Unique macrophage and tick cell-specific protein expression from the p28/ p30-outer membrane protein multigene locus in Ehrlichia chaffeensis and Ehrlichia canis

Cellular Microbiology

Volumn 8, Issue 9, 2006, Pages 1475-1487

  Singu, Vijayakrishna ^a   Peddireddi, Lalitha ^a   Sirigireddy, Kamesh R ^a   Cheng, Chuanmin ^a   Munderloh, Ulrike ^b   Ganta, Roman R ^a  

^a KANSAS STATE UNIVERSITY   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

OUTER MEMBRANE PROTEIN; PROTEIN P28; PROTEIN P30;

AMBLYOMMA; ANIMAL CELL; ARTICLE; BACTERIUM ISOLATE; CELL CULTURE; CELL LINE; CONTROLLED STUDY; EHRLICHIA CANIS; EHRLICHIA CHAFFEENSIS; GENE EXPRESSION; GENE LOCUS; HOST CELL; IXODES SCAPULARIS; LIFE CYCLE; MACROPHAGE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING; TICK;

AMINO ACID SEQUENCE; ANIMALS; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL PROTEINS; BLOTTING, NORTHERN; BLOTTING, WESTERN; CELL LINE; CHROMATOGRAPHY, LIQUID; EHRLICHIA CANIS; EHRLICHIA CHAFFEENSIS; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; FEMALE; GENE EXPRESSION REGULATION, BACTERIAL; GLYCOPROTEINS; MACROPHAGES; MASS SPECTROMETRY; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; PHOSPHORYLATION; PROTEOMICS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TICKS;

ACARI; AMBLYOMMA AMERICANUM; EHRLICHIA; EHRLICHIA CANIS; EHRLICHIA CHAFFEENSIS; IXODES SCAPULARIS; IXODIDA; VERTEBRATA;

EID: 33747009964     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2006.00727.x     Document Type: Article

References (52)

1. Anderson, B. E., Sims, K. G., Olson, J. G., Childs, J. E., Piesman, J. F., Happ, C. M., et al. (1993) Amblyomma americanum: A potential vector of human ehrlichiosis. Am J Trop Med Hyg 49: 239-244.
2. Andrew, H. R., and Norval, R. A. (1989) The carrier status of sheep, cattle and African buffalo recovered from heartwater. Vet Parasitol 34: 261-266.
3. Barbet, A. F., Lundgren, A., Yi, J., Rurangirwa, F. R., and Palmer, G. H. (2000) Antigenic variation of Anaplasma marginale by expression of MSP2 mosaics. Infect Immun 68: 6133-6138.
4. Bekker, C. P., Postigo, M., Taoufik, A., Bell-Sakyi, L., Ferraz, C., Martinez, D., and Jongejan, F. (2005) Transcription analysis of the major antigenic protein 1 multigene family of three in vitro -cultured Ehrlichia ruminantium isolates. J Bacteriol 187: 4782-4791.
5. Bell-Sakyi, L., Paxton, E. A., Munderloh, U. G., and Sumption, K. J. (2000) Growth of Cowdria ruminantium, the causative agent of heartwater, in a tick cell line. J Clin Microbiol 38: 1238-1240.
6. Blouin, E. F., de la Fuente, J., Garcia-Garcia, J. C., Sauer, J. R., Saliki, J. T., and Kocan, K. M. (2002) Applications of a cell culture system for studying the interaction of Anaplasma marginale with tick cells. Anim Health Res Rev 3: 57-68.
7. Buhles, W. C. J., Huxsoll, D. L., and Ristic, M. (1974) Tropical canine pancytopenia: Clinical, hematologic, and serologic response of dogs to Ehrlichia canis infection, tetracycline therapy, and challenge inoculation. J Infect Dis 130: 357-367.
8. Buller, R. S., Arens, M., Hmiel, S. P., Paddock, C. D., Sumner, J. W., Rikhisa, Y., et al. (1999) Ehrlichia ewingii, a newly recognized agent of human ehrlichiosis. N Engl J Med 341: 148-155.
9. Chen, S. M., Dumler, J. S., Bakken, J. S., and Walker, D. H. (1994a) Identification of a granulocytotropic Ehrlichia species as the etiologic agent of human disease. J Clin Microbiol 32: 589-595.
10. Chen, S. M., Dumler, J. S., Feng, H. M., and Walker, D. H. (1994b) Identification of the antigenic constituents of Ehrlichia chaffeensis. Am J Trop Med Hyg 50: 52-58.
11. Chen, S. M., Popov, V. L., Feng, H. M., and Walker, D. H. (1996) Analysis and ultrastructural localization of Ehrlichia chaffeensis proteins with monoclonal antibodies. Am J Trop Med Hyg 54: 405-412.
12. Cheng, C., Paddock, C. D., and Reddy, G. R. (2003) Molecular heterogeneity of Ehrlichia chaffeensis isolates determined by sequence analysis of the 28-kilodalton outer membrane protein genes and other regions of the genome. Infect Immun 71: 187-195.
13. Davidson, W. R., Lockhart, J. M., Stallknecht, D. E., Howerth, E. W., Dawson, J. E., and Rechav, Y. (2001) Persistent Ehrlichia chaffeensis infection in white-tailed deer. J Wild Dis 37: 538-546.
14. Dawson, J. E., Anderson, B. E., Fishbein, D. B., Sanchez, C. Y., Goldsmith, C. Y., Wilson, K. H., and Duntley, C. W. (1991) Isolation and characterization of an Ehrlichia sp. from a patient diagnosed with human ehrlichiosis. J Clin Microbiol 29: 2741-2745.
15. Dumler, J. S., Sutker, W. L., and Walker, D. H. (1993) Persistent Infection with Ehrlichia chaffeensis. Clin Infect Dis 17: 903-905.
16. Dumler, J. S., Barbet, A. F., Bekker, C. P. J., Dasch, G. A., Palmer, G. H., Ray, S. C., et al. (2001) Reorganization of genera in the families Rickettsiaceae and Anaplasmataceae in the order Rickettsiales: unification of some species of Ehrlichia with Anaplasma, Cowdria with Ehrlichia and Ehrlichia with Neorickettsia, descriptions of six new species combinations and designation of Ehrlichia equi and 'HGE agent'as subjective synonyms of Ehrlichia phagocytophila. Int J Syst Evol Microbiol 51: 2145-2165.
17. Fikrig, E., Pal, U., Chen, M., Anderson, J. F., and Flavell, R. A. (2004) OspB antibody prevents Borrelia burgdorferi colonization of Ixodes scapularis. Infect Immun 72: 1755-1759.
18. French, D. M., Brown, W. C., and Palmer, G. H. (1999) Emergence of Anaplasma marginale antigenic variants during persistent rickettsemia. Infect Immun 67: 5834-5840.
19. de la Fuente, J., Garcia-Garcia, J. C., Blouin, E. F., and Kocan, K. M. (2001) Differential adhesion of major surface proteins 1a and 1b of the ehrlichial cattle pathogen Anaplasma marginale in bovine erythrocytes and tick cells. J Int Parasitol 31: 145-153.
20. Futse, J. E., Brayton, K. A., Knowles, D. P., Jr, and Palmer, G. H. (2005) Structural basis for segmental gene conversion in generation of Anaplasma marginale outer membrane protein variants. Mol Microbiol 57: 212-221.
21. Ganta, R. R., Wilkerson, M. J., Cheng, C., Rokey, A. M., and Chapes, S. K. (2002) Persistent Ehrlichia chaffeensis infection occurs in the absence of functional major histocompatibility complex class II genes. Infect Immun 70: 380-388.
22. Garcia-Garcia, J. C., de la Fuente, J., Bell-Eunice, G., Blouin, E. F., and Kocan, K. M. (2004) Glycosylation of Anaplasma marginale major surface protein 1a and its putative role in adhesion to tick cells. Infect Immun 72: 3022-3030.
23. Gorg, A. (1993) Two-dimensional electrophoresis with immobilized pH gradients: Current state. Biochem Soc Trans 21: 130-132.
24. Gusa, A. A., Buller, R. S., Storch, G. A., Huycke, M. M., Machado, L. J., Slater, L. N., et al. (2001) Identification of a p28 gene in Ehrlichia ewingii: Evaluation of gene for use as a target for a species-specific PCR diagnostic assay. J Clin Microbiol 39: 3871-3876.
25. Jauron, S. D., Nelson, C. M., Fingerle, V., Ravyn, M. D., Goodman, J. L., Johnson, R. C., et al. (2001) Host cell-specific expression of a p44 epitope by the human granulocytic ehrlichiosis agent. J Infect Dis 184: 1445-1450.
26. Keefe, T. J., Holland, C. J., Salyer, P. E., and Ristic, M. (1982) Distribution of Ehrlichia canis among military working dogs in the world and selected civilian dogs in the United States. J Am Vet Med Assoc 181: 236-238.
27. Löhr, C. V., Brayton, K. A., Shkap, V., Molad, T., Barbet, A. F., Brown, W. C., and Palmer, G. H. (2002) Expression of Anaplasma marginale major surface protein 2 operon-associated proteins during mammalian and arthropod infection. Infect Immun 70: 6005-6012.
28. Löhr, C. V., Brayton, K. A., Barbet, A. F., and Palmer, G. H. (2004) Characterization of the Anaplasma marginale msp2 locus and its synteny with the omp1/p30 loci of Ehrlichia chaffeensis and E. canis. Gene 325: 115-121.
29. Long, S. W., Zhang, X. F., Qi, H., Standaert, S., Walker, D. H., and Yu, X. J. (2002) Antigenic variation of Ehrlichia chaffeensis resulting from differential expression of the 28-kilodalton protein gene family. Infect Immun 70: 1824-1831.
30. McBride, J. W., Yu, X. J., and Walker, D. H. (2000) Glycosylation of homologous immunodominant proteins of Ehrlichia chaffeensis and Ehrlichia canis. Infect Immun 68: 13-18.
31. Maniatis, T., Fritsch, E. F., and Sambrook, J. (1982) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
32. Munderloh, U. G., Liu, Y., Wang, M., Chen, C., and Kurtti, T. J. (1994) Establishment, maintenance and description of cell lines from the tick Ixodes scapularis. J Parasitol 80: 533-543.
33. Munderloh, U. G., Madigan, J. E., Dumler, J. S., Goodman, J. L., Hayes, S. F., Barlough, J. E., et al. (1996) Isolation of the equine granulocytic ehrlichiosis agent, Ehrlichia equi, in tick cell culture. J Clin Microbiol 34: 664-670.
34. Munderloh, U. G., Jauron, S. D., Fingerle, V., Leitritz, L., Hayes, S. F., Hautman, J. M., et al. (1999) Invasion and intracellular development of the human granulocytic ehrlichiosis agent in tick cell culture. J Clin Microbiol 37: 2518-2524.
35. Ohashi, N., Zhi, N., Zhang, Y., and Rikihisa, Y. (1998) Immunodominant major outer membrane proteins of Ehrlichia chaffeensis are encoded by a polymorphic multigene family. Infect Immun 66: 132-139.
36. Ohashi, N., Rikihisa, Y., and Unver, A. (2001) Analysis of transcriptionally active gene clusters of major outer membrane protein multigene family in Ehrlichia canis and E. chaffeensis. Infect Immun 69: 2083-2091.
37. Pal, U., Li, X., Wang, T., Montgomery, R. R., Ramamoorthi, N., Desilva, A. M., et al. (2004) TROSPA, an Ixodes scapularis receptor for Borrelia burgdorferi. Cell 119: 457-468.
38. Pantanowitz, L., Telford, S. R., and Cannon, M. E. (2002) Tick-borne diseases in transfusion medicine. Transfus Med 12: 85-106.
39. Reddy, G. R., and Streck, C. P. (1999) Variability in the 28-kDa surface antigen protein multigene locus of isolates of the emerging disease agent Ehrlichia chaffeensis suggests that it plays a role in immune evasion. Mol Cell Biol Res Commun 1: 167-175.
40. Reddy, G. R., Sulsona, C. R., Harrison, R. H., Mahan, S. M., Burridge, M. J., and Barbet, A. F. (1996) Sequence heterogeneity of the major antigenic protein 1 genes from Cowdria ruminantium isolates from different geographical areas. Clin Diag Lab Immunol 3: 417-422.
41. Reddy, G. R., Sulsona, C. R., Barbet, A. F., Mahan, S. M., Burridge, M. J., and Alleman, A. R. (1998) Molecular characterization of a 28 kDa surface antigen gene family of the tribe Ehrlichia. Biochem Biophys Res Commun 247: 636-643.
42. Rikihisa, Y., Ewing, S. A., and Fox, J. C. (1994) Western immunoblot analysis of Ehrlichia chaffeensis, E. canis, or E. ewingii infections in dogs and humans. J Clin Microbiol 32: 2107-2112.
43. Schwan, T. G., Piesman, J., Golde, W. T., Dolan, M. C., and Rosa, P. A. (1995) Induction of an outer surface protein on Borrelia burgdorferi during tick feeding. Proc Natl Acad Sci USA 92: 2909-2913.
44. de Silva, A. M., Telford, S. R., Brunet, L. R., Barthold, S. W., and Fikrig, E. (1996) Borrelia burgdorferi OspA is an arthropod-specific transmission-blocking Lyme disease vaccine. J Exp Med 183: 271-275.
45. Singu, V., Liu, H., Cheng, C., and Ganta, R. R. (2005) Ehrlichia chaffeensis expresses macrophage- and tick cell-specific 28-kilodalton outer membrane proteins. Infect Immun 73: 79-87.
46. Sirigireddy, K. R., and Ganta, R. R. (2005) Multiplex detection of Ehrlichia and Anaplasma species pathogens in peripheral blood by real-time reverse transcriptase-polymerase chain reaction. J Mol Diagn 7: 308-316.
47. Stuen, S., Engvall, E. O., and Artursson, K. (1998) Persistence of Ehrlichia phagocytophila infection in lambs in relation to clinical parameters and antibody responses. Vet Rec 143: 553-555.
48. Unver, A., Ohashi, N., Tajima, T., Stich, R. W., Grover, D., and Rikihisa, Y. (2001) Transcriptional analysis of p30 major outer membrane multigene family of Ehrlichia canis in dogs, ticks, and cell culture at different temperatures. Infect Immun 69: 6172-6178.
49. Unver, A., Rikihisa, Y., Stich, R. W., Ohashi, N., and Felek, S. (2002) The omp-1 major outer membrane multigene family of Ehrlichia chaffeensis is differentially expressed in canine and tick hosts. Infect Immun 70: 4701-4704.
50. Van, H. H., Collins, N. E., Brayton, K. A., Rademeyer, C., and Allsopp, B. A. (2004) Characterization of a major outer membrane protein multigene family in Ehrlichia ruminantium. Gene 330: 159-168.
51. Yu, X. J., McBride, J. W., Zhang, X., and Walker, D. H. (2000) Characterization of the complete transcriptionally active Ehrlichia chaffeensis 28 kDa outer membrane protein multigene family. Gene 248: 59-68.
52. Zhi, N., Ohashi, N., and Rikihisa, Y. (1999) Multiple p44 genes encoding major outer membrane proteins are expressed in the human granulocytic ehrlichiosis agent. J Biol Chem 274: 17828-17836.