Advertisement

Amino Acids

, Volume 48, Issue 8, pp 1751–1774 | Cite as

Cellular compartmentation of energy metabolism: creatine kinase microcompartments and recruitment of B-type creatine kinase to specific subcellular sites

  • Uwe Schlattner
  • Anna Klaus
  • Sacnicte Ramirez Rios
  • Rita Guzun
  • Laurence Kay
  • Malgorzata Tokarska-Schlattner
Invited Review
Part of the following topical collections:
  1. Creatine

Abstract

There is an increasing body of evidence for local circuits of ATP generation and consumption that are largely independent of global cellular ATP levels. These are mostly based on the formation of multiprotein(-lipid) complexes and diffusion limitations existing in cells at different levels of organization, e.g., due to the viscosity of the cytosolic medium, macromolecular crowding, multiple and bulky intracellular structures, or controlled permeability across membranes. Enzymes generating ATP or GTP are found associated with ATPases and GTPases enabling the direct fueling of these energy-dependent processes, and thereby implying that it is the local and not the global concentration of high-energy metabolites that is functionally relevant. A paradigm for such microcompartmentation is creatine kinase (CK). Cytosolic and mitochondrial isoforms of CK constitute a well established energy buffering and shuttling system whose functions are very much based on local association of CK isoforms with ATP-providing and ATP-consuming processes. Here we review current knowledge on the subcellular localization and direct protein and lipid interactions of CK isoforms, in particular about cytosolic brain-type CK (BCK) much less is known compared to muscle-type CK (MCK). We further present novel data on BCK, based on three different experimental approaches: (1) co-purification experiments, suggesting association of BCK with membrane structures such as synaptic vesicles and mitochondria, involving hydrophobic and electrostatic interactions, respectively; (2) yeast-two-hybrid analysis using cytosolic split-protein assays and the identifying membrane proteins VAMP2, VAMP3 and JWA as putative BCK interaction partners; and (3) phosphorylation experiments, showing that the cellular energy sensor AMP-activated protein kinase (AMPK) is able to phosphorylate BCK at serine 6 to trigger BCK localization at the ER, in close vicinity of the highly energy-demanding Ca2+ ATPase pump. Thus, membrane localization of BCK seems to be an important and regulated feature for the fueling of membrane-located, ATP-dependent processes, stressing again the importance of local rather than global ATP concentrations.

Keywords

Interactomics Local fueling Microcompartments Channeling Protein complexes 

Notes

Acknowledgments

We thank Drs. Nicolas Lentze and Daniel Auerbach (both formerly at Dual Systems, Dualsystems Biotech, Schlieren, Switzerland) for providing their proprietary Y2H systems, experimental support and initial discussions. We also thank present and former members of LBFA-Inserm U1055 involved in the studies presented here for their valuable contributions, notably Prof. emer. Valdur Saks. In particular we would like to thank Prof. emer. Theo Wallimann (Zurich, Switzerland) for his long-lasting encouragement and support, as well as the many fruitful discussions. Profs. T. Wallimann and R. Harris are also acknowledged for their editorial work. The work by the authors described herein was supported among others by the EU 6 and 7th framework programs (contract LSHM-CT-2004-005272 EXGENESIS, and contracts ANTHRAWES no. 041870 and ANTHRAPLUS no. 249202 to M.T.S.), the Agence Nationale de Recherche (France, “chaire d’excellence” to U.S., and SYBECAR no. RA0000C407), the Fondation pour la Recherche Médicale (France, to A.K.), and CONACYT (Mexico, contract no. 183832, to S.R.).

Compliance with ethical standards

This study does not involve human studies or animal experimentation.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Alekseev AE, Reyes S, Selivanov VA, Dzeja PP, Terzic A (2012) Compartmentation of membrane processes and nucleotide dynamics in diffusion-restricted cardiac cell microenvironment. J Mol Cell Cardiol 52(2):401–409PubMedCrossRefGoogle Scholar
  2. Alekseev AE, Guzun R, Reyes S, Pison C, Schlattner U, Selivanov VA, Cascante M (2016) Restrictions in ATP diffusion within sarcomeres can provoke ATP-depleted zones impairing exercise capacity in chronic obstructive pulmonary disease. Biochim Biophys Acta (in press)Google Scholar
  3. Aliev MK, van Dorsten FA, Nederhoff MG, van Echteld CJ, Veksler V, Nicolay K, Saks VA (1998) Mathematical model of compartmentalized energy transfer: its use for analysis and interpretation of 31P-NMR studies of isolated heart of creatine kinase deficient mice. Mol Cell Biochem 184(1–2):209–229PubMedCrossRefGoogle Scholar
  4. Ames A 3rd (2000) CNS energy metabolism as related to function. Brain Res Brain Res Rev 34(1–2):42–68PubMedCrossRefGoogle Scholar
  5. 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 (2006) 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 1757(12):1597–1606PubMedCrossRefGoogle Scholar
  6. Aranda B, Achuthan P, Alam-Faruque Y, Armean I, Bridge A, Derow C, Feuermann M, Ghanbarian AT, Kerrien S, Khadake J, Kerssemakers J, Leroy C, Menden M, Michaut M, Montecchi-Palazzi L, Neuhauser SN, Orchard S, Perreau V, Roechert B, van Eijk K, Hermjakob H (2010) The IntAct molecular interaction database in 2010. Nucleic Acids Res 38(Database issue):D525–D531PubMedCrossRefGoogle Scholar
  7. Bai J, Zhang J, Wu J, Shen L, Zeng J, Ding J, Wu Y, Gong Z, Li A, Xu S, Zhou J, Li G (2010) JWA regulates melanoma metastasis by integrin alphaVbeta3 signaling. Oncogene 29(8):1227–1237PubMedCrossRefGoogle Scholar
  8. Bandorowicz-Pikula J, Pikula S (1998) Annexins and ATP in membrane traffic: a comparison with membrane fusion machinery. Acta Biochim Pol 45(3):721–733PubMedGoogle Scholar
  9. Barbour RL, Ribaudo J, Chan SH (1984) Effect of creatine kinase activity on mitochondrial ADP/ATP transport. Evidence for a functional interaction. J Biol Chem 259(13):8246–8251PubMedGoogle Scholar
  10. Barrantes FJ, Braceras A, Caldironi HA, Mieskes G, Moser H, Toren EC Jr, Roque ME, Wallimann T, Zechel A (1985) Isolation and characterization of acetylcholine receptor membrane-associated (nonreceptor v2-protein) and soluble electrocyte creatine kinases. J Biol Chem 260(5):3024–3034PubMedGoogle Scholar
  11. Barry PH, Diamond JM (1984) Effects of unstirred layers on membrane phenomena. Physiol Rev 64(3):763–872PubMedGoogle Scholar
  12. Bessman SP, Carpenter CL (1985) The creatine-creatine phosphate energy shuttle. Ann Rev Biochem 54:831–862PubMedCrossRefGoogle Scholar
  13. Bessman SP, Geiger PJ (1981) Transport of energy in muscle: the phosphorylcreatine shuttle. Science 211(4481):448–452PubMedCrossRefGoogle Scholar
  14. Boehm E, Veksler V, Mateo P, Lenoble C, Wieringa B, Ventura-Clapier R (1998) Maintained coupling of oxidative phosphorylation to creatine kinase activity in sarcomeric mitochondrial creatine kinase-deficient mice. J Mol Cell Cardiol 30(5):901–912PubMedCrossRefGoogle Scholar
  15. Boissan M, Montagnac G, Shen Q, Griparic L, Guitton J, Romao M, Sauvonnet N, Lagache T, Lascu I, Raposo G, Desbourdes C, Schlattner U, Lacombe ML, Polo S, van der Bliek AM, Roux A, Chavrier P (2014) Membrane trafficking. Nucleoside diphosphate kinases fuel dynamin superfamily proteins with GTP for membrane remodeling. Science 344(6191):1510–1515PubMedPubMedCentralCrossRefGoogle Scholar
  16. Booth RF, Clark JB (1978) A rapid method for the preparation of relatively pure metabolically competent synaptosomes from rat brain. Biochem J 176(2):365–370PubMedPubMedCentralCrossRefGoogle Scholar
  17. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254PubMedCrossRefGoogle Scholar
  18. Braissant O, Henry H, Villard AM, Zurich MG, Loup M, Eilers B, Parlascino G, Matter E, Boulat O, Honegger P, Bachmann C (2002) Ammonium-induced impairment of axonal growth is prevented through glial creatine. J Neurosci 22(22):9810–9820PubMedGoogle Scholar
  19. Bruckner A, Polge C, Lentze N, Auerbach D, Schlattner U (2009) Yeast two-hybrid, a powerful tool for systems biology. Int J Mol Sci 10(6):2763–2788PubMedPubMedCentralCrossRefGoogle Scholar
  20. Burklen TS, Schlattner U, Homayouni R, Gough K, Rak M, Szeghalmi A, Wallimann T (2006) The creatine kinase/creatine connection to Alzheimer’s disease: CK-inactivation, APP-CK complexes and focal creatine deposits. J Biomed Biotechnol 3:35936Google Scholar
  21. Burklen TS, Hirschy A, Wallimann T (2007) Brain-type creatine kinase BB-CK interacts with the Golgi Matrix Protein GM130 in early prophase. Mol Cell Biochem 297(1–2):53–64PubMedCrossRefGoogle Scholar
  22. Carling D, Viollet B (2015) Beyond energy homeostasis: the expanding role of AMP-activated protein kinase in regulating metabolism. Cell Metab 21(6):799–804PubMedCrossRefGoogle Scholar
  23. Carre M, Andre N, Carles G, Borghi H, Brichese L, Briand C, Braguer D (2002) Tubulin is an inherent component of mitochondrial membranes that interacts with the voltage-dependent anion channel. J Biol Chem 277(37):33664–33669PubMedCrossRefGoogle Scholar
  24. Ceol A, Chatr Aryamontri A, Licata L, Peluso D, Briganti L, Perfetto L, Castagnoli L, Cesareni G (2010) MINT, the molecular interaction database: 2009 update. Nucleic Acids Res 38(Database issue):D532–D539PubMedCrossRefGoogle Scholar
  25. Chang EJ, Ha J, Oerlemans F, Lee YJ, Lee SW, Ryu J, Kim HJ, Lee Y, Kim HM, Choi JY, Kim JY, Shin CS, Pak YK, Tanaka S, Wieringa B, Lee ZH, Kim HH (2008) Brain-type creatine kinase has a crucial role in osteoclast-mediated bone resorption. Nat Med 14(9):966–972PubMedCrossRefGoogle Scholar
  26. Chen L, Roberts R, Friedman DL (1995) Expression of brain-type creatine kinase and ubiquitous mitochondrial creatine kinase in the fetal rat brain: evidence for a nuclear energy shuttle. J Comp Neurol 363(3):389–401PubMedCrossRefGoogle Scholar
  27. Chen C, Ko Y, Delannoy M, Ludtke SJ, Chiu W, Pedersen PL (2004) Mitochondrial ATP synthasome: three-dimensional structure by electron microscopy of the ATP synthase in complex formation with carriers for Pi and ADP/ATP. J Biol Chem 279(30):31761–31768PubMedCrossRefGoogle Scholar
  28. Chen H, Bai J, Ye J, Liu Z, Chen R, Mao W, Li A, Zhou J (2007) JWA as a functional molecule to regulate cancer cells migration via MAPK cascades and F-actin cytoskeleton. Cell Signal 19(6):1315–1327PubMedCrossRefGoogle Scholar
  29. Chen Z, Zhao TJ, Li J, Gao YS, Meng FG, Yan YB, Zhou HM (2011) Slow skeletal muscle myosin-binding protein-C (MyBPC1) mediates recruitment of muscle-type creatine kinase (CK) to myosin. Biochem J 436(2):437–445PubMedCrossRefGoogle Scholar
  30. Chen L, Wang J, Zhang YY, Yan SF, Neumann D, Schlattner U, Wang ZX, Wu JW (2012a) AMP-activated protein kinase undergoes nucleotide-dependent conformational changes. Nat Struct Mol Biol 19(7):716–718PubMedCrossRefGoogle Scholar
  31. Chen Z, Li J, Zhao TJ, Li XH, Meng FG, Mu H, Yan YB, Zhou HM (2012b) Metallothioneins protect cytosolic creatine kinases against stress induced by nitrogen-based oxidants. Biochem J 441(2):623–632PubMedCrossRefGoogle Scholar
  32. Chida K, Tsunenaga M, Kasahara K, Kohno Y, Kuroki T (1990) Regulation of creatine phosphokinase B activity by protein kinase C. Biochem Biophys Res Commun 173(1):346–350PubMedCrossRefGoogle Scholar
  33. Chin LS, Nugent RD, Raynor MC, Vavalle JP, Li L (2000) SNIP, a novel SNAP-25-interacting protein implicated in regulated exocytosis. J Biol Chem 275(2):1191–1200PubMedCrossRefGoogle Scholar
  34. de Groof AJ, Fransen JA, Errington RJ, Willems PH, Wieringa B, Koopman WJ (2002) The creatine kinase system is essential for optimal refill of the sarcoplasmic reticulum Ca2+ store in skeletal muscle. J Biol Chem 277(7):5275–5284PubMedCrossRefGoogle Scholar
  35. Debrincat MA, Zhang JG, Willson TA, Silke J, Connolly LM, Simpson RJ, Alexander WS, Nicola NA, Kile BT, Hilton DJ (2007) Ankyrin repeat and suppressors of cytokine signaling box protein asb-9 targets creatine kinase B for degradation. J Biol Chem 282(7):4728–4737PubMedCrossRefGoogle Scholar
  36. DeFuria RA, Ingwall JS, Fossel ET, Dygert MK (1980) The integration of isoenzymes for energy distribution. In: Jacobus WE, Ingwall JS (eds) Heart creatine kinase. Williams & Wilkins Co., Baltimore, pp 135–141Google Scholar
  37. Dhar-Chowdhury P, Malester B, Rajacic P, Coetzee WA (2007) The regulation of ion channels and transporters by glycolytically derived ATP. Cell Mol Life Sci 64(23):3069–3083PubMedCrossRefGoogle Scholar
  38. Dickmanns A, Kehlenbach RH, Fahrenkrog B (2015) Nuclear pore complexes and nucleocytoplasmic transport: from structure to function to disease. Int Rev Cell Mol Biol 320:171–233PubMedCrossRefGoogle Scholar
  39. Dix JA, Verkman AS (2008) Crowding effects on diffusion in solutions and cells. Ann Rev Biophys 37:247–263CrossRefGoogle Scholar
  40. Dong Y, Zhang M, Liang B, Xie Z, Zhao Z, Asfa S, Choi HC, Zou MH (2010) Reduction of AMP-activated protein kinase alpha2 increases endoplasmic reticulum stress and atherosclerosis in vivo. Circulation 121(6):792–803PubMedPubMedCentralCrossRefGoogle Scholar
  41. Dunant Y, Loctin F, Marsal J, Muller D, Parducz A, Rabasseda X (1988) Energy metabolism and quantal acetylcholine release: effects of botulinum toxin, 1-fluoro-2,4-dinitrobenzene, and diamide in the Torpedo electric organ. J Neurochem 50(2):431–439PubMedCrossRefGoogle Scholar
  42. Eder M, Schlattner U, Becker A, Wallimann T, Kabsch W, Fritz-Wolf K (1999) Crystal structure of brain-type creatine kinase at 1.41 A resolution. Protein Sci 8(11):2258–2269PubMedPubMedCentralCrossRefGoogle Scholar
  43. Ellington WR (2001) Evolution and physiological roles of phosphagen systems. Ann Rev Physiol 63:289–325CrossRefGoogle Scholar
  44. Epand RF, Tokarska-Schlattner M, Schlattner U, Wallimann T, Epand RM (2007) Cardiolipin clusters and membrane domain formation induced by mitochondrial proteins. J Mol Biol 365(4):968–980PubMedCrossRefGoogle Scholar
  45. Fei X, Gu X, Fan S, Yang Z, Li F, Zhang C, Gong W, Mao Y, Ji C (2012) Crystal structure of Human ASB9-2 and substrate-recognition of CKB. Protein J 31(4):275–284PubMedCrossRefGoogle Scholar
  46. Friedhoff AJ, Lerner MH (1977) Creatine kinase isoenzyme associated with synaptosomal membrane and synaptic vesicles. Life Sci 20(5):867–873PubMedCrossRefGoogle Scholar
  47. Friedman DL, Roberts R (1992) Purification and localization of brain-type creatine kinase in sodium chloride transporting epithelia of the spiny dogfish, Squalus acanthias. J Biol Chem 267(6):4270–4276PubMedGoogle Scholar
  48. Funanage VL, Carango P, Shapiro IM, Tokuoka T, Tuan RS (1992) Creatine kinase activity is required for mineral deposition and matrix synthesis in endochondral growth cartilage. Bone Miner 17(2):228–236PubMedCrossRefGoogle Scholar
  49. Gazzaniga MS, Bizzi E, Black IB (2004) The cognitive neurosciences III, 3rd edn. MIT Press, CambridgeGoogle Scholar
  50. Gellerich FN, Schlame M, Bohnensack R, Kunz W (1987) Dynamic compartmentation of adenine nucleotides in the mitochondrial intermembrane space of rat-heart mitochondria. Biochim Biophys Acta 890(2):117–126PubMedCrossRefGoogle Scholar
  51. Gellerich FN, Wagner M, Kapischke M, Wicker U, Brdiczka D (1993) Effect of macromolecules on the regulation of the mitochondrial outer membrane pore and the activity of adenylate kinase in the inter-membrane space. Biochim Biophys Acta 1142(3):217–227PubMedCrossRefGoogle Scholar
  52. Gietz RD, Woods RA (2006) Yeast transformation by the LiAc/SS carrier DNA/PEG method. Methods Mol Biol 313:107–120PubMedGoogle Scholar
  53. Guerrero ML, Beron J, Spindler B, Groscurth P, Wallimann T, Verrey F (1997) Metabolic support of Na+ pump in apically permeabilized A6 kidney cell epithelia: role of creatine kinase. Am J Physiol 272(2 Pt 1):C697–C706PubMedGoogle Scholar
  54. Guo CW, Xiong S, Liu G, Wang YF, He QY, Zhang XE, Zhang ZP, Ge F, Kitazato K (2010) Proteomic analysis reveals novel binding partners of MIP-T3 in human cells. Proteomics 10(12):2337–2347PubMedCrossRefGoogle Scholar
  55. Guzun R, Saks V (2010) Application of the principles of systems biology and Wiener’s cybernetics for analysis of regulation of energy fluxes in muscle cells in vivo. Int J Mol Sci 11(3):982–1019PubMedPubMedCentralCrossRefGoogle Scholar
  56. Guzun R, Timohhina N, Tepp K, Monge C, Kaambre T, Sikk P, Kuznetsov AV, Pison C, Saks V (2009) Regulation of respiration controlled by mitochondrial creatine kinase in permeabilized cardiac cells in situ. Importance of system level properties. Biochim Biophys Acta 1787(9):1089–1105PubMedCrossRefGoogle Scholar
  57. Guzun R, Karu-Varikmaa M, Gonzalez-Granillo M, Kuznetsov AV, Michel L, Cottet-Rousselle C, Saaremae M, Kaambre T, Metsis M, Grimm M, Auffray C, Saks V (2011) Mitochondria-cytoskeleton interaction: distribution of beta-tubulins in cardiomyocytes and HL-1 cells. Biochim Biophys Acta 1807(4):458–469PubMedCrossRefGoogle Scholar
  58. Guzun R, Kaambre T, Bagur R, Grichine A, Usson Y, Varikmaa M, Anmann T, Tepp K, Timohhina N, Shevchuk I, Chekulayev V, Boucher F, Dos Santos P, Schlattner U, Wallimann T, Kuznetsov AV, Dzeja P, Aliev M, Saks V (2015) Modular organization of cardiac energy metabolism: energy conversion, transfer and feedback regulation. Acta Physiol (Oxf) 213(1):84–106CrossRefGoogle Scholar
  59. Hanna-El-Daher L, Braissant O (2016) Creatine synthesis and exchanges between brain cells: What can be learned from human creatine deficiencies and various experimental models? Amino Acids (in press)Google Scholar
  60. Hardie DG, Ashford ML (2014) AMPK: regulating energy balance at the cellular and whole body levels. Physiology (Bethesda) 29(2):99–107Google Scholar
  61. Hardie DG, Carling D, Gamblin SJ (2011) AMP-activated protein kinase: also regulated by ADP? Trends Biochem Sci 36(9):470–477PubMedCrossRefGoogle Scholar
  62. Hardie DG, Schaffer BE, Brunet A (2016) AMPK: an energy-sensing pathway with multiple inputs and outputs. Trends Cell Biol 26(3):190–201PubMedCrossRefGoogle Scholar
  63. Hemmer W, Riesinger I, Wallimann T, Eppenberger HM, Quest AF (1993) Brain-type creatine kinase in photoreceptor cell outer segments: role of a phosphocreatine circuit in outer segment energy metabolism and phototransduction. J Cell Sci 106(Pt 2):671–683PubMedGoogle Scholar
  64. Hemmer W, Furter-Graves EM, Frank G, Wallimann T, Furter R (1995) Autophosphorylation of creatine kinase: characterization and identification of a specifically phosphorylated peptide. Biochim Biophys Acta 1251(2):81–90PubMedCrossRefGoogle Scholar
  65. Holthuis JC, Ungermann C (2013) Cellular microcompartments constitute general suborganellar functional units in cells. Biol Chem 394(2):151–161PubMedCrossRefGoogle Scholar
  66. Hornemann T, Stolz M, Wallimann T (2000) Isoenzyme-specific interaction of muscle-type creatine kinase with the sarcomeric M-line is mediated by NH2-terminal lysine charge-clamps. J Cell Biol 149(6):1225–1234PubMedPubMedCentralCrossRefGoogle Scholar
  67. Hornemann T, Kempa S, Himmel M, Hayess K, Furst DO, Wallimann T (2003) Muscle-type creatine kinase interacts with central domains of the M-band proteins myomesin and M-protein. J Mol Biol 332(4):877–887PubMedCrossRefGoogle Scholar
  68. Inoue K, Ueno S, Fukuda A (2004) Interaction of neuron-specific K+-Cl cotransporter, KCC2, with brain-type creatine kinase. FEBS Lett 564(1–2):131–135PubMedCrossRefGoogle Scholar
  69. Inoue K, Yamada J, Ueno S, Fukuda A (2006) Brain-type creatine kinase activates neuron-specific K+-Cl co-transporter KCC2. J Neurochem 96(2):598–608PubMedCrossRefGoogle Scholar
  70. Jacobus WE, Lehninger AL (1973) Creatine kinase of rat heart mitochondria. Coupling of creatine phosphorylation to electron transport. J Biol Chem 248(13):4803–4810PubMedGoogle Scholar
  71. Johnsson N, Varshavsky A (1994) Split ubiquitin as a sensor of protein interactions in vivo. Proc Natl Acad Sci USA 91(22):10340–10344PubMedPubMedCentralCrossRefGoogle Scholar
  72. Jost CR, Van Der Zee CE, In’t Zandt HJ, Oerlemans F, Verheij M, Streijger F, Fransen J, Heerschap A, Cools AR, Wieringa B (2002) Creatine kinase B-driven energy transfer in the brain is important for habituation and spatial learning behaviour, mossy fibre field size and determination of seizure susceptibility. Eur J Neurosci 15(10):1692–1706PubMedCrossRefGoogle Scholar
  73. Kagan VE, Jiang J, Huang Z, Tyurina YY, Desbourdes C, Cottet-Rousselle C, Dar HH, Verma M, Tyurin VA, Kapralov AA, Cheikhi A, Mao G, Stolz D, St Croix CM, Watkins S, Shen Z, Li Y, Greenberg ML, Tokarska-Schlattner M, Boissan M, Lacombe ML, Epand RM, Chu CT, Mallampalli RK, Bayir H, Schlattner U (2016) NDPK-D (NM23-H4)-mediated externalization of cardiolipin enables elimination of depolarized mitochondria by mitophagy. Cell Death Differ 23(7):1140–1151Google Scholar
  74. Kahle KT, Delpire E (2016) Kinase-KCC2 coupling: Cl− rheostasis, disease susceptibility, therapeutic target. J Neurophysiol 115(1):8–18PubMedCrossRefGoogle Scholar
  75. Kay L, Nicolay K, Wieringa B, Saks V, Wallimann T (2000) Direct evidence for the control of mitochondrial respiration by mitochondrial creatine kinase in oxidative muscle cells in situ. J Biol Chem 275(10):6937–6944PubMedCrossRefGoogle Scholar
  76. Kholodenko BN, Hancock JF, Kolch W (2010) Signalling ballet in space and time. Nat Rev Mol Cell Biol 11(6):414–426PubMedPubMedCentralCrossRefGoogle Scholar
  77. Kim HJ, Eom CY, Kwon J, Joo J, Lee S, Nah SS, Kim IC, Jang IS, Chung YH, Kim SI, Chung JH, Choi JS (2012) Roles of interferon-gamma and its target genes in schizophrenia: proteomics-based reverse genetics from mouse to human. Proteomics 12(11):1815–1829PubMedCrossRefGoogle Scholar
  78. Knull HR (1978) Association of glycolytic enzymes with particulate fractions from nerve endings. Biochim Biophys Acta 522(1):1–9PubMedCrossRefGoogle Scholar
  79. Kobayashi M, Hamanoue M, Masaki T, Furuta Y, Takamatsu K (2012) Hippocalcin mediates calcium-dependent translocation of brain-type creatine kinase (BB-CK) in hippocampal neurons. Biochem Biophys Res Commun 429(3–4):142–147PubMedCrossRefGoogle Scholar
  80. Korge P, Byrd SK, Campbell KB (1993) Functional coupling between sarcoplasmic-reticulum-bound creatine kinase and Ca2+-ATPase. Eur J Biochem 213(3):973–980PubMedCrossRefGoogle Scholar
  81. Kottke M, Adams V, Wallimann T, Nalam VK, Brdiczka D (1991) Location and regulation of octameric mitochondrial creatine kinase in the contact sites. Biochim Biophys Acta 1061(2):215–225PubMedCrossRefGoogle Scholar
  82. Kuiper JW (2009) Role of brain-type creatine kinase in cytoskeletal dynamics. Ph.D. thesis, Radboud University Nimjegen Medical Centre, NijmegenGoogle Scholar
  83. Kuiper JW, Pluk H, Oerlemans F, van Leeuwen FN, de Lange F, Fransen J, Wieringa B (2008) Creatine kinase-mediated ATP supply fuels actin-based events in phagocytosis. PLoS Biol 6(3):e51PubMedPubMedCentralCrossRefGoogle Scholar
  84. Kuiper JW, van Horssen R, Oerlemans F, Peters W, van Dommelen MM, te Lindert MM, ten Hagen TL, Janssen E, Fransen JA, Wieringa B (2009) Local ATP generation by brain-type creatine kinase (CK-B) facilitates cell motility. PLoS One 4(3):e5030PubMedPubMedCentralCrossRefGoogle Scholar
  85. Kuznetsov AV, Veksler V, Gellerich FN, Saks V, Margreiter R, Kunz WS (2008) Analysis of mitochondrial function in situ in permeabilized muscle fibers, tissues and cells. Nat Protoc 3(6):965–976PubMedCrossRefGoogle Scholar
  86. Lerner MH, Friedhoff AJ (1980) Characterization of a brain particulate bound form of creatine kinase. Life Sci 26(23):1969–1976PubMedCrossRefGoogle Scholar
  87. Lim L, Hall C, Leung T, Mahadevan L, Whatley S (1983) Neurone-specific enolase and creatine phosphokinase are protein components of rat brain synaptic plasma membranes. J Neurochem 41(4):1177–1182PubMedCrossRefGoogle Scholar
  88. Lin CI, Orlov I, Ruggiero AM, Dykes-Hoberg M, Lee A, Jackson M, Rothstein JD (2001) Modulation of the neuronal glutamate transporter EAAC1 by the interacting protein GTRAP3-18. Nature 410(6824):84–88PubMedCrossRefGoogle Scholar
  89. Lin YS, Chen CM, Soong BW, Wu YR, Chen HM, Yeh WY, Wu DR, Lin YJ, Poon PW, Cheng ML, Wang CH, Chern Y (2011a) Dysregulated brain creatine kinase is associated with hearing impairment in mouse models of Huntington disease. J Clin Invest 121(4):1519–1523PubMedPubMedCentralCrossRefGoogle Scholar
  90. Lin YS, Wang CH, Chern Y (2011b) Besides Huntington’s disease, does brain-type creatine kinase play a role in other forms of hearing impairment resulting from a common pathological cause? Aging (Albany NY) 3(6):657–662CrossRefGoogle Scholar
  91. Lin YS, Cheng TH, Chang CP, Chen HM, Chern Y (2013) Enhancement of brain-type creatine kinase activity ameliorates neuronal deficits in Huntington’s disease. Biochim Biophys Acta 1832(6):742–753PubMedCrossRefGoogle Scholar
  92. Linton JD, Holzhausen LC, Babai N, Song H, Miyagishima KJ, Stearns GW, Lindsay K, Wei J, Chertov AO, Peters TA, Caffe R, Pluk H, Seeliger MW, Tanimoto N, Fong K, Bolton L, Kuok DL, Sweet IR, Bartoletti TM, Radu RA, Travis GH, Zagotta WN, Townes-Anderson E, Parker E, Van der Zee CE, Sampath AP, Sokolov M, Thoreson WB, Hurley JB (2010) Flow of energy in the outer retina in darkness and in light. Proc Natl Acad Sci USA 107(19):8599–8604PubMedPubMedCentralCrossRefGoogle Scholar
  93. Lowe MT, Kim EH, Faull RL, Christie DL, Waldvogel HJ (2013) Dissociated expression of mitochondrial and cytosolic creatine kinases in the human brain: a new perspective on the role of creatine in brain energy metabolism. J Cereb Blood Flow Metab 33(8):1295–1306PubMedPubMedCentralCrossRefGoogle Scholar
  94. Luby-Phelps K (2000) Cytoarchitecture and physical properties of cytoplasm: volume, viscosity, diffusion, intracellular surface area. Int Rev Cytol 192:189–221PubMedCrossRefGoogle Scholar
  95. Mahajan VB, Pai KS, Lau A, Cunningham DD (2000) Creatine kinase, an ATP-generating enzyme, is required for thrombin receptor signaling to the cytoskeleton. Proc Natl Acad Sci USA 97(22):12062–12067PubMedPubMedCentralCrossRefGoogle Scholar
  96. Maldonado EN, Patnaik J, Mullins MR, Lemasters JJ (2010) Free tubulin modulates mitochondrial membrane potential in cancer cells. Cancer Res 70(24):10192–10201PubMedPubMedCentralCrossRefGoogle Scholar
  97. Mayinger P, Meyer DI (1993) An ATP transporter is required for protein translocation into the yeast endoplasmic reticulum. EMBO J 12(2):659–666PubMedPubMedCentralGoogle Scholar
  98. McLeish MJ, Kenyon GL (2005) Relating structure to mechanism in creatine kinase. Crit Rev Biochem Mol Biol 40(1):1–20PubMedCrossRefGoogle Scholar
  99. Mihaylova MM, Shaw RJ (2011) The AMPK signalling pathway coordinates cell growth, autophagy and metabolism. Nat Cell Biol 13(9):1016–1023PubMedPubMedCentralCrossRefGoogle Scholar
  100. Miller K, Halow J, Koretsky AP (1993) Phosphocreatine protects transgenic mouse liver expressing creatine kinase from hypoxia and ischemia. Am J Physiol 265(6 Pt 1):C1544–C1551PubMedGoogle Scholar
  101. Minton AP (2006) Macromolecular crowding. Curr Biol 16(8):R269–R271PubMedCrossRefGoogle Scholar
  102. Mironov SL (2009) Complexity of mitochondrial dynamics in neurons and its control by ADP produced during synaptic activity. Int J Biochem Cell Biol 41(10):2005–2014PubMedCrossRefGoogle Scholar
  103. Mockli N, Deplazes A, Hassa PO, Zhang Z, Peter M, Hottiger MO, Stagljar I, Auerbach D (2007) Yeast split-ubiquitin-based cytosolic screening system to detect interactions between transcriptionally active proteins. Biotechniques 42(6):725–730PubMedCrossRefGoogle Scholar
  104. Monge C, Beraud N, Kuznetsov AV, Rostovtseva T, Sackett D, Schlattner U, Vendelin M, Saks VA (2008) Regulation of respiration in brain mitochondria and synaptosomes: restrictions of ADP diffusion in situ, roles of tubulin, and mitochondrial creatine kinase. Mol Cell Biochem 318(1–2):147–165PubMedCrossRefGoogle Scholar
  105. Muller M, Moser R, Cheneval D, Carafoli E (1985) Cardiolipin is the membrane receptor for mitochondrial creatine phosphokinase. J Biol Chem 260(6):3839–3843PubMedGoogle Scholar
  106. Nicholls DG, Ferguson SJ (2013) Bioenergetics. Academic Press, New YorkGoogle Scholar
  107. Nie F, Wong-Riley MT (1996) Differential glutamatergic innervation in cytochrome oxidase-rich and -poor regions of the macaque striate cortex: quantitative EM analysis of neurons and neuropil. J Comp Neurol 369(4):571–590PubMedCrossRefGoogle Scholar
  108. Noskov SY, Rostovtseva TK, Bezrukov SM (2013) ATP transport through VDAC and the VDAC-tubulin complex probed by equilibrium and nonequilibrium MD simulations. Biochemistry 52(51):9246–9256PubMedCrossRefGoogle Scholar
  109. Noskov SY, Rostovtseva TK, Chamberlin AC, Teijido O, Jiang W, Bezrukov SM (2016) Current state of theoretical and experimental studies of the voltage-dependent anion channel (VDAC). Biochim Biophys Acta 1858(7):1778–1790Google Scholar
  110. Oakhill JS, Scott JW, Kemp BE (2012) AMPK functions as an adenylate charge-regulated protein kinase. Trends Endocrinol Metab 23(3):125–132PubMedCrossRefGoogle Scholar
  111. Ovadi J, Srere PA (2000) Macromolecular compartmentation and channeling. Int Rev Cytol 192:255–280PubMedCrossRefGoogle Scholar
  112. Peral MJ, Vazquez-Carretero MD, Ilundain AA (2010) Na+/Cl/creatine transporter activity and expression in rat brain synaptosomes. Neuroscience 165(1):53–60PubMedCrossRefGoogle Scholar
  113. Ponticos M, Lu QL, Morgan JE, Hardie DG, Partridge TA, Carling D (1998) Dual regulation of the AMP-activated protein kinase provides a novel mechanism for the control of creatine kinase in skeletal muscle. EMBO J 17(6):1688–1699PubMedPubMedCentralCrossRefGoogle Scholar
  114. Pucar D, Dzeja PP, Bast P, Juranic N, Macura S, Terzic A (2001) Cellular energetics in the preconditioned state: protective role for phosphotransfer reactions captured by 18O-assisted 31P NMR. J Biol Chem 276(48):44812–44819PubMedCrossRefGoogle Scholar
  115. Quest AF, Soldati T, Hemmer W, Perriard JC, Eppenberger HM, Wallimann T (1990) Phosphorylation of chicken brain-type creatine kinase affects a physiologically important kinetic parameter and gives rise to protein microheterogeneity in vivo. FEBS Lett 269(2):457–464PubMedCrossRefGoogle Scholar
  116. Raichle ME, Gusnard DA (2002) Appraising the brain’s energy budget. Proc Natl Acad Sci USA 99(16):10237–10239PubMedPubMedCentralCrossRefGoogle Scholar
  117. Ramirez Rios S, Lamarche F, Cottet-Rousselle C, Klaus A, Tuerk R, Thali R, Auchli Y, Brunisholz R, Neumann D, Barret L, Tokarska-Schlattner M, Schlattner U (2014) Regulation of brain-type creatine kinase by AMP-activated protein kinase: interaction, phosphorylation and ER localization. Biochim Biophys Acta 1837(8):1271–1283PubMedCrossRefGoogle Scholar
  118. Reifschneider NH, Goto S, Nakamoto H, Takahashi R, Sugawa M, Dencher NA, Krause F (2006) Defining the mitochondrial proteomes from five rat organs in a physiologically significant context using 2D blue-native/SDS-PAGE. J Proteome Res 5(5):1117–1132PubMedCrossRefGoogle Scholar
  119. Reiss NA, Kaye AM (1981) Identification of the major component of the estrogen-induced protein of rat uterus as the BB isozyme of creatine kinase. J Biol Chem 256(11):5741–5749PubMedGoogle Scholar
  120. Rossi AM, Eppenberger HM, Volpe P, Cotrufo R, Wallimann T (1990) 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 265(9):5258–5266PubMedGoogle Scholar
  121. Rostovtseva TK, Sheldon KL, Hassanzadeh E, Monge C, Saks V, Bezrukov SM, Sackett DL (2008) Tubulin binding blocks mitochondrial voltage-dependent anion channel and regulates respiration. Proc Natl Acad Sci USA 105(48):18746–18751PubMedPubMedCentralCrossRefGoogle Scholar
  122. Rual JF, Venkatesan K, Hao T, Hirozane-Kishikawa T, Dricot A, Li N, Berriz GF, Gibbons FD, Dreze M, Ayivi-Guedehoussou N, Klitgord N, Simon C, Boxem M, Milstein S, Rosenberg J, Goldberg DS, Zhang LV, Wong SL, Franklin G, Li S, Albala JS, Lim J, Fraughton C, Llamosas E, Cevik S, Bex C, Lamesch P, Sikorski RS, Vandenhaute J, Zoghbi HY, Smolyar A, Bosak S, Sequerra R, Doucette-Stamm L, Cusick ME, Hill DE, Roth FP, Vidal M (2005) Towards a proteome-scale map of the human protein-protein interaction network. Nature 437(7062):1173–1178PubMedCrossRefGoogle Scholar
  123. Ruggiero AM, Liu Y, Vidensky S, Maier S, Jung E, Farhan H, Robinson MB, Sitte HH, Rothstein JD (2008) The endoplasmic reticulum exit of glutamate transporter is regulated by the inducible mammalian Yip6b/GTRAP3-18 protein. J Biol Chem 283(10):6175–6183PubMedCrossRefGoogle Scholar
  124. Saks VA, Kuznetsov AV, Kupriyanov VV, Miceli MV, Jacobus WE (1985) Creatine kinase of rat heart mitochondria. The demonstration of functional coupling to oxidative phosphorylation in an inner membrane-matrix preparation. J Biol Chem 260(12):7757–7764PubMedGoogle Scholar
  125. Saks VA, Kuznetsov AV, Khuchua ZA, Vasilyeva EV, Belikova JO, Kesvatera T, Tiivel T (1995) Control of cellular respiration in vivo by mitochondrial outer membrane and by creatine kinase. A new speculative hypothesis: possible involvement of mitochondrial-cytoskeleton interactions. J Mol Cell Cardiol 27(1):625–645PubMedCrossRefGoogle Scholar
  126. Saks V, Dos Santos P, Gellerich FN, Diolez P (1998) Quantitative studies of enzyme-substrate compartmentation, functional coupling and metabolic channelling in muscle cells. Mol Cell Biochem 184(1–2):291–307PubMedCrossRefGoogle Scholar
  127. Saks VA, Kongas O, Vendelin M, Kay L (2000) Role of the creatine/phosphocreatine system in the regulation of mitochondrial respiration. Acta Physiol Scand 168(4):635–641PubMedCrossRefGoogle Scholar
  128. 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 (2001) Intracellular energetic units in red muscle cells. Biochem J 356(Pt 2):643–657PubMedPubMedCentralCrossRefGoogle Scholar
  129. Saks V, Favier R, Guzun R, Schlattner U, Wallimann T (2006) Molecular system bioenergetics: regulation of substrate supply in response to heart energy demands. J Physiol 577(Pt 3):769–777PubMedPubMedCentralCrossRefGoogle Scholar
  130. Saks V, Kaambre T, Guzun R, Anmann T, Sikk P, Schlattner U, Wallimann T, Aliev M, Vendelin M (2007) The creatine kinase phosphotransfer network: thermodynamic and kinetic considerations, the impact of the mitochondrial outer membrane and modelling approaches. Subcell Biochem 46:27–65PubMedCrossRefGoogle Scholar
  131. Saks V, Guzun R, Timohhina N, Tepp K, Varikmaa M, Monge C, Beraud N, Kaambre T, Kuznetsov A, Kadaja L, Eimre M, Seppet E (2010) Structure-function relationships in feedback regulation of energy fluxes in vivo in health and disease: mitochondrial interactosome. Biochim Biophys Acta 1797(6–7):678–697PubMedCrossRefGoogle Scholar
  132. Saks V, Kuznetsov AV, Gonzalez-Granillo M, Tepp K, Timohhina N, Karu-Varikmaa M, Kaambre T, Dos Santos P, Boucher F, Guzun R (2012) Intracellular energetic units regulate metabolism in cardiac cells. J Mol Cell Cardiol 52(2):419–436PubMedCrossRefGoogle Scholar
  133. Salin-Cantegrel A, Shekarabi M, Holbert S, Dion P, Rochefort D, Laganiere J, Dacal S, Hince P, Karemera L, Gaspar C, Lapointe JY, Rouleau GA (2008) HMSN/ACC truncation mutations disrupt brain-type creatine kinase-dependant activation of K+/Cl co-transporter 3. Hum Mol Genet 17(17):2703–2711PubMedCrossRefGoogle Scholar
  134. Schlattner U, Wallimann T (2000) Octamers of mitochondrial creatine kinase isoenzymes differ in stability and membrane binding. J Biol Chem 275(23):17314–17320PubMedCrossRefGoogle Scholar
  135. Schlattner U, Tokarska-Schlattner M, Wallimann T (2013) Metabolite channeling. In: Lennarz WJ, Lane MD (eds) Encyclopedia of biological chemistry, 2nd edn. Academic Press, New York, pp 80–85CrossRefGoogle Scholar
  136. Schlattner U, Forstner M, Eder M, Stachowiak O, Fritz-Wolf K, Wallimann T (1998) Functional aspects of the X-ray structure of mitochondrial creatine kinase: a molecular physiology approach. Mol Cell Biochem 184(1–2):125–140PubMedCrossRefGoogle Scholar
  137. Schlattner U, Eder M, Dolder M, Khuchua ZA, Strauss AW, Wallimann T (2000) Divergent enzyme kinetics and structural properties of the two human mitochondrial creatine kinase isoenzymes. Biol Chem 381(11):1063–1070PubMedCrossRefGoogle Scholar
  138. Schlattner U, Dolder M, Wallimann T, 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(51):48027–48030 PubMedGoogle Scholar
  139. Schlattner U, Reinhart C, Hornemann T, Tokarska-Schlattner M, Wallimann T (2002a) Isoenzyme-directed selection and characterization of anti-creatine kinase single chain Fv antibodies from a human phage display library. Biochim Biophys Acta 1579(2–3):124–132PubMedCrossRefGoogle Scholar
  140. Schlattner U, Mockli N, Speer O, Werner S, Wallimann T (2002b) Creatine kinase and creatine transporter in normal, wounded, and diseased skin. J Invest Dermatol 118(3):416–423PubMedCrossRefGoogle Scholar
  141. Schlattner U, Gehring F, Vernoux N, Tokarska-Schlattner M, Neumann D, Marcillat O, Vial C, Wallimann T (2004) C-terminal lysines determine phospholipid interaction of sarcomeric mitochondrial creatine kinase. J Biol Chem 279(23):24334–24342PubMedCrossRefGoogle Scholar
  142. Schlattner U, Tokarska-Schlattner M, Wallimann T (2006a) Mitochondrial creatine kinase in human health and disease. Biochim Biophys Acta 1762(2):164–180PubMedCrossRefGoogle Scholar
  143. Schlattner U, Tokarska-Schlattner M, Wallimann T (2006b) Molecular structure and function of mitochondrial creatine kinases. In: Vial C (ed) Creatine kinase. Nova Science Publishers, New York, pp 123–170Google Scholar
  144. Schlattner U, Tokarska-Schlattner M, Ramirez S, Bruckner A, Kay L, Polge C, Epand RF, Lee RM, Lacombe ML, Epand RM (2009) Mitochondrial kinases and their molecular interaction with cardiolipin. Biochim Biophys Acta 1788(10):2032–2047PubMedCrossRefGoogle Scholar
  145. Schlattner U, Tokarska-Schlattner M, Ramirez S, Tyurina YY, Amoscato AA, Mohammadyani D, Huang Z, Jiang J, Yanamala N, Seffouh A, Boissan M, Epand RF, Epand RM, Klein-Seetharaman J, Lacombe ML, Kagan VE (2013) Dual function of mitochondrial Nm23-H4 protein in phosphotransfer and intermembrane lipid transfer: a cardiolipin-dependent switch. J Biol Chem 288(1):111–121PubMedCrossRefGoogle Scholar
  146. Sekrecka-Belniak A, Balcerzak M, Buchet R, Pikula S (2010) Active creatine kinase is present in matrix vesicles isolated from femurs of chicken embryo: implications for bone mineralization. Biochem Biophys Res Commun 391(3):1432–1436PubMedCrossRefGoogle Scholar
  147. 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 (2005) Intracellular energetic units in healthy and diseased hearts. Exp Clin Cardiol 10(3):173–183PubMedPubMedCentralGoogle Scholar
  148. Shin JB, Streijger F, Beynon A, Peters T, Gadzala L, McMillen D, Bystrom C, Van der Zee CE, Wallimann T, Gillespie PG (2007) Hair bundles are specialized for ATP delivery via creatine kinase. Neuron 53(3):371–386PubMedPubMedCentralCrossRefGoogle Scholar
  149. Simionescu-Bankston A, Pichavant C, Canner JP, Apponi LH, Wang Y, Steeds C, Olthoff JT, Belanto JJ, Ervasti JM, Pavlath GK (2015) Creatine kinase B is necessary to limit myoblast fusion during myogenesis. Am J Physiol Cell Physiol 308(11):C919–C931PubMedPubMedCentralCrossRefGoogle Scholar
  150. Sistermans EA, de Kok YJ, Peters W, Ginsel LA, Jap PH, Wieringa B (1995a) Tissue- and cell-specific distribution of creatine kinase B: a new and highly specific monoclonal antibody for use in immunohistochemistry. Cell Tissue Res 280(2):435–446PubMedCrossRefGoogle Scholar
  151. Sistermans EA, Klaassen CH, Peters W, Swarts HG, Jap PH, De Pont JJ, Wieringa B (1995b) Co-localization and functional coupling of creatine kinase B and gastric H+/K+-ATPase on the apical membrane and the tubulovesicular system of parietal cells. Biochem J 311(Pt 2):445–451PubMedPubMedCentralCrossRefGoogle Scholar
  152. Smith TA (2000) Mammalian hexokinases and their abnormal expression in cancer. Br J Biomed Sci 57(2):170–178PubMedGoogle Scholar
  153. Squire LR, Zigmond MJ (2002) Fundamental neuroscience, 2nd edn. Academic Press, AmsterdamGoogle Scholar
  154. Srere PA (1991) Channeling: the pathway that cannot be beaten. J Theor Biol 152(1):23PubMedCrossRefGoogle Scholar
  155. Srere PA, Knull HR (1998) Location-location-location. Trends Biochem Sci 23(9):319–320PubMedCrossRefGoogle Scholar
  156. Stachowiak O, Schlattner U, Dolder M, Wallimann T (1998) Oligomeric state and membrane binding behaviour of creatine kinase isoenzymes: implications for cellular function and mitochondrial structure. Mol Cell Biochem 184(1–2):141–151PubMedCrossRefGoogle Scholar
  157. Stagljar I, Korostensky C, Johnsson N, te Heesen S (1998) A genetic system based on split-ubiquitin for the analysis of interactions between membrane proteins in vivo. Proc Natl Acad Sci USA 95(9):5187–5192PubMedPubMedCentralCrossRefGoogle Scholar
  158. Steeghs K, Benders A, Oerlemans F, de Haan A, Heerschap A, Ruitenbeek W, Jost C, van Deursen J, Perryman B, Pette D, Bruckwilder M, Koudijs J, Jap P, Veerkamp J, Wieringa B (1997) Altered Ca2+ responses in muscles with combined mitochondrial and cytosolic creatine kinase deficiencies. Cell 89(1):93–103PubMedCrossRefGoogle Scholar
  159. Steven AC, Baumeister W, Johnson IN, Perham RN (2016) Molecular biology of assemblies and machines. Garland Science, New YorkGoogle Scholar
  160. Stolz M, Wallimann T (1998) Myofibrillar interaction of cytosolic creatine kinase (CK) isoenzymes: allocation of N-terminal binding epitope in MM-CK and BB-CK. J Cell Sci 111(Pt 9):1207–1216PubMedGoogle Scholar
  161. Streijger F, Jost CR, Oerlemans F, Ellenbroek BA, Cools AR, Wieringa B, Van der Zee CE (2004) Mice lacking the UbCKmit isoform of creatine kinase reveal slower spatial learning acquisition, diminished exploration and habituation, and reduced acoustic startle reflex responses. Mol Cell Biochem 256–257(1–2):305–318PubMedCrossRefGoogle Scholar
  162. Swaminathan R, Bicknese S, Periasamy N, Verkman AS (1996) Cytoplasmic viscosity near the cell plasma membrane: translational diffusion of a small fluorescent solute measured by total internal reflection-fluorescence photobleaching recovery. Biophys J 71(2):1140–1151PubMedPubMedCentralCrossRefGoogle Scholar
  163. Tachikawa M, Fukaya M, Terasaki T, Ohtsuki S, Watanabe M (2004) Distinct cellular expressions of creatine synthetic enzyme GAMT and creatine kinases uCK-Mi and CK-B suggest a novel neuron-glial relationship for brain energy homeostasis. Eur J Neurosci 20(1):144–160PubMedCrossRefGoogle Scholar
  164. Tafelmeyer P, Johnsson N, Johnsson K (2004) Transforming a (beta/alpha) 8-barrel enzyme into a split-protein sensor through directed evolution. Chem Biol 11(5):681–689PubMedGoogle Scholar
  165. Takamori S, Holt M, Stenius K, Lemke EA, Gronborg M, Riedel D, Urlaub H, Schenck S, Brugger B, Ringler P, Muller SA, Rammner B, Grater F, Hub JS, De Groot BL, Mieskes G, Moriyama Y, Klingauf J, Grubmuller H, Heuser J, Wieland F, Jahn R (2006) Molecular anatomy of a trafficking organelle. Cell 127(4):831–846PubMedCrossRefGoogle Scholar
  166. Teng FY, Tang BL (2008) Cell autonomous function of Nogo and reticulons: the emerging story at the endoplasmic reticulum. J Cell Physiol 216(2):303–308PubMedCrossRefGoogle Scholar
  167. Timohhina N, Guzun R, Tepp K, Monge C, Varikmaa M, Vija H, Sikk P, Kaambre T, Sackett D, Saks V (2009) Direct measurement of energy fluxes from mitochondria into cytoplasm in permeabilized cardiac cells in situ: some evidence for Mitochondrial Interactosome. J Bioenerg Biomembr 41(3):259–275PubMedCrossRefGoogle Scholar
  168. Tokarska-Schlattner M, Dolder M, Gerber I, Speer O, Wallimann T, Schlattner U (2007) Reduced creatine-stimulated respiration in doxorubicin challenged mitochondria: particular sensitivity of the heart. Biochim Biophys Acta 1767(11):1276–1284PubMedCrossRefGoogle Scholar
  169. Turner DC, Wallimann T, Eppenberger HM (1973) A protein that binds specifically to the M-line of skeletal muscle is identified as the muscle form of creatine kinase. Proc Natl Acad Sci USA 70(3):702–705PubMedPubMedCentralCrossRefGoogle Scholar
  170. Veit M, Sollner TH, Rothman JE (1996) Multiple palmitoylation of synaptotagmin and the t-SNARE SNAP-25. FEBS Lett 385(1–2):119–123PubMedCrossRefGoogle Scholar
  171. Vendelin M, Kongas O, Saks V (2000) Regulation of mitochondrial respiration in heart cells analyzed by reaction-diffusion model of energy transfer. Am J Physiol Cell Physiol 278(4):C747–C764PubMedGoogle Scholar
  172. Venter G, Polling S, Pluk H, Venselaar H, Wijers M, Willemse M, Fransen JA, Wieringa B (2015) Submembranous recruitment of creatine kinase B supports formation of dynamic actin-based protrusions of macrophages and relies on its C-terminal flexible loop. Eur J Cell Biol 94(2):114–127PubMedCrossRefGoogle Scholar
  173. Verkman AS, Dix JA (1984) Effect of unstirred layers on binding and reaction kinetics at a membrane surface. Anal Biochem 142(1):109–116PubMedCrossRefGoogle Scholar
  174. Wallimann T, Hemmer W (1994) Creatine kinase in non-muscle tissues and cells. Mol Cell Biochem 133–134:193–220PubMedCrossRefGoogle Scholar
  175. Wallimann T, Turner DC, Eppenberger HM (1977) Localization of creatine kinase isoenzymes in myofibrils. I. Chicken skeletal muscle. J Cell Biol 75(2 Pt 1):297–317PubMedCrossRefGoogle Scholar
  176. Wallimann T, Schlosser T, Eppenberger HM (1984) Function of M-line-bound creatine kinase as intramyofibrillar ATP regenerator at the receiving end of the phosphorylcreatine shuttle in muscle. J Biol Chem 259(8):5238–5246PubMedGoogle Scholar
  177. Wallimann T, Walzthony D, Wegmann G, Moser H, Eppenberger HM, Barrantes FJ (1985) Subcellular localization of creatine kinase in Torpedo electrocytes: association with acetylcholine receptor-rich membranes. J Cell Biol 100(4):1063–1072PubMedCrossRefGoogle Scholar
  178. Wallimann T, Wyss M, Brdiczka D, Nicolay K, Eppenberger HM (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 281(Pt 1):21–40PubMedPubMedCentralCrossRefGoogle Scholar
  179. Wallimann T, Tokarska-Schlattner M, Neumann D, Epand RM, Epand RF, Hornemann T, Saks V, Agarkova I, Schlattner U (2007) The phosphocreatine circuit: molceular and cellular physiology of creatine kinases, sensitivity to free radicals, and enhancement by creatine supplementation. Molecular system bioenergetics: energy for life. WILEY-VCH Verlag GmbH & Co. KGaA edn, Weinheim, pp 195–264CrossRefGoogle Scholar
  180. Wallimann T, Tokarska-Schlattner M, Schlattner U (2011) The creatine kinase system and pleiotropic effects of creatine. Amino Acids 40(5):1271–1296PubMedPubMedCentralCrossRefGoogle Scholar
  181. Whittaker VP, Michaelson IA, Kirkland RJ (1964) The separation of synaptic vesicles from nerve-ending particles (‘synaptosomes’). Biochem J 90(2):293–303PubMedPubMedCentralCrossRefGoogle Scholar
  182. Wong AC, Velamoor S, Skelton MR, Thorne PR, Vlajkovic SM (2012) Expression and distribution of creatine transporter and creatine kinase (brain isoform) in developing and mature rat cochlear tissues. Histochem Cell Biol 137(5):599–613PubMedCrossRefGoogle Scholar
  183. Wong-Riley MT (1989) Cytochrome oxidase: an endogenous metabolic marker for neuronal activity. Trends Neurosci 12(3):94–101PubMedCrossRefGoogle Scholar
  184. Wong-Riley MT, Huang Z, Liebl W, Nie F, Xu H, Zhang C (1998) Neurochemical organization of the macaque retina: effect of TTX on levels and gene expression of cytochrome oxidase and nitric oxide synthase and on the immunoreactivity of Na+ K+ ATPase and NMDA receptor subunit I. Vision Res 38(10):1455–1477PubMedCrossRefGoogle Scholar
  185. Xu CJ, Klunk WE, Kanfer JN, Xiong Q, Miller G, Pettegrew JW (1996) Phosphocreatine-dependent glutamate uptake by synaptic vesicles. A comparison with atp-dependent glutamate uptake. J Biol Chem 271(23):13435–13440PubMedCrossRefGoogle Scholar
  186. Yan YB (2016) Creatine kinase in cell cycle regulation and cancer. Amino Acids (in press)Google Scholar
  187. Yang YC, Kao LS (2013) Regulation of sodium-calcium exchanger activity by creatine kinase. Adv Exp Med Biol 961:163–173PubMedCrossRefGoogle Scholar
  188. Yang YC, Fann MJ, Chang WH, Tai LH, Jiang JH, Kao LS (2010) Regulation of sodium-calcium exchanger activity by creatine kinase under energy-compromised conditions. J Biol Chem 285(36):28275–28285PubMedPubMedCentralCrossRefGoogle Scholar
  189. Zala D, Hinckelmann MV, Yu H, Lyra da Cunha MM, Liot G, Cordelieres FP, Marco S, Saudou F (2013) Vesicular glycolysis provides on-board energy for fast axonal transport. Cell 152(3):479–491PubMedCrossRefGoogle Scholar
  190. Zhao J, Schmieg FI, Simmons DT, Molloy GR (1994) Mouse p53 represses the rat brain creatine kinase gene but activates the rat muscle creatine kinase gene. Mol Cell Biol 14(12):8483–8492PubMedPubMedCentralCrossRefGoogle Scholar
  191. Zheng X, Bobich JA (1998) A sequential view of neurotransmitter release. Brain Res Bull 47(2):117–128PubMedCrossRefGoogle Scholar
  192. Zhou HX, Rivas G, Minton AP (2008) Macromolecular crowding and confinement: biochemical, biophysical, and potential physiological consequences. Ann Rev Biophys 37:375–397CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Wien 2016

Authors and Affiliations

  1. 1.Laboratory of Fundamental and Applied Bioenergetics (LBFA) and SFR Environmental and Systems Biology (BEeSy)University Grenoble AlpesGrenobleFrance
  2. 2.Inserm, U1055GrenobleFrance
  3. 3.Institut für medizinische DiagnostikBerlinGermany
  4. 4.Grenoble Institute of Neurosciences, Inserm U1209, University Grenoble AlpesGrenobleFrance

Personalised recommendations