Interleukin-6 is essential for primary resistance to Francisella tularensis live Vaccine strain infection

Infection and Immunity

Volumn 81, Issue 2, 2013, Pages 585-597

  Kurtz, Sherry L ^a   Foreman, Oded ^b   Bosio, Catharine M ^c   Anver, Miriam R ^d   Elkins, Karen L ^a  

^a CENTER FOR BIOLOGICS EVALUATION AND RESEARCH   (United States)

^b JACKSON LABORATORY   (United States)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

^d SAIC FREDERICK INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID A PROTEIN; HAPTOGLOBIN; INTERLEUKIN 6; LIVE VACCINE; TULAREMIA VACCINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY BLOOD LEVEL; ANTIBODY PRODUCTION; ARTICLE; BACTERIAL IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; IMMUNOCOMPETENT CELL; IN VITRO STUDY; INFECTION RESISTANCE; INFECTION SENSITIVITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN FUNCTION; SPLEEN CELL; SURVIVAL; T LYMPHOCYTE ACTIVATION;

ANIMALS; BACTERIAL VACCINES; FRANCISELLA TULARENSIS; HAPTOGLOBINS; INTERLEUKIN-6; LYMPHOCYTE ACTIVATION; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; SERUM AMYLOID A PROTEIN; T-LYMPHOCYTES; TULAREMIA; VACCINES, ATTENUATED;

EID: 84873029204     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01249-12     Document Type: Article

References (54)

1. Sjöstedt A. 2004. Family XVII. Francisellaceae, p 200-210. In Brenner DJ (ed), Bergey's manual of systematic bacteriology. Springer, New York, NY.
2. Eigelsbach HT, Downs CM. 1961. Prophylactic effectiveness of live and killed tularemia vaccines. J. Immunol. 87:415-425.
3. Sändstrom G. 1994. The tularemia vaccine. J. Chem. Technol. Biotechnol. 59:315-320.
4. Tigertt WD. 1962. Soviet viable Pasteurella tularensis vaccines. A review of selected articles. Bacteriol. Rev. 26:354-373.
5. Oyston PC. 2009. Francisella tularensis vaccines. Vaccine 27(Suppl 4): D48-D51.
6. Conlan JW. 2004. Vaccines against Francisella tularensis: past, present and future. Expert Rev. Vaccines 3:307-314.
7. Elkins KL, Cowley SC, Bosio CM. 2003. Innate and adaptive immune responses to an intracellular bacterium, Francisella tularensis live vaccine strain. Microbes Infect. 5:132-142.
8. Cowley SC, Elkins KL. 2011. Immunity to Francisella. Front. Microbiol. 2:26. doi:10.3389/fmicb.2011.00026.
9. De Pascalis R, Chou AY, Bosio CM, Huang CY, Follmann DA, Elkins KL. 2012. Development of functional and molecular correlates of vaccineinduced protection for a model intracellular pathogen, F. tularensis LVS. PLoS Pathog. 8:e1002494. doi:10.1371/journal.ppat.1002494.
10. Elkins KL, Rhinehart-Jones TR, Culkin SJ, Yee D, Winegar RK. 1996. Minimal requirements for murine resistance to infection with Francisella tularensis LVS. Infect. Immun. 64:3288-3293.
11. Elkins KL, Colombini SM, Meierovics AI, Chu MC, Chou AY, Cowley SC. 2010. Survival of secondary lethal systemic Francisella LVS challenge depends largely on interferon gamma. Microbes Infect. 12:28-36.
12. Gabay C, Kushner I. 1999. Acute-phase proteins and other systemic responses to inflammation. N. Engl. J. Med. 340:448-454.
13. Jones SA. 2005. Directing transition from innate to acquired immunity: defining a role for IL-6. J. Immunol. 175:3463-3468.
14. Kishimoto T. 2006. Interleukin-6: discovery of a pleiotropic cytokine. Arthritis Res. Ther. 8(Suppl 2):S2.
15. Kaplanski G, Marin V, Montero-Julian F, Mantovani A, Farnarier C. 2003. IL-6: a regulator of the transition from neutrophil to monocyte recruitment during inflammation. Trends Immunol. 24:25-29.
16. Dienz O, Rincon M. 2009. The effects of IL-6 on CD4 T cell responses. Clin. Immunol. 130:27-33.
17. Chomarat P, Banchereau J, Davoust J, Palucka AK. 2000. IL-6 switches the differentiation of monocytes from dendritic cells to macrophages. Nat. Immunol. 1:510-514.
18. Dalrymple SA, Lucian LA, Slattery R, McNeil T, Aud DM, Fuchino S, Lee F, Murray R. 1995. Interleukin-6-deficient mice are highly susceptible to Listeria monocytogenes infection: correlation with inefficient neutrophilia. Infect. Immun. 63:2262-2268.
19. Williams DM, Grubbs BG, Darville T, Kelly K, Rank RG. 1998. A role for interleukin-6 in host defense against murine Chlamydia trachomatis infection. Infect. Immun. 66:4564-4567.
20. Dalrymple SA, Slattery R, Aud DM, Krishna M, Lucian LA, Murray R. 1996. Interleukin-6 is required for a protective immune response to systemic Escherichia coli infection. Infect. Immun. 64:3231-3235.
21. Dube PH, Handley SA, Lewis J, Miller VL. 2004. Protective role of interleukin-6 during Yersinia enterocolitica infection is mediated through themodulation of inflammatory cytokines. Infect. Immun. 72:3561-3570.
22. Kingry LC, Troyer RM, Marlenee NL, Bielefeldt-Ohmann H, Bowen RA, Schenkel AR, Dow SW, Slayden RA. 2011. Genetic identification of unique immunological responses in mice infected with virulent and attenuated Francisella tularensis. Microbes Infect. 13:261-275.
23. Periasamy S, Singh A, Sahay B, Rahman T, Feustel PJ, Pham GH, Gosselin EJ, Sellati TJ. 2011. Development of tolerogenic dendritic cells and regulatory T cells favors exponential bacterial growth and survival during early respiratory tularemia. J. Leukoc. Biol. 90:493-507.
24. Cole LE, Elkins KL, Michalek SM, Qureshi N, Eaton LJ, Rallabhandi P, Cuesta N, Vogel SN. 2006. Immunologic consequences of Francisella tularensis live vaccine strain infection: role of the innate immune response in infection and immunity. J. Immunol. 176:6888-6899.
25. Huntley JF, Conley PG, Rasko DA, Hagman KE, Apicella MA, Norgard MV. 2008. Native outer membrane proteins protect mice against pulmonary challenge with virulent type A Francisella tularensis. Infect. Immun. 76:3664-3671.
26. Sharma J, Mares CA, Li Q, Morris EG, Teale JM. 2011. Features of sepsis caused by pulmonary infection with Francisella tularensis type A strain. Microb. Pathog. 51:39-47.
27. Chiavolini D, Alroy J, King CA, Jorth P, Weir S, Madico G, Murphy JR, Wetzler LM. 2008. Identification of immunologic and pathologic parameters of death versus survival in respiratory tularemia. Infect. Immun. 76:486-496.
28. Shen H, Harris G, Chen W, Sjostedt A, Ryden P, Conlan W. 2010. Molecular immune responses to aerosol challenge with Francisella tularensis in mice inoculated with live vaccine candidates of varying efficacy. PLoS One 5:e13349. doi:10.1371/journal.pone.0013349.
29. Kopf M, Baumann H, Ferre G, Freudenberg M, Lamers M, Kishimoto T, Zinkernagel R, Bluethmann H, Kohler G. 1994. Impaired immune and acute-phase responses in interleukin-6-deficient mice. Nature 368:339-341.
30. Fortier AH, Slayter MV, Ziemba R, Meltzer MS, Nacy CA. 1991. Live vaccine strain of Francisella tularensis: infection and immunity in mice. Infect. Immun. 59:2922-2928.
31. Rhinehart-Jones TR, Fortier AH, Elkins KL. 1994. Transfer of immunity against lethal murine Francisella infection by specific antibody depends on host gamma interferon and T cells. Infect. Immun. 62:3129-3137.
32. Bosio CM, Elkins KL. 2001. Susceptibility to secondary Francisella tularensis LVS infection in B cell deficient mice is associated with neutrophilia but not with defects in specific T cell mediated immunity. Infect. Immun. 69:194-203.
33. Cowley SC, Elkins KL. 2003. Multiple T cell subsets control Francisella tularensis LVS intracellular growth without stimulation through macrophage interferon gamma receptors. J. Exp. Med. 198:379-389.
34. Cowley SC, Hamilton E, Frelinger JA, Su J, Forman J, Elkins KL. 2005. CD4-CD8-T cells control intracellular bacterial infections both in vitro and in vivo. J. Exp. Med. 202:309-319.
35. Elkins KL, Cooper A, Colombini SM, Cowley SC, Kieffer TL. 2002. In vivo clearance of an intracellular bacterium, Francisella tularensis LVS, is dependent on the p40 subunit of interleukin-12 (IL-12) but not on IL-12 p70. Infect. Immun. 70:1936-1948.
36. Collazo CM, Meierovics AI, De Pascalis R, Wu TH, Lyons CR, Elkins KL. 2009. T cells from lungs and livers of Francisella tularensis-immune mice control the growth of intracellular bacteria. Infect. Immun. 77:2010-2021.
37. Elkins KL, Cowley SC, Conlan JW. 2011. Measurement of macrophagemediated killing of intracellular bacteria, including Francisella and Mycobacteria. Curr. Protoc. Immunol. 93:14.25.11-14.25.13.
38. Reed LJ, Muench H. 1938. A simple method of estimating fifty per cent endpoints. Am. J. Hyg. 25:493-497.
39. Gervois P, Kleemann R, Pilon A, Percevault F, Koenig W, Staels B, Kooistra T. 2004. Global suppression of IL-6-induced acute phase response gene expression after chronic in vivo treatment with the peroxisome proliferator-activated receptor-alpha activator fenofibrate. J. Biol. Chem. 279:16154-16160.
40. Gomez CR, Goral J, Ramirez L, Kopf M, Kovacs EJ. 2006. Aberrant acute-phase response in aged interleukin-6 knockout mice. Shock 25:581-585.
41. Urieli-Shoval S, Linke RP, Matzner Y. 2000. Expression and function of serum amyloid A, a major acute-phase protein, in normal and disease states. Curr. Opin. Hematol. 7:64-69.
42. Hari-Dass R, Shah C, Meyer DJ, Raynes JG. 2005. Serum amyloid A protein binds to outer membrane protein A of gram-negative bacteria. J. Biol. Chem. 280:18562-18567.
43. He RL, Zhou J, Hanson CZ, Chen J, Cheng N, Ye RD. 2009. Serum amyloid A induces G-CSF expression and neutrophilia via Toll-like receptor 2. Blood 113:429-437.
44. Lim SK, Kim H, bin Ali A, Lim YK, Wang Y, Chong SM, Costantini F, Baumman H. 1998. Increased susceptibility in Hp knockout mice during acute hemolysis. Blood 92:1870-1877.
45. Eaton JW, Brandt P, Mahoney, Jr, Lee JT, Jr. 1982. Haptoglobin: a natural bacteriostat. Science 215:691-693.
46. Conlan JW, KuoLee R, Shen H, Webb A. 2002. Different host defences are required to protect mice from primary systemic vs pulmonary infection with the facultative intracellular bacterial pathogen, Francisella tularensis LVS. Microb. Pathog. 32:127-134.
47. Matsuoka T, Okamoto Y, Matsuzaki Z, Endo S, Ito E, Tsutsumi H, Williamson RA, Sakurai H, Burton DR, Saito I. 2002. Characteristics of immunity induced by viral antigen or conferred by antibody via different administration routes. Clin. Exp. Immunol. 130:386-392.
48. Perry LL, Feilzer K, Caldwell HD. 1997. Immunity to Chlamydia trachomatis is mediated by T helper 1 cells through IFN-γ-dependent and-independent pathways. J. Immunol. 158:3344-3352.
49. Ladel CH, Szalay G, Riedel D, Kaufmann SHE. 1997. Interleukin-12 secretion by Mycobacterium tuberculosis-infected macrophages. Infect. Immun. 65:1936-1938.
50. Okada M, Kita Y, Kanamaru N, Hashimoto S, Uchiyama Y, Mihara M, Inoue Y, Ohsugi Y, Kishimoto T, Sakatani M. 2011. Anti-IL-6 receptor antibody causes less promotion of tuberculosis infection than anti-TNF-α antibody in mice. Clin. Dev. Immunol. 2011:404929.
51. Saunders BM, Frank AA, Orme IM, Cooper AM. 2000. Interleukin-6 induces early gamma interferon production in the infected lung but is not required for generation of specific immunity to Mycobacterium tuberculosis infection. Infect. Immun. 68:3322-3326.
52. + T helper cell 1 development in interleukin 6-deficient mice infected with Candida albicans. J. Exp. Med. 183:1345-1355.
53. Cole LE, Yang Y, Elkins KL, Fernandez ET, Qureshi N, Shlomchik MJ, Herzenberg LA, Vogel SN. 2009. Antigen-specific B-1a antibodies induced by Francisella tularensis LPS provide long-term protection against F. tularensis LVS challenge. Proc. Natl. Acad. Sci. U. S. A. 106:4343-4348.
54. Kirimanjeswara GS, Olmos S, Bakshi CS, Metzger DW. 2008. Humoral and cell-mediated immunity to the intracellular pathogen Francisella tularensis. Immunol. Rev. 225:244-255.