Increased sensitivity to binge alcohol-induced gut leakiness and inflammatory liver disease in HIV transgenic rats

PLoS ONE

Volumn 10, Issue 10, 2015, Pages

  Banerjee, Atrayee ^a   Abdelmegeed, Mohamed A ^a   Jang, Sehwan ^a   Song, Byoung Joon ^a  

^a NATIONAL INSTITUTE ON ALCOHOL ABUSE AND ALCOHOLISM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE AMINOTRANSFERASE; ALCOHOL; CHEMOKINE RECEPTOR CCR2; ENDOTOXIN; LEPTIN; LEPTIN RECEPTOR; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; TOLL LIKE RECEPTOR 4; TRIACYLGLYCEROL; CENTRAL DEPRESSANT AGENT;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ALCOHOL CONSUMPTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINGE DRINKING; CELL CULTURE; CONTROLLED STUDY; DISEASE PREDISPOSITION; ENTEROPATHY; FATTY LIVER; FEMALE; GENE EXPRESSION; GUT LEAKINESS; HEPATITIS; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; KUPFFER CELL; LIPID STORAGE; LIVER CELL; LIVER LEVEL; MOLECULAR BIOLOGY; MOUSE; NONHUMAN; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; SIMULATION; STAINING; TRANSGENIC RAT; UPREGULATION; WILD TYPE; ANIMAL; CHEMICALLY INDUCED; DOSE RESPONSE; DRUG EFFECTS; FISCHER 344 RAT; GENETICS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; INTESTINE; LIVER DISEASES, ALCOHOLIC; METABOLISM; PATHOLOGY; PERMEABILITY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VIROLOGY;

ANIMALS; CELLS, CULTURED; CENTRAL NERVOUS SYSTEM DEPRESSANTS; CHEMOKINE CCL2; DOSE-RESPONSE RELATIONSHIP, DRUG; ETHANOL; FEMALE; GENE EXPRESSION; HEPATOCYTES; HIV; HIV INFECTIONS; HUMANS; INTESTINAL DISEASES; INTESTINES; LEPTIN; LIVER DISEASES, ALCOHOLIC; PERMEABILITY; RATS, INBRED F344; RATS, TRANSGENIC; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TOLL-LIKE RECEPTOR 4;

EID: 84949035027     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0140498     Document Type: Article

References (71)

1. Centerfor Disease Control (CDC), Division of HIV/AIDS Prevention. HIV in the United States. 2011.
2. Petry NM (1999) Alcohol use in HIV patients: what we don't know may hurt us. Int J Std AIDS 10: 561-570. PMID: 10492422
3. Baum MK, Rafie C, Lai S, Sales S, Page JB, Campa A (2010) Alcohol use accelerates HIV disease progression. AIDS Res. Hum. Retroviruses 26: 511-518. doi: 10.1089/aid.2009.0211 PMID: 20455765
4. Conigliaro J, Gordon AJ, McGinnis KA, Rabeneck L, Justice AC, Veterans Aging Cohort 3-Site Study (2003) How harmful is hazadous alcohol use and abuse in HIV infection: do health care provides know who is at risk? J Acquir Immune Defic Syndr 33: 521-525. PMID: 12869842
5. Chang SL, Connaghan KP, Wei Y, Li MD (2014) NeuroHIV and use of addictive substances. Int Rev Neurobiol 118: 403-440. doi: 10.1016/B978-0-12-801284-0.00013-0 PMID: 25175871
6. Galvan FH, Bing EG, Fleishman JA, London AS, Caetano R, Burnam MA, et al. (2002) The prevalence of alcohol consumption and heavy drinking among people with HIV in the United States: results from the HIV cost and services utilization study. J Stud Alcohol 63:179-186. PMID: 12033694
7. Samet JH, Phillips SJ, Horton NJ, Traphagen ET, Freedberg KA(2004) Detecting alcohol problems in HIV-infected patients: use of the CAGE questionnaire. AIDS Res Hum Retroviruses 20:151-155. PMID: 15018702
8. Szabo G, Zakhari S(2011) Mechanisms of alcohol-mediated hepatotoxicity in human-immunodeficiency-virus-infected patients. World J Gastroenterol 17: 2500-2506. doi: 10.3748/wjg.v17.i20.2500 PMID: 21633654
9. Ioannou GN, Bryson CL, Weiss NS, Miller R, Scott JD, Boyko EJ (2013) The prevalence of cirrhosis and hepatocellular carcinoma in patients with human immunodeficiency virus infection. Hepatology 57: 249-257. doi: 10.1002/hep.25800 PMID: 22532055
10. Lucey M, Mathurin P, Morgan TR (2009) Alcoholic hepatitis. N Engl J Med 360: 2758-2769. doi: 10. 1056/NEJMra0805786 PMID: 19553649
11. Stickel F, Seitz HK (2010) Alcoholic steatohepatitis. Best Pract Res Clin Gastroenterol 24: 683-693. doi: 10.1016/j.bpg.2010.07.003 PMID: 20955970
12. Mandrekar P, Szabo G (2009) Signalling pathways in alcohol-induced liver inflammation. J. Hepatol 50:1258-1266. doi: 10.1016/j.jhep.2009.03.007 PMID: 19398236
13. Thakur V, McMullen MR, Pritchard MT, Nagy LE (2007) Regulation of macrophage activation in alcoholic liverdisease. J Gastroenterol Hepatol 22 Suppl 1: S53-56. PMID: 17567466
14. Afford SC, Fisher NC, Neil DA, Fear J, Brun P, Hubscher SG, et al. (1998) Distinct patterns of chemo-kine expression are associated with leukocyte recruitment in alcoholic hepatitis and alcoholic cirrhosis. J Pathol 186: 82-89. PMID: 9875144
15. Bautista AP (2002) Chronic alcohol intoxication primes Kupffer cells and endothelial cells for enhanced CC-chemokine production and concomitantly suppresses phagocytosis and chemotaxis. Front Biosci 7: a117-125. PMID: 12045006
16. Fisher NC, Neil DA, Williams A, Adams DH (1999) Serum concentrations and peripheral secretion of the beta chemokines monocyte chemoattractant protein 1 and macrophage inflammatory protein 1alpha in alcoholic liver disease. Gut 45: 416-420. PMID: 10446112
17. Mandrekar P, Ambade A, Lim A, Szabo G, Catalano D (2011) An essential role for monocyte chemoattractant protein-1 in alcoholic liver injury: regulation of proinflammatory cytokines and hepatic steatosis in mice. Hepatology 54: 2185-2197. doi: 10.1002/hep.24599 PMID: 21826694
18. Das S, Kumar A, Seth RK, Tokar E, Kadiiska MB, Waalkes MP, et al. (2013) Proinflammatory adipokine leptin mediates disinfection byproduct bromodichloromethane-induced early steatohepatitic injury in obesity. Toxicol Appl Pharmacol 269: 297-306. doi: 10.1016/j.taap.2013.02.003 PMID: 23438451
19. An L, Wang X, Cederbaum AI (2012) Cytokines in alcoholic liver disease. Arch Toxicol 86:1337-1348. doi: 10.1007/s00204-012-0814-6 PMID: 22367091
20. Bala S, Marcos M, Gattu A, Catalano D, Szabo G (2014) Acute binge drinking increases serum endotoxin and bacterial DNA levels in healthy individuals. PLoS One 9:e96864. doi: 10.1371/journal.pone. 0096864 PMID: 24828436
21. Tilg H, Moschen AR (2006) Adipocytokines: mediators linking adipose tissue, inflammation and immunity. Nat Rev Immunol. 6: 772-783. PMID: 16998510
22. Baumann H, Morella KK, White DW, Dembski M, Bailon PS, Kim H, et al. (1996) The full length leptin receptor has signaling capabilities of interlukin 6-type cytokine receptors. Proc Natl Acad Sci. 93: 8374-8378. PMID: 8710878
23. Fantuzzi G, Sennello JA, Batra A, Fedke I. Lehr HA, Zeitz M, et al. (2005) Defining the role of T cell-derived leptin in the modulation of hepatic or intestinal inflammation in mice. Clin Exp. Immunol. 142: 31-38. PMID: 16178853
24. Marra F (2002) Leptin and liver fibrosis: matterof fat. Gastroenterology. 122:1529-1532. PMID: 11984539
25. Yang SQ, Lin HZ, Lan MD, Clemens M, Diehl AM (1997) Obesity increases sensitivity to endotoxin liver injury: implications for the pathogenesis of steatohepatitis. Proc Natl Acad Sci USA. 94: 2557-2562. PMID: 9122234
26. Saxena NK, Ikeda K, Rockey DC, Friedman SL, Anania FA (2002) Leptin in hepatic fibrosis: evidence for increased collagen production in stellate cells and lean littermates of ob/ob mice. Hepatology. 35: 762-771. PMID: 11915021
27. Clary CR, Guidot DM, Bratina MA, Otis JS (2011) Chronic alcohol ingestion exacerbates skeletal muscle myopathy in HIV-1 transgenic rats. AIDS Res Ther 8: 30. doi: 10.1186/1742-6405-8-30 PMID: 21846370
28. Brailoiu E, Brailoiu GC, Mameli G, Dolei A, Sawaya BE, Dun NJ (2006) Acute exposure to ethanol potentiates human immunodeficiency virus type 1 Tat-induced Ca(2+) overload and neuronal death in cultured rat cortical neurons. J Neurovirol 12:17-24. PMID: 16595370
29. Fan X, Joshi PC, Koval M, Guidot DM (2011) Chronic alcohol ingestion exacerbates lung epithelial barrier dysfunction in HIV-1 transgenic rats. Alcohol Clin Exp Res 35:1866-1875. doi: 10.1111/j.1530-0277.2011.01531.x PMID: 21569054
30. Flora G, Pu H, Lee YW, Ravikumar R, Nath A, Hennig B, et al. (2005) Proinflammatory synergism of ethanol and HIV-1 Tat protein in brain tissue. Exp Neurol 191: 2-12. PMID: 15589507
31. Persidsky Y, Ho W, Ramirez SH, Potula R, Abood ME, Unterwald E, et al. (2011) HIV-1 infection and alcohol abuse: neurocognitive impairment, mechanisms of neurodegeneration and therapeutic interventions. Brain Behav Immunol 25 Suppl 1: S61-70.
32. Singh AK, Jiang Y, Gupta S (2007) Effects of chronic alcohol drinking on receptor-binding, internalization, and degradation of human immunodeficiency virus 1 envelope protein gp120 in hepatocytes. Alcohol 41: 591-606. PMID: 17980997
33. Singh AK, Gupta S, Jiang Y (2008) Oxidative stress and protein oxidation in the brain of water drinking and alcohol drinking rats administered the HIV envelope protein, gp120. J Neurochem 104:1478-1493. PMID: 18067547
34. Reid W, Sadowska M, Denaro F, Rao S, Foulke J, Hayes N, et al. (2001) An HIV-1 transgenic rat that develops HIV-related pathology and immunologic dysfunction. Proc Natl Acad Sci USA 98: 9271-9276. PMID: 11481487
35. Sun R, Park O, Horiguchi N, Kulkarni S, Jeong WI, Sun HY, et al. (2006) STAT1 contributes to dsRNA inhibition of liver regeneration after partial hepatectomy in mice. Hepatology 44: 955-966. PMID: 17006930
36. Moon KH, Hood BL, Kim BJ, Hardwick JP, Conrads TP, Veenstra TD, et al. (2006) Inactivation of oxidized and S-nitrosylated mitochondrial proteins in alcoholic fatty liver of rats. Hepatology 44:1218-1230. PMID: 17058263
37. Moon KH, Hood BL, Mukhopadhyay P, Rajesh M, Abdelmegeed MA, Kwon YI, et al. (2008a)Oxidative inactivation of key mitochondrial proteins leads to dysfunction and injury in hepatic ischemia reperfu-sion. Gastroenterology 135:1344-1357.
38. Abdelmegeed MA, Banerjee A, Jang S, Yoo SH, Yun JW, Gonzalez FJ, et al. (2013b)CYP2E1 potentiates binge alcohol-induced gut leakiness, steatohepatitis, and apoptosis. Free Radic Biol Med 65: 1238-1245.
39. Abdelmegeed MA, Jang S, Banerjee A, Hardwick JP, Song BJ (2013a) Robust protein nitration contributes to acetaminophen-induced mitochondrial dysfunction and acute liver injury. Free Radic Biol Med 60: 211-222
40. Banerjee A, Abdelmegeed MA, Jang S, Song BJ (2013) Zidovudine (AZT) and hepatic lipid accumulation: implication of inflammation, oxidative and endoplasmic reticulum stress mediators. PLoS One 8: e76850. doi: 10.1371/journal.pone.0076850 PMID: 24146933
41. Moon KH, Upreti VV, Yu LR, Lee IJ, Ye X, Eddington ND, et al. (2008b) Mechanism of 3, 4-methylene-dioxymethamphetamine (MDMA, ecstasy)-mediated mitochondrial dysfunction in rat liver. Proteomics 8: 3906-3918.
42. Bode C, Kugler V, Bode JC (1987) Endotoxemia in patients with alcoholic and non-alcoholic cirrhosis and in subjects with no evidence of chronic liver disease following acute alcohol excess. J Hepatol 4: 8-14. PMID: 3571935
43. Keshavarzian A, Farhadi A, Forsyth CB, Rangan J, Jakate S, Shaikh M, et al. (2009) Evidence that chronic alcohol exposure promotes intestinal oxidative stress, intestinal hyperpermeability and endotoxemia prior to development of alcoholic steatohepatitis in rats. J Hepatol 50: 538-547. doi: 10.1016/j. jhep.2008.10.028 PMID: 19155080
44. Szabo G, Csak T (2012) Inflammasomes in liver diseases. J Hepatol 57(3):642-654. doi: 10.1016/j. jhep.2012.03.035 PMID: 22634126
45. Peng J, Vigorito M, Liu X, Zhou D, Wu X, Chang SL (2010) The HIV-1 transgenic rats as a model for HIV-1 infected individuals on HAART J NeuroImmunol 218: 94-101. doi: 10.1016/j.jneuroim.2009.09. 014 PMID: 19913921
46. Hadigan C, Liebau J, Anderson R, Holalkere NS, Sahani DV (2007) Magnetic resonance spectroscopy of hepatic lipid content and associated risk factors in HIV infection. JAcqui Immune Defic Syndr 46: 312-317.
47. Sarkar S, Chang SL (2013) Ethanol concentration-dependent alterations in gene expression during acute binge drinking in the HIV-1 transgenic rat. Alcohol Clin Exp Res 37:1082-1090. doi: 10.1111/acer.12077 PMID: 23413777
48. Abdelmegeed MA, Banerjee A, Yoo SH, Jang S, Gonzalez FJ, Song BJ (2012) Critical role of cytochrome P450 2E1 (CYP2E1) in the development of high fat-induced non-alcoholic steatohepatitis. J Hepatol 57: 860-866. doi: 10.1016/j.jhep.2012.05.019 PMID: 22668639
49. Kwon HJ, Won YS, Park O, Chang B, Duryee MJ, Thiele GE, et al. (2014) Aldehyde dehydrogenase 2 deficiency ameliorates alcoholic fatty liver but worsens liver inflammation and fibrosis in mice. Hepatol-ogy 60:146-157. doi: 10.1002/hep.27036 PMID: 24492981
50. Nagano J, Shimizu M, Hara T, Shirakami Y, Kochi T, Nakamura N, et al. (2013) Effects of indoleamine 2, 3-dioxygenase deficiency on high-fat diet-induced hepatic inflammation. PLoS One 8: e73404. doi: 10.1371/journal.pone.0073404 PMID: 24039933
51. Zhong W, McClain CJ, Cave M, Kang YJ, Zhou Z (2010) The role of zinc deficiency in alcohol-induced intestinal barrier dysfunction. Am J Physiol Gastrointest Liver Physiol 298: G625-633. doi: 10.1152/ajpgi.00350.2009 PMID: 20167873
52. Fan X, Joshi PC, Koval M, Guidot DM (2011) Chronic alcohol ingestion exacerbates lung epithelial barrier dysfunction in HIV-1 transgenic rats. Alcohol Clin Exp Res. 35:1866-1875. doi: 10.1111/j.1530-0277.2011.01531.x PMID: 21569054
53. Dallasta LM, Pisarov LA, Esplen JE, Werley JV, Moses AV, Nelson JA, et al. (1999) Blood brain barrier tight junction disruption in human immunodeficiency virus-1 encephalitis. Am J Pathol. 155:1915-1927. PMID: 10595922
54. Banerjee A, Zhang X, Manda KR, Banks WA, Ercal N (2010) HIV proteins and methamphetamine in oxidative stress induced damage in the brain: potential role of thiol antioxidant N-acetylcysteine amide. Free Radic Biol Med. 48:1388-1398. doi: 10.1016/j.freeradbiomed.2010.02.023 PMID: 20188164
55. Brenchley JM, Price DA, Schacker TW, Asher TE, Silvestri G, Rao S, et al. (2006) Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med 12:1365-1371. PMID: 17115046
56. Nazli A, Chan O, Dobson-Belaire WN, Ouellet M, Tremblay MJ, Gray-Owen SD, et al. (2010) Exposure to HIV-1 directly impairs mucosal epithelial barrier integrity allowing microbial translocation. PLoS Pathol 6: e1000852.
57. Sandler NG, Douek DC (2012) Microbial translocation in HIV infection: causes, consequences and treatment opportunities. Nat Rev Microbiol 10: 655-666. doi: 10.1038/nrmicro2848 PMID: 22886237
58. da Silva Correia J, Soldau K, Christen U, Tobias PS, Ulevitch RJ (2001) Lipopolysaccharide is in close proximity to each of the proteins in its membrane receptor complex: Transfer from CD14 to TLR4 and MD-2. J Biol Chem 276: 21129-21135. PMID: 11274165
59. Lippai D, Bala S, Csak T, Kurt-Jones EA, Szabo G (2013) Chronic alcohol-induced microRNA-155 contributes to neuroinflammation in aTLR4-dependentmannerin mice. PLoS One 8: e70945. doi: 10. 1371/journal.pone.0070945 PMID: 23951048
60. Pascual M, Balino P, Aragon CM, Guerri C (2014) Cytokines and chemokines as biomarkers of etha-nol-induced neuroinflammation and anxiety related behavior: Role of TLR4 and TLR2. Neuropharmacology 89C: 352-359.
61. Paik YH, Schwabe RF, Bataller R, Russo MP, Jobin C, Brenner DA (2003) Toll-like receptor 4 mediates inflammatory signaling by bacterial lipopolysaccharide in human hepatic stellate cells. Hepatology 37: 1043-1055. PMID: 12717385
62. Poltorak A, He X, Smirnova I, Liu MY, Van Huffel C, Du X, et al. (1998) Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 282(5396): 2085-2088. PMID: 9851930
63. Schwandner R, Dziarski R, Wesche H, Rothe M, Kirschning CJ (1999) Peptidoglycan-and lipoteichoic acid-induced cell activation is mediated by toll-like receptor 2. J Biol Chem 274:17406-17409. PMID: 10364168
64. Baeck C, Wehr A, Karlmark KR, Heymann F, Vucur M, Gassler N, et al. (2012) Pharmacological inhibition of the chemokine CCL2 (MCP-1) diminishes liver macrophage infiltration and steatohepatitis in chronic hepatic injury. Gut 61: 416-426. doi: 10.1136/gutjnl-2011-300304 PMID: 21813474
65. Bautista AP (2000) Impact of alcohol on the ability of Kupffer cells to produce chemokines and its role in alcoholic liver disease. J Gastroenterol Hepatol 15: 349-356. PMID: 10824877
66. Seki E, de Minicis S, Inokuchi S, Taura K, Miyai K, van Rooijen N, et al. (2009) CCR2 promotes hepatic fibrosis in mice. Hepatology 50:185-197. doi: 10.1002/hep.22952 PMID: 19441102
67. Baeck C, Wei X, Bartneck M, Fech V, Heymann F, Gassler N, et al. (2014) Pharmacological inhibition of the chemokine C-C motif chemokine ligand 2 (monocyte chemoattractant protein 1) accelerates liver fibrosis regression by suppressing Ly-6C(+) macrophage infiltration in mice. Hepatology 59:1060-1072. doi: 10.1002/hep.26783 PMID: 24481979
68. Imajo K, Fujita K, Yoneda M, Nozaki Y, Ogawa Y, Shiohara Y, et al. (2012) Hyperresponsivity to low dose endotoxin during progression to nonalcoholic steatohepatitis is regulated by leptin-mediated signaling. Cell Metab. 16: 44-54. doi: 10.1016/j.cmet.2012.05.012 PMID: 22768838
69. Chen JX, Stinnett A (2008) Critical role of the NADPH oxidase subunitp47phox on vascularTLR expression and neointimal lesion formation in high fat diet induced obesity. Lab Invest. 88:1316-1328. doi: 10.1038/labinvest.2008.92 PMID: 18779779
70. Zhou Z, Neupane M, Zhou HR, Wu D, Chang CC, Moustaid-Moussa N, et al. (2012) Leptin differentially regulate STAT3 activation in ob/ob mouse adipose mesenchymal stem cells. Nutr Metab. 5:109.
71. Miura K, Yang L, van Rooijen N, Ohnishi H, Seki E(2012) Hepatic recruitment of macrophages promoted nonalcoholic steatohepatitis through CCR2. Am J Physiol Gastrointest Liver Physiol. 302: G1310-1321. doi: 10.1152/ajpgi.00365.2011 PMID: 22442158