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http://dx.doi.org/10.4014/jmb.2103.03053

IL-17A Secreted by Th17 Cells Is Essential for the Host against Streptococcus agalactiae Infections  

Chen, Jing (College of Animal Science and Veterinary Medicine, Heilongjiang Bayi Agricultural University)
Yang, Siyu (College of Life Science and Technology, Heilongjiang Bayi Agricultural University)
Li, Wanyu (College of Life Science and Technology, Heilongjiang Bayi Agricultural University)
Yu, Wei (College of Life Science and Technology, Heilongjiang Bayi Agricultural University)
Fan, Zhaowei (College of Life Science and Technology, Heilongjiang Bayi Agricultural University)
Wang, Mengyao (College of Life Science and Technology, Heilongjiang Bayi Agricultural University)
Feng, Zhenyue (College of Life Science and Technology, Heilongjiang Bayi Agricultural University)
Tong, Chunyu (College of Life Science and Technology, Heilongjiang Bayi Agricultural University)
Song, Baifen (College of Life Science and Technology, Heilongjiang Bayi Agricultural University)
Ma, Jinzhu (College of Life Science and Technology, Heilongjiang Bayi Agricultural University)
Cui, Yudong (College of Animal Science and Veterinary Medicine, Heilongjiang Bayi Agricultural University)
Publication Information
Journal of Microbiology and Biotechnology / v.31, no.5, 2021 , pp. 667-675 More about this Journal
Abstract
Streptococcus agalactiae is an important bacterial pathogen and causative agent of diseases including neonatal sepsis and meningitis, as well as infections in healthy adults and pregnant women. Although antibiotic treatments effectively relieve symptoms, the emergence and transmission of multidrug-resistant strains indicate the need for an effective immunotherapy. Effector T helper (Th) 17 cells are a relatively newly discovered subpopulation of helper CD4+ T lymphocytes, and which, by expressing interleukin (IL)-17A, play crucial roles in host defenses against a variety of pathogens, including bacteria and viruses. However, whether S. agalactiae infection can induce the differentiation of CD4+ T cells into Th17 cells, and whether IL-17A can play an effective role against S. agalactiae infections, are still unclear. In this study, we analyzed the responses of CD4+ T cells and their defensive effects after S. agalactiae infection. The results showed that S. agalactiae infection induces not only the formation of Th1 cells expressing interferon (IFN)-γ, but also the differentiation of mouse splenic CD4+ T cells into Th17 cells, which highly express IL-17A. In addition, the bacterial load of S. agalactiae was significantly increased and decreased in organs as determined by antibody neutralization and IL-17A addition experiments, respectively. The results confirmed that IL-17A is required by the host to defend against S. agalactiae and that it plays an important role in effectively eliminating S. agalactiae. Our findings therefore prompt us to adopt effective methods to regulate the expression of IL-17A as a potent strategy for the prevention and treatment of S. agalactiae infection.
Keywords
Streptococcus agalactiae; T helper 17 cells; interleukin-17A;
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1 Veldhoen M, Hocking RJ, Atkins CJ, Locksley RM, Stockinger B. 2006. TGFbeta in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 24: 179-189.   DOI
2 Wang B, Dileepan T, Briscoe S, Hyland KA, Kang J, Khoruts A, et al. 2010. Induction of TGF-beta1 and TGF-beta1-dependent predominant Th17 differentiation by group A streptococcal infection. Proc. Natl. Acad. Sci. USA. 107: 5937-5942.   DOI
3 Yildirim AO, Lammler C, Weiss R, Kopp P. 2002. Pheno- and genotypic properties of streptococci of serological group B of canine and feline origin. FEMS Microbiol. Lett. 212: 187-192.   DOI
4 Fooksman DR. 2014. Organizing MHC Class II Presentation. Front. Immunol. 5: 158.   DOI
5 Elliott JA, Facklam RR, Richter CB. 1990. Whole-cell protein patterns of nonhemolytic group B, type Ib, streptococci isolated from humans, mice, cattle, frogs, and fish. J. Clin. Microbiol. 28: 628-630.   DOI
6 Mian GF, Godoy DT, Leal CA, Yuhara TY, Costa GM, Figueiredo HCP. 2009. Aspects of the natural history and virulence of S. agalactiae infection in Nile tilapia. Vet. Microbiol. 136: 180-183.   DOI
7 Raabe VN, Shane AL. 2019. Group B Streptococcus (Streptococcus agalactiae). Microbiol. Spectr. 7: 10.1128/microbiolspec.GPP3-0007-2018.   DOI
8 Rosen GH, Randis TM, Desai PV, Sapra KJ, Ma B, Gajer P, et al. 2017. Group B Streptococcus and the vaginal microbiota. J. Infect. Dis. 216: 744-751.   DOI
9 McGeachy MJ, Bak-Jensen KS, Chen Y, Tato CM, Blumenschein W, McClanahan T, et al. 2007. TGF-beta and IL-6 drive the production of IL-17 and IL-10 by T cells and restrain T(H)-17 cell-mediated pathology. Nat. Immunol. 8: 1390-1397.   DOI
10 Mangan PR, Harrington LE, O'Quinn DB, helms WS, Bullard DC,Elson Co, et al. 2006. Transforming growth factor-beta induces development of the T(H)17 lineage. Nature 441: 231-234.   DOI
11 Conti HR, Gaffen SL. 2015. IL-17-Mediated immunity to the opportunistic fungal pathogen Candida albicans. J. Immunol. 195: 780-788.   DOI
12 Yu W, Yao D, Yu S, Wang X, Li X, Wang M, et al. 2018. Protective humoral and CD4+ T cellular immune responses of Staphylococcus aureus vaccine MntC in a murine peritonitis model. Sci. Rep. 8: 3580.   DOI
13 Bai H, Cheng J, Gao X, Joyee AG, Fan Y, Wang S, et al. 2009. IL-17/Th17 promotes type 1 T cell immunity against pulmonary intracellular bacterial infection through modulating dendritic cell function. J. Immunol. 183: 5886-5895.   DOI
14 Zhang X, Gao L, Lei L, Zhong Y, Dube P, Berton MT, et al. 2009. A MyD88-dependent early IL-17 production protects mice against airway infection with the obligate intracellular pathogen Chlamydia muridarum. J. Immunol. 183: 1291-300.   DOI
15 Gao J, Barkema HW, Zhang L, Liu G, Deng Z, Cai L, et al. 2017. Incidence of clinical mastitis and distribution of pathogens on large Chinese dairy farms. J. Dairy Sci. 100: 4797-4806.   DOI
16 Lin JS, Kummer LW, Szaba FM, Smiley ST. 2011. IL-17 contributes to cell-mediated defense against pulmonary Yersinia pestis infection. J. Immunol. 186: 1675-1684.   DOI
17 Beringer A, Noack M, Miossec P. 2016. IL-17 in chronic inflammation: from discovery to targeting. Trends Mol. Med. 22: 230-241.   DOI
18 Zelante T, De Luca A, Bonifazi P, Montagnoli C, Bozza S, Moretti S, et al. 2007. IL-23 and the Th17 pathway promote inflammation and impair antifungal immune resistance. Eur. J. Immunol. 37: 2695-2706.   DOI
19 Hogeveen H, Huijps K, Lam TJ. 2011. Economic aspects of mastitis: new developments. NZ Vet. J. 59: 16-23.   DOI
20 Keefe GP. 1997. Streptococcus agalactiae mastitis: a review. Can. Vet. J. 38: 429-437.
21 Manning SD, Springman AC, Million AD, Millton NR, McNamara SE, Somsel PA, et al. 2010. Association of Group B Streptococcus colonization and bovine exposure: a prospective cross-sectional cohort study. PLoS One 5: e8795.   DOI
22 Sendi P, Johansson L, Norrby-Teglund A. 2008. Invasive group B Streptococcal disease in non-pregnant adults : a review with emphasis on skin and soft-tissue infections. Infection 36: 100-111.   DOI
23 Cobo-Angel CG, Jaramillo-Jaramillo AS, Palacio-Aguilera M, Jurado-Vargas L, Calvo-Villegas EA, Ospina-Loaiza DA, et al. 2019. Potential group B Streptococcus interspecies transmission between cattle and people in Colombian dairy farms. Sci. Rep. 9: 14025.   DOI
24 Longtin J, Vermeiren C, Shahinas D, Tamber GS, McGeer A, Low DE, et al. 2011. Novel mutations in a patient isolate of Streptococcus agalactiae with reduced penicillin susceptibility emerging after long-term oral suppressive therapy. Antimicrob. Agents Chemother. 55: 2983-2985.   DOI
25 Teti G, Mancuso G, Tomasello F. 1993. Cytokine appearance and effects of anti-tumor necrosis factor alpha antibodies in a neonatal rat model of group B streptococcal infection. Infect. Immun. 61: 227-235.   DOI
26 Arachchi PS, Fernando N, Weerasekera MM, Senevirathna B, Weerasekera DD, Gunasekara CP. 2017. Proinflammatory cytokine IL-17 shows a significant association with Helicobacter pylori infection and disease severity. Gastroenterol. Res. Pract. 2017: 6265150.
27 Clarke D, Letendre C, Lecours MP, Lemire P, Galbas T, Thibodeau J, et al. 2016. Group B Streptococcus induces a rbust IFN-gamma response by CD4(+) T cells in an In Vitro and In Vivo model. J. Immunol. Res. 2016: 5290604.   DOI
28 Al Sweih N, Mokaddas E, Jamal W, Phillips OA, Rotimi VO. 2005. In vitro activity of linezolid and other antibiotics against Grampositive bacteria from the major teaching hospitals in Kuwait. J. Chemother. 17: 607-613.   DOI
29 Doran KS, Nizet V. 2004. Molecular pathogenesis of neonatal group B streptococcal infection: no longer in its infancy. Mol. Microbiol. 54: 23-31.   DOI
30 Lu YJ, Gross J, Bogaert D, Finn A, Bagrase L, Zhang Q, et al. 2008. Interleukin-17A mediates acquired immunity to pneumococcal colonization, PLoS Pathog. 4: e1000159.   DOI
31 Kimura K, Matsubara K, Yamamoto G, Shibayama K, Arakawa Y. 2013. Active screening of group B streptococci with reduced penicillin susceptibility and altered serotype distribution isolated from pregnant women in Kobe, Japan. Jpn. J. Infect. Dis. 66: 158-160.   DOI
32 Zielinski CE, Mele F, Aschenbrenner D, Jarrossay D, Ronchi F, Gattorno M, et al. 2012. Pathogen-induced human TH17 cells produce IFN-gamma or IL-10 and are regulated by IL-1beta. Nature 484: 514-518.   DOI
33 Bettelli E, Korn T, Kuchroo VK. 2007. Th17: the third member of the effector T cell trilogy. Curr. Opin. Immunol. 19: 652-657.   DOI
34 Cusumano V, Mancuso G, Genovese F, Delfino D, Beninati E, Losi E, et al. 1996. Role of gamma interferon in a neonatal mouse model of group B streptococcal disease. Infect. Immun. 64: 2941-2944.   DOI
35 Walsh KP, Mills KH. 2013. Dendritic cells and other innate determinants of T helper cell polarisation. Trends Immunol. 34: 521-530.   DOI
36 KornT, Bettelli E, Oukka M, Kuchroo VK. 2009. IL-17 and Th17 Cells, Annu Rev. Immunol. 27: 485-517.   DOI
37 Yasuda K, Takeuchi Y, Hirota K. 2019. The pathogenicity of Th17 cells in autoimmune diseases. Semin. Immunopathol. 41: 283-297.   DOI
38 Ishigame H, Kakuta S, Nagai T, Kadoki M, Nam,bu A, Komiyama Y, et al. 2009. Differential roles of interleukin-17A and -17F in host defense against mucoepithelial bacterial infection and allergic responses. Immunity 30: 108-119.   DOI
39 Chai LY, van de Veerdonk F, Marijnissen RJ, Cheng S-C, Khoo AL, Hectors M, et al. 2010. Anti-aspergillus human host defence relies on type 1 T helper (Th1), rather than type 17 T helper (Th17), cellular immunity. Immunology 130: 46-54.   DOI
40 Li Y, Wei C, Xu H, Jia J, Wei X, Gou R, et al. 2018. The immunoregulation of Th17 in host against intracellular bacterial infection, Mediators Inflamm. 2018: 6587296.   DOI
41 Kagami S, Rizzo HL, Kurtz SE, Miller LS, Blauvelt A. 2010, IL-23 and IL-17A, but not IL-12 and IL-22, are required for optimal skin host defense against Candida albicans. J. Immunol. 185: 5453-5462.   DOI
42 Ye P, Garvey PB, Zhang P, Nelson S, Bagby G, Summer WR, et al. 2001. Interleukin-17 and lung host defense against Klebsiella pneumoniae infection. Am. J. Respir. Cell Mol. Biol. 25: 335-340.   DOI
43 Ziegler SF, Ramsdell F, Alderson MR. 1994. The activation antigen CD69. Stem Cells 12: 456-465.   DOI
44 Szulc-Dabrowska L, Gierynska M, Depczynska D, Schollenberger A, Toka FN. 2015. [Th17 lymphocytes in bacterial infections], Postepy Hig. Med. Dosw. (Online). 69: 398-417.   DOI
45 Pitts SI, Maruthur NM, Langley GE, Pondo T, Shutt KA, Hollick R, et al. 2018. Obesity, diabetes, and the risk of invasive group B Streptococcal disease in nonpregnant adults in the United States. Open Forum Infect. Dis. 5: ofy030.   DOI
46 Melin P. 2011. Neonatal group B streptococcal disease: from pathogenesis to preventive strategies. Clin. Microbiol. Infect. 17: 1294-1303.   DOI
47 Edmond KM, Kortsalioudaki C, Scott S, Schraf SJ, Zaidi AKM, Cousens S, et al. 2012. Group B streptococcal disease in infants aged younger than 3 months: systematic review and meta-analysis. Lancet 379: 547-556.   DOI
48 Seale AC, Blencowe H, Bianchi-Jassir F, Embleton N, Bassat Q, Ordi J, et al. 2017. Stillbirth with group B Streptococcus disease worldwide: systematic review and meta-analyses. Clin. Infect. Dis. 65(suppl_2): S125-S132.   DOI
49 Francois Watkins LK, McGee L, Schrag SJ, Bella B, Jian JH, Pondo T, et al. 2019. Epidemiology of invasive group B Streptococcal infections among nonpregnant adults in the United States. 2008-2016. JAMA Intern. Med.179: 479-488.   DOI
50 Randis TM, Baker JA, Ratner AJ. 2017. Group B Streptococcal infections. Pediatr. Rev. 38: 254-262.   DOI
51 Le Doare K, Heath PT. 2013. An overview of global GBS epidemiology. Vaccine 31 Suppl 4: D7-12.   DOI
52 Khan MA, Faiz A, Ashshi AM. 2015. Maternal colonization of group B streptococcus: prevalence, associated factors and antimicrobial resistance. Ann. Saudi Med. 35: 423-427.   DOI
53 Bettelli E, Carrier Y, Gao W, Korn T, Strom TB, Oukka M, et al. 2006. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441: 235-238.   DOI
54 Yang L, Anderson DE, Baecher-Allan C, Hastings WD, Bettelli E, Oukka M, et al. 2008. IL-21 and TGF-beta are required for differentiation of human T(H)17 cells. Nature 454: 350-352.   DOI