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Forever young: the key to rejuvenation during gametogenesis

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Abstract

Cell aging is the result of deteriorating competence in maintaining cellular homeostasis and quality control. Certain cell types are able to rejuvenate through asymmetric cell division by excluding aging factors, including damaged cellular compartments and extrachromosomal rDNA circles, from entering the daughter cell. Recent findings from the budding yeast S. cerevisiae have shown that gametogenesis represents another type of cellular rejuvenation. Gametes, whether produced by an old or a young mother cell, are granted a renewed replicative lifespan through the formation of a fifth nuclear compartment that sequesters the harmful senescence factors accumulated by the mother. Here, we describe the importance and mechanism of cellular remodeling at the nuclear envelope mediated by ESCRT-III and the LEM-domain proteins, with a focus on nuclear pore biogenesis and chromatin interaction during gamete rejuvenation.

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References

  • Arai K, Sato M, Tanaka K, Yamamoto M (2010) Nuclear compartmentalization is abolished during fission yeast meiosis. Curr Biol 20:1913–1918

    Article  CAS  Google Scholar 

  • Asakawa H, Kojidani T, Mori C, Osakada H, Sato M, Ding DQ, Hiraoka Y, Haraguchi T (2010) Virtual breakdown of the nuclear envelope in fission yeast meiosis. Curr Biol 20:1919–1925

    Article  CAS  Google Scholar 

  • Beck M, Hurt E (2017) The nuclear pore complex: understanding its function through structural insight. Nat Rev Mol Cell Biol 18:73–89

    Article  CAS  Google Scholar 

  • Chu S, DeRisi J, Eisen M, Mulholland J, Botstein D, Brown PO, Herskowitz I (1998) The transcriptional program of sporulation in budding yeast. Science 282:699–705

    Article  CAS  Google Scholar 

  • Colombi P, Webster BM, Frohlich F, Lusk CP (2013) The transmission of nuclear pore complexes to daughter cells requires a cytoplasmic pool of Nsp1. J Cell Biol 203:215–232

    Article  CAS  Google Scholar 

  • Dey G, Culley S, Curran S, Schmidt U, Henriques R, Kukulski W, Baum B (2020) Closed mitosis requires local disassembly of the nuclear envelope. Nature 585:119–123

    Article  CAS  Google Scholar 

  • Dultz E, Zanin E, Wurzenberger C, Braun M, Rabut G, Sironi L, Ellenberg J (2008) Systematic kinetic analysis of mitotic dis- and reassembly of the nuclear pore in living cells. J Cell Biol 180:857–865

    Article  CAS  Google Scholar 

  • Fernandez-Alvarez A, Bez C, O’Toole ET, Morphew M, Cooper JP (2016) Mitotic nuclear envelope breakdown and spindle nucleation are controlled by interphase contacts between centromeres and the nuclear envelope. Dev Cell 39:544–559

    Article  CAS  Google Scholar 

  • Fuchs J, Loidl J (2004) Behaviour of nucleolus organizing regions (NORs) and nucleoli during mitotic and meiotic divisions in budding yeast. Chromosome Res 12:427–438

    Article  CAS  Google Scholar 

  • Grund SE, Fischer T, Cabal GG, Antunez O, Perez-Ortin JE, Hurt E (2008) The inner nuclear membrane protein Src1 associates with subtelomeric genes and alters their regulated gene expression. J Cell Biol 182:897–910

    Article  CAS  Google Scholar 

  • Kaeberlein M (2010) Lessons on longevity from budding yeast. Nature 464:513–519

    Article  CAS  Google Scholar 

  • Kim SJ, Fernandez-Martinez J, Nudelman I, Shi Y, Zhang W, Raveh B, Herricks T, Slaughter BD, Hogan JA, Upla P, Chemmama IE, Pellarin R, Echeverria I, Shivaraju M, Chaudhury AS, Wang J, Williams R, Unruh JR, Greenberg CH, Jacobs EY, Yu Z, de la Cruz MJ, Mironska R, Stokes DL, Aitchison JD, Jarrold MF, Gerton JL, Ludtke SJ, Akey CW, Chait BT, Sali A, Rout MP (2018) Integrative structure and functional anatomy of a nuclear pore complex. Nature 555:475–482

    Article  CAS  Google Scholar 

  • King GA, Unal E (2020) The dynamic nuclear periphery as a facilitator of gamete health and rejuvenation. Curr Genet 8:1–7

    Article  Google Scholar 

  • King GA, Goodman JS, Schick JG, Chetlapalli K, Jorgens DM, McDonald KL, Unal E (2019) Meiotic cellular rejuvenation is coupled to nuclear remodeling in budding yeast. Elife 8:e47156

    Article  CAS  Google Scholar 

  • Knockenhauer KE, Schwartz TU (2016) The nuclear pore complex as a flexible and dynamic gate. Cell 164:1162–1171

    Article  CAS  Google Scholar 

  • Koch BA, Staley E, Jin H, Yu HG (2020) The ESCRT-III complex is required for nuclear pore complex sequestration and regulates gamete replicative lifespan in budding yeast meiosis. Nucleus 11:219–236

    Article  CAS  Google Scholar 

  • Longo VD, Shadel GS, Kaeberlein M, Kennedy B (2012) Replicative and chronological aging in Saccharomyces cerevisiae. Cell Metab 16:18–31

    Article  CAS  Google Scholar 

  • Makio T, Lapetina DL, Wozniak RW (2013) Inheritance of yeast nuclear pore complexes requires the Nsp1p subcomplex. J Cell Biol 203:187–196

    Article  CAS  Google Scholar 

  • Markossian S, Suresh S, Osmani AH, Osmani SA (2015) Nup2 requires a highly divergent partner, NupA, to fulfill functions at nuclear pore complexes and the mitotic chromatin region. Mol Biol Cell 26:605–621

    Article  Google Scholar 

  • Mekhail K, Seebacher J, Gygi SP, Moazed D (2008) Role for perinuclear chromosome tethering in maintenance of genome stability. Nature 456:667–670

    Article  CAS  Google Scholar 

  • Meszaros N, Cibulka J, Mendiburo MJ, Romanauska A, Schneider M, Kohler A (2015) Nuclear pore basket proteins are tethered to the nuclear envelope and can regulate membrane curvature. Dev Cell 33:285–298

    Article  CAS  Google Scholar 

  • Neiman AM (2011) Sporulation in the budding yeast Saccharomyces cerevisiae. Genetics 189:737–765

    Article  CAS  Google Scholar 

  • Pieper GH, Sprenger S, Teis D, Oliferenko S (2020) ESCRT-III/Vps4 controls heterochromatin-nuclear envelope attachments. Dev Cell 53(27–41):e26

    Google Scholar 

  • Sinclair D, Mills K, Guarente L (1998) Aging in Saccharomyces cerevisiae. Annu Rev Microbiol 52:533–560

    Article  CAS  Google Scholar 

  • Suresh S, Markossian S, Osmani AH, Osmani SA (2017) Mitotic nuclear pore complex segregation involves Nup2 in Aspergillus nidulans. J Cell Biol 216:2813–2826

    Article  CAS  Google Scholar 

  • Thaller DJ, Allegretti M, Borah S, Ronchi P, Beck M, Lusk CP (2019) An ESCRT-LEM protein surveillance system is poised to directly monitor the nuclear envelope and nuclear transport system. Elife. 8:e45284

    Article  Google Scholar 

  • Unal E, Amon A (2011) Gamete formation resets the aging clock in yeast. Cold Spring Harb Symp Quant Biol 76:73–80

    Article  CAS  Google Scholar 

  • Unal E, Kinde B, Amon A (2011) Gametogenesis eliminates age-induced cellular damage and resets life span in yeast. Science 332:1554–1557

    Article  Google Scholar 

  • Ungricht R, Kutay U (2015) Establishment of NE asymmetry-targeting of membrane proteins to the inner nuclear membrane. Curr Opin Cell Biol 34:135–141

    Article  CAS  Google Scholar 

  • von Appen A, LaJoie D, Johnson IE, Trnka MJ, Pick SM, Burlingame AL, Ullman KS, Frost A (2020) LEM2 phase separation promotes ESCRT-mediated nuclear envelope reformation. Nature 582:115–118

    Article  Google Scholar 

  • Webster BM, Colombi P, Jager J, Lusk CP (2014) Surveillance of nuclear pore complex assembly by ESCRT-III/Vps4. Cell 159:388–401

    Article  CAS  Google Scholar 

  • Webster BM, Thaller DJ, Jager J, Ochmann SE, Borah S, Lusk CP (2016) Chm7 and Heh1 collaborate to link nuclear pore complex quality control with nuclear envelope sealing. EMBO J 35:2447–2467

    Article  CAS  Google Scholar 

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Acknowledgements

We thank Charles Badland and Jen Kennedy for their assistance. The work in authors’ lab is supported by the National Institutes of Health GM138838 and the National Science Foundation MCB1951313.

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Authors and Affiliations

  1. Department of Biological Science, Florida State University, Tallahassee, FL, 32306, USA

    Bailey A. Koch-Bojalad, Lauren Carson & Hong-Guo Yu

  2. Department of Cell and Developmental Biology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, 19104, USA

    Bailey A. Koch-Bojalad

Authors
  1. Bailey A. Koch-Bojalad
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  2. Lauren Carson
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  3. Hong-Guo Yu
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Correspondence to Hong-Guo Yu.

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Communicated by M.Kupiec.

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Koch-Bojalad, B.A., Carson, L. & Yu, HG. Forever young: the key to rejuvenation during gametogenesis. Curr Genet 67, 231–235 (2021). https://doi.org/10.1007/s00294-020-01133-4

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  • DOI: https://doi.org/10.1007/s00294-020-01133-4

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