Peroxisome proliferator-activated receptor-γ (PPAR-γ) ligands as potential therapeutic agents to treat arthritis

Pharmacological Research

Volumn 60, Issue 3, 2009, Pages 160-169

  Giaginis, Costas ^a   Giagini, Athina ^a   Theocharis, Stamatios ^a  

^a UNIVERSITY OF ATHENS MEDICAL SCHOOL   (Greece)

Author keywords

Arthritis; Inflammation; Osteoarthritis; PPAR ligands; Rheumatoid arthritis

Indexed keywords

AJULEMIC ACID; CELECOXIB; CIGLITAZONE; CLX 090717; DELTA12 PROSTAGLANDIN J2; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDOMETACIN; INTERLEUKIN 1BETA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA AGONIST; PIOGLITAZONE; PROSTAGLANDIN E2; ROSIGLITAZONE; THR 0921; TROGLITAZONE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANTIINFLAMMATORY ACTIVITY; ARTICULAR CARTILAGE; CARTILAGE CELL; CARTILAGE DEGENERATION; CELL POPULATION; DRUG MECHANISM; DRUG RESEARCH; DRUG TARGETING; ENDOTHELIUM CELL; FIBROBLAST; GOUT; HUMAN; NONHUMAN; OSTEOARTHRITIS; PLEIOTROPY; PRIORITY JOURNAL; PROSTAGLANDIN SYNTHESIS INHIBITION; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; PSORIATIC ARTHRITIS; REVIEW; RHEUMATOID ARTHRITIS; SIGNAL TRANSDUCTION; SYNOVIOCYTE;

ANIMALS; ARTHRITIS; GENE EXPRESSION; HUMANS; LIGANDS; POLYMORPHISM, GENETIC; PPAR GAMMA;

EID: 67651089911     PISSN: 10436618     EISSN: 10961186     Source Type: Journal    
DOI: 10.1016/j.phrs.2009.02.005     Document Type: Review

References (88)

1. Abramson S.B., Attur M., and Yazici Y. Prospects for disease modification in osteoarthritis. Nat Clin Pract Rheumatol 2 (2006) 304-312
2. Goldring M.B., and Goldring S.R. Osteoarthritis. J Cell Physiol 213 (2007) 626-634
3. Firestein G.S. Evolving concepts of rheumatoid arthritis. Nature 423 (2003) 356-361
4. Slezes L., Torocsik D., and Nagy L. PPARγ in immunity and inflammation: cell types and diseases. Biochim Biophys Acta 1771 (2007) 1014-1030
5. Muller-Ladner U., Pap T., Gay R.E., Neidhart M., and Gay S. Mechanisms of disease: the molecular and cellular basis of joint destruction in rheumatoid arthritis. Nat Clin Pract Rheumatol 1 (2005) 102-110
6. Shirtliff M.E., and Mader J.T. Acute septic arthritis. Clin Microbiol Rev 15 (2002) 527-544
7. Hueber A.J., and McInnes I.B. Immune regulation in psoriasis and psoriatic arthritis-recent developments. Immunol Lett 114 (2007) 59-65
8. Ene-Stroescu D., and Gorbien M.J. Gouty arthritis. A primer on late-onset gout. Geriatrics 60 (2005) 24-31
9. Thalhamer T., McGrath M.A., and Harnett M.M. MAPKs and their relevence to arthritis and inflammation. Rheumatology 47 (2008) 409-414
10. Raman M., Chen W., and Cobb M.H. Differential regulation and properties of MAPKs. Oncogene 26 (2007) 3100-3112
11. Simmonds R.E., and Foxwell B.M. NF-κB and its relevance to arthritis and inflammation. Rheumatology 47 (2008) 584-590
12. Sacre S.M., Andreakos E., Taylor P., Feldmann M., and Foxwell B.M. Molecular therapeutic targets in rheumatoid arthritis. Expert Rev Mol Med 7 (2005) 1-20
13. Shi S., and Klotz U. Clinical use and pharmacological properties of selective COX-2 inhibitors. Eur J Clin Pharmacol 64 (2008) 233-252
14. Tu G., Xu W., Huang H., and Li S. Progress in the development of matrix metalloproteinase inhibitors. Curr Med Chem 15 (2008) 1388-1395
15. Desvergne B., and Wahli W. Peroxisome proliferator-activated receptors: nuclear control of metabolism. Endocr Rev 20 (1999) 649-688
16. Berger J., and Moller D.E. The mechanisms of action of PPARs. Annu Rev Med 53 (2002) 409-435
17. Kliewer S.A., Forman B.M., Blumberg B., Ong E.S., Borgmeyer U., Mangelsdorf D.J., et al. Differential expression and activation of a family of murine peroxisome proliferator-activated receptors. Proc Natl Acad Sci USA 91 (1994) 7355-7359
18. Chawla A., Schwarz E.J., Dimaculangan D.D., and Lazar M.A. Peroxisome proliferator-activated receptor (PPAR) gamma: adipose-predominant expression and induction early in adipocyte differentiation. Endocrinology 135 (1994) 798-800
19. Braissant O., Foufelle F., Scotto C., Dauça M., and Wahli W. Differential expression of peroxisome proliferator-activated receptors (PPARs): tissue distribution of PPAR-alpha, -beta, and -gamma in the adult rat. Endocrinology 137 (1996) 354-366
20. Jain S., Pulikuri S., Zhu Y., Qi C., Kanwar Y.S., Yeldandi A.V., et al. Differential expression of the peroxisome proliferator-activated receptor gamma (PPARgamma) and its coactivators steroid receptor coactivator-1 and PPAR-binding protein PBP in the brown fat, urinary bladder, colon, and breast of the mouse. Am J Pathol 153 (1998) 349-354
21. Fajas L., Auboeuf D., Raspe E., Schoonjans K., Lefebvre A.M., Saladin R., et al. The organization, promoter analysis, and expression of the human PPARgamma gene. J Biol Chem 272 (1997) 18779-18789
22. Gearing K.L., Gottlicher M., Teboul M., Widmark E., and Gustafsson J.A. Interaction of the peroxisome proliferator-activated receptor and retinoid X receptor. Proc Natl Acad Sci USA 90 (1993) 1440-1444
23. Nolte R.T., Wisely G.B., Westin S., Cobb J.E., Lambert M.H., Kurokawa R., et al. Ligand binding and co-activator assembly of the peroxisome proliferator-activated receptor-gamma. Nature 395 (1998) 137-143
24. Feige J.N., Gelman L., Michalik L., Desvergne B., and Wahli W. From molecular action to physiological outputs: peroxisome proliferator-activated receptors are nuclear receptors at the crossroads of key cellular functions. Progr Lipid Res 45 (2006) 120-159
25. Tolon R.M., Castillo A.I., and Aranda A. Activation of the prolactin protein gene by peroxisome proliferator-activated receptor-alpha appears to be DNA binding-independent. J Biol Chem 273 (1998) 26652-26661
26. Ricote M., Li A.C., Willson T.M., Kelly C.J., and Glass C.K. The peroxisome proliferator-activated receptor-γ is a negative regulator of macrophage activation. Nature 391 (1998) 79-82
27. Feinstein D.L., Spangolo A., Akar C., Weinberg G., Murphy P., Gavrilyuk V., et al. Receptor-independent actions of PPAR thiazolidinedione agonists: Is a mitochondrial function the key?. Biochem Pharm 70 (2005) 177-188
28. Willson T.M., Brown P.J., Strenbach D.D., and Henke B.R. The PPARs: from orphan receptors to drug discovery. J Med Chem 43 (2000) 527-550
29. Schopfer F.J., Lin Y., Baker P.R., Cui T., Garcia-Barrio M., Zhang J., et al. Nitrolinoleic acid: An endogenous peroxisome proliferator-activated receptor gamma ligand. Proc Natl Acad Sci USA 102 (2005) 2340-2345
30. Lehmann J.M., Moore L.B., Smith-Oliver T.A., Wilkison W.O., Willson T.M., and Kliewer S.A. An antidiabetic thiazolidinedione is a high affinity ligand for peroxisome-proliferator-activated receptor γ (PPARγ). J Biol Chem 270 (1995) 12953-12956
31. Henke B.R., Blanchard S.G., Brackeen M.F., Brown K.K., Cobb J.E., Collins J.L., et al. N-(2-Benzoylphenyl)-l-tyrosine PPARγ Agonists. 1. Discovery of a novel series of potent antihyperglycemic and antihyperlipidemic agent. J Med Chem 41 (1998) 5020-5036
32. Lehmann J.M., Lenhard J.M., Oliver B.B., Ringold G.M., and Kliewer S.A. Peroxisome proliferator-activated receptors alpha and gamma are activated by indomethacin and other non-steroidal anti-inflammatory drugs. J Biol Chem 272 (1997) 3406-3410
33. Wysowski D.K., Armstrong G., and Governale L. Rapid increase in the use of oral antidiabetic drugs in the United States, 1990-2001. Diabetes Care 26 (2003) 1852-1855
34. Theocharis S., Margeli A., Vielh P., and Kouraklis G. Peroxisome proliferator-activated receptor-gamma ligands as cell-cycle modulators. Cancer Treat Rev 30 (2004) 545-554
35. Giaginis C., Margeli A., and Theocharis S. Peroxisome proliferator activated receptor-gamma ligands as investigational modulators of angiogenesis. Expert Opin Investig Drugs 16 (2007) 1561-1572
36. Krishnan A., Nair S.A., and Pillai M.R. Biology of PPAR gamma in cancer: a critical review on existing lacunae. Curr Mol Med 7 (2007) 532-540
37. Hamerman D. Osteoporosis and atherosclerosis: biological linkages and the emergence of dual-purpose therapies. Q J Med 98 (2005) 467-484
38. Giaginis C., Tsantili-Kakoulidou A., and Theocharis S. Peroxisome proliferator-activated receptors (PPARs) in the control of bone metabolism. Fundam Clin Pharm 21 (2007) 231-244
39. Tenenbaum A., Motro M., and Fisman E.Z. Dual and pan-peroxisome proliferator-activated receptors (PPAR) co-agonism: the bezafibrate lessons. Cardiovasc Diabetol 4 (2005) 14
40. Rücker C., Scarsi M., and Meringer M. 2D QSAR of PPARgamma agonist binding and transactivation. Bioorg Med Chem 14 (2006) 5178-5195
41. Giaginis C., Theocharis S., and Tsantili-kakoulidou A. Quantitative structure-activity relationships for PPAR-gamma binding and gene transactivation of tyrosine-based agonists using multivariate statistics. Chem Biol Drug Des 72 (2008) 257-264
42. Rizzo G., and Fiorucci S. PPARs and other nuclear receptors in inflammation. Curr Opin Pharm 6 (2006) 421-427
43. Moraes L.A., Piqueras L., and Bishop-Bailey D. Peroxisome proliferator-activated receptors and inflammation. Pharmacol Ther 110 (2006) 371-385
44. Belvisi M.G., Hele D.J., and Birrell M.A. Peroxisome proliferator-activated receptor gamma agonists as therapy for chronic airway inflammation. Eur J Pharmacol 533 (2006) 101-109
45. Delerive P., Fruchart J.C., and Staels B. Peroxisome proliferator-activated receptors in inflammation control. J Endocrinol 169 (2001) 453-459
46. Ueki S., Kato H., Kobayashi Y., Ito W., Adachi T., Nagase H., et al. Anti- and proinflammatory effects of 15-deoxy-delta-prostaglandin J2(15d-PGJ2) on human eosinophil functions. Int Arch Allergy Immunol 143 (2007) 15-22
47. Kodera Y., Takeyama K., Murayama A., Suzawa M., Masuhiro Y., and Kato S. Ligand type-specific interactions of peroxisome proliferator-activated receptor gamma with transcriptional coactivators. J Biol Chem 275 (2000) 33201-33204
48. Abdelrahman M., Sivarajah A., and Thiemermann C. Beneficial effects of PPAR-gamma ligands in ischemia-reperfusion injury, inflammation and shock. Cardiovasc Res 65 (2005) 772-781
49. Desreumaux P., Dubuquoy L., Nutten S., Peuchmaur M., Englaro W., Schoonjans K., et al. Attenuation of colon inflammation through activators of the retinoid X receptor (RXR)/peroxisome proliferator-activated receptor gamma (PPARgamma) heterodimer. A basis for new therapeutic strategies. J Exp Med 193 (2001) 827-838
50. Bordji K., Grillasca J.P., Gouze J.N., Magdalou J., Schohn H., Keller J.M., et al. Evidence for the presence of peroxisome proliferator-activated receptor (PPAR) α and γ and retinoid Z receptor in cartilage. PPARγ activation modulates the effects of interleukin-1β on rat chondrocytes. J Biol Chem 275 (2000) 12243-12250
51. Fahmi H., Di Battista J.A., Pelletier J.P., Mineau F., Ranger P., and Martel-Pelletier J. Peroxisome proliferators-activated receptor gamma activators inhibit interleukin-1beta-induced nitric oxide and matrix metalloproteinase 13 production in human chondrocytes. Arthritis Rheum 44 (2001) 595-607
52. Boyault S., Simonin M.A., Bianchi A., Compe E., Liagre B., Mainard D., et al. 15-Deoxy-delta12,14-PGJ2, but not troglitazone, modulates IL-1beta effects in human chondrocytes by inhibiting NF-kappaB and AP-1 activation pathways. FEBS Lett 501 (2001) 24-30
53. Shao Y.Y., Wang L., Hicks D.G., Tarr S., and Ballock R.T. Expression and activation of peroxisome proliferator-activated receptors in growth plate chondrocytes. J Orthopaedic Res 23 (2005) 1139-1145
54. Ji J.D., Cheon H., Jun J.B., Choi S.J., Kim Y.R., Lee Y.H., et al. Effects of peroxisome proliferator-activated receptor-gamma (PPAR-gamma) on the expression of inflammatory cytokines and apoptosis induction in rheumatoid synovial fibroblasts and monocytes. J Autoimmun 17 (2001) 215-221
55. Kalajdzic T., Faour W.H., He Q.W., Fahmi H., Martel-Pelletier J., Pelletier J.P., et al. Nimesulide, a preferential cyclooxygenase 2 inhibitor, suppresses peroxisome proliferator-activated receptor induction of cyclooxygenase 2 gene expression in human synovial fibroblasts: evidence for receptor antagonism. Arthritis Rheum 46 (2002) 494-506
56. Afif H., Benderdour M., Mfuna-Endam L., Martel-Pelletier J., Pelletier J.P., Duval N., et al. Peroxisome proliferator-activated receptor gamma1 expression is diminished in human osteoarthritic cartilage and is downregulated by interleukin-1beta in articular chondrocytes. Arthritis Res Ther 9 (2007) R31
57. Jiang Y., Mishima H., Sakai S., Liu Y.K., Ohyabu Y., and Uemura T. Gene expression analysis of major lineage-defining factors in human bone marrow cells: effect of aging, gender, and age-related disorders. J Orthop Res 26 (2008) 910-917
58. Yamazaki R., Kusunoki N., Matsuzaki T., Hashimoto S., and Kawai S. Nonsteroidal anti-inflammatory drugs induce apoptosis in association with activation of peroxisome proliferator-activated receptor gamma in rheumatoid synovial cells. J Pharmacol Exp Ther 302 (2002) 18-25
59. Kawahito Y., Kondo M., Tsubouchi Y., Hashiramoto A., Bishop-Bailey D., Inoue K., et al. 15-deoxy-delta(12,14)-PGJ(2) induces synoviocyte apoptosis and suppresses adjuvant-induced arthritis in rats. J Clin Invest 106 (2000) 189-197
60. Cheng S., Afif H., Martel-Pelletier J., Benderdour M., Pelletier J.P., Hilal G., et al. Association of polymorphisms in the peroxisome proliferator-activated receptor gamma gene and osteoarthritis of the knee. Ann Rheum Dis 65 (2006) 1394-1397
61. El-Sohemy A., Cornelis M.C., Park Y.W., and Bae S.C. Catalase and PPARgamma2 genotype and risk of rheumatoid arthritis in Koreans. Rheumatol Int 26 (2006) 388-392
62. Butt C., Gladman D., and Rahman P. PPAR-gamma gene polymorphisms and psoriatic arthritis. J Rheumatol 33 (2006) 1631-1633
63. Fahmi H., Pelletier J.P., Di Battista J.A., Cheung H.S., Fernandes J.C., and Martel-Pelletier J. Peroxisome proliferator-activated receptor gamma activators inhibit MMP-1 production in human synovial fibroblasts likely by reducing the binding of the activator protein 1. Osteoarthritis Cartilage 10 (2002) 100-108
64. Kanata S., Akagi M., Nishimura S., Hayakawa S., Yoshida K., Sawamura T., et al. Oxidized LDL binding to LOX-1 upregulates VEGF expression in cultured bovine chondrocytes through activation of PPAR-gamma. Biochem Biophys Res Commun 348 (2006) 1003-1010
65. Panigrahy D., Huang S., Kieran M.W., and Kaipainen A. PPARγ as a therapeutic target for tumor angiogenesis and metastasis. Cancer Biol Ther 4 (2005) 687-693
66. Giaginis C., Tsantili-Kakoulidou A., and Theocharis S. Peroxisome proliferator activated receptor-gamma ligands: potential pharmacological agents for targeting the angiogenesis signaling cascade in cancer. PPAR Res 2008 (2008) 431763
67. Shan Z.Z., Masuko-Hongo K., Dai S.M., Nakamura H., Kato T., and Nishioka K. A potential role of 15-deoxy-delta(12,14)-prostaglandin J2 for induction of human articular chondrocyte apoptosis in arthritis. J Biol Chem 279 (2004) 37939-37950
68. Cheng S., Afif H., Martel-Pelletier J., Pelletier J.P., Li X., Farrajota K., et al. Activation of peroxisome proliferator-activated receptor gamma inhibits interleukin-1beta-induced membrane-associated prostaglandin E2 synthase-1 expression in human synovial fibroblasts by interfering with Egr-1. J Biol Chem 279 (2004) 22057-22065
69. Yamasaki S., Nakashima T., Kawakami A., Miyashita T., Tanaka F., Ida H., et al. Cytokines regulate fibroblast-like synovial cell differentiation to adipocyte-like cells. Rheumatology (Oxford) 43 (2004) 448-452
70. Boileau C., Martel-Pelletier J., Fahmi H., Mineau F., Boily M., and Pelletier J.P. The peroxisome proliferator-activated receptor gamma agonist pioglitazone reduces the development of cartilage lesions in an experimental dog model of osteoarthritis: in vivo protective effects mediated through the inhibition of key signaling and catabolic pathways. Arthritis Rheum 56 (2007) 2288-2298
71. Kobayashi T., Notoya K., Naito T., Unno S., Nakamura A., Martel-Pelletier J., et al. Pioglitazone, a peroxisome proliferator-activated receptor gamma agonist, reduces the progression of experimental osteoarthritis in guinea pigs. Arthritis Rheum 52 (2005) 479-487
72. Hounoki H., Sugiyama E., Mohamed S.G., Shinoda K., Taki H., Abdel-Aziz H.O., et al. Activation of peroxisome proliferator-activated receptor gamma inhibits TNF-alpha-mediated osteoclast differentiation in human peripheral monocytes in part via suppression of monocyte chemoattractant protein-1 expression. Bone 42 (2008) 765-774
73. Sumariwalla P.F., Palmer C.D., Pickford L.B., Feldmann M., Foxwell B.M., and Brennan F.M. Suppression of tumour necrosis factor production from mononuclear cells by a novel synthetic compound, CLX-090717. Rheumatology (Oxford) 48 (2009) 32-38
74. Ishino H., Kawahito Y., Tsubouchi Y., Kohno M., Wada M., Yamamoto A., et al. Feedback control of the arachidonate cascade in osteoblastic cells by 15-deoxy-delta-prostaglandin J(2). J Clin Biochem Nutr 42 (2008) 64-69
75. Tsubouchi Y., Kawahito Y., Kohno M., Inoue K., Hla T., and Sano H. Feedback control of the arachidonate cascade in rheumatoid synoviocytes by 15-deoxy-Delta(12,14)-prostaglandin J2. Biochem Biophys Res Commun 283 (2001) 750-755
76. Simonin M.A., Bordji K., Boyault S., Bianchi A., Gouze E., Bécuwe P., et al. PPAR-gamma ligands modulate effects of LPS in stimulated rat synovial fibroblasts. Am J Physiol Cell Physiol 282 (2002) C125-133
77. Moulin D., Poleni P.E., Kirchmeyer M., Sebillaud S., Koufany M., Netter P., et al. Effect of peroxisome proliferator activated receptor (PPAR)gamma agonists on prostaglandins cascade in joint cells. Biorheology 43 (2006) 561-575
78. Meier C.A., Chicheportiche R., Juge-Aubry C.E., Dreyer M.G., and Dayer J.M. Regulation of the interleukin-1 receptor antagonist in THP-1 cells by ligands of the peroxisome proliferator-activated receptor gamma. Cytokine 18 (2002) 320-328
79. Bianchi A., Moulin D., Sebillaud S., Koufany M., Galteau M.M., Netter P., et al. Contrasting effects of peroxisome-proliferator-activated receptor (PPAR)gamma agonists on membrane-associated prostaglandin E2 synthase-1 in IL-1beta-stimulated rat chondrocytes: evidence for PPARgamma-independent inhibition by 15-deoxy-Delta12,14prostaglandin J2. Arthritis Res Ther 7 (2005) R1325-1337
80. Johnson D.R., Stebulis J.A., Rossetti R.G., Burstein S.H., and Zurier R.B. Suppression of fibroblast metalloproteinases by ajulemic acid, a nonpsychoactive cannabinoid acid. J Cell Biochem 100 (2007) 184-190
81. Parker J., Atez F., Rossetti R.G., Skulas A., Patel R., and Zurier R.B. Suppression of human macrophage interleukin-6 by a nonpsychoactive cannabinoid acid. Rheumatol Int 28 (2008) 631-635
82. Yamasaki S., Nakashima T., Kawakami A., Miyashita T., Ida H., Migita K., et al. Functional changes in rheumatoid fibroblast-like synovial cells through activation of peroxisome proliferator-activated receptor gamma-mediated signalling pathway. Clin Exp Immunol 129 (2002) 379-384
83. Kusunoki N., Yamazaki R., and Kawai S. Induction of apoptosis in rheumatoid synovial fibroblasts by celecoxib, but not by other selective cyclooxygenase 2 inhibitors. Arthritis Rheum 46 (2002) 3159-3167
84. Shiojiri T., Wada K., Nakajima A., Katayama K., Shibuya A., Kudo C., et al. PPAR gamma ligands inhibit nitrotyrosine formation and inflammatory mediator expressions in adjuvant-induced rheumatoid arthritis mice. Eur J Pharmacol 448 (2002) 231-238
85. Koufany M., Moulin D., Bianchi A., Muresan M., Sebillaud S., Netter P., et al. Anti-inflammatory effect of antidiabetic thiazolidinediones prevents bone resorption rather than cartilage changes in experimental polyarthritis. Arthritis Res Ther 10 (2008) R6
86. Tomita T., Kakiuchi Y., and Tsao P.S. THR0921, a novel peroxisome proliferator-activated receptor gamma agonist, reduces the severity of collagen-induced arthritis. Arthritis Res Ther 8 (2006) R7
87. Bongartz T., Coras B., Vogt T., Schölmerich J., and Müller-Ladner U. Treatment of active psoriatic arthritis with the PPARgamma ligand pioglitazone: an open-label pilot study. Rheumatology (Oxford) 44 (2005) 126-129
88. Akahoshi T., Namai R., Murakami Y., Watanabe M., Matsui T., Nishimura A., et al. Rapid induction of peroxisome proliferator-activated receptor gamma expression in human monocytes by monosodium urate monohydrate crystals. Arthritis Rheum 48 (2003) 231-239