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        Intestinal inflammation and the microbiota: Beyond diversity

        2022-12-02 08:06:13AlbercaGGFCardosoNSSSolisCastroRLNakanoAlbercaRW
        World Journal of Gastroenterology 2022年26期

        Alberca GGF, Cardoso NSS, Solis-Castro RL, Nakano V, Alberca RW

        Abstract

        Key Words: Inflammation; Microbiota; Toxins; Intestinal; Ulcerative; Colitis; Cancer

        TO THE EDlTOR

        We read with great interest the manuscript entitled “Relationship between clinical features and intestinal microbiota in Chinese patients with ulcerative colitis” published by Heet al[1] in the World Journal Gastroenterology. Heet al[1] performed an investigation on the microbiota composition on the fecal and mucosa samples from patients with ulcerative colitis. Their work reinforces the importance of the microbiota on the inflammatory process and gastrointestinal disorders. Importantly, the manuscript provided information on the composition of the gastrointestinal microbiota of patients with ulcerative colitis of various severity and patients without ulcerative colitis[1]. We would like to raise a few considerations regarding the microbiota and gastrointestinal inflammatory disorders.

        The microbiota is an ecosystem in constant regulation, influenced by the diet, antibiotics, sanitary conditions, environmental stimulus, and the host’s immune system[2]. The gastrointestinal tract is the largest reservoir of bacteria in the human body and shapes both the local and systemic immune responses[3-5]. The microbiome influences the maturation and development of the host’s immune system[6], regulating the development of food tolerance, response to inflammation, infections,vaccination, and metabolism[7,8]. Importantly, the microbiota directly influences the development of the inflammatory process independent of dietary intake[9], and abrupt alterations in the microbiota composition can result in an inflammatory insult[10]. Heet al[1] identified an increase inEscherichiaandShigellain patients with ulcerative colitis in comparison to patients without ulcerative colitis[1].EscherichiaandShigellahas been implicated in a reduction in the response to anticoagulation therapy and could impact the treatment of patients with gastrointestinal disorders and under anticoagulation therapy such as coronavirus disease 2019 patients[11-14].

        Shiga toxin-producingShigellaspecies andEscherichia coliare considered pathogenic, associated with diarrhea and colitis[15]. These toxins can induce the activation of the NOD-like receptor protein 3 inflammasome, inducing the production of interleukin (IL)-1β and IL-18 and cellular death by pyroptosis[16]. The virulence of Shiga-toxin-producingEscherichia colican lead to diarrheal sicknesses and death[17,18]. Shiga-toxins can be encapsulated within microvesicles and influence the inflammatory response in other organs, such as the kidneys[19]. Shiga toxin-producingEscherichia coli(O26:H11 strain 97-3250 and O145:H28 strain 4865/96) induces a greater production of chemokines and cytokines, such as IL-8 and IL-1β, in comparison toEscherichia coli(O9:H4 strain HS)[20].

        The complex symbiotic interaction between the microbiota and the host is mediated by an equilibrium in the tolerance and inflammatory response to microbial products in the gut[6]. Heet al[1]did not identify an increase in other strains in patients with ulcerative colitis. Nevertheless, in addition to the microbiota composition, certain commensal bacteria, such asClostridium perfringensandBacteroides fragilis, can express a wide range of toxins and metabolic compounds to induce inflammation[21-23].Clostridium perfringensis a gram-positive anaerobic bacteria, commonly in the environment and is part of the resident microbiota but can become virulent by the expression of toxin genes[24,25].Clostridium perfringenscan produce over 20 toxins including alpha (α), beta (β), epsilon (e), enterotoxins,and hydrolytic enzymes[26-29]. These toxins can damage and kill intestinal cells, disturb the epithelial barrier, and induce proinflammatory and propathogenic milieu[26,30,31].

        The alpha toxin produced byClostridium perfringensis a zinc-dependent metalloenzyme, is able to rupture the plasma membrane of the host’s cells[25,32], induces an immature profile in the host’s innate immune response (neutrophils), and is involved in the formation of myonecrosis in animals, including humans[33,34]. The β toxin is a pore-forming toxin associated with hemorrhagic diarrhea[35].Clostridium perfringenswith the expression of α and β toxins is associated with necrotic enteritis in animals and humans[36-38]. The e toxin is also pore-forming and is involved in intestinal and neurological diseases in humans[39-43].

        In addition,Clostridium perfringensis able to produce several other toxins such as enterotoxins[44-46],NetB[47,48], and TpeL[49,50], which can induce inflammatory responses, biofilm formation, and chronically disrupt the intestinal epithelium[44,47,50].Bacteroides fragilis,another resident bacteria, can produce a zinc-dependent metalloprotease called fragilisyn[51]. Fragilisyn-producingBacteroides fragilisare namedEnterotoxigenic Bacteroides Fragilis(ETBF)[52]. ETBF toxin is coded by thebftgene and is highly correlated with diarrhea in humans[53,54]. ETBF can cleave E-cadherin in the epithelial cells,allowing bacterial translocation[55,56]. ETBF induces an IL-17-mediated immune response with the infiltration of lymphocytes and neutrophils and damages the DNAviathe formation of microadenoma[4,53,54]. In addition, the inflammatory process may be mediated by several bacteria. For example, in the “driver-passenger” model, the colonization by one bacteria may facilitate the expansion and proinflammatory action of another microorganism[55].

        A recent manuscript by Avril and DePaolo[56], identified that the co-colonization of ETBF andEscherichia colistrains, harboring the pks island, promotes the development of intestinal cancer. ETBF promotes the degradation of the intestinal mucus and induction of IL-17-mediated inflammation by the host’s immune cells. This process enables the adherence ofEscherichia colito the intestinal wall, releases colibactin, and promotes cancer development[56]. Therefore, quantitative analyses are important to characterize the composition of the microbiota in several diseases and aid in the design of possible interventions to modulate the immune response of the host in microbiota-mediated inflammatory disorders[1]. Nevertheless, due to the potential pathobiont role of several resident bacteria, investigations on toxin-producing bacteria are crucial for an overall interpretation of the role of the microbiota on gastrointestinal disorders.

        FOOTNOTES

        Author contributions:All authors wrote and reviewed the manuscript.

        Conflict-of-interest statement:All the authors report no relevant conflicts of interest for this article.

        Open-Access:This article is an open-access article that was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution NonCommercial (CC BYNC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non

        commercial. See: https://creativecommons.org/Licenses/by-nc/4.0/

        Country/Territory of origin:Brazil

        ORClD number:Gabriela Gama Freire Alberca 0000-0002-3467-5562; Naiane Samira Souza Cardoso 0000-0002-3305-6567;Rosa Liliana Solis-Castro 0000-0002-1813-8644; Viviane Nakano 0000-0002-7005-3701; Ricardo Wesley Alberca 0000-0002-3602-3306.

        S-Editor:Wang JJ

        L-Editor:Filipodia

        P-Editor:Wang JJ

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