Use of a MAIT Activating Ligand, 5-OP-RU, as a Mucosal Adjuvant in a Murine Model of Vibrio cholerae O1 Vaccination

Main Article Content

Owen Jensen
Shubhanshi Trivedi
Kelin Li
Jeffrey Aubé
J. Scott Hale
Edward T. Ryan
Daniel T. Leung

Abstract

Background: Mucosal-associated invariant T (MAIT) cells are innate-like T cells enriched in the mucosa with capacity for B-cell help. We hypothesize that targeting MAIT cells, using a MAIT-activating ligand as an adjuvant, could improve mucosal vaccine responses to bacterial pathogens such as Vibrio cholerae.


Methods: We utilized murine models of V. cholerae vaccination to test the adjuvant potential of the MAIT-activating ligand, 5-(2-oxopropylideneamino)-6-D-ribitylaminouracil (5-OP-RU). We measured V. cholerae-specific antibody and antibody-secreting cell responses and used flow cytometry to examine MAIT-cell and B-cell phenotype, in blood, bronchoalveolar lavage fluid (BALF), and mucosal tissues, following intranasal vaccination with live V. cholerae O1 or a V. cholerae O1 polysaccharide conjugate vaccine. 


Results: We report significant expansion of MAIT cells in the lungs (P < 0.001) and BALF (P < 0.001) of 5-OP-RU treated mice, and higher mucosal (BALF, P = 0.045) but not systemic (serum, P = 0.21) V. cholerae O-specific-polysaccharide IgG responses in our conjugate vaccine model when adjuvanted with low-dose 5-OP-RU. In contrast, despite significant MAIT cell expansion, no significant differences in V. cholerae-specific humoral responses were found in our live V. cholerae vaccination model.


Conclusions: Using a murine model, we demonstrate the potential, as well as the limitations, of targeting MAIT cells to improve antibody responses to mucosal cholera vaccines. Our study highlights the need for future research optimizing MAIT-cell targeting for improving mucosal vaccines.

Downloads

Download data is not yet available.

Article Details

How to Cite
1.
Jensen O, Trivedi S, Li K, Aubé J, Hale JS, Ryan ET, Leung DT. Use of a MAIT Activating Ligand, 5-OP-RU, as a Mucosal Adjuvant in a Murine Model of Vibrio cholerae O1 Vaccination. PAI [Internet]. 2022 Aug. 24 [cited 2022 Sep. 27];7(1):122-44. Available from: https://www.paijournal.com/index.php/paijournal/article/view/525
Section
Articles

References

1. Tilloy F, Treiner E, Park SH, Garcia C, Lemonnier F, de la Salle H, Bendelac A, Bonneville M, Lantz O. An invariant T cell receptor alpha chain defines a novel TAP-independent major histocompatibility complex class Ib-restricted alpha/beta T cell subpopulation in mammals. J Exp Med. 1999;189(12):1907-21. doi: 10.1084/jem.189.12.1907. PubMed PMID: 10377186; PMCID: PMC2192962.

2. Reantragoon R, Corbett AJ, Sakala IG, Gherardin NA, Furness JB, Chen Z, Eckle SB, Uldrich AP, Birkinshaw RW, Patel O, Kostenko L, Meehan B, Kedzierska K, Liu L, Fairlie DP, Hansen TH, Godfrey DI, Rossjohn J, McCluskey J, Kjer-Nielsen L. Antigen-loaded MR1 tetramers define T cell receptor heterogeneity in mucosal-associated invariant T cells. J Exp Med. 2013;210(11):2305-20. doi: 10.1084/jem.20130958. PubMed PMID: 24101382; PMCID: PMC3804952.

3. Lepore M, Kalinichenko A, Colone A, Paleja B, Singhal A, Tschumi A, Lee B, Poidinger M, Zolezzi F, Quagliata L, Sander P, Newell E, Bertoletti A, Terracciano L, De Libero G, Mori L. Parallel T-cell cloning and deep sequencing of human MAIT cells reveal stable oligoclonal TCRbeta repertoire. Nat Commun. 2014;5:3866. doi: 10.1038/ncomms4866. PubMed PMID: 24832684.

4. Treiner E, Duban L, Bahram S, Radosavljevic M, Wanner V, Tilloy F, Affaticati P, Gilfillan S, Lantz O. Selection of evolutionarily conserved mucosal-associated invariant T cells by MR1. Nature. 2003;422(6928):164-9. doi: 10.1038/nature01433. PubMed PMID: 12634786.

5. Kjer-Nielsen L, Patel O, Corbett AJ, Le Nours J, Meehan B, Liu L, Bhati M, Chen Z, Kostenko L, Reantragoon R, Williamson NA, Purcell AW, Dudek NL, McConville MJ, O’Hair RA, Khairallah GN, Godfrey DI, Fairlie DP, Rossjohn J, McCluskey J. MR1 presents microbial vitamin B metabolites to MAIT cells. Nature. 2012;491(7426):717-23. doi: 10.1038/nature11605. PubMed PMID: 23051753.

6. Patel O, Kjer-Nielsen L, Le Nours J, Eckle SB, Birkinshaw R, Beddoe T, Corbett AJ, Liu L, Miles JJ, Meehan B, Reantragoon R, Sandoval-Romero ML, Sullivan LC, Brooks AG, Chen Z, Fairlie DP, McCluskey J, Rossjohn J. Recognition of vitamin B metabolites by mucosal-associated invariant T cells. Nat Commun. 2013;4:2142. doi: 10.1038/ncomms3142. PubMed PMID: 23846752.

7. Dusseaux M, Martin E, Serriari N, Peguillet I, Premel V, Louis D, Milder M, Le Bourhis L, Soudais C, Treiner E, Lantz O. Human MAIT cells are xenobiotic-resistant, tissue-targeted, CD161hi IL-17-secreting T cells. Blood. 2011;117(4):1250-9. doi: 10.1182/blood-2010-08-303339. PubMed PMID: 21084709.

8. Rahimpour A, Koay HF, Enders A, Clanchy R, Eckle SB, Meehan B, Chen Z, Whittle B, Liu L, Fairlie DP, Goodnow CC, McCluskey J, Rossjohn J, Uldrich AP, Pellicci DG, Godfrey DI. Identification of phenotypically and functionally heterogeneous mouse mucosal-associated invariant T cells using MR1 tetramers. J Exp Med. 2015;212(7):1095-108. doi: 10.1084/jem.20142110. PubMed PMID: 26101265; PMCID: PMC4493408.

9. Lamichhane R, Schneider M, de la Harpe SM, Harrop TWR, Hannaway RF, Dearden PK, Kirman JR, Tyndall JDA, Vernall AJ, Ussher JE. TCR- or Cytokine-Activated CD8(+) Mucosal-Associated Invariant T Cells Are Rapid Polyfunctional Effectors That Can Coordinate Immune Responses. Cell Rep. 2019;28(12):3061-76 e5. doi: 10.1016/j.celrep.2019.08.054. PubMed PMID: 31533031.

10. Leung DT, Bhuiyan TR, Nishat NS, Hoq MR, Aktar A, Rahman MA, Uddin T, Khan AI, Chowdhury F, Charles RC, Harris JB, Calderwood SB, Qadri F, Ryan ET. Circulating mucosal associated invariant T cells are activated in Vibrio cholerae O1 infection and associated with lipopolysaccharide antibody responses. PLoS Negl Trop Dis. 2014;8(8):e3076. doi: 10.1371/journal.pntd.0003076. PubMed PMID: 25144724; PMCID: PMC4140671.

11. Le Bourhis L, Dusseaux M, Bohineust A, Bessoles S, Martin E, Premel V, Core M, Sleurs D, Serriari NE, Treiner E, Hivroz C, Sansonetti P, Gougeon ML, Soudais C, Lantz O. MAIT cells detect and efficiently lyse bacterially-infected epithelial cells. PLoS Pathog. 2013;9(10):e1003681. doi: 10.1371/journal.ppat.1003681. PubMed PMID: 24130485; PMCID: PMC3795036.

12. Bennett MS, Trivedi S, Iyer AS, Hale JS, Leung DT. Human mucosal-associated invariant T (MAIT) cells possess capacity for B cell help. J Leukoc Biol. 2017;102(5):1261-9. doi: 10.1189/jlb.4A0317-116R. PubMed PMID: 28807929; PMCID: PMC5636046.

13. Murayama G, Chiba A, Suzuki H, Nomura A, Mizuno T, Kuga T, Nakamura S, Amano H, Hirose S, Yamaji K, Suzuki Y, Tamura N, Miyake S. A Critical Role for Mucosal-Associated Invariant T Cells as Regulators and Therapeutic Targets in Systemic Lupus Erythematosus. Front Immunol. 2019;10:2681. doi: 10.3389/fimmu.2019.02681. PubMed PMID: 31849932; PMCID: PMC6895065.

14. Rahman MA, Ko EJ, Bhuyan F, Enyindah-Asonye G, Hunegnaw R, Helmold Hait S, Hogge CJ, Venzon DJ, Hoang T, Robert-Guroff M. Mucosal-associated invariant T (MAIT) cells provide B-cell help in vaccinated and subsequently SIV-infected Rhesus Macaques. Sci Rep. 2020;10(1):10060. doi: 10.1038/s41598-020-66964-0. PubMed PMID: 32572140; PMCID: PMC7308357.

15. Jiang J, Cao Z, Qu J, Liu H, Han H, Cheng X. PD-1-expressing MAIT cells from patients with tuberculosis exhibit elevated production of CXCL13. Scand J Immunol. 2020;91(4):e12858. doi: 10.1111/sji.12858. PubMed PMID: 31833092.

16. Provine NM, Amini A, Garner LC, Spencer AJ, Dold C, Hutchings C, Silva Reyes L, FitzPatrick MEB, Chinnakannan S, Oguti B, Raymond M, Ulaszewska M, Troise F, Sharpe H, Morgan SB, Hinks TSC, Lambe T, Capone S, Folgori A, Barnes E, Rollier CS, Pollard AJ, Klenerman P. MAIT cell activation augments adenovirus vector vaccine immunogenicity. Science. 2021;371(6528):521-6. doi: 10.1126/science.aax8819. PubMed PMID: 33510029; PMCID: PMC7610941.

17. Jensen O, Trivedi S, Meier JD, Fairfax KC, Hale JS, Leung DT. A subset of follicular helper-like MAIT cells can provide B cell help and support antibody production in the mucosa. Sci Immunol. 2022;7(67):eabe8931. doi: 10.1126/sciimmunol.abe8931. PubMed PMID: 35030034; PMCID: PMC9001248.

18. Boulouis C, Kammann T, Cuapio A, Parrot T, Gao Y, Mouchtaridi E, Wullimann D, Lange J, Chen P, Akber M, Rivera Ballesteros O, Muvva JR, group Cs, Smith CIE, Vesterbacka J, Kieri O, Nowak P, Bergman P, Buggert M, Ljunggren HG, Aleman S, Sandberg JK. MAIT cell compartment characteristics are associated with the immune response magnitude to the BNT162b2 mRNA anti-SARS-CoV-2 vaccine. Mol Med. 2022;28(1):54. doi: 10.1186/s10020-022-00484-7. PubMed PMID: 35562666; PMCID: PMC9100314.

19. Ali M, Nelson AR, Lopez AL, Sack DA. Updated global burden of cholera in endemic countries. PLoS Negl Trop Dis. 2015;9(6):e0003832. doi: 10.1371/journal.pntd.0003832. PubMed PMID: 26043000; PMCID: PMC4455997.

20. World Health O. Cholera vaccine: WHO position paper, August 2017 - Recommendations. Vaccine. 2018;36(24):3418-20. doi: 10.1016/j.vaccine.2017.09.–34. PubMed PMID: 29555219.

21. Kauffman RC, Bhuiyan TR, Nakajima R, Mayo-Smith LM, Rashu R, Hoq MR, Chowdhury F, Khan AI, Rahman A, Bhaumik SK, Harris L, O’Neal JT, Trost JF, Alam NH, Jasinskas A, Dotsey E, Kelly M, Charles RC, Xu P, Kovac P, Calderwood SB, Ryan ET, Felgner PL, Qadri F, Wrammert J, Harris JB. Single-Cell Analysis of the Plasmablast Response to Vibrio cholerae Demonstrates Expansion of Cross-Reactive Memory B Cells. mBio. 2016;7(6). doi: 10.1128/mBio.02021-16. PubMed PMID: 27999163; PMCID: PMC5181778.

22. Bi Q, Ferreras E, Pezzoli L, Legros D, Ivers LC, Date K, Qadri F, Digilio L, Sack DA, Ali M, Lessler J, Luquero FJ, Azman AS, Cavailler P, Date K, Sreenivasan N, Matzger H, Luquero F, Grais R, Wiesner L, Ko M, Rouzier V, Peak C, Qadri F, Landegger J, Lynch J, Azman A, Sack D, Henkens M, Ciglenecki I, Ivers L, Diggle E, Weiss M, Hinman A, Maina K, Mirza I, Gimeno G, Levine M. Protection against cholera from killed whole-cell oral cholera vaccines: a systematic review and meta-analysis. The Lancet Infectious Diseases. 2017;17(10):1080-8. doi: 10.1016/s1473-3099(17)30359-6.

23. Harris JB, LaRocque RC, Chowdhury F, Khan AI, Logvinenko T, Faruque AS, Ryan ET, Qadri F, Calderwood SB. Susceptibility to Vibrio cholerae infection in a cohort of household contacts of patients with cholera in Bangladesh. PLoS Negl Trop Dis. 2008;2(4):e221. doi: 10.1371/journal.pntd.0000221. PubMed PMID: 18398491; PMCID: PMC2271133.

24. Patel SM, Rahman MA, Mohasin M, Riyadh MA, Leung DT, Alam MM, Chowdhury F, Khan AI, Weil AA, Aktar A, Nazim M, LaRocque RC, Ryan ET, Calderwood SB, Qadri F, Harris JB. Memory B cell responses to Vibrio cholerae O1 lipopolysaccharide are associated with protection against infection from household contacts of patients with cholera in Bangladesh. Clin Vaccine Immunol. 2012;19(6):842-8. doi: 10.1128/CVI.00037-12. PubMed PMID: 22518009; PMCID: PMC3370438.

25. Leung DT, Uddin T, Xu P, Aktar A, Johnson RA, Rahman MA, Alam MM, Bufano MK, Eckhoff G, Wu-Freeman Y, Yu Y, Sultana T, Khanam F, Saha A, Chowdhury F, Khan AI, Charles RC, Larocque RC, Harris JB, Calderwood SB, Kovac P, Qadri F, Ryan ET. Immune responses to the O-specific polysaccharide antigen in children who received a killed oral cholera vaccine compared to responses following natural cholera infection in Bangladesh. Clin Vaccine Immunol. 2013;20(6):780-8. doi: 10.1128/CVI.00035-13. PubMed PMID: 23515016; PMCID: PMC3675980.

26. Cadoz M. Potential and limitations of polysaccharide vaccines in infancy. Vaccine. 1998;16(14-15):1391-5. doi: 10.1016/s0264-410x(98)00097-8.

27. Lavelle EC, Ward RW. Mucosal vaccines - fortifying the frontiers. Nat Rev Immunol. 2022;22(4):236-50. doi: 10.1038/s41577-021-00583-2. PubMed PMID: 34312520; PMCID: PMC8312369.

28. Li YQ, Yan C, Luo R, Liu Z. iNKT cell agonists as vaccine adjuvants to combat infectious diseases. Carbohydr Res. 2022;513:108527. doi: 10.1016/j.carres.2022.108527. PubMed PMID: 35240551.

29. Davitt CJH, Longet S, Albutti A, Aversa V, Nordqvist S, Hackett B, McEntee CP, Rosa M, Coulter IS, Lebens M, Tobias J, Holmgren J, Lavelle EC. Alpha-galactosylceramide enhances mucosal immunity to oral whole-cell cholera vaccines. Mucosal Immunol. 2019;12(4):1055-64. doi: 10.1038/s41385-019-0159-z. PubMed PMID: 30953000; PMCID: PMC7746523.

30. Wingender G, Kronenberg M. Role of NKT cells in the digestive system. IV. The role of canonical natural killer T cells in mucosal immunity and inflammation. Am J Physiol Gastrointest Liver Physiol. 2008;294(1):G1-8. doi: 10.1152/ajpgi.00437.2007. PubMed PMID: 17947447.

31. Saez de Guinoa J, Jimeno R, Gaya M, Kipling D, Garzon MJ, Dunn-Walters D, Ubeda C, Barral P. CD1d-mediated lipid presentation by CD11c(+) cells regulates intestinal homeostasis. EMBO J. 2018;37(5). doi: 10.15252/embj.201797537. PubMed PMID: 29378774; PMCID: PMC5830915.

32. Zeissig S, Kaser A, Dougan SK, Nieuwenhuis EE, Blumberg RS. Role of NKT cells in the digestive system. III. Role of NKT cells in intestinal immunity. Am J Physiol Gastrointest Liver Physiol. 2007;293(6):G1101-5. doi: 10.1152/ajpgi.00342.2007. PubMed PMID: 17717040.

33. Martin E, Treiner E, Duban L, Guerri L, Laude H, Toly C, Premel V, Devys A, Moura IC, Tilloy F, Cherif S, Vera G, Latour S, Soudais C, Lantz O. Stepwise development of MAIT cells in mouse and human. PLoS Biol. 2009;7(3):e54. doi: 10.1371/journal.pbio.1000054. PubMed PMID: 19278296; PMCID: PMC2653554 co-owns the filled patent for the 3C10 antibody. EM has received salary through this funding.

34. Tang XZ, Jo J, Tan AT, Sandalova E, Chia A, Tan KC, Lee KH, Gehring AJ, De Libero G, Bertoletti A. IL-7 licenses activation of human liver intrasinusoidal mucosal-associated invariant T cells. J Immunol. 2013;190(7):3142-52. doi: 10.4049/jimmunol.1203218. PubMed PMID: 23447689.

35. Jeffery HC, van Wilgenburg B, Kurioka A, Parekh K, Stirling K, Roberts S, Dutton EE, Hunter S, Geh D, Braitch MK, Rajanayagam J, Iqbal T, Pinkney T, Brown R, Withers DR, Adams DH, Klenerman P, Oo YH. Biliary epithelium and liver B cells exposed to bacteria activate intrahepatic MAIT cells through MR1. J Hepatol. 2016;64(5):1118-27. doi: 10.1016/j.jhep.2015.12.017. PubMed PMID: 26743076; PMCID: PMC4822535.

36. Tominaga K, Yamagiwa S, Setsu T, Kimura N, Honda H, Kamimura H, Honda Y, Takamura M, Yokoyama J, Suzuki K, Wakai T, Terai S. Possible involvement of mucosal-associated invariant T cells in the progression of inflammatory bowel diseases. Biomed Res. 2017;38(2):111-21. doi: 10.2220/biomedres.38.111. PubMed PMID: 28442662.

37. Hama I, Tominaga K, Yamagiwa S, Setsu T, Kimura N, Kamimura H, Wakai T, Terai S. Different distribution of mucosal-associated invariant T cells within the human cecum and colon. Cent Eur J Immunol. 2019;44(1):75-83. doi: 10.5114/ceji.2019.84020. PubMed PMID: 31114440; PMCID: PMC6526592.

38. Corbett AJ, Eckle SB, Birkinshaw RW, Liu L, Patel O, Mahony J, Chen Z, Reantragoon R, Meehan B, Cao H, Williamson NA, Strugnell RA, Van Sinderen D, Mak JY, Fairlie DP, Kjer-Nielsen L, Rossjohn J, McCluskey J. T-cell activation by transitory neo-antigens derived from distinct microbial pathways. Nature. 2014;509(7500):361-5. doi: 10.1038/nature13160. PubMed PMID: 24695216.

39. Chen Z, Wang H, D’Souza C, Sun S, Kostenko L, Eckle SB, Meehan BS, Jackson DC, Strugnell RA, Cao H, Wang N, Fairlie DP, Liu L, Godfrey DI, Rossjohn J, McCluskey J, Corbett AJ. Mucosal-associated invariant T-cell activation and accumulation after in vivo infection depends on microbial riboflavin synthesis and co-stimulatory signals. Mucosal Immunol. 2017;10(1):58-68. doi: 10.1038/mi.2016.39. PubMed PMID: 27143301.

40. Wang H, D’Souza C, Lim XY, Kostenko L, Pediongco TJ, Eckle SBG, Meehan BS, Shi M, Wang N, Li S, Liu L, Mak JYW, Fairlie DP, Iwakura Y, Gunnersen JM, Stent AW, Godfrey DI, Rossjohn J, Westall GP, Kjer-Nielsen L, Strugnell RA, McCluskey J, Corbett AJ, Hinks TSC, Chen Z. MAIT cells protect against pulmonary Legionella longbeachae infection. Nat Commun. 2018;9(1):3350. doi: 10.1038/s41467-018-05202-8. PubMed PMID: 30135490; PMCID: PMC6105587.

41. Sakai S, Kauffman KD, Oh S, Nelson CE, Barry CE, 3rd, Barber DL. MAIT cell-directed therapy of Mycobacterium tuberculosis infection. Mucosal Immunol. 2021;14(1):199-208. doi: 10.1038/s41385-020-0332-4. PubMed PMID: 32811991; PMCID: PMC7790750.

42. Vorkas CK, Levy O, Skular M, Li K, Aube J, Glickman MS. Efficient 5-OP-RU-Induced Enrichment of Mucosa-Associated Invariant T Cells in the Murine Lung Does Not Enhance Control of Aerosol Mycobacterium tuberculosis Infection. Infect Immun. 2020;89(1). doi: 10.1128/IAI.00524-20. PubMed PMID: 33077620; PMCID: PMC7927919.

43. Vorkas CK, Krishna C, Li K, Aube J, Fitzgerald DW, Mazutis L, Leslie CS, Glickman MS. Single-Cell Transcriptional Profiling Reveals Signatures of Helper, Effector, and Regulatory MAIT Cells during Homeostasis and Activation. J Immunol. 2022;208(5):1042-56. doi: 10.4049/jimmunol.2100522. PubMed PMID: 35149530; PMCID: PMC9012082.

44. Yan J, Allen S, McDonald E, Das I, Mak JYW, Liu L, Fairlie DP, Meehan BS, Chen Z, Corbett AJ, Varelias A, Smyth MJ, Teng MWL. MAIT Cells Promote Tumor Initiation, Growth, and Metastases via Tumor MR1. Cancer Discov. 2020;10(1):124-41. doi: 10.1158/2159-8290.CD-19-0569. PubMed PMID: 31826876.

45. Sakai S, Lora NE, Kauffman KD, Dorosky DE, Oh S, Namasivayam S, Gomez F, Fleegle JD, Tuberculosis Imaging P, Arlehamn CSL, Sette A, Sher A, Freeman GJ, Via LE, Barry Iii CE, Barber DL. Functional inactivation of pulmonary MAIT cells following 5-OP-RU treatment of non-human primates. Mucosal Immunol. 2021;14(5):1055-66. doi: 10.1038/s41385-021-00425-3. PubMed PMID: 34158594; PMCID: PMC8217205.

46. Li K, Vorkas CK, Chaudhry A, Bell DL, Willis RA, Rudensky A, Altman JD, Glickman MS, Aube J. Synthesis, stabilization, and characterization of the MR1 ligand precursor 5-amino-6-D-ribitylaminouracil (5-A-RU). PLoS One. 2018;13(2):e0191837. doi: 10.1371/journal.pone.0191837. PubMed PMID: 29401462; PMCID: PMC5798775.

47. Nygren E, Holmgren J, Attridge SR. Murine antibody responses following systemic or mucosal immunization with viable or inactivated Vibrio cholerae. Vaccine. 2008;26(52):6784-90. doi: 10.1016/j.vaccine.2008.10.011. PubMed PMID: 18951939.

48. Pankhurst TE, Buick KH, Lange JL, Marshall AJ, Button KR, Palmer OR, Farrand KJ, Stewart IFN, Bird T, Mason NC, Compton BJ, Comoletti D, Salio M, Cerundolo V, Painter GF, Hermans IF, Connor LM. MAIT cells activate dendritic cells to promote T follicular helper cell differentiation and humoral immunity. bioRxiv. 2022:1-37. doi: 10.1101/2022.03.31.486638.

49. Alam MM, Bufano MK, Xu P, Kalsy A, Yu Y, Freeman YW, Sultana T, Rashu MR, Desai I, Eckhoff G, Leung DT, Charles RC, LaRocque RC, Harris JB, Clements JD, Calderwood SB, Qadri F, Vann WF, Kovac P, Ryan ET. Evaluation in mice of a conjugate vaccine for cholera made from Vibrio cholerae O1 (Ogawa) O-specific polysaccharide. PLoS Negl Trop Dis. 2014;8(2):e2683. doi: 10.1371/journal.pntd.0002683. PubMed PMID: 24516685; PMCID: PMC3916310.

50. Aktar A, Rahman MA, Afrin S, Akter A, Uddin T, Yasmin T, Sami MIN, Dash P, Jahan SR, Chowdhury F, Khan AI, LaRocque RC, Charles RC, Bhuiyan TR, Mandlik A, Kelly M, Kovac P, Xu P, Calderwood SB, Harris JB, Qadri F, Ryan ET. Plasma and memory B cell responses targeting O-specific polysaccharide (OSP) are associated with protection against Vibrio cholerae O1 infection among household contacts of cholera patients in Bangladesh. PLoS Negl Trop Dis. 2018;12(4):e0006399. doi: 10.1371/journal.pntd.0006399. PubMed PMID: 29684006; PMCID: PMC5912711.

51. Islam K, Hossain M, Kelly M, Mayo Smith LM, Charles RC, Bhuiyan TR, Kovac P, Xu P, LaRocque RC, Calderwood SB, Simon JK, Chen WH, Haney D, Lock M, Lyon CE, Kirkpatrick BD, Cohen M, Levine MM, Gurwith M, Harris JB, Qadri F, Ryan ET. Anti-O-specific polysaccharide (OSP) immune responses following vaccination with oral cholera vaccine CVD 103-HgR correlate with protection against cholera after infection with wild-type Vibrio cholerae O1 El Tor Inaba in North American volunteers. PLoS Negl Trop Dis. 2018;12(4):e0006376. doi: 10.1371/journal.pntd.0006376. PubMed PMID: 29624592; PMCID: PMC5906022.

52. Petley EV, Koay HF, Henderson MA, Sek K, Todd KL, Keam SP, Lai J, House IG, Li J, Zethoven M, Chen AXY, Oliver AJ, Michie J, Freeman AJ, Giuffrida L, Chan JD, Pizzolla A, Mak JYW, McCulloch TR, Souza-Fonseca-Guimaraes F, Kearney CJ, Millen R, Ramsay RG, Huntington ND, McCluskey J, Oliaro J, Fairlie DP, Neeson PJ, Godfrey DI, Beavis PA, Darcy PK. MAIT cells regulate NK cell-mediated tumor immunity. Nat Commun. 2021;12(1):4746. doi: 10.1038/s41467-021-25009-4. PubMed PMID: 34362900; PMCID: PMC8346465.

53. Crowther MD, Dolton G, Legut M, Caillaud ME, Lloyd A, Attaf M, Galloway SAE, Rius C, Farrell CP, Szomolay B, Ager A, Parker AL, Fuller A, Donia M, McCluskey J, Rossjohn J, Svane IM, Phillips JD, Sewell AK. Genome-wide CRISPR-Cas9 screening reveals ubiquitous T cell cancer targeting via the monomorphic MHC class I-related protein MR1. Nat Immunol. 2020;21(2):178-85. doi: 10.1038/s41590-019-0578-8. PubMed PMID: 31959982; PMCID: PMC6983325.

54. Yu H, Yang A, Derrick S, Mak JYW, Liu L, Fairlie DP, Cowley S. Artificially induced MAIT cells inhibit M. bovis BCG but not M. tuberculosis during in vivo pulmonary infection. Sci Rep. 2020;10(1):13579. doi: 10.1038/s41598-020-70615-9. PubMed PMID: 32788608; PMCID: PMC7423888.

55. Qadri F, Ali M, Lynch J, Chowdhury F, Khan AI, Wierzba TF, Excler J-L, Saha A, Islam MT, Begum YA, Bhuiyan TR, Khanam F, Chowdhury MI, Khan IA, Kabir A, Riaz BK, Akter A, Khan A, Asaduzzaman M, Kim DR, Siddik AU, Saha NC, Cravioto A, Singh AP, Clemens JD. Efficacy of a single-dose regimen of inactivated whole-cell oral cholera vaccine: results from 2 years of follow-up of a randomised trial. The Lancet Infectious Diseases. 2018;18(6):666-74. doi: 10.1016/s1473-3099(18)30108-7.

56. Leung DT, Rahman MA, Mohasin M, Patel SM, Aktar A, Khanam F, Uddin T, Riyadh MA, Saha A, Alam MM, Chowdhury F, Khan AI, Charles R, LaRocque R, Harris JB, Calderwood SB, Qadri F, Ryan ET. Memory B cell and other immune responses in children receiving two doses of an oral killed cholera vaccine compared to responses following natural cholera infection in Bangladesh. Clin Vaccine Immunol. 2012;19(5):690-8. doi: 10.1128/CVI.05615-11. PubMed PMID: 22441386; PMCID: PMC3346319.

57. Charles RC, Kelly M, Tam JM, Akter A, Hossain M, Islam K, Biswas R, Kamruzzaman M, Chowdhury F, Khan AI, Leung DT, Weil A, LaRocque RC, Bhuiyan TR, Rahman A, Mayo-Smith LM, Becker RL, Vyas JM, Faherty CS, Nickerson KP, Giffen S, Ritter AS, Waldor MK, Xu P, Kovac P, Calderwood SB, Kauffman RC, Wrammert J, Qadri F, Harris JB, Ryan ET. Humans Surviving Cholera Develop Antibodies against Vibrio cholerae O-Specific Polysaccharide That Inhibit Pathogen Motility. mBio. 2020;11(6). doi: 10.1128/mBio.02847-20. PubMed PMID: 33203761; PMCID: PMC7683404.

58. Salerno-Goncalves R, Rezwan T, Sztein MB. B cells modulate mucosal associated invariant T cell immune responses. Front Immunol. 2014;4:511. doi: 10.3389/fimmu.2013.00511. PubMed PMID: 24432025; PMCID: PMC3882667.

59. Konforte D, Simard N, Paige CJ. IL-21: an executor of B cell fate. J Immunol. 2009;182(4):1781-7. doi: 10.4049/jimmunol.0803009. PubMed PMID: 19201828.

60. Salio M, Gasser O, Gonzalez-Lopez C, Martens A, Veerapen N, Gileadi U, Verter JG, Napolitani G, Anderson R, Painter G, Besra GS, Hermans IF, Cerundolo V. Activation of Human Mucosal-Associated Invariant T Cells Induces CD40L-Dependent Maturation of Monocyte-Derived and Primary Dendritic Cells. J Immunol. 2017;199(8):2631-8. doi: 10.4049/jimmunol.1700615. PubMed PMID: 28877992; PMCID: PMC5632842.

61. Meierovics AI, Cowley SC. MAIT cells promote inflammatory monocyte differentiation into dendritic cells during pulmonary intracellular infection. J Exp Med. 2016;213(12):2793-809. doi: 10.1084/jem.20160637. PubMed PMID: 27799620; PMCID: PMC5110023.

62. Cavallari M, Stallforth P, Kalinichenko A, Rathwell DC, Gronewold TM, Adibekian A, Mori L, Landmann R, Seeberger PH, De Libero G. A semisynthetic carbohydrate-lipid vaccine that protects against S. pneumoniae in mice. Nat Chem Biol. 2014;10(11):950-6. doi: 10.1038/nchembio.1650. PubMed PMID: 25282505.

63. Pollard AJ, Perrett KP, Beverley PC. Maintaining protection against invasive bacteria with protein-polysaccharide conjugate vaccines. Nat Rev Immunol. 2009;9(3):213-20. doi: 10.1038/nri2494. PubMed PMID: 19214194.

64. Sayeed MA, Bufano MK, Xu P, Eckhoff G, Charles RC, Alam MM, Sultana T, Rashu MR, Berger A, Gonzalez-Escobedo G, Mandlik A, Bhuiyan TR, Leung DT, LaRocque RC, Harris JB, Calderwood SB, Qadri F, Vann WF, Kovac P, Ryan ET. A Cholera Conjugate Vaccine Containing O-specific Polysaccharide (OSP) of V. cholerae O1 Inaba and Recombinant Fragment of Tetanus Toxin Heavy Chain (OSP:rTTHc) Induces Serum, Memory and Lamina Proprial Responses against OSP and Is Protective in Mice. PLoS Negl Trop Dis. 2015;9(7):e0003881. doi: 10.1371/journal.pntd.0003881. PubMed PMID: 26154421; PMCID: PMC4495926.

Most read articles by the same author(s)