Preventive effects of citrulline on Western diet-induced non-alcoholic fatty liver disease in rats

British Journal of Nutrition

Volumn 116, Issue 2, 2016, Pages 191-203

  Jegatheesan, Prasanthi ^a   Beutheu, Stéphanie ^a   Freese, Kim ^a   Waligora Dupriet, Anne Judith ^a   Nubret, Esther ^a   Butel, Marie Jo ^a   Bergheim, Ina ^b   De Bandt, Jean Pascal ^a,c  

^a UNIVERSITÉ PARIS DESCARTES   (France)

^b FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^c ASSISTANCE PUBLIQUE HÔPITAUX DE PARIS   (France)

Author keywords

Gut permeability; Liver; Microbiota; Non alcoholic steatohepatitis; Non essential amino acids

Indexed keywords

CCAAT ENHANCER BINDING PROTEIN; CITRULLINE; CLAUDIN 1; GLUTATHIONE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; INSULIN; INTERLEUKIN 6; MESSENGER RNA; MYELOPEROXIDASE; PROTEIN ZO1; TOLL LIKE RECEPTOR 4; TRIACYLGLYCEROL; TUMOR NECROSIS FACTOR ALPHA; ANTIINFLAMMATORY AGENT; ANTIOXIDANT; FAT DROPLET; TUMOR NECROSIS FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTEROIDES; CONTROLLED STUDY; DRUG MECHANISM; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVITY; GENE EXPRESSION; HEPATITIS; INSULIN SENSITIVITY; INTESTINE FLORA; LIPID DIET; LIPID LIVER LEVEL; LIPID STORAGE; LIVER FUNCTION; MALE; NONALCOHOLIC FATTY LIVER; NONHUMAN; OBESITY; PREVOTELLA; PROTEIN EXPRESSION; RAT; SPRAGUE DAWLEY RAT; TRIACYLGLYCEROL BLOOD LEVEL; WESTERN DIET; ADVERSE EFFECTS; ANIMAL; BLOOD; COLON; DRUG EFFECTS; GROWTH, DEVELOPMENT AND AGING; INFLAMMATION; INSULIN RESISTANCE; LIVER; METABOLISM; MICROBIOLOGY; NON-ALCOHOLIC FATTY LIVER DISEASE;

ANIMALS; ANTI-INFLAMMATORY AGENTS; ANTIOXIDANTS; BACTEROIDES; CITRULLINE; CLAUDIN-1; COLON; DIET, WESTERN; ENDOPLASMIC RETICULUM STRESS; INFLAMMATION; INSULIN; INSULIN RESISTANCE; INTERLEUKIN-6; LIPID DROPLETS; LIVER; MALE; NON-ALCOHOLIC FATTY LIVER DISEASE; PREVOTELLA; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; TOLL-LIKE RECEPTOR 4; TRIGLYCERIDES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84969612602     PISSN: 00071145     EISSN: 14752662     Source Type: Journal    
DOI: 10.1017/S0007114516001793     Document Type: Article

References (65)

1. Tarantino G (2007) Should nonalcoholic fatty liver disease be regarded as a hepatic illness only? World J. Gastroenterol 13, 4669-4672
2. Pinzani M (2011) Pathophysiology of non-alcoholic steatohepatitis and basis for treatment. Dig Dis 29, 243-248
3. Zhang X-Q, Xu C-F, Yu C-H, et al. (2014) Role of endoplasmic reticulum stress in the pathogenesis of nonalcoholic fatty liver disease. World J Gastroenterol 20, 1768-1776
4. Takaki A, Kawai D &Yamamoto K (2014) Molecular mechanisms and new treatment strategies for non-alcoholic steatohepatitis (NASH). Int J Mol Sci 15, 7352-7379
5. Volynets V, Küper MA, Strahl S, et al. (2012) Nutrition, intestinal permeability, and blood ethanol levels are altered in patients with nonalcoholic fatty liver disease (NAFLD). Dig Dis Sci 57, 1932-1941
6. Sobrecases H, Lê K-A, Bortolotti M, et al. (2010) Effects of short-term overfeeding with fructose, fat and fructose plus fat on plasma and hepatic lipids in healthy men. Diabetes Metab 36, 244-246
7. Ilan Y (2012) Leaky gut and the liver: a role for bacterial translocation in nonalcoholic steatohepatitis. World J. Gastroenterol 18, 2609-2618
8. Chassaing B, Etienne-Mesmin L &Gewirtz AT (2014) Microbiota-liver axis in hepatic disease. Hepatology 59, 328-339
9. Thuy S, Ladurner R, Volynets V, et al. (2008) Nonalcoholic fatty liver disease in humans is associated with increased plasma endotoxin and plasminogen activator inhibitor 1 concentrations and with fructose intake. J Nutr 138, 1452-1455
10. Chalasani N, Younossi Z, Lavine JE, et al. (2012) The diagnosis and management of non-alcoholic fatty liver disease: practice Guideline by the American Association for the Study of Liver Diseases, American College of Gastroenterology, and the American Gastroenterological Association. Hepatology 55, 2005-2023
11. Theytaz F, Noguchi Y, Egli L, et al. (2012) Effects of supplementation with essential amino acids on intrahepatic lipid concentrations during fructose overfeeding in humans. Am J Clin Nutr 96, 1008-1016
12. Lee S-M, Han HW &Yim SY (2014) Beneficial effects of soy milk and fiber on high cholesterol diet-induced alteration of gut microbiota and inflammatory gene expression in rats. Food Funct 6, 492-500
13. Lopez-Legarrea P, Fuller NR, Zulet MA, et al. (2014) The influence of Mediterranean, carbohydrate and high protein diets on gut microbiota composition in the treatment of obesity and associated inflammatory state. Asia Pac J Clin Nutr 23, 360-368
14. Rhoads MJ &Wu G (2009) Glutamine, arginine, and leucine signaling in the intestine. Amino Acids 37, 111-122
15. Ginguet A, Cynober L &De Bandt J-P (2016) Indications for infusing individual amino acids (arginine, glutamine, taurine, carnitine, leucine, citrulline) in critical illness? Curr Opin Clin Nutr Metab Care 19, 161-169
16. Antunes MM, Leocádio PCL, Teixeira LG, et al. (2016) Pretreatment with L-citrulline positively affects the mucosal architecture and permeability of the small intestine in a murine mucositis model. J Parenter Enteral Nutr 40, 279-286
17. Lai C-H, Lee C-H, Hung C-Y, et al. (2015) Oral citrulline mitigates inflammation and jejunal damage via the inactivation of neuronal nitric oxide synthase and nuclear factor-κb in intestinal ischemia and reperfusion. J Parenter Enteral Nutr (Epublication ahead of print 30 June 2015)
18. Jegatheesan PP, Beutheu S, Ventura G, et al. (2015) Effect of specific amino acids on hepatic lipid metabolism in fructose-induced non-alcoholic fatty liver disease. Clin Nutr 35, 175-182
19. Jegatheesan P, Beutheu S, Ventura G, et al. (2015) Citrulline and nonessential amino acids prevent fructose-induced nonalcoholic fatty liver disease in rats. J. Nutr 145, 2273-2279
20. Osowska S, Moinard C, Neveux N, et al. (2004) Citrulline increases arginine pools and restores nitrogen balance after massive intestinal resection. Gut 53, 1781-1786
21. Ren W, Chen S, Yin J, et al. (2014) Dietary arginine supplementation of mice alters the microbial population and activates intestinal innate immunity. J Nutr 144, 988-995
22. Barone FC, Hillegass LM, Price WJ, et al. (1991) Polymorphonuclear leukocyte infiltration into cerebral focal ischemic tissue: myeloperoxidase activity assay and histologic verification. J Neurosci Res 29, 336-345
23. Beutheu Youmba S, Belmonte L, Galas L, et al. (2012) Methotrexate modulates tight junctions through NF-κB, MEK, and JNK pathways. J Pediatr Gastroenterol Nutr 54, 463-470
24. Kalach N, Kapel N, Waligora-Dupriet A-J, et al. (2013) Intestinal permeability and fecal eosinophil-derived neurotoxin are the best diagnosis tools for digestive non-IgE-mediated cow's milk allergy in toddlers. Clin Chem Lab Med 51, 351-361
25. Sailer M, Dahlhoff C, Giesbertz P, et al. (2013) Increased plasma citrulline in mice marks diet-induced obesity and may predict the development of the metabolic syndrome. PLOS ONE 8, e63950
26. Wu G, Bazer FW, Davis TA, et al. (2009) Arginine metabolism and nutrition in growth, health and disease. Amino Acids 37, 153-168
27. Vanni E, Rosso C, Mezzabotta L, et al. (2014) Metabolomic analysis identifies new biomarkers of liver damage in NAFLD. Hepatology 60, Suppl., 227A
28. Ibrahim M, Singh C, Ganie MA, et al. (2009) NASH: the hepatic injury of metabolic syndrome: a brief update. Int J Health Sci (Qassim) 3, 265-270
29. Moussaoui F, Binimbi A, Cottart CH, et al. (2009) Hepatoprotective effect of citrulline against ischemia-reperfusion injury in rat. J Hepatol 50, S68
30. Moran TH (2009) Fructose and satiety. J Nutr 139, 1253S-1256S
31. Tsuchiya H, Ebata Y, Sakabe T, et al. (2013) High-fat, highfructose diet induces hepatic iron overload via a hepcidinindependent mechanism prior to the onset of liver steatosis and insulin resistance in mice. Metab Clin Exp 62, 62-69
32. Zelber-Sagi S, Nitzan-Kaluski D, Goldsmith R, et al. (2007) Long term nutritional intake and the risk for non-alcoholic fatty liver disease (NAFLD): a population based study. J Hepatol 47, 711-717
33. Moinard C, Le Plenier S, Noirez P, et al. (2015) Citrulline supplementation induces changes in body composition and limits age-related metabolic changes in healthy male rats. J Nutr 145, 1429-1437
34. Joffin N, Jaubert A-M, Durant S, et al. (2014) Citrulline induces fatty acid release selectively in visceral adipose tissue from old rats. Mol Nutr Food Res 58, 1765-1775
35. Joffin N, Jaubert A-M, Durant S, et al. (2014) Citrulline reduces glyceroneogenesis and induces fatty acid release in visceral adipose tissue from overweight rats. Mol Nutr Food Res 58, 2320-2330
36. Joffin N, Jaubert A-M, Bamba J, et al. (2015) Acute induction of uncoupling protein 1 by citrulline in cultured explants of white adipose tissue from lean and high-fat-diet-fed rats. Adipocyte 4, 129-134
37. Garaulet M, Hernandez-Morante JJ, Lujan J, et al. (2006) Relationship between fat cell size and number and fatty acid composition in adipose tissue from different fat depots in overweight/obese humans. Int J Obes (Lond) 30, 899-905
38. Vasanthakumar A, Moro K, Xin A, et al. (2015) The transcriptional regulators IRF4, BATF and IL-33 orchestrate development and maintenance of adipose tissue-resident regulatory T cells. Nat Immunol 16, 276-285
39. Breuillard C, Bonhomme S, Couderc R, et al. (2015) In vitro antiinflammatory effects of citrulline on peritoneal macrophages in Zucker diabetic fatty rats. Br J Nutr 113, 120-124
40. Gaggini M, Morelli M, Buzzigoli E, et al. (2013) Non-alcoholic fatty liver disease (NAFLD) and its connection with insulin resistance, dyslipidemia, atherosclerosis and coronary heart disease. Nutrients 5, 1544-1560
41. De Moura RF, Ribeiro C, de Oliveira JA, et al. (2009) Metabolic syndrome signs in Wistar rats submitted to different high-fructose ingestion protocols. Br J Nutr 101, 1178-1184
42. Cynober L, Moinard C &De Bandt J-P (2010) The 2009 ESPEN Sir David Cuthbertson. Citrulline: a new major signaling molecule or just another player in the pharmaconutrition game? Clin Nutr 29, 545-551
43. Stephens FB, Chee C, Wall BT, et al. (2015) Lipid-induced insulin resistance is associated with an impaired skeletal muscle protein synthetic response to amino acid ingestion in healthy young men. Diabetes 64, 1615-1620
44. Dhar I, Dhar A, Wu L, et al. (2013) Increased methylglyoxal formation with upregulation of renin angiotensin system in fructose fed Sprague Dawley rats. PLOS ONE 8, e74212
45. Srinivas PR, Wagner AS, Reddy LV, et al. (1993) Serum alpha 2-HS-glycoprotein is an inhibitor of the human insulin receptor at the tyrosine kinase level. Mol Endocrinol 7, 1445-1455
46. Fabbrini E, Serafini M, Colic Baric I, et al. (2014) Effect of plasma uric acid on antioxidant capacity, oxidative stress, and insulin sensitivity in obese subjects. Diabetes 63, 976-981
47. Osowska S, Duchemann T, Walrand S, et al. (2006) Citrulline modulates muscle protein metabolism in old malnourished rats. Am J Physiol Endocrinol Metab 291, E582-E586
48. Tarantino G, Savastano S, Capone D, et al. (2011) Spleen: a new role for an old player? World J Gastroenterol 17, 3776-3784
49. Gao B (2004) Therapeutic potential of interleukin-6 in preventing obesity-and alcohol-associated fatty liver transplant failure. Alcohol 34, 59-65
50. Bian Z, Peng Y, You Z, et al. (2013) CCN1 expression in hepatocytes contributes to macrophage infiltration in nonalcoholic fatty liver disease in mice. J Lipid Res 54, 44-54
51. Ritze Y, Böhle M, Haub S, et al. (2013) Role of serotonin in fatty acid-induced non-alcoholic fatty liver disease in mice. BMC Gastroenterol 13, 169
52. Spruss A &Bergheim I (2009) Dietary fructose and intestinal barrier: potential risk factor in the pathogenesis of nonalcoholic fatty liver disease. J Nutr Biochem 20, 657-662
53. Hold GL (2014) Western lifestyle: a 'master' manipulator of the intestinal microbiota? Gut 63, 5-6
54. De Bandt J-P, Waligora-Dupriet A-J &Butel M-J (2011) Intestinal microbiota in inflammation and insulin resistance: relevance to humans. Curr Opin Clin Nutr Metab Care 14, 334-340
55. Mouzaki M, Comelli EM, Arendt BM, et al. (2013) Intestinal microbiota in patients with nonalcoholic fatty liver disease. Hepatology 58, 120-127
56. Raman M, Ahmed I, Gillevet PM, et al. (2013) Fecal microbiome and volatile organic compound metabolome in obese humans with nonalcoholic fatty liver disease. Clin Gastroenterol Hepatol 11, 868-875
57. Mazmanian SK, Liu CH, Tzianabos AO, et al. (2005) An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell 122, 107-118
58. Everard A, Belzer C, Geurts L, et al. (2013) Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc Natl Acad Sci U S A 110, 9066-9071
59. Zhang X, Shen D, Fang Z, et al. (2013) Human gut microbiota changes reveal the progression of glucose intolerance. PLOS ONE 8, e71108
60. Morizono H, Cabrera-Luque J, Shi D, et al. (2006) Acetylornithine transcarbamylase: a novel enzyme in arginine biosynthesis. J Bacteriol 188, 2974-2982
61. Xu Y, Labedan B &Glansdorff N (2007) Surprising arginine biosynthesis: a reappraisal of the enzymology and evolution of the pathway in microorganisms. Microbiol Mol Biol Rev 71, 36-47
62. Noack J, Kleessen B, Proll J, et al. (1998) Dietary guar gum and pectin stimulate intestinal microbial polyamine synthesis in rats. J Nutr 128, 1385-1391
63. Mong M, Chao C &Yin M (2011) Histidine and carnosine alleviated hepatic steatosis in mice consumed high saturated fat diet. Eur J Pharmacol 653, 82-88
64. Senthilkumar R, Viswanathan P &Nalini N (2003) Glycine modulates hepatic lipid accumulation in alcohol-induced liver injury. Pol J Pharmacol 55, 603-611
65. Caldow MK, Ham DJ, Godeassi DP, et al. (2015) Glycine supplementation during calorie restriction accelerates fat loss and protects against further muscle loss in obese mice. Clin Nutr (Epublication ahead of print 22 September 2015)