KRAB型锌指蛋白的进化及在物种演化中的功能

doi:10.16288/j.yczz.16-056

遗传 ›› 2016, Vol. 38 ›› Issue (11): 971-978.doi: 10.16288/j.yczz.16-056

KRAB型锌指蛋白的进化及在物种演化中的功能

王进龙, 王建, 田春艳

军事医学科学院放射与辐射医学研究所,国家蛋白质科学中心(北京),国家蛋白质组学重点实验室,蛋白质药家工程研究中心,北京 102206

收稿日期:2016-06-07 出版日期:2016-11-20 发布日期:2016-09-09
通讯作者: 王建,博士,副研究员,研究方向：蛋白质相互作用、炎症与免疫调控。E-mail: wangj@bmi.ac.cn;田春艳,博士,副研究员,研究方向：基因的转录调控。E-mail: tiancy@bmi.ac.cn
作者简介:王进龙,硕士研究生,专业方向：生物化学与分子生物学。E-mail: wang993476@163.com
基金资助:
国家自然科学基金项目(编号：31270799),北京市自然科学基金项目(编号：5142019)和国家国际科技合作专项项目(编号：2014DFB30020)资助

Evolution of KRAB-containing zinc finger proteins and their roles in species evolution

Jinlong Wang, Jian Wang, Chunyan Tian

State Key Laboratory of Proteomics, National Center for Proteomics Science (Beijing), China National Engineering Research Center for Protein Drugs, Beijing Institute of Radiation Medicine, Beijing 102206, China

Received:2016-06-07 Online:2016-11-20 Published:2016-09-09
Supported by:
[Supported by the National Natural Science Foundation of China(No. 31270799), Beijing Municipal Natural Science Foundation(No. 5142019) and International Science & Technology Cooperation Program of China(No. 2014DFB30020)]

摘要/Abstract

摘要： C2H2型锌指蛋白家族是目前发现的哺乳动物中最大的转录/转录调控因子家族,由一小群古老的含有真核锌指结构的转录因子经过多次基因复制和功能分化演化而来。KRAB型锌指蛋白(KRAB-containing zinc finger proteins, KRAB-ZFPs)作为C2H2型锌指蛋白家族中最大的亚家族,最早出现在四足脊椎动物,并随物种的进化数量快速增长,在人类中占据C2H2型锌指蛋白的60%左右。在物种演化中,进化压力主要改变KRAB-ZFPs的DNA结合能力,而KRAB-ZFPs介导的转录抑制能力则稳定存在。同时,多种KRAB-ZFPs能够与KRAB相关蛋白1(KRAB-associated protein 1, KAP1)协同作用沉默哺乳动物中反转录元件的活性,并与之协同进化,严格限制反转录原件的跳跃能力。本文综述了KRAB-ZFPs的数量倍增、锌指结构的灵活多变、KRAB-ZFPs/KAP1的转录抑制能力和反转录元件的跳跃性在促进哺乳动物调控网络的差异、基因组稳定性的变化和物种进化中的作用,旨在进一步揭示KRAB-ZFPs在推动物种稳定演化中的特点和功能。

关键词: KRAB, 锌指, KRAB-ZFPs, 进化, KAP1, 转座子

Abstract: The C2H2 zinc finger protein family, one of the largest families of transcription factor/transcriptional regulator in mammal, arose from a small ancestral group of eukaryotic zinc finger transcription factors through many repeated gene duplications accompanied by functional divergence. As the biggest subfamily of C2H2 zinc finger protein family, Kruppel-associated box-containing zinc finger proteins (KRAB-ZFPs) appeared at the period oftetrapod, expand rapidly along with species evolution, and take about 60% of the total C2H2 zinc finger proteins in human. During species evolution, the DNA binding ability of KRAB-ZFPs is changed while the KRAB-ZFPs-mediate transcriptional repression ability maintains stable under the evolution pressure. Moreover, multiple KRAB-ZFPs function synergistically with KAP1 on transcriptional silencing of retroelements, and the coevolution between KRAB-ZFPs and target retrotransposons restrict the jumping ability of the retroelements. In this review, we summarize the roles of KRAB-ZFPs duplication, the flexibility of zinc finger structure, transcriptional repression of KRAB-ZFPs/KAP1 and retroelement “jump” in promoting the divergence in regulatory network, stable genome change and species evolution, in order to reveal the characters and functions of KRAB-ZFPs in driving species evolution stably.

Key words: KRAB, zinc finger, KRAB-ZFPs, evolution, KAP1, transposons

王进龙, 王建, 田春艳. KRAB型锌指蛋白的进化及在物种演化中的功能[J]. 遗传, 2016, 38(11): 971-978.

Jinlong Wang, Jian Wang, Chunyan Tian. Evolution of KRAB-containing zinc finger proteins and their roles in species evolution[J]. Hereditas(Beijing), 2016, 38(11): 971-978.

参考文献

[1] Collins T, Stone JR, Williams AJ. All in the family: the BTB/POZ, KRAB, and SCAN domains. Mol Cell Biol , 2001, 21(11): 3609-3615.
[2] Stubbs L, Sun Y, Caetano-Anolles D. Function and evolution of C 2 H 2 zinc finger arrays. Subcell Biochem , 2011, 52: 75-94.
[3] Emerson RO, Thomas JH. Adaptive evolution in zinc finger transcription factors. PLoS Genet , 2009, 5(1): e1000325.
[4] Tadepally HD, Burger G, Aubry M. Evolution of C 2 H 2 - zinc finger genes and subfamilies in mammals: species-specific duplication and loss of clusters, genes and effector domains. BMC Evol Biol , 2008, 8: 176.
[5] Tian CY, Zhang LQ, He FC. Progress in the study of KRAB zinc finger protein. Hereditas ( Beijing ), 2006, 28(11): 1451-1456. 田春艳, 张令强, 贺福初. KRAB型锌指蛋白(KZNF)的研究进展. 遗传, 2006, 28(11): 1451-1456.
[6] Schultz DC, Ayyanathan K, Negorev D, Maul GG, Rauscher FJ. 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 , 2002, 16(8): 919-932.
[7] Ivanov AV, Peng H, Yurchenko V, Yap KL, Negorev DG, Schultz DC, Psulkowski E, Fredericks WJ, White DE, Maul GG, Sadofsky MJ, Zhou MM, Rauscher FJ. PHD domain-mediated E3 ligase activity directs intramolecular sumoylation of an adjacent bromodomain required for gene silencing. Mol Cell , 2007, 28(5): 823-837.
[8] Rowe HM, Trono D. Dynamic control of endogenous retroviruses during development. Virology , 2011, 411(2): 273-287.
[9] Huntley S, Baggott DM, Hamilton AT, Tran-Gyamfi M, Yang S, Kim J, Gordon L, Branscomb E, Stubbs L. A comprehensive catalog of human KRAB-associated zinc finger genes: insights into the evolutionary history of a large family of transcriptional repressors. Genome Res , 2006, 16(5): 669-677.
[10] Birtle Z, Ponting CP. Meisetz and the birth of the KRAB motif. Bioinformatics , 2006, 22(23): 2841-2845.
[11] Kono H, Tamura M, Osada N, Suzuki H, Abe K, Moriwaki K, Ohta K, Shiroishi T. Prdm9 polymorphism unveils mouse evolutionary tracks. DNA Res , 2014, 21(3): 315-326.
[12] Liu H, Chang LH, Sun Y, Lu XC, Stubbs L. Deep vertebrate roots for mammalian zinc finger transcription factor subfamilies. Genome Biol Evol , 2014, 6(3): 510-525.
[13] Vinogradov AE. Human more complex than mouse at cellular level. PLoS One , 2012, 7(7): e41753.
[14] Vogel MJ, Guelen L, de Wit E, Peric-Hupkes D, Lodén M, Talhout W, Feenstra M, Abbas B, Classen AK, van Steensel B. Human heterochromatin proteins form large domains containing KRAB-ZNF genes. Genome Res , 2006, 16(12): 1493-1504.
[15] Westphal T, Reuter G. Recombinogenic effects of suppressors of position-effect variegation in Drosophila. Genetics , 2002, 160(2): 609-621.
[16] Cam HP, Sugiyama T, Chen ES, Chen X, FitzGerald PC, Grewal SIS. Comprehensive analysis of heterochromatin-and RNAi-mediated epigenetic control of the fission yeast genome. Nat Genet , 2005, 37(8): 809-819.
[17] Vissing H, Meyer WK, Aagaard L, Tommerup N, Thiesen HJ. Repression of transcriptional activity by heterologous KRAB domains present in zinc finger proteins. FEBS Lett , 1995, 369(2-3): 153-157.
[18] Lupo A, Cesaro E, Montano G, Zurlo D, Izzo P, Costanzo P. KRAB-zinc finger proteins: a repressor family displaying multiple biological functions. Curr Genomics , 2013, 14(4): 268-278.
[19] Urrutia R. KRAB-containing zinc-finger repressor proteins. Genome Biol , 2003, 4(10): 231.
[20] Emerson RO, Thomas JH. Gypsy and the birth of the SCAN domain. J Virol , 2011, 85(22): 12043-12052.
[21] King M, Wilson A. Evolution at two levels in humans and chimpanzees. Science , 1975, 188(4184): 107-116.
[22] Nadimpalli S, Persikov AV, Singh M. Pervasive variation of transcription factor orthologs contributes to regulatory network evolution. PLoS Genet , 2015, 11(3): e1005011.
[23] Looman C, Åbrink 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(12): 2118-2130.
[24] Jacobs FMJ, Greenberg D, Nguyen N, Haeussler M, Ewing AD, Katzman S, Paten B, Salama SR, Haussler D. An evolutionary arms race between KRAB zinc-finger genes ZNF91 / 93 and SVA/L1 retrotransposons. Nature , 2014, 516 (7530): 242-245.
[25] Brayer KJ, Segal DJ. Keep your fingers off my DNA: protein-protein interactions mediated by C2H2 zinc finger domains. Cell Biochem Biophys , 2008, 50(3): 111-131.
[26] Hoffmann A, Ciani E, Boeckardt J, Holsboer F, Journot L, Spengler D. Transcriptional activities of the zinc finger protein Zac are differentially controlled by DNA binding. Mol Cell Biol , 2003, 23(3): 988-1003.
[27] Siggers T, Reddy J, Barron B, Bulyk ML. Diversification of transcription factor paralogs via noncanonical modularity in C2H2 zinc finger DNA binding. Mol Cell , 2014, 55(4): 640-648.
[28] Cordaux R, Batzer MA. The impact of retrotransposons on human genome evolution. Nat Rev Genet , 2009, 10(10): 691-703.
[29] Brouha B, Schustak J, Badge RM, Lutz-Prigge S, Farley AH, Moran JV, Kazazian HH Jr. Hot L1s account for the bulk of retrotransposition in the human population. Proc Natl Acad Sci USA , 2003, 100(9): 5280-5285.
[30] Rowe HM, Jakobsson J, Mesnard D, Rougemont J, Reynard S, Aktas T, Maillard PV, Layard-Liesching H, Verp S, Marquis J, Spitz F, Constam DB, Trono D. KAP1 controls endogenous retroviruses in embryonic stem cells. Nature , 2010, 463(7278): 237-240.
[31] Castro-Diaz N, Ecco G, Coluccio A, Kapopoulou A, Yazdanpanah B, Friedli M, Duc J, Jang SM, Turelli P, Trono D. Evolutionally dynamic L1 regulation in embryonic stem cells. Genes Dev , 2014, 28(13): 1397-1409.
[32] Turelli P, Castro-Diaz N, Marzetta F, Kapopoulou A, Raclot C, Duc J, Tieng V, Quenneville S, Trono D. Interplay of TRIM28 and DNA methylation in controlling human endogenous retroelements. Genome Res , 2014, 24(8): 1260-1270.
[33] Wolf D, Goff SP. TRIM28 mediates primer binding site-targeted silencing of murine leukemia virus in embryonic cells. Cell , 2007, 131(1): 46-57.
[34] Wolf D, Goff SP. Embryonic stem cells use ZFP809 to silence retroviral DNAs. Nature , 2009, 458(7242): 1201- 1204.
[35] Lukic S, Nicolas JC, Levine AJ. The diversity of zinc-finger genes on human chromosome 19 provides an evolutionary mechanism for defense against inherited endogenous retroviruses. Cell Death Differ , 2014, 21(3): 381-387.
[36] Imbeault M, Trono D. As time goes by: KRABs evolve to KAP endogenous retroelements. Dev Cell , 2014, 31(3): 257-258.
[37] Quenneville S, Turelli P, Bojkowska K, Raclot C, Offner S, Kapopoulou A, Trono D. The KRAB-ZFP/KAP1 system contributes to the early embryonic establishment of site-specific DNA methylation patterns maintained during development. Cell Rep , 2012, 2(4): 766-773.
[38] Rowe HM, Friedli M, Offner S, Verp S, Mesnard D, Marquis J, Aktas T, Trono D. De novo DNA methylation of endogenous retroviruses is shaped by KRAB-ZFPs/ KAP1 and ESET. Development , 2013, 140(3): 519-529.
[39] Orr HA. Dobzhansky, Bateson, and the genetics of speciation. Genetics , 1996, 144(4): 1331-1335.
[40] Nowick K, Carneiro M, Faria R. A prominent role of KRAB-ZNF transcription factors in mammalian speciation?. Trends Genet , 2013, 29(3): 130-139.
[41] Hayashi K, Yoshida K, Matsui Y. A histone H3 methyltransferase controls epigenetic events required for meiotic prophase. Nature , 2005, 438(7066): 374-378.
[42] Mihola O, Trachtulec Z, Vlcek C, Schimenti JC, Forejt J. A mouse speciation gene encodes a meiotic histone H3 methyltransferase. Science , 2009, 323(5912): 373-375.
[43] Ségurel L, Leffler EM, Przeworski M. The case of the fickle fingers: how the PRDM9 zinc finger protein specifies meiotic recombination hotspots in humans. PLoS Biol , 2011, 9(12): e1001211.
[44] Persikov AV, Wetzel JL, Rowland EF, Oakes BL, Xu DJ, Singh M, Noyes MB. A systematic survey of the Cys 2 His 2 zinc finger DNA-binding landscape. Nucleic Acids Res , 2015, 43(3): 1965-1984.
[45] Wolf G, Greenberg D, Macfarlan TS. Spotting the enemy within: Targeted silencing of foreign DNA in mammalian genomes by the Krüppel-associated box zinc finger protein family. Mob DNA , 2015, 6: 17.
[46] Itokawa Y, Yanagawa T, Yamakawa H, Watanabe N, Koga H, Nagase T. KAP1-independent transcriptional repression of SCAN-KRAB-containing zinc finger proteins. Biochem Biophys Res Commun , 2009, 388(4): 689-694.
[47] Santoni de Sio FR. Kruppel-associated box (KRAB) proteins in the adaptive immune system. Nucleus , 2014, 5(2): 138-148.
[48] Ma ZF, Yang D, He FC, Jiang Y. Review for the regulatory functions of KRAB zinc finger proteins in embryonic development and tumorgenesis of higher vertebrates. Hereditas ( Beijing ), 2010, 32(5): 431-436. 马占福, 杨冬, 贺福初, 姜颖. KRAB型锌指蛋白在高等脊椎动物胚胎发育和肿瘤发生、发展中的调控功能. 遗传, 2010, 32(5): 431-436.
[49] Tian CY, Xing GC, Xie P, Lu KF, Nie J, Wang J, Li L, Gao M, Zhang LQ, He FC. KRAB-type zinc-finger protein Apak specifically regulates p53-dependent apoptosis. Nat Cell Biol , 2009, 11(5): 580-591.
[50] Yuan L, Tian CY, Wang HY, Song SS, Li DY, Xing GC, Yin YX, He FC, Zhang LQ. Apak competes with p53 for direct binding to intron 1 of p53AIP1 to regulate apoptosis. EMBO Rep , 2012, 13(4): 363-370.
[51] Chien HC, Wang HY, Su YN, Lai KY, Lu LC, Chen PC, Tsai SF, Wu CI, Hsieh WS, Shen CKJ. Targeted disruption in mice of a neural stem cell-maintaining, KRAB-Zn finger-encoding gene that has rapidly evolved in the human lineage. PLoS One , 2012, 7(10): e47481.
[52] Oliver CH, Khaled WT, Frend H, Nichols J, Watson CJ. The Stat6-regulated KRAB domain zinc finger protein Zfp157 regulates the balance of lineages in mammary glands and compensates for loss of Gata-3. Genes Dev , 2012, 26(10): 1086-1097.
[53] Krebs CJ, Larkins LK, Price R, Tullis KM, Miller RD, Robins DM. Regulator of sex - limitation ( Rsl ) encodes a pair of KRAB zinc-finger genes that control sexually dimorphic liver gene expression. Genes Dev , 2003, 17(21): 2664-2674.
[54] Bojkowska K, Aloisio F, Cassano M, Kapopoulou A, Santoni de Sio F, Zangger N, Offner S, Cartoni C, Thomas C, Quenneville S, Johnsson K, Trono D. Liver-specific ablation of Krüppel-associated box-associated protein 1 in mice leads to male-predominant hepatosteatosis and development of liver adenoma. Hepatology , 2012, 56(4): 1279-1290.

编辑推荐

Metrics

www.chinagene.cn
备案号：京ICP备09063187号-4
总访问:,今日访问:,当前在线:

KRAB型锌指蛋白的进化及在物种演化中的功能

Evolution of KRAB-containing zinc finger proteins and their roles in species evolution

PDF (PC)

可视化

摘要/Abstract

引用本文

使用本文

参考文献

相关文章 15

编辑推荐

Metrics

[1]	何超,沈文龙,李平,张彦,曾晶,殷作明,赵志虎. Alu元件在染色质三维结构层次上的生物信息学分析[J]. 遗传, 2019, 41(3): 254-261.
[2]	孟玉,杨若林. 基于基因家族大小的比较研究脊椎动物的适应性进化[J]. 遗传, 2019, 41(2): 158-174.
[3]	汪德州,莫晓婷,张霞,徐妙云,赵军,王磊. 玉米逆境响应相关转录因子ZmC2H2-1基因克隆及功能验证[J]. 遗传, 2018, 40(9): 767-778.
[4]	胡广东,郝科兴,黄涛,曾维斌,谷新利,王静. 绵羊高效转基因通用型piggyBac转座子载体构建及功能验证[J]. 遗传, 2018, 40(8): 647-656.
[5]	邓雯文,龙梅,杨盛智,邹立扣. β-内酰胺酶耐药基因bla_OKP进化及其侧翼序列特征研究[J]. 遗传, 2018, 40(7): 585-592.
[6]	刘启鹏, 安妮, 岑山, 李晓宇. piRNA抑制基因转座的分子机制[J]. 遗传, 2018, 40(6): 445-450.
[7]	冯平, 罗瑞健. 灵长类苦味受体基因研究进展[J]. 遗传, 2018, 40(2): 126-134.
[8]	许磊,陈文,司国阳,黄艺园,林毅,蔡永萍,高俊山. 陆地棉GST基因家族全基因组分析[J]. 遗传, 2017, 39(8): 737-752.
[9]	蓝洋,胡江涛,张玉娟. 化学计量基因组学研究进展[J]. 遗传, 2017, 39(2): 89-97.
[10]	赵永欣, 李孟华, 赵要风. 中国绵羊起源、进化和遗传多样性研究进展[J]. 遗传, 2017, 39(11): 958-973.
[11]	白东义, 赵一萍, 李蓓, 格日乐其木格, 张心壮, 芒来. 马属动物全基因组高通量测序研究进展[J]. 遗传, 2017, 39(11): 974-983.
[12]	沈丹,陈才,王赛赛,陈伟,高波,宋成义. Tc1/Mariner转座子超家族的研究进展[J]. 遗传, 2017, 39(1): 1-13.
[13]	王哲. 植物杂交后代中基因偏分离的产生原因及其进化意义[J]. 遗传, 2016, 38(9): 801-810.
[14]	任丽倩, 刘薇, 李文博, 刘文军, 孙蕾. 脊椎动物Cyclophilin A肽基脯氨酰顺反异构酶活性及遗传变异分析[J]. 遗传, 2016, 38(8): 736-745.
[15]	苏鹏冯少姝李庆伟. NF-кB和IκB在不同动物类群中的结构及功能研究进展[J]. 遗传, 2016, 38(6): 523-531.