Independent mechanisms target SMCHD1 to trimethylated histone H3 lysine 9-modified chromatin and the inactive X chromosome

Molecular and Cellular Biology

Volumn 35, Issue 23, 2015, Pages 4053-4068

  Brideau, Nicholas J ^a   Coker, Heather ^a   Gendrel, Anne Valerie ^a,d   Siebert, C Alistair ^b   Bezstarosti, Karel ^c   Demmers, Jeroen ^c   Poot, Raymond A ^c   Nesterova, Tatyana B ^a   Brockdorff, Neil ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c ERASMUS MEDICAL CENTER   (Netherlands)

^d INSTITUT CURIE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CHROMOSOME PROTEIN; CONDENSIN; HETEROCHROMATIN PROTEIN 1 GAMMA; HISTONE H3; HOMODIMER; LYSINE; PROTEIN; PROTEIN GHKL; PROTEIN LRIF1; PROTEIN SMCHD1; UNCLASSIFIED DRUG; CHROMATIN; HETEROCHROMATIN-SPECIFIC NONHISTONE CHROMOSOMAL PROTEIN HP-1; HISTONE; NONHISTONE PROTEIN; SMCHD1 PROTEIN, HUMAN; SMCHD1 PROTEIN, MOUSE;

ARTICLE; CHROMOSOME ARM; COMPLEX FORMATION; CONTROLLED STUDY; ELECTRON MICROSCOPY; HISTONE METHYLATION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; MOLECULAR BIOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEOMICS; REGULATORY MECHANISM; SF9 CELL LINE; TRIMETHYLATION; WESTERN BLOTTING; X CHROMOSOME; AMINO ACID SEQUENCE; ANIMAL; CELL LINE; CHEMISTRY; CHROMATIN; HEK293 CELL LINE; METABOLISM; MOLECULAR GENETICS; MOLECULAR MODEL; MOUSE; PROTEIN MULTIMERIZATION; PROTEIN TERTIARY STRUCTURE; SEQUENCE ALIGNMENT;

ADENOSINE TRIPHOSPHATASES; AMINO ACID SEQUENCE; ANIMALS; CELL LINE; CHROMATIN; CHROMOSOMAL PROTEINS, NON-HISTONE; HEK293 CELLS; HISTONES; HUMANS; LYSINE; MICE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN INTERACTION MAPS; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT; X CHROMOSOME;

EID: 84946232835     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00432-15     Document Type: Article

References (50)

1. Blewitt ME, Vickaryous NK, Hemley SJ, Ashe A, Bruxner TJ, Preis JI, Arkell R, Whitelaw E. 2005. An N-ethyl-N-nitrosourea screen for genes involved in variegation in the mouse. Proc Natl Acad Sci U S A 102:7629-7634. http://dx.doi.org/10.1073/pnas.0409375102.
2. Ashe A, Morgan DK, Whitelaw NC, Bruxner TJ, Vickaryous NK, Cox LL, Butterfield NC, Wicking C, Blewitt ME, Wilkins SJ, Anderson GJ, Cox TC, Whitelaw E. 2008. A genome-wide screen for modifiers of transgene variegation identifies genes with critical roles in development. Genome Biol 9:R182. http://dx.doi.org/10.1186/gb-2008-9-12-r182.
3. Blewitt ME, Gendrel AV, Pang Z, Sparrow DB, Whitelaw N, Craig JM, Apedaile A, Hilton DJ, Dunwoodie SL, BrockdorffN, Kay GF, Whitelaw E. 2008. SmcHD1, containing a structural-maintenance-of-chromosomes hinge domain, has a critical role in X inactivation. Nat Genet 40:663-669. http://dx.doi.org/10.1038/ng.142.
4. Gendrel AV, Tang YA, Suzuki M, Godwin J, Nesterova TB, Greally JM, Heard E, BrockdorffN. 2013. Epigenetic functions of smchd1 repress gene clusters on the inactive X chromosome and on autosomes. Mol Cell Biol 33:3150-3165. http://dx.doi.org/10.1128/MCB.00145-13.
5. Mould AW, Pang Z, Pakusch M, Tonks ID, Stark M, Carrie D, Mukhopadhyay P, Seidel A, Ellis JJ, Deakin J, Wakefield MJ, Krause L, Blewitt ME, Kay GF. 2013. Smchd1 regulates a subset of autosomal genes subject to monoallelic expression in addition to being critical for X inactivation. Epigenetics Chromatin 6:19. http://dx.doi.org/10.1186/1756-8935-6-19.
6. Gendrel AV, Apedaile A, Coker H, Termanis A, Zvetkova I, Godwin J, Tang YA, Huntley D, Montana G, Taylor S, Giannoulatou E, Heard E, Stancheva I, BrockdorffN. 2012. Smchd1-dependent and -independent pathways determine developmental dynamics of CpG island methylation on the inactive X chromosome. Dev Cell 23:265-279. http://dx.doi.org/10.1016/j.devcel.2012.06.011.
7. Nozawa RS, Nagao K, Igami KT, Shibata S, Shirai N, Nozaki N, Sado T, Kimura H, Obuse C. 2013. Human inactive X chromosome is compacted through a PRC2-independent SMCHD1-HBiX1 pathway. Nat Struct Mol Biol 20:566-573. http://dx.doi.org/10.1038/nsmb.2532.
8. Larsen M, Rost S, El Hajj N, Ferbert A, Deschauer M, Walter MC, Schoser B, Tacik P, Kress W, Muller CR. 2015. Diagnostic approach for FSHD revisited:SMCHD1mutations cause FSHD2 and act as modifiers of disease severity in FSHD1. Eur J Hum Genet 23:808-816. http://dx.doi.org/10.1038/ejhg.2014.191.
9. Lemmers RJ, Tawil R, Petek LM, Balog J, Block GJ, Santen GW, Amell AM, van der Vliet PJ, Almomani R, Straasheijm KR, Krom YD, Klooster R, Sun Y, den Dunnen JT, Helmer Q, Donlin-Smith CM, Padberg GW, van Engelen BG, de Greef JC, Aartsma-Rus AM, Frants RR, de Visser M, Desnuelle C, Sacconi S, Filippova GN, Bakker B, Bamshad MJ, Tapscott SJ, Miller DG, van der Maarel SM. 2012. Digenic inheritance of an SMCHD1 mutation and an FSHD-permissive D4Z4 allele causes facioscapulohumeral muscular dystrophy type 2. Nat Genet 44:1370-1374. http://dx.doi.org/10.1038/ng.2454.
10. Sacconi S, Lemmers RJ, Balog J, van der Vliet PJ, Lahaut P, van Nieuwenhuizen MP, Straasheijm KR, Debipersad RD, Vos-Versteeg M, Salviati L, Casarin A, Pegoraro E, Tawil R, Bakker E, Tapscott SJ, Desnuelle C, van der Maarel SM. 2013. The FSHD2 gene SMCHD1 is a modifier of disease severity in families affected by FSHD1. Am J Hum Genet 93:744-751. http://dx.doi.org/10.1016/j.ajhg.2013.08.004.
11. Bohmdorfer G, Schleiffer A, Brunmeir R, Ferscha S, Nizhynska V, Kozak J, Angelis KJ, Kreil DP, Schweizer D. 2011. GMI1, a structural-maintenance-of-chromosomes-hinge domain-containing protein, is involved in somatic homologous recombination in Arabidopsis. Plant J 67:420-433. http://dx.doi.org/10.1111/j.1365-313X.2011.04604.x.
12. Coker H, BrockdorffN. 2014. SMCHD1 accumulates at DNA damage sites and facilitates the repair of DNA double-strand breaks. J Cell Sci 127:1869-1874. http://dx.doi.org/10.1242/jcs.140020.
13. Tang M, Li Y, Zhang X, Deng T, Zhou Z, Ma W, Songyang Z. 2014. Structural maintenance of chromosomes flexible hinge domain containing 1 (SMCHD1) promotes non-homologous end joining and inhibits homologous recombination repair upon DNA damage. J Biol Chem 289:34024-34032. http://dx.doi.org/10.1074/jbc. M114.601179.
14. Iyer LM, Abhiman S, Aravind L. 2008. MutL homologs in restriction-modification systems and the origin of eukaryotic MORC ATPases. Biol Direct 3:8. http://dx.doi.org/10.1186/1745-6150-3-8.
15. Dignam JD, Lebovitz RM, Roeder RG. 1983. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res 11:1475-1489. http://dx.doi.org/10.1093/nar/11.5.1475.
16. van den Berg DL, Snoek T, Mullin NP, Yates A, Bezstarosti K, Demmers J, Chambers I, Poot RA. 2010. An Oct4-centered protein interaction network in embryonic stem cells. Cell Stem Cell 6:369-381. http://dx.doi.org/10.1016/j.stem.2010.02.014.
17. Elderkin S, Maertens GN, Endoh M, Mallery DL, Morrice N, Koseki H, Peters G, BrockdorffN, Hiom K. 2007. A phosphorylated form of Mel-18 targets the Ring1B histone H2A ubiquitin ligase to chromatin. Mol Cell 28:107-120. http://dx.doi.org/10.1016/j.molcel.2007.08.009.
18. Ran FA, Hsu PD, Wright J, Agarwala V, Scott DA, Zhang F. 2013. Genome engineering using the CRISPR-Cas9 system. Nat Protoc 8:2281-2308. http://dx.doi.org/10.1038/nprot.2013.143.
19. Schleiffer A, Kaitna S, Maurer-Stroh S, Glotzer M, Nasmyth K, Eisenhaber F. 2003. Kleisins: a superfamily of bacterial and eukaryotic SMC protein partners. Mol Cell 11:571-575. http://dx.doi.org/10.1016/S1097-2765(03)00108-4.
20. Jeppsson K, Kanno T, Shirahige K, Sjogren C. 2014. The maintenance of chromosome structure: positioning and functioning of SMC complexes. Nat Rev Mol Cell Biol 15:601-614. http://dx.doi.org/10.1038/nrm3857.
21. Nasmyth K, Haering CH. 2005. The structure and function of SMC and kleisin complexes. Annu Rev Biochem 74:595-648. http://dx.doi.org/10.1146/annurev.biochem.74.082803.133219.
22. Nolivos S, Sherratt D. 2014. The bacterial chromosome: architecture and action of bacterial SMC and SMC-like complexes. FEMS Microbiol Rev 38:380-392. http://dx.doi.org/10.1111/1574-6976.12045.
23. Soh YM, Burmann F, Shin HC, Oda T, Jin KS, Toseland CP, Kim C, Lee H, Kim SJ, Kong MS, Durand-Diebold ML, Kim YG, Kim HM, Lee NK, Sato M, Oh BH, Gruber S. 2015. Molecular basis for SMC rod formation and its dissolution upon DNA binding. Mol Cell 57:290-303. http://dx.doi.org/10.1016/j.molcel.2014.11.023.
24. Melby TE, Ciampaglio CN, Briscoe G, Erickson HP. 1998. The symmetrical structure of structural maintenance of chromosomes (SMC) and MukB proteins: long, antiparallel coiled coils, folded at a flexible hinge. J Cell Biol 142:1595-1604. http://dx.doi.org/10.1083/jcb.142.6.1595.
25. Arnold K, Bordoli L, Kopp J, Schwede T. 2006. The SWISS-MODEL workspace: a Web-based environment for protein structure homology modelling. Bioinformatics 22:195-201. http://dx.doi.org/10.1093/bioinformatics/bti770.
26. Biasini M, Bienert S, Waterhouse A, Arnold K, Studer G, Schmidt T, Kiefer F, Cassarino TG, Bertoni M, Bordoli L, Schwede T. 2014. SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Res 42:W252-W258. http://dx.doi.org/10.1093/nar/gku340.
27. Tran PT, Liskay RM. 2000. Functional studies on the candidate ATPase domains of Saccharomyces cerevisiae MutLalpha. Mol Cell Biol 20:6390-6398. http://dx.doi.org/10.1128/MCB.20.17.6390-6398.2000.
28. Panaretou B, Prodromou C, Roe SM, O'Brien R, Ladbury JE, Piper PW, Pearl LH. 1998. ATP binding and hydrolysis are essential to the function of the Hsp90 molecular chaperone in vivo. EMBO J 17:4829-4836. http://dx.doi.org/10.1093/emboj/17.16.4829.
29. Hirano M, Anderson DE, Erickson HP, Hirano T. 2001. Bimodal activation of SMC ATPase by intra- and inter-molecular interactions. EMBO J 20:3238-3250. http://dx.doi.org/10.1093/emboj/20.12.3238.
30. Kurze A, Michie KA, Dixon SE, Mishra A, Itoh T, Khalid S, Strmecki L, Shirahige K, Haering CH, Lowe J, Nasmyth K. 2011. A positively charged channel within the Smc1/Smc3 hinge required for sister chromatid cohesion. EMBO J 30:364-378. http://dx.doi.org/10.1038/emboj.2010.315.
31. Dutta R, Inouye M. 2000. GHKL, an emergent ATPase/kinase superfamily. Trends Biochem Sci 25:24-28. http://dx.doi.org/10.1016/S0968-0004(99)01503-0.
32. Corbett KD, Berger JM. 2006. Structural basis for topoisomerase VI inhibition by the anti-Hsp90 drug radicicol. Nucleic Acids Res 34:4269-4277. http://dx.doi.org/10.1093/nar/gkl567.
33. Gadelle D, Bocs C, Graille M, Forterre P. 2005. Inhibition of archaeal growth and DNA topoisomerase VI activities by the Hsp90 inhibitor radicicol. Nucleic Acids Res 33:2310-2317. http://dx.doi.org/10.1093/nar/gki526.
34. Plath K, Fang J, Mlynarczyk-Evans SK, Cao R, Worringer KA, Wang H, de la Cruz CC, Otte AP, Panning B, Zhang Y. 2003. Role of histone H3 lysine 27 methylation in X inactivation. Science 300:131-135. http://dx.doi.org/10.1126/science.1084274.
35. Silva J, Mak W, Zvetkova I, Appanah R, Nesterova TB, Webster Z, Peters AH, Jenuwein T, Otte AP, BrockdorffN. 2003. Establishment of histone H3 methylation on the inactive X chromosome requires transient recruitment of Eed-Enx1 polycomb group complexes. Dev Cell 4:481-495. http://dx.doi.org/10.1016/S1534-5807(03)00068-6.
36. Eberl HC, Spruijt CG, Kelstrup CD, Vermeulen M, Mann M. 2013. A map of general and specialized chromatin readers in mouse tissues generated by label-free interaction proteomics. Mol Cell 49:368-378. http://dx.doi.org/10.1016/j.molcel.2012.10.026.
37. Nikolov M, Stutzer A, Mosch K, Krasauskas A, Soeroes S, Stark H, Urlaub H, Fischle W. 2011. Chromatin affinity purification and quantitative mass spectrometry defining the interactome of histone modification patterns. Mol Cell Proteomics 10:M110.005371. http://dx.doi.org/10.1074/mcp. M110.005371.
38. Armache KJ, Garlick JD, Canzio D, Narlikar GJ, Kingston RE. 2011. Structural basis of silencing: Sir3 BAH domain in complex with a nucleosome at 3.0 A resolution. Science 334:977-982. http://dx.doi.org/10.1126/science.1210915.
39. Chambers AL, Pearl LH, Oliver AW, Downs JA. 2013. The BAH domain of Rsc2 is a histone H3 binding domain. Nucleic Acids Res 41:9168-9182. http://dx.doi.org/10.1093/nar/gkt662.
40. Kuo AJ, Song J, Cheung P, Ishibe-Murakami S, Yamazoe S, Chen JK, Patel DJ, Gozani O. 2012. The BAH domain of ORC1 links H4K20me2 to DNA replication licensing and Meier-Gorlin syndrome. Nature 484:115-119. http://dx.doi.org/10.1038/nature10956.
41. Du J, Zhong X, Bernatavichute YV, Stroud H, Feng S, Caro E, Vashisht AA, Terragni J, Chin HG, Tu A, Hetzel J, Wohlschlegel JA, Pradhan S, Patel DJ, Jacobsen SE. 2012. Dual binding of chromomethylase domains to H3K9me2-containing nucleosomes directsDNAmethylation in plants. Cell 151:167-180. http://dx.doi.org/10.1016/j.cell.2012.07.034.
42. Hayakawa T, Haraguchi T, Masumoto H, Hiraoka Y. 2003. Cell cycle behavior of human HP1 subtypes: distinct molecular domains of HP1 are required for their centromeric localization during interphase and metaphase. J Cell Sci 116:3327-3338. http://dx.doi.org/10.1242/jcs.00635.
43. Minc E, Courvalin JC, Buendia B. 2000. HP1gamma associates with euchromatin and heterochromatin in mammalian nuclei and chromosomes. Cytogenet Cell Genet 90:279-284. http://dx.doi.org/10.1159/000056789.
44. Heard E, Rougeulle C, Arnaud D, Avner P, Allis CD, Spector DL. 2001. Methylation of histone H3 at Lys-9 is an early mark on the X chromosome during X inactivation. Cell 107:727-738. http://dx.doi.org/10.1016/S0092-8674(01)00598-0.
45. Chen K, Hu J, Moore DL, Liu R, Kessans SA, Breslin K, Lucet IS, Keniry A, Leong HS, Parish CL, Hilton DJ, Lemmers RJ, van der Maarel SM, Czabotar PE, Dobson RC, Ritchie ME, Kay GF, Murphy JM, Blewitt ME. 2015. Genome-wide binding and mechanistic analyses of Smchd1-mediated epigenetic regulation. Proc Natl Acad Sci U S A 112:E3535-E3544. http://dx.doi.org/10.1073/pnas.1504232112.
46. Song J, Teplova M, Ishibe-Murakami S, Patel DJ. 2012. Structure-based mechanistic insights into DNMT1-mediated maintenance DNA methylation. Science 335:709-712. http://dx.doi.org/10.1126/science.1214453.
47. Canudas S, Houghtaling BR, Bhanot M, Sasa G, Savage SA, Bertuch AA, Smith S. 2011. A role for heterochromatin protein 1gamma at human telomeres. Genes Dev 25:1807-1819. http://dx.doi.org/10.1101/gad.17325211.
48. Zeng W, de Greef JC, Chen YY, Chien R, Kong X, Gregson HC, Winokur ST, Pyle A, Robertson KD, Schmiesing JA, Kimonis VE, Balog J, Frants RR, Ball AR, Jr, Lock LF, Donovan PJ, van der Maarel SM, Yokomori K. 2009. Specific loss of histone H3 lysine 9 trimethylation and HP1gamma/cohesin binding at D4Z4 repeats is associated with facioscapulohumeral dystrophy (FSHD). PLoS Genet 5:e1000559. http://dx.doi.org/10.1371/journal.pgen.1000559.
49. Dejardin J, Kingston RE. 2009. Purification of proteins associated with specific genomic loci. Cell 136:175-186. http://dx.doi.org/10.1016/j.cell.2008.11.045.
50. Ciosk R, Shirayama M, Shevchenko A, Tanaka T, Toth A, Shevchenko A, Nasmyth K. 2000. Cohesin's binding to chromosomes depends on a separate complex consisting of Scc2 and Scc4 proteins. Mol Cell 5:243-254. http://dx.doi.org/10.1016/S1097-2765(00)80420-7.