The mouse as a model for investigation of human granulocytic ehrlichiosis: Current knowledge and future directions

Comparative Medicine

Volumn 52, Issue 5, 2002, Pages 403-413

  Borjesson, Dori L ^a   Barthold, Stephen W ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANAPLASMA; ANAPLASMA PHAGOCYTOPHILA; ANIMAL EXPERIMENT; ANIMAL MODEL; EHRLICHIOSIS; EXPERIMENTAL ANIMAL; GRANULOCYTE; HUMAN; IMMUNE RESPONSE; MOUSE; NEUTROPHIL; NONHUMAN; REVIEW; TICK BORNE DISEASE; TRANSGENIC MOUSE; ZOONOSIS;

ANAPLASMA PHAGOCYTOPHILUM; ANIMALS; CYTOKINES; DISEASE MODELS, ANIMAL; EHRLICHIOSIS; GRANULOCYTES; HUMANS; MICE; RODENT DISEASES;

EID: 0036775385     PISSN: 00236764     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (94)

1. Gordon, W. S., A. Brownlee, D. R. Wilson, and J. MacLeod. 1932. Tick-borne fever (a hitherto undescribed disease of sheep). J. Comp. Pathol. 45:301-312.
2. Buller, R. S., M. Arens, S. P. Hmiel, C. D. Paddock, J. W. Sumner, Y. Rikhisa, A. Unver, M. Gaudreault-Keener, F. A. Manian, A. M. Liddell, N. Schmulewitz, and G. A. Storch. 1999. Ehrlichia ewingii, a newly recognized agent of human ehrlichiosis. N. Engl. J. Med. 341:148-155.
3. Walker, D. H. and J. S. Dumler. 1996. Emergence of the ehrlichioses as human health problems. Emerg. Infect. Dis. 2:18- 29.
4. 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.
5. Goodman, J. L., C. Nelson, B. Vitale, J. E. Madigan, J. S. Dumler, T. J. Kurtti, and U. G. Munderloh. 1996. Direct cultivation of the causative agent of human granulocytic ehrlichiosis. N. Engl. J. Med. 334:209-215.
6. 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.
7. Barthold, S.W. 2000. Lyme borreliosis, p. 281-304. In J. P. Nataro, M. J. Blaser, and S. Cunningham (ed.), Persistent Bacterial Infections. ASM Press, Washington, D.C.
8. Bakken, J. S., J. Krueth, C. Wilson-Nordskog, R. L. Tilden, K Asanovich, and J. S. Dumler. 1996. Clinical and laboratory characteristics of human granulocytic ehrlichiosis. Jama 275:199-205.
9. Dumler, J. S. and J. S. Bakken. 1995. Ehrlichial diseases of humans: Emerging tick-bome infections. Clin. Infect. Dis. 20:1102-1110.
10. Bakken, J. S., M. E. Aguero-Rosenfeld, R. L. Tilden, G. P. Wormser, H. W. Horowitz, J. T. Raffalli, M. Baluch, D. Riddell, J. J. Walls, and J. S. Dumler. 2001. Serial measurements of hematologic counts during the active phase of human granulocytic ehrlichiosis. Clin. Infect. Dis. 32:862-870.
11. Brouqui, P. and D. Raoult. 1995. Human ehrlichiosis with features of toxic shock syndrome. Am. J. Med. 99:107.
12. Fichtenbaum, C. J., L. R. Peterson, and G. J. Weil. 1993. Ehrlichiosis presenting as a life-threatening illness with features of the toxic shock syndrome. Am. J. Med. 95:351-357.
13. Hardalo, C. J., V. Quagliarello, and J. S. Dumler. 1995. Human granulocytic ehrlichiosis in Connecticut: Report of a fatal case. Clin. Infect. Dis. 21:910-914.
14. Jahangir, A., C. Kolbert, W. Edwards, P. Mitchell, J. S. Dumler, and D. H. Persing. 1998. Fatal pancarditis associated with human granulocytic Ehrlichiosis in a 44-year-old man. Clin. Infect. Dis. 27:1424-1427.
15. Patel, R. G. and M. A. Byrd. 1999. Near fatal acute respiratory distress syndrome in a patient with human ehrlichiosis. South Med. J. 92:333-335.
16. Pick, N., I. Potasman, C. Strenger, A. Keysary, and I. Schwartz. 2000. Ehrlichiosis associated vasculitis. J. Intern. Med. 247:674-678.
17. Behl, R., M. B. Klein, L. Dandelet, R. R. Bach, J. L. Goodman, and N. S. Key. 2000. Induction of tissue factor procoagulant activity in myelomonocytic cells inoculated by the agent of human granulocytic ehrlichiosis. Thromb. Haemost. 83:114-118.
18. Woldehiwet, Z. 1987. The effects of tick-borne fever on some functions of polymorphonuclear cells of sheep. J. Comp. Pathol. 97:481-485.
19. Pusterla, N. and U. Braun. 1997. Clinical findings in cows after experimental infection with Ehrlichia phagocytophila. Zentralbl. Veterinarmed. A. 44:385-390.
20. Woldehiwet, Z. 1983. Tick-borne fever: A review. Vet. Res. Commun. 6:163-175.
21. Pusterla, N., J. B. Pusterla, U. Braun, and H. Lutz. 1999. Experimental cross-infections with Ehrlichia phagocytophila and human granulocytic ehrlichia-like agent in cows and horses. Vet. Rec. 145:311-314.
22. Jones, G. L. and I. H. Davies. 1995. An ovine abortion storm caused by infection with Cytoecetes phagocytophila. Vet. Rec. 136:127.
23. Foggie, A. 1951. Studies on the infectious agent of tick-borne fever in sheep. J. Pathol. Bacteriol. 63:1-15.
24. Foggie, A. 1956. The effects of tick-borne fever infection on the susceptiblity of lambs to staphylococci. J. Comp. Pathol. 66:278-285.
25. Gronstol, H. and M. J. Ulvand. 1977. Listeric septicaemia in sheep associated with tick-borne fever (Ehrlichia phagocytophila). Acta Vet. Scand. 18:575-577.
26. Macleod, J. and W. S. Gordon. 1933. Studies of tick-borne fever of sheep. Transmission by the tick Ixodes ricinus with a description of the disease produced. Parasitology 25:273-283.
27. Munro, R.,A. R. Hunter, G. MacKenzie, and D.A. McMartin. 1982. Pulmonary lesions in sheep following experimental infection by Ehrlichia phagocytophilia and Chlamydia psittaci. J. Comp. Pathol. 92:117-129.
28. Gilmour, J. L., T. A. Brodie, and P. H. Holmes. 1982. Tickborne fever and pasteurellosis in sheep. Vet. Rec. 111:512.
29. Batungbacal, M. R., and G. R. Scott. 1982. Tick-borne fever and concurrent parainfluenza-3 virus infection in sheep. J. Comp. Pathol. 92:415-428.
30. Ogden, N. H., Z. Woldehiwet, and C. A. Hart. 1998. Granulocytic ehrlichiosis: An emerging or rediscovered tick-borne disease? J. Med. Microbiol. 47:475-82.
31. Gribble, D. H. 1969. Equine ehrlichiosis. J. Am. Vet. Med. Assoc. 155:462-469.
32. Madigan, J. E., P. J. Richter, Jr., R. B. Kimsey, J. E. Barlough, J. S. Bakken, and J. S. Dumler. 1995. Transmission and passage in horses of the agent of human granulocytic ehrlichiosis. J. Infect. Dis. 172:1141-1144.
33. Madigan, J. E., and D. Gribble. 1987. Equine ehrlichiosis in northern California: 49 Cases (1968-1981). J. Am. Vet. Med. Assoc. 190:445-458.
34. Madigan, J. E., J. E. Barlough, J. S. Dumler, N. S. Schankman, and E. DeRock. 1996. Equine granulocytic ehrlichiosis in Connecticut caused by an agent resembling the human granulocytotropic ehrlichia. J. Clin. Microbiol. 34:434-435.
35. Stannard,A. A., D. H. Gribble, and R. S. Smith. 1969. Equine ehrlichiosis: A disease with similarities to tick-borne fever and bovine petechial fever. Vet. Rec. 84:149-150.
36. Madigan, J. E., S. Hietala, S. Chalmers, and E. DeRock. 1990. Seroepidemiologic survey of antibodies to Ehrlichia equi in horses of northern California. J. Am. Vet. Med. Assoc. 196:1962-1964.
37. Lepidi, H., J. E. Bunnell, M. E. Martin, J. E. Madigan, S. Stuen, and J. S. Dumler. 2000. Comparative pathology, and immunohistology associated with clinical illness after Ehrlichia phagocytophila-group infections. Am. J. Trop. Med. Hyg. 62:29-37.
38. Ewing S. A., R. G. Buckner, and C. S. Hayat. 1971. A new strain of Ehrlichia canis. J. Am. Vet. Med. Assoc. 159:1771-1774.
39. Anderson, B. E., C. E. Greene, D. C. Jones, and J. E. Dawson. 1992. Ehrlichia ewingii sp. nov., the etiologic agent of canine granulocytic ehrlichiosis. Int. J. Syst. Bacteriol. 42:299-302.
40. Bellah, J. R., R. M. Shull, and E. V. Selcer. 1986. Ehrlichia canis-related polyarthritis in a dog. J. Am. Vet. Med. Assoc. 189:922-923.
41. Goldman, E. E., E. B. Breitschwerdt, C. B. Grindem, B. C. Hegarty, J. J. Walls, and J. S. Dumler. 1998. Granulocytic ehrlichiosis in dogs from North Carolina and Virginia. J. Vet. Intern. Med. 12:61-70.
42. Stockham, S. L., D. A. Schmidt, K. S. Curtis, B. G. Schauf, J. W. Tyler, and S. T. Simpson. 1992. Evaluation of granulocytic ehrlichiosis in dogs of Missouri, including serologic status to Ehrlichia canis, Ehrlichia equi, and Borrelia burgdorferi. Am. J. Vet. Res. 53:63-68.
43. Cowell, R. L., R. D. Tyler, K. D. Clinkenbeard, and J. H. Meinkoth. 1988. Ehrlichiosis and polyarthritis in three dogs. J. Am. Vet. Med. Assoc. 192:1093-1095.
44. Maretzki, C. H., D. J. Fisher, and C. E. Greene. 1994. Granulocytic ehrlichiosis and meningitis in a dog. J. Am. Vet. Med. Assoc. 205:1554-1556.
45. Lewis, G. E., Jr., D. L. Huxsoll, M. Ristic, and A. J. Johnson. 1975. Experimentally induced infection of dogs, cats, and nonhuman primates with Ehrlichia equi, etiologic agent of equine ehrlichiosis. Am. J. Vet. Res. 36:85-88.
46. Madewell, B. R. and D. H. Gribble. 1982. Infection in two dogs with an agent resembling Ehrlichia equi. J. Am. Vet. Med. Assoc. 180:512-514.
47. Greig, B., K. M. Asanovich, P. J. Armstrong, and J. S. Dumler. 1996. Geographic, clinical, serologic, and molecular evidence of granulocytic ehrlichiosis, a likely zoonotic disease, in Minnesota and Wisconsin dogs. J. Clin. Microbiol. 34:44-48.
48. Magnarelli, L. A., J. W. Ijdo, J. F. Anderson, J. E. Madigan, J. S. Dumler, and E. Fikrig. 1997. Antibodies to Ehrlichia equi in dogs from the northeastern United States. J Am. Vet. Med. Assoc. 211:1134-1137.
49. Egenvall, A., A. Bjoersdorff, I. Lilliehook, E. Olsson Engvall, E. Karlstam, K. Artursson, A. Hedhammar, and A. Gunnarsson. 1998. Early manifestations of granulocytic ehrlichiosis in dogs inoculated experimentally with a Swedish Ehrlichia species isolate. Vet. Rec. 143:412-417.
50. Telford, S. R., 3rd, J. E. Dawson, P. Katavolos, C. K. Warner, C. P. Kolbert, and D. H. Persing. 1996. Perpetuation of the agent of human granulocytic ehrlichiosis in a deer tick-rodent cycle. Proc. Natl. Acad. Sci. USA 93:6209-6214.
51. Hodzic, E., J. W. Ijdo, S. Feng, P. Katavolos, W. Sun, C. H. Maretzki, D. Fish, E. Fikrig, S. R. Telford, 3rd, and S. W. Barthold. 1998. Granulocytic ehrlichiosis in the laboratory mouse. J. Infect. Dis. 177:737-745.
52. Borjesson, D. L., S. I. Simon, F. Tablin, and S. W. Barthold. 2001. Thrombocytopenia in a mouse model of human granulocytic ehrlichiosis. J. Infect. Dis. 184:1475-1479.
53. Martin, M. E., J. E. Bunnell, and J. S. Dumler. 2000. Pathology, immunohistology, and cytokine responses in early phases of human granulocytic ehrlichiosis in a murine model. J. Infect. Dis. 181:374-378.
54. Herron, M. J., C. M. Nelson, J. Larson, K. R. Snapp, G. S. Kansas, and J. L. Goodman. 2000. Intracellular parasitism by the human granulocytic ehrlichiosis bacterium through the Pselectin ligand, PSGL-1. Science 288:1653-1656.
55. Goodman, J. L., C. M. Nelson, M. B. Klein, S. F. Hayes, and B. W. Weston. 1999. Leukocyte infection by the granulocytic ehrlichiosis agent is linked to expression of a selectin ligand. J. Clin. Invest. 103:407-412.
56. McEver, R. P. and R. D. Cummings. 1997. Perspectives series: Cell adhesion in vascular biology. Role of PSGL-1 binding to selectins in leukocyte recruitment. J. Clin. Invest. 100:485-491.
57. Yang, J., B. C. Furie, and B. Furie. 1999. The biology of P-selectin glycoprotein ligand-1: Its role as a selectin counterreceptor in leukocyte-endothelial and leukocyte-platelet interaction. Thromb. Haemost. 81:1-7.
58. Blanks, J. E., T. Moll, R. Eytner, and D. Vestweber. 1998. Stimulation of P-selectin glycoprotein ligand-1 on mouse neutrophils activates beta 2-integrin mediated cell attachment to ICAM-1. Eur. J. Immunol. 28:433-443.
59. Webster, P., L. M. Chicoine, and E. Fikrig. 1998. The agent of human granulocytic ehrlichiosis resides in an endosomal compartment. J. Clin. Invest. 101:1932-1941.
60. 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.
61. Gokce, H. I., G. Ross, and Z. Woldehiwet. 1999. Inhibition of phagosome-lysosome fusion in ovine polymorphonuclear leucocytes by Ehrlichia (Cytoecetes) phagocytophila. J. Comp. Pathol.120:369-381.
62. 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.
63. Bozue, J. A. and W. Johnson. 1996. Interaction of Legionella pneumophila with Acanthamoeba castellanii: Uptake by coiling phagocytosis and inhibition of phagosome-lysosome fusion. Infect Immun. 64:668-773.
64. Clemens, D. L. and M. A. Horwitz. 1996. The Mycobacterium tuberculosis phagosome interacts with early endosomes and is accessible to exogenously administered transferrin. J. Exp. Med. 184:1349-1355.
65. Wells, M. Y. and Y. Rikihisa. 1988. Lack of lysosomal fusion with phagosomes containing Ehrlichia risticii in P388D1 cells: abrogation of inhibition with oxytetracycline. Infect Immun. 56:3209-3215.
66. Klein, M. B., J. S. Miller, C. M. Nelson, and J. L. Goodman. 1997. Primary bone marrow progenitors of both granulocytic and monocytic lineages are susceptible to infection with the agent of human granulocytic ehrlichiosis. J. Infect Dis. 176:1405-1409.
67. Bunnell, J. E., L. A. Magnarelli, and J. S. Dumler. 1999. Infection of laboratory mice with the human granulocytic ehrlichiosis agent does not induce antibodies to diagnostically significant Borrelia burgdorferi antigens. J. Clin. Microbiol. 37:2077-2079.
68. Hodzic, E., S. Feng, D. Fish, C. M. Leutenegger, K. J. Freet, and S. W. Barthold. 2001. Infection of mice with the agent of human granulocytic ehrlichiosis after different routes of inoculation. J. Infect. Dis. 183:1781-1786.
69. Yoshiie, K., H. Y. Kim, J. Mott, and Y. Rikihisa. 2000. Intracellular infection by the human granulocytic ehrlichiosis agent inhibits human neutrophil apoptosis. Infect. Immun. 68:1125-1133.
70. Banerjee, R., J. Anguita, D. Roos, and E. Fikrig. 2000. Cutting edge: Infection by the agent of human granulocytic ehrlichiosis prevents the respiratory burst by down-regulating gp91phox. J. Immunol. 164:3946-3949.
71. Mott, J. and Y. Rikihisa. 2000. Human granulocytic ehrlichiosis agent inhibits superoxide anion generation by human neutrophils. Infect. Immun. 68:6697-6703.
72. Banerjee, R., J. Anguita, and E. Fikrig. 2000. Granulocytic ehrlichiosis in mice deficient in phagocyte oxidase or inducible nitric oxide synthase. Infect. Immun. 68:4361-4362.
73. Akkoyunlu, M. and E. Fikrig. 2000. Gamma interferon dominates the murine cytokine response to the agent of human granulocytic ehrlichiosis and helps to control the degree of early rickettsemia. Infect. Immun. 68:1827-1833.
74. Borjesson, D. L., S. I. Simon, E. Hodzic, C. M. Ballantyne, and S. W. Barthold. 2002. Kinetics of CD11b/CD18 upregulation during infection with the agent of human granulocytic ehrlichiosis in mice. Lab. Invest. 82:303-311.
75. Borjesson, D. L., S. I. Simon, E. Hodzic, H. E. V. DeCock, C. M. Ballantyne, and S. W. Barthold. 2002. Roles of neutrophil B2 integrins in kinetics of bacteremia, extravasation and tick acquisition of Anaplasma phagocytophila in mice. Blood (In review).
76. Akkoyunlu, M., S. E. Malawista, J. Anguita, and E. Fikrig. 2001. Exploitation of interleukin-8-induced neutrophil chemotaxis by the agent of human granulocytic ehrlichiosis. Infect. Immun. 69:5577-5588.
77. Hodzic, E., D. L. Borjesson, S. Feng and S.W. Barthold. 2001. Acquisition dynamics of Borrelia burgdorferi and the agent of human granulocytic ehrlichiosis at the host-vector interface. Vector Borne Zoonot. Dis. 1:149-158.
78. Iqbal, Z. and Y. Rikihisa. 1994. Reisolation of Ehrlichia canis from blood and tissues of dogs after doxycycline treatment. J. Clin. Microbiol. 32:1644-1649.
79. Barbet, A. F., S. M. Semu, N. Chigagure, P. J. Kelly, F. Jongejan, and S. M. Mahan. 1994. Size variation of the major immunodominant protein of Cowdria ruminantium. Clin. Diagn. Lab. Immunol. 1:744-746.
80. Brouqui, P., J. S. Dumler, D. Raoult, and D. H. Walker. 1992. Antigenic characterization of ehrlichiae: Protein immunoblotting of Ehrlichia canis, Ehrlichia sennetsu, and Ehrlichia risticii. J. Clin. Microbiol. 30:1062-1066.
81. Eriks, I. S., G. H. Palmer, T. C. McGuire, D. R. Allred, and A. F. Barbet. 1989. Detection and quantitation of Anaplasma marginale in carrier cattle by using a nucleic acid probe. J. Clin. Microbiol 27:279-284.
82. Ijdo,J. W.,W. Sun,Y. Zhang, L. A. Magnarelli, and E. Fikrig. 1998. Cloning of the gene encoding the 44-kilodalton antigen of the agent of human granulocytic ehrlichiosis and characterization of the humoral response. Infect. Immun. 66:3264-3269.
83. French, D. M., W. C. Brown, and G. H. Palmer. 1999. Emergence of Anaplasma marginale antigenic variants during persistent rickettsemia. Infect Immun. 67:5834-5840.
84. Egenvall, A., I. Lilliehook, A. Bjoersdorff, E. O. Engvall, E. Karlstam, K. Artursson, M. Heldtander, and A. Gunnarsson. 2000. Detection of granulocytic Ehrlichia species DNA by PCR in persistently infected dogs. Vet. Rec. 146:186-190.
85. Dumler, J. S. and J. S. Bakken. 1996. Human granulocytic ehrlichiosis in Wisconsin and Minnesota: A frequent infection with the potential for persistence. J. Infect Dis. 173:1027-1030.
86. Wong, S. J. and J. A. Thomas. 1998. Cytoplasmic, nuclear, and platelet autoantibodies in human granulocytic ehrlichiosis patients. J. Clin Microbiol. 36:1959-1963.
87. Batungbacal, M. R., G. R. Scott, and C. Burrells. 1982. The lymphocytopaenia in tick-bome fever. J. Comp. Pathol. 92:403-407.
88. Woldehiwet, Z. 1991. Lymphocyte subpopulations in peripheral blood of sheep experimentally infected with tick-borne fever. Res. Vet Sci. 51:40-43.
89. Woldehiwet, Z. 1987. Depression of lymphocyte response to mitogens in sheep infected with tick-bome fever. J. Comp. Pathol. 97:637-643.
90. Bunnell, J. E., E. R. Trigiani, S. R. Srinivas, and J. S. Dumler. 1999. Development and distribution of pathologic lesions are related to immune status and tissue deposition of human granulocytic ehrlichiosis agent-infected cells in a murine model system. J. Infect. Dis. 180:546-550.
91. Kim, H. Y. and Y. Rikihisa. 2000. Expression of interleukin1beta, tumor necrosis factor alpha, and interleukin-6 in human peripheral blood leukocytes exposed to human granulocytic ehrlichiosis agent or recombinant major surface protein P44. Infect. Immun. 68:3394-3402.
92. Klein, M. B., S. Hu, C. C. Chao, and J. L. Goodman. 2000. The agent of human granulocytic ehrlichiosis induces the production of myelosuppressing chemokines without induction of proinflammatory cytokines. J. Infect. Dis 182:200-205.
93. Martin, M. E., K. Caspersen, and J. S. Dumler. 2001. Immunopathology and ehrlichial propagation are regulated by interferon-gamma and interleukin-10 in a murine model of human granulocytic ehrlichiosis. Am. J. Pathol. 158:1881-1888.
94. Hodzic, E., S. Feng, and S. W. Barthold. Unpublished data.