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PMID: 23466875 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

Linking receptor activation to changes in Sw I and II of Gα proteins.

Journal of structural biology ·Vol. 184 ·No. 1 ·2013-10-00 ·Pages 63-74

Hamm HE, Kaya AI, Gilbert JA, Preininger AM

Abstract

G-protein coupled receptors catalyze nucleotide exchange on G proteins, which results in subunit dissociation and effector activation. In the recent β2AR-Gs structure, portions of Switch I and II of Gα are not fully elucidated. We paired fluorescence studies of receptor-Gαi interactions with the β2AR-Gs and other Gi structures to investigate changes in Switch I and II during receptor activation and GTP binding. The β2/β3 loop containing Leu194 of Gαi is located between Switches I and II, in close proximity to IC2 of the receptor and the C-terminus of Gα, thus providing an allosteric connection between these Switches and receptor activation. We compared the environment of residues in myristoylated Gαi proteins in the heterotrimer to that upon receptor activation and subsequent GTP binding. Upon receptor activation, residues in both Switch regions are less solvent-exposed, as compared to the heterotrimer. Upon GTPγS binding, the environment of several residues in Switch I resemble the receptor-bound state, while Switch II residues display effects on their environment which are consistent with their role in GTP binding and Gβγ dissociation. The ability to merge available crystal structures with solution studies is a powerful tool to gain insight into conformational changes associated with receptor-mediated Gi protein activation.

Keywords
G(i) Gα(i) N-terminal myristoylation Site-directed fluorescence Switch I/II α5 helix
MeSH Terms
Amino Acid Sequence Animals GTP-Binding Proteins/metabolism Guanosine Triphosphate/metabolism Molecular Sequence Data Protein Binding Rats Receptors, G-Protein-Coupled/metabolism
Chemicals
Receptors, G-Protein-Coupled Guanosine Triphosphate GTP-Binding Proteins
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Hamm Heidi E
Vanderbilt University Medical Center, Department of Pharmacology, Nashville, TN 37232-6600, United States.
Kaya Ali I
Gilbert James A
Preininger Anita M
References (67)
67 references, click to expand
  1. Helix dipole movement and conformational variability contribute to allosteric GDP release in Galphai subunits.
    Biochemistry. 2009 Mar 31;48(12):2630-42 PMID: 19222191
  2. Site of G protein binding to rhodopsin mapped with synthetic peptides from the alpha subunit.
    Science. 1988 Aug 12;241(4867):832-5 PMID: 3136547
  3. Interaction of a G protein with an activated receptor opens the interdomain interface in the alpha subunit.
    Proc Natl Acad Sci U S A. 2011 Jun 7;108(23):9420-4 PMID: 21606326
  4. Mapping of contact sites in complex formation between light-activated rhodopsin and transducin by covalent crosslinking: use of a chemically preactivated reagent.
    Proc Natl Acad Sci U S A. 2001 Apr 24;98(9):4883-7 PMID: 11320238
  5. Light-induced conformational changes of rhodopsin probed by fluorescent alexa594 immobilized on the cytoplasmic surface.
    Biochemistry. 2000 Dec 12;39(49):15225-33 PMID: 11106502
  6. Roles of G(o)alpha tryptophans in GTP hydrolysis, GDP release, and fluorescence signals.
    Biochemistry. 1998 Jan 20;37(3):837-43 PMID: 9454573
  7. Mapping of contact sites in complex formation between transducin and light-activated rhodopsin by covalent crosslinking: use of a photoactivatable reagent.
    Proc Natl Acad Sci U S A. 2001 Apr 24;98(9):4877-82 PMID: 11320237
  8. Mechanism of the receptor-catalyzed activation of heterotrimeric G proteins.
    Nat Struct Mol Biol. 2006 Sep;13(9):772-7 PMID: 16892066
  9. The structure of the G protein heterotrimer Gi alpha 1 beta 1 gamma 2.
    Cell. 1995 Dec 15;83(6):1047-58 PMID: 8521505
  10. Characterization of heterotrimeric nucleotide-depleted Gα(i)-proteins by Bodipy-FL-GTPγS fluorescence anisotropy.
    Arch Biochem Biophys. 2012 Aug 15;524(2):93-8 PMID: 22659491
  11. UCSF Chimera--a visualization system for exploratory research and analysis.
    J Comput Chem. 2004 Oct;25(13):1605-12 PMID: 15264254
  12. Myristoylation of G-protein alpha subunits.
    Methods Enzymol. 1994;237:254-68 PMID: 7935001
  13. Probing the mechanism of rhodopsin-catalyzed transducin activation.
    J Neurochem. 2001 Apr;77(1):202-10 PMID: 11279276
  14. Two amino acids within the alpha4 helix of Galphai1 mediate coupling with 5-hydroxytryptamine1B receptors.
    J Biol Chem. 1999 May 21;274(21):14963-71 PMID: 10329698
  15. Disease-causing mutation in GPR54 reveals the importance of the second intracellular loop for class A G-protein-coupled receptor function.
    J Biol Chem. 2008 Nov 7;283(45):31068-78 PMID: 18772143
  16. Disruption of the alpha5 helix of transducin impairs rhodopsin-catalyzed nucleotide exchange.
    Biochemistry. 2002 Jun 4;41(22):6988-94 PMID: 12033931
  17. Functional importance of the amino terminus of Gq alpha.
    J Biol Chem. 1996 Jan 5;271(1):496-504 PMID: 8550609
  18. Structural basis of G protein-coupled receptor-G protein interactions.
    Nat Chem Biol. 2010 Jul;6(7):541-8 PMID: 20512139
  19. Quality of protein crystal structures.
    Acta Crystallogr D Biol Crystallogr. 2007 Sep;63(Pt 9):941-50 PMID: 17704562
  20. Effects of Mg2+ and the beta gamma-subunit complex on the interactions of guanine nucleotides with G proteins.
    J Biol Chem. 1987 Jan 15;262(2):762-6 PMID: 3100519
  21. The 2.2 A crystal structure of transducin-alpha complexed with GTP gamma S.
    Nature. 1993 Dec 16;366(6456):654-63 PMID: 8259210
  22. Receptor-mediated changes at the myristoylated amino terminus of Galpha(il) proteins.
    Biochemistry. 2008 Sep 30;47(39):10281-93 PMID: 18771287
  23. The Uppsala Electron-Density Server.
    Acta Crystallogr D Biol Crystallogr. 2004 Dec;60(Pt 12 Pt 1):2240-9 PMID: 15572777
  24. Conformational changes in the G protein Gs induced by the β2 adrenergic receptor.
    Nature. 2011 Sep 28;477(7366):611-5 PMID: 21956331
  25. Structural and dynamical changes in an alpha-subunit of a heterotrimeric G protein along the activation pathway.
    Proc Natl Acad Sci U S A. 2006 Oct 31;103(44):16194-9 PMID: 17053066
  26. Crystal structure of the β2 adrenergic receptor-Gs protein complex.
    Nature. 2011 Jul 19;477(7366):549-55 PMID: 21772288
  27. The receptor-bound "empty pocket" state of the heterotrimeric G-protein alpha-subunit is conformationally dynamic.
    Biochemistry. 2006 Oct 31;45(43):12986-97 PMID: 17059215
  28. Conformational changes associated with receptor-stimulated guanine nucleotide exchange in a heterotrimeric G-protein alpha-subunit: NMR analysis of GTPgammaS-bound states.
    J Biol Chem. 2006 Mar 17;281(11):7635-48 PMID: 16407225
  29. Activation of G-protein Galpha subunits by receptors through Galpha-Gbeta and Galpha-Ggamma interactions.
    Trends Biochem Sci. 2003 Jan;28(1):13-7 PMID: 12517447
  30. Biological and structural characterization of a Ras transforming mutation at the phenylalanine-156 residue, which is conserved in all members of the Ras superfamily.
    Proc Natl Acad Sci U S A. 1995 Feb 28;92(5):1272-6 PMID: 7877967
  31. The nucleotide exchange factor Ric-8A is a chaperone for the conformationally dynamic nucleotide-free state of Gαi1.
    PLoS One. 2011;6(8):e23197 PMID: 21853086
  32. Substitution of three amino acids switches receptor specificity of Gq alpha to that of Gi alpha.
    Nature. 1993 May 20;363(6426):274-6 PMID: 8387644
  33. Hydrophobic amino acid in the i2 loop plays a key role in receptor-G protein coupling.
    J Biol Chem. 1993 Oct 25;268(30):22273-6 PMID: 8226735
  34. Myristoylation exerts direct and allosteric effects on Gα conformation and dynamics in solution.
    Biochemistry. 2012 Mar 6;51(9):1911-24 PMID: 22329346
  35. Structures of active conformations of Gi alpha 1 and the mechanism of GTP hydrolysis.
    Science. 1994 Sep 2;265(5177):1405-12 PMID: 8073283
  36. Rapid GTP binding and hydrolysis by G(q) promoted by receptor and GTPase-activating proteins.
    Proc Natl Acad Sci U S A. 1999 Aug 17;96(17):9539-44 PMID: 10449728
  37. The surface of visual arrestin that binds to rhodopsin.
    Mol Vis. 2004 Jun 15;10:392-8 PMID: 15215746
  38. A novel Gs alpha mutant in a patient with Albright hereditary osteodystrophy uncouples cell surface receptors from adenylyl cyclase.
    J Biol Chem. 1994 Oct 14;269(41):25387-91 PMID: 7523385
  39. Structural determinants in the second intracellular loop of the human cannabinoid CB1 receptor mediate selective coupling to G(s) and G(i).
    Br J Pharmacol. 2010 Dec;161(8):1817-34 PMID: 20735408
  40. Allosteric modulation of metabotropic glutamate receptors: structural insights and therapeutic potential.
    Neuropharmacology. 2011 Jan;60(1):66-81 PMID: 20637216
  41. Structural analysis of rod GTP-binding protein, Gt. Limited proteolytic digestion pattern of Gt with four proteases defines monoclonal antibody epitope.
    J Biol Chem. 1991 Jul 25;266(21):14072-81 PMID: 1713215
  42. A novel site on the Galpha -protein that recognizes heptahelical receptors.
    J Biol Chem. 2001 Feb 2;276(5):3262-9 PMID: 11027680
  43. Structure of the GDP-Pi complex of Gly203-->Ala gialpha1: a mimic of the ternary product complex of galpha-catalyzed GTP hydrolysis.
    Structure. 1996 Nov 15;4(11):1277-90 PMID: 8939752
  44. Crystal structures of the G protein Gi alpha 1 complexed with GDP and Mg2+: a crystallographic titration experiment.
    Biochemistry. 1998 Oct 13;37(41):14376-85 PMID: 9772163
  45. The 2.0 A crystal structure of a heterotrimeric G protein.
    Nature. 1996 Jan 25;379(6563):311-9 PMID: 8552184
  46. Reorganizing the protein space at the Universal Protein Resource (UniProt).
    Nucleic Acids Res. 2012 Jan;40(Database issue):D71-5 PMID: 22102590
  47. Integrating computation and visualization for biomolecular analysis: an example using python and AVS.
    Pac Symp Biocomput. 1999;:401-12 PMID: 10380214
  48. G protein mechanisms: insights from structural analysis.
    Annu Rev Biochem. 1997;66:639-78 PMID: 9242920
  49. Structural determinants for activation of the alpha-subunit of a heterotrimeric G protein.
    Nature. 1994 Jun 23;369(6482):621-8 PMID: 8208289
  50. Crystal structure of the adenylyl cyclase activator Gsalpha.
    Science. 1997 Dec 12;278(5345):1943-7 PMID: 9395396
  51. Evidence for structural changes in carboxyl-terminal peptides of transducin alpha-subunit upon binding a soluble mimic of light-activated rhodopsin.
    Biochemistry. 2003 Jan 21;42(2):302-11 PMID: 12525157
  52. Conformational changes in the amino-terminal helix of the G protein alpha(i1) following dissociation from Gbetagamma subunit and activation.
    Biochemistry. 2002 Aug 6;41(31):9962-72 PMID: 12146960
  53. Identification of a stretch of six divergent amino acids on the alpha5 helix of Galpha16 as a major determinant of the promiscuity and efficiency of receptor coupling.
    Biochem J. 2004 Jun 1;380(Pt 2):361-9 PMID: 15005654
  54. Mapping allosteric connections from the receptor to the nucleotide-binding pocket of heterotrimeric G proteins.
    Proc Natl Acad Sci U S A. 2007 May 8;104(19):7927-32 PMID: 17463080
  55. G Protein activation without subunit dissociation depends on a G{alpha}(i)-specific region.
    J Biol Chem. 2005 Jul 1;280(26):24584-90 PMID: 15866880
  56. Identification of a receptor/G-protein contact site critical for signaling specificity and G-protein activation.
    Proc Natl Acad Sci U S A. 1995 Dec 5;92(25):11642-6 PMID: 8524820
  57. Trp fluorescence reveals an activation-dependent cation-pi interaction in the Switch II region of Galphai proteins.
    Protein Sci. 2009 Nov;18(11):2326-35 PMID: 19760664
  58. Environment and mobility of a series of fluorescent reporters at the amino terminus of structurally related peptide agonists and antagonists bound to the cholecystokinin receptor.
    J Biol Chem. 2002 May 24;277(21):18552-60 PMID: 11893747
  59. G alpha COOH-terminal minigene vectors dissect heterotrimeric G protein signaling.
    Sci STKE. 2002 Feb 05;2002(118):pl1 PMID: 11836477
  60. The myristoylated amino terminus of Galpha(i)(1) plays a critical role in the structure and function of Galpha(i)(1) subunits in solution.
    Biochemistry. 2003 Jul 8;42(26):7931-41 PMID: 12834345
  61. Structural evidence for a sequential release mechanism for activation of heterotrimeric G proteins.
    J Mol Biol. 2009 Nov 6;393(4):882-97 PMID: 19703466
  62. Receptor and betagamma binding sites in the alpha subunit of the retinal G protein transducin.
    Science. 1997 Jan 17;275(5298):381-4 PMID: 8994033
  63. NMR structure of a receptor-bound G-protein peptide.
    Nature. 1993 May 20;363(6426):276-81 PMID: 8487866
  64. Lipid modifications of G protein subunits. Myristoylation of Go alpha increases its affinity for beta gamma.
    J Biol Chem. 1991 Mar 5;266(7):4654-9 PMID: 1900297
  65. Rhodopsin recognition by mutant G(s)alpha containing C-terminal residues of transducin.
    J Biol Chem. 2000 Jan 28;275(4):2669-75 PMID: 10644728
  66. Crystal structure of opsin in its G-protein-interacting conformation.
    Nature. 2008 Sep 25;455(7212):497-502 PMID: 18818650
  67. Tryptophan207 is involved in the GTP-dependent conformational switch in the alpha subunit of the G protein transducin: chymotryptic digestion patterns of the GTP gamma S and GDP-bound forms.
    J Protein Chem. 1993 Apr;12(2):215-21 PMID: 8489707
Article Info
Journal
Journal of structural biology
Abbr.
J Struct Biol
ISSN
1095-8657
Published
2013-10-00
Epub
2013-00-04
Pages
63-74
Language
English
Region
United States
NLM ID
9011206
PMCID
PMC3726552
Subset
IM
Grants
NEI NIH HHS · R01 EY006062 · United States
NIGMS NIH HHS · R01 GM095633 · United States
NIGMS NIH HHS · GM095633 · United States
NEI NIH HHS · EY006062 · United States
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