The case for an expanded concept of trained immunity

mBio

Volumn 9, Issue 3, 2018, Pages

  Cassone, Antonio ^a  

^a UNIVERSITY OF PERUGIA   (Italy)

Author keywords

Candida; Immunity; Inflammation; Innate

Indexed keywords

INFLAMMASOME; CYTOKINE;

ADAPTIVE IMMUNITY; ARTICLE; BACILLUS THURINGIENSIS; BACTERIAL CELL; BACTERIAL TRANSMISSION; CANDIDA ALBICANS; CELL EXPANSION; CELL LINEAGE; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; EPIGENETICS; EPITHELIUM CELL; FUNGAL STRAIN; HUMAN; IMMUNOLOGICAL TOLERANCE; IMMUNOMODULATION; INFLAMMATORY DISEASE; INNATE IMMUNITY; MEMORY CELL; NONHUMAN; PRIORITY JOURNAL; STAPHYLOCOCCUS AUREUS; ANIMAL; FEMALE; GENETICS; IMMUNOLOGY; MICROBIOLOGY; NATURAL KILLER CELL; PHYSIOLOGY; VAGINA CANDIDIASIS;

ADAPTIVE IMMUNITY; ANIMALS; CANDIDA ALBICANS; CANDIDIASIS, VULVOVAGINAL; CYTOKINES; FEMALE; HUMANS; IMMUNITY, INNATE; KILLER CELLS, NATURAL;

EID: 85047522834     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00570-18     Document Type: Article

References (42)

1. Locati M, Mantovani A, Sica A. 2013. Macrophage activation and polarization as an adaptive component of innate immunity. Adv Immunol 120:163-184. https://doi.org/10.1016/B978-0-12-417028-5.00006-5.
2. Kurtz J. 2005. Specific memory within innate immune systems. Trends Immunol 26:186-192. https://doi.org/10.1016/j.it.2005.02.001.
3. Netea MG, Quintin J, van der Meer JW. 2011. Trained immunity: a memory for innate host defense. Cell Host Microbe 9:355-361. https://doi.org/10.1016/j.chom.2011.04.006.
4. Netea MG. 2013. Training innate immunity: the changing concept of immunological memory in innate host defense. Eur J Clin Invest 43: 881-884. https://doi.org/10.1111/eci.12132.
5. Netea MG, Joosten LA, Latz E, Mills KH, Natoli G, Stunnenberg HG, O’Neill LA, Xavier RJ. 2016. Trained immunity: a program of innate immune memory in health and disease. Science 352:aaf1098. https://doi.org/10.1126/science.aaf1098.
6. Kurtz J, Franz K. 2003. Innate defence: evidence for memory in invertebrate immunity. Nature 425:37-38. https://doi.org/10.1038/425037a.
7. Tero A, Takagi S, Saigusa T, Ito K, Bebber DP, Fricker MD, Yumiki K, Kobayashi R, Nakagaki T. 2010. Rules for biologically inspired adaptive network design. Science 327:439-442. https://doi.org/10.1126/science.1177894.
8. Gagliano M, Renton M, Depczynski M, Mancuso S. 2014. Experience teaches plants to learn faster and forget slower in environments where it matters. Oecologia 175:63-72. https://doi.org/10.1007/s00442-013-2873-7.
9. Saeed S, Quintin J, Kerstens HH, Rao NA, Aghajanirefah A, Matarese F, Cheng SC, Ratter J, Berentsen K, van der Ent MA, Sharifi N, Janssen-Megens EM, Ter Huurne M, Mandoli A, van Schaik T, Ng A, Burden F, Downes K, Frontini M, Kumar V, Giamarellos-Bourboulis EJ, Ouwehand WH, van der Meer JW, Joosten LA, Wijmenga C, Martens JH, Xavier RJ, Logie C, Netea MG, Stunnenberg HG. 2014. Epigenetic programming of monocyte-to-macrophage differentiation and trained innate immunity. Science 345:1251086. https://doi.org/10.1126/science.1251086.
10. De Santa F, Totaro MG, Prosperini E, Notarbartolo S, Testa G, Natoli G. 2007. The histone H3 lysine-27 demethylase Jmjd3 links inflammation to inhibition of polycomb-mediated gene silencing. Cell 130:1083-1094. https://doi.org/10.1016/j.cell.2007.08.019.
11. Mitroulis I, Ruppova K, Wang B, Chen LS, Grzybek M, Grinenko T, Eugster A, Troullinaki M, Palladini A, Kourtzelis I, Chatzigeorgiou A, Schlitzer A, Beyer M, Joosten LAB, Isermann B, Lesche M, Petzold A, Simons K, Henry I, Dahl A, Schultze JL, Wielockx B, Zamboni N, Mirtschink P, Coskun Ü, Hajishengallis G, Netea MG, Chavakis T. 2018. Modulation of myelopoiesis progenitors is an integral component of trained immunity. Cell 172:147-161.e12. https://doi.org/10.1016/j.cell.2017.11.034.
12. Flanagan KL, van Crevel R, Curtis N, Shann F, Levy O, Optimmunize Network. 2013. Heterologous (“nonspecific”) and sex-differential effects of vaccines: epidemiology, clinical trials, and emerging immunologic mechanisms. Clin Infect Dis 57:283-289. https://doi.org/10.1093/cid/cit209.
13. Kaufmann E, Sanz J, Dunn JL, Khan N, Mendonça LE, Pacis A, Tzelepis F, Pernet E, Dumaine A, Grenier JC, Mailhot-Léonard F, Ahmed E, Belle J, Besla R, Mazer B, King IL, Nijnik A, Robbins CS, Barreiro LB, Divangahi M. 2018. BCG educates hematopoietic stem cells to generate protective innate immunity against tuberculosis. Cell 172:176-190.e19. https://doi.org/10.1016/j.cell.2017.12.031.
14. Haley MJ, Brough D, Quintin J, Allan SM. 2017. Microglial priming as trained immunity in the brain. Neuroscience https://doi.org/10.1016/j.neuroscience.2017.12.039.
15. Bistoni F, Vecchiarelli A, Cenci E, Puccetti P, Marconi P, Cassone A. 1986. Evidence for macrophage-mediated protection against lethal Candida albicans infection. Infect Immun 51:668-674.
16. Bistoni F, Verducci G, Perito S, Vecchiarelli A, Puccetti P, Marconi P, Cassone A. 1988. Immunomodulation by a low-virulence, agerminative variant of Candida albicans. Further evidence for macrophage activation as one of the effector mechanisms of non-specific anti-infectious protection. J Med Vet Mycol 26:285-299. https://doi.org/10.1080/02681218880000401.
17. Vecchiarelli A, Cenci E, Puliti M, Blasi E, Puccetti P, Cassone A, Bistoni F. 1989. Protective immunity induced by low-virulence Candida albicans: cytokine production in the development of the anti-infectious state. Cell Immunol 124:334-344. https://doi.org/10.1016/0008-8749(89)90135-4.
18. Mattia E, Carruba G, Angiolella L, Cassone A. 1982. Induction of germ tube formation by N-acetyl-D-glucosamine in Candida albicans: uptake of inducer and germinative response. J Bacteriol 152:555-562.
19. Quintin J, Saeed S, Martens JHA, Giamarellos-Bourboulis EJ, Ifrim DC, Logie C, Jacobs L, Jansen T, Kullberg BJ, Wijmenga C, Joosten LAB, Xavier RJ, van der Meer JWM, Stunnenberg HG, Netea MG. 2012. Candida albicans infection affords protection against reinfection via functional reprogramming of monocytes. Cell Host Microbe 12:223-232. https://doi.org/10.1016/j.chom.2012.06.006.
20. Moorlag SJCFM, Röring RJ, Joosten LAB, Netea MG. 2018. The role of the interleukin-1 family in trained immunity. Immunol Rev 281:28-39. https://doi.org/10.1111/imr.12617.
21. Goodridge HS, Ahmed SS, Curtis N, Kollmann TR, Levy O, Netea MG, Pollard AJ, van Crevel R, Wilson CB. 2016. Harnessing the beneficial heterologous effects of vaccination. Nat Rev Immunol 16:392-400. https://doi.org/10.1038/nri.2016.43.
22. Tate AT, Andolfatto P, Demuth JP, Graham AL. 2017. The within-host dynamics of infection in trans-generationally primed flour beetles. Mol Ecol 26:3794-3807. https://doi.org/10.1111/mec.14088.
23. Garcia-Valtanen P, Guzman-Genuino RM, Williams DL, Hayball JD, Diener KR. 2017. Evaluation of trained immunity by β-1, 3(d)-glucan on murine monocytes in vitro and duration of response in vivo. Immunol Cell Biol 95:601-610. https://doi.org/10.1038/icb.2017.13.
24. Rizzetto L, Ifrim DC, Moretti S, Tocci N, Cheng SC, Quintin J, Renga G, Oikonomou V, De Filippo C, Weil T, Blok BA, Lenucci MS, Santos MA, Romani L, Netea MG, Cavalieri D. 2016. Fungal chitin induces trained immunity in human monocytes during cross-talk of the host with Saccharomyces cerevisiae. J Biol Chem 291:7961-7972. https://doi.org/10.1074/jbc.M115.699645.
25. Cassone A, Vecchiarelli A, Hube B. 2016. Aspartyl proteinases of eukaryotic microbial pathogens: from eating to heating. PLoS Pathog 12: e1005992. https://doi.org/10.1371/journal.ppat.1005992.
26. Richardson JP, Willems HME, Moyes DL, Shoaie S, Barker KS, Tan SL, Palmer GE, Hube B, Naglik JR, Peters BM. 2018. Candidalysin drives epithelial signaling, neutrophil recruitment, and immunopathology at the vaginal mucosa. Infect Immun 86:e00645-17. https://doi.org/10.1128/IAI.00645-17.
27. Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, Hsu PD, Wu X, Jiang W, Marraffini LA, Zhang F. 2013. Multiplex genome engineering using CRISPR/Cas systems. Science 339:819-823. https://doi.org/10.1126/science.1231143.
28. Drummond RA, Gaffen SL, Hise AG, Brown GD. 2014. Innate defense against fungal pathogens. Cold Spring Harb Perspect Med 5:a019620. https://doi.org/10.1101/cshperspect.a019620.
29. Barousse MM, Espinosa T, Dunlap K, Fidel PL, Jr. 2005. Vaginal epithelial cell anti-Candida albicans activity is associated with protection against symptomatic vaginal candidiasis. Infect Immun 73:7765-7767. https://doi.org/10.1128/IAI.73.11.7765-7767.2005.
30. Moyes DL, Murciano C, Runglall M, Islam A, Thavaraj S, Naglik JR. 2011. Candida albicans yeast and hyphae are discriminated by MAPK signaling in vaginal epithelial cells. PLoS One 6:e26580. https://doi.org/10.1371/journal.pone.0026580.
31. Gow NA, van de Veerdonk FL, Brown AJ, Netea MG. 2011. Candida albicans morphogenesis and host defence: discriminating invasion from colonization. Nat Rev Microbiol 10:112-122. https://doi.org/10.1038/nrmicro2711.
32. Roselletti E, Perito S, Gabrielli E, Mencacci A, Pericolini E, Sabbatini S, Cassone A, Vecchiarelli A. 2017. NLRP3 inflammasome is a key player in human vulvovaginal disease caused by Candida albicans. Sci Rep 7:17877. https://doi.org/10.1038/s41598-017-17649-8.
33. Lev-Sagie A, Prus D, Linhares IM, Lavy Y, Ledger WJ, Witkin SS. 2009. Polymorphism in a gene coding for the inflammasome component NALP3 and recurrent vulvovaginal candidiasis in women with vulvar vestibulitis syndrome. Am J Obstet Gynecol 200:303.e1-303.e6. https://doi.org/10.1016/j.ajog.2008.10.039.
34. Jaeger M, Carvalho A, Cunha C, Plantinga TS, van de Veerdonk F, Puccetti M, Galosi C, Joosten LA, Dupont B, Kullberg BJ, Sobel JD, Romani L, Netea MG. 2016. Association of a variable number tandem repeat in the NLRP3 gene in women with susceptibility to RVVC. Eur J Clin Microbiol Infect Dis 35:797-801. https://doi.org/10.1007/s10096-016-2600-5.
35. Bruno VM, Shetty AC, Yano J, Fidel PL, Jr, Noverr MC, Peters BM. 2015. Transcriptomic analysis of vulvovaginal candidiasis identifies a role for the NLRP3 inflammasome. mBio 6:e00182-15. https://doi.org/10.1128/mBio.00182-15.
36. Pericolini E, Gabrielli E, Amacker M, Kasper L, Roselletti E, Luciano E, Sabbatini S, Kaeser M, Moser C, Hube B, Vecchiarelli A, Cassone A. 2015. Secretory aspartyl proteinases cause vaginitis and can mediate vaginitis caused by Candida albicans in mice. mBio 6:e00724. https://doi.org/10.1128/mBio.00724-15.
37. Levy M, Thaiss CA, Zeevi D, Dohnalová L, Zilberman-Schapira G, Mahdi JA, David E, Savidor A, Korem T, Herzig Y, Pevsner-Fischer M, Shapiro H, Christ A, Harmelin A, Halpern Z, Latz E, Flavell RA, Amit I, Segal E, Elinav E. 2015. Microbiota-modulated metabolites shape the intestinal microenvironment by regulating NLRP6 inflammasome signaling. Cell 163: 1428-1443. https://doi.org/10.1016/j.cell.2015.10.048.
38. Naik S, Larsen SB, Gomez NC, Alaverdyan K, Sendoel A, Yuan S, Polak L, Kulukian A, Chai S, Fuchs E. 2017. Inflammatory memory sensitizes skin epithelial stem cells to tissue damage. Nature 550:475-480. https://doi.org/10.1038/nature24271.
39. Nasrollahi S, Walter C, Loza AJ, Schimizzi GV, Longmore GD, Pathak A. 2017. Past matrix stiffness primes epithelial cells and regulates their future collective migration through a mechanical memory. Biomaterials 146:146-155. https://doi.org/10.1016/j.biomaterials.2017.09.012.
40. Cassone A. 2013. Development of vaccines for Candida albicans: fighting a skilled transformer. Nat Rev Microbiol 11:884-891. https://doi.org/10.1038/nrmicro3156.
41. Yano J, Peters BM, Noverr MC, Fidel PL, Jr. 2018. Novel mechanism behind the immunopathogenesis of vulvovaginal candidiasis: “neutrophil anergy”. Infect Immun 86:e00684-17. https://doi.org/10.1128/IAI.00684-17.
42. Mowat AM. 28 February 2018. To respond or not to respond—a personal perspective of intestinal tolerance. Nat Rev Immunol https://doi.org/10.1038/s41577-018-0002-x.