Abstract
The nucleus is a complex organelle that hosts the genome and is essential for vital processes like DNA replication, DNA repair, transcription, and splicing. The genome is non-randomly organized in the three-dimensional space of the nucleus. This functional sub-compartmentalization was thought to be organized on the framework of nuclear matrix (NuMat), a non-chromatin scaffold that functions as a substratum for various molecular processes of the nucleus. More recently, nuclear bodies or membrane-less subcompartments of the nucleus are thought to arise due to phase separation of chromatin, RNA, and proteins. The nuclear architecture is an amalgamation of the relative organization of chromatin, epigenetic landscape, the nuclear bodies, and the nucleoskeleton in the three-dimensional space of the nucleus. During mitosis, the nucleus undergoes drastic changes in morphology to the degree that it ceases to exist as such; various nuclear components, including the envelope that defines the nucleus, disintegrate, and the chromatin acquires mitosis-specific epigenetic marks and condenses to form chromosome. Upon mitotic exit, chromosomes are decondensed, re-establish hierarchical genome organization, and regain epigenetic and transcriptional status similar to that of the mother cell. How this mitotic memory is inherited during cell division remains a puzzle. NuMat components that are a part of the mitotic chromosome in the form of mitotic chromosome scaffold (MiCS) could potentially be the seeds that guide the relative re-establishment of the epigenome, chromosome territories, and the nuclear bodies. Here, we synthesize the advances towards understanding cellular memory of nuclear architecture across mitosis and propose a hypothesis that a subset of NuMat proteome essential for nucleation of various nuclear bodies are retained in MiCS to serve as seeds of mitotic memory, thus ensuring the daughter cells re-establish the complex status of nuclear architecture similar to that of the mother cells, thereby maintaining the pre-mitotic transcriptional status.
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Abbreviations
- hnRNP:
-
Heterogenous nuclear ribonucleoprotein
- LAD:
-
Lamina-associated domains
- MiCS:
-
Mitotic chromosome scaffolds
- NuMat:
-
Nuclear matrix
- NOR:
-
Nucleolar-organizing region
- SAF-A:
-
Scaffold attachment factor A
- SAF-B:
-
Scaffold attachment factor B
- S/MARs:
-
Scaffold/matrix-associated regions
- TAD:
-
Topologically associated domains
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The authors acknowledge the members of the RKM lab and Shivakumara Manu for carefully reading the manuscript and providing critical feedback.
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Research in the RKM lab is supported by grants from the Council for Scientific and Industrial Research (MLP0139), the Government of India, and the JC Bose fellowship (GAP0466). MS is supported by DBT-SRF fellowship.
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Soujanya, M., Bihani, A., Hajirnis, N. et al. Nuclear architecture and the structural basis of mitotic memory. Chromosome Res 31, 8 (2023). https://doi.org/10.1007/s10577-023-09714-y
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DOI: https://doi.org/10.1007/s10577-023-09714-y