Antigenicity evaluation of synthetic α-(1,3)-linked D, D-heptoglycan of Helicobacter pylori serotype O6 lipopolysaccharide

References

• Kusters, J. G.; van Vliet, A. H.; Kuipers, E. J. Pathogenesis of Helicobacter pylori infection. Clin. Microbiol. Rev. 2006, 19(3), 449–490. DOI: 10.1128/cmr.00054-05.
   PubMed Web of Science ®Google Scholar
• Eslick, G. D.; Lim, L. L.; Byles, J. E.; Xia, H. H.; Talley, N. J. Association of Helicobacter pylori infection with gastric carcinoma: a meta-analysis. Am. J. Gastroenterol. 1999, 94(9), 2373–2379. DOI: 10.1016/S0002-9270(99)00416-5.
   PubMed Web of Science ®Google Scholar
• Group, H. a C C. Gastric cancer and Helicobacter pylori: a combined analysis of 12 case control studies nested within prospective cohorts. Gut 2001, 49(3), 347–353. DOI: 10.1136/gut.49.3.347.
   PubMed Web of Science ®Google Scholar
• Huang, J. Q.; Zheng, G. F.; Sumanac, K.; Irvine, E. J.; Hunt, R. H. Meta-analysis of the relationship between cagA seropositivity and gastric cancer. Gastroenterology 2003, 125(6), 1636–1644. DOI: 10.1053/j.gastro.2003.08.033.
   PubMed Web of Science ®Google Scholar
• Kamangar, F.; Dawsey, S. M.; Blaser, M. J.; Perez-Perez, G. I.; Pietinen, P.; Newschaffer, C. J.; Abnet, C. C.; Albanes, D.; Virtamo, J.; Taylor, P. R.; et al. Opposing risks of gastric cardia and noncardia gastric adenocarcinomas associated with Helicobacter pylori seropositivity. J. Natl. Cancer Inst. 2006, 98(20), 1445–1452. DOI: 10.1093/jnci/djj393.
   PubMedGoogle Scholar
• Bessède, E.; Dubus, P.; Mégraud, F.; Varon, C. Helicobacter pylori infection and stem cells at the origin of gastric cancer. Oncogene 2015, 34(20), 2547–2555. DOI: 10.1038/onc.2014.187.
   PubMed Web of Science ®Google Scholar
• Godavarthy, P. K.; Puli, C. From antibiotic resistance to antibiotic renaissance: a new era in Helicobacter pylori treatment. Cureus 2023, 15(3), e36041. DOI: 10.7759/cureus.36041.
   PubMed Web of Science ®Google Scholar
• De Francesco, V.; Giorgio, F.; Hassan, C.; et al. Worldwide H. pylori antibiotic resistance: a systematic review. J. Gastrointest Liver 2010, 19(4), 409–414. pubmed.ncbi.nlm.nih.gov/21188333/.
   Google Scholar
• Ayala, G.; Escobedo-Hinojosa, W. I.; de la Cruz-Herrera, C. F.; Romero, I. Exploring alternative treatments for Helicobacter pylori infection. World J. Gastroenterol. 2014, 20(6), 1450–1469. DOI: 10.3748/wjg.v20.i6.1450.
   PubMed Web of Science ®Google Scholar
• Selgrad, M.; Malfertheiner, P. New strategies for Helicobacter pylori eradication. Curr. Opin. Pharmacol. 2008, 8(5), 593–597. DOI: 10.1016/j.coph.2008.04.010.
   PubMed Web of Science ®Google Scholar
• Yunle, K.; Tong, W.; Jiyang, L.; Guojun, W. Advances in Helicobacter pylori vaccine research: From candidate antigens to adjuvants-A review. Helicobacter 2024, 29(1), e13034. DOI: 10.1111/hel.13034.
   PubMedGoogle Scholar
• Michetti, P.; Kreiss, C.; Kotloff, K. L.; Porta, N.; Blanco, J. L.; Bachmann, D.; Herranz, M.; Saldinger, P. F.; Corthésy-Theulaz, I.; Losonsky, G.; et al. Oral immunization with urease and Escherichia coli heat-labile enterotoxin is safe and immunogenic in Helicobacter pylori-infected adults. Gastroenterology 1999, 116(4), 804–812. DOI: 10.1016/s0016-5085(99)70063-6.
   PubMed Web of Science ®Google Scholar
• Banerjee, S.; Medina-Fatimi, A.; Nichols, R.; Tendler, D.; Michetti, M.; Simon, J.; Kelly, C. P.; Monath, T. P.; Michetti, P. Safety and efficacy of low dose Escherichia coli enterotoxin adjuvant for urease based oral immunisation against Helicobacter pylori in healthy volunteers. Gut 2002, 51(5), 634–640. DOI: 10.1136/gut.51.5.634.
   PubMed Web of Science ®Google Scholar
• Kotloff, K. L.; Sztein, M. B.; Wasserman, S. S.; Losonsky, G. A.; DiLorenzo, S. C.; Walker, R. I. Safety and immunogenicity of oral inactivated whole-cell Helicobacter pylori vaccine with adjuvant among volunteers with or without subclinical infection. Infect. Immun. 2001, 69(6), 3581–3590. DOI: 10.1128/iai.69.6.3581-3590.2001.
   PubMed Web of Science ®Google Scholar
• Aebischer, T.; Bumann, D.; Epple, H. J.; Metzger, W.; Schneider, T.; Cherepnev, G.; Walduck, A. K.; Kunkel, D.; Moos, V.; Loddenkemper, C.; et al. Correlation of T cell response and bacterial clearance in human volunteers challenged with Helicobacter pylori revealed by randomised controlled vaccination with Ty21a-based Salmonella vaccines. Gut 2008, 57(8), 1065–1072. DOI: 10.1136/gut.2007.145839.
   PubMed Web of Science ®Google Scholar
• Zeng, M.; Mao, X.-H.; Li, J.-X.; Tong, W.-D.; Wang, B.; Zhang, Y.-J.; Guo, G.; Zhao, Z.-J.; Li, L.; Wu, D.-L.; et al. Efficacy, safety, and immunogenicity of an oral recombinant Helicobacter pylori vaccine in children in China: a randomised, double-blind, placebo-controlled, phase 3 trial. Lancet 2015, 386(10002), 1457–1464. DOI: 10.1016/S0140-6736(15)60310-5.
   PubMed Web of Science ®Google Scholar
• Malfertheiner, P.; Selgrad, M.; Wex, T.; Romi, B.; Borgogni, E.; Spensieri, F.; Zedda, L.; Ruggiero, P.; Pancotto, L.; Censini, S.; et al. Efficacy, immunogenicity, and safety of a parenteral vaccine against Helicobacter pylori in healthy volunteers challenged with a Cag-positive strain: a randomised, placebo-controlled phase 1/2 study. Lancet. Gastroenterol. Hepatol. 2018, 3(10), 698–707. DOI: 10.1016/S2468-1253(18)30125-0.
   PubMed Web of Science ®Google Scholar
• Nell, S.; Estibariz, I.; Krebes, J.; Bunk, B.; Graham, D. Y.; Overmann, J.; Song, Y.; Spröer, C.; Yang, I.; Wex, T.; et al. Genome and methylome variation in Helicobacter pylori with a cag pathogenicity island during early stages of human infection. Gastroenterology 2018, 154(3), 612–623.e7. e617. DOI: 10.1053/j.gastro.2017.10.014.
   PubMed Web of Science ®Google Scholar
• Zhang, Y.; Li, X.; Shan, B.; Zhang, H.; Zhao, L. Perspectives from recent advances of Helicobacter pylori vaccines research. Helicobacter 2022, 27(6), e12926. DOI: 10.1111/hel.12926.
   PubMed Web of Science ®Google Scholar
• Friedrich, V.; Gerhard, M. Vaccination against Helicobacter pylori-An approach for cancer prevention? Mol. Mol. Aspects Med. 2023, 92, 101183. DOI: 10.1016/j.mam.2023.101183.
   PubMed Web of Science ®Google Scholar
• Adamo, R. Glycoconjugate vaccines: classic and novel approaches. Glycoconj. J. 2021, 38(4), 397–398. DOI: 10.1007/s10719-021-09997-5.
   PubMed Web of Science ®Google Scholar
• Del Bino, L.; Østerlid, K. E.; Wu, D.-Y.; Nonne, F.; Romano, M. R.; Codée, J.; Adamo, R. Synthetic glycans to improve current glycoconjugate vaccines and fight antimicrobial resistance. Chem. Rev. 2022, 122(20), 15672–15716. DOI: 10.1021/acs.chemrev.2c00021.
   PubMed Web of Science ®Google Scholar
• Avci, F. Y.; Kasper, D. L. How bacterial carbohydrates influence the adaptive immune system. Annu. Rev. Immunol. 2010, 28(1), 107–130. DOI: 10.1146/annurev-immunol-030409-101159.
   PubMedGoogle Scholar
• Avci, F. Y.; Li, X.; Tsuji, M.; Kasper, D. L. A mechanism for glycoconjugate vaccine activation of the adaptive immune system and its implications for vaccine design. Nat. Med. 2011, 17(12), 1602–1609. DOI: 10.1038/nm.2535.
   PubMed Web of Science ®Google Scholar
• Berti, F.; Adamo, R. Recent mechanistic insights on glycoconjugate vaccines and future perspectives. ACS Chem. Biol. 2013, 8(8), 1653–1663. DOI: 10.1021/cb400423g.
   PubMed Web of Science ®Google Scholar
• Grebowska, A.; Moran, A. P.; Matusiak, A.; et al. Anti-phagocytic activity of Helicobacter Pylori lipopolysaccharide (LPS) - Possible modulation of the innate immune response to these bacteria. Pol. J. Microbiol 2008, 57(3), 185–192. DOI: pubmed.ncbi.nlm.nih.gov/19004238.
   PubMed Web of Science ®Google Scholar
• Lukácová, M.; Barák, I.; Kazár, J. Role of structural variations of polysaccharide antigens in the pathogenicity of gram-negative bacteria. Clin. Microbiol. Infect. 2008, 14(3), 200–206. DOI: 10.1111/j.1469-0691.2007.01876.x.
   PubMed Web of Science ®Google Scholar
• Altman, E.; Chandan, V.; Harrison, B. A.; Veloso-Pita, R.; Li, J.; KuoLee, R.; Chen, W.; Vérez-Bencomo, V., Regional Helicobacter pylori Study Group Design and immunological properties of Helicobacter pylori glycoconjugates based on a truncated lipopolysaccharide lacking Lewis antigen and comprising an α-1,6-glucan chain. Vaccine 2012, 30(50), 7332–7341. DOI: 10.1016/j.vaccine.2012.04.035.
   PubMed Web of Science ®Google Scholar
• Altman, E.; Chandan, V.; Harrison, B. A.; Vinogradov, E. 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. 2018, 456, 19–23. DOI: 10.1016/j.carres.2017.10.024.
   PubMed Web of Science ®Google Scholar
• Esmaeilli, D.; Mobarez, A. M.; Salmanian, A. H. Bioactivity and immunological evaluation of LPS from different serotypes of Helicobacter pylori. Iran. J. Biotechnol 2013, 5(2), 142–146. DOI: pubmed.ncbi.nlm.nih.gov/23825732/.
   Google Scholar
• Monteiro, M. A.; Britton, S.; Applebee, L. A.; Baqar, S. Synthesis and immunogenicity of a Helicobacter pylori lipopolysaccharide-based conjugate. Vaccine 2011, 29(17), 3098–3102. DOI: 10.1016/j.vaccine.2011.02.063.
   PubMed Web of Science ®Google Scholar
• Aspinall, G. O.; Monteiro, M. A.; Shaver, R. T.; Kurjanczyk, L. A.; Penner, J. L. Lipopolysaccharides of Helicobacter pylori serogroups O:3 and O:6 - Structures of a class of lipopolysaccharides with reference to the location of oligomeric units of D-glycero-alpha-D-manno-heptose residues. Eur. J. Biochem. 1997, 248(2), 592–601. DOI: 10.1111/j.1432-1033.1997.00592.x.
   PubMedGoogle Scholar
• Ferreira, J.; Silva, L. M.; Monteiro, M.; et al. Helicobacter pylori cell-surface glycans structural features: role in gastric colonization, pathogenesis, and carbohydrate-based vaccines. Carbohydr. Chem 2011, 37, 160–193. DOI: 10.1039/9781849732765-00160.
   Google Scholar
• Monteiro, M. A.; St Michael, F.; Rasko, D. A.; Taylor, D. E.; Conlan, J. W.; Chan, K. H.; Logan, S. M.; Appelmelk, B. J.; Perry, M. B. 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. 2001, 79(4), 449–459. DOI: 10.1139/bcb-79-4-449.
   PubMedGoogle Scholar
• Monteiro, M. A. 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. 2001, 57, 99–158. DOI: 10.1016/s0065-2318(01)57016-x.
   PubMed Web of Science ®Google Scholar
• Tian, G.; Hu, J.; Qin, C.; Li, L.; Zou, X.; Cai, J.; Seeberger, P. H.; Yin, J. Chemical synthesis and immunological evaluation of Helicobacter pylori serotype O6 tridecasaccharide O-antigen containing a dd-Heptoglycan. Angew. Chem. Int. Ed. Engl. 2020, 59(32), 13362–13370. DOI: 10.1002/anie.202004267.
   PubMed Web of Science ®Google Scholar
• Wang, J.; Zhang, Y.; Zhu, Y.; Liu, J.; Chen, Y.; Cao, X.; Yang, Y. Total synthesis and immunological evaluation of the Tri-D-glycero-D-manno-heptose Antigen of the lipopolysaccharide as a vaccine candidate against Helicobacter pylori. Org. Lett. 2020, 22(22), 8780–8785. DOI: 10.1021/acs.orglett.0c03105.
   PubMed Web of Science ®Google Scholar
• Zou, X.; Qin, C.; Pereira, C. L.; Tian, G.; Hu, J.; Seeberger, P. H.; Yin, J. Synergistic glycosylation as key to the chemical synthesis of an outer core octasaccharide of Helicobacter pylori. Chemistry 2018, 24(12), 2868–2872. DOI: 10.1002/chem.201800049.
   PubMed Web of Science ®Google Scholar
• Zou, X.; Hu, J.; Zhao, M.; Qin, C.; Zhu, Y.; Tian, G.; Cai, J.; Seeberger, P. H.; Yin, J. Chemical synthesis of the highly sterically hindered core undecasaccharide of Helicobacter pylori lipopolysaccharide for antigenicity evaluation with human serum. J. Am. Chem. Soc. 2022, 144(32), 14535–14547. DOI: 10.1021/jacs.2c03068.
   PubMed Web of Science ®Google Scholar
• Lian, G. Y.; Zhang, X. H.; Yu, B. Thioglycosides in carbohydrate research. Carbohydr. Res. 2015, 403, 13–22. DOI: 10.1016/j.carres.2014.06.009.
   PubMed Web of Science ®Google Scholar
• Aspinall, G. O.; Monteiro, M. A.; Pang, H.; Walsh, E. J.; Moran, A. P. Lipopolysaccharide of the Helicobacter pylori type strain NCTC 11637 (ATCC 43504): structure of the O antigen chain and core oligosaccharide regions. Biochemistry 1996, 35(7), 2489–2497. DOI: 10.1021/bi951852s.
   PubMed Web of Science ®Google Scholar
• Li, Y.; Powell, D. A.; Shaffer, S. A.; Rasko, D. A.; Pelletier, M. R.; Leszyk, J. D.; Scott, A. J.; Masoudi, A.; Goodlett, D. R.; Wang, X.; et al. LPS remodeling is an evolved survival strategy for bacteria. Proc. Natl. Acad. Sci. U S A. U S A 2012, 109(22), 8716–8721. DOI: 10.1073/pnas.1202908109.
   PubMed Web of Science ®Google Scholar