Expression analysis of the Theileria parva subtelomere-encoded variable secreted protein gene family

PLoS ONE

Volumn 4, Issue 3, 2009, Pages

  Schmuckli Maurer, Jacqueline ^a   Casanova, Carlo ^a,f   Schmied, Stéfanie ^a,g   Affentranger, Sarah ^a,h   Parvanova, Iana ^a   Kang'a, Simon ^b,i   Nene, Vishvanath ^b,j   Katzer, Frank ^c,k   McKeever, Declan ^c,l   Müller, Joachim ^a   Bishop, Richard ^d   Pain, Arnab ^e   Dobbelaere, Dirk A E ^a  

^a UNIVERSITY OF BERN   (Switzerland)

^b J CRAIG VENTER INSTITUTE   (United States)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

^d INTERNATIONAL LIVESTOCK RESEARCH INSTITUTE   (Kenya)

^e WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^f Institute for Infectious Diseases   (Switzerland)

^g UNIVERSITY OF BERN   (Switzerland)

^h S   (Switzerland)

ⁱ NEW YORK UNIVERSITY   (United States)

^j UNIVERSITY OF MARYLAND   (United States)

^k MOREDUN RESEARCH INSTITUTE   (United Kingdom)

^l ROYAL VETERINARY COLLEGE   (United Kingdom)

more..

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; MESSENGER RNA; PROTOZOAL PROTEIN; SUBTELOMERIC VARIABLE SECRETED PROTEIN; UNCLASSIFIED DRUG; PROTOZOAL RNA;

ANIMAL CELL; ARTICLE; B LYMPHOCYTE; CELL LINE; CELL NUCLEUS; CELL TYPE; CONTROLLED STUDY; GENE EXPRESSION REGULATION; GENE TRANSLOCATION; GENOTYPE; HOST CELL; IMMUNOFLUORESCENCE; IN VITRO STUDY; MAMMAL CELL; MICROARRAY ANALYSIS; MOLECULAR CLONING; NONHUMAN; PHENOTYPE; PROTEIN FUNCTION; PROTEIN SECRETION; PROTOZOAL INFECTION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; T LYMPHOCYTE; TELOMERE; THEILERIA PARVA; ANIMAL; CATTLE; CHEMISTRY; GENE EXPRESSION PROFILING; GENETICS; LYMPHOCYTE; PARASITOLOGY; PATHOGENICITY; SECRETION;

BOVINAE; MAMMALIA; PROTOZOA; THEILERIA; THEILERIA PARVA;

ANIMALS; B-LYMPHOCYTES; CATTLE; GENE EXPRESSION PROFILING; LYMPHOCYTES; PROTOZOAN PROTEINS; RNA, PROTOZOAN; T-LYMPHOCYTES; THEILERIA PARVA;

EID: 63449117109     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0004839     Document Type: Article

References (50)

1. Barry JD, Ginger ML, Burton P, McCulloch R (2003) Why are parasite contingency genes often associated with telomeres? International Journal for Parasitology 33: 29-45.
2. Scherf A, Hernandez-Rivas R, Buffet P, Bottius E, Benatar C, et al. (1998) Antigenic variation in malaria: in situ switching, relaxed and mutually exclusive transcription of var genes during intra-erythrocytic development in Plasmodium falciparum. EMBO J 17: 5418-5426.
3. Borst P, Ulbert S (2001) Control of VSG gene expression sites. Mol Biochem Parasitol 114: 17-27.
4. Filler SG (2006) Candida-host cell receptor-ligand interactions. Curr Opin Microbiol 9: 333-339.
5. Gottschling DE, Aparicio OM, Billington BL, Zakian VA (1990) Position effect at S. cerevisiae telomeres: reversible repression of Pol II transcription. Cell 63: 751-762.
6. Merrick CJ, Duraisingh MT (2006) Heterochromatin-mediated control of virulence gene expression. Mol Microbiol 62: 612-620.
7. Shaw MK (2002) Theileria development and host cell invasion. In: Dobbelaere DAE, McKeever DJ, eds. Theileria. Boston: Kluwer Academic Publishers. pp 1-22.
8. Dobbelaere DAE, Heussler VT (1999) Transformation of leukocytes by Theileria parva and T. annulata. Annu Rev Microbiol 53: 1-42.
9. Heussler V, Sturm A, Langsley G (2006) Regulation of host cell survival by intracellular Plasmodium and Theileria parasites. Parasitology 132 Suppl: S49-60.
10. Dobbelaere DA, Kuenzi P (2004) The strategies of the Theileria parasite: a new twist in host-pathogen interactions. Curr Opin Immunol 16: 524-530.
11. Dobbelaere DA, Rottenberg S (2003) Theileria-induced leukocyte transformation. Curr Opin Microbiol 6: 377-382.
12. Shiels B, Langsley G, Weir W, Pain A, McKellar S, et al. (2006) Alteration of host cell phenotype by Theileria annulata and Theileria parva: mining for manipulators in the parasite genomes. Int J Parasitol 36: 9-21.
13. Heussler VT, Stanway RR (2008) Cellular and molecular interactions between the apicomplexan parasites Plasmodium and Theileria and their host cells. Parasite 15: 211-218.
14. Heussler VT, Rottenberg S, Schwab R, Kuenzi P, Fernandez PC, et al. (2002) Hijacking of host cell IKK signalosomes by the transforming parasite Theileria. Science 298: 1033-1036.
15. Shiels BR, McKellar S, Katzer F, Lyons K, Kinnaird J, et al. (2004) A Theileria annulata DNA binding protein localized to the host cell nucleus alters the phenotype of a bovine macrophage cell line. Eukaryot Cell 3: 495-505.
16. Swan DG, Stern R, McKellar S, Phillips K, Oura CA, et al. (2001) Characterisation of a cluster of genes encoding Theileria annulata AT hook DNA-binding proteins and evidence for localisation to the host cell nucleus. J Cell Sci 114: 2747-2754.
17. Ravindran S, Boothroyd JC (2008) Secretion of proteins into host cells by Apicomplexan parasites. Traffic 9: 647-656.
18. McKeever DJ, Morrison WI (1994) Immunity to a parasite that transforms T lymphocytes. Curr Opin Immunol 6: 564-567.
19. Morrison WI, McKeever DJ (2006) Current status of vaccine development against Theileria parasites. Parasitology 133 Suppl: S169-187.
20. Graham SP, Honda Y, Pelle R, Mwangi DM, Glew EJ, et al. (2007) A novel strategy for the identification of antigens that are recognised by bovine MHC class I restricted cytotoxic T cells in a protozoan infection using reverse vaccinology. Immunome Res 3: 2.
21. Graham SP, Pelle R, Honda Y, Mwangi DM, Tonukari NJ, et al. (2006) Theileria parva candidate vaccine antigens recognized by immune bovine cytotoxic T lymphocytes. Proc Natl Acad Sci U S A 103: 3286-3291.
22. Baylis HA, Allsopp BA, Hall R, Carrington M (1993) Characterisation of a glutamine- and proline-rich protein (QP protein) from Theileria parva. Mol Biochem Parasitol 61: 171-178.
23. Toye P, Gobright E, Nyanjui J, Nene V, Bishop R (1995) Structure and sequence variation of the genes encoding the polymorphic, immunodominant molecule (PIM), an antigen of Theileria parva recognized by inhibitory monoclonal antibodies. Mol Biochem Parasitol 73: 165-177.
24. Gardner MJ, Bishop R, Shah T, de Villiers EP, Carlton JM, et al. (2005) Genome sequence of Theileria parva, a bovine pathogen that transforms lymphocytes. Science 309: 134-137.
25. Pain A, Renauld H, Berriman M, Murphy L, Yeats CA, et al. (2005) Genome of the host-cell transforming parasite Theileria annulata compared with T. parva. Science 309: 131-133.
26. Nielsen H, Engelbrecht J, Brunak S, von Heijne G (1997) Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng 10: 1-6.
27. Prilusky J, Felder CE, Zeev-Ben-Mordehai T, Rydberg EH, Man O, et al. (2005) FoldIndex: a simple tool to predict whether a given protein sequence is intrinsically unfolded. Bioinformatics 21: 3435-3438.
28. Bishop R, Shah T, Pelle R, Hoyle D, Pearson T, et al. (2005) Analysis of the transcriptome of the protozoan Theileria parva using MPSS reveals that the majority of genes are transcriptionally active in the schizont stage. Nucleic Acids Res 33: 5503-5511.
29. Brown CG, Stagg DA, Purnell RE, Kanhai GK, Payne RC (1973) Letter: Infection and transformation of bovine lymphoid cells in vitro by infective particles of Theileria parva. Nature 245: 101-103.
30. Katzer F, Ngugi D, Schnier C, Walker AR, McKeever DJ (2007) Influence of host immunity on parasite diversity in Theileria parva. Infect Immun 75: 4909-4916.
31. Katzer F, Ngugi D, Oura C, Bishop RP, Taracha EL, et al. (2006) Extensive genotypic diversity in a recombining population of the apicomplexan parasite Theileria parva. Infect Immun 74: 5456-5464.
32. Volkman SK, Hartl DL, Wirth DF, Nielsen KM, Choi M, et al. (2002) Excess polymorphisms in genes for membrane proteins in Plasmodium falciparum. Science 298: 216-218.
33. Bishop R, Gobright E, Nene V, Morzaria S, Musoke A, et al. (2000) Polymorphic open reading frames encoding secretory proteins are located less than 3 kilobases from Theileria parva telomeres. Mol Biochem Parasitol 110: 359-371.
34. Horton P, Nakai K (1997) Better prediction of protein cellular localization sites with the k nearest neighbors classifier. Proc Int Conf Intell Syst Mol Biol 5: 147-152.
35. Brameier M, Krings A, MacCallum RM (2007) NucPred-predicting nuclear localization of proteins. Bioinformatics 23: 1159-1160.
36. Swan DG, Phillips K, Tait A, Shiels BR (1999) Evidence for localisation of a Theileria parasite AT hook DNA-binding protein to the nucleus of immortalised bovine host cells. Mol Biochem Parasitol 101: 117-129.
37. Swan DG, Stadler L, Okan E, Hoffs M, Katzer F, et al. (2003) TashHN, a Theileria annulata encoded protein transported to the host nucleus displays an association with attenuation of parasite differentiation. Cell Microbiol 5: 947-956.
38. Boisvert FM, van Koningsbruggen S, Navascue's J, Lamond AI (2007) The multifunctional nucleolus. Nat Rev Mol Cell Biol 8: 574-585.
39. Baydoun H, Duc-Dodon M, Lebrun S, Gazzolo L, Bex F (2007) Regulation of the human T-cell leukemia virus gene expression depends on the localization of regulatory proteins Tax, Rex and p30II in specific nuclear subdomains. Gene 386: 191-201.
40. Bevington JM, Needham PG, Verrill KC, Collaco RF, Basrur V, et al. (2007) Adeno-associated virus interactions with B23/Nucleophosmin: identification of sub-nucleolar virion regions. Virology 357: 102-113.
41. Andersen JS, Lam YW, Leung AK, Ong SE, Lyon CE, et al. (2005) Nucleolar proteome dynamics. Nature 433: 77-83.
42. Deitsch KW, Calderwood MS, Wellems TE (2001) Malaria. Cooperative silencing elements in var genes. Nature 412: 875-876.
43. Chookajorn T, Dzikowski R, Frank M, Li F, Jiwani AZ, et al. (2007) Epigenetic memory at malaria virulence genes. Proc Natl Acad Sci U S A 104: 899-902.
44. McKeever DJ (2006) Theileria parva and the bovine CTL response: down but not out? Parasite Immunol 28: 339-345.
45. Serwold T, Gaw S, Shastri N (2001) ER aminopeptidases generate a unique pool of peptides for MHC class I molecules. Nat Immunol 2: 644-651.
46. Oura CA, Odongo DO, Lubega GW, Spooner PR, Tait A, et al. (2003) A panel of microsatellite and minisatellite markers for the characterisation of field isolates of Theileria parva. Int J Parasitol 33: 1641-1653.
47. Dobbelaere DAE, Prospero TD, Roditi IJ, Kelke C, Baumann I, et al. (1990) Expression of Tac antigen component of bovine interleukin-2 receptor in different leukocyte populations infected with Theileria parva or Theileria annulata. Infect Immun 58: 3847-3855.
48. Dudoit S, Gentleman RC, Quackenbush J (2003) Open source software for the analysis of microarray data. Biotechniques Suppl: 45-51.
49. Smyth GK (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: Article3.
50. Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132: 365-386.