Targeting of a fixed bacterial immunogen to Fc receptors reverses the anti-inflammatory properties of the gram-negative bacterium, Francisella tularensis, during the early stages of infection

PLoS ONE

Volumn 10, Issue 6, 2015, Pages

  Babadjanova, Zulfia ^a   Wiedinger, Kari ^a   Gosselin, Edmund J ^b   Bitsaktsis, Constantine ^a  

^a SETON HALL UNIVERSITY   (United States)

^b ALBANY MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B7 ANTIGEN; CD11B ANTIGEN; CD86 ANTIGEN; CHEMOKINE RECEPTOR CCR7; FC RECEPTOR; GAMMA INTERFERON; INFLAMMASOME; INTERLEUKIN 10; INTERLEUKIN 12P70; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MONOCLONAL ANTIBODY; TUMOR NECROSIS FACTOR ALPHA; ANTIGEN ANTIBODY COMPLEX; AUTACOID; BACTERIAL ANTIGEN; CYTOKINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN ANTIBODY COMPLEX; ANTIGEN EXPRESSION; ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BACTERIAL INFECTION; BACTERIAL LOAD; CELL ISOLATION; CELL POLARITY; COLONY FORMING UNIT; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DOWN REGULATION; ENDOTOXEMIA; ENZYME LINKED IMMUNOSORBENT ASSAY; EX VIVO STUDY; FLOW CYTOMETRY; FRANCISELLA TULARENSIS; GRAM NEGATIVE BACTERIUM; IMMUNE RESPONSE; IMMUNIZATION; INNATE IMMUNITY; LEUKOCYTE; LUNG ALVEOLUS MACROPHAGE; MOUSE; NONHUMAN; PATHOGENESIS; PERITONEAL EXUDATE CELL; PERITONEUM CELL; PHENOTYPE; POLARIZATION; PROTEIN SYNTHESIS; SUPERNATANT; T LYMPHOCYTE ACTIVATION; TH1 CELL; TULAREMIA; ANIMAL; DISEASE MODEL; IMMUNOLOGY; KNOCKOUT MOUSE; LUNG; MACROPHAGE ACTIVATION; METABOLISM; MICROBIOLOGY; PATHOLOGY; PERITONEUM MACROPHAGE;

BACTERIA (MICROORGANISMS); FRANCISELLA TULARENSIS; NEGIBACTERIA;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGEN-ANTIBODY COMPLEX; ANTIGENS, BACTERIAL; CYTOKINES; DISEASE MODELS, ANIMAL; FRANCISELLA TULARENSIS; INFLAMMATION MEDIATORS; LUNG; MACROPHAGE ACTIVATION; MACROPHAGES, PERITONEAL; MICE; MICE, KNOCKOUT; RECEPTORS, FC; RECEPTORS, IGG; TULAREMIA;

EID: 84938322895     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0129981     Document Type: Article

References (49)

1. Medzhitov R, Janeway CA Jr (1997) Innate immunity: the virtues of a nonclonal system of recognition. Cell 91: 295-298. PMID: 9363937
2. Pashine A, Valiante NM, Ulmer JB (2005) Targeting the innate immune response with improved vaccine adjuvants. Nat Med 11: S63-68. PMID: 15812492
3. Kalinski P (2012) Regulation of immune responses by prostaglandin E2. J Immunol 188: 21-28. doi: 10.4049/jimmunol.1101029 PMID: 22187483
4. Alfano M, Poli G (2005) Role of cytokines and chemokines in the regulation of innate immunity and HIV infection. Mol Immunol 42: 161-182. PMID: 15488606
5. Lacy P, Stow JL (2011) Cytokine release from innate immune cells: association with diverse membrane trafficking pathways. Blood 118: 9-18. doi: 10.1182/blood-2010-08-265892 PMID: 21562044
6. Shibata Y, Foster LA, Kurimoto M, Okamura H, Nakamura RM, et al. (1998) Immunoregulatory roles of IL-10 in innate immunity: IL-10 inhibits macrophage production of IFN-gamma-inducing factors but enhances NK cell production of IFN-gamma. J Immunol 161: 4283-4288. PMID: 9780204
7. Pestka S, Krause CD, Sarkar D, Walter MR, Shi Y, et al. (2004) Interleukin-10 and related cytokines and receptors. Annu Rev Immunol 22: 929-979. PMID: 15032600
8. Asadullah K, Sterry W, Volk HD (2003) Interleukin-10 therapy - review of a new approach. Pharmacol Rev 55: 241-269. PMID: 12773629
9. Abrahamsohn IA, Coffman RL (1996) Trypanosoma cruzi: IL-10, TNF, IFN-gamma, and IL-12 regulate innate and acquired immunity to infection. Exp Parasitol 84: 231-244. PMID: 8932773
10. Sing A, Roggenkamp A, Geiger AM, Heesemann J (2002) Yersinia enterocolitica evasion of the host innate immune response by V antigen-induced IL-10 production of macrophages is abrogated in IL-10-deficient mice. J Immunol 168: 1315-1321. PMID: 11801671
11. Salek-Ardakani S, Arrand JR, Mackett M (2002) Epstein-Barr virus encoded interleukin-10 inhibits HLA-class I, ICAM-1, and B7 expression on human monocytes: implications for immune evasion by EBV. Virology 304: 342-351. PMID: 12504574
12. Metzger DW, Salmon SL, Kirimanjeswara G (2013) Differing effects of interleukin-10 on cutaneous and pulmonary Francisella tularensis live vaccine strain infection. Infect Immun 81: 2022-2027. doi: 10.1128/IAI.00024-13 PMID: 23529615
13. Metzger DW, Bakshi CS, Kirimanjeswara G (2007) Mucosal immunopathogenesis of Francisella tularensis. Ann N Y Acad Sci 1105: 266-283. PMID: 17395728
14. Rotz LD, Khan AS, Lillibridge SR, Ostroff SM, Hughes JM (2002) Public health assessment of potential biological terrorism agents. Emerg Infect Dis 8: 225-230. PMID: 11897082
15. Elkins KL, Cowley SC, Bosio CM (2003) Innate and adaptive immune responses to an intracellular bacterium, Francisella tularensis live vaccine strain. Microbes Infect 5: 135-142. PMID: 12650771
16. Leiby DA, Fortier AH, Crawford RM, Schreiber RD, Nacy CA (1992) In vivo modulation of the murine immune response to Francisella tularensis LVS by administration of anticytokine antibodies. Infect Immun 60: 84-89. PMID: 1729199
17. Duckett NS, Olmos S, Durrant DM, Metzger DW (2005) Intranasal interleukin-12 treatment for protection against respiratory infection with the Francisella tularensis live vaccine strain. Infect Immun 73: 2306-2311. PMID: 15784575
18. Bosio CM, Bielefeldt-Ohmann H, Belisle JT (2007) Active suppression of the pulmonary immune response by Francisella tularensis Schu4. J Immunol 178: 4538-4547. PMID: 17372012
19. Rawool DB, Bitsaktsis C, Li Y, Gosselin DR, Lin Y, et al. (2008) Utilization of Fc receptors as a mucosal vaccine strategy against an intracellular bacterium, Francisella tularensis. J Immunol 180: 5548-5557. PMID: 18390739
20. Singh A, Rahman T, Malik M, Hickey AJ, Leifer CA, et al., Discordant results obtained with Francisella tularensis during in vitro and in vivo immunological studies are attributable to compromised bacterial structural integrity. PLOS ONE 8: e58513. doi: 10.1371/journal.pone.0058513 PMID: 23554897
21. Hajjar AM, Harvey MD, Shaffer SA, Goodlett DR, Sjostedt A, et al. (2006) Lack of in vitro and in vivo recognition of Francisella tularensis subspecies lipopolysaccharide by Toll-like receptors. Infect Immun 74: 6730-6738. PMID: 16982824
22. Duenas AI, Aceves M, Orduna A, Diaz R, Sanchez Crespo M, et al. (2006) Francisella tularensis LPS induces the production of cytokines in human monocytes and signals via Toll-like receptor 4 with much lower potency than E. coli LPS. Int Immunol 18: 785-795. PMID: 16574669
23. Ancuta P, Pedron T, Girard R, Sandstrom G, Chaby R (1996) Inability of the Francisella tularensis lipopolysaccharide to mimic or to antagonize the induction of cell activation by endotoxins. Infect Immun 64: 2041-2046. PMID: 8675305
24. Barker JH, Weiss J, Apicella MA, Nauseef WM (2006) Basis for the failure of Francisella tularensis lipopolysaccharide to prime human polymorphonuclear leukocytes. Infect Immun 74: 3277-3284. PMID: 16714555
25. Bitsaktsis C, Babadjanova Z, Gosselin EJ (2015) In Vivo Mechanisms Involved in Enhanced Protection Utilizing an FcR-Targeted Mucosal Vaccine Platform in a Bacterial Vaccine and Challenge Model. Infect Immun 83(1): 77-89. doi: 10.1128/IAI.02289-14 PMID: 25312957
26. Iglesias BV, Bitsaktsis C, Pham G, Drake JR, Hazlett KR, et al. (2013) Multiple mechanisms mediate enhanced immunity generated by mAb-inactivated F. tularensis immunogen. Immunol Cell Biol 91: 139-148. doi: 10.1038/icb.2012.66 PMID: 23247654
27. Bosio CM (2011) The subversion of the immune system by francisella tularensis. Front Microbiol 2: 9. doi: 10.3389/fmicb.2011.00009 PMID: 21687406
28. Ding L, Linsley PS, Huang LY, Germain RN, Shevach EM (1993) IL-10 inhibits macrophage costimulatory activity by selectively inhibiting the up-regulation of B7 expression. J Immunol 151: 1224-1234. PMID: 7687627
29. Donnelly RP, Freeman SL, Hayes MP (1995) Inhibition of IL-10 expression by IFN-gamma up-regulates transcription of TNF-alpha in human monocytes. J Immunol 155: 1420-1427. PMID: 7636207
30. Brustoski K, Moller U, Kramer M, Petelski A, Brenner S, et al. (2005) IFN-gamma and IL-10 mediate parasite-specific immune responses of cord blood cells induced by pregnancy-associated Plasmodium falciparum malaria. J Immunol 174: 1738-1745. PMID: 15661939
31. Cope A, Le Friec G, Cardone J, Kemper C (2011) The Th1 life cycle: molecular control of IFN-gamma to IL-10 switching. Trends Immunol 32: 278-286. doi: 10.1016/j.it.2011.03.010 PMID: 21531623
32. Sharma J, Li Q, Mishra BB, Georges MJ, Teale JM (2009) Vaccination with an attenuated strain of Francisella novicida prevents T-cell depletion and protects mice infected with the wild-type strain from severe sepsis. Infect Immun 77: 4314-4326. doi: 10.1128/IAI.00654-09 PMID: 19635830
33. Mares CA, Ojeda SS, Morris EG, Li Q, Teale JM (2008) Initial delay in the immune response to Francisella tularensis is followed by hypercytokinemia characteristic of severe sepsis and correlating with upregulation and release of damage-associated molecular patterns. Infect Immun 76: 3001-3010. doi: 10.1128/IAI.00215-08 PMID: 18411294
34. Shirey KA, Cole LE, Keegan AD, Vogel SN (2008) Francisella tularensis live vaccine strain induces macrophage alternative activation as a survival mechanism. J Immunol 181: 4159-4167. PMID: 18768873
35. Tomioka H, Tatano Y, Maw WW, Sano C, Kanehiro Y, et al. (2012) Characteristics of suppressor macrophages induced by mycobacterial and protozoal infections in relation to alternatively activated M2 macrophages. Clin Dev Immunol 2012: 635451. doi: 10.1155/2012/635451 PMID: 22666284
36. Katakura T, Miyazaki M, Kobayashi M, Herndon DN, Suzuki F (2004) CCL17 and IL-10 as effectors that enable alternatively activated macrophages to inhibit the generation of classically activated macrophages. J Immunol 172: 1407-1413. PMID: 14734716
37. Mantovani A, Sica A, Sozzani S, Allavena P, Vecchi A, et al. (2004) The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol 25: 677-686. PMID: 15530839
38. Woolard MD, Wilson JE, Hensley LL, Jania LA, Kawula TH, et al. (2007) Francisella tularensis-infected macrophages release prostaglandin E2 that blocks T cell proliferation and promotes a Th2-like response. J Immunol 178: 2065-2074. PMID: 17277110
39. Huang MT, Mortensen BL, Taxman DJ, Craven RR, Taft-Benz S, et al. (2010) Deletion of ripA alleviates suppression of the inflammasome and MAPK by Francisella tularensis. J Immunol 185: 5476-5485. doi: 10.4049/jimmunol.1002154 PMID: 20921527
40. Ulland TK, Buchan BW, Ketterer MR, Fernandes-Alnemri T, Meyerholz DK, et al. (2010) Cutting edge: mutation of Francisella tularensis mviN leads to increased macrophage absent in melanoma 2 inflammasome activation and a loss of virulence. J Immunol 185: 2670-2674. doi: 10.4049/jimmunol.1001610 PMID: 20679532
41. Dotson RJ, Rabadi SM, Westcott EL, Bradley S, Catlett SV, et al. (2013) Repression of inflammasome by Francisella tularensis during early stages of infection. J Biol Chem 288: 23844-23857. doi: 10.1074/jbc.M113.490086 PMID: 23821549
42. Dai WJ, Kohler G, Brombacher F (1997) Both innate and acquired immunity to Listeria monocytogenes infection are increased in IL-10-deficient mice. J Immunol 158: 2259-2267. PMID: 9036973
43. Brockman MA, Kwon DS, Tighe DP, Pavlik DF, Rosato PC, et al. (2009) IL-10 is up-regulated in multiple cell types during viremic HIV infection and reversibly inhibits virus-specific T cells. Blood 114: 346-356. doi: 10.1182/blood-2008-12-191296 PMID: 19365081
44. Lin Y, Ritchea S, Logar A, Slight S, Messmer M, et al. (2009) Interleukin-17 is required for T helper 1 cell immunity and host resistance to the intracellular pathogen Francisella tularensis. Immunity 31: 799-810. doi: 10.1016/j.immuni.2009.08.025 PMID: 19853481
45. Gosselin EJ, Wardwell K, Gosselin DR, Alter N, Fisher JL, et al. (1992) Enhanced antigen presentation using human Fc gamma receptor (monocyte/macrophage)-specific immunogens. J Immunol 149: 3477-3481. PMID: 1431118
46. Walters KA, Olsufka R, Kuestner RE, Cho JH, Li H, et al. (2013) Francisella tularensis subsp. tularensis induces a unique pulmonary inflammatory response: role of bacterial gene expression in temporal regulation of host defense responses. PLOS ONE 8: e62412. doi: 10.1371/journal.pone.0062412 PMID: 23690939
47. Shinozawa Y, Matsumoto T, Uchida K, Tsujimoto S, Iwakura Y, et al. (2002) Role of interferon-gamma in inflammatory responses in murine respiratory infection with Legionella pneumophila. J Med Microbiol 51: 225-230. PMID: 11871617
48. Santic M, Molmeret M, Abu Kwaik Y (2005) Modulation of biogenesis of the Francisella tularensis subsp. novicida-containing phagosome in quiescent human macrophages and its maturation into a phagolysosome upon activation by IFN-gamma. Cell Microbiol 7: 957-967. PMID: 15953028
49. Benoit M, Desnues B, Mege JL (2008) Macrophage polarization in bacterial infections. J Immunol 181: 3733-3739. PMID: 18768823