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Cells
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Exploring the Molecular Functionality of Microbiome-Immune System Interaction
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Exploring the Molecular Functionality of Microbiome-Immune System Interaction

A special issue of Cells (ISSN 2073-4409). This special issue belongs to the section "Cellular Immunology".

Deadline for manuscript submissions: closed (30 June 2022) | Viewed by 22792

Special Issue Editors

Dr. Carlos R. Zárate-Bladés

E-Mail Website
Guest Editor
Laboratory of Immunoregulation, Dept of Microbiology, Immunology and Parasitology, Federal University of Santa Catarina, Campus Trindade, Florianopolis SC 88040-900, Brazil
Interests: microbiome influence on immunity; immune regulatory mechanisms; therapeutic use of microbiome and its metabolites; One Health–microbiome relationship
Dr. Melissa P. Mezzari

E-Mail Website1 Website2
Guest Editor
Alkek Center for Metagenomics and Microbiome Research, Department of Molecular Virology & Microbiology, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA
Interests: microbial ecology; microbiome of the built environment; biomonitoring; epidemiology; toxicology; bioinformatics; genome sequencing

Special Issue Information

Dear Colleagues,

Commensal microbial communities represent a complex eco-system, pivotal for several aspects of host homeostasis. The alteration of their composition and structure is a direct response of the several pathological conditions that implicate infectious and non-infectious diseases. Exciting discoveries are being made regarding the role of the microbiome in human health, and microbial dysbiosis is a particular key aspect to be considered in order to prevent or treat a wide array of conditions. Examples include persistent Clostridioides difficile infection, inflammatory bowel disease, some types of tumors and autoimmune diseases, allergy, metabolic disorders autism, and many others. However, the microbiome-related molecular events underlying the beneficial effects for host physiology remain far from being completely understood. Nonetheless, important insights of these effects came from studies about the role of the immune system since it acts as a decoder system of the microbiome signals for the host. In turn, the microbiome affects not only the function but also the development of the innate and adaptive components of the immune system. This dialogue allows the elicitation of effective immune responses against pathogens, the induction of tolerance to innocuous antigens and the production of several metabolites which are important for the function of basically all other human systems.

Therefore, the study of the molecular pathways implicated in host immunity and microbiome function crosstalk is a cutting edge of research in the complex host–microbiome interaction area. This Special Issue calls for studies on the molecular events that define the influence of microbiome on host immunity and vice versa. Special interests will focus on, but are not limited to, studies exploring host–microbiome interactions from a metagenomic and metabolomic integrative perspective. Other omics approaches will also be considered. Articles on experimental models or clinical/interventional studies in humans are welcome.

Dr. Carlos R. Zárate-Bladés
Dr. Melissa P. Mezzari
Guest Editors

Manuscript Submission Information

Manuscripts should be submitted online at www.mdpi.com by registering and logging in to this website. Once you are registered, click here to go to the submission form. Manuscripts can be submitted until the deadline. All submissions that pass pre-check are peer-reviewed. Accepted papers will be published continuously in the journal (as soon as accepted) and will be listed together on the special issue website. Research articles, review articles as well as short communications are invited. For planned papers, a title and short abstract (about 100 words) can be sent to the Editorial Office for announcement on this website.

Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Cells is an international peer-reviewed open access semimonthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2700 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

  • microbiota
  • commensal microorganism
  • immunity
  • immune mechanism
  • omics science
  • metabolomics
  • 16S sequencing
  • disease model
  • metabolite
  • signaling pathway

Published Papers (7 papers)

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Research

19 pages, 3610 KiB  
Article
Ulcerative Colitis in Response to Fecal Microbiota Transplantation via Modulation of Gut Microbiota and Th17/Treg Cell Balance
by Chunlan Huang, Qixiang Mei, Lihong Lou, Zehua Huang, Yang Fu, Junjie Fan, Jingjing Wang, Nuoming Yin, Yi Zheng, Yingying Lu and Yue Zeng
Cells 2022, 11(11), 1851; https://0-doi-org.brum.beds.ac.uk/10.3390/cells11111851 - 05 Jun 2022
Cited by 9 | Viewed by 2932
Abstract
Background: Fecal microbiota transplantation (FMT) may contribute to disease remission in ulcerative colitis (UC). We studied the microbiota change and its regulation on T cells after FMT. Methods: Patients with mild to moderately active UC were included to receive FMT. The intestinal histopathological [...] Read more.
Background: Fecal microbiota transplantation (FMT) may contribute to disease remission in ulcerative colitis (UC). We studied the microbiota change and its regulation on T cells after FMT. Methods: Patients with mild to moderately active UC were included to receive FMT. The intestinal histopathological changes and barrier function were evaluated. The fecal samples of donors and patients were analyzed by 16S rRNA gene-based microbiota analysis, and the colon Th17 and Treg cells were assessed. Results: Fifteen patients completed the 8-week-follow-up. A total of 10 patients (66.7%) were in the responders (RE) group and five in the non-responders (NR) group. The Nancy histological index and fecal calprotectin decreased (p < 0.001, p = 0.06, respectively) and Occludin and Claudin1 increased in the RE group. The abundance of Faecalibaterium increased significantly by 2.3-fold in the RE group at week 8 (p = 0.043), but it was suppressed in the NR group. Fecal calprotectin (r = −0.382, p = 0.003) and Nancy index (r = −0.497, p = 0.006) were correlated inversely with the abundance of Faecalibacterium, respectively. In the RE group the relative mRNA expression of RORγt decreased and Foxp3 increased. Significantly decreased CD4+ RORγt+ Th17 and increased CD4+ Foxp3+ Treg were also observed in the RE group. The relative abundance of Faecalibacterium correlated with CD4+ RORγt+ Th17 (r = −0.430, p = 0.018) and CD4+ Foxp3+ Treg (r = 0.571, p = 0.001). Conclusions: The long-term Faecalibaterium colonization following FMT plays a crucial role in UC remission by alleviating intestinal inflammation. This anti-inflammatory effect of Faecalibacterium may be achieved by regulating the imbalance of Th17/Treg levels in UC. Full article
(This article belongs to the Special Issue Exploring the Molecular Functionality of Microbiome-Immune System Interaction)
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18 pages, 1668 KiB  
Article
The Impact of Escherichia coli Probiotic Strain O83:K24:H31 on the Maturation of Dendritic Cells and Immunoregulatory Functions In Vitro and In Vivo
by Lenka Súkeníková, Viktor Černý, Jan Věcek, Petra Petrásková, Olga Novotná, Šimon Vobruba, Tereza Michalčíková, Jan Procházka, Libuše Kolářová, Ludmila Prokešová and Jiří Hrdý
Cells 2022, 11(10), 1624; https://0-doi-org.brum.beds.ac.uk/10.3390/cells11101624 - 12 May 2022
Cited by 2 | Viewed by 1830
Abstract
Early postnatal events are important for the development of the neonatal immune system. Harboring the pioneering microorganisms forming the microbiota of the neonatal gastrointestinal tract is important for priming the immune system, as well as inducing appropriate tolerance to the relatively innocuous environmental [...] Read more.
Early postnatal events are important for the development of the neonatal immune system. Harboring the pioneering microorganisms forming the microbiota of the neonatal gastrointestinal tract is important for priming the immune system, as well as inducing appropriate tolerance to the relatively innocuous environmental antigens and compounds of normal healthy microbiota. Early postnatal supplementation of suitable, safe probiotics could accelerate this process. In the current study, the immunomodulatory capacity of the probiotic strain of Escherichia coli O83:K24:H31 (EcO83) was characterized in vitro and in vivo. We compared the capacity of EcO83 with and without hemolytic activity on selected immune characteristics in vitro as determined by flow cytometry and quantitative real-time PCR. Both strains with and without hemolytic activity exerted comparable capacity on the maturation of dendritic cells while preserving the induction of interleukin 10 (Il10) expression in dendritic cells and T cells cocultured with EcO83 primed dendritic cells. Early postnatal supplementation with EcO83 led to massive but transient colonization of the neonatal gastrointestinal tract, as detected by in vivo bioimaging. Early postnatal EcO83 administration promoted gut barrier function by increasing the expression of claudin and occludin and the expression of Il10. Early postnatal EcO83 application promotes maturation of the neonatal immune system and promotes immunoregulatory and gut barrier functions. Full article
(This article belongs to the Special Issue Exploring the Molecular Functionality of Microbiome-Immune System Interaction)
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17 pages, 10626 KiB  
Article
Metabolomics of Acute vs. Chronic Spinach Intake in an Apc–Mutant Genetic Background: Linoleate and Butanoate Metabolites Targeting HDAC Activity and IFN–γ Signaling
by Ying-Shiuan Chen, Jia Li, Sultan Neja, Sabeeta Kapoor, Jorge Enrique Tovar Perez, Chakrapani Tripathi, Rani Menon, Arul Jayaraman, Kyongbum Lee, Wan Mohaiza Dashwood, Shan Wang, Ke Zhang, Koichi Kobayashi, Praveen Rajendran and Roderick Dashwood
Cells 2022, 11(3), 573; https://0-doi-org.brum.beds.ac.uk/10.3390/cells11030573 - 07 Feb 2022
Cited by 3 | Viewed by 3171
Abstract
There is growing interest in the crosstalk between the gut microbiome, host metabolomic features, and disease pathogenesis. The current investigation compared long–term (26 week) and acute (3 day) dietary spinach intake in a genetic model of colorectal cancer. Metabolomic analyses in the polyposis [...] Read more.
There is growing interest in the crosstalk between the gut microbiome, host metabolomic features, and disease pathogenesis. The current investigation compared long–term (26 week) and acute (3 day) dietary spinach intake in a genetic model of colorectal cancer. Metabolomic analyses in the polyposis in rat colon (Pirc) model and in wild–type animals corroborated key contributions to anticancer outcomes by spinach–derived linoleate bioactives and a butanoate metabolite linked to increased α–diversity of the gut microbiome. Combining linoleate and butanoate metabolites in human colon cancer cells revealed enhanced apoptosis and reduced cell viability, paralleling the apoptosis induction in colon tumors from rats given long–term spinach treatment. Mechanistic studies in cell–based assays and in vivo implicated the linoleate and butanoate metabolites in targeting histone deacetylase (HDAC) activity and the interferon–γ (IFN–γ) signaling axis. Clinical translation of these findings to at–risk patients might provide valuable quality–of–life benefits by delaying surgical interventions and drug therapies with adverse side effects. Full article
(This article belongs to the Special Issue Exploring the Molecular Functionality of Microbiome-Immune System Interaction)
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21 pages, 45692 KiB  
Article
Endocannabinoid Anandamide Attenuates Acute Respiratory Distress Syndrome through Modulation of Microbiome in the Gut-Lung Axis
by Muthanna Sultan, Kiesha Wilson, Osama A. Abdulla, Philip Brandon Busbee, Alina Hall, Taylor Carter, Narendra Singh, Saurabh Chatterjee, Prakash Nagarkatti and Mitzi Nagarkatti
Cells 2021, 10(12), 3305; https://0-doi-org.brum.beds.ac.uk/10.3390/cells10123305 - 25 Nov 2021
Cited by 15 | Viewed by 4089
Abstract
Acute respiratory distress syndrome (ARDS) is a serious lung condition characterized by severe hypoxemia leading to limitations of oxygen needed for lung function. In this study, we investigated the effect of anandamide (AEA), an endogenous cannabinoid, on Staphylococcal enterotoxin B (SEB)-mediated ARDS in [...] Read more.
Acute respiratory distress syndrome (ARDS) is a serious lung condition characterized by severe hypoxemia leading to limitations of oxygen needed for lung function. In this study, we investigated the effect of anandamide (AEA), an endogenous cannabinoid, on Staphylococcal enterotoxin B (SEB)-mediated ARDS in female mice. Single-cell RNA sequencing data showed that the lung epithelial cells from AEA-treated mice showed increased levels of antimicrobial peptides (AMPs) and tight junction proteins. MiSeq sequencing data on 16S RNA and LEfSe analysis demonstrated that SEB caused significant alterations in the microbiota, with increases in pathogenic bacteria in both the lungs and the gut, while treatment with AEA reversed this effect and induced beneficial bacteria. AEA treatment suppressed inflammation both in the lungs as well as gut-associated mesenteric lymph nodes (MLNs). AEA triggered several bacterial species that produced increased levels of short-chain fatty acids (SCFAs), including butyrate. Furthermore, administration of butyrate alone could attenuate SEB-mediated ARDS. Taken together, our data indicate that AEA treatment attenuates SEB-mediated ARDS by suppressing inflammation and preventing dysbiosis, both in the lungs and the gut, through the induction of AMPs, tight junction proteins, and SCFAs that stabilize the gut-lung microbial axis driving immune homeostasis. Full article
(This article belongs to the Special Issue Exploring the Molecular Functionality of Microbiome-Immune System Interaction)
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21 pages, 6743 KiB  
Article
SP-1, a Serine Protease from the Gut Microbiota, Influences Colitis and Drives Intestinal Dysbiosis in Mice
by Aicha Kriaa, Amin Jablaoui, Soufien Rhimi, Souha Soussou, Héla Mkaouar, Vincent Mariaule, Natalia Gruba, Ali Gargouri, Emmanuelle Maguin, Adam Lesner and Moez Rhimi
Cells 2021, 10(10), 2658; https://0-doi-org.brum.beds.ac.uk/10.3390/cells10102658 - 05 Oct 2021
Cited by 3 | Viewed by 2365
Abstract
Increased protease activity has been linked to the pathogenesis of IBD. While most studies have been focusing on host proteases in gut inflammation, it remains unclear how to address the potential contribution of their bacterial counterparts. In the present study, we report a [...] Read more.
Increased protease activity has been linked to the pathogenesis of IBD. While most studies have been focusing on host proteases in gut inflammation, it remains unclear how to address the potential contribution of their bacterial counterparts. In the present study, we report a functional characterization of a newly identified serine protease, SP-1, from the human gut microbiota. The serine protease repertoire of gut Clostridium was first explored, and the specificity of SP-1 was analyzed using a combinatorial chemistry method. Combining in vitro analyses and a mouse model of colitis, we show that oral administration of recombinant bacteria secreting SP-1 (i) compromises the epithelial barrier, (ii) alters the microbial community, and (ii) exacerbates colitis. These findings suggest that gut microbial protease activity may constitute a valuable contributor to IBD and could, therefore, represent a promising target for the treatment of the disease. Full article
(This article belongs to the Special Issue Exploring the Molecular Functionality of Microbiome-Immune System Interaction)
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16 pages, 4999 KiB  
Article
Obesity-Induced Dysbiosis Exacerbates IFN-γ Production and Pulmonary Inflammation in the Mycobacterium tuberculosis Infection
by Sandra Patricia Palma Albornoz, Thais Fernanda de Campos Fraga-Silva, Ana Flávia Gembre, Rômulo Silva de Oliveira, Fernanda Mesquita de Souza, Tamara Silva Rodrigues, Isis do Carmo Kettelhut, Camila Sanches Manca, Alceu Afonso Jordao, Leandra Naira Zambelli Ramalho, Paulo Eduardo Martins Ribolla, Daniela Carlos and Vânia Luiza Deperon Bonato
Cells 2021, 10(7), 1732; https://0-doi-org.brum.beds.ac.uk/10.3390/cells10071732 - 08 Jul 2021
Cited by 5 | Viewed by 3152
Abstract
The microbiota of the gut–lung axis affects local and far-reaching immune responses and might also trigger chronic and inflammatory diseases. We hypothesized that gut dysbiosis induced by obesity, which coexists in countries with a high tuberculosis burden, aggravates the host susceptibility and the [...] Read more.
The microbiota of the gut–lung axis affects local and far-reaching immune responses and might also trigger chronic and inflammatory diseases. We hypothesized that gut dysbiosis induced by obesity, which coexists in countries with a high tuberculosis burden, aggravates the host susceptibility and the pulmonary damage tolerance. To assess our hypothesis, we used a model of high-fat diet (HFD)-induced obesity, followed by infection of C57BL/6 mice with Mycobacterium tuberculosis. We showed that obesity increased the susceptibility, the pulmonary inflammation and IFN-γ levels in M. tuberculosis-infected mice. During the comorbidity obesity and tuberculosis, there is an increase of Bacteroidetes and Firmicutes in the lungs, and an increase of Firmicutes and butyrate in the feces. Depletion of gut microbiota by antibiotic treatment in the obese infected mice reduced the frequencies of CD4+IFN-γ+IL-17− cells and IFN-γ levels in the lungs, associated with an increase of Lactobacillus. Our findings reinforce the role of the gut–lung axis in chronic infections and suggest that the gut microbiota modulation may be a potential host-directed therapy as an adjuvant to treat TB in the context of IFN-γ-mediated immunopathology. Full article
(This article belongs to the Special Issue Exploring the Molecular Functionality of Microbiome-Immune System Interaction)
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15 pages, 5918 KiB  
Article
Gut Microbiome Profiles and Associated Metabolic Pathways in HIV-Infected Treatment-Naïve Patients
by Wellinton M. do Nascimento, Aline Machiavelli, Luiz G. E. Ferreira, Luisa Cruz Silveira, Suwellen S. D. de Azevedo, Gonzalo Bello, Daniel P. Smith, Melissa P. Mezzari, Joseph F. Petrosino, Rubens Tadeu Delgado Duarte, Carlos R. Zárate-Bladés and Aguinaldo R. Pinto
Cells 2021, 10(2), 385; https://0-doi-org.brum.beds.ac.uk/10.3390/cells10020385 - 13 Feb 2021
Cited by 7 | Viewed by 3649
Abstract
The normal composition of the intestinal microbiota is a key factor for maintaining healthy homeostasis, and accordingly, dysbiosis is well known to be present in HIV-1 patients. This article investigates the gut microbiota profile of antiretroviral therapy-naive HIV-1 patients and healthy donors living [...] Read more.
The normal composition of the intestinal microbiota is a key factor for maintaining healthy homeostasis, and accordingly, dysbiosis is well known to be present in HIV-1 patients. This article investigates the gut microbiota profile of antiretroviral therapy-naive HIV-1 patients and healthy donors living in Latin America in a cohort of 13 HIV positive patients (six elite controllers, EC, and seven non-controllers, NC) and nine healthy donors (HD). Microbiota compositions in stool samples were determined by sequencing the V3-V4 region of the bacterial 16S rRNA, and functional prediction was inferred using PICRUSt. Several taxa were enriched in EC compared to NC or HD groups, including Acidaminococcus, Clostridium methylpentosum, Barnesiella, Eubacterium coprostanoligenes, and Lachnospiraceae UCG-004. In addition, our data indicate that the route of infection is an important factor associated with changes in gut microbiome composition, and we extend these results by identifying several metabolic pathways associated with each route of infection. Importantly, we observed several bacterial taxa that might be associated with different viral subtypes, such as Succinivibrio, which were more abundant in patients infected by HIV subtype B, and Streptococcus enrichment in patients infected by subtype C. In conclusion, our data brings a significant contribution to the understanding of dysbiosis-associated changes in HIV infection and describes, for the first time, differences in microbiota composition according to HIV subtypes. These results warrant further confirmation in a larger cohort of patients. Full article
(This article belongs to the Special Issue Exploring the Molecular Functionality of Microbiome-Immune System Interaction)
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