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Characterization of Drosophila Nidogen/entactin reveals roles in basement membrane stability, barrier function and nervous system patterning

Wolfstetter, Georg ; Dahlitz, Ina ; Pfeifer, Kathrin ; Töpfer, Uwe ; Alt, Joscha Arne ; Pfeifer, Daniel Christoph ; Lakes-Harlan, Reinhard ; Baumgartner, Stefan LU orcid ; Palmer, Ruth H. and Holz, Anne (2019) In Development (Cambridge) 146(2).
Abstract

Basement membranes (BMs) are specialized layers of extracellular matrix (ECM) mainly composed of Laminin, type IV Collagen, Perlecan and Nidogen/entactin (NDG). Recent in vivo studies challenged the initially proposed role of NDG as a major ECM linker molecule by revealing dispensability for viability and BM formation. Here, we report the characterization of the single Ndg gene in Drosophila. Embryonic Ndg expression was primarily observed in mesodermal tissues and the chordotonal organs, whereas NDG protein localized to all BMs. Although loss of Laminin strongly affected BM localization of NDG, Ndg-null mutants exhibited no overt changes in the distribution of BM components. Although Drosophila Ndg mutants were viable, loss of NDG led... (More)

Basement membranes (BMs) are specialized layers of extracellular matrix (ECM) mainly composed of Laminin, type IV Collagen, Perlecan and Nidogen/entactin (NDG). Recent in vivo studies challenged the initially proposed role of NDG as a major ECM linker molecule by revealing dispensability for viability and BM formation. Here, we report the characterization of the single Ndg gene in Drosophila. Embryonic Ndg expression was primarily observed in mesodermal tissues and the chordotonal organs, whereas NDG protein localized to all BMs. Although loss of Laminin strongly affected BM localization of NDG, Ndg-null mutants exhibited no overt changes in the distribution of BM components. Although Drosophila Ndg mutants were viable, loss of NDG led to ultrastructural BM defects that compromised barrier function and stability in vivo Moreover, loss of NDG impaired larval crawling behavior and reduced responses to vibrational stimuli. Further morphological analysis revealed accompanying defects in the larval peripheral nervous system, especially in the chordotonal organs and the neuromuscular junction (NMJ). Taken together, our analysis suggests that NDG is not essential for BM assembly but mediates BM stability and ECM-dependent neural plasticity during Drosophila development.

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organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
Axon guidance, Collagen, Dorsal median cells, ECM, Extracellular matrix, Laminin, Morphogenesis, Muscle, NMJ, Perlecan
in
Development (Cambridge)
volume
146
issue
2
publisher
The Company of Biologists Ltd
external identifiers
  • pmid:30567930
  • scopus:85060157527
ISSN
1477-9129
DOI
10.1242/dev.168948
language
English
LU publication?
yes
id
1ffb8632-5845-4162-896e-8d9127843432
date added to LUP
2019-01-29 08:00:50
date last changed
2025-05-14 09:58:26
@article{1ffb8632-5845-4162-896e-8d9127843432,
  abstract     = {{<p>Basement membranes (BMs) are specialized layers of extracellular matrix (ECM) mainly composed of Laminin, type IV Collagen, Perlecan and Nidogen/entactin (NDG). Recent in vivo studies challenged the initially proposed role of NDG as a major ECM linker molecule by revealing dispensability for viability and BM formation. Here, we report the characterization of the single Ndg gene in Drosophila. Embryonic Ndg expression was primarily observed in mesodermal tissues and the chordotonal organs, whereas NDG protein localized to all BMs. Although loss of Laminin strongly affected BM localization of NDG, Ndg-null mutants exhibited no overt changes in the distribution of BM components. Although Drosophila Ndg mutants were viable, loss of NDG led to ultrastructural BM defects that compromised barrier function and stability in vivo Moreover, loss of NDG impaired larval crawling behavior and reduced responses to vibrational stimuli. Further morphological analysis revealed accompanying defects in the larval peripheral nervous system, especially in the chordotonal organs and the neuromuscular junction (NMJ). Taken together, our analysis suggests that NDG is not essential for BM assembly but mediates BM stability and ECM-dependent neural plasticity during Drosophila development.</p>}},
  author       = {{Wolfstetter, Georg and Dahlitz, Ina and Pfeifer, Kathrin and Töpfer, Uwe and Alt, Joscha Arne and Pfeifer, Daniel Christoph and Lakes-Harlan, Reinhard and Baumgartner, Stefan and Palmer, Ruth H. and Holz, Anne}},
  issn         = {{1477-9129}},
  keywords     = {{Axon guidance; Collagen; Dorsal median cells; ECM; Extracellular matrix; Laminin; Morphogenesis; Muscle; NMJ; Perlecan}},
  language     = {{eng}},
  number       = {{2}},
  publisher    = {{The Company of Biologists Ltd}},
  series       = {{Development (Cambridge)}},
  title        = {{Characterization of Drosophila Nidogen/entactin reveals roles in basement membrane stability, barrier function and nervous system patterning}},
  url          = {{http://dx.doi.org/10.1242/dev.168948}},
  doi          = {{10.1242/dev.168948}},
  volume       = {{146}},
  year         = {{2019}},
}