{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,25]],"date-time":"2026-10-25T00:18:31Z","timestamp":1792887511759,"version":"4.5.0"},"reference-count":41,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2021,3,18]],"date-time":"2021-03-18T00:00:00Z","timestamp":1616025600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2021,3,18]],"date-time":"2021-03-18T00:00:00Z","timestamp":1616025600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"name":"The National Advisory Unit for Women\u2019s Health"},{"DOI":"10.13039\/501100009707","name":"Diabetesforbundet","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100009707","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Freia"},{"name":"Blix"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Cholesteryl ester transfer protein (CETP) regulates high density lipoproteins (HDL)-cholesterol (C) and HDL-C is essential for fetal development. We hypothesized that women giving birth to large-for-gestational-age (LGA) and small-for-gestational age (SGA) infants differed in longitudinal changes in lipoproteins, CETP activity and HDL-C and that placentas from women with higher or lower circulating HDL-C displayed differential expression of mRNAs involved in cholesterol\/nutrient transport, insulin signaling, inflammation\/ extracellular matrix (ECM) remodeling. Circulating lipids and CETP activity was measured during pregnancy, NMR lipidomics in late pregnancy, and associations with LGA and SGA infants investigated. RNA sequencing was performed in 28 placentas according to higher and lower maternal HDL-C levels. Lipidomics revealed high triglycerides in large VLDL and lipids\/cholesterol\/cholesteryl esters in small HDL in women giving birth to SGA infants. Placentas from women with higher HDL-C had decreased levels of<jats:italic>CETP<\/jats:italic>expression which was associated with mRNAs involved in cholesterol\/nutrient transport, insulin signaling and inflammation\/ECM remodeling. Both placental and circulating CETP levels were associated with growth of the fetus. Low circulating CETP activity at 36\u201338\u00a0weeks was associated with giving birth to SGA infants. Our findings suggest a link between increased maternal HDL-C levels, low CETP levels both in circulation and placenta, and SGA infants.<\/jats:p>","DOI":"10.1038\/s41598-021-85777-3","type":"journal-article","created":{"date-parts":[[2021,3,18]],"date-time":"2021-03-18T16:48:15Z","timestamp":1616086095000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":12,"title":["Low CETP activity and unique composition of large VLDL and small HDL in women giving birth to small-for-gestational age infants"],"prefix":"10.1038","volume":"11","author":[{"given":"Marie Cecilie Paasche","family":"Roland","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kristin","family":"Godang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"P\u00e5l","family":"Aukrust","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tore","family":"Henriksen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tove","family":"Lekva","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2021,3,18]]},"reference":[{"key":"85777_CR1","doi-asserted-by":"publisher","first-page":"391","DOI":"10.1016\/j.atherosclerosis.2014.09.027","volume":"237","author":"S Visentin","year":"2014","unstructured":"Visentin, S. et al. Early origins of adult disease: Low birth weight and vascular remodeling. Atherosclerosis 237, 391\u2013399 (2014).","journal-title":"Atherosclerosis"},{"key":"85777_CR2","doi-asserted-by":"publisher","first-page":"1088","DOI":"10.1161\/hc0902.104677","volume":"105","author":"CM Law","year":"2002","unstructured":"Law, C. M. et al. Fetal, infant, and childhood growth and adult blood pressure: A longitudinal study from birth to 22 years of age. Circulation 105, 1088\u20131092 (2002).","journal-title":"Circulation"},{"key":"85777_CR3","doi-asserted-by":"publisher","first-page":"852","DOI":"10.1111\/aogs.12665","volume":"94","author":"LM Mudd","year":"2015","unstructured":"Mudd, L. M., Holzman, C. B. & Evans, R. W. Maternal mid-pregnancy lipids and birthweight. Acta Obstet. Gynecol. Scand. 94, 852\u2013860 (2015).","journal-title":"Acta Obstet. Gynecol. Scand."},{"key":"85777_CR4","doi-asserted-by":"publisher","first-page":"2706","DOI":"10.2337\/dc12-2445","volume":"36","author":"SR Kulkarni","year":"2013","unstructured":"Kulkarni, S. R. et al. Maternal lipids are as important as glucose for fetal growth: Findings from the Pune Maternal Nutrition Study. Diabetes Care 36, 2706\u20132713 (2013).","journal-title":"Diabetes Care"},{"key":"85777_CR5","first-page":"128","volume":"84","author":"N Sattar","year":"1999","unstructured":"Sattar, N. et al. Lipid and lipoprotein concentrations in pregnancies complicated by intrauterine growth restriction. J. Clin. Endocrinol. Metab. 84, 128\u2013130 (1999).","journal-title":"J. Clin. Endocrinol. Metab."},{"key":"85777_CR6","doi-asserted-by":"publisher","first-page":"59","DOI":"10.1016\/j.placenta.2016.12.006","volume":"54","author":"LA Gallo","year":"2017","unstructured":"Gallo, L. A., Barrett, H. L. & Dekker Nitert, M. Review: Placental transport and metabolism of energy substrates in maternal obesity and diabetes. Placenta 54, 59\u201367 (2017).","journal-title":"Placenta"},{"key":"85777_CR7","doi-asserted-by":"publisher","first-page":"735","DOI":"10.1016\/0002-9378(77)90713-X","volume":"128","author":"DS Lin","year":"1977","unstructured":"Lin, D. S., Pitkin, R. M. & Connor, W. E. Placental transfer of cholesterol into the human fetus. Am. J. Obstet. Gynecol. 128, 735\u2013739 (1977).","journal-title":"Am. J. Obstet. Gynecol."},{"key":"85777_CR8","doi-asserted-by":"publisher","first-page":"2584","DOI":"10.1172\/JCI107075","volume":"51","author":"RM Pitkin","year":"1972","unstructured":"Pitkin, R. M., Connor, W. E. & Lin, D. S. Cholesterol metabolism and placental transfer in the pregnant Rhesus monkey. J. Clin. Investig. 51, 2584\u20132592 (1972).","journal-title":"J. Clin. Investig."},{"key":"85777_CR9","doi-asserted-by":"publisher","first-page":"737","DOI":"10.1016\/j.bbalip.2012.12.015","volume":"1831","author":"I Sreckovic","year":"2013","unstructured":"Sreckovic, I. et al. Distinct composition of human fetal HDL attenuates its anti-oxidative capacity. Biochim. Biophys. Acta 1831, 737\u2013746 (2013).","journal-title":"Biochim. Biophys. Acta"},{"issue":"Suppl 2","key":"85777_CR10","doi-asserted-by":"publisher","first-page":"S218","DOI":"10.1016\/j.placenta.2011.01.011","volume":"32","author":"LA Woollett","year":"2011","unstructured":"Woollett, L. A. Review: Transport of maternal cholesterol to the fetal circulation. Placenta 32(Suppl 2), S218\u2013S221 (2011).","journal-title":"Placenta"},{"key":"85777_CR11","doi-asserted-by":"publisher","first-page":"2575","DOI":"10.1194\/jlr.R035725","volume":"54","author":"AS Shah","year":"2013","unstructured":"Shah, A. S., Tan, L., Long, J. L. & Davidson, W. S. Proteomic diversity of high density lipoproteins: Our emerging understanding of its importance in lipid transport and beyond. J. Lipid Res. 54, 2575\u20132585 (2013).","journal-title":"J. Lipid Res."},{"key":"85777_CR12","doi-asserted-by":"publisher","first-page":"341","DOI":"10.1016\/j.pharmthera.2012.12.001","volume":"137","author":"G Marsche","year":"2013","unstructured":"Marsche, G., Saemann, M. D., Heinemann, A. & Holzer, M. Inflammation alters HDL composition and function: Implications for HDL-raising therapies. Pharmacol. Ther. 137, 341\u2013351 (2013).","journal-title":"Pharmacol. Ther."},{"key":"85777_CR13","doi-asserted-by":"publisher","first-page":"2466","DOI":"10.1210\/jc.2011-2969","volume":"97","author":"M Scholler","year":"2012","unstructured":"Scholler, M. et al. Phospholipid transfer protein is differentially expressed in human arterial and venous placental endothelial cells and enhances cholesterol efflux to fetal HDL. J. Clin. Endocrinol. Metab. 97, 2466\u20132474 (2012).","journal-title":"J. Clin. Endocrinol. Metab."},{"key":"85777_CR14","doi-asserted-by":"publisher","first-page":"2339","DOI":"10.1194\/jlr.M300228-JLR200","volume":"44","author":"RL Kitchens","year":"2003","unstructured":"Kitchens, R. L., Thompson, P. A., Munford, R. S. & O\u2019Keefe, G. E. Acute inflammation and infection maintain circulating phospholipid levels and enhance lipopolysaccharide binding to plasma lipoproteins. J. Lipid Res. 44, 2339\u20132348 (2003).","journal-title":"J. Lipid Res."},{"key":"85777_CR15","doi-asserted-by":"publisher","first-page":"424","DOI":"10.1016\/S0022-2275(20)34481-3","volume":"41","author":"JA McConihay","year":"2000","unstructured":"McConihay, J. A., Honkomp, A. M., Granholm, N. A. & Woollett, L. A. Maternal high density lipoproteins affect fetal mass and extra-embryonic fetal tissue sterol metabolism in the mouse. J. Lipid Res. 41, 424\u2013432 (2000).","journal-title":"J. Lipid Res."},{"key":"85777_CR16","doi-asserted-by":"publisher","first-page":"717","DOI":"10.1096\/fj.201700528R","volume":"32","author":"SL Rebholz","year":"2018","unstructured":"Rebholz, S. L. et al. Studies in genetically modified mice implicate maternal HDL as a mediator of fetal growth. FASEB J. 32, 717\u2013727 (2018).","journal-title":"FASEB J."},{"key":"85777_CR17","doi-asserted-by":"publisher","first-page":"983","DOI":"10.1016\/j.jpeds.2013.05.014","volume":"163","author":"MS Kramer","year":"2013","unstructured":"Kramer, M. S. et al. Maternal lipids and small for gestational age birth at term. J. Pediatr. 163, 983\u2013988 (2013).","journal-title":"J. Pediatr."},{"key":"85777_CR18","doi-asserted-by":"publisher","first-page":"21","DOI":"10.3390\/diseases5040021","volume":"5","author":"TD Filippatos","year":"2017","unstructured":"Filippatos, T. D., Kei, A. & Elisaf, M. S. Anacetrapib, a new CETP inhibitor: The new tool for the management of dyslipidemias?. Diseases 5, 21 (2017).","journal-title":"Diseases"},{"key":"85777_CR19","doi-asserted-by":"publisher","first-page":"e39324","DOI":"10.1371\/journal.pone.0039324","volume":"7","author":"MC Roland","year":"2012","unstructured":"Roland, M. C. et al. Fetal growth versus birthweight: The role of placenta versus other determinants. PLoS ONE 7, e39324 (2012).","journal-title":"PLoS ONE"},{"key":"85777_CR20","doi-asserted-by":"publisher","first-page":"63","DOI":"10.1530\/EJE-15-0153","volume":"173","author":"T Lekva","year":"2015","unstructured":"Lekva, T. et al. Beta-cell dysfunction in women with previous gestational diabetes is associated with visceral adipose tissue distribution. Eur. J. Endocrinol. 173, 63\u201370 (2015).","journal-title":"Eur. J. Endocrinol."},{"key":"85777_CR21","doi-asserted-by":"crossref","first-page":"440","DOI":"10.1034\/j.1600-0412.2000.079006440.x","volume":"79","author":"R Skjaerven","year":"2000","unstructured":"Skjaerven, R., Gjessing, H. K. & Bakketeig, L. S. Birthweight by gestational age in Norway. Acta Obstet. Gynecol. Scand. 79, 440\u2013449 (2000).","journal-title":"Acta Obstet. Gynecol. Scand."},{"key":"85777_CR22","doi-asserted-by":"publisher","first-page":"e0232749","DOI":"10.1371\/journal.pone.0232749","volume":"15","author":"MCP Roland","year":"2020","unstructured":"Roland, M. C. P., Lekva, T., Godang, K., Bollerslev, J. & Henriksen, T. Changes in maternal blood glucose and lipid concentrations during pregnancy differ by maternal body mass index and are related to birthweight: A prospective, longitudinal study of healthy pregnancies. PLoS ONE 15, e0232749 (2020).","journal-title":"PLoS ONE"},{"key":"85777_CR23","doi-asserted-by":"publisher","first-page":"499","DOI":"10.1093\/clinchem\/18.6.499","volume":"18","author":"WT Friedewald","year":"1972","unstructured":"Friedewald, W. T., Levy, R. I. & Fredrickson, D. S. Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin. Chem. 18, 499\u2013502 (1972).","journal-title":"Clin. Chem."},{"key":"85777_CR24","first-page":"dgz119","volume":"105","author":"T Ueland","year":"2019","unstructured":"Ueland, T. et al. Elevated cholesteryl ester transfer protein activity early in pregnancy predicts prediabetes 5 years later. J. Clin. Endocrinol. Metab. 105, dgz119 (2019).","journal-title":"J. Clin. Endocrinol. Metab."},{"key":"85777_CR25","doi-asserted-by":"publisher","first-page":"29715","DOI":"10.1038\/srep29715","volume":"6","author":"T Lekva","year":"2016","unstructured":"Lekva, T. et al. Gene expression in term placentas is regulated more by spinal or epidural anesthesia than by late-onset preeclampsia or gestational diabetes mellitus. Sci. Rep. 6, 29715 (2016).","journal-title":"Sci. Rep."},{"key":"85777_CR26","doi-asserted-by":"publisher","first-page":"550","DOI":"10.1186\/s13059-014-0550-8","volume":"15","author":"MI Love","year":"2014","unstructured":"Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).","journal-title":"Genome Biol."},{"key":"85777_CR27","doi-asserted-by":"publisher","first-page":"1101","DOI":"10.1161\/CIRCRESAHA.115.306052","volume":"116","author":"JW Heinecke","year":"2015","unstructured":"Heinecke, J. W. Small HDL promotes cholesterol efflux by the ABCA1 pathway in macrophages: Implications for therapies targeted to HDL. Circ. Res. 116, 1101\u20131103 (2015).","journal-title":"Circ. Res."},{"key":"85777_CR28","doi-asserted-by":"publisher","first-page":"144","DOI":"10.1038\/ncpcardio0500","volume":"3","author":"A Kontush","year":"2006","unstructured":"Kontush, A. & Chapman, M. J. Antiatherogenic small, dense HDL\u2014guardian angel of the arterial wall?. Nat. Clin. Pract. Cardiovasc. Med. 3, 144\u2013153 (2006).","journal-title":"Nat. Clin. Pract. Cardiovasc. Med."},{"key":"85777_CR29","doi-asserted-by":"publisher","first-page":"775","DOI":"10.1042\/BST20190129","volume":"48","author":"S Kallol","year":"2020","unstructured":"Kallol, S. & Albrecht, C. Materno-fetal cholesterol transport during pregnancy. Biochem. Soc. Trans. 48, 775\u2013786 (2020).","journal-title":"Biochem. Soc. Trans."},{"key":"85777_CR30","doi-asserted-by":"publisher","first-page":"1079","DOI":"10.1016\/j.placenta.2013.06.309","volume":"34","author":"M Baumann","year":"2013","unstructured":"Baumann, M. et al. Placental ABCA1 and ABCG1 expression in gestational disease: Pre-eclampsia affects ABCA1 levels in syncytiotrophoblasts. Placenta 34, 1079\u20131086 (2013).","journal-title":"Placenta"},{"key":"85777_CR31","doi-asserted-by":"publisher","first-page":"2552","DOI":"10.1210\/jc.2017-00289","volume":"102","author":"T Lekva","year":"2017","unstructured":"Lekva, T. et al. Large reduction in adiponectin during pregnancy is associated with large-for-gestational-age newborns. J. Clin. Endocrinol. Metab. 102, 2552\u20132559 (2017).","journal-title":"J. Clin. Endocrinol. Metab."},{"key":"85777_CR32","doi-asserted-by":"publisher","first-page":"6225","DOI":"10.1038\/s41598-019-42522-1","volume":"9","author":"H Melhem","year":"2019","unstructured":"Melhem, H. et al. Placental secretion of apolipoprotein A1 and E: The anti-atherogenic impact of the placenta. Sci. Rep. 9, 6225 (2019).","journal-title":"Sci. Rep."},{"key":"85777_CR33","doi-asserted-by":"publisher","first-page":"16153","DOI":"10.3390\/ijms150916153","volume":"15","author":"KE Brett","year":"2014","unstructured":"Brett, K. E., Ferraro, Z. M., Yockell-Lelievre, J., Gruslin, A. & Adamo, K. B. Maternal-fetal nutrient transport in pregnancy pathologies: The role of the placenta. Int. J. Mol. Sci. 15, 16153\u201316185 (2014).","journal-title":"Int. J. Mol. Sci."},{"key":"85777_CR34","doi-asserted-by":"publisher","first-page":"4225","DOI":"10.1210\/jc.2018-02778","volume":"104","author":"LB James-Allan","year":"2019","unstructured":"James-Allan, L. B., Arbet, J., Teal, S. B., Powell, T. L. & Jansson, T. Insulin stimulates GLUT4 trafficking to the syncytiotrophoblast basal plasma membrane in the human placenta. J. Clin. Endocrinol. Metab. 104, 4225\u20134238 (2019).","journal-title":"J. Clin. Endocrinol. Metab."},{"key":"85777_CR35","doi-asserted-by":"publisher","first-page":"951","DOI":"10.3389\/fphys.2017.00951","volume":"8","author":"E Winterhager","year":"2017","unstructured":"Winterhager, E. & Gellhaus, A. Transplacental nutrient transport mechanisms of intrauterine growth restriction in rodent models and humans. Front. Physiol. 8, 951 (2017).","journal-title":"Front. Physiol."},{"key":"85777_CR36","doi-asserted-by":"publisher","first-page":"1290","DOI":"10.1172\/JCI115993","volume":"90","author":"XC Jiang","year":"1992","unstructured":"Jiang, X. C., Agellon, L. B., Walsh, A., Breslow, J. L. & Tall, A. Dietary cholesterol increases transcription of the human cholesteryl ester transfer protein gene in transgenic mice. Dependence on natural flanking sequences. J. Clin. Investig. 90, 1290\u20131295 (1992).","journal-title":"J. Clin. Investig."},{"key":"85777_CR37","doi-asserted-by":"publisher","first-page":"1322","DOI":"10.1194\/jlr.M200425-JLR200","volume":"44","author":"W Le Goff","year":"2003","unstructured":"Le Goff, W., Guerin, M., Petit, L., Chapman, M. J. & Thillet, J. Regulation of human CETP gene expression: Role of SP1 and SP3 transcription factors at promoter sites -690, -629, and -37. J. Lipid Res. 44, 1322\u20131331 (2003).","journal-title":"J. Lipid Res."},{"key":"85777_CR38","doi-asserted-by":"publisher","first-page":"63","DOI":"10.1016\/0009-9120(94)90013-2","volume":"27","author":"A Iglesias","year":"1994","unstructured":"Iglesias, A., Montelongo, A., Herrera, E. & Lasuncion, M. A. Changes in cholesteryl ester transfer protein activity during normal gestation and postpartum. Clin. Biochem. 27, 63\u201368 (1994).","journal-title":"Clin. Biochem."},{"key":"85777_CR39","doi-asserted-by":"publisher","first-page":"4543","DOI":"10.1210\/jcem.85.12.7027","volume":"85","author":"K Winkler","year":"2000","unstructured":"Winkler, K. et al. Low density lipoprotein (LDL) subfractions during pregnancy: Accumulation of buoyant LDL with advancing gestation. J. Clin. Endocrinol. Metab. 85, 4543\u20134550 (2000).","journal-title":"J. Clin. Endocrinol. Metab."},{"key":"85777_CR40","doi-asserted-by":"publisher","first-page":"1318","DOI":"10.1016\/j.jacl.2017.08.020","volume":"11","author":"SM Kim","year":"2017","unstructured":"Kim, S. M. et al. Cord and maternal sera from small neonates share dysfunctional lipoproteins with proatherogenic properties: Evidence for Barker\u2019s hypothesis. J. Clin. Lipidol. 11, 1318-1328 e1313 (2017).","journal-title":"J. Clin. Lipidol."},{"key":"85777_CR41","doi-asserted-by":"publisher","first-page":"723","DOI":"10.1053\/meta.2001.23307","volume":"50","author":"S Kaser","year":"2001","unstructured":"Kaser, S. et al. Lipoprotein profile and cholesteryl ester transfer protein in neonates. Metabolism 50, 723\u2013728 (2001).","journal-title":"Metabolism"}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41598-021-85777-3.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-021-85777-3","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-021-85777-3.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,10,31]],"date-time":"2023-10-31T19:20:19Z","timestamp":1698780019000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41598-021-85777-3"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,3,18]]},"references-count":41,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2021,12]]}},"alternative-id":["85777"],"URL":"https:\/\/doi.org\/10.1038\/s41598-021-85777-3","relation":{},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,3,18]]},"assertion":[{"value":"3 August 2020","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"4 March 2021","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"18 March 2021","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"6213"}}