Guanylate-cyclase-inhibitory protein is a frog retinal Ca2+-binding protein related to mammalian guanylate-cyclase-activating proteins

European Journal of Biochemistry

Volumn 252, Issue 3, 1998, Pages 591-599

  Li, Ning ^a,b   Fariss, Robert N ^c   Zhang, Kai ^a,b   Otto Bruc, Annie ^c   Haeseleer, Françoise ^c   Bronson, Darin ^a   Qin, Ning ^b   Yamazaki, Akio ^d   Subbaraya, Iswari ^b   Milam, Ann H ^c   Palczewski, Krzysztof ^c,e   Baehr, Wolfgang ^a  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

^d WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

Calcium binding protein; Frog retina; Guanylate cyclase activating protein; Photoreceptor

Indexed keywords

CALCIUM BINDING PROTEIN; CALCIUM ION; GUANYLATE CYCLASE; GUANYLATE CYCLASE INHIBITOR;

ANIMAL TISSUE; ARTICLE; ENZYME INHIBITION; FROG; NONHUMAN; NUCLEOTIDE SEQUENCE; PHOTORECEPTOR; PRIORITY JOURNAL; RETINA; RETINA CONE;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CALCIUM-BINDING PROTEINS; CATTLE; CLONING, MOLECULAR; DNA PRIMERS; GENE LIBRARY; GUANYLATE CYCLASE-ACTIVATING PROTEINS; MAMMALS; MOLECULAR SEQUENCE DATA; PHOTORECEPTORS; PROTEIN STRUCTURE, SECONDARY; RANA PIPIENS; RECOMBINANT PROTEINS; RETINA; ROD OUTER SEGMENTS; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID;

ANIMALIA; ANURA; MAMMALIA; VERTEBRATA;

EID: 6844260531     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1432-1327.1998.2520591.x     Document Type: Article

References (40)

1. Falke, J. J., Drake, S. K., Hazard, A. L. & Peerson, O. B. (1994) Molecular tuning of ion binding to calcium signaling proteins, Q. Rev. Biophys. 27, 219-290.
2. Celio, M. R. (1996) Guidebook in the calcium-binding proteins, Oxford Academic Press, Oxford.
3. 2+-binding proteins in the retina, Trends Neurosci. 19, 547-554.
4. Yau, K.-W. (1991) Calcium and light adaptation in retinal photoreceptors, Curr. Opin. Neurobiol. 1, 252-257.
5. Lagnado, L. & Baylor, D. (1992) Signal flow in visual transduction, Neuron 8, 995-1002.
6. Koutalos, Y. & Yau, K. W. (1996) Regulation of sensitivity in vertebrate rod photoreceptors by calcium, Trends Neurosci. 19, 73-81.
7. Hsu, Y.-T. & Molday, R. S. (1993) Modulation of the cGMP-gated channel of rod photoreceptor cells by calmodulin, Nature 361, 76-79.
8. Porter, J. A., Yu, M., Doberstein, S. K., Pollard, T. D. & Montell, C. (1993) Dependence of calmodulin localization in the retina on the NINAC unconventional myosin, Science 262, 1038-1042.
9. Dizhoor, A. M., Ray, S., Kumar, S., Niemi, G., Spencer, M., Brolley, D., Walsh, K. A., Philipov, P. P., Hurley, J. B. & Stryer, L. (1991) Recoverin: a calcium sensitive activator of retinal rod guanylate cyclase, Science 251, 915-918.
10. Gorczyca, W. A., Gray-Keller, M. P., Detwiler, P. B. & Palczewski, K. (1994) Purification and physiological evaluation of a guanylate cyclase activating protein from retinal rods, Proc. Natl Acad. Sci. USA 91, 4014-4018.
11. Palczewski, K., Subbaraya, I., Gorczyca, W. A., Helekar, B. S., Ruiz, C. C. Ohguro, H., Huang, J., Zhao, X., Crabb, J. W., Johnson, R. S., Walsh, K. A., Gray-Keller, M. P., Detwiler, P. B. & Baehr, W. (1994) Molecular cloning and characterization of retinal photoreceptor guanylyl cyclase activating protein (GCAP), Neuron 13, 395-404.
12. Subbaraya, I., Ruiz, C. C., Helekar, B. S., Zhao, X., Gorczyca, W. A., Pettenati, M. J., Rao, P. N., Palczewski, K. & Baehr, W. (1994) Molecular characterization of human and mouse photoreceptor guanylate cyclase activating protein (GCAP) and chromosomal localization of the human gene, J. Biol. Chem. 269, 31080-31089.
13. Dizhoor, A. M., Lowe, D. G., Olshevskaya, E. V., Laura, R. P. & Hurley, J. B. (1994) The human photoreceptor membrane guanylyl cyclase, RetGC, is present in outer segments and is regulated by calcium and a soluble activator, Neuron 12, 1345-1352.
14. Gorczyca, W. A., Polans, A. S., Surgucheva, I., Subbaraya, I., Baehr, W. & Palczewski, K. (1995) Guanylyl cyclase activating protein: a calcium-sensitive regulator of phototransduction, J. Biol. Chem. 270, 22029-22036.
15. Chen, T. Y., Peng, Y. W., Dhallan, R. S., Ahamed, B., Reed, R. R. & Yau, K.-W. (1994) A new subunit of the cyclic nucleotide-gated cation channel in retinal rods, Nature 362, 764-767.
16. Koerschen, H. G., Illing, M., Seifert, R., Sesti, F, Williams, A., Gotzes, S., Colville, C., Mueller, F., Dose, A., Godde, M., Molday, L., Kaupp, U. B. & Molday, R. S. (1995) A 240 kDa protein represents the complete beta subunit of the cyclic nucleotide-gated channel from rod photoreceptor, Neuron 15, 627-636.
17. Kawamura, S. & Murakami, M. (1991) Calcium-dependent regulation of cyclic GMP phosphodiesterase by a protein from frog retinal rods, Nature 349, 420-423.
18. Kawamura, S., Hisatomi, O., Kayada, S., Tokunaga, F. & Kuo, C.-H. (1993) Recoverin has S-modulin activity in frog rods, J. Biol. Chem. 268, 14579-14582.
19. Kawamura, S., Kuwata, O., Yamada, M., Matsuda, S., Hisatomi, O. & Tokunaga, F. (1996) Photoreceptor protein s26, a cone homologue of S-modulin in frog retina, J. Biol. Chem. 271, 21 359-21 364.
20. Duda, T., Goraczniak, R., Surgucheva, I., Rudnicka-Nawrot, M., Palczewski, K., Sitaramayya, A., Baehr, W. & Sharma, R. K. (1996) Calcium modulation of bovine photoreceptor guanylate cyclase, Biochemistry 35, 8478-8482.
21. Laura, R. P., Dizhoor, A. M. & Hurley, J. B. (1996) The membrane guanylyl cyclase, retinal guanylyl cyclase-1, is activated through its intracellular domain, J. Biol. Chem. 271, 11 646-11 651.
22. Frins, S., Boenigk, W., Mueller, F., Kellner, R. & Koch, K.-W. (1996) Functional characterization of a guanylyl cyclase-activating protein from vertebrate rods, J Biol. Chem. 271, 8022-8027.
23. Otto-Bruc, A., Fariss, R. N., Haeseleer, F., Huang, J., Buczylko, J., Surgucheva, I., Baehr, W., Milam, A. H. & Palczewski, K. (1997) Localization of guanylate cyclase activating protein 2 in mammalian retinas, Proc. Natl Acad. Sci. USA 94, 4727-4732.
24. Howes, K. A., Bronson, J. D., Dang, Y. L., Li, N., Zhang, K., Ruiz, C. C., Helekar, B. S., Lee, M., Subbaraya, I., Kolb, H., Chen, J. & Baehr, W. (1998) Gene array and expression of mouse retina guanylate cyclase activating proteins 1 and 2 (GCAP1 and GCAP2), Invest. Ophthalmol. & Vis. Sci., in the press.
25. Surguchov, A., Bronson, J. D., Banerjee, P., Knowles, J. A., Ruiz, C. C., Subbaraya, I., Palczewski, K. & Baehr, W. (1997) The human GCAP1 and GCAP2 genes are arranged in a tail-to-tail array on the short arm of chromosome 6 (p21.1), Genomics 39, 312-322.
26. Baehr, W., Falk, J. D., Bugra, K., Triantafyllos, J. T. & McGinnis, J. F. (1988) Isolation and analysis of the mouse opsin gene, FEBS Lett. 238, 253-256.
27. Campbell, A. M. (1984) Monoclonal antibody technology, Elsevier, Amsterdam.
28. Yamazaki, A., Hayashi, F., Tatsumi, M., Bitensky, M. W. & George, J. S. (1990) Interactions between the subunits of transducin and cyclic GMP phosphodiesterase in Rana catesbiana rod photoreceptors, J. Biol. Chem. 265, 11 539-11 548.
29. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4, Nature 227, 680-685.
30. Burnette, W. N. (1981) Western blotting: electrophoretic transfer of proteins from sodium dodecyl sulfate-polyacrylamide gels to unmodified nitrocellulose and radiographic detection with antibody and radioiodinated protein A, Anal. Biochem. 112, 195-203.
31. Qin, N. & Baehr, W. (1994) Expression and mutagenesis of mouse rod photoreceptor cGMP phosphodiesterase, J. Biol. Chem. 269, 3265-3271.
32. Hayashi, F. & Yamazaki, A. (1991) Polymorphism in purified guanylate cyclase from vertebrate rod photoreceptors, Proc. Natl Acad. Sci. USA 88, 4746-4750.
33. Hale, I. L. & Matsumoto, B. (1993) Resolution of subcellular detail in thick tissue sections: immunohistochemical preparation and fluorescence confocal microscopy, Methods Cell Biol. 38, 289-324.
34. Otto-Bruc, A., Buczylko, J., Surgucheva, I., Subbaraya, I., Rudnicka-Nawrot, M., Crabb, J., Arendt, A., Hargrave, P. A., Baehr, W. & Palczewski, K. (1997) Functional reconstitution of photoreceptor guanylate cyclase with native and mutant forms of guanylate cyclase activating protein 1, Biochemistry 36, 4295-4302.
35. Rudnicka-Nawrot, M., Surgucheva, I., Hulmes, J. D., Haeseleer, F., Sokal, I., Crabb, J. W., Baehr, W. & Palczewski, K. (1997) Changes in biological activity and folding of guanylate cyclase activating protein 1 as a function of calcium, Biochemistry 37, 248-257.
36. Liu, X., Seno, K., Nishizawa, Y., Hayashi, F., Yamazaki, A., Matsumoto, H., Wakabayashi, T. & Usukura, J. (1994) Ultrastructural localization of retinal guanylate cyclase in human and monkey retina, Exp. Eye Res. 59, 761-768.
37. Cooper, N., Liu, L., Yoshida, A., Pozdnyakov, N., Margulis, A. & Sitaramayya, A. (1995) The bovine rod outer segment guanylate cyclase, ROS-GC, is present in both outer segment and synaptic layers of the retina, J. Mol. Neurosci. 6, 211-222.
38. 2+-induced 'activator-to-inhibitor' transition, J. Biol. Chem. 271, 19 346-19 350.
39. Murakami, A., Yajima, T. & Inana, G. (1992) Isolation of human retinal genes: recoverin cDNA and gene, Biochem. Biophys. Res. Commun. 187, 234-244.
40. Engelkamp, D., Schafer, B. W., Mattei, M. G., Erne, P. & Heizmann, C. W. (1993) Six S100 genes are clustered on human chromosome 1q21: identification of two genes coding for the two previously unreported calcium-binding proteins S100D and S100E, Proc. Natl Acad. Sci. USA 90, 6547-6551.