Exposure to Obesogenic Environments during Perinatal Development Modulates Offspring Energy Balance Pathways in Adipose Tissue and Liver of Rodent Models
Obesogenic environments such as Westernized diets, overnutrition, and exposure to glycation during gestation and lactation can alter peripheral neuroendocrine factors in offspring, predisposing for metabolic diseases in adulthood. Thus, we hypothesized that exposure to obesogenic environments during...
| Main Authors: | , , , , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
MDPI AG
2023-03-01
|
| Series: | Nutrients |
| Subjects: | |
| Online Access: | https://www.mdpi.com/2072-6643/15/5/1281 |
| _version_ | 1797614620940173312 |
|---|---|
| author | Diana Sousa Mariana Rocha Andreia Amaro Marcos Divino Ferreira-Junior Keilah Valéria Naves Cavalcante Tamaeh Monteiro-Alfredo Cátia Barra Daniela Rosendo-Silva Lucas Paulo Jacinto Saavedra José Magalhães Armando Caseiro Paulo Cezar de Freitas Mathias Susana P. Pereira Paulo J. Oliveira Rodrigo Mello Gomes Paulo Matafome |
| author_facet | Diana Sousa Mariana Rocha Andreia Amaro Marcos Divino Ferreira-Junior Keilah Valéria Naves Cavalcante Tamaeh Monteiro-Alfredo Cátia Barra Daniela Rosendo-Silva Lucas Paulo Jacinto Saavedra José Magalhães Armando Caseiro Paulo Cezar de Freitas Mathias Susana P. Pereira Paulo J. Oliveira Rodrigo Mello Gomes Paulo Matafome |
| author_sort | Diana Sousa |
| collection | DOAJ |
| description | Obesogenic environments such as Westernized diets, overnutrition, and exposure to glycation during gestation and lactation can alter peripheral neuroendocrine factors in offspring, predisposing for metabolic diseases in adulthood. Thus, we hypothesized that exposure to obesogenic environments during the perinatal period reprograms offspring energy balance mechanisms. Four rat obesogenic models were studied: maternal diet-induced obesity (DIO); early-life obesity induced by postnatal overfeeding; maternal glycation; and postnatal overfeeding combined with maternal glycation. Metabolic parameters, energy expenditure, and storage pathways in visceral adipose tissue (VAT) and the liver were analyzed. Maternal DIO increased VAT lipogenic [NPY receptor-1 (NPY1R), NPY receptor-2 (NPY2R), and ghrelin receptor], but also lipolytic/catabolic mechanisms [dopamine-1 receptor (D1R) and p-AMP-activated protein kinase (AMPK)] in male offspring, while reducing NPY1R in females. Postnatally overfed male animals only exhibited higher NPY2R levels in VAT, while females also presented NPY1R and NPY2R downregulation. Maternal glycation reduces VAT expandability by decreasing NPY2R in overfed animals. Regarding the liver, D1R was decreased in all obesogenic models, while overfeeding induced fat accumulation in both sexes and glycation the inflammatory infiltration. The VAT response to maternal DIO and overfeeding showed a sexual dysmorphism, and exposure to glycotoxins led to a thin-outside-fat-inside phenotype in overfeeding conditions and impaired energy balance, increasing the metabolic risk in adulthood. |
| first_indexed | 2024-03-11T07:15:06Z |
| format | Article |
| id | doaj.art-f49df1bb5fbe41baa1172441c184d90d |
| institution | Directory Open Access Journal |
| issn | 2072-6643 |
| language | English |
| last_indexed | 2024-03-11T07:15:06Z |
| publishDate | 2023-03-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Nutrients |
| spelling | doaj.art-f49df1bb5fbe41baa1172441c184d90d2023-11-17T08:22:09ZengMDPI AGNutrients2072-66432023-03-01155128110.3390/nu15051281Exposure to Obesogenic Environments during Perinatal Development Modulates Offspring Energy Balance Pathways in Adipose Tissue and Liver of Rodent ModelsDiana Sousa0Mariana Rocha1Andreia Amaro2Marcos Divino Ferreira-Junior3Keilah Valéria Naves Cavalcante4Tamaeh Monteiro-Alfredo5Cátia Barra6Daniela Rosendo-Silva7Lucas Paulo Jacinto Saavedra8José Magalhães9Armando Caseiro10Paulo Cezar de Freitas Mathias11Susana P. Pereira12Paulo J. Oliveira13Rodrigo Mello Gomes14Paulo Matafome15Coimbra Institute for Clinical and Biomedical Research (iCBR) and Institute of Physiology, Faculty of Medicine, University of Coimbra, 3000-548 Coimbra, PortugalCoimbra Institute for Clinical and Biomedical Research (iCBR) and Institute of Physiology, Faculty of Medicine, University of Coimbra, 3000-548 Coimbra, PortugalCoimbra Institute for Clinical and Biomedical Research (iCBR) and Institute of Physiology, Faculty of Medicine, University of Coimbra, 3000-548 Coimbra, PortugalDepartment of Physiological Sciences, Institute of Biological Sciences, University Federal of Goiás, Goiânia 74690-900, BrazilDepartment of Physiological Sciences, Institute of Biological Sciences, University Federal of Goiás, Goiânia 74690-900, BrazilCoimbra Institute for Clinical and Biomedical Research (iCBR) and Institute of Physiology, Faculty of Medicine, University of Coimbra, 3000-548 Coimbra, PortugalCoimbra Institute for Clinical and Biomedical Research (iCBR) and Institute of Physiology, Faculty of Medicine, University of Coimbra, 3000-548 Coimbra, PortugalCoimbra Institute for Clinical and Biomedical Research (iCBR) and Institute of Physiology, Faculty of Medicine, University of Coimbra, 3000-548 Coimbra, PortugalLaboratory of Secretion Cell Biology, Department of Biotechnology, Genetics and Cell Biology, State University of Maringa, Maringa 87020-900, BrazilLaboratory of Metabolism and Exercise (LaMetEx), Research Centre in Physical Activity, Health and Leisure (CIAFEL) and Laboratory for Integrative and Translational Research in Population Health (ITR), Faculty of Sports, University of Porto, 4200-450 Porto, PortugalPolytechnic Institute of Coimbra, Coimbra Health School (ESTeSC), 3046-854 Coimbra, PortugalLaboratory of Secretion Cell Biology, Department of Biotechnology, Genetics and Cell Biology, State University of Maringa, Maringa 87020-900, BrazilCenter for Innovative Biomedicine and Biotechnology (CIBB), University of Coimbra, 3000-548 Coimbra, PortugalCenter for Innovative Biomedicine and Biotechnology (CIBB), University of Coimbra, 3000-548 Coimbra, PortugalDepartment of Physiological Sciences, Institute of Biological Sciences, University Federal of Goiás, Goiânia 74690-900, BrazilCoimbra Institute for Clinical and Biomedical Research (iCBR) and Institute of Physiology, Faculty of Medicine, University of Coimbra, 3000-548 Coimbra, PortugalObesogenic environments such as Westernized diets, overnutrition, and exposure to glycation during gestation and lactation can alter peripheral neuroendocrine factors in offspring, predisposing for metabolic diseases in adulthood. Thus, we hypothesized that exposure to obesogenic environments during the perinatal period reprograms offspring energy balance mechanisms. Four rat obesogenic models were studied: maternal diet-induced obesity (DIO); early-life obesity induced by postnatal overfeeding; maternal glycation; and postnatal overfeeding combined with maternal glycation. Metabolic parameters, energy expenditure, and storage pathways in visceral adipose tissue (VAT) and the liver were analyzed. Maternal DIO increased VAT lipogenic [NPY receptor-1 (NPY1R), NPY receptor-2 (NPY2R), and ghrelin receptor], but also lipolytic/catabolic mechanisms [dopamine-1 receptor (D1R) and p-AMP-activated protein kinase (AMPK)] in male offspring, while reducing NPY1R in females. Postnatally overfed male animals only exhibited higher NPY2R levels in VAT, while females also presented NPY1R and NPY2R downregulation. Maternal glycation reduces VAT expandability by decreasing NPY2R in overfed animals. Regarding the liver, D1R was decreased in all obesogenic models, while overfeeding induced fat accumulation in both sexes and glycation the inflammatory infiltration. The VAT response to maternal DIO and overfeeding showed a sexual dysmorphism, and exposure to glycotoxins led to a thin-outside-fat-inside phenotype in overfeeding conditions and impaired energy balance, increasing the metabolic risk in adulthood.https://www.mdpi.com/2072-6643/15/5/1281metabolic diseasesenergy balancemetabolic programmingsugars and AGEsobesity/adipose tissue |
| spellingShingle | Diana Sousa Mariana Rocha Andreia Amaro Marcos Divino Ferreira-Junior Keilah Valéria Naves Cavalcante Tamaeh Monteiro-Alfredo Cátia Barra Daniela Rosendo-Silva Lucas Paulo Jacinto Saavedra José Magalhães Armando Caseiro Paulo Cezar de Freitas Mathias Susana P. Pereira Paulo J. Oliveira Rodrigo Mello Gomes Paulo Matafome Exposure to Obesogenic Environments during Perinatal Development Modulates Offspring Energy Balance Pathways in Adipose Tissue and Liver of Rodent Models Nutrients metabolic diseases energy balance metabolic programming sugars and AGEs obesity/adipose tissue |
| title | Exposure to Obesogenic Environments during Perinatal Development Modulates Offspring Energy Balance Pathways in Adipose Tissue and Liver of Rodent Models |
| title_full | Exposure to Obesogenic Environments during Perinatal Development Modulates Offspring Energy Balance Pathways in Adipose Tissue and Liver of Rodent Models |
| title_fullStr | Exposure to Obesogenic Environments during Perinatal Development Modulates Offspring Energy Balance Pathways in Adipose Tissue and Liver of Rodent Models |
| title_full_unstemmed | Exposure to Obesogenic Environments during Perinatal Development Modulates Offspring Energy Balance Pathways in Adipose Tissue and Liver of Rodent Models |
| title_short | Exposure to Obesogenic Environments during Perinatal Development Modulates Offspring Energy Balance Pathways in Adipose Tissue and Liver of Rodent Models |
| title_sort | exposure to obesogenic environments during perinatal development modulates offspring energy balance pathways in adipose tissue and liver of rodent models |
| topic | metabolic diseases energy balance metabolic programming sugars and AGEs obesity/adipose tissue |
| url | https://www.mdpi.com/2072-6643/15/5/1281 |
| work_keys_str_mv | AT dianasousa exposuretoobesogenicenvironmentsduringperinataldevelopmentmodulatesoffspringenergybalancepathwaysinadiposetissueandliverofrodentmodels AT marianarocha exposuretoobesogenicenvironmentsduringperinataldevelopmentmodulatesoffspringenergybalancepathwaysinadiposetissueandliverofrodentmodels AT andreiaamaro exposuretoobesogenicenvironmentsduringperinataldevelopmentmodulatesoffspringenergybalancepathwaysinadiposetissueandliverofrodentmodels AT marcosdivinoferreirajunior exposuretoobesogenicenvironmentsduringperinataldevelopmentmodulatesoffspringenergybalancepathwaysinadiposetissueandliverofrodentmodels AT keilahvalerianavescavalcante exposuretoobesogenicenvironmentsduringperinataldevelopmentmodulatesoffspringenergybalancepathwaysinadiposetissueandliverofrodentmodels AT tamaehmonteiroalfredo exposuretoobesogenicenvironmentsduringperinataldevelopmentmodulatesoffspringenergybalancepathwaysinadiposetissueandliverofrodentmodels AT catiabarra exposuretoobesogenicenvironmentsduringperinataldevelopmentmodulatesoffspringenergybalancepathwaysinadiposetissueandliverofrodentmodels AT danielarosendosilva exposuretoobesogenicenvironmentsduringperinataldevelopmentmodulatesoffspringenergybalancepathwaysinadiposetissueandliverofrodentmodels AT lucaspaulojacintosaavedra exposuretoobesogenicenvironmentsduringperinataldevelopmentmodulatesoffspringenergybalancepathwaysinadiposetissueandliverofrodentmodels AT josemagalhaes exposuretoobesogenicenvironmentsduringperinataldevelopmentmodulatesoffspringenergybalancepathwaysinadiposetissueandliverofrodentmodels AT armandocaseiro exposuretoobesogenicenvironmentsduringperinataldevelopmentmodulatesoffspringenergybalancepathwaysinadiposetissueandliverofrodentmodels AT paulocezardefreitasmathias exposuretoobesogenicenvironmentsduringperinataldevelopmentmodulatesoffspringenergybalancepathwaysinadiposetissueandliverofrodentmodels AT susanappereira exposuretoobesogenicenvironmentsduringperinataldevelopmentmodulatesoffspringenergybalancepathwaysinadiposetissueandliverofrodentmodels AT paulojoliveira exposuretoobesogenicenvironmentsduringperinataldevelopmentmodulatesoffspringenergybalancepathwaysinadiposetissueandliverofrodentmodels AT rodrigomellogomes exposuretoobesogenicenvironmentsduringperinataldevelopmentmodulatesoffspringenergybalancepathwaysinadiposetissueandliverofrodentmodels AT paulomatafome exposuretoobesogenicenvironmentsduringperinataldevelopmentmodulatesoffspringenergybalancepathwaysinadiposetissueandliverofrodentmodels |