Lymphoid Tissue-resident Alcaligenes LPS Induces IgA Production Without Excessive Inflammatory Responses Via Weak TLR4 Agonist Activity

Overview

Journal Mucosal Immunol

Publisher Elsevier

Specialty Allergy & Immunology

Date 2018 Feb 8

PMID 29411777

Citations 18

Authors

Naoko Shibata

Jun Kunisawa

Koji Hosomi

Yukari Fujimoto

Keisuke Mizote

Naohiro Kitayama

Atsushi Shimoyama

Hitomi Mimuro

Shintaro Sato

Natsuko Kishishita

Ken J Ishii

Koichi Fukase

Hiroshi Kiyono

Affiliations

Soon will be listed here.

Abstract

Alcaligenes are opportunistic commensal bacteria that reside in gut-associated lymphoid tissues such as Peyer's patches (PPs); however, how they create and maintain their homeostatic environment, without inducing an excessive inflammatory response remained unclear. We show here that Alcaligenes-derived lipopolysaccharide (Alcaligenes LPS) acts as a weak agonist of toll-like receptor 4 and promotes IL-6 production from dendritic cells, which consequently enhances IgA production. The inflammatory activity of Alcaligenes LPS was weaker than that of Escherichia coli-derived LPS and therefore no excessive inflammation was induced by Alcaligenes LPS in vitro or in vivo. Alcaligenes LPS also showed adjuvanticity, inducing antigen-specific immune responses without excessive inflammation. These findings reveal the presence of commensal bacteria-mediated homeostatic inflammatory conditions within PPs that produce optimal IgA induction without causing pathogenic inflammation and suggest that Alcaligenes LPS could be a safe and potent adjuvant.

Citing Articles

Alcaligenes lipid A functions as a superior mucosal adjuvant to monophosphoryl lipid A via the recruitment and activation of CD11b+ dendritic cells in nasal tissue.

Sun X, Hosomi K, Shimoyama A, Yoshii K, Saika A, Yamaura H Int Immunol. 2023; 36(1):33-43.

PMID: 38006376 PMC: 10823578. DOI: 10.1093/intimm/dxad045.

Changes of gut microbiota in colorectal cancer patients with infection.

Zhang H, Yu Y, Li J, Gong P, Wang X, Li X Front Cell Infect Microbiol. 2022; 12:961974.

PMID: 36118043 PMC: 9471007. DOI: 10.3389/fcimb.2022.961974.

Immunoglobulin A antibody composition is sculpted to bind the self gut microbiome.

Yang C, Chen-Liaw A, Spindler M, Tortorella D, Moran T, Cerutti A Sci Immunol. 2022; 7(73):eabg3208.

PMID: 35857580 PMC: 9421563. DOI: 10.1126/sciimmunol.abg3208.

Chemically Synthesized Lipid A as an Adjuvant to Augment Immune Responses to Type B Conjugate Vaccine.

Liu Z, Hosomi K, Shimoyama A, Yoshii K, Sun X, Lan H Front Pharmacol. 2021; 12:763657.

PMID: 34744743 PMC: 8569242. DOI: 10.3389/fphar.2021.763657.

Lipid A-Mediated Bacterial-Host Chemical Ecology: Synthetic Research of Bacterial Lipid As and Their Development as Adjuvants.

Shimoyama A, Fukase K Molecules. 2021; 26(20).

PMID: 34684874 PMC: 8538916. DOI: 10.3390/molecules26206294.

References

Bromander A, Ekman L, Kopf M, Nedrud J, Lycke N . IL-6-deficient mice exhibit normal mucosal IgA responses to local immunizations and Helicobacter felis infection. J Immunol. 1996; 156(11):4290-7. View

Yoshimura A, Kaneko T, Kato Y, Golenbock D, Hara Y . Lipopolysaccharides from periodontopathic bacteria Porphyromonas gingivalis and Capnocytophaga ochracea are antagonists for human toll-like receptor 4. Infect Immun. 2001; 70(1):218-25. PMC: 127593. DOI: 10.1128/IAI.70.1.218-225.2002. View

Sato A, Linehan M, Iwasaki A . Dual recognition of herpes simplex viruses by TLR2 and TLR9 in dendritic cells. Proc Natl Acad Sci U S A. 2006; 103(46):17343-8. PMC: 1859932. DOI: 10.1073/pnas.0605102103. View

Hirata N, Yanagawa Y, Ebihara T, Seya T, Uematsu S, Akira S . Selective synergy in anti-inflammatory cytokine production upon cooperated signaling via TLR4 and TLR2 in murine conventional dendritic cells. Mol Immunol. 2008; 45(10):2734-42. DOI: 10.1016/j.molimm.2008.02.010. View

Kunisawa J, Sugiura Y, Wake T, Nagatake T, Suzuki H, Nagasawa R . Mode of Bioenergetic Metabolism during B Cell Differentiation in the Intestine Determines the Distinct Requirement for Vitamin B1. Cell Rep. 2015; 13(1):122-131. DOI: 10.1016/j.celrep.2015.08.063. View

Ogawa T, Suda Y, Kashihara W, Hayashi T, Shimoyama T, Kusumoto S . Immunobiological activities of chemically defined lipid A from Helicobacter pylori LPS in comparison with Porphyromonas gingivalis lipid A and Escherichia coli-type synthetic lipid A (compound 506). Vaccine. 1997; 15(15):1598-605. DOI: 10.1016/s0264-410x(97)00102-3. View

Erridge C, Bennett-Guerrero E, Poxton I . Structure and function of lipopolysaccharides. Microbes Infect. 2002; 4(8):837-51. DOI: 10.1016/s1286-4579(02)01604-0. View

Pulendran B, Kumar P, Cutler C, Mohamadzadeh M, Van Dyke T, Banchereau J . Lipopolysaccharides from distinct pathogens induce different classes of immune responses in vivo. J Immunol. 2001; 167(9):5067-76. PMC: 3739327. DOI: 10.4049/jimmunol.167.9.5067. View

Elin R, Sandberg A, Rosentreich D . Comparison of the pyrogenicity, Limulus activity mitogenicity and complement reactivity of several bacterial endotoxins and related compounds. J Immunol. 1976; 117(4):1238-42. View

10.

Guo X, Liang Y, Zhang Y, Lasorella A, Kee B, Fu Y . Innate Lymphoid Cells Control Early Colonization Resistance against Intestinal Pathogens through ID2-Dependent Regulation of the Microbiota. Immunity. 2015; 42(4):731-43. PMC: 4725053. DOI: 10.1016/j.immuni.2015.03.012. View

11.

Beagley K, Eldridge J, Lee F, Kiyono H, Everson M, Koopman W . Interleukins and IgA synthesis. Human and murine interleukin 6 induce high rate IgA secretion in IgA-committed B cells. J Exp Med. 1989; 169(6):2133-48. PMC: 2189333. DOI: 10.1084/jem.169.6.2133. View

12.

Mathias A, Pais B, Favre L, Benyacoub J, Corthesy B . Role of secretory IgA in the mucosal sensing of commensal bacteria. Gut Microbes. 2014; 5(6):688-95. PMC: 4615909. DOI: 10.4161/19490976.2014.983763. View

13.

Nakayama H, Kurokawa K, Lee B . Lipoproteins in bacteria: structures and biosynthetic pathways. FEBS J. 2012; 279(23):4247-68. DOI: 10.1111/febs.12041. View

14.

Fung T, Bessman N, Hepworth M, Kumar N, Shibata N, Kobuley D . Lymphoid-Tissue-Resident Commensal Bacteria Promote Members of the IL-10 Cytokine Family to Establish Mutualism. Immunity. 2016; 44(3):634-646. PMC: 4845739. DOI: 10.1016/j.immuni.2016.02.019. View

15.

de Waal Malefyt R, Abrams J, Bennett B, Figdor C, De Vries J . Interleukin 10(IL-10) inhibits cytokine synthesis by human monocytes: an autoregulatory role of IL-10 produced by monocytes. J Exp Med. 1991; 174(5):1209-20. PMC: 2119001. DOI: 10.1084/jem.174.5.1209. View

16.

Ivanov I, Atarashi K, Manel N, Brodie E, Shima T, Karaoz U . Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell. 2009; 139(3):485-98. PMC: 2796826. DOI: 10.1016/j.cell.2009.09.033. View

17.

Hooper L, Gordon J . Commensal host-bacterial relationships in the gut. Science. 2001; 292(5519):1115-8. DOI: 10.1126/science.1058709. View

18.

Kunisawa J, Gohda M, Hashimoto E, Ishikawa I, Higuchi M, Suzuki Y . Microbe-dependent CD11b+ IgA+ plasma cells mediate robust early-phase intestinal IgA responses in mice. Nat Commun. 2013; 4:1772. PMC: 3644083. DOI: 10.1038/ncomms2718. View

19.

Atarashi K, Tanoue T, Shima T, Imaoka A, Kuwahara T, Momose Y . Induction of colonic regulatory T cells by indigenous Clostridium species. Science. 2011; 331(6015):337-41. PMC: 3969237. DOI: 10.1126/science.1198469. View

20.

Niwa M, MILNER K, Ribi E, Rudbach J . Alteration of physical, chemical, and biological properties of endotoxin by treatment with mild alkali. J Bacteriol. 1969; 97(3):1069-77. PMC: 249816. DOI: 10.1128/jb.97.3.1069-1077.1969. View