Maternal green tea extract intake during lactation attenuates hepatic lipid accumulation in adult male rats exposed to a continuous high-fat diet from the foetal period

  • Shojiro Yamasaki Hokkaido University
  • Goh Kimura Hokkaido University
  • Kazunari Koizumi Hokkaido University
  • Ning Dai Hokkaido University
  • Rahel Mesfin Ketema Hokkaido University
  • Tomomi Tomihara Hokkaido University
  • Yukako Ueno Hokkaido University
  • Yuki Ohno Hokkaido University
  • Shin Sato Aomori University of Health and Welfare
  • Masaaki Kurasaki Hokkaido University
  • Toshiyuki Hosokawa Hokkaido University
  • Takeshi Saito Hokkaido University
Keywords: maternal supplements, high-fat diet, green tea extract, adult offspring, hepatic fat accumulation

Abstract

Background: Maternal lipid intake in the early postnatal period has a long-term effect on the possibility of fatty liver formation in children; besides, the importance of lipid consumption during lactation for children’s health has been suggested. Green tea extract (GTE) contains abundant catechins, and it has been reported to improve lipid metabolism and prevent fatty liver.

Objective: The aim of this study was to examine the effects of maternal GTE intake during lactation on hepatic lipid accumulation in adult male rats exposed to a continuous high-fat (HF) diet from the foetal period.

Methods: Pregnant Wistar rats received diets containing 13% (control-fat, CON) or 45% (high-fat, HF) fat. CON-fed mothers received the same diet during lactation, whereas HF-fed mothers received either HF diet alone or HF diet supplemented with 0.24% GTE. At weaning, male offspring were divided into three groups, i.e. CON/CON/CON, HF/HF/HF (HF-offspring) or HF/HF+GTE/HF (GTE-offspring), and were fed until 51 weeks.

Results: A significant hepatic triglyceride (Tg) accumulation was observed in the HF-offspring when compared with the other offspring. This is presumed to be caused by the promotion of Tg synthesis derived from exogenous fatty acid due to a significant increase in diacylglycerol O-acyltransferase 1 and a decrease in Tg expenditure caused by decreasing microsomal triglyceride transfer protein (MTTP) and long-chain acyl-CoA dehydrogenase. On the other hand, attenuated hepatic Tg accumulation was observed in the GTE-offspring. The levels of the hepatic lipid metabolism-related enzymes were improved to the same level as the CON-offspring, and particularly, MTTP was significantly increased as compared with the HF-offspring.

Conclusion: This study indicates the potential protective effects of maternal GTE intake during lactation on HF diet-induced hepatic lipid accumulation in adult male rat offspring and the possible underlying mechanisms.

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Author Biographies

Shojiro Yamasaki, Hokkaido University

Graduate School of Health Sciences

Goh Kimura, Hokkaido University

Graduate School of Health Sciences

Kazunari Koizumi, Hokkaido University

Graduate School of Health Sciences

Ning Dai, Hokkaido University

Graduate School of Health Sciences

Rahel Mesfin Ketema, Hokkaido University

Graduate School of Health Sciences

Tomomi Tomihara, Hokkaido University

Graduate School of Health Sciences

Yukako Ueno, Hokkaido University

Graduate School of Health Sciences

Yuki Ohno, Hokkaido University

Graduate School of Health Sciences

Shin Sato, Aomori University of Health and Welfare
Department of Nutrition
Masaaki Kurasaki, Hokkaido University
Faculty of Environmental Earth Science
Toshiyuki Hosokawa, Hokkaido University
Institute for the Advancement of Higher Education

References


  1. Graham HN. Green tea composition, consumption, and polyphenol chemistry. Prev Med (Baltim) 1992; 21(3): 334–50. doi: 10.1016/0091-7435(92)90041-F

  2. Kao Y-H, Chang H-H, Lee M-J, Chen C-L. Tea, obesity, and diabetes. Mol Nutr Food Res 2006; 50(2): 188–210. doi: 10.1002/mnfr.200500109

  3. Chu C, Deng J, Man Y, Qu Y. Green tea extracts epigallocatechin-3-gallate for different treatments. Biomed Res Int 2017; 2017: 5615647. doi: 10.1155/2017/5615647

  4. Chen C, Liu Q, Liu L, Hu Y, Feng Q. Potential biological effects of (-)-epigallocatechin-3-gallate on the treatment of nonalcoholic fatty liver disease. Mol Nutr Food Res 2018; 62(1): 1700483. doi: 10.1002/mnfr.201700483

  5. Mahmoodi M, Hosseini R, Kazemi A, Ofori-Asenso R, Mazidi M, Mazloomi SM. Effects of green tea or green tea catechin on liver enzymes in healthy individuals and people with nonalcoholic fatty liver disease: a systematic review and meta-analysis of randomized clinical trials. Phyther Res 2020; 34(7): ptr.6637. doi: 10.1002/ptr.6637

  6. Musial C, Kuban-Jankowska A, Gorska-Ponikowska M. Beneficial properties of green tea catechins. Int J Mol Sci 2020; 21(5): 1744. doi: 10.3390/ijms21051744

  7. Li J, Sapper TN, Mah E, Rudraiah S, Schill KE, Chitchumroonchokchai C, et al. Green tea extract provides extensive Nrf2-independent protection against lipid accumulation and NFκB pro- inflammatory responses during nonalcoholic steatohepatitis in mice fed a high-fat diet. Mol Nutr Food Res 2016; 60(4): 858–70. doi: 10.1002/mnfr.201500814

  8. Bae U-J, Park J, Park IW, Byung, Chae M, Oh M-R, et al. Epigallocatechin-3-gallate-rich green tea extract ameliorates fatty liver and weight gain in mice fed a high fat diet by activating the sirtuin 1 and AMP activating protein kinase pathway. Am J Chin Med 2018; 46(3): 617–32. doi: 10.1142/S0192415X18500325

  9. Santamarina AB, Oliveira JL, Silva FP, Carnier J, Mennitti LV., Santana AA, et al. Green tea extract rich in epigallocatechin-3-gallate prevents fatty liver by AMPK activation via LKB1 in mice fed a high-fat diet. PLoS One 2015; 10(11): e0141227. doi: 10.1371/journal.pone.0141227

  10. Santamarina AB, Carvalho-Silva M, Gomes LM, Okuda MH, Santana AA, Streck EL, et al. Decaffeinated green tea extract rich in epigallocatechin-3-gallate prevents fatty liver disease by increased activities of mitochondrial respiratory chain complexes in diet-induced obesity mice. J Nutr Biochem 2015 Nov; 26(11): 1348–56. doi: 10.1016/j.jnutbio.2015.07.002

  11. Huang J, Feng S, Liu A, Dai Z, Wang H, Reuhl K, et al. Green tea polyphenol EGCG alleviates metabolic abnormality and fatty liver by decreasing bile acid and lipid absorption in mice. Mol Nutr Food Res 2018; 62(4): 1700696. doi: 10.1002/mnfr.201700696

  12. Bruce KD, Cagampang FR, Argenton M, Zhang J, Ethirajan PL, Burdge GC, et al. Maternal high-fat feeding primes steatohepatitis in adult mice offspring, involving mitochondrial dysfunction and altered lipogenesis gene expression. Hepatology 2009; 50(6): 1796–808. doi: 10.1002/hep.23205

  13. Ribaroff GA, Wastnedge E, Drake AJ, Sharpe RM, Chambers TJG. Animal models of maternal high fat diet exposure and effects on metabolism in offspring: a meta-regression analysis. Obes Rev 2017; 18(6): 673–86. doi: 10.1111/obr.12524

  14. Li S-W, Yu H-R, Sheen J-M, Tiao M-M, Tain Y-L, Lin I-C, et al. A maternal high-fat diet during pregnancy and lactation, in addition to a postnatal high-fat diet, leads to metabolic syndrome with spatial learning and memory deficits: beneficial effects of resveratrol. Oncotarget 2017; 8(67): 111998–2013. doi: 10.18632/oncotarget.22960

  15. Sheen JM, Yu HR, Tain YL, Tsai WL, Tiao MM, Lin IC, et al. Combined maternal and postnatal high-fat diet leads to metabolic syndrome and is effectively reversed by resveratrol: a multiple-organ study. Sci Rep 2018; 8(1): 5607. doi: 10.1038/s41598-018-24010-0

  16. Gregorio BM, Souza-Mello V, Carvalho JJ, Mandarim-De-Lacerda CA, Aguila MB. Maternal high-fat intake predisposes nonalcoholic fatty liver disease in C57BL/6 offspring. Am J Obstet Gynecol 2010; 203(5): 495.e1–495.e8. doi: 10.1016/j.ajog.2010.06.042

  17. Alemdaroglu NC, Wolffram S, Boissel JP, Closs E, Spahn-Langguth H, Langguth P. Inhibition of folic acid uptake by catechins and tea extracts in caco-2 cells. Planta Med 2007; 73(1): 27–32. doi: 10.1055/s-2006-951745

  18. Otake M, Sakurai K, Watanabe M, Mori C. Association between serum folate levels and caffeinated beverage consumption in pregnant women in chiba: the Japan environment and children’s study. J Epidemiol 2018; 28(10): 414–19. doi: 10.2188/jea.JE20170019

  19. Okubo H, Miyake Y, Tanaka K, Sasaki S, Hirota Y. Maternal total caffeine intake, mainly from Japanese and Chinese tea, during pregnancy was associated with risk of preterm birth: the Osaka maternal and child health study. Nutr Res 2015; 35(4): 309–16. doi: 10.1016/j.nutres.2015.02.009

  20. Tanaka M, Kita T, Yamasaki S, Kawahara T, Ueno Y, Yamada M, et al. Maternal resveratrol intake during lactation attenuates hepatic triglyceride and fatty acid synthesis in adult male rat offspring. Biochem Biophys Rep 2017; 9: 173–9. doi: 10.1016/j.bbrep.2016.12.011

  21. Yamasaki S, Tomihara T, Kimura G, Ueno Y, Ketema RM, Sato S, et al. Long-term effects of maternal resveratrol intake during lactation on cholesterol metabolism in male rat off spring. Int J Food Sci Nutr 2019; 71(2): 226–34. doi: 10.1080/09637486.2019.1639638

  22. Sun B, Purcell RH, Terrillion CE, Yan J, Moran TH, Tamashiro KLK. Maternal high-fat diet during gestation or suckling differentially affects offspring leptin sensitivity and obesity. Diabetes 2012; 61(11): 2833–41. doi: 10.2337/db11-0957

  23. Sato S, Mukai Y, Hamaya M, Sun Y, Kurasaki M. Long-term effect of green tea extract during lactation on AMPK expression in rat offspring exposed to fetal malnutrition. Nutrition 2013; 29(9): 1152–8. doi: 10.1016/j.nut.2013.03.021

  24. Kataoka S, Norikura T, Sato S. Maternal green tea polyphenol intake during lactation attenuates kidney injury in high-fat-diet-fed male offspring programmed by maternal protein restriction in rats. J Nutr Biochem 2018; 56: 99–108. doi: 10.1016/j.jnutbio.2018.01.012

  25. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976; 72(1–2): 248–54. doi: 10.1016/0003-2697(76)90527-3

  26. Shimomura I, Shimano H, Korn BS, Bashmakov Y, Horton JD. Nuclear sterol regulatory element-binding proteins activate genes responsible for the entire program of unsaturated fatty acid biosynthesis in transgenic mouse liver. J Biol Chem 1998; 273(52): 35299–306. doi: 10.1074/jbc.273.52.35299

  27. Hussain MM, Rava P, Walsh M, Rana M, Iqbal J. Multiple functions of microsomal triglyceride transfer protein. Nutr Metab (Lond) 2012; 9(1): 14. doi: 10.1186/1743-7075-9-14

  28. Kurtz DM, Rinaldo P, Rhead WJ, Tian L, Millington DS, Vockley J, et al. Targeted disruption of mouse long-chain acyl-CoA dehydrogenase gene reveals crucial roles for fatty acid oxidation. Proc Natl Acad Sci U S A 1998; 95(26): 15592–7. doi: 10.1073/pnas.95.26.15592

  29. Wurie HR, Buckett L, Zammit VA. Diacylglycerol acyltransferase 2 acts upstream of diacylglycerol acyltransferase 1 and utilizes nascent diglycerides and de novo synthesized fatty acids in HepG2 cells. FEBS J 2012; 279(17): 3033–47. doi: 10.1111/j.1742-4658.2012.08684.x

  30. Koonen DPY, Jacobs RL, Febbraio M, Young ME, Soltys CLM, Ong H, et al. Increased hepatic CD36 expression contributes to dyslipidemia associated with diet-induced obesity. Diabetes 2007; 56(12): 2863–71. doi: 10.2337/db07-0907

  31. Donnelly KL, Smith CI, Schwarzenberg SJ, Jessurun J, Boldt MD, Parks EJ. Sources of fatty acids stored in liver and secreted via lipoproteins in patients with nonalcoholic fatty liver disease. J Clin Invest 2005; 115(5): 1343–51. doi: 10.1172/JCI23621

  32. Yamazaki T, Sasaki E, Kakinuma C, Yano T, Miura S, Ezaki O. Increased very low density lipoprotein secretion and gonadal fat mass in mice overexpressing liver DGAT1. J Biol Chem 2005; 280(22): 21506–14. doi: 10.1074/jbc.M412989200

  33. Raabe M, Véniant MM, Sullivan MA, Zlot CH, Björkegren J, Nielsen LB, et al. Analysis of the role of microsomal triglyceride transfer protein in the liver of tissue-specific knockout mice. J Clin Invest 1999; 103(9): 1287–98. doi: 10.1172/JCI6576

  34. Jun WL, Wei ZH, Ya ZJ, Liu Y, Yang Y, Ling CX, et al. Betaine attenuates hepatic steatosis by reducing methylation of the MTTP promoter and elevating genomic methylation in mice fed a high-fat diet. J Nutr Biochem 2014; 25(3): 329–36. doi: 10.1016/j.jnutbio.2013.11.007

  35. Chen L, Lee MJ, Li H, Yang CS. Absorption, distribution, and elimination of tea polyphenols in rats. Drug Metab Dispos 1997; 25(9): 1045–50.

  36. Lambert JD, Lee M-J, Lu H, Meng X, Hong JJJ, Seril DN, et al. Epigallocatechin-3-gallate is absorbed but extensively glucuronidated following oral administration to mice. J Nutr 2003; 133(12): 4172–7. doi: 10.1093/jn/133.12.4172

  37. Ehara T, Kamei Y, Takahashi M, Yuan X, Kanai S, Tamura E, et al. Role of DNA methylation in the regulation of lipogenic glycerol-3-phosphate acyltransferase 1 gene expression in the mouse neonatal liver. Diabetes 2012; 61(10): 2442–50. doi: 10.2337/db11-1834

  38. Gracia A, Elcoroaristizabal X, Fernández-Quintela A, Miranda J, Bediaga NG, de Pancorbo MM, et al. Fatty acid synthase methylation levels in adipose tissue: effects of an obesogenic diet and phenol compounds. Genes Nutr 2014; 9(4): 411. doi: 10.1007/s12263-014-0411-9

  39. Ehara T, Kamei Y, Yuan X, Takahashi M, Kanai S, Tamura E, et al. Ligand-activated PPARα-dependent DNA demethylation regulates the fatty acid β-oxidation genes in the postnatal liver. Diabetes 2015; 64(3): 775–84. doi: 10.2337/db14-0158

  40. Yuan X, Tsujimoto K, Hashimoto K, Kawahori K, Hanzawa N, Hamaguchi M, et al. Epigenetic modulation of Fgf21 in the perinatal mouse liver ameliorates diet-induced obesity in adulthood. Nat Commun 2018; 9(1): 636. doi: 10.1038/s41467-018-03038-w

  41. Reizel Y, Spiro A, Sabag O, Skversky Y, Hecht M, Keshet I, et al. Gender-specific postnatal demethylation and establishment of epigenetic memory. Genes Dev 2015; 29(9): 923–33. doi: 10.1101/gad.259309.115

  42. Sun Y, Mukai Y, Tanaka M, Saito T, Sato S, Kurasaki M. Green tea extract increases mRNA expression of enzymes which influence epigenetic marks in newborn female offspring from undernourished pregnant mother. PLoS One 2013; 8(8): e74559. doi: 10.1371/journal.pone.0074559

  43. Kitade H, Chen G, Ni Y, Ota T. Nonalcoholic fatty liver disease and insulin resistance: new insights and potential new treatments. Nutrients 2017; 9(4): 387. doi: 10.3390/nu9040387

  44. Li S, Tse IMY, Li ETS. Maternal green tea extract supplementation to rats fed a high-fat diet ameliorates insulin resistance in adult male offspring. J Nutr Biochem 2012; 23(12): 1655–60. doi: 10.1016/j.jnutbio.2011.11.008

  45. Hachul ACL, Boldarine VT, Neto NIP, Moreno MF, Ribeiro EB, Do Nascimento CMO, et al. Maternal consumption of green tea extract during pregnancy and lactation alters offspring’s metabolism in rats. PLoS One 2018; 13(7): e0199969. doi: 10.1371/journal.pone.0199969

  46. Gomes RM, Bueno FG, Schamber CR, de Mello JCP, de Oliveira JC, Francisco FA, et al. Maternal diet-induced obesity during suckling period programs offspring obese phenotype and hypothalamic leptin/insulin resistance. J Nutr Biochem 2018; 61: 24–32. doi: 10.1016/j.jnutbio.2018.07.006

Published
2020-10-05
How to Cite
Yamasaki, S., Kimura, G., Koizumi, K., Dai, N., Ketema, R., Tomihara, T., Ueno, Y., Ohno, Y., Sato, S., Kurasaki, M., Hosokawa, T., & Saito, T. (2020). Maternal green tea extract intake during lactation attenuates hepatic lipid accumulation in adult male rats exposed to a continuous high-fat diet from the foetal period. Food & Nutrition Research, 64. https://doi.org/10.29219/fnr.v64.5231
Section
Original Articles