The Fgf8 Subfamily (Fgf8, Fgf17 and Fgf18) is Required for Closure of the Embryonic Ventral Body Wall

Overview

Journal Development

Specialty Biology

Date 2020 Sep 10

PMID 32907848

Citations 8

Authors

Michael Boylan

Matthew J Anderson

David M Ornitz

Mark Lewandoski

Affiliations

Soon will be listed here.

Abstract

The closure of the embryonic ventral body wall in amniotes is an important morphogenetic event and is essential for life. Defects in human ventral wall closure are a major class of birth defect and a significant health burden. Despite this, very little is understood about how the ventral body wall is formed. Here, we show that fibroblast growth factor (FGF) ligands FGF8, FGF17 and FGF18 are essential for this process. Conditional mouse mutants for these genes display subtle migratory defects in the abdominal muscles of the ventral body wall and an enlarged umbilical ring, through which the internal organs are extruded. By refining where and when these genes are required using different Cre lines, we show that and are required in the presomitic mesoderm, whereas is required in the somites. This study identifies complex and multifactorial origins of ventral wall defects and has important implications for understanding their origins during embryonic development.

Citing Articles

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References

Benazet J, Zeller R . Vertebrate limb development: moving from classical morphogen gradients to an integrated 4-dimensional patterning system. Cold Spring Harb Perspect Biol. 2010; 1(4):a001339. PMC: 2773624. DOI: 10.1101/cshperspect.a001339. View

Peters K, Werner S, Chen G, Williams L . Two FGF receptor genes are differentially expressed in epithelial and mesenchymal tissues during limb formation and organogenesis in the mouse. Development. 1992; 114(1):233-43. DOI: 10.1242/dev.114.1.233. View

Murdoch J, Damrau C, Paudyal A, Bogani D, Wells S, Greene N . Genetic interactions between planar cell polarity genes cause diverse neural tube defects in mice. Dis Model Mech. 2014; 7(10):1153-63. PMC: 4174526. DOI: 10.1242/dmm.016758. View

Carnaghan H, Roberts T, Savery D, Norris F, McCann C, Copp A . Novel exomphalos genetic mouse model: the importance of accurate phenotypic classification. J Pediatr Surg. 2013; 48(10):2036-42. PMC: 4030649. DOI: 10.1016/j.jpedsurg.2013.04.010. View

Yoon J, Moon R, Wold B . The bHLH class protein pMesogenin1 can specify paraxial mesoderm phenotypes. Dev Biol. 2000; 222(2):376-91. DOI: 10.1006/dbio.2000.9717. View

Jin L, Wu J, Bellusci S, Zhang J . Fibroblast Growth Factor 10 and Vertebrate Limb Development. Front Genet. 2019; 9:705. PMC: 6338048. DOI: 10.3389/fgene.2018.00705. View

Kitagaki J, Ueda Y, Chi X, Sharma N, Elder C, Truffer E . FGF8 is essential for formation of the ductal system in the male reproductive tract. Development. 2011; 138(24):5369-78. PMC: 3222212. DOI: 10.1242/dev.051888. View

Orr-Urtreger A, Givol D, Yayon A, Yarden Y, Lonai P . Developmental expression of two murine fibroblast growth factor receptors, flg and bek. Development. 1991; 113(4):1419-34. DOI: 10.1242/dev.113.4.1419. View

Herman T, Siegel M . Apert syndrome with omphalocele. J Perinatol. 2010; 30(10):695-7. DOI: 10.1038/jp.2010.72. View

10.

Sun X, Meyers E, Lewandoski M, Martin G . Targeted disruption of Fgf8 causes failure of cell migration in the gastrulating mouse embryo. Genes Dev. 1999; 13(14):1834-46. PMC: 316887. DOI: 10.1101/gad.13.14.1834. View

11.

Xu J, Liu Z, Ornitz D . Temporal and spatial gradients of Fgf8 and Fgf17 regulate proliferation and differentiation of midline cerebellar structures. Development. 2000; 127(9):1833-43. DOI: 10.1242/dev.127.9.1833. View

12.

Jukkola T, Trokovic R, Maj P, Lamberg A, Mankoo B, Pachnis V . Meox1Cre: a mouse line expressing Cre recombinase in somitic mesoderm. Genesis. 2005; 43(3):148-53. DOI: 10.1002/gene.20163. View

13.

Boucherat O, Nadeau V, Berube-Simard F, Charron J, Jeannotte L . Crucial requirement of ERK/MAPK signaling in respiratory tract development. Development. 2014; 141(16):3197-211. DOI: 10.1242/dev.110254. View

14.

Anderson M, Schimmang T, Lewandoski M . An FGF3-BMP Signaling Axis Regulates Caudal Neural Tube Closure, Neural Crest Specification and Anterior-Posterior Axis Extension. PLoS Genet. 2016; 12(5):e1006018. PMC: 4856314. DOI: 10.1371/journal.pgen.1006018. View

15.

Xu J, Lawshe A, MacArthur C, Ornitz D . Genomic structure, mapping, activity and expression of fibroblast growth factor 17. Mech Dev. 1999; 83(1-2):165-78. DOI: 10.1016/s0925-4773(99)00034-9. View

16.

Stolte D, Huang R, Christ B . Spatial and temporal pattern of Fgf-8 expression during chicken development. Anat Embryol (Berl). 2002; 205(1):1-6. DOI: 10.1007/s00429-002-0227-z. View

17.

Williams T . Animal models of ventral body wall closure defects: a personal perspective on gastroschisis. Am J Med Genet C Semin Med Genet. 2008; 148C(3):186-91. DOI: 10.1002/ajmg.c.30179. View

18.

Choi H, Schwarzkopf M, Fornace M, Acharya A, Artavanis G, Stegmaier J . Third-generation hybridization chain reaction: multiplexed, quantitative, sensitive, versatile, robust. Development. 2018; 145(12). PMC: 6031405. DOI: 10.1242/dev.165753. View

19.

Maruoka Y, Ohbayashi N, Hoshikawa M, Itoh N, Hogan B, Furuta Y . Comparison of the expression of three highly related genes, Fgf8, Fgf17 and Fgf18, in the mouse embryo. Mech Dev. 1998; 74(1-2):175-7. DOI: 10.1016/s0925-4773(98)00061-6. View

20.

Ornitz D, Itoh N . The Fibroblast Growth Factor signaling pathway. Wiley Interdiscip Rev Dev Biol. 2015; 4(3):215-66. PMC: 4393358. DOI: 10.1002/wdev.176. View