Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Proteomic analysis of the endometrium during early pregnancy in the domestic pig

Justyna Kolakowska A , Serhiy Souchelnytskyi B C D , Ravi Kanth Rao Saini B E F and Anita Franczak A G
+ Author Affiliations
- Author Affiliations

A Department of Animal Physiology, Faculty of Biology and Biotechnology, University of Warmia and Mazury in Olsztyn, Oczapowskiego 1A, 10-719 Olsztyn, Poland.

B Neurocentrum, Karolinska University Hospital, Neurologmottagningen, 171 76, Solna, Stockholm, Sweden.

C Oranta Cancer Diagnostics AB, Norrens väg 73, 752 63, Uppsala, Sweden.

D College of Medicine, Qatar University, Building H12, PO Box 2713, Doha, Qatar.

E Sahlgrenska Cancer Center, University of Gothenburg, Medicinaregatan 1F, Box 425, 405 30, Gothenburg, Sweden.

F The Scripps Research Institute, 10550 North Torrey Pines Road, MB27, La Jolla, CA 92037, USA.

G Corresponding author. Email: anitaf@uwm.edu.pl

Reproduction, Fertility and Development - https://doi.org/10.1071/RD16435
Submitted: 31 October 2016  Accepted: 21 February 2017   Published online: 18 April 2017

Abstract

Reproductive processes in domestic pigs have been studied extensively. Pigs are one of the main sources of meat for human consumption and are an established model for investigations into mammalian, including human, reproductive physiology. Studies of the uterus during early pregnancy will lead to a better understanding of mechanisms governing pregnancy. Proteomics provides the possibility to explore endometrial functions in an unbiased way. The aim of the study was to compare endometrium harvested from Days 12–13 and 15–16 of pregnancy with the corresponding days of the oestrous cycle. We identified endometrial proteins that are unique to the early stages of pregnancy (Days 12–13 and 15–16). Twenty-one proteins were identified that were uniquely expressed on the selected days of pregnancy or the oestrous cycle. Out of 21 identified proteins, 14 referred to the pregnancy periods. Systemic analysis of the identified proteins revealed cell adhesion and cytoskeletal organisation as two of the major functions, both of which are important for the establishment and maintenance of pregnancy. Thrombospondin 1 expression was validated using western blotting analysis and the results suggest its involvement in the adhesiveness of the embryo during the peri-implantation period in pigs.

Additional keywords: implantation, maternal recognition of pregnancy, thrombospondin 1.


References

Adams, J. C. (2001). Thrombospondins: multifunctional regulators of cell interactions. Annu. Rev. Cell Dev. Biol. 17, 25–51.
Thrombospondins: multifunctional regulators of cell interactions.CrossRef | 1:CAS:528:DC%2BD3MXos1OmsL8%3D&md5=55fd88aae7a72a6ac9ab5f549727c6fcCAS | open url image1

Adams, J. C. (2004). Functions of the conserved thrombospondin carboxy-terminal cassette in cell–extracellular matrix interactions and signaling. Int. J. Biochem. Cell Biol. 36, 1102–1114.
Functions of the conserved thrombospondin carboxy-terminal cassette in cell–extracellular matrix interactions and signaling.CrossRef | 1:CAS:528:DC%2BD2cXjt1ant7c%3D&md5=98b48a7b9366082b58c3f9aba3b33c9fCAS | open url image1

Akins, E. L., and Morrisette, M. C. (1968). Gross ovarian changes during oestrus cycle of swine. Am. J. Vet. Res. 29, 1953–1957.
| 1:STN:280:DyaF1M%2FgsVGqsg%3D%3D&md5=26f988f80bc2473618cf21081a9ea714CAS | open url image1

Al-Gubory, K. H., Arianmanesh, M., Garrel, C., Bhattacharya, S., Cash, P., and Fowler, P. A. (2014). Proteomic analysis of the sheep caruncular and intercaruncular endometrium reveals changes in functional proteins crucial for the establishment of pregnancy. Reproduction 147, 599–614.
Proteomic analysis of the sheep caruncular and intercaruncular endometrium reveals changes in functional proteins crucial for the establishment of pregnancy.CrossRef | 1:CAS:528:DC%2BC2cXovFGntbg%3D&md5=7095ea59b2cf3e83f295c88e36c8c350CAS | open url image1

Bazer, F. W., Vallet, J. L., Roberts, R. M., Sharp, D. C., and Thatcher, W. W. (1986). Role of conceptus secretory products in establishment of pregnancy. J. Reprod. Fertil. 76, 841–850.
| 1:CAS:528:DyaL28XitVShtbs%3D&md5=32f744f99672c5b40346e1aba5b511bdCAS | open url image1

Bornstein, P., Agah, A., and Kyriakides, T. R. (2004). The role of thrombospondins 1 and 2 in the regulation of cell–matrix interactions, collagen fibril formation, and the response to injury. Int. J. Biochem. Cell Biol. 36, 1115–1125.
The role of thrombospondins 1 and 2 in the regulation of cell–matrix interactions, collagen fibril formation, and the response to injury.CrossRef | 1:CAS:528:DC%2BD2cXjt1antL4%3D&md5=1fcfd08dbb0dd36d09f2b2ac7eaa11a8CAS | open url image1

Bowen, J. A., Bazer, F. W., and Burghardt, R. C. (1996). Spatial and temporal analyses of integrin and Muc-1 expression in porcine uterine epithelium and trophectoderm in vivo. Biol. Reprod. 55, 1098–1106.
Spatial and temporal analyses of integrin and Muc-1 expression in porcine uterine epithelium and trophectoderm in vivo.CrossRef | 1:CAS:528:DyaK28Xmtlart78%3D&md5=23c8297e2e69e35180e2ef2970b39a7bCAS | open url image1

Burghardt, R. C., Johnson, G. A., Jaeger, L. A., Ka, H., Garlow, J. E., Spencer, T. E., and Bazer, F. W. (2002). Integrins and extracellular matrix proteins at the maternal–fetal interface in domestic animals. Cells Tissues Organs 172, 202–217.
Integrins and extracellular matrix proteins at the maternal–fetal interface in domestic animals.CrossRef | 1:CAS:528:DC%2BD38XpsVSjur8%3D&md5=817c8d2d764ca9f4d81ed85b15d55c67CAS | open url image1

Cencic, A., Guillomot, M., Koren, S., and La, B. C. (2003). Trophoblastic interferons: do they modulate uterine cellular markers at the time of conceptus attachment in the pig? Placenta 24, 862–869.
Trophoblastic interferons: do they modulate uterine cellular markers at the time of conceptus attachment in the pig?CrossRef | 1:CAS:528:DC%2BD3sXnt1amtbs%3D&md5=eef495bb8087dc8f16ca29a9e969e379CAS | open url image1

Chae, J.-I., Kim, J., Lee, S. G., Jeon, Y.-J., Kim, D.-W., Soh, Y., Seo, K. S., Lee, H. K., Choi, N.-J., Ryu, J., Kang, S., Cho, S. K., Lee, D. S., Chung, H. M., and Koo, A. D. (2011). Proteomic analysis of pregnancy-related proteins from pig uterus endometrium during pregnancy. Proteome Sci. 9, 41.
Proteomic analysis of pregnancy-related proteins from pig uterus endometrium during pregnancy.CrossRef | 1:CAS:528:DC%2BC3MXhtFCkurrN&md5=99f9f388649ea4697b341c2144297237CAS | open url image1

Chandrasekaran, L., He, C. Z., Al-Bazarzi, H., Krutzsch, H. C., and Roberts, D. D. (2000). Cell contact-dependent activation of alpha3beta1 integrin modulates endothelial cell responses tothrombospondin-1. Mol. Biol. Cell 11, 2885–2900.
Cell contact-dependent activation of alpha3beta1 integrin modulates endothelial cell responses tothrombospondin-1.CrossRef | 1:CAS:528:DC%2BD3cXmvFSiurs%3D&md5=4a06e497115b8a24f1714ac9b6d8ecb5CAS | open url image1

Choi, Y., Seo, H., Kim, M., and Ka, H. (2009). Dynamic expression of calcium-regulatory molecules, TRPV6 and S100G, in the uterine endometrium during pregnancy in pigs. Biol. Reprod. 81, 1122–1130.
Dynamic expression of calcium-regulatory molecules, TRPV6 and S100G, in the uterine endometrium during pregnancy in pigs.CrossRef | 1:CAS:528:DC%2BD1MXhsV2lt7jI&md5=18bf9bdbc8067838f719cf125fb4efbcCAS | open url image1

Christenson, L. K., Farleyd, D. B., Anderson, L. H., and Ford, S. P. (1994). Luteal maintenance during early pregnancy in the pig: role for prostaglandin E2. Prostaglandins 47, 61–75.
Luteal maintenance during early pregnancy in the pig: role for prostaglandin E2.CrossRef | 1:CAS:528:DyaK2cXht1Gqs7w%3D&md5=6520418735a3b802c487565130e750c7CAS | open url image1

Cross, J. C., Werb, Z., and Fisher, S. J. (1994). Implantation and the placenta: key pieces of the development puzzle. Science 266, 1508–1518.
Implantation and the placenta: key pieces of the development puzzle.CrossRef | 1:CAS:528:DyaK2MXisVGmu78%3D&md5=f872eee7072554486edcfdbe73177cb9CAS | open url image1

Damsky, C., Sutherland, A., and Fisher, S. (1993). Extracellular matrix 5: adhesive interactions in early mammalian embryogenesis, implantation, and placentation. FASEB J. 7, 1320–1329.
| 1:CAS:528:DyaK2cXisl2mtQ%3D%3D&md5=d776a5a7526abdeb7ac98b67bad2a305CAS | open url image1

Dantzer, V. (1985). Electron microscopy of the initial stages of placentation in the pig. Anat. Embryol. (Berl.) 172, 281–293.
Electron microscopy of the initial stages of placentation in the pig.CrossRef | 1:STN:280:DyaL28%2FkvVGqtA%3D%3D&md5=308d515c6bd0e7d33a2f9cee07045446CAS | open url image1

Degrelle, S. A., Blomberg, L. A., Garrett, W. M., Li, R. W., and Talbot, N. C. (2009). Comparative proteomic and regulatory network analyses of the elongating pig conceptus. Proteomics 9, 2678–2694.
Comparative proteomic and regulatory network analyses of the elongating pig conceptus.CrossRef | 1:CAS:528:DC%2BD1MXmtlOmtb8%3D&md5=59ee65155149c5f66942eed3a899dc40CAS | open url image1

Edwards, A. K., van den Heuvel, M. J., Wessels, J. M., Lamarre, J., Croy, B. A., and Tayade, C. (2011). Expression of angiogenic basic fibroblast growth factor, platelet derived growth factor, thrombospondin-1 and their receptors at the porcine maternal–fetal interface. Reprod. Biol. Endocrinol. 9, 5.
Expression of angiogenic basic fibroblast growth factor, platelet derived growth factor, thrombospondin-1 and their receptors at the porcine maternal–fetal interface.CrossRef | 1:CAS:528:DC%2BC3MXht1Kks7k%3D&md5=9e4346bf427167ae23a1551f5c775a44CAS | open url image1

Ferrara, N., Carver-Moore, K., Chen, H., Dowd, M., Lu, L., O’Shea, K. S., Powell-Braxton, L., Hillan, K. J., and Moore, M. W. (1996). Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 380, 439–442.
Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene.CrossRef | 1:CAS:528:DyaK28XitVKqtLk%3D&md5=073cb96192014915e87143c4d3a316e2CAS | open url image1

Franczak, A. (2008). Endometrial and myometrial secretion of androgens and estrone during early pregnancy and luteolysis in pigs. Reprod. Biol. 8, 213–228.
Endometrial and myometrial secretion of androgens and estrone during early pregnancy and luteolysis in pigs.CrossRef | open url image1

Franczak, A., and Kotwica, G. (2008). Secretion of estradiol-17beta by porcine endometrium and myometrium during early pregnancy and luteolysis. Theriogenology 69, 283–289.
Secretion of estradiol-17beta by porcine endometrium and myometrium during early pregnancy and luteolysis.CrossRef | 1:CAS:528:DC%2BD1cXlvV2itA%3D%3D&md5=c56c0c920e84f1cd78462cef2776417bCAS | open url image1

Franczak, A., and Kotwica, G. (2010). Androgens and estradiol-17beta production by porcine uterine cells: In vitro study. Theriogenology 73, 232–241.
Androgens and estradiol-17beta production by porcine uterine cells: In vitro study.CrossRef | 1:CAS:528:DC%2BD1MXhsFGrsrfF&md5=b52363341c26c706a7a56c9cea464fa7CAS | open url image1

Franczak, A., Kotwica, G., Kurowicka, B., Oponowicz, A., Wocławek-Potocka, I., and Petroff, B. K. (2006a). Expression of enzymes of cyclooxygenase pathway and secretion of prostaglandin E2 and F2alpha by porcine myometrium during luteolysis and early pregnancy. Theriogenology 66, 1049–1056.
Expression of enzymes of cyclooxygenase pathway and secretion of prostaglandin E2 and F2alpha by porcine myometrium during luteolysis and early pregnancy.CrossRef | 1:CAS:528:DC%2BD28XotleqsL0%3D&md5=eb118da94e92cd6033735b4545defceaCAS | open url image1

Franczak, A., Kurowicka, B., Oponowicz, A., Petroff, B. K., and Kotwica, G. (2006b). The effect of progesterone on oxytocin-stimulated intracellular mobilization of Ca2+ and prostaglandin E2 and F2alpha secretion from porcine myometrial cells. Prostaglandins Other Lipid Mediat. 81, 37–44.
The effect of progesterone on oxytocin-stimulated intracellular mobilization of Ca2+ and prostaglandin E2 and F2alpha secretion from porcine myometrial cells.CrossRef | 1:CAS:528:DC%2BD28XpvFSjtLs%3D&md5=712cb7ac60079ec27a3d8e251f77abd1CAS | open url image1

Franczak, A., Zmijewska, A., Kurowicka, B., Wojciechowicz, B., and Kotwica, G. (2010). Interleukin 1β-induced synthesis and secre-tion of prostaglandin E2 in the porcine uterus during various periods of pregnancy and the estrous cycle. J. Physiol. Pharmacol. 61, 733–742.
| 1:CAS:528:DC%2BC3MXitVSrtL4%3D&md5=fbe5c6787d9de443e9d8630f3ede876dCAS | open url image1

Franczak, A., Zmijewska, A., Kurowicka, B., Wojciechowicz, B., Petroff, B. K., and Kotwica, G. (2012). The effect of tumor necrosis factor α (TNFα), interleukin 1β (IL1β) and interleukin 6 (IL6) on endometrial PGF2α synthesis, metabolism and release in early-pregnant pigs. Theriogenology 77, 155–165.
The effect of tumor necrosis factor α (TNFα), interleukin 1β (IL1β) and interleukin 6 (IL6) on endometrial PGF2α synthesis, metabolism and release in early-pregnant pigs.CrossRef | 1:CAS:528:DC%2BC3MXhsF2rt7rL&md5=59d95bcd073bd54e83f5bf7c2ebf397aCAS | open url image1

Franczak, A., Wojciechowicz, B., and Kotwica, G. (2013). Transcriptomic analysis of the porcine endometrium during early pregnancy and the estrous cycle. Reprod. Biol. 13, 229–237.
Transcriptomic analysis of the porcine endometrium during early pregnancy and the estrous cycle.CrossRef | open url image1

Franczak, A., Wojciechowicz, B., Kołakowska, J., Zglejc, K., and Kotwica, G. (2014). Transcriptomic analysis of the myometrium during peri-implantation period and luteolysis – the study on the pig model. Funct. Integr. Genomics 14, 673–682.
Transcriptomic analysis of the myometrium during peri-implantation period and luteolysis – the study on the pig model.CrossRef | 1:CAS:528:DC%2BC2cXhsFyhsbrJ&md5=90154d40aae47be2df5110b7ffcd4b6aCAS | open url image1

Garlow, J. E., Ka, H., Johnson, G. A., Burghardt, R. C., Jaeger, L. A., and Bazer, F. W. (2002). Analysis of osteopontin at the maternal–placental interface in pigs. Biol. Reprod. 66, 718–725.
Analysis of osteopontin at the maternal–placental interface in pigs.CrossRef | 1:CAS:528:DC%2BD38XhvVeiur8%3D&md5=0a2b7efa4b4bbe8481ecbfc7321d7ca0CAS | open url image1

Geisert, R. D., and Schmitt, R. A. M. (2002). Early embryonic survival in the pig: can it be improved? J. Anim. Sci. 80, E54–E65. open url image1

Geisert, R. D., Brookbank, J. W., Roberts, R. M., and Bazer, F. W. (1982a). Establishment of pregnancy in the pig: II. Cellular remodeling of the porcine blastocysts during elongation on day 12 of pregnancy. Biol. Reprod. 27, 941–955.
Establishment of pregnancy in the pig: II. Cellular remodeling of the porcine blastocysts during elongation on day 12 of pregnancy.CrossRef | 1:STN:280:DyaL3s%2FnsFKjtw%3D%3D&md5=a5d7194e3cb19662a1b6111481dc610aCAS | open url image1

Geisert, R. D., Renegar, R. H., Thatcher, W. W., Roberts, R. M., and Bazer, F. W. (1982b). Establishment of pregnancy in the pig: I. Interrelationships between preimplantation development of the pig blastocyst and uterine endometrial secretions. Biol. Reprod. 27, 925–939.
Establishment of pregnancy in the pig: I. Interrelationships between preimplantation development of the pig blastocyst and uterine endometrial secretions.CrossRef | 1:CAS:528:DyaL3sXjt1Wrtw%3D%3D&md5=526158a2588bf57129341913a7aa6984CAS | open url image1

Godkin, J. D., and Dore, J. J. E. (1998). Transforming growth factor β and the endometrium. Rev. Reprod. 3, 1–6.
Transforming growth factor β and the endometrium.CrossRef | 1:CAS:528:DyaK1cXht1WrsLg%3D&md5=2c4c9c72e12010098e1bf9b9ab5e0b27CAS | open url image1

Gupta, A., Bazer, F. W., and Jaeger, L. A. (1996). Differential expression of beta transforming growth factors (TGF beta 1, TGF beta 2 and TGF beta 3) and their receptors (type I and type II) in peri-implantation porcine conceptuses. Biol. Reprod. 55, 796–802.
Differential expression of beta transforming growth factors (TGF beta 1, TGF beta 2 and TGF beta 3) and their receptors (type I and type II) in peri-implantation porcine conceptuses.CrossRef | 1:CAS:528:DyaK28Xls1GktL8%3D&md5=37e6fce97fbe47693cd59c29770aafa0CAS | open url image1

Gupta, A., Bazer, F. W., and Jaeger, L. A. (1997). Immunolocalization of acidic and basic fibroblast growth factors in porcine uterine and conceptus tissues. Biol. Reprod. 56, 1527–1536.
Immunolocalization of acidic and basic fibroblast growth factors in porcine uterine and conceptus tissues.CrossRef | 1:CAS:528:DyaK2sXjtlKntrw%3D&md5=6cbcff2026ddcf276a70d2096ef2d5ffCAS | open url image1

Gupta, A., Dekaney, C. M., Bazer, F. W., Madrigal, M. M., and Jaeger, L. A. (1998a). Beta transforming growth factors (TGFβ) at the porcine conceptus–maternal interface. Part II: uterine TGFβ bioactivity and expression of immunoreactive TGF betas (TGFβ1, TGFβ2, and TGFβ3) and their receptors (type I and type II). Biol. Reprod. 59, 911–917.
Beta transforming growth factors (TGFβ) at the porcine conceptus–maternal interface. Part II: uterine TGFβ bioactivity and expression of immunoreactive TGF betas (TGFβ1, TGFβ2, and TGFβ3) and their receptors (type I and type II).CrossRef | 1:CAS:528:DyaK1cXmsVGrtrw%3D&md5=8aea3cffe37d26be22762c62ebfbea76CAS | open url image1

Gupta, A., Ing, N. H., Bazer, F. W., Bustamante, L. S., and Jaeger, L. A. (1998b). Beta transforming growth factors (TGFβ) at the porcine conceptus–maternal interface. Part I: expression of TGFβ1, TGFβ2, and TGFβ3 messenger ribonucleic acids. Biol. Reprod. 59, 905–910.
Beta transforming growth factors (TGFβ) at the porcine conceptus–maternal interface. Part I: expression of TGFβ1, TGFβ2, and TGFβ3 messenger ribonucleic acids.CrossRef | 1:CAS:528:DyaK1cXmsVGrtr8%3D&md5=f59650b2749ecb4bab4f9e6305d5343bCAS | open url image1

Harvey, M. B., Leco, K. J., Arcellana-Panlilio, M. Y., Zhang, X., Edwards, D. R., and Schultz, G. A. (1995). Roles of growth factors during peri-implantation development. Hum. Reprod. 10, 712–718.
Roles of growth factors during peri-implantation development.CrossRef | 1:CAS:528:DyaK2MXmtVWgtro%3D&md5=d895cf2e1b29b8def82e1f20bd22ba28CAS | open url image1

Isenberg, J. S., Martin-Manso, G., Maxhimer, J. B., and Roberts, D. D. (2009). Regulation of nitric oxide signalling by thrombospondin 1: implications for anti-angiogenic therapies. Nat. Rev. Cancer 9, 182–194.
Regulation of nitric oxide signalling by thrombospondin 1: implications for anti-angiogenic therapies.CrossRef | 1:CAS:528:DC%2BD1MXhsVCrtLk%3D&md5=19f0646a87597cc192c9e2f658be823dCAS | open url image1

Jaeger, L. A., Burghardt, R. C., Johnson, G. A., and Bazer, F. W. (2000). Activation of conceptus and maternal integrins by transforming growth factor beta latency associated peptide. Biol. Reprod. Suppl. 62, 281. open url image1

Jaeger, L. A., Spiegel, A. K., Ing, N. H., Johnson, G. A., Bazer, F. W., and Burghardt, R. C. (2005). Functional effects of transforming growth factor on adhesive properties of porcine trophectoderm. Endocrinology 146, 3933–3942.
Functional effects of transforming growth factor on adhesive properties of porcine trophectoderm.CrossRef | 1:CAS:528:DC%2BD2MXpsVegsLw%3D&md5=7c38f735229c6c7ea5ef1636923a89d7CAS | open url image1

Jalali, B. M., Bogacki, M., Dietrich, M., Likszo, P., and Wasielak, M. (2015). Proteomic analysis of porcine endometrial tissue during peri-implantation period reveals altered protein abundance. J. Proteomics 125, 76–88.
Proteomic analysis of porcine endometrial tissue during peri-implantation period reveals altered protein abundance.CrossRef | 1:CAS:528:DC%2BC2MXotlGrtL0%3D&md5=6117c8aa0a1edd316eb12e164eca1cd2CAS | open url image1

Johnson, G. A., Burghardt, R. C., Bazer, F. W., and Spencer, T. E. (2003). Osteopontin: roles in implantation and placentation. Biol. Reprod. 69, 1458–1471.
Osteopontin: roles in implantation and placentation.CrossRef | 1:CAS:528:DC%2BD3sXosV2kur8%3D&md5=cfc397026bb119b05e0afce49521ff09CAS | open url image1

Ka, H., Spencer, T. E., Johnson, G. A., and Bazer, F. W. (2000). Keratinocyte growth factor: expression by endometrial epithelia of the porcine uterus. Biol. Reprod. 62, 1772–1778.
Keratinocyte growth factor: expression by endometrial epithelia of the porcine uterus.CrossRef | 1:CAS:528:DC%2BD3cXjsF2hsbc%3D&md5=1925faac8bfa85bbab52d94731b136d3CAS | open url image1

Keys, J. L., and King, G. J. (1988). Morphological evidence for increased uterine vascular permeability at the time of embryonic attachment in the pig. Biol. Reprod. 39, 473–487.
Morphological evidence for increased uterine vascular permeability at the time of embryonic attachment in the pig.CrossRef | 1:STN:280:DyaL1M%2Fis12qsQ%3D%3D&md5=2440b2faeb12888f9e17d0b6bbb8d1a8CAS | open url image1

Khaleduzzaman, M., Sumiyoshi, H., Ueki, Y., Inoguchi, K., Ninomiya, Y., and Yoshioka, H. (1997). Structure of the human type XIX collagen (COL19A1) gene, which suggests it has arisen from an ancestor gene of the FACIT family. Genomics 45, 304–312.
Structure of the human type XIX collagen (COL19A1) gene, which suggests it has arisen from an ancestor gene of the FACIT family.CrossRef | 1:CAS:528:DyaK2sXntVamtrs%3D&md5=fd6f2c9d8ded825f09b718b94838a49cCAS | open url image1

Lawler, J. (2002). Thrombospondin-1 as an endogenous inhibitor of angiogenesis and tumor growth. J. Cell. Mol. Med. 6, 1–12.
Thrombospondin-1 as an endogenous inhibitor of angiogenesis and tumor growth.CrossRef | 1:CAS:528:DC%2BD38XksVCjt74%3D&md5=9c35d3caf2f2db4cc7f349a083196314CAS | open url image1

Lawler, J., and Detmar, M. (2004). Tumor progression: the effects of thrombospondin-1 and -2. Int. J. Biochem. Cell Biol. 36, 1038–1045.
Tumor progression: the effects of thrombospondin-1 and -2.CrossRef | 1:CAS:528:DC%2BD2cXjt1ant70%3D&md5=a63537b37f0fd639c9e96adb7be0771cCAS | open url image1

Lin, H., Wang, X., Liu, G., Fu, J., and Wang, A. (2007). Expression of alphaV and beta3 integrin subunits during implantation in pig. Mol. Reprod. Dev. 74, 1379–1385.
Expression of alphaV and beta3 integrin subunits during implantation in pig.CrossRef | 1:CAS:528:DC%2BD2sXhtFektr7N&md5=fbe45e5e777da127a3e90011a5b69d3dCAS | open url image1

Linton, N. F., Wessels, J. M., Cnossen, S. A., van den Heuvel, M. J., Croy, B. A., and Tayade, C. (2010). Angiogenic DC-SIGN(+) cells are present at the attachment sites of epitheliochorial placentae. Immunol. Cell Biol. 88, 63–71.
Angiogenic DC-SIGN(+) cells are present at the attachment sites of epitheliochorial placentae.CrossRef | 1:CAS:528:DC%2BC3cXhvFWlsA%3D%3D&md5=e6e6bfc7545db7cff96ee9b5c85bd443CAS | open url image1

Madsen, K. L., Tavernini, M. M., Yachimec, C., Mendrick, D. L., Alfonso, P. J., Buergin, M., Olsen, H. S., Antonaccio, M. J., Thomson, A. B., and Fedorak, R. N. (1998). Stanniocalcin: a novel protein regulating calcium and phosphate transport across mammalian intestine. Am. J. Physiol. 274, G96–G102.
| 1:CAS:528:DyaK1cXotF2ksQ%3D%3D&md5=ae49b56a3a2e808db46a79545d0f41e3CAS | open url image1

Massuto, D. A., Kneese, E. C., Johnson, G. A., Burghardt, R. C., Hooper, R. N., Ing, N. H., and Jaeger, L. A. (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.
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.CrossRef | 1:CAS:528:DC%2BC3cXitFKitb4%3D&md5=540a6f9e38beb28fa56801ef0f926ec5CAS | open url image1

Moeljono, M. P. F., Bazer, F. W., and Thatcher, W. W. (1976). A study of prostaglandin F as luteolysin in swine. I. Effects of prostaglandin F in hysterectomized gilts. Prostaglandins 11, 737–743.
A study of prostaglandin F as luteolysin in swine. I. Effects of prostaglandin F in hysterectomized gilts.CrossRef | 1:CAS:528:DyaE28XksVWgtrw%3D&md5=a916821e5ff33037ffdf3c4c4eee2fa6CAS | open url image1

Nakamura, Y., Tagawa, K., Oka, T., Sasabe, T., Ito, H., Shiwaku, H., La Spada, A. R., and Okazawa, H. (2012). Ataxin-7 associates with microtubules and stabilizes the cytoskeletal network. Hum. Mol. Genet. 21, 1099–1110.
Ataxin-7 associates with microtubules and stabilizes the cytoskeletal network.CrossRef | 1:CAS:528:DC%2BC38XitFCnsLs%3D&md5=0d5a783b17f49f2a98a438554be8f5d0CAS | open url image1

Østrup, E., Bauersachs, S., Blum, H., Wolf, E., and Hyttel, P. (2010). Differential endometrial gene expression in pregnant and nonpregnant sows. Biol. Reprod. 83, 277–285.
Differential endometrial gene expression in pregnant and nonpregnant sows.CrossRef | open url image1

Rashev, P., Georgieva, R., and Rees, D. (2005). Expression of alpha5beta1 integrin and fibronectin during early pregnancy in pigs. Folia Biol. (Praha) 51, 121–125.
| 1:CAS:528:DC%2BD2MXht1CgsrfN&md5=321d2ca5720567a304aaa20c646478f4CAS | open url image1

Ross, J. W., Malayer, J. R., Ritchey, J. W., and Geisert, R. D. (2003). Characterization of the interleukin-1beta system during porcine trophoblastic elongation and early placental attachment. Biol. Reprod. 69, 1251–1259.
Characterization of the interleukin-1beta system during porcine trophoblastic elongation and early placental attachment.CrossRef | 1:CAS:528:DC%2BD3sXnsV2nsL4%3D&md5=dbfd0641d10bf41c04334fb080a56ce9CAS | open url image1

Ross, J. W., Ashworth, M. D., White, F. J., Johnson, G. A., Ayoubi, P. J., DeSilva, U., Whitworth, K. M., Prather, R. S., and Geisert, R. D. (2007). Premature estrogen exposure alters endometrial gene expression to disrupt pregnancy in the pig. Endocrinology 148, 4761–4773.
Premature estrogen exposure alters endometrial gene expression to disrupt pregnancy in the pig.CrossRef | 1:CAS:528:DC%2BD2sXhtFWls7jP&md5=e12fe1ac9e056e1d77c16ad6d70a0300CAS | open url image1

Samborski, A., Graf, A., Krebs, S., Kessler, B., Reichenbach, M., Reichenbach, H.-D., Ulbrich, S. E., and Bauersachs, S. (2013). Transcriptome changes in the porcine endometrium during the preattachment phase. Biol. Reprod. 89, 134.
Transcriptome changes in the porcine endometrium during the preattachment phase.CrossRef | open url image1

Schultz-Cherry, S., and Murphy-Ullrich, J. E. (1993). Thrombospondin causes activation of latent transforming growth factor-beta secreted by endothelial cells by a novel mechanism. J. Cell Biol. 122, 923–932.
Thrombospondin causes activation of latent transforming growth factor-beta secreted by endothelial cells by a novel mechanism.CrossRef | 1:CAS:528:DyaK3sXltV2rs70%3D&md5=31ae151ae87fdf319a6a652ec7725773CAS | open url image1

Schultz-Cherry, S., Lawler, J., and Murphy-Ullrich, J. E. (1994a). The type 1 repeats of thrombospondin 1 activate latent transforming growth factor-beta. J. Biol. Chem. 269, 26783–26788.
| 1:CAS:528:DyaK2cXmt1artrg%3D&md5=8b6456cf0da02907597daf785dcc23ceCAS | open url image1

Schultz-Cherry, S., Ribeiro, S., Gentry, L., and Murphy-Ullrich, J. E. (1994b). Thrombospondin binds and activates the small and large forms of latent transforming growth factor-beta in a chemically defined system. J. Biol. Chem. 269, 26775–26782.
| 1:CAS:528:DyaK2cXmt1artLw%3D&md5=43a514853ccbd6fe80e94283df7d0142CAS | open url image1

Schultz-Cherry, S., Chen, H., Mosher, D. F., Misenheimer, T. M., Krutzsch, H. C., Roberts, D. D., and Murphy-Ullrich, J. E. (1995). Regulation of transforming growth factor-beta activation by discrete sequences of thrombospondin 1. J. Biol. Chem. 270, 7304–7310.
Regulation of transforming growth factor-beta activation by discrete sequences of thrombospondin 1.CrossRef | 1:CAS:528:DyaK2MXkvVOjsrw%3D&md5=e8084e0c4c77c9003af6016f1a1987bdCAS | open url image1

Seo, H., Kim, M., Choi, Y., and Ka, H. (2011). Salivary lipocalin is uniquely expressed in the uterine endometrial glands at the time of conceptus implantation and induced by interleukin 1beta in pigs. Biol. Reprod. 84, 279–287.
Salivary lipocalin is uniquely expressed in the uterine endometrial glands at the time of conceptus implantation and induced by interleukin 1beta in pigs.CrossRef | 1:CAS:528:DC%2BC3MXhsVeltr8%3D&md5=17e26dcfe75d3ee904dee4ac48bb1a40CAS | open url image1

Shaw, L. M., and Olsen, B. R. (1991). FACIT collagens: diverse molecular bridges in extracellular matrices. Trends Biochem. Sci. 16, 191–194.
FACIT collagens: diverse molecular bridges in extracellular matrices.CrossRef | 1:CAS:528:DyaK3MXks1Krt7g%3D&md5=5dc62c17a56544b54c7fc867ec514c0aCAS | open url image1

Simmen, R. C., Simmen, F. A., Hofig, A., Farmer, S. J., and Bazer, F. W. (1990). Hormonal regulation of insulin-like growth factor gene expression in pig uterus. Endocrinology 127, 2166–2174.
Hormonal regulation of insulin-like growth factor gene expression in pig uterus.CrossRef | 1:CAS:528:DyaK3cXmt1Cks78%3D&md5=a011ab099d73b101d3b5af6bb67da7bdCAS | open url image1

Simmen, F. A., Simmen, R. C., Geisert, R. D., Martinat-Botte, F., Bazer, F. W., and Terqui, M. (1992). Differential expression, during the estrous cycle and pre- and postimplantation conceptus development, of messenger ribonucleic acids encoding components of the pig uterine insulin-like growth factor system. Endocrinology 130, 1547–1556.
| 1:CAS:528:DyaK38XhvVymu78%3D&md5=4369f60d0ff1166ed0ba74062441004dCAS | open url image1

Simón, C., Moreno, C., Remohí, J., and Pellicer, A. (1998). Cytokines and embryo implantation. J. Reprod. Immunol. 39, 117–131.
Cytokines and embryo implantation.CrossRef | open url image1

Souchelnytskyi, S. (2005). Bridging proteomics and systems biology: what are the roads to be traveled? Proteomics 5, 4123–4137.
Bridging proteomics and systems biology: what are the roads to be traveled?CrossRef | 1:CAS:528:DC%2BD2MXht1Grtb3N&md5=39c6deb07657aa551ddc32630f92b7afCAS | open url image1

Taraboletti, G., Morbidelli, L., Donnini, S., Parenti, A., Granger, H. J., Giavazzi, R., and Ziche, M. (2000). The heparin binding 25 kDa fragment of thrombospondin-1 promotes angiogenesis and modulates gelatinase and TIMP-2 production in endothelial cells. FASEB J. 14, 1674–1676.
| 1:CAS:528:DC%2BD3cXmsFGqurg%3D&md5=9063d320da7bfed91177a4775b1bf016CAS | open url image1

Tayade, C., Black, G. P., Fang, Y., and Croy, B. A. (2006). Differential gene expression in endometrium, endometrial lymphocytes, and trophoblasts during successful and abortive embryo implantation. J. Immunol. 176, 148–156.
Differential gene expression in endometrium, endometrial lymphocytes, and trophoblasts during successful and abortive embryo implantation.CrossRef | 1:CAS:528:DC%2BD2MXhtlagt7bL&md5=f0f920c9d38dea05a32f925bbe0760f9CAS | open url image1

Tayade, C., Fang, Y., Hilchie, D., and Croy, B. A. (2007). Lymphocyte contributions to altered endometrial angiogenesis during early and midgestation fetal loss. J. Leukoc. Biol. 82, 877–886.
Lymphocyte contributions to altered endometrial angiogenesis during early and midgestation fetal loss.CrossRef | 1:CAS:528:DC%2BD2sXhtFKmt7jP&md5=1e370c329ec93e457d53da8565377746CAS | open url image1

Tuo, W., and Bazer, F. W. (1996). Expression of oncofetal fibronectin in porcine conceptuses and uterus throughout gestation. Reprod. Fertil. Dev. 8, 1207–1213.
Expression of oncofetal fibronectin in porcine conceptuses and uterus throughout gestation.CrossRef | 1:CAS:528:DyaK2sXkslSntA%3D%3D&md5=e22300070466304d583f37db6214b99dCAS | open url image1

Verma, N., Rettenmeier, A. W., and Schmitz-Spanke, S. (2011). Recent advances in the use of Sus scrofa (pig) as a model system for proteomic studies. Proteomics 11, 776–793.
Recent advances in the use of Sus scrofa (pig) as a model system for proteomic studies.CrossRef | 1:CAS:528:DC%2BC3MXhsVSnurw%3D&md5=fd8ca4a7c56b23364e726da2fc03c711CAS | open url image1

Waclawik, A., Blitek, A., and Ziecik, A. J. (2010). Oxytocin and tumor necrosis factor alpha stimulate expression of prostaglandin E2 synthase and secretion of prostaglandin E2 by luminal epithelial cells of the porcine endometrium during early pregnancy. Reproduction 140, 613–622.
Oxytocin and tumor necrosis factor alpha stimulate expression of prostaglandin E2 synthase and secretion of prostaglandin E2 by luminal epithelial cells of the porcine endometrium during early pregnancy.CrossRef | 1:CAS:528:DC%2BC3cXhtlCqurvN&md5=09f6b59d640df2c3cc43fff1bd449ae5CAS | open url image1

Wagner, G. F., Hampong, M., Park, C. M., and Copp, D. H. (1986). Purification, characterization, and bioassay of teleocalcin, a glycoprotein from salmon corpuscles of Stannius. Gen. Comp. Endocrinol. 63, 481–491.
Purification, characterization, and bioassay of teleocalcin, a glycoprotein from salmon corpuscles of Stannius.CrossRef | 1:CAS:528:DyaL28XlsVyntLc%3D&md5=5dc8eb6e1274e35e0ece4a9753333fbaCAS | open url image1

Wang, S., Wu, Z., Sorenson, C. M., Lawler, J., and Sheibani, N. (2003). Thrombospondin-1-deficient mice exhibit increased vascular density during retinal vascular development and are less sensitive to hyperoxia-mediated vessel obliteration. Dev. Dyn. 228, 630–642.
Thrombospondin-1-deficient mice exhibit increased vascular density during retinal vascular development and are less sensitive to hyperoxia-mediated vessel obliteration.CrossRef | 1:CAS:528:DC%2BD2cXhvFCqsQ%3D%3D&md5=8e587cffe5bbcbece92bef3ccf01ab7fCAS | open url image1

Wang, Y., Wang, C., Hou, Z., Miao, K., Zhao, H., Wang, R., Guo, M., Wu, Z., Tian, J., and An, L. (2013). Comparative analysis of proteomic profiles between endometrial caruncular and intercaruncular areas in ewes during the peri-implantation period. J. Anim. Sci. Biotechnol. 4, 39.
Comparative analysis of proteomic profiles between endometrial caruncular and intercaruncular areas in ewes during the peri-implantation period.CrossRef | 1:CAS:528:DC%2BC2cXmslCku74%3D&md5=6216822db0b7b9105fadcd775119296aCAS | open url image1

Weinert, S., Bergmann, N., Luo, X., Erdmann, B., and Gotthardt, M. (2006). M line–deficient titin causes cardiac lethality through impaired maturation of the sarcomere. J. Cell Biol. 173, 559–570.
M line–deficient titin causes cardiac lethality through impaired maturation of the sarcomere.CrossRef | 1:CAS:528:DC%2BD28XltVaqtr4%3D&md5=5efb1fb39ef21059b5f2faf2fb04693eCAS | open url image1

Wojciechowicz, B., Kotwica, G., Kolakowska, J., and Franczak, A. (2013). The activity and localization of 3β-hydroxysteroid dehydrogenase/Δ(5)-Δ(4) isomerase and release of androstenedione and progesterone by uterine tissues during early pregnancy and the estrous cycle in pigs. J. Reprod. Dev. 59, 49–58.
| 1:CAS:528:DC%2BC3sXjvFOjt7Y%3D&md5=82d062394b067a5565aad129e2e8fa9dCAS | open url image1

Yelich, J. V., Pomp, D., and Geisert, R. D. (1997). Ontogeny of elongation and gene expression in the early developing porcine conceptus. Biol. Reprod. 57, 1256–1265.
Ontogeny of elongation and gene expression in the early developing porcine conceptus.CrossRef | 1:CAS:528:DyaK2sXmvFSkur4%3D&md5=2633ba6536ba75666044dd1a93ce856eCAS | open url image1

Yoshioka, H., Zhang, H., Ramirez, F., Mattei, M. G., Moradi-Ameli, M., van der Rest, M., and Gordon, M. K. (1992). Synteny between the loci for a novel FACIT-like collagen locus (D6S228E) and alpha 1 (IX) collagen (COL9A1) on 6q12-q14 in humans. Genomics 13, 884–886.
Synteny between the loci for a novel FACIT-like collagen locus (D6S228E) and alpha 1 (IX) collagen (COL9A1) on 6q12-q14 in humans.CrossRef | 1:CAS:528:DyaK3sXhs1aitrc%3D&md5=e8fb95e44656acece90e9b97cad3f443CAS | open url image1

Zakharchenko, O., Greenwood, C., Lewandowska, A., Hellman, U., Alldridge, L., and Souchelnytskyi, S. (2011). Meta-data analysis as a strategy to evaluate individual and common features of proteomic changes in breast cancer. Cancer Genomics Proteomics 8, 1–14.
| 1:CAS:528:DC%2BC3MXitFSmu7s%3D&md5=78216c1f4229da6529e2e2e0c9948326CAS | open url image1

Zhang, H., Wang, S., Liu, M., Zhang, A., Wu, Z., Zhang, Z., and Li, J. (2013). Differential gene expression in the endometrium on Gestation Day 12 provides insight into sow prolificacy. BMC Genomics 14, 45.
Differential gene expression in the endometrium on Gestation Day 12 provides insight into sow prolificacy.CrossRef | open url image1



Export Citation