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. 1994 Dec;3(12):2428–2434. doi: 10.1002/pro.5560031226

Topographic study of arrestin using differential chemical modifications and hydrogen/deuterium exchange.

H Ohguro 1, K Palczewski 1, K A Walsh 1, R S Johnson 1
PMCID: PMC2142757  PMID: 7756996

Abstract

Arrestin is involved in the quenching of phototransduction by binding to photoactivated and phosphorylated rhodopsin (P-Rho*). To study its conformational changes and regions interacting with P-Rho*, arrestin was subjected to (1) differential acetylation at lysine residues in the presence and absence of P-Rho*, and (2) amide hydrogen/deuterium exchange. Labeled protein was proteolysed and analyzed by mass spectrometry. Three Lys residues, 28, 176, and 211, were protected from acetylation in native arrestin, although they were not located in regions exhibiting slow amide hydrogen exchange rates. The presence of P-Rho* protected lysine 201 from acetylation and partially protected 14 other lysyl residues, including (2, 5), (163, 166, 167), (232, 235, 236, 238), (267, 276), (298, 300), and 367, where parentheses indicate lysine residues found within the same peptide. In contrast, in the C-terminal region of arrestin, lysyl residues (386, 392, 395) were more exposed upon binding to P-Rho*. These data allowed us to identify functional regions in the arrestin molecule.

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Selected References

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  1. Attramadal H., Arriza J. L., Aoki C., Dawson T. M., Codina J., Kwatra M. M., Snyder S. H., Caron M. G., Lefkowitz R. J. Beta-arrestin2, a novel member of the arrestin/beta-arrestin gene family. J Biol Chem. 1992 Sep 5;267(25):17882–17890. [PubMed] [Google Scholar]
  2. Biemann K. Sequencing of peptides by tandem mass spectrometry and high-energy collision-induced dissociation. Methods Enzymol. 1990;193:455–479. doi: 10.1016/0076-6879(90)93433-l. [DOI] [PubMed] [Google Scholar]
  3. Buechler J. A., Taylor S. S. Identification of aspartate-184 as an essential residue in the catalytic subunit of cAMP-dependent protein kinase. Biochemistry. 1988 Sep 20;27(19):7356–7361. doi: 10.1021/bi00419a027. [DOI] [PubMed] [Google Scholar]
  4. Chabre M., Deterre P. Molecular mechanism of visual transduction. Eur J Biochem. 1989 Feb 1;179(2):255–266. doi: 10.1111/j.1432-1033.1989.tb14549.x. [DOI] [PubMed] [Google Scholar]
  5. Craft C. M., Whitmore D. H., Wiechmann A. F. Cone arrestin identified by targeting expression of a functional family. J Biol Chem. 1994 Feb 11;269(6):4613–4619. [PubMed] [Google Scholar]
  6. Englander J. J., Rogero J. R., Englander S. W. Protein hydrogen exchange studied by the fragment separation method. Anal Biochem. 1985 May 15;147(1):234–244. doi: 10.1016/0003-2697(85)90033-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Englander S. W., Kallenbach N. R. Hydrogen exchange and structural dynamics of proteins and nucleic acids. Q Rev Biophys. 1983 Nov;16(4):521–655. doi: 10.1017/s0033583500005217. [DOI] [PubMed] [Google Scholar]
  8. Fenn J. B., Mann M., Meng C. K., Wong S. F., Whitehouse C. M. Electrospray ionization for mass spectrometry of large biomolecules. Science. 1989 Oct 6;246(4926):64–71. doi: 10.1126/science.2675315. [DOI] [PubMed] [Google Scholar]
  9. Gregory R. B., Rosenberg A. Protein conformational dynamics measured by hydrogen isotope exchange techniques. Methods Enzymol. 1986;131:448–508. doi: 10.1016/0076-6879(86)31052-8. [DOI] [PubMed] [Google Scholar]
  10. Gurevich V. V., Benovic J. L. Cell-free expression of visual arrestin. Truncation mutagenesis identifies multiple domains involved in rhodopsin interaction. J Biol Chem. 1992 Oct 25;267(30):21919–21923. [PubMed] [Google Scholar]
  11. Gurevich V. V., Benovic J. L. Visual arrestin interaction with rhodopsin. Sequential multisite binding ensures strict selectivity toward light-activated phosphorylated rhodopsin. J Biol Chem. 1993 Jun 5;268(16):11628–11638. [PubMed] [Google Scholar]
  12. Gurevich V. V., Chen C. Y., Kim C. M., Benovic J. L. Visual arrestin binding to rhodopsin. Intramolecular interaction between the basic N terminus and acidic C terminus of arrestin may regulate binding selectivity. J Biol Chem. 1994 Mar 25;269(12):8721–8727. [PubMed] [Google Scholar]
  13. Gurevich V. V., Richardson R. M., Kim C. M., Hosey M. M., Benovic J. L. Binding of wild type and chimeric arrestins to the m2 muscarinic cholinergic receptor. J Biol Chem. 1993 Aug 15;268(23):16879–16882. [PubMed] [Google Scholar]
  14. Hofmann K. P., Pulvermüller A., Buczyłko J., Van Hooser P., Palczewski K. The role of arrestin and retinoids in the regeneration pathway of rhodopsin. J Biol Chem. 1992 Aug 5;267(22):15701–15706. [PubMed] [Google Scholar]
  15. Hyde D. R., Mecklenburg K. L., Pollock J. A., Vihtelic T. S., Benzer S. Twenty Drosophila visual system cDNA clones: one is a homolog of human arrestin. Proc Natl Acad Sci U S A. 1990 Feb;87(3):1008–1012. doi: 10.1073/pnas.87.3.1008. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kieselbach T., Irrgang K. D., Rüppel H. A segment corresponding to amino acids Val170-Arg182 of bovine arrestin is capable of binding to phosphorylated rhodopsin. Eur J Biochem. 1994 Nov 15;226(1):87–97. doi: 10.1111/j.1432-1033.1994.tb20029.x. [DOI] [PubMed] [Google Scholar]
  17. Krupnick J. G., Gurevich V. V., Schepers T., Hamm H. E., Benovic J. L. Arrestin-rhodopsin interaction. Multi-site binding delineated by peptide inhibition. J Biol Chem. 1994 Feb 4;269(5):3226–3232. [PubMed] [Google Scholar]
  18. Lohse M. J., Benovic J. L., Codina J., Caron M. G., Lefkowitz R. J. beta-Arrestin: a protein that regulates beta-adrenergic receptor function. Science. 1990 Jun 22;248(4962):1547–1550. doi: 10.1126/science.2163110. [DOI] [PubMed] [Google Scholar]
  19. McDowell J. H., Nawrocki J. P., Hargrave P. A. Phosphorylation sites in bovine rhodopsin. Biochemistry. 1993 May 11;32(18):4968–4974. doi: 10.1021/bi00069a036. [DOI] [PubMed] [Google Scholar]
  20. Murakami A., Yajima T., Sakuma H., McLaren M. J., Inana G. X-arrestin: a new retinal arrestin mapping to the X chromosome. FEBS Lett. 1993 Nov 15;334(2):203–209. doi: 10.1016/0014-5793(93)81712-9. [DOI] [PubMed] [Google Scholar]
  21. Ohguro H., Johnson R. S., Ericsson L. H., Walsh K. A., Palczewski K. Control of rhodopsin multiple phosphorylation. Biochemistry. 1994 Feb 1;33(4):1023–1028. doi: 10.1021/bi00170a022. [DOI] [PubMed] [Google Scholar]
  22. Palczewski K., Benovic J. L. G-protein-coupled receptor kinases. Trends Biochem Sci. 1991 Oct;16(10):387–391. doi: 10.1016/0968-0004(91)90157-q. [DOI] [PubMed] [Google Scholar]
  23. Palczewski K., Buczylko J., Ohguro H., Annan R. S., Carr S. A., Crabb J. W., Kaplan M. W., Johnson R. S., Walsh K. A. Characterization of a truncated form of arrestin isolated from bovine rod outer segments. Protein Sci. 1994 Feb;3(2):314–324. doi: 10.1002/pro.5560030215. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Palczewski K., Buczyłko J., Imami N. R., McDowell J. H., Hargrave P. A. Role of the carboxyl-terminal region of arrestin in binding to phosphorylated rhodopsin. J Biol Chem. 1991 Aug 15;266(23):15334–15339. [PubMed] [Google Scholar]
  25. Palczewski K., Pulvermüller A., Buczylko J., Gutmann C., Hofmann K. P. Binding of inositol phosphates to arrestin. FEBS Lett. 1991 Dec 16;295(1-3):195–199. doi: 10.1016/0014-5793(91)81416-6. [DOI] [PubMed] [Google Scholar]
  26. Palczewski K., Pulvermüller A., Buczyłko J., Hofmann K. P. Phosphorylated rhodopsin and heparin induce similar conformational changes in arrestin. J Biol Chem. 1991 Oct 5;266(28):18649–18654. [PubMed] [Google Scholar]
  27. Palczewski K., Riazance-Lawrence J. H., Johnson W. C., Jr Structural properties of arrestin studied by chemical modification and circular dichroism. Biochemistry. 1992 Apr 28;31(16):3902–3906. doi: 10.1021/bi00131a003. [DOI] [PubMed] [Google Scholar]
  28. Palczewski K. Structure and functions of arrestins. Protein Sci. 1994 Sep;3(9):1355–1361. doi: 10.1002/pro.5560030901. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Papac D. I., Oatis J. E., Jr, Crouch R. K., Knapp D. R. Mass spectrometric identification of phosphorylation sites in bleached bovine rhodopsin. Biochemistry. 1993 Jun 15;32(23):5930–5934. doi: 10.1021/bi00074a002. [DOI] [PubMed] [Google Scholar]
  30. Riordan J. F. Functional arginyl residues in carboxypeptidase A. Modification with butanedione. Biochemistry. 1973 Sep 25;12(20):3915–3923. doi: 10.1021/bi00744a020. [DOI] [PubMed] [Google Scholar]
  31. Schleicher A., Kühn H., Hofmann K. P. Kinetics, binding constant, and activation energy of the 48-kDa protein-rhodopsin complex by extra-metarhodopsin II. Biochemistry. 1989 Feb 21;28(4):1770–1775. doi: 10.1021/bi00430a052. [DOI] [PubMed] [Google Scholar]
  32. Shinohara T., Dietzschold B., Craft C. M., Wistow G., Early J. J., Donoso L. A., Horwitz J., Tao R. Primary and secondary structure of bovine retinal S antigen (48-kDa protein). Proc Natl Acad Sci U S A. 1987 Oct;84(20):6975–6979. doi: 10.1073/pnas.84.20.6975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Smith D. P., Shieh B. H., Zuker C. S. Isolation and structure of an arrestin gene from Drosophila. Proc Natl Acad Sci U S A. 1990 Feb;87(3):1003–1007. doi: 10.1073/pnas.87.3.1003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Smith W. C., Milam A. H., Dugger D., Arendt A., Hargrave P. A., Palczewski K. A splice variant of arrestin. Molecular cloning and localization in bovine retina. J Biol Chem. 1994 Jun 3;269(22):15407–15410. [PubMed] [Google Scholar]
  35. Sterne-Marr R., Gurevich V. V., Goldsmith P., Bodine R. C., Sanders C., Donoso L. A., Benovic J. L. Polypeptide variants of beta-arrestin and arrestin3. J Biol Chem. 1993 Jul 25;268(21):15640–15648. [PubMed] [Google Scholar]
  36. Suckau D., Mak M., Przybylski M. Protein surface topology-probing by selective chemical modification and mass spectrometric peptide mapping. Proc Natl Acad Sci U S A. 1992 Jun 15;89(12):5630–5634. doi: 10.1073/pnas.89.12.5630. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Yamada T., Takeuchi Y., Komori N., Kobayashi H., Sakai Y., Hotta Y., Matsumoto H. A 49-kilodalton phosphoprotein in the Drosophila photoreceptor is an arrestin homolog. Science. 1990 Apr 27;248(4954):483–486. doi: 10.1126/science.2158671. [DOI] [PubMed] [Google Scholar]

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