Impact of oral probiotic Lactobacillus acidophilus vaccine strains on the immune response and gut microbiome of mice
Autoři:
Zaid Abdo aff001; Jonathan LeCureux aff001; Alora LaVoy aff001; Bridget Eklund aff001; Elizabeth P. Ryan aff002; Gregg A. Dean aff001
Působiště autorů:
Department of Microbiology, Immunology and Pathology, Colorado State University, Fort Collins, Colorado, United States of America
aff001; Department of Environmental and Radiological Health Sciences, Colorado State University, Fort Collins, Colorado, United States of America
aff002
Vyšlo v časopise:
PLoS ONE 14(12)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0225842
Souhrn
The potential role of probiotic bacteria as adjuvants in vaccine trials led to their use as nonparenteral live mucosal vaccine vectors. Yet, interactions between these vectors, the host and the microbiome are poorly understood. This study evaluates impact of three probiotic, Lactobacillus acidophilus, vector strains, and their interactions with the host’s immune response, on the gut microbiome. One strain expressed the membrane proximal external region from HIV-1 (MPER). The other two expressed MPER and either secreted interleukin-1ß (IL-1ß) or expressed the surface flagellin subunit C (FliC) as adjuvants. We also used MPER with rice bran as prebiotic supplement. We observed a strain dependent, differential effect suggesting that MPER and IL-1β induced a shift of the microbiome while FliC had minimal impact. Joint probiotic and prebiotic use resulted in a compound effect, highlighting a potential synbiotic approach to impact efficacy of vaccination. Careful consideration of constitutive adjuvants and use of prebiotics is needed depending on whether or not to target microbiome modulation to improve vaccine efficacy. No clear associations were observed between total or MPER-specific IgA and the microbiome suggesting a role for other immune mechanisms or a need to focus on IgA-bound, resident microbiota, most affected by an immune response.
Klíčová slova:
Rice – Immune response – Vaccination and immunization – Vaccines – Microbiome – Immunologic adjuvants – Lactobacillus – Probiotics
Zdroje
1. Sekirov I, Russell SL, Antunes LCM, Finlay BB. Gut Microbiota in Health and Disease. Physiol Rev. 2010;90: 859–904. doi: 10.1152/physrev.00045.2009 20664075
2. Kinross JM, Darzi AW, Nicholson JK. Gut microbiome-host interactions in health and disease. Genome Med. 2011;3: 14. doi: 10.1186/gm228 21392406
3. Cho I, Blaser MJ. The human microbiome: at the interface of health and disease. Nat Rev Genet. 2012;13: nrg3182. doi: 10.1038/nrg3182 22411464
4. Ley RE, Bäckhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI. Obesity alters gut microbial ecology. Proc Natl Acad Sci. 2005;102: 11070–11075. doi: 10.1073/pnas.0504978102 16033867
5. Bäckhed F, Fraser CM, Ringel Y, Sanders ME, Sartor RB, Sherman PM. Defining a healthy human gut microbiome: current concepts, future directions, and clinical applications. Cell Host Microbe. 2012;12. doi: 10.1016/j.chom.2012.10.012 23159051
6. Bokulich NA, Chung J, Battaglia T, Henderson N, Jay M, Li H, et al. Antibiotics, birth mode, and diet shape microbiome maturation during early life. Sci Transl Med. 2016;8: 343ra82–343ra82. doi: 10.1126/scitranslmed.aad7121 27306664
7. Preidis GA, Versalovic J. Targeting the Human Microbiome With Antibiotics, Probiotics, and Prebiotics: Gastroenterology Enters the Metagenomics Era. Gastroenterology. 2009;136: 2015–2031. doi: 10.1053/j.gastro.2009.01.072 19462507
8. Raymond F, Ouameur AA, Déraspe M, Iqbal N, Gingras H, Dridi B, et al. The initial state of the human gut microbiome determines its reshaping by antibiotics. ISME J. 2015 [cited 25 Mar 2016]. http://www.nature.com/ismej/journal/vaop/ncurrent/full/ismej2015148a.html
9. Petschow B, Doré J, Hibberd P, Dinan T, Reid G, Blaser M, et al. Probiotics, prebiotics, and the host microbiome: the science of translation: Probiotics, prebiotics, and the host microbiome. Ann N Y Acad Sci. 2013;1306: 1–17. doi: 10.1111/nyas.12303 24266656
10. Saulnier DM, Ringel Y, Heyman MB, Foster JA, Bercik P, Shulman RJ, et al. The intestinal microbiome, probiotics and prebiotics in neurogastroenterology. Gut Microbes. 2013;4: 17–27. doi: 10.4161/gmic.22973 23202796
11. Sheflin AM, Borresen EC, Wdowik MJ, Rao S, Brown RJ, Heuberger AL, et al. Pilot Dietary Intervention with Heat-Stabilized Rice Bran Modulates Stool Microbiota and Metabolites in Healthy Adults. Nutrients. 2015;7: 1282–1300. doi: 10.3390/nu7021282 25690418
12. Gerritsen J, Smidt H, Rijkers GT, Vos WM. Intestinal microbiota in human health and disease: the impact of probiotics. Genes Nutr. 2011;6: 209. doi: 10.1007/s12263-011-0229-7 21617937
13. Ng SC, Hart AL, Kamm MA, Stagg AJ, Knight SC. Mechanisms of Action of Probiotics: Recent Advances. Inflamm Bowel Dis. 2009;15: 300–310. doi: 10.1002/ibd.20602 18626975
14. Sonnenburg JL, Chen CTL, Gordon JI. Genomic and Metabolic Studies of the Impact of Probiotics on a Model Gut Symbiont and Host. PLOS Biol. 2006;4: e413. doi: 10.1371/journal.pbio.0040413 17132046
15. O’Toole PW, Cooney JC. Probiotic Bacteria Influence the Composition and Function of the Intestinal Microbiota. Interdiscip Perspect Infect Dis. 2008; 9. doi: 10.1155/2008/175285 19277099
16. Vanhoutvin SALW, Troost FJ, Hamer HM, Lindsey PJ, Koek GH, Jonkers DMAE, et al. Butyrate-Induced Transcriptional Changes in Human Colonic Mucosa. PLOS ONE. 2009;4: e6759. doi: 10.1371/journal.pone.0006759 19707587
17. Valdez Y, Brown EM, Finlay BB. Influence of the microbiota on vaccine effectiveness. Trends Immunol. 2014;35: 526–537. doi: 10.1016/j.it.2014.07.003 25113637
18. Harris V, Ali A, Fuentes S, Korpela K, Kazi M, Tate J, et al. Rotavirus vaccine response correlates with the infant gut microbiota composition in Pakistan. Gut Microbes. 2017;0: 1–9. doi: 10.1080/19490976.2017.1376162 28891751
19. Harris VC, Armah G, Fuentes S, Korpela KE, Parashar U, Victor JC, et al. Significant Correlation Between the Infant Gut Microbiome and Rotavirus Vaccine Response in Rural Ghana. J Infect Dis. 2017;215: 34–41. doi: 10.1093/infdis/jiw518 27803175
20. Kandasamy S, Chattha KS, Vlasova AN, Rajashekara G, Saif LJ. Lactobacilli and Bifidobacteria enhance mucosal B cell responses and differentially modulate systemic antibody responses to an oral human rotavirus vaccine in a neonatal gnotobiotic pig disease model. Gut Microbes. 2014;5: 639–651. doi: 10.4161/19490976.2014.969972 25483333
21. Marelli B, Perez AR, Banchio C, de Mendoza D, Magni C. Oral immunization with live Lactococcus lactis expressing rotavirus VP8* subunit induces specific immune response in mice. J Virol Methods. 2011;175: 28–37. doi: 10.1016/j.jviromet.2011.04.011 21530589
22. Pant N, Marcotte H, Brüssow H, Svensson L, Hammarström L. Effective prophylaxis against rotavirus diarrhea using a combination of Lactobacillus rhamnosus GG and antibodies. BMC Microbiol. 2007;7: 86. doi: 10.1186/1471-2180-7-86 17900343
23. Park MS, Kwon B, Ku S, Ji GE. The Efficacy of Bifidobacterium longum BORI and Lactobacillus acidophilus AD031 Probiotic Treatment in Infants with Rotavirus Infection. Nutrients. 2017;9: 887. doi: 10.3390/nu9080887 28813007
24. Lee I-C, Tomita S, Kleerebezem M, Bron PA. The quest for probiotic effector molecules—Unraveling strain specificity at the molecular level. Pharmacol Res. 2013;69: 61–74. doi: 10.1016/j.phrs.2012.09.010 23059538
25. Tarahomjoo S. Development of Vaccine Delivery Vehicles Based on Lactic Acid Bacteria. Mol Biotechnol. 2012;51: 183–199. doi: 10.1007/s12033-011-9450-2 21901278
26. LeBlanc JG, Aubry C, Cortes-Perez NG, de Moreno de LeBlanc A, Vergnolle N, Langella P, et al. Mucosal targeting of therapeutic molecules using genetically modified lactic acid bacteria: an update. FEMS Microbiol Lett. 2013;344: 1–9. doi: 10.1111/1574-6968.12159 23600579
27. LeCureux JS, Dean GA. Lactobacillus Mucosal Vaccine Vectors: Immune Responses against Bacterial and Viral Antigens. mSphere. 2018;3: e00061–18. doi: 10.1128/mSphere.00061-18 29769376
28. Ruiz L, Margolles A, Sánchez B. Bile resistance mechanisms in Lactobacillus and Bifidobacterium. Front Microbiol. 2013;4. doi: 10.3389/fmicb.2013.00396 24399996
29. Kajikawa A, Nordone SK, Zhang L, Stoeker LL, LaVoy AS, Klaenhammer TR, et al. Dissimilar Properties of Two Recombinant Lactobacillus acidophilus Strains Displaying Salmonella FliC with Different Anchoring Motifs. Appl Environ Microbiol. 2011;77: 6587–6596. doi: 10.1128/AEM.05153-11 21784918
30. Wells JM, Mercenier A. Mucosal delivery of therapeutic and prophylactic molecules using lactic acid bacteria. Nat Rev Microbiol. 2008;6: 349–362. doi: 10.1038/nrmicro1840 18345021
31. Lebeer S, Vanderleyden J, De Keersmaecker SCJ. Host interactions of probiotic bacterial surface molecules: comparison with commensals and pathogens. Nat Rev Microbiol. 2010;8: 171–184. doi: 10.1038/nrmicro2297 20157338
32. Girardin SE, Boneca IG, Viala J, Chamaillard M, Labigne A, Thomas G, et al. Nod2 Is a General Sensor of Peptidoglycan through Muramyl Dipeptide (MDP) Detection. J Biol Chem. 2003;278: 8869–8872. doi: 10.1074/jbc.C200651200 12527755
33. Matsuguchi T, Takagi A, Matsuzaki T, Nagaoka M, Ishikawa K, Yokokura T, et al. Lipoteichoic Acids from Lactobacillus Strains Elicit Strong Tumor Necrosis Factor Alpha-Inducing Activities in Macrophages through Toll-Like Receptor 2. Clin Diagn Lab Immunol. 2003;10: 259–266. doi: 10.1128/CDLI.10.2.259-266.2003 12626452
34. Zeuthen LH, Fink LN, Frøkiær H. Toll-like receptor 2 and nucleotide-binding oligomerization domain-2 play divergent roles in the recognition of gut-derived lactobacilli and bifidobacteria in dendritic cells. Immunology. 2008;124: 489–502. doi: 10.1111/j.1365-2567.2007.02800.x 18217947
35. Chorny A, Puga I, Cerutti A. Chapter 2—Innate Signaling Networks in Mucosal IgA Class Switching. In: Fagarasan S, Cerutti A, editors. Advances in Immunology. Academic Press; 2010. pp. 31–69. doi: 10.1016/B978-0-12-381300-8.00002-2 21034970
36. Konstantinov SR, Smidt H, de Vos WM, Bruijns SC, Singh SK, Valence F, et al. S layer protein A of Lactobacillus acidophilus NCFM regulates immature dendritic cell and T cell functions. Proc Natl Acad Sci. 2008;105: 19474–19479. doi: 10.1073/pnas.0810305105 19047644
37. Van Tassell ML, Miller MJ. Lactobacillus Adhesion to Mucus. Nutrients. 2011;3: 613–636. doi: 10.3390/nu3050613 22254114
38. Vélez MP, De Keersmaecker SCJ, Vanderleyden J. Adherence factors of Lactobacillus in the human gastrointestinal tract. FEMS Microbiol Lett. 2007;276: 140–148. doi: 10.1111/j.1574-6968.2007.00908.x 17888009
39. Kajikawa A, Zhang L, LaVoy A, Bumgardner S, Klaenhammer TR, Dean GA. Mucosal Immunogenicity of Genetically Modified Lactobacillus acidophilus Expressing an HIV-1 Epitope within the Surface Layer Protein. Ho PL, editor. PLOS ONE. 2015;10: e0141713. doi: 10.1371/journal.pone.0141713 26509697
40. Kajikawa A, Masuda K, Katoh M, Igimi S. Adjuvant Effects for Oral Immunization Provided by Recombinant Lactobacillus casei Secreting Biologically Active Murine Interleukin-1β. Clin Vaccine Immunol. 2010;17: 43–48. doi: 10.1128/CVI.00337-09 19923575
41. Kajikawa A, Zhang L, Long J, Nordone S, Stoeker L, LaVoy A, et al. Construction and Immunological Evaluation of Dual Cell Surface Display of HIV-1 Gag and Salmonella enterica Serovar Typhimurium FliC in Lactobacillus acidophilus for Vaccine Delivery. Clin Vaccine Immunol. 2012;19: 1374–1381. doi: 10.1128/CVI.00049-12 22761297
42. Yang X, Twitchell E, Li G, Wen K, Weiss M, Kocher J, et al. High protective efficacy of rice bran against human rotavirus diarrhea via enhancing probiotic growth, gut barrier function, and innate immunity. Sci Rep. 2015;5: 15004. doi: 10.1038/srep15004 26459937
43. Chassaing B, Ley RE, Gewirtz AT. Intestinal Epithelial Cell Toll-like Receptor 5 Regulates the Intestinal Microbiota to Prevent Low-Grade Inflammation and Metabolic Syndrome in Mice. Gastroenterology. 2014;147: 1363–1377.e17. doi: 10.1053/j.gastro.2014.08.033 25172014
44. Kajikawa A, Igimi S. Development of Recombinant Vaccines in Lactobacilli for Elimination of Salmonella. Biosci Microflora. 2011;30: 93–98. doi: 10.12938/bifidus.30.93 25045314
45. Gerritsen J, Smidt H, Rijkers GT, de Vos WM. Intestinal microbiota in human health and disease: the impact of probiotics. Genes Nutr. 2011;6: 209. doi: 10.1007/s12263-011-0229-7 21617937
46. Cleland EJ, Drilling A, Bassiouni A, James C, Vreugde S, Wormald P-J. Probiotic manipulation of the chronic rhinosinusitis microbiome. Int Forum Allergy Rhinol. 2014;4: 309–314. doi: 10.1002/alr.21279 24415658
47. Kandasamy S, Vlasova AN, Fischer DD, Chattha KS, Shao L, Kumar A, et al. Unraveling the Differences between Gram-Positive and Gram-Negative Probiotics in Modulating Protective Immunity to Enteric Infections. Front Immunol. 2017;8. doi: 10.3389/fimmu.2017.00334 28396664
48. Harris VC. The Significance of the Intestinal Microbiome for Vaccinology: From Correlations to Therapeutic Applications. Drugs. 2018;78: 1063–1072. doi: 10.1007/s40265-018-0941-3 29943376
49. Parker EPK, Praharaj I, Zekavati A, Lazarus RP, Giri S, Operario DJ, et al. Influence of the intestinal microbiota on the immunogenicity of oral rotavirus vaccine given to infants in south India. Vaccine. 2018;36: 264–272. doi: 10.1016/j.vaccine.2017.11.031 29217369
50. Parker EP, Ramani S, Lopman BA, Church JA, Iturriza-Gómara M, Prendergast AJ, et al. Causes of impaired oral vaccine efficacy in developing countries. Future Microbiol. 2018;13: 97–118. doi: 10.2217/fmb-2017-0128 29218997
51. Sheflin AM, Borresen EC, Kirkwood JS, Boot CM, Whitney AK, Lu S, et al. Dietary supplementation with rice bran or navy bean alters gut bacterial metabolism in colorectal cancer survivors. Mol Nutr Food Res. 2017;61: 1500905. doi: 10.1002/mnfr.201500905 27461523
52. Broussard JL, Devkota S. The changing microbial landscape of Western society: Diet, dwellings and discordance. Mol Metab. 2016;5: 737–742. doi: 10.1016/j.molmet.2016.07.007 27617196
53. Smits SA, Marcobal A, Higginbottom S, Sonnenburg JL, Kashyap PC. Individualized Responses of Gut Microbiota to Dietary Intervention Modeled in Humanized Mice. Dorrestein PC, editor. mSystems. 2016;1: e00098–16. doi: 10.1128/mSystems.00098-16 27822551
54. Bisanz JE, Upadhyay V, Turnbaugh JA, Ly K, Turnbaugh P. Diet Induces Reproducible Alterations in the Mouse and Human Gut Microbiome. Rochester, NY: Social Science Research Network; 2019 Feb. Report No.: ID 3330558. https://papers.ssrn.com/abstract=3330558
55. Meehan CJ, Beiko RG. A Phylogenomic View of Ecological Specialization in the Lachnospiraceae, a Family of Digestive Tract-Associated Bacteria. Genome Biol Evol. 2014;6: 703–713. doi: 10.1093/gbe/evu050 24625961
56. Milani C, Lugli GA, Duranti S, Turroni F, Mancabelli L, Ferrario C, et al. Bifidobacteria exhibit social behavior through carbohydrate resource sharing in the gut. Sci Rep. 2015;5: 15782. doi: 10.1038/srep15782 26506949
57. Wang X, Brown IL, Evans AJ, Conway PL. The protective effects of high amylose maize (amylomaize) starch granules on the survival of Bifidobacterium spp. in the mouse intestinal tract. J Appl Microbiol. 1999;87: 631–639. doi: 10.1046/j.1365-2672.1999.00836.x 10594702
58. Laukens D, Brinkman BM, Raes J, De Vos M, Vandenabeele P. Heterogeneity of the gut microbiome in mice: guidelines for optimizing experimental design. FEMS Microbiol Rev. 2016;40: 117–132. doi: 10.1093/femsre/fuv036 26323480
59. Kumar A, Henderson A, Forster GM, Goodyear AW, Weir TL, Leach JE, et al. Dietary rice bran promotes resistance to Salmonella enterica serovar Typhimurium colonization in mice. BMC Microbiol. 2012;12: 71. doi: 10.1186/1471-2180-12-71 22583915
60. Kajikawa A, Zhang L, LaVoy A, Bumgardner S, Klaenhammer TR, Dean GA. Mucosal Immunogenicity of Genetically Modified Lactobacillus acidophilus Expressing an HIV-1 Epitope within the Surface Layer Protein. Ho PL, editor. PLOS ONE. 2015;10: e0141713. doi: 10.1371/journal.pone.0141713 26509697
61. Bumgardner SA, Zhang L, LaVoy AS, Andre B, Frank CB, Kajikawa A, et al. Nod2 is required for antigen-specific humoral responses against antigens orally delivered using a recombinant Lactobacillus vaccine platform. PLOS ONE. 2018;13: e0196950. doi: 10.1371/journal.pone.0196950 29734365
62. Stoeker L, Nordone S, Gunderson S, Zhang L, Kajikawa A, LaVoy A, et al. Assessment of Lactobacillus gasseri as a Candidate Oral Vaccine Vector. Clin Vaccine Immunol. 2011;18: 1834–1844. doi: 10.1128/CVI.05277-11 21900526
63. Frey A, Di Canzio J, Zurakowski D. A statistically defined endpoint titer determination method for immunoassays. J Immunol Methods. 1998;221: 35–41. doi: 10.1016/s0022-1759(98)00170-7 9894896
64. Methé BA, Nelson KE, Pop M, Creasy HH, Giglio MG, Huttenhower C, et al. A framework for human microbiome research. Nature. 2012;486: 215–221. doi: 10.1038/nature11209 22699610
65. Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD. Development of a Dual-Index Sequencing Strategy and Curation Pipeline for Analyzing Amplicon Sequence Data on the MiSeq Illumina Sequencing Platform. Appl Environ Microbiol. 2013;79: 5112–5120. doi: 10.1128/AEM.01043-13 23793624
66. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, et al. Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities. Appl Environ Microbiol. 2009;75: 7537–7541. doi: 10.1128/AEM.01541-09 19801464
67. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013;41: D590–D596. doi: 10.1093/nar/gks1219 23193283
68. Westcott SL, Schloss PD. OptiClust, an Improved Method for Assigning Amplicon-Based Sequence Data to Operational Taxonomic Units. mSphere. 2017;2: e00073–17. doi: 10.1128/mSphereDirect.00073-17 28289728
69. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, et al. vegan: Community Ecology Package. 2014. http://CRAN.R-project.org/package=vegan
70. R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria; 2017. https://www.R-project.org/.
71. McMurdie PJ, Holmes S. phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data. PLOS ONE. 2013;8: e61217. doi: 10.1371/journal.pone.0061217 23630581
72. Plummer M, Stukalov A, Denwood M. Package ‘rjags.’ 2016. http://mcmc-jags.sourceforge.net/
73. Plummer M, others. JAGS: A program for analysis of Bayesian graphical models using Gibbs sampling. Proceedings of the 3rd international workshop on distributed statistical computing. Vienna; 2003. p. 125. http://www.ci.tuwien.ac.at/Conferences/DSC-2003/Drafts/Plummer.pdf
74. Spiegelhalter DJ, Best NG, Carlin BP, Van Der Linde A. Bayesian measures of model complexity and fit. J R Stat Soc Ser B Stat Methodol. 2002;64: 583–639.
75. Gelman A, Rubin DB. Inference from iterative simulation using multiple sequences. Stat Sci. 1992;7: 457–511.
76. Legendre P, Legendre L. Numerical Ecology. 2nd ed. Amsterdam, The Netherlands: Elsevier B.V.; 1998.
77. Paulson JN, Stine OC, Bravo HC, Pop M. Differential abundance analysis for microbial marker-gene surveys. Nat Methods. 2013;10: 1200–1202. doi: 10.1038/nmeth.2658 24076764
78. Wickham H. ggplot2: Elegant graphics for data analysis. New York, NY: Springer Science+Business Media; 2009.
79. Breiman L. Random forests. Mach Learn. 2001;45: 5–32.
80. Breiman L, Cutler A, Liaw A, Wiener M. Package ‘randomForest.’ 2015. ftp://ie.freshrpms.net/pub/CRAN/web/packages/randomForest/randomForest.pdf
81. Spearman C. Correlation between arrays in a table of correlations. Proc R Soc Lond Ser Contain Pap Math Phys Character. 1922;101: 94–100.
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