Macrophage epoxygenase determines a profibrotic transcriptome signature

Journal of Immunology

Volumn 194, Issue 10, 2015, Pages 4705-4716

  Behmoaras, Jacques ^a   Diaz, Ana Garcia ^b   Venda, Lara ^b   Ko, Jeong Hun ^a   Srivastava, Prashant ^b,c   Montoya, Alex ^b   Faull, Peter ^b   Webster, Zoe ^b   Moyon, Ben ^b   Pusey, Charles D ^d   Abraham, David J ^e   Petretto, Enrico ^b,c   Cook, Terence H ^a   Aitman, Timothy J ^a,f  

^a HAMMERSMITH HOSPITAL   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c DUKE NUS MEDICAL SCHOOL   (Singapore)

^d IMPERIAL COLLEGE LONDON   (United Kingdom)

^e ROYAL FREE AND UNIVERSITY COLLEGE MEDICAL SCHOOL   (United Kingdom)

^f UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN TYPE 1; CYTOCHROME P450 2J2; EPOXYGENASE CYP2J4; EPOXYICOSATRIENOIC ACID; FIBRONECTIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; RNA; UNCLASSIFIED DRUG; ZINC FINGER NUCLEASE; ARACHIDONATE EPOXYGENASE; CYP2J4 PROTEIN, RAT; CYTOCHROME P450; TRANSCRIPTOME;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ANALYSIS; ENZYME REGULATION; EXTRACELLULAR MATRIX; FATTY ACID SYNTHESIS; FIBROSIS; GENE DELETION; GENE EXPRESSION; GLOMERULONEPHRITIS; HIGH THROUGHPUT SEQUENCING; HUMAN; HUMAN CELL; IN VITRO STUDY; INFLAMMATION; LIQUID CHROMATOGRAPHY; MACROPHAGE FUNCTION; MALE; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN EXPRESSION; PROTEOMICS; RAT; TANDEM MASS SPECTROMETRY; TRANSCRIPTOMICS; UPREGULATION; URETER OBSTRUCTION; ANIMAL; DISEASE MODEL; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYMOLOGY; GENE INACTIVATION; GENETICS; MACROPHAGE; METABOLISM; REAL TIME POLYMERASE CHAIN REACTION; RNA INTERFERENCE; WESTERN BLOTTING; WISTAR KYOTO RAT;

ANIMALS; BLOTTING, WESTERN; CHROMATOGRAPHY, LIQUID; CYTOCHROME P-450 ENZYME SYSTEM; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FIBROSIS; GENE KNOCKOUT TECHNIQUES; GLOMERULONEPHRITIS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; MACROPHAGES; MALE; RATS; RATS, INBRED WKY; REAL-TIME POLYMERASE CHAIN REACTION; RNA INTERFERENCE; TANDEM MASS SPECTROMETRY; TRANSCRIPTOME;

EID: 84929094973     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1402979     Document Type: Article

References (51)

1. Barrios-Rodiles, M., and K. Chadee. 1998. Novel regulation of cyclooxygenase-2 expression and prostaglandin E2 production by IFN-gamma in human macrophages. J. Immunol. 161: 2441-2448.
2. Dalli, J., and C. N. Serhan. 2012. Specific lipid mediator signatures of human phagocytes: microparticles stimulate macrophage efferocytosis and pro-resolving mediators. Blood 120: e60-e72. Available at: http://www.bloodjournal.org/content/120/15/e60.long?sso-checked=true.
3. Martinez, F. O., S. Gordon, M. Locati, and A. Mantovani. 2006. Transcriptional profiling of the human monocyte-to-macrophage differentiation and polarization: new molecules and patterns of gene expression. J. Immunol. 177: 7303-7311.
4. Peters-Golden, M., and W. R. Henderson, Jr. 2007. Leukotrienes. N. Engl. J. Med. 357: 1841-1854.
5. Murray, P. J., and T. A. Wynn. 2011. Protective and pathogenic functions of macrophage subsets. Nat. Rev. Immunol. 11: 723-737.
6. Frömel, T., K. Kohlstedt, R. Popp, X. Yin, K. Awwad, E. Barbosa-Sicard, A. C. Thomas, R. Lieberz, M. Mayr, and I. Fleming. 2013. Cytochrome P4502S1: a novel monocyte/macrophage fatty acid epoxygenase in human atherosclerotic plaques. Basic Res. Cardiol. 108: 319.
7. Imig, J. D. 2012. Epoxides and soluble epoxide hydrolase in cardiovascular physiology. Physiol. Rev. 92: 101-130.
8. Zeldin, D. C. 2001. Epoxygenase pathways of arachidonic acid metabolism. J. Biol. Chem. 276: 36059-36062.
9. Node, K., Y. Huo, X. Ruan, B. Yang, M. Spiecker, K. Ley, D. C. Zeldin, and J. K. Liao. 1999. Anti-inflammatory properties of cytochrome P450 epoxygenase-derived eicosanoids. Science 285: 1276-1279.
10. Imig, J. D., and B. D. Hammock. 2009. Soluble epoxide hydrolase as a therapeutic target for cardiovascular diseases. Nat. Rev. Drug Discov. 8: 794-805.
11. Wang, X., L. Ni, L. Yang, Q. Duan, C. Chen, M. L. Edin, D. C. Zeldin, and D. W. Wang. 2014. CYP2J2-derived epoxyeicosatrienoic acids suppress endoplasmic reticulum stress in heart failure. Mol. Pharmacol. 85: 105-115.
12. Ma, B., X. Xiong, C. Chen, H. Li, X. Xu, X. Li, R. Li, G. Chen, R. T. Dackor, D. C. Zeldin, and D. W. Wang. 2013. Cardiac-specific overexpression of CYP2J2 attenuates diabetic cardiomyopathy in male streptozotocin-induced diabetic mice. Endocrinology 154: 2843-2856.
13. Moshal, K. S., D. C. Zeldin, S. D. Sithu, U. Sen, N. Tyagi, M. Kumar, W. M. Hughes, Jr., N. Metreveli, D. S. Rosenberger, M. Singh, et al. 2008. Cytochrome P450 (CYP) 2J2 gene transfection attenuates MMP-9 via inhibition of NF-kappabeta in hyperhomocysteinemia. J. Cell. Physiol. 215: 771-781.
14. Cai, Z., G. Zhao, J. Yan, W. Liu, W. Feng, B. Ma, L. Yang, J. A. Wang, L. Tu, and D. W. Wang. 2013. CYP2J2 overexpression increases EETs and protects against angiotensin II-induced abdominal aortic aneurysm in mice. J. Lipid Res. 54: 1448-1456.
15. Hye Khan, M. A., J. Neckár, V. Manthati, R. Errabelli, T. S. Pavlov, A. Staruschenko, J. R. Falck, and J. D. Imig. 2013. Orally active epoxyeicosatrienoic acid analog attenuates kidney injury in hypertensive Dahl salt-sensitive rat. Hypertension 62: 905-913.
16. Bystrom, J., S. J. Thomson, J. Johansson, M. L. Edin, D. C. Zeldin, D. W. Gilroy, A. M. Smith, and D. Bishop-Bailey. 2013. Inducible CYP2J2 and its product 11,12-EET promotes bacterial phagocytosis: a role for CYP2J2 deficiency in the pathogenesis of Crohn's disease? PLoS ONE 8: e75107. Available at: http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0075107.
17. Nakayama, K., T. Nitto, T. Inoue, and K. Node. 2008. Expression of the cytochrome P450 epoxygenase CYP2J2 in human monocytic leukocytes. Life Sci. 83: 339-345.
18. Nichols, J. L., W. Gladwell, K. C. Verhein, H. Y. Cho, J. Wess, O. Suzuki, T. Wiltshire, and S. R. Kleeberger. 2014. Genome-wide association mapping of acute lung injury in neonatal inbred mice. FASEB J. 28: 2538-2550.
19. Smith, K. R., K. E. Pinkerton, T. Watanabe, T. L. Pedersen, S. J. Ma, and B. D. Hammock. 2005. Attenuation of tobacco smoke-induced lung inflammation by treatment with a soluble epoxide hydrolase inhibitor. Proc. Natl. Acad. Sci. USA 102: 2186-2191.
20. Fleming, I. 2014. The pharmacology of the cytochrome P450 epoxygenase/ soluble epoxide hydrolase axis in the vasculature and cardiovascular disease. Pharmacol. Rev. 66: 1106-1140.
21. Zhou, G. L., A. Beloiartsev, B. Yu, D. M. Baron, W. Zhou, R. Niedra, N. Lu, L. T. Tainsh, W. M. Zapol, B. Seed, and K. D. Bloch. 2013. Deletion of the murine cytochrome P450 Cyp2j locus by fused BAC-mediated recombination identifies a role for Cyp2j in the pulmonary vascular response to hypoxia. PLoS Genet. 9: e1003950. Available at: http://journals.plos.org/plosgenetics/article?id10.1371/journal.pgen.1003950.
22. Wu, S., C. R. Moomaw, K. B. Tomer, J. R. Falck, and D. C. Zeldin. 1996. Molecular cloning and expression of CYP2J2, a human cytochrome P450 arachidonic acid epoxygenase highly expressed in heart. J. Biol. Chem. 271: 3460-3468.
23. Robinson, M. D., D. J. McCarthy, and G. K. Smyth. 2010. edgeR: a Bio-conductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139-140.
24. Lefterova, M. I., Y. Zhang, D. J. Steger, M. Schupp, J. Schug, A. Cristancho, D. Feng, D. Zhuo, C. J. Stoeckert, Jr., X. S. Liu, and M. A. Lazar. 2008. PPARgamma and C/EBP factors orchestrate adipocyte biology via adjacent binding on a genome-wide scale. Genes Dev. 22: 2941-2952.
25. D'Souza, Z., S. P. McAdoo, J. Smith, C. D. Pusey, H. T. Cook, J. Behmoaras, and T. J. Aitman. 2013. Experimental crescentic glomerulonephritis: a new bicongenic rat model. Dis. Model. Mech. 6: 1477-1486.
26. Seluanov, A., A. Vaidya, and V. Gorbunova. 2010. Establishing primary adult fibroblast cultures from rodents. J. Vis. Exp. 44. Available at: http://www.jove.com/video/2033/establishing-primary-adult-fibroblast-cultures-from-rodents.
27. Rotival, M., J. H. Ko, P. K. Srivastava, A. Kerloc'h, A. Montoya, C. Mauro, P. Faull, P. R. Cutillas, E. Petretto, and J. Behmoaras. 2015. Integrating phosphoproteome and transcriptome reveals new determinants of macrophage multinucleation. Mol. Cell. Proteomics 14: 484-498.
28. Liu, Y., Y. Zhang, K. Schmelzer, T. S. Lee, X. Fang, Y. Zhu, A. A. Spector, S. Gill, C. Morisseau, B. D. Hammock, and J. Y. Shyy. 2005. The antiinflammatory effect of laminar flow: the role of PPARgamma, epoxyeicosatrienoic acids, and soluble epoxide hydrolase. Proc. Natl. Acad. Sci. USA 102: 16747-16752.
29. Tam, F. W., J. Smith, D. Morel, A. M. Karkar, E. M. Thompson, H. T. Cook, and C. D. Pusey. 1999. Development of scarring and renal failure in a rat model of crescentic glomerulonephritis. Nephrol. Dial. Transplant. 14: 1658-1666.
30. Abraham, N. G., K. Sodhi, A. M. Silvis, L. Vanella, G. Favero, R. Rezzani, C. Lee, D. C. Zeldin, and M. L. Schwartzman. 2014. CYP2J2 targeting to endothelial cells attenuates adiposity and vascular dysfunction in mice fed a highfat diet by reprogramming adipocyte phenotype. Hypertension 64: 1352-1361.
31. Deng, Y., M. L. Edin, K. N. Theken, R. N. Schuck, G. P. Flake, M. A. Kannon, L. M. DeGraff, F. B. Lih, J. Foley, J. A. Bradbury, et al. 2011. Endothelial CYP epoxygenase overexpression and soluble epoxide hydrolase disruption attenuate acute vascular inflammatory responses in mice. FASEB J. 25: 703-713.
32. Manhiani, M., J. E. Quigley, S. F. Knight, S. Tasoobshirazi, T. Moore, M. W. Brands, B. D. Hammock, and J. D. Imig. 2009. Soluble epoxide hydrolase gene deletion attenuates renal injury and inflammation with DOCA-salt hypertension. Am. J. Physiol. Renal Physiol. 297: F740-F748.
33. Rosen, E. D., C. H. Hsu, X. Wang, S. Sakai, M. W. Freeman, F. J. Gonzalez, and B. M. Spiegelman. 2002. C/EBPalpha induces adipogenesis through PPARgamma: a unified pathway. Genes Dev. 16: 22-26.
34. Lehrke, M., and M. A. Lazar. 2005. The many faces of PPARgamma. Cell 123: 993-999.
35. Ghosh, A. K., S. Bhattacharyya, G. Lakos, S. J. Chen, Y. Mori, and J. Varga. 2004. Disruption of transforming growth factor beta signaling and profibrotic responses in normal skin fibroblasts by peroxisome proliferator-activated receptor gamma. Arthritis Rheum. 50: 1305-1318.
36. Ghosh, A. K., S. Bhattacharyya, J. Wei, S. Kim, Y. Barak, Y. Mori, and J. Varga. 2009. Peroxisome proliferator-activated receptor-gamma abrogates Smaddependent collagen stimulation by targeting the p300 transcriptional coactivator. FASEB J. 23: 2968-2977.
37. Panigrahy, D., B. T. Kalish, S. Huang, D. R. Bielenberg, H. D. Le, J. Yang, M. L. Edin, C. R. Lee, O. Benny, D. K. Mudge, et al. 2013. Epoxyeicosanoids promote organ and tissue regeneration. Proc. Natl. Acad. Sci. USA 110: 13528-13533.
38. Leask, A., and D. J. Abraham. 2004. TGF-beta signaling and the fibrotic response. FASEB J. 18: 816-827.
39. Rennard, S. I., G. W. Hunninghake, P. B. Bitterman, and R. G. Crystal. 1981. Production of fibronectin by the human alveolar macrophage: mechanism for the recruitment of fibroblasts to sites of tissue injury in interstitial lung diseases. Proc. Natl. Acad. Sci. USA 78: 7147-7151.
40. Yamauchi, K., Y. Martinet, and R. G. Crystal. 1987. Modulation of fibronectin gene expression in human mononuclear phagocytes. J. Clin. Invest. 80: 1720-1727.
41. Schnoor, M., P. Cullen, J. Lorkowski, K. Stolle, H. Robenek, D. Troyer, J. Rauterberg, and S. Lorkowski. 2008. Production of type VI collagen by human macrophages: a new dimension in macrophage functional heterogeneity. J. Immunol. 180: 5707-5719.
42. Pollard, J. W. 2008. Macrophages define the invasive microenvironment in breast cancer. J. Leukoc. Biol. 84: 623-630.
43. Martinez, F. O., and S. Gordon. 2014. The M1 and M2 paradigm of macrophage activation: time for reassessment. F1000Prime Rep. 6: 13.
44. Meng, X. M., D. J. Nikolic-Paterson, and H. Y. Lan. 2014. Inflammatory processes in renal fibrosis. Nat. Rev. Nephrol. 10: 493-503.
45. Behmoaras, J., G. Bhangal, J. Smith, K. McDonald, B. Mutch, P. C. Lai, J. Domin, L. Game, A. Salama, B. M. Foxwell, et al. 2008. Jund is a determinant of macrophage activation and is associated with glomerulonephritis susceptibility. Nat. Genet. 40: 553-559.
46. Behmoaras, J., J. Smith, Z. D'Souza, G. Bhangal, R. Chawanasuntoropoj, F. W. Tam, C. D. Pusey, T. J. Aitman, and H. T. Cook. 2010. Genetic loci modulate macrophage activity and glomerular damage in experimental glomerulonephritis. J. Am. Soc. Nephrol. 21: 1136-1144.
47. Kang, H., A. Kerloc'h, M. Rotival, X. Xu, Q. Zhang, Z. D'Souza, M. Kim, J. C. Scholz, J. H. Ko, P. K. Srivastava, et al. 2014. Kcnn4 is a regulator of macrophage multinucleation in bone homeostasis and inflammatory disease. Cell Reports 8: 1210-1224.
48. Zhao, G., L. Tu, X. Li, S. Yang, C. Chen, X. Xu, P. Wang, and D. W. Wang. 2012. Delivery of AAV2-CYP2J2 protects remnant kidney in the 5/6-nephrectomized rat via inhibition of apoptosis and fibrosis. Hum. Gene Ther. 23: 688-699.
49. Shahabi, P., G. Siest, U. A. Meyer, and S. Visvikis-Siest. 2014. Human cytochrome P450 epoxygenases: variability in expression and role in inflammationrelated disorders. Pharmacol. Ther. 144: 134-161.
50. Schwartzman, M. L., P. Martasek, A. R. Rios, R. D. Levere, K. Solangi, A. I. Goodman, and N. G. Abraham. 1990. Cytochrome P450-dependent arachidonic acid metabolism in human kidney. Kidney Int. 37: 94-99.
51. Hull, R. P., P. K. Srivastava, Z. D'Souza, S. S. Atanur, F. Mechta-Grigoriou, L. Game, E. Petretto, H. T. Cook, T. J. Aitman, and J. Behmoaras. 2013. Combined ChIP-Seq and transcriptome analysis identifies AP-1/JunD as a primary regulator of oxidative stress and IL-1β synthesis in macrophages. BMC Genomics 14: 92.