Mouse strain-dependent differences in susceptibility to Neisseria gonorrhoeae infection and induction of innate immune responses

Infection and Immunity

Volumn 78, Issue 1, 2010, Pages 433-440

  Packiam, Mathanraj ^a   Veit, Sandra J ^a   Anderson, Deborah J ^b   Ingalls, Robin R ^c   Jerse, Ann E ^a  

^a UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

^b BOSTON MEDICAL CENTER   (United States)

^c BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; ESTRADIOL; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 2; STREPTOMYCIN SULFATE; TRIMETHOPRIM SULFATE; TUMOR NECROSIS FACTOR ALPHA; VANCOMYCIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL COLONIZATION; CELL TRANSPORT; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE PREDISPOSITION; FEMALE; GONORRHEA; HEREDITY; INFLAMMATION; INNATE IMMUNITY; INOCULATION; KERATINOCYTE; MOUSE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; VAGINA SECRETION;

ANIMALS; FEMALE; GENETIC PREDISPOSITION TO DISEASE; GONORRHEA; IMMUNITY, INNATE; INFLAMMATION; MICE; MICE, INBRED STRAINS; NEISSERIA GONORRHOEAE; VAGINA;

EID: 73449137235     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00711-09     Document Type: Article

References (49)

1. Bradley, D. J. 1974. Letter: genetic control of natural resistance to Leishmania donovani. Nature 250:353-354.
2. Cacalano, G., J. Lee, K. Kikly, A. M. Ryan, S. Pitts-Meek, B. Hultgren, W. I. Wood, and M. W. Moore. 1994. Neutrophil and B cell expansion in mice that lack the murine IL-8 receptor homolog. Science 265:682-684.
3. Christodoulides, M., J. S. Everson, B. L. Liu, P. R. Lambden, P. J. Watt, E. J. Thomas, and J. E. Heckels. 2000. Interaction of primary human endometrial cells with Neisseria gonorrhoeae expressing green fluorescent protein. Mol. Microbiol. 35:32-43.
4. Cohen, M. S., J. G. Cannon, A. E. Jerse, L. M. Charniga, S. F. Isbey, and L. G. Whicker. 1994. Human experimentation with Neisseria gonorrhoeae: rationale, methods, and implications for the biology of infection and vaccine development. J. Infect. Dis. 169:532-537.
5. Cone, R. A., T. Hoen, X. Wong, R. Abusuwwa, D. J. Anderson, and T. R. Moench. 2006. Vaginal microbicides: detecting toxicities in vivo that paradoxically increase pathogen transmission. BMC Infect. Dis. 6:90.
6. Criss, A. K., B. Z. Katz, and H. S. Seifert. 2009. Resistance of Neisseria gonorrhoeae to non-oxidative killing by adherent human polymorphonuclear leucocytes. Cell. Microbiol. 11:1074-1087.
7. Dalal, S. J., J. S. Estep, I. E. Valentin-Bon, and A. E. Jerse. 2001. Standardization of the Whitten Effect to induce susceptibility to Neisseria gonorrhoeae in female mice. Contemp. Top. Lab. Anim. Sci. 40:13-17.
8. Darville, T., C. W. Andrews, Jr., K. K. Laffoon, W. Shymasani, L. R. Kishen, and R. G. Rank. 1997. Mouse strain-dependent variation in the course and outcome of chlamydial genital tract infection is associated with differences in host response. Infect. Immun. 65:3065-3073.
9. Darville, T., C. W. Andrews, Jr., J. D. Sikes, P. L. Fraley, and R. G. Rank. 2001. Early local cytokine profiles in strains of mice with different outcomes from chlamydial genital tract infection. Infect. Immun. 69:3556-3561.
10. de la Maza, L. M., S. Pal, A. Khamesipour, and E. M. Peterson. 1994. Intravaginal inoculation of mice with the Chlamydia trachomatis mouse pneumonitis biovar results in infertility. Infect. Immun. 62:2094-2097.
11. Fichorova, R. N., A. O. Cronin, E. Lien, D. J. Anderson, and R. R. Ingalls. 2002. Response to Neisseria gonorrhoeae by cervicovaginal epithelial cells occurs in the absence of toll-like receptor 4-mediated signaling. J. Immunol. 168:2424-2432.
12. Fichorova, R. N., P. J. Desai, F. C. Gibson III, and C. A. Genco. 2001. Distinct proinflammatory host responses to Neisseria gonorrhoeae infection in immortalized human cervical and vaginal epithelial cells. Infect. Immun. 69:5840-5848.
13. Forbes, J. R., and P. Gros. 2001. Divalent-metal transport by NRAMP proteins at the interface of host-pathogen interactions. Trends Microbiol. 9:397-403.
14. Gambero, A., E. C. Landucci, M. H. Toyama, S. Marangoni, J. R. Giglio, H. B. Nader, C. P. Dietrich, G. De Nucci, and E. Antunes. 2002. Human neutrophil migration in vitro induced by secretory phospholipases A2: a role for cell surface glycosaminoglycans. Biochem. Pharmacol. 63:65-72.
15. Granata, F., A. Petraroli, E. Boilard, S. Bezzine, J. Bollinger, L. Del Vecchio, M. H. Gelb, G. Lambeau, G. Marone, and M. Triggiani. 2005. Activation of cytokine production by secreted phospholipase A2 in human lung macrophages expressing the M-type receptor. J. Immunol. 174:464-474.
16. Gros, P., E. Skamene, and A. Forget. 1981. Genetic control of natural resistance to Mycobacterium bovis (BCG) in mice. J. Immunol. 127:2417-2421.
17. Harvey, H. A., D. M. Post, and M. A. Apicella. 2002. Immortalization of human urethral epithelial cells: a model for the study of the pathogenesis of and the inflammatory cytokine response to Neisseria gonorrhoeae infection. Infect. Immun. 70:5808-5815.
18. Hedges, S. R., M. S. Mayo, J. Mestecky, E. W. Hook III, and M. W. Russell. 1999. Limited local and systemic antibody responses to Neisseria gonorrhoeae during uncomplicated genital infections. Infect. Immun. 67:3937-3946.
19. Hedges, S. R., D. A. Sibley, M. S. Mayo, E. W. Hook III, and M. W. Russell. 1998. Cytokine and antibody responses in women infected with Neisseria gonorrhoeae: effects of concomitant infections. J. Infect. Dis. 178:742-751.
20. Imarai, M., E. Candia, C. Rodriguez-Tirado, J. Tognarelli, M. Pardo, T. Perez, D. Valdes, S. Reyes-Cerpa, P. Nelson, C. Acuna-Castillo, and K. Maisey. 2008. Regulatory T cells are locally induced during intravaginal infection of mice with Neisseria gonorrhoeae. Infect. Immun. 76:5456-5465.
21. Jerse, A. E. 1999. Experimental gonococcal genital tract infection and opacity protein expression in estradiol-treated mice. Infect. Immun. 67:5699-5708.
22. Jerse, A. E., E. T. Crow, A. N. Bordner, I. Rahman, C. N. Cornelissen, T. R. Moench, and K. Mehrazar. 2002. Growth of Neisseria gonorrhoeae in the female mouse genital tract does not require the gonococcal transferrin or hemoglobin receptors and may be enhanced by commensal lactobacilli. Infect. Immun. 70:2549-2558.
23. Jerse, A. E., N. D. Sharma, A. N. Simms, E. T. Crow, L. A. Snyder, and W. M. Shafer. 2003. A gonococcal efflux pump system enhances bacterial survival in a female mouse model of genital tract infection. Infect. Immun. 71:5576-5582.
24. Kellogg, D. S., Jr., W. L. Peacock, Jr., W. E. Deacon, L. Brown, and D. I. Pirkle. 1963. Neisseria gonorrhoeae. I. Virulence genetically linked to clonal variation. J. Bacteriol. 85:1274-1279.
25. Kelly, K. A., and R. G. Rank. 1997. Identification of homing receptors that mediate the recruitment of CD4 T cells to the genital tract following intravaginal infection with Chlamydia trachomatis. Infect. Immun. 65:5198-5208.
26. Kennedy, B. P., P. Payette, J. Mudgett, P. Vadas, W. Pruzanski, M. Kwan, C. Tang, D. E. Rancourt, and W. A. Cromlish. 1995. A natural disruption of the secretory group II phospholipase A2 gene in inbred mouse strains. J. Biol. Chem. 270:22378-22385.
27. Kramnik, I., and V. Boyartchuk. 2002. Immunity to intracellular pathogens as a complex genetic trait. Curr. Opin. Microbiol. 5:111-117.
28. Kudo, I., and M. Murakami. 2002. Phospholipase A2 enzymes. Prostaglandins Other Lipid Mediat. 68-69:3-58.
29. Maisey, K., G. Nardocci, M. Imarai, H. Cardenas, M. Rios, H. B. Croxatto, J. E. Heckels, M. Christodoulides, and L. A. Velasquez. 2003. Expression of proinflammatory cytokines and receptors by human fallopian tubes in organ culture following challenge with Neisseria gonorrhoeae. Infect. Immun. 71: 527-532.
30. Makepeace, B. L., P. J. Watt, J. E. Heckels, and M. Christodoulides. 2001. Interactions of Neisseria gonorrhoeae with mature human macrophage opacity proteins influence production of proinflammatory cytokines. Infect. Immun. 69:1909-1913.
31. Morales, P., P. Reyes, M. Vargas, M. Rios, M. Imarai, H. Cardenas, H. Croxatto, P. Orihuela, R. Vargas, J. Fuhrer, J. E. Heckels, M. Christodoulides, and L. Velasquez. 2006. Infection of human fallopian tube epithelial cells with Neisseria gonorrhoeae protects cells from tumor necrosis factor alpha-induced apoptosis. Infect. Immun. 74:3643-3650.
32. Muench, D. F., D. J. Kuch, H. Wu, A. A. Begum, S. J. Veit, M. E. Pelletier, A. A. Soler-Garcia, and A. E. Jerse. 2009. Hydrogen peroxide-producing lactobacilli inhibit gonococci in vitro but not during experimental genital tract infection. J. Infect. Dis. 199:1369-1378.
33. Naumann, M., S. Wessler, C. Bartsch, B. Wieland, and T. F. Meyer. 1997. Neisseria gonorrhoeae epithelial cell interaction leads to the activation of the transcription factors nuclear factor kappaB and activator protein 1 and the induction of inflammatory cytokines. J. Exp. Med. 186:247-258.
34. Patrone, J. B., S. E. Bish, and D. C. Stein. 2006. TNF-alpha-independent IL-8 expression: alterations in bacterial challenge dose cause differential human monocytic cytokine response. J. Immunol. 177:1314-1322.
35. Patrone, J. B., and D. C. Stein. 2007. Effect of gonococcal lipooligosaccharide variation on human monocytic cytokine profile. BMC Microbiol. 7:7.
36. Plant, J., and A. A. Glynn. 1976. Genetics of resistance to infection with Salmonella typhimurium in mice. J. Infect. Dis. 133:72-78.
37. Ramsey, K. H., H. Schneider, A. S. Cross, J. W. Boslego, D. L. Hoover, T. L. Staley, R. A. Kuschner, and C. D. Deal. 1995. Inflammatory cytokines produced in response to experimental human gonorrhea. J. Infect. Dis. 172: 186-191.
38. Ramsey, K. H., H. Schneider, R. A. Kuschner, A. F. Trofa, A. S. Cross, and C. D. Deal. 1994. Inflammatory cytokine response to experimental human infection with Neisseria gonorrhoeae. Ann. N. Y. Acad. Sci. 730:322-325.
39. Rarick, M., C. McPheeters, S. Bright, A. Navis, J. Skefos, P. Sebastiani, and M. Montano. 2006. Evidence for cross-regulated cytokine response in human peripheral blood mononuclear cells exposed to whole gonococcal bacteria in vitro. Microb. Pathog. 40:261-270.
40. Schneider, H., J. M. Griffiss, J. W. Boslego, P. J. Hitchcock, K. M. Zahos, and M. A. Apicella. 1991. Expression of paragloboside-like lipooligosaccharides may be a necessary component of gonococcal pathogenesis in men. J. Exp. Med. 174:1601-1605.
41. Simms, A. N., and A. E. Jerse. 2006. In vivo selection for Neisseria gonorrhoeae opacity protein expression in the absence of human carcinoembryonic antigen cell adhesion molecules. Infect. Immun. 74:2965-2974.
42. Simons, M. P., W. M. Nauseef, and M. A. Apicella. 2005. Interactions of Neisseria gonorrhoeae with adherent polymorphonuclear leukocytes. Infect. Immun. 73:1971-1977.
43. Soler-Garciá, A. A., and A. E. Jerse. 2007. Neisseria gonorrhoeae catalase is not required for experimental genital tract infection despite the induction of a localized neutrophil response. Infect. Immun. 75:2225-2233.
44. Song, W., S. Condron, B. T. Mocca, S. J. Veit, D. Hill, A. Abbas, and A. E. Jerse. 2008. Local and humoral immune responses against primary and repeat Neisseria gonorrhoeae genital tract infections of 17beta-estradiol-treated mice. Vaccine 26:5741-5751.
45. Straub, R. H. 2007. The complex role of estrogens in inflammation. Endocr. Rev. 28:521-574.
46. Streeter, P. R., and L. B. Corbeil. 1981. Gonococcal infection in endotoxin-resistant and endotoxin-susceptible mice. Infect. Immun. 32:105-110.
47. Triggiani, M., F. Granata, A. Oriente, M. Gentile, A. Petraroli, B. Balestrieri, and G. Marone. 2002. Secretory Phospholipases A2 induce cytokine release from blood and synovial fluid monocytes. Eur. J. Immunol. 32:67-76.
48. Warner, D. M., W. M. Shafer, and A. E. Jerse. 2008. Clinically relevant mutations that cause derepression of the Neisseria gonorrhoeae MtrC-MtrD-MtrE efflux pump system confer different levels of antimicrobial resistance and in vivo fitness. Mol. Microbiol. 70:462-478.
49. Wu, H., A. A. Soler-Garcia, and A. E. Jerse. 2009. A strain-specific catalase mutation and mutation of the metal-binding transporter gene mntC attenuate Neisseria gonorrhoeae in vivo but not by increasing susceptibility to oxidative killing by phagocytes. Infect. Immun. 77:1091-1102.