Characterization of the myristoyl lipid modification of membrane-bound GCAP-2 by 2H solid-state NMR spectroscopy

Biochimica et Biophysica Acta - Biomembranes

Volumn 1768, Issue 12, 2007, Pages 3171-3181

  Vogel, Alexander ^a   Schröder, Thomas ^a   Lange, Christian ^a   Huster, Daniel ^a  

^a MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

Author keywords

2H solid state NMR; Guanylate cyclase activating protein; Lipid modification; Membrane binding; Myristoylation; Neuronal calcium sensor; Order parameter

Indexed keywords

CALCIUM SENSING RECEPTOR; DIMYRISTOYLPHOSPHATIDYLCHOLINE; GUANYLATE CYCLASE; GUANYLATE CYCLASE ACTIVATING PROTEIN 2; MEMBRANE LIPID; MYRISTIC ACID; PHOSPHOLIPID; UNCLASSIFIED DRUG;

ARTICLE; BINDING ASSAY; CALCIUM BINDING; DEUTERON NUCLEAR MAGNETIC RESONANCE; ELECTRICITY; LIPID MEMBRANE; MEMBRANE BINDING; MYRISTYLATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PHOTOTRANSDUCTION; PRIORITY JOURNAL; PROTEIN ANALYSIS;

DEUTERIUM; GUANYLATE CYCLASE-ACTIVATING PROTEINS; LIPID METABOLISM; MAGNETIC RESONANCE SPECTROSCOPY; MEMBRANE PROTEINS; MYRISTIC ACID;

VERTEBRATA;

EID: 36849092841     PISSN: 00052736     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamem.2007.08.024     Document Type: Article

References (64)

1. 2+-binding protein activating photoreceptor guanylyl cyclase. J. Biol. Chem. 270 (1995) 25200-25206
2. Gorczyca W.A., Gray-Keller M.P., Detwiler P.B., and Palczewski K. Purification and physiological evaluation of a guanylate cyclase activating protein from retinal rods. Proc. Natl. Acad. Sci. U. S. A. 91 (1994) 4014-4018
3. Palczewski K., Subbaraya I., Gorczyca W.A., Helekar B.S., Ruiz C.C., Ohguro H., Huang J., Zhao X.Y., Crabb J.W., Johnson R.S., Walsh K.A., Gray-Keller M.P., Detwiler P.B., and Baehr W. Molecular-cloning and characterization of retinal photoreceptor guanylyl cyclase-activating protein. Neuron 13 (1994) 395-404
4. Frins S., Bönigk W., Müller F., Kellner R., and Koch K.W. Functional characterization of a guanylyl cyclase-activating protein from vertebrate rods - cloning, heterologous expression, and localization. J. Biol. Chem. 271 (1996) 8022-8027
5. Haeseleer F., Sokal I., Li N., Pettenati M., Rao N., Bronson D., Wechter R., Baehr W., and Palczewski K. Molecular characterization of a third member of the guanylyl cyclase-activating protein subfamily. J. Biol. Chem. 274 (1999) 6526-6535
6. Laura R.P., Dizhoor A.M., and Hurley J.B. The membrane guanylyl cyclase, retinal guanylyl cyclase-1, is activated through its intracellular domain. J. Biol. Chem. 271 (1996) 11646-11651
7. Koch K.W. Purification and identification of photoreceptor guanylate cyclase. J. Biol. Chem. 266 (1991) 8634-8637
8. Shyjan A.W., Desauvage F.J., Gillett N.A., Goeddel D.V., and Lowe D.G. Molecular-cloning of a retina-specific membrane guanylyl cyclase. Neuron 9 (1992) 727-737
9. Lowe D.G., Dizhoor A.M., Liu K., Gu Q., Spencer M., Laura R., Lu L., and Hurley J.B. Cloning and expression of a second photoreceptor-specific membrane retina guanylyl cyclase (RetGC), RetGC-2. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 5535-5539
10. Yang R.B., Foster D.C., Garbers D.L., and Fulle H.J. 2 Membrane forms of guanylyl cyclase found in the eye. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 602-606
11. Koch K.W., and Stryer L. Highly cooperative feedback control of retinal rod guanylate cyclase by calcium ions. Nature 334 (1988) 64-66
12. Pugh E.N., and Lamb T.D. Cyclic-GMP and calcium - the internal messengers of excitation and adaptation in vertebrate photoreceptors. Vis. Res. 30 (1990) 1923-1948
13. Gray-Keller M.P., and Detwiler P.B. The calcium feedback signal in the phototransduction cascade of vertebrate rods. Neuron 13 (1994) 849-861
14. Fain G.L., Matthews H.R., Cornwall M.C., and Koutalos Y. Adaptation in vertebrate photoreceptors. Physiol. Rev. 81 (2001) 117-151
15. Mendez A., Burns M.E., Sokal I., Dizhoor A.M., Baehr W., Palczewski K., Baylor D.A., and Chen J. Role of guanylate cyclase-activating proteins (GCAPs) in setting the flash sensitivity of rod photoreceptors. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 9948-9953
16. Burns M.E., Mendez A., Chen J., and Baylor D.A. Dynamics of cyclic GMP synthesis in retinal rods. Neuron 36 (2002) 81-91
17. Olshevskaya E.V., Hughes R.E., Hurley J.B., and Dizhoor A.M. Calcium binding, but not a calcium-myristoyl switch, controls the ability of guanylyl cyclase-activating protein GCAP-2 to regulate photoreceptor guanylyl cyclase. J. Biol. Chem. 272 (1997) 14327-14333
18. Wilcox C., Hu J.S., and Olson E.N. Acylation of proteins with myristic acid occurs cotranslationally. Science 238 (1987) 1275-1278
19. Neubert T.A., Johnson R.S., Hurley J.B., and Walsh K.A. The rod transducin alpha subunit amino terminus is heterogeneously fatty acylated. J. Biol. Chem. 267 (1992) 18274-18277
20. Dizhoor A.M., Ericsson L.H., Johnson R.S., Kumar S., Olshevskaya E., Zozulya S., Neubert T.A., Stryer L., Hurley J.B., and Walsh K.A. The NH2 terminus of retinal recoverin is acylated by a small family of fatty-acids. J. Biol. Chem. 267 (1992) 16033-16036
21. Towler D.A., Adams S.P., Eubanks S.R., Towery D.S., Jacksonmachelski E., Glaser L., and Gordon J.I. Purification and characterization of yeast myristoyl-CoA - protein N-myristoyltransferase. Proc. Natl. Acad. Sci. U. S. A. 84 (1987) 2708-2712
22. Duronio R.J., Towler D.A., Heuckeroth R.O., and Gordon J.I. Disruption of the yeast N-myristoyl transferase gene causes recessive lethality. Science 243 (1989) 796-800
23. Glover C.J., Goddard C., and Felsted R.L. N-myristoylation of p60src. Identification of a myristoyl-CoA:glycylpeptide N-myristoyltransferase in rat tissues. Biochem. J. 250 (1988) 485-491
24. Tanaka T., Ames J.B., Harvey T.S., Stryer L., and Ikura M. Sequestration of the membrane-targeting myristoyl group of recoverin in the calcium-free state. Nature 376 (1995) 444-447
25. Flaherty K.M., Zozulya S., Stryer L., and Mckay D.B. 3-Dimensional structure of recoverin, A Calcium Sensor in Vision. Cell 75 (1993) 709-716
26. Hughes R.E., Brzovic P.S., Klevit R.E., and Hurley J.B. Calcium-dependent solvation of the myristoyl group of recoverin. Biochemistry 34 (1995) 11410-11416
27. Zozulya S., and Stryer L. Calcium-myristoyl protein switch. Proc. Natl. Acad. Sci. U. S. A. 89 (1992) 11569-11573
28. Ladant D. Calcium and membrane-binding properties of bovine neurocalcin-delta expressed in Escherichia-coli. J. Biol. Chem. 270 (1995) 3179-3185
29. Kobayashi M., Takamatsu K., Saitoh S., and Noguchi T. Myristoylation of hippocalcin is linked to its calcium-dependent membrane association properties. J. Biol. Chem. 268 (1993) 18898-18904
30. 2+ signal transduction. J. Biol. Chem. 274 (1999) 30258-30265
31. Hwang J.Y., and Koch K.W. Calcium- and myristoyl-dependent properties of guanylate cyclase-activating protein-1 and protein-2. Biochemistry 41 (2002) 13021-13028
32. Ames J.B., Dizhoor A.M., Ikura M., Palczewski K., and Stryer L. Three-dimensional structure of guanylyl cyclase activating protein-2, a calcium-sensitive modulator of photoreceptor guanylyl cyclases. J. Biol. Chem. 274 (1999) 19329-19337
33. Stephen R., Paiczewski K., and Sousa M.C. The crystal structure of GCAP3 suggests molecular mechanism of GCAP-linked cone dystrophies. J. Mol. Biol. 359 (2006) 266-275
34. Pool C.T., and Thompson T.E. Chain length and temperature dependence of the reversible association of model acylated proteins with lipid bilayers. Biochemistry 37 (1998) 10246-10255
35. Peitzsch R.M., and McLaughlin S. Binding of acylated peptides and fatty acids to phospholipid vesicles: pertinence to myristoylated proteins. Biochemistry 32 (1993) 10436-10443
36. McLaughlin S., and Aderem A. The myristoyl-electrostatic switch: a modulator of reversible protein-membrane interactions. Trends Biochem. Sci. 20 (1995) 272-276
37. Lange C., and Koch K.W. Calcium-dependent binding of recoverin to membranes monitored by surface plasmon resonance spectroscopy in real time. Biochemistry 36 (1997) 12019-12026
38. Brown M.F., Lope-Piedrafita S., Martinez G.V., and Petrache H.I. Solid-state deuterium NMR spectroscopy of membranes. In: Webb G. (Ed). Modern Magnetic Resonance (2006), Springer, Heidelberg 241-252
39. Valentine K.G., Mesleh M.F., Opella S.J., Ikura M., and Ames J.B. Structure, topology, and dynamics of myristoylated recoverin bound to phospholipid bilayers. Biochemistry 42 (2003) 6333-6340
40. Thennarasu S., Lee D.K., Tan A., Kari U.P., and Ramamoorthy A. Antimicrobial activity and membrane selective interactions of a synthetic lipopeptide MSI-843. Biochim. Biophys. Acta 1711 (2005) 49-58
41. Vogt T.C., Killian J.A., and de Kruijff B. Structure and dynamics of the acyl chain of a transmembrane polypeptide. Biochemistry 33 (1994) 2063-2070
42. Reuther G., Tan K.-T., Vogel A., Nowak C., Kuhlmann J., Waldmann H., and Huster D. The lipidated membrane anchor of the N-ras protein shows an extensive dynamics as revealed by solid-state NMR. J. Am. Chem. Soc. 128 (2006) 13840-13846
43. Reuther G., Tan K.-T., Köhler J., Nowak C., Pampel A., Arnold K., Kuhlmann J., Waldmann H., and Huster D. Structural model of the membrane-bound C terminus of lipid-modified human N-ras protein. Angew. Chem., Int. Ed. Engl. 45 (2006) 5387-5390
44. Huster D., Kuhn K., Kadereit D., Waldmann H., and Arnold K. High resolution magic angle spinning NMR for the investigation of a ras lipopeptide in a lipid bilayer. Angew. Chem., Int. Ed. Engl. 40 (2001) 1056-1058
45. Huster D., Vogel A., Katzka C., Scheidt H.A., Binder H., Dante S., Gutberlet T., Zschörnig O., Waldmann H., and Arnold K. Membrane insertion of a lipidated ras peptide studied by FTIR, solid-state NMR, and neutron diffraction spectroscopy. J. Am. Chem. Soc. 125 (2003) 4070-4079
46. 2H solid-state NMR. J. Am. Chem. Soc. 127 (2005) 12263-12272
47. 2H solid-state NMR and molecular dynamics simulations. Biophys. J. 93 (2007) 2697-2712
48. Anderson R.E., and Maude M.B. Phospholipids of bovine rod outer segments. Biochemistry 9 (1970) 3624-&
49. Rudolph R., Böhm G., Lilie H., and Jaenicke R. Folding proteins. In: Creighton T. (Ed). Protein Function: A Practical Approach (1997), IRL Oxford University Press, Oxford 57-99
50. Duronio R.J., Jackson-Machelski E., Heuckeroth R.O., Olins P.O., Devine C.S., Yonemoto W., Slice L.W., Taylor S.S., and Gordon J.I. Protein N-myristoylation in Escherichia coli: reconstitution of a eukaryotic protein modification in bacteria. Proc. Natl. Acad. Sci. U. S. A. 87 (1990) 1506-1510
51. 2+-sensors guanylate cyclase-activating protein 1 and 2. Biochim. Biophys. Acta 1600 (2002) 111-117
52. Davis J.H., Jeffrey K.R., Bloom M., Valic M.I., and Higgs T.P. Quadrupolar echo deuteron magnetic resonance spectroscopy in ordered hydrocarbon chains. Chem. Phys. Lett. 42 (1976) 390-394
53. McCabe M.A., and Wassall S.R. Fast-Fourier-transform DePaking. J. Magn. Reson., Ser. B 106 (1995) 80-82
54. Huster D., Arnold K., and Gawrisch K. Influence of docosahexaenoic acid and cholesterol on lateral lipid organization in phospholipid membranes. Biochemistry 37 (1998) 17299-17308
55. 2H NMR spectroscopy. Biophys. J. 79 (2000) 3172-3192
56. Barré P., Zschörnig O., Arnold K., and Huster D. Structural and dynamical changes of the bindin B18 peptide upon binding to lipid membranes. A solid-state NMR study. Biochemistry 42 (2003) 8377-8386
57. Koenig B.W., Ferretti J.A., and Gawrisch K. Site-specific deuterium order parameters and membrane-bound behavior of a peptide fragment from the intracellular domain of HIV-1 gp41. Biochemistry 38 (1999) 6327-6334
58. Henzler-Wildman K.A., Martinez G.V., Brown M.F., and Ramamoorthy A. Perturbation of the hydrophobic core of lipid bilayers by the human antimicrobial peptide LL-37. Biochemistry 43 (2004) 8459-8469
59. Huster D., Yao X., Jakes K.S., and Hong M. Conformational changes of colicin Ia channel-forming domain upon membrane binding: a solid-state NMR study. Biochim. Biophys. Acta 1561 (2002) 159-170
60. 2H and 14N quadrupolar relaxation. J. Chem. Phys. 77 (1982) 1576-1799
61. Otten D., Brown M.F., and Beyer K. Softening of membrane bilayers by detergents elucidated by deuterium NMR spectroscopy. J. Phys. Chem., B 104 (2000) 12119-12129
62. Silvius J.R., and l'Heureux F. Fluorimetric evaluation of the affinities of isoprenylated peptides for lipid bilayers. Biochemistry 33 (1994) 3014-3022
63. Tanford C. The Hydrophobic Effect: Formation of Micelles and Biological Membranes (1980), John Wiley & Sons, New York
64. Buser C.A., Sigal C.T., Resh M.D., and McLaughlin S. Membrane binding of myristoylated peptides corresponding to the NH2 terminus of Src. Biochemistry 33 (1994) 13093-13101