Manipulation of Cellular Processes via Nucleolus Hijaking in the Course of Viral Infection in Mammals

Olga V. Iarovaia; Elena S. Ioudinkova; Artem K. Velichko; Sergey V. Razin

doi:10.3390/cells10071597

journal article Open Access Jun 25, 2021

Manipulation of Cellular Processes via Nucleolus Hijaking in the Course of Viral Infection in Mammals

Olga V. Iarovaia Elena S. Ioudinkova Artem K. Velichko Sergey V. Razin

Cells Vol. 10 No. 7 pp. 1597 · MDPI AG

View at Publisher Save 10.3390/cells10071597

Abstract

Due to their exceptional simplicity of organization, viruses rely on the resources, molecular mechanisms, macromolecular complexes, regulatory pathways, and functional compartments of the host cell for an effective infection process. The nucleolus plays an important role in the process of interaction between the virus and the infected cell. The interactions of viral proteins and nucleic acids with the nucleolus during the infection process are universal phenomena and have been described for almost all taxonomic groups. During infection, proteins of the nucleolus in association with viral components can be directly used for the processes of replication and transcription of viral nucleic acids and the assembly and transport of viral particles. In the course of a viral infection, the usurpation of the nucleolus functions occurs and the usurpation is accompanied by profound changes in ribosome biogenesis. Recent studies have demonstrated that the nucleolus is a multifunctional and dynamic compartment. In addition to the biogenesis of ribosomes, it is involved in regulating the cell cycle and apoptosis, responding to cellular stress, repairing DNA, and transcribing RNA polymerase II-dependent genes. A viral infection can be accompanied by targeted transport of viral proteins to the nucleolus, massive release of resident proteins of the nucleolus into the nucleoplasm and cytoplasm, the movement of non-nucleolar proteins into the nucleolar compartment, and the temporary localization of viral nucleic acids in the nucleolus. The interaction of viral and nucleolar proteins interferes with canonical and non-canonical functions of the nucleolus and results in a change in the physiology of the host cell: cell cycle arrest, intensification or arrest of ribosome biogenesis, induction or inhibition of apoptosis, and the modification of signaling cascades involved in the stress response. The nucleolus is, therefore, an important target during viral infection. In this review, we discuss the functional impact of viral proteins and nucleic acid interaction with the nucleolus during infection.

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References

144

[1]

The multifunctional nucleolus

François-Michel Boisvert, Silvana van Koningsbruggen, Joaquín Navascués et al.

Nature Reviews Molecular Cell Biology 2007 10.1038/nrm2184

[2]

Grummt "Dynamic regulation of nucleolar architecture" Curr. Opin. Cell Biol. (2018) 10.1016/j.ceb.2018.02.013

[3]

Pederson "The Nucleolus" Cold Spring Harb. Perspect. Biol. (2011) 10.1101/cshperspect.a000638

[4]

The nucleolus as a multiphase liquid condensate

Denis L. J. Lafontaine, Joshua A. Riback, Rümeyza Bascetin et al.

Nature Reviews Molecular Cell Biology 2021 10.1038/s41580-020-0272-6

[5]

Thiry "Birth of a nucleolus: The evolution of nucleolar compartments" Trends Cell Biol. (2005) 10.1016/j.tcb.2005.02.007

[6]

Gonzalez "Complete Sequence of the 43-kb Human Ribosomal DNA Repeat: Analysis of the Intergenic Spacer" Genomics (1995) 10.1006/geno.1995.1049

[7]

Srivastava "Structure and organization of ribosomal DNA" Biochimie (1991) 10.1016/0300-9084(91)90042-y

[8]

Olson "The nucleolus: An old factory with unexpected capabilities" Trends Cell Biol. (2000) 10.1016/s0962-8924(00)01738-4

[9]

The plurifunctional nucleolus

T Pederson

Nucleic Acids Research 1998 10.1093/nar/26.17.3871

[10]

Bensaddek "Quantitative Proteomic Analysis of the Human Nucleolus" Methods Mol. Biol (2016) 10.1007/978-1-4939-3792-9_20

[11]

Andersen "Nucleolar proteome dynamics" Nature (2005) 10.1038/nature03207

[12]

Cerqueira "Ribosomal DNA and the Nucleolus as Keystones of Nuclear Architecture, Organization, and Function" Trends Genet. (2019) 10.1016/j.tig.2019.07.011

[13]

Mapping the nucleolar proteome reveals a spatiotemporal organization related to intrinsic protein disorder

Lovisa Stenström, Diana Mahdessian, Christian Gnann et al.

Molecular Systems Biology 2020 10.15252/msb.20209469

[14]

Latonen "Phase-to-Phase with Nucleoli—Stress Responses, Protein Aggregation and Novel Roles of RNA" Front. Cell. Neurosci. (2019) 10.3389/fncel.2019.00151

[15]

Martin "Principles of protein targeting to the nucleolus" Nucleus (2015) 10.1080/19491034.2015.1079680

[16]

Scott "Characterization and prediction of protein nucleolar localization sequences" Nucleic Acids Res. (2010) 10.1093/nar/gkq653

[17]

Emmott "Nucleolar targeting: The hub of the matter" EMBO Rep. (2009) 10.1038/embor.2009.14

[18]

Weeks "The nucleolus: A central response hub for the stressors that drive cancer progression" Cell. Mol. Life Sci. (2019) 10.1007/s00018-019-03231-0

[19]

Boulon "The Nucleolus under Stress" Mol. Cell (2010) 10.1016/j.molcel.2010.09.024

[20]

Pirogov, S.A., Gvozdev, V.A., and Klenov, M.S. (2019). Long Noncoding RNAs and Stress Response in the Nucleolus. Cells, 8. 10.3390/cells8070668

[21]

Zhao "lncRNA PAPAS tethered to the rDNA enhancer recruits hypophosphorylated CHD4/NuRD to repress rRNA synthesis at elevated temperatures" Genes Dev. (2018) 10.1101/gad.311688.118

[22]

Yang "Nucleolar Stress: Hallmarks, sensing mechanism and diseases" Cell Stress (2018) 10.15698/cst2018.06.139

[23]

Rawlinson "The nucleolar interface of RNA viruses" Cell. Microbiol. (2015) 10.1111/cmi.12465

[24]

Viruses and the nucleolus: The fatal attraction

Anna Salvetti, Anna Greco

Biochimica et Biophysica Acta (BBA) - Molecular Ba... 2014 10.1016/j.bbadis.2013.12.010

[25]

Ni "The nucleolus and herpesviral usurpation" J. Med. Microbiol. (2012) 10.1099/jmm.0.045963-0

[26]

Wang "The nucleolus and viral infection" Virol. Sin. (2010) 10.1007/s12250-010-3093-5

[27]

Hiscox "Nucleolar proteomics and viral infection" Proteomics (2010) 10.1002/pmic.201000251

[28]

Sirri "Nucleolus: The fascinating nuclear body" Histochem. Cell Biol. (2007) 10.1007/s00418-007-0359-6

[29]

Hiscox "RNA viruses: Hijacking the dynamic nucleolus" Nat. Rev. Microbiol. (2007) 10.1038/nrmicro1597

[30]

Hiscox "The nucleolus—A gateway to viral infection?" Arch. Virol. (2002) 10.1007/s00705-001-0792-0

[31]

Reyes "Identifying Host Factors Associated with DNA Replicated During Virus Infection" Mol. Cell. Proteom. (2017) 10.1074/mcp.m117.067116

[32]

Nouri, K., Moll, J.M., Milroy, L.-G., Hain, A., Dvorsky, R., Amin, E., Lenders, M., Nagel-Steger, L., Howe, S., and Smits, S.H.J. (2015). Biophysical Characterization of Nucleophosmin Interactions with Human Immunodeficiency Virus Rev and Herpes Simplex Virus US11. PLoS ONE, 10. 10.1371/journal.pone.0143634

[33]

Guirimand "VirHostNet 2.0: Surfing on the web of virus/host molecular interactions data" Nucleic Acids Res. (2015) 10.1093/nar/gku1121

[34]

Calderone "VirusMentha: A new resource for virus-host protein interactions" Nucleic Acids Res. (2015) 10.1093/nar/gku830

[35]

Lam "Proteomics Analysis of the Nucleolus in Adenovirus-infected Cells" Mol. Cell. Proteom. (2010) 10.1074/mcp.m900338-mcp200

[36]

Pyper "The Nucleolus Is the Site of Borna Disease Virus RNA Transcription and Replication" J. Virol. (1998) 10.1128/jvi.72.9.7697-7702.1998

[37]

Li "RNA-Templated Replication of Hepatitis Delta Virus: Genomic and Antigenomic RNAs Associate with Different Nuclear Bodies" J. Virol. (2006) 10.1128/jvi.02650-05

[38]

Behrens "Nuclear Export Signal Masking Regulates HIV-1 Rev Trafficking and Viral RNA Nuclear Export" J. Virol. (2017) 10.1128/jvi.02107-16

[39]

Michienzi "Ribozyme-mediated inhibition of HIV 1 suggests nucleolar trafficking of HIV-1 RNA" Proc. Natl. Acad. Sci. USA (2000) 10.1073/pnas.97.16.8955

[40]

Zolotukhin "Nucleoporins Nup98 and Nup214 Participate in Nuclear Export of Human Immunodeficiency Virus Type 1 Rev" J. Virol. (1999) 10.1128/jvi.73.1.120-127.1999

[41]

Vercruysse "HIV-1 Rev multimerization: Mechanism and insights" Curr. HIV Res. (2014) 10.2174/1570162x12666140307094603

[42]

Michienzi "A nucleolar localizing Rev binding element inhibits HIV replication" AIDS Res. Ther. (2006) 10.1186/1742-6405-3-13

[43]

Johnson "Enhancement of Adeno-Associated Virus Infection by Mobilizing Capsids into and Out of the Nucleolus" J. Virol. (2009) 10.1128/jvi.02309-08

[44]

Sonntag "A viral assembly factor promotes AAV2 capsid formation in the nucleolus" Proc. Natl. Acad. Sci. USA (2010) 10.1073/pnas.1001673107

[45]

Miyamoto, S., Nakano, M., Morikawa, T., Hirabayashi, A., Tamura, R., Fujita, Y., Hirose, N., Muramoto, Y., and Noda, T. (2021). Influenza virus ribonucleoprotein complex formation occurs in the nucleolus. BioRxiv. 10.1101/2021.02.24.432647

[46]

Schmid "DNA Virus Replication Compartments" J. Virol. (2014) 10.1128/jvi.02046-13

[47]

Nucleolin Is Required for an Efficient Herpes Simplex Virus Type 1 Infection

Aleth Callé, Iva Ugrinova, Alberto L. Epstein et al.

Journal of Virology 2008 10.1128/jvi.00077-08

[48]

Strang "Viral and cellular subnuclear structures in human cytomegalovirus-infected cells" J. Gen. Virol. (2015) 10.1099/vir.0.071084-0

[49]

Strang "Nucleolin Associates with the Human Cytomegalovirus DNA Polymerase Accessory Subunit UL44 and Is Necessary for Efficient Viral Replication" J. Virol. (2009) 10.1128/jvi.01510-09

[50]

Bender "Dynamic and Nucleolin-Dependent Localization of Human Cytomegalovirus UL84 to the Periphery of Viral Replication Compartments and Nucleoli" J. Virol. (2014) 10.1128/jvi.01889-14

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Details

Published: Jun 25, 2021
Vol/Issue: 10(7)
Pages: 1597
License: View

Authors

O

Olga V. Iarovaia

Institute of Gene Biology Russian Academy of Sciences, 119334 Moscow, Russia

E

Elena S. Ioudinkova

Institute of Gene Biology Russian Academy of Sciences, 119334 Moscow, Russia

A

Artem K. Velichko

Institute of Gene Biology Russian Academy of Sciences, 119334 Moscow, Russia

S

Sergey V. Razin

Institute of Gene Biology Russian Academy of Sciences, 119334 Moscow, Russia

Funding

Russian Science Foundation Award: 21-64-00001

Cite This Article

Olga V. Iarovaia, Elena S. Ioudinkova, Artem K. Velichko, et al. (2021). Manipulation of Cellular Processes via Nucleolus Hijaking in the Course of Viral Infection in Mammals. Cells, 10(7), 1597. https://doi.org/10.3390/cells10071597

Manipulation of Cellular Processes via Nucleolus Hijaking in the Course of Viral Infection in Mammals

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