Postnatal development of mouse heart: Formation of energetic microdomains

Journal of Physiology

Volumn 588, Issue 13, 2010, Pages 2443-2454

  Piquereau, Jérôme ^a,b   Novotova, Marta ^c   Fortin, Dominique ^a,b   Garnier, Anne ^a,b   Ventura Clapier, Renée ^a,b   Veksler, Vladimir ^a,b   Joubert, Frédéric ^a,b  

^a INSERM   (France)

^b UNIVERSITÉ PARIS SACLAY   (France)

^c INSTITUTE OF MOLECULAR PHYSIOLOGY AND GENETICS   (Slovakia)

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE NUCLEOTIDE; ADENOSINE TRIPHOSPHATASE; MYOSIN ADENOSINE TRIPHOSPHATASE; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; CALCIUM; MYOSIN; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; CALCIUM ION; CREATINE KINASE; MAGNESIUM; SAPONIN;

ARTICLE; CALCIUM TRANSPORT; CELL MATURATION; CELL MEMBRANE; HEART DEVELOPMENT; HEART MUSCLE CELL; MOUSE; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; ANIMAL; C57BL MOUSE; CARDIOMEGALY; ELECTRON MICROSCOPY; ENERGY METABOLISM; GROWTH, DEVELOPMENT AND AGING; HEART; HEART MITOCHONDRION; HEART MUSCLE; METABOLISM; MUSCLE FIBRIL; NEWBORN; PATHOLOGY; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SARCOPLASMIC RETICULUM; ULTRASTRUCTURE; WESTERN BLOTTING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; CELL ENERGY; CELL FUNCTION; CELL STRUCTURE; CELL TRANSFORMATION; CELL ULTRASTRUCTURE; CONTROLLED STUDY; CYTOSOL; ENZYME REGULATION; HEART LEFT VENTRICLE; MITOCHONDRIAL RESPIRATION; PROTEIN PROTEIN INTERACTION;

ADENINE NUCLEOTIDES; ANIMALS; ANIMALS, NEWBORN; BLOTTING, WESTERN; CALCIUM; CARDIOMEGALY; ENERGY METABOLISM; HEART; MICE; MICE, INBRED C57BL; MICROSCOPY, ELECTRON; MITOCHONDRIA, HEART; MYOCARDIUM; MYOCYTES, CARDIAC; MYOFIBRILS; MYOSINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SARCOPLASMIC RETICULUM; SARCOPLASMIC RETICULUM CALCIUM-TRANSPORTING ATPASES;

EID: 77954502577     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2010.189670     Document Type: Article

References (36)

1. Anmann T, Guzun R, Beraud N, Pelloux S, Kuznetsov AV, Kogerman L, Kaambre T, Sikk P, Paju K, Peet N, Seppet E, Ojeda C, Tourneur Y, Saks V. Different kinetics of the regulation of respiration in permeabilized cardiomyocytes and in HL-1 cardiac cells. Importance of cell structure/organization for respiration regulation. Biochim Biophys Acta 2006, 1757:1597-1606.
2. De Sousa E, Veksler V, Minajeva A, Kaasik A, Mateo P, Mayoux E, Hoerter J, Bigard X, Serrurier B, Ventura-Clapier R. Subcellular creatine kinase alterations. Implications in heart failure. Circ Res 1999, 85:68-76.
3. Estornell E, Fato R, Pallotti F, Lenaz G. Assay conditions for the mitochondrial NADH:coenzyme Q oxidoreductase. FEBS Lett 1993, 332:127-131.
4. Garnier A, Fortin D, Delomenie C, Momken I, Veksler V, Ventura-Clapier R. Depressed mitochondrial transcription factors and oxidative capacity in rat failing cardiac and skeletal muscles. J Physiol 2003, 551:491-501.
5. Hew KW, Keller KA. Postnatal anatomical and functional development of the heart: a species comparison. Birth Defects Res B Dev Reprod Toxicol 2003, 68:309-320.
6. Hoerter JA, Kuznetsov A, Ventura-Clapier R. Functional development of the creatine kinase system in perinatal rabbit heart. Circ Res 1991, 69:665-676.
7. Hoerter JA, Ventura-Clapier R, Kuznetsov A. Compartmentation of creatine kinases during perinatal development of mammalian heart. Mol Cell Biochem 1994, 133-134:277-286.
8. Kaasik A, Veksler V, Boehm E, Novotova M, Minajeva A, Ventura-Clapier R. Energetic crosstalk between organelles: architectural integration of energy production and utilization. Circ Res 2001, 89:153-159.
9. Kuznetsov AV, Veksler V, Gellerich FN, Saks V, Margreiter R, Kunz WS. Analysis of mitochondrial function in situ in permeabilized muscle fibres, tissues and cells. Nat Protoc 2008, 3:965-976.
10. Leu M, Ehler E, Perriard JC. Characterisation of postnatal growth of the murine heart. Anat Embryol (Berl) 2001, 204:217-224.
11. Minajeva A, Ventura-Clapier R, Veksler V. Ca2+ uptake by cardiac sarcoplasmic reticulum ATPase in situ strongly depends on bound creatine kinase. Pflugers Arch 1996, 432:904-912.
12. Muhlfeld C, Urru M, Rumelin R, Mirzaie M, Schondube F, Richter J, Dorge H. Myocardial ischemia tolerance in the newborn rat involving opioid receptors and mitochondrial K+ channels. Anat Rec A Discov Mol Cell Evol Biol 2006, 288:297-303.
13. Ogata T, Yamasaki Y. Scanning electron-microscopic studies on the three-dimensional structure of mitochondria in the mammalian red, white and intermediate muscle fibres. Cell Tissue Res 1985, 241:251-256.
14. Ostadal B, Ostadalova I, Dhalla NS. Development of cardiac sensitivity to oxygen deficiency: comparative and ontogenetic aspects. Physiol Rev 1999, 79:635-659.
15. Rossi AM, Eppenberger HM, Volpe P, Cotrufo R, Wallimann T. Muscle-type MM creatine kinase is specifically bound to sarcoplasmic reticulum and can support Ca2+ uptake and regulate local ATP/ADP ratios. J Biol Chem 1990, 265:5258-5266.
16. Saks VA, Belikova YO, Kuznetsov AV. In vivo regulation of mitochondrial respiration in cardiomyocytes: specific restrictions for intracellular diffusion of ADP. Biochim Biophys Acta 1991, 1074:302-311.
17. Saks VA, Kaambre T, Sikk P, Eimre M, Orlova E, Paju K, Piirsoo A, Appaix F, Kay L, Regitz-Zagrosek V, Fleck E, Seppet E. Intracellular energetic units in red muscle cells. Biochem J 2001, 356:643-657.
18. Saks VA, Khuchua ZA, Vasilyeva EV, Belikova OYu, Kuznetsov AV. Metabolic compartmentation and substrate channelling in muscle cells. Role of coupled creatine kinases in in vivo regulation of cellular respiration: a synthesis. Mol Cell Biochem 1994, 133-134:155-192.
19. Schiaffino S, Reggiani C. Molecular diversity of myofibrillar proteins: gene regulation and functional significance. Physiol Rev 1996, 76:371-423.
20. Schroder EA, Wei Y, Satin J. The developing cardiac myocyte: maturation of excitability and excitation-contraction coupling. Ann N Y Acad Sci 2006, 1080:63-75.
21. Seppet EK, Eimre M, Anmann T, Seppet E, Peet N, Kaambre T, Paju K, Piirsoo A, Kuznetsov AV, Vendelin M, Gellerich FN, Zierz S, Saks VA. Intracellular energetic units in healthy and diseased hearts. Exp Clin Cardiol 2005, 10:173-183.
22. Seppet EK, Kaambre T, Sikk P, Tiivel T, Vija H, Tonkonogi M, Sahlin K, Kay L, Appaix F, Braun U, Eimre M, Saks VA. Functional complexes of mitochondria with Ca, MgATPases of myofibrils and sarcoplasmic reticulum in muscle cells. Biochim Biophys Acta 2001, 1504:379-395.
23. Skarka L, Bardova K, Brauner P, Flachs P, Jarkovska D, Kopecky J, Ostadal B. Expression of mitochondrial uncoupling protein 3 and adenine nucleotide translocase 1 genes in developing rat heart: putative involvement in control of mitochondrial membrane potential. J Mol Cell Cardiol 2003, 35:321-330.
24. Tanaka H, Sekine T, Nishimaru K, Shigenobu K. Role of sarcoplasmic reticulum in myocardial contraction of neonatal and adult mice. Comp Biochem Physiol A Mol Integr Physiol 1998, 120:431-438.
25. Tiivel T, Kadaya L, Kuznetsov A, Kaambre T, Peet N, Sikk P, Braun U, Ventura-Clapier R, Saks V, Seppet EK. Developmental changes in regulation of mitochondrial respiration by ADP and creatine in rat heart in vivo. Mol Cell Biochem 2000, 208:119-128.
26. Timohhina N, Guzun R, Tepp K, Monge C, Varikmaa M, Vija H, Sikk P, Kaambre T, Sackett D, Saks V. Direct measurement of energy fluxes from mitochondria into cytoplasm in permeabilized cardiac cells in situ: some evidence for mitochondrial interactosome. J Bioenerg Biomembr 2009, 41:259-275.
27. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 2002, 3:research0034.1-0034.II.
28. Veksler VI, Kuznetsov AV, Anflous K, Mateo P, van Deursen J, Wieringa B, Ventura-Clapier R. Muscle creatine kinase-deficient mice. II. Cardiac and skeletal muscles exhibit tissue-specific adaptation of the mitochondrial function. J Biol Chem 1995, 270:19921-19929.
29. Veksler VI, Kuznetsov AV, Sharov VG, Kapelko VI, Saks VA. Mitochondrial respiratory parameters in cardiac tissue: a novel method of assessment by using saponin-skinned fibres. Biochim Biophys Acta 1987, 892:191-196.
30. Ventura-Clapier R, Kuznetsov A, Veksler V, Boehm E, Anflous K. Functional coupling of creatine kinases in muscles: species and tissue specificity. Mol Cell Biochem 1998, 184:231-247.
31. Ventura-Clapier R, Kuznetsov AV, d'Albis A, van Deursen J, Wieringa B, Veksler VI. Muscle creatine kinase-deficient mice. I. Alterations in myofibrillar function. J Biol Chem 1995, 270:19914-19920.
32. Ventura-Clapier R, Veksler V. Myocardial ischemic contracture. Metabolites affect rigor tension development and stiffness. Circ Res 1994, 74:920-929.
33. Wallimann T, Eppenberger HM. Localization and function of M-line-bound creatine kinase. M-band model and creatine phosphate shuttle. Cell Muscle Motil 1985, 6:239-285.
34. Wallimann T, Wyss M, Brdiczka D, Nicolay K, Eppenberger HM. Intracellular compartmentation, structure and function of creatine kinase isoenzymes in tissues with high and fluctuating energy demands: the 'phosphocreatine circuit' for cellular energy homeostasis. Biochem J 1992, 281:21-40.
35. Wharton DC, Tzagoloff A. Cytochrome oxidase from beef heart mitochondria. Methods Enzymol 1967, 10:245-250.
36. Wilding JR, Joubert F, de Araujo C, Fortin D, Novotova M, Veksler V, Ventura-Clapier R. Altered energy transfer from mitochondria to sarcoplasmic reticulum after cytoarchitectural perturbations in mice hearts. J Physiol 2006, 575:191-200.