Molecular investigation of cytolysin genes among bacterial isolates recovered from pyospermic patients in Hilla City, Iraq
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Abstract
Enterococcus faecalis and Uropathogenic Escherichia coli (UPEC) are the most common causal agents of urinary tract infections (UTI) and infertility in humans. They secrete many cytolytic toxins that impact sperm functions and spermatogenesis. The current paper aimed to investigate the cytolysins among Bacteriospermia associated bacteria in pyospermic patients. 110 Seminal fluid swabs were collected from pyospermic patients (age Mean±SD, 35.5±2.12 years) from September 2020 to January 2021. All swabs were inoculated on UTI chromogenic medium for primary isolation of bacteria. Then the suspected Es. coli and En. faecalis have been confirmed by PCR using uidA and ddl genes, respectively. The results revealed that Es. coli compile 42.9% of bacteriospermia while En. faecalis 25.71%. Results of PCR for cytolysins reveal that all E. coli isolates have lta, hylA, sta, and stb (100%) genes, sheA (96.7%), stx2 (20%), and stx1(3.3%). All En. faecalis (100%) have Hyl, cylLS, cyILL genes. The current study concludes that both Es. coli and En. faecalis have a set of toxins with possible damage to sperm function, causing indirect infertility.
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Keywords
Escherichia coli, En faecalis, Bacteriospermia, Pyospermia, Toxins
References
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Barati, S. (2012). Antibiotic resistance of enterotoxigenic and entroaggrigative Escherichia coli isolated from gastroenteritis cases. Asian Journal of Biomedical and Pharmaceutical Sciences, 2(14),54-58.
Bej, A.K., Dicesare, J.L., Haff, L. & Atlas, R.M. (1991). Detection of Escherichia coli and Shigella spp. in water by using the polymerase chain reaction and gene probes for uid. Applied and Environmental Microbiology, 57(4),1013-1017.
Brons, J.K., Vink, S.N., de Vos, M.G., Reuter, S., Dobrindt, U. & van Elsas, J.D. (2020). Fast identification of Escherichia coli in urinary tract infections using a virulence gene based PCR approach in a novel thermal cycler. Journal of Microbiological Methods, 169, 1-10
Brötz, H. & Sahl, H.G. (2000). New insights into the mechanism of action of lantibiotics—diverse biological effects by binding to the same molecular target. Journal of Antimicrobial Chemotherapy, 46(1),1-6.
Cha, J.O., Jung, Y.H., Lee, H.R., Yoo, J.I. & Lee, Y.S. (2012). Comparison of genetic epidemiology of vancomycin-resistant Enterococcus faecium isolates from humans and poultry. Journal of medical microbiology, 61(8),1121-1128.
Chandran, A. & Mazumder, A. (2013). Prevalence of diarrhea-associated virulence genes and genetic diversity in Escherichia coli isolates from fecal material of various animal hosts. Applied and Environmental Microbiology, 79(23),7371-7380.
Chi, X., Zhao, X., Wang, W., Niu, Y., Cheng, M., Liu, X., Cui, S. & Yang, W. (2017). Fusion expression of Occludin extracellular loops and an α-helical bundle: A new research model for tight junction. PloS One, 12(4), 1-13.
Chumbler, N.M., Farrow, M.A., Lapierre, L.A., Franklin, J.L. & Lacy, D.B. (2016). Clostridium difficile toxins TcdA and TcdB cause colonic tissue damage by distinct mechanisms. Infection and Immunity, 84(10), 2871-2877.
Comerlato, C.B., Resende, M.C.C.D., Caierão, J. & d'Azevedo, P.A. (2013). Presence of virulence factors in Enterococcus faecalis and Enterococcus faecium susceptible and resistant to vancomycin. Memórias do Instituto Oswaldo Cruz, 108,590-595.
Peraro, M.D. & Van Der Goot, F.G. (2016). Pore-forming toxins: ancient, but never really out of fashion. Nature Reviews Microbiology, 14(2),77-92.
Düzgün, A.Ö., Okumuş, F., Saral, A., Çiçek, A.Ç. & Cinemre, S. (2019). Determination of antibiotic resistance genes and virulence factors in Escherichia coli isolated from Turkish patients with urinary tract infection. Revista da Sociedade Brasileira de Medicina Tropical, 52,1-5
Elmalı, M. & Can, H.Y. (2018). The prevalence, vancomycin resistance and virulence gene profiles of Enterococcus species recovered from different foods of animal origin. Veterinarski Arhiv, 88(1),111-124.
Farhan, Z.A. & AL-Iedani, A.A. (2019). Molecular detection of shiga toxin (stx1 and stx2) and intimin (eae A) genes in Escherichia coli isolated from fecal samples of cattle, sheep, and human in Basrah governorate. Basrah J Vet Res, 18(2),288-305.
Han, W., Liu, B., Cao, B., Beutin, L., Krüger, U., Liu, H., Li, Y., Liu, Y., Feng, L. & Wang, L. (2007). DNA microarray-based identification of serogroups and virulence gene patterns of Escherichia coli isolates associated with porcine postweaning diarrhea and edema disease. Applied and Environmental Microbiology, 73(12), 4082-4088.
Hashem, Y.A., Abdelrahman, K.A. & Aziz, R.K. (2021). Phenotype–genotype correlations and distribution of key virulence factors in Enterococcus faecalis isolated from patients with urinary tract infections. Infection and Drug Resistance, 14, p.1713.
Hassan, M.H. (2020). The cytotoxicity effects of liable and stable enterotoxins produced by uropathogenic Escherichia coli. Systematic Reviews in Pharmacy, 11(12), pp.997-999.
Heidari, H., Hasanpour, S., Ebrahim-Saraie, H.S. & Motamedifar, M. (2017). High incidence of virulence factors among clinical Enterococcus faecalis isolates in Southwestern Iran. Infection & Chemotherapy, 49(1), pp.51-56.
Heydari, F.E., Bonyadian, M., Moshtaghi, H. & Sami, M. (2020). Prevalence and antibiotic resistance profile of Shiga toxin-producing Escherichia coli isolated from diarrheal samples. Iranian Journal of Microbiology, 12(4), p.289.
Hynes, W.L. & Walton, S.L. (2000). Hyaluronidases of Gram-positive bacteria. FEMS Microbiology Letters, 183(2), pp.201-207.
Islam, M.R., Nagao, J.I., Zendo, T. & Sonomoto, K. (2012). Antimicrobial mechanism of lantibiotics. Biochemical Society Transactions, 40(6), 1528-1533.
Jiang, L., Zhu, Y., Luan, P., Xu, J., Ru, G., Fu, J. G., Sang, N., Xiong, Y., He, Y., Lin, G. Q., Wang, J., Zhang, J. & Li, R. (2021). Bacteria-anchoring hybrid liposome capable of absorbing multiple toxins for antivirulence therapy of Escherichia coli infection. ACS Nano, 15(3), 4173–4185.
Kerényi, M., Allison, H. E., Bátai, I., Sonnevend, A., Emödy, L., Plaveczky, N. & Pál, T. (2005). Occurrence of hlyA and sheA genes in extraintestinal Escherichia coli strains. Journal of Clinical Microbiology, 43(6), 2965–2968.
Kotlowski, R., Bernstein, C. N., Sepehri, S. & Krause, D. O. (2007). High prevalence of Escherichia coli belonging to the B2+ D phylogenetic group in inflammatory bowel disease. Gut, 56(5), 669–675.
Krug, S.M. & Fromm, M. (2020). Special issue on “The tight junction and its proteins: more than just a barrier”. International Journal of Molecular Sciences, 21(13),4612.
Leitão, A. L., Costa, M. C., Gabriel, A. F., & Enguita, F. J. (2020). Interspecies communication in Holobionts by non-coding RNA exchange. International Journal of Molecular Sciences, 21(7), 2333.
Lorenz, S. C., Son, I., Maounounen-Laasri, A., Lin, A., Fischer, M., & Kase, J. A. (2013). Prevalence of hemolysin genes and comparison of ehxA subtype patterns in Shiga toxin-producing Escherichia coli (STEC) and non-STEC strains from clinical, food, and animal sources. Applied and Environmental Microbiology, 79(20), 6301–6311.
Lui, W. Y., Lee, W. M., & Cheng, C. Y. (2001). Transforming growth factor-beta3 perturbs the inter-Sertoli tight junction permeability barrier in vitro possibly mediated via its effects on occludin, zonula occludens-1, and claudin-11. Endocrinology, 142(5), 1865–1877.
Marrs, C. F., Zhang, L., Tallman, P., Manning, S. D., Somsel, P., Raz, P., Colodner, R., Jantunen, M. E., Siitonen, A., Saxen, H., & Foxman, B. (2002). Variations in 10 putative uropathogen virulence genes among urinary, faecal and peri-urethral Escherichia coli. Journal of Medical Microbiology, 51(2), 138–142.
Mete, E., Kaleli, İ., Cevahir, N., Demir, M., Akkaya, Y. & Kiriş Satılmış, Ö. (2017). Evaluation of virulence factors in Enterococcus species. Mikrobiyoloji Bulteni, 51(2), 101–114.
Nassour, H. & Dubreuil, J.D. (2014). Escherichia coli STb enterotoxin dislodges claudin-1 from epithelial tight junctions. PloS One, 9(11), 1-11.
Osek, J., Gallien, P., Truszczyñski, M., & Protz, D. (1999). The use of polymerase chain reaction for determination of virulence factors of Escherichia coli strains isolated from pigs in Poland. Comparative Immunology, Microbiology and Infectious Diseases, 22(3), 163–174.
Parmegiani, L., Cognigni, G. E., Ciampaglia, W., Pocognoli, P., Marchi, F. & Filicori, M. (2010). Efficiency of hyaluronic acid (HA) sperm selection. Journal of Assisted Reproduction and Genetics, 27(1), 13–16.
Parvez, S.A. & Rahman, D. (2018). Virulence Factors of Uropathogenic E. coli. Microbiology of Urinary Tract Infections-Microbial Agents and Predisposing Factors,7-21.
Pearce, K. L., Hill, A.. & Tremellen, K. P. (2019). Obesity related metabolic endotoxemia is associated with oxidative stress and impaired sperm DNA integrity. Basic and Clinical Andrology, 29(1), 6.
Popoff, M. R. (2018). ‘Bacterial Toxins’ section in the journal toxins: A fantastic multidisciplinary interplay between bacterial pathogenicity mechanisms, physiological processes, genomic evolution, and subsequent development of identification methods, efficient treatment, and prevention of toxigenic bacteria. Toxins, 10(1).
Roderer, D. & Glockshuber, R. (2017). Assembly mechanism of the α-pore–forming toxin cytolysin A from Escherichia coli. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 372(1726), 20160211.
Rubab, M. & Oh, D. H. (2020). Virulence characteristics and antibiotic resistance profiles of shiga toxin-producing Escherichia coli isolates from diverse sources. Antibiotics, 9(9), 587.
Santo, E., Macedo, C. & Marin, J. M. (2006). Virulence factors of uropathogenic Escherichia coli from a university hospital in Ribeirão Preto, São Paulo, Brazil. Revista do Instituto de Medicina Tropical de São Paulo, 48(4), 185–188.
Semedo, T., Almeida Santos, M., Martins, P., Silva Lopes, M. F., Figueiredo Marques, J. J., Tenreiro, R. & Barreto Crespo, M. T. (2003). Comparative study using type strains and clinical and food isolates to examine hemolytic activity and occurrence of the cyl operon in enterococci. Journal of Clinical Microbiology, 41(6), 2569–2576.
Shokoohizadeh, L., Ekrami, A., Labibzadeh, M., Ali, L. & Alavi, S. M. (2018). Antimicrobial resistance patterns and virulence factors of enterococci isolates in hospitalized burn patients. BMC Research Notes, 11(1), 1.
Soong, G., Parker, D., Magargee, M. & Prince, A. S. (2008). The type III toxins of Pseudomonas aeruginosa disrupt epithelial barrier function. Journal of Bacteriology, 190(8), 2814–2821.
Stępień-Pyśniak, D., Hauschild, T., Kosikowska, U., Dec, M. & Urban-Chmiel, R. (2019). Biofilm formation capacity and presence of virulence factors among commensal Enterococcus spp. from wild birds. Scientific Reports, 9(1), 11204.
Tanaka, K., Caaveiro, J. M., Morante, K., González-Mañas, J. M. & Tsumoto, K. (2015). Structural basis for self-assembly of a cytolytic pore lined by protein and lipid. Nature Communications, 6(1), 6337.
Vankerckhoven, V., Van Autgaerden, T., Vael, C., Lammens, C., Chapelle, S., Rossi, R., Jabes, D. & Goossens, H. (2004). Development of a multiplex PCR for the detection of asa1, gelE, cylA, esp, and hyl genes in enterococci and survey for virulence determinants among European hospital isolates of Enterococcus faecium. Journal of Clinical Microbiology, 42(10), 4473–4479.
Viswanathan, V. K., Koutsouris, A., Lukic, S., Pilkinton, M., Simonovic, I., Simonovic, M. & Hecht, G. (2004). Comparative analysis of EspF from enteropathogenic and enterohemorrhagic Escherichia coli in alteration of epithelial barrier function. Infection and Immunity, 72(6), 3218–3227.
Wiles, T. J., Dhakal, B. K., Eto, D. S. & Mulvey, M. A. (2008). Inactivation of host Akt/protein kinase B signaling by bacterial pore-forming toxins. Molecular Biology of the Cell, 19(4), 1427–1438.
Zeb, Z., Azam, S., Rehman, N., Khan, I., Afzal, S., Sehra, G. E., Ullah, A. & Absar, M. (2021). Phenotypic and molecular characterization of virulence factors of extra-intestinal pathogenic Escherichia coli isolated from patients of Peshawar, Pakistan. Pakistan Journal of Pharmaceutical Sciences, 34(1), 85–94.
Bakhtiari, M., Sobhani, A., Akbari, M., Pasbakhsh, P., Abasi, M., Hedayatpour, A., Amidi, F. & Sargolzaei, A.F. (2007). The effect of hyaluronic acid on motility, vitality and fertilization capability of mouse sperms after cryopreservation. International Journal of Reproductive Biomedicine, 5(2),45-50.
Barati, S. (2012). Antibiotic resistance of enterotoxigenic and entroaggrigative Escherichia coli isolated from gastroenteritis cases. Asian Journal of Biomedical and Pharmaceutical Sciences, 2(14),54-58.
Bej, A.K., Dicesare, J.L., Haff, L. & Atlas, R.M. (1991). Detection of Escherichia coli and Shigella spp. in water by using the polymerase chain reaction and gene probes for uid. Applied and Environmental Microbiology, 57(4),1013-1017.
Brons, J.K., Vink, S.N., de Vos, M.G., Reuter, S., Dobrindt, U. & van Elsas, J.D. (2020). Fast identification of Escherichia coli in urinary tract infections using a virulence gene based PCR approach in a novel thermal cycler. Journal of Microbiological Methods, 169, 1-10
Brötz, H. & Sahl, H.G. (2000). New insights into the mechanism of action of lantibiotics—diverse biological effects by binding to the same molecular target. Journal of Antimicrobial Chemotherapy, 46(1),1-6.
Cha, J.O., Jung, Y.H., Lee, H.R., Yoo, J.I. & Lee, Y.S. (2012). Comparison of genetic epidemiology of vancomycin-resistant Enterococcus faecium isolates from humans and poultry. Journal of medical microbiology, 61(8),1121-1128.
Chandran, A. & Mazumder, A. (2013). Prevalence of diarrhea-associated virulence genes and genetic diversity in Escherichia coli isolates from fecal material of various animal hosts. Applied and Environmental Microbiology, 79(23),7371-7380.
Chi, X., Zhao, X., Wang, W., Niu, Y., Cheng, M., Liu, X., Cui, S. & Yang, W. (2017). Fusion expression of Occludin extracellular loops and an α-helical bundle: A new research model for tight junction. PloS One, 12(4), 1-13.
Chumbler, N.M., Farrow, M.A., Lapierre, L.A., Franklin, J.L. & Lacy, D.B. (2016). Clostridium difficile toxins TcdA and TcdB cause colonic tissue damage by distinct mechanisms. Infection and Immunity, 84(10), 2871-2877.
Comerlato, C.B., Resende, M.C.C.D., Caierão, J. & d'Azevedo, P.A. (2013). Presence of virulence factors in Enterococcus faecalis and Enterococcus faecium susceptible and resistant to vancomycin. Memórias do Instituto Oswaldo Cruz, 108,590-595.
Peraro, M.D. & Van Der Goot, F.G. (2016). Pore-forming toxins: ancient, but never really out of fashion. Nature Reviews Microbiology, 14(2),77-92.
Düzgün, A.Ö., Okumuş, F., Saral, A., Çiçek, A.Ç. & Cinemre, S. (2019). Determination of antibiotic resistance genes and virulence factors in Escherichia coli isolated from Turkish patients with urinary tract infection. Revista da Sociedade Brasileira de Medicina Tropical, 52,1-5
Elmalı, M. & Can, H.Y. (2018). The prevalence, vancomycin resistance and virulence gene profiles of Enterococcus species recovered from different foods of animal origin. Veterinarski Arhiv, 88(1),111-124.
Farhan, Z.A. & AL-Iedani, A.A. (2019). Molecular detection of shiga toxin (stx1 and stx2) and intimin (eae A) genes in Escherichia coli isolated from fecal samples of cattle, sheep, and human in Basrah governorate. Basrah J Vet Res, 18(2),288-305.
Han, W., Liu, B., Cao, B., Beutin, L., Krüger, U., Liu, H., Li, Y., Liu, Y., Feng, L. & Wang, L. (2007). DNA microarray-based identification of serogroups and virulence gene patterns of Escherichia coli isolates associated with porcine postweaning diarrhea and edema disease. Applied and Environmental Microbiology, 73(12), 4082-4088.
Hashem, Y.A., Abdelrahman, K.A. & Aziz, R.K. (2021). Phenotype–genotype correlations and distribution of key virulence factors in Enterococcus faecalis isolated from patients with urinary tract infections. Infection and Drug Resistance, 14, p.1713.
Hassan, M.H. (2020). The cytotoxicity effects of liable and stable enterotoxins produced by uropathogenic Escherichia coli. Systematic Reviews in Pharmacy, 11(12), pp.997-999.
Heidari, H., Hasanpour, S., Ebrahim-Saraie, H.S. & Motamedifar, M. (2017). High incidence of virulence factors among clinical Enterococcus faecalis isolates in Southwestern Iran. Infection & Chemotherapy, 49(1), pp.51-56.
Heydari, F.E., Bonyadian, M., Moshtaghi, H. & Sami, M. (2020). Prevalence and antibiotic resistance profile of Shiga toxin-producing Escherichia coli isolated from diarrheal samples. Iranian Journal of Microbiology, 12(4), p.289.
Hynes, W.L. & Walton, S.L. (2000). Hyaluronidases of Gram-positive bacteria. FEMS Microbiology Letters, 183(2), pp.201-207.
Islam, M.R., Nagao, J.I., Zendo, T. & Sonomoto, K. (2012). Antimicrobial mechanism of lantibiotics. Biochemical Society Transactions, 40(6), 1528-1533.
Jiang, L., Zhu, Y., Luan, P., Xu, J., Ru, G., Fu, J. G., Sang, N., Xiong, Y., He, Y., Lin, G. Q., Wang, J., Zhang, J. & Li, R. (2021). Bacteria-anchoring hybrid liposome capable of absorbing multiple toxins for antivirulence therapy of Escherichia coli infection. ACS Nano, 15(3), 4173–4185.
Kerényi, M., Allison, H. E., Bátai, I., Sonnevend, A., Emödy, L., Plaveczky, N. & Pál, T. (2005). Occurrence of hlyA and sheA genes in extraintestinal Escherichia coli strains. Journal of Clinical Microbiology, 43(6), 2965–2968.
Kotlowski, R., Bernstein, C. N., Sepehri, S. & Krause, D. O. (2007). High prevalence of Escherichia coli belonging to the B2+ D phylogenetic group in inflammatory bowel disease. Gut, 56(5), 669–675.
Krug, S.M. & Fromm, M. (2020). Special issue on “The tight junction and its proteins: more than just a barrier”. International Journal of Molecular Sciences, 21(13),4612.
Leitão, A. L., Costa, M. C., Gabriel, A. F., & Enguita, F. J. (2020). Interspecies communication in Holobionts by non-coding RNA exchange. International Journal of Molecular Sciences, 21(7), 2333.
Lorenz, S. C., Son, I., Maounounen-Laasri, A., Lin, A., Fischer, M., & Kase, J. A. (2013). Prevalence of hemolysin genes and comparison of ehxA subtype patterns in Shiga toxin-producing Escherichia coli (STEC) and non-STEC strains from clinical, food, and animal sources. Applied and Environmental Microbiology, 79(20), 6301–6311.
Lui, W. Y., Lee, W. M., & Cheng, C. Y. (2001). Transforming growth factor-beta3 perturbs the inter-Sertoli tight junction permeability barrier in vitro possibly mediated via its effects on occludin, zonula occludens-1, and claudin-11. Endocrinology, 142(5), 1865–1877.
Marrs, C. F., Zhang, L., Tallman, P., Manning, S. D., Somsel, P., Raz, P., Colodner, R., Jantunen, M. E., Siitonen, A., Saxen, H., & Foxman, B. (2002). Variations in 10 putative uropathogen virulence genes among urinary, faecal and peri-urethral Escherichia coli. Journal of Medical Microbiology, 51(2), 138–142.
Mete, E., Kaleli, İ., Cevahir, N., Demir, M., Akkaya, Y. & Kiriş Satılmış, Ö. (2017). Evaluation of virulence factors in Enterococcus species. Mikrobiyoloji Bulteni, 51(2), 101–114.
Nassour, H. & Dubreuil, J.D. (2014). Escherichia coli STb enterotoxin dislodges claudin-1 from epithelial tight junctions. PloS One, 9(11), 1-11.
Osek, J., Gallien, P., Truszczyñski, M., & Protz, D. (1999). The use of polymerase chain reaction for determination of virulence factors of Escherichia coli strains isolated from pigs in Poland. Comparative Immunology, Microbiology and Infectious Diseases, 22(3), 163–174.
Parmegiani, L., Cognigni, G. E., Ciampaglia, W., Pocognoli, P., Marchi, F. & Filicori, M. (2010). Efficiency of hyaluronic acid (HA) sperm selection. Journal of Assisted Reproduction and Genetics, 27(1), 13–16.
Parvez, S.A. & Rahman, D. (2018). Virulence Factors of Uropathogenic E. coli. Microbiology of Urinary Tract Infections-Microbial Agents and Predisposing Factors,7-21.
Pearce, K. L., Hill, A.. & Tremellen, K. P. (2019). Obesity related metabolic endotoxemia is associated with oxidative stress and impaired sperm DNA integrity. Basic and Clinical Andrology, 29(1), 6.
Popoff, M. R. (2018). ‘Bacterial Toxins’ section in the journal toxins: A fantastic multidisciplinary interplay between bacterial pathogenicity mechanisms, physiological processes, genomic evolution, and subsequent development of identification methods, efficient treatment, and prevention of toxigenic bacteria. Toxins, 10(1).
Roderer, D. & Glockshuber, R. (2017). Assembly mechanism of the α-pore–forming toxin cytolysin A from Escherichia coli. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 372(1726), 20160211.
Rubab, M. & Oh, D. H. (2020). Virulence characteristics and antibiotic resistance profiles of shiga toxin-producing Escherichia coli isolates from diverse sources. Antibiotics, 9(9), 587.
Santo, E., Macedo, C. & Marin, J. M. (2006). Virulence factors of uropathogenic Escherichia coli from a university hospital in Ribeirão Preto, São Paulo, Brazil. Revista do Instituto de Medicina Tropical de São Paulo, 48(4), 185–188.
Semedo, T., Almeida Santos, M., Martins, P., Silva Lopes, M. F., Figueiredo Marques, J. J., Tenreiro, R. & Barreto Crespo, M. T. (2003). Comparative study using type strains and clinical and food isolates to examine hemolytic activity and occurrence of the cyl operon in enterococci. Journal of Clinical Microbiology, 41(6), 2569–2576.
Shokoohizadeh, L., Ekrami, A., Labibzadeh, M., Ali, L. & Alavi, S. M. (2018). Antimicrobial resistance patterns and virulence factors of enterococci isolates in hospitalized burn patients. BMC Research Notes, 11(1), 1.
Soong, G., Parker, D., Magargee, M. & Prince, A. S. (2008). The type III toxins of Pseudomonas aeruginosa disrupt epithelial barrier function. Journal of Bacteriology, 190(8), 2814–2821.
Stępień-Pyśniak, D., Hauschild, T., Kosikowska, U., Dec, M. & Urban-Chmiel, R. (2019). Biofilm formation capacity and presence of virulence factors among commensal Enterococcus spp. from wild birds. Scientific Reports, 9(1), 11204.
Tanaka, K., Caaveiro, J. M., Morante, K., González-Mañas, J. M. & Tsumoto, K. (2015). Structural basis for self-assembly of a cytolytic pore lined by protein and lipid. Nature Communications, 6(1), 6337.
Vankerckhoven, V., Van Autgaerden, T., Vael, C., Lammens, C., Chapelle, S., Rossi, R., Jabes, D. & Goossens, H. (2004). Development of a multiplex PCR for the detection of asa1, gelE, cylA, esp, and hyl genes in enterococci and survey for virulence determinants among European hospital isolates of Enterococcus faecium. Journal of Clinical Microbiology, 42(10), 4473–4479.
Viswanathan, V. K., Koutsouris, A., Lukic, S., Pilkinton, M., Simonovic, I., Simonovic, M. & Hecht, G. (2004). Comparative analysis of EspF from enteropathogenic and enterohemorrhagic Escherichia coli in alteration of epithelial barrier function. Infection and Immunity, 72(6), 3218–3227.
Wiles, T. J., Dhakal, B. K., Eto, D. S. & Mulvey, M. A. (2008). Inactivation of host Akt/protein kinase B signaling by bacterial pore-forming toxins. Molecular Biology of the Cell, 19(4), 1427–1438.
Zeb, Z., Azam, S., Rehman, N., Khan, I., Afzal, S., Sehra, G. E., Ullah, A. & Absar, M. (2021). Phenotypic and molecular characterization of virulence factors of extra-intestinal pathogenic Escherichia coli isolated from patients of Peshawar, Pakistan. Pakistan Journal of Pharmaceutical Sciences, 34(1), 85–94.
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Molecular investigation of cytolysin genes among bacterial isolates recovered from pyospermic patients in Hilla City, Iraq. (2022). Journal of Applied and Natural Science, 14(4), 1110-1118. https://doi.org/10.31018/jans.v14i4.3630
