Skip to main content

Sponge OAS has a distinct genomic structure within the 2-5A synthetase family

Abstract

2′,5′-Oligoadenylate synthetases (2-5A synthetases, OAS) are enzymes that play an important role in the interferon-induced antiviral defense mechanisms in mammals. Sponges, the evolutionarily lowest multicellular animals, also possess OAS; however, their function is presently unclear. Low homology between primary structures of 2-5A synthetases from vertebrates and sponges renders their evolutionary relationship obscure. The genomic structure of vertebrate OASs has been thoroughly examined, making it possible to elucidate molecular evolution and expansion of this gene family. Until now, no OAS gene structure was available from sponges to compare it with the corresponding genes from higher organisms. In the present work, we determined the exon/intron structure of the OAS gene from the marine sponge Geodia cydonium and found it to be completely different from the strictly conserved exon/intron pattern of the OAS genes from vertebrates. This finding was corroborated by the analysis of OAS genes from another sponge, Amphimedon queenslandica, whose genome was recently sequenced. Our data suggest that vertebrate and sponge OAS genes have no direct common intron-containing ancestor and two (sub)types of OAS may be discriminated. This study opens new perspectives for understanding the phylogenesis and evolution of 2-5A synthetases as well as functional aspects of this multigene family.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

References

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    PubMed  Article  CAS  Google Scholar 

  • Aravind A, Koonin E (1999) DNA polymerase β-like nucleotidyltransferase superfamily: identification of three new families, classification and evolutionary history. Nucleic Acids Res 27:1609–1618

    PubMed  Article  CAS  Google Scholar 

  • Borojevič R, Fry WG, Jones WC, Levi C, Rasmont R, Sara M, Vacelet J (1968) A reassessment of the terminology for sponges. Bull Mus Nat Hist Nat Paris 39:1124–1135

    Google Scholar 

  • Cannon SB, Mitra A, Baumgarten A, Young ND, May G (2004) The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol 4:10

    PubMed  Article  Google Scholar 

  • Chawla-Sarkar M, Lindner DJ, Liu YF, Williams BR, Sen GC, Silverman RH, Borden EC (2003) Apoptosis and interferons: role of interferon-stimulated genes as mediators of apoptosis. Apoptosis 8:237–249

    PubMed  Article  CAS  Google Scholar 

  • Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium tiocyanate–phenol–chloroform extraction. Anal Biochem 162:156–159

    PubMed  Article  CAS  Google Scholar 

  • Degnan B (2007) The origin of animal development: insights from sponge evolutionary and functional genomics. In: Fourth international symposium on networks in bioinformatics (ISNB), 16–19 April 2007, Amsterdam, The Netherlands. http://www.nbic.nl/content/documents/10920/Degnan_ISNB07.pdf

  • Eskildsen S, Hartmann R, Kjeldgaard NO, Justesen J (2002) Gene structure of the murine 2′-5′-oligoadenylate synthetase family. Cell Mol Life Sci 59:1212–1222

    PubMed  Article  CAS  Google Scholar 

  • Gauthier M, Degnan BM (2008) Partitioning of genetically distinct cell populations in chimeric juveniles of the sponge Amphimedon queenslandica. Dev Comp Immunol 32(11):1270–1280. doi:10.1016/j.dci.2008.04.002

    PubMed  Article  CAS  Google Scholar 

  • Ghosh A, Sarkar SN, Sen GC (2000) Cell growth regulatory and antiviral effects of the P69 isozyme of 2–5 (A) synthetase. Virology 266:319–328

    PubMed  Article  CAS  Google Scholar 

  • Grebenjuk VA, Kuusksalu A, Kelve M, Schütze J, Schröder HC, Müller WE (2002) Induction of (2′-5′)oligoadenylate synthetase in the marine sponges Suberites domuncula and Geodia cydonium by the bacterial endotoxin lipopolysaccharide. Eur J Biochem 269:1382–1392

    PubMed  Article  CAS  Google Scholar 

  • Hartman WD, Reiswig HM (1973) The individuality of sponges. Animal colonies. Dowden, Hutchinson and Ross Inc, Stroudsburg, pp 567–584

    Google Scholar 

  • Hartmann R, Justesen J, Sarkar SN, Sen GC, Yee VC (2003) Crystal structure of the 2′-specific and double-stranded RNA-activated interferon-induced antiviral protein 2′-5′-oligoadenylate synthetase. Mol Cell 12:1173–1185

    PubMed  Article  CAS  Google Scholar 

  • Holm L, Sander C (1995) DNA polymerase β belongs to an ancient nucleotidyltransferase superfamily. Trends Biochim Sci 20:345–347

    Article  CAS  Google Scholar 

  • Hovanessian AG (2007) On the discovery of interferon-inducible, double-stranded RNA activated enzymes: the 2′-5′ oligoadenylate synthetases and the protein kinase PKR. Cytokine and Growth Factor Rev 18:351–361

    Article  CAS  Google Scholar 

  • Imsiecke G, Custodio M, Borojevic R, Steffen R, Moustafa A, Müller WEG (1995) Genome size and chromosomes in marine sponges [Suberites domuncula, Geodia cydonium]. Cell Biol Int 19:995–1000

    PubMed  Article  CAS  Google Scholar 

  • Justesen J, Hartmann R, Kjeldgaard NO (2000) Gene structure and function of the 2′, 5′-oligoadenylate synthetase family. Cell Mol Life Sci 57:1593–1612

    PubMed  Article  CAS  Google Scholar 

  • Kumar S, Mitnik C, Valente G, Floyd-Smith G (2000) Expansion and molecular evolution of the interferon-induced 2′-5′ oligoadenylate synthetase gene family. Mol Biol Evol 17:738–750

    PubMed  CAS  Google Scholar 

  • Kuusksalu A, Pihlak A, Müller WE, Kelve M (1995) The (2′-5′)oligoadenylate synthetase is present in the lowest multicellular organisms, the marine sponges. Demonstration of the existence and identification of its reaction products. Eur J Biochem 232:351–357

    PubMed  Article  CAS  Google Scholar 

  • Kuusksalu A, Subbi J, Pehk T, Reintamm T, Müller WE, Kelve M (1998) Identification of the reaction products of (2′-5′)oligoadenylate synthetase in the marine sponge. Eur J Biochem 257:420–426

    PubMed  Article  CAS  Google Scholar 

  • Lieberkühn N (1856) Zusätze zur Entwicklungsgeschichte der Spongilliden. Arch Anat Physiol, pp 496–514

  • Lopp A, Kuusksalu A, Reintamm T, Müller WEG, Kelve M (2002) 2′, 5′-oligoadenylate synthetase from a lower invertebrate, the marine sponge Geodia cydonium, does not need dsRNA for its enzymatic activity. Biochim Biophys Acta 1590:140–149

    PubMed  Article  CAS  Google Scholar 

  • Lynch M, Conery JS (2000) The evolutionary fate and consequences of duplicate genes. Science 290:1151–1155

    PubMed  Article  CAS  Google Scholar 

  • Martin G, Keller W (2007) RNA-specific ribonucleotidyl transferases. RNA 11:1834–1849

    Article  Google Scholar 

  • Mashimo T, Glaser P, Lucas M, Simon-Chazottes D, Ceccaldi PE, Montagutelli X, Desprès P, Guénet JL (2003) Structural and functional genomics and evolutionary relationships in the cluster of genes encoding murine 2′,5′-oligoadenylate synthetases. Genomics 82:537–552

    PubMed  Article  CAS  Google Scholar 

  • Mirsky AE, Ris H (1951) The desoxyribonucleic acid content of animal cells and its evolutionary significance. J Gen Physiol 34:451–462

    PubMed  Article  CAS  Google Scholar 

  • Müller WEG, Müller IM (2003) Origin of the metazoan immune system: identification of the molecules and their functions in sponges. Integr Comp Biol 43:281–292

    Article  Google Scholar 

  • Müller WE, Böhm M, Grebenjuk VA, Skorokhod A, Müller IM, Gamulin V (2002) Conservation of the positions of metazoan introns from sponges to humans. Gene 295:299–309

    PubMed  Article  Google Scholar 

  • Müller WEG, Brümmer F, Batel R, Müller IM, Schröder HC (2003) Molecular biodiversity. Case study: Porifera (sponges). Naturwissenschaften 90:103–120

    PubMed  Article  Google Scholar 

  • Nichols SA, Dirks W, Pearse JS, King N (2006) Early evolution of animal cell signaling and adhesion genes. Proc Natl Acad Sci USA 103:12451–12456

    PubMed  Article  CAS  Google Scholar 

  • Päri M, Kuusksalu A, Lopp A, Reintamm T, Justesen J, Kelve M (2007) Expression and characterization of recombinant 2′, 5′-oligoadenylate synthetase from the marine sponge Geodia cydonium. FEBS J 274:3462–3474

    PubMed  Article  Google Scholar 

  • Perelygin AA, Zharkikh AA, Scherbik SV, Brinton MA (2006) The mammalian 2′-5′ oligoadenylate synthetase gene family: evidence for concerted evolution of paralogous Oas1 genes in Rodentia and Artiodactyla. J Mol Evol 63:562–576

    PubMed  Article  CAS  Google Scholar 

  • Player MR, Torrence PF (1998) The 2-5A system: modulation of viral and cellular processes through acceleration of RNA degradation. Pharmacol Ther 78:55–113

    PubMed  Article  CAS  Google Scholar 

  • Reintamm T, Lopp A, Kuusksalu A, Subbi J, Kelve M (2003) Qualitative and quantitative aspects of 2-5A synthesizing capacity of different marine sponges. Biomol Eng 20:389–399

    PubMed  Article  CAS  Google Scholar 

  • Rogozin IB, Aravind L, Koonin EV (2003) Differential action of natural selection on the A and C-terminal domains of 2′-5′ oligoadenylate synthetases and the potential nuclease function of the C-terminal domain. J Mol Biol 326:1449–1461

    PubMed  Article  CAS  Google Scholar 

  • Rogozin IB, Sverdlov AV, Babenko VN, Koonin EV (2005) Analysis of evolution of exon-intron structure of eukaryotic genes. Brief Bioinform 6:118–134

    PubMed  Article  CAS  Google Scholar 

  • Salzberg S, Hyman T, Turm H, Kinar Y, Schwartz Y, Nir U, Lejbkowicz F, Huberman E (1997) Ectopic expression of 2-5A synthetase in myeloid cells induces growth arrest and facilitates the appearance of a myeloid differentiation marker. Cancer Res 57:2732–2740

    PubMed  CAS  Google Scholar 

  • Sarkar SN, Miyagi M, Crabb JW, Sen GC (2002) Identification of the substrate-binding sites of 2′-5′-oligoadenylate synthetase. J Biol Chem 277:24321–24330

    PubMed  Article  CAS  Google Scholar 

  • Schmidt O (1864) Supplement der Spongien des Adriatischen Meeres. Leipzig 23

  • Schröder HC, Natalio F, Wiens M, Tahir MN, Shukoor MI, Tremel W, Belikov SI, Krasko A, Müller WEG (2008) The 2′-5′-oligoadenylate in the lowest metazoa: isolation, cloning, expression and functional activity in the sponge Lubomirskia baicalensis. Mol Immunol 45:945–953

    PubMed  Article  Google Scholar 

  • Sperling J, Chebath J, Arad-Dann H, Offen D, Spann P, Lehrer R, Goldblatt D, Jolles B, Sperling R (1991) Possible involvement of (2′-5′)oligoadenylate synthetase activity in pre-mRNA splicing. Proc Natl Acad Sci USA 88:10377–10381

    PubMed  Article  CAS  Google Scholar 

  • Venkatesh B, Kirkness EF, Loh YH, Halpern AL, Lee AP, Johnson J, Dandona N, Viswanathan LD, Tay A, Venter JC, Strausberg RL, Brenner S (2007) Survey sequencing and comparative analysis of the elephant shark (Callorhinchus milii) genome. PLoS Biol 5:e101

    PubMed  Article  Google Scholar 

  • Wiens M, Kuusksalu A, Kelve M, Müller WE (1999) Origin of the interferon-inducible (2′-5′)oligoadenylate synthetases: cloning of the (2′-5′)oligoadenylate synthetase from the marine sponge Geodia cydonium. FEBS Lett 462:12–18

    PubMed  Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the European Comission (project COOP-CT-2005, contract number 017800) and the Estonian Science Foundation (grant No. 5932).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Merike Kelve.

Additional information

Abbreviations

The nomenclature of particular OASs in the present paper is based on the level of their sequence similarities. OAS1 refers to the OAS consisting of a single OAS domain. Capital letters (OAS1X) are used to differentiate between OAS1 types with sequence homologies of less than 50%; their variants are additionally marked in small letters (OASXx, sequence homology ~70 to ~95%). Labels prime and double prime denote sponge OAS1Xx gene haplotypes (sequence homology close to 100%, a few amino acid substitutions).

Communicated by S. Hohmann.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Electronic supplementary material (DOC 109 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Reintamm, T., Kuusksalu, A., Metsis, M. et al. Sponge OAS has a distinct genomic structure within the 2-5A synthetase family. Mol Genet Genomics 280, 453–466 (2008). https://doi.org/10.1007/s00438-008-0379-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-008-0379-5

Keywords

  • 2′,5′-Oligoadenylate synthetase
  • OAS
  • Genomic structure
  • Sponge
  • Geodia cydonium
  • Amphimedon queenslandica