‘Hot Spots’ of creatine kinase localization in brain: Cerebellum, hippocampus and choroid plexus

Developmental Neuroscience

Volumn 18, Issue 5-6, 1996, Pages 542-554

  Kaldis, Philipp ^a   Hemmer, Wolfram ^a   Zanolla, Else ^a   Holtzman, David ^b   Wallimann, Theo ^a  

^a ETH ZURICH   (Switzerland)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Bergmann glia; Brain energy metabolism; Cerebellum; Creatine kinase; Epithelial cells of choroid plexus; Granular and pyramidal cells of hippocampus; Immunofluorescence microscopy; Purkinje neurons

Indexed keywords

BRAIN ENZYME; CREATINE KINASE; CREATINE KINASE ISOENZYME; MITOCHONDRIAL ENZYME;

ANIMAL CELL; BRAIN DEVELOPMENT; BRAIN METABOLISM; BRAIN NERVE CELL; CALCIUM CELL LEVEL; CEREBELLUM; CHICKEN; CHOROID PLEXUS; CONFERENCE PAPER; CYTOSOL; ENERGY METABOLISM; ENZYME LOCALIZATION; EPITHELIUM CELL; GLIA CELL; GRANULE CELL; HIPPOCAMPUS; IMMUNOFLUORESCENCE; IMMUNOFLUORESCENCE MICROSCOPY; NONHUMAN; PRIORITY JOURNAL; PURKINJE CELL;

ANIMALS; CEREBELLUM; CHICKENS; CHOROID PLEXUS; CREATINE KINASE; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; FLUORESCENT ANTIBODY TECHNIQUE; HIPPOCAMPUS; ISOENZYMES; MICROSCOPY, FLUORESCENCE; MITOCHONDRIA; RATS; TISSUE DISTRIBUTION;

EID: 0029842655     PISSN: 03785866     EISSN: 14219859     Source Type: Journal    
DOI: 10.1159/000111452     Document Type: Article

References (75)

1. Wallimann T. Hemmer W: Creatine kinase in non-muscle tissues and cells. Mol Cell Bio-chem 1994:133/134:193-220.
2. Wallimann T. Wyss M. Brdiezka D. Nicolay K. Eppenberger 11M: Intracellular compartmenta-tion. 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.
3. Wallimann T. Schlosser T, Eppenberger HM: Function of M-line bound creatine kinase as iniramyofibrillar ATP regenerator at the receiving end of the phosphorylcreatine shuttle in muscle. J Biol Chent 1984:259:5238-5246.
4. Krause SM. Jacobus WE: Specific enhancement of the cardiac myofibrillar ATPasc by bound creatine kinase. J Biol Chem 1992:267: 2480-2486.
5. Rossi AM. Eppenberger IIM. Volpe P. Cotrufo R. Wallimann T: Muscle-type MM creatine kinase is specifically bound to sarcoplasmic reticulum and can support Ca* uptake and regulate local ATP/ADP ratios. J Biol Chem 1990; 265:5258-5266.
6. Korge P. Byrd S. Campbell KB: Functional coupling between sarcoplasmatic-rcticulum-bound creatine kinase and Ca‘'-ATPase. Eur J Biochem 1993:213:973-980.
7. Blum H. Balschi JA. Johnson RG: Coupled in vivo activity of creatine phosphokina.se and the membrane-bound (Na\ K*)-ATPase in the resting and stimulated electric organ of the electric fish Narcine brasiUcnsis. J Biol Client 1991:266:10254-10259.
8. Jacobus WE. Lcltningcr AL: Creatine kinase of rat heart mitochondria. J Biol Chem 1973:248: 4803-4810.
9. Schlegel J. Wyss M. Eppenberger HM. Wallimann T: Functional studies with the octameric and dimeric form of mitochondrial creatine kinase. J Biol Chem 1990:265:9221-9227.
10. Payne RM. Haas RC. Strauss AW: Structural characterization and tissue-specific expression of the messenger RNAs encoding isoenzymes from two rat mitochondrial creatine kinase genes. Biochim Biophys Acta 1991:1089: 352-361.
11. Wyss M. Schlegel J. James P, Eppenberger HM. Wallimann T: Mitochondrial creatine kinase from chicken brain. J Biol Chem 1990: 265:15900-15908.
12. Schlegel J. Wyss M. Schürdt U. Sclmyder T. Quest A. Wegmann G. Eppenberger HM. Wallimann T: Mitochondrial creatine kinase front cardiac muscle and brain are two distinct isoenzymes but both form octameric molecules. J Biol Client 1988:263:16963-16969.
13. llossle JP. Schlegel J. Wegmann G. Wyss M. Böhlen P, Eppenberger HM. Wallimann T, Per-riard J-C: Distinct tissue-specific mitochondrial creatine kinases front chicken brain and striated muscle with a conserved CK framework. Biochem Biophys Res Commun 1988; 151:408-416.
14. Wyss M. Snteitink J. Wcvers RA. Wallimann T: Mitochondrial creatine kinase: A key enzyme of aerobic energy metabolism. Biochim Biophys Acta 1992; 1102:119-166.
15. Quest AFG. Eppenberger HM. Wallimann T: Purification of brain-type creatine kinase (B-CK) from several tissues of the chicken: B-CK subspecies. Enzyme 1989:41:33-42.
16. Quest AFG. Soldati T. Hemmer W. Perriard J C. Eppenberger HM. Wallimann T: Phosphorylation of chicken brain-type creatine kinase affects a physiologically important kinetic parameter and gives rise to protein micro-heterogeneity in vivo. FEBS Lett 1990:269: 457-464.
17. Hentnter W, Furter-Graves EM. Frank G. Wallimann T. Furter R: Autophosphorylation of creatine kinase: characterization and identification of a specifically pltosphorylatcd peptide. Biochim Biophys Acta 1995:1251: 81-90.
18. Kuzhikandathil EV. Molloy GR: Transcription of the brain creatine kinase gene in glial cells is modulated by cyclic AMP-dependent protein kinase. J Neurosci Res 1994:39:70-82.
19. Brand A. Richter-Landsberg C. Leibfritz D: Multinuclear NMR studies on the energy metabolism of glial and neuronal cells. Dev Neurosci 1993:15:289-298.
20. Manos P. Edmond J: Immunofluorescent analysis of creatine kinase in cultured astrocytes by conventional and confocal microscopy: A nuclear localization. J Comp Neurol 1992:326:273-282.
21. Molloy GR. Wilson CD. Bcnficld PA, deVellis J. Kunta S: Rat brain creatine kinase messenger RNA levels are high in primary cultures of brain astrocytes and oligodenrocytes and low in neurons. J Neurochcm 1992:59:1925-1932.
22. Manos P, Bryan GK, Edmond J: Creatine kinase activity in postnatal rat brain development and in cultured neurons, astrocytes, and oligodendrocytes. J Ncurochem 1991:56: 2101-2107.
23. Kato K, Suzuki F. Shimizu A. Shinoliara H, Semba R: Highly sensitive immunoassay for rat brain-type creatine kinase: Determination in isolated Purkinje cells. J Neurochcm 1986: 46:1783-1788.
24. Cadoux-Hudson TA, Blackledge MJ. Radda GK: Imaging of human brain creatine kinase activity in vivo. FASEB J 1989:3:2660-2665.
25. JIP nuclear magnetic resonance. Brain Res 1996:707:146-154.
26. Holtzman D. Mulkem R. Tsuji M. Cook C. Meyers R: Phosphocreatinc and creatine kinase systems in gray and white matter of the developing piglet brain. Dev Ncurosci 1996; 18:535-541.
27. 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.
28. Hemmer W. Zanolla E. Furier-Gravcs EM. Eppenberger HM. Wallimann T: Creatine kinase isoenzymes in chicken cerebellum: specific localization of brain-type CK in Bergmann glial cells and muscle-type CK in Purkinje neurons. Eur J Neurosci 1994;6:538-549.
29. Hemmer W. Wallimann T: Functional aspects of creatine kinase in brain. Dev Neurosci 1993; 15:249-260.
30. Sistermans EA. de Kok YJM, Peters W. Ginsel LA. Jap PHK. Wieringa B: Tissue- and cell-specific distribution of creatine kinase B: A new and highly specific monoclonal antibody for use in immunohistochcmistry. Cell Tissue Res 1995:280:435-446.
31. Ramirez O. Licea G: Rat brain MM and MB isoenzymes of creatine kinase. Exp Neurol 1982:77:225-229.
32. Hamburg RJ. Friedman DL, Olson EN. Ma TS. Cortez MD. Goodman C. Puelo PR. Perryman MB: Muscle creatine kinase isoenzyme expression in adult human brain. J Biol Chcm 1990;265:6403-6409.
33. Kaldis P: Mitochondrial creatine kinase isoenzymes: Structure/function-relationship. Swiss Federal Institute of Technology (ETH) Zürich. Switzerland 1994; PhD thesis. Diss. No. 10686.
34. Holtzman D, Tsuji M, Wallimann T. Hemmer W: Functional maturation of creatine kinase in rat brain. Dev Neurosci 1993; 15:261-270.
35. Hemmer W. Skarli M. Pcrriard J-C. Wallimann T: Effect of okadaic acid on protein phosphorylation patterns of chicken myogenic cells with special reference to creatine kinase. FEBS Lett 1993:327:35-40.
36. Schlegel J. Zurbriggcn B. Wegmann G. Wyss M. Eppenberger HM. Wallimann T: Native mitochondrial creatine kinase forms octamcric structures. I. Isolation of two interconvertible mitochondrial creatine kinase forms, dimeric and octamcric mitochondrial creatine kinase: Characterization, localization and structure-function relationships. J Biol Chcm 1988:263: 16942-16953.
37. Caravatti M. Perriard J-C. Eppenberger HM: Developmental regulation of creatine kinase isoenzymes in myogenic cultures from chicken. J Biol Client 1979;254:1388-1394.
38. Schneider WJ. Slaughter J. Goldstein JL. Anderson RGW. Capra JD. Brown MS: Use of antipeptidc antibodies to demonstrate external orientation of the NH.-terminusofthc low density lipoprotein receptor in the plasma membrane of fibroblasts. J Biol Chcm 1983:97: 1635-1640.
39. O'Farrell PZ. Goodman HM. O'Farrell PH: High resolution two-dimensional electrophoresis of basic as well as acidic proteins. Cell 1977:12:1133-1142.
40. Laemmli UK: Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970;227:680-685.
41. Kaldis P, Stolz M. Wyss M. Zanolla E. Rothcn-Rutishauser B, Vorherr T. Wallimann T: Identification of two distinctly localized mitochondrial creatine kinase isoenzymes in spermatozoa, Cell Sei 1996 (in press).
42. Rakic P: Neuron-glia relation ship during granule cell migration in developing cerebellar cortex: A Golgi and electron-microscopic study in Macacas rhesus. J Comp Neurol 1971:141: 283-312.
43. Palay SL. Chan-Palay V: Cerebellar Cortex: Cytology and Organization. New York. Springer. 1974.
44. Hertz L. Peng L: Energy metabolism at the cellular level of the CNS. Can J Physiol Pharmacol 1991;71:S145-S157.
45. Whitlingham I S. Liplon P: Cerebral synaptic transmission during anoxia is protected by creatine. J Neurochem 1981:37:1618-1621.
46. Carter AJ. Muller ER. Pschom U. Stransky W: Preincubation with creatine enhances levels of creatine phosphate and prevents anoxic damage in rat hippocampus slices. J Neurochem 1995:64:2691-2699.
47. Manos P. Bryan GK: Cellular and subccllular compartmentation of creatine kinase in brain. Dev Neurosci 1993:15:271-279.
48. Ito M: The cellular basis of cerebellar plasticity. CurrOpin Neurobiol 1991:1:616-620.
49. 2* stores in Purkinje neurons: Endoplasmic reticulum subcompanments demonstrated by het-eregenous distribution of InsP, receptor. Ca’*-ATPase. and calscqucstrin. J Neurosci 1992: 12:489-505.
50. Villa A. Podini P. Clegg DO. Pozzan T. Mel-dolesi J: Intracellular Ca"‘stores in chicken Purkinje neurons: Differential distribution of the low affinity-high capacity C;r* binding protein, calscqueslrin. of Ca"*-ATPase and of ER lumcnal protein. Bip. J Cell Biol 1991:113: 779-791.
51. Volpc P. Aldcrson-Lang BH. Madeddu L. Damiani E. Collins JH. Margreth A: Calse-questrin. a component of the inositol 1,4.5-triphosphate-sensitive Ca‘"-store of chicken cerebellum. Neuron 1990:5:713-721.
52. Campbell AM. Wuytack F, Fambrough DM: Differential distribution of the alternative forms of the sarcolasmic/cndoplasmic reticulum Ca’*-ATPase, SERCA2b and SERCA2a. in the avian brain. Brain Res 1993:605:67-76.
53. Michelangcli F. Di Virgilio F. Villa A. Podini P. Meldolesi J. Pozzan T: Identification, kinetic properties and intracellular localization of the Ca*-MgU-ATPasc from the intracellular stores of chicken cerebellum. Biochcm J 1991: 275:555-561.
54. Kuwajima G. Fulalsugi A, Niinobe M. Nakan-ishi S. Mikoshiba K: Two types of ryanodine receptors in mouse brain: Skeletal muscle type exclusively in Purkinje cells and cardiac muscle type in various neurons. Neuron 1992:9: 1133-1142.
55. Ellisman MH. Deerinck TJ. Ouyang Y. Beck CF. Tanksley SJ. Walton PD. Airey JA. Sulko JL: Identification and localization of ryanodine binding proteins in the avian central nervous system. Neuron 1990:5:135-146.
56. Korgc P. Campbell KB: Local ATP regeneration is important for sarcoplasmic reticulum C:r* pump function. Am J Physiol 1994:267: C357-C366.
57. Wallimann T: Dissecting the role of creatine kinase. Curr Biol 1994;1:42-46.
58. Ikeda K. Tomonaga M: The presence of creatine kinase (CK)-immunoreactive neurons in the zona incerta and lateral hypothalamic area of the mouse brain. Brain Res 1987:435: 348-350.
59. Bolshakov VY. Sicgelbaum SA; Regulation of hippocampus transmitter release during development and long-term potentation. Science 1995:269:1730-1734.
60. Nelson WJ, Mays RW. Marrs JA: Regulation of plasticity in Na/K-ATPnsc distribution in polarized epithelial cells. Proc 13th Int Congr Electron Microscopy (1CEM). Paris. 1994. vol 3A. pp 3-6.
61. Wallimann T, Walzthbny D, Wegmann G. Moser H. Eppenberger HM. Barrantes FJ: Sub-cellular localization of creatine kinase in Torpedo electrocytcs: Association with acetylcholine receptor-rich membranes. J Cell Biol 1985:100:1063-1073.
62. Delfalco AJ. Davies RK: The synthesis of creatine by the brain of the intact rat. J Neurochem 1961:7:308-312.
63. Holtzman D. McFarland E. Moerland T. Koutcher J, Kushmeric MJ. Neuringer U: Brain creatine phosphate and creatine kinase in mice fed an analogue of creatine. Brain Res 1989;483:68-77.
64. Mollcr A. Hampreclu B: Creatine transport in cultured cells of rat and mouse brain. J Ncu-rochem 1989:52:544-550.
65. Guimbal C. Kilimann MF: Na'-dependem creatine transporter in rabbit brain, muscle, heart and kidney. J Biol Client 1993:268:8418-8421.
66. Schloss R Mayser W. Betz H: The putative rat choline transporter C1IOT-I transports creatine and is highly expressed in neural and muscle-rich tissues. Biochint Biophys Res Com-rnun 1994;198:637-645.
67. Saltarclli MD. Bauman AL. Moore KR. Bradley CC, Blakely RD: Expression of die rat brain creatine transporter in situ and in transfected HeLa cells. Dev Neurosci 1996; 18: 524-534.
68. Happe HK, Murrin LC: In situ hybridization analysis of CHOT1. a creatine transporter, in the nervous system. J Comp Neurol 1995:351: 94-103.
69. Chen L. Roberts R. Friedman D: Expression of brain-type creatine kinase and ubiquitous mitochondrial creatine kinase in the fetal rat brain. J Comp Neurol 1995:363:389-401.
70. Stockier S. Holzbach U, Hanefcld F. Marquardt I. Helms G. Rcquart M, Hänickc W. Frahm J: Creatine deficiency in the brain: A new treatable inborn error of metabolism. PediatrRes 1994:36:409-413.
71. !IP MR sectroscopy in 28 patients with mitochondrial cytopathics. J Ccrcbr Blood Flow Metab 1993;13:469-474.
72. Stadhouders AM. Jap PHK. Winkler H-P. Eppcnberger HM. Wallimann T: Mitochondrial creatine kinase: A major constituent of pathological inclusions seen in mitochondrial myopathies. Proc Natl Acad Sei USA 1994:91: 5089-5093.
73. Wallace DC. Bohr VA. Cortopassi G. Kadenbach B. Linn S. Linnane AW, Richter C, Shay JW: Group report: The role of biocncrgelics and mitochondrial DNA mutations in aging and age-related diseases; in Esser K. Martin GM (cds): Molecular Aspects of Aging. Chichester, Wiley, 1995, pp 199-225.
74. Whittingham TS. Lust WD, Passonncau JV: An in vitro model of ischemia: Metabolic and electric alterations in the hippocampal slice. J Neurosci 1984;4:7993-8002.
75. Ilagcnfcldt L. von Döbeln U. Solder G. Kaijscr L: Creatine treatment in MELAS. Muscle Nerve 1994:17:1236.