Role of reactive nitrogen species in development of hepatic injury in a C57BL/6 mouse model of human granulocytic anaplasmosis

Comparative Medicine

Volumn 56, Issue 1, 2006, Pages 55-62

  Browning, Michelle D ^a   Garyu, Justin W ^a   Dumler, J Stephen ^a   Scorpio, Diana G ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE AMINOTRANSFERASE; GLUCOSE; INDUCIBLE NITRIC OXIDE SYNTHASE; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; REACTIVE NITROGEN SPECIES;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANAPLASMA PHAGOCYTOPHILUM; ANAPLASMOSIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GLUCOSE BLOOD LEVEL; HUMAN; HUMAN CELL; IMMUNOPATHOGENESIS; LIVER INJURY; MOUSE; NONHUMAN; OXIDATIVE STRESS; PATHOPHYSIOLOGY;

ANAPLASMA PHAGOCYTOPHILUM; ANIMALS; DISEASE MODELS, ANIMAL; EHRLICHIOSIS; ENZYME INHIBITORS; HEPATITIS; HUMANS; LIVER; MICE; MICE, INBRED C57BL; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE SYNTHASE; REACTIVE NITROGEN SPECIES;

EID: 33646493811     PISSN: 15320820     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (38)

1. Bakken JS, Aguero-Rosenfeld ME, Tilden RL, Wormser GP, Horowitz HW, Raffalli JT, Baluch M, Riddell D, Walls JJ, Dumler JS. 2001. Serial measurements of hematologic counts during the active phase of human granulocytic ehrlichiosis. Clin Infect Dis 32:862-870.
2. Bakken JS, Dumler JS, Chen SM, Eckman MR, Van Etta LL, Walker DH. 1994. Human granulocytic ehrlichiosis in the upper Midwest United States. A new species emerging? J Am Med Assoc 272:212-218.
3. Banerjee R, Anguita J, Fikrig E. 2000. Granulocytic ehrlichiosis in mice deficient in phagocyte oxidase or inducible nitric oxide synthase. Infect Immun 68:4361-4362.
4. Borjesson DL, Barthold SW. 2002. The mouse as a model for investigation of human granulocytic ehrlichiosis: current knowledge and future directions. Comp Med 52:403-413.
5. Borjesson DL, Kobayashi SD, Whitney AR, Voyich JM, Argue CM, Deleo FR. 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. Brennan RE, Russell K, Zhang G, Samuel JE. 2004. Both inducible nitric oxide synthase and NADPH oxidase contribute to the control of virulent phase I Coxiella burnetti infections. Infect Immun 72:6666-6675.
7. Bunnell J, Trigiani ER, Srinivas SR, Dumler JS. 1999. Development and distribution of pathologic lesions are related to immune status and tissue deposition of HGE agent-infected cells in a murine model system. J Infect Dis 180:546-550.
8. Chen S-M, Dumler JS, Bakken JS, Walker DH. 1994. Identification of a granulocytotropic Ehrlichia species as the etiologic agent of human disease. J Clin Microbiol 32:589-595.
9. des Vignes F, Piesman J, Heffernan R, Schulze TL, Stafford KC III, Fish D. 2001. Effect of tick removal on transmission of Borrelia burgdorferi and Ehrlichia phagocytophila by Ixodes scapulnris nymphs. J Infect Dis 183:773-778.
10. Dowling RB, Newton R, Robichaud A, Cole PJ, Barnes PJ, Wilson R. 1998. Effect of inhibition of nitric oxide synthase on Pseudomonas aeruginosa infection of respiratory mucosa in vitro. Am J Respir Cell Mol Biol 19:950-958.
11. Dumler JS, Trigiani ER, Bakken JS, Aguero-Rosenfeld ME, Wormser GP. 2000. Serum cytokine responses during acute human granulocytic ehrlichiosis. Clin Diagn Lab Immunol 7:6-8.
12. Dumler JS, Walker DH. 2001. Tick-borne ehrlichioses: more of them, higher incidences, and greater clinical diversity. Lancet Infect Dis 0:21-28 (preview edition).
13. Gentilcore D, Visvanathan R, Russo A, Chaikomin R, Stevens JE, Wishart JM, Tonkin A, Horowitz M, Jones KL. 2005. Role of nitric oxide mechanisms in gastric emptying of, and the blood pressure and glycemic responses to, oral glucose in healthy older subjects. Am J Physiol Gastrointest Liver Physiol 288:1227-1232.
14. Hodzic E, Feng S, Fish D, Leutenegger CM, Freet KJ, Barthold SW. 2001. Infection of mice with the agent of human granulocytic ehrlichiosis after different routes of inoculation. J Infect Dis 183:1781-1786.
15. Ijdo JW, Wu C, Telford SR III, Fikrig E. 2002. Differential expression of the p44 gene family in the agent of human granulocytic ehrlichiosis. Infect Immun 70:5295-5298.
16. Kim HY, Rikihisa Y. 2000. Expression of interleukin 1β, tumor necrosis factor α, 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.
17. Klein MB, Hu S, Chao CC, Goodman JL. 2000. The agent of human granulocytic ehrlichiosis induces the production of myelosuppressing chemokines without induction of prainflammatory cytokines. J Infect Dis 182:200-205.
18. Lepidi H, Bunnell JE, Martin ME, Madigan JE, Stuen S, Dumler JS. 2000. Comparative pathology and immunohistology associated with clinical illness after Ehrlichia phagocytophila-group infections. Am J Trop Med Hyg 62:29-37.
19. Liaudet L, Rosselet A, Schaller MD, Markert M, Perret C, Feihl F. 1998. Nonselective versus selective inhibition of inclucible nitric oxide synthase in experimental endotoxic shock. J Infect Dis 177:127-132.
20. Liu TH, Robinson EK, Helmer KS, West SD, Castaneda AA, Chang L, Mercer DW. 2002. Does upregulation of inducible nitric oxide synthase play a role in hepatic injury? Shock 18:549-554.
21. Lowenstein C. 2005. Personal communication.
22. Martin ME, Bunnell JE, Dumler JS. 2000. Pathology, immunohistology, and cytokine responses in early phases of HGE in a murine model. J Infect Dis 181:374-378.
23. Martin ME, Caspersen K, Dumler JS. 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.
24. National Research Council. 1996. Guide for the care and use of laboratory animals. Washington (DC): National Academy Press.
25. Olano JP, Wen G, Feng H-M, McBride JW, Walker DH. 2004. Histologic, serologic, and molecular analysis of persistent ehrlichiosis in a murine model. Am J Pathol 165:997-1006.
26. Ou J, Carlos TM, Watkins SC, Saavedra JE, Keffer LK, Kim Y-M, Harbrecht BG, Billiar TR. 1997. Differential effects of nonselective nitric oxide synthase (NOS) and selective inducible NOS inhibition on hepatic necrosis, apoptosis, ICAM-1 expression, and neutrophil accumulation during endotoxemia. Nitric Oxide Biol Chem 1:404-416.
27. Pusterla N, Leutenegger CM, Chae JS, Lutz H, Kimsey RB, Dumler JS, Madigan JE. 1999. Quantitative evaluation of ehrlichial burden in horses after experimental transmission of human granulocytic Ehrlichia agent by intravenous inoculation with infected leukocytes and by infected ticks. J Clin Microbiol 37:4042-4044.
28. Salvemini D, Ischiropoulos H, Cuzzocrea S. 2003. Roles of nitric oxide and superoxide in inflammation. Methods Mol Biol. 225:291-303.
29. Scorpio DG, Akkoyunlu M, Fikrig E, Dumler JS. 2004. CXCR2 blockade influences Anaplasma phagocytaphilum propagation but not histopathology in the mouse model of human granulocytic anaplasmosis. Clin Diag Lab Immunol 11:963-968.
30. Scorpio DG, von Loewenich FD, Bogdan C, Dumler JS. Tissue injury in the murine model of granulocytic anaplasmosis relates to host innate immune response and not pathogen load. Ann N Y Acad Sci. Forthcoming.
31. Szabo C, Ohshima H. 1997. DNA damage induced by peroxynitrite: subsequent biological effects. Nitric Oxide Biol Chem 1:373-385.
32. Tarpey MM, Wink DA, Grisham MB. 2004. Methods for detection of reactive metabolites of oxygen and nitrogen: in vitro and in vivo considerations. Am J Physiol Regul Integr Comp Physiol 286:431-444.
33. Taylor BS, Alarcon LH, Billiar TR. 1998. Inducible nitric oxide synthase in the liver: regulation and function. Biochemistry 63:766-781.
34. Turco J, Liu H, Gottlieb SF, Winkler HH. 1998. Nitric oxide-mediated inhibition of the ability of Rickettsia prowazekii to infect mouse fibroblasts and mouse macrophagelike cells. Infect Immun 66:558-566.
35. von Loewenich FD, Scorpio DG, Reischl U, Dumler JS, Bogdan C. 2004. Frontline: control of Anaplasma phagocytophilum, an obligate intracellular pathogen, in the absence of inducible nitric oxide synthase, phagocyte NADPH oxidase, tumor necrosis factor, Toll-like receptor (TLR)2 and TLR4, or the TLR adaptor molecule MyD88. Eur J Immunol 34:1789-1797.
36. Walker DH, Dumler JS. 1997. Human monocytic and granulocytic ehrlichioses. Discovery and diagnosis of emerging tick-borne infections and the critical role of the pathologist. Arch Pathol Lab Med 121:785-791.
37. Zeidner NS, Dolan MC, Massung R, Piesman J, Fish D. 2000. Coinfection with Borrelia burgdorferi and the agent of human granulocytic ehrlichiosis suppresses IL-2 and IFN gamma production and promotes an IL-4 response in C3H/HeJ mice. Parasite Immunol 22:581-588.
38. Zhang J, Snyder SH. 1992. Nitric oxide stimulates auto-ADP-ribosylation of glyceraldehyde-3-phosphate dehydrogenase. Proc Natl Acad Sci U S A 89:9382-9385.