Axis Patterning by BMPs: Cnidarian Network Reveals Evolutionary Constraints

Cell Reports
Grigory GenikhovichUlrich Technau

Abstract

BMP signaling plays a crucial role in the establishment of the dorso-ventral body axis in bilaterally symmetric animals. However, the topologies of the bone morphogenetic protein (BMP) signaling networks vary drastically in different animal groups, raising questions about the evolutionary constraints and evolvability of BMP signaling systems. Using loss-of-function analysis and mathematical modeling, we show that two signaling centers expressing different BMPs and BMP antagonists maintain the secondary axis of the sea anemone Nematostella. We demonstrate that BMP signaling is required for asymmetric Hox gene expression and mesentery formation. Computational analysis reveals that network parameters related to BMP4 and Chordin are constrained both in Nematostella and Xenopus, while those describing the BMP signaling modulators can vary significantly. Notably, only chordin, but not bmp4 expression needs to be spatially restricted for robust signaling gradient formation. Our data provide an explanation of the evolvability of BMP signaling systems in axis formation throughout Eumetazoa.

References

Sep 1, 1994·Nature·D Arendt, K Nübler-Jung
Feb 26, 2003·Proceedings of the National Academy of Sciences of the United States of America·Samuel SidiFrédéric M Rosa
May 8, 2004·Science·John R FinnertyMark Q Martindale
Jun 7, 2005·Developmental Cell·Claudia Mieko MizutaniArthur D Lander
Jul 14, 2006·Proceedings of the National Academy of Sciences of the United States of America·David Q MatusMark Q Martindale
Nov 16, 2006·Journal of Mathematical Biology·Dagmar Iber, Giorgio Gaglia
Feb 5, 2008·Cell·E M De Robertis
Sep 18, 2009·Proceedings. Biological Sciences·Andreas HejnolCasey W Dunn
Oct 17, 2009·Proceedings of the National Academy of Sciences of the United States of America·Michael SainaUlrich Technau
Feb 11, 2010·Current Biology : CB·Lise Zakin, E M De Robertis
Feb 12, 2010·Cold Spring Harbor Protocols·Grigory Genikhovich, Ulrich Technau
Jun 3, 2011·Proceedings of the National Academy of Sciences of the United States of America·Malte PaulsenChristof Niehrs
Jul 26, 2011·Current Biology : CB·Dian-Han Kuo, David A Weisblat
Sep 23, 2011·Current Opinion in Genetics & Development·Jean-Louis PlouhinecEdward M De Robertis
Aug 10, 2013·Current Biology : CB·Edward M De Robertis, Gabriele Colozza

❮ Previous
Next ❯

Citations

Feb 20, 2016·Wiley Interdisciplinary Reviews. Developmental Biology·Michael J LaydenEric Röttinger
Dec 4, 2015·International Journal of Molecular Sciences·Aldine R AmielEric Röttinger
Oct 28, 2015·Developmental Cell·Martin BlumChristof Niehrs
Oct 1, 2015·Marine Genomics·Ulrich Technau, Michaela Schwaiger
Jul 1, 2015·Seminars in Cell & Developmental Biology·Francesca B Tuazon, Mary C Mullins
May 28, 2016·Nature Communications·Yulia KrausGrigory Genikhovich
Jun 17, 2016·Open Biology·Arseniy R MorovKinya Yasui
Jun 20, 2016·Current Opinion in Genetics & Development·Fabian Rentzsch, Ulrich Technau
Jun 21, 2016·Current Opinion in Genetics & Development·Andreas Hejnol, Kevin Pang
Nov 11, 2015·Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences·Iva KelavaUlrich Technau
Dec 21, 2016·Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences·Leslie S Babonis, Mark Q Martindale
Feb 15, 2018·Proceedings of the National Academy of Sciences of the United States of America·Anastasia KirillovaUlrich Technau
Oct 5, 2017·Development·Grigory Genikhovich, Ulrich Technau
Aug 23, 2017·ELife·Joseph ZinskiMary C Mullins
Sep 29, 2018·Science·Detlev Arendt
Apr 2, 2019·Scientific Reports·Yan Huang, David M Umulis
Nov 25, 2016·Wiley Interdisciplinary Reviews. Developmental Biology·Fabian RentzschMichaël Manuel
Aug 16, 2017·Nature Ecology & Evolution·José M Martín-DuránAndreas Hejnol
Nov 7, 2017·Biological Reviews of the Cambridge Philosophical Society·Frances S DunnPhilip C J Donoghue
Mar 13, 2019·Nature Ecology & Evolution·Lucas LeclèreRichard R Copley
Aug 24, 2018·Nature Ecology & Evolution·Claus NielsenDetlev Arendt
Mar 5, 2020·Communicative & Integrative Biology·Chris Fields, Michael Levin
Jun 28, 2017·Proceedings of the National Academy of Sciences of the United States of America·Naveen WijesenaMark Q Martindale
Aug 18, 2017·Development, Growth & Differentiation·Edward M De RobertisGabriele Colozza
Nov 28, 2020·Developmental Dynamics : an Official Publication of the American Association of Anatomists·Lakshmi Surekha KrishnapatiSurendra Ghaskadbi
Nov 12, 2020·ELife·Katherine W RogersPatrick Müller
Apr 3, 2021·Development·Aasakiran MadamanchiDavid M Umulis
Aug 27, 2021·Development·Aasakiran MadamanchiDavid M Umulis

❮ Previous
Next ❯

Methods Mentioned

BETA
gene knockdown
transgenic

Related Concepts

Related Feeds

Aphasia

Aphasia affects the ability to process language, including formulation and comprehension of language and speech, as well as the ability to read or write. Here is the latest research on aphasia.