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Initial Crystallographic Studies of Visual Arrestin: Insights and Perspectives

  • Joel A. HirschEmail author
Chapter

Abstract

Crystallographic studies of visual arrestin in the late nineties built upon fundamental biochemical work that had identified arrestins as proteins central to desensitization of GPCR signaling. The structural findings revealed the arrestin fold that had two related domains and a C-tail, which folded onto the molecule’s surface. The structures had a curious “polar core” that sat at the fulcrum of the two domains and which acts as an active site for conformational activation. The structures also served as the basis for elaborating the arrestin fold, found in all the kingdoms of life. Finally, the results suggested that quaternary structure i.e. the oligomeric state played a role in self-regulation.

Keywords

Arrestin Crystal structure Arrestin fold Phosphate sensor Activation Conformational change 

References

  1. Alvarez CE (2008) On the origins of arrestin and rhodopsin. BMC Evol Biol 8:222CrossRefPubMedPubMedCentralGoogle Scholar
  2. Aubry L, Guetta D, Klein G (2009) The arrestin fold: variations on a theme. Curr Genomics 10:133–142CrossRefPubMedPubMedCentralGoogle Scholar
  3. Benovic JL, Strasser RH, Caron MG, Lefkowitz RJ (1986) Beta-adrenergic receptor kinase: identification of a novel protein kinase that phosphorylates the agonist-occupied form of the receptor. Proc Natl Acad Sci USA 83:2797–2801CrossRefPubMedPubMedCentralGoogle Scholar
  4. Benovic JL, Kuhn H, Weyand I, Codina J, Caron MG, Lefkowitz RJ (1987) Functional desensitization of the isolated beta-adrenergic receptor by the beta-adrenergic receptor kinase: potential role of an analog of the retinal protein arrestin (48-kDa protein). Proc Natl Acad Sci USA 84:8879–8882CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bolon DN, Mayo SL (2001) Polar residues in the protein core of Escherichia coli thioredoxin are important for fold specificity. Biochemistry 40:10047–10053CrossRefPubMedGoogle Scholar
  6. Chen Q, Zhuo Y, Kim M, Hanson SM, Francis DJ, Vishnivetskiy SA, Altenbach C, Klug CS, Hubbell WL, Gurevich VV (2014) Self-association of arrestin family members. Handb Exp Pharmacol 219:205–223CrossRefPubMedPubMedCentralGoogle Scholar
  7. Cumberworth A, Lamour G, Babu MM, Gsponer J (2013) Promiscuity as a functional trait: intrinsically disordered regions as central players of interactomes. Biochem J 454:361–369CrossRefPubMedGoogle Scholar
  8. Dixon RA, Kobilka BK, Strader DJ, Benovic JL, Dohlman HG, Frielle T, Bolanowski MA, Bennett CD, Rands E, Diehl RE, Mumford RA, Slater EE, Sigal IS, Caron MG, Lefkowitz RJ, Strader CD (1986) Cloning of the gene and cDNA for mammalian beta-adrenergic receptor and homology with rhodopsin. Nature 321:75–79CrossRefPubMedGoogle Scholar
  9. Granzin J, Wilden U, Choe HW, Labahn J, Krafft B, Buldt G (1998) X-ray crystal structure of arrestin from bovine rod outer segments. Nature 391:918–921CrossRefPubMedGoogle Scholar
  10. Granzin J, Stadler A, Cousin A, Schlesinger R, Batra-Safferling R (2015) Structural evidence for the role of polar core residue Arg175 in arrestin activation. Sci Rep 5:15808CrossRefPubMedPubMedCentralGoogle Scholar
  11. Gurevich VV, Benovic JL (1992) Cell-free expression of visual arrestin. Truncation mutagenesis identifies multiple domains involved in rhodopsin interaction. J Biol Chem 267:21919–21923PubMedGoogle Scholar
  12. Gurevich VV, Benovic JL (1993) Visual arrestin interaction with rhodopsin: sequential multisite binding ensures strict selectivity towards light-activated phosphorylated rhodopsin. J Biol Chem 268:11628–11638PubMedGoogle Scholar
  13. Gurevich VV, Benovic JL (1995) Visual arrestin binding to rhodopsin: diverse functional roles of positively charged residues within the phosphorylation-recignition region of arrestin. J Biol Chem 270:6010–6016CrossRefPubMedGoogle Scholar
  14. Gurevich VV, Benovic JL (1997) Mechanism of phosphorylation-recognition by visual arrestin and the transition of arrestin into a high affinity binding state. Mol Pharmacol 51:161–169PubMedGoogle Scholar
  15. Han M, Gurevich VV, Vishnivetskiy SA, Sigler PB, Schubert C (2001) Crystal structure of beta-arrestin at 1.9 Å: possible mechanism of receptor binding and membrane translocation. Structure 9:869–880CrossRefPubMedGoogle Scholar
  16. Hanson SM, Francis DJ, Vishnivetskiy SA, Kolobova EA, Hubbell WL, Klug CS, Gurevich VV (2006) Differential interaction of spin-labeled arrestin with inactive and active phosphorhodopsin. Proc Natl Acad Sci USA 103:4900–4905CrossRefPubMedPubMedCentralGoogle Scholar
  17. Hanson SM, Gurevich EV, Vishnivetskiy SA, Ahmed MR, Song X, Gurevich VV (2007a) Each rhodopsin molecule binds its own arrestin. Proc Nat Acad Sci USA 104:3125–3128CrossRefPubMedPubMedCentralGoogle Scholar
  18. Hanson SM, Van Eps N, Francis DJ, Altenbach C, Vishnivetskiy SA, Arshavsky VY, Klug CS, Hubbell WL, Gurevich VV (2007b) Structure and function of the visual arrestin oligomer. EMBO J 26:1726–1736CrossRefPubMedPubMedCentralGoogle Scholar
  19. Hanson SM, Dawson ES, Francis DJ, Van Eps N, Klug CS, Hubbell WL, Meiler J, Gurevich VV (2008) A model for the solution structure of the rod arrestin tetramer. Structure 16:924–934CrossRefPubMedPubMedCentralGoogle Scholar
  20. Hirsch JA, Schubert C, Gurevich VV, Sigler PB (1999) The 2.8 Å crystal structure of visual arrestin: a model for arrestin’s regulation. Cell 97:257–269CrossRefPubMedGoogle Scholar
  21. Kang Y, Zhou XE, Gao X, He Y, Liu W, Ishchenko A, Barty A, White TA, Yefanov O, Han GW, Xu Q, de Waal PW, Ke J, Tan MH, Zhang C, Moeller A, West GM, Pascal BD, Van Eps N, Caro LN, Vishnivetskiy SA, Lee RJ, Suino-Powell KM, Gu X, Pal K, Ma J, Zhi X, Boutet S, Williams GJ, Messerschmidt M, Gati C, Zatsepin NA, Wang D, James D, Basu S, Roy-Chowdhury S, Conrad CE, Coe J, Liu H, Lisova S, Kupitz C, Grotjohann I, Fromme R, Jiang Y, Tan M, Yang H, Li J, Wang M, Zheng Z, Li D, Howe N, Zhao Y, Standfuss J, Diederichs K, Dong Y, Potter CS, Carragher B, Caffrey M, Jiang H, Chapman HN, Spence JC, Fromme P, Weierstall U, Ernst OP, Katritch V, Gurevich VV, Griffin PR, Hubbell WL, Stevens RC, Cherezov V, Melcher K, Xu HE (2015) Crystal structure of rhodopsin bound to arrestin by femtosecond X-ray laser. Nature 523:561–567CrossRefPubMedPubMedCentralGoogle Scholar
  22. Kim YJ, Hofmann KP, Ernst OP, Scheerer P, Choe HW, Sommer ME (2013) Crystal structure of pre-activated arrestin p44. Nature 497:142–146CrossRefPubMedGoogle Scholar
  23. Kuhn H, Hall SW, Wilden U (1984) Light-induced binding of 48-kDa protein to photoreceptor membranes is highly enhanced by phosphorylation of rhodopsin. FEBS Lett 176:473–478CrossRefPubMedGoogle Scholar
  24. Li W, Kinch LN, Karplus PA, Grishin NV (2015) ChSeq: a database of chameleon sequences. Protein Sci 24:1075–1086CrossRefPubMedPubMedCentralGoogle Scholar
  25. Lohse MJ, Benovic JL, Codina J, Caron MG, Lefkowitz RJ (1990) Beta-arrestin: a protein that regulates beta-adrenergic receptor function. Science 248:1547–1550CrossRefPubMedGoogle Scholar
  26. Lucas M, Gershlick DC, Vidaurrazaga A, Rojas AL, Bonifacino JS, Hierro A (2016) Structural mechanism for cargo recognition by the retromer complex. Cell 167(1623–1635):e1614Google Scholar
  27. Milano SK, Pace HC, Kim YM, Brenner C, Benovic JL (2002) Scaffolding functions of arrestin-2 revealed by crystal structure and mutagenesis. Biochemistry 41:3321–3328CrossRefPubMedGoogle Scholar
  28. Ovchinnikov YA (1982) Rhodopsin and bacteriorhodopsin: structure-function relationship. FEBS Lett 148:179–191CrossRefPubMedGoogle Scholar
  29. Palczewski K, Buczylko J, Imami NR, McDowell JH, Hargrave PA (1991a) Role of the carboxyl-terminal region of arrestin in binding to phosphorylated rhodopsin. J Biol Chem 266:15334–15339PubMedGoogle Scholar
  30. Palczewski K, Pulvermuller A, Buczylko J, Hofmann KP (1991b) Phosphorylated rhodopsin and heparin induce similar conformational changes in arrestin. J Biol Chem 266:18649–18654PubMedGoogle Scholar
  31. Palczewski K, Buczylko J, Ohguro H, Annan RS, Carr SA, Crabb JW, Kaplan MW, Johnson RS, Walsh KA (1994) Characterization of a truncated form of arrestin isolated from bovine rod outer segments. Protein Sci 3:314–324CrossRefPubMedPubMedCentralGoogle Scholar
  32. Schleicher A, Kuhn H, Hofmann KP (1989) Kinetics, binding constant, and activation energy of the 48-kDa protein-rhodopsin complex by extra-metarhodopsin II. Biochemistry 28:1770–1775CrossRefPubMedGoogle Scholar
  33. Schubert C, Hirsch JA, Gurevich VV, Engelman DM, Sigler PB, Fleming KG (1999) Visual arrestin activity may be regulated by self-association. J Biol Chem 274:21186–21190CrossRefPubMedGoogle Scholar
  34. Shi H, Rojas R, Bonifacino JS, Hurley JH (2006) The retromer subunit Vps26 has an arrestin fold and binds Vps35 through its C-terminal domain. Nat Struct Mol Biol 13:540–548CrossRefPubMedPubMedCentralGoogle Scholar
  35. Shinohara T, Dietzschold B, Craft CM, Wistow G, Early JJ, Donoso LA, Horwitz J, Tao R (1987) Primary and secondary structure of bovine retinal S antigen (48-kDa protein). Proc Natl Acad Sci USA 84:6975–6979CrossRefPubMedPubMedCentralGoogle Scholar
  36. Song X, Vishnivetskiy SA, Seo J, Chen J, Gurevich EV, Gurevich VV (2011) Arrestin-1 expression in rods: balancing functional performance and photoreceptor health. Neuroscience 174:37–49CrossRefPubMedGoogle Scholar
  37. Strissel KJ, Sokolov M, Trieu LH, Arshavsky VY (2006) Arrestin translocation is induced at a critical threshold of visual signaling and is superstoichiometric to bleached rhodopsin. J Neurosci 26:1146–1153CrossRefPubMedGoogle Scholar
  38. Sutton RB, Vishnivetskiy SA, Robert J, Hanson SM, Raman D, Knox BE, Kono M, Navarro J, Gurevich VV (2005) Crystal structure of cone arrestin at 2.3 Å: evolution of receptor specificity. J Mol Biol 354:1069–1080CrossRefPubMedGoogle Scholar
  39. Vishnivetskiy SA, Paz CL, Schubert C, Hirsch JA, Sigler PB, Gurevich VV (1999) How does arrestin respond to the phosphorylated state of rhodopsin? J Biol Chem 274:11451–11454CrossRefPubMedGoogle Scholar
  40. Wacker WB, Donoso LA, Kalsow CM, Yankeelov JA Jr, Organisciak DT (1977) Experimental allergic uveitis. Isolation, characterization, and localization of a soluble uveitopathogenic antigen from bovine retina. J Immunol 119:1949–1958PubMedGoogle Scholar
  41. Wilden U, Hall SW, Kuhn H (1986a) Phosphodiesterase activation by photoexcited rhodopsin is quenched when rhodopsin is phosphorylated and binds the intrinsic 48-kDa protein of rod outer segments. Proc Natl Acad Sci 83:1174–1178CrossRefPubMedPubMedCentralGoogle Scholar
  42. Wilden U, Wust E, Weyand I, Kuhn H (1986b) Rapid affinity purification of retinal arrestin (48 kDa protein) via its light-dependent binding to phosphorylated rhodopsin. FEBS Lett 207:292–295Google Scholar
  43. Wilden U, Choe HW, Krafft B, Granzin J (1997) Crystallization and preliminary X-ray analysis of arrestin from bovine rod outer segment. FEBS Lett 415:268–270CrossRefPubMedGoogle Scholar
  44. Yamaki K, Takahashi Y, Sakuragi S, Matsubara K (1987) Molecular cloning of the S-antigen cDNA from bovine retina. Biochem Biophys Res Commun 142:904–910CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Department of Biochemistry and Molecular Biology, Sagol School of Neuroscience, George S. Wise Faculty of Life SciencesTel Aviv UniversityTel AvivIsrael

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