Treponema pallidum flagellins elicit proinflammatory cytokines from human monocytes via TLR5 signaling pathway

Immunobiology

Volumn 222, Issue 5, 2017, Pages 709-718

  Xu, Man ^a   Xie, Yafeng ^a,b   Jiang, Chuanhao ^c   Xiao, Yongjian ^b   Kuang, Xingxing ^a   wen, Yating ^a   Tan, Yuan ^a   Tan, Manyi ^a   Zhao, Feijun ^a   Zeng, Tiebing ^a   Wu, Yimou ^a  

^a UNIVERSITY OF SOUTH CHINA   (China)

^b THE SECOND AFFILIATED HOSPITAL OF UNIVERSITY OF SOUTH CHINA   (China)

^c CENTRAL SOUTH UNIVERSITY   (China)

Author keywords

Flagellin; Human monocytes; Inflammation; TLR5 signaling; Treponema pallidum

Indexed keywords

FLAGELLIN; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; MYELOID DIFFERENTIATION FACTOR 88; PATHOGEN ASSOCIATED MOLECULAR PATTERN; SMALL INTERFERING RNA; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 5; TUMOR NECROSIS FACTOR; AUTACOID; CYTOKINE;

ARTICLE; CELL STIMULATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE ASSOCIATION; DOWN REGULATION; ENZYME INHIBITION; GENE; GENE SILENCING; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; INFLAMMATION; MONOCYTE; PATHOGENESIS; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SYPHILIS; TISSUE INJURY; TLR5 GENE; TREPONEMA PALLIDUM; WESTERN BLOTTING; CELL LINE; DOSE RESPONSE; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; MAPK SIGNALING; METABOLISM; MICROBIOLOGY; RNA INTERFERENCE;

CELL LINE; CYTOKINES; DOSE-RESPONSE RELATIONSHIP, DRUG; DOSE-RESPONSE RELATIONSHIP, IMMUNOLOGIC; FLAGELLIN; GENE EXPRESSION REGULATION; HUMANS; INFLAMMATION MEDIATORS; MAP KINASE SIGNALING SYSTEM; MONOCYTES; MYELOID DIFFERENTIATION FACTOR 88; NF-KAPPA B; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SYPHILIS; TOLL-LIKE RECEPTOR 5; TREPONEMA PALLIDUM;

EID: 85009958081     PISSN: 01712985     EISSN: 18783279     Source Type: Journal    
DOI: 10.1016/j.imbio.2017.01.002     Document Type: Article

References (45)

1. Abdul-Aziz, M., Tsolaki, A.G., Kouser, L., Carroll, M.V., Al-Ahdal, M.N., Sim, R.B., Kishore, U., Complement factor H interferes with Mycobacterium bovis BCG entry into macrophages and modulates the pro-inflammatory cytokine response. Immunobiology, 221, 2016, 944.
2. Aderem, A., Ulevitch, R.J., Toll-like receptors in the induction of the innate immune response. Nature, 406, 2000, 782.
3. Andersen-Nissen, E., Smith, K.D., Strobe, K.L., Barrett, S.L., Cookson, B.T., Logan, S.M., Aderem, A., Evasion of Toll-like receptor 5 by flagellated bacteria. Proc. Natl. Acad. Sci. U. S. A., 102, 2005, 9247.
4. Bandyopadhaya, A., Sarkar, M., Chaudhuri, K., IL-1beta expression in Int407 is induced by flagellin of Vibrio cholerae through TLR5 mediated pathway. Microb. Pathog., 44, 2008, 524.
5. Batah, J., Deneve-Larrazet, C., Jolivot, P.A., Kuehne, S., Collignon, A., Marvaud, J.C., Kansau, I., Clostridium difficile flagella predominantly activate TLR5-linked NF-kappaB pathway in epithelial cells. Anaerobe, 38, 2016, 116.
6. Baughn, R.E., Musher, D.M., Secondary syphilitic lesions. Clin. Microbiol. Rev., 18, 2005, 205.
7. Bellhouse, C., Walker, S., Fairley, C.K., Vodstrcil, L.A., Bradshaw, C.S., Chen, M.Y., Chow, E.P., Patterns of sexual behaviour and sexual healthcare needs among transgender individuals in Melbourne, Australia. Sex Transm. Infect., 2016, 10.1136/sextrans-2016-052710.
8. Bernardino, A.L., Myers, T.A., Alvarez, X., Hasegawa, A., Philipp, M.T., Toll-like receptors: insights into their possible role in the pathogenesis of lyme neuroborreliosis. Infect. Immun., 76, 2008, 4385.
9. Bjekic, M., Markovic, M., Sipetic, S., Clinical manifestations of primary syphilis in homosexual men. Braz. J. Infect. Dis., 16, 2012, 387.
10. Chaban, B., Hughes, H.V., Beeby, M., The flagellum in bacterial pathogens: for motility and a whole lot more. Semin. Cell Dev. Biol., 46, 2015, 91.
11. Cho, H.Y., Choi, E.K., Lee, S.W., Kim, K.H., Park, S.J., Lee, C.K., Lee, S.W., All-trans retinoic acid induces TLR-5 expression and cell differentiation and promotes flagellin-mediated cell functions in human THP-1 cells. Immunol. Lett., 136, 2011, 97.
12. Gmiterek, A., Klopot, A., Wojtowicz, H., Trindade, S.C., Olczak, M., Olczak, T., Immune response of macrophages induced by Porphyromonas gingivalis requires HmuY protein. Immunobiology, 221, 2016, 1382.
13. Hayden, M.S., Ghosh, S., Shared principles in NF-kappaB signaling. Cell, 132, 2008, 344.
14. Haiko, J., Westerlund-Wikstrom, B., The role of the bacterial flagellum in adhesion and virulence. Biology (Basel), 2, 2013, 1242.
15. Harrison, L.M., Rallabhandi, P., Michalski, J., Zhou, X., Steyert, S.R., Vogel, S.N., Kaper, J.B., Vibrio cholerae flagellins induce Toll-like receptor 5-mediated interleukin-8 production through mitogen-activated protein kinase and NF-kappaB activation. Infect. Immun., 76, 2008, 5524.
16. Ho, E.L., Lukehart, S.A., Syphilis: using modern approaches to understand an old disease. J. Clin. Invest., 121, 2011, 4584.
17. Introcaso, C.E., Gruber, D., Bradley, H., Peterman, T.A., Ewell, J., Wendell, D., Foxhood, J., Su, J.R., Weinstock, H.S., Markowitz, L.E., Challenges in congenital syphilis surveillance: how are congenital syphilis investigations classified?. Sex Transm. Dis., 40, 2013, 695.
18. Jandhyala, D.M., Rogers, T.J., Kane, A., Paton, A.W., Paton, J.C., Thorpe, C.M., Shiga toxin 2 and flagellin from shiga-toxigenic Escherichia coli superinduce interleukin-8 through synergistic effects on host stress-activated protein kinase activation. Infect. Immun., 78, 2010, 2984.
19. Janeway, C.A. Jr., Medzhitov, R., Innate immune recognition. Annu. Rev. Immunol., 20, 2002, 197.
20. Jeon, J.H., Ahn, K.B., Kim, S.K., Im, J., Yun, C.H., Han, S.H., Bacterial flagellin induces IL-6 expression in human basophils. Mol. Immunol., 65, 2015, 168.
21. Jiang, C., Xiao, J., Xie, Y., Xiao, Y., Wang, C., Kuang, X., Xu, M., Li, R., Zeng, T., Liu, S., Yu, J., Zhao, F., Wu, Y., Evaluation of FlaB1, FlaB2, FlaB3, and Tp0463 of Treponema pallidum for serodiagnosis of syphilis. Diagn. Microbiol. Infect. Dis., 84, 2016, 105.
22. Kalichman, S.C., Pellowski, J., Turner, C., Prevalence of sexually transmitted co-infections in people living with HIV/AIDS: systematic review with implications for using HIV treatments for prevention. Sex. Transm. Infect., 87, 2011, 183.
23. Kim, Y.J., Lee, J.H., Lee, Y., Jia, J., Paek, S.H., Kim, H.B., Jin, S., Ha, U.H., Nucleoside diphosphate kinase and flagellin from Pseudomonas aeruginosa induce interleukin 1 expression via the Akt/NF-kappaB signaling pathways. Infect. Immun., 82, 2014, 3252.
24. Klapproth, J.M., Sasaki, M., Bacterial induction of proinflammatory cytokines in inflammatory bowel disease. Inflamm. Bowel Dis., 16, 2010, 2173.
25. Lee, S.K., Stack, A., Katzowitsch, E., Aizawa, S.I., Suerbaum, S., Josenhans, C., Helicobacter pylori flagellins have very low intrinsic activity to stimulate human gastric epithelial cells via TLR5. Microbes Infect., 5, 2003, 1345.
26. Liu, J., Howell, J.K., Bradley, S.D., Zheng, Y., Zhou, Z.H., Norris, S.J., Cellular architecture of Treponema pallidum: novel flagellum, periplasmic cone, and cell envelope as revealed by cryo electron tomography. J. Mol. Biol., 403, 2010, 546.
27. Liu, S., Wang, S., Wu, Y., Zhao, F., Zeng, T., Zhang, Y., Zhang, Q., Gao, D., Production of proinflammatory cytokines in the human THP-1 monocyte cell line following induction by Tp0751, a recombinant protein of Treponema pallidum. Sci. China Life Sci., 53, 2010, 229.
28. Majewska, M., Szczepanik, M., The role of Toll-like receptors (TLR) in innate and adaptive immune responses and their function in immune response regulation. Postepy Hig Med. Dosw (Online), 60, 2006, 52.
29. Medzhitov, R., Toll-like receptors and innate immunity. Nat. Rev. Immunol., 1, 2001, 135.
30. Oliver, S.E., Aubin, M., Atwell, L., Matthias, J., Cope, A., Mobley, V., Goode, A., Minnerly, S., Stoltey, J., Bauer, H.M., Hennessy, R.R., DiOrio, D., Fanfair, R.N., Peterman, T.A., Markowitz, L., Ocular syphilis – eight jurisdictions, United States, 2014–2015. MMWR. Morb. Mortal. Wkly. Rep., 65, 2016, 1185.
31. Pachathundikandi, S.K., Lind, J., Tegtmeyer, N., El-Omar, E.M., Backert, S., Interplay of the gastric pathogen helicobacter pylori with toll-like receptors. BioMed Res. Int., 2015, 2015, 192420.
32. Parthasarathy, G., Philipp, M.T., Inflammatory mediator release from primary rhesus microglia in response to Borrelia burgdorferi results from the activation of several receptors and pathways. J. Neuroinflamm., 12, 2015, 60.
33. Pathela, P., Braunstein, S.L., Blank, S., Shepard, C., Schillinger, J.A., The high risk of an HIV diagnosis following a diagnosis of syphilis: a population-level analysis of New York City men. Clin. Infect. Dis., 61, 2015, 281.
34. Price, J.C., Sheldon, I.M., Granulosa cells from emerged antral follicles of the bovine ovary initiate inflammation in response to bacterial pathogen-associated molecular patterns via toll-like receptor pathways. Biol. Reprod., 89, 2013, 119.
35. Rajagopala, S.V., Titz, B., Goll, J., Parrish, J.R., Wohlbold, K., McKevitt, M.T., Palzkill, T., Mori, H., Finley, R.L. Jr., Uetz, P., The protein network of bacterial motility. Mol. Syst. Biol., 3, 2007, 128.
36. Ramos, H.C., Rumbo, M., Sirard, J.C., Bacterial flagellins: mediators of pathogenicity and host immune responses in mucosa. Trends Microbiol., 12, 2004, 509.
37. Rollauer, S.E., Sooreshjani, M.A., Noinaj, N., Buchanan, S.K., Outer membrane protein biogenesis in Gram-negative bacteria. Philos. Trans. R Soc. Lond. B Biol. Sci., 370, 2015.
38. Sabharwal, H., Cichon, C., Olschlager, T.A., Sonnenborn, U., Schmidt, M.A., Interleukin-8, CXCL1, and MicroRNA miR-146a responses to probiotic escherichia coli nissle 1917 and enteropathogenic E. coli in human intestinal epithelial T84 and monocytic THP-1cells after apical or basolateral infection. Infect. Immun., 84, 2016, 2482.
39. Shen, P., Fillatreau, S., Antibody-independent functions of B cells: a focus on cytokines. Nat. Rev. Immunol., 15, 2015, 441.
40. Silva-Garcia, O., Valdez-Alarcon, J.J., Baizabal-Aguirre, V.M., The Wnt/beta-catenin signaling pathway controls the inflammatory response in infections caused by pathogenic bacteria. Mediators Inflamm., 2014, 2014, 310183.
41. Taxman, D.J., Huang, M.T., Ting, J.P., Inflammasome inhibition as a pathogenic stealth mechanism. Cell Host Microbe, 8, 2010, 7.
42. Titz, B., Rajagopala, S.V., Ester, C., Hauser, R., Uetz, P., Novel conserved assembly factor of the bacterial flagellum. J. Bacteriol., 188, 2006, 7700.
43. Wanke, D., Mauch-Mucke, K., Holler, E., Hehlgans, T., Human beta-defensin-2 and −3 enhance pro-inflammatory cytokine expression induced by TLR ligands via ATP-release in a P2 × 7R dependent manner. Immunobiology, 221, 2016, 1259.
44. Xie, Y., Xu, M., Xiao, Y., Liu, Z., Jiang, C., Kuang, X., Wang, C., Wu, H., Peng, J., Li, C., Wang, Y., Liu, H., Liu, B., Zhang, X., Zhao, F., Zeng, T., Liu, S., Wu, Y., Treponema pallidum flagellin FlaA2 induces IL-6 secretion in THP-1 cells via the Toll-like receptor 2 signaling pathway. Mol. Immunol., 81, 2016, 42.
45. Zhou, X., Giron, J.A., Torres, A.G., Crawford, J.A., Negrete, E., Vogel, S.N., Kaper, J.B., Flagellin of enteropathogenic Escherichia coli stimulates interleukin-8 production in T84 cells. Infect. Immun., 71, 2003, 2120.