Conservation and evolution in and among SRF- and MEF2-Type MADS domains and their binding sites

Molecular Biology and Evolution

Volumn 28, Issue 1, 2011, Pages 501-511

  Wu, Wenwu ^a   Huang, Xiaotai ^a   Cheng, Jian ^a   Li, Zhenggang ^a   De Folter, Stefan ^b   Huang, Zhuoran ^a   Jiang, Xiaoqian ^a   Pang, Hongxia ^a   Tao, Shiheng ^a  

^a NORTHWEST A F UNIVERSITY   (China)

^b INSTITUTO POLITÉCNICO NACIONAL   (Mexico)

Author keywords

CArG box; conservation; evolution; MADS; MEF2; SRF

Indexed keywords

MYOCYTE ENHANCER FACTOR 2; SERUM RESPONSE FACTOR;

AMINO ACID SEQUENCE; ARTICLE; BINDING SITE; DNA BINDING; DNA SEQUENCE; GENE MUTATION; GENETIC CONSERVATION; MOLECULAR EVOLUTION; MOLECULAR PHYLOGENY; NUCLEOTIDE SEQUENCE; PHYLOGENY; PROTEIN DOMAIN; PROTEIN STRUCTURE;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; BINDING SITES; DNA; EVOLUTION, MOLECULAR; HUMANS; MICE; MOLECULAR SEQUENCE DATA; MYOGENIC REGULATORY FACTORS; PHYLOGENY; PROTEIN STRUCTURE, TERTIARY; SERUM RESPONSE FACTOR;

ANIMALIA; FUNGI;

EID: 78650509132     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msq214     Document Type: Article

References (66)

1. Adamczyk BJ, Fernandez DE. 2009. MIKC* MADS domain hetero-dimers are required for pollen maturation and tube growth in Arabidopsis. Plant Physiol. 149:1713-1723.
2. Alvarez-Buylla ER, Pelaz S, Liljegren SJ, Gold SE, Burgeff C, Ditta GS, Ribas DPL, Martinez-Castilla L, Yanofsky MF. 2000. An ancestral MADS-box gene duplication occurred before the divergence of plants and animals. Proc Natl Acad Sci USA. 97:5328-5333.
3. Andres V, Cervera M, Mahdavi V. 1995. Determination of the consensus binding site for MEF2 expressed in muscle and brain reveals tissue-specific sequence constraints. J Biol Chem. 270:23246-23249.
4. Balza RO Jr., Misra RP. 2006. Role of the serum response factor in regulating contractile apparatus gene expression and sarcomeric integrity in cardiomyocytes. J Biol Chem. 281:6498-651.
5. Chen CH, Wu ML, Lee YC, Layne MD, Yet SF. 2010. Intronic CArG box regulates cysteine-rich protein 2 expression in the adult but not in developing vasculature. Arterioscler Thromb Vasc Biol. 4:835-842.
6. Cooper SJ, Trinklein ND, Nguyen L, Myers RM. 2007. Serum response factor binding sites differ in three human cell types. Genome Res. 17:136-144.
7. Crooks GE, Hon G, Chandonia JM, Brenner SE. 2004. WebLogo: a sequence logo generator. Genome Res. 14:1188-1190.
8. de Folter S, Angenent GC. 2006. trans meets cis in MADS science. Trends Plant Sci. 11:224-231.
9. Flavell SW, Kim TK, Gray JM, Harmin DA, Hemberg M, Hong EJ, Markenscoff-Papadimitriou E, Bear DM, Greenberg ME. 2008. Genome-wide analysis of MEF2 transcriptional program reveals synaptic target genes and neuronal activity-dependent poly-adenylation site selection. Neuron 60:1022-1038.
10. Fornara F, Marziani G, Mizzi L, Kater M, Colombo L. 2003. MADS-box genes controlling flower development in rice. Plant Biol. 5:16-22.
11. Freddie CT, Ji Z, Marais A, Sharrocks AD. 2007. Functional interactions between the Forkhead transcription factor FOXK1 and the MADS-box protein SRF. Nucleic Acids Res. 15:5203-5212.
12. Gramzow L, Ritz MS, Theissen G. 2010. On the origin of MADS-domain transcription factors. Trends Genet. 26:149-153.
13. Haeseleer PD. 2006. What are DNA sequence motifs? Nat Biotechnol. 24:423-425.
14. Hendrix JA, Wamhoff BR, McDonald OG, Sinha S, Yoshida T, Owens GK. 2005. 5' CArG degeneracy in smooth muscle alpha-actin is required for injury-induced gene suppression in vivo. J Clin Invest. 115:418-427.
15. Herskowitz I. 1989. A regulatory hierarchy for cell specialization in yeast. Nature 342:749-757.
16. Huang K, Louis JM, Donaldson L, Lim FL, Sharrocks AD, Clore GM. 2000. Solution structure of the MEF2A-DNA complex: structural basis for the modulation of DNA bending and specificity by MADS-box transcription factors. EMBO J. 19:2615.
17. Immink RG, Gadella TJ, Ferrario S, Busscher M, Angenent GC. 2002. Analysis of MADS box protein-protein interactions in living plant cells. Proc Natl Acad Sci USA. 99:2416-2421.
18. Kaufmann K, Melzer R, Theissen G. 2005. MIKC-type MADS-domain proteins: structural modularity, protein interactions and network evolution in land plants. Gene 347:183-198.
19. Kofuji R, Sumikawa N, Yamasaki M, Kondo K, Ueda K, Ito M, Hasebe M. 2003. Evolution and divergence of the MADS-box gene family based on genome-wide expression analyses. Mol Biol Evol. 20:1963-1977.
20. Larkin MA, Blackshields G, Brown NP, et al. (13 coauthors). 2007. ClustalW and ClustalX version 2.0. Bioinformatics 23:2947-2948.
21. Li H, Coghlan A, Ruan J, et al. (15 coauthors). 2006. TreeFam: a curated database of phylogenetic trees of animal gene families. Nucleic Acids Res. 34:D572-D580.
22. Mack CP, Owens GK. 1999. Regulation of smooth muscle alpha-actin expression in vivo is dependent on CArG elements within the 5# and first intron promoter regions. Circ Res. 84:852-861.
23. Madsen O, Scally M, Douady CJ, et al. (10 coauthors). 2001. Parallel adaptive radiations in two major clades of placental mammals. Nature 409:610-614. (Pubitemid 32154811)
24. Messenguy F, Dubois E. 2003. Role of MADS box proteins and their cofactors in combinatorial control of gene expression and cell development. Gene 316:1-21.
25. Miano JM. 2003. Serum response factor: toggling between disparate programs of gene expression. J Mol Cell Cardiol. 35:577-593.
26. Molkentin JD, Black BL, Martin JF, Olson EN. 1996. Mutational analysis of the DNA binding, dimerization, and transcriptional activation domains of MEF2C. Mol Cell Biol. 16:2627-2636.
27. Muller J, Muller K. 2004. TreeGraph: automated drawing of complex tree figures using an extensible tree description format. Mol Ecol Notes. 4:786-788.
28. Munster T, Pahnke J, Di Rosa A, Kim JT, Martin W, Saedler H, Theissen G. 1997. Floral homeotic genes were recruited from homologous MADS-box genes preexisting in the common ancestor of ferns and seed plants. Proc Natl Acad Sci USA. 94:2415-2420.
29. Murphy WJ, Eizirik E, Johnson WE, Zhang YP, Ryder OA, O'Brien SJ. 2001. Molecular phylogenetics and the origins of placental mammals. Nature 409:614-618.
30. Ng M, Yanofsky MF. 2001. Function and evolution of the plant MADS-box gene family. Nat Rev Genet. 2:186-195.
31. Norman C, Runswick M, Pollock R, Treisman R. 1988. Isolation and properties of cDNA clones encoding SRF, a transcription factor that binds to the c-fos serum response element. Cell 55:989-1003.
32. Nurrish SJ, Treisman R. 1995. DNA binding specificity determinants in MADS-box transcription factors. Mol Cell Biol. 15:4076-4085.
33. Page RD. 1996. TreeView: an application to display phylogenetic trees on personal computers. Comput Appl Biosci. 12:357-358.
34. Parenicova L, de Folter S, Kieffer M, et al. (12 coauthors). 2003. Molecular and phylogenetic analyses of the complete MADS-box transcription factor family in Arabidopsis: new openings to the MADS world. Plant Cell. 15:1538-1551.
35. Passmore S, Elble R, Tye BK. 1989. A protein involved in minichromosome maintenance in yeast binds a transcriptional enhancer conserved in eukaryotes. Genes Dev. 3:921-935.
36. Pellegrini L, Tan S, Richmond TJ. 1995. Structure of serum response factor core bound to DNA. Nature 376:490-498.
37. Petit MM, Lindskog H, Larsson E, et al. (12 coauthors). 2008. Smooth muscle expression of lipoma preferred partner is mediated by an alternative intronic promoter that is regulated by serum response factor/myocardin. Circ Res. 103:61-69.
38. Philippar U, Schratt G, Dieterich C, et al. (11 coauthors). 2004. The SRF target gene Fhl2 antagonizes RhoA/MAL-dependent activation of SRF. Mol Cell. 16:867-880.
39. Pollock R, Treisman R. 1990. A sensitive method for the determination of protein-DNA binding specificities. Nucleic Acids Res. 18:6197-6204.
40. Pollock R, Treisman R. 1991. Human SRF-related proteins: DNA-binding properties and potential regulatory targets. Genes Dev. 5:2327-2341.
41. Potthoff MJ, Olson EN. 2007. MEF2: a central regulator of diverse developmental programs. Development 134:4131-4140.
42. Reyes A, Gissi C, Catzeflis F, Nevo E, Pesole G, Saccone C. 2004. Congruent mammalian trees from mitochondrial and nuclear genes using Bayesian methods. Mol Biol Evol. 21:397-403.
43. Santelli E, Richmond TJ. 2000. Crystal structure of MEF2A core bound to DNA at 1.5 A resolution. J Mol Biol. 297:437-449.
44. Schwarz-Sommer Z, Huijser P, Nacken W, Saedler H, Sommer H. 1990. Genetic control of flower development by homeotic genes in Antirrhinum majus. Science 250:931-936.
45. Selvaraj A, Prywes R. 2004. Expression profiling of serum inducible genes identifies a subset of SRF target genes that are MKL dependent. BMC Mol Biol. 5:13.
46. Shore P, Sharrocks AD. 1995. The MADS-box family of transcription factors. Eur J Biochem 229:1-13.
47. Sommer H, Beltran JP, Huijser P, Pape H, Lonnig WE, Saedler H, Schwarz-Sommer Z. 1990. Deficiens, a homeotic gene involved in the control of flower morphogenesis in Antirrhinum majus: the protein shows homology to transcription factors. EMBO J. 9:605-613.
48. Stepanek J, Vincent M, Turpin PY, Paulin D, Fermandjian S, Alpert B, Zentz C. 2007. C / G base mutations in the CArG box of c-fos serum response element alter its bending flexibility. Consequences for core-SRF recognition. FEBS J. 274:2333-2348.
49. Stormo GD. 2000. DNA binding sites: representation and discovery. Bioinformatics 16:16-23.
50. Strobeck M, Kim S, Zhang J, Clendenin C, Du KL, Parmacek MS. 2001. Binding of serum response factor to CArG box sequences is necessary but not sufficient to restrict gene expression to arterial smooth muscle cells. J Biol Chem. 276:16418.
51. Sun Q, Chen G, Streb JW, Long X, Yang Y, Stoeckert CJ, Miano JM. 2006. Defining the mammalian CArGome. Genome Res. 16:197-207.
52. Tan S, Richmond TJ. 1998. Crystal structure of the yeast MATalpha2/MCM1/DNA ternary complex. Nature 391: 660-666.
53. Thakare D, Tang W, Hill K, Perry SE. 2008. The MADS-domain transcriptional regulator AGAMOUS-LIKE15 promotes somatic embryo development in Arabidopsis and soybean. Plant Physiol. 146:1663-1672.
54. Theissen G, Kim JT, Saedler H. 1996. Classification and phylogeny of the MADS-box multigene family suggest defined roles of MADS-box gene subfamilies in the morphological evolution of eukaryotes. J Mol Evol. 43:484-516.
55. Tilly JJ, Allen DW, Jack T. 1998. The CArG boxes in the promoter of the Arabidopsis floral organ identity gene APETALA3 mediate diverse regulatory effects. Development 125:1647.
56. Treisman R, Ammerer G. 1992. The SRF and MCM1 transcription factors. Curr Opin Genet Dev. 2:221-226.
57. Wakaguri H, Yamashita R, Suzuki Y, Sugano S, Nakai K. 2008. DBTSS: database of transcription start sites, progress report 2008. Nucleic Acids Res. 36:D97-D101.
58. West AG, Sharrocks AD. 1999. MADS-box transcription factors adopt alternative mechanisms for bending DNA. J Mol Biol. 286:1311-1323.
59. West AG, Shore P, Sharrocks AD. 1997. DNA binding by MADS-box transcription factors: a molecular mechanism for differential DNA bending. Mol Cell Biol. 17:2876-2887.
60. Wheeler DL, Barrett T, Benson DA, et al. (30 coauthors). 2007. Database resources of the National Center for Biotechnology Information. Nucleic Acids Res. 35:D5-D12.
61. Workman CT, Yin Y, Corcoran DL, Ideker T, Stormo GD, Benos PV. 2005. enoLOGOS: a versatile web tool for energy normalized sequence logos. Nucleic Acids Res. 33:W389-W392.
62. Wu WW, Shen X, Tao SH. 2010. Characteristics of the CArG-SRF binding context in mammalian genomes. Mamm Genome. 21:104-113.
63. Yanofsky MF, Ma H, Bowman JL, Drews GN, Feldmann KA, Meyerowitz EM. 1990. The protein encoded by the Arabidopsis homeotic gene agamous resembles transcription factors. Nature 346:35-39.
64. Zhang J, Nei M. 1997. Accuracies of ancestral amino acid sequences inferred by the parsimony, likelihood, and distance methods. J Mol Evol. 44:S139-S146.
65. Zhang SX, Garcia-Gras E, Wycuff DR, et al. (10 coauthors). 2005. Identification of direct serum-response factor gene targets during Me2SO-induced P19 cardiac cell differentiation. J Biol Chem. 280:19115-19126.
66. Zheng Y, Ren N, Wang H, Stromberg AJ, Perry SE. 2009. Global identification of targets of the Arabidopsis MADS domain protein AGAMOUS-Like15. Plant Cell. 21:2563-2577.