137. Xie S, Jakoncic J, Qian C (2012) UHRF1 double tudor domain and the adjacent PHD finger
act together to recognize K9me3-containing histone H3 tail. J Mol Biol 415(2):318–328.
https://doi.org/10.1016/j.jmb.2011.11.012
138. Franz H, Greschik H, Willmann D, Ozretic L, Jilg CA, Wardelmann E, Jung M, Buettner R,
Schule R (2015) The histone code reader SPIN1 controls RET signaling in liposarcoma.
Oncotarget 6(7):4773–4789. https://doi.org/10.18632/oncotarget.3000
139. Wang W, Chen Z, Mao Z, Zhang H, Ding X, Chen S, Zhang X, Xu R, Zhu B (2011) Nucleolar
protein Spindlin1 recognizes H3K4 methylation and stimulates the expression of rRNA genes.
EMBO Rep 12(11):1160–1166. https://doi.org/10.1038/embor.2011.184
140. Oh B, Hwang SY, Solter D, Knowles BB (1997) Spindlin, a major maternal transcript
expressed in the mouse during the transition from oocyte to embryo. Development
124(2):493–503
141. Yue W, Sun LY, Li CH, Zhang LX, Pei XT (2004) Screening and identification of ovarian
carcinomas related genes. Ai Zheng 23(2):141–145
142. Wang JX, Zeng Q, Chen L, Du JC, Yan XL, Yuan HF, Zhai C, Zhou JN, Jia YL, Yue W,
Pei XT (2012) SPINDLIN1 promotes cancer cell proliferation through activation of WNT/
TCF-4 signaling. Mol Cancer Res 10(3):326–335. https://doi.org/10.1158/1541-7786.MCR11-0440
143. Zhang P, Cong B, Yuan H, Chen L, Lv Y, Bai C, Nan X, Shi S, Yue W, Pei X (2008)
Overexpression of spindlin1 induces metaphase arrest and chromosomal instability. J Cell
Physiol 217(2):400–408. https://doi.org/10.1002/jcp.21515
144. Zhao Q, Qin L, Jiang F, Wu B, Yue W, Xu F, Rong Z, Yuan H, Xie X, Gao Y, Bai C,
Bartlam M, Pei X, Rao Z (2007) Structure of human spindlin1. Tandem tudor-like domains for
cell cycle regulation. J Biol Chem 282(1):647–656. https://doi.org/10.1074/jbc.M604029200
145. Su X, Zhu G, Ding X, Lee SY, Dou Y, Zhu B, Wu W, Li H (2014) Molecular basis underlying
histone H3 lysine-arginine methylation pattern readout by Spin/Ssty repeats of Spindlin1.
Genes Dev 28(6):622–636. https://doi.org/10.1101/gad.233239.113
146. Perfetti MT, Baughman BM, Dickson BM, Mu Y, Cui G, Mader P, Dong A, Norris JL,
Rothbart SB, Strahl BD, Brown PJ, Janzen WP, Arrowsmith CH, Mer G, McBride KM,
James LI, Frye SV (2015) Identification of a fragment-like small molecule ligand for the
methyl-lysine binding protein, 53BP1. ACS Chem Biol 10(4):1072–1081. https://doi.org/10.
1021/cb500956g
147. Fradet-Turcotte A, Canny MD, Escribano-Diaz C, Orthwein A, Leung CC, Huang H,
Landry MC, Kitevski-LeBlanc J, Noordermeer SM, Sicheri F, Durocher D (2013) 53BP1 is
a reader of the DNA-damage-induced H2A Lys 15 ubiquitin mark. Nature 499(7456):50–54.
https://doi.org/10.1038/nature12318
148. Gelato KA, Tauber M, Ong MS, Winter S, Hiragami-Hamada K, Sindlinger J, Lemak A,
Bultsma Y, Houliston S, Schwarzer D, Divecha N, Arrowsmith CH, Fischle W (2014)
Accessibility of different histone H3-binding domains of UHRF1 is allosterically regulated
by phosphatidylinositol 5-phosphate. Mol Cell 54(6):905–919. https://doi.org/10.1016/j.
molcel.2014.04.004
149. Fang J, Cheng J, Wang J, Zhang Q, Liu M, Gong R, Wang P, Zhang X, Feng Y, Lan W,
Gong Z, Tang C, Wong J, Yang H, Cao C, Xu Y (2016) Hemi-methylated DNA opens a closed
conformation of UHRF1 to facilitate its histone recognition. Nat Commun 7:11197. https://
doi.org/10.1038/ncomms11197
150. Harrison JS, Cornett EM, Goldfarb D, DaRosa PA, Li ZM, Yan F, Dickson BM, Guo AH,
Cantu DV, Kaustov L, Brown PJ, Arrowsmith CH, Erie DA, Major MB, Klevit RE,
Krajewski K, Kuhlman B, Strahl BD, Rothbart SB (2016) Hemi-methylated DNA regulates
DNA methylation inheritance through allosteric activation of H3 ubiquitylation by UHRF1.
eLife 5:e17101. https://doi.org/10.7554/eLife.17101
151. Houliston RS, Lemak A, Iqbal A, Ivanochko D, Duan S, Kaustov L, Ong MS, Fan L,
Senisterra G, Brown PJ, Wang YX, Arrowsmith CH (2017) Conformational dynamics
of the TTD-PHD histone reader module of the UHRF1 epigenetic regulator reveals
multiple histone-binding states, allosteric regulation, and druggability. J Biol Chem
292(51):20947–20959. https://doi.org/10.1074/jbc.M117.799700
392
G. Sbardella
act together to recognize K9me3-containing histone H3 tail. J Mol Biol 415(2):318–328.
https://doi.org/10.1016/j.jmb.2011.11.012
138. Franz H, Greschik H, Willmann D, Ozretic L, Jilg CA, Wardelmann E, Jung M, Buettner R,
Schule R (2015) The histone code reader SPIN1 controls RET signaling in liposarcoma.
Oncotarget 6(7):4773–4789. https://doi.org/10.18632/oncotarget.3000
139. Wang W, Chen Z, Mao Z, Zhang H, Ding X, Chen S, Zhang X, Xu R, Zhu B (2011) Nucleolar
protein Spindlin1 recognizes H3K4 methylation and stimulates the expression of rRNA genes.
EMBO Rep 12(11):1160–1166. https://doi.org/10.1038/embor.2011.184
140. Oh B, Hwang SY, Solter D, Knowles BB (1997) Spindlin, a major maternal transcript
expressed in the mouse during the transition from oocyte to embryo. Development
124(2):493–503
141. Yue W, Sun LY, Li CH, Zhang LX, Pei XT (2004) Screening and identification of ovarian
carcinomas related genes. Ai Zheng 23(2):141–145
142. Wang JX, Zeng Q, Chen L, Du JC, Yan XL, Yuan HF, Zhai C, Zhou JN, Jia YL, Yue W,
Pei XT (2012) SPINDLIN1 promotes cancer cell proliferation through activation of WNT/
TCF-4 signaling. Mol Cancer Res 10(3):326–335. https://doi.org/10.1158/1541-7786.MCR11-0440
143. Zhang P, Cong B, Yuan H, Chen L, Lv Y, Bai C, Nan X, Shi S, Yue W, Pei X (2008)
Overexpression of spindlin1 induces metaphase arrest and chromosomal instability. J Cell
Physiol 217(2):400–408. https://doi.org/10.1002/jcp.21515
144. Zhao Q, Qin L, Jiang F, Wu B, Yue W, Xu F, Rong Z, Yuan H, Xie X, Gao Y, Bai C,
Bartlam M, Pei X, Rao Z (2007) Structure of human spindlin1. Tandem tudor-like domains for
cell cycle regulation. J Biol Chem 282(1):647–656. https://doi.org/10.1074/jbc.M604029200
145. Su X, Zhu G, Ding X, Lee SY, Dou Y, Zhu B, Wu W, Li H (2014) Molecular basis underlying
histone H3 lysine-arginine methylation pattern readout by Spin/Ssty repeats of Spindlin1.
Genes Dev 28(6):622–636. https://doi.org/10.1101/gad.233239.113
146. Perfetti MT, Baughman BM, Dickson BM, Mu Y, Cui G, Mader P, Dong A, Norris JL,
Rothbart SB, Strahl BD, Brown PJ, Janzen WP, Arrowsmith CH, Mer G, McBride KM,
James LI, Frye SV (2015) Identification of a fragment-like small molecule ligand for the
methyl-lysine binding protein, 53BP1. ACS Chem Biol 10(4):1072–1081. https://doi.org/10.
1021/cb500956g
147. Fradet-Turcotte A, Canny MD, Escribano-Diaz C, Orthwein A, Leung CC, Huang H,
Landry MC, Kitevski-LeBlanc J, Noordermeer SM, Sicheri F, Durocher D (2013) 53BP1 is
a reader of the DNA-damage-induced H2A Lys 15 ubiquitin mark. Nature 499(7456):50–54.
https://doi.org/10.1038/nature12318
148. Gelato KA, Tauber M, Ong MS, Winter S, Hiragami-Hamada K, Sindlinger J, Lemak A,
Bultsma Y, Houliston S, Schwarzer D, Divecha N, Arrowsmith CH, Fischle W (2014)
Accessibility of different histone H3-binding domains of UHRF1 is allosterically regulated
by phosphatidylinositol 5-phosphate. Mol Cell 54(6):905–919. https://doi.org/10.1016/j.
molcel.2014.04.004
149. Fang J, Cheng J, Wang J, Zhang Q, Liu M, Gong R, Wang P, Zhang X, Feng Y, Lan W,
Gong Z, Tang C, Wong J, Yang H, Cao C, Xu Y (2016) Hemi-methylated DNA opens a closed
conformation of UHRF1 to facilitate its histone recognition. Nat Commun 7:11197. https://
doi.org/10.1038/ncomms11197
150. Harrison JS, Cornett EM, Goldfarb D, DaRosa PA, Li ZM, Yan F, Dickson BM, Guo AH,
Cantu DV, Kaustov L, Brown PJ, Arrowsmith CH, Erie DA, Major MB, Klevit RE,
Krajewski K, Kuhlman B, Strahl BD, Rothbart SB (2016) Hemi-methylated DNA regulates
DNA methylation inheritance through allosteric activation of H3 ubiquitylation by UHRF1.
eLife 5:e17101. https://doi.org/10.7554/eLife.17101
151. Houliston RS, Lemak A, Iqbal A, Ivanochko D, Duan S, Kaustov L, Ong MS, Fan L,
Senisterra G, Brown PJ, Wang YX, Arrowsmith CH (2017) Conformational dynamics
of the TTD-PHD histone reader module of the UHRF1 epigenetic regulator reveals
multiple histone-binding states, allosteric regulation, and druggability. J Biol Chem
292(51):20947–20959. https://doi.org/10.1074/jbc.M117.799700
392
G. Sbardella