Role of interleukin-6 in hemopoietic and non-hemopoietic synergy mediating TLR4-triggered late murine ileus and endotoxic shock

Neurogastroenterology and Motility

Volumn 24, Issue 7, 2012, Pages

  Buchholz, B M ^a,b   Chanthaphavong, R S ^c   Billiar, T R ^c   Bauer, A J ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b UNIVERSITY OF BONN   (Germany)

^c UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

Author keywords

Endotoxin; Gastrointestinal motility; IL 6R blockade; Inflammation; Lipopolysaccharide; Sepsis; Shock

Indexed keywords

INTERLEUKIN 6; LIPOPOLYSACCHARIDE; RECOMBINANT INTERLEUKIN 6; TOLL LIKE RECEPTOR 4;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL LINEAGE; CONTROLLED STUDY; HEMATOPOIETIC CELL; ILEUS; INFLAMMATION; MACROPHAGE; MALE; MOUSE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; SEPTIC SHOCK; SIGNAL TRANSDUCTION;

ANIMALS; CELL LINEAGE; ILEUS; IMMUNOHISTOCHEMISTRY; INTERLEUKIN-6; INTESTINAL MUCOSA; MACROPHAGES; MALE; MICE; MICE, KNOCKOUT; MUSCLE CONTRACTION; MUSCLE, SMOOTH; NEUTROPHILS; SHOCK, SEPTIC; TOLL-LIKE RECEPTOR 4;

EID: 84862661265     PISSN: 13501925     EISSN: 13652982     Source Type: Journal    
DOI: 10.1111/j.1365-2982.2012.01914.x     Document Type: Article

References (57)

1. Buchholz BM, Bauer AJ. Membrane TLR signaling mechanisms in the gastrointestinal tract during sepsis. Neurogastroenterol Motil 2010; 22: 232-45.
2. Medzhitov R, Janeway J. The Toll receptor family and microbial recognition. Trends in Microbiol 2000; 10: 452-6.
3. Akira S, Takeda K. Toll-like receptor signalling. Nat Rev Immunol 2004; 4: 499-511.
4. Angus DCM, Linde-Zwirble WT, Lidicker JM, Clermont GM, Carcillo JM, Pinsky MRM. Epidemiology of severe sepsis in the United States: analysis of incidence, outcome, and associated costs of care. Crit Care Med 2001; 29: 1303-10.
5. Melamed A, Sorvillo FJ. The burden of sepsis-associated mortality in the United States from 1999 to 2005: an analysis of multiple-cause-of-death data. Crit Care (London, England) 2009; 13: R28.
6. Deitch EA. Bacterial translocation or lymphatic drainage of toxic products from the gut: what is important in human beings? Surgery 2002; 131: 241-4.
7. Eskandari MK, Kalff JC, Billiar TR, Lee KK, Bauer AJ. Lipopolysaccharide activates the muscularis macrophage network and suppresses circular smooth muscle activity. Am J Physiol 1997; 273(3 Pt 1): G727-34.
8. Buchholz BM, Chanthaphavong RS, Bauer AJM. Nonhemopoietic cell TLR4 signaling is critical in causing early lipopolysaccharide-induced ileus. J Immunol 2009; 183: 6744-53.
9. Buchholz BM, Billiar TR, Bauer AJ. Dominant role of the MyD88-dependent signaling pathway in mediating early endotoxin-induced murine ileus. Am J Physiol Gastrointest Liver Physiol 2010; 299: G531-8.
10. Binck BW, Tsen MF, Islas M et al. Bone marrow-derived cells contribute to contractile dysfunction in endotoxic shock. Am J Physiol Heart Circ Physiol 2005; 288: H577-83.
11. Mollen KP, Levy RM, Prince JM et al. Systemic inflammation and end organ damage following trauma involves functional TLR4 signaling in both bone marrow-derived cells and parenchymal cells. J Leukoc Biol 2008; 83: 80-8.
12. Chakravarty S, Herkenham M. Toll-like receptor 4 on nonhematopoietic cells sustains CNS inflammation during endotoxemia, independent of systemic cytokines. J Neurosci 2005;25:1788-96.
13. Hui W, Jinxiang Z, Heshui W, Zhuoya L, Qichang Z. Bone marrow and non-bone marrow TLR4 regulates hepatic ischemia/reperfusion injury. Biochem Biophys Res Commun 2009; 389: 328-32.
14. Overhaus M, Togel S, Pezzone MA, Bauer AJ. Mechanisms of polymicrobial sepsis-induced ileus. Am J Physiol Gastrointest Liver Physiol 2004; 287: G685-94.
15. Schwarz NT, Engel B, Eskandari MK, Kalff JC, Grandis JR, Bauer AJ. Lipopolysaccharide preconditioning and cross-tolerance: the induction of protective mechanisms for rat intestinal ileus. Gastroenterology 2002; 123: 586-98.
16. Bozza FA, Salluh JI, Japiassu AM et al. Cytokine profiles as markers of disease severity in sepsis: a multiplex analysis. Crit Care 2007; 11: R49.
17. Greenhill CJ, Rose-John S, Lissilaa R et al. IL-6 trans-signaling modulates TLR4-dependent inflammatory responses via STAT3. J Immunol 2011; 186: 1199-208.
18. McCarthy DO. Tumor necrosis factor alpha and interleukin-6 have differential effects on food intake and gastric emptying in fasted rats. Res Nurs Health 2000; 23: 222-8.
19. Buchholz BM, Masutani K, Kawamura T et al. Hydrogen-enriched preservation protects the isogeneic intestinal graft and amends recipient gastric function during transplantation. Transplantation 2011; 92: 985-92.
20. Schmidt J, Stoffels B, Moore BA et al. Proinflammatory role of leukocyte-derived Egr-1 in the development of murine postoperative ileus. Gastroenterology 2008; 135: 926-36.
21. Okazaki M, Yamada Y, Nishimoto N, Yoshizaki K, Mihara M. Characterization of anti-mouse interleukin-6 receptor antibody. Immunol Lett 2002; 84: 231-40.
22. Kalff JC, Schwarz NT, Walgenbach KJ, Schraut WH, Bauer AJ. Leukocytes of the intestinal muscularis: their phenotype and isolation. J Leukoc Biol 1998; 63: 683-91.
23. Kalff JC, Carlos TM, Schraut WH, Billiar TR, Simmons RL, Bauer AJ. Surgically induced leukocytic infiltrates within the rat intestinal muscularis mediate postoperative ileus. Gastroenterology 1999; 117: 378-87.
24. Eskandari MK, Kalff JC, Billiar TR, Lee KK, Bauer AJ. LPS-induced muscularis macrophage nitric oxide suppresses rat jejunal circular muscle activity. Am J Physiol 1999; 277: G478-86.
25. Turler A, Schwarz NT, Turler E, Kalff JC, Bauer AJ. MCP-1 causes leukocyte recruitment and subsequently endotoxemic ileus in rat. Am J Physiol Gastrointest Liver Physiol 2002; 282: G145-55.
26. Lodato RF, Khan AR, Zembowicz MJ et al. Roles of IL-1 and TNF in the decreased ileal muscle contractility induced by lipopolysaccharide. Am J Physiol 1999; 276(6 Pt 1): G1356-62.
27. Xu H, Gonzalo JA, St PY et al. Leukocytosis and resistance to septic shock in intercellular adhesion molecule 1-deficient mice. J Exp Med 1994; 180: 95-109.
28. Andonegui G, Zhou H, Bullard D et al. Mice that exclusively express TLR4 on endothelial cells can efficiently clear a lethal systemic Gram-negative bacterial infection. J Clin Invest 2009; 119: 1921-30.
29. Pearce EJ, Kane CM, Sun J. Regulation of dendritic cell function by pathogen-derived molecules plays a key role in dictating the outcome of the adaptive immune response. Chem Immunol Allergy 2006; 90: 82-90.
30. Martinez FO, Sica A, Mantovani A, Locati M. Macrophage activation and polarization. Front Biosci 2008; 13: 453-61.
31. Koscielny A, Boerner T, Wehner S, Kurts C, Kalff JC. The role of dendritic cells in the gastrointestinal field effect. Transplant Proc 2007; 38: 1815-7.
32. Engel DR, Koscielny A, Wehner S et al. T helper type 1 memory cells disseminate postoperative ileus over the entire intestinal tract. Nat Med 2010; 16: 1407-13.
33. De TC, Pajak B, Brait M et al. TLR4 and Toll-IL-1 receptor domain-containing adapter-inducing IFN-beta, but not MyD88, regulate Escherichia coli-induced dendritic cell maturation and apoptosis in vivo. J Immunol 2005; 175: 839-46.
34. Napolitani G, Rinaldi A, Bertoni F, Sallusto F, Lanzavecchia A. Selected Toll-like receptor agonist combinations synergistically trigger a T helper type 1-polarizing program in dendritic cells. Nat Immunol 2005; 6: 769-76.
35. Coombes JL, Powrie F. Dendritic cells in intestinal immune regulation. Nat Rev Immunol 2008; 8: 435-46.
36. Zanin-Zhorov A, Tal-Lapidot G, Cahalon L et al. Cutting edge: T cells respond to lipopolysaccharide innately via TLR4 signaling. J Immunol 2007; 179: 41-4.
37. Song M, Kellum JA. Interleukin-6. Crit Care Med 2005; 33(12 Suppl): S463-5.
38. Fang C, Zhang X, Miwa T, Song WC. Complement promotes the development of inflammatory T-helper 17 cells through synergistic interaction with Toll-like receptor signaling and interleukin-6 production. Blood 2009; 114: 1005-15.
39. Wehner S, Schwarz NT, Hundsdoerfer R et al. Induction of IL-6 within the rodent intestinal muscularis after intestinal surgical stress. Surgery 2005; 137: 436-46.
40. Ruhl A, Hurst S, Collins SM. Synergism between interleukins 1 beta and 6 on noradrenergic nerves in rat myenteric plexus. Gastroenterology 1994; 107: 993-1001.
41. Montuschi P, Preziosi P, Navarra P. Interleukin-1α and tumor necrosis factor inhibit rat gastric fundus motility in vitro. Eur J Pharmacol 1993; 233: 303-4.
42. Jones SA, Horiuchi S, Topley N, Yamamoto N, Fuller GM. The soluble interleukin 6 receptor: mechanisms of production and implications in disease. FASEB J 2001; 15: 43-58.
43. Lust JA, Donovan KA, Kline MP, Greipp PR, Kyle RA, Maihle NJ. Isolation of an mRNA encoding a soluble form of the human interleukin-6 receptor. Cytokine 1992; 4: 96-100.
44. Briso EM, Dienz O, Rincon M. Cutting edge: soluble IL-6R is produced by IL-6R ectodomain shedding in activated CD4 T cells. J Immunol 2008; 180: 7102-6.
45. Sha Y, Markovic-Plese S. A role of IL-1R1 signaling in the differentiation of Th17 cells and the development of autoimmune diseases. Self Nonself 2011; 2: 35-42.
46. Francis J, MohanKumar PS, MohanKumar SM. Lipopolysaccharide stimulates norepinephrine efflux from the rat hypothalamus in vitro: blockade by soluble IL-1 receptor. Neurosci Lett 2001; 308: 71-4.
47. Cichy J, Rose-John S, Pryjma J, Travis J. Effect of soluble interleukin-6 receptor on interleukin-6 synthesis in human skin fibroblasts. Biochem Biophys Res Commun 1996; 227: 318-21.
48. Klouche M, Bhakdi S, Hemmes M, Rose-John S. Novel path to activation of vascular smooth muscle cells: up-regulation of gp130 creates an autocrine activation loop by IL-6 and its soluble receptor. J Immunol 1999; 163: 4583-9.
49. Van Wagoner NJ, Oh JW, Repovic P, Benveniste EN. Interleukin-6 (IL-6) production by astrocytes: autocrine regulation by IL-6 and the soluble IL-6 receptor. J Neurosci 1999; 19: 5236-44.
50. Modur V, Li Y, Zimmerman GA, Prescott SM, McIntyre TM. Retrograde inflammatory signaling from neutrophils to endothelial cells by soluble interleukin-6 receptor alpha. J Clin Invest 1997; 100: 2752-6.
51. Aschermann S, Lux A, Baerenwaldt A, Biburger M, Nimmerjahn F. The other side of immnoglobulin G: suppressor of inflammation. Clin Exp Immunol 2009; 160: 161-7.
52. Juskewitch JE, Kudsen BE, Platt JL et al. LPS-induced murine systemic inflammation is driven by parenchymal cell activation and exclusively predicted by early MCP-1 plasma levels. Am J Pathol 2012; 180: 32-40.
53. Xiao H, Siddiqui J, Remick DG. Mechanisms of mortality in early and late sepsis. Infect Immun 2006; 74: 5227-35.
54. März P, Cheng J-G, Gadient RA et al. Sympathetic neurons can produce and respond to interleukin-6. Proc Natl Acad Sci USA 1998; 95: 3251-6.
55. März P, Heese K, Dimitriades-Schmutz B, Rose-John S, Otten U. Role of interleukin-6 and soluble IL-6 receptor in region-specific induction of astrocyte differentiation and neurotrophin expression. Glia 1999; 26: 191-200.
56. Chen X, Das R, Komorowski R et al. Blockade of interleukin-6 signaling augments regulatory T-cell reconstitution and attenuates the severity of graft-versus-host disease. Blood 2009; 114: 891-900.
57. Yoshida H, Hashizume M, Mihara M. IL-6 blockade preferentially inhibits Th17 differentiation in collagen-induced arthritis. Rheumatol Int 2011; 31: 127-31.