Endocrine and paracrine interaction of growth factors during early pregnancy: A comparative perceptiveness in mammals

Growth factors and embryo implantation

  • Randhir Kumar Department of Zoology, Institute of Science, Banaras Hindu University, Varanasi-221005, India
  • Chandana Haldar Department of Zoology, Institute of Science, Banaras Hindu University, Varanasi-221005, India
  • Pranab Lal Pakrasi Department of Zoology, Institute of Science, Banaras Hindu University, Varanasi-221005, India

Abstract

Infertility is one of the devastating problems worldwide in recent decades which adversely affect the socio-economic status of a person. Loss of early pregnancy due to failure in embryo implantation is considered as one of the major cause of infertility in females and most important limiting factor for achieving a successful outcome using the assisted reproductive techniques (ART). Growth factors are multifunctional signaling molecules secreted by endometrium or blastocyst having a critical role in making uterus receptive for successful progression of early pregnancy. Although various aspects of molecular signaling of growth factors during early pregnancy in different mammals has been studied, a comprehensive understanding of molecular cascade among growth factors and their interaction with other implantation specific molecules is still missing. This review focuses on the role of different growth factors and their regulation during the window of implantation in different mammals. These studies expand our knowledge regarding the molecular signaling of different growth factors in the uterus during the process of early pregnancy. Understanding molecular cascade of growth factors may provide a new insight to improve the outcome of natural pregnancy and enhances the success rate of in vitro fertilization.

 

References

Abrahamsohn PA, Zorn TM (1993) Implantation and decidualization in rodents. J Exp Zool 266:603-28
Aflalo ED, Sod-Moriah UA, Potashnik G, Har-Vardi I (2007) EGF increases expression and activity of PAs in preimplantation rat embryos and their implantation rate. Reprod Biol Endocrinol 5:4
Anteby EY, Greenfield C, Natanson-Yaron S, Goldman-Wohl D, Hamani Y, Khudyak V, Ariel I, Yagel S (2004) Vascular endothelial growth factor, epidermal growth factor and fibroblast growth factor-4 and -10 stimulate trophoblast plasminogen activator system and metalloproteinase-9. Mol Hum Reprod 10:229-235
Battersby S, Critchley HO, Morgan K, Millar RP, Jabbour HN (2004) Expression and regulation of the prokineticins (endocrine gland-derived vascular endothelial growth factor and Bv8) and their receptors in the human endometrium across the menstrual cycle. J Clin Endocrinol Metab 89:2463-2469
Beier HM, Beier-Hellwig K (1998) Molecular and cellular aspects of endometrial receptivity. Hum Reprod Update 4:448-458
Birdsall MA, Hopkisson JF, Grant KE, Barlow DH, Mardon HJ (1996) Expression of heparin-binding epidermal growth factor messenger RNA in the human endometrium. Mol Hum Reprod 2:31-34
Bischof P, Campana A (2000) Molecular mediators of implantation. Baillieres Best Pract Res Clin Obstet Gynaecol 14:801-814
Bonilla AQ, Ozawa M, Hansen PJ (2011) Timing and dependence upon mitogen-activated protein kinase signaling for pro-developmental actions of insulin-like growth factor 1 on the preimplantation bovine embryo. Growth Horm IGF Res 21:107-111
Bourgain C, Devroey P (2003) The endometrium in stimulated cycles for IVF. Hum Reprod Update 9:515-522
Byun HS, Lee GS, Lee BM, Hyun SH, Choi KC, Jeung EB (2008) Implantation-related expression of epidermal growth factor family molecules and their regulation by progesterone in the pregnant rat. Reprod Sci 15:678-689
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
Caron PL, Frechette-Frigon G, Shooner C, Leblanc V, Asselin E (2009) Transforming growth factor beta isoforms regulation of Akt activity and XIAP levels in rat endometrium during estrous cycle, in a model of pseudopregnancy and in cultured decidual cells. Reprod Biol Endocrinol 7:80
Carpenter G (1987) Receptors for epidermal growth factor and other polypeptide mitogens. Annu Rev Biochem 56:881-914
Carson DD, Bagchi I, Dey SK, Enders AC, Fazleabas AT, Lessey BA, Yoshinaga K (2000) Embryo implantation. Dev Biol 223:217-237
Cha J, Sun X, Dey SK (2012) Mechanisms of implantation: strategies for successful pregnancy. Nat Med 18:1754-1767
Chakraborty I, Das SK, Dey SK (1995) Differential expression of vascular endothelial growth factor and its receptor mRNAs in the mouse uterus around the time of implantation. J Endocrinol 147:339-352
Cheng EH, Liu JY, Lee TH, Huang CC, Chen CI, Huang LS, Lee MS (2016) Requirement of Leukemia Inhibitory Factor or Epidermal Growth Factor for Pre-Implantation Embryogenesis via JAK/STAT3 Signaling Pathways. PLoS One 11:e0153086
Cheon YP, Li Q, Xu X, DeMayo FJ, Bagchi IC, Bagchi MK (2002) A genomic approach to identify novel progesterone receptor regulated pathways in the uterus during implantation. Mol Endocrinol 16: 2853-2871
Chia CM, Winston RM, Handyside AH (1995) EGF, TGF-alpha and EGFR expression in human preimplantation embryos. Development 121:299-307
Chobotova K, Spyropoulou I, Carver J, Manek S, Heath JK, Gullick WJ, Barlow DH, Sargent IL, Mardon HJ (2002) Heparin-binding epidermal growth factor and its receptor ErbB4 mediate implantation of the human blastocyst. Mech Dev 119:137-44
Cittadini E, Palermo R (1991) The endometrium in human assisted reproduction. Ann N Y Acad Sci 622:230-235
Cross JC, Werb Z, Fisher SJ (1994) Implantation and the placenta: key pieces of the development puzzle. Science 266:1508-1518
Das A, Mantena SR, Kannan A, Evans DB, Bagchi MK, Bagchi IC (2009) De novo synthesis of estrogen in pregnant uterus is critical for stromal decidualization and angiogenesis. Proc Natl Acad Sci U S A 106:12542-12547.
Das M, Saikia PJ, Sarma HN (2013) Crude bark extract of Dysoxylum alliarium induces alteration in histological structures and VEGF-C expression in uterus during days 4–7 of gestation in albino rat. Reprod Med Biol 12:85–98.
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
Das SK, Wang XN, Paria BC, Damm D, Abraham JA, Klagsbrun M, Andrews GK, Dey SK (1994) Heparin-binding EGF-like growth factor gene is induced in the mouse uterus temporally by the blastocyst solely at the site of its apposition: a possible ligand for interaction with blastocyst EGF-receptor in implantation. Development 120:1071-1083
De La Fuente R, O'Brien MJ, Eppig JJ (1999) Epidermal growth factor enhances preimplantation developmental competence of maturing mouse oocytes. Hum Reprod 14:3060-3068
Deb K, Reese J, Paria BC (2006) Methodologies to study implantation in mice. Methods Mol Med 121:9-34
Dey SK, Lim H, Das SK, Reese J, Paria BC, Daikoku T, Wang H (2004) Molecular cues to implantation. Endocr Rev 25:341-373
Diao H, Xiao S, Li R, Zhao F, Ye X (2013) Distinct spatiotemporal expression of serine proteases Prss23 and Prss35 in periimplantation mouse uterus and dispensable function of Prss35 in fertility. PLoS One 8:e56757
Douglas NC, Tang H, Gomez R, Pytowski B, Hicklin DJ, Sauer CM, Kitajewski J, Sauer MV, Zimmermann RC (2009) Vascular endothelial growth factor receptor 2 (VEGFR-2) functions to promote uterine decidual angiogenesis during early pregnancy in the mouse. Endocrinology 150: 3845-3854
Fang CX, Nong YQ, Liu FH, Fan L, Chen Y (2017) Heparin-Binding Epidermal Growth Factor-Like Growth Factor Enhances Aquaporin 3 Expression and Function During Mouse Embryo Implantation. Reprod Sci 24:463-470
Fang X, Gao Y, Li Q (2016) SMAD3 Activation: A Converging Point of Dysregulated TGF-Beta Superfamily Signaling and Genetic Aberrations in Granulosa Cell Tumor Development? Biol Reprod 95:105
Ferrara N (2000) Vascular endothelial growth factor and the regulation of angiogenesis. Recent Prog Horm Res 55: 15-35; discussion 35-36
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
Folkman J (1995) Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat Med 1:27-31
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
Fowler DJ, Nicolaides KH, Miell JP (2000) Insulin-like growth factor binding protein-1 (IGFBP-1): a multifunctional role in the human female reproductive tract. Hum Reprod Update 6:495-504
Fritz R, Jain C, Armant DR (2014) Cell signaling in trophoblast-uterine communication. Int J Dev Biol 58:261-271
Garcia EV, Hamdi M, Barrera AD, Sanchez-Calabuig MJ, Gutierrez-Adan A, Rizos D (2017) Bovine embryo-oviduct interaction in vitro reveals an early cross talk mediated by BMP signaling. Reproduction 153:631-643
Gardner HG, Kaye PL (1995) Characterization of glucose transport in preimplantation mouse embryos. Reprod Fertil Dev 7:41-50
Ghosh D, Kumar PG, Sengupta J (1998) Effect of early luteal phase administration of mifepristone (RU486) on leukaemia inhibitory factor, transforming growth factor beta and vascular endothelial growth factor in the implantation stage endometrium of the rhesus monkey. J Endocrinol 157:115-125
Ghosh D, Sharkey AM, Charnock-Jones DS, Dhawan L, Dhara S, Smith SK, Sengupta J (2000) Expression of vascular endothelial growth factor (VEGF) and placental growth factor (PlGF) in conceptus and endometrium during implantation in the rhesus monkey. Mol Hum Reprod 6:935-941
Godkin JD, Dore JJ (1998) Transforming growth factor beta and the endometrium. Rev Reprod 3:1-6
Goldman S, Gonen Y (1998) Monoclonal antibodies against epidermal growth factor prevent outgrowth of mouse embryos in vitro. Hum Reprod 13:2231-2233
Gou J, Jia J, Feng J, Zhao X, Yi T, Cui T, Li Z (2017) Stathmin 1 plays a role in endometrial decidualisation by regulating hypoxia inducible factor-1alpha and vascular endothelial growth factor during embryo implantation. Reprod Fertil Dev 29:1530-1537
Gou J, Jia J, Zhao X, Yi T, Li Z (2015) Identification of stathmin 1 during peri-implantation period in mouse endometrium by a proteomics-based analysis. Biochem Biophys Res Commun 461:211-216
Green CJ, Day ML (2013) Insulin-like growth factor 1 acts as an autocrine factor to improve early embryogenesis in vitro. Int J Dev Biol 57:837-844
Green CJ, Fraser ST, Day ML (2015) Insulin-like growth factor 1 increases apical fibronectin in blastocysts to increase blastocyst attachment to endometrial epithelial cells in vitro. Hum Reprod 30:284-298
Green CJ, Fraser ST, Day ML (2015) Insulin-like growth factor 1 increases apical fibronectin in blastocysts to increase blastocyst attachment to endometrial epithelial cells in vitro. Hum Reprod 30:284-298
Halder JB, Zhao X, Soker S, Paria BC, Klagsbrun M, Das SK, Dey SK (2000) Differential expression of VEGF isoforms and VEGF (164)-specific receptor neuropilin-1 in the mouse uterus suggests a role for VEGF (164) in vascular permeability and angiogenesis during implantation. Genesis 26:213-224
Hamilton GS, Lysiak JJ, Han VK, Lala PK (1998) Autocrine-paracrine regulation of human trophoblast invasiveness by insulin-like growth factor (IGF)-II and IGF-binding protein (IGFBP)-1. Exp Cell Res 244:147-156
Harvey MB, Leco KJ, Arcellana-Panlilio MY, Zhang X, Edwards DR, Schultz GA (1995) Proteinase expression in early mouse embryos is regulated by leukaemia inhibitory factor and epidermal growth factor. Development 121:1005-1014
Herbert SP, Stainier DY (2011) Molecular control of endothelial cell behaviour during blood vessel morphogenesis. Nat Rev Mol Cell Biol 12:551-564
Hess AP, Hirchenhain J, Schanz A, Talbi S, Hamilton AE, Giudice LC, Krussel JS (2006) Angiopoietin-1 and -2 mRNA and protein expression in mouse preimplantation embryos and uteri suggests a role in angiogenesis during implantation. Reprod Fertil Dev 18:509-516
Hewitt SC, Li Y, Li L, Korach KS (2010) Estrogen-mediated regulation of Igf1 transcription and uterine growth involves direct binding of estrogen receptor alpha to estrogen-responsive elements. J Biol Chem 285:2676-2685
Houck KA, Ferrara N, Winer J, Cachianes G, Li B, Leung DW (1991) The vascular endothelial growth factor family: identification of a fourth molecular species and characterization of alternative splicing of RNA. Mol Endocrinol 5:1806-1814
Irving JA, Lala PK (1995) Functional role of cell surface integrins on human trophoblast cell migration: regulation by TGF-beta, IGF-II, and IGFBP-1. Exp Cell Res 217:419-427
Jakeman LB, Armanini M, Phillips HS, Ferrara N (1993) Developmental expression of binding sites and messenger ribonucleic acid for vascular endothelial growth factor suggests a role for this protein in vasculogenesis and angiogenesis. Endocrinology 133:848-859
Jiang Y, Sun L, Xuan X, Wang J (2016) Impacts of N-Butylphthalide on expression of growth factors in rats with focal cerebral ischemia. Bosn J Basic Med Sci 16: 102-107
Johnson DC, Chatterjee S (1993) Epidermal growth factor (EGF) replaces estradiol for the initiation of embryo implantation in the hypophysectomized rat. Placenta 14:429-438
Jones RL, Stoikos C, Findlay JK, Salamonsen LA (2006) TGF-beta superfamily expression and actions in the endometrium and placenta. Reproduction 132:217-232
Kamei Y, Tsutsumi O, Kuwabara Y, Taketani Y (1993) Intrauterine growth retardation and fetal losses are caused by epidermal growth factor deficiency in mice. Am J Physiol 264:597-600
Kaneko Y, Murphy CR, Day ML (2013) Extracellular matrix proteins secreted from both the endometrium and the embryo are required for attachment: a study using a co-culture model of rat blastocysts and Ishikawa cells. J Morphol 274:63-72
Kapur S, Tamada H, Dey SK, Andrews GK (1992) Expression of insulin-like growth factor-I (IGF-I) and its receptor in the peri-implantation mouse uterus, and cell-specific regulation of IGF-I gene expression by estradiol and progesterone. Biol Reprod 46:208-219
Khamsi F, Armstrong DT, Zhang X (1996) Expression of urokinase-type plasminogen activator in human preimplantation embryos. Mol Hum Reprod 2:273-276
Krussel J, Behr B, Hirchenhain J, Wen Y, Milki AA, Cupisti S, Bielfeld P, Polan ML (2000) Expression of vascular endothelial growth factor mRNA in human preimplantation embryos derived from tripronuclear zygotes. Fertil Steril 74:1220-1226
Krussel JS, Behr B, Milki AA, Hirchenhain J, Wen Y, Bielfeld P, Lake Polan M (2001) Vascular endothelial growth factor (VEGF) mRNA splice variants are differentially expressed in human blastocysts. Mol Hum Reprod 7:57-63
Krussel JS, Bielfeld P, Polan ML, Simon C (2003) Regulation of embryonic implantation. Eur J Obstet Gynecol Reprod Biol 110 Suppl 1:2-9
Larsen EC, Christiansen OB, Kolte AM, Macklon N (2013) New insights into mechanisms behind miscarriage. BMC Med 11:154
Leach RE, Khalifa R, Ramirez ND, Das SK, Wang J, Dey SK, Romero R, Armant DR (1999) Multiple roles for heparin-binding epidermal growth factor-like growth factor are suggested by its cell-specific expression during the human endometrial cycle and early placentation. J Clin Endocrinol Metab 84:3355-3363
Li G, Khateeb K, Schaeffer E, Zhang B, Khatib H (2012) Genes of the transforming growth factor-beta signalling pathway are associated with pre-implantation embryonic development in cattle. J Dairy Res 79: 310-317
Licht P, Fluhr H, Neuwinger J, Wallwiener D, Wildt L (2007) Is human chorionic gonadotropin directly involved in the regulation of human implantation? Mol Cell Endocrinol 269:85-92
Lighten AD, Moore GE, Winston RM, Hardy K (1998) Routine addition of human insulin-like growth factor-I ligand could benefit clinical in-vitro fertilization culture. Hum Reprod 13:3144-3150
Lim H, Das SK, Dey SK (1998) erbB genes in the mouse uterus: cell-specific signaling by epidermal growth factor (EGF) family of growth factors during implantation. Dev Biol 204:97-110
Lim HJ, Dey SK (2009) HB-EGF: a unique mediator of embryo-uterine interactions during implantation. Exp Cell Res 315:619-626
Liu J, Gao F, Liu YF, Dou HT, Yan JQ, Fan ZM, Yang ZM (2017) HB-EGF regulates Prss56 expression during mouse decidualization via EGFR/ERK/EGR2 signaling pathway. J Endocrinol 234:247-254
Ma W, Tan J, Matsumoto H, Robert B, Abrahamson DR, Das SK, Dey SK (2001) Adult tissue angiogenesis: evidence for negative regulation by estrogen in the uterus. Mol Endocrinol 15:1983-1992
Makker A, Singh MM (2006) Endometrial receptivity: clinical assessment in relation to fertility, infertility, and antifertility. Med Res Rev 26:699-746
Martin KL, Barlow DH, Sargent IL (1998) Heparin-binding epidermal growth factor significantly improves human blastocyst development and hatching in serum-free medium. Hum Reprod 13:1645-1652
Martin-Estal I, de la Garza RG, Castilla-Cortazar I (2016) Erratum to: Intrauterine Growth Retardation (IUGR) as a Novel Condition of Insulin-Like Growth Factor-1 (IGF-1) Deficiency. Rev Physiol Biochem Pharmacol 170:129
Matsumoto H, Fukui E, Yoshizawa M (2015) Angiogenesis and hormonal regulation on uterine receptivity for blastocyst implantation. J Mamm Ova Res, 32:79–85.
Matzuk MM, Li Q (2013) How the oocyte influences follicular cell function and why. In: Coticchio G, Albertini DF, De Santis L, editors. Oogenesis. London: Springer London, p. 75–92.
Mueller MD, Vigne JL, Minchenko A, Lebovic DI, Leitman DC, Taylor RN (2000) Regulation of vascular endothelial growth factor (VEGF) gene transcription by estrogen receptors alpha and beta. Proc Natl Acad Sci U S A 97:10972-10977
Ni N, Li Q (2017) TGFbeta superfamily signaling and uterine decidualization. Reprod Biol Endocrinol 15:84
Nong YQ, Liu FH, Chen Y, Wang F (2013) The expression and distribution of aquaporin 3 in mouse embryos before and after vitrification. J Assist Reprod Genet 30:601-6
Perrot-Applanat M, Ancelin M, Buteau-Lozano H, Meduri G, Bausero P (2000) Ovarian steroids in endometrial angiogenesis. Steroids 65:599-603
Poltorak Z, Cohen T, Sivan R, Kandelis Y, Spira G, Vlodavsky I, Keshet E, Neufeld G (1997) VEGF145, a secreted vascular endothelial growth factor isoform that binds to extracellular matrix. J Biol Chem 272:7151-7158
Rabbani ML, Rogers PA (2001) Role of vascular endothelial growth factor in endometrial vascular events before implantation in rats. Reproduction 122:85-90
Rappolee DA, Sturm KS, Behrendtsen O, Schultz GA, Pedersen RA, Werb Z (1992) Insulin-like growth factor II acts through an endogenous growth pathway regulated by imprinting in early mouse embryos. Genes Dev 6:939-952
Rechler MM, Nissley SP (1985) The nature and regulation of the receptors for insulin-like growth factors. Annu Rev Physiol 47:425-442
Reyes de Mochel NS, Luong M, Chiang M, Javier AL, Luu E, Toshihiko F, MacGregor GR, Cinquin O, Cho KW (2015) BMP signaling is required for cell cleavage in preimplantation-mouse embryos. Dev Biol 397:45-55
Riese DJ, 2nd, Stern DF (1998) Specificity within the EGF family/ErbB receptor family signaling network. Bioessays 20:41-48
Rockwell LC, Pillai S, Olson CE, Koos RD (2002) Inhibition of vascular endothelial growth factor/vascular permeability factor action blocks estrogen-induced uterine edema and implantation in rodents. Biol Reprod 67:1804-1810
Saikia PJ, Das D, Mize D, Das M, Sarma HN (2017) Spatiotemporal expression of Vascular Endothelial Growth Factor-C in mice fetal-maternal tissues during periimplantation (D4–D7). Middle East Fertility Society Journal 22:115-124
Salleh N, Giribabu N (2014) Leukemia inhibitory factor: roles in embryo implantation and in nonhormonal contraception. Scientific World Journal 2014:201514
Scott RT, Jr., Hofmann GE, Veeck LL, Jones HW, Jr., Muasher SJ (1991) Embryo quality and pregnancy rates in patients attempting pregnancy through in vitro fertilization. Fertil Steril 55:426-428
Sengupta J, Lalitkumar PG, Najwa AR, Charnock-Jones DS, Evans AL, Sharkey AM, Smith SK, Ghosh D (2007) Immunoneutralization of vascular endothelial growth factor inhibits pregnancy establishment in the rhesus monkey (Macaca mulatta). Reproduction 133:1199-1211
Seshagiri PB, Mishra A, Ramesh G, Rao RP (2002) Regulation of peri-attachment embryo development in the golden hamster: role of growth factors. J Reprod Immunol 53:203-213
Shibuya M (1995) Role of VEGF-flt receptor system in normal and tumor angiogenesis. Adv Cancer Res 67:281-316
Shifren JL, Tseng JF, Zaloudek CJ, Ryan IP, Meng YG, Ferrara N, Jaffe RB, Taylor RN (1996) Ovarian steroid regulation of vascular endothelial growth factor in the human endometrium: implications for angiogenesis during the menstrual cycle and in the pathogenesis of endometriosis. J Clin Endocrinol Metab 81:3112-3118
Shooner C, Caron PL, Frechette-Frigon G, Leblanc V, Dery MC, Asselin E (2005) TGF-beta expression during rat pregnancy and activity on decidual cell survival. Reprod Biol Endocrinol 3:20
Simon A, Laufer N (2012) Repeated implantation failure: clinical approach. Fertil Steril 97:1039-1043
Simon C, Martin JC, Pellicer A (2000) Paracrine regulators of implantation. Baillieres Best Pract Res Clin Obstet Gynaecol 14:815-826
Smith SK (1994) Growth factors in the human endometrium. Hum Reprod 9:936-946
Staun-Ram E, Goldman S, Gabarin D, Shalev E (2004) Expression and importance of matrix metalloproteinase 2 and 9 (MMP-2 and -9) in human trophoblast invasion. Reprod Biol Endocrinol 2:59
Sugino N, Kashida S, Karube-Harada A, Takiguchi S, Kato H (2002) Expression of vascular endothelial growth factor (VEGF) and its receptors in human endometrium throughout the menstrual cycle and in early pregnancy. Reproduction 123:379-387
Sun X, Bartos A, Whitsett JA, Dey SK (2013) Uterine deletion of Gp130 or Stat3 shows implantation failure with increased estrogenic responses. Mol Endocrinol 27: 1492-501
Threadgill DW, Dlugosz AA, Hansen LA, Tennenbaum T, Lichti U, Yee D, LaMantia C, Mourton T, Herrup K, Harris RC, et al. (1995) Targeted disruption of mouse EGF receptor: effect of genetic background on mutant phenotype. Science 269:230-234
Toth B, Wurfel W, Germeyer A, Hirv K, Makrigiannakis A, Strowitzki T (2011) Disorders of implantation--are there diagnostic and therapeutic options? J Reprod Immunol 90: 117-23
Tsutsumi O, Oka T (1987) Epidermal growth factor deficiency during pregnancy causes abortion in mice. Am J Obstet Gynecol 156:241-244
Wang X, Wang H, Matsumoto H, Roy SK, Das SK, Paria BC (2002) Dual source and target of heparin-binding EGF-like growth factor during the onset of implantation in the hamster. Development 129:4125-4134
Wang XN, Das SK, Damm D, Klagsbrun M, Abraham JA, Dey SK (1994) Differential regulation of heparin-binding epidermal growth factor-like growth factor in the adult ovariectomized mouse uterus by progesterone and estrogen. Endocrinology 135: 1264-1271
Watson ED, Cross JC (2005) Development of structures and transport functions in the mouse placenta. Physiology (Bethesda); 20:180-193
Wooding P, Burton G (2008) Implantation, Maternofetal Exchange and Vascular Relationships. In: Comparative Placentation: Structures, Functions and Evolution. Berlin: Springer; 47-82
Xie H, Wang H, Tranguch S, Iwamoto R, Mekada E, Demayo FJ, Lydon JP, Das SK, Dey SK (2007) Maternal heparin-binding-EGF deficiency limits pregnancy success in mice. Proc Natl Acad Sci U S A 104:18315-18320
Yancopoulos GD, Davis S, Gale NW, Rudge JS, Wiegand SJ, Holash J (2000) Vascular-specific growth factors and blood vessel formation. Nature 407:242-248
Yarden Y (2001) The EGFR family and its ligands in human cancer. signalling mechanisms and therapeutic opportunities. Eur J Cancer 37 Suppl 4:S3-8
Yi XJ, Jiang HY, Lee KK, O WS, Tang PL, Chow PH (1999) Expression of vascular endothelial growth factor (VEGF) and its receptors during embryonic implantation in the golden hamster (Mesocricetus auratus). Cell Tissue Res 296:339-349
Yoo HJ, Barlow DH, Mardon HJ (1997) Temporal and spatial regulation of expression of heparin-binding epidermal growth factor-like growth factor in the human endometrium: a possible role in blastocyst implantation. Dev Genet 21:102-108
Yoshinaga K (1988) Uterine receptivity for blastocyst implantation. Ann N Y Acad Sci 541:424-431
Yoshinaga K (2014) Progesterone and its downstream molecules as blastocyst implantation essential factors. Am J Reprod Immunol 72:117-128
Young SL, Lessey BA, Fritz MA, Meyer WR, Murray MJ, Speckman PL, Nowicki BJ (2002) In vivo and in vitro evidence suggest that HB-EGF regulates endometrial expression of human decay-accelerating factor. J Clin Endocrinol Metab 87:1368-1375
Zhang J, Wang L, Cai QL (2001) The expression and function of VEGF at embryo implantation ‘window’ in the mouse. Chinese Sci, Bull, 46:409–411.
Zygmunt M, Herr F, Munstedt K, Lang U, Liang OD (2003) Angiogenesis and vasculogenesis in pregnancy. Eur J Obstet Gynecol Reprod Biol 110 Suppl 1:S10-18











Abrahamsohn PA, Zorn TM (1993) Implantation and decidualization in rodents. J Exp Zool 266:603-28
Aflalo ED, Sod-Moriah UA, Potashnik G, Har-Vardi I (2007) EGF increases expression and activity of PAs in preimplantation rat embryos and their implantation rate. Reprod Biol Endocrinol 5:4
Anteby EY, Greenfield C, Natanson-Yaron S, Goldman-Wohl D, Hamani Y, Khudyak V, Ariel I, Yagel S (2004) Vascular endothelial growth factor, epidermal growth factor and fibroblast growth factor-4 and -10 stimulate trophoblast plasminogen activator system and metalloproteinase-9. Mol Hum Reprod 10:229-235
Battersby S, Critchley HO, Morgan K, Millar RP, Jabbour HN (2004) Expression and regulation of the prokineticins (endocrine gland-derived vascular endothelial growth factor and Bv8) and their receptors in the human endometrium across the menstrual cycle. J Clin Endocrinol Metab 89:2463-2469
Beier HM, Beier-Hellwig K (1998) Molecular and cellular aspects of endometrial receptivity. Hum Reprod Update 4:448-458
Birdsall MA, Hopkisson JF, Grant KE, Barlow DH, Mardon HJ (1996) Expression of heparin-binding epidermal growth factor messenger RNA in the human endometrium. Mol Hum Reprod 2:31-34
Bischof P, Campana A (2000) Molecular mediators of implantation. Baillieres Best Pract Res Clin Obstet Gynaecol 14:801-814
Bonilla AQ, Ozawa M, Hansen PJ (2011) Timing and dependence upon mitogen-activated protein kinase signaling for pro-developmental actions of insulin-like growth factor 1 on the preimplantation bovine embryo. Growth Horm IGF Res 21:107-111
Bourgain C, Devroey P (2003) The endometrium in stimulated cycles for IVF. Hum Reprod Update 9:515-522
Byun HS, Lee GS, Lee BM, Hyun SH, Choi KC, Jeung EB (2008) Implantation-related expression of epidermal growth factor family molecules and their regulation by progesterone in the pregnant rat. Reprod Sci 15:678-689
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
Caron PL, Frechette-Frigon G, Shooner C, Leblanc V, Asselin E (2009) Transforming growth factor beta isoforms regulation of Akt activity and XIAP levels in rat endometrium during estrous cycle, in a model of pseudopregnancy and in cultured decidual cells. Reprod Biol Endocrinol 7:80
Carpenter G (1987) Receptors for epidermal growth factor and other polypeptide mitogens. Annu Rev Biochem 56:881-914
Carson DD, Bagchi I, Dey SK, Enders AC, Fazleabas AT, Lessey BA, Yoshinaga K (2000) Embryo implantation. Dev Biol 223:217-237
Cha J, Sun X, Dey SK (2012) Mechanisms of implantation: strategies for successful pregnancy. Nat Med 18:1754-1767
Chakraborty I, Das SK, Dey SK (1995) Differential expression of vascular endothelial growth factor and its receptor mRNAs in the mouse uterus around the time of implantation. J Endocrinol 147:339-352
Cheng EH, Liu JY, Lee TH, Huang CC, Chen CI, Huang LS, Lee MS (2016) Requirement of Leukemia Inhibitory Factor or Epidermal Growth Factor for Pre-Implantation Embryogenesis via JAK/STAT3 Signaling Pathways. PLoS One 11:e0153086
Cheon YP, Li Q, Xu X, DeMayo FJ, Bagchi IC, Bagchi MK (2002) A genomic approach to identify novel progesterone receptor regulated pathways in the uterus during implantation. Mol Endocrinol 16: 2853-2871
Chia CM, Winston RM, Handyside AH (1995) EGF, TGF-alpha and EGFR expression in human preimplantation embryos. Development 121:299-307
Chobotova K, Spyropoulou I, Carver J, Manek S, Heath JK, Gullick WJ, Barlow DH, Sargent IL, Mardon HJ (2002) Heparin-binding epidermal growth factor and its receptor ErbB4 mediate implantation of the human blastocyst. Mech Dev 119:137-44
Cittadini E, Palermo R (1991) The endometrium in human assisted reproduction. Ann N Y Acad Sci 622:230-235
Cross JC, Werb Z, Fisher SJ (1994) Implantation and the placenta: key pieces of the development puzzle. Science 266:1508-1518
Das A, Mantena SR, Kannan A, Evans DB, Bagchi MK, Bagchi IC (2009) De novo synthesis of estrogen in pregnant uterus is critical for stromal decidualization and angiogenesis. Proc Natl Acad Sci U S A 106:12542-12547.
Das M, Saikia PJ, Sarma HN (2013) Crude bark extract of Dysoxylum alliarium induces alteration in histological structures and VEGF-C expression in uterus during days 4–7 of gestation in albino rat. Reprod Med Biol 12:85–98.
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
Das SK, Wang XN, Paria BC, Damm D, Abraham JA, Klagsbrun M, Andrews GK, Dey SK (1994) Heparin-binding EGF-like growth factor gene is induced in the mouse uterus temporally by the blastocyst solely at the site of its apposition: a possible ligand for interaction with blastocyst EGF-receptor in implantation. Development 120:1071-1083
De La Fuente R, O'Brien MJ, Eppig JJ (1999) Epidermal growth factor enhances preimplantation developmental competence of maturing mouse oocytes. Hum Reprod 14:3060-3068
Deb K, Reese J, Paria BC (2006) Methodologies to study implantation in mice. Methods Mol Med 121:9-34
Dey SK, Lim H, Das SK, Reese J, Paria BC, Daikoku T, Wang H (2004) Molecular cues to implantation. Endocr Rev 25:341-373
Diao H, Xiao S, Li R, Zhao F, Ye X (2013) Distinct spatiotemporal expression of serine proteases Prss23 and Prss35 in periimplantation mouse uterus and dispensable function of Prss35 in fertility. PLoS One 8:e56757
Douglas NC, Tang H, Gomez R, Pytowski B, Hicklin DJ, Sauer CM, Kitajewski J, Sauer MV, Zimmermann RC (2009) Vascular endothelial growth factor receptor 2 (VEGFR-2) functions to promote uterine decidual angiogenesis during early pregnancy in the mouse. Endocrinology 150: 3845-3854
Fang CX, Nong YQ, Liu FH, Fan L, Chen Y (2017) Heparin-Binding Epidermal Growth Factor-Like Growth Factor Enhances Aquaporin 3 Expression and Function During Mouse Embryo Implantation. Reprod Sci 24:463-470
Fang X, Gao Y, Li Q (2016) SMAD3 Activation: A Converging Point of Dysregulated TGF-Beta Superfamily Signaling and Genetic Aberrations in Granulosa Cell Tumor Development? Biol Reprod 95:105
Ferrara N (2000) Vascular endothelial growth factor and the regulation of angiogenesis. Recent Prog Horm Res 55: 15-35; discussion 35-36
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
Folkman J (1995) Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat Med 1:27-31
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
Fowler DJ, Nicolaides KH, Miell JP (2000) Insulin-like growth factor binding protein-1 (IGFBP-1): a multifunctional role in the human female reproductive tract. Hum Reprod Update 6:495-504
Fritz R, Jain C, Armant DR (2014) Cell signaling in trophoblast-uterine communication. Int J Dev Biol 58:261-271
Garcia EV, Hamdi M, Barrera AD, Sanchez-Calabuig MJ, Gutierrez-Adan A, Rizos D (2017) Bovine embryo-oviduct interaction in vitro reveals an early cross talk mediated by BMP signaling. Reproduction 153:631-643
Gardner HG, Kaye PL (1995) Characterization of glucose transport in preimplantation mouse embryos. Reprod Fertil Dev 7:41-50
Ghosh D, Kumar PG, Sengupta J (1998) Effect of early luteal phase administration of mifepristone (RU486) on leukaemia inhibitory factor, transforming growth factor beta and vascular endothelial growth factor in the implantation stage endometrium of the rhesus monkey. J Endocrinol 157:115-125
Ghosh D, Sharkey AM, Charnock-Jones DS, Dhawan L, Dhara S, Smith SK, Sengupta J (2000) Expression of vascular endothelial growth factor (VEGF) and placental growth factor (PlGF) in conceptus and endometrium during implantation in the rhesus monkey. Mol Hum Reprod 6:935-941
Godkin JD, Dore JJ (1998) Transforming growth factor beta and the endometrium. Rev Reprod 3:1-6
Goldman S, Gonen Y (1998) Monoclonal antibodies against epidermal growth factor prevent outgrowth of mouse embryos in vitro. Hum Reprod 13:2231-2233
Gou J, Jia J, Feng J, Zhao X, Yi T, Cui T, Li Z (2017) Stathmin 1 plays a role in endometrial decidualisation by regulating hypoxia inducible factor-1alpha and vascular endothelial growth factor during embryo implantation. Reprod Fertil Dev 29:1530-1537
Gou J, Jia J, Zhao X, Yi T, Li Z (2015) Identification of stathmin 1 during peri-implantation period in mouse endometrium by a proteomics-based analysis. Biochem Biophys Res Commun 461:211-216
Green CJ, Day ML (2013) Insulin-like growth factor 1 acts as an autocrine factor to improve early embryogenesis in vitro. Int J Dev Biol 57:837-844
Green CJ, Fraser ST, Day ML (2015) Insulin-like growth factor 1 increases apical fibronectin in blastocysts to increase blastocyst attachment to endometrial epithelial cells in vitro. Hum Reprod 30:284-298
Green CJ, Fraser ST, Day ML (2015) Insulin-like growth factor 1 increases apical fibronectin in blastocysts to increase blastocyst attachment to endometrial epithelial cells in vitro. Hum Reprod 30:284-298
Halder JB, Zhao X, Soker S, Paria BC, Klagsbrun M, Das SK, Dey SK (2000) Differential expression of VEGF isoforms and VEGF (164)-specific receptor neuropilin-1 in the mouse uterus suggests a role for VEGF (164) in vascular permeability and angiogenesis during implantation. Genesis 26:213-224
Hamilton GS, Lysiak JJ, Han VK, Lala PK (1998) Autocrine-paracrine regulation of human trophoblast invasiveness by insulin-like growth factor (IGF)-II and IGF-binding protein (IGFBP)-1. Exp Cell Res 244:147-156
Harvey MB, Leco KJ, Arcellana-Panlilio MY, Zhang X, Edwards DR, Schultz GA (1995) Proteinase expression in early mouse embryos is regulated by leukaemia inhibitory factor and epidermal growth factor. Development 121:1005-1014
Herbert SP, Stainier DY (2011) Molecular control of endothelial cell behaviour during blood vessel morphogenesis. Nat Rev Mol Cell Biol 12:551-564
Hess AP, Hirchenhain J, Schanz A, Talbi S, Hamilton AE, Giudice LC, Krussel JS (2006) Angiopoietin-1 and -2 mRNA and protein expression in mouse preimplantation embryos and uteri suggests a role in angiogenesis during implantation. Reprod Fertil Dev 18:509-516
Hewitt SC, Li Y, Li L, Korach KS (2010) Estrogen-mediated regulation of Igf1 transcription and uterine growth involves direct binding of estrogen receptor alpha to estrogen-responsive elements. J Biol Chem 285:2676-2685
Houck KA, Ferrara N, Winer J, Cachianes G, Li B, Leung DW (1991) The vascular endothelial growth factor family: identification of a fourth molecular species and characterization of alternative splicing of RNA. Mol Endocrinol 5:1806-1814
Irving JA, Lala PK (1995) Functional role of cell surface integrins on human trophoblast cell migration: regulation by TGF-beta, IGF-II, and IGFBP-1. Exp Cell Res 217:419-427
Jakeman LB, Armanini M, Phillips HS, Ferrara N (1993) Developmental expression of binding sites and messenger ribonucleic acid for vascular endothelial growth factor suggests a role for this protein in vasculogenesis and angiogenesis. Endocrinology 133:848-859
Jiang Y, Sun L, Xuan X, Wang J (2016) Impacts of N-Butylphthalide on expression of growth factors in rats with focal cerebral ischemia. Bosn J Basic Med Sci 16: 102-107
Johnson DC, Chatterjee S (1993) Epidermal growth factor (EGF) replaces estradiol for the initiation of embryo implantation in the hypophysectomized rat. Placenta 14:429-438
Jones RL, Stoikos C, Findlay JK, Salamonsen LA (2006) TGF-beta superfamily expression and actions in the endometrium and placenta. Reproduction 132:217-232
Kamei Y, Tsutsumi O, Kuwabara Y, Taketani Y (1993) Intrauterine growth retardation and fetal losses are caused by epidermal growth factor deficiency in mice. Am J Physiol 264:597-600
Kaneko Y, Murphy CR, Day ML (2013) Extracellular matrix proteins secreted from both the endometrium and the embryo are required for attachment: a study using a co-culture model of rat blastocysts and Ishikawa cells. J Morphol 274:63-72
Kapur S, Tamada H, Dey SK, Andrews GK (1992) Expression of insulin-like growth factor-I (IGF-I) and its receptor in the peri-implantation mouse uterus, and cell-specific regulation of IGF-I gene expression by estradiol and progesterone. Biol Reprod 46:208-219
Khamsi F, Armstrong DT, Zhang X (1996) Expression of urokinase-type plasminogen activator in human preimplantation embryos. Mol Hum Reprod 2:273-276
Krussel J, Behr B, Hirchenhain J, Wen Y, Milki AA, Cupisti S, Bielfeld P, Polan ML (2000) Expression of vascular endothelial growth factor mRNA in human preimplantation embryos derived from tripronuclear zygotes. Fertil Steril 74:1220-1226
Krussel JS, Behr B, Milki AA, Hirchenhain J, Wen Y, Bielfeld P, Lake Polan M (2001) Vascular endothelial growth factor (VEGF) mRNA splice variants are differentially expressed in human blastocysts. Mol Hum Reprod 7:57-63
Krussel JS, Bielfeld P, Polan ML, Simon C (2003) Regulation of embryonic implantation. Eur J Obstet Gynecol Reprod Biol 110 Suppl 1:2-9
Larsen EC, Christiansen OB, Kolte AM, Macklon N (2013) New insights into mechanisms behind miscarriage. BMC Med 11:154
Leach RE, Khalifa R, Ramirez ND, Das SK, Wang J, Dey SK, Romero R, Armant DR (1999) Multiple roles for heparin-binding epidermal growth factor-like growth factor are suggested by its cell-specific expression during the human endometrial cycle and early placentation. J Clin Endocrinol Metab 84:3355-3363
Li G, Khateeb K, Schaeffer E, Zhang B, Khatib H (2012) Genes of the transforming growth factor-beta signalling pathway are associated with pre-implantation embryonic development in cattle. J Dairy Res 79: 310-317
Licht P, Fluhr H, Neuwinger J, Wallwiener D, Wildt L (2007) Is human chorionic gonadotropin directly involved in the regulation of human implantation? Mol Cell Endocrinol 269:85-92
Lighten AD, Moore GE, Winston RM, Hardy K (1998) Routine addition of human insulin-like growth factor-I ligand could benefit clinical in-vitro fertilization culture. Hum Reprod 13:3144-3150
Lim H, Das SK, Dey SK (1998) erbB genes in the mouse uterus: cell-specific signaling by epidermal growth factor (EGF) family of growth factors during implantation. Dev Biol 204:97-110
Lim HJ, Dey SK (2009) HB-EGF: a unique mediator of embryo-uterine interactions during implantation. Exp Cell Res 315:619-626
Liu J, Gao F, Liu YF, Dou HT, Yan JQ, Fan ZM, Yang ZM (2017) HB-EGF regulates Prss56 expression during mouse decidualization via EGFR/ERK/EGR2 signaling pathway. J Endocrinol 234:247-254
Ma W, Tan J, Matsumoto H, Robert B, Abrahamson DR, Das SK, Dey SK (2001) Adult tissue angiogenesis: evidence for negative regulation by estrogen in the uterus. Mol Endocrinol 15:1983-1992
Makker A, Singh MM (2006) Endometrial receptivity: clinical assessment in relation to fertility, infertility, and antifertility. Med Res Rev 26:699-746
Martin KL, Barlow DH, Sargent IL (1998) Heparin-binding epidermal growth factor significantly improves human blastocyst development and hatching in serum-free medium. Hum Reprod 13:1645-1652
Martin-Estal I, de la Garza RG, Castilla-Cortazar I (2016) Erratum to: Intrauterine Growth Retardation (IUGR) as a Novel Condition of Insulin-Like Growth Factor-1 (IGF-1) Deficiency. Rev Physiol Biochem Pharmacol 170:129
Matsumoto H, Fukui E, Yoshizawa M (2015) Angiogenesis and hormonal regulation on uterine receptivity for blastocyst implantation. J Mamm Ova Res, 32:79–85.
Matzuk MM, Li Q (2013) How the oocyte influences follicular cell function and why. In: Coticchio G, Albertini DF, De Santis L, editors. Oogenesis. London: Springer London, p. 75–92.
Mueller MD, Vigne JL, Minchenko A, Lebovic DI, Leitman DC, Taylor RN (2000) Regulation of vascular endothelial growth factor (VEGF) gene transcription by estrogen receptors alpha and beta. Proc Natl Acad Sci U S A 97:10972-10977
Ni N, Li Q (2017) TGFbeta superfamily signaling and uterine decidualization. Reprod Biol Endocrinol 15:84
Nong YQ, Liu FH, Chen Y, Wang F (2013) The expression and distribution of aquaporin 3 in mouse embryos before and after vitrification. J Assist Reprod Genet 30:601-6
Perrot-Applanat M, Ancelin M, Buteau-Lozano H, Meduri G, Bausero P (2000) Ovarian steroids in endometrial angiogenesis. Steroids 65:599-603
Poltorak Z, Cohen T, Sivan R, Kandelis Y, Spira G, Vlodavsky I, Keshet E, Neufeld G (1997) VEGF145, a secreted vascular endothelial growth factor isoform that binds to extracellular matrix. J Biol Chem 272:7151-7158
Rabbani ML, Rogers PA (2001) Role of vascular endothelial growth factor in endometrial vascular events before implantation in rats. Reproduction 122:85-90
Rappolee DA, Sturm KS, Behrendtsen O, Schultz GA, Pedersen RA, Werb Z (1992) Insulin-like growth factor II acts through an endogenous growth pathway regulated by imprinting in early mouse embryos. Genes Dev 6:939-952
Rechler MM, Nissley SP (1985) The nature and regulation of the receptors for insulin-like growth factors. Annu Rev Physiol 47:425-442
Reyes de Mochel NS, Luong M, Chiang M, Javier AL, Luu E, Toshihiko F, MacGregor GR, Cinquin O, Cho KW (2015) BMP signaling is required for cell cleavage in preimplantation-mouse embryos. Dev Biol 397:45-55
Riese DJ, 2nd, Stern DF (1998) Specificity within the EGF family/ErbB receptor family signaling network. Bioessays 20:41-48
Rockwell LC, Pillai S, Olson CE, Koos RD (2002) Inhibition of vascular endothelial growth factor/vascular permeability factor action blocks estrogen-induced uterine edema and implantation in rodents. Biol Reprod 67:1804-1810
Saikia PJ, Das D, Mize D, Das M, Sarma HN (2017) Spatiotemporal expression of Vascular Endothelial Growth Factor-C in mice fetal-maternal tissues during periimplantation (D4–D7). Middle East Fertility Society Journal 22:115-124
Salleh N, Giribabu N (2014) Leukemia inhibitory factor: roles in embryo implantation and in nonhormonal contraception. Scientific World Journal 2014:201514
Scott RT, Jr., Hofmann GE, Veeck LL, Jones HW, Jr., Muasher SJ (1991) Embryo quality and pregnancy rates in patients attempting pregnancy through in vitro fertilization. Fertil Steril 55:426-428
Sengupta J, Lalitkumar PG, Najwa AR, Charnock-Jones DS, Evans AL, Sharkey AM, Smith SK, Ghosh D (2007) Immunoneutralization of vascular endothelial growth factor inhibits pregnancy establishment in the rhesus monkey (Macaca mulatta). Reproduction 133:1199-1211
Seshagiri PB, Mishra A, Ramesh G, Rao RP (2002) Regulation of peri-attachment embryo development in the golden hamster: role of growth factors. J Reprod Immunol 53:203-213
Shibuya M (1995) Role of VEGF-flt receptor system in normal and tumor angiogenesis. Adv Cancer Res 67:281-316
Shifren JL, Tseng JF, Zaloudek CJ, Ryan IP, Meng YG, Ferrara N, Jaffe RB, Taylor RN (1996) Ovarian steroid regulation of vascular endothelial growth factor in the human endometrium: implications for angiogenesis during the menstrual cycle and in the pathogenesis of endometriosis. J Clin Endocrinol Metab 81:3112-3118
Shooner C, Caron PL, Frechette-Frigon G, Leblanc V, Dery MC, Asselin E (2005) TGF-beta expression during rat pregnancy and activity on decidual cell survival. Reprod Biol Endocrinol 3:20
Simon A, Laufer N (2012) Repeated implantation failure: clinical approach. Fertil Steril 97:1039-1043
Simon C, Martin JC, Pellicer A (2000) Paracrine regulators of implantation. Baillieres Best Pract Res Clin Obstet Gynaecol 14:815-826
Smith SK (1994) Growth factors in the human endometrium. Hum Reprod 9:936-946
Staun-Ram E, Goldman S, Gabarin D, Shalev E (2004) Expression and importance of matrix metalloproteinase 2 and 9 (MMP-2 and -9) in human trophoblast invasion. Reprod Biol Endocrinol 2:59
Sugino N, Kashida S, Karube-Harada A, Takiguchi S, Kato H (2002) Expression of vascular endothelial growth factor (VEGF) and its receptors in human endometrium throughout the menstrual cycle and in early pregnancy. Reproduction 123:379-387
Sun X, Bartos A, Whitsett JA, Dey SK (2013) Uterine deletion of Gp130 or Stat3 shows implantation failure with increased estrogenic responses. Mol Endocrinol 27: 1492-501
Threadgill DW, Dlugosz AA, Hansen LA, Tennenbaum T, Lichti U, Yee D, LaMantia C, Mourton T, Herrup K, Harris RC, et al. (1995) Targeted disruption of mouse EGF receptor: effect of genetic background on mutant phenotype. Science 269:230-234
Toth B, Wurfel W, Germeyer A, Hirv K, Makrigiannakis A, Strowitzki T (2011) Disorders of implantation--are there diagnostic and therapeutic options? J Reprod Immunol 90: 117-23
Tsutsumi O, Oka T (1987) Epidermal growth factor deficiency during pregnancy causes abortion in mice. Am J Obstet Gynecol 156:241-244
Wang X, Wang H, Matsumoto H, Roy SK, Das SK, Paria BC (2002) Dual source and target of heparin-binding EGF-like growth factor during the onset of implantation in the hamster. Development 129:4125-4134
Wang XN, Das SK, Damm D, Klagsbrun M, Abraham JA, Dey SK (1994) Differential regulation of heparin-binding epidermal growth factor-like growth factor in the adult ovariectomized mouse uterus by progesterone and estrogen. Endocrinology 135: 1264-1271
Watson ED, Cross JC (2005) Development of structures and transport functions in the mouse placenta. Physiology (Bethesda); 20:180-193
Wooding P, Burton G (2008) Implantation, Maternofetal Exchange and Vascular Relationships. In: Comparative Placentation: Structures, Functions and Evolution. Berlin: Springer; 47-82
Xie H, Wang H, Tranguch S, Iwamoto R, Mekada E, Demayo FJ, Lydon JP, Das SK, Dey SK (2007) Maternal heparin-binding-EGF deficiency limits pregnancy success in mice. Proc Natl Acad Sci U S A 104:18315-18320
Yancopoulos GD, Davis S, Gale NW, Rudge JS, Wiegand SJ, Holash J (2000) Vascular-specific growth factors and blood vessel formation. Nature 407:242-248
Yarden Y (2001) The EGFR family and its ligands in human cancer. signalling mechanisms and therapeutic opportunities. Eur J Cancer 37 Suppl 4:S3-8
Yi XJ, Jiang HY, Lee KK, O WS, Tang PL, Chow PH (1999) Expression of vascular endothelial growth factor (VEGF) and its receptors during embryonic implantation in the golden hamster (Mesocricetus auratus). Cell Tissue Res 296:339-349
Yoo HJ, Barlow DH, Mardon HJ (1997) Temporal and spatial regulation of expression of heparin-binding epidermal growth factor-like growth factor in the human endometrium: a possible role in blastocyst implantation. Dev Genet 21:102-108
Yoshinaga K (1988) Uterine receptivity for blastocyst implantation. Ann N Y Acad Sci 541:424-431
Yoshinaga K (2014) Progesterone and its downstream molecules as blastocyst implantation essential factors. Am J Reprod Immunol 72:117-128
Young SL, Lessey BA, Fritz MA, Meyer WR, Murray MJ, Speckman PL, Nowicki BJ (2002) In vivo and in vitro evidence suggest that HB-EGF regulates endometrial expression of human decay-accelerating factor. J Clin Endocrinol Metab 87:1368-1375
Zhang J, Wang L, Cai QL (2001) The expression and function of VEGF at embryo implantation ‘window’ in the mouse. Chinese Sci, Bull, 46:409–411.
Zygmunt M, Herr F, Munstedt K, Lang U, Liang OD (2003) Angiogenesis and vasculogenesis in pregnancy. Eur J Obstet Gynecol Reprod Biol 110 Suppl 1:S10-18
Published
2018-03-31
How to Cite
[1]
Kumar, R., Haldar, C. and Pakrasi, P. 2018. Endocrine and paracrine interaction of growth factors during early pregnancy: A comparative perceptiveness in mammals. Journal of Biological Sciences and Medicine. 4, 1 (Mar. 2018), 27-40.
Section
Review Articles