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7 - Implantation is a sticky situation

from General discussion I

Published online by Cambridge University Press:  07 August 2009

By
Olga Genbacev ,
Akraporn Prakobphol ,
Russell A. Foulk  and
Susan J. Fisher
Edited by
Ashley Moffett ,
Charlie Loke  and
Anne McLaren
Ashley Moffett
Affiliation:
University of Cambridge
Charlie Loke
Affiliation:
University of Cambridge
Anne McLaren
Affiliation:
Cancer Research, UK
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Summary

Abstract. For many reasons the implantation process has been extraordinarily difficult to study. The molecules that orchestrate this highly specialised event are likely localised to the interacting surfaces of only a few embryonic and maternal cells. Additionally, their expression, which is precisely timed, may also be transient. Therefore, much of what we know about this process at a molecular level, such as the importance of leukaemia inhibitory factor (LIF), is a by-product of studying mutant mice that were generated for other purposes. In other cases, the ‘candidate molecule’ approach has been fruitful, as exemplified by recently published evidence that L-selectin and its carbohydrate ligands are involved in the initial stages of implantation. In this review we discuss the current body of knowledge regarding L-selectin functions, which prompted experiments to examine expression of this receptor and its specialised carbohydrate ligands during implantation and the early stages of placentation. The results highlight the amazing plasticity of trophoblast cells that have co-opted portions of vascular and leukocyte differentiation programmes. The challenge now is to use our knowledge of the trophoblast L-selectin adhesion system to benefit women who fail to conceive due to defects in the implantation process.

Introduction

After fertilization, the next major hurdle for human reproduction is trophoblast differentiation, which is required for implantation, followed in lockstep by rapid assembly of these embryonic cells into a functional placenta.

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Biology and Pathology of Trophoblast , pp. 132 - 147
Publisher: Cambridge University Press
Print publication year: 2006

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References

Andrews, P., Ford, W. L. & Stoddart, R. W. (1980). Metabolic studies of high-walled endothelium of postcapillary venules in rat lymph nodes. Ciba Found. Symp., 71, 211–30.Google ScholarPubMed
Arbones, M. L., Ord, D. C., Ley, K.et al. (1994). Lymphocyte homing and leukocyte rolling and migration are impaired in L-selectin-deficient mice. Immunity, 1, 247–60.CrossRefGoogle ScholarPubMed
Bistrup, A., Bhakta, S., Lee, J. K.et al. (1999). Sulfotransferases of two specificities function in the reconstitution of high endothelial cell ligands for L-selectin. J. Cell Biol., 145, 899–910.CrossRefGoogle ScholarPubMed
Butcher, E. C. & Picker, L. J. (1996). Lymphocyte homing and homeostasis. Science, 272, 60–6.CrossRefGoogle ScholarPubMed
Carson, D. D., Bagchi, I., Dey, S. K.et al. (2000). Embryo implantation. Dev. Biol., 223, 217–37.CrossRefGoogle ScholarPubMed
Chantakru, S., Wang, W. C., Heuvel, M.et al. (2003). Coordinate regulation of lymphocyte-endothelial interactions by pregnancy-associated hormones. J. Immunol., 171, 4011–19.CrossRefGoogle ScholarPubMed
Chen, S. & Springer, T. A. (1999). An automatic braking system that stabilizes leukocyte rolling by an increase in selectin bond number with shear. J. Cell Biol., 144, 185–200.CrossRefGoogle ScholarPubMed
Drake, P. M., Gunn, M. D., Charo, I. F.et al. (2001). Human placental cytotrophoblasts attract monocytes and CD56 (bright) natural killer cells via the actions of monocyte inflammatory protein 1alpha. J. Exp. Med. 193, 1199–212.CrossRefGoogle ScholarPubMed
Finger, E. B., Puri, K. D., Alon, R.et al. (1996). Adhesion through L-selectin requires a threshold hydrodynamic shear. Nature, 379, 266–9.CrossRefGoogle ScholarPubMed
Gallatin, W. M., Weissman, I. L. & Butcher, E. C. (1983). A cell-surface molecule involved in organ-specific homing of lymphocytes. Nature, 304, 30–4.CrossRefGoogle ScholarPubMed
Genbacev, O., Schubach, S. A. & Miller, R. K. (1992). Villous culture of first trimester human placenta – model to study extravillous trophoblast (EVT) differentiation. Placenta, 13, 439–61.CrossRefGoogle ScholarPubMed
Gesner, B. M. & Ginsburg, V. (1964). Effect of glycosidases on the fate of transfused lymphocytes. Proc. Natl. Acad. Sci. U.S.A., 52, 750–5.CrossRefGoogle ScholarPubMed
Gowans, J. L. & Knight, E. J. (1964). The route of re-circulation of lymphocytes in the rat. Proc. R. Soc. Lond. B. Biol. Sci., 159, 257–82.CrossRefGoogle ScholarPubMed
Guleria, I. & Pollard, J. W. (2000). The trophoblast is a component of the innate immune system during pregnancy. Nat. Med., 6, 589–93.CrossRefGoogle ScholarPubMed
Hemmerich, S., Leffler, H. & Rosen, S. D. (1995). Structure of the O-glycans in GlyCAM-1, an endothelial-derived ligand for L-selectin. J. Biol. Chem., 270, 12035–47.CrossRefGoogle ScholarPubMed
Imai, Y., Singer, M. S., Fennie, C., Lasky, L. A. & Rosen, S. D. (1991). Identification of a carbohydrate-based endothelial ligand for a lymphocyte homing receptor. J. Cell Biol., 113, 1213–21.CrossRefGoogle ScholarPubMed
Kanamori, A., Kojima, N., Uchimura, K.et al. (2002). Distinct sulfation requirements of selectins disclosed using cells that support rolling mediated by all three selectins under shear flow. L-selectin prefers carbohydrate 6-sulphation to tyrosine sulphation, whereas P-selectin does not. J. Biol. Chem., 277, 32578–86.CrossRefGoogle Scholar
Kao, L. C., Tulac, S., Lobo, S.et al. (2002). Global gene profiling in human endometrium during the window of implantation. Endocrinology, 143, 2119–38.CrossRefGoogle ScholarPubMed
Kao, L. C., Germeyer, A., Tulac, S.et al. (2003). Expression profiling of endometrium from women with endometriosis reveals candidate genes for disease-based implantation failure and infertility. Endocrinology, 144, 2870–81.CrossRefGoogle ScholarPubMed
Kimura, N., Mitsuoka, C., Kanamori, A.et al. (1999). Reconstitution of functional L-selectin ligands on a cultured human endothelial cell line by cotransfection of alpha1→3 fucosyltransferase VII and newly cloned GlcNAcbeta:6-sulfotransferase cDNA. Proc. Natl. Acad. Sci. U.S.A., 96, 4530–5.CrossRefGoogle ScholarPubMed
Lasky, L. A. (1995). Selectin–carbohydrate interactions and the initiation of the inflammatory response. Annu. Rev. Biochem., 64, 113–39.CrossRefGoogle ScholarPubMed
Lowe, J. B. (2002). Glycosylation in the control of selectin counter-receptor structure and function. Immunol. Rev., 186, 19–36.CrossRefGoogle ScholarPubMed
Maly, P., Thall, A., Petryniak, B.et al. (1996). The alpha(1,3)fucosyltransferase Fuc-TVII controls leukocyte trafficking through an essential role in L-, E-, and P-selectin ligand biosynthesis. Cell, 86, 643–53.CrossRefGoogle Scholar
McNagny, K. M., Pettersson, I., Rossi, F.et al. (1997). Thrombomucin, a novel cell surface protein that defines thrombocytes and multipotent hematopoietic progenitors. J. Cell Biol., 138, 1395–407.CrossRefGoogle ScholarPubMed
Paria, B. C., Reese, J., Das, S. K. & Dey, S. K. (2002). Deciphering the crosstalk of implantation: advances and challenges. Science, 296, 2185–8.CrossRefGoogle Scholar
Puri, K. D., Finger, E. B., Gaudernack, G. & Springer, T. A. (1995). Sialomucin CD34 is the major L-selectin ligand in human tonsil high endothelial venules. J. Cell Biol., 131, 261– 70.CrossRefGoogle ScholarPubMed
Renkonen, J., Tynninen, O., Hayry, P., Paavonen, T. & Renkonen, R. (2002). Glycosylation might provide endothelial zip codes for organ-specific leukocyte traffic into inflammatory sites. Am. J. Pathol., 161, 543–50.CrossRefGoogle ScholarPubMed
Rosen, S. D. (1999). Endothelial ligands for L-selectin: from lymphocyte recirculation to allograft rejection. Am. J. Pathol., 155, 1013–20.CrossRefGoogle ScholarPubMed
Rosen, S. D., Singer, M. S., Yednock, T. A. & Stoolman, L. M. (1985). Involvement of sialic acid on endothelial cells in organ-specific lymphocyte recirculation. Science, 228, 1005–7.CrossRefGoogle ScholarPubMed
Salmi, M. & Jalkanen, S. (1997). How do lymphocytes know where to go: current concepts and enigmas of lymphocyte homing. Adv. Immunol., 64, 139–218.CrossRefGoogle ScholarPubMed
Sassetti, C., Tangemann, K., Singer, M. S., Kershaw, D. B. & Rosen, S. D. (1998). Identification of podocalyxin-like protein as a high endothelial venule ligand for L-selectin: parallels to CD34. J. Exp. Med., 187, 1965–75.CrossRefGoogle ScholarPubMed
Satomaa, T., Renkonen, O., Helin, J.et al. (2002). O-glycans on human high endothelial CD34 putatively participating in L-selectin recognition. Blood, 99, 2609–11.CrossRefGoogle ScholarPubMed
Scudder, P. R., Shailubhai, K., Duffin, K. L., Streeter, P. R. & Jacob, G. S. (1994). Enzymatic synthesis of a 6′-sulfated sialyl-Lewis ⅹ which is an inhibitor of L-selectin binding to peripheral addressin. Glycobiology, 4, 929–32.CrossRefGoogle Scholar
Springer, T. A. (1994). Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell, 76, 301–14.CrossRefGoogle ScholarPubMed
Stamper, H. B. & Woodruff, J. J. (1976). Lymphocyte homing into lymph nodes: in vitro demonstration of the selective affinity of recirculating lymphocytes for high-endothelial venules. J. Exp. Med., 144, 828–33.CrossRefGoogle ScholarPubMed
Stoolman, L. M. & Rosen, S. D. (1983). Possible role for cell-surface carbohydrate-binding molecules in lymphocyte recirculation. J. Cell Biol., 96, 722–9.CrossRefGoogle ScholarPubMed
Streeter, P. R., Rouse, B. T. & Butcher, E. C. (1988). Immunohistologic and functional characterization of a vascular addressin involved in lymphocyte homing into peripheral lymph nodes. J. Cell Biol., 107, 1853–62.CrossRefGoogle ScholarPubMed
Suzuki, A., Andrew, D. P., Gonzalo, J. A.et al. (1996). CD34-deficient mice have reduced eosinophil accumulation after allergen exposure and show a novel crossreactive 90-kD protein. Blood, 87, 3550–62.Google ScholarPubMed
Varki, A. (1997). Selectin ligands: will the real ones please stand up?J. Clin. Invest., 100, S31–5.Google ScholarPubMed
Andrian, U. H. (1996). Intravital microscopy of the peripheral lymph node microcirculation in mice. Microcirculation, 3, 287–300.CrossRefGoogle Scholar
Andrian, U. H. & Mackay, C. R. (2000). T-cell function and migration. Two sides of the same coin. New Engl. J. Med., 343, 1020–34.CrossRefGoogle Scholar
Yednock, T. A., Butcher, E. C., Stoolman, L. M. & Rosen, S. D. (1987). Receptors involved in lymphocyte homing: relationship between a carbohydrate-binding receptor and the MEL-14 antigen. J. Cell Biol., 104, 725–31.CrossRefGoogle ScholarPubMed
Yeh, J. C., Hiraoka, N., Petryniak, B.et al. (2001). Novel sulfated lymphocyte homing receptors and their control by a Core 1 extension beta 1,3-N-acetylglucosaminyltransferase. Cell, 105, 957–69.CrossRefGoogle Scholar
Kirby, D. R. S. & Cowell, T. P. (1968). Trophoblast–host interaction. In Fleischmajer, R. and Billingham, R. E., eds., Epithelial–Mesenchymal Interactions. Baltimore: Williams & Wilkins, pp. 64–77.Google Scholar
Lindenberg, S., Hyttel, P., Sjogren, A. & Geve, T. (1989). A comparative study of attachment of human, bovine and mouse blastocysts to uterine epithelial monolayer. Hum. Reprod., 4, 446–56.CrossRefGoogle ScholarPubMed

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