Development and Reproduction (한국발생생물학회지:발생과생식)

The Korean Society of Developmental Biology (한국발생생물학회)
권호 표지
DOI QR코드

DOI QR Code

A Feasible Role of Neuropilin Signaling in Pharyngeal Pouch Formation in Zebrafish

  • Chong Pyo Choe (Division of Life Science, Gyeongsang National University)
  • Received : 2023.07.21
  • Accepted : 2023.09.14
  • Published : 2023.09.30
Download PDF
⟨ Previous Next ⟩

Abstract

Pharyngeal pouches are an important epithelial structure controlling facial skeletal development in vertebrates. A series of pouches arise sequentially in the pharyngeal endoderm through collective cell migration followed by rearrangement of pouch-forming cells. While crucial transcription factors and signaling molecules have been identified in pouch formation, a role for Neuropilins (Nrps) in pouch development has not yet been analyzed in any vertebrates. Nrps are cell surface receptors essential for angiogenesis and axon guidance. In all vertebrates, the two Nrp family members, Nrp1 and Nrp2, are conserved in the genome, with two paralogs for Nrp1 (Nrp1a and Nrp1b) and Nrp2 (Nrp2a and Nrp2b) being identified in zebrafish. Here, I report a potential requirement of Nrp signaling in pouch development in zebrafish. nrp1a and nrp2b were expressed in the developing pouches, with sema3d, a ligand for Nrps, being expressed in the pouches. Knocking down Nrps signaling in the pharyngeal endoderm led to severe defects in pouches and facial cartilages. In addition, blocking Mitogen-activated protein kinase (MAPK) activities, a downstream effector of Nrp signaling, in the pharyngeal endoderm caused similar defects in pouches and facial skeleton to those by knocking down Nrps signaling. My results suggest that Nrp signaling acts for pouch formation through MAPK.

Keywords

Acknowledgement

I thank Sil Jin for technical assistance. 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).

References

  1. Bechara A, Nawabi H, Moret F, Yaron A, Weaver E, Bozon M, Abouzid K, Guan JL, Tessier-Lavigne M, Lemmon V, Castellani V (2008) FAK-MAPK-dependent adhesion disassembly downstream of L1 contributes to semaphorin3A-induced collapse. EMBO J 27:1549-1562. https://doi.org/10.1038/emboj.2008.86
  2. Bovenkamp DE, Goishi K, Bahary N, Davidson AJ, Zhou Y, Becker T, Becker CG, Zon LI, Klagsbrun M (2004) Expression and mapping of duplicate neuropilin-1 and neuropilin-2 genes in developing zebrafish. Gene Expr Patterns 4:361-370. https://doi.org/10.1016/j.modgep.2004.01.014
  3. Caunt M, Mak J, Liang WC, Stawicki S, Pan Q, Tong RK, Kowalski J, Ho C, Reslan HB, Ross J, Berry L, Kasman I, Zlot C, Cheng Z, Le Couter J, Filvaroff EH, Plowman G, Peale F, French D, Carano R, Koch AW, Wu Y, Watts RJ, Tessier-Lavigne M, Bagri A (2008) Blocking neuropilin-2 function inhibits tumor cell metastasis. Cancer Cell 13:331-342. https://doi.org/10.1016/j.ccr.2008.01.029
  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. https://doi.org/10.1016/j.devcel.2012.12.003
  5. Choe CP, Crump JG (2014) Tbx1 controls the morphogenesis of pharyngeal pouch epithelia through mesodermal Wnt11r and Fgf8a. Development 141:3583-3593. https://doi.org/10.1242/dev.111740
  6. Choe CP, Crump JG (2015) Eph-Pak2a signaling regulates branching of the pharyngeal endoderm by inhibiting late-stage epithelial dynamics. Development 142:1089-1094.
  7. Costa G, Harrington KI, Lovegrove HE, Page DJ, Chakravartula S, Bentley K, Herbert SP (2016) Asymmetric division coordinates collective cell migration in angiogenesis. Nat Cell Biol 18: 1292-1301. https://doi.org/10.1038/ncb3443
  8. 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. https://doi.org/10.1242/dev.01444
  9. 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. https://doi.org/10.1101/gad.196901
  10. Driscoll DA, Budarf ML, Emanuel BS (1992) A genetic etiology for DiGeorge syndrome: Consistent deletions and microdeletions of 22q11. Am J Hum Genet 50:924-933.
  11. Fantin A, Vieira JM, Plein A, Denti L, Fruttiger M, Pollard JW, Ruhrberg C (2013) NRP1 acts cell autonomously in endothelium to promote tip cell function during sprouting angiogenesis. Blood 121:2352-2362. https://doi.org/10.1182/blood-2012-05-424713
  12. Fung TM, Ng KY, Tong M, Chen JN, Chai S, Chan KT, Law S, Lee NP, Choi MY, Li B, Cheung AL, Tsao SW, Qin YR, Guan XY, Chan KW, Ma S (2016) Neuropilin-2 promotes tumourigenicity and metastasis in oesophageal squamous cell carcinoma through ERK-MAPK-ETV4-MMP-E-cadherin deregulation. J Pathol 239:309-319. https://doi.org/10.1002/path.4728
  13. Grevellec A, Tucker AS (2010) The pharyngeal pouches and clefts: Development, evolution, structure and derivatives. Semin Cell Dev Biol 21:325-332. https://doi.org/10.1016/j.semcdb.2010.01.022
  14. Guo HF, Vander Kooi CW (2015) Neuropilin functions as an essential cell surface receptor. J Biol Chem 290:29120-29126.
  15. Hai R, You Q, Wu F, Qiu G, Yang Q, Shu L, Xie L, Zhou X (2022) Semaphorin 3D inhibits proliferation and migration of papillary thyroid carcinoma by regulating MAPK/ERK signaling pathway. Mol Biol Rep 49:3793-3802. https://doi.org/10.1007/s11033-022-07220-8
  16. Izumi Y, Kim S, Namba M, Yasumoto H, Miyazaki H, Hoshiga M, Kaneda Y, Morishita R, Zhan Y, Iwao H (2001) Gene transfer of dominant-negative mutants of extracellular signal-regulated kinase and c-Jun NH2-terminal kinase prevents neointimal formation in balloon-injured rat artery. Circ Res 88:1120-1126. https://doi.org/10.1161/hh1101.091267
  17. 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. https://doi.org/10.1016/j.ydbio.2018.06.011
  18. Jones EAV, Yuan L, Breant C, Watts RJ, Eichmann A (2008) Separating genetic and hemodynamic defects in neuropilin 1 knockout embryos. Development 135:2479-2488. https://doi.org/10.1242/dev.014902
  19. Karpanen T, Heckman CA, Keskitalo S, Jeltsch M, Ollila H, Neufeld G, Tamagnone L, Alitalo K (2006) Functional interaction of VEGF-C and VEGF-D with neuropilin receptors. FASEB J 20:1462-1472. https://doi.org/10.1096/fj.05-5646com
  20. Kikuchi Y, Agathon A, Alexander J, Thisse C, Waldron S, Yelon D, Thisse B, Stainier DYR (2001) casanova Encodes a novel Sox-related protein necessary and sufficient for early endoderm formation in zebrafish. Genes Dev 15:1493-1505. https://doi.org/10.1101/gad.892301
  21. Kwan KM, Fujimoto E, Grabher C, Mangum BD, Hardy ME, Campbell DS, Parant JM, Joseph Yost H, Kanki JP, Chien CB (2007) The Tol2kit: A multisite gateway-based construction kit for Tol2 transposon transgenesis constructs. Dev Dyn 236:3088-3099. https://doi.org/10.1002/dvdy.21343
  22. Lee P, Goishi K, Davidson AJ, Mannix R, Zon L, Klagsbrun M (2002) Neuropilin-1 is required for vascular development and is a mediator of VEGF-dependent angiogenesis in zebrafish. Proc Natl Acad Sci USA 99:10470-10475. https://doi.org/10.1073/pnas.162366299
  23. 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. https://doi.org/10.1038/35065105
  24. Liu YH, Lin TC, Hwang SPL (2020) Zebrafish Pax1a and Pax1b are required for pharyngeal pouch morphogenesis and ceratobranchial cartilage development. Mech Dev 161:103598.
  25. Mork L, Crump JG (2015) Chapter ten - Zebrafish craniofacial development: A window into early patterning. Curr Top Dev Biol 115:235-269. https://doi.org/10.1016/bs.ctdb.2015.07.001
  26. Mumblat Y, Kessler O, Ilan N, Neufeld G (2015) Full-length semaphorin-3C is an inhibitor of tumor lymphangiogenesis and metastasis. Cancer Res 75:2177-2186.
  27. Nakayama H, Bruneau S, Kochupurakkal N, Coma S, Briscoe DM, Klagsbrun M (2015) Regulation of mTOR signaling by semaphorin 3F-neuropilin 2 interactions in vitro and in vivo. Sci Rep 5:11789.
  28. 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. https://doi.org/10.1242/dev.00455
  29. Ober EA, Olofsson B, Makinen T, Jin SW, Shoji W, Koh GY, Alitalo K, Stainier DYR (2004) Vegfc is required for vascular development and endoderm morphogenesis in zebrafish. EMBO Rep 5:78-84.
  30. 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.
  31. Parker MW, Guo HF, Li X, Linkugel AD, Vander Kooi CW (2012) Function of members of the neuropilin family as essential pleiotropic cell surface receptors. Biochemistry 51:9437-9446. https://doi.org/10.1021/bi3012143
  32. 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. https://doi.org/10.1006/dbio.2000.9842
  33. Piotrowski T, Ahn D, 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. https://doi.org/10.1242/dev.00704
  34. Renzi MJ, Feiner L, Koppel AM, Raper JA (1999) A dominant negative receptor for specific secreted semaphorins is generated by deleting an extracellular domain from neuropilin-1. J Neurosci 19:7870-7880. https://doi.org/10.1523/JNEUROSCI.19-18-07870.1999
  35. Serini G, Valdembri D, Zanivan S, Morterra G, Burkhardt C, Caccavari F, Zammataro L, Primo L, Tamagnone L, Logan M, Tessier-Lavigne M, Taniguchi M, Puschel AW, Bussolino F (2003) Class 3 semaphorins control vascular morphogenesis by inhibiting integrin function. Nature 424:391-397. https://doi.org/10.1038/nature01784
  36. Soker S, Takashima S, Miao HQ, Neufeld G, Klagsbrun M (1998) Neuropilin-1 is expressed by endothelial and tumor cells as an isoform-specific receptor for vascular endothelial growth factor. Cell 92:735-745. https://doi.org/10.1016/S0092-8674(00)81402-6
  37. Takashima S, Kitakaze M, Asakura M, Asanuma H, Sanada S, Tashiro F, Niwa H, Miyazaki Ji J, Hirota S, Kitamura Y, Kitsukawa T, Fujisawa H, Klagsbrun M, Hori M (2002) Targeting of both mouse neuropilin-1 and neuropilin-2 genes severely impairs developmental yolk sac and embryonic angiogenesis. Proc Natl Acad Sci USA 99:3657-3662. https://doi.org/10.1073/pnas.022017899
  38. 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. https://doi.org/10.1242/dev.00662
  39. Tamagnone L, Mazzone M (2011) Semaphorin signals on the road of endothelial tip cells. Dev Cell 21:189-190.
  40. 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. https://doi.org/10.1002/dvdy.22765
  41. Wey JS, Gray MJ, Fan F, Belcheva A, McCarty MF, Stoeltzing O, Somcio R, Liu W, Evans DB, Klagsbrun M, Gallick GE, Ellis LM (2005) Overexpression of neuropilin-1 promotes constitutive MAPK signalling and chemoresistance in pancreatic cancer cells. Br J Cancer 93: 233-241. https://doi.org/10.1038/sj.bjc.6602663
  42. Xu Y, Yuan L, Mak J, Pardanaud L, Caunt M, Kasman I, Larrivee B, del Toro R, Suchting S, Medvinsky A, Silva J, Yang J, Thomas JL, Koch AW, Alitalo K, Eichmann A, Bagri A (2010) Neuropilin-2 mediates VEGF-C-induced lymphatic sprouting together with VEGFR3. J Cell Biol 188:115-130. https://doi.org/10.1083/jcb.200903137
  43. Yang WJ, Hu J, Uemura A, Tetzlaff F, Augustin HG, Fischer A (2015) Semaphorin-3C signals through Neuropilin-1 and PlexinD1 receptors to inhibit pathological angiogenesis. EMBO Mol Med 7:1267-1284.
  44. Yaniv K, Isogai S, Castranova D, Dye L, Hitomi J, Weinstein BM (2006) Live imaging of lymphatic development in the zebrafish. Nat Med 12:711-716. https://doi.org/10.1038/nm1427
  45. Yuan L, Moyon D, Pardanaud L, Bréant C, Karkkainen MJ, Alitalo K, Eichmann A (2002) Abnormal lymphatic vessel development in neuropilin 2 mutant mice. Development 129:4797-4806. https://doi.org/10.1242/dev.129.20.4797
  46. Zhang W, Liu HT (2002) MAPK signal pathways in the regulation of cell proliferation in mammalian cells. Cell Res 12:9-18. https://doi.org/10.1038/sj.cr.7290105
  47. 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. https://doi.org/10.1242/dev.067785