Amino acids 89-96 of Salmonella typhimurium flagellin represent the major domain responsible for TLR5-independent adjuvanticity in the humoral immune response

Cellular and Molecular Immunology

Volumn 12, Issue 5, 2015, Pages 625-632

  Zhang, Lei ^a,b   Pan, Zhiming ^a   Kang, Xilong ^a   Yang, Yun ^a   Kang, Heekap ^b   Zhang, Na ^a   Rosati, James M ^b   Jiao, Xinan ^a  

^a YANGZHOU UNIVERSITY   (China)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

adjuvanticity; amino acids 89 96; Salmonella typhimurium flagellin; TLR5 activity

Indexed keywords

AMINO ACID; IMMUNOLOGICAL ADJUVANT; INTERLEUKIN 18; INTERLEUKIN 1BETA; TOLL LIKE RECEPTOR 5; AUTACOID; FLAGELLIN; INTERLEUKIN 6; RECOMBINANT PROTEIN; TUMOR NECROSIS FACTOR;

ADAPTIVE IMMUNITY; ANIMAL EXPERIMENT; ARTICLE; BACTERIUM IDENTIFICATION; BINDING AFFINITY; BINDING SITE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; FEMALE; HUMORAL IMMUNITY; IMMUNE RESPONSE; MOLECULAR DYNAMICS; MOLECULAR RECOGNITION; MOUSE; NONHUMAN; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN FUNCTION; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; SIGNAL TRANSDUCTION; ANIMAL; BLOOD; C57BL MOUSE; CHEMISTRY; GENE DELETION; GENETIC RECOMBINATION; GENETICS; HEK293 CELL LINE; HUMAN; KNOCKOUT MOUSE; METABOLISM; MUTATION; PROTEIN TERTIARY STRUCTURE; STRUCTURE ACTIVITY RELATION;

ADJUVANTS, IMMUNOLOGIC; AMINO ACIDS; ANIMALS; FEMALE; FLAGELLIN; HEK293 CELLS; HUMANS; IMMUNITY, HUMORAL; INFLAMMATION MEDIATORS; INTERLEUKIN-6; MICE, INBRED C57BL; MICE, KNOCKOUT; MUTATION; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; RECOMBINATION, GENETIC; SALMONELLA TYPHIMURIUM; SEQUENCE DELETION; STRUCTURE-ACTIVITY RELATIONSHIP; TOLL-LIKE RECEPTOR 5; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84941127257     PISSN: 16727681     EISSN: 20420226     Source Type: Journal    
DOI: 10.1038/cmi.2014.76     Document Type: Article

References (31)

1. Donnelly MA, Steiner TS. Two nonadjacent regions in enteroaggregative Escherichia coli flagellin are required for activation of Toll-like receptor 5. J Biol Chem 2002; 277: 40456-40461.
2. Eaves-Pyles TD, Wong HR, Odoms K, Pyles RB. Salmonella flagellindependent proinflammatory responses are localized to the conserved amino and carboxyl regions of the protein. J Immunol 2001; 167: 7009-7016.
3. Murthy KG, Deb A, Goonesekera S, Szabo C, Salzman AL. Identification of conserved domains in Salmonella muenchen flagellin that are essential for its ability to activate TLR5 and to induce an inflammatory response in vitro. J Biol Chem 2004; 279: 5667-5675.
4. Lightfield KL, Persson J, Brubaker SW, Witte CE, von Moltke J, Dunipace EA et al. Critical function for Naip5 in inflammasome activation by a conserved carboxy-terminal domain of flagellin. Nat Immunol 2008; 9: 1171-1178.
5. Miao EA, Andersen-Nissen E, Warren SE, Aderem A. TLR5 and Ipaf: dual sensors of bacterial flagellin in the innate immune system. Semin Immunopathol 2007; 29: 275-288.
6. Strindelius L, Filler M, Sjoholm I. Mucosal immunization with purified flagellin from Salmonella induces systemic and mucosal immune responses in C3H/HeJ mice. Vaccine 2004; 22: 3797-3808.
7. McSorley SJ, Cookson BT, Jenkins MK. Characterization of CD41 T cell responses during natural infection with Salmonella typhimurium. J Immunol 2000; 164: 986-993.
8. Andersen-Nissen E, Smith KD, Strobe KL, Barrett SL, Cookson BT, Logan SM et al. Evasion of Toll-like receptor 5 by flagellated bacteria. Proc Natl Acad Sci USA 2005; 102: 9247-9252.
9. Yoon SI, Kurnasov O, Natarajan V, Hong M, Gudkov AV, Osterman AL et al. Structural basis of TLR5-flagellin recognition and signaling. Science 2012; 335: 859-864.
10. Newton SM, Jacob CO, Stocker BA. Immune response to cholera toxin epitope inserted in Salmonella flagellin. Science 1989; 244: 70-72.
11. Taylor DN, Treanor JJ, Sheldon EA, Johnson C, Umlauf S, Song L et al. Development of VAX128, a recombinant hemagglutinin (HA) influenza-flagellin fusion vaccine with improved safety and immune response. Vaccine 2012; 30: 5761-5769.
12. Zhang H, Liu L, Wen K, Huang J, Geng S, Shen J et al. Chimeric flagellin expressed by Salmonella typhimurium induces an ESAT-6-specific Th1-type immune response and CTL effects following intranasal immunization. Cell Mol Immunol 2011; 8: 496-501.
13. Mizel SB, Bates JT. Flagellin as an adjuvant: cellular mechanisms and potential. J Immunol 2010; 185: 5677-5682.
14. Nempont C, Cayet D, Rumbo M, Bompard C, Villeret V, Sirard, JC. Deletion of flagellins hypervariable region abrogates antibodymediated neutralization and systemic activation of TLR5-dependent immunity. J Immunol 2008; 181: 2036-2043.
15. Sanders CJ, Franchi L, Yarovinsky F, Uematsu S, Akira S, Nunez G et al. Induction of adaptive immunity by flagellin does not require robust activation of innate immunity. Eur J Immunol 2009; 39: 359-371.
16. Vijay-Kumar M, Carvalho FA, Aitken JD, Fifadara NH, Gewirtz AT. TLR5 or NLRC4 is necessary and sufficient for promotion of humoral immunity by flagellin. Eur J Immunol 2010; 40: 3528-3534.
17. Saha S, Takeshita F, Matsuda T, Jounai N, Kobiyama K, Matsumoto T et al. Blocking of the TLR5 activation domain hampers protective potential of flagellin DNA vaccine. J Immunol 2007; 179: 1147-1154.
18. Bullas LR, Ryu JI. Salmonella typhimurium LT2 strains which are rm1 for all three chromosomally located systems of DNA restriction and modification. J Bacteriol 1983; 156: 471-474.
19. Raffatellu M, Chessa D, Wilson RP, Dusold R, Rubino S, Baumler AJ. The Vi capsular antigen of Salmonella enterica serotype Typhi reduces Toll-like receptor-dependent interleukin-8 expression in the intestinal mucosa. Infect Immun 2005; 73: 3367-3374.
20. Smith KD, Andersen-Nissen E, Hayashi F, Strobe K, Bergman MA, Barrett SL et al. Toll-like receptor 5 recognizes a conserved site on flagellin required for protofilament formation and bacterial motility. Nat Immunol 2003; 4: 1247-1253.
21. Yoshioka K, Aizawa S, Yamaguchi S. Flagellar filament structure and cell motility of Salmonella typhimurium mutants lacking part of the outer domain of flagellin. J Bacteriol 1995; 177: 1090-1093.
22. Smith KD, Valenzuela A, Vigna JL, Aalbers K, Lutz CT. Unwanted mutations in PCR mutagenesis: avoiding the predictable. PCR Methods Appl 1993; 2: 253-257.
23. Ibrahim GF, Fleet GH, Lyons MJ, Walker RA. Method for the isolation of highly purified Salmonella flagellins. J Clin Microbiol 1985; 22: 1040-1044.
24. Rolli J, Loukili N, Levrand S, Rosenblatt-Velin N, Rignault-Clerc S, Waeber B et al. Bacterial flagellin elicits widespread innate immune defense mechanisms, apoptotic signaling, and a sepsis-like systemic inflammatory response in mice. Crit Care 2010; 14: R160.
25. Lamkanfi M, Dixit VM. Inflammasomes: guardians of cytosolic sanctity. Immunol Rev 2009; 227: 95-105.
26. Miao EA, Mao DP, Yudkovsky N, Bonneau R, Lorang CG, Warren SE et al. Innate immune detection of the type III secretion apparatus through the NLRC4 inflammasome. Proc Natl Acad Sci USA 2010; 107: 3076-3080.
27. Poyraz O, Schmidt H, Seidel K, Delissen F, Ader C, TenenboimHet al. Protein refolding is required for assembly of the type three secretion needle. Nat Struct Mol Biol 2010; 17: 788-792.
28. Descamps D, Le Gars M, Balloy V, Barbier D, Maschalidi S, Tohme M et al. Toll-like receptor 5 (TLR5), IL-1beta secretion, and asparagine endopeptidase are critical factors for alveolar macrophage phagocytosis and bacterial killing. Proc Natl Acad Sci USA 2012; 109: 1619-1624.
29. Carvalho FA, Aitken JD, Gewirtz AT, Vijay-Kumar M. TLR5 activation induces secretory interleukin-1 receptor antagonist (sIL-1Ra) and reduces inflammasome-associated tissue damage. Mucosal Immunol 2011; 4: 102-111.
30. McSorley SJ, Ehst BD, Yu Y, Gewirtz AT. Bacterial flagellin is an effective adjuvant for CD41 T cells in vivo. J Immunol 2002; 169: 3914-3919.
31. Lopez-Yglesias AH, Zhao X, Quarles EK, Lai MA, VandenBos T, Strong RK et al. Flagellin induces antibody responses through a TLR5-and inflammasome-independent pathway. J Immunol 2014; 192: 1587-1596.