BMPs Regulate Gene Expression in the Dorsal Neuroectoderm of and Vertebrates by Distinct Mechanisms
The trunk nervous system of both vertebrates and invertebrates develops from three primary rows of neural stem cells whose fate is determined by neural identity genes expressed in an evolutionarily conserved dorso-ventral pattern. Establishment of this pattern requires a shared signaling pathway in both groups of animals. Previous studies suggested that a shared signaling pathway functions in opposite ways in vertebrates and invertebrates, despite the final patterning outcomes having remained the same. Here, we employ bioinformatics, biochemistry, and transgenic animal technology to elucidate the genetic mechanism by which this pathway can engage the same components to generate opposite instructions and yet arrive at similar outcomes in patterning of the nervous system. Our findings highlight how natural selection can act to conserve a particular output pattern despite changes during evolution in the genetic mechanisms underlying the formation of this pattern.
Vyšlo v časopise:
BMPs Regulate Gene Expression in the Dorsal Neuroectoderm of and Vertebrates by Distinct Mechanisms. PLoS Genet 10(9): e32767. doi:10.1371/journal.pgen.1004625
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1004625
Souhrn
The trunk nervous system of both vertebrates and invertebrates develops from three primary rows of neural stem cells whose fate is determined by neural identity genes expressed in an evolutionarily conserved dorso-ventral pattern. Establishment of this pattern requires a shared signaling pathway in both groups of animals. Previous studies suggested that a shared signaling pathway functions in opposite ways in vertebrates and invertebrates, despite the final patterning outcomes having remained the same. Here, we employ bioinformatics, biochemistry, and transgenic animal technology to elucidate the genetic mechanism by which this pathway can engage the same components to generate opposite instructions and yet arrive at similar outcomes in patterning of the nervous system. Our findings highlight how natural selection can act to conserve a particular output pattern despite changes during evolution in the genetic mechanisms underlying the formation of this pattern.
Zdroje
1. BierE (1997) Anti-neural-inhibition: a conserved mechanism for neural induction. Cell 89: 681–684.
2. ArendtD, DenesAS, JékelyG, Tessmar-RaibleK (2008) The evolution of nervous system centralization. Philos Trans R Soc Lond, B, Biol Sci 363: 1523–1528.
3. MizutaniCM, BierE (2008) EvoD/Vo: the origins of BMP signalling in the neuroectoderm. Nat Rev Genet 9(9): 663–77.
4. RustenTE, CanteraR, KafatosFC, BarrioR (2002) The role of TGF beta signaling in the formation of the dorsal nervous system is conserved between Drosophila and chordates. Development 129: 3575–3584.
5. BierE (2011) Evolution of development: diversified dorsoventral patterning. Curr Biol 21: R591–594.
6. BiehsB, FrançoisV, BierE (1996) The Drosophila short gastrulation gene prevents Dpp from autoactivating and suppressing neurogenesis in the neuroectoderm. Genes & Development 10: 2922–2934.
7. MizutaniCM, MeyerN, RoelinkH, BierE (2006) Threshold-dependent BMP-mediated repression: a model for a conserved mechanism that patterns the neuroectoderm. PLoS Biol 4: e313.
8. De RobertisEM, LarrainJ, OelgeschlagerM, WesselyO (2000) The establishment of Spemann's organizer and patterning of the vertebrate embryo. Nat Rev Genet 1: 171–181.
9. LeeKJ, JessellTM (1999) The specification of dorsal cell fates in the vertebrate central nervous system. Annu Rev Neurosci 22: 261–294.
10. HuQ, UenoN, BehringerRR (2004) Restriction of BMP4 activity domains in the developing neural tube of the mouse embryo. EMBO Rep 5: 734–739.
11. Von OhlenT (2000) Convergence of Dorsal, Dpp, and Egfr Signaling Pathways Subdivides the Drosophila Neuroectoderm into Three Dorsal-Ventral Columns. Developmental Biology 224: 362–372.
12. TribuloC, AybarMJ, NguyenVH, MullinsMC, MayorR (2003) Regulation of Msx genes by a BMP gradient is essential for neural crest specification. Development 130: 6441–6452.
13. YuJ-K, MeulemansD, MckeownSJ, Bronner-FraserM (2008) Insights from the amphioxus genome on the origin of vertebrate neural crest. Genome Research 18: 1127–1132.
14. LaprazF, BesnardeauL, LepageT (2009) Patterning of the dorsal-ventral axis in echinoderms: insights into the evolution of the BMP-chordin signaling network. Plos Biol 7: e1000248.
15. SaudemontA, HaillotE, MekpohF, BessodesN, QuirinM, et al. (2010) Ancestral regulatory circuits governing ectoderm patterning downstream of Nodal and BMP2/4 revealed by gene regulatory network analysis in an echinoderm. PLoS Genet 6: e1001259.
16. RossS, HillCS (2008) How the Smads regulate transcription. Int J Biochem Cell Biol 40: 383–408.
17. PyrowolakisG, HartmannB, MullerB, BaslerK, AffolterM (2004) A simple molecular complex mediates widespread BMP-induced repression during Drosophila development. Dev Cell 7: 229–240.
18. GaoS, SteffenJ, LaughonA (2005) Dpp-responsive silencers are bound by a trimeric Mad-Medea complex. J Biol Chem 280: 36158–36164.
19. CrockerJ, ErivesA (2013) A Schnurri/Mad/Medea complex attenuates the dorsal-twist gradient readout at vnd. Dev Biol 378: 64–72.
20. GarciaM, StathopoulosA (2011) Lateral gene expression in Drosophila early embryos is supported by grainyhead-mediated activation and tiers of dorsally-localized repression. PLoS ONE 6: e29172.
21. DaiH (2000) The Zinc Finger Protein Schnurri Acts as a Smad Partner in Mediating the Transcriptional Response to Decapentaplegic. Developmental Biology 227: 373–387.
22. MartyT, MullerB, BaslerK, AffolterM (2000) Schnurri mediates Dpp-dependent repression of brinker transcription. Nat Cell Biol 2: 745–749.
23. MüllerB, HartmannB, PyrowolakisG, AffolterM, BaslerK (2003) Conversion of an extracellular Dpp/BMP morphogen gradient into an inverse transcriptional gradient. Cell 113: 221–233.
24. WeissA, CharbonnierE, EllertsdóttirE, TsirigosA, WolfC, et al. (2010) A conserved activation element in BMP signaling during Drosophila development. Nat Struct Mol Biol 17: 69–76.
25. Von OhlenT, MosesC, PoulsonW (2009) Ind represses msh expression in the intermediate column of the Drosophila neuroectoderm, through direct interaction with upstream regulatory DNA. Dev Dyn 238: 2735–2744.
26. LiXY, MacArthurS, BourgonR, NixD, PollardDA, et al. (2008) Transcription factors bind thousands of active and inactive regions in the Drosophila blastoderm. PLoS Biol 6: e27.
27. MacArthurS, LiXY, LiJ, BrownJB, ChuHC, et al. (2009) Developmental roles of 21 Drosophila transcription factors are determined by quantitative differences in binding to an overlapping set of thousands of genomic regions. Genome Biol 10: R80.
28. VenkenKJT, HeY, HoskinsRA, BellenHJ (2006) P[acman]: a BAC transgenic platform for targeted insertion of large DNA fragments in D. melanogaster. Science 314: 1747–1751.
29. StathopoulosA, LevineM (2005) Localized repressors delineate the neurogenic ectoderm in the early Drosophila embryo. Dev Biol 280: 482–493.
30. FisherS, GriceEA, VintonRM, BesslingSL, UrasakiA, et al. (2006) Evaluating the biological relevance of putative enhancers using Tol2 transposon-mediated transgenesis in zebrafish. Nat Protoc 1: 1297–1305.
31. PhillipsBT, KwonHJ, MeltonC, HoughtalingP, FritzA, et al. (2006) Zebrafish msxB, msxC and msxE function together to refine the neural-nonneural border and regulate cranial placodes and neural crest development. Dev Biol 294: 376–390.
32. AdayAW, ZhuLJ, LakshmananA, WangJ, LawsonND (2011) Identification of cis regulatory features in the embryonic zebrafish genome through large-scale profiling of H3K4me1 and H3K4me3 binding sites. Dev Biol 357: 450–462.
33. FisherS, GriceEA, VintonRM, BesslingSL, McCallionAS (2006) Conservation of RET regulatory function from human to zebrafish without sequence similarity. Science 312: 276–279.
34. KagueE, BesslingSL, LeeJ, HuG, Passos-BuenoMR, et al. (2010) Functionally conserved cis-regulatory elements of COL18A1 identified through zebrafish transgenesis. Dev Biol 337: 496–505.
35. JaźwińskaA, RushlowC, RothS (1999) The role of brinker in mediating the graded response to Dpp in early Drosophila embryos. Development 126: 3323–3334.
36. PyrowolakisG, HartmannB, MüllerB, BaslerK, AffolterM (2004) A simple molecular complex mediates widespread BMP-induced repression during Drosophila development. Dev Cell 7: 229–240.
37. YaoL-C, BlitzIL, PeifferDA, PhinS, WangY, et al. (2006) Schnurri transcription factors from Drosophila and vertebrates can mediate Bmp signaling through a phylogenetically conserved mechanism. Development 133: 4025–4034.
38. SatijaR, BradleyRK (2012) The TAGteam motif facilitates binding of 21 sequence-specific transcription factors in the Drosophila embryo. Genome Research 22: 656–665.
39. ArnostiDN, BaroloS, LevineM, SmallS (1996) The eve stripe 2 enhancer employs multiple modes of transcriptional synergy. Development 122: 205–214.
40. DenesAS, JekelyG, SteinmetzPR, RaibleF, SnymanH, et al. (2007) Molecular architecture of annelid nerve cord supports common origin of nervous system centralization in bilateria. Cell 129: 277–288.
41. HaywardDC, SamuelG, PontynenPC, CatmullJ, SaintR, et al. (2002) Localized expression of a dpp/BMP2/4 ortholog in a coral embryo. Proc Natl Acad Sci U S A 99: 8106–8111.
42. SamuelG, MillerD, SaintR (2001) Conservation of a DPP/BMP signaling pathway in the nonbilateral cnidarian Acropora millepora. Evol Dev 3: 241–250.
43. Reber-MullerS, Streitwolf-EngelR, YanzeN, SchmidV, StierwaldM, et al. (2006) BMP2/4 and BMP5–8 in jellyfish development and transdifferentiation. Int J Dev Biol 50: 377–384.
44. RentzschF, AntonR, SainaM, HammerschmidtM, HolsteinTW, 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.
45. FinnertyJR, PangK, BurtonP, PaulsonD, MartindaleMQ (2004) Origins of bilateral symmetry: Hox and dpp expression in a sea anemone. Science 304: 1335–1337.
46. Valentine JW (2004) On The Origin of Phyla. Chicago: University of Chicago Press. 614 p.
47. LoweCJ, TerasakiM, WuM, FreemanRMJr, RunftL, et al. (2006) Dorsoventral patterning in hemichordates: insights into early chordate evolution. PLoS Biol 4: e291.
48. FurutaY, PistonDW, HoganBL (1997) Bone morphogenetic proteins (BMPs) as regulators of dorsal forebrain development. Development 124: 2203–2212.
49. GoldenJA, BracilovicA, McFaddenKA, BeesleyJS, RubensteinJL, et al. (1999) Ectopic bone morphogenetic proteins 5 and 4 in the chicken forebrain lead to cyclopia and holoprosencephaly. Proc Natl Acad Sci U S A 96: 2439–2444.
50. HartleyKO, HardcastleZ, FridayRV, AmayaE, PapalopuluN (2001) Transgenic Xenopus embryos reveal that anterior neural development requires continued suppression of BMP signaling after gastrulation. Dev Biol 238: 168–184.
51. LiemKFJr, JessellTM, BriscoeJ (2000) Regulation of the neural patterning activity of sonic hedgehog by secreted BMP inhibitors expressed by notochord and somites. Development 127: 4855–4866.
52. PieraniA, Brenner-MortonS, ChiangC, JessellTM (1999) A sonic hedgehog-independent, retinoid-activated pathway of neurogenesis in the ventral spinal cord. Cell 97: 903–915.
53. Reber-MüllerS, Streitwolf-EngelR, YanzeN, SchmidV, StierwaldM, et al. (2006) BMP2/4 and BMP5–8 in jellyfish development and transdifferentiation. Int J Dev Biol 50: 377–384.
54. TakahashiH, KamiyaA, IshiguroA, SuzukiAC, SaitouN, et al. (2008) Conservation and diversification of Msx protein in metazoan evolution. Mol Biol Evol 25: 69–82.
55. RebeizM, PosakonyJW (2004) GenePalette: a universal software tool for genome sequence visualization and analysis. Dev Biol 271: 431–438.
56. HanssonMD, RzeznickaK, RosenbäckM, HanssonM, SirijovskiN (2008) PCR-mediated deletion of plasmid DNA. Anal Biochem 375: 373–375.
57. ChocronS, VerhoevenMC, RentzschF, HammerschmidtM, BakkersJ (2007) Zebrafish Bmp4 regulates left-right asymmetry at two distinct developmental time points. Dev Biol 305: 577–588.
58. HashiguchiM, MullinsMC (2013) Anteroposterior and dorsoventral patterning are coordinated by an identical patterning clock. Development 140: 1970–1980.
59. KosmanD, MizutaniC, LemonsD, CoxG, McGinnisW, et al. (2004) Multiplex detection of RNA expression in Drosophila embryos. Science 305: 846.
60. O'Neill JW, Bier E (1994) Double-label in situ hybridization using biotin and digoxigenin-tagged RNA probes. Biotechniques 17: : 870, 874–875.
61. BlanchetteM, LabourierE, GreenRE, BrennerSE, RioDC (2004) Genome-wide analysis reveals an unexpected function for the Drosophila splicing factor U2AF50 in the nuclear export of intronless mRNAs. Mol Cell 14: 775–786.
62. HouzelsteinD, Auda-BoucherG, CheraudY, RouaudT, BlancI, et al. (1999) The homeobox gene Msx1 is expressed in a subset of somites, and in muscle progenitor cells migrating into the forelimb. Development 126: 2689–2701.
63. AjuriaL, NievaC, WinklerC, KuoD, SamperN, et al. (2011) Capicua DNA-binding sites are general response elements for RTK signaling in Drosophila. Development 138: 915–924.
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Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
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