Damage to enteric neurons occurs in mice that develop fatty liver disease but not diabetes in response to a high-fat diet

Neurogastroenterology and Motility

Volumn 26, Issue 8, 2014, Pages 1188-1199

  Rivera, L R ^a   Leung, C ^b   Pustovit, R V ^a   Hunne, B L ^a   Andrikopoulos, S ^a   Herath, C ^b   Testro, A ^b   Angus, P W ^b   Furness, J B ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b AUSTIN HEALTH   (Australia)

Author keywords

Diabetes; Enteric nervous system; Fatty liver disease; Neuropathy

Indexed keywords

ADVERSE EFFECTS; ANIMAL; C57BL MOUSE; DIABETES MELLITUS; INSULIN RESISTANCE; INTESTINE; INTESTINE INNERVATION; LIPID DIET; MOUSE; NERVE CELL; NON-ALCOHOLIC FATTY LIVER DISEASE; PATHOLOGY;

ANIMALS; DIABETES MELLITUS; DIET, HIGH-FAT; ENTERIC NERVOUS SYSTEM; INSULIN RESISTANCE; INTESTINES; MICE; MICE, INBRED C57BL; NEURONS; NON-ALCOHOLIC FATTY LIVER DISEASE;

EID: 84904410273     PISSN: 13501925     EISSN: 13652982     Source Type: Journal    
DOI: 10.1111/nmo.12385     Document Type: Article

References (47)

1. Adams LA, Lindor KD. Nonalcoholic fatty liver disease. Ann Epidemiol 2007; 17: 863-9.
2. Law K, Brunt EM. Nonalcoholic fatty liver disease. Clin Liver Dis 2010; 14: 591-604.
3. Williams CD, Stengel O, Asike MI, Torres DM, Shaw J, Contreras M, Landt CL, Harrison SA. 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: 124-31.
4. Bugianesi E, Leone N, Vanni E, Marchesini G, Brunello F, Carucci P, Musso A, De Paolis P et al. Expanding the natural history of nonalcoholic steatohepatitis: from cryptogenic cirrhosis to hepatocellular carcinoma. Gastroenterology 2002; 123: 134-40.
5. Serfaty L, Lemoine M. Definition and natural history of metabolic steatosis: clinical aspects of NAFLD, NASH and cirrhosis. Diabetes Metab 2008; 34: 634-7.
6. Loomba R, Sanyal AJ. The global NAFLD epidemic. Nat Rev Gastroenterol Hepatol 2013; 10: 686-90.
7. Karlas T, Wiegand J, Berg T. Gastrointestinal complications of obesity: non-alcoholic fatty liver disease (NAFLD) and its sequelae. Best Pract Res Clin Gastroenterol 2013; 27: 195-208.
8. De Giorgio R, Camilleri M. Human enteric neuropathies: morphology and molecular pathology. Neurogastroenterol Motil 2004; 16: 515-31.
9. Belai A, Burnstock G. Selective damage of intrinsic calcitonin gene-related peptide-like immunoreactive enteric nerve fibers in streptozotocin-induced diabetic rats. Gastroenterology 1987; 92: 730-4.
10. Kashyap P, Farrugia G. Diabetic gastroparesis: what we have learned and had to unlearn in the past 5 years. Gut 2010; 59: 1716-26.
11. Chandrasekharan B, Anitha M, Blatt R, Shahnavaz N, Kooby D, Staley C, Mwangi S, Jones DP et al. Colonic motor dysfunction in human diabetes is associated with enteric neuronal loss and increased oxidative stress. Neurogastroenterol Motil 2011; 23: 131-e26.
12. Stenkamp-Strahm CM, Kappmeyer AJ, Schmalz JT, Gericke M, Balemba O. High-fat diet ingestion correlates with neuropathy in the duodenum myenteric plexus of obese mice with symptoms of type 2 diabetes. Cell Tissue Res 2013; 354: 381-94.
13. Wong N, Morahan G, Stathopoulos M, Proietto J, Andrikopoulos S. A novel mechanism regulating insulin secretion involving Herpud1 in mice. Diabetologia 2013; 56: 1569-76.
14. James J, Bosch KS, Aronson DC, Houtkooper JM. Sirius Red histophotometry and spectrophotometry of sections in the assessment of the collagen content of liver tissue and its application in growing rat liver. Liver 1990; 10: 1-5.
15. Leung C, Herath CB, Jia Z, Goodwin M, Mak KY, Watt MJ, Forbes JM, Angus PW. Dietary glycotoxins exacerbate progression of experimental fatty liver disease. J Hepatol 2014; 60: 832-8.
16. Kleiner DE, Brunt EM, Van Natta M, Behling C, Contos MJ, Cummings OW, Ferrell LD, Liu Y-C et al. Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology 2005; 41: 1313-21.
17. Rivera LR, Poole DP, Thacker M, Furness JB. The involvement of nitric oxide synthase neurons in enteric neuropathies. Neurogastroenterol Motil 2011; 23: 980-8.
18. Mao Y, Wang B, Kunze W. Characterization of myenteric sensory neurons in the mouse small intestine. J Neurophysiol 2006; 96: 998-1010.
19. Qu Z-D, Thacker M, Castelucci P, Bagyánszki M, Epstein ML, Furness JB. Immunohistochemical analysis of neuron types in the mouse small intestine. Cell Tissue Res 2008; 334: 147-61.
20. Watkins CC, Sawa A, Jaffrey S, Blackshaw S, Barrow RK, Snyder SH, Ferris CD. Insulin restores neuronal nitric oxide synthase expression and function that is lost in diabetic gastropathy. J Clin Invest 2000; 106: 373-84.
21. Pereira RVF, Tronchini EA, Tashima CM, Alves EPB, Lima MM, Zanoni JN. L-Glutamine supplementation prevents myenteric neuron loss and has gliatrophic effects in the ileum of diabetic rats. Dig Dis Sci 2011; 56: 3507-16.
22. Di Nardo G, Blandizzi C, Volta U, Colucci R, Stanghellini V, Barbara G, Del Tacca M, Tonini M et al. Review article: molecular, pathological and therapeutic features of human enteric neuropathies. Aliment Pharmacol Ther 2008; 28: 25-45.
23. Ferreira PEB, Lopes CRP, Alves AMP, Alves ÉPB, Linden DR, Zanoni JN, Buttow NC. Diabetic neuropathy: an evaluation of the use of quercetin in the cecum of rats. World J Gastroenterol 2013; 19: 6416-26.
24. Ma J, Checklin HL, Wishart JM, Stevens JE, Jones KL, Horowitz M, Meyer JH, Rayner CK. A randomised trial of enteric-coated nutrient pellets to stimulate gastrointestinal peptide release and lower glycaemia in type 2 diabetes. Diabetologia 2013; 56: 1236-42.
25. Elmadfa I, Kornsteiner M. Dietary fat intake - A global perspective. Ann Nutr Metab 2009; 54: 8-14.
26. Voss U, Sand E, Olde B, Ekblad E. Enteric neuropathy can be induced by high fat diet in vivo and palmitic acid exposure in vitro. PLoS ONE 2013; 8: e81413.
27. Lelliott C, Vidal-Puig AJ. Lipotoxicity, an imbalance between lipogenesis de novo and fatty acid oxidation. Int J Obesity 2004; 28: S22-8.
28. Malhi H, Gores GJ. Cellular and molecular mechanisms of liver injury. Gastroenterology 2008; 134: 1641-54.
29. Csak T, Ganz M, Pespisa J, Kodys K, Dolganiuc A, Szabo G. Fatty acid and endotoxin activate inflammasomes in mouse hepatocytes that release danger signals to stimulate immune cells. Hepatology 2011; 54: 133-44.
30. Almaguel FG, Liu J-W, Pacheco FJ, Casiano CA, De Leon M. Activation and reversal of lipotoxicity in PC12 and rat cortical cells following exposure to palmitic acid. J Neurosci Res 2009; 87: 1207-18.
31. Martínez de Morentin PB, Varela L, Fernø J, Nogueiras R, Diéguez C, López M. Hypothalamic lipotoxicity and the metabolic syndrome. Biochim Biophys Acta 2010; 1801: 350-61.
32. Rivera LR, Thacker M, Castelucci P, Bron R, Furness JB. The reactions of specific neuron types to intestinal ischemia in the guinea pig enteric nervous system. Acta Neuropathol 2009; 118: 261-70.
33. Mearin F, Mourelle M, Guarner F, Salas A, Riveros-Moreno V, Moncada S, Malagelada JR. Patients with achalasia lack nitric oxide synthase in the gastro-oesophageal junction. Eur J Clin Invest 1993; 23: 724-8.
34. De Giorgio R, Di Simone MP, Stanghellini V, Barbara G, Tonini M, Salvioli B, Mattioli S, Corinaldesi R. Esophageal and gastric nitric oxide synthesizing innervation in primary achalasia. Am J Gastroenterol 1999; 94: 2357-62.
35. Vanderwinden JM, Mailleux P, Schiffmann SN, Vanderhaeghen JJ, De Laet MH. Nitric oxide synthase activity in infantile hypertrophic pyloric stenosis. N Eng J Med 1992; 327: 511-5.
36. Furness JB. The enteric nervous system and neurogastroenterology. Nat Rev Gastroenterol Hepatol 2012; 9: 286-94.
37. Volynets V, Küper MA, Strahl S, Maier IB, Spruss A, Wagnerberger S, Konigsrainer A, Bischoff SC et al. Nutrition, intestinal permeability, and blood ethanol levels are altered in patients with nonalcoholic fatty liver disease (NAFLD). Dig Dis Sci 2012; 57: 1932-41.
38. Keast JR. Mucosal innervation and control of water and ion transport in the intestine. Rev Physiol Biochem Pharmacol 1987; 109: 1-59.
39. Lundgren O, Peregrin AT, Persson K, Kordasti S, Uhnoo I, Svensson L. Role of the enteric nervous system in the fluid and electrolyte secretion of rotavirus diarrhea. Science 2000; 287: 491-5.
40. Palmer JM, Wong Riley M, Sharkey KA. Functional alterations in jejunal myenteric neurons during inflammation in nematode-infected guinea pigs. Am J Physiol 1998; 275: G922-35.
41. Linden DR, Couvrette JM, Ciolino A, McQuoid C, Blaszyk H, Sharkey KA, Mawe GM. Indiscriminate loss of myenteric neurones in the TNBS-inflamed guinea-pig distal colon. Neurogastroenterol Motil 2005; 17: 751-60.
42. Nurgali K, Nguyen TV, Matsuyama H, Thacker M, Robbins HL, Furness JB. Phenotypic changes of morphologically identified guinea-pig myenteric neurons following intestinal inflammation. J Physiol (Lond) 2007; 583: 593-609.
43. Krauter EM, Strong DS, Brooks EM, Linden DR, Sharkey KA, Mawe GM. Changes in colonic motility and the electrophysiological properties of myenteric neurons persist following recovery from trinitrobenzene sulfonic acid colitis in the guinea pig. Neurogastroenterol Motil 2007; 19: 990-1000.
44. Lomax AE, O'Hara JR, Hyland NP, Mawe GM, Sharkey KA. Persistent alterations to enteric neural signaling in the guinea pig colon following the resolution of colitis. Am J Physiol 2007; 292: 482-91.
45. Pontell L, Castelucci P, Bagyanszki M, Jovic T, Thacker M, Nurgali K, Bron R, Furness JB. Structural changes in the epithelium of the small intestine and immune cell infiltration of enteric ganglia following acute mucosal damage and local inflammation. Virchows Arch 2009; 455: 55-65.
46. Fairman CL, Clagett Dame M, Lennon VA, Epstein ML. Appearance of neurons in the developing chick gut. Dev Dyn 1995; 204: 192-201.
47. Williamson S, Pompolo S, Furness JB. GABA and nitric oxide synthase immunoreactivities are colocalized in a subset of inhibitory motor neurons of the guinea-pig small intestine. Cell Tissue Res 1996; 284: 29-37.