Fgf is required to regulate anterior-posterior patterning in the Xenopus lateral plate mesoderm

Mechanisms of Development

Volumn 128, Issue 7-10, 2011, Pages 327-341

  Deimling, Steven J ^a,b   Drysdale, Thomas A ^a,b  

^a CHILDREN S HEALTH RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

Fibroblast growth factor; Foxf1; Hand1; Heart; Lateral plate mesoderm; Retinoic acid

Indexed keywords

FIBROBLAST GROWTH FACTOR; RETINOIC ACID; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FOXF1; TRANSCRIPTION FACTOR HAND1; TRANSCRIPTION FACTOR NKX2.5; TRANSCRIPTION FACTOR SALL3; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ANTERIOR POSTERIOR AXIS; ARTICLE; CONTROLLED STUDY; DIFFERENTIATION; EMBRYO; EMBRYO PATTERN FORMATION; FEMALE; HEART DEVELOPMENT; LATERAL PLATE MESODERM; MESODERM; NEURULATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; XENOPUS;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BODY PATTERNING; CARDIOVASCULAR SYSTEM; FEMALE; FIBROBLAST GROWTH FACTORS; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEART; IN SITU HYBRIDIZATION; MESODERM; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRETINOIN; XENOPUS LAEVIS; XENOPUS PROTEINS;

EID: 82855161395     PISSN: 09254773     EISSN: 18726356     Source Type: Journal    
DOI: 10.1016/j.mod.2011.06.002     Document Type: Article

References (82)

1. Alsan B.H., Schultheiss T.M. Regulation of avian cardiogenesis by Fgf8 signaling. Development 2002, 129:1935-1943.
2. Amaya E., Musci T.J., Kirschner M.W. Expression of a dominant negative mutant of the FGF receptor disrupts mesoderm formation in Xenopus embryos. Cell 1991, 66:257-270.
3. Astorga J., Carlsson P. Hedgehog induction of murine vasculogenesis is mediated by Foxf1 and Bmp4. Development 2007, 134:3753-3761.
4. Bertwistle D., Walmsley M.E., Read E.M., Pizzey J.A., Patient R.K. GATA factors and the origins of adult and embryonic blood in Xenopus: responses to retinoic acid. Mech. Dev. 1996, 57:199-214.
5. Bottcher R.T., Niehrs C. Fibroblast growth factor signaling during early vertebrate development. Endocr. Rev. 2005, 26:63-77.
6. Brade T., Gessert S., Kuhl M., Pandur P. The amphibian second heart field: Xenopus islet-1 is required for cardiovascular development. Dev. Biol. 2007, 311:297-310.
7. Chen Y., Pollet N., Niehrs C., Pieler T. Increased XRALDH2 activity has a posteriorizing effect on the central nervous system of Xenopus embryos. Mech. Dev. 2001, 101:91-103.
8. Chien K.R., Domian I.J., Parker K.K. Cardiogenesis and the complex biology of regenerative cardiovascular medicine. Science 2008, 322:1494-1497.
9. Christen B., Beck C.W., Lombardo A., Slack J.M. Regeneration-specific expression pattern of three posterior Hox genes. Dev. Dyn. 2003, 226:349-355.
10. Christen B., Slack J.M. FGF-8 is associated with anteroposterior patterning and limb regeneration in Xenopus. Dev. Biol. 1997, 192:455-466.
11. Christen B., Slack J.M. Spatial response to fibroblast growth factor signalling in Xenopus embryos. Development 1999, 126:119-125.
12. Chung W.C., Moyle S.S., Tsai P.S. Fibroblast growth factor 8 signaling through fibroblast growth factor receptor 1 is required for the emergence of gonadotropin-releasing hormone neurons. Endocrinology 2008, 149:4997-5003.
13. Ciau-Uitz A., Walmsley M., Patient R. Distinct origins of adult and embryonic blood in Xenopus. Cell 2000, 102:787-796.
14. Collop A.H., Broomfield J.A., Chandraratna R.A., Yong Z., Deimling S.J., Kolker S.J., Weeks D.L., Drysdale T.A. Retinoic acid signaling is essential for formation of the heart tube in Xenopus. Dev. Biol. 2006, 291:96-109.
15. Costa R.M., Soto X., Chen Y., Zorn A.M., Amaya E. Spib is required for primitive myeloid development in Xenopus. Blood 2008, 112:2287-2296.
16. Crump J.G., Maves L., Lawson N.D., Weinstein B.M., Kimmel C.B. An essential role for Fgfs in endodermal pouch formation influences later craniofacial skeletal patterning. Development 2004, 131:5703-5716.
17. de Roos K., Sonneveld E., Compaan B., ten Berge D., Durston A.J., van der Saag P.T. Expression of retinoic acid 4-hydroxylase (CYP26) during mouse and Xenopus laevis embryogenesis. Mech. Dev. 1999, 82:205-211.
18. Deimling S.J., Drysdale T.A. Retinoic acid regulates anterior-posterior patterning within the lateral plate mesoderm of Xenopus. Mech. Dev. 2009, 126:913-923.
19. Delaune E., Lemaire P., Kodjabachian L. Neural induction in Xenopus requires early FGF signalling in addition to BMP inhibition. Development 2005, 132:299-310.
20. Devic E., Paquereau L., Vernier P., Knibiehler B., Audigier Y. Expression of a new G protein-coupled receptor X-msr is associated with an endothelial lineage in Xenopus laevis. Mech. Dev. 1996, 59:129-140.
21. Diez del Corral R., Olivera-Martinez I., Goriely A., Gale E., Maden M., Storey K. Opposing FGF and retinoid pathways control ventral neural pattern, neuronal differentiation, and segmentation during body axis extension. Neuron 2003, 40:65-79.
22. Drysdale T.A., Patterson K.D., Saha M., Krieg P.A. Retinoic acid can block differentiation of the myocardium after heart specification. Dev. Biol. 1997, 188:205-215.
23. Drysdale T.A., Tonissen K.F., Patterson K.D., Crawford M.J., Krieg P.A. Cardiac troponin I is a heart-specific marker in the Xenopus embryo: expression during abnormal heart morphogenesis. Dev. Biol. 1994, 165:432-441.
24. Faber, J., Nieuwkoop, P.D., (1994). Normal table of Xenopus laevis (Daudin): a systematical and chronological survey of the development from the fertilized egg till the end of metamorphosis. Garland Pub., New York, pp. 252 (p., 10 leaves of plates).
25. 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., Garry D.J. 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 2009, 106:814-819.
26. Fletcher R.B., Harland R.M. The role of FGF signaling in the establishment and maintenance of mesodermal gene expression in Xenopus. Dev. Dyn. 2008, 237:1243-1254.
27. Frontini M.J., Nong Z., Gros R., Drangova M., O'Neil C., Rahman M.N., Akawi O., Yin H., Ellis C.G., Pickering J.G. Fibroblast growth factor 9 delivery during angiogenesis produces durable, vasoresponsive microvessels wrapped by smooth muscle cells. Nat. Biotechnol. 2011, 29:421-427.
28. Garavito-Aguilar Z.V., Riley H.E., Yelon D. Hand2 ensures an appropriate environment for cardiac fusion by limiting Fibronectin function. Development 2010, 137:3215-3220.
29. Griffin K., Patient R., Holder N. Analysis of FGF function in normal and no tail zebrafish embryos reveals separate mechanisms for formation of the trunk and the tail. Development 1995, 121:2983-2994.
30. Harland R.M. In situ hybridization: an improved whole-mount method for Xenopus embryos. Methods Cell Biol. 1991, 36:685-695.
31. Hochgreb T., Linhares V.L., Menezes D.C., Sampaio A.C., Yan C.Y., Cardoso W.V., Rosenthal N., Xavier-Neto J. A caudorostral wave of RALDH2 conveys anteroposterior information to the cardiac field. Development 2003, 130:5363-5374.
32. Hollemann T., Chen Y., Grunz H., Pieler T. Regionalized metabolic activity establishes boundaries of retinoic acid signalling. EMBO J. 1998, 17:7361-7372.
33. Hollemann T., Schuh R., Pieler T., Stick R. Xenopus Xsal-1, a vertebrate homolog of the region specific homeotic gene spalt of Drosophila. Mech. Dev. 1996, 55:19-32.
34. Horb M.E., Slack J.M. Endoderm specification and differentiation in Xenopus embryos. Dev. Biol. 2001, 236:330-343.
35. Isaacs H.V., Pownall M.E., Slack J.M. EFGF regulates Xbra expression during Xenopus gastrulation. EMBO J. 1994, 13:4469-4481.
36. Isaacs H.V., Tannahill D., Slack J.M. Expression of a novel FGF in the Xenopus embryo. A new candidate inducing factor for mesoderm formation and anteroposterior specification. Development 1992, 114:711-720.
37. Keegan B.R., Feldman J.L., Begemann G., Ingham P.W., Yelon D. Retinoic acid signaling restricts the cardiac progenitor pool. Science 2005, 307:247-249.
38. Keren-Politansky A., Keren A., Bengal E. Neural ectoderm-secreted FGF initiates the expression of Nkx2.5 in cardiac progenitors via a p38 MAPK/CREB pathway. Dev. Biol. 2009, 335:374-384.
39. Knochel W., Beck J., Meyerhof W. Nucleotide sequence of the Xenopus tropicalis larval beta globin gene. Nucleic Acids Res. 1987, 15:10062.
40. Koga M., Kudoh T., Hamada Y., Watanabe M., Kageura H. A new triple staining method for double in situ hybridization in combination with cell lineage tracing in whole-mount Xenopus embryos. Dev. Growth Differ. 2007, 49:635-645.
41. Koster M., Dillinger K., Knochel W. Genomic structure and embryonic expression of the Xenopus winged helix factors XFD-13/13'. Mech. Dev. 1999, 88:89-93.
42. Lea R., Papalopulu N., Amaya E., Dorey K. Temporal and spatial expression of FGF ligands and receptors during Xenopus development. Dev. Dyn. 2009, 238:1467-1479.
43. Lynch J., McEwan J., Beck C.W. Analysis of the expression of retinoic acid metabolising genes during Xenopus laevis organogenesis. Gene Expr. Patterns. 2011, 11:112-117.
44. Maroon H., Walshe J., Mahmood R., Kiefer P., Dickson C., Mason I. Fgf3 and Fgf8 are required together for formation of the otic placode and vesicle. Development 2002, 129:2099-2108.
45. 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.
46. Martin B.L., Kimelman D. Brachyury establishes the embryonic mesodermal progenitor niche. Genes Dev. 2010, 24:2778-2783.
47. Martinez-Estrada O.M., Lettice L.A., Essafi A., Guadix J.A., Slight J., Velecela V., Hall E., Reichmann J., Devenney P.S., Hohenstein P., Hosen N., Hill R.E., Munoz-Chapuli R., Hastie N.D. Wt1 is required for cardiovascular progenitor cell formation through transcriptional control of Snail and E-cadherin. Nat. Genet. 2010, 42:89-93.
48. Mead P.E., Kelley C.M., Hahn P.S., Piedad O., Zon L.I. SCL specifies hematopoietic mesoderm in Xenopus embryos. Development 1998, 125:2611-2620.
49. Misfeldt A.M., Boyle S.C., Tompkins K.L., Bautch V.L., Labosky P.A., Baldwin H.S. Endocardial cells are a distinct endothelial lineage derived from Flk1+ multipotent cardiovascular progenitors. Dev. Biol. 2009, 333:78-89.
50. Mohammadi M., McMahon G., Sun L., Tang C., Hirth P., Yeh B.K., Hubbard S.R., Schlessinger J. Structures of the tyrosine kinase domain of fibroblast growth factor receptor in complex with inhibitors. Science 1997, 276:955-960.
51. Moreno T.A., Kintner C. Regulation of segmental patterning by retinoic acid signaling during Xenopus somitogenesis. Dev. Cell 2004, 6:205-218.
52. Moretti A., Caron L., Nakano A., Lam J.T., Bernshausen A., Chen Y., Qyang Y., Bu L., Sasaki M., Martin-Puig S., Sun Y., Evans S.M., Laugwitz K.L., Chien K.R. Multipotent embryonic isl1+ progenitor cells lead to cardiac, smooth muscle, and endothelial cell diversification. Cell 2006, 127:1151-1165.
53. Morikawa Y., Cserjesi P. Extra-embryonic vasculature development is regulated by the transcription factor HAND1. Development 2004, 131:2195-2204.
54. Mudumana S.P., Hentschel D., Liu Y., Vasilyev A., Drummond I.A. Odd skipped related1 reveals a novel role for endoderm in regulating kidney versus vascular cell fate. Development 2008, 135:3355-3367.
55. Nakamura K., Yamamoto A., Kamishohara M., Takahashi K., Taguchi E., Miura T., Kubo K., Shibuya M., Isoe T. KRN633: a selective inhibitor of vascular endothelial growth factor receptor-2 tyrosine kinase that suppresses tumor angiogenesis and growth. Mol. Cancer Ther. 2004, 3:1639-1649.
56. Nakazawa F., Nagai H., Shin M., Sheng G. Negative regulation of primitive hematopoiesis by the FGF signaling pathway. Blood 2006, 108:3335-3343.
57. Nechiporuk A., Linbo T., Raible D.W. Endoderm-derived Fgf3 is necessary and sufficient for inducing neurogenesis in the epibranchial placodes in zebrafish. Development 2005, 132:3717-3730.
58. 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.
59. Pownall M.E., Tucker A.S., Slack J.M., Isaacs H.V. EFGF, Xcad3 and Hox genes form a molecular pathway that establishes the anteroposterior axis in Xenopus. Development 1996, 122:3881-3892.
60. Ryckebusch L., Wang Z., Bertrand N., Lin S.C., Chi X., Schwartz R., Zaffran S., Niederreither K. Retinoic acid deficiency alters second heart field formation. Proc. Natl. Acad. Sci. USA 2008, 105:2913-2918.
61. Salanga M.C., Meadows S.M., Myers C.T., Krieg P.A. ETS family protein ETV2 is required for initiation of the endothelial lineage but not the hematopoietic lineage in the Xenopus embryo. Dev. Dyn. 2010, 239:1178-1187.
62. Samuel L.J., Latinkic B.V. Early activation of FGF and nodal pathways mediates cardiac specification independently of Wnt/beta-catenin signaling. PLoS ONE 2009, 4:e7650.
63. Schoenebeck J.J., Keegan B.R., Yelon D. Vessel and blood specification override cardiac potential in anterior mesoderm. Dev. Cell 2007, 13:254-267.
64. Scholpp S., Groth C., Lohs C., Lardelli M., Brand M. Zebrafish fgfr1 is a member of the fgf8 synexpression group and is required for fgf8 signalling at the midbrain-hindbrain boundary. Dev. Genes. Evol. 2004, 214:285-295.
65. Shin M., Nagai H., Sheng G. Notch mediates Wnt and BMP signals in the early separation of smooth muscle progenitors and blood/endothelial common progenitors. Development 2009, 136:595-603.
66. Shiotsugu J., Katsuyama Y., Arima K., Baxter A., Koide T., Song J., Chandraratna R.A., Blumberg B. Multiple points of interaction between retinoic acid and FGF signaling during embryonic axis formation. Development 2004, 131:2653-2667.
67. Sirbu I.O., Zhao X., Duester G. Retinoic acid controls heart anteroposterior patterning by down-regulating Isl1 through the Fgf8 pathway. Dev. Dyn. 2008, 237:1627-1635.
68. Sive H.L., Grainger R.M., Harland R.M. Early Development of Xenopus laevis: A Laboratory Manual 2000, Cold Spring Harbor Laboratory Press, New York.
69. Smart N., Dube K.N., Riley P.R. Identification of Thymosin beta4 as an effector of Hand1-mediated vascular development. Nat. Commun. 2010, 1:1-10.
70. Smith J.C., Price B.M., Green J.B., Weigel D., Herrmann B.G. Expression of a Xenopus homolog of Brachyury (T) is an immediate-early response to mesoderm induction. Cell 1991, 67:79-87.
71. Smith S.J., Kotecha S., Towers N., Latinkic B.V., Mohun T.J. XPOX2-peroxidase expression and the XLURP-1 promoter reveal the site of embryonic myeloid cell development in Xenopus. Mech. Dev. 2002, 117:173-186.
72. Sparrow D.B., Kotecha S., Towers N., Mohun T.J. Xenopus eHAND: a marker for the developing cardiovascular system of the embryo that is regulated by bone morphogenetic proteins. Mech. Dev. 1998, 71:151-163.
73. Teng M., Duong T.T., Johnson A.T., Klein E.S., Wang L., Khalifa B., Chandraratna R.A. Identification of highly potent retinoic acid receptor alpha-selective antagonists. J. Med. Chem. 1997, 40:2445-2451.
74. Tonissen K.F., Drysdale T.A., Lints T.J., Harvey R.P., Krieg P.A. XNkx-2.5, a Xenopus gene related to Nkx-2.5 and tinman: evidence for a conserved role in cardiac development. Dev. Biol. 1994, 162:325-328.
75. van Wijk B., van den Berg G., Abu-Issa R., Barnett P., van der Velden S., Schmidt M., Ruijter J.M., Kirby M.L., Moorman A.F., van den Hoff M.J. Epicardium and myocardium separate from a common precursor pool by crosstalk between bone morphogenetic protein- and fibroblast growth factor-signaling pathways. Circ. Res. 2009, 105:431-441.
76. Walmsley M., Cleaver D., Patient R. Fibroblast growth factor controls the timing of Scl, Lmo2, and Runx1 expression during embryonic blood development. Blood 2008, 111:1157-1166.
77. Waxman J.S., Keegan B.R., Roberts R.W., Poss K.D., Yelon D. Hoxb5b acts downstream of retinoic acid signaling in the forelimb field to restrict heart field potential in zebrafish. Dev. Cell 2008, 15:923-934.
78. Xiong J.W. Molecular and developmental biology of the hemangioblast. Dev. Dyn. 2008, 237:1218-1231.
79. Yang L., Soonpaa M.H., Adler E.D., Roepke T.K., Kattman S.J., Kennedy M., Henckaerts E., Bonham K., Abbott G.W., Linden R.M., Field L.J., Keller G.M. Human cardiovascular progenitor cells develop from a KDR+ embryonic-stem-cell-derived population. Nature 2008, 453:524-528.
80. Yin C., Kikuchi K., Hochgreb T., Poss K.D., Stainier D.Y. Hand2 regulates extracellular matrix remodeling essential for gut-looping morphogenesis in zebrafish. Dev. Cell 2010, 18:973-984.
81. Zhao X., Duester G. Effect of retinoic acid signaling on Wnt/beta-catenin and FGF signaling during body axis extension. Gene Expr. Patterns 2009, 9:430-435.
82. Zhao X., Sirbu I.O., Mic F.A., Molotkova N., Molotkov A., Kumar S., Duester G. Retinoic acid promotes limb induction through effects on body axis extension but is unnecessary for limb patterning. Curr. Biol. 2009, 19:1050-1057.