Developmental expression of FOG‐1/CPEB protein and its control in the <i>Caenorhabditis elegans</i> hermaphrodite germ line

Lamont, Liana B.; Kimble, Judith

doi:10.1002/dvdy.21081

Cited by 26 publications

(23 citation statements)

References 56 publications

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“…In addition, there is a direct correlation between the similarity of the predicted binding elements to the 5BE and the affinity with which PUF-5 is able to bind the site. We identified a potential target (fog-1), which has known roles in regulating cell fate decisions in the germline (Barton and Kimble 1990;Luitjens et al 2000;Thompson et al 2005;Lamont and Kimble 2007), consistent with roles for PUF-5/-6/-7 in the germline. From the candidate mRNA targets we identified, other roles for PUF-5/-6/-7 can be inferred.…”

Section: Discussionmentioning

confidence: 52%

A Caenorhabditis elegans PUF protein family with distinct RNA binding specificity

Stumpf

Kimble²,

Wickens³

2008

RNA

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PUF proteins comprise a highly conserved family of sequence-specific RNA binding proteins that regulate target mRNAs via binding directly to their 39UTRs. The Caenorhabditis elegans genome encodes several PUF proteins, which cluster into four groups based on sequence similarity; all share amino acids that interact with the RNA in the cocrystal of human Pumilio with RNA. Members of the FBF and the PUF-8/9 groups bind different but related RNA sequences. We focus here on the binding specificity of representatives of a third cluster, comprising PUF-5, -6, and -7. We performed in vivo selection experiments using the yeast three-hybrid system to identify RNA sequences that bind PUF-5 and PUF-6, and we confirmed binding to optimal sites in vitro. The consensus sequences derived from the screens are similar for PUF-5 and PUF-6 but differ from those of the FBF or PUF-8/-9 groups. Similarly, neither PUF-5 nor PUF-6 bind the recognition sites preferred by the other clusters. Mutagenesis studies confirmed the unique RNA specificity of PUF-5/-6. Using the PUF-5 consensus derived from our experiments, we searched a database of C. elegans 39UTRs to identify potential targets of PUF-5, several of which indeed bind PUF-5. Therefore the consensus has predictive value and provides a route to finding genuine targets of these proteins.

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Section: Discussionmentioning

confidence: 52%

A Caenorhabditis elegans PUF protein family with distinct RNA binding specificity

Stumpf

Kimble²,

Wickens³

2008

RNA

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“…3E), changing from a typical spermatogenic pattern to a typical oogenic pattern of FOG-1 expression (22). Finally, the oocyte-promoting GLD-1 protein expanded dramatically within 8 h of treatment from a small patch at the MZ/TZ border in DMSO-treated germ lines to a large area extending into the pachytene zone of U0126-treated germ lines (Fig.…”

Section: Key Sperm-oocyte Fate Regulators Change Abundance Upon Chemicalmentioning

confidence: 89%

Mitosis–meiosis and sperm–oocyte fate decisions are separable regulatory events

Morgan

Noble

Kimble

2013

Proc. Natl. Acad. Sci. U.S.A.

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Germ cell fate decisions are poorly understood, despite their central role in reproduction. One fundamental question has been whether germ cells are regulated to enter the meiotic cell cycle (i.e., mitosis–meiosis decision) and to be sperm or oocyte (i.e., sperm–oocyte decision) through one or two cell fate choices. If a single decision is used, a male-specific or female-specific meiotic entry would lead necessarily toward spermatogenesis or oogenesis, respectively. If two distinct decisions are used, meiotic entry should be separable from specification as sperm or oocyte. Here, we investigate the relationship of these two decisions with tools uniquely available in the nematode Caenorhabditis elegans . Specifically, we used a temperature-sensitive Notch allele to drive germ-line stem cells into the meiotic cell cycle, followed by chemical inhibition of the Ras/ERK pathway to reprogram the sperm–oocyte decision. We found that germ cells already in meiotic prophase can nonetheless be sexually transformed from a spermatogenic to an oogenic fate. This finding cleanly uncouples the mitosis–meiosis decision from the sperm–oocyte decision. In addition, we show that chemical reprogramming occurs in a germ-line region where germ cells normally transition from the mitotic to the meiotic cell cycle and that it dramatically changes the abundance of key sperm–oocyte fate regulators in meiotic germ cells. We conclude that the C . elegans mitosis–meiosis and sperm–oocyte decisions are separable regulatory events and suggest that this fundamental conclusion will hold true for germ cells throughout the animal kingdom.

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“…Their most direct regulators are the FBF RNA-binding protein (Thompson et al 2005) and TRA-1/GLI, a conserved transcription factor and regulator of nuclear export (Zarkower & Hodgkin 1992, Chen & Ellis 2000, Jin et al 2001, Segal et al 2001, Lamont & Kimble 2007. FBF promotes oogenesis by repressing fog-1, fog-3, and fem-3 mRNAs (Figure 5a) (Zhang et al 1997, Thompson et al 2005 Regulation of the sperm/oocyte decision.…”

Section: Regulators Of the Sperm/oocyte Decisionmentioning

confidence: 95%

“…Deletions of single components of the network do not eliminate the switch but instead shift its position in the gonad. For example, in fbf-1 single mutants, the switch occurs closer to the DTC than in wild type because fewer germ cells than normal are maintained in mitosis (Crittenden et al 2002, Lamont & Kimble 2007. In gld-2 and gld-3 single mutants, more germ cells than normal occupy the mitotic region, and the switch occurs further from the DTC, suggesting that removal of the GLD-2/GLD-3 branch makes the switch less efficient (Eckmann et al 2004).…”

Section: A Regulatory Network Controls the Balance Between Proliferatmentioning

confidence: 98%

Controls of Germline Stem Cells, Entry into Meiosis, and the Sperm/Oocyte Decision inCaenorhabditis elegans

Kimble

Crittenden

2007

Annu. Rev. Cell Dev. Biol.

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440

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The Caenorhabditis elegans germ line provides an exceptional model for analysis of the molecular controls governing stem cell maintenance, the cell cycle transition from mitosis to meiosis, and the choice of sexual identity-sperm or oocyte. Germline stem cells are maintained in an undifferentiated state within a well-defined niche formed by a single somatic cell, the distal tip cell (DTC). In both sexes, the DTC employs GLP-1/Notch signaling and FBF/PUF RNA-binding proteins to maintain stem cells and promote mitotic divisions, three additional RNA regulators (GLD-1/quaking, GLD-2/poly(A) polymerase, and GLD-3/Bicaudal-C) control entry into meiosis, and FOG-1/CPEB and FOG-3/Tob proteins govern sperm specification. These key regulators are part of a robust regulatory network that controls germ cell proliferation, stem cell maintenance, and sex determination. Parallels with controls in other organisms include the use of PUF proteins for stem cell maintenance and the prominence of mRNA regulation for the control of germline development.

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Developmental expression of FOG‐1/CPEB protein and its control in the Caenorhabditis elegans hermaphrodite germ line

Cited by 26 publications

References 56 publications

A Caenorhabditis elegans PUF protein family with distinct RNA binding specificity

A Caenorhabditis elegans PUF protein family with distinct RNA binding specificity

Mitosis–meiosis and sperm–oocyte fate decisions are separable regulatory events

Controls of Germline Stem Cells, Entry into Meiosis, and the Sperm/Oocyte Decision inCaenorhabditis elegans

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