Inflammaluteolin protects mice from severe acute pancreatitis by exerting HO-1-mediated anti-inflammatory and antioxidant effects

International Journal of Molecular Medicine

Volumn 39, Issue 1, 2017, Pages 113-125

  Xiong, Jie ^a   Wang, Kezhou ^a   Yuan, Chunxiao ^b   Xing, Rong ^b   Ni, Jianbo ^a   Hu, Guoyong ^a   Chen, Fengling ^a   Wang, Xingpeng ^a  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b DALIAN MEDICAL UNIVERSITY   (China)

Author keywords

Heme oxygenase 1; Interleukin 10; Luteolin; Nuclear factor B; Severe acute pancreatitis

Indexed keywords

AMYLASE; BETA ACTIN; CERULETIDE; HEME OXYGENASE 1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 10; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; LUTEOLIN; MALONALDEHYDE; MYELOPEROXIDASE; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; NUCLEOPROTEIN; PROTOPORPHYRIN ZINC; SUPEROXIDE DISMUTASE; TRIACYLGLYCEROL LIPASE; TUMOR NECROSIS FACTOR; ANTIINFLAMMATORY AGENT; ANTIOXIDANT; AUTACOID; CYTOKINE; PROTECTIVE AGENT; PROTOPORPHYRIN;

ACUTE PANCREATITIS; ANALYSIS OF VARIANCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; ARTICLE; CELL INFILTRATION; CENTRIFUGATION; CONTROLLED STUDY; DISEASE SEVERITY; ENZYME LINKED IMMUNOSORBENT ASSAY; FATALITY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; MULTIPLE ORGAN FAILURE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ACUTE DISEASE; ANIMAL; BIOLOGICAL MODEL; BLOOD; DRUG EFFECTS; ENZYMOLOGY; INSTITUTE FOR CANCER RESEARCH MOUSE; METABOLISM; NECROSIS; PANCREAS; PANCREATITIS; PATHOLOGY;

ACUTE DISEASE; ANIMALS; ANTI-INFLAMMATORY AGENTS; ANTIOXIDANTS; CERULETIDE; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CYTOKINES; HEME OXYGENASE-1; INFLAMMATION MEDIATORS; LIPOPOLYSACCHARIDES; LUTEOLIN; MALE; MICE, INBRED ICR; MODELS, BIOLOGICAL; NECROSIS; NF-KAPPA B; PANCREAS; PANCREATITIS; PROTECTIVE AGENTS; PROTOPORPHYRINS;

EID: 85007524374     PISSN: 11073756     EISSN: 1791244X     Source Type: Journal    
DOI: 10.3892/ijmm.2016.2809     Document Type: Article

References (61)

1. Di Fabio F, Abu Hilal M and Johnson CD: Acute pancreatitis: mild, severe or potentially fatal. Pancreatology 11:373-375, 2011.
2. Rebours V: Acute pancreatitis: an overview of the management. Rev Med Interne 35:649-655, 2014 (In French).
3. Talukdar R and Vege SS: Acute pancreatitis. Curr Opin Gastroenterol 31:374-379, 2015.
4. Seelinger G, Merfort I and Schempp CM: Anti-oxidant, anti.inflammatory and anti-allergic activities of luteolin. Planta Med 74:1667-1677, 2008.
5. Kuo MY, Liao MF, Chen FL, Li YC, Yang ML, Lin RH and Kuan YH: Luteolin attenuates the pulmonary inflammatory response involves abilities of antioxidation and inhibition of MAPK and NFκB pathways in mice with endotoxin-induced acute lung injury. Food Chem Toxicol 49:2660-2666, 2011.
6. Nabavi SF, Braidy N, Gortzi O, Sobarzo-Sanchez E, Daglia M, Skalicka-Woiniak K and Nabavi SM: Luteolin as an anti.inflammatory and neuroprotective agent: a brief review. Brain Res Bull 119:1-11, 2015.
7. Sung J and Lee J: Anti-Inflammatory activity of butein and luteolin through suppression of NFκB activation and induction of heme oxygenase-1. J Med Food 18:557-564, 2015.
8. Maines MD: The heme oxygenase system: a regulator of second messenger gases. Annu Rev Pharmacol Toxicol 37:517-554, 1997.
9. Yu M, Wang J, Fang Q, Liu P, Chen S, Zhe N, Lin X, Zhang Y, Zhao J and Zhou Z: High expression of heme oxygenase-1 in target organs may attenuate acute graft-versus-host disease through regulation of immune balance of TH17/Treg. Transpl Immunol 37:10-17, 2016.
10. Wu B, Song HL, Yang Y, Yin ML, Zhang BY, Cao Y, Dong C and Shen ZY: Improvement of liver transplantation outcome by heme oxygenase-1-transduced bone marrow mesenchymal stem cells in rats. Stem Cells Int 2016:9235073, 2016.
11. Nath KA: Heme oxygenase-1 and acute kidney injury. Curr Opin Nephrol Hypertens 23:17-24, 2014.
12. Lever JM, Boddu R, George JF and Agarwal A: Heme oxygenase-1 in kidney health and disease. Antioxid Redox Signal 25:165-183, 2016.
13. Durante W: Targeting heme oxygenase-1 in vascular disease. Curr Drug Targets 11:1504-1516, 2010.
14. Wu ML, Ho YC and Yet SF: A central role of heme oxygenase-1 in cardiovascular protection. Antioxid Redox Signal 15:1835.1846, 2011.
15. Chang M, Xue J, Sharma V and Habtezion A: Protective role of hemeoxygenase-1 in gastrointestinal diseases. Cell Mol Life Sci 72:1161-1173, 2015.
16. Habtezion A, Kwan R, Akhtar E, Wanaski SP, Collins SD, Wong RJ, Stevenson DK, Butcher EC and Omary MB: Panhematin provides a therapeutic benefit in experimental pancreatitis. Gut 60:671-679, 2011.
17. Nakamichi I, Habtezion A, Zhong B, Contag CH, Butcher EC and Omary MB: Hemin-activated macrophages home to the pancreas and protect from acute pancreatitis via heme oxygenase-1 induction. J Clin Invest 115:3007-3014, 2005.
18. Nuhn P, Mitkus T, Ceyhan GO, Kunzli BM, Bergmann F, Fischer L, Giese N, Friess H and Berberat PO: Heme oxygenase 1-generated carbon monoxide and biliverdin attenuate the course of experimental necrotizing pancreatitis. Pancreas 42:265-271, 2013.
19. Habtezion A, Kwan R, Yang AL, Morgan ME, Akhtar E, Wanaski SP, Collins SD, Butcher EC, Kamal A and Omary MB: 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:G12-G20, 2011.
20. Bellezza I, Tucci A, Galli F, Grottelli S, Mierla AL, Pilolli F and Minelli A: Inhibition of NF-κB nuclear translocation via HO-1 activation underlies α-tocopheryl succinate toxicity. J Nutr Biochem 23:1583-1591, 2012.
21. Yeh CH, Chen TP, Wang YC, Lin YM and Lin PJ: HO-1 activation can attenuate cardiomyocytic apoptosis via inhibition of NF-kappaB and AP-1 translocation following cardiac global ischemia and reperfusion. J Surg Res 155:147-156, 2009.
22. Lopez Martin A and Carrillo Alcaraz A: Oxidative stress and acute pancreatitis. Rev Esp Enferm Dig 103:559-562, 2011.
23. Rakonczay Z Jr, Hegyi P, Takacs T, McCarroll J and Saluja AK: The role of NF-kappaB activation in the pathogenesis of acute pancreatitis. Gut 57:259-267, 2008.
24. Peng Y, Gallagher SF, Landmann R, Haines K and Murr MM: The role of p65 NF-kappaB/RelA in pancreatitis-induced Kupffer cell apoptosis. J Gastrointest Surg 10:837-847, 2006.
25. Norkina O, Graf R, Appenzeller P and De Lisle RC: Caerulein. induced acute pancreatitis in mice that constitutively overexpress Reg/PAP genes. BMC Gastroenterol 6:16, 2006.
26. Niederau C, Ferrell LD and Grendell JH: Caerulein-induced acute necrotizing pancreatitis in mice: protective effects of proglumide, benzotript, and secretin. Gastroenterology 88:1192.1204, 1985.
27. Song HJ, Shin CY, Oh TY and Sohn UD: The protective effect of eupatilin on indomethacin-induced cell damage in cultured feline ileal smooth muscle cells: involvement of HO-1 and ERK. J Ethnopharmacol 118:94-101, 2008.
28. Song HJ, Shin CY, Oh TY, Min YS, Park ES and Sohn UD: Eupatilin with heme oxygenase-1-inducing ability protects cultured feline esophageal epithelial cells from cell damage caused by indomethacin. Biol Pharm Bull 32:589-596, 2009.
29. Rongione AJ, Kusske AM, Kwan K, Ashley SW, Reber HA and McFadden DW: Interleukin 10 reduces the severity of acute pancreatitis in rats. Gastroenterology 112:960-967, 1997.
30. Van Laere SJ, Van der Auwera I, Van den Eynden GG, Elst HJ, Weyler J, Harris AL, van Dam P, Van Marck EA, Vermeulen PB and Dirix LY: Nuclear factor-kappaB signature of inflammatory breast cancer by cDNA microarray validated by quantitative real-time reverse transcription-PCR, immunohistochemistry, and nuclear factor-kappaB DNA-binding. Clin Cancer Res 12:3249-3256, 2006.
31. Fujioka K, Kalish F, Wong RJ and Stevenson DK: Inhibition of heme oxygenase activity using a microparticle formulation of zinc protoporphyrin in an acute hemolytic newborn mouse model. Pediatr Res 79:251-257, 2016.
32. Sun GB, Sun X, Wang M, Ye JX, Si JY, Xu HB, Meng XB, Qin M, Sun J, Wang HW, et al: Oxidative stress suppression by luteolin-induced heme oxygenase-1 expression. Toxicol Appl Pharmacol 265:229-240, 2012.
33. Liu HS, Pan CE, Liu QG, Yang W and Liu XM: Effect of NF-kappaB and p38 MAPK in activated monocytes/macrophages on pro-inflammatory cytokines of rats with acute pancreatitis. World J Gastroenterol 9:2513-2518, 2003.
34. Wang X, Wang B and Wu J: Pancreatitis-associated protein-I mRNA expression in mouse pancreas is upregulated by lipopolysaccharide independent of cerulein-pancreatitis. J Gastroenterol Hepatol 16:79-86, 2001.
35. Domitrovi. R, Jakovac H, Tomac J and Sain I: Liver fibrosis in mice induced by carbon tetrachloride and its reversion by luteolin. Toxicol Appl Pharmacol 241:311-321, 2009.
36. Chen CY, Peng WH, Wu LC, Wu CC and Hsu SL: Luteolin ameliorates experimental lung fibrosis both in vivo and in vitro: implications for therapy of lung fibrosis. J Agric Food Chem 58:11653-11661, 2010.
37. Qiao H, Dong L, Zhang X, Zhu C, Zhang X, Wang L, Liu Z, Chen L, Xing Y, Wang C and Li Y: Protective effect of luteolin in experimental ischemic stroke: upregulated SOD1, CAT, Bcl-2 and claudin-5, down-regulated MDA and Bax expression. Neurochem Res 37:2014-2024, 2012.
38. Qiao H, Zhang X, Zhu C, Dong L, Wang L, Zhang X, Xing Y, Wang C, Ji Y and Cao X: Luteolin downregulates TLR4, TLR5, NF-κB and p-p38MAPK expression, upregulates the p-ERK expression, and protects rat brains against focal ischemia. Brain Res 1448:71-81, 2012.
39. Ramudo L and Manso MA: N-acetylcysteine in acute pancreatitis. World J Gastrointest Pharmacol Ther 1:21-26, 2010.
40. Modzelewski B, Janiak A and Hollynski J: Hyperlipoproteinemia in necrotizing pancreatitis. Pol Merkur Lekarski 18:415-417, 2005 (In Polish).
41. Booth DM, Mukherjee R, Sutton R and Criddle DN: Calcium and reactive oxygen species in acute pancreatitis: friend or foe? Antioxid Redox Signal 15:2683-2698, 2011.
42. Hackert T and Werner J: Antioxidant therapy in acute pancreatitis: experimental and clinical evidence. Antioxid Redox Signal 15:2767-2777, 2011.
43. Kim H: Inhibitory mechanism of lycopene on cytokine expression in experimental pancreatitis. Ann NYAcad Sci 1229:99-102, 2011.
44. Ramudo L, De Dios I, Yubero S, Vicente S and Manso MA: ICAM-1 and CD11b/CD18 expression during acute pancreatitis induced by bile-pancreatic duct obstruction: effect of N-acetylcysteine. Exp Biol Med (Maywood) 232:737-743, 2007.
45. Li YY, Li XL, Yang CX, Zhong H, Yao H and Zhu L: Effects of tetrandrine and QYT on ICAM-1 and SOD gene expression in pancreas and liver of rats with acute pancreatitis. World J Gastroenterol 9:155-159, 2003.
46. Fan J, Xu G, Jiang T and Qin Y: Pharmacologic induction of heme oxygenase-1 plays a protective role in diabetic retinopathy in rats. Invest Ophthalmol Vis Sci 53:6541-6556, 2012.
47. Turkseven S, Kruger A, Mingone CJ, Kaminski P, Inaba M, Rodella LF, Ikehara S, Wolin MS and Abraham NG: Antioxidant mechanism of heme oxygenase-1 involves an increase in superoxide dismutase and catalase in experimental diabetes. Am J Physiol Heart Circ Physiol 289:H701-H707, 2005.
48. Kim H, Seo JY and Kim KH: NF-kappaB and cytokines in pancreatic acinar cells. J Korean Med Sci 15(Suppl):S53-S54, 2000.
49. Jin S, Orabi AI, Le T, Javed TA, Sah S, Eisses JF, Bottino R, Molkentin JD and Husain SZ: Exposure to radiocontrast agents induces pancreatic inflammation by activation of nuclear factor-κB, calcium signaling, and calcineurin. Gastroenterology 149:753-764, 2015.
50. Yang X, Jin H, Liu K, Gu Q and Xu X: A novel peptide derived from human pancreatitis-associated protein inhibits inflammation in vivo and in vitro and blocks NF-kappa B signaling pathway. PLoS One 6:e29155, 2011.
51. Constantin M, Choi AJ, Cloonan SM and Ryter SW: Therapeutic potential of heme oxygenase-1/carbon monoxide in lung disease. Int J Hypertens. 2012:8592352012.
52. Barbagallo I, Marrazzo G, Frigiola A, Zappala A and Li Volti G: Role of carbon monoxide in vascular diseases. Curr Pharm Biotechnol. 13:787–796. 2012.
53. MacGarvey NC, Suliman HB, Bartz RR, Fu P, Withers CM, Welty-Wolf KE and Piantadosi CA: Activation of mitochondrial biogenesis by heme oxygenase-1-mediated NF-E2-related factor-2 induction rescues mice from lethal Staphylococcus aureus sepsis. Am J Respir Crit Care Med. 185:851–861. 2012
54. Drechsler Y, Dolganiuc A, Norkina O, Romics L, Li W, Kodys K, Bach FH, Mandrekar P and Szabo G: Heme oxygenase-1 mediates the anti-inflammatory effects of acute alcohol on IL-10 induction involving p38 MAPK activation in monocytes. J Immunol. 177:2592–2600. 2006
55. Vasseur P, Devaure I, Sellier J, Delwail A, Chagneau-Derrode C, Charier F, Tougeron D, Tasu JP, Rabeony H, Lecron JC and Silvain C: High plasma levels of the pro-inflammatory cytokine IL-22 and the anti-inflammatory cytokines IL-10 and IL-1ra in acute pancreatitis. Pancreatology. 14:465–469. 2014
56. Zhang F, Fei J, Zhao B, Chen E and Mao E: Protective effect of adenoviral transfer of heme oxygenase-1 gene on rats with severe acute pancreatitis. Am J Med Sci. 348:224–231. 2014
57. Pandurangan AK, Kumar SA, Dharmalingam P and Ganapasam S: Luteolin, a bioflavonoid inhibits azoxymethane-induced colon carcinogenesis: involvement of iNOS and COX-2. Pharmacogn Mag. 10(Suppl 2): S306–S310. 2014
58. Pandurangan AK, Dharmalingam P, Sadagopan SK and Ganapasam S: Luteolin inhibits matrix metalloproteinase 9 and 2 in azoxymethane-induced colon carcinogenesis. Hum Exp Toxicol. 33:1176–1185. 2014
59. Pandurangan AK, Ananda Sadagopan SK, Dharmalingam P and Ganapasam S: Luteolin, a bioflavonoid inhibits azoxymethane-induced colorectal cancer through activation of Nrf2 signaling. Toxicol Mech Methods. 24:13–20. 2014
60. Huang CS, Lii CK, Lin AH, Yeh YW, Yao HT, Li CC, Wang TS and Chen HW: Protection by chrysin, apigenin, and luteolin against oxidative stress is mediated by the Nrf2-dependent up-regulation of heme oxygenase 1 and glutamate cysteine ligase in rat primary hepatocytes. Arch Toxicol. 87:167–178. 2013
61. Innamorato NG, Rojo AI, García-Yagüe AJ, Yamamoto M, de Ceballos ML and Cuadrado A: The transcription factor Nrf2 is a therapeutic target against brain inflammation. J Immunol. 181:680–689. 2008