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http://dx.doi.org/10.4062/biomolther.2021.192

The Role of Mitochondrial Biogenesis Dysfunction in Diabetic Cardiomyopathy  

Tao, Li-Chan (The Third Affiliated Hospital of Soochow University)
Wang, Ting-ting (The Third Affiliated Hospital of Soochow University)
Zheng, Lu (The Third Affiliated Hospital of Soochow University)
Hua, Fei (The Third Affiliated Hospital of Soochow University)
Li, Jian-Jun (State Key Laboratory of Cardiovascular Diseases, Fu Wai Hospital, National Center for Cardiovascular Diseases, Chinese Academy of Medical Sciences and Peking Union Medical College)
Publication Information
Biomolecules & Therapeutics / v.30, no.5, 2022 , pp. 399-408 More about this Journal
Abstract
Diabetic cardiomyopathy (DCM) is described as abnormalities of myocardial structure and function in diabetic patients without other well-established cardiovascular factors. Although multiple pathological mechanisms involving in this unique myocardial disorder, mitochondrial dysfunction may play an important role in its development of DCM. Recently, considerable progresses have suggested that mitochondrial biogenesis is a tightly controlled process initiating mitochondrial generation and maintaining mitochondrial function, appears to be associated with DCM. Nonetheless, an outlook on the mechanisms and clinical relevance of dysfunction in mitochondrial biogenesis among patients with DCM is not completely understood. In this review, hence, we will summarize the role of mitochondrial biogenesis dysfunction in the development of DCM, especially the molecular underlying mechanism concerning the signaling pathways beyond the stimulation and inhibition of mitochondrial biogenesis. Additionally, the evaluations and potential therapeutic strategies regarding mitochondrial biogenesis dysfunction in DCM is also presented.
Keywords
Mitochondrial biogenesis; Diabetes; Cardiomyopathy; $PGC-1{\alpha}$; Diabetic cardiomyopathy;
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1 Zhou, L., Yu, M., Arshad, M., Wang, W., Lu, Y., Gong, J., Gu, Y., Li, P. and Xu, L. (2018) Coordination among lipid droplets, peroxisomes, and mitochondria regulates energy expenditure through the CIDE-ATGL-PPARα pathway in adipocytes. Diabetes 67, 1935-1948.   DOI
2 Takada, S., Masaki, Y., Kinugawa, S., Matsumoto, J., Furihata, T., Mizushima, W., Kadoguchi, T., Fukushima, A., Homma, T., Takahashi, M., Harashima, S., Matsushima, S., Yokota, T., Tanaka, S., Okita, K. and Tsutsui, H. (2016) Dipeptidyl peptidase-4 inhibitor improved exercise capacity and mitochondrial biogenesis in mice with heart failure via activation of glucagon-like peptide-1 receptor signalling. Cardiovasc. Res. 111, 338-347.   DOI
3 Thirupathi, A. and de Souza, C. T. (2017) Multi-regulatory network of ROS: the interconnection of ROS, PGC-1 alpha, and AMPK-SIRT1 during exercise. J. Physiol. Biochem. 73, 487-494.   DOI
4 Veeranki, S., Givvimani, S., Kundu, S., Metreveli, N., Pushpakumar, S. and Tyagi, S. C. (2016) Moderate intensity exercise prevents diabetic cardiomyopathy associated contractile dysfunction through restoration of mitochondrial function and connexin 43 levels in db/db mice. J. Mol. Cell. Cardiol. 92, 163-173.   DOI
5 Shen, X., Zheng, S., Thongboonkerd, V., Xu, M., Pierce, W. M., Jr., Klein, J. B. and Epstein, P. N. (2004) Cardiac mitochondrial damage and biogenesis in a chronic model of type 1 diabetes. Am. J. Physiol. Endocrinol. Metab. 287, E896-E905.   DOI
6 Momiyama, Y., Furutani, M., Suzuki, Y., Ohmori, R., Imamura, S., Mokubo, A., Asahina, T., Murata, C., Kato, K., Anazawa, S., Hosokawa, K., Atsumi, Y., Matsuoka, K., Kimura, M., Kasanuki, H., Ohsuzu, F. and Matsuoka, R. (2003) A mitochondrial DNA variant associated with left ventricular hypertrophy in diabetes. Biochem. Biophys. Res. Commun. 312, 858-864.   DOI
7 Momiyama, Y., Suzuki, Y., Ohtomo, M., Atsumi, Y., Matsuoka, K., Ohsuzu, F. and Kimura, M. (2002) Cardiac autonomic nervous dysfunction in diabetic patients with a mitochondrial DNA mutation: assessment by heart rate variability. Diabetes Care 25, 2308-2313.   DOI
8 Moore, M. L., Park, E. A. and McMillin, J. B. (2003) Upstream stimulatory factor represses the induction of carnitine palmitoyltransferase-Ibeta expression by PGC-1. J. Biol. Chem. 278, 17263-17268.   DOI
9 Murtaza, G., Virk, H. U. H., Khalid, M., Lavie, C. J., Ventura, H., Mukherjee, D., Ramu, V., Bhogal, S., Kumar, G., Shanmugasundaram, M. and Paul, T. K. (2019) Diabetic cardiomyopathy - a comprehensive updated review. Prog. Cardiovasc. Dis. 62, 315-326.   DOI
10 Nakae, J., Cao, Y., Oki, M., Orba, Y., Sawa, H., Kiyonari, H., Iskandar, K., Suga, K., Lombes, M. and Hayashi, Y. (2008) Forkhead transcription factor FoxO1 in adipose tissue regulates energy storage and expenditure. Diabetes 57, 563-576.   DOI
11 Nauck, M. A., Meier, J. J., Cavender, M. A., Abd El Aziz, M. and Drucker, D. J. (2017) Cardiovascular actions and clinical outcomes with glucagon-like peptide-1 receptor agonists and dipeptidyl peptidase-4 inhibitors. Circulation 136, 849-870.   DOI
12 Melser, S., Lavie, J. and Benard, G. (2015) Mitochondrial degradation and energy metabolism. Biochim. Biophys. Acta 1853, 2812-2821.   DOI
13 Ploumi, C., Daskalaki, I. and Tavernarakis, N. (2017) Mitochondrial biogenesis and clearance: a balancing act. FEBS J. 284, 183-195.   DOI
14 Golpich, M., Amini, E., Mohamed, Z., Azman Ali, R., Mohamed Ibrahim, N. and Ahmadiani, A. (2017) Mitochondrial dysfunction and biogenesis in neurodegenerative diseases: pathogenesis and treatment. CNS Neurosci. Ther. 23, 5-22.   DOI
15 Wiviott, S. D., Raz, I., Bonaca, M. P., Mosenzon, O., Kato, E. T., Cahn, A., Silverman, M. G., Zelniker, T. A., Kuder, J. F., Murphy, S. A., Bhatt, D. L., Leiter, L. A., McGuire, D. K., Wilding, J. P. H., Ruff, C. T., Gause-Nilsson, I. A. M., Fredriksson, M., Johansson, P. A., Langkilde, A. M. and Sabatine, M. S. (2019) Dapagliflozin and cardiovascular outcomes in type 2 diabetes. N. Engl. J. Med. 380, 347-357.   DOI
16 Yan, W., Zhang, H., Liu, P., Wang, H., Liu, J., Gao, C., Liu, Y., Lian, K., Yang, L., Sun, L., Guo, Y., Zhang, L., Dong, L., Lau, W. B., Gao, E., Gao, F., Xiong, L., Wang, H., Qu, Y. and Tao, L. (2013) Impaired mitochondrial biogenesis due to dysfunctional adiponectin-AMPK-PGC-1α signaling contributing to increased vulnerability in diabetic heart. Basic Res. Cardiol. 108, 329.
17 Yang, Z. F., Drumea, K., Mott, S., Wang, J. and Rosmarin, A. G. (2014) GABP transcription factor (nuclear respiratory factor 2) is required for mitochondrial biogenesis. Mol. Cell. Biol. 34, 3194-3201.   DOI
18 Popov, L. D. (2020) Mitochondrial biogenesis: an update. J. Cell. Mol. Med. 24, 4892-4899.   DOI
19 Fernandez-Marcos, P. J. and Auwerx, J. (2011) Regulation of PGC-1α, a nodal regulator of mitochondrial biogenesis. Am. J. Clin. Nutr. 93, 884s-890s.   DOI
20 Ji, H., Wang, J., Muid, D., Song, W., Jiang, Y. and Zhou, H. (2022) FUNDC1 activates the mitochondrial unfolded protein response to preserve mitochondrial quality control in cardiac ischemia/reperfusion injury. Cell. Signal. 92, 110249.
21 Kannel, W. B., Hjortland, M. and Castelli, W. P. (1974) Role of diabetes in congestive heart failure: the Framingham study. Am. J. Cardiol. 34, 29-34.   DOI
22 Kim, H. K., Ko, T. H., Song, I. S., Jeong, Y. J., Heo, H. J., Jeong, S. H., Kim, M., Park, N. M., Seo, D. Y., Kha, P. T., Kim, S. W., Lee, S. R., Cho, S. W., Won, J. C., Youm, J. B., Ko, K. S., Rhee, B. D., Kim, N., Cho, K. I., Shimizu, I., Minamino, T., Ha, N. C., Park, Y. S., Nilius, B. and Han, J. (2020) BH4 activates CaMKK2 and rescues the cardiomyopathic phenotype in rodent models of diabetes. Life Sci. Alliance 3, e201900619.   DOI
23 Lee, H. C. and Wei, Y. H. (2000) Mitochondrial role in life and death of the cell. J. Biomed. Sci. 7, 2-15.   DOI
24 Li, Y., Wei, X., Liu, S. L., Zhao, Y., Jin, S. and Yang, X. Y. (2021b) Salidroside protects cardiac function in mice with diabetic cardiomyopathy via activation of mitochondrial biogenesis and SIRT3. Phytother. Res. 35, 4579-4591.   DOI
25 Sun, W., Quan, N., Wang, L., Yang, H., Chu, D., Liu, Q., Zhao, X., Leng, J. and Li, J. (2016) Cardiac-specific deletion of the Pdha1 gene sensitizes heart to toxicological actions of ischemic stress. Toxicol. Sci. 153, 411.
26 Yao, K., Zhang, W. W., Yao, L., Yang, S., Nie, W. and Huang, F. (2016) Carvedilol promotes mitochondrial biogenesis by regulating the PGC-1/TFAM pathway in human umbilical vein endothelial cells (HUVECs). Biochem. Biophys. Res. Commun. 470, 961-966.   DOI
27 Yu, L. M., Dong, X., Xue, X. D., Xu, S., Zhang, X., Xu, Y. L., Wang, Z. S., Wang, Y., Gao, H., Liang, Y. X., Yang, Y. and Wang, H. S. (2021) Melatonin attenuates diabetic cardiomyopathy and reduces myocardial vulnerability to ischemia-reperfusion injury by improving mitochondrial quality control: role of SIRT6. J. Pineal Res. 70, e12698.
28 Kosuru, R., Kandula, V., Rai, U., Prakash, S., Xia, Z. and Singh, S. (2018) Pterostilbene decreases cardiac oxidative stress and inflammation via activation of AMPK/Nrf2/HO-1 pathway in fructosefed diabetic rats. Cardiovasc. Drugs Ther. 32, 147-163.   DOI
29 Bruggisser, J., Kaser, S., Mani, J. and Schneider, A. (2017) Biogenesis of a mitochondrial outer membrane protein in Trypanosoma brucei: targeting signal and dependence on a unique biogenesis factor. J. Biol. Chem. 292, 3400-3410.   DOI
30 Shao, Q., Meng, L., Lee, S., Tse, G., Gong, M., Zhang, Z., Zhao, J., Zhao, Y., Li, G. and Liu, T. (2019) Empagliflozin, a sodium glucose co-transporter-2 inhibitor, alleviates atrial remodeling and improves mitochondrial function in high-fat diet/streptozotocin-induced diabetic rats. Cardiovasc. Diabetol. 18, 165.
31 Tanajak, P., Sa-Nguanmoo, P., Sivasinprasasn, S., Thummasorn, S., Siri-Angkul, N., Chattipakorn, S. C. and Chattipakorn, N. (2018) Cardioprotection of dapagliflozin and vildagliptin in rats with cardiac ischemia-reperfusion injury. J. Endocrinol. 236, 69-84.   DOI
32 Tao, L., Huang, X., Xu, M., Yang, L. and Hua, F. (2020) MiR-144 protects the heart from hyperglycemia-induced injury by regulating mitochondrial biogenesis and cardiomyocyte apoptosis. FASEB J. 34, 2173-2197.   DOI
33 Ueno, H. and Shiotani, H. (1999) Cardiac abnormalities in diabetic patients with mutation in the mitochondrial tRNA(Leu(UUR)) gene. Jpn. Circ. J. 63, 877-880.   DOI
34 Vafai, S. B. and Mootha, V. K. (2012) Mitochondrial disorders as windows into an ancient organelle. Nature 491, 374-383.   DOI
35 Xiong, Y., Hai, C. X., Fang, W. J., Lei, Y. P., Li, X. M. and Zhou, X. K. (2020) Endogenous asymmetric dimethylarginine accumulation contributes to the suppression of myocardial mitochondrial biogenesis in type 2 diabetic rats. Nutr. Metab. 17, 72.
36 Bruni, F., Polosa, P. L., Gadaleta, M. N., Cantatore, P. and Roberti, M. (2010) Nuclear respiratory factor 2 induces the expression of many but not all human proteins acting in mitochondrial DNA transcription and replication. J. Biol. Chem. 285, 3939-3948.   DOI
37 Cook, G. A., Lavrentyev, E. N., Pham, K. and Park, E. A. (2017) Streptozotocin diabetes increases mRNA expression of ketogenic enzymes in the rat heart. Biochim. Biophys. Acta Gen. Subj. 1861, 307-312.   DOI
38 Cayci, T., Kurt, Y. G., Akgul, E. O. and Kurt, B. (2012) Does mtDNA copy number mean mitochondrial abundance? J. Assist. Reprod. Genet. 29, 855.
39 Taherzadeh-Fard, E., Saft, C., Akkad, D. A., Wieczorek, S., Haghikia, A., Chan, A., Epplen, J. T. and Arning, L. (2011) PGC-1alpha downstream transcription factors NRF-1 and TFAM are genetic modifiers of Huntington disease. Mol. Neurodegener. 6, 32.
40 Wang, H., Bei, Y., Lu, Y., Sun, W., Liu, Q., Wang, Y., Cao, Y., Chen, P., Xiao, J. and Kong, X. (2015) Exercise prevents cardiac injury and improves mitochondrial biogenesis in advanced diabetic cardiomyopathy with PGC-1α and Akt activation. Cell. Physiol. Biochem. 35, 2159-2168.   DOI
41 Xiong, Y., He, Y. L., Li, X. M., Nie, F. and Zhou, X. K. (2021) Endogenous asymmetric dimethylarginine accumulation precipitates the cardiac and mitochondrial dysfunctions in type 1 diabetic rats. Eur. J. Pharmacol. 902, 174081.
42 Verma, S., McGuire, D. K., Bain, S. C., Bhatt, D. L., Leiter, L. A., Mazer, C. D., Monk Fries, T., Pratley, R. E., Rasmussen, S., Vrazic, H., Zinman, B. and Buse, J. B. (2020) Effects of glucagon-like peptide-1 receptor agonists liraglutide and semaglutide on cardiovascular and renal outcomes across body mass index categories in type 2 diabetes: results of the LEADER and SUSTAIN 6 trials. Diabetes Obes. Metab. 22, 2487-2492.   DOI
43 Jia, G., Hill, M. A. and Sowers, J. R. (2018a) Diabetic cardiomyopathy: an update of mechanisms contributing to this clinical entity. Circ. Res. 122, 624-638.   DOI
44 Gleyzer, N. and Scarpulla, R. C. (2016) Concerted action of PGC-1-related coactivator (PRC) and c-MYC in the stress response to mitochondrial dysfunction. J. Biol. Chem. 291, 25529-25541.   DOI
45 Habibi, J., Aroor, A. R., Sowers, J. R., Jia, G., Hayden, M. R., Garro, M., Barron, B., Mayoux, E., Rector, R. S., Whaley-Connell, A. and DeMarco, V. G. (2017) Sodium glucose transporter 2 (SGLT2) inhibition with empagliflozin improves cardiac diastolic function in a female rodent model of diabetes. Cardiovasc. Diabetol. 16, 9.
46 Herzig, S., Long, F., Jhala, U. S., Hedrick, S., Quinn, R., Bauer, A., Rudolph, D., Schutz, G., Yoon, C., Puigserver, P., Spiegelman, B. and Montminy, M. (2001) CREB regulates hepatic gluconeogenesis through the coactivator PGC-1. Nature 413, 179-183.   DOI
47 Jia, G., Whaley-Connell, A. and Sowers, J. R. (2018b) Diabetic cardiomyopathy: a hyperglycaemia- and insulin-resistance-induced heart disease. Diabetologia 61, 21-28.   DOI
48 Angus, L. M., Chakkalakal, J. V., Mejat, A., Eibl, J. K., Belanger, G., Megeney, L. A., Chin, E. R., Schaeffer, L., Michel, R. N. and Jasmin, B. J. (2005) Calcineurin-NFAT signaling, together with GABP and peroxisome PGC-1{alpha}, drives utrophin gene expression at the neuromuscular junction. Am. J. Physiol. Cell Physiol. 289, C908-C917.   DOI
49 Biswas, M. and Chan, J. Y. (2010) Role of Nrf1 in antioxidant response element-mediated gene expression and beyond. Toxicol. Appl. Pharmacol. 244, 16-20.   DOI
50 Balaban, R. S. (1990) Regulation of oxidative phosphorylation in the mammalian cell. Am. J. Physiol. 258, C377-C389.   DOI
51 Blesa, J. R., Prieto-Ruiz, J. A., Abraham, B. A., Harrison, B. L., Hegde, A. A. and Hernandez-Yago, J. (2008) NRF-1 is the major transcription factor regulating the expression of the human TOMM34 gene. Biochem. Cell Biol. 86, 46-56.   DOI
52 Dillmann, W. H. (2019) Diabetic cardiomyopathy. Circ. Res. 124, 1160-1162.   DOI
53 Fang, W. J., Wang, C. J., He, Y., Zhou, Y. L., Peng, X. D. and Liu, S. K. (2018) Resveratrol alleviates diabetic cardiomyopathy in rats by improving mitochondrial function through PGC-1α deacetylation. Acta Pharmacol. Sin. 39, 59-73.   DOI
54 GBD 2015 Disease and Injury Incidence and Prevalence Collaborators (2016) Global, regional, and national incidence, prevalence, and years lived with disability for 310 diseases and injuries, 1990-2015: a systematic analysis for the Global Burden of Disease Study 2015. Lancet 388, 1545-1602.   DOI
55 Kristensen, S. L., Rorth, R., Jhund, P. S., Docherty, K. F., Sattar, N., Preiss, D., Kober, L., Petrie, M. C. and McMurray, J. J. V. (2019) Cardiovascular, mortality, and kidney outcomes with GLP-1 receptor agonists in patients with type 2 diabetes: a systematic review and meta-analysis of cardiovascular outcome trials. Lancet Diabetes Endocrinol. 7, 776-785.   DOI
56 Liang, Q. and Kobayashi, S. (2016) Mitochondrial quality control in the diabetic heart. J. Mol. Cell. Cardiol. 95, 57-69.   DOI
57 Liu, J., Zou, Y., Tang, Y., Xi, M., Xie, L., Zhang, Q. and Gong, J. (2016) Circulating cell-free mitochondrial deoxyribonucleic acid is increased in coronary heart disease patients with diabetes mellitus. J. Diabetes Investig. 7, 109-114.   DOI
58 Karamanlidis, G., Nascimben, L., Couper, G. S., Shekar, P. S., del Monte, F. and Tian, R. (2010) Defective DNA replication impairs mitochondrial biogenesis in human failing hearts. Circ. Res. 106, 1541-1548.   DOI
59 Knapp, M., Tu, X. and Wu, R. (2019) Vascular endothelial dysfunction, a major mediator in diabetic cardiomyopathy. Acta Pharmacol. Sin. 40, 1-8.   DOI
60 Ko, T. H., Marquez, J. C., Kim, H. K., Jeong, S. H., Lee, S., Youm, J. B., Song, I. S., Seo, D. Y., Kim, H. J., Won, D. N., Cho, K. I., Choi, M. G., Rhee, B. D., Ko, K. S., Kim, N., Won, J. C. and Han, J. (2018) Resistance exercise improves cardiac function and mitochondrial efficiency in diabetic rat hearts. Pflugers Arch. 470, 263-275.   DOI
61 Lam, C. S. (2015) Diabetic cardiomyopathy: an expression of stage B heart failure with preserved ejection fraction. Diab. Vasc. Dis. Res. 12, 234-238.   DOI
62 Li, N. and Zhou, H. (2020) SGLT2 Inhibitors: a novel player in the treatment and prevention of diabetic cardiomyopathy. Drug Des. Devel. Ther. 14, 4775-4788.   DOI
63 Li, Y., Feng, Y. F., Liu, X. T., Li, Y. C., Zhu, H. M., Sun, M. R., Li, P., Liu, B. and Yang, H. (2021a) Songorine promotes cardiac mitochondrial biogenesis via Nrf2 induction during sepsis. Redox Biol. 38, 101771.
64 Berthiaume, J. M., Kurdys, J. G., Muntean, D. M. and Rosca, M. G. (2019) Mitochondrial NAD(+)/NADH redox state and diabetic cardiomyopathy. Antioxid. Redox. Signal. 30, 375-398.   DOI
65 Kannel, W. B. and McGee, D. L. (1979) Diabetes and cardiovascular disease. The Framingham study. JAMA 241, 2035-2038.   DOI
66 Nayor, M., Shah, R. V., Miller, P. E., Blodgett, J. B., Tanguay, M., Pico, A. R., Murthy, V. L., Malhotra, R., Houstis, N. E., Deik, A., Pierce, K. A., Bullock, K., Dailey, L., Velagaleti, R. S., Moore, S. A., Ho, J. E., Baggish, A. L., Clish, C. B., Larson, M. G., Vasan, R. S. and Lewis, G. D. (2020) Metabolic architecture of acute exercise response in middle-aged adults in the community. Circulation 142, 1905-1924.   DOI
67 Neal, B., Perkovic, V., Matthews, D. R., Mahaffey, K. W., Fulcher, G., Meininger, G., Erondu, N., Desai, M., Shaw, W., Vercruysse, F., Yee, J., Deng, H. and de Zeeuw, D. (2017) Rationale, design and baseline characteristics of the CANagliflozin cardioVascular Assessment Study-Renal (CANVAS-R): a randomized, placebo-controlled trial. Diabetes Obes. Metab. 19, 387-393.   DOI
68 Packer, M. (2020) Autophagy-dependent and -independent modulation of oxidative and organellar stress in the diabetic heart by glucose-lowering drugs. Cardiovasc. Diabetol. 19, 62.
69 Al Amir Dache, Z., Otandault, A., Tanos, R., Pastor, B., Meddeb, R., Sanchez, C., Arena, G., Lasorsa, L., Bennett, A., Grange, T., El Messaoudi, S., Mazard, T., Prevostel, C. and Thierry, A. R. (2020) Blood contains circulating cell-free respiratory competent mitochondria. FASEB J. 34, 3616-3630.   DOI
70 Liu, X. D., Li, Y. G., Wang, G. Y., Bi, Y. G., Zhao, Y., Yan, M. L., Liu, X., Wei, M., Wan, L. L. and Zhang, Q. Y. (2020) Metformin protects high glucose-cultured cardiomyocytes from oxidative stress by promoting NDUFA13 expression and mitochondrial biogenesis via the AMPK signaling pathway. Mol. Med. Rep. 22, 5262-5270.   DOI
71 Marciniak, C., Marechal, X., Montaigne, D., Neviere, R. and Lancel, S. (2014) Cardiac contractile function and mitochondrial respiration in diabetes-related mouse models. Cardiovasc. Diabetol. 13, 118.
72 Lorenzo-Almoros, A., Tunon, J., Orejas, M., Cortes, M., Egido, J. and Lorenzo, O. (2017) Diagnostic approaches for diabetic cardiomyopathy. Cardiovasc. Diabetol. 16, 28.
73 Ma, S., Feng, J., Zhang, R., Chen, J., Han, D., Li, X., Yang, B., Li, X., Fan, M., Li, C., Tian, Z., Wang, Y. and Cao, F. (2017) SIRT1 activation by resveratrol alleviates cardiac dysfunction via mitochondrial regulation in diabetic cardiomyopathy mice. Oxid. Med. Cell. Longev. 2017, 4602715.
74 Malik, A. N. and Czajka, A. (2013) Is mitochondrial DNA content a potential biomarker of mitochondrial dysfunction? Mitochondrion 13, 481-492.   DOI
75 Marso, S. P., Daniels, G. H., Brown-Frandsen, K., Kristensen, P., Mann, J. F., Nauck, M. A., Nissen, S. E., Pocock, S., Poulter, N. R., Ravn, L. S., Steinberg, W. M., Stockner, M., Zinman, B., Bergenstal, R. M. and Buse, J. B. (2016) Liraglutide and cardiovascular outcomes in type 2 diabetes. N. Engl. J. Med. 375, 311-322.   DOI
76 Bordoni, L., Petracci, I., Pelikant-Malecka, I., Radulska, A., Piangerelli, M., Samulak, J. J., Lewicki, L., Kalinowski, L., Gabbianelli, R. and Olek, R. A. (2021) Mitochondrial DNA copy number and trimethylamine levels in the blood: new insights on cardiovascular disease biomarkers. FASEB J. 35, e21694.
77 Cameron, R. B., Beeson, C. C. and Schnellmann, R. G. (2016) Development of therapeutics that induce mitochondrial biogenesis for the treatment of acute and chronic degenerative diseases. J. Med. Chem. 59, 10411-10434.   DOI
78 Qiu, C., Hevner, K., Abetew, D., Sedensky, M., Morgan, P., Enquobahrie, D. A. and Williams, M. A. (2013) Mitochondrial DNA copy number and oxidative DNA damage in placental tissues from gestational diabetes and control pregnancies: a pilot study. Clin. Lab. 59, 655-660.
79 Zinman, B., Inzucchi, S. E., Lachin, J. M., Wanner, C., Ferrari, R., Fitchett, D., Bluhmki, E., Hantel, S., Kempthorne-Rawson, J., Newman, J., Johansen, O. E., Woerle, H. J. and Broedl, U. C. (2014) Rationale, design, and baseline characteristics of a randomized, placebo-controlled cardiovascular outcome trial of empagliflozin (EMPA-REG OUTCOMETM). Cardiovasc. Diabetol. 13, 102.
80 De Jong, K. A. and Lopaschuk, G. D. (2017) Complex energy metabolic changes in heart failure with preserved ejection fraction and heart failure with reduced ejection fraction. Can. J. Cardiol. 33, 860-871.   DOI
81 Quan, Y., Xin, Y., Tian, G., Zhou, J. and Liu, X. (2020) Mitochondrial ROS-modulated mtDNA: a potential target for cardiac aging. Oxid. Med. Cell. Longev. 2020, 9423593.
82 Reaven, P. D., Emanuele, N. V., Wiitala, W. L., Bahn, G. D., Reda, D. J., McCarren, M., Duckworth, W. C. and Hayward, R. A. (2019) Intensive glucose control in patients with type 2 diabetes - 15-year follow-up. N. Engl. J. Med. 380, 2215-2224.   DOI
83 Riehle, C. and Bauersachs, J. (2018) Of mice and men: models and mechanisms of diabetic cardiomyopathy. Basic Res. Cardiol. 114, 2.
84 Zhang, X., Zhang, Z., Yang, Y., Suo, Y., Liu, R., Qiu, J., Zhao, Y., Jiang, N., Liu, C., Tse, G., Li, G. and Liu, T. (2018) Alogliptin prevents diastolic dysfunction and preserves left ventricular mitochondrial function in diabetic rabbits. Cardiovasc. Diabetol. 17, 160.
85 Lu, S., Liao, Z., Lu, X., Katschinski, D. M., Mercola, M., Chen, J., Heller Brown, J., Molkentin, J. D., Bossuyt, J. and Bers, D. M. (2020) Hyperglycemia acutely increases cytosolic reactive oxygen species via O-linked GlcNAcylation and CaMKII activation in mouse ventricular myocytes. Circ. Res. 126, e80-e96.
86 Yurista, S. R., Sillje, H. H. W., Rienstra, M., de Boer, R. A. and Westenbrink, B. D. (2020) Sodium-glucose co-transporter 2 inhibition as a mitochondrial therapy for atrial fibrillation in patients with diabetes? Cardiovasc. Diabetol. 19, 5.
87 Zhang, M., Lin, J., Wang, S., Cheng, Z., Hu, J., Wang, T., Man, W., Yin, T., Guo, W., Gao, E., Reiter, R. J., Wang, H. and Sun, D. (2017) Melatonin protects against diabetic cardiomyopathy through Mst1/Sirt3 signaling. J. Pineal Res. 63, e12418.
88 Zhang, Z., Zhang, X., Meng, L., Gong, M., Li, J., Shi, W., Qiu, J., Yang, Y., Zhao, J., Suo, Y., Liang, X., Wang, X., Tse, G., Jiang, N., Li, G., Zhao, Y. and Liu, T. (2021) Pioglitazone inhibits diabetes-induced atrial mitochondrial oxidative stress and improves mitochondrial biogenesis, dynamics, and function through the PPAR-γ/PGC-1α signaling pathway. Front. Pharmacol. 12, 658362.
89 Satoh, J., Kawana, N. and Yamamoto, Y. (2013) Pathway analysis of ChIP-Seq-based NRF1 target genes suggests a logical hypothesis of their involvement in the pathogenesis of neurodegenerative diseases. Gene Regul. Syst. Bio. 7, 139-152.
90 Sakamoto, T., Matsuura, T. R., Wan, S., Ryba, D. M., Kim, J. U., Won, K. J., Lai, L., Petucci, C., Petrenko, N., Musunuru, K., Vega, R. B. and Kelly, D. P. (2020) A critical role for estrogen-related receptor signaling in cardiac maturation. Circ. Res. 126, 1685-1702.   DOI
91 Scheen, A. J. (2018) Cardiovascular effects of new oral glucose-lowering agents: DPP-4 and SGLT-2 inhibitors. Circ. Res. 122, 1439-1459.   DOI
92 Paolillo, S., Marsico, F., Prastaro, M., Renga, F., Esposito, L., De Martino, F., Di Napoli, P., Esposito, I., Ambrosio, A., Ianniruberto, M., Mennella, R., Paolillo, R. and Gargiulo, P. (2019) Diabetic cardiomyopathy: definition, diagnosis, and therapeutic implications. Heart Fail. Clin. 15, 341-347.   DOI
93 Parim, B., Sathibabu Uddandrao, V. V. and Saravanan, G. (2019) Diabetic cardiomyopathy: molecular mechanisms, detrimental effects of conventional treatment, and beneficial effects of natural therapy. Heart Fail. Rev. 24, 279-299.   DOI
94 Peng, X., Li, L., Zhang, M., Zhao, Q., Wu, K., Bai, R., Ruan, Y. and Liu, N. (2020) Sodium-glucose cotransporter 2 inhibitors potentially prevent atrial fibrillation by ameliorating ion handling and mitochondrial dysfunction. Front. Physiol. 11, 912.
95 Peterson, L. R. and Gropler, R. J. (2020) Metabolic and molecular imaging of the diabetic cardiomyopathy. Circ. Res. 126, 1628-1645.   DOI