RNA-seq analysis of the rat placentation site reveals maternal obesity-associated changes in placental and offspring thyroid hormone signaling

Placenta

Volumn 35, Issue 12, 2014, Pages 1013-1020

  Saben, J ^a,b,c   Kang, P ^a,b   Zhong, Y ^a,b   Thakali, K M ^a,b   Gomez Acevedo, H ^a,b   Borengasser, S J ^a,b   Andres, A ^a,b   Badger, T M ^a,b   Shankar, K ^a,b  

^a UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^b UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Metabolism; Obesity; Placenta; RNA seq; Thyroid hormone; Uncoupling proteins

Indexed keywords

APOLIPOPROTEIN B100; APOLIPOPROTEIN C2; BETA2 GLYCOPROTEIN 1; DEIODINASE 1; DEIODINASE 2; DEIODINASE 3; EARLY GROWTH RESPONSE FACTOR 1; FATTY ACID BINDING PROTEIN; LEPTIN; MALATE DEHYDROGENASE (DECARBOXYLATING); MATRIX METALLOPROTEINASE; MESSENGER RNA; MICROSOMAL TRIGLYCERIDE TRANSFER PROTEIN; MYELIN BASIC PROTEIN; NOGGIN; PALMITOYL COENZYME A HYDROLASE; PROTIRELIN; SECRETED FRIZZLED RELATED PROTEIN 4; SECRETED FRIZZLED RELATED PROTEIN 5; THYROID HORMONE; THYROID HORMONE RECEPTOR ALPHA; THYROID HORMONE RECEPTOR BETA; THYROTROPIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; UNCOUPLING PROTEIN 1; UNCOUPLING PROTEIN 2; UNCOUPLING PROTEIN 3; TRANSCRIPTOME;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; ENERGY METABOLISM; FAT MASS; FATTY ACID METABOLISM; FEMALE; FETUS; FETUS LIVER; GENE EXPRESSION; HUMAN; HUMAN CELL; LIPID METABOLISM; MALE; MATERNAL OBESITY; NONHUMAN; OXIDATIVE STRESS; PLACENTA LOCALIZATION; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REPRODUCTION; RNA ANALYSIS; RNA SEQUENCE; SIGNAL TRANSDUCTION; ANIMAL; GENE EXPRESSION PROFILING; GENETICS; LIVER; MATERNAL NUTRITION; METABOLISM; OBESITY; PHYSIOLOGY; PLACENTA; PREGNANCY; SPRAGUE DAWLEY RAT;

ANIMALS; FEMALE; GENE EXPRESSION PROFILING; HUMANS; LIVER; MATERNAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; OBESITY; PLACENTA; PLACENTATION; PREGNANCY; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; THYROID HORMONES; TRANSCRIPTOME;

EID: 84922328954     PISSN: 01434004     EISSN: 15323102     Source Type: Journal    
DOI: 10.1016/j.placenta.2014.09.015     Document Type: Article

References (42)

1. Shankar K, Harrell A, Liu X, Gilchrist JM, Ronis MJ, Badger TM. Maternal obesity at conception programs obesity in the offspring. Am J Physiol Regul Integr Comp Physiol 2008;294:R528-38.
2. Shankar K, Kang P, Harrell A, Zhong Y, Marecki JC, Ronis MJ, et al. Maternal overweight programs insulin and adiponectin signaling in the offspring. Endocrinology 2010;151:2577-89.
3. Shankar K, Zhong Y, Kang P, Lau F, Blackburn ML, Chen JR, et al. Maternal obesity promotes a proinflammatory signature in rat uterus and blastocyst. Endocrinology 2011;152:4158-70.
4. Borengasser SJ, Zhong Y, Kang P, Lindsey F, Ronis MJ, Badger TM, et al. Maternal obesity enhances white adipose tissue differentiation and alters genome-scale DNA methylation in male rat offspring. Endocrinology 2013;154:4113-25.
5. Borengasser SJ, Lau F, Kang P, Blackburn ML, Ronis MJ, Badger TM, et al. Maternal obesity during gestation impairs fatty acid oxidation and mitochondrial SIRT3 expression in rat offspring at weaning. PLoS One 2011;6:e24068.
6. Borengasser SJ, Kang P, Faske J, Gomez-Acevedo H, Blackburn ML, Badger TM, et al. High fat diet and in utero exposure to maternal obesity disrupts circadian rhythm and leads to metabolic programming of liver in rat offspring. PLoS One 2014;9:e84209.
7. Cross JC. Placental function in development and disease. Reprod Fertil Dev 2006;18:71-6.
8. Maltepe E, Bakardjiev AI, Fisher SJ. The placenta: transcriptional, epigenetic, and physiological integration during development. J Clin Invest 2010;120:1016-25.
9. Ain R, Canham LN, Soares MJ. Gestation stage-dependent intrauterine trophoblast cell invasion in the rat and mouse: novel endocrine phenotype and regulation. Dev Biol 2003;260:176-90.
10. Shankar K, Zhong Y, Kang P, Blackburn ML, Soares MJ, Badger TM, et al. RNA-seq analysis of the functional compartments within the rat placentation site. Endocrinology 2012;153:1999-2011.
11. Shankar K, Harrell A, Kang P, Singhal R, Ronis MJ, Badger TM. Carbohydrate responsive gene expression in the adipose tissue of rats. Endocrinology 2009;151:153-64.
12. Ain R, Konno T, Canham LN, Soares MJ. Phenotypic analysis of the rat placenta. Methods Mol Med 2006;121:295-313.
13. Saben J, Lindsey F, Zhong Y, Thakali K, Badger TM, Andres A, et al. Maternal obesity is associated with a lipotoxic placental environment. Placenta 2014;35:171-7.
14. Saben J, Zhong Y, McKelvey S, Dajani NK, Andres A, Badger TM, et al. A comprehensive analysis of the human placenta transcriptome. Placenta 2013;35:125-31.
15. Audic S, Claverie JM. The significance of digital gene expression profiles. Genome Res 1997;7:986-95.
16. Eden E, Navon R, Steinfeld I, Lipson D, Yakhini Z. GOrilla: a tool for discovery and visualization of enriched GO terms in ranked gene lists. BMC Bioinforma 2009;10:48.
17. Saben J, Zhong Y, Gomez-Acevedo H, Thakali KM, Borengasser SJ, Andres A, et al. Early growth response protein-1 mediates lipotoxicity-associated placental inflammation: role in maternal obesity. Am J Physiol Endocrinol Metab 2013;305:E1-14.
18. de Jonge HJ, Fehrman RS, de Bont ES, Hofstra RM, Gerbens F, Kamps WA, et al. Evidence based selection of housekeeping genes. PLoS One 2007;2:e898.
19. Ainge H, Thompson C, Ozanne SE, Rooney KB. A systematic review on animal models of maternal high fat feeding and offspring glycaemic control. Int J Obes (Lond) 2011;35:325-35.
20. Alfaradhi MZ, Ozanne SE. Developmental programming in response to maternal overnutrition. Front Genet 2011;2:27.
21. Samuelsson AM, Matthews PA, Argenton M, Christie MR, McConnell JM, Jansen EH, et al. Diet-induced obesity in female mice leads to offspring hyperphagia, adiposity, hypertension, and insulin resistance: a novel murine model of developmental programming. Hypertension 2008;51:383-92.
22. Nathanielsz PW, Poston L, Taylor PD. In utero exposure to maternal obesity and diabetes: animal models that identify and characterize implications for future health. Clin Perinatol 2007;34:515-26 [v].
23. Heerwagen MJ, Stewart MS, de la Houssaye BA, Janssen RC, Friedman JE. Transgenic increase in N-3/n-6 fatty acid ratio reduces maternal obesityassociated inflammation and limits adverse developmental programming in mice. PLoS One 2013;8:e67791.
24. Basu S, Haghiac M, Surace P, Challier JC, Guerre-Millo M, Singh K, et al. Pregravid obesity associates with increased maternal endotoxemia and metabolic inflammation. Obes Silver Spring 2011;19:476-82.
25. Basu S, Leahy P, Challier JC, Minium J, Catalano P, Hauguel-de Mouzon S. Molecular phenotype of monocytes at the maternal-fetal interface. Am J Obstet Gynecol 2011;205:265-8.
26. Challier JC, Basu S, Bintein T, Minium J, Hotmire K, Catalano PM, et al. Obesity in pregnancy stimulates macrophage accumulation and inflammation in the placenta. Placenta 2008;29:274-81.
27. Farley D, Tejero ME, Comuzzie AG, Higgins PB, Cox L, Werner SL, et al. Fetoplacental adaptations to maternal obesity in the baboon. Placenta 2009;30: 752-60.
28. Roberts KA, Riley SC, Reynolds RM, Barr S, Evans M, Statham A, et al. Placental structure and inflammation in pregnancies associated with obesity. Placenta 2011;32:247-54.
29. Mark PJ, Sisali C, Connor K, Patel R, Lewis JL, Vickers MH, et al. A maternal high-fat diet in rat pregnancy reduces growth of the fetus and the placental junctional zone, but not placental labyrinth zone growth. J Dev Orig Health Dis 2011;2:63-70.
30. Lichtner B, Knaus P, Lehrach H, Adjaye J. BMP10 as a potent inducer of trophoblast differentiation in human embryonic and induced pluripotent stem cells. Biomaterials 2013;34:9789-802.
31. Knofler M, Pollheimer J. Human placental trophoblast invasion and differentiation: a particular focus on Wnt signaling. Front Genet 2013;4:190.
32. Suter MA, Sangi-Haghpeykar H, Showalter L, Shope C, Hu M, Brown K, et al. Maternal high-fat diet modulates the fetal thyroid axis and thyroid gene expression in a nonhuman primate model. Mol Endocrinol 2012;26:2071-80.
33. Williams GR, Bassett JH. Deiodinases: the balance of thyroid hormone: local control of thyroid hormone action: role of type 2 deiodinase. J Endocrinol 2011;209:261-72.
34. Franco JG, Fernandes TP, Rocha CP, Calvino C, Pazos-Moura CC, Lisboa PC, et al. Maternal high-fat diet induces obesity and adrenal and thyroid dysfunction in male rat offspring at weaning. J Physiol 2012;590:5503-18.
35. Chan SY, Vasilopoulou E, Kilby MD. The role of the placenta in thyroid hormone delivery to the fetus. Nat Clin Pract Endocrinol Metab 2009;5:45-54.
36. Vasilopoulou E, Loubiere LS, Heuer H, Trajkovic-Arsic M, Darras VM, Visser TJ, et al. Monocarboxylate transporter 8 modulates the viability and invasive capacity of human placental cells and fetoplacental growth in mice. PLoS One 2013;8:e65402.
37. Canettieri G, Franchi A, Guardia MD, Moranette I, Santaguida MG, Harney JW, et al. Activation of thyroid hormone is transcriptionally regulated by epidermal growth factor in human placenta-derived JEG3 cells. Endocrinology 2008;149:695-702.
38. Patel J, Landers K, Li H, Mortimer RH, Richard K. Delivery of maternal thyroid hormones to the fetus. Trends Endocrinol Metab 2011;22:164-70.
39. Bajoria R, Babawale M. Ontogeny of endogenous secretion of immunoreactive-thyrotropin releasing hormone by the human placenta. J Clin Endocrinol Metab 1998;83:4148-55.
40. Huo L, Munzberg H, Nillni EA, Bjorbaek C. Role of signal transducer and activator of transcription 3 in regulation of hypothalamic trh gene expression by leptin. Endocrinology 2004;145:2516-23.
41. von Versen-Hoynck F, Rajakumar A, Parrott MS, Powers RW. Leptin affects system A amino acid transport activity in the human placenta: evidence for STAT3 dependent mechanisms. Placenta 2009;30:361-7.
42. Tessier DR, Ferraro ZM, Gruslin A. Role of leptin in pregnancy: consequences of maternal obesity. Placenta 2013;34:205-11.