Activating Connexin43 gap junctions primes adipose tissue for therapeutic intervention

Acta Pharmaceutica Sinica B - Tập 12 - Trang 3063-3072 - 2022
Yi Zhu1,2, Na Li1, Mingyang Huang2, Xi Chen2, Yu A. An1, Jianping Li3, Shangang Zhao1, Jan-Bernd Funcke1, Jianhong Cao4, Zhenyan He4, Qingzhang Zhu1, Zhuzhen Zhang1, Zhao V. Wang3, Lin Xu5,6, Kevin W. Williams4, Chien Li7, Kevin Grove7, Philipp E. Scherer1,8
1Touchstone Diabetes Center, Department of Internal Medicine, The University of Texas Southwestern Medical Center at Dallas, Dallas, TX 75390, USA
2Children's Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine, Houston, TX 77030, USA
3Division of Cardiology, Department of Internal Medicine, the University of Texas Southwestern Medical Center at Dallas, Dallas, TX 75390, USA
4Division of Hypothalamic Research, Department of Internal Medicine, The University of Texas Southwestern Medical Center at Dallas, Dallas, TX 75390, USA
5Quantitative Biomedical Research Center, Department of Population and Data Sciences, the University of Texas Southwestern Medical Center at Dallas, Dallas, TX 75390, USA
6Department of Pediatrics, the University of Texas Southwestern Medical Center at Dallas, Dallas, TX 75390, USA
7Novo Nordisk Research Center, Seattle, WA 98109, USA
8Department of Cell Biology, the University of Texas Southwestern Medical Center at Dallas, Dallas, TX 75390, USA

Tài liệu tham khảo

Khaodhiar, 1999, Obesity and its comorbid conditions, Clin Cornerstone, 2, 17, 10.1016/S1098-3597(99)90002-9 White, 2014, A brief history of the development of diabetes medications, Diabetes Spectr, 27, 82, 10.2337/diaspect.27.2.82 Gimeno, 2014, FGF21-based pharmacotherapy—potential utility for metabolic disorders, Trends Endocrinol Metabol, 25, 303, 10.1016/j.tem.2014.03.001 Moller, 2012, Metabolic disease drug discovery—"hitting the target" is easier said than done, Cell Metabol, 15, 19, 10.1016/j.cmet.2011.10.012 Crewe, 2017, The ominous triad of adipose tissue dysfunction: inflammation, fibrosis, and impaired angiogenesis, J Clin Invest, 127, 74, 10.1172/JCI88883 Kusminski, 2016, Targeting adipose tissue in the treatment of obesity-associated diabetes, Nat Rev Drug Discov, 15, 639, 10.1038/nrd.2016.75 Petrovic, 2010, J Biol Chem, 285, 7153, 10.1074/jbc.M109.053942 Wu, 2012, Beige adipocytes are a distinct type of thermogenic fat cell in mouse and human, Cell, 150, 366, 10.1016/j.cell.2012.05.016 Shinoda, 2015, Genetic and functional characterization of clonally derived adult human brown adipocytes, Nat Med, 21, 389, 10.1038/nm.3819 Rogers, 2012, Aging leads to a programmed loss of brown adipocytes in murine subcutaneous white adipose tissue, Aging Cell, 11, 1074, 10.1111/acel.12010 Hanssen, 2015, Short-term cold acclimation improves insulin sensitivity in patients with type 2 diabetes mellitus, Nat Med, 21, 863, 10.1038/nm.3891 Yoneshiro, 2011, Age-related decrease in cold-activated brown adipose tissue and accumulation of body fat in healthy humans, Obesity, 19, 1755, 10.1038/oby.2011.125 Frayn, 2014, Regulation of human subcutaneous adipose tissue blood flow, Int J Obes, 38, 1019, 10.1038/ijo.2013.200 Baskin, 2018, Regulation of human adipose tissue activation, gallbladder size, and bile acid metabolism by a β3-adrenergic receptor agonist, Diabetes, 67, 2113, 10.2337/db18-0462 Cypess, 2015, Activation of human brown adipose tissue by a β3-adrenergic receptor agonist, Cell Metabol, 21, 33, 10.1016/j.cmet.2014.12.009 Cawthorne, 1992, BRL 35135, a potent and selective atypical β-adrenoceptor agonist, Am J Clin Nutr, 55, 10.1093/ajcn/55.1.252s Weyer, 1998, Increase in insulin action and fat oxidation after treatment with CL 316,243, a highly selective β3-adrenoceptor agonist in humans, Diabetes, 47, 1555, 10.2337/diabetes.47.10.1555 Larsen, 2002, Effect of a 28-d treatment with L-796568, a novel β3-adrenergic receptor agonist, on energy expenditure and body composition in obese men, Am J Clin Nutr, 76, 780, 10.1093/ajcn/76.4.780 Redman, 2007, Lack of an effect of a novel β3-adrenoceptor agonist, TAK-677, on energy metabolism in obese individuals: a double-blind, placebo-controlled randomized study, J Clin Endocrinol Metab, 92, 527, 10.1210/jc.2006-1740 Kharitonenkov, 2005, FGF-21 as a novel metabolic regulator, J Clin Invest, 115, 1627, 10.1172/JCI23606 Fisher, 2012, FGF21 regulates PGC-1α and browning of white adipose tissues in adaptive thermogenesis, Genes Dev, 26, 271, 10.1101/gad.177857.111 Gaich, 2013, The effects of LY2405319, an FGF21 analog, in obese human subjects with type 2 diabetes, Cell Metabol, 18, 333, 10.1016/j.cmet.2013.08.005 Talukdar, 2016, A long-acting FGF21 molecule, PF-05231023, decreases body weight and improves lipid profile in non-human primates and type 2 diabetic subjects, Cell Metabol, 23, 427, 10.1016/j.cmet.2016.02.001 Zhu, 2016, Connexin 43 mediates white adipose tissue beiging by facilitating the propagation of sympathetic neuronal signals, Cell Metabol, 24, 420, 10.1016/j.cmet.2016.08.005 Zhu, 2013, Cardiac PI3K–Akt impairs insulin-stimulated glucose uptake independent of mTORC1 and GLUT4 translocation, Mol Endocrinol, 27, 172, 10.1210/me.2012-1210 Zhu, 2017, Hepatic GALE regulates whole-body glucose homeostasis by modulating Tff3 expression, Diabetes, 66, 2789, 10.2337/db17-0323 Wang, 2012, PrimerBank: a PCR primer database for quantitative gene expression analysis, 2012 update, Nucleic Acids Res, 40, D1144, 10.1093/nar/gkr1013 Zhu, 2021, Adipose tissue hyaluronan production improves systemic glucose homeostasis and primes adipocytes for CL 316,243-stimulated lipolysis, Nat Commun, 12, 4829, 10.1038/s41467-021-25025-4 Zhu, 2013, Mechanistic target of rapamycin (Mtor) is essential for murine embryonic heart development and growth, PLoS One, 8, e54221, 10.1371/journal.pone.0054221 Shao, 2016, Zfp423 maintains white adipocyte identity through suppression of the beige cell thermogenic gene program, Cell Metabol, 23, 1167, 10.1016/j.cmet.2016.04.023 Burke, 2014, Adipocytes in both brown and white adipose tissue of adult mice are functionally connected via gap junctions: implications for Chagas disease, Microb Infect, 16, 893, 10.1016/j.micinf.2014.08.006 So, 2016, Fibroblast growth factor 21 as an emerging therapeutic target for type 2 diabetes mellitus, Med Res Rev, 36, 672, 10.1002/med.21390 Lewis, 2017, Reduced adiposity attenuates FGF21 mediated metabolic improvements in the Siberian hamster, Sci Rep, 7, 4238, 10.1038/s41598-017-03607-x Veniant, 2012, FGF21 promotes metabolic homeostasis via white adipose and leptin in mice, PLoS One, 7, e40164, 10.1371/journal.pone.0040164 Schulz, 2015, Connexin 43 is an emerging therapeutic target in ischemia/reperfusion injury, cardioprotection and neuroprotection, Pharmacol Ther, 153, 90, 10.1016/j.pharmthera.2015.06.005 Sun, 2013, Fibrosis and adipose tissue dysfunction, Cell Metabol, 18, 470, 10.1016/j.cmet.2013.06.016 Chau, 2010, Fibroblast growth factor 21 regulates energy metabolism by activating the AMPK–SIRT1–PGC-1α pathway, Proc Natl Acad Sci U S A, 107, 12553, 10.1073/pnas.1006962107 Holland, 2013, An FGF21–adiponectin–ceramide axis controls energy expenditure and insulin action in mice, Cell Metabol, 17, 790, 10.1016/j.cmet.2013.03.019 Lin, 2013, Adiponectin mediates the metabolic effects of FGF21 on glucose homeostasis and insulin sensitivity in mice, Cell Metabol, 17, 779, 10.1016/j.cmet.2013.04.005 Owen, 2014, FGF21 acts centrally to induce sympathetic nerve activity, energy expenditure, and weight loss, Cell Metabol, 20, 670, 10.1016/j.cmet.2014.07.012 Lan, 2017, FGF19, FGF21, and an FGFR1/β-Klotho-activating antibody act on the nervous system to regulate body weight and glycemia, Cell Metabol, 26, 10.1016/j.cmet.2017.09.005 BonDurant, 2017, FGF21 regulates metabolism through adipose-dependent and -independent mechanisms, Cell Metabol, 25, 935, 10.1016/j.cmet.2017.03.005 Keipert, 2020, Endogenous FGF21-signaling controls paradoxical obesity resistance of UCP1-deficient mice, Nat Commun, 11, 624, 10.1038/s41467-019-14069-2 Samms, 2016, Overexpression of β-Klotho in adipose tissue sensitizes male mice to endogenous FGF21 and provides protection from diet-induced obesity, Endocrinology, 157, 1467, 10.1210/en.2015-1722