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J. Biol. Chem., Vol. 280, Issue 18, 17732-17736, May 6, 2005

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Spatial Distribution of Di- and Tri-methyl Lysine 36 of Histone H3 at Active Genes^*

Andrew J. Bannister, Robert Schneider¶, Fiona A. Myers||, Alan W. Thorne||, Colyn Crane-Robinson||, and Tony Kouzarides**

From the Wellcome Trust/Cancer Research UK Gurdon Institute and Department of Pathology, Tennis Court Road, Cambridge, CB2 1QN, United Kingdom, the ^¶Max Planck Institute for Immunbiology, 79108 Freiburg, Germany, and the ^||Biophysics Laboratories, Institute of Biomedical and Biomolecular Sciences, University of Portsmouth, Portsmouth PO1 2DT, United Kingdom

Received for publication, January 21, 2005 , and in revised form, March 9, 2005.

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Methylation of lysine 4 of histone H3 (K4/H3) is linked to transcriptional activity, whereas methylation of K9/H3 is tightly associated with gene inactivity. These are well characterized sites of methylation within histones, but there are numerous other, less characterized, sites of modification. In Saccharomyces cerevisiae, methylation of K36/H3 has been linked to active genes, but little is known about this methylation in higher eukaryotes. Here we analyzed for the first time the levels and spatial distribution of di- and tri-methyl (di- and tri-Me) K36/H3 in metazoan genes. We analyzed chicken genes that are developmentally regulated, constitutively active, or inactive. We found that active genes contain high levels of these modifications compared with inactive genes. Furthermore, in actively transcribed regions the levels of di- and tri-Me K36/H3 peak toward the 3' end of the gene. This is in striking contrast to the distributions of di- and tri-Me K4/H3, which peak early in actively transcribed regions. Thus, di/tri-Me K4/H3 and di/tri-Me K36/H3 are both useful markers of active genes, but their genic distribution indicates differing roles. Our data suggest that the unique spatial distribution of di- and tri-Me K36/H3 plays a role in transcriptional termination and/or early RNA processing.

	INTRODUCTION

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Histone N-terminal tails are subject to a variety of post-translational covalent modifications. These include acetylation, phosphorylation, and methylation, all of which have the potential to alter chromatin architecture and thereby to affect all aspects of DNA processing (1–3). Over the last few years it has become increasingly clear that deregulation of the enzymes performing these modifications can be linked to various human pathologies including cancer (4, 5). For instance, mutations in histone acetyltransferases have been linked to cancer, and histone deacetylase inhibitors are now in the clinician's armory as anti-cancer chemotherapeutic agents (4). Histone kinases, such as the aurora kinases, have also been linked to oncogenesis (4). More recently evidence has begun to emerge implicating histone methyltransferases in developmental disorders as well as in cancer (6).

In vivo histone lysines may be mono-, di-, or tri-methylated, but little is known concerning the functional interplay between these different levels of methylation. In metazoa the levels of the di- and tri-methyl forms of lysine 4 of histone H3 (K4/H3) have been shown to peak in the 5' transcribed region of active genes, implicating both in the early phases of transcriptional elongation (7). Consistent with this the yeast Set1p enzyme that is responsible for methylating K4/H3 is found associated with the initiation-elongation phosphorylated form of RNA pol II,¹ RNAPII-5P (8). Another H3 modification, di-methyl K36/H3, also has been found in the transcribed region of active genes in yeast (9, 10). In this case, the Set2p enzyme that methylates K36/H3 associates with the elongation-termination form of RNA pol II, RNAPII-2P (9, 10).

Recently, the mammalian NSD1 protein has been shown to possess K36/H3 methyltransferase activity (6). Haploinsufficiency of the NSD1 gene leads to Sotos syndrome, which is a neurological disorder characterized by overgrowth in childhood, advanced bone age, craniofacial abnormalities, mental retardation, and possibly a susceptibility to cancer (11, 12). In addition, translocation of the NSD1 gene leads to the development of certain leukemias (13). Taken together, these facts suggest that deregulation of K36/H3 methylation and the resulting effect on transcription may be crucial events in cellular transformation.

Mapping studies have analyzed the spatial distribution of di-methyl K36/H3 in active yeast genes and have found that this modification is generally enriched in transcribed regions, but no definitive trend within transcribed regions has been observed (9, 10). Furthermore, recent experiments performed in mammalian cells have mapped di-Me K36/H3 to active genes but not inactive genes (14). However, to date nothing is known concerning the role of tri-Me K36/H3. Here, we describe the characterization of anti tri-Me K36/H3 antisera and use the antibody to map tri-Me K36/H3 to active metazoan genes. Analysis of the spatial distribution of di- and tri-Me K36/H3 within active genes indicates that the levels of these modifications increase toward the 3' end of actively transcribing genes.

	MATERIALS AND METHODS

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Antibodies—Di-methyl K36/H3-specific antibodies were purchased from Upstate Biotechnology. Tri-methyl K36/H3-specific antibodies are now available from Abcam Ltd.

Nucleosome Preparation and Chromatin Immunoprecipitation— Chicken mononucleosomes were prepared and chromatin immunoprecipitations (ChIPs) performed essentially as described previously (20, 21). Typically, 150 µg of sucrose gradient-purified input mononucleosomes (as DNA) were dialyzed into the immunoprecipitation buffer (150 mM NaCl, 0.02% SDS, 20 mM Tris·HCl, pH 8.0, 2 mM EDTA, 0.9% Triton X-100) and immunoprecipitated at 4 °C with 10 µg of affinity-purified antibodies in the presence of protein A/G beads (Amersham Biosciences). The beads were then washed five times with immunoprecipitation buffer and twice with wash buffer (350 mM NaCl, 0.02% SDS, 20 mM Tris·HCl, pH 8.0, 2 mM EDTA, 0.9% Triton X-100). The histones and DNA from the input, unbound (supernatant), and bound fractions were recovered as described (20).

Quantitative Real-time PCR—Using an ABI 7000 real-time PCR system and the TaqMan PCR Master Mix protocol (Applied Biosystems), differences in the DNA content of the bound and input fractions were determined. Bound to input (B/I) ratios were determined for each amplicon by taking a fixed aliquot of the DNA extracted from the input and bound nucleosomal samples. These were amplified together with a defined amount of genomic DNA on the same plate, using the latter to construct the standard curve. B/I values for any one amplicon are thus in the correct quantitative ratio to B/I values for other amplicons measured for the same ChIP, because this procedure compensates for differences in the PCR efficiencies of different probe/primer combinations and for nucleosome representation. However, B/I values derived using different ChIPs cannot be quantitatively compared because of variations in the efficiency of individual immunoprecipitations. All data within each graphical representation are derived from a single representative ChIP experiment; repeat ChIPs were found to give the same relative spatial distributions of B/I values across all amplicons. PCR reactions were carried out in triplicate using fixed amounts of template DNA from each fraction: 50 °C for 2 min and 95 °C for 10 min followed by 40 cycles of 15 s at 95 °C and 1 min at 60 °C. The threshold (C_T) was set such that the fluorescence signal was above the base-line noise but as low as possible in the exponential amplification phase. For each amplicon a standard curve was determined by plotting the number of cycles at which the fluorescence crossed the threshold (crossing values) against increasing amounts of genomic DNA template. Based on this standard curve, the DNA sequence content of the input and bound fractions was determined. All primers and TaqMan probes were designed using ABI Primer Express software. The PCR products were substantially shorter than 200 bp, the length of DNA in a nucleosome. Primer and TaqMan sequences are available on request.

	RESULTS

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To better evaluate the role of methylation of K36/H3 in transcription in metazoans, we asked whether the tri-methylation of K36/H3 is more tightly associated with gene activity or inactivity and determined the spatial distribution of this modification within several genes. To this end we performed ChIPs with anti tri-Me K36/H3 antibodies and mapped the presence of this modification in the promoter and transcribed region of developmentally regulated, constitutively active and inactive chicken genes. Input chromatin was in the form of mononucleosomes purified from the nuclei of 15-day chicken embryo erythrocytes; the DNA sequence content of the antibody-bound nucleosomes was analyzed by real-time PCR with short amplicons. The resulting mapping is thus at the mononucleosome level. The experimental methods used were exactly as described for our previous determination of the distribution of di- and tri-Me K4/H3 (7).

First, the specificity of the antibody against tri-Me K36/H3 was verified. This was done by using the antibodies in Western blots of various histone preparations (Fig. 1). We prepared total cellular extracts from three strains of Schizosaccharomyces pombe: wild type; a set1 knock-out lacking the Set1p K4/H3 methyltransferase; and a set2 knock-out, which lacks the Set2p K36/H3 methyltransferase. The antibody specifically recognizes a band corresponding to histone H3 in the wild type strain. Importantly, this recognition is maintained in the set1 knock-out strain but is lost in the set2 knock-out strain (Fig. 1A). This confirms the specificity of the antibodies for Me K36/H3. Furthermore, recognition of the H3 epitope is specifically blocked by an H3 peptide containing tri-Me Lys-36 but not by peptides bearing mono-Me or di-Me Lys-36, nor is it affected by peptides containing tri-Me lysine at positions other than Lys-36 (Fig. 1B and data not shown). We conclude that the antibody is specific for the tri-methylated form of K36/H3.

View larger version (14K): [in this window] [in a new window]   FIG. 1. Characterization of the K36/H3 tri-methyl-specific antibody. A, total cellular extract was prepared from three strains of S. pombe: wild type (WT), a set1 knock-out (which lacks the Set1p K4/H3 methyltransferase; set1), and a set2 knock-out (which lacks the Set2p K36/H3 methyltransferase; set2). The extract was resolved on a 20% SDS-PAGE, transferred to nitrocellulose, and Western blotted with the anti tri-Me K36/H3 antibody. B, 250 ng of purified H3 (Roche Applied Science) was Western blotted as described above with the anti-tri-Me K36/H3 antibody either in the presence (1 µg/ml) or absence of specific peptide competitors as indicated.

View larger version (22K): [in this window] [in a new window]   FIG. 2. Distribution of tri-Me K36/H3 at the chicken -globin locus. a, map of the -globin locus indicating the position of the genes (, H, A, ) and TaqMan probes. Amplicons: heterochromatin, in the 16 kb of 5'-heterochromatin; prom, promoter; trans, transcribed region. b, distribution of tri-Me K36/H3 in 15-day chicken embryo erythrocytes. The enrichment of a given sequence is plotted as the ratio of the antibody bound to input signals (B/I) of the amplicon. The H and the A genes are transcriptionally active, whereas the and the genes are inactive. Each data point indicates the average of independent PCR analysis with the standard deviation shown by the error bars. c, comparison of tri-Me K36/H3 at active and inactive genes in 15-day erythrocytes. Tri-Me K36/H3 levels are plotted at amplicons in the 5' transcribed regions of the transcriptionally active vimentin, Gas41, carbonic anhydrase, GAPDH, and L30 genes and in the 5' transcribed regions of the transcriptionally inactive troponin T, -amylase, insulin, calcitonin, myoD, and myf-5 genes.

View larger version (8K): [in this window] [in a new window]   FIG. 3. Comparison of tri-Me K36/H3 at the 5' and 3' ends of active genes. Tri-Me K36/H3 levels at amplicons in the 5' transcribed regions and the 3' transcribed regions of the transcriptionally active vimentin, DNAPKcs (DNA-dependent protein kinase, catalytic subunit), and ribosomal protein L30 and MHCII genes are plotted.

View larger version (19K): [in this window] [in a new window]   FIG. 4. Spatial distribution of di- and tri-Me K36/H3 across active genes. a, organization of the chicken GAPDH gene with the positions of the amplicons analyzed. Amplicon 1 is in the GAPDH promoter, and amplicons 2–4 are in the transcribed region. Di-Me K36/H3, tri-Me K36/H3, and tri-Me K4/H3 levels are shown. b, organization of the CA (chicken carbonic anhydrase) gene with the positions of the amplicons analyzed. Amplicon 1 is in the CA promoter, and amplicons 2–5 are in the transcribed region. Di-Me K36/H3, Tri-Me K36/H3, and tri-Me K4/H3 levels are shown.

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

The above data clearly show that in metazoans di- and tri-Me K36/H3 is associated with the process of active transcription, but what process could require Me K36/H3? We previously reported that di- and tri-Me K4/H3 levels peak in the early transcribed region of the active genes analyzed here (7). This led us to suggest that methyl K4/H3 has an important role in the early phase of transcriptional elongation. In contrast, in the present study we find that di- and tri-Me K36/H3 peak toward the 3' end of actively transcribing regions, implying that methyl K36/H3 has a different role than that of di- and tri-Me K4/H3. Furthermore, we detect no significant differences between the spatial distributions of di- and tri-Me K36/H3, suggesting that these modifications may have very similar or overlapping functions. Me K36/H3 modification levels reach a maximum right at the end of the 4-kb GAPDH gene but 15 nucleosomes before the end of the four times longer CA gene, so the peak might occur at an approximately fixed distance from the start of transcription. However, the DNAPKcs gene is 85 kb long, and the 3' amplicon monitored (Fig. 3) is in the last of 86 exons; so the peak of tri-Me K36/H3 is clearly located close to the end of the transcribed region, whatever its length, and might therefore be directly involved in transcription termination or have a role in transcriptionally linked early mRNA processing. Consistent with the second possibility, the transcribing RNA polymerase (to which Set2p binds) has been shown to be involved in the early phase of RNA processing (18). Furthermore, the yeast Set2 protein contains a WW motif, a motif recently shown to be essential in proteins involved in pre-mRNA splicing, which is a process that occurs in vivo in concert with transcription (19). Whatever the detailed explanations, the mapping studies reported here suggest that methylated K4/H3 and methylated K36/H3 have distinct roles at active genes.

	FOOTNOTES

 
^* This work was supported by Cancer Research UK and European Union Grant QLG1-CT-2000-01935 (to T. K. laboratory) and by Biotechnology and Biological Sciences Research Council (to C. C.-R. laboratory). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

These authors contributed equally.

^** To whom correspondence should be addressed: Wellcome Cancer Research UK Gurdon Institute, Tennis Ct. Rd., Cambridge CB2 1QN, UK. Tel.: 44-1223-334112; Fax: 44-1223-334089; E-mail: tk106{at}mole.bio.cam.ac.uk.

¹ The abbreviations used are: pol II, polymerase II; ChIP, chromatin immunoprecipitation.

	REFERENCES

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 

1. Fischle, W., Wang, Y., and Allis, C. D. (2003) Curr. Opin. Cell Biol. 2, 172–183
2. Strahl, B. D., and Allis, C. D. (2002) Nature 403, 41–45
3. Turner, B. M. (1993) Cell 75, 5–8[CrossRef][Medline] [Order article via Infotrieve]
4. Hake, S. B., Xiao, A., and Allis, C. D. (2004) Br. J. Cancer 90, 761–769[CrossRef][Medline] [Order article via Infotrieve]
5. Schneider, R., Bannister, A. J., and Kouzarides T. (2002) Trends Biochem. Sci. 27, 396–402[CrossRef][Medline] [Order article via Infotrieve]
6. Rayasam, G. V., Wendling, O., Angrand, P. O., Mark, M., Niederreither, K., Song, L., Lerouge, T., Hager, G. L., Chambon, P., and Losson, R. (2003) EMBO J. 16, 3153–3163[CrossRef]
7. Schneider, R., Bannister, A. J., Myers, F. A., Thorne, A. W., Crane-Robinson, C., and Kouzarides, T. (2004) Nat. Cell. Biol. 6, 73–77[CrossRef][Medline] [Order article via Infotrieve]
8. Ng, H. H., Robert, F., Young, R. A., and Struhl, K. (2003) Mol. Cell 11, 709–719[CrossRef][Medline] [Order article via Infotrieve]
9. Xiao, T., Hall, H., Kizer, K. O., Shibata, Y., Hall, M. C., Borchers, C. H., and Strahl, B. D. (2003) Genes Dev. 17, 654–663[Abstract/Free Full Text]
10. Krogan, N. J., Kim, M., Tong, A., Golshani, A., Cagney, G., Canadien, V., Richards, D. P, Beattie, B. K., Emili, A., Boone, C., Shilatifard, A., Buratowski, S., and Greenblatt, J. (2003) Mol. Cell. Biol. 23, 4207–4218[Abstract/Free Full Text]
11. Visser, R., and Matsumoto, N. (2003) Curr. Opin. Pediatr. 15, 598–606[CrossRef][Medline] [Order article via Infotrieve]
12. De Boer, L., Duyvenvoorde, H. A., Willemstein-Van Hove, E. C., Hoogerbrugge, C. M., Van Doorn, J., Maassen, J. A., Karperien, M., and Wit, J. M. (2004) Eur. J. Endocrinol. 151, 333–341[Abstract]
13. Al-Mulla, N., Belgaumi, A. F., and Teebi, A. (2004) J. Pediatr. Hematol. Oncol. 26, 204–208[Medline] [Order article via Infotrieve]
14. Zhou, M., Deng, L., Lacoste, V., Park, H. U., Pumfery, A., Kashanchi, F., Brady, J. N., and Kumar, A. (2004) J. Virol. 78, 13522–13533[Abstract/Free Full Text]
15. Felsenfeld, G. (1993) Gene 135, 119–124[CrossRef][Medline] [Order article via Infotrieve]
16. Strahl, B. D., Grant P, A., Briggs, S. D., Sun, Z., Bone, J. R., Caldwell, J. A., Mollah, S., Cook, R. G., Shabanowitz, J., Hunt, D. F., and Allis, C. D. (2002) Mol. Cell. Biol. 22, 1298–1306[Abstract/Free Full Text]
17. Landry, J., Sutton, A., Hesman, T., Min, J., Rui-Ming, X., Johnston, M., and Sternglanz, R. (2003) Mol. Cell. Biol. 23, 5972–5978[Abstract/Free Full Text]
18. Bird, G., Zorio, D. A., and Bentley, D. L. (2004) Mol. Cell. Biol. 24, 8963–8969[Abstract/Free Full Text]
19. Lin, K.-T., Lu, R.-M., and Tarn, W.-Y. (2004) Mol. Cell. Biol. 24, 9176–9185[Abstract/Free Full Text]
20. Hebbes, T. R., Clayton, A. L., Thorne, A. W., and Crane-Robinson, C. (1994) EMBO J. 13, 1823–1830[Medline] [Order article via Infotrieve]
21. Myers, F. A., Evans, D. R., Clayton, A. L., Thorne, A. W., and Crane-Robinson, C. (2001) J. Biol. Chem. 276, 20197–20205[Abstract/Free Full Text]

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This Article Abstract Full Text (PDF) All Versions of this Article: 280/18/17732    most recent M500796200v1 Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Bannister, A. J. Articles by Kouzarides, T. Search for Related Content PubMed PubMed Citation Articles by Bannister, A. J. Articles by Kouzarides, T. Social Bookmarking                      What's this?