An epigenetic switch induced by Shh signalling regulates gene activation during development and medulloblastoma growth

Nature Communications

Volumn 5, Issue , 2014, Pages

  Shi, Xuanming ^a   Zhang, Zilai ^a   Zhan, Xiaoming ^a   Cao, Mou ^a   Satoh, Takashi ^b   Akira, Shizuo ^b   Shpargel, Karl ^c   Magnuson, Terry ^c   Li, Qingtian ^d   Wang, Rongfu ^d   Wang, Chaochen ^e   Ge, Kai ^e   Wu, Jiang ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b OSAKA UNIVERSITY   (Japan)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^d HOUSTON METHODIST RESEARCH INSTITUTE   (United States)

^e NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE; METHYLTRANSFERASE; POLYCOMB REPRESSIVE COMPLEX 2; SONIC HEDGEHOG PROTEIN; GLI PROTEIN, MOUSE; HISTONE DEMETHYLASE; HISTONE LYSINE METHYLTRANSFERASE; KDM6B PROTEIN, MOUSE; KRUPPEL LIKE FACTOR; MIXED LINEAGE LEUKEMIA PROTEIN; MLL PROTEIN, MOUSE; SHH PROTEIN, MOUSE; TRANSCRIPTION FACTOR GLI1;

CANCER; CHROMOSOME; DEVELOPMENTAL BIOLOGY; DISEASE PREVALENCE; ENZYME ACTIVITY; GENE EXPRESSION; GENETIC ANALYSIS; GROWTH; PROTEIN; SIGNALING; TUMOR;

3T3 CELL LINE; ANIMAL CELL; ARTICLE; CANCER GROWTH; CELL GROWTH; CELL PROLIFERATION; CEREBELLUM; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA BINDING; EMBRYO; ENZYME ACTIVITY; EPIGENETIC SWITCH; EPIGENETICS; FIBROBLAST; GENE ACTIVATION; GENE CONTROL; GENE EXPRESSION; GENE REPRESSION; GENE TARGETING; HAIR FOLLICLE; HISTONE MODIFICATION; IN VIVO STUDY; MEDULLOBLASTOMA; MOUSE; NEURAL TUBE; NONHUMAN; PROMOTER REGION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; CELL CULTURE; FEMALE; GENETIC EPIGENESIS; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PREGNANCY;

ERINACEIDAE;

ANIMALS; CELLS, CULTURED; CEREBELLUM; EPIGENESIS, GENETIC; FEMALE; HEDGEHOG PROTEINS; HISTONE-LYSINE N-METHYLTRANSFERASE; JUMONJI DOMAIN-CONTAINING HISTONE DEMETHYLASES; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MEDULLOBLASTOMA; MICE, INBRED C57BL; MYELOID-LYMPHOID LEUKEMIA PROTEIN; POLYCOMB REPRESSIVE COMPLEX 2; PREGNANCY; ZINC FINGER PROTEIN GLI1;

EID: 84923337150     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms6425     Document Type: Article

References (70)

1. Jiang, J. & Hui, C. C. Hedgehog signaling in development and cancer. Dev. Cell 15, 801-812 (2008).
2. Fuccillo, M., Joyner, A. L. & Fishell, G. Morphogen to mitogen: the multiple roles of hedgehog signalling in vertebrate neural development. Nat. Rev. Neurosci. 7, 772-783 (2006).
3. Ingham, P. W., Nakano, Y. & Seger, C. Mechanisms and functions of Hedgehog signalling across the metazoa. Nat. Rev. Genet. 12, 393-406 (2011).
4. Barakat, M. T., Humke, E. W. & Scott, M. P. Learning from Jekyll to control Hyde: Hedgehog signaling in development and cancer. Trends Mol. Med. 16, 337-348 (2010).
5. Gilbertson, R. J. & Ellison, D. W. The origins of medulloblastoma subtypes. Annu. Rev. Pathol. 3, 341-365 (2008).
6. Oosterveen, T. et al. Mechanistic differences in the transcriptional interpretation of local and long-range shh morphogen signaling. Dev. Cell. 23, 1006-1019 (2012).
7. Peterson, K. A. et al. Neural-specific Sox2 input and differential Gli-binding affinity provide context and positional information in Shh-directed neural patterning. Genes Dev. 26, 2802-2816 (2012).
8. Corrales, J. D., Rocco, G. L., Blaess, S., Guo, Q. & Joyner, A. L. Spatial pattern of sonic hedgehog signaling through Gli genes during cerebellum development. Development 131, 5581-5590 (2004).
9. Dahmane, N. & Ruiz i Altaba, A. Sonic hedgehog regulates the growth and patterning of the cerebellum. Development 126, 3089-3100 (1999).
10. Wallace, V. A. Purkinje-cell-derived Sonic hedgehog regulates granule neuron precursor cell proliferation in the developing mouse cerebellum. Curr. Biol. 9, 445-448 (1999).
11. Wechsler-Reya, R. J. & Scott, M. P. Control of neuronal precursor proliferation in the cerebellum by Sonic Hedgehog. Neuron 22, 103-114 (1999).
12. Zhan, X., Shi, X., Zhang, Z., Chen, Y. & Wu, J. I. Dual role of Brg chromatin remodeling factor in Sonic hedgehog signaling during neural development. Proc. Natl Acad. Sci. USA 108, 12758-12763 (2011).
13. Margueron, R. & Reinberg, D. The Polycomb complex PRC2 and its mark in life. Nature 469, 343-349 (2011).
14. Bernstein, B. E. et al. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125, 315-326 (2006).
15. Mills, A. A. Throwing the cancer switch: reciprocal roles of polycomb and trithorax proteins. Nat. Rev. Cancer 10, 669-682 (2010).
16. Voigt, P., Tee, W. W. & Reinberg, D. A double take on bivalent promoters. Genes Dev. 27, 1318-1338 (2013).
17. Cao, R. et al. Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 298, 1039-1043 (2002).
18. Agger, K. et al. UTX and JMJD3 are histone H3K27 demethylases involved in HOX gene regulation and development. Nature 449, 731-734 (2007).
19. Lan, F. et al. A histone H3 lysine 27 demethylase regulates animal posterior development. Nature 449, 689-694 (2007).
20. Lee, M. G. et al. Demethylation of H3K27 regulates polycomb recruitment and H2A ubiquitination. Science 318, 447-450 (2007).
21. De Santa, F. et al. The histone H3 lysine-27 demethylase Jmjd3 links inflammation to inhibition of polycomb-mediated gene silencing. Cell 130, 1083-1094 (2007).
22. Hong, S. et al. Identification of JmjC domain-containing UTX and JMJD3 as histone H3 lysine 27 demethylases. Proc. Natl Acad. Sci. USA 104, 18439-18444 (2007).
23. Cho, Y. W. et al. PTIP associates with MLL3- and MLL4-containing histone H3 lysine 4 methyltransferase complex. J. Biol. Chem. 282, 20395-20406 (2007).
24. Burgold, T. et al. The H3K27 demethylase JMJD3 is required for maintenance of the embryonic respiratory neuronal network, neonatal breathing, and survival. Cell Rep. 2, 1244-1258 (2012).
25. Satoh, T. et al. The Jmjd3-Irf4 axis regulates M2 macrophage polarization and host responses against helminth infection. Nat. Immunol. 11, 936-944 (2010).
26. Shpargel, K. B., Sengoku, T., Yokoyama, S. & Magnuson, T. UTX and UTY demonstrate histone demethylase-independent function in mouse embryonic development. PLoS. Genet. 8, e1002964 (2012).
27. Wang, C. et al. UTX regulates mesoderm differentiation of embryonic stem cells independent of H3K27 demethylase activity. Proc. Natl Acad. Sci. USA 109, 15324-15329 (2012).
28. Bilodeau, S., Kagey, M. H., Frampton, G. M., Rahl, P. B. & Young, R. A. SetDB1 contributes to repression of genes encoding developmental regulators and maintenance of ES cell state. Genes Dev. 23, 2484-2489 (2009).
29. Taipale, J. et al. Effects of oncogenic mutations in Smoothened and Patched can be reversed by cyclopamine. Nature 406, 1005-1009 (2000).
30. Lee, E. Y. et al. Hedgehog pathway-regulated gene networks in cerebellum development and tumorigenesis. Proc. Natl Acad. Sci. USA 107, 9736-9741 (2010).
31. Vokes, S. A., Ji, H.,Wong, W. H. & McMahon, A. P. A genome-scale analysis of the cis-regulatory circuitry underlying sonic hedgehog-mediated patterning of the mammalian limb. Genes Dev. 22, 2651-2663 (2008).
32. Kallin, E. M. et al. Genome-wide uH2A localization analysis highlights Bmi1- dependent deposition of the mark at repressed genes. PLoS Genet. 5, e1000506 (2009).
33. Mikkelsen, T. S. et al. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448, 553-560 (2007).
34. Su, I. H. et al. Ezh2 controls B cell development through histone H3 methylation and Igh rearrangement. Nat. Immunol. 4, 124-131 (2003).
35. Wang, L., Jin, Q., Lee, J. E., Su, I. H. & Ge, K. Histone H3K27 methyltransferase Ezh2 represses Wnt genes to facilitate adipogenesis. Proc. Natl Acad. Sci. USA 107, 7317-7322 (2010).
36. Wyngaarden, L. A., Delgado-Olguin, P., Su, I. H., Bruneau, B. G. & Hopyan, S. Ezh2 regulates anteroposterior axis specification and proximodistal axis elongation in the developing limb. Development 138, 3759-3767 (2011).
37. Di Meglio, T. et al. Ezh2 orchestrates topographic migration and connectivity of mouse precerebellar neurons. Science 339, 204-207 (2013).
38. Pavletich, N. P. & Pabo, C. O. Crystal structure of a five-finger GLI-DNA complex: new perspectives on zinc fingers. Science 261, 1701-1707 (1993).
39. Smith, E., Lin, C. & Shilatifard, A. The super elongation complex (SEC) and MLL in development and disease. Genes Dev. 25, 661-672 (2011).
40. Ding, Q. et al. Diminished Sonic hedgehog signaling and lack of floor plate differentiation in Gli2 mutant mice. Development 125, 2533-2543 (1998).
41. Lei, Q., Zelman, A. K., Kuang, E., Li, S. & Matise, M. P. Transduction of graded Hedgehog signaling by a combination of Gli2 and Gli3 activator functions in the developing spinal cord. Development 131, 3593-3604 (2004).
42. Mill, P. et al. Sonic hedgehog-dependent activation of Gli2 is essential for embryonic hair follicle development. Genes Dev. 17, 282-294 (2003).
43. De Santa, F. et al. Jmjd3 contributes to the control of gene expression in LPS-activated macrophages. EMBO J. 28, 3341-3352 (2009).
44. Estaras, C. et al. Genome-wide analysis reveals that Smad3 and JMJD3 HDM co-activate the neural developmental program. Development 139, 2681-2691 (2012).
45. Paus, R. et al. A comprehensive guide for the recognition and classification of distinct stages of hair follicle morphogenesis. J. Invest. Dermatol. 113, 523-532 (1999).
46. Zhao, W. et al. Jmjd3 inhibits reprogramming by upregulating expression of INK4a/Arf and targeting PHF20 for ubiquitination. Cell 152, 1037-1050 (2013).
47. Parsons, D. W. et al. The genetic landscape of the childhood cancer medulloblastoma. Science 331, 435-439 (2011).
48. Mao, J. et al. A novel somatic mouse model to survey tumorigenic potential applied to the Hedgehog pathway. Cancer Res. 66, 10171-10178 (2006).
49. Berger, M. F. et al. Melanoma genome sequencing reveals frequent PREX2 mutations. Nature 485, 502-506 (2012).
50. Robinson, G. et al. Novel mutations target distinct subgroups of medulloblastoma. Nature 488, 43-48 (2012).
51. Jones, D. T. et al. Dissecting the genomic complexity underlying medulloblastoma. Nature 488, 100-105 (2012).
52. Northcott, P. A. et al. Subgroup-specific structural variation across 1,000 medulloblastoma genomes. Nature 488, 49-56 (2012).
53. Pugh, T. J. et al. Medulloblastoma exome sequencing uncovers subtype-specific somatic mutations. Nature 488, 106-110 (2012).
54. Ho, L. et al. esBAF facilitates pluripotency by conditioning the genome for LIF/ STAT3 signalling and by regulating polycomb function. Nat. Cell Biol. 13, 903-913 (2011).
55. Miller, S. A., Mohn, S. E. & Weinmann, A. S. 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 (2010).
56. Canettieri, G. et al. Histone deacetylase and Cullin3-REN(KCTD11) ubiquitin ligase interplay regulates Hedgehog signalling through Gli acetylation. Nat. Cell Biol. 12, 132-142 (2010).
57. Dai, P. et al. Sonic Hedgehog-induced activation of the Gli1 promoter is mediated by GLI3. J. Biol. Chem. 274, 8143-8152 (1999).
58. Malatesta, M. et al. Histone acetyltransferase PCAF is required for Hedgehog- Gli-dependent transcription and cancer cell proliferation. Cancer Res. 73, 6323-6333 (2013).
59. van der Vlag, J. & Otte, A. P. Transcriptional repression mediated by the human polycomb-group protein EED involves histone deacetylation. Nat. Genet. 23, 474-478 (1999).
60. Pasini, D. et al. Characterization of an antagonistic switch between histone H3 lysine 27 methylation and acetylation in the transcriptional regulation of Polycomb group target genes. Nucleic Acids Res. 38, 4958-4969 (2010).
61. Jin, Q. et al. Distinct roles of GCN5/PCAF-mediated H3K9ac and CBP/p300- mediated H3K18/27ac in nuclear receptor transactivation. EMBO J. 30, 249-262 (2011).
62. Chen, S. et al. The histone H3 Lys 27 demethylase JMJD3 regulates gene expression by impacting transcriptional elongation. Genes Dev. 26, 1364-1375 (2012).
63. Balaskas, N. et al. Gene regulatory logic for reading the Sonic Hedgehog signaling gradient in the vertebrate neural tube. Cell 148, 273-284 (2012).
64. Rallu, M. et al. Dorsoventral patterning is established in the telencephalon of mutants lacking both Gli3 and Hedgehog signaling. Development 129, 4963-4974 (2002).
65. Wijgerde, M., McMahon, J. A., Rule, M. & McMahon, A. P. A direct requirement for Hedgehog signaling for normal specification of all ventral progenitor domains in the presumptive mammalian spinal cord. Genes Dev. 16, 2849-2864 (2002).
66. Hayashi, S. & McMahon, A. P. 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 (2002).
67. Chen, J. K., Taipale, J., Young, K. E., Maiti, T. & Beachy, P. A. Small molecule modulation of Smoothened activity. Proc. Natl Acad. Sci. USA 99, 14071-14076 (2002).
68. Li, H. et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics. 25, 2078-2079 (2009).
69. Trapnell, C. et al. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 28, 511-515 (2010).
70. Sen, G. L., Webster, D. E., Barragan, D. I., Chang, H. Y. & Khavari, P. A. Control of differentiation in a self-renewing mammalian tissue by the histone demethylase JMJD3. Genes Dev. 22, 1865-1870 (2008).