Hyperoxia accelerates progression of hepatic fibrosis by up-regulation of transforming growth factor-β expression

World Journal of Gastroenterology

Volumn 20, Issue 11, 2014, Pages 3011-3017

  Lee, Sang Hwa ^a   Do, Sung Im ^b   Kim, Hyun Soo ^a  

^a Republic of Korea Air Force   (South Korea)

^b School of Medicine   (South Korea)

Author keywords

Cirrhosis; Hepatic fibrosis; Hyperoxia; Hypoxia; Transforming growth factor

Indexed keywords

BETA ACTIN; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE COURSE; HISTOLOGY; HYPEROXIA; HYPOXIA; LIVER CIRRHOSIS; LIVER FIBROSIS; MALE; NONHUMAN; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION; ANIMAL; ANOXIA; COMPLICATION; LIVER; METABOLISM; RANDOMIZATION; SPRAGUE DAWLEY RAT;

ANIMALS; ANOXIA; DISEASE PROGRESSION; HYPEROXIA; LIVER; LIVER CIRRHOSIS; MALE; RANDOM ALLOCATION; RATS, SPRAGUE-DAWLEY; TRANSFORMING GROWTH FACTOR BETA;

EID: 84896452566     PISSN: 10079327     EISSN: 22192840     Source Type: Journal    
DOI: 10.3748/wjg.v20.i11.3011     Document Type: Article

References (55)

1. Moreira RK. Hepatic stellate cells and liver fibrosis. Arch Pathol Lab Med 2007; 131: 1728-1734 [PMID: 17979495]
2. Guyot C, Lepreux S, Combe C, Doudnikoff E, Bioulac-Sage P, Balabaud C, Desmoulière A. Hepatic fibrosis and cirrhosis: the (myo)fibroblastic cell subpopulations involved. Int J Biochem Cell Biol 2006; 38: 135-151 [PMID: 16257564 DOI: 10.1016/j.biocel.2005.08.021]
3. Bataller R, Brenner DA. Liver fibrosis. J Clin Invest 2005; 115: 209-218 [PMID: 15690074 DOI: 10.1172/JCI200524282]
4. Friedman SL. Liver fibrosis--from bench to bedside. J Hepatol 2003; 38 Suppl 1: S38-S53 [PMID: 12591185]
5. Canbay A, Higuchi H, Bronk SF, Taniai M, Sebo TJ, Gores GJ. Fas enhances fibrogenesis in the bile duct ligated mouse: a link between apoptosis and fibrosis. Gastroenterology 2002; 123: 1323-1330 [PMID: 12360492 DOI: 10.1053/gast.2002.35953]
6. Takehara T, Tatsumi T, Suzuki T, Rucker EB, Hennighausen L, Jinushi M, Miyagi T, Kanazawa Y, Hayashi N. Hepatocyte-specific disruption of Bcl-xL leads to continuous hepatocyte apoptosis and liver fibrotic responses. Gastroenterology 2004; 127: 1189-1197 [PMID: 15480996 DOI: 10.1053/j.gastro.2004.07.019]
7. Sahai A, Malladi P, Melin-Aldana H, Green RM, Whitington PF. Upregulation of osteopontin expression is involved in the development of nonalcoholic steatohepatitis in a dietary murine model. Am J Physiol Gastrointest Liver Physiol 2004; 287: G264-G273 [PMID: 15044174 DOI: 10.1152/ajpgi.00002.2004]
8. Streetz KL, Tacke F, Leifeld L, Wüstefeld T, Graw A, Klein C, Kamino K, Spengler U, Kreipe H, Kubicka S, Müller W, Manns MP, Trautwein C. Interleukin 6/gp130-dependent pathways are protective during chronic liver diseases. Hepatology 2003; 38: 218-229 [PMID: 12830005 DOI: 10.1053/jhep.2003.50268]
9. Bataller R, Schwabe RF, Choi YH, Yang L, Paik YH, Lindquist J, Qian T, Schoonhoven R, Hagedorn CH, Lemasters JJ, Brenner DA. NADPH oxidase signal transduces angiotensin II in hepatic stellate cells and is critical in hepatic fibrosis. J Clin Invest 2003; 112: 1383-1394 [PMID: 14597764 DOI: 10.1172/JCI200318212]
10. Shi Z, Wakil AE, Rockey DC. Strain-specific differences in mouse hepatic wound healing are mediated by divergent T helper cytokine responses. Proc Natl Acad Sci USA 1997; 94: 10663-10668 [PMID: 9380692 DOI: 10.1073/pnas.94.20.10663]
11. Bissell DM, Roulot D, George J. Transforming growth factor beta and the liver. Hepatology 2001; 34: 859-867 [PMID: 11679955 DOI: 10.1053/jhep.2001.28457]
12. Forbes SJ, Parola M. Liver fibrogenic cells. Best Pract Res Clin Gastroenterol 2011; 25: 207-217 [PMID: 21497739 DOI: 10.1016/j.bpg.2011.02.006]
13. Ueberham E, Löw R, Ueberham U, Schönig K, Bujard H, Gebhardt R. Conditional tetracycline-regulated expression of TGF-beta1 in liver of transgenic mice leads to reversible intermediary fibrosis. Hepatology 2003; 37: 1067-1078 [PMID: 12717387 DOI: 10.1053/jhep.2003.50196]
14. George J, Roulot D, Koteliansky VE, Bissell DM. In vivo inhibition of rat stellate cell activation by soluble transforming growth factor beta type II receptor: a potential new therapy for hepatic fibrosis. Proc Natl Acad Sci USA 1999; 96: 12719-12724 [PMID: 10535989 DOI: 10.1073/pnas.96.22.12719]
15. George J, Wang SS, Sevcsik AM, Sanicola M, Cate RL, Koteliansky VE, Bissell DM. Transforming growth factor-beta initiates wound repair in rat liver through induction of the EIIIA-fibronectin splice isoform. Am J Pathol 2000; 156: 115-124 [PMID: 10623659 DOI: 10.1016/S0002-9440(10)64711-6]
16. Schnur J, Oláh J, Szepesi A, Nagy P, Thorgeirsson SS. Thioacetamide-induced hepatic fibrosis in transforming growth factor beta-1 transgenic mice. Eur J Gastroenterol Hepatol 2004; 16: 127-133 [PMID: 15075984 DOI: 10.1097/00042737-200402000-00002]
17. Shek FW, Benyon RC. How can transforming growth factor beta be targeted usefully to combat liver fibrosis? Eur J Gastroenterol Hepatol 2004; 16: 123-126 [PMID: 15075983 DOI: 10.1097/00042737-200402000-00001]
18. Higgins DF, Kimura K, Iwano M, Haase VH. Hypoxia-inducible factor signaling in the development of tissue fibrosis. Cell Cycle 2008; 7: 1128-1132 [PMID: 18418042 DOI: 10.4161/cc.7.9.5804]
19. Kietzmann T, Dimova EY, Flügel D, Scharf JG. Oxygen: modulator of physiological and pathophysiological processes in the liver. Z Gastroenterol 2006; 44: 67-76 [PMID: 16397842 DOI: 10.1055/s-2005-858987]
20. Ben-Yosef Y, Lahat N, Shapiro S, Bitterman H, Miller A. Regulation of endothelial matrix metalloproteinase-2 by hypoxia/reoxygenation. Circ Res 2002; 90: 784-791 [PMID: 11964371 DOI: 10.1161/01.RES.0000015588.70132.DC]
21. Chen PS, Zhai WR, Zhou XM, Zhang JS, Zhang YE, Ling YQ, Gu YH. Effects of hypoxia, hyperoxia on the regulation of expression and activity of matrix metalloproteinase-2 in hepatic stellate cells. World J Gastroenterol 2001; 7: 647-651 [PMID: 11819847]
22. Copple BL, Bai S, Burgoon LD, Moon JO. Hypoxia-inducible factor-1α regulates the expression of genes in hypoxic hepatic stellate cells important for collagen deposition and angiogenesis. Liver Int 2011; 31: 230-244 [PMID: 20880076 DOI: 10.1111/j.1478-3231.2010.02347.x]
23. Pugh CW, Ratcliffe PJ. Regulation of angiogenesis by hypoxia: role of the HIF system. Nat Med 2003; 9: 677-684 [PMID: 12778166 DOI: 10.1038/nm0603-677]
24. Shi YF, Fong CC, Zhang Q, Cheung PY, Tzang CH, Wu RS, Yang M. Hypoxia induces the activation of human hepatic stellate cells LX-2 through TGF-beta signaling pathway. FEBS Lett 2007; 581: 203-210 [PMID: 17187782 DOI: 10.1016/j.febslet.2006.12.010]
25. Troeger JS, Schwabe RF. Hypoxia and hypoxia-inducible factor 1α: potential links between angiogenesis and fibrogenesis in hepatic stellate cells. Liver Int 2011; 31: 143-145 [PMID: 21176093 DOI: 10.1111/j.1478-3231.2010.02426.x]
26. Gill AL, Bell CN. Hyperbaric oxygen: its uses, mechanisms of action and outcomes. QJM 2004; 97: 385-395 [PMID: 15208426 DOI: 10.1093/qjmed/hch074]
27. Eppihimer MJ, Granger DN. Ischemia/reperfusion-induced leukocyte-endothelial interactions in postcapillary venules. Shock 1997; 8: 16-25 [PMID: 9249908 DOI: 10.1097/00024382-199707000-00004]
28. Parks DA, Bulkley GB, Granger DN. Role of oxygen-derived free radicals in digestive tract diseases. Surgery 1983; 94: 415-422 [PMID: 6351311]
29. Britton RS, Bacon BR. Role of free radicals in liver diseases and hepatic fibrosis. Hepatogastroenterology 1994; 41: 343-348 [PMID: 7959569]
30. Farrell GC, Teoh NC, McCuskey RS. Hepatic microcirculation in fatty liver disease. Anat Rec (Hoboken) 2008; 291: 684-692 [PMID: 18484615 DOI: 10.1002/ar.20715]
31. Estrada KD, Chesler NC. Collagen-related gene and protein expression changes in the lung in response to chronic hypoxia. Biomech Model Mechanobiol 2009; 8: 263-272 [PMID: 18642127 DOI: 10.1007/s10237-008-0133-2]
32. Lin YM, Huang SK, Wang HF, Chen LM, Tsai FJ, Hsu HH, Kuo CH, Wang PS, Huang CY, Lee SD. Short-term versus long-term intermittent hypobaric hypoxia on cardiac fibrosis and Fas death receptor dependent apoptotic pathway in rat hearts. Chin J Physiol 2008; 51: 308-316 [PMID: 19175187]
33. Park YN, Kim H, Chon CY, Park JB, Sohn JH, Yang SH, Yu E, Lee MS, Jang JJ, Chang HK, Jeong JJ, Kang DY, Kim YI, Park C. Histological grading and staging of chronic hepatitis: Standardized guideline proposed by the Korean Study Group for Pathology of Digestive Diseases. Korean J Pathol 1999; 33: 337-346
34. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T) Method. Methods 2001; 25: 402-408 [PMID: 11846609 DOI: 10.1006/meth.2001.1262]
35. Ankoma-Sey V, Wang Y, Dai Z. Hypoxic stimulation of vascular endothelial growth factor expression in activated rat hepatic stellate cells. Hepatology 2000; 31: 141-148 [PMID: 10613739 DOI: 10.1002/hep.510310122]
36. Novo E, Cannito S, Zamara E, Valfrè di Bonzo L, Caligiuri A, Cravanzola C, Compagnone A, Colombatto S, Marra F, Pinzani M, Parola M. Proangiogenic cytokines as hypoxia-dependent factors stimulating migration of human hepatic stellate cells. Am J Pathol 2007; 170: 1942-1953 [PMID: 17525262 DOI: 10.2353/ajpath.2007.060887]
37. Taura K, De Minicis S, Seki E, Hatano E, Iwaisako K, Osterreicher CH, Kodama Y, Miura K, Ikai I, Uemoto S, Brenner DA. Hepatic stellate cells secrete angiopoietin 1 that induces angiogenesis in liver fibrosis. Gastroenterology 2008; 135: 1729-1738 [PMID: 18823985 DOI: 10.1053/j.gastro.2008.07.065]
38. Hernández-Guerra M, de Ganzo ZA, González-Méndez Y, Salido E, Abreu P, Moreno M, Felipe V, Abrante B, Quintero E. Chronic intermittent hypoxia aggravates intrahepatic endothelial dysfunction in cirrhotic rats. Hepatology 2013; 57: 1564-1574 [PMID: 23174804 DOI: 10.1002/hep.26152]
39. Bitterman H. Oxygen: an anti-inflammatory drug. Isr Med Assoc J 2007; 9: 874-876 [PMID: 18210929]
40. Bitterman H, Bitterman N, Melamed Y, Cohen L. Effects of hyperbaric oxygen in circulatory shock induced by splanchnic artery occlusion and reperfusion in rats. Can J Physiol Pharmacol 1989; 67: 1033-1037 [PMID: 2598128 DOI: 10.1139/y89-163]
41. Stogner SW, Payne DK. Oxygen toxicity. Ann Pharmacother 1992; 26: 1554-1562 [PMID: 1336412]
42. Gille JJ, van Berkel CG, Joenje H. Mutagenicity of metabolic oxygen radicals in mammalian cell cultures. Carcinogenesis 1994; 15: 2695-2699 [PMID: 8001223 DOI: 10.1093/carcin/15.12.2695]
43. Freeman BA, Crapo JD. Hyperoxia increases oxygen radical production in rat lungs and lung mitochondria. J Biol Chem 1981; 256: 10986-10992 [PMID: 7287745]
44. D'Angio CT, Finkelstein JN. Oxygen regulation of gene expression: a study in opposites. Mol Genet Metab 2000; 71: 371-380 [PMID: 11001829 DOI: 10.1006/mgme.2000.3074]
45. Weiss SJ. Tissue destruction by neutrophils. N Engl J Med 1989; 320: 365-376 [PMID: 2536474]
46. Bissell DM. Chronic liver injury, TGF-beta, and cancer. Exp Mol Med 2001; 33: 179-190 [PMID: 11795478 DOI: 10.1038/emm.2001.31]
47. Casini A, Ceni E, Salzano R, Biondi P, Parola M, Galli A, Foschi M, Caligiuri A, Pinzani M, Surrenti C. Neutrophil-derived superoxide anion induces lipid peroxidation and stimulates collagen synthesis in human hepatic stellate cells: role of nitric oxide. Hepatology 1997; 25: 361-367 [PMID: 9021948 DOI: 10.1053/jhep.1997.v25.pm0009021948]
48. Bhandari S, Agarwal MP, Dwivedi S, Banerjee BD. Monitoring oxidative stress across worsening Child Pugh class of cirrhosis. Indian J Med Sci 2008; 62: 444-451 [PMID: 19265234 DOI: 10.4103/0019-5359.48456]
49. Lecart C, Cayabyab R, Buckley S, Morrison J, Kwong KY, Warburton D, Ramanathan R, Jones CA, Minoo P. Bioactive transforming growth factor-beta in the lungs of extremely low birthweight neonates predicts the need for home oxygen supplementation. Biol Neonate 2000; 77: 217-223 [PMID: 10828572 DOI: 10.1159/000014219]
50. Alejandre-Alcázar MA, Kwapiszewska G, Reiss I, Amarie OV, Marsh LM, Sevilla-Pérez J, Wygrecka M, Eul B, Köbrich S, Hesse M, Schermuly RT, Seeger W, Eickelberg O, Morty RE. Hyperoxia modulates TGF-beta/BMP signaling in a mouse model of bronchopulmonary dysplasia. Am J Physiol Lung Cell Mol Physiol 2007; 292: L537-L549 [PMID: 17071723 DOI: 10.1152/ajplung.00050.2006]
51. Suzuki A, Kusakai G, Shimojo Y, Chen J, Ogura T, Kobayashi M, Esumi H. Involvement of transforming growth factor-beta 1 signaling in hypoxia-induced tolerance to glucose starvation. J Biol Chem 2005; 280: 31557-31563 [PMID: 16014625 DOI: 10.1074/jbc.M503714200]
52. Jeong WI, Do SH, Yun HS, Song BJ, Kim SJ, Kwak WJ, Yoo SE, Park HY, Jeong KS. Hypoxia potentiates transforming growth factor-beta expression of hepatocyte during the cirrhotic condition in rat liver. Liver Int 2004; 24: 658-668 [PMID: 15566519 DOI: 10.1111/j.1478-3231.2004.0961.x]
53. Falanga V, Qian SW, Danielpour D, Katz MH, Roberts AB, Sporn MB. Hypoxia upregulates the synthesis of TGF-beta 1 by human dermal fibroblasts. J Invest Dermatol 1991; 97: 634-637 [PMID: 1940433 DOI: 10.1111/1523-1747.ep12483126]
54. Papakonstantinou E, Roth M, Tamm M, Eickelberg O, Perruchoud AP, Karakiulakis G. Hypoxia differentially enhances the effects of transforming growth factor-beta isoforms on the synthesis and secretion of glycosaminoglycans by human lung fibroblasts. J Pharmacol Exp Ther 2002; 301: 830-837 [PMID: 12023510 DOI: 10.1124/jpet.301.3.830]
55. Chen CP, Yang YC, Su TH, Chen CY, Aplin JD. Hypoxia and transforming growth factor-beta 1 act independently to increase extracellular matrix production by placental fibroblasts. J Clin Endocrinol Metab 2005; 90: 1083-1090 [PMID: 15522940 DOI: 10.1210/jc.2004-0803]