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Helicobacter Old Herborn University Seminar Monograph 18: From friends to foes. Editors: Peter J. Heidt, Tore Midtvedt, Volker Rusch, and Dirk van der Waaij. Herborn Litterae, Herborn-Dill, Germany: 1-10 (2005). HELICOBACTER: CHRONIC EFFECTS AND ROLE IN HOST MICROECOLOGY TORKEL WADSTRÖM and ÅSA LJUNGH Department of Medical Microbiology, Dermatology and Infection, Lund University, Lund, Sweden SUMMARY Helicobacter pylori is the first named species of the Helicobac- ter/Wolinella family, now including more than 20 species and about 10 candidate species. The organisms are all micro-aerophilic “mucino- philes” with a few exceptions. H. pylori is the prototype for a number of bile-sensitive species colonising the stomach of most mammals, in- cluding dolphins and whales. The low toxicity of the lipopolysaccharide (LPS) and a number of properties unique for these species determine how they may cause life-long infections. H. pylori carries the vacA toxin as well as a set of other virulence traits permitting optimal early coloni- sation of the host, e.g. in childhood. The cagA pathogenicity island (PAI) makes cagA+ strains of H. pylori more virulent than cagA- strains to develop chronic active gastritis, gastric atrophy and pre-cancerous le- sions in the host as well as in mouse and mongolian gerbil models. H. pylori as well as a number of entero-hepatic bile-tolerant species are camouflaged from the innate immune system of the GI epithelial cell surfaces, yet cagA+ H. pylori transcribe NF-κB to the nucleus of these cells and of macrophages and other cells. At least H. pylori evades the host immune system by a number of responses such as molecular mimicry of the H–K adenosine triphosphatase and of gastric cell surface fucosylated antigens. The degree of inflammation is modulated by the IL-1β cytokine polymorphism and probably by a number of other host factors. The co-evolution of H. pylori and man back to the origin of mankind is clearly defined with a sophisticated haemostasis between the H. pylori as a pathogen. Alternative scenarios in the 21st century in several parts of the world with a “clean” Helicobacter-free human stomach are ad- dressed as well as recent reports of a newly discovered gastro-oeso- phageal microflora and the rapid increase in GERD, Barrett´s oesopha- gus, oesophageal cancer and obesity as well as changes in living condi- tions in Western societies. INTRODUCTION Helicobacter pylori lives in the mu- the area of colonisation is invariably in- cus layer overlying the gastric epithe- flamed (chronic superficial gastritis; lium and does not appear to invade tis- Northfield et al., 1994). Most infected sues. However, the mucosa underneath persons do not show clinical manifesta- 1 Table 1: Entero-hepatic bile-tolerant Helicobacter species ————————————————————————————— Species Comment ————————————————————————————— Helicobacter pylori some strains are bile-tolerant Helicobacter pullorum common in chicken Helicobacter bilis common in rodents Helicobacter hepaticus common in rodents Helicobacter cholecystus common in hamster Helicobacter canis common in dogs Helicobacter rappinii certain subtype common in sheep Helicobacter ganmani anaerobic ————————————————————————————— tions of the inflammation. Studies that manii as a second gastric species. This include human volunteers, experimental species and some others are highly fas- animal infections and treatment of pa- tidious and difficult or impossible to tients with antimicrobial agents show culture in vitro under micro-aerophilic that H. pylori plays a critical role in this or anaerobic conditions with H. gan- inflammation and in these diseases. mani as the prototype of the second Much evidence suggest that H. pylori is group (Robertson et al., 2001). All spe- an indigenous microbe of the human cies are highly motile and possess non- stomach and that most, if not all, mam- sheathed or sheathed flagellae enabling malian species harbour related Helico- them to swim in the mucin layer (An- bacter species with a long co-evolution dersen and Wadström, 2001). Suer- of microbe and host (Blaser, 1998; baum and colleagues (Schreiber et al., Richter, 2001). H. pylori probably 2004) recently showed that H. pylori evolved from bile-tolerant enteric Heli- prefers a specific part of the gastric cobacter species colonising rodents and mucin layer, probably regulated by acid other mammals, including primates and secretion, H. pylori urease and ammonia man (Fox et al., 2001; Tables 1 and 2). formation, a metabolite most toxic for The phylogenetic tree of proteobacteria the gastric mucosa. Urease-negative as includes Sulphurospirillum, Arcobacter, well as catalase-negative mutants are un- Campylobacter, Helicobacter and able to colonise and infect the mouse Wolinellae (On, 2001; Figure 1). stomach, suggesting that ammonia pro- More than 20 species of Helicobac- duction and the redox potential are cru- ter are recognised today, with H. heil- cial to initiate the infection. Several ge- Table 2: Evidence that Helicobacter pylori infection of humans is of ancient origin. ——————————————————————————————————————— • Extensive genetic heterogeneity • Acid-secreting stomachs arose early (300 million years ago!) in vertebrates • Helicobacter genus is highly prevalent in the stomach and gut of all vertebrates? • H. pylori-like organisms are widely present in the stomach of primates • High incidence among human populations in Asia and Africa of H. pylori (>80-90%) • H. pylori is adapted to persist for lifetime in the human stomach ——————————————————————————————————————— 2 Figure 1: Representation of the phylogenetic tree of proteobacteria (modified from On, 2001). netic studies of H. pylori isolates from a not a post mortem “by-stander” was single human stomach show that these not addressed properly until Marshall microbes are highly adaptive organisms, and Warren (1984) in 1982 grew the which partly explains that this pathogen first Campylobacter pyloridis (later C. can persist for decades in a single stom- pylori and renamed to Helicobacter py- ach inducing a low grade tissue inflam- lori in 1989). By drinking viable in vitro mation (Blaser and Atherton, 2004). cultured H. pylori cells, Marshall and This adaptation involves mutations and colleagues showed that it induced acute recombination, and many strains may be achlorhydria and dyspepsia, which was classified as hypermutation phenotypes. suppressed or cured by a bismuth-anti- H. pylori is able to maximise diversity biotic therapy. of genetic sequences under strong se- Later, in vitro co-culture studies of lective pressure while maintaining alleles H. pylori and gastric cancer epithelial critical for its lifestyle (Björkholm et al., (AGS) cells showed that strains con- 2004). taining the 35 to 40 kilobase cag patho- Helicobacter-like organisms, resem- genicity island (PAI) flanked by specific bling the syphilis spirochete, were re- 39 basepair direct DNA repeats induced ported by several pathologists in human a higher cytokine response (IL-8), and and animal stomachs already in the pe- promoted an anti-apoptotic pathway riod from1880 to 1890, including beau- aiding persistence of the organism in the tiful studies in dogs by Bizzozeroni in gastric mucosa (Crabtree, 2001). Italy, describing a species today named Another reason for its persistence is H. bizzozeron (On, 2001). However, its the molecular mimicry, in part due to the possible role as a gastric pathogen and low biological activity of its lipopoly- 3 saccharide (LPS)(Moran et al. 2000; vates CD4+ T cells in the stomach. This Blaser and Atherton, 2004). Molecular leads to gastric autoimmunity in geneti- mimicry between H. pylori antigens and cally susceptible individuals via mo- H+,K+-adenosine triphosphatase acti- lecular mimicry (Amedei et al., 2003). H. PYLORI PATHOGENESIS – A MULTIPLE STEP INFECTION TO CHRONIC GASTRITIS AND GASTRIC ATROPHY Early development of mouse models Toll-like receptor (TLR4) and not gas- has clearly given good opportunities to tric TLR4 (Bäckhed et al, 2003). CagA- elucidate the H. pylori pathogenesis, and positive strains induce transcription of to develop alternative prophylactic and NF-κB in the epithelium through rec- treatment schedules to standard proton ognition of Nod1, an innate intracellular pump inhibitor (PPI) and antibiotics pathogen-recognition molecule, recog- (Hamilton-Miller, 2003). Mice given the nising soluble bacterial peptidoglycan vacuolating (vac) toxin orally developed fragments (Kim et al., 2004). How such ulcers. However, strains producing a vac molecules as well as other cell surface, toxin with an S1/m2 mid-region seem to extra-cellular and cell lysis molecules, bind poorly to specific cell lines and in- including nucleic acids, are delivered to duce less tissue damage and cell mem- the gastric mucosa is poorly understood. brane pores (Blaser and Atherton, Further studies are needed to define new 2004). Moreover, the S2 genotype is possible interventions, such as probiotic- associated with a lack of the cag PAI based strategies including anti- and may induce a less severe gastric in- Helicobacter peptides and bacteriocins flammation. Transient oral and gastric (Hamilton-Miller, 2003; Lorca et al., H. pylori colonisation occurs in chil- 2001). dren, as shown in a study from Dhaka, The H. pylori infection down-regu- Bangladesh (Casswall et al., 1999). It is lates the immune response, suppresses likely that H. pylori is a paediatric in- T-cell proliferation and induces selective fection, “achieved” soon after weaning T-cell apoptosis (Shirin and
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