Intestinal macrophage/epithelial cell-derived CCL11/eotaxin-1 mediates eosinophil recruitment and function in pediatric ulcerative colitis

Journal of Immunology

Volumn 181, Issue 10, 2008, Pages 7390-7399

  Ahrens, Richard ^a   Waddell, Amanda ^a   Seidu, Luqman ^a   Blanchard, Carine ^a   Carey, Rebecca ^a   Forbes, Elizabeth ^a   Lampinen, Maria ^c   Wilson, Tara ^a   Cohen, Elizabeth ^a   Stringer, Keith ^a   Ballard, Edgar ^a   Munitz, Ariel ^a   Xu, Huan ^a   Lee, Nancy ^b   Lee, James J ^b   Rothenberg, Marc E ^a   Denson, Lee ^a   Hogan, Simon P ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^b MAYO CLINIC   (United States)

^c UPPSALA UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

DEXTRAN SULFATE; EOSINOPHIL PEROXIDASE; EOTAXIN; EOTAXIN 2; MESSENGER RNA;

ADOLESCENT; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CHILD; COLON BIOPSY; CONTROLLED STUDY; DISEASE SEVERITY; DNA MICROARRAY; EOSINOPHIL; EPITHELIUM CELL; FEMALE; FLUORESCENCE ACTIVATED CELL SORTING; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; INTESTINE CELL; MACROPHAGE; MAJOR CLINICAL STUDY; MALE; MOUSE; NONHUMAN; NORTHERN BLOTTING; PRESCHOOL CHILD; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SCHOOL CHILD; SIGMOID; ULCERATIVE COLITIS; ANIMAL; BIOSYNTHESIS; COLON; CYTOLOGY; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOLOGY; INTESTINE MUCOSA; METABOLISM; NEUTROPHIL CHEMOTAXIS; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ADOLESCENT; ANIMALS; CHEMOKINE CCL11; CHEMOTAXIS, LEUKOCYTE; CHILD; CHILD, PRESCHOOL; COLITIS, ULCERATIVE; COLON; EOSINOPHILS; EPITHELIAL CELLS; FEMALE; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; IMMUNOHISTOCHEMISTRY; INTESTINAL MUCOSA; MACROPHAGES; MALE; MICE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

EID: 58149179172     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.181.10.7390     Document Type: Article

References (65)

1. Bouma, G., and W. Strober. 2003. The immunological and genetic basis of in- flammatory bowel disease. Nat. Rev. Immunol. 3: 521-533. (Pubitemid 37328672)
2. Walsh, R. E., and T. S. Gaginella. 1991. The eosinophil in inflammatory bowel disease. Scand. J. Gastrorenterol. 26: 1217-1224.
3. Desreumaux, P., S. Nutten, and J. F. Colombel. 1999. Activated eosinophils in inflammatory bowel disease: do they matter? Am. J. Gastroenterol. 94: 3396-3398.
4. Nishitani, H., M. Okabayashi, M. Satomi, T. Shimoyama, and Y. Dohi. 1998. Infiltration of peroxidase-producing eosinophils into the lamina propria of patients with ulcerative colitis. J. Gastroenterol. 33: 189-195. (Pubitemid 28143395)
5. Rothenberg, M. E., and S. P. Hogan. 2006. The eosinophil. Annu. Rev. Immunol. 24: 147-174.
6. Raab, Y., K. Fredens, B. Gerdin, and R. Hallgren. 1998. Eosinophil activation in ulcerative colitis: studies on mucosal release and localization of eosinophil granule constituents. Dig. Dis. Sci. 43: 1061-1070. (Pubitemid 28211468)
7. Carlson, M., Y. Raab, C. Peterson, R. Hallgren, and P. Venge. 1999. Increased intraluminal release of eosinophil granule proteins EPO, ECP, EPX, and cytokines in ulcerative colitis and proctitis in segmental perfusion. Am. J. Gastroenterol. 94: 1876-1883. (Pubitemid 29315903)
8. Moser, R., J. Fehr, and P. L. Bruijnzeel. 1992. IL-4 controls the selective endothelium- driven transmigration of eosinophils from allergic individuals. J. Immunol. 149: 1432-1438.
9. Sher, A., R. L. Coffman, S. Hieny, and A. W. Cheever. 1990. Ablation of eosinophil and IgE responses with anti-IL-5 or anti-IL-4 antibodies fails to affect immunity against Schistosoma mansoni in the mouse. J. Immunol. 145: 3911-3916.
10. Horie, S., Y. Okubo, M. Hossain, E. Sato, H. Nomura, S. Koyama, J. Suzuki, M. Isobe, and M. Sekiguchi. 1997. Interleukin-13 but not interleukin-4 prolongs eosinophil survival and induces eosinophil chemotaxis. Intern. Med. 36: 179-185. (Pubitemid 27249724)
11. Bochner, B. S., and R. P. Schleimer. 1994. The role of adhesion molecules in human eosinophil and basophil recruitment. J. Allergy Clin. Immunol. 94: 427-438. (Pubitemid 124006650)
12. Zimmermann, N., G. K. Hershey, P. S. Foster, and M. E. Rothenberg. 2003. Chemokines in asthma: cooperative interaction between chemokines and IL-13. J. Allergy Clin. Immunol. 111: 227-242. (Pubitemid 36228539)
13. Zhu, Z., T. Zheng, R. J. Homer, Y. K. Kim, N. Y. Chen, L. Cohn, Q. Hamid, and J. A. Elias. 2004. Acidic mammalian chitinase in asthmatic Th2 inflammation and IL-13 pathway activation. Science 304: 1678-1682. (Pubitemid 38765861)
14. Rankin, S. M., D. M. Conroy, and T. J. Williams. 2000. Eotaxin and eosinophil recruitment: implications for human disease. Mol. Med. Today 6: 20-27. (Pubitemid 30010233)
15. Collins, P. D., S. Marleau, D. A. Griffiths-Johnson, P. J. Jose, and T. J. Williams. 1995. Cooperation between interleukin-5 and the chemokine eotaxin to induce eosinophil accumulation in vivo. J. Exp. Med. 182: 1169-1174.
16. Flood-Page, P., S. Phipps, A. Menzies-Gow, Y. E. Ong, and A. B. Kay. 2003. Effect of intravenous administration of an anti-IL-5 (mepolizumab) on allergen-induced tissue eosinophilia, the late-phase allergic reaction and the expression of a marker of repair/remodeling in human atopic subjects. J. Allergy Clin. Immunol. 111: S261.
17. Hogan, S. P., A. Koskinen, and P. S. Foster. 1997. Interleukin-5 and eosinophils induce airway damage and bronchial hyperreactivity during allergic airway in- flammation in BALB/c mice. Immunol. Cell Biol. 75: 284-288.
18. Foster, P., S. Hogan, A. Ramsay, K. Matthaei, and I. Young. 1996. Interleukin-5 deficiency abolishes eosinophilia, airway hyperreactivity and lung damage in mouse asthma model. J. Exp. Med. 183: 195-201. (Pubitemid 26028759)
19. Forbes, E., V. E. Smart, A. D'Aprile, P. Henry, M. Yang, K. I. Matthaei, M. E. Rothenberg, P. S. Foster, and S. P. Hogan. 2004. T helper-2 immunity regulates bronchial hyperresponsiveness in eosinophil-associated gastrointestinal disease in mice. Gastroenterology 127: 105-118. (Pubitemid 38962279)
20. Gurish, M. F., A. Humbles, H. Tao, S. Finkelstein, J. A. Boyce, C. Gerard, D. S. Friend, and K. F. Austen. 2002. CCR3 is required for tissue eosinophilia and larval cytotoxicity after infection with Trichinella spiralis. J. Immunol. 168: 5730-5736.
21. Rothenberg, M. E., J. A. MacLean, E. Pearlman, A. D. Luster, and P. Leder. 1997. Targeted disruption of the chemokine eotaxin partially reduces antigen-induced tissue eosinophilia. J. Exp. Med. 185: 785-790.
22. Pope, S. M., P. C. Fulkerson, C. Blanchard, H. S. Akei, N. M. Nikolaidis, N. Zimmermann, J. D. Molkentin, and M. E. Rothenberg. 2005. Identification of a cooperative mechanism involving interleukin-13 and eotaxin-2 in experimental allergic lung inflammation. J. Biol. Chem. 280: 13952-13961.
23. Gonzalo, J. A., C. M. Lloyd, D. Wen, J. P. Albar, T. N. Wells, A. Proudfoot, A. C. Martinez, M. Dorf, T. Bjerke, A. J. Coyle, and J. C. Gutierrez-Ramos. 1998. The coordinated action of CC chemokines in the lung orchestrates allergic in- flammation and airway hyperresponsiveness. J. Exp. Med. 188: 157-167.
24. Chen, W., B. Paulus, D. Shu, I. Wilson, and V. Chadwick. 2001. Increased serum levels of eotaxin in patients with inflammatory bowel disease. Scand J. Gastroenterol. 36: 515-520. (Pubitemid 32328442)
25. Mir, A., M. Minguez, J. Tatay, I. Pascual, A. Pena, V. Sanchiz, P. Almela, F. Mora, and A. Benages. 2002. Elevated serum eotaxin levels in patients with inflammatory bowel disease. Am. J. Gastroenterol. 97: 1452-1457. (Pubitemid 34664791)
26. Jeziorska, M., N. Haboubi, P. Schofield, and D. E. Woolley. 2001. Distribution and activation of eosinophils in inflammatory bowel disease using an improved immunohistochemical technique. J. Pathol. 194: 484-492. (Pubitemid 32782675)
27. Park, Y., S. Choi, S. C. Lee, K. P. Kim, S. C. Chae, and H. L. Chung. 2005. The association of eotaxin-2 and eotaxin-3 gene polymorphisms in a Korean population with ulcerative colitis. Exp. Mol. Med. 37: 553-558. (Pubitemid 43143518)
28. Turner, D., C. M. Walsh, E. I. Benchimol, E. H. Mann, K. E. Thomas, C. Chow, R. A. McLernon, T. D. Walters, A. H. Steinhart, and A. M. Griffiths. 2007. Severe paediatric ulcerative colitis: incidence, outcomes, and optimal timing for second line therapy. Gut 57: 331-338. (Pubitemid 351288098)
29. Satsangi, J., M. S. Silverberg, S. Vermeire, and J. F. Colombel. 2006. The Montreal classification of inflammatory bowel disease: controversies, consensus, and implications. Gut 55: 749-753. (Pubitemid 43764536)
30. Rutter, M., B. Saunders, K. Wilkinson, S. Rumbles, G. Schofield, M. Kamm, C. Williams, A. Price, I. Talbot, and A. Forbes. 2004. Severity of inflammation is a risk factor for colorectal neoplasia in ulcerative colitis. Gastroenterology 126: 451-459. (Pubitemid 38182302)
31. Pope, S. M., N. Zimmermann, K. F. Stringer, M. L. Karow, and M. E. Rothenberg. 2005. The eotaxin chemokines and CCR3 are fundamental regulators of allergen-induced pulmonary eosinophilia. J. Immunol. 175: 5341-5350.
32. Lee, J. J., D. Dimina, M. P. Macias, S. I. Ochkur, M. P. McGarry, K. R. O'Neill, C. Protheroe, R. Pero, T. Nguyen, S. A. Cormier, et al. 2004. Defining a link with asthma in mice congenitally deficient in eosinophils. Science 305: 1773-1776.
33. Hogan, S. P., A. Mishra, E. B. Brandt, M. P. Royalty, S. M. Pope, N. Zimmermann, P. S. Foster, and M. E. Rothenberg. 2001. A pathological function for eotaxin and eosinophils in eosinophilic gastrointestinal inflammation. Nat. Immunol. 2: 353-360.
34. Blanchard, C., N. Wang, K. F. Stringer, A. Mishra, P. C. Fulkerson, J. P. Abonia, S. C. Jameson, C. Kirby, M. R. Konikoff, M. H. Collins, et al. 2006. Eotaxin-3 and a uniquely conserved gene-expression profile in eosinophilic esophagitis. J. Clin. Invest. 116: 536-547.
35. Matthews, A. N., D. S. Friend, N. Zimmermann, M. N. Sarafi, A. D. Luster, E. Pearlman, S. E. Wert, and M. E. Rothenberg. 1998. Eotaxin is required for the baseline level of tissue eosinophils. Proc. Natl. Acad. Sci. USA 95: 6273-6278.
36. Rothenberg, M., A. D. Luster, and P. Leder. 1995. Murine eotaxin: an eosinophil chemoattractant inducible in endothelial cells and in interleukin 4-induced tumour suppression. Proc. Natl. Acad. Sci. USA 92: 8960-8964.
37. Ten Hove, T., P. Drillenburg, J. Wijnholds, A. A. te Velde, and S. J. van Deventer. 2002. Differential susceptibility of multidrug resistance protein-1 deficient mice to DSS and TNBS-induced colitis. Dig. Dis. Sci. 47: 2056-2063.
38. Crocker, P. R., and S. Gordon. 1986. Properties and distribution of a lectin-like hemagglutinin differentially expressed by murine stromal tissue macrophages. J. Exp. Med. 164: 1862-1875.
39. Schenk, M., A. Bouchon, F. Seibold, and C. Mueller. 2007. TREM-1-expressing intestinal macrophages crucially amplify chronic inflammation in experimental colitis and inflammatory bowel diseases. J. Clin. Invest. 117: 3097-3106. (Pubitemid 47529639)
40. Bischoff, S. C., J. Mayer, Q. T. Nguyen, M. Stolte, and M. P. Manns. 1999. Immunohistological assessment of intestinal eosinophil activation in patients with eosinophilic gastroenteritis and inflammatory bowel disease. Am. J. Gastroenterol. 94: 3521-3529.
41. Carvalho, A. T., C. C. Elia, H. S. de Souza, P. R. Elias, E. L. Pontes, H. P. Lukashok, F. C. de Freitas, and J. R. Lapa e Silva. 2003. Immunohistochemical study of intestinal eosinophils in inflammatory bowel disease. J. Clin. Gastroenterol. 36: 120-125.
42. Hyams, J. S., P. Davis, K. Grancher, T. Lerer, C. J. Justinich, and J. Markowitz. 1996. Clinical outcome of ulcerative colitis in children. J. Pediatr. 129: 81-88. (Pubitemid 26277250)
43. Kugathasan, S., R. H. Judd, R. G. Hoffmann, J. Heikenen, G. Telega, F. Khan, S. Weisdorf-Schindele, W. San Pablo, Jr., J. Perrault, R. Park, et al. 2003. Epidemiologic and clinical characteristics of children with newly diagnosed inflammatory bowel disease in Wisconsin: a statewide population-based study. J. Pediatr. 143: 525-531.
44. Henriksen, M., J. Jahnsen, I. Lygren, J. Sauar, O. Kjellevold, T. Schulz, M. H. Vatn, and B. Moum. 2006. Ulcerative colitis and clinical course: results of a 5-year population-based follow-up study (the IBSEN study). Inflamm. Bowel Dis. 12: 543-550. (Pubitemid 43977734)
45. Faubion, W. A., Jr., E. V. Loftus, Jr., W. S. Harmsen, A. R. Zinsmeister, and W. J. Sandborn. 2001. The natural history of corticosteroid therapy for inflammatory bowel disease: a population-based study. Gastroenterology 121: 255-260. (Pubitemid 32729372)
46. Robert, M. E., M. Skacel, T. Ullman, C. N. Bernstein, K. Easley, and J. R. Goldblum. 2004. Patterns of colonic involvement at initial presentation in ulcerative colitis: a retrospective study of 46 newly diagnosed cases. Am. J. Clin. Pathol. 122: 94-99.
47. Lampinen, M., M. Carlson, P. Sangfelt, Y. Taha, M. Thorn, L. Loof, Y. Raab, and P. Venge. 2001. IL-5 and TNF-α participate in recruitment of eosinophils to intestinal mucosa in ulcerative colitis. Dig. Dis. Sci. 46: 2004-2009. (Pubitemid 32844170)
48. Miner, P. B., Jr. 2004. Seeing red in inflammatory bowl disease: the eosinophil at center stage? Inflamm. Bowel. Dis. 10: 329-330.
49. Dvorak, A. M. 1980. Ultrastructural evidence for release of major basic protein-containing crystalline cores of eosinophil granules in vivo: cytotoxic potential in Crohn's disease. J. Immunol. 125: 460-462.
50. MacPherson, J. C., S. A. Comhair, S. C. Erzurum, D. F. Klein, M. F. Lipscomb, M. S. Kavuru, M. K. Samoszuk, and S. L. Hazen. 2001. Eosinophils are a major source of nitric oxide-derived oxidants in severe asthma: characterization of pathways available to eosinophils for generating reactive nitrogen species. J. Immunol. 166: 5763-5772.
51. Forbes, E., T. Murase, M. Yang, K. I. Matthaei, J. J. Lee, N. A. Lee, P. S. Foster, and S. P. Hogan. 2004. Immunopathogenesis of experimental ulcerative colitis is mediated by eosinophil peroxidase. J. Immunol. 172: 5664-5675. (Pubitemid 38542070)
52. Katsuta, T., C. Lim, K. Shimoda, K. Shibuta, P. Mitra, B. F. Banner, M. Mori, and G. F. Barnard. 2000. Interleukin-8 and SDF1-α mRNA expression in colonic biopsies from patients with inflammatory bowel disease. Am. J. Gastroenterol. 95: 3157-3164. (Pubitemid 30826290)
53. Banks, C., A. Bateman, R. Payne, P. Johnson, and N. Sheron. 2003. Chemokine expression in IBD: mucosal chemokine expression is unselectively increased in both ulcerative colitis and Crohn's disease. J. Pathol. 199: 28-35. (Pubitemid 36054726)
54. Egesten, A., M. Eliasson, A. I. Olin, J. S. Erjefalt, A. Bjartell, P. Sangfelt, and M. Carlson. 2007. The proinflammatory CXC-chemokines GRO-α/CXCL1 and MIG/CXCL9 are concomitantly expressed in ulcerative colitis and decrease during treatment with topical corticosteroids. Int. J. Colorectal Dis. 22: 1421-1427. (Pubitemid 47543330)
55. Berrebi, D., J. Languepin, L. Ferkdadji, A. Foussat, P. De Lagausie, R. Paris, D. Emilie, J. F. Mougenot, J. P. Cezard, J. Navarro, and M. Peuchmaur. 2003. Cytokines, chemokine receptors, and homing molecule distribution in the rectum and stomach of pediatric patients with ulcerative colitis. J. Pediatr. Gastroenterol. Nutr. 37: 300-308. (Pubitemid 39274521)
56. Papadakis, K. A., J. Prehn, D. Zhu, C. Landers, J. Gaiennie, P. Fleshner, and S. R. Targan. 2004. Expression and regulation of the chemokine receptor CXCR3 on lymphocytes from normal and inflammatory bowel disease mucosa. Inflamm. Bowel Dis. 10: 778-788.
57. Sasaki, S., H. Yoneyama, K. Suzuki, H. Suriki, T. Aiba, S. Watanabe, Y. Kawauchi, H. Kawachi, F. Shimizu, K. Matsushima, et al. 2002. Blockade of CXCL10 protects mice from acute colitis and enhances crypt cell survival. Eur. J. Immunol. 32: 3197-3205. (Pubitemid 35414877)
58. Wu, F., T. Dassopoulos, L. Cope, A. Maitra, S. R. Brant, M. L. Harris, T. M. Bayless, G. Parmigiani, and S. Chakravarti. 2007. Genome-wide gene expression differences in Crohn's disease and ulcerative colitis from endoscopic pinch biopsies: insights into distinctive pathogenesis. Inflamm. Bowel Dis. 13: 807-821. (Pubitemid 47203859)
59. Clevers, H. C. 2004. At the crossroads of inflammation and cancer. Cell 118: 671-674.
60. Laurent, F., L. Eckmann, T. C. Savidge, G. Morgan, C. Theodos, M. Naciri, and M. F. Kagnoff. 1997. Cryptosporidium parvum infection of human intestinal epithelial cells induces the polarized secretion of C-X-C chemokines. Infect. Immun. 65: 5067-5073. (Pubitemid 27513551)
61. Kim, J. M., Y. K. Oh, Y. J. Kim, H. B. Oh, and Y. J. Cho. 2001. Polarized secretion of CXC chemokines by human intestinal epithelial cells in response to Bacteroides fragilis enterotoxin: NF-κB plays a major role in the regulation of IL-8 expression. Clin. Exp. Immunol. 123: 421-427.
62. Rogler, G., K. Brand, D. Vogl, S. Page, R. Hofmeister, T. Andus, R. Knuechel, P. A. Baeuerle, J. Scholmerich, and V. Gross. 1998. Nuclear factor κB is activated in macrophages and epithelial cells of inflamed intestinal mucosa. Gastroenterology 115: 357-369. (Pubitemid 28363428)
63. Voehringer, D., N. Van Rooijen, and R. M. Locksley. 2007. Eosinophils develop in distinct stages and are recruited to peripheral sites by alternatively activated macrophages. J. Leukocyte Biol. 81: 1434-1444. (Pubitemid 46827966)
64. Matsukura, S., C. Stellato, J. R. Plitt, C. Bickel, K. Miura, S. N. Georas, V. Casolaro, and R. P. Schleimer. 1999. Activation of eotaxin gene transcription by NF-κB and STAT6 in human airway epithelial cells. J. Immunol. 163: 6876-6883.
65. Fichtner-Feigl, S., I. J. Fuss, J. C. Preiss, W. Strober, and A. Kitani. 2005. Treatment of murine Th1- and Th2-mediated inflammatory bowel disease with NF-κB decoy oligonucleotides. J. Clin. Invest. 115: 3057-3071. (Pubitemid 41567571)