Overlapping functions of Pea3 ETS transcription factors in FGF signaling during zebrafish development

Developmental Biology

Volumn 342, Issue 1, 2010, Pages 11-25

  Znosko, Wade A ^a,b   Yu, Shibin ^c   Thomas, Kirk ^c   Molina, Gabriela A ^a   Li, Chengjian ^a   Tsang, Warren ^a   Dawid, Igor B ^d   Moon, Anne M ^c   Tsang, Michael ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PITTSBURGH   (United States)

^c UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^d EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

Author keywords

Cilia; Dusp6; FGF; Heart; Kupffer's vesicle; Left right patterning; Pea3 ETS factors; Zebrafish

Indexed keywords

DUAL SPECIFICITY PHOSPHATASE 3; FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 8; TRANSCRIPTION FACTOR ERM; TRANSCRIPTION FACTOR ETS; TRANSCRIPTION FACTOR ETV5; TRANSCRIPTION FACTOR PEA3; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BINDING SITE; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; EMBRYO PATTERN FORMATION; GENE EXPRESSION REGULATION; HEART DEVELOPMENT; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; ZEBRA FISH;

DANIO RERIO;

EID: 77952585199     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2010.03.011     Document Type: Article

References (89)

1. Abu-Issa R., Smyth G., Smoak I., Yamamura K., Meyers E.N. Fgf8 is required for pharyngeal arch and cardiovascular development in the mouse. Development 2002, 129:4613-4625.
2. Albertson R.C., Yelick P.C. Roles for fgf8 signaling in left-right patterning of the visceral organs and craniofacial skeleton. Dev. Biol. 2005, 283:310-321.
3. Arber S., Ladle D.R., Lin J.H., Frank E., Jessell T.M. ETS gene Er81 controls the formation of functional connections between group Ia sensory afferents and motor neurons. Cell 2000, 101:485-498.
4. Bally-Cuif L., Goutel C., Wassef M., Wurst W., Rosa F. Coregulation of anterior and posterior mesendodermal development by a hairy-related transcriptional repressor. Genes Dev. 2000, 14:1664-1677.
5. Berdougo E., Coleman H., Lee D.H., Stainier D.Y., Yelon D. Mutation of weak atrium/atrial myosin heavy chain disrupts atrial function and influences ventricular morphogenesis in zebrafish. Development 2003, 130:6121-6129.
6. Bonnafe E., Touka M., AitLounis A., Baas D., Barras E., Ucla C., Moreau A., Flamant F., Dubruille R., Couble P., Collignon J., Durand B., Reith W. The transcription factor RFX3 directs nodal cilium development and left-right asymmetry specification. Mol. Cell. Biol. 2004, 24:4417-4427.
7. Brent A.E., Tabin C.J. FGF acts directly on the somitic tendon progenitors through the Ets transcription factors Pea3 and Erm to regulate scleraxis expression. Development 2004, 131:3885-3896.
8. Brody S.L., Yan X.H., Wuerffel M.K., Song S.K., Shapiro S.D. Ciliogenesis and left-right axis defects in forkhead factor HFH-4-null mice. Am. J. Respir. Cell Mol. Biol. 2000, 23:45-51.
9. Brown L.A., Amores A., Schilling T.F., Jowett T., Baert J.L., de Launoit Y., Sharrocks A.D. Molecular characterization of the zebrafish PEA3 ETS-domain transcription factor. Oncogene 1998, 17:93-104.
10. Chen J.N., Fishman M.C. Zebrafish tinman homolog demarcates the heart field and initiates myocardial differentiation. Development 1996, 122:3809-3816.
11. Chen C., Ouyang W., Grigura V., Zhou Q., Carnes K., Lim H., Zhao G.Q., Arber S., Kurpios N., Murphy T.L., Cheng A.M., Hassell J.A., Chandrashekar V., Hofmann M.C., Hess R.A., Murphy K.M. ERM is required for transcriptional control of the spermatogonial stem cell niche. Nature 2005, 436:1030-1034.
12. Cooper M.S., D'Amico L.A. A cluster of noninvoluting endocytic cells at the margin of the zebrafish blastoderm marks the site of embryonic shield formation. Dev. Biol. 1996, 180:184-198.
13. Dailey L., Ambrosetti D., Mansukhani A., Basilico C. Mechanisms underlying differential responses to FGF signaling. Cytokine Growth Factor Rev. 2005, 16:233-247.
14. Dickinson R.J., Eblaghie M.C., Keyse S.M., Morriss-Kay G.M. Expression of the ERK-specific MAP kinase phosphatase PYST1/MKP3 in mouse embryos during morphogenesis and early organogenesis. Mech. Dev. 2002, 113:193-196.
15. Draper B.W., Morcos P.A., Kimmel C.B. Inhibition of zebrafish fgf8 pre-mRNA splicing with morpholino oligos: a quantifiable method for gene knockdown. Genesis 2001, 30:154-156.
16. Draper B.W., Stock D.W., Kimmel C.B. Zebrafish fgf24 functions with fgf8 to promote posterior mesodermal development. Development 2003, 130:4639-4654.
17. Ekerot M., Stavridis M.P., Delavaine L., Mitchell M.P., Staples C., Owens D.M., Keenan I.D., Dickinson R.J., Storey K.G., Keyse S.M. Negative-feedback regulation of FGF signalling by DUSP6/MKP-3 is driven by ERK1/2 and mediated by Ets factor binding to a conserved site within the DUSP6/MKP-3 gene promoter. Biochem. J. 2008, 412:287-298.
18. Essner J.J., Amack J.D., Nyholm M.K., Harris E.B., Yost H.J. Kupffer's vesicle is a ciliated organ of asymmetry in the zebrafish embryo that initiates left-right development of the brain, heart and gut. Development 2005, 132:1247-1260.
19. Frank D.U., Fotheringham L.K., Brewer J.A., Muglia L.J., Tristani-Firouzi M., Capecchi M.R., Moon A.M. An Fgf8 mouse mutant phenocopies human 22q11 deletion syndrome. Development 2002, 129:4591-4603.
20. Furthauer M., Reifers F., Brand M., Thisse B., Thisse C. sprouty4 acts in vivo as a feedback-induced antagonist of FGF signaling in zebrafish. Development 2001, 128:2175-2186.
21. Furthauer M., Lin W., Ang S.L., Thisse B., Thisse C. Sef is a feedback-induced antagonist of Ras/MAPK-mediated FGF signalling. Nat. Cell Biol. 2002, 4:170-174.
22. Furthauer M., Van Celst J., Thisse C., Thisse B. Fgf signalling controls the dorsoventral patterning of the zebrafish embryo. Development 2004, 131:2853-2864.
23. Guo B., Sharrocks A.D. Extracellular signal-regulated kinase mitogen-activated protein kinase signaling initiates a dynamic interplay between sumoylation and ubiquitination to regulate the activity of the transcriptional activator PEA3. Mol. Cell. Biol. 2009, 29:3204-3218.
24. Hacohen N., Kramer S., Sutherland D., Hiromi Y., Krasnow M.A. sprouty encodes a novel antagonist of FGF signaling that patterns apical branching of the Drosophila airways. Cell 1998, 92:253-263.
25. Herzog W., Sonntag C., von der Hardt S., Roehl H.H., Varga Z.M., Hammerschmidt M. Fgf3 signaling from the ventral diencephalon is required for early specification and subsequent survival of the zebrafish adenohypophysis. Development 2004, 131:3681-3692.
26. Hong S.K., Dawid I.B. FGF-dependent left-right asymmetry patterning in zebrafish is mediated by Ier2 and Fibp1. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:2230-2235.
27. Hwang S.P., Tsou M.F., Lin Y.C., Liu C.H. The zebrafish BMP4 gene: sequence analysis and expression pattern during embryonic development. DNA Cell Biol. 1997, 16:1003-1011.
28. Ilagan R., Abu-Issa R., Brown D., Yang Y.P., Jiao K., Schwartz R.J., Klingensmith J., Meyers E.N. Fgf8 is required for anterior heart field development. Development 2006, 133:2435-2445.
29. Itoh N. The Fgf families in humans, mice, and zebrafish: their evolutional processes and roles in development, metabolism, and disease. Biol. Pharm. Bull. 2007, 30:1819-1825.
30. Kawakami Y., Rodriguez-Leon J., Koth C.M., Buscher D., Itoh T., Raya A., Ng J.K., Esteban C.R., Takahashi S., Henrique D., Schwarz M.F., Asahara H., Izpisua Belmonte J.C. MKP3 mediates the cellular response to FGF8 signalling in the vertebrate limb. Nat. Cell Biol. 2003, 5:513-519.
31. Keegan B.R., Meyer D., Yelon D. Organization of cardiac chamber progenitors in the zebrafish blastula. Development 2004, 131:3081-3091.
32. Kiefer P., Mathieu M., Mason I., Dickson C. Secretion and mitogenic activity of zebrafish FGF3 reveal intermediate properties relative to mouse and Xenopus homologues. Oncogene 1996, 12:1503-1511.
33. Kobberup S., Nyeng P., Juhl K., Hutton J., Jensen J. ETS-family genes in pancreatic development. Dev. Dyn. 2007, 236:3100-3110.
34. Kramer S., Okabe M., Hacohen N., Krasnow M.A., Hiromi Y. Sprouty: a common antagonist of FGF and EGF signaling pathways in Drosophila. Development 1999, 126:2515-2525.
35. Kramer-Zucker A.G., Olale F., Haycraft C.J., Yoder B.K., Schier A.F., Drummond I.A. Cilia-driven fluid flow in the zebrafish pronephros, brain and Kupffer's vesicle is required for normal organogenesis. Development 2005, 132:1907-1921.
36. Krauss S., Johansen T., Korzh V., Fjose A. Expression of the zebrafish paired box gene pax[zf-b] during early neurogenesis. Development 1991, 113:1193-1206.
37. Kudoh T., Tsang M., Hukriede N.A., Chen X., Dedekian M., Clarke C.J., Kiang A., Schultz S., Epstein J.A., Toyama R., Dawid I.B. A gene expression screen in zebrafish embryogenesis. Genome Res. 2001, 11:1979-1987.
38. Laget M.P., Defossez P.A., Albagli O., Baert J.L., Dewitte F., Stehelin D., de Launoit Y. Two functionally distinct domains responsible for transactivation by the Ets family member ERM. Oncogene 1996, 12:1325-1336.
39. Lee R.K., Stainier D.Y., Weinstein B.M., Fishman M.C. Cardiovascular development in the zebrafish. II. Endocardial progenitors are sequestered within the heart field. Development 1994, 120:3361-3366.
40. Liao E.C., Paw B.H., Oates A.C., Pratt S.J., Postlethwait J.H., Zon L.I. SCL/Tal-1 transcription factor acts downstream of cloche to specify hematopoietic and vascular progenitors in zebrafish. Genes Dev. 1998, 12:621-626.
41. Liu Y., Jiang H., Crawford H.C., Hogan B.L. Role for ETS domain transcription factors Pea3/Erm in mouse lung development. Dev. Biol. 2003, 261:10-24.
42. Livet J., Sigrist M., Stroebel S., De Paola V., Price S.R., Henderson C.E., Jessell T.M., Arber S. ETS gene Pea3 controls the central position and terminal arborization of specific motor neuron pools. Neuron 2002, 35:877-892.
43. Long S., Ahmad N., Rebagliati M. The zebrafish nodal-related gene southpaw is required for visceral and diencephalic left-right asymmetry. Development 2003, 130:2303-2316.
44. Lu B.C., Cebrian C., Chi X., Kuure S., Kuo R., Bates C.M., Arber S., Hassell J., MacNeil L., Hoshi M., Jain S., Asai N., Takahashi M., Schmidt-Ott K.M., Barasch J., D'Agati V., Costantini F. Etv4 and Etv5 are required downstream of GDNF and Ret for kidney branching morphogenesis. Nat. Genet. 2009, 41:1295-1302.
45. Macatee T.L., Hammond B.P., Arenkiel B.R., Francis L., Frank D.U., Moon A.M. Ablation of specific expression domains reveals discrete functions of ectoderm- and endoderm-derived FGF8 during cardiovascular and pharyngeal development. Development 2003, 130:6361-6374.
46. Mao J., McGlinn E., Huang P., Tabin C.J., McMahon A.P. Fgf-dependent Etv4/5 activity is required for posterior restriction of Sonic Hedgehog and promoting outgrowth of the vertebrate limb. Dev. Cell 2009, 16:600-606.
47. Maroulakou I.G., Papas T.S., Green J.E. Differential expression of ets-1 and ets-2 proto-oncogenes during murine embryogenesis. Oncogene 1994, 9:1551-1565.
48. Marques S.R., Lee Y., Poss K.D., Yelon D. Reiterative roles for FGF signaling in the establishment of size and proportion of the zebrafish heart. Dev. Biol. 2008, 321:397-406.
49. Melby A.E., Warga R.M., Kimmel C.B. Specification of cell fates at the dorsal margin of the zebrafish gastrula. Development 1996, 122:2225-2237.
50. Meyers E.N., Martin G.R. Differences in left-right axis pathways in mouse and chick: functions of FGF8 and SHH. Science 1999, 285:403-406.
51. Meyers E.N., Lewandoski M., Martin G.R. An Fgf8 mutant allelic series generated by Cre- and Flp-mediated recombination. Nat. Genet. 1998, 18:136-141.
52. Molina G.A., Watkins S.C., Tsang M. Generation of FGF reporter transgenic zebrafish and their utility in chemical screens. BMC Dev. Biol. 2007, 7:62.
53. Molina G., Vogt A., Bakan A., Dai W., Queiroz de Oliveira P., Znosko W., Smithgall T.E., Bahar I., Lazo J.S., Day B.W., Tsang M. Zebrafish chemical screening reveals an inhibitor of Dusp6 that expands cardiac cell lineages. Nat. Chem. Biol. 2009, 5:680-687.
54. Munchberg S.R., Ober E.A., Steinbeisser H. Expression of the Ets transcription factors erm and pea3 in early zebrafish development. Mech. Dev. 1999, 88:233-236.
55. Neugebauer J.M., Amack J.D., Peterson A.G., Bisgrove B.W., Yost H.J. FGF signalling during embryo development regulates cilia length in diverse epithelia. Nature 2009, 458:651-654.
56. Nutt S.L., Dingwell K.S., Holt C.E., Amaya E. Xenopus Sprouty2 inhibits FGF-mediated gastrulation movements but does not affect mesoderm induction and patterning. Genes Dev. 2001, 15:1152-1166.
57. O'Hagan R.C., Tozer R.G., Symons M., McCormick F., Hassell J.A. The activity of the Ets transcription factor PEA3 is regulated by two distinct MAPK cascades. Oncogene 1996, 13:1323-1333.
58. Oikawa T., Yamada T. Molecular biology of the Ets family of transcription factors. Gene 2003, 303:11-34.
59. Okabe N., Xu B., Burdine R.D. Fluid dynamics in zebrafish Kupffer's vesicle. Dev. Dyn. 2008, 237:3602-3612.
60. Ornitz D.M., Itoh N. Fibroblast growth factors. Genome Biol. 2001, 2(3). REVIEWS3005.
61. Park E.J., Ogden L.A., Talbot A., Evans S., Cai C.L., Black B.L., Frank D.U., Moon A.M. Required, tissue-specific roles for Fgf8 in outflow tract formation and remodeling. Development 2006, 133:2419-2433.
62. Park E.J., Watanabe Y., Smyth G., Miyagawa-Tomita S., Meyers E., Klingensmith J., Camenisch T., Buckingham M., Moon A.M. An FGF autocrine loop initiated in second heart field mesoderm regulates morphogenesis at the arterial pole of the heart. Development 2008, 135:3599-3610.
63. Pham V.N., Lawson N.D., Mugford J.W., Dye L., Castranova D., Lo B., Weinstein B.M. Combinatorial function of ETS transcription factors in the developing vasculature. Dev. Biol. 2007, 303:772-783.
64. Picker A., Brennan C., Reifers F., Clarke J.D., Holder N., Brand M. Requirement for the zebrafish mid-hindbrain boundary in midbrain polarisation, mapping and confinement of the retinotectal projection. Development 1999, 126:2967-2978.
65. Powers C.J., McLeskey S.W., Wellstein A. Fibroblast growth factors, their receptors and signaling. Endocr. Relat. Cancer 2000, 7:165-197.
66. Raible F., Brand M. Tight transcriptional control of the ETS domain factors Erm and Pea3 by Fgf signaling during early zebrafish development. Mech. Dev. 2001, 107:105-117.
67. Reifers F., Bohli H., Walsh E.C., Crossley P.H., Stainier D.Y., Brand M. Fgf8 is mutated in zebrafish acerebellar (ace) mutants and is required for maintenance of midbrain-hindbrain boundary development and somitogenesis. Development 1998, 125:2381-2395.
68. Reifers F., Walsh E.C., Leger S., Stainier D.Y., Brand M. Induction and differentiation of the zebrafish heart requires fibroblast growth factor 8 (fgf8/acerebellar). Development 2000, 127:225-235.
69. Reiter J.F., Alexander J., Rodaway A., Yelon D., Patient R., Holder N., Stainier D.Y. Gata5 is required for the development of the heart and endoderm in zebrafish. Genes Dev. 1999, 13:2983-2995.
70. Roehl H., Nusslein-Volhard C. Zebrafish pea3 and erm are general targets of FGF8 signaling. Curr. Biol. 2001, 11:503-507.
71. Roussigne M., Blader P. Divergence in regulation of the PEA3 family of ETS transcription factors. Gene Expr. Patterns 2006, 6:777-782.
72. Schoenebeck J.J., Keegan B.R., Yelon D. Vessel and blood specification override cardiac potential in anterior mesoderm. Dev. Cell 2007, 13:254-267.
73. Schulte-Merker S., Lee K.J., McMahon A.P., Hammerschmidt M. The zebrafish organizer requires chordino. Nature 1997, 387:862-863.
74. Sekine K., Ohuchi H., Fujiwara M., Yamasaki M., Yoshizawa T., Sato T., Yagishita N., Matsui D., Koga Y., Itoh N., Kato S. Fgf10 is essential for limb and lung formation. Nat. Genet. 1999, 21:138-141.
75. Serbedzija G.N., Chen J.N., Fishman M.C. Regulation in the heart field of zebrafish. Development 1998, 125:1095-1101.
76. Sharrocks A.D. The ETS-domain transcription factor family. Nat. Rev. Mol. Cell Biol. 2001, 2:827-837.
77. Stainier D.Y., Lee R.K., Fishman M.C. Cardiovascular development in the zebrafish. I. Myocardial fate map and heart tube formation. Development 1993, 119:31-40.
78. Sun X., Meyers E.N., Lewandoski M., Martin G.R. Targeted disruption of Fgf8 causes failure of cell migration in the gastrulating mouse embryo. Genes Dev. 1999, 13:1834-1846.
79. Tefft D., Lee M., Smith S., Crowe D.L., Bellusci S., Warburton D. mSprouty2 inhibits FGF10-activated MAP kinase by differentially binding to upstream target proteins. Am. J. Physiol. Lung Cell. Mol. Physiol. 2002, 283:L700-L706.
80. Thisse B., Thisse C. Functions and regulations of fibroblast growth factor signaling during embryonic development. Dev. Biol. 2005, 287:390-402.
81. Tsang M., Dawid I.B. Promotion and attenuation of FGF signaling through the Ras-MAPK pathway. Sci. STKE 2004, pe17.
82. Tsang M., Kim R., de Caestecker M.P., Kudoh T., Roberts A.B., Dawid I.B. Zebrafish nma is involved in TGFbeta family signaling. Genesis 2000, 28:47-57.
83. Tsang M., Friesel R., Kudoh T., Dawid I.B. Identification of Sef, a novel modulator of FGF signalling. Nat. Cell Biol. 2002, 4:165-169.
84. Tsang M., Maegawa S., Kiang A., Habas R., Weinberg E., Dawid I.B. A role for MKP3 in axial patterning of the zebrafish embryo. Development 2004, 131:2769-2779.
85. Wasylyk B., Hagman J., Gutierrez-Hartmann A. Ets transcription factors: nuclear effectors of the Ras-MAP-kinase signaling pathway. Trends Biochem. Sci. 1998, 23:213-216.
86. Yamauchi H., Miyakawa N., Miyake A., Itoh N. Fgf4 is required for left-right patterning of visceral organs in zebrafish. Dev. Biol. 2009, 332:177-185.
87. Yelon D., Horne S.A., Stainier D.Y. Restricted expression of cardiac myosin genes reveals regulated aspects of heart tube assembly in zebrafish. Dev. Biol. 1999, 214:23-37.
88. Yelon D., Ticho B., Halpern M.E., Ruvinsky I., Ho R.K., Silver L.M., Stainier D.Y. The bHLH transcription factor hand2 plays parallel roles in zebrafish heart and pectoral fin development. Development 2000, 127:2573-2582.
89. Zhang Z., Verheyden J.M., Hassell J.A., Sun X. FGF-regulated Etv genes are essential for repressing Shh expression in mouse limb buds. Dev. Cell 2009, 16:607-613.