Lipopolysaccharide induces CD25-psitive, IL-10-producing lymphocytes without secretion of proinflammatory cytokines in the human colon: Low MD-2 mRNA expression in colonic macrophages

Journal of Clinical Immunology

Volumn 24, Issue 1, 2004, Pages 42-52

  Shirai, Yuko ^a   Hashimoto, Masahito ^a   Kato, Rie ^a   Kawamura, Yuki I ^a   Kirikae, Teruo ^a   Yano, Hideaki ^a   Takashima, Junya ^a   Kirihara, Yujiro ^a   Saito, Yukio ^a   Fujino, Masayuki A ^b   Dohi, Taeko ^a  

^a NATIONAL CENTER FOR GLOBAL HEALTH AND MEDICINE   (Japan)

^b UNIVERSITY OF YAMANASHI   (Japan)

Author keywords

Colon; Cytokines; Human; Lipopolysaccharide; Mucosa

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; CD19 ANTIGEN; CD3 ANTIGEN; CD33 ANTIGEN; CD4 ANTIGEN; CD8 ANTIGEN; CYTOKINE; INTERLEUKIN 10; INTERLEUKIN 2 RECEPTOR; INTERLEUKIN 6; MESSENGER RNA; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; BACTEROIDES FRAGILIS; BACTEROIDES VULGATUS; COLON DISEASE; COLON MUCOSA; CONTROLLED STUDY; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNE SYSTEM; INFLAMMATION; INTESTINE FLORA; MACROPHAGE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SALMONELLA;

AGED; ANTIGENS, CD; ANTIGENS, DIFFERENTIATION, MYELOMONOCYTIC; ANTIGENS, SURFACE; BACTEROIDES FRAGILIS; CD4-POSITIVE T-LYMPHOCYTES; COLON; CYTOKINES; HUMANS; INTERLEUKIN-10; LIPOPOLYSACCHARIDES; LYMPHOCYTE ANTIGEN 96; LYMPHOCYTES; MACROPHAGES; RECEPTORS, INTERLEUKIN-2; RNA, MESSENGER; SALMONELLA;

EID: 12144285841     PISSN: 02719142     EISSN: None     Source Type: Journal    
DOI: 10.1023/B:JOCI.0000018062.01980.ba     Document Type: Article

References (50)

1. Elson CO, Sartor RB, Tennyson GS, Riddell RH: Experimental models of inflammatory bowel disease. Gastroenterology 109:1344, 1995
2. Duchmann R, Kaiser I, Hermann E, Mayet W, Ewe K, Meyer Z, Buschenfelde KH: Tolerance exists towards resident intestinal flora but is broken in active inflammatory bowel disease (IBD). Clin Exp Immunol 102:448, 1995
3. Duchmann R, May E, Heike M, Knolle P, Neurath M, Meyer Z, Buschenfelde KH: T cell specificity and cross reactivity towards enterobacteria, bacteroides, bifidobacterium, and antigens from resident intestinal flora in humans. Gut 44:812, 1999
4. Braegger CP, MacDonald TT: Immune mechanisms in chronic inflammatory bowel disease. Ann Allergy 72:135, 1994
5. Simon GL, Gorbach SL: Intestinal flora in health and disease. Gastroenterology 86:174, 1984
6. Onderdonk AB, Cisneros RL, Bronson RT: Enhancement of experimental ulcerative colitis by immunization with Bacteroides vulgatus. Infect Immun 42:783, 1983
7. Onderdonk AB, Bronson R, Cisneros R: Comparison of Bacteroides vulgatus strains in the enhancement of experimental ulcerative colitis. Infect Immun 55:835, 1987
8. Sellon RK, Tonkonogy S, Schultz M, Dieleman LA, Grenther W, Balish E, Rennick DM, Sartor RB: Resident enteric bacteria are necessary for development of spontaneous colitis and immune system activation in interleukin-10-deficient mice. Infect Immun 66:5224, 1998
9. Rath HC, Wilson KH, Sartor RB: Differential induction of colitis and gastritis in HLA-B27 transgenic rats selectively colonized with Bacteroides vulgatus or Escherichia coli. Infect Immun 67:2969, 1999
10. Kishi D, Takahashi I, Kai Y, Tamagawa H, Iijima H, Obunai S, Nezu R, Ito T, Matsuda H, Kiyono H: Alteration of V beta usage and cytokine production of CD4+ TCR beta beta homodimer T cells by elimination of Bacteroides vulgatus prevents colitis in TCR alpha-chain-deficient mice. J Immunol 165:5891, 2000
11. Ursing B, Aim T, Barany F, Bergelin I, Ganrot-Norlin K, Hoevels J, Huitfeldt B, Jarnerot G, Krause U, Krook A, Lindstrom B, Nordle O, Rosen A: A comparative study of metronidazole and sulfasalazine for active Crohn's disease: The cooperative Crohn's disease study in Sweden. II. Result. Gastroenterology 83:550, 1982
12. Bamba T, Matsuda H, Endo M, Fujiyama Y: The pathogenic role of Bacteroides vulgatus in patients with ulcerative colitis. J Gastroenterol 8:45, 1995
13. Tobias PS, Soldau K, Ulevitch RJ: Isolation of a lipopolysaccharide- binding acute phase reactant from rabbit serum. J Exp Med 164:777, 1986
14. Ozinsky A, Underhill DM, Fontenot JD, Hajjar AM, Smith KD, Wilson CB, Schroeder L, Aderem A: The repertoire for pattern recognition of pathogens by the innate immune system is defined by cooperation between toll-like receptors. Proc Natl Acad Sci USA 97:13766, 2000
15. Shimazu R, Akashi S, Ogata H, Nagai Y, Fukudome K, Miyake K, Kimoto M: MD-2, a molecule that confers lipopolysaccharide responsiveness on Toll-like receptor 4. J Exp Med 189:1777, 1999
16. Ortega-Cava CF, Ishihara S, Rumi MA, Kawashima K, Ishimura N, Kazumori H, Udagawa J, Kadowaki Y, Kinoshita Y: Strategic compartmentalization of toll-like receptor4 in the mouse gut. J Immunol 170:3977, 2003
17. Hornef MW, Frisan T, Vandewalle A, Normark S, Richter-Dahlfors A: Toll-like receptor 4 resides in the Golgi apparatus and colocalizes with internalized lipopolysaccharide in intestinal epithelial cells. J Exp Med 195:559, 2002
18. Hashimoto M, Kirikae F, Dohi T, Adachi S, Kusumoto S, Suda Y, Fujita T, Naoki H, Kirikae T: Structural study on lipid A and the O-specific polysaccharide of the lipopolysaccharide from a clinical isolate of Bacteroides vulgatus from a patient with Crohn's disease. Eur J Biochem 269:3715, 2002
19. Bull DM, Bookman MA: Isolation and functional characterization of human intestinal mucosal lymphoid cells. J Clin Invest 59:966, 1977
20. Burdin N, Peronne C, Banchereau J, Rousset F: Epstein-Barr virus transformation induces B lymphocytes to produce human interleukin 10. J Exp Med 177:295, 1993
21. Zarember KA, Godowski PJ: Tissue expression of human Toll-like receptors and differential regulation of Toll-like receptor mRNAs in leukocytes in response to microbes, their products, and cytokines. J Immunol 168:554, 2002
22. Smith PD, Smythies LE, Mosteller-Barnum M, Sibley DA, Russell MW, Merger M, Sellers MT, Orenstein JM, Shimada T, Graham MF, Kubagawa H: Intestinal macrophages lack CD14 and CD89 and consequently are down-regulated for LPS-and IgA-mediated activities. J Immunol 167:2651, 2001
23. Hausmann M, Kiessling S, Mestermann S, Webb G, Spottl T, Andus T, Scholmerich J, Herfarth H, Ray K, Falk W, Rogler G: Toll-like receptors 2 and 4 are up-regulated during intestinal inflammation. Gastroenterology 122:1987, 2002
24. Abreu MT, Arnold ET, Thomas LS, Gonsky R, Zhou Y, Hu B, Arditi M: TLR4 and MD-2 expression is regulated by immune-mediated signals in human intestinal epithelial cells. J Biol Chem 277:20431, 2002
25. Fontenot JD, Gavin MA, Rudensky AY: Foxp3 programs the development and function of CD4+ CD25+ regulatory T cells. Nat Immunol 4:330, 2003
26. Hori S, Nomura T, Sakaguchi S: Control of regulatory T cell development by the transcription factor Foxp3. Science 299:1057, 2003
27. Schilling D, Thomas K, Nixdorff K, Vogel SN, Fenton MJ: Toll-like receptor 4 and Toll-IL-1 receptor domain-containing adapter protein (TIRAP)/myeIoid differentiation protein 88 adapter-like (Mal) contribute to maximal IL-6 expression in macrophages. J Immunol 169:5874, 2002
28. Nagai Y, Akashi S, Nagafuku M, Ogata M, Iwakura Y, Akira S, Kitamura T, Kosugi A, Kimoto M, Miyake K: Essential role of MD-2 in LPS responsiveness and TLR4 distribution. Nat Immunol 3:667, 2002
29. Hajjar AM, Ernst RK, Tsai JH, Wilson CB, Miller SI: Human Toll-like receptor 4 recognizes host-specific LPS modifications. Nat Immunol 3:354, 2002
30. Jotwani R, Tanaka Y, Watanabe K, Tanaka-Bandoh K, Kato N, Ueno K: Comparison of cytokine induction by lipopolysaccharide of Bacteroides fragilis with Salmonella typhimurium in mice. Microbiol Immunol 38:763, 1994
31. de Waal Malefyt R, Abrams J, Bennett B, Figdor CG, de Vries JE: Interleukin 10(IL-10) inhibits cytokine synthesis by human monocytes: an autoregulatory role of IL-10 produced by monocytes. J Exp Med 174:1209, 1991
32. Wang JE, Jorgensen PF, AImlof M, Thiemermann C, Foster SJ, Aasen AO, Solberg R: Peptidoglycan and lipoteichoic acid from Staphylococcus aureus induce tumor necrosis factor alpha, interleukin 6 (IL-6), and IL-10 production in both T cells and monocytes in a human whole blood model. Infect Immun 68:3965, 2000
33. Hoshino K, Takeuchi O, Kawai T, Sanjo H, Ogawa T, Takeda Y, Takeda K, Akira S: Cutting edge: Toll-like receptor 4 (TLR4)-deficient mice are hyporesponsive to lipopolysaccharide: evidence for TLR4 as the Lps gene product. J Immunol 162:3749, 1999
34. Anderson CF, Mosser DM: Cutting edge: biasing immune responses by directing antigen to macrophage Fc gamma receptors. Journal of Immunology. 168:3697, 2002
35. Gerber JS, Mosser DM: Reversing lipopolysaccharide toxicity by ligating the macrophage Fc gamma receptors. J Immunol 166:6861, 2001
36. West MA, Heagy W: Endotoxin tolerance: A review. Crit Care Med 30:564, 2002
37. Dickensheets HL, Freeman SL, Smith MF, Donnelly RP: Interleukin-10 upregulates tumor necrosis factor receptor type-II (p75) gene expression in endotoxin-stimulated human monocytes. Blood 90:4162, 1997
38. Frankenberger M, Pechumer H, Ziegler-Heitbrock HW: Interleukin-10 is upregulated in LPS tolerance. J Inflamm 45:56, 1995
39. Wolk K, Docke WD, von Baehr V, Volk HD, Sabat R: Impaired antigen presentation by human monocytes during endotoxin tolerance. Blood 96:218, 2000
40. Sfeir T, Saha DC, Astiz M, Rackow EC: Role of interleukin-10 in monocyte hyporesponsiveness associated with septic shock. Crit Care Med 29:129, 2001
41. Wittmann M, Larsson VA, Schmidt P, Begemann G, Kapp A, Werfel T: Suppression of interleukin-12 production by human monocytes after preincubation with lipopolysaccharide. Blood 94:1717, 1999
42. Nomura F, Akashi S, Sakao Y, Sato S, Kawai T, Matsumoto M, Nakanishi K, Kimoto M, Miyake K, Takeda K, Akira S: Cutting edge: Endotoxin tolerance in mouse peritoneal macrophages correlates with down-regulation of surface toll-like receptor 4 expression. J Immunol 164:3476, 2000
43. Medvedev AE, Henneke P, Schromm A, Lien E, Ingalls R, Fenton MJ, Golenbock DT, Vogel SN: Induction of tolerance to lipopolysaccharide and mycobacterial components in Chinese hamster ovary/CD14 cells is not affected by overexpression of Toll-like receptors 2 or 4. J Immunol 167:2257, 2001
44. Medvedev AE, Lentschat A, Wahl LM, Golenbock DT, Vogel SN: Dysregulation of LPS-induced Toll-like receptor 4-MyD88 complex formation and IL-1 receptor-associated kinase 1 activation in endotoxin-tolerant cells. J Immunol 169:5209, 2002
45. Sakaguchi S, Sakaguchi N, Asano M, Itoh M, Toda M: Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor alpha-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J Immunol 155:1151, 1995
46. Kullberg MC, Jankovic D, Gorelick PL, Caspar P, Letterio JJ, Cheever AW, Sher A: Bacteria-triggered CD4(+) T regulatory cells suppress Helicobacter hepaticus-induced colitis. J Exp Med 196:505, 2002
47. Svand Rietdijk WF, Ype De Jong, Ana Abadia-Molina, Kareem Clerke, Ryan Sartor, Cox Terhorst: CD4+CD25+ regulatory T cells originating from germ free mice have inpaired suppressive abilities. Gastroenterology A, 2002
48. Mattern T, Thanhauser A, Reiling N, et al.: Endotoxin and lipid A stimulate proliferation of human T cells in the presence of autologous monocytes. J Immunol 153:2996, 1994
49. Mattern T, Flad HD, Ulmer AJ: Stimulation of human T lymphocytes by lipopolysaccaride (LPS) in the presence of autologous and heterologous monocytes. Prog Clin Biol Res 397:243, 1998
50. Mattern T, Flad HD, Brade L, Rietschel ET, Ulmer AJ: Stimulation of human T lymphocytes by LPS is MHC unrestricted, but strongly dependent on B7 interactions. J Immunol 160:3412, 1998