Initiation of electron transport chain activity in the embryonic heart coincides with the activation of mitochondrial complex 1 and the formation of supercomplexes

PLoS ONE

Volumn 9, Issue 11, 2014, Pages

  Beutner, Gisela ^a   Eliseev, Roman A ^a   Porter, George A ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME C; CYTOCHROME C OXIDASE; MITOCHONDRIAL DNA; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SUCCINATE DEHYDROGENASE (UBIQUINONE); UBIQUINOL CYTOCHROME C REDUCTASE; UBIQUINONE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOGENESIS; CITRIC ACID CYCLE; COMPLEX FORMATION; DEVELOPMENTAL STAGE; DNA DETERMINATION; EMBRYO; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME ASSAY; HEART DEVELOPMENT; HEART MITOCHONDRION; MITOCHONDRIAL ENERGY TRANSFER; MOUSE; NONHUMAN; OXIDATIVE PHOSPHORYLATION; OXYGEN CONSUMPTION; AGE; ANIMAL; ANIMAL EMBRYO; C57BL MOUSE; ELECTRON TRANSPORT; GENE EXPRESSION REGULATION; GENETICS; HEART MUSCLE; METABOLISM; MITOCHONDRIAL MEMBRANE; PROTEIN MULTIMERIZATION;

AGE FACTORS; ANIMALS; ELECTRON TRANSPORT; ELECTRON TRANSPORT COMPLEX I; ELECTRON TRANSPORT COMPLEX II; ELECTRON TRANSPORT COMPLEX III; ELECTRON TRANSPORT COMPLEX IV; EMBRYO, MAMMALIAN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MICE; MICE, INBRED C57BL; MITOCHONDRIA, HEART; MITOCHONDRIAL MEMBRANES; MYOCARDIUM; OXIDATIVE PHOSPHORYLATION; PROTEIN MULTIMERIZATION;

EID: 84913553691     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0113330     Document Type: Article

References (51)

1. Porter GA Jr, Hom J, Hoffman D, Quintanilla R, de Mesy Bentley K, et al. Bioenergetics, mitochondria, and cardiac myocyte differentiation. Prog Pediatr Cardiol. 2011;31:75-81.
2. Ascuitto RJ, Ross-Ascuitto NT. Substrate metabolism in the developing heart. Semin Perinatol. 1996;20:542-563.
3. Lopaschuk GD, Jaswal JS. Energy metabolic phenotype of the cardiomyocyte during development, differentiation, and postnatal maturation. J Cardiovasc Pharmacol. 2010;56:130-140.
4. Baker CN, Ebert SN. Development of aerobic metabolism in utero: Requirement for mitochondrial function during embryonic and fetal periods. OA Biotechnology. 2013;2.
5. Ingraham CA, Burwell LS, Skalska J, Brookes PS, Howell RL, et al. NDUFS4: creation of a mouse model mimicking a Complex I disorder. Mitochondrion. 2009;9:204-210.
6. Hom JR, Quintanilla RA, Hoffman DL, de Mesy Bentley KL, Molkentin JD, et al. The permeability transition pore controls cardiac mitochondrial maturation and myocyte differentiation. Dev Cell. 2011;21:469-478.
7. Folmes CD, Dzeja PP, Nelson TJ, Terzic A. Mitochondria in control of cell fate. Circ Res. 2012;110:526-529.
8. Acin-Perez R, Fernandez-Silva P, Peleato ML, Perez-Martos A, Enriquez JA. Respiratory active mitochondrial supercomplexes. Mol Cell. 2008;32:529-539.
9. Lapuente-Brun E, Moreno-Loshuertos R, Acin-Perez R, Latorre-Pellicer A, Colas C, et al. Supercomplex assembly determines electron flux in the mitochondrial electron transport chain. Science. 2013;340:1567-1570.
10. Wittig I, Carrozzo R, Santorelli FM, Schagger H. Supercomplexes and subcomplexes of mitochondrial oxidative phosphorylation. Biochim Biophys Acta. 2006;1757:1066-1072.
11. Moreno-Lastres D, Fontanesi F, Garcia-Consuegra I, Martin MA, Arenas J, et al. Mitochondrial complex I plays an essential role in human respirasome assembly. Cell Metab. 2012;15:324-335.
12. Baines CP, Kaiser RA, Purcell NH, Blair NS, Osinska H, et al. Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature. 2005;434:658-662.
13. Elrod JW, Wong R, Mishra S, Vagnozzi RJ, Sakthievel B, et al. Cyclophilin D controls mitochondrial pore-dependent Ca(2+) exchange, metabolic flexibility, and propensity for heart failure in mice. J Clin Invest. 2010;120:3680-3687.
14. Sokolova N, Pan S, Provazza S, Beutner G, Vendelin M, et al. ADP Protects Cardiac Mitochondria under Severe Oxidative Stress. PLoS One. 2013;8:e83214.
15. Beutner G, Sharma VK, Lin L, Ryu SY, Dirksen RT, et al. Type 1 ryanodine receptor in cardiac mitochondria: transducer of excitation-metabolism coupling. Biochim Biophys Acta. 2005;1717:1-10.
16. Nicholls DG, Ferguson SJ. The oxygen electrode: monitoring proton current. Bionenergetis 4. 2013; Amsterdam: Elsevier.pp. 60-61.
17. Villani G, Attardi G. In vivo measurements of respiration control by cytochrome c oxidase and in situ analysis of oxidative phosphorylation. Methods Cell Biol. 2001;65:119-131.
18. Birch-Machin MA, Turnbull DM. Assaying mitochondrial respiratory complex activity in mitochondria isolated from human cells and tissues. Methods Cell Biol. 2001;65:97-117.
19. Degli Esposti M. Assessing functional integrity of mitochondria in vitro and in vivo. Methods Cell Biol. 2001;65:75-96.
20. Devlin TM. Textbook of Biochemistry With Clinical Correlations. 1997; New York: Wiley.
21. Reisch AS, Elpeleg O. Biochemical assays for mitochondrial activity: assays of TCA cycle enzymes and PDHc. Methods Cell Biol. 2007;80:199-222.
22. Wittig I, Karas M, Schagger H. High resolution clear native electrophoresis for in-gel functional assays and fluorescence studies of membrane protein complexes. Mol Cell Proteomics. 2007;6:1215-1225.
23. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970;227:680-685.
24. Wittig I, Carrozzo R, Santorelli FM, Schagger H. Functional assays in high-resolution clear native gels to quantify mitochondrial complexes in human biopsies and cell lines. Electrophoresis. 2007;28:3811-3820.
25. Brand MD, Nicholls DG. Assessing mitochondrial dysfunction in cells. Biochem J. 2011;435:297-312.
26. Villani G, Greco M, Papa S, Attardi G. Low reserve of cytochrome c oxidase capacity in vivo in the respiratory chain of a variety of human cell types. J Biol Chem. 1998;273:31829-31836.
27. Dahout-Gonzalez C, Nury H, Trezeguet V, Lauquin GJ, Pebay-Peyroula E, et al. Molecular, functional, and pathological aspects of the mitochondrial ADP/ATP carrier. Physiology (Bethesda). 2006;21:242-249.
28. Marzo I, Brenner C, Zamzami N, Susin SA, Beutner G, et al. The permeability transition pore complex: a target for apoptosis regulation by caspases and bcl-2-related proteins. J Exp Med. 1998;187:1261-1271.
29. Halestrap AP, Pasdois P. The role of the mitochondrial permeability transition pore in heart disease. Biochim Biophys Acta. 2009;1787:1402-1415.
30. Genova ML, Lenaz G. Functional role of mitochondrial respiratory supercomplexes. Biochim Biophys Acta. 2014;1837:427-443.
31. Galkin A, Abramov AY, Frakich N, Duchen MR, Moncada S. Lack of oxygen deactivates mitochondrial complex I: implications for ischemic injury? J Biol Chem. 2009;284:36055-36061.
32. Lenaz G, Fato R, Genova ML, Bergamini C, Bianchi C, et al. Mitochondrial Complex I: structural and functional aspects. Biochim Biophys Acta. 2006;1757:1406-1420.
33. Fukuda R, Zhang H, Kim JW, Shimoda L, Dang CV, et al. HIF-1 regulates cytochrome oxidase subunits to optimize efficiency of respiration in hypoxic cells. Cell. 2007;129:111-122.
34. Saks V, Guzun R, Timohhina N, Tepp K, Varikmaa M, et al. Structure-function relationships in feedback regulation of energy fluxes in vivo in health and disease: mitochondrial interactosome. Biochim Biophys Acta. 2010;1797:678-697.
35. Cox SJ, Gunberg DL. Metabolite utilization by isolated embryonic rat hearts in vitro. J Embryol Exp Morphol. 1972;28:235-245.
36. Owen OE, Kalhan SC, Hanson RW. The key role of anaplerosis and cataplerosis for citric acid cycle function. J Biol Chem. 2002;277:30409-30412.
37. Hirst J. Mitochondrial complex I. Annu Rev Biochem. 2013;82:551-575.
38. Mimaki M, Wang X, McKenzie M, Thorburn DR, Ryan MT. Understanding mitochondrial complex I assembly in health and disease. Biochim Biophys Acta. 2012;1817:851-862.
39. Babot M, Birch A, Labarbuta P, Galkin A. Characterisation of the active/de-active transition of mitochondrial complex I. Biochim Biophys Acta. 2014.
40. Babot M, Labarbuta P, Birch A, Kee S, Fuszard M, et al. ND3, ND1 and 39 kDa subunits are more exposed in the de-active form of bovine mitochondrial complex I. Biochim Biophys Acta. 2014;1837:929-939.
41. Stroud DA, Formosa LE, Wijeyeratne XW, Nguyen TN, Ryan MT. Gene knockout using transcription activator-like effector nucleases (TALENs) reveals that human NDUFA9 protein is essential for stabilizing the junction between membrane and matrix arms of complex I. J Biol Chem. 2013;288:1685-1690.
42. Acin-Perez R, Enriquez JA. The function of the respiratory supercomplexes: the plasticity model. Biochim Biophys Acta. 2014;1837:444-450.
43. Huang TT, Naeemuddin M, Elchuri S, Yamaguchi M, Kozy HM, et al. Genetic modifiers of the phenotype of mice deficient in mitochondrial superoxide dismutase. Hum Mol Genet. 2006;15:1187-1194.
44. Huang G, Lu H, Hao A, Ng DC, Ponniah S, et al. GRIM-19, a cell death regulatory protein, is essential for assembly and function of mitochondrial complex I. Mol Cell Biol. 2004;24:8447-8456.
45. Bushdid PB, Osinska H, Waclaw RR, Molkentin JD, Yutzey KE. NFATc3 and NFATc4 are required for cardiac development and mitochondrial function. Circ Res. 2003;92:1305-1313.
46. Koushik SV, Wang J, Rogers R, Moskophidis D, Lambert NA, et al. Targeted inactivation of the sodium-calcium exchanger (Ncx1) results in the lack of a heartbeat and abnormal myofibrillar organization. FASEB J. 2001;15:1209-1211.
47. Ruiz-Lozano P, Smith SM, Perkins G, Kubalak SW, Boss GR, et al. Energy deprivation and a deficiency in downstream metabolic target genes during the onset of embryonic heart failure in RXRalpha2/2 embryos. Development. 1998;125:533-544.
48. Haworth RA, Hunter DR. Control of the mitochondrial permeability transition pore by high-affinity ADP binding at the ADP/ATP translocase in permeabilized mitochondria. J Bioenerg Biomembr. 2000;32:91-96.
49. Alavian KN, Beutner G, Lazrove E, Sacchetti S, Park H-A, et al. An uncoupling channel within the csubunit ring of the F1FO ATP synthase is the mitochondrial permeability transition pore. Proceedings of the National Academy of Sciences In press. 2014.
50. Cogliati S, Frezza C, Soriano ME, Varanita T, Quintana-Cabrera R, et al. Mitochondrial cristae shape determines respiratory chain supercomplexes assembly and respiratory efficiency. Cell. 2013;155:160-171.
51. Scalettar BA, Abney JR, Hackenbrock CR. Dynamics, structure, and function are coupled in the mitochondrial matrix. Proc Natl Acad Sci U S A. 1991;88:8057-8061.