DIG-1, a novel giant protein, non-autonomously mediates maintenance of nervous system architecture

Claire Y. Bénard, Alexander Boyanov, David H. Hall, Oliver Hobert

Research output: Contribution to journalArticle

24 Citations (Scopus)

Abstract

Dedicated mechanisms exist to maintain the architecture of an animal's nervous system after development is completed. To date, three immunoglobulin superfamily members have been implicated in this process in the nematode Caenorhabditis elegans: the secreted two-Ig domain protein ZIG-4, the FGF receptor EGL-15 and the L1-like SAX-7 protein. These proteins provide crucial information for neuronal structures, such as axons, that allows them to maintain the precise position they acquired during development. Yet, how widespread this mechanism is throughout the nervous system, and what other types of factors underlie such a maintenance mechanism, remains poorly understood. Here, we describe a new maintenance gene, dig-1, that encodes a predicted giant secreted protein containing a large number of protein interaction domains. With 13,100 amino acids, the DIG-1 protein is the largest secreted protein identifiable in any genome database. dig-1 functions post-developmentally to maintain axons and cell bodies in place within axonal fascicles and ganglia. The failure to maintain axon and cell body position is accompanied by defects in basement membrane structure, as evidenced by electron microscopy analysis of dig-1 mutants. Expression pattern and mosaic analysis reveals that dig-1 is produced by muscles to maintain nervous system architecture, demonstrating that dig-1 functions non-autonomously to preserve the proper layout of neural structures. We propose that DIG-1 is a component of the basement membrane that mediates specific contacts between cellular surfaces and their environment through the interaction with a cell-type specific set of other maintenance factors.

Original languageEnglish (US)
Pages (from-to)3329-3340
Number of pages12
JournalDevelopment
Volume133
Issue number17
DOIs
StatePublished - Sep 2006

Fingerprint

Nervous System
Maintenance
Axons
Proteins
Basement Membrane
Protein Interaction Domains and Motifs
Fibroblast Growth Factor Receptors
Caenorhabditis elegans
Ganglia
Immunoglobulins
Electron Microscopy
Genome
Databases
Amino Acids
Muscles
Genes
Cell Body

Keywords

  • Adhesion
  • Axon
  • Basement membrane
  • Caenorhabditis elegans
  • dig-1
  • Extracellular matrix
  • Fnll
  • lg
  • Maintenance
  • Sax-8

ASJC Scopus subject areas

  • Anatomy
  • Cell Biology

Cite this

DIG-1, a novel giant protein, non-autonomously mediates maintenance of nervous system architecture. / Bénard, Claire Y.; Boyanov, Alexander; Hall, David H.; Hobert, Oliver.

In: Development, Vol. 133, No. 17, 09.2006, p. 3329-3340.

Research output: Contribution to journalArticle

Bénard, Claire Y. ; Boyanov, Alexander ; Hall, David H. ; Hobert, Oliver. / DIG-1, a novel giant protein, non-autonomously mediates maintenance of nervous system architecture. In: Development. 2006 ; Vol. 133, No. 17. pp. 3329-3340.
@article{1520c9f588e444ab8e36344397f06d36,
title = "DIG-1, a novel giant protein, non-autonomously mediates maintenance of nervous system architecture",
abstract = "Dedicated mechanisms exist to maintain the architecture of an animal's nervous system after development is completed. To date, three immunoglobulin superfamily members have been implicated in this process in the nematode Caenorhabditis elegans: the secreted two-Ig domain protein ZIG-4, the FGF receptor EGL-15 and the L1-like SAX-7 protein. These proteins provide crucial information for neuronal structures, such as axons, that allows them to maintain the precise position they acquired during development. Yet, how widespread this mechanism is throughout the nervous system, and what other types of factors underlie such a maintenance mechanism, remains poorly understood. Here, we describe a new maintenance gene, dig-1, that encodes a predicted giant secreted protein containing a large number of protein interaction domains. With 13,100 amino acids, the DIG-1 protein is the largest secreted protein identifiable in any genome database. dig-1 functions post-developmentally to maintain axons and cell bodies in place within axonal fascicles and ganglia. The failure to maintain axon and cell body position is accompanied by defects in basement membrane structure, as evidenced by electron microscopy analysis of dig-1 mutants. Expression pattern and mosaic analysis reveals that dig-1 is produced by muscles to maintain nervous system architecture, demonstrating that dig-1 functions non-autonomously to preserve the proper layout of neural structures. We propose that DIG-1 is a component of the basement membrane that mediates specific contacts between cellular surfaces and their environment through the interaction with a cell-type specific set of other maintenance factors.",
keywords = "Adhesion, Axon, Basement membrane, Caenorhabditis elegans, dig-1, Extracellular matrix, Fnll, lg, Maintenance, Sax-8",
author = "B{\'e}nard, {Claire Y.} and Alexander Boyanov and Hall, {David H.} and Oliver Hobert",
year = "2006",
month = "9",
doi = "10.1242/dev.02507",
language = "English (US)",
volume = "133",
pages = "3329--3340",
journal = "Development (Cambridge)",
issn = "0950-1991",
publisher = "Company of Biologists Ltd",
number = "17",

}

TY - JOUR

T1 - DIG-1, a novel giant protein, non-autonomously mediates maintenance of nervous system architecture

AU - Bénard, Claire Y.

AU - Boyanov, Alexander

AU - Hall, David H.

AU - Hobert, Oliver

PY - 2006/9

Y1 - 2006/9

N2 - Dedicated mechanisms exist to maintain the architecture of an animal's nervous system after development is completed. To date, three immunoglobulin superfamily members have been implicated in this process in the nematode Caenorhabditis elegans: the secreted two-Ig domain protein ZIG-4, the FGF receptor EGL-15 and the L1-like SAX-7 protein. These proteins provide crucial information for neuronal structures, such as axons, that allows them to maintain the precise position they acquired during development. Yet, how widespread this mechanism is throughout the nervous system, and what other types of factors underlie such a maintenance mechanism, remains poorly understood. Here, we describe a new maintenance gene, dig-1, that encodes a predicted giant secreted protein containing a large number of protein interaction domains. With 13,100 amino acids, the DIG-1 protein is the largest secreted protein identifiable in any genome database. dig-1 functions post-developmentally to maintain axons and cell bodies in place within axonal fascicles and ganglia. The failure to maintain axon and cell body position is accompanied by defects in basement membrane structure, as evidenced by electron microscopy analysis of dig-1 mutants. Expression pattern and mosaic analysis reveals that dig-1 is produced by muscles to maintain nervous system architecture, demonstrating that dig-1 functions non-autonomously to preserve the proper layout of neural structures. We propose that DIG-1 is a component of the basement membrane that mediates specific contacts between cellular surfaces and their environment through the interaction with a cell-type specific set of other maintenance factors.

AB - Dedicated mechanisms exist to maintain the architecture of an animal's nervous system after development is completed. To date, three immunoglobulin superfamily members have been implicated in this process in the nematode Caenorhabditis elegans: the secreted two-Ig domain protein ZIG-4, the FGF receptor EGL-15 and the L1-like SAX-7 protein. These proteins provide crucial information for neuronal structures, such as axons, that allows them to maintain the precise position they acquired during development. Yet, how widespread this mechanism is throughout the nervous system, and what other types of factors underlie such a maintenance mechanism, remains poorly understood. Here, we describe a new maintenance gene, dig-1, that encodes a predicted giant secreted protein containing a large number of protein interaction domains. With 13,100 amino acids, the DIG-1 protein is the largest secreted protein identifiable in any genome database. dig-1 functions post-developmentally to maintain axons and cell bodies in place within axonal fascicles and ganglia. The failure to maintain axon and cell body position is accompanied by defects in basement membrane structure, as evidenced by electron microscopy analysis of dig-1 mutants. Expression pattern and mosaic analysis reveals that dig-1 is produced by muscles to maintain nervous system architecture, demonstrating that dig-1 functions non-autonomously to preserve the proper layout of neural structures. We propose that DIG-1 is a component of the basement membrane that mediates specific contacts between cellular surfaces and their environment through the interaction with a cell-type specific set of other maintenance factors.

KW - Adhesion

KW - Axon

KW - Basement membrane

KW - Caenorhabditis elegans

KW - dig-1

KW - Extracellular matrix

KW - Fnll

KW - lg

KW - Maintenance

KW - Sax-8

UR - http://www.scopus.com/inward/record.url?scp=33749393939&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=33749393939&partnerID=8YFLogxK

U2 - 10.1242/dev.02507

DO - 10.1242/dev.02507

M3 - Article

C2 - 16887823

AN - SCOPUS:33749393939

VL - 133

SP - 3329

EP - 3340

JO - Development (Cambridge)

JF - Development (Cambridge)

SN - 0950-1991

IS - 17

ER -