Adipose Mitochondrial Biogenesis Is Suppressed in db/db and High-Fat Diet–Fed Mice and Improved by Rosiglitazone
Abstract
The objective of this study was to further establish and confirm the relationship of adipose mitochondrial biogenesis in diabetes/obesity and the effects of rosiglitazone (RSG), a peroxisome proliferator-activated receptor (PPAR) gamma agonist, by systematically analyzing mitochondrial gene expression and function in two mouse models of obesity and type 2 diabetes. Using microarray technology, adipose mitochondrial gene transcription was studied in db/db, high-fat diet-fed C57BL/6 (HFD) and respective control mice with or without RSG treatment. The findings were extended using mitochondrial staining, DNA quantification, and measurements of citrate synthase activity. In db/db and HFD mice, gene transcripts associated with mitochondrial ATP production, energy uncoupling, mitochondrial ribosomal proteins, outer and inner membrane translocases, and mitochondrial heat-shock proteins were decreased in abundance, compared with db/+ and standard-fat diet-fed control mice, respectively. RSG dose-dependently increased these transcripts in both db/db and HFD mice and induced transcription of mitochondrial structural proteins and cellular antioxidant enzymes responsible for removal of reactive oxygen species generated by increased mitochondrial activity. Transcription factors, including PPAR coactivator (PGC)-1beta, PGC-1alpha, estrogen-related receptor alpha, and PPARalpha, were suppressed in both models and induced by RSG. The effects of RSG on adipose mitochondrial genes were confirmed by quantitative RT-PCR and further supported by mitochondrial staining, mitochondrial DNA quantification, and citrate synthase activity. Adipose mitochondrial biogenesis was overwhelmingly suppressed in both mouse models of diabetes/obesity and globally induced by RSG. These findings suggest an important role of adipose mitochondria in diabetes/obesity and the potential for new treatment approaches targeting adipose mitochondria.
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Administration of thiazolidinediones induces changes in mitochondrial content and remodeling in white adipocytes concomitantly with an improvement in insulin sensitivity.
“Administration of thiazolidinediones induces changes in mitochondrial content and remodeling in white adipocytes concomitantly with an improvement in insulin sensitivity (170, 173, 177, 190, 194 -198).”
From The role of mitochondria in the pathogenesis of type 2 diabetes (2010) · cites this paper as [190]
Both genetic and diet-induced obesity result in decreased mitochondrial density and OXPHOS activity in adipose tissue, potentially contributing to adipose tissue dysfunction and exacerbation of insulin resistance.
“Conversely, both genetic and dietinduced obesity result in decreased mitochondrial density and OXPHOS activity in adipose tissue (127, 177, 189 -191), potentially contributing to adipose tissue dysfunction and exacerbation of insulin resistance.”
From The role of mitochondria in the pathogenesis of type 2 diabetes (2010) · cites this paper as [190]
White adipocyte mitochondrial content is decreased in both rodent and human obesity and correlates with insulin resistance that accompanies obesity.
“White adipocyte mitochondrial content is decreased in both rodent and human obesity (177, 188 -191) and correlates with insulin resistance that accompanies obesity.”
From The role of mitochondria in the pathogenesis of type 2 diabetes (2010) · cites this paper as [190]
Cites
Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing
Benjamini, Y., & Hochberg, Y. (1995) · Journal of the Royal Statistical Society Series B: Statistical Methodology · doi:10.1111/j.2517-6161.1995.tb02031.x · Cited by 109,482 · see citing works
Obesity is associated with macrophage accumulation in adipose tissue
Weisberg, S. P., McCann, D., Desai, M., Rosenbaum, M., Leibel, R. L., & Ferrante, A. W. (2003) · Journal of Clinical Investigation · doi:10.1172/jci200319246 · Cited by 10,041 · see citing works
Xu, H., Barnes, G. T., Yang, Q., Tan, G., Yang, D., Chou, C. J., Sole, J., Nichols, A., Ross, J. S., Tartaglia, L. A., et al. (2003) · Journal of Clinical Investigation · doi:10.1172/jci200319451 · Cited by 6,760 · see citing works
A Novel Serum Protein Similar to C1q, Produced Exclusively in Adipocytes
Scherer, P. E., Williams, S. P., Fogliano, M., Baldini, G., & Lodish, H. F. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.45.26746 · Cited by 3,238 · see citing works
Adiponectin and adiponectin receptors in insulin resistance, diabetes, and the metabolic syndrome
Kadowaki, T. (2006) · Journal of Clinical Investigation · doi:10.1172/jci29126 · Cited by 2,824 · see citing works
Transcriptional co-activator PGC-1α drives the formation of slow-twitch muscle fibres
Lin, J., Wu, H., Tarr, P. T., Zhang, C.-Y., Wu, Z., Boss, O., Michael, L. F., Puigserver, P., Isotani, E., Olson, E. N., et al. (2002) · Nature · doi:10.1038/nature00904 · Cited by 2,546 · see citing works
Reactive oxygen species have a causal role in multiple forms of insulin resistance
Houstis, N., Rosen, E. D., & Lander, E. S. (2006) · Nature · doi:10.1038/nature04634 · Cited by 2,525 · see citing works
Abnormal splicing of the leptin receptor in diabetic mice
Lee, G.-H., Proenca, R., Montez, J. M., Carroll, K. M., Darvishzadeh, J. G., Lee, J. I., & Friedman, J. M. (1996) · Nature · doi:10.1038/379632a0 · Cited by 2,327 · see citing works
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 · see citing works
Metabolic control through the PGC-1 family of transcription coactivators
Lin, J., Handschin, C., & Spiegelman, B. M. (2005) · Cell Metabolism · doi:10.1016/j.cmet.2005.05.004 · Cited by 2,130 · cited 2× · see citing works
“The dual RSG actions on mitochondria and antioxidant enzymes could work through the upregulation of one or both of the PGC-1 proteins (Table 3) that have been shown to regulate both mitochondrial biogenesis and the antioxidant machinery (13,45).”
BackgroundPatti, M. E., Butte, A. J., Crunkhorn, S., Cusi, K., Berria, R., Kashyap, S., Miyazaki, Y., Kohane, I., Costello, M., Saccone, R., et al. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1032913100 · Cited by 1,952 · see citing works
Absence of S6K1 protects against age- and diet-induced obesity while enhancing insulin sensitivity
Um, S. H., Frigerio, F., Watanabe, M., Picard, F., Joaquin, M., Sticker, M., Fumagalli, S., Allegrini, P. R., Kozma, S. C., Auwerx, J., et al. (2004) · Nature · doi:10.1038/nature02866 · Cited by 1,677 · see citing works
PPARs and the complex journey to obesity
Evans, R. M., Barish, G. D., & Wang, Y.-X. (2004) · Nature Medicine · doi:10.1038/nm1025 · Cited by 1,621 · see citing works
CCR2 modulates inflammatory and metabolic effects of high-fat feeding
Weisberg, S. P., Hunter, D., Huber, R., Lemieux, J., Slaymaker, S., Vaddi, K., Charo, I., Leibel, R. L., & Jr., A. W. F. (2006) · Journal of Clinical Investigation · doi:10.1172/jci24335 · Cited by 1,497 · see citing works
Lehrke, M., & Lazar, M. A. (2005) · Cell · doi:10.1016/j.cell.2005.11.026 · Cited by 1,452 · see citing works
CCR2 modulates inflammatory and metabolic effects of high-fat feeding
Weisberg, S. P. (2006) · Journal of Clinical Investigation · doi:10.1172/jci24335c1 · Cited by 1,424 · see citing works
Mootha, V. K., Bunkenborg, J., Olsen, J. V., Hjerrild, M., Wisniewski, J. R., Stahl, E., Bolouri, M. S., Ray, H. N., Sihag, S., Kamal, M., et al. (2003) · Cell · doi:10.1016/s0092-8674(03)00926-7 · Cited by 889 · see citing works
Cinti, S. (2005) · Prostaglandins Leukotrienes and Essential Fatty Acids · doi:10.1016/j.plefa.2005.04.010 · Cited by 690 · see citing works
The mitochondrial uncoupling-protein homologues
Krauss, S., Zhang, C., & Lowell, B. B. (2005) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1592 · Cited by 663 · see citing works
Uldry, M., Yang, W., St‐Pierre, J., Lin, J. D., Seale, P., & Spiegelman, B. M. (2006) · Cell Metabolism · doi:10.1016/j.cmet.2006.04.002 · Cited by 644 · see citing works
Short, K. R., Vittone, J. L., Bigelow, M. L., Proctor, D. N., Rizza, R. A., Coenen-Schimke, J. M., & Nair, K. S. (2003) · Diabetes · doi:10.2337/diabetes.52.8.1888 · Cited by 631 · see citing works
Mitochondrial remodeling in adipose tissue associated with obesity and treatment with rosiglitazone.
Wilson-Fritch, L., Nicoloro, S., Chouinard, M., Lazar, M. A., Chui, P. C., Leszyk, J., Straubhaar, J., Czech, M. P., & Corvera, S. (2004) · Journal of Clinical Investigation · doi:10.1172/jci21752 · Cited by 616 · see citing works
The Biology of Mitochondrial Uncoupling Proteins
Rousset, S., Alves‐Guerra, M., Mozo, J., Miroux, B., Cassard, A., Bouillaud, F., & Ricquier, D. (2004) · Diabetes · doi:10.2337/diabetes.53.2007.s130 · Cited by 556 · see citing works
Kopecky, J., Clarke, G., Enerbäck, S., Spiegelman, B., & Kozak, L. P. (1995) · Journal of Clinical Investigation · doi:10.1172/jci118363 · Cited by 553 · see citing works
St‐Pierre, J., Lin, J. D., Krauss, S., Tarr, P. T., Yang, R., Newgard, C. B., & Spiegelman, B. M. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m301850200 · Cited by 543 · see citing works
Cidea-deficient mice have lean phenotype and are resistant to obesity
Zhou, Z., Toh, S. Y., Chen, Z., Guo, K., Ng, C. P., Ponniah, S., Lin, S., Hong, W., & Li, P. (2003) · Nature Genetics · doi:10.1038/ng1225 · Cited by 468 · see citing works
Pioglitazone Induces Mitochondrial Biogenesis in Human Subcutaneous Adipose Tissue In Vivo
Bogacka, I., Xie, H., Bray, G. A., & Smith, S. R. (2005) · Diabetes · doi:10.2337/diabetes.54.5.1392 · Cited by 467 · see citing works
The Mitochondrial Inner Membrane Protein Mitofilin Controls Cristae Morphology
John, G. B., Shang, Y., Li, L., Renken, C. W., Mannella, C. A., Selker, J. M. L., Rangell, L. K., Bennett, M. J., & Zha, J. (2005) · Molecular Biology of the Cell · doi:10.1091/mbc.e04-08-0697 · Cited by 459 · see citing works
Wilson-Fritch, L., Burkart, A., Bell, G., Mendelson, K., Leszyk, J., Nicoloro, S., Czech, M., & Corvera, S. (2003) · Molecular and Cellular Biology · doi:10.1128/mcb.23.3.1085-1094.2003 · Cited by 459 · see citing works
Olichon, A., Emorine, L. J., Descoins, E., Pelloquin, L., Brichese, L., Gas, N., Guillou, E., Delettre, C., Valette, A., Hamel, C., et al. (2002) · FEBS Letters · doi:10.1016/s0014-5793(02)02985-x · Cited by 430 · see citing works
Arany, Z., Lebrasseur, N., Morris, C., Smith, E., Yang, W., Ma, Y., Chin, S., & Spiegelman, B. M. (2007) · Cell Metabolism · doi:10.1016/j.cmet.2006.12.003 · Cited by 370 · see citing works
Mitochondria are impaired in the adipocytes of type 2 diabetic mice.
Choo, H.-J., Kim, J.-H., Kwon, O.-B., Lee, C. S., Mun, J. Y., Han, S. S., Yoon, Y.-S., Yoon, G., Choi, K.-M., & Ko, Y.-G. (2006) · Diabetologia · doi:10.1007/s00125-006-0170-2 · Cited by 365 · see citing works
Visapää, I., Fellman, V., Vesa, J., Dasvarma, A., Hutton, J., Kumar, V., Payne, G. S., Makarow, M., Coster, R. V., Taylor, R. W., et al. (2002) · The American Journal of Human Genetics · doi:10.1086/342773 · Cited by 300 · see citing works
Lelliott, C. J., Medina-Gomez, G., Petrovic, N., Kis, A., Feldmann, H. M., Bjursell, M., Parker, N., Curtis, K., Campbell, M., Hu, P., et al. (2006) · PLoS Biology · doi:10.1371/journal.pbio.0040369 · Cited by 280 · cited 1× · see citing works
“co-activators (PGC) 1α and 1β have been implicated as key regulators of mitochondrial biogenesis in adipose tissue (3,6,34-37) and muscle (11,36-40).”
BackgroundPowelka, A. M. (2005) · Journal of Clinical Investigation · doi:10.1172/jci26040 · Cited by 236 · see citing works
Rapid transformation of white adipocytes into fat-oxidizing machines
Orci, L., Cook, W. S., Ravazzola, M., Wang, M.-Y., Park, B.-H., Montesano, R., & Unger, R. H. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0308258100 · Cited by 234 · see citing works
MacLellan, J. D., Gerrits, M. F., Gowing, A., Smith, P. J. S., Wheeler, M. B., & Harper, M.-E. (2005) · Diabetes · doi:10.2337/diabetes.54.8.2343 · Cited by 213 · see citing works
Meirhaeghe, A., Crowley, V., Lenaghan, C., Lelliott, C. J., GREEN, K., Stewart, A., Kevin, H. A. R. T., Schinner, S., Sethi, J. K., Yeo, G. S. H., et al. (2003) · Biochemical Journal · doi:10.1042/bj20030200 · Cited by 210 · see citing works
Reversal of diet-induced obesity and diabetes in C57BL/6J mice
Parekh, P. I., Petro, A. E., Tiller, J. M., Feinglos, M. N., & Surwit, R. S. (1998) · Metabolism · doi:10.1016/s0026-0495(98)90283-9 · Cited by 197 · see citing works
Rosiglitazone Induces Mitochondrial Biogenesis in Mouse Brain
Strum, J. C., Shehee, R., Virley, D. J., Richardson, J. C., Mattie, M. D., Selley, P., Ghosh, S., Nock, C. M., Saunders, A. M., & Roses, A. D. (2007) · Journal of Alzheimer s Disease · doi:10.3233/jad-2007-11108 · Cited by 183 · see citing works
RIP140-Targeted Repression of Gene Expression in Adipocytes
Christian, M., Kiskinis, E., Debevec, D., Leonardsson, G., White, R., & Parker, M. G. (2005) · Molecular and Cellular Biology · doi:10.1128/mcb.25.21.9383-9391.2005 · Cited by 181 · see citing works
Bogacka, I., Ukropcova, B., McNeil, M., Gimble, J. M., & Smith, S. R. (2005) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2005-1024 · Cited by 138 · see citing works
Williams, S. L., Valnot, I., Rustin, P., & Taanman, J. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m309232200 · Cited by 133 · see citing works
β-Adrenergic Receptors and Regulation of Energy Expenditure: A Family Affair
Robidoux, J., Martin, T. L., & Collins, S. (2004) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev.pharmtox.44.101802.121659 · Cited by 130 · see citing works
BROWN, N. F., HILL, J. K., Esser, V., Kirkland, J. L., Corkey, B. E., Foster, D. W., & McGarry, J. (1997) · Biochemical Journal · doi:10.1042/bj3270225 · Cited by 112 · see citing works
Statistical Significance Threshold Criteria For Analysis of Microarray Gene Expression Data
Cheng, C., Pounds, S. B., Boyett, J. M., Pei, D., Kuo, M.-L., & Roussel, M. F. (2004) · Statistical Applications in Genetics and Molecular Biology · doi:10.2202/1544-6115.1064 · Cited by 47 · see citing works
Receptor-activated Smad localisation in Bleomycin-induced pulmonary fibrosis
Higashiyama, H., Yoshimoto, D., Okamoto, Y., Kikkawa, H., Asano, S., & Kinoshita, M. (2006) · Journal of Clinical Pathology · doi:10.1136/jcp.2006.037606 · Cited by 40 · see citing works
Effects of Alzheimer's peptide and α1-antichymotrypsin on astrocyte gene expression
Baker, C., Nielsen, H. M., Minthon, L., Wright, H. T., Chappell, S., Okyere, J., May, S. T., Morgan, K., Kalsheker, N. A., & Janciauskiene, S. M. (2005) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2005.10.017 · Cited by 11 · see citing works
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Brown and beige fat: Development, function and therapeutic potential
Harms, M., & Seale, P. (2013) · Nature Medicine · doi:10.1038/nm.3361 · Cited by 2,328 · see citing works
Bhatti, J. S., Bhatti, G. K., & Reddy, P. H. (2017) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2016.11.010 · Cited by 1,655 · see citing works
Petrovic, N., Walden, T. B., Shabalina, I. G., Timmons, J. A., Cannon, B., & Nedergaard, J. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.053942 · Cited by 1,263 · see citing works
PPARγ agonists Induce a White-to-Brown Fat Conversion through Stabilization of PRDM16 Protein
Ohno, H., Shinoda, K., Spiegelman, B. M., & Kajimura, S. (2012) · Cell Metabolism · doi:10.1016/j.cmet.2012.01.019 · Cited by 749 · see citing works
PGC-1 α , Inflammation, and Oxidative Stress: An Integrative View in Metabolism
Rius‐Pérez, S., Torres-Cuevas, I., Millán, I., Ortega, Á., & Pérez, S. (2020) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2020/1452696 · Cited by 648 · see citing works
Transcriptional Control of Mitochondrial Biogenesis and Function
Hock, M. B., & Kralli, A. (2009) · Annual Review of Physiology · doi:10.1146/annurev.physiol.010908.163119 · Cited by 616 · see citing works
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 · see citing works
Mitochondrial dysfunction in obesity
de Mello, A. H., Costa, A. B., Engel, J. D. G., & Rezin, G. T. (2018) · Life Sciences · doi:10.1016/j.lfs.2017.11.019 · Cited by 508 · see citing works
Resveratrol induces mitochondrial biogenesis in endothelial cells
Csiszár, A., Labinskyy, N., Pinto, J. T., Ballabh, P., Zhang, H., Losonczy, G., Pearson, K. J., de Cabo, R., Pacher, P., Zhang, C., et al. (2009) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00368.2009 · Cited by 450 · see citing works
Mitochondrial dysfunction in type 2 diabetes mellitus: an organ-based analysis
Pinti, M. V., Fink, G. K., Hathaway, Q. A., Durr, A. J., Kunovac, A., & Hollander, J. M. (2019) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00314.2018 · Cited by 432 · see citing works
Kajimura, S., & Saito, M. (2013) · Annual Review of Physiology · doi:10.1146/annurev-physiol-021113-170252 · Cited by 428 · see citing works
Villena, J. A. (2014) · FEBS Journal · doi:10.1111/febs.13175 · Cited by 404 · see citing works
Metabolic adaptation and maladaptation in adipose tissue
Chouchani, E. T., & Kajimura, S. (2019) · Nature Metabolism · doi:10.1038/s42255-018-0021-8 · Cited by 383 · see citing works
Impaired Mitochondrial Biogenesis in Adipose Tissue in Acquired Obesity
Heinonen, S., Buzkova, J., Muniandy, M., Kaksonen, R., Ollikainen, M., Ismail, K., Hakkarainen, A., Lundbom, J., Lundbom, N., Vuolteenaho, K., et al. (2015) · Diabetes · doi:10.2337/db14-1937 · Cited by 362 · see citing works
Contribution of Adipose Tissue Inflammation to the Development of Type 2 Diabetes Mellitus
Burhans, M. S., Hagman, D. K., Kuzma, J. N., Schmidt, K. A., & Kratz, M. (2018) · Comprehensive physiology · doi:10.1002/cphy.c170040 · Cited by 427 · see citing works
Bjørndal, B., Burri, L., Staalesen, V., Skorve, J., & Berge, R. K. (2011) · Journal of Obesity · doi:10.1155/2011/490650 · Cited by 372 · see citing works
Lu, Q., Zhu, Y., Deng, C., Liang, Z., Chen, J., Chen, Y., Wang, X., Liu, Y., Tian, Y., & Yang, Y. (2024) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-024-01756-w · Cited by 360 · see citing works
Transcriptional and epigenetic control of brown and beige adipose cell fate and function
Inagaki, T., Sakai, J., & Kajimura, S. (2016) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2016.62 · Cited by 341 · see citing works
Goossens, G. H., Bizzarri, A., Venteclef, N., Essers, Y., Cleutjens, J. P., Konings, E., Jocken, J. W. E., Čajlaković, M., Ribitsch, V., Clément, K., et al. (2011) · Circulation · doi:10.1161/circulationaha.111.027813 · Cited by 324 · see citing works
Pharmacological and nutritional agents promoting browning of white adipose tissue
Bonet, M. L., Oliver, P., & Palou, A. (2012) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2012.12.002 · Cited by 276 · see citing works
Lee, J. H., Park, A., Oh, K., Lee, S. C., Kim, W. K., & Bae, K. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20194924 · Cited by 270 · see citing works
Mitochondrial (Dys)function in Adipocyte (De)differentiation and Systemic Metabolic Alterations
Pauw, A. D., Tejerina, S., Raes, M. J., Keijer, J., & Arnould, T. (2009) · American Journal Of Pathology · doi:10.2353/ajpath.2009.081155 · Cited by 270 · see citing works
Vernochet, C., Mourier, A., Bezy, O., Macotela, Y., Boucher, J., Rardin, M. J., An, D., Lee, K. Y., Ilkayeva, O. R., Zingaretti, C. M., et al. (2012) · Cell Metabolism · doi:10.1016/j.cmet.2012.10.016 · Cited by 245 · see citing works
Obesity May Accelerate the Aging Process
Salvestrini, V., Sell, C., & Lorenzini, A. (2019) · Frontiers in Endocrinology · doi:10.3389/fendo.2019.00266 · Cited by 260 · see citing works
White adipose tissue mitochondrial metabolism in health and in obesity
Heinonen, S., Jokinen, R., Rissanen, A., & Pietiläinen, K. H. (2019) · Obesity Reviews · doi:10.1111/obr.12958 · Cited by 243 · see citing works
Obesity and aging: Molecular mechanisms and therapeutic approaches
Santos, A. L., & Sinha, S. (2021) · Ageing Research Reviews · doi:10.1016/j.arr.2021.101268 · Cited by 240 · see citing works
Adipose extracellular matrix remodelling in obesity and insulin resistance
Lin, D., Chun, T., & Kang, L. (2016) · Biochemical Pharmacology · doi:10.1016/j.bcp.2016.05.005 · Cited by 231 · see citing works
Pipatpiboon, N., Pratchayasakul, W., Chattipakorn, N., & Chattipakorn, S. C. (2011) · Endocrinology · doi:10.1210/en.2011-1502 · Cited by 213 · see citing works
Omega-3 fatty acids and adipose tissue function in obesity and metabolic syndrome
Martínez‐Fernández, L., Laiglesia, L. M., Huerta, A. E., Martínez, J. A., & Moreno-Aliaga, M. J. (2015) · Prostaglandins & Other Lipid Mediators · doi:10.1016/j.prostaglandins.2015.07.003 · Cited by 208 · see citing works
Exercise and adrenaline increase PGC‐1α mRNA expression in rat adipose tissue
Sutherland, L., Bomhof, M. R., Capozzi, L., Basaraba, S. A. U., & Wright, D. C. (2009) · The Journal of Physiology · doi:10.1113/jphysiol.2008.165464 · Cited by 201 · see citing works
Mitochondrial Biogenesis as a Pharmacological Target: A New Approach to Acute and Chronic Diseases
Whitaker, R. M., Corum, D. G., Beeson, C., & Schnellmann, R. G. (2015) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev-pharmtox-010715-103155 · Cited by 200 · see citing works
Uncoupling protein 1 expression and high-fat diets
Fromme, T., & Klingenspor, M. (2010) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00411.2010 · Cited by 200 · see citing works
The Impact of Oxidative Stress on Adipose Tissue Energy Balance
Masschelin, P. M., Cox, A. R., Chernis, N., & Hartig, S. M. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2019.01638 · Cited by 200 · see citing works
Vroegrijk, I. O. C. M., van Diepen, J. A., van den Berg, S. A. A., Westbroek, I., Keizer, H. G., Gambelli, L., Hontecillas, R., Bassaganya-Riera, J., Zondag, G. C. M., Romijn, J. A., et al. (2011) · Food and Chemical Toxicology · doi:10.1016/j.fct.2011.03.037 · Cited by 177 · see citing works
Mechanisms of human insulin resistance and thiazolidinedione-mediated insulin sensitization
Sears, D. D., Hsiao, G., Hsiao, A., Yu, J., Courtney, C. H., Ofrecio, J. M., Chapman, J., & Subramaniam, S. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0903032106 · Cited by 177 · see citing works
Trevellin, E., Scorzeto, M., Olivieri, M., Granzotto, M., Valerio, A., Tedesco, L., Fabris, R., Serra, R., Quarta, M., Reggiani, C., et al. (2014) · Diabetes · doi:10.2337/db13-1234 · Cited by 176 · see citing works
Metabolic remodeling of white adipose tissue in obesity
Cummins, T. D., Holden, C. R., Sansbury, B. E., Gibb, A., Shah, J., Zafar, N., Tang, Y., Hellmann, J. L., Rai, S. N., Spite, M. R., et al. (2014) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00271.2013 · Cited by 169 · see citing works
Role of obesity-associated dysfunctional adipose tissue in cancer: A molecular nutrition approach
Prieto-Hontoria, P. L., Pérez‐Matute, P., Fernández‐Galilea, M., Bustos, M., Martínez, J. A., & Moreno-Aliaga, M. J. (2010) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2010.11.004 · Cited by 165 · see citing works
Isolation and Differentiation of Stromal Vascular Cells to Beige/Brite Cells
Aune, U. L., Ruiz, L., & Kajimura, S. (2013) · Journal of Visualized Experiments · doi:10.3791/50191 · Cited by 161 · see citing works
Sansbury, B. E., Cummins, T. D., Tang, Y., Hellmann, J., Holden, C. R., Harbeson, M. A., Chen, Y., Patel, R. P., Spite, M., Bhatnagar, A., et al. (2012) · Circulation Research · doi:10.1161/circresaha.112.266395 · Cited by 156 · see citing works
Insulin Resistance and Mitochondrial Dysfunction
González-Franquesa, A., & Patti, M. (2017) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-55330-6_25 · Cited by 154 · see citing works
Adipose Tissue Dysfunction and Impaired Metabolic Health in Human Obesity: A Matter of Oxygen?
Goossens, G. H., & Blaak, E. E. (2015) · Frontiers in Endocrinology · doi:10.3389/fendo.2015.00055 · Cited by 147 · see citing works
Mitochondrial function/dysfunction in white adipose tissue
Boudina, S., & Graham, T. E. (2014) · Experimental Physiology · doi:10.1113/expphysiol.2014.081414 · Cited by 146 · see citing works
Transcriptional Regulatory Circuits Controlling Brown Fat Development and Activation
Seale, P. (2015) · Diabetes · doi:10.2337/db15-0203 · Cited by 143 · see citing works
Oxygenation of adipose tissue: A human perspective
Lempesis, I. G., van Meijel, R. L. J., Manolopoulos, K. N., & Goossens, G. H. (2019) · Acta Physiologica · doi:10.1111/apha.13298 · Cited by 138 · see citing works
Perrone, C. E., Mattocks, D. A. L., Jarvis-Morar, M., Plummer, J. D., & Orentreich, N. (2010) · Metabolism · doi:10.1016/j.metabol.2009.10.023 · Cited by 136 · see citing works
Crosstalk between mitochondrial (dys)function and mitochondrial abundance
Michel, S., Wanet, A., Pauw, A. D., Rommelaere, G., Arnould, T., & Renard, P. (2011) · Journal of Cellular Physiology · doi:10.1002/jcp.23021 · Cited by 132 · see citing works
Dietary polyphenols and their roles in fat browning
Silvester, A. J., Aseer, K. R., & Yun, J. W. (2018) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2018.09.028 · Cited by 131 · see citing works
Miglio, G., Rosa, A. C., Rattazzi, L., Collino, M., Lombardi, G., & Fantozzi, R. (2009) · Neurochemistry International · doi:10.1016/j.neuint.2009.05.001 · Cited by 131 · see citing works
Lipidomics as a Principal Tool for Advancing Biomedical Research
Lam, S. M., & Shui, G. (2013) · Journal of genetics and genomics/Journal of Genetics and Genomics · doi:10.1016/j.jgg.2013.06.007 · Cited by 128 · see citing works
Breast milk alkylglycerols sustain beige adipocytes through adipose tissue macrophages
Yu, H., Dilbaz, S., Coßmann, J., Hoang, A. C., Diedrich, V., Herwig, A., Harauma, A., Hoshi, Y., Moriguchi, T., Landgraf, K., et al. (2019) · Journal of Clinical Investigation · doi:10.1172/jci125646 · Cited by 123 · see citing works
Wang, L., Teng, R., Di, L., Rogers, H. M., Wu, H., Kopp, J. B., & Noguchi, C. T. (2013) · Diabetes · doi:10.2337/db13-0518 · Cited by 122 · see citing works
The role of mitochondria in the aetiology of insulin resistance and type 2 diabetes
Martin, S. D., & McGee, S. L. (2013) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2013.09.019 · Cited by 112 · see citing works
Cardiotrophin-1 Is a Key Regulator of Glucose and Lipid Metabolism
Moreno-Aliaga, M. J., Pérez-Echarri, N., Marcos‐Gómeź, B., Larequi, E., Gil-Bea, F. J., Viollet, B., Gimenez-Lopez, I., Martínez, J. A., Prìeto, J., & Bustos, M. (2011) · Cell Metabolism · doi:10.1016/j.cmet.2011.05.013 · Cited by 113 · see citing works
Adipose tissue in health and disease
Harvey, I. C., Boudreau, A., & Stephens, J. M. (2020) · Open Biology · doi:10.1098/rsob.200291 · Cited by 117 · see citing works
Mitochondrial stress: A bridge between mitochondrial dysfunction and metabolic diseases?
Hu, F., & Liu, F. (2011) · Cellular Signalling · doi:10.1016/j.cellsig.2011.05.008 · Cited by 112 · see citing works
The Mitochondrial Ca2+ Uptake and the Fine-Tuning of Aerobic Metabolism
Gherardi, G., Monticelli, H., Rizzuto, R., & Mammucari, C. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.554904 · Cited by 109 · see citing works
Jokinen, R., Pirnes-Karhu, S., Pietiläinen, K. H., & Pirinen, E. (2017) · Redox Biology · doi:10.1016/j.redox.2017.02.011 · Cited by 103 · see citing works
Deng, W.-J., Nie, S., Dai, J., Wu, J., & Zeng, R. (2009) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m900020-mcp200 · Cited by 101 · see citing works
Tripathi, M., Yen, P. M., & Singh, B. K. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21051645 · Cited by 98 · see citing works
Wei, D., Liao, L., Wang, H., Zhang, W., Wang, T., & Xu, Z. (2020) · Life Sciences · doi:10.1016/j.lfs.2020.117414 · Cited by 96 · see citing works
Ji, C., Chen, X., Gao, C., Jiao, L., Wang, J., Xu, G., Fu, H., Guo, X., & Zhao, Y. (2011) · Journal of Bioenergetics and Biomembranes · doi:10.1007/s10863-011-9361-8 · Cited by 99 · see citing works
Cavaliere, G., Cimmino, F., Trinchese, G., Catapano, A., Petrella, L., D’Angelo, M., Lucchin, L., & Mollica, M. P. (2023) · Antioxidants · doi:10.3390/antiox12061172 · Cited by 97 · see citing works
PPARγ and PPARα synergize to induce robust browning of white fat in vivo
Kroon, T., Harms, M. J., Maurer, S., Bonnet, L., Alexandersson, I., Lindblom, A., Ahnmark, A., Nilsson, D., Gennemark, P., O’Mahony, G., et al. (2020) · Molecular Metabolism · doi:10.1016/j.molmet.2020.02.007 · Cited by 90 · see citing works
Mitochondrial oxidative injury: a key player in nonalcoholic fatty liver disease
Dornas, W. C., & Schuppan, D. (2020) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00121.2020 · Cited by 90 · see citing works
Wan, X., Wen, J.-J., Koo, S.-J., Liang, L. Y., & Garg, N. J. (2016) · PLoS Pathogens · doi:10.1371/journal.ppat.1005954 · Cited by 87 · see citing works
Autophagy in adipose tissue biology
Zhang, Y., Zeng, X., & Jin, S. V. (2012) · Pharmacological Research · doi:10.1016/j.phrs.2012.09.004 · Cited by 87 · see citing works
MitoNEET-mediated effects on browning of white adipose tissue
Kusminski, C. M., Park, J., & Scherer, P. E. (2014) · Nature Communications · doi:10.1038/ncomms4962 · Cited by 84 · see citing works
Mitochondria and endocrine function of adipose tissue
Medina‐Gómez, G. (2012) · Best Practice & Research Clinical Endocrinology & Metabolism · doi:10.1016/j.beem.2012.06.002 · Cited by 86 · see citing works
Pardo, R., Enguix, N., Lasheras, J., Felíu, J. E., Kralli, A., & Villena, J. A. (2011) · PLoS ONE · doi:10.1371/journal.pone.0026989 · Cited by 85 · see citing works
Role of Mitochondrial Complex IV in Age-Dependent Obesity
Soro-Arnáiz, I., Li, Q. O. Y., Torres‐Capelli, M., Meléndez‐Rodríguez, F., Veiga, S. R., Veys, K., Sebastián, D., Elorza, A., Tello, D., Hernansanz‐Agustín, P., et al. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.08.041 · Cited by 83 · see citing works
Laiglesia, L. M., Lorente-Cebrián, S., Prieto-Hontoria, P. L., Fernández-Galilea, M., Ribeiro, S. M. R., Sáinz, N., Martínez, J. A., & Moreno-Aliaga, M. J. (2016) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2016.07.019 · Cited by 85 · see citing works
Mitochondrial function in vascular endothelial cell in diabetes
Pangare, M., & Makino, A. (2012) · Journal of Smooth Muscle Research · doi:10.1540/jsmr.48.1 · Cited by 83 · see citing works
Podocyte energy metabolism and glomerular diseases
Imasawa, T., & Rossignol, R. (2013) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2013.06.013 · Cited by 84 · see citing works
Adipocyte ALK7 links nutrient overload to catecholamine resistance in obesity
Guo, T., Mármol, P., Moliner, A., Björnholm, M., Zhang, C., Shokat, K. M., & Ibáñez, C. F. (2014) · eLife · doi:10.7554/elife.03245 · Cited by 81 · see citing works
Multi-tissue, selective PPARγ modulation of insulin sensitivity and metabolic pathways in obese rats
Hsiao, G., Chapman, J., Ofrecio, J. M., Wilkes, J. J., Resnik, J. L., Thapar, D., Subramaniam, S., & Sears, D. D. (2010) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00219.2010 · Cited by 80 · see citing works
Mitochondrial oxidative stress in obesity: role of the mineralocorticoid receptor
Lefranc, C., Friederich‐Persson, M., Palacios, R., & Cat, A. N. D. (2018) · Journal of Endocrinology · doi:10.1530/joe-18-0163 · Cited by 79 · see citing works
Schöttl, T., Kappler, L., Fromme, T., & Klingenspor, M. (2015) · Molecular Metabolism · doi:10.1016/j.molmet.2015.07.001 · Cited by 75 · see citing works
Moreno‐Navarrete, J. M., Ortega, F. J., Moreno, M., Ricart, W., & Fernández‐Real, J. M. (2014) · Diabetologia · doi:10.1007/s00125-014-3298-5 · Cited by 77 · see citing works
Melatonin promotes adipogenesis and mitochondrial biogenesis in 3T3‐L1 preadipocytes
Kato, H., Tanaka, G., Masuda, S., Ogasawara, J., Sakurai, T., Kizaki, T., Ohno, H., & Izawa, T. (2015) · Journal of Pineal Research · doi:10.1111/jpi.12259 · Cited by 72 · see citing works
Mitochondria as target of endocrine-disrupting chemicals: implications for type 2 diabetes
Marroquí, L., Tudurí, E., Alonso‐Magdalena, P., Quesada, I., Nadal, Á., & dos Santos, R. S. (2018) · Journal of Endocrinology · doi:10.1530/joe-18-0362 · Cited by 70 · see citing works
Shui, G., Stebbins, J. W., Lam, B. D., Cheong, W. F., Lam, S. M., Gregoire, F. M., Kusonoki, J., & Wenk, M. R. (2011) · PLoS ONE · doi:10.1371/journal.pone.0019731 · Cited by 68 · see citing works
Triacylglycerol lipases and metabolic control: implications for health and disease
Watt, M. J., & Spriet, L. L. (2010) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00698.2009 · Cited by 66 · see citing works
Mitochondrially-targeted treatment strategies
Bozi, L. H. M., Campos, J. C., Zambelli, V. O., Ferreira, N. D., & Ferreira, J. C. B. (2019) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2019.100836 · Cited by 65 · see citing works
Khalil, M., Shanmugam, H., Abdallah, H., JohnBritto, J. S., Galerati, I., Gómez‐Ambrosi, J., Frühbeck, G., & Portincasa, P. (2022) · Nutrients · doi:10.3390/nu14153112 · Cited by 66 · see citing works
Contribution of Adipose Tissue Inflammation to the Development of Type 2 Diabetes Mellitus
Burhans, M. S., Hagman, D. K., Kuzma, J. N., Schmidt, K. A., & Kratz, M. (2019) · Comprehensive physiology · doi:10.1002/j.2040-4603.2019.tb00055.x · Cited by 65 · see citing works
Maternal malnutrition programs pancreatic islet mitochondrial dysfunction in the adult offspring
Theys, N., Ahn, M., Bouckenooghe, T., Reusens, B., & Remacle, C. (2010) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2010.08.015 · Cited by 65 · see citing works
Mitochondrial bioenergetics is not impaired in nonobese subjects with type 2 diabetes mellitus
Chattopadhyay, M., GuhaThakurta, I., Behera, P., Ranjan, K. R., Khanna, M., Mukhopadhyay, S., & Chakrabarti, S. (2011) · Metabolism · doi:10.1016/j.metabol.2011.04.015 · Cited by 64 · see citing works
A nutritional perspective on UCP1-dependent thermogenesis
Bonet, M. L., Mercader, J., & Palou, A. (2017) · Biochimie · doi:10.1016/j.biochi.2016.12.014 · Cited by 66 · see citing works
Could very low-calorie ketogenic diets turn off low grade inflammation in obesity? Emerging evidence
Barrea, L., Caprio, M., Watanabe, M., Cammarata, G., Feraco, A., Muscogiuri, G., Verde, L., Colao, A., & Savastano, S. (2022) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2022.2054935 · Cited by 65 · see citing works
Shiota, A., Shimabukuro, M., Fukuda, D., Soeki, T., Sato, H., Uematsu, E., Hirata, Y., Kurobe, H., Maeda, N., Sakaue, H., et al. (2012) · Cardiovascular Diabetology · doi:10.1186/1475-2840-11-139 · Cited by 64 · see citing works
Influencing Factors of Thermogenic Adipose Tissue Activity
Zhang, G., Sun, Q., & Liu, C. (2016) · Frontiers in Physiology · doi:10.3389/fphys.2016.00029 · Cited by 67 · see citing works
Shen, W., Hao, J., Tian, C., Ren, J., Yang, L., Li, X., Luo, C., Cotma, C. W., & Liu, J. (2008) · PLoS ONE · doi:10.1371/journal.pone.0002328 · Cited by 63 · see citing works
Fernández‐Galilea, M., Pérez‐Matute, P., Prieto-Hontoria, P. L., Houssier, M., Burrell, M. A., Langin, D., Martínez, J. A., & Moreno-Aliaga, M. J. (2014) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2014.12.013 · Cited by 62 · see citing works
Prohibitin has an important role in adipocyte differentiation
Ande, S. R., Xu, Z., Gu, Y., & Mishra, S. (2011) · International Journal of Obesity · doi:10.1038/ijo.2011.227 · Cited by 62 · see citing works
Skeletal muscle and beyond: the role of exercise as a mediator of systemic mitochondrial biogenesis
Little, J. P., Safdar, A., Benton, C. R., & Wright, D. C. (2011) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/h11-076 · Cited by 62 · see citing works
Goossens, G. H., & Blaak, E. E. (2012) · Current Opinion in Clinical Nutrition & Metabolic Care · doi:10.1097/mco.0b013e328358fa87 · Cited by 62 · see citing works
Ryu, M. J., Kim, S. J., Kim, Y. K., Choi, M. J., Tadi, S., Lee, M. H., Lee, S. E., Chung, H. K., Jung, S. B., Kim, H. J., et al. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003356 · Cited by 61 · see citing works
PPARγ agonists delay age‐associated metabolic disease and extend longevity
Xu, L., Ma, X., Verma, N., Pèrié, L., Pendse, J., Shamloo, S., Josephson, A. M., Wang, D., Qiu, J., Guo, M., et al. (2020) · Aging Cell · doi:10.1111/acel.13267 · Cited by 63 · see citing works
Mäkelä, J., Tselykh, T. V., Kukkonen, J. P., Eriksson, O., Korhonen, L., & Lindholm, D. (2015) · Neuropharmacology · doi:10.1016/j.neuropharm.2015.11.020 · Cited by 60 · see citing works
- Authors
- Rong, J. X., Qiu, Y., Hansen, M. K., Zhu, L., Zhang, V., Xie, M., Okamoto, Y., Mattie, M. D., Higashiyama, H., Asano, S., Strum, J. C., & Ryan, T. E.
- Affiliations
- High Throughput Biology, Discovery Research, GlaxoSmithKline, Research Triangle Park, North Carolina
- GlaxoSmithKline (United States) (US)
- GlaxoSmithKline (Japan) (JP)
- Venue
- Diabetes
- Publisher
- American Diabetes Association
- Published
- 2007-07-01
- Volume
- 56
- Issue
- 7
- Pages
- 1751-1760
- ISSN
- 0012-1797 (ISSN-L)
- 1939-327X
- OpenAlex
- W2116872683
- Cited by
- 335
- References
- 48
- Citations by year
- 2026: 6 · 2025: 10 · 2024: 14 · 2023: 16 · 2022: 17 · 2021: 13 · 2020: 21 · 2019: 19 · 2018: 16 · 2017: 23 · 2016: 27 · 2015: 23 · 2014: 27 · 2013: 23 · 2012: 17
- FWCI
- 9.58
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Diabetes (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Physiology › Adipose Tissue and Metabolism
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Peroxisome Proliferator-Activated Receptors
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
- Keywords
- rosiglitazone, type 2 diabetes, obesity, db/db mice, high-fat diet, PPARγ agonists, PGC-1α, PGC-1β, mitochondrial gene expression, mitochondrial DNA, citrate synthase, reactive oxygen species, antioxidant enzymes, mitochondrial uncoupling, mitochondrial heat shock proteins
- MeSH terms
- Rosiglitazone, Adipose Tissue, Animals, Diabetes Mellitus, Type 2, Dietary Fats, Disease Models, Animal, Hypoglycemic Agents, Male, Mice, Inbred C57BL, Mitochondria, Obesity, Transcription, Genetic, Gene Expression, Gene Expression Profiling, Thiazolidinediones, PPAR gamma, Mice
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