Anaplasma phagocytophilum APH-1387 is expressed throughout bacterial intracellular development and localizes to the pathogen-occupied vacuolar membrane

Infection and Immunity

Volumn 78, Issue 5, 2010, Pages 1864-1873

  Huang, Bernice ^a   Troese, Matthew J ^a   Ye, Shaojing ^b   Sims, Jonathan T ^b   Galloway, Nathan L ^a   Borjesson, Dori L ^c   Carlyon, Jason A ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACID PROTEIN;

ALPHA HELIX; ANAPLASMA PHAGOCYTOPHILUM; ARTICLE; CELL STRAIN HL 60; CELL SURFACE; HOST CELL; HUMAN; HUMAN CELL; MOLECULAR WEIGHT; NEUTROPHIL; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; TICK; TONOPLAST;

ANAPLASMA PHAGOCYTOPHILUM; ANIMALS; BACTERIAL PROTEINS; CELL LINE; CELL MEMBRANE; EHRLICHIOSIS; GENE EXPRESSION; HUMANS; MICE; MICROSCOPY, CONFOCAL; MICROSCOPY, IMMUNOELECTRON; NEUTROPHILS; TICKS; VACUOLES;

EID: 77951215124     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01418-09     Document Type: Article

References (56)

1. Ades, E. W., F. J. Candal, R. A. Swerlick, V. G. George, S. Summers, D. C. Bosse, and T. J. Lawley. 1992. HMEC-1: establishment of an immortalized human microvascular endothelial cell line. J. Invest. Dermatol. 99:683-690.
2. Alvarez-Martinez, C. E., and P. J. Christie. 2009. Biological diversity of prokaryotic type IV secretion systems. Microbiol. Mol. Biol. Rev. 73:775-808.
3. Bannantine, J. P., R. S. Griffiths, W. Viratyosin, W. J. Brown, and D. D. Rockey. 2000. A secondary structure motif predictive of protein localization to the chlamydial inclusion membrane. Cell. Microbiol. 2:35-47.
4. Bannantine, J. P., W. E. Stamm, R. J. Suchland, and D. D. Rockey. 1998. Chlamydia trachomatis IncA is localized to the inclusion membrane and is recognized by antisera from infected humans and primates. Infect. Immun. 66:6017-6021.
5. Borjesson, D. L., S. D. Kobayashi, A. R. Whitney, J. M. Voyich, C. M. Argue, and F. R. Deleo. 2005. Insights into pathogen immune evasion mechanisms: Anaplasma phagocytophilum fails to induce an apoptosis differentiation program in human neutrophils. J. Immunol. 174:6364-6372.
6. Borjesson, D. L., S. I. Simon, E. Hodzic, H. E. DeCock, C. M. Ballantyne, and S. W. Barthold. 2003. Roles of neutrophil beta 2 integrins in kinetics of bacteremia, extravasation, and tick acquisition of Anaplasma phagocytophila in mice. Blood 101:3257-3264.
7. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
8. Brayton, K. A., L. S. Kappmeyer, D. R. Herndon, M. J. Dark, D. L. Tibbals, G. H. Palmer, T. C. McGuire, and D. P. Knowles, Jr. 2005. Complete genome sequencing of Anaplasma marginale reveals that the surface is skewed to two superfamilies of outer membrane proteins. Proc. Natl. Acad. Sci. U. S. A. 102:844-849.
9. Carlyon, J. A. 2005. Laboratory maintenance of Anaplasma phagocytophilum, p. 3A.2.9.-3A.2.13. In R. Coico, T. F. Kowalik, J. M. Quarles, B. Stevenson, and R. Taylor (ed.), Current protocols in microbiology. J. Wiley and Sons, Hoboken, NJ.
10. Carlyon, J. A., D. Abdel-Latif, M. Pypaert, P. Lacy, and E. Fikrig. 2004. Anaplasma phagocytophilum utilizes multiple host evasion mechanisms to thwart NADPH oxidase-mediated killing during neutrophil infection. Infect. Immun. 72:4772-4783.
11. Carlyon, J. A., W. T. Chan, J. Galan, D. Roos, and E. Fikrig. 2002. Repression of rac2 mRNA expression by Anaplasma phagocytophila is essential to the inhibition of superoxide production and bacterial proliferation. J. Immunol. 169:7009-7018.
12. Carlyon, J. A., D. Ryan, K. Archer, and E. Fikrig. 2005. Effects of Anaplasma phagocytophilum on host cell ferritin mRNA and protein levels. Infect. Immun. 73:7629-7636.
13. Caturegli, P., K. M. Asanovich, J. J. Walls, J. S. Bakken, J. E. Madigan, V. L. Popov, and J. S. Dumler. 2000. ankA: an Ehrlichia phagocytophila group gene encoding a cytoplasmic protein antigen with ankyrin repeats. Infect. Immun. 68:5277-5283.
14. Chen, S. M., J. S. Dumler, J. S. Bakken, and D. H. Walker. 1994. Identification of a granulocytotropic Ehrlichia species as the etiologic agent of human disease. J. Clin. Microbiol. 32:589-595.
15. Clifton, D. R., K. A. Fields, S. S. Grieshaber, C. A. Dooley, E. R. Fischer, D. J. Mead, R. A. Carabeo, and T. Hackstadt. 2004. A chlamydial type III translocated protein is tyrosine-phosphorylated at the site of entry and associated with recruitment of actin. Proc. Natl. Acad. Sci. U. S. A. 101:10166-10171.
16. Dark, M. J., D. R. Herndon, L. S. Kappmeyer, M. P. Gonzales, E. Nordeen, G. H. Palmer, D. P. Knowles, Jr., and K. A. Brayton. 2009. Conservation in the face of diversity: multistrain analysis of an intracellular bacterium. BMC Genomics 10:16.
17. de la Fuente, J., J. C. Garcia-Garcia, A. F. Barbet, E. F. Blouin, and K. M. Kocan. 2004. Adhesion of outer membrane proteins containing tandem repeats of Anaplasma and Ehrlichia species (Rickettsiales: Anaplasmataceae) to tick cells. Vet. Microbiol. 98:313-322.
18. Doyle, C. K., K. A. Nethery, V. L. Popov, and J. W. McBride. 2006. Differentially expressed and secreted major immunoreactive protein orthologs of Ehrlichia canis and E. chaffeensis elicit early antibody responses to epitopes on glycosylated tandem repeats. Infect. Immun. 74:711-720.
19. Eisenberg, D. 1984. Three-dimensional structure of membrane and surface proteins. Annu. Rev. Biochem. 53:595-623.
20. Futse, J. E., K. A. Brayton, S. D. Nydam, and G. H. Palmer. 2009. Generation of antigenic variants via gene conversion: evidence for recombination fitness selection at the locus level in Anaplasma marginale. Infect. Immun. 77:3181-3187.
21. Garcia-Garcia, J. C., N. C. Barat, S. J. Trembley, and J. S. Dumler. 2009. Epigenetic silencing of host cell defense genes enhances intracellular survival of the rickettsial pathogen Anaplasma phagocytophilum. PLoS Pathog. 5:e1000488.
22. Garnier, J., D. J. Osguthorpe, and B. Robson. 1978. Analysis of the accuracy and implications of simple methods for predicting the secondary structure of globular proteins. J. Mol. Biol. 120:97-120.
23. Gokce, H. I., G. Ross, and Z. Woldehiwet. 1999. Inhibition of phagosomelysosome fusion in ovine polymorphonuclear leucocytes by Ehrlichia (Cytoecetes) phagocytophila. J. Comp. Pathol. 120:369-381.
24. Goodman, J. L. 2005. Human granulocytic anaplasmosis, p. 218-238. In J. L. Goodman, D. T. Dennis, and D. E. Sonenshine (ed.), Tick-borne diseases of humans. ASM Press, Washington, DC.
25. Hotopp, J. C., M. Lin, R. Madupu, J. Crabtree, S. V. Angiuoli, J. Eisen, R. Seshadri, Q. Ren, M. Wu, T. R. Utterback, S. Smith, M. Lewis, H. Khouri, C. Zhang, H. Niu, Q. Lin, N. Ohashi, N. Zhi, W. Nelson, L. M. Brinkac, R. J. Dodson, M. J. Rosovitz, J. Sundaram, S. C. Daugherty, T. Davidsen, A. S. Durkin, M. Gwinn, D. H. Haft, J. D. Selengut, S. A. Sullivan, N. Zafar, L. Zhou, F. Benahmed, H. Forberger, R. Halpin, S. Mulligan, J. Robinson, O. White, Y. Rikihisa, and H. Tettelin. 2006. Comparative genomics of emerging human ehrlichiosis agents. PLoS Genet. 2:e21.
26. Hussain, M., A. Haggar, G. Peters, G. S. Chhatwal, M. Herrmann, J. I. Flock, and B. Sinha. 2008. More than one tandem repeat domain of the extracellular adherence protein of Staphylococcus aureus is required for aggregation, adherence, and host cell invasion but not for leukocyte activation. Infect. Immun. 76:5615-5623.
27. IJdo, J., A. C. Carlson, and E. L. Kennedy. 2007. Anaplasma phagocytophilum AnkA is tyrosine-phosphorylated at EPIYA motifs and recruits SHP-1 during early infection. Cell. Microbiol. 9:1284-1296.
28. IJdo, J. W., and A. C. Mueller. 2004. Neutrophil NADPH oxidase is reduced at the Anaplasma phagocytophilum phagosome. Infect. Immun. 72:5392-5401.
29. Kumar, Y., and R. H. Valdivia. 2009. Leading a sheltered life: intracellular pathogens and maintenance of vacuolar compartments. Cell Host Microbe 5:593-601.
30. Kyte, J., and R. F. Doolittle. 1982. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157:105-132.
31. Lin, M., A. den Dulk-Ras, P. J. Hooykaas, and Y. Rikihisa. 2007. Anaplasma phagocytophilum AnkA secreted by type IV secretion system is tyrosine phosphorylated by Abl-1 to facilitate infection. Cell. Microbiol. 9:2644-2657.
32. Luo, T., X. Zhang, A. Wakeel, V. L. Popov, and J. W. McBride. 2008. A variable-length PCR target protein of Ehrlichia chaffeensis contains major species-specific antibody epitopes in acidic serine-rich tandem repeats. Infect. Immun. 76:1572-1580.
33. Mott, J., R. E. Barnewall, and Y. Rikihisa. 1999. Human granulocytic ehrlichiosis agent and Ehrlichia chaffeensis reside in different cytoplasmic compartments in HL-60 cells. Infect. Immun. 67:1368-1378.
34. Munderloh, U. G., M. J. Lynch, M. J. Herron, A. T. Palmer, T. J. Kurtti, R. D. Nelson, and J. L. Goodman. 2004. Infection of endothelial cells with Anaplasma marginale and A. phagocytophilum. Vet. Microbiol. 101:53-64.
35. Nelson, C. M., M. J. Herron, R. F. Felsheim, B. R. Schloeder, S. M. Grindle, A. O. Chavez, T. J. Kurtti, and U. G. Munderloh. 2008. Whole genome transcription profiling of Anaplasma phagocytophilum in human and tick host cells by tiling array analysis. BMC Genomics 9:364.
36. Ohashi, N., N. Zhi, Q. Lin, and Y. Rikihisa. 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.
37. Park, J., K. S. Choi, and J. S. Dumler. 2003. Major surface protein 2 of Anaplasma phagocytophilum facilitates adherence to granulocytes. Infect. Immun. 71:4018-4025.
38. Petsko, G. A., and D. Ringe. 2004. From sequence to structure. Protein structure and function, 1st ed. New Science Press, London, United Kingdom.
39. Popov, V. L., X. Yu, and D. H. Walker. 2000. The 120 kDa outer membrane protein of Ehrlichia chaffeensis: preferential expression on dense-core cells and gene expression in Escherichia coli associated with attachment and entry. Microb. Pathog. 28:71-80.
40. Reneer, D. V., M. J. Troese, B. Huang, S. A. Kearns, and J. A. Carlyon. 2008. Anaplasma phagocytophilum PSGL-1-independent infection does not require Syk and leads to less efficient AnkA delivery. Cell. Microbiol. 10:1827-1838.
41. Rockey, D. D., and D. Alzhanov. 2006. Proteins in the chlamydial inclusion membrane, p. 235-254. In P. M. Bavoil and P. B. Wyrick (ed.), Chlamydia genomics and pathogenesis. Horizon Bioscience, Norfolk, United Kingdom.
42. Rockey, D. D., R. A. Heinzen, and T. Hackstadt. 1995. Cloning and characterization of a Chlamydia psittaci gene coding for a protein localized in the inclusion membrane of infected cells. Mol. Microbiol. 15:617-626.
43. Rockey, D. D., and J. L. Rosquist. 1994. Protein antigens of Chlamydia psittaci present in infected cells but not detected in the infectious elementary body. Infect. Immun. 62:106-112.
44. Scorpio, D. G., K. Caspersen, H. Ogata, J. Park, and J. S. Dumler. 2004. Restricted changes in major surface protein-2 (msp2) transcription after prolonged in vitro passage of Anaplasma phagocytophilum. BMC Microbiol. 4:1.
45. Storey, J. R., L. A. Doros-Richert, C. Gingrich-Baker, K. Munroe, T. N. Mather, R. T. Coughlin, G. A. Beltz, and C. I. Murphy. 1998. Molecular cloning and sequencing of three granulocytic Ehrlichia genes encoding high-molecular-weight immunoreactive proteins. Infect. Immun. 66:1356-1363.
46. Teng, C. H., R. U. Palaniappan, and Y. F. Chang. 2003. Cloning and characterization of an Ehrlichia canis gene encoding a protein localized to the morula membrane. Infect. Immun. 71:2218-2225.
47. Thomas, R. J., J. S. Dumler, and J. A. Carlyon. 2009. Current management of human granulocytic anaplasmosis, human monocytic ehrlichiosis and Ehrlichia ewingii ehrlichiosis. Expert Rev. Anti Infect. Ther. 7:709-722.
48. Troese, M. J., and J. A. Carlyon. 2009. Anaplasma phagocytophilum dense-cored organisms mediate cellular adherence through recognition of human P-selectin glycoprotein ligand 1. Infect. Immun. 77:4018-4027.
49. Vergunst, A. C., M. C. van Lier, A. den Dulk-Ras, T. A. Stuve, A. Ouwehand, and P. J. Hooykaas. 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. U. S. A. 102:832-837.
50. Wakeel, A., J. A. Kuriakose, and J. W. McBride. 2009. An Ehrlichia chaffeensis tandem repeat protein interacts with multiple host targets involved in cell signaling, transcriptional regulation, and vesicle trafficking. Infect. Immun. 77:1734-1745.
51. Webster, P., J. W. IJdo, L. M. Chicoine, and E. Fikrig. 1998. The agent of human granulocytic ehrlichiosis resides in an endosomal compartment. J. Clin. Invest. 101:1932-1941.
52. Wistedt, A. C., U. Ringdahl, W. Muller-Esterl, and U. Sjobring. 1995. Identification of a plasminogen-binding motif in PAM, a bacterial surface protein. Mol. Microbiol. 18:569-578.
53. Woldehiwet, Z., B. K. Horrocks, H. Scaife, G. Ross, U. G. Munderloh, K. Bown, S. W. Edwards, and C. A. Hart. 2002. Cultivation of an ovine strain of Ehrlichia phagocytophila in tick cell cultures. J. Comp. Pathol. 127:142-149.
54. Yu, X. J., P. Crocquet-Valdes, L. C. Cullman, and D. H. Walker. 1996. The recombinant 120-kilodalton protein of Ehrlichia chaffeensis, a potential diagnostic tool. J. Clin. Microbiol. 34:2853-2855.
55. Yu, X. J., P. Crocquet-Valdes, and D. H. Walker. 1997. Cloning and sequencing of the gene for a 120-kDa immunodominant protein of Ehrlichia chaffeensis. Gene 184:149-154. (Pubitemid 27045941)
56. Zhu, B., K. A. Nethery, J. A. Kuriakose, A. Wakeel, X. Zhang, and J. W. McBride. 2009. Nuclear translocated Ehrlichia chaffeensis ankyrin protein interacts with a specific adenine-rich motif of host promoter and intronic Alu elements. Infect. Immun. 77:4243-4255.