Lipidomic characterization of streptozotocin-induced heart mitochondrial dysfunction

Mitochondrion

Volumn 13, Issue 6, 2013, Pages 762-771

  Ferreira, Rita ^a   Guerra, Gabriela ^a   Padrão, Ana Isabel ^a   Melo, Tânia ^a   Vitorino, Rui ^a   Duarte, José Alberto ^b   Remião, Fernando ^b   Domingues, Pedro ^a   Amado, Francisco ^a   Domingues, M Rosário ^a  

^a UNIVERSITY OF AVEIRO   (Portugal)

^b UNIVERSITY OF PORTO   (Portugal)

Author keywords

Cardiolipin; Mitochondria; Oxidative modifications; Phospholipids; Respiratory chain complexes

Indexed keywords

CARDIOLIPIN; CITRATE SYNTHASE; CYTOCHROME C; MITOCHONDRIAL TRANSCRIPTION FACTOR A; PHOSPHATIDYLGLYCEROL; PHOSPHATIDYLINOSITOL; SPHINGOMYELIN; UNCOUPLING PROTEIN 3;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CARDIOMYOPATHY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DOWN REGULATION; ENZYME ACTIVITY; FATTY ACID OXIDATION; HEART MITOCHONDRION; INSULIN DEPENDENT DIABETES MELLITUS; LIPID PEROXIDATION; LIPIDOMICS; MALE; MITOCHONDRIAL MEMBRANE; NITRATION; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN CARBONYLATION; PROTEIN CONTENT; PROTEIN EXPRESSION; RAT;

CARDIOLIPIN; MITOCHONDRIA; OXIDATIVE MODIFICATIONS; PHOSPHOLIPIDS; RESPIRATORY CHAIN COMPLEXES;

ANIMALS; LIPIDS; MALE; MITOCHONDRIA, HEART; OXIDATIVE PHOSPHORYLATION; PHOSPHOLIPIDS; RATS; RATS, WISTAR; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; STREPTOZOCIN;

EID: 84887002981     PISSN: 15677249     EISSN: 18728278     Source Type: Journal    
DOI: 10.1016/j.mito.2013.05.001     Document Type: Article

References (50)

1. Ascensao A., Magalhaes J., Soares J.M., Ferreira R., Neuparth M.J., Marques F., Oliveira P.J., Duarte J.A. Moderate endurance training prevents doxorubicin-induced in vivo mitochondriopathy and reduces the development of cardiac apoptosis. Am. J. Physiol. Heart Circ. Physiol. 2005, 289(2):H722-H731.
2. Bartlett E.M., Lewis D.H. Spectrophotometric determination of phosphate esters in the presence and absence of orthophosphate. Anal. Biochem. 1970, 36(1):159-167.
3. Baseler W.A., Dabkowski E.R., Williamson C.L., Croston T.L., Thapa D., Powell M.J., Razunguzwa T.T., Hollander J.M. Proteomic alterations of distinct mitochondrial subpopulations in the type 1 diabetic heart: contribution of protein import dysfunction. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2011, 300(2):R186-R200.
4. Bayir H., Tyurin V.A., Tyurina Y.Y., Viner R., Ritov V., Amoscato A.A., Zhao Q., Zhang X.J., Janesko-Feldman K.L., Alexander H., Basova L.V., Clark R.S., Kochanek P.M., Kagan V.E. Selective early cardiolipin peroxidation after traumatic brain injury: an oxidative lipidomics analysis. Ann. Neurol. 2007, 62(2):154-169.
5. Bertholf R.L., Nicholson J.R., Wills M.R., Savory J. Measurement of lipid peroxidation products in rabbit brain and organs (response to aluminum exposure). Ann. Clin. Lab. Sci. 1987, 17(6):418-423.
6. Birch-Machin M.A., Briggs H.L., Saborido A.A., Bindoff L.A., Turnbull D.M. An evaluation of the measurement of the activities of complexes I-IV in the respiratory chain of human skeletal muscle mitochondria. Biochem. Med. Metab. Biol. 1994, 51(1):35-42.
7. Bligh E.G., Dyer W.J. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 1959, 37(8):911-917.
8. Bogdanov M., Mileykovskaya E., Dowhan W. Lipids in the assembly of membrane proteins and organization of protein supercomplexes: implications for lipid-linked disorders. Subcell. Biochem. 2008, 49:197-239.
9. Boudina S., Abel E.D. Diabetic cardiomyopathy, causes and effects. Rev. Endocr. Metab. Disord. 2010, 11(1):31-39.
10. Chicco A.J., Sparagna G.C. Role of cardiolipin alterations in mitochondrial dysfunction and disease. Am. J. Physiol. Cell Physiol. 2007, 292(1):C33-C44.
11. Choksi K.B., Papaconstantinou J. Age-related alterations in oxidatively damaged proteins of mouse heart mitochondrial electron transport chain complexes. Free Radic. Biol. Med. 2008, 44(10):1795-1805.
12. Claypool S.M. Cardiolipin, a critical determinant of mitochondrial carrier protein assembly and function. Biochim. Biophys. Acta 2009, 1788(10):2059-2068.
13. Coore H.G., Denton R.M., Martin B.R., Randle P.J. Regulation of adipose tissue pyruvate dehydrogenase by insulin and other hormones. Biochem. J. 1971, 125(1):115-127.
14. Dabkowski E.R., Baseler W.A., Williamson C.L., Powell M., Razunguzwa T.T., Frisbee J.C., Hollander J.M. Mitochondrial dysfunction in the type 2 diabetic heart is associated with alterations in spatially distinct mitochondrial proteomes. Am. J. Physiol. Heart Circ. Physiol. 2009, 299(2):H529-H540.
15. Doria M.L., Cotrim Z., Macedo B., Simoes C., Domingues P., Helguero L., Domingues M.R. Lipidomic approach to identify patterns in phospholipid profiles and define class differences in mammary epithelial and breast cancer cells. Breast Cancer Res. Treat. 2012, 133(2):635-648.
16. Duncan J.G. Mitochondrial dysfunction in diabetic cardiomyopathy. Biochim. Biophys. Acta 2011, 1813(7):1351-1359.
17. Figueiredo P.A., Ferreira R.M., Appell H.J., Duarte J.A. Age-induced morphological, biochemical, and functional alterations in isolated mitochondria from murine skeletal muscle. J. Gerontol. A Biol. Sci. Med. Sci. 2008, 63(4):350-359.
18. Gao J., Tarcea V.G., Karnovsky A., Mirel B.R., Weymouth T.E., Beecher C.W., Cavalcoli J.D., Athey B.D., Omenn G.S., Burant C.F., Jagadish H.V. Metscape: a Cytoscape plug-in for visualizing and interpreting metabolomic data in the context of human metabolic networks. Bioinformatics 2010, 26(7):971-973.
19. Gao X., Xu Y., Xu B., Liu Y., Cai J., Liu H.M., Lei S., Zhong Y.Q., Irwin M.G., Xia Z. Allopurinol attenuates left ventricular dysfunction in rats with early stages of streptozotocin-induced diabetes. Diabetes Metab. Res. Rev. 2012, 28(5):409-417.
20. Gerber L.K., Aronow B.J., Matlib M.A. Activation of a novel long-chain free fatty acid generation and export system in mitochondria of diabetic rat hearts. Am. J. Physiol. Cell Physiol. 2006, 291(6):C1198-C1207.
21. Guide for the Care and Use of Laboratory Animals The National Academies Press 1996.
22. Han X., Abendschein D.R., Kelley J.G., Gross R.W. Diabetes-induced changes in specific lipid molecular species in rat myocardium. Biochem. J. 2000, 35(Pt 1):79-89.
23. Han X., Yang J., Cheng H., Yang K., Abendschein D.R., Gross R.W. Shotgun lipidomics identifies cardiolipin depletion in diabetic myocardium linking altered substrate utilization with mitochondrial dysfunction. Biochemistry 2005, 44(50):16684-16694.
24. Han X., Yang J., Yang K., Zhao Z., Abendschein D.R., Gross R.W. Alterations in myocardial cardiolipin content and composition occur at the very earliest stages of diabetes: a shotgun lipidomics study. Biochemistry 2007, 46(21):6417-6428.
25. Hansford R.G., Tsuchiya N., Pepe S. Mitochondria in heart ischaemia and aging. Biochem. Soc. Symp. 1999, 66:141-147.
26. Hoppel C.L., Tandler B., Fujioka H., Riva A. Dynamic organization of mitochondria in human heart and in myocardial disease. Int. J. Biochem. Cell Biol. 2009, 41(10):1949-1956.
27. Houtkooper R.H., Vaz F.M. Cardiolipin, the heart of mitochondrial metabolism. Cell. Mol. Life Sci. 2008, 65(16):2493-2506.
28. Janssen A.J., Trijbels F.J., Sengers R.C., Smeitink J.A., van den Heuvel L.P., Wintjes L.T., Stoltenborg-Hogenkamp B.J., Rodenburg R.J. Spectrophotometric assay for complex I of the respiratory chain in tissue samples and cultured fibroblasts. Clin. Chem. 2007, 53(4):729-734.
29. Jin J., Hou Q., Mullen T.D., Zeidan Y.H., Bielawski J., Kraveka J.M., Bielawska A., Obeid L.M., Hannun Y.A., Hsu Y.T. Ceramide generated by sphingomyelin hydrolysis and the salvage pathway is involved in hypoxia/reoxygenation-induced Bax redistribution to mitochondria in NT-2 cells. J. Biol. Chem. 2008, 283(39):26509-26517.
30. Kanazawa A., Nishio Y., Kashiwagi A., Inagaki H., Kikkawa R., Horiike K. Reduced activity of mtTFA decreases the transcription in mitochondria isolated from diabetic rat heart. Am. J. Physiol. Endocrinol. Metab. 2002, 282(4):E778-E785.
31. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227(5259):680-685.
32. Lowry O.H., Rosebrough N.J., Farr A.L., Randall R.J. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 1951, 193(1):265-275.
33. Lumini-Oliveira J., Magalhaes J., Pereira C.V., Moreira A.C., Oliveira P.J., Ascensao A. Endurance training reverts heart mitochondrial dysfunction, permeability transition and apoptotic signaling in long-term severe hyperglycemia. Mitochondrion 2011, 11(1):54-63.
34. Maciel E., Domingues P., Domingues M.R. Liquid chromatography/tandem mass spectrometry analysis of long-chain oxidation products of cardiolipin induced by the hydroxyl radical. Rapid Commun. Mass Spectrom. 2011, 25(2):316-326.
35. MacLellan J.D., Gerrits M.F., Gowing A., Smith P.J., Wheeler M.B., Harper M.E. Physiological increases in uncoupling protein 3 augment fatty acid oxidation and decrease reactive oxygen species production without uncoupling respiration in muscle cells. Diabetes 2005, 54(8):2343-2350.
36. Nakamura H., Matoba S., Iwai-Kanai E., Kimata M., Hoshino A., Nakaoka M., Katamura M., Okawa Y., Ariyoshi M., Mita Y., Ikeda K., Okigaki M., Adachi S., Tanaka H., Takamatsu T., Matsubara H. p53 promotes cardiac dysfunction in diabetic mellitus caused by excessive mitochondrial respiration-mediated reactive oxygen species generation and lipid accumulation. Circ. Heart Fail. 2012, 5(1):106-115.
37. Novgorodov S.A., Gudz T.I. Ceramide and mitochondria in ischemia/reperfusion. J. Cardiovasc. Pharmacol. 2009, 53(3):198-208.
38. Padrao A.I., Ferreira R.M.P., Vitorino R., Alves R.M.P., Neuparth M.J., Duarte J.A., Amado F. OXPHOS susceptibility to oxidative modifications: the role of heart mitochondrial subcellular location. Biochim. Biophys. Acta Bioenerg. 2011, 1807(9):1106-1113.
39. Padrao A.I., Ferreira R., Vitorino R., Alves R.M., Figueiredo P., Duarte J.A., Amado F. Effect of lifestyle on age-related mitochondrial protein oxidation in mice cardiac muscle. Eur. J. Appl. Physiol. 2012, 112(4):1467-1474.
40. Padrao A.I., Carvalho T., Vitorino R., Alves R.M., Caseiro A., Duarte J.A., Ferreira R., Amado F. Impaired protein quality control system underlies mitochondrial dysfunction in skeletal muscle of streptozotocin-induced diabetic rats. Biochim. Biophys. Acta 2012, 1822(8):1189-1197.
41. 2+ in mitochondrial dysfunction and disease. Cell Calcium 2009, 45(6):643-650.
42. Rolo A.P., Palmeira C.M. Diabetes and mitochondrial function: role of hyperglycemia and oxidative stress. Toxicol. Appl. Pharmacol. 2006, 212(2):167-178.
43. Schagger H., von Jagow G. Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form. Anal. Biochem. 1991, 199(2):223-231.
44. Shen X., Zheng S., Thongboonkerd V., Xu M., Pierce W.M., Klein J.B., Epstein P.N. Cardiac mitochondrial damage and biogenesis in a chronic model of type 1 diabetes. Am. J. Physiol. Endocrinol. Metab. 2004, 287(5):E896-E905.
45. Sparagna G.C., Lesnefsky E.J. Cardiolipin remodeling in the heart. J. Cardiovasc. Pharmacol. 2009, 53(4):290-301.
46. Taylor R.W., Birch-Machin M.A., Bartlett K., Lowerson S.A., Turnbull D.M. The control of mitochondrial oxidations by complex III in rat muscle and liver mitochondria. Implications for our understanding of mitochondrial cytopathies in man. J. Biol. Chem. 1994, 269(5):3523-3528.
47. Turko I.V., Li L., Aulak K.S., Stuehr D.J., Chang J.Y., Murad F. Protein tyrosine nitration in the mitochondria from diabetic mouse heart. Implications to dysfunctional mitochondria in diabetes. J. Biol. Chem. 2003, 278(36):33972-33977.
48. Tyurin V.A., Tyurina Y.Y., Feng W., Mnuskin A., Jiang J., Tang M., Zhang X., Zhao Q., Kochanek P.M., Clark R.S., Bayir H., Kagan V.E. Mass-spectrometric characterization of phospholipids and their primary peroxidation products in rat cortical neurons during staurosporine-induced apoptosis. J. Neurochem. 2008, 107(6):1614-1633.
49. Vance J.E., Tasseva G. Formation and function of phosphatidylserine and phosphatidylethanolamine in mammalian cells. Biochim. Biophys. Acta. 2013, 1831(3):543-554.
50. Zerbetto E., Vergani L., Dabbeni-Sala F. Quantification of muscle mitochondrial oxidative phosphorylation enzymes via histochemical staining of blue native polyacrylamide gels. Electrophoresis 1997, 18(11):2059-2064.