Alterations in Expression of Endometrial Genes Coding for Proteins Secreted into the Uterine Lumen During Conceptus Elongation in Cattle

Overview

Journal BMC Genomics

Publisher Biomed Central

Specialty Genetics

Date 2013 May 14

PMID 23663413

Citations 21

Authors

Niamh Forde

Jai P Mehta

Paul A McGettigan

Solomon Mamo

Fuller W Bazer

Thomas E Spencer

Pat Lonergan

Affiliations

Soon will be listed here.

Abstract

Background: We hypothesized that genes that are up-regulated in the uterine endometrium at the initiation of conceptus elongation in cattle, and that encode for secreted proteins, contribute to the composition of the uterine luminal fluid (ULF) and ultimately, drive conceptus elongation. The aims of this study were to: 1) screen endometrial transcriptomic data for genes that encode secreted proteins on Day 13; 2) determine temporal changes in the expression of these genes during the estrous cycle/early pregnancy; 3) determine if expression of these genes is affected by altered concentrations of progesterone (P4) in vivo and 4) determine if the protein products of these genes are detectable in ULF.

Results: Of the fourteen candidate genes examined, quantitative real-time PCR analysis revealed the expression of APOA1, ARSA, DCN, LCAT, MUC13, NCDN, NMN, NPNT, NXPH3, PENK, PLIN2 and TINAGL1 was modulated in the endometrium (P<0.05) as the estrous cycle/early pregnancy progressed. APOA1, DCN and NPNT expression was higher in cyclic compared to pregnant heifers, and pregnancy increased (P<0.05) the expression of LCAT, NCDN, NMN, PLIN2 and TINAGL1. The magnitude of the increase in expression of APOA1, PENK and TINAGL1 on Day 13 was reduced (P<0.05) in heifers with low P4. Furthermore, low P4 decreased (P<0.05) the expression of LCAT and NPNT on Day 7, while an early increase (P<0.05) in the expression of NXPH3 and PLIN2 was observed in heifers with high P4. The protein products of 5 of the candidate genes (APOA1, ARSA, LCAT, NCDN and PLIN) were detected in the ULF on either Days 13, 16 or 19 of pregnancy.

Conclusion: Using a candidate gene approach, we determined that both P4 concentration and the presence of the conceptus alter endometrial expression of PLIN2, TINAGL1, NPNT, LCAT, NMN and APOA1. Comparison of the expression profiles of these genes to proteins detected in ULF during conceptus elongation (i.e., Days 13 through 19) revealed the presence of APOA1, ARSA, LCAT, NCDN as well as members of the PLIN family of proteins that may play roles in driving conceptus elongation in cattle.

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References

Bazer F . Uterine protein secretions: Relationship to development of the conceptus. J Anim Sci. 1975; 41(5):1376-82. DOI: 10.2527/jas1975.4151376x. View

Clemente M, de la Fuente J, Fair T, Al Naib A, Gutierrez-Adan A, Roche J . Progesterone and conceptus elongation in cattle: a direct effect on the embryo or an indirect effect via the endometrium?. Reproduction. 2009; 138(3):507-17. DOI: 10.1530/REP-09-0152. View

Diskin M, Murphy J, Sreenan J . Embryo survival in dairy cows managed under pastoral conditions. Anim Reprod Sci. 2006; 96(3-4):297-311. DOI: 10.1016/j.anireprosci.2006.08.008. View

Mann G, Fray M, Lamming G . Effects of time of progesterone supplementation on embryo development and interferon-tau production in the cow. Vet J. 2006; 171(3):500-3. DOI: 10.1016/j.tvjl.2004.12.005. View

Song G, Bazer F, Wagner G, Spencer T . Stanniocalcin (STC) in the endometrial glands of the ovine uterus: regulation by progesterone and placental hormones. Biol Reprod. 2006; 74(5):913-22. DOI: 10.1095/biolreprod.106.050807. View

Heid H, Schnolzer M, Keenan T . Adipocyte differentiation-related protein is secreted into milk as a constituent of milk lipid globule membrane. Biochem J. 1996; 320 ( Pt 3):1025-30. PMC: 1218030. DOI: 10.1042/bj3201025. View

Brandao D, Maddox-Hyttel P, Lovendahl P, Rumpf R, Stringfellow D, Callesen H . Post hatching development: a novel system for extended in vitro culture of bovine embryos. Biol Reprod. 2004; 71(6):2048-55. DOI: 10.1095/biolreprod.103.025916. View

Chen C, Spencer T, Bazer F . Fibroblast growth factor-10: a stromal mediator of epithelial function in the ovine uterus. Biol Reprod. 2000; 63(3):959-66. DOI: 10.1095/biolreprod63.3.959. View

Dorniak P, Bazer F, Spencer T . Prostaglandins regulate conceptus elongation and mediate effects of interferon tau on the ovine uterine endometrium. Biol Reprod. 2011; 84(6):1119-27. DOI: 10.1095/biolreprod.110.089979. View

10.

McNeill R, Diskin M, Sreenan J, Morris D . Associations between milk progesterone concentration on different days and with embryo survival during the early luteal phase in dairy cows. Theriogenology. 2005; 65(7):1435-41. DOI: 10.1016/j.theriogenology.2005.08.015. View

11.

Ferguson E, Leese H . A potential role for triglyceride as an energy source during bovine oocyte maturation and early embryo development. Mol Reprod Dev. 2006; 73(9):1195-201. DOI: 10.1002/mrd.20494. View

12.

Northey D, French L . Effect of embryo removal and intrauterine infusion of embryonic homogenates on the lifespan of the bovine corpus luteum. J Anim Sci. 1980; 50(2):298-302. DOI: 10.2527/jas1980.502298x. View

13.

Spencer T, Bartol F, Bazer F, Johnson G, Joyce M . Identification and characterization of glycosylation-dependent cell adhesion molecule 1-like protein expression in the ovine uterus. Biol Reprod. 1999; 60(2):241-50. DOI: 10.1095/biolreprod60.2.241. View

14.

Johnson G, Bazer F, Jaeger L, Ka H, Garlow J, Pfarrer C . Muc-1, integrin, and osteopontin expression during the implantation cascade in sheep. Biol Reprod. 2001; 65(3):820-8. DOI: 10.1095/biolreprod65.3.820. View

15.

Spencer T, Gray C . Sheep uterine gland knockout (UGKO) model. Methods Mol Med. 2005; 121:85-94. DOI: 10.1385/1-59259-983-4:083. View

16.

Mullen M, Forde N, Parr M, Diskin M, Morris D, Nally J . Alterations in systemic concentrations of progesterone during the early luteal phase affect RBP4 expression in the bovine uterus. Reprod Fertil Dev. 2012; 24(5):715-22. DOI: 10.1071/RD11246. View

17.

Garrett J, Geisert R, Zavy M, Morgan G . Evidence for maternal regulation of early conceptus growth and development in beef cattle. J Reprod Fertil. 1988; 84(2):437-46. DOI: 10.1530/jrf.0.0840437. View

18.

Song G, Spencer T, Bazer F . Progesterone and interferon-tau regulate cystatin C in the endometrium. Endocrinology. 2006; 147(7):3478-83. DOI: 10.1210/en.2006-0122. View

19.

Song G, Satterfield M, Kim J, Bazer F, Spencer T . Gastrin-releasing peptide (GRP) in the ovine uterus: regulation by interferon tau and progesterone. Biol Reprod. 2008; 79(2):376-86. PMC: 2714990. DOI: 10.1095/biolreprod.108.068403. View

20.

Bazer F, Kim J, Ka H, Johnson G, Wu G, Song G . Select nutrients in the uterine lumen of sheep and pigs affect conceptus development. J Reprod Dev. 2012; 58(2):180-8. DOI: 10.1262/jrd.2011-019. View