A new low molecular weight, MnII-containing scavenger of superoxide anion protects cardiac muscle cells from hypoxia/reoxygenation injury

Free Radical Research

Volumn 49, Issue 1, 2015, Pages 67-77

  Nistri, Silvia ^a   Boccalini, G ^a   Bencini, A ^b   Becatti, M ^b   Valtancoli, B ^b   Conti, L ^b   Lucarini, L ^b   Bani, D ^a  

^a UNIVERSITY OF FLORENCE   (Italy)

^b UNIVERSITY OF FLORENCE   (Italy)

Author keywords

H9c2 cardiac muscle cells; Hypoxia; Oxidative stress; Reoxygenation; ROS scavenger; Superoxide anion

Indexed keywords

3 NITROTYROSINE; 8 HYDROXYDEOXYGUANOSINE; ANTIOXIDANT; CASPASE 3; DICHLORODIHYDROFLUORESCEIN DIACETATE; DNA NUCLEOTIDYLEXOTRANSFERASE; MANGANESE 4,10 DIMETHYL 1,4,7,10 TETRAAZACYCLODODECANE 1,7 DIACETATE; MANGANESE DERIVATIVE; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; REACTIVE OXYGEN METABOLITE; SCAVENGER; SUPEROXIDE; UNCLASSIFIED DRUG; ZINC 4,10 DIMETHYL 1,4,7,10 TETRAAZACYCLODODECANE 1,7 DIACETATE; ZINC DERIVATIVE; COORDINATION COMPOUND; MANGANESE;

ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DAMAGE; CELL HYPOXIA; CELL PROTECTION; CELL VIABILITY; CONTROLLED STUDY; CULTURE MEDIUM; EMBRYO; HEART MUSCLE CELL; IN VITRO STUDY; MEMBRANE POTENTIAL; MITOCHONDRIAL MEMBRANE POTENTIAL; MOLECULAR WEIGHT; MTT ASSAY; NICK END LABELING; NONHUMAN; OXIDATION REDUCTION POTENTIAL; OXIDATIVE STRESS; PROTEIN EXPRESSION; RAT; REOXYGENATION; ANIMAL; CELL LINE; DRUG EFFECTS; METABOLISM; MYOCARDIAL REPERFUSION INJURY; PHYSIOLOGY;

ANIMALS; ANTIOXIDANTS; CELL HYPOXIA; CELL LINE; COORDINATION COMPLEXES; FREE RADICAL SCAVENGERS; MANGANESE; MOLECULAR WEIGHT; MYOCARDIAL REPERFUSION INJURY; MYOCYTES, CARDIAC; OXIDATIVE STRESS; RATS; REACTIVE OXYGEN SPECIES; SUPEROXIDES;

EID: 84915821698     PISSN: 10715762     EISSN: 10292470     Source Type: Journal    
DOI: 10.3109/10715762.2014.979168     Document Type: Article

References (45)

1. Gerschman R, Gilbert DL, Nye SW, Dwyer P, Fenn WO. Oxygen poisoning and x-irradiation: a mechanism in common. Science 1954;119:623-626.
2. Murphy E, Steenbergen C. Mechanisms underlying acute protection from cardiac ischemia-reperfusion injury. Physiol Rev 2008;88:581-609.
3. McCord JM, Fridovich I. Superoxide dismutase: an enzymatic function for erythrocuprein (hemocuprein). J Biol Chem 1969;244:6049-6055.
4. Fridovich I. Superoxide dismutases. An adaptation to a paramagnetic gas. J Biol Chem 1989;264:7761-7764.
5. Johnson F, Giulivi C. Superoxide dismutases and their impact upon human health. Mol Aspects Med 2005;26:340-352.
6. Finkel T. Radical medicine: treating ageing to cure disease. Nat Rev Mol Cell Biol 2005;6:971-976.
7. Wang ZQ, Porreca F, Cuzzocrea S, Galen K, Lightfoot R, Masini E, et al. A newly identified role for superoxide in inflammatory pain. J Pharmacol Exp Ther 2004;309:869-878.
8. Salvemini D, Wang ZQ, Zweier JL, Samouilov A, Macarthur H, Misko TP, et al. A nonpeptidyl mimic of superoxide dismutase with therapeutic activity in rats. Science 1999;286:304-306.
9. Jaeschke H, Woolbright BL. Current strategies to minimize hepatic ischemia-reperfusion injury by targeting reactive oxygen species. Transplant Rev (Orlando) 2012;26:103-114.
10. Murphy MP. How mitochondria produce reactive oxygen species. Biochem J 2009;417:1-13.
11. Poyton RO, Ball KA, Castello PR. Mitochondrial generation of free radicals and hypoxic signaling. Trends Endocrinol Metab 2009;20:332-340.
12. Castello PR, Woo DK, Ball K, Wojcik J, Liu L, Poyton RO. Oxygen-regulated isoforms of cytochrome c oxidase have differential effects on its nitric oxide production and on hypoxic signaling. Proc Natl Acad Sci USA 2008;105:8203-8208.
13. Galkin A, Higgs A, Moncada S. Nitric oxide and hypoxia. Essays Biochem 2007;3:29-42.
14. Kokura S, Yoshida N, Yoshikawa T. Anoxia/reoxygenation-induced leukocyte-endothelial cell interactions. Free Radic Biol Med 2002;33:427-432.
15. Bencini A, Failli P, Valtancoli B, Bani D. Low molecular weight compounds with transition metals as free radical scavengers and novel therapeutic agents. Cardiovasc Hematol Agents Med Chem 2010;8:128-146.
16. Ferrer-Sueta G, Radi R. Chemical biology of peroxynitrite: kinetics, diffusion, and radicals. ACS Chem Biol 2009;4:161-177.
17. Xie YW, Kaminski PM, Wolin MS. Inhibition of rat cardiac muscle contraction and mitochondrial respiration by endogenous peroxynitrite formation during posthypoxic reoxygenation. Circ Res 1998;82:891-897.
18. Seal JB, Gewertz BL. Vascular dysfunction in ischemia-reperfusion injury. Ann Vasc Surg. 2005;19:572-584.
19. Liu J, Hou J, Xia ZY, Zeng W, Wang X, Li R, et al. Recombinant PTD-Cu/Zn SOD attenuates hypoxia-reoxygenation injury in cardiomyocytes. Free Radic Res 2013;47:386-393.
20. McCord JM, Edeas MA. SOD, oxidative stress and human pathologies: a brief history and a future vision. Biomed Pharmacother 2005;59:139-142.
21. Slemmer JE, Shacka JJ, Sweeney MI, Weber JT. Antioxidants and free radical scavengers for the treatment of stroke, traumatic brain injury and aging. Curr Med Chem 2008;15:404-414.
22. Riley DP, Weiss RH. Manganese macrocyclic ligand complexes as mimics of superoxide dismutase. J Am Chem Soc 1994;116:387-388.
23. Bani D, Bencini A. Developing ROS scavenging agents for pharmacological purposes: recent advances in design of manganese-based complexes with anti-inflammatory and anti-nociceptive activity. Curr Med Chem 2012;19:4431-4444.
24. Batinic-Haberle I, Tovmasyan A, Roberts ERH, Vujaskovic Z, Leong KW, Spasojevic I. SOD Therapeutics: latest insights into their structure-activity relationships and impact on the cellular redox-based signaling pathways. Antioxid Redox Signal 2014;20:2372-2415.
25. Failli P, Bani D, Bencini A, Cantore M, Di Cesare Mannelli L, Ghelardini C, et al. A novel manganese complex effective as superoxide anion scavenger and therapeutic agent against cell and tissue oxidative injury. J Med Chem 2009;52:7273-7283.
26. Bianchi A, Calabi L, Corana F, Fontana S, Losi P, Maiocchi A, et al. Thermodynamics and structural properties of Gd(III) complexes with polyamino-polycarboxylic ligands: basic compound for the development of MRI contrast agents. Coord Chem Rev 2000;24:309-393.
27. Merbach AE, Tóth E. The Chemistry of Contrast Agents in Medical Magnetic Resonance Imaging. New York: John Wiley & Sons; 2001.
28. Cinci L, Masini E, Bencini A, Valtancoli B, Mastroianni R, Calosi L, Bani D. Suppression of allergen-induced respiratory dysfunction and airway inflammation in sensitized guinea pigs by Mn(II)(Me(2)DO2A), a novel superoxide scavenger compound. Free Radic Biol Med 2010;48:1525-1534.
29. Di Cesare Mannelli L, Bani D, Bencini A, Brandi ML, Calosi L, Cantore M, et al. Therapeutic effects of the superoxide dismutase mimetic compound Mn II Me 2 DO2A on experimental articular pain in rats. Mediat Inflamm 2013:2013:905360.
30. Bani D, Bencini A, Cantore M, Failli P, Giorgi C, Valtancoli B. Manganese and cobalt complexes, their preparation and use. International patent Appl. No. PCT/IB2009/053859, University of Florence, Italy, March 11th, 2010. Owned by General Project Ltd., Montespertoli (Florence), Italy.
31. Lindoy LF. The Chemistry of Macrocyclic Ligand Complexes Cambridge, UK: Cambridge University Press; 1989.
32. Taqui-Khan M, Martell AE. Thermodynamic quantities associated with the interaction of adenosine triphosphate with metal ions. J Am Chem Soc 1966;88:668-671.
33. Martin RB, Edsall JT. The association of divalent cations with glutathione. J Am Chem Soc 1959;81:4044-4047.
34. Amico P, Bonomo RP, Calì R, Cucinotta V, Daniele PG, Ostacoli G, Rizzarelli E. Ligand-ligand interactions in metal complexes. Thermodynamic and spectroscopic investigation of simple and mixed copper(II) and zinc(II) substituted malonate complexes with 2,2′-bipyridyl in aqueous solution Inorg Chem 1989;28:3555-3561.
35. Martell AE, Smith RM. NIST Standard Reference Database 46 Version 8.0 Gaithersburg. USA: NIST; 2004.
36. Thun H, Guns W, Verbeek F. The stability constants of some bivalent metal complexes of α-hydroxyisobutyrate and lactate. Anal Chim Acta 1967;37:332-336.
37. Spasojevic I, Li AM, Tovmasyan A, Rajic Z, Salvemini D, St. Clair D, et al. Accumulation of porphyrin-based SOD mimics in mitochondria is proportional to their lipophilicity. S. cerevisiae study of ortho Mn(III) N-alkylpyridylporphyrins. Free Radic Biol Med 2010;S199:49.
38. Cotton FA, Wilkinson G, Murillo CA, Bochmann M. Advanced Inorganic Chemistry, 6th ed New York: Wiley-Interscience; 1999.
39. Zhang ZL, Fan Y, Liu ML. Ginsenoside Rg1 inhibits autophagy in H9c2 cardiomyocytes exposed to hypoxia/reoxygenation. Mol Cell Biochem 2012;365:243-250.
40. Petronilli V, Miotto G, Canton M, Brini M, Colonna R, Bernardi P, Di Lisa F. Transient and longlasting openings of the mitochondrial permeability transition pore can be monitored directly in intact cells by changes in mitochondrial calcein fluorescence. Biophys J 1999;765:725-754.
41. Masini E, Cuzzocrea S, Mazzon E, Muià C, Vannacci A, Fabrizi F, Bani D. Protective effects of relaxin in ischemia/reperfusion-induced intestinal injury due to splanchnic artery occlusion. Br J Pharmacol 2006;148:1124-1132.
42. Robin E, Derichard A, Vallet B, Hassoun SM, Neviere R. Nitric oxide scavenging modulates mitochondrial dysfunction induced by hypoxia/reoxygenation. Pharmacol Rep 2011;63:1189-1194.
43. Masini E, Cuzzocrea S, Mazzon E, Marzocca C, Mannaioni PF, Salvemini D. Protective effects of M40403, a selective superoxide dismutase mimetic, in myocardial ischaemia and reperfusion injury in vivo. Br J Pharmacol 2002;136:905-917.
44. Bourdillon PD, Poole-Wilson PA. Effects of ischaemia and reperfusion on calcium exchange and mechanical function in isolated rabbit myocardium. Cardiovasc Res 1981;15:121-130.
45. Filipović MR, Koh AC, Arbault S, Niketić V, Debus A, Schleicher U, et al. Striking inflammation from both sides: manganese(II) pentaazamacrocyclic SOD mimics act also as nitric oxide dismutases: a single-cell study. Angew Chem Int Ed Engl 2010;49:4228-4232.