Zfp819, a novel KRAB-zinc finger protein, interacts with KAP1 and functions in genomic integrity maintenance of mouse embryonic stem cells

Stem Cell Research

Volumn 11, Issue 3, 2013, Pages 1045-1059

  Tan, Xiaoying ^a   Xu, Xingbo ^a   Elkenani, Manar ^a   Smorag, Lukasz ^a   Zechner, Ulrich ^b   Nolte, Jessica ^a   Engel, Wolfgang ^a   Pantakani, D V Krishna ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

ERVs; ESCs; IAP; KD; KRAB; LINE; OE; Zfp819

Indexed keywords

KAP1 PROTEIN; OCTAMER TRANSCRIPTION FACTOR 4; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG; ZFP819 PROTEIN; ZINC FINGER PROTEIN;

ANIMAL CELL; ARTICLE; DNA DAMAGE; DNA METHYLATION; EMBRYONIC STEM CELL; IMMUNOPRECIPITATION; IN VITRO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RETROPOSON; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

EMBRYONIC STEM CELLS; ENDOGENOUS RETROVIRUSES; ERVS; ESCS; IAP; INTRACISTERNAL A PARTICLE; KD; KNOCKDOWN; KRAB; KRÜPPEL ASSOCIATED BOX; LINE; LONG INTERSPERSED NUCLEAR ELEMENTS; OE; OVEREXPRESSION; ZFP819; ZINC FINGER PROTEIN 819;

AMINO ACID SEQUENCE; ANIMALS; CARRIER PROTEINS; CELL DIFFERENTIATION; CELL LINE; CELL NUCLEUS; DNA DAMAGE; EMBRYONIC STEM CELLS; HISTONES; HOMEODOMAIN PROTEINS; MICE; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; OCTAMER TRANSCRIPTION FACTOR-3; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; REPRESSOR PROTEINS; RNA, SMALL INTERFERING; SOXB1 TRANSCRIPTION FACTORS; UP-REGULATION;

EID: 84882800012     PISSN: 18735061     EISSN: 18767753     Source Type: Journal    
DOI: 10.1016/j.scr.2013.07.006     Document Type: Article

References (67)

1. Bartova E., Sustackova G., Stixova L., Kozubek S., Legartova S., Foltankova V. Recruitment of Oct4 protein to UV-damaged chromatin in embryonic stem cells. PLoS One 2011, 6:e27281.
2. Bellefroid E.J., Poncelet D.A., Lecocq P.J., Revelant O., Martial J.A. The evolutionarily conserved Kruppel-associated box domain defines a subfamily of eukaryotic multifingered proteins. Proc. Natl. Acad. Sci. U. S. A. 1991, 88:3608-3612.
3. Bernstein B.E., Mikkelsen T.S., Xie X., Kamal M., Huebert D.J., Cuff J., Fry B., Meissner A., Wernig M., Plath K., Jaenisch R., Wagschal A., Feil R., Schreiber S.L., Lander E.S. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 2006, 125:315-326.
4. Boyer L.A., Lee T.I., Cole M.F., Johnstone S.E., Levine S.S., Zucker J.P., Guenther M.G., Kumar R.M., Murray H.L., Jenner R.G., Gifford D.K., Melton D.A., Jaenisch R., Young R.A. Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 2005, 122:947-956.
5. Burnicka-Turek O., Kata A., Buyandelger B., Ebermann L., Kramann N., Burfeind P., Hoyer-Fender S., Engel W., Adham I.M. Pelota interacts with HAX1, EIF3G and SRPX and the resulting protein complexes are associated with the actin cytoskeleton. BMC Cell Biol. 2010, 11:28.
6. Cammas F., Mark M., Dolle P., Dierich A., Chambon P., Losson R. Mice lacking the transcriptional corepressor TIF1beta are defective in early postimplantation development. Development 2000, 127:2955-2963.
7. Cammas F., Oulad-Abdelghani M., Vonesch J.L., Huss-Garcia Y., Chambon P., Losson R. Cell differentiation induces TIF1beta association with centromeric heterochromatin via an HP1 interaction. J. Cell Sci. 2002, 115:3439-3448.
8. Cammas F., Herzog M., Lerouge T., Chambon P., Losson R. Association of the transcriptional corepressor TIF1beta with heterochromatin protein 1 (HP1): an essential role for progression through differentiation. Genes Dev. 2004, 18:2147-2160.
9. Chen X., Xu H., Yuan P., Fang F., Huss M., Vega V.B., Wong E., Orlov Y.L., Zhang W., Jiang J., Loh Y.H., Yeo H.C., Yeo Z.X., Narang V., Govindarajan K.R., Leong B., Shahab A., Ruan Y., Bourque G., Sung W.K., Clarke N.D., Wei C.L., Ng H.H. Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell 2008, 133:1106-1117.
10. Collins T., Stone J.R., Williams A.J. All in the family: the BTB/POZ, KRAB, and SCAN domains. Mol. Cell. Biol. 2001, 21:3609-3615.
11. Dejosez M., Zwaka T.P. Pluripotency and nuclear reprogramming. Annu. Rev. Biochem. 2012, 81:737-765.
12. Doi A., Park I.H., Wen B., Murakami P., Aryee M.J., Irizarry R., Herb B., Ladd-Acosta C., Rho J., Loewer S., Miller J., Schlaeger T., Daley G.Q., Feinberg A.P. Differential methylation of tissue- and cancer-specific CpG island shores distinguishes human induced pluripotent stem cells, embryonic stem cells and fibroblasts. Nat. Genet. 2009, 41:1350-1353.
13. Eiges R., Schuldiner M., Drukker M., Yanuka O., Itskovitz-Eldor J., Benvenisty N. Establishment of human embryonic stem cell-transfected clones carrying a marker for undifferentiated cells. Curr. Biol. 2001, 11:514-518.
14. Fong Y.W., Inouye C., Yamaguchi T., Cattoglio C., Grubisic I., Tjian R. A DNA repair complex functions as an Oct4/Sox2 coactivator in embryonic stem cells. Cell 2011, 147:120-131.
15. Friedman J.R., Fredericks W.J., Jensen D.E., Speicher D.W., Huang X.P., Neilson E.G., Rauscher F.J. KAP-1, a novel corepressor for the highly conserved KRAB repression domain. Genes Dev. 1996, 10:2067-2078.
16. Germain-Desprez D., Bazinet M., Bouvier M., Aubry M. Oligomerization of transcriptional intermediary factor 1 regulators and interaction with ZNF74 nuclear matrix protein revealed by bioluminescence resonance energy transfer in living cells. J. Biol. Chem. 2003, 278:22367-22373.
17. Gietz R.D., Schiestl R.H., Willems A.R., Woods R.A. Studies on the transformation of intact yeast cells by the LiAc/SS-DNA/PEG procedure. Yeast 1995, 11:355-360.
18. Hu G., Kim J., Xu Q., Leng Y., Orkin S.H., Elledge S.J. A genome-wide RNAi screen identifies a new transcriptional module required for self-renewal. Genes Dev. 2009, 23:837-848.
19. Hu C., Zhang S., Gao X., Gao X., Xu X., Lv Y., Zhang Y., Zhu Z., Zhang C., Li Q., Wong J., Cui Y., Zhang W., Ma L., Wang C. Roles of Kruppel-associated box (KRAB)-associated co-repressor KAP1 Ser-473 phosphorylation in DNA damage response. J. Biol. Chem. 2012, 287:18937-18952.
20. Ivanova N., Dobrin R., Lu R., Kotenko I., Levorse J., DeCoste C., Schafer X., Lun Y., Lemischka I.R. Dissecting self-renewal in stem cells with RNA interference. Nature 2006, 442:533-538.
21. Kim J., Chu J., Shen X., Wang J., Orkin S.H. An extended transcriptional network for pluripotency of embryonic stem cells. Cell 2008, 132:1049-1061.
22. Khromov T., Pantakani D.V., Nolte J., Wolf M., Dressel R., Engel W., Zechner U. Global and gene-specific histone modification profiles of mouse multipotent adult germline stem cells. Mol. Hum. Reprod. 2011, 17:166-174.
23. Lai A.Y., Wade P.A. Cancer biology and NuRD: a multifaceted chromatin remodelling complex. Nat. Rev. Cancer 2011, 11:588-596.
24. Lander E.S., Linton L.M., Birren B., Nusbaum C., Zody M.C., Baldwin J., Devon K., Dewar K., Doyle M., FitzHugh W., et al. Initial sequencing and analysis of the human genome. Nature 2001, 409:860-921.
25. Larsen D.H., Poinsignon C., Gudjonsson T., Dinant C., Payne M.R., Hari F.J., Rendtlew Danielsen J.M., Menard P., Sand J.C., Stucki M., Lukas C., Bartek J., Andersen J.S., Lukas J. The chromatin-remodeling factor CHD4 coordinates signaling and repair after DNA damage. J. Cell Biol. 2010, 190:731-740.
26. Lee B.J., Cansizoglu A.E., Suel K.E., Louis T.H., Zhang Z., Chook Y.M. Rules for nuclear localization sequence recognition by karyopherin beta 2. Cell 2006, 126:543-558.
27. Li X., Lee Y.K., Jeng J.C., Yen Y., Schultz D.C., Shih H.M., Ann D.K. Role for KAP1 serine 824 phosphorylation and sumoylation/desumoylation switch in regulating KAP1-mediated transcriptional repression. J. Biol. Chem. 2007, 282:36177-36189.
28. Li X., Lin H.H., Chen H., Xu X., Shih H.M., Ann D.K. SUMOylation of the transcriptional co-repressor KAP1 is regulated by the serine and threonine phosphatase PP1. Sci. Signal. 2010, 3:ra32.
29. Lin T., Chao C., Saito S., Mazur S.J., Murphy M.E., Appella E., Xu Y. p53 induces differentiation of mouse embryonic stem cells by suppressing Nanog expression. Nat. Cell Biol. 2005, 7:165-171.
30. Loh Y.H., Wu Q., Chew J.L., Vega V.B., Zhang W., Chen X., Bourque G., George J., Leong B., Liu J., Wong K.Y., Sung K.W., Lee C.W., Zhao X.D., Chiu K.P., Lipovich L., Kuznetsov V.A., Robson P., Stanton L.W., Wei C.L., Ruan Y., Lim B., Ng H.H. The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells. Nat. Genet. 2006, 38:431-440.
31. Looman C., Abrink M., Mark C., Hellman L. KRAB zinc finger proteins: an analysis of the molecular mechanisms governing their increase in numbers and complexity during evolution. Mol. Biol. Evol. 2002, 19:2118-2130.
32. Maksakova I.A., Romanish M.T., Gagnier L., Dunn C.A., van de Lagemaat L.N., Mager D.L. Retroviral elements and their hosts: insertional mutagenesis in the mouse germ line. PLoS Genet. 2006, 2:e2.
33. Marson A., Levine S.S., Cole M.F., Frampton G.M., Brambrink T., Johnstone S., Guenther M.G., Johnston W.K., Wernig M., Newman J., Calabrese J.M., Dennis L.M., Volkert T.L., Gupta S., Love J., Hannett N., Sharp P.A., Bartel D.P., Jaenisch R., Young R.A. Connecting microRNA genes to the core transcriptional regulatory circuitry of embryonic stem cells. Cell 2008, 134:521-533.
34. Meshorer E. Chromatin in embryonic stem cell neuronal differentiation. Histol. Histopathol. 2007, 22:311-319.
35. Meshorer E., Misteli T. Chromatin in pluripotent embryonic stem cells and differentiation. Nat. Rev. Mol. Cell Biol. 2006, 7:540-546.
36. Meyer S., Nolte J., Opitz L., Salinas-Riester G., Engel W. Pluripotent embryonic stem cells and multipotent adult germline stem cells reveal similar transcriptomes including pluripotency-related genes. Mol. Hum. Reprod. 2010, 16:846-855.
37. Mikkelsen T.S., Ku M., Jaffe D.B., Issac B., Lieberman E., Giannoukos G., Alvarez P., Brockman W., Kim T.K., Koche R.P., Lee W., Mendenhall E., O'Donovan A., Presser A., Russ C., Xie X., Meissner A., Wernig M., Jaenisch R., Nusbaum C., Lander E.S., Bernstein B.E. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 2007, 448:553-560.
38. Mitsui K., Tokuzawa Y., Itoh H., Segawa K., Murakami M., Takahashi K., Maruyama M., Maeda M., Yamanaka S. The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 2003, 113:631-642.
39. Ng H.H., Surani M.A. The transcriptional and signalling networks of pluripotency. Nat. Cell Biol. 2011, 13:490-496.
40. Nishii T., Oikawa Y., Ishida Y., Kawaichi M., Matsuda E. CtBP-interacting BTB zinc finger protein (CIBZ) promotes proliferation and G1/S transition in embryonic stem cells via Nanog. J. Biol. Chem. 2012, 287:12417-12424.
41. Pan G., Tian S., Nie J., Yang C., Ruotti V., Wei H., Jonsdottir G.A., Stewart R., Thomson J.A. Whole-genome analysis of histone H3 lysine 4 and lysine 27 methylation in human embryonic stem cells. Cell Stem Cell 2007, 1:299-312.
42. Peng H., Begg G.E., Harper S.L., Friedman J.R., Speicher D.W., Rauscher F.J. Biochemical analysis of the Kruppel-associated box (KRAB) transcriptional repression domain. J. Biol. Chem. 2000, 275:18000-18010.
43. Peng H., Feldman I., Rauscher F.J. Hetero-oligomerization among the TIF family of RBCC/TRIM domain-containing nuclear cofactors: a potential mechanism for regulating the switch between coactivation and corepression. J. Mol. Biol. 2002, 320:629-644.
44. Rosati M., Marino M., Franze A., Tramontano A., Grimaldi G. Members of the zinc finger protein gene family sharing a conserved N-terminal module. Nucleic Acids Res. 1991, 19:5661-5667.
45. Rowe H.M., Jakobsson J., Mesnard D., Rougemont J., Reynard S., Aktas T., Maillard P.V., Layard-Liesching H., Verp S., Marquis J., Spitz F., Constam D.B., Trono D. KAP1 controls endogenous retroviruses in embryonic stem cells. Nature 2010, 463:237-240.
46. Seki Y., Kurisaki A., Watanabe-Susaki K., Nakajima Y., Nakanishi M., Arai Y., Shiota K., Sugino H., Asashima M. TIF1beta regulates the pluripotency of embryonic stem cells in a phosphorylation-dependent manner. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:10926-10931.
47. Smeenk G., Wiegant W.W., Vrolijk H., Solari A.P., Pastink A., van Attikum H. The NuRD chromatin-remodeling complex regulates signaling and repair of DNA damage. J. Cell Biol. 2010, 190:741-749.
48. Smorag L., Zheng Y., Nolte J., Zechner U., Engel W., Pantakani D.V. MicroRNA signature in various cell types of mouse spermatogenesis: evidence for stage-specifically expressed miRNA-221, -203, and -34b-5p mediated spermatogenesis regulation. Biol. Cell 2012, 104:677-692.
49. Sridharan R., Tchieu J., Mason M.J., Yachechko R., Kuoy E., Horvath S., Zhou Q., Plath K. Role of the murine reprogramming factors in the induction of pluripotency. Cell 2009, 136:364-377.
50. Urquhart A.J., Gatei M., Richard D.J., Khanna K.K. ATM mediated phosphorylation of CHD4 contributes to genome maintenance. Genome Integr. 2011, 2:1.
51. Urrutia R. KRAB-containing zinc-finger repressor proteins. Genome Biol. 2003, 4:231.
52. Walsh C.P., Chaillet J.R., Bestor T.H. Transcription of IAP endogenous retroviruses is constrained by cytosine methylation. Nat. Genet. 1998, 20:116-117.
53. Wang Z.X., Kueh J.L., Teh C.H., Rossbach M., Lim L., Li P., Wong K.Y., Lufkin T., Robson P., Stanton L.W. Zfp206 is a transcription factor that controls pluripotency of embryonic stem cells. Stem Cells 2007, 25:2173-2182.
54. Wang Z.X., Teh C.H., Chan C.M., Chu C., Rossbach M., Kunarso G., Allapitchay T.B., Wong K.Y., Stanton L.W. The transcription factor Zfp281 controls embryonic stem cell pluripotency by direct activation and repression of target genes. Stem Cells 2008, 26:2791-2799.
55. White D.E., Negorev D., Peng H., Ivanov A.V., Maul G.G., Rauscher F.J. KAP1, a novel substrate for PIKK family members, colocalizes with numerous damage response factors at DNA lesions. Cancer Res. 2006, 66:11594-11599.
56. Witzgall R., O'Leary E., Leaf A., Onaldi D., Bonventre J.V. The Kruppel-associated box-A (KRAB-A) domain of zinc finger proteins mediates transcriptional repression. Proc. Natl. Acad. Sci. U. S. A. 1994, 91:4514-4518.
57. Wolf D., Goff S.P. Embryonic stem cells use ZFP809 to silence retroviral DNAs. Nature 2009, 458:1201-1204.
58. Wolfe S.A., Nekludova L., Pabo C.O. DNA recognition by Cys2His2 zinc finger proteins. Annu. Rev. Biophys. Biomol. Struct. 2000, 29:183-212.
59. Yu H.B., Kunarso G., Hong F.H., Stanton L.W. Zfp206, Oct4, and Sox2 are integrated components of a transcriptional regulatory network in embryonic stem cells. J. Biol. Chem. 2009, 284:31327-31335.
60. Zechner U., Nolte J., Wolf M., Shirneshan K., Hajj N.E., Weise D., Kaltwasser B., Zovoilis A., Haaf T., Engel W. Comparative methylation profiles and telomerase biology of mouse multipotent adult germline stem cells and embryonic stem cells. Mol. Hum. Reprod. 2009, 15:345-353.
61. Zhang J., Tam W.L., Tong G.Q., Wu Q., Chan H.Y., Soh B.S., Lou Y., Yang J., Ma Y., Chai L., Ng H.H., Lufkin T., Robson P., Lim B. Sall4 modulates embryonic stem cell pluripotency and early embryonic development by the transcriptional regulation of Pou5f1. Nat. Cell Biol. 2006, 8:1114-1123.
62. Zhang W., Walker E., Tamplin O.J., Rossant J., Stanford W.L., Hughes T.R. Zfp206 regulates ES cell gene expression and differentiation. Nucleic Acids Res. 2006, 34:4780-4790.
63. Zhang J.Z., Gao W., Yang H.B., Zhang B., Zhu Z.Y., Xue Y.F. Screening for genes essential for mouse embryonic stem cell self-renewal using a subtractive RNA interference library. Stem Cells 2006, 24:2661-2668.
64. Zhang X., Zhang J., Wang T., Esteban M.A., Pei D. Esrrb activates Oct4 transcription and sustains self-renewal and pluripotency in embryonic stem cells. J. Biol. Chem. 2008, 283:35825-35833.
65. Zheng Y., Tan X., Pyczek J., Nolte J., Pantakani D.V., Engel W. Generation and characterization of yeast two-hybrid cDNA libraries derived from two distinct mouse pluripotent cell types. Mol. Biotechnol. 2012, 54:228-237.
66. Ziv Y., Bielopolski D., Galanty Y., Lukas C., Taya Y., Schultz D.C., Lukas J., Bekker-Jensen S., Bartek J., Shiloh Y. Chromatin relaxation in response to DNA double-strand breaks is modulated by a novel ATM- and KAP-1 dependent pathway. Nat. Cell Biol. 2006, 8:870-876.
67. Zuo X., Sheng J., Lau H.T., McDonald C.M., Andrade M., Cullen D.E., Bell F.T., Iacovino M., Kyba M., Xu G., Li X. Zinc finger protein ZFP57 requires its co-factor to recruit DNA methyltransferases and maintains DNA methylation imprint in embryonic stem cells via its transcriptional repression domain. J. Biol. Chem. 2011, 287:2107-2118.