Effects of histone demethylase JMJD3 in macrophages_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

JING Donghong ^1,2 , DENG Minghua ¹ , GONG Jianping ¹ ,  LAI Xing ¹

1. Department of Hepatobiliary Surgery, The Second Affiliated Hospital, Chongqing Medical University, Chongqing 400010, P. R. China;
2. Department of General Surgery, Chongqing Public Health Center, Chongqing 400030, P. R. China;

Corresponding author：

LAI Xing, Email: 260426944@qq.com

Keywords：

epigenetic modification; jumonji-domaincontaining protein 3; macrophage; immune reaction

DOI：

10.7507/1007-9424.201901013

Video：

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Objective To analyze effects of histone demethylase Jumonji-domaincontaining protein 3 (JMJD3) in macrophages in order to provide a new target for treatment of macrophage-related inflammatory reactions, autoimmune diseases, and organ transplantation rejection.Method The related literatures of researches on the effects of JMJD3 in the macrophages in recent years were searched and reviewed.Results The macrophages played the important roles in maintaining tissue homeostasis and host response, clearing pathogens and apoptotic cells, and promoting tissue repair and wound healing. The JMJD3 could regulate the balance of M1 and M2 types of macrophages through the different ways and had different effects on the polarization of M2 macrophages when it was stimulated by the different extracellular substances. In some immune diseases and wound repairing, the JMJD3 could not only promote the inflammatory responses, but also polarize the M2 macrophages so as to inhibit the inflammation and promote the tissue repair. Clinically, the JMJD3 expression might be different in the different diseases and its low or high expression both might be involved in the occurrence of diseases.Conclusion Histone demethylase enzyme JMJD3 is involved in macrophage polarization and expression of inflammatory genes, but there are still many problems that require further to be investigated.

Citation： JING Donghong, DENG Minghua, GONG Jianping, LAI Xing. Effects of histone demethylase JMJD3 in macrophages. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2019, 26(6): 753-757. doi: 10.7507/1007-9424.201901013 Copy

1.	Burchfield JS, Li Q, Wang HY, et al. JMJD3 as an epigenetic regulator in development and disease. Int J Biochem Cell Biol, 2015, 67: 148-157.
2.	Pan MR, Hsu MC, Chen LT, et al. Orchestration of H3K27 methylation: mechanisms and therapeutic implication. Cell Mol Life Sci, 2018, 75(2): 209-223.
3.	张恬莹, 兰涛, 魏玲玲, 等. 甲基化在肝纤维化过程中的作用及其机制的研究进展. 中国普外基础与临床杂志, 2019, 26(2): 229-235.
4.	Gu X, Xu T, He Y. A histone H3 lysine-27 methyltransferase complex represses lateral root formation in Arabidopsis thaliana. Mol Plant, 2014, 7(6): 977-988.
5.	王钰莹, 王新力, 张冉, 等. 27 位氨基酸三甲基化的组蛋白 3(H3K27me3)及其修饰酶在小鼠不同组织中分布. 细胞与分子免疫学杂志, 2017, 33(11): 1491-1497.
6.	Varol C, Mildner A, Jung S. Macrophages: development and tissue specialization. Annu Rev Immunol, 2015, 33: 643-675.
7.	Kruidenier L, Chung CW, Cheng Z, et al. A selective jumonji H3K27 demethylase inhibitor modulates the proinflammatory macrophage response. Nature, 2012, 488(7411): 404-408.
8.	Chen Z, Zang J, Whetstine J, et al. Structural insights into histone demethylation by JMJD2 family members. Cell, 2006, 125(4): 691-702.
9.	Klose RJ, Kallin EM, Zhang Y. JmjC-domain-containing proteins and histone demethylation. Nat Rev Genet, 2006, 7(9): 715-727.
10.	Sica A, Mantovani A. Macrophage plasticity and polarization: in vivo veritas. J Clin Invest, 2012, 122(3): 787-795.
11.	Shapouri-Moghaddam A, Mohammadian S, Vazini H, et al. Macrophage plasticity, polarization, and function in health and disease. J Cell Physiol, 2018, 233(9): 6425-6440.
12.	Russo L, Giller K, Pfitzner E, et al. Insight into the molecular recognition mechanism of the coactivator NCoA1 by STAT6. Sci Rep, 2017, 7(1): 16845.
13.	Sinden RE, Talman A, Marques SR, et al. The flagellum in malarial parasites. Curr Opin Microbiol, 2010, 13(4): 491-500.
14.	Liu T, Jin H, Ullenbruch M, et al. Regulation of found in inflammatory zone 1 expression in bleomycin-induced lung fibrosis: role of IL-4/IL-13 and mediation via STAT-6. J Immunol, 2004, 173(5): 3425-3431.
15.	Ishii M, Wen H, Corsa CA, et al. Epigenetic regulation of the alternatively activated macrophage phenotype. Blood, 2009, 114(15): 3244-3254.
16.	He C, Larson-Casey JL, Gu L, et al. Cu, Zn-superoxide dismutase-mediated redox regulation of Jumonji domain containing 3 modulates macrophage polarization and pulmonary fibrosis. Am J Respir Cell Mol Biol, 2016, 55(1): 58-71.
17.	Yasui T, Hirose J, Tsutsumi S, et al. Epigenetic regulation of osteoclast differentiation: possible involvement of Jmjd3 in the histone demethylation of Nfatc1. J Bone Miner Res, 2011, 26(11): 2665-2671.
18.	Meng YH, Zhou WJ, Jin LP, et al. RANKL-mediated harmonious dialogue between fetus and mother guarantees smooth gestation by inducing decidual M2 macrophage polarization. Cell Death Dis, 2017, 8(10): e3105.
19.	Kreider T, Anthony RM, Urban JF Jr, et al. Alternatively activated macrophages in helminth infections. Curr Opin Immunol, 2007, 19(4): 448-453.
20.	Satoh T, Takeuchi O, Vandenbon A, et al. The Jmjd3-Irf4 axis regulates M2 macrophage polarization and host responses against helminth infection. Nat Immunol, 2010, 11(10): 936-944.
21.	Alexaki VI, Fodelianaki G, Neuwirth A, et al. DHEA inhibits acute microglia-mediated inflammation through activation of the TrkA-Akt1/2-CREB-Jmjd3 pathway. Mol Psychiatry, 2018, 23(6): 1410-1420.
22.	Liu PS, Wang H, Li X, et al. α-ketoglutarate orchestrates macrophage activation through metabolic and epigenetic reprogramming. Nat Immunol, 2017, 18(9): 985-994.
23.	Liu R, Fan T, Geng W, et al. Negative immune regulator TIPE2 promotes M2 macrophage differentiation through the activation of PI3K-AKT signaling pathway. PLoS One, 2017, 12(1): e0170666.
24.	Zhang Y, Igwe OJ. Exogenous oxidants activate nuclear factor kappa B through Toll-like receptor 4 stimulation to maintain inflammatory phenotype in macrophage. Biochem Pharmacol, 2018, 147: 104-118.
25.	Chen X, Xiu M, Xing J, et al. Lanthanum chloride Inhibits LPS mediated expressions of pro-inflammatory cytokines and adhesion molecules in HUVECs: involvement of NF-κB-Jmjd3 signaling. Cell Physiol Biochem, 2017, 42(5): 1713-1724.
26.	De Santa F, Totaro MG, Prosperini E, et al. The histone H3 lysine-27 demethylase Jmjd3 links inflammation to inhibition of polycomb-mediated gene silencing. Cell, 2007, 130(6): 1083-1094.
27.	De Santa F, Narang V, Yap ZH, et al. Jmjd3 contributes to the control of gene expression in LPS-activated macrophages. EMBO J, 2009, 28(21): 3341-3352.
28.	Morozov VM, Li Y, Clowers MM, et al. Inhibitor of H3K27 demethylase JMJD3/UTX GSK-J4 is a potential therapeutic option for castration resistant prostate cancer. Oncotarget, 2017, 8(37): 62131-62142.
29.	Das A, Arifuzzaman S, Yoon T, et al. RNA sequencing reveals resistance of TLR4 ligand-activated microglial cells to inflammation mediated by the selective jumonji H3K27 demethylase inhibitor. Sci Rep, 2017, 7(1): 6554.
30.	Francis RC, Vaporidi K, Bloch KD, et al. Protective and detrimental effects of sodium sulfide and hydrogen sulfide in murine ventilator-induced lung injury. Anesthesiology, 2011, 115(5): 1012-1021.
31.	Liu S, Wang X, Pan L, et al. Endogenous hydrogen sulfide regulates histone demethylase JMJD3-mediated inflammatory response in LPS-stimulated macrophages and in a mouse model of LPS-induced septic shock. Biochem Pharmacol, 2018, 149: 153-162.
32.	Yan Q, Sun L, Zhu Z, et al. Jmjd3-mediated epigenetic regulation of inflammatory cytokine gene expression in serum amyloid A-stimulated macrophages. Cell Signal, 2014, 26(9): 1783-1791.
33.	Patel KM, Strong A, Tohyama J, et al. Macrophage sortilin promotes LDL uptake, foam cell formation, and atherosclerosis. Circ Res, 2015, 116(5): 789-796.
34.	Neele AE, Prange KH, Hoeksema MA, et al. Macrophage Kdm6b controls the pro-fibrotic transcriptome signature of foam cells. Epigenomics, 2017, 9(4): 383-391.
35.	Mahajan S, Dkhar HK, Chandra V, et al. Mycobacterium tuberculosis modulates macrophage lipid-sensing nuclear receptors PPARγ and TR4 for survival. J Immunol, 2012, 188(11): 5593-5603.
36.	Holla S, Prakhar P, Singh V, et al. MUSASHI-mediated expression of JMJD3, a H3K27me3 demethylase, is involved in foamy macrophage generation during mycobacterial infection. PLoS Pathog, 2016, 12(8): e1005814.
37.	Tang Y, Li T, Li J, et al. Jmjd3 is essential for the epigenetic modulation of microglia phenotypes in the immune pathogenesis of Parkinson’s disease. Cell Death Differ, 2014, 21(3): 369-380.
38.	Gallagher KA, Joshi A, Carson WF, et al. Epigenetic changes in bone marrow progenitor cells influence the inflammatory phenotype and alter wound healing in type 2 diabetes. Diabetes, 2015, 64(4): 1420-1430.
39.	骆俊民. JMJD3 在结肠癌中的表达及临床意义研究. 临床医药文献电子杂志, 2016, 3(39): 7785-7786.
40.	胡贺芳, 时辉, 车国卫, 等. 肺癌组织中含十字形结构域蛋白 3 表达的意义. 中国呼吸与危重监护杂志, 2011, 10(2): 168-170.
41.	李彦伟, 王哲. 胶质瘤细胞组蛋白去甲基化酶 JMJD3 表达降低. 细胞与分子免疫学杂志, 2014, 30(5): 525-526, 529.
42.	张庆, 丁澍, 张慧琳. 启动子区 H3K27me3 修饰异常促使系统性红斑狼疮患者 CD4⁺ T 细胞 CREMα 过表达. 南方医科大学学报, 2017, 37(12): 1597-1602.

1. Burchfield JS, Li Q, Wang HY, et al. JMJD3 as an epigenetic regulator in development and disease. Int J Biochem Cell Biol, 2015, 67: 148-157.
2. Pan MR, Hsu MC, Chen LT, et al. Orchestration of H3K27 methylation: mechanisms and therapeutic implication. Cell Mol Life Sci, 2018, 75(2): 209-223.
3. 张恬莹, 兰涛, 魏玲玲, 等. 甲基化在肝纤维化过程中的作用及其机制的研究进展. 中国普外基础与临床杂志, 2019, 26(2): 229-235.
4. Gu X, Xu T, He Y. A histone H3 lysine-27 methyltransferase complex represses lateral root formation in Arabidopsis thaliana. Mol Plant, 2014, 7(6): 977-988.
5. 王钰莹, 王新力, 张冉, 等. 27 位氨基酸三甲基化的组蛋白 3(H3K27me3)及其修饰酶在小鼠不同组织中分布. 细胞与分子免疫学杂志, 2017, 33(11): 1491-1497.
6. Varol C, Mildner A, Jung S. Macrophages: development and tissue specialization. Annu Rev Immunol, 2015, 33: 643-675.
7. Kruidenier L, Chung CW, Cheng Z, et al. A selective jumonji H3K27 demethylase inhibitor modulates the proinflammatory macrophage response. Nature, 2012, 488(7411): 404-408.
8. Chen Z, Zang J, Whetstine J, et al. Structural insights into histone demethylation by JMJD2 family members. Cell, 2006, 125(4): 691-702.
9. Klose RJ, Kallin EM, Zhang Y. JmjC-domain-containing proteins and histone demethylation. Nat Rev Genet, 2006, 7(9): 715-727.
10. Sica A, Mantovani A. Macrophage plasticity and polarization: in vivo veritas. J Clin Invest, 2012, 122(3): 787-795.
11. Shapouri-Moghaddam A, Mohammadian S, Vazini H, et al. Macrophage plasticity, polarization, and function in health and disease. J Cell Physiol, 2018, 233(9): 6425-6440.
12. Russo L, Giller K, Pfitzner E, et al. Insight into the molecular recognition mechanism of the coactivator NCoA1 by STAT6. Sci Rep, 2017, 7(1): 16845.
13. Sinden RE, Talman A, Marques SR, et al. The flagellum in malarial parasites. Curr Opin Microbiol, 2010, 13(4): 491-500.
14. Liu T, Jin H, Ullenbruch M, et al. Regulation of found in inflammatory zone 1 expression in bleomycin-induced lung fibrosis: role of IL-4/IL-13 and mediation via STAT-6. J Immunol, 2004, 173(5): 3425-3431.
15. Ishii M, Wen H, Corsa CA, et al. Epigenetic regulation of the alternatively activated macrophage phenotype. Blood, 2009, 114(15): 3244-3254.
16. He C, Larson-Casey JL, Gu L, et al. Cu, Zn-superoxide dismutase-mediated redox regulation of Jumonji domain containing 3 modulates macrophage polarization and pulmonary fibrosis. Am J Respir Cell Mol Biol, 2016, 55(1): 58-71.
17. Yasui T, Hirose J, Tsutsumi S, et al. Epigenetic regulation of osteoclast differentiation: possible involvement of Jmjd3 in the histone demethylation of Nfatc1. J Bone Miner Res, 2011, 26(11): 2665-2671.
18. Meng YH, Zhou WJ, Jin LP, et al. RANKL-mediated harmonious dialogue between fetus and mother guarantees smooth gestation by inducing decidual M2 macrophage polarization. Cell Death Dis, 2017, 8(10): e3105.
19. Kreider T, Anthony RM, Urban JF Jr, et al. Alternatively activated macrophages in helminth infections. Curr Opin Immunol, 2007, 19(4): 448-453.
20. Satoh T, Takeuchi O, Vandenbon A, et al. The Jmjd3-Irf4 axis regulates M2 macrophage polarization and host responses against helminth infection. Nat Immunol, 2010, 11(10): 936-944.
21. Alexaki VI, Fodelianaki G, Neuwirth A, et al. DHEA inhibits acute microglia-mediated inflammation through activation of the TrkA-Akt1/2-CREB-Jmjd3 pathway. Mol Psychiatry, 2018, 23(6): 1410-1420.
22. Liu PS, Wang H, Li X, et al. α-ketoglutarate orchestrates macrophage activation through metabolic and epigenetic reprogramming. Nat Immunol, 2017, 18(9): 985-994.
23. Liu R, Fan T, Geng W, et al. Negative immune regulator TIPE2 promotes M2 macrophage differentiation through the activation of PI3K-AKT signaling pathway. PLoS One, 2017, 12(1): e0170666.
24. Zhang Y, Igwe OJ. Exogenous oxidants activate nuclear factor kappa B through Toll-like receptor 4 stimulation to maintain inflammatory phenotype in macrophage. Biochem Pharmacol, 2018, 147: 104-118.
25. Chen X, Xiu M, Xing J, et al. Lanthanum chloride Inhibits LPS mediated expressions of pro-inflammatory cytokines and adhesion molecules in HUVECs: involvement of NF-κB-Jmjd3 signaling. Cell Physiol Biochem, 2017, 42(5): 1713-1724.
26. De Santa F, Totaro MG, Prosperini E, et al. The histone H3 lysine-27 demethylase Jmjd3 links inflammation to inhibition of polycomb-mediated gene silencing. Cell, 2007, 130(6): 1083-1094.
27. De Santa F, Narang V, Yap ZH, et al. Jmjd3 contributes to the control of gene expression in LPS-activated macrophages. EMBO J, 2009, 28(21): 3341-3352.
28. Morozov VM, Li Y, Clowers MM, et al. Inhibitor of H3K27 demethylase JMJD3/UTX GSK-J4 is a potential therapeutic option for castration resistant prostate cancer. Oncotarget, 2017, 8(37): 62131-62142.
29. Das A, Arifuzzaman S, Yoon T, et al. RNA sequencing reveals resistance of TLR4 ligand-activated microglial cells to inflammation mediated by the selective jumonji H3K27 demethylase inhibitor. Sci Rep, 2017, 7(1): 6554.
30. Francis RC, Vaporidi K, Bloch KD, et al. Protective and detrimental effects of sodium sulfide and hydrogen sulfide in murine ventilator-induced lung injury. Anesthesiology, 2011, 115(5): 1012-1021.
31. Liu S, Wang X, Pan L, et al. Endogenous hydrogen sulfide regulates histone demethylase JMJD3-mediated inflammatory response in LPS-stimulated macrophages and in a mouse model of LPS-induced septic shock. Biochem Pharmacol, 2018, 149: 153-162.
32. Yan Q, Sun L, Zhu Z, et al. Jmjd3-mediated epigenetic regulation of inflammatory cytokine gene expression in serum amyloid A-stimulated macrophages. Cell Signal, 2014, 26(9): 1783-1791.
33. Patel KM, Strong A, Tohyama J, et al. Macrophage sortilin promotes LDL uptake, foam cell formation, and atherosclerosis. Circ Res, 2015, 116(5): 789-796.
34. Neele AE, Prange KH, Hoeksema MA, et al. Macrophage Kdm6b controls the pro-fibrotic transcriptome signature of foam cells. Epigenomics, 2017, 9(4): 383-391.
35. Mahajan S, Dkhar HK, Chandra V, et al. Mycobacterium tuberculosis modulates macrophage lipid-sensing nuclear receptors PPARγ and TR4 for survival. J Immunol, 2012, 188(11): 5593-5603.
36. Holla S, Prakhar P, Singh V, et al. MUSASHI-mediated expression of JMJD3, a H3K27me3 demethylase, is involved in foamy macrophage generation during mycobacterial infection. PLoS Pathog, 2016, 12(8): e1005814.
37. Tang Y, Li T, Li J, et al. Jmjd3 is essential for the epigenetic modulation of microglia phenotypes in the immune pathogenesis of Parkinson’s disease. Cell Death Differ, 2014, 21(3): 369-380.
38. Gallagher KA, Joshi A, Carson WF, et al. Epigenetic changes in bone marrow progenitor cells influence the inflammatory phenotype and alter wound healing in type 2 diabetes. Diabetes, 2015, 64(4): 1420-1430.
39. 骆俊民. JMJD3 在结肠癌中的表达及临床意义研究. 临床医药文献电子杂志, 2016, 3(39): 7785-7786.
40. 胡贺芳, 时辉, 车国卫, 等. 肺癌组织中含十字形结构域蛋白 3 表达的意义. 中国呼吸与危重监护杂志, 2011, 10(2): 168-170.
41. 李彦伟, 王哲. 胶质瘤细胞组蛋白去甲基化酶 JMJD3 表达降低. 细胞与分子免疫学杂志, 2014, 30(5): 525-526, 529.
42. 张庆, 丁澍, 张慧琳. 启动子区 H3K27me3 修饰异常促使系统性红斑狼疮患者 CD4⁺ T 细胞 CREMα 过表达. 南方医科大学学报, 2017, 37(12): 1597-1602.

CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Effects of histone demethylase JMJD3 in macrophages

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