Tissue eosinophilia in a mouse model of colitis is highly dependent on TLR2 and independent of mast cells

American Journal of Pathology

Volumn 178, Issue 1, 2011, Pages 150-160

  Albert, Eric J ^a   Duplisea, Jon ^a   Dawicki, Wojciech ^a   Haidl, Ian D ^a   Marshall, Jean S ^a  

^a DALHOUSIE UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

DEXTRAN SULFATE; EOTAXIN; FSL 1; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR AGONIST; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; BONE MARROW CELL; CELL DIFFERENTIATION; COLITIS; CONTROLLED STUDY; DISEASE ASSOCIATION; ENZYME LINKED IMMUNOSORBENT ASSAY; EOSINOPHIL COUNT; EOSINOPHILIA; LEUKOCYTE COUNT; MAST CELL; MOUSE; NONHUMAN; OUTCOME ASSESSMENT; PERITONEAL CAVITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; WEIGHT REDUCTION;

EID: 79251529194     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2010.11.041     Document Type: Article

References (61)

1. Xavier RJ, Podolsky DK: Unravelling the pathogenesis of inflammatory bowel disease. Nature 2007, 448:427-434 (Pubitemid 47123518)
2. Rothenberg ME, Mishra A, Brandt EB, Hogan SP: Gastrointestinal eosinophils. Immunol Rev 2001, 179:139-155
3. King T, Biddle W, Bhatia P, Moore J, Miner PB Jr: Colonic mucosal mast cell distribution at line of demarcation of active ulcerative colitis. Dig Dis Sci 1992, 37:490-495
4. Nishida Y, Murase K, Isomoto H, Furusu H, Mizuta Y, Riddell RH, Kohno S: Different distribution of mast cells and macrophages in colonic mucosa of patients with collagenous colitis and inflammatory bowel disease. Hepatogastroenterology 2002, 49:678-682 (Pubitemid 34615326)
5. Weller PF: Eosinophils: structure and functions. Curr Opin Immunol 1994, 6:85-90
6. Gleich GJ, Loegering DA: Immunobiology of eosinophils. Annu Rev Immunol 1984, 2:429-459
7. Rothenberg ME, Hogan SP: The eosinophil. Annu Rev Immunol 2006, 24:147-174
8. Lopez AF, Sanderson CJ, Gamble JR, Campbell HD, Young IG, Vadas MA: Recombinant human interleukin 5 is a selective activator of human eosinophil function. J Exp Med 1988, 167:219-224
9. Collins PD, Marleau S, Griffiths-Johnson DA, Jose PJ, Williams TJ: Cooperation between interleukin-5 and the chemokine eotaxin to induce eosinophil accumulation in vivo. J Exp Med 1995, 182:1169-1174
10. Dent LA, Strath M, Mellor AL, Sanderson CJ: Eosinophilia in transgenic mice expressing interleukin 5. J Exp Med 1990, 172:1425-1431 (Pubitemid 20366218)
11. Rothenberg ME, Pomerantz JL, Owen WF Jr, Avraham S, Soberman RJ, Austen KF, Stevens RL: Characterization of a human eosinophil proteoglycan, and augmentation of its biosynthesis and size by interleukin 3, interleukin 5, and granulocyte/macrophage colony stimulating factor. J Biol Chem 1988, 263:13901-13908
12. Koga M, Fujiwara M, Hotta N, Matsubara T, Suzuki E, Furukawa S: MBP deposition in eosinophilic gastroenteritis. Allergy 2000, 55:985-986
13. Bischoff SC, Mayer J, Nguyen QT, Stolte M, Manns MP: Immunnohistological assessment of intestinal eosinophil activation in patients with eosinophilic gastroenteritis and inflammatory bowel disease. Am J Gastroenterol 1999, 94:3521-3529
14. Carvalho AT, Elia CC, de Souza HS, Elias PR, Pontes EL, Lukashok HP, de Freitas FC, Lapa e Silva JR: Immunohistochemical study of intestinal eosinophils in inflammatory bowel disease. J Clin Gastroenterol 2003, 36:120-125
15. Bischoff SC, Wedemeyer J, Herrmann A, Meier PN, Trautwein C, Cetin Y, Maschek H, Stolte M, Gebel M, Manns MP: Quantitative assessment of intestinal eosinophils and mast cells in inflammatory bowel disease. Histopathology 1996, 28:1-13
16. Forbes E, Murase T, Yang M, Matthaei KI, Lee JJ, Lee NA, Foster PS, Hogan SP: Immunopathogenesis of experimental ulcerative colitis is mediated by eosinophil peroxidase. J Immunol 2004, 172:5664-5675
17. Stevceva L, Pavli P, Husband A, Matthaei KI, Young IG, Doe WF: Eosinophilia is attenuated in experimental colitis induced in IL-5 deficient mice. Genes Immun 2000, 1:213-218
18. Ahrens R, Waddell A, Seidu L, Blanchard C, Carey R, Forbes E, Lampinen M, Wilson T, Cohen E, Stringer K, Ballard E, Munitz A, Xu H, Lee N, Lee JJ, Rothenberg ME, Denson L, Hogan SP: Intestinal macrophage/epithelial cell-derived CCL11/eotaxin-1 mediates eosinophil recruitment and function in pediatric ulcerative colitis. J Immunol 2008, 181:7390-7399
19. Szebeni B, Veres G, Dezsofi A, Rusai K, Vannay A, Mraz M, Majorova E, Arató A: Increased expression of Toll-like receptor (TLR) 2 and TLR4 in the colonic mucosa of children with inflammatory bowel disease. Clin Exp Immunol 2008, 151:34-41
20. Hart AL, AL-Hassi HO, Rigby RJ, Bell SJ, Emmanuel AV, Knight SC, Kamm MA, Stagg AJ: Characteristics of intestinal dendritic cells in inflammatory bowel diseases. Gastroenterology 2005, 129:50-65
21. Cario E, Rosenberg IM, Brandwein SL, Beck PL, Reinecker HC, Podolsky DK: Lipopolysaccharide activates distinct signaling pathways in intestinal epithelial cell lines expressing Toll-like receptors. J Immunol 2000, 164:966-972
22. Abreu MT, Fukata M, Arditi M: TLR signaling in the gut in health and disease. J Immunol 2005, 174:4453-4460
23. Fukata M, Michelsen KS, Eri R, Thomas LS, Hu B, Lukasek K, Nast CC, Lechago J, Xu R, Naiki Y, Soliman A, Arditi M, Abreu MT: Toll-like receptor-4 is required for intestinal response to epithelial injury and limiting bacterial translocation in a murine model of acute colitis. Am J Physiol Gastrointest Liver Physiol 2005, 288:G1055-G1065
24. Rhee SH, Keates AC, Moyer MP, Pothoulakis C: MEK is a key modulator for TLR5-induced interleukin-8 and MIP3alpha gene expression in non-transformed human colonic epithelial cells. J Biol Chem 2004, 279:25179-25188
25. Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, Edberg S, Medzhitov R: Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 2004, 118:229-241 (Pubitemid 38962578)
26. Albert EJ, Marshall JS: Aging in the absence of TLR2 is associated with reduced IFN-gamma responses in the large intestine and increased severity of induced colitis. J Leukoc Biol 2008, 83:833-842
27. Cario E, Gerken G, Podolsky DK: Toll-like receptor 2 controls mucosal inflammation by regulating epithelial barrier function. Gastroenterology 2007, 132:1359-1374 (Pubitemid 46627595)
28. D'Avila H, Almeida PE, Roque NR, Castro-Faria-Neto HC, Bozza PT: Toll-like receptor-2-mediated C-C chemokine receptor 3 and eotaxin-driven eosinophil influx induced by Mycobacterium bovis BCG pleurisy. Infect Immun 2007, 75:1507-1511
29. Barrett KE, Metcalfe DD: The mucosal mast cell and its role in gastrointestinal allergic diseases. Clin Rev Allergy 1984, 2:39-53
30. Malaviya R, Ikeda T, Ross E, Abraham SN: Mast cell modulation of neutrophil influx and bacterial clearance at sites of infection through TNF-alpha. Nature 1996, 381:77-80
31. Woodbury RG, Miller HR, Huntley JF, Newlands GF, Palliser AC, Wakelin D: Mucosal mast cells are functionally active during spontaneous expulsion of intestinal nematode infections in rat. Nature 1984, 312:450-452
32. Wei OL, Hilliard A, Kalman D, Sherman M: Mast cells limit systemic bacterial dissemination but not colitis in response to Citrobacter rodentium. Infect Immun 2005, 73:1978-1985
33. Supajatura V, Ushio H, Nakao A, Okumura K, Ra C, Ogawa H: Protective roles of mast cells against enterobacterial infection are mediated by Toll-like receptor 4. J Immunol 2001, 167:2250-2256
34. McDermott JR, Bartram RE, Knight PA, Miller HR, Garrod DR, Grencis RK: Mast cells disrupt epithelial barrier function during enteric nematode infection. Proc Natl Acad Sci USA 2003, 100:7761-7766
35. Fox CC, Lazenby AJ, Moore WC, Yardley JH, Bayless TM, Lichtenstein LM: Enhancement of human intestinal mast cell mediator release in active ulcerative colitis. Gastroenterology 1990, 99:119-124
36. Nolte H, Spjeldnaes N, Kruse A, Windelborg B: Histamine release from gut mast cells from patients with inflammatory bowel diseases. Gut 1990, 31:791-794 (Pubitemid 20233946)
37. Bischoff SC: Role of mast cells in allergic and non-allergic immune responses: comparison of human and murine data. Nat Rev Immunol 2007, 7:93-104
38. Bischoff S, Crowe SE: Gastrointestinal food allergy: new insights into pathophysiology and clinical perspectives. Gastroenterology 2005, 128:1089-1113
39. Theoharides TC, Kempuraj D, Tagen M, Conti P, Kalogeromitros D: Differential release of mast cell mediators and the pathogenesis of inflammation [Erratum appeared in Immunol Rev 2007;219:204]. Immunol Rev 2007, 217:65-78
40. Lorentz A, Schwengberg S, Mierke C, Manns MP, Bischoff SC: Human intestinal mast cells produce IL-5 in vitro upon IgE receptor cross-linking and in vivo in the course of intestinal inflammatory disease. Eur J Immunol 1999, 29:1496-1503
41. Supajatura V, Ushio H, Nakao A, Akira S, Okumura K, Ra C, Ogawa H: Differential responses of mast cell Toll-like receptors 2 and 4 in allergy and innate immunity. J Clin Invest 2002, 109:1351-1359
42. McCurdy JD, Olynych TJ, Maher LH, Marshall JS: Cutting edge: distinct Toll-like receptor 2 activators selectively induce different classes of mediator production from human mast cells. J Immunol 2003, 170:1625-1629
43. Olynych TJ, Jakeman DL, Marshall JS: Fungal zymosan induces leukotriene production by human mast cells through a dectin-1-dependent mechanism. J Allergy Clin Immunol 2006, 118:837-843
44. W-sh/W-sh mice as a model for investigating mast cell biology in vivo. Am J Pathol 2005, 167:835-848
45. Albert EJ, Sommerfeld K, Gophna S, Marshall JS, Gophna U: The gut microbiota of toll-like receptor 2-deficient mice exhibits lineage-specific modifications. Environ Microbiol Rep 2009, 1:65-70
46. Tertian G, Yung YP, Guy-Grand D, Moore MA: Long-term in vitro culture of murine mast cells. I. Description of a growth factor-dependent culture technique. J Immunol 1981, 127:788-794
47. Nakano T, Sonoda T, Hayashi C, Yamatodani A, Kanayama Y, Yamamura T, Asai H, Yonezawa T, Kitamura Y, Galli SJ: Fate of bone marrow-derived cultured mast cells after intracutaneous, intraperitoneal, and intravenous transfer into genetically mast cell-deficient W/Wv mice. Evidence that cultured mast cells can give rise to both connective tissue type and mucosal mast cells. J Exp Med 1985, 162:1025-1043
48. Strobel S, Miller HR, Ferguson A: Human intestinal mucosal mast cells: evaluation of fixation and staining techniques. J Clin Pathol 1981, 34:851-858
49. Zhang JQ, Biedermann B, Nitschke L, Crocker PR: The murine inhibitory receptor mSiglec-E is expressed broadly on cells of the innate immune system whereas mSiglec-F is restricted to eosinophils. Eur J Immunol 2004, 34:1175-1184
50. Tanaka K, Yamagami S, Streilein JW: Evidence that T-helper type 2 cell-derived cytokines and eosinophils contribute to acute rejection of orthotopic corneal xenografts in mice. Transplantation 2005, 79: 1317-1323 (Pubitemid 40734793)
51. Reese TA, Liang HE, Tager AM, Luster AD, Van Rooijen N, Voehringer D, Locksley RM: Chitin induces accumulation in tissue of innate immune cells associated with allergy. Nature 2007, 447:92-96
52. Jeziorska M, Haboubi N, Schofield P, Woolley DE: Distribution and activation of eosinophils in inflammatory bowel disease using an improved immunohistochemical technique. J Pathol 2001, 194:484-492
53. Jacob C, Yang PC, Darmoul D, Amadesi S, Saito T, Cottrell GS, Coelho AM, Singh P, Grady EF, Perdue M, Bunnett NW: Mast cell tryptase controls paracellular permeability of the intestine. Role of protease-activated receptor 2 and beta-arrestins. J Biol Chem 2005, 280:31936-31948
54. Perdue MH, Ramage JK, Burget D, Marshall J, Masson S: Intestinal mucosal injury is associated with mast cell activation and leukotriene generation during Nippostrongylus-induced inflammation in the rat. Dig Dis Sci 1989, 34:724-731
55. Yu LC, Perdue MH: Role of mast cells in intestinal mucosal function: studies in models of hypersensitivity and stress. Immunol Rev 2001, 179:61-73
56. Berin MC, Kiliaan AJ, Yang PC, Groot JA, Kitamura Y, Perdue MH: The influence of mast cells on pathways of transepithelial antigen transport in rat intestine. J Immunol 1998, 161:2561-2566
57. Crowe SE, Luthra GK, Perdue MH: Mast cell mediated ion transport in intestine from patients with and without inflammatory bowel disease. Gut 1997, 41:785-792
58. Yu M, Tsai M, Tam SY, Jones C, Zehnder J, Galli SJ: Mast cells can promote the development of multiple features of chronic asthma in mice. J Clin Invest 2006, 116:1633-1641
59. Mrabet-Dahbi S, Dalpke AH, Niebuhr M, Frey M, Draing C, Brand S, Heeg K, Werfel T, Renz H: The Toll-like receptor 2 R753Q mutation modifies cytokine production and Toll-like receptor expression in atopic dermatitis. J Allergy Clin Immunol 2008, 121:1013-1019
60. Ahmad-Nejad P, Mrabet-Dahbi S, Breuer K, Klotz M, Werfel T, Herz U, Heeg K, Neumaier M, Renz H: The toll-like receptor 2 R753Q polymorphism defines a subgroup of patients with atopic dermatitis having severe phenotype. J Allergy Clin Immunol 2004, 113:565-567
61. Eder W, Klimecki W, Yu L, von Mutius E, Riedler J, Braun-Fahrländer C, Nowak D, Martinez FD; ALEX Study Team: Toll-like receptor 2 as a major gene for asthma in children of European farmers. J Allergy Clin Immunol 2004, 113:482-488 (Pubitemid 38338954)