High-avidity IgA protects the intestine by enchaining growing bacteria

Nature

Volumn 544, Issue 7651, 2017, Pages 498-502

  Moor, Kathrin ^a,h   Diard, Médéric ^a   Sellin, Mikael E ^a,b   Felmy, Boas ^a   Wotzka, Sandra Y ^a   Toska, Albulena ^a   Bakkeren, Erik ^a   Arnoldini, Markus ^a   Bansept, Florence ^c   Co, Alma Dal ^a,d   Völler, Tom ^a   Minola, Andrea ^e   Fernandez Rodriguez, Blanca ^f   Agatic, Gloria ^e   Barbieri, Sonia ^f   Piccoli, Luca ^f   Casiraghi, Costanza ^f,i   Corti, Davide ^e   Lanzavecchia, Antonio ^a,f   Regoes, Roland R ^a   Loverdo, Claude ^c   Stocker, Roman ^a   Brumley, Douglas R ^a,g   Hardt, Wolf Dietrich ^a   Slack, Emma ^a   more..

^a ETH ZURICH   (Switzerland)

^b UPPSALA UNIVERSITY   (Sweden)

^c University Paris Diderot   (France)

^d SWISS FEDERAL INSTITUTE OF AQUATIC SCIENCE AND TECHNOLOGY   (Switzerland)

^e Swiss Federal Institute of Aquatic Science and Technology ^*  (Switzerland)

^f INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Switzerland)

^g UNIVERSITY OF MELBOURNE   (Australia)

^h UNIVERSITY OF ZURICH   (Switzerland)

ⁱ UNIVERSITY OF BOLOGNA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN A; STREPTOMYCIN; BACTERIAL VACCINE;

ANTIBODY; BACTERIUM; DIGESTIVE SYSTEM; GROWTH RESPONSE; IMMUNE SYSTEM; INFECTIVITY; INVASIVE SPECIES; PATHOGEN; PLASMID; SUBSPECIES; VACCINE; VIRULENCE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN ANTIBODY REACTION; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GROWTH; BACTERICIDAL ACTIVITY; CELL DENSITY; COLONY FORMING UNIT; CONJUGATION; CONTROLLED STUDY; CROSS LINKING; DAUGHTER CELL; FEMALE; HORIZONTAL GENE TRANSFER; IN VITRO STUDY; INTESTINE FLORA; MALE; MATHEMATICAL MODEL; MOUSE; NONHUMAN; PATHOGEN CLEARANCE; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; ANIMAL; ANTIBODY AFFINITY; BACTERIAL COUNT; BACTERIUM ADHERENCE; BACTERIUM CONJUGATION; CECUM; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; IMMUNOLOGY; INTESTINE; MICROBIOLOGY; PATHOGENICITY; PLASMID; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; SALMONELLA INFECTIONS;

BACTERIA (MICROORGANISMS); SALMONELLA ENTERICA;

ANIMALS; ANTIBODY AFFINITY; BACTERIAL ADHESION; BACTERIAL VACCINES; CECUM; COLONY COUNT, MICROBIAL; CONJUGATION, GENETIC; FEMALE; HUMANS; IMMUNOGLOBULIN A; INTESTINES; MALE; MICE; PLASMIDS; SALMONELLA INFECTIONS; SALMONELLA TYPHIMURIUM;

EID: 85017350184     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature22058     Document Type: Article

References (54)

1. Mantis, N. J., Rol, N., & Corthésy, B. Secretory IgA?s complex roles in immunity and mucosal homeostasis in the gut. Mucosal Immunol. 4, 603-611 (2011
2. Pabst, O. New concepts in the generation and functions of IgA. Nat. Rev. Immunol. 12, 821-832 (2012
3. Slack, E., Balmer, M. L., & Macpherson, A. J. B cells as a critical node in the microbiota-host immune system network. Immunol. Rev. 260, 50-66 (2014
4. WHO. Risk assessments of Salmonella in eggs and broiler chickens. http://www. who.int/foodsafety/publications/micro/salmonella/en/ (2002
5. Gopinath, S., Carden, S., & Monack, D. Shedding light on Salmonella carriers. Trends Microbiol. 20, 320-327 (2012
6. White, P. B. Further Studies of the Salmonella Group. Great Britain Medical Research Council (Her Majesty?s Stationary Office) 103, 3-160 (1926
7. Le Minor, L., & Popoff, M. Y. Kauffmann-White-Scheme (Behring Diagnostika, 1988
8. Endt, K., et al. The microbiota mediates pathogen clearance from the gut lumen after non-Typhoidal Salmonella diarrhea. PLoS Pathog. 6, e1001097 (2010
9. Hendrickx, A. P., et al. Antibiotic-driven dysbiosis mediates intraluminal agglutination and alternative segregation of Enterococcus faecium from the intestinal epithelium. MBio 6, e01346e15 (2015
10. Levinson, K. J., De Jesus, M., & Mantis, N. J. Rapid effects of a protective O-polysaccharide-specific monoclonal IgA on Vibrio cholerae agglutination, motility, and surface morphology. Infect. Immun. 83, 1674-1683 (2015
11. Kiørboe, T. A mechanistic approach to plankton ecology. (Princeton Univ. Press, 2008
12. van Schothorst, M., & Beckers, H. J. Persistent excretion of salmonellas. BMJ 2, 1301 (1978
13. Forbes, S. J., Eschmann, M., & Mantis, N. J. Inhibition of Salmonella enterica serovar Typhimurium motility and entry into epithelial cells by a protective antilipopolysaccharide monoclonal immunoglobulin A antibody. Infect. Immun. 76, 4137-4144 (2008
14. Forbes, S. J., et al. Association of a protective monoclonal IgA with the O antigen of Salmonella enterica serovar Typhimurium impacts type 3 secretion and outer membrane integrity. Infect. Immun. 80, 2454-2463 (2012
15. Amarasinghe, J. J., D'Hondt, R. E., Waters, C. M., & Mantis, N. J. Exposure of Salmonella enterica serovar Typhimurium to a protective monoclonal IgA triggers exopolysaccharide production via a diguanylate cyclase-dependent pathway. Infect. Immun. 81, 653-664 (2013
16. Michetti, P., Mahan, M. J., Slauch, J. M., Mekalanos, J. J., & Neutra, M. R. Monoclonal secretory immunoglobulin A protects mice against oral challenge with the invasive pathogen Salmonella typhimurium. Infect. Immun. 60, 1786-1792 (1992
17. Michetti, P., et al. Monoclonal immunoglobulin A prevents adherence and invasion of polarized epithelial cell monolayers by Salmonella typhimurium. Gastroenterology 107, 915-923 (1994
18. Barthel, M., et al. Pretreatment of mice with streptomycin provides a Salmonella enterica serovar Typhimurium colitis model that allows analysis of both pathogen and host. Infect. Immun. 71, 2839-2858 (2003
19. Kaiser, P., Diard, M., Stecher, B., & Hardt, W. D. The streptomycin mouse model for Salmonella diarrhea: functional analysis of the microbiota, the pathogen?s virulence factors, and the host?s mucosal immune response. Immunol. Rev. 245, 56-83 (2012
20. Hapfelmeier, S., et al. The Salmonella pathogenicity island (SPI)-2 and SPI-1 type III secretion systems allow Salmonella serovar Typhimurium to trigger colitis via MyD88-dependent and MyD88-independent mechanisms. J. Immunol. 174, 1675-1685 (2005
21. Moor, K., et al. Peracetic acid treatment generates potent inactivated oral vaccines from a broad range of culturable bacterial species. Front. Immunol. 7, 34 (2016
22. Kaiser, P., Slack, E., Grant, A. J., Hardt, W. D., & Regoes, R. R. Lymph node colonization dynamics after oral Salmonella typhimurium infection in mice. PLoS Pathog. 9, e1003532 (2013
23. Perfeito, L., Fernandes, L., Mota, C., & Gordo, I. Adaptive mutations in bacteria: high rate and small effects. Science 317, 813-815 (2007
24. Barlow, M. Methods in Molecular Biology. Horizontal Gene Transfer 532, 397-411 (2009
25. Grant, A. J., et al. Modelling within-host spatiotemporal dynamics of invasive bacterial disease. PLoS Biol. 6, e74 (2008
26. Maier, L., et al. Granulocytes impose a tight bottleneck upon the gut luminal pathogen population during Salmonella typhimurium colitis. PLoS Pathog. 10, e1004557 (2014
27. Stecher, B., et al. Salmonella enterica serovar typhimurium exploits inflammation to compete with the intestinal microbiota. PLoS Biol. 5, 2177-2189 (2007
28. Stecher, B., et al. Gut inflammation can boost horizontal gene transfer between pathogenic and commensal Enterobacteriaceae. Proc. Natl Acad. Sci. USA 109, 1269-1274 (2012
29. Stecher, B., et al. Like will to like: abundances of closely related species can predict susceptibility to intestinal colonization by pathogenic and commensal bacteria. PLoS Pathog. 6, e1000711 (2010
30. Palm, N. W., et al. Immunoglobulin A coating identifies colitogenic bacteria in inflammatory bowel disease. Cell 158, 1000-1010 (2014
31. Müller, A. J., et al. Salmonella gut invasion involves TTSS-2-dependent epithelial traversal, basolateral exit, and uptake by epithelium-sampling lamina propria phagocytes. Cell Host Microbe 11, 19-32 (2012
32. Harriman, G. R., et al. Targeted deletion of the IgA constant region in mice leads to IgA deficiency with alterations in expression of other Ig isotypes. J. Immunol. 162, 2521-2529 (1999
33. Uren, T. K., et al. Role of the polymeric Ig receptor in mucosal B cell homeostasis. J. Immunol. 170, 2531-2539 (2003
34. Slack, E., et al. Innate and adaptive immunity cooperate flexibly to maintain host-microbiota mutualism. Science 325, 617-620 (2009
35. Diard, M., et al. Antibiotic treatment selects for cooperative virulence of Salmonella typhimurium. Curr. Biol. 24, 2000-2005 (2014
36. Hoiseth, S. K., & Stocker, B. A. Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature 291, 238-239 (1981
37. Maier, L., et al. Microbiota-derived hydrogen fuels Salmonella typhimurium invasion of the gut ecosystem. Cell Host Microbe 14, 641-651 (2013
38. Stecher, B., et al. Flagella and chemotaxis are required for efficient induction of Salmonella enterica serovar Typhimurium colitis in streptomycin-pretreated mice. Infect. Immun. 72, 4138-4150 (2004
39. Ilg, K., et al. O-Antigen-negative Salmonella enterica serovar Typhimurium is attenuated in intestinal colonization but elicits colitis in streptomycin-Treated mice. Infect. Immun. 77, 2568-2575 (2009
40. Diard, M., et al. Inflammation boosts bacteriophage transfer between Salmonella spp. Science 355, 1211-1215 (2017
41. Nutter, R. L., Bullas, L. R., & Schultz, R. L. Some properties of five new Salmonella bacteriophages. J. Virol. 5, 754-764 (1970
42. Mobley, H. L., et al. Pyelonephritogenic Escherichia coli and killing of cultured human renal proximal tubular epithelial cells: role of hemolysin in some strains. Infect. Immun. 58, 1281-1289 (1990
43. Drecktrah, D., et al. Dynamic behavior of Salmonella-induced membrane tubules in epithelial cells. Traffic 9, 2117-2129 (2008
44. Gil, D., & Bouché, J. P. ColE1-Type vectors with fully repressible replication. Gene 105, 17-22 (1991
45. Moor, K., et al. Analysis of bacterial-surface-specific antibodies in body fluids using bacterial flow cytometry. Nat. Protocols 11, 1531-1553 (2016
46. Traggiai, E., et al. An efficient method to make human monoclonal antibodies from memory B cells: potent neutralization of SARS coronavirus. Nat. Med. 10, 871-875 (2004
47. Helaine, S., et al. Dynamics of intracellular bacterial replication at the single cell level. Proc. Natl Acad. Sci. USA 107, 3746-3751 (2010
48. Sellin, M. E., et al. Epithelium-intrinsic NAIP/NLRC4 inflammasome drives infected enterocyte expulsion to restrict Salmonella replication in the intestinal mucosa. Cell Host Microbe 16, 237-248 (2014
49. Sommer, C., Strähle, C., Köthe, U., & Hamprecht, F. A. ilastik: Interactive Learning and Segmentation Toolkit. Proc. Eighth IEEE International Symposium on Biomedical Imaging (ISBI). 2011, 230-233 (2011
50. Kaiser, P., et al. Cecum lymph node dendritic cells harbor slow-growing bacteria phenotypically tolerant to antibiotic treatment. PLoS Biol. 12, e1001793 (2014
51. Berg, H. C. Random Walks in Biology (Princeton Univ. Press, 1993
52. Jackson, G. A. A model of the formation of marine algal flocs by physical coagulation processes. Deep-Sea Res. A, Oceanogr. Res. Pap. 37, 1197-1211 (1990
53. Kiørboe, T., Andersen, K. P., & Dam, H. G. Coagulation efficiency and aggregate formation in marine phytoplankton. Mar. Biol. 107, 235-245 (1990
54. Lentle, R. G., Hemar, Y., Hall, C. E., & Stafford, K. J. Periodic fluid extrusion and models of digesta mixing in the intestine of a herbivore, the common brushtail possum (Trichosurus vulpecula). J. Comp. Physiol. B 175, 337-347 (2005