Evolution of the TGF-β signaling pathway and its potential role in the ctenophore, mnemiopsis leidyi

PLoS ONE

Volumn 6, Issue 9, 2011, Pages

  Pang, Kevin ^a   Ryan, Joseph F ^b   Baxevanis, Andreas D ^b   Martindale, Mark Q ^a  

^a UNIVERSITY OF HAWAII   (United States)

^b NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 [4 (1,3 BENZODIOXOL 5 YL) 5 (2 PYRIDINYL) 1H IMIDAZOL 2 YL]BENZAMIDE; MESSENGER RNA; 1,3 DIOXOLANE DERIVATIVE; 4 (5 BENZO(1,3)DIOXOL 5 YL 4 PYRIDIN 2 YL 1H IMIDAZOL 2 YL)BENZAMIDE; 4-(5-BENZO(1,3)DIOXOL-5-YL-4-PYRIDIN-2-YL-1H-IMIDAZOL-2-YL)BENZAMIDE; BENZAMIDE DERIVATIVE; SMAD PROTEIN; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR;

AMINO ACID SEQUENCE; AMPHIMEDON; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CTENOPHORA; EMBRYO; EMBRYO AXIS; EMBRYO DEVELOPMENT; GENE; GENE EXPRESSION REGULATION; GENE FUNCTION; GENETIC CODE; GENOME ANALYSIS; IN SITU HYBRIDIZATION; MNEMIOPSIS LEIDYI; MOLECULAR EVOLUTION; MORPHOGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; RECEPTOR GENE; SIGNAL TRANSDUCTION; SMAD1S GENE; SMAD2 GENE; SMAD4 GENE; SMAD6 GENE; SPECIES COMPARISON; SPONGE (PORIFERA); TRANSFORMING GROWTH FACTOR BETA GENE; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1 GENE; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 2 GENE; TRANSFORMING GROWTH FACTOR BETA RECEPTOR GENE; TRICHOPLAX; ANIMAL; ANIMAL EMBRYO; BAYES THEOREM; CLASSIFICATION; DRUG ANTAGONISM; DRUG EFFECT; GENE EXPRESSION PROFILING; GENETICS; METABOLISM; MOLECULAR GENETICS; PHYLOGENY; PRENATAL DEVELOPMENT; SEQUENCE HOMOLOGY;

AMPHIMEDON; ANIMALIA; BILATERIA; CNIDARIA; CTENOPHORA (COELENTERATES); METAZOA; MNEMIOPSIS; MNEMIOPSIS LEIDYI; TRICHOPLAX;

AMINO ACID SEQUENCE; ANIMALS; BAYES THEOREM; BENZAMIDES; CTENOPHORA; DIOXOLES; EMBRYO, NONMAMMALIAN; EVOLUTION, MOLECULAR; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IN SITU HYBRIDIZATION; MOLECULAR SEQUENCE DATA; PHYLOGENY; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION; SMAD PROTEINS; TRANSFORMING GROWTH FACTOR BETA;

EID: 80052529162     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0024152     Document Type: Article

References (53)

1. Derynck R, Jarrett JA, Chen EY, Eaton DH, Bell JR, et al. (1985) Human transforming growth factor-beta complementary DNA sequence and expression in normal and transformed cells. Nature 316: 701-705.
2. Kingsley DM, (1995) The TGF-β superfamily: new members, new receptors, and new genetic tests of function in different organisms. Genes Dev 8: 133-146.
3. Massague J, (1998) TGF-β signal transduction. Annu Rev Biochem 67: 753-791.
4. Massague J, Blain SW, Lo RS, (2000) TGFB signaling in growth control, cancer, and heritable disorders. Cell 103: 295-309.
5. Herpin A, Lelong C, Favrel P, (2004) Transforming growth factor-β-related proteins: an ancestral and widespread superfamily of cytokines in metazoans. Dev Comp Immunol 28: 461-485.
6. De Robertis EM, Sasai Y, (1996) A common plan for dorsoventral patterning in Bilateria. Nature 380: 37-40.
7. De Robertis EM, Kuroda H, (2004) Dorsal-ventral patterning and neural induction in Xenopus embryos. Annu Rev Cell Dev Biol 20: 285-308.
8. Massague J, Chen YG, (2000) Controlling TGF-β signaling. Genes Dev 14: 627-644.
9. Dubois CM, Laprise MH, Blanchette F, Gentry LE, Leduc R, (1995) Processing of transforming growth factor β1 precursor by human furin convertase. J Biol Chem 270: 10618-10624.
10. Attisano L, Lee-Hoeflich ST, (2000) The Smads. Genome Biol 2: reviews3010.1-3010.8.
11. Newfeld SJ, Wisotzkey RG, (2006) Molecular evolution of Smad proteins. In: Helden G, ten Dijke P, editors. Smad Signal Transduction Netherlands Springer pp. 15-35.
12. Tsukazaki T, Chiang TA, Davidson AF, Attisano L, Wrana JL, (1998) SARA, a FYVE domain protein recruits Smad2 to the TGF-β receptor. Cell 95: 779-791.
13. Derynck R, Zhang YE, (2003) Smad-dependent and Smad-independent pathways in TGF-β family signaling. Nature 425: 577-584.
14. Balemans W, Van Hul W, (2002) Extracellular regulation of BMP signaling in vertebrates: a cocktail of modulators. Dev Biol 250: 231-250.
15. Marques G, Musacchio M, Shimell MJ, Wunnenberg-Stapleton K, Cho KW, et al. (1997) Production of a DPP activity gradient in the early Drosophila embryo through the opposing actions of the SOG and TLD proteins. Cell 91: 417-426.
16. Kessler E, Takahara K, Biniaminov L, Brusel M, Greenspan DS, (1996) Bone morphogenetic protein-1: the type I procollagen C-proteinase. Science 5247: 360-362.
17. von Marschall Z, Fisher LW, (2010) Decorin is processed by three isoforms of bone morphogenetic protein-1 (BMP1). Biochem Biophys Res Commun 391: 1374-1378.
18. Chen YG, Liu F, Massague J, (1997) Mechanism of TGFβ receptor inhibition by FKBP12. EMBO J 16: 3866-3876.
19. Onichtchouk D, Chen YG, Dosch R, Gawantka V, Delius H, et al. (1999) Silencing of TGF-β signaling by the pseudoreceptor BAMBI. Nature 401: 480-485.
20. Lonn P, Moren A, Raja E, Dahl M, Moustakas A, (2009) Regulating the stability of TGFβ receptors and Smads. Cell Res 19: 21-35.
21. Zhu H, Kavsak P, Abdollah S, Wrana JL, Thomsen GH, (1999) A SMAD ubiquitin ligase targets the BMP pathway and affects embryonic pattern formation. Nature 400: 687-693.
22. Liu X, Sun Y, Weinberg RA, Lodish HF, (2001) Ski/Sno and TGF-β signaling. Cytokine Growth Factor Rev 12: 1-8.
23. Huminiecki L, Goldovsky L, Freilich S, Moustakas A, Ouzounis C, et al. (2009) Emergence, development and diversification of the TGF-β signaling pathway within the animal kingdom. BMC Evol Biol 9: 28.
24. Richards GS, Degnan BM, (2009) The dawn of developmental signaling in the Metazoa. Cold Spring Har Symp Quant Biol 74: 81-90.
25. Srivastava M, Simakov O, Chapman J, Fahey B, Gauthier ME, et al. (2010) The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 466: 720-726.
26. Hayward DC, Samuel G, Pontynen PC, Catmull J, Saint R, et al. (2002) Localized expression of a dpp/BMP2/4 ortholog in a coral embryo. Proc Natl Acad Sci USA 99: 8106-8111.
27. Finnerty JR, Pang K, Burton P, Paulson D, Martindale MQ, (2004) Origins of bilateral symmetry: Hox and Dpp expression in a sea anemone. Science 304: 1335-1337.
28. Reinhardt B, Broun M, Blitz IL, Bode HR, (2004) HyBMP5-8b, a BMP5-8 orthologue, acts during axial patterning and tentacle formation in hydra. Dev Biol 267: 43-59.
29. Matus DQ, Pang K, Marlow H, Dunn CW, Thomsen GH, et al. (2006) Molecular evidence for deep evolutionary roots of bilaterality in animal development. Proc Natl Acad Sci USA 103: 11195-11200.
30. Matus DQ, Thomsen GH, Martindale MQ, (2006) Dorso/ventral genes are asymmetrically expressed and involved in germ-layer demarcation during cnidarian gastrulation. Curr Biol 16: 499-505.
31. Rentzsch F, Anton R, Saina M, Hammerschmidt M, Holstein TW, et al. (2006) Asymmetric expression of the BMP antagonists chordin and gremlin in the sea anemone Nematostella vectensis: implications for the evolution of axial patterning. Dev Biol 296: 375-387.
32. Saina M, Genikhovic G, Renfer E, Technau U, (2009) BMPs and chordin regulate patterning of the directive axis in a sea anemone. Proc Natl Acad Sci USA 106: 18592-18597.
33. Saina M, Technau U, (2009) Characterization of myostatin/gdf8/11 in the starlet sea anemone Nematostella vectensis. J Exp Zool B Mol Dev Evol 312: 780-788.
34. Adamska M, Degnan SM, Green KM, Adamski M, Craigie A, et al. (2007) Wnt and TGF-beta expression in the sponge Amphimedon queenslandica and the origin of metazoan embryonic patterning. PLoS One 2: e1031.
35. Letunic I, Doerks T, Bork P, (2008) SMART 6: recent updates and new developments. Nucleic Acids Res 37: D229-D232.
36. Runyan CE, Schnaper HW, Poncelet A-C, (2005) The role of internalization in transforming growth factor-β1 induced Smad2 association with Smad anchor for receptor activation (SARA) and Smad2-dependent signaling in human mesangial cells. J Biol Chem 9: 8300-8308.
37. Wotton D, Knoefpler PS, Laherty CD, Eisenman RN, Massague J, (2001) The Smad transcriptional corepressor TGIF recruits mSin3. Cell Growth Diff 12: 457-463.
38. Inman GJ, Nicolas FJ, Callahan JF, Harling JD, Gaster LM, et al. (2002) SB-431542 is a potent and specific inhibitor of transforming growth factor-β superfamily type I activin receptor-like kinase (ALK) receptors ALK4, ALK5, and ALK7. Molecular Pharmacology 62: 65-74.
39. Freeman G, (1976) The role of cleavage in the localization of developmental potential in the ctenophore Mnemiopsis leidyi. Dev Biol 49: 143-177.
40. Freeman G, (1977) The establishment of the oral-aboral axis in the ctenophore embryo. J Embryol Exp Morph 42: 237-260.
41. Zhang YE, (2009) Non-Smad pathways in TGF-β signaling. Cell Res 19: 128-139.
42. Descargues P, Sil AK, Sano Y, Korchynskyi O, Han G, et al. (2008) IKKalpha is a critical coregulator of a Smad4-independent TGFβ-Smad2/3 signaling pathway that controls keratinocyte differentiation. Proc Natl Acad Sci USA 105: 2487-2492.
43. He W, Dorn DC, Erdjument-Bromage H, Tempst P, Moore MAS, et al. (2006) Hematopoiesis controlled by distinct TIF1gamma and Smad4 branches of the TGFβ pathway. Cell 125: 929-941.
44. Wolfman NM, McPherron AC, Pappano WN, Davies MV, Song K, et al. (2003) Activation of latent myostatin by the BMP-1/tolloid family of metalloproteinases. Proc Natl Acad Sci USA 100: 15842-15846.
45. Ge G, Hopkins DR, Ho WB, Greenspan DS, (2005) GDF11 forms a bone morphogenetic protein 1-activated latent complex that can modulate nerve growth factor-induced differentiation of PC12 cells. Mol Cell Biol 25: 5846-5858.
46. Serpe M, O'Connor MB, (2006) The metalloprotease Tolloid-related and its TGF-β-like substrate Dawdle regulate Drosophila motoneuron axon guidance. Development 133: 4969-4979.
47. Yamada A, Martindale MQ, Fukui A, Tochina S, (2010) Highly conserved functions of the Brachyury gene on morphogenetic movements: insights from the early-diverging phylum Ctenophora. Dev Biol 339: 212-222.
48. Latinkic BV, Umbhauer M, Neal KA, Lerchner W, Smith JC, et al. (1997) The Xenopus brachyury promoter is activated by FGF and low concentrations of activin and suppressed by high concentrations of activin and by paired-type homeodomain proteins. Genes Dev 11: 3265-3276.
49. Kispert A, Ortner H, Cooke J, Herrmann BG, (1995) The chick brachyury gene: developmental expression pattern and response to axial induction by localized activin. Dev Biol 168: 406-415.
50. Ryan JF, Pang K, Mullikin JC, Martindale MQ, et al. NISC Comparative Sequencing Program (2010) The homeodomain complement of the ctenophore Mnemiopsis leidyi suggests that Ctenophora and Porifera diverged prior to ParaHoxozoa. Evo Devo 1: 9.
51. Pang K, Ryan JF, Mullikin JC, Baxevanis AD, et al. NISC Comparative Sequencing Program (2010) Genomic insights into Wnt signaling in an early diverging metazoan, the ctenophore Mnemiopsis leidyi. Evo Devo 1: 10.
52. Rohnquist F, Huelsenbeck JP, (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.
53. Pang K, Martindale MQ, (2009) Comb jellies (Ctenophora): a model for basal metazoan evolution and development. In: Crotty DA, Gann A, editors. Emerging Model Organisms, vol. 1 Cold Spring Harbor Cold Spring Harbor Laboratory Press pp. 167-195.