Transcription factors STAT6 and KLF4 implement macrophage polarization via the dual catalytic powers of MCPIP

Journal of Immunology

Volumn 194, Issue 12, 2015, Pages 6011-6023

  Kapoor, Nidhi ^a   Niu, Jianli ^a   Saad, Yasser ^a   Kumar, Sanjay ^a   Sirakova, Tatiana ^a   Becerra, Edilu ^a   Li, Xiaoman ^a   Kolattukudy, Pappachan E ^a  

^a UNIVERSITY OF CENTRAL FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CCAAT ENHANCER BINDING PROTEIN BETA; DEUBIQUITINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; KRUPPEL LIKE FACTOR 4; LIPOPOLYSACCHARIDE; MCP 1 INDUCED PROTEIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; REACTIVE OXYGEN METABOLITE; RIBONUCLEASE; STAT6 PROTEIN; UNCLASSIFIED DRUG; INTERLEUKIN 4; KRUPPEL LIKE FACTOR; ZC3H12A PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; AUTOPHAGY; BONE MARROW CELL; CATALYSIS; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVITY; MACROPHAGE; MOUSE; NONHUMAN; PHAGOCYTOSIS; POLARIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANIMAL; BIOLOGICAL MODEL; GENE EXPRESSION; GENE INACTIVATION; GENETICS; HUMAN; IMMUNOLOGY; MACROPHAGE ACTIVATION; METABOLISM; MUTATION; RNA INTERFERENCE; TRANSGENIC MOUSE;

ANIMALS; AUTOPHAGY; CATALYSIS; CCAAT-ENHANCER-BINDING PROTEIN-BETA; ENDOPLASMIC RETICULUM STRESS; GENE EXPRESSION; GENE KNOCKOUT TECHNIQUES; HUMANS; INTERLEUKIN-4; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MACROPHAGE ACTIVATION; MACROPHAGES; MICE; MICE, TRANSGENIC; MODELS, BIOLOGICAL; MUTATION; NF-KAPPA B; PPAR GAMMA; REACTIVE OXYGEN SPECIES; RIBONUCLEASES; RNA INTERFERENCE; STAT6 TRANSCRIPTION FACTOR;

EID: 84931414766     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1402797     Document Type: Article

References (44)

1. Murray, P. J., J. E. Allen, S. K. Biswas, E. A. Fisher, D. W. Gilroy, S. Goerdt, S. Gordon, J. A. Hamilton, L. B. Ivashkiv, T. Lawrence, et al. 2014. Macrophage activation and polarization: nomenclature and experimental guidelines. Immunity 41: 14-20.
2. Epelman, S., K. J. Lavine, and G. J. Randolph. 2014. Origin and functions of tissue macrophages. Immunity 41: 21-35.
3. Odegaard, J. I., and A. Chawla. 2011. Alternative macrophage activation and metabolism. Annu. Rev. Pathol. 6: 275-297.
4. Tugal, D., X. Liao, and M. K. Jain. 2013. Transcriptional control of macrophage polarization. Arterioscler. Thromb. Vasc. Biol. 33: 1135-1144.
5. Yang, Z., and X. F. Ming. 2014. Functions of arginase isoforms in macrophage inflammatory responses: impact on cardiovascular diseases and metabolic disorders. Front. Immunol. 5: 533.
6. Gordon, S., and F. O. Martinez. 2010. Alternative activation of macrophages: mechanism and functions. Immunity 32: 593-604.
7. Zhou, D., C. Huang, Z. Lin, S. Zhan, L. Kong, C. Fang, and J. Li. 2014. Macrophage polarization and function with emphasis on the evolving roles of coordinated regulation of cellular signaling pathways. Cell. Signal. 26: 192-197.
8. De Paoli, F., B. Staels, and G. Chinetti-Gbaguidi. 2014. Macrophage phenotypes and their modulation in atherosclerosis. Circ. J. 78: 1775-1781.
9. Liao, X., N. Sharma, F. Kapadia, G. Zhou, Y. Lu, H. Hong, K. Paruchuri, G. H. Mahabeleshwar, E. Dalmas, N. Venteclef, et al. 2011. Krüppel-like factor 4 regulates macrophage polarization. J. Clin. Invest. 121: 2736-2749.
10. Zhou, L., A. Azfer, J. Niu, S. Graham, M. Choudhury, F. M. Adamski, C. Younce, P. F. Binkley, and P. E. Kolattukudy. 2006. Monocyte chemoattractant protein-1 induces a novel transcription factor that causes cardiac myocyte apoptosis and ventricular dysfunction. Circ. Res. 98: 1177-1185.
11. Liang, J., J. Wang, A. Azfer, W. Song, G. Tromp, P. E. Kolattukudy, and M. Fu. 2008. A novel CCCH-zinc finger protein family regulates proinflammatory activation of macrophages. J. Biol. Chem. 283: 6337-6346.
12. Skalniak, L., D. Mizgalska, A. Zarebski, P. Wyrzykowska, A. Koj, and J. Jura. 2009. Regulatory feedback loop between NF-kappaB and MCP-1-induced protein 1 RNase. FEBS J. 276: 5892-5905.
13. Liang, J., Y. Saad, T. Lei, J. Wang, D. Qi, Q. Yang, P. E. Kolattukudy, and M. Fu. 2010. MCP-induced protein 1 deubiquitinates TRAF proteins and negatively regulates JNK and NF-kappaB signaling. J. Exp. Med. 207: 2959-2973.
14. Matsushita, K., O. Takeuchi, D. M. Standley, Y. Kumagai, T. Kawagoe, T. Miyake, T. Satoh, H. Kato, T. Tsujimura, H. Nakamura, and S. Akira. 2009. Zc3h12a is an RNase essential for controlling immune responses by regulating mRNA decay. Nature 458: 1185-1190.
15. Mizgalska, D., P. Wegrzyn, K. Murzyn, A. Kasza, A. Koj, J. Jura, B. Jarzab, and J. Jura. 2009. Interleukin-1-inducible MCPIP protein has structural and functional properties of RNase and participates in degradation of IL-1beta mRNA. FEBS J. 276: 7386-7399.
16. Jeltsch, K. M., D. Hu, S. Brenner, J. Zöller, G. A. Heinz, D. Nagel, K. U. Vogel, N. Rehage, S. C. Warth, S. L. Edelmann, et al. 2014. Cleavage of roquin and regnase-1 by the paracaspase MALT1 releases their cooperatively repressed targets to promote T(H)17 differentiation. Nat. Immunol. 15: 1079-1089.
17. Younce, C. W., and P. E. Kolattukudy. 2010. MCP-1 causes cardiomyoblast death via autophagy resulting from ER stress caused by oxidative stress generated by inducing a novel zinc-finger protein, MCPIP. Biochem. J. 426: 43-53.
18. Wang, K., J. Niu, H. Kim, and P. E. Kolattukudy. 2011. Osteoclast precursor differentiation by MCPIP via oxidative stress, endoplasmic reticulum stress, and autophagy. J. Mol. Cell Biol. 3: 360-368.
19. Roy, A., and P. E. Kolattukudy. 2012. Monocyte chemotactic protein-induced protein (MCPIP) promotes inflammatory angiogenesis via sequential induction of oxidative stress, endoplasmic reticulum stress and autophagy. Cell. Signal. 24: 2123-2131.
20. Zhang, Y., S. Choksi, K. Chen, Y. Pobezinskaya, I. Linnoila, and Z. G. Liu. 2013. ROS play a critical role in the differentiation of alternatively activated macrophages and the occurrence of tumor-associated macrophages. Cell Res. 23: 898-914.
21. Zhang, Y., M. J. Morgan, K. Chen, S. Choksi, and Z. G. Liu. 2012. Induction of autophagy is essential for monocyte-macrophage differentiation. Blood 119: 2895-2905.
22. Oh, J., A. E. Riek, S. Weng, M. Petty, D. Kim, M. Colonna, M. Cella, and C. Bernal-Mizrachi. 2012. Endoplasmic reticulum stress controls M2 macrophage differentiation and foam cell formation. J. Biol. Chem. 287: 11629-11641.
23. Roy, A., M. Zhang, Y. Saad, and P. E. Kolattukudy. 2013. Antidicer RNase activity of monocyte chemotactic protein-induced protein-1 is critical for inducing angiogenesis. Am. J. Physiol. Cell Physiol. 305: C1021-C1032.
24. Horton, R. M., Z. Cai, S. M. Ho, and L. R. Pease. 2013. Gene splicing by overlap extension: tailor-made genes using the polymerase chain reaction. Biotechniques 54: 129-133.
25. Suzuki, H. I., M. Arase, H. Matsuyama, Y. L. Choi, T. Ueno, H. Mano, K. Sugimoto, and K. Miyazono. 2011. MCPIP1 ribonuclease antagonizes dicer and terminates microRNA biogenesis through precursor microRNA degradation. Mol. Cell 44: 424-436.
26. Charo, I. F. 2007. Macrophage polarization and insulin resistance: PPARgamma in control. Cell Metab. 6: 96-98.
27. Chawla, A. 2010. Control of macrophage activation and function by PPARs. Circ. Res. 106: 1559-1569.
28. Ruffell, D., F. Mourkioti, A. Gambardella, P. Kirstetter, R. G. Lopez, N. Rosenthal, and C. Nerlov. 2009. A CREB-C/EBPbeta cascade induces M2 macrophage-specific gene expression and promotes muscle injury repair. Proc. Natl. Acad. Sci. USA 106: 17475-17480.
29. Clausen, B. E., C. Burkhardt, W. Reith, R. Renkawitz, and I. Förster. 1999. Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic Res. 8: 265-277.
30. Kim, J. Y., E. D. Anderson, W. Huynh, A. Dey, and K. Ozato. 2011. Proteomic survey of ubiquitin-linked nuclear proteins in interferon-stimulated macrophages. J. Interferon Cytokine Res. 31: 619-628.
31. Graff, J. W., A. M. Dickson, G. Clay, A. P. McCaffrey, and M. E. Wilson. 2012. Identifying functional microRNAs in macrophages with polarized phenotypes. J. Biol. Chem. 287: 21816-21825.
32. Zhang, Y., M. Zhang, M. Zhong, Q. Suo, and K. Lv. 2013. Expression profiles of miRNAs in polarized macrophages. Int. J. Mol. Med. 31: 797-802.
33. O'Connell, R. M., K. D. Taganov, M. P. Boldin, G. Cheng, and D. Baltimore. 2007. MicroRNA-155 is induced during the macrophage inflammatory response. Proc. Natl. Acad. Sci. USA 104: 1604-1609.
34. He, M., Z. Xu, T. Ding, D. M. Kuang, and L. Zheng. 2009. MicroRNA-155 regulates inflammatory cytokine production in tumor-associated macrophages via targeting C/EBPbeta. Cell. Mol. Immunol. 6: 343-352.
35. Ye, S., H. Xu, J. Jin, M. Yang, C. Wang, Y. Yu, and X. Cao. 2012. The E3 ubiquitin ligase neuregulin receptor degradation protein 1 (Nrdp1) promotes M2 macrophage polarization by ubiquitinating and activating transcription factor CCAAT/enhancer-binding protein β (C/EBPβ). J. Biol. Chem. 287: 26740-26748.
36. Riek, A. E., J. Oh, and C. Bernal-Mizrachi. 2013. 1,25(OH)2 vitamin D suppresses macrophage migration and reverses atherogenic cholesterol metabolism in type 2 diabetic patients. J. Steroid Biochem. Mol. Biol. 136: 309-312.
37. Yang, M., J. Liu, J. Shao, Y. Qin, Q. Ji, X. Zhang, and J. Du. 2014. Cathepsin S-mediated autophagic flux in tumor-associated macrophages accelerate tumor development by promoting M2 polarization. Mol. Cancer 13: 43-57.
38. Boyce, M., K. F. Bryant, C. Jousse, K. Long, H. P. Harding, D. Scheuner, R. J. Kaufman, D. Ma, D. M. Coen, D. Ron, and J. Yuan. 2005. A selective inhibitor of eIF2alpha dephosphorylation protects cells from ER stress. Science 307: 935-939.
39. Uehata, T., and S. Akira. 2013. mRNA degradation by the endoribonuclease Regnase-1/ZC3H12a/MCPIP-1. Biochim. Biophys. Acta 1829: 708-713.
40. Lee, J. 2013. Adipose tissue macrophages in the development of obesity-induced inflammation, insulin resistance and type 2 diabetes. Arch. Pharm. Res. 36: 208-222.
41. Stöger, J. L., M. J. Gijbels, S. van der Velden, M. Manca, C. M. van der Loos, E. A. Biessen, M. J. Daemen, E. Lutgens, and M. P. de Winther. 2012. Distribution of macrophage polarization markers in human atherosclerosis. Atherosclerosis 225: 461-468.
42. Schmieder, A., J. Michel, K. Schönhaar, S. Goerdt, and K. Schledzewski. 2012. Differentiation and gene expression profile of tumor-associated macrophages. Semin. Cancer Biol. 22: 289-297.
43. Sica, A., T. Schioppa, A. Mantovani, and P. Allavena. 2006. Tumour-associated macrophages are a distinct M2 polarised population promoting tumour progression: potential targets of anti-cancer therapy. Eur. J. Cancer 42: 717-727.
44. Chambers, S. E., C. L. O'Neill, T. M. O'Doherty, R. J. Medina, and A. W. Stitt. 2013. The role of immune-related myeloid cells in angiogenesis. Immunobiology 218: 1370-1375.