Engagement of heterogeneous nuclear ribonucleoprotein M with listeriolysin O induces type I interferon expression and restricts Listeria monocytogenes growth in host cells

Immunobiology

Volumn 217, Issue 10, 2012, Pages 972-981

  Luo, Zheng ^a   Li, Zhonghua ^a   Chen, Kun ^a   Liu, Ruochen ^a   Li, Xiaoqi ^a   Cao, Hong ^a   Zheng, Shijun J ^a  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

Author keywords

Heterogeneous nuclear ribonucleoprotein M; Immune response; Listeiosis; Listeria monocytogene; Listeriolysin O

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN M; INTERFERON; LISTERIOLYSIN O; TRANSCRIPTION FACTOR AP 1;

ANIMAL CELL; ARTICLE; BACTERIAL GROWTH; CONTROLLED STUDY; HOST CELL; HOST PATHOGEN INTERACTION; HOST RESISTANCE; IMMUNE RESPONSE; IMMUNOPRECIPITATION; LISTERIA MONOCYTOGENES; MASS SPECTROMETRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RNA SPLICING;

ANIMALS; BACTERIAL TOXINS; CELL LINE; GENE EXPRESSION REGULATION; HEAT-SHOCK PROTEINS; HEMOLYSIN PROTEINS; HEMOLYSIS; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEIN GROUP M; HOST-PATHOGEN INTERACTIONS; HUMANS; INTERFERON TYPE I; LISTERIA MONOCYTOGENES; MICE; MICE, INBRED BALB C; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTEIN TRANSPORT; RECOMBINANT PROTEINS; RNA INTERFERENCE;

EID: 84865349354     PISSN: 01712985     EISSN: 18783279     Source Type: Journal    
DOI: 10.1016/j.imbio.2012.01.009     Document Type: Article

References (40)

1. Vazquez-Boland J.A., Kuhn M., Berche P., Chakraborty T., Dominguez-Bernal G., Goebel W., Gonzalez-Zorn B., Wehland J., Kreft J. Listeria pathogenesis and molecular virulence determinants. Clin. Microbiol. Rev. 2001, 14:584.
2. Zenewicz L.A., Shen H. Innate and adaptive immune responses to Listeria monocytogenes: a short overview. Microbes Infect. 2007, 9:1208.
3. Cameron L.A., Giardini P.A., Soo F.S., Theriot J.A. Secrets of actin-based motility revealed by a bacterial pathogen. Nat. Rev. Mol. Cell Biol. 2000, 1:110.
4. Cossart P., Toledo-Arana A. Listeria monocytogenes, a unique model in infection biology: an overview. Microbes Infect. 2008, 10:1041.
5. Mauder N., Ecke R., Mertins S., Loeffler D.I., Seidel G., Sprehe M., Hillen W., Goebel W., Muller-Altrock S. Species-specific differences in the activity of PrfA, the key regulator of listerial virulence genes. J. Bacteriol. 2006, 188:7941.
6. Toledo-Arana A., Dussurget O., Nikitas G., Sesto N., Guet-Revillet H., Balestrino D., Loh E., Gripenland J., Tiensuu T., Vaitkevicius K., Barthelemy M., Vergassola M., Nahori M.A., Soubigou G., Regnault B., Coppee J.Y., Lecuit M., Johansson J., Cossart P. The Listeria transcriptional landscape from saprophytism to virulence. Nature 2009, 459:950.
7. Singh R., Jamieson A., Cresswell P. GILT is a critical host factor for Listeria monocytogenes infection. Nature 2008, 455:1244.
8. Kayal S., Charbit A. Listeriolysin O: a key protein of Listeria monocytogenes with multiple functions. FEMS Microbiol. Rev. 2006, 30:514.
9. Kohda C., Kawamura I., Baba H., Nomura T., Ito Y., Kimoto T., Watanabe I., Mitsuyama M. Dissociated linkage of cytokine-inducing activity and cytotoxicity to different domains of listeriolysin O from Listeria monocytogenes. Infect. Immun. 2002, 70:1334.
10. Carrero J.A., Calderon B., Unanue E.R. Listeriolysin O from Listeria monocytogenes is a lymphocyte apoptogenic molecule. J. Immunol. 2004, 172:4866.
11. Hara H., Tsuchiya K., Nomura T., Kawamura I., Shoma S., Mitsuyama M. Dependency of caspase-1 activation induced in macrophages by Listeria monocytogenes on cytolysin, listeriolysin O, after evasion from phagosome into the cytoplasm. J. Immunol. 2008, 180:7859.
12. Fink S.L., Cookson B.T. Apoptosis, pyroptosis, and necrosis: mechanistic description of dead and dying eukaryotic cells. Infect. Immun. 2005, 73:1907.
13. Zwaferink H., Stockinger S., Hazemi P., Lemmens-Gruber R., Decker T. IFN-beta increases listeriolysin O-induced membrane permeabilization and death of macrophages. J. Immunol. 2008, 180:4116.
14. Birmingham C.L., Canadien V., Kaniuk N.A., Steinberg B.E., Higgins D.E., Brumell J.H. Listeriolysin O allows Listeria monocytogenes replication in macrophage vacuoles. Nature 2008, 451:350.
15. Birmingham C.L., Canadien V., Gouin E., Troy E.B., Yoshimori T., Cossart P., Higgins D.E., Brumell J.H. Listeria monocytogenes evades killing by autophagy during colonization of host cells. Autophagy 2007, 3:442.
16. Meyer-Morse N., Robbins R.J., Rae C.S., Mochegova S.N., Swanson M.S., Zhao Z., Virgin H.W., Portnoy D. Listeriolysin O is necessary and sufficient to induce autophagy during Listeria monocytogenes infection. PLoS One 2010, 5:e8610.
17. Beckerle M.C. Spatial control of actin filament assembly: lessons from Listeria. Cell 1998, 95:741.
18. Goldberg M.B. Actin-based motility of intracellular microbial pathogens. Microbiol. Mol. Biol. Rev. 2001, 65:595.
19. Luo Z., Liu R., Zheng S. Prokaryotic expression of Listeria monocytogene (LM) hly and development of monoclonal antibodies against listeriolysin O (LLO). Sheng Wu Gong Cheng Xue Bao 2009, 25:1652.
20. Xu L.G., Wang Y.Y., Han K.J., Li L.Y., Zhai Z., Shu H.B. VISA is an adapter protein required for virus-triggered IFN-beta signaling. Mol. Cell 2005, 19:727.
21. Payvandi F., Amrute S., Fitzgerald-Bocarsly P. Exogenous and endogenous IL-10 regulate IFN-alpha production by peripheral blood mononuclear cells in response to viral stimulation. J. Immunol. 1998, 160:5861.
22. Sharma P., Kumar S., Kundu G.C. Transcriptional regulation of human osteopontin promoter by histone deacetylase inhibitor, trichostatin A in cervical cancer cells. Mol. Cancer 2010, 9:178.
23. Datar K.V., Dreyfuss G., Swanson M.S. The human hnRNP M proteins: identification of a methionine/arginine-rich repeat motif in ribonucleoproteins. Nucleic Acids Res. 1993, 21:439.
24. Michel E., Reich K.A., Favier R., Berche P., Cossart P. Attenuated mutants of the intracellular bacterium Listeria monocytogenes obtained by single amino acid substitutions in listeriolysin O. Mol. Microbiol. 1990, 4:2167.
25. Decatur A.L., Portnoy D.A. A PEST-like sequence in listeriolysin O essential for Listeria monocytogenes pathogenicity. Science 2000, 290:992.
26. Rogers S., Wells R., Rechsteiner M. Amino acid sequences common to rapidly degraded proteins: the PEST hypothesis. Science 1986, 234:364.
27. Schnupf P., Portnoy D.A. Listeriolysin O: a phagosome-specific lysin. Microbes Infect. 2007, 9:1176.
28. Lety M.A., Frehel C., Berche P., Charbit A. Critical role of the N-terminal residues of listeriolysin O in phagosomal escape and virulence of Listeria monocytogenes. Mol. Microbiol. 2002, 46:367.
29. Schnupf P., Hofmann J., Norseen J., Glomski I.J., Schwartzstein H., Decatur A.L. Regulated translation of listeriolysin O controls virulence of Listeria monocytogenes. Mol. Microbiol. 2006, 61:999.
30. Dreyfuss G., Kim V., Kataoka N. Messenger-RNA-binding proteins and the messages they carry. Nat. Rev. Mol. Cell Biol. 2002, 3:195.
31. Kiesler E., Hase M.E., Brodin D., Visa N. Hrp59, an hnRNP M protein in Chironomus and Drosophila, binds to exonic splicing enhancers and is required for expression of a subset of mRNAs. J. Cell Biol. 2005, 168:1013.
32. Zhong B., Tien P., Shu H.B. Innate immune responses: crosstalk of signaling and regulation of gene transcription. Virology 2006, 352:14.
33. Wilkinson K.A., Henley J.M. Mechanisms, regulation and consequences of protein SUMOylation. Biochem. J. 2010, 428:133.
34. Vertegaal A.C., Ogg S.C., Jaffray E., Rodriguez M.S., Hay R.T., Andersen J.S., Mann M., Lamond A.I. A proteomic study of SUMO-2 target proteins. J. Biol. Chem. 2004, 279:33791.
35. Ribet D., Hamon M., Gouin E., Nahori M.A., Impens F., Neyret-Kahn H., Gevaert K., Vandekerckhove J., Dejean A., Cossart P. Listeria monocytogenes impairs SUMOylation for efficient infection. Nature 2010, 464:1192.
36. Ruben H., Hovhannisyan R.P.c. Heterogeneous ribonucleoprotein M Is a splicing regulatory protein that can enhance or silence splicing of alternatively spliced exons. J. Biol. Chem. 2007, 282:36265.
37. Gattoni R., Mahe D., Mahl P., Fischer N., Mattei M.G., Stevenin J., Fuchs J.P. The human hnRNP-M proteins: structure and relation with early heat shock-induced splicing arrest and chromosome mapping. Nucleic Acids Res. 1996, 24:2535.
38. Hessle V., Björk P., Sokolowski M., de Valdivia E.G., Silverstein R., Artemenko K., Tyagi A., Maddalo G., Ilag L., Helbig R., Zubarev R.A., Visa N. The exosome associates cotranscriptionally with the nascent Pre-mRNP through interactions with heterogeneous nuclear ribonucleoproteins. Mol. Biol. Cell 2009, 20:3459.
39. Marko M., Leichter M., Patrinou-Georgoula M., Guialis A. hnRNP M interacts with PSF and p54(nrb) and co-localizes within defined nuclear structures. Exp. Cell Res. 2010, 316:390.
40. Lleres D., Denegri M., Biggiogera M., Ajuh P., Lamond A.I. Direct interaction between hnRNP-M and CDC5L/PLRG1 proteins affects alternative splice site choice. EMBO Rep. 2010, 11:445.