Running the gauntlet: an overview of the modalities of travel employed by the putative morphogen Nodal

Current Opinion in Genetics and Development

Volumn 19, Issue 4, 2009, Pages 302-307

  Constam, Daniel B ^a  

^a EPFL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

MORPHOGEN; PROTEIN NODAL;

CELL FATE; DIFFUSION; ENDOSOME; GERM LAYER; NONHUMAN; PRIORITY JOURNAL; PROTEIN STABILITY; PROTEIN TARGETING; PROTEIN TRANSPORT; REVIEW; SIGNAL TRANSDUCTION; STEM CELL; VERTEBRATE;

ANIMALS; BODY PATTERNING; EMBRYO, NONMAMMALIAN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; LEFT-RIGHT DETERMINATION FACTORS; NODAL PROTEIN; NODAL SIGNALING LIGANDS; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

VERTEBRATA;

EID: 68949164494     PISSN: 0959437X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.gde.2009.06.006     Document Type: Review

References (47)

1. Shen M.M. Nodal signaling: developmental roles and regulation. Development 134 (2007) 1023-1034
2. Arnold S.J., and Robertson E.J. Making a commitment: cell lineage allocation and axis patterning in the early mouse embryo. Nat Rev Mol Cell Biol 10 (2009) 91-103
3. Shiratori H., and Hamada H. The left-right axis in the mouse: from origin to morphology. Development 133 (2006) 2095-2104
4. Constam D.B. Riding shotgun: a dual role for the epidermal growth factor-Cripto/FRL-1/Cryptic protein Cripto in Nodal trafficking. Traffic 10 (2009) 783-791
5. Schmierer B., and Hill C.S. TGFbeta-SMAD signal transduction: molecular specificity and functional flexibility. Nat Rev Mol Cell Biol 8 (2007) 970-982
6. Lander A.D. Morpheus unbound: reimagining the morphogen gradient. Cell 128 (2007) 245-256
7. Varlet I., Collignon J., and Robertson E.J. Nodal expression in the primitive endoderm is required for specification of the anterior axis during mouse gastrulation. Development 124 (1997) 1033-1044
8. Chu J., Ding J., Jeays-Ward K., Price S.M., Placzek M., and Shen M.M. Non-cell-autonomous role for Cripto in axial midline formation during vertebrate embryogenesis. Development 132 (2005) 5539-5551
9. Minchiotti G., Manco G., Parisi S., Lago C.T., Rosa F., and Persico M.G. Structure-function analysis of the EGF-CFC family member Cripto identifies residues essential for nodal signalling. Development 128 (2001) 4501-4510
10. Sakuma R., Ohnishi Yi Y., Meno C., Fujii H., Juan H., Takeuchi J., Ogura T., Li E., Miyazono K., and Hamada H. Inhibition of Nodal signalling by Lefty mediated through interaction with common receptors and efficient diffusion. Genes Cells 7 (2002) 401-412
11. Watanabe K., Hamada S., Bianco C., Mancino M., Nagaoka T., Gonzales M., Bailly V., Strizzi L., and Salomon D.S. Requirement of glycosylphosphatidylinositol anchor of cripto-1 for 'trans' activity as a nodal co-receptor. J Biol Chem 282 (2007) 35772-35786. Deletion of the GPI signal sequence, or GPI cleavage by phospholipase C blocks the ability of Cripto to stimulate Nodal signaling in tissue culture cells. A mutant Cripto in which the GPI anchor is replaced by a transmembrane domain is also severely inhibited except in cells that overexpress the Nodal signaling receptor ALK4.
12. Vincent S.D., Dunn N.R., Hayashi S., Norris D.P., and Robertson E.J. Cell fate decisions within the mouse organizer are governed by graded Nodal signals. Genes Dev 17 (2003) 1646-1662
13. Chen Y., and Schier A.F. The zebrafish Nodal signal Squint functions as a morphogen. Nature 411 (2001) 607-610
14. Williams P.H., Hagemann A., Gonzalez-Gaitan M., and Smith J.C. Visualizing long-range movement of the morphogen Xnr2 in the Xenopus embryo. Curr Biol 14 (2004) 1916-1923
15. Mesnard D., Guzman-Ayala M., and Constam D.B. Nodal specifies embryonic visceral endoderm and sustains pluripotent cells in the epiblast before overt axial patterning. Development 133 (2006) 2497-2505
16. Camus A., Perea-Gomez A., Moreau A., and Collignon J. Absence of Nodal signaling promotes precocious neural differentiation in the mouse embryo. Dev Biol 295 (2006) 743-755
17. Brennan J., Lu C.C., Norris D.P., Rodriguez T.A., Beddington R.S., and Robertson E.J. Nodal signalling in the epiblast patterns the early mouse embryo. Nature 411 (2001) 965-969
18. Brennan J., Norris D.P., and Robertson E.J. Nodal activity in the node governs left-right asymmetry. Genes Dev 16 (2002) 2339-2344
19. Nakamura T., Mine N., Nakaguchi E., Mochizuki A., Yamamoto M., Yashiro K., Meno C., and Hamada H. Generation of robust left-right asymmetry in the mouse embryo requires a self-enhancement and lateral-inhibition system. Dev Cell 11 (2006) 495-504
20. Ohi Y., and Wright C.V. Anteriorward shifting of asymmetric Xnr1 expression and contralateral communication in left-right specification in Xenopus. Dev Biol 301 (2007) 447-463
21. Oki S., Hashimoto R., Okui Y., Shen M.M., Mekada E., Otani H., Saijoh Y., and Hamada H. Sulfated glycosaminoglycans are necessary for Nodal signal transmission from the node to the left lateral plate in the mouse embryo. Development 134 (2007) 3893-3904. Although Cryptic normally is expressed in both the node and lateral plate, a Cryptic transgene targeted to the latter tissue is sufficient to rescue Nodal signalling from the node to lateral plate mesoderm in Cryptic mutants.
22. Tanaka C., Sakuma R., Nakamura T., Hamada H., and Saijoh Y. Long-range action of Nodal requires interaction with GDF1. Genes Dev 21 (2007) 3272-3282. Shows that Nodal signaling in Gdf1-/- embryos during LR axis formation can be rescued by a transgene that expresses Gdf1 in the node, but not by a transgene that restores expression of Gdf1 in the lateral plate mesoderm. In addition, GDF1 bound Nodal in coimmunoprecipitation assays and potentiated its activity when the two proteins were coexpressed in Xenopus oocytes, possibly through heterodimerization.
23. Yan Y.T., Gritsman K., Ding J., Burdine R.D., Corrales J.D., Price S.M., Talbot W.S., Schier A.F., and Shen M.M. Conserved requirement for EGF-CFC genes in vertebrate left-right axis formation. Genes Dev 13 (1999) 2527-2537
24. Rankin C.T., Bunton T., Lawler A.M., and Lee S.J. Regulation of left-right patterning in mice by growth/differentiation factor-1. Nat Genet 24 (2000) 262-265
25. Andersson O., Bertolino P., and Ibanez C.F. Distinct and cooperative roles of mammalian Vg1 homologs GDF1 and GDF3 during early embryonic development. Dev Biol 311 (2007) 500-511. Consistent with a role for Gdf1,3/Nodal heterodimers, this study shows that GDF1 and GDF3 are barely active when expressed alone, but greatly enhance the activity of Nodal.
26. Shimmi O., Umulis D., Othmer H., and O'Connor M.B. Facilitated transport of a Dpp/Scw heterodimer by Sog/Tsg leads to robust patterning of the Drosophila blastoderm embryo. Cell 120 (2005) 873-886
27. Kramer K.L., and Yost H.J. Ectodermal syndecan-2 mediates left-right axis formation in migrating mesoderm as a cell-nonautonomous Vg1 cofactor. Dev Cell 2 (2002) 115-124
28. Eldar A., Rosin D., Shilo B.Z., and Barkai N. Self-enhanced ligand degradation underlies robustness of morphogen gradients. Dev Cell 5 (2003) 635-646
29. Kicheva A., Pantazis P., Bollenbach T., Kalaidzidis Y., Bittig T., Julicher F., and Gonzalez-Gaitan M. Kinetics of morphogen gradient formation. Science 315 (2007) 521-525. Imaging and fluorescence recovery after photobleaching (FRAP) analysis of GFP-fusion proteins revealed the shape and kinetic parameters of Dpp and Wg morphogen gradients in the Drosophila wing imaginal disc.
30. Le Good J.A., Joubin K., Giraldez A.J., Ben-Haim N., Beck S., Chen Y., Schier A.F., and Constam D.B. Nodal stability determines signaling range. Curr Biol 15 (2005) 1-20
31. Tian J., Andree B., Jones C.M., and Sampath K. The pro-domain of the zebrafish Nodal-related protein Cyclops regulates its signaling activities. Development 135 (2008) 2649-2658
32. Beck S., Le Good J.A., Guzman M., Haim N.B., Roy K., Beermann F., and Constam D.B. Extraembryonic proteases regulate Nodal signalling during gastrulation. Nat Cell Biol 4 (2002) 981-985
33. BenHaim N., Lu C., Pescatore L., Mesnard D., Bischofberger M., Naef F., Robertson E.J., Guzman M., and Constam D.B. The Nodal precursor acting via activin receptors induces mesoderm by maintaining a source of its convertases and BMP4. Dev Cell 11 (2006) 1-11
34. Blanchet M.-H., Le Good J.A., Mesnard D., Oorschot V., Baflast S., Minchiotti G., Klumperman J., and Constam D.B. Cripto recruits Furin and PACE4 and controls Nodal trafficking during proteolytic maturation. EMBO J 27 (2008) 2580-2591. Coimmunoprecipitation assays revealed binding of Cripto to the Nodal precursor and its proprotein convertases Furin and Pace4. In addition, a Cripto-interacting region in the Nodal prosegment was found to be necessary to efficiently activate Nodal signaling, indicating that Nodal probably matures in a complex with Cripto.
35. Entchev E.V., Schwabedissen A., and Gonzalez-Gaitan M. Gradient formation of the TGF-beta homolog Dpp. Cell 103 (2000) 981-991
36. Blanchet M.-H., Le Good J.A., Oorschot V., Baflast S., Minchiotti G., Klumperman J., and Constam D.B. Cripto localizes Nodal at the limiting membrane of early endosomes. Sci Signal 1 (2008) ra13
37. van der Goot F.G., and Gruenberg J. Intra-endosomal membrane traffic. Trends Cell Biol 16 (2006) 514-521
38. Trajkovic K., Hsu C., Chiantia S., Rajendran L., Wenzel D., Wieland F., Schwille P., Brugger B., and Simons M. Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science 319 (2008) 1244-1247. This study shows a role for ceramide in the budding of intralumenal vesicles that are released as exosomes when the limiting membrane of multivesicular endosomes backfuses with the plasma membrane.
39. Gonzalez-Gaitan M. Endocytic trafficking during Drosophila development. Mech Dev 120 (2003) 1265-1282
40. Jullien J., and Gurdon J. Morphogen gradient interpretation by a regulated trafficking step during ligand-receptor transduction. Genes Dev 19 (2005) 2682-2694
41. Wolpert L. Positional information and the spatial pattern of cellular differentiation. J Theor Biol 25 (1969) 1-47
42. Kerszberg M., and Wolpert L. Specifying positional information in the embryo: looking beyond morphogens. Cell 130 (2007) 205-209
43. Jaeger J., Irons D., and Monk N. Regulative feedback in pattern formation: towards a general relativistic theory of positional information. Development 135 (2008) 3175-3183
44. Hagos E.G., and Dougan S.T. Time-dependent patterning of the mesoderm and endoderm by Nodal signals in zebrafish. BMC Dev Biol 7 (2007) 22. Shows that the timing and choice of cell fates in gastrulating zebrafish embryos depend on the level and duration of Nodal signalling.
45. Meinhardt H. Space-dependent cell determination under the control of morphogen gradient. J Theor Biol 74 (1978) 307-321
46. Bokel C., Schwabedissen A., Entchev E., Renaud O., and Gonzalez-Gaitan M. Sara endosomes and the maintenance of Dpp signaling levels across mitosis. Science 314 (2006) 1135-1139
47. Marques S., Borges A.C., Silva A.C., Freitas S., Cordenonsi M., and Belo J.A. The activity of the Nodal antagonist Cerl-2 in the mouse node is required for correct L/R body axis. Genes Dev 18 (2004) 2342-2347