The Collagens DPY-17 and SQT-3 Direct Anterior–Posterior Migration of the Q Neuroblasts in <i>C. elegans</i>

Cell adhesion molecules and their extracellular ligands control morphogenetic events such as directed cell migration. The migration of neuroblasts and neural crest cells establishes the structure of the central and peripheral nervous systems. In <i>C. elegans</i>, the bilateral Q neurobl...

Full description

Bibliographic Details
Main Authors: Angelica E. Lang, Erik A. Lundquist
Format: Article
Language:English
Published: MDPI AG 2021-02-01
Series:Journal of Developmental Biology
Subjects:
Online Access:https://www.mdpi.com/2221-3759/9/1/7
id doaj-4a3b862bb3c449198b733dc102849776
record_format Article
spelling doaj-4a3b862bb3c449198b733dc1028497762021-02-20T00:06:37ZengMDPI AGJournal of Developmental Biology2221-37592021-02-0197710.3390/jdb9010007The Collagens DPY-17 and SQT-3 Direct Anterior–Posterior Migration of the Q Neuroblasts in <i>C. elegans</i>Angelica E. Lang0Erik A. Lundquist1Department of Molecular Biosciences, The University of Kansas, Lawrence, KS 66046, USADepartment of Molecular Biosciences, The University of Kansas, Lawrence, KS 66046, USACell adhesion molecules and their extracellular ligands control morphogenetic events such as directed cell migration. The migration of neuroblasts and neural crest cells establishes the structure of the central and peripheral nervous systems. In <i>C. elegans</i>, the bilateral Q neuroblasts and their descendants undergo long-range migrations with left/right asymmetry. QR and its descendants on the right migrate anteriorly, and QL and its descendants on the left migrate posteriorly, despite identical patterns of cell division, cell death, and neuronal generation. The initial direction of protrusion of the Q cells relies on the left/right asymmetric functions of the transmembrane receptors UNC-40/DCC and PTP-3/LAR in the Q cells. Here, we show that Q cell left/right asymmetry of migration is independent of the GPA-16/Ga pathway which regulates other left/right asymmetries, including nervous system L/R asymmetry. No extracellular cue has been identified that guides initial Q anterior versus posterior migrations. We show that collagens DPY-17 and SQT-3 control initial Q direction of protrusion. Genetic interactions with UNC-40/DCC and PTP-3/LAR suggest that DPY-17 and SQT-3 drive posterior migration and might act with both receptors or in a parallel pathway. Analysis of mutants in other collagens and extracellular matrix components indicated that general perturbation of collagens and the extracellular matrix (ECM) did not result in directional defects, and that the effect of DPY-17 and SQT-3 on Q direction is specific. DPY-17 and SQT-3 are components of the cuticle, but a role in the basement membrane cannot be excluded. Possibly, DPY-17 and SQT-3 are part of a pattern in the cuticle and/or basement membrane that is oriented to the anterior–posterior axis of the animal and that is deciphered by the Q cells in a left–right asymmetric fashion. Alternatively, DPY-17 and SQT-3 might be involved in the production or stabilization of a guidance cue that directs Q migrations. In any case, these results describe a novel role for the DPY-17 and SQT-3 collagens in directing posterior Q neuroblast migration.https://www.mdpi.com/2221-3759/9/1/7directed neuronal migrationcollagenUNC-40/DCCPTP-3/LARextracellular matrix<i>C. elegans</i>
collection DOAJ
language English
format Article
sources DOAJ
author Angelica E. Lang
Erik A. Lundquist
spellingShingle Angelica E. Lang
Erik A. Lundquist
The Collagens DPY-17 and SQT-3 Direct Anterior–Posterior Migration of the Q Neuroblasts in <i>C. elegans</i>
Journal of Developmental Biology
directed neuronal migration
collagen
UNC-40/DCC
PTP-3/LAR
extracellular matrix
<i>C. elegans</i>
author_facet Angelica E. Lang
Erik A. Lundquist
author_sort Angelica E. Lang
title The Collagens DPY-17 and SQT-3 Direct Anterior–Posterior Migration of the Q Neuroblasts in <i>C. elegans</i>
title_short The Collagens DPY-17 and SQT-3 Direct Anterior–Posterior Migration of the Q Neuroblasts in <i>C. elegans</i>
title_full The Collagens DPY-17 and SQT-3 Direct Anterior–Posterior Migration of the Q Neuroblasts in <i>C. elegans</i>
title_fullStr The Collagens DPY-17 and SQT-3 Direct Anterior–Posterior Migration of the Q Neuroblasts in <i>C. elegans</i>
title_full_unstemmed The Collagens DPY-17 and SQT-3 Direct Anterior–Posterior Migration of the Q Neuroblasts in <i>C. elegans</i>
title_sort collagens dpy-17 and sqt-3 direct anterior–posterior migration of the q neuroblasts in <i>c. elegans</i>
publisher MDPI AG
series Journal of Developmental Biology
issn 2221-3759
publishDate 2021-02-01
description Cell adhesion molecules and their extracellular ligands control morphogenetic events such as directed cell migration. The migration of neuroblasts and neural crest cells establishes the structure of the central and peripheral nervous systems. In <i>C. elegans</i>, the bilateral Q neuroblasts and their descendants undergo long-range migrations with left/right asymmetry. QR and its descendants on the right migrate anteriorly, and QL and its descendants on the left migrate posteriorly, despite identical patterns of cell division, cell death, and neuronal generation. The initial direction of protrusion of the Q cells relies on the left/right asymmetric functions of the transmembrane receptors UNC-40/DCC and PTP-3/LAR in the Q cells. Here, we show that Q cell left/right asymmetry of migration is independent of the GPA-16/Ga pathway which regulates other left/right asymmetries, including nervous system L/R asymmetry. No extracellular cue has been identified that guides initial Q anterior versus posterior migrations. We show that collagens DPY-17 and SQT-3 control initial Q direction of protrusion. Genetic interactions with UNC-40/DCC and PTP-3/LAR suggest that DPY-17 and SQT-3 drive posterior migration and might act with both receptors or in a parallel pathway. Analysis of mutants in other collagens and extracellular matrix components indicated that general perturbation of collagens and the extracellular matrix (ECM) did not result in directional defects, and that the effect of DPY-17 and SQT-3 on Q direction is specific. DPY-17 and SQT-3 are components of the cuticle, but a role in the basement membrane cannot be excluded. Possibly, DPY-17 and SQT-3 are part of a pattern in the cuticle and/or basement membrane that is oriented to the anterior–posterior axis of the animal and that is deciphered by the Q cells in a left–right asymmetric fashion. Alternatively, DPY-17 and SQT-3 might be involved in the production or stabilization of a guidance cue that directs Q migrations. In any case, these results describe a novel role for the DPY-17 and SQT-3 collagens in directing posterior Q neuroblast migration.
topic directed neuronal migration
collagen
UNC-40/DCC
PTP-3/LAR
extracellular matrix
<i>C. elegans</i>
url https://www.mdpi.com/2221-3759/9/1/7
work_keys_str_mv AT angelicaelang thecollagensdpy17andsqt3directanteriorposteriormigrationoftheqneuroblastsinicelegansi
AT erikalundquist thecollagensdpy17andsqt3directanteriorposteriormigrationoftheqneuroblastsinicelegansi
AT angelicaelang collagensdpy17andsqt3directanteriorposteriormigrationoftheqneuroblastsinicelegansi
AT erikalundquist collagensdpy17andsqt3directanteriorposteriormigrationoftheqneuroblastsinicelegansi
_version_ 1724259964929703936