Erratum: Inhibiting heme oxygenase-1 attenuates rat liver fibrosis by removing iron accumulation (World Journal of Gastroenterology (2013) 19 (2921-2934) DOI: 10.3748/wjg.v19.i19.2921);Inhibiting heme oxygenase-1 attenuates rat liver fibrosis by removing iron accumulation

World Journal of Gastroenterology

Volumn 19, Issue 19, 2013, Pages 2921-2934

  Wang, Qiu Ming ^a   Du, Jian Ling ^a   Duan, Zhi Jun ^a   Guo, Shi Bin ^a   Sun, Xiao Yu ^a   Liu, Zhen ^a  

^a DALIAN MEDICAL UNIVERSITY   (China)

Author keywords

Bile duct ligation; Carboxyhemoglobin; Heme oxygenase 1; Hepcidin; Iron accumulation; Oxidative stress; Portal vein pressure

Indexed keywords

ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; CARBOXYHEMOGLOBIN; DEFEROXAMINE; GELATINASE A; GENTAMICIN; HEME OXYGENASE 1; HEPCIDIN; IRON; MALONALDEHYDE; MESSENGER RNA; PROTOPORPHYRIN COBALT; PROTOPORPHYRIN ZINC; SUPEROXIDE DISMUTASE; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TRANSCRIPTION FACTOR NRF2; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD SAMPLING; CONTROLLED STUDY; ENZYME INHIBITION; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; LIVER FIBROSIS; LIVER HISTOLOGY; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PORTAL VEIN BLOOD PRESSURE; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; WESTERN BLOTTING;

EID: 84878071811     PISSN: 10079327     EISSN: 22192840     Source Type: Journal    
DOI: 10.3748/wjg.v28.i35.5237     Document Type: Erratum

References (67)

1. Shaw GC, Cope JJ, Li L, Corson K, Hersey C, Ackermann GE, Gwynn B, Lambert AJ, Wingert RA, Traver D, Trede NS, Barut BA, Zhou Y, Minet E, Donovan A, Brownlie A, Balzan R, Weiss MJ, Peters LL, Kaplan J, Zon LI, Paw BH. Mitoferrin is essential for erythroid iron assimilation. Nature 2006; 440: 96-100 [PMID: 16511496 DOI: 10.1038/nature04512]
2. Brown KE, Dennery PA, Ridnour LA, Fimmel CJ, Kladney RD, Brunt EM, Spitz DR. Effect of iron overload and dietary fat on indices of oxidative stress and hepatic fibrogenesis in rats. Liver Int 2003; 23: 232-242 [PMID: 12895262]
3. Kayali Z, Ranguelov R, Mitros F, Shufelt C, Elmi F, Rayhill SC, Schmidt WN, Brown KE. Hemosiderosis is associated with accelerated decompensation and decreased survival in patients with cirrhosis. Liver Int 2005; 25: 41-48 [PMID: 15698397 DOI: 10.1111/j.1478-3231.2005.01022.x]
4. Horowitz JM, Nikolaidis P, Chen ZM, Siegelman E, Garg A, Feng C, Miller FH. Iron deposition surrounding the hepatic veins of cirrhotic patients on MRI. J Magn Reson Imaging 2011; 33: 598-602 [PMID: 21563243 DOI: 10.1002/jmri.22503]
5. Parkes JG, Templeton DM. Modulation of stellate cell proliferation and gene expression by rat hepatocytes: effect of toxic iron overload. Toxicol Lett 2003; 144: 225-233 [PMID: 12927366]
6. Arezzini B, Lunghi B, Lungarella G, Gardi C. Iron overload enhances the development of experimental liver cirrhosis in mice. Int J Biochem Cell Biol 2003; 35: 486-495 [PMID: 12565710]
7. Niederau C, Fischer R, Sonnenberg A, Stremmel W, Trampisch HJ, Strohmeyer G. Survival and causes of death in cirrhotic and in noncirrhotic patients with primary hemochromatosis. N Engl J Med 1985; 313: 1256-1262 [PMID: 4058506 DOI: 10.1056/NEJM198511143132004]
8. Deugnier Y, Turlin B, Ropert M, Cappellini MD, Porter JB, Giannone V, Zhang Y, Griffel L, Brissot P. Improvement in liver pathology of patients with β-thalassemia treated with deferasirox for at least 3 years. Gastroenterology 2011; 141: 1202-1211 [PMID: 21741344 DOI: 10.1053/j.gastro.2011.06.065]
9. Hendrickson JE, Hillyer CD. Noninfectious serious hazards of transfusion. Anesth Analg 2009; 108: 759-769 [PMID: 19224780 DOI: 10.1213/ane.0b013e3181930a6e]
10. Maines MD, Trakshel GM, Kutty RK. Characterization of two constitutive forms of rat liver microsomal heme oxygenase. Only one molecular species of the enzyme is inducible. J Biol Chem 1986; 261: 411-419 [PMID: 3079757]
11. Maines MD. Heme oxygenase: function, multiplicity, regulatory mechanisms, and clinical applications. FASEB J 1988; 2: 2557-2568 [PMID: 3290025]
12. Yang H, Zhao LF, Zhao ZF, Wang Y, Zhao JJ, Zhang L. Heme oxygenase-1 prevents liver fibrosis in rats by regulating the expression of PPARγ and NF-κB. World J Gastroenterol 2012; 18: 1680-1688 [PMID: 22529699 DOI: 10.3748/wjg. v18.i14.1680]
13. Malaguarnera L, Madeddu R, Palio E, Arena N, Malaguarnera M. Heme oxygenase-1 levels and oxidative stress-related parameters in non-alcoholic fatty liver disease patients. J Hepatol 2005; 42: 585-591 [PMID: 15763346 DOI: 10.1016/ j.jhep.2004.11.040]
14. Wen T, Guan L, Zhang YL, Zhao JY. Dynamic changes of heme oxygenase-1 and carbon monoxide production in acute liver injury induced by carbon tetrachloride in rats. Toxicology 2006; 228: 51-57 [PMID: 16978757 DOI: 10.1016/ j.tox.2006.08.014]
15. Zeng Z, Huang HF, Chen MQ, Song F, Zhang YJ. Heme oxygenase-1 protects donor livers from ischemia/reperfusion injury: the role of Kupffer cells. World J Gastroenterol 2010; 16: 1285-1292 [PMID: 20222175]
16. Geuken E, Buis CI, Visser DS, Blokzijl H, Moshage H, Nemes B, Leuvenink HG, de Jong KP, Peeters PM, Slooff MJ, Porte RJ. Expression of heme oxygenase-1 in human livers before transplantation correlates with graft injury and function after transplantation. Am J Transplant 2005; 5: 1875-1885 [PMID: 15996234 DOI: 10.1111/j.1600-6143.2005.00960.x]
17. Guo SB, Duan ZJ, Li Q, Sun XY. Effect of heme oxygenase-1 on renal function in rats with liver cirrhosis. World J Gastroenterol 2011; 17: 322-328 [PMID: 21253390 DOI: 10.3748/wjg. v17.i3.322]
18. Guo SB, Duan ZJ, Li Q, Sun XY. Effects of heme oxygenase-1 on pulmonary function and structure in rats with liver cirrhosis. Chin Med J (Engl) 2011; 124: 918-922 [PMID: 21518603]
19. Froh M, Conzelmann L, Walbrun P, Netter S, Wiest R, Wheeler MD, Lehnert M, Uesugi T, Scholmerich J, Thurman RG. Heme oxygenase-1 overexpression increases liver injury after bile duct ligation in rats. World J Gastroenterol 2007; 13: 3478-3486 [PMID: 17659695]
20. Khan ZA, Barbin YP, Cukiernik M, Adams PC, Chakrabarti S. Heme-oxygenase-mediated iron accumulation in the liver. Can J Physiol Pharmacol 2004; 82: 448-456 [PMID: 15389291 DOI: 10.1139/y04-052]
21. Fallon MB, Abrams GA, McGrath JW, Hou Z, Luo B. Common bile duct ligation in the rat: a model of intrapulmonary vasodilatation and hepatopulmonary syndrome. Am J Physiol 1997; 272: G779-G784 [PMID: 9142908]
22. Luo B, Abrams GA, Fallon MB. Endothelin-1 in the rat bile duct ligation model of hepatopulmonary syndrome: correlation with pulmonary dysfunction. J Hepatol 1998; 29: 571-578 [PMID: 9824266]
23. Amersi F, Buelow R, Kato H, Ke B, Coito AJ, Shen XD, Zhao D, Zaky J, Melinek J, Lassman CR, Kolls JK, Alam J, Ritter T, Volk HD, Farmer DG, Ghobrial RM, Busuttil RW, Kupiec-Weglinski JW. Upregulation of heme oxygenase-1 protects genetically fat Zucker rat livers from ischemia/reperfusion injury. J Clin Invest 1999; 104: 1631-1639 [PMID: 10587527 DOI: 10.1172/JCI7903]
24. Feron VJ, Kittel B, Kuper CF, Ernst H, Rittinghausen S, Muhle H, Koch W, Gamer A, Mallett AK, Hoffmann HD. Chronic pulmonary effects of respirable methylene diphenyl diisocyanate (MDI) aerosol in rats: combination of findings from two bioassays. Arch Toxicol 2001; 75: 159-175 [PMID: 11409538]
25. BUNTING H. The histochemical detection of iron in tissues. Stain Technol 1949; 24: 109-115 [PMID: 18116085]
26. Remmele W, Stegner HE. [Recommendation for uniform definition of an immunoreactive score (IRS) for immunohistochemical estrogen receptor detection (ER-ICA) in breast cancer tissue]. Pathologe 1987; 8: 138-140 [PMID: 3303008]
27. Brown KE, Poulos JE, Li L, Soweid AM, Ramm GA, O'Neill R, Britton RS, Bacon BR. Effect of vitamin E supplementation on hepatic fibrogenesis in chronic dietary iron overload. Am J Physiol 1997; 272: G116-G123 [PMID: 9038884]
28. Koliaraki V, Marinou M, Vassilakopoulos TP, Vavourakis E, Tsochatzis E, Pangalis GA, Papatheodoridis G, Stamoulakatou A, Swinkels DW, Papanikolaou G, Mamalaki A. A novel immunological assay for hepcidin quantification in human serum. PLoS One 2009; 4: e4581 [PMID: 19238200 DOI: 10.1371/journal.pone.0004581]
29. Kakinuma S, Tanaka Y, Chinzei R, Watanabe M, Shimizu-Saito K, Hara Y, Teramoto K, Arii S, Sato C, Takase K, Yasumizu T, Teraoka H. Human umbilical cord blood as a source of transplantable hepatic progenitor cells. Stem Cells 2003; 21: 217-227 [PMID: 12634418 DOI: 10.1634/stemcells.21-2-217]
30. Lamireau T, Desmoulière A, Bioulac-Sage P, Rosenbaum J. [Mechanisms of hepatic fibrogenesis]. Arch Pediatr 2002; 9: 392-405 [PMID: 11998427]
31. Olynyk JK, St Pierre TG, Britton RS, Brunt EM, Bacon BR. Duration of hepatic iron exposure increases the risk of significant fibrosis in hereditary hemochromatosis: a new role for magnetic resonance imaging. Am J Gastroenterol 2005; 100: 837-841 [PMID: 15784029 DOI: 10.1111/ j.1572-0241.2005.41287.x]
32. Bessa SS, Mohamed Ali EM, Abd El-Wahab Ael S, Nor El-Din SA. Heme oxygenase-1 mRNA expression in egyptian patients with chronic liver disease. Hepat Mon 2012; 12: 278-285 [PMID: 22690236 DOI: 10.5812/hepatmon.846]
33. Barikbin R, Neureiter D, Wirth J, Erhardt A, Schwinge D, Kluwe J, Schramm C, Tiegs G, Sass G. Induction of heme oxygenase 1. prevents progression of liver fibrosis in Mdr2 knockout mice. Hepatology 2012; 55: 553-562 [PMID: 21953613 DOI: 10.1002/hep.24711]
34. Wang RQ, Nan YM, Wu WJ, Kong LB, Han F, Zhao SX, Kong L, Yu J. Induction of heme oxygenase-1 protects against nutritional fibrosing steatohepatitis in mice. Lipids Health Dis 2011; 10: 31 [PMID: 21314960 DOI: 10.1186/1476-511X-10-31]
35. Suttner DM, Dennery PA. Reversal of HO-1 related cytoprotection with increased expression is due to reactive iron. FASEB J 1999; 13: 1800-1809 [PMID: 10506583]
36. Wang F, Duan ZJ, Sun YJ. Influence of heme oxygenase-1 expression on immune liver fibrosis induced by cobalt protoporphyrin in rats. World J Gastroenterol 2009; 15: 3009-3014 [PMID: 19554654]
37. Giles TD, Sander GE, Nossaman BD, Kadowitz PJ. Impaired vasodilation in the pathogenesis of hypertension: focus on nitric oxide, endothelial-derived hyperpolarizing factors, and prostaglandins. J Clin Hypertens (Greenwich) 2012; 14: 198-205 [PMID: 22458740 DOI: 10.1111/j.1751-7176.2012.00606.x]
38. Van Landeghem L, Laleman W, Vander Elst I, Zeegers M, van Pelt J, Cassiman D, Nevens F. Carbon monoxide produced by intrasinusoidally located haem-oxygenase-1 regulates the vascular tone in cirrhotic rat liver. Liver Int 2009; 29: 650-660 [PMID: 18795901 DOI: 10.1111/j.1478-3231.2008.01857.x]
39. Tarquini R, Masini E, La Villa G, Barletta G, Novelli M, Mastroianni R, Romanelli RG, Vizzutti F, Santosuosso U, Laffi G. Increased plasma carbon monoxide in patients with viral cirrhosis and hyperdynamic circulation. Am J Gastroenterol 2009; 104: 891-897 [PMID: 19277027 DOI: 10.1038/ajg.2009.2]
40. Kartikasari AE, Wagener FA, Yachie A, Wiegerinck ET, Kemna EH, Swinkels DW. Hepcidin suppression and defective iron recycling account for dysregulation of iron homeostasis in heme oxygenase-1 deficiency. J Cell Mol Med 2009; 13: 3091-3102 [PMID: 18774956 DOI: 10.1111/ j.1582-4934.2008.00494.x]
41. Ren H, Leib SL, Ferriero DM, Täuber MG, Christen S. Induction of haem oxygenase-1 causes cortical non-haem iron increase in experimental pneumococcal meningitis: evidence that concomitant ferritin up-regulation prevents ironinduced oxidative damage. J Neurochem 2007; 100: 532-544 [PMID: 17116231 DOI: 10.1111/j.1471-4159.2006.04230.x]
42. Costa-Matos L, Batista P, Monteiro N, Simões M, Egas C, Pereira J, Pinho H, Santos N, Ribeiro J, Cipriano MA, Henriques P, Girão F, Rodrigues A, Carvalho A. Liver hepcidin mRNA expression is inappropriately low in alcoholic patients compared with healthy controls. Eur J Gastroenterol Hepatol 2012; 24: 1158-1165 [PMID: 22732356 DOI: 10.1097/ MEG.0b013e328355cfd0]
43. Nicolas G, Bennoun M, Devaux I, Beaumont C, Grandchamp B, Kahn A, Vaulont S. Lack of hepcidin gene expression and severe tissue iron overload in upstream stimulatory factor 2 (USF2) knockout mice. Proc Natl Acad Sci USA 2001; 98: 8780-8785 [PMID: 11447267 DOI: 10.1073/pnas.151179498]
44. Jaroszewicz J, Rogalska M, Flisiak R. Serum prohepcidin reflects the degree of liver function impairment in liver cir-rhosis. Biomarkers 2008; 13: 478-485 [PMID: 18979640]
45. Huang YH, Chuang JH, Yang YL, Huang CC, Wu CL, Chen CL. Cholestasis downregulate hepcidin expression through inhibiting IL-6-induced phosphorylation of signal transducer and activator of transcription 3 signaling. Lab Invest 2009; 89: 1128-1139 [PMID: 19652645 DOI: 10.1038/labinvest. 2009.82]
46. Huang YH, Yu-Hsieh H, Huang CC, Shin-Mu VT, Tai MH, Chen CL, Chuang JH. Liver hepcidin and stainable iron expression in biliary atresia. Pediatr Res 2006; 59: 662-666 [PMID: 16627878 DOI: 10.1203/01.pdr.0000214974.55049.f1]
47. Huang YH, Chou MH, Du YY, Huang CC, Wu CL, Chen CL, Chuang JH. Expression of toll-like receptors and type 1. interferon specific protein MxA in biliary atresia. Lab Invest 2007; 87: 66-74 [PMID: 17075576 DOI: 10.1038/labinvest. 3700490]
48. Huang H, Constante M, Layoun A, Santos MM. Contribution of STAT3 and SMAD4 pathways to the regulation of hepcidin by opposing stimuli. Blood 2009; 113: 3593-3599 [PMID: 19204324 DOI: 10.1182/blood-2008-08-173641]
49. Ganz T. Hepcidin, a key regulator of iron metabolism and mediator of anemia of inflammation. Blood 2003; 102: 783-788 [PMID: 12663437 DOI: 10.1182/blood-2003-03-0672]
50. Andrews NC. Forging a field: the golden age of iron biology. Blood 2008; 112: 219-230 [PMID: 18606887 DOI: 10.1182/ blood-2007-12-077388]
51. Pae HO, Lee YC, Chung HT. Heme oxygenase-1 and carbon monoxide: emerging therapeutic targets in inflammation and allergy. Recent Pat Inflamm Allergy Drug Discov 2008; 2: 159-165 [PMID: 19076005]
52. Yao P, Nussler A, Liu L, Hao L, Song F, Schirmeier A, Nussler N. Quercetin protects human hepatocytes from ethanol-derived oxidative stress by inducing heme oxygenase-1 via the MAPK/Nrf2 pathways. J Hepatol 2007; 47: 253-261 [PMID: 17433488 DOI: 10.1016/j.jhep.2007.02.008]
53. Lamb NJ, Quinlan GJ, Mumby S, Evans TW, Gutteridge JM. Haem oxygenase shows pro-oxidant activity in microsomal and cellular systems: implications for the release of lowmolecular-mass iron. Biochem J 1999; 344 Pt 1: 153-158 [PMID: 10548545]
54. Okada S. Iron-induced tissue damage and cancer: the role of reactive oxygen species-free radicals. Pathol Int 1996; 46: 311-332 [PMID: 8809878]
55. Pietrangelo A. Metals, oxidative stress, and hepatic fibrogenesis. Semin Liver Dis 1996; 16: 13-30 [PMID: 8723320 DOI: 10.1055/s-2007-1007215]
56. Pietrangelo A. Hereditary hemochromatosis--a new look at an old disease. N Engl J Med 2004; 350: 2383-2397 [PMID: 15175440 DOI: 10.1056/NEJMra031573]
57. Myers BM, Prendergast FG, Holman R, Kuntz SM, LaRusso NF. Alterations in the structure, physicochemical properties, and pH of hepatocyte lysosomes in experimental iron overload. J Clin Invest 1991; 88: 1207-1215 [PMID: 1918375 DOI: 10.1172/JCI115423]
58. Pietrangelo A, Borella F, Casalgrandi G, Montosi G, Ceccarelli D, Gallesi D, Giovannini F, Gasparetto A, Masini A. Antioxidant activity of silybin in vivo during long-term iron overload in rats. Gastroenterology 1995; 109: 1941-1949 [PMID: 7498660]
59. Moon MS, McDevitt EI, Zhu J, Stanley B, Krzeminski J, Amin S, Aliaga C, Miller TG, Isom HC. Elevated hepatic iron activates NF-E2-related factor 2-regulated pathway in a dietary iron overload mouse model. Toxicol Sci 2012; 129: 74-85 [PMID: 22649188 DOI: 10.1093/toxsci/kfs193]
60. Numazawa S, Ishikawa M, Yoshida A, Tanaka S, Yoshida T. Atypical protein kinase C mediates activation of NF-E2-related factor 2 in response to oxidative stress. Am J Physiol Cell Physiol 2003; 285: C334-C342 [PMID: 12700136 DOI: 10.1152/ajpcell.00043.2003]
61. Baird L, Dinkova-Kostova AT. The cytoprotective role of the Keap1-Nrf2 pathway. Arch Toxicol 2011; 85: 241-272 [PMID: 21365312 DOI: 10.1007/s00204-011-0674-5]
62. Parola M, Robino G. Oxidative stress-related molecules and liver fibrosis. J Hepatol 2001; 35: 297-306 [PMID: 11580156]
63. Maher JJ, Tzagarakis C, Giménez A. Malondialdehyde stimulates collagen production by hepatic lipocytes only upon activation in primary culture. Alcohol Alcohol 1994; 29: 605-610 [PMID: 7811345]
64. De Bleser PJ, Xu G, Rombouts K, Rogiers V, Geerts A. Glutathione levels discriminate between oxidative stress and transforming growth factor-beta signaling in activated rat hepatic stellate cells. J Biol Chem 1999; 274: 33881-33887 [PMID: 10567349]
65. Farmaki K, Tzoumari I, Pappa C, Chouliaras G, Berdoukas V. Normalisation of total body iron load with very intensive combined chelation reverses cardiac and endocrine complications of thalassaemia major. Br J Haematol 2010; 148: 466-475 [PMID: 19912219 DOI: 10.1111/j.1365-2141.2009.07970.x]
66. Anderson LJ, Westwood MA, Holden S, Davis B, Prescott E, Wonke B, Porter JB, Walker JM, Pennell DJ. Myocardial iron clearance during reversal of siderotic cardiomyopathy with intravenous desferrioxamine: a prospective study using T2* cardiovascular magnetic resonance. Br J Haematol 2004; 127: 348-355 [PMID: 15491298 DOI: 10.1111/ j.1365-2141.2004.05202.x]
67. Kew MC. Hepatic iron overload and hepatocellular carcinoma. Cancer Lett 2009; 286: 38-43 [PMID: 19081672 DOI: 10.1016/j.canlet.2008.11.001]