MicroRNA-155 aggravates ischemia–reperfusion injury by modulation of inflammatory cell recruitment and the respiratory oxidative burst

Basic Research in Cardiology

Volumn 110, Issue 3, 2015, Pages

  Eisenhardt, Steffen U ^a   Weiss, Jakob B W ^a   Smolka, Christian ^b   Maxeiner, Johanna ^b   Pankratz, Franziska ^b   Bemtgen, Xavier ^b   Kustermann, Max ^b   Thiele, Jan R ^a   Schmidt, Yvonne ^a   Bjoern Stark, G ^a   Moser, Martin ^b   Bode, Christoph ^b   Grundmann, Sebastian ^b  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Inflammation; Ischemia reperfusion injury; microRNA; Myocardial infarction

Indexed keywords

CASPASE 3; ENDOGLIN; INTERLEUKIN 1BETA; MICRORNA 155; REACTIVE OXYGEN METABOLITE; SUPPRESSOR OF CYTOKINE SIGNALING 1; TUMOR NECROSIS FACTOR ALPHA; MICRORNA; MIRN155 MICRORNA, HUMAN; MIRN155 MICRORNA, MOUSE; SOCS1 PROTEIN, HUMAN; SOCS1 PROTEIN, MOUSE; SUPPRESSOR OF CYTOKINE SIGNALING;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL INFILTRATION; CORONARY ARTERY DISSECTION; DOWN REGULATION; GENE TARGETING; HEART INFARCTION; HUMAN; HUMAN CELL; HUMAN TISSUE; INFLAMMATORY CELL; LEUKOCYTE; MACROPHAGE; MALE; MICROSCOPY; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PROTEIN EXPRESSION; REPERFUSION INJURY; RESPIRATORY BURST; RNA ANALYSIS; TISSUE NECROSIS; WILD TYPE; ANIMAL; C57BL MOUSE; ENZYME LINKED IMMUNOSORBENT ASSAY; FLUORESCENT ANTIBODY TECHNIQUE; GENETIC TRANSFECTION; GENETICS; INFLAMMATION; KNOCKOUT MOUSE; METABOLISM; NEUTROPHIL CHEMOTAXIS; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION;

ANIMALS; CHEMOTAXIS, LEUKOCYTE; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; INFLAMMATION; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICRORNAS; REAL-TIME POLYMERASE CHAIN REACTION; REPERFUSION INJURY; RESPIRATORY BURST; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION; TRANSFECTION;

EID: 84928804165     PISSN: 03008428     EISSN: 14351803     Source Type: Journal    
DOI: 10.1007/s00395-015-0490-9     Document Type: Article

References (58)

1. Ambros V (2004) The functions of animal microRNAs. Nature 431:350–355. doi:10.1038/nature02871
2. Ayhan S, Tugay C, Norton S, Araneo B, Siemionow M (2003) Dehydroepiandrosterone protects the microcirculation of muscle flaps from ischemia-reperfusion injury by reducing the expression of adhesion molecules. Plast Reconstr Surg 111:2286–2294. doi:10.1097/01.PRS.0000060242.85268.8F
3. Baars T, Skyschally A, Klein-Hitpass L, Cario E, Erbel R, Heusch G, Kleinbongard P (2014) microRNA expression and its potential role in cardioprotection by ischemic postconditioning in pigs. Pflugers Arch 466:1953–1961. doi:10.1007/s00424-013-1429-3
4. Baez S (1973) An open cremaster muscle preparation for the study of blood vessels by in vivo microscopy. Microvasc Res 5:384–394
5. Ceppi M, Pereira PM, Dunand-Sauthier I, Barras E, Reith W, Santos MA, Pierre P (2009) MicroRNA-155 modulates the interleukin-1 signaling pathway in activated human monocyte-derived dendritic cells. Proc Natl Acad Sci U S A 106:2735–2740. doi:10.1073/pnas.0811073106
6. Du F, Yu F, Wang Y, Hui Y, Carnevale K, Fu M, Lu H, Fan D (2014) MicroRNA-155 deficiency results in decreased macrophage inflammation and attenuated atherogenesis in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol 34:759–767. doi:10.1161/ATVBAHA.113.302701
7. Eisenhardt SU, Schmidt Y, Karaxha G, Iblher N, Penna V, Torio-Padron N, Stark GB, Bannasch H (2012) Monitoring molecular changes induced by ischemia/reperfusion in human free muscle flap tissue samples. Ann Plast Surg 68:202–208. doi:10.1097/SAP.0b013e3181f77ba5
8. Eisenhardt SU, Schmidt Y, Thiele JR, Iblher N, Penna V, Torio-Padron N, Stark GB, Bannasch H (2012) Negative pressure wound therapy reduces the ischaemia/reperfusion-associated inflammatory response in free muscle flaps. J Plast Reconstr Aesthet Surg 65:640–649. doi:10.1016/j.bjps.2011.11.037
9. Faraoni I, Antonetti FR, Cardone J, Bonmassar E (2009) miR-155 gene: a typical multifunctional microRNA. Biochim Biophys Acta 1792:497–505. doi:10.1016/j.bbadis.2009.02.013
10. Farhood A, McGuire GM, Manning AM, Miyasaka M, Smith CW, Jaeschke H (1995) Intercellular adhesion molecule 1 (ICAM-1) expression and its role in neutrophil-induced ischemia-reperfusion injury in rat liver. J Leukoc Biol 57:368–374
11. Frantz S, Hofmann U, Fraccarollo D, Schafer A, Kranepuhl S, Hagedorn I, Nieswandt B, Nahrendorf M, Wagner H, Bayer B, Pachel C, Schon MP, Kneitz S, Bobinger T, Weidemann F, Ertl G, Bauersachs J (2013) Monocytes/macrophages prevent healing defects and left ventricular thrombus formation after myocardial infarction. FASEB J 27:871–881. doi:10.1096/fj.12-214049
12. Grundmann S, Hans FP, Kinniry S, Heinke J, Helbing T, Bluhm F, Sluijter JP, Hoefer I, Pasterkamp G, Bode C, Moser M (2011) MicroRNA-100 regulates neovascularization by suppression of mammalian target of rapamycin in endothelial and vascular smooth muscle cells. Circulation 123:999–1009. doi:10.1161/CIRCULATIONAHA.110.000323
13. Grundmann S, Hoefer I, Ulusans S, van Royen N, Schirmer SH, Ozaki CK, Bode C, Piek JJ, Buschmann I (2005) Anti-tumor necrosis factor-{alpha} therapies attenuate adaptive arteriogenesis in the rabbit. Am J Physiol Heart Circ Physiol 289:H1497–1505. doi:10.1152/ajpheart.00959.2004
14. Harris TA, Yamakuchi M, Ferlito M, Mendell JT, Lowenstein CJ (2008) MicroRNA-126 regulates endothelial expression of vascular cell adhesion molecule 1. Proc Natl Acad Sci USA 105:1516–1521. doi:10.1073/pnas.0707493105
15. Hausenloy DJ, Baxter G, Bell R, Botker HE, Davidson SM, Downey J, Heusch G, Kitakaze M, Lecour S, Mentzer R, Mocanu MM, Ovize M, Schulz R, Shannon R, Walker M, Walkinshaw G, Yellon DM (2010) Translating novel strategies for cardioprotection: the Hatter workshop recommendations. Basic Res Cardiol 105:677–686
16. He B, Xiao J, Ren AJ, Zhang YF, Zhang H, Chen M, Xie B, Gao XG, Wang YW (2011) Role of miR-1 and miR-133a in myocardial ischemic postconditioning. J Biomed Sci 18:22. doi:10.1186/1423-0127-18-22
17. Heusch G, Libby P, Gersh B, Yellon D, Bohm M, Lopaschuk G, Opie L (2014) Cardiovascular remodelling in coronary artery disease and heart failure. Lancet 383:1933–1943
18. Heymans S, Corsten MF, Verhesen W, Carai P, van Leeuwen RE, Custers K, Peters T, Hazebroek M, Stoger L, Wijnands E, Janssen BJ, Creemers EE, Pinto YM, Grimm D, Schurmann N, Vigorito E, Thum T, Stassen F, Yin X, Mayr M, de Windt LJ, Lutgens E, Wouters K, de Winther MP, Zacchigna S, Giacca M, van Bilsen M, Papageorgiou AP, Schroen B (2013) Macrophage microRNA-155 promotes cardiac hypertrophy and failure. Circulation 128:1420–1432. doi:10.1161/CIRCULATIONAHA.112.001357
19. Hsieh CH, Jeng JC, Jeng SF, Wu CJ, Lu TH, Liliang PC, Rau CS, Chen YC, Lin CJ (2010) MicroRNA profiling in ischemic injury of the gracilis muscle in rats. BMC Musculoskelet Disord 11:123. doi:10.1186/1471-2474-11-123
20. Johns DG, Ao Z, Eybye M, Olzinski A, Costell M, Gruver S, Smith SA, Douglas SA, Macphee CH (2005) Rosiglitazone protects against ischemia/reperfusion-induced leukocyte adhesion in the zucker diabetic fatty rat. J Pharmacol Exp Ther 315:1020–1027
21. Junker A, Krumbholz M, Eisele S, Mohan H, Augstein F, Bittner R, Lassmann H, Wekerle H, Hohlfeld R, Meinl E (2009) MicroRNA profiling of multiple sclerosis lesions identifies modulators of the regulatory protein CD47. Brain 132:3342–3352. doi:10.1093/brain/awp300
22. Kalyanaraman B, Darley-Usmar V, Davies KJ, Dennery PA, Forman HJ, Grisham MB, Mann GE, Moore K, Roberts LJ 2nd, Ischiropoulos H (2012) Measuring reactive oxygen and nitrogen species with fluorescent probes: challenges and limitations. Free Radic Biol Med 52:1–6. doi:10.1016/j.freeradbiomed.2011.09.030
23. Kishore R, Verma SK, Mackie AR, Vaughan EE, Abramova TV, Aiko I, Krishnamurthy P (2013) Bone marrow progenitor cell therapy-mediated paracrine regulation of cardiac miRNA-155 modulates fibrotic response in diabetic hearts. PLoS One 8:e60161. doi:10.1371/journal.pone.0060161
24. Lehr HA, Guhlmann A, Nolte D, Keppler D, Messmer K (1991) Leukotrienes as mediators in ischemia-reperfusion injury in a microcirculation model in the hamster. J Clin Invest 87:2036–2041
25. Li X, Tian F, Wang F (2013) Rheumatoid arthritis-associated microRNA-155 targets SOCS1 and upregulates TNF-alpha and IL-1beta in PBMCs. Int J Mol Sci 14:23910–23921. doi:10.3390/ijms141223910
26. Liu J, van Mil A, Aguor EN, Siddiqi S, Vrijsen K, Jaksani S, Metz C, Zhao J, Strijkers GJ, Doevendans PA, Sluijter JP (2012) MiR-155 inhibits cell migration of human cardiomyocyte progenitor cells (hCMPCs) via targeting of MMP-16. J Cell Mol Med 16:2379–2386. doi:10.1111/j.1582-4934.2012.01551.x
27. Luo X, Cai H, Ni J, Bhindi R, Lowe HC, Chesterman CN, Khachigian LM (2009) c-Jun DNAzymes inhibit myocardial inflammation, ROS generation, infarct size, and improve cardiac function after ischemia-reperfusion injury. Arterioscler Thromb Vasc Biol 29:1836–1842. doi:10.1161/ATVBAHA.109.189753
28. Martin MM, Buckenberger JA, Jiang J, Malana GE, Nuovo GJ, Chotani M, Feldman DS, Schmittgen TD, Elton TS (2007) The human angiotensin II type 1 receptor +1166 A/C polymorphism attenuates microRNA-155 binding. J Biol Chem 282:24262–24269. doi:10.1074/jbc.M701050200
29. Matsumoto S, Sakata Y, Nakatani D, Suna S, Mizuno H, Shimizu M, Usami M, Sasaki T, Sato H, Kawahara Y, Hamasaki T, Nanto S, Hori M, Komuro I (2012) A subset of circulating microRNAs are predictive for cardiac death after discharge for acute myocardial infarction. Biochem Biophys Res Commun 427:280–284. doi:10.1016/j.bbrc.2012.09.039
30. Nahrendorf M, Swirski FK, Aikawa E, Stangenberg L, Wurdinger T, Figueiredo JL, Libby P, Weissleder R, Pittet MJ (2007) The healing myocardium sequentially mobilizes two monocyte subsets with divergent and complementary functions. J Exp Med 204:3037–3047. doi:10.1084/jem.20070885
31. Nazari-Jahantigh M, Wei Y, Noels H, Akhtar S, Zhou Z, Koenen RR, Heyll K, Gremse F, Kiessling F, Grommes J, Weber C, Schober A (2012) MicroRNA-155 promotes atherosclerosis by repressing Bcl6 in macrophages. J Clin Invest 122:4190–4202. doi:10.1172/JCI61716
32. O’Connell RM, Rao DS, Chaudhuri AA, Boldin MP, Taganov KD, Nicoll J, Paquette RL, Baltimore D (2008) Sustained expression of microRNA-155 in hematopoietic stem cells causes a myeloproliferative disorder. J Exp Med 205:585–594. doi:10.1084/jem.20072108
33. O’Connell RM, Taganov KD, Boldin MP, Cheng G, Baltimore D (2007) MicroRNA-155 is induced during the macrophage inflammatory response. Proc Natl Acad Sci U S A 104:1604–1609. doi:10.1073/pnas.0610731104
34. Oyama J, Blais C Jr, Liu X, Pu M, Kobzik L, Kelly RA, Bourcier T (2004) Reduced myocardial ischemia-reperfusion injury in toll-like receptor 4-deficient mice. Circulation 109:784–789. doi:10.1161/01.CIR.0000112575.66565.84
35. Rao R, Rieder SA, Nagarkatti P, Nagarkatti M (2014) Staphylococcal enterotoxin B-induced microRNA-155 targets SOCS1 to promote acute inflammatory lung injury. Infect Immun 82:2971–2979. doi:10.1128/IAI.01666-14
36. Rashid MA, William-Olsson G (1991) Are leukocytosis and lipid peroxidation involved in ischemic or reperfusion injury in cardiac surgery? Thorac Cardiovasc Surg 39:193–195
37. Rodriguez A, Vigorito E, Clare S, Warren MV, Couttet P, Soond DR, van Dongen S, Grocock RJ, Das PP, Miska EA, Vetrie D, Okkenhaug K, Enright AJ, Dougan G, Turner M, Bradley A (2007) Requirement of bic/microRNA-155 for normal immune function. Science 316:608–611. doi:10.1126/science.1139253
38. Roy S, Khanna S, Hussain SR, Biswas S, Azad A, Rink C, Gnyawali S, Shilo S, Nuovo GJ, Sen CK (2009) MicroRNA expression in response to murine myocardial infarction: miR-21 regulates fibroblast metalloprotease-2 via phosphatase and tensin homologue. Cardiovasc Res 82:21–29. doi:10.1093/cvr/cvp015
39. Seddiki N, Brezar V, Ruffin N, Levy Y, Swaminathan S (2014) Role of miR-155 in the regulation of lymphocyte immune function and disease. Immunology 142:32–38. doi:10.1111/imm.12227
40. Seok HY, Chen J, Kataoka M, Huang ZP, Ding J, Yan J, Hu X, Wang DZ (2014) Loss of MicroRNA-155 protects the heart from pathological cardiac hypertrophy. Circ Res 114:1585–1595. doi:10.1161/CIRCRESAHA.114.303784
41. Silvestre JS, Mallat Z, Tedgui A, Levy BI (2008) Post-ischaemic neovascularization and inflammation. Cardiovasc Res 78:242–249. doi:10.1093/cvr/cvn027
42. Sluijter JP, Smeets MB, Velema E, Pasterkamp G, de Kleijn DP (2004) Increased collagen turnover is only partly associated with collagen fiber deposition in the arterial response to injury. Cardiovasc Res 61:186–195. doi:10.1016/j.cardiores.2003.09.028
43. Stanczyk J, Pedrioli DM, Brentano F, Sanchez-Pernaute O, Kolling C, Gay RE, Detmar M, Gay S, Kyburz D (2008) Altered expression of MicroRNA in synovial fibroblasts and synovial tissue in rheumatoid arthritis. Arthritis Rheum 58:1001–1009. doi:10.1002/art.23386
44. Suzuki K, Murtuza B, Smolenski RT, Sammut IA, Suzuki N, Kaneda Y, Yacoub MH (2001) Overexpression of interleukin-1 receptor antagonist provides cardioprotection against ischemia-reperfusion injury associated with reduction in apoptosis. Circulation 104:I303–I308. doi:10.1161/hc37t1.094871
45. Thiele JR, Goerendt K, Stark GB, Eisenhardt SU (2012) Real-time digital imaging of leukocyte-endothelial interaction in ischemia-reperfusion injury (IRI) of the rat cremaster muscle. J Vis Exp (66):e3973. doi:10.3791/3973
46. Thiele JR, Habersberger J, Braig D, Schmidt Y, Goerendt K, Maurer V, Bannasch H, Scheichl A, Woollard KJ, von Dobschutz E, Kolodgie F, Virmani R, Stark GB, Peter K, Eisenhardt SU (2014) Dissociation of pentameric to monomeric C-reactive protein localizes and aggravates inflammation: in vivo proof of a powerful proinflammatory mechanism and a new anti-inflammatory strategy. Circulation 130:35–50. doi:10.1161/CIRCULATIONAHA.113.007124
47. Tili E, Michaille JJ, Cimino A, Costinean S, Dumitru CD, Adair B, Fabbri M, Alder H, Liu CG, Calin GA, Croce CM (2007) Modulation of miR-155 and miR-125b levels following lipopolysaccharide/TNF-alpha stimulation and their possible roles in regulating the response to endotoxin shock. J Immunol 179:5082–5089
48. Urbich C, Kuehbacher A, Dimmeler S (2008) Role of microRNAs in vascular diseases, inflammation, and angiogenesis. Cardiovasc Res 79:581–588. doi:10.1093/cvr/cvn156
49. van Rooij E, Sutherland LB, Thatcher JE, DiMaio JM, Naseem RH, Marshall WS, Hill JA, Olson EN (2008) Dysregulation of microRNAs after myocardial infarction reveals a role of miR-29 in cardiac fibrosis. Proc Natl Acad Sci U S A 105:13027–13032. doi:10.1073/pnas.0805038105
50. Vigorito E, Perks KL, Abreu-Goodger C, Bunting S, Xiang Z, Kohlhaas S, Das PP, Miska EA, Rodriguez A, Bradley A, Smith KG, Rada C, Enright AJ, Toellner KM, Maclennan IC, Turner M (2007) microRNA-155 regulates the generation of immunoglobulin class-switched plasma cells. Immunity 27:847–859. doi:10.1016/j.immuni.2007.10.009
51. Vollmar B, Menger MD, Glasz J, Leiderer R, Messmer K (1994) Impact of leukocyte-endothelial cell interaction in hepatic ischemia-reperfusion injury. Am J Physiol 267:G786–793
52. Wang J, Yu F, Jia X, Iwanowycz S, Wang Y, Huang S, Ai W, Fan D (2015) MicroRNA-155 deficiency enhances the recruitment and functions of myeloid-derived suppressor cells in tumor microenvironment and promotes solid tumor growth. Int J Cancer 136:E602–613. doi:10.1002/ijc.29151
53. Wang X, Zhang X, Ren XP, Chen J, Liu H, Yang J, Medvedovic M, Hu Z, Fan GC (2010) MicroRNA-494 targeting both proapoptotic and antiapoptotic proteins protects against ischemia/reperfusion-induced cardiac injury. Circulation 122:1308–1318. doi:10.1161/CIRCULATIONAHA.110.964684
54. Xie W, Li P, Wang Z, Chen J, Lin Z, Liang X, Mo Y (2014) Rosuvastatin May Reduce the Incidence of Cardiovascular Events in Patients with Acute Coronary Syndromes Receiving Percutaneous Coronary Intervention by Suppressing miR-155/SHIP-1 Signaling Pathway. Cardiovasc Ther 32:276–282. doi:10.1111/1755-5922.12098
55. Yellon DM, Hausenloy DJ (2007) Myocardial reperfusion injury. N Engl J Med 357:1121–1135. doi:10.1056/NEJMra071667
56. Ysebaert DK, De Greef KE, Vercauteren SR, Ghielli M, Verpooten GA, Eyskens EJ, De Broe ME (2000) Identification and kinetics of leukocytes after severe ischaemia/reperfusion renal injury. Nephrol Dial Transplant 15:1562–1574
57. Zhao XD, Zhang W, Liang HJ, Ji WY (2013) Overexpression of miR -155 promotes proliferation and invasion of human laryngeal squamous cell carcinoma via targeting SOCS1 and STAT3. PLoS One 8:e56395. doi:10.1371/journal.pone.0056395
58. Zimmerman BJ, Granger DN (1994) Mechanisms of reperfusion injury. Am J Med Sci 307:284–292