The role of the peroxisome proliferator-activated receptor-α (PPAR-α) in the regulation of acute inflammation

Journal of Leukocyte Biology

Volumn 79, Issue 5, 2006, Pages 999-1010

  Cuzzocrea, Salvatore ^a   Mazzon, Emanuela ^a   Di Paola, Rosanna ^a   Peli, Angelo ^b   Bonato, Andrea ^b   Britti, Domenico ^c   Genovese, Tiziana ^a   Muià, Carmelo ^a   Crisafulli, Concetta ^a   Caputi, Achille P ^a  

^a UNIVERSITY OF MESSINA   (Italy)

^b UNIVERSITY OF BOLOGNA   (Italy)

^c UNIVERSITY OF TERAMO   (Italy)

Author keywords

Carrageenan induced paw edema; Carrageenan induced pleurisy; Cytokines; Neutrophil infiltration

Indexed keywords

CARRAGEENAN; CELL NUCLEUS RECEPTOR; FAS LIGAND; INTERLEUKIN 1BETA; MYELOPEROXIDASE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; TRANSCRIPTION FACTOR; TUMOR NECROSIS FACTOR ALPHA; AUTACOID; FASL PROTEIN, MOUSE; IMMUNOLOGIC FACTOR; INTERLEUKIN 1; MEMBRANE PROTEIN; TUMOR NECROSIS FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; GENE EXPRESSION; HISTOLOGY; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PAW EDEMA; PLEURISY; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ACUTE DISEASE; ANIMAL; CHEMICALLY INDUCED DISORDER; DISEASE MODEL; DRUG EFFECT; EDEMA; FEMALE; FOOT; GENETICS; IMMUNOLOGY; LUNG; MALE; METABOLISM; MOUSE MUTANT; PATHOPHYSIOLOGY; SIGNAL TRANSDUCTION; UPREGULATION;

ANIMALIA;

ACUTE DISEASE; ANIMALS; CARRAGEENAN; CHEMOTAXIS, LEUKOCYTE; DISEASE MODELS, ANIMAL; EDEMA; FAS LIGAND PROTEIN; FEMALE; FOOT; IMMUNOLOGIC FACTORS; INFLAMMATION; INFLAMMATION MEDIATORS; INTERLEUKIN-1; LUNG; MALE; MEMBRANE GLYCOPROTEINS; MICE; MICE, KNOCKOUT; PLEURISY; PPAR ALPHA; SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTOR-ALPHA; TUMOR NECROSIS FACTORS; UP-REGULATION;

EID: 33745309774     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0605341     Document Type: Article

References (51)

1. Tomlinson, A., Appleton, I., Moore, A. R., Gilroy, D. W., Willis, D., Mitchell, J. A., Willoughby, D. A. (1994) Cyclo-oxygenase and nitric oxide synthase isoforms in rat carrageenin-induced pleurisy. Br. J. Pharmacol. 113, 693-698.
2. Nantel, F., Denis, D., Gordon, R., Northey, A., Cirino, M., Metters, K. M., Chan, C. C. (1999) Distribution and regulation of cyclooxygenase-2 in carrageenan-induced inflammation. Br. J. Pharmacol. 128, 853-859.
3. Salvemini, D., Wang, Z. Q., Bourdon, D. M., Stern, M. K., Currie, M. G., Manning, P. T. (1996) Evidence of peroxynitrite involvement in the carrageenan-induced rat paw edema. Eur. J. Pharmacol. 303, 217-220.
4. Evans, R. M. (1988) The steroid and thyroid hormone receptor superfamily. Science 240, 889-895.
5. Murphy, G. J., Holder, J. C. (2000) PPAR-γ agonists: therapeutic role in diabetes, inflammation and cancer. Trends Pharmacol. Sci. 21, 469-474.
6. Wayman, N., McDonald, M. C., Threadgill, M. D., Thiemermann, C. (2001) 5 Amino isoquinolinone, a potent inhibitor of poly (adenosine 5′-diphosphate ribose) polymerase, reduces myocardial infarct size. Eur. J. Pharmacol. 430, 93-100.
7. Sher, T., Yi, H. F., McBride, O. W., Gonzalez, F. J. (1993) cDNA cloning, chromosomal mapping, and functional characterization of the human peroxisome proliferator activated receptor. Biochemistry 32, 5598-5604.
8. Lovett-Racke, A. E., Hussain, R. Z., Northrop, S., Choy, J., Rocchini, A., Matthes, L., Chavis, J. A., Diab, A., Drew, P. D., Racke, M. K. (2004) Peroxisome proliferator-activated receptor α agonists as therapy for autoimmune disease. J. Immunol. 172, 5790-5798.
9. Cunard, R., Ricote, M., DiCampli, D., Archer, D. C., Kahn, D. A., Glass, C. K., Kelly, C. J. (2002) Regulation of cytokine expression by ligands of peroxisome proliferator activated receptors. J. Immunol. 168, 2795-2802.
10. Marx, N., Kehrle, B., Kohlhammer, K., Grub, M., Koenig, W., Hombach, V., Libby, P., Plutzky, J. (2002) PPAR activators as antiinflammatory mediators in human T lymphocytes: implications for atherosclerosis and transplantation- associated arteriosclerosis. Circ. Res. 90, 703-710.
11. Devchand, P. R., Keller, H., Peters, J. M., Vazquez, M., Gonzalez, F. J., Wahli, W. (1996) The PPARα-leukotriene B4 pathway to inflammation control. Nature 384, 39-43.
12. Staels, B., Koenig, W., Habib, A., Merval, R., Lebret, M., Torra, I. P., Delerive, P., Fadel, A., Chinetti, G., Fruchart, J. C., Najib, J., Maclouf, J., Tedgui, A. (1998) Activation of human aortic smooth-muscle cells is inhibited by PPARα but not by PPARγ activators. Nature 393, 790-793.
13. Cuzzocrea, S., Di Paola, R., Mazzon, E., Genovese, T., Muia, C., Centorrino, T., Caputi, A. P. (2004) Role of endogenous and exogenous ligands for the peroxisome proliferators activated receptors α (PPAR-α) in the development of inflammatory bowel disease in mice. Lab. Invest. 84, 1643-1654.
14. Genovese, T., Mazzon, E., Di Paola, R., Cannavo, G., Muia, C., Bramanti, P., Cuzzocrea, S. (2005) Role of endogenous ligands for the peroxisome proliferators activated receptors α in the secondary damage in experimental spinal cord trauma. Exp. Neurol. 194, 267-278.
15. Forman, B. M., Chen, J., Evans, R. M. (1996) The peroxisome proliferator-activated receptors: ligands and activators. Ann. N. Y. Acad. Sci. 804, 266-275.
16. Staels, B., Dallongeville, J., Auwerx, J., Schoonjans, K., Leitersdorf, E., Fruchart, J. C. (1998) Mechanism of action of fibrates on lipid and lipoprotein metabolism. Circulation 98, 2088-2093 (Review).
17. Takano, H., Nagai, T., Asakawa, M., Toyozaki, T., Oka, T., Komuro, I., Saito, T., Masuda, Y. (2000) Peroxisome proliferator-activated receptor activators inhibit lipopolysaccharide-induced tumor necrosis factor-α expression in neonatal rat cardiac myocytes. Circ. Res. 87, 596-602.
18. Okamoto, H., Iwamoto, T., Kotake, S., Momohara, S., Yamanaka, H., Kamatani, N. (2005) Inhibition of NF-κB signaling by fenofibrate, a peroxisome proliferator-activated receptor-α ligand, presents a therapeutic strategy for rheumatoid arthritis. Clin. Exp. Rheumatol. 23, 323-330.
19. Delerive, P., De Bosscher, K., Besnard, S., Vanden Berghe, W., Peters, J. M., Gonzalez, F. J., Fruchart, J. C., Tedgui, A., Haegeman, G., Staels, B. (1999) Peroxisome proliferator-activated receptor α negatively regulates the vascular inflammatory gene response by negative cross-talk with transcription factors NF-κB and AP-1. J. Biol. Chem. 274, 32048-32054.
20. Spencer, N. F., Poynter, M. E., Im, S. Y., Daynes, R. A. (1997) Constitutive activation of NF-κ B in an animal model of aging. Int. Immunol. 9, 1581-1588.
21. Delerive, P., Gervois, P., Fruchart, J. C., Staels, B. (2000) Induction of IκBα expression as a mechanism contributing to the anti-inflammatory activities of peroxisome proliferator-activated receptor-α activators. J. Biol. Chem. 275, 36703-36707.
22. Hill, M. R., Clarke, S., Rodgers, K., Thornhill, B., Peters, J. M., Gonzalez, F. J., Gimble, J. M. (1999) Effect of peroxisome proliferator- activated receptor α activators on tumor necrosis factor expression in mice during endotoxemia. Infect. Immun. 67, 3488-3493.
23. Dyroy, E., Yndestad, A., Ueland, T., Halvorsen, B., Damas, J. K., Aukrust, P., Berge, R. K. (2005) Antiinflammatory effects of tetradecylthioacetic acid involve both peroxisome proliferator-activated receptor α-dependent and -independent pathways. Arterioscler. Thromb. Vasc. Biol. 25, 1364-1369.
24. Jackson, T. A., Richer, J. K., Bain, D. L., Takimoto, G. S., Tung, L., Horwitz, K. B. (1997) The partial agonist activity of antagonist-occupied steroid receptors is controlled by a novel hinge domain-binding coactivator L7/SPA and the corepressors N-CoR or SMRT. Mol. Endocrinol. 11, 693-705.
25. Cuzzocrea, S., Mazzon, E., Bevilaqua, C., Costantino, G., Britti, D., Mazzullo, G., De Sarro, A., Caputi, A. P. (2000) Cloricromene, a coumarine derivative, protects against collagen-induced arthritis in Lewis rats. Br. J. Pharmacol. 131, 1399-1407.
26. Lo Verme, J., Fu, J., Astarita, G., La Rana, G., Russo, R., Calignano, A., Piomelli, D. (2005) The nuclear receptor peroxisome proliferator-activated receptor-α mediates the anti-inflammatory actions of palmitoylethanolamide. Mol. Pharmacol. 67, 15-19.
27. Cuzzocrea, S., McDonald, M. C., Mazzon, E., Siriwardena, D., Serraino, I., Dugo, L., Britti, D., Mazzullo, G., Caputi, A. P., Thiemermann, C. (2000) Calpain inhibitor I reduces the development of acute and chronic inflammation. Am. J. Pathol. 157, 2065-2079.
28. Mullane, K. M., Kraemer, R., Smith, B. (1985) Myeloperoxidase activity as a quantitative assessment of neutrophil infiltration into ischemic myocardium. J. Pharmacol. Methods 14, 157-167.
29. Bustin, S. A. (2000) Absolute quantification of mRNA using real-time reverse transcription polymerase chain reaction assay. J. Mol. Endocrinol. 25, 169-193.
30. Rioja, I., Bush, K. A., Buckton, J. B., Dickson, M. C., Life, P. F. (2004) Joint cytokine quantification in two rodent arthritis models: kinetics of expression, correlation of mRNA and protein levels and response to prednisolone treatment. Clin. Exp. Immunol. 137, 65-73.
31. Hargreaves, K. M., Troullos, E. S., Dionne, R. A., Schmidt, E. A., Schafer, S. C., Joris, J. L. (1988) Bradykinin is increased during acute and chronic inflammation: therapeutic implications. Clin. Pharmacol. Ther. 44, 613-621.
32. Clark, R.B. (2002) The role of PPARs in inflammation and immunity. J. Leukoc. Biol. 71, 388-400.
33. Peters, J. M., Hennuyer, N., Staels, B., Fruchart, J-C., Fievet, C., Gonzales, F. J., Auwerx, J. (1997) Alterations in lipoprotein metabolism in peroxisome proliferator-activated receptor α-deficient mice. J. Biol. Chem. 272, 27307-27312.
34. Aoyama, T., Peters, J. M., Iritani, N., Nakajima, T., Furihata, K., Hashimoto, T., Gonzalez, F. J. (1998) Altered constitutive expression of fatty-acid-metabolizing enzymes in mice lacking the peroxisome proliferator receptor α. J. Biol. Chem. 273, 5678-5684.
35. Devchand, P. R., Keller, H., Peters, J. M., Vasquez, M., Gonzales, F. J., Wahli, W. (1996) The PPARα-leukotriene B4 pathway to inflammation control. Nature 384, 39-43.
36. Kleemann, R., Gervois, P. P., Verschuren, L., Staels, B., Princen, H. M., Kooistra, T. (2003) Fibrates down-regulate IL-1-stimulated C-reactive protein gene expression in hepatocytes by reducing nuclear p50-NFκ B-C/EBP-β complex formation. Blood 101, 545-551.
37. Gervois, P., Vu-Dac, N., Kleemann, R., Kockx, M., Dubois, G., Laine, B., Kosykh, V., Fruchart, J. C., Kooistra, T., Staels, B. (2001) Negative regulation of human fibrinogen gene expression by peroxisome proliferator-activated receptor α agonists via inhibition of CCAAT box/enhancer-binding protein β. J. Biol. Chem. 276, 33471-33477.
38. Sharma, K., Wang, R. X., Zhang, L. Y., Yin, D. L., Luo, X. Y., Solomon, J. C., Jiang, R. F., Markos, K., Davidson, W., Scott, D. W., Shi, Y. F. (2000) Death the Fas way: regulation and pathophysiology of CD95 and its ligand. Pharmacol. Ther. 88, 333-347.
39. Dosreis, G. A., Borges, V. M., Zin, W. A. (2004) The central role of Fas-ligand cell signaling in inflammatory lung diseases. J. Cell. Mol. Med. 8, 285-293.
40. Bauer, M. K., Vogt, M., Los, M., Siegel, J., Wesselborg, S., Schulze-Osthoff, K. (1998) Role of reactive oxygen intermediates in activation-induced CD95 (APO-1/Fas) ligand expression. J. Biol. Chem. 273, 8048-8055.
41. Cuzzocrea, S., Pisano, B., Dugo, L., Ianaro, A., Ndengele, M., Salvemini, D. (2004) Superoxide-related signaling cascade mediates nuclear factor-κB activation in acute inflammation. Antioxid. Redox Signal. 6, 699-704.
42. Salvemini, D., Mazzon, E., Dugo, L., Riley, D. P., Serraino, I., Caputi, A. P., Cuzzocrea, S. (2001) Pharmacological manipulation of the inflammatory cascade by the superoxide dismutase mimetic, M40403. Br. J. Pharmacol. 132, 815-827.
43. Hohlbaum, A. M., Gregory, M. S., Ju, S. T., Marshak-Rothstein, A. (2001) Fas ligand engagement of resident peritoneal macrophages in vivo induces apoptosis and the production of neutrophil chemotactic factors. J. Immunol. 167, 6217-6224.
44. Yamamoto, K., Arakawa, T., Ueda, N., Yamamoto, S. (1995) Transcriptional roles of nuclear factor κ B and nuclear factor-interleukin-6 in the tumor necrosis factor-α-dependent induction of cyclooxygenase-2 in MC3T3-E1 cells. J. Biol. Chem. 270, 31315-31320.
45. Crofford, L. J., Tan, B., McCarthy, C. J., Hla, T. (1997) Involvement of nuclear factor κ B in the regulation of cyclooxygenase-2 expression by interleukin-1 in rheumatoid synoviocytes. Arthritis Rheum. 40, 226-236.
46. Inoue, S., Kawanishi, S. (1995) Oxidative DNA damage induced by simultaneous generation of nitric oxide and superoxide. FEBS Lett. 371, 86-88.
47. Hill, M. R., Clarke, S., Rodgers, K., Thornhill, B., Peters, J. M., Gonzalez, F. J., Gimble, J. M. (1999) Effect of perooxisome proliferatoractivated receptor α activators on tumor necrosis factor expression in mice during endotoxemia. Infect. Immun. 67, 3488-3493.
48. Cuzzocrea, S., Di Paola, R., Mazzon, E., Genovese, T., Muia, C., Centorrino, T., Caputi, A. P. (2004) Role of endogenous and exogenous ligands for the peroxisome proliferators activated receptors α (PPAR-α) in the development of inflammatory bowel disease in mice. Lab. Invest. 84, 1643-1654.
49. Jackson, S. M., Parhami, F., Xi, X. P., Berliner, J. A., Hsueh, W. A., Law, R. E., Demer, L. L. (1999) Peroxisome proliferator-activated receptor activators target human endothelial cells to inhibit leukocyte-endothelial cell interaction. Arterioscler. Thromb. Vasc. Biol. 19, 2094-2104.
50. Lee, H., Shi, W., Tontonoz, P., Wang, S., Subbanagounder, G., Hedrick, C. C., Hama, S., Borromeo, C., Evans, R. M., Berliner, J. A., Nagy, L. (2000) Role for peroxisome proliferator-activated receptor α in oxidized phospholipid-induced synthesis of monocyte chemotactic protein-1 and interleukin-8 by endothelial cells. Circ. Res. 87, 516-521.
51. Marx, N., Sukhova, G., Collins, T., Libby, P., Plutzky, J. (1999) PPAR α activators inhibit cytokine-induced vascular cell adhesion molecule-1 expression in human endothelial cells. Circulation 99, 3125-3131.