Anaplasma phagocytophilum AnkA secreted by type IV secretion system is tyrosine phosphorylated by Abl-1 to facilitate infection

Cellular Microbiology

Volumn 9, Issue 11, 2007, Pages 2644-2657

  Lin, Mingqun ^a   den Dulk Ras, Amke ^b   Hooykaas, Paul J J ^b   Rikihisa, Yasuko ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b LEIDEN UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ABELSON KINASE; ADAPTOR PROTEIN; ANKA PROTEIN; BACTERIAL PROTEIN; CRE RECOMBINASE; IMATINIB; MONOCLONAL ANTIBODY; PROTEIN TYROSINE KINASE; SMALL INTERFERING RNA; TYROSINE; UNCLASSIFIED DRUG;

ALPHAPROTEOBACTERIA; ANAPLASMA PHAGOCYTOPHILUM; ANAPLASMOSIS; ANTIBACTERIAL ACTIVITY; ARTICLE; CELL STRAIN HL 60; CENTRIFUGATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOPLASM; ENZYME ASSAY; GRANULOCYTE; HOST CELL; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; INHIBITION KINETICS; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; PROTEIN TRANSPORT; PROTEOMICS; SIGNAL TRANSDUCTION; TWO HYBRID SYSTEM;

ANAPLASMA PHAGOCYTOPHILUM; BACTERIAL PROTEINS; EHRLICHIOSIS; HL-60 CELLS; HUMANS; IMMUNOPRECIPITATION; MICROSCOPY, CONFOCAL; MOLECULAR WEIGHT; PHOSPHORYLATION; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS C-ABL; TWO-HYBRID SYSTEM TECHNIQUES; TYROSINE;

AGROBACTERIUM TUMEFACIENS; ALPHAPROTEOBACTERIA; ANAPLASMA PHAGOCYTOPHILUM; BACTERIA (MICROORGANISMS);

EID: 34848862803     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2007.00985.x     Document Type: Article

References (44)

1. Aoshiba, K., Yokohori, N., and Nagai, A. (2003) Alveolar wall apoptosis causes lung destruction and emphysematous changes. Am J Respir Cell Mol Biol 28: 555-562.
2. Backert, S., and Selbach, M. (2005) Tyrosine-phosphorylated bacterial effector proteins: The enemies within. Trends Microbiol 13: 476-484.
3. Barnewall, R.E., and Rikihisa, Y. (1994) Abrogation of gamma interferon-induced inhibition of Ehrlichia chaffeensis infection in human monocytes with iron-transferrin. Infect Immun 62: 4804-4810.
4. Buchdunger, E., O'Reilly, T., and Wood, J. (2002) Pharmacology of imatinib (STI571). Eur J Cancer 38 (Suppl. 5): S28-S36.
5. Burton, E.A., Plattner, R., and Pendergast, A.M. (2003) Abl tyrosine kinases are required for infection by Shigella flexneri. EMBO J 22: 5471-5479.
6. Capdeville, R., Buchdunger, E., Zimmermann, J., and Matter, A. (2002) Glivec (STI571, imatinib), a rationally developed, targeted anticancer drug. Nat Rev Drug Discov 1: 493-502.
7. Cascales, E., and Christie, P.J. (2003) The versatile bacterial type IV secretion systems. Nat Rev Microbiol 1: 137-149.
8. Caturegli, P., Asanovich, K.M., Walls, J.J., Bakken, J.S., Madigan, J.E., Popov, V.L., and Dumler, J.S. (2000) ankA: An Ehrlichia phagocytophila group gene encoding a cytoplasmic protein antigen with ankyrin repeats. Infect Immun 68: 5277-5283.
9. Cozzone, A.J., Grangeasse, C., Doublet, P., and Duclos, B. (2004) Protein phosphorylation on tyrosine in bacteria. Arch Microbiol 181: 171-181.
10. Druker, B.J., Sawyers, C.L., Kantarjian, H., Resta, D.J., Reese, S.F., Ford, J.M., et al. (2001) Activity of a specific inhibitor of the BCR-ABL tyrosine kinase in the blast crisis of chronic myeloid leukemia and acute lymphoblastic leukemia with the Philadelphia chromosome. N Engl J Med 344: 1038-1042.
11. Dumler, J.S., and Bakken, J.S. (1998) Human ehrlichioses: Newly recognized infections transmitted by ticks. Annu Rev Med 49: 201-213.
12. Dunning Hotopp, J.C., Lin, M., Madupu, R., Crabtree, J., Angiuoli, S.V., Eisen, J., et al. (2006) Comparative genomics of emerging human ehrlichiosis agents. PLoS Genet 2: E21.
13. Ghosh, P. (2004) Process of protein transport by the type III secretion system. Microbiol Mol Biol Rev 68: 771-795.
14. Goodman, J.L., Nelson, C., Vitale, B., Madigan, J.E., Dumler, J.S., Kurtti, T.J., and Munderloh, U.G. (1996) Direct cultivation of the causative agent of human granulocytic ehrlichiosis. N Engl J Med 334: 209-215.
15. Hubbard, S.R., and Till, J.H. (2000) Protein tyrosine kinase structure and function. Annu Rev Biochem 69: 373-398.
16. Hubber, A., Vergunst, A.C., Sullivan, J.T., Hooykaas, P.J., and Ronson, C.W. (2004) Symbiotic phenotypes and translocated effector proteins of the Mesorhizobium loti strain R7A VirB/D4 type IV secretion system. Mol Microbiol 54: 561-574.
17. IJdo, J.W., Carlson, A.C., and Kennedy, E.L. (2007) Anaplasma phagocytophilum AnkA is tyrosine phosphorylated at EPIYA motifs and recruits SHP-1 during early infection. Cell Microbiol 9: 1284-1296.
18. Kim, H.Y., and Rikihisa, Y. (1998) Characterization of monoclonal antibodies to the 44-kilodalton major outer membrane protein of the human granulocytic ehrlichiosis agent. J Clin Microbiol 36: 3278-3284.
19. Lanier, L.M., and Gertler, F.B. (2000) From Abl to actin: Abl tyrosine kinase and associated proteins in growth cone motility. Curr Opin Neurobiol 10: 80-87.
20. Lin, M., and Rikihisa, Y. (2003) Obligatory intracellular parasitism by Ehrlichia chaffeensis and Anaplasma phagocytophilum involves caveolae and glycosylphosphatidylinositol-anchored proteins. Cell Microbiol 5: 809-820.
21. Lin, M., and Rikihisa, Y. (2004) Bacteria-specific tyrosine-phosphorylated proteins in Ehrlichia chaffeensis and Anaplasma phagocytophilum-infected host cells. In ASM 104th General Meeting. ASM General Meeting Committee (ed.). New Orleans, LA: American Society for Microbiology, p. 127.
22. Lin, M., Zhu, M.X., and Rikihisa, Y. (2002) Rapid activation of protein tyrosine kinase and phospholipase C-γ2 and increase in cytosolic free calcium are required by Ehrlichia chaffeensis for internalization and growth in THP-1 cells. Infect Immun 70: 889-898.
23. Maruoka, M., Suzuki, J., Kawata, S., Yoshida, K., Hirao, N., Sato, S., et al. (2005) Identification of B cell adaptor for PI3-kinase (BCAP) as an Abl interactor 1-regulated substrate of Abl kinases. FEBS Lett 579: 2986-2990.
24. Morris, M.C., Depollier, J., Mery, J., Heitz, F., and Divita, G. (2001) A peptide carrier for the delivery of biologically active proteins into mammalian cells. Nat Biotechnol 19: 1173-1176.
25. Mott, J., Rikihisa, Y., and Tsunawaki, S. (2002) Effects of Anaplasma phagocytophila on NADPH oxidase components in human neutrophils and HL-60 cells. Infect Immun 70: 1359-1366.
26. Niu, H., Rikihisa, Y., Yamaguchi, M., and Ohashi, N. (2006) Differential expression of VirB9 and VirB6 during the life cycle of Anaplasma phagocytophilum in human leucocytes is associated with differential binding and avoidance of lysosome pathway. Cell Microbiol 8: 523-534.
27. Ohashi, N., Zhi, N., Lin, Q., and Rikihisa, Y. (2002) Characterization and transcriptional analysis of gene clusters for a type IV secretion machinery in human granulocytic and monocytic ehrlichiosis agents. Infect Immun 70: 2128-2138.
28. Park, J., Kim, K.J., Choi, K.S., Grab, D.J., and Dumler, J.S. (2004) Anaplasma phagocytophilum AnkA binds to granulocyte DNA and nuclear proteins. Cell Microbiol 6: 743-751.
29. Plattner, R., Irvin, B.J., Guo, S., Blackburn, K., Kazlauskas, A., Abraham, R.T., et al. (2003) A new link between the c-Abl tyrosine kinase and phosphoinositide signalling through PLC-gamma1. Nat Cell Biol 5: 309-319.
30. Rikihisa, Y., Zhi, N., Wormser, G.P., Wen, B., Horowitz, H.W., and Hechemy, K.E. (1997) Ultrastructural and antigenic characterization of a granulocytic ehrlichiosis agent directly isolated and stably cultivated from a patient in New York state. J Infect Dis 175: 210-213.
31. Robinson, D.R., Wu, Y.M., and Lin, S.F. (2000) The protein tyrosine kinase family of the human genome. Oncogene 19: 5548-5557.
32. Schrammeijer, B., den Dulk-Ras, A., Vergunst, A.C., Jurado Jacome, E., and Hooykaas, P.J. (2003) Analysis of Vir protein translocation from Agrobacterium tumefaciens using Saccharomyces cerevisiae as a model: evidence for transport of a novel effector protein VirE3. Nucleic Acids Res 31: 860-868.
33. Shaul, Y. (2000) c-Abl: Activation and nuclear targets. Cell Death Differ 7: 10-16.
34. Storey, J.R., Doros-Richert, L.A., Gingrich-Baker, C., Munroe, K., Mather, T.N., Coughlin, R.T., et al. (1998) Molecular cloning and sequencing of three granulocytic Ehrlichia genes encoding high-molecular-weight immunoreactive proteins. Infect Immun 66: 1356-1363.
35. Tani, K., Sato, S., Sukezane, T., Kojima, H., Hirose, H., Hanafusa, H., and Shishido, T. (2003) Abl interactor 1 promotes tyrosine 296 phosphorylation of mammalian enabled (Mena) by c-Abl kinase. J Biol Chem 278: 21685-21692.
36. Thomas, V., and Fikrig, E. (2007) Anaplasma phagocytophilum specifically induces tyrosine phosphorylation of ROCK1 during infection. Cell Microbiol 9: 1730-1737.
37. Tsuchiya, S., Yamabe, M., Yamaguchi, Y., Kobayashi, Y., Konno, T., and Tada, K. (1980) Establishment and characterization of a human acute monocytic leukemia cell line (THP-1). Int J Cancer 26: 171-176.
38. Van Etten, R.A. (1999) Cycling, stressed-out and nervous: Cellular functions of c-Abl. Trends Cell Biol 9: 179-186.
39. Vergunst, A.C., Schrammeijer, B., den Dulk-Ras, A., de Vlaam, C.M., Regensburg-Tuink, T.J., and Hooykaas, P.J. (2000) VirB/D4-dependent protein translocation from Agrobacterium into plant cells. Science 290: 979-982.
40. Vergunst, A.C., van Lier, M.C., den Dulk-Ras, A., and Hooykaas, P.J. (2003) Recognition of the Agrobacterium tumefaciens VirE2 translocation signal by the VirB/D4 transport system does not require VirE1. Plant Physiol 133: 978-988.
41. Vergunst, A.C., van Lier, M.C.M., den Dulk-Ras, A., Grosse Stuve, T.A., Ouwehand, A., and Hooykaas, P.J.J. (2005) Positive charge is an important feature of the C-terminal transport signal of the VirB/ D4-translocated proteins of Agrobacterium. Proc Natl Acad Sci USA 102: 832-837.
42. Wang, J.Y. (2000) Regulation of cell death by the Abl tyrosine kinase. Oncogene 19: 5643-5650.
43. Yoshiie, K., Kim, H.Y., Mott, J., and Rikihisa, Y. (2000) Intracellular infection by the human granulocytic ehrlichiosis agent inhibits human neutrophil apoptosis. Infect Immun 68: 1125-1133.
44. Zhang, Y., and Rikihisa, Y. (1997) Tyrosine phosphorylation is required for ehrlichial internalization and replication in P388D1 cells. Infect Immun 65: 2959-2964.