TAK1 promotes BMP4/Smad1 signaling via inhibition of erk MAPK: A new link in the FGF/BMP regulatory network

Differentiation

Volumn 83, Issue 4, 2012, Pages 210-219

  Liu, Chen ^a,b   Goswami, Mousumi ^a,c   Talley, Julia ^a   Chesser Martinez, Patricia L ^a   Lou, Chih Hong ^a,d   Sater, Amy K ^a  

^a University of Houston   (United States)

^b UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^c Houston Community College   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

BMP; Embryo; Erk MAP kinase; Smad1; TAK1; Xenopus

Indexed keywords

BONE MORPHOGENETIC PROTEIN 4; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE KINASE; MITOGEN ACTIVATED PROTEIN KINASE PHOSPHATASE 1; SMAD1 PROTEIN; SYNAPTOPHYSIN; TRANSFORMING GROWTH FACTOR BETA ACTIVATED KINASE 1;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; ECTODERM; EMBRYO; ENDODERM; ENZYME INHIBITION; GASTRULA; GENE; GENE OVEREXPRESSION; MESODERM; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; UPREGULATION; XENOPUS; XVENT1 GENE; XVENT2 GENE;

ANIMALS; BONE MORPHOGENETIC PROTEIN 4; DOWN-REGULATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FIBROBLAST GROWTH FACTORS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MAP KINASE KINASE KINASES; REAL-TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SMAD1 PROTEIN; XENOPUS; XENOPUS PROTEINS;

VERTEBRATA;

EID: 84862787759     PISSN: 03014681     EISSN: 14320436     Source Type: Journal    
DOI: 10.1016/j.diff.2011.12.007     Document Type: Article

References (56)

1. Abramoff M.D., Magalhaes P.J., Ram S.J. Image processing with Image J. Biophotonics International 2004, 11:36-42.
2. Afouda B.A., Ciau-Uitz A., Patient R. GATA4, 5 and 6 mediate TGF-beta maintenance of endodermal gene expression in Xenopus embryos. Development 2005, 132:763-774.
3. Aubin J., Davy A., Soriano P. In vivo convergence of BMP and MAPK signaling pathways: impact of differential Smad1 phosphorylation on development and homeostasis. Genes & Development 2004, 18:1482-1494.
4. Boswell B.A., Overbeek P.A., Musil L.S. Essential role of BMPs in FGF-induced secondary lens fiber differentiation. Developmental Biology 2008, 324:202-212.
5. Cheng B., Song J., Zou Y., Wang Q., Lei Y., Zhu C., Hu C. Responses of vascular smooth muscle cells to estrogen are dependent on balance between ERK and p38 MAPK pathway activities. International Journal of Cardiology 2009, 134:356-365.
6. Cohn M.J., Izpisúa-Belmonte J.C., Abud H., Heath J.K., Tickle C. Fibroblast growth factors induce additional limb development from the flank of chick embryos. Cell 1995, 80:739-746.
7. de Almeida I., Rolo A., Batut J., Hill C., Stern C.D., Linker C. Unexpected activities of Smad7 in Xenopus mesodermal and neural induction. Mechanisms of Development 2008, 125:421-431.
8. Delaune E., Lemaire P., Kodjabachian L. Neural induction in Xenopus requires early FGF signalling in addition to BMP inhibition. Development 2005, 132:299-310.
9. De Robertis E.M., Kuroda H. Dorsal-ventral patterning and neural induction in Xenopus embryos. Annual Review of Cell and Developmental Biology 2004, 20:285-308.
10. Esterberg R., Fritz A. dlx3b/4b are required for the formation of the preplacodal region and otic placode through local modulation of BMP activity. Developmental Biology 2009, 325:189-199.
11. Fainsod A., Steinbeisser H., De Robertis E.M. On the function of BMP-4 in patterning the marginal zone of the Xenopus embryo. EMBO Journal 1994, 13:5015-5025.
12. Fuentealba L.C., Eivers E., Ikeda A., Hurtado C., Kuroda H., Pera E.M., De Robertis E.M. Integrating patterning signals: Wnt/GSK3 regulates the duration of the BMP/Smad1 signal. Cell 2007, 131:980-993.
13. Gabay L., Seger R., Shilo B.Z. MAP kinase in situ activation atlas during Drosophila embryogenesis. Development 1997, 124:3535-3541.
14. Glavic A., Maris Honoré S., Gloria Feijóo C., Bastidas F., Allende M.L., Mayor R. Role of BMP signaling and the homeoprotein Iroquois in the specification of the cranial placodal field. Developmental Biology 2004, 272:89-103.
15. Goswami M., Uzgare A.R., Sater A.K. Regulation of MAP kinase by the BMP-4/TAK1 pathway in Xenopus ectoderm. Developmental Biology 2001, 236:259-270.
16. Grethe S., Pörn-Ares M.I. p38 MAPK regulates phosphorylation of Bad via PP2A-dependent suppression of the MEK1/2-ERK1/2 survival pathway in TNF-alpha induced endothelial apoptosis. Cellular Signalling 2006, 18:531-540.
17. Hoffmann A., Preobrazhenska O., Wodarczyk C., Medler Y., Winkel A., Shahab S., Huylebroeck D., Gross G., Verschueren K. Transforming growth factor-beta-activated kinase-1 (TAK1), a MAP3K, interacts with Smad proteins and interferes with osteogenesis in murine mesenchymal progenitors. Journal of Biological Chemistry 2005, 280:27271-27283.
18. Khokha M.K., Yeh J., Grammer T.C., Harland R.M. Depletion of three BMP antagonists from Spemann's organizer leads to a catastrophic loss of dorsal structures. Developmental Cell 2005, 8:401-411.
19. Knockaert M., Sapkota G., Alarcón C., Massagué J., Brivanlou A.H. Unique players in the BMP pathway: small C-terminal domain phosphatases dephosphorylate Smad1 to attenuate BMP signaling. Proceedings of the National Academy of Sciences USA 2006, 103:11940-11945.
20. Kretzschmar M., Doody J., Massagué J. Opposing BMP and EGF signalling pathways converge on the TGF-beta family mediator Smad1. Nature 1997, 389:618-622.
21. Kudoh T., Concha M.L., Houart C., Dawid I.B., Wilson S.W. Combinatorial Fgf and Bmp signalling patterns the gastrula ectoderm into prospective neural and epidermal domains. Development 2004, 131:3581-3592.
22. Kwon H.J., Bhat N., Sweet E.M., Cornell R.A., Riley B.B. Identification of early requirements for preplacodal ectoderm and sensory organ development. PLoS Genetics 2010, 6:e1001133.
23. Lamb T.M., Harland R.M. Fibroblast growth factor is a direct neural inducer, which combined with noggin generates anterior-posterior neural pattern. Development 1995, 121:3627-3636.
24. Liu Q., Hofmann P.A. Protein phosphatase 2A-mediated cross-talk between p38 MAPK and ERK in apoptosis of cardiac myocytes. American Journal of Physiology Heart and Circulatory Physiology 2004, 286:H2204-H2212.
25. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔcT method. Methods 2001, 25:402-408.
26. Londin E.R., Niemiec J., Sirotkin H.I. Chordin, FGF signaling, and mesodermal factors cooperate in zebrafish neural induction. Developmental Biology 2005, 279:1-19.
27. Maier E., von Hofsten J., Nord H., Fernandes M., Paek H., Hébert J.M., Gunhaga L. Opposing Fgf and Bmp activities regulate the specification of olfactory sensory and respiratory epithelial cell fates. Development 2010, 137:1601-1611.
28. Marchal L., Luxardi G., Thomé V., Kodjabachian L. BMP inhibition initiates neural induction via FGF signaling and Zic genes. Proceedings of the National Academy of Sciences USA 2009, 106:17437-17442.
29. Miura S., Davis S., Klingensmith J., Mishina Y. BMP signaling in the epiblast is required for proper recruitment of the prospective paraxial mesoderm and development of the somites. Development 2006, 133:3767-3775.
30. Mitchell T.S., Sheets M.D. The FGFR pathway is required for the trunk-inducing functions of Spemann's organizer. Developmental Biology 2001, 237:295-305.
31. Ohkawara B., Shirakabe K., Hyodo-Miura J., Matsuo R., Ueno N., Matsumoto K., Shibuya H. Role of the TAK1-NLK-STAT3 pathway in TGF-beta-mediated mesoderm induction. Genes & Development 2004, 18:381-386.
32. Patil S.S., Alexander T.B., Uzman J.A., Lou C.H., Gohil H., Sater A.K. The novel gene ashwin functions in Xenopus cell survival and anteroposterior patterning. Developmental Dynamics 2006, 235:1895-1907.
33. Pera E.M., Ikeda A., Eivers E., De Robertis E.M. Integration of IGF, FGF, and anti-BMP signals via Smad1 phosphorylation in neural induction. Genes & Development 2003, 17:3023-3028.
34. Rastegar S., Friedle H., Frommer G., Knöchel W. Transcriptional regulation of Xvent homeobox genes. Mechanisms of Development 1999, 81:139-149.
35. Richard-Parpaillon L., Héligon C., Chesnel F., Boujard D., Philpott A. The IGF pathway regulates head formation by inhibiting Wnt signaling in Xenopus. Developmental Biology 2002, 244:407-417.
36. Rogers C.D., Moody S.A., Casey E.S. Neural induction and factors that stabilize a neural fate. Birth Defects Research Part C: Embryo Today 2009, 87:249-262.
37. Sander V., Reversade B., De Robertis E.M. The opposing homeobox genes Goosecoid and Vent1/2 self-regulate Xenopus patterning. EMBO Journal 2007, 26:2955-2965.
38. Sapkota G., Alarcón C., Spagnoli F.M., Brivanlou A.H., Massagué J. Balancing BMP signaling through integrated inputs into the Smad1 linker. Molecular Cell 2007, 25:441-454.
39. Sater A.K., El-Hodiri H.M., Goswami M., Alexander T.B., Al-Sheikh O., Etkin L.D., Uzman J.A. Evidence for antagonism of BMP-4 signals by MAP kinase during Xenopus axis determination and neural specification. Differentiation 2003, 71:434-444.
40. Sheng N., Xie Z., Wang C., Bai G., Zhang K., Zhu Q., Song J., Guillemot F., Chen Y.G., Lin A., Jing N. Retinoic acid regulates bone morphogenic protein signal duration by promoting the degradation of phosphorylated Smad1. Proceedings of the National Academy of Sciences USA 2010, 107:18886-18891.
41. Shibuya H., Iwata H., Masuyama N., Gotoh Y., Yamaguchi K., Irie K., Matsumoto K., Nishida E., Ueno N. Role of TAK1 and Table1 in BMP signaling in early Xenopus development. EMBO Journal 1998, 17:1019-1028.
42. Shin D., Shin C.H., Tucker J., Ober E.A., Rentzsch F., Poss K.D., Hammerschmidt M., Mullins M.C., Stainier D.Y. Bmp and Fgf signaling are essential for liver specification in zebrafish. Development 2007, 134:2041-2050.
43. Stavridis M.P., Lunn J.S., Collins B.J., Storey K.G. A discrete period of FGF-induced Erk1/2 signalling is required for vertebrate neural specification. Development 2007, 134:2889-2894.
44. Streit A., Berliner A.J., Papanayotou C., Sirulnik A., Stern C.D. Initiation of neural induction by FGF signalling before gastrulation. Nature 2000, 406:74-78.
45. Tecarro E., Bui T., Lisi M., Sater A., Uzman A. A simple model of two interacting signaling pathways in embryonic Xenopus laevis. Discrete and Continuous Dynamical Systems 2009, (Suppl.):753-760.
46. Uzgare A.R., Uzman J.A., El-Hodiri H.M., Sater A.K. Mitogen-activated protein kinase and neural specification in Xenopus. Proceedings of the National Academy of Sciences USA 1998, 95:14833-14838.
47. Uzman J.A., Patil S., Uzgare A.R., Sater A.K. The role of intracellular alkalinization in the establishment of anterior neural fate in Xenopus. Developmental Biology 1998, 193:10-20.
48. van Wijk B., van den Berg G., Abu-Issa R., Barnett P., van der Velden S., Schmidt M., Ruijter J.M., Kirby M.L., Moorman A.F., van den Hoff M.J. Epicardium and myocardium separate from a common precursor pool by crosstalk between bone morphogenetic protein- and fibroblast growth factor-signaling pathways. Circulation Research 2009, 105:431-441.
49. Virshup D.M., Shenolikar S. From promiscuity to precision: protein phosphatases get a makeover. Molecular Cell 2009, 33:537-545.
50. Vonica A., Brivanlou A.H. An obligatory caravanserai stop on the silk road to neural induction: inhibition of BMP/GDF signaling. Seminars in Cell and Developmental Biology 2006, 17:117-132.
51. Walsh D.W., Godson C., Brazil D.P., Martin F. Extracellular BMP-antagonist regulation in development and disease: tied up in knots. Trends in Cell Biology 2010, 20:244-256.
52. Westermarck J., Li S.P., Kallunki T., Han J., Kähäri V.M. p38 mitogen-activated protein kinase-dependent activation of protein phosphatases 1 and 2A inhibits MEK1 and MEK2 activity and collagenase 1 (MMP-1) gene expression. Molecular and Cellular Biology 2001, 21:2373-2383.
53. Wilson S.I., Graziano E., Harland R., Jessell T.M., Edlund T. An early requirement for FGF signalling in the acquisition of neural cell fate in the chick embryo. Current Biology 2000, 10:421-429.
54. Yokota C., Kofron M., Zuck M., Houston D.W., Isaacs H., Asashima M., Wylie C.C., Heasman J. A novel role for a nodal-related protein; Xnr3 regulates convergent extension movements via the FGF receptor. Development 2003, 130:2199-2212.
55. Zhao Z., Rivkees S.A. Programmed cell death in the developing heart: regulation by BMP4 and FGF2. Developmental Dynamics 2000, 217:388-400.
56. Zohn I.E., Brivanlou A.H. Expression cloning of Xenopus Os4, an evolutionarily conserved gene, which induces mesoderm and dorsal axis. Developmental Biology 2001, 239:118-131.