The transcription factor mesp1 Interacts with cAMPresponsive element binding protein 1 (creb1) and coactivates Ets variant 2 (Etv2) gene expression

Journal of Biological Chemistry

Volumn 290, Issue 15, 2015, Pages 9614-9625

  Shi, Xiaozhong ^a   Zirbes, Katie M ^a   Rasmussen, Tara L ^a   Ferdous, Anwarul ^b   Garry, Mary G ^a   Koyano Nakagawa, Naoko ^a   Garry, Daniel J ^a  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CULTURE; CELL PROLIFERATION; CYTOLOGY; GENE EXPRESSION REGULATION; GENES; PROTEINS; TRANSCRIPTION;

CELL POPULATIONS; ELEMENT-BINDING PROTEINS; EMBRYONIC LETHALITY; LINEAGE SPECIFICATION; LINEAGE TRACING; PROTEIN-PROTEIN INTERACTIONS; TRANSACTIVATORS; TRANSCRIPTIONAL REGULATION;

GENE EXPRESSION;

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; ETS VARIANT 2 PROTEIN; MESODERM POSTERIOR 1 PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; CREB1 PROTEIN, MOUSE; ER71 PROTEIN, MOUSE; GREEN FLUORESCENT PROTEIN; MESP1 PROTEIN, MOUSE; PROTEIN BINDING;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL POPULATION; CONTROLLED STUDY; CREB1 GENE; EMBRYO; EMBRYO CELL; EMBRYO DEATH; EMBRYO DEVELOPMENT; ETV2 GENE; GENE DELETION; GENE EXPRESSION REGULATION; GENE TARGETING; HEMATOLOGIC DISEASE; IN VITRO STUDY; IN VIVO STUDY; MESP1 GENE; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; TRANSACTIVATION; TRANSCRIPTION REGULATION; VASCULAR DISEASE; YOLK SAC; 129 MOUSE; 3T3 CELL LINE; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL LINE; FLUORESCENCE MICROSCOPY; GENETICS; METABOLISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSCRIPTION INITIATION; TRANSGENIC MOUSE; WESTERN BLOTTING;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BLOTTING, WESTERN; CELL LINE; CELLS, CULTURED; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; EMBRYONIC DEVELOPMENT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GREEN FLUORESCENT PROTEINS; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROSCOPY, FLUORESCENCE; NIH 3T3 CELLS; PROTEIN BINDING; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSCRIPTION FACTORS; TRANSCRIPTIONAL ACTIVATION;

EID: 84927145269     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.614628     Document Type: Article

References (56)

1. Keller, G., Lacaud, G., and Robertson, S. (1999) Development of the hematopoietic system in the mouse. Exp. Hematol. 27, 777-787
2. Ferkowicz, M. J., and Yoder, M. C. (2005) Blood island formation: longstanding observations and modern interpretations. Exp. Hematol. 33, 1041-1047
3. Li, W., Ferkowicz, M. J., Johnson, S. A., Shelley, W. C., and Yoder, M. C. (2005) Endothelial cells in the early murine yolk sac give rise to CD41- expressing hematopoietic cells. Stem. Cells Dev. 14, 44-54
4. Wilson, N. K., Foster, S. D., Wang, X., Knezevic, K., Schütte, J., Kaimakis, P., Chilarska, P. M., Kinston, S., Ouwehand, W. H., Dzierzak, E., Pimanda, J. E., de Bruijn, M. F., and Göttgens, B. (2010) Combinatorial transcriptional control in blood stem/progenitor cells: genome-wide analysis of ten major transcriptional regulators. Cell Stem Cell 7, 532-544
5. Moignard, V., Woodhouse, S., Fisher, J., and Göttgens, B. (2013) Transcriptional hierarchies regulating early blood cell development. Blood Cells Mol. Dis. 51, 239-247
6. Saga, Y., Hata, N., Kobayashi, S., Magnuson, T., Seldin, M. F., and Taketo, M. M. (1996) MesP1: a novel basic helix-loop-helix protein expressed in the nascent mesodermal cells during mouse gastrulation. Development 122, 2769-2778
7. Lee, D., Park, C., Lee, H., Lugus, J. J., Kim, S. H., Arentson, E., Chung, Y. S., Gomez, G., Kyba, M., Lin, S., Janknecht, R., Lim, D. S., and Choi, K. (2008) ER71 acts downstream of BMP, Notch, and Wnt signaling in blood and vessel progenitor specification. Cell Stem Cell 2, 497-507
8. Ferdous, A., Caprioli, A., Iacovino, M., Martin, C. M., Morris, J., Richardson, J. A., Latif, S., Hammer, R. E., Harvey, R. P., Olson, E. N., Kyba, M., and Garry, D. J. (2009) Nkx2-5 transactivates the Ets-related protein 71 gene and specifies an endothelial/endocardial fate in the developing embryo. Proc. Natl. Acad. Sci. U.S.A. 106, 814-819
9. Chan, S. S., Shi, X., Toyama, A., Arpke, R. W., Dandapat, A., Iacovino, M., Kang, J., Le, G., Hagen, H. R., Garry, D. J., and Kyba, M. (2013) Mesp1patterns mesoderm into cardiac, hematopoietic, or skeletal myogenic progenitors in a context-dependent manner. Cell Stem Cell 12, 587-601
10. Bondue, A., Lapouge, G., Paulissen, C., Semeraro, C., Iacovino, M., Kyba, M., and Blanpain, C. (2008) Mesp1 acts as a master regulator of multipotent cardiovascular progenitor specification. Cell Stem Cell 3, 69-84
11. Lindsley, R. C., Gill, J. G., Murphy, T. L., Langer, E. M., Cai, M., Mashayekhi, M., Wang, W., Niwa, N., Nerbonne, J. M., Kyba, M., and Murphy, K. M. (2008) Mesp1 coordinately regulates cardiovascular fate re-striction and epithelial-mesenchymal transition in differentiating ESCs. Cell Stem Cell 3, 55-68
12. Bondue, A., and Blanpain, C. (2010) Mesp1: a key regulator of cardiovascular lineage commitment. Circ. Res. 107, 1414-1427
13. David, R., Brenner, C., Stieber, J., Schwarz, F., Brunner, S., Vollmer, M., Mentele, E., Müller-Höcker, J., Kitajima, S., Lickert, H., Rupp, R., and Franz, W. M. (2008) MesP1 drives vertebrate cardiovascular differentiation through Dkk-1-mediated blockade of Wnt-signalling. Nat. Cell Biol. 10, 338-345
14. Saga, Y., Miyagawa-Tomita, S., Takagi, A., Kitajima, S., Miyazaki, J., and Inoue, T. (1999) MesP1 is expressed in the heart precursor cells and required for the formation of a single heart tube. Development 126, 3437-3447
15. Kitajima, S., Takagi, A., Inoue, T., and Saga, Y. (2000) MesP1 and MesP2 are essential for the development of cardiac mesoderm. Development 127, 3215-3226
16. Kataoka, H., Hayashi, M., Nakagawa, R., Tanaka, Y., Izumi, N., Nishikawa, S., Jakt, M. L., and Tarui, H. (2011) Etv2/ER71 induces vascular mesoderm from Flk1-PDGFR- primitive mesoderm. Blood 118, 6975-6986
17. Palencia-Desai, S., Kohli, V., Kang, J., Chi, N. C., Black, B. L., and Sumanas, S. (2011) Vascular endothelial and endocardial progenitors differentiate as cardiomyocytes in the absence of Etsrp/Etv2 function. Development 138, 4721-4732
18. Lammerts van Bueren, K., and Black, B. L. (2012) Regulation of endothelial and hematopoietic development by the ETS transcription factor Etv2. Curr. Opin. Hematol. 19, 199-205
19. Wareing, S., Eliades, A., Lacaud, G., and Kouskoff, V. (2012) ETV2 expression marks blood and endothelium precursors, including hemogenic endothelium, at the onset of blood development. Dev. Dyn. 241, 1454-1464
20. Liu, F., Kang, I., Park, C., Chang, L. W., Wang, W., Lee, D., Lim, D. S., Vittet, D., Nerbonne, J. M., and Choi, K. (2012) ER71 specifies Flk-1- hemangiogenic mesoderm by inhibiting cardiac mesoderm and Wnt signaling. Blood 119, 3295-3305
21. Rasmussen, T. L., Kweon, J., Diekmann, M. A., Belema-Bedada, F., Song, Q., Bowlin, K., Shi, X., Ferdous, A., Li, T., Kyba, M., Metzger, J. M., Koyano-Nakagawa, N., and Garry, D. J. (2011) ER71 directs mesodermal fate decisions during embryogenesis. Development 138, 4801-4812
22. Schupp, M. O., Waas, M., Chun, C. Z., and Ramchandran, R. (2014) Transcriptional inhibition of etv2 expression is essential for embryonic cardiac development. Dev. Biol. 393, 71-83
23. Rasmussen, T. L., Shi, X., Wallis, A., Kweon, J., Zirbes, K. M., Koyano- Nakagawa, N., and Garry, D. J. (2012) VEGF/Flk1 signaling cascade transactivates Etv2 gene expression. PloS ONE 7, e50103
24. Koyano-Nakagawa, N., Kweon, J., Iacovino, M., Shi, X., Rasmussen, T. L., Borges, L., Zirbes, K. M., Li, T., Perlingeiro, R. C., Kyba, M., and Garry, D. J. (2012) Etv2 is expressed in the yolk sac hematopoietic and endothelial progenitors and regulates Lmo2 gene expression. Stem Cells 30, 1611-1623
25. Behrens, A. N., Zierold, C., Shi, X., Ren, Y., Koyano-Nakagawa, N., Garry, D. J., and Martin, C. M. (2014) Sox7 is regulated by ETV2 during cardiovascular development. Stem Cells Dev. 23, 2004-2013
26. Abedin, M. J., Nguyen, A., Jiang, N., Perry, C. E., Shelton, J. M., Watson, D. K., and Ferdous, A. (2014) Fli1 acts downstream of Etv2 to govern cell survival and vascular homeostasis via positive autoregulation. Circ. Res. 114, 1690-1699
27. Shaywitz, A. J., and Greenberg, M. E. (1999) CREB: a stimulus-induced transcription factor activated by a diverse array of extracellular signals. Annu. Rev. Biochem. 68, 821-861
28. Sands, W. A., and Palmer, T. M. (2008) Regulating gene transcription in response to cyclic AMP elevation. Cell. Signal. 20, 460-466
29. Fujii, Y., Shimizu, T., Toda, T., Yanagida, M., and Hakoshima, T. (2000)Structural basis for the diversity of DNA recognition by bZIP transcription factors. Nat. Struct. Biol. 7, 889-893
30. Rudolph, D., Tafuri, A., Gass, P., Hämmerling, G. J., Arnold, B., and Schütz, G. (1998) Impaired fetal T cell development and perinatal lethality in mice lacking the cAMP response element binding protein. Proc. Natl. Acad. Sci. U.S.A. 95, 4481-4486
31. Blendy, J. A., Kaestner, K. H., Weinbauer, G. F., Nieschlag, E., and Schütz, G. (1996) Severe impairment of spermatogenesis in mice lacking the CREM gene. Nature 380, 162-165
32. Nantel, F., Monaco, L., Foulkes, N. S., Masquilier, D., LeMeur, M., Henriksén, K., Dierich, A., Parvinen, M., and Sassone-Corsi, P. (1996) Spermiogenesis deficiency and germ-cell apoptosis in CREM-mutant mice. Nature 380, 159-162
33. Bleckmann, S. C., Blendy, J. A., Rudolph, D., Monaghan, A. P., Schmid, W., and Schütz, G. (2002) Activating transcription factor 1 and CREB are important for cell survival during early mouse development. Mol. Cell. Biol. 22, 1919-1925
34. Mantamadiotis, T., Lemberger, T., Bleckmann, S. C., Kern, H., Kretz, O., Martin Villalba, A., Tronche, F., Kellendonk, C., Gau, D., Kapfhammer, J., Otto, C., Schmid, W., and Schütz, G. (2002) Disruption of CREB function in brain leads to neurodegeneration. Nat. Genet. 31, 47-54
35. Benbrook, D. M., and Jones, N. C. (1994) Different binding specificities and transactivation of variant CRE's by CREB complexes. Nucleic Acids Res. 22, 1463-1469
36. Mayr, B., and Montminy, M. (2001) Transcriptional regulation by the phosphorylation-dependent factor CREB. Nat. Rev. Mol. Cell Biol. 2, 599-609
37. Matsuo, N., Tanaka, S., Gordon, M. K., Koch, M., Yoshioka, H., and Ramirez, F. (2006) CREB-AP1 protein complexes regulate transcription of the collagen XXIV gene (Col24a1) in osteoblasts. J. Biol. Chem. 281, 5445-5452
38. Zhao, L., Li, G., and Zhou, G. Q. (2009) SOX9 directly binds CREB as a novel synergism with the PKA pathway in BMP-2-induced osteochondrogenic differentiation. J. Bone Miner. Res. 24, 826-836
39. Magenta, A., Cenciarelli, C., De Santa, F., Fuschi, P., Martelli, F., Caruso, M., and Felsani, A. (2003) MyoD stimulates RB promoter activity via the CREB/p300 nuclear transduction pathway. Mol. Cell. Biol. 23, 2893-2906
40. Muir, T., Wilson-Rawls, J., Stevens, J. D., Rawls, A., Schweitzer, R., Kang, C., and Skinner, M. K. (2008) Integration of CREB and bHLH transcriptional signaling pathways through direct heterodimerization of the proteins: role in muscle and testis development. Mol. Reprod. Dev. 75, 1637-1652
41. Bowlin, K. M., Embree, L. J., Garry, M. G., Garry, D. J., and Shi, X. (2013) Kbtbd5 is regulated by MyoD and restricted to the myogenic lineage. Differentiation 86, 184-191
42. Ahn, S., Olive, M., Aggarwal, S., Krylov, D., Ginty, D. D., and Vinson, C. (1998) A dominant-negative inhibitor of CREB reveals that it is a general mediator of stimulus-dependent transcription of c-fos. Mol. Cell. Biol. 18, 967-977
43. Rasmussen, T. L., Martin, C. M., Walter, C. A., Shi, X., Perlingeiro, R., Koyano-Nakagawa, N., and Garry, D. J. (2013) Etv2 rescues Flk1 mutant embryoid bodies. Genesis 51, 471-480
44. Shi, X., Seldin, D. C., and Garry, D. J. (2012) Foxk1 recruits the Sds3 complex and represses gene expression in myogenic progenitors. Biochem. J. 446, 349-357
45. Shi, X., and Garry, D. J. (2010) Myogenic regulatory factors transactivate the Tceal7 gene and modulate muscle differentiation. Biochem. J. 428, 213-221
46. Iacovino, M., Bosnakovski, D., Fey, H., Rux, D., Bajwa, G., Mahen, E., Mitanoska, A., Xu, Z., and Kyba, M. (2011) Inducible cassette exchange: a rapid and efficient system enabling conditional gene expression in embryonic stem and primary cells. Stem Cells 29, 1580-1588
47. Iacovino, M., Roth, M. E., and Kyba, M. (2014) Rapid genetic modification of mouse embryonic stem cells by inducible cassette exchange recombination. Methods Mol. Biol. 1101, 339-351
48. Madisen, L., Zwingman, T. A., Sunkin, S. M., Oh, S. W., Zariwala, H. A., Gu, H., Ng, L. L., Palmiter, R. D., Hawrylycz, M. J., Jones, A. R., Lein, E. S., and Zeng, H. (2010) A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat. Neurosci. 13, 133-140
49. Soriano, P. (1999) Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 21, 70-71
50. Garry, D. J., Meeson, A., Elterman, J., Zhao, Y., Yang, P., Bassel-Duby, R., and Williams, R. S. (2000) Myogenic stem cell function is impaired in micelacking the forkhead/winged helix protein MNF. Proc. Natl. Acad. Sci. U.S.A. 97, 5416-5421
51. Farley, F. W., Soriano, P., Steffen, L. S., and Dymecki, S. M. (2000) Widespread recombinase expression using FLPeR (flipper) mice. Genesis 28, 106-110
52. Lakso, M., Pichel, J. G., Gorman, J. R., Sauer, B., Okamoto, Y., Lee, E., Alt, F. W., and Westphal, H. (1996) Efficient in vivo manipulation of mouse genomic sequences at the zygote stage. Proc. Natl. Acad. Sci. U.S.A. 93, 5860-5865
53. Shi, X., Richard, J., Zirbes, K. M., Gong, W., Lin, G., Kyba, M., Thomson, J. A., Koyano-Nakagawa, N., and Garry, D. J. (2014) Cooperative interaction of Etv2 and Gata2 regulates the development of endothelial and hematopoietic lineages. Dev. Biol. 389, 208-218
54. Veldman, M. B., and Lin, S. (2012) Etsrp/Etv2 is directly regulated by Foxc1a/b in the zebrafish angioblast. Circ. Res. 110, 220-229
55. Yamamizu, K., Matsunaga, T., Katayama, S., Kataoka, H., Takayama, N., Eto, K., Nishikawa, S., and Yamashita, J. K. (2012) PKA/CREB signaling triggers initiation of endothelial and hematopoietic cell differentiation via Etv2 induction. Stem Cells 30, 687-696
56. Zhang, X., Odom, D. T., Koo, S. H., Conkright, M. D., Canettieri, G., Best, J., Chen, H., Jenner, R., Herbolsheimer, E., Jacobsen, E., Kadam, S., Ecker, J. R., Emerson, B., Hogenesch, J. B., Unterman, T., Young, R. A., and Montminy, M. (2005) Genome-wide analysis of cAMP-response element binding protein occupancy, phosphorylation, and target gene activation in human tissues. Proc. Natl. Acad. Sci. U.S.A. 102, 4459-4464