Microarray Analysis of Gene Expression in the Uterine Endometrium during the Implantation Period in Pigs |
Kim, Min-Goo
(Division of Biological Science and Technology, Institute of Biomaterials, and IPAID, Yonsei University)
Seo, Hee-Won (Division of Biological Science and Technology, Institute of Biomaterials, and IPAID, Yonsei University) Choi, Yo-Han (Division of Biological Science and Technology, Institute of Biomaterials, and IPAID, Yonsei University) Shim, Jang-Soo (Division of Biological Science and Technology, Institute of Biomaterials, and IPAID, Yonsei University) Kim, Hee-Bal (Department of Agricultural Biotechnology, Seoul National University) Lee, Chang-Kyu (Department of Agricultural Biotechnology, Seoul National University) Ka, Hak-Hyun (Division of Biological Science and Technology, Institute of Biomaterials, and IPAID, Yonsei University) |
1 | Kim, J. G., J. L. Vallet, G. A. Rohrer and R. K. Christenson. 2002. Characterization of porcine uterine estrogen sulfotransferase. Domest. Anim. Endocrinol. 23:493-506. DOI ScienceOn |
2 | La Bonnardiere, C., F. Martinat-Botte, M. Terqui, F. Lefevre, K. Zouari, J. Martal and F. W. Bazer. 1991. Production of two species of interferon by Large White and Meishan pig conceptuses during the peri-attachment period. J. Reprod. Fertil. 91:469-478. DOI ScienceOn |
3 | Lee, S. H., S. H. Zhao, J. C. Recknor, D. Nettleton, S. Orley, S. K. Kang, B. C. Lee, W. S. Hwang and C. K. Tuggle. 2005. Transcriptional profiling using a novel cDNA array identifies differential gene expression during porcine embryo elongation. Mol. Reprod. Dev. 71:129-139. DOI ScienceOn |
4 | Lefevre, F., M. Guillomot, S. D'Andrea, S. Battegay and C. La Bonnardiere. 1998. Interferon-delta: the first member of a novel type I interferon family. Biochimie 80:779-788. DOI ScienceOn |
5 | Leonardsson, G., M. A. Jacobs, R. White, R. Jeffery, R. Poulsom, S. Milligan and M. Parker. 2002. Embryo transfer experiments and ovarian transplantation identify the ovary as the only site in which nuclear receptor interacting protein 1/RIP140 action is crucial for female fertility. Endocrinology 143:700-707. DOI ScienceOn |
6 | Liu, G., H. Lin, X. Zhang, Q. Li, H. Wang, D. Qian, J. Ni and C. Zhu. 2004. Expression of Smad2 and Smad4 in mouse uterus during the oestrous cycle and early pregnancy. Placenta 25:530-537. DOI ScienceOn |
7 | Livak, K. J. and T. D. Schmittgen. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25:402-408. DOI ScienceOn |
8 | Green, J. A., J. G. Kim, K. M. Whitworth, C. Agca and R. S. Prather. 2006. The use of microarrays to define functionally-related genes that are differentially expressed in the cycling pig uterus. Soc. Reprod. Fertil. Suppl. 62:163-176. |
9 | Gupta, A., C. M. Dekaney, F. W. Bazer, M. M. Madrigal and J. A. Jaeger. 1998. Beta transforming growth factors (TGFbeta) at the porcine conceptus-maternal interface. Part II: uterine TGFbeta bioactivity and expression of immunoreactive TGFbetas (TGFbeta1, TGFbeta2, and TGFbeta3) and their receptors (type I and type II). Biol. Reprod. 59:911-917. DOI ScienceOn |
10 | Hanna, J., O. Wald, D. Goldman-Wohl, D. Prus, G. Markel, R. Gazit, G. Katz, R. Haimov-Kochman, N. Fujii, S. Yagel, A. Peled and Mandelboim O. 2003. CXCL12 expression by invasive trophoblasts induces the specific migration of CD16- human natural killer cells. Blood 102:1569-1577. DOI ScienceOn |
11 | Ka, H., H. Seo, M. Kim, S. Moon, H. Kim and C. K. Lee. 2008. Gene expression profiling of the uterus with embryos cloned by somatic cell nuclear transfer on day 30 of pregnancy. Anim. Reprod. Sci. 108:79-91. DOI ScienceOn |
12 | Ka, H., H. Seo, M. Kim, Y. Choi and C. K. Lee. 2009. Identification of differentially expressed genes in the uterine endometrium on day 12 of the estrous cycle and pregnancy in pigs. Mol. Reprod. Dev. 76:75-84. DOI ScienceOn |
13 | Ka, H., L. A. Jaeger, G. A. Johnson, T. E. Spencer and F. W. Bazer. 2001. Keratinocyte growth factor is up-regulated by estrogen in the porcine uterine endometrium and functions in trophectoderm cell proliferation and differentiation. Endocrinology 142:2303-2310. DOI ScienceOn |
14 | Ka, H., T. E. Spencer, G. A. Johnson and F. W. Bazer. 2000. Keratinocyte growth factor: expression by endometrial epithelia of the porcine uterus. Biol. Reprod. 62:1772-1778. DOI ScienceOn |
15 | Kaeoket, K., E. Persson and A. M. Dalin. 2003. Influence of pre-ovulatory insemination and early pregnancy on the infiltration by cells of the immune system in the sow endometrium. Anim. Reprod. Sci. 75:55-71. DOI ScienceOn |
16 | Geisert, R. D., R. M. Brenner, R. J. Moffatt, J. P. Harney, T. Yellin and F. W. Bazer. 1993.Changes in oestrogen receptor protein, mRNA expression and localization in the endometrium of cyclic and pregnant gilts. Reprod. Fertil. Dev. 5:247-260. DOI |
17 | Fritah, A. 2009. Control of skeletal muscle metabolic properties by the nuclear receptor corepressor RIP140. Appl. Physiol. Nutr. Metab. 34:362-367. DOI |
18 | Garlow, J. E., H. Ka, G. A. Johnson, R. C. Burghardt, L. A. Jaeger and F. W. Bazer. 2002. Analysis of osteopontin at the maternal-placental interface in pigs. Biol. Reprod. 66:718-725. DOI ScienceOn |
19 | Geisert, R. D., R. H. Renegar, W. W. Thatcher, R. M. Roberts and F. W. Bazer. 1982. Establishment of pregnancy in the pig: I. Interrelationships between preimplantation development of the pig blastocyst and uterine endometrial secretions. Biol. Reprod. 27:925-939. DOI ScienceOn |
20 | Geisert, R. D., T. N. Pratt, F. W. Bazer, J. S. Mayes and G. H. Watson. 1994. Immunocytochemical localization and changes in endometrial progestin receptor protein during the porcine oestrous cycle and early pregnancy. Reprod. Fertil. Dev. 6:749-760. DOI |
21 | Geisert, R. D. and J. V. Yelich. 1997. Regulation of conceptus development and attachment in pigs. J. Reprod. Fertil. Suppl. 52:133-149. |
22 | Gendler, S. J. and A. P. Spicer. 1995. Epithelial mucin genes. Annu. Rev. Physiol. 57:607-634. DOI ScienceOn |
23 | Gipson, I. K., S. B. Ho, S. J. Spurr-Michaud, A. S. Tisdale, Q. Zhan, E. Torlakovic, J. Pudney, D. J. Anderson, N. W. Toribara and J. A. Hill 3rd. 1997. Mucin genes expressed by human female reproductive tract epithelia. Biol. Reprod. 56:999-1011. DOI ScienceOn |
24 | Glynn, D. J., B. T. Sherman, D. A. Hosack, J. Yang, M. W. Baseler, H. C. Lane and R. A. Lempicki. 2003. DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol. 4:P3. DOI |
25 | Bischof, R. J., R. Lee, C. S. Lee and E. Meeusen. 1996. Dynamic changes in the lymphocyte subpopulations of pig uterine lymph nodes. Vet. Immunol. Immunopathol. 51:315-324. DOI ScienceOn |
26 | Bazer, F. W. and W. W. Thatcher. 1977. Theory of maternal recognition of pregnancy in swine based on estrogen controlled endocrine versus exocrine secretion of prostaglandin F2alpha by the uterine endometrium. Prostaglandins 14:397-400. DOI ScienceOn |
27 | Bazer, F. W., J. L. Vallet, R. M. Roberts, D. C. Sharp and W. W. Thatcher. 1986. Role of conceptus secretory products in establishment of pregnancy. J. Reprod. Fertil. 76:841-850. DOI ScienceOn |
28 | Bennett, G. L. and K. A. Leymaster. 1989. Integration of ovulation rate, potential embryonic viability and uterine capacity into a model of litter size in swine. J. Anim. Sci. 67:1230-1241. |
29 | Caballero, V., R. Ruiz, J. A. Sainz, M. Cruz, M. A. Lopez-Nevot, J. J. Galan, L. M. Real, F. de Castro, V. Lopez-Villaverde and A. Ruiz. 2005. Preliminary molecular genetic analysis of the Receptor Interacting Protein 140 (RIP140) in women affected by endometriosis. J. Exp. Clin. Assist. Reprod. 2:11. DOI |
30 | Carson, D. D., M. M. DeSouza and E. G. Regisford. 1998. Mucin and proteoglycan functions in embryo implantation. Bioessays 20:577-583. DOI |
31 | Cencic, A., M. Guillomot, S. Koren and C. La Bonnardiere. 2003. Trophoblastic interferons: do they modulate uterine cellular markers at the time of conceptus attachment in the pig? Placenta 24:862-869. DOI ScienceOn |
32 | Croy, B. A., W. Wood and G. J. King. 1987. Evaluation of intrauterine immune suppression during pregnancy in a species with epitheliochorial placentation. J. Immunol. 139:1088-1095. |
33 | Whitworth, K. M., C. Agca, J. G. Kim, R. V. Patel, G. K. Springer, N. J. Bivens, L. J. Forrester, N. Mathialagan, J. A. Green and R. S. Prather. 2005. Transcriptional profiling of pig embryogenesis by using a 15-K member unigene set specific for pig reproductive tissues and embryos. Biol. Reprod. 72:1437-1451. DOI ScienceOn |
34 | Dantzer, V. 1985. Electron microscopy of the initial stages of placentation in the pig. Anat. Embryol. (Berl). 172:281-293. DOI |
35 | Banchereau, J., F. Briere, C. Caux, J. Davoust, S. Lebecque, Y. J. Liu, B. Pulendran and K. Palucka. 2000. Immunobiology of dendritic cells. Annu. Rev. Immunol. 18:767-811. DOI ScienceOn |
36 | Kao, L. C., S. Tulac, S. Lobo, B. Imani, J. P. Yang, A. Germeyer, K. Osteen, R. N. Taylor, B. A. Lessey and L. C. Giudice. 2002. Global gene profiling in human endometrium during the window of implantation. Endocrinology 143:2119-2138. DOI ScienceOn |
37 | Ushizawa, K., C. B. Herath, K. Kaneyama, S. Shiojima, A. Hirasawa, T. Takahashi, K. Imai, K. Ochiai, T. Tokunaga, Y. Tsunoda, G. Tsujimoto and K. Hashizume. 2004. cDNA microarray analysis of bovine embryo gene expression profiles during the pre-implantation period. Reprod. Biol. Endocrinol. 2:77. DOI ScienceOn |
38 | Vallee, M., D. Beaudry, C. Roberge, J. J. Matte, R. Blouin and M. F. Palin. 2003. Isolation of differentially expressed genes in conceptuses and endometrial tissue of sows in early gestation. Biol. Reprod. 69:1697-1706. DOI ScienceOn |
39 | White, F. J., J. W. Ross, M. M. Joyce, R. D. Geisert, R. C. Burghardt and G. A. Johnson. 2005. Steroid regulation of cell specific secreted phosphoprotein 1 (osteopontin) expression in the pregnant porcine uterus. Biol. Reprod. 73:1294-1301. DOI ScienceOn |
40 | White, R., G. Leonardsson, I. Rosewell, M. Ann Jacobs, S. Milligan and M. Parker. 2000. The nuclear receptor co-repressor nrip1 (RIP140) is essential for female fertility. Nat. Med. 6:1368-1374. DOI ScienceOn |
41 | Wu, X., D. J. Li, M. M. Yuan, Y. Zhu and M. Y. Wang. 2004. The expression of CXCR4/CXCL12 in first-trimester human trophoblast cells. Biol. Reprod. 70:1877-1885. DOI ScienceOn |
42 | Zhou, W. H., M. R. Du, L. Dong, J. Yu and D. J. Li. 2008. Chemokine CXCL12 promotes the cross-talk between trophoblasts and decidual stromal cells in human first-trimester pregnancy. Hum. Reprod. 23:2669-2679. DOI ScienceOn |
43 | Ziecik, A. J. 2002. Old, new and the newest concepts of inhibition of luteolysis during early pregnancy in pig. Domest. Anim. Endocrinol. 23:265-275. DOI ScienceOn |
44 | Ross, J. W., J. R. Malayer, J. W. Ritchey and R. D. Geisert. 2003a. Characterization of the interleukin-1beta system during porcine trophoblastic elongation and early placental attachment. Biol. Reprod. 69:1251-1259. DOI ScienceOn |
45 | Ross, J. W., M. D. Ashworth, A. G. Hurst, J. R. Malayer and R. D. Geisert. 2003b. Analysis and characterization of differential gene expression during rapid trophoblastic elongation in the pig using suppression subtractive hybridization. Reprod. Biol. Endocrinol. 1:23. DOI ScienceOn |
46 | Satterfield, M. C., G. Song, K. J. Kochan, P. K. Riggs, R. M. Simmons, C. G. Elsik, D. L. Adelson, F. W. Bazer, H. Zhou and T. E. Spencer. 2009. Discovery of candidate genes and pathways in the endometrium regulating ovine blastocyst growth and conceptus elongation. Physiol. Genomics 39:85-99. DOI ScienceOn |
47 | ten Dijke, P. and C. S. Hill. 2004. New insights into TGF-beta-Smad signalling. Trends Biochem. Sci. 29:265-273. DOI ScienceOn |
48 | Seo, H., M. Kim,Y. Choi, C. K. Lee and H. Ka. 2008. Analysis of lysophosphatidic acid (LPA) receptor and LPA-induced endometrial prostaglandin-endoperoxide synthase 2 expression in the porcine uterus. Endocrinology 149:6166-6175. DOI ScienceOn |
49 | Spencer, T. E. and F. W. Bazer. 2004. Conceptus signals for establishment and maintenance of pregnancy. Reprod. Biol. Endocrinol. 2:49. DOI ScienceOn |
50 | Spencer, T. E., G. A. Johnson, F. W. Bazer and R. C. Burghardt. 2004. Implantation mechanisms: insights from the sheep. Reproduction 128:657-668. DOI ScienceOn |
51 | Tsai, S., J. P. Cassady, B. A. Freking, D. J. Nonneman, G. A. Rohrer and J. A. Piedrahita. 2006. Annotation of the Affymetrix porcine genome microarray. Anim. Genet. 37:423-424. DOI ScienceOn |
52 | Tuo, W., J. P. Harney and F. W. Bazer. 1996. Developmentally regulated expression of interleukin-1 beta by peri-implantation conceptuses in swine. J. Reprod. Immunol. 31:185-198. DOI ScienceOn |
53 | Mansouri-Attia, N., J. Aubert, P. Reinaud, C. Giraud-Delville, G. Taghouti, L. Galio, R. E. Everts, S. Degrelle, C. Richard, I. Hue, X. Yang, X. C. Tian, H. A. Lewin, J. P. Renard and O. Sandra. 2009. Gene expression profiles of bovine caruncular and intercaruncular endometrium at implantation. Physiol. Genomics 39:14-27. DOI ScienceOn |
54 | Massuto, D. A., E. C. Kneese, G. A. Johnson, R. C. Burghardt, R. N. Hooper, N. H. Ing and L. A. Jaeger. 2010. Transforming growth factor beta (TGFB) signaling is activated during porcine implantation: proposed role for latency-associated peptide interactions with integrins at the conceptus-maternal interface. Reproduction 139:465-478. DOI ScienceOn |
55 | Ostrup, E., S. Bauersachs, H. Blum, E. Wolf and P. Hyttel. 2010. Differential endometrial gene expression in pregnant and nonpregnant sows. Biol. Reprod. 83:277-285. DOI ScienceOn |
56 | Moritani, S., R. Kushima, S. Ichihara, H. Okabe, T. Hattori, T. K. Kobayashi and S. G. Silverberg. 2005. Eosinophilic cell change of the endometrium: a possible relationship to mucinous differentiation. Mod. Pathol. 18:1243-1248. DOI ScienceOn |
57 | Murdoch, C. 2000. CXCR4: chemokine receptor extraordinaire. Immunol. Rev. 177:175-184. DOI ScienceOn |
58 | Nephew, K. P., X. Long, E. Osborne, K. A. Burke, A. Ahluwalia and R. M. Bigsby. 2000. Effect of estradiol on estrogen receptor expression in rat uterine cell types. Biol. Reprod. 62:168-177. DOI ScienceOn |
59 | Reese, J., S. K. Das, B.C. Paria, H. Lim, H. Song, H. Matsumoto, K. L. Knudtson, R. N. DuBois and S. K. Dey. 2001. Global gene expression analysis to identify molecular markers of uterine receptivity and embryo implantation. J. Biol. Chem. 276:44137-44145. DOI ScienceOn |
60 | Repnik, U., T. Tilburgs, D. L. Roelen, B. J. van der Mast, H. H. Kanhai, S. Scherjon and F. H. Claas. 2008. Comparison of macrophage phenotype between decidua basalis and decidua parietalis by flow cytometry. Placenta 29:405-412. DOI ScienceOn |