1887

Chapter 38 : Adaptive Characteristics of Innate Immune Responses in Macrophages

Authors: Rob J. W. Arts1, Mihai G. Netea2
VIEW AFFILIATIONS HIDE AFFILIATIONS
Affiliations: 1: Department of Internal Medicine, Radboud University Medical Center, Nijmegen, The Netherlands; 2: Department of Internal Medicine, Radboud University Medical Center, Nijmegen, The Netherlands
Content Type: Monograph
Publication Year: 2017

Category: Microbial Genetics and Molecular Biology

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Preview Magnify
Zoom in
Zoomout

Adaptive Characteristics of Innate Immune Responses in Macrophages, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555819194/9781555819187_Chap38-1.gif /docserver/preview/fulltext/10.1128/9781555819194/9781555819187_Chap38-2.gif

Abstract:

Macrophages are a central component of antimicrobial host defense, described as being crucial for both innate immune mechanisms and adaptive immunity ( ). The dichotomy between the immediate antimicrobial responses seen as nonspecific and the relatively late-onset specific T- and B-cell responses has driven our understanding of host defense for more than half a century. Innate immunity reacts instantly upon an encounter with a pathogen but has been viewed as nonspecific and incapable of building immunological memory. In contrast, adaptive immune responses can specifically recognize pathogenic microorganisms and build memory capable of protection against reinfection. Macrophages are involved in both of these responses: on the one hand, macrophages have the capacity to phagocytose and kill microorganisms in a nonspecific fashion, as well as to release proinflammatory mediators that drive inflammation; but on the other hand, they can also present antigens and initiate and modulate the specific T-cell responses through expression of costimulatory molecules and specific cytokines ( ).

Citation: Arts R, Netea M. 2017. Adaptive Characteristics of Innate Immune Responses in Macrophages, p 679-686. In Gordon S (ed), Myeloid Cells in Health and Disease. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MCHD-0023-2015
Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Figures

Adaptive Characteristics of Innate Immune Responses in Macrophages
[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555819194.chap38-1,webId=/content/author/10.1128/9781555819194.chap38-1,properties={foaf_givenname=Rob J. W., foaf_name=Rob J. W. Arts, foaf_surname=Arts, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555819194.chap38-aff1]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555819194.chap38-2,webId=/content/author/10.1128/9781555819194.chap38-2,properties={foaf_givenname=Mihai G., foaf_name=Mihai G. Netea, foaf_surname=Netea, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555819194.chap38-aff2]]}]]
Citation: Arts R, Netea M. 2017. Adaptive Characteristics of Innate Immune Responses in Macrophages, p 679-686. In Gordon S (ed), Myeloid Cells in Health and Disease. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MCHD-0023-2015
/content/10.1128/9781555819194.chap38.fig38-1
Figure 1

Priming, activation, and tolerance as adaptive macrophage responses. A schematic representation of the possible responses of macrophages to a novel stimulus (e.g., LPS). While LPS causes macrophage activation followed by tolerance, low doses of LPS prime macrophages for enhanced innate immune responses: trained innate immunity. Both tolerance and trained innate immunity are results of long-term epigenetic changes in macrophage function (“memory”).

10.1128/9781555819194/fig38-1_thmb.gif
10.1128/9781555819194/fig38-1.gif
Image of Figure 1
Figure 1

Priming, activation, and tolerance as adaptive macrophage responses. A schematic representation of the possible responses of macrophages to a novel stimulus (e.g., LPS). While LPS causes macrophage activation followed by tolerance, low doses of LPS prime macrophages for enhanced innate immune responses: trained innate immunity. Both tolerance and trained innate immunity are results of long-term epigenetic changes in macrophage function (“memory”).

Citation: Arts R, Netea M. 2017. Adaptive Characteristics of Innate Immune Responses in Macrophages, p 679-686. In Gordon S (ed), Myeloid Cells in Health and Disease. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MCHD-0023-2015
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/10.1128/9781555819194.chap38.fig38-2
Figure 2

Macrophages play a double role in inducing immunological memory following an infectious insult: on the one hand, they initiate adaptive immune responses; and on the other hand, they undergo epigenetic reprogramming to respond with an increased array of PRR expression and inflammatory cytokine production to a secondary infection (“trained innate immunity”). MHC, major histocompatibility complex.

10.1128/9781555819194/fig38-2_thmb.gif
10.1128/9781555819194/fig38-2.gif
Image of Figure 2
Figure 2

Macrophages play a double role in inducing immunological memory following an infectious insult: on the one hand, they initiate adaptive immune responses; and on the other hand, they undergo epigenetic reprogramming to respond with an increased array of PRR expression and inflammatory cytokine production to a secondary infection (“trained innate immunity”). MHC, major histocompatibility complex.

Citation: Arts R, Netea M. 2017. Adaptive Characteristics of Innate Immune Responses in Macrophages, p 679-686. In Gordon S (ed), Myeloid Cells in Health and Disease. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MCHD-0023-2015
Permissions and Reprints Request Permissions
Download as Powerpoint

References

/content/book/10.1128/9781555819194.chap38
1. Gordon S,, Mantovani A . 2011. Diversity and plasticity of mononuclear phagocytes. Eur J Immunol 41 : 2470– 2472.[PubMed] [CrossRef]
2. Taylor PR,, Martinez-Pomares L,, Stacey M,, Lin HH,, Brown GD,, Gordon S . 2005. Macrophage receptors and immune recognition. Annu Rev Immunol 23 : 901– 944.[PubMed] [CrossRef]
3. Takeuchi O,, Akira S . 2010. Pattern recognition receptors and inflammation. Cell 140 : 805– 820.[PubMed] [CrossRef]
4. Mackaness GB . 1969. The influence of immunologically committed lymphoid cells on macrophage activity in vivo. J Exp Med 129 : 973– 992.[PubMed] [CrossRef]
5. Adams DO,, Hamilton TA . 1984. The cell biology of macrophage activation. Annu Rev Immunol 2 : 283– 318.[PubMed] [CrossRef]
6. Evans R,, Alexander P . 1970. Cooperation of immune lymphoid cells with macrophages in tumour immunity. Nature 228 : 620– 622.[PubMed] [CrossRef]
7. Bowdish DM,, Loffredo MS,, Mukhopadhyay S,, Mantovani A,, Gordon S . 2007. Macrophage receptors implicated in the “adaptive” form of innate immunity. Microbes Infect 9 : 1680– 1687.[PubMed] [CrossRef]
8. Netea MG,, Quintin J,, van der Meer JW . 2011. Trained immunity: a memory for innate host defense. Cell Host Microbe 9 : 355– 361.[PubMed] [CrossRef]
9. Durrant WE,, Dong X . 2004. Systemic acquired resistance. Annu Rev Phytopathol 42 : 185– 209.[PubMed] [CrossRef]
10. Pham LN,, Dionne MS,, Shirasu-Hiza M,, Schneider DS . 2007. A specific primed immune response in Drosophila is dependent on phagocytes. PLoS Pathog 3 : e26. doi:10.1371/journal.ppat.0030026.g001.
11. Kurtz J . 2005. Specific memory within innate immune systems. Trends Immunol 26 : 186– 192.[PubMed] [CrossRef]
12. Sun JC,, Beilke JN,, Lanier LL . 2009. Adaptive immune features of natural killer cells. Nature 457 : 557– 561.[PubMed] [CrossRef]
13. Paust S,, Gill HS,, Wang BZ,, Flynn MP,, Moseman EA,, Senman B,, Szczepanik M,, Telenti A,, Askenase PW,, Compans RW,, von Andrian UH . 2010. Critical role for the chemokine receptor CXCR6 in NK cell-mediated antigen-specific memory of haptens and viruses. Nat Immunol 11 : 1127– 1135.[PubMed] [CrossRef]
14. 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.[PubMed] [CrossRef]
15. Nathan CF,, Prendergast TJ,, Wiebe ME,, Stanley ER,, Platzer E,, Remold HG,, Welte K,, Rubin BY,, Murray HW . 1984. Activation of human macrophages. Comparison of other cytokines with interferon-γ. J Exp Med 160 : 600– 605.[PubMed] [CrossRef]
16. Meltzer MS,, Occhionero M,, Ruco LP . 1982. Macrophage activation for tumor cytotoxicity: regulatory mechanisms for induction and control of cytotoxic activity. Fed Proc 41 : 2198– 2205.[PubMed]
17. Bosisio D,, Polentarutti N,, Sironi M,, Bernasconi S,, Miyake K,, Webb GR,, Martin MU,, Mantovani A,, Muzio M . 2002. Stimulation of toll-like receptor 4 expression in human mononuclear phagocytes by interferon-γ: a molecular basis for priming and synergism with bacterial lipopolysaccharide. Blood 99 : 3427– 3431.[PubMed] [CrossRef]
18. Stein M,, Keshav S,, Harris N,, Gordon S . 1992. Interleukin 4 potently enhances murine macrophage mannose receptor activity: a marker of alternative immunologic macrophage activation. J Exp Med 176 : 287– 292.[PubMed] [CrossRef]
19. Sica A,, Mantovani A . 2012. Macrophage plasticity and polarization: in vivo veritas. J Clin Invest 122 : 787– 795.[PubMed] [CrossRef]
20. Martinez FO,, Gordon S,, Locati M,, Mantovani A . 2006. Transcriptional profiling of the human monocyte-to-macrophage differentiation and polarization: new molecules and patterns of gene expression. J Immunol 177 : 7303– 7311.[PubMed] [CrossRef]
21. Monticelli S,, Natoli G . 2013. Short-term memory of danger signals and environmental stimuli in immune cells. Nat Immunol 14 : 777– 784.[PubMed] [CrossRef]
22. Medzhitov R,, Schneider DS,, Soares MP . 2012. Disease tolerance as a defense strategy. Science 335 : 936– 941.[PubMed] [CrossRef]
23. Akey JM . 2009. Constructing genomic maps of positive selection in humans: where do we go from here? Genome Res 19 : 711– 722.[PubMed] [CrossRef]
24. Biswas SK,, Lopez-Collazo E . 2009. Endotoxin tolerance: new mechanisms, molecules and clinical significance. Trends Immunol 30 : 475– 487.[PubMed] [CrossRef]
25. Willment JA,, Lin HH,, Reid DM,, Taylor PR,, Williams DL,, Wong SY,, Gordon S,, Brown GD . 2003. Dectin-1 expression and function are enhanced on alternatively activated and GM-CSF-treated macrophages and are negatively regulated by IL-10, dexamethasone, and lipopolysaccharide. J Immunol 171 : 4569– 4573.[PubMed] [CrossRef]
26. Ricklin D,, Lambris JD . 2013. Complement in immune and inflammatory disorders: pathophysiological mechanisms. J Immunol 190 : 3831– 3838.[PubMed] [CrossRef]
27. Hajishengallis G,, Chavakis T . 2013. Endogenous modulators of inflammatory cell recruitment. Trends Immunol 34 : 1– 6.[PubMed] [CrossRef]
28. Bottazzi B,, Doni A,, Garlanda C,, Mantovani A . 2010. An integrated view of humoral innate immunity: pentraxins as a paradigm. Annu Rev Immunol 28 : 157– 183.[PubMed] [CrossRef]
29. Jeannin P,, Bottazzi B,, Sironi M,, Doni A,, Rusnati M,, Presta M,, Maina V,, Magistrelli G,, Haeuw JF,, Hoeffel G,, Thieblemont N,, Corvaia N,, Garlanda C,, Delneste Y,, Mantovani A . 2005. Complexity and complementarity of outer membrane protein A recognition by cellular and humoral innate immunity receptors. Immunity 22 : 551– 560.[PubMed] [CrossRef]
30. Deban L,, Russo RC,, Sironi M,, Moalli F,, Scanziani M,, Zambelli V,, Cuccovillo I,, Bastone A,, Gobbi M,, Valentino S,, Doni A,, Garlanda C,, Danese S,, Salvatori G,, Sassano M,, Evangelista V,, Rossi B,, Zenaro E,, Constantin G,, Laudanna C,, Bottazzi B,, Mantovani A . 2010. Regulation of leukocyte recruitment by the long pentraxin PTX3. Nat Immunol 11 : 328– 334.[PubMed] [CrossRef]
31. Naessens T,, Vander Beken S,, Bogaert P,, Van Rooijen N,, Lienenklaus S,, Weiss S,, De Koker S,, Grooten J . 2012. Innate imprinting of murine resident alveolar macrophages by allergic bronchial inflammation causes a switch from hypoinflammatory to hyperinflammatory reactivity. Am J Pathol 181 : 174– 184.[PubMed] [CrossRef]
32. Didierlaurent A,, Goulding J,, Patel S,, Snelgrove R,, Low L,, Bebien M,, Lawrence T,, van Rijt LS,, Lambrecht BN,, Sirard JC,, Hussell T . 2008. Sustained desensitization to bacterial Toll-like receptor ligands after resolution of respiratory influenza infection. J Exp Med 205 : 323– 329.[PubMed] [CrossRef]
33. Kleinnijenhuis J,, Quintin J,, Preijers F,, Joosten LA,, Ifrim DC,, Saeed S,, Jacobs C,, van Loenhout J,, de Jong D,, Stunnenberg HG,, Xavier RJ,, van der Meer JW,, van Crevel R,, Netea MG . 2012. Bacille Calmette-Guerin induces NOD2-dependent nonspecific protection from reinfection via epigenetic reprogramming of monocytes. Proc Natl Acad Sci U S A 109 : 17537– 17542.[PubMed] [CrossRef]
34. Boehm T,, McCurley N,, Sutoh Y,, Schorpp M,, Kasahara M,, Cooper MD . 2012. VLR-based adaptive immunity. Annu Rev Immunol 30 : 203– 220.[PubMed] [CrossRef]
35. Levy O . 2007. Innate immunity of the newborn: basic mechanisms and clinical correlates. Nat Rev Immunol 7 : 379– 390.[PubMed] [CrossRef]
36. Philbin VJ,, Dowling DJ,, Gallington LC,, Cortes G,, Tan Z,, Suter EE,, Chi KW,, Shuckett A,, Stoler-Barak L,, Tomai M,, Miller RL,, Mansfield K,, Levy O . 2012. Imidazoquinoline Toll-like receptor 8 agonists activate human newborn monocytes and dendritic cells through adenosine-refractory and caspase-1-dependent pathways. J Allergy Clin Immunol 130 : 195– 204.e9. doi:10.1016/j.jaci.2012.02.042. [CrossRef]
37. van den Burg HA,, Takken FL . 2009. Does chromatin remodeling mark systemic acquired resistance? Trends Plant Sci 14 : 286– 294.[PubMed] [CrossRef]
38. Conrath U . 2011. Molecular aspects of defence priming. Trends Plant Sci 16 : 524– 531.[PubMed] [CrossRef]
39. Slaughter A,, Daniel X,, Flors V,, Luna E,, Hohn B,, Mauch-Mani B . 2012. Descendants of primed Arabidopsis plants exhibit resistance to biotic stress. Plant Physiol 158 : 835– 843.[PubMed] [CrossRef]
40. Maitra U,, Deng H,, Glaros T,, Baker B,, Capelluto DG,, Li Z,, Li L . 2012. Molecular mechanisms responsible for the selective and low-grade induction of proinflammatory mediators in murine macrophages by lipopolysaccharide. J Immunol 189 : 1014– 1023.[PubMed] [CrossRef]
41. Ifrim DC,, Quintin J,, Joosten LA,, Jacobs C,, Jansen T,, Jacobs L,, Gow NA,, Williams DL,, van der Meer JW,, Netea MG . 2014. Trained immunity or tolerance: opposing functional programs induced in human monocytes after engagement of various pattern recognition receptors. Clin Vaccine Immunol 21 : 534– 545.[PubMed] [CrossRef]
42. Foster SL,, Hargreaves DC,, Medzhitov R . 2007. Gene-specific control of inflammation by TLR-induced chromatin modifications. Nature 447 : 972– 978.[CrossRef]
43. Liu TF,, Yoza BK,, El Gazzar M,, Vachharajani VT,, McCall CE . 2011. NAD +-dependent SIRT1 deacetylase participates in epigenetic reprogramming during endotoxin tolerance. J Biol Chem 286 : 9856– 9864.[PubMed] [CrossRef]
44. Liu TF,, Vachharajani VT,, Yoza BK,, McCall CE . 2012. NAD +-dependent sirtuin 1 and 6 proteins coordinate a switch from glucose to fatty acid oxidation during the acute inflammatory response. J Biol Chem 287 : 25758– 25769.[PubMed] [CrossRef]
45. Ostuni R,, Piccolo V,, Barozzi I,, Polletti S,, Termanini A,, Bonifacio S,, Curina A,, Prosperini E,, Ghisletti S,, Natoli G . 2013. Latent enhancers activated by stimulation in differentiated cells. Cell 152 : 157– 171.[PubMed] [CrossRef]
46. 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. doi:10.1126/science.1251086. [CrossRef]
47. Warburg O,, Wind F,, Negelein E . 1927. The metabolism of tumors in the body. J Gen Physiol 8 : 519– 530.[PubMed] [CrossRef]
48. Rodríguez-Prados JC,, Través PG,, Cuenca J,, Rico D,, Aragonés J,, Martín-Sanz P,, Cascante M,, Boscá L . 2010. Substrate fate in activated macrophages: a comparison between innate, classic, and alternative activation. J Immunol 185 : 605– 614.[PubMed] [CrossRef]
49. Cheng SC,, Quintin J,, Cramer RA,, Shepardson KM,, Saeed S,, Kumar V,, Giamarellos-Bourboulis EJ,, Martens JH,, Rao NA,, Aghajanirefah A,, Manjeri GR,, Li Y,, Ifrim DC,, Arts RJ,, van der Veer BM,, Deen PM,, Logie C,, O’Neill LA,, Willems P,, van de Veerdonk FL,, van der Meer JW,, Ng A,, Joosten LA,, Wijmenga C,, Stunnenberg HG,, Xavier RJ,, Netea MG . 2014. mTOR- and HIF-1α-mediated aerobic glycolysis as metabolic basis for trained immunity. Science 345 : 1250684. doi:10.1126/science.1250684. [CrossRef]
50. Barton ES,, White DW,, Cathelyn JS,, Brett-McClellan KA,, Engle M,, Diamond MS,, Miller VL,, Virgin HW IV . 2007. Herpesvirus latency confers symbiotic protection from bacterial infection. Nature 447 : 326– 329.[PubMed] [CrossRef]
51. van ‘t Wout JW,, Poell R,, van Furth R . 1992. The role of BCG/PPD-activated macrophages in resistance against systemic candidiasis in mice. Scand J Immunol 36 : 713– 719.[PubMed] [CrossRef]
52. Spencer JC,, Ganguly R,, Waldman RH . 1977. Nonspecific protection of mice against influenza virus infection by local or systemic immunization with Bacille Calmette-Guérin. J Infect Dis 136 : 171– 175.[PubMed] [CrossRef]
53. Aaby P,, Roth A,, Ravn H,, Napirna BM,, Rodrigues A,, Lisse IM,, Stensballe L,, Diness BR,, Lausch KR,, Lund N,, Biering-Sørensen S,, Whittle H,, Benn CS . 2011. Randomized trial of BCG vaccination at birth to low-birth-weight children: beneficial nonspecific effects in the neonatal period? J Infect Dis 204 : 245– 252.[PubMed] [CrossRef]
54. Roth AE,, Stensballe LG,, Garly ML,, Aaby P . 2006. Beneficial non-targeted effects of BCG—ethical implications for the coming introduction of new TB vaccines. Tuberculosis (Edinb) 86 : 397– 403.[PubMed] [CrossRef]
55. Lopez MJ,, Pardo-Seco JJ,, Martinon-Torres F . 2015. Nonspecific (heterologous) protection of neonatal BCG vaccination against hospitalization due to respiratory infection and sepsis. Clin Infect Dis 60 : 1611– 1619.[PubMed] [CrossRef]
56. Sørup S,, Benn CS,, Poulsen A,, Krause TG,, Aaby P,, Ravn H . 2014. Live vaccine against measles, mumps, and rubella and the risk of hospital admissions for nontargeted infections. JAMA 311 : 826– 835.[PubMed] [CrossRef]
57. Sørup S,, Benn CS,, Stensballe LG,, Aaby P,, Ravn H . 2015. Measles-mumps-rubella vaccination and respiratory syncytial virus-associated hospital contact. Vaccine 33 : 237– 245.[PubMed] [CrossRef]
58. Buffen K,, Oosting M,, Quintin J,, Ng A,, Kleinnijenhuis J,, Kumar V,, van de Vosse E,, Wijmenga C,, van Crevel R,, Oosterwijk E,, Grotenhuis AJ,, Vermeulen SH,, Kiemeney LA,, van de Veerdonk FL,, Chamilos G,, Xavier RJ,, van der Meer JW,, Netea MG,, Joosten LA . 2014. Autophagy controls BCG-induced trained immunity and the response to intravesical BCG therapy for bladder cancer. PLoS Pathog 10 : e1004485. doi:10.1371/journal.ppat.1004485. [CrossRef]

Tables

Adaptive Characteristics of Innate Immune Responses in Macrophages
[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555819194.chap38-1,webId=/content/author/10.1128/9781555819194.chap38-1,properties={foaf_givenname=Rob J. W., foaf_name=Rob J. W. Arts, foaf_surname=Arts, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555819194.chap38-aff1]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555819194.chap38-2,webId=/content/author/10.1128/9781555819194.chap38-2,properties={foaf_givenname=Mihai G., foaf_name=Mihai G. Netea, foaf_surname=Netea, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555819194.chap38-aff2]]}]]
Citation: Arts R, Netea M. 2017. Adaptive Characteristics of Innate Immune Responses in Macrophages, p 679-686. In Gordon S (ed), Myeloid Cells in Health and Disease. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MCHD-0023-2015
/content/10.1128/9781555819194.chap38.tab38-1
Table 1

Examples of memory of innate immunity in plants, invertebrates, and mammals

Generic image for table
Table 1

Examples of memory of innate immunity in plants, invertebrates, and mammals

Citation: Arts R, Netea M. 2017. Adaptive Characteristics of Innate Immune Responses in Macrophages, p 679-686. In Gordon S (ed), Myeloid Cells in Health and Disease. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MCHD-0023-2015

Back to top
This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error