The ubiquitin ligase Nedd4 regulates craniofacial development by promoting cranial neural crest cell survival and stem-cell like properties

Developmental Biology

Volumn 383, Issue 2, 2013, Pages 186-200

  Wiszniak, Sophie ^a   Kabbara, Samuela ^a   Lumb, Rachael ^a   Scherer, Michaela ^a   Secker, Genevieve ^a   Harvey, Natasha ^a,b,c   Kumar, Sharad ^a,b,c   Schwarz, Quenten ^a,b,c  

^a CENTRE FOR CANCER BIOLOGY   (Australia)

^b UNIVERSITY OF ADELAIDE   (Australia)

^c UNIVERSITY OF SOUTH AUSTRALIA   (Australia)

Author keywords

Ectomesenchyme; Nedd4; Neural crest cell; Neuroglial; Stem cell maintenance; Ubiquitin ligase

Indexed keywords

PROTEIN FOXD3; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SOX10; TRANSCRIPTION FACTOR SOX9; UBIQUITIN PROTEIN LIGASE NEDD4; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BONE MALFORMATION; CELL SURVIVAL; CONTROLLED STUDY; CRANIOFACIAL DEVELOPMENT; CRANIOFACIAL MALFORMATION; EMBRYO; ENZYME ACTIVITY; ENZYME REGULATION; MOUSE; NEURAL CREST CELL; NEURAL STEM CELL; NEURAL TUBE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TRIGEMINUS GANGLION;

MAMMALIA;

EID: 84885840960     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2013.09.024     Document Type: Article

References (56)

1. Akiyama H., Chaboissier M.C., Martin J.F., Schedl A., de Crombrugghe B. The transcription factor Sox9 has essential roles in successive steps of the chondrocyte differentiation pathway and is required for expression of Sox5 and Sox6. Genes and Development 2002, 16:2813-2828.
2. Baroffio A., Dupin E., Le Douarin N.M. Common precursors for neural and mesectodermal derivatives in the cephalic neural crest. Development 1991, 112:301-305.
3. Begbie J., Graham A. Integration between the epibranchial placodes and the hindbrain. Science 2001, 294:595-598.
4. Bi W., Huang W., Whitworth D.J., Deng J.M., Zhang Z., Behringer R.R., de Crombrugghe B. Haploinsufficiency of Sox9 results in defective cartilage primordia and premature skeletal mineralization. Proceedings of the National Academy of Sciences of the United States of America 2001, 98:6698-6703.
5. Bronner-Fraser M., Fraser S.E. Cell lineage analysis reveals multipotency of some avian neural crest cells. Nature 1988, 335:161-164.
6. Bronner-Fraser M., Sieber-Blum M., Cohen A.M. Clonal analysis of the avian neural crest: migration and maturation of mixed neural crest clones injected into host chicken embryos. Journal of Comparative Neurology 1980, 193:423-434.
7. Cao X.R., Lill N.L., Boase N., Shi P.P., Croucher D.R., Shan H., Qu J., Sweezer E.M., Place T., Kirby P.A., Daly R.J., Kumar S., Yang B. Nedd4 controls animal growth by regulating IGF-1 signalling. Sci Signal. 2008, 1:ra5.
8. Cheung M., Briscoe J. Neural crest development is regulated by the transcription factor Sox9. Development 2003, 130:5681-5693.
9. Cheung M., Chaboissier M.C., Mynett A., Hirst E., Schedl A., Briscoe J. The transcriptional control of trunk neural crest induction, survival, and delamination. Developmental Cell 2005, 8:179-192.
10. Christie K.J., Martinez J.A., Zochodne D.W. Disruption of E3 ligase NEDD4 in peripheral neurons interrupts axon outgrowth: Linkage to PTEN. Molecular and Cellular Neuroscience 2011, 50:179-192.
11. Cordero D.R., Brugmann S., Chu Y., Bajpai R., Jame M., Helms J.A. Cranial neural crest cells on the move: their roles in craniofacial development. American Journal of Medical Genetics A 2010, 155A:270-279.
12. Crane J.F., Trainor P.A. Neural crest stem and progenitor cells. Annual Review of Cell and Developmental Biology 2006, 22:267-286.
13. Delfino-Machin M., Chipperfield T.R., Rodrigues F.S., Kelsh R.N. The proliferating field of neural crest stem cells. Developmental Dynamics 2007, 236:3242-3254.
14. Drinjakovic J., Jung H., Campbell D.S., Strochlic L., Dwivedy A., Holt C.E. E3 ligase Nedd4 promotes axon branching by downregulating PTEN. Neuron 2010, 65:341-357.
15. Duan W.R., Garner D.S., Williams S.D., Funckes-Shippy C.L., Spath I.S., Blomme E.A. Comparison of immunohistochemistry for activated caspase-3 and cleaved cytokeratin 18 with the TUNEL method for quantification of apoptosis in histological sections of PC-3 subcutaneous xenografts. Journal of Pathology 2003, 199:221-228.
16. Fouladkou F., Lu C., Jiang C., Zhou L., She Y., Walls J.R., Kawabe H., Brose N., Henkelman R.M., Huang A., Bruneau B.G., Rotin D. The ubiquitin ligase Nedd4-1 is required for heart development and is a suppressor of thrombospondin-1. Journal of Biological Chemistry 2010, 285:6770-6780.
17. Helms J.A., Schneider R.A. Cranial skeletal biology. Nature 2003, 423:326-331.
18. Herbarth B., Pingault V., Bondurand N., Kuhlbrodt K., Hermans-Borgmeyer I., Puliti A., Lemort N., Goossens M., Wegner M. Mutation of the Sry-related Sox10 gene in Dominant megacolon, a mouse model for human Hirschsprung disease. Proceedings of the National Academy of Sciences of the United States of America 1998, 95:5161-5165.
19. Ito K., Sieber-Blum M. In vitro clonal analysis of quail cardiac neural crest development. Developmental Biology 1991, 148:95-106.
20. John N., Cinelli P., Wegner M., Sommer L. Transforming growth factor beta-mediated Sox10 suppression controls mesenchymal progenitor generation in neural crest stem cells. Stem Cells 2011, 29:689-699.
21. Kalinichenko S.V., Itoh K., Korobko E.V., Sokol S.Y., Buchman V.L., Korobko I.V. Identification of Nedd4 E3 ubiquitin ligase as a binding partner and regulator of MAK-V protein kinase. PLoS ONE 2012, 7:e39505.
22. Kapur R.P. Early death of neural crest cells is responsible for total enteric aganglionosis in Sox10(Dom)/Sox10(Dom) mouse embryos. Pediatric and Developmental Pathology 1999, 2:559-569.
23. Kawabe H., Neeb A., Dimova K., Young S.M., Takeda M., Katsurabayashi S., Mitkovski M., Malakhova O.A., Zhang D.E., Umikawa M., Kariya K., Goebbels S., Nave K.A., Rosenmund C., Jahn O., Rhee J., Brose N. Regulation of Rap2A by the ubiquitin ligase Nedd4-1 controls neurite development. Neuron 2010, 65:358-372.
24. Kerscher O., Felberbaum R., Hochstrasser M. Modification of proteins by ubiquitin and ubiquitin-like proteins. Annual Review of Cell Biology 2006, 22:159-180.
25. Kim B.G., Lee J.H., Yasuda J., Ryoo H.M., Cho J.Y. Phospho-Smad1 modulation by nedd4 E3 ligase in BMP/TGF-beta signalling. Journal of Bone and Mineral Research 2011, 26:1411-1424.
26. Kim J., Lo L., Dormand E., Anderson D.J. SOX10 maintains multipotency and inhibits neuronal differentiation of neural crest stem cells. Neuron 2003, 38:17-31.
27. Kleber M., Lee H.Y., Wurdak H., Buchstaller J., Riccomagno M.M., Ittner L.M., Suter U., Epstein D.J., Sommer L. Neural crest stem cell maintenance by combinatorial Wnt and BMP signalling. Journal of Cell Biology 2005, 169:309-320.
28. Kontges G., Lumsden A. Rhombencephalic neural crest segmentation is preserved throughout craniofacial ontogeny. Development 1996, 122:3229-3242.
29. Kumar S., Harvey K.F., Kinoshita M., Copeland N.G., Noda M., Jenkins N.A. cDNA cloning, expression analysis, and mapping of the mouse Nedd4 gene. Genomics 1997, 40:435-443.
30. Labosky P.A., Kaestner K.H. The winged helix transcription factor Hfh2 is expressed in neural crest and spinal cord during mouse development. Mechanisms of Development 1998, 76:185-190.
31. Le Douarin N.M., Creuzet S., Couly G., Dupin E. Neural crest cell plasticity and its limits. Development 2004, 131:4637-4650.
32. Lu X., Liu S., Kornberg T.B. The C-terminal tail of the Hedgehog receptor Patched regulates both localisation and turnover. Genes and Development 2006, 20:2539-2551.
33. Mori-Akiyama Y., Akiyama H., Rowitch D.H., de Crombrugghe B. Sox9 is required for determination of the chondrogenic cell lineage in the cranial neural crest. Proceedings of the National Academy of Sciences of the United States of America 2003, 100:9360-9365.
34. Mundell N.A., Labosky P.A. Neural crest stem cell multipotency requires Foxd3 to maintain neural potential and repress mesenchymal fates. Development 2011, 138:641-652.
35. Murphy M., Bernard O., Reid K., Bartlett P.F. Cell lines derived from mouse neural crest are representative of cells at various stages of differentiation. Journal of Neurobiology 1991, 22:522-535.
36. Nagy A., Gertsenstein M., Vintersten K., Behringer R. Manipulating the Mouse Embryo. A Laboratory Manual 2003, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
37. Onuma T.A., Ding Y., Abraham E., Zohar Y., Ando H., Duan C. Regulation of temporal and spatial organization of newborn GnRH neurons by IGF signalling in zebrafish. Journal of Neuroscience 2011, 31:11814-11824.
38. Osumi-Yamashita N., Ninomiya Y., Doi H., Eto K. The contribution of both forebrain and midbrain crest cells to the mesenchyme in the frontonasal mass of mouse embryos. Developmental Biology 1994, 164:409-419.
39. Persaud A., Alberts P., Amsen E.M., Xiong X., Wasmuth J., Saadon Z., Fladd C., Parkinson J., Rotin D. Comparison of substrate specificity of the ubiquitin ligases Nedd4 and Nedd4-2 using proteome arrays. Molecular Systems Biology 2009, 5:333.
40. Rotin D., Kumar S. Physiological functions of the HECT family of ubiquitin ligases. Nature Reviews Molecular Cell Biology 2009, 10:398-409.
41. Santagati F., Rijli F.M. Cranial neural crest and the building of the vertebrate head. Nature Reviews Neuroscience 2003, 4:806-818.
42. Schofer C., Frei K., Weipoltshammer K., Wachtler F. The apical ectodermal ridge, fibroblast growth factors (FGF-2 and FGF-4) and insulin-like growth factor I (IGF-I) control the migration of epidermal melanoblasts in chicken wing buds. Anatomy and Embryology (Berlin) 2001, 203:137-146.
43. Schwarz Q., Gu C., Fujisawa H., Sabelko K., Gertsenstein M., Nagy A., Taniguchi M., Kolodkin A.L., Ginty D.D., Shima D.T., Ruhrberg C. Vascular endothelial growth factor controls neuronal migration and cooperates with Sema3A to pattern distinct compartments of the facial nerve. Genes and Development 2004, 18:2822-2834.
44. Scott C.E., Wynn S.L., Sesay A., Cruz C., Cheung M., Gomez Gaviro M.V., Booth S., Gao B., Cheah K.S., Lovell-Badge R., Briscoe J. SOX9 induces and maintains neural stem cells. Nature Neuroscience 2011, 13:1181-1189.
45. Sieber-Blum M., Cohen A.M. Clonal analysis of quail neural crest cells: they are pluripotent and differentiate in vitro in the absence of noncrest cells. Developmental Biology 1980, 80:96-106.
46. Smith-Thomas L.C., Kent C., Mayer R.J., Scotting P.J. Protein ubiquitination and neuronal differentiation in chick embryos. Developmental Brain Research 1994, 81:171-177.
47. Sonnenberg-Riethmacher E., Miehe M., Stolt C.C., Goerich D.E., Wegner M., Riethmacher D. Development and degeneration of dorsal root ganglia in the absence of the HMG-domain transcription factor Sox10. Mechanisms of Development 2001, 109:253-265.
48. Southard-Smith E.M., Kos L., Pavan W.J. Sox10 mutation disrupts neural crest development in Dom Hirschsprung mouse model. Nature Genetics 1998, 18:60-64.
49. Stemple D.L., Anderson D.J. Isolation of a stem cell for neurons and glia from the mammalian neural crest. Cell 1992, 71:973-985.
50. Steventon B., Carmona-Fontaine C., Mayor R. Genetic network during neural crest induction: from cell specification to cell survival. Seminars in Cell and Developmental Biology 2005, 16:647-654.
51. Teng L., Mundell N.A., Frist A.Y., Wang Q., Labosky P.A. Requirement for Foxd3 in the maintenance of neural crest progenitors. Development 2008, 135:1615-1624.
52. Trentin A., Glavieux-Pardanaud C., Le Douarin N.M., Dupin E. Self-renewal capacity is a widespread property of various types of neural crest precursor cells. Proceedings of the National Academy of Sciences of the United States of America 2004, 101:4495-4500.
53. Weston A.D., Underhill T.M. Analysis of Nedd4 expression during skeletal development in the mouse limb. Mechanisms of Development 2000, 94:247-250.
54. Wiszniak, S., Lumb, R., Kabbara, S., Scherer, M., Schwarz, Q., 2013. Li-gazing at the crest: Modulation of the neural crest by the ubiquitin pathway. International Journal of Biochemistry and Cell Biology.
55. Zeng F., Xu J., Harris R.C. Nedd4 mediates ErbB4 JM-a/CYT-1 ICD ubiquitination and degradation in MDCK II cells. FASEB Journal 2009, 23:1935-1945.
56. Zou W., Chen X., Shim J.H., Huang Z., Brady N., Hu D., Drapp R., Sigrist K., Glimcher L.H., Jones D. The E3 ubiquitin ligase Wwp2 regulates craniofacial development through mono-ubiquitylation of Goosecoid. Nature Cell Biology 2010, 13:59-65.