A Bovine Lymphosarcoma Cell Line Infected with Theileria annulata Exhibits an Irreversible Reconfiguration of Host Cell Gene Expression

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Kinnaird, Jane H ^a   Weir, William ^a   Durrani, Zeeshan ^a   Pillai, Sreerekha S ^a,b   Baird, Margaret ^a   Shiels, Brian R ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BUPARVAQUONE; NAPHTHOQUINONE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CHROMATIN; CONTROLLED STUDY; DEATH; GENE EXPRESSION; HOST CELL; HOST PARASITE INTERACTION; MICROARRAY ANALYSIS; NONHUMAN; PARASITE VIABILITY; PHENOTYPE; REGULATORY MECHANISM; THEILERIA ANNULATA; TROPICAL THEILERIOSIS; ANIMAL; BOVINE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; LEUKOCYTE; METABOLISM; NONHODGKIN LYMPHOMA; PARASITOLOGY; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE;

BOVINAE; THEILERIA; THEILERIA ANNULATA;

ANIMALS; CATTLE; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; GENE EXPRESSION REGULATION; HOST-PARASITE INTERACTIONS; LEUKOCYTES; LYMPHOMA, NON-HODGKIN; NAPHTHOQUINONES; THEILERIA ANNULATA; TRANSCRIPTION, GENETIC;

EID: 84879489002     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0066833     Document Type: Article

References (82)

1. Dobbelaere D, Heussler V, (1999) Transformation of leukocytes by Theileria parva and T. annulata. AnnuRevMicrobiol 53: 1-42.
2. Irvin AD, Morrison WI (1987) Immunopathology, immunology and immunoprophylaxis of Theileria infections. In: Soulsby EJL, editor. Immune Responses in Parasitic Infections: Immunology, Immunopathology and Immunoprophylaxis vol III Protozoa Baton Rouge, Florida: CRC Press Inc. 223-274.
3. Dobbelaere DA, Roditi IJ, Coquerelle TM, Kelke C, Eichhorn M, et al. (1991) Lymphocytes infected with Theileria parva require both cell-cell contact and growth factor to proliferate. Eur J Immunol 21: 89-95.
4. Guergnon J, Dessauge F, Langsley G, Garcia A, (2003) Apoptosis of Theileria-infected lymphocytes induced upon parasite death involves activation of caspases 9 and 3. Biochimie 85: 771-776.
5. Wang CY, Mayo MW, Korneluk RG, Goeddel DV, Baldwin AS Jr, (1998) NF-kappaB antiapoptosis: induction of TRAF1 and TRAF2 and c-IAP1 and c-IAP2 to suppress caspase-8 activation. Science 281: 1680-1683.
6. 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.
7. Baylis HA, Megson A, Hall R, (1995) Infection with Theileria annulata induces expression of matrix metalloproteinase 9 and transcription factor AP-1 in bovine leucocytes. MolBiochemParasitol 69: 211-222.
8. Lizundia R, Chaussepied M, Huerre M, Werling D, Di Santo JP, et al. (2006) c-Jun NH2-terminal kinase/c-Jun signaling promotes survival and metastasis of B lymphocytes transformed by Theileria. Cancer Res 66: 6105-6110.
9. Chaussepied M, Janski N, Baumgartner M, Lizundia R, Jensen K, et al. (2010) TGF-b2 induction regulates invasiveness of Theileria-transformed leukocytes and disease susceptibility. PLoSPathog 6: e1001197.
10. Baumgartner M, Chaussepied M, Moreau MF, Werling D, Davis WC, et al. (2000) Constitutive PI3-K activity is essential for proliferation, but not survival, of Theileria parva-transformed B cells. Cell Microbiol 2: 329-339.
11. Dessauge F, Hilaly S, Baumgartner M, Blumen B, Werling D, et al. (2005) c-Myc activation by Theileria parasites promotes survival of infected B-lymphocytes. Oncogene 24: 1075-1083.
12. Schmuckli-Maurer J, Casanova C, Schmied S, Affentranger S, Parvanova I, et al. (2009) Expression analysis of the Theileria parva subtelomere-encoded variable secreted protein gene family. PLoSONE 4: e4839.
13. 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. IntJParasitol 36: 9-21.
14. 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. JCell Sci 114: 2747-2754.
15. Oura CA, McKellar S, Swan DG, Okan E, Shiels BR, (2006) Infection of bovine cells by the protozoan parasite Theileria annulata modulates expression of the ISGylation system. Cell Microbiol 8: 276-288.
16. 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. EukaryotCell 3: 495-505.
17. Jensen K, Makins GD, Kaliszewska A, Hulme MJ, Paxton E, et al. (2009) The protozoan parasite Theileria annulata alters the differentiation state of the infected macrophage and suppresses musculoaponeurotic fibrosarcoma oncogene (MAF) transcription factors. Int J Parasitol 39: 1099-1108.
18. Sager H, Davis WC, Dobbelaere DA, Jungi TW, (1997) Macrophage-parasite relationship in theileriosis. Reversible phenotypic and functional dedifferentiation of macrophages infected with Theileria annulata. JLeukocBiol 61: 459-468.
19. Luder CG, Stanway RR, Chaussepied M, Langsley G, Heussler VT, (2009) Intracellular survival of apicomplexan parasites and host cell modification. IntJParasitol 39: 163-173.
20. Jensen K, Paxton E, Waddington D, Talbot R, Darghouth MA, et al. (2008) Differences in the transcriptional responses induced by Theileria annulata infection in bovine monocytes derived from resistant and susceptible cattle breeds. IntJParasitol 38: 313-325.
21. Jensen K, Talbot R, Paxton E, Waddington D, Glass EJ, (2006) Development and validation of a bovine macrophage specific cDNA microarray. BMC Genomics 7: 224.
22. Durrani Z, Weir W, Pillai S, Kinnaird J, Shiels B, (2012) Modulation of activation-associated host cell gene expression by the apicomplexan parasite Theileria annulata. Cell Microbiol 14: 1434-1454.
23. Morzaria SP, Roeder PL, Roberts DH, Chasey D, Drew TW (1982) Characteristics of a continuous suspension cell line derived from a calf with sporadic leukosis. In: Straub OC, editor; 519-528.
24. Shiels BR, McDougall C, Tait A, Brown CG, (1986) Identification of infection-associated antigens in Theileria annulata transformed cells. Parasite Immunol 8: 69-77.
25. Schmuckli-Maurer J, Kinnaird J, Pillai S, Hermann P, McKellar S, et al. (2010) Modulation of NF-kappaB activation in Theileria annulata-infected cloned cell lines is associated with detection of parasite-dependent IKK signalosomes and disruption of the actin cytoskeleton. Cell Microbiol 12: 158-173.
26. Glascodine J, Tetley L, Tait A, Brown D, Shiels B, (1990) Developmental expression of a Theileria annulata merozoite surface antigen. MolBiochemParasitol 40: 105-112.
27. Shiels B, Kinnaird J, McKellar S, Dickson J, Miled LB, et al. (1992) Disruption of synchrony between parasite growth and host cell division is a determinant of differentiation to the merozoite in Theileria annulata. JCell Sci 101 (Pt 1): 99-107.
28. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, et al. (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4: 249-264.
29. Breitling R, Armengaud P, Amtmann A, Herzyk P, (2004) Rank products: a simple, yet powerful, new method to detect differentially regulated genes in replicated microarray experiments. FEBS Lett 573: 83-92.
30. Hong F, Breitling R, (2008) A comparison of meta-analysis methods for detecting differentially expressed genes in microarray experiments. Bioinformatics 24: 374-382.
31. Schnittger L, Katzer F, Biermann R, Shayan P, Boguslawski K, et al. (2002) Characterization of a polymorphic Theileria annulata surface protein (TaSP) closely related to PIM of Theileria parva: implications for use in diagnostic tests and subunit vaccines. MolBiochemParasitol 120: 247-256.
32. McHardy N, Wekesa LS, Hudson AT, Randall AW, (1985) Antitheilerial activity of BW720C (buparvaquone): a comparison with parvaquone. ResVetSci 39: 29-33.
33. Kuenzi P, Schneider P, Dobbelaere DA, (2003) Theileria parva-transformed T cells show enhanced resistance to Fas/Fas ligand-induced apoptosis. J Immunol 171: 1224-1231.
34. Mhadhbi M, Naouach A, Boumiza A, Chaabani MF, Ben Abderazzak S, et al. (2010) In vivo evidence for the resistance of Theileria annulata to buparvaquone. VetParasitol 169: 241-247.
35. Sharifiyazdi H, Namazi F, Oryan A, Shahriari R, Razavi M, (2012) Point mutations in the Theileria annulata cytochrome b gene is associated with buparvaquone treatment failure. Vet Parasitol 187: 431-435.
36. Cock-Rada AM, Medjkane S, Janski N, Yousfi N, Perichon M, et al. (2012) SMYD3 promotes cancer invasion by epigenetic upregulation of the metalloproteinase MMP-9. Cancer Res 72: 810-820.
37. Adamson R, Logan M, Kinnaird J, Langsley G, Hall R, (2000) Loss of matrix metalloproteinase 9 activity in Theileria annulata-attenuated cells is at the transcriptional level and is associated with differentially expressed AP-1 species. MolBiochemParasitol 106: 51-61.
38. Hall R, Ilhan T, Kirvar E, Wilkie G, Preston PM, et al. (1999) Mechanism(s) of attenuation of Theileria annulata vaccine cell lines. TropMedIntHealth 4: A78-A84.
39. Hermey G, (2009) The Vps10p-domain receptor family. Cell Mol Life Sci 66: 2677-2689.
40. Fenner BJ, Scannell M, Prehn JH, (2010) Expanding the substantial interactome of NEMO using protein microarrays. PLoS One 5: e8799.
41. Soligo M, Camperio C, Caristi S, Scotta C, Del Porto P, et al. (2011) CD28 costimulation regulates FOXP3 in a RelA/NF-kappaB-dependent mechanism. Eur J Immunol 41: 503-513.
42. Zhang H, Cowan-Jacob SW, Simonen M, Greenhalf W, Heim J, et al. (2000) Structural basis of BFL-1 for its interaction with BAX and its anti-apoptotic action in mammalian and yeast cells. J Biol Chem 275: 11092-11099.
43. Pouyet L, Roisin-Bouffay C, Clement A, Millet V, Garcia S, et al. (2010) Epithelial vanin-1 controls inflammation-driven carcinogenesis in the colitis-associated colon cancer model. Inflamm Bowel Dis 16: 96-104.
44. Vogler M, (2012) BCL2A1: the underdog in the BCL2 family. Cell Death Differ 19: 67-74.
45. Forget A, Ayrault O, den Besten W, Kuo ML, Sherr CJ, et al. (2008) Differential post-transcriptional regulation of two Ink4 proteins, p18 Ink4c and p19 Ink4d. Cell Cycle 7: 3737-3746.
46. Sherr CJ, Roberts JM, (1999) CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev 13: 1501-1512.
47. Besson A, Dowdy SF, Roberts JM, (2008) CDK inhibitors: cell cycle regulators and beyond. Dev Cell 14: 159-169.
48. Zheng D, Cho YY, Lau AT, Zhang J, Ma WY, et al. (2008) Cyclin-dependent kinase 3-mediated activating transcription factor 1 phosphorylation enhances cell transformation. Cancer Res 68: 7650-7660.
49. Magli MC, Largman C, Lawrence HJ, (1997) Effects of HOX homeobox genes in blood cell differentiation. J Cell Physiol 173: 168-177.
50. Mann RS, Lelli KM, Joshi R, (2009) Hox specificity unique roles for cofactors and collaborators. Curr Top Dev Biol 88: 63-101.
51. Liu J, Wang Y, Birnbaum MJ, Stoffers DA, (2010) Three-amino-acid-loop-extension homeodomain factor Meis3 regulates cell survival via PDK1. Proc Natl Acad Sci U S A 107: 20494-20499.
52. Svingen T, Tonissen KF, (2006) Hox transcription factors and their elusive mammalian gene targets. Heredity (Edinb) 97: 88-96.
53. Marchetti L, Comelli L, D'Innocenzo B, Puzzi L, Luin S, et al. (2010) Homeotic proteins participate in the function of human-DNA replication origins. Nucleic Acids Res 38: 8105-8119.
54. Barber BA, Rastegar M, (2010) Epigenetic control of Hox genes during neurogenesis, development, and disease. Ann Anat 192: 261-274.
55. Hatano SY, Tada M, Kimura H, Yamaguchi S, Kono T, et al. (2005) Pluripotential competence of cells associated with Nanog activity. Mech Dev 122: 67-79.
56. Kashyap V, Rezende NC, Scotland KB, Shaffer SM, Persson JL, et al. (2009) Regulation of stem cell pluripotency and differentiation involves a mutual regulatory circuit of the NANOG, OCT4, and SOX2 pluripotency transcription factors with polycomb repressive complexes and stem cell microRNAs. Stem Cells Dev 18: 1093-1108.
57. Wu X, Ellmann S, Rubin E, Gil M, Jin K, et al. (2012) ADP ribosylation by PARP-1 suppresses HOXB7 transcriptional activity. PLoS One 7: e40644.
58. Malik S, Jiang S, Garee JP, Verdin E, Lee AV, et al. (2010) Histone deacetylase 7 and FoxA1 in estrogen-mediated repression of RPRM. Mol Cell Biol 30: 399-412.
59. Shaulian E, (2010) AP-1- The Jun proteins: Oncogenes or tumor suppressors in disguise? Cell Signal 22: 894-899.
60. Chaussepied M, Lallemand D, Moreau MF, Adamson R, Hall R, et al. (1998) Upregulation of Jun and Fos family members and permanent JNK activity lead to constitutive AP-1 activation in Theileria-transformed leukocytes. MolBiochemParasitol 94: 215-226.
61. Taira T, Maeda J, Onishi T, Kitaura H, Yoshida S, et al. (1998) AMY-1, a novel C-MYC binding protein that stimulates transcription activity of C-MYC. Genes Cells 3: 549-565.
62. Qing G, Xiao G, (2005) Essential role of IkappaB kinase alpha in the constitutive processing of NF-kappaB2 p100. J Biol Chem 280: 9765-9768.
63. Savinova OV, Hoffmann A, Ghosh G, (2009) The Nfkb1 and Nfkb2 proteins p105 and p100 function as the core of high-molecular-weight heterogeneous complexes. Mol Cell 34: 591-602.
64. Machado J Jr, Fernandez PC, Baumann I, Dobbelaere DA, (2000) Characterisation of NF-kappa B complexes in Theileria parva-transformedT cells. Microbes Infect 2: 1311-1320.
65. Kuo TC, Schlissel MS, (2009) Mechanisms controlling expression of the RAG locus during lymphocyte development. Curr Opin Immunol 21: 173-178.
66. He Y, Sun S, Sha H, Liu Z, Yang L, et al. (2010) Emerging roles for XBP1, a sUPeR transcription factor. Gene Expr 15: 13-25.
67. Green CB, Takahashi JS, Bass J, (2008) The meter of metabolism. Cell 134: 728-742.
68. Reisman D, Glaros S, Thompson EA, (2009) The SWI/SNF complex and cancer. Oncogene 28: 1653-1668.
69. Kannan S, Fang W, Song G, Mullighan CG, Hammitt R, et al. (2011) Notch/HES1-mediated PARP1 activation: a cell type-specific mechanism for tumor suppression. Blood 117: 2891-2900.
70. Sang L, Roberts JM, Coller HA, (2010) Hijacking HES1: how tumors co-opt the anti-differentiation strategies of quiescent cells. Trends Mol Med 16: 17-26.
71. Fahraeus R, Paramio JM, Ball KL, Lain S, Lane DP, (1996) Inhibition of pRb phosphorylation and cell-cycle progression by a 20-residue peptide derived from p16CDKN2/INK4A. Curr Biol 6: 84-91.
72. Niture SK, Jain AK, Shelton PM, Jaiswal AK, (2011) Src subfamily kinases regulate nuclear export and degradation of transcription factor Nrf2 to switch off Nrf2-mediated antioxidant activation of cytoprotective gene expression. J Biol Chem 286: 28821-28832.
73. Vousden KH, Prives C, (2009) Blinded by the Light: The Growing Complexity of p53. Cell 137: 413-431.
74. Polager S, Ginsberg D, (2009) p53 and E2f: partners in life and death. Nat Rev Cancer 9: 738-748.
75. Loose M, Swiers G, Patient R, (2007) Transcriptional networks regulating hematopoietic cell fate decisions. Curr Opin Hematol 14: 307-314.
76. Lim CA, Yao F, Wong JJ, George J, Xu H, et al. (2007) Genome-wide mapping of RELA(p65) binding identifies E2F1 as a transcriptional activator recruited by NF-kappaB upon TLR4 activation. Mol Cell 27: 622-635.
77. Quintana AM, Zhou YE, Pena JJ, O'Rourke JP, Ness SA, (2011) Dramatic repositioning of c-Myb to different promoters during the cell cycle observed by combining cell sorting with chromatin immunoprecipitation. PLoS One 6: e17362.
78. Fan J, Zeller K, Chen YC, Watkins T, Barnes KC, et al. (2010) Time-dependent c-Myc transactomes mapped by Array-based nuclear run-on reveal transcriptional modules in human B cells. PLoS One 5: e9691.
79. Kim SK, Fouts AE, Boothroyd JC, (2007) Toxoplasma gondii dysregulates IFN-gamma-inducible gene expression in human fibroblasts: insights from a genome-wide transcriptional profiling. JImmunol 178: 5154-5165.
80. Leng J, Denkers EY, (2009) Toxoplasma gondii inhibits covalent modification of histone H3 at the IL-10 promoter in infected macrophages. PLoSONE 4: e7589.
81. Rosowski EE, Lu D, Julien L, Rodda L, Gaiser RA, et al. (2011) Strain-specific activation of the NF-kappaB pathway by GRA15, a novel Toxoplasma gondii dense granule protein. JExpMed 208: 195-212.
82. Saeij JP, Coller S, Boyle JP, Jerome ME, White MW, et al. (2007) Toxoplasma co-opts host gene expression by injection of a polymorphic kinase homologue. Nature 445: 324-327.