Transgenic knockdown of cardiac sodium/glucose cotransporter 1 (SGLT1) attenuates PRKAG2 cardiomyopathy, whereas transgenic overexpression of cardiac SGLT1 causes pathologic hypertrophy and dysfunction in mice

Journal of the American Heart Association

Volumn 3, Issue 4, 2014, Pages

  Ramratnam, Mohun ^a,b   Sharma, Ravi K ^b   D'Auria, Stephen ^b   Lee, So Jung ^b   Wang, David ^b   Huang, Xue Yin N ^b   Ahmad, Ferhaan ^b,c,d  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

^c UNIVERSITY OF PITTSBURGH   (United States)

^d UNIVERSITY OF IOWA   (United States)

Author keywords

Cardiomyopathy; Glucose; Heart failure; Hypertrophy

Indexed keywords

COMPLEMENTARY DNA; GLYCOGEN; RNA; SODIUM GLUCOSE COTRANSPORTER 1; GLUCOSE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MESSENGER RNA; PRKAG2 PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CARDIOMYOPATHY; CONTROLLED STUDY; FEMALE; GENE; GENOTYPE; HEART HYPERTROPHY; HEART LEFT VENTRICLE FAILURE; HEART MUSCLE CELL; HEART MUSCLE FIBROSIS; HEART WEIGHT; HISTOPATHOLOGY; MALE; MOUSE; MUSCLE CELL; MUTANT; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PRKAG2 CARDIOMYOPATHY; PRKAG2 GENE; PROTEIN ANALYSIS; PROTEIN EXPRESSION; RNA ANALYSIS; RNA INTERFERENCE; TRANSGENIC MOUSE; TRANSTHORACIC ECHOCARDIOGRAPHY; WILD TYPE; ANIMAL; DANON DISEASE; DISEASE MODEL; GENETICS; HEART LEFT VENTRICLE FUNCTION; HEART LEFT VENTRICLE HYPERTROPHY; METABOLISM;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; CARDIOMYOPATHIES; DISEASE MODELS, ANIMAL; GLUCOSE; GLYCOGEN STORAGE DISEASE TYPE IIB; HYPERTROPHY, LEFT VENTRICULAR; MICE; MICE, TRANSGENIC; RNA, MESSENGER; SODIUM-GLUCOSE TRANSPORTER 1; VENTRICULAR DYSFUNCTION, LEFT;

EID: 84921312956     PISSN: None     EISSN: 20479980     Source Type: Journal    
DOI: 10.1161/JAHA.114.000899     Document Type: Article

References (23)

1. Kemp BE, Mitchelhill KI, Stapleton D, Michell BJ, Chen ZP, Witters LA. Dealing with energy demand: the AMP-activated protein kinase. Trends Biochem Sci. 1999;24:22-25.
2. Hardie DG. Minireview: the AMP-activated protein kinase cascade: the key sensor of cellular energy status. Endocrinology. 2003;144:5179-5183.
3. Arad M, Benson DW, Perez-Atayde AR, McKenna WJ, Sparks EA, Kanter RJ, McGarry K, Seidman JG, Seidman CE. Constitutively active AMP kinase mutations cause glycogen storage disease mimicking hypertrophic cardiomyopathy. J Clin Invest. 2002;109:357-362.
4. Banerjee SK, Ramani R, Saba S, Rager J, Tian R, Mathier MA, Ahmad F. A PRKAG2 mutation causes biphasic changes in myocardial AMPK activity and does not protect against ischemia. Biochem Biophys Res Commun. 2007;360:381-387.
5. Arad M, Moskowitz IP, Patel VV, Ahmad F, Perez-Atayde AR, Sawyer DB, Walter M, Li GH, Burgon PG, Maguire CT, Stapleton D, Schmitt JP, Guo XX, Pizard A, Kuperchmidt S, Roden DM, Berul CI, Seidman CE, Seidman JG. Transgenic mice overexpressing mutant PRKAG2 define the cause of Wolff-Parkinson-White syndrome in glycogen storage cardiomyopathy. Circulation. 2003;107:2850-2856.
6. Sidhu JS, Rajawat YS, Rami TG, Gollob MH, Wang Z, Yuan R, Marian AJ, DeMayo FJ, Weilbacher D, Taffet GE, Davies JK, Carling D, Khoury DS, Roberts R. Transgenic mouse model of ventricular preexcitation and atrioventricular reentrant tachycardia induced by an AMP-activated protein kinase loss-offunction mutation responsible for Wolff-Parkinson-White syndrome. Circulation. 2005;111:21-29.
7. Davies JK, Wells DJ, Liu K, Whitrow HR, Daniel TD, Grignani R, Lygate CA, Schneider JE, Noel G, Watkins H, Carling D. Characterization of the role of gamma2 R531G mutation in AMP-activated protein kinase in cardiac hypertrophy and Wolff-Parkinson-White syndrome. Am J Physiol Heart Circ Physiol. 2006;290:H1942-H1951.
8. Luptak I, Shen M, He H, Hirshman MF, Musi N, Goodyear LJ, Yan J, Wakimoto H, Morita H, Arad M, Seidman CE, Seidman JG, Ingwall JS, Balschi JA, Tian R. Aberrant activation of AMP-activated protein kinase remodels metabolic network in favor of cardiac glycogen storage. J Clin Invest. 2007;117:1432-1439.
9. Banerjee SK, McGaffin KR, Huang XN, Ahmad F. Activation of cardiac hypertrophic signaling pathways in a transgenic mouse with the human PRKAG2 Thr400Asn mutation. Biochim Biophys Acta. 2010;1802:284-291.
10. Kim M, Hunter RW, Garcia-Menendez L, Gong G, Yang YY, Kolwicz SC Jr, Xu J, Sakamoto K, Wang W, Tian R. Mutation in the gamma2-subunit of AMPactivated protein kinase stimulates cardiomyocyte proliferation and hypertrophy independent of glycogen storage. Cir Res. 2014;114:966-975.
11. Schwenk RW, Luiken JJ, Bonen A, Glatz JF. Regulation of sarcolemmal glucose and fatty acid transporters in cardiac disease. Cardiovasc Res. 2008;79:249-258.
12. Banerjee SK, McGaffin KR, Pastor-Soler NM, Ahmad F. SGLT1 is a novel cardiac glucose transporter that is perturbed in disease states. Cardiovasc Res. 2009;84:111-118.
13. Banerjee SK, Wang DW, Alzamora R, Huang XN, Pastor-Soler NM, Hallows KR, McGaffin KR, Ahmad F. SGLT1, a novel cardiac glucose transporter, mediates increased glucose uptake in PRKAG2 cardiomyopathy. J Mol Cell Cardiol. 2010;49:683-692.
14. Claycomb WC, Lanson NA Jr, Stallworth BS, Egeland DB, Delcarpio JB, Bahinski A, Izzo NJ Jr. HL-1 cells: a cardiac muscle cell line that contracts and retains phenotypic characteristics of the adult cardiomyocyte. Proc Natl Acad Sci USA. 1998;95:2979-2984.
15. Gulick J, Subramaniam A, Neumann J, Robbins J. Isolation and characterization of the mouse cardiac myosin heavy chain genes. J Biol Chem. 1991;266:9180-9185.
16. Ahmad F, Banerjee SK, Lage ML, Huang XN, Smith SH, Saba S, Rager J, Conner DA, Janczewski AM, Tobita K, Tinney JP, Moskowitz IP, Perez-Atayde AR, Keller BB, Mathier MA, Shroff SG, Seidman CE, Seidman JG. The role of cardiac troponin T quantity and function in cardiac development and dilated cardiomyopathy. PLoS ONE. 2008;3:e2642.
17. Sanbe A, Gulick J, Hanks MC, Liang Q, Osinska H, Robbins J. Reengineering inducible cardiac-specific transgenesis with an attenuated myosin heavy chain promoter. Cir Res. 2003;92:609-616.
18. Ahmad F, Arad M, Musi N, He H, Wolf C, Branco D, Perez-Atayde AR, Stapleton D, Bali D, Xing Y, Tian R, Goodyear LJ, Berul CI, Ingwall JS, Seidman CE, Seidman JG. Increased alpha2 subunit-associated AMPK activity and PRKAG2 cardiomyopathy. Circulation. 2005;112:3140-3148.
19. Abel ED, Kaulbach HC, Tian R, Hopkins JC, Duffy J, Doetschman T, Minnemann T, Boers ME, Hadro E, Oberste-Berghaus C, Quist W, Lowell BB, Ingwall JS, Kahn BB. Cardiac hypertrophy with preserved contractile function after selective deletion of GLUT4 from the heart. J Clin Invest. 1999;104:1703-1714.
20. Wright EM. Renal Na(+)-glucose cotransporters. Am J Physiol Renal Physiol. 2001;280:F10-F18.
21. von Lewinski D, Gasser R, Rainer PP, Huber MS, Wilhelm B, Roessl U, Haas T, Wasler A, Grimm M, Bisping E, Pieske B. Functional effects of glucose transporters in human ventricular myocardium. Eur J Heart Fail. 2010;12:106-113.
22. von Lewinski D, Rainer PP, Gasser R, Huber MS, Khafaga M, Wilhelm B, Haas T, Machler H, Rossl U, Pieske B. Glucose-transporter-mediated positive inotropic effects in human myocardium of diabetic and nondiabetic patients. Metabolism. 2010;59:1020-1028.
23. Balteau M, Tajeddine N, de Meester C, Ginion A, Des Rosiers C, Brady NR, SommereynsC, HormanS, Vanoverschelde JL, Gailly P, Hue L, BertrandL, Beauloye C.NADPHoxidase activation by hyperglycaemia in cardiomyocytes is independent of glucose metabolism but requires SGLT1. Cardiovasc Res. 2011;92:237-246.