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Review

Mitochondrial integrity: preservation through Akt/Pim-1 kinase signaling in the cardiomyocyte

Pages 929-938 | Published online: 10 Jan 2014

References

  • Nakayama H, Chen X, Baines CP et al. Ca2+- and mitochondrial-dependent cardiomyocyte necrosis as a primary mediator of heart failure. J. Clin. Invest.117, 2431–2444 (2007).
  • Javadov S, Karmazyn M. Mitochondrial permeability transition pore opening as an endpoint to initiate cell death and as a putative target for cardioprotection. Cell Physiol. Biochem.20, 1–22 (2007).
  • Del Re DP, Miyamoto S, Brown JH. RhoA/Rho kinase up-regulate Bax to activate a mitochondrial death pathway and induce cardiomyocyte apoptosis. J. Biol. Chem.282, 8069–8078 (2007).
  • Murphy E, Steenbergen C. Preconditioning: the mitochondrial connection. Annu. Rev. Physiol.69, 51–67 (2007).
  • Das DK, Maulik N. Mitochondrial function in cardiomyocytes: target for cardioprotection. Curr. Opin. Anaesthesiol.18, 77–82 (2005).
  • Zhang D, Mott JL, Chang SW, Stevens M, Mikolajczak P, Zassenhaus HP. Mitochondrial DNA mutations activate programmed cell survival in the mouse heart. Am. J. Physiol. Heart Circ. Physiol.288, H2476–H2483 (2005).
  • Imahashi K, Schneider MD, Steenbergen C, Murphy E. Transgenic expression of Bcl-2 modulates energy metabolism, prevents cytosolic acidification during ischemia, and reduces ischemia/reperfusion injury. Circ. Res.95, 734–741 (2004).
  • Hausenloy DJ, Yellon DM. New directions for protecting the heart against ischaemia–reperfusion injury: targeting the reperfusion injury salvage kinase (RISK)-pathway. Cardiovasc. Res.61, 448–460 (2004).
  • McFalls EO, Liem D, Schoonderwoerd K, Lamers J, Sluiter W, Duncker D. Mitochondrial function: the heart of myocardial preservation. J. Lab. Clin. Med.142, 141–148 (2003).
  • Adams JW, Pagel AL, Means CK, Oksenberg D, Armstrong RC, Brown JH. Cardiomyocyte apoptosis induced by Gαq signaling is mediated by permeability transition pore formation and activation of the mitochondrial death pathway. Circ. Res.87, 1180–1187 (2000).
  • Gustafsson AB, Gottlieb RA. Heart mitochondria: gates of life and death. Cardiovasc. Res.77, 334–343 (2008).
  • Horbinski C, Chu CT. Kinase signaling cascades in the mitochondrion: a matter of life or death. Free Radic. Biol. Med.38, 2–11 (2005).
  • Hausenloy DJ, Tsang A, Yellon DM. The reperfusion injury salvage kinase pathway: a common target for both ischemic preconditioning and postconditioning. Trends Cardiovasc. Med.15, 69–75 (2005).
  • Kowalczyk JE, Zablocka B. [Protein kinases in mitochondria]. Postepy Biochem.54, 209–216 (2008).
  • Li Y, Sato T. Dual signaling via protein kinase C and phosphatidylinositol 3´-kinase/Akt contributes to bradykinin B2 receptor-induced cardioprotection in guinea pig hearts. J. Mol. Cell. Cardiol.33, 2047–2053 (2001).
  • Murriel CL, Churchill E, Inagaki K, Szweda LI, Mochly-Rosen D. Protein kinase Cδ activation induces apoptosis in response to cardiac ischemia and reperfusion damage: a mechanism involving BAD and the mitochondria. J. Biol. Chem.279, 47985–47991 (2004).
  • Ohori K, Miura T, Tanno M et al. Ser9 phosphorylation of mitochondrial GSK-3β is a primary mechanism of cardiomyocyte protection by erythropoietin against oxidant-induced apoptosis. Am. J. Physiol. Heart Circ. Physiol.295, H2079–H2086 (2008).
  • Park SS, Zhao H, Mueller RA, Xu Z. Bradykinin prevents reperfusion injury by targeting mitochondrial permeability transition pore through glycogen synthase kinase 3β. J. Mol. Cell. Cardiol.40, 708–716 (2006).
  • Cohen MV, Philipp S, Krieg T et al. Preconditioning-mimetics bradykinin and DADLE activate PI3-kinase through divergent pathways. J. Mol. Cell. Cardiol.42, 842–851 (2007).
  • Das M, Gherghiceanu M, Lekli I, Mukherjee S, Popescu LM, Das DK. Essential role of lipid raft in ischemic preconditioning. Cell Physiol. Biochem.21, 325–334 (2008).
  • Downey JM, Krieg T, Cohen MV. Mapping preconditioning’s signaling pathways: an engineering approach. Ann. NY Acad. Sci.1123, 187–196 (2008).
  • Halestrap AP, Clarke SJ, Khaliulin I. The role of mitochondria in protection of the heart by preconditioning. Biochim. Biophys. Acta1767, 1007–1031 (2007).
  • Uchiyama T, Engelman RM, Maulik N, Das DK. Role of Akt signaling in mitochondrial survival pathway triggered by hypoxic preconditioning. Circulation109, 3042–3049 (2004).
  • Zhang Y, Park TS, Gidday JM. Hypoxic preconditioning protects human brain endothelium from ischemic apoptosis by Akt-dependent survivin activation. Am. J. Physiol. Heart Circ. Physiol.292, H2573–H2581 (2007).
  • Smart N, Mojet MH, Latchman DS, Marber MS, Duchen MR, Heads RJ. IL-6 induces PI 3-kinase and nitric oxide-dependent protection and preserves mitochondrial function in cardiomyocytes. Cardiovasc. Res.69, 164–177 (2006).
  • Smith CC, Mocanu MM, Davidson SM, Wynne AM, Simpkin JC, Yellon DM. Leptin, the obesity-associated hormone, exhibits direct cardioprotective effects. Br. J. Pharmacol.149, 5–13 (2006).
  • Lai HC, Liu TJ, Ting CT, Sharma PM, Wang PH. Insulin-like growth factor-1 prevents loss of electrochemical gradient in cardiac muscle mitochondria via activation of PI 3 kinase/Akt pathway. Mol. Cell. Endocrinol.205, 99–106 (2003).
  • Satoh M, Matter CM, Ogita H et al. Inhibition of apoptosis-regulated signaling kinase-1 and prevention of congestive heart failure by estrogen. Circulation115, 3197–3204 (2007).
  • Tissier R, Waintraub X, Couvreur N et al. Pharmacological postconditioning with the phytoestrogen genistein. J. Mol. Cell. Cardiol.42, 79–87 (2007).
  • Lai HC, Liu TJ, Ting CT et al. Regulation of IGF-I receptor signaling in diabetic cardiac muscle: dysregulation of cytosolic and mitochondria HSP60. Am. J. Physiol. Endocrinol. Metab.292, E292–E297 (2007).
  • Ahmad N, Wang Y, Haider KH et al. Cardiac protection by mitoKATP channels is dependent on Akt translocation from cytosol to mitochondria during late preconditioning. Am. J. Physiol. Heart Circ. Physiol.290, H2402–H2408 (2006).
  • Davidson SM, Hausenloy D, Duchen MR, Yellon DM. Signalling via the reperfusion injury signalling kinase (RISK) pathway links closure of the mitochondrial permeability transition pore to cardioprotection. Int. J. Biochem. Cell Biol.38, 414–419 (2006).
  • Juhaszova M, Zorov DB, Kim SH et al. Glycogen synthase kinase-3β mediates convergence of protection signaling to inhibit the mitochondrial permeability transition pore. J. Clin. Invest.113, 1535–1549 (2004).
  • Bhamra GS, Hausenloy DJ, Davidson SM et al. Metformin protects the ischemic heart by the Akt-mediated inhibition of mitochondrial permeability transition pore opening. Basic Res. Cardiol.103, 274–284 (2008).
  • Kobayashi H, Miura T, Ishida H et al. Limitation of infarct size by erythropoietin is associated with translocation of Akt to the mitochondria after reperfusion. Clin. Exp. Pharmacol. Physiol.35, 812–819 (2008).
  • Nagy N, Malik G, Tosaki A, Ho YS, Maulik N, Das DK. Overexpression of glutaredoxin-2 reduces myocardial cell death by preventing both apoptosis and necrosis. J. Mol. Cell. Cardiol.44, 252–260 (2008).
  • Hui ST, Andres AM, Miller AK et al. Txnip balances metabolic and growth signaling via PTEN disulfide reduction. Proc. Natl Acad. Sci. USA105, 3921–3926 (2008).
  • Philipp S, Critz SD, Cui L, Solodushko V, Cohen MV, Downey JM. Localizing extracellular signal-regulated kinase (ERK) in pharmacological preconditioning’s trigger pathway. Basic Res. Cardiol.101, 159–167 (2006).
  • Sahach VF, Korkach Iu P, Kotsiuruba AV, Rudyk OV, Vavilova HL. [Mitochondrial permeability transition pore opening inhibition by ecdysterone in heart mitochondria of aging rats]. Fiziol. Zh.54, 3–10 (2008).
  • Xu Z, Park SS, Mueller RA, Bagnell RC, Patterson C, Boysen PG. Adenosine produces nitric oxide and prevents mitochondrial oxidant damage in rat cardiomyocytes. Cardiovasc. Res.65, 803–812 (2005).
  • Bijur GN, Jope RS. Rapid accumulation of Akt in mitochondria following phosphatidylinositol 3-kinase activation. J. Neurochem.87, 1427–1435 (2003).
  • Sasaki K, Sato M, Umezawa Y. Fluorescent indicators for Akt/protein kinase B and dynamics of Akt activity visualized in living cells. J. Biol. Chem.278, 30945–30951 (2003).
  • Piantadosi CA, Carraway MS, Babiker A, Suliman HB. Heme oxygenase-1 regulates cardiac mitochondrial biogenesis via Nrf2-mediated transcriptional control of nuclear respiratory factor-1. Circ. Res.103, 1232–1240 (2008).
  • Parcellier A, Tintignac LA, Zhuravleva E, Hemmings BA. PKB and the mitochondria: AKTing on apoptosis. Cell Signal20, 21–30 (2008).
  • Datta SR, Dudek H, Tao X et al. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell91, 231–241 (1997).
  • Pastukh V, Ricci C, Solodushko V, Mozaffari M, Schaffer SW. Contribution of the PI 3-kinase/Akt survival pathway toward osmotic preconditioning. Mol. Cell. Biochem.269, 59–67 (2005).
  • Kato K, Yin H, Agata J, Yoshida H, Chao L, Chao J. Adrenomedullin gene delivery attenuates myocardial infarction and apoptosis after ischemia and reperfusion. Am. J. Physiol. Heart Circ. Physiol.285, H1506–H1514 (2003).
  • Jonassen AK, Sack MN, Mjos OD, Yellon DM. Myocardial protection by insulin at reperfusion requires early administration and is mediated via Akt and p70s6 kinase cell-survival signaling. Circ. Res.89, 1191–1198 (2001).
  • Negoro S, Oh H, Tone E et al. Glycoprotein 130 regulates cardiac myocyte survival in doxorubicin-induced apoptosis through phosphatidylinositol 3-kinase/Akt phosphorylation and Bcl-xL/caspase-3 interaction. Circulation103, 555–561 (2001).
  • Kuwahara K, Saito Y, Kishimoto I et al. Cardiotrophin-1 phosphorylates akt and BAD, and prolongs cell survival via a PI3K-dependent pathway in cardiac myocytes. J. Mol. Cell. Cardiol.32, 1385–1394 (2000).
  • Le Bras M, Rouy I, Brenner C. The modulation of inter-organelle cross-talk to control apoptosis. Med. Chem.2, 1–12 (2006).
  • Robey RB, Hay N. Mitochondrial hexokinases: guardians of the mitochondria. Cell Cycle4, 654–658 (2005).
  • Robey RB, Hay N. Mitochondrial hexokinases, novel mediators of the antiapoptotic effects of growth factors and Akt. Oncogene25, 4683–4696 (2006).
  • Birnbaum MJ. On the InterAktion between hexokinase and the mitochondrion. Dev. Cell7, 781–782 (2004).
  • Majewski N, Nogueira V, Bhaskar P et al. Hexokinase-mitochondria interaction mediated by Akt is required to inhibit apoptosis in the presence or absence of Bax and Bak. Mol. Cell16, 819–830 (2004).
  • Majewski N, Nogueira V, Robey RB, Hay N. Akt inhibits apoptosis downstream of BID cleavage via a glucose-dependent mechanism involving mitochondrial hexokinases. Mol. Cell. Biol.24, 730–740 (2004).
  • Gottlob K, Majewski N, Kennedy S, Kandel E, Robey RB, Hay N. Inhibition of early apoptotic events by Akt/PKB is dependent on the first committed step of glycolysis and mitochondrial hexokinase. Genes Dev.15, 1406–1418 (2001).
  • Miyamoto S, Murphy AN, Brown JH. Akt mediates mitochondrial protection in cardiomyocytes through phosphorylation of mitochondrial hexokinase-II. Cell Death Differ.15(3), 521–529 (2008).
  • Walsh K. Akt signaling and growth of the heart. Circulation113, 2032–2034 (2006).
  • Shiraishi I, Melendez J, Ahn Y et al. Nuclear targeting of Akt enhances kinase activity and survival of cardiomyocytes. Circ. Res.94, 884–891 (2004).
  • Fujio Y, Nguyen T, Wencker D, Kitsis RN, Walsh K. Akt promotes survival of cardiomyocytes in vitro and protects against ischemia–reperfusion injury in mouse heart. Circulation101, 660–667 (2000).
  • Bullock AN, Debreczeni J, Amos AL, Knapp S, Turk BE. Structure and substrate specificity of the Pim-1 kinase. J. Biol. Chem.280, 41675–41682 (2005).
  • Hoover D, Friedmann M, Reeves R, Magnuson NS. Recombinant human Pim-1 protein exhibits serine/threonine kinase activity. J. Biol. Chem.266, 14018–14023 (1991).
  • Wang Z, Bhattacharya N, Weaver M et al. Pim-1: a serine/threonine kinase with a role in cell survival, proliferation, differentiation and tumorigenesis. J. Vet. Sci.2, 167–179 (2001).
  • Bachmann M, Moroy T. The serine/threonine kinase Pim-1. Int. J. Biochem. Cell Biol.37, 726–730 (2005).
  • Mally MI, Vogt M, Swift SE, Haas M. Oncogene expression in murine splenic T cells and in murine T-cell neoplasms. Virology144, 115–126 (1985).
  • Nagarajan L, Louie E, Tsujimoto Y, ar-Rushdi A, Huebner K, Croce CM. Localization of the human Pim oncogene (PIM) to a region of chromosome 6 involved in translocations in acute leukemias. Proc. Natl Acad. Sci. USA83, 2556–2560 (1986).
  • Meeker TC, Nagarajan L, ar-Rushdi A, Rovera G, Huebner K, Croce CM. Characterization of the human PIM-1 gene: a putative proto-oncogene coding for a tissue specific member of the protein kinase family. Oncogene Res.1, 87–101 (1987).
  • Stewart BE, Rice RH. Differentiation-associated expression of the proto-oncogene Pim-1 in cultured human keratinocytes. J. Invest. Dermatol.105, 699–703 (1995).
  • Liang H, Hittelman W, Nagarajan L. Ubiquitous expression and cell cycle regulation of the protein kinase PIM-1. Arch. Biochem. Biophys.330, 259–265 (1996).
  • Leduc I, Karsunky H, Mathieu N et al. The Pim-1 kinase stimulates maturation of TCRβ-deficient T cell progenitors: implications for the mechanism of Pim-1 action. Int. Immunol.12, 1389–1396 (2000).
  • Ellwood-Yen K, Graeber TG, Wongvipat J et al. Myc-driven murine prostate cancer shares molecular features with human prostate tumors. Cancer Cell4, 223–238 (2003).
  • Katakami N, Kaneto H, Hao H et al. Role of Pim-1 in smooth muscle cell proliferation. J. Biol. Chem.279, 54742–54749 (2004).
  • Matikainen S, Sareneva T, Ronni T, Lehtonen A, Koskinen PJ, Julkunen I. Interferon-α activates multiple STAT proteins and upregulates proliferation-associated IL-2Rα, c-myc, and Pim-1 genes in human T cells. Blood93, 1980–1991 (1999).
  • Paukku K, Silvennoinen O. STATs as critical mediators of signal transduction and transcription: lessons learned from STAT5. Cytokine Growth Factor Rev.15, 435–455 (2004).
  • Stout BA, Bates ME, Liu LY, Farrington NN, Bertics PJ. IL-5 and granulocyte-macrophage colony-stimulating factor activate STAT3 and STAT5 and promote Pim-1 and cyclin D3 protein expression in human eosinophils. J. Immunol.173, 6409–6417 (2004).
  • Krishnan N, Pan H, Buckley DJ, Buckley A. Prolactin-regulated Pim-1 transcription: identification of critical promoter elements and Akt signaling. Endocrine20, 123–130 (2003).
  • Aho TL, Sandholm J, Peltola KJ, Mankonen HP, Lilly M, Koskinen PJ. Pim-1 kinase promotes inactivation of the pro-apoptotic Bad protein by phosphorylating it on the Ser112 gatekeeper site. FEBS Lett.571, 43–49 (2004).
  • Yan B, Zemskova M, Holder S et al. The PIM-2 kinase phosphorylates BAD on serine 112 and reverses BAD-induced cell death. J. Biol. Chem.278, 45358–45367 (2003).
  • Amaravadi R, Thompson CB. The survival kinases Akt and Pim as potential pharmacological targets. J. Clin. Invest.115, 2618–2624 (2005).
  • Hammerman PS, Fox CJ, Birnbaum MJ, Thompson CB. Pim and Akt oncogenes are independent regulators of hematopoietic cell growth and survival. Blood105, 4477–4483 (2005).
  • Jacobs MD, Black J, Futer O et al. Pim-1 ligand-bound structures reveal the mechanism of serine/threonine kinase inhibition by LY294002. J. Biol. Chem.280, 13728–13734 (2005).
  • Kunkel MT, Ni Q, Tsien RY, Zhang J, Newton AC. Spatio–temporal dynamics of protein kinase B/Akt signaling revealed by a genetically encoded fluorescent reporter. J. Biol. Chem.280, 5581–5587 (2005).
  • Camper-Kirby D, Welch S, Walker A et al. Myocardial Akt activation and gender: increased nuclear activity in females versus males. Circ. Res.88, 1020–1027 (2001).
  • Muraski JA, Rota M, Misao Y et al. Pim-1 regulates cardiomyocyte survival downstream of Akt. Nat. Med.13, 1467–1475 (2007).
  • Muraski JA, Fischer KM, Wu W et al. Pim-1 kinase antagonizes aspects of myocardial hypertrophy and compensation to pathological pressure overload. Proc. Natl Acad. Sci. USA105, 13889–13894 (2008).
  • Fox CJ, Hammerman PS, Cinalli RM, Master SR, Chodosh LA, Thompson CB. The serine/threonine kinase Pim-2 is a transcriptionally regulated apoptotic inhibitor. Genes Dev.17, 1841–1854 (2003).
  • Kim KT, Levis M, Small D. Constitutively activated FLT3 phosphorylates BAD partially through Pim-1. Br. J. Haematol.134, 500–509 (2006).
  • Lilly M, Sandholm J, Cooper JJ, Koskinen PJ, Kraft A. The PIM-1 serine kinase prolongs survival and inhibits apoptosis-related mitochondrial dysfunction in part through a bcl-2-dependent pathway. Oncogene18, 4022–4031 (1999).
  • Condorelli G, Drusco A, Stassi G et al. Akt induces enhanced myocardial contractility and cell size in vivo in transgenic mice. Proc. Natl Acad. Sci. USA99, 12333–12338 (2002).
  • Matsui T, Li L, Wu JC, Cook SA et al. Phenotypic spectrum caused by transgenic overexpression of activated Akt in the heart. J. Biol. Chem.277, 22896–22901 (2002).
  • Matsui T, Nagoshi T, Hong EG et al. Effects of chronic Akt activation on glucose uptake in the heart. Am. J. Physiol. Endocrinol. Metab.290, E789–E797 (2006).
  • Nagoshi T, Matsui T, Aoyama T et al. PI3K rescues the detrimental effects of chronic Akt activation in the heart during ischemia/reperfusion injury. J. Clin. Invest.115, 2128–2138 (2005).
  • Shiojima I, Sato K, Izumiya Y et al. Disruption of coordinated cardiac hypertrophy and angiogenesis contributes to the transition to heart failure. J. Clin. Invest.115, 2108–2118 (2005).
  • Shioi T, McMullen JR, Kang PM et al. Akt/protein kinase B promotes organ growth in transgenic mice. Mol. Cell. Biol.22, 2799–2809 (2002).
  • Grandemange S, Herzig S, Martinou JC. Mitochondrial dynamics and cancer. Semin. Cancer Biol.19(1), 50–56 (2009).
  • Herzig S, Martinou JC. Mitochondrial dynamics: to be in good shape to survive. Curr. Mol. Med.8, 131–137 (2008).
  • Westermann B. Molecular machinery of mitochondrial fusion and fission. J. Biol. Chem.283, 13501–13505 (2008).
  • Berman SB, Pineda FJ, Hardwick JM. Mitochondrial fission and fusion dynamics: the long and short of it. Cell Death Differ.15, 1147–1152 (2008).
  • Devenish RJ. Mitophagy: growing in intricacy. Autophagy3, 293–294 (2007).
  • Lemasters JJ. Selective mitochondrial autophagy, or mitophagy, as a targeted defense against oxidative stress, mitochondrial dysfunction, and aging. Rejuvenation Res.8, 3–5 (2005).
  • Mijaljica D, Prescott M, Devenish RJ. Different fates of mitochondria: alternative ways for degradation? Autophagy3, 4–9 (2007).
  • Miyamoto S, Rubio M, Sussman MA. Nuclear and mitochondrial signalling Akts in cardiomyocytes. Cardiovasc. Res.82(2), 272–285 (2009).
  • White E. The Pims and outs of survival signaling: role for the Pim-2 protein kinase in the suppression of apoptosis by cytokines. Genes Dev.17, 1813–1816 (2003).

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