دورية أكاديمية

The presence of virulence factor genes downregulates uterine AQP3 and alters glutathione peroxidase activity and uterine histopathology in canine pyometra.

التفاصيل البيبلوغرافية
العنوان: The presence of virulence factor genes downregulates uterine AQP3 and alters glutathione peroxidase activity and uterine histopathology in canine pyometra.
المؤلفون: Yazlık MO; Department of Obstetrics and Gynecology, Faculty of Veterinary Medicine, Ankara University, Ankara, Turkey., Müştak İB; Department of Microbiology, Faculty of Veterinary Medicine, Ankara University, Ankara, Turkey., Özkan H; Department of Genetics, Faculty of Veterinary Medicine, Hatay Mustafa Kemal University, Hatay, Turkey., Vural SA; Department of Pathology, Faculty of Veterinary Medicine, Ankara University, Ankara, Turkey., Kaya U; Department of Biostatistics, Faculty of Veterinary Medicine, Hatay Mustafa Kemal University, Hatay, Turkey., Özöner Ö; Department of Pathology, Faculty of Veterinary Medicine, Siirt University, Siirt, Turkey., Mutluer İ; Department of Obstetrics and Gynecology, Faculty of Veterinary Medicine, Ankara University, Ankara, Turkey.; Ankara University Graduate School of Health Sciences, Ankara, Turkey., Altınbaş YF; Department of Obstetrics and Gynecology, Faculty of Veterinary Medicine, Ankara University, Ankara, Turkey.; Ankara University Graduate School of Health Sciences, Ankara, Turkey., Soylu MS; Department of Obstetrics and Gynecology, Faculty of Veterinary Medicine, Ankara University, Ankara, Turkey.; Ankara University Graduate School of Health Sciences, Ankara, Turkey., Vural MR; Department of Obstetrics and Gynecology, Faculty of Veterinary Medicine, Ankara University, Ankara, Turkey.
المصدر: Reproduction in domestic animals = Zuchthygiene [Reprod Domest Anim] 2024 May; Vol. 59 (5), pp. e14615.
نوع المنشور: Journal Article
اللغة: English
بيانات الدورية: Publisher: Paul Parey Scientific Publishers Country of Publication: Germany NLM ID: 9015668 Publication Model: Print Cited Medium: Internet ISSN: 1439-0531 (Electronic) Linking ISSN: 09366768 NLM ISO Abbreviation: Reprod Domest Anim Subsets: MEDLINE
أسماء مطبوعة: Original Publication: Berlin ; Hamburg : Paul Parey Scientific Publishers, c1990-
مواضيع طبية MeSH: Virulence Factors*/genetics , Virulence Factors*/metabolism , Aquaporin 3*/genetics , Aquaporin 3*/metabolism , Pyometra*/veterinary , Pyometra*/microbiology , Pyometra*/pathology , Dog Diseases*/microbiology , Uterus*/pathology , Uterus*/microbiology , Uterus*/metabolism , Escherichia coli*/genetics , Escherichia coli*/pathogenicity , Glutathione Peroxidase*/genetics , Glutathione Peroxidase*/metabolism, Animals ; Female ; Dogs ; Escherichia coli Infections/veterinary ; Escherichia coli Infections/microbiology ; Anti-Bacterial Agents/pharmacology ; Down-Regulation ; Microbial Sensitivity Tests/veterinary
مستخلص: Present study was designed to evaluate the role of virulence factor genes (papG, cnf1 and hylA) in the pathogenesis of canine pyometra. Antimicrobial susceptibility test and detection of virulence genes were performed Escherichia coli (E. coli) detected in uterine swab samples. Animals were divided into two groups based on the presence (VF+, n:14) or absence (VF-, n:7) of the virulence factor genes papG, cnf1 and hylA. Blood and tissue glutathione peroxidase activity, uterine histopathologic analysis and AQP3, ESR1, PGR, OXTR gene expressions were determined in both groups. Statistical analyses were performed using Stata version 15.1. All E. coli isolates were susceptible to amikacin, whereas resistant to ampicillin, amoxicillin/clavulanic acid and lincomycin. None of the isolates were susceptible to cefotaxime. E. coli isolates had at least one virulence gene. The most prevalent gene was fimH (100%), followed by fyuA (95.8%), usp (83.3%), sfa (75%), cnf1 and hlyA (70.8%) genes. Blood GPx activity was greater in VF+ animals. On the other hand, uterine tissue GPx activity was lower in VF+ group compared to the control group. Expression levels of AQP3 were upregulated more than fivefold in VF-dogs compared to the control group. In addition, AQP3 expression levels were found approximately threefold higher in VF (-) than VF (+) group (p < .05). Varying degree of inflammation noted for all animals with pyometra, but the presence of bacteria noted only in VF+ animals. In conclusion, the presence of virulence factor genes does not play a role in the histopathological degree of inflammation, the presence of bacteria was found to vary. Serum GPx activity increased in VF+ animals. While the hormone receptor expressions were similar, AQP expression was upregulated in the absence of virulence factor genes.
(© 2024 The Author(s). Reproduction in Domestic Animals published by Wiley‐VCH GmbH.)
References: Alizade, H., Ghanbarpour, R., & Aflatoonian, M. R. (2014). Virulence genotyping of Escherichia coli isolates from diarrheic and urinary tract infections in relation to phylogeny in southeast of Iran. Tropical Biomedicine, 31(1), 174–182.
Ananias, M., & Yano, T. (2008). Serogroups and virulence genotypes of Escherichia coli isolated from patients with sepsis. Brazilian Journal of Medical and Biological Research, 41, 877–883. https://doi.org/10.1590/s0100‐879x2008001000008.
Arenas, F. A., Díaz, W. A., Leal, C. A., Pérez‐Donoso, J. M., Imlay, J. A., & Vásquez, C. C. (2010). The Escherichia coli btuE gene, encodes a glutathione peroxidase that is induced under oxidative stress conditions. Biochemical and Biophysical Research Communications, 398(4), 690–694. https://doi.org/10.1016/j.bbrc.2010.07.002.
Arora, N. (2007). Role of uropathogenic virulence factors in the pathogenesis of E. coli‐induced cystic endometrial hyperplasia/pyometra complex in the bitch. Doctoral dissertation, University of Melbourne. https://minerva‐access.unimelb.edu.au/items/426d1cdf‐6853‐56ee‐895f‐5603e9b720c0.
Bello‐López, J. M., Cabrero‐Martínez, O. A., Ibáñez‐Cervantes, G., Hernández‐Cortez, C., Pelcastre‐Rodríguez, L. I., Gonzalez‐Avila, L. U., & Castro‐Escarpulli, G. (2019). Horizontal gene transfer and its association with antibiotic resistance in the genus Aeromonas spp. Microorganisms, 7(9), 363. https://doi.org/10.3390/microorganisms7090363.
Bien, J., Sokolova, O., & Bozko, P. (2012). Role of uropathogenic Escherichia coli virulence factors in development of urinary tract infection and kidney damage. International Journal of Nephrology, 2012, 1–15. https://doi.org/10.1155/2012/681473.
Carlini, F., Maroccia, Z., Fiorentini, C., Travaglione, S., & Fabbri, A. (2021). Effects of the Escherichia coli bacterial toxin cytotoxic necrotizing factor 1 on different human and animal cells: A systematic review. International Journal of Molecular Sciences, 22(22), 12610. https://doi.org/10.3390/ijms222212610.
Chen, Y. M., Wright, P. J., Lee, C. S., & Browning, G. F. (2003). Uropathogenic virulence factors in isolates of Escherichia coli from clinical cases of canine pyometra and feces of healthy bitches. Veterinary Microbiology, 94(1), 57–69. https://doi.org/10.1016/s0378‐1135(03)00063‐4.
Chernigova, S. V., Chernigov, Y. V., Vatnikov, Y. A., Kulikov, E. V., Popova, I. A., Shirmanov, V. I., Molchanova, M. A., Likhacheva, I. F., Voronina, Y. Y., & Lukina, D. M. (2019). Special aspects of systemic inflammation course in animals. Veterinary World, 12(7), 932–937. https://doi.org/10.14202/vetworld.2019.932‐937.
CLSI. (2019). Performance Standards for Antimicrobial Susceptibility Testing. 29th ed. CLSI supplement M100. Wayne, PA ABD.
Coggan, J. A., Melville, P. A., Oliveira, C. M. D., Faustino, M., Moreno, A. M., & Benites, N. R. (2008). Microbiological and histopathological aspects of canine pyometra. Brazilian Journal of Microbiology, 39, 477–483. https://doi.org/10.1590/s1517‐838220080003000012.
De Cock, H., Vermeirsch, H., Ducatelle, R., & De Schepper, J. (1997). Immunohistochemical analysis of estrogen receptors in cystic‐endometritis‐pyometra complex in the bitch. Theriogenology, 48(6), 1035–1047. https://doi.org/10.1016/s0093‐691x(97)00330‐0.
de Menezes, M. P., Facin, A. C., Cardozo, M. V., Costa, M. T., & Moraes, P. C. (2021). Evaluation of the resistance profile of bacteria obtained from infected sites of dogs in a veterinary teaching hospital in Brazil: A retrospective study. Topics in Companion Animal Medicine, 42, 100489. https://doi.org/10.1016/j.tcam.2020.100489.
Dhakal, B. K., & Mulvey, M. A. (2012). The UPEC pore‐forming toxin α‐hemolysin triggers proteolysis of host proteins to disrupt cell adhesion, inflammatory, and survival pathways. Cell Host & Microbe, 11(1), 58–69. https://doi.org/10.1016/j.chom.2011.12.003.
Dhaliwal, G. K., England, G. C. W., & Noakes, D. E. (1999). Oestrogen and progesterone receptors in the uterine wall of bitches with cystic endometrial hyperplasia/pyometra. Veterinary Record, 145(16), 455–457. https://doi.org/10.1136/vr.145.16.455.
Donnenberg, M. S., & Welch, R. A. (1996). Virulence determinants of uropathogenic Escherichia coli. In H. L. T. Mobley & J. W. Warren (Eds.), Urinary tract infection: Pathogenesis and clinical management (pp. 135–174). American Society for Microbiology.
Dröge, W. (2002). Free radicals in the physiological control of cell function. Physiological Reviews, 82, 47–95. https://doi.org/10.1152/physrev.00018.2001.
Egenvall, A., Hagman, R., Bonnett, B. N., Hedhammar, A., Olson, P., & Lagerstedt, A. S. (2001). Breed risk of pyometra in insured dogs in Sweden. Journal of Veterinary Internal Medicine, 15(6), 530–538. https://doi.org/10.1892/0891‐6640(2001)015%3C0530:bropii%3E2.3.co;2.
Falzano, L., Quaranta, M. G., Travaglione, S., Filippini, P., Fabbri, A., Viora, M., Donelli, G., & Fiorentini, C. (2003). Cytotoxic necrotizing factor 1 enhances reactive oxygen species‐dependent transcription and secretion of proinflammatory cytokines in human uroepithelial cells. Infection and Immunity, 71(7), 4178–4181. 10.1128%2FIAI.71.7.4178‐4181.2003.
Fieni, F., Topie, E., & Gogny, A. (2014). Medical treatment for pyometra in dogs. Reproduction in Domestic Animals, 49, 28–32. https://doi.org/10.1111/rda.12302.
Gunther, N. W., IV, Snyder, J. A., Lockatell, V., Blomfield, I., Johnson, D. E., & Mobley, H. L. (2002). Assessment of virulence of uropathogenic Escherichia coli type 1 fimbrial mutants in which the invertible element is phase‐locked on or off. Infection and Immunity, 70(7), 3344–3354. https://doi.org/10.1128/iai.70.7.3344‐3354.2002.
Hagman, R. (2018). Pyometra in small animals. Veterinary Clinics: Small Animal Practice, 48(4), 639–661. https://doi.org/10.1016/j.cvsm.2018.03.001.
Hagman, R., & Kühn, I. (2002). Escherichia coli strains isolated from the uterus and urinary bladder of bitches suffering from pyometra: Comparison by restriction enzyme digestion and pulsed‐field gel electrophoresis. Veterinary Microbiology, 84(1–2), 143–153. https://doi.org/10.1016/S0378‐1135(01)00449‐7.
Halliwell, B., & Whiteman, M. (2004). Measuring reactive species and oxidative damage in vivo and in cell culture: How should you do it and what do the results mean? British Journal of Pharmacology, 142(2), 231–255. https://doi.org/10.1038/sj.bjp.0705776.
Henriques, S. C. R. D. B. (2016). Escherichia coli: Host interactions in the pathogenesis of canine pyometra bitch. Doctoral dissertation, University of Melbourne. https://www.repository.utl.pt/handle/10400.5/12273.
Hull, R. A., Gill, R. E., Hsu, P. A. T. R. I. C. I. A., Minshew, B. H., & Falkow, S. (1981). Construction and expression of recombinant plasmids encoding type 1 or D‐mannose‐resistant pili from a urinary tract infection Escherichia coli isolate. Infection and Immunity, 33(3), 933–938. https://doi.org/10.1128/iai.33.3.933‐938.1981.
Johnson, J. R., & Stell, A. L. (2000). Extended virulence genotypes of Escherichia coli strains from patients with urosepsis in relation to phylogeny and host compromise. The Journal of Infectious Diseases, 181(1), 261–272. https://doi.org/10.1086/315217.
Karimian, A., Momtaz, H., & Madani, M. (2012). Detection of uropathogenic Escherichia coli virulence factors in patients with urinary tract infections in Iran. African Journal of Microbiology Research, 6(39), 6811–6816. https://doi.org/10.5897/AJMR12.1462.
Krekeler, N., Marenda, M. S., Browning, G. F., Holden, K. M., Charles, J. A., & Wright, P. J. (2012). Uropathogenic virulence factor FimH facilitates binding of uteropathogenic Escherichia coli to canine endometrium. Comparative Immunology, Microbiology and Infectious Diseases, 35(5), 461–467. https://doi.org/10.1016/j.cimid.2012.04.001.
Krekeler, N., Marenda, M. S., Browning, G. F., Holden, K. M., Charles, J. A., & Wright, P. J. (2013). The role of type 1, P and S fimbriae in binding of Escherichia coli to the canine endometrium. Veterinary Microbiology, 164(3–4), 399–404. https://doi.org/10.1016/j.vetmic.2013.02.028.
Livak, K. J., & Schmittgen, T. D. (2001). Analysis of relative gene expression data using real‐time quantitative PCR and the 2−ΔΔCT method. Methods, 25(4), 402–408. https://doi.org/10.1006/meth.2001.1262.
Lopes, C. E., De Carli, S., Riboldi, C. I., De Lorenzo, C., Panziera, W., Driemeier, D., & Siqueira, F. M. (2021). Pet pyometra: Correlating bacteria pathogenicity to endometrial histological changes. Pathogens, 10(7), 833. https://doi.org/10.3390/pathogens10070833.
Maluta, R. P., Borges, C. A., Beraldo, L. G., Cardozo, M. V., Voorwald, F. A., Santana, A. M., Rigobelo, E. C., Toniollo, G. H., & Ávila, F. A. (2014). Frequencies of virulence genes and pulse field gel electrophoresis fingerprints in Escherichia coli isolates from canine pyometra. The Veterinary Journal, 202(2), 393–395. https://doi.org/10.1016/j.tvjl.2014.08.016.
Mare, A. D., Ciurea, C. N., Man, A., Tudor, B., Moldovan, V., Decean, L., & Toma, F. (2021). Enteropathogenic Escherichia coli—A summary of the literature. Gastroenterology Insights, 12(1), 28–40. https://doi.org/10.3390/gastroent12010004.
Mateus, L., Henriques, S., Merino, C., Pomba, C., da Costa, L. L., & Silva, E. (2013). Virulence genotypes of Escherichia coli canine isolates from pyometra, cystitis and fecal origin. Veterinary Microbiology, 166(3–4), 590–594. https://doi.org/10.1016/j.vetmic.2013.07.018.
Meli, R., Pirozzi, C., & Pelagalli, A. (2018). New perspectives on the potential role of aquaporins (AQPs) in the physiology of inflammation. Frontiers in Physiology, 9, 101. https://doi.org/10.3389/fphys.2018.00101.
Millemann, Y., Gaubert, S., Remy, D., & Colmin, C. (2000). Evaluation of IS 200‐PCR and comparison with other molecular markers to trace salmonella enterica subsp. enterica serotype Typhimurium bovine isolates from farm to meat. Journal of Clinical Microbiology, 38(6), 2204–2209.
Ozkan, H., & Kerman, E. (2020). Comparative evaluation of RNAlater solution and snap frozen methods for gene expression studies in different tissues. Romanian Journal of Laboratory Medicine, 28(3), 287–297. https://doi.org/10.2478/rrlm‐2020‐0024.
Picard, B., Garcia, J. S., Gouriou, S., Duriez, P., Brahimi, N., Bingen, E., Elion, E., & Denamur, E. (1999). The link between phylogeny and virulence in Escherichia coli extraintestinal infection. Infection and Immunity, 67(2), 546–553. 10.1128%2Fiai.67.2.546‐553.1999.
Qian, C., & Hou, J. (2017). Escherichia coli virulence influences the roles of sex hormone receptors in female dogs with simulated pyometra. Experimental and Therapeutic Medicine, 14(4), 3013–3021. https://doi.org/10.3892/etm.2017.4894.
Quinn, P. J., Carter, M. E., Markey, B., & Carter, G. R. (1994). Clinical veterinary microbiology. Wolfe.
Ragnarsdóttir, B., Lutay, N., Grönberg‐Hernandez, J., Köves, B., & Svanborg, C. (2011). Genetics of innate immunity and UTI susceptibility. Nature Reviews Urology, 8(8), 449–468. https://doi.org/10.1038/nrurol.2011.100.
Rautela, R., & Katiyar, R. (2019). Review on canine pyometra, oxidative stress and current trends in diagnostics. Asian Pacific Journal of Reproduction, 8(2), 45–55. https://doi.org/10.4103/2305‐0500.254645.
Rio, D. C., Ares, M., Hannon, G. J., & Nilsen, T. W. (2010). Purification of RNA using TRIzol (TRI reagent). Cold Spring Harbor Protocols, 2010(6), pdb.prot5439. https://doi.org/10.1101/pdb.prot5439.
Sándor, S., Tátrai, K., Czeibert, K., Egyed, B., & Kubinyi, E. (2021). CDKN2A gene expression as a potential aging biomarker in dogs. Frontiers in Veterinary Science, 8, 660435. https://doi.org/10.3389/fvets.2021.660435.
Schmidt, H., & Hensel, M. (2004). Pathogenicity islands in bacterial pathogenesis. Clinical Microbiology Reviews, 17(1), 14–56. https://doi.org/10.1128/cmr.17.1.14‐56.2004.
Seetharama, S., Cavalieri, S. J., & Snyder, I. S. (1988). Immune response to Escherichia coli alpha‐hemolysin in patients. Journal of Clinical Microbiology, 26(5), 850–856. https://doi.org/10.1128/JCM.26.5.850‐856.1988.
Siqueira, A. K., Ribeiro, M. G., Leite, D. D. S., Tiba, M. R., de Moura, C., Lopes, M. D., Prestes, N. C., Salerno, T., & da Silva, A. V. (2009). Virulence factors in Escherichia coli strains isolated from urinary tract infection and pyometra cases and from feces of healthy dogs. Research in Veterinary Science, 86(2), 206–210. https://doi.org/10.1016/j.rvsc.2008.07.018.
Smith, Y. C., Rasmussen, S. B., Grande, K. K., Conran, R. M., & O'Brien, A. D. (2008). Hemolysin of uropathogenic Escherichia coli evokes extensive shedding of the uroepithelium and hemorrhage in bladder tissue within the first 24 hours after intraurethral inoculation of mice. Infection and Immunity, 76(7), 2978–2990. https://doi.org/10.1128/IAI.00075‐08.
Tavares Pereira, M., Nowaczyk, R., Payan‐Carreira, R., Miranda, S., Aslan, S., Kaya, D., & Kowalewski, M. P. (2021). Selected uterine immune events associated with the establishment of pregnancy in the dog. Frontiers in Veterinary Science, 7, 625921. https://doi.org/10.3389/fvets.2020.625921.
Thon, P., Rahmel, T., Ziehe, D., Palmowski, L., Marko, B., Nowak, H., & Rump, K. (2024). AQP3 and AQP9—Contrary players in sepsis? International Journal of Molecular Sciences, 25(2), 1209. https://doi.org/10.3390/ijms25021209.
Ververidis, H. N., Boscos, C. M., Stefanakis, A., Saratsis, P., Stamou, A. I., & Krambovitis, E. (2004). Serum estradiol‐17β, progesterone and respective uterine cytosol receptor concentrations in bitches with spontaneous pyometra. Theriogenology, 62(3–4), 614–623. https://doi.org/10.1016/j.theriogenology.2003.11.011.
Welch, R. A., Burland, V., Plunkett, G., III, Redford, P., Roesch, P., Rasko, D., Buckles, E. L., Liou, S.‐R., Boutin, A., Hackett, J., Stroud, D., Mayhew, G. F., Rose, D. J., Zhou, S., Schwartz, D. C., Perna, N. T., Mobley, H. L. T., Donnenberg, M. S., & Blattner, F. R. (2002). Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli. Proceedings of the National Academy of Sciences, 99(26), 17020–17024. https://doi.org/10.1073/pnas.252529799.
Wiles, T. J., Kulesus, R. R., & Mulvey, M. A. (2008). Origins and virulence mechanisms of uropathogenic Escherichia coli. Experimental and Molecular Pathology, 85(1), 11–19. https://doi.org/10.1016/j.yexmp.2008.03.007.
Wiles, T. J., & Mulvey, M. A. (2013). The RTX pore‐forming toxin α‐hemolysin of uropathogenic Escherichia coli: Progress and perspectives. Future Microbiology, 8(1), 73–84. https://doi.org/10.2217/fmb.12.131.
Xavier, R. G. C., Santana, C. H., da Silva, P. H. S., Paraguassú, A. O., Nicolino, R. R., Freitas, P. M. C., Santos, R. L., & Silva, R. O. S. (2024). Association between bacterial pathogenicity, endometrial histological changes and clinical prognosis in canine pyometra. Theriogenology, 214, 118–123. https://doi.org/10.1016/j.theriogenology.2023.10.007.
Yazlık, M., Müştak, İ., Unal, G., & Kaya, U. (2022). The Association of Intrauterine Antimicrobial Resistant Trueperella pyogenes with cytological endometrial inflammation status in repeat breeder cows. Pakistan Journal of Zoology, 54(1), 115–121. https://doi.org/10.17582/journal.pjz/20200127120153.
Yazlık, M. O., Mutluer, İ., Kaya, U., Özkan, H., Müştak, İ. B., Çolakoğlu, H. E., Altınbaş, Y. F., & Vural, M. R. (2023). The role of nutritional‐immunological indices in estimating serum LPS and antioxidant enzyme activity and sepsis status in female dogs with pyometra caused by E. coli. Animal Reproduction Science, 255, 107276. https://doi.org/10.1016/j.anireprosci.2023.107276.
Yazlık, M. O., Mutluer, İ., Yıldırım, M., Kaya, U., Çolakoğlu, H. E., & Vural, M. R. (2022). The evaluation of SIRS status with hemato‐biochemical indices in bitches affected from pyometra and the usefulness of these indices as a potential diagnostic tool. Theriogenology, 193, 120–127. https://doi.org/10.1016/j.theriogenology.2022.09.015.
معلومات مُعتمدة: 120O543 Türkiye Bilimsel ve Teknolojik Araştırma Kurumu
فهرسة مساهمة: Keywords: aquaporin; canine; glutathione peroxidase; pyometra; virulence factor genes
المشرفين على المادة: 0 (Virulence Factors)
158801-98-0 (Aquaporin 3)
EC 1.11.1.9 (Glutathione Peroxidase)
0 (Anti-Bacterial Agents)
تواريخ الأحداث: Date Created: 20240527 Date Completed: 20240527 Latest Revision: 20240603
رمز التحديث: 20240603
DOI: 10.1111/rda.14615
PMID: 38798181
قاعدة البيانات: MEDLINE
الوصف
تدمد:1439-0531
DOI:10.1111/rda.14615