The Drosophila fragile X protein functions as a negative regulator in the orb autoregulatory pathway

Alexandre Costa; Yan Wang; Thomas C. Dockendorff; Hediye Erdjument-Bromage; Paul Tempst; Paul Schedl; Thomas A. Jongens

doi:10.1016/j.devcel.2005.01.011

The Drosophila fragile X protein functions as a negative regulator in the orb autoregulatory pathway

Alexandre Costa, Yan Wang, Thomas C. Dockendorff, Hediye Erdjument-Bromage, Paul Tempst, Paul Schedl, Thomas A. Jongens

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

81 Scopus citations

Abstract

Translational regulation of maternal mRNAs in distinct temporal and spatial patterns underlies many key decisions in developing eggs and embryos. In Drosophila, Orb is responsible for mediating the translational activation of mRNAs localized within the developing oocyte. Orb is a germline-specific RNA binding protein and is one of the founding members of the CPEB family of translational regulators. Here we show that Orb associates with the Drosophila Fragile X Mental Retardation (dFMR1) protein as part of a ribonucleoprotein complex that controls the localized translation of mRNAs in developing egg chambers. One of the key orb regulatory targets is orb mRNA, and this autoregulatory activity is critical for ensuring that Orb protein is expressed at high levels in the oocyte. We show that dFMR1 functions as a negative regulator in the orb autoregulatory circuit, downregulating orb mRNA translation.

Original language	English (US)
Pages (from-to)	331-342
Number of pages	12
Journal	Developmental cell
Volume	8
Issue number	3
DOIs	https://doi.org/10.1016/j.devcel.2005.01.011
State	Published - Mar 2005
Externally published	Yes

ASJC Scopus subject areas

Molecular Biology
General Biochemistry, Genetics and Molecular Biology
Developmental Biology
Cell Biology

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10.1016/j.devcel.2005.01.011

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title = "The Drosophila fragile X protein functions as a negative regulator in the orb autoregulatory pathway",

abstract = "Translational regulation of maternal mRNAs in distinct temporal and spatial patterns underlies many key decisions in developing eggs and embryos. In Drosophila, Orb is responsible for mediating the translational activation of mRNAs localized within the developing oocyte. Orb is a germline-specific RNA binding protein and is one of the founding members of the CPEB family of translational regulators. Here we show that Orb associates with the Drosophila Fragile X Mental Retardation (dFMR1) protein as part of a ribonucleoprotein complex that controls the localized translation of mRNAs in developing egg chambers. One of the key orb regulatory targets is orb mRNA, and this autoregulatory activity is critical for ensuring that Orb protein is expressed at high levels in the oocyte. We show that dFMR1 functions as a negative regulator in the orb autoregulatory circuit, downregulating orb mRNA translation.",

author = "Alexandre Costa and Yan Wang and Dockendorff, {Thomas C.} and Hediye Erdjument-Bromage and Paul Tempst and Paul Schedl and Jongens, {Thomas A.}",

note = "Funding Information: We thank G. Dreyfuss for anti-dFMR1 antibodies, R. Cohen for anti-Fs(1)K10 antibodies, A. Ephrussi and P. McDonald for anti-Osk antibodies, L. Lacomis for help with mass spectrometry, J. Goodhouse for technical assistance with confocal microscopy, and G. Deshpande and A. Pepper for helpful comments on the manuscript. We would especially like to thank Dr. A. Pepper for analyzing orb mRNA levels in wild-type and dfmr1 by quantitative RT-PCR and providing us with this information. A.C. was supported by a fellowship from CNPq, Brazil. Y.W. and T.C.D. were supported in part by a fellowship from the Fragile X Research Foundation (FRAXA). This work was supported by National Institutes of Health, the FRAXA Research Foundation, and the National Cancer Institute (NCI) Cancer Center Support Grant (to P.T.). ",

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T1 - The Drosophila fragile X protein functions as a negative regulator in the orb autoregulatory pathway

AU - Costa, Alexandre

AU - Wang, Yan

AU - Dockendorff, Thomas C.

AU - Erdjument-Bromage, Hediye

AU - Tempst, Paul

AU - Schedl, Paul

AU - Jongens, Thomas A.

N1 - Funding Information: We thank G. Dreyfuss for anti-dFMR1 antibodies, R. Cohen for anti-Fs(1)K10 antibodies, A. Ephrussi and P. McDonald for anti-Osk antibodies, L. Lacomis for help with mass spectrometry, J. Goodhouse for technical assistance with confocal microscopy, and G. Deshpande and A. Pepper for helpful comments on the manuscript. We would especially like to thank Dr. A. Pepper for analyzing orb mRNA levels in wild-type and dfmr1 by quantitative RT-PCR and providing us with this information. A.C. was supported by a fellowship from CNPq, Brazil. Y.W. and T.C.D. were supported in part by a fellowship from the Fragile X Research Foundation (FRAXA). This work was supported by National Institutes of Health, the FRAXA Research Foundation, and the National Cancer Institute (NCI) Cancer Center Support Grant (to P.T.).

PY - 2005/3

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N2 - Translational regulation of maternal mRNAs in distinct temporal and spatial patterns underlies many key decisions in developing eggs and embryos. In Drosophila, Orb is responsible for mediating the translational activation of mRNAs localized within the developing oocyte. Orb is a germline-specific RNA binding protein and is one of the founding members of the CPEB family of translational regulators. Here we show that Orb associates with the Drosophila Fragile X Mental Retardation (dFMR1) protein as part of a ribonucleoprotein complex that controls the localized translation of mRNAs in developing egg chambers. One of the key orb regulatory targets is orb mRNA, and this autoregulatory activity is critical for ensuring that Orb protein is expressed at high levels in the oocyte. We show that dFMR1 functions as a negative regulator in the orb autoregulatory circuit, downregulating orb mRNA translation.

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The Drosophila fragile X protein functions as a negative regulator in the orb autoregulatory pathway

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