Catastrophic nuclear envelope collapse in cancer cell micronuclei
Open accessAbstract
During mitotic exit, missegregated chromosomes can recruit their own nuclear envelope (NE) to form micronuclei (MN). MN have reduced functioning compared to primary nuclei in the same cell, although the two compartments appear to be structurally comparable. Here we show that over 60% of MN undergo an irreversible loss of compartmentalization during interphase due to NE collapse. This disruption of the MN, which is induced by defects in nuclear lamina assembly, drastically reduces nuclear functions and can trigger massive DNA damage. MN disruption is associated with chromatin compaction and invasion of endoplasmic reticulum (ER) tubules into the chromatin. We identified disrupted MN in both major subtypes of human non-small-cell lung cancer, suggesting that disrupted MN could be a useful objective biomarker for genomic instability in solid tumors. Our study shows that NE collapse is a key event underlying MN dysfunction and establishes a link between aberrant NE organization and aneuploidy.
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Suppressing micronuclear envelope rupture through mCherry-Lamin B2 overexpression reduced cytosolic dsDNA staining without influencing chromosome segregation errors.
“Suppressing micronuclear envelope rupture through mCherry-Lamin B2 overexpression20 reduced cytosolic dsDNA staining without influencing chromosome segregation errors.”
From Chromosomal instability drives metastasis through a cytosolic DNA response (2018) · cites this paper as [20]
The Results section, “NE collapse is triggered by lamin disorganization” (page unavailable), reports that LmnB2 expression increased the proportion of intact micronuclei. It does not report reduced cytosolic dsDNA staining or test whether LmnB2 overexpression affects chromosome segregation errors. A separate Results passage finds no significant effect of micronuclear disruption on micronucleus formation after a second mitosis, but that is not the stated overexpression comparison. (LLM, conf=0.88)
Experimental — accuracy not yet measuredImpeding micronuclear rupture through Lamin B2 overexpression significantly diminished the relative fraction of cGAS+ micronuclei.
“Impeding micronuclear rupture through Lamin B2 overexpression20 significantly diminished the relative fraction of cGAS+ micronuclei (Fig. 6a–b).”
From Chromosomal instability drives metastasis through a cytosolic DNA response (2018) · cites this paper as [20]
Defective nuclear envelope assembly in MN impairs replication and repair of MN DNA.
“which affects many processes in MN, including defective replication and repair of MN DNA (Crasta et al., 2012; Hatch et al., 2013; Umbreit et al., 2020; Zhang et al., 2015).”
From Cytoplasmic DNA: sources, sensing, and role in aging and disease (2021) · cites this paper as Hatch et al., 2013
MN are initially enclosed by a nuclear envelope, but this envelope can spontaneously lose integrity and rupture.
“MN are initially surrounded by a nuclear envelope which compartmentalizes MN away from the cytoplasm; however, the integrity of this nuclear envelope can be spontaneously lost, leading to rupture (Hatch et al., 2013) (Fig. 1B).”
From Cytoplasmic DNA: sources, sensing, and role in aging and disease (2021) · cites this paper as Hatch et al., 2013
Knockdown of Lamin B1 drives formation of CCF-like foci.
“Knockdown of Lamin B1 is known to drive CCF-like foci formation (Hatch et al., 2013), while the overexpression of Lamin B1 delays onset of senescence (Shimi et al., 2011), suggesting that Lamin B1 loss may be upstream of CCF formation.”
From Cytoplasmic DNA: sources, sensing, and role in aging and disease (2021) · cites this paper as Hatch et al., 2013
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- Authors
- Hatch, E. M., Fischer, A. H., Deerinck, T. J., & Hetzer, M. W.
- Affiliations
- Salk Institute for Biological Studies (US)
- University of Massachusetts Chan Medical School (US)
- University of California San Diego (US)
- Corresponding author
- Hetzer, Martin W.
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2013-07
- Volume
- 154
- Issue
- 1
- Pages
- 47-60
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC3749778
- OpenAlex
- W2077145482
- Cited by
- 741
- References
- 51
- Citations by year
- 2026: 52 · 2025: 70 · 2024: 69 · 2023: 69 · 2022: 78 · 2021: 76 · 2020: 81 · 2019: 49 · 2018: 65 · 2017: 39 · 2016: 40 · 2015: 29 · 2014: 19 · 2013: 5
- FWCI
- 13.87
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Cancer Institute (P30CA014118195, P30CA014195)
- National Institute of General Medical Sciences (R01GM098749, P41GM103412, GM103412)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nuclear Structure and Function
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Microtubule and mitosis dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
- Keywords
- micronuclei, non-small cell lung cancer, genomic instability, aneuploidy, chromatin condensation, DNA damage, nuclear compartmentalization, biomarkers
- MeSH terms
- Carcinoma, Non-Small-Cell Lung, Cell Nucleus, DNA Damage, Humans, Interphase, Lung Neoplasms, Nuclear Envelope, Lamins, Genomic Instability, Cell Line, Tumor, Micronuclei, Chromosome-Defective
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