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

European Journal of Neuroscience

Volumn 15, Issue 10, 2002, Pages 1692-1706

  Jost, Carolina R ^a,b   Van der Zee, Catharina E E M ^a   In 't Zandt, Henricus J A ^a   Oerlemans, Frank ^a   Verheij, Michel ^a   Streijger, Femke ^a   Fransen, Jack ^a   Heerschap, Arend ^a   Cools, Alexander R ^a   Wieringa, Bé ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b LEIDEN UNIVERSITY   (Netherlands)

Author keywords

Brain creatine kinase deficient mice; Brain energy metabolism; Magnetic resonance spectroscopy; Phosphocreatine; Seizure development; Water maze spatial learning

Indexed keywords

ADENOSINE TRIPHOSPHATE; CREATINE KINASE; CREATINE KINASE B; CREATINE PHOSPHATE; PENTETRAZOLE; UNCLASSIFIED DRUG;

ANIMAL BEHAVIOR; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENERGY TRANSFER; ENZYME ACTIVITY; ENZYME LOCALIZATION; GENOTYPE; HABITUATION; HIPPOCAMPUS; IMMUNOCYTOCHEMISTRY; LEARNING; MALE; MAZE TEST; MEMORY; MOSSY FIBER; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OPEN FIELD BEHAVIOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEIZURE SUSCEPTIBILITY; TASK PERFORMANCE; ULTRASTRUCTURE;

ANIMALS; BEHAVIOR, ANIMAL; BRAIN; CONVULSANTS; CREATINE KINASE; CREATINE KINASE, BB FORM; DISEASE SUSCEPTIBILITY; ENERGY TRANSFER; EXPLORATORY BEHAVIOR; HABITUATION, PSYCHOPHYSIOLOGIC; ISOENZYMES; MAGNETIC RESONANCE SPECTROSCOPY; MALE; MAZE LEARNING; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MOSSY FIBERS, HIPPOCAMPAL; NEURONS; PENTYLENETETRAZOLE; PHOSPHORUS; SEIZURES; SPACE PERCEPTION; SWIMMING;

EID: 0036460110     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.2002.02001.x     Document Type: Article

References (73)

1. Bach, M.E., Barad, M., Son, H., Zhuo, M., Lu, Y.F., Shih, R., Mansuy, I., Hawkins, R.D. & Kandel, E.R. (1999) Age-related defects in spatial memory are correlated with defects in the late phase of hippocampal long-term potentiation in vitro and are attenuated by drugs that enhance the cAMP signaling pathway. Proc. Natl Acad. Sci. USA, 96, 5280-5285.
2. Barinaga, M. (1997) What makes brain neurons run? Science
3. Beal, M.F. (1992) Does impairment of energy metabolism result in excitotoxic neuronal death in neurodegenerative illnesses? Ann. Neurol., 31, 119-130.
4. Belliveau, J.W., Kennedy, D.N. Jr, McKinstry, R.C., Buchbinder, B.R., Weisskoff, R.M., Cohen, M.S., Vevea, J.M., Brady, T.J. & Rosen, B.R. (1991) Functional mapping of the human cortex by magnetic resonance imaging. Science, 254, 716-719.
5. Bessman, S.P. & Carpenter, C.L. (1985) The creatine-creatine phosphate energy shuttle. Annu. Rev. Biochem., 54, 831-862.
6. 31P magnetization transfer study. Magn. Reson. Med., 38, 551-557.
7. Chih, C.-P., Lipton, P. & Roberts, E.L. Jr (2001) Do active cerebral neurons really use lactate rather than glucose? Trends Neurosci., 24, 573-578.
8. Cools, A.R., Dierx, J., Coenders, C., Heeren, D., Ried, S., Jenks, B.G. & Ellenbroek, B. (1993) Apomorphine-susceptible and apomorphine-unsusceptible Wistar rats differ in novelty-induced changes in hippocampal dynorphin B expression and two-way active avoidance: A new key in the search for the role of the hippocampal-accumbens axis. Behav. Brain Res., 55, 213-221.
9. Crusio, W.E., Bertholet, J.-Y. & Schwegler, H. (1990) No correlations between spatial and non-spatial reference memory in a T-maze task and hippocampal mossy fibre distribution in the mouse. Behav. Brain Res., 41, 251-259.
10. Danscher, G. (1981) Histochemical demonstration of heavy metals. A revised version of the sulphide silver method suitable for both light and electron microscopy. Histochemistry, 71, 1-16.
11. De Groof, A.J.C., Oerlemans, F., Jost, C.R. & Wieringa, B. (2001) Changes in glycolytic network and mitochondrial design in creatine kinase deficient muscle. Muscle Nerve, 24, 1188-1196.
12. Deitmer, J.W. (2000) Glial strategy for metabolic shuttling and neuronal function. Bioessays, 22, 747-752.
13. DeLorey, T.M., Handforth, A., Anagnostaras, S.G., Homanics, G.E., Minassian, B.A., Asatourian, A., Fanselow, M.S., Delgado-Escueta, A., Ellison, G.D. & Olsen, R.W. (1998) Mice lacking the beta-3 subunit of the GABA-A receptor have the epilepsy phenotype and many of the behavioral characteristics of Angelman syndrome. J. Neurosci., 18, 8505-8514.
14. Dzeja, P.P., Zeleznikar, R.J. & Goldberg, N.D. (1996) Suppression of creatine kinase-catalyzed phosphotransfer results in increased phosphoryl transfer by adenylate kinase in intact skeletal muscle. J. Biol. Chem., 271, 12847- 12851.
15. Dzeja, P.P., Zeleznikar, R.J. & Goldberg, N.D. (1998) Adenylate kinase: Kinetic behavior in intact cells indicates it is integral to multiple cellular processes. Mol. Cell Biochem., 184, 169-182.
16. Erecinska, M. & Silver, I.A. (1994) Ions and energy in mammalian brain. Prog. Neurobiol., 43, 37-71.
17. Ferrante, R.J., Andreassen, O.A., Jenkins, B.G., Dedeoglu, A., Kuemmerle, S., Kubilus, J.K., Kaddurah-Daouk, R., Hersch, S.M. & Beal, M.F. (2000) Neuroprotective effects of creatine in a transgenic mouse model of Huntington's disease. J. Neurosci., 20, 4389-4397.
18. Fox, P.T., Raichle, M.E., Mintun, M.A. & Dence, C. (1988) Nonoxidative glucose consumption during focal physiologic neural activity
19. Friedman, D.L. & Perryman, M.B. (1991) Compartmentation of multiple forms of creatine kinase in the distal nephron of the rat kidney. J. Biol. Chem., 266, 22404-22410.
20. Gerlai, R. (1996) Gene-targeting studies of mammalian behavior: Is it the mutation or the background genotype? Trends Neurosci., 19, 177-181.
21. Hamburg, R.J., Friedman, D.L., Olson, E.N., Ma, T.S., Cortez, M.D., Goodman, C., Puleo, P.R. & Perryman, M.B. (1990) Muscle creatine kinase isoenzyme expression in adult human brain. J. Biol. Chem., 265, 6403-6409.
22. El Hamdi, G., de Vasconcelos, A.P., Vert, P. & Nehlig, A. (1992) An experimental model of generalized seizures for the measurement of local glucose utilization in the immature rat. I. Behavioral characterization and determination of lumped constant. Brain Res. Dev. Brain Res., 69, 233-242.
23. Hemmer, W., Zanolla, E., Furter-Graves, E.M., Eppenberger, H.M. & Wallimann, T. (1994) Creatine kinase isoenzymes in chicken cerebellum: Specific localization of brain-type creatine kinase in Bergmann glial cells and muscle-type creatine kinase in Purkinje neurons. Eur. J. Neurosci., 6, 538-549.
24. Hertz, L., Dringen, R., Schousboe, A. & Robinson, S.R. (1999) Astrocytes: glutamate producers for neurons. J. Neurosci. Res., 57, 417-428.
25. Hochachka, P.W. (1999) The metabolic implications of intracellular circulation. Proc. Natl Acad. Sci. USA, 96, 12233-12239.
26. Holtzman, D., Brown, M., O'Gorman, E., Allred, E. & Wallimann, T. (1998a) Brain ATP metabolism in hypoxia resistant mice fed guanidinopropionic acid. Dev. Neurosci., 20, 469-477.
27. Holtzman, D., Meyers, R., Khait, I. & Jensen, F. (1997) Brain creatine kinase reaction rates and reactant concentrations during seizures in developing rats. Epilepsy Res., 27, 7-11.
28. Holtzman, D., Togliatti, A., Khait, I. & Jensen, F. (1998b) Creatine increases survival and suppresses seizures in the hypoxic immature rat. Pediatr. Res., 44, 410-414.
29. Holtzman, D., Tsuji, M., Wallimann, T. & Hemmer, W. (1993) Functional maturation of creatine kinase in rat brain. Dev. Neurosci., 15, 261-270.
30. Ikonomidou, C. & Turski, L. (1996) Neurodegenerative disorders: Clues from glutamate and energy metabolism. Crit. Rev. Neurobiol., 10, 239-263.
31. Janssen, E., Dzeja, P.P., Oerlemans, F., Simonetti, A.W., Heerschap, A., Haan, A., Rush, P.S., Terjung, R.R., Wieringa, B. & Terzic, A. (2000) Adenylate kinase 1 gene deletion disrupts muscle energetic economy despite metabolic rearrangement. EMBO J., 19, 6371-6381.
32. Jeong, H., Tombor, B., Albert, R., Oltvai, Z.N. & Barabasi, A.L. (2000) The large-scale organization of metabolic networks. Nature, 407, 651-654.
33. Klivenyi, P., Ferrante, R.J., Matthews, R.T., Bogdanov, M.B., Klein, A.M., Andreassen, O.A., Mueller, G., Wermer, M., Kaddurah-Daouk, R. & Beal, M.F. (1999) Neuroprotective effects of creatine in a transgenic animal model of amyotrophic lateral sclerosis. Nat. Med., 5, 347-350.
34. Lipp, H.P. & Wolfer, D.P. (1998) Genetically modified mice and cognition. Curr. Opin. Neurobiol., 8, 272-280.
35. Magistretti, P.J., Pellerin, L., Rothman, D.L. & Shulman, R.G. (1999) Energy on demand. Science, 283, 496-497.
36. Manfredi, G. & Beal, M.F. (2000) The role of mitochondria in the pathogenesis of neurodegenerative diseases. Brain Pathol., 10, 462-472.
37. Manfredi, G. & Beal, M.F. (2000) The role of mitochondria in the pathogenesis of neurodegenerative diseases. Brain Pathol., 10, 462-472.
38. Matthews, R.T., Ferrante, R.J., Klivenyi, P., Yang, L., Klein, A.M., Mueller, G., Kaddurah-Daouk, R. & Beal, M.F. (1999) Creatine and cyclocreatine attenuate MPTP neurotoxicity. Exp. Neurol., 157, 142-149.
39. Matthews, R.T., Yang, L., Jenkins, B.G., Ferrante, R.J., Rosen, B.R., Kaddurah-Daouk, R. & Beal, M.F. (1998) Neuroprotective effects of creatine and cyclocreatine in animal models of Huntington's disease. J. Neurosci., 18, 156-163.
40. Mayford, M. & Kandel, E.R. (1999) Genetic approaches to memory storage. Trends Genet., 15, 463-470.
41. Mekhfi, H., Veksler, V., Mateo, P., Maupoil, V., Rochette, L. & Ventura-Clapier, R. (1996) Creatine kinase is the main target of reactive oxygen species in cardiac myofibrils. Circ. Res., 78, 1016-1027.
42. O'Gorman, E., Beutner, G., Wallimann, T. & Brdiczka, D. (1996) Differential effects of creatine depletion on the regulation of enzyme activities and on creatine-stimulated mitochondrial respiration in skeletal muscle, heart, and brain. Biochim. Biophys. Acta, 1276, 161-170.
43. Pardon, M.-C., Perez-Diaz, F., Joubert, C. & Cohen-Salmon, C. (2000) Age-dependent effects of a chronic ultramild stress procedure on open-field behaviour in B6D2F1 female mice. Physiol. Behav., 70, 7-13.
44. Ramirez-Amaya, V., Balderas, I., Sandoval, J., Escobar, M.L. & Bermudez-Rattoni, F. (2001) Spatial long-term memory is related to mossy fiber synaptogenesis. J. Neurosci., 21, 7340-7348.
45. 2+ uptake and regulate local ATP/ADP ratios. J. Biol. Chem., 265, 5258-5266.
46. Roullet, P. & Lassalle, J.M. (1990) Genetic variation, hippocampal mossy fibres distribution, novelty reactions and spatial representation in mice. Behav. Brain Res., 41, 61-69.
47. Roullet, P. & Lassalle, J.M. (1992) Behavioural strategies, sensorial processes and hippocampal mossy fibre distribution in radial maze performance in mice. Behav. Brain Res., 48, 77-85.
48. Sakic, B., Szechtman, H., Talangbayan, H., Denburg, S.D., Carbotte, R.M. & Denburg, J.A. (1994) Disturbed emotionality in autoimmune MRL-lpr mice. Physiol. Behav., 56, 609-617.
49. Sauter, A. & Rudin, M. (1993) Determination of creatine kinase kinetic parameters in rat brain by NMR magnetization transfer. Correlation with brain function. J. Biol. Chem., 268, 13166-13171.
50. Schlattner, U. (1997) Adenylate kinase isoforms in higher plants. Recent Res. Devel. Phytochem., 1, 439-465.
51. Schroder, J.M. (1993) Neuropathy associated with mitochondrial disorders. Brain Pathol., 3, 177-190.
52. Schwegler, H. & Crusio, W.E. (1995) Correlations between radial-maze learning and structural variations of septum and hippocampus in rodents. Behav. Brain Res., 67, 29-41.
53. Schwegler, H., Crusio, W.E. & Brust, I. (1990) Hippocampal mossy fibers and radial-maze learning in the mouse: A correlation with spatial working memory but not with non-spatial reference memory. Neuroscience, 34, 293- 298.
54. +-ATPase on the apical membrane and the tubulovesicular system of parietal cells. Biochem. J., 311, 445-451.
55. Smith, C.D., Landrum, W., Carney, J.M., Landfield, P.W. & Avison, M.J. (1997) Brain creatine kinase with aging in F-344 rats: Analysis by saturation transfer magnetic resonance spectroscopy. Neurobiol. Aging, 18, 617-622.
56. Spooren, W.P.J.M., Lubbers, L., Jenks, B.G. & Cools, A.R. (1999) Variation in hippocampal dynorphin b-immunoreactive mossy fiber terminal fields of apomorphine-(un) susceptible rats. J. Chem. Neuroanat., 17, 59-64.
57. 2+ responses in muscles with combined mitochondrial and cytosolic creatine kinase deficiencies. Cell, 89, 93-103.
58. Steeghs, K., Oerlemans, F. & Wieringa, B. (1995) Mice deficient in ubiquitous mitochondrial creatine kinase are viable and fertile. Biochim. Biophys. Acta, 1230, 130-138.
59. Stockler, S., Isbrandt, D., Hanefeld, F., Schmidt, B. & von Figura, K. (1996) Guanidinoacetate methyltransferase deficiency: the first inborn error of creatine metabolism in man. Am. J. Hum. Genet., 58, 914-922.
60. Tchernichovski, O. & Golani, I. (1995) A phase plane representation of rat exploratory behavior. J. Neurosci. Meth, 62, 21-27.
61. Tsacopoulos, M. & Magistretti, P.J. (1996) Metabolic coupling between glia and neurons. J. Neurosci., 16, 877-885.
62. Tsuji, M., Allred, E., Jensen, F. & Holtzman, D. (1995) Phosphocreatine and ATP regulation in the hypoxic developing rat brain. Dev. Brain Res., 85, 192-200.
63. Van der Zee, C.E.E.M., Rashid, K., Le, K., Moore, K.-A., Stanisz, J., Diamond, J., Racine, R.J. & Fahnestock, M. (1995) Intraventricular administration of antibodies to nerve growth factor retards kindling and blocks mossy fiber sprouting in adult rats. J. Neurosci., 15, 5316-5323.
64. van Deursen, J., Heerschap, A., Oerlemans, F., Ruitenbeek, W., Jap, P.H., Ter Laak, H. & Wieringa, B. (1993) Skeletal muscle of mice deficient in muscle creatine kinase lack burst activity. Cell, 74, 621-631.
65. van Deursen, J. & Wieringa, B. (1994) Approaching the multifaceted nature of energy metabolism: Inactivation of the cytosolic creatine kinases via homologous recombination in mouse embryonic stem cells. Mol. Cell Biochem., 133-134, 263-274.
66. Wallace, D.C. (1999) Mitochondrial diseases in man and mouse. Science, 283, 1482-1488.
67. Wallimann, T., Wyss, M., Brdiczka, D., Nicolay, K. & Eppenberger, H.M. (1992) Intracellular compartmentation, structure and function of creatine kinase isoenzymes in tissues with high and fluctuating energy demands: the 'phospho-creatine circuit' for cellular energy homeostasis. Biochem. J., 281, 21-40.
68. A receptor mRNA levels and GABA stimulation of benzodiazepine binding with no effect on benzodiazepine binding site density. J. Pharmacol. Exp. Ther., 289, 1626-1633.
69. Wong-Riley, M.T. (1989) Cytochrome oxidase: An endogenous metabolic marker for neuronal activity. Trends Neurosci., 12, 94-101.
70. Wu, K., Aoki, C., Elste, A., Rogalski-Wilk, A.A. & Siekevitz, P. (1997) The synthesis of ATP by glycolytic enzymes in the postsynaptic density and the effect of endogenously generated nitric oxide. Proc. Natl Acad. Sci. USA, 94, 13273-13278.
71. Wyss, M. & Kaddurah-Daouk, R. (2000) Creatine and creatine metabolism. Physiol. Rev., 80, 1107-1213.
72. 31P MR-spectroscopy and -imaging reveal changes in metabolite levels and morphology of creatine kinase (CK) -deficient mouse brain. ISBN 90-64642054 Thesis book, Chpt. 7, University of Nijmegen, The Netherlands.
73. In 't Zandt, H.J.A., Klomp, D.W.J., Oerlemans, F., Wieringa, B., Hilbers, C.W. & Heerschap, A. (2000) Proton MR spectroscopy of wildtype and creatine deficient mouse skeletal muscle: Dipole-dipole coupling effects and postmortem changes. Magn. Res. Med., 43, 517-524.