Açaí (Euterpe oleracea Martius) supplementation in the diet during gestation and lactation attenuates liver steatosis in dams and protects offspring
- 27 Downloads
Maternal high-fat diet affects offspring and can induce metabolic disorders such as non-alcoholic fatty liver disease (NAFLD). New therapeutic strategies are being investigated as way to prevent or attenuate this condition. The objective of this study was to evaluate the effect of açaí supplementation in the maternal high-fat diet on dams and offspring lipid metabolism.
Female Fisher rats were divided in four groups and fed a control diet (C), a high-fat diet (HF), an açaí supplemented diet (CA) and a high-fat diet supplemented with açaí (HFA) 2 weeks before mating, during gestation and lactation. The effects of açaí were evaluated in the male offspring after birth (P1) and weaning (P21).
HFA reduced relative liver weight, fat and cholesterol liver content in dams and improved liver steatosis as confirmed by histological analyses. HFA increased serum cholesterol and expression of Srebpf1 and Fasn genes. In offspring, HFA decreased relative liver weight, and serum cholesterol only in P21. An increase in the Sirt1, Srebpf1 and Fasn genes expression was observed in P21.
These results suggest that açaí supplementation may attenuate NAFLD in dams and protect offspring from the detrimental effects of lipid excess from a maternal high-fat diet.
KeywordsAçaí Euterpe oleracea Martius High-fat maternal diet Metabolic programming Non-alcoholic fatty liver disease
The authors are grateful to the Jair Pastor Mota and Laboratory of Experimental Nutrition for technical support and supply of animals, Dr Daniela Pala (UFOP, Brazil), Dr Carla Teixeira Silva (UFOP, Brazil), MSc. Miliane Fagundes (UFOP, Brazil), MSc. Ana Maria Viana (UFOP, Brazil), MSc. Talita Magalhães (UFOP, Brazil), MSc. Raiana Souza e Silva (UFOP, Brazil), Maraisa Porfirio (UFOP, Brazil) and Daniel de Souza Paula (UFOP, Brazil) for helping with the animal handling. We thank Professor Dr Maria Terezinha Bahia (UFOP, Brazil) who provided laboratory reagents to perform biochemistry analysis, and Dr Gemma Barron (RGU, UK) for help with gene expression and western blotting experiments.
This research was supported by Federal University of Ouro Preto (UFOP, Minas Gerais, Brazil), Fundação de Amparo a Pesquisa do Estado de Minas Gerais (FAPEMIG, Minas Gerais, Brazil), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) from Brazilian government (P.O.B. scholarship) and Robert Gordon University (Aberdeen, Scotland, United Kingdom).
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
- 4.Hochberg Z, Feil R, Constancia M, Fraga M, Junien C, Carel JC, Boileau P, Le Bouc Y, Deal CL, Lillycrop K, Scharfmann R, Sheppard A, Skinner M, Szyf M, Waterland RA, Waxman DJ, Whitelaw E, Ong K, Albertsson-Wikland K (2011) Child health, developmental plasticity, and epigenetic programming. Endocr Rev 32(2):159–224. https://doi.org/10.1210/er.2009-0039 Google Scholar
- 12.Suter MA, Chen A, Burdine MS, Choudhury M, Harris RA, Lane RH, Friedman JE, Grove KL, Tackett AJ, Aagaard KM (2012) A maternal high-fat diet modulates fetal SIRT1 histone and protein deacetylase activity in nonhuman primates. FASEB J 26(12):5106–5114. https://doi.org/10.1096/fj.12-212878 Google Scholar
- 14.Bruce KD, Cagampang FR, Argenton M, Zhang J, Ethirajan PL, Burdge GC, Bateman AC, Clough GF, Poston L, Hanson MA, McConnell JM, Byrne CD (2009) Maternal high-fat feeding primes steatohepatitis in adult mice offspring, involving mitochondrial dysfunction and altered lipogenesis gene expression. Hepatology 50(6):1796–1808. https://doi.org/10.1002/hep.23205 Google Scholar
- 15.Rolo AP, Teodoro JS, Palmeira CM (2012) Role of oxidative stress in the pathogenesis of nonalcoholic steatohepatitis. Free Radic Biol Med 52(1):59–69. https://doi.org/10.1016/j.freeradbiomed.2011.10.003 Google Scholar
- 16.Nedergaard J, Cannon B (2003) The 'novel' 'uncoupling' proteins UCP2 and UCP3: what do they really do? Pros and cons for suggested functions. Exp Physiol 88(1):65–84Google Scholar
- 17.Baffy G (2005) Uncoupling protein-2 and non-alcoholic fatty liver disease. Front Biosci 10:2082–2096Google Scholar
- 19.Tanaka M, Kita T, Yamasaki S, Kawahara T, Ueno Y, Yamada M, Mukai Y, Sato S, Kurasaki M, Saito T (2017) Maternal resveratrol intake during lactation attenuates hepatic triglyceride and fatty acid synthesis in adult male rat offspring. Biochem Biophys Rep 9:173–179. https://doi.org/10.1016/j.bbrep.2016.12.011 Google Scholar
- 20.Tiao MM, Lin YJ, Yu HR, Sheen JM, Lin IC, Lai YJ, Tain YL, Huang LT, Tsai CC (2018) Resveratrol ameliorates maternal and post-weaning high-fat diet-induced nonalcoholic fatty liver disease via renin-angiotensin system. Lipids Health Dis 17(1):178. https://doi.org/10.1186/s12944-018-0824-3 Google Scholar
- 23.Guerra JFC, Maciel PS, Abreu ICME, Pereira RR, Silva M, Cardoso LM, Pinheiro-Sant'Ana HM, Lima WG, Silva ME, Pedrosa ML (2015) Dietary açai attenuates hepatic steatosis via adiponectin-mediated effects on lipid metabolism in high-fat diet mice. J Funct Foods 14:192–202. https://doi.org/10.1016/j.jff.2015.01.025 Google Scholar
- 24.Pereira RR, de Abreu IC, Guerra JF, Lage NN, Lopes JM, Silva M, de Lima WG, Silva ME, Pedrosa ML (2016) Acai (Euterpe oleracea Mart.) upregulates paraoxonase 1 gene expression and activity with concomitant reduction of hepatic steatosis in high-fat diet-fed rats. Oxid Med Cell Longev 2016:8379105. https://doi.org/10.1155/2016/8379105 Google Scholar
- 28.Burgueno AL, Cabrerizo R, Gonzales Mansilla N, Sookoian S, Pirola CJ (2013) Maternal high-fat intake during pregnancy programs metabolic-syndrome-related phenotypes through liver mitochondrial DNA copy number and transcriptional activity of liver PPARGC1A. J Nutr Biochem 24(1):6–13. https://doi.org/10.1016/j.jnutbio.2011.12.008 Google Scholar
- 31.Folch J, Lees M, Sloane Stanley GH (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226(1):497–509Google Scholar
- 35.Renault KM, Carlsen EM, Norgaard K, Nilas L, Pryds O, Secher NJ, Cortes D, Jensen JE, Olsen SF, Halldorsson TI (2015) Intake of carbohydrates during pregnancy in obese women is associated with fat mass in the newborn offspring. Am J Clin Nutr 102(6):1475–1481. https://doi.org/10.3945/ajcn.115.110551 Google Scholar
- 38.Argentato PP, Morais CA, Santamarina AB, César HC, Estadella D, Rosso VV, Pisani LP (2017) Jussara (Euterpe edulis Mart.) supplementation during pregnancy and lactation modulates UCP-1 and inflammation biomarkers induced by trans-fatty acids in the brown adipose tissue of offspring. Clin Nutr Exp 12:50–65. https://doi.org/10.1016/j.yclnex.2016.12.002 Google Scholar
- 39.Mennitti LV, Oyama LM, Santamarina AB, Nascimento OD, Pisani LP (2018) Influence of maternal consumption of different types of fatty acids during pregnancy and lactation on lipid and glucose metabolism of the 21-day-old male offspring in rats. Prostaglandins Leukot Essent Fatty Acids 135:54–62. https://doi.org/10.1016/j.plefa.2018.07.001 Google Scholar
- 40.Kemper JK, Choi SE, Kim DH (2013) Sirtuin 1 deacetylase: a key regulator of hepatic lipid metabolism. Vitam Horm 91:385–404. https://doi.org/10.1016/B978-0-12-407766-9.00016-X Google Scholar
- 43.Borengasser SJ, Kang P, Faske J, Gomez-Acevedo H, Blackburn ML, Badger TM, Shankar K (2014) 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 9(1):e84209. https://doi.org/10.1371/journal.pone.0084209 Google Scholar
- 45.Jump DB, Tripathy S, Depner CM (2013) Fatty acid-regulated transcription factors in the liver. Annu Rev Nutr 33:249–269. https://doi.org/10.1146/annurev-nutr-071812-161139 Google Scholar
- 48.de Souza MO, Souza ESL, de Brito Magalhaes CL, de Figueiredo BB, Costa DC, Silva ME, Pedrosa ML (2012) The hypocholesterolemic activity of acai (Euterpe oleracea Mart.) is mediated by the enhanced expression of the ATP-binding cassette, subfamily G transporters 5 and 8 and low-density lipoprotein receptor genes in the rat. Nutr Res 32(12):976–984. https://doi.org/10.1016/j.nutres.2012.10.001 Google Scholar
- 50.Garcia-Heredia A, Kensicki E, Mohney RP, Rull A, Triguero I, Marsillach J, Tormos C, Mackness B, Mackness M, Shih DM, Pedro-Botet J, Joven J, Saez G, Camps J (2013) Paraoxonase-1 deficiency is associated with severe liver steatosis in mice fed a high-fat high-cholesterol diet: a metabolomic approach. J Proteome Res 12(4):1946–1955. https://doi.org/10.1021/pr400050u Google Scholar
- 58.Caz V, Gil-Ramirez A, Largo C, Tabernero M, Santamaria M, Martin-Hernandez R, Marin FR, Reglero G, Soler-Rivas C (2015) Modulation of cholesterol-related gene expression by dietary fiber fractions from edible mushrooms. J Agric Food Chem 63(33):7371–7380. https://doi.org/10.1021/acs.jafc.5b02942 Google Scholar
- 59.Simino LAP, de Fante T, Fontana MF, Borges FO, Torsoni MA, Milanski M, Velloso LA, Torsoni AS (2017) Lipid overload during gestation and lactation can independently alter lipid homeostasis in offspring and promote metabolic impairment after new challenge to high-fat diet. Nutr Metab Lond 14:16. https://doi.org/10.1186/s12986-017-0168-4 Google Scholar
- 60.Pirola CJ, Gianotti TF, Burgueno AL, Rey-Funes M, Loidl CF, Mallardi P, Martino JS, Castano GO, Sookoian S (2013) Epigenetic modification of liver mitochondrial DNA is associated with histological severity of nonalcoholic fatty liver disease. Gut 62(9):1356–1363. https://doi.org/10.1136/gutjnl-2012-302962 Google Scholar
- 61.Baselga-Escudero L, Pascual-Serrano A, Ribas-Latre A, Casanova E, Salvado MJ, Arola L, Arola-Arnal A, Blade C (2015) Long-term supplementation with a low dose of proanthocyanidins normalized liver miR-33a and miR-122 levels in high-fat diet-induced obese rats. Nutr Res 35(4):337–345. https://doi.org/10.1016/j.nutres.2015.02.008 Google Scholar