The Neuronal Calcium Sensor Protein Acrocalcin: A Potential Target of Calmodulin Regulation during Development in the Coral Acropora millepora

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Reyes Bermudez, Alejandro ^a,b   Miller, David J ^a   Sprungala, Susanne ^a  

^a JAMES COOK UNIVERSITY   (Australia)

^b OKINAWA INSTITUTE OF SCIENCE AND TECHNOLOGY GRADUATE UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ACROCALCIN; CALMODULIN; COMPLEMENTARY DNA; MESSENGER RNA; NEURONAL CALCIUM SENSOR; UNCLASSIFIED DRUG;

ACROPORA MILLEPORA; AMAC GENE; AMCAM GENE; ARTICLE; BINDING SITE; CALCIUM SIGNALING; CONTROLLED STUDY; CORAL; DEVELOPMENTAL BIOLOGY; DNA DETERMINATION; GASTRULATION; GENE IDENTIFICATION; GENE TARGETING; IN VIVO STUDY; LARVAL STAGE; METAMORPHOSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING;

AMINO ACID SEQUENCE; ANIMALS; ANTHOZOA; BLOTTING, NORTHERN; CALCIUM; CALMODULIN; CHROMATOGRAPHY, AFFINITY; DNA, COMPLEMENTARY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IN SITU HYBRIDIZATION; LARVA; METAMORPHOSIS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; NEURONAL CALCIUM-SENSOR PROTEINS; PROTEIN BINDING; REAL-TIME POLYMERASE CHAIN REACTION; RECOMBINANT PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SEQUENCE HOMOLOGY, AMINO ACID;

ACROPORA MILLEPORA; ANTHOZOA; SCLERACTINIA;

EID: 84871311574     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0051689     Document Type: Article

References (56)

1. Gunderson L, (2007) Ecology: a different route to recovery for coral reefs. Curr Biol 17: R27-28.
2. Veron J (2000) Corals of the world. Townsville: Australian Institute of Marine Sciences.
3. DeSalvo MK, Voolstra CR, Sunagawa S, Schwarz JA, Stillman JH, et al. (2008) Differential gene expression during thermal stress and bleaching in the Caribbean coral Montastraea faveolata. Mol Ecol 17: 3952-3971.
4. Grasso LC, Maindonald J, Rudd S, Hayward DC, Saint R, et al. (2008) Microarray analysis identifies candidate genes for key roles in coral development. BMC Genomics 9: 540.
5. Reyes-Bermudez A, Desalvo MK, Voolstra CR, Sunagawa S, Szmant AM, et al. (2009) Gene expression microarray analysis encompassing metamorphosis and the onset of calcification in the scleractinian coral Montastraea faveolata. Marine Genomics 2: 149-159.
6. Grasso LC, Negri AP, Foret S, Saint R, Hayward DC, et al. (2011) The biology of coral metamorphosis: molecular responses of larvae to inducers of settlement and metamorphosis. Dev Biol 353: 411-419.
7. Miller DJ (2011) Coralbase: Acropora millepora genome assembly pre-release www.coralbase.org.
8. Shinzato C, Shoguchi E, Kawashima T, Hamada M, Hisata K, et al. (2011) Using the Acropora digitifera genome to understand coral responses to environmental change. Nature 476: 320-323.
9. Carafoli E, (2002) Calcium signaling: a tale for all seasons. Proc Natl Acad Sci U S A 99: 1115-1122.
10. Haeseleer F, Imanishi Y, Sokal I, Filipek S, Palczewski K, (2002) Calcium-binding proteins: intracellular sensors from the calmodulin superfamily. Biochem Biophys Res Comm 290: 615-623.
11. Carafoli E, Genazzani A, Guerini D, (1999) Calcium controls the transcription of its own transporters and channels in developing neurons. Biochem Biophys Res Comm 266: 624-632.
12. Bähler M, Rhoads A, (2002) Calmodulin signalling via the IQ motif. FEBS Letters 513: 107-113.
13. Bhattacharya S, Bunick CG, Chazin WJ, (2004) Target selectivity in EF-hand calcium binding proteins. Biochim Biophys Acta 1742: 69-79.
14. Gifford JL, Walsh MP, Vogel HJ, (2007) Structures and metal-ion-binding properties of the Ca2+-binding helix-loop-helix EF-hand motifs. Biochem J 405: 199-221.
15. Cyert MS, (2001) Genetic analysis of calmodulin and its targets in Saccharomyces cerevisiae. Ann Rev Genet 35: 647-672.
16. Carafoli E, (2005) Calcium-a universal carrier of biological signals. Delivered on 3 July 2003 at the Special FEBS Meeting in Brussels. FEBS J 272: 1073-1089.
17. Jamieson GA, Bronson DD, Schachat FH, Vanaman TC, (1980) Structure and function relationships among Calmodulins and tropinin C-like proteins from divergent eukaryotic organisms. Annals NY Acad Sci 356: 1-13.
18. Morita M, Iguchi A, Takemura A, (2009) Roles of calmodulin and calcium/calmodulin-dependent protein kinase in flagellar motility regulation in the coral Acropora digitifera. Mar Biotech 11: 118-123.
19. Yuasa HJ, Suzuki T, Yazawa M, (2001) Structural organization of lower marine nonvertebrate calmodulin genes. Gene 279: 205-212.
20. Chen IP, Tang CY, Chiou CY, Hsu JH, Wei NV, et al. (2009) Comparative analyses of coding and noncoding DNA regions indicate that Acropora (Anthozoa: Scleractina) possesses a similar evolutionary tempo of nuclear vs. mitochondrial genomes as in plants. Mar Biotech 11: 141-152.
21. Moya A, Huisman L, Ball EE, Hayward DC, Grasso LC, et al. (2012) Whole transcriptome analysis of the coral Acropora millepora reveals complex responses to CO2-driven acidification during the initiation of calcification. Mol Ecol 21: 2440-2454.
22. Hayward DC, Catmull J, Reece-Hoyes JS, Berghammer H, Dodd H, et al. (2001) Gene structure and larval expression of cnox-2Am from the coral Acropora millepora. Dev Genes Evol 211: 10-19.
23. Hayward DC, Hetherington S, Behm CA, Grasso LC, Foret S, et al. (2011) Differential gene expression at coral settlement and metamorphosis- a subtractive hybridization study. PloS One 6: e26411.
24. Sambrook JF, Fritsch EF, Maniatis T (1989) Molecular Cloning: A laboratory manual. Cold Spring Harbour, New York: Cold Spring Harbour Press.
25. de Jong DM, Hislop NR, Hayward DC, Reece-Hoyes JS, Pontynen PC, et al. (2006) Components of both major axial patterning systems of the Bilateria are differentially expressed along the primary axis of a 'radiate' animal, the anthozoan cnidarian Acropora millepora. Dev Biol 298: 632-643.
26. Burgoyne RD, O'Callaghan DW, Hasdemir B, Haynes LP, Tepikin AV, (2004) Neuronal Ca2+-sensor proteins: multitalented regulators of neuronal function. Trends Neurosci 27: 203-209.
27. Ball EE, Hayward DC, Reece-Hoyes JS, Hislop NR, Samuel G, et al. (2002) Coral development: from classical embryology to molecular control. Int J Dev Biol 46: 671-678.
28. Ball EE, Hayward DC, Catmull J, Reece-Hoyes JS, Hislop NR, et al. (2000) Molecular control of development in the reef coral, Acropora millepora. Proc 9th Int Coral Reefs Symp: 395-401.
29. Morse ANC, Iwao K, Baba M, Shimoike K, Hayashibara T, et al. (1996) An ancient chemosensory mechanism brings new life to coral reefs. Biol Bull 191: 149-154.
30. Harrison PL, Wallace CC (1990) Reproduction, dispersal and recruitment of Scleractinian corals. In: Dubinsky Z, editor. Coral Reefs. Amsterdam: Elsevier Science Publisher BV 133-207.
31. Vandermeulen JH, (1975) Studies on Coral Reefs.III. Fine Structural Changes of Calicoblast Cells in Pocillopora damicornis during Settling and Calcification. Mar Biol 31: 69-77.
32. Vetter SW, Leclerc E, (2003) Novel aspects of calmodulin target recognition and activation. Eur J Biochem 270: 404-414.
33. Lab I (2002) Calmodulin Target Database http://calcium.uhnres.utoronto.ca/ctdb/.
34. Rhoads AR, Friedberg F, (1997) Sequence motifs for calmodulin recognition. FASEB J 11: 331-340.
35. Benaim G, Villalobo A, (2002) Phosphorylation of calmodulin. Functional implications. Eur J Biochem 269: 3619-3631.
36. Wallace RW, Tallant EA, Dockter ME, Cheung WY, (1982) Calcium binding domains of calmodulin. Sequence of fill as determined with terbium luminescence. J Biol Chem 257: 1845-1854.
37. Burgess WH, Jemiolo DK, Kretsinger RH, (1980) Interaction of calcium and calmodulin in the presence of sodium dodecyl sulfate. Biochim Biophys Acta 623: 257-270.
38. Burgoyne RD, Weiss JL, (2001) The neuronal calcium sensor family of Ca2+-binding proteins. Biochem J 353: 1-12.
39. Burgoyne RD, (2007) Neuronal calcium sensor proteins: generating diversity in neuronal Ca2+ signalling. Nat Rev Neurosci 8: 182-193.
40. Ames JB, Lim S, (2012) Molecular structure and target recognition of neuronal calcium sensor proteins. Biochim Biophys Acta 1820: 1205-1213.
41. Pongs O, Lindemeier J, Zhu XR, Theil T, Engelkamp D, et al. (1993) Frequenin-a novel calcium-binding protein that modulates synaptic efficacy in the Drosophila nervous system. Neuron 11: 15-28.
42. McCue HV, Haynes LP, Burgoyne RD, (2010) The diversity of calcium sensor proteins in the regulation of neuronal function. Cold Spring Harbor Perspectives in Biology 2: a004085.
43. De Castro E, Nef S, Fiumelli H, Lenz SE, Kawamura S, et al. (1995) Regulation of rhodopsin phosphorylation by a family of neuronal calcium sensors. Biochem Biophys Res Comm 216: 133-140.
44. Putnam NH, Srivastava M, Hellsten U, Dirks B, Chapman J, et al. (2007) Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 317: 86-94.
45. Zoccola D, Tambutte E, Kulhanek E, Puverel S, Scimeca JC, et al. (2004) Molecular cloning and localization of a PMCA P-type calcium ATPase from the coral Stylophora pistillata. Biochim Biophys Acta 1663: 117-126.
46. Ishida H, Nakashima K, Kumaki Y, Nakata M, Hikichi K, et al. (2002) The solution structure of apocalmodulin from Saccharomyces cerevisiae implies a mechanism for its unique Ca2+ binding property. Biochem 41: 15536-15542.
47. O'Donnell SE, Newman RA, Witt TJ, Hultman R, Froehlig JR, et al. (2009) Thermodynamics and conformational change governing domain-domain interactions of calmodulin. Methods Enzymol 466: 503-526.
48. O'Donnell SE, Yu L, Fowler CA, Shea MA, (2011) Recognition of beta-calcineurin by the domains of calmodulin: thermodynamic and structural evidence for distinct roles. Proteins 79: 765-786.
49. Amici M, Doherty A, Jo J, Jane D, Cho K, et al. (2009) Neuronal calcium sensors and synaptic plasticity. Biochem Soc Trans 37: 1359-1363.
50. Hilfiker S, (2003) Neuronal calcium sensor-1: a multifunctional regulator of secretion. Biochem Soc Trans 31: 828-832.
51. Weiss JL, Hui H, Burgoyne RD, (2010) Neuronal calcium sensor-1 regulation of calcium channels, secretion, and neuronal outgrowth. Cell Mol Neurobiol 30: 1283-1292.
52. Haynes LP, Fitzgerald DJ, Wareing B, O'Callaghan DW, Morgan A, et al. (2006) Analysis of the interacting partners of the neuronal calcium-binding proteins L-CaBP1, hippocalcin, NCS-1 and neurocalcin delta. Proteomics 6: 1822-1832.
53. Ivings L, Pennington SR, Jenkins R, Weiss JL, Burgoyne RD, (2002) Identification of Ca2+-dependent binding partners for the neuronal calcium sensor protein neuroncalcin: interaction with actin, clathrin and tubulin. Biochem J 363: 599-608.
54. Clode PL, Marshall AT, (2004) Calcium localisation by X-ray microanalysis and fluorescence microscopy in larvae of zooxanthellate and azooxanthellate corals. Tissue Cell 36: 379-390.
55. Vandermeulen JH, Watabe N, (1973) Studies on Reef Corals. I. Skeleton formation by newly settled planula larva of Pocillopora damicornis. Mar Biol 23: 47-57.
56. Vandermeulen JH, (1974) Studies on Reefs Corals II. Fine structure of planktonic planula larva of Pocillopora damicornis with emphasis on the aboral epidermis. Mar Biol 27: 239-249.