Ablation of Akt2 protects against lipopolysaccharide-induced cardiac dysfunction: Role of Akt ubiquitination E3 ligase TRAF6

Journal of Molecular and Cellular Cardiology

Volumn 74, Issue , 2014, Pages 76-87

  Zhang, Yingmei ^a,b,c   Xu, Xihui ^c   Ceylan Isik, Asli F ^c   Dong, Maolong ^a,c   Pei, Zhaohui ^d   Li, Yan ^a   Ren, Jun ^b,c  

^a FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^b FUDAN UNIVERSITY   (China)

^c UNIVERSITY OF WYOMING COLLEGE OF HEALTH SCIENCES   (United States)

^d Third Hospital of Nanchang   (China)

Author keywords

Apoptosis; Cardiac function; Lipopolysaccharide; TRAF6; Ubiquitination

Indexed keywords

CASPASE 12; CASPASE 3; GLYCOGEN SYNTHASE KINASE 3BETA; PROTEIN KINASE B BETA; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6; AKT2 PROTEIN, MOUSE; ALDEHYDE DEHYDROGENASE; ALDEHYDE DEHYDROGENASE 2, MOUSE; CASPASE; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA; LIPOPOLYSACCHARIDE; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN KINASE B; SMALL INTERFERING RNA; TLR4 PROTEIN, MOUSE; UBIQUITIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CALCIUM CELL LEVEL; CELL STRESS; CONTROLLED STUDY; DOWN REGULATION; ECHOCARDIOGRAPHY; ENZYME INHIBITION; HEART ARRHYTHMIA; HEART MUSCLE CELL; HEART PROTECTION; KNOCKOUT MOUSE; MALE; MITOCHONDRIAL MEMBRANE POTENTIAL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; UBIQUITINATION; UPREGULATION; WILD TYPE; ANIMAL; ANTAGONISTS AND INHIBITORS; CARDIOMYOPATHY; CHEMICALLY INDUCED; DEFICIENCY; GENE EXPRESSION REGULATION; GENETICS; HEART CONTRACTION; HEART MUSCLE; METABOLISM; PATHOLOGY;

ALDEHYDE DEHYDROGENASE; ANIMALS; APOPTOSIS; CARDIOMYOPATHIES; CASPASES; GENE EXPRESSION REGULATION; GLYCOGEN SYNTHASE KINASE 3; LIPOPOLYSACCHARIDES; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MICE, KNOCKOUT; MYOCARDIAL CONTRACTION; MYOCARDIUM; MYOCYTES, CARDIAC; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PROTO-ONCOGENE PROTEINS C-AKT; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TNF RECEPTOR-ASSOCIATED FACTOR 6; TOLL-LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR-ALPHA; UBIQUITIN;

EID: 84904737046     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2014.04.020     Document Type: Article

References (46)

1. Angus D.C., Pereira C.A., Silva E. Epidemiology of severe sepsis around the world. Endocr Metab Immune Disord Drug Targets 2006, 6:207-212.
2. Angus D.C., Wax R.S. Epidemiology of sepsis: an update. Crit Care Med 2001, 29:S109-S116.
3. Opal S.M., Scannon P.J., Vincent J.L., et al. Relationship between plasma levels of lipopolysaccharide (LPS) and LPS-binding protein in patients with severe sepsis and septic shock. J Infect Dis 1999, 180:1584-1589.
4. Lin X.W., Xu W.C., Luo J.G., et al. WW domain containing E3 ubiquitin protein ligase 1 (WWP1) negatively regulates TLR4-mediated TNF-alpha and IL-6 production by proteasomal degradation of TNF receptor associated factor 6 (TRAF6). PLoS One 2013, 8:e67633.
5. Medzhitov R., Preston-Hurlburt P., Kopp E., et al. MyD88 is an adaptor protein in the hToll/IL-1 receptor family signaling pathways. Mol Cell 1998, 2:253-258.
6. Ward P.A. The sepsis seesaw: seeking a heart salve. Nat Med 2009, 15:497-498.
7. Ren J., Wu S. A burning issue: do sepsis and systemic inflammatory response syndrome (SIRS) directly contribute to cardiac dysfunction?. Front Biosci 2006, 11:15-22.
8. 2+ in cardiac myocytes. Circ Res 1997, 81:1011-1020.
9. Zhang W.J., Wei H., Frei B. Genetic deficiency of NADPH oxidase does not diminish, but rather enhances, LPS-induced acute inflammatory responses in vivo. Free Radic Biol Med 2009, 46:791-798.
10. Ben-Shaul V., Lomnitski L., Nyska A., Zurovsky Y., Bergman M., Grossman S. The effect of natural antioxidants, NAO and apocynin, on oxidative stress in the rat heart following LPS challenge. Toxicol Lett 2001, 123:1-10.
11. Fiers W., Beyaert R., Declercq W., Vandenabeele P. More than one way to die: apoptosis, necrosis and reactive oxygen damage. Oncogene 1999, 18:7719-7730.
12. Sakon S., Xue X., Takekawa M., et al. NF-kappaB inhibits TNF-induced accumulation of ROS that mediate prolonged MAPK activation and necrotic cell death. EMBO J 2003, 22:3898-3909.
13. Ceylan-Isik A.F., Zhao P., Zhang B., Xiao X., Su G., Ren J. Cardiac overexpression of metallothionein rescues cardiac contractile dysfunction and endoplasmic reticulum stress but not autophagy in sepsis. J Mol Cell Cardiol 2010, 48:367-378.
14. Zhao P., Turdi S., Dong F., et al. Cardiac-specific overexpression of insulin-like growth factor I (IGF-1) rescues lipopolysaccharide-induced cardiac dysfunction and activation of stress signaling in murine cardiomyocytes. Shock 2009, 32:100-107.
15. Yao Y.W., Zhang G.H., Zhang Y.Y., et al. Lipopolysaccharide pretreatment protects against ischemia/reperfusion injury via increase of HSP70 and inhibition of NF-kappaB. Cell Stress Chaperones 2011, 16:287-296.
16. Hotchkiss R.S., Karl I.E. The pathophysiology and treatment of sepsis. N Engl J Med 2003, 348:138-150.
17. Hers I., Vincent E.E., Tavare J.M. Akt signalling in health and disease. Cell Signal 2011, 23:1515-1527.
18. Zhang Y., Xia Z., La Cour K.H., Ren J. Activation of Akt rescues endoplasmic reticulum stress-impaired murine cardiac contractile function via glycogen synthase kinase-3beta-mediated suppression of mitochondrial permeation pore opening. Antioxid Redox Signal 2011, 15:2407-2424.
19. Dong M., Hu N., Hua Y., et al. Chronic Akt activation attenuated lipopolysaccharide-induced cardiac dysfunction via Akt/GSK3beta-dependent inhibition of apoptosis and ER stress. Biochim Biophys Acta 1832, 2013:848-863.
20. Jiang S., Zhu W., Li C., et al. Alpha-lipoic acid attenuates LPS-induced cardiac dysfunction through a PI3K/Akt-dependent mechanism. Int Immunopharmacol 2013, 16:100-107.
21. Ha T., Hua F., Liu X., et al. Lipopolysaccharide-induced myocardial protection against ischaemia/reperfusion injury is mediated through a PI3K/Akt-dependent mechanism. Cardiovasc Res 2008, 78:546-553.
22. Yao Y., Zhang F., Wang L., et al. Lipopolysaccharide preconditioning enhances the efficacy of mesenchymal stem cells transplantation in a rat model of acute myocardial infarction. J Biomed Sci 2009, 16:74.
23. Roe N.D., Ren J. Akt2 knockout mitigates chronic iNOS inhibition-induced cardiomyocyte atrophy and contractile dysfunction despite persistent insulin resistance. Toxicol Lett 2011, 207:222-231.
24. Xu X., Hua Y., Nair S., Zhang Y., Ren J. Akt2 knockout preserves cardiac function in high-fat diet-induced obesity by rescuing cardiac autophagosome maturation. J Mol Cell Biol 2013, 5:61-63.
25. Verstak B., Nagpal K., Bottomley S.P., Golenbock D.T., Hertzog P.J., Mansell A. MyD88 adapter-like (Mal)/TIRAP interaction with TRAF6 is critical for TLR2- and TLR4-mediated NF-kappaB proinflammatory responses. J Biol Chem 2009, 284:24192-24203.
26. Ma J., Bang B.R., Lu J., et al. The TNF family member 4-1BBL sustains inflammation by interacting with TLR signaling components during late-phase activation. Sci Signal 2013, 6:ra87.
27. Xia M., Liu J., Wu X., et al. Histone methyltransferase Ash1l suppresses interleukin-6 production and inflammatory autoimmune diseases by inducing the ubiquitin-editing enzyme A20. Immunity 2013, 39:470-481.
28. Yang W.L., Wang J., Chan C.H., et al. The E3 ligase TRAF6 regulates Akt ubiquitination and activation. Science 2009, 325:1134-1138.
29. Jakus P.B., Kalman N., Antus C., et al. TRAF6 is functional in inhibition of TLR4-mediated NF-kappaB activation by resveratrol. J Nutr Biochem 2013, 24:819-823.
30. Cho H., Mu J., Kim J.K., et al. Insulin resistance and a diabetes mellitus-like syndrome in mice lacking the protein kinase Akt2 (PKB beta). Science 2001, 292:1728-1731.
31. Peng T., Lu X., Feng Q. Pivotal role of gp91phox-containing NADH oxidase in lipopolysaccharide-induced tumor necrosis factor-alpha expression and myocardial depression. Circulation 2005, 111:1637-1644.
32. Manning W.J., Wei J.Y., Katz S.E., Litwin S.E., Douglas P.S. In vivo assessment of LV mass in mice using high-frequency cardiac ultrasound: necropsy validation. Am J Physiol 1994, 266:H1672-H1675.
33. Doser T.A., Turdi S., Thomas D.P., Epstein P.N., Li S.Y., Ren J. Transgenic overexpression of aldehyde dehydrogenase-2 rescues chronic alcohol intake-induced myocardial hypertrophy and contractile dysfunction. Circulation 2009, 119:1941-1949.
34. Cheng Y.C., Chen L.M., Chang M.H., et al. Lipopolysaccharide upregulates uPA, MMP-2 and MMP-9 via ERK1/2 signaling in H9c2 cardiomyoblast cells. Mol Cell Biochem 2009, 325:15-23.
35. Zhang B., Turdi S., Li Q., et al. Cardiac overexpression of insulin-like growth factor 1 attenuates chronic alcohol intake-induced myocardial contractile dysfunction but not hypertrophy: roles of Akt, mTOR, GSK3beta, and PTEN. Free Radic Biol Med 2010, 49:1238-1253.
36. Zhang Y., Babcock S.A., Hu N., Maris J.R., Wang H., Ren J. Mitochondrial aldehyde dehydrogenase (ALDH2) protects against streptozotocin-induced diabetic cardiomyopathy: role of GSK3beta and mitochondrial function. BMC Med 2012, 10:40.
37. Adebiyi A., Narayanan D., Jaggar J.H. Caveolin-1 assembles type 1 inositol 1,4,5-trisphosphate receptors and canonical transient receptor potential 3 channels into a functional signaling complex in arterial smooth muscle cells. J Biol Chem 2011, 286:4341-4348.
38. Rivers E., Nguyen B., Havstad S., et al. Early goal-directed therapy in the treatment of severe sepsis and septic shock. N Engl J Med 2001, 345:1368-1377.
39. Niederbichler A.D., Westfall M.V., Su G.L., et al. Cardiomyocyte function after burn injury and lipopolysaccharide exposure: single-cell contraction analysis and cytokine secretion profile. Shock 2006, 25:176-183.
40. Ren J., Ren B.H., Sharma A.C. Sepsis-induced depressed contractile function of isolated ventricular myocytes is due to altered calcium transient properties. Shock 2002, 18:285-288.
41. Obata T., Brown G.E., Yaffe M.B. MAP kinase pathways activated by stress: the p38 MAPK pathway. Crit Care Med 2000, 28:N67-N77.
42. Joshi M.S., Julian M.W., Huff J.E., Bauer J.A., Xia Y., Crouser E.D. Calcineurin regulates myocardial function during acute endotoxemia. Am J Respir Crit Care Med 2006, 173:999-1007.
43. Liu H., Tamashiro S., Baritaki S., et al. TRAF6 activation in multiple myeloma: a potential therapeutic target. Clin Lymphoma Myeloma Leuk 2012, 12:155-163.
44. Cui Z., Scruggs S.B., Gilda J.E., Ping P., Gomes A.V. Regulation of cardiac proteasomes by ubiquitination, SUMOylation, and beyond. J Mol Cell Cardiol 2014, 71C:32-42.
45. Sixt S.U., Dahlmann B. Extracellular, circulating proteasomes and ubiquitin - incidence and relevance. Biochim Biophys Acta 2008, 1782:817-823.
46. Zhan Z., Xie X., Cao H., et al. Autophagy facilitates TLR4- and TLR3-triggered migration and invasion of lung cancer cells through the promotion of TRAF6 ubiquitination. Autophagy 2014, 10:257-268.