Basal filopodia and vascular mechanical stress organize fibronectin into pillars bridging the mesoderm-endoderm gap

Yuki Sato, Kei Nagatoshi, Ayumi Hamano, Yuko Imamura, David Huss, Seiichi Uchida, Rusty Lansford

Research output: Contribution to journalArticle

8 Citations (Scopus)

Abstract

Cells may exchange information with other cells and tissues by exerting forces on the extracellular matrix (ECM). Fibronectin (FN) is an important ECM component that forms fibrils through cell contacts and creates directionally biased geometry. Here, we demonstrate that FN is deposited as pillars between widely separated germ layers, namely the somitic mesoderm and the endoderm, in quail embryos. Alongside the FN pillars, long filopodia protrude from the basal surfaces of somite epithelial cells. Loss-of-function of Ena/VASP, α5β1-integrins or talin in the somitic cells abolished the FN pillars, indicating that FN pillar formation is dependent on the basal filopodia through these molecules. The basal filopodia and FN pillars are also necessary for proper somite morphogenesis. We identified a new mechanism contributing to FN pillar formation by focusing on cyclic expansion of adjacent dorsal aorta. Maintenance of the directional alignment of the FN pillars depends on pulsatile blood flow through the dorsal aortae. These results suggest that the FN pillars are specifically established through filopodia-mediated and pulsating force-related mechanisms.

Original languageEnglish
Pages (from-to)281-291
Number of pages11
JournalDevelopment (Cambridge, England)
Volume144
Issue number2
DOIs
Publication statusPublished - Jan 15 2017

Fingerprint

Endoderm
Mechanical Stress
Pseudopodia
Mesoderm
Fibronectins
Blood Vessels
Somites
Extracellular Matrix
Aorta
Talin
Pulsatile Flow
Germ Layers
Quail
Morphogenesis
Integrins
Embryonic Structures
Epithelial Cells
Maintenance

All Science Journal Classification (ASJC) codes

  • Molecular Biology
  • Developmental Biology

Cite this

Basal filopodia and vascular mechanical stress organize fibronectin into pillars bridging the mesoderm-endoderm gap. / Sato, Yuki; Nagatoshi, Kei; Hamano, Ayumi; Imamura, Yuko; Huss, David; Uchida, Seiichi; Lansford, Rusty.

In: Development (Cambridge, England), Vol. 144, No. 2, 15.01.2017, p. 281-291.

Research output: Contribution to journalArticle

Sato, Yuki ; Nagatoshi, Kei ; Hamano, Ayumi ; Imamura, Yuko ; Huss, David ; Uchida, Seiichi ; Lansford, Rusty. / Basal filopodia and vascular mechanical stress organize fibronectin into pillars bridging the mesoderm-endoderm gap. In: Development (Cambridge, England). 2017 ; Vol. 144, No. 2. pp. 281-291.
@article{a6db501ab7ba4da6a9c496c14d2e622e,
title = "Basal filopodia and vascular mechanical stress organize fibronectin into pillars bridging the mesoderm-endoderm gap",
abstract = "Cells may exchange information with other cells and tissues by exerting forces on the extracellular matrix (ECM). Fibronectin (FN) is an important ECM component that forms fibrils through cell contacts and creates directionally biased geometry. Here, we demonstrate that FN is deposited as pillars between widely separated germ layers, namely the somitic mesoderm and the endoderm, in quail embryos. Alongside the FN pillars, long filopodia protrude from the basal surfaces of somite epithelial cells. Loss-of-function of Ena/VASP, α5β1-integrins or talin in the somitic cells abolished the FN pillars, indicating that FN pillar formation is dependent on the basal filopodia through these molecules. The basal filopodia and FN pillars are also necessary for proper somite morphogenesis. We identified a new mechanism contributing to FN pillar formation by focusing on cyclic expansion of adjacent dorsal aorta. Maintenance of the directional alignment of the FN pillars depends on pulsatile blood flow through the dorsal aortae. These results suggest that the FN pillars are specifically established through filopodia-mediated and pulsating force-related mechanisms.",
author = "Yuki Sato and Kei Nagatoshi and Ayumi Hamano and Yuko Imamura and David Huss and Seiichi Uchida and Rusty Lansford",
year = "2017",
month = "1",
day = "15",
doi = "10.1242/dev.141259",
language = "English",
volume = "144",
pages = "281--291",
journal = "Development (Cambridge)",
issn = "0950-1991",
publisher = "Company of Biologists Ltd",
number = "2",

}

TY - JOUR

T1 - Basal filopodia and vascular mechanical stress organize fibronectin into pillars bridging the mesoderm-endoderm gap

AU - Sato, Yuki

AU - Nagatoshi, Kei

AU - Hamano, Ayumi

AU - Imamura, Yuko

AU - Huss, David

AU - Uchida, Seiichi

AU - Lansford, Rusty

PY - 2017/1/15

Y1 - 2017/1/15

N2 - Cells may exchange information with other cells and tissues by exerting forces on the extracellular matrix (ECM). Fibronectin (FN) is an important ECM component that forms fibrils through cell contacts and creates directionally biased geometry. Here, we demonstrate that FN is deposited as pillars between widely separated germ layers, namely the somitic mesoderm and the endoderm, in quail embryos. Alongside the FN pillars, long filopodia protrude from the basal surfaces of somite epithelial cells. Loss-of-function of Ena/VASP, α5β1-integrins or talin in the somitic cells abolished the FN pillars, indicating that FN pillar formation is dependent on the basal filopodia through these molecules. The basal filopodia and FN pillars are also necessary for proper somite morphogenesis. We identified a new mechanism contributing to FN pillar formation by focusing on cyclic expansion of adjacent dorsal aorta. Maintenance of the directional alignment of the FN pillars depends on pulsatile blood flow through the dorsal aortae. These results suggest that the FN pillars are specifically established through filopodia-mediated and pulsating force-related mechanisms.

AB - Cells may exchange information with other cells and tissues by exerting forces on the extracellular matrix (ECM). Fibronectin (FN) is an important ECM component that forms fibrils through cell contacts and creates directionally biased geometry. Here, we demonstrate that FN is deposited as pillars between widely separated germ layers, namely the somitic mesoderm and the endoderm, in quail embryos. Alongside the FN pillars, long filopodia protrude from the basal surfaces of somite epithelial cells. Loss-of-function of Ena/VASP, α5β1-integrins or talin in the somitic cells abolished the FN pillars, indicating that FN pillar formation is dependent on the basal filopodia through these molecules. The basal filopodia and FN pillars are also necessary for proper somite morphogenesis. We identified a new mechanism contributing to FN pillar formation by focusing on cyclic expansion of adjacent dorsal aorta. Maintenance of the directional alignment of the FN pillars depends on pulsatile blood flow through the dorsal aortae. These results suggest that the FN pillars are specifically established through filopodia-mediated and pulsating force-related mechanisms.

UR - http://www.scopus.com/inward/record.url?scp=85010028411&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85010028411&partnerID=8YFLogxK

U2 - 10.1242/dev.141259

DO - 10.1242/dev.141259

M3 - Article

C2 - 28096216

AN - SCOPUS:85010028411

VL - 144

SP - 281

EP - 291

JO - Development (Cambridge)

JF - Development (Cambridge)

SN - 0950-1991

IS - 2

ER -