The stress granule RNA-binding protein TIAR-1 protects female germ cells from heat shock in Caenorhabditis elegans

Gabriela Huelgas-Morales, Carlos Giovanni Silva-García, Laura S. Salinas, David Greenstein, Rosa E. Navarro

Research output: Contribution to journalArticlepeer-review

11 Scopus citations

Abstract

In response to stressful conditions, eukaryotic cells launch an arsenal of regulatory programs to protect the proteome. One major protective response involves the arrest of protein translation and the formation of stress granules, cytoplasmic ribonucleoprotein complexes containing the conserved RNA-binding proteins TIA-1 and TIAR. The stress granule response is thought to preserve mRNA for translation when conditions improve. For cells of the germline-the immortal cell lineage required for sexual reproduction-protection from stress is critically important for perpetuation of the species, yet how stress granule regulatory mechanisms are deployed in animal reproduction is incompletely understood. Here, we show that the stress granule protein TIAR-1 protects the Caenorhabditis elegans germline from the adverse effects of heat shock. Animals containing strong loss-of-function mutations in tiar-1 exhibit significantly reduced fertility compared to the wild type following heat shock. Analysis of a heat-shock protein promoter indicates that tiar-1 mutants display an impaired heat-shock response. We observed that TIAR-1 was associated with granules in the gonad core and oocytes during several stressful conditions. Both gonad core and oocyte granules are dynamic structures that depend on translation; protein synthesis inhibitors altered their formation. Nonetheless, tiar-1 was required for the formation of gonad core granules only. Interestingly, the gonad core granules did not seem to be needed for the germ cells to develop viable embryos after heat shock. This suggests that TIAR-1 is able to protect the germline from heat stress independently of these structures.

Original languageEnglish (US)
Pages (from-to)1031-1047
Number of pages17
JournalG3: Genes, Genomes, Genetics
Volume6
Issue number4
DOIs
StatePublished - 2016

Bibliographical note

Funding Information:
We thank the members of the Navarro and Greenstein labs for their insightful comments on the development of this project. Thanks also to Jack Powers for his helpful comments on the manuscript. We also thank WormBase release WS204 (July 29, 2009) for gathering information and making it available. This work was supported by grants from PAPIIT-UNAM (Programa de Apoyo a Proyectos de Investigaci?n e Innovaci?n Tecnol?gica, Universidad Nacional Aut?noma de M?xico; IN207412 and IN207415), Consejo Nacional de Ciencia y Tecnologia (CONACyT)-MEXICO (103856-Q and 220987), and Fundaci?n Miguel Alem?n in collaboration with UNAM to R.E.N. This work was also supported by National Institutes of Health (NIH) grants GM57173 and NS095109 to D.G. G.H.M. is a doctoral student from Programa de Doctorado en Ciencias Biom?dicas, UNAM, and received fellowships 315426 and 317550 from CONACyT. G.H.M. received additional financial support from the Programa de Apoyo a los Estudios de Posgrado (PAEP) program and PAPIITUNAM (IN207415). We thank the Caenorhabditis Genetics Center (CGC), which is funded by NIH Office of Research Infrastructure Programs (P40 OD010440), and the National Bioresource Project in Japan for kindly providing some strains used in this work.

Keywords

  • C. elegans
  • Germ cells
  • Stress
  • Stress granules
  • TIA-1/TIAR

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