Partial liver kinase B1 (LKB1) deficiency promotes diastolic dysfunction, De Novo systolic dysfunction, apoptosis, and mitochondrial dysfunction with dietary metabolic challenge

Journal of the American Heart Association

Volumn 5, Issue 1, 2016, Pages

  Miller, Edward J ^a   Calamaras, Timothy ^a   Elezaby, Aly ^a   Sverdlov, Aaron ^a   Qin, Fuzhong ^a   Luptak, Ivan ^a   Wang, Ke ^a   Sun, Xinxin ^a   Vijay, Andrea ^a   Croteau, Dominique ^a   Bachschmid, Markus ^a   Cohen, Richard A ^a   Walsh, Kenneth ^a   Colucci, Wilson S ^a  

^a BOSTON MEDICAL CENTER   (United States)

Author keywords

Diabetes mellitus; Heart failure; Metabolism; Obesity

Indexed keywords

CASPASE 3; LIVER ENZYME; LIVER KINASE B1; PUMA PROTEIN; UNCLASSIFIED DRUG; APOPTOSIS REGULATORY PROTEIN; CASP3 PROTEIN, MOUSE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; PROTEIN P53; PROTEIN SERINE THREONINE KINASE; PUMA PROTEIN, MOUSE; STK11 PROTEIN, MOUSE; SUGAR INTAKE; TUMOR SUPPRESSOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DIASTOLIC DYSFUNCTION; DIETARY INTAKE; DISEASE COURSE; DISEASE SEVERITY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENZYME DEFICIENCY; HEART DILATATION; HEART LEFT VENTRICLE EJECTION FRACTION; HEART LEFT VENTRICLE HYPERTROPHY; HEART PROTECTION; LIPID DIET; MALE; METABOLIC STRESS; MOUSE; MYOCARDIAL DISEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SUGAR INTAKE; SYSTOLIC DYSFUNCTION; WILD TYPE; ANIMAL; CARDIAC MUSCLE; DEFICIENCY; DIASTOLE; DISEASE MODEL; ENZYMOLOGY; GENETIC PREDISPOSITION; GENETICS; HEART LEFT VENTRICLE FUNCTION; HEART MITOCHONDRION; HEART VENTRICLE REMODELING; HETEROZYGOTE; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHENOTYPE; SIGNAL TRANSDUCTION; SYSTOLE; TIME FACTOR;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CASPASE 3; DIASTOLE; DIET, HIGH-FAT; DIETARY SUCROSE; DISEASE MODELS, ANIMAL; GENETIC PREDISPOSITION TO DISEASE; HETEROZYGOTE; HYPERTROPHY, LEFT VENTRICULAR; MICE, KNOCKOUT; MITOCHONDRIA, HEART; MYOCARDIUM; PHENOTYPE; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; SYSTOLE; TIME FACTORS; TUMOR SUPPRESSOR PROTEIN P53; TUMOR SUPPRESSOR PROTEINS; VENTRICULAR DYSFUNCTION, LEFT; VENTRICULAR FUNCTION, LEFT; VENTRICULAR REMODELING;

EID: 84997724677     PISSN: None     EISSN: 20479980     Source Type: Journal    
DOI: 10.1161/JAHA.115.002277     Document Type: Article

References (30)

1. Korsse SE, Peppelenbosch MP, van Veelen W. Targeting LKB1 signaling in cancer. Biochim Biophys Acta. 2013;1835:194-210.
2. Alessi DR, Sakamoto K, Bayascas JR. LKB1-dependent signaling pathways. Annu Rev Biochem. 2006;75:137-163.
3. Lizcano JM, Goransson O, Toth R, Deak M, Morrice NA, Boudeau J, Hawley SA, Udd L, Makela TP, Hardie DG, Alessi DR. LKB1 is a master kinase that activates 13 kinases of the AMPK subfamily, including MARK/PAR-1. EMBO J. 2004;23:833-843.
4. Sakamoto K, Zarrinpashneh E, Budas GR, Pouleur AC, Dutta A, Prescott AR, Vanoverschelde JL, Ashworth A, Jovanovic A, Alessi DR, Bertrand L. Deficiency of LKB1 in heart prevents ischemia-mediated activation of AMPKalpha2 but not AMPKalpha1. Am J Physiol Endocrinol Metab. 2006;290:E780-E788.
5. Russell RR III, Li J, Coven DL, Pypaert M, Zechner C, Palmeri M, Giordano FJ, Mu J, Birnbaum MJ, Young LH. AMP-activated protein kinase mediates ischemic glucose uptake and prevents postischemic cardiac dysfunction, apoptosis, and injury. J Clin Invest. 2004;114:495-503.
6. Turdi S, Kandadi MR, Zhao J, Huff AF, Du M, Ren J. Deficiency in AMP-activated protein kinase exaggerates high fat diet-induced cardiac hypertrophy and contractile dysfunction. J Mol Cell Cardiol. 2011;50:712-722.
7. Dolinsky VW, Chan AY, Robillard Frayne I, Light PE, Rosiers Des C, Dyck JR. Resveratrol prevents the prohypertrophic effects of oxidative stress on LKB1. Circulation. 2009;119:1643-1652.
8. Shao D, Oka S-I, Liu T, Zhai P, Ago T, Sciarretta S, Li H, Sadoshima J. A redoxdependent mechanism for regulation of AMPK activation by Thioredoxin1 during energy starvation. Cell Metab. 2014;19:232-245.
9. Rines AK, Burke MA, Fernandez RP, Volpert OV, Ardehali H. Snf1-related kinase inhibits colon cancer cell proliferation through calcyclin-binding proteindependent reduction of β-catenin. FASEB J. 2012;26:4685-4695.
10. Koh HJ, Toyoda T, Fujii N, Jung MM, Rathod A, Middelbeek RJW, Lessard SJ, Treebak JT, Tsuchihara K, Esumi H, Richter EA, Wojtaszewski JFP, Hirshman MF, Goodyear LJ. Sucrose nonfermenting AMPK-related kinase (SNARK) mediates contraction-stimulated glucose transport in mouse skeletal muscle. Proc Natl Acad Sci USA. 2010;107:15541-15546.
11. Qin F, Siwik DA, Luptak I, Hou X, Wang L, Higuchi A, Weisbrod RM, Ouchi N, Tu VH, Calamaras TD, Miller EJ, Verbeuren TJ, Walsh K, Cohen RA, Colucci WS. The polyphenols resveratrol and S17834 prevent the structural and functional sequelae of diet-induced metabolic heart disease in mice. Circulation. 2012;125:1757-1764.
12. Calamaras TD, Lee C, Lan F, Ido Y, Siwik DA, Colucci WS. Post-translational modification of serine/threonine kinase LKB1 via adduction of the reactive lipid species 4-hydroxy-trans-2-nonenal (HNE) at lysine residue 97 directly inhibits kinase activity. J Biol Chem. 2012;287:42400-42406.
13. Weisbrod RM, Shiang T, Al Sayah L, Fry JL, Bajpai S, Reinhart-King CA, Lob HE, Santhanam L, Mitchell G, Cohen RA, Seta F. Arterial stiffening precedes systolic hypertension in diet-induced obesity. Hypertension. 2013;62:1105-1110.
14. Ikeda Y, Sato K, Pimentel DR, Sam F, Shaw RJ, Dyck JR, Walsh K. Cardiacspecific deletion of LKB1 leads to hypertrophy and dysfunction. J Biol Chem. 2009;284:35839-35849.
15. Sverdlov AL, Elezaby A, Behring JB, Bachschmid MM, Luptak I, Tu VH, Siwik DA, Miller EJ, Liesa M, Shirihai OS, Pimentel DR, Cohen RA, Colucci WS. High fat, high sucrose diet causes cardiac mitochondrial dysfunction due in part to oxidative post-translational modification of mitochondrial complex II. J Mol Cell Cardiol. 2015;78:165-173.
16. Qin F, Lennon-Edwards S, Lancel S, Biolo A, Siwik DA, Pimentel DR, Dorn GW, Kang YJ, Colucci WS. Cardiac-specific overexpression of catalase identifies hydrogen peroxide-dependent and-independent phases of myocardial remodeling and prevents the progression to overt heart failure in G(alpha)qoverexpressing transgenic mice. Circ Heart Fail. 2010;3:306-313.
17. Elezaby A, Sverdlov AL, Tu VH, Soni K, Luptak I, Qin F, Liesa M, Shirihai OS, Rimer J, Schaffer JE, Wilson SC, Colucci WS, Edward JM, Miller EJ. Mitochondrial remodeling in mice with cardiomyocyte-specific lipid overload. J Mol Cell Cardiol. 2015;79:275-283.
18. 2 mediates hypertrophy, apoptosis, and decreased SERCA activity in mice with chronic hemodynamic overload. Am J Physiol Heart Circ Physiol. 2014;306:H1453-H1463.
19. Bright NJ, Thornton C, Carling D. The regulation and function of mammalian AMPK-related kinases. Acta Physiol. 2009;196:15-26.
20. Yoshida K, Yamada M, Nishio C, Konishi A, Hatanaka H. SNRK, a member of the SNF1 family, is related to low K(+)-induced apoptosis of cultured rat cerebellar granule neurons. Brain Res. 2000;873:274-282.
21. Cossette SM, Gastonguay AJ, Bao X, Lerch-Gaggl A, Zhong L, Harmann LM, Koceja C, Miao RQ, Vakeel P, Chun C, Li K, Foeckler J, Bordas M, Weiler H, Strande J, Palecek SP, Ramchandran R. Sucrose non-fermenting related kinase enzyme is essential for cardiac metabolism. Biol Open. 2014;4:48-61.
22. Finucane MM, Stevens GA, Cowan MJ, Danaei G, Lin JK, Paciorek CJ, Singh GM, Gutierrez HR, Lu Y, Bahalim AN, Farzadfar F, Riley LM, Ezzati M; Global Burden of Metabolic Risk Factors of Chronic Diseases Collaborating Group (Body Mass Index). National, regional, and global trends in body-mass index since 1980: systematic analysis of health examination surveys and epidemiological studies with 960 country-years and 9.1 million participants. Lancet. 2011;377:557-567.
23. Ho JE, Lyass A, Lee DS, Vasan RS, Kannel WB, Larson MG, Levy D. Predictors of new-onset heart failure: differences in preserved versus reduced ejection fraction. Circ Heart Fail. 2013;6:279-286.
24. Jaleel M, McBride A, Lizcano JM, Deak M, Toth R, Morrice NA, Alessi DR. Identification of the sucrose non-fermenting related kinase SNRK, as a novel LKB1 substrate. FEBS Lett. 2005;579:1417-1423.
25. Jessen N, Koh H-J, Folmes CD, Wagg C, Fujii N, Løfgren B, Wolf CM, Berul CI, Hirshman MF, Lopaschuk GD. Ablation of LKB1 in the heart leads to energy deprivation and impaired cardiac function. Biochim Biophys Acta. 2010;1802:593-600.
26. Athéa Y, Viollet B, Mateo P, Rousseau D, Novotova M, Garnier A, Vaulont S, Wilding JR, Grynberg A, Veksler V, Hoerter J, Ventura-Clapier R. AMP-activated protein kinase alpha2 deficiency affects cardiac cardiolipin homeostasis and mitochondrial function. Diabetes. 2007;56:786-794.
27. Barreto-Torres G, Soto Hernandez J, Jang S, Rodríguez-Muñoz AR, Torres-Ramos CA, Basnakian AG, Javadov S. The beneficial effects of AMP-kinase activation against oxidative stress are associated with prevention of PPARγcyclophilin D interaction in cardiomyocytes. Am J Physiol Heart Circ Physiol. 2015;308:H758.
28. Karuman P, Gozani O, Odze RD, Zhou XC, Zhu H, Shaw R, Brien TP, Bozzuto CD, Ooi D, Cantley LC, Yuan J. The Peutz-Jegher gene product LKB1 is a mediator of p53-dependent cell death. Mol Cell. 2001;7:1307-1319.
29. Nelson LE, Valentine RJ, Cacicedo JM, Gauthier MS, Ido Y, Ruderman NB. A novel inverse relationship between metformin-triggered AMPK-SIRT1 signaling and p53 protein abundance in high glucose-exposed HepG2 cells. Am J Physiol Cell Physiol. 2012;303:C4-C13.
30. Ghillebert R, Swinnen E, Wen J, Vandesteene L, Ramon M, Norga K, Rolland F, Winderickx J. The AMPK/SNF1/SnRK1 fuel gauge and energy regulator: structure, function and regulation. FEBS J. 2011;278:3978-3990.