Regulating colonic dendritic cells by commensal glycosylated large surface layer protein A to sustain gut homeostasis against pathogenic inflammation.
Animals
Bacterial Proteins
/ genetics
Cell Adhesion Molecules
/ genetics
Cell Differentiation
Cells, Cultured
Colitis
/ chemically induced
Colon
/ immunology
Dendritic Cells
/ immunology
Humans
Inflammatory Bowel Diseases
/ immunology
Lectins, C-Type
/ genetics
Listeria
/ physiology
Listeriosis
/ immunology
Lymphocyte Activation
Mice
Mice, Inbred C57BL
Mice, Knockout
Propionibacterium
/ metabolism
Protein Binding
Receptors, Cell Surface
/ genetics
Symbiosis
T-Lymphocytes
/ immunology
Journal
Mucosal immunology
ISSN: 1935-3456
Titre abrégé: Mucosal Immunol
Pays: United States
ID NLM: 101299742
Informations de publication
Date de publication:
01 2020
01 2020
Historique:
received:
08
07
2019
accepted:
23
09
2019
revised:
30
08
2019
pubmed:
18
10
2019
medline:
8
1
2021
entrez:
18
10
2019
Statut:
ppublish
Résumé
Microbial interaction with the host through sensing receptors, including SIGNR1, sustains intestinal homeostasis against pathogenic inflammation. The newly discovered commensal Propionibacterium strain, P. UF1, regulates the intestinal immunity against pathogen challenge. However, the molecular events driving intestinal phagocytic cell response, including colonic dendritic cells (DCs), by this bacterium are still elusive. Here, we demonstrate that the glycosylation of bacterial large surface layer protein A (LspA) by protein O-mannosyltransferase 1 (Pmt1) regulates the interaction with SIGNR1, resulting in the control of DC transcriptomic and metabolomic machineries. Programmed DCs promote protective T cell response to intestinal Listeria infection and resist chemically induced colitis in mice. Thus, our findings may highlight a novel molecular mechanism by which commensal surface glycosylation interacting with SIGNR1 directs the intestinal homeostasis to potentially protect the host against proinflammatory signals inducing colonic tissue damage.
Identifiants
pubmed: 31619761
doi: 10.1038/s41385-019-0210-0
pii: S1933-0219(22)00239-2
pmc: PMC6917853
mid: NIHMS1540822
doi:
Substances chimiques
Bacterial Proteins
0
Cell Adhesion Molecules
0
DC-specific ICAM-3 grabbing nonintegrin
0
Lectins, C-Type
0
Receptors, Cell Surface
0
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Langues
eng
Sous-ensembles de citation
IM
Pagination
34-46Subventions
Organisme : NIDDK NIH HHS
ID : R01 DK109560
Pays : United States
Organisme : NIH HHS
ID : S10 OD018530
Pays : United States
Références
Littman, D. R. & Pamer, E. G. Role of the commensal microbiota in normal and pathogenic host immune responses. Cell Host Microbe 10, 311–323 (2011).
pubmed: 22018232
pmcid: 3202012
doi: 10.1016/j.chom.2011.10.004
Lathrop, S. K. et al. Peripheral education of the immune system by colonic commensal microbiota. Nature 478, 250–254 (2011).
pubmed: 21937990
pmcid: 3192908
doi: 10.1038/nature10434
Lebeer, S., Vanderleyden, J. & De Keersmaecker, S. C. Host interactions of probiotic bacterial surface molecules: comparison with commensals and pathogens. Nat. Rev. Microbiol 8, 171–184 (2010).
pubmed: 20157338
doi: 10.1038/nrmicro2297
Akira, S., Uematsu, S. & Takeuchi, O. Pathogen recognition and innate immunity. Cell 124, 783–801 (2006).
pubmed: 16497588
doi: 10.1016/j.cell.2006.02.015
Fagan, R. P. & Fairweather, N. F. Biogenesis and functions of bacterial S-layers. Nat. Rev. Microbiol 12, 211–222 (2014).
pubmed: 24509785
doi: 10.1038/nrmicro3213
Thaiss, C. A., Zmora, N., Levy, M. & Elinav, E. The microbiome and innate immunity. Nature 535, 65–74 (2016).
pubmed: 27383981
doi: 10.1038/nature18847
Banchereau, J. & Steinman, R. M. Dendritic cells and the control of immunity. Nature 392, 245–252 (1998).
pubmed: 9521319
doi: 10.1038/32588
Medzhitov, R. Recognition of microorganisms and activation of the immune response. Nature 449, 819–826 (2007).
pubmed: 17943118
doi: 10.1038/nature06246
Colliou, N. et al. Commensal Propionibacterium strain UF1 mitigates intestinal inflammation via Th17 cell regulation. J. Clin. Invest. 127, 3970–3986 (2017).
pubmed: 28945202
pmcid: 5663347
doi: 10.1172/JCI95376
Littman, D. R. & Rudensky, A. Y. Th17 and regulatory T cells in mediating and restraining inflammation. Cell 140, 845–858 (2010).
pubmed: 20303875
doi: 10.1016/j.cell.2010.02.021
Colliou, N. et al. Regulation of Th17 cells by P. UF1 against systemic Listeria monocytogenes infection. Gut Microbes. 279–287 (2018).
pubmed: 29420115
pmcid: 6219594
doi: 10.1080/19490976.2017.1417731
Ge, Y. et al. Neonatal intestinal immune regulation by the commensal bacterium, P. UF1. Mucosal Immunol. 12, 434–444 (2019).
pubmed: 30647410
pmcid: 6375783
doi: 10.1038/s41385-018-0125-1
Lightfoot, Y. L. et al. SIGNR3-dependent immune regulation by Lactobacillus acidophilus surface layer protein A in colitis. EMBO J. 34, 881–895 (2015).
pubmed: 25666591
pmcid: 4388597
doi: 10.15252/embj.201490296
Kordulakova, J. et al. Definition of the first mannosylation step in phosphatidylinositol mannoside synthesis PimA is essential for growth of mycobacteria. J. Biol. Chem. 277, 31335–31344 (2002).
pubmed: 12068013
doi: 10.1074/jbc.M204060200
Tatituri, R. V. et al. Inactivation of Corynebacterium glutamicum NCgl0452 and the role of MgtA in the biosynthesis of a novel mannosylated glycolipid involved in lipomannan biosynthesis. J. Biol. Chem. 282, 4561–4572 (2007).
pubmed: 17179146
doi: 10.1074/jbc.M608695200
Gentzsch, M. & Tanner, W. The PMT gene family: protein O-glycosylation in Saccharomyces cerevisiae is vital. EMBO J. 15, 5752–5759 (1996).
pubmed: 8918452
pmcid: 452322
doi: 10.1002/j.1460-2075.1996.tb00961.x
Herrmann, J. L., OGaora, P., Gallagher, A., Thole, J. E. R. & Young, D. B. Bacterial glycoproteins: A link between glycosylation and proteolytic cleavage of a 19 kDa antigen from Mycobacterium tuberculosis. EMBO J. 15, 3547–3554 (1996).
pubmed: 8670858
pmcid: 451952
doi: 10.1002/j.1460-2075.1996.tb00724.x
Sancho, D. & Reis e Sousa, C. Signaling by myeloid C-type lectin receptors in immunity and homeostasis. Annu. Rev. Immunol. 30, 491–529 (2012).
pubmed: 22224766
pmcid: 4480235
doi: 10.1146/annurev-immunol-031210-101352
Bekiaris, V., Persson, E. K. & Agace, W. W. Intestinal dendritic cells in the regulation of mucosal immunity. Immunol. Rev. 260, 86–101 (2014).
pubmed: 24942684
doi: 10.1111/imr.12194
Schlitzer, A. et al. IRF4 transcription factor-dependent CD11b+ dendritic cells in human and mouse control mucosal IL-17 cytokine responses. Immunity 38, 970–983 (2013).
pubmed: 23706669
pmcid: 3666057
doi: 10.1016/j.immuni.2013.04.011
Price, J. G. et al. CDKN1A regulates Langerhans cell survival and promotes Treg cell generation upon exposure to ionizing irradiation. Nat. Immunol. 16, 1060–1068 (2015).
pubmed: 26343536
pmcid: 4620552
doi: 10.1038/ni.3270
Cohen, N. et al. GILZ expression in human dendritic cells redirects their maturation and prevents antigen-specific T lymphocyte response. Blood 107, 2037–2044 (2006).
pubmed: 16293609
doi: 10.1182/blood-2005-07-2760
Liu, J. N. et al. The complement inhibitory protein DAF (CD55) suppresses T cell immunity in vivo. J. Exp. Med. 201, 567–577 (2005).
pubmed: 15710649
pmcid: 2213052
doi: 10.1084/jem.20040863
Niess, J. H. & Reinecker, H. C. Lamina propria dendritic cells in the physiology and pathology of the gastrointestinal tract. Curr. Opin. Gastroenterol. 21, 687–691 (2005).
pubmed: 16220046
doi: 10.1097/01.mog.0000181710.96904.58
Rescigno, M. & Di Sabatino, A. Dendritic cells in intestinal homeostasis and disease. J. Clin. Invest. 119, 2441–2450 (2009).
pubmed: 19729841
pmcid: 2735931
doi: 10.1172/JCI39134
Dalod, M., Chelbi, R., Malissen, B. & Lawrence, T. Dendritic cell maturation: functional specialization through signaling specificity and transcriptional programming. EMBO J. 33, 1104–1116 (2014).
pubmed: 24737868
pmcid: 4193918
doi: 10.1002/embj.201488027
Everts, B. et al. Commitment to glycolysis sustains survival of NO-producing inflammatory dendritic cells. Blood 120, 1422–1431 (2012).
pubmed: 22786879
pmcid: 3423780
doi: 10.1182/blood-2012-03-419747
Pearce, E. J. & Everts, B. Dendritic cell metabolism. Nat. Rev. Immunol. 15, 18–29 (2015).
pubmed: 25534620
pmcid: 4495583
doi: 10.1038/nri3771
Sahu, N. et al. Proline starvation induces unresolved ER stress and hinders mTORC1-dependent tumorigenesis. Cell Metab. 24, 753–761 (2016).
pubmed: 27618686
doi: 10.1016/j.cmet.2016.08.008
Tang, C. et al. Suppression of IL-17F, but not of IL-17A, provides protection against colitis by inducing Treg cells through modification of the intestinal microbiota. Nat. Immunol. 19, 755–765 (2018).
pubmed: 29915298
doi: 10.1038/s41590-018-0134-y
Lee, J. S. et al. Interleukin-23-independent IL-17 production regulates intestinal epithelial permeability. Immunity 43, 727–738 (2015).
pubmed: 26431948
pmcid: 6044435
doi: 10.1016/j.immuni.2015.09.003
Verma, R. et al. Cell surface polysaccharides of Bifidobacterium bifidum induce the generation of Foxp3(+) regulatory T cells. Sci. Immunol. 3, eaat6975 (2018).
pubmed: 30341145
doi: 10.1126/sciimmunol.aat6975
Kamada, N., Seo, S. U., Chen, G. Y. & Nunez, G. Role of the gut microbiota in immunity and inflammatory disease. Nat. Rev. Immunol. 13, 321–335 (2013).
pubmed: 23618829
doi: 10.1038/nri3430
Deutsch, S. M. et al. Identification of proteins involved in the anti-inflammatory properties of Propionibacterium freudenreichii by means of a multi-strain study. Sci. Rep. 7, 46409 (2017).
pubmed: 28406170
pmcid: 5390290
doi: 10.1038/srep46409
Le Marechal, C. et al. Surface proteins of Propionibacterium freudenreichii are involved in its anti-inflammatory properties. J. Proteom. 113, 447–461 (2015).
doi: 10.1016/j.jprot.2014.07.018
do Carmo, F. L. R. et al. Extractable bacterial surface proteins in probiotic-host interaction. Front. Microbiol. 9, 645 (2018).
pubmed: 29670603
pmcid: 5893755
doi: 10.3389/fmicb.2018.00645
do Carmo, F. L. R. et al. Propionibacterium freudenreichii surface protein SlpB is involved in adhesion to intestinal HT-29 cells. Front. Microbiol. 8, 1033 (2017).
pubmed: 28642747
pmcid: 5462946
doi: 10.3389/fmicb.2017.01033
Michon, C., Langella, P., Eijsink, V. G., Mathiesen, G. & Chatel, J. M. Display of recombinant proteins at the surface of lactic acid bacteria: strategies and applications. Micro. Cell Fact. 15, 70 (2016).
doi: 10.1186/s12934-016-0468-9
Ewing, C. P., Andreishcheva, E. & Guerry, P. Functional characterization of flagellin glycosylation in Campylobacter jejuni 81-176. J. Bacteriol. 191, 7086–7093 (2009).
pubmed: 19749047
pmcid: 2772469
doi: 10.1128/JB.00378-09
Nothaft, H. & Szymanski, C. M. Protein glycosylation in bacteria: sweeter than ever. Nat. Rev. Microbiol. 8, 765–778 (2010).
pubmed: 20948550
doi: 10.1038/nrmicro2383
Liu, C. F. et al. Bacterial protein-O-mannosylating enzyme is crucial for virulence of Mycobacterium tuberculosis. Proc. Natl Acad. Sci. USA 110, 6560–6565 (2013).
pubmed: 23550160
pmcid: 3631654
doi: 10.1073/pnas.1219704110
Girrbach, V. & Strahl, S. Members of the evolutionarily conserved PMT family of protein O-mannosyltransferases form distinct protein complexes among themselves. J. Biol. Chem. 278, 12554–12562 (2003).
pubmed: 12551906
doi: 10.1074/jbc.M212582200
Geijtenbeek, T. B. & Gringhuis, S. I. C-type lectin receptors in the control of T helper cell differentiation. Nat. Rev. Immunol. 16, 433–448 (2016).
pubmed: 27291962
doi: 10.1038/nri.2016.55
Zhou, Y. et al. Oral tolerance to food-induced systemic anaphylaxis mediated by the C-type lectin SIGNR1. Nat. Med. 16, 1128–1133 (2010).
pubmed: 20835248
pmcid: 3058254
doi: 10.1038/nm.2201
Lanoue, A. et al. SIGN-R1 contributes to protection against lethal pneumococcal infection in mice. J. Exp. Med. 200, 1383–1393 (2004).
pubmed: 15583012
pmcid: 2211941
doi: 10.1084/jem.20040795
Song, X. et al. Growth factor FGF2 cooperates with interleukin-17 to repair intestinal epithelial damage. Immunity 43, 488–501 (2015).
pubmed: 26320657
doi: 10.1016/j.immuni.2015.06.024
Kreisman, L. S. & Cobb, B. A. Infection, inflammation and host carbohydrates: a Glyco-Evasion Hypothesis. Glycobiology 22, 1019–1030 (2012).
pubmed: 22492234
pmcid: 3382345
doi: 10.1093/glycob/cws070
Dewald, J. H., Colomb, F., Bobowski-Gerard, M., Groux-Degroote, S., Delannoy, P. Role of cytokine-induced glycosylation changes in regulating cell interactions and cell signaling in inflammatory diseases and cancer. Cells 5, 43 (2016).
pmcid: 5187527
doi: 10.3390/cells5040043
Gevers, D. et al. The treatment-naive microbiome in new-onset Crohn’s disease. Cell Host Microbe 15, 382–392 (2014).
pubmed: 24629344
pmcid: 4059512
doi: 10.1016/j.chom.2014.02.005
Shreiner, A. B., Kao, J. Y. & Young, V. B. The gut microbiome in health and in disease. Curr. Opin. Gastroenterol. 31, 69–75 (2015).
pubmed: 25394236
pmcid: 4290017
doi: 10.1097/MOG.0000000000000139
Kaplan, G. G. The global burden of IBD: from 2015 to 2025. Nat. Rev. Gastroenterol. Hepatol. 12, 720–727 (2015).
pubmed: 26323879
doi: 10.1038/nrgastro.2015.150
Li, W. et al. Targeting T cell activation and lupus autoimmune phenotypes by inhibiting glucose transporters. Front Immunol. 10, 833 (2019).
pubmed: 31057554
pmcid: 6478810
doi: 10.3389/fimmu.2019.00833