退火解旋酶SMARCAL1在维持基因组稳定中的作用与机制

doi:10.16288/j.yczz.19-158

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Hereditas(Beijing) ›› 2019, Vol. 41 ›› Issue (12): 1084-1098.doi: 10.16288/j.yczz.19-158

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SMARCAL1, roles and mechanisms in genome stability maintenance

Yalei Wen¹, Kenao Lü², Xiaokang Xu¹, Xin Zhang¹, Liang Ding¹(), Xuefeng Pan^1,^2,³()

^1. Department of Pharmacology, Medical College of Hebei University, Baoding 071000, China
^2. School of Life Science, Beijing Institute of Technology, Beijing 100081, China
^3. School of Chemistry and Environmental Science, Hebei University, Baoding 071000, China

Received:2019-07-07 Revised:2019-09-04 Online:2019-12-20 Published:2019-09-18
Contact: Ding Liang,Pan Xuefeng E-mail:345823685@qq.com;xuefengpancam@aliyun.com
Supported by:
Supported by the Beijing Natural Science Foundation No(5132014);and the Hebei Provincial Key Research Programs for Medical Science No(20160051)

Abstract

Abstract:

SMARCAL1 is an ATP-driven DNA annealing helicase that is similar in structure to the chromatin regulators in the subfamily A group of the SWI/SNF-related matrix-associated actin-dependent chromatin regulators. SMARCAL1 catalyzes the formation of dsDNA by annealing the single-stranded binding protein RPA coated ssDNA with its complementary strand both in vitro and in vivo. In humans, different mutations of Smarcal1 gene are found to be closely related to different symptoms shown in individuals with Schimke immuno-osseous dysplasia (SIOD). This paper reviews the recent research progress of SMARCAL1 functions in remodeling DNA replication forks at damaged DNA sites, working in classical non-homologous end joining (NHEJ) repair of DNA double-stranded breaks, and in maintaining chromosomal telomere integrity. The relationships between the mutations of Smarcal1 gene in different SIOD symptoms, and the possible involvements of SMARCAL1 in neuromuscular degenerative diseases associated with trinucleotide repeats expansions are also updated and discussed to better understand the roles and mechanisms of the annealing helicase in genome stability maintenance.

Key words: SMARCAL1, RPA, DNA replication fork, SIOD, expansions of trinucleotide repeats

Yalei Wen, Kenao Lü, Xiaokang Xu, Xin Zhang, Liang Ding, Xuefeng Pan. SMARCAL1, roles and mechanisms in genome stability maintenance[J]. Hereditas(Beijing), 2019, 41(12): 1084-1098.

Figures/Tables 6

Fig. 1

Fig. 2

Fig. 3

Fig. 4

Fig. 5

Table 1

The correlations of Smarcal1 mutations and the symptoms of SIOD patients"

突变位点	突变类型	功能	症状	参考文献
c.1129G>C, p. E377Q	错义突变	SNP和非致病突变	无	[86]
c.1933C>T, p. R645C	错义突变	ATP酶活性缺失和解旋酶活性缺失	T细胞免疫缺陷、肾功能衰竭和生长迟缓
c.1334+1G>A	剪切突变	非致病突变	无
c.2142-1G>A	剪切突变	非致病突变	无
NM_014140.3：c.2070t2insT	mRNA剪切突变	非致病突变	无	[20]
p.[M288_D366del]+[M288_D366del]	双等位基因突变	缺乏解旋酶活性	生长迟缓、全血细胞减少症、短暂性脑缺血和肾病综合征	[12]
p.[E377Q]+[I755fsX2]	双等位基因突变	缺乏解旋酶活性	T细胞免疫缺陷、FSGS和生长迟缓
p.[Y342X]+[I755S]	双等位基因突变	缺乏解旋酶活性	生长迟缓、全血细胞减少症、反复感染和肾病综合征
c.445C>T(p.Q149X)	无义突变	导致氨基酸的改变	生长迟缓、蛋白尿和T细胞免疫缺陷	[87]
p.R817H	错义突变	缺乏解旋酶活性	生长迟缓、T细胞免疫缺陷和肾功能不全	[88]
c.1615C> G(p.[Leu539Val])	错义突变	缺乏解旋酶活性	生长迟缓、FSGS、肾衰竭和T细胞免疫缺陷	[89]
p. R247P	错义突变	退火酶活性	甲状腺功能不全、骨骼发育不良和蛋白尿	[90]
p. E848*	无义突变	退火酶活性	甲状腺功能不全、骨骼发育不良和蛋白尿	[90]
p.L397fsX40	移码突变	退火酶活性	FSGS、T细胞免疫缺陷、生长发育不良和鼻窦癌	[91]
p.S859P	错义突变	ATP酶活性	FSGS、T细胞免疫缺陷、生长发育不良和鼻窦癌	[91]
c.3G> A(p.M1?)	剪切突变	与RPA相互作用	生长迟缓、复发感染和中性粒细胞增多症、FSGS,T细胞免疫缺陷和严重腕骨骨质衰老	[92]
c.1682G> A(p. R561H)	错义突变	ATP酶活性	生长迟缓、复发感染和中性粒细胞增多症、FSGS,T细胞免疫缺陷和严重腕骨骨质衰老	[92]
R561C	错义突变	ATP酶活性	T细胞免疫缺陷、面部畸形、肾病综合征和FSGS	[93]
c.2542G> T, p.E848x	无义突变	退火酶活性	生长迟缓和慢性肾功能衰竭	[94]
c.1934G> A, p.R645H	错义突变	ATP酶活性	生长迟缓和慢性肾功能衰竭	[94]
IVS4-2A>G	剪接突变	非致病突变	肾脏畸形、生长迟缓和T细胞免疫缺陷	[14]
1136A> C, H379P	无义突变	非致病突变	生长迟缓、肾衰、FSGS和T细胞免疫缺陷	[95]
836T> C, F279S	错义突变	ATP酶活性	生长迟缓、肾衰、FSGS和T细胞免疫缺陷	[95]
1-BP INS,1849C	插入		生长迟缓和面部畸形	[96]
1-BP DEL.2161C	缺失		生长迟缓和面部畸形	[96]
R586W	错义突变	ATP酶活性	生长迟缓、蛋白尿和T细胞免疫缺陷	[97]
R644W	错义突变	ATP酶活性	生长迟缓、FSGS、肾衰竭和T细胞免疫缺陷
R645C	错义突变	ATP酶活性	生长迟缓、蛋白尿和T细胞免疫缺陷
R764Q	错义突变	ATP酶活性	生长迟缓、FSGS、肾衰竭和T细胞免疫缺陷
c.797-798delCC	微缺失突变	解旋酶活性	骨骼发育不良、蛋白尿和肾病综合征	[81]
IVSA7+1G>7	剪切突变	ATP酶活性	骨骼发育不良、蛋白尿和肾病综合征	[81]
A468P	错义突变	ATP酶活性	生长迟缓、蛋白尿和T细胞免疫缺陷	[93]
I548N	错义突变	ATP酶活性
S579L	错义突变	ATP酶活性

Table 1

References 101

[1]	Pan XF ed . The Molecular Biology of Gene and Diseases. Beijing: Chemical Industry Press, 2014, 1-450.
	潘学峰 . 基因疾病的分子生物学. 北京: 化学工业出版社, 2014, 1-450.
[2]	Pan XF, Xiao P, Li HQ, Zhao DX, Duan F . The gratuitous repair on undamaged DNA misfold, DNA Repair, 2011: 401-430. doi: 10.1016/j.dnarep.2012.01.007 pmid: 22365498
[3]	Poole LA, Cortez D . Functions of SMARCAL1, ZRANB3, and HLTF in maintaining genome stability. Crit Rev Biochem Mol Biol, 2017,52(6):696-714. doi: 10.1080/10409238.2017.1380597 pmid: 28954549
[4]	Bansal R, Arya V, Sethy R, Rakesh R, Muthuswami R. RecA-like domain 2 of DNA-dependent ATPase A domain, a SWI2/SNF2 protein, mediates conformational integrity and ATP hydrolysis. Biosci Rep, 2018,38(3): BSR20180568. doi: 10.1042/BSR20180568 pmid: 29748240
[5]	Bansbach CE, Bétous R, Lovejoy CA, Glick GG, Cortez D . The annealing helicase SMARCAL1 maintains genome integrity at stalled replication forks. Genes Dev, 2009,23(20):2405-2414. doi: 10.1101/gad.1839909 pmid: 19793861
[6]	Bétous R, Mason AC, Rambo RP, Bansbach CE, Badu- Nkansah A, Sirbu BM, Cortez D . SMARCAL1 catalyzes fork regression and Holliday junction migration to maintain genome stability during DNA replication. Genes Dev, 2012,26(2):151-162. doi: 10.1101/gad.178459.111 pmid: 22279047
[7]	Lugli N, Sotiriou SK, Halazonetis TD . The role of SMARCAL1 in replication fork stability and telomere maintenance. DNA Repair, 2017,56:129-134. doi: 10.1016/j.dnarep.2017.06.015 pmid: 28623093
[8]	Severino M, Giacomini T, Verrina E, Prato G, Rossi A . Reversible cerebral vasoconstriction complicating cerebral atherosclerotic vascular disease in Schimke immuno- osseous dysplasia. Neuroradiology, 2018,60(9):885-888. doi: 10.1007/s00234-018-2052-y pmid: 29978300
[9]	Driscoll R, Cimprich KA . HARPing on about the DNA damage response during replication. Genes Dev, 2009,23(20):2359-2365. doi: 10.1101/gad.1860609 pmid: 19833762
[10]	Kakar S, Fang X, Lubkowska L, Zhou YN, Shaw GX, Wang YX, Kashlev M, Ji X . Allosteric activation of bacterial Swi2/Snf2 (Switch/Sucrose non-fermentable) protein RapA by RNA polymerase: biochemical and structural studies. J Biol Chem, 2015,290(39):23656-23669. doi: 10.1074/jbc.M114.618801 pmid: 26272746
[11]	Hargreaves DC, Crabtree GR . ATP-dependent chromatin remodeling: genetics, genomics and mechanisms. Cell Res, 2011,21(3):396-420. doi: 10.1038/cr.2011.32
[12]	Morimoto M . Characterization of the disease pathogenesis of Schimke immuno-osseous dysplasia. University Of British Columbia, 2016: 27-46. doi: 10.1016/j.ejmg.2016.06.002 pmid: 27282802
[13]	Baradaran-Heravi A, Raams A, Lubieniecka J, Cho KS, DeHaai KA, Basiratnia M, Mari PO, Xue Y, Rauth M, Olney AH, Shago M, Choi K, Weksberg RA, Nowaczyk MJ, Wang W, Jaspers NG, Boerkoel CF. SMARCAL1 deficiency predisposes to non-Hodgkin lymphoma and hypersensitivity to genotoxic agents in vivo. Am J Med Genet A, 2012,158A(9):2204-2213. doi: 10.1002/ajmg.a.35532
[14]	Dekel B, Metsuyanim S, Goldstein N, Pode-Shakked N, Kovalski Y, Cohen Y, Davidovits M, Anikster Y . Schimke immuno-osseous dysplasia: expression of SMARCAL1 in blood and kidney provides novel insight into disease phenotype. Pediatr Res, 2008,63(4):398-403. doi: 10.1203/PDR.0b013e31816721cc pmid: 18356746
[15]	Haokip, Thangminlen D, Kumari . Human SMARCAL1-a member of the SWI2/SNF2 family-is required for cell division. Faseb J, 2011,25(12):3515-3524.
[16]	Elizondo LI, Cho KS, Zhang W, Yan J, Huang C, Huang Y, Choi K, Sloan EA, Deguchi K, Lou S, Baradaran- Heravi A, Takashima H, Lücke T, Quiocho FA, Boerkoel CF . Schimke immuno-osseous dysplasia: SMARCAL1 loss-of-function and phenotypic correlation. J Med Genet, 2009,46(1):49-59. doi: 10.1136/jmg.2008.060095 pmid: 18805831
[17]	Patne K, Rakesh R, Arya V, Chanana UB, Sethy R, Swer PB, Muthuswami R . BRG1 and SMARCAL1 transcriptionally co-regulate DROSHA, DGCR8 and DICER in response to doxorubicin-induced DNA damage. Biochim Biophys Acta Gene Regul Mech, 2017,1860(9):936-951. doi: 10.1016/j.bbagrm.2017.07.003 pmid: 28716689
[18]	Baradaran-Heravi A, Lange J, Asakura Y, Cochat P, Massella L, Boerkoel CF . Bone marrow transplantation in Schimke immuno‐osseous dysplasia. Am J Med Genet A, 2013,161A(10):2609-2613. doi: 10.1002/ajmg.a.36111 pmid: 23950031
[19]	Zhang L, Fan S, Liu H, Huang C . Targeting SMARCAL1 as a novel strategy for cancer therapy. Biochem Biophys Res Commun, 2012,427(2):232-235. doi: 10.1016/j.bbrc.2012.09.060 pmid: 22995303
[20]	Carroll C, Hunley TE, Guo Y, Cortez D . A novel splice site mutation in SMARCAL1 results in aberrant exon definition in a child with schimke immunoosseous dysplasia. Am J Med Genet A, 2015,167A(10):2260-2264. doi: 10.1002/ajmg.a.37146 pmid: 25943327
[21]	Prato G, Grandis ED, Mancardi MM, Croci C, Pisciotta D, Uccella S, Costanzo C, Severino S, Tortora D, Pavanello M, Venesellividovits E . Schimke Immuno-osseous dysplasia: a peculiar EEG pattern. Neuropediatrics, 2018,49(S 01):S1-S12. pmid: 28256679
[22]	Yusufzai T, Kadonaga JT . HARP is an ATP-driven annealing helicase. Science, 2008,322(5902):748-750. doi: 10.1126/science.1161233 pmid: 18974355
[23]	Ghosal G, Yuan J, Chen J . The HARP domain dictates the annealing helicase activity of HARP/SMARCAL1. EMBO Rep, 2011,12(6):574-580. doi: 10.1038/embor.2011.74
[24]	Ciccia A, Bredemeyer AL, Sowa ME, Terret ME, Jallepalli PV, Harper JW, Elledge SJ . The SIOD disorder protein SMARCAL1 is an RPA-interacting protein involved in replication fork restart. Genes Dev, 2009,23(20):2415-2425. doi: 10.1101/gad.1832309 pmid: 19793862
[25]	Hauk G, Bowman GD . Structural insights into regulation and action of SWI2/SNF2 ATPases. Curr Opin Struct Biol, 2011,21(6):719-727. doi: 10.1016/j.sbi.2011.09.003 pmid: 21996440
[26]	Aydin ?Z, Vermeulen W, Lans H . ISWI chromatin remodeling complexes in the DNA damage response. Cell Cycle, 2014,13(19):3016-3025. doi: 10.4161/15384101.2014.956551
[27]	Kohashi K, Yamamoto H, Yamada Y, Kinoshita I, Taguchi T, Iwamoto Y, Oda Y . SWI/SNF Chromatin-remodeling Complex Status in SMARCB1/INI1-preserved Epithelioid Sarcoma. Am J Surg Pathol, 2018,42(3):312-318. doi: 10.1097/PAS.0000000000001011 pmid: 29309303
[28]	Han JJ, Song ZT, Sun JL, Yang ZT, Xian MJ, Wang S, Sun L, Liu JX . Chromatin remodeling factor CHR18 interacts with replication protein RPA1A to regulate the DNA replication stress response in Arabidopsis. New Phytol, 2018,220(2):476-487. doi: 10.1111/nph.15311 pmid: 29974976
[29]	Bétous R, Couch FB, Mason AC, Eichman BF, Manosas M, Cortez D . Substrate-selective repair and restart of replication forks by DNA translocases. Cell Rep, 2013,3(6):1958-1969. doi: 10.1016/j.celrep.2013.05.002 pmid: 23746452
[30]	芦广庆, 段金志, 张昱 . 哺乳动物DNA连接酶在DNA双链断裂修复通路中的作用. 遗传, 2016,38(2):178-179.
[31]	Maréchal A, Zou L . RPA-coated single-stranded DNA as a platform for post-translational modifications in the DNA damage response. Cell Res, 2015,25(1):9-23. doi: 10.1038/cr.2014.147 pmid: 25403473
[32]	Holsclaw JK, Sekelsky J . Annealing of complementary DNA sequences during Double-Strand Break repair in Drosophila is mediated by the ortholog of SMARCAL1. Genetics, 2017,206(1):467-480. doi: 10.1534/genetics.117.200238 pmid: 28258182
[33]	Bhat KP, Bétous R, Cortez D . High-affinity DNA-binding domains of replication protein A (RPA) direct SMARCAL1- dependent replication fork remodeling. J Biol Chem, 2015,290(7):4110-4117. doi: 10.1074/jbc.M114.627083 pmid: 25552480
[34]	Oakley GG, Patrick SM . Replication protein A: directing traffic at the intersection of replication and repair. Front Biosci, 2010,15:883-900. doi: 10.2741/3652 pmid: 20515732
[35]	Xie S, Lu Y, Jakoncic J, Sun H, Xia J, Qian C . Structure of RPA32 bound to the N-terminus of SMARCAL1 redefines the binding interface between RPA32 and its interacting proteins. FEBS J, 2014,281(15):3382-3396. doi: 10.1111/febs.12867
[36]	Sotiriou SK, Kamileri I, Lugli N, Evangelou K, Da-Ré C, Huber F, Padayachy L, Tardy S, Nicati NL, Barriot S, Ochs F, Lukas C, Lukas J, Gorgoulis VG, Scapozza L, Halazonetis TD . Mammalian RAD52 functions in break-induced replication repair of collapsed DNA replication Forks. Mol Cell, 2016,64(6):1127-1134. doi: 10.1016/j.molcel.2016.10.038 pmid: 27984746
[37]	Feldkamp MD, Mason AC, Eichman BF, Chazin WJ . Structural analysis of replication protein A recruitment of the DNA damage response protein SMARCAL1. Biochemistry, 2014,53(18):3052-3061. doi: 10.1021/bi500252w
[38]	Lovejoy CA, Cortez D . Common mechanisms of PIKK regulation. DNA Repair, 2009,8(9):1004-1008. doi: 10.1016/j.dnarep.2009.04.006
[39]	Couch FB, Bansbach CE, Driscoll R, Luzwick JW, Glick GG, Bétous R, Carroll CM, Jung SY, Qin J, Cimprich KA, Cortez D . ATR phosphorylates SMARCAL1 to prevent replication fork collapse. Genes Dev, 2013,27(14):1610-1623. doi: 10.1101/gad.214080.113 pmid: 23873943
[40]	Bétous R, Glick GG, Zhao R, Cortez D . Identification and characterization of SMARCAL1 protein complexes. PLoS One, 2013,8(5):e63149. doi: 10.1371/journal.pone.0063149 pmid: 23671665
[41]	Atkinson J, McGlynn P. Replication fork reversal and the maintenance of genome stability. Nucleic Acids Res, 2009,37(11):3475-3492. doi: 10.1093/nar/gkp244 pmid: 19406929
[42]	Neelsen KJ, Lopes M . Replication fork reversal in eukaryotes: from dead end to dynamic response. Nat Rev Mol Cell Biol, 2015,16(4):207-220. doi: 10.1038/nrm3935 pmid: 25714681
[43]	Margalef P, Kotsantis P, Borel V, Bellelli R, Panier S, Boulton S J . Stabilization of reversed replication forks by telomerase drives telomere catastrophe. Cell, 2018,172(3):439-453. doi: 10.1016/j.cell.2017.11.047 pmid: 29290468
[44]	Bianco PR, Lyubchenko YL . SSB and the RecG DNA helicase: an intimate association to rescue a stalled replication fork. Protein Sci, 2017,26(4):638-649. doi: 10.1002/pro.3114 pmid: 28078722
[45]	Wu XM, Tang WR, Luo Y . ALT-Alternative lengthening of telomere. Hereditas(Beijing) , 2009,31(12):1185-1191. doi: 10.3724/SP.J.1005.2009.01185
	吴晓明, 唐文如, 罗瑛 . ALT-端粒延长替代机制. 遗传, 2009,31(12):1185-1191. doi: 10.3724/SP.J.1005.2009.01185
[46]	Ying SY, Xiong JX, Mai HX, Lin JJ, Jiang LN, Cheng L, Ye QN . Advances on the regulation of telomerase. Hereditas(Beijing) , 2016,38(4):289-299 doi: 10.16288/j.yczz.15-356 pmid: 27103453
	营孙阳, 熊加秀, 麦洪旭, 林佳佳, 姜丽娜, 程龙, 叶棋浓 . 端粒酶调控研究进展. 遗传, 2016,38(4):289-299. doi: 10.16288/j.yczz.15-356 pmid: 27103453
[47]	Sfeir A, Kosiyatrakul ST, Hockemeyer D, MacRae SL, Karlseder J, Schildkraut CL, de Lange T . Mammalian telomeres resemble fragile sites and require TRF1 for efficient replication. Cell, 2009,138(1):90-103. doi: 10.1016/j.cell.2009.06.021 pmid: 19596237
[48]	Sobinoff AP, Pickett HA . Alternative lengthening of telomeres: DNA repair pathways converge. Trends Gene, 2017,33(12):921-932. doi: 10.1016/j.tig.2017.09.003 pmid: 28969871
[49]	Cox KE, Maréchal A, Flynn RL . SMARCAL1 resolves replication stress at ALT telomeres. Cell Rep, 2016,14(5):1032-1040. doi: 10.1016/j.celrep.2016.01.011 pmid: 26832416
[50]	Poole LA, Cortez D . SMARCAL1 and telomeres: replicating the troublesome ends. Nucleus, 2016,7(3):270-274. doi: 10.1080/19491034.2016.1179413 pmid: 27355316
[51]	Pannunzio NR, Watanabe G, Lieber MR . Nonhomologous DNA end-joining for repair of DNA double-strand breaks. J Biol Chem, 2018,293(27):10512-10523. doi: 10.1074/jbc.TM117.000374 pmid: 29247009
[52]	Orthwein A, Fradet-Turcotte A, Noordermeer SM, Canny MD, Brun CM, Strecker J, Escribano-Diaz C, Durocher D . Mitosis inhibits DNA double-strand break repair to guard against telomere fusions. Science, 2014,344(6180):189-193. doi: 10.1126/science.1248024 pmid: 24652939
[53]	Sims J, Copenhaver GP, Schloegelhofer P . Meiotic DNA repair in the nucleolus employs a non-homologous end joining mechanism. Plant Cell, doi: https://doi.org/10.1101/553529. doi: 10.1105/tpc.19.00638 pmid: 31826966
[54]	Lu HM, Shamanna RA, de Freitas JK, Okur M, Khadka P, Kulikowicz T, Holland PP, Tian J, Croteau DL, Davis AJ, Bohr VA . Cell cycle-dependent phosphorylation regulates RECQL4 pathway choice and ubiquitination in DNA double-strand break repair. Nat Commun, 2017,8(1):2039. doi: 10.1038/s41467-017-02146-3 pmid: 29229926
[55]	Keka IS, Mohiuddin , Maede Y, Rahman MM, Sakuma T, Honma M, Yamamoto T, Takeda S, Sasanuma H. Smarcal1 promotes double-strand-break repair by nonhomologous end-joining. Nucleic Acids Res, 2015,43(13):6359-6372. doi: 10.1093/nar/gkv621 pmid: 26089390
[56]	Mimitou EP, Symington LS . Ku prevents Exo1 and Sgs1-dependent resection of DNA ends in the absence of a functional MRX complex or Sae2. Embo J, 2010,29(19):3358-3369. doi: 10.1038/emboj.2010.193 pmid: 20729809
[57]	Ling AK, So CC, Le MX, Chen AY, Hung L, Martin A . Double-stranded DNA break polarity skews repair pathway choice during intrachromosomal and interchromosomal recombination. Proc Natl Acad Sci USA, 2018,115(11):2800-2805. doi: 10.1073/pnas.1720962115 pmid: 29472448
[58]	Jette N, Lees-Miller SP . The DNA-dependent protein kinase: A multifunctional protein kinase with roles in DNA double strand break repair and mitosis. Prog Biophys Mol Biol, 2015,117(2-3):194-205. doi: 10.1016/j.pbiomolbio.2014.12.003 pmid: 25550082
[59]	Chang HHY, Pannunzio NR, Adachi N, Lieber MR . Non-homologous DNA end joining and alternative pathways to double-strand break repair. Nat Rev Mol Cell Biol, 2017,18(8):495-506. doi: 10.1038/nrm.2017.48 pmid: 28512351
[60]	Hammel M, Yu Y, Radhakrishnan SK, Chokshi C, Tsai MS, Matsumoto Y, Kuzdovich M, Remesh SG, Fang S, Tomkinson AE, Lees-Miller SP, Tainer JA . An intrinsically disordered APLF links Ku, DNA-PKcs, and XRCC4-DNA ligase IV in an extended flexible non- homologous end joining complex. J Biol Chem, 2016,291(53):26987-27006. doi: 10.1074/jbc.M116.751867 pmid: 27875301
[61]	Hinde E, Kong X, Yokomori K, Gratton E . Chromatin dynamics during DNA repair revealed by pair correlation analysis of molecular flow in the nucleus. Biophys J, 2014,107(1):55-65. doi: 10.1016/j.bpj.2014.05.027 pmid: 24988341
[62]	Sibanda BL, Chirgadze DY, Ascher DB, Blundell TL . DNA-PKcs structure suggests an allosteric mechanism modulating DNA double-strand break repair. Science, 2017,355(6324):520-524. doi: 10.1126/science.aak9654 pmid: 28154079
[63]	Ma Y, Pannicke U, Lu H, Niewolik D, Schwarz K, Lieber MR . The DNA-dependent protein kinase catalytic subunit phosphorylation sites in human Artemis. J Biol Chem, 2005, 280(40):33839-33846. doi: 10.1074/jbc.M507113200 pmid: 16093244
[64]	Zhou Y, Caron P, Legube G, Paull TT . Quantitation of DNA double-strand break resection intermediates in human cells. Nucleic Acids Res, 2014,42(3):e19. doi: 10.1093/nar/gkt1309 pmid: 24362840
[65]	Yin X, Liu M, Tian Y, Wang J, Xu Y . Cryo-EM structure of human DNA-PK holoenzyme. Cell Res, 2017,27(11):1341-1350. doi: 10.1038/cr.2017.110 pmid: 28840859
[66]	Hiom K . Coping with DNA double strand breaks. DNA Repair, 2010,9(12):1256-1263. doi: 10.1016/j.dnarep.2010.09.018
[67]	Shibata A, Moiani D, Arvai AS, Perry J, Harding SM, Genois MM, Maity R, van Rossum-Fikkert S, Kertokalio A, Romoli F, Ismail A, Ismalaj E, Petricci E, Neale MJ, Bristow RG, Masson JY, Wyman C, Jeggo PA, Tainer JA. DNA double-strand break repair pathway choice is directed by distinct MRE11 nuclease activities. Mol Cell, 2014,53(1):7-18. doi: 10.1016/j.molcel.2013.11.003 pmid: 24316220
[68]	Casari E, Rinaldi C, Marsella A, Gnugnoli M, Colombo CV, Bonetti D, Longhese MP . Processing of DNA double-strand breaks by the MRX complex in a chromatin context. Front Mol Biosci, 2019,6:43. doi: 10.3389/fmolb.2019.00043 pmid: 31231660
[69]	Korsholm LM, Gál Z, Lin L, Quevedo O, Ahmad DA, Dulina E, Luo YL, Bartek J, Larsen DH . Double-strand breaks in ribosomal RNA genes activate a distinct signaling and chromatin response to facilitate nucleolar restructuring and repair. Nucleic Acids Res, 2019,47(15):8019-8035. doi: 10.1093/nar/gkz518 pmid: 31184714
[70]	Parsons DW, Jones S, Zhang X, Lin JC, Leary RJ, Angenendt P, Mankoo P, Carter H, Siu IM, Gallia GL, Olivi A, McLendon R, Rasheed BA, Keir S, Nikolskaya T, Nikolsky Y, Busam DA, Tekleab H, Diaz LA Jr, Hartigan J, Smith DR, Strausberg RL, Marie SK, Shinjo SM, Yan H, Riggins GJ, Bigner DD, Karchin R, Papadopoulos N, Parmigiani G, Vogelstein B, Velculescu VE, Kinzler KW . An integrated genomic analysis of human glioblastoma multiforme. Science, 2008,321(5897):1807-1812. doi: 10.1126/science.1164382 pmid: 18772396
[71]	Kolinjivadi AM, Sannino V, De Antoni A, Zadorozhny K, Kilkenny M, Técher H, Baldi G, Shen R, Ciccia A, Pellegrini L, Krejci L, Costanzo V . Smarcal1-mediated fork reversal triggers Mre11-dependent degradation of nascent DNA in the absence of Brca2 and stable Rad51 nucleofilaments. Mol Cell, 2017,67(5):867-881. doi: 10.1016/j.molcel.2017.07.001 pmid: 28757209
[72]	Levens DL . Reconstructing myc. Genes Dev, 2003,17(9):1071-1077. doi: 10.1101/gad.1095203 pmid: 12730130
[73]	Barna M, Pusic A, Zollo O, Costa M, Kondrashov N, Rego E, Rao PH, Ruggero D . Suppression of Myc oncogenic activity by ribosomal protein haploinsufficiency. Nature, 2008,456(7224):971-975. doi: 10.1038/nature07449 pmid: 19011615
[74]	Sutherland C, Cui YX, Mao HB, Hurley LH . A mechanosensor mechanism controls the G-quadruplex/ i-motif molecular switch in the MYC promoter NHE III₁. J Am Chem Soc, 2016,138(42):14138-14151. doi: 10.1021/jacs.6b09196 pmid: 27669098
[75]	Baradaran-Heravi A, Cho KS, Tolhuis B, Sanyal M, Morozova O, Morimoto M, Elizondo LI, Bridgewater D, Lubieniecka J, Beirnes K, Myung C, Leung D, Fam HK, Choi K, Huang Y, Dionis KY, Zonana J, Keller K, Stenzel P, Mayfield C, Lücke T, Bokenkamp A, Marra MA, van Lohuizen M, Lewis DB, Shaw C, Boerkoel CF. Penetrance of biallelic SMARCAL1 mutations is associated with environmental and genetic disturbances of gene expression. Hum Mol Genet, 2012,21(11):2572-2587. doi: 10.1093/hmg/dds083
[76]	Sharma T, Bansal R, Haokip DT, Goel I, Muthuswami R . SMARCAL1 negatively regulates c-Myc transcription by altering the conformation of the promoter region. Sci Rep, 2015,5:17910. doi: 10.1038/srep17910 pmid: 26648259
[77]	Pan XF . Mechanism of trinucleotide repeats instabilities: the necessities of repeat non-B secondary structure formation and the roles of cellular trans-acting factors. Yi Chuan Xue Bao, 2006,33(1):1-11. doi: 10.1016/S0379-4172(06)60001-2 pmid: 16450581
[78]	Pan XF, Jiang N, Chen XF, Zhou XH, Ding L, Duan F . R-loop structure: the formation and the effects on genomic stability. Hereditas(Beijing), 2014,36(12):1185-1194. doi: 10.3724/SP.J.1005.2014.1185 pmid: 25487262
	潘学峰, 姜楠, 陈细芳, 周晓宏, 丁良, 段斐 . R环的形成及对基因组稳定性的影响. 遗传, 2014,36(12):1185-1194. doi: 10.3724/SP.J.1005.2014.1185 pmid: 25487262
[79]	Wang XH, Pan XF, Li HQ . Advances in the studies of the expansion of (CAG) n·(CTG) n trinucleotide repeats and mecha-nisms underlying its related diseases. Int J Genet, 2016,39(15):274-281.
	王希恒, 潘学峰, 李红权 . (CAG)n·(CTG)n三核苷酸重复序列扩增及相关疾病机制研究进展. 国际遗传学杂志, 2016,39(15):274-281.
[80]	Kononenko AV, Ebersole T, Vasquez KM, Mirkin SM . Mechanisms of genetic instability caused by (CGG)n repeats in an experimental mammalian system. Nat Struct Mol Biol, 2018,25(8):669-676. doi: 10.1038/s41594-018-0094-9 pmid: 30061600
[81]	王晓慧, 方方, 丁昌红, 黄昱, 王旭, 李楠 . Schimke免疫-骨发育不良一例. 中华儿科杂志, 2015,53(8):631-632.
[82]	Lücke T, Franke D, Clewing JM, Boerkoel CF, Ehrich JH, Das AM, Zivicnjak M . Schimke versus non-Schimke chronic kidney disease: an anthropometric approach. Pediatrics, 2006,118(2):e400-407. doi: 10.1542/peds.2005-2614 pmid: 16816006
[83]	Gupta M, Mazumder M, Dhatchinamoorthy K, Nongkhlaw M, Haokip DT, Gourinath S, Komath SS, Muthuswami R . Ligand-induced conformation changes drive ATP hydrolysis and function in SMARCAL1. FEBS J, 2015,282(19):3841-3859. doi: 10.1111/febs.13382 pmid: 26195148
[84]	Saraiva JM, Dinis A, Resende C, Faria E, Gomes C, Correia AJ, Gil J, da Fonseca N. Schimke immuno- osseous dysplasia: case report and review of 25 patients. J Med Genet, 1999,36(10):786-789. doi: 10.1136/jmg.36.10.786 pmid: 10528861
[85]	Boerkoel CF, O'Neill S, André JL, Benke PJ, Bogdanoví? R, Bulla M, Burguet A, Cockfield S, Cordeiro I, Ehrich JH, Fründ S, Geary DF, Ieshima A, Illies F, Joseph MW, Kaitila I, Lama G, Leheup B, Ludman MD, McLeod DR, Medeira A, Milford DV, Orm?l? T, Rener-Primec Z, Santava A, Santos HG, Schmidt B, Smith GC, Spranger J, Zupancic N, Weksberg R. Manifestations and treatment of Schimke immuno-osseous dysplasia: 14 new cases and a review of the literature. Eur J Pediatr, 2000,159(1-2):1-7. doi: 10.1007/s004310050001
[86]	Wang W, Song H, Wei M, Qiu Z, Wang C, Zhang Y, Li M, Yuan YH, Tang XY . SMARCAL1 gene analysis of 2 Chinese Schimke immuno-osseous dysplasia children. Chin J Pediatr. 2015,53(1):45-50.
	王薇, 宋红梅, 魏珉, 邱正庆, 王晨, 张玉, 李明, 袁裕衡, 唐晓艳 . Schimke免疫-骨发育不良儿童基因分析. 中华儿科杂志, 2015,53(1):45-50.
[87]	Liu ZQ, Song FY, Liu Y, Qiu MF, Qian Y, Chen XB . Schimke immuno-osseous dysplasia (SIOD): A case report and review of literatures. Chin J Endocrinol Metabolism. 2017,33(2):111-115.
	刘子勤, 宋福英, 刘颖, 邱明芳, 钱晔, 陈晓波 . Schimke免疫-骨发育不良一例并文献复习. 中华内分泌代谢杂志, 2017,33(2):111-115.
[88]	Liu SM, Zhang MC, Ni MX, Zhu PR, Xia XY . A novel compound heterozygous mutation of the SMARCAL1 gene leading to mild Schimke immune-osseous dysplasia: a case report. BMC Pediatr, 2017,17(1):217. doi: 10.1186/s12887-017-0968-8 pmid: 29282041
[89]	Barraza-García J, Rivera-Pedroza CI, Belinchón A, Fernández-Camblor C, Valenciano-Fuente B, Lapunzina P, Heath KE . A novel SMARCAL1 missense mutation that affects splicing in a severely affected Schimke immunoosseous dysplasia patient. Eur J Med Genet, 2016,59(8):363-366. doi: 10.1016/j.ejmg.2016.06.002 pmid: 27282802
[90]	Santangelo L, Gigante M, Netti GS, Diella S, Puteo F, Carbone V, Gesualdo L . A novel SMARCAL1 mutation associated with a mild phenotype of Schimke immuno- osseous dysplasia (SIOD). BMC Nephrol, 2014,15(1):41. doi: 10.1186/1471-2369-15-41 pmid: 24589093
[91]	Carroll C, Badu-Nkansah A, Hunley T, Baradaran- Heravi A, Cortez D, Frangoul H . Schimke Immunoosseous Dysplasia associated with undifferentiated carcinoma and a novel SMARCAL1 mutation in a child. Pediatr Blood Cancer, 2013,60(9):E88-90. doi: 10.1002/pbc.24542
[92]	Yue Z, Xiong S, Sun L, Huang W, Mo Y, Huang L, Jiang X, Chen S, Hu B, Wang Y . Novel compound mutations of SMARCAL1 associated with severe Schimke immuno- osseous dysplasia in a Chinese patient . Nephrol Dial Transplant, 2010,25(5):1697-1702. doi: 10.1093/ndt/gfq071 pmid: 20179009
[93]	B?kenkamp A, deJong M, van Wijk JA, Block D, van Hagen JM, Ludwig M . R561C missense mutation in the SMARCAL1 gene associated with mild Schimke immuno- osseous dysplasia. Pediatr Nephrol, 2005,20(12):1724-1728. doi: 10.1007/s00467-005-2047-x
[94]	Zivicnjak M, Franke D, Zenker M, Hoyer J, Lücke T, Pape L, Ehrich JH . SMARCAL1 mutations: a cause of prepubertal idiopathic steroid-resistant nephrotic syndrome. Pediatr Res, 2009,65(5):564-568. doi: 10.1203/PDR.0b013e3181998a74 pmid: 19127206
[95]	Kilic SS, Donmez O, Sloan EA, Elizondo LI, Huang C, André JL, Bogdanovic R, Cockfield S, Cordeiro I, Deschenes G, Fründ S, Kaitila I, Lama G, Lamfers P, Lücke T, Milford DV, Najera L, Rodrigo F, Saraiva JM, Schmidt B, Smith GC, Stajic N, Stein A, Taha D, Wand D, Armstrong D, Boerkoel CF . Association of migraine- like headaches with Schimke immuno-osseous dysplasia. Am J Med Genet A, 2005,135(2):206-210. doi: 10.1002/ajmg.a.30692 pmid: 15884045
[96]	Simon AJ, Lev A, Jeison M, Borochowitz ZU, Korn D, Lerenthal Y, Somech R . Novel SMARCAL1 bi-allelic mutations associated with a chromosomal breakage phenotype in a severe SIOD patient. J Clin Immunol, 2014,34(1):76-83. doi: 10.1007/s10875-013-9957-3
[97]	Boerkoel CF, Takashima H, John J, Yan J, Stankiewicz P, Rosenbarker L, André JL, Bogdanovic R, Burguet A, Cockfield S, Cordeiro I, Fründ S, Illies F, Joseph M, Kaitila I, Lama G, Loirat C, McLeod DR, Milford DV, Petty EM, Rodrigo F, Saraiva JM, Schmidt B, Smith GC, Spranger J, Stein A, Thiele H, Tizard J, Weksberg R, Lupski JR, Stockton DW. Mutant chromatin remodeling protein SMARCAL1 causes Schimke immuno-osseous dysplasia. Nat Genet, 2002,30(2):215-220. doi: 10.1038/ng821 pmid: 11799392
[98]	Meek K, Gupta S, Ramsden DA, Lees-Miller SP . The DNA-dependent protein kinase: the director at the end. Immunol Rev, 2004,200:132-141. doi: 10.1111/j.0105-2896.2004.00162.x pmid: 15242401
[99]	Buck D, Moshous D, de Chasseval R, Ma Y, le Deist F, Cavazzana-Calvo M, Fischer A, Casanova JL, Lieber MR, de Villartay JP . Severe combined immunodeficiency and microcephaly in siblings with hypomorphic mutations in DNA ligase IV. Eur J Immunol, 2006,36(1):224-235. doi: 10.1002/eji.200535401 pmid: 16358361
[100]	Lev A, Amariglio N, Levy Y, Spirer Z, Anikster Y, Rechavi G, Dekel B, Somech R . Molecular assessment of thymic capacities in patients with Schimke immuno- osseous dysplasia. Clin Immunol, 2009,133(3):375-381. doi: 10.1016/j.clim.2009.08.017 pmid: 19796992
[101]	Dutta P, Tanti GK, Sharma S, Goswami SK, Komath SS, Mayo MW, Hockensmith JW, Muthuswami R . Global epigenetic changes induced by SWI2/SNF2 inhibitors characterize neomycin-resistant mammalian cells. PLoS One, 2012,7(11):e49822. doi: 10.1371/journal.pone.0049822 pmid: 23209606

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SMARCAL1, roles and mechanisms in genome stability maintenance

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