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Published in: Inflammation 6/2011

01-12-2011

Up-Regulation of the Inflammatory Response by Ovariectomy in Collagen-Induced Arthritis. Effects of Tin Protoporphyrin IX

Authors: Lidia Ibáñez, Maria José Alcaraz, Nuria Maicas, David Guede, José Ramón Caeiro, Marije I. Koenders, Wim B. van den Berg, Maria Luisa Ferrándiz

Published in: Inflammation | Issue 6/2011

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Abstract

We have studied the influence of ovariectomy on the inflammatory response and bone metabolism on CIA as a model of postmenopausal arthritis as well as the effects of tin protoporphyrin IX (SnPP), a heme oxygenase inhibitor. Ovariectomy in non-arthritic mice produced increased serum PGD2 levels and up-regulated the expression of COX-2, h-PGDS, l-PGDS, and HO-1 in the joints. In CIA, ovariectomy potentiated the inflammatory response with higher levels of serum IL-6 and MMP-3, local PGD2 and MMP-3 as well as trabecular bone erosion. In OVX-CIA, SnPP decreased the serum levels of IL-6, MMP-3, and PGD2; down-regulated TNFα, COX-2, hPGDS, PGD2, PGE2, and MMP-3 in joint tissues; and also decreased focal bone loss in the inflamed joint. Ovariectomy up-regulates inflammatory mediators in non-arthritic and in arthritic animals. In the OVX-CIA model, SnPP exerts anti-inflammatory effects which are not associated with the prevention of systemic bone loss.
Literature
1.
go back to reference Goldring, S.R., and E.M. Gravallese. 2000. Mechanisms of bone loss in inflammatory arthritis: Diagnosis and therapeutic implications. Arthritis Research 2(1): 33–37.PubMedCrossRef Goldring, S.R., and E.M. Gravallese. 2000. Mechanisms of bone loss in inflammatory arthritis: Diagnosis and therapeutic implications. Arthritis Research 2(1): 33–37.PubMedCrossRef
2.
go back to reference Forsblad, D.H., A. Larsen, E. Waltbrand, G. Kvist, D. Mellstrom, T. Saxne, C. Ohlsson, E. Nordborg, and H. Carlsten. 2003. Radiographic joint destruction in postmenopausal rheumatoid arthritis is strongly associated with generalised osteoporosis. Annals of the Rheumatic Diseases 62(7): 617–623.CrossRef Forsblad, D.H., A. Larsen, E. Waltbrand, G. Kvist, D. Mellstrom, T. Saxne, C. Ohlsson, E. Nordborg, and H. Carlsten. 2003. Radiographic joint destruction in postmenopausal rheumatoid arthritis is strongly associated with generalised osteoporosis. Annals of the Rheumatic Diseases 62(7): 617–623.CrossRef
3.
go back to reference Goemaere, S., C. Ackerman, K. Goethals, F. De Keyser, C. Van der Straeten, G. Verbruggen, H. Mielants, and E.M. Veys. 1990. Onset of symptoms of rheumatoid arthritis in relation to age, sex and menopausal transition. The Journal of Rheumatology 17(12): 1620–1622.PubMed Goemaere, S., C. Ackerman, K. Goethals, F. De Keyser, C. Van der Straeten, G. Verbruggen, H. Mielants, and E.M. Veys. 1990. Onset of symptoms of rheumatoid arthritis in relation to age, sex and menopausal transition. The Journal of Rheumatology 17(12): 1620–1622.PubMed
4.
go back to reference D’Elia, H.F., A. Larsen, L.A. Mattsson, E. Waltbrand, G. Kvist, D. Mellstrom, T. Saxne, C. Ohlsson, E. Nordborg, and H. Carlsten. 2003. Influence of hormone replacement therapy on disease progression and bone mineral density in rheumatoid arthritis. The Journal of Rheumatology 30(7): 1456–1463.PubMed D’Elia, H.F., A. Larsen, L.A. Mattsson, E. Waltbrand, G. Kvist, D. Mellstrom, T. Saxne, C. Ohlsson, E. Nordborg, and H. Carlsten. 2003. Influence of hormone replacement therapy on disease progression and bone mineral density in rheumatoid arthritis. The Journal of Rheumatology 30(7): 1456–1463.PubMed
5.
go back to reference Engdahl, C., C. Jochems, S.H. Windahl, A.E. Borjesson, C. Ohlsson, H. Carlsten, and M.K. Lagerquist. 2010. Amelioration of collagen-induced arthritis and immune-associated bone loss through signaling via estrogen receptor alpha, and not estrogen receptor beta or G protein-coupled receptor 30. Arthritis and Rheumatism 62(2): 524–533.PubMed Engdahl, C., C. Jochems, S.H. Windahl, A.E. Borjesson, C. Ohlsson, H. Carlsten, and M.K. Lagerquist. 2010. Amelioration of collagen-induced arthritis and immune-associated bone loss through signaling via estrogen receptor alpha, and not estrogen receptor beta or G protein-coupled receptor 30. Arthritis and Rheumatism 62(2): 524–533.PubMed
6.
go back to reference Jochems, C., U. Islander, M. Erlandsson, M. Verdrengh, C. Ohlsson, and H. Carlsten. 2005. Osteoporosis in experimental postmenopausal polyarthritis: The relative contributions of estrogen deficiency and inflammation. Arthritis Research & Therapy 7(4): R837–R843.CrossRef Jochems, C., U. Islander, M. Erlandsson, M. Verdrengh, C. Ohlsson, and H. Carlsten. 2005. Osteoporosis in experimental postmenopausal polyarthritis: The relative contributions of estrogen deficiency and inflammation. Arthritis Research & Therapy 7(4): R837–R843.CrossRef
7.
go back to reference Alcaraz, M.J., P. Fernandez, and M.I. Guillen. 2003. Anti-inflammatory actions of the heme oxygenase-1 pathway. Current Pharmaceutical Design 9(30): 2541–2551.PubMedCrossRef Alcaraz, M.J., P. Fernandez, and M.I. Guillen. 2003. Anti-inflammatory actions of the heme oxygenase-1 pathway. Current Pharmaceutical Design 9(30): 2541–2551.PubMedCrossRef
8.
go back to reference Zwerina, J., S. Tzima, S. Hayer, K. Redlich, O. Hoffmann, B. Hanslik-Schnabel, J.S. Smolen, G. Kollias, and G. Schett. 2005. Heme oxygenase 1 (HO-1) regulates osteoclastogenesis and bone resorption. The FASEB Journal 19(14): 2011–2013.PubMed Zwerina, J., S. Tzima, S. Hayer, K. Redlich, O. Hoffmann, B. Hanslik-Schnabel, J.S. Smolen, G. Kollias, and G. Schett. 2005. Heme oxygenase 1 (HO-1) regulates osteoclastogenesis and bone resorption. The FASEB Journal 19(14): 2011–2013.PubMed
9.
go back to reference Chae, H.J., H.Y. Chin, G.Y. Lee, H.R. Park, S.K. Yang, H.T. Chung, H.O. Pae, H.M. Kim, S.W. Chae, and H.R. Kim. 2006. Carbon monoxide and nitric oxide protect against tumor necrosis factor-alpha-induced apoptosis in osteoblasts: HO-1 is necessary to mediate the protection. Clinica Chimica Acta 65(1–2): 270–278.CrossRef Chae, H.J., H.Y. Chin, G.Y. Lee, H.R. Park, S.K. Yang, H.T. Chung, H.O. Pae, H.M. Kim, S.W. Chae, and H.R. Kim. 2006. Carbon monoxide and nitric oxide protect against tumor necrosis factor-alpha-induced apoptosis in osteoblasts: HO-1 is necessary to mediate the protection. Clinica Chimica Acta 65(1–2): 270–278.CrossRef
10.
go back to reference Lin, T.H., C.H. Tang, S.Y. Hung, S.H. Liu, Y.M. Lin, W.M. Fu, and R.S. Yang. 2010. Upregulation of heme oxygenase-1 inhibits the maturation and mineralization of osteoblasts. Journal of Cell Physiology 222(3): 757–768. Lin, T.H., C.H. Tang, S.Y. Hung, S.H. Liu, Y.M. Lin, W.M. Fu, and R.S. Yang. 2010. Upregulation of heme oxygenase-1 inhibits the maturation and mineralization of osteoblasts. Journal of Cell Physiology 222(3): 757–768.
11.
go back to reference Devesa, I., M.L. Ferrandiz, M.C. Terencio, L.A. Joosten, W.B. van den Berg, and M.J. Alcaraz. 2005. Influence of heme oxygenase 1 modulation on the progression of murine collagen-induced arthritis. Arthritis and Rheumatism 52(10): 3230–3238.PubMedCrossRef Devesa, I., M.L. Ferrandiz, M.C. Terencio, L.A. Joosten, W.B. van den Berg, and M.J. Alcaraz. 2005. Influence of heme oxygenase 1 modulation on the progression of murine collagen-induced arthritis. Arthritis and Rheumatism 52(10): 3230–3238.PubMedCrossRef
12.
go back to reference Joosten, L.A., E. Lubberts, P. Durez, M.M. Helsen, M.J. Jacobs, M. Goldman, and W.B. van den Berg. 1997. Role of interleukin-4 and interleukin-10 in murine collagen-induced arthritis. Protective effect of interleukin-4 and interleukin-10 treatment on cartilage destruction. Arthritis & Rheumatism 40(2): 249–260.CrossRef Joosten, L.A., E. Lubberts, P. Durez, M.M. Helsen, M.J. Jacobs, M. Goldman, and W.B. van den Berg. 1997. Role of interleukin-4 and interleukin-10 in murine collagen-induced arthritis. Protective effect of interleukin-4 and interleukin-10 treatment on cartilage destruction. Arthritis & Rheumatism 40(2): 249–260.CrossRef
13.
go back to reference Kind, P.R., and E.J. King. 1954. Estimation of plasma phosphatase by determination of hydrolysed phenol with amino-antipyrine. Journal of Clinical Pathology 7(4): 322–326.PubMedCrossRef Kind, P.R., and E.J. King. 1954. Estimation of plasma phosphatase by determination of hydrolysed phenol with amino-antipyrine. Journal of Clinical Pathology 7(4): 322–326.PubMedCrossRef
14.
go back to reference Moroney, M.A., M.J. Alcaraz, R.A. Forder, F. Carey, and J.R.S. Hoult. 1988. Selectivity of neutrophil 5-lipoxygenase and cyclo-oxygenase inhibition by an anti-inflammatory flavonoid glycoside and related aglycone flavonoids. The Journal of Pharmacy and Pharmacology 40(11): 787–792.PubMedCrossRef Moroney, M.A., M.J. Alcaraz, R.A. Forder, F. Carey, and J.R.S. Hoult. 1988. Selectivity of neutrophil 5-lipoxygenase and cyclo-oxygenase inhibition by an anti-inflammatory flavonoid glycoside and related aglycone flavonoids. The Journal of Pharmacy and Pharmacology 40(11): 787–792.PubMedCrossRef
15.
go back to reference Feldkamp, L.A., L.C. Davis, and C. Krettek. 1984. Practical cone-beam algorithm. Journal of the Optical Society of America A 1(1): 612–619.CrossRef Feldkamp, L.A., L.C. Davis, and C. Krettek. 1984. Practical cone-beam algorithm. Journal of the Optical Society of America A 1(1): 612–619.CrossRef
16.
go back to reference Hildebrand, T., and P. Rüegsegger. 1997. A new method for the model-independent assessment of thickness in three-dimensional images. Journal of Microscopy 185(1): 67–75.CrossRef Hildebrand, T., and P. Rüegsegger. 1997. A new method for the model-independent assessment of thickness in three-dimensional images. Journal of Microscopy 185(1): 67–75.CrossRef
17.
go back to reference Ulrich, D., B. van Rietbergen, A. Laib, and P. Ruegsegger. 1999. The ability of three-dimensional structural indices to reflect mechanical aspects of trabecular bone. Bone 25(1): 55–60.PubMedCrossRef Ulrich, D., B. van Rietbergen, A. Laib, and P. Ruegsegger. 1999. The ability of three-dimensional structural indices to reflect mechanical aspects of trabecular bone. Bone 25(1): 55–60.PubMedCrossRef
18.
go back to reference Kong, Y.Y., U. Feige, I. Sarosi, B. Bolon, A. Tafuri, S. Morony, C. Capparelli, J. Li, R. Elliott, S. McCabe, T. Wong, G. Campagnuolo, E. Moran, E.R. Bogoch, G. Van, L.T. Nguyen, P.S. Ohashi, D.L. Lacey, E. Fish, W.J. Boyle, and J.M. Penninger. 1999. Activated T cells regulate bone loss and joint destruction in adjuvant arthritis through osteoprotegerin ligand. Nature 402(6759): 304–309.PubMedCrossRef Kong, Y.Y., U. Feige, I. Sarosi, B. Bolon, A. Tafuri, S. Morony, C. Capparelli, J. Li, R. Elliott, S. McCabe, T. Wong, G. Campagnuolo, E. Moran, E.R. Bogoch, G. Van, L.T. Nguyen, P.S. Ohashi, D.L. Lacey, E. Fish, W.J. Boyle, and J.M. Penninger. 1999. Activated T cells regulate bone loss and joint destruction in adjuvant arthritis through osteoprotegerin ligand. Nature 402(6759): 304–309.PubMedCrossRef
19.
go back to reference Stolina, M., B. Bolon, D. Dwyer, S. Middleton, D. Duryea, P.J. Kostenuik, U. Feige, and D.J. Zack. 2008. The evolving systemic and local biomarker milieu at different stages of disease progression in rat collagen-induced arthritis. Biomarkers 13(7): 692–712.PubMedCrossRef Stolina, M., B. Bolon, D. Dwyer, S. Middleton, D. Duryea, P.J. Kostenuik, U. Feige, and D.J. Zack. 2008. The evolving systemic and local biomarker milieu at different stages of disease progression in rat collagen-induced arthritis. Biomarkers 13(7): 692–712.PubMedCrossRef
20.
go back to reference Geusens, P.P., R.B. Landewe, P. Garnero, D. Chen, C.R. Dunstan, W.F. Lems, P. Stinissen, D.M. van der Heijde, L.S. Van Der, and M. Boers. 2006. The ratio of circulating osteoprotegerin to RANKL in early rheumatoid arthritis predicts later joint destruction. Arthritis and Rheumatism 54(6): 1772–1777.PubMedCrossRef Geusens, P.P., R.B. Landewe, P. Garnero, D. Chen, C.R. Dunstan, W.F. Lems, P. Stinissen, D.M. van der Heijde, L.S. Van Der, and M. Boers. 2006. The ratio of circulating osteoprotegerin to RANKL in early rheumatoid arthritis predicts later joint destruction. Arthritis and Rheumatism 54(6): 1772–1777.PubMedCrossRef
21.
go back to reference Shimizu, S., S. Shiozawa, K. Shiozawa, S. Imura, and T. Fujita. 1985. Quantitative histologic studies on the pathogenesis of periarticular osteoporosis in rheumatoid arthritis. Arthritis and Rheumatism 28(1): 25–31.PubMedCrossRef Shimizu, S., S. Shiozawa, K. Shiozawa, S. Imura, and T. Fujita. 1985. Quantitative histologic studies on the pathogenesis of periarticular osteoporosis in rheumatoid arthritis. Arthritis and Rheumatism 28(1): 25–31.PubMedCrossRef
22.
go back to reference Bezerra, M.C., J.F. Carvalho, A.S. Prokopowitsch, and R.M. Pereira. 2005. RANK, RANKL and osteoprotegerin in arthritic bone loss. Brazilian Journal of Medicinal and Biological Research 38(2): 161–170.CrossRef Bezerra, M.C., J.F. Carvalho, A.S. Prokopowitsch, and R.M. Pereira. 2005. RANK, RANKL and osteoprotegerin in arthritic bone loss. Brazilian Journal of Medicinal and Biological Research 38(2): 161–170.CrossRef
23.
go back to reference Jilka, R.L., G. Hangoc, G. Girasole, G. Passeri, D.C. Williams, J.S. Abrams, B. Boyce, H. Broxmeyer, and S.C. Manolagas. 1992. Increased osteoclast development after estrogen loss: Mediation by interleukin-6. Science 257(5066): 88–91.PubMedCrossRef Jilka, R.L., G. Hangoc, G. Girasole, G. Passeri, D.C. Williams, J.S. Abrams, B. Boyce, H. Broxmeyer, and S.C. Manolagas. 1992. Increased osteoclast development after estrogen loss: Mediation by interleukin-6. Science 257(5066): 88–91.PubMedCrossRef
24.
go back to reference Hembry, R.M., M.R. Bagga, J.J. Reynolds, and D.L. Hamblen. 1995. Immunolocalisation studies on six matrix metalloproteinases and their inhibitors, TIMP-1 and TIMP-2, in synovia from patients with osteo- and rheumatoid arthritis. Annals of the Rheumatic Diseases 54(1): 25–32.PubMedCrossRef Hembry, R.M., M.R. Bagga, J.J. Reynolds, and D.L. Hamblen. 1995. Immunolocalisation studies on six matrix metalloproteinases and their inhibitors, TIMP-1 and TIMP-2, in synovia from patients with osteo- and rheumatoid arthritis. Annals of the Rheumatic Diseases 54(1): 25–32.PubMedCrossRef
25.
go back to reference Seeuws, S., P. Jacques, J. Van Praet, M. Drennan, J. Coudenys, T. Decruy, E. Deschepper, L. Lepescheux, P. Pujuguet, L. Oste, N. Vandeghinste, R. Brys, G. Verbruggen, and D. Elewaut. 2010. A multiparameter approach to monitor disease activity in collagen-induced arthritis. Arthritis Research & Therapy 12(4): R160. Epub 2010 Aug 23.CrossRef Seeuws, S., P. Jacques, J. Van Praet, M. Drennan, J. Coudenys, T. Decruy, E. Deschepper, L. Lepescheux, P. Pujuguet, L. Oste, N. Vandeghinste, R. Brys, G. Verbruggen, and D. Elewaut. 2010. A multiparameter approach to monitor disease activity in collagen-induced arthritis. Arthritis Research & Therapy 12(4): R160. Epub 2010 Aug 23.CrossRef
26.
go back to reference Kusano, K., C. Miyaura, M. Inada, T. Tamura, A. Ito, H. Nagese, K. Kamoi, and T. Suda. 1998. Regulation of matrix metalloproteinases (MMP-2-3-9, and -13) by interleukin-1 and interleukin-6 in mouse calvaria: Association of MMP induction with bone resorption. Endocrinology 139: 1338–1345.PubMedCrossRef Kusano, K., C. Miyaura, M. Inada, T. Tamura, A. Ito, H. Nagese, K. Kamoi, and T. Suda. 1998. Regulation of matrix metalloproteinases (MMP-2-3-9, and -13) by interleukin-1 and interleukin-6 in mouse calvaria: Association of MMP induction with bone resorption. Endocrinology 139: 1338–1345.PubMedCrossRef
27.
go back to reference Bingham, C.O. 2002. The pathogenesis of rheumatoid arthritis: Pivotal cytokines involved in bone degradation and inflammation. Journal of Rheumatology 65(Suppl): 3–9.PubMed Bingham, C.O. 2002. The pathogenesis of rheumatoid arthritis: Pivotal cytokines involved in bone degradation and inflammation. Journal of Rheumatology 65(Suppl): 3–9.PubMed
28.
go back to reference Okada, Y., J.A. Lorenzo, A.M. Freeman, M. Tomita, S.G. Morham, L.G. Raisz, and C.C. Pilbeam. 2000. Prostaglandin G/H synthase-2 is required for maximal formation of osteoclast-like cells in culture. The Journal of Clinical Investigation 105(6): 823–832.PubMedCrossRef Okada, Y., J.A. Lorenzo, A.M. Freeman, M. Tomita, S.G. Morham, L.G. Raisz, and C.C. Pilbeam. 2000. Prostaglandin G/H synthase-2 is required for maximal formation of osteoclast-like cells in culture. The Journal of Clinical Investigation 105(6): 823–832.PubMedCrossRef
29.
go back to reference Liu, X.H., A. Kirschenbaum, S. Yao, and A.C. Levine. 2005. Cross-talk between the interleukin-6 and prostaglandin E(2) signaling systems results in enhancement of osteoclastogenesis through effects on the osteoprotegerin/receptor activator of nuclear factor-{kappa}B (RANK) ligand/RANK system. Endocrinology 146(4): 1991–1998.PubMedCrossRef Liu, X.H., A. Kirschenbaum, S. Yao, and A.C. Levine. 2005. Cross-talk between the interleukin-6 and prostaglandin E(2) signaling systems results in enhancement of osteoclastogenesis through effects on the osteoprotegerin/receptor activator of nuclear factor-{kappa}B (RANK) ligand/RANK system. Endocrinology 146(4): 1991–1998.PubMedCrossRef
30.
go back to reference Hikiji, H., T. Takato, T. Shimizu, and S. Ishii. 2008. The roles of prostanoids, leukotrienes, and platelet-activating factor in bone metabolism and disease. Progress in Lipid Research 47(2): 107–126.PubMedCrossRef Hikiji, H., T. Takato, T. Shimizu, and S. Ishii. 2008. The roles of prostanoids, leukotrienes, and platelet-activating factor in bone metabolism and disease. Progress in Lipid Research 47(2): 107–126.PubMedCrossRef
31.
go back to reference Keila, S., A. Kelner, and M. Weinreb. 2001. Systemic prostaglandin E2 increases cancellous bone formation and mass in aging rats and stimulates their bone marrow osteogenic capacity in vivo and in vitro. The Journal of Endocrinology 168(1): 131–139.PubMedCrossRef Keila, S., A. Kelner, and M. Weinreb. 2001. Systemic prostaglandin E2 increases cancellous bone formation and mass in aging rats and stimulates their bone marrow osteogenic capacity in vivo and in vitro. The Journal of Endocrinology 168(1): 131–139.PubMedCrossRef
32.
go back to reference Gao, Q., P. Zhan, C.B. Alander, B.E. Kream, C. Hao, M.D. Breyer, C.C. Pilbeam, and L.G. Raisz. 2009. Effects of global or targeted deletion of the EP4 receptor on the response of osteoblasts to prostaglandin in vitro and on bone histomorphometry in aged mice. Bone 45(1): 98–103.PubMedCrossRef Gao, Q., P. Zhan, C.B. Alander, B.E. Kream, C. Hao, M.D. Breyer, C.C. Pilbeam, and L.G. Raisz. 2009. Effects of global or targeted deletion of the EP4 receptor on the response of osteoblasts to prostaglandin in vitro and on bone histomorphometry in aged mice. Bone 45(1): 98–103.PubMedCrossRef
33.
go back to reference Kasukawa, Y., N. Miyakoshi, A.K. Srivastava, K. Nozaka, S. Maekawa, D.J. Baylink, S. Mohan, and E. Itoi. 2007. The selective cyclooxygenase-2 inhibitor celecoxib reduces bone resorption, but not bone formation, in ovariectomized mice in vivo. The Tohoku Journal of Experimental Medicine 211(3): 275–283.PubMedCrossRef Kasukawa, Y., N. Miyakoshi, A.K. Srivastava, K. Nozaka, S. Maekawa, D.J. Baylink, S. Mohan, and E. Itoi. 2007. The selective cyclooxygenase-2 inhibitor celecoxib reduces bone resorption, but not bone formation, in ovariectomized mice in vivo. The Tohoku Journal of Experimental Medicine 211(3): 275–283.PubMedCrossRef
34.
go back to reference Yoshida, K., H. Oida, T. Kobayashi, T. Maruyama, M. Tanaka, T. Katayama, K. Yamaguchi, E. Segi, T. Tsuboyama, M. Matsushita, K. Ito, Y. Ito, Y. Sugimoto, F. Ushikubi, S. Ohuchida, K. Kondo, T. Nakamura, and S. Narumiya. 2002. Stimulation of bone formation and prevention of bone loss by prostaglandin E EP4 receptor activation. Proceeding of the National Academy of Sciences USA 99(7): 4580–4585.CrossRef Yoshida, K., H. Oida, T. Kobayashi, T. Maruyama, M. Tanaka, T. Katayama, K. Yamaguchi, E. Segi, T. Tsuboyama, M. Matsushita, K. Ito, Y. Ito, Y. Sugimoto, F. Ushikubi, S. Ohuchida, K. Kondo, T. Nakamura, and S. Narumiya. 2002. Stimulation of bone formation and prevention of bone loss by prostaglandin E EP4 receptor activation. Proceeding of the National Academy of Sciences USA 99(7): 4580–4585.CrossRef
35.
go back to reference Tsujisawa, T., H. Inoue, and T. Nishihara. 2005. SC-19220, antagonist of prostaglandin E2 receptor EP1, inhibits osteoclastogenesis by RANKL. Journal of Bone and Mineral Research 20(1): 15–22.PubMedCrossRef Tsujisawa, T., H. Inoue, and T. Nishihara. 2005. SC-19220, antagonist of prostaglandin E2 receptor EP1, inhibits osteoclastogenesis by RANKL. Journal of Bone and Mineral Research 20(1): 15–22.PubMedCrossRef
36.
go back to reference Gallant, M.A., R. Samadfam, J.A. Hackett, J. Antoniou, J.L. Parent, and A.J. Brum-Fernandes. 2005. Production of prostaglandin D(2) by human osteoblasts and modulation of osteoprotegerin, RANKL, and cellular migration by DP and CRTH2 receptors. Journal of Bone and Mineral Research 20(4): 672–681.PubMedCrossRef Gallant, M.A., R. Samadfam, J.A. Hackett, J. Antoniou, J.L. Parent, and A.J. Brum-Fernandes. 2005. Production of prostaglandin D(2) by human osteoblasts and modulation of osteoprotegerin, RANKL, and cellular migration by DP and CRTH2 receptors. Journal of Bone and Mineral Research 20(4): 672–681.PubMedCrossRef
37.
go back to reference Durand, M., M.A. Gallant, and A.J. Brum-Fernandes. 2008. Prostaglandin D2 receptors control osteoclastogenesis and the activity of human osteoclasts. Journal of Bone and Mineral Research 23(7): 1097–1105.PubMedCrossRef Durand, M., M.A. Gallant, and A.J. Brum-Fernandes. 2008. Prostaglandin D2 receptors control osteoclastogenesis and the activity of human osteoclasts. Journal of Bone and Mineral Research 23(7): 1097–1105.PubMedCrossRef
38.
go back to reference Grundemar, L., and L. Ny. 1997. Pitfalls using metalloporphyrins in carbon monoxide research. Trends in Pharmacological Sciences 18(6): 193–195.PubMedCrossRef Grundemar, L., and L. Ny. 1997. Pitfalls using metalloporphyrins in carbon monoxide research. Trends in Pharmacological Sciences 18(6): 193–195.PubMedCrossRef
39.
go back to reference Kaizu, T., T. Tamaki, M. Tanaka, Y. Uchida, S. Tsuchihashi, A. Kawamura, and A. Kakita. 2003. Preconditioning with tin-protoporphyrin IX attenuates ischemia/reperfusion injury in the rat kidney. Kidney International 63(4): 1393–1403.PubMedCrossRef Kaizu, T., T. Tamaki, M. Tanaka, Y. Uchida, S. Tsuchihashi, A. Kawamura, and A. Kakita. 2003. Preconditioning with tin-protoporphyrin IX attenuates ischemia/reperfusion injury in the rat kidney. Kidney International 63(4): 1393–1403.PubMedCrossRef
Metadata
Title
Up-Regulation of the Inflammatory Response by Ovariectomy in Collagen-Induced Arthritis. Effects of Tin Protoporphyrin IX
Authors
Lidia Ibáñez
Maria José Alcaraz
Nuria Maicas
David Guede
José Ramón Caeiro
Marije I. Koenders
Wim B. van den Berg
Maria Luisa Ferrándiz
Publication date
01-12-2011
Publisher
Springer US
Published in
Inflammation / Issue 6/2011
Print ISSN: 0360-3997
Electronic ISSN: 1573-2576
DOI
https://doi.org/10.1007/s10753-010-9266-4

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