CD14+CD33+ myeloid cell-CCL11-eosinophil signature in ulcerative colitis

Journal of Leukocyte Biology

Volumn 94, Issue 5, 2013, Pages 1061-1070

  Lampinen, Maria ^a   Waddell, Amanda ^b   Ahrens, Richard ^b   Carlson, Marie ^a   Hogan, Simon P ^b  

^a UPPSALA UNIVERSITY HOSPITAL   (Sweden)

^b CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

Author keywords

Chemokine; Eotaxins; Inflammatory bowel disease

Indexed keywords

CD14 ANTIGEN; CD33 ANTIGEN; EOTAXIN; EOTAXIN 2; EOTAXIN 3; INTERLEUKIN 5; MESSENGER RNA;

ADULT; AGED; ARTICLE; BONE MARROW CELL; CELL ACTIVATION; CELL COUNT; CLINICAL ARTICLE; COLON BIOPSY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE SEVERITY; EOSINOPHIL; FEMALE; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; MACROPHAGE; MALE; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; RECTUM BIOPSY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ULCERATIVE COLITIS;

CHEMOKINE; EOTAXINS; INFLAMMATORY BOWEL DISEASE;

ADULT; AGED; ANTIGENS, CD14; CHEMOKINE CCL11; COLITIS, ULCERATIVE; EOSINOPHILS; FEMALE; HUMANS; MALE; MIDDLE AGED; MYELOID CELLS; RECTUM; RNA, MESSENGER; SIALIC ACID BINDING IG-LIKE LECTIN 3;

EID: 84887013969     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.1212640     Document Type: Article

References (68)

1. Farrell, R. J., Peppercorn, M. A. (2004) Endoscopy in inflammatory bowel disease. In Kirsner's Inflammatory Bowel Disease (B. Sartor, R. J. Sandborn, eds.), W. Saunders, Edinburgh, London, New York, Oxford, Philadelphia, St. Louis, Sydney, Toronto, 380-398.
2. Riddell, R H. (2004) Pathology of idiopathic inflammatory bowel disease. In Inflammatory Bowel Diseases (B. Sartor, R J. Sandborn, eds.), W. Saunders, Edinburgh, London, New York, Oxford, Philadelphia, St. Louis, Sydney, Toronto, 399-424.
3. Rothenberg, M. E., Hogan, S. P. (2006) The eosinophil. Annu.Rev.Immunol. 24, 147-174.
4. Venge, P., Bergstrand, H., Hakansson, L. (1996) Neutrophils and eosin-ophils. In Textbook of Rheumatology (N. Kelley, W. D. Harris, E. Ruddy, S. D. Sledge, eds.), C. W. B. Saunders, Philadelphia, 146-160.
5. Hogan, S. P., Rosenberg, H. F., Moqbel, R, Phipps, S., Foster, P. S., Lacy, P., Kay, A. B., Rothenberg, M. E. (2008) Eosinophils: biological properties and role in health and disease. Clin. Exp. Allergy 38, 709-750.
6. Bischoff, S. C, Wedemeyer, J., Herrmann, A., Meier, P. N., Trautwein, C, Cetin, Y, Maschek, H., Stolte, M., Gebel, M., Manns, M. P. (1996) Quantitative assessment of intestinal eosinophils and mast cells in inflammatory bowel disease. Histopathology 28, 1-13.
7. Carlson, M., Raab, Y, Peterson, C, Hällgren, R, Venge, P. (1999) Increased intraluminal release of eosinophil granule proteins EPO, ECP, EPX, and cytokines in ulcerative colitis and proctitis in segmental perfu-sion. Am. J. Gastroenterol. 94, 1876-1883.
8. Sangfelt, P., Carlson, M., Thörn, M., Lööf, L., Raab, R (2001) Neutro-phil and eosinophil granule proteins as markers of response to local prednisolone treatment in distal ulcerative colitis and proctitis. Am. J. Gastroenterol. 96, 1085-1090.
9. 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, J. J., Rothenberg, M. E., Denson, L., Hogan, S. P. (2008) Intestinal macrophage/epithelial cell-derived CCL11/eo-taxin-1 mediates eosinophil recruitment and function in pediatric ulcerative colitis. J. Immunol. 181, 7390-7399.
10. Forbes, E., Murase, T, Yang, M., Matthaei, K I., Lee, J. J., Lee, N A., Foster, P. S., Hogan, S. P. (2004) Immunopathogenesis of experimental ulcerative colitis is mediated by eosinophil peroxidase. J. Immunol 172, 5664-5675.
11. Forbes, E., Hulett, M., Ahrens, R, Wagner, N., Smart, V., Matthaei, K. I., Brandt, E. B., Dent, L. A, Rothenberg, M. E., Tang, M., Foster, P. S., Hogan, S. P. (2006) ICAM-1-dependent pathways regulate colonic eosinophilic inflammation. J. Leukoc. Biol. 80, 330-341.
12. Takedatsu, H., Mitsuyama, K, Matsumoto, S., Handa, K, Suzuki, A, Takedatsu, H., Funabashi, H., Okabe, Y, Hara, T., Toyonaga, A, Sata, M. (2004) Interleukin-5 participates in the pathogenesis of ileitis in SAMP1/Yit mice. Eur. J. Immunol. 34, 1561-1569.
13. Matsumoto, S., Okabe, Y, Setoyama, H., Takayama, K, Ohtsuka, J., Fu-nahashi, H., Imaoka, A, Okada, Y, Umesaki, Y (1998) Inflammatory bowel disease-like enteritis and caecitis in a senescence accelerated mouse P1/Yit strain. Gut 43, 71-78.
14. Phipps, S., Ying, S., Wangoo, A, Ong, Y-E., Levi-Schaffer, F., Kay, B. (2002) The relationship between allergen-induced tissue eosinophilia and markers of repair and remodeling in human atopic skin. J. Immunol. 169, 4604-4612.
15. Moser, R, Fehr, J., Bruijnzeel, P. L. B. (1992) IL-4 controls the selective endothelial-driven transmigration of eosinophils from allergic individuals. J. Immunol. 149, 1432-1438.
16. Lampinen, M., Carlson, M., Sangfelt, P., Taha, Y, Thörn, M., Lööf, L., Raab, Y, Venge, P. (2001) IL-5 and TNF-cra participate in the recruitment of eosinophils to intestinal mucosa in ulcerative colitis. Dig. Dis. Sci. 46, 2004-2009.
17. Kameyoshi, Y, Schröder, J-M., Christophers, E., Yamamoto, S. (1994) Identification of the cytokine RANTES released from platelets as an eosinophil che-motactic factor. IntArch.Allergy Immunol. 104 (Suppl. 1), 49-51.
18. Jose, P. J., Griffiths-Johnson, D. A, Collins, P. D., Walsh, D. T., Moqbel, R, Totty, N. F., Truong, O., Hsuan, J. J., Williams, T. J. (1994) Eotaxin: a potent eosinophil chemoattractant cytokine detected in a guinea pig model of allergic airways inflammation. J. Exp. Med. 179, 881-887.
19. Banwell, M. E., Tolley, N. S., Williams, T. J., Mitchell, T. J. (2002) Regulation of human eotaxin-3/CCL26 expression: modulation by cytokines and glucocorticoids. Cytokine 17, 17-23.
20. Collins, P. D., Marleau, S., Griffiths-Johnson, D. A, Jose, P. J., Williams, T J. (1995) Cooperation between interleukin-5 and the chemokine eotaxin to induce eosinophil accumulation in vivo. J. Exp. Med. 182, 1169-1174.
21. Van, L. J., Russell, R K, Drummond, H. E., Aldhous, M. C, Round, N. K, Nimmo, E. R, Smith, L., Gillett, P. M., McGrogan, P., Weaver, L.T., Bisset, W. M., Mahdi, G., Arnott, I. D., Satsangi, J., Wilson, D. C. (2008) Definition of phenotypic characteristics of childhood-onset inflammatory bowel disease. Gastroenterology 135, 1114-1122.
22. Sands, B. E. (2004) From symptom to diagnosis: clinical distinctions among various forms of intestinal inflammation. Gastroenterology 126, 1518-1532.
23. Binder, V. (1970) A comparison between clinical state, macroscopic and microscopic appearances of rectal mucosa, and cytologic picture of mucosal exudate in ulcerative colitis. Scand. J. Gastroent. 5, 627-632.
24. Kristjansson, G., Venge, P., Wanders, A, Loof, L., Hallgren, R (2004) Clinical and subclinical intestinal inflammation assessed by the mucosal patch technique: studies of mucosal neutrophil and eosinophil activation in inflammatory bowel diseases and irritable bowel syndrome. Gut 53, 1806-1812.
25. Lampinen, M., Ronnblom, A, Amin, K, Kristjansson, G., Rorsman, F., Sangfelt, P., Safsten, B., Wagner, M., Wanders, A., Winqvist, O., Carlson, M. (2005) Eosinophil granulocytes are activated during the remission phase of ulcerative colitis. Gut 54, 1714-1720.
26. Amin, K, Rinne, J., Haahtela, T., Simola, M., Peterson, C.G.B., Roomans, G.M., Malmberg, H., Venge, P., Sevéus, L. (2004) Inflammatory cell and epithelial characteristics of perennial allergic and nonaller-gic rhinitis with a symptom history of 1 to 3 years' duration. J. Allergy Clin. Immunol. 107, 249-257.
27. Satin, S. K, Malhotra, V., Sen, G. S., Karol, A, Gaur, S. K, Anand, B. S. (1987) Significance of eosinophil and mast cell counts in rectal mucosa in ulcerative colitis. A prospective controlled study. Dig. Dis. Sci. 32, 363-367.
28. Schleimer, R. P., Bochner, B. S. (1994) The effects of glucocorticoids on human eosinophils. J. Allergy Clin. Immunol. 94, 1202-1213.
29. Peterson, C. G., Sangfelt, P., Wagner, M., Hansson, T., Lettesjo, H., Carlson, M. (2007) Fecal levels of leukocyte markers reflect disease activity in patients with ulcerative colitis. Scand J. Clin. Lab. Invest. 67, 810-820.
30. Awano, N., Ryu, T., Yoshimura, N., Takazoe, M., Kitamura, S., Tanaka, M. (2011) Successful treatment of ulcerative colitis associated with hype-reosinophilic syndrome/chronic eosinophilic leukemia. Intern. Med. 50, 1741-1745.
31. Nixon, J., Riddell, R. (1990) Histopathology in ulcerative colitis. In Inflammatory Bowel Disease (R. Allan, M. Keighley, C. Alexander-Williams, C. Hawkins), Churchill Livingstone, Edinburgh, 247-285.
32. Raab, Y., Fredens, K, Gerdin, B., Hällgren, R. (1998) Eosinophil activation in ulcerative colitis. Studies on mucosal release and localization of eosinophil granule constituents. Dig. Dis. Sci. 43, 1061-1070.
33. Venge, P. (2010) The eosinophil and airway remodelling in asthma. Clin. Respir. J. 4 (Suppl. 1), 15-19.
34. Li-Kim-Moy, J. P., Tobias, V., Day, A. S., Leach, S., Lemberg, D. A. (2011) Esophageal subepithelial fibrosis and hyalinization are features of eosinophilic esophagitis. J. Pediatr. Gastroenterol. Nutr. 52, 147-153.
35. Aceves, S. S., Ackerman, S. J. (2009) Relationships between eosinophilic inflammation, tissue remodeling, and fibrosis in eosinophilic esophagitis. Immunol. Allergy Clin. North Am. 29, 197-211.
36. Lee, J. M., Dedhar, S., Kalluri, R., Thompson, E. W. (2006) The epithe-lial-mesenchymal transition: new insights in signaling, development, and disease. J. Cell Biol. 172,973-981.
37. Minshall, E. M., Leung, D. Y, Martin, R. J., Song, Y L., Cameron, L., Ernst, P., Hamid, Q. (1997) Eosinophil-associated TGF-/31 mRNA expression and airways fibrosis in bronchial asthma. Am. J. Respir. Cell Mol. Biol. 17, 326-333.
38. Kagalwalla, A. F., Akhtar, N., Woodruff, S. A., Rea, B. A., Masterson, J. C., Mukkada, V., Parashette, K. R., Du, J., Fillon, S., Protheroe, C. A., Lee, J. J., Amsden, K, Melin-Aldana, H., Capocelli, K. E., Furuta, G. T., Ackerman, S. J. (2012) Eosinophilic esophagitis: epithelial mesenchymal transition contributes to esophageal remodeling and reverses with treatment. J. Allergy Clin. Immunol. 129, 1387-1396.
39. Rieder, F., Fiocchi, C. (2008) Intestinal fibrosis in inflammatory bowel disease-current knowledge and future perspectives. J Crohns Colitis 2, 279-290.
40. Rieder, F., Fiocchi, C. (2009) Intestinal fibrosis in IBD-a dynamic, mul-tifactorial process. Nat. Rev. Gastroenterol. Hepatol. 6, 228-235.
41. Dallaire, M-J., Ferland, C, Lavigne, S., Chakir, J., Laviolette, M. (2002) Migration through basement membrane modulates eosinophil expression of CD44. Clin. Exp. Allergy 32, 898-905.
42. Matsumoto, K, Appiah-Pippirn, J., Schleimer, R. P., Bickel, C, Beck, L., Bochner, B. S. (1998) CD44 and CD69 represent different types of cell-surface activation markers for human eosinophils. Am. J. Respir. Cell Mol. Biol. 18, 860-866.
43. Ohkawara, Y, Tamura, G., Iwasaki, T., Tanaka, A., Kikuchi, T., Shirato, K (2000) Activation and transforming growth factor-/3 production in eosinophils by hyaluronan. Am. J. Respir. Cell Mol. Biol. 23, 444-451.
44. Mishra, A., Hogan, S. P., Brandt, E., Wagner, N., Crossman, M. W., Foster, P. S., Rothenberg, M. E. (2002) Enterocyte expression of the eo-taxin and interleukin-5 transgenes induces compartmentalized dysregu-lation of eosinophil trafficking. J. Biol. Chem. 277, 4406-4412.
45. Ying, S., Robinson, D.S., Meng, Q., Barata, L. T., McEuen, A. R., Buckley, M. G., Walls, A. F., Askenase, P. W., Kay, A. B. (1999) C-C chemo-kines in allergen-induced late-phase cutaneous responses in atopic subjects: association of eotaxin with early 6-hour eosinophils, and of eotaxin-2 and monocyte chemoattractant protein-4 with the later 24-hour tissue eosinophilia, and relationship to basophils and other C-C chemo-kines (monocyte chemoattractant protein-3 and RANTES). J. Immunol. 163, 3976-3984.
46. Matthews, A. N., Friend, D. S., Zimmerman, N., Sarafi, M. N., Luster, A. D., Pearlman, E., Wert, S. E., Rothenberg, M. E. (1998) Eotaxin is required for the baseline level of tissue eosinophils. Proc. Natl. Acad. Sci. USA 95, 6273-6278.
47. Wardlaw, A. J. (1999) Molecular basis for selective eosinophil trafficking in asthma: a multistep paradigm. J. Allergy Clin. Immunol. 104, 917-926.
48. Blanchard, C, Wang, N., Stringer, K. F., Mishra, A., Fulkerson, P. C, Abonia, J. P., Jameson, S. C, Kirby, C, Konikoff, M. R., Collins, M. H., Cohen, M. B., Akers, R., Hogan, S. P., Assa'ad, A. H., Putnam, P. E., Aronow, B. J., Rothenberg, M. E. (2006) Eotaxin-3 and a uniquely conserved gene-expression profile in eosinophilic esophagitis. J. Clin. Invest. 116, 536-547.
49. Bjerrum, J. T, Hansen, M., Olsen, J., Nielsen, O. H. (2010) Genome-wide gene expression analysis of mucosal colonic biopsies and isolated colonocytes suggests a continuous inflammatory state in the lamina propria of patients with quiescent ulcerative colitis. Inflamm. Bowel Dis. 16, 999-1007.
50. Christophi, G. P., Rong, R., Holtzapple, P. G., Massa, P. T., Landas, S. K (2012) Immune markers and differential signaling networks in ulcerative colitis and Crohn's disease. Inflamm. Bowel Dis. 18, 2342-2356.
51. Yamamoto, T, Umegae, S., Kitagawa, T, Matsumoto, K (2005) Systemic and local cytokine production in quiescent ulcerative colitis and its relationship to future relapse: a prospective pilot study. Inflamm. BowelDis. 11, 589-596.
52. Garcia-Sanchez, V., Gonzalez, R., Iglesias-Flores, E., Gisbert, J. P., Angel-Rey, J. M., Soto-Escribano, P., Galvez-Calderon, C, Reyes-Lopez, A., Perez-Jimenez, F., de Dios-Vega, J. F., Muntane, J., Gomez-Camacho, F. (2010) Can systemic cytokines predict relapse of inflammatory bowel disease? Hepatogastroenterology 57, 524-530.
53. Kamada, N., Hisamatsu, T., Okamoto, S., Chinen, H., Kobayashi, T., Sato, T., Sakuraba, A., Kitazume, M. T., Sugita, A., Koganei, K, Aka-gawa, K. S., Hibi, T. (2008) Unique CD14 intestinal macrophages contribute to the pathogenesis of Crohn disease via IL-23/IFN-7 axis. J. Clin. Invest. 118, 2269-2280.
54. Kamada, N, Hisamatsu, T, Honda, H., Kobayashi, T, Chinen, H, Kitazume, M. T, Takayama, T, Okamoto, S., Koganei, K, Sugita, A, Kanai, T, Hibi, T (2009) Human CD14+ macrophages in intestinal lamina propria exhibit potent antigen-presenting ability. J. Immunol. 183, 1724-1731.
55. Rogler, G, Andus, T, Aschenbrenner, E., Vogl, D., Falk, W., Scholmerich, J., Gross, V. (1997) Alterations of the phenotype of colonic macrophages in inflammatory bowel disease. Eur. J. Gastroenterol. Hepatol. 9, 893-899.
56. Waddell, A, Ahrens, R., Steinbrecher, K, Donovan, B., Rothenberg, M. E., Mu-nitz, A, Hogan, S. P. (2011) Colonic eosinophilic inflammation in experimental colitis is mediated by Ly6C(high) CCR2(+) inflammatory monocyte/mac-rophage-derived CCLll. J Immunol. 186, 5993-6003.
57. Waddell, A., Ahrens, R., Tsai, Y T., Sherril, J. D., Denson, L., Steinbrecher, K, Hogan, S. P. (2013) Intestinal CCL11 and eosinophilic inflammation is regulated by myeloid cell-specific RelA/p65 in mice. J. Immunol. 190, 4783-4785.
58. Marenholz, I., Heizmann, C. W., Fritz, G. (2004) S100 proteins in mouse and man: from evolution to function and pathology (including an update of the nomenclature). Biochem. Biophys. Res. Commun. 322, 1111-1122
59. Sunahori, K, Yamamura, M., Yamana, J., Takasugi, K, Kawashima, M., Yamamoto, H., Chazin, W. J., Nakatani, Y, Yui, S., Makino, H. (2006) The S100A8/A9 heterodimer amplifies proinflammatory cytokine production by macrophages via activation of nuclear factor k B and p38 mitogen-activated protein kinase in rheumatoid arthritis. Arthritis Res.Ther. 8, R69.
60. Kerkhoff, C, Eue, I., Sorg, C. (1999) The regulatory role of MRP8 (S100A8) and MRP14 (S100A9) in the transendothelial migration of human leukocytes. Pathobiology 67, 230-232.
61. Kerkhoff, C, Klempt, M., Sorg, C. (1998) Novel insights into structure and function of MRP8 (S100A8) and MRP14 (S100A9). Biochim. Biophys. Ada 1448, 200-211.
62. Gebhardt, C, Riehl, A., Durchdewald, M., Nemeth, J., Furstenberger, G, Muller-Decker, K., Enk, A., Arnold, B., Bierhaus, A., Nawroth, P. P., Hess, J., Angel, P. (2008) RAGE signaling sustains inflammation and promotes tumor development. J. Exp. Med. 205, 275-285.
63. Turovskaya, O., Foell, D., Sinha, P., Vogl, T., Newlin, R., Nayak, J., Nguyen, M., Olsson, A., Nawroth, P. P., Bierhaus, A., Varki, N., Kronen-berg, M., Freeze, H. H., Srikrishna, G. (2008) RAGE, carboxylated gly-cans and S100A8/A9 play essential roles in colitis-associated carcinogen-esis. Carcinogenesis 29, 2035-2043.
64. Aomatsu, T., Yoden, A., Matsumoto, K, Kimura, E., Inoue, K, Andoh, A, Tamai, H. (2011) Fecal calprotectin is a useful marker for disease activity in pediatric patients with inflammatory bowel disease. Dig. Dis. Sci. 56, 2372-2377.
65. Lewis, J. D. (2011) The utility of biomarkers in the diagnosis and therapy of inflammatory bowel disease. Gastroenterology 140, 1817-1826.
66. Dabritz, J., Friedrichs, F., Weinhage, T., Hampe, J., Kucharzik, T., Lu-gering, A., Broeckel, U., Schreiber, S., Spieker, T., Stoll, M., Foell, D. (2011) The functional-374T/A polymorphism of the receptor for ad vanced glycation end products may modulate Crohn's disease. Am. J. Physiol. Gastrointest. Liver Physiol. 300, G823-G832.
67. Molodecky, N. A., Soon, I. S., Rabi, D. M., Ghali, W. A., Ferris, M., Cher-noff, G., Benchimol, E. I., Panaccione, R., Ghosh, S., Barkema, H. W., Kaplan, G. G. (2012) Increasing incidence and prevalence of the inflammatory bowel diseases with time, based on systematic review. Gastroenterology 142, 46-54.
68. Smith, P. D., Smythies, L. E., Mosteller-Barnum, M., Sibley, D. A., Russell, M. W., Merger, M., Sellers, M. T., Orenstein, J. M., Shimada, T., Graham, M. F., Kubagawa, H. (2001) Intestinal macrophages lack CD14 and CD89 and consequently are down-regulated for LPS-and IgA-medi-ated activities. J. Immunol. 167, 2651-2656.