Francisella tularensis live vaccine strain folate metabolism and pseudouridine synthase gene mutants modulate macrophage caspase-1 activation

Infection and Immunity

Volumn 81, Issue 1, 2013, Pages 201-208

  Ulland, Tyler K ^a   Janowski, Ann M ^a   Buchan, Blake W ^a   Faron, Matthew ^a   Cassel, Suzanne L ^a,b   Jones, Bradley D ^a   Sutterwala, Fayyaz S ^a,b,c  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF IOWA   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 FORMYLTETRAHYDROFOLATE CYCLOLIGASE; BACTERIAL VACCINE; FOLIC ACID; INFLAMMASOME; INTERLEUKIN 18; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; LIGASE; LIVE VACCINE; PSEUDOURIDINE SYNTHASE; SYNTHETASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL GENE; BACTERIAL METABOLISM; BACTERIAL STRAIN; BACTERIUM MUTANT; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOKINE RESPONSE; DRUG CYTOTOXICITY; ENZYME ACTIVATION; FOLATE METABOLISM; FRANCISELLA TULARENSIS; GENE IDENTIFICATION; IN VITRO STUDY; IN VIVO STUDY; INFECTION CONTROL; MACROPHAGE; MACROPHAGE ACTIVATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; TULAREMIA; WILD TYPE;

ANIMALS; BACTERIAL VACCINES; CARBON-NITROGEN LIGASES; CASPASE 1; FOLIC ACID; FRANCISELLA TULARENSIS; INFLAMMASOMES; INTERLEUKIN-18; INTERLEUKIN-1BETA; INTRAMOLECULAR TRANSFERASES; MACROPHAGE ACTIVATION; MACROPHAGES; MICE; MICE, INBRED C57BL; MUTATION; PHAGOSOMES; TULAREMIA; VACCINES, ATTENUATED; VIRULENCE;

EID: 84871886258     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00991-12     Document Type: Article

References (42)

1. McLendon MK, Apicella MA, Allen LA. 2006. Francisella tularensis: taxonomy, genetics, and immunopathogenesis of a potential agent of biowarfare. Annu. Rev. Microbiol. 60:167-185.
2. Saslaw S, Eigelsback HT, Wilson HE, Prior JA, Carhart S. 1961. Tularemia vaccine study I. Intracutaneous challenge. Arch. Intern. Med. 107:121-133.
3. Saslaw S, Eigelsback HT, Prior JA, Wilson HE, Carhart S. 1961. Tularemia vaccine study II. Respiratory challenge. Arch. Intern. Med. 107:134-146.
4. Sjöstedt A. 2003. Virulence determinants and protective antigens of Fran-cisella tularensis. Curr. Opin. Microbiol. 6:66-71.
5. Cole LE, Shirley KA, Barry E, Santiago A, Rallabhandi P, Elkins KL, Puche AC, Michalek SM, Vogel SN. 2007. Toll-like receptor 2-mediated signaling requirements for Francisella tularensis live vaccine strain infection of murine macrophages. Infect. Immun. 75:4127-4137.
6. Fernandes-Alnemri T, Yu JW, Juliana C, Solorzano L, Kang S, Wu J, Datta P, McCormick M, Huang L, McDermott E, Eisenlohr L, Landel CP, Alnemri ES. 2010. The AIM2 inflammasome is critical for innate immunity to Francisella tularensis. Nat. Immunol. 11:385-393.
7. Hong K, Wickstrum JR, Yeh H, Parmely MJ. 2007. Toll-like receptor 2 controls the gamma interferon response to Francisella tularensis by mouse liver lymphocytes. Infect. Immun. 75:5338-5345.
8. Jones JW, Kayagaki N, Broz P, Henry T, Newton K, O'Rourke K, Chan S, Dong J, Qu Y, Roose-Girma M, Dixit VM, Monack DM. 2010. Absent in melanoma 2 is required for innate immune recognition of Francisella tularensis. Proc. Natl. Acad. Sci. U. S. A. 107:9771-9776.
9. Rathinam VA, Jiang Z, Waggoner SN, Sharma S, Cole LE, Waggoner L, Vanaja SK, Monks BG, Ganesan S, Latz E, Hornung V, Vogel SN, Szomolanyi-Tsuda E, Fitzgerald KA. 2010. The AIM2 inflammasome is essential for host defense against cytosolic bacteria and DNA viruses. Nat. Immunol. 11:395-402.
10. Checroun C, Wehrly TD, Fischer ER, Hayes SF, Celli J. 2006. Autophagy-mediated reentry of Francisella tularensis into the endocytic compartment after cytoplasmic replication. Proc. Natl. Acad. Sci. U. S. A. 103:14578-14583.
11. Clemens DL, Lee BY, Horwitz MA. 2004. Virulent and avirulent strains of Francisella tularensis prevent acidification and maturation of their phagosomes and escape into the cytoplasm in human macrophages. Infect. Immun. 72:3204-3217.
12. Huang MT, Mortensen BL, Taxman DJ, Craven RR, Taft-Benz S, Kijek TM, Fuller JR, Davis BK, Allen IC, Brickey WJ, Gris D, Wen H, Kawula TH, Ting JP. 2010. Deletion of ripA alleviates suppression of the inflammasome and MAPK by Francisella tularensis. J. Immunol. 185:5476-5485.
13. Peng K, Broz P, Jones J, Joubert L, Monack D. 2011. Elevated AIM2-mediated pyroptosis triggered by hypercytotoxic Francisella mutant strains is attributed to increased intracellular bacteriolysis. Cell. Microbiol. 13:1586-1600.
14. Shimada T, Park BG, Wolf AJ, Brikos C, Goodridge HS, Becker CA, Reyes CN, Miao EA, Aderem A, Gotz F, Liu GY, Underhill DM. 2010. Staphylococcus aureus evades lysozyme-based peptidoglycan digestion that links phagocytosis, inflammasome activation, and IL-1Β secretion. Cell Host Microbe 7:38-49.
15. Sutterwala FS, Mijares LA, Li L, Ogura Y, Kazmierczak BI, Flavell RA. 2007. Immune recognition of Pseudomonas aeruginosa mediated by the IPAF/NLRC4 inflammasome. J. Exp. Med. 204:3235-3245.
16. Ulland TK, Buchan BW, Ketterer MR, Fernandes-Alnemri T, Meyer-holz DK, Apicella MA, Alnemri ES, Jones BD, Nauseef WM, Sutterwala FS. 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.
17. Jayakar HR, Parvathareddy J, Fitzpatrick EA, Bina XR, Bina JE, Re F, Emery FD, Miller MA. 2011. A galU mutant of Francisella tularensis is attenuated for virulence in a murine pulmonary model of tularemia. BMC Microbiol. 11:179-194.
18. Weiss DS, Brotcke A, Henry T, Margolis JJ, Chan K, Monack DM. 2007. In vivo negative selection screen identifies genes required for Francisella virulence. Proc. Natl. Acad. Sci. U. S. A. 104:6037-6042.
19. Buchan BW, McLendon MK, Jones BD. 2008. Identification of differentially regulated Francisella tularensis genes by use of a newly developed Tn5-based transposon delivery system. Appl. Environ. Microbiol. 74:2637-2645.
20. Buchan BW, McCaffrey RL, Lindemann SR, Allen LA, Jones BD. 2009. Identification of migR, a regulatory element of the Francisella tularensis live vaccine strain iglABCD virulence operon required for normal replication and trafficking in macrophages. Infect. Immun. 77:2517-2529.
21. Chamberlain RE. 1965. Evaluation of live tularemia vaccine prepared in a chemically defined medium. Appl. Microbiol. 13:232-235.
22. Glaccum MB, Stocking KL, Charrier K, Smith JL, Willis CR, Maliszewski C, Livingston DJ, Peschon JJ, Morrissey PJ. 1997. Phenotypic and functional characterization of mice that lack the type I receptor for IL-1. J. Immunol. 159:3364-3371.
23. Kuida K, Lippke JA, Ku G, Harding MW, Livingston DJ, Su MS, Flavell RA. 1995. Altered cytokine export and apoptosis in mice deficient in interleukin-1Β converting enzyme. Science 267:2000-2003.
24. Lara-Tejero M, Sutterwala FS, Ogura Y, Grant EP, Bertin J, Coyle AJ, Flavell RA, Gaĺaln JE. 2006. Role of the caspase-1 inflammasome in Salmonella typhimurium pathogenesis. J. Exp. Med. 203:1407-1412.
25. Sutterwala FS, Ogura Y, Szczepanik M, Lara-Tejero M, Lichtenberger GS, Grant EP, Bertin J, Coyle AJ, Galán JE, Askenase PW, Flavell RA. 2006. Critical role for NALP3/CIAS1/Cryopyrin in innate and adaptive immunity through its regulation of caspase-1. Immunity 24:317-327.
26. Takeda K, Tsutsui H, Yoshimoto T, Adachi O, Yoshida N, Kishimoto T, Okamura H, Nakanishi K, Akira S. 1998. Defective NK cell activity and Th1 response in IL-18-deficient mice. Immunity 8:383-390.
27. Sutterwala FS, Noel GJ, Clynes R, Mosser DM. 1997. Selective suppression of interleukin-12 induction after macrophage receptor ligation. J. Exp. Med. 185:1977-1985.
28. Cassel SL, Eisenbarth SC, Iyer SS, Sadler JJ, Colegio OR, Tephly LA, Carter AB, Rothman PB, Flavell RA, Sutterwala FS. 2008. The Nalp3 inflammasome is essential for the development of silicosis. Proc. Natl. Acad. Sci. U. S. A. 105:9035-9040.
29. Grimshaw CE, Henderson GB, Soppe GG, Hansen G, Mathur EJ, Huennekens FM. 1984. Purification and properties of 5,10,-methenyltetrahydrofolate synthetase from Lactobacillus casei. J. Biol. Chem. 259:2728-2733.
30. Hancock AN, Coleman RS, Johnson RT, Sarisky CA, Johann TW. 2008. Investigations of the roles of arginine 115 and lysine 120 in the active site of 5,10-methenyltetrahydrofolate synthetase from Mycoplasma pneumoniae. Protein J. 27:303-308.
31. Leemans JC, Cassel SL, Sutterwala FS. 2011. Sensing damage by the NLRP3 inflammasome. Immunol. Rev. 243:152-162.
32. Schroder K, Sagulenko V, Zamoshnikova A, Richards AA, Cridland JA, Irvine KM, Stacey KJ, Sweet MJ. 27 July2012. Acute lipopolysaccharide priming boosts inflammasome activation independently of inflammasome sensor induction. Immunobiology [Epub ahead of print.]
33. Pedra JH, Cassel SL, Sutterwala FS. 2009. Sensing pathogens and danger signals by the inflammasome. Curr. Opin. Immunol. 21:10-16.
34. Bürckstümmer T, Baumann C, Blüml S, Dixit E, Durnberger G, Jahn H, Planyavsky M, Bilban M, Colinge J, Bennett KL, Superti-Furga G. 2009. An orthogonal proteomic-genomic screen identifies AIM2 as a cytoplasmic DNA sensor for the inflammasome. Nat. Immunol. 10:266-272.
35. Hornung V, Ablasser A, Charrel-Dennis M, Bauernfeind F, Horvath G, Caffrey DR, Latz E, Fitzgerald KA. 2009. AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC. Nature 458:514-518.
36. Roberts TL, Idris A, Dunn JA, Kelly GM, Burnton CM, Hodgson S, Hardy LL, Garceau V, Sweet MJ, Ross IL, Hume DA, Stacey KJ. 2009. HIN-200 proteins regulate caspase activation in response to foreign cytoplasmic DNA. Science 323:1057-1060.
37. Gutgsell NS, Deutscher MP, Ofengand J. 2005. The pseudouridine synthase RluD is required for normal ribosome assembly and function in Escherichia coli. RNA 11:1141-1152.
38. Leppik M, Peil L, Kipper K, Liiv A, Remme J. 2007. Substrate specificity of the pseudouridine synthase RluD in Escherichia coli. FEBS J. 274:5759-5766.
39. Fernandes-Alnemri T, Yu JW, Datta P, Wu J, Alnemri ES. 2009. AIM2 activates the inflammasome and cell death in response to cytoplasmic DNA. Nature 458:509-513.
40. Barker JR, Chong A, Wehrly TD, Yu J, Rodriguez SA, Liu J, Celli J, Arulanandam BP, Klose KE. 2009. The Francisella tularensis pathogenicity island encodes a secretion system that is required for phagosome escape and virulence. Mol. Microbiol. 74:1459-1470.
41. Gavrilin MA, Bouakl IJ, Knatz NL, Duncan MD, Hall MW, Gunn JS, Wewers MD. 2006. Internalization and phagosome escape required for Francisella to induce human monocyte IL-1Β processing and release. Proc. Natl. Acad. Sci. U. S. A. 103:141-146.
42. Mariathasan S, Weiss DS, Dixit VM, Monack DM. 2005. Innate immunity against Francisella tularensis is dependent on the ASC/caspase 1 axis. J. Exp. Med. 202:1043-1049.