IgA-protease activity coupled to cellular enzymes of different Streptococcus pneumonia serotypes isolated in pediatric bacteria carriers

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Abstract

Streptococcus pneumoniae are significant causative agents of severe and life-threatening acute pneumonia, meningitis, as well as otitis and sinusitis both in children and elderly. As many as 1.2 million pediatric lethal outcomes due to pneumonia and infections of the central nervous system (meningitis) caused by S. pneumoniae, are recorded worldwide annually, a large proportion of which occur in developing countries. Metal-dependent IgA1 proteases derived from pathogenic bacteria comprise an important group of bacterial enzymes cleaving human immunoglobulin A1 (IgA1) at the hinge region, thereby interfering with fully-executed host antibacterial immunity.

Objective. To study activity of IgA1proteinases and their class profile (Na2-EDTA and PMSF-inhibited) in various pneumococcal serotypes isolated from nasopharyngeal carrier children.

Materials and methods. There were examined 585 children attending preschool facilities residing in Kazan (n = 331) and rural areas (n = 254). Microbiological, molecular genetics and immunochemical methods were used to identify, serotyping composition and protease activity of Streptococcus pneumoniae isolates. Data statistical processing was carried out by using software Graph Pad Prism version 5.0.

Results. Prevalence of S. pneumonie in pediatric carriers aged 1.5–3 years was 35.1%, 3–5 years — 23.4%, 5–7 years — 19.6%, and over 7 years — 21.9%. Vaccine serotypes 14, 19F, 23F as a part of current pneumococcal vaccines (Prevenar, Pneumavax-23) comprised as high as 55.8%. However, in 19% of cases were positive for non-vaccine S. pneumoniae strains. Non-typeable strains were detected in 5.8% isolates. IgA-proteinase activity was detected in cell lysates of 45 (86.5%) S. pneumoniae strains isolated from pediatric carriers. Cell lysates of S. pneumoniae strains showing no proteolytic properties, were assigned to serotypes 12F, Sg18. Thus, studies on development of alternative vaccines containing immunogenic proteins, adhesins or other virulence factors common to capsulated and non-typeable (encapsulated) pneumococcal strains hold promise. All the aforementioned accounts for a need for microbiological monitoring of S. pneumoniae carriage and search for new diagnostic approaches for etiological interpretation of S. pneumoniae-associated diseases.

About the authors

A. Z. Zaripova

Kazan State Medical University

Email: albina.fahrislamova@yandex.ru

Assistant Professor, Department of Microbiology

Kazan

Russian Federation

Yu. A. Tyurin

Kazan State Medical University; Kazan Scientific-Research Institute for Epidemiology and Microbiology

Author for correspondence.
Email: tyurin.yurii@yandex.ru

Yury A. Tyurin, PhD (Medicine), Assistant Professor, Department Biochemistry and Clinical Laboratory Diagnostics; Head of Scientific Research Laboratory of Immunology and Allergens Development

420015, Kazan, Bol’shaya Krasnaya str., 67.

Phone: +7 (843) 238-89-79 (office).

Russian Federation

L. T. Bayazitova

Kazan State Medical University; Kazan Scientific-Research Institute for Epidemiology and Microbiology

Email: bajalt@mail.ru

PhD (Medicine), Associate Professor, Department of Microbiology; Head of Scientific Research Department of Microbiology

Kazan 

Russian Federation

O. F. Tyupkina

Kazan Scientific-Research Institute for Epidemiology and Microbiology

Email: tyupkina.olga@mail.ru

Senior Researcher, Scientific Research Department of Microbiology

Kazan

Russian Federation

G. Sh. Isaeva

Kazan State Medical University; Kazan Scientific-Research Institute for Epidemiology and Microbiology

Email: guisaeva@rambler.ru

PhD, MD (Medicine), Head of Microbiology Department; Director

Kazan

References

  1. Баязитова Л.Т., Тюпкина О.Ф., Чазова Т.А., Тюрин Ю.А., Исаева Г.Ш., Зарипова А.З., Патяшина М.А., Авдонина Л.Г., Юзлибаева Л.Р. Внебольничные пневмонии пневмококковой этиологии и микробиологические аспекты назофарингеального носительства Streptococcus pneumoniae у детей в Республике Татарстан // Инфекция и иммунитет. 2017. Т. 7, № 3. С. 271–278. doi: 10.15789/2220-7619-2017-3-271-278
  2. Белоцерковская Ю.Г., Романовская А.Г., Стырт Е.А. Пневмококковая вакцина у взрослых снижает риск инфекций, вызванных Streptococcus pneumonia // Клиническая медицина. 2016, Т. 94, № 1. С. 61–66. doi: 10.18821/0023-2149-2016-94-1-61-66
  3. Боронина Л.Г., Саматова Е.В. Эпидемиологические особенности Streptococcus pneumoniae, выделенного у детей, при неинвазивных пневмококковых инфекциях и носоглоточном бактерионосительстве // Вопросы диагностики в педиатрии. 2013. Т. 5, № 3. С. 22–26.
  4. Козлов Р.С., Кречикова О.И., Муравьев А.А., Миронов К.О., Платонов А.Е., Дунаева Е.А., Таточенко В.К., Щербаков М.Е., Родникова В.Ю., Романенко В.В., Сафьянов К.Н., группа исследователей PAPIRUS. Результаты исследования распространенности в России внебольничной пневмонии и острого среднего отита у детей в возрасте до 5 лет (PAPIRUS). Роль S. pneumoniae и H. influenza в этиологии данных заболеваний // Клиническая микробиология и антимикробная химиотерапия. 2013. T. 15, № 4. С. 246–260.
  5. Костинов М.П. Иммунокоррекция вакцинального процесса у лиц с нарушенным состоянием здоровья. М.: Медицина для всех, 2006. 172 с.
  6. Муравьев А.А., Козлов Р.С., Лебедева Н.Н. Эпидемиология серотипов S. pneumoniae на территории Российской Федерации // Клиническая микробиология и антимикробная химиотерапия. 2017. T. 19, № 3. С. 200–206.
  7. Тюрин Ю.А., Шамсутдинов А.Ф., Фассахов Р.С. Изучение полиморфизма однонуклеотидных фрагментов aur-гена металлозависимой протеазы штаммов Staphylococcus aureus, выделенных с кожи больных атопическим дерматитом // Молекулярная генетика, микробиология и вирусология. 2014. № 4. C. 5–7.
  8. Bethe G., Nau R., Wellmer A., Hakenbeck R., Reinert R.R., Heinz H.P., Zysk G. The cell wall-associated serine protease PrtA: a highly conserved virulence factor of Streptococcus pneumoniae. FEMS Microbiol Lett., 2001, vol. 205, no. 1, pp. 99–104. doi: 10.1111/j.1574-6968.2001.tb10931.x
  9. Cassone M., Gagne A.L., Spruce L.A., Seeholzer S.H., Sebert M.E. The HtrA protease from Streptococcus pneumoniae digests both denatured proteins and the competence-stimulating peptide. J. Biol. Chem., 2012, vol. 287, no. 46, pp. 38449–38459. doi: 10.1074/jbc.M112.391482
  10. Courtney H.S. Degradation of connective tissue proteins by serine proteases from Streptococcus pneumonia. Biochem. Biophys. Res. Commun., 1991, vol. 175, no. 3, pp. 1023–1028. doi: 10.1016/0006-291X(91)91667-2
  11. Dawid S., Sebert M.E., Weiser J.N. Bacteriocin activity of Streptococcus pneumoniae is controlled by the serine protease HtrA via posttranscriptional regulation. J. Bacteriol., 2009, vol. 191, no. 5, pp. 1509–1518. doi: 10.1128/JB.01213-08
  12. Feldman C., Anderson R. Review: current and new generation pneumococcal vaccines. J. Infect., 2014, vol. 69, no. 4, pp. 309–325. doi: 10.1016/j.jinf.2014.06.006
  13. Geno K.A., Gilbert G.L., Song J.Y., Skovsted I.C., Klugman K.P., Jones C., Konradsen H.B., Nahm M.H. Pneumococcal capsules and their types: past, present, and future. Clin. Microbiol. Rev., 2015, vol. 28, no. 3, pp. 871–899. doi: 10.1128/CMR.00024-15
  14. Gupta A., Khaw F.M, Stokle E.L, George R.C., Pebody R., Stansfield R.E., Sheppard C.L., Slack M., Gorton R., Spencer D.A. Outbreak of Streptococcus pneumoniae serotype 1 pneumonia in a United Kingdom school. BMJ, 2008, vol. 337: a2964. doi: 10.1136/bmj.a2964
  15. Hausdorff W.P., Bryant J., Paradiso P.R., Siber G.R. Which pneumococcal serogroups cause the most invasive disease: implications for conjugate vaccine formulation and use, part I. Clin. Infect. Dis., 2000, vol. 30, pp. 100–121. doi: 10.1086/313608
  16. Ibrahim Y.M., Kerr A.R., McCluskey J., Mitchell T.J. Role of HtrA in the virulence and competence of Streptococcus pneumoniae. Infect. Immun., 2004, vol. 72, no. 6, pp. 3584–3591. doi: 10.1128/IAI.72.6.3584-3591.2004
  17. Keller L.E., Robinson D.A., McDaniel L.S. Non encapsulated Streptococcus pneumoniae: emergence and pathogenesis. MBio, 2016, vol. 7, no. 2: e01792. doi: 10.1128/mBio.01792-15
  18. Kriger O., Regev-Yochay G. The effect of pneumococcal conjugate vaccine on pneumococcalcarriage and invasive disease. Harefuah., 2019, vol. 158, no. 5, pp. 316–320.
  19. Pai R., Gertz R.E., Beall B. Sequential multiplex PCR approach for determining capsular serotypes of streptococcus pneumoniae isolates. J. Clin. Microbiol., 2006, vol. 44, no. 1, pp. 124–131. doi: 10.1128/JCM.44.1.124-131.2006
  20. Prevention of pneumococcal disease: recommendations of the (ACIP). MMWR Recomm. Rep., 1997, no. 4, vol. 46 (RR-8). pp. 1–24.
  21. Reshetnikova I.D., Bayazitova L.T., Tupkina O.F., Tyurin Y.A., Shamsutdinov A.F., Kadkina V., Rizvanov A.A. Characteristics of antibiotic resistance nasopharyngeal strains of Streptococcus pneumoniae in children suffering from respiratory pathologies. BioNanoScience, 2017, vol. 7, no. 1, pp. 182–185. doi: 10.1007/s12668-016-0324-8
  22. Simell B., Auranen K., K ä yhty H., Goldblatt D., Dagan R., O’Brien K. L. The fundamental link between pneumococcal carriage and disease. Expert. Rev. Vaccines, 2012, vol. 11, no. 7, pp. 841–855. doi: 10.1586/erv.12.53
  23. Van der Poll T., Opal S.M. Pathogenesis, treatment, and prevention of pneumococcal pneumonia. Lancet, 2009, vol. 374, pp. 1543–1556. doi: 10.1016/S0140-6736(09)61114-4
  24. Wani J.H., Gilbert J.V., Plaut A.G., Weiser J.N. Identification, cloning and sequencing of the immunoglobulin A1 protease gene of Streptococcus pneumoniae. Infect. Immun., 1996, vol. 64, pp. 3967–3974.
  25. Yoshioka C.R., Martinez M.B., Brandileone M.C., Ragazzi S.B., Guerra M.L., Santos S.R., Shieh H.H., Gilio A.E. Analysis of invasive pneumonia-causing strains of Streptococcus pneumoniae: serotypes and antimicrobial susceptibility. J. Pediatr. (Rio J.)., 2011, vol. 87, no. 1, pp. 70–75. doi: 10.2223/JPED.2063

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Copyright (c) 2019 Zaripova A.Z., Tyurin Y.A., Bayazitova L.T., Tyupkina O.F., Isaeva G.S.

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