Canonical notch pathway protects hepatocytes from ischemia/reperfusion injury in mice by repressing reactive oxygen species production through JAK2/STAT3 signaling

Hepatology

Volumn 54, Issue 3, 2011, Pages 979-988

  Yu, Heng Chao ^a,b   Qin, Hong Yan ^a   He, Fei ^a   Wang, Lin ^a,b   Fu, Wei ^a   Liu, Dong ^b   Guo, Feng Cheng ^b   Liang, Liang ^a   Dou, Ke Feng ^b   Han, Hua ^a,b  

^a FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^b FOURTH MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN J RECOMBINATION SIGNAL SEQUENCE BINDING PROTEIN; JANUS KINASE 2; NOTCH RECEPTOR; REACTIVE OXYGEN METABOLITE; STAT3 PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL PROTECTION; CONTROLLED STUDY; DOWN REGULATION; HEPATITIS; IN VITRO STUDY; IN VIVO STUDY; LIVER CELL; LIVER FUNCTION; LIVER INJURY; LIVER ISCHEMIA; LIVER NECROSIS; LIVER PERFUSION; LIVER PROTECTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REPERFUSION INJURY; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; CELLS, CULTURED; CYTOPROTECTION; HEPATOCYTES; JANUS KINASE 2; LIVER; MICE; MICE, INBRED C57BL; REACTIVE OXYGEN SPECIES; RECEPTORS, NOTCH; REPERFUSION INJURY; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; SUPEROXIDE DISMUTASE;

EID: 80052026460     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.24469     Document Type: Article

References (35)

1. Jaeschke H. Molecular mechanisms of hepatic ischemia-reperfusion injury and preconditioning. Am J Physiol Gastrointest Liver Physiol 2003; 284: G15-G26.
2. Balaban RS, Nemoto S, Finkel T. Mitochondria, oxidants, and aging. Cell 2005; 120: 483-495.
3. Murphy MP. How mitochondria produce reactive oxygen species. Biochem J 2009; 417: 1-13.
4. Di Lisa F, Kaludercic N, Carpi A, Menabo R, Giorgio M. Mitochondrial pathways for ROS formation and myocardial injury: the relevance of p66(Shc) and monoamine oxidase. Basic Res Cardiol 2009; 104: 131-139.
5. D'Autreaux B, Toledano MB. ROS as signaling molecules: mechanisms that generate specificity in ROS homeostasis. Nat Rev Mol Cell Biol 2007; 8: 813-824.
6. Zwacka RM, Zhou W, Zhang Y, Darby CJ, Dudus L, Halldorson J, et al. Redox gene therapy for ischemia/reperfusion injury of the liver reduces AP1 and NF-kappaB activation. Nat Med 1998; 4: 698-704.
7. Li C, Jackson RM. Reactive species mechanisms of cellular hypoxia-reoxygenation injury. Am J Physiol Cell Physiol 2002; 282: C227- C241.
8. Lentsch AB, Kato A, Yoshidome H, McMasters KM, Edwards MJ. Inflammatory mechanisms and therapeutic strategies for warm hepatic ischemia/reperfusion injury. HEPATOLOGY 2000; 32: 169-173.
9. King LA, Toledo AH, Rivera-Chavez FA, Toledo-Pereyra LH. Role of p38 and JNK in liver ischemia and reperfusion. J Hepatobiliary Pancreat Surg 2009; 16: 763-770.
10. Mullonkal CJ, Toledo-Pereyra LH. Akt in ischemia and reperfusion. J Invest Surg 2007; 20: 195-203.
11. Wang L, Wang CM, Hou LH, Dou GR, Wang YC, Hu XB, et al. Disruption of the transcription factor recombination signal-binding protein-Jkappa (RBP-J) leads to veno-occlusive disease and interfered liver regeneration in mice. HEPATOLOGY 2009; 49: 268-277.
12. Arumugam TV, Chan SL, Jo DG, Yilmaz G, Tang SC, Cheng A, et al. Gamma secretase-mediated Notch signaling worsens brain damage and functional outcome in ischemic stroke. Nat Med 2006; 12: 621-623.
13. Kopan R, Ilagan MX. The canonical Notch signaling pathway: unfolding the activation mechanism. Cell 2009; 137: 216-233.
14. Gude NA, Emmanuel G, Wu W, Cottage CT, Fischer K, Quijada P, et al. Activation of Notch-mediated protective signaling in the myocardium. Circ Res 2008; 102: 1025-1035.
15. Bheeshmachar G, Purushotaman D, Sade H, Gunasekharan V, Rangarajan A, Sarin A. Evidence for a role for notch signaling in the cytokine-dependent survival of activated T cells. J Immunol 2006; 177: 5041-5050.
16. Han H, Tanigaki K, Yamamoto N, Kuroda K, Yoshimoto M, Nakahata T, et al. Inducible gene knockout of transcription factor recombination signal binding protein-J reveals its essential role in T versus B lineage decision. Int Immunol 2002; 14: 637-645.
17. Kuboki S, Shin T, Huber N, Eismann T, Galloway E, Schuster R, et al. Peroxisome proliferator-activated receptor-gamma protects against hepatic ischemia/reperfusion injury in mice. HEPATOLOGY 2008; 47: 215-224.
18. Malassagne B, Ferret PJ, Hammoud R, Tulliez M, Bedda S, Trebeden H, et al. The superoxide dismutase mimetic MnTBAP prevents Fas-induced acute liver failure in the mouse. Gastroenterology 2001; 121: 1451-1459.
19. Terui K, Enosawa S, Haga S, Zhang HQ, Kuroda H, Kouchi K, et al. Stat3 confers resistance against hypoxia/reoxygenation-induced oxidative injury in hepatocytes through upregulation of Mn-SOD. J Hepatol 2004; 41: 957-965.
20. Kawamata S, Du C, Li K, Lavau C. Overexpression of the Notch target genes Hes in vivo induces lymphoid and myeloid alterations. Oncogene 2002; 21: 3855-3863.
21. Nie Y, Erion DM, Yuan Z, Dietrich M, Shulman GI, Horvath TL, et al. STAT3 inhibition of gluconeogenesis is downregulated by SirT1. Nat Cell Biol 2009; 11: 492-500.
22. Schmitt TM, de Pooter RF, Gronski MA, Cho SK, Ohashi PS, Zuniga-Pflucker JC. Induction of T cell development and establishment of T cell competence from embryonic stem cells differentiated in vitro. Nat Immunol 2004; 5: 410-417.
23. Wang YC, He F, Feng F, Liu XW, Dong GY, Qin HY, et al. Notch signaling determines the M1 versus M2 polarization of macrophages in antitumor immune responses. Cancer Res; 70: 4840-4849.
24. Tsung A, Hoffman RA, Izuishi K, Critchlow ND, Nakao A, Chan MH, et al. Hepatic ischemia/reperfusion injury involves functional TLR4 signaling in nonparenchymal cells. J Immunol 2005; 175: 7661-7668.
25. Miralles C, Busquets X, Santos C, Togores B, Hussain S, Rahman I, et al. Regulation of iNOS expression and glutathione levels in rat liver by oxygen tension. FEBS Lett 2000; 476: 253-257.
26. Hensley K, Robinson KA, Gabbita SP, Salsman S, Floyd RA. Reactive oxygen species, cell signaling, and cell injury. Free Radic Biol Med 2000; 28: 1456-1462.
27. Hohmeier HE, Thigpen A, Tran VV, Davis R, Newgard CB. Stable expression of manganese superoxide dismutase (MnSOD) in insulinoma cells prevents IL-1beta-induced cytotoxicity and reduces nitric oxide production. J Clin Invest 1998; 101: 1811-1820.
28. Nogueira V, Park Y, Chen CC, Xu PZ, Chen ML, Tonic I, et al. Akt determines replicative senescence and oxidative or oncogenic premature senescence and sensitizes cells to oxidative apoptosis. Cancer Cell 2008; 14: 458-470.
29. Jung JE, Kim GS, Narasimhan P, Song YS, Chan PH. Regulation of Mn-superoxide dismutase activity and neuroprotection by STAT3 in mice after cerebral ischemia. J Neurosci 2009; 29: 7003-7014.
30. Kamakura S, Oishi K, Yoshimatsu T, Nakafuku M, Masuyama N, Gotoh Y. Hes binding to STAT3 mediates crosstalk between Notch and JAK-STAT signalling. Nat Cell Biol 2004; 6: 547-554.
31. Valdivia A, Perez-Alvarez S, Aroca-Aguilar JD, Ikuta I, Jordan J. Superoxide dismutases: a physiopharmacological update. J Physiol Biochem 2009; 65: 195-208.
32. O'shea JJ, Murray PJ. Cytokine signaling modules in inflammatory responses. Immunity 2008; 28: 477-487.
33. Freitas MC, Uchida Y, Zhao D, Ke B, Busuttil RW, Kupiec-Weglinski JW. Blockade of Janus kinase-2 signaling ameliorates mouse liver damage due to ischemia and reperfusion. Liver Transpl; 16: 600-610.
34. Boengler K, Hilfiker-Kleiner D, Drexler H, Heusch G, Schulz R. The myocardial JAK/STAT pathway: from protection to failure. Pharmacol Ther 2008; 120: 172-185.
35. Foldi J, Chung AY, Xu H, Zhu J, Outtz HH, Kitajewski J, et al. Autoamplification of Notch signaling in macrophages by TLR-induced and RBP-J-dependent induction of Jagged1. J Immunol; 185: 5023-5031.