Structural investigation on the adsorption of the MARCKS peptide on anionic lipid monolayers - Effects beyond electrostatic

Chemistry and Physics of Lipids

Volumn 164, Issue 4, 2011, Pages 266-275

  Dietrich, Undine ^a   Krüger, Peter ^a,b   Käs, Josef A ^a  

^a UNIVERSITY OF LEIPZIG   (Germany)

^b FRAUNHOFER INSTITUTE FOR NON DESTRUCTIVE TESTING   (Germany)

Author keywords

Anionic lipids; Fluorescence microscopy; Isotherms; MARCKS (151 175); Monolayer; X ray diffraction

Indexed keywords

1,2 DIPALMITOYL SN GLYCERO 3 PHOSPHO LEVO SERINE; LIPID; MARCKS PROTEIN; UNCLASSIFIED DRUG;

ADSORPTION; ARTICLE; CHEMICAL STRUCTURE; CLUSTER ANALYSIS; FLUORESCENCE MICROSCOPY; LIPID MONOLAYER; PRIORITY JOURNAL; STATIC ELECTRICITY; SURFACE CHARGE; X RAY DIFFRACTION;

1,2-DIPALMITOYLPHOSPHATIDYLCHOLINE; ADSORPTION; ANIONS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; MEMBRANES, ARTIFICIAL; PHOSPHATIDYLSERINES; PROTEIN CONFORMATION; STATIC ELECTRICITY; SURFACE PROPERTIES;

EID: 79957788715     PISSN: 00093084     EISSN: 18732941     Source Type: Journal    
DOI: 10.1016/j.chemphyslip.2011.02.004     Document Type: Article

References (63)

1. Aderem, A., 1992. Signal transduction and the actin cytoskeleton: the role of MARCKS and profilin. Trends Biochem. Sci., 438-443.
2. Alberts, B., Johnson, A., Lewis, J., 2003. Molekularbiologie der Zelle. Wiley VCH, Weinheim.
3. Alonso, S., Dietrich, U., Händel, C., Käs, J.A., Bär, M., 2011. Oscillations in the lateral pressure of lipid monolayers induced by nonlinear chemical dynamics of the second messengers MARCKS and protein kinase C. Biophys. J. 100, 939-947.
4. Arbuzova, A., Murray, D., McLaughlin, S., 1998. MARCKS, membranes, and calmodulin: kinetics of their interaction. Biochim. Biophys. Acta 1376, 369-379.
5. Arbuzova, A., Wang, J., Murray, D., Jacob, J., Cafiso, D.S., McLaughlin, S., 1997. Kinetics of interaction of the myristoylated alanine-rich C kinase substrate, membranes, and calmodulin. J. Biol. Chem. 272 (43), 27167-27177.
6. Arbuzova, A., Wang, L., Wang, J., Hangyás-Milháyné, G., Murray, D., Honig, B., McLaughlin, S., 2000. 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. Biochem. 39, 10330-10339.
7. Armen, R.S., Uitto, O.D., Feller, S.E., 1998. Phospholipid component volumes: determination and application to bilayer structure calculations. Biophys. J. 75, 734-744. (Pubitemid 28357515)
8. Bähr, G., Diederich, A., Vergères, G., Winterhalter, M., 1998. Interaction of the effector domain of MARCKS and MARCKS-related protein with lipid membranes revealed by electric potential measurements. Biochemistry 37 (46), 16252-16261. (Pubitemid 28536261)
9. Blackshear, P.J., 1993. The MARCKS family of cellular protein kinase C substrates. J. Biol. Chem. 268 (3), 1501-1504.
10. Blume, A., 1979. A comparative study of the phase transitions of phospholipid bilayers and monolayers. Biochim. Biophys. Acta 557, 32-44.
11. Bradshaw, J.P., Bushby, R.J., Giles, C.C.D., Saunders, M.R., 1999. Orientation of the headgroup of phosphatidylinositol in a model biomembrane as determined by neutron diffraction. Biochemistry 38, 8393-8401.
12. Cascales, J.J.L., Berendsen, H.J.C., de la Torre, J.G., 1996a. Molecular dynamics simulation of water between two charged layers of dipalmitoylphosphatidylserine. J. Phys. Chem. 100, 8621-8627.
13. Cascales, J.J.L., de la Torre, J.G., Marrink, S.J., Berendsen, H.J.C., 1996b. Molecular dynamics simulation of a charged biological membrane. J. Chem. Phys. 104 (7), 2713-2720.
14. Denisov, G., Wanaski, S., Luan, P., Glaser, M., McLaughlin, S., 1998. Binding of basic peptides to membrane produces lateral domains enriched in the acidic lipids phosphatidylserine and phosphatidylinositol 4,5-bisphosphate: an electrostatic model and experimental results. Biophys. J. 74, 731-744. (Pubitemid 28345268)
15. DeWolf, C., Leporatti, S., Kirsch, C., Klinger, R., Brezesinski, G., 1999. Phase separation in phosphatidylinositol/phosphatidylcholine mixed monolayers. Chem. Phys. Lip. 97 (2), 129-138.
16. 2 in phospholipid monolayers. Biochim. Biophys. Acta 1788, 1474-1481.
17. Dyck, M., 2006. Lipid Headgroup Organization and Interaction of Neuropeptide Y with Phospholipid Membranes. Ph.D. thesis, Universität Leipzig.
18. Dyck, M., Lösche, M., 2006. Interaction of the neurotransmitter, neuropeptide Y, with phospholipid membranes: film balance and fluorescence microscopy studies. J. Phys. Chem. B 110, 22143-22151.
19. Ellena, J.F., Burnitz, M.C., Cafiso, D.S., 2003. Location of the myristoylated alanine rich C kinase substrate (MARCKS) effector domain in negatively charged phospholipid bicells. Biophys. J. 85 (4), 2442-2448. (Pubitemid 37210791)
20. Farge, E., 1995. Increased vesicle endocytosis due to an increase in the plasma membrane phosphatidylserine concentration. Biophys. J. 69, 2501-2506.
21. Fernandes, F., Loura, L.M.S., Fedorov, A., Prieto, M., 2006. Absence of clustering of phosphatidylinositol-(4,5)-biphosphate in fluid phosphatidylcholine. J. Lipid Res. 47, 1521-1525.
22. Filippov, A., Orädd, G., Lindblom, G., 2004. Lipid lateral diffusion in ordered and disordered phases in raft mixtures. Biophys. J. 86, 891-896. (Pubitemid 38209533)
23. Foster, W.J., Janmey, P.A., 2001. The distribution of polyphosphoinositides in lipid films. Biophys. Chem. 91 (3), 211-218.
24. Gambhir, A., Hangyás-Mihályné, G., Zaitseva, I., Cafiso, D.S., Wang, J., Murray, D., Pentyala, S.N., Smith, S.O., McLaughlin, S., 2004. Electrostatic sequestration of PIP2 on phospholipidmembranesby basic/aromatic regions of proteins. Biophys. J. 86, 2188-2207. (Pubitemid 38524409)
25. Glaser, M., Wanaski, S., Buser, C.A., Boguslavsky, V., Rashidzada, W., Morris, A., Rebecchi, M., Scarlata, S.F., Runnels, L.W., Prestwich, G.D., Chen, J., Aderem, A., Ahn, J., McLaughlin, S., 1996. Myristoylated alanine-rich C kinase substrate (MARCKS) produces reversible inhibition of phospholipase C by sequestering phosphatidylinositol 4,5-biphosphate in lateral domains. J. Biol. Chem. 271 (42), 26184-26193.
26. 2+ on structure of phosphatidylcholine/phosphatidylserine bilayers. Biophys. J. 66, 382-393.
27. Golebiewska, U., Gambhir, A., Hangyás-Milháyné, G., Zaitseva, I., Rädler, J., McLaughlin, S., 2006. Membrane-bound basic peptides sequester multivalent (PIP2), but not monovalent (PS), acidic lipids. Biophys. J. 91, 588-599.
28. Haleva, E., Ben-Tal, N., Diamant, H., 2004. Increased concentration of polyvalent phospholipids in the adsorption domain of a charged protein. Biophys. J. 86, 2165-2178. (Pubitemid 38524407)
29. Hartwig, J.H., Thelen, M., Rosen, A., Janmey, P.A., Nairn, A.C., Aderem, A., 1992. MARCKS is an actin filament crosslinking protein regulated by protein kinase C and calcium-calmodulin. Nature 356, 618-622.
30. Hinderliter, A.K., Huang, J., Feigenson, G.F., 1994. Detection of phase separation in fluid phosphatidylserine/phosphatidylcholine mixtures. Biophys. J. 67, 1906-1911. (Pubitemid 24342062)
31. Jensen, T.R., Kjaer, K., 2001. Structural properties and interactions of thin films at the air-liquid interface explored by synchrotron X-ray scattering. Stud. Interface Sci. 11, 205-254.
32. Kim, J., Blackshear, P.J., Johnson, J.D., McLaughlin, S., 1994. Phosphorylation reverses the membrane association of peptides that correspond to the basic domains of MARCKS and neuromodulin. Biophys. J. 67, 227-237. (Pubitemid 24197888)
33. Krüger, P., Schalke, M.,Wang, Z., Notter, R.H., Dluhy, R.A., Lösche, M., 1999. Effect of hydrophobic surfactant peptides SP-B and SP-C on binary phospholipid monolayers. I. Fluorescence and dark-field microscopy. Biophys. J. 77, 943-952.
34. 2 plasmalemmal rafts, and regulate cell cortex actin dynamics through a common mechanism. J. Cell Biol. 149 (7), 1455-1471.
35. Lee, K.Y.C., Majewski, J., Kuhl, T.L., Howes, P.B., Kjaer, K., Lipp, M.M., Waring, A.J., Zasadzinski, J.A., Smith, G.S., 2001. Synchrotron X-ray study of lung surfactant-specific protein SP-B in lipid monolayers. Biophys. J. 81, 572-585. (Pubitemid 32605995)
36. Leventhal, I., Janmey, P.A., Cebers, A., 2008. Electrostatic contribution to the surface pressure of charged monolayers containing polyphosphoinositides. Biophys. J. 95, 1199-1205.
37. Lindblom, G., Orädd, G., 2007. Order and disorder in a liquid crystalline bilayer: pulsed field gradient NMR studies of lateral phase separation. J. Disper. Sci. Technol. 28, 55-61.
38. 2α- C2 domains adsorbed onto Langmuir monolayers of SOPC. Biophys. J. 89, 1861-1873.
39. McLaughlin, S., Aderem, A., 1995. The myristoyl-electrostatic switch: a modulator of reversible protein-membrane interactions. Trends Biochem. Sci. 20, 272-276.
40. 2 and proteins: interactions, organization, and information flow. Annu. Rev. Biophys. Biomol. Struct. 31, 151-175.
41. Möhwald, H., Baltes, H., Schwendler, M., Helm, C., Brezesinski, G., Haas, H., 1995. Phospholipid and protein monolayers. Jpn. J. Appl. Phys. 34, 3906-3913.
42. Murray, D., Arbuzova, A., Honig, B., McLaughlin, S., 2002. The role of electrostatic and nonpolar interactions in the association of peripheral proteins with membranes. Curr. Top. Membr. 52, 277-307.
43. Myat, M.M., Anderson, S., Allen, L.-H.H., Aderem, A., 1997. MARCKS regulates membrane ruffling and cell spreading. Curr. Biol. 7, 611-614.
44. Ohmori, S., Sakai, N., Shirai, Y., Yamamoto, H., Miyamoto, E., Shimizu, N., Saito, N., 2000. Importance of protein kinase C targeting for the phosphorylation of its substrate, myristoylated alanine-rich C-kinase substrate. J. Biol. Chem. 275 (34), 26449-26457.
45. Palsdottir, H., Hunte, C., 2004. Lipids in membrane protein structures. Biochim. Biophys. Acta 1666, 2-18.
46. Qin, Z., Cafiso, D.S., 1996. Membrane structure of protein kinase C and calmodulin binding domain of myristoylated alanine rich C kinase substrate determined by site-directed spin labeling. Biochemistry 35, 2917-2925. (Pubitemid 26086801)
47. Rauch, M.E., Ferguson, C.G., Prestwich, G.D., Cafiso, D.S., 2002. Myristoylated alanine rich C kinase substrate (MARCKS) sequesters spin-labeled phosphatidylinositol 4,5-biphosphate in lipid bilayers. J. Biol. Chem. 266, 14068-14076.
48. Rusu, L., Gambhir, A., McLaughlin, S., Rädler, J., 2004. Fluorescence correlation spectroscopy studies of peptide and protein binding to phospholipid vesicles. Biophys. J. 87, 1044-1053. (Pubitemid 39095083)
49. Schalke, M., Krüger, P., Weygand, M., Lösche, M., 2000. Submolecular organization of DMPA in surface monolayers: beyond the two-layer model. Biochim. Biophys. Acta 1464, 113-126.
50. Schalke, M., Lösche, M., 2000. Structural models of lipid surface monolayers from X-ray and neutron reflectivity measurements. Adv. Colloid Interface Sci. 88, 243-274.
51. Seki, K., Sheu, F.-S., Huang, K.-P., 1996. Binding of myristoylated alanine-rich protein kinase C substrate to phosphoinositides attenuates the phosphorylation by protein kinase C. Arch. Biochem. Biophys. 326 (2), 193-201.
52. Seykora, J.T., Myat, M.M., Allen, L.-A.H., Ravetch, J.V., Aderem, A., 1996. Molecular determinants of the myristoyl-electrostatic switch of MARCKS. J. Biol. Chem. 271 (31), 18797-18802.
53. Teif, V.B., Harries, D., Lando, D.Y., Ben-Shaul, A., 2008. Matrix formalism for site-specific binding of unstructured proteins to multicomponent lipid membranes. J. Pept. Sci. 14, 368-373.
54. Tzlil, S., Ben-Shaul, A., 2005. Flexible charged macromolecules on mixed fluid membranes: theory and Monte Carlo simulations. Biophys. J. 89, 2972-2987. (Pubitemid 41636054)
55. Vaknin, D., Kjaer, K., Als-Nielsen, J., Lösche, M., 1991. Structural properties of phosphatidylcholine in a monolayer at the air/water interface. Biophys. J. 59, 1325-1332.
56. Victor, K., Jacob, J., Cafiso, D.S., 1999. Interactions controlling the membrane binding of basic protein domains: phenylalanine and the attachment of the myristoylated alanine-rich C-kinase substrate protein to interfaces. Biochemistry 38, 12527-12536. (Pubitemid 29463247)
57. Wang, J., Arbuzova, A., Hangás-Milháyné, G., McLaughlin, S., 2001. The effector domain of myristoylated alanine-rich C kinase substrate binds strongly to phosphatidylinositol 4,5-biphosphate. J. Biol. Chem. 276 (7), 5012-5019.
58. Wang, J., Gambhir, A., Hangyás-Mihályné, G., Murray, D., Golebiewska, U., McLaughlin, S., 2002. Lateral sequestration of phosphatidylinositol 4,5-biphosphate by the basic effector domain of myristoylated alanine-rich C kinase substrate is due to nonspecific electrostatic interactions. J. Biol. Chem. 277 (37), 34401-34412.
59. Wang, J., Gambhir, A., McLaughlin, S., Murray, D., 2004. A computational model for the electrostatic sequestration of PI(4,5)P2 by membrane-adsorbed basic peptides. Biophys. J. 86, 1969-1986.
60. Weygand, M., Wetzer, B., Pum, D., Sleytr, U.B., Cuvillier, N., Kjaer, K., Howes, P.B., Lösche, M., 1999. Bacterial S-layer protein coupling to lipids: X-ray reflectivity and gracing incidence diffraction studies. Biophys. J. 76, 458-468. (Pubitemid 29202473)
61. Wohnsland, F., Schmitz, A.A.P., Steinmetz, M.O., Aebi, U., Vergères, G., 2000. Interaction between actin and the effector peptide of MARCKS-related protein. J. Biol. Chem. 275 (27), 20873s-20879s.
62. Zhang, W., Crocker, E., McLaughlin, S., Smith, S.O., 2003. Binding of peptides with basic and aromatic residues to bilayer membranes. J. Biol. Chem. 278 (24), 21459-21466.
63. Zhou, C., Garigapati, V., Robert, M.F., 1997. Short-chain phosphatidylinositol conformation and its relevance to phosphatidylinositol- specific phospholipase C. Biochemistry 36, 15925-15931. (Pubitemid 28027396)