Structural basis of multisite single-stranded DNA recognition and acta2 repression by purine-rich element binding protein B (Purβ)

Biochemistry

Volumn 52, Issue 26, 2013, Pages 4439-4450

  Rumora, Amy E ^a   Wang, Shu Xia ^b   Ferris, Lauren A ^a   Everse, Stephen J ^b   Kelm, Robert J ^a,b,c  

^a UNIVERSITY OF VERMONT   (United States)

^b UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

^c University of Vermont Colchester Research Facility   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMICAL ANALYSIS; CO-OPERATIVE ASSEMBLY; ELEMENT-BINDING PROTEINS; INTRAMOLECULAR INTERACTIONS; MOUSE EMBRYO FIBROBLASTS; PROTEIN-PROTEIN INTERACTIONS; QUATERNARY STRUCTURE; STRUCTURAL ARRANGEMENT;

BINDING SITES; BIOASSAY; CELL CULTURE; DNA; FIBROBLASTS; GENE ENCODING; TRANSCRIPTION;

PROTEINS;

ALPHA SMOOTH MUSCLE ACTIN; BINDING PROTEIN; PURINE RICH ELEMENT BINDING PROTEIN B; SHORT HAIRPIN RNA; SINGLE STRANDED DNA; UNCLASSIFIED DRUG;

ACTA2 GENE; ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; BINDING SITE; CELL DIFFERENTIATION; CELL MIGRATION; CELL STRUCTURE; CHEMICAL ANALYSIS; CONTROLLED STUDY; DNA BINDING; DNA STRUCTURE; EMBRYO; EXPRESSION VECTOR; FIBROBLAST; GENE; GENE REPRESSION; GENE SILENCING; IMMUNOBLOTTING; MOUSE; MOUSE EMBRYO; MYOFIBROBLAST; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; TRANSIENT TRANSFECTION;

ACTINS; ANIMALS; BINDING SITES; CELL DIFFERENTIATION; DNA, SINGLE-STRANDED; DNA-BINDING PROTEINS; ENHANCER ELEMENTS, GENETIC; FIBROBLASTS; MICE; MYOFIBROBLASTS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PURINES;

EID: 84880155869     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi400283r     Document Type: Article

References (69)

1. Walker, G. A., Guerrero, I. A., and Leinwand, L. A. (2001) Myofibroblasts: Molecular crossdressers Curr. Top. Dev. Biol. 51, 91-107
2. Tomasek, J. J., Gabbiani, G., Hinz, B., Chaponnier, C., and Brown, R. A. (2002) Myofibroblasts and mechano-regulation of connective tissue remodelling Nat. Rev. Mol. Cell Biol. 3, 349-363
3. Gabbiani, G., Ryan, G. B., and Majne, G. (1971) Presence of modified fibroblasts in granulation tissue and their possible role in wound contraction Experientia 27, 549-550
4. Gabbiani, G., Hirschel, B. J., Ryan, G. B., Statkov, P. R., and Majno, G. (1972) Granulation tissue as a contractile organ. A study of structure and function J. Exp. Med. 135, 719-734
5. Hinz, B. (2007) Formation and function of the myofibroblast during tissue repair J. Invest. Dermatol. 127, 526-537
6. Hinz, B., Phan, S. H., Thannickal, V. J., Galli, A., Bochaton-Piallat, M. L., and Gabbiani, G. (2007) The myofibroblast: One function, multiple origins Am. J. Pathol. 170, 1807-1816
7. De Wever, O. and Mareel, M. (2003) Role of tissue stroma in cancer cell invasion J. Pathol. 200, 429-447
8. Zalewski, A., Shi, Y., and Johnson, A. G. (2002) Diverse origin of intimal cells: smooth muscle cells, myofibroblasts, fibroblasts, and beyond? Circ. Res. 91, 652-655
9. Hao, H., Gabbiani, G., Camenzind, E., Bacchetta, M., Virmani, R., and Bochaton-Piallat, M. L. (2006) Phenotypic modulation of intima and media smooth muscle cells in fatal cases of coronary artery lesion Arterioscler., Thromb., Vasc. Biol. 26, 326-332
10. Darby, I., Skalli, O., and Gabbiani, G. (1990) Alpha-smooth muscle actin is transiently expressed by myofibroblasts during experimental wound healing Lab. Invest. 63, 21-29
11. Wang, J., Zohar, R., and McCulloch, C. A. (2006) Multiple roles of alpha-smooth muscle actin in mechanotransduction Exp. Cell Res. 312, 205-214
12. Hinz, B., Celetta, G., Tomasek, J. J., Gabbiani, G., and Chaponnier, C. (2001) Alpha-smooth muscle actin expression upregulates fibroblast contractile activity Mol. Biol. Cell 12, 2730-2741
13. Stoflet, E. S., Schmidt, L. J., Elder, P. K., Korf, G. M., Foster, D. N., Strauch, A. R., and Getz, M. J. (1992) Activation of a muscle-specific actin gene promoter in serum-stimulated fibroblasts Mol. Biol. Cell 3, 1073-1083
14. Foster, D. N., Min, B., Foster, L. K., Stoflet, E. S., Sun, S., Getz, M. J., and Strauch, A. R. (1992) Positive and negative cis-acting regulatory elements mediate expression of the mouse vascular smooth muscle alpha-actin gene J. Biol. Chem. 267, 11995-12003
15. Sun, S., Stoflet, E. S., Cogan, J. G., Strauch, A. R., and Getz, M. J. (1995) Negative regulation of the vascular smooth muscle alpha-actin gene in fibroblasts and myoblasts: disruption of enhancer function by sequence-specific single-stranded-DNA-binding proteins Mol. Cell. Biol. 15, 2429-2436
16. Subramanian, S. V., Polikandriotis, J. A., Kelm, R. J., Jr., David, J. J., Orosz, C. G., and Strauch, A. R. (2004) Induction of vascular smooth muscle alpha-actin gene transcription in transforming growth factor beta1-activated myofibroblasts mediated by dynamic interplay between the Pur repressor proteins and Sp1/Smad coactivators Mol. Biol. Cell 15, 4532-4543
17. Carlini, L. E., Getz, M. J., Strauch, A. R., and Kelm, R. J., Jr. (2002) Cryptic MCAT enhancer regulation in fibroblasts and smooth muscle cells. Suppression of TEF-1 mediated activation by the single-stranded DNA-binding proteins, Pur alpha, Pur beta, and MSY1 J. Biol. Chem. 277, 8682-8692
18. Gan, Q., Yoshida, T., Li, J., and Owens, G. K. (2007) Smooth muscle cells and myofibroblasts use distinct transcriptional mechanisms for smooth muscle alpha-actin expression Circ. Res. 101, 883-892
19. Sandbo, N., Kregel, S., Taurin, S., Bhorade, S., and Dulin, N. O. (2009) Critical role of serum response factor in pulmonary myofibroblast differentiation induced by TGF-beta Am. J. Respir. Cell Mol. Biol. 41, 332-338
20. Cogan, J. G., Subramanian, S. V., Polikandriotis, J. A., Kelm, R. J., Jr., and Strauch, A. R. (2002) Vascular smooth muscle alpha-actin gene transcription during myofibroblast differentiation requires Sp1/3 protein binding proximal to the MCAT enhancer J. Biol. Chem. 277, 36433-36442
21. Cogan, J. G., Sun, S., Stoflet, E. S., Schmidt, L. J., Getz, M. J., and Strauch, A. R. (1995) Plasticity of vascular smooth muscle alpha-actin gene transcription. Characterization of multiple, single-, and double-strand specific DNA-binding proteins in myoblasts and fibroblasts J. Biol. Chem. 270, 11310-11321
22. Kelm, R. J., Jr., Cogan, J. G., Elder, P. K., Strauch, A. R., and Getz, M. J. (1999) Molecular interactions between single-stranded DNA-binding proteins associated with an essential MCAT element in the mouse smooth muscle alpha-actin promoter J. Biol. Chem. 274, 14238-14245
23. Bergemann, A. D. and Johnson, E. M. (1992) The HeLa Pur factor binds single-stranded DNA at a specific element conserved in gene flanking regions and origins of DNA replication Mol. Cell. Biol. 12, 1257-1265
24. Bergemann, A. D., Ma, Z. W., and Johnson, E. M. (1992) Sequence of cDNA comprising the human pur gene and sequence-specific single-stranded-DNA-binding properties of the encoded protein Mol. Cell. Biol. 12, 5673-5682
25. Johnson, E. M., Daniel, D. C., and Gordon, J. (2013) The pur protein family: Genetic and structural features in development and disease J. Cell. Physiol. 228, 930-937
26. Kelm, R. J., Jr., Elder, P. K., Strauch, A. R., and Getz, M. J. (1997) Sequence of cDNAs encoding components of vascular actin single-stranded DNA-binding factor 2 establish identity to Puralpha and Purbeta J. Biol. Chem. 272, 26727-26733
27. Darbinian, N., Gallia, G. L., and Khalili, K. (2001) Helix-destabilizing properties of the human single-stranded DNA-and RNA-binding protein Puralpha J. Cell. Biochem. 80, 589-595
28. Wortman, M. J., Johnson, E. M., and Bergemann, A. D. (2005) Mechanism of DNA binding and localized strand separation by Pur alpha and comparison with Pur family member, Pur beta Biochim. Biophys. Acta 1743, 64-78
29. Kelm, R. J., Jr., Wang, S. X., Polikandriotis, J. A., and Strauch, A. R. (2003) Structure/function analysis of mouse Purbeta, a single-stranded DNA-binding repressor of vascular smooth muscle alpha-actin gene transcription J. Biol. Chem. 278, 38749-38757
30. Knapp, A. M., Ramsey, J. E., Wang, S. X., Godburn, K. E., Strauch, A. R., and Kelm, R. J., Jr. (2006) Nucleoprotein interactions governing cell type-dependent repression of the mouse smooth muscle alpha-actin promoter by single-stranded DNA-binding proteins Pur alpha and Pur beta J. Biol. Chem. 281, 7907-7918
31. Gupta, M., Sueblinvong, V., Raman, J., Jeevanandam, V., and Gupta, M. P. (2003) Single-stranded DNA-binding proteins PURalpha and PURbeta bind to a purine-rich negative regulatory element of the alpha-myosin heavy chain gene and control transcriptional and translational regulation of the gene expression. Implications in the repression of alpha-myosin heavy chain during heart failure J. Biol. Chem. 278, 44935-44948
32. Ji, J., Tsika, G. L., Rindt, H., Schreiber, K. L., McCarthy, J. J., Kelm, R. J., Jr., and Tsika, R. (2007) Puralpha and Purbeta collaborate with Sp3 to negatively regulate beta-myosin heavy chain gene expression during skeletal muscle inactivity Mol. Cell. Biol. 27, 1531-1543
33. Gupta, M., Sueblinvong, V., and Gupta, M. P. (2007) The single-strand DNA/RNA-binding protein, Purbeta, regulates serum response factor (SRF)-mediated cardiac muscle gene expression Can. J. Physiol. Pharmacol. 85, 349-359
34. McCarthy, J. J., Esser, K. A., Peterson, C. A., and Dupont-Versteegden, E. E. (2009) Evidence of MyomiR network regulation of beta-myosin heavy chain gene expression during skeletal muscle atrophy Physiol. Genomics 39, 219-226
35. van Rooij, E., Quiat, D., Johnson, B. A., Sutherland, L. B., Qi, X., Richardson, J. A., Kelm, R. J., Jr., and Olson, E. N. (2009) A family of microRNAs encoded by myosin genes governs myosin expression and muscle performance Dev. Cell 17, 662-673
36. Ramsey, J. E., Daugherty, M. A., and Kelm, R. J., Jr. (2007) Hydrodynamic studies on the quaternary structure of recombinant mouse Purbeta J. Biol. Chem. 282, 1552-1560
37. Ramsey, J. E. and Kelm, R. J., Jr. (2009) Mechanism of strand-specific smooth muscle alpha-actin enhancer interaction by purine-rich element binding protein B (Purbeta) Biochemistry 48, 6348-6360
38. Graebsch, A., Roche, S., Kostrewa, D., Soding, J., and Niessing, D. (2010) Of bits and bugs -on the use of bioinformatics and a bacterial crystal structure to solve a eukaryotic repeat-protein structure PLoS One 5 e13402
39. Graebsch, A., Roche, S., and Niessing, D. (2009) X-ray structure of Pur-alpha reveals a Whirly-like fold and an unusual nucleic-acid binding surface Proc. Natl. Acad. Sci. U. S. A. 106, 18521-18526
40. Rumora, A. E., Steere, A. N., Ramsey, J. E., Knapp, A. M., Ballif, B. A., and Kelm, R. J., Jr. (2010) Isolation and characterization of the core single-stranded DNA-binding domain of purine-rich element binding protein B (Purbeta) Biochem. Biophys. Res. Commun. 400, 340-345
41. Wang, J., Niu, W., Nikiforov, Y., Naito, S., Chernausek, S., Witte, D., LeRoith, D., Strauch, A., and Fagin, J. A. (1997) Targeted overexpression of IGF-I evokes distinct patterns of organ remodeling in smooth muscle cell tissue beds of transgenic mice J. Clin. Invest. 100, 1425-1439
42. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R., Thompson, J. D., Gibson, T. J., and Higgins, D. G. (2007) Clustal W and Clustal X version 2.0 Bioinformatics 23, 2947-2948
43. Goujon, M., McWilliam, H., Li, W., Valentin, F., Squizzato, S., Paern, J., and Lopez, R. (2010) A new bioinformatics analysis tools framework at EMBL-EBI Nucleic Acids Res. 38, W695-699
44. Biegert, A. and Soding, J. (2008) De novo identification of highly diverged protein repeats by probabilistic consistency Bioinformatics 24, 807-814
45. Buchan, D. W., Ward, S. M., Lobley, A. E., Nugent, T. C., Bryson, K., and Jones, D. T. (2010) Protein annotation and modelling servers at University College London Nucleic Acids Res. 38, W563-568
46. Zhang, Y. (2008) I-TASSER server for protein 3D structure prediction BMC Bioinf. 9 40
47. Roy, A., Kucukural, A., and Zhang, Y. (2010) I-TASSER: A unified platform for automated protein structure and function prediction Nat. Protoc. 5, 725-738
48. Arnold, K., Bordoli, L., Kopp, J., and Schwede, T. (2006) The SWISS-MODEL workspace: A web-based environment for protein structure homology modelling Bioinformatics 22, 195-201
49. Kiefer, F., Arnold, K., Kunzli, M., Bordoli, L., and Schwede, T. (2009) The SWISS-MODEL Repository and associated resources Nucleic Acids Res. 37, D387-392
50. Bordoli, L., Kiefer, F., Arnold, K., Benkert, P., Battey, J., and Schwede, T. (2009) Protein structure homology modeling using SWISS-MODEL workspace Nat. Protoc. 4, 1-13
51. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot Acta Crystallogr., Sect. D: Biol. Crystallogr. 66, 486-501
52. Brunger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J. S., Kuszewski, J., Nilges, M., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination Acta Crystallogr., Sect. D: Biol. Crystallogr. 54, 905-921
53. Brunger, A. T. (2007) Version 1.2 of the Crystallography and NMR system Nat. Protoc. 2, 2728-2733
54. Schrodinger, LLC. (2010) The PyMOL Molecular Graphics System, Version 1.3r1.
55. Gasteiger, E., Gattiker, A., Hoogland, C., Ivanyi, I., Appel, R. D., and Bairoch, A. (2003) ExPASy: The proteomics server for in-depth protein knowledge and analysis Nucleic Acids Res. 31, 3784-3788
56. Knapp, A. M., Ramsey, J. E., Wang, S. X., Strauch, A. R., and Kelm, R. J., Jr. (2007) Structure-function analysis of mouse Pur beta II. Conformation altering mutations disrupt single-stranded DNA and protein interactions crucial to smooth muscle alpha-actin gene repression J. Biol. Chem. 282, 35899-35909
57. Wang, S. X., Elder, P. K., Zheng, Y., Strauch, A. R., and Kelm, R. J., Jr. (2005) Cell cycle-mediated regulation of smooth muscle alpha-actin gene transcription in fibroblasts and vascular smooth muscle cells involves multiple adenovirus E1A-interacting cofactors J. Biol. Chem. 280, 6204-6214
58. Becker, N. A., Kelm, R. J., Jr., Vrana, J. A., Getz, M. J., and Maher, L. J., 3rd (2000) Altered sensitivity to single-strand-specific reagents associated with the genomic vascular smooth muscle alpha-actin promoter during myofibroblast differentiation J. Biol. Chem. 275, 15384-15391
59. White, M. K., Johnson, E. M., and Khalili, K. (2009) Multiple roles for Puralpha in cellular and viral regulation Cell Cycle 8, 1-7
60. Ronnov-Jessen, L. and Petersen, O. W. (1996) A function for filamentous alpha-smooth muscle actin: retardation of motility in fibroblasts J. Cell Biol. 134, 67-80
61. Hinz, B., Phan, S. H., Thannickal, V. J., Prunotto, M., Desmouliere, A., Varga, J., De Wever, O., Mareel, M., and Gabbiani, G. (2012) Recent developments in myofibroblast biology: paradigms for connective tissue remodeling Am. J. Pathol. 180, 1340-1355
62. Zhang, A., David, J. J., Subramanian, S. V., Liu, X., Fuerst, M. D., Zhao, X., Leier, C. V., Orosz, C. G., Kelm, R. J., Jr., and Strauch, A. R. (2008) Serum response factor neutralizes Pur alpha-and Pur beta-mediated repression of the fetal vascular smooth muscle alpha-actin gene in stressed adult cardiomyocytes Am. J. Physiol.: Cell Physiol. 294, C702-714
63. Johnson, E. M., Chen, P. L., Krachmarov, C. P., Barr, S. M., Kanovsky, M., Ma, Z. W., and Lee, W. H. (1995) Association of human Pur alpha with the retinoblastoma protein, Rb, regulates binding to the single-stranded DNA Pur alpha recognition element J. Biol. Chem. 270, 24352-24360
64. Barr, S. M. and Johnson, E. M. (2001) Ras-induced colony formation and anchorage-independent growth inhibited by elevated expression of Puralpha in NIH3T3 cells J. Cell. Biochem. 81, 621-638
65. Khalili, K., Del Valle, L., Muralidharan, V., Gault, W. J., Darbinian, N., Otte, J., Meier, E., Johnson, E. M., Daniel, D. C., Kinoshita, Y., Amini, S., and Gordon, J. (2003) Puralpha is essential for postnatal brain development and developmentally coupled cellular proliferation as revealed by genetic inactivation in the mouse Mol. Cell. Biol. 23, 6857-6875
66. Liu, H., Barr, S. M., Chu, C., Kohtz, D. S., Kinoshita, Y., and Johnson, E. M. (2005) Functional interaction of Puralpha with the Cdk2 moiety of cyclin A/Cdk2 Biochem. Biophys. Res. Commun. 328, 851-857
67. Darbinian, N., Gallia, G. L., Kundu, M., Shcherbik, N., Tretiakova, A., Giordano, A., and Khalili, K. (1999) Association of Pur alpha and E2F-1 suppresses transcriptional activity of E2F-1 Oncogene 18, 6398-6402
68. Darbinian, N., White, M. K., Gallia, G. L., Amini, S., Rappaport, J., and Khalili, K. (2004) Interaction between the pura and E2F-1 transcription factors Anticancer Res. 24, 2585-2594
69. Zhang, Q., Pedigo, N., Shenoy, S., Khalili, K., and Kaetzel, D. M. (2005) Puralpha activates PDGF-A gene transcription via interactions with a G-rich, single-stranded region of the promoter Gene 348, 25-32