{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,4]],"date-time":"2026-03-04T13:17:07Z","timestamp":1772630227108,"version":"3.50.1"},"reference-count":77,"publisher":"MDPI AG","issue":"23","license":[{"start":{"date-parts":[[2024,11,29]],"date-time":"2024-11-29T00:00:00Z","timestamp":1732838400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"National Institutes of Health","award":["HL102866"],"award-info":[{"award-number":["HL102866"]}]},{"name":"National Institutes of Health","award":["HL58144"],"award-info":[{"award-number":["HL58144"]}]},{"name":"National Institutes of Health","award":["DK114689"],"award-info":[{"award-number":["DK114689"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>A prenatal low-protein (LP) diet disrupts glucose homeostasis in adult offspring. Skeletal muscles are one of the main sites of glucose clearance, and mitochondria residing in the muscle fibers are central to glucose homeostasis. Our previous studies indicated that impaired mitochondrial health is central to dysregulated glucose metabolism in the gastrocnemius muscle of the LP-programmed female rats. In addition, dysfunctional mitochondria are often an indicator of underlying irregularities in energy metabolism and metabolic inflexibility. Therefore, this study examined the mitochondrial function and metabolic flexibility in the skeletal muscles of prenatal LP-programmed adult male rats. Pregnant Wistar rats were randomly allotted to a control diet (20% protein) or an isocaloric LP diet (6% protein). Standard laboratory rat chow was given to the dams and the pups after delivery and weaning. Gene and protein expressions, mtDNA copy number, and electron microscopy were assessed in gastrocnemius (GS) muscle, and the mitochondrial oxygen consumption rate was determined using isolated flexor digitorum brevis muscle fibers. The genes associated with mitochondrial outer membrane fusion, mitofusin1 and 2 (Mfn1 and Mfn2), fission (Fis1), and biogenesis (Pgc1B, Nrf1, and Esrra) were lower in the LP group. Further, our functional studies showed that the ATP-linked oxygen consumption rate (OCR), maximal, spare respiratory, and non-mitochondrial respiration-associated OCRs were lower in the LP rats. Further, the mRNA and protein expressions of Ndufb8, a key factor involved in the complex-I catalytic activity, were downregulated in the LP group. In addition, the expression of genes linked to mitochondrial pyruvate transport (Mpc1) and metabolism (Pdha1) was lower in the LP group. In contrast, the expression of mitochondrial fatty acid transporters (Cpt1a and Cpt2) was higher in the LP when compared to the control group. However, electron microscopic analysis exhibited no difference in the mitochondrial ultrastructure in the LP muscle compared to the control. Altogether, our results indicate that the LP diet affects the mitochondrial complex-I integrity and dynamics and leads to altered expression of genes associated with substrate oxidation and mitochondrial dysfunction in the skeletal muscle of the male LP offspring.<\/jats:p>","DOI":"10.3390\/ijms252312860","type":"journal-article","created":{"date-parts":[[2024,11,29]],"date-time":"2024-11-29T08:24:14Z","timestamp":1732868654000},"page":"12860","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":8,"title":["Maternal Low-Protein Diet Leads to Mitochondrial Dysfunction and Impaired Energy Metabolism in the Skeletal Muscle of Male Rats"],"prefix":"10.3390","volume":"25","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-1527-7753","authenticated-orcid":false,"given":"Vipin A.","family":"Vidyadharan","sequence":"first","affiliation":[{"name":"Basic Sciences Perinatology Research Laboratories, Department of Obstetrics and Gynecology, Baylor College of Medicine, Houston, TX 77030, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ancizar","family":"Betancourt","sequence":"additional","affiliation":[{"name":"Basic Sciences Perinatology Research Laboratories, Department of Obstetrics and Gynecology, Baylor College of Medicine, Houston, TX 77030, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Craig","family":"Smith","sequence":"additional","affiliation":[{"name":"Agilent Technologies Inc., Santa Clara, CA 95051, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0476-4457","authenticated-orcid":false,"given":"Chellakkan S.","family":"Blesson","sequence":"additional","affiliation":[{"name":"Reproductive Endocrinology and Infertility Division, Baylor College of Medicine, Houston, TX 77030, USA"},{"name":"Family Fertility Center, Texas Children\u2019s Hospital, Houston, TX 77030, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4873-8314","authenticated-orcid":false,"given":"Chandra","family":"Yallampalli","sequence":"additional","affiliation":[{"name":"Basic Sciences Perinatology Research Laboratories, Department of Obstetrics and Gynecology, Baylor College of Medicine, Houston, TX 77030, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2024,11,29]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1474","DOI":"10.1136\/bmj.303.6809.1019","article-title":"Fetal and infant growth and impaired glucose tolerance","volume":"303","author":"Hales","year":"1991","journal-title":"BMJ"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1447","DOI":"10.1152\/physrev.00031.2010","article-title":"Fiber types in mammalian skeletal muscles","volume":"91","author":"Schiaffino","year":"2011","journal-title":"Physiol. Rev."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"195","DOI":"10.1016\/S0079-6107(00)00006-7","article-title":"Human skeletal muscle fibres: Molecular and functional diversity","volume":"73","author":"Bottinelli","year":"2000","journal-title":"Prog. Biophys. Mol. Biol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"265","DOI":"10.1146\/annurev-genet-110410-132529","article-title":"Fusion and fission: Interlinked processes critical for mitochondrial health","volume":"46","author":"Chan","year":"2012","journal-title":"Annu. Rev. Genet."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"243","DOI":"10.1038\/s41574-021-00626-7","article-title":"Mitochondrial and metabolic dysfunction in ageing and age-related diseases","volume":"18","author":"Amorim","year":"2022","journal-title":"Nat. Rev. Endocrinol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"489","DOI":"10.1210\/er.2017-00211","article-title":"Metabolic Flexibility as an Adaptation to Energy Resources and Requirements in Health and Disease","volume":"39","author":"Smith","year":"2018","journal-title":"Endocr. Rev."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1184","DOI":"10.1002\/1873-3468.14077","article-title":"Mitochondrial dynamics in health and disease","volume":"595","author":"Yapa","year":"2021","journal-title":"FEBS Lett."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"4892","DOI":"10.1111\/jcmm.15194","article-title":"Mitochondrial biogenesis: An update","volume":"24","author":"Popov","year":"2020","journal-title":"J. Cell Mol. Med."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1038\/nature19754","article-title":"Accessory subunits are integral for assembly and function of human mitochondrial complex I","volume":"538","author":"Stroud","year":"2016","journal-title":"Nature"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1062","DOI":"10.1002\/1873-3468.13995","article-title":"Mitochondrial disorders of the OXPHOS system","volume":"595","author":"Zeviani","year":"2021","journal-title":"FEBS Lett."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"580","DOI":"10.1002\/emmm.201303782","article-title":"Mitochondrial response to nutrient availability and its role in metabolic disease","volume":"6","author":"Gao","year":"2014","journal-title":"EMBO Mol. Med."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1376","DOI":"10.2337\/db06-0783","article-title":"Impaired mitochondrial substrate oxidation in muscle of insulin-resistant offspring of type 2 diabetic patients","volume":"56","author":"Befroy","year":"2007","journal-title":"Diabetes"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"2042018819888824","DOI":"10.1177\/2042018819888824","article-title":"Reduced physical activity in young and older adults: Metabolic and musculoskeletal implications","volume":"10","author":"Pickles","year":"2019","journal-title":"Ther. Adv. Endocrinol. Metab."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1016\/S2213-8587(17)30186-9","article-title":"Type 2 diabetes in adolescents and young adults","volume":"6","author":"Lascar","year":"2018","journal-title":"Lancet Diabetes Endocrinol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"2419","DOI":"10.1056\/NEJM200406033502320","article-title":"Impaired mitochondrial activity and insulin-resistant offspring of patients with type 2 diabetes","volume":"350","author":"Mohlig","year":"2004","journal-title":"N. Engl. J. Med."},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Schoenmann, N., Tannenbaum, N., Hodgeman, R.M., and Raju, R.P. (2023). Regulating mitochondrial metabolism by targeting pyruvate dehydrogenase with dichloroacetate, a metabolic messenger. Biochim. Biophys. Acta Mol. Basis Dis., 1869.","DOI":"10.1016\/j.bbadis.2023.166769"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1016\/j.ceb.2014.10.008","article-title":"Mitochondrial pyruvate import and its effects on homeostasis","volume":"33","author":"Vanderperre","year":"2015","journal-title":"Curr. Opin. Cell Biol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"RP86944","DOI":"10.7554\/eLife.86944","article-title":"Loss of Ptpmt1 limits mitochondrial utilization of carbohydrates and leads to muscle atrophy and heart failure in tissue-specific knockout mice","volume":"12","author":"Zheng","year":"2023","journal-title":"Elife"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"2422","DOI":"10.1016\/j.bbamcr.2016.01.023","article-title":"Carnitine transport and fatty acid oxidation","volume":"1863","author":"Longo","year":"2016","journal-title":"Biochim. Biophys. Acta"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"409","DOI":"10.1017\/S2040174418000132","article-title":"Maternal low-quality protein diet exerts sex-specific effects on plasma amino acid profile and alters hepatic expression of methyltransferases in adult rat offspring","volume":"9","author":"Akyol","year":"2018","journal-title":"J. Dev. Orig. Health Dis."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"62","DOI":"10.1007\/s12020-018-1719-9","article-title":"Maternal low-protein diet during lactation combined with early overfeeding impair male offspring\u2019s long-term glucose homeostasis","volume":"63","author":"Almeida","year":"2019","journal-title":"Endocrine"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"592","DOI":"10.1017\/S0007114521003639","article-title":"A maternal low-protein diet during gestation induces hepatic autophagy-related gene expression in a sex-specific manner in Sprague-Dawley rats","volume":"128","author":"Cai","year":"2022","journal-title":"Br. J. Nutr."},{"key":"ref_23","first-page":"299","article-title":"Maternal low-protein diet programmes low ovarian reserve in offspring","volume":"156","author":"Winship","year":"2018","journal-title":"Reproduction"},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Zheng, J., Xiao, X., Zhang, Q., Wang, T., Yu, M., and Xu, J. (2017). Maternal Low-Protein Diet Modulates Glucose Metabolism and Hepatic MicroRNAs Expression in the Early Life of Offspring dagger. Nutrients, 9.","DOI":"10.3390\/nu9030205"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"218","DOI":"10.12688\/wellcomeopenres.17124.1","article-title":"Quantification of fetal organ sparing in maternal low-protein dietary models","volume":"6","author":"Serpente","year":"2021","journal-title":"Wellcome Open Res."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"540.e1","DOI":"10.1016\/j.ajog.2016.02.004","article-title":"Novel lean type 2 diabetic rat model using gestational low-protein programming","volume":"214","author":"Blesson","year":"2016","journal-title":"Am. J. Obstet. Gynecol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"756","DOI":"10.1210\/en.2016-1675","article-title":"Gestational Protein Restriction Impairs Glucose Disposal in the Gastrocnemius Muscles of Female Rats","volume":"158","author":"Blesson","year":"2017","journal-title":"Endocrinology"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"3036","DOI":"10.1210\/en.2014-1094","article-title":"Gestational protein restriction impairs insulin-regulated glucose transport mechanisms in gastrocnemius muscles of adult male offspring","volume":"155","author":"Blesson","year":"2014","journal-title":"Endocrinology"},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Vidyadharan, V.A., Betancourt, A., Smith, C., Yallampalli, C., and Blesson, C.S. (2022). Prenatal Low-Protein Diet Affects Mitochondrial Structure and Function in the Skeletal Muscle of Adult Female Offspring. Nutrients, 14.","DOI":"10.3390\/nu14061158"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"185","DOI":"10.4239\/wjd.v13.i3.185","article-title":"Maternal low protein diet and fetal programming of lean type 2 diabetes","volume":"13","author":"Vipin","year":"2022","journal-title":"World J. Diabetes"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"204","DOI":"10.1038\/s41580-020-0210-7","article-title":"The cell biology of mitochondrial membrane dynamics","volume":"21","author":"Giacomello","year":"2020","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"e21620","DOI":"10.1096\/fj.202100067R","article-title":"Mitochondrial fusion and fission: The fine-tune balance for cellular homeostasis","volume":"35","author":"Adebayo","year":"2021","journal-title":"FASEB J."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"341","DOI":"10.1042\/EBC20170104","article-title":"Mitochondrial dynamics: Overview of molecular mechanisms","volume":"62","author":"Tilokani","year":"2018","journal-title":"Essays Biochem."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"424","DOI":"10.1007\/s00125-020-05335-w","article-title":"Human skeletal muscle mitochondrial dynamics in relation to oxidative capacity and insulin sensitivity","volume":"64","author":"Houzelle","year":"2021","journal-title":"Diabetologia"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"17190","DOI":"10.1074\/jbc.M212754200","article-title":"Mitofusin-2 determines mitochondrial network architecture and mitochondrial metabolism. A novel regulatory mechanism altered in obesity","volume":"278","author":"Bach","year":"2003","journal-title":"J. Biol. Chem."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1016\/j.trsl.2018.07.011","article-title":"Mitochondrial dynamics in skeletal muscle insulin resistance and type 2 diabetes","volume":"202","author":"Fealy","year":"2018","journal-title":"Transl. Res."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"645","DOI":"10.2337\/dc09-1305","article-title":"Subjects with early-onset type 2 diabetes show defective activation of the skeletal muscle PGC-1{alpha}\/Mitofusin-2 regulatory pathway in response to physical activity","volume":"33","author":"Thabit","year":"2010","journal-title":"Diabetes Care"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"444","DOI":"10.1016\/j.tem.2012.05.007","article-title":"Muscle mitochondria and insulin resistance: A human perspective","volume":"23","author":"Hoeks","year":"2012","journal-title":"Trends Endocrinol. Metab."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"205","DOI":"10.3892\/mmr.2013.1457","article-title":"Overexpression of mitofusin 2 improves translocation of glucose transporter 4 in skeletal muscle of highfat dietfed rats through AMPactivated protein kinase signaling","volume":"8","author":"Kong","year":"2013","journal-title":"Mol. Med. Rep."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"e99748","DOI":"10.15252\/embj.201899748","article-title":"Human Fis1 regulates mitochondrial dynamics through inhibition of the fusion machinery","volume":"38","author":"Yu","year":"2019","journal-title":"EMBO J."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"710","DOI":"10.1016\/j.tem.2022.07.003","article-title":"OPA1 regulation of mitochondrial dynamics in skeletal and cardiac muscle","volume":"33","author":"Noone","year":"2022","journal-title":"Trends Endocrinol. Metab."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"1269","DOI":"10.1016\/j.bbamcr.2010.09.019","article-title":"Metabolic control of mitochondrial biogenesis through the PGC-1 family regulatory network","volume":"1813","author":"Scarpulla","year":"2011","journal-title":"Biochim. Biophys. Acta"},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"Ikeda, M., Ide, T., Fujino, T., Arai, S., Saku, K., Kakino, T., Tyynismaa, H., Yamasaki, T., Yamada, K.-I., and Kang, D. (2015). Overexpression of TFAM or twinkle increases mtDNA copy number and facilitates cardioprotection associated with limited mitochondrial oxidative stress. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0119687"},{"key":"ref_44","doi-asserted-by":"crossref","unstructured":"Otten, A.B.C., Kamps, R., Lindsey, P., Gerards, M., Pendeville-Samain, H., Muller, M., van Tienen, F.H.J., and Smeets, H.J.M. (2020). Tfam Knockdown Results in Reduction of mtDNA Copy Number, OXPHOS Deficiency and Abnormalities in Zebrafish Embryos. Front. Cell Dev. Biol., 8.","DOI":"10.3389\/fcell.2020.00381"},{"key":"ref_45","doi-asserted-by":"crossref","unstructured":"Knorre, D.A. (2020). Intracellular quality control of mitochondrial DNA: Evidence and limitations. Philos. Trans. R. Soc. Lond. B Biol. Sci., 375.","DOI":"10.1098\/rstb.2019.0176"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"425","DOI":"10.1042\/bj3480425","article-title":"Increase of mitochondria and mitochondrial DNA in response to oxidative stress in human cells","volume":"348","author":"Lee","year":"2000","journal-title":"Biochem. J."},{"key":"ref_47","doi-asserted-by":"crossref","unstructured":"Van Huynh, T., Rethi, L., Rethi, L., Chen, C.H., Chen, Y.J., and Kao, Y.H. (2023). The Complex Interplay between Imbalanced Mitochondrial Dynamics and Metabolic Disorders in Type 2 Diabetes. Cells, 12.","DOI":"10.3390\/cells12091223"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1016\/j.molmet.2018.11.012","article-title":"The impact of exercise on mitochondrial dynamics and the role of Drp1 in exercise performance and training adaptations in skeletal muscle","volume":"21","author":"Moore","year":"2019","journal-title":"Mol. Metab."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"267","DOI":"10.1038\/ng1180","article-title":"PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes","volume":"34","author":"Mootha","year":"2003","journal-title":"Nat. Genet."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"491","DOI":"10.1016\/j.cmet.2013.03.002","article-title":"Mitochondrial dynamics in the regulation of nutrient utilization and energy expenditure","volume":"17","author":"Liesa","year":"2013","journal-title":"Cell Metab."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"803","DOI":"10.1038\/ncb3376","article-title":"PTP1B controls non-mitochondrial oxygen consumption by regulating RNF213 to promote tumour survival during hypoxia","volume":"18","author":"Banh","year":"2016","journal-title":"Nat. Cell Biol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"1592","DOI":"10.2337\/db06-0981","article-title":"Mitochondrial respiration is decreased in skeletal muscle of patients with type 2 diabetes","volume":"56","author":"Mogensen","year":"2007","journal-title":"Diabetes"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"2943","DOI":"10.2337\/db08-0391","article-title":"Lower intrinsic ADP-stimulated mitochondrial respiration underlies in vivo mitochondrial dysfunction in muscle of male type 2 diabetic patients","volume":"57","author":"Phielix","year":"2008","journal-title":"Diabetes"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"2142","DOI":"10.2337\/db07-0141","article-title":"Effects of physical activity and weight loss on skeletal muscle mitochondria and relationship with glucose control in type 2 diabetes","volume":"56","author":"Toledo","year":"2007","journal-title":"Diabetes"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"976","DOI":"10.1002\/1873-3468.14021","article-title":"Mitochondrial DNA copy number in human disease: The more the better?","volume":"595","author":"Filograna","year":"2021","journal-title":"FEBS Lett."},{"key":"ref_56","doi-asserted-by":"crossref","unstructured":"Blesson, C.S., Schutt, A., Chacko, S., Marini, J.C., Mathew, P.R., Tanchico, D., Balakrishnan, M., and Yallampalli, C. (2019). Sex Dependent Dysregulation of Hepatic Glucose Production in Lean Type 2 Diabetic Rats. Front. Endocrinol., 10.","DOI":"10.3389\/fendo.2019.00538"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"833","DOI":"10.1093\/brain\/awp058","article-title":"Mitochondrial complex I deficiency: From organelle dysfunction to clinical disease","volume":"132","author":"Distelmaier","year":"2009","journal-title":"Brain"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"443","DOI":"10.1016\/j.bbadis.2010.02.001","article-title":"Mitochondrial bioenergetics and dynamics interplay in complex I-deficient fibroblasts","volume":"1802","author":"Moran","year":"2010","journal-title":"Biochim. Biophys. Acta"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"6187","DOI":"10.1113\/jphysiol.2012.240077","article-title":"Impaired mitochondrial respiration and decreased fatigue resistance followed by severe muscle weakness in skeletal muscle of mitochondrial DNA mutator mice","volume":"590","author":"Yamada","year":"2012","journal-title":"J. Physiol."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"1423","DOI":"10.1016\/j.freeradbiomed.2007.07.027","article-title":"Age-related increases in oxidatively damaged proteins of mouse kidney mitochondrial electron transport chain complexes","volume":"43","author":"Choksi","year":"2007","journal-title":"Free Radic. Biol. Med."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"826","DOI":"10.1016\/j.freeradbiomed.2008.06.006","article-title":"Age-related alterations in oxidatively damaged proteins of mouse skeletal muscle mitochondrial electron transport chain complexes","volume":"45","author":"Choksi","year":"2008","journal-title":"Free Radic. Biol. Med."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"E49","DOI":"10.1152\/ajpendo.00317.2009","article-title":"Deficiency of electron transport chain in human skeletal muscle mitochondria in type 2 diabetes mellitus and obesity","volume":"298","author":"Ritov","year":"2010","journal-title":"Am. J. Physiol. Endocrinol. Metab."},{"key":"ref_63","doi-asserted-by":"crossref","unstructured":"Vidyadharan, V.A., Blesson, C.S., Tanchico, D., Betancourt, A., Smith, C., and Yallampalli, C. (2023). Low Protein Programming Causes Increased Mitochondrial Fusion and Decreased Oxygen Consumption in the Hepatocytes of Female Rats. Nutrients, 15.","DOI":"10.3390\/nu15071568"},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"S38","DOI":"10.1186\/1423-0127-17-S1-S38","article-title":"A maternal low protein diet has pronounced effects on mitochondrial gene expression in offspring liver and skeletal muscle; protective effect of taurine","volume":"17","author":"Mortensen","year":"2010","journal-title":"J. Biomed. Sci."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"2861","DOI":"10.1007\/s00125-015-3772-8","article-title":"Impaired mitochondrial oxidative phosphorylation and supercomplex assembly in rectus abdominis muscle of diabetic obese individuals","volume":"58","author":"Antoun","year":"2015","journal-title":"Diabetologia"},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/S1388-1981(00)00044-5","article-title":"Fatty acid import into mitochondria","volume":"1486","author":"Kerner","year":"2000","journal-title":"Biochim. Biophys. Acta"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"e111901","DOI":"10.15252\/embj.2022111901","article-title":"Mitochondrial morphology controls fatty acid utilization by changing CPT1 sensitivity to malonyl-CoA","volume":"42","author":"Ngo","year":"2023","journal-title":"EMBO J."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"E33","DOI":"10.1152\/ajpendo.00074.2022","article-title":"The mitochondrial pyruvate carrier at the crossroads of intermediary metabolism","volume":"323","author":"Yiew","year":"2022","journal-title":"Am. J. Physiol. Endocrinol. Metab."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"259","DOI":"10.14348\/molcells.2023.2128","article-title":"The Role of Pyruvate Metabolism in Mitochondrial Quality Control and Inflammation","volume":"46","author":"Kim","year":"2023","journal-title":"Mol. Cells"},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"108767","DOI":"10.1016\/j.celrep.2021.108767","article-title":"PDK4 dictates metabolic resistance to ferroptosis by suppressing pyruvate oxidation and fatty acid synthesis","volume":"34","author":"Song","year":"2021","journal-title":"Cell Rep."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"E855","DOI":"10.1152\/ajpendo.00526.2002","article-title":"Recent advances in mechanisms regulating glucose oxidation at the level of the pyruvate dehydrogenase complex by PDKs","volume":"284","author":"Sugden","year":"2003","journal-title":"Am. J. Physiol. Endocrinol. Metab."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"383","DOI":"10.2337\/diab.39.3.383","article-title":"Operation of Randle\u2019s cycle in patients with NIDDM","volume":"39","author":"Bevilacqua","year":"1990","journal-title":"Diabetes"},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"1253","DOI":"10.1016\/j.cell.2014.11.034","article-title":"Metabolic inflexibility: When mitochondrial indecision leads to metabolic gridlock","volume":"159","author":"Muoio","year":"2014","journal-title":"Cell"},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"261","DOI":"10.1530\/EC-19-0553","article-title":"Prenatal androgen induced lean PCOS impairs mitochondria and mRNA profiles in oocytes","volume":"9","author":"Chappell","year":"2020","journal-title":"Endocr. Connect."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"402","DOI":"10.1006\/meth.2001.1262","article-title":"Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method","volume":"25","author":"Livak","year":"2001","journal-title":"Methods"},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"R712","DOI":"10.1152\/ajpregu.00229.2011","article-title":"Measuring mitochondrial respiration in intact single muscle fibers","volume":"302","author":"Schuh","year":"2012","journal-title":"Am. J. Physiol. Regul. Integr. Comp. Physiol."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"1110","DOI":"10.1093\/biolre\/ioaa133","article-title":"In utero low-protein-diet-programmed type 2 diabetes in adult offspring is mediated by sex hormones in ratsdagger","volume":"103","author":"Blesson","year":"2020","journal-title":"Biol. Reprod."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/25\/23\/12860\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T16:42:36Z","timestamp":1760114556000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/25\/23\/12860"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,11,29]]},"references-count":77,"journal-issue":{"issue":"23","published-online":{"date-parts":[[2024,12]]}},"alternative-id":["ijms252312860"],"URL":"https:\/\/doi.org\/10.3390\/ijms252312860","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,11,29]]}}}