Enzymatic properties and regulation of the native isozymes of retinal membrane guanylyl cyclase (RetGC) from mouse photoreceptors

Biochemistry

Volumn 50, Issue 25, 2011, Pages 5590-5600

  Peshenko, Igor V ^a   Olshevskaya, Elena V ^a   Savchenko, Andrey B ^a   Karan, Sukanya ^b   Palczewski, Krzysztof ^c   Baehr, Wolfgang ^b   Dizhoor, Alexander M ^a  

^a SALUS UNIVERSITY   (United States)

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

^c CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BASAL ACTIVITIES; CATALYTIC CONSTANTS; ENZYMATIC PROPERTIES; GUANYLYL CYCLASE; HIGH RATE; INTRINSIC PROPERTY; MOLAR RATIO; OUTER SEGMENTS; PHYSIOLOGICAL CONCENTRATIONS; SENSOR PROPERTIES; SYNTHESIS RATE;

CALCIUM; CHEMICAL ACTIVATION; GENES; MAMMALS; OPHTHALMOLOGY; PHYSIOLOGY; VISION;

ISOENZYMES;

CALCIUM ION; GUANYLATE CYCLASE; GUANYLATE CYCLASE ACTIVATOR; ISOENZYME; PROTEIN GCAP1; PROTEIN GCAP2; RETINAL MEMBRANE GUANYLYL CYCLASE; RETINAL MEMBRANE GUANYLYL CYCLASE 1; RETINAL MEMBRANE GUANYLYL CYCLASE 2; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; BINDING AFFINITY; CATALYSIS; ENZYME ACTIVATION; ENZYME ANALYSIS; ENZYME REGULATION; EPIRETINAL MEMBRANE; MOUSE; NONHUMAN; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN TARGETING;

ANIMALS; CALCIUM SIGNALING; CATALYSIS; CATTLE; GUANYLATE CYCLASE; GUANYLATE CYCLASE-ACTIVATING PROTEINS; ISOENZYMES; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; PHOTORECEPTOR CELLS, VERTEBRATE; RECEPTORS, CELL SURFACE; ROD CELL OUTER SEGMENT;

BOVINAE; MAMMALIA; MUS;

EID: 79959428038     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi200491b     Document Type: Article

References (62)

1. Fu, Y. and Yau, K. W. (2007) Phototransduction in mouse rods and cones Pflugers Arch. 454, 805-819 (Pubitemid 46976598)
2. Pugh, E. N., Jr., Duda, T., Sitaramayya, A., and Sharma, R. K. (1997) Photoreceptor guanylate cyclases: a review Biosci. Rep. 17, 429-473 (Pubitemid 28005868)
3. Hodgkin, A. L. and Nunn, B. J. (1988) Control of light-sensitive current in salamander rods J. Physiol. 403, 439-471
4. Koch, K. W. and Stryer, L. (1988) Highly cooperative feedback control of retinal rod guanylate cyclase by calcium ions Nature 334, 64-66
5. Gorczyca, W. A., Gray-Keller, M. P., Detwiler, P. B., and Palczewski, K. (1994) Purification and physiological evaluation of a guanylate cyclase activating protein from retinal rods Proc. Natl. Acad. Sci. U.S.A. 91, 4014-4018 (Pubitemid 24139563)
6. Dizhoor, A. M., Lowe, D. G., Olshevskaya, E. V., Laura, R. P., and 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 (Pubitemid 24186801)
7. 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., Detwiller, P. B., and Baehr, W. (1994) Molecular cloning and characterization of retinal photoreceptor guanylyl cyclase-activating protein Neuron 13, 395-404 (Pubitemid 24275096)
8. Lowe, D. G., Dizhoor, A. M., Liu, K., Gu, Q., Spencer, M., Laura, R., Lu, L., and Hurley, J. B. (1995) Cloning and expression of a second photoreceptor-specific membrane retina guanylyl cyclase (RetGC), RetGC-2 Proc. Natl. Acad. Sci. U.S.A. 92, 5535-5539
9. Mendez, A., Burns, M. E., Sokal, I., Dizhoor, A. M., Baehr, W., Palczewski, K., Baylor, D. A., and Chen, J. (2001) Role of guanylate cyclase-activating proteins (GCAPs) in setting the flash sensitivity of rod photoreceptors Proc. Natl. Acad. Sci. U.S.A. 98, 9948-9953 (Pubitemid 32771350)
10. 2+ cation binding cycle of guanylyl cyclase activating proteins (GCAPs): role in regulation of photoreceptor guanylyl cyclase Mol. Cell. Biochem. 334, 117-124
11. 2+ -dependent regulation of phototransduction Photochem. Photobiol. 84, 903-910
12. Burns, M. E., Mendez, A., Chen, J., and Baylor, D. A. (2002) Dynamics of cyclic GMP synthesis in retinal rods Neuron 36, 81-91
13. Howes, K. A., Pennesi, M. E., Sokal, I., Church-Kopish, J., Schmidt, B., Margolis, D., Frederick, J. M., Rieke, F., Palczewski, K., Wu, S. M., Detwiler, P. B., and Baehr, W. (2002) GCAP1 rescues rod photoreceptor response in GCAP1/GCAP2 knockout mice EMBO J. 21, 1545-1554 (Pubitemid 34614611)
14. 2+ and causes photoreceptor degeneration in transgenic mice J. Neurosci. 24, 6078-6085 (Pubitemid 38891098)
15. Pennesi, M. E., Howes, K. A., Baehr, W., and Wu, S. M. (2003) Guanylate cyclase-activating protein (GCAP) 1 rescues cone recovery kinetics in GCAP1/GCAP2 knockout mice Proc. Natl. Acad. Sci. U.S.A. 100, 6783-6788 (Pubitemid 36666657)
16. Makino, C. L., Peshenko, I. V., Wen, X. H., Olshevskaya, E. V., Barrett, R., and Dizhoor, A. M. (2008) A role for GCAP2 in regulating the photoresponse. Guanylyl cyclase activation and rod electrophysiology in GUCA1B knock-out mice J. Biol. Chem. 283, 29135-29143
17. Yang, R. B., Robinson, S. W., Xiong, W. H., Yau, K. W., Birch, D. G., and Garbers, D. L. (1999) Disruption of a retinal guanylyl cyclase gene leads to cone-specific dystrophy and paradoxical rod behavior J. Neurosci. 19, 5889-5897 (Pubitemid 29327924)
18. Baehr, W., Karan, S., Maeda, T., Luo, D. G., Li, S., Bronson, J. D., Watt, C. B., Yau, K. W., Frederick, J. M., and Palczewski, K. (2007) The function of guanylate cyclase 1 and guanylate cyclase 2 in rod and cone photoreceptors J. Biol. Chem. 282, 8837-8847 (Pubitemid 47093526)
19. Imanishi, Y., Li, N., Sokal, I., Sowa, M. E., Lichtarge, O., Wensel, T. G., Saperstein, D. A., Baehr, W., and Palczewski, K. (2002) Characterization of retinal guanylate cyclase-activating protein 3 (GCAP3) from zebrafish to man Eur. J. Neurosci. 15, 63-78 (Pubitemid 35478010)
20. Imanishi, Y., Yang, L., Sokal, I., Filipek, S., Palczewski, K., and Baehr, W. (2004) Diversity of guanylate cyclase-activating proteins (GCAPs) in teleost fish: characterization of three novel GCAPs (GCAP4, GCAP5, GCAP7) from zebrafish (Danio rerio) and prediction of eight GCAPs (GCAP1-8) in pufferfish (Fugu rubripes) J. Mol. Evol. 59, 204-217 (Pubitemid 39128343)
21. Takemoto, N., Tachibanaki, S., and Kawamura, S. (2009) High cGMP synthetic activity in carp cones Proc. Natl. Acad. Sci. U.S.A. 106, 11788-11793
22. 2+)-binding protein activating photoreceptor guanylyl cyclase J. Biol. Chem. 270, 25200-25206
23. Gorczyca, W. A., Polans, A. S., Surgucheva, I. G., Subbaraya, I., Baehr, W., and Palczewski, K. (1995) Guanylyl cyclase activating protein. A calcium-sensitive regulator of phototransduction J. Biol. Chem. 270, 22029-22036
24. 2+ sensors: implications for photoreceptor guanylyl cyclase (RetGC) regulation in mammalian photoreceptors J. Biol. Chem. 279, 16903-16906 (Pubitemid 38560441)
25. Dizhoor, A. M., Boikov, S. G., and Olshevskaya, E. V. (1998) Constitutive activation of photoreceptor guanylate cyclase by Y99C mutant of GCAP-1. Possible role in causing human autosomal dominant cone degeneration J. Biol. Chem. 273, 17311-17314 (Pubitemid 28355054)
26. Sokal, I., Li, N., Surgucheva, I., Warren, M. J., Payne, A. M., Bhattacharya, S. S., Baehr, W., and Palczewski, K. (1998) GCAP1 (Y99C) mutant is constitutively active in autosomal dominant cone dystrophy Mol. Cell 2, 129-133 (Pubitemid 128378974)
27. Woodruff, M. L., Olshevskaya, E. V., Savchenko, A. B., Peshenko, I. V., Barrett, R., Bush, R. A., Sieving, P. A., Fain, G. L., and Dizhoor, A. M. (2007) Constitutive excitation by Gly90Asp rhodopsin rescues rods from degeneration caused by elevated production of cGMP in the dark J. Neurosci. 27, 8805-8815 (Pubitemid 47292752)
28. Yang, R. B., Foster, D. C., Garbers, D. L., and Fulle, H. J. (1995) Two membrane forms of guanylyl cyclase found in the eye Proc. Natl. Acad. Sci. U.S.A. 92, 602-606
29. Duda, T., Goraczniak, R., Surgucheva, I., Rudnicka-Nawrot, M., Gorczyca, W. A., Palczewski, K., Sitaramayya, A., Baehr, W., and Sharma, R. K. (1996) Calcium modulation of bovine photoreceptor guanylate cyclase Biochemistry 35, 8478-8482 (Pubitemid 26240180)
30. Garbers, D. L. (1999) The guanylyl cyclase receptors Methods 19, 477-484 (Pubitemid 30025791)
31. Ramamurthy, V., Tucker, C., Wilkie, S. E., Daggett, V., Hunt, D. M., and Hurley, J. B. (2001) Interactions within the coiled-coil domain of RetGC-1 guanylyl cyclase are optimized for regulation rather than for high affinity J. Biol. Chem. 276, 26218-26229
32. Tucker, C. L., Hurley, J. H., Miller, T. R., and Hurley, J. B. (1998) Two amino acid substitutions convert a guanylyl cyclase, RetGC-1, into an adenylyl cyclase Proc. Natl. Acad. Sci. U.S.A. 95, 5993-5997 (Pubitemid 28248952)
33. Liu, Y., Ruoho, A. E., Rao, V. D., and Hurley, J. H. (1997) Catalytic mechanism of the adenylyl and guanylyl cyclases: modeling and mutational analysis Proc. Natl. Acad. Sci. U.S.A. 94, 13414-13419 (Pubitemid 28009596)
34. Perrault, I., Rozet, J. M., Gerber, S., Ghazi, I., Ducroq, D., Souied, E., Leowski, C., Bonnemaison, M., Dufier, J. L., Munnich, A., and Kaplan, J. (2000) Spectrum of retGC1 mutations in Leber's congenital amaurosis Eur. J. Hum. Genet. 8, 578-582 (Pubitemid 30639363)
35. Perrault, I., Rozet, J. M., Gerber, S., Kelsell, R. E., Souied, E., Cabot, A., Hunt, D. M., Munnich, A., and Kaplan, J. (1998) A retGC-1 mutation in autosomal dominant cone-rod dystrophy Am. J. Hum. Genet. 63, 651-654 (Pubitemid 30418647)
36. 2+-sensitivity Eur. J. Biochem. 270, 3814-3821 (Pubitemid 37123253)
37. Helten, A., Saftel, W., and Koch, K. W. (2007) Expression level and activity profile of membrane bound guanylate cyclase type 2 in rod outer segments J. Neurochem. 103, 1439-46 (Pubitemid 47631833)
38. Aparicio, J. G. and Applebury, M. L. (1995) The bovine photoreceptor outer segment guanylate cyclase: purification, kinetic properties, and molecular size Protein Expression Purif. 6, 501-511
39. Duda, T., Venkataraman, V., Krishnan, A., and Sharma, R. K. (1998) Rod outer segment membrane guanylate cyclase type 1 (ROS-GC1) gene: structure, organization and regulation by phorbol ester, a protein kinase C activator Mol. Cell. Biochem. 189, 63-70 (Pubitemid 28556549)
40. 2+-free guanylyl cyclase activating proteins (GCAPs) and recombinant photoreceptor guanylyl cyclase 1 (RetGC-1) Biochemistry 43, 13796-13804 (Pubitemid 39431063)
41. Nickell, S., Park, P. S., Baumeister, W., and Palczewski, K. (2007) Three-dimensional architecture of murine rod outer segments determined by cryoelectron tomography J. Cell Biol. 177, 917-925 (Pubitemid 46873096)
42. Liang, Y., Fotiadis, D., Maeda, T., Maeda, A., Modzelewska, A., Filipek, S., Saperstein, D. A., Engel, A., and Palczewski, K. (2004) Rhodopsin signaling and organization in heterozygote rhodopsin knockout mice J. Biol. Chem. 279, 48189-48196 (Pubitemid 39540974)
43. Olshevskaya, E. V., Hughes, R. E., Hurley, J. B., and Dizhoor, A. M. (1997) Calcium binding, but not a calcium-myristoyl switch, controls the ability of guanylyl cyclase-activating protein GCAP-2 to regulate photoreceptor guanylyl cyclase J. Biol. Chem. 272, 14327-14333 (Pubitemid 27232847)
44. 2+ exchange in EF-hand domains J. Biol. Chem. 282, 21645-21652 (Pubitemid 47195776)
45. Laura, R. P. and Hurley, J. B. (1998) The kinase homology domain of retinal guanylyl cyclases 1 and 2 specifies the affinity and cooperativity of interaction with guanylyl cyclase activating protein-2 Biochemistry 37, 11264-11271 (Pubitemid 28394875)
46. 2+ with quin2 Methods Enzymol. 172, 230-262 (Pubitemid 19170355)
47. 2+-bound form is the physiological activator of photoreceptor guanylyl cyclase J. Biol. Chem. 281, 23830-23841 (Pubitemid 44274159)
48. Haeseleer, F., Sokal, I., Li, N., Pettenati, M., Rao, N., Bronson, D., Wechter, R., Baehr, W., and Palczewski, K. (1999) Molecular characterization of a third member of the guanylyl cyclase-activating protein subfamily J. Biol. Chem. 274, 6526-6535 (Pubitemid 29111069)
49. 2+, and myristoylation on guanylyl cyclase activating protein 1 structure and stability Biochemistry 48, 850-862
50. Chen, C., Nakatani, K., and Koutalos, Y. (2003) Free magnesium concentration in salamander photoreceptor outer segments J Physiol. 553, 125-135 (Pubitemid 37483921)
51. Gray-Keller, M. P. and Detwiler, P. B. (1994) The calcium feedback signal in the phototransduction cascade of vertebrate rods Neuron 13, 849-861 (Pubitemid 24347298)
52. Woodruff, M. L., Sampath, A. P., Matthews, H. R., Krasnoperova, N. V., Lem, J., and Fain, G. L. (2002) Measurement of cytoplasmic calcium concentration in the rods of wild-type and transducin knock-out mice J. Physiol. 542, 843-854 (Pubitemid 34947277)
53. Tucker, C. L., Laura, R. P., and Hurley, J. B. (1997) Domain-specific stabilization of photoreceptor membrane guanylyl cyclase by adenine nucleotides and guanylyl cyclase activating proteins (GCAPs) Biochemistry 36, 11995-12000 (Pubitemid 27424129)
54. Yang, R. B. and Garbers, D. L. (1997) Two eye guanylyl cyclases are expressed in the same photoreceptor cells and form homomers in preference to heteromers J. Biol. Chem. 272, 13738-13742 (Pubitemid 27224810)
55. Jeon, C. J., Strettoi, E., and Masland, R. H. (1998) The major cell populations of the mouse retina J. Neurosci. 18, 8936-8946 (Pubitemid 28491758)
56. Daniele, L. L., Lillo, C., Lyubarsky, A. L., Nikonov, S. S., Philp, N., Mears, A. J., Swaroop, A., Williams, D. S., and Pugh, E. N., Jr. (2005) Cone-like morphological, molecular, and electrophysiological features of the photoreceptors of the Nrl knockout mouse Invest. Ophthalmol. Vis. Sci. 46, 2156-2167
57. Biernbaum, M. S. and Bownds, M. D. (1985) Light-induced changes in GTP and ATP in frog rod photoreceptors. Comparison with recovery of dark current and light sensitivity during dark adaptation J. Gen. Physiol. 85, 107-121 (Pubitemid 15197554)
58. Okawa, H., Sampath, A. P., Laughlin, S. B., and Fain, G. L. (2008) ATP consumption by mammalian rod photoreceptors in darkness and in light Curr. Biol. 18, 1917-1921
59. Gray-Keller, M. P. and Detwiler, P. B. (1994) The calcium feedback signal in the phototransduction cascade of vertebrate rods Neuron 13, 849-861 (Pubitemid 24347298)
60. Woodruff, M. L., Sampath, A. P., Matthews, H. R., Krasnoperova, N. V., Lem, J., and Fain, G. L. (2002) Measurement of cytoplasmic calcium concentration in the rods of wild-type and transducin knock-out mice J. Physiol. 542, 843-854 (Pubitemid 34947277)
61. Peshenko, I. V., Olshevskaya, E. V., Yao, S., Ezzeldin, H. H., Pittler, S. J., and Dizhoor, A. M. (2010) Activation of retinal guanylyl cyclase RetGC1 by GCAP1: stoichiometry of binding and effect of new LCA-related mutations Biochemistry 49, 709-717
62. Duda, T., Fik-Rymarkiewicz, E., Venkataraman, V., Krishnan, R., Koch, K. W., and Sharma, R. K. (2005) The calcium-sensor guanylate cyclase activating protein type 2 specific site in rod outer segment membrane guanylate cyclase type 1 Biochemistry 44, 7336-7345 (Pubitemid 40656676)