Innate Memory Reprogramming by Gold Nanoparticles Depends on the Microbial Agents That Induce Memory
Innate immune memory, the ability of innate cells to react in a more protective way to secondary challenges, is induced by exposure to infectious and other exogeous and endogenous agents. Engineered nanoparticles are particulate exogenous agents that, as such, could trigger an inflammatory reaction...
| Main Authors: | , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2021-11-01
|
| Series: | Frontiers in Immunology |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fimmu.2021.751683/full |
| _version_ | 1830273052400680960 |
|---|---|
| author | Benjamin J. Swartzwelter Benjamin J. Swartzwelter Sara Michelini Tobias Frauenlob Francesco Barbero Alessandro Verde Anna Chiara De Luca Victor Puntes Victor Puntes Victor Puntes Albert Duschl Jutta Horejs-Hoeck Paola Italiani Diana Boraschi Diana Boraschi Diana Boraschi |
| author_facet | Benjamin J. Swartzwelter Benjamin J. Swartzwelter Sara Michelini Tobias Frauenlob Francesco Barbero Alessandro Verde Anna Chiara De Luca Victor Puntes Victor Puntes Victor Puntes Albert Duschl Jutta Horejs-Hoeck Paola Italiani Diana Boraschi Diana Boraschi Diana Boraschi |
| author_sort | Benjamin J. Swartzwelter |
| collection | DOAJ |
| description | Innate immune memory, the ability of innate cells to react in a more protective way to secondary challenges, is induced by exposure to infectious and other exogeous and endogenous agents. Engineered nanoparticles are particulate exogenous agents that, as such, could trigger an inflammatory reaction in monocytes and macrophages and could therefore be also able to induce innate memory. Here, we have evaluated the capacity of engineered gold nanoparticles (AuNPs) to induce a memory response or to modulate the memory responses induced by microbial agents. Microbial agents used were in soluble vs. particulate form (MDP and the gram-positive bacteria Staphylococcus aureus; β-glucan and the β-glucan-producing fungi C. albicans), and as whole microrganisms that were either killed (S. aureus, C. albicans) or viable (the gram-negative bacteria Helicobacter pylori). The memory response was assessed in vitro, by exposing human primary monocytes from 2-7 individual donors to microbial agents with or without AuNPs (primary response), then resting them for 6 days to allow return to baseline, and eventually challenging them with LPS (secondary memory response). Primary and memory responses were tested as production of the innate/inflammatory cytokine TNFα and other inflammatory and anti-inflammatory factors. While inactive on the response induced by soluble microbial stimuli (muramyl dipeptide -MDP-, β-glucan), AuNPs partially reduced the primary response induced by whole microorganisms. AuNPs were also unable to directly induce a memory response but could modulate stimulus-induced memory in a circumscribed fashion, limited to some agents and some cytokines. Thus, the MDP-induced tolerance in terms of TNFα production was further exacerbated by co-priming with AuNPs, resulting in a less inflammatory memory response. Conversely, the H. pylori-induced tolerance was downregulated by AuNPs only relative to the anti-inflammatory cytokine IL-10, which would lead to an overall more inflammatory memory response. These effects of AuNPs may depend on a differential interaction/association between the reactive particle surfaces and the microbial components and agents, which may lead to a change in the exposure profiles. As a general observation, however, the donor-to-donor variability in memory response profiles and reactivity to AuNPs was substantial, suggesting that innate memory depends on the individual history of exposures. |
| first_indexed | 2024-12-18T23:38:11Z |
| format | Article |
| id | doaj.art-fccd5c0e1c344ac3b1ba44cd8b3015ad |
| institution | Directory Open Access Journal |
| issn | 1664-3224 |
| language | English |
| last_indexed | 2024-12-18T23:38:11Z |
| publishDate | 2021-11-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Immunology |
| spelling | doaj.art-fccd5c0e1c344ac3b1ba44cd8b3015ad2022-12-21T20:47:29ZengFrontiers Media S.A.Frontiers in Immunology1664-32242021-11-011210.3389/fimmu.2021.751683751683Innate Memory Reprogramming by Gold Nanoparticles Depends on the Microbial Agents That Induce MemoryBenjamin J. Swartzwelter0Benjamin J. Swartzwelter1Sara Michelini2Tobias Frauenlob3Francesco Barbero4Alessandro Verde5Anna Chiara De Luca6Victor Puntes7Victor Puntes8Victor Puntes9Albert Duschl10Jutta Horejs-Hoeck11Paola Italiani12Diana Boraschi13Diana Boraschi14Diana Boraschi15 Institute of Biochemistry and Cell Biology (IBBC), National Research Council (CNR), Napoli, ItalyDepartment Biosciences, Paris Lodron University of Salzburg (PLUS), Salzburg, AustriaDepartment Biosciences, Paris Lodron University of Salzburg (PLUS), Salzburg, AustriaDepartment Biosciences, Paris Lodron University of Salzburg (PLUS), Salzburg, AustriaInstitut Català de Nanociència i Nanotecnologia (ICN2), Consejo Superior de Investigaciones Científicas (CSIC) and The Barcelona Institute of Science and Technology (BIST), Barcelona, Spain Institute of Biochemistry and Cell Biology (IBBC), National Research Council (CNR), Napoli, Italy Institute of Biochemistry and Cell Biology (IBBC), National Research Council (CNR), Napoli, ItalyInstitut Català de Nanociència i Nanotecnologia (ICN2), Consejo Superior de Investigaciones Científicas (CSIC) and The Barcelona Institute of Science and Technology (BIST), Barcelona, SpainVall d’Hebron Research Institute (VHIR), Barcelona, SpainInstitució Catalana de Recerca I Estudis Avançats (ICREA), Barcelona, SpainDepartment Biosciences, Paris Lodron University of Salzburg (PLUS), Salzburg, AustriaDepartment Biosciences, Paris Lodron University of Salzburg (PLUS), Salzburg, Austria Institute of Biochemistry and Cell Biology (IBBC), National Research Council (CNR), Napoli, Italy Institute of Biochemistry and Cell Biology (IBBC), National Research Council (CNR), Napoli, ItalyStazione Zoologica Anton Dohrn, Napoli, ItalyShenzhen Institute of Advanced Technology (SIAT), Chinese Academy of Sciences (CAS), Shenzhen, ChinaInnate immune memory, the ability of innate cells to react in a more protective way to secondary challenges, is induced by exposure to infectious and other exogeous and endogenous agents. Engineered nanoparticles are particulate exogenous agents that, as such, could trigger an inflammatory reaction in monocytes and macrophages and could therefore be also able to induce innate memory. Here, we have evaluated the capacity of engineered gold nanoparticles (AuNPs) to induce a memory response or to modulate the memory responses induced by microbial agents. Microbial agents used were in soluble vs. particulate form (MDP and the gram-positive bacteria Staphylococcus aureus; β-glucan and the β-glucan-producing fungi C. albicans), and as whole microrganisms that were either killed (S. aureus, C. albicans) or viable (the gram-negative bacteria Helicobacter pylori). The memory response was assessed in vitro, by exposing human primary monocytes from 2-7 individual donors to microbial agents with or without AuNPs (primary response), then resting them for 6 days to allow return to baseline, and eventually challenging them with LPS (secondary memory response). Primary and memory responses were tested as production of the innate/inflammatory cytokine TNFα and other inflammatory and anti-inflammatory factors. While inactive on the response induced by soluble microbial stimuli (muramyl dipeptide -MDP-, β-glucan), AuNPs partially reduced the primary response induced by whole microorganisms. AuNPs were also unable to directly induce a memory response but could modulate stimulus-induced memory in a circumscribed fashion, limited to some agents and some cytokines. Thus, the MDP-induced tolerance in terms of TNFα production was further exacerbated by co-priming with AuNPs, resulting in a less inflammatory memory response. Conversely, the H. pylori-induced tolerance was downregulated by AuNPs only relative to the anti-inflammatory cytokine IL-10, which would lead to an overall more inflammatory memory response. These effects of AuNPs may depend on a differential interaction/association between the reactive particle surfaces and the microbial components and agents, which may lead to a change in the exposure profiles. As a general observation, however, the donor-to-donor variability in memory response profiles and reactivity to AuNPs was substantial, suggesting that innate memory depends on the individual history of exposures.https://www.frontiersin.org/articles/10.3389/fimmu.2021.751683/fullinnate immunityinnate memorynanoparticlesmicrobial agentsmonocytes |
| spellingShingle | Benjamin J. Swartzwelter Benjamin J. Swartzwelter Sara Michelini Tobias Frauenlob Francesco Barbero Alessandro Verde Anna Chiara De Luca Victor Puntes Victor Puntes Victor Puntes Albert Duschl Jutta Horejs-Hoeck Paola Italiani Diana Boraschi Diana Boraschi Diana Boraschi Innate Memory Reprogramming by Gold Nanoparticles Depends on the Microbial Agents That Induce Memory Frontiers in Immunology innate immunity innate memory nanoparticles microbial agents monocytes |
| title | Innate Memory Reprogramming by Gold Nanoparticles Depends on the Microbial Agents That Induce Memory |
| title_full | Innate Memory Reprogramming by Gold Nanoparticles Depends on the Microbial Agents That Induce Memory |
| title_fullStr | Innate Memory Reprogramming by Gold Nanoparticles Depends on the Microbial Agents That Induce Memory |
| title_full_unstemmed | Innate Memory Reprogramming by Gold Nanoparticles Depends on the Microbial Agents That Induce Memory |
| title_short | Innate Memory Reprogramming by Gold Nanoparticles Depends on the Microbial Agents That Induce Memory |
| title_sort | innate memory reprogramming by gold nanoparticles depends on the microbial agents that induce memory |
| topic | innate immunity innate memory nanoparticles microbial agents monocytes |
| url | https://www.frontiersin.org/articles/10.3389/fimmu.2021.751683/full |
| work_keys_str_mv | AT benjaminjswartzwelter innatememoryreprogrammingbygoldnanoparticlesdependsonthemicrobialagentsthatinducememory AT benjaminjswartzwelter innatememoryreprogrammingbygoldnanoparticlesdependsonthemicrobialagentsthatinducememory AT saramichelini innatememoryreprogrammingbygoldnanoparticlesdependsonthemicrobialagentsthatinducememory AT tobiasfrauenlob innatememoryreprogrammingbygoldnanoparticlesdependsonthemicrobialagentsthatinducememory AT francescobarbero innatememoryreprogrammingbygoldnanoparticlesdependsonthemicrobialagentsthatinducememory AT alessandroverde innatememoryreprogrammingbygoldnanoparticlesdependsonthemicrobialagentsthatinducememory AT annachiaradeluca innatememoryreprogrammingbygoldnanoparticlesdependsonthemicrobialagentsthatinducememory AT victorpuntes innatememoryreprogrammingbygoldnanoparticlesdependsonthemicrobialagentsthatinducememory AT victorpuntes innatememoryreprogrammingbygoldnanoparticlesdependsonthemicrobialagentsthatinducememory AT victorpuntes innatememoryreprogrammingbygoldnanoparticlesdependsonthemicrobialagentsthatinducememory AT albertduschl innatememoryreprogrammingbygoldnanoparticlesdependsonthemicrobialagentsthatinducememory AT juttahorejshoeck innatememoryreprogrammingbygoldnanoparticlesdependsonthemicrobialagentsthatinducememory AT paolaitaliani innatememoryreprogrammingbygoldnanoparticlesdependsonthemicrobialagentsthatinducememory AT dianaboraschi innatememoryreprogrammingbygoldnanoparticlesdependsonthemicrobialagentsthatinducememory AT dianaboraschi innatememoryreprogrammingbygoldnanoparticlesdependsonthemicrobialagentsthatinducememory AT dianaboraschi innatememoryreprogrammingbygoldnanoparticlesdependsonthemicrobialagentsthatinducememory |