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Ca2+-dependent regulatory activity of recoverin in photoreceptor raft structures: The role of caveolin-1

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Biochemistry (Moscow) Supplement Series A: Membrane and Cell Biology Aims and scope

Abstract

Recoverin is a Ca2+-binding protein implicated in the Ca2+-dependent regulation of desensitization of visual receptor rhodopsin in vertebrate retinal rods. Here we report that Ca2+ sensitivity of recoverin regulating rhodopsin phosphorylation increases in the presence of the photoreceptor membranes enriched in raft structures. The observed effect is mediated by a key protein component of raft structures caveolin-1. The presence of recombinant fragment Phe81-Arg101 of the caveolin-1 cytoplasmic domain enhances Ca2+ affinity of recoverin, therefore affecting its Ca2+-dependent regulatory activity.

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References

  1. Brown D.A., London E. 2000. Structure and function of sphingolipid- and cholesterol-rich membrane rafts. J. Biol. Chem. 275, 17221–17224.

    Article  CAS  PubMed  Google Scholar 

  2. Smart E.J., Ying Y., Donzell W.C., Anderson R.G. 1996. A role for caveolin in transport of cholesterol from endoplasmic reticulum to plasma membrane. J. Biol. Chem. 271, 29427–29435.

    Article  CAS  PubMed  Google Scholar 

  3. Anderson R.G. 1998. The caveolae membrane system. Annu. Rev. Biochem. 67, 199–225.

    Article  CAS  PubMed  Google Scholar 

  4. Seno K., Kishimoto M., Abe M., Higuchi Y., Mieda M., Owada Y., Yoshiyama W., Liu H., Hayashi F. 2001. Light- and guanosine 5′-3-O-(thio)triphosphate-sensitive localization of a G protein and its effector on detergent-resistant membrane rafts in rod photoreceptor outer segments. J. Biol. Chem. 276, 20813–20816.

    Article  CAS  PubMed  Google Scholar 

  5. Nair K.S., Balasubramanian N., Slepak V.Z. 2002. Signal-dependent translocation of transducin, RGS9-1-Gβ5L complex, and arrestin to detergent-resistant membrane rafts in photoreceptors. Curr. Biol. 12, 421–425.

    Article  CAS  PubMed  Google Scholar 

  6. Senin I.I., Höppner-Heitmann D., Polkovnikova O.O., Churumova V.A., Tikhomirova N.K., Philippov P.P., Koch K.W. 2004. Recoverin and rhodopsin kinase activity in detergent-resistant membrane rafts from rod outer segments. J. Biol. Chem. 279, 48647–48653.

    Article  CAS  PubMed  Google Scholar 

  7. Philippov P.P., Senin I.I., Koch K.-W. 2006. Recoverin: A calcium-dependent regulator of the visual-transduction. In: Neuronal calcium sensor proteins. Eds Philippov P., Koch K.-W. Nova Science Publishers. p. 139–151.

    Google Scholar 

  8. Kawamura S. 1993. Rhodopsin phosphorylation as a mechanism of cyclic GMP phosphodiesterase regulation by S-modulin. Nature. 362, 855–857.

    Article  CAS  PubMed  Google Scholar 

  9. Grigoriev I.I., Senin I.I., Tikhomirova N.K., Komolov K.E., Permyakov S.E., Zernii E.Yu., Koch K.W., Philippov, P.P. 2012. Synergetic effect of recoverin and calmodulin on regulation of rhodopsin kinase. Front. Mol. Neurosci. 5, 28.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  10. Komolov K.E., Senin I.I., Kovaleva N.A., Christoph M.P., Churumova V.A., Grigoriev I.I., Akhtar M., Philippov P.P., Koch K.W. 2009. Mechanism of rhodopsin kinase regulation by recoverin. J. Neurochem. 110, 72–79.

    Article  CAS  PubMed  Google Scholar 

  11. Gorodovikova E.N., Gimelbrant A.A., Senin I.I., Philippov P.P. 1994. Recoverin mediates the calcium effect upon rhodopsin phosphorylation and cGMP hydrolysis in bovine rerina rod cells. FEBS Lett. 349, 187–190.

    Article  CAS  PubMed  Google Scholar 

  12. Gorodovikova E.N., Senin I.I., Philippov P.P. 1994. Calcium-sensitive control of rhodopsin phosphorylation in the reconstituted system consisting of photoreceptor membranes, rhodopsin kinase and recoverin. FEBS Lett. 353, 171–172.

    Article  CAS  PubMed  Google Scholar 

  13. Permyakov S.E., Cherskaya A.M., Senin I.I., Zargarov A.A., Shulga-Morskoy S.V., Alekseev A.M., Zinchenko D.V., Lipkin V.M., Philippov P.P., Uversky V.N., Permyakov E.A. 2000. Effects of mutations in the calcium-binding sites of recoverin on its calcium affinity: Evidence for successive filling of the calcium binding sites. Protein Eng. 13, 783–790.

    Article  CAS  PubMed  Google Scholar 

  14. Senin I.I., Fischer T., Komolov K.E., Zinchenko D.V., Philippov P.P., Koch K.W. 2002. Ca2+-Myristoyl switch in the neuronal calcium sensor recoverin requires different functions of Ca2+-binding sites. J. Biol. Chem. 277, 50365–50372.

    Article  CAS  PubMed  Google Scholar 

  15. Weiergräber O.H., Senin I.I., Philippov P.P., Granzin J., Koch K.W. 2003. Impact of N-terminal myristoylation on the Ca2+-dependent conformational transition in recoverin. J. Biol. Chem. 278, 22972–22979.

    Article  PubMed  Google Scholar 

  16. Permyakov S.E., Senin I.I., Uversky V.N., Cherskaia A.M., Shul’ga-Morskoy S.V., Zinchenko D.V., Alekseev A.M., Zargarov A.A., Lipkin V.M., Philippov P.P., Permyakov E.A. 1999. Point amino acid substitutions in the Ca2+-binding centers of recoverin. I. Mechanism of successive filling of Ca2+-binding centers. Bioorg. Khim. (Rus.). 25, 742–746.

    CAS  Google Scholar 

  17. Uversky V.N., Permiakov S.E., Senin I.I., Cherskaia A.M., Shul’ga-Morskoy S.V., Zinchenko D.V., Alekseev A.M., Zargarov A.A., Lipkin V.M., Philippov P.P., Permiakov E.A. 2000. Single amino acid substitutions in the Ca2+-binding site of recoverin. II. The unusual behavior of the protein upon the binding of calcium ions. Bioorg. Khim. (Rus.). 26, 173–178.

    Google Scholar 

  18. Tanaka T., Ames J.B., Harvey T.S., Stryer L., Ikura M. 1995. Sequestration of the membrane-targeting myristoyl group of recoverin in the calcium-free state. Nature. 376, 444–447.

    Article  CAS  PubMed  Google Scholar 

  19. Gensch, T., Komolov, K.E., Senin I.I., Philippov P.P., Koch K.W. 2007. Ca2+-Dependent conformational changes in the neuronal Ca2+ sensor recoverin probed by the fluorescent dye Alexa647. Proteins. 66, 492–499.

    Article  CAS  PubMed  Google Scholar 

  20. Ames J.B., Ishima R., Tanaka T., Gordon J.I., Stryer L., Ikura M. 1997. Molecular mechanics of calciummyristoyl switches. Nature. 389, 198–202.

    Article  CAS  PubMed  Google Scholar 

  21. Valentine K.G., Mesleh M.F., Opella S.J., Ikura M., Ames J.B. 2003. Structure, topology, and dynamics of myristoylated recoverin bound to phospholipid bilayers. Biochemistry. 42, 6333–6340.

    Article  CAS  PubMed  Google Scholar 

  22. Ames J.B., Levay K., Wingard J.N., Lusin J.D., Slepak V.Z. 2006. Structural basis for calcium-induced inhibition of rhodopsin kinase by recoverin. J. Biol. Chem. 281, 37237–37245.

    Article  CAS  PubMed  Google Scholar 

  23. Zernii E.Y., Komolov K.E., Permyakov S.E., Kolpakova T., Dell’orco D., Poetzsch A., Knyazeva E.L., Grigoriev I.I., Permyakov E.A., Senin I.I., Philippov P.P., Koch K.W. 2011. Involvement of the recoverin C-terminal segment in recognition of the target enzyme rhodopsin kinase. Biochem. J. 435, 441–450.

    Article  CAS  PubMed  Google Scholar 

  24. Miyagawa Y., Ohguro H., Odagiri H., Maruyama I., Maeda T., Maeda A., Sasaki M., Nakazawa M. 2003. Aberrantly expressed recoverin is functionally associated with G-protein-coupled receptor kinases in cancer cell lines. Biochem. Biophys. Res. Commun. 300, 669–673.

    Article  CAS  PubMed  Google Scholar 

  25. Senin I.I., Zargarov A.A., Akhtar M., Philippov, P.P. 1997. Rhodopsin phosphorylation in bovine rod outer segments is more sensitive to the inhibitory action of recoverin at the low rhodopsin bleaching than it is at the high bleaching. FEBS Lett. 408, 251–254.

    Article  CAS  PubMed  Google Scholar 

  26. Permyakov S.E., Zernii E.Y., Knyazeva E.L., Denesyuk A.I., Nazipova A.A., Kolpakova T.V., Zinchenko D.V., Philippov P.P., Permyakov E.A., Senin I.I. 2012. Oxidation mimicking substitution of conservative cysteine in recoverin suppresses its membrane association. Amino acids. 42, 1435–1442.

    Article  CAS  PubMed  Google Scholar 

  27. Senin I.I., Tikhomirova N.K., Churumova V.A., Grigoriev I.I., Kolpakova T.A., Zinchenko D.V., Philippov P.P., Zernii E.Y. 2011. Amino acid sequences of two immune-dominant epitopes of recoverin are involved in Ca2+/recoverin-dependent inhibition of phosphorylation of rhodopsin. Biochemistry (Moscow). 76, 332–338.

    Article  CAS  Google Scholar 

  28. Li S., Okamoto T., Chun M., Sargiacomo M., Casanova J.E., Hansen S.E., Nishimoto I., Lisanti M.P. 1995. Evidence for a regulated interaction between heterotrimeric G proteins and caveolin. J. Biol. Chem. 270, 15693–15701.

    Article  CAS  PubMed  Google Scholar 

  29. Weiergräber O.H., Senin I.I., Zernii E.Y., Churumova V.A., Kovaleva N.A., Nazipova A.A., Permyakov S.E., Permyakov E.A., Philippov P.P., Granzin J., Koch K.W. 2006. Tuning of a neuronal calcium sensor. J. Biol. Chem. 281, 37594–37602.

    Article  PubMed  Google Scholar 

  30. Senin I.I., Bosch L., Ramon E., Zernii E.Y., Manyosa J., Philippov P.P., Garriga P. 2006. Ca2+/recoverin dependent regulation of phosphorylation of the rhodopsin mutant R135L associated with retinitis pigmentosa. Biochem. Biophys. Res. Commun. 349, 345–352.

    Article  CAS  PubMed  Google Scholar 

  31. Ramon E., Cordomi A., Bosch L., Zernii E.Y., Senin I.I., Manyosa J., Philippov P.P., Perez J.J., Garriga P. 2007. Critical role of electrostatic interactions of amino acids at the cytoplasmic region of helices 3 and 6 in rhodopsin conformational properties and activation. J. Biol. Chem. 282, 14272–14282.

    Article  CAS  PubMed  Google Scholar 

  32. Bradford 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.

    Article  CAS  PubMed  Google Scholar 

  33. Komolov K.E., Zinchenko D.V., Churumova V.A., Vaganova S.A., Weiergraber O.H., Senin I.I., Philippov P.P., Koch K.W. 2005. One of the Ca2+-binding sites of recoverin exclusively controls interaction with rhodopsin kinase. Biol. Chem. 386, 285–289.

    Article  CAS  PubMed  Google Scholar 

  34. Boesze-Battaglia K., Dispoto J., Kahoe M.A. 2002. Association of a photoreceptor-specific tetraspanin protein, ROM-1, with triton X-100-resistant membrane rafts from rod outer segment disk membranes. J. Biol. Chem. 277, 41843–41849.

    Article  CAS  PubMed  Google Scholar 

  35. Boesze-Battaglia K., Hennessey T., Albert A.D. 1989. Cholesterol heterogeneity in bovine rod outer segment disk membranes. J. Biol. Chem. 264, 8151–8155.

    CAS  PubMed  Google Scholar 

  36. Boesze-Battaglia K., Fliesler S.J., Albert A.D. 1990. Relationship of cholesterol content to spatial distribution and age of disc membranes in retinal rod outer segments. J. Biol. Chem. 265, 18867–18870.

    CAS  PubMed  Google Scholar 

  37. Woodruff M.L., Wang Z., Chung H.Y., Redmond T.M., Fain G.L., Lem J. 2003 Spontaneous activity of opsin apoprotein is a cause of Leber congenital amaurosis. Nat. Genet. 35, 158–164.

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Belozersky Institute of Physico-Chemical Biology, Moscow Lomonosov Moscow State University, Moscow, 119991, Russia

    E. Y. Zernii, I. I. Grigoriev, E. E. Skorikova, V. E. Baksheeva, P. P. Philippov & I. I. Senin

  2. Branch of Shemyakin-Ovchinnikov Institute of Bioorganic Chemistry of the Russian Academy of Sciences, Pushchino, Moscow oblast, 142290, Russia

    D. V. Zinchenko, V. I. Vladimirov & V. M. Lipkin

Authors
  1. E. Y. Zernii
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  2. D. V. Zinchenko
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  3. V. I. Vladimirov
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  4. I. I. Grigoriev
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  5. E. E. Skorikova
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  6. V. E. Baksheeva
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  7. V. M. Lipkin
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  8. P. P. Philippov
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  9. I. I. Senin
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Correspondence to I. I. Senin.

Additional information

Original Russian Text © E.Y. Zernii, D.V. Zinchenko, V.I. Vladimirov, I.I. Grigoriev, E.E. Skorikova, V.E. Baksheeva, V.M. Lipkin, P.P. Philippov, I.I. Senin, 2013, published in Biologicheskie Membrany, 2013, Vol. 30, No. 5–6, pp. 380–386.

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Zernii, E.Y., Zinchenko, D.V., Vladimirov, V.I. et al. Ca2+-dependent regulatory activity of recoverin in photoreceptor raft structures: The role of caveolin-1. Biochem. Moscow Suppl. Ser. A 8, 44–49 (2014). https://doi.org/10.1134/S1990747813050255

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  • DOI: https://doi.org/10.1134/S1990747813050255

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