Axon-Dependent Patterning and Maintenance of Somatosensory Dendritic Arbors

Nelson J. Ramirez-Suarez, Helen M. Belalcazar, Christopher J. Salazar, Burcu Beyaz, Benjamin Raja, Ken C.Q. Nguyen, Kevin Celestrin, Julius Fredens, Nils J. Færgeman, David H. Hall, Hannes E. Buelow

Research output: Contribution to journalArticle

1 Citation (Scopus)

Abstract

The mechanisms that pattern and maintain dendritic arbors are key to understanding the principles that govern nervous system assembly. The activity of presynaptic axons has long been known to shape dendrites, but activity-independent functions of axons in this process have remained elusive. Here, we show that in Caenorhabditis elegans, the axons of the ALA neuron control guidance and extension of the 1° dendrites of PVD somatosensory neurons independently of ALA activity. PVD 1° dendrites mimic ALA axon guidance defects in loss-of-function mutants for the extracellular matrix molecule MIG-6/Papilin or the UNC-6/Netrin pathway, suggesting that axon-dendrite adhesion is important for dendrite formation. We found that the SAX-7/L1CAM cell adhesion molecule engages in distinct molecular mechanisms to mediate extensions of PVD 1° dendrites and maintain the ALA-PVD axon-dendritic fascicle, respectively. Thus, axons can serve as critical scaffolds to pattern and maintain dendrites through contact-dependent but activity-independent mechanisms.

Original languageEnglish (US)
Pages (from-to)229-244.e4
JournalDevelopmental Cell
Volume48
Issue number2
DOIs
StatePublished - Jan 28 2019

Fingerprint

Dendrites
Axons
Maintenance
Physical vapor deposition
Neurons
Neural Cell Adhesion Molecule L1
Caenorhabditis elegans
Cell Adhesion Molecules
Neurology
Scaffolds
Nervous System
Extracellular Matrix
Adhesion
Defects
Molecules

Keywords

  • activity-dependent
  • activity-independent
  • axon
  • dendrite
  • L1CAM
  • maintenance
  • Menorin
  • Netrin
  • Papilin
  • self-assembly

ASJC Scopus subject areas

  • Molecular Biology
  • Biochemistry, Genetics and Molecular Biology(all)
  • Developmental Biology
  • Cell Biology

Cite this

Axon-Dependent Patterning and Maintenance of Somatosensory Dendritic Arbors. / Ramirez-Suarez, Nelson J.; Belalcazar, Helen M.; Salazar, Christopher J.; Beyaz, Burcu; Raja, Benjamin; Nguyen, Ken C.Q.; Celestrin, Kevin; Fredens, Julius; Færgeman, Nils J.; Hall, David H.; Buelow, Hannes E.

In: Developmental Cell, Vol. 48, No. 2, 28.01.2019, p. 229-244.e4.

Research output: Contribution to journalArticle

Ramirez-Suarez, NJ, Belalcazar, HM, Salazar, CJ, Beyaz, B, Raja, B, Nguyen, KCQ, Celestrin, K, Fredens, J, Færgeman, NJ, Hall, DH & Buelow, HE 2019, 'Axon-Dependent Patterning and Maintenance of Somatosensory Dendritic Arbors', Developmental Cell, vol. 48, no. 2, pp. 229-244.e4. https://doi.org/10.1016/j.devcel.2018.12.015
Ramirez-Suarez NJ, Belalcazar HM, Salazar CJ, Beyaz B, Raja B, Nguyen KCQ et al. Axon-Dependent Patterning and Maintenance of Somatosensory Dendritic Arbors. Developmental Cell. 2019 Jan 28;48(2):229-244.e4. https://doi.org/10.1016/j.devcel.2018.12.015
Ramirez-Suarez, Nelson J. ; Belalcazar, Helen M. ; Salazar, Christopher J. ; Beyaz, Burcu ; Raja, Benjamin ; Nguyen, Ken C.Q. ; Celestrin, Kevin ; Fredens, Julius ; Færgeman, Nils J. ; Hall, David H. ; Buelow, Hannes E. / Axon-Dependent Patterning and Maintenance of Somatosensory Dendritic Arbors. In: Developmental Cell. 2019 ; Vol. 48, No. 2. pp. 229-244.e4.
@article{1383eb9863d541ce8e17bc1f852581f5,
title = "Axon-Dependent Patterning and Maintenance of Somatosensory Dendritic Arbors",
abstract = "The mechanisms that pattern and maintain dendritic arbors are key to understanding the principles that govern nervous system assembly. The activity of presynaptic axons has long been known to shape dendrites, but activity-independent functions of axons in this process have remained elusive. Here, we show that in Caenorhabditis elegans, the axons of the ALA neuron control guidance and extension of the 1° dendrites of PVD somatosensory neurons independently of ALA activity. PVD 1° dendrites mimic ALA axon guidance defects in loss-of-function mutants for the extracellular matrix molecule MIG-6/Papilin or the UNC-6/Netrin pathway, suggesting that axon-dendrite adhesion is important for dendrite formation. We found that the SAX-7/L1CAM cell adhesion molecule engages in distinct molecular mechanisms to mediate extensions of PVD 1° dendrites and maintain the ALA-PVD axon-dendritic fascicle, respectively. Thus, axons can serve as critical scaffolds to pattern and maintain dendrites through contact-dependent but activity-independent mechanisms.",
keywords = "activity-dependent, activity-independent, axon, dendrite, L1CAM, maintenance, Menorin, Netrin, Papilin, self-assembly",
author = "Ramirez-Suarez, {Nelson J.} and Belalcazar, {Helen M.} and Salazar, {Christopher J.} and Burcu Beyaz and Benjamin Raja and Nguyen, {Ken C.Q.} and Kevin Celestrin and Julius Fredens and F{\ae}rgeman, {Nils J.} and Hall, {David H.} and Buelow, {Hannes E.}",
year = "2019",
month = "1",
day = "28",
doi = "10.1016/j.devcel.2018.12.015",
language = "English (US)",
volume = "48",
pages = "229--244.e4",
journal = "Developmental Cell",
issn = "1534-5807",
publisher = "Cell Press",
number = "2",

}

TY - JOUR

T1 - Axon-Dependent Patterning and Maintenance of Somatosensory Dendritic Arbors

AU - Ramirez-Suarez, Nelson J.

AU - Belalcazar, Helen M.

AU - Salazar, Christopher J.

AU - Beyaz, Burcu

AU - Raja, Benjamin

AU - Nguyen, Ken C.Q.

AU - Celestrin, Kevin

AU - Fredens, Julius

AU - Færgeman, Nils J.

AU - Hall, David H.

AU - Buelow, Hannes E.

PY - 2019/1/28

Y1 - 2019/1/28

N2 - The mechanisms that pattern and maintain dendritic arbors are key to understanding the principles that govern nervous system assembly. The activity of presynaptic axons has long been known to shape dendrites, but activity-independent functions of axons in this process have remained elusive. Here, we show that in Caenorhabditis elegans, the axons of the ALA neuron control guidance and extension of the 1° dendrites of PVD somatosensory neurons independently of ALA activity. PVD 1° dendrites mimic ALA axon guidance defects in loss-of-function mutants for the extracellular matrix molecule MIG-6/Papilin or the UNC-6/Netrin pathway, suggesting that axon-dendrite adhesion is important for dendrite formation. We found that the SAX-7/L1CAM cell adhesion molecule engages in distinct molecular mechanisms to mediate extensions of PVD 1° dendrites and maintain the ALA-PVD axon-dendritic fascicle, respectively. Thus, axons can serve as critical scaffolds to pattern and maintain dendrites through contact-dependent but activity-independent mechanisms.

AB - The mechanisms that pattern and maintain dendritic arbors are key to understanding the principles that govern nervous system assembly. The activity of presynaptic axons has long been known to shape dendrites, but activity-independent functions of axons in this process have remained elusive. Here, we show that in Caenorhabditis elegans, the axons of the ALA neuron control guidance and extension of the 1° dendrites of PVD somatosensory neurons independently of ALA activity. PVD 1° dendrites mimic ALA axon guidance defects in loss-of-function mutants for the extracellular matrix molecule MIG-6/Papilin or the UNC-6/Netrin pathway, suggesting that axon-dendrite adhesion is important for dendrite formation. We found that the SAX-7/L1CAM cell adhesion molecule engages in distinct molecular mechanisms to mediate extensions of PVD 1° dendrites and maintain the ALA-PVD axon-dendritic fascicle, respectively. Thus, axons can serve as critical scaffolds to pattern and maintain dendrites through contact-dependent but activity-independent mechanisms.

KW - activity-dependent

KW - activity-independent

KW - axon

KW - dendrite

KW - L1CAM

KW - maintenance

KW - Menorin

KW - Netrin

KW - Papilin

KW - self-assembly

UR - http://www.scopus.com/inward/record.url?scp=85060282874&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85060282874&partnerID=8YFLogxK

U2 - 10.1016/j.devcel.2018.12.015

DO - 10.1016/j.devcel.2018.12.015

M3 - Article

VL - 48

SP - 229-244.e4

JO - Developmental Cell

JF - Developmental Cell

SN - 1534-5807

IS - 2

ER -