Serotype 3 Streptococcus pneumoniae Escapes the Immune Responses Induced by PCV13 in Mice With High Susceptibility to Infection

IF 3.1 4区医学 Q3 IMMUNOLOGY

Immunity, Inflammation and Disease Pub Date : 2024-12-06 DOI:10.1002/iid3.70062

Giuliana S. Oliveira, Johanna Rivera, Tasson C. Rodrigues, Giovanna B. Carneiro, Orlando G. Ribeiro, Eliane N. Miyaji, Liise-anne Pirofski, Maria Leonor S. Oliveira

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Abstract

Background

Streptococcus pneumoniae (pneumococcus) is a common cause of respiratory and invasive infections in humans. PCV13, a pneumococcal conjugate vaccine used globally, is highly effective against diseases caused by pneumococcal serotypes included in its formulation. However, one of them, the serotype 3 (ST3) is still being relatively commonly isolated from patients, suggesting an escape from vaccine-induced immunity. The thick capsule produced by ST3 facilitates bacterial evasion from the immune system. Additionally, host immune responses may influence the outcome of ST3 infection. Here we evaluated the influence of inflammation in the adaptive immune responses and protection induced by PCV13 against ST3, using two outbred mice lines that were phenotypically selected for high (AIRmax) and low (AIRmin) inflammatory responses.

Methods

AIRmin and AIRmax mice were immunized with PCV13. Inbred BALB/c mice were used as reference for vaccine efficacy. Induction of IgG against polysaccharides (PS) from pneumococcal serotype 1 (ST1) and ST3 were evaluated by ELISA. Protection was tested against invasive infections with ST1 and ST3 pneumococcal strains. Sera were compared by IgG binding to pneumococcal surface, induction of pneumococcal agglutination and opsonophagocytosis. The phagocytic capacity of mice-derived neutrophils was also evaluated.

Results

Immunization of AIRmin, AIRmax and BALB/c mice with PCV13 induced IgG against PS from ST1 and ST3 pneumococci. Despite vaccination, AIRmin mice were not protected against fatal infection with ST3. Sera from AIRmin mice immunized with PCV13 presented lower levels of anti-PS3 IgG, with reduced capacity to bind to pneumococcal surface. Reduced capacity to induce opsonophagocytosis of ST3 pneumococci in vitro was also observed. Conversely, PCV13 protected AIRmin mice against fatal infection with ST1 and this correlated with the capacity of the sera to induce ST1 opsonophagocytosis.

Conclusions

Our results show that both host and bacterial features can influence the outcome of protection induced by PCV13 against ST3 pneumococcal infection.

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血清3型肺炎链球菌逃避PCV13诱导的高易感小鼠免疫应答

背景：肺炎链球菌（肺炎球菌）是人类呼吸道和侵袭性感染的常见原因。PCV13是一种全球使用的肺炎球菌结合疫苗，对其配方中包括的肺炎球菌血清型引起的疾病非常有效。然而，其中一种，血清型3 （ST3）仍然相对普遍地从患者中分离出来，这表明从疫苗诱导的免疫中逃脱。ST3产生的厚胶囊有助于细菌逃避免疫系统。此外，宿主免疫反应可能影响ST3感染的结果。在这里，我们评估了炎症对适应性免疫反应的影响以及PCV13诱导的对ST3的保护作用，使用两种远交种小鼠系，表型上选择高（AIRmax）和低（AIRmin）炎症反应。方法：用PCV13免疫AIRmin和AIRmax小鼠。以近交系BALB/c小鼠为对照，观察疫苗的效力。采用ELISA法观察IgG对1型和3型肺炎球菌多糖（PS）的诱导作用。测试了对ST1和ST3肺炎球菌菌株侵袭性感染的保护作用。比较血清中IgG与肺炎球菌表面的结合、诱导肺炎球菌凝集和调理吞噬作用。小鼠源性中性粒细胞的吞噬能力也被评估。结果：用PCV13免疫AIRmin、AIRmax和BALB/c小鼠可诱导IgG抗ST1和ST3型肺炎球菌的PS。尽管接种了疫苗，但AIRmin小鼠对ST3致命感染没有保护。用PCV13免疫的AIRmin小鼠血清中抗ps3 IgG水平降低，与肺炎球菌表面的结合能力降低。体外还观察到ST3肺炎球菌诱导调理吞噬的能力降低。相反，PCV13保护AIRmin小鼠免受ST1致命感染，这与血清诱导ST1调性噬噬作用的能力相关。结论：我们的研究结果表明，宿主和细菌特征都可以影响PCV13对ST3肺炎球菌感染的保护效果。

本文章由计算机程序翻译，如有差异，请以英文原文为准。

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来源期刊

Immunity, Inflammation and Disease Medicine-Immunology and Allergy

CiteScore

3.60

自引率

0.00%

发文量

146

审稿时长

8 weeks

期刊介绍： Immunity, Inflammation and Disease is a peer-reviewed, open access, interdisciplinary journal providing rapid publication of research across the broad field of immunology. Immunity, Inflammation and Disease gives rapid consideration to papers in all areas of clinical and basic research. The journal is indexed in Medline and the Science Citation Index Expanded (part of Web of Science), among others. It welcomes original work that enhances the understanding of immunology in areas including: • cellular and molecular immunology • clinical immunology • allergy • immunochemistry • immunogenetics • immune signalling • immune development • imaging • mathematical modelling • autoimmunity • transplantation immunology • cancer immunology