The B-cell inhibitory receptor CD22 is a major factor in host resistance to Streptococcus pneumoniae infection
Autoři:
Vitor E. Fernandes aff001; Giuseppe Ercoli aff002; Alan Bénard aff003; Carolin Brandl aff004; Hannah Fahnenstiel aff004; Jennifer Müller-Winkler aff004; Georg F. Weber aff003; Paul Denny aff005; Lars Nitschke aff004; Peter W. Andrew aff001
Působiště autorů:
Department of Infection, Immunity and Inflammation, University of Leicester, Leicester, United Kingdom
aff001; Department of Genetics, University of Leicester, Leicester, United Kingdom
aff002; Department of Surgery, University Hospital Erlangen, Erlangen, Germany
aff003; Division of Genetics, Department of Biology, University of Erlangen, Erlangen, Germany
aff004; Mammalian Genetics Unit, Medical Research Council, Harwell, United Kingdom
aff005
Vyšlo v časopise:
The B-cell inhibitory receptor CD22 is a major factor in host resistance to Streptococcus pneumoniae infection. PLoS Pathog 16(4): e32767. doi:10.1371/journal.ppat.1008464
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.ppat.1008464
Souhrn
Streptococcus pneumoniae is a major human pathogen, causing pneumonia and sepsis. Genetic components strongly influence host responses to pneumococcal infections, but the responsible loci are unknown. We have previously identified a locus on mouse chromosome 7 from a susceptible mouse strain, CBA/Ca, to be crucial for pneumococcal infection. Here we identify a responsible gene, Cd22, which carries a point mutation in the CBA/Ca strain, leading to loss of CD22 on B cells. CBA/Ca mice and gene-targeted CD22-deficient mice on a C57BL/6 background are both similarly susceptible to pneumococcal infection, as shown by bacterial replication in the lungs, high bacteremia and early death. After bacterial infections, CD22-deficient mice had strongly reduced B cell populations in the lung, including GM-CSF producing, IgM secreting innate response activator B cells, which are crucial for protection. This study provides striking evidence that CD22 is crucial for protection during invasive pneumococcal disease.
Klíčová slova:
B cells – Blood – Escherichia coli infections – Genetic loci – Pneumococcus – Respiratory infections – Spleen – Streptococcal infections
Zdroje
1. Gingles NA, Alexander JE, Kadioglu A, Andrew PW, Kerr A, Mitchell TJ, et al. Role of genetic resistance in invasive pneumococcal infection: identification and study of susceptibility and resistance in inbred mouse strains. Infect Immun. 2001;69(1):426–34. doi: 10.1128/IAI.69.1.426-434.2001 11119534; PubMed Central PMCID: PMC97900.
2. Denny P, Hopes E, Gingles N, Broman KW, McPheat W, Morten J, et al. A major locus conferring susceptibility to infection by Streptococcus pneumoniae in mice. Mamm Genome. 2003;14(7):448–53. doi: 10.1007/s00335-002-2261-9 12925893.
3. Jonczyk MS, Simon M, Kumar S, Fernandes VE, Sylvius N, Mallon AM, et al. Genetic factors regulating lung vasculature and immune cell functions associate with resistance to pneumococcal infection. PLoS One. 2014;9(3):e89831. doi: 10.1371/journal.pone.0089831 24594938; PubMed Central PMCID: PMC3940657.
4. Crocker PR, Paulson JC, Varki A. Siglecs and their roles in the immune system. Nat Rev Immunol. 2007;7(4):255–66. doi: 10.1038/nri2056 17380156.
5. Müller J, Nitschke L. The role of CD22 and Siglec-G in B-cell tolerance and autoimmune disease. Nat Rev Rheumatol. 2014;10(7):422–8. Epub 2014/04/26. nrrheum.2014.54 [pii] doi: 10.1038/nrrheum.2014.54 24763061
6. Nitschke L. CD22 and Siglec-G regulate inhibition of B-cell signaling by sialic acid ligand binding and control B-cell tolerance. Glycobiology. 2014;24(9):807–17. Epub 2014/07/09. cwu066 [pii] doi: 10.1093/glycob/cwu066 25002414
7. van der Merwe PA, Crocker PR, Vinson M, Barclay AN, Schauer R, Kelm S. Localization of the putative sialic acid-binding site on the immunoglobulin superfamily cell-surface molecule CD22. J Biol Chem. 1996;271(16):9273–80. 8621588
8. Wen T, Mingler MK, Blanchard C, Wahl B, Pabst O, Rothenberg ME. The pan-B cell marker CD22 is expressed on gastrointestinal eosinophils and negatively regulates tissue eosinophilia. J Immunol. 2012;188(3):1075–82. Epub 2011/12/23. jimmunol.1102222 [pii] doi: 10.4049/jimmunol.1102222 22190185; PubMed Central PMCID: PMC3262961.
9. Nitschke L, Carsetti R, Ocker B, Kohler G, Lamers MC. CD22 is a negative regulator of B-cell receptor signalling. Curr Biol. 1997;7(2):133–43. doi: 10.1016/s0960-9822(06)00057-1 9016707
10. O'Keefe TL, Williams GT, Davies SL, Neuberger MS. Hyperresponsive B cells in CD22-deficient mice. Science. 1996;274(5288):798–801. doi: 10.1126/science.274.5288.798 8864124
11. Otipoby KL, Andersson KB, Draves KE, Klaus SJ, Farr AG, Kerner JD, et al. CD22 regulates thymus-independent responses and the lifespan of B cells. Nature. 1996;384(6610):634–7. doi: 10.1038/384634a0 8967951
12. Sato S, Miller AS, Inaoki M, Bock CB, Jansen PJ, Tang ML, et al. CD22 is both a positive and negative regulator of B lymphocyte antigen receptor signal transduction: altered signaling in CD22-deficient mice. Immunity. 1996;5(6):551–62. doi: 10.1016/s1074-7613(00)80270-8 8986715
13. Weber GF, Chousterman BG, Hilgendorf I, Robbins CS, Theurl I, Gerhardt LM, et al. Pleural innate response activator B cells protect against pneumonia via a GM-CSF-IgM axis. J Exp Med. 2014;211(6):1243–56. doi: 10.1084/jem.20131471 24821911; PubMed Central PMCID: PMC4042649.
14. Becher B, Tugues S, Greter M. GM-CSF: From Growth Factor to Central Mediator of Tissue Inflammation. Immunity. 2016;45(5):963–73. doi: 10.1016/j.immuni.2016.10.026 27851925.
15. Baumgarth N. The double life of a B-1 cell: self-reactivity selects for protective effector functions. Nat Rev Immunol. 2011;11(1):34–46. Epub 2010/12/15. nri2901 [pii] doi: 10.1038/nri2901 21151033.
16. Haas KM, Poe JC, Steeber DA, Tedder TF. B-1a and B-1b cells exhibit distinct developmental requirements and have unique functional roles in innate and adaptive immunity to S. pneumoniae. Immunity. 2005;23(1):7–18. doi: 10.1016/j.immuni.2005.04.011 16039575.
17. Haas KM, Johnson KL, Phipps JP, Do C. CD22 Promotes B-1b Cell Responses to T Cell-Independent Type 2 Antigens. J Immunol. 2018;200(5):1671–81. doi: 10.4049/jimmunol.1701578 29374074; PubMed Central PMCID: PMC5821584.
18. Samardzic T, Marinkovic D, Danzer CP, Gerlach J, Nitschke L, Wirth T. Reduction of marginal zone B cells in CD22-deficient mice. Eur J Immunol. 2002;32(2):561–7. doi: 10.1002/1521-4141(200202)32:2<561::AID-IMMU561>3.0.CO;2-H 11828373
19. Jellusova J, Wellmann U, Amann K, Winkler TH, Nitschke L. CD22 x Siglec-G double-deficient mice have massively increased B1 cell numbers and develop systemic autoimmunity. J Immunol. 2010;184(7):3618–27. Epub 2010/03/05. jimmunol.0902711 [pii] doi: 10.4049/jimmunol.0902711 20200274.
20. O'Keefe TL, Williams GT, Batista FD, Neuberger MS. Deficiency in CD22, a B cell-specific inhibitory receptor, is sufficient to predispose to development of high affinity autoantibodies. J Exp Med. 1999;189(8):1307–13. doi: 10.1084/jem.189.8.1307 10209047
21. Gjertsson I, Nitschke L, Tarkowski A. The role of B cell CD22 expression in Staphylococcus aureus arthritis and sepsis. Microbes Infect. 2004;6(4):377–82. doi: 10.1016/j.micinf.2003.12.013 15050965.
22. Ma DY, Suthar MS, Kasahara S, Gale M Jr., Clark EA. CD22 is required for protection against West Nile virus Infection. J Virol. 2013;87(6):3361–75. Epub 2013/01/11. JVI.02368-12 [pii] doi: 10.1128/JVI.02368-12 23302871; PubMed Central PMCID: PMC3592166.
23. Müller J, Obermeier I, Wohner M, Brandl C, Mrotzek S, Angermuller S, et al. CD22 ligand-binding and signaling domains reciprocally regulate B-cell Ca2+ signaling. Proc Natl Acad Sci U S A. 2013;110(30):12402–7. Epub 2013/07/10. 1304888110 [pii] doi: 10.1073/pnas.1304888110 23836650; PubMed Central PMCID: PMC3725054.
24. Chapman SJ, Khor CC, Vannberg FO, Rautanen A, Segal S, Moore CE, et al. NFKBIZ polymorphisms and susceptibility to pneumococcal disease in European and African populations. Genes Immun. 2010;11(4):319–25. doi: 10.1038/gene.2009.76 19798075; PubMed Central PMCID: PMC3051152.
25. Ferwerda B, Valls Seron M, Jongejan A, Zwinderman AH, Geldhoff M, van der Ende A, et al. Variation of 46 Innate Immune Genes Evaluated for their Contribution in Pneumococcal Meningitis Susceptibility and Outcome. EBioMedicine. 2016;10:77–84. doi: 10.1016/j.ebiom.2016.07.011 27432718; PubMed Central PMCID: PMC5006661.
26. Lingappa JR, Dumitrescu L, Zimmer SM, Lynfield R, McNicholl JM, Messonnier NE, et al. Identifying host genetic risk factors in the context of public health surveillance for invasive pneumococcal disease. PLoS One. 2011;6(8):e23413. doi: 10.1371/journal.pone.0023413 21858107; PubMed Central PMCID: PMC3156135.
27. Lander ES, Schork NJ. Genetic dissection of complex traits. Science. 1994;265(5181):2037–48. doi: 10.1126/science.8091226 8091226.
28. Kadioglu A, Gingles NA, Grattan K, Kerr A, Mitchell TJ, Andrew PW. Host cellular immune response to pneumococcal lung infection in mice. Infect Immun. 2000;68(2):492–501. doi: 10.1128/iai.68.2.492-501.2000 10639409; PubMed Central PMCID: PMC97168.
29. Morton DB, Griffiths PH. Guidelines on the recognition of pain, distress and discomfort in experimental animals and an hypothesis for assessment. Vet Rec. 1985;116(16):431–6. doi: 10.1136/vr.116.16.431 3923690.
30. Rauch PJ, Chudnovskiy A, Robbins CS, Weber GF, Etzrodt M, Hilgendorf I, et al. Innate response activator B cells protect against microbial sepsis. Science. 2012;335(6068):597–601. doi: 10.1126/science.1215173 22245738; PubMed Central PMCID: PMC3279743.
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