Soluble LILRA3, a potential natural antiinflammatory protein, is increased in patients with rheumatoid arthritis and is tightly regulated by interleukin 10, tumor necrosis factor-α, and interferon-γ

Journal of Rheumatology

Volumn 37, Issue 8, 2010, Pages 1596-1606

  An, Hongyan ^a   Chandra, Vasudha ^a   Piraino, Barbara ^a   Borges, Luis ^b   Geczy, Carolyn ^a   McNeil, H Patrick ^a,c   Bryant, Katherine ^a,c   Tedla, Nicodemus ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b AMGEN INC   (United States)

^c LIVERPOOL HOSPITAL   (Australia)

Author keywords

Cytokines; enzyme linked immunosorbent assay; Leukocyte immunoglobulin like receptor A3; Rheumatoid arthritis

Indexed keywords

CELL RECEPTOR; CYTOKINE; DNA; GAMMA INTERFERON; IMMUNOGLOBULIN RECEPTOR; INTERLEUKIN 10; LEUKOCYTE IMMUNOGLOBULIN LIKE RECEPTOR A3; MESSENGER RNA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ADULT; ARTICLE; CHRONIC DISEASE; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; GOUT; HUMAN; INCIDENCE; INFLAMMATION; LEUKOCYTE; MALE; MAST CELL; MONOCYTE; MULTIPLE SCLEROSIS; OSTEOARTHRITIS; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RHEUMATOID ARTHRITIS; SERUM; SJOEGREN SYNDROME; WESTERN BLOTTING;

ADULT; AGED; ARTHRITIS, RHEUMATOID; CELLS, CULTURED; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; GENE EXPRESSION; HEALTH STATUS; HUMANS; INTERFERON-GAMMA; INTERLEUKIN-10; MALE; MAST CELLS; MIDDLE AGED; MONOCYTES; RECEPTORS, IMMUNOLOGIC; RNA, MESSENGER; SEVERITY OF ILLNESS INDEX; SYNOVIAL FLUID; TUMOR NECROSIS FACTOR-ALPHA; UP-REGULATION;

EID: 77955480482     PISSN: 0315162X     EISSN: None     Source Type: Journal    
DOI: 10.3899/jrheum.091119     Document Type: Article

References (60)

1. Brown D, Trowsdale J, Allen R. Review: The LILR family: Modulators of innate and adaptive immune pathways in health and disease. Tissue Antigens 2004;64:215-25.
2. Norman PJ, Carey BS, Stephens HA, Vaughan RW. DNA sequence variation and molecular genotyping of natural killer leukocyte immunoglobulin-like receptor, LILRA3. Immunogenetics 2003;55:165-71.
3. Anderson KJ, Allen RL. Regulation of T-cell immunity by leucocyte immunoglobulin-like receptors: innate immune receptors for self on antigen presenting cells. Immunology 2009;127:8-17.
4. Borges L, Hsu ML, Fanger N, Kubin M, Cosman D. A family of human lymphoid and myeloid Ig-like receptors, some of which bind to MHC class I molecules. J Immunol 1997;159:5192-6.
5. Samaridis J, Colonna M. Cloning of novel immunoglobulin superfamily receptors expressed on human myeloid and lymphoid cells. Eur J Immunol 1997;27:660-5.
6. Borges L, Cosman D. Mini review: LIRs/ILTs/MIRs, inhibitory and stimulatory Ig-superfamily receptors expressed in myeloid and lymphoid cells. Cytokine Growth Factor Rev 2000;11:209-17.
7. Colonna M, Nakajima H, Navarro F, Lopez-Botet M. A novel family of Ig-like receptors for HLA class I molecules that modulate function of lymphoid and myeloid cells. J Leuk Biol 1999;66:375-81.
8. Fanger NA, Cosman D, Peterson L, Braddy SC, Maliszewski CR, Borges L. The MHC class I binding proteins LIR-1 and LIR-2 inhibit Fc receptor mediated signaling in monocytes. Eur J Immunol 1998;28:3423-34.
9. Nakajima H, Samaridis J, Angman L, Colonna M. Human myeloid cells express an activating ILT receptor (ILT1) that associates with FC receptor gamma - chain. J Immunol 1999;162:5-8.
10. Borges L, Kubin M, Kuhlman T. LIR9, an Ig-superfamily activating receptor is expressed as transmembrane and a secreted molecule. Blood 2003;101:1484-6.
11. Wilson MJ, Torkar M, Haude A, Milne S, Jones T, Sheer D, et al. Plasticity in the organization and sequences of human KIR/ILT gene families. Proc Natl Acad Sci USA 2000;97:4778-83.
12. Torkar M, Haude A, Milne S, Beck S, Trowsdale J, Wilson MJ. Arrangement of the ILT gene cluster: a common null allele of the ILT6 gene results from a 6.7-kbp deletion. Eur J Immunol 2000;30:3655-62.
13. Norman PJ, Cook J, Carey MA, Carrington BS, Verity CVF, Hameed DH, et al. SNP haplotypes and allele frequencies show evidence for disruptive and balancing selection in the human leukocyte receptor complex. Immunogenetics 2004;56:225-37.
14. Norman PJ, Stephens HA, Vaughan RW. DNA sequence variation and molecular genotyping of natural killer leukocyte immunoglobulin-like receptor, LILRA3. Immunogenetics 2004;55:165-71.
15. Hirayasu K, Ohashi J, Kashiwase K, Takanashi M, Satake M, Tokunaga K, et al. Long-term persistence of both functional and non-functional alleles at the leukocyte immunoglobulin-like receptor A3 (LILRA3) locus suggests balancing selection. Hum Genetics 2006;119:436-43.
16. Colonna M, Samaridis J, Cella M, Angman L, Allen RL, O'Callaghan CA, et al. Human myelomonocytic cells express an inhibitory receptor for classical and nonclassical MHC class I molecules. J Immunol 1998;160:3096-100.
17. Cosman D, Fanger N, Borges L, Kubin M, Chin W, Peterson L, et al. A novel immunoglobulin superfamily receptor for cellular and viral MHC class I molecules. Immunity 1997;7:273-82.
18. Allen RL, Raine T, Haude A, Trowsdale J, Wilson MJ. Leukocyte receptor complex-encoded immunomodulatory receptors show differing specificity for alternative HLA-B27 structures. J Immunol 2001;167:5543-7.
19. Nakayama M, Underhill DM, Petersen TW, Li B, Kitamura T, Takai T, et al. Paired immunoglobulin-like receptors bind to bacteria and shape TLR-mediated cytokine production. J Immunol 2007;178:4250-59.
20. Atwal JK, Pinkston-Gosse J, Syken J, Stawicki S, Wu Y, Shatz C, et al. PirB is a functional receptor for myelin inhibitors of axonal regeneration. Science 2008;322:967-70.
21. Cao W, Bover L, Cho M, Wen X, Hanbuchi S, Bao M, et al. Regulation of TLR7/9 responses in plasmacytoid dendritic cells by BST2 and ILT7 receptor interaction. J Exp Med 2009;206:1603-14.
22. Tedla N, Bandeira-Melo C, Tassinari P, Sloane DE, Samplaski M, Cosman D, et al. The activation of human eosinophils by leukocyte immunoglobulin-like receptor-7 (ILT-1). Proc Natl Acad Sci USA 2003;100:1174-9.
23. Cao W, Rosen DB, Ito T, Bover L, Bao M, Wanatabe G, et al. Plasmacytoid dendritic cell-specific receptor ILT7-FceRI inhibit Toll-like receptor-induced interferon production. J Exp Med 2006;203:1399-405.
24. Chang CC, Ciubotariu R, Manavalan JS, Yuan J, Colovai AI, Piazza F, et al. Tolerization of dendritic cells by T(S) cells: the crucial role of inhibitory receptors ILT3 and ILT4. Nat Immunol 2002;3:237-43.
25. Cella M, Dohring C, Samaridis J, Dessing M, Brockhaus M, Lanzavecchia A, et al. A novel inhibitory receptor (ILT3) expressed on monocytes, macrophages, and dendritic cells involved in antigen processing. J Exp Med 1997;185:1743-51.
26. Zhou J, Friend DS, Feldweg AM, Daheshia M, Li L, Austen KF, et al. Prevention of LPS induced microangiopathy by gp49B1: evidence for an important role for gp49B1 expression on neutrophils. J Exp Med 2003;198:1243-51.
27. Tak PP, Bresnihan B. The pathogenesis and prevention of joint damage in rheumatoid arthritis: advances from synovial biopsy and tissue analysis. Arthritis Rheum 2000;43:2619-33.
28. Bromley M, Wooley DE. Histopathology of the rheumatoid lesion. Identification of cell types at sites of cartilage erosion. Arthritis Rheum 1984;27:857-63.
29. Tedla N, Gibson K, McNeil HP, Cosman D, Borges L, Arm JP. The co-expression of activating and inhibitory leukocyte immunoglobulin-like receptors in rheumatoid synovium. Am J Pathol 2002;160:425-31.
30. Mitchell A, Rentero C, Endoh Y, Hsu K, Gaus K, Geczy CL, et al. LILRA5 is expressed by synovial tissue macrophages in rheumatoid arthritis, selectively induces pro-inflammatory cytokines and IL-10 and is regulated by TNF-α, IL-10 and IFN-γ. Eur J Immunol 2008;38:3459-73.
31. Huynh OA, Hampartzoumian T, Arm JP, Hunt J, Borges L, Ahern M, et al. Down-regulation of leucocyte immunoglobulin-like receptor expression in the synovium of rheumatoid arthritis patients after treatment with disease-modifying anti-rheumatic drugs. Rheumatology 2007;46:742-51.
32. Arnett FC, Edworthy SM, Bloch DA, McShane DJ, Fries JF, Cooper NS, et al. The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum 1987;31:315-24.
33. Prevoo ML, van 't Hof MA, Kuper HH, van Leeuwen MA, van de Putte LB, van Riel PL. Modified disease activity scores that include twenty-eight-joint counts. Development and validation in a prospective longitudinal study of patients with rheumatoid arthritis. Arthritis Rheum 1995;38:44-8.
34. van Gestel AM, Prevoo ML, van 't Hof MA, van Rijswijk MH, van de Putte LB, van Riel PL. Development and validation of the European League Against Rheumatism response criteria for rheumatoid arthritis. Comparison with the preliminary American College of Rheumatology and the World Health Organization/International League Against Rheumatism Criteria. Arthritis Rheum 1996;39:34-40.
35. 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;83:334-43.
36. Mitchell A, Rentero C, Endoh Y, Hsu K, Gaus K, Geczy CL, et al. LILRA5 is expressed by synovial tissue macrophages in rheumatoid arthritis, selectively induces pro-inflammatory cytokines and IL-10 and is regulated by TNF-α, IL-10 and IFN-γ. Eur J Immunol 2008;38:3459-73.
37. Pietruczuk A, Swierzbinska R, Pancewicz S, Pietruczuk M, Hermanowska-Szpakowicz T. Serum levels of interleukin-18 (IL-18), interleukin-1β (IL-1β), its soluble receptor sIL-1RII and C-reactive protein (CRP) in patients with Lyme arthritis. Infection 2006;34:158-62.
38. Van Zee KJ, Kohno T, Fischer E, Rock CS, Moldawer LL, Lowry SF. Tumor necrosis factor soluble receptors circulate during experimental and clinical inflammation and can protect against excessive tumor necrosis factor alpha in vitro and in vivo. Proc Natl Acad Sci USA 1992;89:4845-9.
39. Itoh Y, Okanoue T, Ohnishi N, Sakamoto M, Nishioji K, Nakagawa Y, et al. Serum levels of soluble tumor necrosis factor receptors and effects of interferon therapy in patients with chronic hepatitis C virus infection. Am J Gastroenterol 1999;94:1332-40.
40. Ohkubo T, Takei M, Mitamura K, Horie T, Fujiwara S, Shimizu K, et al. Increased soluble CD4 molecules and the role of soluble CD4 production in patients with rheumatoid arthritis. J Int Med Res 2001;29:488-96.
41. Kitchens RL, Thompson PA, Viriyakosol S, O'Keefe GE, Munford RS. Plasma CD14 decreases monocyte responses to LPS by transferring cell-bound LPS to plasma lipoproteins. J Clin Invest 2001;108:485-93.
42. Cope AP, Aderka D, Doherty M, Engelmann H, Gibbons D, Jones AC, et al. Increased levels of soluble tumor necrosis factor receptors in the sera and synovial fluid of patients with rheumatic diseases. Arthritis Rheum 1992;35:1160-9.
43. Barrera P, Boerbooms AM, Janssen EM, Sauerwein RW, Gallati H, Mulder J, et al. Circulating soluble tumor necrosis factor receptors, interleukin-2 receptors, tumor necrosis factor α, and interleukin-6 levels in rheumatoid arthritis. Longitudinal evaluation during methotrexate and azathioprine therapy. Arthritis Rheum 1993;36:1070-9.
44. Mattey DL, Glossop JR, Nixon NB, Dawes PT. Circulating levels of tumor necrosis factor receptors are highly predictive of mortality in patients with rheumatoid arthritis. Arthritis Rheum 2007;56:3940-8.
45. Davas EM, Tsirogianni A, Kappou I, Karamitsos D, Economidou I, Dantis PC. Serum IL-6, TNFα, p55 srTNFα, p75srTNFα, srIL-2 levels and disease activity in systemic lupus erythematosus. Clin Rheumatol 1999;18:17-22.
46. Gabay C, Cakir N, Moral F, Roux-Lombard P, Meyer O, Dayer JM, et al. Circulating levels of tumor necrosis factor soluble receptors in systemic lupus erythematosus are significantly higher than in other rheumatic diseases and correlate with disease activity. J Rheumatol 1997;24:303-8.
47. Rieckmann P, Martin S, Weichselbraun I, Albrecht M, Kitze B, Weber T, et al. Serial analysis of circulating adhesion molecules and TNF receptor in serum from patients with multiple sclerosis: A cICAM-1 is an indicator for relapse. Neurology 1994;44:2367-72.
48. Koch S, Goedde R, Nigmatova V, Epplen JT, Müller N, de Seze J, et al. Brief communication: association of multiple sclerosis with ILT6 deficiency. Genes Immun 2005;6:445-7.
49. Ordonez D, Sánchez AJ, Martínez-Rodríguez JE, Cisneros E, Ramil E, Romo N, et al. Multiple sclerosis associates with LILRA3 deletion in Spanish patients. Genes Immun 2009;10:579-85.
50. Kabalak G, Dobberstein SB, Matthias T, Reuter S, The YH, Dorner T, et al. Association of immunoglobulin-like transcript 6 deficiency with Sjogren's syndrome. Arthritis Rheum 2009;60:2923-5.
51. Jung M, Sabat R, Krätzschmar J, Seidel H, Wolk K, Schönbein C, et al. Expression profiling of IL-10-regulated genes in human monocytes and peripheral blood mononuclear cells from psoriatic patients during IL-10 therapy. Eur J Immunol 2004;34:481-93.
52. Wisniewski A, Luszczek W, Manczak M, Jasek M, Kubicka W, Cislo M, et al. Distribution of LILRA3 (ILT6/LIR4) deletion in psoriatic patients and healthy controls. Hum Immunol 2003;64:458-61.
53. Kabalak G, Dobberstein SB, Matthias T, Reuter S, The YH, Dorner T, et al. Association of immunoglobulin-like transcript 6 deficiency with Sjogren's syndrome. Arthritis Rheum 2009;60:2923-5.
54. Moore KW, de Waal Malefyt R, Coffman RL, O'Garra A. Interleukin-10 and the interleukin-10 receptor. Annu Rev Immunol 2001;19:683-765.
55. Pestka S, Krause CD, Sarkar D, Walter MR, Shi Y, Fisher PB. Interleukin-10 and related cytokines and receptors. Annu Rev Immunol 2004;22:929-79.
56. te Velde AA, de Waal Malefijt R, Huijbens RJ, de Vries JE, Figdor CG. IL-10 stimulates monocyte Fcγ R surface expression and cytotoxic activity. Distinct regulation of antibody-dependent cellular cytotoxicity by IFN-γ, IL-4, and IL-10. J Immunol 1992;149:4048-52.
57. Calzada-Wack JC, Frankenberger M, Ziegler-Heitbrock HW. Interleukin-10 drives human monocytes to CD16 positive macrophages. J Inflamm 1996;46:78-85.
58. Buechler C, Ritter M, Orsó E, Langmann T, Klucken J, Schmitz G. Regulation of scavenger receptor CD163 expression in human monocytes and macrophages by pro- and antiinflammatory stimuli. J Leuk Biol 2000;67:97-103.
59. Beinhauer BG, McBride JM, Graf P, Pursch E, Bongers M, Rogy M, et al. Interleukin 10 regulates cell surface and soluble LIR-2 (CD85d) expression on dendritic cells resulting in T cell hyporesponsiveness in vitro. Eur J immunol 2004;34:74-80.
60. Hart PH, Hunt EK, Bonder CS, Watson CJ, Finlay-Jones JJ. Regulation of surface and soluble TNF receptor expression on human monocytes and synovial fluid macrophages by IL-4 and IL-10. J Immunol 1996;157:3672-80.