Identification and characterization of a novel calcium-activated apyrase from cryptosporidium parasites and its potential role in pathogenesis

PLoS ONE

Volumn 7, Issue 2, 2012, Pages

  Manque, Patricio A ^a   Woehlbier, Ute ^a   Lara, Ana M ^a   Tenjo, Fernando ^a   Alves, João M ^a   Buck, Gregory A ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APYRASE; CALCIUM ACTIVATED APYRASE; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG; CALCIUM; GUANOSINE DIPHOSPHATE; PROTOZOAL PROTEIN; PROTOZOON ANTIBODY; URIDINE DIPHOSPHATE;

ANIMAL CELL; ARTICLE; CANCER CELL CULTURE; CAPY GENE; CONTROLLED STUDY; CRYPTOSPORIDIOSIS; CRYPTOSPORIDIUM; CRYPTOSPORIDIUM HOMINIS; CRYPTOSPORIDIUM PARVUM; DOSE RESPONSE; ENZYME ACTIVITY; FEMALE; GENE PRODUCT; GENE SEQUENCE; GENETIC IDENTIFICATION; HOST PARASITE INTERACTION; HUMAN; HUMAN CELL; IN VITRO STUDY; MOUSE; NEOSPORA; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYST; PATHOGENESIS; PHYLOGENY; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; SPECIES INVASION; SPOROZOITE; TOXOPLASMA; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; DNA SEQUENCE; DRUG EFFECT; ENZYME ACTIVATION; ENZYME SPECIFICITY; ENZYMOLOGY; EPITHELIUM CELL; GLYCOSYLATION; IMMUNOLOGY; ISOLATION AND PURIFICATION; METABOLISM; MOLECULAR GENETICS; PARASITE; PARASITOLOGY; PHYSIOLOGY; PROTEIN BINDING; PROTEIN REFOLDING; PROTEIN TRANSPORT;

CRYPTOSPORIDIUM; CRYPTOSPORIDIUM PARVUM; HEXAPODA; NEOSPORA; TOXOPLASMA;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES, PROTOZOAN; APYRASE; CALCIUM; CRYPTOSPORIDIOSIS; CRYPTOSPORIDIUM; ENZYME ACTIVATION; EPITHELIAL CELLS; GLYCOSYLATION; GUANOSINE DIPHOSPHATE; HUMANS; MICE; MOLECULAR SEQUENCE DATA; PARASITES; PHYLOGENY; PROTEIN BINDING; PROTEIN REFOLDING; PROTEIN TRANSPORT; PROTOZOAN PROTEINS; RECOMBINANT PROTEINS; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; SPOROZOITES; SUBSTRATE SPECIFICITY; URIDINE DIPHOSPHATE;

EID: 84856695115     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0031030     Document Type: Article

References (56)

1. Goodgame RW, (1996) Understanding intestinal spore-forming protozoa: cryptosporidia, microsporidia, isospora, and cyclospora. Ann Intern Med 124: 429-441.
2. Guerrant RL, (1997) Cryptosporidiosis: an emerging, highly infectious threat. Emerg Infect Dis 3: 51-57.
3. Smith HV, Nichols RA, Grimason AM, (2005) Cryptosporidium excystation and invasion: getting to the guts of the matter. Trends Parasitol 21: 133-142.
4. Mizumoto N, Kumamoto T, Robson SC, Sevigny J, Matsue H, et al. (2002) CD39 is the dominant Langerhans cell-associated ecto-NTPDase: modulatory roles in inflammation and immune responsiveness. Nat Med 8: 358-365.
5. Kohler D, Eckle T, Faigle M, Grenz A, Mittelbronn M, et al. (2007) CD39/ectonucleoside triphosphate diphosphohydrolase 1 provides myocardial protection during cardiac ischemia/reperfusion injury. Circulation 116: 1784-1794.
6. Eltzschig HK, Kohler D, Eckle T, Kong T, Robson SC, et al. (2009) Central role of Sp1-regulated CD39 in hypoxia/ischemia protection. Blood 113: 224-232.
7. Di Virgilio F, Chiozzi P, Ferrari D, Falzoni S, Sanz JM, et al. (2001) Nucleotide receptors: an emerging family of regulatory molecules in blood cells. Blood 97: 587-600.
8. Silverman JA, Qi H, Riehl A, Beckers C, Nakaar V, et al. (1998) Induced activation of the Toxoplasma gondii nucleoside triphosphate hydrolase leads to depletion of host cell ATP levels and rapid exit of intracellular parasites from infected cells. J Biol Chem 273: 12352-12359.
9. Barros FS, De Menezes LF, Pinheiro AA, Silva EF, Lopes AH, et al. (2000) Ectonucleotide diphosphohydrolase activities in Entamoeba histolytica. Arch Biochem Biophys 375: 304-314.
10. Bisaggio DF, Peres-Sampaio CE, Meyer-Fernandes JR, Souto-Padron T, (2003) Ecto-ATPase activity on the surface of Trypanosoma cruzi and its possible role in the parasite-host cell interaction. Parasitol Res 91: 273-282.
11. Sansom FM, Newton HJ, Crikis S, Cianciotto NP, Cowan PJ, et al. (2007) A bacterial ecto-triphosphate diphosphohydrolase similar to human CD39 is essential for intracellular multiplication of Legionella pneumophila. Cell Microbiol 9: 1922-1935.
12. Santos RF, Possa MA, Bastos MS, Guedes PM, Almeida MR, et al. (2009) Influence of Ecto-Nucleoside Triphosphate Diphosphohydrolase Activity on Trypanosoma cruzi Infectivity and Virulence. PLoS Negl Trop Dis 3: e387.
13. Berredo-Pinho M, Peres-Sampaio CE, Chrispim PP, Belmont-Firpo R, Lemos AP, et al. (2001) A Mg-dependent ecto-ATPase in Leishmania amazonensis and its possible role in adenosine acquisition and virulence. Arch Biochem Biophys 391: 16-24.
14. de Souza Leite M, Thomaz R, Fonseca FV, Panizzutti R, Vercesi AE, et al. (2007) Trypanosoma brucei brucei: biochemical characterization of ecto-nucleoside triphosphate diphosphohydrolase activities. Exp Parasitol 115: 315-323.
15. Jesus JB, Lopes AH, Meyer-Fernandes JR, (2002) Characterization of an ecto-ATPase of Tritrichomonas foetus. Vet Parasitol 103: 29-42.
16. Fietto JL, DeMarco R, Nascimento IP, Castro IM, Carvalho TM, et al. (2004) Characterization and immunolocalization of an NTP diphosphohydrolase of Trypanosoma cruzi. Biochem Biophys Res Commun 316: 454-460.
17. Peres-Sampaio CE, Palumbo ST, Meyer-Fernandes JR, (2001) An ecto-ATPase activity present in Leishmania tropica stimulated by dextran sulfate. Z Naturforsch C 56: 820-825.
18. Plesner L, (1995) Ecto-ATPases: identities and functions. Int Rev Cytol 158: 141-214.
19. Steinberg TH, Di Virgilio F, (1991) Cell-mediated cytotoxicity: ATP as an effector and the role of target cells. Curr Opin Immunol 3: 71-75.
20. Filippini A, Taffs RE, Agui T, Sitkovsky MV, (1990) Ecto-ATPase activity in cytolytic T-lymphocytes. Protection from the cytolytic effects of extracellular ATP. J Biol Chem 265: 334-340.
21. Margolis RN, Schell MJ, Taylor SI, Hubbard AL, (1990) Hepatocyte plasma membrane ECTO-ATPase (pp120/HA4) is a substrate for tyrosine kinase activity of the insulin receptor. Biochem Biophys Res Commun 166: 562-566.
22. Najjar SM, Accili D, Philippe N, Jernberg J, Margolis R, et al. (1993) pp120/ecto-ATPase, an endogenous substrate of the insulin receptor tyrosine kinase, is expressed as two variably spliced isoforms. J Biol Chem 268: 1201-1206.
23. Dubyak GR, el-Moatassim C, (1993) Signal transduction via P2-purinergic receptors for extracellular ATP and other nucleotides. Am J Physiol 265: C577-606.
24. Clifford EE, Martin KA, Dalal P, Thomas R, Dubyak GR, (1997) Stage-specific expression of P2Y receptors, ecto-apyrase, and ecto-5′-nucleotidase in myeloid leukocytes. Am J Physiol 273: C973-987.
25. Knowles AF, (1995) The rat liver ecto-ATPase/C-CAM cDNA detects induction of carcinoembryonic antigen but not the mercurial-insensitive ecto-ATPase in human hepatoma Li-7A cells treated by epidermal growth factor and cholera toxin. Biochem Biophys Res Commun 207: 529-535.
26. Stout JG, Strobel RS, Kirley TL, (1995) Properties of and proteins associated with the extracellular ATPase of chicken gizzard smooth muscle. A monoclonal antibody study. J Biol Chem 270: 11845-11850.
27. Kirley TL, (1997) Complementary DNA cloning and sequencing of the chicken muscle ecto-ATPase. Homology with the lymphoid cell activation antigen CD39. J Biol Chem 272: 1076-1081.
28. Roberto Meyer-Fernandes J, (2002) Ecto-ATPases in protozoa parasites: looking for a function. Parasitol Int 51: 299-303.
29. Maliszewski CR, Delespesse GJ, Schoenborn MA, Armitage RJ, Fanslow WC, et al. (1994) The CD39 lymphoid cell activation antigen. Molecular cloning and structural characterization. J Immunol 153: 3574-3583.
30. Wang TF, Guidotti G, (1998) Widespread expression of ecto-apyrase (CD39) in the central nervous system. Brain Res 790: 318-322.
31. Valenzuela JG, Charlab R, Galperin MY, Ribeiro JM, (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: 30583-30590.
32. Uccelletti D, Pascoli A, Farina F, Alberti A, Mancini P, et al. (2008) APY-1, a novel Caenorhabditis elegans apyrase involved in unfolded protein response signalling and stress responses. Mol Biol Cell 19: 1337-1345.
33. Valenzuela JG, Belkaid Y, Rowton E, Ribeiro JM, (2001) The salivary apyrase of the blood-sucking sand fly Phlebotomus papatasi belongs to the novel Cimex family of apyrases. J Exp Biol 204: 229-237.
34. Smith TM, Hicks-Berger CA, Kim S, Kirley TL, (2002) Cloning, expression, and characterization of a soluble calcium-activated nucleotidase, a human enzyme belonging to a new family of extracellular nucleotidases. Arch Biochem Biophys 406: 105-115.
35. Devader C, Webb RJ, Thomas GM, Dale L, (2006) Xenopus apyrase (xapy), a secreted nucleotidase that is expressed during early development. Gene 367: 135-141.
36. Charlab R, Valenzuela JG, Rowton ED, Ribeiro JM, (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: 15155-15160.
37. Failer BU, Braun N, Zimmermann H, (2002) Cloning, expression, and functional characterization of a Ca(2+)-dependent endoplasmic reticulum nucleoside diphosphatase. J Biol Chem 277: 36978-36986.
38. Murphy DM, Ivanenkov VV, Kirley TL, (2003) Bacterial expression and characterization of a novel, soluble, calcium-binding, and calcium-activated human nucleotidase. Biochemistry 42: 2412-2421.
39. Joe A, Verdon R, Tzipori S, Keusch GT, Ward HD, (1998) Attachment of Cryptosporidium parvum sporozoites to human intestinal epithelial cells. Infect Immun 66: 3429-3432.
40. Manque PM, Eichinger D, Juliano MA, Juliano L, Araya JE, et al. (2000) Characterization of the cell adhesion site of Trypanosoma cruzi metacyclic stage surface glycoprotein gp82. Infect Immun 68: 478-484.
41. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
42. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948.
43. Guindon S, Gascuel O, (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696-704.
44. Hillis DM, Moritz C, Mable BK, (1996) Molecular systematics Sunderland, Mass. Sinauer Associates pp. xvi, 655.
45. Keane TM, Creevey CJ, Pentony MM, Naughton TJ, McLnerney JO, (2006) Assessment of methods for amino acid matrix selection and their use on empirical data shows that ad hoc assumptions for choice of matrix are not justified. BMC Evol Biol 6: 29.
46. Xu P, Widmer G, Wang Y, Ozaki LS, Alves JM, et al. (2004) The genome of Cryptosporidium hominis. Nature 431: 1107-1112.
47. Abrahamsen MS, Templeton TJ, Enomoto S, Abrahante JE, Zhu G, et al. (2004) Complete genome sequence of the apicomplexan, Cryptosporidium parvum. Science 304: 441-445.
48. Manque PA, Tenjo F, Woehlbier U, Lara AM, Serrano MG, et al. (2011) Identification and immunological characterization of three potential vaccinogens against Cryptosporidium. Clin Vaccine Immunol.
49. Keeling PJ, Burger G, Durnford DG, Lang BF, Lee RW, et al. (2005) The tree of eukaryotes. Trends Ecol Evol 20: 670-676.
50. Cavalier-Smith T, (2003) The excavate protozoan phyla Metamonada Grasse emend. (Anaeromonadea, Parabasalia, Carpediemonas, Eopharyngia) and Loukozoa emend. (Jakobea, Malawimonas): their evolutionary affinities and new higher taxa. Int J Syst Evol Microbiol 53: 1741-1758.
51. Sansom FM, Robson SC, Hartland EL, (2008) Possible effects of microbial ecto-nucleoside triphosphate diphosphohydrolases on host-pathogen interactions. Microbiol Mol Biol Rev 72: 765-781, Table of Contents.
52. Pinheiro CM, Martins-Duarte ES, Ferraro RB, Fonseca de Souza AL, Gomes MT, et al. (2006) Leishmania amazonensis: Biological and biochemical characterization of ecto-nucleoside triphosphate diphosphohydrolase activities. Exp Parasitol 114: 16-25.
53. Laurent F, Eckmann L, Savidge TC, Morgan G, Theodos C, et al. (1997) Cryptosporidium parvum infection of human intestinal epithelial cells induces the polarized secretion of C-X-C chemokines. Infect Immun 65: 5067-5073.
54. Laurent F, McCole D, Eckmann L, Kagnoff MF, (1999) Pathogenesis of Cryptosporidium parvum infection. Microbes Infect 1: 141-148.
55. Luttikhuizen DT, Harmsen MC, de Leij LF, van Luyn MJ, (2004) Expression of P2 receptors at sites of chronic inflammation. Cell Tissue Res 317: 289-298.
56. Dai J, Liu J, Deng Y, Smith TM, Lu M, (2004) Structure and protein design of a human platelet function inhibitor. Cell 116: 649-659.