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Lipopolysaccharide-induced modulation in the expression of progesterone receptor and estradiol receptor leads to early pregnancy loss in mouse

Published online by Cambridge University Press:  19 July 2012

Varkha Agrawal ,
Mukesh Kumar Jaiswal  and
Yogesh Kumar Jaiswal
Varkha Agrawal
Affiliation:
Molecular Biology and Reproductive Immunology Laboratory, School of Studies in Biochemistry, Jiwaji University, Gwalior-474 011, India. Obstetrics and Gynecology, North Shore University Health System, Evanston, IL 60201, USA.
Mukesh Kumar Jaiswal
Affiliation:
Molecular Biology and Reproductive Immunology Laboratory, School of Studies in Biochemistry, Jiwaji University, Gwalior-474 011, India. Clinical Immunology Laboratory, Rosalind Franklin University of Medical and Science, 3333 Green Bay Road, North Chicago, IL 60064, USA.
Yogesh Kumar Jaiswal*
Affiliation:
Molecular Biology and Reproductive Immunology Laboratory, School of Studies in Biochemistry, Jiwaji University, Gwalior-474 011(M.P.), India.
*
All correspondence to: Y.K. Jaiswal. Molecular Biology and Reproductive Immunology Laboratory, School of Studies in Biochemistry, Jiwaji University, Gwalior-474 011(M.P.), India. e-mail: jaiswalmbri@gmail.com
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Summary

The objective of the present study was to investigate the effect of Gram-negative bacteria infection on ovarian steroid receptors, i.e. progesterone receptor (PR) and estradiol receptor (ER) during preimplantation days of pregnancy. A well established mouse model of Gram-negative bacteria infection was used to test this objective. Mice were treated with normal saline or lipopolysaccharide (LPS) on day 0.5 of pregnancy and used to collect embryos and uterine horns on day 1.5 to day 4.42 preimplantation day of pregnancy. Total RNA was extracted and reverse-transcription polymerase chain reaction (PCR) was performed to check the expression of PR and ER genes. The mRNA expression of PR and ER was altered in embryos and uterus of LPS-treated animals during preimplantation days of pregnancy studied. These results suggest that PR and ER play an important role in Gram-negative bacteria infection and induced implantation failure in mouse.

Keywords

17β-EstradiolEstrogen receptorLipopolysaccharideProgesteroneProgesterone receptor
Type
Research Article
Information
Zygote , Volume 21 , Issue 4 , November 2013 , pp. 337 - 344
Copyright
Copyright © Cambridge University Press 2012 

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References

Agrawal, V., Jaiswal, M.K., Chaturvedi, M.M., Tiwari, D.C. & Jaiswal, Y.K. (2009). Lipopolysaccharide alters the vaginal electrical resistance in cycling and pregnant mice. Am. J. Reprod. Immunol. 61, 158–66.CrossRefGoogle ScholarPubMed
Agrawal, V., Jaiswal, M.K. & Jaiswal, Y.K. (2011). Lipopolysaccharide induces alterations in ovaries and serum level of progesterone and 17beta-estradiol in the mouse. Fertil. Steril. 95, 1471–4.CrossRefGoogle ScholarPubMed
Curtis Hewitt, S., Goulding, E.H., Eddy, E.M. & Korach, K.S. (2002). Studies using the estrogen receptor α knockout uterus demonstrate that implantation but not decidualization-associated signaling is estrogen dependent. Biol. Reprod. 67, 1268–77.CrossRefGoogle Scholar
Das, S.K., Tan, J., Johnson, D.C. & Dey, S.K. (1998). Differential spatiotemporal regulation of lactoferrin and progesterone receptor genes in the mouse uterus by primary estrogen, catechol estrogen, and xenoestrogen. Endocrinology 139, 2905–15.CrossRefGoogle ScholarPubMed
Deb, K., Chaturvedi, M.M. & 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.CrossRefGoogle ScholarPubMed
FidelP.I., Jr. P.I., Jr., Romero, R., Maymon, E. & Hertelendy, F. (1998). Bacteria-induced or bacterial product-induced preterm parturition in mice and rabbits is preceded by a significant fall in serum progesterone concentrations. J. Matern. Fetal. Med. 7, 222–6.Google ScholarPubMed
Hamatani, T., Daikoku, T., Wang, H., Matsumoto, H., Carter, M.G., Ko, M.S. & Dey, S.K. (2004). Global gene expression analysis identifies molecular pathways distinguishing blastocyst dormancy and activation. Proc. Natl. Acad. Sci. USA 101, 10326–31.CrossRefGoogle ScholarPubMed
Hardy, D.B., Janowski, B.A., Corey, D.R. & Mendelson, C.R. (2006). Progesterone receptor plays a major anti-inflammatory role in human myometrial cells by antagonism of nuclear factor-kappaB activation of cyclooxygenase 2 expression. Mol. Endocrinol. 20, 2724–33.CrossRefGoogle Scholar
Hou, Q. & Gorski, J. (1993). Estrogen receptor and progesterone receptor genes are expressed differentially in mouse embryos during preimplantation development. Proc. Natl. Acad. Sci. USA 90, 9460–4.CrossRefGoogle ScholarPubMed
Jaiswal, Y.K., Chaturvedi, M.M. & Deb, K. (2006). Effect of bacterial endotoxins on superovulated mouse embryos in vivo: is CSF-1 involved in endotoxin-induced pregnancy loss? Infect. Dis. Obstet. Gynecol. 2006, 32050.CrossRefGoogle ScholarPubMed
Jaiswal, Y.K., Jaiswal, M.K., Agrawal, V. & Chaturvedi, M.M. (2009). Bacterial endotoxin (LPS)-induced DNA damage in preimplanting embryonic and uterine cells inhibits implantation. Fertil. Steril. 91, 2095–103.CrossRefGoogle ScholarPubMed
Koga, K. & Mor, G. (2010). Toll-like receptors at the maternal–fetal interface in normal pregnancy and pregnancy disorders. Am. J. Reprod. Immunol. 63, 587–600.CrossRefGoogle ScholarPubMed
Lee, Y.J. & Gorski, J. (1996). Estrogen-induced transcription of the progesterone receptor gene does not parallel estrogen receptor occupancy. Proc. Natl. Acad. Sci. USA 93, 15180–4.CrossRefGoogle Scholar
Lee, K., Jeong, J., Tsai, M.J., Tsai, S., Lydon, J.P. & DeMayo, F.J. (2006). Molecular mechanisms involved in progesterone receptor regulation of uterine function. J. Steroid Biochem. Mol. Biol. 102, 41–50.CrossRefGoogle ScholarPubMed
Ma, W-G., Song, H., Das, S.K., Paria, B.C. & Dey, S.K. (2003). Estrogen is a critical determinant that specifies the duration of the window of uterine receptivity for implantation. Proc. Natl. Acad. Sci. USA 100, 2963–8.CrossRefGoogle ScholarPubMed
Martin, J.A., Hamilton, B.E., Sutton, P.D., Ventura, S.J., Mathews, T.J., Kirmeyer, S. & Osterman, M.J. (2010). Births: final data for 2007. Natl. Vital Stat. Rep. 58, 1–85.Google ScholarPubMed
Minorics, R., Ducza, E., Marki, A., Paldy, E. & Falkay, G. (2004). Investigation of estrogen receptor alpha and beta mRNA expression in the pregnant rat uterus. Mol. Reprod. Dev. 68, 463–8.CrossRefGoogle ScholarPubMed
Mulac-Jericevic, B. & Conneely, O.M. (2004). Reproductive tissue selective actions of progesterone receptors. Reproduction 128, 139–46.CrossRefGoogle ScholarPubMed
Murata, T. & Higuchi, T. (2003). Progesterone receptor mRNA levels during pregnancy, labor, lactation and the estrous cycle in rat uterus. J. Reprod. Dev. 49, 425–32.CrossRefGoogle ScholarPubMed
Paria, B.C., Huet-Hudson, Y.M. & Dey, S.K. (1993). Blastocyst's state of activity determines the “window” of implantation in the receptive mouse uterus. Proc. Natl. Acad. Sci. USA 90, 10159–62.CrossRefGoogle ScholarPubMed
Paria, B.C., Tan, J., Lubahn, D.B., Dey, S.K. & Das, S.K. (1999). Uterine decidual response occurs in estrogen receptor-alpha-deficient mice. Endocrinology 140, 2704–10.CrossRefGoogle ScholarPubMed
Peltier, M.R. (2003). Immunology of term and preterm labor. Reprod. Biol. Endocrinol. 1, 122.CrossRefGoogle ScholarPubMed
Peltier, M.R., Tee, S.C. & Smulian, J.C. (2008). Effect of progesterone on proinflammatory cytokine production by monocytes stimulated with pathogens associated with preterm birth. Am. J. Reprod. Immunol. 60, 346–53.CrossRefGoogle ScholarPubMed
Refojo, D., Arias, P., Moguilevsky, J.A. & Feleder, C. (1998). Effect of bacterial endotoxin on in vivo pulsatile gonadotropin secretion in adult male rats. Neuroendocrinology 67, 275–81.CrossRefGoogle ScholarPubMed
Stouffer, R.L. (2003). Progesterone as a mediator of gonadotrophin action in the corpus luteum: beyond steroidogenesis. Hum. Reprod. Update 9, 99–117.CrossRefGoogle ScholarPubMed
Sugino, N., Telleria, C.M. & Gibori, G. (1998). Differential regulation of copper–zinc superoxide dismutase and manganese superoxide dismutase in the rat corpus luteum: induction of manganese superoxide dismutase messenger ribonucleic acid by inflammatory cytokines. Biol. Reprod. 59, 208–15.CrossRefGoogle ScholarPubMed
Tan, J., Paria, B.C., Dey, S.K. & Das, S.K. (1999). Differential uterine expression of estrogen and progesterone receptors correlates with uterine preparation for implantation and decidualization in the mouse. Endocrinology 140, 5310–21.CrossRefGoogle ScholarPubMed
Wang, H., Eriksson, H. & Sahlin, L. (2000). Estrogen receptors alpha and beta in the female reproductive tract of the rat during the estrous cycle. Biol. Reprod. 63, 1331–40.CrossRefGoogle ScholarPubMed
Williams, E.J., Sibley, K., Miller, A.N., Lane, E.A., Fishwick, J., Nash, D.M., Herath, S., England, G.C., Dobson, H. & Sheldon, I.M. (2008). The effect of Escherichia coli lipopolysaccharide and tumour necrosis factor alpha on ovarian function. Am. J. Reprod. Immunol. 60, 462–73.CrossRefGoogle ScholarPubMed
You, X., Yang, R., Tang, X., Gao, L. & Ni, X. (2006). Corticotropin-releasing hormone stimulates estrogen biosynthesis in cultured human placental trophoblasts. Biol. Reprod. 74, 1067–72.CrossRefGoogle ScholarPubMed