Photoreceptor Current and Photoorientation in Chlamydomonas Mediated by 9-Demethylchlamyrhodopsin (original) (raw)

Abstract

Green flagellates possess rhodopsin-like photoreceptors involved in control of their behavior via generation of photocurrents across the plasma membrane. Chlamydomonas mutants blocked in retinal biosynthesis are “blind,” but they can be rescued by the addition of exogenous retinoids. Photosignaling by chlamyrhodopsin regenerated with 9-demethylretinal was investigated by recording photocurrents from single cells and cell suspensions, and by measuring phototactic orientation.

Loading...

Loading Preview

Sorry, preview is currently unavailable. You can download the paper by clicking the button above.

References (56)

  1. Chemerilova, V. I. 1978. Study of pigmentation-modifying mutations of Chlamydomonas reinhardtii strains of different ploidy: II. Compounds for lts1 mutations and their use for obtaining triploid cultures. Sov. Genet. 14:110 -115.
  2. Corson, D. W., M. C. Cornwall, E. F. Macnichol, S. Tsang, F. Derguini, R. K. Crouch, and K. Nakanishi. 1994. Relief of opsin desensitization and prolonged excitation of rod photoreceptors by 9-desmethylretinal. Proc. Natl. Acad. Sci. U.S.A. 91:6958 -6962.
  3. Corson, D. W., and R. Crouch. 1996. Physiological activity of retinoids in natural and artificial visual pigments. Photobiol. 63: 595-600.
  4. Der, A., R. Toth-Boconadi, and L. Keszthelyi. 1997. Electric currents evoked by double-flash excitation of the phototactic alga Chlamydomo- nas reinhardtii. J. Photochem. Photobiol. B: Biol. 38:76 -80.
  5. Feinleib, M. E. H., and G. M. Curry. 1971. The relationship between stimulus intensity and oriented phototactic response (topotaxis) in Chlamydomonas. Physiol. Plant. 25:346 -352.
  6. Foster, K.-W., J. Saranak, F. Derguini, G. Zarrilli, R. Johnson, M. Okabe, and K. Nakanishi. 1989. Activation of Chlamydomonas rhodopsin in vivo does not require isomerization of retinal. Biochemistry. 28: 819 -824.
  7. Foster, K.-W., J. Saranak, N. Patel, G. Zarrilli, M. Okabe, T. Kline, and K. Nakanishi. 1984. A rhodopsin is the functional photoreceptor for pho- totaxis in the unicelullar eukaryote Chlamydomonas. Nature. 311: 756 -759.
  8. Foster, K.-W., and R. D. Smyth. 1980. Light antennas in phototactic algae. Microbiol. Rev. 44:572-630.
  9. Ganter, U. M., E. D. Schmid, D. Perez-Sala, R. R. Rando, and F. Siebert. 1989. Removal of the 9-methyl group of retinal inhibits signal transduc- tion in the visual process: a Fourier transform infrared and biochemical investigation. Biochemistry. 28:5954 -5962.
  10. Ga ¨rtner, W., P. Towner, H. Hopf, and D. Oesterhelt. 1983. Removal of methyl groups from retinal controls the activity of bacteriorhodopsin. Biochemistry. 22:2637-2644.
  11. Govorunova, E. G., I. M. Altschuler, D.-P. Haeder, and O. A. Sinesh- chekov. 2000a. A novel express bioassay for detecting toxic substances in water by recording rhodopsin-mediated photoelectric responses in Chlamydomonas cell suspensions. Photochem. Photobiol. 72:320 -326.
  12. Govorunova, E. G., O. A. Sineshchekov, W. Ga ¨rtner, A. S. Chunaev, and P. Hegemann. 2000b. Photocurrents and phototactic orientation in Chlamydomonas reconstituted with 9-desmethylretinal. Proceedings of the 9th International Conference on Retinal Proteins. Hungarian Acad- emy of Sciences, Szeged, Hungary.
  13. Govorunova, E. G., O. A. Sineshchekov, and P. Hegemann. 1997. Desen- sitization and dark recovery of the photoreceptor current in Chlamydo- monas reinhardtii. Plant Physiol. 115:633-642.
  14. Han, M., M. Groesbeek, T. P. Sakmar, and S. O. Smith. 1997. The C9 methyl group of retinal interacts with glycine-121 in rhodopsin. Proc. Natl. Acad. Sci. U.S.A. 94:13442-13447.
  15. Han, M., M. Groesbeek, S. O. Smith, and T. P. Sakmar. 1998. Role of the C9 methyl group in rhodopsin activation: characterization of mutant opsins with the artificial chromophore 11-cis-9-demethylretinal. Bio- chemistry. 37: 538 -545.
  16. Harris, E. 1989. The Chlamydomonas Source Book: A Comprehensive Guide to Biology and Laboratory Use. Academic Press, San Diego.
  17. Harz, H., and P. Hegemann. 1991. Rhodopsin-regulated calcium currents in Chlamydomonas. Nature. 351:489 -491.
  18. Hegemann, P., W. Ga ¨rtner, and R. Uhl. 1991. All-trans retinal constitutes the functional chromophore in Chlamydomonas rhodopsin. Biophys. J. 60:1477-1489.
  19. Hoff, W. D., K. H. Jung, and J. L. Spudich. 1997. Molecular mechanism of photosignaling by archaeal sensory rhodopsins. Annu. Rev. Biophys. Biomol. Struct. 26:223-258.
  20. Holland, E.-M., H. Harz, R. Uhl, and P. Hegemann. 1997. Control of phobic behavioral responses by rhodopsin-induced photocurrents in Chlamydomonas. Biophys. J. 73:1395-1401.
  21. Iwasa, T., M. Takao, M. Yamada, K. Tsujimoto, and F. Tokunaga. 1984. Properties of on analogue pigment bacteriorhodopsin synthesized with naphtylretinal. Biochemistry. 23:838 -843.
  22. Jin, J., R. K. Crouch, D. W. Corson, B. M. Katz, E. F. McNichol, and M. C. Cornwall. 1993. Noncovalent occupancy of the retinal-binding pocket of opsin diminishes bleaching adaptation of retinal cones. Neuron. 11: 513-522.
  23. Kamiya, R., and G. B. Witman. 1984. Submicromolar levels of calcium control the balance of beating between the two flagella in demem- branated models of Chlamydomonas. J. Cell Biol. 98:97-107.
  24. Lawson, M. A., D. N. Zacks, F. Derguini, K. Nakanishi, and J. L. Spudich. 1991. Retinal analog restoration of photophobic responses in a blind Chlamydomonas reinhardtii mutant. Biophys. J. 60:1490 -1498.
  25. Litvin, F. F., O. A. Sineshchekov, and V. A. Sineshchekov. 1978. Photo- receptor electric potential in the phototaxis of the alga Haematococcus pluvialis. Nature. 271:476 -478.
  26. Lou, J., Q. Tan, E. Karnaukhova, N. Berova, K. Nakanishi, and R. K. Crouch. 2000. Synthetic retinals: convenient probes of rhodopsin and visual transduction process. Methods Enzymol. 315:219 -237.
  27. Meyer, C. K., M. Bohme, A. Ockenfels, W. Ga ¨rtner, K. P. Hofmann, and O. P. Ernst. 2000. Signaling states of rhodopsin: retinal provides a scaffold for activating proton transfer switches. J. Biol. Chem. 275: 19713-19718.
  28. Morel-Laurens, N. 1987. Calcium control of phototactic orientation in Chlamydomonas reinhardtii: sign and strength of response. Photochem. Photobiol. 45:119 -128.
  29. Nakanishi, K., and R. Crouch. 1995. Application of artificial pigments to structure determination and study of photoinduced transformations of retinal proteins. Israel J. Chem. 35:253-272.
  30. Nultsch, W., G. Throm, and I. von Rimscha. 1971. Phototactic investiga- tions in Chlamydomonas reinhardtii in homocontinuous culture. Arch. Mikrobiol. 80:351-369.
  31. Rueffer, U., and W. Nultsch. 1990. Flagella photoresponses of Chlamydo- monas cells held on micropipettes: I. Change in flagellar beat frequency. Cell Motil. Cytoskelet. 15:162-167.
  32. Rueffer, U., and W. Nultsch. 1991. Flagellar photoresponses of Chlamy- domonas cells held on micropipettes: II. Change in flagellar beat pattern. Cell Motil. Cytoskelet. 18:269 -278.
  33. Sakamoto, M., A. Wada, A. Akai, M. Ito, T. Goshima, and T. Takahashi. 1998. Evidence for the archaebacterial-type conformation about the bond between the ␤-ionone ring and the polyene chain of the chro- mophore retinal in chlamyrhodopsin. FEBS Lett. 434:335-338.
  34. Sineshchekov, O. A. 1991a. Photoreception in unicellular flagellates: bio- electric phenomena in phototaxis. In Light in Biology and Medicine. R.D. Douglas, editor. Plenum Press, New York. 523-532.
  35. Sineshchekov, O. A. 1991b. Electrophysiology of photomovements in flagellated algae. In Biophysics of Photoreceptors and Photomovements in Microorganisms. F. Lenci, F. Ghetti, G. Colombetti, D.-P. Haeder, and P.-S. Song, editors. Plenum Press, New York. 191-202.
  36. Sineshchekov, O. A., and E. G. Govorunova. 1999. Rhodopsin-mediated photosensing in green flagellated algae. Trends Plant Sci. 4:58 -63.
  37. Sineshchekov, O. A., and E. G. Govorunova. 2001a. Electrical events in photomovements of green flagellated algae. In Comprehensive Series in Photosciences, Vol. 1: Photomovements. D.-P. Haeder, M. Lebert, and G. Jori, editors. Elsevier, Amsterdam. 245-280.
  38. Sineshchekov, O. A., and E. G. Govorunova. 2001b. Rhodopsin receptors of phototaxis in green flagellated algae. Biochemistry (Moscow). 66: 1609 -1622.
  39. Sineshchekov, O. A., E. G. Govorunova, A. Der, L. Keszthelyi, and W. Nultsch. 1992. Photoelectric responses in phototactic flagellated algae measured in cell suspension. J. Photochem. Photobiol. B: Biol. 13: 119 -134.
  40. Sineshchekov, O. A., E. G. Govorunova, A. Der, L. Keszthelyi, and W. Nultsch. 1994. Photoinduced electric currents in carotenoid-deficient Chlamydomonas mutants reconstituted with retinal and its analogs. Biophys. J. 66:2073-2084.
  41. Sineshchekov, O. A., M. Lebert, and D.-P. Haeder. 2000. Effects of light on gravitaxis and velocity in Chlamydomonas reinardtii. J. Plant Physiol. 157:247-254.
  42. Sineshchekov, O. A., F. F. Litvin, and L. Keszthelyi. 1990. Two compo- nents of photoreceptor potential in phototaxis of the flagellated green alga Haematococcus pluvialis. Biophys. J. 57:33-39.
  43. Spudich, J. L., C. S. Yang, K. H. Jung, and E. N. Spudich. 2000. Retinyli- dene proteins: structures and functions from archaea to humans. Annu. Rev. Cell Dev. Biol. 16:365-392.
  44. Spudich, J. L., D. N. Zacks, and R. A. Bogomolni. 1995. Microbial sensory rhodopsins: photochemistry and function. Israel J. Chem. 35:495-513.
  45. Takahashi, T., M. Kubota, M. Watanabe, K. Yoshihara, F. Derguini, and K. Nakanishi. 1992a. Diversion of the sign of phototaxis in a Chlamydo- monas reinhardtii mutant incorporated with retinal and its analogs. FEBS Lett. 314:275-279.
  46. Takahashi, T., B. Yan, and J. L. Spudich. 1992b. Sensitivity increase in the photophobic response of Halobacterium halobium reconstituted with retinal analogs: a novel interpretation for the fluence-response relation- ship and a kinetic modeling. Photochem. Photobiol. 56:1119 -1128.
  47. Takahashi, T., K. Yoshihara, M. Watanabe, M. Kubota, R. Johnson, F. Derguini, and K. Nakanishi. 1991. Photoisomerization of retinal at 13-ene is important for phototaxis of Chlamydomonas reinhardtii: si- multaneous measurements of phototactic and photophobic responses. Biochem. Biophys. Res. Commun. 178:1273-1279.
  48. Uhl, R., and P. Hegemann. 1990. Adaptation of Chlamydomonas phototaxis: I. A light-scattering apparatus for measuring the phototactic rate of microorganisms with high time resolution. Cell Motil. Cytoskelet. 15:230 -244.
  49. Weidlich, O., B. Schalt, N. Friedman, M. Sheves, J. K. Lanyi, L. S. Brown, and F. Siebert. 1996. Steric interaction between the 9-methyl group of the retinal and tryptophan 182 controls 13-cis to all-trans reisomeriza- tion and proton uptake in the bacteriorhodopsin photocycle. Biochemis- try. 35:10807-10814.
  50. Yamazaki, Y., J. Sasaki, M. Hatanaka, H. Kandori, A. Maeda, R. Needle- man, T. Shinada, K. Yoshihara, L. S. Brown, and J. K. Lanyi. 1995. Interaction of tryptophan-182 with the retinal 9-methyl group in the L intermediate of bacteriorhodopsin. Biochemistry. 34:577-582.
  51. Yan, B., and J. L. Spudich. 1991. Evidence that the repellent receptor form of sensory rhodopsin I is an attractant signalling state. Photochem. Photobiol. 54:1023-1026.
  52. Yan, B., T. Takahashi, R. Johnson, and J. L. Spudich. 1991. Identification of signalling states of a sensory receptor by modulation of lifetimes of stimulus-induced conformations: the case of sensory rhodopsin II. Bio- chemistry. 30:10686 -10692.
  53. Yan, B., A. Xie, G. U. Nienhaus, Y. Katsuta, and J. L. Spudich. 1993. Steric constraints in the retinal binding pocket of sensory rhopdopsin I. Biochemistry. 32:10224 -10232.
  54. Yoshimura, K. 1998. Mechanosensitive channels in the cell body of Chlamydomonas. J. Membr. Biol. 166:149 -155.
  55. Zacks, D. N., F. Derguini, K. Nakanishi, and J. L. Spudich. 1993. Com- parative study of phototactic and photophobic receptor chromophore properties in Chlamydomonas reinhardtii. Biophys. J. 65:508 -518.
  56. Zacks, D. N., and J. L. Spudich. 1994. Gain setting in Chlamydomonas reinhardtii: mechanism of phototaxis and the role of the photophobic response. Cell Motil. Cytoskelet. 29:225-230.