|
肺炎链球菌表面蛋白逃避补体系统介导的免疫反应机制的研究进展
|
Abstract:
尽管抗生素及疫苗的使用降低了肺炎链球菌肺炎的发病率及病死率,肺炎链球菌性疾病仍然是全球5岁以下儿童感染和死亡的常见原因。补体系统对肺炎链球菌的免疫防御相关研究众多,研究表明肺炎球菌表面蛋白在限制补体介导的免疫系统的溶菌过程和吞噬过程中发挥了重要的作用。本文综述了肺炎链球菌表面蛋白为逃避机体补体系统介导的免疫反应的机制,为后续相关研究开展提供借鉴。
The widespread use of antibiotics and vaccines has reduced the incidence and mortality of Streptococcus pneumonia, yet, pneumococcal disease remains a common cause of infection and death in children under 5 years old. Studies related to the immune defense of the complement system against streptococcus pneumoniae are numbered, and show that pneumococcal surface proteins play an important role in limiting complement mediated opsonization and phagocytosis of the immune system. This review focuses on the mechanism of Streptococcus pneumoniae surface proteins evading the immune response mediated by the complement system, providing a reference for the future related research.
[1] | Geno, K.A., Gilbert, G.L., Song, J.Y., Skovsted, I.C., Klugman, K.P., Jones, C., et al. (2015) Pneumococcal Capsules and Their Types: Past, Present, and Future. Clinical Microbiology Reviews, 28, 871-899. https://doi.org/10.1128/cmr.00024-15 |
[2] | 鲍燕敏, 郑跃杰, 杨永弘. 《中国儿童肺炎链球菌性疾病诊断,治疗和预防专家共识》解读[J]. 中华实用儿科临床杂志, 2021, 36(21): 1601-1604. |
[3] | Wang, B., Lin, W., Qian, C., Zhang, Y., Zhao, G., Wang, W., et al. (2023) Disease Burden of Meningitis Caused by Streptococcus Pneumoniae among Under-Fives in China: A Systematic Review and Meta-Analysis. Infectious Diseases and Therapy, 12, 2567-2580. https://doi.org/10.1007/s40121-023-00878-y |
[4] | Heggi, M.T., Nour El-Din, H.T., Morsy, D.I., Abdelaziz, N.I. and Attia, A.S. (2024) Microbial Evasion of the Complement System: A Continuous and Evolving Story. Frontiers in Immunology, 14, Article 1281096. https://doi.org/10.3389/fimmu.2023.1281096 |
[5] | Hyams, C., Camberlein, E., Cohen, J.M., Bax, K. and Brown, J.S. (2010) Thestreptococcuspneumoniaecapsule Inhibits Complement Activity and Neutrophil Phagocytosis by Multiple Mechanisms. Infection and Immunity, 78, 704-715. https://doi.org/10.1128/iai.00881-09 |
[6] | Hyams, C., Trzcinski, K., Camberlein, E., Weinberger, D.M., Chimalapati, S., Noursadeghi, M., et al. (2013) Streptococcus Pneumoniae Capsular Serotype Invasiveness Correlates with the Degree of Factor H Binding and Opsonization with C3b/iC3b. Infection and Immunity, 81, 354-363. https://doi.org/10.1128/iai.00862-12 |
[7] | Thompson, C.D., Bradshaw, J.L., Miller, W.S., Vidal, A.G.J., Vidal, J.E., Rosch, J.W., et al. (2023) Oligopeptide Transporters of Nonencapsulated Streptococcus Pneumoniae Regulate CbpAC and PspA Expression and Reduce Complement-Mediated Clearance. mBio, 14, e03325-22. https://doi.org/10.1128/mbio.03325-22 |
[8] | Li, J., Szalai, A.J., Hollingshead, S.K., Nahm, M.H. and Briles, D.E. (2009) Antibody to the Type 3 Capsule Facilitates Immune Adherence of Pneumococci to Erythrocytes and Augments Their Transfer to Macrophages. Infection and Immunity, 77, 464-471. https://doi.org/10.1128/iai.00892-08 |
[9] | Brady, A.M., Calix, J.J., Yu, J., Geno, K.A., Cutter, G.R. and Nahm, M.H. (2014) Low Invasiveness of Pneumococcal Serotype 11A Is Linked to Ficolin-2 Recognition of O-Acetylated Capsule Epitopes and Lectin Complement Pathway Activation. The Journal of Infectious Diseases, 210, 1155-1165. https://doi.org/10.1093/infdis/jiu195 |
[10] | Yother, J. and Briles, D.E. (1992) Structural Properties and Evolutionary Relationships of PspA, a Surface Protein of Streptococcus Pneumoniae, as Revealed by Sequence Analysis. Journal of Bacteriology, 174, 601-609. https://doi.org/10.1128/jb.174.2.601-609.1992 |
[11] | Mukerji, R., Mirza, S., Roche, A.M., Widener, R.W., Croney, C.M., Rhee, D., et al. (2012) Pneumococcal Surface Protein a Inhibits Complement Deposition on the Pneumococcal Surface by Competing with the Binding of C-Reactive Protein to Cell-Surface Phosphocholine. The Journal of Immunology, 189, 5327-5335. https://doi.org/10.4049/jimmunol.1201967 |
[12] | Ren, B., Szalai, A.J., Hollingshead, S.K. and Briles, D.E. (2004) Effects of PspA and Antibodies to PspA on Activation and Deposition of Complement on the Pneumococcal Surface. Infection and Immunity, 72, 114-122. https://doi.org/10.1128/iai.72.1.114-122.2004 |
[13] | Ren, B., McCrory, M.A., Pass, C., Bullard, D.C., Ballantyne, C.M., Xu, Y., et al. (2004) The Virulence Function of Streptococcus Pneumoniae Surface Protein a Involves Inhibition of Complement Activation and Impairment of Complement Receptor-Mediated Protection. The Journal of Immunology, 173, 7506-7512. https://doi.org/10.4049/jimmunol.173.12.7506 |
[14] | Ren, B., Li, J., Genschmer, K., Hollingshead, S.K. and Briles, D.E. (2012) The Absence of PspA or Presence of Antibody to PspA Facilitates the Complement-Dependent Phagocytosis of Pneumococci in Vitro. Clinical and Vaccine Immunology, 19, 1574-1582. https://doi.org/10.1128/cvi.00393-12 |
[15] | Li, J., Glover, D.T., Szalai, A.J., Hollingshead, S.K. and Briles, D.E. (2007) PspA and PspC Minimize Immune Adherence and Transfer of Pneumococci from Erythrocytes to Macrophages through Their Effects on Complement Activation. Infection and Immunity, 75, 5877-5885. https://doi.org/10.1128/iai.00839-07 |
[16] | Darrieux, M., Miyaji, E.N., Ferreira, D.M., Lopes, L.M., Lopes, A.P.Y., Ren, B., et al. (2007) Fusion Proteins Containing Family 1 and Family 2 PspA Fragments Elicit Protection against Streptococcus Pneumoniae That Correlates with Antibody-Mediated Enhancement of Complement Deposition. Infection and Immunity, 75, 5930-5938. https://doi.org/10.1128/iai.00940-07 |
[17] | Moreno, A.T., Oliveira, M.L.S., Ferreira, D.M., Ho, P.L., Darrieux, M., Leite, L.C.C., et al. (2010) Immunization of Mice with Single PspA Fragments Induces Antibodies Capable of Mediating Complement Deposition on Different Pneumococcal Strains and Cross-protection. Clinical and Vaccine Immunology, 17, 439-446. https://doi.org/10.1128/cvi.00430-09 |
[18] | Goulart, C., Darrieux, M., Rodriguez, D., Pimenta, F.C., Brandileone, M.C.C., de Andrade, A.L.S.S., et al. (2011) Selection of Family 1 PspA Molecules Capable of Inducing Broad-Ranging Cross-Reactivity by Complement Deposition and Opsonophagocytosis by Murine Peritoneal Cells. Vaccine, 29, 1634-1642. https://doi.org/10.1016/j.vaccine.2010.12.074 |
[19] | Ochs, M.M., Bartlett, W., Briles, D.E., Hicks, B., Jurkuvenas, A., Lau, P., et al. (2008) Vaccine-Induced Human Antibodies to PspA Augment Complement C3 Deposition on Streptococcus Pneumoniae. Microbial Pathogenesis, 44, 204-214. https://doi.org/10.1016/j.micpath.2007.09.007 |
[20] | Pathak, A., Bergstrand, J., Sender, V., Spelmink, L., Aschtgen, M., Muschiol, S., et al. (2018) Factor H Binding Proteins Protect Division Septa on Encapsulated Streptococcus Pneumoniae against Complement C3b Deposition and Amplification. Nature Communications, 9, Article No.3398. https://doi.org/10.1038/s41467-018-05494-w |
[21] | Herbert, A.P., Makou, E., Chen, Z.A., Kerr, H., Richards, A., Rappsilber, J., et al. (2015) Complement Evasion Mediated by Enhancement of Captured Factor H: Implications for Protection of Self-Surfaces from Complement. The Journal of Immunology, 195, 4986-4998. https://doi.org/10.4049/jimmunol.1501388 |
[22] | Orihuela, C.J., Mahdavi, J., Thornton, J., Mann, B., Wooldridge, K.G., Abouseada, N., et al. (2009) Laminin Receptor Initiates Bacterial Contact with the Blood Brain Barrier in Experimental Meningitis Models. Journal of Clinical Investigation, 119, 1638-1646. https://doi.org/10.1172/jci36759 |
[23] | Dave, S., Carmicle, S., Hammerschmidt, S., Pangburn, M.K. and McDaniel, L.S. (2004) Dual Roles of PspC, a Surface Protein of Streptococcus Pneumoniae, in Binding Human Secretory Iga and Factor H. The Journal of Immunology, 173, 471-477. https://doi.org/10.4049/jimmunol.173.1.471 |
[24] | Smith, B.L. and Hostetter, M.K. (2000) C3 as Substrate for Adhesion of Streptococcus Pneumoniae. The Journal of Infectious Diseases, 182, 497-508. https://doi.org/10.1086/315722 |
[25] | Kerr, A.R., Paterson, G.K., McCluskey, J., Iannelli, F., Oggioni, M.R., Pozzi, G., et al. (2006) The Contribution of PspC to Pneumococcal Virulence Varies between Strains and Is Accomplished by Both Complement Evasion and Complement-Independent Mechanisms. Infection and Immunity, 74, 5319-5324. https://doi.org/10.1128/iai.00543-06 |
[26] | Rai, P., He, F., Kwang, J., Engelward, B.P. and Chow, V.T.K. (2016) Pneumococcal Pneumolysin Induces DNA Damage and Cell Cycle Arrest. Scientific Reports, 6, Article No. 22972. https://doi.org/10.1038/srep22972 |
[27] | Chang, S., Chen, C., Lin, J., Wang, H., Mori, S., Li, J., et al. (2020) Truncated Pneumolysin from Streptococcus Pneumoniae as a Tlr4-Antagonizing New Drug for Chronic Inflammatory Conditions. Cells, 9, Article 1183. https://doi.org/10.3390/cells9051183 |
[28] | Malley, R., Henneke, P., Morse, S.C., Cieslewicz, M.J., Lipsitch, M., Thompson, C.M., et al. (2003) Recognition of Pneumolysin by Toll-Like Receptor 4 Confers Resistance to Pneumococcal Infection. Proceedings of the National Academy of Sciences, 100, 1966-1971. https://doi.org/10.1073/pnas.0435928100 |
[29] | McNeela, E.A., Burke, Á., Neill, D.R., Baxter, C., Fernandes, V.E., Ferreira, D., et al. (2010) Pneumolysin Activates the NLRP3 Inflammasome and Promotes Proinflammatory Cytokines Independently of Tlr4. PLOS Pathogens, 6, e1001191. https://doi.org/10.1371/journal.ppat.1001191 |
[30] | Nel, J.G., Theron, A.J., Durandt, C., Tintinger, G.R., Pool, R., Mitchell, T.J., et al. (2016) Pneumolysin Activates Neutrophil Extracellular Trap Formation. Clinical and Experimental Immunology, 184, 358-367. https://doi.org/10.1111/cei.12766 |
[31] | Henderson, B. and Martin, A. (2011) Bacterial Virulence in the Moonlight: Multitasking Bacterial Moonlighting Proteins Are Virulence Determinants in Infectious Disease. Infection and Immunity, 79, 3476-3491. https://doi.org/10.1128/iai.00179-11 |
[32] | Henderson, B. and Martin, A. (2011) Bacterial Moonlighting Proteins and Bacterial Virulence. In: Current Topics in Microbiology and Immunology, Springer, 155-213. https://doi.org/10.1007/82_2011_188 |
[33] | Li, S., Zhang, H., Xiao, J., Yuan, T., Shu, Z., Min, Y., et al. (2020) Streptococcus Pneumoniae Endopeptidase O Promotes the Clearance of Staphylococcus Aureus and Streptococcus Pneumoniae via SH2 Domain-Containing Inositol Phosphatase 1-Mediated Complement Receptor 3 Upregulation. Frontiers in Cellular and Infection Microbiology, 10, Article 358. https://doi.org/10.3389/fcimb.2020.00358 |
[34] | Agarwal, V., Sroka, M., Fulde, M., Bergmann, S., Riesbeck, K. and Blom, A.M. (2014) Binding of Streptococcus Pneumoniae Endopeptidase O (Pepo) to Complement Component C1q Modulates the Complement Attack and Promotes Host Cell Adherence. Journal of Biological Chemistry, 289, 15833-15844. https://doi.org/10.1074/jbc.m113.530212 |
[35] | Bergmann, S., Rohde, M., Preissner, K.T. and Hammerschmidt, S. (2005) The Nine Residue Plasminogen-Binding Motif of the Pneumococcal Enolase Is the Major Cofactor of Plasmin-Mediated Degradation of Extracellular Matrix, Dissolution of Fibrin and Transmigration. Thrombosis and Haemostasis, 94, 304-311. https://doi.org/10.1160/th05-05-0369 |
[36] | Bergmann, S., Schoenen, H. and Hammerschmidt, S. (2013) The Interaction between Bacterial Enolase and Plasminogen Promotes Adherence of Streptococcus Pneumoniae to Epithelial and Endothelial Cells. International Journal of Medical Microbiology, 303, 452-462. https://doi.org/10.1016/j.ijmm.2013.06.002 |
[37] | Agarwal, V. and Blom, A.M. (2015) Roles of Complement C1q in Pneumococcus-Host Interactions. Critical Reviews in Immunology, 35, 173-184. https://doi.org/10.1615/critrevimmunol.2015012177 |
[38] | Agarwal, V., Hammerschmidt, S., Malm, S., Bergmann, S., Riesbeck, K. and Blom, A.M. (2012) Enolase of Streptococcus Pneumoniae Binds Human Complement Inhibitor C4b-Binding Protein and Contributes to Complement Evasion. The Journal of Immunology, 189, 3575-3584. https://doi.org/10.4049/jimmunol.1102934 |
[39] | Attali, C., Durmort, C., Vernet, T. and Di Guilmi, A.M. (2008) The Interaction of Streptococcus Pneumoniae with Plasmin Mediates Transmigration across Endothelial and Epithelial Monolayers by Intercellular Junction Cleavage. Infection and Immunity, 76, 5350-5356. https://doi.org/10.1128/iai.00184-08 |
[40] | Terrasse, R., Tacnet-Delorme, P., Moriscot, C., Pérard, J., Schoehn, G., Vernet, T., et al. (2012) Human and Pneumococcal Cell Surface Glyceraldehyde-3-Phosphate Dehydrogenase (GAPDH) Proteins Are Both Ligands of Human C1q Protein. Journal of Biological Chemistry, 287, 42620-42633. https://doi.org/10.1074/jbc.m112.423731 |
[41] | Fulde, M., Bernardo-García, N., Rohde, M., Nachtigall, N., Frank, R., Preissner, K.T., et al. (2014) Pneumococcal Phosphoglycerate Kinase Interacts with Plasminogen and Its Tissue Activator. Thrombosis and Haemostasis, 112, 401-416. https://doi.org/10.1160/th13-05-0421 |
[42] | Blom, A.M., Bergmann, S., Fulde, M., Riesbeck, K. and Agarwal, V. (2014) Streptococcus Pneumoniae Phosphoglycerate Kinase Is a Novel Complement Inhibitor Affecting the Membrane Attack Complex Formation. Journal of Biological Chemistry, 289, 32499-32511. https://doi.org/10.1074/jbc.m114.610212 |