A point mutation uncouples transducin-α from the photoreceptor RGS and effector proteins

Journal of Neurochemistry

Volumn 87, Issue 5, 2003, Pages 1262-1271

  Natochin, Michael ^a   Artemyev, Nikolai O ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

EGL 30; G proteins; PDE6; RGS9; Signal transduction; Transducin

Indexed keywords

GUANOSINE TRIPHOSPHATASE; GUANOSINE TRIPHOSPHATE; PROTEIN SUBUNIT; RGS PROTEIN; RHODOPSIN; TRANSDUCIN; TRANSDUCIN ALPHA; UNCLASSIFIED DRUG;

ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; CRYSTAL STRUCTURE; DATA ANALYSIS; ENZYME ACTIVITY; HYPOTHESIS; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN HYDROLYSIS; PROTEIN STRUCTURE; STATISTICAL SIGNIFICANCE; STRUCTURE ANALYSIS;

AMINO ACID SEQUENCE; CANDIDA; CONSERVED SEQUENCE; ENZYME ACTIVATION; FUNGAL PROTEINS; GTP-BINDING PROTEIN ALPHA SUBUNITS, GQ-G11; GUANOSINE TRIPHOSPHATE; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; POINT MUTATION; PROTEIN BINDING; PROTEIN FOLDING; RGS PROTEINS; RHODOPSIN; STRUCTURE-ACTIVITY RELATIONSHIP; TRANSDUCIN;

CAENORHABDITIS; CAENORHABDITIS ELEGANS; CANDIDA; CANDIDA ALBICANS; FELIS CATUS;

EID: 0344874686     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.2003.02103.x     Document Type: Article

References (57)

1. Arshavsky V. Y., Lamb T. D. and Pugh E. N. Jr (2002) G proteins and phototransduction. Annu. Rev. Physiol. 264, 153-187.
2. Artemyev N. O. (1997) Binding of transducin to light-activated rho-dopsin prevents transducin interaction with the rod cGMP phosphodiesterase γ-subunit. Biochemistry 36, 4188-4193.
3. Artemyev N. O. and Hamm H. E. (1992) Two-site high-affinity interaction between inhibitory and catalytic subunuts of rod cyclic GMP phosphodiesterase. Biochem. J. 283, 273-279.
4. Artemyev N. O., Arshavsky V. Y. and Cote R. H. (1998) Photoreceptor phosphodiesterase: interaction of inhibitory γ subunits and cyclic GMP with specific binding sites on the catalytic subunits. Methods 14, 93-104.
5. Berman D. M. and Gilman A. G. (1998) Mammalian RGS proteins: barbarians at the gate. J. Biol. Chem. 273, 1269-1272.
6. Berman D. M., Kozasa T. and Gilman A. G. (1996b) The GTPase-activating protein RGS4 stabilizes the transition state for nucleotide hydrolysis. J. Biol. Chem. 271, 27209-27212.
7. Berman D. M., Wilkie T. M. and Gilman A. G. (1996a) GAIP and RGS4 are GTPase-activating proteins for the Gi subfamily of G protein α subunits. Cell 86, 445-452.
8. Bourne H. R. (1997) How receptors talk to trimeric G proteins. Curr. Opin. Cell Biol. 9, 134-142.
9. 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.
10. Chase D. L., Patikoglou G. A. and Koelle M. R. (2001) Two RGS proteins that inhibit Gαo and Gαq signaling in C. elegans neurons require a Gβ5-like subunit for function. Curr. Biol. 11, 222-231.
11. Coleman D. E., Berghuis A. M., Lee E., Linder M. E., Gilman A. G. and Sprang S. R. (1994) Structures of active conformations of Giα1 and the mechanism of GTP hydrolysis. Science 265, 1405-1412.
12. Cowan C. W., He W. and Wensel T. G. (2001) RGS proteins: lessons from the RGS9 subfamily. Prog. Nucleic Acid Res. Mol. Biol. 65, 341-359.
13. DiBello P. R., Garrison T. R., Apanovitch D. M., Hoffman G., Shuey D. J., Mason K., Cockett M. I. and Dohlman H. G. (1998) Selective uncoupling of RGS action by a single point mutation in the G protein α-subunit. J. Biol. Chem. 273, 5780-5784.
14. Doi M. and Iwasaki K. (2002) Regulation of retrograde signaling at neuromuscular junctions by the novel C2 domain protein AEX-1. Neuron 33, 249-259.
15. Dryja T. P., Hahn L. B., Reboul T. and Arnaud B. (1996) Missense mutation in the gene encoding the α subunit of rod transducin in the Nougaret form of congenital stationary night blindness. Nat. Genet. 13, 358-360.
16. Farfel Z., Bourne H. R. and Iiri T. (1999) The expanding spectrum of G protein diseases. N. Engl. J. Med. 340, 1012-1020.
17. Freissmuth M. and Gilman A. G. (1989) Mutations of Gsα designed to alter the reactivity of the protein with bacterial toxins. Substitutions at ARG187 result in loss of GTPase activity. J. Biol. Chem. 264, 21907-21914.
18. Gilman A. G. (1987) G proteins: transducers of receptor-generated signals. Annu. Rev. Biochem. 56, 615-649.
19. Graziano M. P. and Gilman A. G. (1989) Synthesis in Escherichia coli of GTPase-deficient mutants of Gsα. J. Biol. Chem. 264, 15475-15482.
20. Guex N. and Peitsch M. C. (1997) SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18, 2714-2723.
21. Hamm, H. E. (1998) The many faces of G protein signaling. J. Biol. Chem. 273, 669-672.
22. He W., Cowan C. W. and Wensel T. G. (1998) RGS9, a GTPase accelerator for phototransduction. Neuron 20, 95-102.
23. Hollinger S. and Hepler J. R. (2002) Cellular regulation of RGS proteins: modulators and integrators of G protein signaling. Pharmacol. Rev. 54, 527-559.
24. Iiri T., Herzmark P., Nakamoto J. M., van Dop C. and Bourne H. R. (1994) Rapid GDP release from Gsα in patients with gain and loss of endocrine function. Nature 371, 164-168.
25. Iiri T., Bell S. M., Baranski T. J., Fujita T. and Boume H. R. (1999) A Gsα mutant designed to inhibit receptor signaling through Gs. Proc. Natl Acad. Sci. USA 96, 499-504.
26. Kleuss C., Pallast M., Brendel S., Rosenthal W. and Schultz G. (1987) Resolution of transducin subunits by chromatography on blue sepharose. J. Chromatogr. 407, 281-289.
27. Laemmli U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
28. 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.
29. αi1 blocks interaction with regulator of G protein signaling proteins. J. Biol. Chem. 273, 12794-12797.
30. Landis C. A., Masters S. B., Spada A., Pace A. M., Bourne H. R. & Vallar L. (1989) GTPase inhibiting mutations activate the alpha chain of Gs and stimulate adenylyl cyclase in human pituitary tumours. Nature 340, 692-696.
31. Li Q. and Cerione R. A. (1997) Communication between switch II and switch III of the transducin α subunit is essential for target activation. J. Biol. Chem. 272, 21673-21676.
32. Lowy D. R. and Willumsen B. M. (1993) Function and regulation of ras. Annu. Rev. Biochem. 62, 851-891.
33. McEntaffer R., Natochin M. and Artemyev N. O. (1999) Modulation of transducin GTPase activity by chimeric RGS16 and RGS9 regulators of G protein signaling and the effector molecule. Biochemistry 38, 4931-4937.
34. Masters S. B., Landis C. A. & Boume H. R. (1990) GTPase-inhibiting mutations in the α subunit of Gs. Adv. Second Messenger Phosphoprotein Res. 24, 70-75.
35. Mittal R., Erickson J. W. and Cerione R. A. (1996) Uncoupling of GTP binding from target stimulation by a single mutation in the transducin α subunit. Science 271, 1413-1416.
36. Muradov K. G. and Artemyev N. O. (2000) Loss of the effector function in a transducin-α mutant associated with Nougaret night blindness. J. Biol. Chem. 275, 6969-6974.
37. Natochin M., Granovsky A. E. and Artemyev N. O. (1997) Regulation of transducin GTPase activity by human retinal RGS. J. Biol. Chem. 272, 17444-17449.
38. Natochin M., Granovsky A. E. and Artemyev N. O. (1998) Identification of effector residues on photoreceptor G protein, transducin. J. Biol. Chem. 273, 21808-21815.
39. Natochin M., Granovsky A. E., Muradov K. G. and Artemyev N. O. (1999) Roles of the transducin α4-helix/α4-β6 loop in the receptor and effector interactions. J. Biol. Chem. 274, 7865-7869.
40. Neer E. J., Denker B. M., Thomas T. C. and Schmidt C. J. (1994) Analysis of G-protein α and βγ subunits by in vitro translation. Methods Enzymol. 237, 226-239.
41. Nekrasova E. R., Berman D. M., Rustandi R. R., Hamm H. E., Gilman A. G. and Arshavsky V. Y. (1997) Activation of transducin guanosine triphosphatase by two proteins of the RGS family. Biochemistry 36, 7638-7643.
42. Noel J. P., Hamm H. E. and Sigler P. B. (1993) The 2.2 A crystal structure of transducin-α complexed with GTPγS. Nature 366, 654-663.
43. Papermaster D. S. and Dreyer W. J. (1974) Rhodopsin content in the outer segment membranes of bovine and frog retinal rods. Biochemistry 13, 2438-2444.
44. Pierce K. L., Premont R. T. and Lefkowitz R. J. (2002) Seven-transmembrane receptors. Nat. Rev. Mol. Cell. Biol. 3, 639-650.
45. Raw A. S., Coleman D. E., Gilman A. G. and Sprang S. R. (1997) Structural and biochemical characterization of the GTPγS-, GDP∼Pi-, and GDP-bound forms of a GTPase-deficient Gly42 → Val mutant of Giα1. Biochemistry 36, 15660-15669.
46. Ross E. M. and Wilkie T. M. (2000) GTPase-activating proteins for heterotrimeric G proteins: regulators of G protein signaling (RGS) and RGS-like proteins. Annu. Rev. Biochem. 69, 795-827.
47. Skiba N. P., Bae H. and Hamm H. E. (1996) Mapping of effector binding sites of transducin α-subunit using Gαt/Gαi1 chimeras. J. Biol. Chem. 271, 413-424.
48. Skiba N. P., Hopp J. A. and Arshavsky V. Y. (2000) The effector enzyme regulates the duration of G protein signaling in vertebrate photoreceptors by increasing the affinity between transducin and RGS protein. J. Biol. Chem. 275, 32716-32720.
49. Skiba N. P., Yang C. S., Huang T., Bae H. and Hamm H. E. (1999) The α-helical domain of Gαt determines specific interaction with regulator of G protein signaling 9. J. Biol. Chem. 274, 8770-8778.
50. 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 2.0A. Nature 409, 1071-1077.
51. -. Nature 372, 276-279.
52. Sprang S. R. (1997) G protein mechanisms: insights from structural analysis. Annu. Rev. Biochem. 66, 639-678.
53. - activated Giα: stabilization of the transition state for GTP hydrolysis. Cell 89, 251-261.
54. Van Dop C., Tsubokawa M., Bourne H. R. and Ramachandran J. (1984) Amino acid sequence of retinal transducin at the site ADP-ribosylated by cholera toxin. J. Biol. Chem. 259, 696-698.
55. Weinstein L. S., Shenker A., Gejman P. V., Merino M. J., Friedman E. and Spiegel A. M. (1991) Activating mutations of the stimulatory G protein in the McCune-Albright syndrome. N. Engl. J. Med. 325, 1688-1695.
56. Wieland T., Chen C. K. and Simon M. I. (1997) The retinal specific protein RGS-r competes with the γ subunit of cGMP phosphodiesterase for the α subunit of transducin and facilitates signal termination. J. Biol. Chem. 272, 8853-8856.
57. Yamanaka G., Eckstein F. and Stryer L. (1985) Stereochemistry of the guanyl nucleotide binding site of transducin probed by phosphorothioate analogues of GTP and GDP. Biochemistry 24, 8094-8101.