Detection of histone modifications at specific gene loci in single cells in histological sections

Nature Methods

Volumn 10, Issue 2, 2013, Pages 171-177

  Gomez, Delphine ^a   Shankman, Laura S ^a   Nguyen, Anh T ^a   Owens, Gary K ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LYSINE;

ARTICLE; ATHEROSCLEROSIS; GENE EXPRESSION; HISTOLOGY; HISTONE MODIFICATION; HUMAN; IN SITU HYBRIDIZATION; IN VIVO STUDY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DETERMINATION; SINGLE CELL ANALYSIS; SMOOTH MUSCLE FIBER;

ANIMALS; ATHEROSCLEROSIS; CELL LINEAGE; CHROMATIN IMMUNOPRECIPITATION; EPIGENESIS, GENETIC; FIXATIVES; FORMALDEHYDE; HISTONES; HUMANS; IN SITU HYBRIDIZATION; LYSINE; MALE; METHYLATION; MICE; MYOCYTES, SMOOTH MUSCLE; MYOSIN HEAVY CHAINS; PARAFFIN EMBEDDING;

EID: 84873383204     PISSN: 15487091     EISSN: 15487105     Source Type: Journal    
DOI: 10.1038/nmeth.2332     Document Type: Article

References (37)

1. Jenuwein, T. & Allis, C.D. Translating the histone code. Science 293, 1074-1080 (2001).
2. Kouzarides, T. Chromatin modifcations and their function. Cell 128, 693-705 (2007).
3. Law, J.A. & Jacobsen, S.E. Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat. Rev. Genet. 11, 204-220 (2010).
4. Azuara, V. et al. Chromatin signatures of pluripotent cell lines. Nat. Cell Biol. 8, 532-538 (2006).
5. Bernstein, B.E. et al. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125, 315-326 (2006).
6. Cedar, H. & Bergman, Y. Epigenetics of haematopoietic cell development. Nat. Rev. Immunol. 11, 478-488 (2011).
7. Rada-Iglesias, A. et al. A unique chromatin signature uncovers early developmental enhancers in humans. Nature 470, 279-283 (2011).
8. Litt, M.D., Simpson, M., Gaszner, M., Allis, C.D. & Felsenfeld, G. Correlation between histone lysine methylation and developmental changes at the chicken β-globin locus. Science 293, 2453-2455 (2001).
9. Shechter, D. et al. Analysis of histones in Xenopus laevis. I. A distinct index of enriched variants and modifcations exists in each cell type and is remodeled during developmental transitions. J. Biol. Chem. 284, 1064-1074 (2009).
10. Manabe, I. & Owens, G.K. Recruitment of serum response factor and hyperacetylation of histones at smooth muscle-specifc regulatory regions during differentiation of a novel P19-derived in vitro smooth muscle differentiation system. Circ. Res. 88, 1127-1134 (2001).
11. McDonald, O.G., Wamhoff, B.R., Hoofnagle, M.H. & Owens, G.K. Control of SRF binding to CArG box chromatin regulates smooth muscle gene expression in vivo. J. Clin. Invest. 116, 36-48 (2006).
12. Miano, J.M., Cserjesi, P., Ligon, K.L., Periasamy, M. & Olson, E.N. Smooth muscle myosin heavy chain exclusively marks the smooth muscle lineage during mouse embryogenesis. Circ. Res. 75, 803-812 (1994).
13. Salmon, M., Gomez, D., Greene, E., Shankman, L. & Owens, G.K. Cooperative binding of KLF4, pELK-1, and HDAC2 to a G/C repressor element in the SM22α promoter mediates transcriptional silencing during SMC phenotypic switching in vivo. Circ. Res. 111, 685-696 (2012).
14. Owens, G.K., Kumar, M.S. & Wamhoff, B.R. Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol. Rev. 84, 767-801 (2004).
15. Alexander, M.R. & Owens, G.K. Epigenetic control of smooth muscle cell differentiation and phenotypic switching in vascular development and disease. Annu. Rev. Physiol. 74, 13-40 (2012).
16. Dahl, J.A. & Collas, P. A rapid micro chromatin immunoprecipitation assay (ChIP). Nat. Protoc. 3, 1032-1045 (2008).
17. Roh, T.Y., Ngau, W.C., Cui, K., Landsman, D. & Zhao, K. High-resolution genome-wide mapping of histone modifcations. Nat. Biotechnol. 22, 1013-1016 (2004).
18. Söderberg, O. et al. Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat. Methods 3, 995-1000 (2006).
19. Lievens, S. & Tavernier, J. Single protein complex visualization: seeing is believing. Nat. Methods 3, 971-972 (2006).
20. Rantala, J.K. et al. SHARPIN is an endogenous inhibitor of ß1-integrin activation. Nat. Cell Biol. 13, 1315-1324 (2011).
21. Brobeil, A. et al. PTPIP51 is phosphorylated by Lyn and c-Src kinases lacking dephosphorylation by PTP1B in acute myeloid leukemia. Leuk. Res. 35, 1367-1375 (2011).
22. Wirth, A. et al. G12-G13-LARG-mediated signaling in vascular smooth muscle is required for salt-induced hypertension. Nat. Med. 14, 64-68 (2008).
23. Lampugnani, M.G. et al. A novel endothelial-specifc membrane protein is a marker of cell-cell contacts. J. Cell Biol. 118, 1511-1522 (1992).
24. Li, L., Miano, J.M., Mercer, B. & Olson, E.N. Expression of the SM22α promoter in transgenic mice provides evidence for distinct transcriptional regulatory programs in vascular and visceral smooth muscle cells. J. Cell Biol. 132, 849-859 (1996).
25. Regan, C.P., Adam, P.J., Madsen, C.S. & Owens, G.K. Molecular mechanisms of decreased smooth muscle differentiation marker expression after vascular injury. J. Clin. Invest. 106, 1139-1147 (2000).
26. Carmeliet, P. Mechanisms of angiogenesis and arteriogenesis. Nat. Med. 6, 389-395 (2000).
27. Hanahan, D. Signaling vascular morphogenesis and maintenance. Science 277, 48-50 (1997).
28. Gomez, D. & Owens, G.K. Smooth muscle cell phenotypic switching in atherosclerosis. Cardiovasc. Res. 95, 156-164 (2012).
29. Weibrecht, I. et al. Visualising individual sequence-specifc protein-DNA interactions in situ. N. Biotechnol. 29, 589-598 (2012).
30. Gustafsdottir, S.M. et al. In vitro analysis of DNA-protein interactions by proximity ligation. Proc. Natl. Acad. Sci. USA 104, 3067-3072 (2007).
31. You, J.S. & Jones, P.A. Cancer genetics and epigenetics: two sides of the same coin? Cancer Cell 22, 9-20 (2012).
32. Cui, K. et al. Chromatin signatures in multipotent human hematopoietic stem cells indicate the fate of bivalent genes during differentiation. Cell Stem Cell 4, 80-93 (2009).
33. Nguyen, A.T., Taranova, O., He, J. & Zhang, Y. DOT1L, the H3K79 methyltransferase, is required for MLL-AF9-mediated leukemogenesis. Blood 117, 6912-6922 (2011).
34. Ng, R.K. & Gurdon, J.B. Epigenetic inheritance of cell differentiation status. Cell Cycle 7, 1173-1177 (2008).
35. Ng, R.K. & Gurdon, J.B. Epigenetic memory of an active gene state depends on histone H3.3 incorporation into chromatin in the absence of transcription. Nat. Cell Biol. 10, 102-109 (2008).
36. Christova, R. & Oelgeschlager, T. Association of human TFIID-promoter complexes with silenced mitotic chromatin in vivo. Nat. Cell Biol. 4, 79-82 (2002).
37. Caplice, N.M. et al. Smooth muscle cells in human coronary atherosclerosis can originate from cells administered at marrow transplantation. Proc. Natl. Acad. Sci. USA 100, 4754-4759 (2003).