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      Giardia co-infection promotes the secretion of antimicrobial peptides beta-defensin 2 and trefoil factor 3 and attenuates attaching and effacing bacteria-induced intestinal disease

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          Abstract

          Our understanding of polymicrobial gastrointestinal infections and their effects on host biology remains incompletely understood. Giardia duodenalis is an ubiquitous intestinal protozoan parasite infecting animals and humans. Concomitant infections with Giardia and other gastrointestinal pathogens commonly occur. In countries with poor sanitation, Giardia infection has been associated with decreased incidence of diarrheal disease and fever, and reduced serum inflammatory markers release, via mechanisms that remain obscure. This study analyzed Giardia spp. co-infections with attaching and effacing (A/E) pathogens, and assessed whether and how the presence of Giardia modulates host responses to A/E enteropathogens, and alters intestinal disease outcome. In mice infected with the A/E pathogen Citrobacter rodentium, co-infection with Giardia muris significantly attenuated weight loss, macro- and microscopic signs of colitis, bacterial colonization and translocation, while concurrently enhancing the production and secretion of antimicrobial peptides (AMPs) mouse β-defensin 3 and trefoil factor 3 (TFF3). Co-infection of human intestinal epithelial cells (Caco-2) monolayers with G. duodenalis trophozoites and enteropathogenic Escherichia coli (EPEC) enhanced the production of the AMPs human β-defensin 2 (HBD-2) and TFF3; this effect was inhibited with treatment of G. duodenalis with cysteine protease inhibitors. Collectively, these results suggest that Giardia infections are capable of reducing enteropathogen-induced colitis while increasing production of host AMPs. Additional studies also demonstrated that Giardia was able to directly inhibit the growth of pathogenic bacteria. These results reveal novel mechanisms whereby Giardia may protect against gastrointestinal disease induced by a co-infecting A/E enteropathogen. Our findings shed new light on how microbial-microbial interactions in the gut may protect a host during concomitant infections.

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          Diarrheagenic Escherichia coli.

          Escherichia coli is the predominant nonpathogenic facultative flora of the human intestine. Some E. coli strains, however, have developed the ability to cause disease of the gastrointestinal, urinary, or central nervous system in even the most robust human hosts. Diarrheagenic strains of E. coli can be divided into at least six different categories with corresponding distinct pathogenic schemes. Taken together, these organisms probably represent the most common cause of pediatric diarrhea worldwide. Several distinct clinical syndromes accompany infection with diarrheagenic E. coli categories, including traveler's diarrhea (enterotoxigenic E. coli), hemorrhagic colitis and hemolytic-uremic syndrome (enterohemorrhagic E. coli), persistent diarrhea (enteroaggregative E. coli), and watery diarrhea of infants (entero-pathogenic E. coli). This review discusses the current level of understanding of the pathogenesis of the diarrheagenic E. coli strains and describes how their pathogenic schemes underlie the clinical manifestations, diagnostic approach, and epidemiologic investigation of these important pathogens.
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            Paneth cells, antimicrobial peptides and maintenance of intestinal homeostasis.

            Building and maintaining a homeostatic relationship between a host and its colonizing microbiota entails ongoing complex interactions between the host and the microorganisms. The mucosal immune system, including epithelial cells, plays an essential part in negotiating this equilibrium. Paneth cells (specialized cells in the epithelium of the small intestine) are an important source of antimicrobial peptides in the intestine. These cells have become the focus of investigations that explore the mechanisms of host-microorganism homeostasis in the small intestine and its collapse in the processes of infection and chronic inflammation. In this Review, we provide an overview of the intestinal microbiota and describe the cell biology of Paneth cells, emphasizing the composition of their secretions and the roles of these cells in intestinal host defence and homeostasis. We also highlight the implications of Paneth cell dysfunction in susceptibility to chronic inflammatory bowel disease.
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              Zoonotic potential and molecular epidemiology of Giardia species and giardiasis.

              Molecular diagnostic tools have been used recently in assessing the taxonomy, zoonotic potential, and transmission of Giardia species and giardiasis in humans and animals. The results of these studies have firmly established giardiasis as a zoonotic disease, although host adaptation at the genotype and subtype levels has reduced the likelihood of zoonotic transmission. These studies have also identified variations in the distribution of Giardia duodenalis genotypes among geographic areas and between domestic and wild ruminants and differences in clinical manifestations and outbreak potentials of assemblages A and B. Nevertheless, our efforts in characterizing the molecular epidemiology of giardiasis and the roles of various animals in the transmission of human giardiasis are compromised by the lack of case-control and longitudinal cohort studies and the sampling and testing of humans and animals living in the same community, the frequent occurrence of infections with mixed genotypes and subtypes, and the apparent heterozygosity at some genetic loci for some G. duodenalis genotypes. With the increased usage of multilocus genotyping tools, the development of next-generation subtyping tools, the integration of molecular analysis in epidemiological studies, and an improved understanding of the population genetics of G. duodenalis in humans and animals, we should soon have a better appreciation of the molecular epidemiology of giardiasis, the disease burden of zoonotic transmission, the taxonomy status and virulences of various G. duodenalis genotypes, and the ecology of environmental contamination.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                16 June 2017
                2017
                : 12
                : 6
                : e0178647
                Affiliations
                [1 ]Department of Biological Sciences, University of Calgary, Calgary, Alberta, Canada
                [2 ]Inflammation Research Network, University of Calgary, Calgary, Alberta, Canada
                [3 ]Host-Parasite Interactions, University of Calgary, Calgary, Alberta, Canada
                [4 ]Department of Pediatrics, Division of Gastroenterology, Child and Family Research Institute, Vancouver, British Columbia, Canada
                [5 ]Department of Physiology & Pharmacology, University of Calgary, Alberta, Canada
                Aga Khan University Hospital Nairobi, KENYA
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                • Conceptualization: AM J-PM JAC AGB.

                • Data curation: AM AO J-PM.

                • Formal analysis: AM AO.

                • Funding acquisition: AGB JLW.

                • Investigation: AM J-PM AO JAC TF.

                • Methodology: AM J-PM JAC BAV JLW AGB.

                • Project administration: AM AGB TF.

                • Resources: AGB BAV JLW.

                • Supervision: AM J-PM JAC BAV JLW AGB.

                • Validation: AM J-PM JAC AGB.

                • Visualization: AM AO J-PM.

                • Writing – original draft: AM J-PM JAC AGB.

                • Writing – review & editing: AM J-PM JAC AO BAV JLW AGB.

                Author information
                http://orcid.org/0000-0002-1205-5936
                Article
                PONE-D-17-05191
                10.1371/journal.pone.0178647
                5473565
                28622393
                44f72c6d-9e8f-48a2-938e-7f98230ba859
                © 2017 Manko et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 24 February 2017
                : 16 May 2017
                Page count
                Figures: 7, Tables: 0, Pages: 22
                Funding
                Funded by: Canadian Network for Research and Innovation in Machining Technology, Natural Sciences and Engineering Research Council of Canada (CA)
                Award ID: Discovery Grant #183681-2011
                Award Recipient :
                Funded by: Natural Sciences and Engineering Research Council of Canada Collaborative Research and Training Experience Program (NSERC CREATE)
                Award ID: #413888-2012
                Award Recipient :
                Funded by: Canadian Institutes of Health Research (CIHR)
                Award ID: # 12033
                Award Recipient :
                Funded by: Crohn’s Colitis Canada (CCC) grant in aid of research
                Award ID: #20142017
                Award Recipient :
                Funded by Natural Sciences and Engineering Research Council of Canada (NSERC), Discovery Grant #183681-2011, www.nserc-crsng.gc.ca, Natural Sciences and Engineering Research Council of Canada Collaborative Research and Training Experience Program (NSERC CREATE), #413888-2012, www.nserc-crsng.gc.ca, Canadian Institutes of Health Research (CIHR) # 12033, www.cihr.gc.ca/e/193.html, Crohn’s Colitis Canada (CCC) grant in aid of research, #20142017.
                Categories
                Research Article
                Biology and Life Sciences
                Organisms
                Protozoans
                Parasitic Protozoans
                Giardia
                Medicine and Health Sciences
                Infectious Diseases
                Co-Infections
                Biology and Life Sciences
                Parasitology
                Parasite Groups
                Apicomplexa
                Trophozoites
                Biology and Life Sciences
                Anatomy
                Digestive System
                Gastrointestinal Tract
                Medicine and Health Sciences
                Anatomy
                Digestive System
                Gastrointestinal Tract
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Pathogenesis
                Host-Pathogen Interactions
                Biology and Life Sciences
                Anatomy
                Digestive System
                Gastrointestinal Tract
                Colon
                Medicine and Health Sciences
                Anatomy
                Digestive System
                Gastrointestinal Tract
                Colon
                Medicine and Health Sciences
                Parasitic Diseases
                Parasitic Intestinal Diseases
                Biology and Life Sciences
                Biochemistry
                Enzymology
                Enzymes
                Proteases
                Cysteine Proteases
                Biology and Life Sciences
                Biochemistry
                Proteins
                Enzymes
                Proteases
                Cysteine Proteases
                Custom metadata
                All relevant data are within the paper and its Supporting Information file.

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