ADAM19 Regulates Wnt Signaling and Neural Crest Specification by Stabilizing ADAM13

Overview

Journal Development

Specialty Biology

Date 2018 Mar 16

PMID 29540504

Citations 10

Authors

Jiejing Li

Mark Perfetto

Russell Neuner

Harinath Bahudhanapati

Laura Christian

Ketan Mathavan

Lance C Bridges

Dominique Alfandari

Shuo Wei

Affiliations

Soon will be listed here.

Abstract

During vertebrate gastrulation, canonical Wnt signaling induces the formation of neural plate border (NPB). Wnt is also thought to be required for the subsequent specification of neural crest (NC) lineage at the NPB, but the direct evidence is lacking. We found previously that the disintegrin metalloproteinase ADAM13 is required for Wnt activation and NC induction in Here, we report that knockdown of ADAM13 or its close paralog ADAM19 severely downregulates Wnt activity at the NPB, inhibiting NC specification without affecting earlier NPB formation. Surprisingly, ADAM19 functions nonproteolytically in NC specification by interacting with ADAM13 and inhibiting its proteasomal degradation. Ectopic expression of stabilized ADAM13 mutants that function independently of ADAM19 can induce the NC marker/specifier in the future epidermis via Wnt signaling. These results unveil the essential roles of a novel protease-protease interaction in regulating a distinct wave of Wnt signaling, which directly specifies the NC lineage.

Citing Articles

Diverse mechanisms of DDX3Y suppression by DDX3X.

Xu X, Wei S bioRxiv. 2025; .

PMID: 39975375 PMC: 11839027. DOI: 10.1101/2025.02.08.637260.

Time to go: neural crest cell epithelial-to-mesenchymal transition.

Leathers T, Rogers C Development. 2022; 149(15).

PMID: 35905012 PMC: 9440755. DOI: 10.1242/dev.200712.

Norrie disease protein is essential for cochlear hair cell maturation.

Hayashi Y, Chiang H, Tian C, Indzhykulian A, Edge A Proc Natl Acad Sci U S A. 2021; 118(39).

PMID: 34544869 PMC: 8488680. DOI: 10.1073/pnas.2106369118.

The RNA helicase DDX3 induces neural crest by promoting AKT activity.

Perfetto M, Xu X, Lu C, Shi Y, Yousaf N, Li J Development. 2020; 148(2).

PMID: 33318149 PMC: 7847268. DOI: 10.1242/dev.184341.

The Tudor-domain protein TDRD7, mutated in congenital cataract, controls the heat shock protein HSPB1 (HSP27) and lens fiber cell morphology.

Barnum C, Al Saai S, Patel S, Cheng C, Anand D, Xu X Hum Mol Genet. 2020; 29(12):2076-2097.

PMID: 32420594 PMC: 7390939. DOI: 10.1093/hmg/ddaa096.

References

Milet C, Maczkowiak F, Roche D, Monsoro-Burq A . Pax3 and Zic1 drive induction and differentiation of multipotent, migratory, and functional neural crest in Xenopus embryos. Proc Natl Acad Sci U S A. 2013; 110(14):5528-33. PMC: 3619367. DOI: 10.1073/pnas.1219124110. View

McCusker C, Cousin H, Neuner R, Alfandari D . Extracellular cleavage of cadherin-11 by ADAM metalloproteases is essential for Xenopus cranial neural crest cell migration. Mol Biol Cell. 2008; 20(1):78-89. PMC: 2613130. DOI: 10.1091/mbc.e08-05-0535. View

Abu-Elmagd M, Garcia-Morales C, Wheeler G . Frizzled7 mediates canonical Wnt signaling in neural crest induction. Dev Biol. 2006; 298(1):285-98. DOI: 10.1016/j.ydbio.2006.06.037. View

Abbruzzese G, Gorny A, Kaufmann L, Cousin H, Kleino I, Steinbeisser H . The Wnt receptor Frizzled-4 modulates ADAM13 metalloprotease activity. J Cell Sci. 2015; 128(6):1139-49. PMC: 4359921. DOI: 10.1242/jcs.163063. View

Kunisada T, Tezulka K, Aoki H, Motohashi T . The stemness of neural crest cells and their derivatives. Birth Defects Res C Embryo Today. 2014; 102(3):251-62. DOI: 10.1002/bdrc.21079. View

Gaultier A, Cousin H, Darribere T, Alfandari D . ADAM13 disintegrin and cysteine-rich domains bind to the second heparin-binding domain of fibronectin. J Biol Chem. 2002; 277(26):23336-44. DOI: 10.1074/jbc.M201792200. View

Tran H, Sekkali B, Van Imschoot G, Janssens S, Vleminckx K . Wnt/beta-catenin signaling is involved in the induction and maintenance of primitive hematopoiesis in the vertebrate embryo. Proc Natl Acad Sci U S A. 2010; 107(37):16160-5. PMC: 2941280. DOI: 10.1073/pnas.1007725107. View

Dornier E, Coumailleau F, Ottavi J, Moretti J, Boucheix C, Mauduit P . TspanC8 tetraspanins regulate ADAM10/Kuzbanian trafficking and promote Notch activation in flies and mammals. J Cell Biol. 2012; 199(3):481-96. PMC: 3483123. DOI: 10.1083/jcb.201201133. View

Hong C, Park B, Saint-Jeannet J . Fgf8a induces neural crest indirectly through the activation of Wnt8 in the paraxial mesoderm. Development. 2008; 135(23):3903-10. PMC: 2888028. DOI: 10.1242/dev.026229. View

10.

Wei S, Xu G, Bridges L, Williams P, White J, DeSimone D . ADAM13 induces cranial neural crest by cleaving class B Ephrins and regulating Wnt signaling. Dev Cell. 2010; 19(2):345-52. PMC: 2951023. DOI: 10.1016/j.devcel.2010.07.012. View

11.

Haining E, Yang J, Bailey R, Khan K, Collier R, Tsai S . The TspanC8 subgroup of tetraspanins interacts with A disintegrin and metalloprotease 10 (ADAM10) and regulates its maturation and cell surface expression. J Biol Chem. 2012; 287(47):39753-65. PMC: 3501075. DOI: 10.1074/jbc.M112.416503. View

12.

Monsoro-Burq A, Wang E, Harland R . Msx1 and Pax3 cooperate to mediate FGF8 and WNT signals during Xenopus neural crest induction. Dev Cell. 2005; 8(2):167-78. DOI: 10.1016/j.devcel.2004.12.017. View

13.

Cai H, Kratzschmar J, Alfandari D, Hunnicutt G, Blobel C . Neural crest-specific and general expression of distinct metalloprotease-disintegrins in early Xenopus laevis development. Dev Biol. 1999; 204(2):508-24. DOI: 10.1006/dbio.1998.9017. View

14.

Steventon B, Araya C, Linker C, Kuriyama S, Mayor R . Differential requirements of BMP and Wnt signalling during gastrulation and neurulation define two steps in neural crest induction. Development. 2009; 136(5):771-9. PMC: 2685944. DOI: 10.1242/dev.029017. View

15.

Session A, Uno Y, Kwon T, Chapman J, Toyoda A, Takahashi S . Genome evolution in the allotetraploid frog Xenopus laevis. Nature. 2016; 538(7625):336-343. PMC: 5313049. DOI: 10.1038/nature19840. View

16.

Powell D, Blasky A, Britt S, Artinger K . Riding the crest of the wave: parallels between the neural crest and cancer in epithelial-to-mesenchymal transition and migration. Wiley Interdiscip Rev Syst Biol Med. 2013; 5(4):511-22. PMC: 3739939. DOI: 10.1002/wsbm.1224. View

17.

Reiss K, Saftig P . The "a disintegrin and metalloprotease" (ADAM) family of sheddases: physiological and cellular functions. Semin Cell Dev Biol. 2008; 20(2):126-37. DOI: 10.1016/j.semcdb.2008.11.002. View

18.

Cousin H, Gaultier A, Bleux C, Darribere T, Alfandari D . PACSIN2 is a regulator of the metalloprotease/disintegrin ADAM13. Dev Biol. 2000; 227(1):197-210. DOI: 10.1006/dbio.2000.9871. View

19.

Bronner M, Simoes-Costa M . The Neural Crest Migrating into the Twenty-First Century. Curr Top Dev Biol. 2016; 116:115-34. PMC: 5100668. DOI: 10.1016/bs.ctdb.2015.12.003. View

20.

Sato T, Sasai N, Sasai Y . Neural crest determination by co-activation of Pax3 and Zic1 genes in Xenopus ectoderm. Development. 2005; 132(10):2355-63. DOI: 10.1242/dev.01823. View