Detergents stabilize the conformation of phosphodiesterase 6

Biochemistry

Volumn 50, Issue 44, 2011, Pages 9520-9531

  Baker, Bo Y ^a   Palczewski, Krzysztof ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BASAL ACTIVITIES; CATALYTIC CORE; HETEROLOGOUS EXPRESSION; MEMBRANE-BOUND; NATIVE MEMBRANES; PHOSPHODIESTERASES; ROD PHOTORECEPTORS; STRUCTURAL STUDIES;

ESTERS; PURIFICATION; SIGNAL TRANSDUCTION;

SOAPS (DETERGENTS);

BINDING PROTEIN; DETERGENT; HOLOENZYME; PHOSPHODIESTERASE VI; PRENYL BINDING PROTEIN DELTA; REACTIVE OXYGEN METABOLITE; TRYPSIN; UNCLASSIFIED DRUG;

ADSORPTION; ARTICLE; ELECTRON MICROSCOPY; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME CONFORMATION; ENZYME PURIFICATION; ENZYME STRUCTURE; PRIORITY JOURNAL; PROTEIN ISOLATION; PROTEIN PRENYLATION; PROTEIN STABILITY; SIGNAL TRANSDUCTION;

ANIMALS; CATALYTIC DOMAIN; CATTLE; CYCLIC NUCLEOTIDE PHOSPHODIESTERASES, TYPE 6; DETERGENTS; ENZYME STABILITY; PROTEIN CONFORMATION; PROTEOLYSIS; SORBITOL; SUCROSE;

EID: 80155206862     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi2014695     Document Type: Article

References (48)

1. 2+-binding proteins in the retina Trends Neurosci. 19, 547-554 (Pubitemid 26390175)
2. Conti, M. and Beavo, J. (2007) Biochemistry and physiology of cyclic nucleotide phosphodiesterases: Essential components in cyclic nucleotide signaling Annu. Rev. Biochem. 76, 481-511
3. Artemyev, N. O., Surendran, R., Lee, J. C., and Hamm, H. E. (1996) Subunit structure of rod cGMP-phosphodiesterase J. Biol. Chem. 271, 25382-25388 (Pubitemid 26337908)
4. Baehr, W., Devlin, M. J., and Applebury, M. L. (1979) Isolation and characterization of cGMP phosphodiesterase from bovine rod outer segments J. Biol. Chem. 254, 11669-11677 (Pubitemid 10140090)
5. Deterre, P., Bigay, J., Forquet, F., Robert, M., and Chabre, M. (1988) cGMP phosphodiesterase of retinal rods is regulated by two inhibitory subunits Proc. Natl. Acad. Sci. U.S.A. 85, 2424-2428
6. Artemyev, N. O. and Hamm, H. E. (1992) Two-site high-affinity interaction between inhibitory and catalytic subunits of rod cyclic GMP phosphodiesterase Biochem. J. 283 (Part 1) 273-279
7. Artemyev, N. O., Rarick, H. M., Mills, J. S., Skiba, N. P., and Hamm, H. E. (1992) Sites of interaction between rod G-protein α-subunit and cGMP-phosphodiesterase γ-subunit. Implications for the phosphodiesterase activation mechanism J. Biol. Chem. 267, 25067-25072
8. Hurley, J. B. and Stryer, L. (1982) Purification and characterization of the γ regulatory subunit of the cyclic GMP phosphodiesterase from retinal rod outer segments J. Biol. Chem. 257, 11094-11099 (Pubitemid 13208917)
9. Song, J., Guo, L. W., Muradov, H., Artemyev, N. O., Ruoho, A. E., and Markley, J. L. (2008) Intrinsically disordered γ-subunit of cGMP phosphodiesterase encodes functionally relevant transient secondary and tertiary structure Proc. Natl. Acad. Sci. U.S.A. 105, 1505-1510 (Pubitemid 351346544)
10. Anant, J. S., Ong, O. C., Xie, H. Y., Clarke, S., OBrien, P. J., and Fung, B. K. (1992) In vivo differential prenylation of retinal cyclic GMP phosphodiesterase catalytic subunits J. Biol. Chem. 267, 687-690
11. Qin, N. and Baehr, W. (1994) Expression and mutagenesis of mouse rod photoreceptor cGMP phosphodiesterase J. Biol. Chem. 269, 3265-3271 (Pubitemid 24237638)
12. Christiansen, J. R., Kolandaivelu, S., Bergo, M. O., and Ramamurthy, V. (2011) RAS-converting enzyme 1-mediated endoproteolysis is required for trafficking of rod phosphodiesterase 6 to photoreceptor outer segments Proc. Natl. Acad. Sci. U.S.A. 108, 8862-8866
13. Cook, T. A., Ghomashchi, F., Gelb, M. H., Florio, S. K., and Beavo, J. A. (2000) Binding of the δ subunit to rod phosphodiesterase catalytic subunits requires methylated, prenylated C-termini of the catalytic subunits Biochemistry 39, 13516-13523
14. Goc, A., Chami, M., Lodowski, D. T., Bosshart, P., Moiseenkova-Bell, V., Baehr, W., Engel, A., and Palczewski, K. (2010) Structural Characterization of the Rod cGMP Phosphodiesterase 6 J. Mol. Biol. 401, 363-373
15. Pandit, J., Forman, M. D., Fennell, K. F., Dillman, K. S., and Menniti, F. S. (2009) Mechanism for the allosteric regulation of phosphodiesterase 2A deduced from the X-ray structure of a near full-length construct Proc. Natl. Acad. Sci. U.S.A. 106, 18225-18230
16. Xu, R. X., Hassell, A. M., Vanderwall, D., Lambert, M. H., Holmes, W. D., Luther, M. A., Rocque, W. J., Milburn, M. V., Zhao, Y., Ke, H., and Nolte, R. T. (2000) Atomic structure of PDE4: Insights into phosphodiesterase mechanism and specificity Science 288, 1822-1825 (Pubitemid 30399019)
17. Sung, B. J., Hwang, K. Y., Jeon, Y. H., Lee, J. I., Heo, Y. S., Kim, J. H., Moon, J., Yoon, J. M., Hyun, Y. L., Kim, E., Eum, S. J., Park, S. Y., Lee, J. O., Lee, T. G., Ro, S., and Cho, J. M. (2003) Structure of the catalytic domain of human phosphodiesterase 5 with bound drug molecules Nature 425, 98-102 (Pubitemid 37101725)
18. Barren, B., Gakhar, L., Muradov, H., Boyd, K. K., Ramaswamy, S., and Artemyev, N. O. (2009) Structural basis of phosphodiesterase 6 inhibition by the C-terminal region of the γ-subunit EMBO J. 28, 3613-3622
19. Grizot, S., Faure, J., Fieschi, F., Vignais, P. V., Dagher, M. C., and Pebay-Peyroula, E. (2001) Crystal structure of the Rac1-RhoGDI complex involved in NADPH oxidase activation Biochemistry 40, 10007-10013 (Pubitemid 32800107)
20. Zhang, H., Constantine, R., Vorobiev, S., Chen, Y., Seetharaman, J., Huang, Y. J., Xiao, R., Montelione, G. T., Gerstner, C. D., Davis, M. W., Inana, G., Whitby, F. G., Jorgensen, E. M., Hill, C. P., Tong, L., and Baehr, W. (2011) UNC119 is required for G protein trafficking in sensory neurons Nat. Neurosci. 14, 874-880
21. Kajimura, N., Yamazaki, M., Morikawa, K., Yamazaki, A., and Mayanagi, K. (2002) Three-dimensional structure of non-activated cGMP phosphodiesterase 6 and comparison of its image with those of activated forms J. Struct. Biol. 139, 27-38 (Pubitemid 35304458)
22. Granovsky, A. E., Natochin, M., McEntaffer, R. L., Haik, T. L., Francis, S. H., Corbin, J. D., and Artemyev, N. O. (1998) Probing domain functions of chimeric PDE6α′/PDE5 cGMP-phosphodiesterase J. Biol. Chem. 273, 24485-24490 (Pubitemid 28454942)
23. Liu, X., Bulgakov, O. V., Wen, X. H., Woodruff, M. L., Pawlyk, B., Yang, J., Fain, G. L., Sandberg, M. A., Makino, C. L., and Li, T. (2004) AIPL1, the protein that is defective in Leber congenital amaurosis, is essential for the biosynthesis of retinal rod cGMP phosphodiesterase Proc. Natl. Acad. Sci. U.S.A. 101, 13903-13908 (Pubitemid 39298505)
24. Kolandaivelu, S., Huang, J., Hurley, J. B., and Ramamurthy, V. (2009) AIPL1, a protein associated with childhood blindness, interacts with α-subunit of rod phosphodiesterase (PDE6) and is essential for its proper assembly J. Biol. Chem. 284, 30853-30861
25. Okada, T., Le Trong, I., Fox, B. A., Behnke, C. A., Stenkamp, R. E., and Palczewski, K. (2000) X-ray diffraction analysis of three-dimensional crystals of bovine rhodopsin obtained from mixed micelles J. Struct. Biol. 130, 73-80 (Pubitemid 30470799)
26. Wang, G. (2008) NMR of membrane-associated peptides and proteins Curr. Protein Pept. Sci. 9, 50-69
27. Dobrovetsky, E., Menendez, J., Edwards, A. M., and Koth, C. M. (2007) A robust purification strategy to accelerate membrane proteomics Methods 41, 381-387 (Pubitemid 46400525)
28. Caffrey, M. (2003) Membrane protein crystallization J. Struct. Biol. 142, 108-132 (Pubitemid 36457895)
29. Cudney, R., Patel, S., Weisgraber, K., Newhouse, Y., and McPherson, A. (1994) Screening and optimization strategies for macromolecular crystal growth Acta Crystallogr. D50, 414-423
30. Papermaster, D. S. (1982) Preparation of retinal rod outer segments Methods Enzymol. 81, 48-52
31. 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
32. Brown, R. L. (1992) Functional regions of the inhibitory subunit of retinal rod cGMP phosphodiesterase identified by site-specific mutagenesis and fluorescence spectroscopy Biochemistry 31, 5918-5925
33. Goc, A., Angel, T. E., Jastrzebska, B., Wang, B., Wintrode, P. L., and Palczewski, K. (2008) Different properties of the native and reconstituted heterotrimeric G protein transducin Biochemistry 47, 12409-12419
34. Pentia, D. C., Hosier, S., Collupy, R. A., Valeriani, B. A., and Cote, R. H. (2005) Purification of PDE6 isozymes from mammalian retina Methods Mol. Biol. 307, 125-140
35. Catty, P., Pfister, C., Bruckert, F., and Deterre, P. (1992) The cGMP phosphodiesterase-transducin complex of retinal rods. Membrane binding and subunits interactions J. Biol. Chem. 267, 19489-19493
36. Gillespie, P. G. and Beavo, J. A. (1989) Inhibition and stimulation of photoreceptor phosphodiesterases by dipyridamole and M&B 22,948 Mol. Pharmacol. 36, 773-781 (Pubitemid 20008225)
37. Gillespie, P. G. and Beavo, J. A. (1989) cGMP is tightly bound to bovine retinal rod phosphodiesterase Proc. Natl. Acad. Sci. U.S.A. 86, 4311-4315 (Pubitemid 19154785)
38. Gillespie, P. G., Prusti, R. K., Apel, E. D., and Beavo, J. A. (1989) A soluble form of bovine rod photoreceptor phosphodiesterase has a novel 15-kDa subunit J. Biol. Chem. 264, 12187-12193 (Pubitemid 19191102)
39. Mou, H., Grazio, H. J., III, Cook, T. A., Beavo, J. A., and Cote, R. H. (1999) cGMP binding to noncatalytic sites on mammalian rod photoreceptor phosphodiesterase is regulated by binding of its γ and δ subunits J. Biol. Chem. 274, 18813-18820
40. 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
41. 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
42. Wensel, T. G. and Stryer, L. (1986) Reciprocal control of retinal rod cyclic GMP phosphodiesterase by its γ subunit and transducin Proteins 1, 90-99 (Pubitemid 17073406)
43. Skiba, N. P., Artemyev, N. O., and Hamm, H. E. (1995) The carboxyl terminus of the γ-subunit of rod cGMP phosphodiesterase contains distinct sites of interaction with the enzyme catalytic subunits and the α-subunit of transducin J. Biol. Chem. 270, 13210-13215
44. Takemoto, D. J., Hurt, D., Oppert, B., and Cunnick, J. (1992) Domain mapping of the retinal cyclic GMP phosphodiesterase γ-subunit. Function of the domains encoded by the three exons of the γ-subunit gene Biochem. J. 281 (Part 3) 637-643
45. Muradov, K. G., Granovsky, A. E., Schey, K. L., and Artemyev, N. O. (2002) Direct interaction of the inhibitory γ-subunit of rod cGMP phosphodiesterase (PDE6) with the PDE6 GAFa domains Biochemistry 41, 3884-3890 (Pubitemid 34251027)
46. Guo, L. W., Assadi-Porter, F. M., Grant, J. E., Wu, H., Markley, J. L., and Ruoho, A. E. (2007) One-step purification of bacterially expressed recombinant transducin α-subunit and isotopically labeled PDE6 γ-subunit for NMR analysis Protein Expression Purif. 51, 187-197 (Pubitemid 44821869)
47. Uversky, V. N., Permyakov, S. E., Zagranichny, V. E., Rodionov, I. L., Fink, A. L., Cherskaya, A. M., Wasserman, L. A., and Permyakov, E. A. (2002) Effect of zinc and temperature on the conformation of the γ subunit of retinal phosphodiesterase: A natively unfolded protein J. Proteome Res. 1, 149-159 (Pubitemid 36050264)
48. Pentia, D. C., Hosier, S., and Cote, R. H. (2006) The glutamic acid-rich protein-2 (GARP2) is a high affinity rod photoreceptor phosphodiesterase (PDE6)-binding protein that modulates its catalytic properties J. Biol. Chem. 281, 5500-5505 (Pubitemid 43847645)