Heparan sulfate proteoglycans and their binding proteins in embryo implantation and placentation

Carson, 2000, Embryo implantation, Dev Biol, 223, 217, 10.1006/dbio.2000.9767 Hacker, 2005, Heparan sulphate proteoglycans: the sweet side of development, Nat Rev, 6, 530, 10.1038/nrm1681 Carter, 2004, Comparative aspects of trophoblast development and placentation, Reprod Biol Endocrinol, 2, 46, 10.1186/1477-7827-2-46 Carter, 2007, Animal models of human placentation—a review, Placenta, 28, S41, 10.1016/j.placenta.2006.11.002 Beauvais, 2004, Syndecans in tumor cell adhesion and signaling, Reprod Biol Endocrinol, 2, 3, 10.1186/1477-7827-2-3 Jokimaa, 1998, Expression of syndecan-1 in human placenta and decidua, Placenta, 19, 157, 10.1016/S0143-4004(98)90004-2 Russo, 2001, In vivo regulation of syndecan-3 expression in the rat uterus by 17 beta-estradiol, J Biol Chem, 276, 686, 10.1074/jbc.M004106200 San Martin, 2004, Perlecan and syndecan-4 in uterine tissues during the early pregnancy in mice, Am J Reprod Immunol, 52, 53, 10.1111/j.1600-0897.2004.00182.x Hjelm Cluff, 2005, Normal labor associated with changes in uterine heparan sulfate proteoglycan expression and localization, Acta obstet gynecol Scand, 84, 217, 10.1111/j.0001-6349.2005.00484.x Crescimanno, 1999, Expression pattern alterations of syndecans and glypican-1 in normal and pathological trophoblast, J Pathol, 189, 600, 10.1002/(SICI)1096-9896(199912)189:4<600::AID-PATH440>3.0.CO;2-Q Sutherland, 1991, Expression of syndecan, a putative low affinity fibroblast growth factor receptor, in the early mouse embryo, Development (Cambridge, England), 113, 339, 10.1242/dev.113.1.339 Ishiguro, 2000, Syndecan-4 deficiency impairs the fetal vessels in the placental labyrinth, Dev Dyn, 219, 539, 10.1002/1097-0177(2000)9999:9999<::AID-DVDY1081>3.0.CO;2-K Khan, 2001, Glypican-3 (GPC3) expression in human placenta: localization to the differentiated syncytiotrophoblast, Histol Histopathol, 16, 71 Bix, 2005, Matrix revolutions: “tails” of basement-membrane components with angiostatic functions, Trends Cell Biol, 15, 52, 10.1016/j.tcb.2004.11.008 Pollheimer, 2004, Expression pattern of collagen XVIII and its cleavage product, the angiogenesis inhibitor endostatin, at the fetal–maternal interface, Placenta, 25, 770, 10.1016/j.placenta.2004.03.003 Nasu, 2003, Expression of collagen XVIII mRNA and protein in human umbilical vein and placenta, Reprod, Fertil Dev, 15, 107, 10.1071/RD02067 Rohde, 1998, Complementary expression of HIP, a cell-surface heparan sulfate binding protein, and perlecan at the human fetal–maternal interface, Biol Reprod, 58, 1075, 10.1095/biolreprod58.4.1075 Dziadek, 1985, Immunological characterization of basement membrane types of heparan sulfate proteoglycan, EMBO J, 4, 905, 10.1002/j.1460-2075.1985.tb03717.x Carson, 1993, Heparan sulfate proteoglycan (perlecan) expression by mouse embryos during acquisition of attachment competence, Dev Biol, 155, 97, 10.1006/dbio.1993.1010 Smith, 1997, Expression of heparan sulfate proteoglycan (perlecan) in the mouse blastocyst is regulated during normal and delayed implantation, Dev Biol, 184, 38, 10.1006/dbio.1997.8521 Forsberg, 2001, Heparan sulfate: lessons from knockout mice, J Clin Invest, 108, 175, 10.1172/JCI200113561 Costell, 1999, Perlecan maintains the integrity of cartilage and some basement membranes, J Cell Biol, 147, 1109, 10.1083/jcb.147.5.1109 Payer, 2003, Stella is a maternal effect gene required for normal early development in mice, Curr Biol, 13, 2110, 10.1016/j.cub.2003.11.026 Esko, 2002, Order out of chaos: assembly of ligand binding sites in heparan sulfate, Annu Rev Biochem, 71, 435, 10.1146/annurev.biochem.71.110601.135458 Tumova, 1997, The interaction between basic fibroblast growth factor and heparan sulfate can prevent the in vitro degradation of the glycosaminoglycan by Chinese hamster ovary cell heparanases, J Biol Chem, 272, 9078, 10.1074/jbc.272.14.9078 Harmer, 2006, Multimers of the fibroblast growth factor (FGF)-FGF receptor-saccharide complex are formed on long oligomers of heparin, Biochem J, 393, 741, 10.1042/BJ20050985 Bernfield, 1999, Functions of cell surface heparan sulfate proteoglycans, Annu Rev Biochem, 68, 729, 10.1146/annurev.biochem.68.1.729 Ashikari-Hada, 2004, Characterization of growth factor-binding structures in heparin/heparan sulfate using an octasaccharide library, J Biol Chem, 279, 12346, 10.1074/jbc.M313523200 Mahalingam, 2007, Cellular adhesion responses to the heparin-binding (HepII) domain of fibronectin require heparan sulfate with specific properties, J Biol Chem, 282, 3221, 10.1074/jbc.M604938200 Kirn-Safran, 2007, Global growth deficiencies in mice lacking the ribosomal protein HIP/RPL29, Dev Dyn, 236, 447, 10.1002/dvdy.21046 Hoke, 1998, Murine HIP/L29 is a heparin-binding protein with a restricted pattern of expression in adult tissues, J Biol Chem, 273, 25148, 10.1074/jbc.273.39.25148 Rohde, 1996, Cell surface expression of HIP, a novel heparin/heparan sulfate binding protein, of human uterine epithelial cells and cell lines, J Biol Chem, 271, 11824, 10.1074/jbc.271.20.11824 Liu, 1997, A heparin-binding synthetic peptide of heparin/heparan sulfate-interacting protein modulates blood coagulation activities, Proc Natl Acad Sci USA, 94, 1739, 10.1073/pnas.94.5.1739 Julian, 2001, Expression of heparin/heparan sulfate interacting protein/ribosomal protein l29 during the estrous cycle and early pregnancy in the mouse, Biol Reprod, 64, 1165, 10.1095/biolreprod64.4.1165 Bame, 2001, Heparanases: endoglycosidases that degrade heparan sulfate proteoglycans, Glycobiology, 11, 91R, 10.1093/glycob/11.6.91R Nakajima, 1984, Metastatic melanoma cell heparanase. Characterization of heparan sulfate degradation fragments produced by B16 melanoma endoglucuronidase, J Biol Chem, 259, 2283, 10.1016/S0021-9258(17)43350-3 Freeman, 1999, Evidence that platelet and tumour heparanases are similar enzymes, Biochem J, 342, 361, 10.1042/0264-6021:3420361 Sewell, 1989, Human mononuclear cells contain an endoglycosidase specific for heparan sulphate glycosaminoglycan demonstrable with the use of a specific solid-phase metabolically radiolabelled substrate, Biochem J, 264, 777, 10.1042/bj2640777 Laskov, 1991, Production of heparanase by normal and neoplastic murine B-lymphocytes, Int J Cancer, 47, 92, 10.1002/ijc.2910470117 Matzner, 1985, Degradation of heparan sulfate in the subendothelial extracellular matrix by a readily released heparanase from human neutrophils. Possible role in invasion through basement membranes, J Clin Invest, 76, 1306, 10.1172/JCI112104 Mollinedo, 1997, Major co-localization of the extracellular-matrix degradative enzymes heparanase and gelatinase in tertiary granules of human neutrophils, Biochem J, 327, 917, 10.1042/bj3270917 Levy-Adam, 2003, Heterodimer formation is essential for heparanase enzymatic activity, Biochem Biophys Res Commun, 308, 885, 10.1016/S0006-291X(03)01478-5 Miao, 2002, Cloning, expression, and purification of mouse heparanase, Protein Expr Purif, 26, 425, 10.1016/S1046-5928(02)00558-2 Goldshmidt, 2003, Heparanase mediates cell adhesion independent of its enzymatic activity, FASEB J, 17, 1015, 10.1096/fj.02-0773com Nasser, 2007, Cloning, expression, and characterization of an alternatively spliced variant of human heparanase, Biochem Biophys Res Commun, 354, 33, 10.1016/j.bbrc.2006.12.189 McKenzie, 2000, Cloning and expression profiling of Hpa2, a novel mammalian heparanase family member, Biochem Biophys Res Commun, 276, 1170, 10.1006/bbrc.2000.3586 Vlodavsky, 2001, Molecular properties and involvement of heparanase in cancer progression and normal development, Biochimie, 83, 831, 10.1016/S0300-9084(01)01318-9 Elkin, 2001, Heparanase as mediator of angiogenesis: mode of action, FASEB J, 15, 1661, 10.1096/fj.00-0895fje Gingis-Velitski, 2004, Heparanase induces endothelial cell migration via protein kinase B/Akt activation, J Biol Chem, 279, 23536, 10.1074/jbc.M400554200 Goshen, 1996, Purification and characterization of placental heparanase and its expression by cultured cytotrophoblasts, Mol Hum Reprod, 2, 679, 10.1093/molehr/2.9.679 Dempsey, 2000, Heparanase expression in invasive trophoblasts and acute vascular damage, Glycobiology, 10, 467, 10.1093/glycob/10.5.467 Kizaki, 2001, Expression of heparanase mRNA in bovine placenta during gestation, Reproduction, 121, 573, 10.1530/rep.0.1210573 Kizaki, 2003, Cloning and localization of heparanase in bovine placenta, Placenta, 24, 424, 10.1053/plac.2002.0909 Hasengaowa, 2006, Heparanase expression in both normal endometrium and endometrial cancer, Int J Gynecol Cancer, 16, 1401, 10.1111/j.1525-1438.2006.00614.x Xu, 2007, Estradiol induces heparanase-1 expression and heparan sulphate proteoglycan degradation in human endometrium, Hum Reprod, 22, 927, 10.1093/humrep/del483 Zcharia, 2004, Transgenic expression of mammalian heparanase uncovers physiological functions of heparan sulfate in tissue morphogenesis, vascularization, and feeding behavior, FASEB J, 18, 252, 10.1096/fj.03-0572com Revel, 2005, Heparanase improves mouse embryo implantation, Fertil Steril, 83, 580, 10.1016/j.fertnstert.2004.11.008 D'Souza, 2007, Heparanase expression and function during early pregnancy in mice, Biol Reprod, 10.1095/biolreprod.107.061317 Temkin, 2004, Eosinophil major basic protein: first identified natural heparanase-inhibiting protein, J Allergy Clin Immunol, 113, 703, 10.1016/j.jaci.2003.11.038 Plager, 2001, A novel human homolog of eosinophil major basic protein, Immunol Rev, 179, 192, 10.1034/j.1600-065X.2001.790119.x Giudice, 2002, Identification and regulation of the IGFBP-4 protease and its physiological inhibitor in human trophoblasts and endometrial stroma: evidence for paracrine regulation of IGF-II bioavailability in the placental bed during human implantation, J Clin Endocrinol Metabol, 87, 2359, 10.1210/jc.87.5.2359 Dhoot, 2001, Regulation of Wnt signaling and embryo patterning by an extracellular sulfatase, Science (New York, NY), 293, 1663, 10.1126/science.293.5535.1663 Morimoto-Tomita, 2002, Cloning and characterization of two extracellular heparin-degrading endosulfatases in mice and humans, J Biol Chem, 277, 49175, 10.1074/jbc.M205131200 Nagamine, 2005, Expression of a heparan sulfate remodeling enzyme, heparan sulfate 6-O-endosulfatase sulfatase FP2, in the rat nervous system, Brain Res Dev Brain Res, 159, 135, 10.1016/j.devbrainres.2005.07.006 Ohto, 2002, Identification of a novel nonlysosomal sulphatase expressed in the floor plate, choroid plexus and cartilage, Genes Cells, 7, 173, 10.1046/j.1356-9597.2001.00502.x Uchimura, 2006, HSulf-2, an extracellular endoglucosamine-6-sulfatase, selectively mobilizes heparin-bound growth factors and chemokines: effects on VEGF, FGF-1, and SDF-1, BMC Biochem, 7, 2, 10.1186/1471-2091-7-2 Ai, 2003, QSulf1 remodels the 6-O sulfation states of cell surface heparan sulfate proteoglycans to promote Wnt signaling, J Cell Biol, 162, 341, 10.1083/jcb.200212083 Lai, 2003, Loss of HSulf-1 up-regulates heparin-binding growth factor signaling in cancer, J Biol Chem, 278, 23107, 10.1074/jbc.M302203200 Lai, 2004, HSulf-1 modulates HGF-mediated tumor cell invasion and signaling in head and neck squamous carcinoma, Oncogene, 23, 1439, 10.1038/sj.onc.1207258 Viviano, 2004, Domain-specific modification of heparan sulfate by Qsulf1 modulates the binding of the bone morphogenetic protein antagonist Noggin, J Biol Chem, 279, 5604, 10.1074/jbc.M310691200 Wang, 2004, QSulf1, a heparan sulfate 6-O-endosulfatase, inhibits fibroblast growth factor signaling in mesoderm induction and angiogenesis, Proc Natl Acad Sci USA, 101, 4833, 10.1073/pnas.0401028101 Lum, 2007, Gene trap disruption of the mouse heparan sulfate 6-o-endosulfatase gene. Sulf2, Mol Cell Biol, 27, 678, 10.1128/MCB.01279-06 Raab, 1996, Mouse preimplantation blastocysts adhere to cells expressing the transmembrane form of heparin-binding EGF-like growth factor, Development (Cambridge, England), 122, 637, 10.1242/dev.122.2.637 Leach, 2004, Heparin-binding EGF-like growth factor regulates human extravillous cytotrophoblast development during conversion to the invasive phenotype, Dev Biol, 266, 223, 10.1016/j.ydbio.2003.09.026 Patel, 2000, A role for hepatocyte growth factor during early postimplantation growth of the placental lineage in mice, Biol Reprod, 62, 904, 10.1095/biolreprod62.4.904 Muhlhauser, 1996, Codistribution of basic fibroblast growth factor and heparan sulfate proteoglycan in the growth zones of the human placenta, Cell Tiss Res, 285, 101, 10.1007/s004410050625 Anteby, 2005, Fibroblast growth factor-10 and fibroblast growth factor receptors 1–4: expression and peptide localization in human decidua and placenta, Eur J Obstet Gynecol Reprod Biol, 119, 27, 10.1016/j.ejogrb.2004.05.014 Demir, 2006, Sequential steps during vasculogenesis and angiogenesis in the very early human placenta, Placenta, 27, 535, 10.1016/j.placenta.2005.05.011 Paria, 2001, Cellular and molecular responses of the uterus to embryo implantation can be elicited by locally applied growth factors, Proc Natl Acad Sci USA, 98, 1047, 10.1073/pnas.98.3.1047 Pfendler, 2000, Nodal and bone morphogenetic protein 5 interact in murine mesoderm formation and implantation, Genesis, 28, 1, 10.1002/1526-968X(200009)28:1<1::AID-GENE10>3.0.CO;2-X Cross, 2006, Branching morphogenesis during development of placental villi, Differ Res Biol Divers, 74, 393, 10.1111/j.1432-0436.2006.00103.x Fan, 2000, Distinct expression of midkine and pleiotrophin in the spinal cord and placental tissues during early mouse development, Dev Growth Differ, 42, 113, 10.1046/j.1440-169x.2000.00497.x Miner, 2004, Compositional and structural requirements for laminin and basement membranes during mouse embryo implantation and gastrulation, Development (Cambridge, England), 131, 2247, 10.1242/dev.01112 Scheele, 2005, Laminin alpha1 globular domains 4-5 induce fetal development but are not vital for embryonic basement membrane assembly, Proc Natl Acad Sci USA, 102, 1502, 10.1073/pnas.0405095102 Kayisli, 2005, Expression of integrin alpha5 and integrin beta4 and their extracellular ligands fibronectin and laminin in human decidua during early pregnancy and its sex steroid-mediated regulation, Acta Histochem, 107, 173, 10.1016/j.acthis.2005.01.005 Rider, 1992, Uterine fibronectin mRNA content and localization are modulated during implantation, Dev Dyn, 195, 1, 10.1002/aja.1001950102 Schultz, 1997, Integrin trafficking regulates adhesion to fibronectin during differentiation of mouse peri-implantation blastocysts, Dev Genet, 21, 31, 10.1002/(SICI)1520-6408(1997)21:1<31::AID-DVG4>3.0.CO;2-9 Lessey, 2002, Integrins and implantation in the human, Rev Endocr Metab Disord, 3, 107, 10.1023/A:1015450727580 Genbacev, 2003, Trophoblast L-selectin-mediated adhesion at the maternal-fetal interface, Science (New York, NY), 299, 405, 10.1126/science.1079546 Prakobphol, 2006, A role for the L-selectin adhesion system in mediating cytotrophoblast emigration from the placenta, Dev Biol, 298, 107, 10.1016/j.ydbio.2006.06.020 Mo, 2002, CYR61 (CCN1) is essential for placental development and vascular integrity, Mol Cell Biol, 22, 8709, 10.1128/MCB.22.24.8709-8720.2002