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Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Effect of lipopolysaccharide on the expression of inflammatory mRNAs and microRNAs in the mouse oviduct

Katheryn L. Cerny A , Rosanne A. C. Ribeiro A , Qing Li A , James C. Matthews A and Phillip J. Bridges A B
+ Author Affiliations
- Author Affiliations

A Department of Animal and Food Sciences, University of Kentucky, Lexington, KY 40546, USA.

B Corresponding author. Email: phillip.bridges@uky.edu

Reproduction, Fertility and Development 30(4) 600-608 https://doi.org/10.1071/RD17241
Submitted: 13 December 2016  Accepted: 25 August 2017   Published: 26 September 2017

Abstract

Infection with Gram-negative bacteria is a major cause of aberrant inflammation in the oviduct; consequences can include tubal-based infertility and/or ectopic pregnancy. Understanding the inflammatory response is necessary for the development of novel treatment options that counter inflammation-induced infertility. The aim of the present study was to determine the effect of intraperitoneal (i.p.) administration of Escherichia coli-derived lipopolysaccharide (LPS) on the acute expression of inflammatory mRNAs and microRNAs (miRNAs) in the oviduct. On the day of oestrus, 6- to 8-week-old CD1 mice were injected i.p. with 0, 2 or 10 µg LPS in 100 μL phosphate-buffered saline. Mice were killed 24 h later and the oviducts collected for gene expression analyses. The effect of treatment on the expression of mRNAs and miRNAs was evaluated by one-way analysis of variance (ANOVA), with treatment means of differentially expressed (P < 0.05) transcripts separated using Scheffé’s test. LPS treatment affected 49 of 179 targeted inflammatory mRNAs and 51 of 578 miRNAs (P < 0.05). The identity of differentially expressed miRNAs predicted as regulators of chemokine and interleukin ligand mRNAs was then extracted using the microRNA.org database. The results of the present study indicate that systemic treatment with LPS induces a robust inflammatory response in the oviducts of mice, and identify key mRNAs and putative miRNAs modulating this effect.

Additional keywords: cytokine, gene expression, inflammation, nanostring.


References

Aggarwal, B. B., Gupta, S. C., and Kim, J. H. (2012). Historical perspectives on tumor necrosis factor and its superfamily: 25 years later, a golden journey. Blood 119, 651–665.
Historical perspectives on tumor necrosis factor and its superfamily: 25 years later, a golden journey.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhs1KjtLw%3D&md5=b770d67fa11064115c7e24533b5e0df6CAS |

Balasubramaniam, E. S., Van Noorden, S., and El-Bahrawy, M. (2012). The expression of interleukin (IL)-6, IL-8, and their receptors in fallopian tubes with ectopic tubal gestation. Fertil. Steril. 98, 898–904.
The expression of interleukin (IL)-6, IL-8, and their receptors in fallopian tubes with ectopic tubal gestation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XpvFOlsL4%3D&md5=8e82db627842355a4a6101cc3d40463dCAS |

Barbai, T., Fejos, Z., Puskas, L. G., Timar, J., and Raso, E. (2015). The importance of microenvironment: the role of CCL8 in metastasis formation of melanoma. Oncotarget 6, 29111–29128.
The importance of microenvironment: the role of CCL8 in metastasis formation of melanoma.Crossref | GoogleScholarGoogle Scholar |

Barnett, R. E., Conklin, D. J., Ryan, L., Keskey, R. C., Ramjee, V., Sepulveda, E. A., Srivastava, S., Bhatnagar, A., and Cheadle, W. G. (2016). Anti-inflammatory effects of miR-21 in the macrophage response to peritonitis. J. Leukoc. Biol. 99, 361–371.
Anti-inflammatory effects of miR-21 in the macrophage response to peritonitis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhtV2js7jE&md5=d2cee404aa4de7ed67e5254a73bfbefdCAS |

Batra, S., Cai, S., Balamayooran, G., and Jeyaseelan, S. (2012). Intrapulmonary administration of leukotriene B(4) augments neutrophil accumulation and responses in the lung to Klebsiella infection in CXCL1 knockout mice. J. Immunol. 188, 3458–3468.
Intrapulmonary administration of leukotriene B(4) augments neutrophil accumulation and responses in the lung to Klebsiella infection in CXCL1 knockout mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XksVOltLo%3D&md5=632fb564d7c694ed9126a74895358352CAS |

Betel, D., Koppal, A., Agius, P., Sander, C., and Leslie, C. (2010). Comprehensive modeling of microRNA targets predicts functional non-conserved and non-canonical sites. Genome Biol. 11, R90.
Comprehensive modeling of microRNA targets predicts functional non-conserved and non-canonical sites.Crossref | GoogleScholarGoogle Scholar |

Bridges, P. J., Jeoung, M., Shim, S., Park, J. Y., Lee, J. E., Sapsford, L. A., Trudgen, K., Ko, C., Gye, M. C., and Jo, M. (2012). Hematopoetic prostaglandin D synthase: an ESR1-dependent oviductal epithelial cell synthase. Endocrinology 153, 1925–1935.
Hematopoetic prostaglandin D synthase: an ESR1-dependent oviductal epithelial cell synthase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XlsVSmsb8%3D&md5=131702e15c9a78273a6850e1de1c1363CAS |

Brocker, C., Thompson, D., Matsumoto, A., Nebert, D. W., and Vasiliou, V. (2010). Evolutionary divergence and functions of the human interleukin (IL) gene family. Hum. Genomics 5, 30–55.
Evolutionary divergence and functions of the human interleukin (IL) gene family.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhvVeks7w%3D&md5=3c30a20e3f17b731713e9503490c3d3eCAS |

Caligioni, C. S. (2009). Assessing reproductive status/stages in mice. Curr. Protoc. Neurosci. Appendix 4, Appendix 4I.
Assessing reproductive status/stages in mice.Crossref | GoogleScholarGoogle Scholar |

Centers for Disease Control and Prevention (2016). ‘Sexually Transmitted Diseases Surveillance 2015.’ (U.S. Department of Health and Human Services: Atlanta.)

Commins, S. P., Borish, L., and Steinke, J. W. (2010). Immunologic messenger molecules: cytokines, interferons, and chemokines. J. Allergy Clin. Immunol. 125, S53–S72.
Immunologic messenger molecules: cytokines, interferons, and chemokines.Crossref | GoogleScholarGoogle Scholar |

Creanga, A. A., Shapiro-Mendoza, C. K., Bish, C. L., Zane, S., Berg, C. J., and Callaghan, W. M. (2011). Trends in ectopic pregnancy mortality in the United States: 1980–2007. Obstet. Gynecol. 117, 837–843.
Trends in ectopic pregnancy mortality in the United States: 1980–2007.Crossref | GoogleScholarGoogle Scholar |

Darville, T., Andrews, C. W., Laffoon, K. K., Shymasani, W., Kishen, L. R., and Rank, R. G. (1997). Mouse strain-dependent variation in the course and outcome of chlamydial genital tract infection is associated with differences in host response. Infect. Immun. 65, 3065–3073.
| 1:CAS:528:DyaK2sXkvVakt7c%3D&md5=30a16aafddd4100864a2958e1fad1375CAS |

Darville, T., Andrews, C. W., Sikes, J. D., Fraley, P. L., Braswell, L., and Rank, R. G. (2001). Mouse strain-dependent chemokine regulation of the genital tract T helper cell type 1 immune response. Infect. Immun. 69, 7419–7424.
Mouse strain-dependent chemokine regulation of the genital tract T helper cell type 1 immune response.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXos1Onsrc%3D&md5=7fd1047586daacd1cd10f8b8637d8c57CAS |

Deb, K., Chaturvedi, M. M., and Jaiswal, Y. K. (2004). A ‘minimum dose’ of lipopolysaccharide required for implantation failure: assessment of its effect on the maternal reproductive organs and interleukin-1alpha expression in the mouse. Reproduction 128, 87–97.
A ‘minimum dose’ of lipopolysaccharide required for implantation failure: assessment of its effect on the maternal reproductive organs and interleukin-1alpha expression in the mouse.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXms1eltr8%3D&md5=b78c1559602ef204d86671d9c265b61dCAS |

Deguchi, T., Nakane, K., Yasuda, M., and Maeda, S. (2010). Emergence and spread of drug resistant Neisseria gonorrhoeae. J. Urol. 184, 851–858.
Emergence and spread of drug resistant Neisseria gonorrhoeae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXpvVejtLk%3D&md5=27a9a8909cb055496338004b60f8a13bCAS |

Diamond, A. K., Sweet, L. M., Oppenheimer, K. H., Bradley, D. F., and Phillippe, M. (2007). Modulation of monocyte chemotactic protein-1 expression during lipopolysaccharide-induced preterm delivery in the pregnant mouse. Reprod. Sci. 14, 548–559.
Modulation of monocyte chemotactic protein-1 expression during lipopolysaccharide-induced preterm delivery in the pregnant mouse.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlCgtbnK&md5=cc688fdd6a756b74786f402afc3aa814CAS |

Donnez, J., and Casanas-Roux, F. (1988). Histology: a prognostic factor in proximal tubal occlusion. Eur. J. Obstet. Gynecol. Reprod. Biol. 29, 33–38.
Histology: a prognostic factor in proximal tubal occlusion.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1M7jslKlsQ%3D%3D&md5=72d9005b618b07203c7bee8466cb0fc8CAS |

Edgar, R., Domrachev, M., and Lash, A. E. (2002). Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 30, 207–210.
Gene Expression Omnibus: NCBI gene expression and hybridization array data repository.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xht12kurs%3D&md5=6fe8e6b063acfc9d4a5de6f104333bacCAS |

Feinen, B., and Russell, M. W. (2012). Contrasting roles of IL-22 and IL-17 in murine genital tract infection by Neisseria gonorrhoeae. Front. Immunol. 3, 11.
Contrasting roles of IL-22 and IL-17 in murine genital tract infection by Neisseria gonorrhoeae.Crossref | GoogleScholarGoogle Scholar |

Feng, Y., Zou, S., Weijdegard, B., Chen, J., Cong, Q., Fernandez-Rodriguez, J., Wang, L., Billig, H., and Shao, R. (2014). The onset of human ectopic pregnancy demonstrates a differential expression of miRNAs and their cognate targets in the Fallopian tube. Int. J. Clin. Exp. Pathol. 7, 64–79.

Fernandez, E. J., and Lolis, E. (2002). Structure, function, and inhibition of chemokines. Annu. Rev. Pharmacol. Toxicol. 42, 469–499.
Structure, function, and inhibition of chemokines.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhvFKntr0%3D&md5=bb4aaac32d6bca834b5786952bc249d4CAS |

García-Ulloa, A. C., and Arrieta, O. (2005). Tubal occlusion causing infertility due to an excessive inflammatory response in patients with predisposition for keloid formation. Med. Hypotheses 65, 908–914.
Tubal occlusion causing infertility due to an excessive inflammatory response in patients with predisposition for keloid formation.Crossref | GoogleScholarGoogle Scholar |

Hobbs, M. M., Anderson, J. E., Balthazar, J. T., Kandler, J. L., Carlson, R. W., Ganguly, J., Begum, A. A., Duncan, J. A., Lin, J. T., Sparling, P. F., Jerse, A. E., and Shafer, W. M. (2013). Lipid A’s structure mediates Neisseria gonorrhoeae fitness during experimental infection of mice and men. MBio 4, e00892-13.
Lipid A’s structure mediates Neisseria gonorrhoeae fitness during experimental infection of mice and men.Crossref | GoogleScholarGoogle Scholar |

Ibrahim, S., Salilew-Wondim, D., Rings, F., Hoelker, M., Neuhoff, C., Tholen, E., Looft, C., Schellander, K., and Tesfaye, D. (2015). Expression pattern of inflammatory response genes and their regulatory microRNAs in bovine oviductal cells in response to lipopolysaccharide: implication for early embryonic development. PLoS One 10, e0119388.
Expression pattern of inflammatory response genes and their regulatory microRNAs in bovine oviductal cells in response to lipopolysaccharide: implication for early embryonic development.Crossref | GoogleScholarGoogle Scholar |

Igietseme, J. U., Omosun, Y., Partin, J., Goldstein, J., He, Q., Joseph, K., Ellerson, D., Ansari, U., Eko, F. O., Bandea, C., Zhong, G., and Black, C. M. (2013). Prevention of Chlamydia-induced infertility by inhibition of local caspase activity. J. Infect. Dis. 207, 1095–1104.
Prevention of Chlamydia-induced infertility by inhibition of local caspase activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjsVKlur4%3D&md5=615e5c4a9ae986ba7d11a2606af4a73fCAS |

Jablonski, K. A., Gaudet, A. D., Amici, S. A., Popovich, P. G., and Guerau-de-Arellano, M. (2016). Control of the inflammatory macrophage transcriptional signature by miR-155. PLoS One 11, e0159724.
Control of the inflammatory macrophage transcriptional signature by miR-155.Crossref | GoogleScholarGoogle Scholar |

Jeoung, M., and Bridges, P. J. (2011). Cyclic regulation of apoptotic gene expression in the mouse oviduct. Reprod. Fertil. Dev. 23, 638–644.
Cyclic regulation of apoptotic gene expression in the mouse oviduct.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXpvVWqurw%3D&md5=695c563b8189280a186501c33ba51ea9CAS |

Jeoung, M., Lee, S., Hawng, H. K., Cheon, Y. P., Jeong, Y. K., Gye, M. C., Iglarz, M., Ko, C., and Bridges, P. J. (2010). Identification of a novel role for endothelins within the oviduct. Endocrinology 151, 2858–2867.
Identification of a novel role for endothelins within the oviduct.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXnsVyqtbo%3D&md5=7a54e0bd13cd6a4225f58635e4279b86CAS |

Jin, L., Batra, S., Douda, D. N., Palaniyar, N., and Jeyaseelan, S. (2014). CXCL1 contributes to host defense in polymicrobial sepsis via modulating T cell and neutrophil functions. J. Immunol. 193, 3549–3558.
CXCL1 contributes to host defense in polymicrobial sepsis via modulating T cell and neutrophil functions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhsFOnsLrN&md5=8e2be24f3aac2240a5f5ea4c71cad822CAS |

Kessler, M., Zielecki, J., Thieck, O., Mollenkopf, H. J., Fotopoulou, C., and Meyer, T. F. (2012). Chlamydia trachomatis disturbs epithelial tissue homeostasis in fallopian tubes via paracrine Wnt signaling. Am. J. Pathol. 180, 186–198.
Chlamydia trachomatis disturbs epithelial tissue homeostasis in fallopian tubes via paracrine Wnt signaling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhs1Oqtb0%3D&md5=76cc01f4c19344075a0399577998dac5CAS |

Koomey, M. (2001). Implications of molecular contacts and signaling initiated by Neisseria gonorrhoeae. Curr. Opin. Microbiol. 4, 53–57.
Implications of molecular contacts and signaling initiated by Neisseria gonorrhoeae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhtlKlsL0%3D&md5=eb94fb0d054b9beef819fd58c4dd46f7CAS |

Koti, M., Siu, A., Clement, I., Bidarimath, M., Turashvili, G., Edwards, A., Rahimi, K., Masson, A. M., and Squire, J. A. (2015). A distinct pre-existing inflammatory tumour microenvironment is associated with chemotherapy resistance in high-grade serous epithelial ovarian cancer. Br. J. Cancer 112, 1215–1222.
A distinct pre-existing inflammatory tumour microenvironment is associated with chemotherapy resistance in high-grade serous epithelial ovarian cancer.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2MnpvVGgtA%3D%3D&md5=57ad7b685448ff1194d0ced611e9fb1cCAS |

Kowsar, R., Hambruch, N., Liu, J., Shimizu, T., Pfarrer, C., and Miyamoto, A. (2013). Regulation of innate immune function in bovine oviduct epithelial cells in culture: the homeostatic role of epithelial cells in balancing Th1/Th2 response. J. Reprod. Dev. 59, 470–478.
Regulation of innate immune function in bovine oviduct epithelial cells in culture: the homeostatic role of epithelial cells in balancing Th1/Th2 response.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvVClsr%2FI&md5=11cadf665f1be10c6c0aeb10d0d99eefCAS |

Le, Y., Zhou, Y., Iribarren, P., and Wang, J. (2004). Chemokines and chemokine receptors: their manifold roles in homeostasis and disease. Cell. Mol. Immunol. 1, 95–104.
| 1:CAS:528:DC%2BD2cXmvF2rs7c%3D&md5=24f110e0f8ba36377bd5b1bc4bd7f933CAS |

Levene, H. (1960). ‘Contributions to Probability and Statistics: Essays in Honor of Harold Hotelling.’ (Eds I. Olkin et al.) pp. 278–292. (Stanford University Press: Stanford, CA.)

Liu, Y., Egilmez, N. K., and Russell, M. W. (2013). Enhancement of adaptive immunity to Neisseria gonorrhoeae by local intravaginal administration of microencapsulated interleukin 12. J. Infect. Dis. 208, 1821–1829.
Enhancement of adaptive immunity to Neisseria gonorrhoeae by local intravaginal administration of microencapsulated interleukin 12.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhslajtbjE&md5=f49a587334dc537cbbe7f6b56bf8292aCAS |

Livak, K. J., and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25, 402–408.
Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhtFelt7s%3D&md5=27001fc4d390214adec9d2e6245c9fd6CAS |

Mårdh, P. A. (2004). Tubal factor infertility, with special regard to chlamydial salpingitis. Curr. Opin. Infect. Dis. 17, 49–52.
Tubal factor infertility, with special regard to chlamydial salpingitis.Crossref | GoogleScholarGoogle Scholar |

Maxion, H. K., and Kelly, K. A. (2002). Chemokine expression patterns differ within anatomically distinct regions of the genital tract during Chlamydia trachomatis infection. Infect. Immun. 70, 1538–1546.
Chemokine expression patterns differ within anatomically distinct regions of the genital tract during Chlamydia trachomatis infection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhsFSltrY%3D&md5=105c7e8b0638101e35bef8ffdb122e4eCAS |

Mayorga, M., Iborra, A., Estany, S., and Martinez, P. (2004). Protective effect of vitamin E in an animal model of LPS-induced inflammation. Am. J. Reprod. Immunol. 52, 356–361.
Protective effect of vitamin E in an animal model of LPS-induced inflammation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2M%2Fjs1ajuw%3D%3D&md5=68e9820cee5fbd6bcd1f870880d80a4bCAS |

Nesargikar, P. N., Spiller, B., and Chavez, R. (2012). The complement system: history, pathways, cascade and inhibitors. Eur. J. Microbiol. Immunol. (Bp.) 2, 103–111.
The complement system: history, pathways, cascade and inhibitors.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2cflslCisA%3D%3D&md5=e7c610120e952e84abafa95659b0bb98CAS |

Perfettini, J. L., Darville, T., Gachelin, G., Souque, P., Huerre, M., Dautry-Varsat, A., and Ojcius, D. M. (2000). Effect of Chlamydia trachomatis infection and subsequent tumor necrosis factor alpha secretion on apoptosis in the murine genital tract. Infect. Immun. 68, 2237–2244.
Effect of Chlamydia trachomatis infection and subsequent tumor necrosis factor alpha secretion on apoptosis in the murine genital tract.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXitFels7w%3D&md5=3703c6d0e233be9f29a4a382ebccbfffCAS |

Phillippe, M., Diamond, A. K., Sweet, L. M., Oppenheimer, K. H., and Bradley, D. F. (2011). Expression of coagulation-related protein genes during LPS-induced preterm delivery in the pregnant mouse. Reprod. Sci. 18, 1071–1079.
Expression of coagulation-related protein genes during LPS-induced preterm delivery in the pregnant mouse.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsV2isL3P&md5=6f31d920d80cb25cc8d441bd72ab6179CAS |

Punnonen, R., Soderstrom, K. O., and Alanen, A. (1984). Isthmic tubal occlusion: etiology and histology. Acta Eur. Fertil. 15, 39–42.
| 1:STN:280:DyaL2c3is12ksw%3D%3D&md5=f85ef6a2627c49fd79e7e1e350259ed7CAS |

Raetz, C. R., and Whitfield, C. (2002). Lipopolysaccharide endotoxins. Annu. Rev. Biochem. 71, 635–700.
Lipopolysaccharide endotoxins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xos1Clt7w%3D&md5=a9994ee319d897f6b094cb7c977e7f42CAS |

Rasmussen, S. J., Eckmann, L., Quayle, A. J., Shen, L., Zhang, Y. X., Anderson, D. J., Fierer, J., Stephens, R. S., and Kagnoff, M. F. (1997). Secretion of proinflammatory cytokines by epithelial cells in response to Chlamydia infection suggests a central role for epithelial cells in chlamydial pathogenesis. J. Clin. Invest. 99, 77–87.
Secretion of proinflammatory cytokines by epithelial cells in response to Chlamydia infection suggests a central role for epithelial cells in chlamydial pathogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjvFKjug%3D%3D&md5=d4894fba245bfdf194222b13eb900b03CAS |

Scheffé, H. (1959). ‘The Analysis of Variance.’ (Wiley: New York.)

Shao, R. (2010). Understanding the mechanisms of human tubal ectopic pregnancies: new evidence from knockout mouse models. Hum. Reprod. 25, 584–587.
Understanding the mechanisms of human tubal ectopic pregnancies: new evidence from knockout mouse models.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXitFeit7o%3D&md5=a589f5a035e7dbdb1fc7eb14bc677839CAS |

Shapiro, S. S., and Wilk, M. B. (1965). An analysis of variance test for normality (complete samples). Biometrika 52, 591–611.
An analysis of variance test for normality (complete samples).Crossref | GoogleScholarGoogle Scholar |

Shaw, J. L., Dey, S. K., Critchley, H. O., and Horne, A. W. (2010). Current knowledge of the aetiology of human tubal ectopic pregnancy. Hum. Reprod. Update 16, 432–444.
Current knowledge of the aetiology of human tubal ectopic pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cvhtlyjtg%3D%3D&md5=5ace4d6f505de848f92edab9ac3599d5CAS |

Shibahara, H., Hirano, Y., Ayustawati, , Kikuchi, K., Taneichi, A., Fujiwara, H., Takamizawa, S., and Sato, I. (2003). Chemokine bioactivity of RANTES is elevated in the sera of infertile women with past Chlamydia trachomatis infection. Am. J. Reprod. Immunol. 49, 169–173.
Chemokine bioactivity of RANTES is elevated in the sera of infertile women with past Chlamydia trachomatis infection.Crossref | GoogleScholarGoogle Scholar |

Steffl, M., Schweiger, M., Sugiyama, T., and Amselgruber, W. M. (2008). Review of apoptotic and non-apoptotic events in non-ciliated cells of the mammalian oviduct. Ann. Anat. 190, 46–52.
Review of apoptotic and non-apoptotic events in non-ciliated cells of the mammalian oviduct.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1c3jt1ehuw%3D%3D&md5=b9a2171f0951b79d55287f26db811b4eCAS |

Sweet, R. L. (2011). Treatment of acute pelvic inflammatory disease. Infect. Dis. Obstet. Gynecol. 2011, 561909.
Treatment of acute pelvic inflammatory disease.Crossref | GoogleScholarGoogle Scholar |

Tuffrey, M., Falder, P., Gale, J., and Taylor-Robinson, D. (1986). Salpingitis in mice induced by human strains of Chlamydia trachomatis. Br. J. Exp. Pathol. 67, 605–616.
| 1:STN:280:DyaL283ps1Gitg%3D%3D&md5=0cbf10c5b82e20467523137b4b62b43fCAS |

Vlachos, I. S., Paraskevopoulou, M. D., Karagkouni, D., Georgakilas, G., Vergoulis, T., Kanellos, I., Anastasopoulos, I. L., Maniou, S., Karathanou, K., Kalfakakou, D., Fevgas, A., Dalamagas, T., and Hatzigeorgiou, A. G. (2015). DIANA-TarBase v7.0: indexing more than half a million experimentally supported miRNA:mRNA interactions. Nucleic Acids Res. 43, D153–D159.
DIANA-TarBase v7.0: indexing more than half a million experimentally supported miRNA:mRNA interactions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXhtVymtLzE&md5=e4cbffbab629cdbfff43fd9cfb69009aCAS |

Wright, V. C., Chang, J., Jeng, G., and Macaluso, M. (2008). Assisted reproductive technology surveillance – United States, 2005. MMWR Surveill. Summ. 57, 1–23.

Yeruva, L., Myers, G. S., Spencer, N., Creasy, H. H., Adams, N. E., Maurelli, A. T., McChesney, G. R., Cleves, M. A., Ravel, J., Bowlin, A., and Rank, R. G. (2014). Early microRNA expression profile as a prognostic biomarker for the development of pelvic inflammatory disease in a mouse model of chlamydial genital infection. MBio 5, e01241-14.

Zhong, G. (2009). Killing me softly: chlamydial use of proteolysis for evading host defenses. Trends Microbiol. 17, 467–474.
Killing me softly: chlamydial use of proteolysis for evading host defenses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFyqt73L&md5=827f001d2a4a96a406553a4558fcc836CAS |

Zhong, G. (2011). Chlamydia trachomatis secretion of proteases for manipulating host signaling pathways. Front. Microbiol. 2, 14.
Chlamydia trachomatis secretion of proteases for manipulating host signaling pathways.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXptVCqu7Y%3D&md5=cd6311a319e68e0373b69bac3fe9d90aCAS |