Deletion of thioredoxin-interacting protein improves cardiac inotropic reserve in the streptozotocin-induced diabetic heart

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 310, Issue 11, 2016, Pages H1748-H1759

  Myers, Ronald B ^a   Fomovsky, Gregory M ^a   Lee, Samuel ^a   Tan, Max ^a   Wang, Bing F ^a   Patwari, Parth ^a   Yoshioka, Jun ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

GLUT1; Isoproterenol; arrestins

Indexed keywords

BETA ADRENERGIC RECEPTOR; BETA ARRESTIN; GLUCOSE; GLUCOSE TRANSPORTER 1; INSULIN; REACTIVE OXYGEN METABOLITE; THIOREDOXIN; THIOREDOXIN INTERACTING PROTEIN; CARRIER PROTEIN; TXNIP PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BETA ADRENERGIC STIMULATION; CARDIAC INOTROPIC RESERVE; CARDIAC MUSCLE; CARDIAC MUSCLE CELL; CONTROLLED STUDY; DIABETIC CARDIOMYOPATHY; ECHOCARDIOGRAPHY; EMBRYO; FEMALE; GENE EXPRESSION; GLUCOSE TRANSPORT; HEART FUNCTION; HEART HEMODYNAMICS; HEART MUSCLE FIBROSIS; HEART VENTRICLE HYPERTROPHY; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HYPERGLYCEMIA; IN VITRO STUDY; IN VIVO STUDY; INOTROPISM; KNOCKOUT MOUSE; MALE; MOUSE; MOUSE MODEL; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEOMICS; RAT; RECEPTOR DOWN REGULATION; SIGNAL TRANSDUCTION; STREPTOZOTOCIN-INDUCED DIABETES MELLITUS; WILD TYPE MOUSE; ANIMAL; CELL LINE; DRUG EFFECTS; EXPERIMENTAL DIABETES MELLITUS; GENETICS; HEART CONTRACTION; METABOLISM;

ANIMALS; CARRIER PROTEINS; CELL LINE; DIABETES MELLITUS, EXPERIMENTAL; FEMALE; GLUCOSE; GLUCOSE TRANSPORTER TYPE 1; HUMANS; MALE; MICE; MICE, KNOCKOUT; MYOCARDIAL CONTRACTION; MYOCARDIUM; MYOCYTES, CARDIAC; RATS; RECEPTORS, ADRENERGIC, BETA; THIOREDOXINS;

EID: 84974638232     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00051.2016     Document Type: Article

References (69)

1. Abel ED. Glucose transport in the heart. Front Biosci 9: 201–215, 2004.
2. Alvarez CE. On the origins of arrestin and rhodopsin. BMC Evol Biol 8: 222, 2008.
3. An D, Rodrigues B. Role of changes in cardiac metabolism in development of diabetic cardiomyopathy. Am J Physiol Heart Circ Physiol 291: H1489–H1506, 2006.
4. Andres AM, Ratliff EP, Sachithanantham S, Hui ST. Diminished AMPK signaling response to fasting in thioredoxin-interacting protein knockout mice. FEBS Lett 585: 1223–1230, 2011.
5. Berlin I, Grimaldi A, Bosquet F, Puech AJ. Decreased beta-adrenergic sensitivity in insulin-dependent diabetic subjects. J Clin Endocrinol Metab 63: 262–265, 1986.
6. Boudina S, Abel ED. Diabetic cardiomyopathy revisited. Circulation 115: 3213–3223, 2007.
7. Boudina S, Abel ED. Diabetic cardiomyopathy, causes and effects. Rev Endocr Metab Disord 11: 31–39, 2010.
8. Boudina S, Bugger H, Sena S, O’Neill BT, Zaha VG, Ilkun O, Wright JJ, Mazumder PK, Palfreyman E, Tidwell TJ, Theobald H, Khali-monchuk O, Wayment B, Sheng X, Rodnick KJ, Centini R, Chen D, Litwin SE, Weimer BE, Abel ED. Contribution of impaired myocardial insulin signaling to mitochondrial dysfunction and oxidative stress in the heart. Circulation 119: 1272–1283, 2009.
9. Bugger H, Abel ED. Molecular mechanisms of diabetic cardiomyopathy. Diabetologia 57: 660–671, 2014.
10. Cai L, Wang J, Li Y, Sun X, Wang L, Zhou Z, Kang YJ. Inhibition of superoxide generation and associated nitrosative damage is involved in metallothionein prevention of diabetic cardiomyopathy. Diabetes 54: 1829–1837, 2005.
11. Chatham JC, Forder JR. A 13 C-NMR study of glucose oxidation in the intact functioning rat heart following diabetes-induced cardiomyopathy. J Mol Cell Cardiol 25: 1203–1213, 1993.
12. Chen J, Saxena G, Mungrue IN, Lusis AJ, Shalev A. Thioredoxin-interacting protein: a critical link between glucose toxicity and beta-cell apoptosis. Diabetes 57: 938–944, 2008.
13. Christoffersen C, Bollano E, Lindegaard ML, Bartels ED, Goetze JP, Andersen CB, Nielsen LB. Cardiac lipid accumulation associated with diastolic dysfunction in obese mice. Endocrinology 144: 3483–3490, 2003.
14. Chutkow WA, Birkenfeld AL, Brown JD, Lee HY, Frederick DW, Yoshioka J, Patwari P, Kursawe R, Cushman SW, Plutzky J, Shul-man GI, Samuel VT, Lee RT. Deletion of the alpha-arrestin protein Txnip in mice promotes adiposity and adipogenesis while preserving insulin sensitivity. Diabetes 59: 1424–1434, 2010.
15. Cura AJ, Carruthers A. Acute modulation of sugar transport in brain capillary endothelial cell cultures during activation of the metabolic stress pathway. J Biol Chem 285: 15430–15439, 2010.
16. Dubois-Rande JL, Merlet P, Roudot F, Benvenuti C, Adnot S, Hit-tinger L, Duval AM, Syrota A, Castaigne A, Loisance D. Beta-adrenergic contractile reserve as a predictor of clinical outcome in patients with idiopathic dilated cardiomyopathy. Am Heart J 124: 679–685, 1992.
17. Dunn LL, Simpson PJ, Prosser HC, Lecce L, Yuen GS, Buckle A, Sieveking DP, Vanags LZ, Lim PR, Chow RW, Lam YT, Clayton Z, Bao S, Davies MJ, Stadler N, Celermajer DS, Stocker R, Bursill CA, Cooke JP, Ng MK. A critical role for thioredoxin-interacting protein in diabetes-related impairment of angiogenesis. Diabetes 63: 675–687, 2014.
18. Gloeckner CJ, Boldt K, Schumacher A, Roepman R, Ueffing M. A novel tandem affinity purification strategy for the efficient isolation and characterisation of native protein complexes. Proteomics 7: 4228–4234, 2007.
19. Green K, Brand MD, Murphy MP. Prevention of mitochondrial oxida-tive damage as a therapeutic strategy in diabetes. Diabetes 53, Suppl 1: S110–S118, 2004.
20. Gunnink SM, Kerk SA, Kuiper BD, Alabi OD, Kuipers DP, Praam-sma RC, Wrobel KE, Louters LL. Alkaline pH activates the transport activity of GLUT1 in L929 fibroblast cells. Biochimie 99: 189–194, 2014.
21. Han SO, Kommaddi RP, Shenoy SK. Distinct roles for beta-arrestin2 and arrestin-domain-containing proteins in beta2 adrenergic receptor traf-ficking. EMBO Rep 14: 164–171, 2013.
22. He X, Ma Q. Redox regulation by nuclear factor erythroid 2-related factor 2: gatekeeping for the basal and diabetes-induced expression of thiore-doxin-interacting protein. Mol Pharmacol 82: 887–897, 2012.
23. Joffe II, Travers KE, Perreault-Micale CL, Hampton T, Katz SE, Morgan JP, Douglas PS. Abnormal cardiac function in the streptozoto-cin-induced non-insulin-dependent diabetic rat: noninvasive assessment with Doppler echocardiography and contribution of the nitric oxide path-way. J Am Coll Cardiol 34: 2111–2119, 1999.
24. Joshi D, Gupta R, Dubey A, Shiwalkar A, Pathak P, Gupta RC, Chauthaiwale V, Dutt C. TRC4186, a novel AGE-breaker, improves diabetic cardiomyopathy and nephropathy in Ob-ZSF1 model of type 2 diabetes. J Cardiovasc Pharmacol 54: 72–81, 2009.
25. Lamounier-Zepter V, Look C, Alvarez J, Christ T, Ravens U, Sc-hunck WH, Ehrhart-Bornstein M, Bornstein SR, Morano I. Adipocyte fatty acid-binding protein suppresses cardiomyocyte contraction: a new link between obesity and heart disease. Circ Res 105: 326–334, 2009.
26. Lee S, Min Kim S, Dotimas J, Li L, Feener EP, Baldus S, Myers RB, Chutkow WA, Patwari P, Yoshioka J, Lee RT. Thioredoxin-interacting protein regulates protein disulfide isomerases and endoplasmic reticulum stress. EMBO Mol Med 6: 732–743, 2014.
27. Liao R, Jain M, Cui L, D’Agostino J, Aiello F, Luptak I, Ngoy S, Mortensen RM, Tian R. Cardiac-specific overexpression of GLUT1 prevents the development of heart failure attributable to pressure overload in mice. Circulation 106: 2125–2131, 2002.
28. Lin CH, MacGurn JA, Chu T, Stefan CJ, Emr SD. Arrestin-related ubiquitin-ligase adaptors regulate endocytosis and protein turnover at the cell surface. Cell 135: 714–725, 2008.
29. Lindsey ML, Escobar GP, Dobrucki LW, Goshorn DK, Bouges S, Mingoia JT, McClister DM Jr, Su H, Gannon J, MacGillivray C, Lee RT, Sinusas AJ, Spinale FG. Matrix metalloproteinase-9 gene deletion facilitates angiogenesis after myocardial infarction. Am J Physiol Heart Circ Physiol 290: H232–H239, 2006.
30. Lindsey ML, Yoshioka J, MacGillivray C, Muangman S, Gannon J, Verghese A, Aikawa M, Libby P, Krane SM, Lee RT. Effect of a cleavage-resistant collagen mutation on left ventricular remodeling. Circ Res 93: 238–245, 2003.
31. Liong E, Kong SK, Au KK, Li JY, Xu GY, Lee YL, Kwok TT, Choy YM, Lee CY, Fung KP. Inhibition of glucose uptake and suppression of glucose transporter 1 mRNA expression in L929 cells by tumour necrosis factor-alpha. Life Sci 65: PL215–PL220, 1999.
32. Louters LL, Scripture JP, Kuipers DP, Gunnink SM, Kuiper BD, Alabi OD. Hydroxylamine acutely activates glucose uptake in L929 fibroblast cells. Biochimie 95: 787–792, 2013.
33. Luptak I, Yan J, Cui L, Jain M, Liao R, Tian R. Long-term effects of increased glucose entry on mouse hearts during normal aging and ischemic stress. Circulation 116: 901–909, 2007.
34. Mahan LC, Motulsky HJ, Insel PA. Do agonists promote rapid inter-nalization of beta-adrenergic receptors? Proc Natl Acad Sci USA 82: 6566–6570, 1985.
35. Maisel AS, Motulsky HJ, Insel PA. Externalization of beta-adrenergic receptors promoted by myocardial ischemia. Science 230: 183–186, 1985.
36. Masutani H, Yoshihara E, Masaki S, Chen Z, Yodoi J. Thioredoxin binding protein (TBP)-2/Txnip and alpha-arrestin proteins in cancer and diabetes mellitus. J Clin Biochem Nutr 50: 23–34, 2012.
37. Matsuda N, Hattori Y, Gando S, Akaishi Y, Kemmotsu O, Kanno M. Diabetes-induced down-regulation of beta1-adrenoceptor mRNA expres-sion in rat heart. Biochem Pharmacol 58: 881–885, 1999.
38. Minn AH, Hafele C, Shalev A. Thioredoxin-interacting protein is stim-ulated by glucose through a carbohydrate response element and induces beta-cell apoptosis. Endocrinology 146: 2397–2405, 2005.
39. Muoio DM. TXNIP links redox circuitry to glucose control. Cell Metab 5: 412–414, 2007.
40. Nakamura K, Kusuoka H, Ambrosio G, Becker LC. Glycolysis is necessary to preserve myocardial Ca 2 homeostasis during beta-adrener-gic stimulation. Am J Physiol Heart Circ Physiol 264: H670–H678, 1993.
41. Nishio Y, Kashiwagi A, Kida Y, Kodama M, Abe N, Saeki Y, Shigeta Y. Deficiency of cardiac beta-adrenergic receptor in streptozocin-induced diabetic rats. Diabetes 37: 1181–1187, 1988.
42. Nishiyama A, Matsui M, Iwata S, Hirota K, Masutani H, Nakamura H, Takagi Y, Sono H, Gon Y, Yodoi J. Identification of thioredoxin-binding protein-2/vitamin D 3 up-regulated protein 1 as a negative regula-tor of thioredoxin function and expression. J Biol Chem 274: 21645–21650, 1999.
43. Pacher P, Liaudet L, Soriano FG, Mabley JG, Szabo E, Szabo C. The role of poly(ADP-ribose) polymerase activation in the development of myocardial and endothelial dysfunction in diabetes. Diabetes 51: 514–521, 2002.
44. Parikh H, Carlsson E, Chutkow WA, Johansson LE, Storgaard H, Poulsen P, Saxena R, Ladd C, Schulze PC, Mazzini MJ, Jensen CB, Krook A, Bjornholm M, Tornqvist H, Zierath JR, Ridderstrale M, Altshuler D, Lee RT, Vaag A, Groop LC, Mootha VK. TXNIP regulates peripheral glucose metabolism in humans. PLoS Med 4: e158, 2007.
45. Parruti G, Peracchia F, Sallese M, Ambrosini G, Masini M, Rotilio D, De Blasi A. Molecular analysis of human beta-arrestin-1: cloning, tissue distribution, and regulation of expression. Identification of two isoforms generated by alternative splicing. J Biol Chem 268: 9753–9761, 1993.
46. Patwari P, Emilsson V, Schadt EE, Chutkow WA, Lee S, Marsili A, Zhang Y, Dobrin R, Cohen DE, Larsen PR, Zavacki AM, Fong LG, Young SG, Lee RT. The arrestin domain-containing 3 protein regulates body mass and energy expenditure. Cell Metab 14: 671–683, 2011.
47. Patwari P, Higgins LJ, Chutkow WA, Yoshioka J, Lee RT. The interaction of thioredoxin with Txnip. Evidence for formation of a mixed disulfide by disulfide exchange. J Biol Chem 281: 21884–21891, 2006.
48. Patwari P, Lee RT. An expanded family of arrestins regulate metabolism. Trends Endocrinol Metab 23: 216–222, 2012.
49. Perrone L, Devi TS, Hosoya K, Terasaki T, Singh LP. Thioredoxin interacting protein (TXNIP) induces inflammation through chromatin modification in retinal capillary endothelial cells under diabetic condi-tions. J Cell Physiol 221: 262–272, 2009.
50. Perrone L, Devi TS, Hosoya KI, Terasaki T, Singh LP. Inhibition of TXNIP expression in vivo blocks early pathologies of diabetic retinopa-thy. Cell Death Dis 1: e65, 2010.
51. Poornima IG, Parikh P, Shannon RP. Diabetic cardiomyopathy: the search for a unifying hypothesis. Circ Res 98: 596–605, 2006.
52. Price SA, Gardiner NJ, Duran-Jimenez B, Zeef LA, Obrosova IG, Tomlinson DR. Thioredoxin interacting protein is increased in sensory neurons in experimental diabetes. Brain Res 1116: 206–214, 2006.
53. Salie MJ, Oram DS, Kuipers DP, Scripture JP, Chenge J, MacDonald GJ, Louters LL. Nitroxyl (HNO) acutely activates the glucose uptake activity of GLUT1. Biochimie 94: 864–869, 2012.
54. Savarese JJ, Berkowitz BA. Beta-adrenergic receptor decrease in dia-betic rat hearts. Life Sci 25: 2075–2078, 1979.
55. Schulze PC, Yoshioka J, Takahashi T, He Z, King GL, Lee RT. Hyperglycemia promotes oxidative stress through inhibition of thiore-doxin function by thioredoxin-interacting protein. J Biol Chem 279: 30369–30374, 2004.
56. Shah A, Xia L, Masson EA, Gui C, Momen A, Shikatani EA, Husain M, Quaggin S, John R, Fantus IG. Thioredoxin-interacting protein deficiency protects against diabetic nephropathy. J Am Soc Nephrol 26: 2963–2977, 2015.
57. Shalev A, Pise-Masison CA, Radonovich M, Hoffmann SC, Hirshberg B, Brady JN, Harlan DM. Oligonucleotide microarray analysis of intact human pancreatic islets: identification of glucose-responsive genes and a highly regulated TGFbeta signaling pathway. Endocrinology 143: 3695–3698, 2002.
58. Sheth SS, Castellani LW, Chari S, Wagg C, Thipphavong CK, Bodnar JS, Tontonoz P, Attie AD, Lopaschuk GD, Lusis AJ. Thioredoxin-interacting protein deficiency disrupts the fasting-feeding metabolic tran-sition. J Lipid Res 46: 123–134, 2005.
59. Singh LP. Thioredoxin interacting protein (TXNIP) and pathogenesis of diabetic retinopathy. J Clin Exp Ophthalmol 2013: 4, 2013.
60. Soriano-Tarraga C, Jimenez-Conde J, Giralt-Steinhauer E, Mola-Caminal M, Vivanco-Hidalgo RM, Ois A, Rodriguez-Campello A, Cuadrado-Godia E, Sayols-Baixeras S, Elosua R, Roquer J. Epig-enome-wide association study identifies TXNIP gene associated with type 2 diabetes mellitus and sustained hyperglycemia. Hum Mol Genet 25: 609–619, 2016.
61. Su H, Ji L, Xing W, Zhang W, Zhou H, Qian X, Wang X, Gao F, Sun X, Zhang H. Acute hyperglycaemia enhances oxidative stress and aggra-vates myocardial ischaemia/reperfusion injury: role of thioredoxin-inter-acting protein. J Cell Mol Med 17: 181–191, 2013.
62. Suarez J, Belke DD, Gloss B, Dieterle T, McDonough PM, Kim YK, Brunton LL, Dillmann WH. In vivo adenoviral transfer of sorcin reverses cardiac contractile abnormalities of diabetic cardiomyopathy. Am J Physiol Heart Circ Physiol 286: H68–H75, 2004.
63. Suzuki H, Kayama Y, Sakamoto M, Iuchi H, Shimizu I, Yoshino T, Katoh D, Nagoshi T, Tojo K, Minamino T, Yoshimura M, Utsunomiya K. Arachidonate 12/15-lipoxygenase-induced inflammation and oxidative stress are involved in the development of diabetic cardiomyopathy. Dia-betes 64: 618–630, 2015.
64. Vasanji Z, Dhalla NS, Netticadan T. Increased inhibition of SERCA2 by phospholamban in the type I diabetic heart. Mol Cell Biochem 261: 245–249, 2004.
65. Wall SR, Lopaschuk GD. Glucose oxidation rates in fatty acid-perfused isolated working hearts from diabetic rats. Biochim Biophys Acta 1006: 97–103, 1989.
66. Wu N, Zheng B, Shaywitz A, Dagon Y, Tower C, Bellinger G, Shen CH, Wen J, Asara J, McGraw TE, Kahn BB, Cantley LC. AMPK-dependent degradation of TXNIP upon energy stress leads to enhanced glucose uptake via GLUT1. Mol Cell 49: 1167–1175, 2013.
67. Yamamoto M, Yang G, Hong C, Liu J, Holle E, Yu X, Wagner T, Vatner SF, Sadoshima J. Inhibition of endogenous thioredoxin in the heart increases oxidative stress and cardiac hypertrophy. J Clin Invest 112: 1395–1406, 2003.
68. Yoshioka J, Imahashi K, Gabel SA, Chutkow WA, Burds AA, Gannon J, Schulze PC, MacGillivray C, London RE, Murphy E, Lee RT. Targeted deletion of thioredoxin-interacting protein regulates cardiac dys-function in response to pressure overload. Circ Res 101: 1328–1338, 2007.
69. Yoshioka J, Schulze PC, Cupesi M, Sylvan JD, MacGillivray C, Gannon J, Huang H, Lee RT. Thioredoxin-interacting protein controls cardiac hypertrophy through regulation of thioredoxin activity. Circula-tion 109: 2581–2586, 2004.