Solution NMR structures of homeodomains from human proteins ALX4, ZHX1, and CASP8AP2 contribute to the structural coverage of the Human Cancer Protein Interaction Network

Journal of Structural and Functional Genomics - Tập 15 Số 4 - Trang 201-207 - 2014
Xu, Xianzhong1, Pulavarti, Surya V. S. R. K.1, Eletsky, Alexander1, Huang, Yuanpeng Janet2, Acton, Thomas B.2, Xiao, Rong2, Everett, John K.2, Montelione, Gaetano T.2,3, Szyperski, Thomas1
1Department of Chemistry, The State University of New York at Buffalo and Northeast Structural Genomics Consortium, Buffalo, USA
2Center of Advanced Biotechnology and Medicine and Department of Molecular Biology and Biochemistry, Rutgers, The State University of New Jersey and Northeast Structural Genomics Consortium, Piscataway, USA
3Department of Biochemistry and Molecular Biology, Robert Wood Johnson Medical School, UMDNJ, Piscataway, USA

Tóm tắt

High-quality solution NMR structures of three homeodomains from human proteins ALX4, ZHX1 and CASP8AP2 were solved. These domains were chosen as targets of a biomedical theme project pursued by the Northeast Structural Genomics Consortium. This project focuses on increasing the structural coverage of human proteins associated with cancer.

Tài liệu tham khảo

citation_journal_title=J Mol Biol; citation_title=SCOP: a structural classification of proteins database for the investigation of sequences and structures; citation_author=AG Murzin, SE Brenner, T Hubbard, C Chothia; citation_volume=247; citation_publication_date=1995; citation_pages=536-540; citation_id=CR1 citation_journal_title=Nucleic Acids Res; citation_title=The Pfam protein families database; citation_author=RD Finn, J Mistry, J Tate, P Coggill, A Heger, JE Pollington, OL Gavin, P Gunasekaran, G Ceric, K Forslund, L Holm, ELL Sonnhammer, SR Eddy, A Bateman; citation_volume=38; citation_publication_date=2010; citation_pages=D211-D222; citation_doi=10.1093/nar/gkp985; citation_id=CR2 citation_journal_title=Genes Dev; citation_title=Cooperative dimerization of paired class homeo domains on DNA; citation_author=D Wilson, G Sheng, T Lecuit, N Dostatni, C Desplan; citation_volume=7; citation_publication_date=1993; citation_pages=2120-2134; citation_doi=10.1101/gad.7.11.2120; citation_id=CR3 citation_journal_title=Development; citation_title=Physical and genetic interactions between Alx4 and Cart1; citation_author=S Qu, SC Tucker, Q Zhao, B deCrombrugghe, R Wisdom; citation_volume=126; citation_publication_date=1999; citation_pages=359-369; citation_id=CR4 citation_journal_title=J Med Genet; citation_title=The ALX4 homeobox gene is mutated in patients with ossification defects of the skull (foramina parietalia permagna, OMIM 1685000); citation_author=W Wuyts, E Cleiren, T Homfray, A Rasore-Quartino, F Vanhoenacker, HW Van; citation_volume=37; citation_publication_date=2000; citation_pages=916-920; citation_doi=10.1136/jmg.37.12.916; citation_id=CR5 citation_journal_title=Hum Mol Genet; citation_title=ALX4 dysfunction disrupts craniofacial and epidermal development; citation_author=H Kayserili, E Uz, C Niessen, I Vargel, Y Alanay, G Tuncbilek, G Yigit, O Uyguner, S Candan, H Okur, S Kaygin, S Balci, E Mavili, M Alikasifoglu, I Haase, B Wollnik, NA Akarsu; citation_volume=18; citation_publication_date=2009; citation_pages=4357-4366; citation_doi=10.1093/hmg/ddp391; citation_id=CR6 citation_journal_title=Dev Biol; citation_title=Loss of Alx4, a stromally-restricted homeodomain protein, impairs mammary epithelial morphogenesis; citation_author=PA Joshi, H Chang, PA Hamel; citation_volume=297; citation_publication_date=2006; citation_pages=284-294; citation_doi=10.1016/j.ydbio.2006.05.032; citation_id=CR7 citation_journal_title=Nature Genet; citation_title=Haploinsufficiency of the human homeobox gene ALX4 causes skull ossification defects; citation_author=LA Mavrogiannis, I Antonopoulou, A Baxova, S Kutilek, CA Kim, SM Sugayama, A Salamanca, SA Wall, GM Morriss-Kay, AOM Wilkie; citation_volume=27; citation_publication_date=2001; citation_pages=17-18; citation_doi=10.1038/83703; citation_id=CR8 Liu WB, Han F, Du XH, Jiang X, Li YH, Liu Y, Chen HQ, Ao L, Cui ZH, Cao J, Liu JY (2013) Epigenetic silencing of Aristaless-like homeobox-4, a potential tumor suppressor gene associated with lung cancer. Int J Cancer 134:1311–1322 citation_journal_title=Clin Cancer Res; citation_title=A novel set of DNA methylation markers in urine sediments for sensitive/specific detection of bladder cancer; citation_author=J Yu, T Zhu, Z Wang, H Zhang, Z Qian, H Xu, B Gao, W Wang, L Gu, J Meng, J Wang, X Feng, Y Li, X Yao, J Zhu; citation_volume=13; citation_publication_date=2007; citation_pages=7296-7304; citation_doi=10.1158/1078-0432.CCR-07-0861; citation_id=CR10 citation_journal_title=Cancer Sci; citation_title=High CpG island methylator phenotype is associated with lymph node metastasis and prognosis in gastric cancer; citation_author=HY Chen, BH Zhu, CH Zhang, DJ Yang, JJ Peng, JH Chen, FK Liu, YL He; citation_volume=103; citation_publication_date=2012; citation_pages=73-79; citation_doi=10.1111/j.1349-7006.2011.02129.x; citation_id=CR11 citation_journal_title=Gastroenterology; citation_title=Aristaless-like homeobox-4 gene methylation is a potential marker for colorectal adenocarcinomas; citation_author=MP Ebert, F Model, S Mooney, K Hale, J Lograsso, L Tonnes-Priddy, J Hoffmann, A Csepregi, C Rocken, B Molnar, HU Schulz, P Malfertheiner, C Lofton-Day; citation_volume=131; citation_publication_date=2006; citation_pages=1418-1430; citation_doi=10.1053/j.gastro.2006.08.034; citation_id=CR12 citation_journal_title=PLoS ONE; citation_title=Performance of epigenetic markers SEPT9 and ALX4 in plasma for detection of colorectal precancerous lesions; citation_author=M Tanzer, B Balluff, J Distler, K Hale, A Leodolter, C Rocken, B Molnar, R Schmid, C Lofton-Day, T Schuster, MP Ebert; citation_volume=5; citation_publication_date=2010; citation_pages=e9061; citation_doi=10.1371/journal.pone.0009061; citation_id=CR13 citation_journal_title=Cancer Epidemiol Biomark Prev; citation_title=Highly methylated genes in colorectal neoplasia: implications for screening; citation_author=H Zou, JJ Harrington, AM Shire, RL Rego, L Wang, ME Campbell, AL Oberg, DA Ahlquist; citation_volume=16; citation_publication_date=2007; citation_pages=2686-2696; citation_doi=10.1158/1055-9965.EPI-07-0518; citation_id=CR14 citation_journal_title=J Clin Pathol; citation_title=Loss of ALX4 expression in epithelial cells and adjacent stromal cells in breast cancer; citation_author=H Chang, N Mohabir, S Done, PA Hamel; citation_volume=62; citation_publication_date=2009; citation_pages=908-914; citation_doi=10.1136/jcp.2009.067298; citation_id=CR15 citation_journal_title=Biochem Biophys Res Commun; citation_title=Human ZHX1: cloning, chromosomal location, and interaction with transcription factor NF-Y; citation_author=K Yamada, RL Printz, H Osawa, DK Granner; citation_volume=261; citation_publication_date=1999; citation_pages=614-621; citation_doi=10.1006/bbrc.1999.1087; citation_id=CR16 citation_journal_title=J Cell Biochem; citation_title=The SUMOylation of zinc-fingers and homeoboxes 1 (ZHX1) by Ubc9 regulates its stability and transcriptional repression activity; citation_author=S Chen, X Yu, Q Lei, L Ma, D Guo; citation_volume=114; citation_publication_date=2013; citation_pages=2323-2333; citation_doi=10.1002/jcb.24579; citation_id=CR17 citation_journal_title=Biochem Biophys Res Commun; citation_title=Zinc-fingers and homeoboxes 1 (ZHX1) binds DNA methyltransferase (DNMT) 3B to enhance DNMT3B-mediated transcriptional repression; citation_author=SH Kim, J Park, MC Choi, HP Kim, JH Park, Y Jung, JH Lee, DY Oh, SA Im, YJ Bang, TY Kim; citation_volume=355; citation_publication_date=2007; citation_pages=318-323; citation_doi=10.1016/j.bbrc.2007.01.187; citation_id=CR18 citation_journal_title=FEBS Lett; citation_title=Identification of proteins that interact with NF-YA; citation_author=K Yamada, H Osawa, DK Granner; citation_volume=460; citation_publication_date=1999; citation_pages=41-45; citation_doi=10.1016/S0014-5793(99)01311-3; citation_id=CR19 citation_journal_title=Kidney Int; citation_title=Early changes in gene expression that influence the course of primary glomerular disease; citation_author=LC Clement, G Liu, I Perez-Torres, YS Kanwar, C Avila-Casado, SS Chugh; citation_volume=72; citation_publication_date=2007; citation_pages=337-347; citation_doi=10.1038/sj.ki.5002302; citation_id=CR20 citation_journal_title=J Biol Chem; citation_title=ZHX proteins regulate podocyte gene expression during the development of nephrotic syndrome; citation_author=G Liu, LC Clement, YS Kanwar, C Avila-Casado, SS Chugh; citation_volume=281; citation_publication_date=2006; citation_pages=39681-39692; citation_doi=10.1074/jbc.M606664200; citation_id=CR21 citation_journal_title=Cell Mol Life Sci; citation_title=Three classes of C2H2 zinc finger proteins; citation_author=S Iuchi; citation_volume=58; citation_publication_date=2001; citation_pages=625-635; citation_doi=10.1007/PL00000885; citation_id=CR22 citation_journal_title=Biochem Biophys Res Commun; citation_title=Functional analysis and the molecular dissection of zinc-fingers and homeoboxes 1 (ZHX1); citation_author=K Yamada, H Kawata, K Matsuura, Z Shou, S Hirano, T Mizutani, T Yazawa, M Yoshino, T Sekiguchi, T Kajitani, K Miyamoto; citation_volume=297; citation_publication_date=2002; citation_pages=368-374; citation_doi=10.1016/S0006-291X(02)02203-9; citation_id=CR23 citation_journal_title=Biochem J; citation_title=Analysis of zinc-fingers and homeoboxes (ZHX)-1-interacting proteins: molecular cloning and characterization of a member of the ZHX family, ZHX3; citation_author=K Yamada, H Kawata, Z Shou, S Hirano, T Mizutani, T Yazawa, T Sekiguchi, M Yoshino, T Kajitani, K Miyamoto; citation_volume=373; citation_publication_date=2003; citation_pages=167-178; citation_doi=10.1042/BJ20021866; citation_id=CR24 citation_journal_title=Biochemistry; citation_title=The tandem zinc-finger region of human ZHX adopts a novel C2H2 zinc finger structure with a C-terminal extension; citation_author=H Wienk, I Lammers, A Hotze, J Wu, RW Wechselberger, R Owens, DK Stammers, D Stuart, R Kaptein, GE Folkers; citation_volume=48; citation_publication_date=2009; citation_pages=4431-4439; citation_doi=10.1021/bi9001997; citation_id=CR25 citation_journal_title=BMC Struct Biol; citation_title=Novel structural features in two ZHX homeodomains derived from a systematic study of single and multiple domains; citation_author=L Bird, J Ren, J Nettleship, G Folkers, R Owens, D Stammers; citation_volume=10; citation_publication_date=2010; citation_pages=13; citation_doi=10.1186/1472-6807-10-13; citation_id=CR26 citation_journal_title=J Steroid Biochem Mol Biol; citation_title=FLASH interacts with p160 coactivator subtypes and differentially suppresses transcriptional activity of steroid hormone receptors; citation_author=T Kino, T Ichijo, GP Chrousos; citation_volume=92; citation_publication_date=2004; citation_pages=357-363; citation_doi=10.1016/j.jsbmb.2004.09.003; citation_id=CR27 citation_journal_title=Proc Natl Acad Sci USA; citation_title=FLASH is required for histone transcription and S-phase progression; citation_author=D Barcaroli, L Bongiorno-Borbone, A Terrinoni, TG Hofmann, M Rossi, RA Knight, AG Matera, G Melino, V Laurenzi; citation_volume=103; citation_publication_date=2006; citation_pages=14808-14812; citation_doi=10.1073/pnas.0604227103; citation_id=CR28 citation_journal_title=EMBO J; citation_title=FLASH links the CD95 signaling pathway to the cell nucleus and nuclear bodies; citation_author=K Milovic-Holm, E Krieghoff, K Jensen, H Will, TG Hofmann; citation_volume=26; citation_publication_date=2007; citation_pages=391-401; citation_doi=10.1038/sj.emboj.7601504; citation_id=CR29 citation_journal_title=Leuk Res; citation_title=CASP8AP2 is a promising prognostic indicator in pediatric acute lymphoblastic leukemia; citation_author=Y Jiao, L Cui, C Gao, W Li, X Zhao, S Liu, M Wu, G Deng, Z Li; citation_volume=36; citation_publication_date=2012; citation_pages=67-71; citation_doi=10.1016/j.leukres.2011.05.023; citation_id=CR30 citation_journal_title=Blood; citation_title=Genes contributing to minimal residual disease in childhood acute lymphoblastic leukemia: prognostic significance of CASP8AP2; citation_author=C Flotho, E Coustan-Smith, D Pei, S Iwamoto, G Song, C Cheng, CH Pui, JR Downing, D Campana; citation_volume=108; citation_publication_date=2006; citation_pages=1050-1057; citation_doi=10.1182/blood-2006-01-0322; citation_id=CR31 citation_journal_title=Mol Cell Biol; citation_title=Interaction of FLASH with arsenite resistance protein 2 is involved in cell cycle progression at S phase; citation_author=M Kiriyama, Y Kobayashi, M Saito, F Ishikawa, S Yonehara; citation_volume=29; citation_publication_date=2009; citation_pages=4729-4741; citation_doi=10.1128/MCB.00289-09; citation_id=CR32 citation_journal_title=J Biol Chem; citation_title=Tumor necrosis factor alpha receptor- and Fas-associated FLASH inhibit transcriptional activity of the glucocorticoid receptor by binding to and interfering with its interaction with p160 type nuclear receptor coactivators; citation_author=T Kino, GP Chrousos; citation_volume=278; citation_publication_date=2003; citation_pages=3023-3029; citation_doi=10.1074/jbc.M209234200; citation_id=CR33 citation_journal_title=Mol Cell Proteomics; citation_title=Targeting the human cancer pathway protein interaction network by structural genomics; citation_author=YJ Huang, D Hang, LJ Lu, L Tong, MB Gerstein, GT Montelione; citation_volume=7; citation_publication_date=2008; citation_pages=2048-2060; citation_doi=10.1074/mcp.M700550-MCP200; citation_id=CR34 citation_journal_title=Methods Enzymol; citation_title=Robotic cloning and protein production platform of the Northeast Structural Genomics Consortium; citation_author=TB Acton, KC Gunsalus, R Xiao, LC Ma, J Aramini, MC Baran, YW Chiang, T Climent, B Cooper, NG Denissova, SM Douglas, JK Everett, CK Ho, D Macapagal, PK Rajan, R Shastry, LY Shih, GVT Swapna, M Wilson, M Wu, M Gerstein, M Inouye, JF Hunt, GT Montelione; citation_volume=394; citation_publication_date=2005; citation_pages=210-243; citation_doi=10.1016/S0076-6879(05)94008-1; citation_id=CR35 citation_journal_title=Methods Enzymol; citation_title=Preparation of protein samples for NMR structure, function, and small-molecule screening studies; citation_author=TB Acton, R Xiao, S Anderson, J Aramini, WA Buchwald, C Ciccosanti, K Conover, J Everett, K Hamilton, YJ Huang, H Janjua, G Kornhaber, J Lau, DY Lee, GH Liu, M Maglaqui, LC Ma, L Mao, D Patel, P Rossi, S Sahdev, R Shastry, GVT Swapna, YF Tang, SC Tong, DY Wang, H Wang, L Zhao, GT Montelione; citation_volume=493; citation_publication_date=2011; citation_pages=21-60; citation_doi=10.1016/B978-0-12-381274-2.00002-9; citation_id=CR36 citation_journal_title=J Struct Biol; citation_title=The high-throughput protein sample production platform of the Northeast Structural Genomics Consortium; citation_author=R Xiao, S Anderson, J Aramini, R Belote, WA Buchwald, C Ciccosanti, K Conover, JK Everett, K Hamilton, YJ Huang, H Janjua, M Jiang, GJ Kornhaber, DY Lee, JY Locke, LC Ma, M Maglaqui, L Mao, S Mitra, D Patel, P Rossi, S Sahdev, S Sharma, R Shastry, GVT Swapna, SN Tong, D Wang, H Wang, L Zhao, GT Montelione, TB Acton; citation_volume=172; citation_publication_date=2010; citation_pages=21-33; citation_doi=10.1016/j.jsb.2010.07.011; citation_id=CR37 citation_journal_title=Biochemistry; citation_title=Stereospecific nuclear magnetic resonance assignments of the methyl groups of valine and leucine in the DNA-binding domain of the 434 repressor by biosynthetically directed fractional 13C labeling; citation_author=D Neri, T Szyperski, G Otting, H Senn, K Wuthrich; citation_volume=28; citation_publication_date=1989; citation_pages=7510-7516; citation_doi=10.1021/bi00445a003; citation_id=CR38 citation_journal_title=Methods Enzymol; citation_title=Automatic determination of protein backbone resonance assignments from triple resonance nuclear magnetic resonance data; citation_author=HNB Moseley, D Monleon, GT Montelione; citation_volume=339; citation_publication_date=2001; citation_pages=91-108; citation_doi=10.1016/S0076-6879(01)39311-4; citation_id=CR39 citation_journal_title=J Mol Biol; citation_title=Automated analysis of protein NMR assignments using methods from artificial intelligence; citation_author=DE Zimmerman, CA Kulikowski, YP Huang, WQ Feng, M Tashiro, S Shimotakahara, CY Chien, R Powers, GT Montelione; citation_volume=269; citation_publication_date=1997; citation_pages=592-610; citation_doi=10.1006/jmbi.1997.1052; citation_id=CR40 citation_journal_title=J Am Chem Soc; citation_title=Protein NMR recall, precision, and F-measure scores (RPF scores): structure quality assessment measures based on information retrieval statistics; citation_author=YJ Huang, R Powers, GT Montelione; citation_volume=127; citation_publication_date=2005; citation_pages=1665-1674; citation_doi=10.1021/ja047109h; citation_id=CR41 citation_journal_title=Proc Natl Acad Sci USA; citation_title=NMR data collection and analysis protocol for high-throughput protein structure determination; citation_author=G Liu, Y Shen, HS Atreya, D Parish, Y Shao, DK Sukumaran, R Xiao, A Yee, A Lemak, A Bhattacharya, TA Acton, CH Arrowsmith, GT Montelione, T Szyperski; citation_volume=102; citation_publication_date=2005; citation_pages=10487-10492; citation_doi=10.1073/pnas.0504338102; citation_id=CR42 citation_journal_title=J Mol Biol; citation_title=Torsion angle dynamics for NMR structure calculation with the new program DYANA; citation_author=P Güntert, C Mumenthaler, K Wüthrich; citation_volume=273; citation_publication_date=1997; citation_pages=283-298; citation_doi=10.1006/jmbi.1997.1284; citation_id=CR43 citation_journal_title=J Mol Biol; citation_title=Protein NMR structure determination with automated NOE assignment using the new software CANDID and the torsion angle dynamics algorithm DYANA; citation_author=T Herrmann, P Güntert, K Wüthrich; citation_volume=319; citation_publication_date=2002; citation_pages=209-227; citation_doi=10.1016/S0022-2836(02)00241-3; citation_id=CR44 citation_journal_title=Proteins; citation_title=A topology-constrained distance network algorithm for protein structure determination from NOESY data; citation_author=YJ Huang, R Tejero, R Powers, GT Montelione; citation_volume=62; citation_publication_date=2006; citation_pages=587-603; citation_doi=10.1002/prot.20820; citation_id=CR45 citation_journal_title=J Biomol NMR; citation_title=Protein backbone angle restraints from searching a database for chemical shift and sequence homology; citation_author=G Cornilescu, F Delaglio, A Bax; citation_volume=13; citation_publication_date=1999; citation_pages=289-302; citation_doi=10.1023/A:1008392405740; citation_id=CR46 citation_journal_title=Acta Crystallogr Sect D: Biol Crystallogr; citation_title=Crystallography & NMR system: a new software suite for macromolecular structure determination; citation_author=AT Brunger, PD Adams, GM Clore, WL DeLano, P Gros, RW Grosse-Kunstleve, JS Jiang, J Kuszewski, M Nilges, NS Pannu, RJ Read, LM Rice, T Simonson, GL Warren; citation_volume=54; citation_publication_date=1998; citation_pages=905-921; citation_doi=10.1107/S0907444998003254; citation_id=CR47 citation_journal_title=Proteins ; citation_title=Evaluating protein structures determined by structural genomics consortia; citation_author=A Bhattacharya, R Tejero, GT Montelione; citation_volume=66; citation_publication_date=2007; citation_pages=778-795; citation_doi=10.1002/prot.21165; citation_id=CR48 citation_journal_title=Nucleic Acids Res; citation_title=The protein data bank; citation_author=HM Berman, J Westbrook, Z Feng, G Gilliland, TN Bhat, H Weissig, IN Shindyalov, PE Bourne; citation_volume=28; citation_publication_date=2000; citation_pages=235-242; citation_doi=10.1093/nar/28.1.235; citation_id=CR49 citation_journal_title=Annu Rev Biochem; citation_title=Homeodomain proteins; citation_author=WJ Gehring, M Affolter, T Burglin; citation_volume=63; citation_publication_date=1994; citation_pages=487-526; citation_doi=10.1146/annurev.bi.63.070194.002415; citation_id=CR50 citation_journal_title=Trends Biochem Sci; citation_title=Dali: a network tool for protein structure comparison; citation_author=L Holm, C Sander; citation_volume=20; citation_publication_date=1995; citation_pages=478-480; citation_doi=10.1016/S0968-0004(00)89105-7; citation_id=CR51 citation_journal_title=The EMBO Journal; citation_title=Cooperative DNA-binding and sequence-recognition mechanism of aristaless and clawless; citation_author=K Miyazono, Y Zhi, Y Takamura, K Nagata, K Saigo, T Kojima, M Tanokura; citation_volume=29; citation_publication_date=2010; citation_pages=1613-1623; citation_doi=10.1038/emboj.2010.53; citation_id=CR52 citation_journal_title=J Biol Chem; citation_title=Site-specific heterodimerization by paired-class homeodomain proteins mediates selective transcriptional responses; citation_author=SC Tucker, R Wisdom; citation_volume=274; citation_publication_date=1999; citation_pages=32325-32332; citation_doi=10.1074/jbc.274.45.32325; citation_id=CR53 citation_journal_title=Dev Biol; citation_title=A concerted action of a paired-type homeobox gene, aristaless, and a homolog of Hox11/tlx homeobox gene, clawless, is essential for the distal tip development of the Drosophila leg; citation_author=T Kojima, T Tsuji, K Saigo; citation_volume=279; citation_publication_date=2005; citation_pages=434-445; citation_doi=10.1016/j.ydbio.2004.12.005; citation_id=CR54 citation_journal_title=Nature; citation_title=Interaction between two homeodomain proteins is specified by a short C-terminal tail; citation_author=MR Stark, AD Johnson; citation_volume=371; citation_publication_date=1994; citation_pages=429-432; citation_doi=10.1038/371429a0; citation_id=CR55 citation_journal_title=J Biomol NMR; citation_title=Assignment validation software suite for the evaluation and presentation of protein resonance assignment data; citation_author=HNB Moseley, G Sahota, GT Montelione; citation_volume=28; citation_publication_date=2004; citation_pages=341-355; citation_doi=10.1023/B:JNMR.0000015420.44364.06; citation_id=CR56