Compartmentalization in cardiomyocytes modulates creatine kinase and adenylate kinase activities.
adenylate kinase
cardiomyocytes
compartmentalization
creatine kinase
diffusion
signaling
Journal
FEBS letters
ISSN: 1873-3468
Titre abrégé: FEBS Lett
Pays: England
ID NLM: 0155157
Informations de publication
Date de publication:
07 Aug 2024
07 Aug 2024
Historique:
revised:
03
06
2024
received:
14
03
2024
accepted:
21
07
2024
medline:
8
8
2024
pubmed:
8
8
2024
entrez:
7
8
2024
Statut:
aheadofprint
Résumé
Intracellular molecules are transported by motor proteins or move by diffusion resulting from random molecular motion. Cardiomyocytes are packed with structures that are crucial for function, but also confine the diffusional spaces, providing cells with a means to control diffusion. They form compartments in which local concentrations are different from the overall, average concentrations. For example, calcium and cyclic AMP are highly compartmentalized, allowing these versatile second messengers to send different signals depending on their location. In energetic compartmentalization, the ratios of AMP and ADP to ATP are different from the average ratios. This is important for the performance of ATPases fuelling cardiac excitation-contraction coupling and mechanical work. A recent study suggested that compartmentalization modulates the activity of creatine kinase and adenylate kinase in situ. This could have implications for energetic signaling through, for example, AMP-activated kinase. It highlights the importance of taking compartmentalization into account in our interpretation of cellular physiology and developing methods to assess local concentrations of AMP and ADP to enhance our understanding of compartmentalization in different cell types.
Identifiants
pubmed: 39112921
doi: 10.1002/1873-3468.14994
doi:
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Eesti Teadusagentuur
ID : PRG1127
Informations de copyright
© 2024 The Author(s). FEBS Letters published by John Wiley & Sons Ltd on behalf of Federation of European Biochemical Societies.
Références
Sweeney HL and Holzbaur ELF (2018) Motor proteins. Cold Spring Harb Perspect Biol 10, a021931.
Shaw RM, Fay AJ, Puthenveedu MA, von Zastrow M, Jan YN and Jan LY (2007) Microtubule plus‐end‐tracking proteins target gap junctions directly from the cell interior to Adherens junctions. Cell 128, 547–560.
Uchida K, Scarborough EA and Prosser BL (2022) Cardiomyocyte microtubules: control of mechanics, transport, and remodeling. Annu Rev Physiol 84, 257–283.
Sommer MS and Schleiff E (2014) Protein targeting and transport as a necessary consequence of increased cellular complexity. Cold Spring Harb Perspect Biol 6, a016055.
Vendelin M, Eimre M, Seppet E, Peet N, Andrienko T, Lemba M, Engelbrecht J, Seppet EK and Saks VA (2004) Intracellular diffusion of adenosine phosphates is locally restricted in cardiac muscle. Mol Cell Biochem 256/257, 229–241.
Jayasinghe ID, Cannell MB and Soeller C (2009) Organization of ryanodine receptors, transverse tubules, and sodium‐calcium exchanger in rat myocytes. Biophys J 97, 2664–2673.
Christian P, Hayley B, Bernard DJ, Trafford AW and Ashraf K (2013) Three‐dimensional reconstruction of cardiac sarcoplasmic reticulum reveals a continuous network linking transverse‐tubules. Circ Res 113, 1219–1230.
Rog‐Zielinska EA, Moss R, Kaltenbacher W, Greiner J, Verkade P, Seemann G, Kohl P and Cannell MB (2021) Nano‐scale morphology of cardiomyocyte t‐tubule/sarcoplasmic reticulum junctions revealed by ultra‐rapid high‐pressure freezing and electron tomography. J Mol Cell Cardiol 153, 86–92.
Katz AM. Physiology of the Heart. 5th ed. Philadelphia, PA: Lippincott Williams & Wilkins; 2010.
Gautel M, Zuffardi O, Freiburg A and Labeit S (1995) Phosphorylation switches specific for the cardiac isoform of myosin binding protein‐C: a modulator of cardiac contraction? EMBO J 14, 1952–1960.
McNamara JW, Singh RR and Sadayappan S (2019) Cardiac myosin binding protein‐C phosphorylation regulates the super‐relaxed state of myosin. Proc Natl Acad Sci U S A 116, 11731–11736.
LeWinter MM and Granzier H (2010) Cardiac titin. Circulation 121, 2137–2145.
Frank D and Frey N (2011) Cardiac Z‐disc signaling network. J Biol Chem 286, 9897–9904.
Suga H (1990) Ventricular energetics. Physiol Rev 70, 247–277.
Boardman N, Hafstad AD, Larsen TS, Severson DL and Aasum E (2009) Increased O2 cost of basal metabolism and excitation‐contraction coupling in hearts from type 2 diabetic mice. Am J Physiol Heart Circ Physiol 296, H1373–H1379.
Stanley WC, Recchia FA and Lopaschuk GD (2005) Myocardial substrate metabolism in the normal and failing heart. Physiol Rev 85, 1093–1129.
Birkedal R, Shiels HA and Vendelin M (2006) Three‐dimensional mitochondrial arrangement in ventricular myocytes: from chaos to order. Am J Physiol Cell Physiol 291, C1148–C1158.
Branovets J, Sepp M, Kotlyarova S, Jepihhina N, Sokolova N, Aksentijevic D, Lygate CA, Neubauer S, Vendelin M and Birkedal R (2013) Unchanged mitochondrial organization and compartmentation of high‐energy phosphates in creatine‐deficient GAMT−/− mouse hearts. Am J Physiol Heart Circ Physiol 305, H506–H520.
Glancy B, Hartnell LM, Combs CA, Femnou A, Sun J, Murphy E, Subramaniam S and Balaban RS (2017) Power grid protection of the muscle mitochondrial reticulum. Cell Rep 19, 487–496.
Glancy B, Hartnell LM, Malide D, Yu ZX, Combs CA, Connelly PS, Subramaniam S and Balaban RS (2015) Mitochondrial reticulum for cellular energy distribution in muscle. Nature 523, 617–620.
Rog‐Zielinska EA, Johnston CM, O'Toole ET, Morphew M, Hoenger A and Kohl P (2016) Electron tomography of rabbit cardiomyocyte three‐dimensional ultrastructure. Prog Biophys Mol Biol 121, 77–84.
Robison P, Caporizzo MA, Ahmadzadeh H, Bogush AI, Chen CY, Margulies KB, Shenoy VB and Prosser BL (2016) Detyrosinated microtubules buckle and bear load in contracting cardiomyocytes. Science 352, aaf0659.
Vendelin M and Birkedal R (2008) Anisotropic diffusion of fluorescently labeled ATP in rat cardiomyocytes determined by raster image correlation spectroscopy. Am J Physiol Cell Physiol 295, C1302–C1315.
Jepihhina N, Beraud N, Sepp M, Birkedal R and Vendelin M (2011) Permeabilized rat Cardiomyocyte response demonstrates intracellular origin of diffusion obstacles. Biophys J 101, 2112–2121.
Illaste A, Laasmaa M, Peterson P and Vendelin M (2012) Analysis of molecular movement reveals Latticelike obstructions to diffusion in heart muscle cells. Biophys J 102, 739–748.
Birkedal R, Laasmaa M and Vendelin M (2014) The location of energetic compartments affects energetic communication in cardiomyocytes. Front Physiol 5, 376.
Birkedal R, Laasmaa M, Branovets J and Vendelin M (2022) Ontogeny of cardiomyocytes: ultrastructure optimization to meet the demand for tight communication in excitation–contraction coupling and energy transfer. Philos Trans R Soc Lond B Biol Sci 377, 20210321.
Ovádi J and Srere PA (1999) Macromolecular compartmentation and channeling. In International Review of Cytology (Walter H, Brooks DE and Srere PA, eds), pp. 255–280. Academic Press. (Microcompartmentation and Phase Separation in Cytoplasm; vol. 192). Available from: https://www.sciencedirect.com/science/article/pii/S007476960860529X
Maughan DW, Henkin JA and Vigoreaux JO (2005) Concentrations of glycolytic enzymes and other cytosolic proteins in the diffusible fraction of a vertebrate muscle proteome*. Mol Cell Proteomics 4, 1541–1549.
Sumegi B and Srere PA (1984) Complex I binds several mitochondrial NAD‐coupled dehydrogenases. J Biol Chem 259, 15040–15045.
Letts JA, Fiedorczuk K and Sazanov LA (2016) The architecture of respiratory supercomplexes. Nature 537, 644–648.
Letts JA and Sazanov LA (2017) Clarifying the supercomplex: the higher‐order organization of the mitochondrial electron transport chain. Nat Struct Mol Biol 24, 800–808.
Cramer P (2019) Organization and regulation of gene transcription. Nature 573, 45–54.
Stewart M (2019) Polyadenylation and nuclear export of mRNAs. J Biol Chem 294, 2977–2987.
Engel KL, Arora A, Goering R, Lo HYG and Taliaferro JM (2020) Mechanisms and consequences of subcellular RNA localization across diverse cell types. Traffic 21, 404–418.
Weis BL, Schleiff E and Zerges W (2013) Protein targeting to subcellular organelles via mRNA localization. Biochim Biophys Acta Mol Cell Res 1833, 260–273.
Gao C and Wang Y (2020) mRNA metabolism in cardiac development and disease: life after transcription. Physiol Rev 100, 673–694.
Paradis AN, Gay MS and Zhang L (2014) Binucleation of cardiomyocytes: the transition from a proliferative to a terminally differentiated state. Drug Discov Today 19, 602–609.
Scarborough EA, Uchida K, Vogel M, Erlitzki N, Iyer M, Phyo SA, Bogush A, Kehat I and Prosser BL (2021) Microtubules orchestrate local translation to enable cardiac growth. Nat Commun 12, 1547.
Lewis YE, Moskovitz A, Mutlak M, Heineke J, Caspi LH and Kehat I (2018) Localization of transcripts, translation, and degradation for spatiotemporal sarcomere maintenance. J Mol Cell Cardiol 116, 16–28.
Russell B, Wenderoth MP and Goldspink PH (1992) Remodeling of myofibrils: subcellular distribution of myosin heavy chain mRNA and protein. Am J Physiol 262, R339–R345.
Kelly CM, Martin JL, Coseno M and Previs MJ (2023) Visualization of cardiac thick filament dynamics in ex vivo heart preparations. J Mol Cell Cardiol 185, 88–98.
Bers DM (2002) Cardiac excitation‐contraction coupling. Nature 415, 198–205.
Bers DM and Shannon TR (2013) Calcium movements inside the sarcoplasmic reticulum of cardiac myocytes. J Mol Cell Cardiol 58, 59–66.
Wang Q and Michalak M (2020) Calsequestrin. Structure, function, and evolution. Cell Calcium 90, 102242.
Agrawal A, Wang K, Polonchuk L, Cooper J, Hendrix M, Gavaghan DJ, Mirams GR and Clerx M (2023) Models of the cardiac L‐type calcium current: a quantitative review. WIREs Mech Dis 15, e1581.
Bassani JW, Yuan W and Bers DM (1995) Fractional SR Ca release is regulated by trigger Ca and SR Ca content in cardiac myocytes. Am J Physiol 268, C1313–C1319.
Louch WE, Mørk HK, Sexton J, Strømme TA, Laake P, Sjaastad I and Sejersted OM (2006) T‐tubule disorganization and reduced synchrony of Ca2+ release in murine cardiomyocytes following myocardial infarction. J Physiol 574, 519–533.
Louch WE, Sejersted OM and Swift F (2010) There goes the neighborhood: pathological alterations in T‐tubule morphology and consequences for Cardiomyocyte Ca2+ handling. J Biomed Biotechnol 2010, 1–18.
Jones PP, MacQuaide N and Louch WE (2018) Dyadic plasticity in cardiomyocytes. Front Physiol 9, 1773.
Novotová M, Zahradníková A, Nichtová Z, Kováč R, Kráľová E, Stankovičová T, Zahradníková A and Zahradník I (2020) Structural variability of dyads relates to calcium release in rat ventricular myocytes. Sci Rep 10, 8076.
McCormack JG, Halestrap AP and Denton RM (1990) Role of calcium ions in regulation of mammalian intramitochondrial metabolism. Physiol Rev 70, 391–425.
Balaban RS (2002) Cardiac energy metabolism homeostasis: role of cytosolic calcium. J Mol Cell Cardiol 34, 1259–1271.
Ramesh V, Sharma VK, Sheu SS and Franzini‐Armstrong C (1998) Structural proximity of mitochondria to calcium release units in rat ventricular myocardium may suggest a role in Ca2+ sequestration. Ann N Y Acad Sci 853, 341–344.
Franzini‐Armstrong C (2007) ER‐mitochondria communication. How privileged? Physiology (Bethesda) 22, 261–268.
Williams GSB, Boyman L, Chikando AC, Khairallah RJ and Lederer WJ (2013) Mitochondrial calcium uptake. Proc Natl Acad Sci U S A 110, 10479–10486.
Molkentin JD (2000) Calcineurin and beyond. Circ Res 87, 731–738.
Parra V and Rothermel BA (2017) Calcineurin signaling in the heart: the importance of time and place. J Mol Cell Cardiol 103, 121–136.
Swulius MT and Waxham MN (2008) Ca2+/Calmodulin‐dependent Protein Kinases. Cell Mol Life Sci 65, 2637–2657.
Laude AJ and Simpson AWM (2009) Compartmentalized signalling: Ca2+ compartments, microdomains and the many facets of Ca2+ signalling. FEBS J 276, 1800–1816.
Li L, Stefan MI and Novère NL (2012) Calcium input frequency, duration and amplitude differentially modulate the relative activation of Calcineurin and CaMKII. PLoS One 7, e43810.
Bootman MD, Lipp P and Berridge MJ (2001) The organisation and functions of local Ca(2+) signals. J Cell Sci 114, 2213–2222.
Leroy J, Vandecasteele G and Fischmeister R (2018) Cyclic AMP signaling in cardiac myocytes. Curr Opin Physio 1, 161–171.
Kritzer MD, Li J, Dodge‐Kafka K and Kapiloff MS (2012) AKAPs: the architectural underpinnings of local cAMP signaling. J Mol Cell Cardiol 52, 351–358.
Ostrom KF, LaVigne JE, Brust TF, Seifert R, Dessauer CW, Watts VJ and Ostrom RS (2022) Physiological roles of mammalian transmembrane adenylyl cyclase isoforms. Physiol Rev 102, 815–857.
Dessauer CW (2009) Adenylyl cyclase–A‐kinase anchoring protein complexes: the next dimension in cAMP signaling. Mol Pharmacol 76, 935–941.
Michel JJC and Scott JD (2002) AKAP mediated signal transduction. Annu Rev Pharmacol Toxicol 42, 235–257.
Lin TY, Mai QN, Zhang H, Wilson E, Chien HC, Yee SW, Giacomini KM, Olgin JE and Irannejad R (2024) Cardiac contraction and relaxation are regulated by distinct subcellular cAMP pools. Nat Chem Biol 20, 62–73.
Faller KME, Atzler D, McAndrew DJ, Zervou S, Whittington HJ, Simon JN, Aksentijevic D, Ten Hove M, Choe C‐U, Isbrandt D et al. (2018) Impaired cardiac contractile function in arginine:glycine amidinotransferase knockout mice devoid of creatine is rescued by homoarginine but not creatine. Cardiovasc Res 114, 417–430.
Wallimann T, Wyss M, Brdiczka D, Nicolay K and Eppenberger H (1992) 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 1, 21–40.
Kammermeier H, Schmidt P and Jüngling E (1982) Free energy change of ATP‐hydrolysis: a causal factor of early hypoxic failure of the myocardium? J Mol Cell Cardiol 14, 267–277.
Tian R and Ingwall JS (1996) Energetic basis for reduced contractile reserve in isolated rat hearts. Am J Physiol 270, H1207–H1216.
Richards M, Lomas O, Jalink K, Ford KL, Vaughan‐Jones RD, Lefkimmiatis K and Swietach P (2016) Intracellular tortuosity underlies slow cAMP diffusion in adult ventricular myocytes. Cardiovasc Res 110, 395–407.
Conti M, Mika D and Richter W (2014) Cyclic AMP compartments and signaling specificity: role of cyclic nucleotide phosphodiesterases. J Gen Physiol 143, 29–38.
Katz LA, Swain JA, Portman MA and Balaban RS (1989) Relation between phosphate metabolites and oxygen consumption of heart in vivo. Am J Physiol 256, H265–H274.
Vendelin M, Kongas O and Saks V (2000) Regulation of mitochondrial respiration in heart cells analyzed by reaction‐diffusion model of energy transfer. Am J Physiol Cell Physiol 278, C747–C764.
Hardie DG, Carling D and Gamblin SJ (2011) AMP‐activated protein kinase: also regulated by ADP? Trends Biochem Sci 36, 470–477.
Kaasik A, Veksler V, Boehm E, Novotova M, Minajeva A and Ventura‐Clapier R (2001) Energetic crosstalk between organelles: architectural integration of energy production and utilization. Circ Res 89, 153–159.
Seppet EK, Kaambre T, Sikk P, Tiivel T, Vija H, Tonkonogi M, Sahlin K, Kay L, Appaix F, Braun U et al. (2001) Functional complexes of mitochondria with Ca,MgATPases of myofibrils and sarcoplasmic reticulum in muscle cells. Biochim Biophys Acta 1504, 379–395.
Saks VA, Kaambre T, Sikk P, Eimre M, Orlova E, Paju K, Piirsoo A, Appaix F, Kay L, Regitz‐Zagrosek V et al. (2001) Intracellular energetic units in red muscle cells. Biochem J 356, 643–657.
Saks VA, Kongas O, Vendelin M and Kay L (2000) Role of the creatine/phosphocreatine system in the regulation of mitochondrial respiration. Acta Physiol Scand 168, 635–641.
Xu KY and Becker LC (1998) Ultrastructural localization of glycolytic enzymes on sarcoplasmic reticulum vesticles. J Histochem Cytochem 46, 419–427.
Xu KY, Zweier JL and Becker LC (1995) Functional coupling between glycolysis and sarcoplasmic reticulum Ca2+ transport. Circ Res 77, 88–97.
Harrison GJ, van Wijhe MH, de Groot B, Dijk FJ, Gustafson LA and van Beek JHGM (2003) Glycolytic buffering affects cardiac bioenergetic signaling and contractile reserve similar to creatine kinase. Am J Physiol Heart Circ Physiol 285, H883–H890.
Boehm E, Ventura‐Clapier R, Mateo P, Lechène P and Veksler V (2000) Glycolysis supports calcium uptake by the sarcoplasmic reticulum in skinned ventricular Fibres of mice deficient in mitochondrial and cytosolic Creatine kinase. J Mol Cell Cardiol 32, 891–902.
Sepp M, Sokolova N, Jugai S, Mandel M, Peterson P and Vendelin M (2014) Tight coupling of Na+/K+‐ATPase with glycolysis demonstrated in permeabilized rat cardiomyocytes. PLoS One 9, e99413.
Simson P, Jepihhina N, Laasmaa M, Peterson P, Birkedal R and Vendelin M (2016) Restricted ADP movement in cardiomyocytes: cytosolic diffusion obstacles are complemented with a small number of open mitochondrial voltage‐dependent anion channels. J Mol Cell Cardiol 97, 197–203.
Kraft T, Hornemann T, Stolz M, Nier V and Wallimann T (2000) Coupling of creatine kinase to glycolytic enzymes at the sarcomeric I‐band of skeletal muscle: a biochemical study in situ. J Muscle Res Cell Motil 21, 691–703.
Wegmann G, Zanolla E, Eppenberger HM and Wallimann T (1992) In situ compartmentation of creatine kinase in intact sarcomeric muscle: the acto‐myosin overlap zone as a molecular sieve. J Muscle Res Cell Motil 13, 420–435.
Krause SM and Jacobus WE (1992) Specific enhancement of the cardiac myofibrillar ATPase by bound creatine kinase. J Biol Chem 267, 2480–2486.
Minajeva A, Ventura‐Clapier R and Veksler V (1996) Ca2+ uptake by cardiac sarcoplasmic reticulum ATPase in situ strongly depends on bound creatine kinase. Pflugers Arch 432, 904–912.
Grosse R, Spitzer E, Kupriyanov VV, Saks VA and Repke KR (1980) Coordinate interplay between (Na+ + K+)‐ATPase and creatine phosphokinase optimizes (Na+/K+)‐antiport across the membrane of vesicles formed from the plasma membrane of cardiac muscle cell. Biochim Biophys Acta 603, 142–156.
Crawford RM, Ranki HJ, Botting CH, Budas GR and Jovanovic A (2002) Creatine kinase is physically associated with the cardiac ATP‐sensitive K+ channel in vivo. FASEB J 16, 102–104.
Müller M, Moser R, Cheneval D and Carafoli E (1985) Cardiolipin is the membrane receptor for mitochondrial creatine phosphokinase. J Biol Chem 260, 3839–3843.
Schlattner U, Gehring F, Vernoux N, Tokarska‐Schlattner M, Neumann D, Marcillat O, Vial C and Wallimann T (2004) C‐terminal Lysines determine phospholipid interaction of sarcomeric mitochondrial creatine kinase. J Biol Chem 279, 24334–24342.
Rojo M, Hovius R, Demel R, Wallimann T, Eppenberger HM and Nicolay K (1991) Interaction of mitochondrial creatine kinase with model membranes a monolayer study. FEBS Lett 281, 123–129.
Karo J, Peterson P and Vendelin M (2012) Molecular dynamics simulations of Creatine kinase and adenine nucleotide translocase in mitochondrial membrane patch. J Biol Chem 287, 7467–7476.
Beyer K and Klingenberg M (1985) ADP/ATP carrier protein from beef heart mitochondria has high amounts of tightly bound cardiolipin, as revealed by phosphorus‐31 nuclear magnetic resonance. Biochemistry 24, 3821–3826.
Vendelin M, Lemba M and Saks VA (2004) Analysis of functional coupling: mitochondrial Creatine kinase and adenine nucleotide translocase. Biophys J 87, 696–713.
Schlattner U, Dolder M, Wallimann T and Tokarska‐Schlattner M (2001) Mitochondrial Creatine kinase and mitochondrial outer membrane Porin show a direct interaction that is modulated by calcium. J Biol Chem 276, 48027–48030.
Rojo M, Hovius R, Demel RA, Nicolay K and Wallimann T (1991) Mitochondrial creatine kinase mediates contact formation between mitochondrial membranes. J Biol Chem 266, 20290–20295.
Brdiczka DG, Zorov DB and Sheu SS (2006) Mitochondrial contact sites: their role in energy metabolism and apoptosis. Biochim Biophys Acta 1762, 148–163.
Branovets J, Soodla K, Vendelin M and Birkedal R (2023) Rat and mouse cardiomyocytes show subtle differences in creatine kinase expression and compartmentalization. PLoS One 18, e0294718.
Panayiotou C, Solaroli N and Karlsson A (2014) The many isoforms of human adenylate kinases. Int J Biochem Cell Biol 49, 75–83.
Carrasco AJ, Dzeja PP, Alekseev AE, Pucar D, Zingman LV, Abraham MR, Hodgson D, Bienengraeber M, Puceat M, Janssen E et al. (2001) Adenylate kinase phosphotransfer communicates cellular energetic signals to ATP‐sensitive potassium channels. Proc Natl Acad Sci U S A 98, 7623–7628.
Gellerich FN (1992) The role of adenylate kinase in dynamic compartmentation of adenine nucleotides in the mitochondrial intermembrane space. FEBS Lett 297, 55–58.
Jacobus WE and Lehninger AL (1973) Creatine kinase of rat heart mitochondria. Coupling of creatine phosphorylation to electron transport. J Biol Chem 248, 4803–4810.
Noma T (2005) Dynamics of nucleotide metabolism as a supporter of life phenomena. J Med Invest 52, 127–136.
Branovets J, Karro N, Barsunova K, Laasmaa M, Lygate CA, Vendelin M and Birkedal R (2021) Cardiac expression and location of hexokinase changes in a mouse model of pure creatine deficiency. Am J Physiol Heart Circ Physiol 320, H613–H629.
Bessman SP and Carpenter CL (1985) The Creatine‐Creatine phosphate energy shuttle. Annu Rev Biochem 54, 831–862.
Jacobus WE (1985) Theoretical support for the heart phosphocreatine energy transport shuttle based on the intracellular diffusion limited mobility of ADP. Biochem Biophys Res Commun 133, 1035–1041.
Meyer RA, Sweeney HL and Kushmerick MJ (1984) A simple analysis of the “phosphocreatine shuttle”. Am J Physiol Cell Physiol 246, C365–C377.
De Sousa E, Veksler V, Minajeva A, Kaasik A, Mateo P, Mayoux E, Hoerter J, Bigard X, Serrurier B and Ventura‐Clapier R (1999) Subcellular creatine kinase alterations. Implications in heart failure. Circ Res 85, 68–76.
Ingwall JS and Weiss RG (2004) Is the failing heart energy starved? Circ Res 95, 135–145.
Gupta A, Akki A, Wang Y, Leppo MK, Chacko VP, Foster DB, Caceres V, Shi S, Kirk JA, Su J et al. (2012) Creatine kinase–mediated improvement of function in failing mouse hearts provides causal evidence the failing heart is energy starved. J Clin Invest 122, 291–302.
Akki A, Su J, Yano T, Gupta A, Wang Y, Leppo MK, Chacko VP, Steenbergen C and Weiss RG (2012) Creatine kinase overexpression improves ATP kinetics and contractile function in postischemic myocardium. Am J Physiol Heart Circ Physiol 303, H844–H852.
Whittington HJ, Ostrowski PJ, McAndrew DJ, Cao F, Shaw A, Eykyn TR, Lake HA, Tyler J, Schneider JE, Neubauer S et al. (2018) Over‐expression of mitochondrial creatine kinase in the murine heart improves functional recovery and protects against injury following ischaemia–reperfusion. Cardiovasc Res 114, 858–869.
Wallimann T, Tokarska‐Schlattner M and Schlattner U (2011) The creatine kinase system and pleiotropic effects of creatine. Amino Acids 40, 1271–1296.
Beard DA (2005) A biophysical model of the mitochondrial respiratory system and oxidative phosphorylation. PLoS Comput Biol 1, e36.
Vendelin M, Hoerter JA, Mateo P, Soboll S, Gillet B and Mazet JL (2010) Modulation of energy transfer pathways between mitochondria and myofibrils by changes in performance of perfused heart. J Biol Chem 285, 37240–37250.
Rostovtseva TK, Sheldon KL, Hassanzadeh E, Monge C, Saks V, Bezrukov SM and Sackett DL (2008) Tubulin binding blocks mitochondrial voltage‐dependent anion channel and regulates respiration. Proc Natl Acad Sci U S A 105, 18746–18751.
Steeghs K, Oerlemans F, de Haan A, Heerschap A, Verdoodt L, de Bie M, Ruitenbeek W, Benders A, Jost C, van Deursen J et al. (1998) Cytoarchitectural and metabolic adaptations in muscles with mitochondrial and cytosolic creatine kinase deficiencies. Mol Cell Biochem 184, 183–194.
Crozatier B, Badoual T, Boehm E, Ennezat PV, Guenoun T, Su J, Veksler V, Hittinger L and Ventura‐Clapier R (2002) Role of creatine kinase in cardiac excitation‐contraction coupling: studies in creatine kinase‐deficient mice. FASEB J 16, 653–660.
Lygate CA (2021) The pitfalls of in vivo cardiac physiology in genetically modified mice – lessons learnt the hard way in the Creatine kinase system. Front Physiol 12, 700.
Lygate CA, Medway DJ, Ostrowski PJ, Aksentijevic D, Sebag‐Montefiore L, Hunyor I, Zervou S, Schneider JE and Neubauer S (2012) Chronic creatine kinase deficiency eventually leads to congestive heart failure, but severity is dependent on genetic background, gender and age. Basic Res Cardiol 107, 276–286.
Ten Hove M, Lygate CA, Fischer A, Schneider JE, Sang AE, Hulbert K, Sebag‐Montefiore L, Watkins H, Clarke K, Isbrandt D et al. (2005) Reduced inotropic reserve and increased susceptibility to cardiac ischemia/reperfusion injury in phosphocreatine‐deficient Guanidinoacetate‐N‐Methyltransferase–knockout mice. Circulation 111, 2477–2485.
Laasmaa M, Branovets J, Barsunova K, Karro N, Lygate CA, Birkedal R and Vendelin M (2021) Altered calcium handling in cardiomyocytes from arginine‐glycine amidinotransferase‐knockout mice is rescued by creatine. Am J Physiol Heart Circ Physiol 320, H805–H825.
Shibuya J, Matsumoto T, Takahashi K, Sugisawa K, Yasutomi N, Kawashima S, Naruse H, Tateishi J, Iwasaki T and Tozawa T (1992) The first report of a case with acute myocardial infarction showing familial deficiency of creatine kinase. Intern Med 31, 611–616.
Yamamichi H, Kasakura S, Yamamori S, Iwasaki R, Jikimoto T, Kanagawa S, Ohkawa J, Kumagai S and Koshiba M (2001) Creatine kinase gene mutation in a patient with muscle Creatine kinase deficiency. Clin Chem 47, 1967–1973.
Garland T, Gleeson TT, Aronovitz BA, Richardson CS and Dohm MR (1995) Maximal sprint speeds and muscle fiber composition of wild and laboratory house mice. Physiol Behav 58, 869–876.
Dzeja PP and Terzic A (2003) Phosphotransfer networks and cellular energetics. J Exp Biol 206, 2039–2047.
Dzeja PP, Hoyer K, Tian R, Zhang S, Nemutlu E, Spindler M and Ingwall JS (2011) Rearrangement of energetic and substrate utilization networks compensate for chronic myocardial creatine kinase deficiency. J Physiol 589, 5193–5211.
Pelosse M, Cottet‐Rousselle C, Bidan CM, Dupont A, Gupta K, Berger I and Schlattner U (2019) Synthetic energy sensor AMPfret deciphers adenylate‐dependent AMPK activation mechanism. Nat Commun 10, 1038.
Herzig S and Shaw RJ (2018) AMPK: guardian of metabolism and mitochondrial homeostasis. Nat Rev Mol Cell Biol 19, 121–135.
Gwinn DM, Shackelford DB, Egan DF, Mihaylova MM, Mery A, Vasquez DS, Turk BE and Shaw RJ (2008) AMPK phosphorylation of raptor mediates a metabolic checkpoint. Mol Cell 30, 214–226.
Habets DDJ, Coumans WA, Voshol PJ, den Boer MAM, Febbraio M, Bonen A, Glatz JFC and Luiken JJFP (2007) AMPK‐mediated increase in myocardial long‐chain fatty acid uptake critically depends on sarcolemmal CD36. Biochem Biophys Res Commun 355, 204–210.
Kurth‐Kraczek EJ, Hirshman MF, Goodyear LJ and Winder WW (1999) 5′ AMP‐activated protein kinase activation causes GLUT4 translocation in skeletal muscle. Diabetes 48, 1667–1671.
Holmes BF, Kurth‐Kraczek EJ and Winder WW (1999) Chronic activation of 5′‐AMP‐activated protein kinase increases GLUT‐4, hexokinase, and glycogen in muscle. J Appl Physiol 87, 1990–1995.
Dzamko N, Schertzer JD, Ryall JG, Steel R, Macaulay SL, Wee S, Chen ZP, Michell BJ, Oakhill JS, Watt MJ et al. (2008) AMPK‐independent pathways regulate skeletal muscle fatty acid oxidation. J Physiol 586, 5819–5831.
Park SH, Gammon SR, Knippers JD, Paulsen SR, Rubink DS and Winder WW (2002) Phosphorylation‐activity relationships of AMPK and acetyl‐CoA carboxylase in muscle. J Appl Physiol 92, 2475–2482.
Jager S, Handschin C, St‐Pierre J and Spiegelman BM (2007) AMP‐activated protein kinase (AMPK) action in skeletal muscle via direct phosphorylation of PGC‐1. Proc Natl Acad Sci U S A 104, 12017–12022.
Drake JC, Wilson RJ, Laker RC, Guan Y, Spaulding HR, Nichenko AS, Shen W, Shang H, Dorn MV, Huang K et al. (2021) Mitochondria‐localized AMPK responds to local energetics and contributes to exercise and energetic stress‐induced mitophagy. Proc Natl Acad Sci U S A 118, e2025932118.
Zong Y, Zhang CS, Li M, Wang W, Wang Z, Hawley SA, Ma T, Feng JW, Tian X, Qi Q et al. (2019) Hierarchical activation of compartmentalized pools of AMPK depends on severity of nutrient or energy stress. Cell Res 29, 460–473.
Carling D (2019) AMPK hierarchy: a matter of space and time. Cell Res 29, 425–426.
Piquereau J, Novotova M, Fortin D, Garnier A, Ventura‐Clapier R, Veksler V and Joubert F (2010) Postnatal development of mouse heart: formation of energetic microdomains. J Physiol (Lond) 588, 2443–2454.
Sokolova N, Vendelin M and Birkedal R (2009) Intracellular diffusion restrictions in isolated cardiomyocytes from rainbow trout. BMC Cell Biol 10, 90.
Karro N, Sepp M, Jugai S, Laasmaa M, Vendelin M and Birkedal R (2017) Metabolic compartmentation in rainbow trout cardiomyocytes: coupling of hexokinase but not creatine kinase to mitochondrial respiration. J Comp Physiol B 187, 103–116.
Li A, Gao M, Jiang W, Qin Y and Gong G (2020) Mitochondrial dynamics in adult Cardiomyocytes and heart diseases. Front Cell Dev Biol 8, 1555.
White J, Wang J, Fan Y, Dube DK, Sanger JW and Sanger JM (2018) Myofibril assembly in cultured mouse neonatal Cardiomyocytes. Anat Rec 301, 2067–2079.
Fischmeister R, Castro LRV, Abi‐Gerges A, Rochais F, Jurevičius J, Leroy J and Vandecasteele G (2006) Compartmentation of cyclic nucleotide signaling in the heart the role of cyclic nucleotide Phosphodiesterases. Circ Res 99, 816–828.
García KD, Shah T and García J (2004) Immunolocalization of type 2 inositol 1,4,5‐trisphosphate receptors in cardiac myocytes from newborn mice. Am J Physiol Cell Physiol 287, C1048–C1057.
Forghani P, Rashid A, Armand LC, Wolfson D, Liu R, Cho HC, Maxwell JT, Jo H, Salaita K and Xu C (2024) Simulated microgravity improves maturation of cardiomyocytes derived from human induced pluripotent stem cells. Sci Rep 14, 2243.