Extracellular phosphorylation of C9 by protein kinase CK2 regulates complement-mediated lysis

European Journal of Immunology

Volumn 35, Issue 6, 2005, Pages 1939-1948

  Bohana Kashtan, Osnat ^a   Pinna, Lorenzo A ^b   Fishelson, Zvi ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b UNIVERSITY OF PADOVA   (Italy)

Author keywords

C9; CK2; Complement; Ecto PK; Phosphorylation

Indexed keywords

CASEIN KINASE II; CD59 ANTIGEN; COMPLEMENT COMPONENT C9; DIMETHYL SULFOXIDE; EMODIN; MONOCLONAL ANTIBODY; PROTEIN KINASE INHIBITOR; RITUXIMAB;

ARTICLE; BLOOD CELL; CANCER CELL; CELL DEATH; CONTROLLED STUDY; CYTOLYSIS; ENZYME ACTIVITY; FIBROBLAST; HUMAN; HUMAN CELL; INHIBITION KINETICS; LYMPHOMA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAJI CELL; REGULATORY MECHANISM; WESTERN BLOTTING;

CASEIN KINASE II; COMPLEMENT C9; CYTOTOXICITY, IMMUNOLOGIC; HUMANS; K562 CELLS; PHOSPHORYLATION; PROTEASE INHIBITORS; PROTEIN KINASES;

EID: 20844455649     PISSN: 00142980     EISSN: None     Source Type: Journal    
DOI: 10.1002/eji.200425716     Document Type: Article

References (51)

1. Fishelson, Z., Donin, N., Zell, S., Schultz, S. and Kirschfink, M., Obstacles to cancer immunotherapy: expression of membrane complement regulatory proteins (mCRPs) in tumors. Mol. Immunol. 2003. 40: 109-123.
2. Jurianz, K., Ziegler, S., Donin, N., Reiter, Y., Fishelson, Z. and Kirschfink, M., K562 erythroleukemic cells are equipped with multiple mechanisms of resistance to lysis by complement. Int. J. Cancer 2001. 93: 848-854.
3. Donin, N., Jurianz, K., Ziporen, L., Schultz, S., Kirschfink, M. and Fishelson, Z., Complement resistance of human carcinoma cells depends on membrane regulatory proteins, protein kinases and sialic acid. Clin. Exp. Immunol. 2003. 131: 254-263.
4. Morgan, B. P. and Harris, C. L., Complement Regulatory Proteins. Academic Press, San Diego 1999
5. Frade, R., Rodrigues-Lima, F., Huang, S., Xie, K., Guillaume, N. and Bar-Eli, M., Procathepsin-L, a proteinase that cleaves human C3 (the third component of complement), confers high tumorigenic and metastatic properties to human melanoma cells. Cancer Res. 1998. 58: 2733-2736.
6. Turianskyj, F. H. and Gyenes, L., The effect of neuraminidase on the sensitivity of tumor cells toward lysis by antibody and complement or by sensitized lymphocytes. Transplantation 1976. 22: 24-30.
7. Kraus, S. and Fishelson, Z., Cell desensitization by sublytic C5b-9 complexes and calcium ionophores depends on activation of protein kinase C. Eur. J. Immunol. 2000. 30: 1272-1280.
8. Kraus, S., Seger, R. and Fishelson, Z., Involvement of the ERK mitogen-activated protein kinase in cell resistance to complement-mediated lysis. Clin. Exp. Immunol. 2001. 123: 366-374.
9. Fishelson, Z., Hochman, I., Greene, L. E. and Eisenberg, E., Contribution of heat shock proteins to cell protection from complement-mediated lysis. Int. Immunol. 2001. 13: 983-991.
10. Sreedhar, A. S., Mihaly, K., Pato, B., Schnaider, T., Stetak, A., Kis-Petik, K., Fidy, J., Simonics, T., Maraz, A. and Csermely, P., Hsp90 inhibition accelerates cell lysis. Anti-Hsp90 ribozyme reveals a complex mechanism of Hsp90 inhibitors involving both superoxide- and Hsp90-dependent events. J. Biol. Chem. 2003. 278: 35231-35240.
11. Redegeld, F. A., Caldwell, C. C. and Sitkovsky, M. V., Ecto-protein kinases: ecto-domain phosphorylation as a novel target for pharmacological manipulation? Trends Pharmacol. Sci. 1999. 20: 453-459.
12. Kubler, D., Pyerin, W., Bill, O., Hotz, A., Sonka, J. and Kinzel, V., Evidence for ecto-protein kinase activity that phosphorylates Kemptide in a cyclic AMP-dependent mode. J. Biol. Chem. 1989. 264: 14549-14555.
13. Babinska, A., Hogan, M. V., Sobocki, T., Sobocka, M. B., Ehrlich, Y. H. and Kornecki, E., Identification of ecto-PKC on surface of human platelets: role in maintenance of latent fibrinogen receptors. Am. J. Physiol. Heart Circ. Physiol. 2000. 278: H2008-2019.
14. Walter, J., Schnolzer, M., Pyerin, W., Kinzel, V. and Kubler, D., Induced release of cell surface protein kinase yields CK1- and CK2-like enzymes in tandem. J. Biol. Chem. 1996. 271: 111-119.
15. Teshima, R., Onose, J., Saito, Y., Ikebuchi, H., Kitani, S. and Sawada, J., Casein kinase II-like ectokinase activity on RBL-2H3 cells. Immunol. Lett. 1999. 68: 369-374.
16. Faust, M. and Montenarh, M., Subcellular localization of protein kinase CK2. A key to its function? Cell Tissue Res. 2000. 301: 329-340.
17. Meggio, F. and Pinna, L. A., One-thousand-and-one substrates of protein kinase CK2? FASEB J. 2003. 17: 349-368.
18. Paas, Y. and Fishelson, Z., Shedding of tyrosine and serine/threonine ecto-protein kinases from human leukemic cells. Arch. Biochem. Biophys. 1995. 316: 780-788.
19. Paas, Y., Bohana-Kashtan, O. and Fishelson, Z., Phosphorylation of the complement component, C9, by an ecto-protein kinase of human leukemic cells. Immunopharmacology 1999. 42: 175-185.
20. Hermoso, T., Fishelson, Z., Becker, S. I., Hirschberg, K. and Jaffe, C. L., Leishmanial protein kinases phosphorylate components of the complement system. EMBO J. 1991. 10: 4061-4067.
21. Ekdahl, K. N. and Nilsson, B., Phosphorylation of complement component C3 and C3 fragments by a human platelet protein kinase. Inhibition of factor I-mediated cleavage of C3b. J. Immunol. 1995. 154: 6502-6510.
22. Muller-Eberhard, H. J., The membrane attack complex of complement. Annu. Rev. Immunol. 1986. 4: 503-528.
23. Tschopp, J., Podack, E. R. and Muller-Eberhard, H. J., The membrane attack complex of complement: C5b-8 complex as accelerator of C9 polymerization. J. Immunol. 1985. 134: 495-499.
24. Sarno, S., Reddy, H., Meggio, F., Ruzzene, M., Davies, S. P., Donella-Deana, A., Shugar, D. and Pinna, L. A., Selectivity of 4,5,6,7-tetrabromobenzotriazole, an ATP site-directed inhibitor of protein kinase CK2 ('casein kinase-2′). FEBS Lett. 2001. 496: 44-48.
25. Harjunpaa, A., Junnikkala, S. and Meri, S., Rituximab (anti-CD20) therapy of B cell lymphomas: direct complement killing is superior to cellular effector mechanisms. Scand. J. Immunol. 2000. 51: 634-641.
26. Maloney, D. G., Mechanism of action of rituximab. Anticancer Drugs 2001. 12 Suppl 2: S1-4.
27. Meri, S., Morgan, B. P., Davies, A., Daniels, R. H., Olavesen, M. G., Waldmann, H. and Lachmann, P. J., Human protectin (CD59), an 18,000-20,000 MW complement lysis restricting factor, inhibits C5b-8 catalysed insertion of C9 into lipid bilayers. Immunology 1990. 71: 1-9.
28. Pinna, L. A., Casein kinase 2: an 'eminence grise' in cellular regulation? Biochim. Biophys. Acta 1990. 1054: 267-284.
29. Hathaway, G. M. and Traugh, J. A., Casein kinase II. Methods Enzymol. 1983. 99: 317-331.
30. Gatica, M., Hinrichs, M. V., Jedlicki, A., Allende, C. C. and Allende, J. E., Effect of metal ions on the activity of casein kinase II from Xenopus laevis. FEBS Lett. 1993. 315: 173-177.
31. Antonelli, M., Daniotti, J. L., Rojo, D., Allende, C. C. and Allende, J. E., Cloning, expression and properties of the alpha' subunit of casein kinase 2 from zebrafish (Danio rerio). Eur. J. Biochem. 1996. 241: 272-279.
32. Marin, O., Meggio, F. and Pinna, L. A., Design and synthesis of two new peptide substrates for the specific and sensitive monitoring of casein kinases-1 and -2. Biochem. Biophys. Res. Commun. 1994. 198: 898-905.
33. Meggio, F., Boldyreff, B., Marin, O., Issinger, O. G. and Pinna, L. A., Phosphorylation and activation of protein kinase CK2 by p34cdc2 are independent events. Eur. J. Biochem. 1995. 230: 1025-1031.
34. Ehrlich, Y. H., Hogan, M. V., Pawlowska, Z., Wieraszko, A., Katz, E., Sobocki, T., Babinska, A. and Kornecki, E., Surface protein phosphorylation by ecto-protein kinases. Role in neuronal development and synaptic plasticity. Adv. Exp. Med. Biol. 1998. 446: 51-71.
35. Redegeld, F. A., Smith, P., Apasov, S. and Sitkovsky, M. V., Phosphorylation of T-lymphocyte plasma membrane-associated proteins by ectoprotein kinases: implications for a possible role for ectophosphorylation in T cell effector functions. Biochim. Biophys. Acta 1997. 1328: 151-165.
36. Bhakdi, S. and Tranum-Jensen, J., C5b-9 assembly: average binding of one C9 molecule to C5b-8 without poly-C9 formation generates a stable transmembrane pore. J. Immunol. 1986. 136: 2999-3005.
37. Tschopp, J., Engel, A. and Podack, E. R., Molecular weight of poly(C9). 12 to 18 C9 molecules form the transmembrane channel of complement. J. Biol. Chem. 1984. 259: 1922-1928.
38. DiScipio, R. G., Gehring, M. R., Podack, E. R., Kan, C. C., Hugli, T. E. and Fey, G. H., Nucleotide sequence of cDNA and derived amino acid sequence of human complement component C9. Proc. Natl. Acad. Sci. USA 1984. 81: 7298-7302.
39. Stanley, K. K., Kocher, H. P., Luzio, J. P., Jackson, P. and Tschopp, J., The sequence and topology of human complement component C9. EMBO J. 1985. 4: 375-382.
40. Yamamoto, K. and Migita, S., Mechanisms for the spontaneous formation of covalently linked polymers of the terminal membranolytic complement protein (C9). J. Biol. Chem. 1983. 258: 7887-7889.
41. Hatanaka, M., Seya, T., Inai, S. and Shimizu, A., The functions of the ninth component of human complement are sustained by disulfide bonds with different susceptibilities to reduction. Biochim. Biophys. Acta 1994. 1209: 117-122.
42. Ahmed, K., Gerber, D. A. and Cochet, C., Joining the cell survival squad: an emerging role for protein kinase CK2. Trends Cell Biol. 2002. 12: 226-230.
43. Litchfield, D. W., Protein kinase CK2: structure, regulation and role in cellular decisions of life and death. Biochem. J. 2003. 369: 1-15.
44. Thornburg, W. and Lindell, T. J., Purification of rat liver nuclear protein kinase NII. J. Biol. Chem. 1977. 252: 6660-6665.
45. Filhol, O., Martiel, J. L. and Cochet, C., Protein kinase CK2: a new view of an old molecular complex. EMBO Rep. 2004. 5: 351-355.
46. Meggio, F., Deana, A. D. and Pinna, L. A., Endogenous phosphate acceptor proteins for rat liver cytosolic casein kinases. J. Biol. Chem. 1981. 256: 11958-11961.
47. Szyszka, R., Grankowski, N., Felczak, K. and Shugar, D., Halogenated benzimidazoles and benzotriazoles as selective inhibitors of protein kinases CK I and CK II from Saccharomyces cerevisiae and other sources. Biochem. Biophys. Res. Commun. 1995. 208: 418-424.
48. Schlesinger, M., Nave, Z., Levy, Y., Slater, P. E. and Fishelson, Z., Prevalence of hereditary properdin, C7 and C8 deficiencies in patients with meningococcal infections. Clin. Exp. Immunol. 1990. 81: 423-427.
49. Laemmli, U. K., Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970. 227: 680-685.
50. Glass, D. B., Masaracchia, R. A., Feramisco, J. R. and Kemp, B. E., Isolation of phosphorylated peptides and proteins on ion exchange papers. Anal. Biochem. 1978. 87: 566-575.
51. Towbin, H., Staehelin, T. and Gordon, J., Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA 1979. 76: 4350-4354.