Ethanol exposure disrupts extraembryonic microtubule cytoskeleton and embryonic blastomere cell adhesion, producing epiboly and gastrulation defects

Swapnalee Sarmah, Pooja Muralidharan, Courtney L. Curtis, Jeanette McClintick, Bryce B. Buente, David J. Holdgrafer, Osato Ogbeifun, Opeyemi C. Olorungbounmi, Liliana Patino, Ryan Lucas, Sonya Gilbert, Evan S. Groninger, Julia Arciero, Howard Edenberg, James A. Marrs

Research output: Contribution to journalArticle

8 Citations (Scopus)

Abstract

Fetal alcohol spectrum disorder (FASD) occurs when pregnant mothers consume alcohol, causing embryonic ethanol exposure and characteristic birth defects that include craniofacial, neural and cardiac defects. Gastrulation is a particularly sensitive developmental stage for teratogen exposure, and zebrafish is an outstanding model to study gastrulation and FASD. Epiboly (spreading blastomere cells over the yolk cell), prechordal plate migration and convergence/extension cell movements are sensitive to early ethanol exposure. Here, experiments are presented that characterize mechanisms of ethanol toxicity on epiboly and gastrulation. Epiboly mechanisms include blastomere radial intercalation cell movements and yolk cell microtubule cytoskeleton pulling the embryo to the vegetal pole. Both of these processes were disrupted by ethanol exposure. Ethanol effects on cell migration also indicated that cell adhesion was affected, which was confirmed by cell aggregation assays. E-cadherin cell adhesion molecule expression was not affected by ethanol exposure, but E-cadherin distribution, which controls epiboly and gastrulation, was changed. E-cadherin was redistributed into cytoplasmic aggregates in blastomeres and dramatically redistributed in the extraembryonic yolk cell. Gene expression microarray analysis was used to identify potential causative factors for early development defects, and expression of the cell adhesion molecule protocadherin-18a (pcdh18a), which controls epiboly, was significantly reduced in ethanol exposed embryos. Injecting pcdh18a synthetic mRNA in ethanol treated embryos partially rescued epiboly cell movements, including enveloping layer cell shape changes. Together, data show that epiboly and gastrulation defects induced by ethanol are multifactorial, and include yolk cell (extraembryonic tissue) microtubule cytoskeleton disruption and blastomere adhesion defects, in part caused by reduced pcdh18a expression.

Original languageEnglish (US)
Pages (from-to)1013-1021
Number of pages9
JournalBiology Open
Volume2
Issue number10
DOIs
StatePublished - Oct 15 2013

Fingerprint

Blastomeres
Gastrulation
blastomeres
Cell adhesion
cytoskeleton
Cytoskeleton
cell adhesion
Cell Adhesion
Microtubules
microtubules
Ethanol
cadherins
ethanol
Defects
cell movement
Cell Movement
fetal alcohol syndrome
Cadherins
Fetal Alcohol Spectrum Disorders
cells

Keywords

  • Cell adhesion
  • Fetal alcohol spectrum disorder
  • Gastrulation
  • Zebrafish

ASJC Scopus subject areas

  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)

Cite this

Sarmah, S., Muralidharan, P., Curtis, C. L., McClintick, J., Buente, B. B., Holdgrafer, D. J., ... Marrs, J. A. (2013). Ethanol exposure disrupts extraembryonic microtubule cytoskeleton and embryonic blastomere cell adhesion, producing epiboly and gastrulation defects. Biology Open, 2(10), 1013-1021. https://doi.org/10.1242/bio.20135546

Ethanol exposure disrupts extraembryonic microtubule cytoskeleton and embryonic blastomere cell adhesion, producing epiboly and gastrulation defects. / Sarmah, Swapnalee; Muralidharan, Pooja; Curtis, Courtney L.; McClintick, Jeanette; Buente, Bryce B.; Holdgrafer, David J.; Ogbeifun, Osato; Olorungbounmi, Opeyemi C.; Patino, Liliana; Lucas, Ryan; Gilbert, Sonya; Groninger, Evan S.; Arciero, Julia; Edenberg, Howard; Marrs, James A.

In: Biology Open, Vol. 2, No. 10, 15.10.2013, p. 1013-1021.

Research output: Contribution to journalArticle

Sarmah, S, Muralidharan, P, Curtis, CL, McClintick, J, Buente, BB, Holdgrafer, DJ, Ogbeifun, O, Olorungbounmi, OC, Patino, L, Lucas, R, Gilbert, S, Groninger, ES, Arciero, J, Edenberg, H & Marrs, JA 2013, 'Ethanol exposure disrupts extraembryonic microtubule cytoskeleton and embryonic blastomere cell adhesion, producing epiboly and gastrulation defects', Biology Open, vol. 2, no. 10, pp. 1013-1021. https://doi.org/10.1242/bio.20135546
Sarmah, Swapnalee ; Muralidharan, Pooja ; Curtis, Courtney L. ; McClintick, Jeanette ; Buente, Bryce B. ; Holdgrafer, David J. ; Ogbeifun, Osato ; Olorungbounmi, Opeyemi C. ; Patino, Liliana ; Lucas, Ryan ; Gilbert, Sonya ; Groninger, Evan S. ; Arciero, Julia ; Edenberg, Howard ; Marrs, James A. / Ethanol exposure disrupts extraembryonic microtubule cytoskeleton and embryonic blastomere cell adhesion, producing epiboly and gastrulation defects. In: Biology Open. 2013 ; Vol. 2, No. 10. pp. 1013-1021.
@article{8f41070135c0416fa760e14b5005d687,
title = "Ethanol exposure disrupts extraembryonic microtubule cytoskeleton and embryonic blastomere cell adhesion, producing epiboly and gastrulation defects",
abstract = "Fetal alcohol spectrum disorder (FASD) occurs when pregnant mothers consume alcohol, causing embryonic ethanol exposure and characteristic birth defects that include craniofacial, neural and cardiac defects. Gastrulation is a particularly sensitive developmental stage for teratogen exposure, and zebrafish is an outstanding model to study gastrulation and FASD. Epiboly (spreading blastomere cells over the yolk cell), prechordal plate migration and convergence/extension cell movements are sensitive to early ethanol exposure. Here, experiments are presented that characterize mechanisms of ethanol toxicity on epiboly and gastrulation. Epiboly mechanisms include blastomere radial intercalation cell movements and yolk cell microtubule cytoskeleton pulling the embryo to the vegetal pole. Both of these processes were disrupted by ethanol exposure. Ethanol effects on cell migration also indicated that cell adhesion was affected, which was confirmed by cell aggregation assays. E-cadherin cell adhesion molecule expression was not affected by ethanol exposure, but E-cadherin distribution, which controls epiboly and gastrulation, was changed. E-cadherin was redistributed into cytoplasmic aggregates in blastomeres and dramatically redistributed in the extraembryonic yolk cell. Gene expression microarray analysis was used to identify potential causative factors for early development defects, and expression of the cell adhesion molecule protocadherin-18a (pcdh18a), which controls epiboly, was significantly reduced in ethanol exposed embryos. Injecting pcdh18a synthetic mRNA in ethanol treated embryos partially rescued epiboly cell movements, including enveloping layer cell shape changes. Together, data show that epiboly and gastrulation defects induced by ethanol are multifactorial, and include yolk cell (extraembryonic tissue) microtubule cytoskeleton disruption and blastomere adhesion defects, in part caused by reduced pcdh18a expression.",
keywords = "Cell adhesion, Fetal alcohol spectrum disorder, Gastrulation, Zebrafish",
author = "Swapnalee Sarmah and Pooja Muralidharan and Curtis, {Courtney L.} and Jeanette McClintick and Buente, {Bryce B.} and Holdgrafer, {David J.} and Osato Ogbeifun and Olorungbounmi, {Opeyemi C.} and Liliana Patino and Ryan Lucas and Sonya Gilbert and Groninger, {Evan S.} and Julia Arciero and Howard Edenberg and Marrs, {James A.}",
year = "2013",
month = "10",
day = "15",
doi = "10.1242/bio.20135546",
language = "English (US)",
volume = "2",
pages = "1013--1021",
journal = "Biology Open",
issn = "2046-6390",
publisher = "Company of Biologists Ltd",
number = "10",

}

TY - JOUR

T1 - Ethanol exposure disrupts extraembryonic microtubule cytoskeleton and embryonic blastomere cell adhesion, producing epiboly and gastrulation defects

AU - Sarmah, Swapnalee

AU - Muralidharan, Pooja

AU - Curtis, Courtney L.

AU - McClintick, Jeanette

AU - Buente, Bryce B.

AU - Holdgrafer, David J.

AU - Ogbeifun, Osato

AU - Olorungbounmi, Opeyemi C.

AU - Patino, Liliana

AU - Lucas, Ryan

AU - Gilbert, Sonya

AU - Groninger, Evan S.

AU - Arciero, Julia

AU - Edenberg, Howard

AU - Marrs, James A.

PY - 2013/10/15

Y1 - 2013/10/15

N2 - Fetal alcohol spectrum disorder (FASD) occurs when pregnant mothers consume alcohol, causing embryonic ethanol exposure and characteristic birth defects that include craniofacial, neural and cardiac defects. Gastrulation is a particularly sensitive developmental stage for teratogen exposure, and zebrafish is an outstanding model to study gastrulation and FASD. Epiboly (spreading blastomere cells over the yolk cell), prechordal plate migration and convergence/extension cell movements are sensitive to early ethanol exposure. Here, experiments are presented that characterize mechanisms of ethanol toxicity on epiboly and gastrulation. Epiboly mechanisms include blastomere radial intercalation cell movements and yolk cell microtubule cytoskeleton pulling the embryo to the vegetal pole. Both of these processes were disrupted by ethanol exposure. Ethanol effects on cell migration also indicated that cell adhesion was affected, which was confirmed by cell aggregation assays. E-cadherin cell adhesion molecule expression was not affected by ethanol exposure, but E-cadherin distribution, which controls epiboly and gastrulation, was changed. E-cadherin was redistributed into cytoplasmic aggregates in blastomeres and dramatically redistributed in the extraembryonic yolk cell. Gene expression microarray analysis was used to identify potential causative factors for early development defects, and expression of the cell adhesion molecule protocadherin-18a (pcdh18a), which controls epiboly, was significantly reduced in ethanol exposed embryos. Injecting pcdh18a synthetic mRNA in ethanol treated embryos partially rescued epiboly cell movements, including enveloping layer cell shape changes. Together, data show that epiboly and gastrulation defects induced by ethanol are multifactorial, and include yolk cell (extraembryonic tissue) microtubule cytoskeleton disruption and blastomere adhesion defects, in part caused by reduced pcdh18a expression.

AB - Fetal alcohol spectrum disorder (FASD) occurs when pregnant mothers consume alcohol, causing embryonic ethanol exposure and characteristic birth defects that include craniofacial, neural and cardiac defects. Gastrulation is a particularly sensitive developmental stage for teratogen exposure, and zebrafish is an outstanding model to study gastrulation and FASD. Epiboly (spreading blastomere cells over the yolk cell), prechordal plate migration and convergence/extension cell movements are sensitive to early ethanol exposure. Here, experiments are presented that characterize mechanisms of ethanol toxicity on epiboly and gastrulation. Epiboly mechanisms include blastomere radial intercalation cell movements and yolk cell microtubule cytoskeleton pulling the embryo to the vegetal pole. Both of these processes were disrupted by ethanol exposure. Ethanol effects on cell migration also indicated that cell adhesion was affected, which was confirmed by cell aggregation assays. E-cadherin cell adhesion molecule expression was not affected by ethanol exposure, but E-cadherin distribution, which controls epiboly and gastrulation, was changed. E-cadherin was redistributed into cytoplasmic aggregates in blastomeres and dramatically redistributed in the extraembryonic yolk cell. Gene expression microarray analysis was used to identify potential causative factors for early development defects, and expression of the cell adhesion molecule protocadherin-18a (pcdh18a), which controls epiboly, was significantly reduced in ethanol exposed embryos. Injecting pcdh18a synthetic mRNA in ethanol treated embryos partially rescued epiboly cell movements, including enveloping layer cell shape changes. Together, data show that epiboly and gastrulation defects induced by ethanol are multifactorial, and include yolk cell (extraembryonic tissue) microtubule cytoskeleton disruption and blastomere adhesion defects, in part caused by reduced pcdh18a expression.

KW - Cell adhesion

KW - Fetal alcohol spectrum disorder

KW - Gastrulation

KW - Zebrafish

UR - http://www.scopus.com/inward/record.url?scp=84979234404&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84979234404&partnerID=8YFLogxK

U2 - 10.1242/bio.20135546

DO - 10.1242/bio.20135546

M3 - Article

AN - SCOPUS:84979234404

VL - 2

SP - 1013

EP - 1021

JO - Biology Open

JF - Biology Open

SN - 2046-6390

IS - 10

ER -