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Fornes, R., Manti, M., Qi, X., Vorontsov, E., Sihlbom, C., Nyström, J., . . . Stener-Victorin, E. (2019). Mice exposed to maternal androgen excess and diet-induced obesity have altered phosphorylation of catechol-O-methyltransferase in the placenta and fetal liver. International Journal of Obesity
Open this publication in new window or tab >>Mice exposed to maternal androgen excess and diet-induced obesity have altered phosphorylation of catechol-O-methyltransferase in the placenta and fetal liver
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2019 (English)In: International Journal of Obesity, ISSN 0307-0565, E-ISSN 1476-5497Article in journal (Refereed) Epub ahead of print
Abstract [en]

Background/objectives: Maternal obesity together with androgen excess in mice negatively affects placental function and maternal and fetal liver function as demonstrated by increased triglyceride content with dysfunctional expression of enzymes and transcription factors involved in de novo lipogenesis and fat storage. To identify changes in molecular pathways that might promote diseases in adulthood, we performed a global proteomic analysis using a liquid-chromatography/mass-spectrometry system to investigate total and phosphorylated proteins in the placenta and fetal liver in a mouse model that combines maternal obesity with maternal androgen excess. Methods: After ten weeks on a control diet (CD) or high fat/high sugar-diet, dams were mated with males fed the CD. Between gestational day (GD) 16.5 and GD 18.5, mice were injected with vehicle or dihydrotestosterone (DHT) and sacrificed at GD 18.5 prior to dissection of the placentas and fetal livers. Four pools of female placentas and fetal livers were subjected to a global proteomic analysis. Total and phosphorylated proteins were filtered by ANOVA q < 0.05, and this was followed by two-way ANOVA to determine the effect of maternal obesity and/or androgen exposure. Results: In placenta, phosphorylated ATP-citrate synthase was decreased due to maternal obesity, and phosphorylated catechol-O-methyltransferase (COMT) was differentially expressed due to the interaction between maternal diet and DHT exposure. In fetal liver, five total proteins and 48 proteins phosphorylated in one or more sites, were differentially expressed due to maternal obesity or androgen excess. In fetal liver, phosphorylated COMT expression was higher in fetus exposed to maternal obesity. Conclusion: These results suggest a common regulatory mechanism of catecholamine metabolism in the placenta and the fetal liver as demonstrated by higher phosphorylated COMT expression in the placenta and fetal liver from animals exposed to diet-induced maternal obesity and lower expression of phosphorylated COMT in animals exposed to maternal androgen excess. © 2019, Springer Nature Limited.

Place, publisher, year, edition, pages
Nature Publishing Group, 2019
National Category
Physiology Basic Medicine
Research subject
Translational Medicine TRIM
Identifiers
urn:nbn:se:his:diva-16617 (URN)10.1038/s41366-018-0314-8 (DOI)30670847 (PubMedID)2-s2.0-85060511172 (Scopus ID)
Available from: 2019-02-11 Created: 2019-02-11 Last updated: 2019-07-05Bibliographically approved
Kokosar, M., Benrick, A., Perfilyev, A., Nilsson, E., Källman, T., Ohlsson, C., . . . Stener-Victorin, E. (2018). A Single Bout of Electroacupuncture Remodels Epigenetic and Transcriptional Changes in Adipose Tissue in Polycystic Ovary Syndrome. Scientific Reports, 8, Article ID 1878.
Open this publication in new window or tab >>A Single Bout of Electroacupuncture Remodels Epigenetic and Transcriptional Changes in Adipose Tissue in Polycystic Ovary Syndrome
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2018 (English)In: Scientific Reports, ISSN 2045-2322, E-ISSN 2045-2322, Vol. 8, article id 1878Article in journal (Refereed) Published
Abstract [en]

A single bout of electroacupuncture results in muscle contractions and increased whole body glucose uptake in women with polycystic ovary syndrome (PCOS). Women with PCOS have transcriptional and epigenetic alterations in the adipose tissue and we hypothesized that electroacupuncture induces epigenetic and transcriptional changes to restore metabolic alterations. Twenty-one women with PCOS received a single bout of electroacupuncture, which increased the whole body glucose uptake. In subcutaneous adipose tissue biopsies, we identified treatment-induced expression changes of 2369 genes (Q < 0.05) and DNA methylation changes of 7055 individual genes (Q = 0.11). The largest increase in expression was observed for FOSB (2405%), and the largest decrease for LOC100128899 (54%). The most enriched pathways included Acute phase response signaling and LXR/RXR activation. The DNA methylation changes ranged from 1-16%, and 407 methylation sites correlated with gene expression. Among genes known to be differentially expressed in PCOS, electroacupuncture reversed the expression of 80 genes, including PPAR gamma and ADIPOR2. Changes in the expression of Nr4 alpha 2 and Junb are reversed by adrenergic blockers in rats demonstrating that changes in gene expression, in part, is due to activation of the sympathetic nervous system. In conclusion, low-frequency electroacupuncture with muscle contractions remodels epigenetic and transcriptional changes that elicit metabolic improvement.

Place, publisher, year, edition, pages
Nature Publishing Group, 2018
National Category
Physiology
Research subject
Translational Medicine TRIM
Identifiers
urn:nbn:se:his:diva-14766 (URN)10.1038/s41598-017-17919-5 (DOI)000423508900049 ()29382850 (PubMedID)2-s2.0-85041298794 (Scopus ID)
Available from: 2018-02-22 Created: 2018-02-22 Last updated: 2019-09-30Bibliographically approved
Stener-Victorin, E., Benrick, A., Fornes, R. & Maliqueo, M. (2018). Acupuncture. In: Stefano Palomba (Ed.), Infertility in Women with Polycystic Ovary Syndrome: Pathogenesis and Management (pp. 227-245). Springer
Open this publication in new window or tab >>Acupuncture
2018 (English)In: Infertility in Women with Polycystic Ovary Syndrome: Pathogenesis and Management / [ed] Stefano Palomba, Springer, 2018, p. 227-245Chapter in book (Refereed)
Abstract [en]

Acupuncture involving insertion of thin sterile needles into the skin, muscles, and fibrous/fat tissues is a part of traditional Chinese medicine (TCM). Western medical acupuncture described in this chapter is an adaptation of Chinese acupuncture using current knowledge of anatomy, physiology, pathology, and evidence-based medicine, instead of using concepts such as meridiansyin/yang, and circulation of qi. This chapter describes the use of acupuncture in the treatment of women with polycystic ovary syndrome (PCOS) from a western medical approach including potential mechanism of action, experimental data as well as clinical data.

Place, publisher, year, edition, pages
Springer, 2018
Keywords
Acupuncture
National Category
Physiology
Identifiers
urn:nbn:se:his:diva-13218 (URN)10.1007/978-3-319-45534-1_17 (DOI)978-3-319-45534-1 (ISBN)978-3-319-45533-4 (ISBN)
Available from: 2016-12-09 Created: 2016-12-09 Last updated: 2018-05-29Bibliographically approved
Manti, M., Fornes, R., Qi, X., Folmerz, E., Lindén Hirschberg, A., de Castro Barbosa, T., . . . Stener-Victorin, E. (2018). Maternal androgen excess and obesity induce sexually dimorphic anxiety-like behavior in the offspring. The FASEB Journal, 32(8), 4158-4171
Open this publication in new window or tab >>Maternal androgen excess and obesity induce sexually dimorphic anxiety-like behavior in the offspring
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2018 (English)In: The FASEB Journal, ISSN 0892-6638, E-ISSN 1530-6860, Vol. 32, no 8, p. 4158-4171Article in journal (Refereed) Published
Abstract [en]

Maternal polycystic ovary syndrome (PCOS), a condition associated with hyperandrogenism, is suggested to increase anxiety-like behavior in the offspring. Because PCOS is closely linked to obesity, we investigated the impact of an adverse hormonal or metabolic maternal environment and offspring obesity on anxiety in the offspring. The obese PCOS phenotype was induced by chronic high-fat-high-sucrose (HFHS) consumption together with prenatal dihydrotestosterone exposure in mouse dams. Anxiety-like behavior was assessed in adult offspring with the elevated-plus maze and open-field tests. The influence of maternal androgens and maternal and offspring diet on genes implicated in anxiety were analyzed in the amygdala and hypothalamus with real-time PCR ( n = 47). Independent of diet, female offspring exposed to maternal androgens were more anxious and displayed up-regulation of adrenoceptor α 1B in the amygdala and up-regulation of hypothalamic corticotropin-releasing hormone ( Crh). By contrast, male offspring exposed to a HFHS maternal diet had increased anxiety-like behavior and showed up-regulation of epigenetic markers in the amygdala and up-regulation of hypothalamic Crh. Overall, there were substantial sex differences in gene expression in the brain. These findings provide novel insight into how maternal androgens and obesity exert sex-specific effects on behavior and gene expression in the offspring of a PCOS mouse model.-Manti, M., Fornes, R., Qi, X., Folmerz, E., Lindén Hirschberg, A., de Castro Barbosa, T., Maliqueo, M., Benrick, A., Stener-Victorin, E. Maternal androgen excess and obesity induce sexually dimorphic anxiety-like behavior in the offspring.

Keywords
amygdala, dihydrotestosterone, high-fat–high-sucrose, polycystic ovary syndrome
National Category
Physiology
Research subject
Translational Medicine TRIM
Identifiers
urn:nbn:se:his:diva-15092 (URN)10.1096/fj.201701263RR (DOI)000439325400009 ()29565738 (PubMedID)2-s2.0-85050872954 (Scopus ID)
Available from: 2018-04-23 Created: 2018-04-23 Last updated: 2018-08-30Bibliographically approved
Nilsson, E., Benrick, A., Kokosar, M., Krook, A., Lindgren, E., Källman, T., . . . Stener-Victorin, E. (2018). Transcriptional and Epigenetic Changes Influencing Skeletal Muscle Metabolism in Women With Polycystic Ovary Syndrome. Journal of Clinical Endocrinology and Metabolism, 103(12), 4465-4477
Open this publication in new window or tab >>Transcriptional and Epigenetic Changes Influencing Skeletal Muscle Metabolism in Women With Polycystic Ovary Syndrome
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2018 (English)In: Journal of Clinical Endocrinology and Metabolism, ISSN 0021-972X, E-ISSN 1945-7197, Vol. 103, no 12, p. 4465-4477Article in journal (Refereed) Published
Abstract [en]

Context: Insulin resistance in skeletal muscle is a major risk factor for the development of type 2 diabetes in women with polycystic ovary syndrome (PCOS). Despite this, the mechanisms underlying insulin resistance in PCOS are largely unknown. Objective: To investigate the genome-wide DNA methylation and gene expression patterns in skeletal muscle from women with PCOS and controls and relate them to phenotypic variations. Design/Participants: In a case-control study, skeletal muscle biopsies from women with PCOS (n = 17) and age-, weight-, and body mass index. matched controls (n = 14) were analyzed by array-based DNA methylation and mRNA expression profiling. Results: Eighty-five unique transcripts were differentially expressed in muscle from women with PCOS vs controls, including DYRK1A, SYNPO2, SCP2, and NAMPT. Furthermore, women with PCOS had reduced expression of genes involved in immune system pathways. Two CpG sites showed differential DNA methylation after correction for multiple testing. However, an mRNA expression of similar to 30% of the differentially expressed genes correlated with DNA methylation levels of CpG sites in or near the gene. Functional follow-up studies demonstrated that KLF10 is under transcriptional control of insulin, where insulin promotes glycogen accumulation in myotubes of human muscle cells. Testosterone downregulates the expression levels of COL1A1 and MAP2K6. Conclusion: PCOS is associated with aberrant skeletal muscle gene expression with dysregulated pathways. Furthermore, we identified specific changes in muscle DNA methylation that may affect gene expression. This study showed that women with PCOS have epigenetic and transcriptional changes in skeletal muscle that, in part, can explain the metabolic abnormalities seen in these women.

Place, publisher, year, edition, pages
Oxford University Press, 2018
National Category
Physiology
Research subject
Translational Medicine TRIM
Identifiers
urn:nbn:se:his:diva-16633 (URN)10.1210/jc.2018-00935 (DOI)000456138900017 ()30113663 (PubMedID)2-s2.0-85052910075 (Scopus ID)
Available from: 2019-02-15 Created: 2019-02-15 Last updated: 2019-05-09Bibliographically approved
Maliqueo, M., Benrick, A., Rodrigues Marcondes, R., Johansson, J., Sun, M. & Stener-Victorin, E. (2017). Acupuncture does not ameliorate metabolic disturbances in the P450 aromatase inhibitor-induced rat model of polycystic ovary syndrome. Experimental Physiology, 102(1), 113-127
Open this publication in new window or tab >>Acupuncture does not ameliorate metabolic disturbances in the P450 aromatase inhibitor-induced rat model of polycystic ovary syndrome
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2017 (English)In: Experimental Physiology, ISSN 0958-0670, E-ISSN 1469-445X, Vol. 102, no 1, p. 113-127Article in journal (Refereed) Published
Abstract [en]

Low-frequency electroacupuncture restores sex steroid synthesis and sympathetic activity in women with polycystic ovary syndrome, which may improve its metabolic disturbances likely by modulating sympathetic nerve activity or sex steroid synthesis. We investigated whether low-frequency electroacupuncture regulates the metabolic function to the same extent as treatment with estradiol or -adrenergic blocking in a rat model of polycystic ovary syndrome induced by a P450 aromatase inhibitor (letrozole). Letrozole (β00 μg per day) or placebo pellets were implanted in pre-pubertal Wistar rats. Six weeks thereafter, rats were treated for 5–6 weeks with: low-frequency electroacupuncture (5 days per week), a -adrenergic blocker (propranolol hydrochloride, 0.1 mg kg-1) (5 days per week), or 17-estradiol (β.0 μg) every fourth day. Body weight development, body composition, locomotor activity, insulin sensitivity, tissue specific glucose uptake, lipid profile, adipocyte size, adiponectin and insulin serum concentrations, and gene expression in inguinal fat were measured. All treatments increased circulating levels of LDL-cholesterol. Estradiol treatment restored locomotor activity and increased insulin sensitivity but did not modify the glucose uptake in muscle and fat. An upregulation of genes related to insulin sensitivity and downregulation of genes related to adipogenesis were observed in subcutaneous adipose tissue from rats exposed to letrozole. Only estradiol treatment normalized the expression of these genes. In conclusions, low-frequency electroacupuncture increased LDL-cholesterol without affecting the insulin sensitivity or adipose tissue function, which could suggest effects on hepatic lipid regulation probably mediated by estradiol action or -adrenergic pathway.

Keywords
Low-frequency electroacupuncture, polycystic ovary syndrome, insulin resistance
National Category
Physiology
Research subject
Medical sciences
Identifiers
urn:nbn:se:his:diva-13216 (URN)10.1113/EP085983 (DOI)000392492600011 ()27790765 (PubMedID)2-s2.0-85007560511 (Scopus ID)
Available from: 2016-12-09 Created: 2016-12-09 Last updated: 2018-01-13Bibliographically approved
Benrick, A., Chanclón, B., Micallef, P., Wu, Y., Hadi, L., Shelton, J. M., . . . Wernstedt Asterholm, I. (2017). Adiponectin protects against development of metabolic disturbances in a PCOS mouse model. Proceedings of the National Academy of Sciences of the United States of America, 114(34), E7187-E7196, Article ID 201708854.
Open this publication in new window or tab >>Adiponectin protects against development of metabolic disturbances in a PCOS mouse model
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2017 (English)In: Proceedings of the National Academy of Sciences of the United States of America, ISSN 0027-8424, E-ISSN 1091-6490, Vol. 114, no 34, p. E7187-E7196, article id 201708854Article in journal (Refereed) Published
Abstract [en]

Adiponectin, together with adipocyte size, is the strongest factor associated with insulin resistance in women with polycystic ovary syndrome (PCOS). This study investigates the causal relationship between adiponectin levels and metabolic and reproductive functions in PCOS. Prepubertal mice overexpressing adiponectin from adipose tissue (APNtg), adiponectin knockouts (APNko), and their wild-type (WT) littermate mice were continuously exposed to placebo or dihydrotestosterone (DHT) to induce PCOS-like traits. As expected, DHT exposure led to reproductive dysfunction, as judged by continuous anestrus, smaller ovaries with a decreased number of corpus luteum, and an increased number of cystic/atretic follicles. A two-way between-groups analysis showed that there was a significant main effect for DHT exposure, but not for genotype, indicating adiponectin does not influence follicle development. Adiponectin had, however, some protective effects on ovarian function. Similar to in many women with PCOS, DHT exposure led to reduced adiponectin levels, larger adipocyte size, and reduced insulin sensitivity in WTs. APNtg mice remained metabolically healthy despite DHT exposure, while APNko-DHT mice were even more insulin resistant than their DHT-exposed littermate WTs. DHT exposure also reduced the mRNA expression of genes involved in metabolic pathways in gonadal adipose tissue of WT and APNko, but this effect of DHT was not observed in APNtg mice. Moreover, APNtg-DHT mice displayed increased pancreatic mRNA levels of insulin receptors, Pdx1 and Igf1R, suggesting adiponectin stimulates beta cell viability/hyperplasia in the context of PCOS. In conclusion, adiponectin improves metabolic health but has only minor effects on reproductive functions in this PCOS-like mouse model.

Keywords
adipose tissue, insulin resistance, polycystic ovary syndrome
National Category
Physiology Basic Medicine Medical and Health Sciences
Research subject
Translational Medicine TRIM
Identifiers
urn:nbn:se:his:diva-13977 (URN)10.1073/pnas.1708854114 (DOI)000408095300019 ()2-s2.0-85027848679 (PubMedID)000408095300019 (Scopus ID)
Available from: 2017-08-11 Created: 2017-08-11 Last updated: 2018-01-13Bibliographically approved
Benrick, A., Kokosar, M., Hu, M., Larsson, M., Maliqueo, M., Marcondes, R. R., . . . Stener-Victorin, E. (2017). Autonomic nervous system activation mediates the increase in whole-body glucose uptake in response to electroacupuncture. The FASEB Journal, 31(8), 3288-3297
Open this publication in new window or tab >>Autonomic nervous system activation mediates the increase in whole-body glucose uptake in response to electroacupuncture
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2017 (English)In: The FASEB Journal, ISSN 0892-6638, E-ISSN 1530-6860, Vol. 31, no 8, p. 3288-3297Article in journal (Refereed) Published
Abstract [en]

A single bout of low-frequency electroacupuncture (EA) causing muscle contractions increases whole-body glucose uptake in insulin-resistant rats. We explored the underlying mechanism of this finding and whether it can be translated into clinical settings. Changes in glucose infusion rate (GIR) were measured by euglycemic-hyperinsulinemic clamp during and after 45 min of low-frequency EA in 21 overweight/obese women with polycystic ovary syndrome (PCOS) and 21 controls matched for age, weight, and body mass index (experiment 1) and in rats receiving autonomic receptor blockers (experiment 2). GIR was higher after EA in controls and women with PCOS. Plasma serotonin levels and homovanillic acid, markers of vagal activity, decreased in both controls and patients with PCOS. Adipose tissue expression of pro-nerve growth factor (proNGF) decreased, and the mature NGF/proNGF ratio increased after EA in PCOS, but not in controls, suggesting increased sympathetic-driven adipose tissue metabolism. Administration of alpha-/beta-adrenergic receptor blockers in rats blocked the increase in GIR in response to EA. Muscarinic and dopamine receptor antagonist also blocked the response but with slower onset. In conclusion, a single bout of EA increases whole-body glucose uptake by activation of the sympathetic and partly the parasympathetic nervous systems, which could have important clinical implications for the treatment of insulin resistance.

National Category
Physiology Basic Medicine Medical and Health Sciences
Research subject
Translational Medicine TRIM
Identifiers
urn:nbn:se:his:diva-13971 (URN)10.1096/fj.201601381R (DOI)000405932400009 ()28404742 (PubMedID)2-s2.0-85026825921 (Scopus ID)
Available from: 2017-08-10 Created: 2017-08-10 Last updated: 2018-01-13Bibliographically approved
Marcondes, R. R., Maliqueo, M., Fornes, R., Benrick, A., Hu, M., Ivarsson, N., . . . Stener-Victorin, E. (2017). Exercise differentially affects metabolic functions and white adipose tissue in female letrozole-and dihydrotestosterone-induced mouse models of polycystic ovary syndrome. Molecular and Cellular Endocrinology, 448, 66-76
Open this publication in new window or tab >>Exercise differentially affects metabolic functions and white adipose tissue in female letrozole-and dihydrotestosterone-induced mouse models of polycystic ovary syndrome
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2017 (English)In: Molecular and Cellular Endocrinology, ISSN 0303-7207, E-ISSN 1872-8057, Vol. 448, p. 66-76Article in journal (Refereed) Published
Abstract [en]

Here we hypothesized that exercise in dihydrotestosterone (DHT) or letrozole (LET)-induced polycystic ovary syndrome mouse models improves impaired insulin and glucose metabolism, adipose tissue morphology, and expression of genes related to adipogenesis, lipid metabolism, Notch pathway and browning in inguinal and mesenteric fat. DHT-exposed mice had increased body weight, increased number of large mesenteric adipocytes. LET-exposed mice displayed increased body weight and fat mass, decreased insulin sensitivity, increased frequency of small adipocytes and increased expression of genes related to lipolysis in mesenteric fat. In both models, exercise decreased fat mass and inguinal and mesenteric adipose tissue expression of Notch pathway genes, and restored altered mesenteric adipocytes morphology. In conclusion, exercise restored mesenteric adipocytes morphology in DHT- and LET-exposed mice, and insulin sensitivity and mesenteric expression of lipolysis-related genes in LET-exposed mice. Benefits could be explained by downregulation of Notch, and modulation of browning and lipolysis pathways in the adipose tissue. 

Place, publisher, year, edition, pages
Elsevier, 2017
Keywords
Polycystic ovary syndrome, Exercise, Adipose tissue
National Category
Medical and Health Sciences Basic Medicine Clinical Medicine
Research subject
Translational Medicine TRIM
Identifiers
urn:nbn:se:his:diva-13727 (URN)10.1016/j.mce.2017.03.025 (DOI)000401218000007 ()28344042 (PubMedID)2-s2.0-85016551867 (Scopus ID)
Available from: 2017-06-20 Created: 2017-06-20 Last updated: 2018-01-13Bibliographically approved
Fornes, R., Maliqueo, M., Hu, M., Hadi, L., Jimenez-Andrade, J. M., Ebefors, K., . . . Stener-Victorin, E. (2017). The effect of androgen excess on maternal metabolism, placental function and fetal growth in obese dams. Scientific Reports, 7, Article ID 8066.
Open this publication in new window or tab >>The effect of androgen excess on maternal metabolism, placental function and fetal growth in obese dams
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2017 (English)In: Scientific Reports, ISSN 2045-2322, E-ISSN 2045-2322, Vol. 7, article id 8066Article in journal (Refereed) Published
Abstract [en]

Pregnant women with polycystic ovary syndrome (PCOS) are often overweight or obese. To study the effects of maternal androgen excess in obese dams on metabolism, placental function and fetal growth, female C57Bl6J mice were fed a control (CD) or a high fat/high sucrose (HF/HS) diet for 4-10 weeks, and then mated. On gestational day (GD) 15.5-17.5, dams were injected with dihydrotestosterone (CD-DHT, HF/HS-DHT) or a vehicle (CD-Veh, HF/HS-Veh). HF/HS dams had higher fat content, both before mating and on GD18.5, with no difference in glucose homeostasis, whereas the insulin sensitivity was higher in DHT-exposed dams. Compared to the CD groups, the livers from HF/HS dams weighed more on GD18.5, the triglyceride content was higher, and there was a dysregulation of liver enzymes related to lipogenesis and higher mRNA expression of Fitm1. Fetuses from HF/HS-Veh dams had lower liver triglyceride content and mRNA expression of Srebf1c. Maternal DHT exposure, regardless of diet, decreased fetal liver Pparg mRNA expression and increased placental androgen receptor protein expression. Maternal diet-induced obesity, together with androgen excess, affects maternal and fetal liver function as demonstrated by increased triglyceride content and dysfunctional expression of enzymes and transcription factors involved in de novo lipogenesis and fat storage.

Place, publisher, year, edition, pages
Nature Publishing Group, 2017
National Category
Physiology
Research subject
Translational Medicine TRIM
Identifiers
urn:nbn:se:his:diva-14117 (URN)10.1038/s41598-017-08559-w (DOI)000407559800033 ()28808352 (PubMedID)2-s2.0-85051626292 (Scopus ID)
Available from: 2017-09-14 Created: 2017-09-14 Last updated: 2018-09-26Bibliographically approved
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