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A Potential Role of fgf4, fgf24, and fgf17 in Pharyngeal Pouch Formation in Zebrafish

  • Sil Jin (Division of Applied Life Science, Gyeongsang National University) ;
  • Chong Pyo Choe (Division of Life Science, Gyeongsang National University)
  • 투고 : 2024.03.19
  • 심사 : 2024.05.15
  • 발행 : 2024.06.30

초록

In vertebrates, Fgf signaling is essential for the development of pharyngeal pouches, which controls facial skeletal development. Genetically, fgf3 and fgf8 are required for pouch formation in mice and zebrafish. However, loss-of-function phenotypes of fgf3 and fgf8 are milder than expected in mice and zebrafish, which suggests that an additional fgf gene(s) would be involved in pouch formation. Here, we analyzed the expression, regulation, and function of three fgfs, fgf4, fgf24, and fgf17, during pouch development in zebrafish. We find that they are expressed in the distinct regions of pharyngeal endoderm in pouch formation, with fgf4 and fgf17 also being expressed in the adjacent mesoderm, in addition to previously reported endodermal fgf3 and mesodermal fgf8 expression. The endodermal expression of fgf4, fgf24, and fgf17 and the mesodermal expression of fgf4 and fgf17 are positively regulated by Tbx1 but not by Fgf3, in pouch formation. Fgf8 is required to express the endodermal expression of fgf4 and fgf24. Interestingly, however, single mutant, all double mutant combinations, and triple mutant for fgf4, fgf24, and fgf17 do not show any defects in pouches and facial skeletons. Considering a high degree of genetic redundancy in the Fgf signaling components in craniofacial development in zebrafish, our result suggests that fgf4, fgf24, and fgf17 have a potential role for pouch formation, with a redundancy with other fgf gene(s).

키워드

과제정보

This work was supported by a grant from Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Science and ICT (2022R1F1A1060199).

참고문헌

  1. Aggarwal VS, Liao J, Bondarev A, Schimmang T, Lewandoski M, Locker J, Shanske A, Campione M, Morrow BE (2006) Dissection of Tbx1 and Fgf interactions in mouse models of 22q11DS suggests functional redundancy. Hum Mol Genet 15:3219-3228.
  2. Brito JM, Teillet MA, Le Douarin NM (2006) An early role for sonic hedgehog from foregut endoderm in jaw development: Ensuring neural crest cell survival. Proc Natl Acad Sci USA 103:11607-11612.
  3. Choe CP (2023) A feasible role of neuropilin signaling in pharyngeal pouch formation in zebrafish. Dev Reprod 27:137-147.
  4. Choe CP, Collazo A, Trinh LA, Pan L, Moens CB, Crump JG (2013) Wnt-dependent epithelial transitions drive pharyngeal pouch formation. Dev Cell 24:296-309.
  5. Choe CP, Crump JG (2014) Tbx1 controls the morphogenesis of pharyngeal pouch epithelia through mesodermal Wnt11r and Fgf8a. Development 141:3583-3593.
  6. Crump JG, Maves L, Lawson ND, Weinstein BM, Kimmel CB (2004) An essential role for Fgfs in endodermal pouch formation influences later craniofacial skeletal patterning. Development 131:5703-5716.
  7. Dickmeis T, Mourrain P, Saint-Etienne L, Fischer N, Aanstad P, Clark M, Strahle U, Rosa F (2001) A crucial component of the endoderm formation pathway, CASANOVA, is encoded by a novel sox-related gene. Genes Dev 15:1487-1492.
  8. Draper BW, Stock DW, Kimmel CB (2003) Zebrafish fgf24 functions with fgf8 to promote posterior mesodermal development. Development 130:4639-4654.
  9. El-Brolosy MA, Kontarakis Z, Rossi A, Kuenne C, Gunther S, Fukuda N, Kikhi K, Boezio GLM, Takacs CM, Lai SL, Fukuda R, Gerri C, Giraldez AJ, Stainier DYR (2019) Genetic compensation triggered by mutant mRNA degradation. Nature 568:193-197.
  10. Furthauer M, Van Celst J, Thisse C, Thisse B (2004) Fgf signalling controls the dorsoventral patterning of the zebrafish embryo. Development 131:2853-2864.
  11. Grevellec A, Tucker AS (2010) The pharyngeal pouches and clefts: Development, evolution, structure and derivatives. Semin Cell Dev Biol 21:325-332.
  12. Herzog W, Sonntag C, von der Hardt S, Roehl HH, Varga ZM, Hammerschmidt M (2004) Fgf3 signaling from the ventral diencephalon is required for early specification and subsequent survival of the zebrafish adenohypophysis. Development 131:3681-3692.
  13. Hwang WY, Fu Y, Reyon D, Maeder ML, Tsai SQ, Sander JD, Peterson RT, Yeh JR, Joung JK (2013) Efficient genome editing in zebrafish using a CRISPR-Cas system. Nat Biotechnol 31:227-229.
  14. Jackson A, Kasah S, Mansour SL, Morrow B, Basson MA (2014) Endoderm-specific deletion of Tbx1 reveals an FGF-independent role for Tbx1 in pharyngeal apparatus morphogenesis. Dev Dyn 243:1143-1151.
  15. Jin S, O J, Stellabotte F, Choe CP (2018) Foxi1 promotes late-stage pharyngeal pouch morphogenesis through ectodermal Wnt4a activation. Dev Biol 441:12-18.
  16. Kikuchi Y, Agathon A, Alexander J, Thisse C, Waldron S, Yelon D, Thisse B, Stainier DY (2001) casanova encodes a novel Sox-related protein necessary and sufficient for early endoderm formation in zebrafish. Genes Dev 15:1493-1505.
  17. Kwan KM, Fujimoto E, Grabher C, Mangum BD, Hardy ME, Campbell DS, Parant JM, Yost HJ, Kanki JP, Chien CB (2007) The Tol2kit: A multisite gateway-based construction kit for Tol2 transposon transgenesis constructs. Dev Dyn 236:3088-3099.
  18. Leerberg DM, Hopton RE, Draper BW (2019) Fibroblast growth factor receptors function redundantly during zebrafish embryonic development. Genetics 212:1301-1319.
  19. Lindsay EA, Vitelli F, Su H, Morishima M, Huynh T, Pramparo T, Jurecic V, Ogunrinu G, Sutherland HF, Scambler PJ, Bradley A, Baldini A (2001) Tbx1 haploinsufficieny in the DiGeorge syndrome region causes aortic arch defects in mice. Nature 410:97-101.
  20. Liu YH, Lin TC, Hwang SL (2020) Zebrafish Pax1a and Pax1b are required for pharyngeal pouch morphogenesis and ceratobranchial cartilage development. Mech Dev 161:103598.
  21. Nissen RM, Yan J, Amsterdam A, Hopkins N, Burgess SM (2003) Zebrafish foxi one modulates cellular responses to Fgf signaling required for the integrity of ear and jaw patterning. Development 130:2543-2554.
  22. Niswander L, Martin GR (1992) Fgf-4 expression during gastrulation, myogenesis, limb and tooth development in the mouse. Development 114:755-768.
  23. Ober EA, Olofsson B, Makinen T, Jin SW, Shoji W, Koh GY, Alitalo K, Stainier DY (2004) Vegfc is required for vascular development and endoderm morphogenesis in zebrafish. EMBO Rep 5:78-84.
  24. Okada K, Inohaya K, Mise T, Kudo A, Takada S, Wada H (2016) Reiterative expression of pax1 directs pharyngeal pouch segmentation in medaka. Development 143:1800-1810.
  25. Piotrowski T, Ahn DG, Schilling TF, Nair S, Ruvinsky I, Geisler R, Rauch GJ, Haffter P, Zon LI, Zhou Y, Foott H, Dawid IB, Ho RK (2003) The zebrafish van gogh mutation disrupts tbx1, which is involved in the DiGeorge deletion syndrome in humans. Development 130:5043-5052.
  26. Piotrowski T, Nusslein-Volhard C (2000) The endoderm plays an important role in patterning the segmented pharyngeal region in zebrafish (Danio rerio). Dev Biol 225:339-356.
  27. Reifers F, Bohli H, Walsh EC, Crossley PH, Stainier DY, Brand M (1998) Fgf8 is mutated in zebrafish acerebellar (ace) mutants and is required for maintenance of midbrain-hindbrain boundary development and somitogenesis. Development 125:2381-2395.
  28. Rossi A, Kontarakis Z, Gerri C, Nolte H, Holper S, Kruger M, Stainier DY (2015) Genetic compensation induced by deleterious mutations but not gene knockdowns. Nature 524:230-233.
  29. Tallafuss A, Bally-Cuif L (2003) Tracing of her5 progeny in zebrafish transgenics reveals the dynamics of midbrain-hindbrain neurogenesis and maintenance. Development 130:4307-4323.
  30. Tran HT, Delvaeye M, Verschuere V, Descamps E, Crabbe E, Van Hoorebeke L, McCrea P, Adriaens D, Van Roy F, Vleminckx K (2011) ARVCF depletion cooperates with Tbx1 deficiency in the development of 22q11.2DS-like phenotypes in Xenopus. Dev Dyn 240:2680-2687.
  31. van Eeden FJ, Granato M, Schach U, Brand M, Furutani-Seiki M, Haffter P, Hammerschmidt M, Heisenberg CP, Jiang YJ, Kane DA, Kelsh RN, Mullins MC, Odenthal J, Warga RM, Nusslein-Volhard C (1996) Genetic analysis of fin formation in the zebrafish, Danio rerio. Development 123:255-262.
  32. Wright TJ, Hatch EP, Karabagli H, Karabagli P, Schoenwolf GC, Mansour SL (2003) Expression of mouse fibroblast growth factor and fibroblast growth factor receptor genes during early inner ear development. Dev Dyn 228:267-272.
  33. Zuniga E, Rippen M, Alexander C, Schilling TF, Crump JG (2011) Gremlin 2 regulates distinct roles of BMP and Endothelin 1 signaling in dorsoventral patterning of the facial skeleton. Development 138:5147-5156.