Paired immunoglobulin-like receptor A is an intrinsic, self-limiting suppressor of IL-5-induced eosinophil development

Nature Immunology

Volumn 15, Issue 1, 2014, Pages 36-44

  Baruch Morgenstern, Netali Ben ^a   Shik, Dana ^a   Moshkovits, Itay ^a   Itan, Michal ^a   Karo Atar, Danielle ^a   Bouffi, Carine ^b   Fulkerson, Patricia C ^b   Rashkovan, Diana ^c   Jung, Steffen ^c   Rothenberg, Marc E ^b   Munitz, Ariel ^a  

^a TEL AVIV UNIVERSITY   (Israel)

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

^c WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

BETA 2 MICROGLOBULIN; BIM PROTEIN; GROWTH FACTOR RECEPTOR BOUND PROTEIN 2; IMMUNOGLOBULIN RECEPTOR; INTERLEUKIN 5; MITOGEN ACTIVATED PROTEIN KINASE; PAIRED IMMUNOGLOBULIN LIKE RECEPTOR A; PAIRED IMMUNOGLOBULIN LIKE RECEPTOR B; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; BONE MARROW; CELL PROLIFERATION; CONTROLLED STUDY; EOSINOPHIL; EOSINOPHILIA; IN VITRO STUDY; LOEFFLER PNEUMONIA; MOUSE; NONHUMAN; PRIORITY JOURNAL; RECOGNITION; TH2 CELL;

EID: 84891018837     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.2757     Document Type: Article

References (48)

1. Nishinakamura, R. et al. Mice deficient for the IL-3/GM-CSF/IL-5 beta c receptor exhibit lung pathology and impaired immune response, while beta IL3 receptor-deficient mice are normal. Immunity 2, 211-222 (1995).
2. Sanderson, C.J. Interleukin-5, eosinophils, and disease. Blood 79, 3101-3109 (1992).
3. Collins, P.D., Marleau, S., Griffiths Johnson, D.A., Jose, P.J. & Williams, T.J. Cooperation between interleukin-5 and the chemokine eotaxin to induce eosinophil accumulation in vivo. J. Exp. Med. 182, 1169-1174 (1995).
4. Rothenberg, M.E. et al. IL-5-dependent conversion of normodense human eosinophils to the hypodense phenotype uses 3T3 fibroblasts for enhanced viability, accelerated hypodensity, and sustained antibody-dependent cytotoxicity. J. Immunol. 143, 2311-2316 (1989). (Pubitemid 19245203)
5. Rothenberg, M.E. & Hogan, S.P. The eosinophil. Annu. Rev. Immunol. 24, 147-174 (2006).
6. Wu, D. et al. Eosinophils sustain adipose alternatively activated macrophages associated with glucose homeostasis. Science 332, 243-247 (2011).
7. Rosenberg, H.F., Dyer, K.D. & Foster, P.S. Eosinophils: changing perspectives in health and disease. Nat. Rev. Immunol. 13, 9-22 (2013).
8. Chu, V.T. et al. Eosinophils are required for the maintenance of plasma cells in the bone marrow. Nat. Immunol. 12, 151-159 (2011).
9. Starr, T.K., Jameson, S.C. & Hogquist, K.A. Positive and negative selection of T cells. Annu. Rev. Immunol. 21, 139-176 (2003). (Pubitemid 37174529)
10. Ljunggren, H.G. & Karre, K. In search of the 'missing self': MHC molecules and NK cell recognition. Immunol. Today 11, 237-244 (1990). (Pubitemid 20198988)
11. Takai, T. Paired immunoglobulin-like receptors and their MHC class I recognition. Immunology 115, 433-440 (2005). (Pubitemid 41032431)
12. Kubagawa, H. et al. Biochemical nature and cellular distribution of the paired immunoglobulin-like receptors, PIR-A and PIR-B. J. Exp. Med. 189, 309-318 (1999).
13. Nakamura, A., Kobayashi, E. & Takai, T. Exacerbated graft-versus-host disease in Pirb-/- mice. Nat. Immunol. 5, 623-629 (2004). (Pubitemid 38811887)
14. Maeda, A., Kurosaki, M. & Kurosaki, T. Paired immunoglobulin-like receptor (PIR)-A is involved in activating mast cells through its association with Fc receptor gamma chain. J. Exp. Med. 188, 991-995 (1998). (Pubitemid 28433426)
15. Blery, M. et al. The paired Ig-like receptor PIR-B is an inhibitory receptor that recruits the protein-tyrosine phosphatase SHP-1. Proc. Natl. Acad. Sci. USA 95, 2446-2451 (1998). (Pubitemid 28145961)
16. Ujike, A. et al. Impaired dendritic cell maturation and increased T(H)2 responses in PIR-B(-/-) mice. Nat. Immunol. 3, 542-548 (2002). (Pubitemid 34662306)
17. Wheadon, H., Paling, N.R. & Welham, M.J. Molecular interactions of SHP1 and SHP2 in IL-3-signalling. Cell. Signal. 14, 219-229 (2002). (Pubitemid 34102451)
18. Mitsuhashi, Y. et al. Regulation of plasmacytoid dendritic cell responses by PIR-B. Blood 120, 3256-3259 (2012).
19. Munitz, A., McBride, M.L., Bernstein, J.S. & Rothenberg, M.E. A dual activation and inhibition role for the paired immunoglobulin-like receptor B in eosinophils. Blood 111, 5694-5703 (2008).
20. Dyer, K.D. et al. Functionally competent eosinophils differentiated ex vivo in high purity from normal mouse bone marrow. J. Immunol. 181, 4004-4009 (2008).
21. Iwasaki, H. et al. Identification of eosinophil lineage-committed progenitors in the murine bone marrow. J. Exp. Med. 201, 1891-1897 (2005). (Pubitemid 41002925)
22. Moshkovits, I. et al. CMRF35-like molecule 1 (CLM-1) regulates eosinophil homeostasis by suppressing cellular chemotaxis. Mucosal Immunol. doi:10.1038/mi.2013.47 (3 July 2013).
23. Uehara, T. et al. Inhibition of IgE-mediated mast cell activation by the paired Ig-like receptor PIR-B. J. Clin. Invest. 108, 1041-1050 (2001). (Pubitemid 32946078)
24. 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).
25. Voehringer, D., van Rooijen, N. & Locksley, R.M. Eosinophils develop in distinct stages and are recruited to peripheral sites by alternatively activated macrophages. J. Leukoc. Biol. 81, 1434-1444 (2007). (Pubitemid 46827966)
26. Bouillet, P. & O'Reilly, L.A. CD95, BIM and T cell homeostasis. Nat. Rev. Immunol. 9, 514-519 (2009).
27. Kopf, M. et al. IL-5-deficient mice have a developmental defect in CD5+ B-1 cells and lack eosinophilia but have normal antibody and cytotoxic T cell responses. Immunity 4, 15-24 (1996).
28. Rennick, D.M. et al. In vivo administration of antibody to interleukin-5 inhibits increased generation of eosinophils and their progenitors in bone marrow of parasitized mice. Blood 76, 312-316 (1990). (Pubitemid 20225520)
29. Rosenberg, H.F., Phipps, S. & Foster, P.S. Eosinophil trafficking in allergy and asthma. J. Allergy Clin. Immunol. 119, 1303-1310 (2007). (Pubitemid 46855872)
30. Tomaki, M. et al. Eosinophilopoiesis in a murine model of allergic airway eosinophilia: involvement of bone marrow IL-5 and IL-5 receptor alpha. J. Immunol. 165, 4040-4050 (2000). (Pubitemid 32057316)
31. Matsushita, H. et al. Differential but competitive binding of Nogo protein and class I major histocompatibility complex (MHCI) to the PIR-B ectodomain provides an inhibition of cells. J. Biol. Chem. 286, 25739-25747 (2011).
32. Kessels, H.W., Ward, A.C. & Schumacher, T.N. Specificity and affinity motifs for Grb2 SH2-ligand interactions. Proc. Natl. Acad. Sci. USA 99, 8524-8529 (2002). (Pubitemid 34693595)
33. Varol, C., Landsman, L. & Jung, S. Probing in vivo origins of mononuclear phagocytes by conditional ablation and reconstitution. Methods Mol. Biol. 531, 71-87 (2009).
34. van Rijt, L.S. et al. In vivo depletion of lung CD11c- dendritic cells during allergen challenge abrogates the characteristic features of asthma. J. Exp. Med. 201, 981-991 (2005). (Pubitemid 40524467)
35. Lanier, L.L. NK cell recognition. Annu. Rev. Immunol. 23, 225-274 (2005). (Pubitemid 40563170)
36. Ho, L.H., Uehara, T., Chen, C.C., Kubagawa, H. & Cooper, M.D. Constitutive tyrosine phosphorylation of the inhibitory paired Ig-like receptor PIR-B. Proc. Natl. Acad. Sci. USA 96, 15086-15090 (1999). (Pubitemid 30019769)
37. van den Berg, T.K. & van der Schoot, C.E. Innate immune 'self' recognition: a role for CD47-SIRPalpha interactions in hematopoietic stem cell transplantation. Trends Immunol. 29, 203-206 (2008).
38. 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).
39. Yang, D. et al. 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. 205, 79-90 (2008). (Pubitemid 351185717)
40. Lee, J.J., Jacobsen, E.A., McGarry, M.P., Schleimer, R.P. & Lee, N.A. Eosinophils in health and disease: the LIAR hypothesis. Clin. Exp. Allergy 40, 563-575 (2010).
41. Bochner, B.S. Verdict in the case of therapies versus eosinophils: the jury is still out. J. Allergy Clin. Immunol. 113, 3-9, quiz 10 (2004).
42. Kano, G., Almanan, M., Bochner, B.S. & Zimmermann, N. Mechanism of Siglec-8-mediated cell death in IL-5-activated eosinophils: Role for reactive oxygen species-enhanced MEK/ERK activation. J. Allergy Clin. Immunol. 132, 437-445 (2013).
43. Munitz, A. et al. The inhibitory receptor IRp60 (CD300a) suppresses the effects of IL-5, GM-CSF, and eotaxin on human peripheral blood eosinophils. Blood 107, 1996-2003 (2006). (Pubitemid 43289383)
44. Chu, J., Liu, Y., Koretzky, G.A. & Durden, D.L. SLP-76-Cbl-Grb2-Shc interactions in FcgammaRI signaling. Blood 92, 1697-1706 (1998).
45. Kanamaru, Y. et al. IgA Fc receptor I signals apoptosis through the FcRγ ITAM and affects tumor growth. Blood 109, 203-211 (2007). (Pubitemid 46070122)
46. Zuo, L. et al. IL-13 induces esophageal remodeling and gene expression by an eosinophil-independent, IL-13R alpha 2-inhibited pathway. J. Immunol. 185, 660-669 (2010).
47. Koller, B.H., Marrack, P., Kappler, J.W. & Smithies, O. Normal development of mice deficient in beta 2M, MHC class I proteins, and CD8+ T cells. Science 248, 1227-1230 (1990).
48. Sapoznikov, A. & Jung, S. Probing in vivo dendritic cell functions by conditional cell ablation. Immunol. Cell Biol. 86, 409-415 (2008). (Pubitemid 351948212)