Are tumor-associated carbohydrates the missing link between the gut microbiome and response to immune checkpoint inhibitor treatment in cancer?

References

• Johnson DB, Nebhan CA, Moslehi JJ, Balko JM. Immune-checkpoint inhibitors: long-term implications of toxicity. Nat Rev Clin Oncol. 2022;19(4):254–5. doi:10.1038/s41571-022-00600-w.
   PubMed Web of Science ®Google Scholar
• Gopalakrishnan V, Spencer CN, Nezi L, Reuben A, Andrews MC, Karpinets TV, Prieto PA, Vicente D, Hoffman K, Wei SC, et al. Gut microbiome modulates response to anti-PD-1 immunotherapy in melanoma patients. Science. 2018;359(6371):97–103. doi:10.1126/science.aan4236.
   PubMed Web of Science ®Google Scholar
• Routy B, Le Chatelier E, Derosa L, Duong CPM, Alou MT, Daillère R, Fluckiger A, Messaoudene M, Rauber C, Roberti MP, et al. Gut microbiome influences efficacy of PD-1-based immunotherapy against epithelial tumors. Science. 2018;359(6371):91–97. doi:10.1126/science.aan3706.
   PubMed Web of Science ®Google Scholar
• Vétizou M, Pitt JM, Daillère R, Lepage P, Waldschmitt N, Flament C, Rusakiewicz S, Routy B, Roberti MP, Duong CPM, et al. Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota. Science. 2015;350(6264):1079–1084. doi:10.1126/science.aad1329.
   PubMed Web of Science ®Google Scholar
• Sivan A, Corrales L, Hubert N, Williams JB, Aquino-Michaels K, Earley ZM, Benyamin FW, Lei YM, Jabri B, Alegre M-L, et al. Commensal Bifidobacterium promotes antitumor immunity and facilitates anti-PD-L1 efficacy. Science. 2015;350(6264):1084–1089. doi:10.1126/science.aac4255.
   PubMed Web of Science ®Google Scholar
• Matson V, Fessler J, Bao R, Chongsuwat T, Zha Y, Alegre M-L, Luke JJ, Gajewski TF. The commensal microbiome is associated with anti-PD-1 efficacy in metastatic melanoma patients. Science. 2018;359(6371):104–108. doi:10.1126/science.aao3290.
   PubMed Web of Science ®Google Scholar
• Routy B, Lenehan JG, Miller WH, Jamal R, Messaoudene M, Daisley BA, Hes C, Al KF, Martinez-Gili L, Punčochář M, et al. Fecal microbiota transplantation plus anti-PD-1 immunotherapy in advanced melanoma: a phase I trial. Nat Med. 2023;29(8):2121–2132. doi:10.1038/s41591-023-02453-x.
   PubMed Web of Science ®Google Scholar
• Dizman N, Meza L, Bergerot P, Alcantara M, Dorff T, Lyou Y, Frankel P, Cui Y, Mira V, Llamas M. et al. Nivolumab plus ipilimumab with or without live bacterial supplementation in metastatic renal cell carcinoma: a randomized phase 1 trial. Nat Med. 2022;28(4):704–712. doi:10.1038/s41591-022-01694-6.
   PubMed Web of Science ®Google Scholar
• Davar D, Dzutsev AK, McCulloch JA, Rodrigues RR, Chauvin J-M, Morrison RM, Deblasio RN, Menna C, Ding Q, Pagliano O. et al. Fecal microbiota transplant overcomes resistance to anti-PD-1 therapy in melanoma patients. Science. 2021;371(6529):595–602. doi:10.1126/science.abf3363.
   PubMed Web of Science ®Google Scholar
• Laskowski TJ, Biederstädt A, Rezvani K. Natural killer cells in antitumour adoptive cell immunotherapy. Nat Rev Cancer. 2022;22(10):557–575. doi:10.1038/s41568-022-00491-0.
   PubMed Web of Science ®Google Scholar
• de Vries NL, van de Haar J, Veninga V, Chalabi M, Ijsselsteijn ME, van der Ploeg M, van den Bulk J, Ruano D, van den Berg JG, Haanen JB. et al. γδ T cells are effectors of immunotherapy in cancers with HLA class I defects. Nature. 2023;613(7945):743–750. doi:10.1038/s41586-022-05593-1.
   PubMed Web of Science ®Google Scholar
• Gutiérrez-Melo N, Baumjohann D. T follicular helper cells in cancer. Trends Cancer. 2023;9(4):309–325. doi:10.1016/j.trecan.2022.12.007.
   Web of Science ®Google Scholar
• Fluckiger A, Daillère R, Sassi M, Sixt BS, Liu P, Loos F, Richard C, Rabu C, Alou MT, Goubet A-G. et al. Cross-reactivity between tumor MHC class I-restricted antigens and an enterococcal bacteriophage. Science. 2020;369(6506):936–942. doi:10.1126/science.aax0701.
   PubMed Web of Science ®Google Scholar
• Goubet A-G, Lordello L, Alves Costa Silva C, Peguillet I, Gazzano M, Mbogning-Fonkou MD, Thelemaque C, Lebacle C, Thibault C, Audenet F, et al. Escherichia coli-specific CXCL13-producing TFH are associated with clinical efficacy of neoadjuvant PD-1 blockade against muscle-invasive bladder cancer. Cancer Discov. 2022;12(10):2280–2307. doi:10.1158/2159-8290.CD-22-0201.
   Web of Science ®Google Scholar
• Arnolds KL, Martin CG, Lozupone CA. Blood type and the microbiome- untangling a complex relationship with lessons from pathogens. Curr Opin Microbiol. 2020;56:59–66. doi:10.1016/j.mib.2020.06.008.
   Web of Science ®Google Scholar
• Springer GF, Williamson P, Readler BL. Blood group active gram-negative bacteria and higher plants. Ann NY Acad Sci. 1962;97(1):104–110. doi:10.1111/j.1749-6632.1962.tb34626.x.
   Web of Science ®Google Scholar
• Kleczko EK, Kwak JW, Schenk EL, Nemenoff RA. Targeting the complement pathway as a therapeutic strategy in lung cancer. Front Immunol. 2019;10:954. doi:10.3389/fimmu.2019.00954.
   PubMed Web of Science ®Google Scholar
• Judd WJ, Annesley TM. The acquired-B phenomenon. Transfus Med Rev. 1996;10(2):111–117. doi:10.1016/s0887-7963(96)80087-3.
   Web of Science ®Google Scholar
• Kaur A, Jain A, Marwaha N, Mahajan JK, Sharma RR. Acquired-B phenomenon in a neonate presenting with necrotizing enterocolitis. Transfus Apher Sci. 2019;58(1):30–31. doi:10.1016/j.transci.2018.10.021.
   Web of Science ®Google Scholar
• Yamamoto M, Cid E, Yamamoto F. Molecular genetic basis of the human Forssman glycolipid antigen negativity. Sci Rep. 2012;2(1):975. doi:10.1038/srep00975.
   Google Scholar
• Yamamoto M, Cid E, Yamamoto F. ABO blood group a transferases catalyze the biosynthesis of FORS blood group FORS1 antigen upon deletion of exon 3 or 4. Blood Adv. 2017;1(27):2756–2766. doi:10.1182/bloodadvances.2017009795.
   Web of Science ®Google Scholar
• Yamamoto M, Tarasco MC, Cid E, Kobayashi H, Yamamoto F. ABO blood group a transferase and its codon 69 substitution enzymes synthesize FORS1 antigen of FORS blood group system. Sci Rep. 2019;9(1):9717. doi:10.1038/s41598-019-46029-7.
   Google Scholar
• Yoda Y, Ishibashi T, Makita A. Isolation, characterization, and biosynthesis of Forssman antigen in human lung and lung carcinoma. J Biochem. 1980;88:1887–1890.
   PubMed Web of Science ®Google Scholar
• Li Q, Anver MR, Li Z, Butcher DO, Gildersleeve JC. GalNAcalpha1-3Gal, a new prognostic marker for cervical cancer. Int J Cancer. 2010;126(2):459–468. doi:10.1002/ijc.24716.
   PubMed Web of Science ®Google Scholar
• Moldvay J, Scheid P, Wild P, Nabil K, Siat J, Borrelly J, Marie B, Farré G, Labib T, Pottier G, et al. Predictive survival markers in patients with surgically resected non-small cell lung carcinoma. Clin Cancer Res. 2000;6(3):1125–1134.
   PubMed Web of Science ®Google Scholar
• Campbell CT, Gulley JL, Oyelaran O, Hodge JW, Schlom J, Gildersleeve JC. Humoral response to a viral glycan correlates with survival on PROSTVAC-VF. Proc Natl Acad Sci U S A. 2014;111(17):E1749–1758. doi:10.1073/pnas.1314722111.
   PubMed Web of Science ®Google Scholar
• Kijimoto-Ochiai S, Takahashi W, Makita A. Anti-Forssman antibody in human sera: properties and decreased level in cancer patients. Jpn J Exp Med. 1981;51:149–155.
   PubMedGoogle Scholar
• Kitamura H, Levine P, Cheng PJ, Egeli RA, Liu YP, Good RA, Day NK. Forssman-like antibody levels in sera of patients with lung cancer. Cancer Res. 1979;39:2909–2913.
   Web of Science ®Google Scholar
• Young WW, Hakomori SI, Levine P. Characterization of anti-forssman (anti-fs) antibodies in human sera: their specificity and possible changes in patients with cancer. J Immunol. 1979;123(1):92–96. doi:10.4049/jimmunol.123.1.92.
   Web of Science ®Google Scholar
• Briles EB, Tomasz A. Physiological studies on the pneumococcal Forssman antigen: a choline-containing lipoteichoic acid. J Gen Microbiol. 1975;86(2):267–274. doi:10.1099/00221287-86-2-267.
   Google Scholar
• Briles EB, Tomasz A. Pneumococcal Forssman antigen. A choline-containing lipoteichoic acid. J Biol Chem. 1973;248(18):6394–6397. doi:10.1016/S0021-9258(19)43459-5.
   Web of Science ®Google Scholar
• Horne D, Tomasz A. Pneumococcal Forssman antigen: enrichment in mesosomal membranes and specific binding to the autolytic enzyme of streptococcus pneumoniae. J Bacteriol. 1985;161(1):18–24. doi:10.1128/jb.161.1.18-24.1985.
   Web of Science ®Google Scholar
• Schneewind O, Missiakas D. Lipoteichoic acids, phosphate-containing polymers in the envelope of gram-positive bacteria. J Bacteriol. 2014;196(6):1133–1142. doi:10.1128/JB.01155-13.
   PubMed Web of Science ®Google Scholar
• Seo HS, Cartee RT, Pritchard DG, Nahm MH. A new model of pneumococcal lipoteichoic acid structure resolves biochemical, biosynthetic, and serologic inconsistencies of the current model. J Bacteriol. 2008;190(7):2379–2387. doi:10.1128/JB.01795-07.
   Web of Science ®Google Scholar
• Jesus C, Hesse C, Rocha C, Osório N, Valado A, Caseiro A, Gabriel A, Svensson L, Moslemi A-R, Siba WA, et al. Prevalence of antibodies to a new histo-blood system: the FORS system. Blood Transfus. 2018;16(2):178–183. doi:10.2450/2016.0120-16.
   PubMed Web of Science ®Google Scholar
• Kappler K, Hennet T. Emergence and significance of carbohydrate-specific antibodies. Genes Immun. 2020;21(4):224–239. doi:10.1038/s41435-020-0105-9.
   Web of Science ®Google Scholar
• Galili U, Mandrell RE, Hamadeh RM, Shohet SB, Griffiss JM. Interaction between human natural anti-alpha-galactosyl immunoglobulin G and bacteria of the human flora. Infect Immun. 1988;56(7):1730–1737. doi:10.1128/iai.56.7.1730-1737.1988.
   PubMed Web of Science ®Google Scholar
• Winand RJ, Devigne JW, Meurisse M, Galili U. Specific stimulation of graves’ disease thyrocytes by the natural anti-gal antibody from normal and autologous serum. J Immunol. 1994;153(3):1386–1395. doi:10.4049/jimmunol.153.3.1386.
   Web of Science ®Google Scholar
• Postow MA, Sidlow R, Hellmann MD, Longo DL. Immune-related adverse events associated with immune checkpoint blockade. N Engl J Med. 2018;378(2):158–168. doi:10.1056/NEJMra1703481.
   PubMed Web of Science ®Google Scholar
• Nishat S, Andreana PR. Entirely carbohydrate-based vaccines: an emerging field for specific and selective immune responses. Vaccines (Basel). 2016;4(2):19. doi:10.3390/vaccines4020019.
   Web of Science ®Google Scholar