Histone demethylase Jumonji D3 (JMJD3/KDM6B) at the nexus of epigenetic regulation of inflammation and the aging process
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  • 作者:Antero Salminen ; Kai Kaarniranta ; Mikko Hiltunen…
  • 关键词:Aging ; Cellular senescence ; Epigenetics ; JMJD3 ; Methylation ; NF ; κB
  • 刊名:Journal of Molecular Medicine
  • 出版年:2014
  • 出版时间:October 2014
  • 年:2014
  • 卷:92
  • 期:10
  • 页码:1035-1043
  • 全文大小:469 KB
  • 参考文献:1. Kondilis-Mangum HD, Wade PA (2013) Epigenetics and the adaptive immune response. Mol Aspects Med 34:813-25 CrossRef
    2. Stender JD, Glass CK (2013) Epigenomic control of the innate immune response. Curr Opin Pharmacol 13:582-87 CrossRef
    3. Gonzalo S (2010) Epigenetic alterations in aging. J Appl Physiol 109:586-97 CrossRef
    4. Han S, Brunet A (2012) Histone methylation makes its mark on longevity. Trends Cell Biol 22:42-9 CrossRef
    5. Natoli G (2009) Control of NF-κB-dependent transcriptional responses by chromatin organization. Cold Spring Harb Perspect Biol 1:a000224 CrossRef
    6. Johansson C, Tumber A, Che K, Cain P, Nowak R, Gileadi C, Oppermann U (2014) The roles of Jumonji-type oxygenases in human disease. Epigenomics 6:89-20 CrossRef
    7. Shpargel KB, Sengoku T, Yokoyama S, Magnuson T (2012) UTX and UTY demonstrate histone demethylase-independent function in mouse embryonic development. PLoS Genet 8:e1002964 CrossRef
    8. Welstead GG, Creyghton MP, Bilodeau S, Cheng AW, Markoulaki S, Young RA, Jaenisch R (2012) X-linked H3K27me3 demethylase Utx is required for embryonic development in a sex-specific manner. Proc Natl Acad Sci U S A 109:13004-3009 CrossRef
    9. Morales Torres C, Laugesen A, Helin K (2013) Utx is required for proper induction of ectoderm and mesoderm during differentiation of embryonic stem cells. PLoS One 8:e60020 CrossRef
    10. Estaras C, Fueyo R, Akizu N, Beltran S, Martinez-Balbas MA (2013) RNA polymerase II progression through H3K27me3-enriched gene bodies requires JMJD3 histone demethylase. Mol Biol Cell 24:351-60 CrossRef
    11. Miller SA, Mohn SE, Weinmann AS (2010) Jmjd3 and UTX play a demethylase-independent role in chromatin remodeling to regulate T-box family member-dependent gene expression. Mol Cell 40:594-05 CrossRef
    12. Agger K, Cloos PA, Christensen J, Pasini D, Rose S, Rappsilber J, Issaeva I, Canaani E, Salcini AE, Helin K (2007) UTX and JMJD3 are histone H3K27 demethylases involved in HOX gene regulation and development. Nature 449:731-34 CrossRef
    13. De Santa F, Totaro MG, Prosperini E, Notarbartolo S, Testa G, Natoli G (2007) The histone H3 lysine-27 demethylase Jmjd3 links inflammation to inhibition of polycomb-mediated gene silencing. Cell 130:1083-094 CrossRef
    14. Lan F, Peter E, Bayliss PE, Rinn JL, Whetstine JR, Wang JK, Chen S, Iwase S, Alpatov R, Issaeva I et al (2007) A histone H3 lysine 27 demethylase regulates animal posterior development. Nature 449
    15. Simon JA, Kingston RE (2013) Occupying chromatin: polycomb mechanisms for getting to genomic targets, stopping transcriptional traffic, and staying put. Mol Cell 49:808-24 CrossRef
    16. Ishii M, Wen H, Corsa CA, Liu T, Coelho AL, Allen RM, Carson WF, Cavassani KA, Li X, Lukacs NW et al (2009) Epigenetic regulation of the alternatively activated macrophage phenotype. Blood 114:3244-254 CrossRef
    17. Shan J, Fu L, Balasubramanian MN, Anthony T, Kilberg MS (2012) ATF4-dependent regulation of the JMJD3 gene during amino acid deprivation can be rescued in ATF-deficient cells by inhibition of deacetylation. J Biol Chem 287:36393-6403 CrossRef
    18. Lee HY, Choi K, Oh H, Park YK, Park H (2014) HIF-1-dependent induction of Jumonji domain-containing protein (JMJD) 3 under hypoxic conditions. Mol Cells 37:43-0 CrossRef
    19. Przanowski P, Dabrowski M, Ellert-Miklaszewska A, Kloss M, Mieczkowski J, Kaza B, Ronowicz A, Hu F, Piotrowski A, Kettenmann H et al (2014) The signal transducers Stat1 and Stat3 and their novel target Jmjd3 drive the expression of inflammatory genes in microglia. J Mol Med (Berlin) 92:239-54 CrossRef
    20. Gargalovic PS, Gharavi NM, Clark MJ, Pagnon J, Yang WP, He A, Truong A, Baruch-Oren T, Berliner JA, Kirchgessner TG et al (2006) The unfolded protein response is an important regulator of inflammatory genes in endothelial cells. Arterioscler Thromb Vasc Biol 26:2490-496 CrossRef
    21. Iwasaki Y, Suganami T, Hachiya R, Shirakawa I, Kim-Saijo M, Tanaka M, Hamaguchi M, Takai-Igarashi T, Nakai M, Miyamoto Y et al (2014) Activating transcription factor 4 links metabolic stress to interleukin-6 expression in macrophages. Diabetes 63:152-61 CrossRef
    22. Scholz CC, Taylor CT (2013) Targeting the HIF pathway in inflammation and immunity. Curr Opin Pharmacol 13:646-53 CrossRef
    23. Chen S, Ma J, Wu F, Xiong L, Ma H, Xu W, Lv R, Li X, Villen J, Gygi SP et al (2012) The histone H3 Lys 27 demethylase JMJD3 regulates gene expression by impacting transcriptional elongation. Genes Dev 26:1364-375 CrossRef
    24. De Santa F, Narang V, Yap ZH, Tusi BK, Burgold T, Austenaa L, Bucci G, Caganova M, Notarbartolo S, Casola S et al (2009) Jmjd3 contributes to the control of gene expression in LPS-activated macrophages. EMBO J 28:3341-352 CrossRef
    25. Das ND, Jung KH, Choi MR, Yoon HS, Kim SH, Chai YG (2012) Gene networking and inflammatory pathway analysis in a JMJD3 knockdown human monocytic cell line. Cell Biochem Funct 30:224-32 CrossRef
    26. Lee K, Na W, Lee JY, Na J, Cho H, Wu H, Yune TY, Kim WS, Ju BG (2012) Molecular mechanism of Jmjd3-mediated interleukin-6 gene regulation in endothelial cells underlying spinal cord injury. J Neurochem 122:272-82 CrossRef
    27. Diamant G, Dikstein R (2013) Transcriptional control by NF-κB: elongation in focus. Biochim Biophys Acta 1829:937-45 CrossRef
    28. Das A, Das ND, Jung KH, Park JH, Lee HT, Han D, Choi MR, Kang SC, Chai YG (2013) Proteomic changes induced by histone demethylase JMJD3 in TNF α-treated human monocytic (THP-1) cells. Mol Immunol 56:113-22 CrossRef
    29. Pertel T, Hausmann S, Morger D, Züger S, Guerra J, Lascano J, Reinhard C, Santoni FA, Uchil PD, Chatel L et al (2011) TRIM5 is an innate immune sensor for the retrovirus capsid lattice. Nature 472:361-65 CrossRef
    30. Ajibade AA, Wang HY, Wang RF (2013) Cell type-specific function of TAK1 in innate immune signaling. Trends Immunol 34:307-16 CrossRef
    31. Casseta L, Cassol E, Poli G (2011) Macrophage polarization in health and disease. Sci World J 11:2391-402 CrossRef
    32. Tugal D, Liao X, Jain MK (2013) Transcriptional control of macrophage polarization. Arterioscler Thromb Vasc Biol 33:1135-144 CrossRef
    33. Satoh T, Takeuchi O, Vandenbon A, Yasuda K, Tanaka Y, Kumagai Y, Miyake T, Matsushita K, Okazaki T, Saitoh T et al (2010) The Jmjd3-Irf4 axis regulates M2 macrophage polarization and host responses against helminth infection. Nat Immunol 11:936-44 CrossRef
    34. Tang Y, Li T, Li J, Yang J, Liu H, Zhang XJ, Le W (2014) Jmjd3 is essential for the epigenetic modulation of microglia phenotypes in the immune pathogenesis of Parkinson’s disease. Cell Death Differ 21:369-80 CrossRef
    35. Kauppinen A, Suuronen T, Ojala J, Kaarniranta K, Salminen A (2013) Antagonistic crosstalk between NF-κB and SIRT1 in the regulation of inflammation and metabolic disorders. Cell Signal 25:1939-948 CrossRef
    36. Pham D, Yu Q, Walline CC, Muthukrishnan R, Blum JS, Kaplan MH (2013) Opposing roles of STAT4 and Dnmt3a in Th1 gene regulation. J Immunol 191:902-11 CrossRef
    37. Yoshimura A, Wakabayashi Y, Mori T (2010) Cellular and molecular basis for the regulation of inflammation by TGF-β. J Biochem 147:781-92 CrossRef
    38. Bonniaud P, Margetts PJ, Ask K, Flanders K, Gauldie J, Kolb M (2005) TGF-β and Smad3 signaling link inflammation to chronic fibrogenesis. J Immunol 175:5390-395 CrossRef
    39. Santibanez JF, Quintanilla M, Bernabeu C (2011) TGF-β/TGF-β receptor system and its role in physiological and pathological conditions. Clin Sci (Lond) 121:233-51 CrossRef
    40. Kubiczkova L, Sedlarikova L, Hajek R, Sevcikova S (2012) TGF-β—an excellent servant but a bad master. J Transl Med 10:183 CrossRef
    41. Martinez FO, Sica A, Mantovani A, Locati M (2008) Macrophage activation and polarization. Front Biosci 13:453-61 CrossRef
    42. Yoshimura A, Muto G (2011) TGF-β function in immune suppression. Curr Top Microbiol Immunol 350:127-47
    43. Dahle O, Kumar A, Kuehn MR (2010) Nodal signaling recruits the histone demethylase Jmjd3 to counteract polycomb-mediated repression at target genes. Sci Signal 3:ra48
    44. Estaras C, Akizu N, Garcia A, Beltran S, de la Cruz X, Martinez-Balbas MA (2012) Genome-wide analysis reveals that Smad3 and JMJD3 HDM co-activates the neural development program. Development 139:2681-691 CrossRef
    45. Huang Y, Min S, Lui Y, Sun J, Su X, Liu Y, Zhang Y, Han D, Che Y, Zhao C et al (2012) Global mapping of H3K4me3 and H3K27me3 reveals chromatin state-based regulation of human monocyte-derived dendritic cells in different environments. Genes Immun 13:311-20 CrossRef
    46. Miller SA, Weinmann AS (2010) Molecular mechanisms by which T-bet regulates T-helper cell commitment. Immunol Rev 238:233-46 CrossRef
    47. Oestreich KJ, Weinmann AS (2012) Transcriptional mechanisms that regulate T helper 1 cell differentiation. Curr Opin Immunol 24:191-95 CrossRef
    48. Takashima Y, Suzuki A (2013) Regulation of organogenesis and stem cell properties by T-box transcription factors. Cell Mol Life Sci 70:3929-945 CrossRef
    49. Kartikasari AE, Zhou JX, Kanji MS, Chan DN, Sinha A, Grapin-Botton A, Magnuson MA, Lowry WE, Bhushan A (2013) The histone demethylase Jmjd3 sequentially associates with the transcription factors Tbx3 and Eomes to drive endoderm differentiation. EMBO J 32:1393-408 CrossRef
    50. Jacobs JJ, Keblusek P, Robanus-Maandag E, Kristel P, Lingbeek M, Nederlof PM, van Welsem T, van de Vijver MJ, Koh EY, Daley GQ et al (2000) Senescence bypass screen identifies TBX2, which represses Cdkn2a (p19ARF) and is amplified in a subset of human breast cancers. Nat Genet 26:291-99 CrossRef
    51. Brummelkamp TR, Kortlever RM, Lingbeek M, Trettel F, MacDonald ME, van Lohuizen M, Bernards R (2002) TBX-3, the gene mutated in Ulnar-Mammary Syndrome, is a negative regulator of p19ARF and inhibits senescence. J Biol Chem 277:6567-572 CrossRef
    52. Sidler C, Woycicki R, Ilnytskyy Y, Metz G, Kovalchuk I, Kovalchuk O (2013) Immunosenescence is associated with altered gene expression and epigenetic regulation in primary and secondary immune organs. Front Genet 4:211 CrossRef
    53. Salminen A, Kauppinen A, Kaarniranta K (2012) Emerging role of NF-κB signaling in the induction of senescence-associated secretory phenotype (SASP). Cell Signal 24:835-45 CrossRef
    54. Sahin E, DePinho RA (2012) Axis of ageing: telomeres, p53 and mitochondria. Nat Rev Mol Cell Biol 13:397-04 CrossRef
    55. Rufini A, Tucci P, Celardo I, Melino G (2013) Senescence and aging: the critical roles of p53. Oncogene 32:5129-143 CrossRef
    56. Gu B, Zhu WG (2012) Surf the post-translational modification network of p53 regulation. Int J Biol Sci 8:672-84 CrossRef
    57. Chuikov S, Kurash JK, Wilson JR, Xiao B, Justin N, Ivanov GS, McKinney K, Tempst P, Prives C, Gamblin SJ et al (2004) Regulation of p53 activity through lysine methylation. Nature 432:353-60 CrossRef
    58. West LE, Gozani O (2011) Regulation of p53 function by lysine methylation. Epigenomics 3:361-69 CrossRef
    59. Green DR, Kroemer G (2009) Cytoplasmic functions of the tumour suppressor p53. Nature 458:1127-130 CrossRef
    60. Sola S, Xavier JM, Santos DM, Aranha MM, Morgado AL, Jepsen K, Rodrigues CM (2011) p53 interaction with JMJD3 results in its nuclear distribution during mouse neural stem cell differentiation. PLoS One 6:e18421 CrossRef
    61. Zhang Y, Xiong Y, Yarbrough WG (1998) ARF promotes MDM2 degradation and stabilizes p53: ARF-INK4a locus deletion impairs both the Rb and p53 tumor suppression pathways. Cell 92:725-34 CrossRef
    62. Ene CI, Edwards L, Riddick G, Baysan M, Woolard K, Kotliarova S, Lai C, Belova G, Cam M, Walling J et al (2012) Histone demethylase Jumonji D3 (JMJD3) as a tumor suppressor by regulating p53 protein nuclear stabilization. PLoS One 7(12):e51407 CrossRef
    63. Chang BD, Watanabe K, Broude EV, Fang J, Poole JC, Kalinichenko TV, Roninson IB (2000) Effects of p21Waf1/Cip1/Sdi1 on cellular gene expression: implications for carcinogenesis, senescence, and age-related diseases. Proc Natl Acad Sci U S A 97:4291-296 CrossRef
    64. Feng Z, Hu W, Teresky AK, Hernando E, Cordon-Cardo C, Arnold J, Levine AJ (2007) Declining p53 function in the aging process: a possible mechanism for the increased tumor incidence in older populations. Proc Natl Acad Sci U S A 104:16633-6638 CrossRef
    65. Ohkusu-Tsukada K, Tsukada T, Isobe K (1999) Accelerated development and aging of the immune system in p53-deficient mice. J Immunol 163:1966-972
    66. Kim WY, Sharpless NE (2006) The regulation of INK4/ARF in cancer and aging. Cell 127:265-75 CrossRef
    67. Aguilo F, Zhou MM, Walsh MJ (2011) Long noncoding RNA, polycomb, and the ghosts haunting INK4b-ARF-INK4a expression. Cancer Res 71:5365-369 CrossRef
    68. Simboeck E, Ribeiro JD, Teichmann S, Di Croce L (2011) Epigenetics and senescence: learning from the INK4-ARF locus. Biochem Pharmacol 82:1361-370 CrossRef
    69. Yap KL, Li S, Munoz-Cabello AM, Raguz S, Zeng L, Mujtaba S, Gil J, Walsh MJ, Zhou MM (2010) Molecular interplay of the noncoding RNA ANRIL and methylated histone H3 lysine 27 by polycomb CBX7 in transcriptional silencing of INK4a. Mol Cell 38:662-74 CrossRef
    70. Kotake Y, Nakagawa T, Kitagawa K, Suzuki S, Liu N, Kitagawa M, Xiong Y (2011) Long non-coding RNA ANRIL is required for the PRC2 recruitment to and silencing of p15(INK4B) tumor suppressor gene. Oncogene 30:1956-962 CrossRef
    71. Pasmant E, Sabbagh A, Vidaud M, Bieche I (2011) ANRIL, a long, noncoding RNA, is an unexpected major hotspot in GWAS. FASEB J 25:444-48 CrossRef
    72. Bracken AP, Kleine-Kohlbrecher D, Dietrich N, Pasini D, Gargiulo G, Beekman C, Theilgaard-Monch K, Minucci S, Porse BT, Marine JC et al (2007) The Polycomb group proteins bind throughout the INK4A-ARF locus and are disassociated in senescent cells. Genes Dev 21:525-30 CrossRef
    73. Agger K, Cloos PA, Rudkjaer L, Williams K, Andersen G, Christensen J, Helin K (2009) The H3K27me3 demethylase JMJD3 contributes to the activation of the INK4A-ARF locus in response to oncogene- and stress-induced senescence. Genes Dev 23:1171-176 CrossRef
    74. Barradas M, Anderton E, Acosta JC, Li S, Banito A, Rodriguez-Niedenführ M, Maertens G, Banck M, Zhou MM, Walsh MJ et al (2009) Histone demethylase JMJD3 contributes to epigenetic control of INK4a/ARF by oncogenic RAS. Genes Dev 23:1177-182 CrossRef
    75. Agherbi H, Gaussmann-Wenger A, Verthuy C, Chasson L, Serrano M, Djabali M (2009) Polycomb mediated epigenetic silencing and replication timing at the INK4a/ARF locus during senescence. PLoS One 4:e5622 CrossRef
  • 作者单位:Antero Salminen (1)
    Kai Kaarniranta (2) (3)
    Mikko Hiltunen (1) (4)
    Anu Kauppinen (2) (3)

    1. Department of Neurology, Institute of Clinical Medicine, University of Eastern Finland, P.O. Box 1627, FIN-70211, Kuopio, Finland
    2. Department of Ophthalmology, Institute of Clinical Medicine, University of Eastern Finland, P.O. Box 1627, FIN-70211, Kuopio, Finland
    3. Department of Ophthalmology, Kuopio University Hospital, P.O. Box 100, FI-70029, Kuopio, Finland
    4. Department of Neurology, Kuopio University Hospital, P.O. Box 100, FI-70029, Kuopio, Finland
  • ISSN:1432-1440
文摘
Histone methylation is involved in the epigenetic control of immune responses and cellular senescence. Jumonji domain-containing protein 3 (JMJD3), also called lysine-specific demethylase 6B (KDM6b), is an inducible histone demethylase which enhances immune responses and can trigger cellular senescence. JMJD3 potentiates gene expression by demethylating repressive H3K27me3 epigenetic marks in promoters and gene bodies. Moreover, JMJD3 also stimulates transcription in a demethylase-independent manner by mediating interactions between chromatin modifiers. JMJD3 can enhance both pro-inflammatory and anti-inflammatory responses by targeting distinct transcription factors in a context-dependent manner in gene promoters. For instance, JMJD3 can induce macrophage M2 polarization via STAT6 signaling. JMJD3 also interacts with T-bet factor and induces Th1 differentiation of CD4+ T cells. Moreover, JMJD3 can activate TGF-β signaling through the SMAD3 pathway. Conversely, JMJD3 displaces polycomb complexes from the INK4 box, which induces the expression of INK4a and triggers cellular senescence. JMJD3 can also enhance the nuclear localization of p53 and thus regulate its function. The control of INK4 box and p53 is closely related to the regulation of the aging process. We will briefly review the inducible properties of JMJD3 expression and then focus on the role of JMJD3 in the regulation of inflammation and senescence through different signaling pathways. We emphasize that an inflammatory milieu and cellular stress can enhance immune responses and provoke cellular senescence via epigenetic regulation through JMJD3 activation.

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