Major sperm protein signaling promotes oocyte microtubule reorganization prior to fertilization in Caenorhabditis elegans

Harris, Jana E.; Govindan, J. Amaranath; Yamamoto, Ikuko; Schwartz, Janet; Kaverina, Irina; Greenstein, David

doi:10.1016/j.ydbio.2006.07.013

Cited by 60 publications

(67 citation statements)

References 59 publications

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“…MSP stimulates oocyte maturation, ovulation, and contraction of gonadal sheath cells and reorganizes oocyte microtubules (18,46). Thus it is possible that suppression of MSP function could be involved in the signals that enhance anoxia response.…”

Section: Discussionmentioning

confidence: 99%

Reduction in ovulation or male sex phenotype increases long-term anoxia survival in adaf-16-independent manner inCaenorhabditis elegans

Mendenhall

LeBlanc

Mohan

et al. 2009

Physiological Genomics

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Mendenhall AR, LeBlanc MG, Mohan DP, Padilla PA. Reduction in ovulation or male sex phenotype increases long-term anoxia survival in a daf-16-independent manner in Caenorhabditis elegans. Physiol Genomics 36: 167-178, 2009. First published December 2, 2008 doi:10.1152/physiolgenomics.90278.2008.-Identifying genotypes and phenotypes that enhance an organism's ability to survive stress is of interest. We used Caenorhabditis elegans mutants, RNA interference (RNAi), and the chemical 5-fluorodeoxyuridine (FUDR) to test the hypothesis that a reduction in progeny would increase oxygen deprivation (anoxia) survival. In the hermaphrodite gonad, germ line processes such as spermatogenesis and oogenesis can be simultaneously as well as independently disrupted by genetic mutations. We analyzed genetic mutants [glp-1(q158), glp-4(bn2ts), plc-1(rx1), ksr-1(ku68), fog-2(q71), fem-3(q20), spe-9(hc52ts), fer-15(hc15ts)] with reduced progeny production due to various reproductive defects. Furthermore, we used RNAi to inhibit the function of gene products in the RTK/Ras/MAPK signaling pathway, which is known to be involved in a variety of developmental processes including gonad function. We determined that reduced progeny production or complete sterility enhanced anoxia survival except in the case of sterile hermaphrodites [spe-9(hc52ts), fer-15(hc15ts)] undergoing oocyte maturation and ovulation as exhibited by the presence of laid unfertilized oocytes. Furthermore, the fog-2(q71) long-term anoxia survival phenotype was suppressed when oocyte maturation and ovulation were induced by mating with males that have functional or nonfunctional sperm. The mutants with a reduced progeny production survive long-term anoxia in a daf-16-and hif-1-independent manner. Finally, we determined that wild-type males were able to survive long-term anoxia in a daf-16-independent manner. Together, these results suggest that the insulin signaling pathway is not the only mechanism to survive oxygen deprivation and that altering gonad function, in particular oocyte maturation and ovulation, leads to a physiological state conducive for oxygen deprivation survival. oxygen deprivation; germ line; insulin-like signaling; stress; anoxia METAZOANS INHABITING aquatic or subterranean ecosystems have evolved mechanisms to survive changes in oxygen levels. For example, repression of energy-requiring processes or reallocation of metabolism increases oxygen deprivation survival (21). Although most terrestrial organisms live in environments where the oxygen tension does not fluctuate much, they do have the capacity to sense and respond to oxygen deprivation. In humans, oxygen deprivation is central to various health conditions including myocardial infarction, stroke, blood loss, pulmonary disorders, and solid tumor progression (37, 62). Thus identifying the molecular mechanisms that govern metazoan response to and survival of oxygen deprivation is of great interest.Oxygen deprivation tolerance spans across various phyla (7,20,53,55,68). The comparison of oxygen d...

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Section: Discussionmentioning

confidence: 99%

Reduction in ovulation or male sex phenotype increases long-term anoxia survival in adaf-16-independent manner inCaenorhabditis elegans

Mendenhall

LeBlanc

Mohan

et al. 2009

Physiological Genomics

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“…C. elegans females, which are mutant hermaphrodites that cannot produce sperm, have been used for these injection assays. MSP induces four events that accompany and facilitate ovulation and fertilization: oocyte maturation, microtubule reorganization in the oocyte undergoing maturation, actin-based cytoplasmic streaming that promotes oocyte growth prior to meiotic arrest, and gonadal sheath cell contractions that promote ovulation (Miller et al 2001;Harris et al 2006;Govindan et al 2009). …”

Section: Developmental Control Of Oocyte Maturation and Activationmentioning

confidence: 99%

Developmental Control of Oocyte Maturation and Egg Activation in Metazoan Models

Stetina

Orr‐Weaver

2011

Cold Spring Harbor Perspectives in Biology

172

128

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“…The VAB-1 MSP/EPH receptor negatively modulates oocyte meiotic maturation in the absence of sperm, and MSP counteracts this modulation (Miller et al, 2003;Cheng et al, 2008). Antagonistic G-protein pathways function in MSP signaling Harris et al, 2006) and regulate the trafficking of VAB-1 in the oocyte (Cheng et al, 2008).…”

Section: Introductionmentioning

confidence: 99%

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

et al. 2009

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Soma-germline interactions control fertility at many levels, including stem cell proliferation, meiosis and gametogenesis, yet the nature of these fundamental signaling mechanisms and their potential evolutionary conservation are incompletely understood. In C. elegans, a sperm-sensing mechanism regulates oocyte meiotic maturation and ovulation, tightly coordinating sperm availability and fertilization. Sperm release the major sperm protein (MSP) signal to trigger meiotic resumption (meiotic maturation) and to promote contraction of the follicle-like gonadal sheath cells that surround oocytes. Using genetic mosaic analysis, we show that all known MSP-dependent meiotic maturation events in the germline require Gα s -adenylate cyclase signaling in the gonadal sheath cells. We show that the MSP hormone promotes the sustained actomyosin-dependent cytoplasmic streaming that drives oocyte growth. Furthermore, we demonstrate that efficient oocyte production and cytoplasmic streaming require Gα s -adenylate cyclase signaling in the gonadal sheath cells, thereby providing a somatic mechanism that coordinates oocyte growth and meiotic maturation with sperm availability. We present genetic evidence that MSP and Gα s -adenylate cyclase signaling regulate oocyte growth and meiotic maturation in part by antagonizing gap-junctional communication between sheath cells and oocytes. In the absence of MSP or Gα s -adenylate cyclase signaling, MSP binding sites are enriched and appear clustered on sheath cells. We discuss these results in the context of a model in which the sheath cells function as the major initial sensor of MSP, potentially via multiple classes of G-protein-coupled receptors. Our findings highlight a remarkable similarity between the regulation of meiotic resumption by soma-germline interactions in C. elegans and mammals.

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Major sperm protein signaling promotes oocyte microtubule reorganization prior to fertilization in Caenorhabditis elegans

Cited by 60 publications

References 59 publications

Reduction in ovulation or male sex phenotype increases long-term anoxia survival in adaf-16-independent manner inCaenorhabditis elegans

Reduction in ovulation or male sex phenotype increases long-term anoxia survival in adaf-16-independent manner inCaenorhabditis elegans

Developmental Control of Oocyte Maturation and Egg Activation in Metazoan Models

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

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