Epigenetic control of skeletal development by the histone methyltransferase Ezh2

Journal of Biological Chemistry

Volumn 290, Issue 46, 2015, Pages 27604-27617

  Dudakovic, Amel ^a   Camilleri, Emily T ^a   Xu, Fuhua ^a   Riester, Scott M ^a   McGee Lawrence, Meghan E ^c   Bradley, Elizabeth W ^a   Paradise, Christopher R ^a   Lewallen, Eric A ^a   Thaler, Roman ^a   Deyle, David R ^a   Larson, A Noelle ^a   Lewallen, David G ^a   Dietz, Allan B ^a   Stein, Gary S ^d   Montecino, Martin A ^e   Westendorf, Jennifer J ^a,b   Van Wijnen, Andre J ^a,b  

^a MAYO CLINIC   (United States)

^b MAYO GRADUATE SCHOOL   (United States)

^c MEDICAL COLLEGE OF GEORGIA   (United States)

^d UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

^e UNIVERSIDAD ANDRÉS BELLO   (Chile)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BONE; GENE EXPRESSION; OSTEOBLASTS; POLYMETHYL METHACRYLATES; THROUGHPUT;

ADIPOGENIC DIFFERENTIATIONS; EXTRACELLULAR MATRIX PROTEIN; HISTONE METHYLTRANSFERASE; HUMAN MESENCHYMAL CELLS; OSTEOBLAST DIFFERENTIATION; OSTEOBLASTIC DIFFERENTIATION; OSTEOGENIC DIFFERENTIATION; POLYCOMB GROUP PROTEINS;

PROTEINS;

ADIPONECTIN; ALKALINE PHOSPHATASE; BONE SIALOPROTEIN; EARLY GROWTH RESPONSE FACTOR 1; FATTY ACID BINDING PROTEIN 4; OSTEOPROTEGERIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; SCLEROPROTEIN; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR EZH2; TRANSCRIPTION FACTOR MSX2; TRANSCRIPTION FACTOR RUNX2; EZH2 PROTEIN, HUMAN; HISTONE; HISTONE LYSINE METHYLTRANSFERASE; HISTONE METHYLTRANSFERASE; POLYCOMB REPRESSIVE COMPLEX 2;

ADIPOSE TISSUE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE DEVELOPMENT; BONE MASS; CELL DIFFERENTIATION; CELL FATE; CELL LINEAGE; CELL MATURATION; CLINODACTYLY; CONTROLLED STUDY; CRANIOFACIAL SYNOSTOSIS; DOWN REGULATION; ENZYME INHIBITION; EPIGENETICS; FEMALE; FORELIMB; GENE SILENCING; GENETIC REGULATION; GROWTH PLATE; HIGH THROUGHPUT SEQUENCING; HISTOPATHOLOGY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LIMB MALFORMATION; MALE; MESENCHYMAL STEM CELL; MOUSE; NONHUMAN; NORMAL HUMAN; OSSIFICATION; OSTEOBLAST; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN INDUCTION; RNA SEQUENCE; SKELETON MALFORMATION; STROMA; STROMAL VASCULAR FRACTION; TRABECULAR BONE; ABNORMALITIES; ANIMAL; ANTAGONISTS AND INHIBITORS; BONE; CELL LINE; CYTOLOGY; EMBRYOLOGY; EPIPHYSIS PLATE; GENETIC EPIGENESIS; GENETICS; MESENCHYMAL STROMA CELL; METABOLISM; MORPHOGENESIS;

ADIPOSE TISSUE; ANIMALS; BODY PATTERNING; BONE AND BONES; CELL DIFFERENTIATION; CELL LINE; ENHANCER OF ZESTE HOMOLOG 2 PROTEIN; EPIGENESIS, GENETIC; GROWTH PLATE; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; HUMANS; MESENCHYMAL STROMAL CELLS; MICE; OSTEOBLASTS; OSTEOGENESIS; POLYCOMB REPRESSIVE COMPLEX 2; RNA, SMALL INTERFERING;

EID: 84946925427     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.672345     Document Type: Article

References (68)

1. Yang, Y. (2013) Skeletal Morphogenesis and Embryonic Development. In Primer on the Metabolic Bone Diseases and Disorders of Mineral Metabolism, pp. 1-14, John Wiley & Sons, Inc.
2. Jiang, Y., and Jahagirdar, B. N., Reinhardt, R. L., Schwartz, R. E., and Keene, C. D., Ortiz-Gonzalez, X.R., Reyes, M., Lenvik, T., Lund, T., Blackstad, M., Du, J., Aldrich, S., Lisberg, A., and Low, W. C., Largaespada, D. A., and Verfaillie, C. M. (2002) Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 418, 41-49
3. Pike, J. W. (2011) Genome-scale techniques highlight the epigenome and redefine fundamental principles of gene regulation. J. Bone Miner Res. 26, 1155-1162
4. Lian, J. B., and Stein, G. S., van Wijnen, A. J., Stein, J. L., Hassan, M. Q., Gaur, T., and Zhang, Y. (2012) MicroRNA control of bone formation and homeostasis. Nat. Rev. Endocrinol. 8, 212-227
5. McGee-Lawrence, M.E., and Westendorf, J.J.(2011) Histone deacetylases in skeletal development and bone mass maintenance. Gene 474, 1-11
6. (1993) Consensus development conference: diagnosis, prophylaxis, and treatment of osteoporosis. Am. J. Med. 94, 646-650
7. Burge, R., Dawson-Hughes, B., Solomon, D. H., and Wong, J. B., King, A., and Tosteson, A. (2007) Incidence and economic burden of osteoporosis-related fractures in the United States, 2005-2025. J. Bone Miner. Res. 22, 465-475
8. Dennison, E., and Cooper, C. (2000) Epidemiology of osteoporotic fractures. Horm. Res. 54, 58-63
9. (2006) Management of osteoporosis in postmenopausal women: 2006 position statement of the North American Menopause Society. Menopause 13, 340-367; quiz 368-349
10. Ettinger, B., Black, D.M., Mitlak, B.H., Knickerbocker, R. K., Nickelsen, T., and Genant, H. K., Christiansen, C., Delmas, P. D., and Zanchetta, J. R., Stakkestad, J., Glüer, C. C., Krueger, K., Cohen, F. J., Eckert, S., and Ensrud, K. E., Avioli, L. V., Lips, P., and Cummings, S. R. (1999) Reduction of vertebral fracture risk in postmenopausal women with osteoporosis treated with raloxifene: results from a 3-year randomized clinical trial: Multiple Outcomes of Raloxifene Evaluation (MORE) Investigators. JAMA 282, 637-645
11. Silverman, S. L., Christiansen, C., Genant, H. K., Vukicevic, S., and Zanchetta, J. R., de Villiers, T. J., Constantine, G. D., and Chines, A. A. (2008) Efficacy of bazedoxifenein reducing new vertebral fracture riskin postmenopausal women with osteoporosis: results from a 3-year, randomized, placebo-, and active-controlled clinical trial. J. Bone Miner. Res. 23, 1923-1934
12. Bekker, P. J., and Holloway, D. L., Rasmussen, A. S., Murphy, R., Martin, S. W., and Leese, P. T., Holmes, G. B., Dunstan, C. R., and DePaoli, A. M. (2004) A single-dose placebo-controlled study of AMG 162, a fully human monoclonal antibodyto RANKL, inpostmenopausal women. J. Bone Miner. Res. 19, 1059-1066
13. Cummings, S. R., San Martin, J., McClung, M. R., and Siris, E. S., Eastell, R., Reid, I. R., Delmas, P., and Zoog, H. B., Austin, M., Wang, A., Kutilek, S., Adami, S., Zanchetta, J., Libanati, C., Siddhanti, S., and Christiansen, C. (2009) Denosumab for prevention of fractures in postmenopausal women with osteoporosis. N. Engl. J. Med. 361, 756-765
14. Canalis, E. (2010) Update in new anabolic therapies for osteoporosis. J. Clin. Endocrinol. Metab. 95, 1496-1504
15. Neer, R. M., and Arnaud, C. D., Zanchetta, J. R., Prince, R., Gaich, G. A., and Reginster, J. Y., Hodsman, A. B., Eriksen, E. F., Ish-Shalom, S., Genant, H. K., Wang, O., and Mitlak, B. H. (2001) Effect of parathyroid hormone (1-34) on fractures and bone mineral density in postmenopausal women with osteoporosis. N. Engl. J. Med. 344, 1434-1441
16. Reszka, A. A., and Rodan, G. A. (2004) Nitrogen-containing bisphosphonate mechanism of action. Mini Rev. Med. Chem. 4, 711-719
17. Papapoulos, S. E. (2006) Bisphosphonate actions: physical chemistry revisited. Bone 38, 613-616
18. Bellido, T., and Plotkin, L. I. (2011) Novel actions of bisphosphonates in bone: preservation of osteoblast and osteocyte viability. Bone 49, 50-55
19. Rodriguez-Merchan, E. C., and Forriol, F. (2004) Nonunion: general principles and experimental data. Clin. Orthop. Relat. Res. 4-12
20. Gibney, E. R., and Nolan, C. M. (2010) Epigenetics and gene expression. Heredity 105, 4-13
21. Zaidi, S. K., and Grandy, R. A., Lopez-Camacho, C., Montecino, M., van Wijnen, A. J., Lian, J. B., Stein, J. L., and Stein, G. S. (2014) Bookmarking target genes in mitosis: a shared epigenetic trait of phenotypic transcription factors and oncogenes? Cancer Res. 74, 420-425
22. Marchesi, I., Giordano, A., and Bagella, L. (2014) Roles of enhancer ofzeste homolog 2: from skeletal muscle differentiation to rhabdomyosarcoma carcinogenesis. Cell Cycle 13, 516-527
23. Francis, N. J., and Kingston, R. E., and Woodcock, C. L. (2004) Chromatin compaction by a polycomb group protein complex. Science 306, 1574-1577
24. O'Carroll, D., Erhardt, S., Pagani, M., Barton, S. C., and Surani, M. A., and Jenuwein, T. (2001) The polycomb-group gene Ezh2 is required for early mouse development. Mol. Cell. Biol. 21, 4330-4336
25. Ramsköld, D., and Wang, E. T., Burge, C. B., and Sandberg, R. (2009) An abundance of ubiquitously expressed genes revealed by tissue transcriptome sequence data. PLoS Comput. Biol. 5, e1000598
26. Cakouros, D., Isenmann, S., Cooper, L., Zannettino, A., Anderson, P., Glackin, C., and Gronthos, S. (2012) Twist-1 induces Ezh2 recruitment regulating histone methylation along the Ink4A/Arf locus in mesenchymal stem cells. Mol. Cell. Biol. 32, 1433-1441
27. Yang, X., and Karuturi, R. K., Sun, F., Aau, M., Yu, K., Shao, R., Miller, L. D., and Tan, P. B., and Yu, Q. (2009) CDKN1C (p57) is a direct target of EZH2 and suppressed by multiple epigenetic mechanisms in breast cancer cells. PLoS One 4, e5011
28. Rando, O. J., and Chang, H. Y. (2009) Genome-wide views of chromatin structure. Annu. Rev. Biochem. 78, 245-271
29. Laird, P. W. (2010) Principles and challenges of genomewide DNA methylation analysis. Nat. Rev. Genet. 11, 191-203
30. de Wit, E., and de Laat, W. (2012) A decade of 3C technologies: insights into nuclear organization. Genes Dev. 26, 11-24
31. Villagra, A., Gutiérrez, J., Paredes, R., Sierra, J., Puchi, M., Imschenetzky, M., Wijnen Av, A, Lian, J, Stein, G., Stein, J., and Montecino, M. (2002) Reduced CpG methylation is associated with transcriptional activation of the bone-specific rat osteocalcin gene in osteoblasts. J. Cell. Biochem. 85, 112-122
32. Lee, J. Y., and Lee, Y. M., Kim, M. J., Choi, J. Y., and Park, E. K., Kim, S. Y., Lee, S. P., and Yang, J. S., and Kim, D. S. (2006) Methylation of the mouse DIx5 and Osx gene promoters regulates cell type-specific gene expression. Mol. Cells 22, 182-188
33. Westendorf, J. J., and Zaidi, S. K., Cascino, J. E., Kahler, R., van Wijnen, A. J., Lian, J. B., Yoshida, M., Stein, G. S., and Li, X. (2002) Runx2 (Cbfa1, AML-3) interacts with histone deacetylase 6 and represses the p21(CIP1/WAF1) promoter. Mol. Cell. Biol. 22, 7982-7992
34. Schroeder, T. M., and Kahler, R. A., Li, X., and Westendorf, J. J. (2004) Histone deacetylase 3 interacts with runx2 to repress the osteocalcin promoter and regulate osteoblast differentiation. J. Biol. Chem. 279, 41998-42007
35. Kang, J. S., Alliston, T., Delston, R., and Derynck, R. (2005) Repression of Runx2 function by TGF-β through recruitment of class II histone deacety-lasesby Smad3. EMBO J. 24, 2543-2555
36. Gori, F., Divieti, P., and Demay, M. B. (2001) Cloning and characterization of a novel WD-40 repeat protein that dramatically accelerates osteoblastic differentiation. J. Biol. Chem. 276, 46515-46522
37. Gori, F., and Friedman, L. G., and Demay, M. B. (2006) Wdr5, a WD-40 protein, regulates osteoblast differentiation during embryonic bone development. Dev. Biol. 295, 498-506
38. Schroeder, T. M., and Westendorf, J. J. (2005) Histone deacetylase inhibitors promote osteoblast maturation. J. Bone Miner. Res. 20, 2254-2263
39. Di Bernardo, G., Squillaro, T., DellAversana, C., Miceli, M., Cipollaro, M., Cascino, A., Altucci, L., and Galderisi, U. (2009) Histone deacetylase inhibitors promote apoptosis and senescence in human mesenchymal stem cells. Stem Cells Dev. 18, 573-581
40. Lee, S., and Park, J. R., Seo, M. S., Roh, K. H., Park, S. B., and Hwang., J. W., Sun, B., Seo, K., Lee, Y. S., and Kang., S. K., Jung, J. W., and Kang, K. S. (2009) Histone deacetylase inhibitors decrease proliferation potential and multilineage differentiation capability of human mesenchymal stem cells. Cell Prolif. 42, 711-720
41. Dudakovic, A., and Evans, J. M., Li, Y., Middha, S., McGee-Lawrence, M. E., van Wijnen, A. J., and Westendorf, J. J. (2013) Histone deacetylase inhibition promotes osteoblast maturation by altering the histone H4 epigenome and reduces Akt phosphorylation. J. Biol. Chem. 288, 28783-28791
42. Crespo-Diaz, R., Behfar, A., and Butler, G. W., Padley, D. J., Sarr, M. G., Bartunek, J., and Dietz, A. B., and Terzic, A. (2011) Platelet lysate consisting of a natural repair proteome supports human mesenchymal stem cell proliferation and chromosomal stability. Cell Transplant. 20, 797-811
43. Mader, E. K., Butler, G., Dowdy, S. C., Mariani, A., Knutson, K. L., Federspiel, M. J., Russell, S. J., Galanis, E., Dietz, A. B., and Peng, K. W. (2013) Optimizing patient derived mesenchymal stem cells as virus carriers for a phase I clinical trial in ovarian cancer. J. Transl. Med. 11, 20
44. Su, I. H., Basavaraj, A., and Krutchinsky., A. N., Hobert, O., Ullrich, A., Chait, B. T., and Tarakhovsky, A. (2003) Ezh2 controls B cell development through histone H3 methylation and Igh rearrangement. Nat. Immunol. 4, 124-131
45. Logan, M., and Martin, J. F., Nagy, A., Lobe, C., and Olson, E. N., and Tabin, C. J. (2002) Expression of Cre recombinase in the developing mouse limb bud driven by a Prxl enhancer. Genesis 33, 77-80
46. Bouxsein, M. L., and Boyd, S. K., Christiansen, B. A., Guldberg, R. E., Jepsen, K.J., and Müller, R. (2010) Guidelines for assessment of bone microstructure in rodents using micro-computed tomography. J. Bone Miner. Res. 25, 1468-1486
47. Dudakovic, A., Camilleri, E., Riester, S. M., and Lewallen, E. A., Kvasha, S., Chen, X., Radel, D. J., and Anderson, J. M., Nair, A. A., Evans, J. M., and Krych, A. J., Smith, J., Deyle, D. R., and Stein, J. L., Stein, G. S., Im, H. J., Cool, S. M., Westendorf, J. J., Kakar, S., Dietz, A. B., and van Wijnen, A. J. (2014) High-resolution molecular validation of self-renewal and spontaneous differentiation in clinical-grade adipose-tissue derived human mesenchymal stem cells. J. Cell. Biochem. 115, 1816-1828
48. Liu, L., and Zhen, X. T., Denton, E., Marsden, B. D., and Schapira, M. (2012) ChromoHub: a data hub for navigators of chromatin-mediated signalling. Bioinformatics 28, 2205-2206
49. Dudakovic, A., and Camilleri, E. T., Lewallen, E. A., McGee-Lawrence, M. E., Riester, S. M., Kakar, S., Montecino, M., Stein, G. S., Ryoo, H. M., Dietz, A. B., Westendorf, J. J., and van Wijnen, A. J. (2015) Histone deacetylase inhibition destabilizes the multi-potent state of uncommitted adipose-derived mesenchymal stromal cells. J. Cell. Physiol. 230, 52-62
50. Margueron, R., Li, G., Sarma, K., Blais, A., Zavadil, J., Woodcock, C. L., and Dynlacht, B. D., and Reinberg, D. (2008) Ezh1 and Ezh2 maintain repressive chromatin through different mechanisms. Mol. Cell 32, 503-518
51. Cao, R., Wang, L., Wang, H., Xia, L., Erdjument-Bromage, H., Tempst, P., and Jones, R. S., and Zhang, Y. (2002) Role of histone H3 lysine 27 methylation in polycomb-group silencing. Science 298, 1039-1043
52. López-Rovira, T., Chalaux, E., Massagué, J., Rosa, J. L., and Ventura, F. (2002) Direct binding of Smad1 and Smad4 to two distinct motifs mediates bone morphogenetic protein-specific transcriptional activation of Id1 gene. J. Biol. Chem. 277, 3176-3185
53. Issa, J. P., and Kantarjian, H. M. (2009) Targeting DNA methylation. Clin. Cancer Res. 15, 3938-3946
54. Khan, O., and La Thangue, N. B. (2012) HDAC inhibitors in cancer biology: emerging mechanisms and clinical applications. Immunol. Cell Biol. 90, 85-94
55. Chuang, D. M. (2005) The antiapoptotic actions of mood stabilizers: molecular mechanisms and therapeutic potentials. Ann. N.Y. Acad. Sci. 1053, 195-204
56. Chouliaras, L., Rutten, B.P., Kenis, G., Peerbooms, O., Visser, P.J., Verhey, F., van Os, J, Steinbusch, H. W., and van den Hove, D. L. (2010) Epigenetic regulation in the pathophysiology of Alzheimer's disease. Prog. Neurobiol. 90, 498-510
57. Chiechio, S., Zammataro, M., Morales, M. E., and Busceti, C. L., Drago, F., Gereau, R. W., 4th, Copani, A., and Nicoletti, F. (2009) Epigenetic modulation of mGlu2 receptors by histone deacetylase inhibitors in the treatment of inflammatory pain. Mol. Pharmacol. 75, 1014-1020
58. Hewagama, A., and Richardson, B. (2009) The genetics and epigenetics of autoimmune diseases. J. Autoimmun. 33, 3-11
59. Wu, H., and Whitfield, T. W., Gordon, J. A., Dobson, J. R., and Tai, P. W., van Wijnen, A. J., Stein, J. L., Stein, G. S., and Lian, J. B. (2014) Genomic occupancy of Runx2 with global expression profiling identifies a novel dimension to control of osteoblastogenesis. Genome Biol. 15, R52
60. Zhu, L., and Xu, P. C. (2013) Downregulated LncRNA-ANCR promotes osteoblast differentiationbytargeting EZH2 and regulating Runx2 expression. Biochem. Biophys. Res. Commun. 432, 612-617
61. Hemming, S., Cakouros, D., Isenmann, S., Cooper, L., Menicanin, D., Zannettino, A., and Gronthos, S. (2014) EZH2 and KDM6A act as an epigenetic switch to regulate mesenchymal stem cell lineage specification. Stem Cells 32, 802-815
62. Wei, Y., and Chen, Y. H., Li, L. Y., Lang, J., Yeh, S. P., Shi, B., and Yang, C. C., Yang, J. Y., Lin, C. Y., and Lai, C. C., and Hung, M. C. (2011) CDK1-dependent phosphorylation of EZH2 suppresses methylation of H3K27 and promotes osteogenic differentiation of human mesenchymal stem cells. Nat Cell Biol. 13, 87-94
63. Hui, T., A, P., Zhao, Y., Wang, C., Gao, B., Zhang, P., Wang, J., Zhou, X., and Ye, L. (2014) EZH2, a potential regulator of dental pulp inflammation and regeneration. J. Endod. 40, 1132-1138
64. Schwarz, D., Varum, S., Zemke, M., Scholer, A., Baggiolini, A., Draganova, K., Koseki, H., Schubeler, D., and Sommer, L. (2014) Ezh2 is required for neural crest-derived cartilage and bone formation. Development 141, 867-877
65. Tatton-Brown, K., Hanks, S., Ruark, E., Zachariou, A., Duarte Sdel, V., Ramsay, E., Snape, K., Murray, A., Perdeaux, E. R., Seal, S., Loveday, C., Banka, S., Clericuzio, C., Flinter, F., Magee, A., McConnell, V., Patton, M., Raith, W., Rankin, J., Splitt, M., Strenger, V., Taylor, C., Wheeler, P., Temple, K. I., Cole, T., Childhood Overgrowth Collaboration, Douglas, J., and Rahman, N. (2011) Germline mutations in the oncogene EZH2 cause Weaver syndrome and increased human height. Oncotarget 2, 1127-1133
66. Weaver, D. D., and Graham, C. B., Thomas, I. T., and Smith, D. W. (1974) A new overgrowth syndrome with accelerated skeletal maturation, unusual facies, and camptodactyly. J. Pediatr. 84, 547-552
67. Gibson, W. T., and Hood, R. L., Zhan, S. H., Bulman, D. E., and Fejes, A. P., Moore, R., Mungall, A. J., Eydoux, P., Babul-Hirji, R., An, J., and Marra, M. A., FORGE Canada Consortium, Chitayat, D., Boycott, K. M., Weaver, D. D., and Jones, S. J. (2012) Mutations in EZH2 cause Weaver syndrome. Am. J. Hum. Genet. 90, 110-118
68. Wyngaarden, L. A., Delgado-Olguin, P., Su, I. H., and Bruneau, B. G., and Hopyan, S. (2011) Ezh2 regulates anteroposterior axis specification and proximodistal axis elongation in the developing limb. Development 138, 3759-3767