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Characterization of Visceral and Subcutaneous Adipose Tissue

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Characterization of Visceral and Subcutaneous Adipose Tissue J. Perinat. Med. 2016; 44(7): 813–835 Shali Mazaki-Tovi*, Adi L. Tarca, Edi Vaisbuch, Juan Pedro Kusanovic, Nandor Gabor Than, Tinnakorn Chaiworapongsa, Zhong Dong, Sonia S. Hassan and Roberto Romero* Characterization of visceral and subcutaneous adipose tissue transcriptome in pregnant women with and without spontaneous labor at term: implication of alternative splicing in the metabolic adaptations of adipose tissue to parturition DOI 10.1515/jpm-2015-0259 groups (unpaired analyses) and adipose tissue regions Received July 27, 2015. Accepted October 26, 2015. Previously (paired analyses). Selected genes were tested by quantita- published online March 19, 2016. tive reverse transcription-polymerase chain reaction. Abstract Results: Four hundred and eighty-two genes were differ- entially expressed between visceral and subcutaneous Objective: The aim of this study was to determine gene fat of pregnant women with spontaneous labor at term expression and splicing changes associated with par- (q-value < 0.1; fold change > 1.5). Biological processes turition and regions (visceral vs. subcutaneous) of the enriched in this comparison included tissue and vascu- adipose tissue of pregnant women. lature development as well as inflammatory and meta- Study design: The transcriptome of visceral and abdomi- bolic pathways. Differential splicing was found for 42 nal subcutaneous adipose tissue from pregnant women at genes [q-value < 0.1; differences in Finding Isoforms using term with (n = 15) and without (n = 25) spontaneous labor Robust Multichip Analysis scores > 2] between adipose was profiled with the Affymetrix GeneChip Human Exon tissue regions of women not in labor. Differential exon 1.0 ST array. Overall gene expression changes and the dif- usage associated with parturition was found for three ferential exon usage rate were compared between patient genes (LIMS1, HSPA5, and GSTK1) in subcutaneous tissues. *Corresponding authors: Shali Mazaki-Tovi, MD, Department of National Institutes of Health, Department of Health and Human Obstetrics and Gynecology, Sheba Medical Center, Tel Hashomer, Services, Bethesda, MD, and Detroit, MI, USA; Department of 52621 Israel, Tel.: (+972) 3-530-2169, Fax: (+972) 3-5302922, Obstetrics and Gynecology, School of Medicine, Pontificia Universidad E-mail: [email protected]; and Tel Aviv University, Tel Aviv, Católica de Chile, Santiago, Chile; and Center for Research and Israel; and Roberto Romero, MD, D(Med)Sci, Perinatology Research Innovation in Maternal-Fetal Medicine (CIMAF), Department of Branch, NICHD/NIH/ DHHS, Hutzel Women’s Hospital, Box No. 4, Obstetrics and Gynecology, Sótero del Río Hospital, Santiago, Chile 3990 John R, Detroit, MI 48201, USA, Tel.: (+313) 993-2700, Nandor Gabor Than: Perinatology Research Branch, Eunice Fax: (+313) 993-2694, E-mail: [email protected]; Kennedy Shriver National Institute of Child Health and Human Department of Obstetrics and Gynecology, University of Michigan, Development, National Institutes of Health, Department of Health Ann Arbor, MI, USA; Department of Biostatistics and Epidemiology, and Human Services, Bethesda, MD, and Detroit, MI, USA; Institute Michigan State University, East Lansing, MI, USA; and Center for of Enzymology, Momentum Research Group, Research Centre for Molecular Medicine and Genetics, Wayne State University, Detroit, Natural Sciences, Hungarian Academy of Sciences, Budapest, MI, USA Hungary; and First Department of Pathology and Experimental Adi L. Tarca: Perinatology Research Branch, Eunice Kennedy Shriver Cancer Research, Semmelweis University, Budapest, Hungary National Institute of Child Health and Human Development, National Tinnakorn Chaiworapongsa and Sonia S. Hassan: Perinatology Institutes of Health, Department of Health and Human Services, Research Branch, Eunice Kennedy Shriver National Institute of Child Bethesda, MD, and Detroit, MI, USA; Department of Computer Health and Human Development, National Institutes of Health, Science, Wayne State University, Detroit, MI, USA; and Department Department of Health and Human Services, Bethesda, MD, and of Obstetrics and Gynecology, Wayne State University School of Detroit, MI, USA; and Department of Obstetrics and Gynecology, Medicine, Detroit, MI, USA Wayne State University School of Medicine, Detroit, MI, USA Edi Vaisbuch: Department of Obstetrics and Gynecology, Kaplan Zhong Dong: Perinatology Research Branch, Eunice Kennedy Shriver Medical Center, Rehovot, Israel National Institute of Child Health and Human Development, National Juan Pedro Kusanovic: Perinatology Research Branch, Eunice Kennedy Institutes of Health, Department of Health and Human Services, Shriver National Institute of Child Health and Human Development, Bethesda, MD, and Detroit, MI, USA 814 Mazaki-Tovi et al., Visceral and subcutaneous adipose tissue transcriptome in labor Conclusion: We show for the first time evidence of impli- well-established association between obesity and these cation of mRNA splicing and processing machinery in the complications of pregnancy [84–113]. subcutaneous adipose tissue of women in labor compared It has been suggested that the implication of adipose to those without labor. tissue in physiological or pathological processes should take into account the region-specific differences between Keywords: Adipokines; delivery; fat depots; gestation; high fat depots. Particularly, differences in function [114–116], dimensional biology; metabolism; obesity; pregnancy. gene expression [115, 117–144], and metabolic effect [145– 150] between the visceral and subcutaneous adipose tissue are to be considered. Indeed, regional variations Introduction of adipose tissue in specific genes were reported in non- pregnant individuals using both high throughput tech- Parturition imposes an increased energy demand on the niques [131–133, 136, 151] and targeted approaches [115, laboring woman. Labor is characterized by increased con- 116, 131, 133, 152–166]. Overall gene expression in the centrations of nutrients including glucose [1–5], free fatty adipose tissue of pregnant women has been previously acids [3, 6], ketone bodies [7], and lactic acid [8]. There is reported [32, 117–123, 167–178]; however, adipose tissue an approximate three-fold increase in whole body glucose gene expression, biological processes, molecular func- utilization during labor and delivery and, as expected, tions, and pathways associated with spontaneous term energy expenditure of the parturient women in the second parturition have not been described. Furthermore, to our stage of labor is 40% higher compared to the first stage knowledge, exon-level changes that can inform on alter- [9]. Additional support for the metabolic burden of labor native promoter usage, alternative splicing, and alterna- can also be found in the examination of myometrial gly- tive transcript termination [179] between the visceral and cogen storage, which is significantly increased at term subcutaneous regions have not been reported in either fat [10], but almost completely depleted during labor [11]. or other tissue of parturient women. Consistent with these findings, examination of the human We undertook this study in order to characterize myometrial transcriptome revealed that biological pro- the transcriptome of human visceral and subcutane- cesses related to metabolism were among the molecular ous adipose tissue during normal labor at term to gain functions enriched in the differentially expressed genes understanding of the global changes in gene expression between pregnant women with and without spontaneous and splicing associated with adiposity using an unbiased term labor [12]. approach. The aims of this study were: 1) to determine dif- The conventional view is that the energy expenditure ferences in visceral and subcutaneous gene expression of labor and delivery is equivalent to that of moderate exer- between pregnant women with and without spontaneous cise [1, 9] and that similar mechanisms (e.g. insulin and labor at term; 2) to determine regional variations in the non-insulin dependent glucose uptake, enhanced hepatic transcriptome of adipose tissue of patients with spontane- gluconeogenesis, and direct sympathetic nervous system ous labor at term; and 3) to identify depot-specific alter- stimulation) govern the metabolic adaptation to parturi- native splicing alterations in the adipose tissue of women tion [9, 13, 14]. However, whether or not adipose tissue, the with spontaneous labor at term. major energy reservoir, is affected by labor and delivery is still unknown. Assessment of the putative role of adipose tissue in human parturition may be of special importance Materials and methods considering the large body of evidence indicating that this endocrinal organ is powerful [15] and exerts auto- Study groups crine, paracrine and endocrine effects by the production and secretion of highly active peptides and proteins col- A prospective study was performed in which visceral and subcutane- lectively termed adipokines [16]. Importantly, adipokines ous adipose tissue samples were obtained from women undergoing have been implicated in physiological adaptations of cesarean section at term ( ≥ 37 weeks) in the following groups: 1) not normal gestation [17–28] as well as in the pathophysiology in labor (n = 25) and 2) spontaneous labor (n = 15). of preeclampsia [21, 29–50], gestational diabetes mellitus The inclusion criteria for both groups were as follows: 1) absence [51–65], preterm birth [66–68], delivery of large-for-gesta- of medical
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