Molecular Mechanism Of Implantation
This document was uploaded by user and they confirmed that they have the permission to share it. If you are author or own the copyright of this book, please report to us by using this DMCA report form. Report DMCA
Overview
Download & View Molecular Mechanism Of Implantation as PDF for free.
More details
- Words: 2,135
- Pages: 5
10/18/2009
http://www.jicef.or.jp/wahec/ful313.htm
Molecular Mechanism of Implantation Michiko N. Fukuda ABSTRACT Implantation following placentation is a unique system for mammals to reproduce. The initial attachment of the embryo to the uterus occurs via the apical cell membranes of two epithelial cells, trophoblast of the blastocyst and surface epithelial cells of the endometrium. Recently, a novel cell adhesion molecule complex, trophinin and tastin, potentially mediating the initial attachment of trophoblast to the endometrial epithelium was discovered (Fukuda, M. N., Sato, T., Nakayama, J., Klier, G., Mikami, M., Aoki, D., Nozawa, S., 1995, Genes & Development, 9, 1199-1210). This review provides a brief overview of cell adhesion molecules involved in implantation and introduces identification and characterization of trophinin and tastin.
KEY WORDS Ovum implantation, Cytoskeleton, Molecular cloning, Cell adhesion molecule, Embryo
INTRODUCTION Implantation is a unique system for mammals to reproduce. Studies on implantation at subcellular and molecular levels have been difficult due to the limitation of the materials to be analyzed. Recently a major break through was made in this area that is a discovery of trophinin and tastin. Availability of genetic probe of these new molecules in-volved in implantation enable us to analyze further the molecular mechanism underlying implantation, an investigation that may also shed light on the process of metastasis and invasion of tumor cells.
EMBRYO IMPLANTATION: A CELL BIOLOGICAL PARADOX A fertilized egg undergoes development from single cell stage to blastocyst. The blastocyst is composed of outer cellular layer and inner cell mass. Inner cell mass is made of the embryonic stem cells. Embryonic stem cells are pluripotent, are able to differentiate into a variety of cell types, and becomes a baby. Outer cellular layer of the blastocyst is composed of trophoblasts, adheres to the surface of endometrium, and becomes placenta. The early events of implantation are an initial apposition of the trophoblast to the uterus and subsequent adhesion and penetration of trophoblast into uterine epi-thelium1). The initial attachment of the trophoblast to the endometrial epithelium is described as "a cell biological paradox"2) since this cell-to-cell contact occurs via the apical cell membranes of two epithelial cells, trophoblast and endometrial epithelial cells. In general, the apical surface of the epithelium is not adhesive, whereas the basolateral surfaces support adhesion. One hypothesis to explain such cell adhesion is that the http://www.jicef.or.jp/wahec/ful313.htm
1/5
10/18/2009
http://www.jicef.or.jp/wahec/ful313.htm
apical surfaces of the trophectoderm and the uterine epithelium express a "basolateral" character that promotes adhesion between these two cell types 3,4,5). Alternatively, the apical plasma membranes of the trophoblast and endometrial epithelial might express unique cell adhesion molecule(s) that mediate an initial attachment between these cells 6).
SEARCH FOR CELL ADHESION MOLECULES INVOLVED IN IMPLANTATION Attempts to identify molecules involved in embryo implantation have been conducted both in vivo and in vitro3,4,5,7,8,9,10,11,12). By using specific antibodies to the cell adhesion molecules such as cadherins and integrins, trophoblasts and endometrial epithelial cells at the time of implantation were investigated4,5,7,8,9,10). For example, when the blastocyst attached to the uterine epithelium, Eand P-cadherins were detected at the cell-cell boundaries but not at the apical surface of either epithelia, suggesting that the initial adhesion of trophoblast cells to the uterine epithelium is mediated by molecules other than E- and P-cad-herins 7,8,9). These studies also suggested that disappearance of cad herins is linked to the acquisition of trophoblast invasiveness 13). An integrin such as 1-integrin is another molecule thought to be involved in implantation. However, recent report of 1-integrin gene knock-out mouse revealed that 1 -integrin is not necessary for implantation itself, but both inner cell mass and trophoblasts of 1-integrin null blastocysts degenerated about one day after implantation14). Several lines of evidence indicate that changes in the state of uterine receptivity correlate with changes in cell surface carbohydrate structures. These studies revealed that subtle modifications of lactosaminoglycan carbohydrates 12), sulfated glycolipids 15), fucosylated carbohydrates 12,16) and heparan sulfate and heparan sulfate binding protein3) are related to the hormonally induced preparative and receptive phases of uterine epithelium. These studies, however, have not identified the cell adhesion molecule unique to embryo implantation.
HT-H AND SNG-M CELL LINES MAY SERVE AS AN IN VITRO MODEL FOR IMPLANTATION Cell lines established from mouse teratocardnomas have been used for an in vitro model for early embryogenesis, as these cell lines often exhibit cells at early embryos. HT-H cells established from testicular teratocarcinoma form syncytia in vitro and synthesize and secrete progesterone and hCG17). They also exhibit phagocytic activity and express a colony-stimulating factor-1 receptor (cfms product). HT-H cells express cytokeratin, but not vimentin, indicative of the epithelial nature of this cell line. These properties of HT-H cells suggested that HT-H cell line represents syncytiotrophoblasts at early embryonic stage. SNG-M cell line has been established from a metastatic region of endometrial adenocarcinoma 8). Various properties suggested that this cell line represents endometrial epithelial cells. When HT-H cells were added to a monolayer of SNG-M cells, HT-H cells immediately adhered to the upper surface of SNG-M cells 22). Electron micrographs of the contact site between HT-H and SNG-M cells showed numerous microvilli on both cell types (Figure 1 A & B). After co-culturing for 6 hours, the microvilli flatten (Figure 1C), and after 4 days co-culturing, formation of junctional complexes consisting of desmosomes was seen which is indicative of stronger adhesion between these two cell http://www.jicef.or.jp/wahec/ful313.htm
2/5
10/18/2009
http://www.jicef.or.jp/wahec/ful313.htm
types (Figure 1-D). These morphological features resemble those that have been reported in the literatures for embryo implantation site19), suggesting that the Hr-H and SNG-M cells are useful models for analyzing adhesive interaction between trophoblast and endometrial epithelial cells at the time of implantation.
IDENTIFICATION OF THE MOLECULES RESPONSIBLE FOR THE ADHESION BETWEEN THE HT-H AND SNG-M CELLS BY EXPRESSION cDNA CLONING20) Molecules responsible for the initial attachment of HT-H cells to a monolayer of SNG-M cells were identified by expression cDNA cloning, as illustrated in Figure 2. Two clones were identified; one is named "trophinin" and the other named "tastin". Trophinin is predicted to be an intrinsic membrane protein composed of 749 amino acids. The amino terminal region is predicted to form a cytoplasmic domain. The most striking structural feature of trophinin is that more than 90% of this molecule is made of tandem repeats of a decapeptide. Trophinin's decapeptide repeats is predicted to form repeated -turn, which may be the structural element of self-binding. Antibodies raised against the predicted cell surface domains of trophinin inhibited the adhesion between HT-H and SNG-M cells. When trophinin polypeptides are added to trophinin expressing cells, such as HT-H and SNG-M cells, trophinin peptides adhered to the surface of these cells. Tastin is predicted to be a cytoplasmic protein made of 778 amino acids. When trophinin was expressed sigly, they were seen as a regularly distributed antigen on the cell surface. In contrast, when trophinin and tastin are expressed together in COS-1 cells, trophinin are seen as clustered patches on the cell surface. Thus tastin appears to induce clustering of trophinin. Association of trophinin with tastin would restrict the distribution of trophinins, creating multivalent and efficient cell adhesion sites on the plasma membranes.
POTENTIAL INVOLVEMENT OF TROPHININ AND TASTIN IN EMBRYO IMPLANTATION20) Immunohistology of various human tissues revealed that neither trophinin nor tastin are expressed in normal adult human cells except macrophages. In human en-dometrium, trophinin and tastin were not detected in the proliferation stage, at the ovulation stage and late secretary phases. Trophinin is strongly expressed on the apical plasma membranes of the surface epithelium at an early secretory phase (Figure 3). Tatsin was also detected in the endometrial epithelial cells where trophinin was expressed. These observations suggest that trophinin and tastin are expressed in surface epithelia at the time of the "implantation window"20). Strong expression of trophinin was detected at the apical plasma membranes of trophectoderm of monkey blastocysts (Figure 4). Trophinins are elevated at the embryonic pole and are relatively weakly expressed at the mural pole. Such polarized distribution of trophinin is consistent with the observations that, in both primates and humans, a blastocyst attaches to endometrial epithelium at its embryonic pole1,2,19). The specific and restricted in vivo expression of trophinin and tastin in the cells involved in implantation strongly suggests that trophinin and tastin are the molecules mediating the initial attachment of embryo to the uterus. http://www.jicef.or.jp/wahec/ful313.htm
3/5
10/18/2009
http://www.jicef.or.jp/wahec/ful313.htm
FUTURE PROSPECT OF THE RESEARCH OF EMBRYO IMPLANTATION The unique cell adhesion process of the trophoblast to endometrium epithelia at the time of implantation and subsequent invasion of the trophoblast into the maternal tissue forms an essential element of embryo implantation. This process is often compared to metastasis and invasion of malignant tumors. Therefore, understanding the mechanisms underlying the adhesive cell-to-cell interactions between trophoblast and endometrial epithelial cells will allow us to better understand both implantation and tumor metastasis and invasion.
ACKNOWLEDGEMENTS This article is based on the lecture that was given on September 6th 1995 at Keio University School of Medi-cine, hosted by Professor Shiro Nozawa, Department of Gynecology and Obstetrics. Detailed version has been given as a review in Keio Journal of Medicine, 45 (1) 37-43, 1996.
REFERENCES 1. Sclafke S and Enders AC: Cellular basis of interaction between trophoblast and uterus at implantation. Biol Repriod 1975, 12: 41-65 2. Denker, H.-W. Trophoblast-endometrial interactions at embryo implantation; A cell biological paradox. In: Trophoblast research, edited by Denker, H.-W. and Aplin, J.D. New York and London: Plenum Medical Book Company. 1990, p. 3-20. 3. Farach MC, Tang JP, Decker GL and Carson DD: Heparin/heparan sulfate is involved in attachment and spreading of mouse embryos in vitro. Dev. Biol 1987, 123: 401-410 4. Stephens LE, Sutherland AE, Klimanskaya IV, Andneux A, Meneses J, Pedersen RA and Damsky CH: Deletion of 1 integrins in mice results in inner cell mass failure and peri-implantation lethality. Genes & Develop 1995. 9: 1883-1895 5. Sutherland AE, Calario PG and Damsky CH: Expression and function of cell surface extracellular matrix receptors in mouse blastocyst attachment and outgrowth. J Cell Biol 1988. 106: 13311348 6. Kliman, H.J., Coutifaris, C., Feinberg, R.F., Straus, J.F.III and Haimowitz, J.E. Implantation: in vitro models utilizing human tissues. In: Blastocyst Implantation, edited by Yoshinaga, K. Boston: Adams Publishing, 1989, pp. 83-91. 7. Damjanov I, Damijanov. A. and Damsky CH: Developmentally regulated expression of the cellcell adhesion glycoprotein cell-CAM120/80 in periimplantation mouse embryos and extraembryonic membranes. Dev Biol 1986, 116: 194-202 8. Svalander PC, Odin P, Nilsson BO and Obrink B: Trophectoderm surface expression of the cell adhesion molecule cell-CAM 105 on rat blastocysts. Development 1987. 100: 653-660 9. Kadokawa Y, Fuketa I, Nose A, Takeichi M and Nakatsuji N: Expression pattern of E- and Pcadherin in mouse embryos and uteri during the periimplantation period. Develop Growth and Diff 1989, 31: 23-30 10. Nose A and Takeichi M: A novel cadherin cell adhesion molecule; Its expression patterns associated with implantation and organogenesis of mouse embryos. J Cell Biol 1986. 103: 2649-2658 11. Dutt A, Tang J-P and Carson DD: Lactosaminoglycans are involved in uterine epithelial cell http://www.jicef.or.jp/wahec/ful313.htm
4/5
10/18/2009
12. 13. 14. 15.
16. 17. 18. 19. 20.
http://www.jicef.or.jp/wahec/ful313.htm
adhesion in vitro. Dev Biol 1987, 119: 27-37 Kimber SJ, Lindenberg S and Lundblad A: Distribution of some Galb 1 -3(4)GlcNAc related carbohydrate antigens on the mouse uterine epithelium in relation to the peri-implantation period. J Reprod Imm 1988, 12: 297-313 Vleminckx K, Vakaet Jr,L., Mareel M, Friers W and Van Roy F: Genetic manipulation of Ecadherin expression by epithelial tumor cells reveals an invasion suppressor role. Cell 1991, 66: 107-119 Stephens, L.E., Sutherland, A.E., Klimanskaya, I V., Andrieux, A., Meneses, J., Pedersen, R.A. and Damsky, C.H. 1995. Deletion of beta 1 integrins in Genes & Develop. 9: 1883-1895. Kubushiro K, Kojima K, Mikami, Nozawa S, Iizuka R, Iwamori M and Nagai Y: Menstrual cycleassociated alteration of sulfogalactosylceramide in human uterine endometrium; possible induction of glycolipid sulfation by sex steroid hormones. Arch Biochem Biophis 1989, 268: 129-136 Yamagata T and Yamazaki K: Implanting mouse embryo stain with a LNF-I bearing fluorescent probe at their mural trophectodermal sided. Biochem Biophys Res Commun 1991, 181: 10041009 Izhar M, Siebert P, Oshima RG, DeWolf WC and Fnkuda MN: Trophoblastic differentiation of human teratocarcinoma cell line HT-H. Dev Biol 1986, 116: 510-518 Ishiwata I, Nozawa S, Inoue T and Okumura H: Development and characterization of established cell lines from primary and metastatic regions of human endometrial carcinomas. Cancer Res 1977, 37: 1777-1785 Lindenberg S, Hyttel P, Lenz S and Holmes PV: Ultrastructure of the early human implantation in vitro. Hum Reprod 1986, 1 : 533-538 Fukuda MN, Sato T, Nakayama J, Klier G, Mikami M, Aoki D and Nozawa S: Trophinin and tastin; A novel cell adhesion complex with potential involvement in embryo implantation. Genes & Develop 1995, 9: I 199-1210
Received on November 5, 1996 and accepted on February 25, 1997 The Burnham Institute La Jolla, California 92037, U.S.A. |Home | Theme | Back |
http://www.jicef.or.jp/wahec/ful313.htm
5/5
http://www.jicef.or.jp/wahec/ful313.htm
Molecular Mechanism of Implantation Michiko N. Fukuda ABSTRACT Implantation following placentation is a unique system for mammals to reproduce. The initial attachment of the embryo to the uterus occurs via the apical cell membranes of two epithelial cells, trophoblast of the blastocyst and surface epithelial cells of the endometrium. Recently, a novel cell adhesion molecule complex, trophinin and tastin, potentially mediating the initial attachment of trophoblast to the endometrial epithelium was discovered (Fukuda, M. N., Sato, T., Nakayama, J., Klier, G., Mikami, M., Aoki, D., Nozawa, S., 1995, Genes & Development, 9, 1199-1210). This review provides a brief overview of cell adhesion molecules involved in implantation and introduces identification and characterization of trophinin and tastin.
KEY WORDS Ovum implantation, Cytoskeleton, Molecular cloning, Cell adhesion molecule, Embryo
INTRODUCTION Implantation is a unique system for mammals to reproduce. Studies on implantation at subcellular and molecular levels have been difficult due to the limitation of the materials to be analyzed. Recently a major break through was made in this area that is a discovery of trophinin and tastin. Availability of genetic probe of these new molecules in-volved in implantation enable us to analyze further the molecular mechanism underlying implantation, an investigation that may also shed light on the process of metastasis and invasion of tumor cells.
EMBRYO IMPLANTATION: A CELL BIOLOGICAL PARADOX A fertilized egg undergoes development from single cell stage to blastocyst. The blastocyst is composed of outer cellular layer and inner cell mass. Inner cell mass is made of the embryonic stem cells. Embryonic stem cells are pluripotent, are able to differentiate into a variety of cell types, and becomes a baby. Outer cellular layer of the blastocyst is composed of trophoblasts, adheres to the surface of endometrium, and becomes placenta. The early events of implantation are an initial apposition of the trophoblast to the uterus and subsequent adhesion and penetration of trophoblast into uterine epi-thelium1). The initial attachment of the trophoblast to the endometrial epithelium is described as "a cell biological paradox"2) since this cell-to-cell contact occurs via the apical cell membranes of two epithelial cells, trophoblast and endometrial epithelial cells. In general, the apical surface of the epithelium is not adhesive, whereas the basolateral surfaces support adhesion. One hypothesis to explain such cell adhesion is that the http://www.jicef.or.jp/wahec/ful313.htm
1/5
10/18/2009
http://www.jicef.or.jp/wahec/ful313.htm
apical surfaces of the trophectoderm and the uterine epithelium express a "basolateral" character that promotes adhesion between these two cell types 3,4,5). Alternatively, the apical plasma membranes of the trophoblast and endometrial epithelial might express unique cell adhesion molecule(s) that mediate an initial attachment between these cells 6).
SEARCH FOR CELL ADHESION MOLECULES INVOLVED IN IMPLANTATION Attempts to identify molecules involved in embryo implantation have been conducted both in vivo and in vitro3,4,5,7,8,9,10,11,12). By using specific antibodies to the cell adhesion molecules such as cadherins and integrins, trophoblasts and endometrial epithelial cells at the time of implantation were investigated4,5,7,8,9,10). For example, when the blastocyst attached to the uterine epithelium, Eand P-cadherins were detected at the cell-cell boundaries but not at the apical surface of either epithelia, suggesting that the initial adhesion of trophoblast cells to the uterine epithelium is mediated by molecules other than E- and P-cad-herins 7,8,9). These studies also suggested that disappearance of cad herins is linked to the acquisition of trophoblast invasiveness 13). An integrin such as 1-integrin is another molecule thought to be involved in implantation. However, recent report of 1-integrin gene knock-out mouse revealed that 1 -integrin is not necessary for implantation itself, but both inner cell mass and trophoblasts of 1-integrin null blastocysts degenerated about one day after implantation14). Several lines of evidence indicate that changes in the state of uterine receptivity correlate with changes in cell surface carbohydrate structures. These studies revealed that subtle modifications of lactosaminoglycan carbohydrates 12), sulfated glycolipids 15), fucosylated carbohydrates 12,16) and heparan sulfate and heparan sulfate binding protein3) are related to the hormonally induced preparative and receptive phases of uterine epithelium. These studies, however, have not identified the cell adhesion molecule unique to embryo implantation.
HT-H AND SNG-M CELL LINES MAY SERVE AS AN IN VITRO MODEL FOR IMPLANTATION Cell lines established from mouse teratocardnomas have been used for an in vitro model for early embryogenesis, as these cell lines often exhibit cells at early embryos. HT-H cells established from testicular teratocarcinoma form syncytia in vitro and synthesize and secrete progesterone and hCG17). They also exhibit phagocytic activity and express a colony-stimulating factor-1 receptor (cfms product). HT-H cells express cytokeratin, but not vimentin, indicative of the epithelial nature of this cell line. These properties of HT-H cells suggested that HT-H cell line represents syncytiotrophoblasts at early embryonic stage. SNG-M cell line has been established from a metastatic region of endometrial adenocarcinoma 8). Various properties suggested that this cell line represents endometrial epithelial cells. When HT-H cells were added to a monolayer of SNG-M cells, HT-H cells immediately adhered to the upper surface of SNG-M cells 22). Electron micrographs of the contact site between HT-H and SNG-M cells showed numerous microvilli on both cell types (Figure 1 A & B). After co-culturing for 6 hours, the microvilli flatten (Figure 1C), and after 4 days co-culturing, formation of junctional complexes consisting of desmosomes was seen which is indicative of stronger adhesion between these two cell http://www.jicef.or.jp/wahec/ful313.htm
2/5
10/18/2009
http://www.jicef.or.jp/wahec/ful313.htm
types (Figure 1-D). These morphological features resemble those that have been reported in the literatures for embryo implantation site19), suggesting that the Hr-H and SNG-M cells are useful models for analyzing adhesive interaction between trophoblast and endometrial epithelial cells at the time of implantation.
IDENTIFICATION OF THE MOLECULES RESPONSIBLE FOR THE ADHESION BETWEEN THE HT-H AND SNG-M CELLS BY EXPRESSION cDNA CLONING20) Molecules responsible for the initial attachment of HT-H cells to a monolayer of SNG-M cells were identified by expression cDNA cloning, as illustrated in Figure 2. Two clones were identified; one is named "trophinin" and the other named "tastin". Trophinin is predicted to be an intrinsic membrane protein composed of 749 amino acids. The amino terminal region is predicted to form a cytoplasmic domain. The most striking structural feature of trophinin is that more than 90% of this molecule is made of tandem repeats of a decapeptide. Trophinin's decapeptide repeats is predicted to form repeated -turn, which may be the structural element of self-binding. Antibodies raised against the predicted cell surface domains of trophinin inhibited the adhesion between HT-H and SNG-M cells. When trophinin polypeptides are added to trophinin expressing cells, such as HT-H and SNG-M cells, trophinin peptides adhered to the surface of these cells. Tastin is predicted to be a cytoplasmic protein made of 778 amino acids. When trophinin was expressed sigly, they were seen as a regularly distributed antigen on the cell surface. In contrast, when trophinin and tastin are expressed together in COS-1 cells, trophinin are seen as clustered patches on the cell surface. Thus tastin appears to induce clustering of trophinin. Association of trophinin with tastin would restrict the distribution of trophinins, creating multivalent and efficient cell adhesion sites on the plasma membranes.
POTENTIAL INVOLVEMENT OF TROPHININ AND TASTIN IN EMBRYO IMPLANTATION20) Immunohistology of various human tissues revealed that neither trophinin nor tastin are expressed in normal adult human cells except macrophages. In human en-dometrium, trophinin and tastin were not detected in the proliferation stage, at the ovulation stage and late secretary phases. Trophinin is strongly expressed on the apical plasma membranes of the surface epithelium at an early secretory phase (Figure 3). Tatsin was also detected in the endometrial epithelial cells where trophinin was expressed. These observations suggest that trophinin and tastin are expressed in surface epithelia at the time of the "implantation window"20). Strong expression of trophinin was detected at the apical plasma membranes of trophectoderm of monkey blastocysts (Figure 4). Trophinins are elevated at the embryonic pole and are relatively weakly expressed at the mural pole. Such polarized distribution of trophinin is consistent with the observations that, in both primates and humans, a blastocyst attaches to endometrial epithelium at its embryonic pole1,2,19). The specific and restricted in vivo expression of trophinin and tastin in the cells involved in implantation strongly suggests that trophinin and tastin are the molecules mediating the initial attachment of embryo to the uterus. http://www.jicef.or.jp/wahec/ful313.htm
3/5
10/18/2009
http://www.jicef.or.jp/wahec/ful313.htm
FUTURE PROSPECT OF THE RESEARCH OF EMBRYO IMPLANTATION The unique cell adhesion process of the trophoblast to endometrium epithelia at the time of implantation and subsequent invasion of the trophoblast into the maternal tissue forms an essential element of embryo implantation. This process is often compared to metastasis and invasion of malignant tumors. Therefore, understanding the mechanisms underlying the adhesive cell-to-cell interactions between trophoblast and endometrial epithelial cells will allow us to better understand both implantation and tumor metastasis and invasion.
ACKNOWLEDGEMENTS This article is based on the lecture that was given on September 6th 1995 at Keio University School of Medi-cine, hosted by Professor Shiro Nozawa, Department of Gynecology and Obstetrics. Detailed version has been given as a review in Keio Journal of Medicine, 45 (1) 37-43, 1996.
REFERENCES 1. Sclafke S and Enders AC: Cellular basis of interaction between trophoblast and uterus at implantation. Biol Repriod 1975, 12: 41-65 2. Denker, H.-W. Trophoblast-endometrial interactions at embryo implantation; A cell biological paradox. In: Trophoblast research, edited by Denker, H.-W. and Aplin, J.D. New York and London: Plenum Medical Book Company. 1990, p. 3-20. 3. Farach MC, Tang JP, Decker GL and Carson DD: Heparin/heparan sulfate is involved in attachment and spreading of mouse embryos in vitro. Dev. Biol 1987, 123: 401-410 4. Stephens LE, Sutherland AE, Klimanskaya IV, Andneux A, Meneses J, Pedersen RA and Damsky CH: Deletion of 1 integrins in mice results in inner cell mass failure and peri-implantation lethality. Genes & Develop 1995. 9: 1883-1895 5. Sutherland AE, Calario PG and Damsky CH: Expression and function of cell surface extracellular matrix receptors in mouse blastocyst attachment and outgrowth. J Cell Biol 1988. 106: 13311348 6. Kliman, H.J., Coutifaris, C., Feinberg, R.F., Straus, J.F.III and Haimowitz, J.E. Implantation: in vitro models utilizing human tissues. In: Blastocyst Implantation, edited by Yoshinaga, K. Boston: Adams Publishing, 1989, pp. 83-91. 7. Damjanov I, Damijanov. A. and Damsky CH: Developmentally regulated expression of the cellcell adhesion glycoprotein cell-CAM120/80 in periimplantation mouse embryos and extraembryonic membranes. Dev Biol 1986, 116: 194-202 8. Svalander PC, Odin P, Nilsson BO and Obrink B: Trophectoderm surface expression of the cell adhesion molecule cell-CAM 105 on rat blastocysts. Development 1987. 100: 653-660 9. Kadokawa Y, Fuketa I, Nose A, Takeichi M and Nakatsuji N: Expression pattern of E- and Pcadherin in mouse embryos and uteri during the periimplantation period. Develop Growth and Diff 1989, 31: 23-30 10. Nose A and Takeichi M: A novel cadherin cell adhesion molecule; Its expression patterns associated with implantation and organogenesis of mouse embryos. J Cell Biol 1986. 103: 2649-2658 11. Dutt A, Tang J-P and Carson DD: Lactosaminoglycans are involved in uterine epithelial cell http://www.jicef.or.jp/wahec/ful313.htm
4/5
10/18/2009
12. 13. 14. 15.
16. 17. 18. 19. 20.
http://www.jicef.or.jp/wahec/ful313.htm
adhesion in vitro. Dev Biol 1987, 119: 27-37 Kimber SJ, Lindenberg S and Lundblad A: Distribution of some Galb 1 -3(4)GlcNAc related carbohydrate antigens on the mouse uterine epithelium in relation to the peri-implantation period. J Reprod Imm 1988, 12: 297-313 Vleminckx K, Vakaet Jr,L., Mareel M, Friers W and Van Roy F: Genetic manipulation of Ecadherin expression by epithelial tumor cells reveals an invasion suppressor role. Cell 1991, 66: 107-119 Stephens, L.E., Sutherland, A.E., Klimanskaya, I V., Andrieux, A., Meneses, J., Pedersen, R.A. and Damsky, C.H. 1995. Deletion of beta 1 integrins in Genes & Develop. 9: 1883-1895. Kubushiro K, Kojima K, Mikami, Nozawa S, Iizuka R, Iwamori M and Nagai Y: Menstrual cycleassociated alteration of sulfogalactosylceramide in human uterine endometrium; possible induction of glycolipid sulfation by sex steroid hormones. Arch Biochem Biophis 1989, 268: 129-136 Yamagata T and Yamazaki K: Implanting mouse embryo stain with a LNF-I bearing fluorescent probe at their mural trophectodermal sided. Biochem Biophys Res Commun 1991, 181: 10041009 Izhar M, Siebert P, Oshima RG, DeWolf WC and Fnkuda MN: Trophoblastic differentiation of human teratocarcinoma cell line HT-H. Dev Biol 1986, 116: 510-518 Ishiwata I, Nozawa S, Inoue T and Okumura H: Development and characterization of established cell lines from primary and metastatic regions of human endometrial carcinomas. Cancer Res 1977, 37: 1777-1785 Lindenberg S, Hyttel P, Lenz S and Holmes PV: Ultrastructure of the early human implantation in vitro. Hum Reprod 1986, 1 : 533-538 Fukuda MN, Sato T, Nakayama J, Klier G, Mikami M, Aoki D and Nozawa S: Trophinin and tastin; A novel cell adhesion complex with potential involvement in embryo implantation. Genes & Develop 1995, 9: I 199-1210
Received on November 5, 1996 and accepted on February 25, 1997 The Burnham Institute La Jolla, California 92037, U.S.A. |Home | Theme | Back |
http://www.jicef.or.jp/wahec/ful313.htm
5/5
Related Documents
Molecular Mechanism Of Implantation
June 2020 6
Embryo Implantation - The Molecular Mechanism
June 2020 4
Molecular Mechanism Of Ebv
October 2019 8
Mechanism
December 2019 34
Mechanism
June 2020 16