Evidence for nuclear membrane fluidity: Proacrosome migration and nuclear pore redistribution during grasshopper spermiogenesis

Troyer, David; Schwager, Petra

doi:10.1002/cm.970020405

Cited by 11 publications

(5 citation statements)

References 29 publications

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“…Given that extensive nuclear remodeling occurs even in young cells, the reorganization of the nuclear periphery appears to be integral to gamete fitness. Importantly, the sequestration of NPCs in budding yeast meiosis is similar to a NPC reorganization event observed in the spermatogenesis of metazoans, including humans (Fawcett and Chemes, 1979; Ho, 2010; Troyer and Schwager, 1982). In this context, acrosome formation, potentially akin to gamete plasma membrane formation, corresponds to the redistribution of nuclear pores to the caudal end of the nucleus, coincident with chromatin condensation and elimination of un-inherited nuclear material.…”

Section: Discussionmentioning

confidence: 59%

Meiotic cellular rejuvenation is coupled to nuclear remodeling in budding yeast

King

Goodman

Schick

et al. 2019

eLife

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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.

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Section: Discussionmentioning

confidence: 59%

Meiotic cellular rejuvenation is coupled to nuclear remodeling in budding yeast

King

Goodman

Schick

et al. 2019

eLife

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“…Given that extensive nuclear remodeling occurs even in young cells, the reorganization of the nuclear periphery appears to be integral to gamete fitness. Importantly, the sequestration of NPCs in budding yeast meiosis is similar to a NPC reorganization event observed in the spermatogenesis of metazoans, including humans (Fawcett and Chemes, 1979;Ho, 2010;Troyer and Schwager, 1982). In this context, acrosome formation, potentially akin to gamete plasma membrane formation, corresponds to the redistribution of nuclear pores to the caudal end of the nucleus, facilitating chromatin condensation and elimination of un-inherited nuclear material.…”

Section: Nuclear Remodeling As a Driver Of Gamete Health And Rejuvenamentioning

confidence: 75%

Meiotic Cellular Rejuvenation is Coupled to Nuclear Remodeling in Budding Yeast

UÌˆnal¹,

King²,

Goodman³

et al. 2019

Preprint

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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 factorsincluding 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 old 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. 420 540 300 MergePM Nsr1 King and Goodman et al. Figure 6 -Supplement 3 PM initiation

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“…1 D). Although speculative, this hypothesis draws support from those observations which indicate that pores within the NE can undergo an MT-independent "capping" (50) and that colcemid-insensitive prophase chromosome movements occur in crane fly spermatocytes in association with the NE (25). A possible alternative mechanism for this alignment, which also involves the NE, is suggested by the following observations of Hughes-Schrader (16): (a) "At all times each fusiform body maintains its form perfectly and seems quite rigid in its movements through the nucleoplasm," and (b) "After the formation and elongation of the fusiform bodies are well advanced, a change comes over the nucleus ... the nuclear membrane seems to shrink and tighten up around the fusiform tetrad sheaths .... " On the basis of her observations, and our observation that MTs were absent and therefore not involved in the alignment process, one can postulate that all of the sheaths and their associated tetrads became passively aligned within the nucleus from forces generated by a shrinking nuclear boundary.…”

Section: Discussionmentioning

confidence: 63%

Intranuclear membranes and the formation of the first meiotic spindle in Xenos peckii (Acroschismus wheeleri) oocytes.

Rieder¹,

Nowogrodzki²

1983

The Journal of Cell Biology

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The ultrastructure of spindle formation during the first meiotic division in oocytes of the Strepsipteran insect Xenos peckii Kirby (Acroschismus wheeleri Pierce) was examined in serial thick (0.25-~m) and thin sections. During late prophase the nuclear envelope became extremely convoluted and fenestrated. At this time vesicular and tubular membrane elements permeated the nucleoplasm and formed a thin fusiform sheath, 5-7 ~m in length, around each of the randomly oriented and condensing tetrads. These membrane elements appeared to arise from the nuclear envelope and/or in association with annulate lamellae in the nuclear region. All of the individual tetrads and their associated fusiform sheaths became aligned within the nucleus subsequent to the breakdown of the nuclear envelope. Microtubules (MTs) were found associated with membranes of the meiotic apparatus only after the nuclear envelope had broken down. Kinetochores, with associated MTs, were first recognizable as electron-opaque patches on the chromosomes at this time. The fully formed metaphase arrested Xenos oocyte meiotic apparatus contained an abundance of membranes and had diffuse poles that lacked distinct polar MT organizing centers.From these observations we conclude that the apparent individual chromosomal spindles--seen in the light microscope to form around each Xenos tetrad during "intranuclear prometaphase" (Hughes-Schrader, S., 1924, J. Morphol. 39:157-197)--actually form during late prophase, lack MTs, and are therefore not complete miniature bipolar spindles, as had been commonly assumed. Thus, the unique mode of spindle formation in Xenos oocytes cannot be used to support the hypothesis that chromosomes (kinetochores) induce the polymerization of their associated MTs. Our observation that MTs appeared in association with and parallel to tubular membrane components of the Xenos meiotic apparatus after these membranes became oriented with respect to the tetrads, is consistent with the notion that membranes associated with the spindle determine the orientation of spindle MTs and also play a part in regulating their formation.In oocytes of the insect Xenos peckii Kirby (Acroschismus wheeleri Pierce; 4) the first meiotic spindle, in specimens fixed and sectioned for light microscopy, appears to arise within the nucleus from the collocation of eight randomly oriented miniature spindles, each of which initially forms in association with a single tetrad (16). This unique manner of spindle formation has been cited, through the years, as evidence to support the argument that chromosomes themselves can organize a functional bipolar spindle in the absence of extrachromosomal organizers (32,43,45,47), that spindle bipolarity is established by the kinetochores (43), and that chromosomal spindle fibers have a tendency to fuse (2). Indeed, more recently Hughes-Schrader's (16) observations on Xenos have even been extrapolated to indicate that kinetochores form their own fibers by nucleating microtubules (MTs~; 7-Abbreviations used in this paper. M...

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Evidence for nuclear membrane fluidity: Proacrosome migration and nuclear pore redistribution during grasshopper spermiogenesis

Cited by 11 publications

References 29 publications

Meiotic cellular rejuvenation is coupled to nuclear remodeling in budding yeast

Meiotic cellular rejuvenation is coupled to nuclear remodeling in budding yeast

Meiotic Cellular Rejuvenation is Coupled to Nuclear Remodeling in Budding Yeast

Intranuclear membranes and the formation of the first meiotic spindle in Xenos peckii (Acroschismus wheeleri) oocytes.

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