Differential clearance and immune responses to tick cell-derived versus macrophage culture-derived Ehrlichia chaffeensis in mice

Infection and Immunity

Volumn 75, Issue 1, 2007, Pages 135-145

  Ganta, Roman R ^a   Cheng, Chuanmin ^a   Miller, Elizabeth C ^a   McGuire, Bridget L ^a   Peddireddi, Lalitha ^a   Sirigireddy, Kamesh R ^a   Chapes, Stephen K ^a  

^a KANSAS STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ANTIGEN; CYTOKINE; HERMES ANTIGEN; IMMUNOGLOBULIN G; INTERLEUKIN 6; L SELECTIN; NITRIC OXIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL GENE; BACTERIAL GENETICS; BACTERIAL GROWTH; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOKINE RELEASE; EHRLICHIA CHAFFEENSIS; EHRLICHIOSIS; EXPERIMENTAL INFECTION; GENE EXPRESSION; HOST RESISTANCE; IMMUNE RESPONSE; IMMUNOPATHOGENESIS; LIVER; MACROPHAGE; MOUSE; NONHUMAN; OMP 14 GENE; OMP 19 GENE; PERITONEUM; PERITONEUM MACROPHAGE; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPLEEN; TICK; TISSUE DISTRIBUTION;

ANIMALS; BACTERIAL OUTER MEMBRANE PROTEINS; BLOTTING, WESTERN; CELLS, CULTURED; DISEASE MODELS, ANIMAL; DOGS; EHRLICHIA CHAFFEENSIS; EHRLICHIOSIS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; IMMUNOGLOBULIN G; MACROPHAGE ACTIVATION; MACROPHAGES; MICE; MICE, INBRED C57BL; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; T-LYMPHOCYTES; TICKS;

EID: 33846003533     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.01127-06     Document Type: Article

References (59)

1. Adachi, Y., A. L. Kindzelskii, N. Ohno, T. Yadomae, and H. R. Petty. 1999. Amplitude and frequency modulation of metabolic signals in leukocytes: synergistic role of IFN-gamma in IL-6- and IL-2-mediated cell activation. J. Immunol. 163:4367-4374.
2. Anderson, B. E., K. G. Sims, J. G. Olson, J. E. Childs, J. F. Piesman, C. M. Happ, G. O. Maupin, and B. J. Johnson, 1993. Amblyomma americanum: a potential vector of human ehrlichiosis. Am. J. Trop. Med. Hyg. 49:239-244.
3. Andrew, H. R., and R. A. Norval. 1989. The carrier status of sheep, cattle, and African buffalo recovered from heartwater. Vet. Parasitol. 34:261-266.
4. Barbet, A. F., A. Lundgren, J. Yi, F. R. Rurangirwa, and G. H. Palmer. 2000. Antigenic variation of Anaplasma marginale by expression of MSP2 mosaics. Infect. Immun. 68:6133-6138.
5. Bitsaktsis, C., J. Huntington, and G. Winslow. 2004. Production of IFN-gamma by CD4 T cells is essential for resolving ehrlichia infection. J. Immunol. 172:6894-6901.
6. Bonecchi, R., S. Sozzani, J. T. Stine, W. Luini, G. D'Amico, P. Allavena, D. Chantry, and A. Mantovani. 1998. Divergent effects of interleukin-4 and interferon-gamma on macrophage-derived chemokine production: an amplification circuit of polarized T helper 2 responses. Blood 92:2668-2671.
7. Brayton, K. A., P. F. Meeus, A. F. Barbet, and G. H. Palmer. 2003. Simultaneous variation of the immunodominant outer membrane proteins, MSP2 and MSP3, during Anaplasma marginale persistence in vivo. Infect. Immun. 71:6627-6632.
8. Chapes, S. K., and A. A. Beharka, 1995. Lipopolysaccharide is required for the lethal effects of enterotoxin B after D-galactosamine sensitization. J. Endotoxin Res. 2:263-271.
9. Chen, S. M., V. L. Popov, H. M. Feng, J. Wen, and D. H. Walker. 1995. Cultivation of Ehrlichia chaffeensis in mouse embryo, Vero, BGM, and L929 cells and study of Ehrlichia-induced cytopathic effect and plaque formation. Infect. Immun. 63:647-655.
10. Davidson, W. R., J. M. Lockhart, D. E. Stallknecht, E. W. Howerth, J. E. Dawson, and Y. Rechav. 2001. Persistent Ehrlichia chaffeensis infection in white-tailed deer. J. Wildl. Dis. 37:538-546.
11. Dawson, J. E., B. E. Anderson, D. B. Fishbein, C. Y. Sanchez, C. Y. Goldsmith, K. H. Wilson, and C. W. Duntley. 1991. Isolation and characterization of an Ehrlichia sp. from a patient diagnosed with human ehrlichiosis. J. Clin. Microbiol. 29:2741-2745.
12. Dawson, J. E., K. L. Biggie, C. K. Warner, K. Cookson, S. Jenkins, J. F. Levine, and J. G. Olson. 1996. Polymerase chain reaction evidence of Ehrlichia chaffeensis, an etiologic agent of human erlichiosis, in dogs from southeast Virginia. Am. J. Vet. Res. 57:1175-1179.
13. Dawson, J. E., J. E. Childs, K. L. Biggie, C. Moore, D. Stallknecht, J. Shaddock, J. Bouseman, E. Hofmeister, and J. G. Olson. 1994. White-tailed deer as a potential reservoir of Ehrlichia spp. J. Wildl. Dis. 30:162-168.
14. De, S. A., S. R. Telford, L. R. Brunet, S. W. Barthold, and E. Fikrig. 1996. Borrelia burgdorferi OspA is an arthropod-specific transmission-blocking Lyme disease vaccine. J. Exp. Med. 183:271-275.
15. Dumler, J. S., A. F. Barbet, C. P. Bekker, G. A. Dasch, G. H. Palmer, S. C. Ray, Y. Rikihisa, and F. R. Rurangirwa. 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.
16. Dumler, J. S., W. L. Sutker, and D. H. Walker. 1993. Persistent Infection with Ehrlichia chaffeensis. Clin. Infect. Dis. 17:903-905.
17. Felek, S., A. Unver, R. W. Stich, and Y. Rikihisa. 2003. Sensitive detection of Ehrlichia chaffeensis in cell culture, blood, and tick specimens by reverse transcription-PCR. J. Clin. Microbiol. 39:460-463.
18. Feng, H. M., and D. H. Walker. 2004. Mechanisms of immunity to Ehrlichia muris: a model of monocytotropic ehrlichiosis. Infect. Immun. 72:966-971.
19. Ferreira, B. R., and J. S. Silva. 1998. Saliva of Rhipicephalus sanguineus tick impairs T-cell proliferation and IFN-gamma-induced macrophage microbicidal activity. Vet. Immunol. Immunopathol. 64:279-293.
20. Ferreira, B. R., and J. S. Silva. 1999. Successive tick infestations selectively promote a T-helper 2 cytokine profile in mice. Immunology 96:434-439.
21. Fikrig, E., U. Pal, M. Chen, J. F. Anderson, and R. A. Flavell. 2004. OspB antibody prevents Borrelia burgdorferi colonization of Ixodes scapularis. Infect. Immun. 72:1755-1759.
22. Fingerle, V., S. Rauser, B. Hammer, O. Kahl, C. Heimerl, U. Schulte-Spechtel, L. Gern, and B. Wilske. 2002. Dynamics of dissemination and outer surface protein expression of different European Borrelia burgdorferi sensu lato strains in artificially infected Ixodes ricinus nymphs. J. Clin. Microbiol. 40:1456-1463.
23. French, D. M., T. F. McElwain, T. C. McGuire, and G. H. Palmer. 1998. Expression of Anaplasma marginale major surface protein 2 variants during persistent cyclic rickettsemia. Infect. Immun. 66:1200-1207.
24. + T-cell knockout mice. Infect. Immun. 72:159-167.
25. Ganta, R. R., M. J. Wilkerson, C. Cheng, A. M. Rokey, and S. K. Chapes. 2002. Persistent Ehrlichia chaffeensis infection occurs in the absence of functional major histocompatibility complex class II genes. Infect. Immun. 70: 380-388.
26. Garcia-Garcia, J. C., J. de la Fuente, E. F. Blouin, T. J. Johnson, T. Halbur, V. C. Onet, J. T. Saliki, and K. M. Kocan. 2004. Differential expression of the msp1alpha gene of Anaplasma marginale occurs in bovine erythrocytes and tick cells. Vet. Microbiol. 98:261-272.
27. Gillespie, R. D., M. L. Mbow, and R. G. Titus. 2000. The immunomodulatory factors of bloodfeeding arthropod saliva. Parasite. Immunol. 22:319-331.
28. Harvey, J. W., C. F. Simpson, and J. M. Gaskin. 1978. Cyclic thrombocytopenia induced by a Rickettsia-like agent in dogs. J. Infect. Dis. 137:182-188.
29. Hasegawa, K., F. Martin, G. Huang, D. Tumas, L. Diehl, and A. C. Chan. 2004. PEST domain-enriched tyrosine phosphatase (PEP) regulation of effector/memory T cells. Science 303:685-689.
30. Inokuma, H., R. L. Kerlin, D. H. Kemp, and P. Willadsen. 1993. Effects of cattle tick (Boophilus microplus) infestation on the bovine immune system. Vet. Parasitol. 47:107-118.
31. + Th1 cells contribute to toxic shock-like syndrome in an animal model of fatal monocytotropic ehrlichiosis. J. Immunol. 172:1786-1800.
32. Jiao, X., R. Lo-Man, N. Winter, E. Deriaud, B. Gicquel, and C. Leclerc. 2003. The shift of Th1 to Th2 immunodominance associated with the chronicity of Mycobacterium bovis bacille Calmette-Guerin infection does not affect the memory response. J. Immunol. 170:1392-1398.
33. Kieser, S. T., I. S. Eriks, and G. H. Palmer. 1990. Cyclic rickettsemia during persistent Anaplasma marginale infection of cattle. Infect. Immun. 58:1117-1119.
34. Kindzelskii, A. L., and H. R. Petty. 1999. Early membrane rupture events during neutrophil-mediated antibody-dependent tumor cell cytolysis. J. Immunol. 162:3188-3192.
35. Kindzelskii, A. L., and H. R. Petty. 2002. Apparent role of traveling metabolic waves in oxidant release by living neutrophils. Proc. Natl. Acad. Sci. USA 99:9207-9212.
36. Klouche, M., S. Bhakdi, M. Hemmes, and S. Rose-John. 1999. Novel path to activation of vascular smooth muscle cells: up-regulation of gp130 creates an autocrine activation loop by IL-6 and its soluble receptor. J. Immunol. 163:4583-4589.
37. Lau, L. L., B. D. Jamieson, T. Somasundaram, and R. Ahmed. 1994. Cytotoxic T-cell memory without antigen. Nature 369:648-652.
38. Maniatis, T., E. F. Fritsch, and J. Sambrook. 1982. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
39. Munderloh, U. G., Y. Liu, M. Wang, C. Chen, and T. J. Kurtti. 1994. Establishment, maintenance and description of cell lines from the tick Ixodes scapularis. J. Parasitol. 80:533-543.
40. Paddock, C. D., and J. E. Childs. 2003. Ehrlichia chaffeensis: a prototypical emerging pathogen. Clin. Microbiol. Rev. 16:37-64.
41. Pal, U., X. Yang, M. Chen, L. K. Bockenstedt, J. F. Anderson, R. A. Flavell, M. V. Norgard, and E. Fikrig. 2004. OspC facilitates Borrelia burgdorferi invasion of Ixodes scapularis salivary glands. J. Clin. Investig. 113:220-230.
42. Rikihisa, Y. 1991. The tribe Ehrlichieae and ehrlichial diseases. Clin. Microbiol. Rev. 4:286-308.
43. AL, p. 704-711. In N. R. Krieg and J. G. Holt (ed.), Bergey's manual of systematic bacteriology, vol. 1. The Williams & Wilkins Co., Baltimore, MD.
44. Sallusto, F., D. Lenig, R. Forster, M. Lipp, and A. Lanzavecchia. 1999. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 401:708-712.
45. Schwan, T. G., J. Piesman, W. T. Golde, M. C. Dolan, and P. A. Rosa. 1995. Induction of an outer surface protein on Borrelia burgdorferi during tick feeding. Proc. Natl. Acad. Sci. USA 92:2909-2913.
46. Singu, V., H. Liu, C. Cheng, and R. R. Ganta. 2005. Ehrlichia chaffeensis expresses macrophage- and tick cell-specific 28-kilodalton outer membrane proteins. Infect. Immun. 73:79-87.
47. Singu, V., L. Peddireddi, K. R. Sirigireddy, C. Cheng, U. G. Munderloh, and R. R. Ganta. 2006. Unique macrophage and tick cell-specific protein expression from the p28/p30 Omp multigene locus in Ehrlichia species. Cell Microbiol. 8:1475-1487.
48. Sirigireddy, K. R., and R. R. Ganta. 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.
49. Sonenshine, D. E. 1991. Biology of ticks, vol. 1, p. 51-64. Oxford University Press, Oxford, United Kingdom.
50. Stamler, J. S., D. J. Singel, and J. Loscalzo. 1992. Biochemistry of nitric oxide and its redox-activated forms. Science 258:1898-1902.
51. Stuehr, D. J., and C. F. Nathan. 1989. Nitric oxide. A macrophage product responsible for cytostasis and respiratory inhibition in tumor target cells. J. Exp. Med. 169:1543-1555.
52. Stuen, S., E. O. Engvall, and K. Artursson. 1998. Persistence of Ehrlichia phagocytophila infection in lambs in relation to clinical parameters and antibody responses. Vet. Rec. 143:553-555.
53. Unver, A., Y. Rikihisa, R. W. Stich, N. Ohashi, and S. Felek. 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.
54. Wigginton, J. E., and D. Kirschner. 2001. A model to predict cell-mediated immune regulatory mechanisms during human infection with Mycobacrerium tuberculosis. J. Immunol. 166:1951-1967.
55. Wikel, S. K. 1999. Tick modulation of host immunity: an important factor in pathogen transmission. Int. J. Parasitol. 29:851-859.
56. Winslow, G. M., E. Yager, K. Shilo, E. Volk, A. Reilly, and F. K. Chu. 2000. Antibody-mediated elimination of the obligate intracellular bacterial pathogen Ehrlichia chaffeensis during active infection. Infect. Immun. 68:2187-2195.
57. Wodarz, D., K. M. Page, R. A. Arnaout, A. R. Thomsen, J. D. Lifson, and M. A, Nowak. 2000. A new theory of cytotoxic T-lymphocyte memory: implications for HIV treatment. Philos. Trans. R. Soc. Lond. B Biol. Sci. 355:329-343.
58. Zhang, J., J. M. Hardham, A, G. Barbour, and S. J. Nords. 1997. Antigenic Variation in Lyme disease borreliae by promiscuous recombination of VMP-like sequence cassettes. Cell 89:275-285.
59. Zhang, X. F., J. Z. Zhang, S. W. Long, R. P. Ruble, and X. J. Yu. 2003. Experimental Ehrlichia chaffeensis infection in beagles. J. Med. Microbiol. 52:1021-1026.