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      Changes of the Intestinal Microbiome–Host Homeostasis in HIV-Infected Individuals – A Focus on the Bacterial Gut Microbiome

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          Abstract

          Human immunodeficiency virus (HIV) infections cause severe CD4+ T cell depletion leading to chronic inflammation and immune activation, impaired barrier function, and microbial translocation. Even under effective antiretroviral therapy, these processes persist, leading to gut microbiome dysbiosis and disturbance of microbiome–host homeostasis. This systematic review aims at analyzing how gut microbiome and host immune system influence each other during HIV pathogenesis. An online search applying the PubMed database was conducted. The number of total results ( n = 35) was narrowed down to 5 relevant studies focusing on the interaction between the host and gut microbiome, whereas strict exclusion criteria were applied, thereby assuring that no other comorbidities impacted study results. Our analyses revealed that gut microbiome diversity correlated positively with CD4+ T cell counts and negatively with microbial translocation markers. However, quantitative changes in bacterial richness did not consistently correlate with the numbers of metabolically active bacterial populations. Despite the reported increase in potentially pathogenic bacteria and, conversely, decrease in protective populations, the gut microbiota exhibited immune-modulating qualities given that mucosal inflammatory sequelae were dampened by decreasing pro-inflammatory and accelerating anti-inflammatory cytokine responses. Future research is needed to further elucidate these findings, to gain a deeper insight into host–microbiota interactions and to develop novel therapeutic strategies.

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          Most cited references31

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          Intestinal microbiota, microbial translocation, and systemic inflammation in chronic HIV infection.

          Despite effective antiretroviral therapy (ART), patients with chronic human immunodeficiency virus (HIV) infection have increased microbial translocation and systemic inflammation. Alterations in the intestinal microbiota may play a role in microbial translocation and inflammation.
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            An altered intestinal mucosal microbiome in HIV-1 infection is associated with mucosal and systemic immune activation and endotoxemia

            HIV-1 infection disrupts the intestinal immune system, leading to microbial translocation and systemic immune activation. We investigated the impact of HIV-1 infection on the intestinal microbiome and its association with mucosal T cell and dendritic cell (DC) frequency and activation, as well as with levels of systemic T cell activation, inflammation and microbial translocation. Bacterial 16S ribosomal DNA sequencing was performed on colon biopsies and fecal samples from subjects with chronic, untreated HIV-1 infection and uninfected control subjects. Colon biopsies of HIV-1 infected subjects had increased abundances of Proteobacteria and decreased abundances of Firmicutes compared to uninfected donors. Furthermore at the genus level, a significant increase in Prevotella and decrease in Bacteroides was observed in HIV-1 infected subjects, indicating a disruption in the Bacteroidetes bacterial community structure. This HIV-1-associated increase in Prevotella abundance was associated with increased numbers of activated colonic T cells and myeloid DCs. Principal coordinates analysis demonstrated an HIV-1-related change in the microbiome that was associated with increased mucosal cellular immune activation, microbial translocation and blood T cell activation. These observations suggest that an important relationship exists between altered mucosal bacterial communities and intestinal inflammation during chronic HIV-1 infection.
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              Gut Microbiota Linked to Sexual Preference and HIV Infection

              The precise effects of HIV-1 on the gut microbiome are unclear. Initial cross-sectional studies provided contradictory associations between microbial richness and HIV serostatus and suggested shifts from Bacteroides to Prevotella predominance following HIV-1 infection, which have not been found in animal models or in studies matched for HIV-1 transmission groups. In two independent cohorts of HIV-1-infected subjects and HIV-1-negative controls in Barcelona (n = 156) and Stockholm (n = 84), men who have sex with men (MSM) predominantly belonged to the Prevotella-rich enterotype whereas most non-MSM subjects were enriched in Bacteroides, independently of HIV-1 status, and with only a limited contribution of diet effects. Moreover, MSM had a significantly richer and more diverse fecal microbiota than non-MSM individuals. After stratifying for sexual orientation, there was no solid evidence of an HIV-specific dysbiosis. However, HIV-1 infection remained consistently associated with reduced bacterial richness, the lowest bacterial richness being observed in subjects with a virological-immune discordant response to antiretroviral therapy. Our findings indicate that HIV gut microbiome studies must control for HIV risk factors and suggest interventions on gut bacterial richness as possible novel avenues to improve HIV-1-associated immune dysfunction.

                Author and article information

                Journal
                Eur J Microbiol Immunol (Bp)
                Eur J Microbiol Immunol (Bp)
                EUJMI
                European Journal of Microbiology & Immunology
                Akadémiai Kiadó (Budapest )
                2062-509X
                2062-8633
                19 August 2017
                September 2017
                : 7
                : 3
                : 158-167
                Affiliations
                Department of Microbiology and Hygiene, Charité – Universitätsmedizin Berlin , Berlin, Germany
                Author notes
                * Department of Microbiology and Hygiene, Charité – University Medicine Berlin, CC5, Campus Benjamin Franklin, FEM, Garystr. 5, D-14195 Berlin, Germany; +49-30-450524318; markus.heimesaat@ 123456charite.de

                Abbreviations: AA, arachidonic acid; ART, antiretroviral therapy; BR, bilirubin; BV, biliverdin; Dol-b-G, dolichol-b-D-glucosyl phosphate; Dol-P, dolichol phosphate; ESR, erythrocyte sedimentation rate; GALT, gut associated lymphoid tissue; GIT, gastrointestinal tract; HIV, human immunodeficiency virus; Hs-CRP, high sensitivity C-reactive protein; INR, immune non-responder; IR, immune responder; LBP, lipopolysaccharide-binding protein; LPS, lipopolysaccharide; LTB4, leukotriene B4; MeSH, medical subject headings; MSM, men having sex with men; Neu5Ac, N-acetylneuraminic acid; SIV, simian immunodeficiency virus; Th, T helper type; UGT, uridine glucuronyl transferases; URO, urobilinogen; VU, viremic untreated patients

                Article
                10.1556/1886.2017.00016
                5632743
                ee95316f-23ad-4e6b-86c6-6dc40d346f57
                © 2017, The Author(s)

                This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 International License ( https://creativecommons.org/licenses/by-nc/4.0/), which permits unrestricted use, distribution, and reproduction in any medium for non-commercial purposes, provided the original author and source are credited, a link to the CC License is provided, and changes – if any – are indicated.

                History
                : 28 June 2017
                : 24 July 2017
                Page count
                Figures: 0, Tables: 2, Equations: 0, References: 42, Pages: 10
                Categories
                Review Article

                hiv,intestinal microbiota,gut microbiome–host homeostasis,dysbiosis,bacterial richness,bacterial translocation,chronic immune activation,inflammation,immune recovery,probiotics

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