Dissociated expression of mitochondrial and cytosolic creatine kinases in the human brain: A new perspective on the role of creatine in brain energy metabolism

Journal of Cerebral Blood Flow and Metabolism

Volumn 33, Issue 8, 2013, Pages 1295-1306

  Lowe, Matthew T J ^a   Kim, Eric H ^a   Faull, Richard L M ^a   Christie, David L ^a   Waldvogel, Henry J ^a  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

creatine kinase; energy metabolism; human brain; immunohistochemistry; phosphocreatine

Indexed keywords

ADENOSINE TRIPHOSPHATE; CREATINE; CREATINE KINASE BB; CREATINE KINASE ISOENZYME; CREATINE PHOSPHATE; GLIAL FIBRILLARY ACIDIC PROTEIN; MOLECULAR LAYER; UBIQUITOUS MITOCHONDRIAL CREATINE KINASE; UNCLASSIFIED DRUG;

ABDUCENS NUCLEUS; AMBIGUUS NUCLEUS; ARTICLE; ASTROCYTE; BRAIN; BRAIN CELL; BRAIN DEVELOPMENT; BRAIN METABOLISM; BRAIN MITOCHONDRION; BRAIN STEM; CAUDATE NUCLEUS; CELL ENERGY; CELL POPULATION; CELL TYPE; CEREBELLAR PEDUNCLE; CEREBELLUM CORTEX; CONTROLLED STUDY; CORPUS STRIATUM; CUNEATE NUCLEUS; CYTOSOL; DENTATE GYRUS; DORSAL RAPHE NUCLEUS; ENERGY METABOLISM; FACIAL NERVE NUCLEUS; GIGANTOCELLULAR RETICULAR NUCLEUS; GLOBUS PALLIDUS; GRACILE NUCLEUS; GRANULE CELL; HIPPOCAMPUS; HUMAN; HUMAN TISSUE; HYPOGLOSSAL NUCLEUS; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INFERIOR COLLICULUS; INFERIOR OLIVE; LOCUS CERULEUS; MEDIAL LEMNISCUS; MEDIAL LONGITUDINAL FASCICULUS; MEDIAN RAPHE NUCLEUS; MESENCEPHALIC TRIGEMINAL NUCLEUS; MOTONEURON NUCLEUS; MOTOR CORTEX; MUSCLE TISSUE; NERVE CELL; OCULOMOTOR NUCLEUS; PONTINE NUCLEUS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PURKINJE CELL; PYRAMIDAL TRACT; RED NUCLEUS; SOLITARY TRACT NUCLEUS; SPINAL CORD; SPINAL CORD DORSAL HORN; SPINAL CORD VENTRAL HORN; SPINOTHALAMIC TRACT; SUBSTANTIA NIGRA PARS COMPACTA; SUBTHALAMIC NUCLEUS; SUPERIOR COLLICULUS; THALAMUS; TRIGEMINAL NERVE; TROCHLEAR NUCLEUS; VAGUS NERVE; WESTERN BLOTTING; WHITE MATTER;

ADULT; AGED; AGED, 80 AND OVER; ANTIBODIES; BRAIN; BRAIN CHEMISTRY; CREATINE; CREATINE KINASE; CYTOSOL; ENERGY METABOLISM; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; IMMUNOHISTOCHEMISTRY; ISOENZYMES; MALE; MIDDLE AGED; MITOCHONDRIA; SPINAL CORD;

EID: 84881186756     PISSN: 0271678X     EISSN: 15597016     Source Type: Journal    
DOI: 10.1038/jcbfm.2013.84     Document Type: Article

References (40)

1. Wallimann T, Wyss M, Brdiczka D, Nicolay K, Eppenberger H. 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.
2. Urdal P, Urdal K, Stromme JH. Cytoplasmic creatine kinase isoenzymes quantitated in tissue specimens obtained at surgery. Clin Chem 1983; 29: 310-313.
3. Meyer RA, Sweeney HL, Kushmerick MJ. A simple analysis of the "phosphocreatine shuttle". Am J Physiol 1984; 246: C365-C377.
4. Stö ckler S, Schutz PW, Salomons GS. Cerebral creatine deficiency syndromes: clinical aspects, treatment and pathophysiology. In: Salomons G, Wyss M (eds) Creatine and Creatine Kinase in Health and Disease. Springer: Dordrecht, 2007, pp 149-166.
5. Andres RH, Ducray AD, Schlattner U, Wallimann T, Widmer HR. Functions and effects of creatine in the central nervous system. Brain Res Bull 2008; 76: 329-343.
6. Kim J, Amante DJ, Moody JP, Edgerly CK, Bordiuk OL, Smith K et al. Reduced creatine kinase as a central and peripheral biomarker in Huntington's disease. Biochim Biophys Acta 2010; 1802: 673-681.
7. Tachikawa M, Fukaya M, Terasaki T, Ohtsuki S, Watanabe M. 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 2004; 20: 144-160.
8. Waldvogel HJ, Curtis MA, Baer K, Rees MI, Faull RLM. Immunohistochemical staining of post-mortem adult human brain sections. Nat Protoc 2006; 1: 2719-2732.
9. Waldvogel HJ, Baer K, Allen KL, Rees MI, Faull RL. Glycine receptors in the striatum, globus pallidus, and substantia nigra of the human brain: an immunohistochemical study. J Comp Neurol 2007; 502: 1012-1029.
10. Wyss M, Kaddurah-Daouk R. Creatine and creatinine metabolism. Physiol Rev 2000; 80: 1107-1213.
11. Friedman DL, Roberts R. Compartmentation of brain-type creatine kinase and ubiquitous mitochondrial creatine kinase in neurons: evidence for a creatine phosphate energy shuttle in adult rat brain. J Comp Neurol 1994; 343: 500-511.
12. Iyengar MR. Creatine kinase as an intracellular regulator. J Muscle Res Cell Motil 1984; 5: 527-534.
13. Yamashita K, Yoshioka T. Profiles of creatine kinase isoenzyme compositions in single muscle fibres of different types. J Muscle Res Cell Motil 1991; 12: 37-44.
14. Saks VA, Ventura-Clapier R, Aliev MK. Metabolic control and metabolic capacity: two aspects of creatine kinase functioning in the cells. Biochim Biophys Acta 1996; 1274: 81-88.
15. Ogata T, Yamasaki Y. Scanning electron-microscopic studies on the threedimensional structure of mitochondria in the mammalian red, white and intermediate muscle fibers. Cell Tissue Res 1985; 241: 251-256.
16. Ames A. CNS energy metabolism as related to function. Brain Res Rev 2000; 34: 42-68.
17. Attwell D, Laughlin SB. An energy budget for signaling in the grey matter of the brain. J Cereb Blood Flow Metab 2001; 21: 1133-1145.
18. Pysh JJ, Khan T. Variations in mitochondrial structure and content of neurons and neuroglia in rat brain: an electron microscopic study. Brain Res 1972; 36: 1-18.
19. Wong-Riley MT. Cytochrome oxidase: an endogenous metabolic marker for neuronal activity. Trends Neurosci 1989; 12: 94-101.
20. Hertz L, Peng L, Dienel GA. Energy metabolism in astrocytes: high rate of oxidative metabolism and spatiotemporal dependence on glycolysis/ glycogenolysis. J Cereb Blood Flow Metab 2007; 27: 219-249.
21. Kauppinen RA, Enkvist K, Holopainen I, Akerman KE. Glucose deprivation depolarizes plasma membrane of cultured astrocytes and collapses transmembrane potassium and glutamate gradients. Neuroscience 1988; 26: 283-289.
22. Mertens-Strijthagen J, Lacremans-Pirsoul J, Baudoux G. Recovery potential in glucose deprived astrocytes. Neurosci Res 1996; 26: 133-139.
23. Yu AC, Gregory GA, Chan PH. Hypoxia-induced dysfunctions and injury of astrocytes in primary cell cultures. J Cereb Blood Flow Metab 1989; 9: 20-28.
24. Schlattner U, Tokarska-Schlattner M, Wallimann T. Mitochondrial creatine kinase in human health and disease. Biochim Biophys Acta 2006; 1762: 164-180.
25. Kay L, Nicolay K, Wieringa B, Saks V, Wallimann T. Direct evidence for the control of mitochondrial respiration by mitochondrial creatine kinase in oxidative muscle cells in situ. J Biol Chem 2000; 275: 6937-6944.
26. Li Z, Okamoto K, Hayashi Y, Sheng M. The importance of dendritic mitochondria in the morphogenesis and plasticity of spines and synapses. Cell 2004; 119: 873-887.
27. Degani H, Alger JR, Shulman RG, Petroff OA, Prichard JW. 31P magnetization transfer studies of creatine kinase kinetics in living rabbit brain. Magn Reson Med 1987; 5: 1-12.
28. Morris PG, Feeney J, Cox DW, Bachelard HS. 31P-saturation-transfer nuclearmagnetic-resonance measurements of phosphocreatine turnover in guinea-pig brain slices. Biochem J 1985; 227: 777-782.
29. Sweeney HL. The importance of the creatine kinase reaction: the concept of metabolic capacitance. Med Sci Sport Exer 1994; 26: 30-36.
30. Inoue K, Ueno S, Fukuda A. Interaction of neuron-specific K\+-Cl-cotransporter, KCC2, with brain-type creatine kinase. FEBS Lett 2004; 564: 131-135.
31. Inoue K, Yamada J, Ueno S, Fukuda A. Brain-type creatine kinase activates neuronspecific K\+-Cl-co-transporter KCC2. J Neurochem 2006; 96: 598-608.
32. Li H, Khirug S, Cai C, Ludwig A, Blaesse P, Kolikova J et al. KCC2 interacts with the dendritic cytoskeleton to promote spine development. Neuron 2007; 56: 1019-1033.
33. Wallimann T. 31P-NMR-measured creatine kinase reaction flux in muscle: a caveat! J Muscle Res Cell Motil 1996; 17: 177-181.
34. Buzsá ki G, Kaila K, Raichle M. Inhibition and brain work. Neuron 2007; 56: 771-783.
35. Hevner RF, Liu S, Wong-Riley MTT. A metabolic map of cytochrome oxidase in the rat brain: histochemical, densitometric and biochemical studies. Neuroscience 1995; 65: 313-342.
36. Beal MF, Brouillet E, Jenkins B, Henshaw R, Rosen B, Hyman BT. Age-dependent striatal excitotoxic lesions produced by the endogenous mitochondrial inhibitor malonate. J Neurochem 1993; 61: 1147-1150.
37. Lennie P. The cost of cortical computation. Curr Biol 2003; 13: 493-497.
38. Lowry JP, Fillenz M. Evidence for uncoupling of oxygen and glucose utilization during neuronal activation in rat striatum. J Physiol 1997; 498: 497-501.
39. Powers WJ, Videen TO, Markham J, McGee-Minnich L, Antenor-Dorsey JV, Hershey T et al. Selective defect of in vivo glycolysis in early Huntington's disease striatum. Proc Natl Acad Sci USA 2007; 104: 2945-2949.
40. Estrada-Sanchez AM, Montiel T, Massieu L. Glycolysis inhibition decreases the levels of glutamate transporters and enhances glutamate neurotoxicity in the R6/2 Huntington's disease mice. Neurochem Res 2010; 35: 1156-1163.