Connexin32 deficiency exacerbates carbon tetrachloride-induced hepatocellular injury and liver fibrosis in mice

References

• Adams LA. (2011). Biomarkers of liver fibrosis. J Gastroenterol Hepatol 26:802–9.
   PubMed Web of Science ®Google Scholar
• Asamoto M, Hokaiwado N, Murasaki T, Shirai T. (2004). Connexin 32 dominant-negative mutant transgenic rats are resistant to hepatic damage by chemicals. Hepatology 40:205–10.
   PubMed Web of Science ®Google Scholar
• Ayala A, Muñoz MF, Argüelles S. (2014). Lipid peroxidation: production, metabolism, and signaling mechanisms of malondialdehyde and 4-hydroxy-2-nonenal. Oxid Med Cell Longev 2014:Article ID 360438. doi:10.1155/2014/360438.
   PubMed Web of Science ®Google Scholar
• Basu S. (2003). Carbon tetrachloride-induced lipid peroxidation: eicosanoid formation and their regulation by antioxidant nutrients. Toxicology 189:113–27.
   PubMed Web of Science ®Google Scholar
• Beste LA, Leipertz SL, Green PK, et al. (2015). Trends in burden of cirrhosis and hepatocellular carcinoma by underlying liver disease in US veterans, 2001–2013. Gastroenterology 149:1471–82.e1475.
   PubMed Web of Science ®Google Scholar
• Blachier M, Leleu H, Peck-Radosavljevic M, et al. (2013). The burden of liver disease in Europe: a review of available epidemiological data. J Hepatol 58:593–608.
   PubMed Web of Science ®Google Scholar
• Bode HP, Wang L, Cassio D, et al. (2002). Expression and regulation of gap junctions in rat cholangiocytes. Hepatology 36:631–40.
   PubMed Web of Science ®Google Scholar
• Bonaventura J, Schroeder WA, Fang S. (1972). Human erythrocyte catalase: an improved method of isolation and a reevaluation of reported properties. Arch Biochem Biophys 150:606–17.
   PubMed Web of Science ®Google Scholar
• Bradford MM. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–54.
   PubMed Web of Science ®Google Scholar
• Brosnan CF, Scemes E, Spray DC. (2001). Cytokine regulation of gap junction connectivity: an open-and-shut case or changing partners at the Nexus? Am J Pathol 158:1565–9.
   PubMed Web of Science ®Google Scholar
• Bustin SA, Benes V, Garson JA, et al. (2009). The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55:611–22.
   PubMed Web of Science ®Google Scholar
• Canbay A, Higuchi H, Bronk SF, et al. (2002). Fas enhances fibrogenesis in the bile duct ligated mouse: a link between apoptosis and fibrosis. Gastroenterology 123:1323–30.
   PubMed Web of Science ®Google Scholar
• Cogliati B, Da Silva TC, Aloia TP, et al. (2011). Morphological and molecular pathology of CCL4-induced hepatic fibrosis in connexin43-deficient mice. Microsc Res Tech 74:421–9.
   PubMed Web of Science ®Google Scholar
• Cogliati B, Pereira HeM, Dagli ML, et al. (2010). Hepatotrophic factors reduce hepatic fibrosis in rats. Arq Gastroenterol 47:79–85.
   PubMedGoogle Scholar
• Cowles C, Mally A, Chipman JK. (2007). Different mechanisms of modulation of gap junction communication by non-genotoxic carcinogens in rat liver in vivo. Toxicology 238:49–59.
   PubMed Web of Science ®Google Scholar
• Dagli ML, Yamasaki H, Krutovskikh V, Omori Y. (2004). Delayed liver regeneration and increased susceptibility to chemical hepatocarcinogenesis in transgenic mice expressing a dominant-negative mutant of connexin32 only in the liver. Carcinogenesis 25:483–92.
   PubMed Web of Science ®Google Scholar
• de Gouville AC, Boullay V, Krysa G, et al. (2005). Inhibition of TGF-beta signaling by an ALK5 inhibitor protects rats from dimethylnitrosamine-induced liver fibrosis. Br J Pharmacol 145:166–77.
   PubMed Web of Science ®Google Scholar
• De Maio A, Gingalewski C, Theodorakis NG, Clemens MG. (2000). Interruption of hepatic gap junctional communication in the rat during inflammation induced by bacterial lipopolysaccharide. Shock 14:53–9.
   PubMed Web of Science ®Google Scholar
• Evert M, Ott T, Temme A, et al. (2002). Morphology and morphometric investigation of hepatocellular preneoplastic lesions and neoplasms in connexin32-deficient mice. Carcinogenesis 23:697–703.
   PubMed Web of Science ®Google Scholar
• Ewing JF, Janero DR. (1995). Microplate superoxide dismutase assay employing a nonenzymatic superoxide generator. Anal Biochem 232:243–8.
   PubMed Web of Science ®Google Scholar
• Fischer R, Reinehr R, Lu TP, et al. (2005). Intercellular communication via gap junctions in activated rat hepatic stellate cells. Gastroenterology 128:433–48.
   PubMed Web of Science ®Google Scholar
• Flohé L, Günzler WA. (1984). Assays of glutathione peroxidase. Methods Enzymol 105:114–21.
   PubMed Web of Science ®Google Scholar
• Friedman SL. (2008). Mechanisms of hepatic fibrogenesis. Gastroenterology 134:1655–69.
   PubMed Web of Science ®Google Scholar
• Frossard JL, Rubbia-Brandt L, Wallig MA, et al. (2003). Severe acute pancreatitis and reduced acinar cell apoptosis in the exocrine pancreas of mice deficient for the Cx32 gene. Gastroenterology 124:481–93.
   PubMed Web of Science ®Google Scholar
• Fukuda T, Ikejima K, Hirose M, et al. (2000). Taurine preserves gap junctional intercellular communication in rat hepatocytes under oxidative stress. J Gastroenterol 35:361–8.
   PubMed Web of Science ®Google Scholar
• Gieling RG, Wallace K, Han YP. (2009). Interleukin-1 participates in the progression from liver injury to fibrosis. Am J Physiol Gastrointest Liver Physiol 296:G1324–31.
   PubMed Web of Science ®Google Scholar
• Gingalewski C, Wang K, Clemens MG, De Maio A. (1996). Posttranscriptional regulation of connexin 32 expression in liver during acute inflammation. J Cell Physiol 166:461–7.
   PubMed Web of Science ®Google Scholar
• González HE, Eugenín EA, Garcés G, et al. (2002). Regulation of hepatic connexins in cholestasis: possible involvement of Kupffer cells and inflammatory mediators. Am J Physiol Gastrointest Liver Physiol 282:G991–1001.
   PubMed Web of Science ®Google Scholar
• Gross A, Yin XM, Wang K, et al. (1999). Caspase cleaved BID targets mitochondria and is required for cytochrome c release, while BCL-XL prevents this release but not tumor necrosis factor-R1/Fas death. J Biol Chem 274:1156–63.
   PubMed Web of Science ®Google Scholar
• Hartley DP, Kolaja KL, Reichard J, Petersen DR. (1999). 4-Hydroxynonenal and malondialdehyde hepatic protein adducts in rats treated with carbon tetrachloride: immunochemical detection and lobular localization. Toxicol Appl Pharmacol 161:23–33.
   PubMed Web of Science ®Google Scholar
• Hikita H, Takehara T, Kodama T, et al. (2011). Delayed-onset caspase-dependent massive hepatocyte apoptosis upon Fas activation in Bak/Bax-deficient mice. Hepatology 54:240–51.
   PubMed Web of Science ®Google Scholar
• Hong YL, Yeh SL, Chang CY, Hu ML. (2000). Total plasma malondialdehyde levels in 16 Taiwanese college students determined by various thiobarbituric acid tests and an improved high-performance liquid chromatography-based method. Clin Biochem 33:619–25.
   PubMed Web of Science ®Google Scholar
• Igarashi I, Maejima T, Kai K, et al. (2014). Role of connexin 32 in acetaminophen toxicity in a knockout mice model. Exp Toxicol Pathol 66:103–10.
   PubMed Web of Science ®Google Scholar
• Ishak K, Baptista A, Bianchi L, et al. (1995). Histological grading and staging of chronic hepatitis. J Hepatol 22:696–9.
   PubMed Web of Science ®Google Scholar
• Iwaisako K, Jiang C, Zhang M, et al. (2014). Origin of myofibroblasts in the fibrotic liver in mice. Proc Natl Acad Sci U S A 111:E3297–305.
   PubMed Web of Science ®Google Scholar
• Kar R, Batra N, Riquelme MA, Jiang JX. (2012). Biological role of connexin intercellular channels and hemichannels. Arch Biochem Biophys 524:2–15.
   PubMed Web of Science ®Google Scholar
• Knittel T, Müller L, Saile B, Ramadori G. (1997). Effect of tumour necrosis factor-alpha on proliferation, activation and protein synthesis of rat hepatic stellate cells. J Hepatol 27:1067–80.
   PubMed Web of Science ®Google Scholar
• Kojima T, Mitaka T, Mizuguchi T, Mochizuki Y. (1996). Effects of oxygen radical scavengers on connexins 32 and 26 expression in primary cultures of adult rat hepatocytes. Carcinogenesis 17:537–44.
   PubMed Web of Science ®Google Scholar
• Kojima T, Mochizuki C, Mitaka T, Mochizuki Y. (1997). Effects of melatonin on proliferation, oxidative stress and Cx32 gap junction protein expression in primary cultures of adult rat hepatocytes. Cell Struct Funct 22:347–56.
   PubMed Web of Science ®Google Scholar
• Lardinois OM, Mestdagh MM, Rouxhet PG. (1996). Reversible inhibition and irreversible inactivation of catalase in presence of hydrogen peroxide. Biochim Biophys Acta 1295:222–38.
   PubMed Web of Science ®Google Scholar
• Lee TF, Lin YL, Huang YT. (2011). Kaerophyllin inhibits hepatic stellate cell activation by apoptotic bodies from hepatocytes. Liver Int 31:618–29.
   PubMed Web of Science ®Google Scholar
• Liang B, Guo XL, Jin J, et al. (2015). Glycyrrhizic acid inhibits apoptosis and fibrosis in carbon-tetrachloride-induced rat liver injury. World J Gastroenterol 21:5271–80.
   PubMed Web of Science ®Google Scholar
• Livak KJ, Schmittgen TD. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402–8.
   PubMed Web of Science ®Google Scholar
• Louis H, Van Laethem JL, Wu W, et al. (1998). Interleukin-10 controls neutrophilic infiltration, hepatocyte proliferation, and liver fibrosis induced by carbon tetrachloride in mice. Hepatology 28:1607–15.
   PubMed Web of Science ®Google Scholar
• Lozano R, Naghavi M, Foreman K, et al. (2012). Global and regional mortality from 235 causes of death for 20 age groups in 1990 and 2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet 380:2095–128.
   PubMed Web of Science ®Google Scholar
• Luckey SW, Petersen DR. (2001). Activation of Kupffer cells during the course of carbon tetrachloride-induced liver injury and fibrosis in rats. Exp Mol Pathol 71:226–40.
   PubMed Web of Science ®Google Scholar
• Maes M, Crespo Yanguas S, Willebrords J, et al. (2015). Connexin and pannexin signaling in gastrointestinal and liver disease. Transl Res 166:332–43.
   PubMed Web of Science ®Google Scholar
• Maes M, Decrock E, Cogliati B, et al. (2014). Connexin and pannexin (hemi)channels in the liver. Front Physiol 4:405.
   PubMed Web of Science ®Google Scholar
• Miyashita T, Takeda A, Iwai M, Shimazu T. (1991). Single administration of hepatotoxic chemicals transiently decreases the gap-junction-protein levels of connexin 32 in rat liver. Eur J Biochem 196:37–42.
   PubMedGoogle Scholar
• Muriel P. (2009). Role of free radicals in liver diseases. Hepatol Int 3:526–36.
   PubMed Web of Science ®Google Scholar
• Naiki-Ito A, Asamoto M, Naiki T, et al. (2010). Gap junction dysfunction reduces acetaminophen hepatotoxicity with impact on apoptotic signaling and connexin 43 protein induction in rat. Toxicol Pathol 38:280–6.
   PubMed Web of Science ®Google Scholar
• Nakashima Y, Ono T, Yamanoi A, et al. (2004). Expression of gap junction protein connexin32 in chronic hepatitis, liver cirrhosis, and hepatocellular carcinoma. J Gastroenterol 39:763–8.
   PubMed Web of Science ®Google Scholar
• Nakata Y, Iwai M, Kimura S, Shimazu T. (1996). Prolonged decrease in hepatic connexin32 in chronic liver injury induced by carbon tetrachloride in rats. J Hepatol 25:529–37.
   PubMed Web of Science ®Google Scholar
• Nelles E, Bützler C, Jung D, et al. (1996). Defective propagation of signals generated by sympathetic nerve stimulation in the liver of connexin32-deficient mice. Proc Natl Acad Sci U S A 93:9565–70.
   PubMed Web of Science ®Google Scholar
• Nicholson B, Dermietzel R, Teplow D, et al. (1987). Two homologous protein components of hepatic gap junctions. Nature 329:732–4.
   PubMed Web of Science ®Google Scholar
• Nieto N, Friedman SL, Cederbaum AI. (2002a). Cytochrome P450 2E1-derived reactive oxygen species mediate paracrine stimulation of collagen I protein synthesis by hepatic stellate cells. J Biol Chem 277:9853–64.
   PubMed Web of Science ®Google Scholar
• Nieto N, Friedman SL, Cederbaum AI. (2002b). Stimulation and proliferation of primary rat hepatic stellate cells by cytochrome P450 2E1-derived reactive oxygen species. Hepatology 35:62–73.
   PubMed Web of Science ®Google Scholar
• Pillai AA, Levitsky J. (2009). Overview of immunosuppression in liver transplantation. World J Gastroenterol 15:4225–33.
   PubMed Web of Science ®Google Scholar
• Poupon R. (2015). Liver alkaline phosphatase: a missing link between choleresis and biliary inflammation. Hepatology 61:2080–90.
   PubMed Web of Science ®Google Scholar
• Rock KL, Kono H. (2008). The inflammatory response to cell death. Annu Rev Pathol 3:99–126.
   PubMed Web of Science ®Google Scholar
• Sewnath ME, Van Der Poll T, Van Noorden CJ, et al. (2002). Endogenous interferon gamma protects against cholestatic liver injury in mice. Hepatology 36:1466–77.
   PubMed Web of Science ®Google Scholar
• Simeonova PP, Gallucci RM, Hulderman T, et al. (2001). The role of tumor necrosis factor-alpha in liver toxicity, inflammation, and fibrosis induced by carbon tetrachloride. Toxicol Appl Pharmacol 177:112–20.
   PubMed Web of Science ®Google Scholar
• Szymonik-Lesiuk S, Czechowska G, Stryjecka-Zimmer M, et al. (2003). Catalase, superoxide dismutase, and glutathione peroxidase activities in various rat tissues after carbon tetrachloride intoxication. J Hepatobiliary Pancreat Surg 10:309–15.
   PubMedGoogle Scholar
• Takehara T, Tatsumi T, Suzuki T, et al. (2004). Hepatocyte-specific disruption of Bcl-xL leads to continuous hepatocyte apoptosis and liver fibrotic responses. Gastroenterology 127:1189–97.
   PubMed Web of Science ®Google Scholar
• Temme A, Buchmann A, Gabriel HD, et al. (1997). High incidence of spontaneous and chemically induced liver tumors in mice deficient for connexin32. Curr Biol 7:713–6.
   PubMed Web of Science ®Google Scholar
• Theodorakis NG, De Maio A. (1999). Cx32 mRNA in rat liver: effects of inflammation on poly(A) tail distribution and mRNA degradation. Am J Physiol 276:R1249–57.
   PubMed Web of Science ®Google Scholar
• Torres LL, Quaglio NB, de Souza GT, et al. (2011). Peripheral oxidative stress biomarkers in mild cognitive impairment and Alzheimer’s disease. J Alzheimers Dis 26:59–68.
   PubMed Web of Science ®Google Scholar
• van Agthoven M, Metselaar HJ, Tilanus HW, et al. (2001). A comparison of the costs and effects of liver transplantation for acute and for chronic liver failure. Transpl Int 14:87–94.
   PubMed Web of Science ®Google Scholar
• Vinken M. (2012). Gap junctions and non-neoplastic liver disease. J Hepatol 57:655–62.
   PubMed Web of Science ®Google Scholar
• Vinken M, Henkens T, De Rop E, et al. (2008). Biology and pathobiology of gap junctional channels in hepatocytes. Hepatology 47:1077–88.
   PubMed Web of Science ®Google Scholar
• Yamamoto T, Kojima T, Murata M, et al. (2005). p38 MAP-kinase regulates function of gap and tight junctions during regeneration of rat hepatocytes. J Hepatol 42:707–18.
   PubMed Web of Science ®Google Scholar
• Yamaoka K, Nouchi T, Tazawa J, et al. (1995). Expression of gap junction protein connexin 32 and E-cadherin in human hepatocellular carcinoma. J Hepatol 22:536–9.
   PubMed Web of Science ®Google Scholar
• Zhang Y, He Y, Yu H, et al. (2015). Liquiritigenin protects rats from carbon tetrachloride induced hepatic injury through PGC-1α pathway. Evid Based Complement Alternat Med 2015:Article ID 649568. doi:10.1155/2015/649568.
   Web of Science ®Google Scholar