Immunobiology of intestinal eosinophils - A dogma in the changing?

Journal of Innate Immunity

Volumn 3, Issue 6, 2011, Pages 565-576

  Svensson Frej, Marcus ^a  

^a LUND UNIVERSITY   (Sweden)

Author keywords

Antiparasite function; Eosinophils; Gastrointestinal tract; Inflammation

Indexed keywords

ADAPTIVE IMMUNITY; ENTERITIS; EOSINOPHIL; HOMEOSTASIS; IMMUNOBIOLOGY; INTESTINE MUCOSA; PRIORITY JOURNAL; REVIEW;

ADAPTIVE IMMUNITY; ANIMALS; CELL MOVEMENT; EOSINOPHILS; HOMEOSTASIS; HUMANS; IMMUNITY, INNATE; INFECTION; INFLAMMATION; INTESTINAL MUCOSA;

EID: 80054961279     PISSN: 1662811X     EISSN: 16628128     Source Type: Journal    
DOI: 10.1159/000328799     Document Type: Review

References (68)

1. Gao JL, Sen AI, Kitaura M, Yoshie O, Rothenberg ME, Murphy PM, Luster AD: Identification of a mouse eosinophil receptor for the CC chemokine eotaxin. Biochem Biophys Res Commun 1996;223:679-784.
2. Lloyd CM, Delaney T, Nguyen T, Tian J, Martinez AC, Coyle AJ, Gutierrez-Ramos JC: CC chemokine receptor (CCR)3/eotaxin is followed by CCR4/monocyte-derived chemokine in mediating pulmonary T helper lymphocyte type 2 recruitment after serial antigen challenge in vivo. JExp Med 2000;191:265-274.
3. 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. (Pubitemid 39255997)
4. Stevens WW, Kim TS, Pujanauski LM, Hao X, Braciale TJ: Detection and quantitation of eosinophils in the murine respiratory tract by flow cytometry. J Immunol Methods 2007;327:63-74. (Pubitemid 47444310)
5. Zhang M, Angata T, Cho JY, Miller M, Broide DH, Varki A: Defining the in vivo function of Siglec-F, a CD33-related Siglec expressed on mouse eosinophils. Blood 2007;109:4280-4287. (Pubitemid 46743394)
6. Carlens J, Wahl B, Ballmaier M, Bulfone-Paus S, Forster R, Pabst O: Common gamma-chain-dependent signals confer selective survival of eosinophils in the murine small intestine. J Immunol 2009;183:5600-5607.
7. Uematsu S, Fujimoto K, Jang MH, Yang BG, Jung YJ, Nishiyama M, Sato S, Tsujimura T, Yamamoto M, Yokota Y, Kiyono H, Miyasaka M, Ishii KJ, Akira S: Regulation of humoral and cellular gut immunity by lamina propria dendritic cells expressing Toll-like receptor 5. Nat Immunol 2008;9:769-776. (Pubitemid 351859160)
8. Mowat AM, Bain CC: News & highlights. Mucosal Immunol 2010;3:420-421.
9. Voehringer D, van Rooijen N, Locksley RM: Eosinophils develop in distinct stages and are recruited to peripheral sites by alternatively activated macrophages. J Leukoc Biol 2007;81:1434-1444. (Pubitemid 46827966)
10. Svensson M, Bell L, Little MC, DeSchoolmeester M, Locksley RM, Else KJ: Accumulation of eosinophils in intestine-draining mesenteric lymph nodes occurs after Trichuris muris infection. Parasite Immunol 2011;33:1-11.
11. Anwar AR, Moqbel R, Walsh GM, Kay AB, Wardlaw AJ: Adhesion to fibronectin prolongs eosinophil survival. J Exp Med 1993;177:839-843. (Pubitemid 23104295)
12. Matthews AN, Friend DS, Zimmermann N, Sarafi MN, Luster AD, Pearlman E, Wert SE, Rothenberg ME: Eotaxin is required for the baseline level of tissue eosinophils. Proc Natl Acad Sci USA 1998;95:6273-6278. (Pubitemid 28249002)
13. Mishra A, Hogan SP, Lee JJ, Foster PS, Rothenberg ME: Fundamental signals that regulate eosinophil homing to the gastrointestinal tract. J Clin Invest 1999;103:1719-1727. (Pubitemid 29534366)
14. Humbles AA, Lu B, Friend DS, Okinaga S, Lora J, Al-Garawi A, Martin TR, Gerard NP, Gerard C: The murine CCR3 receptor regulates both the role of eosinophils and mast cells in allergen-induced airway inflammation and hyperresponsiveness. Proc Natl Acad Sci USA 2002;99:1479-1484. (Pubitemid 34136518)
15. 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.
16. Blanchard C, Durual S, Estienne M, Emami S, Vasseur S, Cuber JC: Eotaxin-3/CCL26 gene expression in intestinal epithelial cells is up-regulated by interleukin-4 and interleukin-13 via the signal transducer and activator of transcription 6. Int J Biochem Cell Biol 2005;37:2559-2573. (Pubitemid 41400325)
17. Neilsen CV, Bryce PJ: Interleukin-13 directly promotes oesophagus production of CCL11 and CCL24 and the migration of eosinophils. Clin Exp Allergy 2010;40:427-434.
18. Hogan SP, Mishra A, Brandt EB, Foster PS, Rothenberg ME: A critical role for eotaxin in experimental oral antigen-induced eosinophilic gastrointestinal allergy. Proc Natl Acad Sci USA 2000;97:6681-6686. (Pubitemid 30412774)
19. Dixon H, Blanchard C, Deschoolmeester ML, Yuill NC, Christie JW, Rothenberg ME, Else KJ: The role of Th2 cytokines, chemokines and parasite products in eosinophil recruitment to the gastrointestinal mucosa during helminth infection. Eur J Immunol 2006;36:1753-1763. (Pubitemid 44089042)
20. Gurish MF, Humbles A, Tao H, Finkelstein S, Boyce JA, Gerard C, Friend DS, Austen KF: CCR3 is required for tissue eosinophilia and larval cytotoxicity after infection with Trichinella spiralis. J Immunol 2002;168:5730-5736. (Pubitemid 34556157)
21. Brandt EB, Zimmermann N, Muntel EE, Yamada Y, Pope SM, Mishra A, Hogan SP, Rothenberg ME: The alpha4bbeta7-integrin is dynamically expressed on murine eosinophils and involved in eosinophil trafficking to the intestine. Clin Exp Allergy 2006;36:543-553.
22. Mishra A, Hogan SP, Brandt EB, Wagner N, Crossman MW, Foster PS, Rothenberg ME: Enterocyte expression of the eotaxin and interleukin-5 transgenes induces compartmentalized dysregulation of eosinophil trafficking. J Biol Chem 2002;277:4406-4412. (Pubitemid 34968707)
23. Forbes E, Hulett M, Ahrens R, Wagner N, Smart V, Matthaei KI, Brandt EB, Dent LA, Rothenberg ME, Tang M, Foster PS, Hogan SP: ICAM-1-dependent pathways regulate colonic eosinophilic inflammation. J Leukoc Biol 2006;80:330-341. (Pubitemid 44835506)
24. Artis D, Humphreys NE, Potten CS, Wagner N, Muller W, McDermott JR, Grencis RK, Else KJ: Beta7 integrin-deficient mice: delayed leukocyte recruitment and attenuated protective immunity in the small intestine during enteric helminth infection. Eur J Immunol 2000;30:1656-1664. (Pubitemid 30342808)
25. Bell LV, Else KJ: Mechanisms of leucocyte recruitment to the inflamed large intestine: redundancy in integrin and addressin usage. Parasite Immunol 2008;30:163-170. (Pubitemid 351171241)
26. Ohnmacht C, Pullner A, van Rooijen N, Voehringer D: Analysis of eosinophil turnover in vivo reveals their active recruitment to and prolonged survival in the peritoneal cavity. J Immunol 2007;179:4766-4774.
27. Friend DS, Gurish MF, Austen KF, Hunt J, Stevens RL: Senescent jejunal mast cells and eosinophils in the mouse preferentially translocate to the spleen and draining lymph node, respectively, during the recovery phase of helminth infection. J Immunol 2000;165:344-352. (Pubitemid 30429526)
28. Mishra A, Hogan SP, Brandt EB, Rothenberg ME: Peyer's patch eosinophils: identification, characterization, and regulation by mucosal allergen exposure, interleukin-5, and eotaxin. Blood 2000;96:1538-1544. (Pubitemid 30658488)
29. Dent LA, Strath M, Mellor AL, Sanderson CJ: Eosinophilia in transgenic mice expressing interleukin 5. J Exp Med 1990;172:1425-1431. (Pubitemid 20366218)
30. Yu C, Cantor AB, Yang H, Browne C, Wells RA, Fujiwara Y, Orkin SH: Targeted deletion of a high-affinity GATA-binding site in the GATA-1 promoter leads to selective loss of the eosinophil lineage in vivo. J Exp Med 2002;195:1387-1395. (Pubitemid 34602816)
31. Lee JJ, Dimina D, Macias MP, Ochkur SI, McGarry MP, O'Neill KR, Protheroe C, Pero R, Nguyen T, Cormier SA, Lenkiewicz E, Colbert D, Rinaldi L, Ackerman SJ, Irvin CG, Lee NA: Defining a link with asthma in mice congenitally deficient in eosinophils. Science 2004;305:1773-1776. (Pubitemid 39249644)
32. Klion AD, Nutman TB: The role of eosinophils in host defense against helminth parasites. J Allergy Clin Immunol 2004;113:30-37. (Pubitemid 38096158)
33. Butterworth AE: Cell-mediated damage to helminths. Adv Parasitol 1984;23:143-235.
34. Gleich GJ, Frigas E, Loegering DA, Wassom DL, Steinmuller D: Cytotoxic properties of the eosinophil major basic protein. J Immunol 1979;123:2925-2927. (Pubitemid 10202545)
35. Behnke J, Harris PD: Heligmosomoides bakeri : a new name for an old worm? Trends Parasitol 2010;26:524-529.
36. Herndon FJ, Kayes SG: Depletion of eosinophils by anti-IL-5 monoclonal antibody treatment of mice infected with Trichinella spiralis does not alter parasite burden or immunologic resistance to reinfection. J Immunol 1992;149:3642-3647.
37. Betts CJ, Else KJ: Mast cells, eosinophils and antibody-mediated cellular cytotoxicity are not critical in resistance to Trichuris muris. Parasite Immunol 1999;21:45-52. (Pubitemid 29050399)
38. Urban JF Jr, Katona IM, Paul WE, Finkelman FD: Interleukin 4 is important in protective immunity to a gastrointestinal nematode infection in mice. Proc Natl Acad Sci USA 1991;88:5513-5517. (Pubitemid 21914775)
39. Coffman RL, Seymour BW, Hudak S, Jackson J, Rennick D: Antibody to interleukin-5 inhibits helminth-induced eosinophilia in mice. Science 1989;245:308-310. (Pubitemid 19196651)
40. Watanabe K, Sasaki O, Hamano S, Kishihara K, Nomoto K, Tada I, Aoki Y: Strongyloides ratti : the role of interleukin-5 in protection against tissue migrating larvae and intestinal adult worms. J Helminthol 2003;77:355-361. (Pubitemid 37463214)
41. Korenaga M, Hitoshi Y, Takatsu K, Tada I: Regulatory effect of anti-interleukin-5 monoclonal antibody on intestinal worm burden in a primary infection with Strongyloides venezuelensis in mice. Int J Parasitol 1994;24:951-957.
42. Vallance BA, Blennerhassett PA, Deng Y, Matthaei KI, Young IG, Collins SM: IL-5 contributes to worm expulsion and muscle hypercontractility in a primary T. spiralis infection. Am J Physiol 1999;277:G400-G408. (Pubitemid 29415068)
43. Ovington KS, McKie K, Matthaei KI, Young IG, Behm CA: Regulation of primary Strongyloides ratti infections in mice: a role for interleukin-5. Immunol 1998;95:488-493. (Pubitemid 28505708)
44. Knott ML, Matthaei KI, Foster PS, Dent LA: The roles of eotaxin and the STAT6 signalling pathway in eosinophil recruitment and host resistance to the nematodes Nippostrongylus brasiliensis and Heligmosomoides bakeri. Mol Immunol 2009;46:2714-2722.
45. Fabre V, Beiting DP, Bliss SK, Gebreselassie NG, Gagliardo LF, Lee NA, Lee JJ, Appleton JA: Eosinophil deficiency compromises parasite survival in chronic nematode infection. J Immunol 2009;182:1577-1583.
46. Knott ML, Matthaei KI, Giacomin PR, Wang H, Foster PS, Dent LA: Impaired resistance in early secondary Nippostrongylus brasiliensis infections in mice with defective eosinophilopoeisis. Int J Parasitol 2007;37:1367-1378. (Pubitemid 47285107)
47. Voehringer D, Reese TA, Huang X, Shinkai K, Locksley RM: Type 2 immunity is controlled by IL-4/IL-13 expression in hematopoietic non-eosinophil cells of the innate immune system. J Exp Med 2006;203:1435-1446. (Pubitemid 43877606)
48. Hokibara S, Takamoto M, Tominaga A, Takatsu K, Sugane K: Marked eosinophilia in interleukin-5 transgenic mice fails to prevent Trichinella spiralis infection. J Parasitol 1997;83:1186-1189. (Pubitemid 28006618)
49. Dent LA, Daly CM, Mayrhofer G, Zimmerman T, Hallett A, Bignold LP, Creaney J, Parsons JC: Interleukin-5 transgenic mice show enhanced resistance to primary infections with Nippostrongylus brasiliensis but not primary infections with Toxocara canis. InfectImmun 1999;67:989-993. (Pubitemid 29059249)
50. El-Malky M, Maruyama H, Hirabayashi Y, Shimada S, Yoshida A, Amano T, Tominaga A, Takatsu K, Ohta N: Intraepithelial infiltration of eosinophils and their contribution to the elimination of adult intestinal nematode, Strongyloides venezuelensis in mice. ParasitolInt 2003;52:71-79. (Pubitemid 36110523)
51. Vallance BA, Matthaei KI, Sanovic S, Young IG, Collins SM: Interleukin-5 deficient mice exhibit impaired host defence against challenge Trichinella spiralis infections. Parasite Immunol 2000;22:487-492.
52. Yousefi S, Gold JA, Andina N, Lee JJ, Kelly AM, Kozlowski E, Schmid I, Straumann A, Reichenbach J, Gleich GJ, Simon HU: Catapult-like release of mitochondrial DNA by eosinophils contributes to antibacterial defense. Nat Med 2008;14:949-953.
53. Rothenberg ME: Eosinophilic gastrointestinal disorders (EGID). J Allergy Clin Immunol 2004;113:11-28, quiz 29.
54. 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.
55. Hogan SP, Mishra A, Brandt EB, Royalty MP, Pope SM, Zimmermann N, Foster PS, Rothenberg ME: A pathological function for eotaxin and eosinophils in eosinophilic gastrointestinal inflammation. Nat Immunol 2001;2:353-360.
56. Garrett JK, Jameson SC, Thomson B, Collins MH, Wagoner LE, Freese DK, Beck LA, Boyce JA, Filipovich AH, Villanueva JM, Sutton SA, Assa'ad AH, Rothenberg ME: Anti-interleukin-5 (mepolizumab) therapy for hypereosinophilic syndromes. J Allergy Clin Immunol 2004;113:115-119. (Pubitemid 38096170)
57. Blanchard C, Rothenberg ME: Biology of the eosinophil. Adv Immunol 2009;101:81-121.
58. Yamada T, Tani Y, Nakanishi H, Taguchi R, Arita M, Arai H: Eosinophils promote resolution of acute peritonitis by producing proresolving mediators in mice. FASEB J 2011;25:561-568.
59. Lee JJ, Jacobsen EA, McGarry MP, Schleimer RP, Lee NA: Eosinophils in health and disease: the LIAR hypothesis. Clin Exp Allergy 2010;40:563-575.
60. Furuta GT, Nieuwenhuis EE, Karhausen J, Gleich G, Blumberg RS, Lee JJ, Ackerman SJ: Eosinophils alter colonic epithelial barrier function: role for major basic protein. Am J Physiol Gastrointest Liver Physiol 2005;289:G890-G897. (Pubitemid 41532582)
61. Shi HZ: Eosinophils function as antigen-presenting cells. J Leukoc Biol 2004;76:520-527.
62. van Rijt LS, Vos N, Hijdra D, de Vries VC, Hoogsteden HC, Lambrecht BN: Airway eosinophils accumulate in the mediastinal lymph nodes but lack antigen-presenting potential for naive T cells. J Immunol 2003;171:3372-3378.
63. Wang HB, Ghiran I, Matthaei K, Weller PF: Airway eosinophils: allergic inflammation recruited professional antigen-presenting cells. J Immunol 2007;179:7585-7592.
64. Yang D, Chen Q, Su SB, Zhang P, Kurosaka K, Caspi RR, Michalek SM, Rosenberg HF, Zhang N, Oppenheim JJ: Eosinophil-derived neurotoxin acts as an alarmin to activate the TLR2-MyD88 signal pathway in dendritic cells and enhances Th2 immune responses. J Exp Med 2008;205:79-90. (Pubitemid 351185717)
65. Chu VT, Frohlich A, Steinhauser G, Scheel T, Roch T, Fillatreau S, Lee JJ, Lohning M, Berek C: Eosinophils are required for the maintenance of plasma cells in the bone marrow. Nat Immunol 2011;12:151-159.
66. Wang HB, Weller PF: Pivotal advance: eosinophils mediate early alum adjuvant-elicited B cell priming and IgM production. J Leukoc Biol 2008;83:817-821.
67. Cerutti A: Location, location, location: Bcell differentiation in the gut lamina propria. Mucosal Immunol 2008;1:8-10.
68. Macpherson AJ, McCoy KD, Johansen FE, Brandtzaeg P: The immune geography of IgA induction and function. Mucosal Immunol 2008;1:11-22.