Myristoylation exerts direct and allosteric effects on gα conformation and dynamics in solution

Biochemistry

Volumn 51, Issue 9, 2012, Pages 1911-1924

  Preininger, Anita M ^a   Kaya, Ali I ^a   Gilbert, James A ^a   Busenlehner, Laura S ^b   Armstrong, Richard N ^a   Hamm, Heidi E ^a  

^a VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^b UNIVERSITY OF ALABAMA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATED PROTEINS; ALLOSTERIC EFFECT; AMINO TERMINUS; FLUORESCENCE QUENCHING; G PROTEIN; G PROTEIN COUPLED RECEPTORS; GTP BINDING; GUANINE RINGS; HETEROTRIMERIC G PROTEINS; HYDROGEN-DEUTERIUM EXCHANGE; MEMBRANE LOCALIZATION; MYRISTOYLATION; N-TERMINALS; NUCLEOTIDE BINDING; NUCLEOTIDE EXCHANGE; PROTEIN STRUCTURES;

ACYLATION; AMIDES; DEUTERIUM; FLUORESCENCE; HYDROGEN; NUCLEOTIDES;

PROTEINS;

DEUTERIUM; GUANINE; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; HYDROGEN;

ALLOSTERISM; ALPHA HELIX; ARTICLE; CONTROLLED STUDY; DYNAMICS; FLUORESCENCE; MYRISTYLATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; SOLUTION AND SOLUBILITY;

ALLOSTERIC REGULATION; ANIMALS; DEUTERIUM EXCHANGE MEASUREMENT; GTP-BINDING PROTEIN ALPHA SUBUNITS, GI-GO; MODELS, MOLECULAR; MYRISTIC ACID; PROTEIN CONFORMATION; RATS; SIGNAL TRANSDUCTION; SOLUTIONS;

EID: 84857862291     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi201472c     Document Type: Article

References (67)

1. Noel, J. P., Hamm, H. E., and Sigler, P. B. (1993) The 2.2 Å crystal structure of transducin-α complexed with GTPγS Nature 366, 654-663
2. iα1 and the Mechanism of GTP Hydrolysis Science 265, 1405-1412
3. iα1 Induced by GTP Hydrolysis Science 270, 954-960
4. - Nature 372, 276-279
5. 2+: A Crystallographic Titration Experiment Biochemistry 37, 14376-14385
6. 2 adrenergic receptor-Gs protein complex Nature 477, 549-555
7. Lambright, D. G., Noel, J. P., Hamm, H. E., and Sigler, P. B. (1994) Structural determinants for activation of the α-subunit of a heterotrimeric G protein Nature 369, 621-628
8. Lambright, D. G., Sondek, J., Bohm, A., Skiba, N. P., Hamm, H. E., and Sigler, P. B. (1996) The 2.0 Å crystal structure of a heterotrimeric G protein Nature 379, 311-319
9. 2 Cell 83, 1047-1058
10. iα1: Stabilization of the Transition State for GTP Hydrolysis Cell 89, 251-261
11. Slep, K. C., Kercher, M. A., He, W., Cowan, C. W., Wensel, T. G., and Sigler, P. B. (2001) Structural determinants for regulation of phosphodiesterase by a G protein at 2.0 Å Nature 409, 1071-1077
12. Preininger, A. M. and Hamm, H. E. (2004) G protein signaling: Insights from new structures Sci. STKE, re3
13. sα·GTPγS Science 278, 1907-1916
14. i1 Subunits in Solution Biochemistry 42, 7931-7941
15. Linder, M. E., Pang, I. H., Duronio, R. J., Gordon, J. I., Sternweis, P. C., and Gilman, A. G. (1991) Lipid modifications of G protein subunits. Myristoylation of Goα increases its affinity for βγ J. Biol. Chem. 266, 4654-4659
16. Mumby, S. M. and Linder, M. E. (1994) Myristoylation of G-protein α subunits Methods Enzymol. 237, 254-268
17. Chen, C. A. and Manning, D. R. (2001) Regulation of G proteins by covalent modification Oncogene 20, 1643-1652
18. Herrmann, R., Heck, M., Henklein, P., Hofmann, K. P., and Ernst, O. P. (2006) Signal transfer from GPCRs to G proteins: Role of the Gα N-terminal region in rhodopsin-transducin coupling J. Biol. Chem. 281, 30234-30241
19. Kisselev, O. G. and Downs, M. A. (2003) Rhodopsin Controls a Conformational Switch on the Transducin γ Subunit Structure 11, 367-373
20. Mumby, S. M., Heukeroth, R. O., Gordon, J. I., and Gilman, A. G. (1990) G-protein α-subunit expression, myristoylation, and membrane association in COS cells Proc. Natl. Acad. Sci. U.S.A. 87, 728-732
21. Jia, L., Linder, M. E., and Blumer, K. J. (2011) Gi/o signaling and the palmitoyltransferase DHHC2 regulate palmitate cycling and shuttling of RGS7 family-binding protein J. Biol. Chem. 286, 13695-13703
22. Resh, M. D. (1996) Regulation of cellular signalling by fatty acid acylation and prenylation of signal transduction proteins Cell. Signalling 8, 403-412
23. Hamm, H. E., Meier, S. M., Liao, G., and Preininger, A. M. (2009) Trp fluorescence reveals an activation-dependent cation-π interaction in the Switch II region of Gαi proteins Protein Sci. 18, 2326-2335
24. il proteins Biochemistry 47, 10281-10293
25. Hoofnagle, A. N., Resing, K. A., and Ahn, N. G. (2003) Protein Analysis by Hydrogen Exchange Mass Spectrometry Annu. Rev. Biophys. Biomol. Struct. 32, 1-25
26. Hoofnagle, A. N., Resing, K. A., and Ahn, N. G. (2004) Practical methods for deuterium exchange/mass spectrometry Methods Mol. Biol. 250, 283-298
27. Busenlehner, L. S. and Armstrong, R. N. (2005) Insights into enzyme structure and dynamics elucidated by amide H/D exchange mass spectrometry Arch. Biochem. Biophys. 433, 34-46
28. Asuru, A. P. and Busenlehner, L. S. (2011) Analysis of human ferrochelatase iron binding via amide hydrogen/deuterium exchange mass spectrometry Int. J. Mass Spectrosc. 302, 76-84
29. Busenlehner, L. S., Salomonsson, L., Brzezinski, P., and Armstrong, R. N. (2006) Mapping protein dynamics in catalytic intermediates of the redox-driven proton pump cytochrome c oxidase Proc. Natl. Acad. Sci. U.S.A. 103, 15398-15403
30. Oldham, W. M., Van Eps, N., Preininger, A. M., Hubbell, W. L., and Hamm, H. E. (2006) Mechanism of the receptor-catalyzed activation of heterotrimeric G proteins Nat. Struct. Mol. Biol. 13, 772-777
31. i1 Following Dissociation from Gβγ Subunit and Activation Biochemistry 41, 9962-9972
32. Preininger, A., Funk, M., Meier, S., Oldham, W., Johnston, C., Adhikary, S., Kimple, A., Siderovski, D., Hamm, H., and Iverson, T. (2009) Helix dipole movement and conformational variability contribute to allosteric GDP release in Gi subunits Biochemistry 48, 2630-2642
33. Mazzoni, M. R. and Hamm, H. E. (1993) Tryptophan207 is involved in the GTP-dependent conformational switch in the α subunit of the G protein transducin: Chymotryptic digestion patterns of the GTPγS and GDP-bound forms J. Protein Chem. 12, 215-221
34. McEwen, D. P., Gee, K. R., Kang, H. C., and Neubig, R. R. (2002) Fluorescence approaches to study G protein mechanisms Methods Enzymol. 344, 403-420
35. Rusconi, F. and Belghazi, M. (2002) Desktop prediction/analysis of mass spectrometric data in proteomic projects by using massXpert Bioinformatics 18, 644-645
36. Clauser, K. R., Baker, P., and Burlingame, A. L. (1999) Role of accurate mass measurement (±10 ppm) in protein identification strategies employing MS or MS/MS and database searching Anal. Chem. 71, 2871-2882
37. Zhang, Z. and Marshall, A. G. (1998) A universal algorithm for fast and automated charge state deconvolution of electrospray mass-to-charge ratio spectra J. Am. Soc. Mass Spectrom. 9, 225-233
38. Van Eps, N., Oldham, W. M., Hamm, H. E., and Hubbell, W. L. (2006) Structural and dynamical changes in an α-subunit of a heterotrimeric G protein along the activation pathway Proc. Natl. Acad. Sci. U.S.A. 103, 16194-16199
39. Hu, J., Wang, Y., Zhang, X., Lloyd, J. R., Li, J. H., Karpiak, J., Costanzi, S., and Wess, J. (2010) Structural basis of G protein-coupled receptor-G protein interactions Nat. Chem. Biol. 6, 541-548
40. Oldham, W. M. and Hamm, H. E. (2008) Heterotrimeric G protein activation by G-protein-coupled receptors Nat. Rev. Mol. Cell Biol. 9, 60-71
41. Kapoor, N., Menon, S. T., Chauhan, R., Sachdev, P., and Sakmar, T. P. (2009) Structural evidence for a sequential release mechanism for activation of heterotrimeric G proteins J. Mol. Biol. 393, 882-897
42. Faurobert, E., Otto-Bruc, A., Chardin, P., and Chabre, M. (1993) Tryptophan W207 in transducin Tα is the fluorescence sensor of the G protein activation switch and is involved in the effector binding EMBO J. 12, 4191-4198
43. Mansoor, S. E., McHaourab, H. S., and Farrens, D. L. (2002) Mapping proximity within proteins using fluorescence spectroscopy. A study of T4 lysozyme showing that tryptophan residues quench bimane fluorescence Biochemistry 41, 2475-2484
44. Goldberg, J. (1998) Structural Basis for Activation of ARF GTPase: Mechanisms of Guanine Nucleotide Exchange and GTP-Myristoyl Switching Cell 95, 237-248
45. Gangal, M., Clifford, T., Deich, J., Cheng, X., Taylor, S. S., and Johnson, D. A. (1999) Mobilization of the A-kinase N-myristate through an isoform-specific intermolecular switch Proc. Natl. Acad. Sci. U.S.A. 96, 12394-12399
46. Tang, C., Loeliger, E., Luncsford, P., Kinde, I., Beckett, D., and Summers, M. F. (2004) Entropic switch regulates myristate exposure in the HIV-1 matrix protein Proc. Natl. Acad. Sci. U.S.A. 101, 517-522
47. Seykora, J. T., Myat, M. M., Allen, L. A., Ravetch, J. V., and Aderem, A. (1996) Molecular determinants of the myristoyl-electrostatic switch of MARCKS J. Biol. Chem. 271, 18797-18802
48. Patwardhan, P. and Resh, M. D. (2010) Myristoylation and membrane binding regulate c-Src stability and kinase activity Mol. Cell. Biol. 30, 4094-4107
49. Ames, J. B., Tanaka, T., Stryer, L., and Ikura, M. (1994) Secondary structure of myristoylated recoverin determined by three-dimensional heteronuclear NMR: Implications for the calcium-myristoyl switch Biochemistry 33, 10743-10753
50. Hanakam, F., Gerisch, G., Lotz, S., Alt, T., and Seelig, A. (1996) Binding of hisactophilin I and II to lipid membranes is controlled by a pH-dependent myristoyl-histidine switch Biochemistry 35, 11036-11044
51. Liu, Y., Kahn, R. A., and Prestegard, J. H. (2010) Dynamic structure of membrane-anchored Arf*GTP Nat. Struct. Mol. Biol. 17, 876-881
52. Yan, S. Z., Huang, Z. H., Rao, V. D., Hurley, J. H., and Tang, W. J. (1997) Three discrete regions of mammalian adenylyl cyclase form a site for Gsα activation J. Biol. Chem. 272, 18849-18854
53. Tesmer, J. J., Sunahara, R. K., Johnson, R. A., Gosselin, G., Gilman, A. G., and Sprang, S. R. (1999) Two-Metal-Ion Catalysis in Adenylyl Cyclase Science 285, 756-760
54. Chen, Z., Singer, W. D., Sternweis, P. C., and Sprang, S. R. (2005) Structure of the p115RhoGEF rgRGS domain-Gα13/i1 chimera complex suggests convergent evolution of a GTPase activator Nat. Struct. Mol. Biol. 12, 191-197
55. q-GRK2-Gβγ Complex Science 310, 1686-1690
56. i1 Chimeras J. Biol. Chem. 271, 413-424
57. Venkatakrishnan, G. and Exton, J. H. (1996) Identification of determinants in the α-subunit of Gq required for phospholipase C activation J. Biol. Chem. 271, 5066-5072
58. Artemyev, N. O., Mills, J. S., Thornburg, K. R., Knapp, D. R., Schey, K. L., and Hamm, H. E. (1993) A site on transducin α-subunit of interaction with the polycationic region of cGMP phosphodiesterase inhibitory subunit J. Biol. Chem. 268, 23611-23615
59. Artemyev, N. O., Natochin, M., Busman, M., Schey, K. L., and Hamm, H. E. (1996) Mechanism of photoreceptor cGMP phosphodiesterase inhibition by its γ-subunits Proc. Natl. Acad. Sci. U.S.A. 93, 5407-5412
60. Grant, J. E., Guo, L. W., Vestling, M. M., Martemyanov, K. A., Arshavsky, V. Y., and Ruoho, A. E. (2006) The N terminus of GTPγS-activated transducin α-subunit interacts with the C terminus of the cGMP phosphodiesterase γ-subunit J. Biol. Chem. 281, 6194-6202
61. iα Science 261, 218-221
62. i2 polypeptide, a G protein α subunit, is required for its signaling and transformation functions Proc. Natl. Acad. Sci. U.S.A. 89, 9695-9699
63. oα Increases its Affinity for βγ J. Biol. Chem. 266, 4654-4659
64. Kerov, V., Rubin, W. W., Natochin, M., Melling, N. A., Burns, M. E., and Artemyev, N. O. (2007) N-terminal fatty acylation of transducin profoundly influences its localization and the kinetics of photoresponse in rods J. Neurosci. 27, 10270-10277
65. iα1 Biochemistry 36, 15660-15669
66. Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., and Ferrin, T. E. (2004) UCSF Chimera: A visualization system for exploratory research and analysis J. Comput. Chem. 25, 1605-1612
67. Van Eps, N., Preininger, A. M., Alexander, N., Kaya, A. I., Meier, S., Meiler, J., Hamm, H. E., and Hubbell, W. L. (2011) Interaction of a G protein with an activated receptor opens the interdomain interface in the α subunit Proc. Natl. Acad. Sci. U.S.A. 108, 9420-9424