The C. Elegans VAPB homolog VPR-1 is a permissive signal for gonad development

Pauline A. Cottee; Tim Cole; Jessica Schultz; Hieu D. Hoang; Jack Vibbert; Sung Min Han; Michael A. Miller

doi:10.1242/dev.152207

The C. Elegans VAPB homolog VPR-1 is a permissive signal for gonad development

Pauline A. Cottee, Tim Cole, Jessica Schultz, Hieu D. Hoang, Jack Vibbert, Sung Min Han, Michael A. Miller

Division of Newborn Medicine

Research output: Contribution to journal › Article › peer-review

7 Scopus citations

Abstract

VAMP/synaptobrevin-associated proteins (VAPs) contain an Nterminal major sperm protein domain (MSPd) that is associated with amyotrophic lateral sclerosis. VAPs have an intracellular housekeeping function, as well as an extracellular signaling function mediated by the secretedMSPd. Herewe show that the C. elegans VAP homolog VPR-1 is essential for gonad development. vpr-1 null mutants are maternal effect sterile due to arrested gonadogenesis following embryo hatching. Somatic gonadal precursor cells and germ cells fail to proliferate fully and complete their respective differentiation programs. Maternal or zygotic vpr-1 expression is sufficient to induce gonadogenesis and fertility. Genetic mosaic and cell type-specific expression studies indicate that vpr-1 activity is important in the nervous system, germ line and intestine. VPR-1 acts in parallel to Notch signaling, a key regulator of germline stem cell proliferation and differentiation. Neuronal vpr-1 expression is sufficient for gonadogenesis induction during a limited time period shortly after hatching. These results support the model that the secreted VPR-1 MSPd acts at least in part on gonadal sheath cell precursors in L1 to early L2 stage hermaphrodites to permit gonadogenesis.

Original language	English
Pages (from-to)	2187-2199
Number of pages	13
Journal	Development (Cambridge)
Volume	144
Issue number	12
DOIs	https://doi.org/10.1242/dev.152207
State	Published - 2017

Keywords

ALS
Caenorhabditis elegans development
Gonad
MSP
Signaling
VAPB

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10.1242/dev.152207

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title = "The C. Elegans VAPB homolog VPR-1 is a permissive signal for gonad development",

abstract = "VAMP/synaptobrevin-associated proteins (VAPs) contain an Nterminal major sperm protein domain (MSPd) that is associated with amyotrophic lateral sclerosis. VAPs have an intracellular housekeeping function, as well as an extracellular signaling function mediated by the secretedMSPd. Herewe show that the C. elegans VAP homolog VPR-1 is essential for gonad development. vpr-1 null mutants are maternal effect sterile due to arrested gonadogenesis following embryo hatching. Somatic gonadal precursor cells and germ cells fail to proliferate fully and complete their respective differentiation programs. Maternal or zygotic vpr-1 expression is sufficient to induce gonadogenesis and fertility. Genetic mosaic and cell type-specific expression studies indicate that vpr-1 activity is important in the nervous system, germ line and intestine. VPR-1 acts in parallel to Notch signaling, a key regulator of germline stem cell proliferation and differentiation. Neuronal vpr-1 expression is sufficient for gonadogenesis induction during a limited time period shortly after hatching. These results support the model that the secreted VPR-1 MSPd acts at least in part on gonadal sheath cell precursors in L1 to early L2 stage hermaphrodites to permit gonadogenesis.",

keywords = "ALS, Caenorhabditis elegans development, Gonad, MSP, Signaling, VAPB",

author = "Cottee, {Pauline A.} and Tim Cole and Jessica Schultz and Hoang, {Hieu D.} and Jack Vibbert and Han, {Sung Min} and Miller, {Michael A.}",

note = "Funding Information: This project was funded by the Muscular Dystrophy Association (MDA381893 to M.A.M.) and National Institutes of Health (R01GM08105 to M.A.M.). Financial support for J.S. came from the National Science Foundation Graduate Research Fellowship Program and the University of Alabama at Birmingham Howard Hughes Medical Institute Med-Grad Program. Some strains were provided by the Caenorhabditis Genetics Center, which is funded by the National Institutes of Health Office of Research Infrastructure Programs (P40 OD010440). Deposited in PMC for immediate release. Publisher Copyright: {\textcopyright} 2017.",

year = "2017",

doi = "10.1242/dev.152207",

language = "English",

volume = "144",

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journal = "Development (Cambridge)",

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T1 - The C. Elegans VAPB homolog VPR-1 is a permissive signal for gonad development

AU - Cottee, Pauline A.

AU - Cole, Tim

AU - Schultz, Jessica

AU - Hoang, Hieu D.

AU - Vibbert, Jack

AU - Han, Sung Min

AU - Miller, Michael A.

N1 - Funding Information: This project was funded by the Muscular Dystrophy Association (MDA381893 to M.A.M.) and National Institutes of Health (R01GM08105 to M.A.M.). Financial support for J.S. came from the National Science Foundation Graduate Research Fellowship Program and the University of Alabama at Birmingham Howard Hughes Medical Institute Med-Grad Program. Some strains were provided by the Caenorhabditis Genetics Center, which is funded by the National Institutes of Health Office of Research Infrastructure Programs (P40 OD010440). Deposited in PMC for immediate release. Publisher Copyright: © 2017.

PY - 2017

Y1 - 2017

N2 - VAMP/synaptobrevin-associated proteins (VAPs) contain an Nterminal major sperm protein domain (MSPd) that is associated with amyotrophic lateral sclerosis. VAPs have an intracellular housekeeping function, as well as an extracellular signaling function mediated by the secretedMSPd. Herewe show that the C. elegans VAP homolog VPR-1 is essential for gonad development. vpr-1 null mutants are maternal effect sterile due to arrested gonadogenesis following embryo hatching. Somatic gonadal precursor cells and germ cells fail to proliferate fully and complete their respective differentiation programs. Maternal or zygotic vpr-1 expression is sufficient to induce gonadogenesis and fertility. Genetic mosaic and cell type-specific expression studies indicate that vpr-1 activity is important in the nervous system, germ line and intestine. VPR-1 acts in parallel to Notch signaling, a key regulator of germline stem cell proliferation and differentiation. Neuronal vpr-1 expression is sufficient for gonadogenesis induction during a limited time period shortly after hatching. These results support the model that the secreted VPR-1 MSPd acts at least in part on gonadal sheath cell precursors in L1 to early L2 stage hermaphrodites to permit gonadogenesis.

AB - VAMP/synaptobrevin-associated proteins (VAPs) contain an Nterminal major sperm protein domain (MSPd) that is associated with amyotrophic lateral sclerosis. VAPs have an intracellular housekeeping function, as well as an extracellular signaling function mediated by the secretedMSPd. Herewe show that the C. elegans VAP homolog VPR-1 is essential for gonad development. vpr-1 null mutants are maternal effect sterile due to arrested gonadogenesis following embryo hatching. Somatic gonadal precursor cells and germ cells fail to proliferate fully and complete their respective differentiation programs. Maternal or zygotic vpr-1 expression is sufficient to induce gonadogenesis and fertility. Genetic mosaic and cell type-specific expression studies indicate that vpr-1 activity is important in the nervous system, germ line and intestine. VPR-1 acts in parallel to Notch signaling, a key regulator of germline stem cell proliferation and differentiation. Neuronal vpr-1 expression is sufficient for gonadogenesis induction during a limited time period shortly after hatching. These results support the model that the secreted VPR-1 MSPd acts at least in part on gonadal sheath cell precursors in L1 to early L2 stage hermaphrodites to permit gonadogenesis.

KW - ALS

KW - Caenorhabditis elegans development

KW - Gonad

KW - MSP

KW - Signaling

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DO - 10.1242/dev.152207

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AN - SCOPUS:85021142711

SN - 0950-1991

VL - 144

SP - 2187

EP - 2199

JO - Development (Cambridge)

JF - Development (Cambridge)

IS - 12

ER -

The C. Elegans VAPB homolog VPR-1 is a permissive signal for gonad development

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Keywords

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