Molecular cloning and expression analysis of a Cryptosporidium parvum gene encoding a new member of the thrombospondin family

Molecular and Biochemical Parasitology

Volumn 92, Issue 1, 1998, Pages 147-162

  Spano, Furio ^a   Putignani, Lorenza ^a   Naitza, Silvia ^b   Puri, Claudia ^a   Wright, Steve ^c   Crisanti, Andrea ^b  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c MOREDUN RESEARCH INSTITUTE   (United Kingdom)

Author keywords

Apical complex; cDNA; Cryptosporidium parvum; Cryptosporidium wrairi; Sporozoite; Sulfatide binding domain; TRAP C1

Indexed keywords

COMPLEMENTARY DNA; THROMBOSPONDIN;

ARTICLE; CRYPTOSPORIDIUM PARVUM; DNA SEQUENCE; GENE EXPRESSION; MOLECULAR CLONING; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SPOROZOITE;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CELL COMPARTMENTATION; CRYPTOSPORIDIUM; CRYPTOSPORIDIUM PARVUM; GENE LIBRARY; GENES, PROTOZOAN; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; POLYMORPHISM, GENETIC; PROTOZOAN PROTEINS; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, AMINO ACID; SPECIES SPECIFICITY; THROMBOSPONDINS;

EID: 0032054344     PISSN: 01666851     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0166-6851(97)00243-0     Document Type: Article

References (50)

1. [1] Current WL, Garcia LS. Cryptosporidiosis. Clin Microbiol Rev 1991;4:325-58.
2. [2] O'Donoghue PJ. Cryptosporidium and cryptosporidiosis in man and animals. Int J Parasitol 1995;25:139-95.
3. [3] Martins CAP, Guerrant RL. Cryptosporidium and cryptosporidiosis. Parasitol Today 1995;11:434-6.
4. [4] Casemore DP. Epidemiological aspects of human cryptosporidiosis. Epidemiol Infect 1990;104:1-28.
5. [5] Molbak K, Andersen M, Aaby P, Hojlyng N, Jakobsen M, Sodemann M, da Silva AP. Cryptosporidium infection in infancy as a cause of malnutrition: a community study from Guinea-Bissau, west Africa. Am J Clin Nutr 1997;65:149-52.
6. [6] Petersen C. Cryptosporidiosis in patients infected with the human immunodeficiency virus. Clin Infect Dis 1992;15:903-9.
7. [7] Chobotar B, Scholtyseck E. Ultrastructure. In: Long PL, editor. The Biology of the Coccidia. London: E. Arnold, 1992:101-65.
8. [8] Tomley FM, Clarke LE, Kawazoe U, Dijkema R, Kok JJ. Sequence of the gene encoding an immunodominant microneme protein of Eimeria tenella. Mol Biochem Parasitol 1991;49:277-88.
9. [9] Robson KJH, Hall JRS, Jennings MW, Harris TJR, Marsh K, Newbold CI, Tate VE, Weatherall DJ. A highly conserved amino-acid sequence in thrombospondin, properdin and in proteins from sporozoites and blood stages of a human malaria parasite. Nature 1988;335:79-82.
10. [10] Rogers WO, Rogers MD, Hedsrtom RC, Hoffman SL. Characterization of the gene encoding sporozoite surface protein 2, a protective Plasmodium yoelii sporozoite antigen. Mol Biochem Parasitol 1992;53:45-52.
11. [11] Wan K-L, Carruthers VB, Sibley LD, Ajioka JW. Molecular characterization of an expressed sequence tag locus of Toxoplasma gondii encoding the micronemal protein MIC2. Mol Biochem Parasitol 1997;84:203-14.
12. [12] Lawler J, Hynes RO. The structure of the human thrombospondin, an adhesive glycoprotein with multiple calcium-binding sites and homologies with several different proteins. J Cell Biol 1986;103:1635-48.
13. [13] Trottein F, Triglia T, Cowman AF. Molecular cloning of a gene from Plasmodium falciparum that codes for a protein sharing motifs found in adhesive molecules from mammals and Plasmodia. Mol Biochem Parasitol 1995;74:129-41.
14. [14] Dame JD, Williams JL, McCutchan TF, Weber JL, Wirtz RA, Hockmeyer WT, Maloy WL, Haynes JD, Schneider I, Roberts DD, Sanders GS, Reddy EP, Diggs CL, Miller LH. Structure of the gene encoding the immunodominant surface antigen on the sporozoite of the human malaria parasite Plasmodium falciparum. Science 1984;225:593-9.
15. [15] Müller H-M, Reckmann I, Hollingdale MR, Bujard H, Robson KJH, Crisanti A. Thrombospondin related anonymous protein (TRAP) of Plasmodium falciparum binds specifically to sulfated glycoconjugates and to HepG2 hepatoma cells suggesting a role for this molecule in sporozoite invasion of hepatocytes. EMBO J 1993;12:2881-9.
16. [16] Robson KJH, Frevert U, Reckmann I, Cowan G, Beier J, Scragg IG, Takehara K, Bishop DHL, Pradel G, Sinden RE, Saccheo S, Müller H-M, Crisanti A. Thrombospondin-related anonymous protein (TRAP) of Plasmodium falciparum: Expression during sporozoite ontogeny and binding to hepatocytes. EMBO J 1995;14:3883-94.
17. [17] Frevert U, Sinnis P, Cerami C, Shreffler W, Takacs B, Nussenzweig V. Malaria circumsporozoite protein binds to heparan sulfate proteoglycans associated with the surface membrane of hepatocytes. J Exp Med 1993;177:1287-98.
18. [18] Sinnis P, Clavijo P, Fenyö D, Chait BT, Cerami C, Nussenzweig V. Structural and functional properties of region II-plus of the malaria circumsporozoite protein. J Exp Med 1994;180:297-306.
19. [19] Spaccapelo R, Naitza S, Robson KJH, Crisanti A. Thrombospondin-related adhesive protein (TRAP) of Plasmodium berghei and parasite motility. The Lancet 1997;350:335.
20. [20] Sultan AA, Thathy V, Frevert U, Robson KJH, Crisanti A, Nussenzweig V, Nussenzweig R, Ménard R. TRAP is necessary for gliding, motility and infectivity of Plasmodium berghei. Cell 1997;90:511-22.
21. [21] Carruthers VB, Sibley LD. Sequential protein secretion from three distinct organelles of Toxoplasma gondii accompanies invasion of human fibroblasts. Eur J Cell Biol 1997;73:114-23.
22. [22] Chrisp CE, Reid WC, Rush HG, Suckow MA, Bush A, Thomann MJ. Cryptosporidiosis in guinea pigs: an animal model. Infect Immun 1990;58:674-9.
23. [23] Ranucci L, Müller H-M, La Rosa G, Reckmann I, Gomez Morales M A, Spano F, Pozio E, Crisanti A. Characterization and immunolocalization of a Cryptosporidium protein containing repeated amino acids motifs. Infect Immun 1993;61:2347-56.
24. [24] Chomezynsky P, Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocynate-phenol-chloroform extraction. Anal Biochem 1987;162:156-9.
25. [25] Crowe J, Dobeli H, Gentz R, Hochuli E, Stuber D, Henco K. 6 x His-Ni-NTA chromatography as a superior technique in recombinant protein expression/purification. Methods Mol Biol 1994;31:371-8.
26. [26] Devereux J, Haeberli P, Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acid Res 1984;12:387-95.
27. [27] Pasamontes L, Hug D, Hümbelin M, Weber G. Sequence of a major Eimeria maxima antigen homologous to the Eimeria tenella microneme protein Etp100. Mol Biochem Parasitol 1993;57:171-4.
28. [28] Kozak M. The scanning model for translation: an update. J Cell Biol 1989;108:229-41.
29. [29] Wickens M. How the messanger got its tail: addition of poly(A) in the nucleus. Trends Biochem Sci 1990;15:277-81.
30. [30] Kozak M. An analysis of 5′-noncoding sequences from 699 vertebrate messanger RNAs. Nucleic Acid Res 1987;15:8125-32.
31. [31] von Heijne G. A new method for predicting signal sequence cleavage sites. Nucleic Acid Res 1986;14:4683-90.
32. [32] Kyte J, Doolittle RF. A simple method for displaying the hydrophathic character of a protein. J Mol Biol 1982;157:105-32.
33. [33] Kuno K, Kanada N, Nakashima E, Fujiki F, Ichimura F, Matsushima K. Molecular cloning of a gene encoding a new type of metalloproteinase-disintergrin family protein with thrombospondin motifs as inflammation associated gene. J Biol Chem 1997;272:556-62.
34. [34] Gobron S, Monneire H, Meiniel R, Creveaux I, Lehmann W, Lamalle D, Dastugue B, Meiniel A. SCO-spondin: a new member of the thrombospondin family secreted by the subcommissural organ is a candidate in the modulation of neuronal aggregation. J Cell Sci 1996;109:1053-61.
35. [35] Adams RH, Betz H, Puschel AW. A novel class of murine semaphorins with homology to thrombospondin is differentially expressed during early embryogenesis. Mech Dev 1996;57:33-45.
36. [36] Goundis D, Reid KB. Properdin, the terminal complement components, thrombospondin and the circumsporozoite protein of malaria parasites contain similar sequence motifs. Nature 1988;335:62-5.
37. [37] Klar A, Baldassare M, Jessell TM. F-spondin: a gene expressed at high levels in the floor plate encodes a secreted protein that promotes neural cell adhesion and neurite extension. Cell 1992;69:95-110.
38. [38] Leung-Hagesteijn C, Spence AM, Stern BD, Zhou Y, Su M, Hedgecock EM, Culotti JG. UNC-5, a transmembrane protein with immunoglobulin and thrombospondin type I domains, guides cell and pioneer axon migration in C. elegans. Cell 1992;71:289-99.
39. [39] Rich KA, George IV FW, Law JL, Martin JM. Cell-adhesive motif in region II of malarial circumsporozoite protein. Science 1990;249:1574-7.
40. [40] Cosman D, Lyman SD, Idzerda RL, Beckmann MP, Park LS, Goodwin RG, March CJ. A new cytokine receptor superfamily. Trends Biochem Sci 1990;15:265-70.
41. [41] Clarke LE, Tomley FM, Wisher MH, Foulds IJ, Boursnell MEG. Regions of an Eimeria tenella antigen contain sequences which are conserved in circumsporozoite proteins from Plasmodium spp. and which are related to the thrombospondin gene family. Mol Biochem Parasitol 1990;41:269-80.
42. [42] Achbarou A, Mercereau-Puijalon O, Autheman JM, Fortier B, Camus D, Dubremetz JF. Characterization of microneme proteins of Toxoplasma gondii. Mol Biochem Parasitol 1991;47:223-34.
43. [43] Lee J-O, Rieu P, Arnaout MA, Liddington R. Crystal structure of the A domain from the α subunit of integrin CR3 (CD11b/CD18). Cell 1995;80:631-8.
44. [44] Robson KJH, Naitza S, Barker G, Sinden RE, Crisanti A. Cloning and expression of the thrombospondin related adhesive protein gene of Plasmodium berghei. Mol Biochem Parasitol 1997;84:1-12.
45. [45] Templeton TJ, Kaslow DC. Cloning and cross-species comparison of the thrombospondin-related anonymous protein (TRAP) gene from Plasmodium knowlesi, Plasmodium vivax and Plasmodium gallinaceum. Mol Biochem Parasitol 1997;84:13-24.
46. [46] Eschenbacher K-H, Klein H, Sommer I, Meyer HE, Entzeroth R, Mehlhorn H, Rüger W. Characterization of cDNA clones encoding a major microneme antigen of Sarcocystis muris (Apicomplexa) cyst merozoites. Mol Biochem Parasitol 1993;62:27-36.
47. [47] Chrisp CE, Suckow MA, Payer R, Arrowood MJ, Healey MC, Sterling CR. Comparison of the host ranges and antigenicity of Cryptosporidium parvum and Cryptosporidium wrairi from guinea pigs. J Protozool 1992;39:406-9.
48. [48] Tilley M, Upton SJ, Chrisp CE. A comparative study on the biology of Cryptosporidium sp. from guinea pigs and Cryptosporidium parvum (Apicomplexa). Can J Microbiol 1991;37:949-52.
49. [49] Robson KJH, Hall JRS, Ceri Davies L, Crisanti A, Hill AVS, Wellems TE. Polymorphism of the TRAP gene of Plasmodium falciparum. Proc R Soc Lond B 1990;242:205-16.
50. [50] Spano F, Putignani L, McLauchlin J, Casemore DP, Crisanti A. PCR-RFLP analysis of the Cryptosporidium oocyst wall protein (COWP) gene discriminates between C. wrairi and C. parvum, and between C. parvum isolates of human and animal origin. FEMS Microbiol Lett 1997;150:209-17.