{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,12]],"date-time":"2026-03-12T04:07:20Z","timestamp":1773288440858,"version":"3.50.1"},"reference-count":98,"publisher":"Portland Press Ltd.","issue":"9","license":[{"start":{"date-parts":[[2021,4,26]],"date-time":"2021-04-26T00:00:00Z","timestamp":1619395200000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/2.0\/"}],"content-domain":{"domain":["portlandpress.com"],"crossmark-restriction":true},"short-container-title":[],"published-print":{"date-parts":[[2021,5,14]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>Poor maternal nutrition in pregnancy affects fetal development, predisposing offspring to cardiometabolic diseases. The role of mitochondria during fetal development on later-life cardiac dysfunction caused by maternal nutrient reduction (MNR) remains unexplored.<\/jats:p>\n               <jats:p>We hypothesized that MNR during gestation causes fetal cardiac bioenergetic deficits, compromising cardiac mitochondrial metabolism and reserve capacity.<\/jats:p>\n               <jats:p>To enable human translation, we developed a primate baboon model (Papio spp.) of moderate MNR in which mothers receive 70% of control nutrition during pregnancy, resulting in intrauterine growth restriction (IUGR) offspring and later exhibiting myocardial remodeling and heart failure at human equivalent \u223c25 years. Term control and MNR baboon offspring were necropsied following cesarean-section, and left ventricle (LV) samples were collected. MNR adversely impacted fetal cardiac LV mitochondria in a sex-dependent fashion. Increased maternal plasma aspartate aminotransferase, creatine phosphokinase (CPK), and elevated cortisol levels in MNR concomitant with decreased blood insulin in male fetal MNR were measured. MNR resulted in a two-fold increase in fetal LV mitochondrial DNA (mtDNA). MNR resulted in increased transcripts for several respiratory chain (NDUFB8, UQCRC1, and cytochrome c) and adenosine triphosphate (ATP) synthase proteins. However, MNR fetal LV mitochondrial complex I and complex II\/III activities were significantly decreased, possibly contributing to the 73% decreased ATP content and increased lipid peroxidation. MNR fetal LV showed mitochondria with sparse and disarranged cristae dysmorphology.<\/jats:p>\n               <jats:p>Conclusion: MNR disruption of fetal cardiac mitochondrial fitness likely contributes to the documented developmental programming of adult cardiac dysfunction, indicating a programmed mitochondrial inability to deliver sufficient energy to cardiac tissues as a chronic mechanism for later-life heart failure.<\/jats:p>","DOI":"10.1042\/cs20201339","type":"journal-article","created":{"date-parts":[[2021,4,26]],"date-time":"2021-04-26T09:07:52Z","timestamp":1619428072000},"page":"1103-1126","update-policy":"https:\/\/doi.org\/10.1042\/crossmark_policy","source":"Crossref","is-referenced-by-count":26,"title":["Sex-dependent vulnerability of fetal nonhuman primate cardiac mitochondria to moderate maternal nutrient reduction"],"prefix":"10.1042","volume":"135","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-1168-2444","authenticated-orcid":false,"given":"Susana\u00a0P.","family":"Pereira","sequence":"first","affiliation":[{"name":"CNC-Center for Neuroscience and Cell Biology, CIBB - Centre for Innovative Biomedicine and Biotechnology, IIIUC - Institute for Interdisciplinary Research, University of Coimbra, Coimbra 3004-504, Portugal"},{"name":"University of Coimbra, Department of Life Sciences, Coimbra 3000-456, Portugal"},{"name":"Center for Pregnancy and Newborn Research, University of Texas Health Science Center at San Antonio, San Antonio 78229-3900, TX, U.S.A."}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2324-1259","authenticated-orcid":false,"given":"Ludgero\u00a0C.","family":"Tavares","sequence":"additional","affiliation":[{"name":"CNC-Center for Neuroscience and Cell Biology, CIBB - Centre for Innovative Biomedicine and Biotechnology, IIIUC - Institute for Interdisciplinary Research, University of Coimbra, Coimbra 3004-504, Portugal"},{"name":"University of Coimbra, Department of Life Sciences, Coimbra 3000-456, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0223-7867","authenticated-orcid":false,"given":"Ana\u00a0I.","family":"Duarte","sequence":"additional","affiliation":[{"name":"CNC-Center for Neuroscience and Cell Biology, CIBB - Centre for Innovative Biomedicine and Biotechnology, IIIUC - Institute for Interdisciplinary Research, University of Coimbra, Coimbra 3004-504, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8106-7308","authenticated-orcid":false,"given":"In\u00eas","family":"Baldeiras","sequence":"additional","affiliation":[{"name":"CNC-Center for Neuroscience and Cell Biology, CIBB - Centre for Innovative Biomedicine and Biotechnology, IIIUC - Institute for Interdisciplinary Research, University of Coimbra, Coimbra 3004-504, Portugal"},{"name":"Neurological Clinic, Faculty of Medicine, University of Coimbra, Coimbra 3000-354, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7382-0339","authenticated-orcid":false,"given":"Teresa","family":"Cunha-Oliveira","sequence":"additional","affiliation":[{"name":"CNC-Center for Neuroscience and Cell Biology, CIBB - Centre for Innovative Biomedicine and Biotechnology, IIIUC - Institute for Interdisciplinary Research, University of Coimbra, Coimbra 3004-504, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3676-3053","authenticated-orcid":false,"given":"Jo\u00e3o\u00a0D.","family":"Martins","sequence":"additional","affiliation":[{"name":"CNC-Center for Neuroscience and Cell Biology, CIBB - Centre for Innovative Biomedicine and Biotechnology, IIIUC - Institute for Interdisciplinary Research, University of Coimbra, Coimbra 3004-504, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6881-9392","authenticated-orcid":false,"given":"Maria\u00a0S.","family":"Santos","sequence":"additional","affiliation":[{"name":"CNC-Center for Neuroscience and Cell Biology, CIBB - Centre for Innovative Biomedicine and Biotechnology, IIIUC - Institute for Interdisciplinary Research, University of Coimbra, Coimbra 3004-504, Portugal"},{"name":"University of Coimbra, Department of Life Sciences, Coimbra 3000-456, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7309-5026","authenticated-orcid":false,"given":"Alina","family":"Maloyan","sequence":"additional","affiliation":[{"name":"Center for Pregnancy and Newborn Research, University of Texas Health Science Center at San Antonio, San Antonio 78229-3900, TX, U.S.A."}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3575-7604","authenticated-orcid":false,"given":"Ant\u00f3nio\u00a0J.","family":"Moreno","sequence":"additional","affiliation":[{"name":"University of Coimbra, Department of Life Sciences, Coimbra 3000-456, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8836-3783","authenticated-orcid":false,"given":"Laura\u00a0A.","family":"Cox","sequence":"additional","affiliation":[{"name":"Department of Genetics, Texas Biomedical Research Institute, San Antonio 78245-0549, TX, U.S.A."}]},{"given":"Cun","family":"Li","sequence":"additional","affiliation":[{"name":"Wyoming Pregnancy and Life Course Health Center, University of Wyoming, Laramie 82071-3684, WY, U.S.A."}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8410-6280","authenticated-orcid":false,"given":"Peter\u00a0W.","family":"Nathanielsz","sequence":"additional","affiliation":[{"name":"Wyoming Pregnancy and Life Course Health Center, University of Wyoming, Laramie 82071-3684, WY, U.S.A."}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0998-8804","authenticated-orcid":false,"given":"Mark\u00a0J.","family":"Nijland","sequence":"additional","affiliation":[{"name":"Center for Pregnancy and Newborn Research, University of Texas Health Science Center at San Antonio, San Antonio 78229-3900, TX, U.S.A."}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5201-9948","authenticated-orcid":false,"given":"Paulo\u00a0J.","family":"Oliveira","sequence":"additional","affiliation":[{"name":"CNC-Center for Neuroscience and Cell Biology, CIBB - Centre for Innovative Biomedicine and Biotechnology, IIIUC - Institute for Interdisciplinary Research, University of Coimbra, Coimbra 3004-504, Portugal"}]}],"member":"288","published-online":{"date-parts":[[2021,5,11]]},"reference":[{"key":"2021113011210172700_B1","article-title":"Noncommunicable diseases","author":"WHO","year":"2018"},{"key":"2021113011210172700_B2","doi-asserted-by":"publisher","first-page":"366","DOI":"10.1017\/S2040174415001300","article-title":"The programming of cardiovascular disease","volume":"6","author":"Thornburg","year":"2015","journal-title":"J. Dev. Orig. Health Dis."},{"key":"2021113011210172700_B3","doi-asserted-by":"publisher","first-page":"537","DOI":"10.1038\/s41390-018-0069-x","article-title":"The lifelong impact of fetal growth restriction on cardiac development","volume":"84","author":"Masoumy","year":"2018","journal-title":"Pediatr. Res."},{"key":"2021113011210172700_B4","doi-asserted-by":"publisher","first-page":"396","DOI":"10.1136\/bmj.315.7105.396","article-title":"Birth weight and risk of cardiovascular disease in a cohort of women followed up since 1976","volume":"315","author":"Rich-Edwards","year":"1997","journal-title":"BMJ"},{"key":"2021113011210172700_B5","doi-asserted-by":"publisher","first-page":"564","DOI":"10.1136\/bmj.298.6673.564","article-title":"Growth in utero, blood pressure in childhood and adult life, and mortality from cardiovascular disease","volume":"298","author":"Barker","year":"1989","journal-title":"BMJ"},{"key":"2021113011210172700_B6","doi-asserted-by":"publisher","first-page":"1115","DOI":"10.1136\/bmj.38434.629630.E0","article-title":"Longitudinal study of birth weight and adult body mass index in predicting risk of coronary heart disease and stroke in women","volume":"330","author":"Rich-Edwards","year":"2005","journal-title":"BMJ"},{"key":"2021113011210172700_B7","doi-asserted-by":"publisher","first-page":"1524","DOI":"10.1136\/bmj.307.6918.1524","article-title":"Growth in utero and serum cholesterol concentrations in adult life","volume":"307","author":"Barker","year":"1993","journal-title":"BMJ"},{"key":"2021113011210172700_B8","doi-asserted-by":"publisher","first-page":"1234","DOI":"10.1093\/ije\/dyi127","article-title":"Cohort Profile: The Hertfordshire Cohort Study","volume":"34","author":"Syddall","year":"2005","journal-title":"Int. J. Epidemiol."},{"key":"2021113011210172700_B9","doi-asserted-by":"publisher","first-page":"4727","DOI":"10.1113\/JP271745","article-title":"Programming of maternal and offspring disease: impact of growth restriction, fetal sex and transmission across generations","volume":"594","author":"Cheong","year":"2016","journal-title":"J. Physiol."},{"key":"2021113011210172700_B10","doi-asserted-by":"publisher","first-page":"036016","DOI":"10.1088\/1752-7163\/aaba84","article-title":"Nonhuman primate breath volatile organic compounds associate with developmental programming and cardio-metabolic status","volume":"12","author":"Bishop","year":"2018","journal-title":"J. Breath Res."},{"key":"2021113011210172700_B11","doi-asserted-by":"publisher","first-page":"4245","DOI":"10.1113\/JP273928","article-title":"Maternal nutrient restriction during pregnancy and lactation leads to impaired right ventricular function in young adult baboons","volume":"13","author":"Kuo","year":"2017","journal-title":"J. Physiol."},{"key":"2021113011210172700_B12","doi-asserted-by":"publisher","first-page":"5777","DOI":"10.1113\/JP275139","article-title":"Intrauterine growth restriction results in persistent vascular mismatch in adulthood","volume":"596","author":"Kuo","year":"2017","journal-title":"J. Physiol."},{"key":"2021113011210172700_B13","doi-asserted-by":"publisher","first-page":"181","DOI":"10.1016\/j.yjmcc.2017.06.006","article-title":"Sexual dimorphism in the fetal cardiac response to maternal nutrient restriction","volume":"108","author":"Muralimanoharan","year":"2017","journal-title":"J. Mol. Cell Cardiol."},{"key":"2021113011210172700_B14","doi-asserted-by":"publisher","first-page":"1093","DOI":"10.1113\/JP272908","article-title":"Cardiac remodelling in a baboon model of intrauterine growth restriction mimics accelerated ageing","volume":"595","author":"Kuo","year":"2017","journal-title":"J. Physiol."},{"key":"2021113011210172700_B15","doi-asserted-by":"publisher","first-page":"293","DOI":"10.1111\/jmp.12290","article-title":"Effect of moderate, 30 percent global maternal nutrient reduction on fetal and postnatal baboon phenotype","volume":"46","author":"Li","year":"2017","journal-title":"J. Med. Primatol."},{"key":"2021113011210172700_B16","doi-asserted-by":"publisher","first-page":"275","DOI":"10.1530\/JOE-13-0012","article-title":"Intrauterine growth restriction alters term fetal baboon hypothalamic appetitive peptide balance","volume":"217","author":"Li","year":"2013","journal-title":"J. Endocrinol."},{"key":"2021113011210172700_B17","doi-asserted-by":"publisher","first-page":"48","DOI":"10.1002\/uog.5210","article-title":"Human fetal cardiovascular profile score and neonatal outcome in intrauterine growth restriction","volume":"31","author":"M\u00e4kikallio","year":"2008","journal-title":"Ultrasound Obstet. Gynecol."},{"key":"2021113011210172700_B18","doi-asserted-by":"publisher","first-page":"8","DOI":"10.1159\/000020969","article-title":"Intrauterine growth retardation and fetal cardiac function","volume":"15","author":"Severi","year":"2000","journal-title":"Fetal Diagn. Ther."},{"key":"2021113011210172700_B19","doi-asserted-by":"publisher","first-page":"5625","DOI":"10.1113\/JP276072","article-title":"The role of miRNA regulation in fetal cardiomyocytes, cardiac maturation and the risk of heart disease in adults","volume":"596","author":"Lock","year":"2018","journal-title":"J. Physiol."},{"key":"2021113011210172700_B20","doi-asserted-by":"publisher","first-page":"20192713","DOI":"10.1098\/rspb.2019.2713","article-title":"Developmental programming of mitochondrial biology: a conceptual framework and review","volume":"287","author":"Gyllenhammer","year":"2020","journal-title":"Proc. R. Soc. B Biol. Sci."},{"key":"2021113011210172700_B21","doi-asserted-by":"publisher","first-page":"3040","DOI":"10.1161\/01.CIR.0000072789.89096.10","article-title":"Abnormal cardiac and skeletal muscle energy metabolism in patients with type 2 diabetes","volume":"107","author":"Scheuermann-Freestone","year":"2003","journal-title":"Circulation"},{"key":"2021113011210172700_B22","doi-asserted-by":"publisher","first-page":"117","DOI":"10.1111\/j.1600-0684.2004.00067.x","article-title":"Development of a system for individual feeding of baboons maintained in an outdoor group social environment","volume":"33","author":"Schlabritz-Loutsevitch","year":"2004","journal-title":"J. Med. Primatol."},{"key":"2021113011210172700_B23","doi-asserted-by":"publisher","first-page":"152","DOI":"10.1111\/j.1600-0684.2004.00066.x","article-title":"Normal concentrations of essential and toxic elements in pregnant baboons and fetuses (Papio species)","volume":"33","author":"Schlabritz-Loutsevitch","year":"2004","journal-title":"J. Med. Primatol."},{"key":"2021113011210172700_B24","doi-asserted-by":"publisher","first-page":"1457","DOI":"10.1089\/neu.2004.21.1457","article-title":"Dietary omega-3 fatty acids normalize BDNF levels, reduce oxidative damage, and counteract learning disability after traumatic brain injury in rats","volume":"21","author":"Wu","year":"2004","journal-title":"J. Neurotrauma"},{"key":"2021113011210172700_B25","doi-asserted-by":"publisher","first-page":"191","DOI":"10.1093\/toxsci\/kfy068","article-title":"Metabolic and phenotypic characterization of human skin fibroblasts after forcing oxidative capacity","volume":"164","author":"Pereira","year":"2018","journal-title":"Toxicol. Sci."},{"key":"2021113011210172700_B26","doi-asserted-by":"publisher","first-page":"67","DOI":"10.1113\/jphysiol.2006.106872","article-title":"Effect of 30 per cent maternal nutrient restriction from 0.16 to 0.5 gestation on fetal baboon kidney gene expression","volume":"572","author":"Cox","year":"2006","journal-title":"J. Physiol."},{"key":"2021113011210172700_B27","doi-asserted-by":"publisher","first-page":"478","DOI":"10.1016\/j.cbi.2010.09.027","article-title":"Sub-chronic administration of doxorubicin to Wistar rats results in oxidative stress and unaltered apoptotic signaling in the lung","volume":"188","author":"Machado","year":"2010","journal-title":"Chem. Biol. Interact."},{"key":"2021113011210172700_B28","doi-asserted-by":"publisher","first-page":"318","DOI":"10.1016\/j.ab.2010.02.036","article-title":"Reversible Ponceau staining as a loading control alternative to actin in Western blots","volume":"401","author":"Romero-Calvo","year":"2010","journal-title":"Anal. Biochem."},{"key":"2021113011210172700_B29","doi-asserted-by":"publisher","first-page":"2844","DOI":"10.1002\/elps.200500785","article-title":"\u03b2-Actin is not a reliable loading control in Western blot analysis","volume":"27","author":"Dittmer","year":"2006","journal-title":"Electrophoresis"},{"key":"2021113011210172700_B30","doi-asserted-by":"publisher","first-page":"250","DOI":"10.1016\/j.jneumeth.2008.05.003","article-title":"The use of total protein stains as loading controls: An alternative to high-abundance single-protein controls in semi-quantitative immunoblotting","volume":"172","author":"Aldridge","year":"2008","journal-title":"J. Neurosci. Methods"},{"key":"2021113011210172700_B31","doi-asserted-by":"publisher","first-page":"F1217","DOI":"10.1152\/ajprenal.00419.2014","article-title":"Effects of moderate global maternal nutrient reduction on fetal baboon renal mitochondrial gene expression at 0.9 gestation","volume":"308","author":"Pereira","year":"2015","journal-title":"Am. J. Physiol. Renal Physiol."},{"key":"2021113011210172700_B32","doi-asserted-by":"publisher","first-page":"276","DOI":"10.1016\/j.lfs.2009.05.019","article-title":"Comparison of two methods for assaying complex I activity in mitochondria isolated from rat liver, brain and heart","volume":"85","author":"Long","year":"2009","journal-title":"Life Sci."},{"key":"2021113011210172700_B33","doi-asserted-by":"publisher","first-page":"213","DOI":"10.1016\/0076-6879(67)10042-6","article-title":"Preparation and properties of succinic-cytochrome c reductase (complex II-III)","volume":"10","author":"Tisdale","year":"1967","journal-title":"Methods Enzymol."},{"key":"2021113011210172700_B34","doi-asserted-by":"publisher","first-page":"38","DOI":"10.1016\/j.cca.2008.04.025","article-title":"An improved spectrophotometric method for a more specific and accurate assay of mitochondrial complex III activity","volume":"395","author":"Luo","year":"2008","journal-title":"Clin. Chim. Acta"},{"key":"2021113011210172700_B35","doi-asserted-by":"publisher","first-page":"128","DOI":"10.1016\/S0076-6879(78)53021-8","article-title":"Mitochondrial cytochrome c: Preparation and activity of native and chemically modified cytochromes c","volume":"53","author":"Brautigan","year":"1978","journal-title":"Methods Enzymol."},{"key":"2021113011210172700_B36","doi-asserted-by":"publisher","first-page":"115","DOI":"10.1042\/bj1250115","article-title":"Regulation of adipose tissue pyruvate dehydrogenase by insulin and other hormones","volume":"125","author":"Coore","year":"1971","journal-title":"Biochem. J."},{"key":"2021113011210172700_B37","doi-asserted-by":"publisher","first-page":"941","DOI":"10.1161\/01.STR.27.5.941","article-title":"Relationships between ATP depletion, membrane potential, and the release of neurotransmitters in rat nerve terminals. An in vitro study under conditions that mimic anoxia, hypoglycemia, and ischemia","volume":"27","author":"Santos","year":"1996","journal-title":"Stroke"},{"key":"2021113011210172700_B38","doi-asserted-by":"publisher","first-page":"118","DOI":"10.1016\/0003-2697(85)90405-1","article-title":"Simultaneous extraction and reverse-phase high-performance liquid chromatographic determination of adenine and pyridine nucleotides in human red blood cells","volume":"146","author":"Stocchi","year":"1985","journal-title":"Anal. Biochem."},{"key":"2021113011210172700_B39","doi-asserted-by":"publisher","first-page":"421","DOI":"10.1016\/0076-6879(90)86135-I","article-title":"Malondialdehyde determination as index of lipid peroxidation","volume":"186","author":"Draper","year":"1990","journal-title":"Methods Enzymol."},{"key":"2021113011210172700_B40","doi-asserted-by":"publisher","first-page":"8","DOI":"10.1080\/01635580701365043","article-title":"Oxidant stress and B vitamins status in patients with non-small cell lung cancer","volume":"59","author":"Tsao","year":"2007","journal-title":"Nutr. Cancer"},{"key":"2021113011210172700_B41","first-page":"158","article-title":"Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase","volume":"70","author":"Paglia","year":"1967","journal-title":"J. Lab. Clin. Med."},{"key":"2021113011210172700_B42","first-page":"258","article-title":"Glutathione reductase","volume-title":"Methods in Enzymatic Analysis","author":"Goldberg","year":"1983"},{"key":"2021113011210172700_B43","first-page":"5","article-title":"Experiments on fixation for electron microscopy","volume":"103","author":"Malhotra","year":"1962","journal-title":"Small"},{"key":"2021113011210172700_B44","doi-asserted-by":"publisher","first-page":"2365","DOI":"10.1210\/en.2012-2111","article-title":"Up-regulation of the fetal baboon hypothalamo-pituitary-adrenal axis in intrauterine growth restriction: Coincidence with hypothalamic glucocorticoid receptor insensitivity and leptin receptor down-regulation","volume":"154","author":"Li","year":"2013","journal-title":"Endocrinology"},{"key":"2021113011210172700_B45","first-page":"1","article-title":"Poor perinatal growth impairs baboon aortic windkessel function","volume":"5038","author":"Kuo","year":"2017","journal-title":"J. Dev. Orig. Health Dis."},{"key":"2021113011210172700_B46","doi-asserted-by":"publisher","first-page":"254.e1","DOI":"10.1016\/j.ajog.2008.06.056","article-title":"Cardiac dysfunction and cell damage across clinical stages of severity in growth-restricted fetuses","volume":"199","author":"Crispi","year":"2008","journal-title":"Am. J. Obstet. Gynecol."},{"key":"2021113011210172700_B47","doi-asserted-by":"publisher","first-page":"2427","DOI":"10.1161\/CIRCULATIONAHA.110.937995","article-title":"Fetal growth restriction results in remodeled and less efficient hearts in children","volume":"121","author":"Crispi","year":"2010","journal-title":"Circulation"},{"key":"2021113011210172700_B48","doi-asserted-by":"publisher","first-page":"989","DOI":"10.1203\/01.PDR.0000061564.86797.78","article-title":"Cardiac hypertrophy and altered hemodynamic adaptation in growth-restricted preterm infants","volume":"53","author":"Leip\u00e4l\u00e4","year":"2003","journal-title":"Pediatr. Res."},{"key":"2021113011210172700_B49","doi-asserted-by":"publisher","first-page":"651","DOI":"10.1038\/pr.2014.22","article-title":"Neonatal cardiac dysfunction in intrauterine growth restriction","volume":"75","author":"Fouzas","year":"2014","journal-title":"Pediatr. Res."},{"key":"2021113011210172700_B50","doi-asserted-by":"publisher","first-page":"57.e1","DOI":"10.1016\/j.ajog.2011.03.010","article-title":"Tissue Doppler echocardiographic markers of cardiac dysfunction in small-for-gestational age fetuses","volume":"205","author":"Comas","year":"2011","journal-title":"YMOB"},{"key":"2021113011210172700_B51","doi-asserted-by":"publisher","first-page":"649","DOI":"10.1161\/CIRCULATIONAHA.107.709717","article-title":"Fetal hemodynamic adaptive changes related to intrauterine growth: The Generation R Study","volume":"117","author":"Verburg","year":"2008","journal-title":"Circulation"},{"key":"2021113011210172700_B52","doi-asserted-by":"publisher","first-page":"84","DOI":"10.1016\/j.theriogenology.2020.01.080","article-title":"Cardiorespiratory consequences of intrauterine growth restriction: influence of timing, severity and duration of hypoxaemia","volume":"150","author":"Darby","year":"2020","journal-title":"Theriogenology"},{"key":"2021113011210172700_B53","doi-asserted-by":"publisher","first-page":"197","DOI":"10.1161\/CIRCULATIONAHA.112.126920","article-title":"Preterm heart in adult life: cardiovascular magnetic resonance reveals distinct differences in left ventricular mass, geometry, and function","volume":"127","author":"Lewandowski","year":"2013","journal-title":"Circulation"},{"key":"2021113011210172700_B54","doi-asserted-by":"publisher","first-page":"880","DOI":"10.1038\/pr.2017.324","article-title":"Impact of preterm birth on the developing myocardium of the neonate","volume":"83","author":"Bensley","year":"2018","journal-title":"Pediatr. Res."},{"key":"2021113011210172700_B55","doi-asserted-by":"publisher","first-page":"4709","DOI":"10.1113\/jphysiol.2011.211185","article-title":"Fetal growth restriction and the programming of heart growth and cardiac insulin-like growth factor 2 expression in the lamb","volume":"589","author":"Wang","year":"2011","journal-title":"J. Physiol."},{"key":"2021113011210172700_B56","doi-asserted-by":"publisher","DOI":"10.1152\/ajpregu.00798.2006","article-title":"Restriction of placental function alters heart development in the sheep fetus","volume":"293","author":"Morrison","year":"2007","journal-title":"Am. J. Physiol. Regul. Integr. Comp. Physiol."},{"key":"2021113011210172700_B57","doi-asserted-by":"publisher","first-page":"871","DOI":"10.1113\/jphysiol.2006.121160","article-title":"Intrauterine growth restriction delays cardiomyocyte maturation and alters coronary artery function in the fetal sheep","volume":"578","author":"Bubb","year":"2007","journal-title":"J. Physiol."},{"key":"2021113011210172700_B58","doi-asserted-by":"publisher","first-page":"884","DOI":"10.1111\/1440-1681.12303","article-title":"Transgenerational left ventricular hypertrophy and hypertension in offspring after uteroplacental insufficiency in male rats","volume":"41","author":"Master","year":"2014","journal-title":"Clin. Exp. Pharmacol. Physiol."},{"key":"2021113011210172700_B59","doi-asserted-by":"publisher","first-page":"291","DOI":"10.1016\/j.ghir.2005.05.003","article-title":"Maternal nutrient restriction during early to mid gestation up-regulates cardiac insulin-like growth factor (IGF) receptors associated with enlarged ventricular size in fetal sheep","volume":"15","author":"Dong","year":"2005","journal-title":"Growth Horm. IGF Res."},{"key":"2021113011210172700_B60","doi-asserted-by":"publisher","first-page":"1258","DOI":"10.1016\/j.jnutbio.2012.10.001","article-title":"Maternal nutrient restriction predisposes ventricular remodeling in adult sheep offspring","volume":"24","author":"Ge","year":"2013","journal-title":"J. Nutr. Biochem."},{"key":"2021113011210172700_B61","doi-asserted-by":"publisher","first-page":"1647","DOI":"10.1056\/NEJMoa021715","article-title":"The incidence of pediatric cardiomyopathy in two regions of the United States","volume":"348","author":"Lipshultz","year":"2003","journal-title":"N. Engl. J. Med."},{"key":"2021113011210172700_B62","doi-asserted-by":"publisher","first-page":"913","DOI":"10.1056\/NEJM199403313301308","article-title":"Inherited cardiomyopathies","volume":"330","author":"Kelly","year":"1994","journal-title":"N. Engl. J. Med."},{"key":"2021113011210172700_B63","doi-asserted-by":"publisher","first-page":"75","DOI":"10.1016\/j.ppedcard.2011.02.002","article-title":"Bioenergetics, mitochondria, and cardiac myocyte differentiation","volume":"31","author":"Porter","year":"2011","journal-title":"Prog. Pediatr. Cardiol."},{"key":"2021113011210172700_B64","doi-asserted-by":"publisher","first-page":"63","DOI":"10.1016\/j.placenta.2017.05.008","article-title":"Mitochondrial DNA content and methylation in fetal cord blood of pregnancies with placental insufficiency","volume":"55","author":"Novielli","year":"2017","journal-title":"Placenta"},{"key":"2021113011210172700_B65","doi-asserted-by":"publisher","first-page":"499","DOI":"10.1016\/j.ebiom.2015.04.002","article-title":"Altered mitochondrial function, mitochondrial DNA and reduced metabolic flexibility in patients with diabetic nephropathy","volume":"2","author":"Czajka","year":"2015","journal-title":"EBioMedicine"},{"key":"2021113011210172700_B66","doi-asserted-by":"publisher","first-page":"768","DOI":"10.1002\/dmrr.2814","article-title":"Reduced peripheral blood mtDNA content is associated with impaired glucose-stimulated islet \u03b2 cell function in a Chinese population with different degrees of glucose tolerance","volume":"32","author":"Zhou","year":"2016","journal-title":"Diabetes Metab. Res. Rev."},{"key":"2021113011210172700_B67","doi-asserted-by":"publisher","first-page":"14","DOI":"10.1016\/j.freeradbiomed.2016.04.001","article-title":"Mitochondrial generation of superoxide and hydrogen peroxide as the source of mitochondrial redox signaling","volume":"100","author":"Brand","year":"2016","journal-title":"Free Radic. Biol. Med."},{"key":"2021113011210172700_B68","doi-asserted-by":"publisher","first-page":"76","DOI":"10.1016\/j.freeradbiomed.2018.01.024","article-title":"ROS and redox signaling in myocardial ischemia-reperfusion injury and cardioprotection","volume":"117","author":"Cadenas","year":"2018","journal-title":"Free Radic. Biol. Med."},{"key":"2021113011210172700_B69","doi-asserted-by":"publisher","first-page":"1278","DOI":"10.1016\/j.freeradbiomed.2005.02.014","article-title":"Mitochondrial dysfunction in cardiovascular disease","volume":"38","author":"Ballinger","year":"2005","journal-title":"Free Radic. Biol. Med."},{"key":"2021113011210172700_B70","doi-asserted-by":"publisher","first-page":"909","DOI":"10.1152\/physrev.00026.2013","article-title":"Mitochondrial reactive oxygen species (ROS) and ROS-induced ROS release","volume":"94","author":"Zorov","year":"2014","journal-title":"Physiol. Rev."},{"key":"2021113011210172700_B71","doi-asserted-by":"publisher","first-page":"514","DOI":"10.1073\/pnas.94.2.514","article-title":"Mitochondrial DNA damage is more extensive and persists longer than nuclear DNA damage in human cells following oxidative stress","volume":"94","author":"Yakes","year":"1997","journal-title":"Proc. Natl. Acad Sci. U.S.A."},{"key":"2021113011210172700_B72","doi-asserted-by":"publisher","first-page":"1853","DOI":"10.1016\/j.bbadis.2018.12.008","article-title":"Mitochondrial regulation of cardiac aging","volume":"1865","author":"Wang","year":"2019","journal-title":"Biochim. Biophys Acta Mol. Basis Dis."},{"key":"2021113011210172700_B73","doi-asserted-by":"publisher","first-page":"226","DOI":"10.1161\/01.RES.0000029232.42227.16","article-title":"Inducible expression of BNIP3 provokes mitochondrial defects and hypoxia-mediated cell death of ventricular myocytes","volume":"91","author":"Regula","year":"2002","journal-title":"Circ. Res."},{"key":"2021113011210172700_B74","doi-asserted-by":"publisher","first-page":"411","DOI":"10.1016\/j.freeradbiomed.2017.08.010","article-title":"Ellagic acid antagonizes Bnip3-mediated mitochondrial injury and necrotic cell death of cardiac myocytes","volume":"112","author":"Dhingra","year":"2017","journal-title":"Free Radic. Biol. Med."},{"key":"2021113011210172700_B75","doi-asserted-by":"publisher","first-page":"72","DOI":"10.1016\/j.cca.2020.02.024","article-title":"Bnip3 in mitophagy: Novel insights and potential therapeutic target for diseases of secondary mitochondrial dysfunction","volume":"506","author":"Gao","year":"2020","journal-title":"Clin. Chim. Acta"},{"key":"2021113011210172700_B76","doi-asserted-by":"publisher","first-page":"602","DOI":"10.1016\/j.bbabio.2010.11.001","article-title":"Electron microscopy morphology of the mitochondrial network in gliomas and their vascular microenvironment","volume":"1807","author":"Arismendi-Morillo","year":"2010","journal-title":"Biochim. Biophys. Acta"},{"key":"2021113011210172700_B77","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1017\/S1462399402004453","article-title":"Mitochondria as targets for detection and treatment of cancer","volume":"4","author":"Modica-Napolitano","year":"2002","journal-title":"Expert Rev. Mol. Med."},{"key":"2021113011210172700_B78","doi-asserted-by":"publisher","first-page":"2672","DOI":"10.1161\/01.CIR.0000100664.10777.B8","article-title":"Clinical characterization of left ventricular noncompaction in children: a relatively common form of cardiomyopathy","volume":"108","author":"Pignatelli","year":"2003","journal-title":"Circulation"},{"key":"2021113011210172700_B79","doi-asserted-by":"publisher","first-page":"330","DOI":"10.1038\/s41419-017-0023-6","article-title":"Mitofusin 2: from functions to disease","volume":"9","author":"Filadi","year":"2018","journal-title":"Cell Death Dis."},{"key":"2021113011210172700_B80","doi-asserted-by":"publisher","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":"2021113011210172700_B81","doi-asserted-by":"publisher","first-page":"R1941","DOI":"10.1152\/ajpregu.90724.2008","article-title":"Sex differences in the developmental origins of hypertension and cardiorenal disease","volume":"295","author":"Gilbert","year":"2008","journal-title":"Am. J. Physiol. Regul. Integr. Comp. Physiol."},{"key":"2021113011210172700_B82","doi-asserted-by":"publisher","first-page":"1","DOI":"10.14814\/phy2.13125","article-title":"Sex-specific differences in mitochondria biogenesis, morphology, respiratory function, and ROS homeostasis in young mouse heart and brain","volume":"5","author":"Khalifa","year":"2017","journal-title":"Physiol. Rep."},{"key":"2021113011210172700_B83","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/s13293-018-0193-7","article-title":"Sex-associated differences in mitochondrial function in human peripheral blood mononuclear cells (PBMCs) and brain","volume":"9","author":"Silaidos","year":"2018","journal-title":"Biol. Sex Differ."},{"key":"2021113011210172700_B84","doi-asserted-by":"publisher","first-page":"101435","DOI":"10.1016\/j.redox.2020.101435","article-title":"Estrogenic control of mitochondrial function","volume":"31","author":"Klinge","year":"2020","journal-title":"Redox Biol."},{"key":"2021113011210172700_B85","doi-asserted-by":"publisher","first-page":"5083","DOI":"10.1113\/JP276338","article-title":"Ageing changes in biventricular cardiac function in male and female baboons (Papio spp.)","volume":"596","author":"Kuo","year":"2018","journal-title":"J. Physiol."},{"key":"2021113011210172700_B86","doi-asserted-by":"publisher","first-page":"1650","DOI":"10.1016\/j.jnutbio.2015.08.004","article-title":"Fetal undernutrition is associated with perinatal sex-dependent alterations in oxidative status","volume":"26","author":"Rodr\u00edguez-Rodr\u00edguez","year":"2015","journal-title":"J. Nutr. Biochem."},{"key":"2021113011210172700_B87","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3389\/fendo.2018.00732","article-title":"Sex differences in cardiac mitochondria in the New Zealand obese mouse","volume":"9","author":"John","year":"2018","journal-title":"Front. Endocrinol. (Lausanne)"},{"key":"2021113011210172700_B88","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3389\/fphys.2018.01133","article-title":"Superior intrinsic mitochondrial respiration in women than in men","volume":"9","author":"Cardinale","year":"2018","journal-title":"Front. Physiol."},{"key":"2021113011210172700_B89","doi-asserted-by":"publisher","first-page":"108","DOI":"10.1016\/j.mad.2016.12.005","article-title":"Mitochondrial activity and dynamics changes regarding metabolism in ageing and obesity","volume":"162","author":"L\u00f3pez-Lluch","year":"2017","journal-title":"Mech. Ageing Dev."},{"key":"2021113011210172700_B90","doi-asserted-by":"publisher","first-page":"746","DOI":"10.3109\/09513590.2011.652720","article-title":"Why sex matters: the biological mechanisms of cardiovascular disease","volume":"28","author":"Vassalle","year":"2012","journal-title":"Gynecol. Endocrinol."},{"key":"2021113011210172700_B91","doi-asserted-by":"publisher","first-page":"93","DOI":"10.1139\/y05-151","article-title":"The role of sex in cardiac function and disease","volume":"84","author":"Czubryt","year":"2006","journal-title":"Can. J. Physiol. Pharmacol."},{"key":"2021113011210172700_B92","doi-asserted-by":"publisher","first-page":"2468","DOI":"10.1161\/01.CIR.96.7.2468","article-title":"Cardiovascular disease in women\u202f: a statement for healthcare professionals from the American Heart Association","volume":"96","author":"Mosca","year":"1997","journal-title":"Circulation"},{"key":"2021113011210172700_B93","doi-asserted-by":"publisher","first-page":"704","DOI":"10.1016\/S0002-8703(96)90274-4","article-title":"Gender-related differences in exercise ventricular function among healthy subjects and patients","volume":"131","author":"Merz","year":"1996","journal-title":"Am. Heart J."},{"key":"2021113011210172700_B94","doi-asserted-by":"publisher","first-page":"1265","DOI":"10.1253\/circj.CJ-10-0196","article-title":"Sex and gender differences in myocardial hypertrophy and heart failure","volume":"74","author":"Regitz-Zagrosek","year":"2010","journal-title":"Circ. J."},{"key":"2021113011210172700_B95","doi-asserted-by":"publisher","first-page":"R757","DOI":"10.1152\/ajpregu.00051.2011","article-title":"Emergence of insulin resistance in juvenile baboon offspring of mothers exposed to moderate maternal nutrient reduction","volume":"301","author":"Choi","year":"2011","journal-title":"Am. J. Physiol. Regul. Integr. Comp. Physiol."},{"key":"2021113011210172700_B96","doi-asserted-by":"publisher","first-page":"R740","DOI":"10.1152\/ajpregu.00161.2015","article-title":"Reduced placental amino acid transport in response to maternal nutrient restriction in the baboon","volume":"309","author":"Pantham","year":"2015","journal-title":"Am. J. Physiol. Integr Comp. Physiol."},{"key":"2021113011210172700_B97","first-page":"97A","article-title":"Accelerated aging of cardiac function in offspring of undernourished pregnant baboons","volume":"22","author":"Kuo","year":"2015","journal-title":"Reprod. Sci."},{"key":"2021113011210172700_B98","doi-asserted-by":"publisher","first-page":"269","DOI":"10.1007\/s11357-018-0024-0","article-title":"Maternal nutrient restriction in baboon programs later-life cellular growth and respiration of cultured skin fibroblasts: a potential model for the study of aging-programming interactions","volume":"40","author":"Salmon","year":"2018","journal-title":"GeroScience"}],"container-title":["Clinical Science"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/portlandpress.com\/clinsci\/article-pdf\/135\/9\/1103\/911021\/cs-2020-1339.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/portlandpress.com\/clinsci\/article-pdf\/135\/9\/1103\/911021\/cs-2020-1339.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,11,30]],"date-time":"2021-11-30T12:17:57Z","timestamp":1638274677000},"score":1,"resource":{"primary":{"URL":"https:\/\/portlandpress.com\/clinsci\/article\/135\/9\/1103\/228457\/Sex-dependent-vulnerability-of-fetal-nonhuman"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,5]]},"references-count":98,"journal-issue":{"issue":"9","published-print":{"date-parts":[[2021,5,14]]}},"URL":"https:\/\/doi.org\/10.1042\/cs20201339","relation":{},"ISSN":["0143-5221","1470-8736"],"issn-type":[{"value":"0143-5221","type":"print"},{"value":"1470-8736","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2021,5]]},"published":{"date-parts":[[2021,5]]}}}