KRAB zinc-finger proteins localise to novel KAP1-containing foci that are adjacent to PML nuclear bodies

Journal of Cell Science

Volumn 122, Issue 7, 2009, Pages 937-946

  Briers, Stephanie ^a   Crawford, Catherine ^a   Bickmore, Wendy A ^a   Sutherland, Heidi G ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Chromatin; Heterochromatin; Histone methylation; HP1; Nuclear organisation; Transcriptional repression

Indexed keywords

HETEROCHROMATIN PROTEIN 1; KRUPPEL ASSOCIATED BOX ASSOCIATED PROTEIN 1; KRUPPEL ASSOCIATED BOX PROTEIN; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN; ANTIBODY; DNA BINDING PROTEIN; GREEN FLUORESCENT PROTEIN; HETEROCHROMATIN SPECIFIC NONHISTONE CHROMOSOMAL PROTEIN HP 1; HETEROCHROMATIN-SPECIFIC NONHISTONE CHROMOSOMAL PROTEIN HP-1; HYBRID PROTEIN; METHYLTRANSFERASE; NONHISTONE PROTEIN; NUCLEAR PROTEIN; REPRESSOR PROTEIN; SUMO PROTEIN; SUV39H1 PROTEIN, MOUSE; TRIM28 PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL NUCLEUS INCLUSION BODY; CONSTITUTIVE HETEROCHROMATIN; CONTROLLED STUDY; EMBRYO; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; ANIMAL; ANTIBODY SPECIFICITY; CELL FRACTIONATION; CYTOLOGY; EMBRYONIC STEM CELL; HETEROCHROMATIN; METABOLISM;

MAMMALIA;

ANIMALS; ANTIBODIES; CELL DIFFERENTIATION; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA-BINDING PROTEINS; EMBRYONIC STEM CELLS; GREEN FLUORESCENT PROTEINS; HETEROCHROMATIN; INTRANUCLEAR INCLUSION BODIES; METHYLTRANSFERASES; MICE; NUCLEAR PROTEINS; ORGAN SPECIFICITY; PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS; REPRESSOR PROTEINS; SMALL UBIQUITIN-RELATED MODIFIER PROTEINS; SUBCELLULAR FRACTIONS; ZINC FINGERS;

EID: 66849091574     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.034793     Document Type: Article

References (49)

1. Ayyanathan, K., Lechner, M. S., Bell, P., Maul, G. G., Schultz, D. C., Yamada, Y., Tanaka, K., Torigoe, K. and Rauscher, F. J., 3rd (2003). Regulated recruitment of HP1 to a euchromatic gene induces mitotically heritable, epigenetic gene silencing: a mammalian cell culture model of gene variegation. Genes Dev. 17, 1855-1869.
2. Bachman, K. E., Rountree, M. R. and Baylin, S. B. (2001). Dnmt3a and Dnmt3b are transcriptional repressors that exhibit unique localization properties to heterochromatin. J. Biol. Chem. 276, 32282-32287.
3. Bernardi, R. and Pandolfi, P. P. (2007). Structure, dynamics and functions of promyelocytic leukaemia nuclear bodies. Nat. Rev. Mol. Cell. Biol. 8, 1006-1016.
4. Billon, N., Jolicoeur, C., Ying, Q. L., Smith, A. and Raff, M. (2002). Normal timing of oligodendrocyte development from genetically engineered, lineage-selectable mouse ES cells. J. Cell Sci. 115, 3657-3665.
5. Boddy, M. N., Howe, K., Etkin, L. D., Solomon, E. and Freemont, P. S. (1996). PIC 1, a novel ubiquitin-like protein which interacts with the PML component of a multiprotein complex that is disrupted in acute promyelocytic leukaemia. Oncogene 13, 971-982.
6. Cammas, F., Mark, M., Dolle, P., Dierich, A., Chambon, P. and Losson, R. (2000). Mice lacking the transcriptional corepressor TIF1beta are defective in early postimplantation development. Development 127, 2955-2963.
7. Cammas, F., Oulad-Abdelghani, M., Vonesch, J. L., Huss-Garcia, Y., Chambon, P. and Losson, R. (2002). Cell differentiation induces TIF1beta association with centromeric heterochromatin via an HP1 interaction. J. Cell Sci. 115, 3439-3448.
8. Cammas, F., Herzog, M., Lerouge, T., Chambon, P. and Losson, R. (2004). Association of the transcriptional corepressor TIF1 beta with heterochromatin protein 1 (HP1): an essential role for progression through differentiation. Genes Dev. 18, 2147-2160.
9. Cammas, F., Janoshazi, A., Lerouge, T. and Losson, R. (2007). Dynamic and selective interactions of the transcriptional corepressor TIF1 beta with the heterochromatin protein HP1 isotypes during cell differentiation. Differentiation 75, 627-637.
10. Fleischer, S., Wiemann, S., Will, H. and Hofmann, T. G. (2006). PML-associated repressor of transcription (PAROT), a novel KRAB-zinc finger repressor, is regulated through association with PML nuclear bodies. Exp. Cell Res. 312, 901-912.
11. Friedman, J. R., Fredericks, W. J., Jensen, D. E., Speicher, D. W., Huang, X. P., Neilson, E. G. and Rauscher, F. J., 3rd (1996). KAP-1, a novel corepressor for the highly conserved KRAB repression domain. Genes Dev. 10, 2067-2078.
12. Gilbert, N., Boyle, S., Sutherland, H., de Las, H. J., Allan, J., Jenuwein, T. and Bickmore, W. A. (2003). Formation of facultative heterochromatin in the absence of HP1. EMBO J. 22, 5540-5550.
13. Gilbert, N., Thomson, I., Boyle, S., Allan, J., Ramsahoye, B. and Bickmore, W. A. (2007). DNA methylation affects nuclear organization, histone modifications, and linker histone binding but not chromatin compaction. J. Cell Biol. 177, 401-411.
14. Gilchrist, S., Gilbert, N., Perry, P. and Bickmore, W. A. (2004). Nuclear organization of centromeric domains is not perturbed by inhibition of histone deacetylases. Chromosome Res. 12, 505-516.
15. Huntley, S., Baggott, D. M., Hamilton, A. T., Tran-Gyamfi, M., Yang, S., Kim, J., Gordon, L., Branscomb, E. and Stubbs, L. (2006). A comprehensive catalog of human KRAB-associated zinc finger genes: insights into the evolutionary history of a large family of transcriptional repressors. Genome Res. 16, 669-677.
16. Ivanov, A. V., Peng, H., Yurchenko, V., Yap, K. L., Negorev, D. G., Schultz, D. C., Psulkowski, E., Fredericks, W. J., White, D. E., Maul, G. G. et al. (2007). PHD domain-mediated E3 ligase activity directs intramolecular sumoylation of an adjacent bromodomain required for gene silencing. Mol. Cell 28, 823-837.
17. Krebs, C. J., Larkins, L. K., Khan, S. M. and Robins, D. M. (2005). Expansion and diversification of KRAB zinc-finger genes within a cluster including Regulator of sex-limitation 1 and 2. Genomics 85, 752-761.
18. Lee, Y. K., Thomas, S. N., Yang, A. J. and Ann, D. K. (2007). Doxorubicin down-regulates Kruppel-associated box domain-associated protein 1 sumoylation that relieves its transcription repression on p21WAF1/CIP1 in breast cancer MCF-7 cells. J. Biol. Chem. 282, 1595-1606.
19. Lehnertz, B., Ueda, Y., Derijck, A. A., Braunschweig, U., Perez-Burgos, L., Kubicek, S., Chen, T., Li, E., Jenuwein, T. and Peters, A. H. (2003). Suv39h-mediated histone H3 lysine 9 methylation directs DNA methylation to major satellite repeats at pericentric heterochromatin. Curr. Biol. 13, 1192-1200.
20. Li, L., Roy, K., Katyal, S., Sun, X., Bleoo, S. and Godbout, R. (2006). Dynamic nature of cleavage bodies and their spatial relationship to DDX1 bodies, Cajal bodies, and gems. Mol. Biol. Cell 17, 1126-1140.
21. Li, X., Lee, Y. K., Jeng, J. C., Yen, Y., Schultz, D. C., Shih, H. M. and Ann, D. K. (2007). Role for KAP1 serine 824 phosphorylation and sumoylation/desumoylation switch in regulating KAP1-mediated transcriptional repression. J. Biol. Chem. 282, 36177-36189.
22. Mascle, X. H., Germain-Desprez, D., Huynh, P., Estephan, P. and Aubry, M. (2007). Sumoylation of the transcriptional intermediary factor 1beta (TIF1beta), the Co-repressor of the KRAB Multifinger proteins, is required for its transcriptional activity and is modulated by the KRAB domain. J. Biol. Chem. 282, 10190-10202.
23. Matsuda, E., Agata, Y., Sugai, M., Katakai, T., Gonda, H. and Shimizu, A. (2001). Targeting of Kruppel-associated box-containing zinc finger proteins to centromeric heterochromatin. Implication for the gene silencing mechanisms. J. Biol. Chem. 276, 14222-14229..
24. Matsui, Y., Zsebo, K. and Hogan, B. L. (1992). Derivation of pluripotential embryonic stem cells from murine primordial germ cells in culture. Cell 70, 841-847.
25. Meroni, G. and ez-Roux, G. (2005). TRIM/RBCC, a novel class of 'single protein RING finger' E3 ubiquitin ligases. BioEssays 27, 1147-1157.
26. Nielsen, A. L., Ortiz, J. A., You, J., Oulad-Abdelghani, M., Khechumian, R., Gansmuller, A., Chambon, P. and Losson, R. (1999). Interaction with members of the heterochromatin protein 1 (HP1) family and histone deacetylation are differentially involved in transcriptional silencing by members of the TIF1 family. EMBO J. 18, 6385-6395.
27. Nikulina, K., Bodeker, M., Warren, J., Matthews, P. and Margolis, T. P. (2006). A novel Kruppel related factor consisting of only a KRAB domain is expressed in the murine trigeminal ganglion. Biochem. Biophys. Res. Commun. 348, 839-849.
28. O'Geen, H., Squazzo, S. L., Iyengar, S., Blahnik, K., Rinn, J. L., Chang, H. Y., Green, R. and Farnham, P. J. (2007). Genome-wide analysis of KAP1 binding suggests autoregulation of KRAB-ZNFs. PLoS Genet. 3, e89.
29. Oh, H. J., Li, Y. and Lau, Y. F. (2005). Sry associates with the heterochromatin protein 1 complex by interacting with a KRAB domain protein. Biol. Reprod. 72, 407-415.
30. Okano, M., Bell, D. W., Haber, D. A. and Li, E. (1999). DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99, 247-257.
31. Payen, E., Verkerk, T., Michalovich, D., Dreyer, S. D., Winterpacht, A., Lee, B., De Zeeuw, C. I., Grosveld, F. and Galjart, N. (1998). The centromeric/nucleolar chromatin protein ZFP-37 may function to specify neuronal nuclear domains. J. Biol. Chem. 273, 9099-9109.
32. Peters, A. H., O'Carroll, D., Scherthan, H., Mechtler, K., Sauer, S., Schofer, C., Weipoltshammer, K., Pagani, M., Lachner, M., Kohlmaier, A. et al. (2001). Loss of the Suv39h histone methyltransferases impairs mammalian heterochromatin and genome stability. Cell 107, 323-337.
33. Quimby, B. B., Yong-Gonzalez, V., Anan, T., Strunnikov, A. V. and Dasso, M. (2006). The promyelocytic leukemia protein stimulates SUMO conjugation in yeast. Oncogene 25, 2999-3005.
34. Ravasi, T., Huber, T., Zavolan, M., Forrest, A., Gaasterland, T., Grimmond, S. and Hume, D. A. (2003). Systematic characterization of the zinc-finger-containing proteins in the mouse transcriptome. Genome Res. 13, 1430-1442.
35. Reymond, A., Meroni, G., Fantozzi, A., Merla, G., Cairo, S., Luzi, L., Riganelli, D., Zanaria, E., Messali, S., Cainarca, S. et al. (2001). The tripartite motif family identifies cell compartments. EMBO J. 20, 2140-2151.
36. Ryan, R. F., Schultz, D. C., Ayyanathan, K., Singh, P. B., Friedman, J. R., Fredericks, W. J. and Rauscher, F. J., 3rd (1999). KAP-1 corepressor protein interacts and colocalizes with heterochromatic and euchromatic HP1 proteins: a potential role for Kruppel-associated box-zinc finger proteins in heterochromatin-mediated gene silencing. Mol. Cell. Biol. 19, 4366-4378.
37. Schultz, D. C., Friedman, J. R. and Rauscher, F. J., 3rd (2001). Targeting histone deacetylase complexes via KRAB-zinc finger proteins: the PHD and bromodomains of KAP-1 form a cooperative unit that recruits a novel isoform of the Mi-2alpha subunit of NuRD. Genes Dev. 15, 428-443.
38. Schultz, D. C., Ayyanathan, K., Negorev, D., Maul, G. G. and Rauscher, F. J., 3rd (2002). SETDB1: a novel KAP-1-associated histone H3, lysine 9-specific methyltransferase that contributes to HP1-mediated silencing of euchromatic genes by KRAB zinc-finger proteins. Genes Dev. 16, 919-932.
39. Shannon, M., Hamilton, A. T., Gordon, L., Branscomb, E. and Stubbs, L. (2003). Differential expansion of zinc-finger transcription factor loci in homologous human and mouse gene clusters. Genome Res. 13, 1097-1110.
40. Sripathy, S. P., Stevens, J. and Schultz, D. C. (2006). The KAP1 corepressor functions to coordinate the assembly of de novo HP1-demarcated microenvironments of heterochromatin required for KRAB zinc finger protein-mediated transcriptional repression. Mol. Cell. Biol. 26, 8623-8638.
41. Sternsdorf, T., Jensen, K. and Will, H. (1997). Evidence for covalent modification of the nuclear dot-associated proteins PML and Sp100 by PIC1/SUMO-1. J. Cell Biol. 139, 1621-1634.
42. Sutherland, H. G., Mumford, G. K., Newton, K., Ford, L. V., Farrall, R., Dellaire, G., Caceres, J. F. and Bickmore, W. A. (2001). Large-scale identification of mammalian proteins localized to nuclear sub-compartments. Hum. Mol. Genet. 10, 1995-2011.
43. Sutherland, H. G., Lam, Y. W., Briers, S., Lamond, A. I. and Bickmore, W. A. (2004). 3D3/lyric: a novel transmembrane protein of the endoplasmic reticulum and nuclear envelope, which is also present in the nucleolus. Exp. Cell Res. 294, 94-105.
44. Tanaka, K., Tsumaki, N., Kozak, C. A., Matsumoto, Y., Nakatani, F., Iwamoto, Y. and Yamada, Y. (2002). A Kruppel-associated box-zinc finger protein, NT2, represses cell-type-specific promoter activity of the alpha 2(XI) collagen gene. Mol. Cell. Biol. 22, 4256-4267.
45. Urrutia, R. (2003). KRAB-containing zinc-finger repressor proteins. Genome Biol. 4, 231.
46. Vertegaal, A. C., Andersen, J. S., Ogg, S. C., Hay, R. T., Mann, M. and Lamond, A. I. (2006). Distinct and overlapping sets of SUMO-1 and SUMO-2 target proteins revealed by quantitative proteomics. Mol. Cell Proteomics. 5, 2298-2310.
47. White, D. E., Negorev, D., Peng, H., Ivanov, A. V., Maul, G. G. and Rauscher, F. J., 3rd (2006). KAP1, a novel substrate for PIKK family members, colocalizes with numerous damage response factors at DNA lesions. Cancer Res. 66, 11594-11599.
48. Zhang, R., Poustovoitov, M. V., Ye, X., Santos, H. A., Chen, W., Daganzo, S. M., Erzberger, J. P., Serebriiskii, I. G., Canutescu, A. A., Dunbrack, R. L. et al. (2005). Formation of MacroH2A-containing senescence-associated heterochromatin foci and senescence driven by ASF1a and HIRA. Dev. Cell 8, 19-30.
49. Zhong, S., Muller, S., Ronchetti, S., Freemont, P. S., Dejean, A. and Pandolfi, P. P. (2000). Role of SUMO-1-modified PML in nuclear body formation. Blood 95, 2748-2752.