본문 바로가기
KERD
논문KCI 등재

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

2

조회

0

다운로드

1

인용

0

참고문헌

키워드

주제분류생물학

초록

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.

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.

참고문헌 (47)

  1. Bechara A, "FAK–MAPK-dependent adhesion disassembly downstream of L1 contributes to semaphorin3A-induced collapse", EMBO J, 27, pp.1549~1562 (2008)
  2. Bovenkamp DE, "Expression and mapping of duplicate neuropilin-1 and neuropilin-2genes in developing zebrafish", Gene Expr Patterns, 4, pp.361~370 (2004)
  3. Caunt M, "Blocking neuropilin-2 function inhibits tumor cell metastasis", Cancer Cell, 13, pp.331~342 (2008)
  4. Choe CP, "Wnt-dependent epithelial transitions drive pharyngeal pouch formation", Dev Cell, 24, pp.296~309 (2013)
  5. Choe CP, "Tbx1 controls the morphogenesis of pharyngeal pouch epithelia through mesodermal Wnt11r and Fgf8a", Development, 141, pp.3583~3593 (2014)
  6. Choe CP, "Eph-Pak2a signaling regulates branching of the pharyngeal endoderm by inhibiting late-stage epithelial dynamics", Development, 142, pp.1089~1094 (2015)
  7. Costa G, "Asymmetric division coordinates collective cell migration in angiogenesis", Nat Cell Biol, 18, pp.1292~1301 (2016)
  8. Crump JG, "An essential role for Fgfs in endodermal pouch formation influences later craniofacial skeletal patterning", Development, 131, pp.5703~5716 (2004)
  9. Dickmeis T, "A crucial component of the endoderm formation pathway, CASANOVA, is encoded by a novel sox-related gene", Genes Dev, 15, pp.1487~1492 (2001)
  10. Driscoll DA, "A genetic etiology for DiGeorge syndrome:Consistent deletions and microdeletions of 22q11", Am J Hum Genet, 50, pp.924~933 (1992)
  11. Fantin A, "NRP1 acts cell autonomously in endothelium to promote tip cell function during sprouting angiogenesis", Blood, 121, pp.2352~2362 (2013)
  12. Fung TM, "Neuropilin-2 promotes tumourigenicity and metastasis in oesophageal squamous cell carcinoma through ERK–MAPK–ETV4–MMP–E-cadherin deregulation", J Pathol, 239, pp.309~319 (2016)
  13. Grevellec A, "The pharyngeal pouches and clefts: Development, evolution, structure and derivatives", Semin Cell Dev Biol, 21, pp.325~332 (2010)
  14. Guo HF, "Neuropilin functions as an essential cell surface receptor", J Biol Chem, 290, pp.29120~29126 (2015)
  15. Hai R, "Semaphorin 3D inhibits proliferation and migration of papillary thyroid carcinoma by regulating MAPK", ERK signaling pathway, 2022, pp.49, 3793~3802
  16. Izumi Y, "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, pp.1120~1126 (2001)
  17. Jin S, "Foxi1 promotes late-stage pharyngeal pouch morphogenesis through ectodermal Wnt4a activation", Dev Biol, 441, pp.12~18 (2018)
  18. Jones EAV, "Separating genetic and hemodynamic defects in neuropilin 1 knockout embryos", Development, 135, pp.2479~2488 (2008)
  19. Kärpänen T, "Functional interaction of VEGF-C and VEGF-D with neuropilin receptors", FASEB J, 20, pp.1462~1472 (2006)
  20. Kikuchi Y, "casanova Encodes a novel Sox-related protein necessary and sufficient for early endoderm formation in zebrafish", Genes Dev, 15, pp.1493~1505 (2001)
  21. Kwan KM, "The Tol2kit: A multisite gateway-based construction kit for Tol2 transposon transgenesis constructs", Dev Dyn, 236, pp.3088~3099 (2007)
  22. Lee P, "Neuropilin-1 is required for vascular development and is a mediator of VEGF-dependent angiogenesis in zebrafish", Proc Natl Acad Sci USA, 99, pp.10470~10475 (2002)
  23. Lindsay EA, "Tbx1 haploinsufficieny in the DiGeorge syndrome region causes aortic arch defects in mice", Nature, 410, pp.97~101 (2001)
  24. Liu YH, "Zebrafish Pax1a and Pax1b are required for pharyngeal pouch morphogenesis and ceratobranchial cartilage development", Mech Dev, 161, pp.103598~ (2020)
  25. Mork L, "Chapter ten - Zebrafish craniofacial development: A window into early patterning", Curr Top Dev Biol, 115, pp.235~269 (2015)
  26. Mumblat Y, "Full-length semaphorin-3C is an inhibitor of tumor lymphangiogenesis and metastasis", Cancer Res, 75, pp.2177~2186 (2015)
  27. Nakayama H, "Regulation of mTOR signaling by semaphorin 3F-neuropilin 2 interactions in vitro and in vivo", Sci Rep, 5, pp.11789~ (2015)
  28. Nissen RM, "Zebrafish foxi one modulates cellular responses to Fgf signaling required for the integrity of ear and jaw patterning", Development, 130, pp.2543~2554 (2003)
  29. Ober EA, "Vegfc is required for vascular development and endoderm morphogenesis in zebrafish", EMBO Rep, 5, pp.78~84 (2004)
  30. Okada K, "Reiterative expression of pax1 directs pharyngeal pouch segmentation in medaka", Development, 143, pp.1800~1810 (2016)
  31. Parker MW, "Function of members of the neuropilin family as essential pleiotropic cell surface receptors", Biochemistry, 51, pp.9437~9446 (2012)
  32. Piotrowski T, "The endoderm plays an important role in patterning the segmented pharyngeal region in zebrafish (Danio rerio)", Dev Biol, 225, pp.339~356 (2000)
  33. Piotrowski T, "The zebrafish van gogh mutation disrupts tbx1, which is involved in the DiGeorge deletion syndrome in humans", Development, 130, pp.5043~5052 (2003)
  34. Renzi MJ, "A dominant negative receptor for specific secreted semaphorins is generated by deleting an extracellular domain from neuropilin-1", J Neurosci, 19, pp.7870~7880 (1999)
  35. Serini G, "Class 3 semaphorins control vascular morphogenesis by inhibiting integrin function", Nature, 424, pp.391~397 (2003)
  36. Soker S, "Neuropilin-1 is expressed by endothelial and tumor cells as an isoform-specific receptor for vascular endothelial growth factor", Cell, 92, pp.735~745 (1998)
  37. Takashima S, "Targeting of both mouse neuropilin-1 and neuropilin-2 genes severely impairs developmental yolk sac and embryonic angiogenesis", Proc Natl Acad Sci USA, 99, pp.3657~3662 (2002)
  38. Tallafuß A, "Tracing of her5 progeny in zebrafish transgenics reveals the dynamics of midbrain-hindbrain neurogenesis and maintenance", Development, 130, pp.4307~4323 (2003)
  39. Tamagnone L, "Semaphorin signals on the road of endothelial tip cells", Dev Cell, 21, pp.189~190 (2011)
  40. Tran HT, "ARVCF depletion cooperates with Tbx1deficiency in the development of 22q11.2DS-like phenotypes in Xenopus", Dev Dyn, 240, pp.2680~2687 (2011)
  41. Wey JS, "Overexpression of neuropilin-1 promotes constitutive MAPK signalling and chemoresistance in pancreatic cancer cells", Br J Cancer, 93, pp.233~241 (2005)
  42. Xu Y, "Neuropilin-2 mediates VEGF-C–induced lymphatic sprouting together with VEGFR3", J Cell Biol, 188, pp.115~130 (2010)
  43. Yang WJ, "Semaphorin-3C signals through Neuropilin-1 and PlexinD1 receptors to inhibit pathological angiogenesis", EMBO Mol Med, 7, pp.1267~1284 (2015)
  44. Yaniv K, "Live imaging of lymphatic development in the zebrafish", Nat Med, 12, pp.711~716 (2006)
  45. Yuan L, "Abnormal lymphatic vessel development in neuropilin 2 mutant mice", Development, 129, pp.4797~4806 (2002)
  46. Zhang W, "MAPK signal pathways in the regulation of cell proliferation in mammalian cells", Cell Res, 12, pp.9~18 (2002)
  47. Zuniga E, "Gremlin 2 regulates distinct roles of BMP and Endothelin 1 signaling in dorsoventral patterning of the facial skeleton", Development, 138, pp.5147~5156 (2011)

관련 논문AI추천

이 간행물의 다른 논문 (5건)