Somatic cAMP signaling regulates MSP-dependent oocyte growth and meiotic maturation in<i>C. elegans</i>

Govindan, J. Amaranath; Nadarajan, Saravanapriah; Kim, Seongseop; Starich, Todd A; Greenstein, David

doi:10.1242/dev.034595

Cited by 88 publications

(220 citation statements)

References 42 publications

(70 reference statements)

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“…MSP signaling is known to regulate the oocyte production and development. The proximal MSP signaling works coordinately with the distal GLP-1 signaling to regulate the proper oocyte growth and function [50,51]. We thus envision that GLP-1 and MSP signaling are both subject to the miRNA regulation, and the loss of the miRNA-specific Argonaute genes leads to alterations in both signaling pathways, likely due to imbalance of these proteins, and thus affecting the fertility of the animals.…”

Section: Discussionmentioning

confidence: 99%

The microRNA pathway controls germ cell proliferation and differentiation in C. elegans

et al. 2012

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The discovery of the miRNA pathway revealed a new layer of molecular control of biological processes. To uncover new functions of this gene regulatory pathway, we undertook the characterization of the two miRNA-specific Argonaute proteins in Caenorhabditis elegans, ALG-1 and ALG-2. We first observed that the loss-of-function of alg-1 and alg-2 genes resulted in reduced progeny number. An extensive analysis of the germline of these mutants revealed a reduced mitotic region, indicating fewer proliferating germ cells. We also observed an early entry into meiosis in alg-1 and alg-2 mutant animals. We detected ALG-1 and ALG-2 protein expressions in the distal tip cell (DTC), a specialized cell located at the tip of both C. elegans gonadal arms that regulates mitosis-meiosis transition. Re-establishing the expression of alg-1 specifically in the DTC of mutant animals partially rescued the observed germline defects. Further analyses also support the implication of the miRNA pathway in gametogenesis. Interestingly, we observed that disruption of five miRNAs expressed in the DTC led to similar phenotypes. Finally, gene expression analysis of alg-1 mutant gonads suggests that the miRNA pathway is involved in the regulation of different pathways important for germline proliferation and differentiation. Collectively, our data indicate that the miRNA pathway plays a crucial role in the control of germ cell biogenesis in C. elegans.

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Section: Discussionmentioning

confidence: 99%

The microRNA pathway controls germ cell proliferation and differentiation in C. elegans

et al. 2012

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“…In the accompanying article (Govindan et al, 2009), we show that MSP signaling triggers the cytoplasmic flows that drive oocyte growth. When MSP is absent, as in mutant hermaphrodites that do not produce sperm (e.g.…”

Section: Introductionmentioning

confidence: 90%

“…fog mutant females), cytoplasmic streaming and oocyte production cease. Gα s -adenylate cyclase signaling in the gonadal sheath cells is required for all the described MSP responses in the germline, including cytoplasmic streaming (Govindan et al, 2009). Thus, MSP signaling via the gonadal sheath cells coordinately regulates the production, growth and meiotic maturation of oocytes.…”

Section: Introductionmentioning

confidence: 99%

MSP and GLP-1/Notch signaling coordinately regulate actomyosin-dependent cytoplasmic streaming and oocyte growth inC. elegans

et al. 2009

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Fertility depends on germline stem cell proliferation, meiosis and gametogenesis, yet how these key transitions are coordinated is unclear. In C. elegans, we show that GLP-1/Notch signaling functions in the germline to modulate oocyte growth when sperm are available for fertilization and the major sperm protein (MSP) hormone is present. Reduction-of-function mutations in glp-1 cause oocytes to grow abnormally large when MSP is present and Gα s -adenylate cyclase signaling in the gonadal sheath cells is active. By contrast, gain-of-function glp-1 mutations lead to the production of small oocytes. Surprisingly, proper oocyte growth depends on distal tip cell signaling involving the redundant function of GLP-1 ligands LAG-2 and APX-1. GLP-1 signaling also affects two cellular oocyte growth processes, actomyosin-dependent cytoplasmic streaming and oocyte cellularization. glp-1 reduction-of-function mutants exhibit elevated rates of cytoplasmic streaming and delayed cellularization. GLP-1 signaling in oocyte growth depends in part on the downstream function of the FBF-1/2 PUF RNA-binding proteins. Furthermore, abnormal oocyte growth in glp-1 mutants, but not the inappropriate differentiation of germline stem cells, requires the function of the cell death pathway. The data support a model in which GLP-1 function in MSP-dependent oocyte growth is separable from its role in the proliferation versus meiotic entry decision. Thus, two major germline signaling centers, distal GLP-1 activation and proximal MSP signaling, coordinate several spatially and temporally distinct processes by which germline stem cells differentiate into functional oocytes.

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“…Gametogenesis requires ongoing cooperation between the soma and germline and disruption of somatic support cells can prevent the production of gametes and lead to sterility (Griswold, 1998;Korta and Hubbard, 2010;Zoller and Schulz, 2012). The soma provides support and instructive cues for the germline, including such roles as forming the stem cell niche that regulates germline stem cells (Kiger et al, 2001;Kimble and White, 1981;Meng et al, 2000;Xie and Spradling, 2000), providing signals that instruct the germline during gamete differentiation (Govindan et al, 2009;Kiger et al, 2000;Killian and Hubbard, 2005;Tran et al, 2000), supplying nutrients to the developing germline (Boussouar and Benahmed, 2004), and maintaining the tissue architecture required for gamete production (Tanentzapf et al, 2007;Vogl et al, 2008). Understanding soma-germline interactions is thus key to understanding gametogenesis.…”

Section: Introductionmentioning

confidence: 99%

A somatic permeability barrier around the germline is essential forDrosophilaspermatogenesis

2015

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Interactions between the soma and germline are essential for gametogenesis. In the Drosophila testis, differentiating germ cells are encapsulated by two somatic cells that surround the germline throughout spermatogenesis. chickadee (chic), the fly ortholog of Profilin, mediates soma-germline interactions. Knockdown of Chic in the soma results in sterility and severely disrupted spermatogenesis due to defective encapsulation. To study this defect further, we developed a permeability assay to analyze whether the germline is isolated from the surrounding environment by the soma. We find that germline encapsulation by the soma is, by itself, insufficient for the formation of a permeability barrier, but that such a barrier gradually develops during early spermatogenesis. Thus, germline stem cells, gonialblasts and early spermatogonia are not isolated from the outside environment. By late spermatocyte stages, however, a permeability barrier is formed by the soma. Furthermore, we find that, concomitant with formation of the permeability barrier, septate junction markers are expressed in the soma and localize to junctional sites connecting the two somatic cells that surround the germline. Importantly, knockdown of septate junction components also disrupts the permeability barrier. Finally, we show that germline differentiation is delayed when the permeability barrier is compromised. We propose that the permeability barrier around the germline serves an important regulatory function during spermatogenesis by shaping the signaling events that take place between the soma and the germline.

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Somatic cAMP signaling regulates MSP-dependent oocyte growth and meiotic maturation inC. elegans

Cited by 88 publications

References 42 publications

The microRNA pathway controls germ cell proliferation and differentiation in C. elegans

The microRNA pathway controls germ cell proliferation and differentiation in C. elegans

MSP and GLP-1/Notch signaling coordinately regulate actomyosin-dependent cytoplasmic streaming and oocyte growth inC. elegans

A somatic permeability barrier around the germline is essential forDrosophilaspermatogenesis

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