Expressed sequence tag (EST) analysis of the erythrocytic stages of Babesia bovis

Veterinary Parasitology

Volumn 138, Issue 1-2, 2006, Pages 61-74

  de Vries, Erik ^a   Corton, Craig ^b   Harris, Barbara ^b   Cornelissen, Albert W C A ^a   Berriman, Matthew ^b  

^a UTRECHT UNIVERSITY   (Netherlands)

^b WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

Babesia bovis; Erythrocytic stages; Expressed sequence tag (EST)

Indexed keywords

ADENOSINE TRIPHOSPHATASE; GLYCEROL 3 PHOSPHATE DEHYDROGENASE; ISOPRENOID; MEMBRANE ANTIGEN; MEMBRANE PROTEIN; MITOCHONDRIAL PROTEIN; RAP1 PROTEIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE;

ALGORITHM; APICOPLAST; ARTICLE; BABESIA BOVIS; BIOSYNTHESIS; CLUSTER ANALYSIS; CYTOPLASM; ERYTHROCYTE; EVOLUTIONARY HOMOLOGY; EXPRESSED SEQUENCE TAG; GENE EXPRESSION; GENETIC TRANSCRIPTION; MEROZOITE; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMODIUM FALCIPARUM; PSEUDOGENE; RELIABILITY; TOXOPLASMA GONDII;

ANIMALS; ANTIGENS, SURFACE; APICOMPLEXA; BABESIA BOVIS; BABESIOSIS; CLUSTER ANALYSIS; ERYTHROCYTES; EXPRESSED SEQUENCE TAGS; ISRAEL; LIFE CYCLE STAGES; ORGANELLES; PROTOZOAN PROTEINS; PURINES; SEQUENCE ANALYSIS, DNA;

APICOMPLEXA; BABESIA BOVIS; PLASMODIUM FALCIPARUM; TOXOPLASMA GONDII;

EID: 33646351961     PISSN: 03044017     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.vetpar.2006.01.040     Document Type: Article

References (64)

1. Abrahamsen M.S., Templeton T.J., Enomoto S., et al. Complete genome sequence of the apicomplexan Cryptosporidium parvum. Science 304 (2004) 441-445
2. Allred D.R., and Al-Khedery B. Antigenic variation and cytoadhesion in Babesia bovis and Plasmodium falciparum: different logics achieve the same goal. Mol. Biochem. Parasitol. 134 (2004) 27-35
3. Allred D.R., Carlton J.M.R., Satcher R.L., Long J.A., Brown W.C., and Patterson P.A. The ves multigene family of B. bovis encodes components of rapid antigenic variation at the infected erythrocyte surface. Mol. Cell 5 (2000) 153-162
4. Allred D.R., Cinque D.M., Lane T.J., and Ahrens K.P. Antigenic variation of parasite-derived antigens on the surface of Babesia bovis-infected erythrocytes. Infect. Immun. 62 (1994) 91-98
5. Allred D.R., Hines S.A., and Ahrens K.P. Isolate-specific parasite antigens of the Babesia bovis-infected erythrocyte surface. Mol. Biochem. Parasitol. 60 (1993) 121-132
6. Altschul S.F., Gish W., Miller W., Myers E.W., and Lipman D.J. Basic local alignment search tool. J. Mol. Biol. 215 (1990) 403-410
7. Bergman L.W., Kaiser K., Fujioka H., Coppens I., Daly T.M., Fox S., Matuschewski K., Nussenzweig V., and Kappe S.H. Myosin A tail-domain interacting protein (MTIP) localizes to the inner membrane complex of Plasmodium sporozoites. J. Cell Sci. 116 (2003) 39-49
8. Brown W.C., and Palmer G.H. Designing blood-stage vaccines against Babesia bovis and B. bigemina. Parasitol. Today 15 (1999) 275-281
9. Brown W.C., McElwain T.F., Hotzel I., Suarez C.E., and Palmer G.H. Helper T-cell epitopes encoded by the Babesia bigemina rap-1 gene family in the constant and variant domains are conserved among parasite strains. Infect. Immun. 66 (1998) 1561-1569
10. Carret C., Delbecq S., Labesse G., Carcy B., Precigout E., Moubri K., Schetters T.P., and Gorenflot A. Characterization and molecular cloning of an adenosine kinase from Babesia canis rossi. Eur. J. Biochem. 265 (1999) 1015-1021
11. Carrion M., Gomez M.J., Merchante-Schubert R., Dongarra S., and Ayala J.A. mraW, an essential gene at the dcw cluster of Escherichia coli encodes for a cytoplasmic protein with methyltransferase activity. Biochimie 81 (1999) 879-888
12. Carulli J.P., Artinger M., Swain P.M., Root C.D., Chee L., Tulig C., Guerin J., Osborne M., Stein G., Lian J., and Lomedico P.T. High throughput analysis of differential gene expression. J. Cell. Biochem. Suppl. 30 (1998) 286-296
13. Chaudhary K., Darling J.A., Fohl L.M., Sullivan Jr. W.J., Donald R.G., Pfefferkorn E.R., Ullman B., and Roos D.S. Purine salvage pathways in the apicomplexan parasite Toxoplasma gondii. J. Biol. Chem. 279 (2004) 31221-31227
14. Clark I.A., and Jacobson L.S. Do babesiosis and malaria share a common disease process?. Ann. Trop. Med. Parasitol. 92 (1998) 483-488
15. Cowman A.F., Bernard O., Stewart N., and Kemp D.J. Genes of the protozoan parasite Babesia bovis that rearrange to produce RNA species with different sequences. Cell 37 (1984) 653-660
16. Dalrymple B.P. Molecular variation and diversity in candidate vaccine antigens from Babesia. Acta Trop. 53 (1993) 227-238
17. Dalrymple B.P., Peters J.M., Goodger B.V., Bushell G.R., Waltisbuhl D.J., and Wright I.G. Cloning and characterisation of cDNA clones encoding two Babesia bovis proteins with homologous amino- and carboxy-terminal domains. Mol. Biochem. Parasitol. 59 (1993) 181-190
18. Dowling S.C., Perryman L.E., and Jasmer D.P. A Babesia bovis 225 kDa spherical body protein: localization to the cytoplasmic face of infected erythrocytes after merozoite invasion. Infect. Immun. 64 (1996) 2618-2626
19. Escalante A.A., and Ayala F.J. Phylogeny of the malarial genus Plasmodium, derived from rRNA gene sequences. Proc. Natl. Acad. Sci. U.S.A. 91 (1994) 11373-11377
20. Feagin J.E. The 6 kb element of Plasmodium falciparum encodes mitochondrial cytochrome genes. Mol. Biochem. Parasitol. 52 (1992) 145-148
21. Florin-Christensen M., Suarez C.E., Hines S.A., Palmer G.H., Brown W.C., and McElwain T.F. The Babesia bovis merozoite surface antigen 2 locus contains four tandemly arranged and expressed genes encoding immunologically distinct proteins. Infect. Immun. 70 (2002) 3566-3575
22. Foth B.J., Ralph S.A., Tonkin C.J., Struck N.S., Fraunholz M., Roos D.S., Cowman A.F., and McFadden G.I. Dissecting apicoplast targeting in the malaria parasite Plasmodium falciparum. Science 299 (2003) 705-708
23. Franssen F.F., Gaffar F.R., Yatsuda A.P., and De Vries E. Characterization of erythrocyte invasion by Babesia bovis merozoites efficiently released from their host cell after high voltage pulsing. Microb. Infect. 23 (2003) 641-653
24. Gaffar F.R., Yatsuda A.P., Franssen F.F., and De Vries E. Erythrocyte invasion by Babesia bovis merozoites is inhibited by polyclonal antisera directed against peptides derived from a homologue of Plasmodium falciparum apical membrane antigen 1 (AMA-1). Infect. Immun. 72 (2004) 2947-2955
25. Gaffar F.R., Yatsuda A.P., Franssen F.F., and De Vries E. A Babesia bovis merozoite protein with a domain architecture highly similar to the thrombospondin related anonymous protein (TRAP) present in Plasmodium sporozoites. Mol. Biochem. Parasitol. 136 (2004) 25-34
26. Gaffar F.R., Wilschut K., Franssen F.F., and De Vries E. An amino acid substitution in Babesia bovis dihydrofolate reductase-thymidilate synthase is correlated to cross-resistance agains pyrimethamine and WR99210. Mol. Biochem. Parasitol. 133 (2004) 209-219
27. Gardner M.J., Hall N., Fung E., et al. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419 (2002) 498-511
28. Goodger B.V., Waltisbuhl D.J., Wright I.G., and White M. Babesia bovis: analysis of and preliminary vaccination studies with a defined infected erythrocyte membrane binding antigen. Int. J. Parasitol. 22 (1992) 533-535
29. Hausmann A., Netz D.A., Balk J., Pierik A.J., Mühlenhoff U., and Lill R. The eukaryotic P loop NTPase Nbp35: an essential component of the cytosolic and nuclear iron-sulfur protein assembly machinery. Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 3266-3271
30. Hines S.A., Palmer G.H., Brown W.C., McElwain T.F., Suarez C.E., Vidotto O., and Rice-Ficht A.C. Genetic and antigenic characterization of Babesia bovis merozoite spherical body protein Bb-1. Mol. Biochem. Parasitol. 69 (1995) 149-159
31. Jasmer D.P., Reduker D.W., Hines S.A., Perryman L.E., and McGuire T.C. Surface epitope localization and gene structure of a Babesia bovis 44-kilodalton variable merozoite surface antigen. Mol. Biochem. Parasitol. 55 (1992) 75-83
32. Jasmer D.P., Reduker D.W., Perryman L.E., and McGuire T.C. A Babesia bovis 225-kilodalton protein located on the cytoplasmic side of the erythrocyte membrane has sequence similarity with a region of glycogen phosphorylase. Mol. Biochem. Parasitol. 52 (1992) 263-270
33. Kairo A., Fairlamb A.H., Gobright E., and Nene V. A 7.1 kb linear DNA molecule of Theileria parva has scrambled rDNA sequences and open reading frames for mitochondrially encoded proteins. EMBO J. 13 (1994) 898-905
34. Kamiyama T., Niinuma S., Ikeda I., and Matsubara J. Incorporation of [3H]hypoxanthine by short-term cultured Theileria sergenti and its inhibition by drugs. J. Parasitol. 78 (1992) 856-860
35. Kang S., and Metzenberg R.L. Insertional mutagenesis in Neurospora crassa: cloning and molecular analysis of the preg(+) gene controlling the activity of the transcriptional activator NUC-1. Genetics 133 (1993) 193-202
36. Krishna S., Woodrow C., Webb R., Penny J., Takeyasu K., Kimura M., and East J.M. Expression and functional characterization of a Plasmodium falciparum Ca2+-ATPase (PfATP4) belonging to a subclass unique to apicomplexan organisms. J. Biol. Chem. 276 (2001) 10782-10787
37. Krungkai J. The multiple roles of the mitochondrion of the malarial parasite. Parasitology 129 (2004) 511-524
38. Lang-Unnasch N., Reith M.E., Munholland J., and Barta J.R. Plastids are widespread and ancient in parasites of the phylum apicomplexa. Int. J. Parasitol. 28 (1998) 1743-1754
39. Leipe D.D., Wolf Y.I., Koonin E.V., and Aravind L. Classification and evolution of P-loop GTPases and related ATPases. J. Mol. Biol. 317 (2002) 41-72
40. Li L., Brunk B.P., Kissinger J.C., Pape D., Tang K., Cole R.H., Martin J., Wylie T., Dante M., Fogarty S.J., Howe D.K., Liberator P., Diaz C., Anderson J., White M., Jerome M.E., Johnson E.A., Radke J.A., Stoeckert Jr. C.J., Waterston R.H., Clifton S.W., Roos D.S., and Sibley L.D. Gene discovery in the apicomplexa as revealed by EST sequencing and assembly of a comparative gene database. Genome Res. 13 (2003) 443-454
41. Morrison D.A., and Ellis J.T. Effects of nucleotide sequence alignment on phylogeny estimation: a case study of 18S rDNAs of apicomplexa. Mol. Biol. Evol. 14 (1997) 428-481
42. Mosqueda J., McElwain T.F., Stiller D., and Palmer G.H. Babesia bovis merozoite surface antigen 1 and rhoptry-associated protein 1 are expressed in sporozoites, and specific antibodies inhibit sporozoite attachment to erythrocytes. Infect. Immun. 70 (2002) 1599-1603
43. Mosqueda J., Falcon A., Antonio Alvarez J., Alberto Ramos J., Oropeza-Hernandez L.F., and Figueroa J.V. Babesia bigemina sexual stages are induced in vitro and are specifically recognized by antibodies in the midgut of infected Boophilus microplus ticks. Int. J. Parasitol. 34 (2004) 1229-1236
44. Munoz E.T., Bogarad L.D., and Deem M.W. Microarray and EST database estimates of mRNA expression levels differ: the protein length versus expression curve for C. elegans. BMC Genomics 5 (2004) 30-38
45. Nott M., Bagnara A.S., O'Sullivan W.J., and Gero A.M. Purine salvage and metabolism in Babesia bovis. Parasitol. Res. 76 (1990) 207-213
46. Norimine J., Mosqueda J., Suarez C., Palmer G.H., McElwain T.F., Mbassa G., and Brown W.C. Stimulation of T-helper cell gamma interferon and immunoglobulin G responses specific for Babesia bovis rhoptry-associated protein 1 (RAP-1) or a RAP-1 protein lacking the carboxy-terminal repeat region is insufficient to provide protective immunity against virulent B. bovis challenge. Infect. Immun. 71 (2003) 5021-5032
47. O'Connor R.M., Lane T.J., Stroup S.E., and Allred D.R. Characterization of a variant erythrocyte surface antigen (VESA1) expressed by Babesia bovis during antigenic variation. Mol. Biochem. Parasitol. 89 (1997) 259-270
48. O'Connor R.M., and Allred D.R. Selection of Babesia bovis-infected erythrocytes for adhesion to endothelial cells co-selects for altered variant erythrocyte surface antigen isoforms. J. Immunol. 164 (2000) 2037-2045
49. O'Connor R.M., Long J.A., and Allred D.R. Cytoadherence of Babesia bovis infected erythrocytes to bovine capillary endothelial cells provides an in vitro model for sequestration. Infect. Immun. 67 (1999) 3921-3928
50. Rigoulet M., Aguilaniu H., Averet N., Bunoust O., Camougrand N., Grandier-Vazeille X., Larrson C., Pahlman I.L., Manon S., and Gustafsson L. Organization and regulation of the cytosolic NADH metabolism in the yeast Saccharomyces cerevisiae. Mol. Cell Biochem. 256 (2004) 73-81
51. Ruef B.J., Dowling S.C., Conley P.G., Perryman L.E., Brown W.C., Jasmer D.P., and Rice-Ficht A.C. A unique Babesia bovis spherical body protein is conserved among geographic isolates and localizes to the infected erythrocyte membrane. Mol. Biochem. Parasitol. 105 (2000) 1-12
52. Shkap V., Pipano E., McElwain T.F., Herzberg U., Krigel Y., Fish L., and Palmer G.H. Cross-protective immunity induced by Babesia bovis clones with antigenically unrelated variable merozoite surface antigens. Vet. Immunol. Immunopathol. 41 (1994) 367-374
53. Skovrar E., and Downs D.M. Lack of the ApbC or ApbE protein results in a defect in Fe-S cluster metabolism in Salmonella enterica Serovar typhimurium. J. Bacteriol. 185 (2003) 98-106
54. Soldati D., Dubremetz J.F., and Lebrun M. Microneme proteins: structural and functional requirements to promote adhesion and invasion by the apicomplexan parasite Toxoplasma gondii. Int. J. Parasitol. 31 (2001) 1293-1302
55. Striepen B., Pruijssers A.J.P., Huang J., Li C., Gubbels M.J., Umejiego N.N., Hedstrom L., and Kissinger J.C. Gene transfer in the evolution of parasite nucleotide biosynthesis. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 3154-3159
56. Suarez C.E., Florin-Christensen M., Hines S.A., Palmer G.H., Brown W.C., and McElwain T.F. Characterization of allelic variation in the Babesia bovis merozoite surface antigen 1 (MSA-1) locus and identification of a cross-reactive inhibition-sensitive MSA-1 epitope. Infect. Immun. 68 (2000) 6865-6870
57. Suarez C.E., Palmer G.H., Hotzel I., and McElwain T.F. Structure, sequence, and transcriptional analysis of the Babesia bovis rap-1 multigene locus. Mol. Biochem. Parasitol. 93 (1998) 215-224
58. Tetzlaff C.L., Rice-Ficht A.C., Woods V.M., and Brown W.C. Induction of proliferative responses of T cells from Babesia bovis-immune cattle with a recombinant 77-Kilodalton merozoite protein (Bb-1). Infect. Immun. 60 (1992) 644-652
59. Tomley F.M., and Soldati D.S. Mix and match modules: structure and function of microneme proteins in apicomplexan parasites. Trends Parasitol. 17 (2001) 81-88
60. Toye P.G., Metzelaar M.J., Wijngaard P.L., Nene V., Iams K., Roose J., Nyanjui J.K., Gobright E., Musoke A.J., and Clevers H.C. Characterization of the gene encoding the polymorphic immunodominant molecule, a neutralizing antigen of Theileria parva. J. Immunol. 155 (1995) 1370-1381
61. Tripp C.A., Wagner G.G., and Rice-Ficht A.C. Babesia bovis: gene isolation and characterization using a mung bean nuclease-derived expression library. Exp. Parasitol. 69 (1989) 211-225
62. Wilson R.J. Progress with parasite plastids. J. Mol. Biol. 319 (2002) 257-274
63. Wu Z., Liang F., Hong B., Young J.C., Sussman M.R., Harper J.F., and Sze H. An endoplasmic reticulum-bound Ca(2+)/Mn(2+) pump, ECA1, supports plant growth and confers tolerance to Mn(2+) stress. Plant Physiol. 130 (2002) 128-137
64. Yokoyama N., Suthisak B., Hirata H., Matsuo T., Inoue N., Sugimoto C., and Igarashi I. Cellular localization of Babesia bovis merozoite rhoptry-associated protein 1 and its erythrocyte-binding activity. Infect. Immun. 70 (2002) 5822-5826