Use of gene targeting for compromising energy homeostasis in neuro-muscular tissues: The role of sarcomeric mitochondrial creatine kinase

Journal of Neuroscience Methods

Volumn 71, Issue 1, 1997, Pages 29-41

  Steeghs, Karen ^a   Heerschap, Arend ^a   De Haan, Arnold ^b   Ruitenbeek, Wim ^a   Oerlemans, Frank ^a   Van Deursen, Jan ^c   Perryman, Benjamin ^d   Pette, Dirk ^e   Brückwilder, Marloes ^a   Koudijs, Jolande ^b   Paul, Jap ^a   Wieringa, Bé ^a  

^a RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^b VU UNIVERSITY AMSTERDAM   (Netherlands)

^c ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^d UNIVERSITY OF COLORADO   (United States)

^e UNIVERSITY OF KONSTANZ   (Germany)

Author keywords

creatine kinase; energy homeostasis; gene targeting; mitochondria; muscle physiology; oxidative phosphorylation

Indexed keywords

CREATINE KINASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; CONTROLLED STUDY; DNA DETERMINATION; EMBRYO; GENE TARGETING; MITOCHONDRION; MOUSE; NEUROMUSCULAR SYNAPSE; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; REVIEW; TRANSGENIC MOUSE;

EID: 18844463016     PISSN: 01650270     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0165-0270(96)00124-0     Document Type: Article

References (84)

1. Adams, V., Bosch, W., Schlegel, J., Wallimann, T. and Brdiczka, D. (1989) Further characterization of contact sites from mitochondria of different tissues: Topology of peripheral kinases, Biochim. Biophys. Acta, 981: 213-225.
2. Balaban, R.S. (1990) Regulation of oxidative phosphorylation in the mammalian cell, Am. J. Physiol., 258: C377-C389.
3. Bessmann, S.P. and Carpenter, L.C. (1985) The creatine-creatine phosphate energy shuttle, Annu. Rev. Biochem. 54, 831-862.
4. Biermans, W., Bakker, A. and Jacob, W. (1990) Contact sites between inner and outer mitochondrial membrane: A dynamic microcompartment for creatine kinase, Biochim. Biophys. Acta, 1018: 225-228.
5. +)-ATPase in the resting and stimulated organ of the electric fish Narcine brasiliensis, J. Biol. Chem., 266: 10254-10259.
6. Brdiczka, D. (1991) Contact sites between mitochondrial envelope membranes. Structure and function in energy-and protein transfer, Biochim. Biophys. Acta, 1071: 291-312.
7. Brdiczka, D. and Wallimann, T. (1994) The importance of the outer mitochondrial compartment in regulation of energy metabolism, Mol. Cell. Biochem. 133/134: 69-83.
8. Bradley, A. (1987) Production and analysis of chimeric mice. In E.J. Robertson (Ed.), Teratocarcinomas and Embryonic Stem Cells: A Practical Approach, IRL Press, Oxford, pp. 113-151.
9. Brandon, E.P., Idzerda, R.L. and McKnight, G.S. (1995) Targeting the mouse genome: A compendium of knockouts, Curr. Biol. 5, 625, 758, 873.
10. Brown, M.D. and Wallace, D.C. (1994) Molecular basis of mitochondrial DNA disease, J. Bioenerg. Biomembr. 26, 273-289.
11. Brosnan, M.J., Chen, L., VanDyke, T.A. and Koretsky, A.P. (1990) Free ADP levels in transgenic mouse liver expressing creatine kinase: effects of enzyme activity, phosphagen type, and substrate concentration, J. Biol. Chem., 265: 20849-20855.
12. Brosnan, M.J., Raman, S.P., Chen, L. and Koretsky, A.P. (1993) Altering creatine kinase isoenzymes in transgenic mouse muscle by overexpression of the B subunit, Am. J. Physiol., 264: C151-C160.
13. Capecchi, M.R. (1989) The new mouse transgenetics: altering the genome by gene targeting, Trends Genet., 5: 70-76.
14. Cooperstein, S.J. and Lazarow, A. (1951) A microspectrophotometric method for the determination of cytochrome oxidase, J. Biol. Chem. 189, 665-680.
15. De Haan, A., Jones, D.A. and Sargeant, A.J. (1989) Changes in velocity of shortening, power output and relaxation rate during fatigue of rat medial gastrocnemius, Pflügers Arch. 413, 422-428.
16. Dunnett, M., Harris, R.C. and Orme, C.E. (1991) Reverse-phase ion-pairing high-performance liquid chromatography of phosphocreatine, creatine and creatinine in equine muscle, Scand. J. Clin. Lab. Invest. 51, 137-141.
17. Edwards, R.H.T., Hill, D.K. and Jones, D.A. (1975) Metabolic changes associated with the slowing of relaxation in fatigued mouse muscle, J. Physiol. 251, 287-301.
18. Erecinska, M. and Wilson, D. (1982) Regulation of cellular energy metabolism, J. Membr. Biol., 70: 1-14.
19. Evans, M.J. (1989) Potential for genetic manipulation of mammals, Mol. Biol. Med., 6: 557-565.
20. Fischer, J.C., Ruitenbeek, W., Gabreëls, F.J.M., Janssen, A.J.M., Renier, W.O., Sengers, R.C.A., Stadhouders, A.M., Ter Laak, H.J., Trijbels, J.M.F. and Veerkamp, J.H. (1986) A mitochondrial encephalomyopathy: the first case with an established defect at the level of coenzyme Q, Eur. J. Pediatr., 144: 441-444.
21. Friedhof, A.J. and Lerner, M.H. (1977) CK isoenzyme association with synaptosomal membrane and synaptic vesicles, Life Sci., 20: 867-872.
22. Friedman, D.L. and Perryman, M.B. (1991) Compartmentalization of multiple forms of creatine kinase in the distal nephron of the rat kidney, J. Biol. Chem., 266: 22404-22410.
23. Friedman, D.L. and Roberts, R. (1994) Compartmentalization 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., 343: 500-511.
24. Gellerich, F.N. (1992) The role of adenylate kinase in dynamic Compart-mentalization of adenine nucleotides in the mitochondrial intermembrane space, FEBS Lett., 297: 55-58.
25. Gellerich, F.N., Kapischke, M., Kunz, W., Neumann, W., Kuznetsov, A., Brdiczka, D. and Nicolay, K. (1994) The influence of the cytosolic oncotic pressure on the permeability of the mitochondrial outer membrane for ADP: implications for the kinetic properties of mitochondrial creatine kinase and for ADP channeling into the intermembrane space, Mol. Cell. Biochem., 133/134: 85-104.
26. +)-antiport across the membrane of vesicles formed from the plasma membrane of cardiac muscle cells, Biochim. Biophys. Acta, 603: 142-156.
27. Haas, R.C., Korenfeld, D.C., Zhang, Z., Perryman, M.B., Roman, D. and Strauss, A.W. (1989) Isolation and characterization of the gene and cDNA encoding human mitochondrial creatine kinase, J. Biol. Chem., 264: 2890-2897, 16332 (correction).
28. Hämäläinen, N. and Pette, D. (1993) The histochemical profiles of fast fiber types IIB, IID, and IIA in skeletal muscles of mouse, rat, and rabbit, J. Histochem. Cytochem. 41, 733-743.
29. Heerschap, A., Bergman, A.H., Vaals, J.J., Wirtz, P., Loermans, H.M.T. and Veerkamp, J.H. (1988a) Alterations in relative phosphocreatine concentrations in preclinical mouse muscular dystrophy revealed by in vivo NMR, NMR Biomed. 1, 27-31.
30. 31P-NMR studies of rat salivary glands, Magn. Reson. Med. 8, 129.
31. Hemmer, W. and Wallimann, T. (1993) Functional aspects of creatine kinase in brain, Dev. Neurosci., 15: 249-260.
32. Hemmer, W., Zanolla, E., Furter-Graves, E.M., Eppenberger, H.M. and 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.
33. Hossle, J.P., Schlegel, J., Wegmann, G., Wyss, M., Böhlen, P., Eppenberger, H.M., Wallimann, T. and Perriard, J.-C. (1988) Distinct tissue-specific mitochondrial creatine kinases from chicken brain and striated muscle with a conserved CK framework, Biochem. Biophys. Res. Commun., 151: 408-416.
34. Ikeda, K. (1988) Localization of brain type creatine kinase in kidney epithelial cell subpopulations in rat, Experientia, 44: 734-735.
35. Ishida, Y., Riesinger, T., Wallimann, T. and Paul, R.J. (1994) Compartmentalization of ATP synthesis and utilization in smooth muscle: roles of aerobic glycolysis and creatine kinase, Mol. Cell. Biochem. 133/134: 39-50.
36. Jacobus, W.E. and Lehninger, A.L. (1973) Creatine kinase of rat heart, mitochondrial coupling of creatine phosphorylation to electron transport, J. Biol. Chem., 248: 4803-4810.
37. Jaenisch, R. (1988) Transgenic animals, Science, 240, 1468-1474.
38. 2 and ATP, Am. J. Physiol., 250: C663-C675.
39. Joyner, A.L. (1991) Gene targeting and gene trap screens using embryonic stem cells: new approaches to mammalian development, Bioessays, 13: 649-656.
40. Knoll, G. and Brdiczka, D. (1983) Changes in freeze-fracture mitochondrial membranes correlated to their energetic state, Biochim. Biophys. Acta, 733: 102-110.
41. Koretsky, A.P., Brosnan, M.J., Chen, L., Chen, J. and VanDyke, T. (1990) NMR detection of creatine kinase expressed in liver of transgenic mice: determination of free ADP levels, Proc. Natl. Acad. Sci. USA, 87: 3112-3116.
42. 2+ pump function, Am. J. Physiol., 267: C357-C366.
43. Levitsky, D.O., Levchenko, T.S., Saks, V.A., Sharov, V.G. and Smirnov, V.N. (1978) The role of creatine phosphokinase in supplying energy for the calcium pump system of heart sarcoplasmic reticulum, Membr. Biochem., 2: 81-96.
44. Lim, L., Hall, C., Leung, T., Mahadevan, L. and Whatley, S. (1989) Neurone-specific enolase and creatine phosphokinase are protein components of rat brain synaptic plasma membranes, J. Neurochem., 41:1177-1182.
45. Lipskaya, T.Yu. and Trofimova, M.E. (1989) Study on heart mitochondrial creatine kinase using a cross-linking bifunctional reagent. I. The binding involves the octameric form of the enzyme, Biochem Int., 18: 1029-1039, 1149-1159.
46. Miller, D.S. and Horowitz, S.B. (1986) Intracellular compartmentalization of adenosine triphosphate, J. Biol. Chem., 261: 13911-13915.
47. Miller, K., Halow, J. and Koretsky, A.P. (1993) Phosphocreatine protects transgenic mouse liver expressing creatine kinase from hypoxia and ischemia. Am. J. Physiol., 265: C1544-C1551.
48. Mühlebach, S.M., Gross, M., Wirz, T., Wallimann, T., Perriard, J.-C. and Wyss, M. (1994) Sequence homology and structure predictions of the creatine kinase isoenzymes, Mol. Cell. Biochem., 133/134: 245-262.
49. Payne, R.M., Haas, R.C. and Strauss, A.W. (1991) Structural characterization and tissue-specific expression of the mRNAs encoding isoenzymes from two rat mitochondrial creatine kinase genes, Biochim. Biophys. Acta, 1089: 352-361.
50. Perriard, J.-C., Perriard, E.R. and Eppenberger, H.M. (1989) Detection and relative quantitation of mRNA for creatine kinase isoenzymes in RNA from myogenic cell cultures and embryonic chicken tissues, J. Biol. Chem., 253: 6529-6535.
51. Pette, D. and Vrbová, G. (1992) Adaptation of mammalian skeletal muscle fibers to chronic electrical stimulation, Rev. Physiol. Biochem. Pharmacol. 120, 115-202.
52. + clearance by diffusion and spatial buffering. In N.J. Abbott (Ed.), Glial-Neuronal Interaction, New York Academy of Sciences, New York, pp. 272-286.
53. Rojo, M., Hovius, R., Demel, R.A., Nicolay, K. and Wallimann, T. (1991) Mitochondrial creatine kinase mediates contact formation between mitochondrial membranes, J. Biol. Chem., 266: 20290-20295.
54. Rossant, J. (1991) Gene disruption in mammals, Curr. Opin. Genet. Dev., 1: 236-240.
55. 2+ uptake and regulate local ATP/ADP ratios, J. Biol. Chem., 265: 5258-5266.
56. Saks, V.A., Chernousova, G.B., Vetter, R., Smirnov, V.N. and Chazov, E.I. (1976) Kinetic properties and the functional role of particulate MM-isoenzyme of creatine phosphokinase bound to heart muscle myofibrils, FEES Lett., 62: 293-296.
57. + ATPase, Biochim. Biophys. Acta, 465: 550-558.
58. Saks, V.A., Khuchua, Z.A., Vasilyeva, E.V., Belikova, O.Yu. and Kuznetsov, A.V. (1994) Metabolic compartmentalization and substrate channeling in muscle cells. Role of coupled creatine kinases in in vivo regulation of cellular respiration - a synthesis, Mol. Cell. Biochem., 133/134: 155-192.
59. Savabi, F. (1994) Interaction of creatine kinase and adenylate kinase systems in muscle cells, Mol. Cell. Biochem., 133/134: 145-152.
60. Schlegel, J., Wyss, M., Eppenberger, H.M. and Wallimann, T. (1990) Functional studies with the octameric and dimeric form of mitochondrial creatine kinase, J. Biol. Chem., 265: 9221-9227.
61. Scopes, R.K. (1973) Studies with a reconstituted muscle glycolytic system - rate and extent of creatine phosphorylation by anaerobic glycolysis, Biochem. J., 134: 197.
62. Sellevold, O.F.M., Jynge, P. and Aarstad, K. (1986) High performance liquid chromatography: a rapid isocratic method for determination of creatine compounds and adenine nucleotides in myocardial tissue, J. Mol. Cell. Cardiol., 18, 517-527.
63. Smithies, O. (1993) Animal models of human genetic diseases. Trends Genet., 9: 112-117.
64. Srere, P. (1987) Complexes of sequential metabolic enzymes, Annu. Rev. Biochem., 56: 89-124.
65. Srere, P.A. (1969) Citrate synthase, citrate oxaloacetate lyase, Methods Enzymol., 13: 3-11.
66. Steeghs, K., Oerlemans, F. and Wieringa, B. (1995a) Mice deficient in ubiquitous mitochondrial creatine kinase are viable and fertile, Biochim. Biophys. Acta, 1230: 130-138.
67. Steeghs, K., Peters, W., Croes, H., Brückwilder, M., Van Alewijck, D. and Wieringa, B. (1995b) Mouse ubiquitous mitochondrial creatine kinase: gene organization and consequences from inactivation in mouse embryonic stem cells, DNA Cell Biol., 14: 539-553.
68. Sweeney, H.L., Kushmerick, M.J., Mabuchi, K., Sreter, F.A. and Gergely, J. (1988) Myosin alkali light chain and heavy chain variations correlate with altered shortening velocity of isolated skeletal muscle fibers, J. Biol. Chem., 263: 9034-9039.
69. Thomas, K.R. and Capecchi, M.R. (1987) Site-directed mutagenesis by gene targeting in mouse embryo-derived stem cells, Cell, 51: 503-512.
70. Trask, R.V., Strauss, A.W. and Billadello, J.J. (1988) Developmental regulation and tissue-specific expression of the human muscle creatine kinase gene, J. Biol. Chem., 263: 17142-17149.
71. Turner, D.C., Wallimann, T. and Eppenberger, H.M. (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: 702-705.
72. Van Deursen, J., Schepens, J., Peters, W., Meijer, D., Grosveld, G., Hendriks, W. and Wieringa, B. (1992) Genetic variability of the murine creatine kinase B gene locus and related pseudogenes in different inbred strains of mice, Genomics, 12: 340-349.
73. Van Deursen, J., Heerschap, A., Oerlemans, F., Ruitenbeek, W., Jap, P., Ter Laak, H. and Wieringa, B. (1993) Skeletal muscles of mice deficient in muscle creatine kinase lack burst activity, Cell, 74: 621-631.
74. Van Deursen, J., Ruitenbeek, W., Heerschap, A., Jap, P., Ter Laak, H. and Wieringa, B. (1994a) Creatine kinase in skeletal muscle energy metabolism: a study of mouse mutants with graded reduction in M-CK expression, Proc. Natl. Acad. Sci. USA, 91: 9091-9095.
75. Van Deursen, J., Jap, P., Heerschap, A., Ter Laak, H., Ruitenbeek, W. and Wieringa, B. (1994b) Effects of the creatine analogue β-guanidinopropionic acid on skeletal muscles of mice deficient in muscle creatine kinase, Biochim. Biophys. Acta, 1185: 327-335.
76. Veksler, V. and Ventura-Clapier, R. (1994) Ischaemic metabolic factors - high inorganic phosphate and acidosis - modulate mitochondrial creatine kinase functional activity in skinned cardiac fibres, J. Mol. Cell. Cardiol., 26: 335-339.
77. Ventura-Clapier, R., Saks, V.A., Vassort, G., Lauer, C. and Elizarova, G.V. (1987) Reversible MM-creatine kinase binding to cardiac muscle, Am. J. Physiol., 253: C444-C455.
78. Ventura-Clapier, R., Veksler, V. and Hoerter, J.A. (1994) Myofibrillar creatine kinase and cardiac contraction, Mol. Cell. Biochem., 133/134: 125-144.
79. Wallimann, T., Wyss, M., Brdiczka, D., Nicolay, K. and Eppenberger, H.M. (1992) Intracellular compartmentalization, 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: 21-40.
80. Wegmann, G., Zanolla, E., Eppenberger, H.M. and Wallimann, T. (1992) In situ compartmentalization of creatine kinase in intact sarcomeric muscle: the acto-myosin overlap zone as a molecular sieve, J. Muscle Res. Cell Motil., 13: 420-435.
81. Wyss, M., Smeitink, J., Wevers, R.A. and Wallimann, T. (1992) Mitochondrial creatine kinase: a key enzyme of aerobic energy metabolism, Biochim. Biophys. Acta, 1102: 119-166.
82. 32P-labeled ATP by isolated rabbit heart mitochondria, Biochem. Biophys. Res. Commun., 76: 882-887.
83. 31P nuclear magnetic resonance saturation transfer, Biophys. J. 51, 883-893.
84. Zeleznikar, R.J., Dzeja, P.P. and Goldberg, N.D. (1995) Adenylate kinase-catalyzed phosphoryl transfer couples ATP utilization with its generation by glycolysis in intact muscle, J. Biol. Chem. 270, 7311-7319.