Motility and Chemotaxis Mediate the Preferential Colonization of Gastric Injury Sites by

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H. pylori is a disease-causing bacterium that commonly infects the human stomach in both developed and underdeveloped countries. Infected individuals can develop digestive diseases, including stomach inflammation, peptic ulcer, and cancer. There has been only limited investigation into the events when H. pylori first interacts with stomach tissue. Using anesthetized mice in which we have induced microscopic damage to the stomach surface, we find that H. pylori is able to rapidly detect and navigate towards this damage site. Within minutes, bacterial accumulation slows repair of the damage. This is the earliest event of H. pylori pathogenesis that has been reported in vivo. We further define that this pathology is due to the bacterial accumulation at damage sites and that this also occurs in a model of larger stomach damage (ulceration). The broader implications of our work are that even sub-clinical insults to the stomach that occur in daily life (damage from grinding of food, ingestion of alcohol, taking an aspirin) can potentially attract H. pylori and not only slow repair of any existing damage, but maybe also provide an initiation site that can start the pathogenic sequence of stomach disease caused by H. pylori.

Vyšlo v časopise: Motility and Chemotaxis Mediate the Preferential Colonization of Gastric Injury Sites by. PLoS Pathog 10(7): e32767. doi:10.1371/journal.ppat.1004275
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004275

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Zdroje

1. MarshallBJ, WarrenJR (1984) Unidentified curved bacilli in the stomach of patients with gastritis and peptic ulceration. Lancet 1 : 1311–1315.

2. OttemannKM, LowenthalAC (2002) Helicobacter pylori uses motility for initial colonization and to attain robust infection. Infect Immun 70 : 1984–1990.

3. TerryK, WilliamsSM, ConnollyL, OttemannKM (2005) Chemotaxis plays multiple roles during Helicobacter pylori animal infection. Infect Immun 73 : 803–811.

4. LertsethtakarnP, OttemannKM, HendrixsonDR (2011) Motility and chemotaxis in Campylobacter and Helicobacter. Annu Rev Microbiol 65 : 389–410.

5. MizoteT, YoshiyamaH, NakazawaT (1997) Urease-independent chemotactic responses of Helicobacter pylori to urea, urease inhibitors, and sodium bicarbonate. Infect Immun 65 : 1519–1521.

6. CerdaO, RivasA, ToledoH (2003) Helicobacter pylori strain ATCC700392 encodes a methyl-accepting chemotaxis receptor protein (MCP) for arginine and sodium bicarbonate. FEMS Microbiol Lett 224 : 175–181.

7. SchreiberS, KonradtM, GrollC, ScheidP, HanauerG, et al. (2004) The spatial orientation of Helicobacter pylori in the gastric mucus. Proc Natl Acad Sci U S A 101 : 5024–5029.

8. CroxenMA, SissonG, MelanoR, HoffmanPS (2006) The Helicobacter pylori chemotaxis receptor TlpB (HP0103) is required for pH taxis and for colonization of the gastric mucosa. J Bacteriol 188 : 2656–2665.

9. SchweinitzerT, MizoteT, IshikawaN, DudnikA, InatsuS, et al. (2008) Functional characterization and mutagenesis of the proposed behavioral sensor TlpD of Helicobacter pylori. J Bacteriol 190 : 3244–3255.

10. GarnerA, FlemstromG, AllenA, HeylingsJR, McQueenS (1984) Gastric mucosal protective mechanisms: roles of epithelial bicarbonate and mucus secretions. Scand J Gastroenterol Suppl 101 : 79–86.

11. StarodubOT, DemitrackES, BaumgartnerHK, MontroseMH (2008) Disruption of the Cox-1 gene slows repair of microscopic lesions in the mouse gastric epithelium. Am J Physiol Cell Physiol 294: C223–232.

12. XueL, AiharaE, PodolskyDK, WangTC, MontroseMH (2010) In vivo action of trefoil factor 2 (TFF2) to speed gastric repair is independent of cyclooxygenase. Gut 59 : 1184–1191.

13. NishioH, TerashimaS, NakashimaM, AiharaE, TakeuchiK (2007) Involvement of prostaglandin E receptor EP3 subtype and prostacyclin IP receptor in decreased acid response in damaged stomach. J Physiol Pharmacol 58 : 407–421.

14. RaderBA, WredenC, HicksKG, SweeneyEG, OttemannKM, et al. (2011) Helicobacter pylori perceives the quorum-sensing molecule AI-2 as a chemorepellent via the chemoreceptor TlpB. Microbiology 157 : 2445–2455.

15. Goers SweeneyE, HendersonJN, GoersJ, WredenC, HicksKG, et al. (2012) Structure and proposed mechanism for the pH-sensing Helicobacter pylori chemoreceptor TlpB. Structure 20 : 1177–1188.

16. BeierD, SpohnG, RappuoliR, ScarlatoV (1997) Identification and characterization of an operon of Helicobacter pylori that is involved in motility and stress adaptation. J Bacteriol 179 : 4676–4683.

17. LowenthalAC, HillM, SycuroLK, MehmoodK, SalamaNR, et al. (2009) Functional analysis of the Helicobacter pylori flagellar switch proteins. J Bacteriol 191 : 7147–7156.

18. FoynesS, DorrellN, WardSJ, StablerRA, McColmAA, et al. (2000) Helicobacter pylori possesses two CheY response regulators and a histidine kinase sensor, CheA, which are essential for chemotaxis and colonization of the gastric mucosa. Infect Immun 68 : 2016–2023.

19. LowenthalAC, SimonC, FairAS, MehmoodK, TerryK, et al. (2009) A fixed-time diffusion analysis method determines that the three cheV genes of Helicobacter pylori differentially affect motility. Microbiology 155 : 1181–1191.

20. SandersL, AndermannTM, OttemannKM (2013) A supplemented soft agar chemotaxis assay demonstrates the Helicobacter pylori chemotactic response to zinc and nickel. Microbiology 159 : 46–57.

21. HowittMR, LeeJY, LertsethtakarnP, VogelmannR, JoubertLM, et al. (2011) ChePep controls Helicobacter pylori Infection of the gastric glands and chemotaxis in the Epsilonproteobacteria. MBio 2: e00098–11.

22. BehrensW, SchweinitzerT, BalJ, DorschM, BleichA, et al. (2013) Role of energy sensor TlpD of Helicobacter pylori in gerbil colonization and genome analyses after adaptation in the gerbil. Infect Immun 81 : 3534–3551.

23. TerryK, GoAC, OttemannKM (2006) Proteomic mapping of a suppressor of non-chemotactic cheW mutants reveals that Helicobacter pylori contains a new chemotaxis protein. Mol Microbiol 61 : 871–882.

24. OkabeS, AmagaseK (2005) An overview of acetic acid ulcer models–the history and state of the art of peptic ulcer research. Biol Pharm Bull 28 : 1321–1341.

25. SmithSI, OyedejiKS, ArigbabuAO, CantetF, MegraudF, et al. (2004) Comparison of three PCR methods for detection of Helicobacter pylori DNA and detection of cagA gene in gastric biopsy specimens. World J Gastroenterol 10 : 1958–1960.

26. LertpiriyapongK, WharyMT, MuthupalaniS, LofgrenJL, GamazonER, et al. (2014) Gastric colonisation with a restricted commensal microbiota replicates the promotion of neoplastic lesions by diverse intestinal microbiota in the Helicobacter pylori INS-GAS mouse model of gastric carcinogenesis. Gut 63 : 54–63.

27. RoligAS, ShanksJ, CarterJE, OttemannKM (2012) Helicobacter pylori requires TlpD-driven chemotaxis to proliferate in the antrum. Infect Immun 80 : 3713–3720.

28. AiharaE, HentzCL, KormanAM, PerryNP, PrasadV, et al. (2013) In vivo epithelial wound repair requires mobilization of endogenous intracellular and extracellular calcium. J Biol Chem 288 : 33585–33597.

29. RoligAS, CarterJE, OttemannKM (2011) Bacterial chemotaxis modulates host cell apoptosis to establish a T-helper cell, type 17 (Th17)-dominant immune response in Helicobacter pylori infection. Proc Natl Acad Sci U S A 108 : 19749–19754.

30. KetoY, EbataM, TomitaK, OkabeS (2002) Influence of Helicobacter pylori infection on healing and relapse of acetic acid ulcers in Mongolian gerbils. Dig Dis Sci 47 : 837–849.

31. KonturekPC, BrzozowskiT, KonturekSJ, StachuraJ, KarczewskaE, et al. (1999) Mouse model of Helicobacter pylori infection: studies of gastric function and ulcer healing. Aliment Pharmacol Ther 13 : 333–346.

32. WatanabeT, HiguchiK, HamaguchiM, TanigawaT, WadaR, et al. (2002) Rebamipide prevents delay of acetic acid-induced gastric ulcer healing caused by Helicobacter pylori infection in Mongolian gerbils. Dig Dis Sci 47 : 1582–1589.

33. BlomH (1985) The structure of normal and regenerating rat oxyntic mucosa. Scand J Gastroenterol Suppl 110 : 73–80.

34. XiaoC, FengR, EngevikAC, MartinJR, TritschlerJA, et al. (2013) Sonic Hedgehog contributes to gastric mucosal restitution after injury. Lab Invest 93 : 96–111.

35. ClyneM, DillonP, DalyS, O'KennedyR, MayFE, et al. (2004) Helicobacter pylori interacts with the human single-domain trefoil protein TFF1. Proc Natl Acad Sci U S A 101 : 7409–7414.

36. SchreiberS, StubenM, JosenhansC, ScheidP, SuerbaumS (1999) In vivo distribution of Helicobacter felis in the gastric mucus of the mouse: experimental method and results. Infect Immun 67 : 5151–5156.

37. Azevedo-VethackeM, GartenD, GrollC, SchreiberS (2009) Specific therapeutic schemes of omeprazole affect the orientation of Helicobacter pylori. Antimicrob Agents Chemother 53 : 3511–3514.

38. PentecostM, OttoG, TheriotJA, AmievaMR (2006) Listeria monocytogenes invades the epithelial junctions at sites of cell extrusion. PLoS Pathog 2: e3.

39. TanS, TompkinsLS, AmievaMR (2009) Helicobacter pylori usurps cell polarity to turn the cell surface into a replicative niche. PLoS Pathog 5: e1000407.

40. ButlerSM, CamilliA (2005) Going against the grain: chemotaxis and infection in Vibrio cholerae. Nat Rev Microbiol 3 : 611–620.

41. EngevikAC, FengR, YangL, ZavrosY (2013) The acid-secreting parietal cell as an endocrine source of Sonic Hedgehog during gastric repair. Endocrinology 154 : 4627–4639.

42. DemitrackES, AiharaE, KennyS, VarroA, MontroseMH (2012) Inhibitors of acid secretion can benefit gastric wound repair independent of luminal pH effects on the site of damage. Gut 61 : 804–811.

43. EngevikMA, AiharaE, MontroseMH, ShullGE, HassettDJ, et al. (2013) Loss of NHE3 alters gut microbiota composition and influences Bacteroides thetaiotaomicron growth. Am J Physiol Gastrointest Liver Physiol 305: G697–711.

44. ColladoMC, DonatE, Ribes-KoninckxC, CalabuigM, SanzY (2009) Specific duodenal and faecal bacterial groups associated with paediatric coeliac disease. J Clin Pathol 62 : 264–269.