Pdgfrα and Flk1 are direct target genes of Mixl1 in differentiating embryonic stem cells

Stem Cell Research

Volumn 8, Issue 2, 2012, Pages 165-179

  Pereira, Lloyd A ^a   Wong, Michael S ^b   Mossman, Anna K ^b   Sourris, Koula ^b   Janes, Mary E ^c   Knezevic, Kathy ^c   Hirst, Claire E ^a   Lim, Sue Mei ^a   Pimanda, John E ^c   Stanley, Edouard G ^b   Elefanty, Andrew G ^b  

^a PETER MACCALLUM CANCER CENTRE   (Australia)

^b MONASH UNIVERSITY   (Australia)

^c UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

HOMEODOMAIN PROTEIN; MIXL1 HOMEODOMAIN PROTEIN; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; UNCLASSIFIED DRUG; VASCULOTROPIN RECEPTOR 2;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL SELECTION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA BINDING; EMBRYOID BODY; EMBRYONIC STEM CELL; ENDODERM; FLOW CYTOMETRY; GASTRULATION; GENE EXPRESSION; GENE TARGETING; GENETIC TRANSCRIPTION; IN VIVO STUDY; KARYOTYPE; MOUSE; NONHUMAN; PRIORITY JOURNAL;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; BINDING SITES; CELL DIFFERENTIATION; CELL LINE; EMBRYONIC STEM CELLS; ENDODERM; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; MESODERM; MICE; MOLECULAR SEQUENCE DATA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; RECEPTOR, PLATELET-DERIVED GROWTH FACTOR ALPHA; RNA, MESSENGER; TRANSCRIPTIONAL ACTIVATION; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

MAMMALIA;

EID: 81255166263     PISSN: 18735061     EISSN: 18767753     Source Type: Journal    
DOI: 10.1016/j.scr.2011.09.007     Document Type: Article

References (56)

1. Alexander J., Rothenberg M., Henry G.L., Stainier D.Y. Casanova plays an early and essential role in endoderm formation in zebrafish. Dev. Biol. 1999, 215(2):343-357.
2. Aparicio O., Geisberg J.V., Sekinger E., Yang A., Moqtaderi Z., Struhl K. Chromatin immunoprecipitation for determining the association of proteins with specific genomic sequences in vivo. Curr. Protoc. Mol. Biol. 2005, 21.3.1-21.3.33.
3. Artinger M., Blitz I., Inoue K., Tran U., Cho K.W. Interaction of goosecoid and brachyury in Xenopus mesoderm patterning. Mech. Dev. 1997, 65(1-2):187-196.
4. Ataliotis P., Symes K., Chou M.M., Ho L., Mercola M. PDGF signalling is required for gastrulation of Xenopus laevis. Development 1995, 121(9):3099-3110.
5. Barnett L.D., Kontgen F. Gene targeting in a centralized facility. Methods Mol. Biol. 2001, 158:65-82.
6. Casey E.S., Tada M., Fairclough L., Wylie C.C., Heasman J., Smith J.C. Bix4 is activated directly by VegT and mediates endoderm formation in Xenopus development. Development 1999, 126(19):4193-4200.
7. Dale T.C., Imam A.M., Kerr I.M., Stark G.R. Rapid activation by interferon alpha of a latent DNA-binding protein present in the cytoplasm of untreated cells. Proc. Natl. Acad. Sci. U. S. A. 1989, 86(4):1203-1207.
8. Danilov V., Blum M., Schweickert A., Campione M., Steinbeisser H. Negative autoregulation of the organiser-specific homeobox gene goosecoid. J. Biol. Chem. 1998, 273(1):627-635.
9. Davis R.P., Ng E.S., Costa M., Mossman A.K., Sourris K., Elefanty A.G. Targeting a GFP reporter gene to the MIXL1 locus of human embryonic stem cells identifies human primitive streak-like cells and enables isolation of primitive hematopoietic precursors. Blood 2008, 111(4):1876-1884.
10. Hart A.H., Hartley L., Sourris K., Stadler E.S., Li R., Stanley E.G. Mixl1 is required for axial mesendoderm morphogenesis and patterning in the murine embryo. Development 2002, 129(15):3597-3608.
11. Hirst C.E., Ng E.S., Azzola L., Voss A.K., Thomas T., Stanley E.G. Transcriptional profiling of mouse and human ES cells identifies SLAIN1, a novel stem cell gene. Dev. Biol. 2006, 293(1):90-103.
12. Hukriede N.A., Tsang T.E., Habas R., Khoo P.L., Steiner K., Weeks D.L. Conserved requirement of Lim1 function for cell movements during gastrulation. Dev. Cell 2003, 4(1):83-94.
13. Izumi N., Era T., Akimaru H., Yasunaga M., Nishikawa S. Dissecting the molecular hierarchy for mesendoderm differentiation through a combination of embryonic stem cell culture and RNA interference. Stem Cells 2007, 25(7):1664-1674.
14. Joosten P.H., Toepoel M., van Oosterhout D., Afink G.B., van Zoelen E.J. A regulating element essential for PDGFRA transcription is recognized by neural tube defect-associated PRX homeobox transcription factors. Biochim. Biophys. Acta 2002, 1588(3):254-260.
15. Kataoka H., Takakura N., Nishikawa S., Tsuchida K., Kodama H., Kunisada T. Expressions of PDGF receptor alpha, c-Kit and Flk1 genes clustering in mouse chromosome 5 define distinct subsets of nascent mesodermal cells. Dev. Growth Differ. 1997, 39(6):729-740.
16. Kikuchi Y., Trinh L.A., Reiter J.F., Alexander J., Yelon D., Stainier D.Y. The zebrafish bonnie and clyde gene encodes a Mix family homeodomain protein that regulates the generation of endodermal precursors. Genes Dev. 2000, 14(10):1279-1289.
17. Kimura Y., Matsunami H., Inoue T., Shimamura K., Uchida N., Ueno T. Cadherin-11 expressed in association with mesenchymal morphogenesis in the head, somite, and limb bud of early mouse embryos. Dev. Biol. 1995, 169(1):347-358.
18. Kimura Y., Matsunami H., Takeichi M. Expression of cadherin-11 delineates boundaries, neuromeres, and nuclei in the developing mouse brain. Dev. Dyn. 1996, 206(4):455-462.
19. Kofron M., Wylie C., Heasman J. The role of Mixer in patterning the early Xenopus embryo. Development 2004, 131(10):2431-2441.
20. Labbe E., Silvestri C., Hoodless P.A., Wrana J.L., Attisano L. Smad2 and Smad3 positively and negatively regulate TGF beta-dependent transcription through the forkhead DNA-binding protein FAST2. Mol. Cell 1998, 2(1):109-120.
21. Latinkic B.V., Smith J.C. Goosecoid and mix.1 repress Brachyury expression and are required for head formation in Xenopus. Development 1999, 126(8):1769-1779.
22. Lemaire P., Darras S., Caillol D., Kodjabachian L. A role for the vegetally expressed Xenopus gene Mix.1 in endoderm formation and in the restriction of mesoderm to the marginal zone. Development 1998, 125(13):2371-2380.
23. Lim S.M., Pereira L., Wong M.S., Hirst C.E., Van Vranken B.E., Pick M. Enforced expression of Mixl1 during mouse ES cell differentiation suppresses hematopoietic mesoderm and promotes endoderm formation. Stem Cells 2009, 27(2):363-374.
24. McGrath K.E., Koniski A.D., Maltby K.M., McGann J.K., Palis J. Embryonic expression and function of the chemokine SDF-1 and its receptor, CXCR4. Dev. Biol. 1999, 213(2):442-456.
25. Mead P.E., Brivanlou I.H., Kelley C.M., Zon L.I. BMP-4-responsive regulation of dorsal-ventral patterning by the homeobox protein Mix.1. Nature 1996, 382(6589):357-360.
26. Mohn D., Chen S.W., Dias D.C., Weinstein D.C., Dyer M.A., Sahr K. Mouse Mix gene is activated early during differentiation of ES and F9 stem cells and induces endoderm in frog embryos. Dev. Dyn. 2003, 226(3):446-459.
27. Morrison G.M., Oikonomopoulou I., Migueles R.P., Soneji S., Livigni A., Enver T. Anterior definitive endoderm from ESCs reveals a role for FGF signaling. Cell Stem Cell 2008, 3(4):402-415.
28. Mossman A.K., Sourris K., Ng E., Stanley E.G., Elefanty A.G. Mixl1 and oct4 proteins are transiently co-expressed in differentiating mouse and human embryonic stem cells. Stem Cells Dev. 2005, 14(6):656-663.
29. Nagasawa T., Hirota S., Tachibana K., Takakura N., Nishikawa S., Kitamura Y. Defects of B-cell lymphopoiesis and bone-marrow myelopoiesis in mice lacking the CXC chemokine PBSF/SDF-1. Nature 1996, 382(6592):635-638.
30. Nair S., Schilling T.F. Chemokine signaling controls endodermal migration during zebrafish gastrulation. Science 2008, 322(5898):89-92.
31. Ng E.S., Azzola L., Sourris K., Robb L., Stanley E.G., Elefanty A.G. The primitive streak gene Mixl1 is required for efficient haematopoiesis and BMP4-induced ventral mesoderm patterning in differentiating ES cells. Development 2005, 132(5):873-884.
32. Pearce J.J., Evans M.J. Mml, a mouse Mix-like gene expressed in the primitive streak. Mech. Dev. 1999, 87(1-2):189-192.
33. Pick M., Azzola L., Mossman A., Stanley E.G., Elefanty A.G. Differentiation of human embryonic stem cells in serum-free medium reveals distinct roles for bone morphogenetic protein 4, vascular endothelial growth factor, stem cell factor, and fibroblast growth factor 2 in hematopoiesis. Stem Cells 2007, 25(9):2206-2214.
34. Pimanda J.E., Chan W.Y., Donaldson I.J., Bowen M., Green A.R., Gottgens B. Endoglin expression in the endothelium is regulated by Fli-1, Erg, and Elf-1 acting on the promoter and a -8-kb enhancer. Blood 2006, 107(12):4737-4745.
35. Robb L., Hartley L., Begley C.G., Brodnicki T.C., Copeland N.G., Gilbert D.J. Cloning, expression analysis, and chromosomal localization of murine and human homologues of a Xenopus mix gene. Dev. Dyn. 2000, 219(4):497-504.
36. Rosa F.M. Mix.1, a homeobox mRNA inducible by mesoderm inducers, is expressed mostly in the presumptive endodermal cells of Xenopus embryos. Cell 1989, 57(6):965-974.
37. Saga Y., Miyagawa-Tomita S., Takagi A., Kitajima S., Miyazaki J., Inoue T. MesP1 is expressed in the heart precursor cells and required for the formation of a single heart tube. Development 1999, 126(15):3437-3447.
38. Sahr K., Dias D.C., Sanchez R., Chen D., Chen S.W., Gudas L.J. Structure, upstream promoter region, and functional domains of a mouse and human Mix paired-like homeobox gene. Gene 2002, 291(1-2):135-147.
39. Shalaby F., Ho J., Stanford W.L., Fischer K.D., Schuh A.C., Schwartz L. A requirement for Flk1 in primitive and definitive hematopoiesis and vasculogenesis. Cell 1997, 89(6):981-990.
40. Shay-Salit A., Shushy M., Wolfovitz E., Yahav H., Breviario F., Dejana E. VEGF receptor 2 and the adherens junction as a mechanical transducer in vascular endothelial cells. Proc. Natl. Acad. Sci. U. S. A. 2002, 99(14):9462-9467.
41. Shibuya M. Vascular endothelial growth factor receptor-2: its unique signaling and specific ligand, VEGF-E. Cancer Sci. 2003, 94(9):751-756.
42. Shiraki N., Lai C.J., Hishikari Y., Kume S. TGF-beta signaling potentiates differentiation of embryonic stem cells to Pdx-1 expressing endodermal cells. Genes Cells 2005, 10(6):503-516.
43. Soriano P. The PDGF alpha receptor is required for neural crest cell development and for normal patterning of the somites. Development 1997, 124(14):2691-2700.
44. Symes K., Mercola M. Embryonic mesoderm cells spread in response to platelet-derived growth factor and signaling by phosphatidylinositol 3-kinase. Proc. Natl. Acad. Sci. U. S. A. 1996, 93(18):9641-9644.
45. Tada M., Casey E.S., Fairclough L., Smith J.C. Bix1, a direct target of Xenopus T-box genes, causes formation of ventral mesoderm and endoderm. Development 1998, 125(20):3997-4006.
46. Takakura N., Yoshida H., Ogura Y., Kataoka H., Nishikawa S. PDGFR alpha expression during mouse embryogenesis: immunolocalization analyzed by whole-mount immunohistostaining using the monoclonal anti-mouse PDGFR alpha antibody APA5. J. Histochem. Cytochem. 1997, 45(6):883-893.
47. Tam P.P., Khoo P.L., Lewis S.L., Bildsoe H., Wong N., Tsang T.E. Sequential allocation and global pattern of movement of the definitive endoderm in the mouse embryo during gastrulation. Development 2007, 134(2):251-260.
48. Tam P.P., Khoo P.L., Wong N., Tsang T.E., Behringer R.R. Regionalization of cell fates and cell movement in the endoderm of the mouse gastrula and the impact of loss of Lhx1(Lim1) function. Dev. Biol. 2004, 274(1):171-187.
49. Tucker S.C., Wisdom R. Site-specific heterodimerization by paired class homeodomain proteins mediates selective transcriptional responses. J. Biol. Chem. 1999, 274(45):32325-32332.
50. Watabe T., Kim S., Candia A., Rothbacher U., Hashimoto C., Inoue K. Molecular mechanisms of Spemann's organizer formation: conserved growth factor synergy between Xenopus and mouse. Genes Dev. 1995, 9(24):3038-3050.
51. Wilkinson D.G., Bhatt S., Herrmann B.G. Expression pattern of the mouse T gene and its role in mesoderm formation. Nature 1990, 343(6259):657-659.
52. Willey S., Ayuso-Sacido A., Zhang H., Fraser S.T., Sahr K.E., Adlam M.J. Acceleration of mesoderm development and expansion of hematopoietic progenitors in differentiating ES cells by the mouse Mix-like homeodomain transcription factor. Blood 2006, 107(8):3122-3130.
53. Wilson D., Sheng G., Lecuit T., Dostatni N., Desplan C. Cooperative dimerization of paired class homeo domains on DNA. Genes Dev. 1993, 7(11):2120-2134.
54. Yusuf F., Rehimi R., Dai F., Brand-Saberi B. Expression of chemokine receptor CXCR4 during chick embryo development. Anat Embryol (Berl) 2005, 210(1):35-41.
55. Zeng H., Sanyal S., Mukhopadhyay D. Tyrosine residues 951 and 1059 of vascular endothelial growth factor receptor-2 (KDR) are essential for vascular permeability factor/vascular endothelial growth factor-induced endothelium migration and proliferation, respectively. J. Biol. Chem. 2001, 276(35):32714-32719.
56. Zhang H., Fraser S.T., Papazoglu C., Hoatlin M.E., Baron M.H. Transcriptional activation by the Mixl1 homeodomain protein in differentiating mouse embryonic stem cells. Stem Cells 2009, 27(12):2884-2895.