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Constitutively activated CK2 potentially plays a pivotal role in Theileria-induced lymphocyte transformation

Published online by Cambridge University Press:  11 November 2005

F. DESSAUGE
Affiliation:
Laboratoire de Biologie Cellulaire Comparative des Apicomplexes, UMR 8104 CNRS/U567 INSERM, Département Maladies Infectieuses, Hôpital Cochin – Bâtiment Gustave Roussy, Institut Cochin, 27, rue du Faubourg-Saint-Jacques, 75014 Paris, France Laboratoire d'Immunologie Cellulaire et Tissulaire, INSERM U543, Bâtiment CERVI Groupe Hospitalier Pitié-Salpêtrière, 83, Boulevard de l'Hôpital, 75651 Paris Cedex 13 France
R. LIZUNDIA
Affiliation:
Laboratoire de Biologie Cellulaire Comparative des Apicomplexes, UMR 8104 CNRS/U567 INSERM, Département Maladies Infectieuses, Hôpital Cochin – Bâtiment Gustave Roussy, Institut Cochin, 27, rue du Faubourg-Saint-Jacques, 75014 Paris, France
G. LANGSLEY
Affiliation:
Laboratoire de Biologie Cellulaire Comparative des Apicomplexes, UMR 8104 CNRS/U567 INSERM, Département Maladies Infectieuses, Hôpital Cochin – Bâtiment Gustave Roussy, Institut Cochin, 27, rue du Faubourg-Saint-Jacques, 75014 Paris, France

Abstract

Activation of casein kinase II (CK2) was one of the first observations made on how Theileria parasites manipulate host cell signal transduction pathways and we argue that CK2 induction may in fact contribute to many of the different activation events that have been described since 1993 for Theileria-infected lymphocytes such as sustained activation of transcription factors c-Myc and NF-κB. CK2 also contributes to infected lymphocyte survival by inhibiting caspase activation and is probably behind constitutive PI3-K activation by phosphorylating PTEN. Finally, we also discuss how CK2A may act not only as a kinase, but also as a stimulatory subunit for the protein phosphatase PP2A, so dampening down the MEK/ERK and Akt/PKB pathways and for all these reasons we propose CK2 as a central player in Theileria-induced lymphocyte transformation.

Type
Research Article
Copyright
© 2005 Cambridge University Press

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References

REFERENCES

BARROGA, C. F., STEVENSON, J. F., SCHWARZ, E. M. & VERMA, I. M. ( 1995). Constitutive phosphorylation of I kappa B alpha by casein kinase II. Proceedings of the National Academy of Sciences, USA 92, 76377641.CrossRefGoogle Scholar
BAUMGARTNER, M., CHAUSSEPIED, M., MOREAU, M. F., WERLING, D., DAVIS, W. C., GARCIA, A. & LANGSLEY, G. ( 2000). Constitutive P13-K activity is essential for proliferation, but not survival, of Theileria parva-transformed B cells. Cellular Microbiology 2, 329339.CrossRefGoogle Scholar
BIERMANN, R., SCHNITTGER, L., BEYER, D. & AHMED, J. S. ( 2003). Initiation of translation and cellular localization of Theileria annulata casein kinase IIalpha: implication for its role in host cell transformation. Journal of Cell Physiology 196, 444453.CrossRefGoogle Scholar
CAYLA, X., GARCIA, A., BAUMGARTNER, M., OZON, R. & LANGSLEY, G. ( 2000). A Theileria parva type 1 protein phosphatase activity. Molecular and Biochemical Parasitology 110, 161166.CrossRefGoogle Scholar
CHANNAVAJHALA, P. & SELDIN, D. C. ( 2002). Functional interaction of protein kinase CK2 and c-Myc in lymphomagenesis. Oncogene 21, 52805288.CrossRefGoogle Scholar
CHAUSSEPIED, M., LALLEMAND, D., MOREAU, M. F., ADAMSON, R., HALL, R. & LANGSLEY, G. ( 1998). Upregulation of Jun and Fos family members and permanent JNK activity lead to constitutive AP-1 activitation in Theileria-transformed leukocytes. Molecular and Biochemical Parasitology 94, 215226.CrossRefGoogle Scholar
CHAUSSEPIED, M. & LANGSLEY, G. ( 1996). Theileria transformation of bovine leukocytes: a parasite model for the study of lymphoproliferation. Research in Immunology 147, 127138.CrossRefGoogle Scholar
DANG, C. V., RESAR, L. M., EMISON, E., KIM, S., LI, Q., PRESCOTT, J. E., WONSEY, D. & ZELLER, F. ( 1999). Function of the c-Myc oncogenic transcription factor. Experimental Cell Research 253, 6377.CrossRefGoogle Scholar
DESSAUGE, F., HILALY, S., BAUMGARTNER, M., BLUMEN, B., WERLING, D. & LANGSLEY, G. ( 2005). c-Myc activation by Theileria parasites promotes survival of infected B-lymphocytes. Oncogene, 24, 10751083.CrossRefGoogle Scholar
DI CRISTOFANO, A., KOTSI, P., PENG, Y. F., CORDON-CARDO, C., ELKON, K. B. & PANDOLFI, P. P. ( 1999). Impaired Fas response and autoimmunity in Pten+/− mice. Science 285, 21222125.CrossRefGoogle Scholar
FARAH, M., PARHAR, F., MOUSSAVI, M., EIVEMARK, S. & SALH, B. ( 2003). 5,6-Dichloro-ribifuranosylbenzimidazole- and apigenin-induced sensitization of colon cancer cells to TNF-alpha-mediated apoptosis. American Journal of Physiology Gastrointest Liver Physiology 285, G919928.CrossRefGoogle Scholar
FILHOL, O., MARTIEL, J. L. & COCHET, C. ( 2004). Protein kinase CK2: a new view of an old moolecular complex. EMBO Rep 5, 351355.CrossRefGoogle Scholar
GALLEY, Y., HAGENS, G., GLASER, I., DAVIS, W., EICHHORN, M. & DOBBELAERE, D. ( 1997). Jun NH2-terminal kinase is constitutively activated in T cells transformed by the intracellular parasite Theileria parva. Proceedings of the National Academy of Sciences, USA 94, 51195124.CrossRefGoogle Scholar
GRUMONT, R. J., STRASSER, A. & GERONDAKIS, S. ( 2002). B cell growth is controlled by phosphatidylinosotol 3-kinase-dependent induction of Rel/NF-kappaB regulated c-myc transcription. Molecular Cell 10, 12831294.CrossRefGoogle Scholar
GUERGNON, J., CHAUSSEPIED, M., SOPP, P., LIZUNDIA, R., MOREAU, M. F., BLUMEN, B., WERLING, D., HOWARD, C. J. & LANGSLEY, G. ( 2003 a). A tumour necrosis factor alpha autocrine loop contributes to proliferation and nuclear factor-kappaB activation of Theileria parva-transformed B cells. Cellular Microbiology 5, 709716.Google Scholar
GUERGNON, J., DESSAUGE, F., LANGSLEY, G. & GARCIA, A. ( 2003 b). Apoptosis of Theileria-infected lymphocytes induced upon parasite death involves activation of caspases 9 and 3. Biochimie 85, 771776.Google Scholar
HERICHE, J. F., LEBRIN, F., RABILLOUD, T., LEROY, D., CHAMBAZ, E. M. & GOLDBERG, Y. ( 1997). Regulation of protein phosphatase 2A by direct interaction with casein kinase salpha. Science 276, 952955.CrossRefGoogle Scholar
HEUSSLER, V. T., KUENZI, P., FRAGA, F., SCHWAB, R. A., HEMMINGS, B. A. & DOBBELAERE, D. A. ( 2001). The Akt/PKB pathway is constitutively activated in Theileria-transformed leucocytes, but does not directly control constitutive NF-kappaB activation. Cellular Microbiology 3, 537550.CrossRefGoogle Scholar
HEUSSLER, V. T., MACHADO, J., Jr., FERNANDEZ, P. C., BOTTERON, C., CHEN, C. G., PEARSE, M. J. & DOBBELAERE, D. A. ( 1999). The intracellular parasite Theileria parva protects infected T cells from apoptosis. Proceedings of the National Academy Sciences, USA 96, 73127317.CrossRefGoogle Scholar
HEUSSLER, V. T., ROTTENBERG, S., SCHWAB, R., KUENZI, P., FERNANDEZ, P. C., McKELLAR, S., SHIELS, B., CHEN, Z. J., ORTH, F., WALLACH, D. & DOBBELAERE, D. A. ( 2002). Hijacking of host cell IKK signalosomes by the transforming parasite Theileria. Science 298, 10331036.CrossRefGoogle Scholar
HILGARD, P., CZAJA, M. J., GERKEN, G. & STOCKERT, R. J. ( 2004). Proapoptotic function of protein kinase CK2alpha is mediated by a JNK signaling cascade. American Journal of Physiol Gastrointest Liver Physiol 287, G192201.CrossRefGoogle Scholar
KATO, T., Jr., DELHASE, M., HOFFMANN, A. & KARIN, M. ( 2003). CK2 Is a C-terminal IkappaB kinase responsible for NF-kappaB activation during the UV response. Mol Cell, 12, 829839.CrossRefGoogle Scholar
KREHAN, A., ANSUINI, H., BOCHER, O., GREIN, S., WIRKNER, U. & PYERIN, W. ( 2000). Transcription factors ets1, NF-kappa B, and Sp1 are major determinants of the promoter activity of the human protein kinase CK2alpha gene. Journal of Biological Chemistry 275, 1832718336.CrossRefGoogle Scholar
KRIPPNER-HEIDENREICH, A., TALANIAN, R. V., SEKUL, R., KRAFT, R., THOLE, H., OTTLEBEN, H. & LUSCHER, B. ( 2001). Targeting of the transcription factor Max during apoptosis: phosphorylation-regulated cleavage by caspase-5 at an unusual glutamic acid residue in position P1. Biochemical Journal 358, 705715.CrossRefGoogle Scholar
KUENZI, P., SCHNEIDER, P. & DOBBELAERE, D. A. ( 2003). Theileria parva-transformed T cells show enhanced resistance to Fas/Fas ligand-induced apoptosis. Journal of Immunology 171, 12241231.CrossRefGoogle Scholar
LIU, W., AKHAND, A. A., TAKEDA, F., KAWAMOTO, Y., ITOIGAWA, M., KATO, M., SUZUKI, H., ISHIKAWA, N. & NAKASHIMA, I. ( 2003). Protein phosphatase 2A-linked and-unlinked caspase-dependent pathways for downregulation of Akt kinase triggered by 4-hydroxynonenal. Cell Death and Differentiation 10, 772781.CrossRefGoogle Scholar
MILLER, S. J., LOU, D. Y., SELDIN, D. C., LANE, W. S. & NEEL, B. G. ( 2002). Direct identification of PTEN phosphorylation sites. FEBS Letters 528, 14553.CrossRefGoogle Scholar
NIEFIND, F., GUERRA, B., ERMAKOWA, I. & ISSINGER, O. G. ( 2001). Crystal structure of human protein kinase CK2: insights into basic properties of the CK2 holoenzyme. EMBO Journal 20, 53205331.CrossRefGoogle Scholar
OLE-MOIYOI, O. F. ( 1995). Casein kinase II in theileriosis. Science 267, 834836.CrossRefGoogle Scholar
OLE-MOIYOI, O. F., BROWN, W. C., IAMS, K. P., NAYAR, A., TSUKAMOTO, T. & MACKLIN, M. D. ( 1993). Theileria parva: an intracellular protozoan parasite that induces reversible lymphocyte transformation. EMBO Journal 12, 16211631.Google Scholar
OLE-MOIYOI, O. F., SUGIMOTO, C., CONRAD, P. A. & MACKLIN, M. D. ( 1992). Cloning and characterization of the casein kinase II alpha subunit gene from the lymphocyte-transforming intracellular protozoan parasite. Theileria parva. Biochemistry 31, 61936202.CrossRefGoogle Scholar
PALMER, G. H., MACHADO, J., Jr., FERNANDEZ, P., HEUSSLER, V., PERINAT, T. & DOBBELAERE, D. A. ( 1997). Parasite-mediated nuclear factor kappaB regulation in lymphoproliferation caused by Theileria parva infection. Proceedings of the National Academy Sciences, USA 94, 1252712532.CrossRefGoogle Scholar
PENNER, C. G., WANG, Z. & LITCHFIELD, D. W. ( 1997). Expression and localization of epitope-tagged protein kinase CK2. Journal of Cellular Biochemistry 64, 525537.3.0.CO;2-T>CrossRefGoogle Scholar
RAVI, R. & BEDI, A. ( 2002). Sensitization of tumor cells to Apo2 ligand/TRAIL-induced apoptosis by inhibition of casein kinase II. Cancer Research 62, 41804185.Google Scholar
SAYED, M., KIM, S. O., SALH, B. S., ISSINGER, O. G. & PELECH, S. L. ( 2000). Stress-induced activation of protein kinase CK2 by direct interaction with p38 mitogen-activated protein kinase. Journal of Biological Chemistry 275, 1656916573.CrossRefGoogle Scholar
SELDIN, D. C. & LEDER, P. ( 1995). Casein kinase II alpha transgene-induced murine lymphoma: relation to theileriosis in cattle. Science 267, 894897.CrossRefGoogle Scholar
SHAYAN, P. & AHMED, J. S. ( 1997). Theileria-mediated constitutive expression of the casein kinase II-alpha subunit in bovine lymphoblastroid cells. Parasitology Research 83, 526532.CrossRefGoogle Scholar
SONTAG, E., FEDOROV, S., KAMIBAYASHI, C., ROBBINS, D., COBB, M. & MUMBY, M. ( 1993). The interaction of SV40 small tumor antigen with protein phosphatase 2A stimulates the map kinase pathway and induces cell proliferation. Cell 75, 887897.CrossRefGoogle Scholar
TORRES, J., RODRIGUEZ, J., MYERS, M. P., VALIENTE, M., GRAVES, J. D., TONKS, N. F. & PULIDO, R. ( 2003). Phosphorylation-regulated cleavage of the tumor suppressor PTEN by caspase-3: implications for the control of protein stability and PTEN-protein interactions. Journal of Biological Chemistry 278, 3065230660.CrossRefGoogle Scholar
VAN ANTWERP, D. J. & VERMA, I. M. ( 1996). Signal-induced degradation of I(kappa)B(alpha): association with NF-kappaB and the PEST sequence in I(kappa)B(alpha) are not required. Molecular Cell Biology 16, 60376045.CrossRefGoogle Scholar