Nuclear pore proteins and the control of genome functions - PubMed (original) (raw)
Review
Nuclear pore proteins and the control of genome functions
Arkaitz Ibarra et al. Genes Dev. 2015.
Abstract
Nuclear pore complexes (NPCs) are composed of several copies of ∼30 different proteins called nucleoporins (Nups). NPCs penetrate the nuclear envelope (NE) and regulate the nucleocytoplasmic trafficking of macromolecules. Beyond this vital role, NPC components influence genome functions in a transport-independent manner. Nups play an evolutionarily conserved role in gene expression regulation that, in metazoans, extends into the nuclear interior. Additionally, in proliferative cells, Nups play a crucial role in genome integrity maintenance and mitotic progression. Here we discuss genome-related functions of Nups and their impact on essential DNA metabolism processes such as transcription, chromosome duplication, and segregation.
Keywords: DNA damage; mitosis; nuclear envelope; nuclear genome; nuclear pore complex; nucleoporin; transcription control.
© 2015 Ibarra and Hetzer; Published by Cold Spring Harbor Laboratory Press.
Figures
Figure 1.
NPC structure and molecular composition. Representation and predicted molecular composition of the vertebrate NPC. For the corresponding orthologs in other model organisms, see Rothballer and Kutay (2012). The NPC core scaffold and its components are represented in dark blue and light blue, the transmembrane subunits are shown in green, the cytoplasmic structures are represented in magenta, and the basket is shown in orange. Peripheral Nups showing higher mobility by FRAP, and other approaches are depicted in black.
Figure 2.
How NPC components affect genome functions. Proposed roles for NPC components in eukaryotic cells regardless of the cell cycle activity (constitutive roles/cell cycle-independent) reported in cycling cells (interphase) and during mitosis (mitosis). (1) NPCs mediate nucleocytoplasmic transport in every eukaryotic nucleus. (2–4) Nups have been proposed to participate in transcriptional regulation, promoting either transcriptional activation (green circles) or repression (red circles) independently of the proliferative status of the cell. Gene expression regulation by Nups takes place mainly at the NE-embedded NPC in yeast (2,3), while in metazoans (4), a subset of mobile Nups (see also Fig. 1) can relocate to the nuclear interior to perform the same gene regulatory functions. (5) In both compartments, Nups might influence chromatin structure or organization of the tethered regions in collaboration with other factors (pink circles). (6) In proliferating cells, NPC–chromatin contacts must be regulated (arrow) during S phase to avoid replication fork collapse. (7) NPC components might facilitate the repair of a subset of persistent DNA lesions recruited to the NPC vicinity in yeast. (8) In organisms with open mitosis, NPC components assist NE breakdown and centrosome migration. (9) After NPC disassembles, some NPC components accumulate at the kinetochores, while other remain dispersed throughout the mitotic cell. By ensuring the localization and function of key mitotic components, Nups promote accurate spindle assembly, mitotic progression, and faithful chromosome segregation.
Similar articles
- The Role of Nucleoporin Elys in Nuclear Pore Complex Assembly and Regulation of Genome Architecture.
Shevelyov YY. Shevelyov YY. Int J Mol Sci. 2020 Dec 13;21(24):9475. doi: 10.3390/ijms21249475. Int J Mol Sci. 2020. PMID: 33322130 Free PMC article. Review. - You are who your friends are-nuclear pore proteins as components of chromatin-binding complexes.
Capelson M. Capelson M. FEBS Lett. 2023 Nov;597(22):2769-2781. doi: 10.1002/1873-3468.14728. Epub 2023 Sep 7. FEBS Lett. 2023. PMID: 37652464 Free PMC article. Review. - The mode of mitosis is dramatically modified by deletion of a single nuclear pore complex gene in Aspergillus nidulans.
Chemudupati M, Johns M, Osmani SA. Chemudupati M, et al. Fungal Genet Biol. 2019 Sep;130:72-81. doi: 10.1016/j.fgb.2019.04.010. Epub 2019 Apr 23. Fungal Genet Biol. 2019. PMID: 31026588 - Metazoan nuclear pore complexes in gene regulation and genome stability.
Nobari P, Doye V, Boumendil C. Nobari P, et al. DNA Repair (Amst). 2023 Oct;130:103565. doi: 10.1016/j.dnarep.2023.103565. Epub 2023 Sep 4. DNA Repair (Amst). 2023. PMID: 37696111 Review. - The Nuclear Pore Complex in Cell Type-Specific Chromatin Structure and Gene Regulation.
Sun J, Shi Y, Yildirim E. Sun J, et al. Trends Genet. 2019 Aug;35(8):579-588. doi: 10.1016/j.tig.2019.05.006. Epub 2019 Jun 15. Trends Genet. 2019. PMID: 31213386 Review.
Cited by
- Improved Determination of Subnuclear Position Enabled by Three-Dimensional Membrane Reconstruction.
Zhao Y, Schreiner SM, Koo PK, Colombi P, King MC, Mochrie SG. Zhao Y, et al. Biophys J. 2016 Jul 12;111(1):19-24. doi: 10.1016/j.bpj.2016.05.036. Biophys J. 2016. PMID: 27410730 Free PMC article. - Daughter-cell-specific modulation of nuclear pore complexes controls cell cycle entry during asymmetric division.
Kumar A, Sharma P, Gomar-Alba M, Shcheprova Z, Daulny A, Sanmartín T, Matucci I, Funaya C, Beato M, Mendoza M. Kumar A, et al. Nat Cell Biol. 2018 Apr;20(4):432-442. doi: 10.1038/s41556-018-0056-9. Epub 2018 Mar 12. Nat Cell Biol. 2018. PMID: 29531309 Free PMC article. - Nuclear and degradative functions of the ESCRT-III pathway: implications for neurodegenerative disease.
Keeley O, Coyne AN. Keeley O, et al. Nucleus. 2024 Dec;15(1):2349085. doi: 10.1080/19491034.2024.2349085. Epub 2024 May 3. Nucleus. 2024. PMID: 38700207 Free PMC article. Review. - ROCK-dependent phosphorylation of NUP62 regulates p63 nuclear transport and squamous cell carcinoma proliferation.
Hazawa M, Lin DC, Kobayashi A, Jiang YY, Xu L, Dewi FRP, Mohamed MS, Hartono, Nakada M, Meguro-Horike M, Horike SI, Koeffler HP, Wong RW. Hazawa M, et al. EMBO Rep. 2018 Jan;19(1):73-88. doi: 10.15252/embr.201744523. Epub 2017 Dec 7. EMBO Rep. 2018. PMID: 29217659 Free PMC article. - Physiological and Pathological Aging Affects Chromatin Dynamics, Structure and Function at the Nuclear Edge.
Robin JD, Magdinier F. Robin JD, et al. Front Genet. 2016 Aug 23;7:153. doi: 10.3389/fgene.2016.00153. eCollection 2016. Front Genet. 2016. PMID: 27602048 Free PMC article. Review.
References
- Akhtar A, Gasser SM. 2007. The nuclear envelope and transcriptional control. Nat Rev Genet 8: 507–517. - PubMed
- Bai XT, Gu BW, Yin T, Niu C, Xi XD, Zhang J, Chen Z, Chen SJ. 2006. Trans-repressive effect of NUP98–PMX1 on PMX1-regulated c-FOS gene through recruitment of histone deacetylase 1 by FG repeats. Cancer Res 66: 4584–4590. - PubMed
Publication types
MeSH terms
Substances
LinkOut - more resources
Full Text Sources
Other Literature Sources