Determination of the contribution of the myristoyl group and hydrophobic amino acids of recoverin on its dynamics of binding to lipid monolayers

Biophysical Journal

Volumn 93, Issue 6, 2007, Pages 2069-2082

  Desmeules, Philippe ^a,b   Penney, Sara Édith ^a,b   Desbat, Bernard ^c   Salesse, Christian ^a,b  

^a LAVAL UNIVERSITY   (Canada)

^b UNIVERSITÉ LAVAL   (Canada)

^c UNIVERSITÉ DE BORDEAUX   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; CALCIUM; MYRISTIC ACID; RECOVERIN; TRYPSIN;

ADSORPTION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM BINDING; CONTROLLED STUDY; HYDROPHOBICITY; INFRARED RADIATION; LIPID MONOLAYER; MEASUREMENT; MEMBRANE BINDING; MOLECULAR DYNAMICS; MYRISTYLATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PARAMETER; PHOSPHOLIPID MEMBRANE; PROTEIN CONFORMATION; PROTEIN LIPID INTERACTION; RETINA ROD; SIMULATION; SPECTROSCOPY; SURFACE PROPERTY;

EID: 34548754512     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.106.103481     Document Type: Article

References (87)

1. Kinnunen, P. K. J., A. Kõiv, J. Y. A. Lehtonen, M. Rytömaa, and P. Mustonen. 1994. Lipid dynamics and peripheral interactions of proteins with membrane surfaces. Chem. Phys. Lipids. 73:181-207.
2. Marsh, D., and T. Páli. 2004. The protein-lipid interface: perspectives from magnetic resonance and crystal structures. Biochim. Biophys. Acta. 1666:118-141.
3. Grenier, S., P. Desmeules, A. K. Dutta, A. Yamazaki, and C. Salesse. 1998. Determination of the depth of penetration of the α subunit of retinal G protein in membranes: a spectroscopic study. Biochim. Biophys. Acta. 1370:199-206.
4. Arbuzova, A., A. A. P. Schmitz, and G. Vergères. 2002. Cross-talk unfolded: MARKS proteins. Biochem. J. 362:1-12.
5. Desmeules, P., M. Grandbois, V. A. Bonderenko, A. Yamazaki, and C. Salesse. 2002. Measurement of membrane binding between recoverin, a calcium-myristoyl switch protein, and lipid bilayers by AFM-based force spectroscopy. Biophys. J. 82:3343-3350.
6. Meister, A., C. Nicolini, H. Waldmann, J. Kuhlmann, A. Kerth, R. Winter, and A. Blume. 2006. Insertion of lipidated Ras proteins into lipid monolayers studied by infrared reflection absorption spectroscopy (IRRAS). Biophys. J. 91:1388-1401.
7. Duronio, R. J., E. Jackson-Machelski, R. O. Heuckeroth, P. O. Olins, C. S. Devine, W. Yonemoto, L. W. Slice, S. S. Taylor, and J. I. Gordon. 1990. Protein N-myristoylation in Escherichia coli: reconstitution of a eukaryotic protein modification in bacteria. Proc. Natl. Acad. Sci. USA. 87:1506-1510.
8. Dunphy, J. T., and M. E. Linder. 1998. Signaling functions of protein palmitoylation. Biochim. Biophys. Acta. 1436:245-261.
9. Resh, M. D. 1999. Fatty acylation of proteins: new insights into membrane targeting of myristoylated and palmitoylated proteins. Biochim. Biophys. Acta. 1451:1-16.
10. Resh, M. D. 2004. Membrane targeting of lipid modified signal transduction proteins. Subcell. Biochem. 37:217-232.
11. McLaughlin, S., and A. Aderem. 1995. The myristoyl-electrostatic switch: a modulator of reversible protein-membrane interactions. Trends Biochem. Sci. 20:272-276.
12. 2+-binding proteins, recoverin and GCAP-2. Adv. Exp. Med. Biol. 514:333-348.
13. Ames, J. B., T. Tanaka, L. Stryer, and M. Ikura. 1996. Portrait of a myristoyl switch protein. Curr. Opin. Struct. Biol. 6:432-438.
14. Dizhoor, A. M., S. Ray, S. Kumar, G. Niemi, M. Spencer, D. Brolley, K. A. Walsh, P. P. Philipov, J. B. Hurley, and L. Stryer. 1991. Recoverin: a calcium sensitive activator of retinal rod guanylate cyclase. Science. 251:915-918.
15. Bazhin, A. V., D. Schadendorf, P. P. Philippov, and S. B. Eichmüller. 2006. Recoverin as a cancer-retina antigen. Cancer Immunol. Immunother. 56:110-116.
16. 2+-induced extrusion of the myristoyl group of recoverin. J. Biol. Chem. 270:30909-30913.
17. Flaherty, K. M., S. Zozulya, L. Stryer, and D. B. McKay. 1993. Three-dimensional structure of recoverin, a calcium sensor in vision. Cell. 75:709-716.
18. Burgoyne, R. D. 2004. The neuronal calcium-sensor proteins. Biochim. Biophys. Acta. 1742:59-68.
19. Dizhoor, A. M., L. H. Ericsson, R. S. Johnson, S. Kumar, E. Olshevskaya, S. Zozulya, T. A. Neubert, L. Stryer, J. B. Hurley, and K. A. Walsh. 1992. The NH2 terminus of retinal recoverin is acylated by a small family of fatty acids. J. Biol. Chem. 267:16033-16036.
20. 2+-dependent membrane interaction. Science. 259:829-832.
21. Zozulya, S., and L. Stryer. 1992. Calcium-myristoyl protein switch. Proc. Natl. Acad. Sci. USA. 89:11569-11573.
22. 2+-dependent interaction of recoverin with rhodopsin kinase. J. Biol. Chem. 270:18060-18066.
23. Gray-Keller, M. P., A. S. Polans, K. Palczewski, and P. B. Detwiler. 1993. The effect of recoverin-like calcium-binding proteins on the photoresponse of retinal rods. Neuron. 10:523-531.
24. Kawamura, S., O. Hisatomi, S. Kayada, F. Tokunaga, and C. H. Kuo. 1993. Recoverin has S-modulin activity in frog rods. J. Biol. Chem. 268:14579-14582.
25. Klenchin, V. A., P. D. Calvert, and M. D. Bownds. 1995. Inhibition of rhodopsin kinase by recoverin. Further evidence for a negative feedback system in phototransduction. J. Biol. Chem. 270:16147-16152.
26. Senin, I. I., A. A. Zargarov, A. M. Alekseev, E. N. Gorodovikova, V. M. Lipkin, and P. P. Philippov. 1995. N-myristoylation of recoverin enhances its efficiency as an inhibitor of rhodopsin kinase. FEBS Lett. 376:87-90.
27. Makino, C. L., R. L. Dodd, J. Chen, M. E. Burns, A. Roca, M. I. Simon, and D. A. Baylor. 2004. Recoverin regulates light-dependent phosphodiesterase activity in retinal rods. J. Gen. Physiol. 123:729-741.
28. Ames, J. B., R. Ishima, T. Tanaka, J. I. Gordon, L. Stryer, and M. Ikura. 1997. Molecular mechanics of calcium-myristoyl switches. Nature. 389:198-202.
29. Hughes, R. E., P. S. Brzovic, R. E. Klevit, and J. B. Hurley. 1995. Calcium-dependent solvation of the myristoyl group of recoverin. Biochemistry. 34:11410-11416.
30. Desmeules, P. 2006. Overexpression and study of the parameters responsible for the binding of acylated proteins to membranes and optimization of recoverin myristoylation in E. coli. PhD thesis, Université du Québec à Trois-Rivières, Canada.
31. Ames, J. B., T. Tanaka, L. Stryer, and M. Ikura. 1994. Secondary structure of myristoylated recoverin determined by three-dimensional heteronuclear NMR: implications for the calcium-myristoyl switch. Biochemistry. 33:10743-10753.
32. Tanaka, T., J. B. Ames, T. S. Harvey, L. Stryer, and M. Ikura. 1995. Sequestration of the membrane-targeting myristoyl group of recoverin in the calcium-free state. Nature. 376:444-447.
33. Permyakov, S. E., A. M. Cherskaya, L. A. Wasserman, T. I. Khoklova, I. I. Senin, A. A. Kargarov, D. V. Zinchenko, E. Y. Zernii, V. M. Lipkin, P. P. Philippov, V. N. Uversky, and E. A. Permyakov. 2003. Recoverin is a zinc-binding protein. J. Proteome Res. 2:51-57.
34. Peitzsch, R. M., and S. McLaughlin. 1993. Binding of acylated peptides and fatty acids to phospholipid vesicles: pertinence to myristoylated proteins. Biochemistry. 32:10436-10443.
35. Pool, C. T., and T. E. Thompson. 1998. Chain length and temperature dependence of the reversible association of model acylated proteins with lipid bilayers. Biochemistry. 37:10246-10255.
36. Murray, D., N. Ben-Tal, B. Honig, and S. McLaughlin. 1997. Electrostatic interaction of myristoylated recoverin with membranes: simple physics, complicated biology. Structure. 15:985-989.
37. Silvius, J. R., and M. J. Zuckermann. 1993. Interbilayer transfer of phospholipid-anchored macromolecules via monomer diffusion. Biochemistry. 32:3153-3161.
38. Finkelstein, A. V., and J. Janin. 1989. The price of lost freedom: entropy of bimolecular complex formation. Protein Eng. 3:1-3.
39. Dynarowicz-Latka, P., A. Dhanabalan, and O. N. Oliveira, Jr. 2001. Modern physicochemical research on Langmuir monolayers. Adv. Colloid Interface Sci. 91:221-293.
40. Mendelsohn, R., and C. R. Flach. 2002. Infrared reflection-absorption spectroscopy of lipids, peptides, and protein in aqueous monolayers. In Current Topics in Membranes: Peptide-Lipid Interaction, Vol. 52. S. A. Simon and T. J. McIntosh, editors. Academic Press, New York.
41. Heitz, F., and N. Van Mau. 2002. Protein structural changes induced by their uptake at interfaces. Biochim. Biophys. Acta. 1597:1-11.
42. Buffeteau, T., B. Desbat, and J. M. Turlet. 1991. Polarization modulation FT-IR spectroscopy of surfaces and ultra-thin films: experimental procedure and quantitative analysis. Appl. Spectrosc. 45:380-389.
43. Blaudez, D., T. Buffeteau, J. C. Cornut, B. Desbat, N. Escafre, and M. Pézolet. 1994. Polarization modulation FTIR spectroscopy at the air-water interface. Thin Solid Films. 242:146-150.
44. Cornut, I., B. Desbat, J.-M. Turlet, and J. Dufourcq. 1996. In situ study by polarization modulated Fourier transform infrared spectroscopy of the structure and orientation of lipids and amphipathic peptides at the air-water interface. Biophys. J. 70:305-312.
45. Flach, C. R., F. G. Prendergast, and R. Mendelsohn. 1996. Infrared reflection-absorption of melittin interaction with phospholipid monolayers at the air/water interface. Biophys. J. 70:539-546.
46. Gallant, J., B. Desbat, D. Vaknin, and C. Salesse. 1998. Polarization-modulated infrared spectroscopy and x-ray reflectivity of photosystem II core complex at the gas-water interface. Biophys. J. 75:2888-2899.
47. Bellet-Amalric, E., D. Blaudez, B. Desbat, F. Graner, F. Gauthier, and A. Renault. 2000. Interaction of the third helix of Antennapedia homeodomain and a phospholipid monolayer, studied by ellipsometry and PM-IRRAS at the air-water interface. Biochim. Biophys. Acta. 1467:131-143.
48. Castano, S., B. Desbat, and J. Dufourcq. 2000. Ideally amphipathic β-sheeted peptides at interfaces: structure, orientation, affinities for lipids and hemolytic activity of KLmK peptides. Biochim. Biophys. Acta. 1463:65-80.
49. j (i=2j) peptides. Biochim. Biophys. Acta. 1416:176-194.
50. Castano, S., D. Blaudez, B. Desbat, J. Dufourcq, and H. Wróblewski. 2002. Secondary structure of spiralin in solution, at the air/water interface, and in interaction with lipid monolayers. Biochim. Biophys. Acta. 1562:45-56.
51. Lavoie, H., B. Desbat, D. Vaknin, and C. Salesse. 2002. Structure of rhodopsin in monolayers at the air-water interface: a PM-IRRAS and x-ray reflectivity study. Biochemistry. 41:13424-13434.
52. 2+ aqueous monolayers: a Brewster angle microscopy/infrared reflection absorption spectroscopy study. Biophys. J. 74:3273-3281.
53. Gericke, A., and H. Hühnerfuss. 1994. IR reflection absorption spectroscopy: a versatile tool for studying interfacial enzymatic processes. Chem. Phys. Lipids. 74:205-210.
54. Grandbois, M., B. Desbat, D. Blaudez, and C. Salesse. 1999. Polarization-modulated infrared absorption spectroscopy measurement of phospholipid monolayer hydrolysis by phospholipase C. Langmuir. 15:6594-6597.
55. Grandbois, M., B. Desbat, and C. Salesse. 2000. Monitoring of phospholipid monolayer hydrolysis by phospholipase A2 by use of polarization-modulated Fourier transform infrared spectroscopy. Biophys. Chem. 88:127-135.
56. 2 with polarization-modulated infrared reflection absorption spectroscopy. Langmuir. 21:1051-1054.
57. Ray, S., S. Zozulya, G. A. Niemi, K. M. Flaherty, D. Brolley, A. M. Dizhoor, D. B. McKay, J. B. Hurley, and L. Stryer. 1992. Cloning, expression, and crystallization of recoverin, a calcium sensor in vision. Proc. Natl. Acad. Sci. USA. 89:5705-5709.
58. Desmeules, P., S.-E. Penney, and C. Salesse. 2006. Single-step purification of myristoylated and nonmyristoylated recoverin and substrate dependence of myristoylation level. Anal. Biochem. 349:25-32.
59. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
60. Pitcher III, W. H., S. L. Keller, and W. H. Huestis. 2002. Interaction of nominally soluble proteins with phospholipid monolayers at the air-water interface. Biochim. Biophys. Acta. 154:107-113.
61. Blaudez, D., J.-M. Turlet, J. Dufourcq, D. Bard, T. Buffeteau, and B. Desbat. 1996. Investigation at the air/water interface using polarization modulation IR spectroscopy. J. Chem. Soc. Faraday Trans. 92:525-530.
62. Saccani, J., T. Buffeteau, B. Desbat, and B. D. Saccani. 2003. Increasing detectivity of polarization modulation infrared reflection-absorption spectroscopy for the study of ultrathin films deposited on various substrates. Appl. Spectrosc. 57:1260-1265.
63. Buffeteau, T., and B. Desbat. 1989. Thin-film optical constants determined from infrared reflectance and transmittance measurements. Appl. Spectrosc. 43:1027-1032.
64. Berreman, D. W. 1972. Optics in stratified and anisotropic media: 4 X 4-matrix formulation. J. Opt. Soc. Am. 62:502-510.
65. -1. Appl. Spectrosc. 50:1047-1057.
66. Buffeteau, T., E. Le Calvez, S. Castano, B. Desbat, D. Blaudez, and J. Dufourcq. 2000. Anisotropic optical constants of α-helix and β-sheet secondary structures in the infrared. J. Phys. Chem. B. 104:4537-4544.
67. Valentine, K. G., M. F. Mesleh, S. J. Opella, M. Ikura, and J. B. Ames. 2003. Structure, topology and dynamics of myristoylated recoverin bound to phospholipids bilayers. Biochemistry. 42:6334-6340.
68. Kataoka, M., K. Mihara, and F. Tokunaga. 1993. Recoverin alters its surface properties depending on both calcium-binding and N-terminal myristoylation. J. Biochem. (Tokyo). 114:535-540.
69. Cho, D., G. Narsimhan, and E. I. Franses. 1997. Adsorption dynamics of native and pentylated bovine serum albumin at air-water interfaces: surface concentration/surface pressure measurements. J. Colloid Interface Sci. 191:312-325.
70. Xia, X.-F., F. Wang, and S.-F. Sui. 2001. Effect of phospholipid on trichosanthin adsorption at the air-water interface. Biochim. Biophys. Acta. 1515:1-11.
71. Wierenga, P. A., M. B. J. Meinders, M. R. Egmond, F. A. G. J. Voragen, and H. H. de Jongh. 2003. Protein exposed hydrophobicity reduces the kinetic barrier for adsorption of ovalbumin to the air-water interface. Langmuir. 19:8964-8970.
72. Lange, C., and K. W. Koch. 1997. Calcium-dependent binding of recoverin to membranes monitored by surface plasmon resonance spectroscopy in real time. Biochemistry. 36:12019-12026.
73. Dousseau, F., and M. Pézolet. 1990. Determination of the secondary structure content of proteins in aqueous solutions from their amide I and amide II infrared bands. Comparison between classical and partial least-squares methods. Biochemistry. 29:8771-8779.
74. Surewicz, W. K., H. H. Mantsch, and D. Chapman. 1993. Determination of protein secondary structure by Fourier transform infrared spectroscopy: a critical assessment. Biochemistry. 32:389-394.
75. Goormaghtigh, E., V. Cabiaux, and J.-M. Ruysschaert. 1994. Determination of soluble and membrane protein structure by Fourier transform infrared spectroscopy. In Subcellular Biochemistry: Physicochemical Methods in the Study of Biomembranes, Vol. 23. H. J. Hildelson and G. B. Ralston, editors. Plenum Press, New York.
76. Flach, C. R., J. W. Brauner, J. W. Taylor, R. C. Baldwin, and R. Mendelsohn. 1994. External reflection FTIR of peptide monolayer films in situ at the air/water interface: experimental design, spectrastructure correlations and effects of hydrogen-deuterium exchange. Biophys. J. 67:402-410.
77. Labrecque, J. 1995. Infrared spectroscopic study of the interaction of polylysine with phosphatidic acid in monolayers. MSc thesis, Université Laval, Québec, Canada.
78. Akiyama, M. 1984. Internal field correction for infrared band intensity measured in solutions. J. Chem. Phys. 81:5229-5230.
79. 2+? Surface plasmon resonance and FTIR spectroscopic studies. Biochemistry. 39:14495-14503.
80. 2+ binding proteins. Biochemistry. 30:9681-9686.
81. 2+ binding. Biochemistry. 28:1294-1301.
82. Surewicz, W. K., and H. H. Mantsch. 1988. New insight into protein secondary structure from resolution-enhanced infrared spectra. Biochim. Biophys. Acta. 952:115-130.
83. Johnson, W. C., Jr., K. Palczewski, W. A. Gorczyca, J. H. Riazance-Lawrence, D. Witkowska, and A. S. Polans. 1997. Calcium binding to recoverin: implication for secondary structure and membrane association. Biochim. Biophys. Acta. 1342:164-174.
84. Ulrich, W.-P., and H. Vogel. 1999. Polarization-modulated FTIR spectroscopy of lipid/gramicidin monolayers at the air/water interface. Biophys. J. 76:1639-1647.
85. Ugarte, M., and N. N. Osborne. 2001. Zinc in the retina. Prog. Neurobiol. 64:219-249.
86. Shuster, T. A., A. K. Nagy, D. C. Conly, and D. B. Farber. 1992. Direct zinc binding to purified rhodopsin and discmembranes. Biochem. J. 282:123-128.
87. Francis, S. H., J. L. Colbran, L. M. McAllister-Lucas, and J. D. Corbin. 1994. Zinc interaction and conserved motifs of the cGMP-binding cGMP-specific phosphodiesterase suggest that it is a zinc hydrolase. J. Biol. Chem. 269:22477-22480.