Proteomic technologies in the development of new vaccines based on serotype-non-specific protein antigens of Streptococcus pneumoniae

Abstract


The review presents a modern strategy to improve the means of vaccine prevention of streptococcal infections aimed at finding and developing new vaccines for immunization of people belonging to risk groups. It should be noted that pneumococci (S. pneumoniae) are members of gram-positive bacteria (diplococci) and become the main cause of various nosological forms of human infectious diseases (such as pneumonia, otitis media, sinusitis, bacteremia and meningitis). Existing pneumococcal vaccines (conjugate and polysaccharide) have some important limitations, for example, serotype dependence, loss of effectiveness due to a change in the serotype landscape, insufficient protective effect from non-invasive forms of pneumococcal infections and high production costs associated with the development of these products. The main part of the review presents the most important research papers that used modern proteomic technologies in the study of the S. pneumoniae proteomic profile. These works allow us to evaluate at the molecular level the importance of bacterial proteins as candidates for creating new combination vaccines that can effectively protect against the full range of pneumococcal serotypes circulating in the human population. So, in particular, the data are provided on the new methodology for the analysis of the proteome of extracellular S. pneumoniae bacterial microvesicles to identify immunoreactive protein antigens, potential candidates for inclusion into vaccines. As a result of these studies, 15 immunoreactive proteins were discovered, 7 of which are cytosolic and 8 proteins are bound to the cell surface (MalX, ABC transporter or substrate binding transport protein, AmiA, AliA, LytC, IgA1 protease, PspA and the putative precursor of β-galactosidase). These are possible candidates for developing combination vaccines. Additionally, the review presents data on the role of significant virulence factors of the protein nature of S. pneumoniae strains in nasopharyngeal colonization, increased infectivity, as well as on overcoming reactions of the host's immune response.


Yu A Tyuri

Kazan State Medical University; Kazan Research Institute of Epidemiology and Microbiology

Author for correspondence.
Email: tyurin.yurii@yandex.ru
Kazan, Russia; Kazan, Russia

A Z Zaripova

Kazan State Medical University; Kazan Research Institute of Epidemiology and Microbiology

Email: tyurin.yurii@yandex.ru
Kazan, Russia; Kazan, Russia

G Sh Isaeva

Kazan State Medical University; Kazan Research Institute of Epidemiology and Microbiology

Email: tyurin.yurii@yandex.ru
Kazan, Russia; Kazan, Russia

I G Mustafin

Kazan State Medical University

Email: tyurin.yurii@yandex.ru
Kazan, Russia

L T Bayazitova

Kazan State Medical University; Kazan Research Institute of Epidemiology and Microbiology

Email: tyurin.yurii@yandex.ru
Kazan, Russia; Kazan, Russia

  1. Sidorenko S.V. Pneumococcal infection – in the centre of attention again. Voprosy sovremennoy pediatrii. 2009; 8 (3): 82–87. (In Russ.)
  2. Lobzin Y.U., Sidorenko S.V., Kharit S.M. et al. Serotypes of Streptococcus pneumo­niae causing major pneumococcal infections. Zhurnal infektologii. 2013; 5 (4): 36–42. (In Russ.)
  3. Austrian R. The pneumococcus at the millennium: not down, not out. J. Infect. Dis. 1999; 179 (2): S338–S341. doi: 10.1086/513841.
  4. Raman R., Sankar J., Putlibai S., Raghavan V. Demographic profile of healthy children with nasopharyngeal colonization of Streptococcus pneumoniae: A research paper. Indian J. Med. Microbiol. 2017; 35 (4): 607–609. doi: 10.4103/ijmm.IJMM_15_347.
  5. Smith H.C., German E., Ferreira D.M., Rylance J. Nasopharyngeal colonization with Streptococcus pneumoniae in malnourished children: a systematic review and meta-analysis of prevalence. Trans. R. Soc. Trop. Med. Hyg. 2019; (9). doi: 10.1093/trstmh/try139.
  6. Simell B., Auranen K., Kayhty H. et al. The fundamental link between pneumococcal carriage and disease. Expert Rev. Vaccines. 2012; 11 (7): 841–855. doi: 10.1586/erv.12.53.
  7. Martynova A.V. Analysis of morbidity of invasive and non-invasive nosological forms of pneumococcal infections in different population groups. Vestnik Rossiyskogo gosudarstvennogo meditsinskogo universiteta. 2008; (5): 38–40. (In Russ.)
  8. Ryapis L.A., Briko N.I. Problem of pneumococcal infections in Russia. Ehpidemiologiya i infek­tsionnye bolezni. 2010; (1): 4–8. (In Russ.)
  9. Bayazitova L.T., Tyupkina O.F., Chazova T.A. et al. Сommunity-acquired pneumonia pneumococcal etiology and microbiological aspects of nasopharyngeal carriage in children in the Republic of Tatarstan. Infektsiya i immunitet. 2017; 7 (3): 271–278. (In Russ.)
  10. Zaripova A.Z., Bayazitova L.T., Tyupkina O.F. et al. Phenotypic and genotypic properties of Streptococcus pneumoniae in case of bacteria carrying. Prakticheskaya meditsina. 2018; 16 (9): 106–112. (In Russ.)
  11. Park I.H., Kim K., Andrade A.L. et al. Nontypeable pneumococci can be dividedinto multiple cps types, inclu­ding one type expressing the novel gene pspK. MBio. 2012; 3 (3): pii: e00035–12. doi: 10.1128/mBio.00035-12.
  12. Keller L.E., Robinson D.A., McDaniel L.S. Nonencapsulated Streptococcus pneumoniae: emergence and pathogenesis. MBio. 2016; 7 (2): e01792. doi: 10.1128/mBio.01792-15.
  13. Keller L.E., Jones C.V., Thornton J.A. et al. PspK of Streptococcus pneumonia increases adherence to epithelial cells and enhances nasopharyngeal colonization. Infect. Immun. 2013; 81 (1): 173–181. doi: 10.1128/IAI.00755-12.
  14. Keller L.E., Bradshaw J.L., Pipkins H., McDa­niel L.S. Surface proteins and pneumolysin of encapsulated and nonencapsulated Streptococcus pneumoniae mediate virulence in a chinchilla model of otitis media. Front. Cell Infect. Microbiol. 2016; (6): 55. doi: 10.3389/fcimb.2016.00055.
  15. Moscoso M., García E., López R. et al. Biofilm formation by Streptococcus pneumoniae: role of choline, extracellular DNA, and capsular polysaccharide in microbial accretion. J. Bacteriol. 2006; 188 (22): 7785–7795. doi: 10.1128/JB.00673-06.
  16. Schaffner T.O., Hinds J., Gould K.A. et al. A point mutation in cpsE renders Streptococcus pneumoniae nonencapsulated and enhances its growth, adherence and competence. BMC Microbiol. 2014; 14: 210. doi: 10.1186/s12866-014-0210-x.
  17. Fedoseenko M.V., Namazova-Baranova L.S. International experience of administration of pneumococ­cal conjugated vaccines: problems, progress, perspectives. Voprosy sovremennoy pediatrii. 2009; 8 (1): 130–134. (In Russ.)
  18. Mayanskiy N.A., Alyabʹeva N.M., Lazareva A.V., Katosova L.K. Serotype diversity and antimicrobial resistance of streptococcus pneumoniae. Vestnik Rossiy­skoy akademii meditsinskikh nauk. 2014; 69 (7–8): 38–45. (In Russ.)
  19. Torres A., Blasi F., Peetermans W.E. et al. The aetiology and antibiotic management of community-acquired pneumonia in adults in Europe: a literature review. Eur. J. Clin. Microbiol. Infect. Dis. 2014; 33 (7): 1065–1079. doi: 10.1007/s10096-014-2067-1.
  20. Picazo J.J. Management of antibiotic-resistant Streptococcus pneumoniae infections and the use of pneumococcal conjugate vaccines. Clin. Microbiol. Infect. 2009; 15 (3): 4–6. doi: 10.1111/j.1469-0691.2009.02723.x.
  21. Briko N.I., Tsapkova N.N., Sukhova V.A. et al. Epidemiological assessment of the first results of the national program of immunization of young children against pneumococcal infection in Russia. Ehpidemiologiya i vaktsinoprofilaktika. 2017; (5): 16–21. (In Russ.)
  22. McDaniel L.S., Swiatlo E. Pneumococcal ­disease: pathogenesis, treatment, and prevention. Infec. Dis. Clin. Pract. 2004; 12: 93–98. doi: 10.1016/S0140-6736(09)61114-4.
  23. Feldman C., Anderson R. Review: current and new generation pneumococcal vaccines. J. Infect. 2014; 69 (4): 309–325. doi: 10.1016/j.jinf.2014.06.006.
  24. Geno K.A., Gilbert G.L., Song J.Y. et al. Pneumococcal capsules and their types: Past, present, and future. Clin. Microbiol. Rev. 2015; 28 (3): 871–899. doi: 10.1128/CMR.00024-15.
  25. Varghese R., Jayaraman R., Veeraraghavan B. Current challenges in the accurate identification of Streptococcus pneumoniae and its serogroups/serotypes in the vaccine era. J. Microbiol. Methods. 2017; 141: 48–54. doi: 10.1016/j.mimet.2017.07.015.
  26. Feldman C., Andersen R. Epidemiology, virulence factors and management of the pneumococcus. F1000Research. 2016; 5: 2320. doi: 10.12688/f1000research.9283.1.
  27. Pichichero M.E., Khan M.N., Xu Q. Next gene­ration protein based Streptococcus pneumoniae vaccines. Hum. Vaccines Immunotherap. 2016; (12): 1. doi: 10.1080/21645515.2015.1052198.
  28. Tettelin H., Nelson K.E., Paulsen I.T. et al. Complete genome sequence of a virulent isolate of Streptococcus pneumoniae. Science. 2001; 293 (5529): 498–506. doi: 10.1126/science.1061217.
  29. Bricker A.L., Camilli A. Transformation of a type 4 encapsulated strain of Streptococcus pneumoniae. FEMS Microbiol. Lett. 1999; 172 (2): 131–135. doi: 10.1111/j.1574-6968.1999.tb13460.x.
  30. Hoskins J., Alborn W.E.Jr., Arnold J. et al. Genome of the bacterium Streptococcus pneumoniae strain R6. J. Bacteriol. 2000; 183 (19): 5709–5717. doi: 10.1128/JB.183.19.5709-5717.2001.
  31. Lanie J.A., Ng W.L., Kazmierczak K.M. et al. Genome sequence of Avery’s virulent serotype 2 strain D39 of Streptococcus pneumoniae and comparison with that of unencapsulated laboratory strain R6. J. Bacteriol. 2007; 189 (1): 38–51. doi: 10.1128/JB.01148-06.
  32. Williams T.M., Loman N.J., Ebruke C. et al. Genome analysis of a highly virulent serotype 1 strain of Streptococcus pneumoniae from West Africa. PLoS ONE. 2012; 7 (10): e26742. doi: 10.1371/journal.pone.0026742.
  33. Choi S.C., Parker J., Richards V.P. et al. Draft genome sequence of an atypical strain of Streptococcus pneumoniae isolated from a respiratory infection. Genome Announc. 2014; 2 (4): e00822–e00814. doi: 10.1128/genomeA.00822-14.
  34. Hiller N.L., Eutsey R.A., Powell E. et al. Diffe­rences in genotype and virulence among four multidrug-­resistant Streptococcus pneumoniae isolates belonging to the PMEN 1 clone. PLoS One. 2011; 6 (12): e28850. doi: 10.1371/journal.pone.0028850.
  35. Brückner R., Nuhn M., Reichmann P. et al. ­Mosaic genes and mosaic chromosomes-genomic variation in Streptococcus pneumoniae. Int. J. Med. Microbiol. 2004; 294 (2–3): 157–168. doi: 10.1016/j.ijmm.2004.06.019.
  36. Croucher N.J., Harris S.R., Fraser C. et al. Rapid pneumococcal evolution in response to clinical interventions. Science. 2011; 331 (6016): 430–434. doi: 10.1126/science.1198545.
  37. Bergmann S., Hammerschmidt S. Versatility of pneumococcal surface proteins. Microbiology. 2006; 152 (2): 295–303. doi: 10.1099/mic.0.28610-0.
  38. Perez-Dorado I., Galan-Bartual S., Hermoso J.A. Pneumococcal surface proteins: when the whole is greater than the sum of its parts. Mol. Oral Microbiol. 2012; 27 (4): 221–245. doi: 10.1111/j.2041-1014.2012.00655.x.
  39. Wizemann T.M., Heinrichs J.H., Adamou J.E. et al. Use of a whole genome approach to identify vaccine molecules affording protection against Streptococcus pneumo­niae infection. Infect. Immun. 2001; 69 (3): 1593–1598. doi: 10.1128/IAI.69.3.1593-1598.2001.
  40. Maione D., Margarit I., Rinaudo C.D. et al. Identification of a universal Group B streptococcus vaccine by multiple genome screen. Science. 2005; 309 (5731): ­148–150. doi: 10.1126/science.1109869.
  41. Kopylov A.T., Zgoda V.G. Quantitative methods in proteomics. Biomeditsinskaya khimiya. 2007; 53 (6): 613–643. (In Russ.)
  42. Bittaye M., Cash P. Streptococcus pneumo­niae proteomics: determinants of pathogenesis and vaccine development. Exp. Rev. Proteomics. 2015; (12): 6. doi: 10.1586/14789450.2015.1108844.
  43. Cole J.N., Djordjevic S.P., Walker M.J. Isolation and solubilization of gram-positive bacterial cell wall-asso­ciated proteins. Methods Mol. Biol. 2008; 425: 295–311. doi: 10.1007/978-1-60327-210-0_24.
  44. Morsczeck C., Prokhorova T., Sigh J. et al. Streptococcus pneumoniae: proteomics of surface proteins for vaccine development. Clin. Microbiol. Infect. 2008; 14 (1): ­74–81. doi: 10.1111/j.1469-0691.2007.01878.x.
  45. Ling E., Feldman G., Portnoi M. et al. Glycolytic enzymes associated with the cell surface of Streptococcus pneumoniae are antigenic in humans and elicit protective immune responses in the mouse. Clin. Exp. Immunol. 2004; 138 (2): 290–298. doi: 10.1111/j.1365-2249.2004.02628.x.
  46. Sabarth N., Lamer S., Zimny-Arndt U. et al. Identification of surface proteins of Helicobacter pylori by selective biotinylation, affinity purification, and two-dimensional gel electrophoresis. J. Biol. Chem. 2002; 277 (31): 27896–27902. doi: 10.1074/jbc.M204473200.
  47. Gatlin C.L., Pieper R., Huang S.T. et al. Proteomic profiling of cell envelope associated proteins from Staphylococcus aureus. Proteomics. 2006; 6 (5): 1530–1549. doi: 10.1002/pmic.200500253.
  48. Cole J.N., Ramirez R.D., Currie B.J. et al. Surface analyses and immune reactivities of major cell wall-associa­ted proteins of Group A Streptococcus. Infect. Immun. 2005; 73 (5): 3137–3146. doi: 10.1128/IAI.73.5.3137-3146.2005.
  49. Rodriguez-Ortega M.J., Norais N., Bensi G. et al. Characterization and identification of vaccine candidate proteins through analysis of the group A Streptococcus surface proteome. Nat. Biotechnol. 2006; 24 (2): 191–197. doi: 10.1038/nbt1179.
  50. Olaya-Abril A., Jimenez-Munguia I., Gomez-Gascon L. et al. Identification of potential new protein vaccine candidates through pan-surfomic analysis of pneumococcal clinical isolates from adults. PLoS ONE. 2013; 8 (7): e70365. doi: 10.1371/journal.pone.0070365.
  51. Lee E.Y., Choi D.Y., Kim D.K. et al. Gram-positive bacteria produce membrane vesicles: proteomics-based characterization of Staphylococcus aureus derived membrane vesicles. J. Proteomics. 2009; 9: 5425–5436. doi: 10.1002/pmic.200900338.
  52. Olaya-Abril A., Prados-Rosales R., McConnell M.J. et al. Characterization of protective extracellular membrane-derived vesicles produced by Streptococcus pneumoniae. J. Proteomics. 2014; 106: 46–60. doi: 10.1016/j.jprot.2014.04.023.
  53. Moffitt K.L., Gierahn T.M., Lu Y.J. et al. T(H)17-based vaccine design for prevention of Streptococcus pneumoniae colonization. Cell Host Microb. 2011; 9 (2): ­158–165. doi: 10.1016/j.chom.2011.01.007.
  54. Moffitt K.L., Malley R., Lu Y.J. Identification of protective pneumococcal T(H)17 antigens from the so­luble fraction of a killed whole cell vaccine. PLoS One. 2012; 7 (8): e43445. doi: 10.1371/journal.pone.0043445.
  55. Ogunniyi A.D., Grabowicz M., Briles D.E. et al. Development of a vaccine against invasive pneumococcal di­sease based on combinations of virulence proteins of Streptococcus pneumoniae. Infect. Immun. 2007; 75 (1): 350–357. doi: 10.1128/IAI.01103-06.
  56. Nouwens A.S., Cordwell S.J., Larsen M.R. et al. Complementing genomics with proteomics: the membrane subproteome of Pseudomonas aeruginosa PAO1. Electrophoresis. 2000; 21 (17): 3797–3809. doi: 10.1002/1522-2683(200011)21:17<3797::AID-ELPS3797>3.0.CO;2-P.
  57. Lee K.J., Bae S.M., Lee M.R. et al. Proteomic ana­lysis of growth phase-dependent proteins of Streptoco­ccus pneumoniae. Proteomics. 2006; 6 (4): 1274–1282. doi: 10.1002/pmic.200500415.

Views

Abstract - 26

PDF (Russian) - 20

Cited-By


PlumX


© 2019 Tyuri Y.A., Zaripova A.Z., Isaeva G.S., Mustafin I.G., Bayazitova L.T.

Creative Commons License

This work is licensed
under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.


Свидетельство о регистрации СМИ ЭЛ № ФС 77-75008 от 1 февраля 2019 года выдано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор)