Stage-Dependent and Locus-Specific Role of Histone Demethylase Jumonji D3 (JMJD3) in the Embryonic Stages of Lung Development

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A chromosome in the eukaryotic nucleus is an organized package of DNA coiled around histone proteins. DNA contains genes and other nucleotide sequences as well as histone proteins including H1, H2A, H2B, H3, and H4. Gene expression is dynamically regulated by DNA and histone modifications, such as methylation and demethylation. The protein Jumonji domain containing-3 (Jmjd3) is a critical demethylase that regulates gene expression. Here, we found that Jmjd3 plays an important role in the regulation of mouse lung development. Global Jmjd3 deletion results in perinatal lethality that is associated with respiratory failure caused by defective lung development. Tissue and stage-specific deletion show that Jmjd3 is dispensable for mouse lung development in the later stages (after E9.5). Jmjd3 deficiency downregulates the expression of genes critical for lung development through interactions with specific transcription factors and epigenetic protein complexes. Our findings provide new insights into the role and molecular mechanism of action of Jmjd3 in embryonic lung development.

Vyšlo v časopise: Stage-Dependent and Locus-Specific Role of Histone Demethylase Jumonji D3 (JMJD3) in the Embryonic Stages of Lung Development. PLoS Genet 10(7): e32767. doi:10.1371/journal.pgen.1004524
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004524

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Zdroje

1. KloseRJ, ZhangY (2007) Regulation of histone methylation by demethylimination and demethylation. Nat Rev Mol Cell Biol 8: 307–318.

2. CloosPA, ChristensenJ, AggerK, HelinK (2008) Erasing the methyl mark: histone demethylases at the center of cellular differentiation and disease. Genes Dev 22: 1115–1140.

3. MosammaparastN, ShiY (2010) Reversal of histone methylation: biochemical and molecular mechanisms of histone demethylases. Annu Rev Biochem 79: 155–179.

4. ChiP, AllisCD, WangGG (2010) Covalent histone modifications–miswritten, misinterpreted and mis-erased in human cancers. Nat Rev Cancer 10: 457–469.

5. MargueronR, ReinbergD (2011) The Polycomb complex PRC2 and its mark in life. Nature 469: 343–349.

6. CaoR, WangL, WangH, XiaL, Erdjument-BromageH, et al. (2002) Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 298: 1039–1043.

7. AggerK, CloosPA, ChristensenJ, PasiniD, RoseS, et al. (2007) UTX and JMJD3 are histone H3K27 demethylases involved in HOX gene regulation and development. Nature 449: 731–734.

8. HongS, ChoYW, YuLR, YuH, VeenstraTD, et al. (2007) Identification of JmjC domain-containing UTX and JMJD3 as histone H3 lysine 27 demethylases. Proc Natl Acad Sci U S A 104: 18439–18444.

9. JepsenK, SolumD, ZhouT, McEvillyRJ, KimHJ, et al. (2007) SMRT-mediated repression of an H3K27 demethylase in progression from neural stem cell to neuron. Nature 450: 415–419.

10. LanF, BaylissPE, RinnJL, WhetstineJR, WangJK, et al. (2007) A histone H3 lysine 27 demethylase regulates animal posterior development. Nature 449: 689–694.

11. KouzaridesT (2007) Chromatin modifications and their function. Cell 128: 693–705.

12. BarradasM, AndertonE, AcostaJC, LiS, BanitoA, et al. (2009) Histone demethylase JMJD3 contributes to epigenetic control of INK4a/ARF by oncogenic RAS. Genes Dev 23: 1177–1182.

13. AggerK, CloosPA, RudkjaerL, WilliamsK, AndersenG, et al. (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: 1171–1176.

14. DahleO, KumarA, KuehnMR (2010) Nodal signaling recruits the histone demethylase Jmjd3 to counteract polycomb-mediated repression at target genes. Sci Signal 3: ra48.

15. SatohT, TakeuchiO, VandenbonA, YasudaK, TanakaY, et al. (2010) The Jmjd3-Irf4 axis regulates M2 macrophage polarization and host responses against helminth infection. Nat Immunol 11: 936–944.

16. PereiraF, BarbachanoA, SilvaJ, BonillaF, CampbellMJ, et al. (2011) KDM6B/JMJD3 histone demethylase is induced by vitamin D and modulates its effects in colon cancer cells. Hum Mol Genet 20: 4655–4665.

17. ZhaoW, LiQ, AyersS, GuY, ShiZ, et al. (2013) Jmjd3 inhibits reprogramming by upregulating expression of INK4a/Arf and targeting PHF20 for ubiquitination. Cell 152: 1037–1050.

18. OhtaniK, ZhaoC, DobrevaG, ManavskiY, KlugeB, et al. (2013) Jmjd3 Controls Mesodermal and Cardiovascular Differentiation of Embryonic Stem Cells. Circ Res 113: 856–862.

19. BurgoldT, VoituronN, CaganovaM, TripathiPP, MenuetC, et al. (2012) The H3K27 Demethylase JMJD3 Is Required for Maintenance of the Embryonic Respiratory Neuronal Network, Neonatal Breathing, and Survival. Cell Rep 2: 1244–1258.

20. MaedaY, DaveV, WhitsettJA (2007) Transcriptional control of lung morphogenesis. Physiol Rev 87: 219–244.

21. MendelsonCR (2000) Role of transcription factors in fetal lung development and surfactant protein gene expression. Annu Rev Physiol 62: 875–915.

22. TurgeonB, MelocheS (2009) Interpreting neonatal lethal phenotypes in mouse mutants: insights into gene function and human diseases. Physiol Rev 89: 1–26.

23. EneCI, EdwardsL, RiddickG, BaysanM, WoolardK, et al. (2012) Histone Demethylase Jumonji D3 (JMJD3) as a Tumor Suppressor by Regulating p53 Protein Nuclear Stabilization. PLoS One 7: e51407.

24. CrouchE, WrightJR (2001) Surfactant proteins a and d and pulmonary host defense. Annu Rev Physiol 63: 521–554.

25. HawgoodS, PoulainFR (2001) The pulmonary collectins and surfactant metabolism. Annu Rev Physiol 63: 495–519.

26. HamvasA, ColeFS, NogeeLM (2007) Genetic disorders of surfactant proteins. Neonatology 91: 311–317.

27. NogeeLM (2004) Alterations in SP-B and SP-C expression in neonatal lung disease. Annu Rev Physiol 66: 601–623.

28. WeaverTE, ConkrightJJ (2001) Function of surfactant proteins B and C. Annu Rev Physiol. 63: 555–578.

29. BeersMF, MulugetaS (2005) Surfactant protein C biosynthesis and its emerging role in conformational lung disease. Annu Rev Physiol 67: 663–696.

30. ClarkJC, WertSE, BachurskiCJ, StahlmanMT, StrippBR, et al. (1995) Targeted disruption of the surfactant protein B gene disrupts surfactant homeostasis, causing respiratory failure in newborn mice. Proc Natl Acad Sci U S A 92: 7794–7798.

31. MeltonKR, NessleinLL, IkegamiM, TichelaarJW, ClarkJC, et al. (2003) SP-B deficiency causes respiratory failure in adult mice. Am J Physiol Lung Cell Mol Physiol 285: L543–549.

32. De SantaF, TotaroMG, ProsperiniE, NotarbartoloS, TestaG, et al. (2007) The histone H3 lysine-27 demethylase Jmjd3 links inflammation to inhibition of polycomb-mediated gene silencing. Cell 130: 1083–1094.

33. RawlinsEL, PerlAK The a“MAZE”ing world of lung-specific transgenic mice. Am J Respir Cell Mol Biol 46: 269–282.

34. OkuboT, HoganBL (2004) Hyperactive Wnt signaling changes the developmental potential of embryonic lung endoderm. J Biol 3: 11.

35. YangL, NaltnerA, KreinerA, YanD, CowenA, et al. (2003) An enhancer region determines hSP-B gene expression in bronchiolar and ATII epithelial cells in transgenic mice. Am J Physiol Lung Cell Mol Physiol 284: L481–488.

36. WertSE, GlasserSW, KorfhagenTR, WhitsettJA (1993) Transcriptional elements from the human SP-C gene direct expression in the primordial respiratory epithelium of transgenic mice. Dev Biol 156: 426–443.

37. FreemLJ, EscotS, TannahillD, DruckenbrodNR, ThaparN, et al. (2010) The intrinsic innervation of the lung is derived from neural crest cells as shown by optical projection tomography in Wnt1-Cre;YFP reporter mice. J Anat 217: 651–664.

38. CassimanD, BarlowA, Vander BorghtS, LibbrechtL, PachnisV (2006) Hepatic stellate cells do not derive from the neural crest. J Hepatol 44: 1098–1104.

39. KempC, WillemsE, AbdoS, LambivL, LeynsL (2005) Expression of all Wnt genes and their secreted antagonists during mouse blastocyst and postimplantation development. Dev Dyn 233: 1064–1075.

40. CaoY, VoT, MillienG, TagneJB, KottonD, et al. (2010) Epigenetic mechanisms modulate thyroid transcription factor 1-mediated transcription of the surfactant protein B gene. J Biol Chem 285: 2152–2164.

41. LiuR, LiuH, ChenX, KirbyM, BrownPO, et al. (2001) Regulation of CSF1 promoter by the SWI/SNF-like BAF complex. Cell 106: 309–318.

42. MillerSA, MohnSE, WeinmannAS (2010) Jmjd3 and UTX play a demethylase-independent role in chromatin remodeling to regulate T-box family member-dependent gene expression. Mol Cell 40: 594–605.

43. ChenS, MaJ, WuF, XiongLJ, MaH, et al. (2012) The histone H3 Lys 27 demethylase JMJD3 regulates gene expression by impacting transcriptional elongation. Genes Dev 26: 1364–1375.

44. LeeS, LeeJW, LeeSK (2012) UTX, a histone H3-lysine 27 demethylase, acts as a critical switch to activate the cardiac developmental program. Dev Cell 22: 25–37.

45. OngCT, CorcesVG (2011) Enhancer function: new insights into the regulation of tissue-specific gene expression. Nat Rev Genet 12: 283–293.

46. Rada-IglesiasA, BajpaiR, SwigutT, BrugmannSA, FlynnRA, et al. (2011) A unique chromatin signature uncovers early developmental enhancers in humans. Nature 470: 279–283.

47. ChoYW, HongT, HongS, GuoH, YuH, et al. (2007) PTIP associates with MLL3- and MLL4-containing histone H3 lysine 4 methyltransferase complex. J Biol Chem 282: 20395–20406.

48. ParrBA, McMahonAP (1995) Dorsalizing signal Wnt-7a required for normal polarity of D-V and A-P axes of mouse limb. Nature 374: 350–353.

49. HayashiS, McMahonAP (2002) Efficient recombination in diverse tissues by a tamoxifen-inducible form of Cre: a tool for temporally regulated gene activation/inactivation in the mouse. Dev Biol 244: 305–318.

50. CrawfordLW, FoleyJF, ElmoreSA (2010) Histology atlas of the developing mouse hepatobiliary system with emphasis on embryonic days 9.5–18.5. Toxicol Pathol 38: 872–906.

51. LiQ, ChuMJ, XuJ (2007) Tissue- and nuclear receptor-specific function of the C-terminal LXXLL motif of coactivator NCoA6/AIB3 in mice. Mol Cell Biol 27: 8073–8086.

52. BarskiA, CuddapahS, CuiK, RohTY, SchonesDE, et al. (2007) High-resolution profiling of histone methylations in the human genome. Cell 129: 823–837.

53. QiHH, SarkissianM, HuGQ, WangZ, BhattacharjeeA, et al. (2010) Histone H4K20/H3K9 demethylase PHF8 regulates zebrafish brain and craniofacial development. Nature 466: 503–507.

54. WangL, FengZ, WangX, ZhangX (2010) DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26: 136–138.