Свободная и связанная фракция cGMP в наружном сегменте фоторецепторов позвоночных


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Аннотация

Каскад фототрансдукции в фоторецепторах сетчатки позвоночных использует в качестве вторичного мессенджера циклический гуанозинмонофосфат (cGMP). Уровень cGMP управляет проводимостью каналов плазматической мембраны клетки, поэтому скорость, с которой меняется уровень cGMP, является критической для быстродействия фоторецептора. Существует кажущееся противоречие между высокой общей концентрацией cGMP в наружных сегментах и экспериментально измеренной высокой скоростью обмена cGMP. Противоречие может быть разрешено, если предположить, что большая часть cGMP находится в связанном состоянии, а динамическая фракция составляет незначительную долю от общего cGMP, но именно она изменяется под действием света и управляет проводимостью каналов. В настоящем обзоре мы разбираем доказательства разделения общего пула cGMP на связанную и свободную фракцию, вероятные сайты связывания cGMP и возможное функциональное значение существования двух фракций.

Об авторах

М. Л. Фирсов

Институт эволюционной физиологии и биохимии им. И.М. Сеченова РАН

Email: Michael.Firsov@gmail.com
194223, Санкт-Петербург, пр-т Тореза, д. 44, Россия

Список литературы

  1. Ames A. 3rd, Barad M. Metabolic flux of cyclic GMP and phototransduction in rabbit retina. J Physiol. 1988. V. 406. P. 163-179. https://doi.org/10.1113/jphysiol.1988.sp017374
  2. Arshavsky V.Y., Dumke C.L., Bownds M.D. Noncatalytic cGMP-binding sites of amphibian rod cGMP phosphodiesterase control interaction with its inhibitory gamma-subunits. A putative regulatory mechanism of the rod photoresponse. J.Biol.Chem. 1992. V. 267. P. 24501-24507. https://doi.org/10.1016/S0021-9258(18)35793-4
  3. Arshavsky V.Y., Lamb T.D., Pugh E.N.Jr. G proteins and phototransduction. Annu Rev Physiol. 2002. V. 64. P. 153-187. https://doi.org/10.1146/annurev.physiol.64.082701.102229
  4. Astakhova L., Firsov M., Govardovskii V. Activation and quenching of the phototransduction cascade in retinal cones as inferred from electrophysiology and mathematical modeling. Mol.Vis. 2015. V. 21. P. 244-263.
  5. Berger S.J., DeVries G.W., Carter J.G., Schulz D.W., Passonneau P.N., Lowry O.H., Ferrendelli J.A. The distribution of the components of the cyclic GMP cycle in retina. The Journal of biological chemistry. 1980. V. 255. P. 3128-3133. https://doi.org/10.1016/S0021-9258(19)85861-1
  6. Cobbs W., Pugh E.Jr. Cyclic GMP can increase rod outer-segment light-sensitive current 10-fold without delay of excitation. Nature. 1985. V. 313. P. 585-587. https://doi.org/10.1038/313585a0
  7. Cohen A.I., Blazynski C. Light-induced losses and dark recovery rates of guanosine 3’,5’-cyclic monophosphate in rod outer segments of intact amphibian photoreceptors. J Gen Physiol. 1988. V. 92. P. 731-746. https://doi.org/10.1085/jgp.92.6.731
  8. Cote R.H. Photoreceptor phosphodiesterase (PDE6): activation and inactivation mechanisms during visual transduction in rods and cones. Pflugers Archiv : European journal of physiology. 2021. V. 473. P. 1377-1391. https://doi.org/10.1007/s00424-021-02562-x
  9. Cote R.H., Gupta R., Irwin M.J., Wang X. Photoreceptor phosphodiesterase (PDE6): structure, regulatory mechanisms, and implications for treatment of retinal diseases. Protein Reviews. 2021. V. 22. P. 33-59.
  10. Cote R.H., Gupta R., Irwin M.J., Wang X. Photoreceptor Phosphodiesterase (PDE6): Structure, Regulatory Mechanisms, and Implications for Treatment of Retinal Diseases. Advances in experimental medicine and biology. 2022. V. 1371. P. 33-59. https://doi.org/10.1007/5584_2021_649
  11. Dumke C.L., Arshavsky V.Y., Calvert P.D., Bownds M.D., Pugh E.N.Jr. Rod outer segment structure influences the apparent kinetic parameters of cyclic GMP phosphodiesterase. J Gen Physiol. 1994. V. 103. P. 1071-1098. https://doi.org/10.1085/jgp.103.6.1071
  12. Ferrendelli J.A., Cohen A.I. The effects of light and dark adaptation on the levels of cyclic nucleotides in retinas of mice heterozygous for a gene for photoreceptor dystrophy. Biochem Biophys Res Commun. 1976. V. 73. P. 421-427. https://doi.org/10.1016/0006-291X(76)90724-5
  13. Fesenko E.E., Kolesnikov S.S., Lyubarsky A.L. Induction by cyclic GMP of cationic conductance in plasma membrane of retinal rod outer segment. Nature. 1985. V. 313. P. 310-313. https://doi.org/10.1038/313310a0
  14. Fletcher R.T., Chader G.J. Cyclic GMP: control of concentration by light in retinal photoreceptors. Biochem Biophys Res Commun. 1976. V. 70. P. 1297-1302. https://doi.org/10.1016/0006-291X(76)91043-3
  15. Fu Y. Phototransduction in rods and cones. Webvision: The Organization of the Retina and Visual System. University of Utah Health Sciences Center, Salt Lake City. 2011. Available at: https://europepmc.org/article/nbk/nbk52768#__NBK52768_dtls__
  16. Giusto N.M., Pasquare S.J., Salvador G.A., Ilincheta de Boschero M.G. Lipid second messengers and related enzymes in vertebrate rod outer segments. J Lipid Res. 2010. V. 51. P. 685-700.
  17. Goridis C., Virmaux N., Cailla H.L., Delaage M.A. Rapid, light-induced changes of retinal cyclic GMP levels. FEBS letters. 1974. V. 49. P. 167-169.
  18. Govardovskii V.I., Berman A.L. Light-induced changes of cyclic GMP content in frog retinal rod outer segments measured with rapid freezing and microdissection. Biophys Struct Mech. 1981. V. 7. P. 125-130. https://doi.org/10.1007/BF00539194
  19. Gupta R., Liu Y., Wang H., Nordyke C.T., Puterbaugh R.Z., Cui W., Varga K., Chu F., Ke H., Vashisth H., Cote R.H. Structural Analysis of the Regulatory GAF Domains of cGMP Phosphodiesterase Elucidates the Allosteric Communication Pathway. J Mol Biol. 2020. V. 432. P. 5765-5783. https://doi.org/10.1016/j.jmb.2020.08.026
  20. Hebert M.C., Schwede F., Jastorff B., Cote R.H. Structural features of the noncatalytic cGMP binding sites of frog photoreceptor phosphodiesterase using cGMP analogs. The Journal of biological chemistry. 1998. V. 273. P. 5557-5565. https://doi.org/10.1074/jbc.273.10.5557
  21. Huang D., Hinds T.R., Martinez S.E., Doneanu C., Beavo J.A. Molecular determinants of cGMP binding to chicken cone photoreceptor phosphodiesterase. The Journal of biological chemistry. 2004. V. 279. P. 48143-48151. https://doi.org/10.1074/jbc.M404338200
  22. Hubbell W.L., Bownds M.D. Visual transduction in vertebrate photoreceptors. Annu Rev Neurosci. 1979. V. 2. P. 17-34.
  23. Kaupp U.B., Koch K.W. Role of cGMP and Ca2+ in vertebrate photoreceptor excitation and adaptation. Annu.Rev.Physiol. 1992a. V. 54. P. 153-175.
  24. Kaupp U.B., Koch K.W. Role of cGMP and Ca2+ in vertebrate photoreceptor excitation and adaptation. Annu Rev Physiol. 1992b. V. 54. P. 153-175.
  25. Krishna G., Krishnan N., Fletcher R.T., Chader G. Effects of light on cyclic GMP metabolism in retinal photoreceptors. J Neurochem. 1976. V. 27. P. 717-722. https://doi.org/10.1111/j.1471-4159.1976.tb10399.x
  26. Lamb T.D. Photoreceptor physiology and evolution: cellular and molecular basis of rod and cone phototransduction. J Physiol. 2022. V. 600. P. 4585-4601. https://doi.org/10.1113/JP282058
  27. Martinez S.E., Heikaus C.C., Klevit R.E., Beavo J.A. The structure of the GAF A domain from phosphodiesterase 6C reveals determinants of cGMP binding, a conserved binding surface, and a large cGMP-dependent conformational change. The Journal of biological chemistry. 2008. V. 283. P. 25913-25919. https://doi.org/10.1074/jbc.M802891200
  28. Miller W.H., Nicol G.D. Evidence that cyclic GMP regulates membrane potential in rod photoreceptors. Nature. 1979. V. 280. P. 64-66. https://doi.org/10.1038/280064a0
  29. Mou H., Cote R.H. The catalytic and GAF domains of the rod cGMP phosphodiesterase (PDE6) heterodimer are regulated by distinct regions of its inhibitory γ subunit. Journal of Biological Chemistry. 2001. V. 276. P. 27527-27534. https://doi.org/10.1074/jbc.M103316200
  30. Muradov H., Boyd K.K., Artemyev N.O. Structural determinants of the PDE6 GAF A domain for binding the inhibitory γ-subunit and noncatalytic cGMP. Vision research. 2004. V. 44. P. 2437-2444. https://doi.org/10.1016/j.visres.2004.05.013
  31. Newton A.C., Bootman M.D., Scott J.D. Second Messengers. Cold Spring Harb Perspect Biol. 2016. V. 8. Article a005926.
  32. Nickell S., Park P.S., Baumeister W., Palczewski K. Three-dimensional architecture of murine rod outer segments determined by cryoelectron tomography. J.Cell Biol. 2007. V. 177(5). P. 917-925. https://doi.org/10.1083/jcb.200612010
  33. Orr H.T., Lowry O.H., Cohen A.I., Ferrendelli J.A. Distribution of 3’:5’-cyclic AMP and 3’:5’-cyclic GMP in rabbit retina in vivo: selective effects of dark and light adaptation and ischemia. Proceedings of the National Academy of Sciences of the United States of America. 1976. V. 73. P. 4442-4445. https://doi.org/10.1073/pnas.73.12.4442
  34. Peet J.A., Bragin A., Calvert P.D., Nikonov S.S., Mani S., Zhao X., Besharse J.C., Pierce E.A., Knox B.E., Pugh E.N.Jr. Quantification of the cytoplasmic spaces of living cells with EGFP reveals arrestin-EGFP to be in disequilibrium in dark adapted rod photoreceptors. J.Cell Sci. 2004. V. 117. P. 3049-3059. https://doi.org/10.1242/jcs.01167
  35. Pentia D.C., Hosier S., Cote R.H. The glutamic acid-rich protein-2 (GARP2) is a high affinity rod photoreceptor phosphodiesterase (PDE6)-binding protein that modulates its catalytic properties. Journal of Biological Chemistry. 2006. V. 281. P. 5500-5505. https://doi.org/10.1074/jbc.M507488200
  36. Russwurm M., Koesling D. Measurement of cGMP-generating and-degrading activities and cGMP levels in cells and tissues: Focus on FRET-based cGMP indicators. Nitric Oxide. 2018. V. 77. P. 44-52. https://doi.org/10.1016/j.niox.2018.04.006
  37. Skiba N.P., Lewis T.R., Spencer W.J., Castillo C.M., Shevchenko A., Arshavsky V.Y. Absolute Quantification of Photoreceptor Outer Segment Proteins. Journal of proteome research. 2023. V. 22. P. 2703-2713. https://doi.org/10.1021/acs.jproteome.3c00267
  38. Woodruff M.L., Bownds M.D. Amplitude, kinetics, and reversibility of a light-induced decrease in guanosine 3’,5’-cyclic monophosphate in frog photoreceptor membranes. J Gen Physiol. 1979. V. 73. P. 629-653. https://doi.org/10.1085/jgp.73.5.629
  39. Yamazaki A., Bartucca F., Ting A., Bitensky M.W. Reciprocal effects of an inhibitory factor on catalytic activity and noncatalytic cGMP binding sites of rod phosphodiesterase. Proc.Natl.Acad.Sci.U.S.A. 1982. V. 79(12). P. 3702-3706. https://doi.org/10.1073/pnas.79.12.3702
  40. Yamazaki A., Sen I., Bitensky M.W., Casnellie J.E., Greengard P. Cyclic GMP-specific, high affinity, noncatalytic binding sites on light-activated phosphodiesterase. J.Biol.Chem. 1980. V. 255. P. 11619-11624. https://doi.org/10.1016/S0021-9258(19)70334-2
  41. Yau K.W., Nakatani K. Light-suppressible, cyclic GMP-sensitive conductance in the plasma membrane of a truncated rod outer segment. Nature. 1985. V. 317. P. 252-255. https://doi.org/10.1038/317252a0
  42. Zhang X.-J., Cahill K.B., Elfenbein A., Arshavsky V.Y., Cote R.H. Direct allosteric regulation between the GAF domain and catalytic domain of photoreceptor phosphodiesterase PDE6. Journal of Biological Chemistry. 2008. V. 283. P. 29699-29705. https://doi.org/10.1074/jbc.M803948200
  43. Zhang X.-J., Gao X.-Z., Yao W., Cote R.H. Functional mapping of interacting regions of the photoreceptor phosphodiesterase (PDE6) γ-subunit with PDE6 catalytic dimer, transducin, and Regulator of G-protein Signaling9–1 (RGS9–1). Journal of Biological Chemistry. 2012. V. 287. P. 26312-26320. https://doi.org/10.1074/jbc.M112.377333

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