Protective role of hemeoxygenase-1 in gastrointestinal diseases

Cellular and Molecular Life Sciences

Volumn 72, Issue 6, 2015, Pages 1161-1173

  Chang, Marisol ^a   Xue, Jing ^a   Sharma, Vishal ^a   Habtezion, Aida ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Biliverdin; Carbon monoxide; Hemeoxygenase 1

Indexed keywords

CASPASE 3; GAMMA INTERFERON; HEMATIN; HEME OXYGENASE 1; HEMIN; INTERLEUKIN 10; INTERLEUKIN 22; INTERLEUKIN 6; MALONALDEHYDE; MITOGEN ACTIVATED PROTEIN KINASE; MYELOPEROXIDASE; OCTREOTIDE; PROTEIN KINASE B; TRANSCRIPTION FACTOR NRF2; TUMOR NECROSIS FACTOR ALPHA; BILIVERDIN; CARBON MONOXIDE;

ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; CELL PROTECTION; CROHN DISEASE; ENZYME ACTIVITY; EPITHELIUM CELL; ESOPHAGITIS; ESOPHAGUS ULCER; GASTROINTESTINAL DISEASE; HUMAN; LARGE INTESTINE DISEASE; LIVER FIBROSIS; LIVER INJURY; LYMPHOCYTE; NECROTIZING ENTEROCOLITIS; NEUTROPHIL; NONHUMAN; PANCREAS ADENOCARCINOMA; PANCREATITIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; RADIATION ENTEROPATHY; REGULATORY MECHANISM; REPERFUSION INJURY; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; SMALL INTESTINE DISEASE; STOMACH PARESIS; STOMACH ULCER; ULCERATIVE COLITIS; UPREGULATION; ANIMAL; DRUG EFFECTS; GASTROINTESTINAL DISEASES; GASTROINTESTINAL TRACT; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; INFLAMMATION; METABOLISM; MOLECULARLY TARGETED THERAPY; PATHOLOGY;

ANIMALS; BILIVERDINE; CARBON MONOXIDE; GASTROINTESTINAL DISEASES; GASTROINTESTINAL TRACT; GENE EXPRESSION REGULATION; HEME OXYGENASE-1; HUMANS; INFLAMMATION; MOLECULAR TARGETED THERAPY;

EID: 84925482428     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-014-1790-1     Document Type: Article

References (154)

1. Tenhunen R, Marver HS, Schmid R (1968) The enzymatic conversion of heme to bilirubin by microsomal heme oxygenase. Proc Natl Acad Sci USA 61(2):748
2. Kapitulnik J, Maines MD (2009) Pleiotropic functions of biliverdin reductase: cellular signaling and generation of cytoprotective and cytotoxic bilirubin. Trends Pharmacol Sci 30(3):129-137
3. Maines MD (1997) The heme oxygenase system: a regulator of second messenger gases. Annu Rev Pharmacol Toxicol 37(1):517-554
4. Mccoubrey WK, Huang T, Maines MD (1997) Isolation and characterization of a cDNA from the rat brain that encodes hemoprotein heme oxygenase-3. Eur J Biochem 247(2):725-732
5. Elbirt KK, Bonkovsky HL (1998) Heme oxygenase: recent advances in understanding its regulation and role. Proc Assoc Am Phys 111(5):438-447
6. Trakshel G, Kutty R, Maines M (1986) Purification and characterization of the major constitutive form of testicular heme oxygenase. The noninducible isoform. J Biol Chem 261(24):11131-11137
7. Maines MD (1992) Heme oxygenase: clinical applications and functions. CRC Press
8. Maines MD, Snyder R (1984) New developments in the regulation of heme metabolism and their implications. CRC Crit Rev Toxicol 12(3):241-314
9. Tsuji T, Kato A, Yasuda H, Miyaji T, Luo J, Sakao Y, Ito H, Fujigaki Y, Hishida A (2009) The dimethylthiourea-induced attenuation of cisplatin nephrotoxicity is associated with the augmented induction of heat shock proteins. Toxicol Appl Pharmacol 234(2):202-208
10. Umeda K, Takahashi T, Inoue K, Shimizu H, Maeda S, Morimatsu H, Omori E, Akagi R, Katayama H, Morita K (2009) Prevention of hemorrhagic shock-induced intestinal tissue injury by glutamine via heme oxygenase-1 induction. Shock 31(1):40-49
11. Cooper KL, Liu KJ, Hudson LG (2009) Enhanced ROS production and redox signaling with combined arsenite and UVA exposure: contribution of NADPH oxidase. Free Radic Biol Med 47(4):381-388
12. Chang AY, Chan JY, Cheng H-L, Tsai C-Y, Chan SH (2009) Hypoxia-inducible factor 1/heme oxygenase 1 cascade as upstream signals in the prolife role of heat shock protein 70 at rostral ventrolateral medulla during experimental brain stem death. Shock 32(6):651-658
13. Terry CM, Clikeman JA, Hoidal JR, Callahan KS (1998) Effect of tumor necrosis factor-α and interleukin-1α on heme oxygenase-1 expression in human endothelial cells. Am J Physiol Heart Circ Physiol 274(3):H883-H891
14. Niess AM, Passek F, Lorenz I, Schneider EM, Dickhuth H-H, Northoff H, Fehrenbach E (1999) Expression of the antioxidant stress protein heme oxygenase-1 (HO-1) in human leukocytes: acute and adaptational responses to endurance exercise. Free Radic Biol Med 26(1):184-192
15. Nath KA, Balla G, Vercellotti GM, Balla J, Jacob HS, Levitt M, Rosenberg ME (1992) Induction of heme oxygenase is a rapid, protective response in rhabdomyolysis in the rat. J Clin Investig 90(1):267
16. Keyse SM, Applegate L, Tromvoukis Y, Tyrrell R (1990) Oxidant stress leads to transcriptional activation of the human heme oxygenase gene in cultured skin fibroblasts. Mol Cell Biol 10(9):4967-4969
17. Applegate LA, Luscher P, Tyrrell RM (1991) Induction of heme oxygenase: a general response to oxidant stress in cultured mammalian cells. Cancer Res 51(3):974-978
18. Abraham NG, Rezzani R, Rodella L, Kruger A, Taller D, Volti GL, Goodman AI, Kappas A (2004) Overexpression of human heme oxygenase-1 attenuates endothelial cell sloughing in experimental diabetes. Am J Physiol Heart Circ Physiol 287(6):H2468-H2477
19. Otterbein LE, Bach FH, Alam J, Soares M, Lu HT, Wysk M, Davis RJ, Flavell RA, Choi AM (2000) Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nat Med 6(4):422-428
20. Petrache I, Otterbein LE, Alam J, Wiegand GW, Choi AM (2000) Heme oxygenase-1 inhibits TNF-α-induced apoptosis in cultured fibroblasts. Am J Physiol-Lung Cell Mol Physiol 278(2):L312-L319
21. Lee T-S, Chau L-Y (2002) Heme oxygenase-1 mediates the anti-inflammatory effect of interleukin-10 in mice. Nat Med 8(3):240-246
22. Stocker R, Yamamoto Y, McDonagh AF, Glazer AN, Ames BN (1987) Bilirubin is an antioxidant of possible physiological importance. Science 235(4792):1043-1046
23. Barañano DE, Rao M, Ferris CD, Snyder SH (2002) Biliverdin reductase: a major physiologic cytoprotectant. Proc Natl Acad Sci 99(25):16093-16098
24. Sedlak TW, Snyder SH (2004) Bilirubin benefits: cellular protection by a biliverdin reductase antioxidant cycle. Pediatrics 113(6):1776-1782
25. Nakao A, Otterbein LE, Overhaus M, Sarady JK, Tsung A, Kimizuka K, Nalesnik MA, Kaizu T, Uchiyama T, Liu F (2004) Biliverdin protects the functional integrity of a transplanted syngeneic small bowel. Gastroenterology 127(2):595-606
26. Xue J, Nguyen DT, Habtezion A (2012) Aryl hydrocarbon receptor regulates pancreatic IL-22 production and protects mice from acute pancreatitis. Gastroenterology 143(6):1670-1680. doi: 10.1053/j.gastro.2012.08.051
27. Balla G, Jacob HS, Balla J, Rosenberg M, Nath K, Apple F, Eaton J, Vercellotti G (1992) Ferritin: a cytoprotective antioxidant stratagem of endothelium. J Biol Chem 267(25):18148-18153
28. Juckett MB, Balla J, Balla G, Jessurun J, Jacob HS, Vercellotti GM (1995) Ferritin protects endothelial cells from oxidized low density lipoprotein in vitro. Am J Pathol 147(3):782
29. Kapturczak MH, Wasserfall C, Brusko T, Campbell-Thompson M, Ellis TM, Atkinson MA, Agarwal A (2004) Heme oxygenase-1 modulates early inflammatory responses: evidence from the heme oxygenase-1-deficient mouse. Am J Pathol 165(3):1045-1053
30. Poss KD, Tonegawa S (1997) Reduced stress defense in heme oxygenase 1-deficient cells. Proc Natl Acad Sci 94(20):10925-10930
31. Tzima S, Victoratos P, Kranidioti K, Alexiou M, Kollias G (2009) Myeloid heme oxygenase-1 regulates innate immunity and autoimmunity by modulating IFN-β production. J Exp Med 206(5):1167-1179
32. True AL, Olive M, Boehm M, San H, Westrick RJ, Raghavachari N, Xu X, Lynn EG, Sack MN, Munson PJ (2007) Heme oxygenase-1 deficiency accelerates formation of arterial thrombosis through oxidative damage to the endothelium, which is rescued by inhaled carbon monoxide. Circ Res 101(9):893-901
33. Vachharajani TJ, Work J, Issekutz AC, Granger DN (2000) Heme oxygenase modulates selectin expression in different regional vascular beds. Am J Physiol Heart Circ Physiol 278(5):H1613-H1617
34. Burnett AL, Johns DG, Kriegsfeld LJ, Klein SL, Calvin DC, Demas GE, Schramm LP, Tonegawa S, Nelson RJ, Snyder SH (1998) Ejaculatory abnormalities in mice with targeted disruption of the gene for heme oxygenase-2. Nat Med 4(1):84-87
35. Yachie A, Niida Y, Wada T, Igarashi N, Kaneda H, Toma T, Ohta K, Kasahara Y, Koizumi S (1999) Oxidative stress causes enhanced endothelial cell injury in human heme oxygenase-1 deficiency. J Clin Investig 103(1):129-135
36. Radhakrishnan N, Yadav SP, Sachdeva A, Pruthi PK, Sawhney S, Piplani T, Wada T, Yachie A (2011) Human heme oxygenase-1 deficiency presenting with hemolysis, nephritis, and asplenia. J Pediatr Hematol Oncol 33(1):74-78
37. Igarashi K, Sun J (2006) The heme-Bach1 pathway in the regulation of oxidative stress response and erythroid differentiation. Antioxid Redox Signal 8(1-2):107-118
38. Jang JS, Piao S, Cha Y-N, Kim C (2009) Taurine chloramine activates Nrf2, increases HO-1 expression and protects cells from death caused by hydrogen peroxide. J Clin Biochem Nutr 45(1):37
39. De Backer O, Elinck E, Blanckaert B, Leybaert L, Motterlini R, Lefebvre RA (2009) Water-soluble CO-releasing molecules reduce the development of postoperative ileus via modulation of MAPK/HO-1 signalling and reduction of oxidative stress. Gut 58(3):347-356
40. Salinas M, Wang J, Rosa de Sagarra M, Martín D, Rojo AI, Martin-Perez J, Ortiz de Montellano PR, Cuadrado A (2004) Protein kinase Akt/PKB phosphorylates heme oxygenase-1 in vitro and in vivo. FEBS Lett 578(1):90-94
41. Exner M, Minar E, Wagner O, Schillinger M (2004) The role of heme oxygenase-1 promoter polymorphisms in human disease. Free Radic Biol Med 37(8):1097-1104
42. Ono K, Mannami T, Iwai N (2003) Association of a promoter variant of the haeme oxygenase-1 gene with hypertension in women. J Hypertens 21(8):1497-1503
43. Ono K, Goto Y, Takagi S, Baba S, Tago N, Nonogi H, Iwai N (2004) A promoter variant of the heme oxygenase-1 gene may reduce the incidence of ischemic heart disease in Japanese. Atherosclerosis 173(2):313-317
44. Gulla A, Evans BJ, Navenot JM, Pundzius J, Barauskas G, Gulbinas A, Dambrauskas Z, Arafat H, Wang Z-X (2014) Heme Oxygenase-1 Gene Promoter Polymorphism Is Associated With the Development of Necrotizing Acute Pancreatitis. Pancreas 43(8):1271-1276
45. Yamada N, Yamaya M, Okinaga S, Nakayama K, Sekizawa K, Shibahara S, Sasaki H (2000) Microsatellite polymorphism in the heme oxygenase-1 gene promoter is associated with susceptibility to emphysema. Am J Human Genet 66(1):187-195
46. Rueda B, Oliver J, Robledo G, López-Nevot MA, Balsa A, Pascual-Salcedo D, González-Gay MA, González-Escribano MF, Martín J (2007) HO-1 promoter polymorphism associated with rheumatoid arthritis. Arthritis Rheum 56(12):3953-3958
47. Schillinger M, Exner M, Minar E, Mlekusch W, Müllner M, Mannhalter C, Bach FH, Wagner O (2004) Heme oxygenase-1 genotype and restenosis after balloon angioplasty: a novel vascular protective factor. J Am Coll Cardiol 43(6):950-957
48. Chen Y-H, Lin S-J, Lin M-W, Tsai H-L, Kuo S-S, Chen J-W, Charng M-J, Wu T-C, Chen L-C, Ding P (2002) Microsatellite polymorphism in promoter of heme oxygenase-1 gene is associated with susceptibility to coronary artery disease in type 2 diabetic patients. Hum Genet 111(1):1-8
49. Immenschuh S, Tan M, Ramadori G (1999) Nitric oxide mediates the lipopolysaccharide dependent upregulation of the heme oxygenase-1 gene expression in cultured rat Kupffer cells. J Hepatol 30(1):61-69
50. Bissell DM, Hammaker L, Schmid R (1972) Liver sinusoidal cells Identification of a subpopulation for erythrocyte catabolism. J Cell Biol 54(1):107-119
51. Chauveau C, Rémy S, Royer PJ, Hill M, Tanguy-Royer S, Hubert F-X, Tesson L, Brion R, Beriou G, Gregoire M (2005) Heme oxygenase-1 expression inhibits dendritic cell maturation and proinflammatory function but conserves IL-10 expression. Blood 106(5):1694-1702
52. Wijayanti N, Huber S, Samoylenko A, Kietzmann T, Immenschuh S (2004) Role of NF-kB and p38 MAP kinase signaling pathways in the lipopolysaccharide-dependent activation of heme oxygenase-1 gene expression. Antioxid Redox Signal 6(5):802-810
53. Lin H-Y, Juan S-H, Shen S-C, Hsu F-L, Chen Y-C (2003) Inhibition of lipopolysaccharide-induced nitric oxide production by flavonoids in RAW264. 7 macrophages involves heme oxygenase-1. Biochem Pharmacol 66(9):1821-1832
54. Rémy S, Blancou P, Tesson L, Tardif V, Brion R, Royer PJ, Motterlini R, Foresti R, Painchaut M, Pogu S (2009) Carbon monoxide inhibits TLR-induced dendritic cell immunogenicity. J Immunol 182(4):1877-1884
55. George JF, Braun A, Brusko TM, Joseph R, Bolisetty S, Wasserfall CH, Atkinson MA, Agarwal A, Kapturczak MH (2008) Suppression by CD4+ CD25+ regulatory t cells is dependent on expression of heme oxygenase-1 in antigen-presenting cells. Am J Pathol 173(1):154-160
56. Moreau A, Hill M, Thebault P, Deschamps J, Chiffoleau E, Chauveau C, Moullier P, Anegon I, Alliot-Licht B, Cuturi M (2009) Tolerogenic dendritic cells actively inhibit T cells through heme oxygenase-1 in rodents and in nonhuman primates. FASEB J 23(9):3070-3077
57. Nakamichi I, Habtezion A, Zhong B, Contag CH, Butcher EC, Omary MB (2005) Hemin-activated macrophages home to the pancreas and protect from acute pancreatitis via heme oxygenase-1 induction. J Clin Investig 115(11):3007-3014
58. Wegiel B, Hedblom A, Li M, Gallo D, Csizmadia E, Harris C, Nemeth Z, Zuckerbraun B, Soares M, Persson JL (2014) Heme oxygenase-1 derived carbon monoxide permits maturation of myeloid cells. Cell Death Dis 5(3):e1139
59. Choi KM, Kashyap PC, Dutta N, Stoltz GJ, Ordog T, Shea Donohue T, Bauer AJ, Linden DR, Szurszewski JH, Gibbons SJ (2010) CD206-positive M2 macrophages that express heme oxygenase-1 protect against diabetic gastroparesis in mice. Gastroenterology 138(7):2399-2409 (e2391)
60. Coëffier M, Le Pessot F, Leplingard A, Marion R, Lerebours E, Ducrotté P, Déchelotte P (2002) Acute enteral glutamine infusion enhances heme oxygenase-1 expression in human duodenal mucosa. J Nutr 132(9):2570-2573
61. Barton S, Rampton D, Winrow V, Domizio P, Feakins R (2003) Expression of heat shock protein 32 (hemoxygenase-1) in the normal and inflamed human stomach and colon: an immunohistochemical study. Cell Stress Chaperones 8(4):329
62. Goda N, Suzuki K, Naito M, Takeoka S, Tsuchida E, Ishimura Y, Tamatani T, Suematsu M (1998) Distribution of heme oxygenase isoforms in rat liver. Topographic basis for carbon monoxide-mediated microvascular relaxation. J Clin Investig 101(3):604
63. Guo J, Cho C, Wang J, Koo M (2002) Expression and immunolocalization of heat shock proteins in the healing of gastric ulcers in rats. Scand J Gastroenterol 37(1):17-22
64. Giriş M, Erbil Y, Doʇru-Abbasoʇlu S, YanIk BT, AlIş H, Olgaç V, Toker GA (2007) The effect of heme oxygenase-1 induction by glutamine on TNBS-induced colitis. Int J Colorectal Dis 22(6):591-599
65. Paul G, Bataille F, Obermeier F, Bock J, Klebl F, Strauch U, Lochbaum D, Rümmele P, Farkas S, Schölmerich J (2005) Analysis of intestinal haem-oxygenase-1 (HO-1) in clinical and experimental colitis. Clin Exp Immunol 140(3):547-555
66. Wang W, Guo X, Koo M, Wong B, Lam S, Ye Y, Cho C (2001) Protective role of heme oxygenase-1 on trinitrobenzene sulfonic acid-induced colitis in rats. American Journal of Physiology-Gastrointestinal and Liver. Physiology 281(2):G586-G594
67. Takagi T, Naito Y, Mizushima K, Nukigi Y, Okada H, Suzuki T, Hirata I, Omatsu T, Okayama T, Handa O (2008) Increased intestinal expression of heme oxygenase-1 and its localization in patients with ulcerative colitis. J Gastroenterol Hepatol 23:S229-S233
68. Tsui TY, Lau CK, Ma J, Wu X, Wang YQ, Farkas S, Xu R, Schlitt HJ, Fan ST (2005) rAAV-mediated stable expression of heme oxygenase-1 in stellate cells: a new approach to attenuate liver fibrosis in rats. Hepatology 42(2):335-342
69. Werkström V, Ny L, Persson K, Andersson KE (1997) Carbon monoxide-induced relaxation and distribution of haem oxygenase isoenzymes in the pig urethra and lower oesophagogastric junction. Br J Pharmacol 120(2):312-318
70. Ny L, Alm P, Ekström P, Larsson B, Grundemar L, Andersson KE (1996) Localization and activity of haem oxygenase and functional effects of carbon monoxide in the feline lower oesophageal sphincter. Br J Pharmacol 118(2):392-399
71. Lillemoe K, Johnson L, Harmon J (1982) Role of the components of the gastroduodenal contents in experimental acid esophagitis. Surgery 92(2):276-284
72. Kruel CRP, Pinto LFR, Blanco TCM, Barja-Fidalgo TC, Melo LL, Kruel CDP (2010) Evaluation of the heme oxygenase-1 expression in esophagitis and esophageal cancer induced by different reflux experimental models and diethylnitrosamine. Acta Cirurgica Brasileira 25(3):304-310
73. Bjorkman D (1998) Nonsteroidal anti-inflammatory drug-associated toxicity of the liver, lower gastrointestinal tract, and esophagus. Am J Med 105(5):17S-21S
74. Uc A, Zhu X, Wagner BA, Buettner GR, Berg DJ (2012) Heme oxygenase-1 is protective against nonsteroidal anti-inflammatory drug-induced gastric ulcers. J Pediatr Gastroenterol Nutr 54(4):471-476
75. Aburaya M, Tanaka K-I, Hoshino T, Tsutsumi S, Suzuki K, Makise M, Akagi R, Mizushima T (2006) Heme oxygenase-1 protects gastric mucosal cells against non-steroidal anti-inflammatory drugs. J Biol Chem 281(44):33422-33432
76. Cheng Y-T, Wu C-H, Ho C-Y, Yen G-C (2013) Catechin protects against ketoprofen-induced oxidative damage of the gastric mucosa by up-regulating Nrf2 in vitro and in vivo. J Nutr Biochem 24(2):475-483
77. Ueda K, Ueyama T, Oka M, Ito T, Tsuruo Y, Ichinose M (2009) Polaprezinc (Zinc L-carnosine) is a potent inducer of anti-oxidative stress enzyme, heme oxygenase (HO)-1-a new mechanism of gastric mucosal protection. J Pharmacol Sci 110(3):285-294
78. Choi E-J, Oh H-M, Na B-R, Ramesh T, Lee H-J, Choi C-S, Choi S-C, Oh T-Y, Choi S-J, Chae J-R (2008) Eupatilin protects gastric epithelial cells from oxidative damage and down-regulates genes responsible for the cellular oxidative stress. Pharm Res 25(6):1355-1364
79. Takagi T, Naito Y, Okada H, Ishii T, Mizushima K, Akagiri S, Adachi S, Handa O, Kokura S, Ichikawa H (2009) Lansoprazole, a proton pump inhibitor, mediates anti-inflammatory effect in gastric mucosal cells through the induction of heme oxygenase-1 via activation of NF-E2-related factor 2 and oxidation of kelch-like ECH-associating protein 1. J Pharmacol Exp Ther 331(1):255-264
80. Song HJ, Shin CY, Oh TY, Min YS, Park ES, Sohn UD (2009) Eupatilin with heme oxygenase-1-inducing ability protects cultured feline esophageal epithelial cells from cell damage caused by indomethacin. Biol Pharm Bull 32(4):589-596
81. Kadinov B, Itzev D, Gagov H, Christova T, Bolton T, Duridanova D (2002) Induction of heme oxygenase in guinea-pig stomach: roles in contraction and in single muscle cell ionic currents. Acta Physiol Scand 175(4):297-313
82. Choi KM, Gibbons SJ, Nguyen TV, Stoltz GJ, Lurken MS, Ordog T, Szurszewski JH, Farrugia G (2008) Heme oxygenase-1 protects interstitial cells of Cajal from oxidative stress and reverses diabetic gastroparesis. Gastroenterology 135(6):2055-2064 (e2052)
83. Takagi T, Naito Y, Mizushima K, Nukigi Y, Okada H, Suzuki T, Hirata I, Omatsu T, Okayama T, Handa O (2008) Increased intestinal expression of heme oxygenase-1 and its localization in patients with ulcerative colitis. J Gastroenterol Hepatol 23(s2):S229-S233
84. Higuchi K, Yoda Y, Amagase K, Kato S, Tokioka S, Murano M, Takeuchi K, Umegaki E (2009) Prevention of NSAID-induced small intestinal mucosal injury: prophylactic potential of lansoprazole. J Clin Biochem Nutr 45(2):125
85. Yoda Y, Amagase K, Kato S, Tokioka S, Murano M, Kakimoto K, Nishio H, Umegaki E, Takeuchi K, Higuchi K (2010) Prevention by lansoprazole, a proton pump inhibitor, of indomethacin-induced small intestinal ulceration in rats through induction of heme oxygenase-1. J Physiol Pharmacol 61(3):287
86. Yeh CT, Chiu HF, Yen GC (2009) Protective effect of sulforaphane on indomethacin-induced cytotoxicity via heme oxygenase-1 expression in human intestinal Int 407 cells. Mol Nutr Food Res 53(9):1166-1176
87. Chung SW, Liu X, Macias AA, Baron RM, Perrella MA (2008) Heme oxygenase-1-derived carbon monoxide enhances the host defense response to microbial sepsis in mice. J Clin Investig 118(1):239-247
88. Tamion F, Richard V, Lacoume Y, Thuillez C (2002) Intestinal preconditioning prevents systemic inflammatory response in hemorrhagic shock. Role of HO-1. Am J Physiol-Gastrointest Liver Physiol 283(2):G408-G414
89. Attuwaybi B, Kozar R, Moore-Olufemi S, Sato N, Hassoun H, Weisbrodt N, Moore F (2004) Heme oxygenase-1 induction by hemin protects against gut ischemia/reperfusion injury. J Surg Res 118(1):53-57
90. Mallick IH, Winslet MC, Seifalian AM (2010) Ischemic preconditioning of small bowel mitigates the late phase of reperfusion injury: heme oxygenase mediates cytoprotection. Am J Surg 199(2):223-231
91. Wasserberg N, Pileggi A, Salgar SK, Ruiz P, Ricordi C, Inverardi L, Tzakis AG (2007) Heme oxygenase-1 upregulation protects against intestinal ischemia/reperfusion injury: a laboratory based study. Int J Surg 5(4):216-224
92. Tamaki T, Konoeda Y, Yasuhara M, Tanaka M, Yokota N, Hayashi T, Katori M, Uchida Y, Kawamura A (1999) Glutamine-induced heme oxygenase-1 protects intestines and hearts from warm ischemic injury. In: Transplantation proceedings, vol 1. Elsevier, pp 1018-1019
93. Mallick IH, Yang W-X, Winslet MC, Seifalian AM (2005) Pyrrolidine dithiocarbamate reduces ischemia-reperfusion injury of the small intestine. World J Gastroenterol 11(46):7308
94. Yoshida T, Maulik N, Ho Y-S, Alam J, Das DK (2001) Hmox-1 constitutes an adaptive response to effect antioxidant cardio protection a study with transgenic mice heterozygous for targeted disruption of the heme oxygenase-1 gene. Circulation 103(12):1695-1701
95. Liu X, Wei J, Peng DH, Layne MD, Yet S-F (2005) Absence of heme oxygenase-1 exacerbates myocardial ischemia/reperfusion injury in diabetic mice. Diabetes 54(3):778-784
96. Yano Y, Ozono R, Oishi Y, Kambe M, Yoshizumi M, Ishida T, Omura S, Oshima T, Igarashi K (2006) Genetic ablation of the transcription repressor Bach1 leads to myocardial protection against ischemia/reperfusion in mice. Genes Cells 11(7):791-803
97. Scott JR, Cukiernik MA, Ott MC, Bihari A, Badhwar A, Gray DK, Harris KA, Parry NG, Potter RF (2009) Low-dose inhaled carbon monoxide attenuates the remote intestinal inflammatory response elicited by hindlimb ischemia-reperfusion. Am J Physiol-Gastrointest Liver Physiol 296(1):G9-G14
98. Nakao A, Kaczorowski DJ, Sugimoto R, Billiar TR, McCurry KR (2008) Application of heme oxygenase-1, carbon monoxide and biliverdin for the prevention of intestinal ischemia/reperfusion injury. J Clin Biochem Nutr 42(2):78
99. Nakao A, Kimizuka K, Stolz DB, Neto JS, Kaizu T, Choi AM, Uchiyama T, Zuckerbraun BS, Nalesnik MA, Otterbein LE (2003) Carbon monoxide inhalation protects rat intestinal grafts from ischemia/reperfusion injury. Am J Pathol 163(4):1587-1598
100. Fondevila C, Shen XD, Tsuchiyashi S, Yamashita K, Csizmadia E, Lassman C, Busuttil RW, Kupiec-Weglinski JW, Bach FH (2004) Biliverdin therapy protects rat livers from ischemia and reperfusion injury. Hepatology 40(6):1333-1341
101. Yun KJ, Choi SC, Oh JM (2005) Expression of heme oxygenase-1 in ischemic colitis. Korean J Gastroenterol (Taehan Sohwagi Hakhoe chi) 45(5):335-339
102. Gasche C, Scholmerich J, Brynskov J, D'Haens G, Hanauer SB, Irvine EJ, Jewell DP, Rachmilewitz D, Sachar DB, Sandborn WJ (2000) A simple classification of Crohn's disease: report of the working party for the World Congresses of Gastroenterology, Vienna 1998. Inflamm Bowel Dis 6(1):8-15
103. Naito Y, Takagi T, Yoshikawa T (2004) Heme oxygenase-1: a new therapeutic target for inflammatory bowel disease. Aliment Pharmacol Ther 20:177-184
104. Zhong W, Xia Z, Hinrichs D, Rosenbaum JT, Wegmann KW, Meyrowitz J, Zhang Z (2010) Hemin Exerts Multiple Protective Mechanisms and Attenuates Dextran Sulfate Sodium-induced Colitis. J Pediatr Gastroenterol Nutr 50(2):132-139
105. Varga C, Laszlo F, Fritz P, Cavicchi M, Lamarque D, Horvath K, Posa A, Berko A, Whittle BJ (2007) Modulation by heme and zinc protoporphyrin of colonic heme oxygenase-1 and experimental inflammatory bowel disease in the rat. Eur J Pharmacol 561(1):164-171
106. Berberat PO, Yamashita K, Warny MM, Csizmadia E, Robson SC, Bach FH (2005) Heme oxygenase-1-generated biliverdin ameliorates experimental murine colitis. Inflamm Bowel Dis 11(4):350-359
107. Khor TO, Huang M-T, Kwon KH, Chan JY, Reddy BS, Kong A-N (2006) Nrf2-deficient mice have an increased susceptibility to dextran sulfate sodium-induced colitis. Cancer Res 66(24):11580-11584
108. Harusato A, Naito Y, Takagi T, Uchiyama K, Mizushima K, Hirai Y, Higashimura Y, Katada K, Handa O, Ishikawa T (2013) BTB and CNC homolog 1 (Bach1) deficiency ameliorates TNBS colitis in mice: role of M2 macrophages and heme oxygenase-1. Inflamm Bowel Dis 19(4):740-753
109. Hegazi RA, Rao KN, Mayle A, Sepulveda AR, Otterbein LE, Plevy SE (2005) Carbon monoxide ameliorates chronic murine colitis through a heme oxygenase 1-dependent pathway. J Exp Med 202(12):1703-1713
110. Sheikh SZ, Hegazi RA, Kobayashi T, Onyiah JC, Russo SM, Matsuoka K, Sepulveda AR, Li F, Otterbein LE, Plevy SE (2011) An anti-inflammatory role for carbon monoxide and heme oxygenase-1 in chronic Th2-mediated murine colitis. J Immunol 186(9):5506
111. Horváth K, Varga C, Berkó A, Pósa A, László F, Whittle BJ (2008) The involvement of heme oxygenase-1 activity in the therapeutic actions of 5-aminosalicylic acid in rat colitis. Eur J Pharmacol 581(3):315-323
112. Schulz S, Wong RJ, Jang KY, Kalish F, Chisholm KM, Zhao H, Vreman HJ, Sylvester KG, Stevenson DK (2013) Heme oxygenase-1 deficiency promotes the development of necrotizing enterocolitis-like intestinal injury in a newborn mouse model. Am J Physiol-Gastrointest Liver Physiol 304(11):G991-G1001
113. Santulli TV, Schullinger JN, Heird WC, Gongaware RD, Wigger J, Barlow B, Blanc WA, Berdon WE (1975) Acute necrotizing enterocolitis in infancy: a review of 64 cases. Pediatrics 55(3):376-387
114. Yeoh E, Horowitz M (1987) Radiation enteritis. Surg Gynecol Obstet 165(4):373-379
115. Giriş M, Erbil Y, Öztezcan S, Olgaç V, Barbaros U, Deveci U, Kirgiz B, Uysal M, Toker GA (2006) The effect of heme oxygenase-1 induction by glutamine on radiation-induced intestinal damage: the effect of heme oxygenase-1 on radiation enteritis. Am J Surg 191(4):503-509
116. Wang J, Zheng H, Sung C-C, Hauer-Jensen M (1999) The synthetic somatostatin analogue, octreotide, ameliorates acute and delayed intestinal radiation injury. Int J Radiat Oncol Biol Phys 45(5):1289-1296
117. Abbasoʇlu SD, Erbil Y, Eren T, Giriş M, Barbaros U, Yücel R, Olgaç V, Uysal M, Toker G (2006) The effect of heme oxygenase-1 induction by octreotide on radiation enteritis. Peptides 27(6):1570-1576
118. Xue J, Sharma V, Habtezion A (2014) Immune cells and immune-based therapy in pancreatitis. Immunol Res 58(2-3):378-386. doi: 10.1007/s12026-014-8504-5
119. Yadav D, Lowenfels AB (2013) The epidemiology of pancreatitis and pancreatic cancer. Gastroenterology 144(6):1252-1261. doi: 10.1053/j.gastro.2013.01.068
120. Sarles H (1986) Etiopathogenesis and definition of chronic pancreatitis. Dig Dis Sci 31(9 Suppl):91S-107S
121. Zheng L, Xue J, Jaffee EM, Habtezion A (2013) Role of immune cells and immune-based therapies in pancreatitis and pancreatic ductal adenocarcinoma. Gastroenterology 144(6):1230-1240. doi: 10.1053/j.gastro.2012.12.042
122. Nuhn P, Mitkus T, Ceyhan GO, Kunzli BM, Bergmann F, Fischer L, Giese N, Friess H, Berberat PO (2013) Heme oxygenase 1-generated carbon monoxide and biliverdin attenuate the course of experimental necrotizing pancreatitis. Pancreas 42(2):265-271. doi: 10.1097/MPA.0b013e318264cc8b
123. Xue J, Habtezion A (2014) Carbon monoxide-based therapy ameliorates acute pancreatitis via TLR4 inhibition. J Clin Invest 124(1):437-447. doi: 10.1172/JCI71362
124. Sato H, Siow RC, Bartlett S, Taketani S, Ishii T, Bannai S, Mann GE (1997) Expression of stress proteins heme oxygenase-1 and-2 in acute pancreatitis and pancreatic islet betaTC3 and acinar AR42J cells. FEBS Lett 405(2):219-223
125. Habtezion A, Kwan R, Yang AL, Morgan ME, Akhtar E, Wanaski SP, Collins SD, Butcher EC, Kamal A, Omary MB (2011) Heme oxygenase-1 is induced in peripheral blood mononuclear cells of patients with acute pancreatitis: a potential therapeutic target. Am J Physiol Gastrointest Liver Physiol 300(1):G12-G20. doi: 10.1152/ajpgi.00231.2010
126. Nakamichi I, Habtezion A, Zhong B, Contag CH, Butcher EC, Omary MB (2005) Hemin-activated macrophages home to the pancreas and protect from acute pancreatitis via heme oxygenase-1 induction. J Clin Invest 115(11):3007-3014. doi: 10.1172/JCI24912
127. Habtezion A, Kwan R, Akhtar E, Wanaski SP, Collins SD, Wong RJ, Stevenson DK, Butcher EC, Omary MB (2011) Panhematin provides a therapeutic benefit in experimental pancreatitis. Gut 60(5):671-679. doi: 10.1136/gut.2010.217208
128. Zhang F, Fei J, Zhao B, Chen E, Mao E (2014) Protective effect of adenoviral transfer of heme oxygenase-1 gene on rats with severe acute pancreatitis. Am J Med Sci. doi: 10.1097/MAJ.0000000000000225
129. Gordon S (2003) Alternative activation of macrophages. Nat Rev Immunol 3(1):23-35. doi: 10.1038/nri978
130. Chen P, Sun B, Chen H, Wang G, Pan S, Kong R, Bai X, Wang S (2010) Effects of carbon monoxide releasing molecule-liberated CO on severe acute pancreatitis in rats. Cytokine 49(1):15-23. doi: 10.1016/j.cyto.2009.09.013
131. Omary MB, Lugea A, Lowe AW, Pandol SJ (2007) The pancreatic stellate cell: a star on the rise in pancreatic diseases. J Clin Invest 117(1):50-59. doi: 10.1172/JCI30082
132. Schwer CI, Guerrero AM, Humar M, Roesslein M, Goebel U, Stoll P, Geiger KK, Pannen BH, Hoetzel A, Schmidt R (2008) Heme oxygenase-1 inhibits the proliferation of pancreatic stellate cells by repression of the extracellular signal-regulated kinase1/2 pathway. J Pharmacol Exp Ther 327(3):863-871. doi: 10.1124/jpet.108.136549
133. Schwer CI, Mutschler M, Stoll P, Goebel U, Humar M, Hoetzel A, Schmidt R (2010) Carbon monoxide releasing molecule-2 inhibits pancreatic stellate cell proliferation by activating p38 mitogen-activated protein kinase/heme oxygenase-1 signaling. Mol Pharmacol 77(4):660-669. doi: 10.1124/mol.109.059519
134. Amersi F, Buelow R, Kato H, Ke B, Coito AJ, Shen X-D, Zhao D, Zaky J, Melinek J, Lassman CR (1999) Upregulation of heme oxygenase-1 protects genetically fat Zucker rat livers from ischemia/reperfusion injury. J Clin Investig 104(11):1631-1639
135. Ben-Ari Z, Issan Y, Katz Y, Sultan M, Safran M, Michal L-S, Nader GA, Kornowski R, Grief F, Pappo O (2013) Induction of heme oxygenase-1 protects mouse liver from apoptotic ischemia/reperfusion injury. Apoptosis 18(5):547-555
136. Wang Y, Shen J, Xiong X, Xu Y, Zhang H, Huang C, Tian Y, Jiao C, Wang X, Li X (2014) Remote Ischemic Preconditioning Protects against Liver Ischemia-Reperfusion Injury via Heme Oxygenase-1-Induced Autophagy. PLoS ONE 9(6):e98834
137. Carchman EH, Rao J, Loughran PA, Rosengart MR, Zuckerbraun BS (2011) Heme oxygenase-1-mediated autophagy protects against hepatocyte cell death and hepatic injury from infection/sepsis in mice. Hepatology 53(6):2053-2062
138. Starzl TE, Demetris AJ (1990) Liver transplantation: a 31-year perspective part III. Curr Probl Surg 27(4):187-240
139. Sass G, Seyfried S, Parreira Soares M, Yamashita K, Kaczmarek E, Neuhuber WL, Tiegs G (2004) Cooperative effect of biliverdin and carbon monoxide on survival of mice in immune-mediated liver injury. Hepatology 40(5):1128-1135
140. Ke B, Buelow R, Shen X-D, Melinek J, Amersi F, Gao F, Ritter T, Volk H-D, Busuttil RW, Kupiec-Weglinski JW (2002) Heme oxygenase 1 gene transfer prevents CD95/Fas ligand-mediated apoptosis and improves liver allograft survival via carbon monoxide signaling pathway. Hum Gene Ther 13(10):1189-1199
141. Geuken E, Buis CI, Visser DS, Blokzijl H, Moshage H, Nemes B, Leuvenink HG, De Jong KP, Peeters PM, Slooff MJ (2005) Expression of Heme Oxygenase-1 in Human Livers Before Transplantation Correlates with Graft Injury and Function After Transplantation. Am J Transplant 5(8):1875-1885
142. Buis CI, van der Steege G, Visser DS, Nolte IM, Hepkema BG, Nijsten M, Slooff MJ, Porte RJ (2008) Heme Oxygenase-1 Genotype of the Donor Is Associated With Graft Survival After Liver Transplantation. Am J Transplant 8(2):377-385
143. Flier JS, Underhill LH, Friedman SL (1993) The Cellular Basis of Hepatic Fibrosis-Mechanisms and Treatment Strategies. N Engl J Med 328(25):1828-1835
144. Sass G, Soares MCP, Yamashita K, Seyfried S, Zimmermann WH, Eschenhagen T, Kaczmarek E, Ritter T, Volk HD, Tiegs G (2003) Heme oxygenase-1 and its reaction product, carbon monoxide, prevent inflammation-related apoptotic liver damage in mice. Hepatology 38(4):909-918
145. Wendela A ICE-protease inhibitors block murine liver injury and apoptosis caused by CD95 or by TNF-a
146. Dey A, Cederbaum AI (2006) Alcohol and oxidative liver injury. Hepatology 43(S1):S63-S74
147. Yao P, Nussler A, Liu L, Hao L, Song F, Schirmeier A, Nussler N (2007) Quercetin protects human hepatocytes from ethanol-derived oxidative stress by inducing heme oxygenase-1 via the MAPK/Nrf2 pathways. J Hepatol 47(2):253-261
148. Yao P, Hao L, Nussler N, Lehmann A, Song F, Zhao J, Neuhaus P, Liu L, Nussler A (2009) The protective role of HO-1 and its generated products (CO, bilirubin, and Fe) in ethanol-induced human hepatocyte damage. Am J Physiol-Gastrointest Liver Physiol 296(6):G1318-G1323
149. Schulz S, Wong RJ, Vreman HJ, Stevenson DK (2012) Metalloporphyrins-an update. Front Pharmacol 3
150. Bharucha AE, Kulkarni A, Choi KM, Camilleri M, Lempke M, Brunn GJ, Gibbons SJ, Zinsmeister AR, Farrugia G (2009) First-in-human study demonstrating pharmacological activation of heme oxygenase-1 in humans. Clin Pharmacol Ther 87(2):187-190
151. Abraham NG, Kappas A (2008) Pharmacological and clinical aspects of heme oxygenase. Pharmacol Rev 60(1):79-127
152. Kappas A (2004) A method for interdicting the development of severe jaundice in newborns by inhibiting the production of bilirubin. Pediatrics 113(1):119-123
153. Nielsen VG, Pretorius E (2014) Carbon monoxide: anticoagulant or procoagulant? Thromb Res 133(3):315-321
154. Bargen JA, Barker NW (1936) Extensive arterial and venous thrombosis complicating chronic ulcerative colitis. Arch Intern Med 58(1):17-31