Neurocalcin δ modulation of ROS-GC1, a new model of Ca2+ signaling

Biochemistry

Volumn 47, Issue 25, 2008, Pages 6590-6601

  Venkataraman, Venkateswar ^b   Duda, Teresa ^a   Ravichandran, Sarangan ^c   Sharma, Rameshwar K ^a  

^a PENNSYLVANIA COLLEGE OF OPTOMETRY   (United States)

^b UMDNJ School of Osteopathic Medicine   (United States)

^c SAIC FREDERICK INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GUANYLATE CYCLASE (GC); NEW MODEL;

CALCIUM;

MODULATION;

AMINO ACID; CALCIUM CHANNEL; GUANYLATE CYCLASE; NEUROCALCIN;

ALPHA HELIX; ARTICLE; CATALYSIS; DIMERIZATION; GENE MAPPING; PRIORITY JOURNAL;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CALCIUM; CALCIUM SIGNALING; CATALYTIC DOMAIN; CERCOPITHECUS AETHIOPS; COS CELLS; GUANYLATE CYCLASE; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; NEUROCALCIN; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, CELL SURFACE; SURFACE PLASMON RESONANCE; TRANSFECTION;

EID: 45749114507     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi800394s     Document Type: Article

References (55)

1. Paul, A. K. (1986) Doctoral Thesis, University of Tennessee.
2. Paul, A. K., Marala, R. B., Jaiswal, R. K., and Sharma, R. K. (1987) Coexistence of guanylate cyclase and atrial natriuretic factor receptor in a 180-kD protein. Science 235, 1224-1226.
3. Kuno, T., Andersen, J. W., Kamisaki, T., Waldman, S. A., Chang, L. Y., Saheki, S., Leitman, D. C., Nakane, M., and Murad, F. (1986) Co-purification of an atrial natriuretic factor receptor and particulate guanylate cyclase from rat lung. J. Biol. Chem. 261, 5817-5823.
4. Margulis, A., Goraczniak, R., Duda, T., Sharma, R. K., and Sitaramayya, A. (1993) Structural and biochemical identity of retinal rod outer segment membrane guanylate cyclase. Biochem. Biophys. Res. Commun. 194, 855-861.
5. Goraczniak, R., Duda, T., Sitaramayya, A., and Sharma, R. K. (1994) Structural and functional characterization of the rod outer segment membrane guanylate cyclase. Biochem. J. 302, 455-461.
6. Sharma, R. K. (2002) Evolution of the membrane guanylate cyclase transduction system. Mol. Cell. Biochem. 230, 3-30.
7. Pugh, E. N., Jr., Duda, T., Sitaramayya, A., and Sharma, R. K. (1997) Photoreceptor guanylate cyclases: a review. Biosci. Rep. 17, 429-473.
8. Koch, K.-W., Duda, T., and Sharma, R. K. (2002) Photoreceptor specific guanylate cyclases in vertebrate phototransduction. Mol. Cell. Biochem. 230, 97-106.
9. Sharma, R. K., Duda, T., Venkataraman, V., and Koch, K.-W. (2004) Calcium-modulated membrane guanylate cyclase, ROS-GC transduction machinery in sensory neurons: a universal concept. Curr. Top. Biochem. Res. 6, 111-144.
10. Schulz, S., Green, C. K., Yuen, P. S., and Garbers, D. L. (1990) Guanylyl cyclase is a heat-stable enterotoxin receptor. Cell 3, 941-948.
11. Koller, K. J., Lowe, D. G., Bennett, G. L., Minamino, N., Kangawa, K., Matsuo, H., and Goeddel, D. V. (1991) Selective activation of the B natriuretic peptide receptor by C-type natriuretic peptide (CNP). Science 252, 120-123.
12. Duda, T., Goraczniak, R., Sitaramayya, A., and Sharma, R. K. (1993) Cloning and expression of an ATP-regulated human retina C-type natriuretic factor receptor guanylate cyclase. Biochemistry 32, 1391-1395.
13. Koch, K.-W., and Stryer, L. (1988) Highly cooperative feedback control of retinal rod guanylate cyclase by calcium ions. Nature 334, 64-66.
14. Duda, T., Koch, K.-W., Venkataraman, V., Lange, C., Beyermann, M., and Sharma, R. K. (2002) Ca(2+) sensor S100beta-modulated sites of membrane guanylate cyclase in the photoreceptor-bipolar synapse. EMBO J. 21, 2547-2556.
15. Venkataraman, V., Duda, T., Vardi, N., Koch, K.-W., and Sharma, R. K. (2003) Calcium-modulated guanylate cyclase transduction machinery in the photoreceptor-bipolar synaptic region. Biochemistry 42, 5640-5648.
16. Krishnan, A., Venkataraman, V., Fik-Rymarkiewicz, E., Duda, T., and Sharma, R. K. (2004) Structural, biochemical, and functional characterization of the calcium sensor neurocalcin delta in the inner retinal neurons and its linkage with the rod outer segment membrane guanylate cyclase transduction system. Biochemistry 43, 2708-2723.
17. Duda, T., Jankowska, A., Venkataraman, V., Nagele, R. G., and Sharma, R. K. (2001) A novel calcium-regulated membrane guanylate cyclase transduction system in the olfactory neuroepithelium. Biochemistry 40, 12067-12077.
18. Duda, T., Fik-Rymarkiewicz, E., Venkataraman, V., Krishnan, A., and Sharma, R. K. (2004) Calcium-modulated ciliary membrane guanylate cyclase transduction machinery: constitution and operational principles. Mol. Cell. Biochem. 267, 107-122.
19. Duda, T., and Sharma, R. K. (2008) ONE-GC membrane guanylate cyclase, a trimodal odorant signal transducer. Biochem. Biophys. Res. Commun. 367, 440-445.
20. 2+- dependent ROS-GC1 transduction machinery in the gustatory epithelium: a new mechanism in gustatory transduction. FEBS Lett. 577, 393-398.
21. 2+-signaling membrane guanylate cyclase (ROS-GC) transduction pathway in bovine hippocampus. Mol. Cell. Biochem. 291, 187-204.
22. Venkataraman, V., Nagele, R., Duda, T., and Sharma, R. K. (2000) Rod outer segment membrane guanylate cyclase type 1-linked stimulatory and inhibitory calcium signaling systems in the pineal gland: biochemical, molecular, and immunohistochemical evidence. Biochemistry 39, 6042-6052.
23. Jankowska, A., Burczynska, B., Duda, T., Warchol, J. B., and Sharma, R. K. (2007) Calcium-modulated rod outer segment membrane guanylate cyclase type 1 transduction machinery in the testes. J. Androl. 28, 50-58.
24. Gorczyca, W. A., Gray-Keller, M., 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.
25. 2+-binding protein activating photoreceptor guanylyl cyclase. J. Biol. Chem. 270, 25200-25206.
26. Frins, S., Bonigk, W., Muller, F., Kellner, R., and Koch, K.-W. (1996) Functional characterization of a guanylyl cyclase-activating protein from vertebrate rods. Cloning, heterologous expression, and localization. J. Biol. Chem. 271, 8022-8027.
27. Krishnan, A., Goraczniak, R. M., Duda, T., and Sharma, R. K. (1998) Third calcium-modulated rod outer segment membrane guanylate cyclase transduction mechanism. Mol. Cell. Biochem. 178, 251-259.
28. 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.
29. Margulis, A., Pozdnyakov, N., and Sitaramayya, A. (1996) Activation of bovine photoreceptor guanylate cyclase by S100 proteins. Biochem. Biophys. Res. Commun. 218, 243-247.
30. Duda, T., Goraczniak, R., and Sharma, R. K. (1996) Molecular characterization of S100A1-S100B protein in retina and its activation mechanism of bovine photoreceptor guanylate cyclase. Biochemistry 35, 6263-6266.
31. Pozdnyakov, N., Goraczniak, R., Margulis, A., Duda, T., Sharma, R. K., Yoshida, A., and Sitaramayya, A. (1997) Structural and functional characterization of retinal calcium-dependent guanylate cyclase activator protein (CD-GCAP): identity with S100beta protein. Biochemistry 36, 14159-14166.
32. Kumar, V. D., Vijay-Kumar, S., Krishnan, A., Duda, T., and Sharma, R. K. (1999) A second calcium regulator of rod outer segment membrane guanylate cyclase, ROS-GC1: neurocalcin. Biochemistry 38, 12614-12620.
33. 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, 5535-9553.
34. Goraczniak, R., Duda, T., and Sharma, R. K. (1997) Structural and functional characterization of a second subfamily member of the calcium-modulated bovine rod outer segment membrane guanylate cyclase, ROS-GC2. Biochem. Biophys. Res. Commun. 234, 666-670.
35. Fülle, H. J., Vassar, R., Foster, D. C., Yang, R. B., Axel, R., and Garbers, D. L. (1995) A receptor guanylyl cyclase expressed specifically in olfactory sensory neurons. Proc. Natl. Acad. Sci. U.S.A. 92, 3571-3575.
36. 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.
37. 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.
38. Duda, T., Venkataraman, V., Krishnan, A., Nagele, R. G., and Sharma, R. K. (2001) Negatively calcium-modulated membrane guanylate cyclase signaling system in the rat olfactory bulb. Biochemistry 40, 4654-4662.
39. Duda, T., Krishnan, R., and Sharma, R. K. (2006) GCAP1: Antithetical calcium sensor of ROS-GC transduction machinery. Calcium Binding Protein 1, 102-107.
40. Nambi, P., Aiyar, N. V., and Sharma, R. K. (1982) Adrenocorticotropin- dependent particulate guanylate cyclase in rat adrenal and adrenocortical carcinoma: comparison of its properties with soluble guanylate cyclase and its relationship with ACTH-induced steroidogenesis. Arch. Biochem. Biophys. 217, 638-646.
41. Kelley, L. A., MacCallum, R. M., and Sternberg, M. J. (2000) Enhanced genome annotation using structural profiles in the program 3D-PSSM. J. Mol. Biol. 299, 499-520.
42. Gribskov, M., McLachlan, A. D., and Eisenberg, D. (1987) Profile analysis: Detection of distantly related proteins. Proc. Natl. Acad. Sci. U.S.A. 84, 4355-4358.
43. 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.
44. Garbers, D. L. (1992) Guanylyl cyclase receptors and their endocrine, paracrine, and autocrine ligands. Cell 71, 1-4.
45. Duda, T., Goraczniak, R., and Sharma, R. K. (1991) Site-directed mutational analysis of a membrane guanylate cyclase cDNA reveals the atrial natriuretic factor signaling site. Proc. Natl. Acad. Sci. U.S.A. 88, 7882-7886.
46. Wilson, E. M., and Chinkers, M. (1995) Identification of sequences mediating guanylyl cyclase dimerization. Biochemistry 34, 4696-4701.
47. 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.
48. Duda, T., Venkataraman, V., Jankowska, A., Lange, C., Koch, K.-W., and Sharma, R. K. (2000) Impairment of the rod outer segment membrane guanylate cyclase dimerization in a cone-rod dystrophy results in defective calcium signaling. Biochemistry 39, 12522-12533.
49. Vijay-Kumar, S., and Kumar, V. D. (1999) Crystal structure of recombinant bovine neurocalcin. Nat. Struct. Biol. 6, 80-88.
50. 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.
51. Tucker, C. L., Hurley, J. M., Miller, T. M., 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.
52. Tesmer, J. J., Sunahara, R. K., Gilman, A. G., and Sprang, S. R. (1997) Crystal structure of the catalytic domains of adenylyl cyclase in a complex with Gsalpha·GTPgammaS. Science 278, 1907-1916.
53. Sharma, R. K., and Duda, T. (2006) Calcium sensor neurocalcin (5-modulated ROS-GC transduction machinery in the retinal and olfactory neurons. Calcium Binding Proteins 1, 7-11.
54. 2+-modulated machinery: Constitution and operational principles, in Neuronal calcium sensor proteins (Phillippov, P., and Koch, K.-W., Eds.) pp 91-113, Nova Science Publishers, Hauppage, NY.
55. Lange, C., Duda, T., Beyermann, M., Sharma, R. K., and Koch, K.-W. (1999) Regions in vertebrate photoreceptor guanylyl cyclase ROS-GC1 involved in Ca(2+)-dependent regulation by guanylyl cyclase-activating protein GCAP-1. FEBS Lett. 460, 27-31.