Anaplasma phagocytophilum APH_0032 is expressed late during infection and localizes to the pathogen-occupied vacuolar membrane

Microbial Pathogenesis

Volumn 49, Issue 5, 2010, Pages 273-284

  Huang, Bernice ^a   Troese, Matthew J ^a   Howe, Dale ^b   Ye, Shaojing ^c   Sims, Jonathan T ^c   Heinzen, Robert A ^b   Borjesson, Dori L ^d   Carlyon, Jason A ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c UNIVERSITY OF KENTUCKY   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Anaplasma; Ehrlichia; Intravacuolar pathogen; Pathogen occupied vacuole; Pathogenesis

Indexed keywords

BACTERIAL PROTEIN; MEMBRANE PROTEIN;

ACIDITY; ANAPLASMA PHAGOCYTOPHILUM; ANAPLASMATACEAE INFECTION; ARTICLE; BACTERIAL TRANSMISSION; CELL STRAIN HL 60; CONTROLLED STUDY; HUMAN; HUMAN CELL; LEGIONELLA PNEUMOPHILA; MOLECULAR WEIGHT; NEUTROPHIL; PREDICTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN ELECTROPHORESIS; PROTEIN LOCALIZATION; PROTEIN SECRETION; PROTEIN TRANSPORT; SALIVARY GLAND; TANDEM REPEAT; TICK; TONOPLAST;

AMINO ACID SEQUENCE; ANAPLASMA PHAGOCYTOPHILUM; ANIMALS; BACTERIAL PROTEINS; CELLS, CULTURED; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; HOST-PATHOGEN INTERACTIONS; HUMANS; INTRACELLULAR MEMBRANES; LEGIONELLA PNEUMOPHILA; MEMBRANE TRANSPORT PROTEINS; MICE; MOLECULAR SEQUENCE DATA; MOLECULAR WEIGHT; NEUTROPHILS; PROTEIN STRUCTURE, TERTIARY; TANDEM REPEAT SEQUENCES; TICKS; TRANSCRIPTION, GENETIC; VACUOLES;

ANAPLASMA; ANAPLASMA PHAGOCYTOPHILUM; EHRLICHIA; IXODIDA; LEGIONELLA PNEUMOPHILA; MURINAE; MUS;

EID: 77955427703     PISSN: 08824010     EISSN: 10961208     Source Type: Journal    
DOI: 10.1016/j.micpath.2010.06.009     Document Type: Article

References (57)

1. Chen S.M., Dumler J.S., Bakken J.S., Walker D.H. Identification of a granulocytotropic Ehrlichia species as the etiologic agent of human disease. J Clin Microbiol 1994, 32:589-595.
2. Thomas R.J., Dumler J.S., Carlyon J.A. Current management of human granulocytic anaplasmosis, human monocytic ehrlichiosis and Ehrlichia ewingii ehrlichiosis. Expert Rev Anti Infect Ther 2009, 7:709-722.
3. Garcia-Garcia J.C., Barat N.C., Trembley S.J., Dumler J.S. Epigenetic silencing of host cell defense genes enhances intracellular survival of the rickettsial pathogen Anaplasma phagocytophilum. PLoS Pathog 2009, 5:e1000488.
4. Munderloh U.G., Lynch M.J., Herron M.J., Palmer A.T., Kurtti T.J., Nelson R.D., et al. Infection of endothelial cells with Anaplasma marginale and A. phagocytophilum. Vet Microbiol 2004, 101:53-64.
5. Woldehiwet Z., Horrocks B.K., Scaife H., Ross G., Munderloh U.G., Bown K., et al. Cultivation of an ovine strain of Ehrlichia phagocytophila in tick cell cultures. J Comp Pathol 2002, 127:142-149.
6. Carlyon J.A., Abdel-Latif D., Pypaert M., Lacy P., Fikrig E. Anaplasma phagocytophilum utilizes multiple host evasion mechanisms to thwart NADPH oxidase-mediated killing during neutrophil infection. Infect Immun 2004, 72:4772-4783.
7. IJdo J.W., Mueller A.C. Neutrophil NADPH oxidase is reduced at the Anaplasma phagocytophilum phagosome. Infect Immun 2004, 72:5392-5401.
8. Mott J., Barnewall R.E., Rikihisa Y. Human granulocytic ehrlichiosis agent and Ehrlichia chaffeensis reside in different cytoplasmic compartments in HL-60 cells. Infect Immun 1999, 67:1368-1378.
9. Webster P., IJdo J.W., Chicoine L.M., Fikrig E. The agent of human granulocytic ehrlichiosis resides in an endosomal compartment. J Clin Invest 1998, 101:1932-1941.
10. Gokce H.I., Ross G., Woldehiwet Z. Inhibition of phagosome-lysosome fusion in ovine polymorphonuclear leucocytes by Ehrlichia (Cytoecetes) phagocytophila. J Comp Pathol 1999, 120:369-381.
11. Huang B., Hubber A., McDonough J.A., Roy C.R., Scidmore M.A., Carlyon J.A. The Anaplasma phagocytophilum-occupied vacuole selectively recruits Rab-GTPases that are predominantly associated with recycling endosomes. Cell Microbiol 2010.
12. Kumar Y., Valdivia R.H. Leading a sheltered life: intracellular pathogens and maintenance of vacuolar compartments. Cell Host Microbe 2009, 5:593-601.
13. Huang B., Troese M.J., Ye S., Sims J.T., Galloway N.L., Borjesson D., et al. Anaplasma phagocytophilum APH1387 is expressed throughout bacterial intracellular development and localizes to the pathogen-occupied vacuolar membrane. Infect Immun 2010, 78:1864-1873.
14. Doyle C.K., Nethery K.A., Popov V.L., McBride J.W. 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 2006, 74:711-720.
15. Popov V.L., Yu X., Walker D.H. 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 2000, 28:71-80.
16. Bannantine J.P., Stamm W.E., Suchland R.J., Rockey D.D. Chlamydia trachomatis IncA is localized to the inclusion membrane and is recognized by antisera from infected humans and primates. Infect Immun 1998, 66:6017-6021.
17. Rockey D.D., Heinzen R.A., Hackstadt T. Cloning and characterization of a Chlamydia psittaci gene coding for a protein localized in the inclusion membrane of infected cells. Mol Microbiol 1995, 15:617-626.
18. Rockey D.D., Rosquist J.L. Protein antigens of Chlamydia psittaci present in infected cells but not detected in the infectious elementary body. Infect Immun 1994, 62:106-112.
19. Storey J.R., Doros-Richert L.A., Gingrich-Baker C., Munroe K., Mather T.N., Coughlin R.T., et al. Molecular cloning and sequencing of three granulocytic Ehrlichia genes encoding high-molecular-weight immunoreactive proteins. Infect Immun 1998, 66:1356-1363.
20. Ades E.W., Candal F.J., Swerlick R.A., George V.G., Summers S., Bosse D.C., et al. HMEC-1: establishment of an immortalized human microvascular endothelial cell line. J Invest Dermatol 1992, 99:683-690.
21. Kyte J., Doolittle R.F. A simple method for displaying the hydropathic character of a protein. J Mol Biol 1982, 157:105-132.
22. Troese M.J., Carlyon J.A. Anaplasma phagocytophilum dense-cored organisms mediate cellular adherence through recognition of human P-selectin glycoprotein ligand 1. Infect Immun 2009, 77:4018-4027.
23. Carlyon J.A., Chan W.T., Galan J., Roos D., Fikrig E. Repression of rac2 mRNA expression by Anaplasma phagocytophila is essential to the inhibition of superoxide production and bacterial proliferation. J Immunol 2002, 169:7009-7018.
24. Scorpio D.G., Caspersen K., Ogata H., Park J., Dumler J.S. Restricted changes in major surface protein-2 (msp2) transcription after prolonged in vitro passage of Anaplasma phagocytophilum. BMC Microbiol 2004, 4:1.
25. Park J., Choi K.S., Dumler J.S. Major surface protein 2 of Anaplasma phagocytophilum facilitates adherence to granulocytes. Infect Immun 2003, 71:4018-4025.
26. Borjesson D.L., Simon S.I., Hodzic E., DeCock H.E., Ballantyne C.M., Barthold S.W. Roles of neutrophil beta 2 integrins in kinetics of bacteremia, extravasation, and tick acquisition of Anaplasma phagocytophila in mice. Blood 2003, 101:3257-3264.
27. Carlyon J.A., Ryan D., Archer K., Fikrig E. Effects of Anaplasma phagocytophilum on host cell ferritin mRNA and protein levels. Infect Immun 2005, 73:7629-7636.
28. Bardill J.P., Miller J.L., Vogel J.P. IcmS-dependent translocation of SdeA into macrophages by the Legionella pneumophila type IV secretion system. Mol Microbiol 2005, 56:90-103.
29. Voth D.E., Howe D., Beare P.A., Vogel J.P., Unsworth N., Samuel J.E., et al. The Coxiella burnetii ankyrin repeat domain-containing protein family is heterogeneous, with C-terminal truncations that influence Dot/Icm-mediated secretion. J Bacteriol 2009, 191:4232-4242.
30. Voth D.E., Howe D., Heinzen R.A. Coxiella burnetii inhibits apoptosis in human THP-1 cells and monkey primary alveolar macrophages. Infect Immun 2007, 75:4263-4271.
31. Nagai H., Kagan J.C., Zhu X., Kahn R.A., Roy C.R. A bacterial guanine nucleotide exchange factor activates ARF on Legionella phagosomes. Science 2002, 295:679-682.
32. Bannantine J.P., Griffiths R.S., Viratyosin W., Brown W.J., Rockey D.D. A secondary structure motif predictive of protein localization to the chlamydial inclusion membrane. Cell Microbiol 2000, 2:35-47.
33. Rockey D.D., Alzhanov D. Proteins in the chlamydial inclusion membrane. Chlamydia genomics and pathogenesis 2006, 235-254. Horizon Bioscience, Norfolk, UK. P.M. Bavoil, P.B. Wyrick (Eds.).
34. de la Fuente J., Garcia-Garcia J.C., Barbet A.F., Blouin E.F., Kocan K.M. Adhesion of outer membrane proteins containing tandem repeats of Anaplasma and Ehrlichia species (Rickettsiales: Anaplasmataceae) to tick cells. Vet Microbiol 2004, 98:313-322.
35. Goodman J.L. Human granulocytic anaplasmosis. Tick-borne diseases of humans 2005, 218-238. ASM Press, Washington, D.C. J.L. Goodman, D.T. Dennis, D.E. Sonenshine (Eds.).
36. Borjesson D.L., Kobayashi S.D., Whitney A.R., Voyich J.M., Argue C.M., Deleo F.R. Insights into pathogen immune evasion mechanisms: Anaplasma phagocytophilum fails to induce an apoptosis differentiation program in human neutrophils. J Immunol 2005, 174:6364-6372.
37. Rikihisa Y. Anaplasma phagocytophilum and Ehrlichia chaffeensis: subversive manipulators of host cells. Nat Rev Microbiol 2010.
38. Lin M., den Dulk-Ras A., Hooykaas P.J., Rikihisa Y. Anaplasma phagocytophilum AnkA secreted by type IV secretion system is tyrosine phosphorylated by Abl-1 to facilitate infection. Cell Microbiol 2007, 9:2644-2657.
39. Shin S., Roy C.R. Host cell processes that influence the intracellular survival of Legionella pneumophila. Cell Microbiol 2008, 10:1209-1220.
40. de Jong M.F., Sun Y.H., den Hartigh A.B., van Dijl J.M., Tsolis R.M. Identification of VceA and VceC, two members of the VjbR regulon that are translocated into macrophages by the Brucella type IV secretion system. Mol Microbiol 2008, 70:1378-1396.
41. Nelson C.M., Herron M.J., Felsheim R.F., Schloeder B.R., Grindle S.M., Chavez A.O., et al. Whole genome transcription profiling of Anaplasma phagocytophilum in human and tick host cells by tiling array analysis. BMC Genomics 2008, 9:364.
42. Petsko G.A., Ringe D. From sequence to structure. Protein structure and function 2004, New Science Press, London, UK. 1 ed.
43. Luo T., Zhang X., Wakeel A., Popov V.L., McBride J.W. A variable-length PCR target protein of Ehrlichia chaffeensis contains major species-specific antibody epitopes in acidic serine-rich tandem repeats. Infect Immun 2008, 76:1572-1580.
44. Yu X.J., Crocquet-Valdes P., Cullman L.C., Walker D.H. The recombinant 120-kilodalton protein of Ehrlichia chaffeensis, a potential diagnostic tool. J Clin Microbiol 1996, 34:2853-2855.
45. Yu X.J., Crocquet-Valdes P., Walker D.H. Cloning and sequencing of the gene for a 120-kDa immunodominant protein of Ehrlichia chaffeensis. Gene 1997, 184:149-154.
46. Wakeel A., Kuriakose J.A., McBride J.W. An Ehrlichia chaffeensis tandem repeat protein interacts with multiple host targets involved in cell signaling, transcriptional regulation, and vesicle trafficking. Infect Immun 2009, 77:1734-1745.
47. Clifton D.R., Fields K.A., Grieshaber S.S., Dooley C.A., Fischer E.R., Mead D.J., et al. 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 2004, 101:10166-10171.
48. Futse J.E., Brayton K.A., Nydam S.D., Palmer G.H. Generation of antigenic variants via gene conversion: evidence for recombination fitness selection at the locus level in Anaplasma marginale. Infect Immun 2009, 77:3181-3187.
49. Hussain M., Haggar A., Peters G., Chhatwal G.S., Herrmann M., Flock J.I., et al. 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 2008, 76:5615-5623.
50. IJdo J., Carlson A.C., Kennedy E.L. Anaplasma phagocytophilum AnkA is tyrosine-phosphorylated at EPIYA motifs and recruits SHP-1 during early infection. Cell Microbiol 2007, 9:1284-1296.
51. Wistedt A.C., Ringdahl U., Muller-Esterl W., Sjobring U. Identification of a plasminogen-binding motif in PAM, a bacterial surface protein. Mol Microbiol 1995, 18:569-578.
52. Zhu B., Nethery K.A., Kuriakose J.A., Wakeel A., Zhang X., McBride J.W. Nuclear translocated Ehrlichia chaffeensis ankyrin protein interacts with a specific adenine-rich motif of host promoter and intronic Alu elements. Infect Immun 2009, 77:4243-4255.
53. Wakeel A., Zhang X., McBride J.W. Mass spectrometric analysis of Ehrlichia chaffeensis tandem repeat proteins reveals evidence of phosphorylation and absence of glycosylation. PLoS One 2010, 5:e9552.
54. Vergunst A.C., van Lier M.C., den Dulk-Ras A., Stuve T.A., Ouwehand A., Hooykaas P.J. 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 2005, 102:832-837.
55. Alvarez-Martinez C.E., Christie P.J. Biological diversity of prokaryotic type IV secretion systems. Microbiol Mol Biol Rev 2009, 73:775-808.
56. Delepelaire P. Type I secretion in gram-negative bacteria. Biochim Biophys Acta 2004, 1694:149-161.
57. Hotopp J.C., Lin M., Madupu R., Crabtree J., Angiuoli S.V., Eisen J., et al. Comparative genomics of emerging human ehrlichiosis agents. PLoS Genet 2006, 2:e21.