Advertisement

Evolution of the 2′-5′-Oligoadenylate Synthetase Family in Eukaryotes and Bacteria

  • Karina Hansen Kjaer
  • Jesper Buchhave Poulsen
  • Tõnu Reintamm
  • Emilie Saby
  • Pia Moeller Martensen
  • Merike Kelve
  • Just Justesen
Article

Abstract

The 2′-5′-oligoadenylate synthetase (OAS) belongs to a nucleotidyl transferase family that includes poly(A) polymerases and CCA-adding enzymes. In mammals and birds, the OAS functions in the interferon system but it is also present in an active form in sponges, which are devoid of the interferon system. In view of these observations, we have pursued the idea that OAS genes could be present in other metazoans and in unicellular organisms as well. We have identified a number of OAS1 genes in annelids, mollusks, a cnidarian, chordates, and unicellular eukaryotes and also found a family of proteins in bacteria that contains the five OAS-specific motifs. This indicates a specific relationship to OAS. The wide distribution of the OAS genes has made it possible to suggest how the OAS1 gene could have evolved from a common ancestor to choanoflagellates and metazoans. Furthermore, we suggest that the OASL may have evolved from an ancestor of cartilaginous fishes, and that the OAS2 and the OAS3 genes evolved from a mammalian ancestor. OAS proteins function in the interferon system in mammals. This system is only found in jawed vertebrates. We therefore suggest that the original function of OAS may differ from its function in the interferon system, and that this original function of OAS is preserved even in OAS genes that code for proteins, which do not have 2′-5′-oligoadenylate synthetase activity.

Keywords

Oligoadenylate synthetase CCA-adding enzyme Evolution Interferon Phylogeny 

Abbreviations

OAS

2′-5′-Oligoadenylate synthetase.

OASL

2′-5′-Oligoadenylate synthetase like.

2-5A

2′-5′-Oligoadenylates.

IFN

Interferon

RNaseL

Ribonuclease L

EST

Expressed sequence tag

BLAST

Basic local alignment search tool

Notes

Acknowledgments

We thank the technical assistance from Lotte Quist. We thank Shawn Iadonato and Christina Scherer Kineta Inc, Seattle, WA, USA and Mia Schødt Dickow for help and stimulating discussions and Mikkel Heide Schierup for critical reading of the manuscript. Niels Larsen has helped us with definition of motifs and discussions on molecular evolution. Peter Funch is thanked for a highly appreciated discussion of this manuscript using his expertise in phylogenetics and systematics. The work was initially supported by a grant from the Danish Natural Science Council and the Carlsberg Foundation. The work was supported by the Estonian Science Foundation (Grant no. 7421).

Supplementary material

239_2009_9299_MOESM1_ESM.doc (4.2 mb)
(DOC 4,269 kb)
239_2009_9299_MOESM2_ESM.doc (106 kb)
(DOC 106 kb)
239_2009_9299_MOESM3_ESM.doc (66 kb)
(DOC 67 kb)
239_2009_9299_MOESM4_ESM.doc (101 kb)
(DOC 101 kb)

References

  1. Bandyopadhyay S, Ghosh A, Sarkar SN, Sen GC (1998) Production and purification of recombinant 2′-5′ oligoadenylate synthetase and its mutants using the baculovirus system. Biochemistry 37:3824–3830CrossRefPubMedGoogle Scholar
  2. Beck G, Habicht GS (1991) Primitive cytokines: harbingers of vertebrate defense. Immunol Today 12:180–183CrossRefPubMedGoogle Scholar
  3. Beck G, Habicht GS (1996) Characterization of an IL-6-like molecule from an echinoderm (Asterias forbesi). Cytokine 8:507–512CrossRefPubMedGoogle Scholar
  4. Beitz E (2000) TEXshade: shading and labeling of multiple sequence alignments using LATEX2 epsilon. Bioinformatics 16:135–139CrossRefPubMedGoogle Scholar
  5. Cayley PJ, White RF, Antoniw JF, Walesby NJ, Kerr IM (1982) Distribution of the ppp(A2’p)nA-binding protein and interferon-related enzymes in animals, plants, and lower organisms. Biochem Biophys Res Commun 108:1243–1250CrossRefPubMedGoogle Scholar
  6. Eskildsen S, Justesen J, Schierup MH, Hartmann R (2003) Characterization of the 2′-5′-oligoadenylate synthetase ubiquitin-like family. Nucleic Acids Res 31:3166–3173CrossRefPubMedGoogle Scholar
  7. Ferbus D, Justesen J, Besancon F, Thang MN (1981) The 2′5′ oligoadenylate synthetase has a multifunctional 2′5′ nucleotidyl-transferase activity. Biochem Biophys Res Commun 100:847–856CrossRefPubMedGoogle Scholar
  8. Ghosh A, Desai SY, Sarkar SN, Ramaraj P, Ghosh SK, Bandyopadhyay S, Sen GC (1997a) Effects of mutating specific residues present near the amino terminus of 2′-5′-oligoadenylate synthetase. J Biol Chem 272:15452–15458CrossRefPubMedGoogle Scholar
  9. Ghosh A, Sarkar SN, Guo W, Bandyopadhyay S, Sen GC (1997b) Enzymatic activity of 2′-5′-oligoadenylate synthetase is impaired by specific mutations that affect oligomerization of the protein. J Biol Chem 272:33220–33226CrossRefPubMedGoogle Scholar
  10. Grebenjuk VA, Kuusksalu A, Kelve M, Schutze J, Schroder HC, Muller 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 269:1382–1392CrossRefPubMedGoogle Scholar
  11. 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 12:1173–1185CrossRefPubMedGoogle Scholar
  12. Hovanessian AG, Justesen J (2007) The human 2′-5′oligoadenylate synthetase family: unique interferon-inducible enzymes catalyzing 2′-5′ instead of 3′-5′ phosphodiester bond formation. Biochimie 89:779–788CrossRefPubMedGoogle Scholar
  13. Hughes TK Jr, Smith EM, Chin R, Cadet P, Sinisterra J, Leung MK, Shipp MA, Scharrer B, Stefano GB (1990) Interaction of immunoactive monokines (interleukin 1 and tumor necrosis factor) in the bivalve mollusc Mytilus edulis. Proc Natl Acad Sci USA 87:4426–4429CrossRefPubMedGoogle Scholar
  14. Justesen J, Hartmann R, Kjeldgaard NO (2000) Gene structure and function of the 2′-5′-oligoadenylate synthetase family. Cell Mol Life Sci 57:1593–1612CrossRefPubMedGoogle Scholar
  15. Kaiser P, Rothwell L, Avery S, Balu S (2004) Evolution of the interleukins. Dev Comp Immunol 28:375–394CrossRefPubMedGoogle Scholar
  16. Kon N, Suhadolnik RJ (1996) Identification of the ATP binding domain of recombinant human 40-kDa 2′, 5′-oligoadenylate synthetase by photoaffinity labeling with 8-azido-[alpha-32P]ATP. J Biol Chem 271:19983–19990CrossRefPubMedGoogle Scholar
  17. 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 17:738–750PubMedGoogle Scholar
  18. Kuusksalu A, Pihlak A, Muller 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 232:351–357CrossRefPubMedGoogle Scholar
  19. Lane KT, Beese LS (2006) Thematic review series: lipid posttranslational modifications. Structural biology of protein farnesyltransferase and geranylgeranyltransferase type I. J Lipid Res 47:681–699CrossRefPubMedGoogle Scholar
  20. Martin G, Keller W (2007) RNA-specific ribonucleotidyl transferases. RNA 13:1834–1849CrossRefPubMedGoogle Scholar
  21. Pari 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 274:3462–3474CrossRefPubMedGoogle Scholar
  22. 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 63:562–576CrossRefPubMedGoogle Scholar
  23. Raftos DA, Cooper EL, Habicht GS, Beck G (1991) Invertebrate cytokines: tunicate cell proliferation stimulated by an interleukin 1-like molecule. Proc Natl Acad Sci USA 88:9518–9522CrossRefPubMedGoogle Scholar
  24. Rogozin IB, Aravind L, Koonin EV (2003) Differential action of natural selection on the N and C-terminal domains of 2′-5′ oligoadenylate synthetases and the potential nuclease function of the C-terminal domain. J Mol Biol 326:1449–1461CrossRefPubMedGoogle Scholar
  25. Sadler AJ, Williams BR (2008) Interferon-inducible antiviral effectors. Nat Rev Immunol 8:559–568CrossRefPubMedGoogle Scholar
  26. 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 57:2732–2740PubMedGoogle Scholar
  27. Samuel CE (2001) Antiviral actions of interferons. Clin Microbiol Rev 14:778–809 table of contentsCrossRefPubMedGoogle Scholar
  28. Sarkar SN, Ghosh A, Wang HW, Sung SS, Sen GC (1999) The nature of the catalytic domain of 2′-5′-oligoadenylate synthetases. J Biol Chem 274:25535–25542CrossRefPubMedGoogle Scholar
  29. Schroder HC, Natalio F, Wiens M, Tahir MN, Shukoor MI, Tremel W, Belikov SI, Krasko A, Muller WE (2008) The 2′-5′-oligoadenylate synthetase in the lowest metazoa: isolation, cloning, expression and functional activity in the sponge Lubomirskia baicalensis. Mol Immunol 45:945–953CrossRefPubMedGoogle Scholar
  30. Seth M, Thurlow DL, Hou YM (2002) Poly(C) synthesis by class I and class II CCA-adding enzymes. Biochemistry 41:4521–4532CrossRefPubMedGoogle Scholar
  31. Tatsumi R, Sekiya S, Nakanishi R, Mizutani M, Kojima S, Sokawa Y (2003) Function of ubiquitin-like domain of chicken 2′-5′-oligoadenylate synthetase in conformational stability. J Interferon Cytokine Res 23:667–676CrossRefPubMedGoogle Scholar
  32. Torralba S, Sojat J, Hartmann R (2008) 2′-5′ Oligoadenylate synthetase shares active site architecture with the archaeal CCA-adding enzyme. Cell Mol Life Sci 65:2613–2620CrossRefGoogle Scholar
  33. 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:e101CrossRefPubMedGoogle Scholar
  34. Wiens M, Kuusksalu A, Kelve M, Muller 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 462:12–18CrossRefPubMedGoogle Scholar
  35. Woese C (1998) The universal ancestor. Proc Natl Acad Sci USA 95:6854–6859CrossRefPubMedGoogle Scholar
  36. Yue D, Maizels N, Weiner AM (1996) CCA-adding enzymes and poly(A) polymerases are all members of the same nucleotidyltransferase superfamily: characterization of the CCA-adding enzyme from the archaeal hyperthermophile Sulfolobus shibatae. RNA 2:895–908PubMedGoogle Scholar
  37. Zimmer SL, Fei Z, Stern DB (2008) Genome-based analysis of Chlamydomonas reinhardtii exoribonucleases and poly(A) polymerases predicts unexpected organellar and exosomal features. Genetics 179:125–136CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  • Karina Hansen Kjaer
    • 1
  • Jesper Buchhave Poulsen
    • 1
  • Tõnu Reintamm
    • 2
  • Emilie Saby
    • 3
  • Pia Moeller Martensen
    • 1
  • Merike Kelve
    • 2
  • Just Justesen
    • 1
    • 4
  1. 1.Department of Molecular BiologyUniversity of AarhusAarhusDenmark
  2. 2.Department of Gene TechnologyTallinn University of TechnologyTallinnEstonia
  3. 3.Department of Benthic Ecology and BiodiversityCentre d’Estudis Avancats de Blanes, CSICBlanesSpain
  4. 4.Mads Clausen InstituteUniversity of Southern DenmarkSønderborgDenmark

Personalised recommendations