA; RECOMBINANT ENZYME; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL REGENERATION; CELL SURVIVAL; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ASSAY; ENZYME PHOSPHORYLATION; ENZYME SPECIFICITY; ENZYME SUBSTRATE; GENE SILENCING; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MUSCLE CELL; MUSCLE DEVELOPMENT; MYOBLAST; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; TRANSCRIPTION REGULATION;

ANIMALS; CELL DIFFERENTIATION; CELL NUCLEUS; HUMANS; HYDROGEN PEROXIDE; MICE; MUSCLE DEVELOPMENT; MUSCLE PROTEINS; MYOBLASTS, SKELETAL; NUCLEAR PROTEINS; OXIDANTS; OXIDATIVE STRESS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN TRANSPORT; PROTO-ONCOGENE PROTEINS C-AKT; REPRESSOR PROTEINS; SERINE;

MURINAE;

EID: 80051675468     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E10-11-0928     Document Type: Article

References (46)

1. Al-Khalili L, Kramer D, Wretenberg P, Krook A (2004). Human skeletal muscle cell differentiation is associated with changes in myogenic markers and enhanced insulin-mediated MAPK and PKB phosphorylation. Acta Physiol Scand 180, 395-403. (Pubitemid 38496699)
2. Alessi DR, Caudwell FB, Andjelkovic M, Hemmings BA, Cohen P (1996). Molecular basis for the substrate specificity of protein kinase B; comparison with MAPKAP kinase-1 and p70 S6 kinase. FEBS Lett 399, 333-338. (Pubitemid 26426877)
3. Andjelkovic M, Alessi DR, Meier R, Fernandez A, Lamb NJ, Frech M, Cron P, Cohen P, Lucocq JM, Hemmings BA (1997). Role of translocation in the activation and function of protein kinase B. J Biol Chem 272, 31515-31524. (Pubitemid 28013293)
4. Ardite E, Barbera JA, Roca J, Fernandez-Checa JC (2004). Glutathione depletion impairs myogenic differentiation of murine skeletal muscle C2C12 cells through sustained NF-kappaB activation. Am J Pathol 165, 719-728. (Pubitemid 39129280)
5. Arimura T et al. (2009). Cardiac ankyrin repeat protein gene (ANKRD1) mutations in hypertrophic cardiomyopathy. J Am Coll Cardiol 54, 334-342.
6. Barash IA, Mathew L, Ryan AF, Chen J, Lieber RL (2004). Rapid muscle-specific gene expression changes after a single bout of eccentric contractions in the mouse. Am J Physiol Cell Physiol 286, C355-C364. (Pubitemid 38146359)
7. Bean C, Facchinello N, Faulkner G, Lanfranchi G (2008). The effects of Ankrd2 alteration indicate its involvement in cell cycle regulation during muscle differentiation. Biochim Biophys Acta 1783, 1023-1035.
8. Bellacosa A, Franke TF, Gonzalez-Portal ME, Datta K, Taguchi T, Gardner J, Cheng JQ, Testa JR, Tsichlis PN (1993). Structure, expression and chromosomal mapping of c-akt: relationship to v-akt and its implications. Oncogene 8, 745-754. (Pubitemid 23093139)
9. Bouzakri K, Zachrisson A, Al-Khalili L, Zhang BB, Koistinen HA, Krook A, Zierath JR (2006). siRNA-based gene silencing reveals specialized roles of IRS-1/Akt2 and IRS-2/Akt1 in glucose and lipid metabolism in human skeletal muscle. Cell Metab 4, 89-96. (Pubitemid 43964475)
10. Brazil DP, Yang ZZ, Hemmings BA (2004). Advances in protein kinase B signalling: AKTion on multiple fronts. Trends Biochem Sci 29, 233-242. (Pubitemid 38591317)
11. Brunet A, Park J, Tran H, Hu LS, Hemmings BA, Greenberg ME (2001). Protein kinase SGK mediates survival signals by phosphorylating the forkhead transcription factor FKHRL1 (FOXO3a). Mol Cell Biol 21, 952-965. (Pubitemid 32104742)
12. Cenciarelli C, De Santa F, Puri PL, Mattei E, Ricci L, Bucci F, Felsani A, Caruso M (1999). Critical role played by cyclin D3 in the MyoD-mediated arrest of cell cycle during myoblast differentiation. Mol Cell Biol 19, 5203-5217. (Pubitemid 29289558)
13. Cenni V et al. (2008). Lamin A Ser404 is a nuclear target of Akt phosphorylation in C2C12 cells. J Proteome Res 7, 4727-4735.
14. Cross DA, Alessi DR, Cohen P, Andjelkovich M, Hemmings BA (1995). Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 378, 785-789. (Pubitemid 26004411)
15. Glass DJ (2003). Signalling pathways that mediate skeletal muscle hypertrophy and atrophy. Nat Cell Biol 5, 87-90.
16. Hansen JM, Klass M, Harris C, Csete M (2007). A reducing redox environment promotes C2C12 myogenesis: implications for regeneration in aged muscle. Cell Biol Int 31, 546-553. (Pubitemid 46660641)
17. Heron-Milhavet L, Franckhauser C, Rana V, Berthenet C, Fisher D, Hemmings BA, Fernandez A, Lamb NJ (2006). Only Akt1 is required for proliferation, while Akt2 promotes cell cycle exit through p21 binding. Mol Cell Biol 26, 8267-8280. (Pubitemid 44748563)
18. Hoffman EP, Nader GA (2004). Balancing muscle hypertrophy and atrophy. Nat Med 10, 584-585. (Pubitemid 38796846)
19. Hong F, Larrea MD, Doughty C, Kwiatkowski DJ, Squillace R, Slingerland JM (2008). mTOR-raptor binds and activates SGK1 to regulate p27 phosphorylation. Mol Cell 30, 701-711. (Pubitemid 351815130)
20. Ishiguro N et al. (2002). Carp, a cardiac ankyrin-repeated protein, and its new homologue, Arpp, are differentially expressed in heart, skeletal muscle, and rhabdomyosarcomas. Am J Pathol 160, 1767-1778. (Pubitemid 34525656)
21. Kojic S, Medeot E, Guccione E, Krmac H, Zara I, Martinelli V, Valle G, Faulkner G (2004). The Ankrd2 protein, a link between the sarcomere and the nucleus in skeletal muscle. J Mol Biol 339, 313-325. (Pubitemid 38596951)
22. Konat GW (2003). H2O2-induced higher order chromatin degradation: a novel mechanism of oxidative genotoxicity. J Biosci 28, 57-60.
23. Langen RC, Schols AM, Kelders MC, Van Der Velden JL, Wouters EF, Janssen-Heininger YM (2002). Tumor necrosis factor-alpha inhibits myogenesis through redox-dependent and -independent pathways. Am J Physiol Cell Physiol 283, C714-C721. (Pubitemid 34920304)
24. Lehti M, Kivela R, Komi P, Komulainen J, Kainulainen H, Kyrolainen H (2009). Effects of fatiguing jumping exercise on mRNA expression of titin-complex proteins and calpains. J Appl Physiol 106, 1419-1424.
25. Manning BD, Cantley LC (2007). AKT/PKB signaling: navigating downstream. Cell 129, 1261-1274. (Pubitemid 46962095)
26. Mercurio F, Manning AM (1999). NF-kappaB as a primary regulator of the stress response. Oncogene 18, 6163-6171.
27. Miller MK, Bang ML, Witt CC, Labeit D, Trombitas C, Watanabe K, Granzier H, McElhinny AS, Gregorio CC, Labeit S (2003). The muscle ankyrin repeat proteins: CARP, ankrd2/Arpp and DARP as a family of titin filament-based stress response molecules. J Mol Biol 333, 951-964. (Pubitemid 37324498)
28. Moritz A et al. (2010). Akt-RSK-S6 kinase signaling networks activated by oncogenic receptor tyrosine kinases. Sci Signal 3, ra64.
29. Moulik M et al. (2009). ANKRD1, the gene encoding cardiac ankyrin repeat protein, is a novel dilated cardiomyopathy gene. J Am Coll Cardiol 54, 325-333.
30. Oldham KM, Bowen PE (1998). Oxidative stress in critical care: is antioxidant supplementation beneficial? J Am Diet Assoc 98, 1001-1008. (Pubitemid 28409310)
31. Orzechowski A, Lokociejewska M, Muras P, Hocquette JF (2002). Preconditioning with millimolar concentrations of vitamin C or N-acetylcysteine protects L6 muscle cells insulin-stimulated viability and DNA synthesis under oxidative stress. Life Sci 71, 1793-1808. (Pubitemid 34876696)
32. Proske U, Morgan DL (2001). Muscle damage from eccentric exercise: mechanism, mechanical signs, adaptation and clinical applications. J Physiol 537, 333-345. (Pubitemid 33130492)
33. Rochat A, Fernandez A, Vandromme M, Moles JP, Bouschet T, Carnac G, Lamb NJ (2004). Insulin and wnt1 pathways cooperate to induce reserve cell activation in differentiation and myotube hypertrophy. Mol Biol Cell 15, 4544-4555. (Pubitemid 39299103)
34. Rotwein P, Wilson EM (2009). Distinct actions of Akt1 and Akt2 in skeletal muscle differentiation. J Cell Physiol 219, 503-511.
35. Salsman S, Felts N, Pye QN, Floyd RA, Hensley K (2001). Induction of Akt phosphorylation in rat primary astrocytes by H2O2 occurs upstream of phosphatidylinositol 3-kinase: no evidence for oxidative inhibition of PTEN. Arch Biochem Biophys 386, 275-280. (Pubitemid 32989318)
36. Shaw M, Cohen P, Alessi DR (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, Pt 1241-246.
37. Shomori K et al. (2007). ARPP protein is selectively expressed in renal oncocytoma, but rarely in renal cell carcinomas. Mod Pathol 20, 199-207. (Pubitemid 46422174)
38. Storz P, Toker A (2003). NF-kappaB signaling - an alternate pathway for oxidative stress responses. Cell Cycle 2, 9-10.
39. 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. (Pubitemid 34164031)
40. Tsukamoto Y, Hijiya N, Yano S, Yokoyama S, Nakada C, Uchida T, Matsuura K, Moriyama M (2008). Arpp/Ankrd2, a member of the muscle ankyrin repeat proteins (MARPs), translocates from the I-band to the nucleus after muscle injury. Histochem Cell Biol 129, 55-64. (Pubitemid 350276139)
41. Ushio-Fukai M, Alexander RW, Akers M, Yin Q, Fujio Y, Walsh K, Griendling KK (1999). Reactive oxygen species mediate the activation of Akt/protein kinase B by angiotensin II in vascular smooth muscle cells. J Biol Chem 274, 22699-22704.
42. 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.
43. Wang X, McCullough KD, Franke TF, Holbrook NJ (2000). Epidermal growth factor receptor-dependent Akt activation by oxidative stress enhances cell survival. J Biol Chem 275, 14624-14631. (Pubitemid 30339753)
44. Wilson EM, Rotwein P (2007). Selective control of skeletal muscle differentiation by Akt1. J Biol Chem 282, 5106-5110. (Pubitemid 47093711)
45. Zaccagnini G, Martelli F, Magenta A, Cencioni C, Fasanaro P, Nicoletti C, Biglioli P, Pelicci PG, Capogrossi MC (2007). p66(ShcA) and oxidative stress modulate myogenic differentiation and skeletal muscle regeneration after hind limb ischemia. J Biol Chem 282, 31453-31459. (Pubitemid 350044897)
46. Zhang H, Zha X, Tan Y, Hornbeck PV, Mastrangelo AJ, Alessi DR, Polakiewicz RD, Comb MJ (2002). Phosphoprotein analysis using antibodies broadly reactive against phosphorylated motifs. J Biol Chem 277, 39379-39387. (Pubitemid 35190911)