Alcoholic vs non-alcoholic fatty liver in rats: Distinct differences in endocytosis and vesicle trafficking despite similar pathology

BMC Gastroenterology

Volumn 16, Issue 1, 2016, Pages

  Rasineni, Karuna ^a,b   Penrice, Daniel D ^a,b   Natarajan, Sathish Kumar ^d   McNiven, Mark A ^c   McVicker, Benita L ^a,b   Kharbanda, Kusum K ^a,b   Casey, Carol A ^a,b   Harris, Edward N ^d  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b VA NEBRASKA WESTERN IOWA HEALTH CARE SYSTEM   (United States)

^c MAYO GRADUATE SCHOOL   (United States)

^d UNIVERSITY OF NEBRASKA LINCOLN   (United States)

Author keywords

Alcoholic fatty liver disease (AFLD); Asialoglycoprotein receptor (ASGPR); Non alcohol fatty liver disease (NAFLD); RabGTPase proteins; Receptor mediated endocytosis

Indexed keywords

ASIALOGLYCOPROTEIN RECEPTOR; ASIALOOROSOMUCOID; GLUTATHIONE; LIPID; RAB PROTEIN; RAB18 PROTEIN; RAB7 PROTEIN; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; ADIPOPHILIN; ALANINE AMINOTRANSFERASE; ALCOHOL; ALKALINE PHOSPHATASE; BILE ACID; CHOLESTEROL; MEMBRANE PROTEIN; MESSENGER RNA; RAB18 PROTEIN, RAT; RAB3D PROTEIN, RAT; SERUM ALBUMIN; SOLVENT;

ALCOHOLIC FATTY LIVER; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARBONYLATION; CELL MIGRATION; CONTROLLED STUDY; ENDOCYTOSIS; FAT INTAKE; GENE EXPRESSION; HISTOLOGY; IMMUNOHISTOCHEMISTRY; INTERNALIZATION; LIPID PEROXIDATION; LIVER CELL; LIVER INJURY; NONALCOHOLIC FATTY LIVER; NONHUMAN; PATHOLOGY; PROTEIN FUNCTION; RAT; TRIACYLGLYCEROL BLOOD LEVEL; WESTERN BLOTTING; ANIMAL; COMPARATIVE STUDY; DISEASE MODEL; FATTY LIVER, ALCOHOLIC; GENETICS; LIPID DIET; METABOLISM; PHYSIOLOGY; TRANSPORT VESICLE;

ALANINE TRANSAMINASE; ALKALINE PHOSPHATASE; ANIMALS; ASIALOGLYCOPROTEIN RECEPTOR; BILE ACIDS AND SALTS; BLOTTING, WESTERN; CHOLESTEROL; DIET, HIGH-FAT; DISEASE MODELS, ANIMAL; ENDOCYTOSIS; ETHANOL; FATTY LIVER, ALCOHOLIC; HEPATOCYTES; IMMUNOHISTOCHEMISTRY; MEMBRANE PROTEINS; NON-ALCOHOLIC FATTY LIVER DISEASE; PERILIPIN-2; RAB GTP-BINDING PROTEINS; RAB3 GTP-BINDING PROTEINS; RATS; RNA, MESSENGER; SERUM ALBUMIN; SOLVENTS; TRANSPORT VESICLES; TRIGLYCERIDES;

EID: 84959199216     PISSN: None     EISSN: 1471230X     Source Type: Journal    
DOI: 10.1186/s12876-016-0433-4     Document Type: Article

References (51)

1. Angulo P, Lindor KD. Non-alcoholic fatty liver disease. J Gastroenterol Hepatol. 2002;17(Suppl):S186-90.
2. Lieber CS. Hepatic, metabolic and toxic effects of ethanol: 1991 update. Alcohol Clin Exp Res. 1991;15(4):573-92.
3. 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):1-26.
4. Heimbach J. Debate: A bridge too far-liver transplantation for nonalcoholic steatohepatitis will overwhelm the organ supply. Liver Transpl. 2014;20 Suppl 2:S32-7.
5. Chalasani N, Younossi Z, Lavine JE, Diehl AM, Brunt EM, Cusi K, et al. 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. 2012;55(6):2005-23.
6. Fernandez DJ, McVicker BL, Tuma DJ, Tuma PL. Ethanol selectively impairs clathrin-mediated internalization in polarized hepatic cells. Biochem Pharmacol. 2009;78(6):648-55.
7. McVicker BL, Casey CA. Effects of ethanol on receptor-mediated endocytosis in the liver. Alcohol. 1999;19(3):255-60.
8. McVicker BL, Tuma DJ, Kubik JA, Hindemith AM, Baldwin CR, Casey CA. The effect of ethanol on asialoglycoprotein receptor-mediated phagocytosis of apoptotic cells by rat hepatocytes. Hepatology. 2002;36(6):1478-87.
9. Rasineni K, McVicker BL, Tuma DJ, McNiven MA, Casey CA. Rab GTPases associate with isolated lipid droplets (LDs) and show altered content after ethanol administration: potential role in alcohol-impaired LD metabolism. Alcohol Clin Exp Res. 2014;38(2):327-35.
10. Tworek BL, Tuma DJ, Casey CA. Decreased binding of asialoglycoproteins to hepatocytes from ethanol-fed rats. Consequence of both impaired synthesis and inactivation of the asialoglycoprotein receptor. J Biol Chem. 1996;271(5):2531-8.
11. Kilkenny C, Browne WJ, Cuthill IC, Emerson M, Altman DG. Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLoS Biol. 2010;8(6):e1000412.
12. Casey CA, McVicker BL, Donohue Jr TM, McFarland MA, Wiegert RL, Nanji AA. Liver asialoglycoprotein receptor levels correlate with severity of alcoholic liver damage in rats. J Appl Physiol. 2004;96(1):76-80.
13. Lieber CS, DeCarli LM. Liquid diet technique of ethanol administration: 1989 update. Alcohol Alcohol. 1989;24(3):197-211.
14. Gopalakrishnan S, Harris EN. In vivo liver endocytosis followed by purification of liver cells by liver perfusion. J Vis Exp. 2011;10(57):3138.
15. Casey CA, Kragskow SL, Sorrell MF, Tuma DJ. Chronic ethanol administration impairs the binding and endocytosis of asialo-orosomucoid in isolated hepatocytes. J Biol Chem. 1987;262(6):2704-10.
16. Folch J, Lees M, Sloane Stanley GH. A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem. 1957;226(1):497-509.
17. Oka JA, Weigel PH. Recycling of the asialoglycoprotein receptor in isolated rat hepatocytes. Dissociation of internalized ligand from receptor occurs in two kinetically and thermally distinguishable compartments. J Biol Chem. 1983;258(17):10253-62.
18. Natarajan SK, Thangaraj KR, Eapen CE, Ramachandran A, Mukhopadhya A, Mathai M, et al. Liver injury in acute fatty liver of pregnancy: possible link to placental mitochondrial dysfunction and oxidative stress. Hepatology. 2010;51(1):191-200.
19. Mihara M, Uchiyama M. Determination of malonaldehyde precursor in tissues by thiobarbituric acid test. Anal Biochem. 1978;86(1):271-8.
20. Tietze F. Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione: applications to mammalian blood and other tissues. Anal Biochem. 1969;27(3):502-22.
21. Chaudhary A, Dhar P, Tomey S, Sachdev A, Agarwal A. Segment III cholangiojejunostomy for carcinoma of the gallbladder. World J Surg. 1997;21(8):866-70. discussion 870-861.
22. Li-Fern H, Rajasoorya C. The elevated serum alkaline phosphatase-the chase that led to two endocrinopathies and one possible unifying diagnosis. Eur J Endocrinol. 1999;140(2):143-7.
23. Canbakan B, Senturk H, Canbakan M, Toptas T, Tabak O, Balci H, et al. Is alanine aminotransferase level a surrogate biomarker of hepatic apoptosis in nonalcoholic fatty liver disease? Biomark Med. 2010;4(2):205-14.
24. Duryee MJ, Willis MS, Schaffert CS, Reidelberger RD, Dusad A, Anderson DR, et al. Precision-cut liver slices from diet-induced obese rats exposed to ethanol are susceptible to oxidative stress and increased fatty acid synthesis. Am J Physiol Gastrointest Liver Physiol. 2014;306(3):G208-17.
25. Duarte JA, Carvalho F, Pearson M, Horton JD, Browning JD, Jones JG, et al. A high-fat diet suppresses de novo lipogenesis and desaturation but not elongation and triglyceride synthesis in mice. J Lipid Res. 2014;55(12):2541-53.
26. Marchesini G, Brizi M, Morselli-Labate AM, Bianchi G, Bugianesi E, McCullough AJ, et al. Association of nonalcoholic fatty liver disease with insulin resistance. Am J Med. 1999;107(5):450-5.
27. Adiels M, Westerbacka J, Soro-Paavonen A, Hakkinen AM, Vehkavaara S, Caslake MJ, et al. Acute suppression of VLDL1 secretion rate by insulin is associated with hepatic fat content and insulin resistance. Diabetologia. 2007;50(11):2356-65.
28. Ramirez T, Longato L, Dostalek M, Tong M, Wands JR, de la Monte SM. Insulin resistance, ceramide accumulation and endoplasmic reticulum stress in experimental chronic alcohol-induced steatohepatitis. Alcohol Alcohol. 2013;48(1):39-52.
29. Paradies G, Paradies V, Ruggiero FM, Petrosillo G. Oxidative stress, cardiolipin and mitochondrial dysfunction in nonalcoholic fatty liver disease. World J Gastroenterol. 2014;20(39):14205-18.
30. Song BJ, Akbar M, Abdelmegeed MA, Byun K, Lee B, Yoon SK, et al. Mitochondrial dysfunction and tissue injury by alcohol, high fat, nonalcoholic substances and pathological conditions through post-translational protein modifications. Redox Biol. 2014;3:109-23.
31. Svegliati-Baroni G, Candelaresi C, Saccomanno S, Ferretti G, Bachetti T, Marzioni M, et al. A model of insulin resistance and nonalcoholic steatohepatitis in rats: role of peroxisome proliferator-activated receptor-alpha and n-3 polyunsaturated fatty acid treatment on liver injury. Am J Pathol. 2006;169(3):846-60.
32. Li Y, Hai J, Li L, Chen X, Peng H, Cao M, et al. Administration of ghrelin improves inflammation, oxidative stress, and apoptosis during and after non-alcoholic fatty liver disease development. Endocrine. 2013;43(2):376-86.
33. Grunnet N, Kondrup J. The effect of ethanol on the beta-oxidation of fatty acids. Alcohol Clin Exp Res. 1986;10(6 Suppl):64S-8.
34. Venkatesan S, Ward RJ, Peters TJ. Effect of chronic ethanol feeding on the hepatic secretion of very-low-density lipoproteins. Biochim Biophys Acta. 1988;960(1):61-6.
35. Nanji AA, Dannenberg AJ, Jokelainen K, Bass NM. Alcoholic liver injury in the rat is associated with reduced expression of peroxisome proliferator-alpha (PPARalpha)-regulated genes and is ameliorated by PPARalpha activation. J Pharmacol Exp Ther. 2004;310(1):417-24.
36. Lieber CS. Alcoholic fatty liver: its pathogenesis and mechanism of progression to inflammation and fibrosis. Alcohol. 2004;34(1):9-19.
37. Tessari P, Coracina A, Cosma A, Tiengo A. Hepatic lipid metabolism and non-alcoholic fatty liver disease. Nutr Metab Cardiovasc Dis. 2009;19(4):291-302.
38. Tiniakos DG, Vos MB, Brunt EM. Nonalcoholic fatty liver disease: pathology and pathogenesis. Annu Rev Pathol. 2010;5:145-71.
39. Uslusoy HS, Nak SG, Gulten M, Biyikli Z. Non-alcoholic steatohepatitis with normal aminotransferase values. World J Gastroenterol. 2009;15(15):1863-8.
40. Milstein HJ, Bloomer JR, Klatskin G. Serum bile acids in alcoholic liver disease. Comparison with histological features of the disease. Am J Dig Dis. 1976;21(4):281-5.
41. Trinchet JC, Gerhardt MF, Balkau B, Munz C, Poupon RE. Serum bile acids and cholestasis in alcoholic hepatitis. Relationship with usual liver tests and histological features. J Hepatol. 1994;21(2):235-40.
42. Singh DK, Rastogi A, Sakhuja P, Gondal R, Sarin SK. Comparison of clinical, biochemical and histological features of alcoholic steatohepatitis and non-alcoholic steatohepatitis in Asian Indian patients. Indian J Pathol Microbiol. 2010;53(3):408-13.
43. Samuel VT, Liu ZX, Qu X, Elder BD, Bilz S, Befroy D, et al. Mechanism of hepatic insulin resistance in non-alcoholic fatty liver disease. J Biol Chem. 2004;279(31):32345-53.
44. Frederich RC, Hamann A, Anderson S, Lollmann B, Lowell BB, Flier JS. Leptin levels reflect body lipid content in mice: evidence for diet-induced resistance to leptin action. Nat Med. 1995;1(12):1311-4.
45. Paulino G, Barbier de la Serre C, Knotts TA, Oort PJ, Newman JW, Adams SH, et al. Increased expression of receptors for orexigenic factors in nodose ganglion of diet-induced obese rats. Am J Physiol Endocrinol Metab. 2009;296(4):E898-903.
46. Rees GM, Miller JA, Casey CA, Tuma DJ. Chronic ethanol administration impairs degradation of formaldehyde-treated albumin by the perfused rat liver. Alcohol Clin Exp Res. 1993;17(6):1309-12.
47. Casey CA, Kragskow SL, Sorrell MF, Tuma DJ. Effect of chronic ethanol administration on total asialoglycoprotein receptor content and intracellular processing of asialoorosomucoid in isolated rat hepatocytes. Biochim Biophys Acta. 1990;1052(1):1-8.
48. Casey CA, Kragskow SL, Sorrell MF, Tuma DJ. Ethanol-induced impairments in receptor-mediated endocytosis of asialoorosomucoid in isolated rat hepatocytes: time course of impairments and recovery after ethanol withdrawal. Alcohol Clin Exp Res. 1989;13(2):258-63.
49. Lieber CS. Cytochrome P-4502E1: its physiological and pathological role. Physiol Rev. 1997;77(2):517-544.
50. Clemens DL, Casey CA, Sorrell MF, Tuma DJ. Ethanol oxidation mediates impaired hepatic receptormediated enocytosis. Alcohol Clin Exp Res. 1998;22(4):778-779.
51. Clemens DL, Tuma DJ, Casey CA. Cyanamide potentiates the ethanol-induced impairment of receptormediatedendocytosis in a recombinant hepatic cell line expressing alcohol dehydrogenase activity. Int JHepatol. 2012;2012:954157.