Home LiteratureArticle Details
PMID: 17517865 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

Toll-like receptor 2-mediated signaling requirements for Francisella tularensis live vaccine strain infection of murine macrophages.

Infection and immunity ·Vol. 75 ·No. 8 ·2007-08-00 ·Pages 4127-37

Cole LE, Shirey KA, Barry E, Santiago A, Rallabhandi P, Elkins KL, Puche AC, Michalek SM, Vogel SN

Abstract

Francisella tularensis, an aerobic, non-spore-forming, gram-negative coccobacillus, is the causative agent of tularemia. We reported previously that F. tularensis live vaccine strain (LVS) elicited strong, dose-dependent NF-kappaB reporter activity in Toll-like receptor 2 (TLR2)-expressing HEK293T cells and proinflammatory gene expression in primary murine macrophages. Herein, we report that F. tularensis LVS-induced murine macrophage proinflammatory cytokine gene and protein expression are overwhelmingly TLR2 dependent, as evidenced by the abrogated responses of TLR2(-/-) macrophages. F. tularensis LVS infection also increased expression of TLR2 both in vitro, in mouse macrophages, and in vivo, in livers from F. tularensis LVS-infected mice. Colocalization of intracellular F. tularensis LVS, TLR2, and MyD88 was visualized by confocal microscopy. Signaling was abrogated if the F. tularensis LVS organisms were heat or formalin killed or treated with chloramphenicol, indicating that the TLR2 agonist activity is dependent on new bacterial protein synthesis. F. tularensis LVS replicates in macrophages; however, bacterial replication was not required for TLR2 signaling because LVSDeltaguaA, an F. tularensis LVS guanine auxotroph that fails to replicate in the absence of exogenous guanine, activated NF-kappaB in TLR2-transfected HEK293T cells and induced cytokine expression in wild-type macrophages comparably to wild-type F. tularensis LVS. Collectively, these data indicate that the primary macrophage response to F. tularensis LVS is overwhelmingly TLR2 dependent, requires de novo bacterial protein synthesis, and is independent of intracellular F. tularensis replication.

MeSH Terms
Animals Bacterial Proteins/biosynthesis Bacterial Vaccines/immunology Cell Line Cytokines/biosynthesis Disease Models, Animal Francisella tularensis/immunology,physiology Gene Expression Humans Liver/pathology Macrophages/chemistry,microbiology Mice Mice, Inbred C57BL Mice, Knockout Microscopy, Confocal Myeloid Differentiation Factor 88/analysis NF-kappa B p50 Subunit/analysis Phagosomes/microbiology RNA, Messenger/analysis Signal Transduction/immunology Toll-Like Receptor 2/analysis,genetics,immunology
Chemicals
Bacterial Proteins Bacterial Vaccines Cytokines Myeloid Differentiation Factor 88 NF-kappa B p50 Subunit NFKB1 protein, human RNA, Messenger Toll-Like Receptor 2
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Cole Leah E
Department of Microbiology and Immunology, University of Maryland, Baltimore, 660 West Redwood Street, Room 324, Baltimore, MD 21201, USA.
Shirey Kari Ann
Barry Eileen
Santiago Araceli
Rallabhandi Prasad
Elkins Karen L
Puche Adam C
Michalek Suzanne M
Vogel Stefanie N
References (59)
59 references, click to expand
  1. Porin of Shigella dysenteriae enhances mRNA levels for Toll-like receptor 2 and MyD88, up-regulates CD80 of murine macrophage, and induces the release of interleukin-12.
    FEMS Immunol Med Microbiol. 2003 Dec 5;39(3):213-9 PMID: 14642305
  2. Upregulation of toll-like receptor 2 gene expression in macrophage response to peptidoglycan and high concentration of lipopolysaccharide is involved in NF-kappa b activation.
    Infect Immun. 2001 May;69(5):2788-96 PMID: 11292690
  3. Genetic control of susceptibility to Salmonella typhimurium in mice: role of the LPS gene.
    J Immunol. 1980 Jan;124(1):20-4 PMID: 6985638
  4. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene.
    Science. 1998 Dec 11;282(5396):2085-8 PMID: 9851930
  5. A Toll-like receptor recognizes bacterial DNA.
    Nature. 2000 Dec 7;408(6813):740-5 PMID: 11130078
  6. Francisella tularensis selectively induces proinflammatory changes in endothelial cells.
    J Immunol. 2003 Sep 1;171(5):2563-70 PMID: 12928407
  7. Bacterial lipopolysaccharide and IFN-gamma induce Toll-like receptor 2 and Toll-like receptor 4 expression in human endothelial cells: role of NF-kappa B activation.
    J Immunol. 2001 Feb 1;166(3):2018-24 PMID: 11160251
  8. Signaling by toll-like receptor 2 and 4 agonists results in differential gene expression in murine macrophages.
    Infect Immun. 2001 Mar;69(3):1477-82 PMID: 11179315
  9. Cutting edge: CATERPILLER: a large family of mammalian genes containing CARD, pyrin, nucleotide-binding, and leucine-rich repeat domains.
    J Immunol. 2002 Oct 15;169(8):4088-93 PMID: 12370334
  10. The importance of a lipopolysaccharide-initiated, cytokine-mediated host defense mechanism in mice against extraintestinally invasive Escherichia coli.
    J Clin Invest. 1995 Aug;96(2):676-86 PMID: 7635960
  11. Peptidoglycan- and lipoteichoic acid-induced cell activation is mediated by toll-like receptor 2.
    J Biol Chem. 1999 Jun 18;274(25):17406-9 PMID: 10364168
  12. Leptospiral lipopolysaccharide activates cells through a TLR2-dependent mechanism.
    Nat Immunol. 2001 Apr;2(4):346-52 PMID: 11276206
  13. Inhibition of lipopolysaccharide-induced signal transduction in endotoxin-tolerized mouse macrophages: dysregulation of cytokine, chemokine, and toll-like receptor 2 and 4 gene expression.
    J Immunol. 2000 Jun 1;164(11):5564-74 PMID: 10820230
  14. Borrelia burgdorferi lipoprotein-mediated TLR2 stimulation causes the down-regulation of TLR5 in human monocytes.
    J Infect Dis. 2006 Mar 15;193(6):849-59 PMID: 16479520
  15. Introduction of Francisella tularensis at skin sites induces resistance to infection and generation of protective immunity.
    Microb Pathog. 1992 Nov;13(5):417-21 PMID: 1297917
  16. Toll-like receptor 4 expression is required to control chronic Mycobacterium tuberculosis infection in mice.
    J Immunol. 2002 Sep 15;169(6):3155-62 PMID: 12218133
  17. Live vaccine strain of Francisella tularensis: infection and immunity in mice.
    Infect Immun. 1991 Sep;59(9):2922-8 PMID: 1879918
  18. The Toll-like receptor 2 is recruited to macrophage phagosomes and discriminates between pathogens.
    Nature. 1999 Oct 21;401(6755):811-5 PMID: 10548109
  19. Toll-like receptor 4 (TLR4) does not confer a resistance advantage on mice against low-dose aerosol infection with virulent type A Francisella tularensis.
    Microb Pathog. 2004 Oct;37(4):185-91 PMID: 15458779
  20. Lipopolysaccharides of Bacteroides fragilis, Chlamydia trachomatis and Pseudomonas aeruginosa signal via toll-like receptor 2.
    J Med Microbiol. 2004 Aug;53(Pt 8):735-40 PMID: 15272059
  21. Tularemia vaccine study. I. Intracutaneous challenge.
    Arch Intern Med. 1961 May;107:689-701 PMID: 13746668
  22. Difference in susceptibility to gram-negative urinary tract infection between C3H/HeJ and C3H/HeN mice.
    Infect Immun. 1984 Dec;46(3):839-44 PMID: 6389367
  23. The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5.
    Nature. 2001 Apr 26;410(6832):1099-103 PMID: 11323673
  24. Mouse genetic locus Lps influences susceptibility to Neisseria meningitidis infection.
    Infect Immun. 1988 Aug;56(8):1950-5 PMID: 3397181
  25. Tularemia transmitted by insect bites--Wyoming, 2001-2003.
    MMWR Morb Mortal Wkly Rep. 2005 Feb 25;54(7):170-3 PMID: 15729218
  26. Rapid local expression of interleukin-12, tumor necrosis factor alpha, and gamma interferon after cutaneous Francisella tularensis infection in tularemia-immune mice.
    Infect Immun. 1999 Apr;67(4):1789-97 PMID: 10085019
  27. Tularemia.
    Clin Microbiol Rev. 2002 Oct;15(4):631-46 PMID: 12364373
  28. Innate and adaptive immune responses to an intracellular bacterium, Francisella tularensis live vaccine strain.
    Microbes Infect. 2003 Feb;5(2):135-42 PMID: 12650771
  29. Toll-like receptor 2 is required for inflammatory responses to Francisella tularensis LVS.
    Infect Immun. 2006 May;74(5):2809-16 PMID: 16622218
  30. Tularemia vaccine study. II. Respiratory challenge.
    Arch Intern Med. 1961 May;107:702-14 PMID: 13746667
  31. Localization of TLR2 and MyD88 to Chlamydia trachomatis inclusions. Evidence for signaling by intracellular TLR2 during infection with an obligate intracellular pathogen.
    J Biol Chem. 2006 Jan 20;281(3):1652-9 PMID: 16293622
  32. An attenuated strain of the facultative intracellular bacterium Francisella tularensis can escape the phagosome of monocytic cells.
    Infect Immun. 2003 Oct;71(10):5940-50 PMID: 14500514
  33. Francisella tularensis LVS initially activates but subsequently down-regulates intracellular signaling and cytokine secretion in mouse monocytic and human peripheral blood mononuclear cells.
    Microb Pathog. 2005 May-Jun;38(5-6):239-47 PMID: 15925273
  34. Cytokine expression in the liver during the early phase of murine tularemia.
    Infect Immun. 1995 Feb;63(2):534-8 PMID: 7822019
  35. Internalization and phagosome escape required for Francisella to induce human monocyte IL-1beta processing and release.
    Proc Natl Acad Sci U S A. 2006 Jan 3;103(1):141-6 PMID: 16373510
  36. Tularaemia: bioterrorism defence renews interest in Francisella tularensis.
    Nat Rev Microbiol. 2004 Dec;2(12):967-78 PMID: 15550942
  37. Nature of protective immunity to Francisella tularensis.
    Rev Infect Dis. 1989 May-Jun;11(3):440-51 PMID: 2665002
  38. Toll-like receptor 4 (TLR4) plays a relatively minor role in murine defense against primary intradermal infection with Francisella tularensis LVS.
    Immunol Lett. 2005 Feb 15;97(1):151-4 PMID: 15626487
  39. Overexpression of CD14, TLR4, and MD-2 in HEK 293T cells does not prevent induction of in vitro endotoxin tolerance.
    J Endotoxin Res. 2003;9(1):60-4 PMID: 12691621
  40. Francisella tularensis inhibits Toll-like receptor-mediated activation of intracellular signalling and secretion of TNF-alpha and IL-1 from murine macrophages.
    Cell Microbiol. 2003 Jan;5(1):41-51 PMID: 12542469
  41. Regulation of phagosome maturation by signals from toll-like receptors.
    Science. 2004 May 14;304(5673):1014-8 PMID: 15143282
  42. NLRs join TLRs as innate sensors of pathogens.
    Trends Immunol. 2005 Aug;26(8):447-54 PMID: 15967716
  43. Prophylactic effectiveness of live and killed tularemia vaccines. I. Production of vaccine and evaluation in the white mouse and guinea pig.
    J Immunol. 1961 Oct;87:415-25 PMID: 13889609
  44. Innate immunity against Francisella tularensis is dependent on the ASC/caspase-1 axis.
    J Exp Med. 2005 Oct 17;202(8):1043-9 PMID: 16230474
  45. Toll-like receptor 2 is required for control of pulmonary infection with Francisella tularensis.
    Infect Immun. 2006 Jun;74(6):3657-62 PMID: 16714598
  46. The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-beta.
    Mol Cell. 2002 Aug;10(2):417-26 PMID: 12191486
  47. Toll-like receptor 2-deficient mice are highly susceptible to Streptococcus pneumoniae meningitis because of reduced bacterial clearing and enhanced inflammation.
    J Infect Dis. 2002 Sep 15;186(6):798-806 PMID: 12198614
  48. Innate immunity: the virtues of a nonclonal system of recognition.
    Cell. 1997 Oct 31;91(3):295-8 PMID: 9363937
  49. Cellular responses to bacterial cell wall components are mediated through MyD88-dependent signaling cascades.
    Int Immunol. 2000 Jan;12(1):113-7 PMID: 10607756
  50. Mutations in TLR4 signaling that lead to increased susceptibility to infection in humans: an overview.
    J Endotoxin Res. 2005;11(6):333-9 PMID: 16303088
  51. Myeloid differentiation factor-88 (MyD88) is essential for control of primary in vivo Francisella tularensis LVS infection, but not for control of intra-macrophage bacterial replication.
    Microbes Infect. 2006 Mar;8(3):779-90 PMID: 16513388
  52. Factors affecting the escape of Francisella tularensis from the phagolysosome.
    J Med Microbiol. 2004 Oct;53(Pt 10):953-8 PMID: 15358816
  53. Immunologic consequences of Francisella tularensis live vaccine strain infection: role of the innate immune response in infection and immunity.
    J Immunol. 2006 Jun 1;176(11):6888-99 PMID: 16709849
  54. Virulent and avirulent strains of Francisella tularensis prevent acidification and maturation of their phagosomes and escape into the cytoplasm in human macrophages.
    Infect Immun. 2004 Jun;72(6):3204-17 PMID: 15155622
  55. Cutting edge: TLR2-deficient and MyD88-deficient mice are highly susceptible to Staphylococcus aureus infection.
    J Immunol. 2000 Nov 15;165(10):5392-6 PMID: 11067888
  56. Tularemia as a biological weapon: medical and public health management.
    JAMA. 2001 Jun 6;285(21):2763-73 PMID: 11386933
  57. Mode of action of chloramphenicol. I. Action of chloramphenicol on assimilation of ammonia and on synthesis of proteins and nucleic acids in Escherichia coli.
    J Bacteriol. 1954 Jun;67(6):662-73 PMID: 13174493
  58. Cytokine expression in the liver of mice infected with a highly virulent strain of Francisella tularensis.
    FEMS Immunol Med Microbiol. 1996 Mar;13(3):239-44 PMID: 8861036
  59. Human toll-like receptor 2 confers responsiveness to bacterial lipopolysaccharide.
    J Exp Med. 1998 Dec 7;188(11):2091-7 PMID: 9841923
Article Info
Journal
Infection and immunity
Abbr.
Infect Immun
ISSN
0019-9567
Published
2007-08-00
Epub
2007-00-21
Pages
4127-37
Language
English
Region
United States
NLM ID
0246127
PMCID
PMC1951974
Subset
IM
Grants
NIDCD NIH HHS · DC 05739 · United States
NIDCR NIH HHS · DE 09081 · United States
NIDCR NIH HHS · R01 DE009081 · United States
NIAID NIH HHS · U01 AI056460 · United States
NIAID NIH HHS · U54 AI 057168 · United States
NIAID NIH HHS · AI 56460 · United States
NIAID NIH HHS · U54 AI057168 · United States
NIDCD NIH HHS · R03 DC005739 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com