Native flagellin does not protect mice against an experimental Proteus mirabilis ascending urinary tract infection and neutralizes the protective effect of MrpA fimbrial protein

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• 作者：Paola Scavone (1)
  Ana Umpiérrez (1)
  Analía Rial (2)
  José A. Chabalgoity (2)
  Pablo Zunino (1)
  
• 关键词：MR/P fimbriae ; Urinary tract infection ; Flagellin ; Adjuvant
• 刊名：Antonie van Leeuwenhoek
• 出版年：2014
• 出版时间：June 2014
• 年：2014
• 卷：105
• 期：6
• 页码：1139-1148
• 全文大小：
• 参考文献：1. Asadi Karam MR, Oloomi M, Mahdavi M, Habibi M, Bouzari S (2013) Vaccination with recombinant FimH fused with flagellin enhances cellular and humoral immunity against urinary tract infection in mice. Vaccine 31:1210-216 CrossRef
  2. Bates JT, Uematsu S, Akira S, Mizel SB (2009) Direct stimulation of tlr5+/+ CD11c+ cells is necessary for the adjuvant activity of flagellin. J Immunol 182:7539-547 CrossRef
  3. Braga CJ, Rittner GM, Mu?oz Henao JE, Teixeira AF, Massis LM, Sbrogio-Almeida ME, Taborda CP, Travassos LR, Ferreira LC (2009) Paracoccidioides brasiliensis vaccine formulations based on the gp43-derived P10 sequence and the / Salmonella enterica FliC flagellin. Infect Immun 77:1700-707 CrossRef
  4. Brunner R, Jensen-Jarolim E, Pali-Sch?ll I (2010) The ABC of clinical and experimental adjuvants—a brief overview. Immunol Lett 128:29-5 CrossRef
  5. Chan CY, St John AL, Abraham SN (2013) Mast cell interleukin-10 drives localized tolerance in chronic bladder infection. Immunity 38:349-59 CrossRef
  6. Cunningham AF, Khan M, Ball J, Toellner KM, Serre K, Mohr E, MacLenna IC (2004) Responses to the soluble flagellar protein FliC are Th2, while those to FliC on / Salmonella are Th1. Eur J Immunol 34:2986-995 CrossRef
  7. Defrance T, Vanbervliet B, Briere F, Durand I, Rousset F, Banchereau J (1992) Interleukin 10 and transforming growth factor beta cooperate to induce anti-CD40-activated naive human B cells to secrete immunoglobulin A. J Exp Med 175:671-82 CrossRef
  8. Didierlaurent A, Ferrero I, Otten LA, Dubois B, Reinhardt M, Carlsen H, Blomhoff R, Akira S, Kraehenbuhl JP, Sirard JC (2004) Flagellin promotes myeloid differentiation factor 88-dependent development of Th2-type response. J Immunol 172:6922-930 CrossRef
  9. Dielubanza EJ, Schaeffer AJ (2011) Urinary tract infections in women. Med Clin N Am 95:27-1 CrossRef
  10. Duan Q, Zhou M, Zhu L, Zhu G (2012) Flagella and bacterial pathogenicity. J Basic Microbiol 52:1- CrossRef
  11. Duell BL, Tan CK, Carey AJ, Wu F, Cripps AW, Ulett GC (2012) Recent insights into microbial triggers of interleukin-10 production in the host and the impact on infectious disease pathogenesis. FEMS Immunol Med Microbiol 64:295-13 CrossRef
  12. Errea A, Moreno G, Sisti F, Fernandez J, Rumbo M, Hozbor DF (2010) Mucosal innate response stimulation induced by lipopolysaccharide protects against / Bordetella pertussis colonization. Med Microbiol Immunol 199:103-08 CrossRef
  13. Faezi S, Safarloo M, Behrouz B, Aminmozafari N, Nikokar I, Mahdavi M (2012) Comparison between active and passive immunization with flagellin-based subunit vaccine from / Pseudomonas aeruginosa in burned-mouse model. Iran J Clin Infect Dis 7:10-6
  14. Hayashi F, Smith KD, Ozinsky A, Hawn TR, Yi EC, Goodlett DR, Eng JK, Akira S, Underhill DM, Aderem A (2001) The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 410:1099-103 CrossRef
  15. Honko AN, Mizel SB (2004) Mucosal administration of flagellin induces innate immunity in the mouse lung. Infect Immun 72:676-79 CrossRef
  16. Jacobsen SM, Stickler DJ, Mobley HLT, Shirtliff ME (2008) Complicated catheter-associated urinary tract infections due to / Escherichia coli and / Proteus mirabilis. Clin Microbiol Rev 21:26-9 CrossRef
  17. Jarchum I, Liu M, Lipuma L, Pamer EG (2011) Toll-like receptor 5 stimulation protects mice from acute / Clostridium difficile colitis. Infect Immun 79:1498-503 CrossRef
  18. Johnson JR (1996) Treatment and Prevention of urinary tract infections. In: Mobley HLT, Warren JW (eds) Urinary tract infections: molecular pathogenesis and clinical management. ASM Press, Washington, pp 95-18
  19. Kinnebrew MA, Ubeda C, Zenewicz LA, Smith N, Flavell RA, Pamer EG (2010) Bacterial flagellin stimulates Toll-like receptor 5-dependent defense against vancomycin-resistant / Enterococcus infection. J Infect Dis 201:534-43 CrossRef
  20. Lee SE, Kim SY, Jeong BC, Kim YR, Bae SJ, Ahn OS, Lee JJ, Song HC, Kim JM, Choy HE, Chung SS, Kweon MN, Rhee JH (2006) A bacterial flagellin, / Vibrio vulnificus FlaB, has a strong mucosal adjuvant activity to induce protective immunity. Infect Immun 74:694-02 CrossRef
  21. Legnani-Fajardo C, Zunino P, Algorta G, Laborde HF (1991) Antigenic and immunogenic activity of flagella and fimbriae preparations from uropathogenic / Proteus mirabilis. Can J Microbiol 37:325-28 CrossRef
  22. Legnani-Fajardo C, Zunino P, Piccini C, Allen A, Maskell D (1996) Defined mutants of / Proteus mirabilis lacking flagella cause ascending urinary tract infection in mice. Microb Pathog 21:395-05 CrossRef
  23. Li X, Erbe JL, Lockatell CV, Johnson DE, Jobling MG, Holmes RK, Mobley HLT (2004) Use of translational fusion of the MrpH fimbrial adhesin-binding domain with the cholera toxin A2 domain, coexpressed with the cholera toxin B subunit, as an intranasal vaccine to prevent experimental urinary tract infection by / Proteus mirabilis. Infect Immun 72:7306-310 CrossRef
  24. Mizel SB, Bates JT (2010) Flagellin as an adjuvant: cellular mechanisms and potential. J Immunol 185:5677-682 CrossRef
  25. Moore KW, Vieira P, Fiorentino DF, Trounstine ML, Khan TA, Mosmann TR (1990) Homology of cytokine synthesis inhibitory factor (IL-10) to the Epstein–Barr virus gene / BCRFI. Science 248:1230-234 CrossRef
  26. Mu?oz N, Van Maele L, Marques JM, Rial A, Sirard JC, Chabalgoity JA (2010) Mucosal administration of flagellin protects mice from / Streptococcus pneumoniae lung infection. Infect Immun 78:4226-233 CrossRef
  27. Nicolle LE (2005) Catheter related urinary tract infection. Drugs Aging 22:627-39 CrossRef
  28. Nielubowicz GR, Mobley HLT (2010) Host-pathogen interactions in urinary tract infection. Nat Rev Urol 7:430-41 CrossRef
  29. Pellegrino R, Galvalisi U, Scavone P, Sosa V, Zunino P (2003) Evaluation of / Proteus mirabilis structural fimbrial proteins as antigens against urinary tract infections. FEMS Immunol Med Microbiol 15:103-10 CrossRef
  30. Rather PN (2005) Swarmer cell differentiation in / Proteus mirabilis. Environ Microbiol 7:1065-073 CrossRef
  31. Salyers AA, Whitt DD (1994) Bacterial pathogenesis, a molecular approach. ASM Press, Washington
  32. Scavone P, Sosa V, Pellegrino R, Galvalisi U, Zunino P (2004) Mucosal vaccination of mice with recombinant / Proteus mirabilis structural fimbrial proteins. Microbes Infect 6:853-60 CrossRef
  33. Scavone P, Miyoshi A, Rial A, Chabalgoity A, Langella P, Azevedo V, Zunino P (2007) Intranasal immunization with recombinant / Lactococcus lactis displaying either anchored or secreted forms of / Proteus mirabilis MrpA fimbrial protein confers specific immune response and induces a significant reduction of kidney bacterial colonisation in mice. Microbes Infect 9:821-28 CrossRef
  34. Scavone P, Rial A, Umpiérrez A, Chabalgoity A, Zunino P (2009) Effects of the administration of cholera toxin as a mucosal adjuvant on the immune and protective response induced by / Proteus mirabilis MrpA fimbrial protein in the urinary tract. Microbiol Immunol 53:233-40 CrossRef
  35. Scavone P, Umpiérrez A, Maskell DJ, Zunino P (2011) Nasal immunization with attenuated / Salmonella Typhimurium expressing an MrpA-TetC fusion protein significantly reduces / Proteus mirabilis colonization in the mouse urinary tract. J Med Microbiol 60:899-04 CrossRef
  36. Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD, Frujimoto EK, Goeke NM, Olson BJ, Klenk DC (1985) Measurement of protein using bicinchoninic acid. Anal Biochem 150:76-5 CrossRef
  37. Smith KD, Andersen-Nissen E, Hayashi F, Strobe K, Bergman MA, Barrett SL, Cookson BT, Aderem A (2003) Toll-like receptor 5 recognizes a conserved site on flagellin required for protofilament formation and bacterial motility. Nat Immunol 4:1247-253 CrossRef
  38. Stamm WE, Martin SM, Bennett JV (1977) Epidemiology of nosocomial infections due to Gram-negative bacilli: aspects relevant to development and use of vaccines. J Infect Dis 136(Suppl):S151–S160 CrossRef
  39. Studier FW, Moffatt BA (1985) Use of a bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J Mol Biol 189:113-30 CrossRef
  40. Subramanian N, Qadri A (2006) Lysophospholipid sensing triggers secretion of flagellin from pathogenic / salmonella. Nat Immunol 7:583-89 CrossRef
  41. Tarahomjoo S (2014) Utilizing bacterial flagellins against infectious diseases and cancers. Antonie Van Leeuwenhoek 105:275-88 CrossRef
  42. Umpiérrez A, Scavone P, Romanin D, Marqués JM, Chabalgoity JA, Rumbo M, Zunino P (2013) Innate immune responses to / Proteus mirabilis flagellin in the urinary tract. Microbes Infect 15:688-96 CrossRef
  43. Warren JW, Tenney JH, Hoopes JM, Muncie HL, Anthony WC (1982) A prospective microbiologic study of bacteriuria in patients with chronic indwelling urethral catheters. J Infect Dis 146:719-23 CrossRef
  44. Yu FS, Cornicelli MD, Kovach MA, Newstead MW, Zeng X, Kumar A, Gao N, Yoon SG, Gallo RL, Standiford TJ (2010) Flagellin stimulates protective lung mucosal immunity: role of cathelicidin-related antimicrobial peptide. J Immunol 185:1142-149 CrossRef
  45. Zunino P, Geymonat L, Allen AG, Legnani-Fajardo C, Maskell DJ (2000) Virulence of a / Proteus mirabilis ATF isogenic mutant is not impaired in a mouse model of ascending urinary tract infection. FEMS Immunol Med Microbiol 29:137-43 CrossRef
  
• 作者单位：Paola Scavone (1)
  Ana Umpiérrez (1)
  Analía Rial (2)
  José A. Chabalgoity (2)
  Pablo Zunino (1)
  
  1. Department of Microbiology, Instituto de Investigaciones Biológicas Clemente Estable, Av. Italia, 3318, CP 11600, Montevideo, Uruguay
  2. Department of Biotechnology, Facultad de Medicina, Instituto de Higiene, UdelaR, Av. A. Navarro, 3051, CP 11600, Montevideo, Uruguay
  
• ISSN：1572-9699

文摘

Proteus mirabilis expresses several virulence factors including MR/P fimbriae and flagella. Bacterial flagellin has frequently shown interesting adjuvant and protective properties in vaccine formulations. However, native P. mirabilis flagellin has not been analyzed so far. Native P. mirabilis flagellin was evaluated as a protective antigen and as an adjuvant in co-immunizations with MrpA (structural subunit of MR/P fimbriae) using an ascending UTI model in the mouse. Four groups of mice were intranasally treated with either MrpA, native flagellin, both proteins and PBS. Urine and blood samples were collected before and after immunization for specific antibodies determination. Cytokine production was assessed in immunized mice splenocytes cultures. Mice were challenged with P. mirabilis, and bacteria quantified in kidneys and bladders. MrpA immunization induced serum and urine specific anti-MrpA antibodies while MrpA coadministered with native flagellin did not. None of the animals developed significant anti-flagellin antibodies. Only MrpA-immunized mice showed a significant decrease of P. mirabilis in bladders and kidneys. Instead, infection levels in MrpA-flagellin or flagellin-treated mice showed no significant differences with the control group. IL-10 was significantly induced in splenocytes of mice that received native flagellin or MrpA-flagellin. Native P. mirabilis flagellin did not protect mice against an ascending UTI. Moreover, it showed an immunomodulatory effect, neutralizing the protective role of MrpA. P. mirabilis flagellin exhibits particular immunological properties compared to other bacterial flagellins.