Campylobacter jejuni increases flagellar expression and adhesion of noninvasive Escherichia coli: Effects on enterocytic toll-like receptor 4 and CXCL-8 expression

Infection and Immunity

Volumn 83, Issue 12, 2015, Pages 4571-4581

  Reti, Kristen L ^a   Tymensen, Lisa D ^b   Davis, Shevaun P ^a   Amrein, Matthias W ^a   Buret, Andre G ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b ALBERTA AGRICULTURE AND RURAL DEVELOPMENT   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 8; TOLL LIKE RECEPTOR 4; CONDITIONED MEDIUM; IL8 PROTEIN, HUMAN; TLR4 PROTEIN, HUMAN;

ARTICLE; ATOMIC FORCE MICROSCOPY; BACTERIAL FLAGELLUM; BACTERIAL GENE; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; CAMPYLOBACTER JEJUNI; COLON; CONTROLLED STUDY; ESCHERICHIA COLI; EXPOSURE; GENE EXPRESSION; HUMAN; HUMAN CELL; INFLAMMATION; INTESTINE CELL; MICROARRAY ANALYSIS; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; TRANSMISSION ELECTRON MICROSCOPY; AGONISTS; ANTAGONISTS AND INHIBITORS; CELL LINE; CONDITIONED MEDIUM; DRUG EFFECTS; FLAGELLUM; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HOST PATHOGEN INTERACTION; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PHARMACOLOGY; SIGNAL TRANSDUCTION; SYMBIOSIS; VIRULENCE;

CAMPYLOBACTER JEJUNI; CELL LINE; CULTURE MEDIA, CONDITIONED; ENTEROCYTES; ESCHERICHIA COLI; FLAGELLA; GENE EXPRESSION REGULATION; HOST-PATHOGEN INTERACTIONS; HUMANS; INTERLEUKIN-8; SIGNAL TRANSDUCTION; SYMBIOSIS; TOLL-LIKE RECEPTOR 4; VIRULENCE;

EID: 84949650095     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00970-15     Document Type: Article

References (88)

1. World Health Organization. 2013. The global view of campylobacteriosis: report of an expert consultation. World Health Organization, Utrecht, Netherlands.
2. Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson M-A, Roy SL, Jones JL, Griffin PM. 2011. Foodborne illness acquired in the United States-major pathogens. Emerg Infect Dis 17:7-15. http://dx.doi.org/10.3201/eid1701.P11101.
3. Scharff RL. 2012. Economic burden from health losses due to foodborne illness in the United States. J Food Prot 75:123-131. http://dx.doi.org/10.4315/0362-028X.JFP-11-058.
4. Acheson D, Allos BM. 2001. Campylobacter jejuni infections: update on emerging issues and trends. Clin Infect Dis 32:1201-1206. http://dx.doi.org/10.1086/319760.
5. Humphrey T, O'Brien S, Madsen M. 2007. Campylobacters as zoonotic pathogens: a food production perspective. Int J Food Microbiol 117:237-257. http://dx.doi.org/10.1016/j.ijfoodmicro.2007.01.006.
6. Black RE, Levine MM, Clements ML, Hughes TP, Blaser MJ. 1988. Experimental Campylobacter jejuni infection in humans. J Infect Dis 157: 472-479 http://dx.doi.org/10.1093/infdis/157.3.472.
7. Blaser MJ, Berkowitz ID, LaForce FM, Cravens J, Reller LB, Wang W-LL. 1979. Campylobacter enteritis: clinical and epidemiologic features. Ann Intern Med 91:179-185. http://dx.doi.org/10.7326/0003-4819-91-2-179.
8. Garcia Rodriguez L, Ruigomez A, Panes J. 2006. Acute gastroenteritis is followed by an increased risk of inflammatory bowel disease. Gastroenterology 130:1588-1594. http://dx.doi.org/10.1053/j.gastro.2006.02.004.
9. Gradel KO, Nielsen HL, Schønheyder HC, Ejlertsen T, Kristensen B, Nielsen H. 2009. Increased short-and long-term risk of inflammatory bowel disease after Salmonella or Campylobacter gastroenteritis. Gastroenterology 137:495-501. http://dx.doi.org/10.1053/j.gastro.2009.04.001.
10. Hannu T, Mattila L, Rautelin H, Pelkonen P, Lahdenne P, Siitonen A, Leirisalo-Repo M. 2002. Campylobacter-triggered reactive arthritis: a population-based study. Rheumatology 41:312-318. http://dx.doi.org/10.1093/rheumatology/41.3.312.
11. Marshall J, Thabane M, Garg A, Clark W, Salvadori M, Collins S. 2006. Incidence and epidemiology of irritable bowel syndrome after a large waterborne outbreak of bacterial dysentery. Gastroenterology 131:445-450. http://dx.doi.org/10.1053/j.gastro.2006.05.053.
12. Rees JH, Soudain SE, Gregson NA, Hughes RAC. 1995. Campylobacter jejuni infection and Guillain-Barré syndrome. N Engl J Med 333:1374-1379. http://dx.doi.org/10.1056/NEJM199511233332102.
13. Rhodes KM, Tattersfield AE. 1982. Guillain-Barre syndrome associated with Campylobacter infection. Br Med J 285:173-174. http://dx.doi.org/10.1136/bmj.285.6336.173.
14. Thabane M, Kottachchi DT, Marshall JK. 2007. Systematic review and meta-analysis: the incidence and prognosis of postinfectious irritable bowel syndrome. Aliment Pharmacol Ther 26:535-544. http://dx.doi.org/10.1111/j.1365-2036.2007.03399.x.
15. Thompson WG, Longstreth GF, Drossman DA, Heaton KW, Irvine EJ, Müller-Lissner SA. 1999. Functional bowel disorders and functional abdominal pain. Gut 45:II43-II47. http://dx.doi.org/10.1136/gut.45.2008.ii43.
16. Sartor RB. 2011. Key questions to guide a better understanding of hostcommensal microbiota interactions in intestinal inflammation. Mucosal Immunol 4:127-132. http://dx.doi.org/10.1038/mi.2010.87.
17. Vermeire S, Van Assche G, Rutgeerts P. 2012. Classification of inflammatory bowel disease: the old and the new. Curr Opin Gastroenterol 28: 321-326. http://dx.doi.org/10.1097/MOG.0b013e328354be1e.
18. Fukuba N, Ishihara S, Tada Y, Oshima N, Moriyama I, Yuki T, Kawashima K, Kushiyama Y, Fujishiro H, Kinoshita Y. 2014. Prevalence of irritable bowel syndrome-like symptoms in ulcerative colitis patients with clinical and endoscopic evidence of remission: prospective multicenter study. Scand J Gastroenterol 49:674-680. http://dx.doi.org/10.1007/s00535-013-0829-7.
19. Minderhoud I, Oldenburg B, Wismeijer J, Van Berge Henegouwen G, Smout AJPM. 2004. IBS-like symptoms in patients with inflammatory bowel disease in remission: relationships with quality of life and coping behavior. Dig Dis Sci 49:469-474. http://dx.doi.org/10.1023/B:DDAS.0000020506.84248.f9.
20. Buret AG, Reti K. 2014. Acute enteric infections alter commensal microbiota: new mechanisms in postinfectious intestinal inflammatory disorders, p 87-106. In Heidt PJ, Rusch V, Walker RI, Lange D, Riddle MS (ed), Persisting consequences of intestinal infection. Seminar 27. Old Herborn University, Herborn, Germany.
21. Kalischuk LD, Buret AG. 2009. A role for Campylobacter jejuni-induced enteritis in inflammatory bowel disease? Am J Physiol Gastrointest Liver Physiol 298:G1-G9. http://dx.doi.org/10.1152/ajpgi.00193.2009.
22. Frank DN, St Amand AL, Feldman RA, Boedeker EC, Harpaz N, Pace NR. 2007. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci U S A 104:13780-13785. http://dx.doi.org/10.1073/pnas.0706625104.
23. Jeffery IB, O'Toole PW, Öhman L, Claesson MJ, Deane J, Quigley EMM, Simrén M. 2012. An irritable bowel syndrome subtype defined by species-specific alterations in faecal microbiota. Gut 61:997-1006. http://dx.doi.org/10.1136/gutjnl-2011-301501.
24. Seksik P, Rigottier-Gois L, Gramet G, Sutren M, Pochart P, Marteau P, Jian R, Doré J. 2003. Alterations of the dominant faecal bacterial groups in patients with Crohn's disease of the colon. Gut 52:237-242. http://dx.doi.org/10.1136/gut.52.2.237.
25. Sokol H, Pigneur B, Watterlot L, Lakhdari O, Bermúdez-Humarán LG, Gratadoux J-J, Blugeon S, Bridonneau C, Furet J-P, Corthier G, Grangette C, Vasquez N, Pochart P, Trugnan G, Thomas G, Blottière HM, Doré J, Marteau P, Seksik P, Langella P. 2008. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci U S A 105:16731-16736. http://dx.doi.org/10.1073/pnas.0804812105.
26. Sokol H, Seksik P, Furet JP, Firmesse O, Nion-Larmurier I, Beaugerie L, Cosnes J, Corthier G, Marteau P, Doré J. 2009. Low counts of Faecalibacterium prausnitzii in colitis microbiota. Inflamm Bowel Dis 15: 1183-1189. http://dx.doi.org/10.1002/ibd.20903.
27. Lopez-Siles M, Martinez-Medina M, Busquets D, Sabat-Mir M, Duncan SH, Flint HJ, Aldeguer X, Garcia-Gil LJ. 2014. Mucosa-associated Faecalibacterium prausnitzii and Escherichia coli co-abundance can distinguish irritable bowel syndrome and inflammatory bowel disease phenotypes. Int J Med Microbiol 304:464-475. http://dx.doi.org/10.1016/j.ijmm.2014.02.009.
28. Martinez-Medina M, Aldeguer X, Gonzalez-Huix F, Acero D, Garcia-Gil JL. 2006. Abnormal microbiota composition in the ileocolonic mucosa of Crohn's disease patients as revealed by polymerase chain reactiondenaturing gradient gel electrophoresis. Inflamm Bowel Dis 12:1136-1145. http://dx.doi.org/10.1097/01.mib.0000235828.09305.0c.
29. Shen L, Weber CR, Raleigh DR, Yu D, Turner JR. 2011. Tight junction pore and leak pathways: a dynamic duo. Annu Rev Physiol 73:283-309. http://dx.doi.org/10.1146/annurev-physiol-012110-142150.
30. O'Hara J, Buret A. 2008. Mechanisms of intestinal tight junctional disruption during infection. Front Biosci 1:7008-7021.
31. MacCallum A, Hardy SP, Everest PH. 2005. Campylobacter jejuni inhibits the absorptive transport functions of Caco-2 cells and disrupts cellular tight junctions. Microbiology 151:2451-2458. http://dx.doi.org/10.1099/mic.0.27950-0.
32. Lamb-Rosteski JM, Kalischuk LD, Inglis GD, Buret AG. 2008. Epidermal growth factor inhibits Campylobacter jejuni-induced claudin-4 disruption, loss of epithelial barrier function, and Escherichia coli translocation. Infect Immun 76:3390-3398. http://dx.doi.org/10.1128/IAI.01698-07.
33. Kalischuk L, Inglis GD, Buret A. 2009. Campylobacter jejuni induces transcellular translocation of commensal bacteria via lipid rafts. Gut Pathog 1:2. http://dx.doi.org/10.1186/1757-4749-1-2.
34. Kalischuk L, Leggett F, Inglis GD. 2010. Campylobacter jejuni induces transcytosis of commensal bacteria across the intestinal epithelium through M-like cells. Gut Pathog 2:14. http://dx.doi.org/10.1186/1757-4749-2-14.
35. Kawai T, Akira S. 2010. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol 11:373-384. http://dx.doi.org/10.1038/ni.1863.
36. Medzhitov R. 2007. Recognition of microorganisms and activation of the immune response. Nature 449:819-826. http://dx.doi.org/10.1038/nature06246.
37. Takeuchi O, Akira S. 2010. Pattern recognition receptors and inflammation. Cell 140:805-820. http://dx.doi.org/10.1016/j.cell.2010.01.022.
38. Cario E. 2010. Toll-like receptors in inflammatory bowel diseases: a decade later. Inflamm Bowel Dis 16:1583-1597. http://dx.doi.org/10.1002/ibd.21282.
39. Cario E, Podolsky DK. 2000. Differential alteration in intestinal epithelial cell expression of Toll-like receptor 3 (TLR3) and TLR4 in inflammatory bowel disease. Infect Immun 68:7010-7017. http://dx.doi.org/10.1128/IAI.68.12.7010-7017.2000.
40. Fuse K, Katakura K, Sakamoto N, Ohira H. 2010. Toll-like receptor 9 gene mutations and polymorphisms in Japanese ulcerative colitis patients. World J Gastroenterol 16:5815-5821. http://dx.doi.org/10.3748/wjg.v16.i46.5815.
41. Torok HP, Glas J, Tonenchi L, Bruennler G, Folwaczny M, Folwaczny C. 2004. Crohn's disease is associated with a Toll-like receptor-9 polymorphism. Gastroenterology 127:365-366. http://dx.doi.org/10.1053/j.gastro.2004.05.051.
42. Villani AC, Lemire M, Thabane M, Belisle A, Geneau G, Garg AX, Clark WF, Moayyedi P, Collins SM, Franchimont D, Marshall JK. 2010. Genetic risk factors for post-infectious irritable bowel syndrome following a waterborne outbreak of gastroenteritis. Gastroenterology 138:1502-1513. http://dx.doi.org/10.1053/j.gastro.2009.12.049.
43. Poltorak A, He X, Smirnova I, Liu M-Y, Huffel CV, Du X, Birdwell D, Alejos E, Silva M, Galanos C, Freudenberg M, Ricciardi-Castagnoli P, Layton B, Beutler B. 1998. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4. Gene Sci 282:2085-2088. http://dx.doi.org/10.1126/science.282.5396.2085.
44. Bauer S, Kirschning CJ, Häcker H, Redecke V, Hausmann S, Akira S, Wagner H, Lipford GB. 2001. Human TLR9 confers responsiveness to bacterial DNA via species-specific CpG motif recognition. Proc Natl Acad Sci U S A 98:9237-9242. http://dx.doi.org/10.1073/pnas.161293498.
45. Hemmi H, Takeuchi O, Kawai T, Kaisho T, Sato S, Sanjo H, Matsumoto M, Hoshino K, Wagner H, Takeda K, Akira S. 2000. A Toll-like receptor recognizes bacterial DNA. Nature 408:740-745. http://dx.doi.org/10.1038/35047123.
46. O'Hara JR, Feener TD, Fischer CD, Buret AG. 2012. Campylobacter jejuni disrupts protective Toll-like receptor 9 signaling in colonic epithelial cells and increases the severity of dextran sulfate sodium-induced colitis in mice. Infect Immun 80:1563-1571. http://dx.doi.org/10.1128/IAI.06066-11.
47. Njoroge J, Sperandio V. 2009. Jamming bacterial communication: new approaches for the treatment of infectious diseases. EMBO Mol Med 1:201-210. http://dx.doi.org/10.1002/emmm.200900032.
48. Sperandio V, Mellies JL, Nguyen W, Shin S, Kaper JB. 1999. Quorum sensing controls expression of the type III secretion gene transcription and protein secretion in enterohemorrhagic and enteropathogenic Escherichia coli. Proc Natl Acad Sci U S A 96:15196-15201. http://dx.doi.org/10.1073/pnas.96.26.15196.
49. Waters CM, Bassler BL. 2005. Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol 21:319-346. http://dx.doi.org/10.1146/annurev.cellbio.21.012704.131001.
50. Sperandio V, Torres AG, Jarvis B, Nataro JP, Kaper JB. 2003. Bacteria-host communication: the language of hormones. Proc Natl Acad SciUSA 100:8951-8956. http://dx.doi.org/10.1073/pnas.1537100100.
51. Stecher B, Denzler R, Maier L, Bernet F, Sanders MJ, Pickard DJ, Barthel M, Westendorf AM, Krogfelt KA, Walker AW, Ackermann M, Dobrindt U, Thomson NR, Hardt W-D. 2012. Gut inflammation can boost horizontal gene transfer between pathogenic and commensal Enterobacteriaceae. Proc Natl Acad Sci U S A 109:1269-1274. http://dx.doi.org/10.1073/pnas.1113246109.
52. Juge N. 2012. Microbial adhesins to gastrointestinal mucus. Trends Microbiol 20:30-39. http://dx.doi.org/10.1016/j.tim.2011.10.001.
53. Kline KA, Fälker S, Dahlberg S, Normark S, Henriques-Normark B. 2009. Bacterial adhesins in host-microbe interactions. Cell Host Microbe 5:580-592. http://dx.doi.org/10.1016/j.chom.2009.05.011.
54. Ramos HC, Rumbo M, Sirard J-C. 2004. Bacterial flagellins: mediators of pathogenicity and host immune responses in mucosa. Trends Microbiol 12:509-517. http://dx.doi.org/10.1016/j.tim.2004.09.002.
55. Konkel ME, Klena JD, Rivera-Amill V, Monteville MR, Biswas D, Raphael B, Mickelson J. 2004. Secretion of virulence proteins from Campylobacter jejuni is dependent on a functional flagellar export apparatus. J Bacteriol 186:3296-3303. http://dx.doi.org/10.1128/JB.186.11.3296-3303.2004.
56. Dhakal Bijaya K, Mulvey Matthew A. 2012. The UPEC pore-forming toxin α-hemolysin triggers proteolysis of host proteins to disrupt cell adhesion, inflammatory, and survival pathways. Cell Host Microbe 11:58-69. http://dx.doi.org/10.1016/j.chom.2011.12.003.
57. Korlath J, Osterholm M, Judy L, Forfang J, Robinson R. 1985. A point-source outbreak of campylobacteriosis associated with consumption of raw milk. J Infect Dis 152:592-596. http://dx.doi.org/10.1093/infdis/152.3.592.
58. Boyer HW, Roulland-dussoix D. 1969. A complementation analysis of the restriction and modification of DNA in Escherichia coli. J Mol Biol 41:459-472. http://dx.doi.org/10.1016/0022-2836(69)90288-5.
59. Kuhnert P, Nicolet J, Frey J. 1995. Rapid and accurate identification of Escherichia coli K-12 strains. Appl Environ Microbiol 61:4135-4139.
60. Mühldorfer I, Hacker J. 1994. Genetic aspects of Escherichia coli viru-lence. Microb Pathog 16:171-181. http://dx.doi.org/10.1006/mpat.1994.1018.
61. Mobley H. 2015. Redefining virulence of bacterial pathogens. Microbe 10:239-246.
62. Yao B, Rakhade S, Li Q, Ahmed S, Krauss R, Draghici S, Loeb J. 2004. Accuracy of cDNA microarray methods to detect small gene expression changes induced by neuregulin on breast epithelial cells. BMC Bioinform 5:99. http://dx.doi.org/10.1186/1471-2105-5-99.
63. Koressaar T, Remm M. 2007. Enhancements and modifications of primer design program Primer3. Bioinformatics 23:1289-1291. http://dx.doi.org/10.1093/bioinformatics/btm091.
64. Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG. 2012. Primer3: new capabilities and interfaces. Nucleic Acids Res 40:e115. http://dx.doi.org/10.1093/nar/gks596.
65. -ΔΔCT method. Methods 25: 402-408. http://dx.doi.org/10.1006/meth.2001.1262.
66. Darfeuille-Michaud A, Neut C, Barnich N, Lederman E, Di Martino P, Desreumaux P, Gambiez L, Joly B, Cortot A, Colombel J-F. 1998. Presence of adherent Escherichia coli strains in ileal mucosa of patients with Crohn's disease. Gastroenterology 115:1405-1413. http://dx.doi.org/10.1016/S0016-5085(98)70019-8.
67. Mukhopadhya I, Hansen R, El-Omar EM, Hold GL. 2012. IBD-what role do proteobacteria play? Nat Rev Gastroenterol Hepatol 9:219-230. http://dx.doi.org/10.1038/nrgastro.2012.14.
68. Boudeau J, Barnich N, Darfeuille-Michaud A. 2001. Type 1 pilimediated adherence of Escherichia coli strain LF82 isolated from Crohn's disease is involved in bacterial invasion of intestinal epithelial cells. Mol Microbiol 39:1272-1284. http://dx.doi.org/10.1111/j.1365-2958.2001.02315.x.
69. Chassaing B, Rolhion N, de Vallée A, Salim SY, Prorok-Hamon M, Neut C, Campbell BJ, Söderholm JD, Hugot J-P, Colombel J-F, Darfeuille-Michaud A. 2011. Crohn disease-associated adherent-invasive E. coli bacteria target mouse and human Peyer's patches via long polar fimbriae. J Clin Invest 121:966-975. http://dx.doi.org/10.1172/JCI44632.
70. Eaves-Pyles T, Allen CA, Taormina J, Swidsinski A, Tutt CB, Jezek GE, Islas-Islas M, Torres AG. 2008. Escherichia coli isolated from a Crohn's disease patient adheres, invades, and induces inflammatory responses in polarized intestinal epithelial cells. Int J Med Microbiol 298:397-409. http://dx.doi.org/10.1016/j.ijmm.2007.05.011.
71. Harada A, Sekido N, Akahoshi T, Wada T, Mukaida N, Matsushima K. 1994. Essential involvement of interleukin-8 (IL-8) in acute inflammation. J Leukoc Biol 56:559-564.
72. Krogfelt KA, Klemm P. 1988. Investigation of minor components of Escherichia coli type 1 fimbriae: protein chemical and immunological aspects. Microb Pathog 4:231-238. http://dx.doi.org/10.1016/0882-4010(88)90073-3.
73. Korea C-G, Badouraly R, Prevost M-C, Ghigo J-M, Beloin C. 2010. Escherichia coli K-12 possesses multiple cryptic but functional chaperone-usher fimbriae with distinct surface specificities. Environ Microbiol 12: 1957-1977. http://dx.doi.org/10.1111/j.1462-2920.2010.02202.x.
74. Maki S, Vonderviszt F, Furukawa Y, Imada K, Namba K. 1998. Plugging interactions of HAP2 pentamer into the distal end of flagellar filament revealed by electron microscopy. J Mol Biol 277:771-777. http://dx.doi.org/10.1006/jmbi.1998.1663.
75. Ludwig A, Tengel C, Bauer S, Bubert A, Benz R, Mollenkopf H-J, Goebel W. 1995. SlyA, a regulatory protein from Salmonella typhimurium, induces a haemolytic and pore-forming protein in Escherichia coli. Mol Gen Genet 249:474-486. http://dx.doi.org/10.1007/BF00290573.
76. Oscarsson J, Mizunoe Y, Uhlin BE, Haydon DJ. 1996. Induction of haemolytic activity in Escherichia coli by the slyA gene product. Mol Microbiol 20:191-199. http://dx.doi.org/10.1111/j.1365-2958.1996.tb02500.x.
77. Ralph ET, Guest JR, Green J. 1998. Altering the anaerobic transcription factor FNR confers a hemolytic phenotype on Escherichia coli K-12. Proc Natl Acad Sci U S A 95:10449-10452. http://dx.doi.org/10.1073/pnas.95.18.10449.
78. Lai X-H, Arencibia I, Johansson A, Wai SN, Oscarsson J, Kalfas S, Sundqvist K-G, Mizunoe Y, Sjöstedt A, Uhlin BE. 2000. Cytocidal and apoptotic effects of the ClyA protein from Escherichia coli on primary and cultured monocytes and macrophages. InfectImmun68:4363-4367. http://dx.doi.org/10.1128/IAI.68.7.4363-4367.2000.
79. Davis SP, Amrein M, Gillrie MR, Lee K, Muruve DA, Ho M. 2012. Plasmodium falciparum-induced CD36 clustering rapidly strengthens cytoadherence via p130CAS-mediated actin cytoskeletal rearrangement. FASEB J 26:1119-1130. http://dx.doi.org/10.1096/fj.11-196923.
80. Ng G, Sharma K, Ward SM, Desrosiers MD, Stephens LA, Schoel WM, Li T, Lowell CA, Ling C-C, Amrein MW, Shi Y. 2008. Receptorindependent, direct membrane binding leads to cell-surface lipid sorting and Syk kinase activation in dendritic cells. Immunity 29:807-818. http://dx.doi.org/10.1016/j.immuni.2008.09.013.
81. Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, Edberg S, Medzhitov R. 2004. Recognition of commensal microflora by Toll-like receptors is required for intestinal homeostasis. Cell 118:229-241. http://dx.doi.org/10.1016/j.cell.2004.07.002.
82. Wassenaar TM, Gunzer F. 2015. The prediction of virulence based on presence of virulence genes in Escherichia coli may not always be accurate. Gut Pathog 7:15. http://dx.doi.org/10.1186/s13099-015-0062-4.
83. Bereswill S, Fischer A, Dunay IR, Kühl AA, Göbel UB, Liesenfeld O, Heimesaat MM. 2013. Proinflammatory potential of Escherichia coli strains K-12 and Nissle 1917 in a murine model of acute ileitis. Eur J Microbiol Immunol 3:126-134. http://dx.doi.org/10.1556/EuJMI.3.2013.2.6.
84. Gerbaba TK, Gupta P, Rioux K, Hansen D, Buret AG. 2015. Giardia duodenalis-induced alterations of commensal bacteria kill Caenorhabditis elegans: a new model to study microbial-microbial interactions in the gut. Am J Physiol Gastrointest Liver Physiol 308:G550-G561. http://dx.doi.org/10.1152/ajpgi.00335.2014.
85. Wassenaar TM, Zschüttig A, Beimfohr C, Geske T, Auerbach C, Cook H, Zimmermann K, Gunzer F. 2015. Virulence genes in a probiotic Escherichia coli product with a recorded long history of safe use. Eur J Microbiol Immunol 5:81-93 http://dx.doi.org/10.1556/EuJMI-D-14-00039.
86. Guenther K, Straube E, Pfister W, Guenther A, Huebler A. 2010. Sever sepsis after probiotic treatment with Escherichia coli NISSLE 1917. Pediatr Infect Dis J 29:188-189. http://dx.doi.org/10.1097/INF.0b013e3181c36eb9.
87. Ludwig A, von Rhein C, Mischke A, Brade V. 2008. Release of latent ClyA cytolysin from Escherichia coli mediated by a bacteriophageassociated putative holin (BlyA) from Borrelia burgdorferi. Int J Med Microbiol 298:473-481. http://dx.doi.org/10.1016/j.ijmm.2007.07.014.
88. Negroni A, Costanzo M, Vitali R, Superti F, Bertuccini L, Tinari A, Minelli F, Di Nardo G, Nuti F, Pierdomenico M, Cucchiara S, Stronati L. 2012. Characterization of adherent-invasive Escherichia coli isolated from pediatric patients with inflammatory bowel disease. Inflamm Bowel Dis 18:913-924. http://dx.doi.org/10.1002/ibd.21899.