Nitro-oleic acid modulates classical and regulatory activation of macrophages and their involvement in pro-fibrotic responses
Jazyk angličtina Země Spojené státy americké Médium print-electronic
Typ dokumentu časopisecké články, Research Support, N.I.H., Extramural, práce podpořená grantem
Grantová podpora
R01 HL132550
NHLBI NIH HHS - United States
P01 HL103455
NHLBI NIH HHS - United States
R37 HL058115
NHLBI NIH HHS - United States
R01 HL058115
NHLBI NIH HHS - United States
R01-HL-058115
NHLBI NIH HHS - United States
R01 HL064937
NHLBI NIH HHS - United States
R01-HL-64937
NHLBI NIH HHS - United States
P01-HL-103455
NHLBI NIH HHS - United States
PubMed
26620549
PubMed Central
PMC4748956
DOI
10.1016/j.freeradbiomed.2015.11.026
PII: S0891-5849(15)01133-8
Knihovny.cz E-zdroje
- Klíčová slova
- Fibrosis, Inflammation, Macrophage functional specialization, Macrophages, Nitro-fatty acids, Nitro-oleic acid,
- MeSH
- aktivace makrofágů účinky léků MeSH
- fibróza MeSH
- interleukin-4 farmakologie MeSH
- kultivované buňky MeSH
- kyseliny olejové farmakologie MeSH
- lipopolysacharidy farmakologie MeSH
- myokard patologie MeSH
- myši inbrední C57BL MeSH
- myši MeSH
- oxid dusnatý biosyntéza MeSH
- PPAR gama fyziologie MeSH
- superoxidy metabolismus MeSH
- transkripční faktor STAT3 fyziologie MeSH
- zvířata MeSH
- Check Tag
- myši MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Research Support, N.I.H., Extramural MeSH
- Názvy látek
- 10-nitro-oleic acid MeSH Prohlížeč
- interleukin-4 MeSH
- kyseliny olejové MeSH
- lipopolysacharidy MeSH
- oxid dusnatý MeSH
- PPAR gama MeSH
- superoxidy MeSH
- transkripční faktor STAT3 MeSH
Inflammation is an immune response triggered by microbial invasion and/or tissue injury. While acute inflammation is directed toward invading pathogens and injured cells, thus enabling tissue regeneration, chronic inflammation can lead to severe pathologies and tissue dysfunction. These processes are linked with macrophage polarization into specific inflammatory "M1-like" or regulatory "M2-like" subsets. Nitro-fatty acids (NO2-FAs), produced endogenously as byproducts of metabolism and oxidative inflammatory conditions, may be useful for treating diseases associated with dysregulated immune homeostasis. The goal of this study was to characterize the role of nitro-oleic acid (OA-NO2) in regulating the functional specialization of macrophages induced by bacterial lipopolysaccharide or interleukin-4, and to reveal specific signaling mechanisms which can account for OA-NO2-dependent modulation of inflammation and fibrotic responses. Our results show that OA-NO2 inhibits lipopolysaccharide-stimulated production of both pro-inflammatory and immunoregulatory cytokines (including transforming growth factor-β) and inhibits nitric oxide and superoxide anion production. OA-NO2 also decreases interleukin-4-induced macrophage responses by inhibiting arginase-I expression and transforming growth factor-β production. These effects are mediated via downregulation of signal transducers and activators of transcription, mitogen-activated protein kinase and nuclear factor-кB signaling responses. Finally, OA-NO2 inhibits fibrotic processes in an in vivo model of angiotensin II-induced myocardial fibrosis by attenuating expression of α-smooth muscle actin, systemic transforming growth factor-β levels and infiltration of both "M1-" and "M2-like" macrophage subsets into afflicted tissue. Overall, the electrophilic fatty acid derivative OA-NO2 modulates a broad range of "M1-" and "M2-like" macrophage functions and represents a potential therapeutic approach to target diseases associated with dysregulated macrophage subsets.
Department of Animal Physiology and Immunology Masaryk University Brno Czech Republic
Department of Pharmacology and Chemical Biology University of Pittsburgh Pittsburgh PA USA
Heart Centre University Hospital of Cologne Cologne Germany
Institute of Biophysics Academy of Sciences of the Czech Republic Brno Czech Republic
Zobrazit více v PubMed
Nahrendorf M, Swirski FK. Monocyte and macrophage heterogeneity in the heart. Circulation research. 2013;112:1624–1633. PubMed PMC
Biswas SK, Chittezhath M, Shalova IN, Lim JY. Macrophage polarization and plasticity in health and disease. Immunologic research. 2012;53:11–24. PubMed
Lawrence T, Natoli G. Transcriptional regulation of macrophage polarization: enabling diversity with identity. Nature reviews. Immunology. 2011;11:750–761. PubMed
Eguchi J, Kong X, Tenta M, Wang X, Kang S, Rosen ED. Interferon regulatory factor 4 regulates obesity-induced inflammation through regulation of adipose tissue macrophage polarization. Diabetes. 2013;62:3394–3403. PubMed PMC
Ohmori Y, Hamilton TA. Requirement for STAT1 in LPS-induced gene expression in macrophages. Journal of leukocyte biology. 2001;69:598–604. PubMed
Zhang Y, Choksi S, Chen K, Pobezinskaya Y, Linnoila I, Liu ZG. ROS play a critical role in the differentiation of alternatively activated macrophages and the occurrence of tumor-associated macrophages. Cell research. 2013;23:898–914. PubMed PMC
Hao NB, Lu MH, Fan YH, Cao YL, Zhang ZR, Yang SM. Macrophages in tumor microenvironments and the progression of tumors. Clinical & developmental immunology. 2012;2012:948098. PubMed PMC
He L, Marneros AG. Doxycycline inhibits polarization of macrophages to the proangiogenic M2-type and subsequent neovascularization. The Journal of biological chemistry. 2014;289:8019–8028. PubMed PMC
Wick G, Grundtman C, Mayerl C, Wimpissinger TF, Feichtinger J, Zelger B, Sgonc R, Wolfram D. The immunology of fibrosis. Annual review of immunology. 2013;31:107–135. PubMed
Wynn TA, Barron L. Macrophages: master regulators of inflammation and fibrosis. Seminars in liver disease. 2010;30:245–257. PubMed PMC
Murray PJ, Wynn TA. Protective and pathogenic functions of macrophage subsets. Nature reviews. Immunology. 2011;11:723–737. PubMed PMC
Ferreira AM, Ferrari MI, Trostchansky A, Batthyany C, Souza JM, Alvarez MN, Lopez GV, Baker PR, Schopfer FJ, O'Donnell V, Freeman BA, Rubbo H. Macrophage activation induces formation of the anti-inflammatory lipid cholesteryl-nitrolinoleate. The Biochemical journal. 2009;417:223–234. PubMed PMC
Klinke A, Moller A, Pekarova M, Ravekes T, Friedrichs K, Berlin M, Scheu KM, Kubala L, Kolarova H, Ambrozova G, Schermuly RT, Woodcock SR, Freeman BA, Rosenkranz S, Baldus S, Rudolph V, Rudolph TK. Protective Effects of 10-Nitro-Oleic Acid in a Hypoxia-Induced Murine Model of Pulmonary Hypertension. Am J Resp Cell Mol. 2014;51:155–162. PubMed PMC
Rudolph TK, Rudolph V, Edreira MM, Cole MP, Bonacci G, Schopfer FJ, Woodcock SR, Franek A, Pekarova M, Khoo NK, Hasty AH, Baldus S, Freeman BA. Nitro-fatty acids reduce atherosclerosis in apolipoprotein E-deficient mice. Arteriosclerosis, thrombosis, and vascular biology. 2010;30:938–945. PubMed PMC
Rudolph V, Rudolph TK, Schopfer FJ, Bonacci G, Woodcock SR, Cole MP, Baker PRS, Ramani R, Freeman BA. Endogenous generation and protective effects of nitro-fatty acids in a murine model of focal cardiac ischaemia and reperfusion. Cardiovascular research. 2010;85:155–166. PubMed PMC
Friedrichs K, Adam M, Remane L, Mollenhauer M, Rudolph V, Rudolph TK, Andrie RP, Stockigt F, Schrickel JW, Ravekes T, Deuschl F, Nickenig G, Willems S, Baldus S, Klinke A. Induction of atrial fibrillation by neutrophils critically depends on CD11b/CD18 integrins. PloS one. 2014;9:e89307. PubMed PMC
Rudolph V, Andrie RP, Rudolph TK, Friedrichs K, Klinke A, Hirsch-Hoffmann B, Schwoerer AP, Lau D, Fu X, Klingel K, Sydow K, Didie M, Seniuk A, von Leitner EC, Szoecs K, Schrickel JW, Treede H, Wenzel U, Lewalter T, Nickenig G, Zimmermann WH, Meinertz T, Boger RH, Reichenspurner H, Freeman BA, Eschenhagen T, Ehmke H, Hazen SL, Willems S, Baldus S. Myeloperoxidase acts as a profibrotic mediator of atrial fibrillation. Nature medicine. 2010;16:470–474. PubMed PMC
Covarrubias A, Byles V, Horng T. ROS sets the stage for macrophage differentiation. Cell research. 2013;23:984–985. PubMed PMC
Shi JH, Guan H, Shi S, Cai WX, Bai XZ, Hu XL, Fang XB, Liu JQ, Tao K, Zhu XX, Tang CW, Hu DH. Protection against TGF-beta1-induced fibrosis effects of IL-10 on dermal fibroblasts and its potential therapeutics for the reduction of skin scarring. Archives of dermatological research. 2013;305:341–352. PubMed
Cui T, Schopfer FJ, Zhang J, Chen K, Ichikawa T, Baker PR, Batthyany C, Chacko BK, Feng X, Patel RP, Agarwal A, Freeman BA, Chen YE. Nitrated fatty acids: Endogenous anti-inflammatory signaling mediators. The Journal of biological chemistry. 2006;281:35686–35698. PubMed PMC
Geisler AC, Rudolph TK. Nitroalkylation--a redox sensitive signaling pathway. Biochimica et biophysica acta. 2012;1820:777–784. PubMed
Salvatore SR, Vitturi DA, Baker PR, Bonacci G, Koenitzer JR, Woodcock SR, Freeman BA, Schopfer FJ. Characterization and quantification of endogenous fatty acid nitroalkene metabolites in human urine. Journal of lipid research. 2013;54:1998–2009. PubMed PMC
Tsikas D, Zoerner A, Mitschke A, Homsi Y, Gutzki FM, Jordan J. Specific GC-MS/MS stable-isotope dilution methodology for free 9- and 10-nitro-oleic acid in human plasma challenges previous LC-MS/MS reports. Journal of chromatography. B, Analytical technologies in the biomedical and life sciences. 2009;877:2895–2908. PubMed
Wang H, Liu H, Jia Z, Olsen C, Litwin S, Guan G, Yang T. Nitro-oleic acid protects against endotoxin-induced endotoxemia and multiorgan injury in mice. American journal of physiology. Renal physiology. 2010;298:F754–762. PubMed PMC
Pekarova M, Kubala L, Martiskova H, Bino L, Twarogova M, Klinke A, Rudolph TK, Kuchtova Z, Kolarova H, Ambrozova G, Kuchta R, Kadlec J, Lojek A. Asymmetric dimethylarginine regulates the lipopolysaccharide-induced nitric oxide production in macrophages by suppressing the activation of NF-kappaB and iNOS expression. Eur J Pharmacol. 2013;713:68–77. PubMed
Viackova D, Pekarova M, Crhak T, Bucsaiova M, Matiasovic J, Lojek A, Kubala L. Redox-sensitive regulation of macrophage-inducible nitric oxide synthase expression in vitro does not correlate with the failure of apocynin to prevent lung inflammation induced by endotoxin. Immunobiology. 2011;216:457–465. PubMed
Kliewer SA, Forman BM, Blumberg B, Ong ES, Borgmeyer U, Mangelsdorf DJ, Umesono K, Evans RM. Differential expression and activation of a family of murine peroxisome proliferator-activated receptors. Proceedings of the National Academy of Sciences of the United States of America. 1994;91:7355–7359. PubMed PMC
Baker PR, Schopfer FJ, O'Donnell VB, Freeman BA. Convergence of nitric oxide and lipid signaling: anti-inflammatory nitro-fatty acids. Free radical biology & medicine. 2009;46:989–1003. PubMed PMC
Freeman BA, Baker PR, Schopfer FJ, Woodcock SR, Napolitano A, d'Ischia M. Nitro-fatty acid formation and signaling. The Journal of biological chemistry. 2008;283:15515–15519. PubMed PMC
Liu H, Jia Z, Soodvilai S, Guan G, Wang MH, Dong Z, Symons JD, Yang T. Nitro-oleic acid protects the mouse kidney from ischemia and reperfusion injury. American journal of physiology. Renal physiology. 2008;295:F942–949. PubMed PMC
Coles B, Bloodsworth A, Clark SR, Lewis MJ, Cross AR, Freeman BA, O'Donnell VB. Nitrolinoleate inhibits superoxide generation, degranulation, and integrin expression by human neutrophils: novel antiinflammatory properties of nitric oxide-derived reactive species in vascular cells. Circulation research. 2002;91:375–381. PubMed
Davis MJ, Tsang TM, Qiu Y, Dayrit JK, Freij JB, Huffnagle GB, Olszewski MA. Macrophage M1/M2 polarization dynamically adapts to changes in cytokine microenvironments in Cryptococcus neoformans infection. mBio. 2013;4:e00264–00213. PubMed PMC
Fujisaka S, Usui I, Bukhari A, Ikutani M, Oya T, Kanatani Y, Tsuneyama K, Nagai Y, Takatsu K, Urakaze M, Kobayashi M, Tobe K. Regulatory mechanisms for adipose tissue M1 and M2 macrophages in diet-induced obese mice. Diabetes. 2009;58:2574–2582. PubMed PMC
Ihle JN. The Stat family in cytokine signaling. Current opinion in cell biology. 2001;13:211–217. PubMed
Ichikawa T, Zhang J, Chen K, Liu Y, Schopfer FJ, Baker PR, Freeman BA, Chen YE, Cui T. Nitroalkenes suppress lipopolysaccharide-induced signal transducer and activator of transcription signaling in macrophages: a critical role of mitogen-activated protein kinase phosphatase 1. Endocrinology. 2008;149:4086–4094. PubMed PMC
Lech M, Anders HJ. Macrophages and fibrosis: How resident and infiltrating mononuclear phagocytes orchestrate all phases of tissue injury and repair. Biochimica et biophysica acta. 2013;1832:989–997. PubMed
Odegaard JI, Chawla A. Alternative macrophage activation and metabolism. Annual review of pathology. 2011;6:275–297. PubMed PMC
Odegaard JI, Ricardo-Gonzalez RR, Red Eagle A, Vats D, Morel CR, Goforth MH, Subramanian V, Mukundan L, Ferrante AW, Chawla A. Alternative M2 activation of Kupffer cells by PPARdelta ameliorates obesity-induced insulin resistance. Cell metabolism. 2008;7:496–507. PubMed PMC
Rawlings JS, Rosler KM, Harrison DA. The JAK/STAT signaling pathway. Journal of cell science. 2004;117:1281–1283. PubMed
Szanto A, Balint BL, Nagy ZS, Barta E, Dezso B, Pap A, Szeles L, Poliska S, Oros M, Evans RM, Barak Y, Schwabe J, Nagy L. STAT6 transcription factor is a facilitator of the nuclear receptor PPARgamma-regulated gene expression in macrophages and dendritic cells. Immunity. 2010;33:699–712. PubMed PMC
Villacorta L, Schopfer FJ, Zhang J, Freeman BA, Chen YE. PPARgamma and its ligands: therapeutic implications in cardiovascular disease. Clin Sci (Lond) 2009;116:205–218. PubMed PMC
Villacorta L, Zhang J, Garcia-Barrio MT, Chen XL, Freeman BA, Chen YE, Cui T. Nitro-linoleic acid inhibits vascular smooth muscle cell proliferation via the Keap1/Nrf2 signaling pathway. American journal of physiology. Heart and circulatory physiology. 2007;293:H770–776. PubMed PMC
Wang G, Ji Y, Li Z, Han X, Guo N, Song Q, Quan L, Wang T, Han W, Pang D, Ouyang H, Tang X. Nitro-oleic acid downregulates lipoprotein-associated phospholipase A2 expression via the p42/p44 MAPK and NFkappaB pathways. Scientific reports. 2014;4:4905. PubMed PMC
Ahmed ST, Ivashkiv LB. Inhibition of IL-6 and IL-10 signaling and Stat activation by inflammatory and stress pathways. J Immunol. 2000;165:5227–5237. PubMed
Feldman N, Rotter-Maskowitz A, Okun E. DAMPs as mediators of sterile inflammation in aging-related pathologies. Ageing research reviews. 2015 PubMed
Xiao YQ, Freire-de-Lima CG, Schiemann WP, Bratton DL, Vandivier RW, Henson PM. Transcriptional and translational regulation of TGF-beta production in response to apoptotic cells. J Immunol. 2008;181:3575–3585. PubMed PMC
Kang K, Reilly SM, Karabacak V, Gangl MR, Fitzgerald K, Hatano B, Lee CH. Adipocyte-derived Th2 cytokines and myeloid PPARdelta regulate macrophage polarization and insulin sensitivity. Cell metabolism. 2008;7:485–495. PubMed PMC
Li Y, Zhang J, Schopfer FJ, Martynowski D, Garcia-Barrio MT, Kovach A, Suino-Powell K, Baker PR, Freeman BA, Chen YE, Xu HE. Molecular recognition of nitrated fatty acids by PPAR gamma. Nature structural & molecular biology. 2008;15:865–867. PubMed PMC
Schopfer FJ, Cole MP, Groeger AL, Chen CS, Khoo NKH, Woodcock SR, Golin-Bisello F, Motanya UN, Li Y, Zhang JF, Garcia-Barrio MT, Rudolph TK, Rudolph V, Bonacci G, Baker PRS, Xu HE, Batthyany CI, Chen YE, Hallis TM, Freeman BA. Covalent Peroxisome Proliferator-activated Receptor gamma Adduction by Nitro-fatty Acids SELECTIVE LIG- AND ACTIVITY AND ANTI-DIABETIC SIGNALING ACTIONS. Journal of Biological Chemistry. 2010;285:12321–12333. PubMed PMC
Reddy AT, Lakshmi SP, Reddy RC. The Nitrated Fatty Acid 10-Nitro-oleate Diminishes Severity of LPS-Induced Acute Lung Injury in Mice. PPAR research. 2012;2012:617063. PubMed PMC
Borniquel S, Jansson EA, Cole MP, Freeman BA, Lundberg JO. Nitrated oleic acid up-regulates PPARgamma and attenuates experimental inflammatory bowel disease. Free radical biology & medicine. 2010;48:499–505. PubMed PMC
Villacorta L, Chang L, Salvatore SR, Ichikawa T, Zhang J, Petrovic-Djergovic D, Jia L, Carlsen H, Schopfer FJ, Freeman BA, Chen YE. Electrophilic nitro-fatty acids inhibit vascular inflammation by disrupting LPS-dependent TLR4 signalling in lipid rafts. Cardiovascular research. 2013;98:116–124. PubMed PMC
Wang X, Liu JZ, Hu JX, Wu H, Li YL, Chen HL, Bai H, Hai CX. ROS-activated p38 MAPK/ERK-Akt cascade plays a central role in palmitic acid-stimulated hepatocyte proliferation. Free radical biology & medicine. 2011;51:539–551. PubMed
Iwata Y, Yoshizaki A, Komura K, Shimizu K, Ogawa F, Hara T, Muroi E, Bae S, Takenaka M, Yukami T, Hasegawa M, Fujimoto M, Tomita Y, Tedder TF, Sato S. CD19, a response regulator of B lymphocytes, regulates wound healing through hyaluronan-induced TLR4 signaling. The American journal of pathology. 2009;175:649–660. PubMed PMC
Sica A, Mantovani A. Macrophage plasticity and polarization: in vivo veritas. The Journal of clinical investigation. 2012;122:787–795. PubMed PMC
Seki E, De Minicis S, Osterreicher CH, Kluwe J, Osawa Y, Brenner DA, Schwabe RF. TLR4 enhances TGF-beta signaling and hepatic fibrosis. Nature medicine. 2007;13:1324–1332. PubMed
Yang M, Zheng J, Miao Y, Wang Y, Cui W, Guo J, Qiu S, Han Y, Jia L, Li H, Cheng J, Du J. Serum-glucocorticoid regulated kinase 1 regulates alternatively activated macrophage polarization contributing to angiotensin II-induced inflammation and cardiac fibrosis. Arteriosclerosis, thrombosis, and vascular biology. 2012;32:1675–1686. PubMed
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