Differential spatial and structural organization of the X chromosome underlies dosage compensation in C. elegans

Genes and Development

Volumn 28, Issue 23, 2014, Pages 2591-2596

  Sharma, Rahul ^a   Jost, Daniel ^b   Kind, Jop ^c   Gómez Saldivar, Georgina ^d   van Steensel, Bas ^c   Askjaer, Peter ^d,e,f   Vaillant, Cédric ^b   Meister, Peter ^a  

^a UNIVERSITY OF BERN   (Switzerland)

^b CNRS   (France)

^c NETHERLANDS CANCER INSTITUTE   (Netherlands)

^d CSIC   (Spain)

^e Universidad Pablo de Olavide   (Spain)

^f UNIVERSIDAD PABLO DE OLAVIDE   (Spain)

Author keywords

C. elegans; Dosage compensation; Nuclear organization; Nuclear pores

Indexed keywords

CAENORHABDITIS ELEGANS;

ANIMAL; BIOLOGICAL MODEL; CAENORHABDITIS ELEGANS; CHEMISTRY; GENE EXPRESSION REGULATION; GENETICS; HERMAPHRODITE; MALE; X CHROMOSOME;

ANIMALS; CAENORHABDITIS ELEGANS; DOSAGE COMPENSATION, GENETIC; GENE EXPRESSION REGULATION; HERMAPHRODITIC ORGANISMS; MALE; MODELS, GENETIC; X CHROMOSOME;

EID: 84914177367     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.248864.114     Document Type: Article

References (40)

1. Askjaer P, Ercan S, Meister P. 2014. Modern techniques for the analysis of chromatin and nuclear organization in C. elegans. In WormBook (ed. The C. elegans Research Community) WormBook, doi: 10.1895/ wormbook.1.169.1. http://www.wormbook.org.
2. Bohn M, Heermann DW. 2010. Diffusion-driven looping provides a consistent framework for chromatin organization. PLoS ONE 5: e12218.
3. Capelson M, Liang Y, Schulte R, Mair W, Wagner U, Hetzer MW. 2010. Chromatin-bound nuclear pore components regulate gene expression in higher eukaryotes. Cell 140: 372-383.
4. Casolari JM, Brown CR, Komili S, West J, Hieronymus H, Silver PA. 2004. Genome-wide localization of the nuclear transport machinery couples transcriptional status and nuclear organization. Cell 117: 427-439.
5. Chow JC, Heard E. 2010. Nuclear organization and dosage compensation. Cold Spring Harb Perspect Biol 2: a000604.
6. Chuang PT, Albertson DG, Meyer BJ. 1994. DPY-27: a chromosome condensation protein homolog that regulates C. elegans dosage compensation through association with the X chromosome. Cell 79: 459-474.
7. Csankovszki G, McDonel P, Meyer BJ. 2004. Recruitment and spreading of the C. elegans dosage compensation complex along X chromosomes. Science 303: 1182-1185.
8. Csankovszki G, Collette K, Spahl K, Carey J, Snyder M, Petty E, Patel U, Tabuchi T, Liu H, McLeod I, et al. 2009. Three distinct condensin complexes control C. elegans chromosome dynamics. Curr Biol 19: 9-19.
9. Dawes HE, Berlin DS, Lapidus DM, Nusbaum C, Davis TL, Meyer BJ. 1999. Dosage compensation proteins targeted to X chromosomes by a determinant of hermaphrodite fate. Science 284: 1800-1804.
10. Deng X, Hiatt JB, Nguyen DK, Ercan S, Sturgill D, Hillier LW, Schlesinger F, Davis CA, Reinke VJ, Gingeras TR, et al. 2011. Evidence for compensatory upregulation of expressed X-linked genes in mammals, Caenorhabditis elegans and Drosophila melanogaster. Nat Genet 43: 1179-1185.
11. Doi M, Edwards SF, ed. 1988. The theory of polymer dynamics. Oxford University Press, Oxford.
12. Ercan S, Dick LL, Lieb JD. 2009. The C. elegans dosage compensation complex propagates dynamically and independently of X chromosome sequence. Curr Biol 19: 1777-1787.
13. Fernandez AG, Piano F. 2006. MEL-28 is downstream of the Ran cycle and is required for nuclear-envelope function and chromatin maintenance. Curr Biol 16: 1757-1763.
14. Ferrari F, Alekseyenko AA, Park PJ, Kuroda MI. 2014. Transcriptional control of a whole chromosome: emerging models for dosage compensation. Nat Struct Mol Biol 21: 118-125.
15. Ferreira HC, Towbin BD, Jegou T, Gasser SM. 2013. The shelterin protein POT-1 anchors Caenorhabditis elegans telomeres through SUN-1 at the nuclear periphery. J Cell Biol 203: 727-735.
16. Galy V, Askjaer P, Franz C, Lopez-Iglesias C, Mattaj IW. 2006. MEL-28, a novel nuclear-envelope and kinetochore protein essential for zygotic nuclear-envelope assembly in C. elegans. Curr Biol 16: 1748-1756.
17. Gonzalez-Aguilera C, Ikegami K, Ayuso C, de Luis A, Iniguez M, Cabello J, Lieb JD, Askjaer P. 2014. Genome-wide analysis links emerin to neuromuscular junction activity in Caenorhabditis elegans. Genome Biol 15: R21.
18. Grimaud C, Becker PB. 2009. The dosage compensation complex shapes the conformation of the X chromosome in Drosophila. Genes Dev 23: 2490-2495.
19. Ikegami K, Lieb JD. 2013. Integral nuclear pore proteins bind to Pol IIItranscribed genes and are required for Pol III transcript processing in C. elegans. Mol Cell 51: 840-849.
20. Ikegami K, Egelhofer TA, Strome S, Lieb JD. 2010. Caenorhabditis elegans chromosome arms are anchored to the nuclear membrane via discontinuous association with LEM-2. Genome Biol 11: R120.
21. Jans J, Gladden JM, Ralston EJ, Pickle CS, Michel AH, Pferdehirt RR, Eisen MB, Meyer BJ. 2009. A condensin-like dosage compensation complex acts at a distance to control expression throughout the genome. Genes Dev 23: 602-618.
22. Kalverda B, Pickersgill H, Shloma VV, Fornerod M. 2010. Nucleoporins directly stimulate expression of developmental and cell-cycle genes inside the nucleoplasm. Cell 140: 360-371.
23. Kranz AL, Jiao CY, Winterkorn LH, Albritton SE, Kramer M, Ercan S. 2013. Genome-wide analysis of condensin binding in Caenorhabditis elegans. Genome Biol 14: R112.
24. Kremer K, Grest GS. 1992. Simulations for structural and dynamic properties of dense polymer systems. J Chem Soc, Faraday Trans 88: 1707-1717.
25. Kruesi WS, Core LJ, Waters CT, Lis JT, Meyer BJ. 2013. Condensin controls recruitment of RNA polymerase II to achieve nematode X-chromosome dosage compensation. eLife 2: e00808.
26. Liang Y, Franks TM, Marchetto MC, Gage FH, Hetzer MW. 2013. Dynamic association ofNUP98 with the human genome. PLoS Genet 9: e1003308.
27. Light WH, Brickner DG, Brand VR, Brickner JH. 2010. Interaction of a DNA zip code with the nuclear pore complex promotes H2A.Z incorporation and INO1 transcriptional memory. Mol Cell 40: 112-125.
28. McDonel P, Jans J, Peterson BK, Meyer BJ. 2006. Clustered DNA motifs mark X chromosomes for repression by a dosage compensation complex. Nature 444: 614-618.
29. Mendjan S, Taipale M, Kind J, Holz H, Gebhardt P, Schelder M, Vermeulen M, Buscaino A, Duncan K, Mueller J, et al. 2006. Nuclear pore components are involved in the transcriptional regulation of dosage compensation in Drosophila. Mol Cell 21: 811-823.
30. Metzger S, Muller M, Binder K, Baschnagel J. 2003. Surface excess in dilute polymer solutions and the adsorption transition versus wetting phenomena. J Chem Phys 118: 8489-8499.
31. Petty E, Laughlin E, Csankovszki G. 2011. Regulation of DCC localization by HTZ-1/H2A.Z and DPY-30 does not correlate with H3K4 methylation levels. PLoS ONE 6: e25973.
32. Pferdehirt RR, Kruesi WS, Meyer BJ. 2011. An MLL/COMPASS subunit functions in the C. elegans dosage compensation complex to target X chromosomes for transcriptional regulation of gene expression. Genes Dev 25: 499-515.
33. Rohner S, Kalck V, Wang X, Ikegami K, Lieb JD, Gasser SM, Meister P. 2013. Promoter- and RNA polymerase II-dependent hsp-16 gene association with nuclear pores in Caenorhabditis elegans. J Cell Biol 200: 589-604.
34. Strome S, Kelly WG, Ercan S, Lieb JD. 2014. Regulation of the X chromosomes in Caenorhabditis elegans. Cold Spring Harb Perspect Biol 6: a018366.
35. Taddei A, Van Houwe G, Hediger F, Kalck V, Cubizolles F, Schober H, Gasser SM. 2006. Nuclear pore association confers optimal expression levels for an inducible yeast gene. Nature 441: 774-778.
36. Towbin BD, Gonzalez-Aguilera C, Sack R, Gaidatzis D, Kalck V, Meister P, Askjaer P, Gasser SM. 2012. Step-wise methylation of histone H3K9 positions heterochromatin at the nuclear periphery. Cell 150: 934-947.
37. Vaquerizas JM, Suyama R, Kind J, Miura K, Luscombe NM, Akhtar A. 2010. Nuclear pore proteins nup153 and megator define transcriptionally active regions in the Drosophila genome. PLoS Genet 6: e1000846.
38. Vielle A, Lang J, Dong Y, Ercan S, Kotwaliwale C, Rechtsteiner A, Appert A, Chen QB, Dose A, Egelhofer T, et al. 2012. H4K20me1 contributes to downregulation of X-linked genes for C. elegans dosage compensation. PLoS Genet 8: e1002933.
39. Wells MB, Snyder MJ, Custer LM, Csankovszki G. 2012. Caenorhabditis elegans dosage compensation regulates histone H4 chromatin state on X chromosomes. Mol Cell Biol 32: 1710-1719.
40. Whittle CM, McClinic KN, Ercan S, Zhang X, Green RD, Kelly WG, Lieb JD. 2008. The genomic distribution and function of histone variant HTZ-1 during C. elegans embryogenesis. PLoS Genet 4: e1000187.