NADPH oxidase 4 modulates hepatic responses to lipopolysaccharide mediated by Toll-like receptor-4

Scientific Reports

Volumn 7, Issue 1, 2017, Pages

  Singh, Anand ^a   Koduru, Bhargav ^a   Carlisle, Cameron ^a   Akhter, Hasina ^b   Liu, Rui Ming ^b   Schroder, Katrin ^c   Brandes, Ralf P ^c   Ojcius, David M ^a,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF ALABAMA SCHOOL OF MEDICINE   (United States)

^c GOETHE UNIVERSITY   (Germany)

^d UNIVERSITY OF THE PACIFIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LIPOPOLYSACCHARIDE; NOX4 PROTEIN, MOUSE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; TLR4 PROTEIN, HUMAN; TOLL LIKE RECEPTOR 4;

ANIMAL; C57BL MOUSE; DRUG EFFECT; GENETICS; HUMAN; LIVER; LIVER CELL; LIVER CELL CARCINOMA; LIVER TUMOR; METABOLISM; MOUSE; PHYSIOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ANIMALS; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; HEPATOCYTES; HUMANS; LIPOPOLYSACCHARIDES; LIVER; LIVER NEOPLASMS; MICE; MICE, INBRED C57BL; NADPH OXIDASE 4; NADPH OXIDASES; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 4;

EID: 85032566127     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-017-14574-8     Document Type: Article

References (46)

1. El-Serag, H. B. Hepatocellular carcinoma. N. Engl. J. Med. 365, 1118-1127 (2011).
2. Grivennikov, S. I., Greten, F. R. & Karin, M. Immunity, inflammation, and cancer. Cell 140, 883-899 (2010).
3. Nolan, J. P. & Leibowitz, A. I. Endotoxins in liver disease. Gastroenterology 75, 765-766 (1978).
4. Yu, L.-X. et al. Endotoxin accumulation prevents carcinogen-induced apoptosis and promotes liver tumorigenesis in rodents. Hepatol. Baltim. Md 52, 1322-1333 (2010).
5. Cirera, I. et al. Bacterial translocation of enteric organisms in patients with cirrhosis. J. Hepatol. 34, 32-37 (2001).
6. Almeida, J., Galhenage, S., Yu, J., Kurtovic, J. & Riordan, S. M. Gut flora and bacterial translocation in chronic liver disease. World J. Gastroenterol. 12, 1493-1502 (2006).
7. Seki, E. et al. CCR1 and CCR5 promote hepatic fibrosis in mice. J. Clin. Invest. 119, 1858-1870 (2009).
8. Wiest, R. & Garcia-Tsao, G. Bacterial translocation (BT) in cirrhosis. Hepatol. Baltim. Md 41, 422-433 (2005).
9. Aderem, A. & Ulevitch, R. J. Toll-like receptors in the induction of the innate immune response. Nature 406, 782-787 (2000).
10. Akira, S., Takeda, K. & Kaisho, T. Toll-like receptors: critical proteins linking innate and acquired immunity. Nat. Immunol. 2, 675-680 (2001).
11. Liu, S. et al. Role of toll-like receptors in changes in gene expression and NF-kappa B activation in mouse hepatocytes stimulated with lipopolysaccharide. Infect. Immun. 70, 3433-3442 (2002).
12. Su, G. L. et al. Kupffer cell activation by lipopolysaccharide in rats: role for lipopolysaccharide binding protein and toll-like receptor 4. Hepatol. Baltim. Md 31, 932-936 (2000).
13. Dapito, D. H. et al. Promotion of hepatocellular carcinoma by the intestinal microbiota and TLR4. Cancer Cell 21, 504-516 (2012).
14. Zhang, H.-L. et al. Profound impact of gut homeostasis on chemically-induced pro-tumorigenic inflammation and hepatocarcinogenesis in rats. J. Hepatol. 57, 803-812 (2012).
15. Kawahara, T. et al. Helicobacter pylori lipopolysaccharide activates Rac1 and transcription of NADPH oxidase Nox1 and its organizer NOXO1 in guinea pig gastric mucosal cells. Am. J. Physiol. Cell Physiol. 288, C450-457 (2005).
16. Maitra, U., Singh, N., Gan, L., Ringwood, L. & Li, L. IRAK-1 contributes to lipopolysaccharide-induced reactive oxygen species generation in macrophages by inducing NOX-1 transcription and Rac1 activation and suppressing the expression of antioxidative enzymes. J. Biol. Chem. 284, 35403-35411 (2009).
17. Kim, J.-S. et al. Glycogen synthase kinase 3beta and beta-catenin pathway is involved in toll-like receptor 4-mediated NADPH oxidase 1 expression in macrophages. FEBS J. 277, 2830-2837 (2010).
18. Park, H. S. et al. Cutting edge: direct interaction of TLR4 with NAD(P)H oxidase 4 isozyme is essential for lipopolysaccharide-induced production of reactive oxygen species and activation of NF-kappa B. J. Immunol. Baltim. Md 1950 173, 3589-3593 (2004).
19. Chiang, E. et al. Cutting edge: apoptosis-regulating signal kinase 1 is required for reactive oxygen species-mediated activation of IFN regulatory factor 3 by lipopolysaccharide. J. Immunol. Baltim. Md 1950 176, 5720-5724 (2006).
20. Park, H. S., Chun, J. N., Jung, H. Y., Choi, C. & Bae, Y. S. Role of NADPH oxidase 4 in lipopolysaccharide-induced proinflammatory responses by human aortic endothelial cells. Cardiovasc. Res. 72, 447-455 (2006).
21. Lee, I.-T., Shih, R.-H., Lin, C.-C., Chen, J.-T. & Yang, C.-M. Role of TLR4/NADPH oxidase/ROS-activated p38 MAPK in VCAM-1 expression induced by lipopolysaccharide in human renal mesangial cells. Cell Commun. Signal. CCS 10, 33 (2012).
22. Lambeth, J. D. NOX enzymes and the biology of reactive oxygen. Nat. Rev. Immunol. 4, 181-189 (2004).
23. Choi, J., Corder, N. L. B., Koduru, B. & Wang, Y. Oxidative stress and hepatic Nox proteins in chronic hepatitis C and hepatocellular carcinoma. Free Radic. Biol. Med. 72, 267-284 (2014).
24. Paik, Y.-H. et al. The nicotinamide adenine dinucleotide phosphate oxidase (NOX) homologues NOX1 and NOX2/gp91(phox) mediate hepatic fibrosis in mice. Hepatol. Baltim. Md 53, 1730-1741 (2011).
25. Jiang, J. X. et al. Liver fibrosis and hepatocyte apoptosis are attenuated by GKT137831, a novel NOX4/NOX1 inhibitor in vivo. Free Radic. Biol. Med. 53, 289-296 (2012).
26. Bataller, R. et al. NADPH oxidase signal transduces angiotensin II in hepatic stellate cells and is critical in hepatic fibrosis. J. Clin. Invest. 112, 1383-1394 (2003).
27. Schröder, K. et al. Nox4 is a protective reactive oxygen species generating vascular NADPH oxidase. Circ. Res. 110, 1217-1225 (2012).
28. Li, W.-C., Ralphs, K. L. & Tosh, D. Isolation and culture of adult mouse hepatocytes. Methods Mol. Biol. Clifton NJ 633, 185-196 (2010).
29. Shen, L., Hillebrand, A., Wang, D. Q.-H. & Liu, M. Isolation and primary culture of rat hepatic cells. J. Vis. Exp. JoVE (2012). https://doi.org/10.3791/3917
30. Kumar, B., Koul, S., Khandrika, L., Meacham, R. B. & Koul, H. K. Oxidative stress is inherent in prostate cancer cells and is required for aggressive phenotype. Cancer Res. 68, 1777-1785 (2008).
31. de Mochel, N. S. R. et al. Hepatocyte NAD(P)H oxidases as an endogenous source of reactive oxygen species during hepatitis C virus infection. Hepatol. Baltim. Md 52, 47-59 (2010).
32. Choi, J. et al. Reactive oxygen species suppress hepatitis C virus RNA replication in human hepatoma cells. Hepatol. Baltim. Md 39, 81-89 (2004).
33. Khan, S. A. et al. NADPH oxidase 2 mediates intermittent hypoxia-induced mitochondrial complex I inhibition: relevance to blood pressure changes in rats. Antioxid. Redox Signal. 14, 533-542 (2011).
34. Cassé, C., Giannoni, F., Nguyen, V. T., Dubois, M. F. & Bensaude, O. The transcriptional inhibitors, actinomycin D and alphaamanitin, activate the HIV-1 promoter and favor phosphorylation of the RNA polymerase II C-terminal domain. J. Biol. Chem. 274, 16097-16106 (1999).
35. Wang, L., Zhu, R., Huang, Z., Li, H. & Zhu, H. Lipopolysaccharide-induced toll-like receptor 4 signaling in cancer cells promotes cell survival and proliferation in hepatocellular carcinoma. Dig. Dis. Sci. 58, 2223-2236 (2013).
36. Jing, Y.-Y. et al. Toll-like receptor 4 signaling promotes epithelial-mesenchymal transition in human hepatocellular carcinoma induced by lipopolysaccharide. BMC Med. 10, 98 (2012).
37. Patel, D. N. et al. TLR4-NOX4-AP-1 signaling mediates lipopolysaccharide-induced CXCR6 expression in human aortic smooth muscle cells. Biochem. Biophys. Res. Commun. 347, 1113-1120 (2006).
38. Forner, A., Llovet, J. M. & Bruix, J. Hepatocellular carcinoma. Lancet Lond. Engl. 379, 1245-1255 (2012).
39. Mencin, A., Kluwe, J. & Schwabe, R. F. Toll-like receptors as targets in chronic liver diseases. Gut 58, 704-720 (2009).
40. Schwabe, R. F., Seki, E. & Brenner, D. A. Toll-like receptor signaling in the liver. Gastroenterology 130, 1886-1900 (2006).
41. Seki, E. et al. TLR4 enhances TGF-beta signaling and hepatic fibrosis. Nat. Med. 13, 1324-1332 (2007).
42. Kagan, J. C. et al. TRAM couples endocytosis of Toll-like receptor 4 to the induction of interferon-beta. Nat. Immunol. 9, 361-368 (2008).
43. Haybaeck, J. et al. A lymphotoxin-driven pathway to hepatocellular carcinoma. Cancer Cell 16, 295-308 (2009).
44. Tai, D. I. et al. Constitutive activation of nuclear factor kappaB in hepatocellular carcinoma. Cancer 89, 2274-2281 (2000).
45. Balmanno, K. & Cook, S. J. Tumour cell survival signalling by the ERK1/2 pathway. Cell Death Differ. 16, 368-377 (2009).
46. Gailhouste, L. et al. RNAi-mediated MEK1 knock-down prevents ERK1/2 activation and abolishes human hepatocarcinoma growth in vitro and in vivo. Int. J. Cancer 126, 1367-1377 (2010).