Nonhemopoietic cell TLR4 signaling is critical in causing early lipopolysaccharide-induced ileus

Journal of Immunology

Volumn 183, Issue 10, 2009, Pages 6744-6753

  Buchholz, Bettina M ^a   Chanthaphavong, R Savanh ^a   Bauer, Anthony J M ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETHANECHOL; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; MESSENGER RNA; TOLL LIKE RECEPTOR 4;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHIMERA; CONTROLLED STUDY; GASTROINTESTINAL MOTILITY DISORDER; GASTROINTESTINAL TRANSIT; ILEUS; INTESTINE CONTRACTION; MALE; MONOCYTE; MOUSE; NEUTROPHIL; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STOMACH EMPTYING;

ANIMALS; GASTROINTESTINAL MOTILITY; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; ILEUS; INTERLEUKIN-10; INTERLEUKIN-1BETA; INTERLEUKIN-6; INTESTINES; JEJUNUM; LIPOPOLYSACCHARIDES; MACROPHAGE COLONY-STIMULATING FACTOR; MACROPHAGES; MICE; MICE, INBRED C3H; MICE, KNOCKOUT; MUSCLE CONTRACTION; NEUTROPHILS; NITRIC OXIDE SYNTHASE TYPE II; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 4;

EID: 76349106672     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0901620     Document Type: Article

References (64)

1. Kaul, D. R., C. D. Collins, and R. C. Hyzy. 2008. New developments in antimicrobial use in sepsis. Curr. Pharm. Des. 14: 1912-1920.
2. Dellinger, R. P., M. M. Levy, J. M. Carlet, J. Bion, M. M. Parker, R. Jaeschke, K. Reinhart, D. C. Angus, C. Brun-Buisson, R. Beale, et al. 2008. Surviving Sepsis Campaign: international guidelines for management of severe sepsis and septic shock: 2008. Crit. Care Med. 36: 296-327.
3. Hotchkiss, R. S., and I. E. Karl. 2003. The pathophysiology and treatment of sepsis. N. Engl. J. Med. 348: 138-150.
4. Russell, J. A. 2006. Management of sepsis. N. Engl. J. Med. 355: 1699-1713.
5. Martin, G. S., D. M. Mannino, S. Eaton, and M. Moss. 2003. The epidemiology of sepsis in the United States from 1979 through 2000. N. Engl. J. Med. 348: 1546-1554.
6. Wang, H. E., N. I. Shapiro, D. C. Angus, and D. M. Yealy. 2007. National estimates of severe sepsis in United States emergency departments. Crit. Care Med. 35: 1928-1936.
7. Deitch, E. A. 2002. Bacterial translocation or lymphatic drainage of toxic products from the gut: what is important in human beings? Surgery 131: 241-244.
8. Cumming, J., G. F. Purdue, J. L. Hunt, and G. E. O'Keefe. 2001. Objective estimates of the incidence and consequences of multiple organ dysfunction and sepsis after burn trauma. J. Trauma 50: 510-515.
9. Elson, G., I. Dunn-Siegrist, B. Daubeuf, and J. Pugin. 2007. Contribution of Toll-like receptors to the innate immune response to Gram-negative and Gram-positive bacteria. Blood 109: 1574-1583.
10. Mitchell, J. A., M. J. Paul-Clark, G. W. Clarke, S. K. McMaster, and N. Cartwright. 2007. Critical role of Toll-like receptors and nucleotide oligomerisation domain in the regulation of health and disease. J. Endocrinol. 193: 323-330.
11. Philpott, D. J., and S. E. Girardin. 2004. The role of Toll-like receptors and Nod proteins in bacterial infection. Mol. Immunol. 41: 1099-1108.
12. Kobayashi, M., S. Saitoh, N. Tanimura, K. Takahashi, K. Kawasaki, M. Nishijima, Y. Fujimoto, K. Fukase, S. Kashi-Takamura, and K. Miyake. 2006. Regulatory roles for MD-2 and TLR4 in ligand-induced receptor clustering. J. Immunol. 176: 6211-6218.
13. Poltorak, A., X. He, I. Smirnova, M. Y. Liu, H. C. Van, X. Du, D. Birdwell, E. Alejos, M. Silva, C. Galanos, et al. 1998. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 282: 2085-2088.
14. Re, F., and J. L. Strominger. 2003. Separate functional domains of human MD-2 mediate Toll-like receptor 4-binding and lipopolysaccharide responsiveness. J. Immunol. 171: 5272-5276. (Pubitemid 37432812)
15. Wright, S. D., R. A. Ramos, P. S. Tobias, R. J. Ulevitch, and J. C. Mathison. 1990. CD14, a receptor for complexes of lipopolysaccharide (LPS) and LPS binding protein [see comment]. Science 249: 1431-1433. (Pubitemid 120034118)
16. Schumann, R. R., S. R. Leong, G. W. Flaggs, P. W. Gray, S. D. Wright, J. C. Mathison, P. S. Tobias, and R. J. Ulevitch. 1990. Structure and function of lipopolysaccharide binding protein. Science 249: 1429-1431.
17. Medzhitov, R., P. Preston-Hurlburt, and C. A. Janeway, Jr. 1997. A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature 388: 394-397.
18. Poltorak, A., X. He, I. Smirnova, M. Y. Liu, H. C. Van, X. Du, D. Birdwell, E. Alejos, M. Silva, C. Galanos, et al. 1998. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 282: 2085-2088.
19. Beutler, B., X. Du, and A. Poltorak. 2001. Identification of Toll-like receptor 4 (Tlr4) as the sole conduit for LPS signal transduction: genetic and evolutionary studies. J. Endotoxin Res. 7: 277-280.
20. Sha, T., M. Sunamoto, T. Kitazaki, J. Sato, M. Ii, and Y. Iizawa. 2007. Therapeutic effects of TAK-242, a novel selective Toll-like receptor 4 signal transduction inhibitor, in mouse endotoxin shock model. Eur. J. Pharmacol. 571: 231-239.
21. Tsung, A., R. A. Hoffman, K. Izuishi, N. D. Critchlow, A. Nakao, M. H. Chan, M. T. Lotze, D. A. Geller, and T. R. Billiar. 2005. Hepatic ischemia/reperfusion injury involves functional TLR4 signaling in nonparenchymal cells. J. Immunol. 175: 7661-7668.
22. Tavener, S. A., E. M. Long, S. M. Robbins, K. M. McRae, H. Van Remmen, and P. Kubes. 2004. Immune cell Toll-like receptor 4 is required for cardiac myocyte impairment during endotoxemia. Circ. Res. 95: 700-707.
23. Mollen, K. P., R. M. Levy, J. M. Prince, R. A. Hoffman, M. J. Scott, D. J. Kaczorowski, R. Vallabhaneni, Y. Vodovotz, and T. R. Billiar. 2008. Systemic inflammation and end organ damage following trauma involves functional TLR4 signaling in both bone marrow-derived cells and parenchymal cells. J. Leukocyte Biol. 83: 80-88.
24. Wu, H., G. Chen, K. R. Wyburn, J. Yin, P. Bertolino, J. M. Eris, S. I. Alexander, A. F. Sharland, and S. J. Chadban. 2007. TLR4 activation mediates kidney ischemia/reperfusion injury. J. Clin. Invest. 117: 2847-2859.
25. Pulskens, W. P., G. J. Teske, L. M. Butter, J. J. Roelofs, P. T. van der, S. Florquin, and J. C. Leemans. 2008. Toll-like receptor-4 coordinates the innate immune response of the kidney to renal ischemia/reperfusion injury. PLoS One 3: e3596.
26. Patole, P. S., S. Schubert, K. Hildinger, S. Khandoga, A. Khandoga, S. Segerer, A. Henger, M. Kretzler, M. Werner, F. Krombach, et al. 2005. Toll-like receptor-4: renal cells and bone marrow cells signal for neutrophil recruitment during pyelonephritis. Kidney Int. 68: 2582-2587.
27. Chakravarty, S., and M. Herkenham. 2005. Toll-like receptor 4 on nonhematopoietic cells sustains CNS inflammation during endotoxemia, independent of systemic cytokines. J. Neurosci. 25: 1788-1796.
28. Binck, B. W., M. F. Tsen, M. Islas, D. J. White, R. A. Schultz, M. S. Willis, J. V. Garcia, J. W. Horton, and J. A. Thomas. 2005. Bone marrow-derived cells contribute to contractile dysfunction in endotoxic shock. Am. J. Physiol. 288: H577-H583.
29. Eskandari, M. K., J. C. Kalff, T. R. Billiar, K. K. Lee, and A. J. Bauer. 1999. LPS-induced muscularis macrophage nitric oxide suppresses rat jejunal circular muscle activity. Am. J. Physiol. 277: t-86.
30. Bauer, A. J. 2008. Mentation on the immunological modulation of gastrointestinal motility. Neurogastroenterol. Motil. 20(Suppl. 1): 81-90.
31. Takakura, K., K. Hasegawa, Y. Goto, and I. Muramatsu. 1997. Nitric oxide produced by inducible nitric oxide synthase delays gastric emptying in lipopolysaccharide-treated rats. Anesthesiology 87: 652-657.
32. Eskandari, M. K., J. C. Kalff, T. R. Billiar, K. K. Lee, and A. J. Bauer. 1997. Lipopolysaccharide activates the muscularis macrophage network and suppresses circular smooth muscle activity. Am. J. Physiol. 273: G727-G734. (Pubitemid 27418794)
33. Lodato, R. F., A. R. Khan, M. J. Zembowicz, N. W. Weisbrodt, T. A. Pressley, Y. F. Li, J. A. Lodato, A. Zembowicz, and F. G. Moody. 1999. Roles of IL-1 and TNF in the decreased ileal muscle contractility induced by lipopolysaccharide. Am. J. Physiol. 276: t-62.
34. Salinthone, S., C. A. Singer, and W. T. Gerthoffer. 2004. Inflammatory gene expression by human colonic smooth muscle cells. Am. J. Physiol. 287: G627-G637.
35. Akiho, H., W. I. Khan, A. Al-Kaabi, P. Blennerhassett, Y. Deng, and S. M. Collins. 2007. Cytokine modulation of muscarinic receptors in the murine intestine. Am. J. Physiol. 293: G250-G255.
36. Bercik, P., R. Diorgio, P. Blennerhassett, E. F. Verdu, G. Barbara, and S. M. Collins. 2002. Immune-mediated neural dysfunction in a murine model of chronic Helicobacter pylori infection. Gastroenterology 123: 1205-1215.
37. Collins, S. M., P. Blennerhassett, D. L. Vermillion, K. Davis, J. Langer, and P. B. Ernst. 1992. Impaired acetylcholine release in the inflamed rat intestine is T cell independent. Am. J. Physiol. 263: G198-G201.
38. Duncan, M., A. Mouihate, K. Mackie, C. M. Keenan, N. E. Buckley, J. S. Davison, K. D. Patel, Q. J. Pittman, and K. A. Sharkey. 2008. Cannabinoid CB2 receptors in the enteric nervous system modulate gastrointestinal contractility in lipopolysaccharide-treated rats. Am. J. Physiol. 295: G78-G87.
39. Mathison, R., W. Ho, Q. J. Pittman, J. S. Davison, and K. A. Sharkey. 2004. Effects of cannabinoid receptor-2 activation on accelerated gastrointestinal transit in lipopolysaccharide-treated rats. Br. J. Pharmacol. 142: 1247-1254.
40. Turler, A., J. C. Kalff, B. A. Moore, R. A. Hoffman, T. R. Billiar, R. L. Simmons, and A. J. Bauer. 2006. Leukocyte-derived inducible nitric oxide synthase mediates murine postoperative ileus. Ann. Surg. 244: 220-229.
41. Binck, B. W., M. F. Tsen, M. Islas, D. J. White, R. A. Schultz, M. S. Willis, J. V. Garcia, J. W. Horton, and J. A. Thomas. 2005. Bone marrow-derived cells contribute to contractile dysfunction in endotoxic shock. Am. J. Physiol. 288: H577-H583.
42. Mosley, R. L., and J. R. Klein. 1992. Repopulation kinetics of intestinal intraepithelial lymphocytes in murine bone marrow radiation chimeras. Transplantation 53: 868-874.
43. Evans, E. P., D. A. Ogden, C. E. Ford, and H. S. Micklem. 1967. Repopulation of Peyer's patches in mice. Nature 216: 36-38.
44. Naito, M., S. Hayashi, H. Yoshida, S. Nishikawa, L. D. Shultz, and K. Takahashi. 1991. Abnormal differentiation of tissue macrophage populations in "osteopetrosis" (op) mice defective in the production of macrophage colony-stimulating factor. Am J Pathol. 139: 657-667.
45. Mikkelsen, H. B., and L. Thuneberg. 1999. Op/op mice defective in production of functional colony-stimulating factor-1 lack macrophages in muscularis externa of the small intestine. Cell Tissue Res. 295: 485-493.
46. Xiong, H., C. Zhu, F. Li, R. Hegazi, K. He, M. Babyatsky, A. J. Bauer, and S. E. Plevy. 2004. Inhibition of interleukin-12 p40 transcription and NF-κB activation by nitric oxide in murine macrophages and dendritic cells. J. Biol. Chem. 279: 10776-10783.
47. The, F. O., W. J. de Jonge, R. J. Bennink, R. M. van den Wijngaard, and G. E. Boeckxstaens. 2005. The ICAM-1 antisense oligonucleotide ISIS-3082 prevents the development of postoperative ileus in mice. Br. J. Pharmacol. 146: 252-258.
48. Schmidt, J., B. Stoffels, B. A. Moore, R. S. Chanthaphavong, A. R. Mazie, B. M. Buchholz, and A. J. Bauer. 2008. Proinflammatory Role of leukocyte-derived Egr-1 in the development of murine postoperative ileus. Gastroenterology 135: 926-936.
49. Ricart-Janq, D., M. Llobera, and M. D. López-Tejero. 2002. Anticoagulants and other preanalytical factors interfere in plasma nitrate/nitrite quantification by the Griess method. Nitric Oxide 6: 178-185.
50. Manthey, C. L., P. Y. Perera, B. E. Henricson, T. A. Hamilton, N. Qureshi, and S. N. Vogel. 1994. Endotoxin-induced early gene expression in C3H/HeJ (Lpsd) macrophages. J. Immunol. 153: 2653-2663. (Pubitemid 24278135)
51. Hirschfeld, M., Y. Ma, J. H. Weis, S. N. Vogel, and J. J. Weis. 2000. Cutting edge: repurification of lipopolysaccharide eliminates signaling through both human and murine Toll-like receptor 2. J. Immunol. 165: 618-622. (Pubitemid 30484724)
52. Nakao, A., B. A. Moore, N. Murase, F. Liu, B. S. Zuckerbraun, F. H. Bach, A. M. Choi, M. A. Nalesnik, L. E. Otterbein, and A. J. Bauer. 2003. Immunomodulatory effects of inhaled carbon monoxide on rat syngeneic small bowel graft motility. Gut 52: 1278-1285.
53. Wehner, S., F. F. Behrendt, B. N. Lyutenski, M. Lysson, A. J. Bauer, A. Hirner, and J. C. Kalff. 2007. Inhibition of macrophage function prevents intestinal inflammation and postoperative ileus in rodents. Gut 56: 176-185.
54. Turler, A., N. T. Schwarz, E. Turler, J. C. Kalff, and A. J. Bauer. 2002. MCP-1 causes leukocyte recruitment and subsequently endotoxemic ileus in rat. Am. J. Physiol. 282: G145-G155. (Pubitemid 34650109)
55. DeFilippis, D., T. Iuvone, A. D'Amico, G. Esposito, L. Steardo, A. G. Herman, P. A. Pelckmans, B. Y. De Winter, and J. G. De Man. 2008. Effect of cannabidiol on sepsis-induced motility disturbances in mice: involvement of CB receptors and fatty acid amide hydrolase. Neurogastroenterol. Motil. 20: 919-927.
56. David, M. D., C. L. Cochrane, S. K. Duncan, and J. W. Schrader. 2005. Pure lipopolysaccharide or synthetic lipid A induces activation of p21Ras in primary macrophages through a pathway dependent on Src family kinases and PI3K. J. Immunol. 175: 8236-8241.
57. Iwaki, Y., T. E. Starzl, A. Yagihashi, S. Taniwaki, K. Abu-Elmagd, A. Tzakis, J. Fung, S. Todo, and Y. Iwaki. 1991. Replacement of donor lymphoid tissue in small-bowel transplants. Lancet 337: 818-819.
58. Grasa, L., M. P. Arruebo, M. A. Plaza, and M. D. Murillo. 2009. A down-regulation of nNOS is associated to dysmotility evoked by lipopolysaccharide in rabbit duodenum. J. Physiol. Pharmacol. 59: 511-524.
59. Lee, H. T., G. W. Hennig, N. W. Fleming, K. D. Keef, N. J. Spencer, S. M. Ward, K. M. Sanders, and T. K. Smith. 2007. Septal interstitial cells of Cajal conduct pacemaker activity to excite muscle bundles in human jejunum. Gastroenterology 133: 907-917.
60. Kito, Y., S. M. Ward, and K. M. Sanders. 2005. Pacemaker potentials generated by interstitial cells of Cajal in the murine intestine. Am. J. Physiol. 288: C710-C720.
61. Walton, K. L. W., L. Holt, and R. B. Sartor. 2009. Lipopolysaccharide activates innate immune responses in murine intestinal myofibroblasts through multiple signaling pathways. Am. J. Physiol. 296: G601-G611.
62. Barajon, I., G. Serrao, F. Arnaboldi, E. Opizzi, G. Ripamonti, A. Balsari, and C. Rumio. Toll-like receptors 3, 4, and 7 are expressed in the enteric nervous system and dorsal root ganglia. J. Histochem. Cytochem. In press.
63. Rumio, C., D. Besusso, F. Arnaboldi, M. Palazzo, S. Selleri, S. Gariboldi, S. Akira, S. Uematsu, P. Bignami, V. Ceriani, et al. 2006. Activation of smooth muscle and myenteric plexus cells of jejunum via Toll-like receptor 4. J. Cell. Physiol. 208: 47-54.
64. Cousins, D. J., D. Z. Staynov, and T. H. Lee. 1994. Regulation of interleukin-5 and granulocyte-macrophage colony-stimulating factor expression. Am. J. Respir. Crit. Care Med. 150: S50-S53.