Skip to main content
Top
Published in: BMC Musculoskeletal Disorders 1/2010

Open Access 01-12-2010 | Research article

TRAIL Death Receptor-4, Decoy Receptor-1 and Decoy Receptor-2 Expression on CD8+ T Cells Correlate with the Disease Severity in Patients with Rheumatoid Arthritis

Authors: Atil Bisgin, Ender Terzioglu, Cigdem Aydin, Burcak Yoldas, Veli Yazisiz, Nilufer Balci, Huseyin Bagci, Reginald M Gorczynski, Cezmi A Akdis, Salih Sanlioglu

Published in: BMC Musculoskeletal Disorders | Issue 1/2010

Login to get access

Abstract

Background

Rheumatoid Arthritis (RA) is a chronic autoimmune inflammatory disorder. Although the pathogenesis of disease is unclear, it is well known that T cells play a major role in both development and perpetuation of RA through activating macrophages and B cells. Since the lack of TNF-Related Apoptosis Inducing Ligand (TRAIL) expression resulted in defective thymocyte apoptosis leading to an autoimmune disease, we explored evidence for alterations in TRAIL/TRAIL receptor expression on peripheral T lymphocytes in the molecular mechanism of RA development.

Methods

The expression of TRAIL/TRAIL receptors on T cells in 20 RA patients and 12 control individuals were analyzed using flow cytometry. The correlation of TRAIL and its receptor expression profile was compared with clinical RA parameters (RA activity scored as per DAS28) using Spearman Rho Analysis.

Results

While no change was detected in the ratio of CD4+ to CD8+ T cells between controls and RA patient groups, upregulation of TRAIL and its receptors (both death and decoy) was detected on both CD4+ and CD8+ T cells in RA patients compared to control individuals. Death Receptor-4 (DR4) and the decoy receptors DcR1 and DcR2 on CD8+ T cells, but not on CD4+ T cells, were positively correlated with patients' DAS scores.

Conclusions

Our data suggest that TRAIL/TRAIL receptor expression profiles on T cells might be important in revelation of RA pathogenesis.
Appendix
Available only for authorised users
Literature
1.
go back to reference Koch AE: Review: angiogenesis: implications for rheumatoid arthritis. Arthritis Rheum. 1998, 41 (6): 951-962. 10.1002/1529-0131(199806)41:6<951::AID-ART2>3.0.CO;2-D.CrossRefPubMed Koch AE: Review: angiogenesis: implications for rheumatoid arthritis. Arthritis Rheum. 1998, 41 (6): 951-962. 10.1002/1529-0131(199806)41:6<951::AID-ART2>3.0.CO;2-D.CrossRefPubMed
2.
go back to reference Walsh DA: Angiogenesis and arthritis. Rheumatology (Oxford). 1999, 38 (2): 103-112. 10.1093/rheumatology/38.2.103.CrossRef Walsh DA: Angiogenesis and arthritis. Rheumatology (Oxford). 1999, 38 (2): 103-112. 10.1093/rheumatology/38.2.103.CrossRef
3.
go back to reference Yin G, Liu W, An P, Li P, Ding I, Planelles V, Schwarz EM, Min W: Endostatin gene transfer inhibits joint angiogenesis and pannus formation in inflammatory arthritis. Mol Ther. 2002, 5 (5 Pt 1): 547-554. 10.1006/mthe.2002.0590.CrossRefPubMed Yin G, Liu W, An P, Li P, Ding I, Planelles V, Schwarz EM, Min W: Endostatin gene transfer inhibits joint angiogenesis and pannus formation in inflammatory arthritis. Mol Ther. 2002, 5 (5 Pt 1): 547-554. 10.1006/mthe.2002.0590.CrossRefPubMed
4.
go back to reference Panayi GS: T-cell-dependent pathways in rheumatoid arthritis. Curr Opin Rheumatol. 1997, 9 (3): 236-240. 10.1097/00002281-199705000-00010.CrossRefPubMed Panayi GS: T-cell-dependent pathways in rheumatoid arthritis. Curr Opin Rheumatol. 1997, 9 (3): 236-240. 10.1097/00002281-199705000-00010.CrossRefPubMed
5.
go back to reference Weyand CM, Goronzy JJ: Pathogenesis of rheumatoid arthritis. Med Clin North Am. 1997, 81 (1): 29-55. 10.1016/S0025-7125(05)70504-6.CrossRefPubMed Weyand CM, Goronzy JJ: Pathogenesis of rheumatoid arthritis. Med Clin North Am. 1997, 81 (1): 29-55. 10.1016/S0025-7125(05)70504-6.CrossRefPubMed
6.
go back to reference Nepom GT: Major histocompatibility complex-directed susceptibility to rheumatoid arthritis. Adv Immunol. 1998, 68: 315-332. full_text.CrossRefPubMed Nepom GT: Major histocompatibility complex-directed susceptibility to rheumatoid arthritis. Adv Immunol. 1998, 68: 315-332. full_text.CrossRefPubMed
7.
go back to reference Koetz K, Bryl E, Spickschen K, O'Fallon WM, Goronzy JJ, Weyand CM: T cell homeostasis in patients with rheumatoid arthritis. Proc Natl Acad Sci USA. 2000, 97 (16): 9203-9208. 10.1073/pnas.97.16.9203.CrossRefPubMedPubMedCentral Koetz K, Bryl E, Spickschen K, O'Fallon WM, Goronzy JJ, Weyand CM: T cell homeostasis in patients with rheumatoid arthritis. Proc Natl Acad Sci USA. 2000, 97 (16): 9203-9208. 10.1073/pnas.97.16.9203.CrossRefPubMedPubMedCentral
8.
go back to reference Weyand CM, Goronzy JJ: T-cell-targeted therapies in rheumatoid arthritis. Nat Clin Pract Rheumatol. 2006, 2 (4): 201-210. 10.1038/ncprheum0142.CrossRefPubMed Weyand CM, Goronzy JJ: T-cell-targeted therapies in rheumatoid arthritis. Nat Clin Pract Rheumatol. 2006, 2 (4): 201-210. 10.1038/ncprheum0142.CrossRefPubMed
9.
go back to reference Smolen JS: What is the place of recently approved T cell-targeted and B cell-targeted therapies in the treatment of rheumatoid arthritis? Lessons from global clinical trials. J Rheumatol Suppl. 2007, 79: 15-20.PubMed Smolen JS: What is the place of recently approved T cell-targeted and B cell-targeted therapies in the treatment of rheumatoid arthritis? Lessons from global clinical trials. J Rheumatol Suppl. 2007, 79: 15-20.PubMed
10.
go back to reference Lefkowitz DL, Lefkowitz SS: Macrophage-neutrophil interaction: a paradigm for chronic inflammation revisited. Immunol Cell Biol. 2001, 79 (5): 502-506. 10.1046/j.1440-1711.2001.01020.x.CrossRefPubMed Lefkowitz DL, Lefkowitz SS: Macrophage-neutrophil interaction: a paradigm for chronic inflammation revisited. Immunol Cell Biol. 2001, 79 (5): 502-506. 10.1046/j.1440-1711.2001.01020.x.CrossRefPubMed
11.
go back to reference Stuart L, Hughes J: Apoptosis and autoimmunity. Nephrol Dial Transplant. 2002, 17 (5): 697-700. 10.1093/ndt/17.5.697.CrossRefPubMed Stuart L, Hughes J: Apoptosis and autoimmunity. Nephrol Dial Transplant. 2002, 17 (5): 697-700. 10.1093/ndt/17.5.697.CrossRefPubMed
12.
go back to reference Marleau AM, Sarvetnick N: T cell homeostasis in tolerance and immunity. J Leukoc Biol. 2005, 78 (3): 575-584. 10.1189/jlb.0105050.CrossRefPubMed Marleau AM, Sarvetnick N: T cell homeostasis in tolerance and immunity. J Leukoc Biol. 2005, 78 (3): 575-584. 10.1189/jlb.0105050.CrossRefPubMed
13.
go back to reference Singer GG, Carrera AC, Marshak-Rothstein A, Martinez C, Abbas AK: Apoptosis, Fas and systemic autoimmunity: the MRL-lpr/lpr model. Curr Opin Immunol. 1994, 6 (6): 913-920. 10.1016/0952-7915(94)90013-2.CrossRefPubMed Singer GG, Carrera AC, Marshak-Rothstein A, Martinez C, Abbas AK: Apoptosis, Fas and systemic autoimmunity: the MRL-lpr/lpr model. Curr Opin Immunol. 1994, 6 (6): 913-920. 10.1016/0952-7915(94)90013-2.CrossRefPubMed
14.
go back to reference Fisher GH, Rosenberg FJ, Straus SE, Dale JK, Middleton LA, Lin AY, Strober W, Lenardo MJ, Puck JM: Dominant interfering Fas gene mutations impair apoptosis in a human autoimmune lymphoproliferative syndrome. Cell. 1995, 81 (6): 935-946. 10.1016/0092-8674(95)90013-6.CrossRefPubMed Fisher GH, Rosenberg FJ, Straus SE, Dale JK, Middleton LA, Lin AY, Strober W, Lenardo MJ, Puck JM: Dominant interfering Fas gene mutations impair apoptosis in a human autoimmune lymphoproliferative syndrome. Cell. 1995, 81 (6): 935-946. 10.1016/0092-8674(95)90013-6.CrossRefPubMed
15.
go back to reference Drappa J, Vaishnaw AK, Sullivan KE, Chu JL, Elkon KB: Fas gene mutations in the Canale-Smith syndrome, an inherited lymphoproliferative disorder associated with autoimmunity. N Engl J Med. 1996, 335 (22): 1643-1649. 10.1056/NEJM199611283352204.CrossRefPubMed Drappa J, Vaishnaw AK, Sullivan KE, Chu JL, Elkon KB: Fas gene mutations in the Canale-Smith syndrome, an inherited lymphoproliferative disorder associated with autoimmunity. N Engl J Med. 1996, 335 (22): 1643-1649. 10.1056/NEJM199611283352204.CrossRefPubMed
16.
go back to reference Lawrence CP, Chow SC: FADD deficiency sensitises Jurkat T cells to TNF-alpha-dependent necrosis during activation-induced cell death. FEBS Lett. 2005, 579 (28): 6465-6472. 10.1016/j.febslet.2005.10.041.CrossRefPubMed Lawrence CP, Chow SC: FADD deficiency sensitises Jurkat T cells to TNF-alpha-dependent necrosis during activation-induced cell death. FEBS Lett. 2005, 579 (28): 6465-6472. 10.1016/j.febslet.2005.10.041.CrossRefPubMed
17.
go back to reference Sanlioglu AD, Koksal T, Baykara M, Luleci G, Karacay B, Sanlioglu S: Current progress in adenovirus mediated gene therapy for patients with prostate carcinoma. Gene Ther Mol Biol. 2003, 7: 113-133. Sanlioglu AD, Koksal T, Baykara M, Luleci G, Karacay B, Sanlioglu S: Current progress in adenovirus mediated gene therapy for patients with prostate carcinoma. Gene Ther Mol Biol. 2003, 7: 113-133.
18.
go back to reference Griffith TS, Lynch DH: TRAIL: a molecule with multiple receptors and control mechanisms. Curr Opin Immunol. 1998, 10 (5): 559-563. 10.1016/S0952-7915(98)80224-0.CrossRefPubMed Griffith TS, Lynch DH: TRAIL: a molecule with multiple receptors and control mechanisms. Curr Opin Immunol. 1998, 10 (5): 559-563. 10.1016/S0952-7915(98)80224-0.CrossRefPubMed
19.
go back to reference Sanlioglu AD, Koksal IT, Karacay B, Baykara M, Luleci G, Sanlioglu S: Adenovirus-mediated IKKbetaKA expression sensitizes prostate carcinoma cells to TRAIL-induced apoptosis. Cancer Gene Ther. 2006, 13 (1): 21-31. 10.1038/sj.cgt.7700877.CrossRefPubMed Sanlioglu AD, Koksal IT, Karacay B, Baykara M, Luleci G, Sanlioglu S: Adenovirus-mediated IKKbetaKA expression sensitizes prostate carcinoma cells to TRAIL-induced apoptosis. Cancer Gene Ther. 2006, 13 (1): 21-31. 10.1038/sj.cgt.7700877.CrossRefPubMed
20.
go back to reference Griffith TS, Rauch CT, Smolak PJ, Waugh JY, Boiani N, Lynch DH, Smith CA, Goodwin RG, Kubin MZ: Functional analysis of TRAIL receptors using monoclonal antibodies. J Immunol. 1999, 162 (5): 2597-2605.PubMed Griffith TS, Rauch CT, Smolak PJ, Waugh JY, Boiani N, Lynch DH, Smith CA, Goodwin RG, Kubin MZ: Functional analysis of TRAIL receptors using monoclonal antibodies. J Immunol. 1999, 162 (5): 2597-2605.PubMed
21.
go back to reference Sanlioglu AD, Karacay B, Koksal IT, Griffith TS, Sanlioglu S: DcR2 (TRAIL-R4) siRNA and adenovirus delivery of TRAIL (Ad5hTRAIL) break down in vitro tumorigenic potential of prostate carcinoma cells. Cancer Gene Ther. 2007, 14 (12): 976-984. 10.1038/sj.cgt.7701087.CrossRefPubMed Sanlioglu AD, Karacay B, Koksal IT, Griffith TS, Sanlioglu S: DcR2 (TRAIL-R4) siRNA and adenovirus delivery of TRAIL (Ad5hTRAIL) break down in vitro tumorigenic potential of prostate carcinoma cells. Cancer Gene Ther. 2007, 14 (12): 976-984. 10.1038/sj.cgt.7701087.CrossRefPubMed
22.
go back to reference Wendling U, Walczak H, Dorr J, Jaboci C, Weller M, Krammer PH, Zipp F: Expression of TRAIL receptors in human autoreactive and foreign antigen-specific T cells. Cell Death Differ. 2000, 7 (7): 637-644. 10.1038/sj.cdd.4400692.CrossRefPubMed Wendling U, Walczak H, Dorr J, Jaboci C, Weller M, Krammer PH, Zipp F: Expression of TRAIL receptors in human autoreactive and foreign antigen-specific T cells. Cell Death Differ. 2000, 7 (7): 637-644. 10.1038/sj.cdd.4400692.CrossRefPubMed
23.
go back to reference Dirice E, Sanlioglu AD, Kahraman S, Ozturk S, Balci MK, Omer A, Griffith TS, Sanlioglu S: Adenovirus-mediated TRAIL gene (Ad5hTRAIL) delivery into pancreatic islets prolongs normoglycemia in streptozotocin-induced diabetic rats. Hum Gene Ther. 2009, 20 (10): 1177-1189. 10.1089/hum.2009.039.CrossRefPubMed Dirice E, Sanlioglu AD, Kahraman S, Ozturk S, Balci MK, Omer A, Griffith TS, Sanlioglu S: Adenovirus-mediated TRAIL gene (Ad5hTRAIL) delivery into pancreatic islets prolongs normoglycemia in streptozotocin-induced diabetic rats. Hum Gene Ther. 2009, 20 (10): 1177-1189. 10.1089/hum.2009.039.CrossRefPubMed
24.
go back to reference Song K, Chen Y, Goke R, Wilmen A, Seidel C, Goke A, Hilliard B, Chen Y: Tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) is an inhibitor of autoimmune inflammation and cell cycle progression. J Exp Med. 2000, 191 (7): 1095-1104. 10.1084/jem.191.7.1095.CrossRefPubMedPubMedCentral Song K, Chen Y, Goke R, Wilmen A, Seidel C, Goke A, Hilliard B, Chen Y: Tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) is an inhibitor of autoimmune inflammation and cell cycle progression. J Exp Med. 2000, 191 (7): 1095-1104. 10.1084/jem.191.7.1095.CrossRefPubMedPubMedCentral
26.
go back to reference Maeda N, Sekigawa I, Iida N, Matsumoto M, Hashimoto H, Hirose S: Relationship between CD4+/CD8+ T cell ratio and T cell activation in systemic lupus erythematosus. Scand J Rheumatol. 1999, 28 (3): 166-170. 10.1080/03009749950154248.CrossRefPubMed Maeda N, Sekigawa I, Iida N, Matsumoto M, Hashimoto H, Hirose S: Relationship between CD4+/CD8+ T cell ratio and T cell activation in systemic lupus erythematosus. Scand J Rheumatol. 1999, 28 (3): 166-170. 10.1080/03009749950154248.CrossRefPubMed
27.
go back to reference Matsushita M, Hayashi T, Ando S, Sekigawa I, Iida N, Hashimoto H, Hirose S: Changes of CD4/CD8 ratio and interleukin-16 in systemic lupus erythematosus. Clin Rheumatol. 2000, 19 (4): 270-274. 10.1007/PL00011171.CrossRefPubMed Matsushita M, Hayashi T, Ando S, Sekigawa I, Iida N, Hashimoto H, Hirose S: Changes of CD4/CD8 ratio and interleukin-16 in systemic lupus erythematosus. Clin Rheumatol. 2000, 19 (4): 270-274. 10.1007/PL00011171.CrossRefPubMed
28.
go back to reference Wang H, Xu J, Ji X, Yang X, Sun K, Liu X, Shen Y: The abnormal apoptosis of T cell subsets and possible involvement of IL-10 in systemic lupus erythematosus. Cell Immunol. 2005, 235 (2): 117-121. 10.1016/j.cellimm.2005.08.031.CrossRefPubMed Wang H, Xu J, Ji X, Yang X, Sun K, Liu X, Shen Y: The abnormal apoptosis of T cell subsets and possible involvement of IL-10 in systemic lupus erythematosus. Cell Immunol. 2005, 235 (2): 117-121. 10.1016/j.cellimm.2005.08.031.CrossRefPubMed
29.
go back to reference Cao D, Malmstrom V, Baecher-Allan C, Hafler D, Klareskog L, Trollmo C: Isolation and functional characterization of regulatory CD25brightCD4+ T cells from the target organ of patients with rheumatoid arthritis. Eur J Immunol. 2003, 33 (1): 215-223. 10.1002/immu.200390024.CrossRefPubMed Cao D, Malmstrom V, Baecher-Allan C, Hafler D, Klareskog L, Trollmo C: Isolation and functional characterization of regulatory CD25brightCD4+ T cells from the target organ of patients with rheumatoid arthritis. Eur J Immunol. 2003, 33 (1): 215-223. 10.1002/immu.200390024.CrossRefPubMed
30.
go back to reference Baecher-Allan C, Brown JA, Freeman GJ, Hafler DA: CD4+CD25high regulatory cells in human peripheral blood. J Immunol. 2001, 167 (3): 1245-1253.CrossRefPubMed Baecher-Allan C, Brown JA, Freeman GJ, Hafler DA: CD4+CD25high regulatory cells in human peripheral blood. J Immunol. 2001, 167 (3): 1245-1253.CrossRefPubMed
31.
go back to reference Lamhamedi-Cherradi SE, Zheng SJ, Maguschak KA, Peschon J, Chen YH: Defective thymocyte apoptosis and accelerated autoimmune diseases in TRAIL-/- mice. Nat Immunol. 2003, 4 (3): 255-260. 10.1038/ni894.CrossRefPubMed Lamhamedi-Cherradi SE, Zheng SJ, Maguschak KA, Peschon J, Chen YH: Defective thymocyte apoptosis and accelerated autoimmune diseases in TRAIL-/- mice. Nat Immunol. 2003, 4 (3): 255-260. 10.1038/ni894.CrossRefPubMed
32.
go back to reference Terzioglu E, Bisgin A, Sanlioglu AD, Ulker M, Yazisiz V, Tuzuner S, Sanlioglu S: Concurrent gene therapy strategies effectively destroy synoviocytes of patients with rheumatoid arthritis. Rheumatology (Oxford). 2007, 46 (5): 783-789. 10.1093/rheumatology/kel448.CrossRef Terzioglu E, Bisgin A, Sanlioglu AD, Ulker M, Yazisiz V, Tuzuner S, Sanlioglu S: Concurrent gene therapy strategies effectively destroy synoviocytes of patients with rheumatoid arthritis. Rheumatology (Oxford). 2007, 46 (5): 783-789. 10.1093/rheumatology/kel448.CrossRef
33.
go back to reference Aydin C, Sanlioglu AD, Karacay B, Ozbilim G, Dertsiz L, Ozbudak O, Akdis CA, Sanlioglu S: Decoy receptor-2 small interfering RNA (siRNA) strategy employing three different siRNA constructs in combination defeats adenovirus-transferred tumor necrosis factor-related apoptosis-inducing ligand resistance in lung cancer cells. Hum Gene Ther. 2007, 18 (1): 39-50. 10.1089/hum.2006.111.CrossRefPubMed Aydin C, Sanlioglu AD, Karacay B, Ozbilim G, Dertsiz L, Ozbudak O, Akdis CA, Sanlioglu S: Decoy receptor-2 small interfering RNA (siRNA) strategy employing three different siRNA constructs in combination defeats adenovirus-transferred tumor necrosis factor-related apoptosis-inducing ligand resistance in lung cancer cells. Hum Gene Ther. 2007, 18 (1): 39-50. 10.1089/hum.2006.111.CrossRefPubMed
34.
go back to reference Yao Q, Wang S, Gambotto A, Glorioso JC, Evans CH, Robbins PD, Ghivizzani SC, Oligino TJ: Intra-articular adenoviral-mediated gene transfer of trail induces apoptosis of arthritic rabbit synovium. Gene Ther. 2003, 10 (12): 1055-1060. 10.1038/sj.gt.3301881.CrossRefPubMed Yao Q, Wang S, Gambotto A, Glorioso JC, Evans CH, Robbins PD, Ghivizzani SC, Oligino TJ: Intra-articular adenoviral-mediated gene transfer of trail induces apoptosis of arthritic rabbit synovium. Gene Ther. 2003, 10 (12): 1055-1060. 10.1038/sj.gt.3301881.CrossRefPubMed
35.
go back to reference Liu Z, Xu X, Hsu HC, Tousson A, Yang PA, Wu Q, Liu C, Yu S, Zhang HG, Mountz JD: CII-DC-AdTRAIL cell gene therapy inhibits infiltration of CII-reactive T cells and CII-induced arthritis. J Clin Invest. 2003, 112 (9): 1332-1341.CrossRefPubMedPubMedCentral Liu Z, Xu X, Hsu HC, Tousson A, Yang PA, Wu Q, Liu C, Yu S, Zhang HG, Mountz JD: CII-DC-AdTRAIL cell gene therapy inhibits infiltration of CII-reactive T cells and CII-induced arthritis. J Clin Invest. 2003, 112 (9): 1332-1341.CrossRefPubMedPubMedCentral
36.
go back to reference Koksal IT, Sanlioglu AD, Karacay B, Griffith TS, Sanlioglu S: Tumor necrosis factor-related apoptosis inducing ligand-R4 decoy receptor expression is correlated with high Gleason scores, prostate-specific antigen recurrence, and decreased survival in patients with prostate carcinoma. Urol Oncol. 2008, 26 (2): 158-165.CrossRefPubMed Koksal IT, Sanlioglu AD, Karacay B, Griffith TS, Sanlioglu S: Tumor necrosis factor-related apoptosis inducing ligand-R4 decoy receptor expression is correlated with high Gleason scores, prostate-specific antigen recurrence, and decreased survival in patients with prostate carcinoma. Urol Oncol. 2008, 26 (2): 158-165.CrossRefPubMed
37.
go back to reference Sanlioglu AD, Korcum AF, Pestereli E, Erdogan G, Karaveli S, Savas B, Griffith TS, Sanlioglu S: TRAIL death receptor-4 expression positively correlates with the tumor grade in breast cancer patients with invasive ductal carcinoma. Int J Radiat Oncol Biol Phys. 2007, 69 (3): 716-723. 10.1016/j.ijrobp.2007.03.057.CrossRefPubMed Sanlioglu AD, Korcum AF, Pestereli E, Erdogan G, Karaveli S, Savas B, Griffith TS, Sanlioglu S: TRAIL death receptor-4 expression positively correlates with the tumor grade in breast cancer patients with invasive ductal carcinoma. Int J Radiat Oncol Biol Phys. 2007, 69 (3): 716-723. 10.1016/j.ijrobp.2007.03.057.CrossRefPubMed
38.
go back to reference Sanlioglu AD, Dirice E, Elpek O, Korcum AF, Balci MK, Omer A, Griffith TS, Sanlioglu S: High levels of endogenous tumor necrosis factor-related apoptosis-inducing ligand expression correlate with increased cell death in human pancreas. Pancreas. 2008, 36 (4): 385-393. 10.1097/MPA.0b013e318158a4e5.CrossRefPubMed Sanlioglu AD, Dirice E, Elpek O, Korcum AF, Balci MK, Omer A, Griffith TS, Sanlioglu S: High levels of endogenous tumor necrosis factor-related apoptosis-inducing ligand expression correlate with increased cell death in human pancreas. Pancreas. 2008, 36 (4): 385-393. 10.1097/MPA.0b013e318158a4e5.CrossRefPubMed
39.
go back to reference Sanlioglu AD, Dirice E, Elpek O, Korcum AF, Ozdogan M, Suleymanlar I, Balci MK, Griffith TS, Sanlioglu S: High TRAIL Death Receptor 4 and Decoy Receptor 2 Expression Correlates With Significant Cell Death in Pancreatic Ductal Adenocarcinoma Patients. Pancreas. 2009, 38 (2): 154-160. 10.1097/MPA.0b013e31818db9e3.CrossRefPubMed Sanlioglu AD, Dirice E, Elpek O, Korcum AF, Ozdogan M, Suleymanlar I, Balci MK, Griffith TS, Sanlioglu S: High TRAIL Death Receptor 4 and Decoy Receptor 2 Expression Correlates With Significant Cell Death in Pancreatic Ductal Adenocarcinoma Patients. Pancreas. 2009, 38 (2): 154-160. 10.1097/MPA.0b013e31818db9e3.CrossRefPubMed
40.
go back to reference Lum JJ, Pilon AA, Sanchez-Dardon J, Phenix BN, Kim JE, Mihowich J, Jamison K, Hawley-Foss N, Lynch DH, Badley AD: Induction of cell death in human immunodeficiency virus-infected macrophages and resting memory CD4 T cells by TRAIL/Apo2l. J Virol. 2001, 75 (22): 11128-11136. 10.1128/JVI.75.22.11128-11136.2001.CrossRefPubMedPubMedCentral Lum JJ, Pilon AA, Sanchez-Dardon J, Phenix BN, Kim JE, Mihowich J, Jamison K, Hawley-Foss N, Lynch DH, Badley AD: Induction of cell death in human immunodeficiency virus-infected macrophages and resting memory CD4 T cells by TRAIL/Apo2l. J Virol. 2001, 75 (22): 11128-11136. 10.1128/JVI.75.22.11128-11136.2001.CrossRefPubMedPubMedCentral
41.
go back to reference Hasegawa H, Yamada Y, Harasawa H, Tsuji T, Murata K, Sugahara K, Tsuruda K, Masuda M, Takasu N, Kamihira S: Restricted expression of tumor necrosis factor-related apoptosis-inducing ligand receptor 4 in human peripheral blood lymphocytes. Cell Immunol. 2004, 231 (1-2): 1-7. 10.1016/j.cellimm.2004.11.001.CrossRefPubMed Hasegawa H, Yamada Y, Harasawa H, Tsuji T, Murata K, Sugahara K, Tsuruda K, Masuda M, Takasu N, Kamihira S: Restricted expression of tumor necrosis factor-related apoptosis-inducing ligand receptor 4 in human peripheral blood lymphocytes. Cell Immunol. 2004, 231 (1-2): 1-7. 10.1016/j.cellimm.2004.11.001.CrossRefPubMed
42.
go back to reference Sanlioglu AD, Koksal IT, Ciftcioglu A, Baykara M, Luleci G, Sanlioglu S: Differential expression of TRAIL and its receptors in benign and malignant prostate tissues. J Urol. 2007, 177 (1): 359-364. 10.1016/j.juro.2006.08.087.CrossRefPubMed Sanlioglu AD, Koksal IT, Ciftcioglu A, Baykara M, Luleci G, Sanlioglu S: Differential expression of TRAIL and its receptors in benign and malignant prostate tissues. J Urol. 2007, 177 (1): 359-364. 10.1016/j.juro.2006.08.087.CrossRefPubMed
43.
go back to reference Ehrenstein MR, Evans JG, Singh A, Moore S, Warnes G, Isenberg DA, Mauri C: Compromised function of regulatory T cells in rheumatoid arthritis and reversal by anti-TNFalpha therapy. J Exp Med. 2004, 200 (3): 277-285. 10.1084/jem.20040165.CrossRefPubMedPubMedCentral Ehrenstein MR, Evans JG, Singh A, Moore S, Warnes G, Isenberg DA, Mauri C: Compromised function of regulatory T cells in rheumatoid arthritis and reversal by anti-TNFalpha therapy. J Exp Med. 2004, 200 (3): 277-285. 10.1084/jem.20040165.CrossRefPubMedPubMedCentral
44.
go back to reference van Amelsfort JM, Jacobs KM, Bijlsma JW, Lafeber FP, Taams LS: CD4(+)CD25(+) regulatory T cells in rheumatoid arthritis: differences in the presence, phenotype, and function between peripheral blood and synovial fluid. Arthritis Rheum. 2004, 50 (9): 2775-2785. 10.1002/art.20499.CrossRefPubMed van Amelsfort JM, Jacobs KM, Bijlsma JW, Lafeber FP, Taams LS: CD4(+)CD25(+) regulatory T cells in rheumatoid arthritis: differences in the presence, phenotype, and function between peripheral blood and synovial fluid. Arthritis Rheum. 2004, 50 (9): 2775-2785. 10.1002/art.20499.CrossRefPubMed
45.
go back to reference Han GM, O'Neil-Andersen NJ, Zurier RB, Lawrence DA: CD4+CD25high T cell numbers are enriched in the peripheral blood of patients with rheumatoid arthritis. Cell Immunol. 2008, 253 (1-2): 92-101. 10.1016/j.cellimm.2008.05.007.CrossRefPubMedPubMedCentral Han GM, O'Neil-Andersen NJ, Zurier RB, Lawrence DA: CD4+CD25high T cell numbers are enriched in the peripheral blood of patients with rheumatoid arthritis. Cell Immunol. 2008, 253 (1-2): 92-101. 10.1016/j.cellimm.2008.05.007.CrossRefPubMedPubMedCentral
Metadata
Title
TRAIL Death Receptor-4, Decoy Receptor-1 and Decoy Receptor-2 Expression on CD8+ T Cells Correlate with the Disease Severity in Patients with Rheumatoid Arthritis
Authors
Atil Bisgin
Ender Terzioglu
Cigdem Aydin
Burcak Yoldas
Veli Yazisiz
Nilufer Balci
Huseyin Bagci
Reginald M Gorczynski
Cezmi A Akdis
Salih Sanlioglu
Publication date
01-12-2010
Publisher
BioMed Central
Published in
BMC Musculoskeletal Disorders / Issue 1/2010
Electronic ISSN: 1471-2474
DOI
https://doi.org/10.1186/1471-2474-11-192

Other articles of this Issue 1/2010

BMC Musculoskeletal Disorders 1/2010 Go to the issue