Binding of human SWI1 ARID domain to DNA without sequence specificity: A molecular dynamics study

Abstract

SWI1 is a member of a new class of tumor DNA-binding proteins named as the AT-rich interaction domain family (ARID), and considered to bind with AT base pairs specifically. Genomic and functional data support ARID1A as a tumor suppressor because ARID1A/BAF250a (SWI1) subunit of the SWI/SNF chromatin-remodeling complex has emerged as recurrently mutated in a broad array of tumor types. But the crystal structure of SWI1 has not been solved as yet. Using docking and molecular dynamics, we predicted the DNA interaction pattern of human SWI1 ARID and made comparisons with the other two representative ARID family members, human Mrf-2 ARID and Drosophila Dri ARID. Dynamic results revealed that the N-terminal and loop L1 of SWI1 ARID bound with the DNA major groove, while the loop L2 and helix H6 bound with the minor groove. Moreover, it was found that SWI1 ARID bound with DNA apparently in a sequence-nonspecific manner. It was concluded that SWI1 ARID can form stable complex with sequence-nonspecific DNA segment comparing to Mrf-2 ARID/DNA and Dri ARID/DNA sequence-specific complexes.

Keywords

AT-rich interaction domain family 1A (ARID) / BAF250a / Mrf-2 ARID / Dri ARID / protein-DNA interaction / ovarian cancer

References

[1] WuJN, RobertsCW. ARID1A mutations in cancer: another epigenetic tumor suppressor. Cancer Discov, 2013, 3(1): 35-43 PMCID: 3546152 PMID: 23208470

[2] JonesS, WangTL, ShihI M, et al. . Frequent mutations of chromatin remodeling gene ARID1A in ovarian clear cell carcinoma. Science, 2010, 330(6001): 228-231 PMCID: 3076894 PMID: 20826764

[3] WiegandKC, LeeAF, Al-AghaOM, et al. . Loss of BAF250a (ARID1A) is frequent in high-grade endometrial carcinomas. J Pathol, 2011, 224(3): 328-333 PMID: 21590771

[4] GuanB, MaoTL, PanugantiPK, et al. . Mutation and loss of expression of ARID1A in uterine low-grade endometrioid carcinoma. Am J Surg Pathol, 2011, 35(5): 625-632 PMCID: 3077471 PMID: 21412130

[5] StreppelMM, LataS, DelaBastideM, et al. . Next-generation sequencing of endoscopic biopsies identifies ARID1A as a tumor-suppressor gene in Barrett’s esophagus. Oncogene, 2014, 33(3): 347-357 PMCID: 3805724 PMID: 23318448

[6] ChandlerRL, BrennanJ, SchislerJC, et al. . ARID1a-DNA interactions are required for promoter occupancy by SWI/SNF. Mol Cell Biol, 2013, 33(2): 265-280 PMCID: 3554127 PMID: 23129809

[7] WiegandKC, ShahSP, Al-AghaOM, et al. . ARID1A mutations in endometriosis-associated ovarian carcinomas. New Engl J Med, 2010, 363(16): 1532-1543 PMCID: 2976679 PMID: 20942669

[8] ZhangZM, XiaoS, SunGY, et al. . The clinicopathologic significance of the loss of BAF250a (ARID1A) expression in endometrial carcinoma. Int J Gynecol Cancer, 2014, 24(3): 534-540 PMID: 24557437

[9] ChoH, KimJS, ChungH, et al. . Loss of ARID1A/BAF250a expression is linked to tumor progression and adverse prognosis in cervical cancer. Hum Pathol, 2013, 44(7): 1365-1374 PMID: 23427874

[10] WiegandKC, SyK, KallogerSE, et al. . ARID1A/BAF250a as a prognostic marker for gastric carcinoma: a study of 2 cohorts. Hum Pathol, 2014, 45(6): 1258-1268 PMID: 24767857

[11] TakebayashiS, LeiI, RybaT, et al. . Murine esBAF chromatin remodeling complex subunits BAF250a and Brg1 are necessary to maintain and reprogram pluripotency-specific replication timing of select replication domains. Epigenet Chromatin, 2013, 6(1): 42

[12] GaoX, TateP, HuP, et al. . ES cell pluripotency and germ-layer formation require the SWI/SNF chromatin remodeling component BAF250a. P Natl Acad Sci USA, 2008, 105(18): 6656-6661

[13] IwaharaJ, ClubbRT. Solution structure of the DNA binding domain from Dead ringer, a sequence-specific AT-rich interaction domain (ARID). Embo J, 1999, 18(21): 6084-6094 PMCID: 1171673 PMID: 10545119

[14] WhitsonRH, HuangT, ItakuraK. The novel Mrf-2 DNA-binding domain recognizes a five-base core sequence through major and minor-groove contacts. Biochem Bioph Res Co, 1999, 258(2): 326-331

[15] WilskerD, PatsialouA, ZumbrunSD, et al. . The DNA-binding properties of the ARID-containing subunits of yeast and mammalian SWI/SNF complexes. Nucleic Acids Res, 2004, 32(4): 1345-1353 PMCID: 390273 PMID: 14982958

[16] DallasPB, PacchioneS, WilskerD, et al. . The human SWI-SNF complex protein p270 is an ARID family member with non-sequence-specific DNA binding activity. Mol Cell Biol, 2000, 20(9): 3137-3146 PMCID: 85608 PMID: 10757798

[17] WangT, ZhangJ, ZhangX, et al. . Solution structure of SWI1 AT-rich interaction domain from Saccharomyces cerevisiae and its nonspecific binding to DNA. Proteins, 2012, 80(7): 1911-1917 PMID: 22488857

[18] WilskerD, PatsialouA, DallasPB, et al. . ARID proteins: a diverse family of DNA binding proteins implicated in the control of cell growth, differentiation, and development. Cell Growth Differ, 2002, 13(3): 95-106 PMID: 11959810

[19] KimS, ZhangZ, UpchurchS, et al. . Structure and DNA-binding sites of the SWI1 AT-rich interaction domain (ARID) suggest determinants for sequence-specific DNA recognition. J Biol Chem, 2004, 279(16): 16670-16676 PMID: 14722072

[20] CaiS, ZhuLY, ZhangZM, et al. . Determination of the three-dimensional structure of the Mrf2-DNA complex using paramagnetic spin labeling. Biochemistry, 2007, 46(17): 4943-4950 PMCID: 2527749 PMID: 17407261

[21] IwaharaJ, IwaharaM, DaughdrillGW, et al. . The structure of the Dead ringer-DNA complex reveals how AT-rich interaction domains (ARIDs) recognize DNA. Embo J, 2002, 21(5): 1197-1209 PMCID: 125891 PMID: 11867548

[22] RitchieDW, VenkatramanV. Ultra-fast FFT protein docking on graphics processors. Bioinformatics, 2010, 26(19): 2398-2405 PMID: 20685958

[23] PhillipsJC, BraunR, WangW, et al. . Scalable molecular dynamics with NAMD. J Comput Chem, 2005, 26(16): 1781-1802 PMCID: 2486339 PMID: 16222654

[24] EwaldPP. Die Berechnung optischer und elektrostatischer Gitterpotentiale. Ann Phys (German), 1921, 369(3): 253-287

[25] DeLano WL. The PyMOL molecular graphics system, www.pymol.org. CA

[26] Von HippelPH. From “simple” DNA-protein interactions to the macromolecular machines of gene expression. Annu Rev Bioph Biom, 2007, 36: 79-105

[27] RohsR, JinX, WestSM, et al. . Origins of specificity in protein-DNA recognition. Annu Rev Biochem, 2010, 79: 233-269 PMCID: 3285485 PMID: 20334529

[28] KalodimosCG, BirisN, BonvinAM, et al. . Structure and flexibility adaptation in nonspecific and specific protein-DNA complexes. Science, 2004, 305(5682): 386-389 PMID: 15256668

[29] WilliamsLD, MaherLJ. Electrostatic mechanisms of DNA deformation. Annu Rev Bioph Biom, 2000, 29: 497-521

[30] PatsialouA, WilskerD, MoranE. DNA-binding properties of ARID family proteins. Nucleic Acids Res, 2005, 33(1): 66-80 PMCID: 546134 PMID: 15640446