A 1.55 Å resolution X-ray crystal structure of HEF2/ERH and insights into its transcriptional and cell-cycle interaction networks

Proteins: Structure, Function and Genetics

Volumn 68, Issue 2, 2007, Pages 427-437

  Jin, Tengchuan ^a   Guo, Feng ^a   Serebriiskii, Ilya G ^b   Howard, Andrew ^a   Zhang, Yu Zhu ^a  

^a ILLINOIS INSTITUTE OF TECHNOLOGY   (United States)

^b FOX CHASE CANCER CENTER   (United States)

Author keywords

Cell cycle; FCP1; HNF1; RNAPII; SPT5; Transcription factor; VHL

Indexed keywords

AMINO ACID; GENE PRODUCT; PROTEIN ERH; PROTEIN HEF2; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; CELL CYCLE PROTEIN; ERH PROTEIN, HUMAN;

ALPHA HELIX; ARTICLE; BETA SHEET; CELL CYCLE; CELL CYCLE PROGRESSION; CRYSTAL STRUCTURE; FUNGUS GROWTH; FUNGUS HYPHAE; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SACCHAROMYCES CEREVISIAE; STRUCTURE ANALYSIS; TRANSCRIPTION REGULATION; CELL DIVISION; CHEMICAL STRUCTURE; CHEMISTRY; CYTOLOGY; GENETIC TRANSFECTION; GENETICS; IMAGE PROCESSING; METABOLISM; MICROFILAMENT; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; POLYMERASE CHAIN REACTION; PROTEIN CONFORMATION; PROTEIN FOLDING; X RAY CRYSTALLOGRAPHY;

SACCHAROMYCETALES;

BASE SEQUENCE; CELL CYCLE; CELL CYCLE PROTEINS; CELL DIVISION; CRYSTALLOGRAPHY, X-RAY; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MICROFILAMENTS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; POLYMERASE CHAIN REACTION; PROTEIN CONFORMATION; PROTEIN FOLDING; SACCHAROMYCES CEREVISIAE; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TRANSFECTION;

EID: 34250795609     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.21343     Document Type: Article

References (59)

1. Buda A, Pignatelli M. Cytoskeletal network in colon cancer: from genes to clinical application. Int J Biochem Cell Biol 2004; 36:759-765.
2. Stehn JR, Schevzov G, O'Neill GM, Gunning PW. Specialisation of the tropomyosin composition of actin filaments provides new potential targets for chemotherapy. Curr Cancer Drug Targets 2006;6:245-256.
3. Hernandez SE, Krishnaswami M, Miller AL, Koleske AJ. How do Abl family kinases regulate cell shape and movement? Trends Cell Biol 2004;14:36-44.
4. Gimeno CJ, Ljungdahl PO, Styles CA, Fink GR. Unipolar cell divisions in the yeast S. cerevisiae lead to filamentous growth: regulation by starvation and RAS. Cell 1992;68:1077-1090.
5. Kron SJ, Styles CA, Fink GR. Symmetric cell division in pseudohyphae of the yeast Saccharomyces cerevisiae. Mol Biol Cell 1994; 5:1003-1022.
6. Rua D, Tobe BT, Kron SJ. Cell cycle control of yeast filamentous growth. Curr Opin Microbiol 2001;4:720-727.
7. Gancedo JM. Control of pseudohyphae formation in Saccharomyces cerevisiae. FEMS Microbiol Rev 2001;25:107-123.
8. Schneper L, Duvel K, Broach JR. Sense and sensibility: nutritional response and signal integration in yeast. Curr Opin Microbiol 2004;7:624-630.
9. Law SF, Estojak J, Wang B, Mysliwiec T, Kruh G, Golemis EA. Human enhancer of filamentation 1, a novel p130cas-like docking protein, associates with focal adhesion kinase and induces pseudohyphal growth in Saccharomyces cerevisiae. Mol Cell Biol 1996;16:3327-3337.
10. Pugacheva EN, Golemis EA. HEF1-aurora A interactions: points of dialog between the cell cycle and cell attachment signaling networks. Cell Cycle 2006;5:384-391.
11. Law SF, Zhang YZ, Fashena SJ, Toby G, Estojak J, Golemis EA. Dimerization of the docking/adaptor protein HEF1 via a carboxy-terminal helix-loop-helix domain. Exp Cell Res 1999,252: 224-235.
12. Dadke D, Jarnik M, Pugacheva EN, Singh MK, Golemis EA. Deregulation of HEF1 impairs M-phase progression by disrupting the RhoA activation cycle. Mol Biol Cell 2006;17:1204-1217.
13. Pugacheva EN, Golemis EA. The focal adhesion scaffolding protein HEF1 regulates activation of the Aurora-A and Nek2 kinases at the centrosome. Nat Cell Biol 2005;7:937-946.
14. Khazak V, Sadhale PP, Woychik NA, Brent R, Golemis EA. Human RNA polymerase II subunit hsRPB7 functions in yeast and influences stress survival and cell morphology. Mol Biol Cell 1995;6:759-775.
15. Einarson MB, Cukierman E, Compton DA, Golemis EA. Human enhancer of invasion-cluster, a coiled-coil protein required for passage through mitosis. Mol Cell Biol 2004;24:3957-3971.
16. Toby GG, Gherraby W, Coleman TR, Golemis EA. A novel RING finger protein, human enhancer of invasion 10, alters mitotic progression through regulation of cyclin B levels. Mol Cell Biol 2003;23:2109-2122.
17. Gronholm M, Muranen T, Toby GG, Utermark T, Hanemann CO, Golemis EA, Carpen O. A functional association between merlin and HEI10, a cell cycle regulator. Oncogene 2006;25:4389-4398.
18. Kim M, Gans JD, Nogueira C, Wang A, Paik JH, Feng B, Brennan C, Hahn WC, Cordon-Cardo C, Wagner SN, Flotte TJ, Duncan LM, Granter SR, Chin L. Comparative oncogenomics identifies NEDD9 as a melanoma metastasis gene. Cell 2006;125: 1269-1281.
19. Minn AJ, Gupta GP, Siegel PM, Bos PD, Shu W, Giri DD, Viale A, Olshen AB, Gerald WL, Massague J. Genes that mediate breast cancer metastasis to lung. Nature 2005;436:518-524.
20. Wojcik E, Murphy AM, Fares H, Dang-Vu K, Tsubota SI. Enhancer of rudimentarypl, e(r)p1, a highly conserved enhancer of the rudimentary gene. Genetics 1994;138:1163-1170.
21. Pacifico S, Liu G, Guest S, Parrish JR, Fotouhi F, Finley RL, Jr. A database and tool, IM Browser, for exploring and integrating emerging gene and protein interaction data for Drosophila. BMC Bioinformatics 2006;7:195.
22. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 2003;13:2498-2504.
23. Jin T, Howard AJ, Golemis EA, Wang Y, Zhang Y. Overexpression, purification, crystallization and preliminary X-ray diffraction studies of the human transcription repressor ERH. Acta Crystallograph Sect F Struct Biol Cryst Commun 2005;61:531-533.
24. Otwinowski Z, Minor W. Processing of X-ray diffraction data collected in oscillation mode. In: Sweet RM, editor. Methods in Enzymology, Vol. 276: Macromolecular Crystallography, part A. New York: Academic Press; 1997. pp 307-326.
25. Howard AJ. Data processing in macromolecular crystallography. In: Watenpauph KD, editor. Proceedings from the Macromolecular Crystallography Computing School, 1996, Vol.7: Crystallographic Computing. Oxford: Oxford University Press; 2000.
26. Weeks CM, Blessing RH, Miller R, Mungee R, Potter SA, Rappleye J, Smith GD, Xu H, Furey W. Towards automated protein structure determination: BnP, the SnB-PHASES interface. Z Kristallogr 2002;217:686-693.
27. Brunger AT, Adams PD, Clore GM, DeLano WL, Gros P, Grosse-Kunstleve RW, Jiang JS, Kuszewski J, Nilges M, Pannu NS, Read RJ, Rice LM, Simonson T, Warren GL. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr D Biol Crystallogr 1998;54:905-921.
28. Terwilliger TC. Automated structure solution, density modification and model building. Acta Crystallogr D Biol Crystallogr 2002; 58:1937-1940.
29. McRee DE. XtalView/Xfit-A versatile program for manipulating atomic coordinates and electron density. J Struct Biol 1999;125: 156-165.
30. Ritchie DW. Evaluation of protein docking predictions using Hex 3.1 in CAPRI rounds 1 and 2. Proteins 2003;52:98-106.
31. Pogge von Strandmann E, Senkel S, Ryffel GU. ERH (enhancer of rudimentary homologue), a conserved factor identical between frog and human, is a transcriptional repressor. Biol Chem 2001; 382:1379-1385.
32. Pontoglio M. Hepatocyte nuclear factor 1, a transcription factor at the crossroads of glucose homeostasis. J Am Soc Nephrol 2000;11 (Suppl 16):S140-S143.
33. Amente S, Napolitano G, Licciardo P, Monti M, Pucci P, Lania L, Majello B. Identification of proteins interacting with the RNAPII FCP1 phosphatase: FCP1 forms a complex with arginine methyl-transferase PRMT5 and it is a substrate for PRMT5-mediated methylation. FEBS Lett 2005;579:683-689.
34. Kwak YT, Guo J, Prajapati S, Park KJ, Surabhi RM, Miller B, Gehrig P, Gaynor RB. Methylation of SPT5 regulates its interaction with RNA polymerase II and transcriptional elongation properties. Mol Cell 2003;11:1055-1066.
35. Ponting CP. Novel domains and orthologues of eukaryotic transcription elongation factors. Nucleic Acids Res 2002;30:3643-3652.
36. Stelzl U, Worm U, Lalowski M, Haenig C, Brembeck FH, Goehler H, Stroedicke M, Zenkner M, Schoenherr A, Koeppen S, Timm J, Mintzlaff S, Abraham C, Bock N, Kietzmann S, Goedde A, Toksoz E, Droege A, Krobitsch S, Korn B, Birchmeier W, Lehrach H, Wanker EE. A human protein-protein interaction network: a resource for annotating the proteome. Cell 2005;122:957-968.
37. Licciardo P, Amente S, Ruggiero L, Monti M, Pucci P, Lania L, Majello B. The FCP1 phosphatase interacts with RNA polymerase II and with MEP50 a component of the methylosome complex involved in the assembly of snRNP. Nucleic Acids Res 2003; 31:999-1005.
38. Zhong J, Zhang H, Stanyon CA, Tromp G, Finley RL, Jr. A strategy for constructing large protein interaction maps using the yeast two-hybrid system: regulated expression arrays and two-phase mating. Genome Res 2003;13:2691-2699.
39. Bader GD, Betel D, Hogue CW. BIND: the Biomolecular Interaction Network Database. Nucleic Acids Res 2003;31:248-250.
40. Gelsthorpe M, Pulumati M, McCallum C, Dang-Vu K, Tsubota SI. The putative cell cycle gene, enhancer of rudimentary, encodes a highly conserved protein found in plants and animals. Gene 1997;186:189-195.
41. Bai C, Sen P, Hofmann K, Ma L, Goebl M, Harper JW, Elledge SJ. SKP1 connects cell cycle regulators to the ubiquitin proteolysis machinery through a novel motif, the F-box. Cell 1996;86: 263-274.
42. Connelly C, Hieter P. Budding yeast SKP1 encodes an evolutionarily conserved kinetochore protein required for cell cycle progression. Cell 1996;86:275-285.
43. Nishitani H, Sugimoto N, Roukos V, Nakanishi Y, Saijo M, Obuse C, Tsurimoto T, Nakayama KI, Nakayama K, Fujita M, Lygerou Z, Nishimoto T Two E3 ubiquitin ligases, SCF-Skp2 and DDB1-Cul4, target human Cdt1 for proteolysis. EMBO J 2006;25:1126-1136.
44. von der Lehr N, Johansson S, Larsson LG. Implication of the ubiquitin/proteasome system in Myc-regulated transcription. Cell Cycle 2003;2:403-407.
45. Li H, Inoue M, Yabuki T, Aoki M, Seki E, Matsuda T, Nunokawa E, Motoda Y, Kobayashi A, Terada T, Shirouzu M, Koshiba S, Lin YJ, Guntert P, Suzuki H, Hayashizaki Y, Kigawa T, Yokoyama S. Solution structure of the mouse enhancer of rudimentary protein reveals a novel fold. J Biomol NMR 2005;32:329-334.
46. Arai R, Kukimoto-Niino M, Uda-Tochio H, Morita S, Uchikubo-Kamo T, Akasaka R, Etou Y, Hayashizaki Y, Kigawa T, Terada T, Shirouzu M, Yokoyama S. Crystal structure of an enhancer of rudimentary homolog (ERH) at 2.1 Angstroms resolution. Protein Sci 2005;14:1888-1893.
47. Wan C, Tempel W, Liu ZJ, Wang BC, Rose RB. Structure of the conserved transcriptional repressor enhancer of rudimentary homolog. Biochemistry 2005;44:5017-5023.
48. Matthews BW. Solvent content of protein crystals. J Mol Biol 1968;33:491-497.
49. Hauer CR, Rebrin I, Thony B, Neuheiser F, Curtius HC, Hunziker P, Blau N, Ghisla S, Heizmann CW. Phenylalanine hydroxylase-stimulating protein/pterin-4 α-carbinolamine dehydratase from rat and human liver. Purification, characterization, and complete amino acid sequence. J Biol Chem 1993;268:4828-4831.
50. Huang CY, Max EE, Kaufman S. Purification and characterization of phenylalanine hydroxylase-stimulating protein from rat liver. J Biol Chem 1973;248:4235-4241.
51. Endrizzi JA, Cronk JD, Wang W, Crabtree GR, Alber T. Crystal structure of DCoH, a bifunctional, protein-binding transcriptional coactivator. Science 1995;268:556-559.
52. Cronk JD, Endrizzi JA, Alber T. High-resolution structures of the bifunctional enzyme and transcriptional coactivator DCoH and its complex with a product analogue. Protein Sci 1996;5: 1963-1972.
53. Narayana N, Hua Q, Weiss MA. The dimerization domain of HNF-1α: structure and plasticity of an intertwined four-helix bundle with application to diabetes mellitus. J Mol Biol 2001; 310:635-658.
54. Rose RB, Bayle JH, Endrizzi JA, Cronk JD, Crabtree GR, Alber T. Structural basis of dimerization, coactivator recognition and MODY3 mutations in HNF-1α. Nat Struct Biol 2000;7:744-748.
55. Chen F, Kishida T, Yao M, Hustad T, Glavac D, Dean M, Gnarra JR, Orcutt ML, Duh FM, Glenn G, Green J, Hsia YE, Lamiell J, Li H, Wei MH, Schmidt L, Tory K, Kuzmin I, Stackhouse T, Latif F, Linehan WM, Lerman M, Zbar B. Germline mutations in the von Hippel-Lindau disease tumor suppressor gene: correlations with phenotype. Hum Mutat 1995;5:66-75.
56. Schraml P, Struckmann K, Hatz F, Sonnet S, Kully C, Gasser T, Sauter G, Mihatsch MJ, Moch H. VHL mutations and their correlation with tumour cell proliferation, microvessel density, and patient prognosis in clear cell renal cell carcinoma. J Pathol 2002;196:186-193.
57. Shuin T, Kondo K, Ashida S, Okuda H, Yoshida M, Kanno H, Yao M. Germline and somatic mutations in von Hippel-Lindau disease gene and its significance in the development of kidney cancer. Contrib Nephrol 1999;128:1-10.
58. Smith AP, Weeraratna AT, Spears JR, Meltzer PS, Becker D. SAGE identification and fluorescence imaging analysis of genes and transcripts in melanomas and precursor lesions. Cancer Biol Ther 2004;3:104-109.
59. Kakiuchi S, Daigo Y, Tsunoda T, Yano S, Sone S, Nakamura Y. Genome-wide analysis of organ-preferential metastasis of human small cell lung cancer in mice. Mol Cancer Res 2003;1: 485-499.