Comparative analysis of cone and rod transducins using chimeric Gα subunits

Biochemistry

Volumn 51, Issue 8, 2012, Pages 1617-1624

  Gopalakrishna, Kota N ^a   Boyd, Kimberly K ^a   Artemyev, Nikolai O ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMICAL PROPERTIES; COMPARATIVE ANALYSIS; GTP HYDROLYSIS; GTPASE ACTIVITY; HELICAL DOMAINS; IN-VITRO; INTER-DOMAIN; MUTATIONAL ANALYSIS; NUCLEOTIDE EXCHANGE; ROD PHOTORECEPTORS; TRANSDUCIN;

HYDROLYSIS; MAMMALS;

NUCLEOTIDES;

ADENOSINE DIPHOSPHATE; CHIMERIC PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN BETA SUBUNIT; GUANOSINE TRIPHOSPHATASE; GUANOSINE TRIPHOSPHATE; INHIBITORY GUANINE NUCLEOTIDE BINDING PROTEIN; NUCLEOTIDE; PERTUSSIS TOXIN; TRANSDUCIN;

ADENOSINE DIPHOSPHATE RIBOSYLATION; ARTICLE; COMPARATIVE STUDY; HYDROLYSIS; MOLECULAR INTERACTION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN METABOLISM; RETINA CONE; RETINA ROD;

ANIMALS; CATTLE; CELLS, CULTURED; GTP PHOSPHOHYDROLASES; PROTEIN STRUCTURE, SECONDARY; RETINAL CONE PHOTORECEPTOR CELLS; RETINAL ROD PHOTORECEPTOR CELLS; TRANSDUCIN;

MAMMALIA;

EID: 84857594626     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi3000935     Document Type: Article

References (45)

1. Burns, M. E. and Arshavsky, V. Y. (2005) Beyond counting photons: trials and trends in vertebrate visual transduction Neuron 48, 387-401
2. Lamb, T. D. and Pugh, E. N., Jr. (2006) Phototransduction, dark adaptation, and rhodopsin regeneration the proctor lecture Invest. Ophthalmol. Vis. Sci. 47, 5137-5152
3. Fu, Y. and Yau, K. W. (2007) Phototransduction in mouse rods and cones Pflugers Archive 454, 805-819
4. Nikonov, S. S., Kholodenko, R., Lem, J., and Pugh, E. N., Jr. (2006) Physiological features of the S- and M-cone photoreceptors of wild-type mice from single-cell recordings J. Gen. Physiol. 127, 359-374
5. Kefalov, V., Fu, Y., Marsh-Armstrong, N., and Yau, K. (2003) Role of visual pigment properties in rod and cone phototransduction Nature 425, 526-531
6. Deng, W. T., Sakurai, K., Liu, J., Dinculescu, A., Li, J., Pang, J., Min, S. H., Chiodo, V. A., Boye, S. L., Chang, B., Kefalov, V. J., and Hauswirth, W. W. (2009) Functional interchangeability of rod and cone transducin α -subunits Proc. Natl. Acad. Sci. U. S. A. 106, 17681-17686
7. Chen, C. K., Woodruff, M. L., Chen, F. S., Shim, H., Cilluffo, M. C., and Fain, G. L. (2010) Replacing the rod with the cone transducin subunit decreases sensitivity and accelerates response decay J. Physiol. 588, 3231-3241
8. Tachibanaki, S., Shimauchi-Matsukawa, Y., Arinobu, D., and Kawamura, S. (2007) Molecular mechanisms characterizing cone photoresponses Photochem. Photobiol. 83, 19-26
9. Muradov, H., Boyd, K. K., and Artemyev, N. O. (2010) Rod phosphodiesterase-6 PDE6A and PDE6B subunits are enzymatically equivalent J. Biol. Chem. 285, 39828-39834
10. Pugh, E. N., Jr. and Lamb, T. D. (1993) Amplification and kinetics of the activation steps in phototransduction Biochim. Biophys. Acta 1141, 111-1149
11. Krispel, C. M., Chen, D., Melling, N., Chen, Y., Martemyanov, K. A., Quillinan, N., Arshavsky, V. Y., Wensel, T. G., Chen, C., and Burns, M. E. (2006) RGS expression rate-limits recovery of rod photoresponses Neuron 51, 409-416
12. 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
13. Skiba, N. P., Bae, H., and Hamm, H. E. (1996) Mapping the effector binding sites of transducin α-subunit using Gαt/Gαi1 chimeras J. Biol. Chem. 271, 413-424
14. 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
15. 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
16. Yamanaka, G., Eckstein, F., and Stryer, L. (1985) Stereochemistry of the guanyl nucleotide binding site of transducin probed by phosphorothionate analogues of GTP and GDP Biochemistry 24, 8094-8101
17. Ford, C. E., Skiba, N. P., Bae, H., Daaka, Y., Reuveny, E., Shekter, L. R., Rosal, R., Weng, G., Yang, C. S., Iyengar, R., Miller, R. J., Jan, L. Y., Lefkowitz, R. J., and Hamm, H. E. (1998) Molecular basis forinteractions of G protein βγ subunits with effectors Science 280, 1271-1274
18. Natochin, M. and Artemyev, N. O. (2003) A point mutation uncouples transducin-α from the photoreceptor RGS and effector proteins J. Neurochem. 87, 1262-1271
19. Arshavsky, V. Y., Gray-Keller, M. P., and Bownds, M. D. (1991) cGMP suppresses GTPase activity of a portion of transducin equimolar to phosphodiesterase in frog rod outer segments J. Biol. Chem. 266, 18530-18537
20. 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
21. Natochin, M., Muradov, K. G., McEntaffer, R. L., and Artemyev, N. O. (2000) Rhodopsin recognition by mutant Gsα containing C-terminal residues of transducin J. Biol. Chem. 275, 2669-2675
22. van Dop, C., Yamanaka, G., Steinberg, F., Sekura, R. D., Manclark, C. R., Stryer, L., and Bourne, H. R. (1984) ADP-ribosylation of transducin by pertussis toxin blocks the light-stimulated hydrolysis of GTP and cGMP in retinal photoreceptors J. Biol. Chem. 259, 23-26
23. Watkins, P. A., Burns, D. L., Kanaho, Y., Liu, T. Y., Hewlett, E. L., and Moss, J. (1985) ADP-ribosylation of transducin by pertussis toxin J. Biol. Chem. 260, 13478-13482
24. West, R. E., Jr., Moss, J., Vaughan, M., Liu, T., and Liu, T. Y. (1985) Pertussis toxin-catalyzed ADP-ribosylation of transducin. Cysteine 347 is the ADP-ribose acceptor site J. Biol. Chem. 260, 14428-14430
25. Zhang, X., Wensel, T. G., and Yuan, C. (2006) Tokay gecko photoreceptors achieve rod-like physiology with cone-like proteins Photochem. Photobiol. 82, 1452-1460
26. Noel, J. P., Hamm, H. E., and Sigler, P. B. (1993) The 2.2A crystal structure of transducin-α complexed with GTPγS Nature 366, 654-663
27. 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
28. Remmers, A. E., Engel, C., Liu, M., and Neubig, R. R. (1999) Interdomain interactions regulate GDP release from heterotrimeric G proteins Biochemistry 38, 13795-13800
29. Marin, E. P., Krishna, A. G., Archambault, V., Simuni, E., Fu, W. Y., and Sakmar, T. P. (2001) The function of interdomain interactions in controlling nucleotide exchange rates in transducin J. Biol. Chem. 276, 23873-23880
30. Nikonov, S., Lamb, T. D., and Pugh, E..N., Jr. (2001) The role of steady phosphodiesterase activity in the kinetics and sensitivity of the light-adapted salamander rod photoresponse J. Gen. Physiol. 116, 795-824
31. Barren, B., Natochin, M., and Artemyev, N. O. (2006) Mutation R238/E in transducin-α yields a GTPase and effector-deficient, but not dominant-negative G-protein α-subunit Mol. Vis. 12, 492-498
32. Gopalakrishna, K. N., Doddapuneni, K., Boyd, K. K., Masuho, I., Martemyanov, K. A., and Artemyev, N. O. (2011) Interaction of transducin with uncoordinated 119 protein (UNC119): implications for the model of transducin trafficking in rod photoreceptors J. Biol. Chem. 286, 28954-28962
33. Grishina, G. and Berlot, C. H. (1998) Mutations at the domain interface of Gsα impair receptor-mediated activation by altering receptor and guanine nucleotide binding J. Biol. Chem. 273, 15053-15060
34. Malinski, J. A. and Wensel, T. G. (1992) Membrane stimulation of cGMP phosphodiesterase activation by transducin: comparison of phospholipid bilayers to rod outer segment membranes Biochemistry 31, 9502-9512
35. Imai, H., Kojima, D., Oura, T., Tachibanaki, S., Terakita, A., and Shichida, Y. (1997) Single amino acid residue as a functional determinant of rod and cone visual pigments Proc. Natl. Acad. Sci. U. S. A. 94, 2322-2326
36. Kennedy, M. J., Dunn, F. A., and Hurley, J. B. (2004) Visual pigment phosphorylation but not transducin translocation can contribute to light adaptation in zebrafish cones Neuron 41, 915-928
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. He, W., Cowan, C. W., and Wensel, T. G. (1998) RGS9, a GTPase accelerator for phototransduction Neuron 20, 95-102
39. 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
40. Zhang, X., Wensel, T. G., and Kraft, T. W. (2003) GTPase regulators and photoresponses in cones of the eastern chipmunk J. Neurosci. 23, 1287-1297
41. 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 A Nature 409, 1071-1077
42. Hu, G. and Wensel, T. G. (2002) R9AP, a membrane anchor for the photoreceptor GTPase accelerating protein, RGS9-1 Proc. Natl. Acad. Sci. U. S. A. 99, 9755-9760
43. Lishko, P. V., Martemyanov, K. A., Hopp, J. A., and Arshavsky, V. Y. (2002) Specific binding of RGS9-Gβ5L to protein anchor in photoreceptor membranes greatly enhances its catalytic activity J. Biol. Chem. 277, 24376-24381
44. Guex, N. and Peitsch, M. C. (1997) SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling Electrophoresis 18, 2714-2723
45. DeLano, W. L. (2004) The PyMOL molecular graphics system; http://www.pymol.org.