840
Views
0
CrossRef citations to date
0
Altmetric
Research PAPER

The perinucleolar compartment: structure, function, and utility in anti-cancer drug development

ORCID Icon & ORCID Icon
Article: 2306777 | Received 25 Sep 2023, Accepted 12 Jan 2024, Published online: 27 Jan 2024

References

  • Spector DL. Higher order nuclear organization: three-dimensional distribution of small nuclear ribonucleoprotein particles. Proc Natl Acad Sci U S A. 1990;87(1):147–8. doi: 10.1073/pnas.87.1.147
  • Bouwman B, Crosetto N, Bienko M. RNA gradients: shapers of 3D genome architecture. Current Opinion In Cell Biology. 2022;74:7–12. doi: 10.1016/j.ceb.2021.12.001
  • Maeshima K, Meshorer E. Editorial: emerging concepts and tools in genome organization and chromatin function in eukaryotes. Curr Opin Cell Biol. 2022;78:102120. doi: 10.1016/j.ceb.2022.102120
  • Misteli T, Spector DL. The cellular organization of gene expression. Curr Opin Cell Biol. 1998;10(3):323–331. doi: 10.1016/S0955-0674(98)80007-0
  • Misteli T, Spector DL. The nucleus. Woodbury, New York: Cold Spring Harbor Laboratory Press; 2011.
  • Spector DL. Nuclear domains. J Cell Sci. 2001;114(16):2891–2893. doi: 10.1242/jcs.114.16.2891
  • Cremer T, Cremer C. Chromosome territories, nuclear architecture and gene regulation in mammalian cells. Nat Rev Genet. 2001;2(4):292–301. doi: 10.1038/35066075
  • Cremer T, Cremer M. Chromosome territories. Cold Spring Harb Perspect Biol. 2010;2(3):a003889. doi: 10.1101/cshperspect.a003889
  • Baserga SJ, Dimario PJ, Duncan FE. Emerging roles for the nucleolus 2019. J Biol Chem. 2020;295(16):5535–5537. doi: 10.1074/jbc.MT120.013346
  • Grummt I. Life on a planet of its own: regulation of RNA polymerase I transcription in the nucleolus. Genes Dev. 2003;17(14):1691–1702. doi: 10.1101/gad.1098503R
  • Hernandez-Verdun D. Nucleolus: from structure to dynamics. Histochem Cell Biol. 2006;125(1–2):127–137. doi: 10.1007/s00418-005-0046-4
  • Iarovaia OV, Minina EP, Sheval EV, et al. Nucleolus: a central hub for nuclear functions. Trends Cell Biol. 2019;29(8):647–659. doi: 10.1016/j.tcb.2019.04.003
  • Nemeth A, Grummt I. Dynamic regulation of nucleolar architecture. Curr Opin Cell Biol. 2018;52:105–111. doi: 10.1016/j.ceb.2018.02.013
  • Pederson T. The plurifunctional nucleolus. Nucleic Acids Res. 1998;26(17):3871–3876. doi: 10.1093/nar/26.17.3871
  • Pederson T. The nucleolus. Cold Spring Harb Perspect Biol. 2011;3(3):209–223. doi: 10.1101/cshperspect.a000638
  • Lafontaine DLJ, Riback JA, Bascetin R, et al. The nucleolus as a multiphase liquid condensate. Nat Rev Mol Cell Biol. 2021;22(3):165–182. doi: 10.1038/s41580-020-0272-6
  • Ghetti A, Piñol-Roma S, Michael WM, et al. hnRNP 1, the polyprimidine tract-binding protein: distinct nuclear localization and association with hnRnas. Nucleic Acids Res. 1992;20(14):3671–3678. doi: 10.1093/nar/20.14.3671
  • Lee B, Matera AG, Ward DC, et al. Association of RNase mitochondrial RNA processing enzyme with ribonuclease P in higher ordered structures in the nucleolus: a possible coordinate role in ribosome biogenesis. Proc Natl Acad Sci U S A. 1996;93(21):11471–11476. doi: 10.1073/pnas.93.21.11471
  • Matera AG, Frey MR, Margelot K, et al. A perinucleolar compartment contains several RNA polymerase III transcripts as well as the polypyrimidine tract-binding protein, hnRNP I. J Cell Bio. 1995;129(5):1181–1193. doi: 10.1083/jcb.129.5.1181
  • Huang S, Deerinck TJ, Ellisman MH, et al. The dynamic organization of the perinucleolar compartment in the cell nucleus. J Cell Bio. 1997;137(5):965–974. doi: 10.1083/jcb.137.5.965
  • Huang S, Deerinck TJ, Ellisman MH, et al. The perinucleolar compartment and transcription. J Cell Bio. 1998;143(1):35–47. doi: 10.1083/jcb.143.1.35
  • Even Y, Escande ML, Fayet C, et al. CDK13, a kinase involved in pre-mRNA splicing, is a component of the perinucleolar compartment. PloS One. 2016;11(2):e0149184. doi: 10.1371/journal.pone.0149184
  • Norton JT, Pollock CB, Wang C, et al. Perinucleolar compartment prevalence is a phenotypic pancancer marker of malignancy. Cancer. 2008;113(4):861–869. doi: 10.1002/cncr.23632
  • Pettaway CA, Pathak S, Greene G, et al. Selection of highly metastatic variants of different human prostatic carcinomas using orthotopic implantation in nude mice. Clin Cancer Res. 1996;2(9):1627–1636.
  • Frankowski KJ, Wang C, Patnaik S, et al. Metarrestin, a perinucleolar compartment inhibitor, effectively suppresses metastasis. Sci Transl Med. 2018;10(441). doi: 10.1126/scitranslmed.aap8307
  • Kamath RV, Thor AD, Wang C, et al. Perinucleolar compartment prevalence has an independent prognostic value for breast cancer. Cancer Res. 2005;65(1):246–253. doi: 10.1158/0008-5472.246.65.1
  • Slusarczyk A, Kamath R, Wang C, et al. Structure and function of the perinucleolar compartment in cancer cells. Cold Spring Harb Symp Quant Biol. 2011;75:599–605. doi: 10.1101/sqb.2010.75.026
  • Yap K, Mukhina S, Zhang G, et al. A short tandem repeat-enriched RNA assembles a nuclear compartment to control alternative splicing and promote cell survival. Mol Cell. 2018;72(3):525–540.e13. doi: 10.1016/j.molcel.2018.08.041
  • Norton JT, Huang S. The perinucleolar compartment: RNA metabolism and cancer. Cancer Treat Res. 2013;158:139–152.
  • Norton JT, Titus SA, Dexter D, et al. Automated high-content screening for compounds that disassemble the perinucleolar compartment. J Biomol Screen. 2009a;14(9):1045–1053. doi: 10.1177/1087057109343120
  • Frankowski KJ, Patnaik S, Wang C, et al. Discovery and optimization of pyrrolopyrimidine derivatives as selective disruptors of the perinucleolar compartment, a marker of tumor progression toward metastasis. J Med Chem. 2022;65(12):8303–8331. doi: 10.1021/acs.jmedchem.2c00204
  • Wang C, Politz JC, Pederson T, et al. RNA polymerase III transcripts and the PTB protein are essential for the integrity of the perinucleolar compartment. Mol Biol Cell. 2003;14(6):2425–2435. doi: 10.1091/mbc.e02-12-0818
  • Pollock C, Daily K, Nguyen VT, et al. Characterization of MRP RNA–protein interactions within the perinucleolar compartment. Mol Biol Cell. 2011;22(6):858–866. doi: 10.1091/mbc.e10-09-0768
  • Fu X-D, Mobley WC. Therapeutic potential of PTB inhibition through converting glial cells to neurons in the brain. Annu Rev Neurosci. 2023;46(1):145–165. doi: 10.1146/annurev-neuro-083022-113120
  • Kafasla P, Mickleburgh I, Llorian M, et al. Defining the roles and interactions of PTB. Biochem Soc Trans. 2012;40(4):815–820. doi: 10.1042/BST20120044
  • Sawicka K, Bushell M, Spriggs KA, et al. Polypyrimidine-tract-binding protein: a multifunctional RNA-binding protein. Biochem Soc Trans. 2008;36(4):641–647. doi: 10.1042/BST0360641
  • Hüttelmaier S, Illenberger S, Grosheva I, et al. Raver1, a dual compartment protein, is a ligand for PTB/hnRNPI and microfilament attachment proteins. J Cell Bio. 2001;155(5):775–786. doi: 10.1083/jcb.200105044
  • Kleinhenz B, Fabienke M, Swiniarski S, et al. Raver2, a new member of the hnRNP family. FEBS Lett. 2005;579(20):4254–4258. doi: 10.1016/j.febslet.2005.07.001
  • Malumbres M. Cyclin-dependent kinases. Genome Bio. 2014;15(6):122. doi: 10.1186/gb4184
  • Hydbring P, Malumbres M, Sicinski P. Non-canonical functions of cell cycle cyclins and cyclin-dependent kinases. Nat Rev Mol Cell Biol. 2016;17(5):280–292. doi: 10.1038/nrm.2016.27
  • Brewer G. Impaired RNA clearance. Nat Rev Cancer. 2023;23(7):428–428. doi: 10.1038/s41568-023-00589-z
  • Insco ML, Abraham BJ, Dubbury SJ, et al. Oncogenic CDK13 mutations impede nuclear RNA surveillance. Science. 2023;380(6642):eabn7625. doi: 10.1126/science.abn7625
  • Qi J-C, Yang Z, Lin T, et al. CDK13 upregulation-induced formation of the positive feedback loop among circCDK13, miR-212-5p/miR-449a and E2F5 contributes to prostate carcinogenesis. J Exp Clin Cancer Res. 2021;40(1):2. doi: 10.1186/s13046-020-01814-5
  • Yap K, Chung TH, Makeyev EV. Hybridization-proximity labeling reveals spatially ordered interactions of nuclear RNA compartments. Molecular Cell. 2022;82(2):463–478.e11. doi: 10.1016/j.molcel.2021.10.009
  • Madl T, Sattler M. Adhesion dance with raver. Structure. 2009;17(6):781–783. doi: 10.1016/j.str.2009.05.004
  • Wang C, Ma H, Baserga SJ, et al. Nucleolar structure connects with global nuclear organization. Mol Biol Cell. 2023 Nov 1;34(12): ar114. doi: 10.1091/mbc.E23-02-0062
  • Norton JT, Wang C, Gjidoda A, et al. The perinucleolar compartment is directly associated with DNA. J Biol Chem. 2009b;284(7):4090–4101. doi: 10.1074/jbc.M807255200