Genome-wide map of quantified epigenetic changes during in vitro chondrogenic differentiation of primary human mesenchymal stem cells

BMC Genomics

Volumn 14, Issue 1, 2013, Pages

  Herlofsen, Sarah R ^a   Bryne, Jan Christian ^a   Høiby, Torill ^a   Wang, Li ^b   Issner, Robbyn ^b   Zhang, Xiaolan ^b   Coyne, Michael J ^b   Boyle, Patrick ^b   Gu, Hongcang ^b   Meza Zepeda, Leonardo A ^a   Collas, Philippe ^c   Mikkelsen, Tarjei S ^b,d   Brinchmann, Jan E ^a,c  

^a OSLO UNIVERSITY HOSPITAL   (Norway)

^b BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^c UNIVERSITY OF OSLO   (Norway)

^d Harvard University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H3; MESSENGER RNA;

ARTICLE; BINDING SITE; CELL DIFFERENTIATION; CELL LINEAGE; CHONDROGENESIS; CHONDROGENIC DIFFERENTIATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA METHYLATION; EPIGENETICS; GENE EXPRESSION; GENE MAPPING; HISTONE H3 GENE; HISTONE MODIFICATION; HUMAN; HUMAN CELL; IN VITRO STUDY; MESENCHYMAL STEM CELL; MICROARRAY ANALYSIS; PROMOTER REGION; QUANTITATIVE ANALYSIS; REGULATORY SEQUENCE; SEQUENCE ANALYSIS; TRANSCRIPTION INITIATION SITE;

CELL DIFFERENTIATION; CELL LINEAGE; CELLS, CULTURED; CHONDROGENESIS; DNA METHYLATION; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION; GENOME, HUMAN; HISTONES; HUMANS; MESENCHYMAL STROMAL CELLS; PROMOTER REGIONS, GENETIC; REGULATORY ELEMENTS, TRANSCRIPTIONAL; TRANSCRIPTION INITIATION SITE;

EID: 84873732990     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-14-105     Document Type: Article

References (52)

1. Ahmed TA, Hincke MT. Strategies for articular cartilage lesion repair and functional restoration. Tissue Eng 2010, 16(3):305-329.
2. Vinatier C, Bouffi C, Merceron C, Gordeladze J, Brondello JM, Jorgensen C, Weiss P, Guicheux J, Noel D. Cartilage tissue engineering: towards a biomaterial-assisted mesenchymal stem cell therapy. Curr Stem Cell Res Ther 2009, 4(4):318-329. 10.2174/157488809789649205, 3218613, 19804369.
3. Bernstein BE, Kamal M, Lindblad-Toh K, Bekiranov S, Bailey DK, Huebert DJ, McMahon S, Karlsson EK, Kulbokas EJ, Gingeras TR, Schreiber SL, Lander ES. Genomic maps and comparative analysis of histone modifications in human and mouse. Cell 2005, 120(2):169-181. 10.1016/j.cell.2005.01.001, 15680324.
4. Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, Giannoukos G, Alvarez P, Brockman W, Kim TK, Koche RP, Lee W, Mendenhall E, O'Donovan A, Presser A, Russ C, Xie X, Meissner A, Wernig M, Jaenisch R, Nusbaum C, Lander ES, Bernstein BE. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 2007, 448(7153):553-560. 10.1038/nature06008, 2921165, 17603471.
5. Hawkins RD, Hon GC, Lee LK, Ngo Q, Lister R, Pelizzola M, Edsall LE, Kuan S, Luu Y, Klugman S, Antosiewicz-Bourget J, Ye Z, Espinoza C, Agarwahl S, Shen L, Ruotti V, Wang W, Stewart R, Thomson JA, Ecker JR, Ren B. Distinct epigenomic landscapes of pluripotent and lineage-committed human cells. Cell Stem Cell 2010, 6(5):479-491. 10.1016/j.stem.2010.03.018, 2867844, 20452322.
6. Challen GA, Sun D, Jeong M, Luo M, Jelinek J, Berg JS, Bock C, Vasanthakumar A, Gu H, Xi Y, Liang S, Lu Y, Darlington GJ, Meissner A, Issa JP, Godley LA, Li W, Goodell MA. Dnmt3a is essential for hematopoietic stem cell differentiation. Nat Genet 2011, 44(1):23-31. 10.1038/ng.1009, 22138693.
7. Guenther MG, Levine SS, Boyer LA, Jaenisch R, Young RA. A chromatin landmark and transcription initiation at most promoters in human cells. Cell 2007, 130(1):77-88. 10.1016/j.cell.2007.05.042, 3200295, 17632057.
8. Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J, Fry B, Meissner A, Wernig M, Plath K, Jaenisch R, Wagschal A, Feil R, Schreiber SL, Lander ES. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 2006, 125(2):315-326. 10.1016/j.cell.2006.02.041, 16630819.
9. Suganuma T, Workman JL. Signals and combinatorial functions of histone modifications. Annu Rev Biochem 2011, 80:473-499. 10.1146/annurev-biochem-061809-175347, 21529160.
10. Mikkelsen TS, Xu Z, Zhang X, Wang L, Gimble JM, Lander ES, Rosen ED. Comparative epigenomic analysis of murine and human adipogenesis. Cell 2010, 143(1):156-169. 10.1016/j.cell.2010.09.006, 2950833, 20887899.
11. Sorensen AL, Jacobsen BM, Reiner AH, Andersen IS, Collas P. Promoter DNA methylation patterns of differentiated cells are largely programmed at the progenitor stage. Mol Biol Cell 2010, 21(12):2066-2077. 10.1091/mbc.E10-01-0018, 2883950, 20410135.
12. Asp P, Blum R, Vethantham V, Parisi F, Micsinai M, Cheng J, Bowman C, Kluger Y, Dynlacht BD. Genome-wide remodeling of the epigenetic landscape during myogenic differentiation. Proc Natl Acad Sci USA 2011, 108(22):E149-158. 10.1073/pnas.1102223108, 3107312, 21551099.
13. Lien WH, Guo X, Polak L, Lawton LN, Young RA, Zheng D, Fuchs E. Genome-wide maps of histone modifications unwind in vivo chromatin states of the hair follicle lineage. Cell Stem Cell 2011, 9(3):219-232. 10.1016/j.stem.2011.07.015, 3166618, 21885018.
14. Cedar H, Bergman Y. Epigenetics of haematopoietic cell development. Nat Rev Immunol 2011, 11(7):478-488. 10.1038/nri2991, 21660052.
15. Cui K, Zang C, Roh TY, Schones DE, Childs RW, Peng W, Zhao K. Chromatin signatures in multipotent human hematopoietic stem cells indicate the fate of bivalent genes during differentiation. Cell Stem Cell 2009, 4(1):80-93. 10.1016/j.stem.2008.11.011, 2785912, 19128795.
16. Hodges E, Molaro A, Dos Santos CO, Thekkat P, Song Q, Uren PJ, Park J, Butler J, Rafii S, McCombie WR, Smith AD, Hannon GJ. Directional DNA methylation changes and complex intermediate states accompany lineage specificity in the adult hematopoietic compartment. Mol Cell 2011, 44(1):17-28. 10.1016/j.molcel.2011.08.026, 3412369, 21924933.
17. Ezura Y, Sekiya I, Koga H, Muneta T, Noda M. Methylation status of CpG islands in the promoter regions of signature genes during chondrogenesis of human synovium-derived mesenchymal stem cells. Arthritis Rheum 2009, 60(5):1416-1426. 10.1002/art.24472, 19404940.
18. Furumatsu T, Asahara H. Histone acetylation influences the activity of Sox9-related transcriptional complex. Acta Med Okayama 2011, 64(6):351-357.
19. Zimmermann P, Boeuf S, Dickhut A, Boehmer S, Olek S, Richter W. Correlation of COL10A1 induction during chondrogenesis of mesenchymal stem cells with demethylation of two CpG sites in the COL10A1 promoter. Arthritis Rheum 2008, 58(9):2743-2753. 10.1002/art.23736, 18759285.
20. Goldring MB, Tsuchimochi K, Ijiri K. The control of chondrogenesis. J Cell Biochem 2006, 97(1):33-44. 10.1002/jcb.20652, 16215986.
21. Ichinose S, Yamagata K, Sekiya I, Muneta T, Tagami M. Detailed examination of cartilage formation and endochondral ossification using human mesenchymal stem cells. Clin Exp Pharmacol Physiol 2005, 32(7):561-570. 10.1111/j.1440-1681.2005.04231.x, 16026516.
22. Lefebvre V, Smits P. Transcriptional control of chondrocyte fate and differentiation. Birth Defects Res C Embryo Today 2005, 75(3):200-212. 10.1002/bdrc.20048, 16187326.
23. Lefebvre V, Behringer RR, de Crombrugghe B. L-Sox5, Sox6 and Sox9 control essential steps of the chondrocyte differentiation pathway. Osteoarthritis and cartilage / OARS, Osteoarthritis Research Society 2001, 9(Suppl A):S69-75.
24. Smits P, Li P, Mandel J, Zhang Z, Deng JM, Behringer RR, de Crombrugghe B, Lefebvre V. The transcription factors L-Sox5 and Sox6 are essential for cartilage formation. Dev Cell 2001, 1(2):277-290. 10.1016/S1534-5807(01)00003-X, 11702786.
25. Ikeda T, Zhang J, Chano T, Mabuchi A, Fukuda A, Kawaguchi H, Nakamura K, Ikegawa S. Identification and characterization of the human long form of Sox5 (L-SOX5) gene. Gene 2002, 298(1):59-68. 10.1016/S0378-1119(02)00927-7, 12406576.
26. Herlofsen SR, Kuchler AM, Melvik JE, Brinchmann JE. Chondrogenic differentiation of human bone marrow-derived mesenchymal stem cells in self-gelling alginate discs reveals novel chondrogenic signature gene clusters. Tissue Eng Part A 2011, 17(7-8):1003-1013. 3063696, 21087199.
27. Heintzman ND, Hon GC, Hawkins RD, Kheradpour P, Stark A, Harp LF, Ye Z, Lee LK, Stuart RK, Ching CW, Ching KA, Antosiewicz-Bourget JE, Liu H, Zhang X, Green RD, Lobanenkov VV, Stewart R, Thomson JA, Crawford GE, Kellis M, Ren B. Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 2009, 459(7243):108-112. 10.1038/nature07829, 2910248, 19295514.
28. Heintzman ND, Stuart RK, Hon G, Fu Y, Ching CW, Hawkins RD, Barrera LO, Van Calcar S, Qu C, Ching KA, Wang W, Weng Z, Green RD, Crawford GE, Ren B. Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat Genet 2007, 39(3):311-318. 10.1038/ng1966, 17277777.
29. Tew SR, Clegg PD, Brew CJ, Redmond CM, Hardingham TE. SOX9 transduction of a human chondrocytic cell line identifies novel genes regulated in primary human chondrocytes and in osteoarthritis. Arthritis Res Ther 2007, 9(5):R107. 10.1186/ar2311, 2212576, 17935617.
30. Kerney R, Hall BK, Hanken J. Regulatory elements of Xenopus col2a1 drive cartilaginous gene expression in transgenic frogs. Int J Dev Biol 2010, 54(1):141-150. 10.1387/ijdb.092848rk, 19757383.
31. Lefebvre V, Huang W, Harley VR, Goodfellow PN, de Crombrugghe B. SOX9 is a potent activator of the chondrocyte-specific enhancer of the pro alpha1(II) collagen gene. Mol Cell Biol 1997, 17(4):2336-2346. 232082, 9121483.
32. Oh CD, Maity SN, Lu JF, Zhang J, Liang S, Coustry F, de Crombrugghe B, Yasuda H. Identification of SOX9 interaction sites in the genome of chondrocytes. PLoS One 2010, 5(4):e10113. 10.1371/journal.pone.0010113, 2852419, 20404928.
33. Zhou G, Lefebvre V, Zhang Z, Eberspaecher H, de Crombrugghe B. Three high mobility group-like sequences within a 48-base pair enhancer of the Col2a1 gene are required for cartilage-specific expression in vivo. J Biol Chem 1998, 273(24):14989-14997. 10.1074/jbc.273.24.14989, 9614106.
34. Park JS, Yang HN, Woo DG, Jeon SY, Do HJ, Lim HY, Kim JH, Park KH. Chondrogenesis of human mesenchymal stem cells mediated by the combination of SOX trio SOX5, 6, and 9 genes complexed with PEI-modified PLGA nanoparticles. Biomaterials 2011, 32(14):3679-3688. 10.1016/j.biomaterials.2011.01.063, 21333351.
35. Amarilio R, Viukov SV, Sharir A, Eshkar-Oren I, Johnson RS, Zelzer E. HIF1alpha regulation of Sox9 is necessary to maintain differentiation of hypoxic prechondrogenic cells during early skeletogenesis. Development 2007, 134(21):3917-3928. 10.1242/dev.008441, 17913788.
36. Greenwel P, Inagaki Y, Hu W, Walsh M, Ramirez F. Sp1 is required for the early response of alpha2(I) collagen to transforming growth factor-beta1. J Biol Chem 1997, 272(32):19738-19745. 10.1074/jbc.272.32.19738, 9242631.
37. Iwamoto M, Higuchi Y, Enomoto-Iwamoto M, Kurisu K, Koyama E, Yeh H, Rosenbloom J, Pacifici M. The role of ERG (ets related gene) in cartilage development. Osteoarthritis and cartilage / OARS, Osteoarthritis Research Society 2001, 9(Suppl A):S41-47.
38. Nakada C, Iida A, Tabata Y, Watanabe S. Forkhead transcription factor foxe1 regulates chondrogenesis in zebrafish. J Exp Zool 2009, 312(8):827-840.
39. Boquest AC, Shahdadfar A, Fronsdal K, Sigurjonsson O, Tunheim SH, Collas P, Brinchmann JE. Isolation and transcription profiling of purified uncultured human stromal stem cells: alteration of gene expression after in vitro cell culture. Mol Biol Cell 2005, 16(3):1131-1141. 10.1091/mbc.E04-10-0949, 551479, 15635089.
40. Nombela-Arrieta C, Ritz J, Silberstein LE. The elusive nature and function of mesenchymal stem cells. Nature reviews 2011, 12(2):126-131. 10.1038/nrm3049, 3346289, 21253000.
41. Weake VM, Workman JL. Inducible gene expression: diverse regulatory mechanisms. Nat Rev Genet 2010, 11(6):426-437. 10.1038/nrg2781, 20421872.
42. Lindeman LC, Andersen IS, Reiner AH, Li N, Aanes H, Ostrup O, Winata C, Mathavan S, Muller F, Alestrom P, Collas P. Prepatterning of developmental gene expression by modified histones before zygotic genome activation. Dev Cell 2011, 21(6):993-1004. 10.1016/j.devcel.2011.10.008, 22137762.
43. Schuettengruber B, Chourrout D, Vervoort M, Leblanc B, Cavalli G. Genome regulation by polycomb and trithorax proteins. Cell 2007, 128(4):735-745. 10.1016/j.cell.2007.02.009, 17320510.
44. Pirngruber J, Shchebet A, Johnsen SA. Insights into the function of the human P-TEFb component CDK9 in the regulation of chromatin modifications and co-transcriptional mRNA processing. Cell cycle (Georgetown, Tex) 2009, 8(22):3636-3642.
45. Vermeulen M, Mulder KW, Denissov S, Pijnappel WW, van Schaik FM, Varier RA, Baltissen MP, Stunnenberg HG, Mann M, Timmers HT. Selective anchoring of TFIID to nucleosomes by trimethylation of histone H3 lysine 4. Cell 2007, 131(1):58-69. 10.1016/j.cell.2007.08.016, 17884155.
46. Vermeulen M, Eberl HC, Matarese F, Marks H, Denissov S, Butter F, Lee KK, Olsen JV, Hyman AA, Stunnenberg HG, Mann M. Quantitative interaction proteomics and genome-wide profiling of epigenetic histone marks and their readers. Cell 2010, 142(6):967-980. 10.1016/j.cell.2010.08.020, 20850016.
47. Yun M, Wu J, Workman JL, Li B. Readers of histone modifications. Cell Res 2011, 21(4):564-578. 10.1038/cr.2011.42, 3131977,3131977, 21423274.
48. Yoh SM, Lucas JS, Jones KA. The Iws1:Spt6:CTD complex controls cotranscriptional mRNA biosynthesis and HYPB/Setd2-mediated histone H3K36 methylation. Genes Dev 2008, 22(24):3422-3434. 10.1101/gad.1720008, 2607075, 19141475.
49. Dysvik B, Jonassen I. J-Express: exploring gene expression data using Java. Bioinformatics (Oxford, England) 2001, 17(4):369-370.
50. Kolasinska-Zwierz P, Down T, Latorre I, Liu T, Liu XS, Ahringer J. Differential chromatin marking of introns and expressed exons by H3K36me3. Nat Genet 2009, 41(3):376-381. 10.1038/ng.322, 2648722, 19182803.
51. Gu H, Bock C, Mikkelsen TS, Jager N, Smith ZD, Tomazou E, Gnirke A, Lander ES, Meissner A. Genome-scale DNA methylation mapping of clinical samples at single-nucleotide resolution. Nat Methods 2010, 7(2):133-136. 10.1038/nmeth.1414, 2860480, 20062050.
52. Murdoch AD, Grady LM, Ablett MP, Katopodi T, Meadows RS, Hardingham TE. Chondrogenic differentiation of human bone marrow stem cells in transwell cultures: generation of scaffold-free cartilage. Stem Cells 2007, 25(11):2786-2796. 10.1634/stemcells.2007-0374, 17656642.