Reciprocal signaling by Wnt and Notch specifies a muscle precursor in the C. elegans embryo

Scott M. Robertson, Jessica Medina, Marieke Oldenbroek, Rueyling Lin

Research output: Contribution to journalArticle

Abstract

The MS blastomere produces one-third of the body wall muscles (BWMs) in the C. elegans embryo. MS-derived BWMs require two distinct cell-cell interactions, the first inhibitory and the second, two cell cycles later, required to overcome this inhibition. The inductive interaction is not required if the inhibitory signal is absent. Although the Notch receptor GLP-1 was implicated in both interactions, the molecular nature of the two signals was unknown. We now show that zygotically expressed MOM-2 (Wnt) is responsible for both interactions. Both the inhibitory and the activating interactions require precise spatiotemporal expression of zygotic MOM-2, which is dependent upon two distinct Notch signals. In a Notch mutant defective only in the inductive interaction, MS-derived BWMs can be restored by preventing zygotic MOM-2 expression, which removes the inhibitory signal. Our results suggest that the inhibitory interaction ensures the differential lineage specification of MS and its sister blastomere, whereas the inductive interaction promotes the expression of muscle-specifying genes by modulating TCF and β-catenin levels. These results highlight the complexity of cell fate specification by cell-cell interactions in a rapidly dividing embryo.

Original languageEnglish (US)
Pages (from-to)419-429
Number of pages11
JournalDevelopment (Cambridge)
Volume144
Issue number3
DOIs
StatePublished - Feb 1 2017

Fingerprint

Embryonic Structures
Blastomeres
Muscles
Cell Communication
Notch Receptors
Catenins
Glucagon-Like Peptide 1
Cell Cycle
Genes

Keywords

  • Body wall muscles
  • C. elegans
  • Glp-1
  • Mom-2
  • MS blastomere
  • Notch
  • Wnt

ASJC Scopus subject areas

  • Molecular Biology
  • Developmental Biology

Cite this

Reciprocal signaling by Wnt and Notch specifies a muscle precursor in the C. elegans embryo. / Robertson, Scott M.; Medina, Jessica; Oldenbroek, Marieke; Lin, Rueyling.

In: Development (Cambridge), Vol. 144, No. 3, 01.02.2017, p. 419-429.

Research output: Contribution to journalArticle

@article{224a726c53154f54b1a340037e7657e2,
title = "Reciprocal signaling by Wnt and Notch specifies a muscle precursor in the C. elegans embryo",
abstract = "The MS blastomere produces one-third of the body wall muscles (BWMs) in the C. elegans embryo. MS-derived BWMs require two distinct cell-cell interactions, the first inhibitory and the second, two cell cycles later, required to overcome this inhibition. The inductive interaction is not required if the inhibitory signal is absent. Although the Notch receptor GLP-1 was implicated in both interactions, the molecular nature of the two signals was unknown. We now show that zygotically expressed MOM-2 (Wnt) is responsible for both interactions. Both the inhibitory and the activating interactions require precise spatiotemporal expression of zygotic MOM-2, which is dependent upon two distinct Notch signals. In a Notch mutant defective only in the inductive interaction, MS-derived BWMs can be restored by preventing zygotic MOM-2 expression, which removes the inhibitory signal. Our results suggest that the inhibitory interaction ensures the differential lineage specification of MS and its sister blastomere, whereas the inductive interaction promotes the expression of muscle-specifying genes by modulating TCF and β-catenin levels. These results highlight the complexity of cell fate specification by cell-cell interactions in a rapidly dividing embryo.",
keywords = "Body wall muscles, C. elegans, Glp-1, Mom-2, MS blastomere, Notch, Wnt",
author = "Robertson, {Scott M.} and Jessica Medina and Marieke Oldenbroek and Rueyling Lin",
year = "2017",
month = "2",
day = "1",
doi = "10.1242/dev.145391",
language = "English (US)",
volume = "144",
pages = "419--429",
journal = "Development (Cambridge)",
issn = "0950-1991",
publisher = "Company of Biologists Ltd",
number = "3",

}

TY - JOUR

T1 - Reciprocal signaling by Wnt and Notch specifies a muscle precursor in the C. elegans embryo

AU - Robertson, Scott M.

AU - Medina, Jessica

AU - Oldenbroek, Marieke

AU - Lin, Rueyling

PY - 2017/2/1

Y1 - 2017/2/1

N2 - The MS blastomere produces one-third of the body wall muscles (BWMs) in the C. elegans embryo. MS-derived BWMs require two distinct cell-cell interactions, the first inhibitory and the second, two cell cycles later, required to overcome this inhibition. The inductive interaction is not required if the inhibitory signal is absent. Although the Notch receptor GLP-1 was implicated in both interactions, the molecular nature of the two signals was unknown. We now show that zygotically expressed MOM-2 (Wnt) is responsible for both interactions. Both the inhibitory and the activating interactions require precise spatiotemporal expression of zygotic MOM-2, which is dependent upon two distinct Notch signals. In a Notch mutant defective only in the inductive interaction, MS-derived BWMs can be restored by preventing zygotic MOM-2 expression, which removes the inhibitory signal. Our results suggest that the inhibitory interaction ensures the differential lineage specification of MS and its sister blastomere, whereas the inductive interaction promotes the expression of muscle-specifying genes by modulating TCF and β-catenin levels. These results highlight the complexity of cell fate specification by cell-cell interactions in a rapidly dividing embryo.

AB - The MS blastomere produces one-third of the body wall muscles (BWMs) in the C. elegans embryo. MS-derived BWMs require two distinct cell-cell interactions, the first inhibitory and the second, two cell cycles later, required to overcome this inhibition. The inductive interaction is not required if the inhibitory signal is absent. Although the Notch receptor GLP-1 was implicated in both interactions, the molecular nature of the two signals was unknown. We now show that zygotically expressed MOM-2 (Wnt) is responsible for both interactions. Both the inhibitory and the activating interactions require precise spatiotemporal expression of zygotic MOM-2, which is dependent upon two distinct Notch signals. In a Notch mutant defective only in the inductive interaction, MS-derived BWMs can be restored by preventing zygotic MOM-2 expression, which removes the inhibitory signal. Our results suggest that the inhibitory interaction ensures the differential lineage specification of MS and its sister blastomere, whereas the inductive interaction promotes the expression of muscle-specifying genes by modulating TCF and β-catenin levels. These results highlight the complexity of cell fate specification by cell-cell interactions in a rapidly dividing embryo.

KW - Body wall muscles

KW - C. elegans

KW - Glp-1

KW - Mom-2

KW - MS blastomere

KW - Notch

KW - Wnt

UR - http://www.scopus.com/inward/record.url?scp=85011554710&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85011554710&partnerID=8YFLogxK

U2 - 10.1242/dev.145391

DO - 10.1242/dev.145391

M3 - Article

VL - 144

SP - 419

EP - 429

JO - Development (Cambridge)

JF - Development (Cambridge)

SN - 0950-1991

IS - 3

ER -