The fusome mediates intercellular endoplasmic reticulum connectivity in Drosophila ovarian cysts

Erik L. Snapp, Takako Iida, David Frescas, Jennifer Lippincott-Schwartz, Mary A. Lilly

Research output: Contribution to journalArticle

72 Citations (Scopus)

Abstract

Drosophila ovarian cysts arise through a series of four synchronous incomplete mitotic divisions. After each round of mitosis, a membranous organelle, the fusome, grows along the cleavage furrow and the remnants of the mitotic spindle to connect all cystocytes in a cyst. The fusome is essential for the pattern and synchrony of the mitotic cyst divisions as well as oocyte differentiation. Using live cell imaging, greenfluorescent protein-tagged proteins, and photobleaching techniques, we demonstrate that fusomal endomembranes are part of a single continuous endoplasmic reticulum (ER) that is shared by all cystocytes in dividing ovarian cysts. Membrane and lumenal proteins of the common ER freely and rapidly diffuse between cystocytes. The fusomal ER mediates intercellular ER connectivity by linking the cytoplasmic ER membranes of all cystocytes within a cyst. Before entry into meiosis and onset of oocyte differentiation (between region 1 and region 2A), ER continuity between cystocytes is lost. Furthermore, analyses of hts and Dhc64c mutants indicate that intercellular ER continuity within dividing ovarian cysts requires the fusome cytoskeletal component and suggest a possible role for the common ER in synchronizing mitotic cyst divisions.

Original languageEnglish (US)
Pages (from-to)4512-4521
Number of pages10
JournalMolecular Biology of the Cell
Volume15
Issue number10
DOIs
StatePublished - Oct 2004
Externally publishedYes

Fingerprint

Ovarian Cysts
Endoplasmic Reticulum
Drosophila
Cysts
Oocytes
Photobleaching
Spindle Apparatus
Meiosis
Mitosis
Organelles
Membrane Proteins
Proteins
Membranes

ASJC Scopus subject areas

  • Molecular Biology
  • Genetics
  • Cell Biology

Cite this

The fusome mediates intercellular endoplasmic reticulum connectivity in Drosophila ovarian cysts. / Snapp, Erik L.; Iida, Takako; Frescas, David; Lippincott-Schwartz, Jennifer; Lilly, Mary A.

In: Molecular Biology of the Cell, Vol. 15, No. 10, 10.2004, p. 4512-4521.

Research output: Contribution to journalArticle

Snapp, EL, Iida, T, Frescas, D, Lippincott-Schwartz, J & Lilly, MA 2004, 'The fusome mediates intercellular endoplasmic reticulum connectivity in Drosophila ovarian cysts', Molecular Biology of the Cell, vol. 15, no. 10, pp. 4512-4521. https://doi.org/10.1091/mbc.E04-06-0475
Snapp, Erik L. ; Iida, Takako ; Frescas, David ; Lippincott-Schwartz, Jennifer ; Lilly, Mary A. / The fusome mediates intercellular endoplasmic reticulum connectivity in Drosophila ovarian cysts. In: Molecular Biology of the Cell. 2004 ; Vol. 15, No. 10. pp. 4512-4521.
@article{d2acdb4e47b94053947d4df8409af8dc,
title = "The fusome mediates intercellular endoplasmic reticulum connectivity in Drosophila ovarian cysts",
abstract = "Drosophila ovarian cysts arise through a series of four synchronous incomplete mitotic divisions. After each round of mitosis, a membranous organelle, the fusome, grows along the cleavage furrow and the remnants of the mitotic spindle to connect all cystocytes in a cyst. The fusome is essential for the pattern and synchrony of the mitotic cyst divisions as well as oocyte differentiation. Using live cell imaging, greenfluorescent protein-tagged proteins, and photobleaching techniques, we demonstrate that fusomal endomembranes are part of a single continuous endoplasmic reticulum (ER) that is shared by all cystocytes in dividing ovarian cysts. Membrane and lumenal proteins of the common ER freely and rapidly diffuse between cystocytes. The fusomal ER mediates intercellular ER connectivity by linking the cytoplasmic ER membranes of all cystocytes within a cyst. Before entry into meiosis and onset of oocyte differentiation (between region 1 and region 2A), ER continuity between cystocytes is lost. Furthermore, analyses of hts and Dhc64c mutants indicate that intercellular ER continuity within dividing ovarian cysts requires the fusome cytoskeletal component and suggest a possible role for the common ER in synchronizing mitotic cyst divisions.",
author = "Snapp, {Erik L.} and Takako Iida and David Frescas and Jennifer Lippincott-Schwartz and Lilly, {Mary A.}",
year = "2004",
month = "10",
doi = "10.1091/mbc.E04-06-0475",
language = "English (US)",
volume = "15",
pages = "4512--4521",
journal = "Molecular Biology of the Cell",
issn = "1059-1524",
publisher = "American Society for Cell Biology",
number = "10",

}

TY - JOUR

T1 - The fusome mediates intercellular endoplasmic reticulum connectivity in Drosophila ovarian cysts

AU - Snapp, Erik L.

AU - Iida, Takako

AU - Frescas, David

AU - Lippincott-Schwartz, Jennifer

AU - Lilly, Mary A.

PY - 2004/10

Y1 - 2004/10

N2 - Drosophila ovarian cysts arise through a series of four synchronous incomplete mitotic divisions. After each round of mitosis, a membranous organelle, the fusome, grows along the cleavage furrow and the remnants of the mitotic spindle to connect all cystocytes in a cyst. The fusome is essential for the pattern and synchrony of the mitotic cyst divisions as well as oocyte differentiation. Using live cell imaging, greenfluorescent protein-tagged proteins, and photobleaching techniques, we demonstrate that fusomal endomembranes are part of a single continuous endoplasmic reticulum (ER) that is shared by all cystocytes in dividing ovarian cysts. Membrane and lumenal proteins of the common ER freely and rapidly diffuse between cystocytes. The fusomal ER mediates intercellular ER connectivity by linking the cytoplasmic ER membranes of all cystocytes within a cyst. Before entry into meiosis and onset of oocyte differentiation (between region 1 and region 2A), ER continuity between cystocytes is lost. Furthermore, analyses of hts and Dhc64c mutants indicate that intercellular ER continuity within dividing ovarian cysts requires the fusome cytoskeletal component and suggest a possible role for the common ER in synchronizing mitotic cyst divisions.

AB - Drosophila ovarian cysts arise through a series of four synchronous incomplete mitotic divisions. After each round of mitosis, a membranous organelle, the fusome, grows along the cleavage furrow and the remnants of the mitotic spindle to connect all cystocytes in a cyst. The fusome is essential for the pattern and synchrony of the mitotic cyst divisions as well as oocyte differentiation. Using live cell imaging, greenfluorescent protein-tagged proteins, and photobleaching techniques, we demonstrate that fusomal endomembranes are part of a single continuous endoplasmic reticulum (ER) that is shared by all cystocytes in dividing ovarian cysts. Membrane and lumenal proteins of the common ER freely and rapidly diffuse between cystocytes. The fusomal ER mediates intercellular ER connectivity by linking the cytoplasmic ER membranes of all cystocytes within a cyst. Before entry into meiosis and onset of oocyte differentiation (between region 1 and region 2A), ER continuity between cystocytes is lost. Furthermore, analyses of hts and Dhc64c mutants indicate that intercellular ER continuity within dividing ovarian cysts requires the fusome cytoskeletal component and suggest a possible role for the common ER in synchronizing mitotic cyst divisions.

UR - http://www.scopus.com/inward/record.url?scp=4644287432&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=4644287432&partnerID=8YFLogxK

U2 - 10.1091/mbc.E04-06-0475

DO - 10.1091/mbc.E04-06-0475

M3 - Article

C2 - 15292454

AN - SCOPUS:4644287432

VL - 15

SP - 4512

EP - 4521

JO - Molecular Biology of the Cell

JF - Molecular Biology of the Cell

SN - 1059-1524

IS - 10

ER -