Carbon monoxide protects against hepatic ischemia/reperfusion injury by modulating the miR-34a/SIRT1 pathway

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1852, Issue 7, 2015, Pages 1550-1559

  Kim, Hyo Jeong ^a   Joe, Yeonsoo ^a   Yu, Jae Kyoung ^a   Chen, Yingqing ^a   Jeong, Sun Oh ^b   Mani, Nithya ^a   Cho, Gyeong Jae ^c   Pae, Hyun Ock ^b   Ryter, Stefan W ^d   Chung, Hun Taeg ^a  

^a University of Ulsan   (South Korea)

^b Wonkwang University School of Medicine   (South Korea)

^c Gyeongsang National University   (South Korea)

^d NEW YORK PRESBYTERIAN HOSPITAL   (United States)

Author keywords

Carbon monoxide; Liver; MiR 34a; P53; SIRT1

Indexed keywords

CARBON MONOXIDE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 6; MICRORNA; MICRORNA 34A; MYELOPEROXIDASE; PROTEIN P53; SIRTUIN 1; SMALL INTERFERING RNA; SYNAPTOTAGMIN I; TUMOR NECROSIS FACTOR ALPHA; INTERLEUKIN-1BETA; INTERLEUKIN-6; MICRORNAS; MIRN34 MICRORNA, MOUSE; NITRIC OXIDE SYNTHASE TYPE II; SIRT1 PROTEIN, MOUSE; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR-ALPHA; TUMOR SUPPRESSOR PROTEIN P53;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DEACETYLATION; ENZYME ACTIVITY; HEPATIC ISCHEMIA REPERFUSION INJURY; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; LIVER CELL DAMAGE; LIVER FUNCTION; LIVER HISTOLOGY; LIVER INJURY; LIVER ISCHEMIA; LIVER NECROSIS; LIVER PROTECTION; LUCIFERASE ASSAY; MACROPHAGE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPERFUSION INJURY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ANIMALS; ANTAGONISTS AND INHIBITORS; BLOOD SUPPLY; CELL LINE; CELLS, CULTURED; DRUG EFFECTS; GENETICS; LIVER; METABOLISM; MICE; MICE, INBRED C57BL;

MUS;

ANIMALS; CARBON MONOXIDE; CELL LINE; CELLS, CULTURED; INTERLEUKIN-1BETA; INTERLEUKIN-6; LIVER; MALE; MICE; MICE, INBRED C57BL; MICRORNAS; NITRIC OXIDE SYNTHASE TYPE II; REPERFUSION INJURY; SIRTUIN 1; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR-ALPHA; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84928595465     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2015.04.017     Document Type: Article

References (47)

1. Lentsch A.B., Kato A., Yoshidome H., McMasters K.M., Edwards M.J. Inflammatory mechanisms and therapeutic strategies for warm hepatic ischemia/reperfusion injury. Hepatology 2000, 32:169-173.
2. Fondevila C., Busuttil R.W., Kupiec-Weglinski J.W. Hepatic ischemia/reperfusion injury-a fresh look. Exp. Mol. Pathol. 2003, 74:86-93.
3. Jaeschke H. Molecular mechanisms of hepatic ischemia-reperfusion injury and preconditioning. Am. J. Physiol. Gastrointest. Liver Physiol. 2003, 284:G15-G26.
4. Brouard S., Otterbein L.E., Anrather J., Tobiasch E., Bach F.H., Choi A.M., Soares M.P. Carbon monoxide generated by heme oxygenase 1 suppresses endothelial cell apoptosis. J. Exp. Med. 2000, 192:1015-1026.
5. Otterbein L.E., Bach F.H., Alam J., Soares M., Tao Lu H., Wysk M., Davis R.J., Flavell R.A., Choi A.M. Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nat. Med. 2000, 6:422-428.
6. Otterbein L.E., Zuckerbraun B.S., Haga M., Liu F., Song R., Usheva A., Stachulak C., Bodyak N., Smith R.N., Csizmadia E., Tyagi S., Akamatsu Y., Flavell R.J., Billiar T.R., Tzeng E., Bach F.H., Choi A.M., Soares M.P. Carbon monoxide suppresses arteriosclerotic lesions associated with chronic graft rejection and with balloon injury. Nat. Med. 2003, 9:183-190.
7. Nakao A., Kimizuka K., Stolz D.B., Neto J.S., Kaizu T., Choi A.M., Uchiyama T., Zuckerbraun B.S., Nalesnik M.A., Otterbein L.E., Murase N. Carbon monoxide inhalation protects rat intestinal grafts from ischemia/reperfusion injury. Am. J. Pathol. 2003, 163:1587-1598.
8. Kaizu T., Ikeda A., Nakao A., Tsung A., Toyokawa H., Ueki S., Geller D.A., Murase N. Protection of transplant-induced hepatic ischemia/reperfusion injury with carbon monoxide via MEK/ERK1/2 pathway downregulation. Am. J. Physiol. Gastrointest. Liver Physiol. 2008, 294:G236-G244.
9. Song R., Kubo M., Morse D., Zhou Z., Zhang X., Dauber J.H., Fabisiak J., Alber S.M., Watkins S.C., Zuckerbraun B.S., Otterbein L.E., Ning W., Oury T.D., Lee P.J., McCurry K.R., Choi A.M. Carbon monoxide induces cytoprotection in rat orthotopic lung transplantation via anti-inflammatory and anti-apoptotic effects. Am. J. Pathol. 2003, 163:231-242.
10. Fujimoto H., Ohno M., Ayabe S., Kobayashi H., Ishizaka N., Kimura H., Yoshida K., Nagai R. Carbon monoxide protects against cardiac ischemia-reperfusion injury in vivo via MAPK and Akt-eNOS pathways. Arterioscler. Thromb. Vasc. Biol. 2004, 24:1848-1853.
11. Amersi F., Shen X.D., Anselmo D., Melinek J., Iyer S., Southard D.J., Katori M., Volk H.D., Busuttil R.W., Buelow R., Kupiec-Weglinski J.W. Ex vivo exposure to carbon monoxide prevents hepatic ischemia/reperfusion injury through p38 MAP kinase pathway. Hepatology 2002, 35:815-823.
12. Kim H.J., Joe Y., Kong J.S., Jeong S.O., Cho G.J., Ryter S.W., Chung H.T. Carbon monoxide protects against hepatic ischemia/reperfusion injury via ROS-dependent Akt signaling and inhibition of glycogen synthase kinase 3beta. Oxid. Med. Cell. Longev. 2013, 2013:306421.
13. Zhang X., Shan P., Alam J., Davis R.J., Flavell R.A., Lee P.J. Carbon monoxide modulates Fas/Fas ligand, caspases, and Bcl-2 family proteins via the p38alpha mitogen-activated protein kinase pathway during ischemia-reperfusion lung injury. J. Biol. Chem. 2003, 278:22061-22070.
14. Zhang X., Shan P., Otterbein L.E., Alam J., Flavell R.A., Davis R.J., Choi A.M., Lee P.J. Carbon monoxide inhibition of apoptosis during ischemia-reperfusion lung injury is dependent on the p38 mitogen-activated protein kinase pathway and involves caspase 3. J. Biol. Chem. 2003, 278:1248-1258.
15. Kim D., Nguyen M.D., Dobbin M.M., Fischer A., Sananbenesi F., Rodgers J.T., Delalle I., Baur J.A., Sui G., Armour S.M., Puigserver P., Sinclair D.A., Tsai L.H. SIRT1 deacetylase protects against neurodegeneration in models for Alzheimer's disease and amyotrophic lateral sclerosis. EMBO J. 2007, 26:3169-3179.
16. Michan S., Sinclair D. Sirtuins in mammals: insights into their biological function. Biochem. J. 2007, 404:1-13.
17. Morris K.C., Lin H.W., Thompson J.W., Perez-Pinzon M.A. Pathways for ischemic cytoprotection: role of sirtuins in caloric restriction, resveratrol, and ischemic preconditioning. J. Cereb. Blood Flow Metab. 2011, 31:1003-1019.
18. Herranz D., Serrano M. SIRT1: recent lessons from mouse models. Nat. Rev. Cancer 2010, 10:819-823.
19. Pfluger P.T., Herranz D., Velasco-Miguel S., Serrano M., Tschop M.H. Sirt1 protects against high-fat diet-induced metabolic damage. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:9793-9798.
20. Escande C., Chini C.C., Nin V., Dykhouse K.M., Novak C.M., Levine J., van Deursen J., Gores G.J., Chen J., Lou Z., Chini E.N. Deleted in breast cancer-1 regulates SIRT1 activity and contributes to high-fat diet-induced liver steatosis in mice. J. Clin. Invest. 2010, 120:545-558.
21. Schug T.T., Xu Q., Gao H., Peres-da-Silva A., Draper D.W., Fessler M.B., Purushotham A., Li X. Myeloid deletion of SIRT1 induces inflammatory signaling in response to environmental stress. Mol. Cell. Biol. 2010, 30:4712-4721.
22. Purushotham A., Schug T.T., Xu Q., Surapureddi S., Guo X., Li X. Hepatocyte-specific deletion of SIRT1 alters fatty acid metabolism and results in hepatic steatosis and inflammation. Cell Metab. 2009, 9:327-338.
23. Yoshizaki T., Milne J.C., Imamura T., Schenk S., Sonoda N., Babendure J.L., Lu J.C., Smith J.J., Jirousek M.R., Olefsky J.M. SIRT1 exerts anti-inflammatory effects and improves insulin sensitivity in adipocytes. Mol. Cell. Biol. 2009, 29:1363-1374.
24. Hsu C.P., Zhai P., Yamamoto T., Maejima Y., Matsushima S., Hariharan N., Shao D., Takagi H., Oka S., Sadoshima J. Silent information regulator 1 protects the heart from ischemia/reperfusion. Circulation 2010, 122:2170-2182.
25. Hernandez-Jimenez M., Hurtado O., Cuartero M.I., Ballesteros I., Moraga A., Pradillo J.M., McBurney M.W., Lizasoain I., Moro M.A. Silent information regulator 1 protects the brain against cerebral ischemic damage. Stroke 2013, 44:2333-2337.
26. Lee J., Padhye A., Sharma A., Song G., Miao J., Mo Y.Y., Wang L., Kemper J.K. A pathway involving farnesoid X receptor and small heterodimer partner positively regulates hepatic sirtuin 1 levels via microRNA-34a inhibition. J. Biol. Chem. 2010, 285:12604-12611.
27. Yamakuchi M., Ferlito M., Lowenstein C.J. miR-34a repression of SIRT1 regulates apoptosis. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:13421-13426.
28. Castro R.E., Ferreira D.M., Afonso M.B., Borralho P.M., Machado M.V., Cortez-Pinto H., Rodrigues C.M. miR-34a/SIRT1/p53 is suppressed by ursodeoxycholic acid in the rat liver and activated by disease severity in human non-alcoholic fatty liver disease. J. Hepatol. 2013, 58:119-125.
29. Derdak Z., Villegas K.A., Harb R., Wu A.M., Sousa A., Wands J.R. Inhibition of p53 attenuates steatosis and liver injury in a mouse model of non-alcoholic fatty liver disease. J. Hepatol. 2013, 58:785-791.
30. Shen X.D., Ke B., Zhai Y., Amersi F., Gao F., Anselmo D.M., Busuttil R.W., Kupiec-Weglinski J.W. CD154-CD40 T-cell costimulation pathway is required in the mechanism of hepatic ischemia/reperfusion injury, and its blockade facilitates and depends on heme oxygenase-1 mediated cytoprotection. Transplantation 2002, 74:315-319.
31. Tsai C.C., Huang W.C., Chen C.L., Hsieh C.Y., Lin Y.S., Chen S.H., Yang K.C., Lin C.F. Glycogen synthase kinase-3 facilitates con a-induced IFN-gamma- mediated immune hepatic injury. J. Immunol. 2011, 187:3867-3877.
32. Fujita T., Toda K., Karimova A., Yan S.F., Naka Y., Yet S.F., Pinsky D.J. Paradoxical rescue from ischemic lung injury by inhaled carbon monoxide driven by derepression of fibrinolysis. Nat. Med. 2001, 7:598-604.
33. Chang T.C., Wentzel E.A., Kent O.A., Ramachandran K., Mullendore M., Lee K.H., Feldmann G., Yamakuchi M., Ferlito M., Lowenstein C.J., Arking D.E., Beer M.A., Maitra A., Mendell J.T. Transactivation of miR-34a by p53 broadly influences gene expression and promotes apoptosis. Mol. Cell 2007, 26:745-752.
34. Kozakowska M., Ciesla M., Stefanska A., Skrzypek K., Was H., Jazwa A., Grochot-Przeczek A., Kotlinowski J., Szymula A., Bartelik A., Mazan M., Yagensky O., Florczyk U., Lemke K., Zebzda A., Dyduch G., Nowak W., Szade K., Stepniewski J., Majka M., Derlacz R., Loboda A., Dulak J., Jozkowicz A. Heme oxygenase-1 inhibits myoblast differentiation by targeting myomirs. Antioxid. Redox Signal. 2012, 16:113-127.
35. Schafer T., Scheuer C., Roemer K., Menger M.D., Vollmar B. Inhibition of p53 protects liver tissue against endotoxin-induced apoptotic and necrotic cell death. FASEB J. 2003, 17:660-667.
36. Kelly K.J., Plotkin Z., Vulgamott S.L., Dagher P.C. P53 mediates the apoptotic response to GTP depletion after renal ischemia-reperfusion: protective role of a p53 inhibitor. J. Am. Soc. Nephrol. 2003, 14:128-138.
37. Yoshizaki T., Schenk S., Imamura T., Babendure J.L., Sonoda N., Bae E.J., Oh D.Y., Lu M., Milne J.C., Westphal C., Bandyopadhyay G., Olefsky J.M. SIRT1 inhibits inflammatory pathways in macrophages and modulates insulin sensitivity. Am. J. Physiol. Endocrinol. Metab. 2010, 298:E419-E428.
38. Ryter S.W., Alam J., Choi A.M. Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol. Rev. 2006, 86:583-650.
39. Lee L.Y., Kaizu T., Toyokawa H., Zhang M., Ross M., Stolz D.B., Huang C., Gandhi C., Geller D.A., Murase N. Carbon monoxide induces hypothermia tolerance in Kupffer cells and attenuates liver ischemia/reperfusion injury in rats. Liver Transpl. 2011, 17:1457-1466.
40. Kaizu T., Nakao A., Tsung A., Toyokawa H., Sahai R., Geller D.A., Murase N. Carbon monoxide inhalation ameliorates cold ischemia/reperfusion injury after rat liver transplantation. Surgery 2005, 138:229-235.
41. Zuckerbraun B.S., Billiar T.R., Otterbein S.L., Kim P.K., Liu F., Choi A.M., Bach F.H., Otterbein L.E. Carbon monoxide protects against liver failure through nitric oxide-induced heme oxygenase 1. J. Exp. Med. 2003, 198:1707-1716.
42. Vaziri H., Dessain S.K., Ng Eaton E., Imai S.I., Frye R.A., Pandita T.K., Guarente L., Weinberg R.A. hSIR2(SIRT1) functions as an NAD-dependent p53 deacetylase. Cell 2001, 107:149-159.
43. Yeung F., Hoberg J.E., Ramsey C.S., Keller M.D., Jones D.R., Frye R.A., Mayo M.W. Modulation of NF-kappaB-dependent transcription and cell survival by the SIRT1 deacetylase. EMBO J. 2004, 23:2369-2380.
44. Kim D.H., Jung Y.J., Lee J.E., Lee A.S., Kang K.P., Lee S., Park S.K., Han M.K., Lee S.Y., Ramkumar K.M., Sung M.J., Kim W. SIRT1 activation by resveratrol ameliorates cisplatin-induced renal injury through deacetylation of p53. Am. J. Physiol. Ren. Physiol. 2011, 301:F427-F435.
45. Zhang C., Feng Y., Qu S., Wei X., Zhu H., Luo Q., Liu M., Chen G., Xiao X. Resveratrol attenuates doxorubicin-induced cardiomyocyte apoptosis in mice through SIRT1-mediated deacetylation of p53. Cardiovasc. Res. 2011, 90:538-545.
46. Nadtochiy S.M., Redman E., Rahman I., Brookes P.S. Lysine deacetylation in ischaemic preconditioning: the role of SIRT1. Cardiovasc. Res. 2011, 89:643-649.
47. Kume S., Haneda M., Kanasaki K., Sugimoto T., Araki S., Isono M., Isshiki K., Uzu T., Kashiwagi A., Koya D. Silent information regulator 2 (SIRT1) attenuates oxidative stress-induced mesangial cell apoptosis via p53 deacetylation. Free Radic. Biol. Med. 2006, 40:2175-2182.