Involvement of the MAP Kinase Cascade in Xenopus Mesoderm Induction

Overview

Journal EMBO J

Specialties Biotechnology
Molecular Biology

Date 1995 Jun 1

PMID 7781601

Citations 31

Authors

Y Gotoh

N Masuyama

A Suzuki

N Ueno

E Nishida

Affiliations

Soon will be listed here.

Abstract

Mitogen-activated protein kinase (MAPK) is activated by MAPK kinase (MAPKK) in a variety of signaling pathways. This kinase cascade has been shown to function in cell proliferation and differentiation, but its role in early vertebrate development remains to be investigated. During early vertebrate embryogenesis, the induction and patterning of mesoderm are thought to be determined by signals from intercellular factors such as members of the fibroblast growth factor (FGF) family and members of the transforming growth factor-beta family. Here we show that the microinjection of either mRNA encoding a constitutively active mutant of MAPKK or mRNA encoding a constitutively active form of STE11, a MAPKK kinase, leads to the induction of mesoderm in ectodermal explants from Xenopus embryos. Moreover, the expression of MAPK phosphatase-1 (MKP-1, also called CL100) blocks the growth factor-stimulated mesoderm induction. Furthermore, injection of CL100 mRNA into two-cell stage embryos causes severe defects in gastrulation and posterior development. The effects induced by CL100 can be rescued by co-injection of wild-type MAPK mRNA. Thus, the MAPK cascade may play a crucial role in early vertebrate embryogenesis, especially during mesoderm induction.

Citing Articles

Multiple roles of the mitogen-activated protein kinase kinase/mitogen-activated protein kinase cascade in Xenopus laevis.

Kosako H, Gotoh Y, Nishida E Dev Growth Differ. 2023; 38(6):577-582.

PMID: 37281037 DOI: 10.1046/j.1440-169X.1996.t01-5-00001.x.

Noggin proteins are multifunctional extracellular regulators of cell signaling.

Karunaraj P, Tidswell O, Duncan E, Lovegrove M, Jefferies G, Johnson T Genetics. 2022; 221(1).

PMID: 35357435 PMC: 9071555. DOI: 10.1093/genetics/iyac049.

A YWHAZ Variant Associated With Cardiofaciocutaneous Syndrome Activates the RAF-ERK Pathway.

Popov I, Hiatt S, Whalen S, Keren B, Ruivenkamp C, van Haeringen A Front Physiol. 2019; 10:388.

PMID: 31024343 PMC: 6465419. DOI: 10.3389/fphys.2019.00388.

Novel Reporter for Faithful Monitoring of ERK2 Dynamics in Living Cells and Model Organisms.

Sipieter F, Cappe B, Gonzalez Pisfil M, Spriet C, Bodart J, Cailliau-Maggio K PLoS One. 2015; 10(10):e0140924.

PMID: 26517832 PMC: 4627772. DOI: 10.1371/journal.pone.0140924.

Stochastic specification of primordial germ cells from mesoderm precursors in axolotl embryos.

Chatfield J, OReilly M, Bachvarova R, Ferjentsik Z, Redwood C, Walmsley M Development. 2014; 141(12):2429-40.

PMID: 24917499 PMC: 4050694. DOI: 10.1242/dev.105346.

References

Wu J, Dent P, Jelinek T, Wolfman A, Weber M, Sturgill T . Inhibition of the EGF-activated MAP kinase signaling pathway by adenosine 3',5'-monophosphate. Science. 1993; 262(5136):1065-9. DOI: 10.1126/science.7694366. View

Cook S, McCormick F . Inhibition by cAMP of Ras-dependent activation of Raf. Science. 1993; 262(5136):1069-72. DOI: 10.1126/science.7694367. View

Shibuya E, Ruderman J . Mos induces the in vitro activation of mitogen-activated protein kinases in lysates of frog oocytes and mammalian somatic cells. Mol Biol Cell. 1993; 4(8):781-90. PMC: 300992. DOI: 10.1091/mbc.4.8.781. View

Boguski M, McCormick F . Proteins regulating Ras and its relatives. Nature. 1993; 366(6456):643-54. DOI: 10.1038/366643a0. View

Graves L, Northrop J, Potts B, KREBS E, Kimelman D . Fibroblast growth factor, but not activin, is a potent activator of mitogen-activated protein kinase in Xenopus explants. Proc Natl Acad Sci U S A. 1994; 91(5):1662-6. PMC: 43223. DOI: 10.1073/pnas.91.5.1662. View

Zheng C, Guan K . Activation of MEK family kinases requires phosphorylation of two conserved Ser/Thr residues. EMBO J. 1994; 13(5):1123-31. PMC: 394921. DOI: 10.1002/j.1460-2075.1994.tb06361.x. View

Cornell R, Kimelman D . Activin-mediated mesoderm induction requires FGF. Development. 1994; 120(2):453-62. DOI: 10.1242/dev.120.2.453. View

Labonne C, Whitman M . Mesoderm induction by activin requires FGF-mediated intracellular signals. Development. 1994; 120(2):463-72. DOI: 10.1242/dev.120.2.463. View

Alessi D, Saito Y, Campbell D, Cohen P, Sithanandam G, Rapp U . Identification of the sites in MAP kinase kinase-1 phosphorylated by p74raf-1. EMBO J. 1994; 13(7):1610-9. PMC: 394991. DOI: 10.1002/j.1460-2075.1994.tb06424.x. View

10.

Neiman A, Herskowitz I . Reconstitution of a yeast protein kinase cascade in vitro: activation of the yeast MEK homologue STE7 by STE11. Proc Natl Acad Sci U S A. 1994; 91(8):3398-402. PMC: 43584. DOI: 10.1073/pnas.91.8.3398. View

11.

Porras A, Muszynski K, Rapp U, Santos E . Dissociation between activation of Raf-1 kinase and the 42-kDa mitogen-activated protein kinase/90-kDa S6 kinase (MAPK/RSK) cascade in the insulin/Ras pathway of adipocytic differentiation of 3T3 L1 cells. J Biol Chem. 1994; 269(17):12741-8. View

12.

Dickson B, Hafen E . Genetics of signal transduction in invertebrates. Curr Opin Genet Dev. 1994; 4(1):64-70. DOI: 10.1016/0959-437x(94)90092-2. View

13.

Alessi D, Smythe C, Keyse S . The human CL100 gene encodes a Tyr/Thr-protein phosphatase which potently and specifically inactivates MAP kinase and suppresses its activation by oncogenic ras in Xenopus oocyte extracts. Oncogene. 1993; 8(7):2015-20. View

14.

Kolch W, Heidecker G, Kochs G, Hummel R, Vahidi H, Mischak H . Protein kinase C alpha activates RAF-1 by direct phosphorylation. Nature. 1993; 364(6434):249-52. DOI: 10.1038/364249a0. View

15.

Davis R . The mitogen-activated protein kinase signal transduction pathway. J Biol Chem. 1993; 268(20):14553-6. View

16.

Blenis J . Signal transduction via the MAP kinases: proceed at your own RSK. Proc Natl Acad Sci U S A. 1993; 90(13):5889-92. PMC: 46831. DOI: 10.1073/pnas.90.13.5889. View

17.

Zhang X, Settleman J, Kyriakis J, Elledge S, Marshall M, Bruder J . Normal and oncogenic p21ras proteins bind to the amino-terminal regulatory domain of c-Raf-1. Nature. 1993; 364(6435):308-13. DOI: 10.1038/364308a0. View

18.

Warne P, Viciana P, Downward J . Direct interaction of Ras and the amino-terminal region of Raf-1 in vitro. Nature. 1993; 364(6435):352-5. DOI: 10.1038/364352a0. View

19.

Vojtek A, Hollenberg S, Cooper J . Mammalian Ras interacts directly with the serine/threonine kinase Raf. Cell. 1993; 74(1):205-14. DOI: 10.1016/0092-8674(93)90307-c. View

20.

Krieg P, Melton D . Functional messenger RNAs are produced by SP6 in vitro transcription of cloned cDNAs. Nucleic Acids Res. 1984; 12(18):7057-70. PMC: 320142. DOI: 10.1093/nar/12.18.7057. View