Skip to main content
Top
Published in: Journal of Inflammation 1/2013

Open Access 01-12-2013 | Research

Cross-linking of IgGs bound on circulating neutrophils leads to an activation of endothelial cells: possible role of rheumatoid factors in rheumatoid arthritis-associated vascular dysfunction

Authors: Emmanuelle Rollet-Labelle, Myriam Vaillancourt, Louis Marois, Marianna M Newkirk, Patrice E Poubelle, Paul H Naccache

Published in: Journal of Inflammation | Issue 1/2013

Login to get access

Abstract

Background

Rheumatoid arthritis is characterized by the presence of circulating auto-antibodies, including rheumatoid factors, which recognize the Fc portion of IgGs. The neutrophil is the most abundant circulating leukocyte and it expresses high levels of FcγRs on its surface. The aim of the present study was to examine the capacity of circulating human neutrophils to be activated by rheumatoid factors and the consequences of these events on endothelium.

Methods

Neutrophil-bound IgGs were cross-linked with anti-human IgGs to mimick the presence of circulating rheumatoid factors and FcγRs-dependent signalling events and functions were examined. The IgG and IgM composition of rheumatoid factors isolated from the serum of RA patients was characterized. Adhesion of neutrophils to endothelial cells was quantified in response to the addition of rheumatoid factors.

Results

Cross-linking of IgGs bound on neutrophils leads to FcγRs-dependent tyrosine phosphorylation, mobilisation of intracellular calcium and the extracellular release of superoxide anions and lysozyme. Incubation of endothelial cells with the supernatant of activated neutrophils increases ICAM-1 expression and IL-8 production by endothelial cells. Finally, rheumatoid factors enhance neutrophil adhesion to endothelial cells.

Conclusions

Our results show that activation of neutrophils’ FcγRs by rheumatoid factors could participate in rheumatoid arthritis-associated vascular damage.
Appendix
Available only for authorised users
Literature
1.
go back to reference Turesson C, Matteson EL: Vasculitis in rheumatoid arthritis. Curr Opin Rheumatol. 2009, 21: 35-40. 10.1097/BOR.0b013e32831c5303.PubMedCrossRef Turesson C, Matteson EL: Vasculitis in rheumatoid arthritis. Curr Opin Rheumatol. 2009, 21: 35-40. 10.1097/BOR.0b013e32831c5303.PubMedCrossRef
2.
go back to reference Doyle MK: Vasculitis associated with connective tissue disorders. Curr Rheumatol Rep. 2006, 8: 312-316. 10.1007/s11926-006-0015-5.PubMedCrossRef Doyle MK: Vasculitis associated with connective tissue disorders. Curr Rheumatol Rep. 2006, 8: 312-316. 10.1007/s11926-006-0015-5.PubMedCrossRef
3.
go back to reference Gabriel SE, Crowson CS, Kremers HM, Doran MF, Turesson C, O'Fallon WM, Matteson EL: Survival in rheumatoid arthritis: a population-based analysis of trends over 40 years. Arthritis Rheum. 2003, 48: 54-58. 10.1002/art.10705.PubMedCrossRef Gabriel SE, Crowson CS, Kremers HM, Doran MF, Turesson C, O'Fallon WM, Matteson EL: Survival in rheumatoid arthritis: a population-based analysis of trends over 40 years. Arthritis Rheum. 2003, 48: 54-58. 10.1002/art.10705.PubMedCrossRef
4.
go back to reference Fietta P, Delsante G: Atherogenesis in rheumatoid arthritis: the "rheumatoid vasculopathy"?. Acta Biomed. 2009, 80: 177-186.PubMed Fietta P, Delsante G: Atherogenesis in rheumatoid arthritis: the "rheumatoid vasculopathy"?. Acta Biomed. 2009, 80: 177-186.PubMed
5.
go back to reference Moreland LW, Curtis JR: Systemic nonarticular manifestations of rheumatoid arthritis: focus on inflammatory mechanisms. Semin Arthritis Rheum. 2009, 39: 132-143. 10.1016/j.semarthrit.2008.08.003.PubMedCrossRef Moreland LW, Curtis JR: Systemic nonarticular manifestations of rheumatoid arthritis: focus on inflammatory mechanisms. Semin Arthritis Rheum. 2009, 39: 132-143. 10.1016/j.semarthrit.2008.08.003.PubMedCrossRef
6.
go back to reference Murdaca G, Colombo BM, Cagnati P, Gulli R, Spanò F, Puppo F: Endothelial dysfunction in rheumatic autoimmune diseases. Atherosclerosis. 2012, 224: 309-317. 10.1016/j.atherosclerosis.2012.05.013.PubMedCrossRef Murdaca G, Colombo BM, Cagnati P, Gulli R, Spanò F, Puppo F: Endothelial dysfunction in rheumatic autoimmune diseases. Atherosclerosis. 2012, 224: 309-317. 10.1016/j.atherosclerosis.2012.05.013.PubMedCrossRef
7.
go back to reference Song YW, Kang EH: Autoantibodies in rheumatoid arthritis: rheumatoid factors and anticitrullinated protein antibodies. QJM. 2010, 103: 139-146. 10.1093/qjmed/hcp165.PubMedPubMedCentralCrossRef Song YW, Kang EH: Autoantibodies in rheumatoid arthritis: rheumatoid factors and anticitrullinated protein antibodies. QJM. 2010, 103: 139-146. 10.1093/qjmed/hcp165.PubMedPubMedCentralCrossRef
8.
go back to reference Svensson L, Jirholt J, Holmdahl R, Jansson L: B cell-deficient mice do not develop type II collagen-induced arthritis (CIA). Clin Exp Immunol. 1998, 111: 521-526. 10.1046/j.1365-2249.1998.00529.x.PubMedPubMedCentralCrossRef Svensson L, Jirholt J, Holmdahl R, Jansson L: B cell-deficient mice do not develop type II collagen-induced arthritis (CIA). Clin Exp Immunol. 1998, 111: 521-526. 10.1046/j.1365-2249.1998.00529.x.PubMedPubMedCentralCrossRef
9.
go back to reference Stuart J, Dixon FJ: Serum transfer of collagen-induced arthritis in mice. J Exp Med. 1983, 158: 378-392. 10.1084/jem.158.2.378.PubMedCrossRef Stuart J, Dixon FJ: Serum transfer of collagen-induced arthritis in mice. J Exp Med. 1983, 158: 378-392. 10.1084/jem.158.2.378.PubMedCrossRef
10.
go back to reference Sutton B, Corper A, Bonagura V, Taussig M: The structure and origin of rheumatoid factors. Immunol Today. 2000, 21: 177-183. 10.1016/S0167-5699(00)01589-9.PubMedCrossRef Sutton B, Corper A, Bonagura V, Taussig M: The structure and origin of rheumatoid factors. Immunol Today. 2000, 21: 177-183. 10.1016/S0167-5699(00)01589-9.PubMedCrossRef
11.
go back to reference Stoop JW, Zegers BJ, Sander PC, Ballieux RE: Serum immunoglobulin levels in healthy children and adults. Clin Exp Immunol. 1969, 4: 101-112.PubMedPubMedCentral Stoop JW, Zegers BJ, Sander PC, Ballieux RE: Serum immunoglobulin levels in healthy children and adults. Clin Exp Immunol. 1969, 4: 101-112.PubMedPubMedCentral
12.
go back to reference Ali H, Haribabu B, Richardson RM, Snyderman R: Mechanisms of inflammation and leukocyte activation. Med Clin North Am. 1997, 81: 1-28. 10.1016/S0025-7125(05)70503-4.PubMedCrossRef Ali H, Haribabu B, Richardson RM, Snyderman R: Mechanisms of inflammation and leukocyte activation. Med Clin North Am. 1997, 81: 1-28. 10.1016/S0025-7125(05)70503-4.PubMedCrossRef
13.
go back to reference Tsuboi N, Asano K, Lauterbach M, Mayadas TN: Human neutrophil Fcgamma receptors initiate and play specialized nonredundant roles in antibody-mediated inflammatory diseases. Immunity. 2008, 28: 833-846. 10.1016/j.immuni.2008.04.013.PubMedPubMedCentralCrossRef Tsuboi N, Asano K, Lauterbach M, Mayadas TN: Human neutrophil Fcgamma receptors initiate and play specialized nonredundant roles in antibody-mediated inflammatory diseases. Immunity. 2008, 28: 833-846. 10.1016/j.immuni.2008.04.013.PubMedPubMedCentralCrossRef
14.
go back to reference Nathan C: Neutrophils and immunity: challenges and opportunities. Nat Rev Immunol. 2006, 6: 173-182. 10.1038/nri1785.PubMedCrossRef Nathan C: Neutrophils and immunity: challenges and opportunities. Nat Rev Immunol. 2006, 6: 173-182. 10.1038/nri1785.PubMedCrossRef
15.
go back to reference Robinson JI, Carr IM, Cooper DL, Rashid LH, Martin SG, Emery P, Isaacs JD, Barton A, Wilson AG, Barrett JH, Morgan AW: Confirmation of association of FCGR3B but not FCGR3A copy number with susceptibility to autoantibody positive rheumatoid arthritis. Hum Mutat. 2012, 33: 741-749. 10.1002/humu.22031.PubMedCrossRef Robinson JI, Carr IM, Cooper DL, Rashid LH, Martin SG, Emery P, Isaacs JD, Barton A, Wilson AG, Barrett JH, Morgan AW: Confirmation of association of FCGR3B but not FCGR3A copy number with susceptibility to autoantibody positive rheumatoid arthritis. Hum Mutat. 2012, 33: 741-749. 10.1002/humu.22031.PubMedCrossRef
16.
go back to reference Tak PP, Smeets TJ, Daha MR, Kluin PM, Meijers KA, Brand R, Meinders AE, Breedveld FC: Analysis of the synovial cell infiltrate in early rheumatoid synovial tissue in relation to local disease activity. Arthritis Rheum. 1997, 40: 217-225. 10.1002/art.1780400206.PubMedCrossRef Tak PP, Smeets TJ, Daha MR, Kluin PM, Meijers KA, Brand R, Meinders AE, Breedveld FC: Analysis of the synovial cell infiltrate in early rheumatoid synovial tissue in relation to local disease activity. Arthritis Rheum. 1997, 40: 217-225. 10.1002/art.1780400206.PubMedCrossRef
17.
go back to reference Boross P, Verbeek JS: The complex role of Fcgamma receptors in the pathology of arthritis. Springer Semin Immunopathol. 2006, 28: 339-350. 10.1007/s00281-006-0049-9.PubMedCrossRef Boross P, Verbeek JS: The complex role of Fcgamma receptors in the pathology of arthritis. Springer Semin Immunopathol. 2006, 28: 339-350. 10.1007/s00281-006-0049-9.PubMedCrossRef
18.
go back to reference Tan Sardjono C, Mottram PL, van de Velde NC, Powell MS, Power D, Slocombe RF, Wicks IP, Campbell IK, McKenzie SE, Brooks M, Stevenson AW, Hogarth PM: Development of spontaneous multisystem autoimmune disease and hypersensitivity to antibody-induced inflammation in Fcgamma receptor IIa-transgenic mice. Arthritis Rheum. 2005, 52: 3220-3229. 10.1002/art.21344.PubMedCrossRef Tan Sardjono C, Mottram PL, van de Velde NC, Powell MS, Power D, Slocombe RF, Wicks IP, Campbell IK, McKenzie SE, Brooks M, Stevenson AW, Hogarth PM: Development of spontaneous multisystem autoimmune disease and hypersensitivity to antibody-induced inflammation in Fcgamma receptor IIa-transgenic mice. Arthritis Rheum. 2005, 52: 3220-3229. 10.1002/art.21344.PubMedCrossRef
19.
go back to reference Kleinau S, Martinsson P, Heyman B: Induction and suppression of collagen-induced arthritis is dependent on distinct fcgamma receptors. J Exp Med. 2000, 191: 1611-1616. 10.1084/jem.191.9.1611.PubMedPubMedCentralCrossRef Kleinau S, Martinsson P, Heyman B: Induction and suppression of collagen-induced arthritis is dependent on distinct fcgamma receptors. J Exp Med. 2000, 191: 1611-1616. 10.1084/jem.191.9.1611.PubMedPubMedCentralCrossRef
20.
go back to reference Van de Velde NC, Mottram PL, Powell MS, Lim B, Holmdahl R, Hogarth PM: Transgenic mice expressing human FcgammaRIIa have enhanced sensitivity to induced autoimmune arthritis as well as elevated Th17 cells. Immunol Lett. 2010, 130: 82-88. 10.1016/j.imlet.2009.12.005.PubMedCrossRef Van de Velde NC, Mottram PL, Powell MS, Lim B, Holmdahl R, Hogarth PM: Transgenic mice expressing human FcgammaRIIa have enhanced sensitivity to induced autoimmune arthritis as well as elevated Th17 cells. Immunol Lett. 2010, 130: 82-88. 10.1016/j.imlet.2009.12.005.PubMedCrossRef
21.
go back to reference Belostocki K, Park MS, Redecha PB, Masuda E, Salmon JE, Pricop L: FcgammaRIIa is a target for modulation by TNFalpha in human neutrophils. Clin Immunol. 2005, 117: 78-86. 10.1016/j.clim.2005.07.001.PubMedCrossRef Belostocki K, Park MS, Redecha PB, Masuda E, Salmon JE, Pricop L: FcgammaRIIa is a target for modulation by TNFalpha in human neutrophils. Clin Immunol. 2005, 117: 78-86. 10.1016/j.clim.2005.07.001.PubMedCrossRef
22.
go back to reference Mayadas TN, Tsokos GC, Tsuboi N: Mechanisms of immune complex-mediated neutrophil recruitment and tissue injury. Circulation. 2009, 120: 2012-2024. 10.1161/CIRCULATIONAHA.108.771170.PubMedPubMedCentralCrossRef Mayadas TN, Tsokos GC, Tsuboi N: Mechanisms of immune complex-mediated neutrophil recruitment and tissue injury. Circulation. 2009, 120: 2012-2024. 10.1161/CIRCULATIONAHA.108.771170.PubMedPubMedCentralCrossRef
23.
go back to reference Baetta R, Corsini A: Role of polymorphonuclear neutrophils in atherosclerosis: current state and future perspectives. Atherosclerosis. 2010, 210: 1-13. 10.1016/j.atherosclerosis.2009.10.028.PubMedCrossRef Baetta R, Corsini A: Role of polymorphonuclear neutrophils in atherosclerosis: current state and future perspectives. Atherosclerosis. 2010, 210: 1-13. 10.1016/j.atherosclerosis.2009.10.028.PubMedCrossRef
24.
go back to reference Norman MU, Van De Velde NC, Timoshanko JR, Issekutz A, Hickey MJ: Overlapping roles of endothelial selectins and vascular cell adhesion molecule-1 in immune complex-induced leukocyte recruitment in the cremasteric microvasculature. Am J Pathol. 2003, 163: 1491-1503. 10.1016/S0002-9440(10)63506-7.PubMedPubMedCentralCrossRef Norman MU, Van De Velde NC, Timoshanko JR, Issekutz A, Hickey MJ: Overlapping roles of endothelial selectins and vascular cell adhesion molecule-1 in immune complex-induced leukocyte recruitment in the cremasteric microvasculature. Am J Pathol. 2003, 163: 1491-1503. 10.1016/S0002-9440(10)63506-7.PubMedPubMedCentralCrossRef
25.
go back to reference Stokol T, O'Donnell P, Xiao L, Knight S, Stavrakis G, Botto M, von Andrian UH, Mayadas TN: C1q governs deposition of circulating immune complexes and leukocyte Fcgamma receptors mediate subsequent neutrophil recruitment. J Exp Med. 2004, 200: 835-846. 10.1084/jem.20040501.PubMedPubMedCentralCrossRef Stokol T, O'Donnell P, Xiao L, Knight S, Stavrakis G, Botto M, von Andrian UH, Mayadas TN: C1q governs deposition of circulating immune complexes and leukocyte Fcgamma receptors mediate subsequent neutrophil recruitment. J Exp Med. 2004, 200: 835-846. 10.1084/jem.20040501.PubMedPubMedCentralCrossRef
26.
go back to reference Skilbeck CA, Lu X, Sheikh S, Savage CO, Nash GB: Capture of flowing human neutrophils by immobilised immunoglobulin: roles of Fc-receptors CD16 and CD32. Cell Immunol. 2006, 241: 26-31. 10.1016/j.cellimm.2006.07.007.PubMedCrossRef Skilbeck CA, Lu X, Sheikh S, Savage CO, Nash GB: Capture of flowing human neutrophils by immobilised immunoglobulin: roles of Fc-receptors CD16 and CD32. Cell Immunol. 2006, 241: 26-31. 10.1016/j.cellimm.2006.07.007.PubMedCrossRef
27.
go back to reference Segel GB, Halterman MW, Lichtman MA: The paradox of the neutrophil's role in tissue injury. J Leukoc Biol. 2011, 89: 359-372. 10.1189/jlb.0910538.PubMedCrossRef Segel GB, Halterman MW, Lichtman MA: The paradox of the neutrophil's role in tissue injury. J Leukoc Biol. 2011, 89: 359-372. 10.1189/jlb.0910538.PubMedCrossRef
28.
go back to reference Rollet E, Caon AC, Roberge CJ, Liao NW, Malawista SE, McColl SR, Naccache PH: Tyrosine phosphorylation in activated human neutrophils -comparison of the effects of different classes of agonists and identification of the signaling pathways involved. J Immunol. 1994, 153: 353-363.PubMed Rollet E, Caon AC, Roberge CJ, Liao NW, Malawista SE, McColl SR, Naccache PH: Tyrosine phosphorylation in activated human neutrophils -comparison of the effects of different classes of agonists and identification of the signaling pathways involved. J Immunol. 1994, 153: 353-363.PubMed
29.
go back to reference van Mirre E, Teeling JL, van der Meer JW, Bleeker WK, Hack CE: Monomeric IgG in intravenous Ig preparations is a functional antagonist of FcgammaRII and FcgammaRIIIb. J Immunol. 2004, 173: 332-339.PubMedCrossRef van Mirre E, Teeling JL, van der Meer JW, Bleeker WK, Hack CE: Monomeric IgG in intravenous Ig preparations is a functional antagonist of FcgammaRII and FcgammaRIIIb. J Immunol. 2004, 173: 332-339.PubMedCrossRef
30.
go back to reference Desmeules P, Dufour M, Fernandes MJ: A rapid flow cytometry assay for the assessment of calcium mobilization in human neutrophils in a small volume of lysed whole-blood. J Immunol Methods. 2009, 340: 154-157. 10.1016/j.jim.2008.10.006.PubMedCrossRef Desmeules P, Dufour M, Fernandes MJ: A rapid flow cytometry assay for the assessment of calcium mobilization in human neutrophils in a small volume of lysed whole-blood. J Immunol Methods. 2009, 340: 154-157. 10.1016/j.jim.2008.10.006.PubMedCrossRef
31.
go back to reference Rollet-Labelle E, Marois S, Barbeau K, Malawista SE, Naccache PH: Recruitment of the cross-linked opsonic receptor CD32A (FcgammaRIIA) to high-density detergent-resistant membrane domains in human neutrophils. Biochem J. 2004, 381: 919-928. 10.1042/BJ20031808.PubMedPubMedCentralCrossRef Rollet-Labelle E, Marois S, Barbeau K, Malawista SE, Naccache PH: Recruitment of the cross-linked opsonic receptor CD32A (FcgammaRIIA) to high-density detergent-resistant membrane domains in human neutrophils. Biochem J. 2004, 381: 919-928. 10.1042/BJ20031808.PubMedPubMedCentralCrossRef
32.
go back to reference Fernandes MJ, Rollet-Labelle E, Pare G, Marois S, Tremblay ML, Teillaud JL, Naccache PH: CD16b associates with high-density, detergent-resistant membranes in human neutrophils. Biochem J. 2006, 393: 351-359. 10.1042/BJ20050129.PubMedPubMedCentralCrossRef Fernandes MJ, Rollet-Labelle E, Pare G, Marois S, Tremblay ML, Teillaud JL, Naccache PH: CD16b associates with high-density, detergent-resistant membranes in human neutrophils. Biochem J. 2006, 393: 351-359. 10.1042/BJ20050129.PubMedPubMedCentralCrossRef
33.
go back to reference Fernandes MJ, Lachance G, Pare G, Rollet-Labelle E, Naccache PH: Signaling through CD16b in human neutrophils involves the Tec family of tyrosine kinases. J Leukoc Biol. 2005, 78: 524-532. 10.1189/jlb.0804479.PubMedCrossRef Fernandes MJ, Lachance G, Pare G, Rollet-Labelle E, Naccache PH: Signaling through CD16b in human neutrophils involves the Tec family of tyrosine kinases. J Leukoc Biol. 2005, 78: 524-532. 10.1189/jlb.0804479.PubMedCrossRef
34.
go back to reference Fossati G, Bucknall RC, Edwards SW: Insoluble and soluble immune complexes activate neutrophils by distinct activation mechanisms: changes in functional responses induced by priming with cytokines. Ann Rheum Dis. 2002, 61: 13-19. 10.1136/ard.61.1.13.PubMedPubMedCentralCrossRef Fossati G, Bucknall RC, Edwards SW: Insoluble and soluble immune complexes activate neutrophils by distinct activation mechanisms: changes in functional responses induced by priming with cytokines. Ann Rheum Dis. 2002, 61: 13-19. 10.1136/ard.61.1.13.PubMedPubMedCentralCrossRef
35.
go back to reference Rollet-Labelle E, Gilbert C, Naccache PH: Modulation of human neutrophil responses to CD32 cross-linking by serine/threonine phosphatase inhibitors: Cross-talk between serine/threonine and tyrosine phosphorylation. J Immunol. 2000, 164: 1020-1028.PubMedCrossRef Rollet-Labelle E, Gilbert C, Naccache PH: Modulation of human neutrophil responses to CD32 cross-linking by serine/threonine phosphatase inhibitors: Cross-talk between serine/threonine and tyrosine phosphorylation. J Immunol. 2000, 164: 1020-1028.PubMedCrossRef
36.
go back to reference Ortiz-Stern A, Rosales C: Fc{gamma}RIIIB stimulation promotes {beta}1 integrin activation in human neutrophils. J Leukoc Biol. 2005, 77: 787-799. 10.1189/jlb.0504310.PubMedCrossRef Ortiz-Stern A, Rosales C: Fc{gamma}RIIIB stimulation promotes {beta}1 integrin activation in human neutrophils. J Leukoc Biol. 2005, 77: 787-799. 10.1189/jlb.0504310.PubMedCrossRef
37.
go back to reference Naccache PH, Jean N, Liao NW, Bator JM, McColl SR, Kubes P: Regulation of stimulated integrin surface expression in human neutrophils by tyrosine phosphorylation. Blood. 1994, 84: 616-624.PubMed Naccache PH, Jean N, Liao NW, Bator JM, McColl SR, Kubes P: Regulation of stimulated integrin surface expression in human neutrophils by tyrosine phosphorylation. Blood. 1994, 84: 616-624.PubMed
38.
go back to reference Kukulski F, Ben Yebdri F, Bahrami F, Fausther M, Tremblay A, Sevigny J: Endothelial P2Y2 receptor regulates LPS-induced neutrophil transendothelial migration in vitro. Mol Immunol. 2010, 47: 991-999. 10.1016/j.molimm.2009.11.020.PubMedCrossRef Kukulski F, Ben Yebdri F, Bahrami F, Fausther M, Tremblay A, Sevigny J: Endothelial P2Y2 receptor regulates LPS-induced neutrophil transendothelial migration in vitro. Mol Immunol. 2010, 47: 991-999. 10.1016/j.molimm.2009.11.020.PubMedCrossRef
39.
go back to reference Middleton J, Patterson AM, Gardner L, Schmutz C, Ashton BA: Leukocyte extravasation: chemokine transport and presentation by the endothelium. Blood. 2002, 100: 3853-3860. 10.1182/blood.V100.12.3853.PubMedCrossRef Middleton J, Patterson AM, Gardner L, Schmutz C, Ashton BA: Leukocyte extravasation: chemokine transport and presentation by the endothelium. Blood. 2002, 100: 3853-3860. 10.1182/blood.V100.12.3853.PubMedCrossRef
40.
go back to reference Alessandri C, Bombardieri M, Papa N, Cinquini M, Magrini L, Tincani A, Valesini G: Decrease of anti-cyclic citrullinated peptide antibodies and rheumatoid factor following anti-TNFalpha therapy (infliximab) in rheumatoid arthritis is associated with clinical improvement. Ann Rheum Dis. 2004, 63: 1218-1221. 10.1136/ard.2003.014647.PubMedPubMedCentralCrossRef Alessandri C, Bombardieri M, Papa N, Cinquini M, Magrini L, Tincani A, Valesini G: Decrease of anti-cyclic citrullinated peptide antibodies and rheumatoid factor following anti-TNFalpha therapy (infliximab) in rheumatoid arthritis is associated with clinical improvement. Ann Rheum Dis. 2004, 63: 1218-1221. 10.1136/ard.2003.014647.PubMedPubMedCentralCrossRef
41.
go back to reference Marois L, Pare G, Vaillancourt M, Rollet-Labelle E, Naccache PH: Fc{gamma}RIIIb Triggers Raft-dependent Calcium Influx in IgG-mediated Responses in Human Neutrophils. J Biol Chem. 2011, 286: 3509-3519. 10.1074/jbc.M110.169516.PubMedPubMedCentralCrossRef Marois L, Pare G, Vaillancourt M, Rollet-Labelle E, Naccache PH: Fc{gamma}RIIIb Triggers Raft-dependent Calcium Influx in IgG-mediated Responses in Human Neutrophils. J Biol Chem. 2011, 286: 3509-3519. 10.1074/jbc.M110.169516.PubMedPubMedCentralCrossRef
42.
go back to reference Lowry MB, Duchemin AM, Robinson JM, Anderson CL: Functional separation of pseudopod extension and particle internalization during Fc gamma receptor-mediated phagocytosis. J Exp Med. 1998, 187: 161-176. 10.1084/jem.187.2.161.PubMedPubMedCentralCrossRef Lowry MB, Duchemin AM, Robinson JM, Anderson CL: Functional separation of pseudopod extension and particle internalization during Fc gamma receptor-mediated phagocytosis. J Exp Med. 1998, 187: 161-176. 10.1084/jem.187.2.161.PubMedPubMedCentralCrossRef
43.
go back to reference Indik ZK, Park JG, Hunter S, Schreiber AD: The molecular dissection of Fc gamma receptor mediated phagocytosis. Blood. 1995, 86: 4389-4399.PubMed Indik ZK, Park JG, Hunter S, Schreiber AD: The molecular dissection of Fc gamma receptor mediated phagocytosis. Blood. 1995, 86: 4389-4399.PubMed
44.
go back to reference Hunter S, Kamoun M, Schreiber AD: Transfection of an Fc gamma receptor cDNA induces T cells to become phagocytic. Proc Nat Acad Sci USA. 1994, 91: 10232-10236. 10.1073/pnas.91.21.10232.PubMedPubMedCentralCrossRef Hunter S, Kamoun M, Schreiber AD: Transfection of an Fc gamma receptor cDNA induces T cells to become phagocytic. Proc Nat Acad Sci USA. 1994, 91: 10232-10236. 10.1073/pnas.91.21.10232.PubMedPubMedCentralCrossRef
45.
go back to reference Edberg JC, Salmon JE, Kimberly RP: Functional capacity of fcgamma receptor-III (CD16) on human neutrophils. Immunol Res. 1992, 11: 239-251. 10.1007/BF02919130.PubMedCrossRef Edberg JC, Salmon JE, Kimberly RP: Functional capacity of fcgamma receptor-III (CD16) on human neutrophils. Immunol Res. 1992, 11: 239-251. 10.1007/BF02919130.PubMedCrossRef
46.
go back to reference Edberg JC, Kimberly RP: Modulation of Fcgamma and complement receptor function by the glycosyl-phosphatidylinositol-anchored form of FcgammaRIII. J Immunol. 1994, 152: 5826-5835.PubMed Edberg JC, Kimberly RP: Modulation of Fcgamma and complement receptor function by the glycosyl-phosphatidylinositol-anchored form of FcgammaRIII. J Immunol. 1994, 152: 5826-5835.PubMed
47.
go back to reference Newkirk MM: Rheumatoid factors: what do they tell us?. J Rheumatol. 2002, 29: 2034-2040.PubMed Newkirk MM: Rheumatoid factors: what do they tell us?. J Rheumatol. 2002, 29: 2034-2040.PubMed
48.
go back to reference Nowak UM, Newkirk MM: Rheumatoid factors: good or bad for you?. Int Arch Allergy Immunol. 2005, 138: 180-188. 10.1159/000088794.PubMedCrossRef Nowak UM, Newkirk MM: Rheumatoid factors: good or bad for you?. Int Arch Allergy Immunol. 2005, 138: 180-188. 10.1159/000088794.PubMedCrossRef
49.
go back to reference Jarvis JN, Petty HR, Tang Y, Frank B, Tessier PA, Dozmorov I, Jiang K, Kindzelski A, Chen Y, Cadwell C, Turner M, McGhee JL, Centola M: Evidence for chronic, peripheral activation of neutrophils in polyarticular juvenile rheumatoid arthritis. Arthritis Res Ther. 2006, 8: R154-10.1186/ar2048.PubMedPubMedCentralCrossRef Jarvis JN, Petty HR, Tang Y, Frank B, Tessier PA, Dozmorov I, Jiang K, Kindzelski A, Chen Y, Cadwell C, Turner M, McGhee JL, Centola M: Evidence for chronic, peripheral activation of neutrophils in polyarticular juvenile rheumatoid arthritis. Arthritis Res Ther. 2006, 8: R154-10.1186/ar2048.PubMedPubMedCentralCrossRef
50.
go back to reference Fairhurst AM, Wallace PK, Jawad AS, Goulding NJ: Rheumatoid peripheral blood phagocytes are primed for activation but have impaired Fc-mediated generation of reactive oxygen species. Arthritis Res Ther. 2007, 9: R29-10.1186/ar2144.PubMedPubMedCentralCrossRef Fairhurst AM, Wallace PK, Jawad AS, Goulding NJ: Rheumatoid peripheral blood phagocytes are primed for activation but have impaired Fc-mediated generation of reactive oxygen species. Arthritis Res Ther. 2007, 9: R29-10.1186/ar2144.PubMedPubMedCentralCrossRef
51.
go back to reference Hewins P, Williams JM, Wakelam MJ, Savage CO: Activation of Syk in neutrophils by antineutrophil cytoplasm antibodies occurs via Fcgamma receptors and CD18. J Am Soc Nephrol. 2004, 15: 796-808. 10.1097/01.ASN.0000113241.98702.77.PubMedCrossRef Hewins P, Williams JM, Wakelam MJ, Savage CO: Activation of Syk in neutrophils by antineutrophil cytoplasm antibodies occurs via Fcgamma receptors and CD18. J Am Soc Nephrol. 2004, 15: 796-808. 10.1097/01.ASN.0000113241.98702.77.PubMedCrossRef
52.
go back to reference Williams JM, Ben-Smith A, Hewins P, Dove SK, Hughes P, McEwan R, Wakelam MJ, Savage CO: Activation of the G(i) heterotrimeric G protein by ANCA IgG F(ab')2 fragments is necessary but not sufficient to stimulate the recruitment of those downstream mediators used by intact ANCA IgG. J Am Soc Nephrol. 2003, 14: 661-669. 10.1097/01.ASN.0000050223.34749.F4.PubMedCrossRef Williams JM, Ben-Smith A, Hewins P, Dove SK, Hughes P, McEwan R, Wakelam MJ, Savage CO: Activation of the G(i) heterotrimeric G protein by ANCA IgG F(ab')2 fragments is necessary but not sufficient to stimulate the recruitment of those downstream mediators used by intact ANCA IgG. J Am Soc Nephrol. 2003, 14: 661-669. 10.1097/01.ASN.0000050223.34749.F4.PubMedCrossRef
53.
go back to reference van de Winkel JG, van Ommen R, Huizinga TW, de Raad MA, Tuijnman WB, Groenen PJ, Capel PJ, Koene RA, Tax WJ: Proteolysis induces increased binding affinity of the monocyte type II FcR for human IgG. J Immunol. 1989, 143: 571-578.PubMed van de Winkel JG, van Ommen R, Huizinga TW, de Raad MA, Tuijnman WB, Groenen PJ, Capel PJ, Koene RA, Tax WJ: Proteolysis induces increased binding affinity of the monocyte type II FcR for human IgG. J Immunol. 1989, 143: 571-578.PubMed
54.
go back to reference Nagarajan S, Venkiteswaran K, Anderson M, Sayed U, Zhu C, Selvaraj P: Cell-specific, activation-dependent regulation of neutrophil CD32A ligand-binding function. Blood. 2000, 95: 1069-1077.PubMed Nagarajan S, Venkiteswaran K, Anderson M, Sayed U, Zhu C, Selvaraj P: Cell-specific, activation-dependent regulation of neutrophil CD32A ligand-binding function. Blood. 2000, 95: 1069-1077.PubMed
55.
go back to reference Belostocki K, Pricop L, Redecha PB, Aydin A, Leff L, Harrison MJ, Salmon JE: Infliximab treatment shifts the balance between stimulatory and inhibitory Fcgamma receptor type II isoforms on neutrophils in patients with rheumatoid arthritis. Arthritis Rheum. 2008, 58: 384-388. 10.1002/art.23200.PubMedCrossRef Belostocki K, Pricop L, Redecha PB, Aydin A, Leff L, Harrison MJ, Salmon JE: Infliximab treatment shifts the balance between stimulatory and inhibitory Fcgamma receptor type II isoforms on neutrophils in patients with rheumatoid arthritis. Arthritis Rheum. 2008, 58: 384-388. 10.1002/art.23200.PubMedCrossRef
56.
go back to reference Murdaca G, Spanò F, Cagnati P, Puppo F: Free radicals and endothelial dysfunction: Potential positive effects of TNF-α inhibitors. Redox Rep. 2013, 18: 95-99. 10.1179/1351000213Y.0000000046.PubMedCrossRef Murdaca G, Spanò F, Cagnati P, Puppo F: Free radicals and endothelial dysfunction: Potential positive effects of TNF-α inhibitors. Redox Rep. 2013, 18: 95-99. 10.1179/1351000213Y.0000000046.PubMedCrossRef
57.
go back to reference Maradit-Kremers H, Nicola PJ, Crowson CS, Ballman KV, Gabriel SE: Cardiovascular death in rheumatoid arthritis: a population-based study. Arthritis Rheum. 2005, 52: 722-732. 10.1002/art.20878.PubMedCrossRef Maradit-Kremers H, Nicola PJ, Crowson CS, Ballman KV, Gabriel SE: Cardiovascular death in rheumatoid arthritis: a population-based study. Arthritis Rheum. 2005, 52: 722-732. 10.1002/art.20878.PubMedCrossRef
58.
go back to reference Suppiah R, Judge A, Batra R, Flossmann O, Harper L, Hoglund P, Javaid MK, Jayne D, Mukhtyar C, Westman K, Davis JC, Hoffman GS, McCune WJ, Merkel PA, St Clair EW, Seo P, Spiera R, Stone JH, Luqmani R: A model to predict cardiovascular events in patients with newly diagnosed Wegener's granulomatosis and microscopic polyangiitis. Arthritis Care Res (Hoboken). 2011, 63: 588-596. 10.1002/acr.20433.CrossRef Suppiah R, Judge A, Batra R, Flossmann O, Harper L, Hoglund P, Javaid MK, Jayne D, Mukhtyar C, Westman K, Davis JC, Hoffman GS, McCune WJ, Merkel PA, St Clair EW, Seo P, Spiera R, Stone JH, Luqmani R: A model to predict cardiovascular events in patients with newly diagnosed Wegener's granulomatosis and microscopic polyangiitis. Arthritis Care Res (Hoboken). 2011, 63: 588-596. 10.1002/acr.20433.CrossRef
59.
go back to reference Hernandez-Vargas P, Ortiz-Munoz G, Lopez-Franco O, Suzuki Y, Gallego-Delgado J, Sanjuan G, Lazaro A, Lopez-Parra V, Ortega L, Egido J, Gomez-Guerrero C: Fcgamma receptor deficiency confers protection against atherosclerosis in apolipoprotein E knockout mice. Circ Res. 2006, 99: 1188-1196. 10.1161/01.RES.0000250556.07796.6c.PubMedCrossRef Hernandez-Vargas P, Ortiz-Munoz G, Lopez-Franco O, Suzuki Y, Gallego-Delgado J, Sanjuan G, Lazaro A, Lopez-Parra V, Ortega L, Egido J, Gomez-Guerrero C: Fcgamma receptor deficiency confers protection against atherosclerosis in apolipoprotein E knockout mice. Circ Res. 2006, 99: 1188-1196. 10.1161/01.RES.0000250556.07796.6c.PubMedCrossRef
60.
go back to reference Colombo BM, Cacciapaglia F, Puntoni M, Murdaca G, Rossi E, Rodriguez G, Nobili F, Pisciotta L, Bertolini S, Moccetti T, Dentali F, Steidl L, Ciprandi G, Afeltra A, Indiveri F, Puppo F: Traditional and non traditional risk factors in accelerated atherosclerosis in systemic lupus erythematosus: role of vascular endothelial growth factor (VEGATS Study). Autoimmun Rev. 2009, 8: 309-315. 10.1016/j.autrev.2008.10.002.PubMedCrossRef Colombo BM, Cacciapaglia F, Puntoni M, Murdaca G, Rossi E, Rodriguez G, Nobili F, Pisciotta L, Bertolini S, Moccetti T, Dentali F, Steidl L, Ciprandi G, Afeltra A, Indiveri F, Puppo F: Traditional and non traditional risk factors in accelerated atherosclerosis in systemic lupus erythematosus: role of vascular endothelial growth factor (VEGATS Study). Autoimmun Rev. 2009, 8: 309-315. 10.1016/j.autrev.2008.10.002.PubMedCrossRef
61.
go back to reference Colombo BM, Murdaca G, Caiti M, Rodriguez G, Grassia L, Rossi E, Indiveri F, Puppo F: Intima-media thickness: a marker of accelerated atherosclerosis in women with systemic lupus erythematosus. Ann N Y Acad Sci. 2007, 1108: 121-126. 10.1196/annals.1422.014.PubMedCrossRef Colombo BM, Murdaca G, Caiti M, Rodriguez G, Grassia L, Rossi E, Indiveri F, Puppo F: Intima-media thickness: a marker of accelerated atherosclerosis in women with systemic lupus erythematosus. Ann N Y Acad Sci. 2007, 1108: 121-126. 10.1196/annals.1422.014.PubMedCrossRef
62.
go back to reference Marois L, Vaillancourt M, Marois S, Proulx S, Pare G, Rollet-Labelle E, Naccache PH: The ubiquitin ligase c-Cbl down-regulates FcgammaRIIa activation in human neutrophils. J Immunol. 2009, 182: 2374-2384. 10.4049/jimmunol.0801420.PubMedCrossRef Marois L, Vaillancourt M, Marois S, Proulx S, Pare G, Rollet-Labelle E, Naccache PH: The ubiquitin ligase c-Cbl down-regulates FcgammaRIIa activation in human neutrophils. J Immunol. 2009, 182: 2374-2384. 10.4049/jimmunol.0801420.PubMedCrossRef
63.
go back to reference Marois L, Vaillancourt M, Pare G, Gagne V, Fernandes MJ, Rollet-Labelle E, Naccache PH: CIN85 modulates the downregulation of Fc{gamma}RIIa expression and function by c-CBL in a PKC-dependent manner in human neutrophils. J Biol Chem. 2011, 286: 15073-15084. 10.1074/jbc.M110.213660.PubMedPubMedCentralCrossRef Marois L, Vaillancourt M, Pare G, Gagne V, Fernandes MJ, Rollet-Labelle E, Naccache PH: CIN85 modulates the downregulation of Fc{gamma}RIIa expression and function by c-CBL in a PKC-dependent manner in human neutrophils. J Biol Chem. 2011, 286: 15073-15084. 10.1074/jbc.M110.213660.PubMedPubMedCentralCrossRef
Metadata
Title
Cross-linking of IgGs bound on circulating neutrophils leads to an activation of endothelial cells: possible role of rheumatoid factors in rheumatoid arthritis-associated vascular dysfunction
Authors
Emmanuelle Rollet-Labelle
Myriam Vaillancourt
Louis Marois
Marianna M Newkirk
Patrice E Poubelle
Paul H Naccache
Publication date
01-12-2013
Publisher
BioMed Central
Published in
Journal of Inflammation / Issue 1/2013
Electronic ISSN: 1476-9255
DOI
https://doi.org/10.1186/1476-9255-10-27

Other articles of this Issue 1/2013

Journal of Inflammation 1/2013 Go to the issue
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.