A key requirement for CD300f in innate immune responses of eosinophils in colitis

Mucosal Immunology

Volumn 10, Issue 1, 2017, Pages 172-183

  Moshkovits, I ^a   Reichman, H ^a   Karo Atar, D ^a   Rozenberg, P ^a   Zigmond, E ^a   Haberman, Y ^b,c   Ben Baruch Morgenstern, N ^a   Lampinen, M ^d   Carlson, M ^d   Itan, M ^a   Denson, L A ^b   Varol, C ^a   Munitz, A ^a  

^a TEL AVIV UNIVERSITY   (Israel)

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

^c SHEBA MEDICAL CENTER   (Israel)

^d UPPSALA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CALGRANULIN A; CD300A; CD300F; CD300LB; INTERLEUKIN 13; INTERLEUKIN 4; MESSENGER RNA; RECEPTOR; UNCLASSIFIED DRUG; CD300LF PROTEIN, HUMAN; CLM-1 PROTEIN, MOUSE; IMMUNOGLOBULIN RECEPTOR;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL INFILTRATION; CONTROLLED STUDY; CORRELATIONAL STUDY; CROHN DISEASE; CYTOKINE PRODUCTION; DISEASE ACTIVITY; DISEASE SEVERITY; EOSINOPHIL; FEMALE; GENE EXPRESSION; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; INFLAMMATORY CELL; INNATE IMMUNITY; MAJOR CLINICAL STUDY; MALE; MONOCYTE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; ULCERATIVE COLITIS; UPREGULATION; WILD TYPE; ANIMAL; C57BL MOUSE; CELL CULTURE; DISEASE MODEL; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; MIDDLE AGED; TH2 CELL; YOUNG ADULT;

ADULT; ANIMALS; CALGRANULIN A; CELLS, CULTURED; COLITIS, ULCERATIVE; CROHN DISEASE; DISEASE MODELS, ANIMAL; EOSINOPHILS; FEMALE; HUMANS; IMMUNITY, INNATE; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MIDDLE AGED; RECEPTORS, IMMUNOLOGIC; TH2 CELLS; YOUNG ADULT;

EID: 85011049804     PISSN: 19330219     EISSN: 19353456     Source Type: Journal    
DOI: 10.1038/mi.2016.37     Document Type: Article

References (50)

1. Rosenberg, H.F., Dyer, K.D. &Foster, P.S. Eosinophils: changing perspectives in health and disease. Nat. Rev. Immunol. 13, 9-22 (2013).
2. Ahrens, R. et al. Intestinal macrophage/epithelial cell-derived CCL11/ eotaxin-1 mediates eosinophil recruitment and function in pediatric ulcerative colitis. J. Immunol. 181, 7390-7399 (2008).
3. Waddell, A. et al. Colonic eosinophilic inflammation in experimental colitis is mediated by Ly6C(high) CCR2(+) inflammatory monocyte/macrophagederived CCL11. J. Immunol. 186, 5993-6003 (2011).
4. Waddell, A. et al. Intestinal CCL11 and eosinophilic inflammation is regulated by myeloid cell-specific RelA/p65 in mice. J. Immunol. 190, 4773-4785 (2013).
5. McNamee, E.N. et al. Novel model of TH2-polarized chronic ileitis: The SAMP1 mouse. Inflamm. Bowel Dis. 16, 743-752 (2010).
6. Furuta, G.T. et al. Eosinophils alter colonic epithelial barrier function: role formajor basic protein. Am. J. Physiol. Gastrointest. Liver Physiol. 289, G890-G897 (2005).
7. Forbes, E. et al. Immunopathogenesis of experimental ulcerative colitis is mediated by eosinophil peroxidase. J. Immunol. 172, 5664-5675 (2004).
8. Chu, V.T. et al. Eosinophils promote generation and maintenance of immunoglobulin-A-expressing plasma cells and contribute to gut immune homeostasis. Immunity 40, 582-593 (2014).
9. Calabrese, L.H. &Rose-John, S. IL-6 biology: implications for clinical targeting in rheumatic disease. Nat. Rev. Rheumatol. 10, 720-727 (2014).
10. Yousefi, S. et al. Catapult-like release of mitochondrial DNA by eosinophils contributes to antibacterial defense. Nat. Med. 14, 949-953 (2008).
11. Munitz, A. Inhibitory receptors on myeloid cells: new targets for therapy? Pharmacol. Ther. 125, 128-137 (2010).
12. Borrego, F. The CD300 molecules: an emerging family of regulators of the immune system. Blood 121, 1951-1960 (2013).
13. Clark, G.J., Ju, X., Tate, C. &Hart, D.N. The CD300 family of molecules are evolutionarily significant regulators of leukocyte functions. Trends Immunol. 30, 209-217 (2009).
14. Alvarez-Errico, D., Sayos, J. &Lopez-Botet, M. The IREM-1 (CD300f) inhibitory receptor associates with the p85alpha subunit of phosphoinositide 3-kinase. J. Immunol. 178, 808-816 (2007).
15. Moshkovits, I. et al. CMRF35-like molecule 1 (CLM-1) regulates eosinophil homeostasis by suppressing cellular chemotaxis. Mucosal Immunol. 7, 292-303 (2014).
16. Haberman, Y. et al. Pediatric Crohn disease patients exhibit specific ileal transcriptome and microbiome signature. J. Clin. Invest. 124, 3617-3633 (2014).
17. Masoodi, I., Tijjani, B.M.,Wani, H., Hassan, N.S., Khan, A.B. &Hussain, S. Biomarkers in the management of ulcerative colitis: a brief review. Ger. Med. Sci. 9, Doc03 (2011).
18. Planell, N. et al. Transcriptional analysis of the intestinal mucosa of patients with ulcerative colitis in remission reveals lasting epithelial cell alterations. Gut 62, 967-976 (2013).
19. Fang, K. et al. Temporal genomewide expression profiling of DSS colitis reveals novel inflammatory and angiogenesis genes similar to ulcerative colitis. Physiol. Genomics 43, 43-56 (2011).
20. Lampinen, M., Waddell, A., Ahrens, R., Carlson, M. &Hogan, S.P. CD14+CD33+ myeloid cell-CCL11-eosinophil signature in ulcerative colitis. J. Leukoc. Biol. 94, 1061-1070 (2013).
21. Zigmond, E. et al. Ly6C hi monocytes in the inflamed colon give rise to proinflammatory effector cells and migratory antigen-presenting cells. Immunity 37, 1076-1090 (2012).
22. Shajib, M.S. et al. Interleukin 13 and serotonin: linking the immune and endocrine systems in murine models of intestinal inflammation. PloS One 8, e72774 (2013).
23. Pushparaj, P.N. et al. Interleukin-33 exacerbates acute colitis via interleukin-4 in mice. Immunology 140, 70-77 (2013).
24. Bustamante, C.D. et al. Natural selection on protein-coding genes in the human genome. Nature 437, 1153-1157 (2005).
25. Burakoff, R. et al. Blood-based biomarkers can differentiate ulcerative colitis from Crohn's disease and noninflammatory diarrhea. Inflamm. Bowel Dis. 17, 1719-1725 (2011).
26. Matsukawa, T. et al. Ceramide-CD300f binding suppresses experimental colitis by inhibiting ATP-mediated mast cell activation. Gut 65, 777-787 (2016).
27. Shik, D., Moshkovits, I., Karo-Atar, D., Reichman, H. &Munitz, A. Interleukin-33 requires CMRF35-like molecule-1 expression for induction of myeloid cell activation. Allergy 69, 719-729 (2014).
28. Karo-Atar, D., Itan, M., Pasmanik-Chor, M. &Munitz, A. MicroRNA profiling reveals opposing expression patterns for miR-511 in alternatively and classically activated macrophages. J. Asthma 52, 1-9 (2014).
29. Moshkovits, I. et al. CD300f associates with IL-4 receptor alpha and amplifies IL-4-induced immune cell responses. Proc. Natl. Acad. Sci. USA 112, 8708-8713 (2015).
30. Nakahashi-Oda,C. et al. Apoptotic epithelial cells control the abundance of T cells at barrier surfaces. Nat. Immunol. 17, 441-450 (2016).
31. Masterson, J.C. et al. Eosinophil-mediated signalling attenuates inflammatory responses in experimental colitis. Gut 64, 1236-1247 (2014).
32. Nickerson, K.P., Chanin, R. and McDonald, C. Deregulation of intestinal antimicrobial defense by the dietary additive, maltodextrin. Gut Microbes 6, 78-83 (2015).
33. Martinez-Barriocanal, A., Comas-Casellas, E., Schwartz, S. Jr., Martin, M. &Sayos, J. CD300 heterocomplexes, a new and family-restricted mechanism for myeloid cell signaling regulation. J. Biol. Chem. 285, 41781-41794 (2010).
34. Xi, H. et al. Negative regulation of autoimmune demyelination by the inhibitory receptor CLM-1. J. Exp. Med. 207, 7-16 (2010).
35. Tian, L. et al. p85alpha recruitment by the CD300f phosphatidylserine receptor mediates apoptotic cell clearance required for autoimmunity suppression. Nat. Commun. 5, 3146 (2014).
36. Bercovitz, Z.T. &Sommers, S.C. Altered inflammatory reaction in nonspecific ulcerative colitis. Arch. Intern. Med. 117, 504-510 (1966).
37. Dvorak, A.M. Ultrastructural evidence for release of major basic proteincontaining crystalline cores of eosinophil granules in vivo: cytotoxic potential in Crohn's disease. J. Immunol. 125, 460-462 (1980).
38. Saitoh, O. et al. Fecal eosinophil granule-derived proteins reflect disease activity in inflammatory bowel disease. Am. J. Gastroenterol. 94, 3513-3520 (1999).
39. Sangfelt, P., Carlson, M., Thorn, M., Loof, L. &Raab, Y. Neutrophil and eosinophil granule proteins as markers of response to local prednisolone treatment in distal ulcerative colitis and proctitis. Am. J. Gastroenterol. 96, 1085-1090 (2001).
40. Mir, A. et al. Elevated serum eotaxin levels in patients with inflammatory bowel disease. Am. J. Gastroenterol. 97, 1452-1457 (2002).
41. Smyth, C.M. et al. Activated eosinophils in association with enteric nerves in inflammatory bowel disease. PloS One 8, e64216 (2013).
42. Phongsisay, V. Campylobacter jejuni targets immunoglobulin-like receptor LMIR5. Mol. Immunol. 63, 574-578 (2015).
43. Simhadri, V.R., Andersen, J.F., Calvo, E., Choi, S.C., Coligan, J.E. &Borrego, F. Human CD300a binds to phosphatidylethanolamine and phosphatidylserine, and modulates the phagocytosis of dead cells. Blood 119, 2799-2809 (2012).
44. Fischbeck, A. et al. Sphingomyelin induces cathepsin D-mediated apoptosis in intestinal epithelial cells and increases inflammation in DSS colitis. Gut 60, 55-65 (2011).
45. Pizarro, T.T., Arseneau, K.O., Bamias, G. &Cominelli, F. Mouse models for the study of Crohn's disease. Trends Mol. Med. 9, 218-222 (2003).
46. Sands, B.E. From symptom to diagnosis: clinical distinctions among various forms of intestinal inflammation. Gastroenterology 126, 1518-1532 (2004).
47. Becker, C., Fantini, M.C. &Neurath, M.F. High resolution colonoscopy in live mice. Nat. Protoc. 1, 2900-2904 (2006).
48. Baruch-Morgenstern, N.B. et al. Paired immunoglobulin-like receptor A is an intrinsic, self-limiting suppressor of IL-5-induced eosinophil development. Nat. Immunol. 15, 36-44 (2013).
49. Karo-Atar, D., Moshkovits, I., Eickelberg, O., Konigshoff, M. &Munitz, A. Paired immunoglobulin-like receptor-B inhibits pulmonary fibrosis by suppressing profibrogenic properties of alveolar macrophages. Am. J. Respir. Cell Mol. Biol. 48, 456-464 (2013).
50. Bachelet, I., Munitz, A., Moretta, A., Moretta, L. &Levi-Schaffer, F. The inhibitory receptor IRp60 (CD300a) is expressed and functional on human mast cells. J. Immunol. 175, 7989-7995 (2005).