Cited by 312Mitochondrial Function and PathologyAutophagy in Disease and TherapyCardiovascular Function and Risk Factors

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Hyperglycemia-Driven Inhibition of AMP-Activated Protein Kinase α2 Induces Diabetic Cardiomyopathy by Promoting Mitochondria-Associated Endoplasmic Reticulum Membranes In Vivo

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Wu, Shengnan, Lu, Qiulun, Ding, Ye, Wu, Yin, Qiu, Yu, Wang, Pei, Mao, Xiaoxiang, Huang, Kai, Xie, Zhonglin, Zou, Ming-Hui·2019·Circulation

DOI 10.1161/circulationaha.118.033552PMC PMC6465113

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Abstract

Background: Fundc1 (FUN14 domain containing 1), an outer mitochondrial membrane protein, is important for mitophagy and mitochondria-associated endoplasmic reticulum membranes (MAMs). The roles of Fundc1 and MAMs in diabetic hearts remain unknown. The aims of this study, therefore, were to determine whether the diabetes mellitus–induced Fundc1 expression could increase MAM formation, and whether disruption of MAM formation improves diabetic cardiac function. Methods: Levels of FUNDC1 were examined in the hearts from diabetic patients and nondiabetic donors. Levels of Fundc1-induced MAMs and mitochondrial and heart function were examined in mouse neonatal cardiomyocytes exposed to high glucose (HG, 30 mmol/L d -glucose for 48 hours), and in streptozotocin-treated cardiac-specific Fundc1 knockout mice and cardiac-specific Fundc1 knockout diabetic Akita mice, as well. Results: FUNDC1 levels were significantly elevated in cardiac tissues from diabetic patients in comparison with those from nondiabetic donors. In cultured mouse neonatal cardiomyocytes, HG conditions increased levels of Fundc1, the inositol 1,4,5-trisphosphate type 2 receptor (Ip 3 r2), and MAMs. Genetic downregulation of either Fundc1 or Ip 3 r2 inhibited MAM formation, reduced endoplasmic reticulum-mitochondrial Ca 2+ flux, and improved mitochondrial function in HG-treated cardiomyocytes. Consistently, adenoviral overexpression of Fundc1 promoted MAM formation, mitochondrial Ca 2+ increase, and mitochondrial dysfunction in cardiomyocytes exposed to normal glucose (5.5 mmol/L d -glucose). In comparison with nondiabetic controls, levels of Fundc1, Ip 3 r2, and MAMs were significantly increased in hearts from streptozotocin-treated mice and Akita mice. Furthermore, in comparison with control hearts, diabetes mellitus markedly increased coimmunoprecipitation of Fundc1 and Ip 3 r2. The binding of Fundc1 to Ip 3 r2 inhibits Ip 3 r2 ubiquitination and proteasome-mediated degradation. Cardiomyocyte-specific Fundc1 deletion ablated diabetes mellitus–induced MAM formation, prevented mitochondrial Ca 2+ increase, mitochondrial fragmentation, and apoptosis with improved mitochondrial functional capacity and cardiac function. In mouse neonatal cardiomyocytes, HG suppressed AMP-activated protein kinase activity. Furthermore, in cardiomyocytes of Prkaa2 knockout mice, expression of Fundc1, MAM formation, and mitochondrial Ca 2+ levels were significantly increased. Finally, adenoviral overexpression of a constitutively active mutant AMP-activated protein kinase ablated HG-induced MAM formation and mitochondrial dysfunction. Conclusions: We conclude that diabetes mellitus suppresses AMP-activated protein kinase, initiating Fundc1-mediated MAM formation, mitochondrial dysfunction, and cardiomyopathy, suggesting that AMP-activated protein kinase–induced Fundc1 suppression is a valid target to treat diabetic cardiomyopathy.

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Biochemistry and molecular cell biology of diabetic complications
Brownlee, M. (2001) · Nature · doi:10.1038/414813a · Cited by 9,107
Down-Regulation of Na+/K+ATPase Activity by Human Parvovirus B19 Capsid Protein VP1
Almilaji, A., Szteyn, K., Fein, E., Pakladok, T., Muñoz, C., Elvira, B., Towhid, S. T., Alesutan, I., Shumilina, E. V., Bock, C. –., et al. (2013) · Cellular Physiology and Biochemistry · doi:10.1159/000350083 · Cited by 8,700
Effect of intensive blood-glucose control with metformin on complications in overweight patients with type 2 diabetes (UKPDS 34)
(1998) · The Lancet · doi:10.1016/s0140-6736(98)07037-8 · Cited by 8,247
Role of AMP-Activated Protein Kinase in Mechanism of Metformin Action
Zhou, G., Myers, R., Li, Y., Chen, Y., Shen, X., Fenyk-Melody, J., Wu, M., Ventre, J., Doebber, T., Fujii, N., et al. (2001) · Journal of Clinical Investigation · doi:10.1172/jci13505 · Cited by 5,652
Anti-Vascular Endothelial Growth Factors Protect Retinal Pigment Epithelium Cells Against Oxidation by Modulating Nitric Oxide Release and Autophagy
Cillà, S. D., Farruggio, S., Vujosevic, S., Raina, G., Filippini, D. A., Gatti, V., Clemente, N., Mary, D., Vezzola, D., Casini, G., et al. (2017) · Cellular Physiology and Biochemistry · doi:10.1159/000479441 · Cited by 5,154
Effect of intensive blood-glucose control with metformin on complications in overweight patients with type 2 diabetes (UKPDS 34). UK Prospective Diabetes Study (UKPDS) Group.
(1998) · PubMed · Cited by 4,290
The Pathophysiology of Mitochondrial Cell Death
Green, D. R., & Kroemer, G. (2004) · Science · doi:10.1126/science.1099320 · Cited by 3,487
Regulation of cell death: the calcium–apoptosis link
Orrenius, S., Zhivotovsky, B., & Nicotera, P. (2003) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1150 · Cited by 3,060
Mitofusin 2 tethers endoplasmic reticulum to mitochondria
de Brito, O. M., & Scorrano, L. (2008) · Nature · doi:10.1038/nature07534 · Cited by 2,442
Dysfunction of Mitochondria in Human Skeletal Muscle in Type 2 Diabetes
Kelley, D. E., He, J., Menshikova, E. V., & Ritov, V. B. (2002) · Diabetes · doi:10.2337/diabetes.51.10.2944 · Cited by 2,321
Mitochondrial dysfunction and type 2 diabetes
Lowell, B. B., & Shulman, G. I. (2005) · Science · doi:10.1126/science.1104343 · Cited by 2,070
Mitochondria as sensors and regulators of calcium signalling
Rizzuto, R., De Stefani, D., Raffaello, A., & Mammucari, C. (2012) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3412 · Cited by 1,781
Mitochondrial outer-membrane protein FUNDC1 mediates hypoxia-induced mitophagy in mammalian cells
Liu, L., Feng, D., Chen, G., Chen, M., Zheng, Q., Song, P., Ma, Q., Zhu, C., Wang, R., Qi, W., et al. (2012) · Nature Cell Biology · doi:10.1038/ncb2422 · Cited by 1,738
Fluorescent indicators for cytosolic calcium based on rhodamine and fluorescein chromophores
Minta, A., Kao, J. P. Y., & Tsien, R. Y. (1989) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)83165-9 · Cited by 1,621
Chaperone-mediated coupling of endoplasmic reticulum and mitochondrial Ca2+ channels
Szabadkai, G., Bianchi, K., Várnai, P., De Stefani, D., Wieckowski, M. R., Cavagna, D., Nagy, A. I., Balla, T., & Rizzuto, R. (2006) · The Journal of Cell Biology · doi:10.1083/jcb.200608073 · Cited by 1,413
Mitophagy: mechanisms, pathophysiological roles, and analysis
Ding, W.-X., & Yin, X.-M. (2012) · bchm · doi:10.1515/hsz-2012-0119 · Cited by 1,032
Essential Regulation of Cell Bioenergetics by Constitutive InsP3 Receptor Ca2+ Transfer to Mitochondria
Cárdenas, C., Miller, R. A., Smith, I., Bui, T., Molgó, J., Müller, M., Vais, H., Cheung, K.-H., Yang, J., Parker, I., et al. (2010) · Cell · doi:10.1016/j.cell.2010.06.007 · Cited by 1,026
Endoplasmic reticulum-mitochondria contacts: Function of the junction
Rowland, A. A., & Voeltz, G. K. (2012) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3440 · Cited by 1,018
Isolation of mitochondria-associated membranes and mitochondria from animal tissues and cells
Wieckowski, M. R., Giorgi, C., Lebiedzinska, M., Duszynski, J., & Pinton, P. (2009) · Nature Protocols · doi:10.1038/nprot.2009.151 · Cited by 979
Circularly permuted green fluorescent proteins engineered to sense Ca 2+
Nagai, T., Sakaue-Sawano, A., Park, E. S., & Miyawaki, A. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.051636098 · Cited by 969
Regulation of mitochondrial dehydrogenases by calcium ions
Denton, R. M. (2009) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2009.01.005 · Cited by 885
NCLX is an essential component of mitochondrial Na + /Ca 2+ exchange
Palty, R., Silverman, W. F., Hershfinkel, M., Caporale, T., Sensi, S. L., Parnis, J., Nolte, C., Fishman, D., Shoshan‐Barmatz, V., Herrmann, S., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0908099107 · Cited by 789
Chronic enrichment of hepatic endoplasmic reticulum–mitochondria contact leads to mitochondrial dysfunction in obesity
Arruda, A. P., Pers, B. M., Parlakgül, G., Güney, E., Inouye, K., & Hotamışlıgil, G. S. (2014) · Nature Medicine · doi:10.1038/nm.3735 · Cited by 741
A Regulatory Signaling Loop Comprising the PGAM5 Phosphatase and CK2 Controls Receptor-Mediated Mitophagy
Chen, G., Han, Z., Feng, D., Chen, Y., Chen, L., Wu, H., Huang, L., Zhou, C., Cai, X., Fu, C., et al. (2014) · Molecular Cell · doi:10.1016/j.molcel.2014.02.034 · Cited by 615
A mutation in the insulin 2 gene induces diabetes with severe pancreatic β-cell dysfunction in the Mody mouse
Wang, J., Takeuchi, T., Tanaka, S., Kubo, S.-K., Kayo, T., Lu, D., Takata, K., Koizumi, A., & Izumi, T. (1999) · Journal of Clinical Investigation · doi:10.1172/jci4431 · Cited by 572
Endogenous Drp1 Mediates Mitochondrial Autophagy and Protects the Heart Against Energy Stress
Ikeda, Y., Shirakabe, A., Maejima, Y., Zhai, P., Sciarretta, S., Toli, J., Nomura, M., Mihara, K., Egashira, K., Ohishi, M., et al. (2015) · Circulation Research · doi:10.1161/circresaha.116.303356 · Cited by 571
Mitochondrial calcium overload is a key determinant in heart failure
Santulli, G., Xie, W., Reiken, S. R., & Marks, A. R. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1513047112 · Cited by 561
The role of mitochondria in the pathogenesis of type 2 diabetes
Patti, M.-E., & Corvera, S. (2010) · Endocrine Reviews · doi:10.1210/er.2009-0027 · Cited by 551
mTOR complex 2-Akt signaling at mitochondria-associated endoplasmic reticulum membranes (MAM) regulates mitochondrial physiology
Betz, C., Stracka, D., Prescianotto-Baschong, C., Frieden, M., Demaurex, N., & Hall, M. N. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1302455110 · Cited by 538
Improvement of Cardiac Functions by Chronic Metformin Treatment Is Associated With Enhanced Cardiac Autophagy in Diabetic OVE26 Mice
Xie, Z., Lau, K., Eby, B., Lozano, P., He, C., Pennington, B., Li, H., Rathi, S., Dong, Y., Tian, R., et al. (2011) · Diabetes · doi:10.2337/db10-0351 · Cited by 490
Self-citation
Mitochondrial Fission and Fusion Factors Reciprocally Orchestrate Mitophagic Culling in Mouse Hearts and Cultured Fibroblasts
Song, M., Mihara, K., Chen, Y., Scorrano, L., & Dorn, G. W. (2015) · Cell Metabolism · doi:10.1016/j.cmet.2014.12.011 · Cited by 482
The endoplasmic reticulum–mitochondria connection: One touch, multiple functions
Marchi, S., Patergnani, S., & Pinton, P. (2014) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2013.10.015 · Cited by 475
Drp-1-Dependent Division of the Mitochondrial Network Blocks Intraorganellar Ca2+ Waves and Protects against Ca2+-Mediated Apoptosis
Szabadkai, G., Simoni, A. M., Chami, M., Wieckowski, M. R., Youle, R. J., & Rizzuto, R. (2004) · Molecular Cell · doi:10.1016/j.molcel.2004.09.026 · Cited by 468
CaMKII determines mitochondrial stress responses in heart
Joiner, M.-L. A., Koval, O. M., Li, J., He, B. J., Allamargot, C., Gao, Z., Luczak, E. D., Hall, D. D., Fink, B. D., Chen, B., et al. (2012) · Nature · doi:10.1038/nature11444 · Cited by 411
Mitochondria-associated endoplasmic reticulum membrane (MAM) integrity is required for insulin signaling and is implicated in hepatic insulin resistance
Tubbs, E., Theurey, P., Vial, G., Bendridi, N., Bravard, A., Chauvin, M.-A., Ji-Cao, J., Zoulim, F., Bartosch, B., Ovize, M., et al. (2014) · Diabetes · doi:10.2337/db13-1751 · Cited by 411
Structural and functional link between the mitochondrial network and the endoplasmic reticulum
Giorgi, C., Stefani, D. D., Bononi, A., Rizzuto, R., & Pinton, P. (2009) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2009.04.010 · Cited by 388
FUNDC1 regulates mitochondrial dynamics at the ER–mitochondrial contact site under hypoxic conditions
Wu, W., Lin, C., Wu, K., Jiang, L., Wang, X., Li, W., Zhuang, H., Zhang, X., Chen, H. H., Li, S., et al. (2016) · The EMBO Journal · doi:10.15252/embj.201593102 · Cited by 370
Metabolic stress–induced activation of FoxO1 triggers diabetic cardiomyopathy in mice
Battiprolu, P. K., Hojayev, B., Jiang, N., Wang, Z. V., Luo, X., Iglewski, M., Shelton, J. M., Gerard, R. D., Rothermel, B. A., Gillette, T. G., et al. (2012) · Journal of Clinical Investigation · doi:10.1172/jci60329 · Cited by 352
Mitochondria-Associated Membranes: Composition, Molecular Mechanisms, and Physiopathological Implications
Giorgi, C., Missiroli, S., Patergnani, S., Duszyński, J., Wieckowski, M. R., & Pinton, P. (2015) · Antioxidants and Redox Signaling · doi:10.1089/ars.2014.6223 · Cited by 343
Binding of FUN14 domain containing 1 with inositol 1,4,5-trisphosphate receptor in mitochondria-associated endoplasmic reticulum membranes maintains mitochondrial dynamics and function in hearts in vivo
Wu, S., Lu, Q., Wang, Q., Ding, Y., Ma, Z., Mao, X., Huang, K., Xie, Z., & Zou, M.-H. (2017) · Circulation · doi:10.1161/circulationaha.117.030235 · Cited by 320
Depressing Mitochondria-Reticulum Interactions Protects Cardiomyocytes From Lethal Hypoxia-Reoxygenation Injury
Paillard, M., Tubbs, E., Thiébaut, P., Gomez, L., Fauconnier, J., Silva, C. C. D., Teixeira, G., Mewton, N., Belaïdi, E., Durand, A., et al. (2013) · Circulation · doi:10.1161/circulationaha.113.001225 · Cited by 301
The mitochondrial calcium uniporter complex: molecular components, structure and physiopathological implications
Marchi, S., & Pinton, P. (2013) · The Journal of Physiology · doi:10.1113/jphysiol.2013.268235 · Cited by 295
Mitochondrial dysfunction due to long-chain Acyl-CoA dehydrogenase deficiency causes hepatic steatosis and hepatic insulin resistance
Zhang, D., Liu, Z.-X., Choi, C. S., Tian, L., Kibbey, R., Dong, J., Cline, G. W., Wood, P. A., & Shulman, G. I. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0707060104 · Cited by 291
A spontaneous mutation in the nicotinamide nucleotide transhydrogenase gene of C57BL/6J mice results in mitochondrial redox abnormalities
Ronchi, J. A., Figueira, T. R., Ravagnani, F. G., Oliveira, H. C. F., Vercesi, A. E., & Castilho, R. F. (2013) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2013.05.049 · Cited by 283
Phosphorylation of LKB1 at Serine 428 by Protein Kinase C-ζ Is Required for Metformin-Enhanced Activation of the AMP-Activated Protein Kinase in Endothelial Cells
Xie, Z., Dong, Y., Scholz, R., Neumann, D., & Zou, M.-H. (2008) · Circulation · doi:10.1161/circulationaha.107.744490 · Cited by 273
Self-citation
Reduction of AMP-Activated Protein Kinase α2 Increases Endoplasmic Reticulum Stress and Atherosclerosis In Vivo
Dong, Y., Zhang, M., Liang, B., Xie, Z., Zhao, Z., Asfa, S., Choi, H. C., & Zou, M. (2010) · Circulation · doi:10.1161/circulationaha.109.900928 · Cited by 262
Diminished Autophagy Limits Cardiac Injury in Mouse Models of Type 1 Diabetes
Xu, X., Kobayashi, S., Chen, K., Timm, D. J., Volden, P. A., Huang, Y., Gulick, J. M., Yue, Z., Robbins, J. M., Epstein, P. N., et al. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.474650 · Cited by 254
Defective intracellular Ca2+ signaling contributes to cardiomyopathy in Type 1 diabetic rats
Choi, K. M., Zhong, Y., Hoit, B. D., Grupp, I. L., Hahn, H. S., Dilly, K. W., Guatimosim, S., Lederer, W. J., & Matlib, M. A. (2002) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00313.2002 · Cited by 251
Subcellular imaging of intramitochondrial Ca2+ with recombinant targeted aequorin: significance for the regulation of pyruvate dehydrogenase activity.
Rutter, G. A., Burnett, P., Rizzuto, R., Brini, M., Murgia, M., Pozzan, T., Tavaré, J. M., & Denton, R. M. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.11.5489 · Cited by 243
Recipes for Creating Animal Models of Diabetic Cardiovascular Disease
Hsueh, W. A., Abel, E. D., Breslow, J. L., Maeda, N., Davis, R. C., Fisher, E. A. A., Dansky, H. M., McClain, D. A., McIndoe, R., Wassef, M. K., et al. (2007) · Circulation Research · doi:10.1161/01.res.0000266449.37396.1f · Cited by 221
Regulation of Cardiomyocyte Proliferation and Myocardial Growth During Development by FOXO Transcription Factors
Evans‐Anderson, H. J., Alfieri, C. M., & Yutzey, K. E. (2008) · Circulation Research · doi:10.1161/circresaha.107.163428 · Cited by 215
Calcium regulates cell death in cancer: Roles of the mitochondria and mitochondria-associated membranes (MAMs)
Danese, A., Patergnani, S., Bonora, M., Wieckowski, M. R., Previati, M., Giorgi, C., & Pinton, P. (2017) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2017.01.003 · Cited by 192
Mitochondria and cardioprotection
Lisa, F. D., Canton, M., Menabò, R., Kaludercic, N., & Bernardi, P. (2007) · Heart Failure Reviews · doi:10.1007/s10741-007-9028-z · Cited by 177
NCLX: The mitochondrial sodium calcium exchanger
Boyman, L., Williams, G. S. B., Khananshvili, D., Sekler, I., & Lederer, W. J. (2013) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2013.03.012 · Cited by 172
Localization and Processing of the Amyloid-β Protein Precursor in Mitochondria-Associated Membranes
Prete, D. D., Suski, J. M., Oulès, B., Debayle, D., Gay, A.-S., Lacas‐Gervais, S., Bussiere, R., Bauer, C., Pinton, P., Paterlini-Bréchot, P., et al. (2016) · Journal of Alzheimer s Disease · doi:10.3233/jad-160953 · Cited by 167
Colocalization Analysis in Fluorescence Micrographs: Verification of a More Accurate Calculation of Pearson's Correlation Coefficient
Barlow, A. L., MacLeod, A., Noppen, S., Sanderson, J., & Guérin, C. J. (2010) · Microscopy and Microanalysis · doi:10.1017/s143192761009389x · Cited by 166
Type 1 diabetic cardiomyopathy in the Akita (Ins2WT/C96Y) mouse model is characterized by lipotoxicity and diastolic dysfunction with preserved systolic function
Basu, R., Oudit, G. Y., Wang, X., Zhang, L., Ussher, J. R., Lopaschuk, G. D., & Kassiri, Z. (2009) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00452.2009 · Cited by 161
Metformin Activates AMP-Activated Protein Kinase by Promoting Formation of the αβγ Heterotrimeric Complex
Meng, S., Cao, J., He, Q., Xiong, L., Chang, E., Radovick, S., Wondisford, F. E., & He, L. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.604421 · Cited by 146
FoxO1 is crucial for sustaining cardiomyocyte metabolism and cell survival
Puthanveetil, P., Wan, A., & Rodrigues, B. B. (2012) · Cardiovascular Research · doi:10.1093/cvr/cvs426 · Cited by 134
Calcium and mitochondria: mechanisms and functions of a troubled relationship
Bianchi, K., Rimessi, A., Prandini, A., Szabadkai, G., & Rizzuto, R. (2004) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2004.09.015 · Cited by 134
The mitochondrial membrane potential and Ca2+ oscillations in smooth muscle
Chalmers, S., & McCarron, J. G. (2007) · Journal of Cell Science · doi:10.1242/jcs.014522 · Cited by 109
RNF170 Protein, an Endoplasmic Reticulum Membrane Ubiquitin Ligase, Mediates Inositol 1,4,5-Trisphosphate Receptor Ubiquitination and Degradation
Lu, J. P., Wang, Y., Sliter, D. A., Pearce, M. M. P., & Wojcikiewicz, R. J. H. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.251983 · Cited by 102
Inhibition of NAPDH Oxidase 2 (NOX2) Prevents Oxidative Stress and Mitochondrial Abnormalities Caused by Saturated Fat in Cardiomyocytes
Joseph, L. C., Barca, E., Subramanyam, P., Komrowski, M., Pajvani, U., Colecraft, H. M., Hirano, M., & Morrow, J. P. (2016) · PLOS ONE · doi:10.1371/journal.pone.0145750 · Cited by 99
New mouse model to study islet transplantation in insulin-dependent diabetes mellitus
Mathews, C. E., Langley, S. H., & Leiter, E. H. (2002) · Transplantation · doi:10.1097/00007890-200204270-00024 · Cited by 95
Activation of Foxo1 by Insulin Resistance Promotes Cardiac Dysfunction and β–Myosin Heavy Chain Gene Expression
Qi, Y., Zhu, Q., Zhang, K., Thomas, C., Wu, Y., Kumar, R., Baker, K. M., Xu, Z., Chen, S., & Guo, S. (2014) · Circulation Heart Failure · doi:10.1161/circheartfailure.114.001457 · Cited by 92
Regulation of intracellular Ca2+ in the heart during diabetes
Pierce, G. N. (1997) · Cardiovascular Research · doi:10.1016/s0008-6363(97)00010-2 · Cited by 91
Comprehensive analysis of mitochondrial permeability transition pore activity in living cells using fluorescence-imaging-based techniques
Bonora, M., Morganti, C., Morciano, G., Giorgi, C., Wieckowski, M. R., & Pinton, P. (2016) · Nature Protocols · doi:10.1038/nprot.2016.064 · Cited by 79
Measurements of mitochondrial calcium in vivo
Pozzan, T., & Rudolf, R. (2008) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2008.11.012 · Cited by 75
Updating Experimental Models of Diabetic Cardiomyopathy
Fuentes‐Antrás, J., Picatoste, B., Gómez‐Hernández, A., Egido, J., Tuñón, J., & Lorenzo, Ó. (2015) · Journal of Diabetes Research · doi:10.1155/2015/656795 · Cited by 74
The Mitochondrial Na+/Ca2+ Exchanger Upregulates Glucose Dependent Ca2+ Signalling Linked to Insulin Secretion
Nita, I. I., Hershfinkel, M., Fishman, D., Ozeri, E., Rutter, G. A., Sensi, S. L., Khananshvili, D., Lewis, E. C., & Sekler, I. (2012) · PLoS ONE · doi:10.1371/journal.pone.0046649 · Cited by 72
Role of extracellular calcium and mitochondrial oxygen species in psychosine-induced oligodendrocyte cell death
Voccoli, V., Tonazzini, I., Signore, G., Caleo, M., & Cecchini, M. G. (2014) · Cell Death and Disease · doi:10.1038/cddis.2014.483 · Cited by 70
Abnormalities in mitochondria-associated membranes and phospholipid biosynthetic enzymes in the mnd/mnd mouse model of neuronal ceroid lipofuscinosis
Vance, J. E., Stone, S. J., & Faust, J. R. (1997) · Biochimica et Biophysica Acta (BBA) - Lipids and Lipid Metabolism · doi:10.1016/s0005-2760(96)00153-1 · Cited by 69
Using Isolated Mitochondria from Minimal Quantities of Mouse Skeletal Muscle for High throughput Microplate Respiratory Measurements
Boutagy, N. E., Rogers, G. W., Pyne, E. S., Ali, M. M., Hulver, M. W., & Frisard, M. I. (2015) · Journal of Visualized Experiments · doi:10.3791/53216 · Cited by 53
Studying mitochondrial Ca2+ uptake – A revisit
Jean-Quartier, C., Bondarenko, A. I., Alam, M. R., Trenker, M., Waldeck‐Weiermair, M., Malli, R., & Graier, W. F. (2011) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2011.10.033 · Cited by 52
Ratiometric Analysis of Fura Red by Flow Cytometry: A Technique for Monitoring Intracellular Calcium Flux in Primary Cell Subsets
Wendt, E., Ferry, H., Greaves, D. R., & Keshav, S. (2015) · PLoS ONE · doi:10.1371/journal.pone.0119532 · Cited by 39
Stimulation‐induced changes in NADH fluorescence and mitochondrial membrane potential in lizard motor nerve terminals
Talbot, J. D., Barrett, J. N., Barrett, E. F., & David, G. (2007) · The Journal of Physiology · doi:10.1113/jphysiol.2006.126383 · Cited by 38
Regulation of metabolism in individual mitochondria during excitation–contraction coupling
Gong, G., Liu, X., & Wang, W. (2014) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2014.09.012 · Cited by 37
A word of caution concerning the use of Nnt‐mutated C57BL/6 mice substrains as experimental models to study metabolism and mitochondrial pathophysiology
Figueira, T. R. (2013) · Experimental Physiology · doi:10.1113/expphysiol.2013.074682 · Cited by 15

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See all 312

Authors: Wu, S., Lu, Q., Ding, Y., Wu, Y., Qiu, Y., Wang, P., Mao, X., Huang, K., Xie, Z., & Zou, M.-H.
Affiliations: Georgia State University (US)
University of Washington (US)
Wuhan Union Hospital (CN)
Corresponding author: Xie, Zhonglin
Zou, Ming-Hui
ORCID: Wu, Shengnan
Lu, Qiulun
Ding, Ye
Wu, Yin
Wang, Pei
Mao, Xiaoxiang
Huang, Kai
Zou, Ming-Hui
Venue: Circulation
Publisher: Ovid Technologies (Wolters Kluwer Health)
Published: 2019-04-16
Volume: 139
Issue: 16
Pages: 1913-1936
ISSN: 0009-7322 (ISSN-L)
1524-4539
DOI: 10.1161/circulationaha.118.033552
PMC: PMC6465113
OpenAlex: W2911037090
Semantic Scholar: 6ae43efb25ca95c487961d8441dedd8e60e67291
Cited by: 298
References: 78
Citations by year: 2026: 37 · 2025: 48 · 2024: 55 · 2023: 43 · 2022: 47 · 2021: 27 · 2020: 32 · 2019: 8
FWCI: 9.43
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Circulation (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: American Heart Association (16POST31160009, 16GRANT29590003, 16POST29960011)
University of Washington
Georgia Research Alliance
National Institute on Aging (AG047776, R01AG047776)
National Heart, Lung, and Blood Institute (HL128014, HL137371, R01HL105157, HL 079584, R01HL079584, HL110488, HL140954, HL-080499, R01HL142287, R01HL137371, R01HL132500, R01HL074399, R01HL080499, HL132500, HL-089920, R01HL140954, R01HL110488, HL142287, R01HL128014, R01HL089920, CA213022, R01HL096032)
National Cancer Institute (CA-213022, R01CA213022)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Autophagy in Disease and Therapy
Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiovascular Function and Risk Factors
Keywords: diabetic cardiomyopathy, hyperglycemia, FUNDC1, mitochondria-associated endoplasmic reticulum membranes, IP3R2, mitochondrial calcium flux, mitophagy, AMPK, mitochondrial dysfunction, cardiomyocytes, streptozotocin-induced diabetes, Akita mice, cardiomyocyte-specific knockout, apoptosis, mitochondrial fragmentation, ubiquitination
MeSH terms: Adult, Aged, Animals, Cell Line, Endoplasmic Reticulum, Female, Gene Expression Regulation, Humans, Male, Membrane Proteins, Mice, Inbred C57BL, Middle Aged, Mitochondria, Myocardial Contraction, Mice, Knockout, Calcium Signaling, Mitochondrial Proteins, Myocytes, Cardiac, Mitochondrial Membranes, Mice, Rats, AMP-Activated Protein Kinases, Diabetic Cardiomyopathies

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Hyperglycemia-Driven Inhibition of AMP-Activated Protein Kinase α2 Induces Diabetic Cardiomyopathy by Promoting Mitochondria-Associated Endoplasmic Reticulum Membranes In Vivo

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