CoChat
Sign Up
Cited by 31Parasitic Diseases Research and TreatmentBiochemical and Molecular ResearchAdenosine and Purinergic Signaling

The DOI matches its Crossref record.

A nucleotidase with unique catalytic properties is secreted by Trichinella spiralis

Gounaris, Kleoniki, Selkirk, Murray E., Sadeghi, Sheila J.·2004·Molecular and Biochemical Parasitology
DOI 10.1016/j.molbiopara.2004.04.008
Open this paper in CoChat — free account

Abstract

We have isolated and expressed a cDNA from the parasitic nematode Trichinella spiralis encoding a novel secreted nucleotidase which catalyses the hydrolysis of nucleoside 5'-diphosphates and 5'-monophosphates, but not 5'-triphosphates. The full length cDNA encodes a protein of 550 amino acids with an N-terminal signal peptide, but lacking a C-terminal signature sequence for addition of a glycosyl phosphatidylinositol (GPI) anchor. Expression in Pichia pastoris resulted in the secretion of an active enzyme with the catalytic properties of both a Mg2+-dependent diphosphohydrolase/apyrase and a 5'-nucleotidase. The protein sequence is homologous to 5'-nucleotidases from a wide variety of organisms but contains no sequences specifically conserved in apyrases, suggesting that it is a representative of a new class of secreted nucleotidase. The enzyme was essentially monospecific for AMP among the nucleoside 5'-monophosphates and catalysed the hydrolysis of nucleoside 5'-diphosphates in the order of UDP >> ADP. The diphosphatase activity was dependent on the presence of magnesium ions and a reducing agent, while the 5'-nucleotidase activity was enhanced by these additions. Kinetic analyses indicated that the enzyme exhibits allosteric behaviour. Determination of the number of active sites suggested that catalysis of the two different reactions occurs at the same active site. The data are discussed in terms of regulation of host purinergic signalling during infection.

Overview

Integrity signals

Registry

Crossref · 10.1016/j.molbiopara.2004.04.008

Cites

Statistics

Recomputing p-values needs the paper’s full text.

Verification

Claims the paper makes

We couldn’t retrieve this paper’s full text, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Citations

Cites

No references could be resolved yet.

Research works printed but not linked: 35

  1. Ralevic, 1998, Receptors for purines and pyrimidines, Pharmacol. Rev, 50, 413
  2. Zimmermann, 2000, Extracellular metabolism of ATP and other nucleotides, Naunyn Schmiedebergs Arch. Pharmacol, 362, 299, 10.1007/s002100000309 · DOI
  3. Handa, 1996, Purification and cloning of a soluble ATP-diphosphohydrolase (apyrase) from potato tubers (Solanum tuberosum), Biochem. Biophys. Res. Commun, 218, 916, 10.1006/bbrc.1996.0162 · DOI
  4. Schulte am Esch, 1999, Structural elements and limited proteolysis of CD39 influence ATP diphosphohydrolase activity, Biochemistry, 38, 2248, 10.1021/bi982426k · DOI
  5. Mulero, 1999, CD39-L4 is a secreted human apyrase, specific for the hydrolysis of nucleoside diphosphates, J. Biol. Chem, 274, 20064, 10.1074/jbc.274.29.20064 · DOI
  6. Yeung, 2000, CD39L2, a gene encoding a human nucleoside diphosphatase, predominantly expressed in the heart, Biochemistry, 39, 12916, 10.1021/bi000959z · DOI
  7. Valenzuela, 1998, Purification, cloning, and expression of an apyrase from the bed bug Cimex lectularius. A new type of nucleotide-binding enzyme, J. Biol. Chem, 273, 30583, 10.1074/jbc.273.46.30583 · DOI
  8. Failer, 2002, Cloning, expression, and functional characterization of a Ca(2+)-dependent endoplasmic reticulum nucleoside diphosphatase, J. Biol. Chem, 277, 36978, 10.1074/jbc.M201656200 · DOI
  9. Smith, 2002, Cloning, expression, and characterization of a soluble calcium-activated nucleotidase, a human enzyme belonging åto a new family of extracellular nucleotidases, Arch Biochem. Biophys, 406, 105, 10.1016/S0003-9861(02)00420-4 · DOI
  10. Champagne, 1995, The salivary gland-specific apyrase of the mosquito Aedes aegypti is a member of the 5′-nucleotidase family, Proc. Natl. Acad. Sci. U.S.A, 92, 694, 10.1073/pnas.92.3.694 · DOI
  11. Zimmermann, 1992, 5′-Nucleotidase: molecular structure and functional aspects, Biochem. J, 285, 345, 10.1042/bj2850345 · DOI
  12. Charlab, 1999, Toward an understanding of the biochemical and pharmacological complexity of the saliva of a hematophagous sand fly Lutzomyia longipalpis, Proc. Natl. Acad. Sci. U.S.A, 96, 15155, 10.1073/pnas.96.26.15155 · DOI
  13. Gounaris, 2002, Nucleotidase cascades Are catalyzed by secreted proteins of the parasitic nematode Trichinella spiralis, Infect. Immun, 70, 4917, 10.1128/IAI.70.9.4917-4924.2002 · DOI
  14. Gounaris, 1996, Structural organisation and lipid composition of the epicuticular accessory layer of infective larvae of Trichinella spiralis, Biochim. Biophys. Acta, 1281, 91, 10.1016/0005-2736(96)00022-3 · DOI
  15. Chevillard, 1993, The competition plot: a simple test of whether two reactions occur at the same active site, Biochem. J, 289, 599, 10.1042/bj2890599 · DOI
  16. Misumi, 1990, Primary structure of rat liver 5′-nucleotidase deduced from the cDNA. Presence of the COOH-terminal hydrophobic domain for possible post-translational modification by glycophospholipid, J. Biol. Chem, 265, 2178, 10.1016/S0021-9258(19)39958-2 · DOI
  17. Murphy, 2003, Bacterial expression and characterization of a novel, soluble, calcium-binding, and calcium-activated human nucleotidase, Biochemistry, 42, 2412, 10.1021/bi026763b · DOI
  18. Grinthal, 2000, Substitution of His59 converts CD39 apyrase into an ADPase in a quaternary structure dependent manner, Biochemistry, 39, 9, 10.1021/bi991751k · DOI
  19. Asai, 1983, A potent nucleoside triphosphate hydrolase from the parasitic protozoan Toxoplasma gondii. Purification, some properties, and activation by thiol compounds, J. Biol. Chem, 258, 6816, 10.1016/S0021-9258(18)32295-6 · DOI
  20. Di Virgilio, 2001, Nucleotide receptors: an emerging family of regulatory molecules in blood cells, Blood, 97, 587, 10.1182/blood.V97.3.587 · DOI
  21. Linden, 2001, Molecular approach to adenosine receptors: receptor-mediated mechanisms of tissue protection, Annu. Rev. Pharmacol. Toxicol, 41, 775, 10.1146/annurev.pharmtox.41.1.775 · DOI
  22. Somers, 1998, Expression of the P2Y6 purinergic receptor in human T cells infiltrating inflammatory bowel disease, Lab. Invest, 78, 1375
  23. Warny, 2001, P2Y6 nucleotide receptor mediates monocyte interleukin-8 production in response to UDP or lipopolysaccharide, J. Biol. Chem, 276, 26051, 10.1074/jbc.M102568200 · DOI
  24. Kottgen, 2003, P2Y6 receptor mediates colonic NaCl secretion via differential activation of cAMP-mediated transport, J. Clin Invest, 111, 371, 10.1172/JCI200316711 · DOI
  25. Gounaris, 2001, Secreted variant of nucleoside diphosphate kinase from the intracellular parasitic nematode Trichinella spiralis, Infect Immun, 69, 3658, 10.1128/IAI.69.6.3658-3662.2001 · DOI
  26. Kim, 1996, Nucleotide-induced mucin release from primary hamster tracheal surface epithelial cells involves the P2u purinoceptor, Eur. Respir. J, 9, 542, 10.1183/09031936.96.09030542 · DOI
  27. Robaye, 2003, Loss of nucleotide regulation of epithelial chloride transport in the jejunum of P2Y4-null mice, Mol. Pharmacol, 63, 777, 10.1124/mol.63.4.777 · DOI
  28. Synnestvedt, 2002, Ecto-5’-nucleotidase (CD73) regulation by hypoxia-inducible factor-1 mediates permeability changes in intestinal epithelia, J. Clin Invest, 110, 993, 10.1172/JCI0215337 · DOI · Paper page
  29. Spychala, 2000, Tumor-promoting functions of adenosine, Pharmacol. Ther, 87, 161, 10.1016/S0163-7258(00)00053-X · DOI
  30. Birk, 2002, Role of extracellular ATP metabolism in regulation of platelet reactivity, J. Lab. Clin Med, 140, 166, 10.1067/mlc.2002.126719 · DOI
  31. Le Moine, 1996, Adenosine enhances IL-10 secretion by human monocytes, J. Immunol, 156, 4408, 10.4049/jimmunol.156.11.4408 · DOI
  32. Fenster, 2000, Activation of adenosine A2 alpha receptors inhibits mast cell degranulation and mast cell-dependent vasoconstriction, Microcirculation, 7, 129
  33. Majumdar, 2003, Adenosine suppresses activation of nuclear factor-kappaB selectively induced by tumor necrosis factor in different cell types, Oncogene, 22, 1206, 10.1038/sj.onc.1206184 · DOI
  34. Hasko, 2000, Adenosine inhibits IL-12 and TNF-a production via adenosine A2a receptor-dependent and independent mechanisms, FASEB J, 14, 2065, 10.1096/fj.99-0508com · DOI
  35. Panther, 2003, Adenosine affects expression of membrane molecules, cytokine and chemokine release, and the T-cell stimulatory capacity of human dendritic cells, Blood, 101, 3985, 10.1182/blood-2002-07-2113 · DOI

Cited by

Sorted by citations

See all 31

Metadata

Authors
Gounaris, K., Selkirk, M. E., & Sadeghi, S. J.
Affiliations
  • Imperial College London (GB)
  • University of California, San Francisco (US)
Corresponding author
Gounaris, Kleoniki
ORCID
Venue
Molecular and Biochemical Parasitology
Publisher
Elsevier BV
Published
2004-08
Volume
136
Issue
2
Pages
257-264
ISSN
0166-6851 (ISSN-L)
DOI
10.1016/j.molbiopara.2004.04.008
OpenAlex
W2043601993
Cited by
31
References
0
Citations by year
2022: 1 · 2021: 1 · 2019: 1 · 2018: 2 · 2016: 3 · 2015: 2 · 2014: 3 · 2012: 3
FWCI
0.99
Type
journal article
Language
en
Open access
closed
Licence
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations
  • Molecular and Biochemical Parasitology (publishedVersion)
  • PubMed (publishedVersion)
Funders
Wellcome Trust
Topics
  • Health Sciences › Medicine › Infectious Diseases › Parasitic Diseases Research and Treatment
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Biochemical and Molecular Research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Physiology › Adenosine and Purinergic Signaling
Keywords
Trichinella spiralis, 5'-nucleotidase, apyrase, AMP hydrolysis, magnesium-dependent enzyme, allosteric regulation, single active site, Pichia pastoris expression, signal peptide
MeSH terms
Amino Acid Sequence, Animals, Base Sequence, Catalysis, Cloning, Molecular, Kinetics, Molecular Sequence Data, Pichia, Recombinant Proteins, 5'-Nucleotidase, Gene Expression, Trichinella spiralis, Genes, Helminth, Sequence Homology, Amino Acid, DNA, Complementary, DNA, Helminth

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review