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http://dx.doi.org/10.12749/RDB.2014.38.1.21

EGF, IGF-I, VEGF and CSF2: Effects on Trophectoderm of Porcine Conceptus  

Jeong, Wooyoung (Department of Animal Resources Science, Dankook University)
Song, Gwonhwa (Department of Biotechnology, Korea University)
Publication Information
Abstract
The majority of early embryonic mortality in pregnancy occurs during the peri-implantation stage, suggesting that this period is important for conceptus viability and the establishment of pregnancy. Successful establishment of pregnancy in all mammalian species depends on the orchestrated molecular events that transpire at the conceptus-uterine interface during the peri-implantation period. This maternal-conceptus interaction is especially crucial in pigs because in them non-invasive epitheliochorial placentation occurs, in which the pre-implantation phase is prolonged. During the pre-implantation period, conceptus survival and the establishment of pregnancy are known to depend on the developing conceptus receiving an adequate supply of histotroph, which contains a wide range of nutrients and growth factors. Evidence links growth factors including epidermal growth factor (EGF), insulin-like growth factor-I (IGF-I), vascular endothelial growth factor (VEGF), and colony-stimulating factor 2 (CSF2) to embryogenesis or implantation in various mammalian species; however, in the case of pig, little is known about such functions of these growth factors, especially their regulatory mechanisms at the maternal-conceptus interface. Our research group has presented evidence for promising growth factors affecting cellular activities of primary porcine trophectoderm (pTr) cells, and we have identified potential intracellular signaling pathways responsible for the activities induced by these factors. Therefore, this review focuses on promising growth factors at the maternal-conceptus interface regulating the development of the porcine conceptus and playing pivotal roles in implantation events during early pregnancy in pigs.
Keywords
Peri-implantation; EGF; IGF-I; VEGF; CSF2;
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1 Yelich JV, Pomp D, Geisert RD (1997a): Detection of transcripts for retinoic acid receptors, retinolbinding protein, and transforming growth factors during rapid trophoblastic elongation in the porcine conceptus. Biol Reprod 57:286-294.   DOI   ScienceOn
2 Ziecik AJ, Waclawik A, Kaczmarek MM, Blitek A, Jalali BM, Andronowska A (2011): Mechanisms for the establishment of pregnancy in the pig. Reprod Domest Anim 46 Suppl 3:31-41. (Received: 3 March 2014/ Accepted: 5 March 2014)   DOI
3 Tremellen KP, Seamark RF, Robertson SA (1998): Seminal transforming growth factor beta1 stimulates granulocyte-macrophage colony-stimulating factor production and inflammatory cell recruitment in the murine uterus. Biol Reprod 58:1217-1225.   DOI   ScienceOn
4 Tuo W, Harney JP, Bazer FW (1995): Colony-stimulating factor-1 in conceptus and uterine tissues in pigs. Biol Reprod 53:133-142.   DOI   ScienceOn
5 Tuo W, Harney JP, Bazer FW (1996): Developmentally regulated expression of interleukin-1 beta by peri-implantation conceptuses in swine. J Reprod Immunol 31:185-198.   DOI   ScienceOn
6 Vaughan TJ, James PS, Pascall JC, Brown KD (1992): Expression of the genes for TGF alpha, EGF and the EGF receptor during early pig development. Development 116:663-669.
7 Waltenberger J, Claesson-Welsh L, Siegbahn A, Shibuya M, Heldin CH (1994): Different signal transduction properties of KDR and Flt1, two receptors for vascular endothelial growth factor. J Biol Chem 269:26988-26995.
8 Wang H, Dey SK (2006): Roadmap to embryo implantation: clues from mouse models. Nat Rev Genet 7:185-199.   DOI   ScienceOn
9 Wieduwilt MJ, Moasser MM (2008): The epidermal growth factor receptor family: biology driving targeted therapeutics. Cell Mol Life Sci 65:1566-1584.   DOI   ScienceOn
10 Wiktor-Jedrzejczak W, Bartocci A, Ferrante AW Jr, Ahmed-Ansari A, Sell KW, Pollard JW, Stanley ER (1990): Total absence of colony-stimulating factor 1 in the macrophage-deficient osteopetrotic (op/op) mouse. Proc Natl Acad Sci U S A 87:4828-4832.   DOI   ScienceOn
11 Wilcox AJ, Baird DD, Weinberg CR (1999): Time of implantation of the conceptus and loss of pregnancy. N Engl J Med 340:1796-1799.   DOI   ScienceOn
12 Spencer TE, Bazer FW (2004): Conceptus signals for establishment and maintenance of pregnancy. Reprod Biol Endocrinol 2:49.   DOI   ScienceOn
13 Spencer TE, Johnson GA, Bazer FW, Burghardt RC (2007): Fetal-maternal interactions during the establishment of pregnancy in ruminants. Soc Reprod Fertil Suppl 64:379-396.
14 Squires MS, Hudson EA, Howells L, Sale S, Houghton CE, Jones JL, Fox LH, Dickens M, Prigent SA, Manson MM (2003): Relevance of mitogen activated protein kinase (MAPK) and phosphotidylinositol- 3-kinase/protein kinase B (PI3K/PKB) pathways to induction of apoptosis by curcumin in breast cells. Biochem Pharmacol 65:361-376.   DOI   ScienceOn
15 Stroband HW, Van der Lende T (1990): Embryonic and uterine development during early pregnancy in pigs. J Reprod Fertil Suppl 40:261-277.
16 Surveyor GA, Gendler SJ, Pemberton L, Das SK, Chakraborty I, Julian J, Pimental RA, Wegner CC, Dey SK, Carson DD (1995): Expression and steroid hormonal control of Muc-1 in the mouse uterus. Endocrinology 136:3639-3647.   DOI
17 Thomas CY, Chouinard M, Cox M, Parsons S, Stallings- Mann M, Garcia R, Jove R, Wharen R (2003): Spontaneous activation and signaling by overexpressed epidermal growth factor receptors in glioblastoma cells. Int J Cancer 104:19-27.   DOI   ScienceOn
18 Tomanek M, Kopecny V, Kanka J (1989): Genome reactivation in developing early pig embryos: an ultrastructural and autoradiographic analysis. Anat Embryol (Berl) 180:309-316.   DOI
19 Tranguch S, Daikoku T, Guo Y, Wang H, Dey SK (2005): Molecular complexity in establishing uterine receptivity and implantation. Cell Mol Life Sci 62:1964-1973.   DOI   ScienceOn
20 Robertson SA, Sjoblom C, Jasper MJ, Norman RJ, Seamark RF (2001): Granulocyte-macrophage colony- stimulating factor promotes glucose transport and blastomere viability in murine preimplantation embryos. Biol Reprod 64:1206-1215.   DOI   ScienceOn
21 Robinson CJ, Stringer SE (2001): The splice variants of vascular endothelial growth factor (VEGF) and their receptors. J Cell Sci 114:853-865.
22 Ross JW, Malayer JR, Ritchey JW, Geisert RD (2003): Characterization of the interleukin-1beta system during porcine trophoblastic elongation and early placental attachment. Biol Reprod 69:1251-1259.   DOI   ScienceOn
23 Schultz GA, Heyner S (1993): Growth factors in preimplantation mammalian embryos. Oxf Rev Reprod Biol 15:43-81.
24 Simmen FA, Simmen RC, Geisert RD, Martinat- Botte F, Bazer FW, 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.
25 Simmen RC, Simmen FA, Hofig A, Farmer SJ, Bazer FW (1990): Hormonal regulation of insulinlike growth factor gene expression in pig uterus. Endocrinology 127:2166-2174.   DOI   ScienceOn
26 Sjoblom C, Roberts CT, Wikland M, Robertson SA (2005): Granulocyte-macrophage colony-stimulating factor alleviates adverse consequences of embryo culture on fetal growth trajectory and placental morphogenesis. Endocrinology 146:2142-2153.   DOI   ScienceOn
27 Spencer TE, Bazer FW (1995): Temporal and spatial alterations in uterine estrogen receptor and progesterone receptor gene expression during the estrous cycle and early pregnancy in the ewe. Biol Reprod 53:1527-1543.   DOI   ScienceOn
28 Psychoyos A (1973): Hormonal control of ovoimplantation. Vitam Horm 31:201-256.
29 Pusateri AE, Rothschild MF, Warner CM, Ford SP (1990): Changes in morphology, cell number, cell size and cellular estrogen content of individual littermate pig conceptuses on days 9 to 13 of gestation. J Anim Sci 68:3727-3735.   DOI
30 Qiu Q, Yang M, Tsang BK, Gruslin A (2004): Both mitogen-activated protein kinase and phosphatidylinositol 3-kinase signalling are required in epidermal growth factor-induced human trophoblast migration. Mol Hum Reprod 10:677-684.   DOI   ScienceOn
31 Rapoport AP, Abboud CN, DiPersio JF (1992): Granulocyte- macrophage colony-stimulating factor (GMCSF) and granulocyte colony-stimulating factor (GCSF): receptor biology, signal transduction, and neutrophil activation. Blood Rev 6:43-57.   DOI   ScienceOn
32 Rechler MM, Nissley SP (1985): The nature and regulation of the receptors for insulin-like growth factors. Annu Rev Physiol 47:425-442.   DOI   ScienceOn
33 Reima I, Lehtonen E, Virtanen I, Flechon JE (1993): The cytoskeleton and associated proteins during cleavage, compaction and blastocyst differentiation in the pig. Differentiation 54:35-45.   DOI
34 Reynolds LP, Kirsch JD, Kraft KC, Redmer DA (1998): Time-course of the uterine response to estradiol- 17beta in ovariectomized ewes: expression of angiogenic factors. Biol Reprod 59:613-620.   DOI   ScienceOn
35 Robertson SA (2007): GM-CSF regulation of embryo development and pregnancy. Cytokine Growth Factor Rev 18:287-298.   DOI   ScienceOn
36 Robertson SA, Seamark RF, Guilbert LJ, Wegmann TG (1994): The role of cytokines in gestation. Crit Rev Immunol 14:239-292.   DOI
37 Mukku VR, Stancel GM (1985): Regulation of epidermal growth factor receptor by estrogen. J Biol Chem 260:9820-9824.
38 Nara BS, Darmadja D, First NL (1981): Effect of removal of follicles, corpora lutea or ovaries on maintenance of pregnancy in swine. J Anim Sci 52:794-801.   DOI
39 Nelson KG, Takahashi T, Bossert NL, Walmer DK, McLachlan JA (1991): Epidermal growth factor replaces estrogen in the stimulation of female genitaltract growth and differentiation. Proc Natl Acad Sci U S A 88:21-25.   DOI   ScienceOn
40 Paria BC, Huet-Hudson YM, Dey SK (1993): Blastocyst's state of activity determines the "window" of implantation in the receptive mouse uterus. Proc Natl Acad Sci U S A 90:10159-10162.   DOI   ScienceOn
41 Perry JS (1981): The mammalian fetal membranes. J Reprod Fertil 62:321-235.   DOI   ScienceOn
42 Perry JS, Heap RB, Amoroso EC (1973): Steroid hormone production by pig blastocysts. Nature 245:45-47.   DOI   ScienceOn
43 Perry JS, Heap RB, Burton RD, Gadsby JE (1976): Endocrinology of the blastocyst and its role in the establishment of pregnancy. J Reprod Fertil Suppl:85-104.
44 Polge C, Rowson LE, Chang MC (1966): The effect of reducing the number of embryos during early stages of gestation on the maintenance of pregnancy in the pig. J Reprod Fertil 12:395-397.   DOI   ScienceOn
45 Pollard JW (1997): Role of colony-stimulating factor- 1 in reproduction and development. Mol Reprod Dev 46:54-60; discussion 60-61.   DOI
46 Pope WF (1988): Uterine asynchrony: a cause of embryonic loss. Biol Reprod 39:999-1003.   DOI   ScienceOn
47 Pope WF, Lawyer MS, Nara BS, First NL (1986): Effect of asynchronous superinduction on embryo survival and range of blastocyst development in swine. Biol Reprod 35:133-137.   DOI   ScienceOn
48 Llimargas M, Casanova J (1999): EGF signalling regulates cell invagination as well as cell migration during formation of tracheal system in Drosophila. Dev Genes Evol 209:174-179.   DOI
49 Mattson BA, Overstrom EW, Albertini DF (1990): Transitions in trophectoderm cellular shape and cytoskeletal organization in the elongating pig blastocyst. Biol Reprod 42:195-205.   DOI   ScienceOn
50 McKinnon T, Chakraborty C, Gleeson LM, Chidiac P, Lala PK (2001): Stimulation of human extravillous trophoblast migration by IGF-II is mediated by IGF type 2 receptor involving inhibitory G protein( s) and phosphorylation of MAPK. J Clin Endocrinol Metab 86:3665-3674.   DOI   ScienceOn
51 Meikle A, Sahlin L, Ferraris A, Masironi B, Blanc JE, Rodriguez-Irazoqui M, Rodriguez-Pinon M, Kindahl H, Forsberg M (2001): Endometrial mRNA expression of oestrogen receptor alpha, progesterone receptor and insulin-like growth factor-I (IGFI) throughout the bovine oestrous cycle. Anim Reprod Sci 68:45-56.   DOI   ScienceOn
52 Keys JL, King GJ (1990): Microscopic examination of porcine conceptus-maternal interface between days 10 and 19 of pregnancy. Am J Anat 188:221-238.   DOI   ScienceOn
53 Michael DD, Wagner SK, Ocon OM, Talbot NC, Rooke JA, Ealy AD (2006): Granulocyte-macrophage colony-stimulating-factor increases interferon-tau protein secretion in bovine trophectoderm cells. Am J Reprod Immunol 56:63-67.   DOI   ScienceOn
54 Miese-Looy G, VAN DEN Heuvel MJ, Edwards AK, Lamarre J, Tayade C (2012): Expression of insulinlike growth factor (IGF) family members in porcine pregnancy. J Reprod Dev 58:51-60.   DOI
55 Modric T, Kowalski AA, Green ML, Simmen RC, Simmen FA (2000): Pregnancy-dependent expression of leukaemia inhibitory factor (LIF), LIF receptorbeta and interleukin-6 (IL-6) messenger ribonucleic acids in the porcine female reproductive tract. Placenta 21:345-353.   DOI   ScienceOn
56 Kim J, Song G, Gao H, Farmer JL, Satterfield MC, Burghardt RC, Wu G, Johnson GA, Spencer TE, Bazer FW (2008): Insulin-like growth factor II activates phosphatidylinositol 3-kinase-protooncogenic protein kinase 1 and mitogen-activated protein kinase cell signaling pathways, and stimulates migration of ovine trophectoderm cells. Endocrinology 149:3085-3094.   DOI   ScienceOn
57 Kol S, Kehat I, Adashi EY (2002): Ovarian interleukin- 1-induced gene expression: privileged genes threshold theory. Med Hypotheses 58:6-8.   DOI   ScienceOn
58 Lawson RA, Parr RA, Cahill LP (1983): Evidence for maternal control of blastocyst growth after asynchronous transfer of embryos to the uterus of the ewe. J Reprod Fertil 67:477-483.   DOI   ScienceOn
59 Lefevre F, Guillomot M, D'Andrea S, Battegay S, La Bonnardiere C (1998): Interferon-delta: the first member of a novel type I interferon family. Biochimie 80:779-788.   DOI   ScienceOn
60 Lessey BA (1995): Integrins and reproduction revisited. Eur J Obstet Gynecol Reprod Biol 62:264-265.   DOI   ScienceOn
61 Jeong W, Kim J, Bazer FW, Song G (2014b): Stimulatory effect of vascular endothelial growth factor on proliferation and migration of porcine trophectoderm cells and their regulation by the phosphatidylinositol- 3-kinase-AKT and mitogen-activated protein kinase cell signaling pathways. Biol Reprod.
62 Lessey BA, Killam AP, Metzger DA, Haney AF, Greene GL, McCarty KS Jr (1988): Immunohistochemical analysis of human uterine estrogen and progesterone receptors throughout the menstrual cycle. J Clin Endocrinol Metab 67:334-340.   DOI
63 Lessey BA, Yeh I, Castelbaum AJ, Fritz MA, Ilesanmi AO, Korzeniowski P, Sun J, Chwalisz K (1996): Endometrial progesterone receptors and markers of uterine receptivity in the window of implantation. Fertil Steril 65:477-483.   DOI
64 Letcher R, Simmen RC, Bazer FW, Simmen FA (1989): Insulin-like growth factor-I expression during early conceptus development in the pig. Biol Reprod 41: 1143-1151.   DOI   ScienceOn
65 Jeong W, Kim J, Bazer FW, Song G (2013): Epidermal growth factor stimulates proliferation and migration of porcine trophectoderm cells through protooncogenic protein kinase 1 and extracellularsignal- regulated kinases 1/2 mitogen-activated protein kinase signal transduction cascades during early pregnancy. Mol Cell Endocrinol 381:302-311.   DOI   ScienceOn
66 Jeong W, Song G, Bazer FW, Kim J (2014c): Insulin- like growth factor I induces proliferation and migration of porcine trophectoderm cells through multiple cell signaling pathways, including protooncogenic protein kinase 1 and mitogen-activated protein kinase. Mol Cell Endocrinol 384:175-184.   DOI   ScienceOn
67 Jeong W, Kim J, Bazer FW, Song G (2014a): Proliferation- stimulating effect of colony stimulating factor 2 on porcine trophectoderm cells is mediated by activation of phosphatidylinositol 3-kinase and extracellular signal-regulated kinase 1/2 mitogen-activated protein kinase. PLoS One 9:e88731.   DOI
68 Jones JI, Clemmons DR (1995): Insulin-like growth factors and their binding proteins: biological actions. Endocr Rev 16:3-34.
69 Joslin EJ, Opresko LK, Wells A, Wiley HS, Lauffenburger DA (2007): EGF-receptor-mediated mammary epithelial cell migration is driven by sustained ERK signaling from autocrine stimulation. J Cell Sci 120: 3688-3699.   DOI   ScienceOn
70 Ka H, Jaeger LA, Johnson GA, Spencer TE, Bazer FW (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
71 Kane MT, Morgan PM, Coonan C (1997): Peptide growth factors and preimplantation development. Hum Reprod Update 3:137-157.   DOI   ScienceOn
72 Guillomot M (1995): Cellular interactions during implantation in domestic ruminants. J Reprod Fertil Suppl 49:39-51.
73 Gupta A, Bazer FW, Jaeger LA (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.   DOI   ScienceOn
74 Gupta A, Ing NH, Bazer FW, Bustamante LS, Jaeger LA (1998): Beta transforming growth factors (TGFss) at the porcine conceptus-maternal interface. Part I: expression of TGFbeta1, TGFbeta2, and TGFbeta3 messenger ribonucleic acids. Biol Reprod 59:905-910.   DOI   ScienceOn
75 Hannan NJ, Paiva P, Meehan KL, Rombauts LJ, Gardner DK, Salamonsen LA (2011): Analysis of fertility- related soluble mediators in human uterine fluid identifies VEGF as a key regulator of embryo implantation. Endocrinology 152:4948-4956.   DOI   ScienceOn
76 Hardy K, Spanos S (2002): Growth factor expression and function in the human and mouse preimplantation embryo. J Endocrinol 172:221-236.   DOI   ScienceOn
77 Hartt LS, Carling SJ, Joyce MM, Johnson GA, Vanderwall DK, Ott TL (2005): Temporal and spatial associations of oestrogen receptor alpha and progesterone receptor in the endometrium of cyclic and early pregnant mares. Reproduction 130:241-250.   DOI   ScienceOn
78 Henic E, Sixt M, Hansson S, Hoyer-Hansen G, Casslen B (2006): EGF-stimulated migration in ovarian cancer cells is associated with decreased internalization, increased surface expression, and increased shedding of the urokinase plasminogen activator receptor. Gynecol Oncol 101:28-39.   DOI   ScienceOn
79 Hynes RO (1992): Integrins: versatility, modulation, and signaling in cell adhesion. Cell 69:11-25.   DOI   ScienceOn
80 Jaeger LA, Johnson GA, Ka H, Garlow JG, Burghardt RC, Spencer TE, Bazer FW (2001): Functional analysis of autocrine and paracrine signalling at the uterine-conceptus interface in pigs. Reprod Suppl 58:191-207.
81 Geisert RD, Zavy MT, Moffatt RJ, Blair RM, Yellin T (1990): Embryonic steroids and the establishment of pregnancy in pigs. J Reprod Fertil Suppl 40: 293-305.
82 Gleeson LM, Chakraborty C, McKinnon T, Lala PK (2001): Insulin-like growth factor-binding protein 1 stimulates human trophoblast migration by signaling through alpha 5 beta 1 integrin via mitogen- activated protein kinase pathway. J Clin Endocrinol Metab 86:2484-293.
83 Gray CA, Burghardt RC, Johnson GA, Bazer FW, Spencer TE (2002): Evidence that absence of endometrial gland secretions in uterine gland knockout ewes compromises conceptus survival and elongation. Reproduction 124:289-300.   DOI   ScienceOn
84 Gray CA, Taylor KM, Ramsey WS, Hill JR, Bazer FW, Bartol FF, Spencer TE (2001): Endometrial glands are required for preimplantation conceptus elongation and survival. Biol Reprod 64:1608-1613.   DOI   ScienceOn
85 Greb RR, Heikinheimo O, Williams RF, Hodgen GD, Goodman AL (1997): Vascular endothelial growth factor in primate endometrium is regulated by oestrogen-receptor and progesterone-receptor ligands in vivo. Hum Reprod 12:1280-1292.   DOI   ScienceOn
86 Green ML, Blaeser LL, Simmen FA, Simmen RC (1996): Molecular cloning of spermidine/spermine N1-acetyltransferase from the periimplantation porcine uterus by messenger ribonucleic acid differential display: temporal and conceptus-modulated gene expression. Endocrinology 137:5447-5455.   DOI
87 Green ML, Simmen RC, Simmen FA (1995): Developmental regulation of steroidogenic enzyme gene expression in the periimplantation porcine conceptus: a paracrine role for insulin-like growth factor-I. Endocrinology 136:3961-3970.   DOI
88 Guan Z, Buckman SY, Miller BW, Springer LD, Morrison AR (1998): Interleukin-1beta-induced cyclooxygenase- 2 expression requires activation of both c-Jun NH2-terminal kinase and p38 MAPK signal pathways in rat renal mesangial cells. J Biol Chem 273:28670-28676.   DOI
89 Garlow JE, Ka H, Johnson GA, Burghardt RC, Jaeger LA, Bazer FW (2002): Analysis of osteopontin at the maternal-placental interface in pigs. Biol Reprod 66:718-725.   DOI   ScienceOn
90 Frank M, Bazer FW, Thatcher WW, Wilcox CJ (1977): A study of prostaglandin $F_2$ alpha as the luteolysin in swine: III effects of estradiol valerate on prostaglandin F, progestins, estrone and estradiol concentrations in the utero-ovarian vein of nonpregnant gilts. Prostaglandins 14:1183-1196.   DOI
91 Gasson JC (1991): Molecular physiology of granulocyte- macrophage colony-stimulating factor. Blood 77:1131-1145.
92 Geisert RD, Brookbank JW, Roberts RM, Bazer FW (1982a): Establishment of pregnancy in the pig: II. Cellular remodeling of the porcine blastocyst during elongation on day 12 of pregnancy. Biol Reprod 27:941-955.   DOI   ScienceOn
93 Geisert RD, Chamberlain CS, Vonnahme KA, Malayer JR, Spicer LJ (2001): Possible role of kallikrein in proteolysis of insulin-like growth factor binding proteins during the oestrous cycle and early pregnancy in pigs. Reproduction 121:719-728.   DOI
94 Geisert RD, Pratt TN, Bazer FW, Mayes JS, Watson GH (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   ScienceOn
95 Geisert RD, Renegar RH, Thatcher WW, Roberts RM, Bazer FW (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.   DOI   ScienceOn
96 Geisert RD, Thatcher WW, Roberts RM, Bazer FW (1982c): Establishment of pregnancy in the pig: III. Endometrial secretory response to estradiol valerate administered on day 11 of the estrous cycle. Biol Reprod 27:957-965.   DOI   ScienceOn
97 Geisert RD, Yelich JV (1997): Regulation of conceptus development and attachment in pigs. J Reprod Fertil Suppl 52:133-149.
98 Das SK, Chakraborty I, Wang J, Dey SK, Hoffman LH (1997): Expression of vascular endothelial growth factor (VEGF) and VEGF-receptor messenger ribonucleic acids in the peri-implantation rabbit uterus. Biol Reprod 56:1390-1399.   DOI   ScienceOn
99 Dziuk PJ (1968): Effect of number of embryos and uterine space on embryo survival in the pig. J Anim Sci 27:673-676.   DOI
100 Diaz-Cueto L, Gerton GL (2001): The influence of growth factors on the development of preimplantation mammalian embryos. Arch Med Res 32:619-626.   DOI   ScienceOn
101 Einspanier R, Schonfelder M, Muller K, Stojkovic M, Kosmann M, Wolf E, Schams D (2002): Expression of the vascular endothelial growth factor and its receptors and effects of VEGF during in vitro maturation of bovine cumulus-oocyte complexes (COC). Mol Reprod Dev 62:29-36.   DOI   ScienceOn
102 Fazleabas AT, Kim JJ, Strakova Z (2004): Implantation: embryonic signals and the modulation of the uterine environment--a review. Placenta 25 Suppl A:S26-S31.   DOI   ScienceOn
103 Ferrara N, Carver-Moore K, Chen H, Dowd M, Lu L, O'Shea KS, Powell-Braxton L, Hillan KJ, Moore MW (1996): Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 380:439-442.   DOI   ScienceOn
104 Ferrara N, Gerber HP, LeCouter J (2003): The biology of VEGF and its receptors. Nat Med 9:669-676.   DOI   ScienceOn
105 Finn CA, Martin L (1974): The control of implantation. J Reprod Fertil 39:195-206.   DOI   ScienceOn
106 Fong GH, Rossant J, Gertsenstein M, Breitman ML (1995): Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium. Nature 376:66-70.   DOI   ScienceOn
107 Ford SP, Christenson LK (1991): Direct effects of oestradiol-17 beta and prostaglandin E-2 in protecting pig corpora lutea from a luteolytic dose of prostaglandin F-2 alpha. J Reprod Fertil 93:203-209.   DOI   ScienceOn
108 Carmeliet P, Ferreira V, Breier G, Pollefeyt S, Kieckens L, Gertsenstein M, Fahrig M, Vandenhoeck A, Harpal K, Eberhardt C, Declercq C, Pawling J, Moons L, Collen D, Risau W, Nagy A (1996): Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 380: 435-439.   DOI   ScienceOn
109 Cencic A, Guillomot M, Koren S, La Bonnardiere C (2003): Trophoblastic interferons: do they modulate uterine cellular markers at the time of conceptus attachment in the pig? Placenta 24:862-869.   DOI   ScienceOn
110 Cartwright JE, Tse WK, Whitley GS (2002): Hepatocyte growth factor induced human trophoblast motility involves phosphatidylinositol-3-kinase, mitogen- activated protein kinase, and inducible nitric oxide synthase. Exp Cell Res 279:219-226.   DOI   ScienceOn
111 Charnock-Jones DS, Sharkey AM, Rajput-Williams J, Burch D, Schofield JP, Fountain SA, Boocock CA, Smith SK (1993): Identification and localization of alternately spliced mRNAs for vascular endothelial growth factor in human uterus and estrogen regulation in endometrial carcinoma cell lines. Biol Reprod 48:1120-1128.   DOI   ScienceOn
112 Choi I, Simmen RC, Simmen FA (1996): Molecular cloning of cytochrome P450 aromatase complementary deoxyribonucleic acid from periimplantation porcine and equine blastocysts identifies multiple novel 5'- untranslated exons expressed in embryos, endometrium, and placenta. Endocrinology 137:1457-1467.   DOI
113 Cullinan-Bove K, Koos RD (1993): Vascular endothelial growth factor/vascular permeability factor expression in the rat uterus: rapid stimulation by estrogen correlates with estrogen-induced increases in uterine capillary permeability and growth. Endocrinology 133:829-837.   DOI
114 Dantzer V (1985): Electron microscopy of the initial stages of placentation in the pig. Anat Embryol (Berl) 172:281-293.   DOI
115 Bazer FW, Kim J, Song G, Ka H, Tekwe CD, Wu G (2012): Select nutrients, progesterone, and interferon tau affect conceptus metabolism and development. Ann N Y Acad Sci 1271:88-96.   DOI   ScienceOn
116 Bazer FW, Spencer TE, Johnson GA, Burghardt RC, Wu G (2009): Comparative aspects of implantation. Reproduction 138:195-209.   DOI   ScienceOn
117 Bazer FW, Vallet JL, Roberts RM, Sharp DC, Thatcher WW (1986): Role of conceptus secretory products in establishment of pregnancy. J Reprod Fertil 76:841-850.   DOI   ScienceOn
118 Burghardt RC, Bowen JA, Newton GR, Bazer FW (1997): Extracellular matrix and the implantation cascade in pigs. J Reprod Fertil Suppl 52:151-164.
119 Biadasiewicz K, Sonderegger S, Haslinger P, Haider S, Saleh L, Fiala C, Pollheimer J, Knofler M (2011): Transcription factor AP-2alpha promotes EGF-dependent invasion of human trophoblast. Endocrinology 152:1458-1469.   DOI   ScienceOn
120 Biswas D, Jung EM, Jeung EB, Hyun SH (2011): Effects of vascular endothelial growth factor on porcine preimplantation embryos produced by in vitro fertilization and somatic cell nuclear transfer. Theriogenology 75:256-267.   DOI   ScienceOn
121 Burton GJ, Jauniaux E, Charnock-Jones DS (2007): Human early placental development: potential roles of the endometrial glands. Placenta 28 Suppl A:S64-S69.   DOI   ScienceOn
122 Bass KE, Morrish D, Roth I, Bhardwaj D, Taylor R, Zhou Y, Fisher SJ (1994): Human cytotrophoblast invasion is up-regulated by epidermal growth factor: evidence that paracrine factors modify this process. Dev Biol 164:550-561.   DOI   ScienceOn
123 Bazer FW (1975): Uterine protein secretions: Relationship to development of the conceptus. J Anim Sci 41:1376-1382.   DOI
124 Allison Gray C, Bartol FF, Taylor KM, Wiley AA, Ramsey WS, Ott TL, Bazer FW, Spencer TE (2000): Ovine uterine gland knock-out model: effects of gland ablation on the estrous cycle. Biol Reprod 62: 448-456.   DOI   ScienceOn
125 Anegon I, Cuturi MC, Godard A, Moreau M, Terqui M, Martinat-Botte F, Soulillou JP (1994): Presence of leukaemia inhibitory factor and interleukin 6 in porcine uterine secretions prior to conceptus attachment. Cytokine 6:493-499.   DOI   ScienceOn
126 Aplin JD, Kimber SJ (2004): Trophoblast-uterine interactions at implantation. Reprod Biol Endocrinol 2:48.   DOI   ScienceOn
127 Barber KJ, Franklyn JA, McCabe CJ, Khanim FL, Bulmer JN, Whitley GS, Kilby MD (2005): The in vitro effects of triiodothyronine on epidermal growth factor-induced trophoblast function. J Clin Endocrinol Metab 90:1655-1661.   DOI
128 Yelich JV, Pomp D, Geisert RD (1997b): Ontogeny of elongation and gene expression in the early developing porcine conceptus. Biol Reprod 57:1256-1265.   DOI   ScienceOn
129 Winther H, Ahmed A, Dantzer V (1999): Immunohistochemical localization of vascular endothelial growth factor (VEGF) and its two specific receptors, Flt-1 and KDR, in the porcine placenta and non-pregnant uterus. Placenta 20:35-43.
130 Robertson SA, Mayrhofer G, Seamark RF (1996): Ovarian steroid hormones regulate granulocyte-macrophage colony-stimulating factor synthesis by uterine epithelial cells in the mouse. Biol Reprod 54:183-196.   DOI   ScienceOn
131 Telford NA, Watson AJ, Schultz GA (1990): Transition from maternal to embryonic control in early mammalian development: a comparison of several species. Mol Reprod Dev 26:90-100.   DOI   ScienceOn
132 Sjoblom C, Wikland M, Robertson SA (1999): Granulocyte- macrophage colony-stimulating factor promotes human blastocyst development in vitro. Hum Reprod 14:3069-3076.   DOI   ScienceOn
133 Li RH, Zhuang LZ (1997): The effects of growth factors on human normal placental cytotrophoblast cell proliferation. Hum Reprod 12:830-834.   DOI   ScienceOn
134 Cohen M, Bischof P (2007): Factors regulating trophoblast invasion. Gynecol Obstet Invest 64:126-30.   DOI   ScienceOn