Mitochondrial creatine kinase interaction with heterogeneous monolayers: Effect on lipid lateral organization

Biochimie

Volumn 91, Issue 6, 2009, Pages 752-764

  Vernoux, Nathalie ^a   Maniti, Ofelia ^a   Marcillat, Olivier ^a   Vial, Christian ^a   Granjon, Thierry ^a  

^a UNIVERSITÉ DE LYON   (France)

Author keywords

Brewster angle microscopy; Langmuir; Mitochondrial creatine kinase; Phase transition; Phospholipid domains

Indexed keywords

DIMYRISTOYLPHOSPHATIDYLCHOLINE; DIMYRISTOYLPHOSPHATIDYLGLYCEROL; DIPALMITOYLPHOSPHATIDYLGLYCEROL; MITOCHONDRIAL CREATINE KINASE; PHOSPHOLIPID;

ARTICLE; CONTROLLED STUDY; LIPID MONOLAYER; NONHUMAN; PHASE TRANSITION; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN STRUCTURE;

ANIMALS; CREATINE KINASE; KINETICS; LIPID BILAYERS; MEMBRANE LIPIDS; MICROSCOPY; MITOCHONDRIA, HEART; MITOCHONDRIAL PROTEINS; PHOSPHOLIPIDS; PROTEIN BINDING; RABBITS; THERMODYNAMICS;

EID: 65549125291     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2009.03.014     Document Type: Article

References (48)

1. Jackson J.H., Li J.W., Buss J.E., Der C.J., and Cochrane C.G. Polylysine domain of K-ras 4B protein is crucial for malignant transformation. Proc. Natl. Acad. Sci. USA 91 (1994) 12730-12734
2. Arbuzova A., Wang L., Wang J., Hangyas-Mihalyne G., Murray D., Honig B., and McLaughlin S. Membrane binding of peptides containing both basic and aromatic residues. Experimental studies with peptides corresponding to the scaffolding region of caveolin and the effector region of MARCKS. Biochemistry 39 (2000) 10330-10339
3. Zhou W., Parent L.J., Wills J.W., and Resh M.D. Identification of a membrane-binding domain within the amino-terminal region of human immunodeficiency virus type 1 Gag protein which interacts with acidic phospholipids. J. Virol. 68 (1994) 2556-2569
4. Sigal C.T., Zhou W., Buser C.A., McLaughlin S., and Resh M.D. Amino-terminal basic residues of Src mediate membrane binding through electrostatic interaction with acidic phospholipids. Proc. Natl. Acad. Sci. USA 91 (1994) 12253-12257
5. Marcillat O., Goldschmidt D., Eichenberger D., and Vial C. Only one of the two interconvertible forms of mitochondrial creatine kinase binds to heart mitoplasts. Biochim. Biophys. Acta 890 (1987) 233-241
6. Schlegel J., Zurbriggen B., Wegmann G., Wyss M., Eppenberger H.M., and Wallimann T. Native mitochondrial creatine kinase forms octameric structures. Isolation of two interconvertible mitochondrial creatine kinase forms, dimeric and octameric mitochondrial creatine kinase: characterization, localization, and structure-function relationships. J. Biol. Chem. 263 (1988) 16942-16953
7. Schnyder T., Engel A., Lustig A., and Wallimann T. Native mitochondrial creatine kinase forms octameric structures. II. Characterization of dimers and octamers by ultracentrifugation, direct mass measurements by scanning transmission electron microscopy, and image analysis of single mitochondrial creatine kinase octamers. J. Biol. Chem. 263 (1988) 16954-16962
8. Nicolay K., Rojo M., Wallimann T., Demel R., and Hovius R. The role of contact sites between inner and outer mitochondrial membrane in energy transfer. Biochim. Biophys. Acta 1018 (1990) 229-233
9. Vacheron M.J., Clottes E., Chautard C., and Vial C. Mitochondrial creatine kinase interaction with phospholipid vesicles. Arch. Biochem. Biophys. 344 (1997) 316-324
10. Muller M., Moser R., Cheneval D., and Carafoli E. Cardiolipin is the membrane receptor for mitochondrial creatine phosphokinase. J. Biol. Chem. 260 (1985) 3839-3843
11. Quemeneur E., Eichenberger D., Goldschmidt D., Vial C., Beauregard G., and Potier M. The radiation inactivation method provides evidence that membrane-bound mitochondrial creatine kinase is an oligomer. Biochem. Biophys. Res. Commun. 153 (1988) 1310-1314
12. Rojo M., Hovius R., Demel R., Wallimann T., Eppenberger H.M., and Nicolay K. Interaction of mitochondrial creatine kinase with model membranes. A monolayer study. FEBS Lett. 281 (1991) 123-129
13. Biermans W., Bernaert I., De Bie M., Nys B., and Jacob W. Ultrastructural localisation of creatine kinase activity in the contact sites between inner and outer mitochondrial membranes of rat myocardium. Biochim. Biophys. Acta 974 (1989) 74-80
14. Bakker A., Bernaert I., Debie M., Ravingerova T., Ziegelhoffer A., Vanbelle H., and Jacob W. The effect of calcium on mitochondrial contact sites: a study on isolated rat hearts. Biochim. Biophys. Acta 1224 (1994) 583-588
15. Rojo M., Hovius R., Demel R.A., Nicolay K., and Wallimann T. Mitochondrial creatine kinase mediates contact formation between mitochondrial membranes. J. Biol. Chem. 266 (1991) 20290-20295
16. Schnyder T., Gross H., Winkler H., Eppenberger H.M., and Wallimann T. Structure of the mitochondrial creatine kinase octamer: high-resolution shadowing and image averaging of single molecules and formation of linear filaments under specific staining conditions. J. Cell Biol. 112 (1991) 95-101
17. Schnyder T., Cyrklaff M., Fuchs K., and Wallimann T. Crystallization of mitochondrial creatine kinase on negatively charged lipid layers. J. Struct. Biol. 112 (1994) 136-147
18. Fritz-Wolf K., Schnyder T., Wallimann T., and Kabsch W. Structure of mitochondrial creatine kinase. Nature 381 (1996) 341-345
19. Eder M., Fritz-Wolf K., Kabsch W., Wallimann T., and Schlattner U. Crystal structure of human ubiquitous mitochondrial creatine kinase. Proteins 39 (2000) 216-225
20. Schlattner U., Gehring F., Vernoux M., Tokarska-Schlattner M., Neumann D., Marcillat O., Vial C., and Walliman T. C-terminal lysines determine phospholipid interaction of sarcomeric mitochondrial creatine kinase. J. Biol. Chem. 279 (2004) 24334-24342
21. Quéméneur E., Marcillat O., Eichenberger D., and Vial C. Isoelectric point heterogeneity of the two oligomeric forms of heart mitochondrial creatine kinase. Biochemistry 18 (1989) 365-371
22. Wyss M., Schlegel J., James P., Eppenberger H.M., and Wallimann T. Mitochondrial creatine kinase from chicken brain. Purification, biophysical characterization, and generation of heterodimeric and heterooctameric molecules with subunits of other creatine kinase isoenzymes. J. Biol. Chem. 265 (1990) 15900-15908
23. Weselake R.J., and Jacobs H.K. Separation of cytoplasmic and mitochondrial isoenzymes of creatine kinase by hydrophobic interaction chromatography. Clin. Chim. Acta 134 (1983)
24. Ventura-Clapier R., Kuznetsov A., Veksler V., Boehm E., and Anflous K. Functional coupling of creatine kinases in muscles: species and tissue specificity. Mol. Cell. Biochem. 184 (1998) 231-247
25. Brdiczka D. Contact sites between mitochondrial envelope membranes. Structure and function in energy- and protein-transfer. Biochim. Biophys. Acta 1071 (1991) 291-312
26. Wallimann T., Wyss M., Brdiczka D., Nicolay K., and Eppenberger H.M. 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 (1992) 21-40
27. Schlattner U., Forstner M., Eder M., Stachowiak O., Fritz-Wolf K., and Wallimann T. Functional aspects of the X-ray structure of mitochondrial creatine kinase: a molecular physiology approach. Mol. Cell. Biochem. 184 (1998) 125-140
28. Vernoux N., Granjon T., Marcillat O., Besson F., and Vial C. Interfacial behavior of cytoplasmic and mitochondrial creatine kinase oligomeric states. Biopolymers 81 (2006) 270-281
29. Vernoux N., Maniti O., Besson F., Granjon T., Marcillat O., and Vial C. Mitochondrial creatine kinase adsorption to biomimetic membranes: a Langmuir monolayer study. J. Colloid Interface Sci. 310 (2007) 436-445
30. Henon S., and Meunier J. Microscope at the Brewster angle: direct observation of first-order phase transitions in monolayers. Rev. Sci. Instrum. 62 (1991) 936-939
31. Marcillat O., Perraut C., Granjon T., Vial C., and Vacheron M.J. Cloning, Escherichia coli expression, and phase-transition chromatography-based purification of recombinant rabbit heart mitochondrial creatine kinase. Prot. Expr. Purif. 17 (1999) 163-168
32. Hönig D., and Möbius D. Direct visualization of monolayers at the air-water interface by Brewster angle microscopy. J. Phys. Chem. 95 12 (1991) 4590-4592
33. Rodriguez Patino J.M., Sanchez C.C., and Rodriguez Nino M.R. Structural and morphological characteristics of [beta]-casein monolayers at the air-water interface. Food Hydrocolloids 13 (1999) 401
34. Rodriguez Patino J.M., Carrera Sanchez C., and Rodriguez Nino M.R. Morphological and structural characteristics of monoglyceride monolayers at the air-water interface observed by Brewster angle microscopy. Langmuir 15 (1999) 2484-2492
35. O. Maniti, M.F. Lecompte, O. Marcillat, B. Desbat, R. Buchet, C. Vial, T. Granjon, Mitochondrial creatine kinase binding to phospholipid monolayers induces cardiolipin segregation, Biophys. J. 96 in press.
36. Yu Z., Jin J., and Cao Y. Characterization of the liquid-expanded to liquid-condensed phase transition of monolayers by means of compressibility. Langmuir 18 (2002) 4530-4531
37. Minones Jr. J., Dynarowicz-Latka P., Minones J., Rodriguez Patino J.M., and Iribarnegaray E. Orientational changes in dipalmitoyl phosphatidyl glycerol Langmuir monolayers. J. Colloid Interface Sci. 265 (2003) 380-385
38. Arnold A., Cloutier I., Ritcey A.M., and Auger M. Temperature and pressure dependent growth and morphology of DMPC/DSPC domains studied by Brewster angle microscopy. Chem. Phys. Lipids 133 (2005) 165-179
39. Garidel P., and Blume A. 1,2-Dimyristoyl-sn-glycero-3-phosphoglycerol (DMPG) monolayers: influence of temperature, pH, ionic strength and binding of alkaline earth cations. Chem. Phys. Lipids 138 (2005) 50-59
40. Granjon T., Vacheron M.J., Vial C., and Buchet R. Mitochondrial creatine kinase binding to phospholipids decreases fluidity of membranes and promotes new lipid-induced beta structures as monitored by red edge excitation shift, laurdan fluorescence, and FTIR. Biochemistry 40 (2001) 6016-6026
41. Marsh D. Lateral pressure in membranes. Biochim. Biophys. Acta 1286 (1996) 183-223
42. Vial C., Marcillat O., Goldschmidt D., Font B., and Eichenberger D. Interaction of creatine kinase with phosphorylating rabbit heart mitochondria and mitoplasts. Arch. Biochem. Biophys. 251 (1986) 558-566
43. Lipskaya T.Y. Mitochondrial creatine kinase: properties and function. Biochemistry (Mosc) 66 (2001) 1098-1111
44. Albrecht O., Gruler H., and Sackmann E. Polymorphism of phospholipid monolayers. J. Physique (Paris) 39 (1978) 301-313
45. Möhwald H. Phospholipid Monolayers vol. 1 (1995), Elsevier Science, B.V. 161-211
46. Peters R., and Beck K. Translational diffusion in phospholipid monolayers measured by fluorescence microphotolysis. Proc. Natl. Acad. Sci. USA 80 (1983) 7183-7187
47. Loidl-Stahlhofen A., Kaufmann S., Braunschweig T., and Bayerl T.M. The thermodynamic control of protein binding to lipid bilayers for protein chromatography. Nat. Biotech. 14 (1996) 999
48. Kasbauer M., and Bayerl T.M. Formation of domains of cationic or anionic lipids in binary lipid mixtures increases the electrostatic coupling strength of water-soluble proteins to supported bilayers. Biochemistry 38 (1999) 15258-15263