Cyclic regulation of apoptotic gene expression in the mouse oviduct
Myoungkun Jeoung A and Phillip J. Bridges A B
+ Author Affiliations
- Author Affiliations
A Division of Clinical and Reproductive Sciences, University of Kentucky, Lexington, KY 40536, USA.
B Corresponding author. Email: pbrid2@email.uky.edu
Reproduction, Fertility and Development 23(5) 638-644 https://doi.org/10.1071/RD11011
Submitted: 7 January 2011 Accepted: 7 February 2011 Published: 5 May 2011
Abstract
The oviduct is a dynamic structure whose function relies upon cyclic changes in the morphology of both ciliated and secretory luminal epithelial cells. Unfortunately, infection of these epithelial cells by sexually transmitted pathogens can lead to pelvic inflammatory disease, ectopic pregnancies and infertility. The disruption of normal, cyclic apoptosis in the oviducal epithelium appears to be a causal factor of oviducal pathology and therefore, these pathways represent a potential target for diagnosis and therapeutic intervention. The objective of this study was to determine the pattern of expression for apoptotic genes in the oviduct of the naturally cycling mouse, generating fundamental information that can be applied to the development of animal models for research and the identification of targets for disease intervention. Whole oviducts were collected from regular cycling mice killed at 1 p.m. on each day of the oestrous cycle and the expression of 84 apoptotic genes determined by targeted PCR super-array. Intact and cleaved caspases were then evaluated by western blotting. The expression of mRNA for genes classified as pro-apoptotic (Bad, Bak1 and Bok) and anti-apoptotic (Bag3, Bnip2 and Xiap) was regulated by day (P < 0.05). Differences in the temporal expression of several p53-related genes (Trp53bp2, Trp53inp1 and Trp73), those specific to the TNF superfamily (Tnfrsf10 and Tnfsf10b) and one caspase (Casp14) were also observed (P < 0.05). The cleaved forms of Caspases-3, -6 and -12 were all detected throughout the oestrous cycle. These results represent the first pathway-wide analysis of apoptotic gene expression in the murine oviduct.
Additional keywords: cell death, epithelial cell, fallopian tube, oestrous cycle.
References
Abe, H., and Oikawa, T. (1993). Observations by scanning electron microscopy of oviductal epithelial cells from cows at follicular and luteal phases. Anat. Rec. 235, 399–410.| Observations by scanning electron microscopy of oviductal epithelial cells from cows at follicular and luteal phases.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3s7lvV2hsg%3D%3D&md5=9ac7582a851d733c1d6f0e4966a8dfbaCAS | 8430910PubMed |
Abe, H., Onodera, M., Sugawara, S., Satoh, T., and Hoshi, H. (1999). Ultrastructural features of goat oviductal secretory cells at follicular and luteal phases of the oestrous cycle. J. Anat. 195, 515–521.
| Ultrastructural features of goat oviductal secretory cells at follicular and luteal phases of the oestrous cycle.Crossref | GoogleScholarGoogle Scholar | 10634690PubMed |
Al-Alem, L., Bridges, P. J., Su, W., Gong, M. C., Iglarz, M., and Ko, C. (2007). Endothelin-2 induces oviductal contraction via endothelin receptor subtype A in rats. J. Endocrinol. 193, 383–391.
| Endothelin-2 induces oviductal contraction via endothelin receptor subtype A in rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXnt1CqtL4%3D&md5=403f607c03ee81d61956eb88362d6f8bCAS | 17535876PubMed |
Antoni, B. A., Sabbatini, P., Rabson, A. B., and White, E. (1995). Inhibition of apoptosis in human immunodeficiency virus-infected cells enhances virus production and facilitates persistent infection. J. Virol. 69, 2384–2392.
| 1:CAS:528:DyaK2MXksVSmtLw%3D&md5=d851b501007d6ec39fba304b48de5913CAS | 7884884PubMed |
Binnicker, M. J., Williams, R. D., and Apicella, M. A. (2003). Infection of human urethral epithelium with Neisseria gonorrhoeae elicits an upregulation of host anti-apoptotic factors and protects cells from staurosporine-induced apoptosis. Cell. Microbiol. 5, 549–560.
| Infection of human urethral epithelium with Neisseria gonorrhoeae elicits an upregulation of host anti-apoptotic factors and protects cells from staurosporine-induced apoptosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmtVyktL8%3D&md5=4ae4c7b34087beee4129f43a6a500b24CAS | 12864814PubMed |
Bridges, P. J., Jo, M., Al Alem, L., Na, G., Su, W., Gong, M. C., Jeoung, M., and Ko, C. (2010). Production and binding of endothelin-2 (EDN2) in the rat ovary: endothelin receptor subtype A (EDNRA)-mediated contraction. Reprod. Fertil. Dev. 22, 780–787.
| Production and binding of endothelin-2 (EDN2) in the rat ovary: endothelin receptor subtype A (EDNRA)-mediated contraction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlsVCqtLs%3D&md5=47209050235371af8b2cbea5cbcf7386CAS | 20450830PubMed |
Caligioni, C. S. (2009). Assessing reproductive status/stages in mice. Curr. Protoc. Neurosci. Appendix 4(Appendix), 4I.
Delhalle, S., Duvoix, A., Schnekenburger, M., Morceau, F., Dicato, M., and Diederich, M. (2003). An introduction to the molecular mechanisms of apoptosis. Ann. N Y Acad. Sci. 1010, 1–8.
| 1:CAS:528:DC%2BD2cXisFeksro%3D&md5=ef4a26ee9150fecc0b5bf028d54485ebCAS | 15033687PubMed |
Dong, F., Pirbhai, M., Xiao, Y., Zhong, Y., Wu, Y., and Zhong, G. (2005). Degradation of the pro-apoptotic proteins Bik, Puma, and Bim with Bcl-2 domain 3 homology in Chlamydia trachomatis-infected cells. Infect. Immun. 73, 1861–1864.
| Degradation of the pro-apoptotic proteins Bik, Puma, and Bim with Bcl-2 domain 3 homology in Chlamydia trachomatis-infected cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXit12mtrk%3D&md5=3a443b9002b1da42b5da241e0cc677e0CAS | 15731089PubMed |
Fan, T., Lu, H., Hu, H., Shi, L., McClarty, G. A., Nance, D. M., Greenberg, A. H., and Zhong, G. (1998). Inhibition of apoptosis in chlamydia-infected cells: blockade of mitochondrial cytochrome c release and caspase activation. J. Exp. Med. 187, 487–496.
| Inhibition of apoptosis in chlamydia-infected cells: blockade of mitochondrial cytochrome c release and caspase activation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXhtFCqt70%3D&md5=75aa01b7139f4cb54ed0c0e121fbd41dCAS | 9463399PubMed |
Fischer, S. F., Vier, J., Kirschnek, S., Klos, A., Hess, S., Ying, S., and Hacker, G. (2004). Chlamydia inhibit host cell apoptosis by degradation of pro-apoptotic BH3-only proteins. J. Exp. Med. 200, 905–916.
| Chlamydia inhibit host cell apoptosis by degradation of pro-apoptotic BH3-only proteins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXot1KhsLw%3D&md5=fa909ac60e0649f982e7a99b2b6fb235CAS | 15452181PubMed |
Gardner, D. K., Lane, M., Calderon, I., and Leeton, J. (1996). Environment of the preimplantation human embryo in vivo: metabolite analysis of oviduct and uterine fluids and metabolism of cumulus cells. Fertil. Steril. 65, 349–353.
| 1:STN:280:DyaK287lsVSitA%3D%3D&md5=5069ec5bd0a49650307b2cae43c76ddbCAS | 8566260PubMed |
Goldman, J. M., Murr, A. S., and Cooper, R. L. (2007). The rodent oestrous cycle: characterization of vaginal cytology and its utility in toxicological studies. Birth Defects Res. B Dev. Reprod. Toxicol. 80, 84–97.
| The rodent oestrous cycle: characterization of vaginal cytology and its utility in toxicological studies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXlsVWmsr8%3D&md5=4c4858df10564b9818f583d64957d89dCAS | 17342777PubMed |
Gown, A. M., and Willingham, M. C. (2002). Improved detection of apoptotic cells in archival paraffin sections: immunohistochemistry using antibodies to cleaved Caspase 3. J. Histochem. Cytochem. 50, 449–454.
| Improved detection of apoptotic cells in archival paraffin sections: immunohistochemistry using antibodies to cleaved Caspase 3.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xis1Wnt74%3D&md5=4abe0d8d479a680bb06f57d7f1a21539CAS | 11897797PubMed |
Hinshelwood, M. M., Shelton, J. M., Richardson, J. A., and Mendelson, C. R. (2005). Temporal and spatial expression of liver receptor homologue-1 (LRH-1) during embryogenesis suggests a potential role in gonadal development. Dev. Dyn. 234, 159–168.
| Temporal and spatial expression of liver receptor homologue-1 (LRH-1) during embryogenesis suggests a potential role in gonadal development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVehtbjM&md5=a7ab92740ea53b03077453daf92a966aCAS | 16003771PubMed |
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=0e05ee1ed74188b2e60095eea5dfe83eCAS | 20357223PubMed |
Kawana, K., Quayle, A. J., Ficarra, M., Ibana, J. A., Shen, L., Kawana, Y., Yang, H., Marrero, L., Yavagal, S., Greene, S. J., Zhang, Y. X., Pyles, R. B., Blumberg, R. S., and Schust, D. J. (2007). CD1d degradation in Chlamydia trachomatis-infected epithelial cells is the result of both cellular and chlamydial proteasomal activity. J. Biol. Chem. 282, 7368–7375.
| CD1d degradation in Chlamydia trachomatis-infected epithelial cells is the result of both cellular and chlamydial proteasomal activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXitlSrtrg%3D&md5=7505b0fc00bc0049cf4ffde0ae3a1aecCAS | 17215251PubMed |
Kent, W. J., Sugnet, C. W., Furey, T. S., Roskin, K. M., Pringle, T. H., Zahler, A. M., and Haussler, D. (2002). The human genome browser at UCSC. Genome Res. 12, 996–1006.
| 1:CAS:528:DC%2BD38Xks12hs7s%3D&md5=e5e00ff134e65ea1ceb0814fce61590aCAS | 12045153PubMed |
Kepp, O., Gottschalk, K., Churin, Y., Rajalingam, K., Brinkmann, V., Machuy, N., Kroemer, G., and Rudel, T. (2009). Bim and Bmf synergize to induce apoptosis in Neisseria gonorrhoeae infection. PLoS Pathog. 5, e1000348.
| Bim and Bmf synergize to induce apoptosis in Neisseria gonorrhoeae infection.Crossref | GoogleScholarGoogle Scholar | 19300516PubMed |
Koomey, M. (2001). Implications of molecular contacts and signalling initiated by Neisseria gonorrhoeae. Curr. Opin. Microbiol. 4, 53–57.
| Implications of molecular contacts and signalling initiated by Neisseria gonorrhoeae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhtlKlsL0%3D&md5=90c408753c63a9a4952ab652af5e8dfbCAS | 11173034PubMed |
Lehrman, D. S., and Brody, P. (1957). Oviduct response to oestrogen and progesterone in the ring dove (Streptopelia risoria). Proc. Soc. Exp. Biol. Med. 95, 373–375.
| 1:CAS:528:DyaG2sXot1Kqsg%3D%3D&md5=f1da6a810758f6c2dca14388aad9e293CAS | 13441743PubMed |
Livak, K. J., and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2-[Delta][Delta]CT method. Methods 25, 402–408.
| Analysis of relative gene expression data using real-time quantitative PCR and the 2-[Delta][Delta]CT method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhtFelt7s%3D&md5=e0ea026c02920b4196beca401ea8984bCAS | 11846609PubMed |
Martin, S. J., and Green, D. R. (1995). Protease activation during apoptosis: death by a thousand cuts? Cell 82, 349–352.
| Protease activation during apoptosis: death by a thousand cuts?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXnsFSgsb8%3D&md5=3ceb69ff162cba6500f3d893084c1b87CAS | 7634323PubMed |
Mason, R. C. (1952). Synergistic and antagonistic effects of progesterone in combination with oestrogens on oviduct weight. Endocrinology 51, 570–572.
| Synergistic and antagonistic effects of progesterone in combination with oestrogens on oviduct weight.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaG2cXnvFGh&md5=3de4a805718cd403af64655c92d2de3aCAS | 13021102PubMed |
Mastroianni, L., (1999). The fallopian tube and reproductive health. J. Pediatr. Adolesc. Gynecol. 12, 121–126.
| 10546902PubMed |
McGee, Z. A., Johnson, A. P., and Taylor-Robinson, D. (1981). Pathogenic mechanisms of Neisseria gonorrhoeae: observations on damage to human fallopian tubes in organ culture by gonococci of colony type 1 or type 4. J. Infect. Dis. 143, 413–422.
| Pathogenic mechanisms of Neisseria gonorrhoeae: observations on damage to human fallopian tubes in organ culture by gonococci of colony type 1 or type 4.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL3M7ptlahsA%3D%3D&md5=6bc4eb948c0d45c9d38520f2dbb3e34fCAS | 6785363PubMed |
Mintz, P. J., Habib, N. A., Jones, L. J., Giamas, G., Lewis, J. S., Bowen, R. L., Coombes, R. C., and Stebbing, J. (2008). The phosphorylated membrane oestrogen receptor and cytoplasmic signalling and apoptosis proteins in human breast cancer. Cancer 113, 1489–1495.
| The phosphorylated membrane oestrogen receptor and cytoplasmic signalling and apoptosis proteins in human breast cancer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFyls7vF&md5=42346588639aae7e5152a099cab0b72bCAS | 18615623PubMed |
Müller, A., Gunther, D., Dux, F., Naumann, M., Meyer, T. F., and Rudel, T. (1999). Neisserial porin (PorB) causes rapid calcium influx in target cells and induces apoptosis by the activation of cysteine proteases. EMBO J. 18, 339–352.
| Neisserial porin (PorB) causes rapid calcium influx in target cells and induces apoptosis by the activation of cysteine proteases.Crossref | GoogleScholarGoogle Scholar | 9889191PubMed |
Murray, M. K., and DeSouza, M. M. (1995). Messenger RNA encoding an oestrogen-dependent oviduct secretory protein in the sheep is localized in the apical tips and basal compartments of fimbria and ampulla epithelial cells implying translation at unique cytoplasmic foci. Mol. Reprod. Dev. 42, 268–283.
| Messenger RNA encoding an oestrogen-dependent oviduct secretory protein in the sheep is localized in the apical tips and basal compartments of fimbria and ampulla epithelial cells implying translation at unique cytoplasmic foci.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXptFykur4%3D&md5=9be06942d55ad86b74c0cae2ee207566CAS | 8579840PubMed |
Nichol, R., Hunter, R. H., Gardner, D. K., Leese, H. J., and Cooke, G. M. (1992). Concentrations of energy substrates in oviductal fluid and blood plasma of pigs during the peri-ovulatory period. J. Reprod. Fertil. 96, 699–707.
| Concentrations of energy substrates in oviductal fluid and blood plasma of pigs during the peri-ovulatory period.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXpvVyqsA%3D%3D&md5=4596ff8bec4928d82106d776d1d37b60CAS | 1339849PubMed |
O’Brien, J. E., Peterson, T. J., Tong, M. H., Lee, E. J., Pfaff, L. E., Hewitt, S. C., Korach, K. S., Weiss, J., and Jameson, J. L. (2006). Oestrogen-induced proliferation of uterine epithelial cells is independent of oestrogen receptor alpha binding to classical oestrogen response elements. J. Biol. Chem. 281, 26 683–26 692.
| Oestrogen-induced proliferation of uterine epithelial cells is independent of oestrogen receptor alpha binding to classical oestrogen response elements.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XovF2jtro%3D&md5=7293b8cac5ca23ef0833bab5e904e419CAS |
Rajalingam, K., Sharma, M., Paland, N., Hurwitz, R., Thieck, O., Oswald, M., Machuy, N., and Rudel, T. (2006). IAP-IAP complexes required for apoptosis resistance of C. trachomatis-infected cells. PLoS Pathog. 2, e114.
| IAP-IAP complexes required for apoptosis resistance of C. trachomatis-infected cells.Crossref | GoogleScholarGoogle Scholar | 17069460PubMed |
Shao, R., Egecioglu, E., Weijdegard, B., Kopchick, J. J., Fernandez-Rodriguez, J., Andersson, N., and Billig, H. (2007). Dynamic regulation of oestrogen receptor-alpha isoform expression in the mouse fallopian tube: mechanistic insight into oestrogen-dependent production and secretion of insulin-like growth factors. Am. J. Physiol. Endocrinol. Metab. 293, E1430–E1442.
| Dynamic regulation of oestrogen receptor-alpha isoform expression in the mouse fallopian tube: mechanistic insight into oestrogen-dependent production and secretion of insulin-like growth factors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlenurjO&md5=242f56f00b312ed73f9e7c98782c10fcCAS | 17848632PubMed |
Shirley, B., and Reeder, R. L. (1996). Cyclic changes in the ampulla of the rat oviduct. J. Exp. Zool. 276, 164–173.
| Cyclic changes in the ampulla of the rat oviduct.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2s%2FlsFOqsQ%3D%3D&md5=9b6a70bf8ecc33a8edb9f27883516df5CAS | 8900079PubMed |
Soumano, K., Silversides, D. W., Doize, F., and Price, C. A. (1996). Follicular 3 beta-hydroxysteroid dehydrogenase and cytochromes P450 17 alpha-hydroxylase and aromatase messenger ribonucleic acids in cattle undergoing superovulation. Biol. Reprod. 55, 1419–1426.
| Follicular 3 beta-hydroxysteroid dehydrogenase and cytochromes P450 17 alpha-hydroxylase and aromatase messenger ribonucleic acids in cattle undergoing superovulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXkvFKnsQ%3D%3D&md5=9738925d9cd3efe62bc68298baa58378CAS | 8949902PubMed |
Tapsall, J. W., Limnios, E. A., Abu Bakar, H. M., Darussalam, B., Ping, Y. Y., Buadromo, E. M., Kumar, P., Singh, S., Lo, J., Bala, M., Risbud, A., Deguchi, T., Tanaka, M., Watanabe, Y., Lee, K., Chong, Y., Noikaseumsy, S., Phouthavane, T., Sam, I. C., Tundev, O., Lwin, K. M., Eh, P. H., Goorant, C., Goursaud, R., Bathgate, T., Brokenshire, M., Latorre, L., Velemu, E., Carlos, C., Leano, S., Telan, E. O., Goh, S. S., Koh, S. T., Ngan, C., Tan, A. L., Mananwatte, S., Piyanoot, N., Lokpichat, S., Sirivongranson, P., Fakahau, M., Sitanilei, H., and Hungle, V. (2010). Surveillance of antibiotic resistance in Neisseria gonorrhoeae in the WHO Western Pacific and South East Asian regions, 2007–2008. Commun. Dis. Intell. 34, 1–7.
| 1:STN:280:DC%2BC3czpsFOqsQ%3D%3D&md5=baab5871688702f386fe34847af971d5CAS | 20521493PubMed |
Teilmann, S. C., Clement, C. A., Thorup, J., Byskov, A. G., and Christensen, S. T. (2006). Expression and localization of the progesterone receptor in mouse and human reproductive organs. J. Endocrinol. 191, 525–535.
| Expression and localization of the progesterone receptor in mouse and human reproductive organs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1egurc%3D&md5=017dd288997e977132ac598605d6e07cCAS | 17170211PubMed |
Whiley, D. M., Goire, N., Lambert, S. B., Ray, S., Limnios, E. A., Nissen, M. D., Sloots, T. P., and Tapsall, J. W. (2010). Reduced susceptibility to ceftriaxone in Neisseria gonorrhoeae is associated with mutations G542S, P551S and P551L in the gonococcal penicillin-binding protein 2. J. Antimicrob. Chemother. 65, 1615–1618.
| Reduced susceptibility to ceftriaxone in Neisseria gonorrhoeae is associated with mutations G542S, P551S and P551L in the gonococcal penicillin-binding protein 2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXptVyrtb0%3D&md5=bcc82c007f84f98af23684a864d89643CAS | 20511367PubMed |
Witt, K., Veale, D. R., Finch, H., Penn, C. W., Sen, D., and Smith, H. (1976). Resistance of Neisseria gonorrhoeae grown in vivo to ingestion and digestion by phagocytes of human blood. J. Gen. Microbiol. 96, 341–350.
| 1:STN:280:DyaE2s%2Flt12rtg%3D%3D&md5=fb68f0914e33003bcdc9a44c4d5e1699CAS | 825610PubMed |
Ying, S., Seiffert, B. M., Hacker, G., and Fischer, S. F. (2005). Broad degradation of pro-apoptotic proteins with the conserved Bcl-2 homology domain 3 during infection with Chlamydia trachomatis. Infect. Immun. 73, 1399–1403.
| Broad degradation of pro-apoptotic proteins with the conserved Bcl-2 homology domain 3 during infection with Chlamydia trachomatis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXit12nu7o%3D&md5=0443f766c7cceaf9ac3516817407db64CAS | 15731037PubMed |
Yoshida, S., Ohara, N., Xu, Q., Chen, W., Wang, J., Nakabayashi, K., Sasaki, H., Morikawa, A., and Maruo, T. (2010). Cell-type specific actions of progesterone receptor modulators in the regulation of uterine leiomyoma growth. Semin. Reprod. Med. 28, 260–273.
| Cell-type specific actions of progesterone receptor modulators in the regulation of uterine leiomyoma growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsVSqurrL&md5=baafb1d3b0382c477c066b53ba374c1bCAS | 20414849PubMed |
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=2a9ef922f65332b685bbdf34f14b6973CAS | 19765998PubMed |
Zhong, J., Douglas, A. L., and Hatch, T. P. (2001). Characterization of integration host factor (IHF) binding upstream of the cysteine-rich protein operon (omcAB) promoter of Chlamydia trachomatis LGV serovar L2. Mol. Microbiol. 41, 451–462.
| Characterization of integration host factor (IHF) binding upstream of the cysteine-rich protein operon (omcAB) promoter of Chlamydia trachomatis LGV serovar L2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlvVClurs%3D&md5=51d7ae944b11a11130814162fe732910CAS | 11489130PubMed |
