Hippocalcin, new Ca2+ sensor of a ROS-GC subfamily member, ONE-GC, membrane guanylate cyclase transduction system

Molecular and Cellular Biochemistry

Volumn 325, Issue 1-2, 2009, Pages 1-14

  Krishnan, Anuradha ^a   Duda, Teresa ^b   Pertzev, Alexandre ^b   Kobayashi, Masaaki ^c   Takamatsu, Ken ^c   Sharma, Rameshwar K ^b  

^a UMDNJ School of Osteopathic Medicine   (United States)

^b SALUS UNIVERSITY   (United States)

^c TOHO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Calcium; Calcium binding proteins; Hippocalcin; Hippocampus; Membrane guanylate cyclase; Olfactory neuroepithelium; Signal transduction

Indexed keywords

CALCIUM ION; GUANYLATE CYCLASE; HIPPOCALCIN; NEURONAL CALCIUM SENSOR; OLFACTORY NEUROEPITHELIAL MEMBRANE GUANYLATE CYCLASE; ROD OUTER SEGMENT MEMBRANE GUANYLATE CYCLASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM SIGNALING; CONTROLLED STUDY; HIPPOCAMPUS; MOLECULAR CLONING; MOLECULAR EVOLUTION; NEUROEPITHELIUM; NONHUMAN; NUCLEOTIDE SEQUENCE; OLFACTORY RECEPTOR; PROTEIN DETERMINATION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; SENSORY NERVE CELL; SEQUENCE ANALYSIS;

AMINO ACID SEQUENCE; ANIMALS; CATTLE; CHROMATOGRAPHY, GEL; CLONING, MOLECULAR; DNA, COMPLEMENTARY; ELECTROPHORESIS, POLYACRYLAMIDE GEL; GUANYLATE CYCLASE; HIPPOCALCIN; HIPPOCAMPUS; MOLECULAR SEQUENCE DATA; RECOMBINANT PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION;

BOVINAE;

EID: 58349094156     PISSN: 03008177     EISSN: 15734919     Source Type: Journal    
DOI: 10.1007/s11010-008-0015-z     Document Type: Article

References (41)

1. Sharma RK (2002) Evolution of the membrane guanylate cyclase transduction system. Mol Cell Biochem 230:3-30. doi: 10.1023/ A:1014280410459 3-30.
2. Sharma RK, Duda T, Venkataraman V, 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
3. Duda T, Sharma RK (2008) ONE-GC membrane guanylate cyclase, a trimodal odorant signal transducer. Biochem Biophys Res Commun 367:440-445. doi: 10.1016/j.bbrc.2007.12.153
4. Sharma RK, Duda T (2006) Calcium sensor neurocalcin δ-modulated ROS-GC transduction machinery in the retinal and olfactory neurons. Calcium Binding Proteins 1:7-11
5. Palczewski K, Sokal I, Baehr W (2004) Guanylate cyclase-activating proteins: Structure, function, and diversity. Biochem Biophys Res Commun 322:1123-1130. doi: 10.1016/j.bbrc.2004.07.122
6. Imanishi Y, Li N, Sokal I, Sowa ME, Lichtarge O, Wensel TG, Saperstein DA, Baehr W, Palczewski K (2002) Characterization of retinal guanylate cyclase-activating protein 3 (GCAP3) from zebrafish to man. Eur J Neurosci 15:63-78. doi: 10.1046/j.0953-816x.2001.01835.x
7. 2+ -binding protein activating photoreceptor guanylyl cyclase. J Biol Chem 270:25200-25206. doi: 10.1074/jbc.270.42.25200
8. Lowe DG, Dizhoor AM, Liu K, Gu Q, Spencer M, Laura R, Lu L, Hurley JB (1995) Cloning and expression of a second photoreceptor-specific membrane retina guanylyl cyclase (RetGC), RetGC-2. Proc Natl Acad Sci USA 92:5535-9553. doi: 10.1073/pnas.92.12.5535
9. Dizhoor AM, Lowe DG, Olshevskaya EV, Laura RP, Hurley JB (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. doi: 10.1016/0896-6273(94)90449-9
10. Duda T, Goraczniak R, Surgucheva I, Rudnicka-Nawrot M, Gorczyca WA, Palczewski K, Sitaramayya A, Baehr W, Sharma RK (1996) Calcium modulation of bovine photoreceptor guanylate cyclase. Biochemistry 35:8478-8482. doi: 10.1021/bi960752z
11. Duda T, Venkataraman V, Krishnan A, Nagele RG, Sharma RK (2001) Negatively calcium-modulated membrane guanylate cyclase signaling system in the rat olfactory bulb. Biochemistry 40:4654-4662. doi: 10.1021/ bi0027985
12. Venkataraman V, Nagele R, Duda T, Sharma RK (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. doi: 10.1021/bi9929960
13. Duda T, Koch K-W, Venkataraman V, Lange C, Beyermann M, Sharma RK (2002) Ca(2+) sensor S100beta-modulated sites of membrane guanylate cyclase in the photoreceptor-bipolar synapse. EMBO J 21:2547-2556. doi: 10.1093/ emboj/21.11.2547
14. 2+ -dependent ROS-GC1 transduction machinery in the gustatory epithelium: A new mechanism in gustatory transduction. FEBS Lett 577:393-398. doi: 10.1016/ j.febslet.2004.09.089
15. Krishnan A, Venkataraman V, Fik-Rymarkiewicz E, Duda T, Sharma RK (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. doi: 10.1021/bi035631v
16. Duda T, Jankowska A, Venkataraman V, Nagele R, Sharma RK (2001) A novel calcium-regulated membrane guanylate cyclase transduction system in the olfactory neuroepithelium. Biochemistry 40:12067-12077. doi: 10.1021/ bi0108406
17. 2+ -signaling membrane guanylate cyclase (ROS-GC) transduction pathway in bovine hippocampus. Mol Cell Biochem 291:187-204. doi: 10.1007/s11010-006-9215-6
18. Duda T, Krishnan R, Sharma RK (2006) GCAP1: Antithetical calcium sensor of ROS-GC transduction machinery. Calcium Binding Proteins 1:102-107
19. Kobayashi M, Takamatsu K, Saitoh S, Miura M, Noguchi T (1992) Molecular cloning of Hpca, a novel calcium-binding protein of the recoverin family exclusively expressed in hippocampus. Biochem Biophys Res Commun 189:511-517. Erratum in: Biochem Biophys Res Commun 196:1017 (1993). doi: 10.1016/0006-291X(92)91587-G
20. Takamatsu K, Kobayashi M, Saitoh S, Fujishiro M, Noguchi T (1994) Molecular cloning of human hippocalcin cDNA and chromosomal mapping of its gene. Biochem Biophys Res Commun 200:606-611. doi: 10.1006/ bbrc.1994.1491
21. Masaki T, Sakai E, Furuta Y, Kobayashi M, Takamatsu K (1998) Genomic structure and chromosomal mapping of the human and mouse hippocalcin genes. Gene 225:117-124. doi: 10.1016/S0378-1119(98)00526-5
22. Brooks SP, Storey KB (1992) Bound and determined: A computer program for making buffers of defined ion concentrations. Anal Biochem 201:119-126. doi: 10.1016/0003-2697(92)90183-8
23. Nambi P, Aiyar NV, Sharma RK (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. doi: 10.1016/0003-9861(82)90545-8
24. Kobayashi M, Masaki T, Hori K, Masuo Y, Miyamoto M, Tsubokawa H, Noguchi H, Nomura M, Takamatsu K (2005) Hippocalcin-deficient mice display a defect in cAMP response element-binding protein activation associated with impaired spatial and associative memory. Neuroscience 133:471-484. doi: 10.1016/j.neuroscience.2005.02.034
25. Zozulya S, Stryer L (1992) Calcium-myristoyl protein switch. Proc Natl Acad Sci USA 89:11569-11573. doi: 10.1073/pnas.89.23.11569
26. Ladant D (1995) Calcium and membrane binding properties of bovine neurocalcin delta expressed in Escherichia coli. J Biol Chem 270:3179-3185
27. McFerran BW, Weiss JL, Burgoyne RD (1999) Neuronal Ca(2+) sensor 1. Characterization of the myristoylated protein, its cellular effects in permeabilized adrenal chromaffin cells, Ca(2+)-independent membrane association, and interaction with binding proteins, suggesting a role in rapid Ca(2+) signal transduction. J Biol Chem 274:30258-30265. doi: 10.1074/jbc.274.42.30258
28. Kobayashi M, Takamatsu K, Saitoh S, Noguchi T (1993) Myristoylation of hippocalcin is linked to its calcium-dependent membrane association properties. J Biol Chem 268:18898-18904
29. 2+ signal transduction. J Biol Chem 277:14227-14237. doi: 10.1074/ jbc.M111750200
30. 2+/myristoyl switch protein hippocalcin in living cells. J Cell Biol 163:715-721. doi: 10.1083/jcb.200306042
31. Caenepeel S, Charydczak G, Sudarsanam S, Hunter T, Manning G (2004) The mouse kinome: Discovery and comparative genomics of all mouse protein kinases. Proc Natl Acad Sci USA 101:11707-11712. doi: 10.1073/ pnas.0306880101
32. Mammen A, Simpson PJ, Nighorn A, Imanishi Y, Palczewski K, Ronnett GV, Moon C (2004) Hippocalcin in the olfactory epithelium: A mediator of second messenger signaling. Biochem Biophys Res Commun 322:1131-1139. Erratum in: Biochem Biophys Res Commun. 326:694 (2005). doi: 10.1016/ j.bbrc.2004.07.123
33. Reisert J, Yau KW, Margolis FL (2007) Olfactory marker protein modulates the cAMP kinetics of the odour-induced response in cilia of mouse olfactory receptor neurons. J Physiol 585:731-740. doi: 10.1113/ jphysiol.2007.142471
34. Bakalyar HA, Reed RR (1990) Identification of a specialized adenylyl cyclase that may mediate odorant detection. Science 250:1403-1406. doi: 10.1126/science.2255909
35. Dhallan RS, Yau KW, Schrader KA, Reed RR (1990) Primary structure and functional expression of a cyclic nucleotide-activated channel from olfactory neurons. Nature 347:184-187. doi: 10.1038/347184a0
36. Sklar PB, Anholt RR, Snyder SH (1986) The odorant-sensitive adenylate cyclase of olfactory receptor cells. Differential stimulation by distinct classes of odorants. J Biol Chem 261:15538-15543
37. Juilfs DM, Fülle HJ, Zhao AZ, Houslay MD, Garbers DL, Beavo JA (1997) A subset of olfactory neurons that selectively express cGMP-stimulated phosphodiesterase (PDE2) and guanylyl cyclase- d define a unique olfactory signal transduction pathway. Proc Natl Acad Sci USA 94:3388-3395. doi: 10.1073/pnas.94.7.3388
38. Leinders-Zufall T, Cockerham RE, Michalakis S, Biel M, Garbers DL, Reed RR, Zufall F, Munger SD (2007) Contribution of the receptor guanylyl cyclase GC-D to chemosensory function in the olfactory epithelium. Proc Natl Acad Sci USA 104:14507-14512. doi: 10.1073/pnas.0704965104
39. Meyer MR, Angele A, Kremmer E, Kaupp UB, Muller F (2000) A cGMP-signaling pathway in a subset of olfactory sensory neurons. Proc Natl Acad Sci USA 97:10595-10600. doi: 10.1073/pnas.97.19.10595
40. Duda T, Fik-Rymarkiewicz E, Venkataraman V, Krishnan A, Sharma RK (2004) Calcium-modulated ciliary membrane guanylate cyclase transduction machinery: Constitution and operational principles. Mol Cell Biochem 267:107-122. Erratum in: Mol Cell Biochem. 273:225-226. doi: 10.1023/ B:MCBI.0000049372.33965.4f
41. 2+-modulated machinery: constitution and operational principles. In: Phillippov P, Koch KW (eds) Neuronal calcium sensor proteins. Nova Science Publishers, Hauppage, NY, USA, pp 91-113