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Content in this edit is translated from the existing French Wikipedia article at fr:Nucléomoduline; see its history for attribution.

Agrobacterium tumefaciens (A) targets the nucleus of a plant cell (D) during an infection.


Nucleomodulins are a family of bacterial proteins that enter the nucleus of eukaryotic cells [1].

This term comes from the contraction between "nucleus" and "modulins", which are microbial molecules that modulate the behaviour of eukaryotic cells. Nucleomodulins are produced by pathogenic or symbiotic bacteria. They act on various processes in the nucleus: remodelling of the chromatin structure[2],[3],[4],[5],[6],[7],[8],[9],[10],[11],[12], transcription [13],[14], splicing of pre-messenger RNA [15],[16], cell division [17]. By acting or expressing genes in host cells or on cell division, nucleomodulins contribute to virulence or bacterial symbiosis.

The identification of nucleomodulins in several species of bacterial pathogens of humans, animals and plants has led to the emergence of the concept that direct control of the nucleus is one of the most sophisticated strategies used by microbes to bypass host defences.

Nucleomodulins can be directly secreted into the intracellular medium after entry of the bacteria into the cell, like Listeria monocytogenes, or they can be injected from the extracellular medium using a type III or IV bacterial secretion system, also known as a "molecular syringe".

More recently, it has been shown that some of them, such as YopM from Yersinia pestis and IpaH9.8 from Shigella flexneri, can autonomously penetrate eukaryotic cells thanks to a membrane transduction domain [18].

The diversity of molecular mechanisms triggered by nucleomodulins [1][19][20] is a source of inspiration for new biotechnologies. They are true nano-machines capable of hijacking a multitude of nuclear processes. In research, nucleomodulins are the subject of in-depth studies that have led to the discovery of new human nuclear regulators, such as the epigenetic regulator BAHD1 [8].

Examples

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Agrobacterium tumefaciens, responsible for crown gall disease, produces an arsenal of Vir proteins, including VirD2 and VirE2, enabling the precise integration of a piece of its DNA, called T-DNA, into that of the host plant [21] (see picture).

Listeria monocytogenes, responsible for listeriosis, can modulate the expression of immunity genes. One of the mechanisms at play involves the bacterial protein LntA, which inhibits the function of the epigenetic regulator BAHD1. The action of this nucleomodulin is associated with chromatin decompaction and activation of an interferon response gene [8],[22].

Shigella flexneri, responsible for shigellosis, secretes the IpaH9.8 protein targeting a mRNA splicing protein that disrupts the production of protein isoforms and the inflammatory response in humans. [16].


References

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  1. ^ a b Bierne, Hélène; Cossart, Pascale (2012-01-31). "When bacteria target the nucleus: the emerging family of nucleomodulins". Cellular Microbiology. 14 (5): 622–633. doi:10.1111/j.1462-5822.2012.01758.x. ISSN 1462-5822. PMID 22289128. Retrieved 2020-02-26. Cite error: The named reference ":2" was defined multiple times with different content (see the help page).
  2. ^ Skrzypek, E.; Cowan, C.; Straley, S. C. (2002-03-01). "Targeting of the Yersinia pestis YopM protein into HeLa cells and intracellular trafficking to the nucleus". Molecular Microbiology. 30 (5): 1051–1065. doi:10.1046/j.1365-2958.1998.01135.x. ISSN 0950-382X. PMID 9988481. Retrieved 2020-02-26. {{cite journal}}: Unknown parameter |displayauthors= ignored (|display-authors= suggested) (help)
  3. ^ Li, Hongtao; Xu, Hao; Zhou, Yan; Zhang, Jie (2007-02-16). "The phosphothreonine lyase activity of a bacterial type III effector family". Science (New York, N.Y.). 315 (5814): 1000–1003. doi:10.1126/science.1138960. ISSN 1095-9203. PMID 17303758. Retrieved 2020-02-26. {{cite journal}}: Unknown parameter |displayauthors= ignored (|display-authors= suggested) (help)
  4. ^ Arbibe, Laurence; Kim, Dong Wook; Batsche, Eric; Pedron, Thierry (2007). "An injected bacterial effector targets chromatin access for transcription factor NF-kappaB to alter transcription of host genes involved in immune responses". Nature Immunology. 8 (1): 47–56. doi:10.1038/ni1423. ISSN 1529-2908. PMID 17159983. Retrieved 2020-02-26. {{cite journal}}: Unknown parameter |displayauthors= ignored (|display-authors= suggested) (help)
  5. ^ Pennini, Meghan E.; Perrinet, Stéphanie; Dautry-Varsat, Alice; Subtil, Agathe (2010-07-15). "Histone methylation by NUE, a novel nuclear effector of the intracellular pathogen Chlamydia trachomatis". PLoS pathogens. 6 (7): e1000995. doi:10.1371/journal.ppat.1000995. ISSN 1553-7374. PMC 2904774. PMID 20657819. Retrieved 2020-02-26. {{cite journal}}: Unknown parameter |displayauthors= ignored (|display-authors= suggested) (help)CS1 maint: unflagged free DOI (link)
  6. ^ Rolando, Monica; Sanulli, Serena; Rusniok, Christophe; Gomez-Valero, Laura (2013). "Legionella pneumophila Effector RomA Uniquely Modifies Host Chromatin to Repress Gene Expression and Promote Intracellular Bacterial Replication". Cell Host & Microbe. 13 (4): 395–405. doi:10.1016/j.chom.2013.03.004. Retrieved 2020-02-26. {{cite journal}}: Unknown parameter |displayauthors= ignored (|display-authors= suggested) (help)
  7. ^ Li, Ting; Lu, Qiuhe; Wang, Guolun; Xu, Hao (2013). "SET‐domain bacterial effectors target heterochromatin protein 1 to activate host rDNA transcription". EMBO reports. 14 (8): 733–740. doi:10.1038/embor.2013.86. ISSN 1469-221X. PMC 3736128. PMID 23797873. Retrieved 2020-02-26. {{cite journal}}: Unknown parameter |displayauthors= ignored (|display-authors= suggested) (help)CS1 maint: PMC format (link)
  8. ^ a b c Lebreton, Alice; Lakisic, Goran; Job, Viviana; Fritsch, Lauriane (2011-03-11). "A bacterial protein targets the BAHD1 chromatin complex to stimulate type III interferon response". Science (New York, N.Y.). 331 (6022): 1319–1321. doi:10.1126/science.1200120. ISSN 1095-9203. PMID 21252314. Retrieved 2020-02-26. {{cite journal}}: Unknown parameter |displayauthors= ignored (|display-authors= suggested) (help) Cite error: The named reference ":0" was defined multiple times with different content (see the help page).
  9. ^ Rennoll-Bankert, Kristen E.; Garcia-Garcia, Jose C.; Sinclair, Sara H.; Dumler, J. Stephen (2015). "Chromatin-bound bacterial effector ankyrin A recruits histone deacetylase 1 and modifies host gene expression: AnkA recruits HDAC1 to modify CYBB expression". Cellular Microbiology. 17 (11): 1640–1652. doi:10.1111/cmi.12461. PMC 5845759. PMID 25996657. Retrieved 2020-02-26. {{cite journal}}: Unknown parameter |displayauthors= ignored (|display-authors= suggested) (help)CS1 maint: PMC format (link)
  10. ^ Farris, Tierra R.; Dunphy, Paige S.; Zhu, Bing; Kibler, Clayton E. (2016). "Ehrlichia chaffeensis TRP32 Is a Nucleomodulin That Directly Regulates Expression of Host Genes Governing Differentiation and Proliferation". Infection and Immunity. 84 (11): 3182–3194. doi:10.1128/IAI.00657-16. ISSN 0019-9567. PMC 5067751. PMID 27572329. Retrieved 2020-02-26. {{cite journal}}: Unknown parameter |displayauthors= ignored (|display-authors= suggested) (help)CS1 maint: PMC format (link)
  11. ^ Mitra, Shubhajit; Dunphy, Paige S.; Das, Seema; Zhu, Bing (2018-01-22). "Ehrlichia chaffeensis TRP120 Effector Targets and Recruits Host Polycomb Group Proteins for Degradation To Promote Intracellular Infection". Infection and Immunity. 86 (4): e00845–17, /iai/86/4/e00845–17.atom. doi:10.1128/IAI.00845-17. ISSN 0019-9567. PMC 5865042. PMID 29358333. Retrieved 2020-02-26. {{cite journal}}: Unknown parameter |displayauthors= ignored (|display-authors= suggested) (help)CS1 maint: PMC format (link)
  12. ^ Yaseen, Imtiyaz; Kaur, Prabhjot; Nandicoori, Vinay Kumar; Khosla, Sanjeev (2015). "Mycobacteria modulate host epigenetic machinery by Rv1988 methylation of a non-tail arginine of histone H3". Nature Communications. 6 (1): 8922. doi:10.1038/ncomms9922. ISSN 2041-1723. Retrieved 2020-02-26. {{cite journal}}: Unknown parameter |displayauthors= ignored (|display-authors= suggested) (help)
  13. ^ Kay, Sabine; Hahn, Simone; Marois, Eric; Hause, Gerd (2007-10-26). "A Bacterial Effector Acts as a Plant Transcription Factor and Induces a Cell Size Regulator". Science. 318 (5850): 648–651. doi:10.1126/science.1144956. ISSN 0036-8075. Retrieved 2020-02-26. {{cite journal}}: Unknown parameter |displayauthors= ignored (|display-authors= suggested) (help)
  14. ^ Römer, Patrick; Hahn, Simone; Jordan, Tina; Strauß, Tina (2007-10-26). "Plant Pathogen Recognition Mediated by Promoter Activation of the Pepper Bs3 Resistance Gene". Science. 318 (5850): 645–648. doi:10.1126/science.1144958. ISSN 0036-8075. Retrieved 2020-02-26. {{cite journal}}: Unknown parameter |displayauthors= ignored (|display-authors= suggested) (help)
  15. ^ Toyotome, Takahito; Suzuki, Toshihiko; Kuwae, Asaomi; Nonaka, Takashi (2001-08-24). "Shigella Protein IpaH 9.8 Is Secreted from Bacteria within Mammalian Cells and Transported to the Nucleus". Journal of Biological Chemistry. 276 (34): 32071–32079. doi:10.1074/jbc.M101882200. ISSN 0021-9258. Retrieved 2020-02-26. {{cite journal}}: Unknown parameter |displayauthors= ignored (|display-authors= suggested) (help)CS1 maint: unflagged free DOI (link)
  16. ^ a b Okuda, Jun; Toyotome, Takahito; Kataoka, Naoyuki; Ohno, Mutsuhito (2005). "Shigella effector IpaH9.8 binds to a splicing factor U2AF35 to modulate host immune responses". Biochemical and Biophysical Research Communications. 333 (2): 531–539. doi:10.1016/j.bbrc.2005.05.145. Retrieved 2020-02-26. {{cite journal}}: Unknown parameter |displayauthors= ignored (|display-authors= suggested) (help) Cite error: The named reference ":1" was defined multiple times with different content (see the help page).
  17. ^ Taieb, Frédéric; Nougayrède, Jean-Philippe; Oswald, Eric (2011-03-29). "Cycle Inhibiting Factors (Cifs): Cyclomodulins That Usurp the Ubiquitin-Dependent Degradation Pathway of Host Cells". Toxins. 3 (4): 356–368. doi:10.3390/toxins3040356. ISSN 2072-6651. PMC 3202828. PMID 22069713. Retrieved 2020-02-26. {{cite journal}}: Unknown parameter |displayauthors= ignored (|display-authors= suggested) (help)CS1 maint: PMC format (link) CS1 maint: unflagged free DOI (link)
  18. ^ Norkowski, Stefanie; Körner, Britta; Greune, Lilo; Stolle, Anne-Sophie; Lubos, Marie-Luise; Hardwidge, Philip R.; Schmidt, M. Alexander; Rüter, Christian (2018-06-01). "Bacterial LPX motif-harboring virulence factors constitute a species-spanning family of cell-penetrating effectors". Cellular and Molecular Life Sciences. 75 (12): 2273–2289. doi:10.1007/s00018-017-2733-4. ISSN 1420-9071. {{cite journal}}: Unknown parameter |displayauthors= ignored (|display-authors= suggested) (help)
  19. ^ Connor, Michael; Arbibe, Laurence; Hamon, Mélanie (2019-03-22). "Customizing Host Chromatin: a Bacterial Tale". Microbiology Spectrum. 7 (2). doi:10.1128/microbiolspec.BAI-0015-2019. ISSN 2165-0497. Retrieved 2020-02-27. {{cite journal}}: Unknown parameter |displayauthors= ignored (|display-authors= suggested) (help)
  20. ^ Bierne, Hélène (2017), Doerfler, Walter; Casadesús, Josep (eds.), "Cross Talk Between Bacteria and the Host Epigenetic Machinery", Epigenetics of Infectious Diseases, Epigenetics and Human Health, Springer International Publishing, pp. 113–158, doi:10.1007/978-3-319-55021-3_6, ISBN 978-3-319-55021-3, retrieved 2020-02-27
  21. ^ Pelczar, Pawel; Kalck, Véronique; Gomez, Divina; Hohn, Barbara (2004). "Agrobacterium proteins VirD2 and VirE2 mediate precise integration of synthetic T-DNA complexes in mammalian cells". EMBO Reports. 5 (6): 632–637. doi:10.1038/sj.embor.7400165. ISSN 1469-221X. PMC 1299075. PMID 15153934. Retrieved 2020-02-26. {{cite journal}}: Unknown parameter |displayauthors= ignored (|display-authors= suggested) (help)
  22. ^ Lebreton, Alice; Job, Viviana; Ragon, Marie; Le Monnier, Alban (2014-01-21). "Structural basis for the inhibition of the chromatin repressor BAHD1 by the bacterial nucleomodulin LntA". mBio. 5 (1): e00775–00713. doi:10.1128/mBio.00775-13. ISSN 2150-7511. PMC 3903274. PMID 24449750. Retrieved 2020-02-26. {{cite journal}}: Unknown parameter |displayauthors= ignored (|display-authors= suggested) (help)

[[Category:Genetics]]

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