Cytolethal distending toxin induces the formation of transient messenger-rich ribonucleoprotein nuclear invaginations in surviving cells
Autoři:
Lamia Azzi-Martin aff001; Wencan He aff001; Christelle Péré-Védrenne aff001; Victoria Korolik aff002; Chloé Alix aff001; Martina Prochazkova-Carlotti aff001; Jean-Luc Morel aff003; Emilie Le Roux-Goglin aff001; Philippe Lehours aff001; Mojgan Djavaheri-Mergny aff005; Christophe F. Grosset aff006; Christine Varon aff001; Pierre Dubus aff001; Armelle Ménard aff001
Působiště autorů:
Univ. Bordeaux, INSERM, Bordeaux Research in Translational Oncology, BaRITOn, U1053, Bordeaux, France
aff001; Institute for Glycomics, Griffith University, Gold Coast Campus, Gold Coast, Australia
aff002; Univ. Bordeaux, CNRS; UMR5293, Institut des maladies neurodégénératives, Bordeaux, France
aff003; CHU de Bordeaux, Laboratoire de Bactériologie, Centre National de Référence des Campylobacters et des Hélicobacters, Bordeaux, France
aff004; Univ. Bordeaux, INSERM U1218 ACTION, Institut Bergonié, Bordeaux France, INSERM U1138, Centre de Recherche des Cordeliers, Paris, France. Metabolomics and Cell Biology Platforms, Institut Gustave Roussy, Villejuif, France
aff005; Univ. Bordeaux, INSERM, Biothérapies des Maladies Génétiques, Inflammatoires et Cancer, BMGIC, U1035, Bordeaux, France
aff006; CHU de Bordeaux, Pôle biologie et pathologie, Service de biologie des tumeurs, Bordeaux, France
aff007
Vyšlo v časopise:
Cytolethal distending toxin induces the formation of transient messenger-rich ribonucleoprotein nuclear invaginations in surviving cells. PLoS Pathog 15(9): e32767. doi:10.1371/journal.ppat.1007921
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.ppat.1007921
Souhrn
Humans are frequently exposed to bacterial genotoxins involved in digestive cancers, colibactin and Cytolethal Distending Toxin (CDT), the latter being secreted by many pathogenic bacteria. Our aim was to evaluate the effects induced by these genotoxins on nuclear remodeling in the context of cell survival. Helicobacter infected mice, coculture experiments with CDT- and colibactin-secreting bacteria and hepatic, intestinal and gastric cells, and xenograft mouse-derived models were used to assess the nuclear remodeling in vitro and in vivo. Our results showed that CDT and colibactin induced-nuclear remodeling can be associated with the formation of deep cytoplasmic invaginations in the nucleus of giant cells. These structures, observed both in vivo and in vitro, correspond to nucleoplasmic reticulum (NR). The core of the NR was found to concentrate ribosomes, proteins involved in mRNA translation, polyadenylated RNA and the main components of the complex mCRD involved in mRNA turnover. These structures are active sites of mRNA translation, correlated with a high degree of ploidy, and involve MAPK and calcium signaling. Additional data show that insulation and concentration of these adaptive ribonucleoprotein particles within the nucleus are dynamic, transient and protect the cell until the genotoxic stress is relieved. Bacterial genotoxins-induced NR would be a privileged gateway for selected mRNA to be preferably transported therein for local translation. These findings offer new insights into the context of NR formation, a common feature of many cancers, which not only appears in response to therapies-induced DNA damage but also earlier in response to genotoxic bacteria.
Klíčová slova:
Cell staining – Cytoplasm – Cytoplasmic staining – DAPI staining – DNA damage – Fluorescence imaging – Messenger RNA – Nuclear staining
Zdroje
1. O Cróinín T, Backert S. Host epithelial cell invasion by Campylobacter jejuni: trigger or zipper mechanism? Front Cell Infect Microbiol. 2012;2: 25. doi: 10.3389/fcimb.2012.00025 22919617
2. Jinadasa RN, Bloom SE, Weiss RS, Duhamel GE. Cytolethal distending toxin: a conserved bacterial genotoxin that blocks cell cycle progression, leading to apoptosis of a broad range of mammalian cell lineages. Microbiol Read Engl. 2011;157: 1851–1875. doi: 10.1099/mic.0.049536–0
3. Bezine E, Vignard J, Mirey G. The cytolethal distending toxin effects on Mammalian cells: a DNA damage perspective. Cells. 2014;3: 592–615. doi: 10.3390/cells3020592 24921185
4. Nougayrède J-P, Homburg S, Taieb F, Boury M, Brzuszkiewicz E, Gottschalk G, et al. Escherichia coli induces DNA double-strand breaks in eukaryotic cells. Science. 2006;313: 848–851. doi: 10.1126/science.1127059 16902142
5. Dellaire G, Kepkay R, Bazett-Jones DP. High resolution imaging of changes in the structure and spatial organization of chromatin, gamma-H2A.X and the MRN complex within etoposide-induced DNA repair foci. Cell Cycle Georget Tex. 2009;8: 3750–3769. doi: 10.4161/cc.8.22.10065 19855159
6. Saltel F, Giese A, Azzi L, Elatmani H, Costet P, Ezzoukhry Z, et al. Unr defines a novel class of nucleoplasmic reticulum involved in mRNA translation. J Cell Sci. 2017;130: 1796–1808. doi: 10.1242/jcs.198697 28386023
7. Malhas A, Goulbourne C, Vaux DJ. The nucleoplasmic reticulum: form and function. Trends Cell Biol. 2011;21: 362–373. doi: 10.1016/j.tcb.2011.03.008 21514163
8. Ceelen LM, Haesebrouck F, D’Herde K, Krysko DV, Favoreel H, Vandenabeele P, et al. Mitotic catastrophe as a prestage to necrosis in mouse liver cells treated with Helicobacter pullorum sonicates. J Morphol. 2009;270: 921–928. doi: 10.1002/jmor.10730 19217023
9. Péré-Védrenne C, Cardinaud B, Varon C, Mocan I, Buissonnière A, Izotte J, et al. The Cytolethal Distending Toxin Subunit CdtB of Helicobacter Induces a Th17-related and Antimicrobial Signature in Intestinal and Hepatic Cells In Vitro. J Infect Dis. 2016;213: 1979–1989. doi: 10.1093/infdis/jiw042 26908757
10. Péré-Védrenne C, Prochazkova-Carlotti M, Rousseau B, He W, Chambonnier L, Sifré E, et al. The Cytolethal Distending Toxin Subunit CdtB of Helicobacter hepaticus Promotes Senescence and Endoreplication in Xenograft Mouse Models of Hepatic and Intestinal Cell Lines. Front Cell Infect Microbiol. 2017;7: 268. doi: 10.3389/fcimb.2017.00268 28713773
11. Le Roux-Goglin E, Dubus P, Asencio C, Jutand M-A, Rosenbaum J, Mégraud F. Hepatic lesions observed in hepatitis C virus transgenic mice infected by Helicobacter hepaticus. Helicobacter. 2013;18: 33–40. doi: 10.1111/j.1523-5378.2012.00995.x 23067369
12. Varon C, Duriez A, Lehours P, Ménard A, Layé S, Zerbib F, et al. Study of Helicobacter pullorum proinflammatory properties on human epithelial cells in vitro. Gut. 2009;58: 629–635. doi: 10.1136/gut.2007.144501 18579667
13. de Planell-Saguer M, Rodicio MC, Mourelatos Z. Rapid in situ codetection of noncoding RNAs and proteins in cells and formalin-fixed paraffin-embedded tissue sections without protease treatment. Nat Protoc. 2010;5: 1061–1073. doi: 10.1038/nprot.2010.62 20539282
14. Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods. 2012;9: 671–675. doi: 10.1038/nmeth.2089 22930834
15. Varon C, Dubus P, Mazurier F, Asencio C, Chambonnier L, Ferrand J, et al. Helicobacter pylori infection recruits bone marrow-derived cells that participate in gastric preneoplasia in mice. Gastroenterology. 2012;142: 281–291. doi: 10.1053/j.gastro.2011.10.036 22062361
16. Lundblad D, Landberg G, Roos G, Lundgren E. Ki-67 as a marker for cell cycle regulation by interferon. Anticancer Res. 1991;11: 2131–2136. 1723263
17. van Oijen MG, Medema RH, Slootweg PJ, Rijksen G. Positivity of the proliferation marker Ki-67 in noncycling cells. Am J Clin Pathol. 1998;110: 24–31. doi: 10.1093/ajcp/110.1.24 9661919
18. Collado-Hilly M, Shirvani H, Jaillard D, Mauger J-P. Differential redistribution of Ca2+-handling proteins during polarisation of MDCK cells: Effects on Ca2+ signalling. Cell Calcium. 2010;48: 215–224. doi: 10.1016/j.ceca.2010.09.003 20932574
19. Ray S, Anderson EC. Stimulation of translation by human Unr requires cold shock domains 2 and 4, and correlates with poly(A) binding protein interaction. Sci Rep. 2016;6: 22461. doi: 10.1038/srep22461 26936655
20. Grosset C, Chen CY, Xu N, Sonenberg N, Jacquemin-Sablon H, Shyu AB. A mechanism for translationally coupled mRNA turnover: interaction between the poly(A) tail and a c-fos RNA coding determinant via a protein complex. Cell. 2000;103: 29–40. doi: 10.1016/s0092-8674(00)00102-1 11051545
21. Wagner BJ, DeMaria CT, Sun Y, Wilson GM, Brewer G. Structure and genomic organization of the human AUF1 gene: alternative pre-mRNA splicing generates four protein isoforms. Genomics. 1998;48: 195–202. doi: 10.1006/geno.1997.5142 9521873
22. Weston A, Sommerville J. Xp54 and related (DDX6-like) RNA helicases: roles in messenger RNP assembly, translation regulation and RNA degradation. Nucleic Acids Res. 2006;34: 3082–3094. doi: 10.1093/nar/gkl409 16769775
23. Damgaard CK, Lykke-Andersen J. Translational coregulation of 5’TOP mRNAs by TIA-1 and TIAR. Genes Dev. 2011;25: 2057–2068. doi: 10.1101/gad.17355911 21979918
24. Legartová S, Stixová L, Laur O, Kozubek S, Sehnalová P, Bártová E. Nuclear structures surrounding internal lamin invaginations. J Cell Biochem. 2014;115: 476–487. doi: 10.1002/jcb.24681 24123263
25. Guerra L, Nemec KN, Massey S, Tatulian SA, Thelestam M, Frisan T, et al. A novel mode of translocation for cytolethal distending toxin. Biochim Biophys Acta. 2009;1793: 489–495. doi: 10.1016/j.bbamcr.2008.11.017 19118582
26. Klupp BG, Granzow H, Fuchs W, Keil GM, Finke S, Mettenleiter TC. Vesicle formation from the nuclear membrane is induced by coexpression of two conserved herpesvirus proteins. Proc Natl Acad Sci U S A. 2007;104: 7241–7246. doi: 10.1073/pnas.0701757104 17426144
27. Reese ML, Boothroyd JC. A helical membrane-binding domain targets the Toxoplasma ROP2 family to the parasitophorous vacuole. Traffic Cph Den. 2009;10: 1458–1470. doi: 10.1111/j.1600-0854.2009.00958.x 19682324
28. Kedersha N, Stoecklin G, Ayodele M, Yacono P, Lykke-Andersen J, Fritzler MJ, et al. Stress granules and processing bodies are dynamically linked sites of mRNP remodeling. J Cell Biol. 2005;169: 871–884. doi: 10.1083/jcb.200502088 15967811
29. Souquere S, Mollet S, Kress M, Dautry F, Pierron G, Weil D. Unravelling the ultrastructure of stress granules and associated P-bodies in human cells. J Cell Sci. 2009;122: 3619–3626. doi: 10.1242/jcs.054437 19812307
30. Kedersha N, Anderson P. Mammalian stress granules and processing bodies. Methods Enzymol. 2007;431: 61–81. doi: 10.1016/S0076-6879(07)31005-7 17923231
31. Kedersha N, Chen S, Gilks N, Li W, Miller IJ, Stahl J, et al. Evidence that ternary complex (eIF2-GTP-tRNA(i)(Met))-deficient preinitiation complexes are core constituents of mammalian stress granules. Mol Biol Cell. 2002;13: 195–210. doi: 10.1091/mbc.01-05-0221 11809833
32. Bozler J, Nguyen HQ, Rogers GC, Bosco G. Condensins exert force on chromatin-nuclear envelope tethers to mediate nucleoplasmic reticulum formation in Drosophila melanogaster. G3 Bethesda Md. 2014;5: 341–352. doi: 10.1534/g3.114.015685 25552604
33. Drozdz MM, Vaux DJ. Shared mechanisms in physiological and pathological nucleoplasmic reticulum formation. Nucl Austin Tex. 2017;8: 34–45. doi: 10.1080/19491034.2016.1252893 27797635
34. Jorgens DM, Inman JL, Wojcik M, Robertson C, Palsdottir H, Tsai W-T, et al. Deep nuclear invaginations are linked to cytoskeletal filaments—integrated bioimaging of epithelial cells in 3D culture. J Cell Sci. 2017;130: 177–189. doi: 10.1242/jcs.190967 27505896
35. Fox DT, Duronio RJ. Endoreplication and polyploidy: insights into development and disease. Dev Camb Engl. 2013;140: 3–12. doi: 10.1242/dev.080531 23222436
36. Goulbourne CN, Malhas AN, Vaux DJ. The induction of a nucleoplasmic reticulum by prelamin A accumulation requires CTP:phosphocholine cytidylyltransferase-α. J Cell Sci. 2011;124: 4253–4266. doi: 10.1242/jcs.091009 22223883
37. Puig P-E, Guilly M-N, Bouchot A, Droin N, Cathelin D, Bouyer F, et al. Tumor cells can escape DNA-damaging cisplatin through DNA endoreduplication and reversible polyploidy. Cell Biol Int. 2008;32: 1031–1043. doi: 10.1016/j.cellbi.2008.04.021 18550395
38. Erenpreisa J, Cragg MS. Three steps to the immortality of cancer cells: senescence, polyploidy and self-renewal. Cancer Cell Int. 2013;13: 92. doi: 10.1186/1475-2867-13-92 24025698
39. Zheng L, Dai H, Zhou M, Li X, Liu C, Guo Z, et al. Polyploid cells rewire DNA damage response networks to overcome replication stress-induced barriers for tumour progression. Nat Commun. 2012;3: 815. doi: 10.1038/ncomms1825 22569363
40. Chuderland D, Seger R. Calcium regulates ERK signaling by modulating its protein-protein interactions. Commun Integr Biol. 2008;1: 4–5. doi: 10.4161/cib.1.1.6107 19704446
41. Schwan C, Kruppke AS, Nölke T, Schumacher L, Koch-Nolte F, Kudryashev M, et al. Clostridium difficile toxin CDT hijacks microtubule organization and reroutes vesicle traffic to increase pathogen adherence. Proc Natl Acad Sci U S A. 2014;111: 2313–2318. doi: 10.1073/pnas.1311589111 24469807
42. Guerra L, Carr HS, Richter-Dahlfors A, Masucci MG, Thelestam M, Frost JA, et al. A bacterial cytotoxin identifies the RhoA exchange factor Net1 as a key effector in the response to DNA damage. PloS One. 2008;3: e2254. doi: 10.1371/journal.pone.0002254 18509476
43. Burnens AP, Stanley J, Nicolet J. Possible association of Helicobacter pullorum with lesions of vibrionic hepatitis in poultry. Campylobacter, Helicobacter and related organisms. Plenum Press, New York. Newell D.J., Ketley J.M., Feldman R.A.:; pp. 291–293.
44. Varon C, Mocan I, Mihi B, Péré-Védrenne C, Aboubacar A, Moraté C, et al. Helicobacter pullorum cytolethal distending toxin targets vinculin and cortactin and triggers formation of lamellipodia in intestinal epithelial cells. J Infect Dis. 2014;209: 588–599. doi: 10.1093/infdis/jit539 24470577
45. Fox JG, Dewhirst FE, Tully JG, Paster BJ, Yan L, Taylor NS, et al. Helicobacter hepaticus sp. nov., a microaerophilic bacterium isolated from livers and intestinal mucosal scrapings from mice. J Clin Microbiol. 1994;32: 1238–1245. 8051250
46. Arnold IC, Zigova Z, Holden M, Lawley TD, Rad R, Dougan G, et al. Comparative whole genome sequence analysis of the carcinogenic bacterial model pathogen Helicobacter felis. Genome Biol Evol. 2011;3: 302–308. doi: 10.1093/gbe/evr022 21402865
47. Lee A, Hazell SL, O’Rourke J, Kouprach S. Isolation of a spiral-shaped bacterium from the cat stomach. Infect Immun. 1988;56: 2843–2850. 3169989
48. Franco AT, Israel DA, Washington MK, Krishna U, Fox JG, Rogers AB, et al. Activation of beta-catenin by carcinogenic Helicobacter pylori. Proc Natl Acad Sci U S A. 2005;102: 10646–10651. doi: 10.1073/pnas.0504927102 16027366
49. Blanchard TG, Nedrud JG. Laboratory maintenance of helicobacter species. Curr Protoc Microbiol. 2006;Chapter 8: Unit8B.1. doi: 10.1002/9780471729259.mc08b01s00 18770594
50. Oh JD, Kling-Bäckhed H, Giannakis M, Xu J, Fulton RS, Fulton LA, et al. The complete genome sequence of a chronic atrophic gastritis Helicobacter pylori strain: evolution during disease progression. Proc Natl Acad Sci U S A. 2006;103: 9999–10004. doi: 10.1073/pnas.0603784103 16788065
51. van Doorn NE, Namavar F, Sparrius M, Stoof J, van Rees EP, van Doorn LJ, et al. Helicobacter pylori-associated gastritis in mice is host and strain specific. Infect Immun. 1999;67: 3040–3046. 10338517
52. Keto Y, Ebata M, Okabe S. Gastric mucosal changes induced by long term infection with Helicobacter pylori in Mongolian gerbils: effects of bacteria eradication. J Physiol Paris. 2001;95: 429–436. 11595471
53. Gouali M, Ruckly C, Carle I, Lejay-Collin M, Weill F-X. Evaluation of CHROMagar STEC and STEC O104 chromogenic agar media for detection of Shiga Toxin-producing Escherichia coli in stool specimens. J Clin Microbiol. 2013;51: 894–900. doi: 10.1128/JCM.03121-12 23284030
54. Schindelin J, Rueden CT, Hiner MC, Eliceiri KW. The ImageJ ecosystem: An open platform for biomedical image analysis. Mol Reprod Dev. 2015;82: 518–529. doi: 10.1002/mrd.22489 26153368
Štítky
Hygiena a epidemiologie Infekční lékařství LaboratořČlánek vyšel v časopise
PLOS Pathogens
2019 Číslo 9
- Perorální antivirotika jako vysoce efektivní nástroj prevence hospitalizací kvůli COVID-19 − otázky a odpovědi pro praxi
- Stillova choroba: vzácné a závažné systémové onemocnění
- Diagnostický algoritmus při podezření na syndrom periodické horečky
- Jak souvisí postcovidový syndrom s poškozením mozku?
- Diagnostika virových hepatitid v kostce – zorientujte se (nejen) v sérologii
Nejčtenější v tomto čísle
- Is reliance on an inaccurate genome sequence sabotaging your experiments?
- The molecular clock of Mycobacterium tuberculosis
- Neutralization-guided design of HIV-1 envelope trimers with high affinity for the unmutated common ancester of CH235 lineage CD4bs broadly neutralizing antibodies
- HLA-B locus products resist degradation by the human cytomegalovirus immunoevasin US11