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Neonatal intake of oleanolic acid attenuates the subsequent development of high fructose diet-induced non-alcoholic fatty liver disease in rats

Published online by Cambridge University Press:  24 May 2018

T. T. Nyakudya ,
E. Mukwevho ,
P. Nkomozepi  and
K. H. Erlwanger
T. T. Nyakudya*
Affiliation:
School of Physiology, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa Department of Human Anatomy and Physiology, Faculty of Health Sciences, University of Johannesburg, Johannesburg, South Africa
E. Mukwevho
Affiliation:
Department of Biology, Faculty of Agriculture, Science and Technology, North West University, Mmabatho, Mafikeng, South Africa
P. Nkomozepi
Affiliation:
Department of Human Anatomy and Physiology, Faculty of Health Sciences, University of Johannesburg, Johannesburg, South Africa
K. H. Erlwanger
Affiliation:
School of Physiology, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa
*
Address for correspondence: T. T. Nyakudya, School of Physiology, Faculty of Health Sciences, University of the Witwatersrand, 7 York Road, 2193, Johannesburg, South Africa. E-mail: trevorn@uj.ac.za
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Abstract

Dietary manipulations during the early postnatal period are associated with the development of metabolic disorders including non-alcoholic fatty liver disease (NAFLD) or long-term protection against metabolic dysfunction. We investigated the potential hepatoprotective effects of neonatal administration of oleanolic acid (OA), a phytochemical, on the subsequent development in adulthood, of dietary fructose-induced NAFLD. Male and female suckling rats (n=112) were gavaged with; distilled water (DW), OA (60 mg/kg), high fructose solution (HF; 20% w/v) and OA+HF (OAHF) for 7 days. The rats were weaned onto normal rat chow on day 21 up to day 55. From day 56, half of the rats in each treatment group were continued on plain water or HF as drinking fluid for 8 weeks. Hepatic lipid accumulation and hepatic histomorphometry were then determined. Fructose consumption in adulthood following neonatal fructose intake (HF+F) caused a 47–49% increase in hepatic lipid content of both male and female rats (P<0.05). However, fructose administered in adulthood only, caused a significant increase (P<0.05) in liver lipid content in females only. NAFLD activity scores for inflammation and steatosis were higher in the fructose-fed rats compared with other groups (P<0.05). Steatosis, low-grade inflammation and fibrosis were observed in rats that received HF+F. NAFLD area fraction for fibrosis was three times higher in rats that received fructose neonatally and in adulthood compared with the rats in the negative control group (P<0.05). Treatment with OA during a critical window of developmental plasticity in rats prevented the development of fructose-induced NAFLD.

Keywords

fructosemetabolic dysfunctionneonatal programmingnon-alcoholic fatty liver diseaseoleanolic acid
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 9 , Issue 5 , October 2018 , pp. 500 - 510
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2018 

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References

1. Basaranoglu, M, Basaranoglu, G, Bugianesi, E. Carbohydrate intake and nonalcoholic fatty liver disease: fructose as a weapon of mass destruction. Hepatobiliary Surg Nutr. 2014; 4, 109–116.Google Scholar
2. Li, Y-C, Hsieh, C-C. Lactoferrin dampens high-fructose corn syrup-induced hepatic manifestations of the metabolic syndrome in a murine model. PLoS One. 2014; 9, e97341.Google Scholar
3. Younossi, ZM, Stepanova, M, Rafiq, N, et al. Pathologic criteria for nonalcoholic steatohepatitis: interprotocol agreement and ability to predict liver‐related mortality. Hepatology. 2011; 53, 1874–1882.Google Scholar
4. Lonardo, A, Ballestri, S, Marchesini, G, Angulo, P, Loria, P. Nonalcoholic fatty liver disease: a precursor of the metabolic syndrome. Dig Liver Dis. 2015; 47, 181–190.Google Scholar
5. Asrih, M, Jornayvaz, FR. Metabolic syndrome and nonalcoholic fatty liver disease: is insulin resistance the link? Mol Cell Endocrinol. 2015; 418, 55–65.Google Scholar
6. Liang, W, Menke, AL, Driessen, A, et al. Establishment of a general NAFLD scoring system for rodent models and comparison to human liver pathology. PLoS One. 2014; 9, e115922.Google Scholar
7. Castro, GS, Cardoso, JF, Vannucchi, H, Zucoloto, S, Jordão, AA. Fructose and NAFLD: metabolic implications and models of induction in rats. Acta Cir Bras. 2011; 26, 45–50.Google Scholar
8. Dietrich, P, Hellerbrand, C. Non-alcoholic fatty liver disease, obesity and the metabolic syndrome. Best Pract Res Clin Gastroenterol. 2014; 28, 637–653.Google Scholar
9. Al Rifai, M, Silverman, MG, Nasir, K, et al. The association of nonalcoholic fatty liver disease, obesity, and metabolic syndrome, with systemic inflammation and subclinical atherosclerosis: the Multi-Ethnic Study of Atherosclerosis (MESA). Atherosclerosis. 2015; 239, 629–633.Google Scholar
10. Bellentani, S, Scaglioni, F, Marino, M, Bedogni, G. Epidemiology of non-alcoholic fatty liver disease. Dig Dis. 2010; 28, 155–161.Google Scholar
11. Tessari, P, Coracina, A, Cosma, A, Tiengo, A. Hepatic lipid metabolism and non-alcoholic fatty liver disease. Nutr Metabol Cardiovasc Dis. 2009; 19, 291–302.Google Scholar
12. Khitan, Z, Kim, DH. Fructose: a key factor in the development of metabolic syndrome and hypertension. J Nutr Metabol. 2013; 2013, 1–12.Google Scholar
13. Musso, G, Gambino, R, Cassader, M. Recent insights into hepatic lipid metabolism in non-alcoholic fatty liver disease (NAFLD). Prog Lipid Res. 2009; 48, 1–26.Google Scholar
14. Day, CP, James, OF. Steatohepatitis: A Tale of Two “Hits”? 1998; Gastroentorol. 1998; 114, 842–845.Google Scholar
15. James, O, Day, C. Non-alcoholic steatohepatitis: another disease of affluence. Lancet. 1999; 353, 1634–1636.Google Scholar
16. Rector, RS, Thyfault, JP, Wei, Y, Ibdah, JA. Non-alcoholic fatty liver disease and the metabolic syndrome: an update. World J Gastroenterol. 2008; 14, 185.Google Scholar
17. Vickers, MH. Developmental programming of the metabolic syndrome-critical windows for intervention. World J Diabetes. 2011; 2, 137–148.Google Scholar
18. Li, M, Reynolds, CM, Segovia, SA, Gray, C, Vickers, MH. Developmental programming of nonalcoholic fatty liver disease: the effect of early life nutrition on susceptibility and disease severity in later life. BioMed Res Int. 2015; 2015, 1–12.Google Scholar
19. Mortensen, OH, Larsen, LH, Ørstrup, LK, Hansen, LH, Grunnet, N, Quistorff, B. Developmental programming by high fructose decreases phosphorylation efficiency in aging offspring brain mitochondria, correlating with enhanced UCP5 expression. J Cereb Blood Flow Metab. 2014; 34, 1205–1211.Google Scholar
20. Tain, Y-L, Wu, KL, Lee, W-C, Leu, S, Chan, JY. Maternal fructose-intake-induced renal programming in adult male offspring. J Nutr Biochem. 2015; 26, 642–650.Google Scholar
21. Rodríguez, L, Panadero, MI, Roglans, N, et al. Fructose only in pregnancy provokes hyperinsulinemia, hypoadiponectinemia, and impaired insulin signaling in adult male, but not female, progeny. Eur J Nutr. 2016; 55, 665–674.Google Scholar
22. Clancy, B, Darlington, R, Finlay, B. Translating developmental time across mammalian species. Neuroscience. 2001; 105, 7–17.Google Scholar
23. Adams, L, Angulo, P. Treatment of non-alcoholic fatty liver disease. Postgrad Med J. 2006; 82, 315–322.Google Scholar
24. Harrison, SA. New treatments for nonalcoholic fatty liver disease. Cur Gastroenterol Rep. 2006; 8, 21–29.Google Scholar
25. Tolman, KG, Dalpiaz, AS. Treatment of non-alcoholic fatty liver disease. Ther Clin Risk Manag. 2007; 3, 1153–1163.Google Scholar
26. Castellano, JM, Guinda, A, Delgado, T, Rada, M, Cayuela, JA. Biochemical basis of the antidiabetic activity of oleanolic acid and related pentacyclic tritepenes. J Diab. 2013; 62, 1791–1799.Google Scholar
27. Liu, J. Pharmacology of oleanolic acid and ursolic acid. J Ethnopharmacol. 1995; 49, 57–68.Google Scholar
28. Camer, D, Yu, Y, Szabo, A, Huang, XF. The molecular mechanisms underpinning the therapeutic properties of oleanolic acid, its isomer and derivatives for type 2 diabetes and associated complications. Mol Nutr Food Res. 2014; 58, 1750–1759.Google Scholar
29. Lin, C, Wen, X, Sun, H. Oleanolic acid derivatives for pharmaceutical use: a patent review. Expert Opin Ther Pat. 2016; 26, 643–655.Google Scholar
30. Liu, J, Liu, Y, Klaassen, CD. Protective effect of oleanolic acid against chemical-induced acute necrotic liver injury in mice. Zhongguo yao li xue bao=Acta pharmacol Sin. 1995; 16, 97–102.Google Scholar
31. Musabayane, C, Tufts, M, Mapanga, R. Synergistic antihyperglycemic effects between plant-derived oleanolic acid and insulin in streptozotocin-induced diabetic rats. Ren Fail. 2010; 32, 832–839.Google Scholar
32. Zeng, X-Y, Wang, Y-P, Cantley, J, et al. Oleanolic acid reduces hyperglycemia beyond treatment period with Akt/FoxO1-induced suppression of hepatic gluconeogenesis in type-2 diabetic mice. PLoS One. 2012; 7, e42115.Google Scholar
33. Nkeh-Chungag, BN, Oyedeji, OO, Oyedeji, AO, Ndebia, EJ. Anti-inflammatory and membrane-stabilizing properties of two semisynthetic derivatives of oleanolic acid. Inflammation. 2015; 38, 61–69.Google Scholar
34. Tsao, S-M, Yin, M-C. Antioxidative and antiinflammatory activities of asiatic acid, glycyrrhizic acid, and oleanolic acid in human bronchial epithelial cells. J Agric Food Chem. 2015; 63, 3196–3204.Google Scholar
35. Yin, M-C, Chan, K-C. Nonenzymatic antioxidative and antiglycative effects of oleanolic acid and ursolic acid. J Agric Food Chem. 2007; 55, 7177–7181.Google Scholar
36. Liu, C, Li, Y, Zuo, G, et al. Oleanolic acid diminishes liquid fructose-induced fatty liver in rats: role of modulation of hepatic sterol regulatory element-binding protein-1c-mediated expression of genes responsible for de novo fatty acid synthesis. Evid Based Complement Alternat Med. 2013; 2013, 1–11.Google Scholar
37. Wang, J, Wu, Z, Li, D, et al. Nutrition, epigenetics, and metabolic syndrome. Antioxid Redox Signal. 2012; 17, 282–301.Google Scholar
38. Wang, X-M. Early life programming and metabolic syndrome. World J Pediatr. 2013; 9, 5–8.Google Scholar
39. Mock, K, Lateef, S, Benedito, VA, Tou, JC. High-fructose corn syrup-55 consumption alters hepatic lipid metabolism and promotes triglyceride accumulation. J Nutr Biochem. 2017; 39, 32–39.Google Scholar
40. Bancroft, JD, Gamble, M. Theory and Practice of Histological Techniques. 2008. Elsevier Churchill Livingstone: London.Google Scholar
41. Kleiner, DE, Brunt, EM, Van Natta, M, et al. Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology. 2005; 41, 1313–1321.Google Scholar
42. Schneider, CA, Rasband, WS, Eliceiri, KW. NIH image to ImageJ: 25 years of image analysis. Nature Methods. 2012; 9, 671.Google Scholar
43. Stewart, MS, Heerwagen, MJ, Friedman, JE. Developmental programming of pediatric non-alcoholic fatty liver disease: redefining the ‘first-hit’. Clin Obstet Gynecol. 2013; 56, 577.Google Scholar
44. Taqueti, VR, Bairey Merz, CN. Sex-Specific Precision Medicine: Targeting CRT-D and Other Cardiovascular Interventions to Those Most Likely to Benefit. 2017. Oxford University Press: Oxford.Google Scholar
45. Bruggeman, EC, Li, C, Ross, AP, et al. A high fructose diet does not affect amphetamine self-administration or spatial water maze learning and memory in female rats. Pharmacol Biochem Behav. 2011; 99, 356–364.Google Scholar
46. Rippe, JM, Angelopoulos, TJ. Sucrose, high-fructose corn syrup, and fructose, their metabolism and potential health effects: what do we really know? Adv Nutr Int Rev J. 2013; 4, 236–245.Google Scholar
47. Ayala, JE, Samuel, VT, Morton, GJ, et al. Standard operating procedures for describing and performing metabolic tests of glucose homeostasis in mice. Dis Model Mech. 2010; 3, 525–534.Google Scholar
48. Wang, X, Liu, R, Zhang, W, et al. Oleanolic acid improves hepatic insulin resistance via antioxidant, hypolipidemic and anti-inflammatory effects. Mol Cell Endocrinol. 2013; 376, 70–80.Google Scholar
49. Lê, K-A, Ith, M, Kreis, R, et al. Fructose overconsumption causes dyslipidemia and ectopic lipid deposition in healthy subjects with and without a family history of type 2 diabetes. Am J Clin Nutr. 2009; 89, 1760–1765.Google Scholar
50. Lim, JS, Mietus-Snyder, M, Valente, A, Schwarz, J-M, Lustig, RH. The role of fructose in the pathogenesis of NAFLD and the metabolic syndrome. Nat Rev Gastroenterol Hepatol. 2010; 7, 251–264.Google Scholar
51. Softic, S, Cohen, DE, Kahn, CR. Role of dietary fructose and hepatic de novo lipogenesis in fatty liver disease. Dig Dis Sci. 2016; 61, 1282–1293.Google Scholar
52. Honda, Y, Yoneda, M, Kessoku, T, et al. The characteristics of non‐obese NAFLD: effect of genetic and environmental factors. Hepatol Res. 2016; 46, 1011–1018.Google Scholar
53. Leitão, HS, Doblas, S, Garteiser, P, et al. Hepatic fibrosis, inflammation, and steatosis: influence on the MR viscoelastic and diffusion parameters in patients with chronic liver disease. Radiology. 2016; 151570.Google Scholar
54. Clayton, ZE, Vickers, MH, Bernal, A, Yap, C, Sloboda, DM. Early life exposure to fructose alters maternal, fetal and neonatal hepatic gene expression and leads to sex-dependent changes in lipid metabolism in rat offspring. PLoS One. 2015; 10, e0141962.Google Scholar
55. Rodríguez-Ortiz, D, Reyes-Pérez, A, León, P, et al. Assessment of two different diagnostic guidelines criteria (National Cholesterol Education Adult Treatment Panel III [ATP III] and International Diabetes Federation [IDF]) for the evaluation of metabolic syndrome remission in a longitudinal cohort of patients undergoing Roux-en-Y gastric bypass. Surgery. 2016; 159, 1121–1128.Google Scholar
56. Weston, SR, Leyden, W, Murphy, R, et al. Racial and ethnic distribution of nonalcoholic fatty liver in persons with newly diagnosed chronic liver disease. Hepatology. 2005; 41, 372–379.Google Scholar
57. Williams, CD, Stengel, J, Asike, MI, et al. Prevalence of nonalcoholic fatty liver disease and nonalcoholic steatohepatitis among a largely middle-aged population utilizing ultrasound and liver biopsy: a prospective study. Gastroenterology. 2011; 140, 124–131.Google Scholar
58. Caballería, L, Pera, G, Auladell, MA, et al. Prevalence and factors associated with the presence of nonalcoholic fatty liver disease in an adult population in Spain. Eur J Gastroenterol Hepatol. 2010; 22, 24–32.Google Scholar
59. Torres, DM, Williams, CD, Harrison, SA. Features, diagnosis, and treatment of nonalcoholic fatty liver disease. Clin Gastroenterol Hepatol. 2012; 10, 837–858.Google Scholar
60. Cichoż-Lach, H, Michalak, A. Oxidative stress as a crucial factor in liver diseases. World J Gastroenterol. 2014; 20, 8082.Google Scholar
61. Mulder, P. The contribution of metabolic and adipose tissue inflammation to non-alcoholic fatty liver disease. 2017, Doctoral thesis.Google Scholar
62. Mulder, P, Morrison, M, Wielinga, P, Van Duyvenvoorde, W, Kooistra, T, Kleemann, R. Surgical removal of inflamed epididymal white adipose tissue attenuates the development of non-alcoholic steatohepatitis in obesity. Int J Obes. 2016; 40, 675–684.Google Scholar
63. Seki, E, Schwabe, RF. Hepatic inflammation and fibrosis: functional links and key pathways. Hepatology. 2015; 61, 1066–1079.Google Scholar
64. Jaeschke, H, Wang, Y, Essani, N. Reactive oxygen species activate the transcription factor NF-KB in the liver by induction of lipid peroxidation. In Hepatology. 1996; pp. 445–445. WB Saunders Co Independence Square West Curtis Center: Philadelphia, PA.Google Scholar
65. Lettéron, P, Fromenty, B, Benoît, T, Degott, C, Pessayre, D. Acute and chronic hepatic steatosis lead to in vivo lipid peroxidation in mice. J Hepatol. 1996; 24, 200–208.Google Scholar
66. Reeves, HL, Friedman, SL. Activation of hepatic stellate cells—a key issue in liver fibrosis. Front Biosci. 2002; 7, 808–826.Google Scholar
67. Miller, A, Adeli, K. Dietary fructose and the metabolic syndrome. Cur Opin Gastroenterol. 2008; 24, 204–209.Google Scholar
68. Zarghani, SS, Soraya, H, Zarei, L, Alizadeh, M. Comparison of three different diet-induced non alcoholic fatty liver disease protocols in rats: a pilot study. Energy (Kcal/g). 2016; 3, 3.18.Google Scholar
69. Calvaruso, V, Craxì, A. Implication of normal liver enzymes in liver disease. J Viral Hepat. 2009; 16, 529–536.Google Scholar
70. Pearce, SG, Thosani, NC, Pan, J-J. Noninvasive biomarkers for the diagnosis of steatohepatitis and advanced fibrosis in NAFLD. Biomark Res. 2013; 1, 7.Google Scholar