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Effect of high chronic intake of sucrose on liver metabolism in aging rats. Modulation by rutin and micronutrients

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Abstract

High-sugar intake and senescence share common deleterious effects, in particular in liver, but combination of these two factors was little studied. Our aims were to examine the effect of a high-sucrose diet in liver of old rats and also the potential benefices of a polyphenol/micronutrient supplementation. Four groups of 22-month-old male rats fed during 5 months with a diet containing either 13 or 62% sucrose, supplemented or not with rutin, vitamin E, A, D, selenium, and zinc were compared. We measured liver macronutrient composition, glycation/oxidative stress, enzyme activities (lipogenesis, β-oxidation, fructokinase), gene expression (enzymes and transcription factors), in vivo protein synthesis rates and plasma parameters. Sucrose induced an increase in plasma and liver lipid content, and a stimulation of liver protein synthesis rates. Gene expression was little changed by sucrose, with lower levels for LXR-α and LXR-β. Polyphenol/micronutrient supplementation tended to limit liver triglyceride infiltration through variations in fatty acid synthase, acyl coA oxidase, and possibly ATP-citrate lyase activities. In conclusion, despite differences in enzymatic regulations, and blunted responses of gene expression, high-sucrose diet was still able to induce a marked increase in liver lipid content in old animals. However, it probably attenuated the positive impact of polyphenol/micronutrients.

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References

  1. Bechmann LP, Hannivoort RA, Gerken G, Hotamisligil GS, Trauner M, Canbay A (2012) The interaction of hepatic lipid and glucose metabolism in liver diseases. J Hepatol 56:952–964. https://doi.org/10.1016/j.jhep.2011.08.025

    Article  CAS  PubMed  Google Scholar 

  2. Bertolotti M, Lonardo A, Mussi C, Baldelli E, Pellegrini E, Ballestri S, Romagnoli D, Loria P (2014) Nonalcoholic fatty liver disease and aging: epidemiology to management. World J Gastroenterol 20:14185–14204. https://doi.org/10.3748/wjg.v20.i39.14185

    Article  PubMed  PubMed Central  Google Scholar 

  3. Chuffa LG, Fioruci-Fontanelli BA, Bordon JG, Pires RB, Braga CP, Seiva FR, Fernandes AA (2014) Rutin ameliorates glycemic index, lipid profile and enzymatic activities in serum, heart and liver tissues of rats fed with a combination of hypercaloric diet and chronic ethanol consumption. Indian J Biochem Biophys 51:215–222

    CAS  PubMed  Google Scholar 

  4. Chypre M, Zaidi N, Smans K (2012) ATP-citrate lyase: a mini-review. Biochem Biophys Res Commun 422:1–4. https://doi.org/10.1016/j.bbrc.2012.04.144

    Article  CAS  PubMed  Google Scholar 

  5. Dekker MJ, Su Q, Baker C, Rutledge AC, Adeli K (2010) Fructose: a highly lipogenic nutrient implicated in insulin resistance, hepatic steatosis, and the metabolic syndrome. Am J Physiol Endocrinol Metab 299:E685–E694. https://doi.org/10.1152/ajpendo.00283.2010

    Article  CAS  PubMed  Google Scholar 

  6. Dong B, Kan CF, Singh AB, Liu J (2013) High-fructose diet downregulates long-chain acyl-CoA synthetase 3 expression in liver of hamsters via impairing LXR/RXR signaling pathway. J Lipid Res 54:1241–1254. https://doi.org/10.1194/jlr.M032599

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Eliades M, Spyrou E (2015) Vitamin D: a new player in non-alcoholic fatty liver disease? World J Gastroenterol 21:1718–1727. https://doi.org/10.3748/wjg.v21.i6.1718

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Faure P, Barclay D, Joyeux-Faure M, Halimi S (2007) Comparison of the effects of zinc alone and zinc associated with selenium and vitamin E on insulin sensitivity and oxidative stress in high-fructose-fed rats. J Trace Elem Med Biol 21:113–119. https://doi.org/10.1016/j.jtemb.2006.12.005

    Article  CAS  PubMed  Google Scholar 

  9. Ferramosca A, Conte A, Damiano F, Siculella L, Zara V (2014) Differential effects of high-carbohydrate and high-fat diets on hepatic lipogenesis in rats. Eur J Nutr 53:1103–1114. https://doi.org/10.1007/s00394-013-0613-8

    Article  CAS  PubMed  Google Scholar 

  10. Giris M, Dogru-Abbasoglu S, Kumral A, Olgac V, Kocak-Toker N, Uysal M (2014) Effect of carnosine alone or combined with alpha-tocopherol on hepatic steatosis and oxidative stress in fructose-induced insulin-resistant rats. J Physiol Biochem 70:385–395. https://doi.org/10.1007/s13105-014-0314-7

    Article  CAS  PubMed  Google Scholar 

  11. Hagopian K, Ramsey JJ, Weindruch R (2005) Fructose metabolizing enzymes from mouse liver: influence of age and caloric restriction. Biochim Biophys Acta 1721:37–43. https://doi.org/10.1016/j.bbagen.2004.10.001

    Article  CAS  PubMed  Google Scholar 

  12. Hsu CL, Wu CH, Huang SL, Yen GC (2009) Phenolic compounds rutin and o-coumaric acid ameliorate obesity induced by high-fat diet in rats. J Agric Food Chem 57:425–431. https://doi.org/10.1021/jf802715t

    Article  CAS  PubMed  Google Scholar 

  13. Hu QH, Zhang X, Pan Y, Li YC, Kong LD (2012) Allopurinol, quercetin and rutin ameliorate renal NLRP3 inflammasome activation and lipid accumulation in fructose-fed rats. Biochem Pharmacol 84:113–125. https://doi.org/10.1016/j.bcp.2012.03.005

    Article  CAS  PubMed  Google Scholar 

  14. Jensen-Urstad AP, Semenkovich CF (2012) Fatty acid synthase and liver triglyceride metabolism: housekeeper or messenger? Biochim Biophys Acta 1821:747–753. https://doi.org/10.1016/j.bbalip.2011.09.017

    Article  CAS  PubMed  Google Scholar 

  15. Lanaspa MA, Sanchez-Lozada LG, Choi YJ, Cicerchi C, Kanbay M, Roncal-Jimenez CA, Ishimoto T, Li N, Marek G, Duranay M, Schreiner G, Rodriguez-Iturbe B, Nakagawa T, Kang DH, Sautin YY, Johnson RJ (2012) Uric acid induces hepatic steatosis by generation of mitochondrial oxidative stress: potential role in fructose-dependent and -independent fatty liver. J Biol Chem 287:40732–40744. https://doi.org/10.1074/jbc.M112.399899

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Lustig RH (2013) Fructose: it’s “alcohol without the buzz”. Advances in nutrition: an international review. Journal 4:226–235. https://doi.org/10.3945/an.112.002998

    Article  CAS  Google Scholar 

  17. Mayot G, Breuille D, Jarret AR, Obled C, Papet I (2008) Systemic low-grade inflammation does not decrease skeletal muscle mass and protein synthesis in old rats. J Musculoskelet Neuronal Interact 8:410–417

    CAS  PubMed  Google Scholar 

  18. Mosoni L, Gatineau E, Gatellier P, Migne C, Savary-Auzeloux I, Remond D, Rocher E, Dardevet D (2014) High whey protein intake delayed the loss of lean body mass in healthy old rats, whereas protein type and polyphenol/antioxidant supplementation had no effects. PLoS One 9:e109098. https://doi.org/10.1371/journal.pone.0109098

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Odbayar TO, Badamhand D, Kimura T, Takashi Y, Tsushida T, Ide T (2006) Comparative studies of some phenolic compounds (quercetin, rutin, and ferulic acid) affecting hepatic fatty acid synthesis in mice. J Agric Food Chem 54:8261–8265. https://doi.org/10.1021/jf061135c

    Article  CAS  PubMed  Google Scholar 

  20. Pagliassotti MJ, Prach PA, Koppenhafer TA, Pan DA (1996) Changes in insulin action, triglycerides, and lipid composition during sucrose feeding in rats. Am J Phys 271:R1319–R1326

    CAS  Google Scholar 

  21. Panchal SK, Poudyal H, Arumugam TV, Brown L (2011) Rutin attenuates metabolic changes, nonalcoholic steatohepatitis, and cardiovascular remodeling in high-carbohydrate, high-fat diet-fed rats. J Nutr 141:1062–1069. https://doi.org/10.3945/jn.111.137877

    Article  CAS  PubMed  Google Scholar 

  22. Park SY, Kim YW, Kim JE, Kim JY (2006) Age-associated changes in fat metabolism in the rat and its relation to sympathetic activity. Life Sci 79:2228–2233. https://doi.org/10.1016/j.lfs.2006.07.014

    Article  CAS  PubMed  Google Scholar 

  23. Peng CH, Liu LK, Chuang CM, Chyau CC, Huang CN, Wang CJ (2011) Mulberry water extracts possess an anti-obesity effect and ability to inhibit hepatic lipogenesis and promote lipolysis. J Agric Food Chem 59:2663–2671. https://doi.org/10.1021/jf1043508

    Article  CAS  PubMed  Google Scholar 

  24. Poirier Y, Antonenkov VD, Glumoff T, Hiltunen JK (2006) Peroxisomal beta-oxidation—a metabolic pathway with multiple functions. Biochim Biophys Acta 1763:1413–1426. https://doi.org/10.1016/j.bbamcr.2006.08.034

    Article  CAS  PubMed  Google Scholar 

  25. Polakof S, Dardevet D, Lyan B, Mosoni L, Gatineau E, Martin JF, Pujos-Guillot E, Mazur A, Comte B (2016) Time course of molecular and metabolic events in the development of insulin resistance in fructose-fed rats. J Proteome Res 15:1862–1874. https://doi.org/10.1021/acs.jproteome.6b00043

    Article  CAS  PubMed  Google Scholar 

  26. Prakash P, Singh V, Jain M, Rana M, Khanna V, Barthwal MK, Dikshit M (2014) Silymarin ameliorates fructose induced insulin resistance syndrome by reducing de novo hepatic lipogenesis in the rat. Eur J Pharmacol 727:15–28. https://doi.org/10.1016/j.ejphar.2014.01.038

    Article  CAS  PubMed  Google Scholar 

  27. Reeves PG, Nielsen FH, Fahey GC Jr (1993) AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J Nutr 123:1939–1951

    Article  CAS  Google Scholar 

  28. Shafrir E, Orevi M (1984) Response of hepatic fructokinase to long-term sucrose diets and diabetes in spiny mice, albino mice and rats. Comp Biochem Physiol B 78:493–498

    Article  CAS  Google Scholar 

  29. She P, Olson KC, Kadota Y, Inukai A, Shimomura Y, Hoppel CL, Adams SH, Kawamata Y, Matsumoto H, Sakai R, Lang CH, Lynch CJ (2013) Leucine and protein metabolism in obese Zucker rats. PLoS One 8:e59443. https://doi.org/10.1371/journal.pone.0059443

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Tappy L, Le KA (2012) Does fructose consumption contribute to non-alcoholic fatty liver disease? Clin Res Hepatol Gastroenterol 36:554–560. https://doi.org/10.1016/j.clinre.2012.06.005

    Article  CAS  PubMed  Google Scholar 

  31. Vila L, Rebollo A, Adalsteisson GS, Alegret M, Merlos M, Roglans N, Laguna JC (2011) Reduction of liver fructokinase expression and improved hepatic inflammation and metabolism in liquid fructose-fed rats after atorvastatin treatment. Toxicol Appl Pharmacol 251:32–40. https://doi.org/10.1016/j.taap.2010.11.011

    Article  CAS  PubMed  Google Scholar 

  32. Vitorica J, Satrustegui J, Machado A (1981) Metabolic implications of ageing: changes in activities of key lipogenic and gluconeogenic enzymes in the aged rat liver. Enzyme 26:144–152

    Article  CAS  Google Scholar 

  33. Wu CH, Lin MC, Wang HC, Yang MY, Jou MJ, Wang CJ (2011) Rutin inhibits oleic acid induced lipid accumulation via reducing lipogenesis and oxidative stress in hepatocarcinoma cells. J Food Sci 76:T65–T72. https://doi.org/10.1111/j.1750-3841.2010.02033.x

    Article  CAS  PubMed  Google Scholar 

  34. Yang L, Zhang Y, Wang S, Zhang W, Shi R (2014) Decreased liver peroxisomal beta-oxidation accompanied by changes in brain fatty acid composition in aged rats. Neurol Sci 35:289–293. https://doi.org/10.1007/s10072-013-1509-3

    Article  PubMed  Google Scholar 

  35. Zhang Y, Wang L, Zhang J, Li Y, He Q, Li H, Guo X, Guo J, Zhang H (2014) Probiotic Lactobacillus casei Zhang ameliorates high-fructose-induced impaired glucose tolerance in hyperinsulinemia rats. Eur J Nutr 53:221–232. https://doi.org/10.1007/s00394-013-0519-5

    Article  CAS  PubMed  Google Scholar 

  36. Zhao S, Li R, Li Y, Chen W, Zhang Y, Chen G (2012) Roles of vitamin a status and retinoids in glucose and fatty acid metabolism. Biochem Cell Biol 90:142–152. https://doi.org/10.1139/o11-079

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank Christophe Del’homme, Philippe Denis, Philippe Lhoste, and Arlette Cissoire for animal management and Nordine Hafnaoui and Brigitte Laillet for technical assistance.

This work was supported by Institut National de la Recherche Agronomique (INRA), France. Similar results as those of this study were published in a preliminary form in the result section of Gatineau Eva thesis on the following website: https://tel.archives-ouvertes.fr/tel-01491088/document.

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  1. UNH, Unité de Nutrition Humaine, PFEM, MetaboHUB-Clermont, Université Clermont Auvergne, INRA, CRNH Auvergne, F-63000 Clermont-Ferrand, 63122, Theix, France

    Eva Gatineau, Frédéric Capel, Dominique Dardevet, Jérémie David, Corinne Pouyet, Sergio Polakof & Laurent Mosoni

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  1. Eva Gatineau
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Correspondence to Laurent Mosoni.

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Gatineau, E., Capel, F., Dardevet, D. et al. Effect of high chronic intake of sucrose on liver metabolism in aging rats. Modulation by rutin and micronutrients. J Physiol Biochem 74, 569–577 (2018). https://doi.org/10.1007/s13105-018-0628-y

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  • DOI: https://doi.org/10.1007/s13105-018-0628-y

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