East-Asian Helicobacter pylori Strains Synthesize Heptan-deficient Lipopolysaccharide

English version

Autoři: Hong Li ^aff001; Michael Marceau ^aff003; Tiandi Yang ^aff004; Tingting Liao ^aff002; Xiaoqiong Tang ^aff001; Renwei Hu ^aff005; Yan Xie ^aff005; Hong Tang ^aff001; Alfred Tay ^aff002; Ying Shi ^aff001; Yalin Shen ^aff001; Tiankuo Yang ^aff001; Xuenan Pi ^aff006; Binit Lamichhane ^aff002; Yong Luo ^aff007; Aleksandra W. Debowski ^aff002; Hans-Olof Nilsson ^aff002; Stuart M. Haslam ^aff004; Barbara Mulloy ^aff004; Anne Dell ^aff004; Keith A. Stubbs ^aff008; Barry J. Marshall ^aff002; Mohammed Benghezal ^aff001
Působiště autorů: West China Marshall Research Center for Infectious Diseases, Center of Infectious Diseases, Division of Infectious Diseases, State Key Laboratory of Biotherapy, West China Hospital, Sichuan University, Chengdu, China ^aff001; Helicobacter pylori Research Laboratory, School of Biomedical Sciences, Marshall Centre for Infectious Disease Research and Training, University of Western Australia, Nedlands, Australia ^aff002; Univ. Lille, CNRS, Inserm, CHU Lille, Institut Pasteur de Lille, U1019—UMR 8204—CIIL—Center for Infection and Immunity of Lille, Lille, France ^aff003; Department of Life Sciences, Imperial College London, South Kensington Campus, London, United Kingdom ^aff004; Department of Gastroenterology, West China Hospital, Sichuan University, Chengdu, China ^aff005; Precision Medicine Key Laboratory of Sichuan Province & Precision Medicine Center, West China Hospital, Sichuan University, Chengdu, China ^aff006; Key Laboratory of Geoscience Spatial Information Technology, Ministry of Land and Resources of the P.R.China, Chengdu University of Technology ^aff007; School of Molecular Sciences, University of Western Australia, Crawley, Australia ^aff008; Ondek Pty Ltd, Rushcutters Bay, New South Wales, Australia ^aff009
Vyšlo v časopise: East-Asian Helicobacter pylori Strains Synthesize Heptan-deficient Lipopolysaccharide. PLoS Genet 15(11): e1008497. doi:10.1371/journal.pgen.1008497
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1008497

Souhrn

The lipopolysaccharide O-antigen structure expressed by the European Helicobacter pylori model strain G27 encompasses a trisaccharide, an intervening glucan-heptan and distal Lewis antigens that promote immune escape. However, several gaps still remain in the corresponding biosynthetic pathway. Here, systematic mutagenesis of glycosyltransferase genes in G27 combined with lipopolysaccharide structural analysis, uncovered HP0102 as the trisaccharide fucosyltransferase, HP1283 as the heptan transferase, and HP1578 as the GlcNAc transferase that initiates the synthesis of Lewis antigens onto the heptan motif. Comparative genomic analysis of G27 lipopolysaccharide biosynthetic genes in strains of different ethnic origin revealed that East-Asian strains lack the HP1283/HP1578 genes but contain an additional copy of HP1105 and JHP0562. Further correlation of different lipopolysaccharide structures with corresponding gene contents led us to propose that the second copy of HP1105 and the JHP0562 may function as the GlcNAc and Gal transferase, respectively, to initiate synthesis of the Lewis antigen onto the Glc-Trio-Core in East-Asian strains lacking the HP1283/HP1578 genes. In view of the high gastric cancer rate in East Asia, the absence of the HP1283/HP1578 genes in East-Asian H. pylori strains warrants future studies addressing the role of the lipopolysaccharide heptan in pathogenesis.

Klíčová slova:

Helicobacter pylori – Comparative genomics – Biosynthesis – Transferases – Antigens – Glucans – Endotoxins – Glycosyltransferases

Zdroje

1. Hooi JKY, Lai WY, Ng WK, Suen MMY, Underwood FE, et al. (2017) Global Prevalence of Helicobacter pylori Infection: Systematic Review and Meta-Analysis. Gastroenterology 153: 420–429. doi: 10.1053/j.gastro.2017.04.022 28456631

2. Malfertheiner P, Megraud F, O'Morain CA, Gisbert JP, Kuipers EJ, et al. (2017) Management of Helicobacter pylori infection-the Maastricht V/Florence Consensus Report. Gut 66: 6–30. doi: 10.1136/gutjnl-2016-312288 27707777

3. Sugano K, Tack J, Kuipers EJ, Graham DY, El-Omar EM, et al. (2015) Kyoto global consensus report on Helicobacter pylori gastritis. Gut 64: 1353–1367. doi: 10.1136/gutjnl-2015-309252 26187502

4. IARC (2014) Helicobacter pylori Eradication as a Strategy for Preventing Gastric Cancer. 8 ed.

5. de Sablet T, Piazuelo MB, Shaffer CL, Schneider BG, Asim M, et al. (2011) Phylogeographic origin of Helicobacter pylori is a determinant of gastric cancer risk. Gut 60: 1189–1195. doi: 10.1136/gut.2010.234468 21357593

6. Li H, Yang T, Liao T, Debowski AW, Nilsson HO, et al. (2017) The redefinition of Helicobacter pylori lipopolysaccharide O-antigen and core-oligosaccharide domains. PLoS Pathog 13: e1006280. doi: 10.1371/journal.ppat.1006280 28306723

7. Cullen TW, Giles DK, Wolf LN, Ecobichon C, Boneca IG, et al. (2011) Helicobacter pylori versus the host: remodeling of the bacterial outer membrane is required for survival in the gastric mucosa. PLoS Pathog 7: e1002454. doi: 10.1371/journal.ppat.1002454 22216004

8. Monteiro MA (2001) Helicobacter pylori: a wolf in sheep's clothing: the glycotype families of Helicobacter pylori lipopolysaccharides expressing histo-blood groups: structure, biosynthesis, and role in pathogenesis. Adv Carbohydr Chem Biochem 57: 99–158. doi: 10.1016/s0065-2318(01)57016-x 11836945

9. Whitfield C, Trent MS (2014) Biosynthesis and export of bacterial lipopolysaccharides. Annu Rev Biochem 83: 99–128. doi: 10.1146/annurev-biochem-060713-035600 24580642

10. Li H, Liao T, Debowski AW, Tang H, Nilsson HO, et al. (2016) Lipopolysaccharide Structure and Biosynthesis in Helicobacter pylori. Helicobacter 21: 445–461. doi: 10.1111/hel.12301 26934862

11. Bergman MP, Engering A, Smits HH, van Vliet SJ, van Bodegraven AA, et al. (2004) Helicobacter pylori modulates the T helper cell 1/T helper cell 2 balance through phase-variable interaction between lipopolysaccharide and DC-SIGN. Journal of Experimental Medicine 200: 979–990. doi: 10.1084/jem.20041061 15492123

12. Zhou P, She Y, Dong N, Li P, He H, et al. (2018) Alpha-kinase 1 is a cytosolic innate immune receptor for bacterial ADP-heptose. Nature 561: 122–126. doi: 10.1038/s41586-018-0433-3 30111836

13. Zimmermann S, Pfannkuch L, Al-Zeer MA, Bartfeld S, Koch M, et al. (2017) ALPK1- and TIFA-Dependent Innate Immune Response Triggered by the Helicobacter pylori Type IV Secretion System. Cell Rep 20: 2384–2395. doi: 10.1016/j.celrep.2017.08.039 28877472

14. Gall A, Gaudet RG, Gray-Owen SD, Salama NR (2017) TIFA Signaling in Gastric Epithelial Cells Initiates the cag Type 4 Secretion System-Dependent Innate Immune Response to Helicobacter pylori Infection. Mbio 8.

15. Stein SC, Faber E, Bats SH, Murillo T, Speidel Y, et al. (2017) Helicobacter pylori modulates host cell responses by CagT4SS-dependent translocation of an intermediate metabolite of LPS inner core heptose biosynthesis. Plos Pathogens 13.

16. Pachathundikandi K, Backert S (2018) Heptose 1,7-Bisphosphate Directed TIFA Oligomerization: A Novel PAMP-Recognizing Signaling Platform in the Control of Bacterial Infections. Gastroenterology 154: 778–783. doi: 10.1053/j.gastro.2018.01.009 29337150

17. Raetz CR, Whitfield C (2002) Lipopolysaccharide endotoxins. Annu Rev Biochem 71: 635–700. doi: 10.1146/annurev.biochem.71.110601.135414 12045108

18. Li H, Tang H, Debowski AW, Stubbs KA, Marshall BJ, et al. (2018) Lipopolysaccharide Structural Differences between Western and Asian Helicobacter pylori Strains. Toxins (Basel) 10.

19. Monteiro MA, Zheng P, Ho B, Yokota S, Amano K, et al. (2000) Expression of histo-blood group antigens by lipopolysaccharides of Helicobacter pylori strains from Asian hosts: the propensity to express type 1 blood-group antigens. Glycobiology 10: 701–713. doi: 10.1093/glycob/10.7.701 10910974

20. Baltrus DA, Amieva MR, Covacci A, Lowe TM, Merrell DS, et al. (2009) The complete genome sequence of Helicobacter pylori strain G27. J Bacteriol 191: 447–448. doi: 10.1128/JB.01416-08 18952803

21. Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B (2014) The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res 42: D490–495. doi: 10.1093/nar/gkt1178 24270786

22. Altman E, Chandan V, Harrison BA, Vinogradov E (2017) Structural and immunological characterization of a glycoconjugate based on the delipidated lipopolysaccharide from a nontypeable Helicobacter pylori strain PJ1 containing an extended d-glycero-d-manno-heptan. Carbohydr Res 456: 19–23. doi: 10.1016/j.carres.2017.10.024 29247909

23. Moran AP, Shiberu B, Ferris JA, Knirel YA, Senchenkova SN, et al. (2004) Role of Helicobacter pylori rfaJ genes (HP0159 and HP1416) in lipopolysaccharide synthesis. FEMS Microbiol Lett 241: 57–65. doi: 10.1016/j.femsle.2004.10.004 15556710

24. Hiratsuka K, Logan SM, Conlan JW, Chandan V, Aubry A, et al. (2005) Identification of a D-glycero-D-manno-heptosyltransferase gene from Helicobacter pylori. J Bacteriol 187: 5156–5165. doi: 10.1128/JB.187.15.5156-5165.2005 16030209

25. Altman E, Chandan V, Li J, Vinogradov E (2011) Lipopolysaccharide structures of Helicobacter pylori wild-type strain 26695 and 26695 HP0826::Kan mutant devoid of the O-chain polysaccharide component. Carbohydr Res 346: 2437–2444. doi: 10.1016/j.carres.2011.06.036 21903201

26. Logan SM, Altman E, Mykytczuk O, Brisson JR, Chandan V, et al. (2005) Novel biosynthetic functions of lipopolysaccharide rfaJ homologs from Helicobacter pylori. Glycobiology 15: 721–733. doi: 10.1093/glycob/cwi057 15814825

27. Pohl MA, Romero-Gallo J, Guruge JL, Tse DB, Gordon JI, et al. (2009) Host-dependent Lewis (Le) antigen expression in Helicobacter pylori cells recovered from Leb-transgenic mice. J Exp Med 206: 3061–3072. doi: 10.1084/jem.20090683 20008521

28. Pohl MA, Kienesberger S, Blaser MJ (2012) Novel functions for glycosyltransferases Jhp0562 and GalT in Lewis antigen synthesis and variation in Helicobacter pylori. Infect Immun 80: 1593–1605. doi: 10.1128/IAI.00032-12 22290141

29. Chua EG, Wise MJ, Khosravi Y, Seow SW, Amoyo AA, et al. (2017) Quantum changes in Helicobacter pylori gene expression accompany host-adaptation. DNA Res 24: 37–49. doi: 10.1093/dnares/dsw046 27803027

30. Logan SM, Conlan JW, Monteiro MA, Wakarchuk WW, Altman E (2000) Functional genomics of Helicobacter pylori: identification of a beta-1,4 galactosyltransferase and generation of mutants with altered lipopolysaccharide. Mol Microbiol 35: 1156–1167. doi: 10.1046/j.1365-2958.2000.01784.x 10712696

31. Appelmelk BJ, Martin SL, Monteiro MA, Clayton CA, McColm AA, et al. (1999) Phase variation in Helicobacter pylori lipopolysaccharide due to changes in the lengths of poly(C) tracts in alpha 3-fucosyltransferase genes (vol 67, pg 5361, 1999). Infection and Immunity 67: 6715–6715.

32. Wang G, Rasko DA, Sherburne R, Taylor DE (1999) Molecular genetic basis for the variable expression of Lewis Y antigen in Helicobacter pylori: analysis of the alpha (1,2) fucosyltransferase gene. Mol Microbiol 31: 1265–1274. doi: 10.1046/j.1365-2958.1999.01268.x 10096092

33. Langdon R, Craig JE, Goldrick M, Houldsworth R, High NJ (2005) Analysis of the role of HP0208, a phase-variable open reading frame, and its homologues HP1416 and HP0159 in the biosynthesis of Helicobacter pylori lipopolysaccharide. J Med Microbiol 54: 697–706. doi: 10.1099/jmm.0.45842-0 16014421

34. Wunder C, Churin Y, Winau F, Warnecke D, Vieth M, et al. (2006) Cholesterol glucosylation promotes immune evasion by Helicobacter pylori. Nat Med 12: 1030–1038. doi: 10.1038/nm1480 16951684

35. Sycuro LK, Pincus Z, Gutierrez KD, Biboy J, Stern CA, et al. (2010) Peptidoglycan crosslinking relaxation promotes Helicobacter pylori's helical shape and stomach colonization. Cell 141: 822–833. doi: 10.1016/j.cell.2010.03.046 20510929

36. Hug I, Couturier MR, Rooker MM, Taylor DE, Stein M, et al. (2010) Helicobacter pylori Lipopolysaccharide Is Synthesized via a Novel Pathway with an Evolutionary Connection to Protein N-Glycosylation. PLoS Pathogens 6: e1000819. doi: 10.1371/journal.ppat.1000819 20333251

37. Debowski AW, Gauntlett JC, Li H, Liao T, Sehnal M, et al. (2012) Xer-cise in Helicobacter pylori: one-step transformation for the construction of markerless gene deletions. Helicobacter 17: 435–443. doi: 10.1111/j.1523-5378.2012.00969.x 23066820

38. Hazell GLMHLTMSL (2001) Helicobacter pylori: physiology and genetics Helicobacter pylori: physiology and genetics Washington, DC: ASM Press

39. van Leeuwen SS, Schoemaker RJ, Gerwig GJ, van Leusen-van Kan EJ, Dijkhuizen L, et al. (2014) Rapid milk group classification by 1H NMR analysis of Le and H epitopes in human milk oligosaccharide donor samples. Glycobiology 24: 728–739. doi: 10.1093/glycob/cwu036 24789815

40. Altman E, Chandan V, Li J, Vinogradov E (2011) A reinvestigation of the lipopolysaccharide structure of Helicobacter pylori strain Sydney (SS1). FEBS J 278: 3484–3493. doi: 10.1111/j.1742-4658.2011.08270.x 21790998

41. Moodley Y, Linz B, Bond RP, Nieuwoudt M, Soodyall H, et al. (2012) Age of the association between Helicobacter pylori and man. PLoS Pathog 8: e1002693. doi: 10.1371/journal.ppat.1002693 22589724

42. Monteiro MA, St Michael F, Rasko DA, Taylor DE, Conlan JW, et al. (2001) Helicobacter pylori from asymptomatic hosts expressing heptoglycan but lacking Lewis O-chains: Lewis blood-group O-chains may play a role in Helicobacter pylori induced pathology. Biochem Cell Biol 79: 449–459. 11527214

43. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, et al. (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19: 455–477. doi: 10.1089/cmb.2012.0021 22506599

44. Seemann T (2014) Prokka: rapid prokaryotic genome annotation. Bioinformatics 30: 2068–2069. doi: 10.1093/bioinformatics/btu153 24642063

45. Debowski AW, Carnoy C, Verbrugghe P, Nilsson HO, Gauntlett JC, et al. (2012) Xer recombinase and genome integrity in Helicobacter pylori, a pathogen without topoisomerase IV. PLoS One 7: e33310. doi: 10.1371/journal.pone.0033310 22511919

46. Heuermann D, Haas R (1998) A stable shuttle vector system for efficient genetic complementation of Helicobacter pylori strains by transformation and conjugation. Mol Gen Genet 257: 519–528. doi: 10.1007/s004380050677 9563837

47. Darveau RP, Hancock RE (1983) Procedure for isolation of bacterial lipopolysaccharides from both smooth and rough Pseudomonas aeruginosa and Salmonella typhimurium strains. J Bacteriol 155: 831–838. 6409884

48. Acquotti D, Sonnino S (2000) Use of nuclear magnetic resonance spectroscopy in evaluation of ganglioside structure, conformation, and dynamics. Methods Enzymol 312: 247–272. doi: 10.1016/s0076-6879(00)12914-3 11070877

49. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155: 945–959. 10835412

50. Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources 4: 359–361.