Taxa of the nasal microbiome are associated with influenza-specificIgA response to live attenuated influenza vaccine

PLoS ONE

Volumn 11, Issue 9, 2016, Pages

  Salk, Hannah M ^a   Simon, Whitney L ^a   Lambert, Nathanield ^a   Kennedy, Richard B ^a   Grill, Diane E ^a   Kabat, Brian F ^a   Poland, Gregory A ^a  

^a MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN A; IMMUNOGLOBULIN A ANTIBODY; INFLUENZA VACCINE; RNA 16S; INFLUENZA VIRUS HEMAGGLUTININ; LIVE VACCINE; VIRUS ANTIBODY;

ADULT; ANTIBODY RESPONSE; ARTICLE; BACTEROIDES OVATUS; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GENE AMPLIFICATION; HUMAN; HUMAN EXPERIMENT; IMMUNE RESPONSE; IMMUNOGLOBULIN PRODUCTION; INFLUENZA VACCINATION; LACTOBACILLUS HELVETICUS; MALE; MICROBIOME; NASAL MICROBIOME; NEXT GENERATION SEQUENCING; NORMAL HUMAN; PREVOTELLA MELANINOGENICA; STREPTOCOCCUS; STREPTOCOCCUS INFANTIS; VEILLONELLA; VEILLONELLA DISPAR; ADOLESCENT; BACTERIUM; CLASSIFICATION; IMMUNOLOGY; INFLUENZA A VIRUS; INFLUENZA, HUMAN; MICROBIOLOGY; MICROFLORA; NOSE CAVITY; YOUNG ADULT;

ADOLESCENT; ADULT; ANTIBODIES, VIRAL; BACTERIA; FEMALE; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HUMANS; IMMUNOGLOBULIN A; INFLUENZA A VIRUS; INFLUENZA VACCINES; INFLUENZA, HUMAN; MALE; MICROBIOTA; NASAL CAVITY; VACCINES, ATTENUATED; YOUNG ADULT;

EID: 84992389893     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0162803     Document Type: Article

References (54)

1. World Health Organization (2003) Influenza Fact Sheet N211. Available: http://www.who.int/mediacentre/factsheets/fs211/en/.
2. Cerf-Bensussan N, Gaboriau-Routhiau V (2010) The immune system and the gut microbiota: friends or foes Nature Reviews Immunology 10: 735-744. doi:10.1038/nri2850 PMID: 20865020.
3. Zhang K, Hornef MW, Dupont A (2015) The intestinal epithelium as guardian of gut barrier integrity. Cellular microbiology 17: 1561-1569. doi:10.1111/cmi.12501PMID: 26294173.
4. Ichinohe T, Pang IK, Kumamoto Y, Peaper DR, Ho JH, Murray TS, et al (2011) Microbiota regulates immune defense against respiratory tract influenza A virus infection. Proceedings of the National Academy of Sciences of the United States of America 108: 5354-5359. doi:10.1073/pnas.1019378108 PMID: 21402903.
5. Tojo R, Suarez A, Clemente MG, de los Reyes-Gavilan CG, Margolles A, et al (2014) Intestinal microbiota in health and disease: Role of bifidobacteria in gut homeostasis. World journal of gastroenterology 20: 15163-15176. doi: 10.3748/wjg.v20.i41.15163 PMID: 25386066.
6. Abt MC, Osborne LC, Monticelli LA, Doering TA, Alenghat T, Sonnenberg GF (2012) Commensal bacteria calibrate the activation threshold of innate antiviral immunity. Immunity 37: 158-170. doi:10.1016/j.immuni.2012.04.011PMID: 22705104.
7. Samuelson DR, Welsh DA, Shellito JE (2015) Regulation of lung immunity and host defense by the intestinal microbiota. Frontiers in microbiology 6: 1085. doi:10.3389/fmicb.2015.01085 PMID: 26500629.
8. Southam DS, Dolovich M, O'Byrne PM, Inman MD (2002) Distribution of intranasal instillations in mice: Effects of volume, time, body position, and anesthesia. American journal of physiology Lung cellular and molecular physiology 282: L833- L839. PMID: 11880310.
9. Oh JZ, Ravindran R, Chassaing B, Carvalho FA, Maddur MS, Bower M, et al. (2014) TLR5-mediated sensing of gut microbiota is necessary for antibody responses to seasonal influenza vaccination. Immunity 41: 478-492. doi:10.1016/j.immuni.2014.08.009 PMID: 25220212.
10. Pabst O, Hornef M (2014) Gut microbiota: A natural adjuvant for vaccination. Immunity 41: 349-351. doi:10.1016/j.immuni.2014.09.002 PMID: 25238091.
11. Minton K (2014) Microbiota:A 'natural' vaccine adjuvant. Nature reviews Immunology 14: 650-651.
12. Yaqoob P (2014) Ageing, immunity and influenza: A role for probiotics The Proceedings of the Nutrition Society 73: 309-317. doi:10.1017/S0029665113003777 PMID: 24300282.
13. Hall JA, Bouladoux N, Sun CM, Wohlfert EA, Blank RB, Zhu Q, et al. (2008) Commensal DNA limits regulatoryT cell conversion and is a natural adjuvant of intestinal immune responses. Immunity 29: 637- 649. doi:10.1016/j.immuni.2008.08.009 PMID: 18835196.
14. Akatsu H, Nagafuchi S, Kurihara R, Okuda K, Kanesaka T, Ogawa N, et al. (2015) Enhanced vaccination effect against influenza by prebiotics in elderly patients receiving enteral nutrition. Geriatrics& gerontology international 16: 205-213.
15. Barria MI, Garrido JL, Stein C, Scher E, Ge Y, Engel SM, et al. (2013) Localizedmucosal response to intranasal live attenuated influenza vaccine in adults. The Journal of Infectious Diseases 207: 115- 124. doi:10.1093/infdis/jis641 PMID: 23087433.
16. Treanor JJ, Kotloff K, Betts RF, Belshe R, Newman F, Iacuzio D, et al. (1999) Evaluation of trivalent, live, cold-Adapted (CAIV-T) and inactivated (TIV) influenza vaccines in prevention of virus infection and illness following challenge of adults with wild-Type influenza A (H1N1), A (H3N2), and B viruses. Vaccine 18: 899-906. PMID: 10580204.
17. Seto CT, Jeraldo P, Orenstein R, Chia N, DiBaise JK (2014) Prolonged use of a proton pump inhibitor reduces microbial diversity: implications for Clostridium difficile susceptibility. Microbiome 2: 42. doi:10.1186/2049-2618-2-42 PMID: 25426290.
18. Jeraldo P, Kalari K, Chen X, Bhavsar J, Mangalam A, White B, et al. (2014) IM-TORNADO: A tool for comparison of 16S reads from paired-end libraries. PLos ONE 9: E114804. doi:10.1371/journal.pone.0114804 PMID: 25506826.
19. McMurdie PJ, Holmes S (2013) phyloseq: An R package for reproducible interactive analysis and graphics of microbiome census data. PLos ONE 8: E61217. doi:10.1371/journal.pone.0061217 PMID: 23630581.
20. Chao A (1987) Estimating the population size for capture-recapture data with unequal catchability. Biometrics 43: 783-791. PMID: 3427163.
21. Chiu CH, Wang YT, Walther BA, Chao A (2014) An improved nonparametric lower bound of species richness via a modified good-Turing frequency formula. Biometrics 70: 671-682. doi:10.1111/biom.12200 PMID: 24945937.
22. O'Hara RB (2005) Species richness estimators: how many species can dance on the head of a pin J Animal Ecol 74: 375-386.
23. Shannon CE (1949) The mathematical theory of communication: University of Illinois Press.
24. Koeppel AF, Wu M (2013) Surprisingly extensive mixed phylogenetic and ecological signals among bacterial Operational Taxonomic Units. Nucleic Acids Research 41: 5175-5188. doi:10.1093/nar/gkt241 PMID: 23571758.
25. Anders S, Huber W(2010) Differential expression analysis for sequence count data. Genome biology 11: R106. doi:10.1186/gb-2010-11-10-r106 PMID: 20979621.
26. McMurdie PJ, Holmes S (2014)Waste not, want not: Why rarefying microbiome data is inadmissible. PLoS computational biology 10: E1003531. doi:10.1371/journal.pcbi.1003531 PMID: 24699258.
27. Friedman J, Hastie T, Tibshirani R (2010) RegularizationPaths for Generalized Linear Models via Coordinate Descent. JStatSoftw 33: 1-22.
28. Shida K, Nanno M (2008) Probiotics and immunology: separating the wheat from the chaff. Trends in immunology 29: 565-573. doi:10.1016/j.it.2008.07.011 PMID: 18835747.
29. Cani PD, Delzenne NM (2009) The role of the gut microbiota in energy metabolism and metabolic disease. Current pharmaceutical design 15: 1546-1558. PMID: 19442172.
30. O'Flaherty S, Saulnier DM, Pot B, Versalovic J (2010) How can probiotics and prebiotics impactmucosal immunity Gut microbes 1: 293-300. PMID: 21327037.
31. Diaz-Ropero MP, Martin R, Sierra S, Lara-Villoslada F, Rodriguez JM, Xaus J, et al. (2007) Two Lactobacillus strains, isolated from breast milk, differently modulate the immune response. Journal of applied microbiology 102: 337-343. PMID: 17241338.
32. Dong H, Rowland I, Yaqoob P (2012) Comparative effects of six probiotic strains on immune function in vitro. The British journal of nutrition 108: 459-470. doi:10.1017/S0007114511005824 PMID: 22054064.
33. Rizzardini G, Eskesen D, Calder PC, Capetti A, Jespersen L, Clerici M(2012) Evaluation of the immune benefits of two probiotic strains Bifidobacterium animalis ssp. lactis, BB-12(R) and Lactobacillus paracasei ssp. paracasei, L. casei 431(R) in an influenza vaccination model: A randomised, double-blind, placebo-controlled study. The British journal of nutrition 107: 876-884. doi:10.1017/S000711451100420X PMID: 21899798.
34. Li R, ChowdhuryMY, Kim JH, Kim TH, Pathinayake P, Koo WS, et al. (2015) Mucosally administered Lactobacillus surface-displayed influenza antigens (sM2 and HA2) with cholera toxin subunit A1 (CTA1) Induce broadly protective immune responses against divergent influenza subtypes. Veterinary microbiology 179: 250-263. doi:10.1016/j.vetmic.2015.07.020 PMID: 26210951.
35. Chowdhury MY, Li R, Kim JH, Park ME, Kim TH, Pathinayake P, et al. (2014) Mucosal vaccination with recombinant Lactobacillus casei-displayed CTA1-conjugated consensus matrix protein-2 (sM2) induces broad protection against divergent influenza subtypes in BALB/c mice. PLos ONE 9: E94051. doi:10.1371/journal.pone.0094051 PMID: 24714362.
36. Hori T, Kiyoshima J, Shida K, Yasui H (2002) Augmentation of cellular immunity and reduction of influenza virus titer in aged mice fed Lactobacillus casei strain Shirota. Clinical and Diagnostic Laboratory Immunology 9: 105-108. PMID: 11777838.
37. Yasui H, Kiyoshima J, Hori T (2004) Reduction of influenza virus titer and protection against influenza virus infection in infant mice fed Lactobacillus casei Shirota. Clinical and Diagnostic LaboratoryImmunology 11: 675-679. PMID: 15242940.
38. Tomosada Y, Chiba E, Zelaya H, Takahashi T, Tsukida K, Kitazawa H, et al. (2013) Nasally administered Lactobacillus rhamnosus strains differentially modulate respiratory antiviral immune responses and induce protection against respiratory syncytial virus infection. BMC immunology 14: 40. doi:10.1186/1471-2172-14-40PMID: 23947615.
39. Davidson LE, Fiorino AM, Snydman DR, Hibberd PL (2011) Lactobacillus GG as an immune adjuvant for live-Attenuated influenza vaccine in healthy adults: A randomized double-blind placebo-controlled trial. European journal of clinical nutrition 65: 501-507. doi:10.1038/ejcn.2010.289 PMID: 21285968.
40. MacDonald TT, Bell I (2010) Probiotics and the immune response to vaccines. The Proceedings of the Nutrition Society 69: 442-446. doi:10.1017/S0029665110001758PMID: 20540823.
41. Tarabichi Y, Li K, Hu S, Nguyen C, Wang X, Elashoff D, et al. (2015) The administration of intranasal live attenuated influenza vaccine induces changes in the nasal microbiota and nasal epithelium gene expression profiles. Microbiome 3: 74. doi:10.1186/s40168-015-0133-2 PMID: 26667497.
42. de Steenhuijsen Piters WA, Huijskens EG, Wyllie AL, Biesbroek G, van den Bergh MR, Veenhoven RH, et al. (2015) Dysbiosis of upper respiratory tract microbiota in elderly pneumonia patients. The ISME journal 10: 97-108. doi:10.1038/ismej.2015.99PMID: 26151645.
43. Bousbia S, Papazian L, Saux P, Forel JM, Auffray JP, Martin C, et al. (2012) Repertoire of intensive care unit pneumonia microbiota. PLos ONE 7: E32486. doi:10.1371/journal.pone.0032486 PMID: 22389704.
44. Hilty M, Burke C, Pedro H, Cardenas P, Bush A, Bossley C, et al. (2010) Disordered microbialcommunities in asthmatic airways. PLos ONE 5: E8578. doi:10.1371/journal.pone.0008578 PMID: 20052417.
45. Bek-Thomsen M, Tettelin H, Hance I, Nelson KE, Kilian M (2008) Population diversity and dynamics of Streptococcus mitis, Streptococcus oralis, and Streptococcus infantis in the upper respiratory tracts of adults, determined by a nonculture strategy. Infection and Immunity 76: 1889-1896. doi:10.1128/IAI.01511-07 PMID: 18316382.
46. Yi H, Yong D, Lee K, Cho YJ, Chun J (2014) Profiling bacterialcommunity in upper respiratory tracts. BMC infectious diseases 14: 583. doi:10.1186/s12879-014-0583-3 PMID: 25391813.
47. Morris EK, Caruso T, Buscot F, Fischer M, Hancock C, Maier TS, et al. (2014) Choosing and using diversity indices: insights for ecological applications from the GermanBiodiversity Exploratories. Ecology and evolution 4: 3514-3524. doi:10.1002/ece3.1155 PMID: 25478144.
48. Mina MJ, McCullers JA, Klugman KP (2014) Live attenuated influenza vaccine enhances colonization of Streptococcus pneumoniae and Staphylococcus aureus in mice. mBio 5.
49. Planet PJ, Parker D, Cohen TS, Smith H, Leon JD, Ryan C, et al. (2016) Lambda Interferon Restructures the Nasal Microbiome and Increases Susceptibility to Staphylococcus aureus Superinfection. mBio 7: E01939-01915. doi:10.1128/mBio.01939-15 PMID: 26861017.
50. Le Chatelier E, Nielsen T, Qin J, Prifti E, Hildebrand F, Falony G, et al. (2013) Richness of human gut microbiome correlates with metabolic markers. Nature 500: 541-546. doi:10.1038/nature12506 PMID: 23985870.
51. Poland GA, Kennedy RB, McKinney BA, Ovsyannikova IG, Lambert ND, Jacobson RM, et al. (2013) Vaccinomics, adversomics, and the immune response network theory: Individualized vaccinology in the 21st century. Seminars in Immunology 25: 89-103. doi:10.1016/j.smim.2013.04.007 PMID: 23755893.
52. Poland GA, Kennedy RB, Ovsyannikova IG (2011) Vaccinomics and personalized vaccinology: Is science leading us toward a new path of directed vaccine development and discovery PLoS Pathogens 7: E1002344. doi:10.1371/journal.ppat.1002344PMID: 22241978.
53. Poland GA, Ovsyannikova IG, Kennedy RB, Haralambieva IH, Jacobson RM (2011) Vaccinomics and a new paradigm for the development of preventive vaccines against viral infections. Omics 15: 625- 636. doi:10.1089/omi.2011.0032 PMID: 21732819.
54. Haralambieva IH, Poland GA (2010) Vaccinomics, predictive vaccinology and the future of vaccine development. Future Microbiol 5: 1757-1760. doi:10.2217/fmb.10.146PMID: 21155658.