50
Views
289
CrossRef citations to date
0
Altmetric
Signal Transduction

AMP-Activated Protein Kinase Protects Cardiomyocytes against Hypoxic Injury through Attenuation of Endoplasmic Reticulum Stress

, , , , , , & show all
Pages 9554-9575 | Received 06 Jun 2005, Accepted 16 Aug 2005, Published online: 27 Mar 2023

REFERENCES

  • Becker, T. C., R. J. Noel, W. S. Coats, A. M. Gomez-Foix, T. Alam, R. D. Gerard, and C. B. Newgard. 1994. Use of recombinant adenovirus for metabolic engineering of mammalian cells. Methods Cell Biol. 43:161–189.
  • Bertolotti, A., Y. Zhang, L. M. Hendershot, H. P. Harding, and D. Ron. 2000. Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat. Cell Biol. 2:326–332.
  • Boyce, M., K. F. Bryant, C. Jousse, K. Long, H. P. Harding, D. Scheuner, R. J. Kaufman, D. Ma, D. M. Coen, D. Ron, and J. Yuan. 2005. A selective inhibitor of eIF2alpha dephosphorylation protects cells from ER stress. Science 307:935–939.
  • Browne, G. J., S. G. Finn, and C. G. Proud. 2002. Stimulation of the AMP-activated protein kinase leads to activation of eukaryotic elongation factor 2 kinase and to its phosphorylation at a novel site, serine 398. J. Biol. Chem. 12:12220–12231.
  • Browne, G. J., and C. G. Proud. 2002. Regulation of peptide-chain elongation in mammalian cells. Eur. J. Biochem. 269:5360–5368.
  • Cardozo, A. K., F. Ortis, J. Storling, Y.-M. Feng, J. Rasschaert, M. Tonnesen, F. Van Eylen, T. Mandrup-Poulsen, A. Herchuelz, and D. L. Eizirik. 2005. Cytokines downregulate the sarcoendoplasmic reticulum pump Ca2+ ATPase 2b and deplete endoplasmic reticulum Ca2+, leading to induction of endoplasmic reticulum stress in pancreatic β-cells. Diabetes 54:452–461.
  • Carling, D. 2004. The AMP-activated protein kinase cascade—a unifying system for energy control. Trends Biochem. Sci. 29:18–24.
  • Chan, A. Y., and J. R. Dyck. 2005. Activation of AMP-activated protein kinase (AMPK) inhibits protein synthesis: a potential strategy to prevent the development of cardiac hypertrophy. Can. J. Physiol. Pharmacol. 83:24–28.
  • Chen, S. J., M. E. Bradley, and T. C. Lee. 1998. Chemical hypoxia triggers apoptosis of cultured neonatal rat cardiac myocytes: modulation by calcium-regulated proteases and protein kinases. Mol. Cell. Biochem. 178:141–149.
  • Crow, M. T., K. Mani, Y. J. Nam, and R. N. Kitsis. 2004. The mitochondrial death pathway and cardiac myocyte apoptosis. Circ. Res. 95:957–970.
  • Donato, M., and R. J. Gelpi. 2003. Adenosine and cardioprotection during reperfusion—an overview. Mol. Cell. Biochem. 251:153–159.
  • Elbashir, S. M., J. Harborth, W. Lendeckel, A. Yalcin, K. Weber, and T. Tuschl. 2001. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411:494–498.
  • Elbashir, S. M., J. Harborth, K. Weber, and T. Tuschl. 2002. Analysis of gene function in somatic mammalian cells using small interfering RNAs. Methods 26:199–213.
  • Ferri, K. F., and G. Kroemer. 2001. Organelle-specific initiation of cell death pathways. Nat. Cell Biol. 3:E255–E263.
  • Forssmann, W. G., K. Nokihara, M. Gagelmann, D. Hock, S. Feller, P. Schulz-Knappe, and F. Herbst. 1989. The heart is the center of a new endocrine, paracrine, and neuroendocrine system. Arch. Histol. Cytol. 52(Suppl.):293–315.
  • Forssmann, W. G., R. Richter, and M. Meyer. 1998. The endocrine heart and natriuretic peptides: histochemistry, cell biology, and functional aspects of the renal urodilatin system. Histochem. Cell Biol. 110:335–357.
  • Frederich, M., L. Zhang, and J. A. Balschi. 2005. Hypoxia and AMP independently regulate AMP-activated protein kinase activity in heart. Am. J. Physiol. Heart Circ. Physiol. 288:H2412–H2421.
  • Fryer, L. G., A. Parbu-Patel, and D. Carling. 2002. The anti-diabetic drugs rosiglitazone and metformin stimulate AMP-activated protein kinase through distinct signaling pathways. J. Biol. Chem. 277:25226–25232.
  • Funamoto, M., Y. Fujio, K. Kunisada, S. Negoro, E. Tone, T. Osugi, H. Hirota, M. Izumi, K. Yoshizaki, K. Walsh, T. Kishimoto, and K. Yamauchi-Takihara. 2000. Signal transducer and activator of transcription 3 is required for glycoprotein 130-mediated induction of vascular endothelial growth factor in cardiac myocytes. J. Biol. Chem. 275:10561–10566.
  • Gollob, M. H., M. S. Green, A. S. Tang, T. Gollob, A. Karibe, A. S. Ali Hassan, F. Ahmad, R. Lozado, G. Shah, L. Fananapazir, L. L. Bachinski, and R. Roberts. 2001. Identification of a gene responsible for familial Wolff-Parkinson-White syndrome. N. Engl. J. Med. 344:1823–1831.
  • Gruber, H. E. 1994. Acadesine: preclinical overview. Adv. Exp. Med. Biol. 370:423–426.
  • Hardie, D. G. 2003. Minireview: the AMP-activated protein kinase cascade: the key sensor of cellular energy status. Endocrinology 144:5179–5183.
  • Hardie, D. G. 2004. AMP-activated protein kinase: the guardian of cardiac energy status. J. Clin. Investig. 114:465–468.
  • Hardie, D. G., and D. Carling. 1997. The AMP-activated protein kinase-fuel gauge of the mammalian cell. Eur. J. Biochem. 246:259–273.
  • Hardie, D. G., D. Carling, and M. Carlson. 1998. The AMP-activated/SNF1 protein kinase subfamily: metabolic sensors of the eukaryotic cell. Annu. Rev. Biochem. 67:821–855.
  • Hayashi, T., A. Saito, S. Okuno, M. Ferrand-Drake, R. L. Dodd, and P. H. Chan. 2003. Oxidative injury to the endoplasmic reticulum in mouse brains after transient focal ischemia. Neurobiol. Dis. 23:229–239.
  • Heaps, C. L., M. Sturek, E. M. Price, M. H. Laughlin, and J. L. Parker. 2001. Sarcoplasmic reticulum Ca2+ uptake is impaired in coronary smooth muscle distal to coronary occlusion. Am. J. Physiol. Heart Circ. Physiol. 281:H223–H231.
  • Horman, S., C. Beauloye, D. Vertommen, J. L. Vanoverschelde, L. Hue, and M. H. Rider. 2003. Myocardial ischemia and increased heart work modulate the phosphorylation state of eukaryotic elongation factor-2. J. Biol. Chem. 278:41970–41976.
  • Imaizumi, K., T. Katayama, and M. Tohyama. 2000. Presenilin and the UPR. Nat. Cell Biol. 85:E104.
  • Kaufman, R. J. 2002. Orchestrating the unfolded protein response in health and disease. J. Clin. Investig. 110:1389–1398.
  • Kudo, N., A. J. Barr, R. L. Barr, S. Desai, and G. D. Lopaschuk. 1995. High rates of fatty acid oxidation during reperfusion of ischemic hearts are associated with a decrease in malonyl-CoA levels due to an increase in 5′-AMP-activated protein kinase inhibition of acetyl-CoA carboxylase. J. Biol. Chem. 270:17513–17520.
  • Lee, K., W. Tirasophon, X. Shen, M. Michalak, R. Prywes, T. Okada, H. Yoshida, K. Mori, and R. J. Kaufman. 2002. IRE1-mediated unconventional mRNA splicing and S2P-mediated ATF6 cleavage merge to regulate XBP1 in signaling the unfolded protein response. Genes Dev. 16:452–466.
  • Levy, A. P., N. S. Levy, J. Loscalzo, A. Calderone, N. Takahashi, K.-T. Yeo, G. Koren, W. S. Colucci, and M. A. Goldberg. 1995. Regulation of vascular endotherial growth factor in cardiac myocytes. Circ. Res. 76:758–766.
  • Li, S., D. M. Perlman, M. S. Peterson, D. Burrichter, S. Avdulov, V. A. Polunovsky, and P. B. Bitterman. 2004. Translation initiation factor 4E blocks endoplasmic reticulum-mediated apoptosis. J. Biol. Chem. 279:21312–21317.
  • Lu, P. D., C. Jousse, S. J. Marciniak, Y. Zhang, I. Novoa, D. Scheuner, R. J. Kaufman, D. Ron, and H. P. Harding. 2004. Cytoprotection by pre-emptive conditional phosphorylation of translation initiation factor 2. EMBO J. 23:169–179.
  • Mangano, D. T., et al. 1997. Effects of acadesine on myocardial infarction, stroke, and death following surgery. A meta-analysis of the 5 international randomized trials. JAMA 277:325–332.
  • Mao, W., C. Iwai, F. Qin, and C. S. Liang. 2005. Norepinephrine induces endoplasmic reticulum stress and downregulation of norepinephrine transporter density in PC12 cells via oxidative stress. Am. J. Physiol. Heart Circ. Physiol. 288:H2381–H2389.
  • Marsin, A. S., L. Bertrand, M. H. Rider, J. Deprez, C. Beauloye, M. F. Vincent, G. Van den Berghe, D. Carling, and L. Hue. 2000. Phosphorylation and activation of heart PFK-2 by AMPK has a role in the stimulation of glycolysis during ischaemia. Curr. Biol. 10:1247–1255.
  • Masaki, M., M. Izumi, Y. Oshima, Y. Nakaoka, T. Kuroda, R. Kimura, S. Sugiyama, K. Terai, M. Kitakaze, K. Yamauchi-Takihara, I. Kawase, and H. Hirota. 2005. Smad1 protects cardiomyocytes from ischemia-reperfusion injury. Circulation 111:2752–2759.
  • Masoudi, F. A., S. E. Inzucchi, Y. Wang, E. P. Havranek, J. M. Foody, and H. M. Krumholz. 2005. Thiazolidinediones, metformin, and outcomes in older patients with diabetes and heart failure: an observational study. Circulation 111:583–590.
  • McLeod, L. E., and C. G. Proud. 2002. ATP depletion increases phosphorylation of elongation factor eEF2 in adult cardiomyocytes independently of inhibition of mTOR signalling. FEBS Lett. 531:448–452.
  • Minokoshi, Y., Y. B. Kim, O. D. Peroni, L. G. Fryer, C. Muller, D. Carling, and B. B. Kahn. 2002. Leptin stimulates fatty-acid oxidation by activating AMP-activated protein kinase. Nature 415:339–343.
  • Mori, K. 2000. Tripartite management of unfolded proteins in the endoplasmic reticulum. Cell 101:451–454.
  • Mullane, K. 1993. Acadesine: the prototype adenosine regulating agent for reducing myocardial ischaemic injury. Cardiovasc. Res. 27:43–47.
  • Nakagawa, T., and J. Yuan. 2000. Cross-talk between two cysteine protease families. Activation of caspase-12 by calpain in apoptosis. J. Cell Biol. 150:887–894.
  • Nakagawa, T., H. Zhu, N. Morishima, E. Li, J. Xu, B. A. Yankner, and J. Yuan. 2000. Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature 403:98–103.
  • Nishino, Y., T. Miura, T. Miki, J. Sakamoto, Y. Nakamura, Y. Ikeda, H. Kobayashi, and K. Shimamoto. 2004. Ischemic preconditioning activates AMPK in a PKC-dependent manner and induces GLUT4 up-regulation in the late phase of cardioprotection. Cardiovasc. Res. 61:610–619.
  • Okada, K., T. Minamino, Y. Tsukamoto, Y. Liao, O. Tsukamoto, S. Takashima, A. Hirata, M. Fujita, Y. Nagamachi, T. Nakatani, C. Yutani, K. Ozawa, S. Ogawa, H. Tomoike, M. Hori, and M. Kitakaze. 2004. Prolonged endoplasmic reticulum stress in hypertrophic and failing heart after aortic constriction: possible contribution of endoplasmic reticulum stress to cardiac myocyte apoptosis. Circulation 110:705–712.
  • Oyadomari, S., A. Koizumi, K. Takeda, T. Gotoh, S. Akira, E. Araki, and M. Mori. 2002. Targeted disruption of the Chop gene delays endoplasmic reticulum stress-mediated diabetes. J. Clin. Investig. 109:525–532.
  • Oyadomari, S., and M. Mori. 2004. Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Diff. 11:381–389.
  • Ozawa, K., T. Kondo, O. Hori, Y. Kitao, D. M. Stern, W. Eisenmenger, S. Ogawa, and T. Ohshima. 2001. Expression of the oxygen-regulated protein ORP150 accelerates wound healing by modulating intracellular VEGF transport. J. Clin. Investig. 108:41–50.
  • Pieper, A. A., A. Verma, J. Zhang, and S. H. Snyder. 1999. Poly (ADP-ribose) polymerase, nitric oxide and cell death. Trends Pharmacol. Sci. 20:171–181.
  • Ron, D. 2002. Translational control in the endoplasmic reticulum stress response. J. Clin. Investig. 110:1383–1388.
  • Russell, R. R., III, J. Li, D. L. Coven, M. Pypaert, C. Zechner, M. Palmeri, F. J. Giordano, J. Mu, M. J. Birnbaum, and L. H. Young. 2004. AMP-activated protein kinase mediates ischemic glucose uptake and prevents postischemic cardiac dysfunction, apoptosis, and injury. J. Clin. Investig. 114:495–503.
  • Sambandam, N., and G. D. Lopaschuk. 2003. AMP-activated protein kinase (AMPK) control of fatty acid and glucose metabolism in the ischemic heart. Prog. Lipid Res. 42:238–256.
  • Scheuner, D., D. V. Mierde, B. Song, D. Flamez, J. W. M. Creemers, K. Tsukamoto, M. Ribick, F. C. Schuit, and R. J. Kaufman. 2005. Control of mRNA translation preserves endoplasmic reticulum function in beta cells and maintains glucose homeostasis. Nat. Med. 11:757–764.
  • Shannon, T. R., and D. M. Bers. 2004. Integrated Ca2+ management in cardiac myocytes. Ann. N. Y. Acad. Sci. 1015:28–38.
  • Shibata, R., N. Ouchi, M. Ito, S. Kihara, I. Shiojima, D. R. Pimentel, M. Kumada, K. Sato, S. Schiekofer, K. Ohashi, T. Funahashi, W. S. Colucci, and K. Walsh. 2004. Adiponectin-mediated modulation of hypertrophic signals in the heart. Nat. Med. 10:1384–1389.
  • Stapleton, D., K. I. Mitchelhill, G. Gao, J. Widmer, B. J. Michell, T. Teh, C. M. House, C. S. Fernandez, T. Cox, L. A. Witters, and B. E. Kemp. 1996. Mammalian AMP-activated protein kinase subfamily. J. Biol. Chem. 271:611–614.
  • Su, H.-L., C.-L. Liao, and Y.-L. Lin. 2002. Japanese encephalitis virus infection initiates endoplasmic reticulum stress and an unfolded protein response. J. Virol. 76:4162–4171.
  • Talapatra, S., J. D. Wagner, and C. B. Thompson. 2002. Elongation factor-1 alpha is a selective regulator of growth factor withdrawal and ER stress-induced apoptosis. Cell Death Diff. 9:856–861.
  • Tatsumi, T., J. Shiraishi, N. Keira, K. Akashi, A. Mano, S. Yamanaka, S. Matoba, S. Fushiki, H. Fliss, and M. Nakagawa. 2003. Intracellular ATP is required for mitochondrial apoptotic pathways in isolated hypoxic rat cardiac myocytes. Cardiovasc. Res. 59:428–440.
  • Tian, R., N. Musi, J. D'Agostino, M. F. Hirshman, and L. J. Goodyear. 2001. Increased adenosine monophosphate-activated protein kinase activity in rat hearts with pressure-overload hypertrophy. Circulation 104:1664–1669.
  • Travers, K. J., C. K. Patil, L. Wodicka, D. J. Lockhart, J. S. Weissman, and P. Walter. 2000. Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell 101:249–258.
  • Urano, F., X. Wang, A. Bertolotti, Y. Zhang, P. Chung, H. P. Harding, and D. Ron. 2000. Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 287:664–666.
  • Woods, A., D. Azzout-Marniche, M. Foretz, S. C. Stein, P. Lemarchand, P. Ferré, F. Foufelle, and D. Carling. 2000. Characterization of the role of AMP-activated protein kinase in the regulation of glucose-activated gene expression using constitutively active and dominant negative forms of the kinase. Mol. Cell. Biol. 20:6704–6711.
  • Xing, Y., N. Musi, N. Fujii, L. Zou, I. Luptak, M. F. Hirshman, L. J. Goodyear, and R. Tian. 2003. Glucose metabolism and energy homeostasis in mouse hearts overexpressing dominant negative alpha2 subunit of AMP-activated protein kinase. J. Biol. Chem. 278:28372–28377.
  • Yamauchi, T., J. Kamon, Y. Minokoshi, Y. Ito, H. Waki, S. Uchida, S. Yamashita, M. Noda, S. Kita, K. Ueki, K. Eto, Y. Akanuma, P. Froguel, F. Foufelle, P. Ferre, D. Carling, S. Kimura, R. Nagai, B. B. Kahn, and T. Kadowaki. 2002. Adiponectin stimulates glucose utilization and fatty-acid oxidation by activating AMP-activated protein kinase. Nat. Med. 8:1288–1295.
  • Yoshida, H., T. Matsui, A. Yamamoto, T. Okada, and K. Mori. 2001. XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 107:881–891.
  • Yoshida, H., T. Matsui, N. Hosokawa, R. J. Kaufman, K. Nagata, and K. Mori. 2003. A time-dependent phase shift in the mammalian unfolded protein response. Dev. Cell 4:265–271.
  • Zhang, K., and R. J. Kaufman. 2003. Signaling the unfolded protein response from the endoplasmic reticulum. J. Biol. Chem. 23:25935–25938.
  • Zhou, G., R. Myers, Y. Li, Y. Chen, X. Shen, J. Fenyk-Melody, M. Wu, J. Ventre, T. Doebber, N. Fujii, N. Musi, M. F. Hirshman, L. J. Goodyear, and D. E. Moller. 2001. Role of AMP-activated protein kinase in mechanism of metformin action. J. Clin. Investig. 108:1167–1174.
  • Zinszner, H., M. Kuroda, X. Wang, N. Batchvarova, R. T. Lightfoot, H. Remotti, J. L. Stevens, and D. Ron. 1998. CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev. 12:982–995.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.