Effects of iron overload, an iron chelator and a T-Type calcium channel blocker on cardiac mitochondrial biogenesis and mitochondrial dynamics in thalassemic mice

European Journal of Pharmacology

Volumn 799, Issue , 2017, Pages 118-127

  Khamseekaew, Juthamas ^a,b   Kumfu, Sirinart ^a,b   Wongjaikam, Suwakon ^a,b   Kerdphoo, Sasiwan ^a,b   Jaiwongkam, Thidarat ^a,b   Srichairatanakool, Somdet ^a   Fucharoen, Suthat ^c   Chattipakorn, Siriporn C ^a,b   Chattipakorn, Nipon ^a,b  

^a Faculty of Medicine Chiang Mai University   (Thailand)

^b CHIANG MAI UNIVERSITY   (Thailand)

^c MAHIDOL UNIVERSITY   (Thailand)

Author keywords

Cardiomyopathy; Iron overload; Mitochondrial dynamics; Oxidative phosphorylation; Thalassemic mice

Indexed keywords

CALCIUM CHANNEL BLOCKING AGENT; CASPASE 3; CYTOCHROME C OXIDASE; DEFERIPRONE; EFONIDIPINE; AMINOPHYLLINE; ATROPINE; CALCIUM CHANNEL T TYPE; DIHYDROPYRIDINE DERIVATIVE; DRUG COMBINATION; GLYCERYL TRINITRATE; IRON; IRON CHELATING AGENT; MALONALDEHYDE; MYOCARDON; NITROPHENOL; ORGANOPHOSPHORUS COMPOUND; PAPAVERINE; PHENOBARBITAL; PYRIDONE DERIVATIVE;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BETA THALASSEMIA; BLOOD LEVEL; CARDIAC MITOCHONDRIAL FUNCTION; CELL FUNCTION; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; HEART DISEASE; HEART LEFT VENTRICLE FUNCTION; HEART RATE VARIABILITY; IRON OVERLOAD; MALE; MITOCHONDRIAL BIOGENESIS; MITOCHONDRIAL DYNAMICS; MOUSE; NONHUMAN; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; PROTEIN EXPRESSION; ANIMAL; BLOOD; BLOOD PRESSURE; CARDIAC MUSCLE; COMPLICATION; DRUG COMBINATION; DRUG EFFECTS; HEART; HEART RATE; METABOLISM; MITOCHONDRION; ORGANELLE BIOGENESIS; PATHOLOGY; PATHOPHYSIOLOGY; SIGNAL TRANSDUCTION; THALASSEMIA;

AMINOPHYLLINE; ANIMALS; APOPTOSIS; ATROPINE; BLOOD PRESSURE; CALCIUM CHANNEL BLOCKERS; CALCIUM CHANNELS, T-TYPE; DIHYDROPYRIDINES; DRUG COMBINATIONS; HEART; HEART RATE; IRON; IRON CHELATING AGENTS; IRON OVERLOAD; MALE; MALONDIALDEHYDE; MICE; MITOCHONDRIA; MYOCARDIUM; NITROGLYCERIN; NITROPHENOLS; ORGANELLE BIOGENESIS; ORGANOPHOSPHORUS COMPOUNDS; OXIDATIVE PHOSPHORYLATION; PAPAVERINE; PHENOBARBITAL; PYRIDONES; SIGNAL TRANSDUCTION; THALASSEMIA;

EID: 85012924821     PISSN: 00142999     EISSN: 18790712     Source Type: Journal    
DOI: 10.1016/j.ejphar.2017.02.015     Document Type: Article

References (36)

1. Anderson, E.R., Shah, Y.M., Iron homeostasis in the liver. Compr. Physiol. 3 (2013), 315–330, 10.1002/cphy.c120016.
2. Arnoult, D., Mitochondrial fragmentation in apoptosis. Trends Cell. Biol. 17 (2007), 6–12, 10.1016/j.tcb.2006.11.001.
3. Bartfay, W.J., Bartfay, E., Iron-overload cardiomyopathy: evidence for a free radical–mediated mechanism of injury and dysfunction in a murine model. Biol. Res. Nurs. 2 (2000), 49–59, 10.1177/109980040000200106.
4. Bossy-Wetzel, E., Barsoum, M.J., Godzik, A., Schwarzenbacher, R., Lipton, S.A., Mitochondrial fission in apoptosis, neurodegeneration and aging. Curr. Opin. Cell. Biol. 15 (2003), 706–716, 10.1016/j.ceb.2003.10.015.
5. Breuer, W., Hershko, C., Cabantchik, Z.I., The importance of non-transferrin bound iron in disorders of iron metabolism. Transfus. Sci. 23 (2000), 185–192, 10.1016/S0955-3886(00)00087-4.
6. Chen, M.P., Cabantchik, Z.I., Chan, S., Chan, G.C., Cheung, Y.F., Iron overload and apoptosis of HL-1 cardiomyocytes: effects of calcium channel blockade. PLoS. One, 9, 2014, e112915, 10.1371/journal.pone.0112915.
7. Chen, Y., Liu, Y., Dorn, G.W. 2nd, Mitochondrial fusion is essential for organelle function and cardiac homeostasis. Circ. Res. 109 (2011), 1327–1331, 10.1161/CIRCRESAHA.111.258723.
8. Das, S.K., Wang, W., Zhabyeyev, P., Basu, R., McLean, B., Fan, D., Parajuli, N., DesAulniers, J., Patel, V.B., Hajjar, R.J., Dyck, J.R., Kassiri, Z., Oudit, G.Y., Iron-overload injury and cardiomyopathy in acquired and genetic models is attenuated by resveratrol therapy. Sci. Rep., 5, 2015, 18132, 10.1038/srep18132.
9. Gao, L., Laude, K., Cai, H., Mitochondrial pathophysiology, reactive oxygen species, and cardiovascular diseases. Vet. Clin. North. Am. Small. Anim. Pract. 38 (2008), 137–155, 10.1016/j.cvsm.2007.10.004.
10. Gao, X., Campian, J.L., Qian, M., Sun, X.F., Eaton, J.W., Mitochondrial DNA damage in iron overload. J. Biol. Chem. 284 (2009), 4767–4775, 10.1074/jbc.M806235200.
11. Gao, X., Qian, M., Campian, J.L., Marshall, J., Zhou, Z., Roberts, A.M., Kang, Y.J., Prabhu, S.D., Sun, X.F., Eaton, J.W., Mitochondrial dysfunction may explain the cardiomyopathy of chronic iron overload. Free. Radic. Biol. Med. 49 (2010), 401–407, 10.1016/j.freeradbiomed.2010.04.033.
12. Ishihara, T., Ban-Ishihara, R., Maeda, M., Matsunaga, Y., Ichimura, A., Kyogoku, S., Aoki, H., Katada, S., Nakada, K., Nomura, M., Mizushima, N., Mihara, K., Ishihara, N., Dynamics of mitochondrial DNA nucleoids regulated by mitochondrial fission is essential for maintenance of homogeneously active mitochondria during neonatal heart development. Mol. Cell. Biol. 35 (2015), 211–223, 10.1128/MCB.01054-14.
13. Karbowski, M., Youle, R.J., Dynamics of mitochondrial morphology in healthy cells and during apoptosis. Cell. Death Differ. 10 (2003), 870–880, 10.1038/sj.cdd.4401260.
14. Khungwanmaythawee, K., Sornjai, W., Paemanee, A., Jaratsittisin, J., Fucharoen, S., Svasti, S., Lithanatudom, P., Roytrakul, S., Smith, D.R., Mitochondrial changes in beta0-thalassemia/Hb E disease. PLoS. One, 11, 2016, e0153831, 10.1371/journal.pone.0153831.
15. Kumfu, S., Chattipakorn, S., Chinda, K., Fucharoen, S., Chattipakorn, N., T-type calcium channel blockade improves survival and cardiovascular function in thalassemic mice. Eur. J. Haematol. 88 (2012), 535–548, 10.1111/j.1600-0609.2012.01779.x.
16. Kumfu, S., Chattipakorn, S., Fucharoen, S., Chattipakorn, N., Mitochondrial calcium uniporter blocker prevents cardiac mitochondrial dysfunction induced by iron overload in thalassemic mice. Biometals 25 (2012), 1167–1175, 10.1007/s10534-012-9579-x.
17. Kumfu, S., Chattipakorn, S., Srichairatanakool, S., Settakorn, J., Fucharoen, S., Chattipakorn, N., T-type calcium channel as a portal of iron uptake into cardiomyocytes of beta-thalassemic mice. Eur. J. Haematol. 86 (2011), 156–166, 10.1111/j.1600-0609.2010.01549.x.
18. Kumfu, S., Chattipakorn, S.C., Fucharoen, S., Chattipakorn, N., Dual T-type and L-type calcium channel blocker exerts beneficial effects in attenuating cardiovascular dysfunction in iron-overloaded thalassaemic mice. Exp. Physiol. 101 (2016), 521–539, 10.1113/EP085517.
19. Lee, Y.J., Jeong, S.Y., Karbowski, M., Smith, C.L., Youle, R.J., Roles of the mammalian mitochondrial fission and fusion mediators Fis1, Drp1, and Opa1 in apoptosis. Mol. Biol. Cell. 15 (2004), 5001–5011, 10.1091/mbc.E04-04-0294.
20. Legros, F., Lombes, A., Frachon, P., Rojo, M., Mitochondrial fusion in human cells is efficient, requires the inner membrane potential, and is mediated by mitofusins. Mol. Biol. Cell. 13 (2002), 4343–4354, 10.1091/mbc.E02-06-0330.
21. Link, G., Pinson, A., Kahane, I., Hershko, C., Iron loading modifies the fatty acid composition of cultured rat myocardial cells and liposomal vesicles: effect of ascorbate and alpha-tocopherol on myocardial lipid peroxidation. J. Lab. Clin. Med. 114 (1989), 243–249 http://www.ncbi.nlm.nih.gov/pubmed/2769018.
22. Ma, Y., Podinovskaia, M., Evans, P.J., Emma, G., Schaible, U.E., Porter, J., Hider, R.C., A novel method for non-transferrin-bound iron quantification by chelatable fluorescent beads based on flow cytometry. Biochem. J. 463 (2014), 351–362, 10.1042/BJ20140795.
23. Matthes, T., Rustin, P., Trachsel, H., Darbellay, R., Costaridou, S., Xaidara, A., Rideau, A., Beris, P., Different pathophysiological mechanisms of intramitochondrial iron accumulation in acquired and congenital sideroblastic anemia caused by mitochondrial DNA deletion. Eur. J. Haematol. 77 (2006), 169–174, 10.1111/j.1600-0609.2006.00674.x.
24. Olivieri, N.F., Brittenham, G.M., Matsui, D., Berkovitch, M., Blendis, L.M., Cameron, R.G., McClelland, R.A., Liu, P.P., Templeton, D.M., Koren, G., Iron-chelation therapy with oral deferipronein patients with thalassemia major. N. Engl. J. Med. 332 (1995), 918–922, 10.1056/NEJM199504063321404.
25. Ong, S.B., Subrayan, S., Lim, S.Y., Yellon, D.M., Davidson, S.M., Hausenloy, D.J., Inhibiting mitochondrial fission protects the heart against ischemia/reperfusion injury. Circulation 121 (2010), 2012–2022, 10.1161/CIRCULATIONAHA.109.906610.
26. Palee, S., Weerateerangkul, P., Chinda, K., Chattipakorn, S.C., Chattipakorn, N., Mechanisms responsible for beneficial and adverse effects of rosiglitazone in a rat model of acute cardiac ischaemia-reperfusion. Exp. Physiol. 98 (2013), 1028–1037, 10.1113/expphysiol.2012.070433.
27. Rebouche, C.J., Wilcox, C.L., Widness, J.A., Microanalysis of non-heme iron in animal tissues. J. Biochem Biophys. Methods 58 (2004), 239–251, 10.1016/j.jbbm.2003.11.003.
28. Samniang, B., Shinlapawittayatorn, K., Chunchai, T., Pongkan, W., Kumfu, S., Chattipakorn, S.C., KenKnight, B.H., Chattipakorn, N., Vagus nerve stimulation improves cardiac function by preventing mitochondrial dysfunction in obese-insulin resistant rats. Sci. Rep., 6, 2016, 19749, 10.1038/srep19749.
29. Smirnova, E., Shurland, D.L., Ryazantsev, S.N., van der Bliek, A.M., A human dynamin-related protein controls the distribution of mitochondria. J. Cell. Biol. 143 (1998), 351–358, 10.1083/jcb.143.2.351.
30. Soriano, F.X., Liesa, M., Bach, D., Chan, D.C., Palacin, M., Zorzano, A., Evidence for a mitochondrial regulatory pathway defined by peroxisome proliferator-activated receptor-gamma coactivator-1 alpha, estrogen-related receptor-alpha, and mitofusin 2. Diabetes 55 (2006), 1783–1791, 10.2337/db05-0509.
31. Sripetchwandee, J., KenKnight, S.B., Sanit, J., Chattipakorn, S., Chattipakorn, N., Blockade of mitochondrial calcium uniporter prevents cardiac mitochondrial dysfunction caused by iron overload. Acta Physiol. 210 (2014), 330–341, 10.1111/apha.12162.
32. Tanajak, P., Sa-Nguanmoo, P., Wang, X., Liang, G., Li, X., Jiang, C., Chattipakorn, S.C., Chattipakorn, N., Fibroblast growth factor 21 (FGF21) therapy attenuates left ventricular dysfunction and metabolic disturbance by improving FGF21 sensitivity, cardiac mitochondrial redox homoeostasis and structural changes in pre-diabetic rats. Acta Physiol. 217 (2016), 287–299, 10.1111/apha.12698.
33. Tanaka, H., Shigenobu, K., Efonidipine hydrochloride: a dual blocker of L- and T-type ca(2+) channels. Cardiovasc. Drug. Rev. 20 (2002), 81–92, 10.1111/j.1527-3466.2002.tb00084.x.
34. Thummasorn, S., Kumfu, S., Chattipakorn, S., Chattipakorn, N., Granulocyte-colony stimulating factor attenuates mitochondrial dysfunction induced by oxidative stress in cardiac mitochondria. Mitochondrion 11 (2011), 457–466, 10.1016/j.mito.2011.01.008.
35. Wang, Y., Wu, M., Al-Rousan, R., Liu, H., Fannin, J., Paturi, S., Arvapalli, R.K., Katta, A., Kakarla, S.K., Rice, K.M., Triest, W.E., Blough, E.R., Iron-induced cardiac damage: role of apoptosis and deferasirox intervention. J. Pharmacol. Exp. Ther. 336 (2011), 56–63, 10.1124/jpet.110.172668.
36. Wood, J.C., Enriquez, C., Ghugre, N., Otto-Duessel, M., Aguilar, M., Nelson, M.D., Moats, R., Coates, T.D., Physiology and pathophysiology of iron cardiomyopathy in thalassemia. Ann. N. Y. Acad. Sci. 1054 (2005), 386–395, 10.1196/annals.1345.047.