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Published in: Arthritis Research & Therapy 4/2002

Open Access 01-06-2002 | Research article

Successful immunotherapy with matrix metalloproteinase-derived peptides in adjuvant arthritis depends on the timing of peptide administration

Authors: Jolanda HM van Bilsen, Josée PA Wagenaar-Hilbers, Maarten JF van der Cammen, Mariska EA van Dijk, Willem van Eden, Marca HM Wauben

Published in: Arthritis Research & Therapy | Issue 4/2002

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Abstract

We have recently found that matrix metalloproteinases (MMPs) are targets for T-cell and B-cell reactivity in experimental arthritis. In the present article, we investigate whether modulation of MMP-specific T-cell responses could influence the course of adjuvant arthritis (AA). Lewis rats were treated nasally with MMP peptides prior to or after AA induction. Administration of the MMP-10 or the MMP-16 peptide prior to AA induction reduced the arthritic symptoms. In contrast, administration of the MMP-10 peptide after AA induction aggravated the arthritic symptoms. The present study shows the possible usefulness of MMP peptides for immunotherapy. However, a clear understanding of proper timing of peptide administration is crucial for the development of such therapies.
Literature
1.
go back to reference Breedveld FC: New insights in the pathogenesis of rheumatoid arthritis. J Rheumatol. 1998, 53 (suppl): S3-S7. Breedveld FC: New insights in the pathogenesis of rheumatoid arthritis. J Rheumatol. 1998, 53 (suppl): S3-S7.
2.
go back to reference Panayi GS, Lanchbury S, Kingsley GH: The importance of the T cell in initiating and maintaining the chronic synovitis of rheumatoid arthritis. Arthritis Rheum. 1992, 35: 729-735.PubMedCrossRef Panayi GS, Lanchbury S, Kingsley GH: The importance of the T cell in initiating and maintaining the chronic synovitis of rheumatoid arthritis. Arthritis Rheum. 1992, 35: 729-735.PubMedCrossRef
3.
go back to reference Barchan D, Souroujon MC, Im SH, Antozzi C, Fuchs S: Antigen-specific modulation of experimental myasthenia gravis: nasal tolerization with recombinant fragments of the human acetylcholine receptor alpha-subunit. Proc Natl Acad Sci USA. 1999, 96: 8086-8091. 10.1073/pnas.96.14.8086.PubMedPubMedCentralCrossRef Barchan D, Souroujon MC, Im SH, Antozzi C, Fuchs S: Antigen-specific modulation of experimental myasthenia gravis: nasal tolerization with recombinant fragments of the human acetylcholine receptor alpha-subunit. Proc Natl Acad Sci USA. 1999, 96: 8086-8091. 10.1073/pnas.96.14.8086.PubMedPubMedCentralCrossRef
4.
go back to reference Karachunski PI, Ostlie NS, Okita DK, Conti-Fine BM: Prevention of experimental myasthenia gravis by nasal administration of synthetic acetylcholine receptor T epitope sequences. J Clin Invest. 1997, 100: 3027-3035.PubMedPubMedCentralCrossRef Karachunski PI, Ostlie NS, Okita DK, Conti-Fine BM: Prevention of experimental myasthenia gravis by nasal administration of synthetic acetylcholine receptor T epitope sequences. J Clin Invest. 1997, 100: 3027-3035.PubMedPubMedCentralCrossRef
5.
go back to reference Tian J, Atkinson MA, Clare-Salzler M, Herschenfeld A, Forsthuber T, Lehmann PV, Kaufman DL: Nasal administration of glutamate decarboxylase (GAD65) peptides induces Th2 responses and prevents murine insulin-dependent diabetes. J Exp Med. 1996, 183: 1561-1567.PubMedCrossRef Tian J, Atkinson MA, Clare-Salzler M, Herschenfeld A, Forsthuber T, Lehmann PV, Kaufman DL: Nasal administration of glutamate decarboxylase (GAD65) peptides induces Th2 responses and prevents murine insulin-dependent diabetes. J Exp Med. 1996, 183: 1561-1567.PubMedCrossRef
6.
go back to reference Dick AD, Cheng YF, Liversidge J, Forrester JV: Intranasal administration of retinal antigens suppresses retinal antigen-induced experimental autoimmune uveoretinitis. Immunology. 1994, 82: 625-631.PubMedPubMedCentral Dick AD, Cheng YF, Liversidge J, Forrester JV: Intranasal administration of retinal antigens suppresses retinal antigen-induced experimental autoimmune uveoretinitis. Immunology. 1994, 82: 625-631.PubMedPubMedCentral
7.
go back to reference Metzler B, Wraith DC: Inhibition of experimental autoimmune encephalomyelitis by inhalation but not oral administration of the encephalitogenic peptide: influence of MHC binding affinity. Int Immunol. 1993, 5: 1159-1165.PubMedCrossRef Metzler B, Wraith DC: Inhibition of experimental autoimmune encephalomyelitis by inhalation but not oral administration of the encephalitogenic peptide: influence of MHC binding affinity. Int Immunol. 1993, 5: 1159-1165.PubMedCrossRef
8.
go back to reference Laliotou B, Liversidge J, Forrester JV, Dick AD: Interphotoreceptor retinoid binding protein is a potent tolerogen in Lewis rat: suppression of experimental autoimmune uveoretinitis is retinal antigen specific. Br J Ophthalmol. 1997, 81: 61-67.PubMedPubMedCentralCrossRef Laliotou B, Liversidge J, Forrester JV, Dick AD: Interphotoreceptor retinoid binding protein is a potent tolerogen in Lewis rat: suppression of experimental autoimmune uveoretinitis is retinal antigen specific. Br J Ophthalmol. 1997, 81: 61-67.PubMedPubMedCentralCrossRef
9.
go back to reference Prakken BJ, van der Zee R, Anderton SM, van Kooten PJ, Kuis W, van Eden W: Peptide-induced nasal tolerance for a mycobac-terial heat shock protein 60 T cell epitope in rats suppresses both adjuvant arthritis and nonmicrobially induced experimental arthritis. Proc Natl Acad Sci USA. 1997, 94: 3284-3289. 10.1073/pnas.94.7.3284.PubMedPubMedCentralCrossRef Prakken BJ, van der Zee R, Anderton SM, van Kooten PJ, Kuis W, van Eden W: Peptide-induced nasal tolerance for a mycobac-terial heat shock protein 60 T cell epitope in rats suppresses both adjuvant arthritis and nonmicrobially induced experimental arthritis. Proc Natl Acad Sci USA. 1997, 94: 3284-3289. 10.1073/pnas.94.7.3284.PubMedPubMedCentralCrossRef
10.
go back to reference Wauben MH: Immunological mechanisms involved in experimental peptide immunotherapy of T-cell-mediated diseases. Crit Rev Immunol. 2000, 20: 451-469.PubMedCrossRef Wauben MH: Immunological mechanisms involved in experimental peptide immunotherapy of T-cell-mediated diseases. Crit Rev Immunol. 2000, 20: 451-469.PubMedCrossRef
11.
go back to reference Myers LK, Seyer JM, Stuart JM, Kang AH: Suppression of murine collagen-induced arthritis by nasal administration of collagen. Immunology. 1997, 90: 161-164. 10.1046/j.1365-2567.1997.00191.x.PubMedPubMedCentralCrossRef Myers LK, Seyer JM, Stuart JM, Kang AH: Suppression of murine collagen-induced arthritis by nasal administration of collagen. Immunology. 1997, 90: 161-164. 10.1046/j.1365-2567.1997.00191.x.PubMedPubMedCentralCrossRef
12.
go back to reference Joosten LA, Coenen-de Roo CJ, Helsen MM, Lubberts E, Boots AM, van den Berg WB, Miltenburg AM: Induction of tolerance with intranasal administration of human cartilage gp-39 in DBA/1 mice: amelioration of clinical, histologic, and radiologic signs of type II collagen-induced arthritis. Arthritis Rheum. 2000, 43: 645-655. 10.1002/1529-0131(200003)43:3<645::AID-ANR22>3.0.CO;2-O.PubMedCrossRef Joosten LA, Coenen-de Roo CJ, Helsen MM, Lubberts E, Boots AM, van den Berg WB, Miltenburg AM: Induction of tolerance with intranasal administration of human cartilage gp-39 in DBA/1 mice: amelioration of clinical, histologic, and radiologic signs of type II collagen-induced arthritis. Arthritis Rheum. 2000, 43: 645-655. 10.1002/1529-0131(200003)43:3<645::AID-ANR22>3.0.CO;2-O.PubMedCrossRef
13.
go back to reference Staines NA, Harper N, Ward FJ, Malmström V, Holmdahl R, Bansal S: Mucosal tolerance and suppression of collagen-induced arthritis (CIA) induced by nasal inhalation of synthetic peptide 184–198 of bovine type II collagen (CII) expressing a dominant T cell epitope. Clin Exp Immunol. 1996, 103: 368-375.PubMedPubMedCentralCrossRef Staines NA, Harper N, Ward FJ, Malmström V, Holmdahl R, Bansal S: Mucosal tolerance and suppression of collagen-induced arthritis (CIA) induced by nasal inhalation of synthetic peptide 184–198 of bovine type II collagen (CII) expressing a dominant T cell epitope. Clin Exp Immunol. 1996, 103: 368-375.PubMedPubMedCentralCrossRef
14.
go back to reference van Bilsen JHM, Wagenaar-Hilbers JPA, Boot EPJ, van Eden W, Wauben MHM: Searching for the cartilage-associated mimicry epitope in adjuvant arthritis. Autoimmunity. 2002, van Bilsen JHM, Wagenaar-Hilbers JPA, Boot EPJ, van Eden W, Wauben MHM: Searching for the cartilage-associated mimicry epitope in adjuvant arthritis. Autoimmunity. 2002,
15.
go back to reference Prakken B, Wauben M, Genini D, Samodal R, Barnett J, Mendivil A, Leoni L, Albani S: Artificial antigen-presenting cells as tool to exploit the immune 'synapse'. Nat Med. 2000, 6: 406-410. Prakken B, Wauben M, Genini D, Samodal R, Barnett J, Mendivil A, Leoni L, Albani S: Artificial antigen-presenting cells as tool to exploit the immune 'synapse'. Nat Med. 2000, 6: 406-410.
16.
go back to reference Anderton S, Burkhart C, Metzler B, Wraith D: Mechanisms of central and peripheral T-cell tolerance: lessons from experimental models of multiple sclerosis. Immunol Rev. 1999, 169: 123-137.PubMedCrossRef Anderton S, Burkhart C, Metzler B, Wraith D: Mechanisms of central and peripheral T-cell tolerance: lessons from experimental models of multiple sclerosis. Immunol Rev. 1999, 169: 123-137.PubMedCrossRef
17.
go back to reference Konttinen YT, Ainola M, Valleala H, Ma J, Ida H, Mandelin J, Kinne RW, Santavirta S, Sorsa T, Lopez-Otin C, Takagi M: Analysis of 16 different matrix metalloproteinases (MMP-1 to MMP-20) in the synovial membrane: different profiles in trauma and rheumatoid arthritis. Ann Rheum Dis. 1999, 58: 691-697.PubMedPubMedCentralCrossRef Konttinen YT, Ainola M, Valleala H, Ma J, Ida H, Mandelin J, Kinne RW, Santavirta S, Sorsa T, Lopez-Otin C, Takagi M: Analysis of 16 different matrix metalloproteinases (MMP-1 to MMP-20) in the synovial membrane: different profiles in trauma and rheumatoid arthritis. Ann Rheum Dis. 1999, 58: 691-697.PubMedPubMedCentralCrossRef
18.
go back to reference Pap T, Shigeyama Y, Kuchen S, Fernihough JK, Simmen B, Gay RE, Billingham M, Gay S: Differential expression pattern of membrane-type matrix metalloproteinases in rheumatoid arthritis. Arthritis Rheum. 2000, 43: 1226-1232. 10.1002/1529-0131(200006)43:6<1226::AID-ANR5>3.0.CO;2-4.PubMedCrossRef Pap T, Shigeyama Y, Kuchen S, Fernihough JK, Simmen B, Gay RE, Billingham M, Gay S: Differential expression pattern of membrane-type matrix metalloproteinases in rheumatoid arthritis. Arthritis Rheum. 2000, 43: 1226-1232. 10.1002/1529-0131(200006)43:6<1226::AID-ANR5>3.0.CO;2-4.PubMedCrossRef
19.
go back to reference Takei I, Takagi M, Santavirta S, Ida H, Ishii M, Ogino T, Ainola M, Konttinen YT: Messenger ribonucleic acid expression of 16 matrix metalloproteinases in bone-implant interface tissues of loose artificial hip joints. J Biomed Mater Res. 2000, 52: 613-620. 10.1002/1097-4636(20001215)52:4<613::AID-JBM5>3.3.CO;2-#.PubMedCrossRef Takei I, Takagi M, Santavirta S, Ida H, Ishii M, Ogino T, Ainola M, Konttinen YT: Messenger ribonucleic acid expression of 16 matrix metalloproteinases in bone-implant interface tissues of loose artificial hip joints. J Biomed Mater Res. 2000, 52: 613-620. 10.1002/1097-4636(20001215)52:4<613::AID-JBM5>3.3.CO;2-#.PubMedCrossRef
20.
go back to reference Ishiguro N, Ito T, Kurokouchi K, Iwahori Y, Nagaya I, Hasegawa Y, Iwata H: mRNA expression of matrix metalloproteinases and tissue inhibitors of metalloproteinase in interface tissue around implants in loosening total hip arthroplasty. J Biomed Mater Res. 1996, 32: 611-617. 10.1002/(SICI)1097-4636(199612)32:4<611::AID-JBM14>3.0.CO;2-G.PubMedCrossRef Ishiguro N, Ito T, Kurokouchi K, Iwahori Y, Nagaya I, Hasegawa Y, Iwata H: mRNA expression of matrix metalloproteinases and tissue inhibitors of metalloproteinase in interface tissue around implants in loosening total hip arthroplasty. J Biomed Mater Res. 1996, 32: 611-617. 10.1002/(SICI)1097-4636(199612)32:4<611::AID-JBM14>3.0.CO;2-G.PubMedCrossRef
21.
go back to reference Blanas E, Carbone FR, Allison J, Miller JFAP, Heath WR: Induction of autoimmune diabetes by oral administration of autoantigen. Science. 1996, 274: 1707-1709. 10.1126/science.274.5293.1707.PubMedCrossRef Blanas E, Carbone FR, Allison J, Miller JFAP, Heath WR: Induction of autoimmune diabetes by oral administration of autoantigen. Science. 1996, 274: 1707-1709. 10.1126/science.274.5293.1707.PubMedCrossRef
22.
go back to reference Lens JW, van den Berg WB, van de Putte LB, van den Bersselaar L: Flare-up of antigen-induced arthritis in mice after challenge with oral antigen. Clin Exp Immunol. 1984, 58: 364-371.PubMedPubMedCentral Lens JW, van den Berg WB, van de Putte LB, van den Bersselaar L: Flare-up of antigen-induced arthritis in mice after challenge with oral antigen. Clin Exp Immunol. 1984, 58: 364-371.PubMedPubMedCentral
23.
go back to reference Weinberg AD, Whitham R, Swain SL, Morrison WJ, Wyrick G, Hoy C, Vandenbark AA, Offner H: Transforming growth factor-b enhances the in vivo effector function and memory phenotype of antigen-specific T helper cells in experimental autoimmune encephalomyelitis. J Immunol. 1992, 148: 2109-2117.PubMed Weinberg AD, Whitham R, Swain SL, Morrison WJ, Wyrick G, Hoy C, Vandenbark AA, Offner H: Transforming growth factor-b enhances the in vivo effector function and memory phenotype of antigen-specific T helper cells in experimental autoimmune encephalomyelitis. J Immunol. 1992, 148: 2109-2117.PubMed
24.
go back to reference Jacob CO, Holoshitz J, van der Meide P, Strober S, McDevitt HO: Heterogeneous effects of IFN-gamma in adjuvant arthritis. J Immunol. 1989, 142: 1500-1505.PubMed Jacob CO, Holoshitz J, van der Meide P, Strober S, McDevitt HO: Heterogeneous effects of IFN-gamma in adjuvant arthritis. J Immunol. 1989, 142: 1500-1505.PubMed
25.
go back to reference Joosten LA, Lubberts E, Helsen MM, van den Berg WB: Dual role of IL-12 in early and late stages of murine collagen type II arthritis. J Immunol. 1997, 159: 4094-4102.PubMed Joosten LA, Lubberts E, Helsen MM, van den Berg WB: Dual role of IL-12 in early and late stages of murine collagen type II arthritis. J Immunol. 1997, 159: 4094-4102.PubMed
26.
go back to reference Thornton S, Boivin GP, Kim KN, Finkelman FD, Hirsch R: Heterogeneous effects of IL-2 on collagen-induced arthritis. J Immunol. 2000, 165: 1557-1563.PubMedCrossRef Thornton S, Boivin GP, Kim KN, Finkelman FD, Hirsch R: Heterogeneous effects of IL-2 on collagen-induced arthritis. J Immunol. 2000, 165: 1557-1563.PubMedCrossRef
S1.
go back to reference van der Zee R, Anderton SM, Buskens CAF, Alonso de Velasco E, van Eden W: Heat shock protein T-cell epitopes as immunogenic carriers in subunit vaccines. In Peptides 1994. Proceedings of the Twenty-Third European Peptide Symposium, September 4–10, Braga, Portugal. Edited by: Maia HLS. 1994, Leiden, The Netherlands: ESCOM, 841-842. van der Zee R, Anderton SM, Buskens CAF, Alonso de Velasco E, van Eden W: Heat shock protein T-cell epitopes as immunogenic carriers in subunit vaccines. In Peptides 1994. Proceedings of the Twenty-Third European Peptide Symposium, September 4–10, Braga, Portugal. Edited by: Maia HLS. 1994, Leiden, The Netherlands: ESCOM, 841-842.
S2.
go back to reference Joosten I, Wauben MHM, Holewijn MC, Reske K, Pedersen LO, Roosenboom CF, Hensen EJ, van Eden W, Buus S: Direct binding of autoimmune disease related T cell epitopes to purified Lewis rat MHC class II molecules. Int Immunol. 1994, 6: 751-759.PubMedCrossRef Joosten I, Wauben MHM, Holewijn MC, Reske K, Pedersen LO, Roosenboom CF, Hensen EJ, van Eden W, Buus S: Direct binding of autoimmune disease related T cell epitopes to purified Lewis rat MHC class II molecules. Int Immunol. 1994, 6: 751-759.PubMedCrossRef
Metadata
Title
Successful immunotherapy with matrix metalloproteinase-derived peptides in adjuvant arthritis depends on the timing of peptide administration
Authors
Jolanda HM van Bilsen
Josée PA Wagenaar-Hilbers
Maarten JF van der Cammen
Mariska EA van Dijk
Willem van Eden
Marca HM Wauben
Publication date
01-06-2002
Publisher
BioMed Central
Published in
Arthritis Research & Therapy / Issue 4/2002
Electronic ISSN: 1478-6362
DOI
https://doi.org/10.1186/ar421

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