Meiotic cellular rejuvenation is coupled to nuclear remodeling in budding yeast

Grant A. King, Jay S. Goodman, Jennifer G. Schick, Keerthana Chetlapalli, Danielle Jorgens, Kent L. McDonald, Elçin Ünal

Research output: Contribution to journalArticle

1 Citation (Scopus)

Abstract

Production of healthy gametes in meiosis relies on the quality control and proper distribution of both nuclear and cytoplasmic contents. Meiotic differentiation naturally eliminates age-induced cellular damage by an unknown mechanism. Using time-lapse fluorescence microscopy in budding yeast, we found that nuclear senescence factors - including protein aggregates, extrachromosomal ribosomal DNA circles, and abnormal nucleolar material - are sequestered away from chromosomes during meiosis II and subsequently eliminated. A similar sequestration and elimination process occurs for the core subunits of the nuclear pore complex in both young and aged cells. Nuclear envelope remodeling drives the formation of a membranous compartment containing the sequestered material. Importantly, de novo generation of plasma membrane is required for the sequestration event, preventing the inheritance of long-lived nucleoporins and senescence factors into the newly formed gametes. Our study uncovers a new mechanism of nuclear quality control and provides insight into its function in meiotic cellular rejuvenation.

Original languageEnglish (US)
JournaleLife
Volume8
DOIs
StatePublished - Aug 9 2019

Fingerprint

Rejuvenation
Saccharomycetales
Meiosis
Germ Cells
Quality Control
Yeast
Quality control
Nuclear Pore Complex Proteins
Nuclear Pore
Fluorescence microscopy
Nuclear Envelope
Cell membranes
Chromosomes
Ribosomal DNA
Fluorescence Microscopy
Cell Membrane
Protein Aggregates

Keywords

  • aging
  • cell biology
  • meiosis
  • nuclear pore complex
  • nucleolus
  • protein aggregation
  • quality control
  • S. cerevisiae

ASJC Scopus subject areas

  • Neuroscience(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Immunology and Microbiology(all)

Cite this

King, G. A., Goodman, J. S., Schick, J. G., Chetlapalli, K., Jorgens, D., McDonald, K. L., & Ünal, E. (2019). Meiotic cellular rejuvenation is coupled to nuclear remodeling in budding yeast. eLife, 8. https://doi.org/10.7554/eLife.47156

Meiotic cellular rejuvenation is coupled to nuclear remodeling in budding yeast. / King, Grant A.; Goodman, Jay S.; Schick, Jennifer G.; Chetlapalli, Keerthana; Jorgens, Danielle; McDonald, Kent L.; Ünal, Elçin.

In: eLife, Vol. 8, 09.08.2019.

Research output: Contribution to journalArticle

King, GA, Goodman, JS, Schick, JG, Chetlapalli, K, Jorgens, D, McDonald, KL & Ünal, E 2019, 'Meiotic cellular rejuvenation is coupled to nuclear remodeling in budding yeast', eLife, vol. 8. https://doi.org/10.7554/eLife.47156
King GA, Goodman JS, Schick JG, Chetlapalli K, Jorgens D, McDonald KL et al. Meiotic cellular rejuvenation is coupled to nuclear remodeling in budding yeast. eLife. 2019 Aug 9;8. https://doi.org/10.7554/eLife.47156
King, Grant A. ; Goodman, Jay S. ; Schick, Jennifer G. ; Chetlapalli, Keerthana ; Jorgens, Danielle ; McDonald, Kent L. ; Ünal, Elçin. / Meiotic cellular rejuvenation is coupled to nuclear remodeling in budding yeast. In: eLife. 2019 ; Vol. 8.
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