Top

Reproductive Biology and Endocrinology

Published in:

Open Access 01-12-2010 | Research

Endometrial caspase 1 and interleukin-18 expression during the estrous cycle and peri-implantation period of porcine pregnancy and response to early exogenous estrogen administration

Authors: Morgan D Ashworth, Jason W Ross, Daniel R Stein, Frank J White, Udaya W DeSilva, Rodney D Geisert

Published in: Reproductive Biology and Endocrinology | Issue 1/2010

Abstract

Background

The role for endometrial secretion of cytokines during the establishment of pregnancy in a number of mammals is well established. The current study determined endometrial expression of caspase 1 (CASP1) and interleukin-18 (IL18) during the estrous cycle and early pregnancy, and following early estrogen administration, which induces conceptus loss during early development in pigs.

Methods

Gilts were hysterectomized on either D 0, 5, 10, 12, 15 and 18 of the estrous cycle, or D 10, 12, 15 or 18 of pregnancy. The abundance of endometrial CASP1 mRNA was unaffected by day of the estrous cycle, however there was a 6 and 10-fold increase in expression on D 15 and 18 of pregnancy. Endometrial expression of IL18 mRNA increased 5-fold between D 10 to 18 in cyclic and pregnant gilts. Total recoverable IL18 in uterine flushings was greater in pregnant compared to cyclic gilts on D 15 and 18.

In the second experiment, mated gilts were treated with either corn oil (CO) or estrogen (E) on D 9 and 10 and hysterectomized on either D 10, 12, 13, 15 or 17 of pregnancy. The current study localizes the presence of CASP1 to the epithelial layer of the endometrium for the first time. Further, a day × treatment interaction was detected for endometrial CASP1 mRNA and protein abundance as E stimulated an earlier increase on D 13 compared to CO gilts. Although IL18 mRNA expression remained unaltered from the E treatment, protein abundance was significantly attenuated on D 15 and 18 in response to E treatment.

Conclusions

Endometrial expression of CASP1 and IL18 is associated with establishment of pregnancy in pigs. Alteration of CASP1 and IL18 following premature exposure of the uterus to estrogen during early pregnancy may contribute to conceptus loss between Days 15 to 18 of pregnancy.

Available only for authorised users

King GJ, Atkinson BA, Robertson HA: Implantation and early placentation in domestic ungulates. J Reprod Fertil Suppl. 1982, 31: 17-30.PubMed

Stroband HW, Lende Van der T: Embryonic and uterine development during early pregnancy in pigs. J Reprod Fertil Suppl. 1990, 40: 261-277.PubMed

Bowen JA, Bazer FW, Burghardt RC: Spatial and temporal analyses of integrin and Muc-1 expression in porcine uterine epithelium and trophectoderm in vivo. Biol Reprod. 1996, 55 (5): 1098-1106. 10.1095/biolreprod55.5.1098.CrossRefPubMed

Geisert RD, Blair RM, Pratt T, Zavy MT: Characterization and proteolytic activity of a cathepsin L-like polypeptide in endometrium and uterine flushings of cycling, pregnant and steroid-treated ovariectomized gilts. Reprod Fertil Dev. 1997, 9 (4): 395-402. 10.1071/R96106.CrossRefPubMed

Geisert RD, Zavy MT, Moffatt RJ, Blair RM, Yellin T: Embryonic steroids and the establishment of pregnancy in pigs. J Reprod Fertil Suppl. 1990, 40: 293-305.PubMed

Keys JL, King GJ: Microscopic examination of porcine conceptus-maternal interface between days 10 and 19 of pregnancy. Am J Anat. 1990, 188 (3): 221-238. 10.1002/aja.1001880302.CrossRefPubMed

Burghardt RC, Bowen JA, Newton GR, Bazer FW: Extracellular matrix and the implantation cascade in pigs. J Reprod Fertil Suppl. 1997, 52: 151-164.PubMed

Jaeger LA, Johnson GA, Ka H, Garlow JG, Burghardt RC, Spencer TE, Bazer FW: Functional analysis of autocrine and paracrine signalling at the uterine-conceptus interface in pigs. Reprod Suppl. 2001, 58: 191-207.PubMed

Ross JW, Malayer JR, Ritchey JW, Geisert RD: Characterization of the interleukin-1beta system during porcine trophoblastic elongation and early placental attachment. Biol Reprod. 2003, 69 (4): 1251-1259. 10.1095/biolreprod.103.015842.CrossRefPubMed

10.

Okamura H, Tsutsi H, Komatsu T, Yutsudo M, Hakura A, Tanimoto T, Torigoe K, Okura T, Nukada Y, Hattori K: Cloning of a new cytokine that induces IFN-gamma production by T cells. Nature. 1995, 378 (6552): 88-91. 10.1038/378088a0.CrossRefPubMed

11.

Ostojic S, Dubanchet S, Chaouat G, Abdelkarim M, Truyens C, Capron F: Demonstration of the presence of IL-16, IL-17 and IL-18 at the murine fetomaternal interface during murine pregnancy. Am J Reprod Immunol. 2003, 49 (2): 101-112. 10.1034/j.1600-0897.2003.01150.x.CrossRefPubMed

12.

Arend WP, Palmer G, Gabay C: IL-1, IL-18, and IL-33 families of cytokines. Immunol Rev. 2008, 223: 20-38. 10.1111/j.1600-065X.2008.00624.x.CrossRefPubMed

13.

Hentze H, Lin XY, Choi MS, Porter AG: Critical role for cathepsin B in mediating caspase-1-dependent interleukin-18 maturation and caspase-1-independent necrosis triggered by the microbial toxin nigericin. Cell Death Differ. 2003, 10 (9): 956-968. 10.1038/sj.cdd.4401264.CrossRefPubMed

14.

Cencic A, La Bonnardiere C: Trophoblastic interferon-gamma: current knowledge and possible role(s) in early pig pregnancy. Vet Res. 2002, 33 (2): 139-157. 10.1051/vetres:2002003.CrossRefPubMed

15.

Morgan GL, Geisert RD, Zavy MT, Fazleabas AT: Development and survival of pig blastocysts after oestrogen administration on day 9 or days 9 and 10 of pregnancy. J Reprod Fertil. 1987, 80 (1): 133-141.CrossRefPubMed

16.

Ross JW, Ashworth MD, Hurst AG, Malayer JR, Geisert RD: Analysis and characterization of differential gene expression during rapid trophoblastic elongation in the pig using suppression subtractive hybridization. Reprod Biol Endocrinol. 2003, 1: 23-10.1186/1477-7827-1-23.PubMedCentralCrossRefPubMed

17.

Ashworth MD, Ross JW, Hu J, White FJ, Stein DR, Desilva U, Johnson GA, Spencer TE, Geisert RD: Expression of porcine endometrial prostaglandin synthase during the estrous cycle and early pregnancy, and following endocrine disruption of pregnancy. Biol Reprod. 2006, 74 (6): 1007-1015. 10.1095/biolreprod.105.046557.CrossRefPubMed

18.

Ashworth MD, Ross JW, Stein DR, Allen DT, Spicer LJ, Geisert RD: Endocrine disruption of uterine insulin-like growth factor expression in the pregnant gilt. Reproduction. 2005, 130 (4): 545-551. 10.1530/rep.1.00821.CrossRefPubMed

19.

Gries LK, Geisert RD, Zavy MT, Garrett JE, Morgan GL: Uterine secretory alterations coincident with embryonic mortality in the gilt after exogenous estrogen administration. J Anim Sci. 1989, 67 (1): 276-284.PubMed

20.

Ross JW, Ashworth MD, Stein DR, Couture OP, Tuggle CK, Geisert RD: Identification of differential gene expression during porcine conceptus rapid trophoblastic elongation and attachment to uterine luminal epithelium. Physiol Genomics. 2009, 36 (3): 140-148.CrossRefPubMed

21.

Hettinger AM, Allen MR, Zhang BR, Goad DW, Malayer JR, Geisert RD: Presence of the acute phase protein, bikunin, in the endometrium of gilts during estrous cycle and early pregnancy. Biol Reprod. 2001, 65 (2): 507-513. 10.1095/biolreprod65.2.507.CrossRefPubMed

22.

Johnson GA, Austin KJ, Collins AM, Murdoch WJ, Hansen TR: Endometrial ISG17 mRNA and a related mRNA are induced by interferon-tau and localized to glandular epithelial and stromal cells from pregnant cows. Endocrine. 1999, 10 (3): 243-252. 10.1007/BF02738623.CrossRefPubMed

23.

Pope WF, Lawyer MS, Butler WR, Foote RH, First NL: Dose-response shift in the ability of gilts to remain pregnant following exogenous estradiol-17 beta exposure. J Anim Sci. 1986, 63 (4): 1208-1210.PubMed

24.

Bazer FW, Thatcher WW: Theory of maternal recognition of pregnancy in swine based on estrogen controlled endocrine versus exocrine secretion of prostaglandin F2alpha by the uterine endometrium. Prostaglandins. 1977, 14 (2): 397-400. 10.1016/0090-6980(77)90185-X.CrossRefPubMed

25.

Geisert RD, Ross JW, Ashworth MD, White FJ, Johnson GA, DeSilva U: Maternal recognition of pregnancy signal or endocrine disruptor: the two faces of oestrogen during establishment of pregnancy in the pig. Soc Reprod Fertil Suppl. 2006, 62: 131-145.PubMed

26.

Muneta Y, Shimoji Y, Mori Y: Porcine caspase-3: its cloning and activity during apoptosis of PK15 cells induced by porcine Fas ligand. J Interferon Cytokine Res. 2001, 21 (6): 409-415. 10.1089/107999001750277880.CrossRefPubMed

27.

Fantuzzi G, Dinarello CA: Interleukin-18 and interleukin-1 beta: two cytokine substrates for ICE (caspase-1). J Clin Immunol. 1999, 19 (1): 1-11. 10.1023/A:1020506300324.CrossRefPubMed

28.

Lee JK, Kim SH, Lewis EC, Azam T, Reznikov LL, Dinarello CA: Differences in signaling pathways by IL-1beta and IL-18. Proc Natl Acad Sci USA. 2004, 101 (23): 8815-8820. 10.1073/pnas.0402800101.PubMedCentralCrossRefPubMed

29.

Yoshino O, Osuga Y, Koga K, Tsutsumi O, Yano T, Fujii T, Kugu K, Momoeda M, Fujiwara T, Tomita K: Evidence for the expression of interleukin (IL)-18, IL-18 receptor and IL-18 binding protein in the human endometrium. Mol Hum Reprod. 2001, 7 (7): 649-654. 10.1093/molehr/7.7.649.CrossRefPubMed

30.

Joyce MM, Burghardt RC, Geisert RD, Burghardt JR, Hooper RN, Ross JW, Ashworth MD, Johnson GA: Pig conceptuses secrete estrogen and interferons to differentially regulate uterine STAT1 in a temporal and cell type-specific manner. Endocrinology. 2007, 148 (9): 4420-4431. 10.1210/en.2007-0505.CrossRefPubMed

31.

Coma G, Pena R, Blanco J, Rosell A, Borras FE, Este JA, Clotet B, Ruiz L, Parkhouse RM, Bofill M: Treatment of monocytes with interleukin (IL)-12 plus IL-18 stimulates survival, differentiation and the production of CXC chemokine ligands (CXCL)8, CXCL9 and CXCL10. Clin Exp Immunol. 2006, 145 (3): 535-544. 10.1111/j.1365-2249.2006.03145.x.PubMedCentralCrossRefPubMed

32.

Blair RM, Geisert RD, Zavy MT, Yellin T, Fulton RW, Short EC: Endometrial surface and secretory alterations associated with embryonic mortality in gilts administered estradiol valerate on days 9 and 10 of gestation. Biol Reprod. 1991, 44 (6): 1063-1079. 10.1095/biolreprod44.6.1063.CrossRefPubMed

33.

Ross JW, Ashworth MD, White FJ, Johnson GA, Ayoubi PJ, DeSilva U, Whitworth KM, Prather RS, Geisert RD: Premature estrogen exposure alters endometrial gene expression to disrupt pregnancy in the pig. Endocrinology. 2007, 148 (10): 4761-4773. 10.1210/en.2007-0599.CrossRefPubMed

Title: Endometrial caspase 1 and interleukin-18 expression during the estrous cycle and peri-implantation period of porcine pregnancy and response to early exogenous estrogen administration
Authors: Morgan D Ashworth
Jason W Ross
Daniel R Stein
Frank J White
Udaya W DeSilva
Rodney D Geisert
Publication date: 01-12-2010
Publisher: BioMed Central
Published in: Reproductive Biology and Endocrinology / Issue 1/2010
Electronic ISSN: 1477-7827
DOI: https://doi.org/10.1186/1477-7827-8-33

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Endometrial caspase 1 and interleukin-18 expression during the estrous cycle and peri-implantation period of porcine pregnancy and response to early exogenous estrogen administration

Abstract

Background

Methods

Conclusions

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Background

Methods

Conclusions

Please log in to get access to this content

Other articles of this Issue 1/2010

GnRH I and II up-regulate MMP-26 expression through the JNK pathway in human cytotrophoblasts

Comparison of estrogens and estrogen metabolites in human breast tissue and urine

Genetic evidence that SMAD2 is not required for gonadal tumor development in inhibin-deficient mice

Remarkable features of ovarian morphology and reproductive hormones in insulin-resistant Zucker fatty (fa/fa) rats

Endoplasmic reticulum protein 29 (ERp29), a protein related to sperm maturation is involved in sperm-oocyte fusion in mouse

Proto-oncogene c-erbB2 initiates rat primordial follicle growth via PKC and MAPK pathways