Abstract
AMP-activated protein kinase α (AMPKα) is a key regulator of energy balance in many model species during hypoxia. In a marine bivalve, the Pacific oyster Crassostrea gigas, we analyzed the protein content of adductor muscle in response to hypoxia during 6 h. In both smooth and striated muscles, the amount of full-length AMP-activated protein kinase α (AMPKα) remained unchanged during hypoxia. However, hypoxia induced a rapid and muscle-specific response concerning truncated isoforms of AMPKα. In the smooth muscle, a truncated isoform of AMPKα was increased from 1 to 6 h of hypoxia, and was linked with accumulation of AKT kinase, a key enzyme of the insulin signaling pathway which controls intracellular glucose metabolism. In this muscle, aerobic metabolism was maintained over the 6 h of hypoxia, as mitochondrial citrate synthase activity remained constant. In contrast, in striated muscle, hypoxia did not induce any significant modification of neither truncated AMPKα nor AKT protein content, and citrate synthase activity was altered after 6 h of hypoxia. Together, our results demonstrate that hypoxia response is specific to muscle type in Pacific oyster, and that truncated AMPKα and AKT proteins might be involved in maintaining aerobic metabolism in smooth muscle. Such regulation might occur in vivo during tidal intervals that cause up to 6 h of hypoxia.
Similar content being viewed by others
References
Akberali HB, Trueman ER (1985) Effects of environmental-stress on marine bivalve mollusks. Adv Mar Biol 22:101–198. doi:10.1016/S0065-2881(08)60051-6
Alessi DR, Andjelkovic M, Caudwell B, Cron P, Morrice N, Cohen P, Hemmings BA (1996) Mechanism of activation of protein kinase B by insulin and IGF-1. EMBO J 15(23):6541–6551
Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25(17):3389–3402. doi:10.1093/nar/25.17.3389
Alvarez-Tejado M, Naranjo-Suarez S, Jimenez C, Carrera AC, Landazuri MO, del Peso L (2001) Hypoxia induces the activation of the phosphatidylinositol 3-kinase/Akt cell survival pathway in PC12 cells: protective role in apoptosis. J Biol Chem 276(25):22368–22374. doi:10.1074/jbc.M011688200
Apfeld J, O’Connor G, McDonagh T, DiStefano PS, Curtis R (2004) The AMP-activated protein kinase AAK-2 links energy levels and insulin-like signals to lifespan in C. elegans. Genes Dev 18(24):3004–3009. doi:10.1101/gad.1255404
Bacca H, Huvet A, Fabioux C, Daniel JY, Delaporte M, Pouvreau S, Van Wormhoudt A, Moal J (2005) Molecular cloning and seasonal expression of oyster glycogen phosphorylase and glycogen synthase genes. Comp Biochem Physiol B Biochem Mol Biol 140(4):635–646. doi:10.1016/j.cbpc.2005.01.005
Beri RK, Marley AE, See CG, Sopwith WF, Aguan K, Carling D, Scott J, Carey F (1994) Molecular cloning, expression and chromosomal localisation of human AMP-activated protein kinase. FEBS Lett 356(1):117–121. doi:10.1016/0014-5793(94)01247-4
Berthelin CH, Kellner K, Mathieu M (2000) Storage metabolism in the Pacific oyster (Crassostrea gigas) in relation to summer mortalities and reproductive cycle (west coast of France). Comp Biochem Physiol B Biochem Mol Biol 125(3):359–369. doi:10.1016/S0305-0491(99)00187-X
Bertrand L, Ginion A, Beauloye C, Hebert AD, Guigas B, Hue L, Vanoverschelde JL (2006) AMPK activation restores the stimulation of glucose uptake in an in vitro model of insulin-resistant cardiomyocytes via the activation of protein kinase B. Am J Physiol Heart Circ Physiol 291(1):H239–H250. doi:10.1152/ajpheart.01269.2005
Carling D, Clarke PR, Zammit VA, Hardie DG (1989) Purification and characterization of the AMP-activated protein kinase. Copurification of acetyl-CoA carboxylase kinase and 3-hydroxy-3-methylglutaryl-CoA reductase kinase activities. Eur J Biochem/FEBS 186(1–2):129–136. doi:10.1111/j.1432-1033.1989.tb15186.x
Carling D, Mayer FV, Sanders MJ, Gamblin SJ (2011) AMP-activated protein kinase: nature’s energy sensor. Nat Chem Biol 7(8):512–518. doi:10.1038/nchembio.610
Choi SL, Kim SJ, Lee KT, Kim J, Mu J, Birnbaum MJ, Soo Kim S, Ha J (2001) The regulation of AMP-activated protein kinase by H2O2. Biochem Biophys Res Commun 287(1):92–97. doi:10.1006/bbrc.2001.5544
Chopra I, Li HF, Wang H, Webster KA (2011) Phosphorylation of the insulin receptor by AMP-activated protein kinase (AMPK) promotes ligand-independent activation of the insulin signalling pathway in rodent muscle. Diabetologia 55(3):783–794. doi:10.1007/s00125-011-2407-y
Combet C, Blanchet C, Geourjon C, Deleage G (2000) NPS@: network protein sequence analysis. Trends Biochem Sci 25(3):147–150. doi:10.1016/S0968-0004(99)01540-6
Corporeau C, Auffret M (2003) In situ hybridisation for flow cytometry: a molecular method for monitoring stress-gene expression in hemolymph cells of oysters. Aquat Toxicol 64(4):427–435. doi:10.1016/S0166-445X(03)00099-7
de Castro E, Sigrist CJ, Gattiker A, Bulliard V, Langendijk-Genevaux PS, Gasteiger E, Bairoch A, Hulo N (2006) ScanProsite: detection of PROSITE signature matches and ProRule-associated functional and structural residues in proteins. Nucleic Acids Res 34 (Web Server issue):362–365. doi:10.1093/nar/gkl124
Elliott A, Bennett PM (1982) Structure of the thick filaments in molluscan adductor muscle. Soc Gen Physiol Ser 37:11–28
Fabioux C, Corporeau C, Quillien V, Favrel P, Huvet A (2009) In vivo RNA interference in oyster-vasa silencing inhibits germ cell development. FEBS J 276(9):2566–2573. doi:10.1111/j.1742-4658.2009.06982.x
Ferri N (2011) AMP-activated protein kinase and the control of smooth muscle cell hyperproliferation in vascular disease. Vasc Pharmacol. doi:10.1016/j.vph.2011.10.003
Fleury E, Huvet A, Lelong C, de Lorgeril J, Boulo V, Gueguen Y, Bachere E, Tanguy A, Moraga D, Fabioux C, Lindeque P, Shaw J, Reinhardt R, Prunet P, Davey G, Lapegue S, Sauvage C, Corporeau C, Moal J, Gavory F, Wincker P, Moreews F, Klopp C, Mathieu M, Boudry P, Favrel P (2009) Generation and analysis of a 29,745 unique expressed sequence tags from the Pacific oyster (Crassostrea gigas) assembled into a publicly accessible database: the GigasDatabase. BMC Genomics 10:341. doi:10.1186/1471-2164-10-341
Frederich M, O’Rourke MR, Furey NB, Jost JA (2009) AMP-activated protein kinase (AMPK) in the rock crab, Cancer irroratus: an early indicator of temperature stress. J Exp Biol 212(Pt 5):722–730. doi:10.1242/jeb.021998
Funai K, Schweitzer GG, Castorena CM, Kanzaki M, Cartee GD (2010) In vivo exercise followed by in vitro contraction additively elevates subsequent insulin-stimulated glucose transport by rat skeletal muscle. Am J Physiol Endocrinol Metab 298(5):E999–E1010. doi:10.1152/ajpendo.00758.2009
Gamboa JL, Garcia-Cazarin ML, Andrade FH (2011) Chronic hypoxia increases insulin-stimulated glucose uptake in mouse soleus muscle. Am J Physiol Regul Integ Comp Physiol 300(1):R85–R91. doi:10.1152/ajpregu.00078.2010
Garcia-Esquivel Z, Bricelj VM, Gonzalez-Gomez MA (2001) Physiological basis for energy demands and early postlarval mortality in the Pacific oyster, Crassostrea gigas. J Exp Mar Biol Ecol 263(1):77–103. doi:10.1016/S0022-0981(01)00300-8
Garcia-Esquivel Z, Bricelj VM, Felbeck H (2002) Metabolic depression and whole-body response to enforced starvation by Crassostrea gigas postlarvae. Comp Biochem Physiol A Mol Integr Physiol 133(1):63–77. doi:10.1016/S1095-6433(02)00112-5
Gasteiger E, Gattiker A, Hoogland C, Ivanyi I, Appel RD, Bairoch A (2003) ExPASy: the proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Res 31(13):3784–3788. doi:10.1093/nar/gkg563
Gray JS, Wu RSS, Or YY (2002) Effects of hypoxia and organic enrichment on the coastal marine environment. Mar Ecol Prog Ser 238:249–279. doi:10.3354/meps238249
Greenway SC, Storey KB (1999) The effect of prolonged anoxia on enzyme activities in oysters (Crassostrea virginica) at different seasons. J Exp Mar Biol Ecol 242(2):259–272. doi:10.1016/S0022-0981(99)00103-3
Gricourt L, Bonnec G, Boujard D, Mathieu M, Kellner K (2003) Insulin-like system and growth regulation in the Pacific oyster Crassostrea gigas: hrIGF-1 effect on protein synthesis of mantle edge cells and expression of an homologous insulin receptor-related receptor. Gen Comp Endocrinol 134(1):44–56. doi:10.1016/s0016-6480(03)00217-x
Hamano K, Awaji M, Usuki H (2005) cDNA structure of an insulin-related peptide in the Pacific oyster and seasonal changes in the gene expression. J Endocrinol 187(1):55–67. doi:10.1677/joe.1.06284
Hanke N, Meissner JD, Scheibe RJ, Endeward V, Gros G, Kubis HP (2008) Metabolic transformation of rabbit skeletal muscle cells in primary culture in response to low glucose. Biochim Biophys Acta 1783(5):813–825. doi:10.1016/j.bbamcr.2007.12.012
Hardie DG (2003) Management of cellular energy by the AMP-activated protein kinase system. FEBS Lett 546(1):113–120. doi:10.1016/s0014-5793(03)00560-x
Hardie DG (2004) The AMP-activated protein kinase pathway—new players upstream and downstream. J Cell Sci 117(Pt 23):5479–5487. doi:10.1242/jcs.01540
Hardie DG (2007) AMP-activated/SNF1 protein kinases: conserved guardians of cellular energy. Nat Rev Mol Cell Bio 8(10):774–785. doi:10.1038/Nrm2249
Hardie DG (2008) AMPK: a key regulator of energy balance in the single cell and the whole organism. Int J Obesity 32(Suppl 4):7–12. doi:10.1038/ijo.2008.116
Hardie DG, Carling D, Carlson M (1998) The AMP-activated/SNF1 protein kinase subfamily: metabolic sensors of the eukaryotic cell? Annu Rev Biochem 67:821–855. doi:10.1146/annurev.biochem.67.1.821
Hawley SA, Davison M, Woods A, Davies SP, Beri RK, Carling D, Hardie DG (1996) Characterization of the AMP-activated protein kinase kinase from rat liver and identification of threonine 172 as the major site at which it phosphorylates AMP-activated protein kinase. J Biol Chem 271(44):27879–27887. doi:10.1074/jbc.271.44.27879
Hayashi T, Hirshman MF, Fujii N, Habinowski SA, Witters LA, Goodyear LJ (2000) Metabolic stress and altered glucose transport—activation of AMP-activated protein kinase as a unifying coupling mechanism. Diabetes 49(4):527–531. doi:10.2337/diabetes.49.4.527
Heinonen J, Kukkonen J, Penttinen OP, Holopainen IJ (1997) Effects of hypoxia on valve-closure time and bioaccumulation of 2,4,5-trichlorophenol by the freshwater clam Sphaerium corneum [L]. Ecotoxicol Environ Saf 36(1):49–56. doi:10.1006/eesa.1996.1486
Hong NY, Cui ZG, Kang HK, Lee DH, Lee YK, Park DB (2012) p-Synephrine stimulates glucose consumption via AMPK in L6 skeletal muscle cells. Biochem Biophys Res Commun. doi:10.1016/j.bbrc.2012.01.085
Horie T, Ono K, Nagao K, Nishi H, Kinoshita M, Kawamura T, Wada H, Shimatsu A, Kita T, Hasegawa K (2008) Oxidative stress induces GLUT4 translocation by activation of P13-K/Akt and dual AMPK kinase in cardiac myocytes. J Cell Physiol 215(3):733–742. doi:10.1002/Jcp.21353
Huvet A, Herpin A, Degremont L, Labreuche Y, Samain JF, Cunningham C (2004) The identification of genes from the oyster Crassostrea gigas that are differentially expressed in progeny exhibiting opposed susceptibility to summer mortality. Gene 343(1):211–220. doi:10.1016/j.gene.2004.09.008
Ivanina AV, Froelich B, Williams T, Sokolov EP, Oliver JD, Sokolova IM (2011) Interactive effects of cadmium and hypoxia on metabolic responses and bacterial loads of eastern oysters Crassostrea virginica Gmelin. Chemosphere 82(3):377–389. doi:10.1016/j.chemosphere.2010.09.075
Jibb LA, Richards JG (2008) AMP-activated protein kinase activity during metabolic rate depression in the hypoxic goldfish, Carassius auratus. J Exp Biol 211(Pt 19):3111–3122. doi:10.1242/jeb.019117
Jost JA, Podolski SM, Frederich M (2012) Enhancing thermal tolerance by eliminating the pejus range: a comparative study with three decapod crustaceans. Mar Ecol Prog Ser 444:263–274. doi:10.3354/Meps09379
Jouaux A, Heude-Berthelin C, Sourdaine P, Blin JL, Mathieu M, Kellner K (2011) Identification of Ras, Pten and p70S6K homologs in the Pacific oyster Crassostrea gigas and diet control of insulin pathway. Gen Comp Endocrinol doi:10.1016/j.ygcen.2011.12.008
Kawabe S, Yokoyama Y (2011a) Novel isoforms of heat shock transcription factor 1 are induced by hypoxia in the Pacific oyster Crassostrea gigas. J Exp Zool A Ecol Genet Physiol 315(7):394–407. doi:10.1002/jez.685
Kawabe S, Yokoyama Y (2011b) Role of hypoxia-inducible factor alpha in response to hypoxia and heat shock in the Pacific oyster Crassostrea gigas. Mar Biotechnol. doi:10.1007/s10126-011-9394-3
Khan T, Hixon JA, Stauffer JK, Lincoln E, Back TC, Brenner J, Lockett S, Nagashima K, Powell D, Wigginton JM (2006) Therapeutic modulation of Akt activity and antitumor efficacy of interleukin-12 against orthotopic murine neuroblastoma. J Natl Cancer Inst 98(3):190–202. doi:10.1093/jnci/djj021
Kim TR, Cho EW, Paik SG, Kim IG (2012) Hypoxia-induced SM22alpha in A549 cells activates the IGF1R/PI3K/Akt pathway, conferring cellular resistance against chemo- and radiation therapy. FEBS Lett doi:10.1016/j.febslet.2011.12.036
Kovacic S, Soltys CLM, Barr AJ, Shiojima I, Walsh K, Dyck JRB (2003) Akt activity negatively regulates phosphorylation of AMP-activated protein kinase in the heart. J Biol Chem 278(41):39422–39427. doi:10.1074/jbc.M305371200
Le Moullac G (2008) Adaptation du métabolisme respiratoire de l’huître creuse Crassostrea gigas. Thèse de doctorat Université de Bretagne Occidentale, 161
Le Moullac G, Bacca H, Huvet A, Moal J, Pouvreau S, Van Wormhoudt A (2007a) Transcriptional regulation of pyruvate kinase and phosphoenolpyruvate carboxykinase in the adductor muscle of the oyster Crassostrea gigas during prolonged hypoxia. J Exp Zool A Ecol Genet Physiol 307(7):371–382. doi:10.1002/jez.390
Le Moullac G, Quéau I, Le Souchu P, Pouvreau S, Moal J, Le Coz JR, Samain JF (2007b) Metabolic adjustments in the oyster Crassostrea gigas according to oxygen level and temperature. Mar Biol Res 3(5):357–366. doi:10.1080/17451000701635128
Letunic I, Doerks T, Bork P (2011) SMART 7: recent updates to the protein domain annotation resource. Nucleic Acids Res. doi:10.1093/nar/gkr931
Manley AR (1983) The effects of copper on the behavior, respiration, filtration and ventilation activity of Mytilus Edulis. J Mar Biol Assoc UK 63(1):205–222
Manning BD, Cantley LC (2007) AKT/PKB signaling: navigating downstream. Cell 129(7):1261–1274. doi:10.1016/j.cell.2007.06.009
Mitchelhill KI, Michell BJ, House CM, Stapleton D, Dyck J, Gamble J, Ullrich C, Witters LA, Kemp BE (1997) Posttranslational modifications of the 5′-AMP-activated protein kinase beta1 subunit. J Biol Chem 272(39):24475–24479. doi:10.1074/jbc.272.39.24475
Mu J, Brozinick JT Jr, Valladares O, Bucan M, Birnbaum MJ (2001) A role for AMP-activated protein kinase in contraction- and hypoxia-regulated glucose transport in skeletal muscle. Mol Cell 7(5):1085–1094. doi:10.1016/S1097-2765(01)00251-9
Mullonkal CJ, Toledo-Pereyra LH (2007) Akt in ischemia and reperfusion. J Invest Surg Off J Acad Surg Res 20(3):195–203. doi:10.1080/08941930701366471
Musi N, Goodyear LJ (2003) AMP-activated protein kinase and muscle glucose uptake. Acta Physiol Scand 178(4):337–345. doi:10.1046/j.1365-201X.2003.01168.x
Neumann D (2003) Mammalian AMP-activated protein kinase: functional, heterotrimeric complexes by co-expression of subunits in Escherichia coli. Protein Expr Purif 30(2):230–237. doi:10.1016/s1046-5928(03)00126-8
Newell RC (1979) Biology of intertidal animals. Mar Ecol Surveys Ltd., Kent
Noy P, Sawasdichai A, Jayaraman PS, Gaston K (2012) Protein kinase CK2 inactivates PRH/Hhex using multiple mechanisms to de-repress VEGF-signalling genes and promote cell survival. Nucleic Acids Res. doi:10.1093/nar/gks687
Parcellier A, Tintignac LA, Zhuravleva E, Hemmings BA (2008) PKB and the mitochondria: AKTing on apoptosis. Cell Signal 20(1):21–30. doi:10.1016/j.cellsig.2007.07.010
Pernet F, Barret J, Gall PL, Corporeau C, Dégremont L, Lagarde F, Pépin JF, Keck N (2012) Mass mortalities of Pacific oysters Crassostrea gigas reflect infectious diseases and vary with farming practises in the Thau lagoon. Aquac Environ Interact. doi:10.3354/aei00041
Pichavant K, Person-Le-Ruyet J, Le Bayon N, Sévère A, Le Roux A, Quéméner L, Maxime V, Nonnotte G, Boeuf G (2000) Effects of hypoxia on growth and metabolism of juvenile turbot. Aquaculture 188(1–2):103–114. doi:10.1016/s0044-8486(00)00316-1
Pinz I, Perry DJ, Frederich M (2005) Activation of 5′-AMP activated protein kinase during anaerobiosis in the rock crab, Cancer irroratus. Bull Mt Desert Isl Biol Lab 44:31–32
Ramanathan L, Sheth PR, Ogas P, Xiao L, Le HV (2010) Purification and characterization of truncated human AMPK alpha 2 beta 2 gamma 3 heterotrimer from baculovirus-infected insect cells. Protein Expr Purif 70(1):13–22. doi:10.1016/j.pep.2009.10.007
Ramnanan CJ, McMullen DC, Groom AG, Storey KB (2010) The regulation of AMPK signaling in a natural state of profound metabolic rate depression. Mol Cell Biochem 335(1–2):91–105. doi:10.1007/s11010-009-0246-7
Rodet F, Lelong C, Dubos MP, Favrel P (2008) Alternative splicing of a single precursor mRNA generates two subtypes of gonadotropin-releasing hormone receptor orthologues and their variants in the bivalve mollusc Crassostrea gigas. Gene 414(1–2):1–9. doi:10.1016/j.gene.2008.01.022
Ruas JL, White JP, Rao RR, Kleiner S, Brannan KT, Harrison BC, Greene NP, Wu J, Estall JL, Irving BA, Lanza IR, Rasbach KA, Okutsu M, Nair KS, Yan Z, Leinwand LA, Spiegelman BM (2012) A PGC-1alpha isoform induced by resistance training regulates skeletal muscle hypertrophy. Cell 151(6):1319–1331. doi:10.1016/j.cell.2012.10.050
Saha AK, Schwarsin AJ, Roduit R, Masse F, Kaushik V, Tornheim K, Prentki M, Ruderman NB (2000) Activation of malonyl-CoA decarboxylase in rat skeletal muscle by contraction and the AMP-activated protein kinase activator 5-aminoimidazole-4-carboxamide-1-beta-d-ribofuranoside. J Biol Chem 275(32):24279–24283. doi:10.1074/jbc.C000291200
Samain JF, McCombie H (2008) Summer mortality of Pacific oyster Crassostrea gigas. The morest project. Edition Ifremer Quae
Sato T, Toyoshima A, Hiraki T, Ohta Y, Katayama K, Arai T, Tazaki H (2011) Effects of metformin on plasma concentrations of glucose and mannose, G6Pase and PEPCK activity, and mRNA expression in the liver and kidney of chickens. Br Poult Sci 52(2):273–277. doi:10.1080/00071668.2011.560595
Schultz J, Milpetz F, Bork P, Ponting CP (1998) SMART, a simple modular architecture research tool: identification of signaling domains. Proc Natl Acad Sci USA 95(11):5857–5864
Stapleton D, Mitchelhill KI, Gao G, Widmer J, Michell BJ, Teh T, House CM, Fernandez CS, Cox T, Witters LA, Kemp BE (1996) Mammalian AMP-activated protein kinase subfamily. J Biol Chem 271(2):611–614. doi:10.1074/jbc.271.2.611
Stenslokken KO, Ellefsen S, Stecyk JA, Dahl MB, Nilsson GE, Vaage J (2008) Differential regulation of AMP-activated kinase and AKT kinase in response to oxygen availability in crucian carp (Carassius carassius). Am J Physiol Regul Integr Comp Physiol 295(6):1803–1814. doi:10.1152/ajpregu.90590.2008
Storey KB (1993) Molecular mechanisms of metabolic arrest in molluscs. In: Surviving hypoxia: mechanisms of control and adaptation. CRC Press, Boca Raton, pp 253–269
Stricker SA (2011) Potential upstream regulators and downstream targets of AMP-activated kinase signaling during oocyte maturation in a marine worm. Reproduction 142(1):29–39. doi:10.1530/Rep-10-0509
Stricker SA, Swiderek L, Nguyen T (2010) Stimulators of AMP-activated kinase (AMPK) inhibit seawater- but not cAMP-induced oocyte maturation in a marine worm: implications for interactions between cAMP and AMPK signaling. Mol Reprod Dev 77(6):497–510. doi:10.1002/mrd.21177
Sung JY, Woo CH, Kang YJ, Lee KY, Choi HC (2011) AMPK induces vascular smooth muscle cell senescence via LKB1 dependent pathway. Biochem Biophys Res Commun 413(1):143–148. doi:10.1016/j.bbrc.2011.08.071
Sussarellu R, Fabioux C, Le Moullac G, Fleury E, Moraga D (2010) Transcriptomic response of the Pacific oyster Crassostrea gigas to hypoxia. Mar Genomics 3(3–4):133–143. doi:10.1016/j.margen.2010.08.005
Sussarellu R, Fabioux C, Le Goic N, Lambert C, Soudant P, Moraga D (2011) Molecular and cellular response to short-term oxygen variations in the Pacific oyster Crassostrea gigas. J Exp Mar Biol Ecol 412:87–95. doi:10.1016/j.jembe.2011.11.007
Suter M, Riek U, Tuerk R, Schlattner U, Wallimann T, Neumann D (2006) Dissecting the role of 5′-AMP for allosteric stimulation, activation, and deactivation of AMP-activated protein kinase. J Biol Chem 281(43):32207–32216. doi:10.1074/jbc.M606357200
Towler MC, Hardie DG (2007) AMP-activated protein kinase in metabolic control and insulin signaling. Circ Res 100(3):328–341. doi:10.1161/01.RES.0000256090.42690.05
Tran D, Boudou A, Massabuau JC (2000) Mechanism for maintaining oxygen consumption under varying oxygenation levels in the freshwater clam Corbicula fluminea. Can J Zool 78(11):2027–2036. doi:10.1139/cjz-78-11-2027
Tripathi G, Verma P (2004) Sex-specific metabolic changes in the annual reproductive cycle of a freshwater catfish. Comp Biochem Physiol B Biochem Mol Biol 137(1):101–106. doi:10.1016/j.cbpc.2003.10.005
Viollet B, Andreelli F, Jorgensen SB, Perrin C, Flamez D, Mu J, Wojtaszewski JF, Schuit FC, Birnbaum M, Richter E, Burcelin R, Vaulont S (2003) Physiological role of AMP-activated protein kinase (AMPK): insights from knockout mouse models. Biochem Soc Trans 31(Pt 1):216–219. doi:10.1042/
Wadley GD, Lee-Young RS, Canny BJ, Wasuntarawat C, Chen ZP, Hargreaves M, Kemp BE, McConell GK (2006) Effect of exercise intensity and hypoxia on skeletal muscle AMPK signaling and substrate metabolism in humans. Am J Physiol Endocrinol Metab 290(4):E694–E702. doi:10.1152/ajpendo.00464.2005
Woods A, Vertommen D, Neumann D, Turk R, Bayliss J, Schlattner U, Wallimann T, Carling D, Rider MH (2003) Identification of phosphorylation sites in AMP-activated protein kinase (AMPK) for upstream AMPK kinases and study of their roles by site-directed mutagenesis. J Biol Chem 278(31):28434–28442. doi:10.1074/jbc.M303946200
Wu RSS (2002) Hypoxia: from molecular responses to ecosystem responses. Mar Pollut Bull 45(1–12):35–45. doi:10.1016/S0025-326X(02)00061-9
Yook K, Harris TW, Bieri T, Cabunoc A, Chan J, Chen WJ, Davis P, de la Cruz N, Duong A, Fang R, Ganesan U, Grove C, Howe K, Kadam S, Kishore R, Lee R, Li Y, Muller HM, Nakamura C, Nash B, Ozersky P, Paulini M, Raciti D, Rangarajan A, Schindelman G, Shi X, Schwarz EM, Ann Tuli M, Van Auken K, Wang D, Wang X, Williams G, Hodgkin J, Berriman M, Durbin R, Kersey P, Spieth J, Stein L, Sternberg PW (2012) WormBase 2012: more genomes, more data, new website. Nucleic Acids Res 40 (Database issue):735–741. doi:10.1093/nar/gkr954
Yoshida EN, Benkel BF, Fong Y, Hickey DA (1999) Sequence and phylogenetic analysis of the SNF4/AMPK gamma subunit gene from Drosophila melanogaster. Genome 42(6):1077–1087
Zhang G, Fang X, Guo X, Li L, Luo R, Xu F, Yang P, Zhang L, Wang X, Qi H, Xiong Z, Que H, Xie Y, Holland PW, Paps J, Zhu Y, Wu F, Chen Y, Wang J, Peng C, Meng J, Yang L, Liu J, Wen B, Zhang N, Huang Z, Zhu Q, Feng Y, Mount A, Hedgecock D, Xu Z, Liu Y, Domazet-Loso T, Du Y, Sun X, Zhang S, Liu B, Cheng P, Jiang X, Li J, Fan D, Wang W, Fu W, Wang T, Wang B, Zhang J, Peng Z, Li Y, Li N, Chen M, He Y, Tan F, Song X, Zheng Q, Huang R, Yang H, Du X, Chen L, Yang M, Gaffney PM, Wang S, Luo L, She Z, Ming Y, Huang W, Huang B, Zhang Y, Qu T, Ni P, Miao G, Wang Q, Steinberg CE, Wang H, Qian L, Liu X, Yin Y (2012) The oyster genome reveals stress adaptation and complexity of shell formation. Nature 490(7418):49–54. doi:10.1038/nature11413
Zhu XJ, Feng CZ, Dai ZM, Zhang RC, Yang WJ (2007) AMPK alpha subunit gene characterization in artemia and expression during development and in response to stress. Stress 10(1):53–63. doi:10.1080/10253890601130773
Acknowledgments
The present research project was supported by “Europole Mer” (www.europolemer.eu; project “OxyGenes”) and by the ANR (project “Gametogenes” ANR-08-GENM-041) with collaboration supported National Basic Research Program of China (973 Program, no. 2010CB126401). Eric Guévélou was funded by Ifremer and a Région Bretagne doctoral grant. Genome information collected for this publication was obtained upon the support provided by the Ministry of Foreign Affairs (MAE). The authors are grateful to Karine Pichavant of the ORPHY laboratory for logistic support, the organization of the experimental hypoxic system and for technical support during the animal conditioning. The authors are indebted to Chantal Cahu for advice and support. We thank Helen McCombie for her help with editing the English.
Conflict of interest
The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by G. Heldmaier.
Rights and permissions
About this article
Cite this article
Guévélou, E., Huvet, A., Sussarellu, R. et al. Regulation of a truncated isoform of AMP-activated protein kinase α (AMPKα) in response to hypoxia in the muscle of Pacific oyster Crassostrea gigas . J Comp Physiol B 183, 597–611 (2013). https://doi.org/10.1007/s00360-013-0743-6
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00360-013-0743-6