Login Register Cart 0
Generic placeholder image

Current Proteomics

Editor-in-Chief

ISSN (Print): 1570-1646
ISSN (Online): 1875-6247

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Research Article

Immunoprotective Potential of Adenylosuccinate Synthetase Protein (PurA) in Streptococcus equi ssp. zooepidemicus Infections

Author(s): Xiaoling Zhang, Sihuan Chen, Shuji Gao, Weiping Yang, Yuxin Wang, Yang Wang* and Li Yi*

Volume 21, Issue 1, 2024

Published on: 23 February, 2024

Page: [43 - 53] Pages: 11

DOI: 10.2174/0115701646284439240218063821

Price: $65

Abstract

Background: Streptococcus equi ssp. zooepidemicus (SEZ) is one important pathogen. There are still sporadic outbreaks in China, northern United States and the Netherlands. Adenylosuccinate synthetase PurA, a newly discovered protein in prior research, requires further assessment of its protective effectiveness.

Methods: In this study, we focused on the expression of recombinant PurA from SEZ ATCC 35246. We evaluated the immunoreactivity of this recombinant protein using convalescent minipig sera. Additionally, we conducted experiments in mice to assess its immunogenic properties.

Results: Our findings revealed that the recombinant PurA triggered a substantial antibody response in mice, resulting in an 80% protection rate against SEZ infection. Notably, mice immunized with PurA exhibited significantly reduced bacterial colonization in all organs compared to the PBS control group. Furthermore, the levels of IL-6, IL-8, IL-1β, and TNF-α in mouse serum were significantly elevated in the PurA-immunized group compared to the control group. Hyperimmune sera targeting PurA effectively eliminated SEZ in bactericidal tests. Remarkably, antibodies against PurA demonstrated a significant inhibitory effect on developing SEZ biofilm.

Conclusion: Immunization with PurA elicited robust humoral and cellular immune responses in mice. These promising results suggest the potential utility of PurA in developing SEZ vaccine immunogens, providing a valuable avenue for further research into SEZ infection prevention and control.

« Previous
Graphical Abstract

[1]
Chen, X.; Mou, K.; Lu, W.; Schumacher, L.; Resende-De-Macedo, N.; Sitthicharoenchai, P.; Derscheid, R.; Burrough, E.; Li, G. Genomic characterization of Streptococcus equi subspecies zooepidemicus from a 2021 outbreak in Indiana with increased sow mortality. MSphere, 2023, 8(6), e00404-23.
[http://dx.doi.org/10.1128/msphere.00404-23] [PMID: 37861318]
[2]
Geiping, L.; Detlefsen, H.; Trittmacher, S.; Baums, C.G.; Bergmann, R.; Hennig-Pauka, I. Streptococcus equi subspecies zooepidemicus - A case report of sudden death in a German sow farm. Porcine Health Manag., 2023, 9(1), 48.
[http://dx.doi.org/10.1186/s40813-023-00344-8] [PMID: 37875963]
[3]
Costa, M.O.; Harding, J.C.S.; Huang, Y.; Nosach, R. Streptococcus equi subsp. Zooepidemicus infection of pigs leads to shedding in faeces and a carrier state. Transbound. Emerg. Dis., 2022, 69(5), e1503-e1509.
[http://dx.doi.org/10.1111/tbed.14481] [PMID: 35182443]
[4]
Feng, Z.G.; Hu, J.S. Outbreak of swine streptococcosis in sichuan province and identification of pathogen. Anim Husbandry Vet Med Lett, 1977, 2, 7-12.
[5]
Costa, M.O.; Lage, B. Streptococcus equi Subspecies zooepidemicus and Sudden Deaths in Swine, Canada. Emerg. Infect. Dis., 2020, 26(10), 2522-2524.
[http://dx.doi.org/10.3201/eid2610.191485] [PMID: 32946731]
[6]
Song, H.; Yuan, C.; Zhang, Y.; Pan, F.; Fan, H.; Ma, Z. Protection efficacy of monoclonal antibodies targeting different regions of specific SzM protein from swine-isolated streptococcus equi ssp. zooepidemicus Strains. Microbiol. Spectr., 2022, 10(6), e01742-22.
[http://dx.doi.org/10.1128/spectrum.01742-22] [PMID: 36255327]
[7]
Wei, Z.; Li, R.; Zhang, A.; He, H.; Hua, Y.; Xia, J.; Cai, X.; Chen, H.; Jin, M. Characterization of Streptococcus suis isolates from the diseased pigs in China between 2003 and 2007. Vet. Microbiol., 2009, 137(1-2), 196-201.
[http://dx.doi.org/10.1016/j.vetmic.2008.12.015] [PMID: 19185432]
[8]
Hau, S.J.; Lantz, K.; Stuart, K.L.; Sitthicharoenchai, P.; Macedo, N.; Derscheid, R.J.; Burrough, E.R.; Robbe-Austerman, S.; Brockmeier, S.L. Replication of Streptococcus equi subspecies zooepidemicus infection in swine. Vet. Microbiol., 2022, 264, 109271.
[http://dx.doi.org/10.1016/j.vetmic.2021.109271] [PMID: 34826647]
[9]
Chen, X.; Resende-De-Macedo, N.; Sitthicharoenchai, P.; Sahin, O.; Burrough, E.; Clavijo, M.; Derscheid, R.; Schwartz, K.; Lantz, K.; Robbe-Austerman, S.; Main, R.; Li, G. Genetic characterization of Streptococcus equi subspecies zooepidemicus associated with high swine mortality in the United States. Transbound. Emerg. Dis., 2020, 67(6), 2797-2808.
[http://dx.doi.org/10.1111/tbed.13645] [PMID: 32460392]
[10]
Sitthicharoenchai, P.; Derscheid, R.; Schwartz, K.; Macedo, N.; Sahin, O.; Chen, X.; Li, G.; Main, R.; Burrough, E. Cases of high mortality in cull sows and feeder pigs associated with Streptococcus equi subsp. zooepidemicus septicemia. J. Vet. Diagn. Invest., 2020, 32(4), 565-571.
[http://dx.doi.org/10.1177/1040638720927669] [PMID: 32532177]
[11]
Surendran Nair, M.; Byukusenge, M.; Li, L.; Nissly, R.H.; Cavener, V.S.; Yon, M.; Barry, R.; Natesan, P.; Thirumalapura, N.; Tewari, D.; Jayarao, B.M.; Kuchipudi, S.V. Draft genome sequences of two virulent streptococcus equi subsp. zooepidemicus Swine isolates from pennsylvania. Microbiol. Resour. Announc., 2020, 9(42), e00974-20.
[http://dx.doi.org/10.1128/MRA.00974-20] [PMID: 33060275]
[12]
Kerdsin, A.; Chopjitt, P.; Hatrongjit, R.; Boueroy, P.; Gottschalk, M. Zoonotic infection and clonal dissemination of Streptococcus equi subspecies zooepidemicus sequence type 194 isolated from humans in Thailand. Transbound. Emerg. Dis., 2022, 69(4), e554-e565.
[http://dx.doi.org/10.1111/tbed.14331] [PMID: 34558797]
[13]
Kuchipudi, S.V.; Surendran Nair, M.; Yon, M.; Gontu, A.; Nissly, R.H.; Barry, R.; Greenawalt, D.; Pierre, T.; Li, L.; Thirumalapura, N.; Tewari, D.; Jayarao, B. A novel real-time pcr assay for the rapid detection of virulent streptococcus equi subspecies zooepidemicus-An emerging pathogen of swine. Front. Vet. Sci., 2021, 8, 604675.
[http://dx.doi.org/10.3389/fvets.2021.604675] [PMID: 33644143]
[14]
Ma, Z.; Geng, J.; Zhang, H.; Yu, H.; Yi, L.; Lei, M.; Lu, C.; Fan, H.; Hu, S. Complete genome sequence of streptococcus equi subsp. zooepidemicus Strain ATCC 35246. J. Bacteriol., 2011, 193(19), 5583-5584.
[http://dx.doi.org/10.1128/JB.05700-11] [PMID: 21914890]
[15]
Jara, L.M.; Angulo-Tisoc, J.; Giménez-Lirola, L.G.; Li, G.; Andrade, R.; Mamani, J. Outbreak of pathogenic streptococcus equi subsp. zooepidemicus in guinea pigs farms of the andean region. Pathogens, 2023, 12(3), 445.
[http://dx.doi.org/10.3390/pathogens12030445] [PMID: 36986367]
[16]
Garmyn, A.; Van de Velde, N.; Braeckmans, D.; Ronsmans, S.; Boyen, F.; Verlinden, M. An outbreak associated with streptococcus equi Subsp. zooepidemicus in Layers: Evidence of fecal transmission. Avian Dis., 2020, 64(3), 343-346.
[http://dx.doi.org/10.1637/aviandiseases-D-19-00191] [PMID: 33205184]
[17]
Blum, S.; Elad, D.; Zukin, N.; Lysnyansky, I.; Weisblith, L.; Perl, S.; Netanel, O.; David, D. Outbreak of Streptococcus equi subsp. zooepidemicus infections in cats. Vet. Microbiol., 2010, 144(1-2), 236-239.
[http://dx.doi.org/10.1016/j.vetmic.2009.12.040] [PMID: 20106608]
[18]
Preziuso, S.; Moriconi, M.; Cuteri, V. Genetic diversity of Streptococcus equi subsp. zooepidemicus isolated from horses. Comp. Immunol. Microbiol. Infect. Dis., 2019, 65, 7-13.
[http://dx.doi.org/10.1016/j.cimid.2019.03.012] [PMID: 31300129]
[19]
Steward, K.F.; Robinson, C.; Holden, M.T.G.; Harris, S.R.; Ros, A.F.; Pérez, G.C.; Baselga, R.; Waller, A.S. Diversity of Streptococcus equi subsp. zooepidemicus strains isolated from the Spanish sheep and goat population and the identification, function and prevalence of a novel arbutin utilisation system. Vet. Microbiol., 2017, 207, 231-238.
[http://dx.doi.org/10.1016/j.vetmic.2017.06.020] [PMID: 28757029]
[20]
Bergmann, R.; Schroedl, W.; Müller, U.; Baums, C.G. A distinct variant of the SzM protein of Streptococcus equi subsp. zooepidemicus recruits C1q independent of IgG binding and inhibits activation of the classical complement pathway. Virulence, 2023, 14(1), 2235461.
[http://dx.doi.org/10.1080/21505594.2023.2235461] [PMID: 37450582]
[21]
Ma, Z.; Yu, L.; Zhou, H.; Liu, T.; Xu, B.; Ma, F.; Peng, J.; Fan, H. Identification of novel genes expressed during host infection in Streptococcus equi ssp. zooepidemicus ATCC35246. Microb. Pathog., 2015, 79, 31-40.
[http://dx.doi.org/10.1016/j.micpath.2015.01.004] [PMID: 25595678]
[22]
Jie, P.; Zhe, M.; Chengwei, H.; Huixing, L.; Hui, Z.; Chengping, L.; Hongjie, F. Virulent and vaccine strains of streptococcus equi ssp. zooepidemicus have different influences on phagocytosis and cytokine secretion of macrophages. J. Proteome Res., 2017, 16(1), 77-86.
[http://dx.doi.org/10.1021/acs.jproteome.6b00571] [PMID: 27726373]
[23]
Eyre, D.W. Streptococcus equi subspecies zooepidemicus meningitis-a case report and review of the literature. Eur. J. Clin. Microbiol. Infect. Dis., 2010, 29(12), 1459-1463.
[http://dx.doi.org/10.1007/s10096-010-1037-5] [PMID: 20820836]
[24]
Chhabra, D.; Bhatia, T.; Goutam, U.; Manuja, A.; Kumar, B. Strangles in equines: An overview. Microb. Pathog., 2023, 178, 106070.
[http://dx.doi.org/10.1016/j.micpath.2023.106070] [PMID: 36924902]
[25]
Pringle, J.; Storm, E.; Waller, A.; Riihimäki, M. Influence of penicillin treatment of horses with strangles on seropositivity to Streptococcus equi ssp. equi ‐specific antibodies. J. Vet. Intern. Med., 2020, 34(1), 294-299.
[http://dx.doi.org/10.1111/jvim.15668] [PMID: 31769122]
[26]
Baliga, P.; Shekar, M.; Venugopal, M.N. Potential outer membrane protein candidates for vaccine development against the pathogen vibrio anguillarum: A reverse vaccinology based identification. Curr. Microbiol., 2018, 75(3), 368-377.
[http://dx.doi.org/10.1007/s00284-017-1390-z] [PMID: 29119233]
[27]
Ahmadi Rouzbahani, H.; Mousavi Gargari, S.L.; Nazarian, S.; Abdollahi, S. Protective immunity against enterotoxigenic escherichia coli by oral vaccination of engineered lactococcus lactis. Curr. Microbiol., 2021, 78(9), 3464-3473.
[http://dx.doi.org/10.1007/s00284-021-02601-x] [PMID: 34264362]
[28]
Riquelme, S.A.; Wozniak, A.; Kalergis, A.M.; Bueno, S.M. Evasion of host immunity by virulent Salmonella: Implications for vaccine design. Curr. Med. Chem., 2011, 18(36), 5666-5675.
[http://dx.doi.org/10.2174/092986711798347333] [PMID: 22172071]
[29]
Dorotkiewicz-Jach, A.; Augustyniak, D.; Olszak, T.; Drulis-Kawa, Z. Modern therapeutic approaches against pseudomonas aeruginosa infections. Curr. Med. Chem., 2015, 22(14), 1642-1664.
[http://dx.doi.org/10.2174/0929867322666150417122531] [PMID: 25882546]
[30]
Robinson, C.; Frykberg, L.; Flock, M.; Guss, B.; Waller, A.S.; Flock, J.I. Strangvac: A recombinant fusion protein vaccine that protects against strangles, caused by Streptococcus equi. Vaccine, 2018, 36(11), 1484-1490.
[http://dx.doi.org/10.1016/j.vaccine.2018.01.030] [PMID: 29398274]
[31]
Borst, L.B.; Patterson, S.K.; Lanka, S.; Barger, A.M.; Fredrickson, R.L.; Maddox, C.W. Evaluation of a commercially available modified-live Streptococcus equi subsp equi vaccine in ponies. Am. J. Vet. Res., 2011, 72(8), 1130-1138.
[http://dx.doi.org/10.2460/ajvr.72.8.1130] [PMID: 21801073]
[32]
Mao, Y.; Fan, H.; Lu, C. Immunoproteomic assay of extracellular proteins in Streptococcus equi ssp. zooepidemicus. FEMS Microbiol. Lett., 2008, 286(1), 103-109.
[http://dx.doi.org/10.1111/j.1574-6968.2008.01259.x] [PMID: 18616598]
[33]
Lin, H.; Huang, D.; Wang, Y.; Lu, C.; Fan, H. A novel vaccine against Streptococcus equi ssp. zooepidemicus infections: The recombinant swinepox virus expressing M-like protein. Vaccine, 2011, 29(40), 7027-7034.
[http://dx.doi.org/10.1016/j.vaccine.2011.07.074] [PMID: 21807055]
[34]
Jores, J.; Meens, J.; Buettner, F.F.R.; Linz, B.; Naessens, J.; Gerlach, G.F. Analysis of the immunoproteome of Mycoplasma mycoides subsp. mycoides small colony type reveals immunogenic homologues to other known virulence traits in related Mycoplasma species. Vet. Immunol. Immunopathol., 2009, 131(3-4), 238-245.
[http://dx.doi.org/10.1016/j.vetimm.2009.04.016] [PMID: 19443045]
[35]
Stayton, M.M.; Rudolph, F.B.; Fromm, H.J. Regulation, genetics, and properties of adenylosuccinate synthetase: A review. Curr. Top. Cell. Regul., 1983, 22, 103-141.
[http://dx.doi.org/10.1016/B978-0-12-152822-5.50008-7] [PMID: 6347525]
[36]
Bubić, A.; Mrnjavac, N.; Stuparević, I.; Łyczek, M.; Wielgus-Kutrowska, B.; Bzowska, A.; Luić, M.; Leščić Ašler, I. In the quest for new targets for pathogen eradication: the adenylosuccinate synthetase from the bacterium Helicobacter pylori. J. Enzyme Inhib. Med. Chem., 2018, 33(1), 1405-1414.
[http://dx.doi.org/10.1080/14756366.2018.1506773] [PMID: 30191734]
[37]
O’Callaghan, D.; Maskell, D.; Liew, F.Y.; Easmon, C.S.; Dougan, G. Characterization of aromatic- and purine-dependent Salmonella typhimurium: Attention, persistence, and ability to induce protective immunity in BALB/c mice. Infect. Immun., 1988, 56(2), 419-423.
[http://dx.doi.org/10.1128/iai.56.2.419-423.1988] [PMID: 3276625]
[38]
Metcalf, D.S.; MacInnes, J.I. Differential expression of Haemophilus parasuis genes in response to iron restriction and cerebrospinal fluid. Can. J. Vet. Res., 2007, 71(3), 181-188.
[PMID: 17695592]
[39]
Hoffman, J.A.; Badger, J.L.; Zhang, Y.; Sik Kim, K. Escherichia coli K1 pur A and sor C are preferentially expressed upon association with human brain microvascular endothelial cells. Microb. Pathog., 2001, 31(2), 69-79.
[http://dx.doi.org/10.1006/mpat.2001.0451] [PMID: 11453702]
[40]
Yi, L.; Wang, Y.; Ma, Z.; Lin, H.X.; Xu, B.; Grenier, D.; Fan, H.J.; Lu, C.P. Identification and characterization of a streptococcus equi ssp. zooepidemicus immunogenic GroEL protein involved in biofilm formation. Vet. Res., 2016, 47(1), 50.
[http://dx.doi.org/10.1186/s13567-016-0334-0] [PMID: 27089967]
[41]
Loera-Muro, A.; Guerrero-Barrera, A.; Tremblay D N, Y.; Hathroubi, S.; Angulo, C. Bacterial biofilm-derived antigens: A new strategy for vaccine development against infectious diseases. Expert Rev. Vaccines, 2021, 20(4), 385-396.
[http://dx.doi.org/10.1080/14760584.2021.1892492] [PMID: 33606569]
[42]
Carriquiriborde, F.; Martin Aispuro, P.; Ambrosis, N.; Zurita, E.; Bottero, D.; Gaillard, M.E.; Castuma, C.; Rudi, E.; Lodeiro, A.; Hozbor, D.F. Pertussis vaccine candidate based on outer membrane vesicles derived from biofilm culture. Front. Immunol., 2021, 12, 730434.
[http://dx.doi.org/10.3389/fimmu.2021.730434] [PMID: 34603306]
[43]
de Gouw, D.; Serra, D.O.; de Jonge, M.I.; Hermans, P.W.M.; Wessels, H.J.C.T.; Zomer, A.; Yantorno, O.M.; Diavatopoulos, D.A.; Mooi, F.R. The vaccine potential of Bordetella pertussis biofilm-derived membrane proteins. Emerg. Microbes Infect., 2014, 3(1), 1-9.
[http://dx.doi.org/10.1038/emi.2014.58] [PMID: 26038752]
[44]
Mansouri, M.; Sadeghpoor, M.; Jahangiri, A.; Ghaini, M.H.; Rasooli, I. Enhanced immunoprotection against acinetobacter baumannii infection: Synergistic effects of Bap and BauA in a murine model. Immunol. Lett., 2023, 262, 18-26.
[http://dx.doi.org/10.1016/j.imlet.2023.08.004] [PMID: 37652189]
[45]
Mohd Ali, N.S.; Saad, M.Z.; Azmai, M.N.A.; Salleh, A.; Zulperi, Z.M.; Manchanayake, T.; Zahaludin, M.A.D.; Basri, L.; Mohamad, A.; Md Yasin, I.S. Immunogenicity and efficacy of a feed-based bivalent vaccine against streptococcosis and motile aeromonad septicemia in red hybrid tilapia (Oreochromis sp.). Animals, 2023, 13(8), 1346.
[http://dx.doi.org/10.3390/ani13081346] [PMID: 37106909]
[46]
Ismail, M.S.; Syafiq, M.R.; Siti-Zahrah, A.; Fahmi, S.; Shahidan, H.; Hanan, Y.; Amal, M.N.A.; Zamri Saad, M. The effect of feed-based vaccination on tilapia farm endemic for streptococcosis. Fish Shellfish Immunol., 2017, 60, 21-24.
[http://dx.doi.org/10.1016/j.fsi.2016.11.040] [PMID: 27864157]
[47]
Yi, L.; Du, Y.; Mao, C.; Li, J.; Jin, M.; Sun, L.; Wang, Y. Immunogenicity and protective ability of RpoE against streptococcus suis serotype 2. J. Appl. Microbiol., 2021, 130(4), 1075-1083.
[http://dx.doi.org/10.1111/jam.14874] [PMID: 32996241]
[48]
Yi, L.; Yang, W.; Sun, L.; Li, J.; Li, X.; Wang, Y. Identification of a novel protective antigen, 3-oxoacyl-[acyl-carrier-protein] synthase II of Streptococcus equi ssp. zooepidemicus which confers protective effects. Comp. Immunol. Microbiol. Infect. Dis., 2020, 71, 101493.
[http://dx.doi.org/10.1016/j.cimid.2020.101493] [PMID: 32447155]
[49]
Liu, M.; Zhu, H.; Zhang, J.; Lei, B. Active and passive immunizations with the streptococcal esterase Sse protect mice against subcutaneous infection with group A streptococci. Infect. Immun., 2007, 75(7), 3651-3657.
[http://dx.doi.org/10.1128/IAI.00038-07] [PMID: 17502395]
[50]
Yi, L.; Wang, Y.; Ma, Z.; Zhang, H.; Li, Y.; Zheng, J.; Yang, Y.; Lu, C.; Fan, H. Contribution of fibronectin-binding protein to pathogenesis of Streptococcus equi ssp. zooepidemicus. Pathog. Dis., 2013, 67(3), 174-183.
[http://dx.doi.org/10.1111/2049-632X.12029] [PMID: 23620180]
[51]
Hong-jie, F.; Fu-yu, T.; Ying, M.; Cheng-ping, L. Virulence and antigenicity of the szp-gene deleted Streptococcus equi ssp. zooepidemicus mutant in mice. Vaccine, 2009, 27(1), 56-61.
[http://dx.doi.org/10.1016/j.vaccine.2008.10.037] [PMID: 18983882]
[52]
de Lima, D.A.; Andreotti, C.E.L.; Antiquera Ferreira, F.; Pauli, K.B.; da Silva, G.R.; Ribeiro, R.C.L.; Dalsenter, P.R.; Boechat, N.; Gasparotto Junior, A.; Lourenço, E.L.B.; Lívero, F.A.R. Safety assessment of MEFAS: An innovative hybrid salt of mefloquine and artesunate for malaria treatment. Drug Chem. Toxicol., 2021, 44(4), 380-385.
[http://dx.doi.org/10.1080/01480545.2019.1607371] [PMID: 31060457]
[53]
Kim, M.; Heo, S.T.; Oh, H.; Kim, M.; Jo, J.; Kim, Y.R.; Lee, K.H.; Yoo, J.R. Human zoonotic infectious disease caused by Streptococcus equi subsp. zooepidemicus. Zoonoses Public Health, 2022, 69(2), 136-142.
[http://dx.doi.org/10.1111/zph.12895] [PMID: 34585529]
[54]
Kittang, B.R.; Pettersen, V.K.; Oppegaard, O.; Skutlaberg, D.H.; Dale, H.; Wiker, H.G.; Skrede, S. Zoonotic necrotizing myositis caused by Streptococcus equi subsp. zooepidemicus in a farmer. BMC Infect. Dis., 2017, 17(1), 147.
[http://dx.doi.org/10.1186/s12879-017-2262-7] [PMID: 28201995]
[55]
Wang, X.; Wang, G.; Li, X.; Fu, J.; Chen, T.; Wang, Z.; Zhao, X. Directed evolution of adenylosuccinate synthetase from Bacillus subtilis and its application in metabolic engineering. J. Biotechnol., 2016, 231, 115-121.
[http://dx.doi.org/10.1016/j.jbiotec.2016.05.032] [PMID: 27234879]
[56]
Stenger, R.M.; Meiring, H.D.; Kuipers, B.; Poelen, M.; van Gaans-van den Brink, J.A.M.; Boog, C.J.P.; de Jong, A.P.J.M.; van Els, C.A.C.M. Bordetella pertussis proteins dominating the major histocompatibility complex class II-presented epitope repertoire in human monocyte-derived dendritic cells. Clin. Vaccine Immunol., 2014, 21(5), 641-650.
[http://dx.doi.org/10.1128/CVI.00665-13] [PMID: 24599530]
[57]
Molzen, T.E.; Burghout, P.; Bootsma, H.J.; Brandt, C.T.; van der Gaast-de Jongh, C.E.; Eleveld, M.J.; Verbeek, M.M.; Frimodt-Møller, N.; Østergaard, C.; Hermans, P.W.M. Genome-wide identification of Streptococcus pneumoniae genes essential for bacterial replication during experimental meningitis. Infect. Immun., 2011, 79(1), 288-297.
[http://dx.doi.org/10.1128/IAI.00631-10] [PMID: 21041497]
[58]
Ataei, S.; Momtazi-Borojeni, A.A.; Ganjali, S.; Banach, M.; Sahebkar, A. The immunogenic potential of PCSK9 peptide vaccine in mice. Curr. Med. Chem., 2023, 30(26), 3024-3031.
[http://dx.doi.org/10.2174/0929867329666220930114429] [PMID: 36200256]
[59]
Kralova, N.; Stepanova, H.; Gebauer, J.; Norek, A.; Matiaskova, K.; Zouharova, M.; Nedbalcova, K.; Babak, V.; Jarosova, R.; Makovicky, P.; Kucharovicova, I.; Simek, B.; Plodkova, H.; Pecka, T.; Matiasovic, J. Vaccine against streptococcus suis infection in pig based on alternative carrier protein conjugate. Vaccines, 2022, 10(10), 1620.
[http://dx.doi.org/10.3390/vaccines10101620] [PMID: 36298485]
[60]
Boksha, I.S.; Lunin, V.G.; Danilova, T.A.; Poponova, M.S.; Polyakov, N.B.; Lyashchuk, A.M.; Konstantinova, S.V.; Galushkina, Z.M.; Ustenko, E.V. Recombinant endopeptidases IdeS and IdeZ and their potential application. Biochemistry, 2023, 88(6), 731-740.
[http://dx.doi.org/10.1134/S0006297923060020] [PMID: 37748870]
[61]
Yi, L.; Fan, Q.; Wang, Y.; Mao, C.; Li, J.; Jin, M.; Zhang, X.; Ding, K.; Wang, Y. Evaluation of immune effect of Streptococcus suis biofilm-associated protein PDH. Vet. Microbiol., 2021, 263, 109270.
[http://dx.doi.org/10.1016/j.vetmic.2021.109270] [PMID: 34749282]
[62]
Romagnani, S. Induction of TH1 and TH2 responses: a key role for the ‘natural’ immune response? Immunol. Today, 1992, 13(10), 379-381.
[http://dx.doi.org/10.1016/0167-5699(92)90083-J] [PMID: 1418371]
[63]
Tanaka, T.; Narazaki, M.; Kishimoto, T. Interleukin (IL-6) immunotherapy. Cold Spring Harb. Perspect. Biol., 2018, 10(8), a028456.
[http://dx.doi.org/10.1101/cshperspect.a028456] [PMID: 28778870]
[64]
Gonzalez-Aparicio, M.; Alfaro, C. Influence of Interleukin-8 and Neutrophil Extracellular Trap (NET) Formation in the Tumor Microenvironment: Is There a Pathogenic Role? J. Immunol. Res., 2019, 2019, 1-7.
[http://dx.doi.org/10.1155/2019/6252138] [PMID: 31093511]
[65]
Chauhan, D.; Vande Walle, L.; Lamkanfi, M. Therapeutic modulation of inflammasome pathways. Immunol. Rev., 2020, 297(1), 123-138.
[http://dx.doi.org/10.1111/imr.12908] [PMID: 32770571]
[66]
Liu, Z. Molecular mechanism of TNF signaling and beyond. Cell Res., 2005, 15(1), 24-27.
[http://dx.doi.org/10.1038/sj.cr.7290259] [PMID: 15686622]
[67]
Su, F.J.; Chen, M.M. Protective Efficacy of Novel Oral Biofilm Vaccines against Lactococcus garvieae Infection in Mullet, Mugil cephalus. Vaccines, 2021, 9(8), 844.
[http://dx.doi.org/10.3390/vaccines9080844] [PMID: 34451969]
[68]
Chen, R.; Du, M.; Liu, C. Strategies for dispersion of cariogenic biofilms: Applications and mechanisms. Front. Microbiol., 2022, 13, 981203.
[http://dx.doi.org/10.3389/fmicb.2022.981203] [PMID: 36134140]
[69]
Dey, A.; Yadav, M.; Kumar, D.; Dey, A.K.; Samal, S.; Tanwar, S.; Sarkar, D.; Pramanik, S.K.; Chaudhuri, S.; Das, A. A combination therapy strategy for treating antibiotic resistant biofilm infection using a guanidinium derivative and nanoparticulate Ag(0) derived hybrid gel conjugate. Chem. Sci., 2022, 13(34), 10103-10118.
[http://dx.doi.org/10.1039/D2SC02980D] [PMID: 36128224]
[70]
Blanchette-Cain, K.; Hinojosa, C.A.; Akula Suresh Babu, R.; Lizcano, A.; Gonzalez-Juarbe, N.; Munoz-Almagro, C.; Sanchez, C.J.; Bergman, M.A.; Orihuela, C.J. Streptococcus pneumoniae biofilm formation is strain dependent, multifactorial, and associated with reduced invasiveness and immunoreactivity during colonization. MBio, 2013, 4(5), e00745-13.
[http://dx.doi.org/10.1128/mBio.00745-13] [PMID: 24129258]
[71]
Yi, L.; Fan, Q.; Wang, H.; Fan, H.; Zuo, J.; Wang, Y.; Wang, Y. Establishment of streptococcus suis biofilm infection model in vivo and comparative analysis of gene expression profiles between in vivo and in vitro biofilms. Microbiol. Spectr., 2023, 11(1), e02686-22.
[http://dx.doi.org/10.1128/spectrum.02686-22] [PMID: 36507687]
[72]
Belyi, Y.; Rybolovlev, I.; Polyakov, N.; Chernikova, A.; Tabakova, I.; Gintsburg, A. Staphylococcus aureus surface protein G is an immunodominant protein and a possible target in an anti-biofilm drug development. Open Microbiol. J., 2018, 12(1), 94-106.
[http://dx.doi.org/10.2174/1874285801812010094] [PMID: 29785216]
[73]
Mirzaei, B.; Babaei, R.; Haghshenas, M.R.; Hagshenas, M.R.; Mohammadi, F.; Homayoni, P.; Shafaei, E. PIA and rSesC mixture arisen antibodies could inhibit the biofilm-formation in staphylococcus aureus. Rep. Biochem. Mol. Biol., 2021, 10(1), 1-12.
[http://dx.doi.org/10.52547/rbmb.10.1.1] [PMID: 34277863]
[74]
Gholami, S.A.; Goli, H.R.; Haghshenas, M.R.; Mirzaei, B. Evaluation of polysaccharide intercellular adhesion (PIA) and glycerol teichoic acid (Gly-TA) arisen antibodies to prevention of biofilm formation in Staphylococcus aureus and Staphylococcus epidermidis strains. BMC Res. Notes, 2019, 12(1), 691.
[http://dx.doi.org/10.1186/s13104-019-4736-8] [PMID: 31653277]
[75]
Corsini, B.; Aguinagalde, L.; Ruiz, S.; Domenech, M.; Antequera, M.L.; Fenoll, A.; García, P.; García, E.; Yuste, J. Immunization with LytB protein of Streptococcus pneumoniae activates complement-mediated phagocytosis and induces protection against pneumonia and sepsis. Vaccine, 2016, 34(50), 6148-6157.
[http://dx.doi.org/10.1016/j.vaccine.2016.11.001] [PMID: 27840016]
[76]
Yi, L.; Wang, Y.; Ma, Z.; Zhang, H.; Li, Y.; Zheng, J.; Yang, Y.; Fan, H.; Lu, C. Biofilm formation of Streptococcus equi ssp. zooepidemicus and comparative proteomic analysis of biofilm and planktonic cells. Curr. Microbiol., 2014, 69(3), 227-233.
[http://dx.doi.org/10.1007/s00284-014-0574-z] [PMID: 24696150]
[77]
Xie, Z.; Meng, K.; Yang, X.; Liu, J.; Yu, J.; Zheng, C.; Cao, W.; Liu, H. Identification of a quorum sensing system regulating capsule polysaccharide production and biofilm formation in streptococcus zooepidemicus. Front. Cell. Infect. Microbiol., 2019, 9, 121.
[http://dx.doi.org/10.3389/fcimb.2019.00121] [PMID: 31058104]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy