Maraviroc, a CCR5 antagonist, ameliorates the development of hepatic steatosis in a mouse model of non-alcoholic fatty liver disease (NAFLD)

Journal of Antimicrobial Chemotherapy

Volumn 69, Issue 7, 2014, Pages 1903-1910

  Pérez Martínez, Laura ^a   Pérez Matute, Patricia ^a   Aguilera Lizarraga, Javier ^a   Rubio Mediavilla, Susana ^b   Narro, Judit ^a   Recio, Emma ^a   Ochoa Callejero, Laura ^a   Oteo, José Antonio ^a   Blanco, José Ramón ^a  

^a CENTER FOR BIOMEDICAL RESEARCH OF LA RIOJA CIBIR   (Spain)

^b HOSPITAL SAN PEDRO   (Spain)

Author keywords

CCL5; Chemokine; High fat diet; Mice models

Indexed keywords

ALANINE AMINOTRANSFERASE; CHEMOKINE RECEPTOR CCR5; GLUCOSE; LIVER PROTECTIVE AGENT; MARAVIROC; TRIACYLGLYCEROL; CYCLOHEXANE DERIVATIVE; TRIAZOLE DERIVATIVE;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY MASS; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; DRUG EFFECT; GLUCOSE BLOOD LEVEL; LIPID DIET; LIPID STORAGE; LIVER EXAMINATION; LIVER INJURY; LIVER PROTECTION; LIVER WEIGHT; MALE; MOUSE; NONALCOHOLIC FATTY LIVER; NONHUMAN; PATHOLOGY; PROTEIN EXPRESSION; STEATOSIS; TRIACYLGLYCEROL BLOOD LEVEL; ANIMAL; C57BL MOUSE; CYTOCHEMISTRY; DISEASE MODEL; DRUG EFFECTS; FATTY LIVER; LIVER; LIVER FUNCTION TEST;

ANIMALS; CYCLOHEXANES; DISEASE MODELS, ANIMAL; FATTY LIVER; HISTOCYTOCHEMISTRY; LIVER; LIVER FUNCTION TESTS; MALE; MICE, INBRED C57BL; NON-ALCOHOLIC FATTY LIVER DISEASE; TRIAZOLES;

EID: 84902435362     PISSN: 03057453     EISSN: 14602091     Source Type: Journal    
DOI: 10.1093/jac/dku071     Document Type: Article

References (47)

1. Angulo P. Nonalcoholic fatty liver disease. N Engl J Med 2002; 346: 1221-31.
2. Matteoni CA, Younossi ZM, Gramlich T et al. Nonalcoholic fatty liver disease: a spectrum of clinical and pathological severity. Gastroenterology 1999; 116: 1413-9.
3. Bugianesi E, Leone N, Vanni E et al. Expanding the natural history of nonalcoholic steatohepatitis: from cryptogenic cirrhosis to hepatocellular carcinoma. Gastroenterology 2002; 123: 134-40.
4. Bedogni G, Miglioli L, Masutti F et al. Prevalence of and risk factors for nonalcoholic fatty liver disease: the Dionysos nutrition and liver study. Hepatology 2005; 42: 44-52.
5. Cohen JC, Horton JD, Hobbs HH. Human fatty liver disease: old questions and new insights. Science 2011; 332: 1519-23.
6. Ratziu V, Bellentani S, Cortez-Pinto H et al. A position statement on NAFLD/NASH based on the EASL 2009 special conference. J Hepatol 2010; 53: 372-84.
7. Joshi D, O'Grady J, Dieterich D et al. Increasing burden of liver disease in patients with HIV infection. Lancet 2011; 377: 1198-209.
8. Gaslightwala I, Bini EJ. Impact of human immunodeficiency virus infection on the prevalence and severity of steatosis in patients with chronic hepatitis C virus infection. J Hepatol 2006; 44: 1026-32.
9. Bani-Sadr F, Carrat F, Bedossa P et al. Hepatic steatosis in HIV-HCV coinfected patients: analysis of risk factors. AIDS 2006; 20: 525-31.
10. McGovern BH, Ditelberg JS, Taylor LE et al. Hepatic steatosis is associated with fibrosis, nucleoside analogue use, and hepatitis C virus genotype 3 infection in HIV-seropositive patients. Clin Infect Dis 2006; 43: 365-72.
11. Macias J, Berenguer J, Japon MA et al. Hepatic steatosis and steatohepatitis in human immunodeficiency virus/hepatitis C viruscoinfected patients. Hepatology 2012; 56: 1261-70.
12. Machado MV, Oliveira AG, Cortez-Pinto H. Hepatic steatosis in patients coinfected with human immunodeficiency virus/hepatitis C virus: a meta-analysis of the risk factors. Hepatology 2010; 52: 71-8.
13. Sahin H, Trautwein C, Wasmuth HE. Functional role of chemokines in liver disease models. Nat Rev Gastroenterol Hepatol 2010; 7: 682-90.
14. Appay V, Rowland-Jones SL. RANTES: a versatile and controversial chemokine. Trends Immunol 2001; 22: 83-7.
15. Schwabe RF, Bataller R, Brenner DA. Human hepatic stellate cells express CCR5 and RANTES to induce proliferation and migration. Am J Physiol Gastrointest Liver Physiol 2003; 285: G949-58.
16. Nischalke HD, Nattermann J, Fischer HP et al. Semiquantitative analysis of intrahepatic CC-chemokine mRNAs in chronic hepatitis C. Mediators Inflamm 2004; 13: 357-9.
17. Seki E, De Minicis S, Gwak GY et al. CCR1 and CCR5 promote hepatic fibrosis in mice. J Clin Invest 2009; 119: 1858-70.
18. Desai MS, Mariscalco MM, Tawil A et al. Atherogenic diet-induced hepatitis is partially dependent on murine TLR4. J Leukoc Biol 2008; 83: 1336-44.
19. Wu H, Ghosh S, Perrard XD et al. T-cell accumulation and regulated on activation, normal T cell expressed and secreted upregulation in adipose tissue in obesity. Circulation 2007; 115: 1029-38.
20. Berres ML, Koenen RR, Rueland A et al. Antagonism of the chemokine Ccl5 ameliorates experimental liver fibrosis in mice. J Clin Invest 2010; 120: 4129-40.
21. Affo S, Bataller R. RANTES antagonism: a promising approach to treat chronic liver diseases. J Hepatol 2011; 55: 936-8.
22. Ochoa-Callejero L, Perez-Martinez L, Rubio-Mediavilla S et al. Maraviroc, a CCR5 antagonist, prevents development of hepatocellular carcinoma in a mouse model. PLoS One 2013; 8: e53992.
23. Stock MK, Hammerich L, do O NT et al. Met-CCL5 modifies monocyte subpopulations during liver fibrosis regression. Int J Clin Exp Pathol 2013; 6: 678-85.
24. Barashi N, Weiss ID, Wald O et al. Inflammation-induced hepatocellular carcinoma is dependent on CCR5 in mice. Hepatology 2013; 58: 1021-30.
25. Gilliam BL, Riedel DJ, Redfield RR. Clinical use of CCR5 inhibitors in HIV and beyond. J Transl Med 2011; 9 Suppl 1: S9.
26. Neff CP, Ndolo T, Tandon A et al. Oral pre-exposure prophylaxis by anti-retrovirals raltegravir and maraviroc protects against HIV-1 vaginal transmission in a humanized mouse model. PLoS One 2010; 5: e15257.
27. Matthews DR, Hosker JP, Rudenski AS et al. Homeostasis model assessment: insulin resistance and β-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 1985; 28: 412-9.
28. Valdecantos MP, Perez-Matute P, Gonzalez-Muniesa P et al. Lipoic acid administration prevents nonalcoholic steatosis linked to long-term high-fat feeding by modulating mitochondrial function. J Nutr Biochem 2012; 23: 1676-84.
29. 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: 1313-21.
30. de Alwis NM, Day CP. Non-alcoholic fatty liver disease: the mist gradually clears. J Hepatol 2008; 48 Suppl 1: S104-12.
31. Kitade H, Sawamoto K, Nagashimada M et al. CCR5 plays a critical role in obesity-induced adipose tissue inflammation and insulin resistance by regulating both macrophage recruitment and M1/M2 status. Diabetes 2012; 61: 1680-90.
32. Perez-Matute CP, Pé rez-Martínez L, Rus A et al. Maraviroc shows differential effects on glucose uptake and lipolysis in human subcutaneous cultured adipocytes in comparison with omental adipocytes. J Int AIDS Soc 2012; 15 Suppl 4: 18306.
33. Díaz-Delfin J, Domingo P, Giralt M et al. Maraviroc reduces cytokine expression and secretion in human adipose cells without altering adipogenic differentiation. Cytokine 2013; 61: 808-15.
34. Tien PC, Schneider MF, Cole SR et al. Antiretroviral therapy exposure and incidence of diabetes mellitus in the Women's Interagency HIV Study. AIDS 2007; 21: 1739-45.
35. Pfleger C, Kaas A, Hansen L et al. Relation of circulating concentrations of chemokine receptor CCR5 ligands to C-peptide, proinsulin and HbA1c and disease progression in type 1 diabetes. Clin Immunol 2008; 128: 57-65.
36. Bigoloni A, Gianotti N, Spagnuolo V et al. Long-term glucose tolerance in highly experienced HIV-infected patients receiving nucleoside analogue-sparing regimens. AIDS 2012; 26: 1837-40.
37. MacInnes A, Lazzarin A, Di Perri G et al. Maraviroc can improve lipid profiles in dyslipidemic patients with HIV: results from the MERIT trial. HIV Clin Trials 2011; 12: 24-36.
38. Cipriani S, Francisci D, Mencarelli A et al. Efficacy of the CCR5 antagonist maraviroc in reducing early, ritonavir-induced atherogenesis and advanced plaque progression in mice. Circulation 2013; 127: 2114-24.
39. Bertola A, Bonnafous S, Anty R et al. Hepatic expression patterns of inflammatory and immune response genes associated with obesity and NASH in morbidly obese patients. PLoS One 2010; 5: e13577.
40. Braunersreuther V, Viviani GL, Mach F et al. Role of cytokines and chemokines in non-alcoholic fatty liver disease. World J Gastroenterol 2012; 18: 727-35.
41. Kirovski G, Gabele E, Dorn C et al. Hepatic steatosis causes induction of the chemokine RANTES in the absence of significant hepatic inflammation. Int J Clin Exp Pathol 2010; 3: 675-80.
42. Crespo J, Cayon A, Fernandez-Gil P et al. Gene expression of tumor necrosis factor α and TNF-receptors, p55 and p75, in nonalcoholic steatohepatitis patients. Hepatology 2001; 34: 1158-63.
43. Hotamisligil GS, Shargill NS, Spiegelman BM. Adipose expression of tumor necrosis factor-α: direct role in obesity-linked insulin resistance. Science 1993; 259: 87-91.
44. Pinto Lde F, Compri CM, Fornari JV et al. The immunosuppressant drug, thalidomide, improves hepatic alterations induced by a high-fat diet in mice. Liver Int 2010; 30: 603-10.
45. Wieckowska A, Papouchado BG, Li Z et al. Increased hepatic and circulating interleukin-6 levels in human nonalcoholic steatohepatitis. Am J Gastroenterol 2008; 103: 1372-9.
46. Yamaguchi K, Itoh Y, Yokomizo C et al. Blockade of interleukin-6 signaling enhances hepatic steatosis but improves liver injury in methionine choline-deficient diet-fed mice. Lab Invest 2010; 90: 1169-78.
47. Nasta P, Gatti F, Borghi F et al. Liver stiffness (LS) change in HIV-hepatitis C (HCV) coinfected patients treated with CCR5 inhibitor based antiretroviral therapy. In: Abstracts of the Fifty-first Interscience Conference on Antimicrobial Agents and Chemotherapy, Chicago, IL, 2011. Abstract H3-810. American Society for Microbiology, Washington, DC, USA.