Developmental exposure to indoor flame retardants and hypothalamic molecular signatures: Sex-dependent reprogramming of lipid homeostasis
Polybrominated diphenyl ethers (PBDEs) are a class of flame-retardant organohalogen pollutants that act as endocrine/neuroendocrine disrupting chemicals (EDCs). In humans, exposure to brominated flame retardants (BFR) or other environmentally persistent organic pollutants (POPs) such as polychlorina...
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Published in | Frontiers in endocrinology (Lausanne) Vol. 13; p. 997304 |
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Main Authors | , , , , , , , , , , , , |
Format | Journal Article |
Language | English |
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Frontiers Media S.A
30.09.2022
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Abstract | Polybrominated diphenyl ethers (PBDEs) are a class of flame-retardant organohalogen pollutants that act as endocrine/neuroendocrine disrupting chemicals (EDCs). In humans, exposure to brominated flame retardants (BFR) or other environmentally persistent organic pollutants (POPs) such as polychlorinated biphenyls (PCBs) and novel organophosphate flame retardants has been associated with increasing trends of diabetes and metabolic disease. However, the effects of PBDEs on metabolic processes and their associated sex-dependent features are poorly understood. The metabolic-disrupting effects of perinatal exposure to industrial penta-PBDE mixture, DE-71, on male and female progeny of C57BL/6N mouse dams were examined in adulthood. Dams were exposed to environmentally relevant doses of PBDEs daily for 10 weeks (
): 0.1 (L-DE-71) and 0.4 mg/kg/d (H-DE-71) and offspring parameters were compared to corn oil vehicle controls (VEH/CON). The following lipid metabolism indices were measured: plasma cholesterol, triglycerides, adiponectin, leptin, and liver lipids. L-DE-71 female offspring were particularly affected, showing hypercholesterolemia, elevated liver lipids and fasting plasma leptin as compared to same-sex VEH/CON, while L- and H-DE-71 male F1 only showed reduced plasma adiponectin. Using the quantitative Folch method, we found that mean liver lipid content was significantly elevated in L-DE-71 female offspring compared to controls. Oil Red O staining revealed fatty liver in female offspring and dams. General measures of adiposity, body weight, white and brown adipose tissue (BAT), and lean and fat mass were weighed or measured using EchoMRI. DE-71 did not produce abnormal adiposity, but decreased BAT depots in L-DE-71 females and males relative to same-sex VEH/CON. To begin to address potential central mechanisms of deregulated lipid metabolism, we used RT-qPCR to quantitate expression of hypothalamic genes in energy-regulating circuits that control lipid homeostasis. Both doses of DE-71 sex-dependently downregulated hypothalamic expression of
,
,
,
,
in female offspring while H-DE-71 downregulated
in exposed females relative to VEH/CON. In contrast, exposed male offspring displayed upregulated
and
. Intestinal barrier integrity was measured using FITC-dextran since it can lead to systemic inflammation that leads to liver damage and metabolic disease, but was not affected by DE-71 exposure. These findings indicate that maternal transfer of PBDEs disproportionately endangers female offspring to lipid metabolic reprogramming that may exaggerate risk for adult metabolic disease. |
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AbstractList | Polybrominated diphenyl ethers (PBDEs) are a class of flame-retardant organohalogen pollutants that act as endocrine/neuroendocrine disrupting chemicals (EDCs). In humans, exposure to brominated flame retardants (BFR) or other environmentally persistent organic pollutants (POPs) such as polychlorinated biphenyls (PCBs) and novel organophosphate flame retardants has been associated with increasing trends of diabetes and metabolic disease. However, the effects of PBDEs on metabolic processes and their associated sex-dependent features are poorly understood. The metabolic-disrupting effects of perinatal exposure to industrial penta-PBDE mixture, DE-71, on male and female progeny of C57BL/6N mouse dams were examined in adulthood. Dams were exposed to environmentally relevant doses of PBDEs daily for 10 weeks (p.o.): 0.1 (L-DE-71) and 0.4 mg/kg/d (H-DE-71) and offspring parameters were compared to corn oil vehicle controls (VEH/CON). The following lipid metabolism indices were measured: plasma cholesterol, triglycerides, adiponectin, leptin, and liver lipids. L-DE-71 female offspring were particularly affected, showing hypercholesterolemia, elevated liver lipids and fasting plasma leptin as compared to same-sex VEH/CON, while L- and H-DE-71 male F1 only showed reduced plasma adiponectin. Using the quantitative Folch method, we found that mean liver lipid content was significantly elevated in L-DE-71 female offspring compared to controls. Oil Red O staining revealed fatty liver in female offspring and dams. General measures of adiposity, body weight, white and brown adipose tissue (BAT), and lean and fat mass were weighed or measured using EchoMRI. DE-71 did not produce abnormal adiposity, but decreased BAT depots in L-DE-71 females and males relative to same-sex VEH/CON. To begin to address potential central mechanisms of deregulated lipid metabolism, we used RT-qPCR to quantitate expression of hypothalamic genes in energy-regulating circuits that control lipid homeostasis. Both doses of DE-71 sex-dependently downregulated hypothalamic expression of Lepr, Stat3, Mc4r, Agrp, Gshr in female offspring while H-DE-71 downregulated Npy in exposed females relative to VEH/CON. In contrast, exposed male offspring displayed upregulated Stat3 and Mc4r. Intestinal barrier integrity was measured using FITC-dextran since it can lead to systemic inflammation that leads to liver damage and metabolic disease, but was not affected by DE-71 exposure. These findings indicate that maternal transfer of PBDEs disproportionately endangers female offspring to lipid metabolic reprogramming that may exaggerate risk for adult metabolic disease. Polybrominated diphenyl ethers (PBDEs) are a class of flame-retardant organohalogen pollutants that act as endocrine/neuroendocrine disrupting chemicals (EDCs). In humans, exposure to brominated flame retardants (BFR) or other environmentally persistent organic pollutants (POPs) such as polychlorinated biphenyls (PCBs) and novel organophosphate flame retardants has been associated with increasing trends of diabetes and metabolic disease. However, the effects of PBDEs on metabolic processes and their associated sex-dependent features are poorly understood. The metabolic-disrupting effects of perinatal exposure to industrial penta-PBDE mixture, DE-71, on male and female progeny of C57BL/6N mouse dams were examined in adulthood. Dams were exposed to environmentally relevant doses of PBDEs daily for 10 weeks ( p.o. ): 0.1 (L-DE-71) and 0.4 mg/kg/d (H-DE-71) and offspring parameters were compared to corn oil vehicle controls (VEH/CON). The following lipid metabolism indices were measured: plasma cholesterol, triglycerides, adiponectin, leptin, and liver lipids. L-DE-71 female offspring were particularly affected, showing hypercholesterolemia, elevated liver lipids and fasting plasma leptin as compared to same-sex VEH/CON, while L- and H-DE-71 male F1 only showed reduced plasma adiponectin. Using the quantitative Folch method, we found that mean liver lipid content was significantly elevated in L-DE-71 female offspring compared to controls. Oil Red O staining revealed fatty liver in female offspring and dams. General measures of adiposity, body weight, white and brown adipose tissue (BAT), and lean and fat mass were weighed or measured using EchoMRI. DE-71 did not produce abnormal adiposity, but decreased BAT depots in L-DE-71 females and males relative to same-sex VEH/CON. To begin to address potential central mechanisms of deregulated lipid metabolism, we used RT-qPCR to quantitate expression of hypothalamic genes in energy-regulating circuits that control lipid homeostasis. Both doses of DE-71 sex-dependently downregulated hypothalamic expression of Lepr , Stat3 , Mc4r , Agrp , Gshr in female offspring while H-DE-71 downregulated Npy in exposed females relative to VEH/CON. In contrast, exposed male offspring displayed upregulated Stat3 and Mc4r . Intestinal barrier integrity was measured using FITC-dextran since it can lead to systemic inflammation that leads to liver damage and metabolic disease, but was not affected by DE-71 exposure. These findings indicate that maternal transfer of PBDEs disproportionately endangers female offspring to lipid metabolic reprogramming that may exaggerate risk for adult metabolic disease. Polybrominated diphenyl ethers (PBDEs) are a class of flame-retardant organohalogen pollutants that act as endocrine/neuroendocrine disrupting chemicals (EDCs). In humans, exposure to brominated flame retardants (BFR) or other environmentally persistent organic pollutants (POPs) such as polychlorinated biphenyls (PCBs) and novel organophosphate flame retardants has been associated with increasing trends of diabetes and metabolic disease. However, the effects of PBDEs on metabolic processes and their associated sex-dependent features are poorly understood. The metabolic-disrupting effects of perinatal exposure to industrial penta-PBDE mixture, DE-71, on male and female progeny of C57BL/6N mouse dams were examined in adulthood. Dams were exposed to environmentally relevant doses of PBDEs daily for 10 weeks ( ): 0.1 (L-DE-71) and 0.4 mg/kg/d (H-DE-71) and offspring parameters were compared to corn oil vehicle controls (VEH/CON). The following lipid metabolism indices were measured: plasma cholesterol, triglycerides, adiponectin, leptin, and liver lipids. L-DE-71 female offspring were particularly affected, showing hypercholesterolemia, elevated liver lipids and fasting plasma leptin as compared to same-sex VEH/CON, while L- and H-DE-71 male F1 only showed reduced plasma adiponectin. Using the quantitative Folch method, we found that mean liver lipid content was significantly elevated in L-DE-71 female offspring compared to controls. Oil Red O staining revealed fatty liver in female offspring and dams. General measures of adiposity, body weight, white and brown adipose tissue (BAT), and lean and fat mass were weighed or measured using EchoMRI. DE-71 did not produce abnormal adiposity, but decreased BAT depots in L-DE-71 females and males relative to same-sex VEH/CON. To begin to address potential central mechanisms of deregulated lipid metabolism, we used RT-qPCR to quantitate expression of hypothalamic genes in energy-regulating circuits that control lipid homeostasis. Both doses of DE-71 sex-dependently downregulated hypothalamic expression of , , , , in female offspring while H-DE-71 downregulated in exposed females relative to VEH/CON. In contrast, exposed male offspring displayed upregulated and . Intestinal barrier integrity was measured using FITC-dextran since it can lead to systemic inflammation that leads to liver damage and metabolic disease, but was not affected by DE-71 exposure. These findings indicate that maternal transfer of PBDEs disproportionately endangers female offspring to lipid metabolic reprogramming that may exaggerate risk for adult metabolic disease. |
Author | Chinthirla, Bhuvaneswari D Truong, Edward DiPatrizio, Nicholas V Bishay, Anthony E Valdez, Matthew C Deol, Poonamjot Kozlova, Elena V Denys, Maximillian E Enriquez, Dave Martins-Green, Manuela Benedum, Jonathan Curras-Collazo, Margarita C Krum, Julia M |
AuthorAffiliation | 2 Neuroscience Graduate Program, University of California, Riverside , Riverside, CA , United States 3 Biomedical Sciences, School of Medicine, University of California, Riverside , Riverside, CA , United States 1 Department of Molecular, Cell & Systems Biology, University of California, Riverside , Riverside, CA , United States |
AuthorAffiliation_xml | – name: 1 Department of Molecular, Cell & Systems Biology, University of California, Riverside , Riverside, CA , United States – name: 2 Neuroscience Graduate Program, University of California, Riverside , Riverside, CA , United States – name: 3 Biomedical Sciences, School of Medicine, University of California, Riverside , Riverside, CA , United States |
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CitedBy_id | crossref_primary_10_1093_toxsci_kfae047 crossref_primary_10_3390_antiox12101804 crossref_primary_10_1016_j_fbio_2024_103777 crossref_primary_10_1016_j_envpol_2024_123966 crossref_primary_10_7717_peerj_15639 crossref_primary_10_3389_fendo_2023_1049708 crossref_primary_10_1093_toxsci_kfad056 |
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Copyright | Copyright © 2022 Kozlova, Denys, Benedum, Valdez, Enriquez, Bishay, Chinthirla, Truong, Krum, DiPatrizio, Deol, Martins-Green and Curras-Collazo. Copyright © 2022 Kozlova, Denys, Benedum, Valdez, Enriquez, Bishay, Chinthirla, Truong, Krum, DiPatrizio, Deol, Martins-Green and Curras-Collazo 2022 Kozlova, Denys, Benedum, Valdez, Enriquez, Bishay, Chinthirla, Truong, Krum, DiPatrizio, Deol, Martins-Green and Curras-Collazo |
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Keywords | leptin - adiponectin polybrominated diphenyl ethers (PBDEs) dyslipidemia (DLP) endocrine-disrupting chemical (EDC) fatty liver metabolic syndrome & type II diabetes hypothalamus maternal |
Language | English |
License | Copyright © 2022 Kozlova, Denys, Benedum, Valdez, Enriquez, Bishay, Chinthirla, Truong, Krum, DiPatrizio, Deol, Martins-Green and Curras-Collazo. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
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Notes | ORCID ID: Elena V. Kozlova, orcid.org/0000-0002-4691-6618; Maximilian E. Denys, orcid.org/0000-0002-7423-6265; Matthew C. Valdez, orcid.org/0000-0002-8227-7921; Anthony E. Bishay, orcid.org/0000-0002-6057-3770; Poonamjot Deol, orcid.org/0000-0002-7109-0619; Margarita C. Curras-Collazo, orcid.org/0000-0002-0189-4179 Reviewed by: Tomohiko Isobe, National Institute for Environmental Studies (NIES), Japan; Taisen Iguchi, Graduate University for Advanced Studies (Sokendai), Japan This article was submitted to Cellular Endocrinology, a section of the journal Frontiers in Endocrinology Edited by: Edith Sánchez-Jaramillo, National Institute of Psychiatry Ramon de la Fuente Muñiz (INPRFM), Mexico |
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SubjectTerms | Adiponectin Agouti-Related Protein Animals Cholesterol Corn Oil Endocrine Disruptors - toxicity endocrine-disrupting chemical (EDC) Endocrinology Environmental Pollutants - toxicity fatty liver Female Flame Retardants - toxicity Halogenated Diphenyl Ethers - toxicity Homeostasis Leptin leptin - adiponectin Male maternal metabolic syndrome & type II diabetes Mice Mice, Inbred C57BL Organophosphates Persistent Organic Pollutants polybrominated diphenyl ethers (PBDEs) Polychlorinated Biphenyls Pregnancy Sex Factors Triglycerides |
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Title | Developmental exposure to indoor flame retardants and hypothalamic molecular signatures: Sex-dependent reprogramming of lipid homeostasis |
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