medigraphic.com
ISSN 2395-8723 (Electronic)
ISSN 1405-888X (Print)
TIP Revista Especializada en Ciencias Químico-Biológicas

2018, Number S1

<< Back Next >>

TIP Rev Esp Cienc Quim Biol 2018; 21 (S1)

Innate immune memory, the missing piece of the immunological response

Pérez-Vázquez D, Contreras-Castillo E, Licona-Limón P

Language: English
References: 60
Page: 112-123
PDF size: 538.73 Kb.


ABSTRACT

In the last decade, growing evidence has shed some light into an unrecognized capacity of the innate immune compartment: the unexpected ability of innate cells to enhance its response upon an immunological re-challenge. This capacity is called Trained immunity and resembles adaptive immune memory but lacks the specificity of antigen recognition by lymphocytes. Mechanistically, this type of memory or trained immunity, unlike somatic recombination or hypermutation of antigen-specific receptors in the adaptive memory; depends on pattern recognition receptors and metabolic changes that lead to long-term modifications on the epigenetic landscape, poising chromatin to readily express inflammatory cytokines upon a pathogenic re-challenge. In this review we will summarize and discuss the current progress made at elucidating the different innate cell populations with memory-like features, their receptors, downstream molecules and effector cytokines involved in the development and maintenance of trained immunity. This novel evidence overrides a very important dogma in immunology dissolving the boundaries separating innate and adaptive compartments of the immune system, and sets immunological memory as a shared mechanism of all immune cell types able to provide long-term protection to the host.


REFERENCES

  1. Abt, M.C., Osborne, L.C., Monticelli, L.A., Doering, T.A., Sonnenberg, G.F., Paley, M.A., Antenus, M., Katie, L., Erikson, J., Wherry, E.J., & Artis, D. (2012). Commensal Bacteria Calibrate the Activation Threshold of Innate Antiviral Immunity. Immunity, 37(1), 158–170. https://doi.org/10.1016/j.immuni.2012.04.011.Abt

  2. Arts, R.J.W., Carvalho, A., La Rocca, C., Palma, C., Rodrigues, F., Silvestre, R., Kleinnijenhuis, J., Lachmandas, E., Gonçalves, L.G., Belinha, A., Cunha, C., Oosting, M., Joosten, L.A.B., Matarese, G., van Crevel, R., & Netea, M.G. (2016). Immunometabolic Pathways in BCG-Induced Trained Immunity. Cell Reports, 17(10), 2562–2571. https://doi. org/10.1016/j.celrep.2016.11.011

  3. Arts, R.J.W., Moorlag, S.J.C.F.M., Novakovic, B., Li, Y., Wang, S.-Y., Oosting, M., Kumar, V., Xavier, R.J., Wijmenga, C., Joosten, L.A.B., Reusken, C.B.E.M., Benn, C.S., Aaby, P., Koopmans, M.P., Stunnenberg, H.G., van Crevel, R., & Netea, M.G. (2018). BCG Vaccination Protects against Experimental Viral Infection in Humans through the Induction of Cytokines Associated with Trained Immunity. Cell Host & Microbe, 23(1), 89–100.e5. https://doi.org/10.1016/j.chom.2017.12.010

  4. Arya, R., & Bassing, C.H. (2017). V(D)J Recombination Exploits DNA Damage Responses to Promote Immunity. Trends in Genetics, 33(7), 479–489. https://doi.org/10.1016/j.tig.2017.04.006 Barrangou, R., & Marraffini, L.A. (2014). CRISPR-cas systems: Prokaryotes upgrade to adaptive immunity. Molecular Cell. https://doi.org/10.1016/j.molcel.2014.03.011

  5. Barton, E.S., White, D.W., Cathelyn, J.S., Brett-McClellan, K.A., Engle, M., Diamond, M.S., Miller, V.L., & Virgin IV, H.W. (2007). Herpesvirus latency confers symbiotic protection from bacterial infection. Nature, 447(7142), 326–329. https://doi. org/10.1038/nature05762

  6. Bekkering, S., Arts, R.J.W., Novakovic, B., Kourtzelis, I., van der Heijden, C.D.C.C., Li, Y., Popa, C.D., ter Horst, R., van Tuijl, J., Netea-Maier, R.T., van de Veerdonk, F.L., Chavakis, T., Joosten, L.A.B., van der Meer, J.W.M., Stunnenberg, H., Riksen, N.P., & Netea, M.G. (2018). Metabolic Induction of Trained Immunity through the Mevalonate Pathway. Cell, 172(1–2), 135–146. e9. https://doi.org/10.1016/j.cell.2017.11.025

  7. 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(2), 668–674.

  8. 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 nonspecific anti-infectious protection. Medical Mycology, 26(5), 285–299. https://doi. org/10.1080/02681218880000401

  9. Boehm, T. (2012). Evolution of vertebrate immunity. Current Biology, 22(17), R722–R732. https://doi.org/10.1016/j.cub.2012.07.003

  10. Bouchery, T., Kyle, R., Camberis, M., Shepherd, A., Filbey, K., Smith, A., Harvie, M., Painter, G., Johnston, K., Ferguson, P., Jain, R., Roediger, B., Delahunt, B., Weninger, W., Forbes-Blom, E., & Le Gros, G. (2015). ILC2s and T cells cooperate to ensure maintenance of M2 macrophages for lung immunity against hookworms. Nature Communications, 6, 1–13. https://doi. org/10.1038/ncomms7970

  11. Bowdish, D.M.E., Loffredo, M.S., Mukhopadhyay, S., Mantovani, A., & Gordon, S. (2007). Macrophage receptors implicated in the “adaptive” form of innate immunity. Microbes and Infection, 9(14–15), 1680–1687. https://doi.org/10.1016/j. micinf.2007.09.002

  12. Burgess, S.L., Gilchrist, C.A., Lynn, T.C., & Petri, W.A. (2017). Parasitic protozoa and interactions with the host intestinal microbiota. Infection and Immunity. https://doi.org/10.1128/IAI.00101-17

  13. Burgess, S.L., & Petri, W.A. (2016). The Intestinal Bacterial Microbiome and E. histolytica Infection. Current Tropical Medicine Reports, 3(3), 71–74. https://doi.org/10.1007/ s40475-016-0083-1

  14. Chen, F., Wu, W., Millman, A., Craft, J.F., Chen, E., Patel, N., Boucher, J.L., Urban, J.F., Kim, C.C., & Gause, W.C. (2014). Neutrophils prime a long-lived effector macrophage phenotype that mediates accelerated helminth expulsion. Nature Immunology, 15(10), 938–946. https://doi.org/10.1038/ni.2984

  15. Christ, A., Günther, P., Lauterbach, M.A.R., Duewell, P., Biswas, D., Pelka, K., Scholz, C.J., Oosting, M., Haendler, K., Baßler, K., Klee, K., Schulte-Schrepping, J., Ulas, T., Moorlag, S.J.C.F.M., Kumar, V., Park, M.H., Joosten, L.A.B., Groh, L.A., Riksen, N.P., Espevik, T., Schlitzer, A., Li, Y., Fitzgerald, M.L., Netea, M.G., Schultze, J.L., & Latz, E. (2018). Western Diet Triggers NLRP3-Dependent Innate Immune Reprogramming. Cell, 172(1–2), 162–175.e14. https://doi.org/10.1016/j. cell.2017.12.013

  16. Denzel, A., Maus, U.A., Gomez, M.R., Moll, C., Niedermeier, M., Winter, C., Maus, R., Hollingshead, S., Briles, D.E., Kunz-Schughart, L.A., Talke, Y., & Mack, M. (2008). Basophils enhance immunological memory responses. Nature Immunology, 9(7), 733–742. https://doi.org/10.1038/ni.1621

  17. Fehniger, T.A., & Cooper, M.A. (2016). Harnessing NK Cell Memory for Cancer Immunotherapy. Trends in Immunology, 37(12), 877–888. https://doi.org/10.1016/j.it.2016.09.005

  18. Fleming, B.D., & Mosser, D.M. (2011). Regulatory macrophages: Setting the threshold for therapy. European Journal of Immunology. https://doi.org/10.1002/eji.201141717 Ganal, S.C., Sanos, S.L., Kallfass, C., Oberle, K., Johner, C., Kirschning, C., Lienenklaus, S., Weiss, S., Staeheli, P., Aichele, P., & Diefenbach, A. (2012). Priming of Natural Killer Cells by Nonmucosal Mononuclear Phagocytes Requires Instructive Signals from Commensal Microbiota. Immunity, 37(1), 171–186. https://doi.org/10.1016/j.immuni.2012.05.020

  19. Glass, Z., Lee, M., Li, Y., & Xu, Q. (2018). Engineering the Delivery System for CRISPR-Based Genome Editing. Trends in Biotechnology, 36(2), 173–185. https://doi.org/10.1016/j. tibtech.2017.11.006

  20. Glatman Zaretsky, A., Engiles, J.B., & Hunter, C.A. (2014). Infectioninduced changes in hematopoiesis. J. Immunol., 192(1), 27–33. https://doi.org/10.4049/jimmunol.1302061

  21. Grainger, J.R., & Grencis, R.K. (2014). Neutrophils worm their way into macrophage long-term memory. Nature Immunology, 15(10), 902–904. https://doi.org/10.1038/ni.2990

  22. Honda, K., & Littman, D.R. (2012). The Microbiome in Infectious Disease and Inflammation. Annual Review of Immunology, 30(1), 759–795. https://doi.org/10.1146/annurevimmunol- 020711-074937

  23. Josefsdottir, K.S., Baldridge, M.T., Kadmon, C.S., & King, K.Y. (2017). Antibiotics impair murine hematopoiesis by depleting the intestinal microbiota. Blood, 129(6), 729–739. https://doi. org/10.1182/blood-2016-03-708594

  24. Kaufmann, E., Sanz, J., Dunn, J.L., Khan, N., Mendonça, L.E., Pacis, A., Tzelepis, F., Pernet, E., Dumaine, A., Grenier, J.-C., Mailhot-Léonard, F., Ahmed, E., Belle, J., Besla, R., Mazer, B., King, I.L., Nijnik, A., Robbins, C.S., Barreiro, L.B., & Divangahi, M. (2018). BCG Educates Hematopoietic Stem Cells to Generate Protective Innate Immunity against Tuberculosis. Cell, 172(1–2), 176–190.e19. https://doi. org/10.1016/j.cell.2017.12.031

  25. Kawabe, T., Jankovic, D., Kawabe, S., Huang, Y., Lee, P.-H., Yamane, H., Zhu, J., Sher, A., Germain, R.N., & Paul, W.E. (2017). Memory-phenotype CD4+ T cells spontaneously generated under steady-state conditions exert innate TH1-like effector function. Science Immunology, 2(12). https://doi.org/10.1126/ sciimmunol.aam9304

  26. Kelly, B., & O’Neill, L.A.J. (2015). Metabolic reprogramming in macrophages and dendritic cells in innate immunity. Cell Research, 25(7), 771–784. https://doi.org/10.1038/cr.2015.68

  27. Khosravi, A., Yáñez, A., Price, J.G., Chow, A., Merad, M., & Helen, S. (2014). Gut microbiota promotes hematopoiesis to control bacterial infection. Cell Host Microbiome, 15(3), 374–381. https://doi.org/10.1016/j.chom.2014.02.006.Gut

  28. Kleinnijenhuis, J., Quintin, J., Preijers, F., Joosten, L.A.B., Ifrim, D.C., Saeed, S., Jacobs, C., van Loenhout, J., de Jong, D., Stunnenberg, H.G., Xavier, R.J., van der Meer, J.W.M., van Crevel, R., & Netea, M.G. (2012). Bacille Calmette-Guerin induces NOD2-dependent nonspecific protection from reinfection via epigenetic reprogramming of monocytes. Proceedings of the National Academy of Sciences, 109(43), 17537–17542. https://doi.org/10.1073/pnas.1202870109

  29. La Scola, B., Desnues, C., Pagnier, I., Robert, C., Barrassi, L., Fournous, G., Merchat, M., Suzan-Monti, M., Forterre, P., Koonin, E., & Raoult, D. (2008). The virophage as a unique parasite of the giant mimivirus. Nature, 455(7209), 100–104. https://doi. org/10.1038/nature07218

  30. Leary, J.G.O., Goodarzi, M., Drayton, D.L., & Andrian, U.H. Von. (2006). T cell – and B cell – independent adaptive immunity mediated by natural killer cells, 7(5), 507–516. https://doi. org/10.1038/ni1332

  31. Levasseur, A., Bekliz, M., Chabrière, E., Pontarotti, P., La Scola, B., & Raoult, D. (2016). MIMIVIRE is a defence system in mimivirus that confers resistance to virophage. Nature, 531(7593), 249–252. https://doi.org/10.1038/nature17146

  32. Lynn, D.J., & Pulendran, B. (2017). The potential of the microbiota to influence vaccine responses. Journal of Leukocyte Biology, jlb.5MR0617-216R. https://doi.org/10.1189/jlb.5MR0617- 216R

  33. Mack, M., Schneider, M. a, Moll, C., Cihak, J., Brühl, H., Ellwart, J.W., Hogarth, M.P., Stangassinger, M., & Schlöndorff, D. (2005). Identification of antigen-capturing cells as basophils. Journal of Immunology (Baltimore, Md. : 1950), 174(2), 735–741. https://doi.org/10.4049/jimmunol.174.2.735

  34. Madera, S., & Sun, J.C. (2015). Cutting Edge: Stage-Specific Requirement of IL-18 for Antiviral NK Cell Expansion. The Journal of Immunology, 194(4), 1408–1412. https://doi. org/10.4049/jimmunol.1402001

  35. Martinez-Gonzalez, I., Mathä, L., Steer, C.A., Ghaedi, M., Poon, G.F.T., & Takei, F. (2016). Allergen-Experienced Group 2 Innate Lymphoid Cells Acquire Memory-like Properties and Enhance Allergic Lung Inflammation. Immunity, 45(1), 198–208. https:// doi.org/10.1016/j.immuni.2016.06.017

  36. Mitroulis, I., Ruppova, K., Wang, B., Chen, L.-S., Grzybek, M., Grinenko, T., Eugster, A., Troullinaki, M., Palladini, A., Kourtzelis, I., Chatzigeorgiou, A., Schlitzer, A., Beyer, M., Joosten, L.A.B., Isermann, B., Lesche, M., Petzold, A., Simons, K., Henry, I., Dahl, A., Schultze, J.L., Wielockx, B., Zamboni, N., Mirtschink, P., Coskun, Ü., Hajishengallis, G., Netea, M.G., & Chavakis, T. (2018). Modulation of Myelopoiesis Progenitors Is an Integral Component of Trained Immunity. Cell, 172(1–2), 147–161.e12. https://doi.org/10.1016/j.cell.2017.11.034

  37. Monticelli, S., & Natoli, G. (2013). perspective Short-term memory of danger signals and environmental stimuli in immune cells, 14(8). https://doi.org/10.1038/ni.2636

  38. Mosser, D.M., & Edwards, J.P. (2008). Exploring the full spectrum of macrophage activation. Nature Reviews Immunology. https:// doi.org/10.1038/nri2448

  39. Murphy, K. (2014). Janeway’s immunobiology. Igarss 2014. https:// doi.org/10.1007/s13398-014-0173-7.2

  40. Murray, P.J., & Wynn, T.A. (2011). Protective and pathogenic functions of macrophage subsets. Nature Reviews Immunology. https:// doi.org/10.1038/nri3073

  41. Nabekura, T., Girard, J.-P., & Lanier, L.L. (2015). IL-33 receptor ST2 amplifies the expansion of NK cells and enhances host defense during mouse cytomegalovirus infection. Journal of Immunology (Baltimore, Md. : 1950), 194(12), 5948–5952. https://doi.org/10.4049/jimmunol.1500424

  42. Nabekura, T., Kanaya, M., Shibuya, A., Fu, G., Gascoigne, N.R.J., & Lanier, L.L. (2014). Costimulatory Molecule DNAM-1 Is Essential for Optimal Differentiation of Memory Natural Killer Cells during Mouse Cytomegalovirus Infection. Immunity, 40(2), 225–234. https://doi.org/10.1016/j.immuni.2013.12.011

  43. Naeslund, C. (1931). Expérience de vaccination par le BCG dans la province du Norrbotten (Suède). Revue de La Tuberculose.

  44. Naik, S., Larsen, S.B., Gomez, N.C., 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(7677), 475–480. https://doi. org/10.1038/nature24271

  45. Netea, M.G., Quintin, J., & Van Der Meer, J.W.M. (2011). Trained immunity: A memory for innate host defense. Cell Host and Microbe, 9(5), 355–361. https://doi.org/10.1016/j. chom.2011.04.006 O’Sullivan, T.E., & Sun, J.C. (2015). Generation of Natural Killer Cell Memory during Viral Infection. Journal of Innate Immunity, 7(6), 557–562. https://doi.org/10.1159/000375494

  46. Ohnmacht & Voehringer, D.C. (2010). Basophils protect against reinfection with hookworms independently of mast cells and memory Th2 cells. The Journal of Immunology, 184(1), 344–350. https://doi.org/10.4049/jimmunol.0901841

  47. Paust, S., Gill, H.S., Wang, B.Z., Flynn, M.P., Moseman, E.A., Senman, B., Szczepanik, M., Telenti, A., Askenase, P.W., Compans, R.W., & Von Andrian, U.H. (2010). Critical role for the chemokine receptor CXCR6 in NK cell-mediated antigenspecific memory of haptens and viruses. Nature Immunology, 11(12), 1127–1135. https://doi.org/10.1038/ni.1953

  48. Quintin, J., Saeed, S., Martens, J.H.A., Giamarellos-Bourboulis, E.J., Ifrim, D.C., Logie, C., Jacobs, L., Jansen, T., Kullberg, B.J., Wijmenga, C., Joosten, L.A.B., Xavier, R.J., Van Der Meer, J.W.M., Stunnenberg, H.G., & Netea, M.G. (2012). Candida albicans infection affords protection against reinfection via functional reprogramming of monocytes. Cell Host and Microbe, 12(2), 223–232. https://doi.org/10.1016/j. chom.2012.06.006

  49. Rodrigues, J., Brayner, F.A., Alves, L.C., Dixit, R., & Barillasmury, C. (2010). Hemocyte Differentiation Mediates Innate Immune Memory in Anopheles gambiae Mosquitoes. Science, 329(5997), 1353–1355. https://doi.org/10.1126/ science.1190689.Hemocyte

  50. Rossato, M., Curtale, G., Tamassia, N., Castellucci, M., Mori, L., Gasperini, S., Mariotti, B., De Luca, M., Mirolo, M., Cassatella, M.A., Locati, M., & Bazzoni, F. (2012). IL-10-induced microRNA-187 negatively regulates TNF- , IL-6, and IL-12p40 production in TLR4-stimulated monocytes. Proceedings of the National Academy of Sciences, 109(45), E3101–E3110. https://doi.org/10.1073/pnas.1209100109

  51. Schwartz, C., & Voehringer, D. (2011). Basophils: Important emerging players in allergic and anti-parasite responses. BioEssays, 33(6), 423–426. https://doi.org/10.1002/bies.201100028

  52. Spits, H., Artis, D., Colonna, M., Diefenbach, A., Di Santo, J.P., Eberl, G., Koyasu, S., Locksley, R.M., McKenzie, A.N.J., Mebius, R.E., Powrie, F., & Vivier, E. (2013). Innate lymphoid cells-a proposal for uniform nomenclature. Nature Reviews Immunology, 13(2), 145–149. https://doi.org/10.1038/nri3365

  53. Sullivan, B.M., Liang, H.E., Bando, J.K., Wu, D., Cheng, L.E., McKerrow, J.K., Allen, C.D.C., & Locksley, R.M. (2011). Genetic analysis of basophil function in vivo. Nature Immunology, 12(6), 527–535. https://doi.org/10.1038/ni.2036

  54. Sun, J.C., Beilke, J.N., & Lanier, L.L. (2009). Adaptive immune features of natural killer cells. Nature, 457(7229), 557–561. https://doi.org/10.1038/nature07665

  55. Sun, J.C., Madera, S., Bezman, N.A., Beilke, J.N., Kaplan, M.H., & Lanier, L.L. (2012). Proinflammatory cytokine signaling required for the generation of natural killer cell memory. The Journal of Experimental Medicine, 209(5), 947–954. https:// doi.org/10.1084/jem.20111760

  56. Tauber, A.I. (2003). Metchnikoff and the phagocytosis theory. Nature Reviews Molecular Cell Biology, 4(11), 897–901. https://doi. org/10.1038/nrm1244

  57. Tribouley, J., Tribouley-Duret, J., & Appriou, M. (1978). [Effect of Bacillus Callmette Guerin (BCG) on the receptivity of nude mice to Schistosoma mansoni]. Comptes Rendus Des Seances de La Societe de Biologie et de Ses Filiales, 172(5), 902–904.

  58. Van’t wout, J.W., Poell, R., & Van furth, R. (1992). The Role of BCG / PPD-Activated Maerophages in Resistance against Systemie Candidiasis in Miee, 713–719.

  59. Wang, N., Liang, H., & Zen, K. (2014). Molecular mechanisms that influence the macrophage M1-M2 polarization balance. Frontiers in Immunology. https://doi.org/10.3389/ fimmu.2014.00614

  60. Wendeln, A., Degenhardt, K., Kaurani, L., Gertig, M., Ulas, T., Jain, G., Wagner, J., Häsler, L.M., Wild, K., Skodras, A., Blank, T., Staszewski, O., Datta, M., Centeno, T.P., Capece, V., Islam, R., Kerimoglu, C., & Staufenbiel, M. (2018). Innate immune memory in the brain shapes neurological disease hallmarks. Nature. https://doi.org/10.1038/s41586-018-0023-4




2020     |     www.medigraphic.com