Literature DB >> 32707057

Optogenetic Rescue of a Patterning Mutant.

Heath E Johnson1, Nareg J V Djabrayan2, Stanislav Y Shvartsman3, Jared E Toettcher4.   

Abstract

Animal embryos are patterned by a handful of highly conserved inductive signals. Yet, in most cases, it is unknown which pattern features (i.e., spatial gradients or temporal dynamics) are required to support normal development. An ideal experiment to address this question would be to "paint" arbitrary synthetic signaling patterns on "blank canvas" embryos to dissect their requirements. Here, we demonstrate exactly this capability by combining optogenetic control of Ras/extracellular signal-related kinase (ERK) signaling with the genetic loss of the receptor tyrosine-kinase-driven terminal signaling patterning in early Drosophila embryos. Blue-light illumination at the embryonic termini for 90 min was sufficient to rescue normal development, generating viable larvae and fertile adults from an otherwise lethal terminal signaling mutant. Optogenetic rescue was possible even using a simple, all-or-none light input that reduced the gradient of Erk activity and eliminated spatiotemporal differences in terminal gap gene expression. Systematically varying illumination parameters further revealed that at least three distinct developmental programs are triggered at different signaling thresholds and that the morphogenetic movements of gastrulation are robust to a 3-fold variation in the posterior pattern width. These results open the door to controlling tissue organization with simple optical stimuli, providing new tools to probe natural developmental processes, create synthetic tissues with defined organization, or directly correct the patterning errors that underlie developmental defects.
Copyright © 2020 Elsevier Inc. All rights reserved.

Entities:  

Keywords:  Drosophila; Erk; MAP kinase; cell fate; embryogenesis; optogenetics; patterning; signal transduction

Year:  2020        PMID: 32707057      PMCID: PMC7730203          DOI: 10.1016/j.cub.2020.06.059

Source DB:  PubMed          Journal:  Curr Biol        ISSN: 0960-9822            Impact factor:   10.834


  61 in total

1.  Capicua DNA-binding sites are general response elements for RTK signaling in Drosophila.

Authors:  Leiore Ajuria; Claudia Nieva; Clint Winkler; Dennis Kuo; Núria Samper; María José Andreu; Aharon Helman; Sergio González-Crespo; Ze'ev Paroush; Albert J Courey; Gerardo Jiménez
Journal:  Development       Date:  2011-01-26       Impact factor: 6.868

Review 2.  The design and logic of terminal patterning in Drosophila.

Authors:  Celia M Smits; Stanislav Y Shvartsman
Journal:  Curr Top Dev Biol       Date:  2020-02-14       Impact factor: 4.897

Review 3.  A quantitative model of developmental RTK signaling.

Authors:  Yogesh Goyal; Trudi Schüpbach; Stanislav Y Shvartsman
Journal:  Dev Biol       Date:  2018-07-17       Impact factor: 3.582

4.  GCL and CUL3 Control the Switch between Cell Lineages by Mediating Localized Degradation of an RTK.

Authors:  Juhee Pae; Ryan M Cinalli; Antonio Marzio; Michele Pagano; Ruth Lehmann
Journal:  Dev Cell       Date:  2017-07-24       Impact factor: 12.270

5.  Control and function of terminal gap gene activity in the posterior pole region of the Drosophila embryo.

Authors:  G Brönner; H Jäckle
Journal:  Mech Dev       Date:  1991-11       Impact factor: 1.882

6.  A protein kinase similar to MAP kinase activator acts downstream of the raf kinase in Drosophila.

Authors:  L Tsuda; Y H Inoue; M A Yoo; M Mizuno; M Hata; Y M Lim; T Adachi-Yamada; H Ryo; Y Masamune; Y Nishida
Journal:  Cell       Date:  1993-02-12       Impact factor: 41.582

Review 7.  Outstanding questions in developmental ERK signaling.

Authors:  Aleena L Patel; Stanislav Y Shvartsman
Journal:  Development       Date:  2018-07-26       Impact factor: 6.868

8.  Regulated expression of nullo is required for the formation of distinct apical and basal adherens junctions in the Drosophila blastoderm.

Authors:  C Hunter; E Wieschaus
Journal:  J Cell Biol       Date:  2000-07-24       Impact factor: 10.539

9.  A scalable pipeline for designing reconfigurable organisms.

Authors:  Sam Kriegman; Douglas Blackiston; Michael Levin; Josh Bongard
Journal:  Proc Natl Acad Sci U S A       Date:  2020-01-13       Impact factor: 11.205

10.  Cancer mutations and targeted drugs can disrupt dynamic signal encoding by the Ras-Erk pathway.

Authors:  L J Bugaj; A J Sabnis; A Mitchell; J E Garbarino; J E Toettcher; T G Bivona; W A Lim
Journal:  Science       Date:  2018-08-31       Impact factor: 47.728

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  9 in total

1.  Temporal integration of inductive cues on the way to gastrulation.

Authors:  Sarah McFann; Sayantan Dutta; Jared E Toettcher; Stanislav Y Shvartsman
Journal:  Proc Natl Acad Sci U S A       Date:  2021-06-08       Impact factor: 11.205

2.  Reverse and Forward Engineering Multicellular Structures with Optogenetics.

Authors:  Thomas R Mumford; Lee Roth; Lukasz J Bugaj
Journal:  Curr Opin Biomed Eng       Date:  2020-10-14

Review 3.  Revealing epithelial morphogenetic mechanisms through live imaging.

Authors:  Payam E Farahani; Celeste M Nelson
Journal:  Curr Opin Genet Dev       Date:  2021-12-01       Impact factor: 5.578

Review 4.  Patterning principles of morphogen gradients.

Authors:  M Fethullah Simsek; Ertuğrul M Özbudak
Journal:  Open Biol       Date:  2022-10-19       Impact factor: 7.124

Review 5.  Novel synthetic biology approaches for developmental systems.

Authors:  Christine Ho; Leonardo Morsut
Journal:  Stem Cell Reports       Date:  2021-05-11       Impact factor: 7.765

6.  Desensitisation of Notch signalling through dynamic adaptation in the nucleus.

Authors:  Ranjith Viswanathan; Jonas Hartmann; Cristina Pallares Cartes; Stefano De Renzis
Journal:  EMBO J       Date:  2021-08-16       Impact factor: 11.598

Review 7.  Synthetic living machines: A new window on life.

Authors:  Mo R Ebrahimkhani; Michael Levin
Journal:  iScience       Date:  2021-05-04

8.  Optogenetic control of the Bicoid morphogen reveals fast and slow modes of gap gene regulation.

Authors:  Anand P Singh; Ping Wu; Sergey Ryabichko; João Raimundo; Michael Swan; Eric Wieschaus; Thomas Gregor; Jared E Toettcher
Journal:  Cell Rep       Date:  2022-03-22       Impact factor: 9.995

Review 9.  Optogenetic approaches for understanding homeostatic and degenerative processes in Drosophila.

Authors:  Wen Kin Lim; Prameet Kaur; Huanyan Huang; Richard Shim Jo; Anupriya Ramamoorthy; Li Fang Ng; Jahnavi Suresh; Fahrisa Islam Maisha; Ajay S Mathuru; Nicholas S Tolwinski
Journal:  Cell Mol Life Sci       Date:  2021-07-07       Impact factor: 9.261

  9 in total

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