Mitochondrially targeted Endonuclease III has a powerful anti-infarct effect in an in vivo rat model of myocardial ischemia/reperfusion

Basic Research in Cardiology

Volumn 110, Issue 2, 2015, Pages

  Yang, Xi Ming ^a   Cui, Lin ^a   White, James ^a   Kuck, Jamie ^a   Ruchko, Mykhaylo V ^a   Wilson, Glenn L ^a   Alexeyev, Mikhail ^a   Gillespie, Mark N ^a   Downey, James M ^a   Cohen, Michael V ^a  

^a UNIVERSITY OF SOUTH ALABAMA COLLEGE OF MEDICINE   (United States)

Author keywords

Cardioprotection; DNase; EndoIII; Mitochondria; Myocardial infarction

Indexed keywords

ADENOSINE RECEPTOR; CANGRELOR; CARDIOVASCULAR AGENT; DEOXYRIBONUCLEASE I; ENDONUCLEASE 3; HYBRID PROTEIN; MITOCHONDRIAL DNA; PHOSPHATIDYLINOSITOL 3 KINASE; UNCLASSIFIED DRUG; ADENOSINE PHOSPHATE; DEOXYRIBONUCLEASE; NTH1 PROTEIN, RAT; PURINERGIC P2Y RECEPTOR ANTAGONIST;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORONARY ARTERY OCCLUSION; DRUG EFFECT; DRUG POTENCY; DRUG POTENTIATION; DRUG TARGETING; ENZYME INHIBITION; HEART HEMODYNAMICS; HEART INFARCTION SIZE; HEART MITOCHONDRION; HEART MUSCLE CELL; HEART MUSCLE ISCHEMIA; HEART MUSCLE NECROSIS; HEART PROTECTION; IN VIVO STUDY; MALE; MONOTHERAPY; NONHUMAN; RAT; RAT MODEL; REPERFUSION INJURY; ANALOGS AND DERIVATIVES; ANIMAL; DISEASE MODEL; DRUG EFFECTS; HEART INFARCTION; HEMODYNAMICS; MITOCHONDRION; MYOCARDIAL REPERFUSION INJURY; PATHOPHYSIOLOGY; SPRAGUE DAWLEY RAT;

ADENOSINE MONOPHOSPHATE; ANIMALS; DEOXYRIBONUCLEASE I; DISEASE MODELS, ANIMAL; ENDODEOXYRIBONUCLEASES; HEMODYNAMICS; MALE; MITOCHONDRIA; MYOCARDIAL INFARCTION; MYOCARDIAL REPERFUSION INJURY; PURINERGIC P2Y RECEPTOR ANTAGONISTS; RATS; RATS, SPRAGUE-DAWLEY; RECOMBINANT FUSION PROTEINS;

EID: 84928264573     PISSN: 03008428     EISSN: 14351803     Source Type: Journal    
DOI: 10.1007/s00395-014-0459-0     Document Type: Article

References (43)

1. Bliksøen M, Mariero LH, Ohm IK, Haugen F, Yndestad A, Solheim S, Seljeflot I, Ranheim T, Andersen GØ, Aukrust P, Valen G, Vinge LE (2012) Increased circulating mitochondrial DNA after myocardial infarction. Int J Cardiol 158:132–134. doi:10.1016/j.ijcard.2012.04.047
2. Boiteux S, Guillet M (2004) Abasic sites in DNA: repair and biological consequences in Saccharomyces cerevisiae. DNA Repair 3:1–12. doi:10.1016/j.dnarep.2003.10.002
3. Burney S, Caulfield JL, Niles JC, Wishnok JS, Tannenbaum SR (1999) The chemistry of DNA damage from nitric oxide and peroxynitrite. Mutat Res 424:37–49. doi:10.1016/S0027-5107(99)00006-8
4. Chatterjee A, Mambo E, Zhang Y, DeWeese T, Sidransky D (2006) Targeting of mutant hogg1 in mammalian mitochondria and nucleus: effect on cellular survival upon oxidative stress. BMC Cancer 6:235. doi:10.1186/1471-2407-6-235
5. Chouteau JM, Obiako B, Gorodnya OM, Pastukh VM, Ruchko MV, Wright AJ, Wilson GL, Gillespie MN (2011) Mitochondrial DNA integrity may be a determinant of endothelial barrier properties in oxidant-challenged rat lungs. Am J Physiol 301:L892–L898. doi:10.1152/ajplung.00210.2011
6. Cuzzocrea S, Riley DP, Caputi AP, Salvemini D (2001) Antioxidant therapy: a new pharmacological approach in shock, inflammation, and ischemia/reperfusion injury. Pharmacol Rev 53:135–159
7. Dobson AW, Grishko V, LeDoux SP, Kelley MR, Wilson GL, Gillespie MN (2002) Enhanced mtDNA repair capacity protects pulmonary artery endothelial cells from oxidant-mediated death. Am J Physiol 283:L205–L210. doi:10.1152/ajplung.00443.2001
8. Dobson AW, Xu Y, Kelley MR, LeDoux SP, Wilson GL (2000) Enhanced mitochondrial DNA repair and cellular survival after oxidative stress by targeting the human 8-oxoguanine glycosylase repair enzyme to mitochondria. J Biol Chem 275:37518–37523. doi:10.1074/jbc.M000831200
9. Fernández-Ruiz I, Arnalich F, Cubillos-Zapata C, Hernández-Jiménez E, Moreno-González R, Toledano V, Fernández-Velasco M, Vallejo-Cremades MT, Esteban-Burgos L, Pérez de Diego R, Llamas-Matias MA, García-Arumi E, Marti R, Boscá L, Andreu AL, López-Sendón JL, López-Collazo E (2014) Mitochondrial DAMPs induce endotoxin tolerance in human monocytes: an observation in patients with myocardial infarction. PLoS One 9:e95073. doi:10.1371/journal.pone.0095073
10. García N, Chávez E (2007) Mitochondrial DNA fragments released through the permeability transition pore correspond to specific gene size. Life Sci 81:1160–1166. doi:10.1016/j.lfs.2007.08.019
11. Grishko V, Solomon M, Wilson GL, LeDoux SP, Gillespie MN (2001) Oxygen radical-induced mitochondrial DNA damage and repair in pulmonary vascular endothelial cell phenotypes. Am J Physiol 280:L1300–L1308
12. Halestrap AP, Clarke SJ, Javadov SA (2004) Mitochondrial permeability transition pore opening during myocardial reperfusion–a target for cardioprotection. Cardiovasc Res 61:372–385. doi:10.1016/S0008-6363(03)00533-9
13. Hashizume M, Mouner M, Chouteau JM, Gorodnya OM, Ruchko MV, Potter BJ, Wilson GL, Gillespie MN, Parker JC (2013) Mitochondrial-targeted DNA repair enzyme 8-oxoguanine DNA glycosylase 1 protects against ventilator-induced lung injury in intact mice. Am J Physiol 304:L287–L297. doi:10.1152/ajplung.00071.2012
14. Hashizume M, Mouner M, Chouteau JM, Gorodnya OM, Ruchko MV, Wilson GL, Gillespie MN, Parker JC (2014) Mitochondrial targeted endonuclease III DNA repair enzyme protects against ventilator induced lung injury in mice. Pharmaceuticals 7:894–912. doi:10.3390/ph7080894
15. Hausenloy DJ, Yellon DM (2003) The mitochondrial permeability transition pore: its fundamental role in mediating cell death during ischaemia and reperfusion. J Mol Cell Cardiol 35:339–341. doi:10.1016/S0022-2828(03)00043-9
16. Heusch G (2013) Cardioprotection: chances and challenges of its translation to the clinic. Lancet 381:166–175. doi:10.1016/S0140-6736(12)60916-7
17. Ho SN, Hunt HD, Horton RM, Pullen JK, Pease LR (1989) Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77:51–59. doi:10.1016/0378-1119(89)90358-2
18. Ibrahim M, Strah H, Scozzi D, Huang HJ, Kreisel D, Krupnick A, Puyo C, Hachem RR, Alouch A, Trulock E, Gelman A (2014) Circulating mitochondrial DNA is elevated in lung transplant recipient patients with immediate early primary graft dysfunction. Am J Respir Crit Care Med 189:A1605
19. Kloner RA (2013) Current state of clinical translation of cardioprotective agents for acute myocardial infarction. Circ Res 113:451–463. doi:10.1161/CIRCRESAHA.112.300627
20. Koczor CA, Shokolenko IN, Boyd AK, Balk SP, Wilson GL, LeDoux SP (2009) Mitochondrial DNA damage initiates a cell cycle arrest by a Chk2-associated mechanism in mammalian cells. J Biol Chem 284:36191–36201. doi:10.1074/jbc.M109.036020
21. Konstantinidis K, Kitsis RN (2012) Cardiovascular biology: escaped DNA inflames the heart. Nature 485:179–180. doi:10.1038/485179a
22. Miki T, Liu GS, Cohen MV, Downey JM (1998) Mild hypothermia reduces infarct size in the beating rabbit heart: a practical intervention for acute myocardial infarction? Basic Res Cardiol 93:372–383. doi:10.1007/s003950050105
23. + exchange inhibitor, Hoe 642: difference from preconditioning in the role of protein kinase C. J Am Coll Cardiol 29:693–701. doi:10.1016/S0735-1097(96)00522-0
24. Oka T, Hikoso S, Yamaguchi O, Taneike M, Takeda T, Tamai T, Oyabu J, Murakawa T, Nakayama H, Nishida K, Akira S, Yamamoto A, Komuro I, Otsu K (2012) Mitochondrial DNA that escapes from autophagy causes inflammation and heart failure. Nature 485:251–255. doi:10.1038/nature10992
25. Otsuka H, Bhushan S, King AL, Polhemus D, Wilson GL, Lefer DJ (2013) Mitochondrial targeted DNA repair enzyme 8-oxoguanene DNA glycosylase 1 (OGG1) attenuates myocardial infarct size. Circulation 128:A14115
26. Otsuka H, Bhushan S, King AL, Polhemus D, Wilson GL, Lefer DJ (2013) Mitochondrial targeted DNA repair enzyme, Endonuclease III (ENDO III), attenuates myocardial ischemia/reperfusion injury. Circulation 128:A14149
27. Panduri V, Liu G, Surapureddi S, Kondapalli J, Soberanes S, de Souza-Pinto NC, Bohr VA, Budinger GRS, Schumacker PT, Weitzman SA, Kamp DW (2009) Role of mitochondrial hOGG1 and aconitase in oxidant-induced lung epithelial cell apoptosis. Free Rad Biol Med 47:750–759. doi:10.1016/j.freeradbiomed.2009.06.010
28. Pinz KG, Bogenhagen DF (2000) Characterization of a catalytically slow AP lyase activity in DNA polymerase γ and other family A DNA polymerases. J Biol Chem 275:12509–12514. doi:10.1074/jbc.275.17.12509
29. Rachek LI, Grishko VI, Alexeyev MF, Pastukh VV, LeDoux SP, Wilson GL (2004) Endonuclease III and endonuclease VIII conditionally targeted into mitochondria enhance mitochondrial DNA repair and cell survival following oxidative stress. Nucleic Acids Res 32:3240–3247. doi:10.1093/nar/gkh648
30. Rachek LI, Grishko VI, LeDoux SP, Wilson GL (2006) Role of nitric oxide-induced mtDNA damage in mitochondrial dysfunction and apoptosis. Free Rad Biol Med 40:754–762. doi:10.1016/j.freeradbiomed.2005.09.028
31. Rachek LI, Grishko VI, Musiyenko SI, Kelley MR, LeDoux SP, Wilson GL (2002) Conditional targeting of the DNA repair enzyme hOGG1 into mitochondria. J Biol Chem 277:44932–44937. doi:10.1074/jbc.M208770200
32. Ricci C, Pastukh V, Leonard J, Turrens J, Wilson G, Schaffer D, Schaffer SW (2008) Mitochondrial DNA damage triggers mitochondrial-superoxide generation and apoptosis. Am J Physiol 294:C413–C422. doi:10.1152/ajpcell.00362.2007
33. Roubille F, Lairez O, Mewton N, Rioufol G, Ranc S, Sanchez I, Cung TT, Elbaz M, Piot C, Ovize M (2012) Cardioprotection by clopidogrel in acute ST-elevated myocardial infarction patients: a retrospective analysis. Basic Res Cardiol 107:275. doi:10.1007/s00395-012-0275-3
34. Ruchko M, Gorodnya O, LeDoux SP, Alexeyev MF, Al-Mehdi A-B, Gillespie MN (2005) Mitochondrial DNA damage triggers mitochondrial dysfunction and apoptosis in oxidant-challenged lung endothelial cells. Am J Physiol 288:L530–L535. doi:10.1152/ajplung.00255.2004
35. Savchenko AS, Borissoff JI, Martinod K, De Meyer SF, Gallant M, Erpenbeck L, Brill A, Wang Y, Wagner DD (2014) VWF-mediated leukocyte recruitment with chromatin decondensation by PAD4 increases myocardial ischemia/reperfusion injury in mice. Blood 123:141–148. doi:10.1182/blood-2013-07-514992
36. Simmons JD, Lee Y-L, Mulekar S, Kuck JL, Brevard SB, Gonzalez RP, Gillespie MN, Richards WO (2013) Elevated levels of plasma mitochondrial DNA DAMPs are linked to clinical outcome in severely injured human subjects. Ann Surg 258:591–596. doi:10.1097/SLA.0b013e3182a4ea46
37. Stenslokken KO, Bilksoen M, Mariero L, Ytrehus K, Baysa A, Vaage JI, Valen G (2014) Extracellular mitochondrial DNA induces cell death in cardiomyocytes. Cardiovasc Res 103(Suppl 1):S122. doi:10.1093/cvr/cvu098.93
38. Tissier R, Hamanaka K, Kuno A, Parker JC, Cohen MV, Downey JM (2007) Total liquid ventilation provides ultra-fast cardioprotective cooling. J Am Coll Cardiol 49:601–605. doi:10.1016/j.jacc.2006.09.041
39. Torres-Gonzalez M, Gawlowski T, Kocalis H, Scott BT, Dillmann WH (2014) Mitochondrial 8-oxoguanine glycosylase decreases mitochondrial fragmentation and improves mitochondrial function in H9C2 cells under oxidative stress conditions. Am J Physiol 306:C221–C229. doi:10.1152/ajpcell.00140.2013
40. Wang J, Wang Q, Watson LJ, Jones SP, Epstein PN (2011) Cardiac overexpression of 8-oxoguanine DNA glycosylase 1 protects mitochondrial DNA and reduces cardiac fibrosis following transaortic constriction. Am J Physiol 301:H2073–H2080. doi:10.1152/ajpheart.00157.2011
41. Yang X-M, Cui L, Alhammouri A, Downey JM, Cohen MV (2013) Triple therapy greatly increases myocardial salvage during ischemia/reperfusion in the in situ rat heart. Cardiovasc Drugs Ther 5:403–412. doi:10.1007/s10557-013-6474-9
42. 12 blockers confer direct postconditioning-like protection in reperfused rabbit hearts. J Cardiovasc Pharmacol Ther 18:251–262. doi:10.1177/1074248412467692
43. Zhang Q, Raoof M, Chen Y, Sumi Y, Sursal T, Junger W, Brohi K, Itagaki K, Hauser CJ (2010) Circulating mitochondrial DAMPs cause inflammatory responses to injury. Nature 464:104–107. doi:10.1038/nature08780