Macrophages from the synovium of active rheumatoid arthritis exhibit an activin a-dependent pro-inflammatory profile

Journal of Pathology

Volumn 235, Issue 3, 2015, Pages 515-526

  Palacios, Blanca Soler ^a   Estrada Capetillo, Lizbeth ^a   Izquierdo, Elena ^b   Criado, Gabriel ^c   Nieto, Concha ^b   Municio, Cristina ^a   González Alvaro, Isidoro ^d   Sánchez Mateos, Paloma ^a,e   Pablos, Jose Luis ^c   Corbí, Angel L ^b   Puig Kröger, Amaya ^a,f  

^a HOSPITAL GENERAL UNIVERSITARIO GREGORIO MARAÑÓN   (Spain)

^b CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^c HOSPITAL UNIVERSITARIO 12 DE OCTUBRE   (Spain)

^d HOSPITAL UNIVERSITARIO DE LA PRINCESA   (Spain)

^e SCHOOL OF MEDICINE   (Spain)

^f HOSPITAL GENERAL UNIVERSITARIO GREGORIO MARAÑÓN   (Spain)

Author keywords

Activin a; Macrophages; Rheumatoid arthritis; Synovial fluid

Indexed keywords

ACTIVIN A; CD14 ANTIGEN; CHEMOKINE RECEPTOR CCR2; HITR2B PROTEIN; MACROPHAGE ELASTASE; MEMBRANE PROTEIN; SMAD PROTEIN; SOMATOMEDIN C; UNCLASSIFIED DRUG; ACTIVIN; CCR2 PROTEIN, HUMAN; EGLN3 PROTEIN, HUMAN; HYPOXIA INDUCIBLE FACTOR PROLINE DIOXYGENASE; TRANSCRIPTOME;

ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; EX VIVO STUDY; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE; IN VITRO STUDY; INFLAMMATION; MACROPHAGE; MONOCYTE; PHENOTYPE; POLARIZATION; PRIORITY JOURNAL; RHEUMATOID ARTHRITIS; SYNOVIAL FLUID; SYNOVIUM; TRANSCRIPTOMICS; ADULT; AGED; CELL CULTURE; FEMALE; MALE; METABOLISM; MIDDLE AGED; PATHOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ACTIVINS; ADULT; AGED; ANTIGENS, CD14; ARTHRITIS, RHEUMATOID; CELLS, CULTURED; FEMALE; HUMANS; HYPOXIA-INDUCIBLE FACTOR-PROLINE DIOXYGENASES; IN VITRO TECHNIQUES; INFLAMMATION; MACROPHAGES; MALE; MATRIX METALLOPROTEINASE 12; MIDDLE AGED; PHENOTYPE; RECEPTORS, CCR2; SIGNAL TRANSDUCTION; SMAD PROTEINS; SYNOVIAL MEMBRANE; TRANSCRIPTOME;

EID: 84920761647     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.4466     Document Type: Article

References (50)

1. Choy EH, Panayi GS. Cytokine pathways and joint inflammation in rheumatoid arthritis. N Engl J Med 2001; 344: 907-916.
2. Brennan FM, McInnes IB. Evidence that cytokines play a role in rheumatoid arthritis. J Clin Invest 2008; 118: 3537-3545.
3. Mulherin D, Fitzgerald O, Bresnihan B. Synovial tissue macrophage populations and articular damage in rheumatoid arthritis. Arthritis Rheum 1996; 39: 115-124.
4. Hamilton JA, Tak PP. The dynamics of macrophage lineage populations in inflammatory and autoimmune diseases. Arthritis Rheum 2009; 60: 1210-1221.
5. Haringman JJ, Gerlag DM, Zwinderman AH, et al. Synovial tissue macrophages: a sensitive biomarker for response to treatment in patients with rheumatoid arthritis. Ann Rheum Dis 2005; 64: 834-838.
6. Wijbrandts CA, Vergunst CE, Haringman JJ, et al. Absence of changes in the number of synovial sublining macrophages after ineffective treatment for rheumatoid arthritis: implications for use of synovial sublining macrophages as a biomarker. Arthritis Rheum 2007; 56: 3869-3871.
7. Gordon S, Taylor PR. Monocyte and macrophage heterogeneity. Nat Rev Immunol 2005; 5: 953-964.
8. Stout RD, Jiang C, Matta B, et al. Macrophages sequentially change their functional phenotype in response to changes in microenvironmental influences. J Immunol 2005; 175: 342-349.
9. Hamilton JA. Colony-stimulating factors in inflammation and autoimmunity. Nat Rev Immunol 2008; 8: 533-544.
10. Akagawa KS. Functional heterogeneity of colony-stimulating factorinduced human monocyte-derivedmacrophages. Int J Hematol 2002; 76: 27-34.
11. Verreck FA, de Boer T, Langenberg DM, et al. Human IL-23-producing type 1 macrophages promote but IL-10-producing type 2 macrophages subvert immunity to (myco)bacteria. Proc Natl Acad Sci USA 2004; 101: 4560-4565.
12. Sierra-Filardi E, Puig-Kroger A, Blanco FJ, et al. Activin A skews macrophage polarization by promoting a proinflammatory phenotype and inhibiting the acquisition of anti-inflammatory macrophage markers. Blood 2011; 117: 5092-5101.
13. Lacey DC, Achuthan A, Fleetwood AJ, et al. Defining GM-CSFand macrophage-CSF-dependent macrophage responses by in vitro models. J Immunol 2012; 188: 5752-5765.
14. Pollard JW. Trophic macrophages in development and disease. Nat Rev Immunol 2009; 9: 259-270.
15. Campbell IK, Rich MJ, Bischof RJ, et al. Protection from collagen-induced arthritis in granulocyte-macrophage colonystimulating factor-deficient mice. J Immunol 1998; 161: 3639-3644.
16. Campbell IK, Rich MJ, Bischof RJ, et al. The colony-stimulating factors and collagen-induced arthritis: exacerbation of disease by M-CSF and G-CSF and requirement for endogenous M-CSF. J Leukoc Biol 2000; 68: 144-150.
17. Cook AD, Braine EL, Campbell IK, et al. Blockade of collageninduced arthritis post-onset by antibody to granulocyte-macrophage colony-stimulating factor (GM-CSF): requirement for GM-CSF in the effector phase of disease. Arthritis Res 2001; 3: 293-298.
18. Li J, Hsu HC, Mountz JD. Managing macrophages in rheumatoid arthritis by reform or removal. Curr Rheumatol Rep 2012; 14: 445-454.
19. Puig-Kroger A, Sierra-Filardi E, Dominguez-Soto A, et al. Folate receptor-β is expressed by tumor-associated macrophages and constitutes a marker for M2 anti-inflammatory/regulatory macrophages. Cancer Res 2009; 69: 9395-9403.
20. Nagayoshi R, Nagai T, Matsushita K, et al. Effectiveness of anti-folate receptor-β antibody conjugated with truncated Pseudomonas exotoxin in the targeting of rheumatoid arthritis synovial macrophages. Arthritis Rheum 2005; 52: 2666-2675.
21. Dominguez-Soto A, Sierra-Filardi E, Puig-Kroger A, et al. Dendritic cell-specific ICAM-3-grabbing nonintegrin expression on M2-polarized and tumor-associated macrophages is macrophage-CSF dependent and enhanced by tumor-derived IL-6 and IL-10. J Immunol 2011; 186: 2192-2200.
22. Escribese MM, Sierra-Filardi E, Nieto C, et al. The prolyl hydroxylase PHD3 identifies proinflammatory macrophages and its expression is regulated by activin A. J Immunol 2012; 189: 1946-1954.
23. Sturn A, Quackenbush J, Trajanoski Z. Genesis: cluster analysis of microarray data. Bioinformatics 2002; 18: 207-208.
24. Buechler C, Ritter M, Orso E, et al. Regulation of scavenger receptor CD163 expression in human monocytes and macrophages by pro- and antiinflammatory stimuli. J Leukoc Biol 2000; 67: 97-103.
25. Cairo G, Recalcati S, Mantovani A, et al. Iron trafficking and metabolism inmacrophages: contribution to the polarized phenotype. Trends Immunol 2011; 32: 241-247.
26. Estecha A, Aguilera-Montilla N, Sanchez-Mateos P, et al. RUNX3 regulates intercellular adhesion molecule 3 (ICAM-3) expression duringmacrophage differentiation and monocyte extravasation. PLoS One 2012; 7: e33313.
27. Puig-Kroger A, Serrano-Gomez D, Caparros E, et al. Regulated expression of the pathogen receptor dendritic cell-specific intercellular adhesion molecule 3 (ICAM-3)-grabbing nonintegrin in THP-1 human leukemic cells, monocytes, and macrophages. J Biol Chem 2004; 279: 25680-25688.
28. Biswas SK, Mantovani A. Orchestration of metabolism by macrophages. Cell Metab 2012; 15: 432-437.
29. de las Casas-Engel M, Dominguez-Soto A, Sierra-Filardi E, et al. Serotonin skews human macrophage polarization through HTR2B and HTR7. J Immunol 2013; 190: 2301-2310.
30. Sierra-Filardi E, Vega MA, Sanchez-Mateos P, et al. Heme oxygenase-1 expression in M-CSF-polarized M2 macrophages contributes to LPS-induced IL-10 release. Immunobiology 2010; 215: 788-795.
31. Recalcati S, Locati M, Marini A, et al. Differential regulation of iron homeostasis during human macrophage polarized activation. Eur J Immunol 2010; 40: 824-835.
32. Zabel BA, Ohyama T, Zuniga L, et al. Chemokine-like receptor 1 expression by macrophages in vivo: regulation by TGFβ and TLR ligands. Exp Hematol 2006; 34: 1106-1114.
33. Biswas SK, Allavena P, Mantovani A. Tumor-associated macrophages: functional diversity, clinical significance, and open questions. Semin Immunopathol 2013; 35: 585-600.
34. Samaniego R, Palacios BS, Domiguez-Soto A, et al. Macrophage uptake and accumulation of folates are polarization-dependent in vitro and in vivo and are regulated by activin A. J Leukoc Biol 2014; 95: 797-808.
35. Massague J. TGFβ signalling in context. Nat Rev Mol Cell Biol 2012; 13: 616-630.
36. Dong F, He X. Activin A: a potential therapeutic target for characterizing and stopping joint pain early in rheumatoid arthritis patients. Inflammation 2014; 37: 170-176.
37. Michel U, Gerber J, A EOC, et al. Increased activin levels in cerebrospinal fluid of rabbits with bacterial meningitis are associated with activation of microglia. J Neurochem 2003; 86: 238-245.
38. Shao L, Frigon NL Jr, Young AL, et al. Effect of activin A on globin gene expression in purified human erythroid progenitors. Blood 1992; 79: 773-781.
39. Sica A, Mantovani A.Macrophage plasticity and polarization: in vivo veritas. J Clin Invest 2012; 122: 787-795.
40. Chawla A, Nguyen KD, Goh YP. Macrophage-mediated inflammation in metabolic disease. Nat Rev Immunol 2011; 11: 738-749.
41. Ambarus CA, Noordenbos T, de Hair MJ, et al. Intimal lining layer macrophages but not synovial sublining macrophages display an IL-10 polarized-like phenotype in chronic synovitis. Arthritis Res Ther 2012; 14: R74.
42. Vandooren B, Noordenbos T, Ambarus C, et al. Absence of a classically activated macrophage cytokine signature in peripheral spondylarthritis, including psoriatic arthritis. Arthritis Rheum 2009; 60: 966-975.
43. Segura E, Touzot M, Bohineust A, et al. Human inflammatory dendritic cells induce Th17 cell differentiation. Immunity 2013; 38: 336-348.
44. Wang X, Liang J, Koike T, et al. Overexpression of human matrix metalloproteinase-12 enhances the development of inflammatory arthritis in transgenic rabbits. Am J Pathol 2004; 165: 1375-1383.
45. Katschke KJ Jr, Rottman JB, Ruth JH, et al. Differential expression of chemokine receptors on peripheral blood, synovial fluid, and synovial tissuemonocytes/macrophages in rheumatoid arthritis. Arthritis Rheum 2001; 44: 1022-1032.
46. Quinones MP, Ahuja SK, Jimenez F, et al. Experimental arthritis in CC chemokine receptor 2-null mice closely mimics severe human rheumatoid arthritis. J Clin Invest 2004; 113: 856-866.
47. Paleolog EM. Angiogenesis in rheumatoid arthritis. Arthritis Res 2002; 4(suppl 3): S81-90.
48. El-Gendi SS, Moniem AE, Tawfik NM, et al. Value of serum and synovial fluid activin A and inhibin A in some rheumatic diseases. Int J Rheum Dis 2010; 13: 273-279.
49. Ota F, Maeshima A, Yamashita S, et al. Activin A induces cell proliferation of fibroblast-like synoviocytes in rheumatoid arthritis. Arthritis Rheum 2003; 48: 2442-2449.
50. Hedger MP, de Kretser DM. The activins and their binding protein, follistatin - diagnostic and therapeutic targets in inflammatory disease and fibrosis. Cytokine Growth Factor Rev 2013; 24: 285-295.