Paired immunoglobulin-like receptor-B inhibits pulmonary fibrosis by suppressing profibrogenic properties of alveolar macrophages

American Journal of Respiratory Cell and Molecular Biology

Volumn 48, Issue 4, 2013, Pages 456-464

  Karo Atar, Danielle ^a   Moshkovits, Itay ^a   Eickelberg, Oliver ^b   Königshoff, Melanie ^b   Munitz, Ariel ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

Author keywords

Idiopathic pulmonary fibrosis; IL 4; Lung; Macrophage; Paired immunoglobulin like receptor B

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; BLEOMYCIN; COLLAGEN; IMMUNOGLOBULIN LIKE RECEPTOR B; IMMUNOGLOBULIN RECEPTOR; INTERLEUKIN 13; INTERLEUKIN 4; LEUKOCYTE IMMUNOGLOBULIN LIKE RECEPTOR SUBFAMILY B MEMBER 3; MACROPHAGE ELASTASE; OSTEOPONTIN; RESISTIN; RESISTIN LIKE MOLECULE ALPHA; TISSUE INHIBITOR OF METALLOPROTEINASE 1; UNCLASSIFIED DRUG; ANTINEOPLASTIC ANTIBIOTIC; PIRB PROTEIN, MOUSE; RETNLA PROTEIN, MOUSE; SIGNAL PEPTIDE; TIMP1 PROTEIN, MOUSE;

ADULT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; BONE MARROW CELL; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FIBROGENESIS; FIBROSING ALVEOLITIS; FLOW CYTOMETRY; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LEUKOCYTE DIFFERENTIAL COUNT; LUNG ALVEOLUS MACROPHAGE; LUNG BIOPSY; LUNG INFILTRATE; LUNG PARENCHYMA; MACROPHAGE ACTIVATION; MALE; MOUSE; NONHUMAN; PATHOGENESIS; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; UPREGULATION; WILD TYPE; ANIMAL; BIOSYNTHESIS; CHEMICALLY INDUCED DISORDER; DRUG EFFECT; GENETICS; LUNG FIBROSIS; METABOLISM; MOUSE MUTANT; PATHOLOGY;

ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; BLEOMYCIN; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; INTERLEUKIN-4; MACROPHAGE ACTIVATION; MACROPHAGES, ALVEOLAR; MATRIX METALLOPROTEINASE 12; MICE; MICE, KNOCKOUT; PULMONARY FIBROSIS; RECEPTORS, IMMUNOLOGIC; TISSUE INHIBITOR OF METALLOPROTEINASE-1; UP-REGULATION;

MLCS; MLOWN;

EID: 84878249878     PISSN: 10441549     EISSN: 15354989     Source Type: Journal    
DOI: 10.1165/rcmb.2012-0329OC     Document Type: Article

References (52)

1. Fernandez Perez ER, Daniels CE, Schroeder DR, St Sauver J, Hartman TE, Bartholmai BJ, Yi ES, Ryu JH. Incidence, prevalence, and clinical course of idiopathic pulmonary fibrosis: a population-based study. Chest 2010;137: 129-137.
2. Wynn TA. Il-13 effector functions. Annu Rev Immunol 2003;21: 425-456.
3. Wynn TA, Ramalingam TR. Mechanisms of fibrosis: therapeutic translation for fibrotic disease. Nat Med 2012;18: 1028-1040.
4. Herbert DR, Orekov T, Perkins C, Rothenberg ME, Finkelman FD. IL-4R alpha expression by bone marrow-derived cells is necessary and sufficient for host protection against acute schistosomiasis. J Immunol 2008;180: 4948-4955.
5. Herbert DR, Holscher C, Mohrs M, Arendse B, Schwegmann A, Radwanska M, Leeto M, Kirsch R, Hall P, Mossmann H, et al. Alternative macrophage activation is essential for survival during schistosomiasis and downmodulates T helper 1 responses and immunopathology. Immunity 2004;20: 623-635.
6. Pesce JT, Ramalingam TR, Mentink-Kane MM, Wilson MS, El Kasmi KC, Smith AM, Thompson RW, Cheever AW, Murray PJ, Wynn TA. Arginase-1-expressing macrophages suppress Th2 cytokine-driven inflammation and fibrosis. PLoS Pathog 2009;5:e1000371.
7. Nair MG, Du Y, Perrigoue JG, Zaph C, Taylor JJ, Goldschmidt M, Swain GP, Yancopoulos GD, Valenzuela DM, Murphy A, et al. Alternatively activated macrophage-derived RELM-{alpha} is a negative regulator of Type 2 inflammation in the lung. J Exp Med 2009; 206: 937-952.
8. Huaux F, Liu T, McGarry B, Ullenbruch M, Phan SH. Dual roles of IL-4 in lung injury and fibrosis. J Immunol 2003;170: 2083-2092.
9. Prasse A, Pechkovsky DV, Toews GB, Jungraithmayr W, Kollert F, Goldmann T, Vollmer E, Muller-Quernheim J, Zissel G. A vicious circle of alveolar macrophages and fibroblasts perpetuates pulmonary fibrosis via CCL18. Am J Respir Crit Care Med 2006;173: 781-792.
10. Niese KA, Chiaramonte MG, Ellies LG, Rothenberg ME, Zimmermann N. The cationic amino acid transporter 2 is induced in inflammatory lung models and regulates lung fibrosis. Respir Res 2010;11:87.
11. Murray LA, Chen Q, Kramer MS, Hesson DP, Argentieri RL, Peng X, Gulati M, Homer RJ, Russell T, van Rooijen N, et al. TGF-beta driven lung fibrosis is macrophage dependent and blocked by serum amyloid P. Int J Biochem Cell Biol 2011;43: 154-162.
12. Yamaji-Kegan K, Su Q, Angelini DJ, Myers AC, Cheadle C, Johns RA. Hypoxia-induced mitogenic factor (HIMF/FIZZ1/RELMalpha) increases lung inflammation and activates pulmonary microvascular endothelial cells via an IL-4-dependent mechanism. J Immunol 2010; 185: 5539-5548.
13. Gordon S. Alternative activation of macrophages. Nat Rev Immunol 2003;3: 23-35.
14. Junttila IS, Mizukami K, Dickensheets H, Meier-Schellersheim M, Yamane H, Donnelly RP, Paul WE. Tuning sensitivity to IL-4 and IL-13: differential expression of IL-4Ralpha, IL-13Ralpha1, and gammaC regulates relative cytokine sensitivity. J Exp Med 2008;205: 2595-2608.
15. Niese KA, Collier AR, Hajek AR, Cederbaum SD, O'Brien WE, Wills- Karp M, Rothenberg ME, Zimmermann N. Bone marrow cell derived arginase I is the major source of allergen-induced lung arginase but is not required for airway hyperresponsiveness, remodeling and lung inflammatory responses in mice. BMC Immunol 2009;10:33.
16. Kubagawa H, Burrows PD, Cooper MD. A novel pair of immunoglobulinlike receptors expressed by B cells and myeloid cells. Proc Natl Acad Sci USA 1997;94: 5261-5266.
17. Kubagawa H, Chen CC, Ho LH, Shimada TS, Gartland L, Mashburn C, Uehara T, Ravetch JV, Cooper MD. Biochemical nature and cellular distribution of the paired immunoglobulin-like receptors, PIR-A and PIR-B. J Exp Med 1999;189: 309-318.
18. Munitz A, McBride ML, Bernstein JS, Rothenberg ME. A dual activation and inhibition role for the paired immunoglobulin-like receptor B in eosinophils. Blood 2008;111: 5694-5703.
19. Pereira S, Zhang H, Takai T, Lowell CA. The inhibitory receptor PIR-B negatively regulates neutrophil and macrophage integrin signaling. J Immunol 2004;173: 5757-5765.
20. Ma G, Pan PY, Eisenstein S, Divino CM, Lowell CA, Takai T, Chen SH. Paired immunoglobulin-like receptor-B regulates the suppressive function and fate of myeloid-derived suppressor cells. Immunity 2011; 34: 385-395.
21. Nakayama M, Underhill DM, Petersen TW, Li B, Kitamura T, Takai T, Aderem A. Paired Ig-like receptors bind to bacteria and shape TLRmediated cytokine production. J Immunol 2007;178: 4250-4259.
22. Takai T, Ono M. Activating and inhibitory nature of the murine paired immunoglobulin-like receptor family. Immunol Rev 2001;181: 215-222.
23. Ujike A, Takeda K, Nakamura A, Ebihara S, Akiyama K, Takai T. Impaired dendritic cell maturation and increased T(h)2 responses in PIR-B(2/2) mice. Nat Immunol 2002;3: 542-548.
24. Munitz A, Brandt EB, Mingler M, Finkelman FD, Rothenberg ME. Distinct roles for IL-13 and IL-4 via IL-13 receptor alpha1 and the Type II IL-4 receptor in asthma pathogenesis. Proc Natl Acad Sci USA 2008;105: 7240-7245.
25. Munitz A, Cole ET, Karo-Atar D, Finkelman FD, Rothenberg ME. Resistin-like molecule-alpha regulates IL-13-induced chemokine production but not allergen-induced airway responses. Am J Respir Cell Mol Biol 2012;46: 703-713.
26. Finkelman FD, Madden KB, Morris SC, Holmes JM, Boiani N, Katona IM, Maliszewski CR. Anti-cytokine antibodies as carrier proteins: prolongation of in vivo effects of exogenous cytokines by injection of cytokine-anti-cytokine antibody complexes. J Immunol 1993;151: 1235-1244.
27. Munitz A, Cole ET, Beichler A, Groschwitz K, Ahrens R, Steinbrecher K, Willson T, Han X, Denson L, Rothenberg ME, et al. Paired immunoglobulin-like receptor B (PIR-B) negatively regulates macrophage activation in experimental colitis. Gastroenterology 2010;139: 530-541.
28. Konigshoff M, Kramer M, Balsara N, Wilhelm J, Amarie OV, Jahn A, Rose F, Fink L, Seeger W, Schaefer L, et al. Wnt1-inducible signaling protein-1 mediates pulmonary fibrosis in mice and is upregulated in humans with idiopathic pulmonary fibrosis. J Clin Invest 2009;119: 772-787.
29. de Heer HJ, Hammad H, Soullie T, Hijdra D, Vos N, Willart MA, Hoogsteden HC, Lambrecht BN. Essential role of lung plasmacytoid dendritic cells in preventing asthmatic reactions to harmless inhaled antigen. J Exp Med 2004;200: 89-98.
30. Yamashita Y, Fukuta D, Tsuji A, Nagabukuro A, Matsuda Y, Nishikawa Y, Ohyama Y, Ohmori H, Ono M, Takai T. Genomic structures and chromosomal location of p91, a novel murine regulatory receptor family. J Biochem 1998;123: 358-368.
31. Takai T. A novel recognition system for MHC Class I molecules constituted by PIR. Adv Immunol 2005;88: 161-192.
32. Wynn TA. Cellular and molecular mechanisms of fibrosis. J Pathol 2008; 214: 199-210.
33. Lawson WE, Polosukhin VV, Zoia O, Stathopoulos GT, Han W, Plieth D, Loyd JE, Neilson EG, Blackwell TS. Characterization of fibroblastspecific protein 1 in pulmonary fibrosis. Am J Respir Crit Care Med 2005;171: 899-907.
34. Takahashi F, Takahashi K, Okazaki T, Maeda K, Ienaga H, Maeda M, Kon S, Uede T, Fukuchi Y. Role of osteopontin in the pathogenesis of bleomycin-induced pulmonary fibrosis. Am J Respir Cell Mol Biol 2001;24: 264-271.
35. Lambrecht BN, Hammad H. Lung dendritic cells in respiratory viral infection and asthma: from protection to immunopathology. Annu Rev Immunol 2012;30: 243-270.
36. Raes G, De Baetselier P, Noel W, Beschin A, Brombacher F, Hassanzadeh G. Differential expression of FIZZ1 and YM1 in alternatively versus classically activated macrophages. J Leukoc Biol 2002;71: 597-602.
37. Wilson MS, Wynn TA. Pulmonary fibrosis: pathogenesis, etiology and regulation. Mucosal Immunol 2009;2: 103-121.
38. Vernon MA, Mylonas KJ, Hughes J. Macrophages and renal fibrosis. Semin Nephrol 2010;30: 302-317.
39. Lohmann-Matthes ML, Steinmuller C, Franke-Ullmann G. Pulmonary macrophages. Eur Respir J 1994;7: 1678-1689.
40. Nieuwenhuizen NE, Kirstein F, Jayakumar J, Emedi B, Hurdayal R, Horsnell WG, Lopata AL, Brombacher F. Allergic airway disease is unaffected by the absence of IL-4Ralpha-dependent alternatively activated macrophages. J Allergy Clin Immunol 2012;130: 743-750.
41. Dhaliwal K, Scholefield E, Ferenbach D, GibbonsM, Duffin R, Dorward DA, Morris AC, Humphries D, Mackinnon A, Wilkinson TS, et al. Monocytes control second-phase neutrophil emigration in established lipopolysaccharide-induced murine lung injury. Am J Respir Crit Care Med 2012;186: 514-524.
42. Murray LA, Rosada R, Moreira AP, Joshi A, Kramer MS, Hesson DP, Argentieri RL, Mathai S, Gulati M, Herzog EL, et al. Serum amyloid P therapeutically attenuates murine bleomycin-induced pulmonary fibrosis via its effects on macrophages. PLoS ONE 2010;5:e9683.
43. Solinas G, Schiarea S, Liguori M, Fabbri M, Pesce S, Zammataro L, Pasqualini F, Nebuloni M, Chiabrando C, Mantovani A, et al. Tumorconditioned macrophages secrete migration-stimulating factor: a new marker for M2-polarization, influencing tumor cell motility. J Immunol 2010;185: 642-652.
44. Lee CG, Homer RJ, Zhu Z, Lanone S, Wang X, Koteliansky V, Shipley JM, Gotwals P, Noble P, Chen Q, et al. Interleukin-13 induces tissue fibrosis by selectively stimulating and activating transforming growth factor beta(1). J Exp Med 2001;194: 809-821.
45. Zheng T, Zhu Z, Wang Z, Homer RJ, Ma B, Riese RJ Jr, Chapman HA Jr, Shapiro SD, Elias JA. Inducible targeting of IL-13 to the adult lung causes matrix metalloproteinase- and cathepsin-dependent emphysema. J Clin Invest 2000;106: 1081-1093.
46. Tsoutsou PG, Gourgoulianis KI, Petinaki E, Germenis A, Tsoutsou AG, Mpaka M, Efremidou S, Molyvdas PA. Cytokine levels in the sera of patients with idiopathic pulmonary fibrosis. RespirMed 2006;100: 938-945.
47. Hardie WD, Glasser SW, Hagood JS. Emerging concepts in the pathogenesis of lung fibrosis. Am J Pathol 2009;175: 3-16.
48. Liu T, Jin H, Ullenbruch M, Hu B, Hashimoto N, Moore B, McKenzie A, Lukacs NW, Phan SH. Regulation of found in inflammatory zone 1 expression in bleomycin-induced lung fibrosis: role of IL-4/IL-13 and mediation via STAT-6. J Immunol 2004;173: 3425-3431.
49. Gordon S, Martinez FO. Alternative activation of macrophages: mechanism and functions. Immunity 2010;32: 593-604.
50. Zhang H, Meng F, Chu CL, Takai T, Lowell CA. The Src family kinases HCK and FGR negatively regulate neutrophil and dendritic cell chemokine signaling via PIR-B. Immunity 2005;22: 235-246.
51. Huynh OA, Hampartzoumian T, Arm JP, Hunt J, Borges L, Ahern M, Smith M, Geczy CL, McNeil HP, Tedla N. Down-regulation of leucocyte immunoglobulin-like receptor expression in the synovium of rheumatoid arthritis patients after treatment with disease-modifying anti-rheumatic drugs. Rheumatology (Oxford) 2007;46: 742-751.
52. Tedla N, Lee CW, Borges L, Geczy CL, Arm JP. Differential expression of leukocyte immunoglobulin-like receptors on cord-blood-derived human mast cell progenitors and mature mast cells. J Leukoc Biol 2008;83: 334-343.