Hijacking of Host Cell Signaling by Theileria

Protein Phosphorylation in Parasites: Novel Targets for Antiparasitic Intervention

Volumn , Issue , 2013, Pages 181-197

  Woods, Kerry ^a   von Schubert, Conrad ^b   Dobbelaere, Dirk ^a  

^a UNIVERSITY OF BERN   (Switzerland)

^b UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 85017342187     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/9783527675401.ch09     Document Type: Chapter

References (64)

1. Shiels, B., Langsley, G., Weir, W., Pain, A., McKellar, S., and Dobbelaere, D. (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.
2. Baumgartner, M. (2011) Enforcing host cell polarity: an apicomplexan parasite strategy towards dissemination. Curr. Opin. Microbiol., 14, 436-444.
3. Dobbelaere, D. and Baumgartner, M. (2009) Theileria, in Intracellular Niches of Microbes: A Pathogens Guide Through the Host Cell (eds U.E. Schaible and A. Haas), Wiley-VCH, pp. 613-632.
4. Shaw, M.K. (2003) Cell invasion by Theileria sporozoites. Trends Parasitol., 19, 2-6.
5. Sinkovics, J.G. (2012) Molecular biology of oncogenic inflammatory processes. I. Non-oncogenic and oncogenic pathogens, intrinsic inflammatory reactions without pathogens, and microRNA/DNA interactions. Int. J. Oncol., 40, 305-349.
6. Durrani, Z., Weir, W., Pillai, S., Kinnaird, J., and Shiels, B. (2012) Modulation of activation-associated host cell gene expression by the apicomplexan parasite Theileria annulata. Cell. Microbiol., 14 (9), 1434-1454.
7. Dyer, M., Hall, R., Shiels, B., and Tait, A. (1992) Theileria annulata: alterations in phosphoprotein and protein kinase activity profiles of infected leukocytes of the bovine host, Bos taurus. Exp. Parasitol., 74, 216227.
8. ole-MoiYoi, O.K., Brown, W.C., Iams, K.P., Nayar, A., Tsukamoto, T., and Macklin, M.D. (1993) Evidence for the induction ofcasein kinase II in bovine lymphocytes transformed by the intracellular protozoan parasite Theileria parva. EMBO J., 12, 16211631.
9. Gardner, M.J., Bishop, R., Shah, T., de Villiers, E.P., Carlton, J.M., Hall, N., Ren, Q., Paulsen, I.T., Pain, A., Berriman, M., Wilson, R.J., Sato, S., Ralph, S.A., Mann, D. J., Xiong, Z., Shallom, S.J., Weidman, J., Jiang, L., Lynn, J., Weaver, B., Shoaibi, A., Domingo, A.R., Wasawo, D., Crabtree, J., Wortman, J.R., Haas, B., Angiuoli, S.V., Creasy, T.H., Lu, C., Suh, B., Silva, J.C., Utterback, T.R., Feldblyum, T.V., Pertea, M., Allen, J., Nierman, W.C., Taracha, E.L., Salzberg, S.L., White, O.R., Fitzhugh, H.A., Morzaria, S., Venter, J.C., Fraser, C.M., and Nene, V. (2005) Genome sequence of Theileria parva, a bovine pathogen that transforms lymphocytes. Science, 309, 134-137.
10. Pain, A., Renauld, H., Berriman, M., Murphy, L., Yeats, C.A., Weir, W., Kerhornou, A., Aslett, M., Bishop, R., Bouchier, C., Cochet, M., Coulson, R.M., Cronin, A., de Villiers, E.P., Fraser, A., Fosker, N., Gardner, M., Goble, A., Griffiths-Jones, S., Harris, D.E., Katzer, F., Larke, N., Lord, A., Maser, P., McKellar, S., Mooney, P., Morton, F., Nene, V., O'Neil, S., Price, C., Quail, M.A., Rabbinowitsch, E., Rawlings, N.D., Rutter, S., Saunders, D., Seeger, K., Shah, T., Squares, R., Squares, S., Tivey, A., Walker, A.R., Woodward, J., Dobbelaere, D.A., Langsley, G., Rajandream, M.A., McKeever, D., Shiels, B., Tait, A., Barrell, B., and Hall, N. (2005) Genome of the host-cell transforming parasite Theileria annulata compared with T. parva. Science, 309, 131-133.
11. Peixoto, L., Chen, F., Harb, O.S., Davis, P. H., Beiting, D.P., Brownback, C.S., Ouloguem, D., and Roos, D.S. (2010) Integrative genomic approaches highlight a family of parasite-specific kinases that regulate host responses. Cell Host Microbe, 8, 208-218.
12. Dessauge, F., Hilaly, S., Baumgartner, M., Blumen, B., Werling, D., and Langsley, G. (2005) c-Myc activation by Theileria parasites promotes survival of infected B-lymphocytes. Oncogene, 24, 1075-1083.
13. Kuenzi, P., Schneider, P., and Dobbelaere, D.A. (2003) Theileria parva-transformed T cells show enhanced resistance to Fas/Fas ligand-induced apoptosis. J. Immunol., 171, 1224-1231.
14. Guergnon, J., Chaussepied, M., Sopp, P., Lizundia, R., Moreau, M.F., Blumen, B., Werling, D., Howard, C.J., and Langsley, G. (2003) A tumour necrosis factor alpha autocrine loop contributes to proliferation and nuclear factor-kB activation of Theileria parva-transformed B cells. Cell. Microbiol., 5, 709-716.
15. Heussler, V., Sturm, A., and Langsley, G. (2006) Regulation of host cell survival by intracellular Plasmodium and Theileria parasites. Parasitology, 132 (Suppl.), S49-S50.
16. Perkins, N.D. (2012) The diverse and complex roles of NF-kB subunits in cancer. Nat. Rev. Cancer, 12, 121-132.
17. Heussler, V.T., Machado, J. Jr, Fernandez, P. C., Botteron, C., Chen, C.G., Pearse, M.J., and Dobbelaere, D.A. (1999) The intracellular parasite Theileria parva protects infected Tcells from apoptosis. Proc. Natl Acad. Sci. USA, 96, 7312-7317.
18. Heussler, V.T., Rottenberg, S., Schwab, R., Kuenzi, P., Fernandez, P.C., McKellar, S., Shiels, B., Chen, Z.J., Orth, K., Wallach, D., and Dobbelaere, D.A. (2002) Hijacking of host cell IKK signalosomes by the transforming parasite Theileria. Science, 298, 1033-1036.
19. Hermann, P. and Dobbelaere, D.A. (2006) Theileria-induced constitutive IKK activation is independent of functional Hsp90. FEBS Lett., 580, 5023-5028.
20. Schmuckli-Maurer, J., Kinnaird, J., Pillai, S., Hermann, P., McKellar, S., Weir, W., Dobbelaere, D., and Shiels, B. (2010) Modulation of NF-kB activation in Theileria annulata-infected cloned cell lines is associated with detection of parasitedependent IKK signalosomes and disruption of the actin cytoskeleton. Cell. Microbiol., 12, 158-173.
21. Hayashida, K., Hattori, M., Nakao, R., Tanaka, Y., Kim, J.Y., Inoue, N., Nene, V., and Sugimoto, C. (2010) A schizont-derived protein, TpSCOP, is involved in the activation of NF-kappaB in Theileria parva-infected lymphocytes. Mol. Biochem. Parasitol., 174, 8-17.
22. Dessauge, F., Lizundia, R., and Langsley, G. (2005) Constitutively activated CK2 potentially plays a pivotal role in Theileria-induced lymphocyte transformation. Parasitology, 130 (Suppl.), S37-S44.
23. Seldin, D.C. and Leder, P. (1995) Casein kinase II alpha transgene-induced murine lymphoma: relation to theileriosis in cattle. Science, 267, 894-897.
24. Shayan, P. and Ahmed, J.S. (1997) Theileria-mediated constitutive expression of the casein kinase II-alpha subunit in bovine lymphoblastoid cells. Parasitol. Res., 83, 526-532.
25. Meyer, N. and Penn, L.Z. (2008) Reflecting on 25 years with MYC. Nat. Rev. Cancer, 8, 976-990.
26. Dessauge, F., Lizundia, R., Baumgartner, M., Chaussepied, M., and Langsley, G. (2005) Taking the Myc is bad for Theileria. Trends Parasitol., 21, 377-385.
27. Channavajhala, P. and Seldin, D.C. (2002) Functional interaction ofprotein kinase CK2 and c-Myc in lymphomagenesis. Oncogene, 21, 5280-5288.
28. Galley, Y., Hagens, G., Glaser, I., Davis, W., Eichhorn, M., and Dobbelaere, D. (1997) Jun NH2-terminal kinase is constitutively activated in Tcells transformed by the intracellular parasite Theileria parva. Proc. Natl Acad. Sci. USA, 94, 5119-5124.
29. Botteron, C. and Dobbelaere, D. (1998) AP-1 and ATF-2 are constitutively activated via the JNK pathway in Theileria parva-transformed T-cells. Biochem. Biophys. Res. Commun., 246, 418-421.
30. Chaussepied, M., Lallemand, D., Moreau, M.F., Adamson, R., Hall, R., and Langsley, G. (1998) Upregulation of Jun and Fos family members and permanent JNK activity lead to constitutive AP-1 activation in Theileria-transformed leukocytes. Mol. Biochem. Parasitol., 94, 215-226.
31. Seitzer, U., Schnittger, L., Boguslawski, K., and Ahmed, J.S. (2006) Investigation of MAP kinase activation in Theileria-infected cell lines. Ann. N. Y. Acad. Sci., 1081, 473-475.
32. Baumgartner, M., Chaussepied, M., Moreau, M.F., Werling, D., Davis, W.C., Garcia, A., and Langsley, G. (2000) Constitutive PI3-K activity is essential for proliferation, but not survival, ofTheileria parva-transformed B cells. Cell. Microbiol., 2, 329-339.
33. Baumgartner, M., Angelisova, P., Setterblad, N., Mooney, N., Werling, D., Horejsi, V., and Langsley, G. (2003) Constitutive exclusion ofCsk from Hck-positive membrane microdomains permits Src kinase-dependent proliferation of Theileria-transformed B lymphocytes. Blood, 101, 1874-1881.
34. Ameyar, M., Wisniewska, M., and Weitzman, J.B. (2003) A role for AP-1 in apoptosis: the case for and against. Biochimie, 85, 747-752.
35. Lizundia, R., Chaussepied, M., Huerre, M., Werling, D., Di Santo, J.P., and Langsley, G. (2006) c-Jun NH2-terminal kinase/c-Jun signaling promotes survival and metastasis ofB lymphocytes transformed by Theileria. Cancer Res., 66, 6105-6110.
36. Seavey, M.M. and Dobrzanski, P. (2012) The many faces of Janus kinase. Biochem. Pharmacol., 83, 1136-1145.
37. Guergnon, J., Dessauge, F., Traincard, F., Cayla, X., Rebollo, A., Bost, P.E., Langsley, G., and Garcia, A. (2006) A PKA survival pathway inhibited by DPT-PKI, a new specific cell permeable PKA inhibitor, is induced by T. annulata in parasitized B-lymphocytes. Apoptosis, 11, 1263-1273.
38. Courtney, K.D., Corcoran, R.B., and Engelman, J.A. (2010) The PI3K pathway as drug target in human cancer. J. Clin. Oncol., 28, 1075-1083.
39. Dobbelaere, D.A., Fernandez, P.C., and Heussler, V.T. (2000) Theileria parva: taking control ofhost cell proliferation and survival mechanisms. Cell. Microbiol., 2, 91-99.
40. Heussler, V.T., Kuenzi, P., Fraga, F., Schwab, R.A., Hemmings, B.A., and Dobbelaere, D.A. (2001) The Akt/PKB pathway is constitutively activated in Theileria-transformed leucocytes, but does not directly control constitutive NF-kB activation. Cell. Microbiol., 3, 537-550.
41. Baumgartner, M., Chaussepied, M., Raposo, G., Goud, B., and Langsley, G. (2005) Accelerated recycling of transferrin receptor in Theileria-transformed B cells. Cell. Microbiol., 7, 637-644.
42. Beard, P., Offord, E., Paduwat, N., and Bruggmann, H. (1991) SV40 activates transcription from the transferrin receptor promoter by inducing a factor which binds to the CRE/AP-1 recognition sequence. Nucleic Acids Res., 19, 7117-7123.
43. Lizundia, R., Chaussepied, M., Naissant, B., Masse, G.X., Quevillon, E., Michel, F., Monier, S., Weitzman, J.B., and Langsley, G. (2007) The JNK/AP-1 pathway upregulates expression of the recycling endosome rab11a gene in B cells transformed by Theileria. Cell. Microbiol., 9, 1936-1945.
44. Bai, D., Ueno, L., and Vogt, P.K. (2009) Aktmediated regulation of NF-kB and the essentialness of NF-kB for the oncogenicity of PI3Kand Akt. Int. J. Cancer, 125, 2863-2870.
45. Fich, C., Klauenberg, U., Fleischer, B., and Broker, B.M. (1998) Modulation of enzymatic activity of Src-family kinases in bovine Tcells transformed by Theileria parva. Parasitology, 117 (Pt 2), 107-115.
46. Eichhorn, M. and Dobbelaere, D.A. (1994) Induction of signal transduction pathways in lymphocytes infected by Theileria parva. Parasitol. Today, 10, 469-472.
47. Baumgartner, M. (2011) Theileria annulata promotes Src kinase-dependent host cell polarization by manipulating actin dynamics in podosomes and lamellipodia. Cell. Microbiol., 13, 538-553.
48. Linder, S. (2007) The matrix corroded: podosomes and invadopodia in extracellular matrix degradation. Trends Cell Biol., 17, 107-117.
49. Chaussepied, M., Janski, N., Baumgartner, M., Lizundia, R., Jensen, K., Weir, W., Shiels, B.R., Weitzman, J.B., Glass, E.J., Werling, D., and Langsley, G. (2010) TGF-b2 induction regulates invasiveness of Theileria-transformed leukocytes and disease susceptibility. PLoS Pathog., 6, e1001197.
50. Adamson, R., Logan, M., Kinnaird, J., Langsley, G., and 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. Mol. Biochem. Parasitol., 106, 51-61.
51. Nigg, E.A. (2001) Mitotic kinases as regulators ofcell division and its checkpoints. Nat. Rev. Mol. Cell Biol., 2, 21-32.
52. Irvin, A.D., Ocama, J.G., and Spooner, P.R. (1982) Cycle ofbovine lymphoblastoid cells parasitised by Theileria parva. Res. Vet. Sci., 33, 298-304.
53. von Schubert, C., Xue, G., Schmuckli-Maurer, J., Woods, K.L., Nigg, E.A., and Dobbelaere, D.A. (2010) The transforming parasite Theileria co-opts host cell mitotic and central spindles to persist in continuously dividing cells. PLoS Biol., 8, e1000499.
54. Yuan, J., Sanhaji, M., Kramer, A., Reindl, W., Hofmann, M., Kreis, N.N., Zimmer, B., Berg, T., and Strebhardt, K. (2011) Polo-box domain inhibitor poloxin activates the spindle assembly checkpoint and inhibits tumor growth in vivo. Am. J. Pathol., 179, 2091-2099.
55. Elia, A.E., Cantley, L.C., and Yaffe, M.B. (2003) Proteomic screen finds pSer/pThr-binding domain localizing Plk1 to mitotic substrates. Science, 299, 1228-1231.
56. Yuan, K., Huang, Y., and Yao, X. (2011) Illumination ofmitotic orchestra during cell division: a Polo view. Cell. Signal., 23, 1-5.
57. Neef, R., Gruneberg, U., Kopajtich, R., Li, X., Nigg, E.A., Sillje, H., and Barr, F.A. (2007) Choice ofPlk1 docking partners during mitosis and cytokinesis is controlled by the activation state ofCdk1. Nat. Cell Biol., 9, 436-444.
58. Zhao, W.M. and Fang, G. (2005) MgcRacGAP controls the assembly of the contractile ring and the initiation of cytokinesis. Proc. Natl Acad. Sci. USA, 102, 13158-13163.
59. Dyer, M.D., Murali, T.M., and Sobral, B.W. (2008) The landscape of human proteins interacting with viruses and other pathogens. PLoS Pathog., 4, e32.
60. Molestina, R.E., Payne, T.M., Coppens, I., and Sinai, A.P. (2003) Activation of NF-kappaB by Toxoplasma gondii correlates with increased expression of antiapoptotic genes and localization of phosphorylated IkappaB to the parasitophorous vacuole membrane. J. Cell Sci., 116, 4359-4371.
61. Payne, T.M., Molestina, R.E., and Sinai, A.P. (2003) Inhibition ofcaspase activation and a requirement for NF-kBfunctioninthe Toxoplasma gondii-mediated blockade of host apoptosis. J. Cell Sci., 116, 4345-4358.
62. Molestina, R.E. and Sinai, A.P. (2005) Detection of a novel parasite kinase activity at the Toxoplasma gondii parasitophorous vacuole membrane capable of phosphorylating host IkappaBalpha. Cell. Microbiol., 7, 351-362.
63. Bagneris, C., Ageichik, A.V., Cronin, N., Wallace, B., Collins, M., Boshoff, C., Waksman, G., and Barrett, T. (2008) Crystal structure of a vFlip-IKKy complex: insights into viral activation of the IKK signalosome. Mol. Cell, 30, 620-631.
64. Matsuoka, M. and Jeang, K.T. (2007) Human T-cell leukaemia virus type 1 (HTLV-1) infectivity and cellular transformation. Nat. Rev. Cancer, 7, 270-280.