bims-bac4me Biomed News
on Microbiome and trained immunity
Issue of 2023‒02‒12
38 papers selected by
Chun-Chi Chang
University Hospital Zurich


  1. Int J Mol Sci. 2023 Jan 24. pii: 2311. [Epub ahead of print]24(3):
      Trained immunity is the process of long-term functional reprogramming (a de facto innate immune memory) of innate immune cells such as monocytes and macrophages after an exposure to pathogens, vaccines, or their ligands. The induction of trained immunity is mediated through epigenetic and metabolic mechanisms. Apart from exogenous stimuli, trained immunity can be induced by endogenous compounds such as oxidized LDL, urate, fumarate, but also cytokines including IL-1α and IL-1β. Here, we show that also recombinant IL-36γ, a pro-inflammatory cytokine of the IL-1-family, is able to induce trained immunity in primary human monocytes, demonstrated by higher cytokine responses and an increase in cellular metabolic pathways both regulated by epigenetic histone modifications. These effects could be inhibited by the IL-36 receptor antagonist as well as by IL-38, an anti-inflammatory cytokine of the IL-1 family which shares its main receptor with IL-36 (IL-1R6). Further, we demonstrated that trained immunity induced by IL-36γ is mediated by NF-κB and mTOR signaling. The inhibitory effect of IL-38 on IL-36γ-induced trained immunity was confirmed in experiments using bone marrow of IL-38KO and WT mice. These results indicate that exposure to IL-36γ results in long-term pro-inflammatory changes in monocytes which can be inhibited by IL-38. Recombinant IL-38 could therefore potentially be used as a therapeutic intervention for diseases characterized by exacerbated trained immunity.
    Keywords:  IL-36; IL-38; epigenetics; immunometabolism; innate immune memory
    DOI:  https://doi.org/10.3390/ijms24032311
  2. Front Immunol. 2023 ;14 1125635
      Atopic dermatitis (AD) is a common chronic inflammatory skin disease that significantly affects the patient's quality of life. A disrupted skin barrier, type 2 cytokine-dominated inflammation, and microbial dysbiosis with increased Staphylococcus aureus colonization are critical components of AD pathogenesis. Patients with AD exhibit decreased expression of antimicrobial peptides (AMPs) which is linked to increased colonization by Staphylococcus aureus. The skin microbiome itself is a source of several AMPs. These host- and microbiome-derived AMPs define the microbial landscape of the skin based on their differential antimicrobial activity against a range of skin microbes or their quorum sensing inhibitory properties. These are particularly important in preventing and limiting dysbiotic colonization with Staphylococcus aureus. In addition, AMPs are critical for immune homeostasis. In this article, we share our perspectives about the implications of microbial derived AMPs in AD patients and their potential effects on overlapping factors involved in AD. We argue and discuss the potential of bacterial AMPs as therapeutics in AD.
    Keywords:  Staphylococcus aureus; antimicrobial peptides; atopic dermatitis; autoinducing peptides; bacteriocins; skin microbiome
    DOI:  https://doi.org/10.3389/fimmu.2023.1125635
  3. Exp Hematol. 2023 Feb 08. pii: S0301-472X(23)00028-0. [Epub ahead of print]
      Immunological memory is a feature typically ascribed to the adaptive arm of the immune system. However, recent studies have demonstrated that hematopoietic stem cells (HSCs) and innate immune cells such as monocytes and macrophages are also capable of gaining epigenetic signatures to enhance their response in the context of reinfection. This suggests the presence of long-term memory, a phenomenon referred to as trained immunity. Trained immunity in HSCs can occur via changes in the epigenetic landscape and enhanced chromatin accessibility in lineage-specific genes, as well as through metabolic alterations. These changes can lead to a skewing in lineage bias, particularly enhanced myelopoiesis and the generation of epigenetically modified innate immune cells that provide better protection against pathogens upon secondary infection. Here, we summarize recent advances in trained immunity and epigenetic memory formation in HSCs and self-renewing alveolar macrophages (AMs), which was the focus of the Spring 2022 International Society for Experimental Hematology (ISEH) webinar.
    DOI:  https://doi.org/10.1016/j.exphem.2023.02.001
  4. Int J Mol Sci. 2023 Jan 25. pii: 2366. [Epub ahead of print]24(3):
      Airborne fungi are ubiquitous in the environment and are commonly associated with airway inflammatory diseases. The innate immune defense system eliminates most inhaled fungi. However, some influence the development of chronic rhinosinusitis. Fungal CRS is thought of as not a common disease, and its incidence increases over time. Fungi are present in CRS patients and in healthy sinonasal mucosa. Although the immunological mechanisms have not been entirely explained, CRS patients may exhibit different immune responses than healthy people against airborne fungi. Fungi can induce Th1 and Th2 immune responses. In CRS, Th2-related immune responses against fungi are associated with pattern recognition receptors in nasal epithelial cells, the production of inflammatory cytokines and chemokines from nasal epithelial cells, and interaction with innate type 2 cells, lymphocytes, and inflammatory cells. Fungi also interact with neutrophils and eosinophils and induce neutrophil extracellular traps (NETs) and eosinophil extracellular traps (EETs). NETs and EETs are associated with antifungal properties and aggravation of chronic inflammation in CRS by releasing intracellular granule proteins. Fungal and bacterial biofilms are commonly found in CRS and may support chronic and recalcitrant CRS infection. The fungal-bacterial interaction in the sinonasal mucosa could affect the survival and virulence of fungi and bacteria and host immune responses. The interaction between the mycobiome and microbiome may also influence the host immune response, impacting local inflammation and chronicity. Although the exact immunopathologic role of fungi in the pathogenesis of CRS is not completely understood, they contribute to the development of sinonasal inflammatory responses in CRS.
    Keywords:  biofilm; chronic rhinosinusitis; extracellular trap; fungus; mucosal immunity
    DOI:  https://doi.org/10.3390/ijms24032366
  5. Cell Host Microbe. 2023 Feb 08. pii: S1931-3128(23)00033-1. [Epub ahead of print]31(2): 168-170
      The cellular and molecular sources of elevated IL-1β and IL-6 in COVID-19 remain unclear. In this issue of Cell Host and Microbe, Barnett et al. determine how immune cells sense SARS-CoV-2 infection in neighboring epithelial cells to trigger inflammasome signaling and IL-1β release, which in turn promotes IL-6 release.
    DOI:  https://doi.org/10.1016/j.chom.2023.01.008
  6. Front Immunol. 2022 ;13 1085551
      Chronic Obstructive Pulmonary Disease (COPD) has significantly contributed to global mortality, with three million deaths reported annually. This impact is expected to increase over the next 40 years, with approximately 5 million people predicted to succumb to COPD-related deaths annually. Immune mechanisms driving disease progression have not been fully elucidated. Airway microbiota have been implicated. However, it is still unclear how changes in the airway microbiome drive persistent immune activation and consequent lung damage. Mechanisms mediating microbiome-immune crosstalk in the airways remain unclear. In this review, we examine how dysbiosis mediates airway inflammation in COPD. We give a detailed account of how airway commensal bacteria interact with the mucosal innate and adaptive immune system to regulate immune responses in healthy or diseased airways. Immune-phenotyping airway microbiota could advance COPD immunotherapeutics and identify key open questions that future research must address to further such translation.
    Keywords:  COPD; adaptive immunity; inflammation; innate immunity; lung microbiome; mucosal immunity
    DOI:  https://doi.org/10.3389/fimmu.2022.1085551
  7. Cell Host Microbe. 2023 Feb 08. pii: S1931-3128(23)00034-3. [Epub ahead of print]31(2): 173-186
      Metabolites produced by commensal gut microbes impact host health through their recognition by the immune system and their influence on numerous metabolic pathways. Notably, the gut microbiota can both transform and synthesize lipids as well as break down dietary lipids to generate secondary metabolites with host modulatory properties. Although lipids have largely been consigned to structural roles, particularly in cell membranes, recent research has led to an increased appreciation of their signaling activities, with potential impacts on host health and physiology. This review focuses on studies that highlight the functions of bioactive lipids in mammalian physiology, with a special emphasis on immunity and metabolism.
    Keywords:  PUFAs; autoimmune disease; bacteria; cholesterol; diet; inflammation; innate immunity; lipids; metabolism; microbiome; phospholipids; sphingolipids
    DOI:  https://doi.org/10.1016/j.chom.2023.01.009
  8. Front Immunol. 2022 ;13 944772
      High mobility group box 1 (HMGB1), a ubiquitous chromatin-binding protein required for gene transcription regulation, is released into the extracellular microenvironment by various structural and immune cells, where it is known to act as an alarmin. Here, we investigated the role of airway epithelium-specific HMGB1 in the pathogenesis of muco-obstructive lung disease in Scnn1b-transgenic (Tg+) mouse, a model of human cystic fibrosis (CF)-like lung disease. We hypothesized that airway epithelium-derived HMGB1 modulates muco-inflammatory lung responses in the Tg+ mice. The airway epithelium-specific HMGB1-deficient mice were generated and the effects of HMGB1 deletion on immune cell recruitment, airway epithelial cell composition, mucous cell metaplasia, and bacterial clearance were determined. The airway epithelium-specific deletion of HMGB1 in wild-type (WT) mice did not result in any morphological alterations in the airway epithelium. The deficiency of HMGB1 in airway epithelial cells in the Tg+ mice, however, resulted in significantly increased infiltration of macrophages, neutrophils, and eosinophils which was associated with significantly higher levels of inflammatory mediators, including G-CSF, KC, MIP-2, MCP-1, MIP-1α, MIP-1β, IP-10, and TNF-α in the airspaces. Furthermore, as compared to the HMGB1-sufficient Tg+ mice, the airway epithelial cell-specific HMGB1-deficient Tg+ mice exhibited poor resolution of spontaneous bacterial infection. The HMGB1 deficiency in the airway epithelial cells of Tg+ mice did not alter airway epithelial cell-specific responses including epithelial cell proliferation, mucous cell metaplasia, and mucus obstruction. Collectively, our findings provide novel insights into the role of airway epithelial cell-derived HMGB1 in the pathogenesis of CF-like lung disease in Tg+ mice.
    Keywords:  HMGB1; Scnn1b-Tg+; airway epithelium; cystic fibrosis; mucus obstruction
    DOI:  https://doi.org/10.3389/fimmu.2022.944772
  9. Front Med (Lausanne). 2022 ;9 1085339
      Autoimmune disorders have been well characterized over the years and many pathways-but not all of them-have been found to explain their pathophysiology. Autoinflammatory disorders, on the other hand, are still hiding most of their molecular and cellular mechanisms. During the past few years, a newcomer has challenged the idea that only adaptive immunity could display memory response. Trained immunity is defined by innate immune responses that are faster and stronger to a second stimulus than to the first one, being the same or not. In response to the trained immunity inducer, and through metabolic and epigenetic changes of hematopoietic stem and progenitor cells in the bone marrow that are transmitted to their cellular progeny (peripheral trained immunity), or directly of tissue-resident cells (local innate immunity), innate cells responsiveness and functions upon stimulation are improved in the long-term. Innate immunity can be beneficial, but it could also be detrimental when maladaptive. Here, we discuss how trained immunity could contribute to the physiopathology of autoimmune and autoinflammatory diseases.
    Keywords:  autoimmune disease; autoinflammatory diseases; innate immunity; pathophysiology; trained immunity
    DOI:  https://doi.org/10.3389/fmed.2022.1085339
  10. Front Immunol. 2023 ;14 1075834
      The inflammasomes are intracellular multimeric protein complexes consisting of an innate immune sensor, the adapter protein ASC and the inflammatory caspases-1 and/or -11 and are important for the host defense against pathogens. Activaton of the receptor leads to formation of the inflammasomes and subsequent processing and activation of caspase-1 that cleaves the proinflammatory cytokines IL-1β and IL-18. Active caspase-1, and in some instances caspase-11, cleaves gasdermin D that translocates to the cell membrane where it forms pores resulting in the cell death program called pyroptosis. Inflammasomes can detect a range of microbial ligands through direct interaction or indirectly through diverse cellular processes including changes in ion fluxes, production of reactive oxygen species and disruption of various host cell functions. In this review, we will focus on the NLRP3, NLRP6, NLRC4 and AIM2 inflammasomes and how they are activated and regulated during infections with Gram-positive bacteria, including Staphylococcus spp., Streptococcus spp. and Listeria monocytogenes.
    Keywords:  Gram-positive bacteria; autophagy; inflammasome; mechanisms of activation; regulation
    DOI:  https://doi.org/10.3389/fimmu.2023.1075834
  11. Int J Mol Sci. 2023 Jan 21. pii: 2143. [Epub ahead of print]24(3):
      Diabetes mellitus is a chronic disease characterized by metabolic dysregulation which is frequently associated with diabetic foot ulcers that result from a severely compromised innate immune system. The high levels of blood glucose characteristic of diabetes cause an increase in circulating inflammatory mediators, which accelerate cellular senescence and dampen antimicrobial activity within dermal tissue. In diabetic wounds, bacteria and fungi proliferate in a protective biofilm forming a structure that a compromised host defense system cannot easily penetrate, often resulting in chronic infections that require antimicrobial intervention to promote the healing process. The designed host defense peptide (dHDP) RP557 is a synthesized peptide whose sequence has been derived from naturally occurring antimicrobial peptides (AMPs) that provide the first line of defense against invading pathogens. AMPs possess an amphipathic α-helix or β-sheet structure and a net positive charge that enables them to incorporate into pathogen membranes and perturb the barrier function of Gram-positive and Gram-negative bacteria along with fungi. The capacity of skin to resist infections is largely dependent upon the activity of endogenous AMPs that provided the basis for the design and testing of RP557 for the resolution of wound infections. In the current study, the topical application of RP557 stopped bacterial growth in the biofilm of methicillin-resistant Staphylococcus aureus (MRSA) USA300 infected wounds on the flanks of clinically relevant diabetic TALLYHO mice. Topical application of RP557 reduced bacterial load and accelerated wound closure, while wound size in control diabetic mice continued to expand. These studies demonstrate that RP557 reduces or eliminates an infection in its biofilm and restores wound-healing capacity.
    Keywords:  MRSA; TALLYHO; antimicrobial peptides (AMPs); designed Host Defense Peptide (dHDP); diabetes; foot ulcers; neutrophils; wound healing
    DOI:  https://doi.org/10.3390/ijms24032143
  12. Front Immunol. 2023 ;14 1114917
      Sepsis is frequently associated with hemostasis activation and thrombus formation, and systematic hemostatic changes are associated with a higher risk of mortality. The key events underlying hemostasis activation during sepsis are the strong activation of innate immune pathways and the excessive inflammatory response triggered by invading pathogens. Pyroptosis is a proinflammatory form of programmed cell death, that defends against pathogens during sepsis. However, excessive pyroptosis can lead to a dysregulation of host immune responses and organ dysfunction. Recently, pyroptosis has been demonstrated to play a prominent role in hemostasis activation in sepsis. Several studies have demonstrated that pyroptosis participates in the release and coagulation activity of tissue factors. In addition, pyroptosis activates leukocytes, endothelial cells, platelets, which cooperate with the coagulation cascade, leading to hemostasis activation in sepsis. This review article attempts to interpret the molecular and cellular mechanisms of the hemostatic imbalance induced by pyroptosis during sepsis and discusses potential therapeutic strategies.
    Keywords:  coagulation; hemostasis; inflammasome; pyroptosis; sepsis; tissue factor
    DOI:  https://doi.org/10.3389/fimmu.2023.1114917
  13. Immunol Lett. 2023 Feb 03. pii: S0165-2478(23)00020-2. [Epub ahead of print]
      The phagocytosis and clearance of dying cells by macrophages, a process termed efferocytosis, is essential for both maintaining homeostasis and promoting tissue repair after infection or sterile injury. If not removed in a timely manner, uncleared cells can undergo secondary necrosis, and necrotic cells lose membrane integrity, release toxic intracellular components, and potentially induce inflammation or autoimmune diseases. Efferocytosis also initiates the repair process by producing a wide range of pro-reparative factors. Accumulating evidence has revealed that macrophage efferocytosis defects are involved in the development and progression of a variety of inflammatory and autoimmune diseases. The underlying mechanisms of efferocytosis impairment are complex, disease-dependent, and incompletely understood. In this review, we will first summarize the current knowledge about the normal signaling and metabolic processes of macrophage efferocytosis and its importance in maintaining tissue homeostasis and repair. We then will focus on analyzing the molecular and cellular mechanisms underlying efferocytotic abnormality (impairment) in disease or injury conditions. Next, we will discuss the potential molecular targets for enhanced efferocytosis in animal models of disease. To provide a balanced view, we will also discuss some deleterious effects of efferocytosis.
    Keywords:  Apoptosis; efferocytosis; inflammation resolution; macrophage; neutrophil; phagocytosis
    DOI:  https://doi.org/10.1016/j.imlet.2023.02.001
  14. Int J Mol Sci. 2023 Jan 19. pii: 2009. [Epub ahead of print]24(3):
      Platelets play a major role in the processes of primary hemostasis and pathological inflammation-induced thrombosis. In the mid-2000s, several studies expanded the role of these particular cells, placing them in the "immune continuum" and thus changing the understanding of their function in both innate and adaptive immune responses. Among the many receptors they express on their surface, platelets express Toll-Like Receptors (TLRs), key receptors in the inflammatory cell-cell reaction and in the interaction between innate and adaptive immunity. In response to an infectious stimulus, platelets will become differentially activated. Platelet activation is variable depending on whether platelets are activated by a hemostatic or pathogen stimulus. This review highlights the role that platelets play in platelet modulation count and adaptative immune response during viral infection.
    Keywords:  TLRs; immune response; inflammatory function; platelets; thrombosis; viral infection
    DOI:  https://doi.org/10.3390/ijms24032009
  15. Am J Physiol Lung Cell Mol Physiol. 2023 Feb 07.
      Acute respiratory distress syndrome (ARDS) remains a significant cause of morbidity and mortality in critically ill patients. Oxidative stress and inflammation play crucial role in pathogenesis of ARDS. Extracellular superoxide dismutase (EC-SOD) is abundant in the lung and is important enzymatic defense against superoxide. Human single nucleotide polymorphism in matrix binding region of EC-SOD leads to substitution of arginine to glycine at position 213 (R213G) and results in release of EC-SOD into alveolar fluid, without affecting enzyme activity. We hypothesized that R213G EC-SOD variant protects against lung injury and inflammation via blockade of neutrophil-recruitment in infectious model of methicillin-resistant S. aureus (MRSA) pneumonia. After inoculation with MRSA, WT mice had impaired integrity of alveolar-capillary barrier and increased levels of IL-1β, IL-6, and TNF-α in the broncho-alveolar lavage fluid (BALF), while infected mice expressing R213G EC-SOD variant maintained the integrity of alveolar-capillary interface and had attenuated levels of proinflammatory cytokines. MRSA-infected mice expressing R213G EC-SOD variant also had attenuated neutrophil numbers in BALF and decreased expression of neutrophil chemoattractant CXCL1 by the alveolar epithelial ATII cells, compared to the infected WT group. The decreased neutrophil numbers in R213G mice were not due to increased rate of apoptosis. Mice expressing R213G variant had differential effect on neutrophil functionality, - the generation of neutrophil extracellular traps (NETs) but not myeloperoxidase (MPO) levels were attenuated in comparison to WT controls. Despite having the same bacterial load in the lung as WT controls, mice expressing R213G EC-SOD variant were protected from extrapulmonary dissemination of bacteria.
    Keywords:  Extracellular Superoxide dismutase; MRSA; acute lung injury; neutrophils
    DOI:  https://doi.org/10.1152/ajplung.00217.2022
  16. Microb Genom. 2022 Dec;8(12):
      Staphylococcus aureus is a leading cause of skin and soft tissue infections and systemic infections. Wall teichoic acids (WTAs) are cell wall-anchored glycopolymers that are important for S. aureus nasal colonization, phage-mediated horizontal gene transfer, and antibiotic resistance. WTAs consist of a polymerized ribitol phosphate (RboP) chain that can be glycosylated with N-acetylglucosamine (GlcNAc) by three glycosyltransferases: TarS, TarM, and TarP. TarS and TarP modify WTA with β-linked GlcNAc at the C-4 (β1,4-GlcNAc) and the C-3 position (β1,3-GlcNAc) of the RboP subunit, respectively, whereas TarM modifies WTA with α-linked GlcNAc at the C-4 position (α1,4-GlcNAc). Importantly, these WTA glycosylation patterns impact immune recognition and clearance of S. aureus. Previous studies suggest that tarS is near-universally present within the S. aureus population, whereas a smaller proportion co-contain either tarM or tarP. To gain more insight into the presence and genetic variation of tarS, tarM and tarP in the S. aureus population, we analysed a collection of 25 652 S. aureus genomes within the PubMLST database. Over 99 % of isolates contained tarS. Co-presence of tarS/tarM or tarS/tarP occurred in 37 and 7 % of isolates, respectively, and was associated with specific S. aureus clonal complexes. We also identified 26 isolates (0.1 %) that contained all three glycosyltransferase genes. At sequence level, we identified tar alleles with amino acid substitutions in critical enzymatic residues or with premature stop codons. Several tar variants were expressed in a S. aureus tar-negative strain. Analysis using specific monoclonal antibodies and human langerin showed that WTA glycosylation was severely attenuated or absent. Overall, our data provide a broad overview of the genetic diversity of the three WTA glycosyltransferases in the S. aureus population and the functional consequences for immune recognition.
    Keywords:  PubMLST; Staphylococcus aureus; glycosylation; tar glycosyltransferases; wall teichoic acid
    DOI:  https://doi.org/10.1099/mgen.0.000902
  17. PLoS Biol. 2023 Feb 10. 21(2): e3002022
      The past 20 years of research has elucidated new innate immune sensing and cell death pathways with disease relevance. Future molecular characterization of these pathways and their crosstalk and functional redundancies will aid in development of therapeutic strategies.
    DOI:  https://doi.org/10.1371/journal.pbio.3002022
  18. Ann Transl Med. 2023 Jan 15. 11(1): 1
      
    Keywords:  Microbiome; asthma; bacteria; infection; virus
    DOI:  https://doi.org/10.21037/atm-22-6009
  19. J Vis Exp. 2023 Jan 20.
      Innate immunity provides the critical first line of defense in response to pathogens and sterile insults. A key mechanistic component of this response is the initiation of innate immune programmed cell death (PCD) to eliminate infected or damaged cells and propagate immune responses. However, excess PCD is associated with inflammation and pathology. Therefore, understanding the activation and regulation of PCD is a central aspect of characterizing innate immune responses and identifying new therapeutic targets across the disease spectrum. This protocol provides methods for characterizing innate immune PCD activation by monitoring caspases, a family of cysteine-dependent proteases that are often associated with diverse PCD pathways, including apoptosis, pyroptosis, necroptosis, and PANoptosis. Initial reports characterized caspase-2, caspase-8, caspase-9, and caspase-10 as initiator caspases and caspase-3, caspase-6, and caspase-7 as effector caspases in apoptosis, while later studies found the inflammatory caspases, caspase-1, caspase-4, caspase-5, and caspase-11, drive pyroptosis. It is now known that there is extensive crosstalk between the caspases and other innate immune and cell death molecules across the previously defined PCD pathways, identifying a key knowledge gap in the mechanistic understanding of innate immunity and PCD and leading to the characterization of PANoptosis. PANoptosis is a unique innate immune inflammatory PCD pathway regulated by PANoptosome complexes, which integrate components, including caspases, from other cell death pathways. Here, methods for assessing the activation of caspases in response to various stimuli are provided. These methods allow for the characterization of PCD pathways both in vitro and in vivo, as activated caspases undergo proteolytic cleavage that can be visualized by western blotting using optimal antibodies and blotting conditions. A protocol and western blotting workflow have been established that allow for the assessment of the activation of multiple caspases from the same cellular population, providing a comprehensive characterization of the PCD processes. This method can be applied across research areas in development, homeostasis, infection, inflammation, and cancer to evaluate PCD pathways throughout cellular processes in health and disease.
    DOI:  https://doi.org/10.3791/64308
  20. Front Immunol. 2023 ;14 1072142
      Infections with influenza A viruses (IAV) cause seasonal epidemics and global pandemics. The majority of these infections remain asymptomatic, especially among children below five years of age. Importantly, this is a time, when immunological imprinting takes place. Whether early-life infections with IAV affect the development of antimicrobial immunity is unknown. Using a preclinical mouse model, we demonstrate here that silent neonatal influenza infections have a remote beneficial impact on the later control of systemic juvenile-onset and adult-onset infections with an unrelated pathogen, Staphylococcus aureus, due to improved pathogen clearance and clinical resolution. Strategic vaccination with a live attenuated IAV vaccine elicited a similar protection phenotype. Mechanistically, the IAV priming effect primarily targets antimicrobial functions of the developing innate immune system including increased antimicrobial plasma activity and enhanced phagocyte functions and antigen-presenting properties at mucosal sites. Our results suggest a long-term benefit from an exposure to IAV during the neonatal phase, which might be exploited by strategic vaccination against influenza early in life to enforce the host's resistance to later bacterial infections.
    Keywords:  Staphylococcus aureus; antimicrobial immunity; influenza A virus; influenza vaccination; innate immunity training; neonate; sepsis
    DOI:  https://doi.org/10.3389/fimmu.2023.1072142
  21. Front Immunol. 2023 ;14 1116548
      The skin contributes critically to health via its role as a barrier tissue against a multitude of external pathogens. The barrier function of the skin largely depends on the uppermost epidermal layer which is reinforced by skin barrier immunity. The integrity and effectiveness of skin barrier immunity strongly depends on the close interplay and communication between immune cells and the skin environment. Skin-associated adipocytes have been recognized to play a significant role in modulating skin immune responses and infection by secreting cytokines, adipokines, and antimicrobial peptides. This review summarizes the recent understanding of the interactions between skin-associated adipocytes and other skin cells in maintaining the integrity and effectiveness of skin barrier immunity.
    Keywords:  adipocytes; adipokines; antimicrobial peptides; infection; skin barrier immunity
    DOI:  https://doi.org/10.3389/fimmu.2023.1116548
  22. Biochem Soc Trans. 2023 Feb 06. pii: BST20221008. [Epub ahead of print]
      The advent of 3D cell culture technology promises to enhance understanding of cell biology within tissue microenvironments. Whilst traditional cell culturing methods have been a reliable tool for decades, they inadequately portray the complex environments in which cells inhabit in vivo. The need for better disease models has pushed the development of effective 3D cell models, providing more accurate drug screening assays. There has been great progress in developing 3D tissue models in fields such as cancer research and regenerative medicine, driven by desires to recreate the tumour microenvironment for the discovery of new chemotherapies, or development of artificial tissues or scaffolds for transplantation. Immunology is one field that lacks optimised 3D models and the biology of tissue resident immune cells such as macrophages has yet to be fully explored. This review aims to highlight the benefits of 3D cell culturing for greater understanding of macrophage biology. We review current knowledge of macrophage interactions with their tissue microenvironment and highlight the potential of 3D macrophage models in the development of more effective treatments for disease.
    Keywords:  3D culture; bioengineering; bioprinting; cell cultures; extracellular matrix; macrophages
    DOI:  https://doi.org/10.1042/BST20221008
  23. Curr Opin Crit Care. 2023 Jan 25.
      PURPOSE OF REVIEW: Study of organ crosstalk in critical illness has uncovered complex biological communication between different organ systems, but the role of microbiota in organ crosstalk has received limited attention. We highlight the emerging understanding of the gut-lung axis, and how the largest biomass of the human body in the gut may affect lung physiology in critical illness.RECENT FINDINGS: Disruption of healthy gut microbial communities and replacement by disease-promoting pathogens (pathobiome) generates a maladaptive transmitter of messages from the gut to the lungs, connected via the portal venous and the mesenteric lymphatic systems. Gut barrier impairment allows for microbial translocation (living organisms or cellular fragments) to the lungs. Host-microbiota interactions in the gut mucosa can also impact lung physiology through microbial metabolite secretion or host-derived messengers (hormones, cytokines or immune cells). Clinical examples like the prevention of ventilator-associated pneumonia by selective decontamination of the digestive tract show that the gut-lung axis can be manipulated therapeutically.
    SUMMARY: A growing body of evidence supports the pathophysiological relevance of the gut-lung axis, yet we are only at the brink of understanding the therapeutic and prognostic relevance of the gut microbiome, metabolites and host-microbe interactions in critical illness.
    DOI:  https://doi.org/10.1097/MCC.0000000000001015
  24. mBio. 2023 Feb 06. e0357122
      The microbial secretome modulates how the organism interacts with its environment. Included in the Staphylococcus aureus secretome are extracellular membrane vesicles (MVs) that consist of cytoplasmic and membrane proteins, as well as exoproteins, some cell wall-associated proteins, and glycopolymers. The extent to which MVs contribute to the diverse composition of the secretome is not understood. We performed a proteomic analysis of MVs purified from the S. aureus strain MRSA252 along with a similar analysis of the whole secretome (culture supernatant) before and after depletion of MVs. The MRSA252 secretome was comprised of 1,001 proteins, of which 667 were also present in MVs. Cell membrane-associated proteins and lipoteichoic acid in the culture supernatant were highly associated with MVs, followed by cytoplasmic and extracellular proteins. Few cell wall-associated proteins were contained in MVs, and capsular polysaccharides were found both in the secretome and MVs. When MVs were removed from the culture supernatant by ultracentrifugation, 54 of the secretome proteins were significantly depleted in abundance. Proteins packaged in MVs were characterized by an isoelectric point that was significantly higher than that of proteins excluded from MVs. Our data indicate that the generation of S. aureus MVs is a mechanism by which lipoteichoic acid, cytoplasmic, and cell membrane-associated proteins are released into the secretome. IMPORTANCE The secretome of Staphylococcus aureus includes soluble molecules and nano-sized extracellular membrane vesicles (MVs). The protein composition of both the secretome and MVs includes cytoplasmic and membrane proteins, as well as exoproteins, some cell wall-associated proteins, and glycopolymers. How the MV cargo differs from the protein composition of the secretome has not yet been addressed. Although the compositions of the secretome and MVs were strikingly similar, we identified 54 proteins that were specifically packaged in MVs. Proteins highly associated with MVs were characterized by their abundance in the secretome, an association with the bacterial membrane, and a basic isoelectric point. This study deepens our limited understanding about the contribution of MVs to the secretome of S. aureus.
    Keywords:  Staphylococcus aureus; extracellular membrane vesicle; membrane proteins; proteomics; secretome
    DOI:  https://doi.org/10.1128/mbio.03571-22
  25. Annu Rev Immunol. 2022 Feb 07.
      As an important sensor in the innate immune system, NLRP3 detects exogenous pathogenic invasions and endogenous cellular damage and responds by forming the NLRP3 inflammasome, a supramolecular complex that activates caspase-1. The three major components of the NLRP3 inflammasome are NLRP3, which captures the danger signals and recruits downstream molecules; caspase-1, which elicits maturation of the cytokines IL-1β and IL-18 and processing of gasdermin D to mediate cytokine release and pyroptosis; and ASC (apoptosis-associated speck-like protein containing a caspase recruitment domain), which functions as a bridge connecting NLRP3 and caspase-1. In this article, we review the structural information that has been obtained on the NLRP3 inflammasome and its components or subcomplexes, with special focus on the inactive NLRP3 cage, NEK7 (NIMA-related kinase 7)-licensing of NLRP3 activation, and the PYD-PYD and CARD-CARD homotypic filamentous scaffolds of the inflammasome. We further implicate structure-derived mechanisms for the assembly and activation of the NLRP3 inflammasome. Expected final online publication date for the Annual Review of Immunology, Volume 41 is April 2023. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.
    DOI:  https://doi.org/10.1146/annurev-immunol-081022-021207
  26. Front Immunol. 2023 ;14 1088501
      Staphylococcus aureus infection is a severe public health concern with the growing number of multidrug-resistant strains. S. aureus can circumvent the defense mechanisms of host immunity with the aid of multiple virulence factors. An efficacious multicomponent vaccine targeting diverse immune evasion strategies developed by S. aureus is thus crucial for its infection control. In this study, we exploited the SpyCatcher-SpyTag system to engineer bacterial outer membrane vesicles (OMVs) for the development of a multitargeting S. aureus click vaccine. We decorated OMVs with surface exposed SpyCatcher via a truncated OmpA(a.a 1-155)-SpyCatcher fusion. The engineered OMVs can flexibly bind with various SpyTag-fused S. aureus antigens to generate an OMV-based click vaccine. Compared with antigens mixed with alum adjuvant, the click vaccine simultaneously induced more potent antigen-specific humoral and Th1-based cellular immune response, which afforded protection against S. aureus Newman lethal challenge in a mouse model. Our study provided a flexible and versatile click vaccine strategy with the potential for fighting against emerging S. aureus clinical isolates.
    Keywords:  SpyCatcher-SpyTag; Staphylococcus aureus vaccine; flexible antigen display; multi-targeting vaccine; outer membrane vesicles; ‘click’ display
    DOI:  https://doi.org/10.3389/fimmu.2023.1088501
  27. Semin Immunol. 2023 Feb 07. pii: S1044-5323(23)00015-5. [Epub ahead of print]66 101724
      Innate effector cells are immune cells endowed with host protective features and cytotoxic functions. By sensing the tissue environment, innate cells have an important role in regulating the transition from homeostasis to inflammation and the establishment of pathological states, including the onset and development of cancer. The tumor microenvironment induces molecular and functional modifications in innate cells, dampening their capability to initiate and sustain anti-tumor immune responses. Emerging studies clearly showed a contribution of the microbiota in modulating the functions of innate cells in cancer. Commensal microorganisms can not only directly interact with innate cells in the tumor microenvironment but can also exert immunomodulatory features from non-tumor sites through the release of microbial products. The microbiota can mediate the priming of innate cells at mucosal tissues and determine the strength of immune responses mediated by such cells when they migrate to non-mucosal tissues, having an impact on cancer. Finally, several evidences reported a strong contribution of the microbiota in promoting innate immune responses during anti-cancer therapies leading to enhanced therapeutic efficacy. In this review, we considered the current knowledge on the role of the microbiota in shaping host innate immune responses in cancer.
    Keywords:  Cancer; Immunotherapies; Innate immune cells; Microbiota
    DOI:  https://doi.org/10.1016/j.smim.2023.101724
  28. bioRxiv. 2023 Jan 29. pii: 2023.01.29.526047. [Epub ahead of print]
      Coinfection with two notorious opportunistic pathogens, the Gram-negative Pseudomonas aeruginosa and Gram-positive Staphylococcus aureus , dominates chronic pulmonary infections. While coinfection is associated with poor patient outcomes, the interspecies interactions responsible for such decline remain unknown. Here, we dissected molecular mechanisms of interspecies sensing between P. aeruginosa and S. aureus . We discovered that P. aeruginosa senses S. aureus secreted peptides and, counterintuitively, moves towards these toxins. P. aeruginosa tolerates such a strategy through "competition sensing", whereby it preempts imminent danger/competition by arming cells with type six secretion (T6S) and iron acquisition systems. Intriguingly, while T6S is predominantly described as weaponry targeting Gram-negative and eukaryotic cells, we find that T6S is essential for full P. aeruginosa competition with S. aureus , a previously undescribed role for T6S. Importantly, competition sensing was activated during coinfection of bronchial epithelia, including T6S islands targeting human cells. This study reveals critical insight into both interspecies competition and how antagonism may cause collateral damage to the host environment.
    DOI:  https://doi.org/10.1101/2023.01.29.526047
  29. Front Immunol. 2022 ;13 1061290
      The systemic bio-organization of humans and other mammals is essentially "preprogrammed", and the basic interacting units, the cells, can be crudely mapped into discrete sets of developmental lineages and maturation states. Over several decades, however, and focusing on the immune system, we and others invoked evidence - now overwhelming - suggesting dynamic acquisition of cellular properties and functions, through tuning, re-networking, chromatin remodeling, and adaptive differentiation. The genetically encoded "algorithms" that govern the integration of signals and the computation of new states are not fully understood but are believed to be "smart", designed to enable the cells and the system to discriminate meaningful perturbations from each other and from "noise". Cellular sensory and response properties are shaped in part by recurring temporal patterns, or features, of the signaling environment. We compared this phenomenon to associative brain learning. We proposed that interactive cell learning is subject to selective pressures geared to performance, allowing the response of immune cells to injury or infection to be progressively coordinated with that of other cell types across tissues and organs. This in turn is comparable to supervised brain learning. Guided by feedback from both the tissue itself and the neural system, resident or recruited antigen-specific and innate immune cells can eradicate a pathogen while simultaneously sustaining functional homeostasis. As informative memories of immune responses are imprinted both systemically and within the targeted tissues, it is desirable to enhance tissue preparedness by incorporating attenuated-pathogen vaccines and informed choice of tissue-centered immunomodulators in vaccination schemes. Fortunately, much of the "training" that a living system requires to survive and function in the face of disturbances from outside or within is already incorporated into its design, so it does not need to deep-learn how to face a new challenge each time from scratch. Instead, the system learns from experience how to efficiently select a built-in strategy, or a combination of those, and can then use tuning to refine its organization and responses. Efforts to identify and therapeutically augment such strategies can take advantage of existing integrative modeling approaches. One recently explored strategy is boosting the flux of uninfected cells into and throughout an infected tissue to rinse and replace the infected cells.
    Keywords:  adaptive differentiation; cellular and cell population learning; context discrimination; functional homeostasis; rinse and replace; smart surveillance; systems immunology; tuning
    DOI:  https://doi.org/10.3389/fimmu.2022.1061290
  30. Front Immunol. 2022 ;13 1108071
      Mucosal associated invariant T (MAIT) cells are a population of unconventional innate T cells due to their non-MHC restriction and rapid effector responses. MAIT cells can recognise bacterial derived antigens presented on the MHC-like protein via their semi-restricted T cell receptor (TCR). Upon TCR triggering MAIT cells rapidly produce a range of effector molecules including cytokines, lytic granules and chemokines. This rapid and robust effector response makes MAIT cells critical in host responses against many bacterial pathogens. MAIT cells can also respond independent of their TCR via innate cytokines such as interleukin (IL)-18, triggering cytokine production, and are important in anti-viral responses. In addition to their protective role, MAIT cells have been implicated in numerous inflammatory diseases, including metabolic diseases often contributing to the pathogenesis via their robust cytokine production. Effector cells such as MAIT cells require significant amounts of energy to support their potent responses, and the type of nutrients available can dictate the functionality of the cell. Although data on MAIT cell metabolism is just emerging, several recent studies are starting to define the intrinsic metabolic requirements and regulators of MAIT cells. In this review we will outline our current understanding of MAIT cell metabolism, and outline their role in metabolic disease, and how disease-related changes in extrinsic metabolism can alter MAIT cell responses.
    Keywords:  MAIT; diabetes; immunometabolism; metabolic disease; obesity
    DOI:  https://doi.org/10.3389/fimmu.2022.1108071
  31. Sci Rep. 2023 Feb 06. 13(1): 2137
      Streptococcus agalactiae, also known as Group B Streptococcus (GBS) is a frequent cause of infections, including bacteraemia and other acute diseases in adults and immunocompromised individuals. We developed a novel system to study GBS within human monocytes to define the co-transcriptome of intracellular GBS (iGBS) and host cells simultaneously using dual RNA-sequencing (RNA-seq) to better define how this pathogen responds to host cells. Using human U937 monocytes and genome-sequenced GBS reference strain 874,391 in antibiotic protection assays we validated a system for dual-RNA seq based on measures of GBS and monocyte viability to ensure that the bacterial and host cell co-transcriptome reflected mainly intracellular (iGBS) rather than extracellular GBS. Elucidation of the co-transcriptome revealed 1119 dysregulated transcripts in iGBS with most genes, including several that encode virulence factors (e.g., scpB, hvgA, ribD, pil2b) exhibiting activation by upregulated expression. Infection with iGBS resulted in significant remodelling of the monocyte transcriptome, with 7587 transcripts differentially expressed including 7040 up-regulated and 547 down-regulated. qPCR confirmed that the most strongly activated genes included sht, encoding Streptococcal Histidine Triad Protein. An isogenic GBS mutant strain deficient in sht revealed a significant effect of this gene on phagocytosis of GBS and survival of the bacteria during systemic infection in mice. Identification of a novel contribution of sht to GBS virulence shows the co-transcriptome responses elucidated in GBS-infected monocytes help to shape the host-pathogen interaction and establish a role for sht in the response of the bacteria to phagocytic uptake. This study provides comprehension of concurrent transcriptional responses that occur in GBS and human monocytes that shape the host-pathogen interaction.
    DOI:  https://doi.org/10.1038/s41598-023-28117-x
  32. R Soc Open Sci. 2023 Feb;10(2): 220810
      Dynamic interactions between host, pathogen and host-associated microbiome dictate infection outcomes. Pathogens including Batrachochytrium dendrobatidis (Bd) threaten global biodiversity, but conservation efforts are hindered by limited understanding of amphibian host, Bd and microbiome interactions. We conducted a vaccination and infection experiment using Eastern hellbender salamanders (Cryptobranchus alleganiensis alleganiensis) challenged with Bd to observe infection, skin microbial communities and gene expression of host skin, pathogen and microbiome throughout the experiment. Most animals survived high Bd loads regardless of their vaccination status and vaccination did not affect pathogen load, but host gene expression differed based on vaccination. Oral vaccination (exposure to killed Bd) stimulated immune gene upregulation while topically and sham-vaccinated animals did not significantly upregulate immune genes. In early infection, topically vaccinated animals upregulated immune genes but orally and sham-vaccinated animals downregulated immune genes. Bd increased pathogenicity-associated gene expression in late infection when Bd loads were highest. The microbiome was altered by Bd, but there was no correlation between anti-Bd microbe abundance or richness and pathogen burden. Our observations suggest that hellbenders initially generate a vigorous immune response to Bd, which is ineffective at controlling disease and is subsequently modulated. Interactions with antifungal skin microbiota did not influence disease progression.
    Keywords:  Batrachochytrium dendrobatidis; amphibian; emerging infectious disease; host–pathogen interaction; microbiome; transcriptome
    DOI:  https://doi.org/10.1098/rsos.220810
  33. Microbiology (Reading). 2022 Dec;168(12):
      Bacteria withstand antibiotic onslaughts by employing a variety of strategies, one of which is persistence. Persistence occurs in a bacterial population where a subpopulation of cells (persisters) survives antibiotic treatment and can regrow in a drug-free environment. Persisters may cause the recalcitrance of infectious diseases and can be a stepping stone to antibiotic resistance, so understanding persistence mechanisms is critical for therapeutic applications. However, current understanding of persistence is pervaded by paradoxes that stymie research progress, and many aspects of this cellular state remain elusive. In this review, we summarize the putative persister mechanisms, including toxin-antitoxin modules, quorum sensing, indole signalling and epigenetics, as well as the reasons behind the inconsistent body of evidence. We highlight present limitations in the field and underscore a clinical context that is frequently neglected, in the hope of supporting future researchers in examining clinically important persister mechanisms.
    Keywords:  antibiotics; indole signalling; persister; quorum sensing; stress response; toxin/antitoxins
    DOI:  https://doi.org/10.1099/mic.0.001266
  34. Front Immunol. 2023 ;14 1032355
      Pulmonary fibrosis is an irreversible disease, and its mechanism is unclear. The lung is a vital organ connecting the respiratory tract and the outside world. The changes in lung microbiota affect the progress of lung fibrosis. The latest research showed that lung microbiota differs in healthy people, including idiopathic pulmonary fibrosis (IPF) and acute exacerbation-idiopathic pulmonary fibrosis (AE-IPF). How to regulate the lung microbiota and whether the potential regulatory mechanism can become a necessary targeted treatment of IPF are unclear. Some studies showed that immune response and lung microbiota balance and maintain lung homeostasis. However, unbalanced lung homeostasis stimulates the immune response. The subsequent biological effects are closely related to lung fibrosis. Core fucosylation (CF), a significant protein functional modification, affects the lung microbiota. CF regulates immune protein modifications by regulating key inflammatory factors and signaling pathways generated after immune response. The treatment of immune regulation, such as antibiotic treatment, vitamin D supplementation, and exosome micro-RNAs, has achieved an initial effect in clearing the inflammatory storm induced by an immune response. Based on the above, the highlight of this review is clarifying the relationship between pulmonary microbiota and immune regulation and identifying the correlation between the two, the impact on pulmonary fibrosis, and potential therapeutic targets.
    Keywords:  IPF – idiopathic pulmonary fibrosis; immune regulation; lung fibrosis; lung microbiota; microecology
    DOI:  https://doi.org/10.3389/fimmu.2023.1032355
  35. Eur J Immunol. 2023 Feb 06. e2250183
      There is no doubt that immunotherapy, particularly Immune checkpoint blockade (ICB), has drastically improved treatment of metastatic cancer patients. Microbiota composition has been proposed to be one of the reasons for failure or success. ICB works via the activation or reactivation of T cells that are 'switched off' by tumor cells or by the tumor microenvironment. Even advanced metastatic disease, previously considered as untreatable, can benefit from cancer immunotherapy. However, still a good proportion of patients does not respond to therapy or acquires resistance during treatment. Some genera or species of bacteria have been associated with treatment response or toxicity, but as the composition of the microbiota is not static, rather, it is very dynamic there is promise that by changing the microbiota composition, or by harnessing the microbiota 'secrete' tricks, one can improve treatment efficacy or reduce toxicity. Several players, including diet, prebiotics, probiotics and postbiotics have been proposed to shape the microbiota. In this minireview, we summarize very recent data on how to train the microbiota to increase ICB efficacy and to reduce toxicity. This article is protected by copyright. All rights reserved.
    Keywords:  Cancer Immunotherapy; Microbiota; metabolites; postbiotics; toxicity; treatment efficacy
    DOI:  https://doi.org/10.1002/eji.202250183
  36. Annu Rev Immunol. 2022 Feb 07.
      The innate immune system detects pathogens via germline-encoded receptors that bind to conserved pathogen ligands called pathogen-associated molecular patterns (PAMPs). Here we consider an additional strategy of pathogen sensing called effector-triggered immunity (ETI). ETI involves detection of pathogen-encoded virulence factors, also called effectors. Pathogens produce effectors to manipulate hosts to create a replicative niche and/or block host immunity. Unlike PAMPs, effectors are often diverse and rapidly evolving and can thus be unsuitable targets for direct detection by germline-encoded receptors. Effectors are instead often sensed indirectly via detection of their virulence activities. ETI is a viable strategy for pathogen sensing and is used across diverse phyla, including plants, but the molecular mechanisms of ETI are complex compared to simple receptor/ligand-based PAMP detection. Here we survey the mechanisms and functions of ETI, with a particular focus on emerging insights from animal studies. We suggest that many examples of ETI may remain to be discovered, hiding in plain sight throughout immunology. Expected final online publication date for the Annual Review of Immunology, Volume 41 is April 2023. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.
    DOI:  https://doi.org/10.1146/annurev-immunol-101721-031732
  37. Nutrients. 2023 Jan 17. pii: 486. [Epub ahead of print]15(3):
      The importance of the microbiome, and of the gut-lung axis in the origin and persistence of asthma, is an ongoing field of investigation. The process of microbial colonisation in the first three years of life is fundamental for health, with the first hundred days of life being critical. Different factors are associated with early microbial dysbiosis, such as caesarean delivery, artificial lactation and antibiotic therapy, among others. Longitudinal cohort studies on gut and airway microbiome in children have found an association between microbial dysbiosis and asthma at later ages of life. A low α-diversity and relative abundance of certain commensal gut bacterial genera in the first year of life are associated with the development of asthma. Gut microbial dysbiosis, with a lower abundance of Phylum Firmicutes, could be related with increased risk of asthma. Upper airway microbial dysbiosis, especially early colonisation by Moraxella spp., is associated with recurrent viral infections and the development of asthma. Moreover, the bacteria in the respiratory system produce metabolites that may modify the inception of asthma and is progression. The role of the lung microbiome in asthma development has yet to be fully elucidated. Nevertheless, the most consistent finding in studies on lung microbiome is the increased bacterial load and the predominance of proteobacteria, especially Haemophilus spp. and Moraxella catarrhalis. In this review we shall update the knowledge on the association between microbial dysbiosis and the origins of asthma, as well as its persistence, phenotypes, and severity.
    Keywords:  asthma; dysbiosis; microbiome; microbiota
    DOI:  https://doi.org/10.3390/nu15030486