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Vita-PAMPs: Signatures of Microbial Viability

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Crossroads Between Innate and Adaptive Immunity IV

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 785))

Abstract

Can the innate immune system detect and respond to microbial viability? Using bacteria as a model, we found that indeed the very essence of microbial infectivity, viability itself, can be detected, and notably, in the absence of the activity of virulence factors. The microbial molecule that serves as the signature of viability is bacterial messenger RNA (mRNA), common to all bacteria, and without which bacteria cannot survive. Prokaryotic mRNAs also differ from eukaryotic mRNAs in several ways, and as such, these features all fulfill the criteria, and more, for a pathogen-associated molecular pattern (PAMP) as originally proposed by Charles Janeway. Because these mRNAs are lost from dead bacteria, they belong to a special class of PAMPs, which we call vita-PAMPs. Here we discuss the possible receptors and pathways involved in the detection of bacterial mRNAs, and thus microbial viability. We also consider examples of vita-PAMPs other than bacterial mRNA.

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References

  1. Janeway CA, Jr. Approaching the asymptote? Evolution and revolution in immunology. Cold Spring Harbor symposia on quantitative biology. 1989;54 Pt 1:1–13. Epub 1989/01/01.

    Google Scholar 

  2. Medzhitov R, Preston-Hurlburt P, Janeway CA, Jr. A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature. 1997;388(6640):394–7. Epub 1997 Jul 24.

    Google Scholar 

  3. Takeuchi O, Akira S. Pattern recognition receptors and inflammation. Cell. 2010;140(6):805–20. Epub 2010 Mar 23.

    Google Scholar 

  4. Kawamura I, Yang JF, Takaesu Y, Fujita M, Nomoto K, Mitsuyama M. Antigen Provoking Gamma-Interferon Production in Response to Mycobacterium-Bovis Bcc and Functional Difference in T-Cell Responses to This Antigen between Viable and Killed Bcg-Immunized Mice. Infection and immunity. 1994;62(10):4396–403.

    PubMed  CAS  Google Scholar 

  5. Orme I. Induction of nonspecific acquired resistance and delayed-type hypersensitivity, but not specific acquired resistance in mice inoculated with killed mycobacterial vaccines. Infection and immunity. 1988;56(12):3310–2.

    PubMed  CAS  Google Scholar 

  6. von Koenig CH, Finger H, Hof H. Failure of killed Listeria monocytogenes vaccine to produce protective immunity. Nature. 1982;297(5863):233–4. Epub 1982 May 20.

    Google Scholar 

  7. Brockstedt DG, Bahjat KS, Giedlin MA, Liu W, Leong M, Luckett W, et al. Killed but metabolically active microbes: a new vaccine paradigm for eliciting effector T-cell responses and protective immunity. Nat Med. 2005;11(8):853–60. Epub 2005 Jul 26.

    Google Scholar 

  8. Jomaa H, Feurle J, Luhs K, Kunzmann V, Tony HP, Herderich M, et al. Vgamma9/Vdelta2 T cell activation induced by bacterial low molecular mass compounds depends on the 1-deoxy-D-xylulose 5-phosphate pathway of isoprenoid biosynthesis. FEMS immunology and medical microbiology. 1999;25(4):371–8. Epub 1999 Aug 25.

    Google Scholar 

  9. Pamer EG. Immune responses to Listeria monocytogenes. Nat Rev Immunol. 2004;4(10):812–23. Epub 2004 Oct 02.

    Google Scholar 

  10. van de Loo AA, Arntz OJ, Bakker AC, van Lent PL, Jacobs MJ, van den Berg WB. Role of interleukin 1 in antigen-induced exacerbations of murine arthritis. Am J Pathol. 1995;146(1):239–49. Epub 1995 Jan 01.

    Google Scholar 

  11. Vance RE, Isberg RR, Portnoy DA. Patterns of pathogenesis: discrimination of pathogenic and nonpathogenic microbes by the innate immune system. Cell Host Microbe. 2009;6(1):10–21. Epub 2009 Jul 21.

    Google Scholar 

  12. Detmer A, Glenting J. Live bacterial vaccines–a review and identification of potential hazards. Microb Cell Fact. 2006;5:23. Epub 2006 Jun 27.

    Google Scholar 

  13. Sander LE, Davis MJ, Boekschoten MV, Amsen D, Dascher CC, Ryffel B, et al. Detection of prokaryotic mRNA signifies microbial viability and promotes immunity. Nature. 2011;474(7351):385–9. Epub 2011 May 24.

    Google Scholar 

  14. Luker KE, Tyler AN, Marshall GR, Goldman WE. Tracheal cytotoxin structural requirements for respiratory epithelial damage in pertussis. Mol Microbiol. 1995;16(4):733–43. Epub 1995 May 01.

    Google Scholar 

  15. Flak TA, Heiss LN, Engle JT, Goldman WE. Synergistic epithelial responses to endotoxin and a naturally occurring muramyl peptide. Infect Immun. 2000;68(3):1235–42. Epub 2000 Feb 26.

    Google Scholar 

  16. Magalhaes JG, Philpott DJ, Nahori MA, Jehanno M, Fritz J, Le Bourhis L, et al. Murine Nod1 but not its human orthologue mediates innate immune detection of tracheal cytotoxin. EMBO Rep. 2005;6(12):1201–7. Epub 2005 Oct 08.

    Google Scholar 

  17. Hintz M, Reichenberg A, Altincicek B, Bahr U, Gschwind R, Kollas A, et al. Identification of (E)-4-hydroxy-3-methyl-but-2-enyl pyrophosphate as a major activator for human gammadelta T cells in Escherichia coli. FEBS letters. 2001;509(2):317–39.

    Article  PubMed  CAS  Google Scholar 

  18. Zimmermann S, Wagner C, Muller W, Brenner-Weiss G, Hug F, Prior B, et al. Induction of neutrophil chemotaxis by the quorum-sensing molecule N-(3-oxododecanoyl)-L-homoserine lactone. Infect Immun. 2006;74(10):5687–92. Epub 2006 Sep 22.

    Google Scholar 

  19. Karaolis DKR, Means TK, Yang D, Takahashi M, Yoshimura T, Muraille E, et al. Bacterial c-di-GMP is an immunostimulatory molecule. Journal of Immunology. 2007;178(4):2171–81.

    CAS  Google Scholar 

  20. McWhirter SM, Barbalat R, Monroe KM, Fontana MF, Hyodo M, Joncker NT, et al. A host type I interferon response is induced by cytosolic sensing of the bacterial second messenger cyclic-di-GMP. J Exp Med. 2009;206(9):1899–911. Epub 2009 Aug 05.

    Google Scholar 

  21. Woodward JJ, Iavarone AT, Portnoy DA. c-di-AMP secreted by intracellular Listeria monocytogenes activates a host type I interferon response. Science. 2010;328(5986):1703–5. Epub 2010 May 29.

    Google Scholar 

  22. Heuston S, Begley M, Gahan CG, Hill C. Isoprenoid biosynthesis in bacterial pathogens. Microbiology. 2012;158(Pt 6):1389–401. Epub 2012 Apr 03.

    Google Scholar 

  23. Eberl M, Hintz M, Reichenberg A, Kollas AK, Wiesner J, Jomaa H. Microbial isoprenoid biosynthesis and human gammadelta T cell activation. FEBS Lett. 2003;544(1–3):4–10. Epub 2003 Jun 05.

    Google Scholar 

  24. Donabedian H. Quorum sensing and its relevance to infectious diseases. J Infect. 2003;46(4):207–14. Epub 2003 Jun 12.

    Google Scholar 

  25. Tamayo R, Pratt JT, Camilli A. Roles of cyclic diguanylate in the regulation of bacterial pathogenesis. Annu Rev Microbiol. 2007;61:131–48. Epub 2007 May 08.

    Google Scholar 

  26. Burdette DL, Monroe KM, Sotelo-Troha K, Iwig JS, Eckert B, Hyodo M, et al. STING is a direct innate immune sensor of cyclic di-GMP. Nature. 2011;478(7370):515–8. Epub 2011 Sep 29.

    Google Scholar 

  27. Hornung V, Ellegast J, Kim S, Brzozka K, Jung A, Kato H, et al. 5′-Triphosphate RNA is the ligand for RIG-I. Science. 2006;314(5801):994–7. Epub 2006 Oct 14.

    Google Scholar 

  28. Pichlmair A, Schulz O, Tan CP, Naslund TI, Liljestrom P, Weber F, et al. RIG-I-mediated antiviral responses to single-stranded RNA bearing 5′-phosphates. Science. 2006;314(5801):997–1001. Epub 2006 Oct 14.

    Google Scholar 

  29. Buchmeier NA, Heffron F. Induction of Salmonella Stress Proteins Upon Infection of Macrophages. Science. 1990;248(4956):730–2.

    Article  PubMed  CAS  Google Scholar 

  30. Davila Lopez M, Samuelsson T. Early evolution of histone mRNA 3′ end processing. RNA. 2008;14(1):1–10. Epub 2007 Nov 14.

    Google Scholar 

  31. Martinon F, Mayor A, Tschopp J. The inflammasomes: guardians of the body. Annu Rev Immunol. 2009;27:229–65. Epub 2009 Mar 24.

    Google Scholar 

  32. Kanneganti TD, Ozoren N, Body-Malapel M, Amer A, Park JH, Franchi L, et al. Bacterial RNA and small antiviral compounds activate caspase-1 through cryopyrin/Nalp3. Nature. 2006;440(7081):233–6. Epub 2006 Jan 13.

    Google Scholar 

  33. Zhang Z, Kim T, Bao M, Facchinetti V, Jung SY, Ghaffari AA, et al. DDX1, DDX21, and DHX36 helicases form a complex with the adaptor molecule TRIF to sense dsRNA in dendritic cells. Immunity. 2011;34(6):866–78. Epub 2011 Jun 28.

    Google Scholar 

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Authors and Affiliations

  1. Department of Medicine, Immunology Institute, Mount Sinai School of Medicine, 1425 Madison Avenue, 12-20D, New York, NY, 10029, USA

    Diego Mourao-Sa, Soumit Roy & J. Magarian Blander

Authors
  1. Diego Mourao-Sa
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  2. Soumit Roy
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  3. J. Magarian Blander
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Correspondence to J. Magarian Blander .

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Editors and Affiliations

  1. College of Medicine, Department Microbiology & Immunology, Drexel University, Queen Lane 2900, Philadelphia, 19129, Pennsylvania, USA

    Peter D. Katsikis

  2. , Laboratory of Cellular Immunology, La Jolla Institute for Allergy and Immun, Athena Circle 9420, La Jolla, 92037, USA

    Stephen P. Schoenberger

  3. Emory Vaccine Center &, Yerkes National Primate Research Center, Emory University, Gatewood Rd. 954, Atlanta, 30329, Georgia, USA

    Bali Pulendran

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Mourao-Sa, D., Roy, S., Blander, J.M. (2013). Vita-PAMPs: Signatures of Microbial Viability. In: Katsikis, P., Schoenberger, S., Pulendran, B. (eds) Crossroads Between Innate and Adaptive Immunity IV. Advances in Experimental Medicine and Biology, vol 785. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-6217-0_1

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