1887

Abstract

Host surface receptors provide bacteria with a foothold from which to attach, colonize and, in some cases, invade tissue and elicit human disease. In this review, we discuss several key host receptors and cognate adhesins that function in bacterial pathogenesis. In particular, we examine the elevated expression of host surface receptors such as CEACAM-1, CEACAM-6, ICAM-1 and PAFR in response to specific stimuli. We explore how upregulated receptors, in turn, expose the host to a range of bacterial infections in the respiratory tract. It is apparent that exploitation of receptor induction for bacterial adherence is not unique to one body system, but is also observed in the central nervous, gastrointestinal and urogenital systems. Prokaryotic pathogens which utilize this mechanism for their infectivity include Streptococcus pneumoniae, Haemophilus influenzae, Neisseria meningitidis and Escherichia coli. A number of approaches have been used, in both in vitro and in vivo experimental models, to inhibit bacterial attachment to temporally expressed host receptors. Some of these novel strategies may advance future targeted interventions for the prevention and treatment of bacterial disease.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000434
2017-04-06
2019-09-24
Loading full text...

Full text loading...

/deliver/fulltext/micro/163/4/421.html?itemId=/content/journal/micro/10.1099/mic.0.000434&mimeType=html&fmt=ahah

References

  1. Kagnoff MF, Eckmann L. Epithelial cells as sensors for microbial infection. J Clin Invest 1997;100:6–10 [CrossRef][PubMed]
    [Google Scholar]
  2. Ribet D, Cossart P. How bacterial pathogens colonize their hosts and invade deeper tissues. Microbes Infect 2015;17:173–183 [CrossRef][PubMed]
    [Google Scholar]
  3. Singh B, Fleury C, Jalalvand F, Riesbeck K. Human pathogens utilize host extracellular matrix proteins laminin and collagen for adhesion and invasion of the host. FEMS Microbiol Rev 2012;36:1122–1180 [CrossRef][PubMed]
    [Google Scholar]
  4. Hauck CR. Cell adhesion receptors—signaling capacity and exploitation by bacterial pathogens. Med Microbiol Immunol 2002;191:55–62 [CrossRef][PubMed]
    [Google Scholar]
  5. Shukla SD, Sohal SS, O'Toole RF, Eapen MS, Walters EH. Platelet activating factor receptor: gateway for bacterial chronic airway infection in chronic obstructive pulmonary disease and potential therapeutic target. Expert Rev Respir Med 2015;9:473–485 [CrossRef][PubMed]
    [Google Scholar]
  6. Chagnot C, Listrat A, Astruc T, Desvaux M. Bacterial adhesion to animal tissues: protein determinants for recognition of extracellular matrix components. Cell Microbiol 2012;14:1687–1696 [CrossRef][PubMed]
    [Google Scholar]
  7. Su YC, Mukherjee O, Singh B, Hallgren O, Westergren-Thorsson G et al. Haemophilus influenzae P4 interacts with extracellular matrix proteins promoting adhesion and serum resistance. J Infect Dis 2016;213:314–323 [CrossRef][PubMed]
    [Google Scholar]
  8. Eberhard T, Virkola R, Korhonen T, Kronvall G, Ullberg M. Binding to human extracellular matrix by Neisseria meningitidis. Infect Immun 1998;66:1791–1794[PubMed]
    [Google Scholar]
  9. Li N, Ren A, Wang X, Fan X, Zhao Y et al. Influenza viral neuraminidase primes bacterial coinfection through TGF-β-mediated expression of host cell receptors. Proc Natl Acad Sci USA 2015;112:238–243 [CrossRef][PubMed]
    [Google Scholar]
  10. Pracht D, Elm C, Gerber J, Bergmann S, Rohde M et al. PavA of Streptococcus pneumoniae modulates adherence, invasion, and meningeal inflammation. Infect Immun 2005;73:2680–2689 [CrossRef][PubMed]
    [Google Scholar]
  11. Neurath M. Expression of tenascin, laminin and fibronectin following traumatic rupture of the anterior cruciate ligament. Z Orthop Ihre Grenzgeb 1993;131:168–172 [CrossRef][PubMed]
    [Google Scholar]
  12. Grigg J, Walters H, Sohal SS, Wood-Baker R, Reid DW et al. Cigarette smoke and platelet-activating factor receptor dependent adhesion of Streptococcus pneumoniae to lower airway cells. Thorax 2012;67:908–913 [CrossRef][PubMed]
    [Google Scholar]
  13. Barczyk M, Carracedo S, Gullberg D. Integrins. Cell Tissue Res 2010;339:269–280 [CrossRef][PubMed]
    [Google Scholar]
  14. Plow EF, Haas TA, Zhang L, Loftus J, Smith JW. Ligand binding to integrins. J Biol Chem 2000;275:21785–21788 [CrossRef][PubMed]
    [Google Scholar]
  15. Kuespert K, Pils S, Hauck CR. CEACAMs: their role in physiology and pathophysiology. Curr Opin Cell Biol 2006;18:565–571 [CrossRef][PubMed]
    [Google Scholar]
  16. Beauchemin N, Draber P, Dveksler G, Gold P, Gray-Owen S et al. Redefined nomenclature for members of the carcinoembryonic antigen family. Exp Cell Res 1999;252:243–249[PubMed][CrossRef]
    [Google Scholar]
  17. Staunton DE, Marlin SD, Stratowa C, Dustin ML, Springer TA. Primary structure of ICAM-1 demonstrates interaction between members of the immunoglobulin and integrin supergene families. Cell 1988;52:925–933[PubMed][CrossRef]
    [Google Scholar]
  18. Tosi MF, Stark JM, Smith CW, Hamedani A, Gruenert DC et al. Induction of ICAM-1 expression on human airway epithelial cells by inflammatory cytokines: effects on neutrophil-epithelial cell adhesion. Am J Respir Cell Mol Biol 1992;7:214–221 [CrossRef][PubMed]
    [Google Scholar]
  19. Frick AG, Joseph TD, Pang L, Rabe AM, St Geme JW et al. Haemophilus influenzae stimulates ICAM-1 expression on respiratory epithelial cells. J Immunol 2000;164:4185–4196[PubMed][CrossRef]
    [Google Scholar]
  20. Huang GT, Eckmann L, Savidge TC, Kagnoff MF. Infection of human intestinal epithelial cells with invasive bacteria upregulates apical intercellular adhesion molecule-1 (ICAM)-1) expression and neutrophil adhesion. J Clin Invest 1996;98:572–583 [CrossRef][PubMed]
    [Google Scholar]
  21. Chan RD, Greenstein SM, Sablay L, Alfonso F, Tellis V et al. Analysis of adhesion molecule expression by tubular epithelial cells using urine immunocytology. Acta Cytol 1995;39:435–442[PubMed]
    [Google Scholar]
  22. Shukla SD, Mahmood MQ, Weston S, Latham R, Muller HK et al. The main rhinovirus respiratory tract adhesion site (ICAM-1) is upregulated in smokers and patients with chronic airflow limitation (CAL). Respir Res 2017;18: [CrossRef][PubMed]
    [Google Scholar]
  23. Albelda SM, Smith CW, Ward PA. Adhesion molecules and inflammatory injury. FASEB J 1994;8:504–512[PubMed]
    [Google Scholar]
  24. Sumagin R, Robin AZ, Nusrat A, Parkos CA. Transmigrated neutrophils in the intestinal lumen engage ICAM-1 to regulate the epithelial barrier and neutrophil recruitment. Mucosal Immunol 2014;7:905–915 [CrossRef][PubMed]
    [Google Scholar]
  25. Ishii S, Nagase T, Shimizu T. Platelet-activating factor receptor. Prostaglandins Other Lipid Mediat 2002;68–69:599–609[CrossRef]
    [Google Scholar]
  26. Keely S, Glover LE, Weissmueller T, Macmanus CF, Fillon S et al. Hypoxia-inducible factor-dependent regulation of platelet-activating factor receptor as a route for Gram-positive bacterial translocation across epithelia. Mol Biol Cell 2010;21:538–546 [CrossRef][PubMed]
    [Google Scholar]
  27. Grigg J. The platelet activating factor receptor: a new anti-infective target in respiratory disease?. Thorax 2012;67:840–841 [CrossRef][PubMed]
    [Google Scholar]
  28. Ferkol T, Schraufnagel D. The global burden of respiratory disease. Ann Am Thorac Soc 2014;11:404–406 [CrossRef][PubMed]
    [Google Scholar]
  29. Brouwer MC, Tunkel AR, van de Beek D. Epidemiology, diagnosis, and antimicrobial treatment of acute bacterial meningitis. Clin Microbiol Rev 2010;23:467–492 [CrossRef][PubMed]
    [Google Scholar]
  30. Murphy TF, Parameswaran GI. Moraxella catarrhalis, a human respiratory tract pathogen. Clin Infect Dis 2009;49:124–131 [CrossRef][PubMed]
    [Google Scholar]
  31. van Eldere J, Slack MP, Ladhani S, Cripps AW. Non-typeable Haemophilus influenzae, an under-recognised pathogen. Lancet Infect Dis 2014;14:1281–1292 [CrossRef][PubMed]
    [Google Scholar]
  32. Kadioglu A, Weiser JN, Paton JC, Andrew PW. The role of Streptococcus pneumoniae virulence factors in host respiratory colonization and disease. Nat Rev Microbiol 2008;6:288–301 [CrossRef][PubMed]
    [Google Scholar]
  33. Hauck CR, Agerer F, Muenzner P, Schmitter T. Cellular adhesion molecules as targets for bacterial infection. Eur J Cell Biol 2006;85:235–242 [CrossRef][PubMed]
    [Google Scholar]
  34. Doran KS, Fulde M, Gratz N, Kim BJ, Nau R et al. Host-pathogen interactions in bacterial meningitis. Acta Neuropathol 2016;131:185–209 [CrossRef][PubMed]
    [Google Scholar]
  35. Yamaguchi M, Terao Y, Mori Y, Hamada S, Kawabata S. PfbA, a novel plasmin- and fibronectin-binding protein of Streptococcus pneumoniae, contributes to fibronectin-dependent adhesion and antiphagocytosis. J Biol Chem 2008;283:36272–36279 [CrossRef][PubMed]
    [Google Scholar]
  36. Agarwal V, Kuchipudi A, Fulde M, Riesbeck K, Bergmann S et al. Streptococcus pneumoniae endopeptidase O (PepO) is a multifunctional plasminogen- and fibronectin-binding protein, facilitating evasion of innate immunity and invasion of host cells. J Biol Chem 2013;288:6849–6863 [CrossRef][PubMed]
    [Google Scholar]
  37. Fink DL, Green BA, St Geme JW. The Haemophilus influenzae Hap autotransporter binds to fibronectin, laminin, and collagen IV. Infect Immun 2002;70:4902–4907[PubMed][CrossRef]
    [Google Scholar]
  38. Tchoupa AK, Lichtenegger S, Reidl J, Hauck CR. Outer membrane protein P1 is the CEACAM-binding adhesin of Haemophilus influenzae. Mol Microbiol 2015;98:440–455 [CrossRef][PubMed]
    [Google Scholar]
  39. Hill DJ, Virji M. A novel cell-binding mechanism of Moraxella catarrhalis ubiquitous surface protein UspA: specific targeting of the N-domain of carcinoembryonic antigen-related cell adhesion molecules by UspA1. Mol Microbiol 2003;48:117–129[PubMed][CrossRef]
    [Google Scholar]
  40. Klaile E, Klassert TE, Scheffrahn I, Müller MM, Heinrich A et al. Carcinoembryonic antigen (CEA)-related cell adhesion molecules are co-expressed in the human lung and their expression can be modulated in bronchial epithelial cells by non-typable Haemophilus influenzae, Moraxella catarrhalis, TLR3, and type I and II interferons. Respir Res 2013;14:85 [CrossRef][PubMed]
    [Google Scholar]
  41. Swords WE, Buscher BA, ver Steeg Ii K, Preston A, Nichols WA et al. Non-typeable Haemophilus influenzae adhere to and invade human bronchial epithelial cells via an interaction of lipooligosaccharide with the PAF receptor. Mol Microbiol 2000;37:13–27[PubMed][CrossRef]
    [Google Scholar]
  42. Barbier M, Oliver A, Rao J, Hanna SL, Goldberg JB et al. Novel phosphorylcholine-containing protein of Pseudomonas aeruginosa chronic infection isolates interacts with airway epithelial cells. J Infect Dis 2008;197:465–473 [CrossRef][PubMed]
    [Google Scholar]
  43. Mushtaq N, Ezzati M, Hall L, Dickson I, Kirwan M et al. Adhesion of Streptococcus pneumoniae to human airway epithelial cells exposed to urban particulate matter. J Allergy Clin Immunol 2011;127:1236–1242 [CrossRef][PubMed]
    [Google Scholar]
  44. Shukla SD, Muller HK, Latham R, Sohal SS, Walters EH. Platelet-activating factor receptor (PAFr) is upregulated in small airways and alveoli of smokers and COPD patients. Respirology 2016;21:504–510 [CrossRef][PubMed]
    [Google Scholar]
  45. Shukla SD, Sohal SS, Mahmood MQ, Reid D, Muller HK et al. Airway epithelial platelet-activating factor receptor expression is markedly upregulated in chronic obstructive pulmonary disease. Int J Chron Obstruct Pulmon Dis 2014;9:853–861 [CrossRef][PubMed]
    [Google Scholar]
  46. Shukla SD, Fairbairn RL, Gell DA, Latham RD, Sohal SS et al. An antagonist of the platelet-activating factor receptor inhibits adherence of both nontypeable Haemophilus influenzae and Streptococcus pneumoniae to cultured human bronchial epithelial cells exposed to cigarette smoke. Int J Chron Obstruct Pulmon Dis 2016;11:1647–1655 [CrossRef][PubMed]
    [Google Scholar]
  47. Poussin C, Laurent A, Peitsch MC, Hoeng J, de Leon H. Systems biology reveals cigarette smoke-induced concentration-dependent direct and indirect mechanisms that promote monocyte-endothelial cell adhesion. Toxicol Sci 2015;147:370–385 [CrossRef][PubMed]
    [Google Scholar]
  48. Greve JM, Davis G, Meyer AM, Forte CP, Yost SC et al. The major human rhinovirus receptor is ICAM-1. Cell 1989;56:839–847[PubMed][CrossRef]
    [Google Scholar]
  49. Papi A, Johnston SL. Rhinovirus infection induces expression of its own receptor intercellular adhesion molecule 1 (ICAM-1) via increased NF-κB-mediated transcription. J Biol Chem 1999;274:9707–9720[PubMed][CrossRef]
    [Google Scholar]
  50. Staunton DE, Merluzzi VJ, Rothlein R, Barton R, Marlin SD et al. A cell adhesion molecule, ICAM-1, is the major surface receptor for rhinoviruses. Cell 1989;56:849–853[PubMed][CrossRef]
    [Google Scholar]
  51. Ledford RM, Patel NR, Demenczuk TM, Watanyar A, Herbertz T et al. VP1 sequencing of all human rhinovirus serotypes: insights into genus phylogeny and susceptibility to antiviral capsid-binding compounds. J Virol 2004;78:3663–3674[PubMed][CrossRef]
    [Google Scholar]
  52. Avadhanula V, Rodriguez CA, Ulett GC, Bakaletz LO, Adderson EE. Nontypeable Haemophilus influenzae adheres to intercellular adhesion molecule 1 (ICAM-1) on respiratory epithelial cells and upregulates ICAM-1 expression. Infect Immun 2006;74:830–838 [CrossRef][PubMed]
    [Google Scholar]
  53. Gulraiz F, Bellinghausen C, Bruggeman CA, Stassen FR. Haemophilus influenzae increases the susceptibility and inflammatory response of airway epithelial cells to viral infections. FASEB J 2015;29:849–858 [CrossRef][PubMed]
    [Google Scholar]
  54. Zandvoort A, van der Geld YM, Jonker MR, Noordhoek JA, Vos JT et al. High ICAM-1 gene expression in pulmonary fibroblasts of COPD patients: a reflection of an enhanced immunological function. Eur Respir J 2006;28:113–122 [CrossRef][PubMed]
    [Google Scholar]
  55. Chan SC, Shum DK, Tipoe GL, Mak JC, Leung ET et al. Upregulation of ICAM-1 expression in bronchial epithelial cells by airway secretions in bronchiectasis. Respir Med 2008;102:287–298 [CrossRef][PubMed]
    [Google Scholar]
  56. Bosch AA, Biesbroek G, Trzcinski K, Sanders EA, Bogaert D. Viral and bacterial interactions in the upper respiratory tract. PLoS Pathog 2013;9:e1003057 [CrossRef][PubMed]
    [Google Scholar]
  57. Avadhanula V, Rodriguez CA, Devincenzo JP, Wang Y, Webby RJ et al. Respiratory viruses augment the adhesion of bacterial pathogens to respiratory epithelium in a viral species- and cell type-dependent manner. J Virol 2006;80:1629–1636 [CrossRef][PubMed]
    [Google Scholar]
  58. Griffiths NJ, Bradley CJ, Heyderman RS, Virji M. IFN-gamma amplifies NFkappaB-dependent Neisseria meningitidis invasion of epithelial cells via specific upregulation of CEA-related cell adhesion molecule 1. Cell Microbiol 2007;9:2968–2983 [CrossRef][PubMed]
    [Google Scholar]
  59. Chen CJ, Lin TT, Shively JE. Role of interferon regulatory factor-1 in the induction of biliary glycoprotein (cell CAM-1) by interferon-gamma. J Biol Chem 1996;271:28181–28188[PubMed][CrossRef]
    [Google Scholar]
  60. Jafri RZ, Ali A, Messonnier NE, Tevi-Benissan C, Durrheim D et al. Global epidemiology of invasive meningococcal disease. Popul Health Metr 2013;11:17 [CrossRef][PubMed]
    [Google Scholar]
  61. O'Brien KL, Wolfson LJ, Watt JP, Henkle E, Deloria-Knoll M et al. Burden of disease caused by Streptococcus pneumoniae in children younger than 5 years: global estimates. Lancet 2009;374:893–902 [CrossRef][PubMed]
    [Google Scholar]
  62. Iovino F, Molema G, Bijlsma JJ. Platelet endothelial cell adhesion molecule-1, a putative receptor for the adhesion of Streptococcus pneumoniae to the vascular endothelium of the blood–brain barrier. Infect Immun 2014;82:3555–3566 [CrossRef][PubMed]
    [Google Scholar]
  63. Iovino F, Molema G, Bijlsma JJ. Streptococcus pneumoniae interacts with pIgR expressed by the brain microvascular endothelium but does not co-localize with PAF receptor. PLoS One 2014;9:e97914 [CrossRef][PubMed]
    [Google Scholar]
  64. Iovino F, Brouwer MC, van de Beek D, Molema G, Bijlsma JJ. Signalling or binding: the role of the platelet-activating factor receptor in invasive pneumococcal disease. Cell Microbiol 2013;15:870–881 [CrossRef][PubMed]
    [Google Scholar]
  65. Shukla SD. Platelet-activating factor receptor and signal transduction mechanisms. FASEB J 1992;6:2296–2301[PubMed]
    [Google Scholar]
  66. Iovino F, Seinen J, Henriques-Normark B, van Dijl JM. How does Streptococcus pneumoniae invade the brain?. Trends Microbiol 2016;24:307–315 [CrossRef][PubMed]
    [Google Scholar]
  67. Iovino F, Hammarlöf DL, Garriss G, Brovall S, Nannapaneni P et al. Pneumococcal meningitis is promoted by single cocci expressing pilus adhesin RrgA. J Clin Invest 2016;126:2821–2826 [CrossRef][PubMed]
    [Google Scholar]
  68. Nelson AL, Ries J, Bagnoli F, Dahlberg S, Fälker S et al. RrgA is a pilus-associated adhesin in Streptococcus pneumoniae. Mol Microbiol 2007;66:329–340 [CrossRef][PubMed]
    [Google Scholar]
  69. Bagnoli F, Moschioni M, Donati C, Dimitrovska V, Ferlenghi I et al. A second pilus type in Streptococcus pneumoniae is prevalent in emerging serotypes and mediates adhesion to host cells. J Bacteriol 2008;190:5480–5492 [CrossRef][PubMed]
    [Google Scholar]
  70. Unkmeir A, Latsch K, Dietrich G, Wintermeyer E, Schinke B et al. Fibronectin mediates Opc-dependent internalization of Neisseria meningitidis in human brain microvascular endothelial cells. Mol Microbiol 2002;46:933–946[PubMed][CrossRef]
    [Google Scholar]
  71. Martin JN, Ball LM, Solomon TL, Dewald AH, Criss AK et al. Neisserial Opa protein-CEACAM interactions: competition for receptors as a means of bacterial invasion and pathogenesis. Biochemistry 2016;55:4286–4294 [CrossRef][PubMed]
    [Google Scholar]
  72. Muenzner P, Naumann M, Meyer TF, Gray-Owen SD. Pathogenic Neisseria trigger expression of their carcinoembryonic antigen-related cellular adhesion molecule 1 (CEACAM1; previously CD66a) receptor on primary endothelial cells by activating the immediate early response transcription factor, nuclear factor-κB. J Biol Chem 2001;276:24331–24340 [CrossRef][PubMed]
    [Google Scholar]
  73. Virji M. Pathogenic neisseriae: surface modulation, pathogenesis and infection control. Nat Rev Microbiol 2009;7:274–286 [CrossRef][PubMed]
    [Google Scholar]
  74. Milner R, Hung S, Erokwu B, Dore-Duffy P, Lamanna JC et al. Increased expression of fibronectin and the α5β1 integrin in angiogenic cerebral blood vessels of mice subject to hypobaric hypoxia. Mol Cell Neurosci 2008;38:43–52 [CrossRef][PubMed]
    [Google Scholar]
  75. Bernard SC, Simpson N, Join-Lambert O, Federici C, Laran-Chich MP et al. Pathogenic Neisseria meningitidis utilizes CD147 for vascular colonization. Nat Med 2014;20:725–731 [CrossRef][PubMed]
    [Google Scholar]
  76. Ke X, Fei F, Chen Y, Xu L, Zhang Z et al. Hypoxia upregulates CD147 through a combined effect of HIF-1α and Sp1 to promote glycolysis and tumor progression in epithelial solid tumors. Carcinogenesis 2012;33:1598–1607 [CrossRef][PubMed]
    [Google Scholar]
  77. Liu L, Johnson HL, Cousens S, Perin J, Scott S et al. Global, regional, and national causes of child mortality: an updated systematic analysis for 2010 with time trends since 2000. Lancet 2012;379:2151–2161 [CrossRef][PubMed]
    [Google Scholar]
  78. Leusch HG, Drzeniek Z, Markos-Pusztai Z, Wagener C. Binding of Escherichia coli and Salmonella strains to members of the carcinoembryonic antigen family: differential binding inhibition by aromatic alpha-glycosides of mannose. Infect Immun 1991;59:2051–2057[PubMed]
    [Google Scholar]
  79. Berger CN, Billker O, Meyer TF, Servin AL, Kansau I. Differential recognition of members of the carcinoembryonic antigen family by Afa/Dr adhesins of diffusely adhering Escherichia coli (Afa/Dr DAEC). Mol Microbiol 2004;52:963–983 [CrossRef][PubMed]
    [Google Scholar]
  80. Ou G, Baranov V, Lundmark E, Hammarström S, Hammarström ML. Contribution of intestinal epithelial cells to innate immunity of the human gut–studies on polarized monolayers of colon carcinoma cells. Scand J Immunol 2009;69:150–161 [CrossRef][PubMed]
    [Google Scholar]
  81. Barnich N, Carvalho FA, Glasser AL, Darcha C, Jantscheff P et al. CEACAM6 acts as a receptor for adherent-invasive E. coli, supporting ileal mucosa colonization in Crohn disease. J Clin Invest 2007;117:1566–1574 [CrossRef][PubMed]
    [Google Scholar]
  82. Rolhion N, Barnich N, Bringer MA, Glasser AL, Ranc J et al. Abnormally expressed ER stress response chaperone Gp96 in CD favours adherent-invasive Escherichia coli invasion. Gut 2010;59:1355–1362 [CrossRef][PubMed]
    [Google Scholar]
  83. Zhang XL, Tsui IS, Yip CM, Fung AW, Wong DK et al. Salmonella enterica serovar Typhi uses type IVB pili to enter human intestinal epithelial cells. Infect Immun 2000;68:3067–3073[PubMed][CrossRef]
    [Google Scholar]
  84. Xicohtencatl-Cortes J, Monteiro-Neto V, Ledesma MA, Jordan DM, Francetic O et al. Intestinal adherence associated with type IV pili of enterohemorrhagic Escherichia coli O157:H7. J Clin Invest 2007;117:3519–3529 [CrossRef][PubMed]
    [Google Scholar]
  85. Tsui IS, Yip CM, Hackett J, Morris C. The type IVB pili of Salmonella enterica serovar Typhi bind to the cystic fibrosis transmembrane conductance regulator. Infect Immun 2003;71:6049–6050[PubMed][CrossRef]
    [Google Scholar]
  86. Lohi H, Mäkelä S, Pulkkinen K, Höglund P, Karjalainen-Lindsberg ML et al. Upregulation of CFTR expression but not SLC26A3 and SLC9A3 in ulcerative colitis. Am J Physiol Gastrointest Liver Physiol 2002;283:G567–575 [CrossRef][PubMed]
    [Google Scholar]
  87. Xicohtencatl-Cortes J, Monteiro-Neto V, Saldaña Z, Ledesma MA, Puente JL et al. The type 4 pili of enterohemorrhagic Escherichia coli O157:H7 are multipurpose structures with pathogenic attributes. J Bacteriol 2009;191:411–421 [CrossRef][PubMed]
    [Google Scholar]
  88. Farfan MJ, Cantero L, Vidal R, Botkin DJ, Torres AG. Long polar fimbriae of enterohemorrhagic Escherichia coli O157:H7 bind to extracellular matrix proteins. Infect Immun 2011;79:3744–3750 [CrossRef][PubMed]
    [Google Scholar]
  89. Kolachala VL, Bajaj R, Wang L, Yan Y, Ritzenthaler JD et al. Epithelial-derived fibronectin expression, signaling, and function in intestinal inflammation. J Biol Chem 2007;282:32965–32973 [CrossRef][PubMed]
    [Google Scholar]
  90. Harding GK, Ronald AR. The management of urinary infections: what have we learned in the past decade?. Int J Antimicrob Agents 1994;4:83–88[PubMed][CrossRef]
    [Google Scholar]
  91. Hooton TM. Clinical practice. uncomplicated urinary tract infection. N Engl J Med 2012;366:1028–1037 [CrossRef][PubMed]
    [Google Scholar]
  92. Nicolle LE. Complicated urinary tract infection in adults. Can J Infect Dis Med Microbiol 2005;16:349–360[PubMed]
    [Google Scholar]
  93. Wright KJ, Hultgren SJ. Sticky fibers and uropathogenesis: bacterial adhesins in the urinary tract. Future Microbiol 2006;1:75–87 [CrossRef][PubMed]
    [Google Scholar]
  94. Flores-Mireles AL, Walker JN, Caparon M, Hultgren SJ. Urinary tract infections: epidemiology, mechanisms of infection and treatment options. Nat Rev Microbiol 2015;13:269–284 [CrossRef][PubMed]
    [Google Scholar]
  95. Olsburgh J, Harnden P, Weeks R, Smith B, Joyce A et al. Uroplakin gene expression in normal human tissues and locally advanced bladder cancer. J Pathol 2003;199:41–49 [CrossRef][PubMed]
    [Google Scholar]
  96. Selvarangan R, Goluszko P, Singhal J, Carnoy C, Moseley S et al. Interaction of Dr adhesin with collagen type IV is a critical step in Escherichia coli renal persistence. Infect Immun 2004;72:4827–4835 [CrossRef][PubMed]
    [Google Scholar]
  97. Muenzner P, Kengmo Tchoupa A, Klauser B, Brunner T, Putze J et al. Uropathogenic E. coli exploit CEA to promote colonization of the urogenital tract mucosa. PLoS Pathog 2016;12:e1005608 [CrossRef][PubMed]
    [Google Scholar]
  98. Holmes CH, Simpson KL, Wainwright SD, Tate CG, Houlihan JM et al. Preferential expression of the complement regulatory protein decay accelerating factor at the fetomaternal interface during human pregnancy. J Immunol 1990;144:3099–3105[PubMed]
    [Google Scholar]
  99. Selvarangan R, Goluszko P, Popov V, Singhal J, Pham T et al. Role of decay-accelerating factor domains and anchorage in internalization of Dr-fimbriated Escherichia coli. Infect Immun 2000;68:1391–1399[PubMed][CrossRef]
    [Google Scholar]
  100. Ventola CL. The antibiotic resistance crisis: part 1: causes and threats. P T 2015;40:277–283[PubMed]
    [Google Scholar]
  101. Cegelski L, Pinkner JS, Hammer ND, Cusumano CK, Hung CS et al. Small-molecule inhibitors target Escherichia coli amyloid biogenesis and biofilm formation. Nat Chem Biol 2009;5:913–919 [CrossRef][PubMed]
    [Google Scholar]
  102. Greene SE, Pinkner JS, Chorell E, Dodson KW, Shaffer CL et al. Pilicide ec240 disrupts virulence circuits in uropathogenic Escherichia coli. MBio 2014;5:e02038 [CrossRef][PubMed]
    [Google Scholar]
  103. Wessler S, Muenzner P, Meyer TF, Naumann M. The anti-inflammatory compound curcumin inhibits Neisseria gonorrhoeae-induced NF-κB signaling, release of pro-inflammatory cytokines/chemokines and attenuates adhesion in late infection. Biol Chem 2005;386:481–490 [CrossRef][PubMed]
    [Google Scholar]
  104. Foryst-Ludwig A, Neumann M, Schneider-Brachert W, Naumann M. Curcumin blocks NF-κB and the motogenic response in Helicobacter pylori-infected epithelial cells. Biochem Biophys Res Commun 2004;316:1065–1072 [CrossRef][PubMed]
    [Google Scholar]
  105. Firon N, Ashkenazi S, Mirelman D, Ofek I, Sharon N. Aromatic alpha-glycosides of mannose are powerful inhibitors of the adherence of type 1 fimbriated Escherichia coli to yeast and intestinal epithelial cells. Infect Immun 1987;55:472–476[PubMed]
    [Google Scholar]
  106. Cusumano CK, Pinkner JS, Han Z, Greene SE, Ford BA et al. Treatment and prevention of urinary tract infection with orally active FimH inhibitors. Sci Transl Med 2011;3:109ra115 [CrossRef][PubMed]
    [Google Scholar]
  107. Virji M, Evans D, Griffith J, Hill D, Serino L et al. Carcinoembryonic antigens are targeted by diverse strains of typable and non-typable Haemophilus influenzae. Mol Microbiol 2000;36:784–795[PubMed][CrossRef]
    [Google Scholar]
  108. Bookwalter JE, Jurcisek JA, Gray-Owen SD, Fernandez S, Mcgillivary G et al. A carcinoembryonic antigen-related cell adhesion molecule 1 homologue plays a pivotal role in nontypeable Haemophilus influenzae colonization of the chinchilla nasopharynx via the outer membrane protein P5-homologous adhesin. Infect Immun 2008;76:48–55 [CrossRef][PubMed]
    [Google Scholar]
  109. Hergott CB, Roche AM, Naidu NA, Mesaros C, Blair IA et al. Bacterial exploitation of phosphorylcholine mimicry suppresses inflammation to promote airway infection. J Clin Invest 2015;125:3878–3890 [CrossRef][PubMed]
    [Google Scholar]
  110. Negro Alvarez JM, Miralles López JC, Ortiz Martínez JL, Abellán Alemán A, Rubio del Barrio R. Platelet-activating factor antagonists. Allergol Immunopathol 1997;25:249–258[PubMed]
    [Google Scholar]
  111. Mallet de Lima CD, da Conceição Costa J, De Oliveira Lima Santos SA, Carvalho S, De Carvalho L et al. Central role of PAFR signalling in ExoU-induced NF-κB activation. Cell Microbiol 2014;16:1244–1254 [CrossRef][PubMed]
    [Google Scholar]
  112. Suri R, Periselneris J, Lanone S, Zeidler-Erdely PC, Melton G et al. Exposure to welding fumes and lower airway infection with Streptococcus pneumoniae. J Allergy Clin Immunol 2016;137:527–534 [CrossRef][PubMed]
    [Google Scholar]
  113. Miller ML, Gao G, Pestina T, Persons D, Tuomanen E. Hypersusceptibility to invasive pneumococcal infection in experimental sickle cell disease involves platelet-activating factor receptor. J Infect Dis 2007;195:581–584 [CrossRef][PubMed]
    [Google Scholar]
  114. Gómez FP, Roca J, Barberà JA, Chung KF, Peinado VI et al. Effect of a platelet-activating factor (PAF) antagonist, SR 27417A, on PAF-induced gas exchange abnormalities in mild asthma. Eur Respir J 1998;11:835–839[PubMed][CrossRef]
    [Google Scholar]
  115. Arnout J, van Hecken A, de Lepeleire I, Miyamoto Y, Holmes I et al. Effectiveness and tolerability of CV-3988, a selective PAF antagonist, after intravenous administration to man. Br J Clin Pharmacol 1988;25:445–451[PubMed][CrossRef]
    [Google Scholar]
  116. Hsieh KH. Effects of PAF antagonist, BN52021, on the PAF-, methacholine-, and allergen-induced bronchoconstriction in asthmatic children. Chest 1991;99:877–882[PubMed][CrossRef]
    [Google Scholar]
  117. Hartung T, Daston G. Are in vitro tests suitable for regulatory use?. Toxicol Sci 2009;111:233–237 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000434
Loading
/content/journal/micro/10.1099/mic.0.000434
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error