Maternal Tobacco Smoke Exposure Causes Sex-Divergent Changes in Placental Lipid Metabolism in the Rat

Claudia Weinheimer1, Haimei Wang2, Jessica Comstock3, Purneet Singh2, Zhengming Wang2, Brent A. Locklear2, Kasi L Goodwin2, J. Alan Maschek4, James E. Cox4, Michelle Baack5, Lisa Joss‐Moore2
1Department of Pediatrics, University of Utah, 295 Chipeta Way, Salt Lake City, UT, 84108, USA
2Department of Pediatrics, University of Utah, Salt Lake City, USA
3Department of Pathology, University of Utah, Salt Lake City, USA
4Health Science Center Cores, University of Utah Health Sciences Center, Salt Lake City, USA
5Sanford Research Center, Sioux Falls, USA

Tóm tắt

Từ khóa


Tài liệu tham khảo

Kyrklund-Blomberg NB, Cnattingius S. Preterm birth and maternal smoking: risks related to gestational age and onset of delivery. Am J Obstet Gynecol. 1998;179(4):1051–5.

Ko TJ, Tsai LY, Chu LC, Yeh SJ, Leung C, Chen CY, et al. Parental smoking during pregnancy and its association with low birth weight, small for gestational age, and preterm birth offspring: a birth cohort study. Pediatrics and neonatology. 2014;55(1):20–7.

Zdravkovic T, Genbacev O, McMaster MT, Fisher SJ. The adverse effects of maternal smoking on the human placenta: a review. Placenta. 2005;26(Suppl A):S81–6.

Gilliland FD, Berhane K, Li YF, Rappaport EB, Peters JM. Effects of early onset asthma and in utero exposure to maternal smoking on childhood lung function. Am J Respir Crit Care Med. 2003;167(6):917–24.

Tager IB, Ngo L, Hanrahan JP. Maternal smoking during pregnancy. Effects on lung function during the first 18 months of life. Am J Respir Crit Care Med. 1995;152(3):977–83.

Thornburg KL. The programming of cardiovascular disease. J Dev Orig Health Dis. 2015;6(5):366–76.

Broere-Brown ZA, Baan E, Schalekamp-Timmermans S, Verburg BO, Jaddoe VW, Steegers EA. Sex-specific differences in fetal and infant growth patterns: a prospective population-based cohort study. Biol Sex Differ. 2016;7:65.

Carpenter T, Grecian SM, Reynolds RM. Sex differences in early-life programming of the hypothalamic-pituitary-adrenal axis in humans suggest increased vulnerability in females: a systematic review. J Dev Orig Health Dis. 2017;8(2):244–55.

Sundrani DP, Roy SS, Jadhav AT, Joshi SR. Sex-specific differences and developmental programming for diseases in later life. Reprod Fertil Dev. 2017.

Drake P, Driscoll AK, Mathews TJ. Cigarette smoking during pregnancy: United States, 2016. NCHS data brief 2018(305):1–8.

Agostoni C, Galli C, Riva E, Colombo C, Giovannini M, Marangoni F. Reduced docosahexaenoic acid synthesis may contribute to growth restriction in infants born to mothers who smoke. J Pediatr. 2005;147(6):854–6.

Kuper SG, Abramovici AR, Jauk VC, Harper LM, Biggio JR, Tita AT. The effect of omega-3 supplementation on pregnancy outcomes by smoking status. Am J Obstet Gynecol. 2017;217(4):476.e471–6.

Lendvai A, Deutsch MJ, Plosch T, Ensenauer R. The peroxisome proliferator-activated receptors under epigenetic control in placental metabolism and fetal development. Am J Physiol Endocrinol Metab. 2016;310(10):E797–810.

Haggarty P. Fatty acid supply to the human fetus. Annu Rev Nutr. 2010;30:237–55.

Schaiff WT, Knapp FF Jr, Barak Y, Biron-Shental T, Nelson DM, Sadovsky Y. Ligand-activated peroxisome proliferator activated receptor gamma alters placental morphology and placental fatty acid uptake in mice. Endocrinology. 2007;148(8):3625–34.

Barak Y, Nelson MC, Ong ES, Jones YZ, Ruiz-Lozano P, Chien KR, et al. PPAR gamma is required for placental, cardiac, and adipose tissue development. Mol Cell. 1999;4(4):585–95.

Shalom-Barak T, Nicholas JM, Wang Y, Zhang X, Ong ES, Young TH, et al. Peroxisome proliferator-activated receptor gamma controls Muc1 transcription in trophoblasts. Mol Cell Biol. 2004;24(24):10661–9.

Shalom-Barak T, Zhang X, Chu T, Timothy Schaiff W, Reddy JK, Xu J, et al. Placental PPARgamma regulates spatiotemporally diverse genes and a unique metabolic network. Dev Biol. 2012;372(1):143–55.

Kolahi K, Louey S, Varlamov O, Thornburg K. Real-time tracking of bodipy-c12 long-chain fatty acid in human term placenta reveals unique lipid dynamics in cytotrophoblast cells. PLoS One. 2016;11(4).

Capparuccia L, Marzioni D, Giordano A, Fazioli F, de Nictolis M, Busso N, et al. PPARgamma expression in normal human placenta, hydatidiform mole and choriocarcinoma. Mol Hum Reprod. 2002;8(6):574–9.

Hewitt DP, Mark PJ, Waddell BJ. Placental expression of peroxisome proliferator-activated receptors in rat pregnancy and the effect of increased glucocorticoid exposure. Biol Reprod. 2006;74(1):23–8.

Alvino G, Cozzi V, Radaelli T, Ortega H, Herrera E, Cetin I. Maternal and fetal fatty acid profile in normal and intrauterine growth restriction pregnancies with and without preeclampsia. Pediatr Res. 2008;64(6):615–20.

Mattace Raso G, Bianco G, Esposito E, Iacono A, Meli R, Autore G. Evaluation of placental protein modifications in normotensive and spontaneously hypertensive rats. Placenta. 2008;29(5):429–35.

Waite LL, Louie RE, Taylor RN. Circulating activators of peroxisome proliferator-activated receptors are reduced in preeclamptic pregnancy. J Clin Endocrinol Metab. 2005;90(2):620–6.

Meher AP, Wadhwani N, Randhir K, Mehendale S, Wagh G, Joshi SR. Placental DHA and mRNA levels of PPARgamma and LXRalpha and their relationship to birth weight. Journal of clinical lipidology. 2016;10(4):767–74.

Larque E, Krauss-Etschmann S, Campoy C, et al. Docosahexaenoic acid supply in pregnancy affects placental expression of fatty acid transport proteins. Am J Clin Nutr. 2006;84(4):853–61.

O'Tierney-Ginn PF, Davina D, Gillingham M, Barker DJ, Morris C, Thornburg KL. Neonatal fatty acid profiles are correlated with infant growth measures at 6 months. J Dev Orig Health Dis. 2017:1–9.

O'Tierney-Ginn P, Roberts V, Gillingham M, Walker J, Glazebrook PA, Thornburg KL, et al. Influence of high fat diet and resveratrol supplementation on placental fatty acid uptake in the Japanese macaque. Placenta. 2015;36(8):903–10.

Zinkhan EK, Lang BY, Yu B, Wang Y, Jiang C, Fitzhugh M, et al. Maternal tobacco smoke increased visceral adiposity and serum corticosterone levels in adult male rat offspring. Pediatr Res. 2014;76(1):17–23.

Ino T, Shibuya T, Saito K, Inaba Y. Relationship between body mass index of offspring and maternal smoking during pregnancy. Int J Obes. 2012;36(4):554–8.

Hukkanen J, Jacob P 3rd, Benowitz NL. Metabolism and disposition kinetics of nicotine. Pharmacol Rev. 2005;57(1):79–115.

Albuquerque CA, Smith KR, Johnson C, Chao R, Harding R. Influence of maternal tobacco smoking during pregnancy on uterine, umbilical and fetal cerebral artery blood flows. Early Hum Dev. 2004;80(1):31–42.

Schneider CA, Rasband WS, Eliceiri KW. NIH image to ImageJ: 25 years of image analysis. Nat Methods. 2012;9(7):671–5.

Bagley HN, Wang Y, Campbell MS, Yu X, Lane RH, Joss-Moore LA. Maternal docosahexaenoic acid increases adiponectin and normalizes IUGR-induced changes in rat adipose deposition. J Obes. 2013;2013:312153.

Joss-Moore L, Carroll T, Yang Y, Fitzhugh M, Metcalfe D, Oman J, et al. Intrauterine growth restriction transiently delays alveolar formation and disrupts retinoic acid receptor expression in the lung of female rat pups. Pediatr Res. 2013;73(5):612–20.

Ke X, Xing B, Yu B, et al. IUGR disrupts the PPARgamma-Setd8-H4K20me and Wnt signaling pathways in the juvenile rat hippocampus. Int J Dev Neurosci. 2014;38c:59–67.

Louwagie EJ, Larsen TD, Wachal AL, Baack ML. Placental lipid processing in response to a maternal high-fat diet and diabetes in rats. Pediatr Res. 2018;83(3):712–22.

Singh AP, Singh N, Singh Bedi PM. Estrogen attenuates renal IRI through PPAR-gamma agonism in rats. J Surg Res. 2016;203(2):324–30.

Sato H, Sugai H, Kurosaki H, Ishikawa M, Funaki A, Kimura Y, et al. The effect of sex hormones on peroxisome proliferator-activated receptor gamma expression and activity in mature adipocytes. Biol Pharm Bull. 2013;36(4):564–73.

Park HJ, Choi JM. Sex-specific regulation of immune responses by PPARs. Exp Mol Med. 2017;49(8):e364.

Barker DJ, Thornburg KL. Placental programming of chronic diseases, cancer and lifespan: a review. Placenta. 2013;34(10):841–5.

Varvarigou AA, Asimakopoulou A, Beratis NG. Impact of maternal smoking on birth size: effect of parity and sex dimorphism. Neonatology. 2009;95(1):61–7.

Niu Z, Xie C, Wen X, et al. Placenta mediates the association between maternal second-hand smoke exposure during pregnancy and small for gestational age. Placenta. 2015;36(8):876–80.

Crane JM, Keough M, Murphy P, Burrage L, Hutchens D. Effects of environmental tobacco smoke on perinatal outcomes: a retrospective cohort study. BJOG : an international journal of obstetrics and gynaecology. 2011;118(7):865–71.

Varvarigou AA, Fouzas S, Beratis NG. Effect of prenatal tobacco smoke exposure on fetal growth potential. J Perinat Med. 2010;38(6):683–7.

Weng SF, Redsell SA, Nathan D, Swift JA, Yang M, Glazebrook C. Estimating overweight risk in childhood from predictors during infancy. Pediatrics. 2013;132(2):e414–21.

Oken E, Levitan EB, Gillman MW. Maternal smoking during pregnancy and child overweight: systematic review and meta-analysis. Int J Obes. 2008;32(2):201–10.

Grzeskowiak LE, Hodyl NA, Stark MJ, Morrison JL, Clifton VL. Association of early and late maternal smoking during pregnancy with offspring body mass index at 4 to 5 years of age. J Dev Orig Health Dis. 2015;6(6):485–92.

Albers L, von Kries R, Sobotzki C, Gao HJ, Buka SL, Clifton VL, et al. Differences in maternal smoking across successive pregnancies - dose-dependent relation to BMI z-score in the offspring: an individual patient data (IPD) meta-analysis. Obes Rev. 2018;19(9):1248–55.

Al Mamun A, Lawlor DA, Alati R, O'Callaghan MJ, Williams GM, Najman JM. Does maternal smoking during pregnancy have a direct effect on future offspring obesity? Evidence from a prospective birth cohort study. Am J Epidemiol. 2006;164(4):317–25.

Dior UP, Lawrence GM, Sitlani C, Enquobahrie D, Manor O, Siscovick DS, et al. Parental smoking during pregnancy and offspring cardio-metabolic risk factors at ages 17 and 32. Atherosclerosis. 2014;235(2):430–7.

O'Tierney-Ginn PF, Gillingham M, Fowler J, Brass E, Marshall NE, Thornburg KL. Maternal weight gain regulates omega-3 fatty acids in male, not female, neonates. Reproductive sciences (Thousand Oaks, Calif). 2017;24(4):560–7.

Cogollos L, Garcia-Contreras C, Vazquez-Gomez M, et al. Effects of fetal genotype and sex on developmental response to maternal malnutrition. Reprod Fertil Dev. 2017;29(6):1155–68.

Matorras R, Lopez De Larrucea A, Sanjurjo P, et al. Increased tissue concentrations of arachidonic acid in umbilical artery and placenta in fetal growth retardation. Acta Obstet Gynecol Scand. 2001;80(9):807–12.

Araya J, Rodrigo R, Videla LA, et al. Increase in long-chain polyunsaturated fatty acid n - 6/n - 3 ratio in relation to hepatic steatosis in patients with non-alcoholic fatty liver disease. Clinical science (London, England : 1979). 2004;106(6):635–43.

Karlsson M, Marild S, Brandberg J, Lonn L, Friberg P, Strandvik B. Serum phospholipid fatty acids, adipose tissue, and metabolic markers in obese adolescents. Obesity (Silver Spring). 2006;14(11):1931–9.

Valenzuela R, Videla LA. The importance of the long-chain polyunsaturated fatty acid n-6/n-3 ratio in development of non-alcoholic fatty liver associated with obesity. Food Funct. 2011;2(11):644–8.

Kalisch-Smith JI, Simmons DG, Dickinson H, Moritz KM. Review: sexual dimorphism in the formation, function and adaptation of the placenta. Placenta. 2017;54:10–6.

Rosenfeld CS. Sex-specific placental responses in fetal development. Endocrinology. 2015;156(10):3422–34.

Sedlmeier EM, Brunner S, Much D, et al. Human placental transcriptome shows sexually dimorphic gene expression and responsiveness to maternal dietary n-3 long-chain polyunsaturated fatty acid intervention during pregnancy. BMC Genomics. 2014;15:941.

Chen PY, Ganguly A, Rubbi L, Orozco LD, Morselli M, Ashraf D, et al. Intrauterine calorie restriction affects placental DNA methylation and gene expression. Physiol Genomics. 2013;45(14):565–76.

Clifton VL. Review: sex and the human placenta: mediating differential strategies of fetal growth and survival. Placenta. 2010;31(Suppl):S33–9.

Thornburg KL, Kolahi K, Pierce M, Valent A, Drake R, Louey S. Biological features of placental programming. Placenta. 2016;48(Suppl 1):S47–s53.

Osei-Kumah A, Smith R, Jurisica I, Caniggia I, Clifton VL. Sex-specific differences in placental global gene expression in pregnancies complicated by asthma. Placenta. 2011;32(8):570–8.

Lagiou P, Samoli E, Hsieh CC, Lagiou A, Xu B, Yu GP, et al. Maternal and cord blood hormones in relation to birth size. Eur J Epidemiol. 2014;29(5):343–51.

Miranda J, Triunfo S, Rodriguez-Lopez M, et al. Performance of third-trimester combined screening model for prediction of adverse perinatal outcome. Ultrasound Obstet Gynecol. 2017;50(3):353–60.

Lefterova MI, Haakonsson AK, Lazar MA, Mandrup S. PPARgamma and the global map of adipogenesis and beyond. Trends Endocrinol Metab. 2014;25(6):293–302.

Wakabayashi K, Okamura M, Tsutsumi S, Nishikawa NS, Tanaka T, Sakakibara I, et al. The peroxisome proliferator-activated receptor gamma/retinoid X receptor alpha heterodimer targets the histone modification enzyme PR-Set7/Setd8 gene and regulates adipogenesis through a positive feedback loop. Mol Cell Biol. 2009;29(13):3544–55.

Joss-Moore LA, Wang Y, Baack ML, Yao J, Norris AW, Yu X, et al. IUGR decreases PPARgamma and SETD8 expression in neonatal rat lung and these effects are ameliorated by maternal DHA supplementation. Early Hum Dev. 2010;86(12):785–91.

Chassen SS, Ferchaud-Roucher V, Gupta MB, Jansson T, Powell TL. Alterations in placental long chain polyunsaturated fatty acid metabolism in human intrauterine growth restriction. Clinical science (London, England : 1979). 2018;132(5):595–607.

Hirschmugl B, Desoye G, Catalano P, Klymiuk I, Scharnagl H, Payr S, et al. Maternal obesity modulates intracellular lipid turnover in the human term placenta. Int J Obes. 2017;41(2):317–23.

Lager S, Ramirez VI, Gaccioli F, Jang B, Jansson T, Powell TL. Protein expression of fatty acid transporter 2 is polarized to the trophoblast basal plasma membrane and increased in placentas from overweight/obese women. Placenta. 2016;40:60–6.

Maccani MA, Avissar-Whiting M, Banister CE, McGonnigal B, Padbury JF, Marsit CJ. Maternal cigarette smoking during pregnancy is associated with downregulation of miR-16, miR-21, and miR-146a in the placenta. Epigenetics. 2010;5(7):583–9.

Tsamou M, Martens DS, Cox B, Madhloum N, Vrijens K, Nawrot TS. Sex-specific associations between telomere length and candidate miRNA expression in placenta. J Transl Med. 2018;16(1):254.

Meakin AS, Saif Z, Jones AR, Aviles PFV, Clifton VL. Review: placental adaptations to the presence of maternal asthma during pregnancy. Placenta. 2017;54:17–23.

Biscetti F, Gaetani E, Flex A, Aprahamian T, Hopkins T, Straface G, et al. Selective activation of peroxisome proliferator-activated receptor (PPAR)alpha and PPAR gamma induces neoangiogenesis through a vascular endothelial growth factor-dependent mechanism. Diabetes. 2008;57(5):1394–404.

Garnier V, Traboulsi W, Salomon A, Brouillet S, Fournier T, Winkler C, et al. PPARgamma controls pregnancy outcome through activation of EG-VEGF: new insights into the mechanism of placental development. Am J Physiol Endocrinol Metab. 2015;309(4):E357–69.

Solleti SK, Simon DM, Srisuma S, Arikan MC, Bhattacharya S, Rangasamy T, et al. Airway epithelial cell PPARgamma modulates cigarette smoke-induced chemokine expression and emphysema susceptibility in mice. Am J Phys Lung Cell Mol Phys. 2015;309(3):L293–304.