Hypoxia-inducible factor-dependent regulation of platelet-activating factor receptor as a route for gram-positive bacterial translocation across epithelia

Molecular Biology of the Cell

Volumn 21, Issue 4, 2010, Pages 538-546

  Keely, Simon ^a   Glover, Louise E ^a   Weissmueller, Thomas ^a   MacManus, Christopher F ^a   Fillon, Sophie ^b   Fennimore, Blair ^a   Colgan, Sean P ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b CHILDREN S HOSPITAL COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYPOXIA INDUCIBLE FACTOR; SHORT HAIRPIN RNA; THROMBOCYTE ACTIVATING FACTOR RECEPTOR;

ARTICLE; BACTERIAL STRAIN; BACTERIAL TRANSLOCATION; CONTROLLED STUDY; ENTEROCOCCUS FAECALIS; GENE REPRESSION; GRAM POSITIVE BACTERIUM; HUMAN; HUMAN CELL; INTESTINE EPITHELIUM; INTESTINE EPITHELIUM CELL; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM;

ANIMALS; ANOXIA; BIOLOGICAL TRANSPORT; CACO-2 CELLS; CELL MEMBRANE; GENE KNOCKDOWN TECHNIQUES; GRAM-POSITIVE BACTERIA; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; INTESTINAL MUCOSA; ISOENZYMES; MICE; PLATELET MEMBRANE GLYCOPROTEINS; RECEPTORS, G-PROTEIN-COUPLED; RNA INTERFERENCE; TRANSCRIPTIONAL ACTIVATION;

BACTERIA (MICROORGANISMS); ENTEROCOCCUS FAECALIS; POSIBACTERIA;

EID: 76649099516     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E09-07-0573     Document Type: Article

References (41)

1. Barbier, M., Oliver, A., Rao, J., Hanna, S. L., Goldberg, J. B., and Alberti, S. (2008). Novel phosphorylcholine-containing protein of Pseudomonas aeruginosa chronic infection isolates interacts with airway epithelial cells. J. Infect. Dis. 197, 465-473.
2. Berney, M., Hammes, F., Bosshard, F., Weilenmann, H. U., and Egli, T. (2007). Assessment and interpretation of bacterial viability by using the LIVE/DEAD BacLight Kit in combination with flow cytometry. Appl. Environ. Microbiol. 73, 3283-3290.
3. Caplan, M. S., Hedlund, E., Adler, L., Lickerman, M., and Hsueh, W. (1997). The platelet-activating factor receptor antagonist WEB 2170 prevents neonatal necrotizing enterocolitis in rats. J. Pediatr. Gastroenterol. Nutr. 24, 296-301.
4. Caplan, M. S., Simon, D., and Jilling, T. (2005). The role of PAF, TLR, and the inflammatory response in neonatal necrotizing enterocolitis. Semin. Pediatr. Surg. 14, 145-151.
5. Claud, E. C., Li, D., Xiao, Y., Caplan, M. S., and Jilling, T. (2002). Platelet-activating factor regulates chloride transport in colonic epithelial cell monolayers. Pediatr. Res. 52, 155-162.
6. Cundell, D. R., Gerard, N. P., Gerard, C., Idanpaan-Heikkila, I., and Tuomanen, E. I. (1995). Streptococcus pneumoniae anchor to activated human cells by the receptor for platelet-activating factor. Nature 377, 435-438.
7. Draing, C., Pfitzenmaier, M., Zummo, S., Mancuso, G., Geyer, A., Hartung, T., and von Aulock, S. (2006). Comparison of lipoteichoic acid from different serotypes of Streptococcus pneumoniae. J. Biol. Chem. 281, 33849-33859.
8. Fillon, S. et al. (2006). Platelet-activating factor receptor and innate immunity: uptake of gram-positive bacterial cell wall into host cells and cell-specific pathophysiology. J. Immunol. 177, 6182-6191.
9. Fink, M. (1997). Cytopathic hypoxia in sepsis. Acta Anaesthesiol. Scand. Suppl. 110, 87-95.
10. Fink, M. P. (1991). Gastrointestinal mucosal injury in experimental models of shock, trauma, and sepsis. Crit. Care Med. 19, 627-641.
11. Fink, M. P. (2001). Cytopathic hypoxia. Mitochondrial dysfunction as mechanism contributing to organ dysfunction in sepsis. Crit. Care Clin. 17, 219-237.
12. Finlay, B. B., Gumbiner, B., and Falkow, S. (1988). Penetration of Salmonella through a polarized Madin-Darby canine kidney epithelial cell monolayer. J. Cell Biol. 107, 221-230.
13. Furuta, G. T., Turner, J. R., Taylor, C. T., Hershberg, R. M., Comerford, K., Narravula, S., Podolsky, D. K., and Colgan, S. P. (2001). Hypoxia-inducible factor 1-dependent induction of intestinal trefoil factor protects barrier function during hypoxia. J. Exp. Med. 193, 1027-1034.
14. Hageman, J. C., Fridkin, S. K., Mohammed, J. M., Steward, C. D., Gaynes, R. P., and Tenover, F. C. (2003). Antimicrobial proficiency testing of National Nosocomial Infections Surveillance System hospital laboratories. Infect. Control Hosp. Epidemiol. 24, 356-361.
15. Han, S. H., Kim, J. H., Seo, H. S., Martin, M. H., Chung, G. H., Michalek, S. M., and Nahm, M. H. (2006). Lipoteichoic acid-induced nitric oxide production depends on the activation of platelet-activating factor receptor and Jak2. J. Immunol. 176, 573-579.
16. Hirayama, K., Yokoi, Y., Sakaguchi, T., Nakamura, T., Kashiwabara, H., Sunayama, K., and Nakamura, S. (2003). Platelet-activating factor, a critical mediator in the pathogenesis of dextran sulfate sodium-induced colitis in rats. Dis. Colon Rectum 46, 100-110.
17. Karhausen, J., Furuta, G. T., Tomaszewski, J. E., Johnson, R. S., Colgan, S. P., and Haase, V. H. (2004). Epithelial hypoxia-inducible factor-1 is protective in murine experimental colitis. J. Clin. Invest. 114, 1098-1106.
18. Karhausen, J., Haase, V. H., and Colgan, S. P. (2005). Inflammatory hypoxia: role of hypoxia-inducible factor. Cell Cycle 4, 256-258.
19. Karhausen, J., Ibla, J. C., and Colgan, S. P. (2003). Implications of hypoxia on mucosal barrier function. Cell. Mol. Biol. 49, 77-87.
20. Keely, S., Rawlinson, L. A., Haddleton, D. M., and Brayden, D. J. (2008). A tertiary amino-containing polymethacrylate polymer protects mucus-covered intestinal epithelial monolayers against pathogenic challenge. Pharm. Res. 25, 1193-1201.
21. Keely, S., Rullay, A., Wilson, C., Carmichael, A., Carrington, S., Corfield, A., Haddleton, D. M., and Brayden, D. J. (2005). In vitro and ex vivo intestinal tissue models to measure mucoadhesion of poly (methacrylate) and N-trimethylated chitosan polymers. Pharm. Res. 22, 38-49.
22. Keely, S., Ryan, S. M., Haddleton, D. M., Limer, A., Mantovani, G., Murphy, E. P., Colgan, S. P., and Brayden, D. J. (2009). Dexamethasone-pDMAEMA polymeric conjugates reduce inflammatory biomarkers in human intestinal epithelial monolayers. J. Control Release 135, 35-43.
23. Kong, T., Eltzschig, H. K., Karhausen, J., Colgan, S. P., and Shelley, C. S. (2004). Leukocyte adhesion during hypoxia is mediated by HIF-1-dependent induction of beta2 integrin gene expression. Proc. Natl. Acad. Sci. USA 101, 10440-10445.
24. Lam, S., Singer, C., Tucci, V., Morthland, V. H., Pfaller, M. A., and Isenberg, H. D. (1995). The challenge of vancomycin-resistant enterococci: a clinical and epidemiologic study. Am. J. Infect. Control 23, 170-180.
25. Lemjabbar, H., and Basbaum, C. (2002). Platelet-activating factor receptor and ADAM10 mediate responses to Staphylococcus aureus in epithelial cells. Nat. Med. 8, 41-46.
26. Lenz, A., Franklin, G. A., and Cheadle, W. G. (2007). Systemic inflammation after trauma. Injury 38, 1336-1345.
27. Louis, N. A., Robinson, A. M., MacManus, C. F., Karhausen, J., Scully, M., and Colgan, S. P. (2008). Control of IFN-alphaA by CD 73, implications for mucosal inflammation. J. Immunol. 180, 4246-4255.
28. Ma, T. Y., Boivin, M. A., Ye, D., Pedram, A., and Said, H. M. (2005). Mechanism of TNF-{alpha} modulation of Caco-2 intestinal epithelial tight junction barrier: role of myosin light-chain kinase protein expression. Am. J. Physiol. Gastrointest. Liver Physiol. 288, G422-G430.
29. Marano, C. W., Lewis, S. A., Garulacan, L. A., Soler, A. P., and Mullin, J. M. (1998). Tumor necrosis factor-alpha increases sodium and chloride conductance across the tight junction of CACO-2 BBE, a human intestinal epithelial cell line. J. Membr. Biol. 161, 263-274.
30. Meakins, J. L., and Marshall, J. C. (1986). The gastrointestinal tract: the "motor" of multiple organ failure. Arch. Surg. 121, 197.
31. NNIS System (2003). National Nosocomial Infections Surveillance (NNIS) System Report, data summary from January 1992 through June 2003, issued August 2003. Am. J. Infect. Control 31, 481-498.
32. Okayasu, I., Hatakeyama, S., Yamada, M., Ohkusa, T., Inagaki, Y., and Nakaya, R. (1990). A novel method in the induction of reliable experimental acute and chronic ulcerative colitis in mice. Gastroenterology 98, 694-702.
33. Pier, G. B., Grout, M., and Zaidi, T. S. (1997). Cystic fibrosis transmembrane conductance regulator is an epithelial cell receptor for clearance of Pseudomonas aeruginosa from the lung. Proc. Natl. Acad. Sci. USA 94, 12088-12093.
34. Rijneveld, A. W., Weijer, S., Florquin, S., Speelman, P., Shimizu, T., Ishii, S., and van der Poll, T. (2004). Improved host defense against pneumococcal pneumonia in platelet-activating factor receptor-deficient mice. J. Infect. Dis. 189, 711-716.
35. Ring, A., Weiser, J. N., and Tuomanen, E. I. (1998). Pneumococcal trafficking across the blood-brain barrier. Molecular analysis of a novel bidirectional pathway. J. Clin. Invest. 102, 347-360.
36. Shah, Y. M., Ito, S., Morimura, K., Chen, C., Yim, S. H., Haase, V. H., and Gonzalez, F. J. (2008). Hypoxia-inducible factor augments experimental colitis through an MIF-dependent inflammatory signaling cascade. Gastroenterology 134, 2036-2048, 2048, e2031-e2033.
37. Synnestvedt, K., Furuta, G. T., Comerford, K. M., Louis, N., Karhausen, J., Eltzschig, H. K., Hansen, K. R., Thompson, L. F., and Colgan, S. P. (2002). Ecto-5′-nucleotidase (CD73) regulation by hypoxia-inducible factor-1 mediates permeability changes in intestinal epithelia. J. Clin. Invest. 110, 993-1002.
38. Taylor, C. T., and Colgan, S. P. (2007). Hypoxia and gastrointestinal disease. J. Mol. Med. 85, 1295-1300.
39. Tyrer, P., Foxwell, A. R., Cripps, A. W., Apicella, M. A., and Kyd, J. M. (2006). Microbial pattern recognition receptors mediate M-cell uptake of a gram-negative bacterium. Infect. Immun. 74, 625-631.
40. Wallace, J. L. (1988). Release of platelet-activating factor (PAF) and accelerated healing induced by a PAF antagonist in an animal model of chronic colitis. Can. J. Physiol. Pharmacol. 66, 422-425.
41. Zinkernagel, A. S., Johnson, R. S., and Nizet, V. (2007). Hypoxia inducible factor (HIF) function in innate immunity and infection. J. Mol. Med. 85, 1339-1346.