Hostname: page-component-8448b6f56d-cfpbc Total loading time: 0 Render date: 2024-04-23T16:43:35.489Z Has data issue: false hasContentIssue false
  • English
  • Français

Green tea extract intake during lactation modified cardiac macrophage infiltration and AMP-activated protein kinase phosphorylation in weanling rats from undernourished mother during gestation and lactation

Published online by Cambridge University Press:  06 December 2016

E. Matsumoto ,
S. Kataoka ,
Y. Mukai ,
M. Sato  and
S. Sato
E. Matsumoto
Affiliation:
Graduate School of Health Sciences, Aomori University of Health and Welfare, Aomori, Japan
S. Kataoka
Affiliation:
Graduate School of Health Sciences, Aomori University of Health and Welfare, Aomori, Japan
Y. Mukai
Affiliation:
School of Nutrition and Dietetics, Faculty of Health and Social Work, Kanagawa University of Human Services, Kanagawa, Japan
M. Sato
Affiliation:
Department of Nutrition, Faculty of Health Sciences, Aomori University of Health and Welfare, Aomori, Japan
S. Sato*
Affiliation:
Graduate School of Health Sciences, Aomori University of Health and Welfare, Aomori, Japan Department of Nutrition, Faculty of Health Sciences, Aomori University of Health and Welfare, Aomori, Japan
*
*Address for correspondence: Dr. S. Sato, Graduate School of Health Sciences, Aomori University of Health and Welfare, Mase 58-1, Hamadate, Aomori 030-8505, Japan. (Email s_sato3@auhw.ac.jp)
Get access Rights & Permissions [Opens in a new window]

Abstract

Maternal dietary restriction is often associated with cardiovascular disease in offspring. The aim of this study was to investigate the effect of green tea extract (GTE) intake during lactation on macrophage infiltration, and activation of adenosine monophosphate (AMP)-activated protein kinase (AMPK) and serine-threonine kinase Akt (Akt) in the hearts of weanlings exposed to maternal dietary protein restriction. Pregnant Wistar rats were fed control (C) or low-protein diets (LP) throughout gestation. Following delivery, the dams received a control or a GTE-containing control diet during lactation: control diet during gestation and lactation (CC), low-protein diet during gestation and lactation (LPC), low-protein diet during gestation and 0.12% GTE-containing low-protein diet during lactation (LPL), and low-protein diet during gestation and 0.24% GTE-containing low-protein diet during lactation (LPH). The female offspring were sacrificed at day 22. Biochemical parameters in the plasma, macrophage infiltration, degree of fibrosis and expression levels of AMPK and Akt were examined. The plasma insulin level increased in LPH compared with LPC. Percentage of the fibrotic areas and the number of macrophages in LPC were higher than those in CC. Conversely, the fibrotic areas and the macrophage number in LPH were smaller (21 and 56%, respectively) than those in LPC. The levels of phosphorylated AMPK in LPL and LPH, and Akt in LPH were greater than those in LPC. In conclusion, maternal protein restriction may induce macrophage infiltration and the decrease of insulin levels. However, GTE intake during lactation may suppress macrophage infiltration and restore insulin secretion function via upregulation of AMPK and insulin signaling in weanlings.

Keywords

Green tea extractmacrophageheartoffspringmaternal protein restriction
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 8 , Issue 2 , April 2017 , pp. 178 - 187
Check for updates
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1. Woodall, SM, Johnston, BM, Breier, BH, Gluckman, PD. Chronic maternal undernutrition in the rat leads to delayed postnatal growth and elevated blood pressure of offspring. Pediatr Res. 1996; 40, 438–443.Google Scholar
2. Langley-Evans, SC. Fetal programming of cardiovascular function through exposure to maternal undernutrition. Proc Nutr Soc. 2001; 60, 505–513.Google Scholar
3. Kaijser, M, Bonamy, AK, Akre, O, et al. Perinatal risk factors for ischemic heart disease: disentangling the roles of birth weight and preterm birth. Circulation. 2008; 117, 405–410.CrossRefGoogle ScholarPubMed
4. Gluckman, PD, Hanson, MA, Cooper, C, Thornburg, KL. Effect of in utero and early-life conditions on adult health and disease. N Engl J Med. 2008; 359, 61–73.Google Scholar
5. Lo Vasco, VR, Salmaso, R, Zanardo, V, et al. Fetal aorta wall inflammation in ultrasound-detected aortic intima/media thickness and growth retardation. J Reprod Immunol. 2011; 91, 103–107.Google Scholar
6. Delghingaro-Augusto, V, Madad, L, Chandra, A, et al. Islet inflammation, hemosiderosis, and fibrosis in intrauterine growth-restricted and high fat-fed Sprague-Dawley rats. Am J Pathol. 2014; 184, 1446–1457.Google Scholar
7. de Melo, JF, da Costa, TB, da Costa Lima, TD, et al. Long-term effects of a neonatal low-protein diet in rats on the number of macrophages in culture and the expression/production of fusion proteins. Eur J Nutr. 2013; 52, 1475–1482.Google Scholar
8. Hardie, DG. AMP-activated protein kinase: an energy sensor that regulates all aspects of cell function. Genes Dev. 2011; 25, 1895–1908.Google Scholar
9. Zhou, G, Sebhat, IK, Zhang, BB. AMPK activators – potential therapeutics for metabolic and other diseases. Acta Physiol (Oxf). 2009; 196, 175–190.Google Scholar
10. Daskalopoulos, EP, Dufeys, C, Bertrand, L, Beauloye, C, Horman, S. AMPK in cardiac fibrosis and repair: actions beyond metabolic regulation. J Mol Cell Cardiol. 2016; 91, 188–200.Google Scholar
11. Bijland, S, Mancini, SJ, Salt, IP. Role of AMP-activated protein kinase in adipose tissue metabolism and inflammation. Clin Sci (Lond). 2013; 124, 491–507.CrossRefGoogle ScholarPubMed
12. Ko, HJ, Zhang, Z, Jung, DY, et al. Nutrient stress activates inflammation and reduces glucose metabolism by suppressing AMP-activated protein kinase in the heart. Diabetes. 2009; 58, 2536–2546.Google Scholar
13. Galic, S, Fullerton, MD, Schertzer, JD, et al. Hematopoietic AMPK beta1 reduces mouse adipose tissue macrophage inflammation and insulin resistance in obesity. J Clin Invest. 2011; 121, 4903–4915.CrossRefGoogle ScholarPubMed
14. Murase, T, Misawa, K, Haramizu, S, Hase, T. Catechin-induced activation of the LKB1/AMP-activated protein kinase pathway. Biochem Pharmacol. 2009; 78, 78–84.Google Scholar
15. Collins, QF, Liu, HY, Pi, J, et al. Epigallocatechin-3-gallate (EGCG), a green tea polyphenol, suppresses hepatic gluconeogenesis through 5’-AMP-activated protein kinase. J Biol Chem. 2007; 282, 30143–30149.Google Scholar
16. Li, Y, Zhao, S, Zhang, W, et al. Epigallocatechin-3-O-gallate (EGCG) attenuates FFAs-induced peripheral insulin resistance through AMPK pathway and insulin signaling pathway in vivo. Diabetes Res Clin Pract. 2011; 93, 205–214.Google Scholar
17. Hao, J, Kim, CH, Ha, TS, Ahn, HY. Epigallocatechin-3 gallate prevents cardiac hypertrophy induced by pressure overload in rats. J Vet Sci. 2007; 8, 121–129.Google Scholar
18. Khurana, S, Venkataraman, K, Hollingsworth, A, Piche, M, Tai, TC. Polyphenols: benefits to the cardiovascular system in health and in aging. Nutrients. 2013; 5, 3779–3827.Google Scholar
19. Ikeda, M, Suzuki, C, Umegaki, K, et al. Preventive effects of green tea catechins on spontaneous stroke in rats. Med Sci Monit. 2007; 13, BR40–BR45.Google Scholar
20. Tanabe, N, Suzuki, H, Aizawa, Y, Seki, N. Consumption of green and roasted teas and the risk of stroke incidence: results from the Tokamachi-Nakasato cohort study in Japan. Int J Epidemiol. 2008; 37, 1030–1040.Google Scholar
21. 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, 1152–1158.Google Scholar
22. Shiojima, I, Yefremashvili, M, Luo, Z, et al. Akt signaling mediates postnatal heart growth in response to insulin and nutritional status. J Biol Chem. 2002; 277, 37670–37677.Google Scholar
23. Beauloye, C, Bertrand, L, Horman, S, Hue, L. AMPK activation, a preventive therapeutic target in the transition from cardiac injury to heart failure. Cardiovasc Res. 2011; 90, 224–233.Google Scholar
24. Calvert, JW, Gundewar, S, Jha, S, et al. Acute metformin therapy confers cardioprotection against myocardial infarction via AMPK-eNOS-mediated signaling. Diabetes. 2008; 57, 696–705.Google Scholar
25. Legeay, S, Rodier, M, Fillon, L, Faure, S, Clere, N. Epigallocatechin Gallate: a review of its beneficial properties to prevent metabolic syndrome. Nutrients. 2015; 7, 5443–5468.Google Scholar
26. Lim, K, Zimanyi, MA, Black, MJ. Effect of maternal protein restriction during pregnancy and lactation on the number of cardiomyocytes in the postproliferative weanling rat heart. Anat Rec (Hoboken). 2010; 293, 431–437.Google Scholar
27. Sheng, R, Gu, ZL, Xie, ML, Zhou, WX, Guo, CY. EGCG inhibits proliferation of cardiac fibroblasts in rats with cardiac hypertrophy. Planta Med. 2009; 75, 113–120.Google Scholar
28. Kitamura, M, Nishino, T, Obata, Y, et al. Epigallocatechin gallate suppresses peritoneal fibrosis in mice. Chem Biol Interact. 2012; 195, 95–104.Google Scholar
29. Leslie, KO, Taatjes, DJ, Schwarz, J, vonTurkovich, M, Low, RB. Cardiac myofibroblasts express alpha smooth muscle actin during right ventricular pressure overload in the rabbit. Am J Pathol. 1991; 139, 207–216.Google Scholar
30. Cao, Y, Bao, S, Yang, W, et al. Epigallocatechin gallate prevents inflammation by reducing macrophage infiltration and inhibiting tumor necrosis factor-alpha signaling in the pancreas of rats on a high-fat diet. Nutr Res. 2014; 34, 1066–1074.Google Scholar
31. Jang, HJ, Ridgeway, SD, Kim, JA. Effects of the green tea polyphenol epigallocatechin-3-gallate on high-fat diet-induced insulin resistance and endothelial dysfunction. Am J Physiol Endocrinol Metab. 2013; 305, E1444–E1451.Google Scholar
32. Krishnan, TR, Velusamy, P, Srinivasan, A, et al. EGCG mediated downregulation of NF-AT and macrophage infiltration in experimental hepatic steatosis. Exp Gerontol. 2014; 57, 96–103.Google Scholar
33. Merezak, S, Reusens, B, Renard, A, et al. Effect of maternal low-protein diet and taurine on the vulnerability of adult Wistar rat islets to cytokines. Diabetologia. 2004; 47, 669–675.Google ScholarPubMed
34. Morimoto, S, Calzada, L, Sosa, TC, et al. Emergence of ageing-related changes in insulin secretion by pancreatic islets of male rat offspring of mothers fed a low-protein diet. Br J Nutr. 2012; 107, 1562–1565.Google Scholar
35. Kim, JJ, Tan, Y, Xiao, L, Sun, YL, Qu, X. Green tea polyphenol epigallocatechin-3-gallate enhance glycogen synthesis and inhibit lipogenesis in hepatocytes. Biomed Res Int. 2013; 2013, 920128.CrossRefGoogle ScholarPubMed
36. Kim, SJ, Li, M, Jeong, CW, et al. Epigallocatechin-3-gallate, a green tea catechin, protects the heart against regional ischemia-reperfusion injuries through activation of RISK survival pathways in rats. Arch Pharm Res. 2014; 37, 1079–1085.Google Scholar
37. Salt, IP, Palmer, TM. Exploiting the anti-inflammatory effects of AMP-activated protein kinase activation. Expert Opin Investig Drugs. 2012; 21, 1155–1167.Google Scholar
38. Shen, CL, Samathanam, C, Tatum, OL, et al. Green tea polyphenols avert chronic inflammation-induced myocardial fibrosis of female rats. Inflamm Res. 2011; 60, 665–672.Google Scholar
39. Dong, J, Zhang, X, Zhang, L, et al. Quercetin reduces obesity-associated ATM infiltration and inflammation in mice: a mechanism including AMPKalpha1/SIRT1. J Lipid Res. 2014; 55, 363–374.CrossRefGoogle ScholarPubMed
40. Wang, XF, Zhang, JY, Li, L, et al. Metformin improves cardiac function in rats via activation of AMP-activated protein kinase. Clin Exp Pharmacol Physiol. 2011; 38, 94–101.Google Scholar
41. Appeldoorn, MM, Venema, DP, Peters, TH, et al. Some phenolic compounds increase the nitric oxide level in endothelial cells in vitro. J Agric Food Chem. 2009; 57, 7693–7699.Google Scholar
42. Fulton, D, Gratton, JP, McCabe, TJ, et al. Regulation of endothelium-derived nitric oxide production by the protein kinase Akt. Nature. 1999; 399, 597–601.Google Scholar
43. Ying, Z, Xie, X, Chen, M, Yi, K, Rajagopalan, S. Alpha-lipoic acid activates eNOS through activation of PI3-kinase/Akt signaling pathway. Vascul Pharmacol. 2015; 64, 28–35.CrossRefGoogle ScholarPubMed
44. Thone-Reineke, C, Kalk, P, Dorn, M, et al. High-protein nutrition during pregnancy and lactation programs blood pressure, food efficiency, and body weight of the offspring in a sex-dependent manner. Am J Physiol Regul Integr Comp Physiol. 2006; 291, R1025–R1030.Google Scholar
45. Elmes, MJ, Haase, A, Gardner, DS, Langley-Evans, SC. Sex differences in sensitivity to beta-adrenergic agonist isoproterenol in the isolated adult rat heart following prenatal protein restriction. Br J Nutr. 2009; 101, 725–734.Google Scholar
46. Moritz, KM, Cuffe, JS, Wilson, LB, et al. Review: sex specific programming: a critical role for the renal renin-angiotensin system. Placenta. 2010; 31(Suppl), S40–S46.CrossRefGoogle ScholarPubMed