In Vitro Tests for Detecting Chemicals Affecting the Embryo Implantation Process

Anon. (1994). ECVAM News & Views. ATLA 22, 7–11.

Bremer S. , Balduzzi D. , Cortvrindt R. , Daston G. , Eletti B. , Galli A. , Huhtaniemi I. , Laws S. , Lazzari G. , Liminga U. , Smitz J. , Spano M. , Themmen A. , Tilloy A. , & Waalkens-Behrends I. (2005). The effects of chemicals on mammalian fertility. The Report and Recommendations of ECVAM Workshop 53 — the First Strategic Workshop of the EU ReProTect Project. ATLA 33, 391–416.

Hartung T. , Bremer S. , Casati S. , Coecke S. , Corvi R. , Fortaner S. , Gribaldo L. , Halder M. , Hoffmann S. , Janusch Roi A. , Prieto P. , Sabbioni E. , Scott L. , Worth A. , & Zuang V. (2004). A modular approach to the ECVAM principles on test validity. ATLA 32, 467–472.

Enders A.C. , & Schlafke S. (1969). Cytological aspects of trophoblast–uterine interaction in early implantation. American Journal of Anatomy 125, 1–29.

Cross J.C. , Werb Z. , Fisher S.J. (1994). Implantation and the placenta: key pieces of the development puzzle. Science, New York 266, 1508–1518.

Hareng L. , Pellizzer C. , Bremer S. , Schwarz M. , & Hartung T. (2005). The Integrated Project ReProTect: A novel approach in reproductive toxicity hazard assessment. Reproductive Toxicology 20, 441–452.

Hoar R.M. (1986). Effects of the environment upon fetal development: concepts and design. Biology of Reproduction 34, 1–4.

Carney W. , Scialli A.R. , Watson R. , & DeSesso J. (2004). Mechanisms regulating toxicant disposition to the embryo during early pregnancy: An inter-species comparison. Birth Defects Research Part C: Embryo Today: Reviews 72, 345–360.

Renfree M.B. (1982). Implantation and placentation. In Reproduction in Mammals (ed. Austin C.R. , & Short R.V. ), pp. 20–26. Cambridge, UK: Cambridge University Press.

Kaufmann P. , & Burton G. (1994). Anatomy and genesis of the placenta. In The Physiology of Reproduction, 2nd edn (ed. Knobil E. , & Neill J.D. ), pp. 441–484. New York, NY, USA: Raven Press.

Holson J.F. , Stump D.G. , Pearce L.B. , Watson R.E. , & DeSesso J.M. (2005). Mode of action: yolk sac poisoning and impeded histiotrophic nutrition — HBOC-related congenital malformations. Critical Reviews in Toxicology 35, 739–745.

Novotna M. , Libra A. , Kopecky M. , Pavek P. , Fendrich Z. , Semecky V. , & Staud F. (2004). P–glycoprotein expression and distribution in the rat placenta during pregnancy. Reproductive Toxicology 18, 785–792.

Sun M. , Kingdom J. , Baczyk D. , Lye S.J. , Matthews S.G. , & Gibb W. (2006). Expression of the multidrug resistance P–glycoprotein, (ABCB1 glycoprotein) in the human placenta decreases with advancing gestation. Placenta 27, 602–609.

Bonnet R. (1884). Beitrage zur embryologie der wiederkauer, gewonnen am schafei. Archiv für pathologische Anatomie und Physiologie 8, 170–230.

Schlafke S. , & Enders A.C. (1975). Cellular basis of interaction between trophoblast and uterus at implantation. Biology of Reproduction 12, 41–65.

Carson D.D. , Bagchi I. , Dey S.K. , Enders A.C. , Fazleabas A.T. , Lessey B.A. , & Yoshinaga K. (2000). Embryo implantation. Developmental Biology 223, 217–237.

Dey S.K. (1996). Implantation. In Reproductive Endocrinology, Surgery and Technology (ed. Adashi E.Y. , Rock J.A. , & Rosenwaks Z. ), pp. 421–434. New York, NY, USA: Lippincott-Raven.

Paria B.C. , Huet H. , & Dey S.K. (1993). Blastocyst's state of activity determines the “window” of implantation in the receptive mouse uterus. Proceedings of the National Academy of Sciences, USA 90, 10159–10162.

Heap R.B. , Flint A.P. , Hartmann P.E. , Gadsby J.E. , Staples L.D. , Ackland N. , & Hamon M. (1981). Oestrogen production in early pregnancy. Journal of Endocrinology 89, 77–94.

Stromstedt M. , Keeney D.S. , Waterman M.R. , Paria B.C. , Conley A.J. , & Dey S.K. (1996). Pre-implantation mouse blastocysts fail to express CYP genes required for estrogen biosynthesis. Molecular Reproduction and Development 43, 428–436.

Dey S. , Lim H. , Das S. , Reese J. , Paria B. , Daikoku T. , & Wang H. (2004). Molecular cues to implantation. Endocrine Reviews 25, 341–373.

Gottmann E. , Kramer S. , Pfahringer B. , & Helma C. (2001). Data quality in predictive toxicology: reproducibility of rodent carcinogenicity. Environmental Health Perspectives 109, 509–511.

Langley G. (2005). Endocrine Disrupting Chemicals. A Non-animal Testing Approach. A BUAV Report Commissioned by Dr Caroline Lucas, Green Party MEP for the South East of England. 20 pp. Website http://www.eceae.org/pdf/ECEAE_Endocrine_Disrupting_Chem_Final.pdf (Accessed 22.10.06).

Ingelman-Sundberg M. (2001). Genetic variability in susceptibility and response to toxicants. Toxicology Letters 120, 259–268.

Knudsen L.E. , Loft S.H. , & Autrup H. (2001). Risk assessment. The importance of genetic polymorphisms in man. Mutation Research 282, 83–88.

Gentry P.R. , Hack C.E. , Haber L. , Maier A. , & Clewell H.J. (2002). An approach for the quantitative consideration of genetic polymorphism data in chemical risk assessment: examples with warfarin and parathion. Toxicological Sciences 70, 120–139.

Stavreus-Evers A. , Nikas G. , Eriksson H. , Sahlin L. , & Landgren B.M. (2001). Formation of pinopodes in human endometrium is associated with the concentration of progesterone and progesterone receptors. Fertility and Sterility 78, 782–791.

Subcommittee on Reproductive and Neurodevelopmental Toxicology, Committee on Biologic Markers, Board on Environmental Studies and Toxicology, National Research Council (1989). Biologic Markers. In Reproductive Toxicology, Free Executive Summary, pp. 1–14. Washington D.C., USA: The National Academies Press. Website http://www.nap.edu/catalog/774.html (Accessed 03.11.06).

Kimber S.J. , & Spanswick C. (2000). Blastocyst implantation: the adhesion cascade. Seminars in Cell & Developmental Biology 11, 77–92.

Meseguer M. , Aplin J.D. , Caballero C. , Connor J.E. , Martin J.C. , Remohi J. , Pellicer A. , & Simon C. (2001). Human endometrial mucin MUC1 is up-regulated by progesterone and down-regulated in vitro by the human blastocyst. Biology of Reproduction 64, 590–601.

Fukuda M.N. , Sato T. , Nakayama J. , Klier G. , Mikami M. , Aoki D. , & Nozawa S. (1995). Trophinin and tastin, a novel cell adhesion molecule complex with potential involvement in embryo implantation. Genes & Development 9, 1199–1210.

Suzuki N. , Nakayama J. , Shih I.M. , Aoki D. , Nozawa S. , & Fukuda M.N. (1999). Expression of trophinin, tastin, and bystin by trophoblast and endometrial cells in human placenta. Biology of Reproduction 60, 621–627.

Aghajanova L. , Stavreus-Evers A. , Nikas G. , Landgren B.M. , & Hovatta O. (2003). Coexpression of pinopodes and leukemia inhibitory factor, as well as its receptor, in human endometrium. Fertility and Sterility 79, 808–814.

Paria B.C. , Zhao X. , Das S.K. , Dey S.K. , & Yoshinaga K. (1999). Zonula occludens-1 and E-cadherin are co-ordinately expressed in the mouse uterus with the initiation of implantation and decidualization. Developmental Biology 208, 488–501.

Riethmacher D. , Brinkmann V. , & Birchmeier C. (1995). A targeted mutation in the mouse E-cadherin gene results in defective preimplantation development. Proceedings of the National Academy of Sciences, USA 92, 855–859.

Genbacev O.D. , Prakobphol A. , Foulk R.A. , Krtolica A. , Ilic D. , Singer M.S. , Yang Z. , Kiessling L. , Rosen S.D. , & Fisher S.J. (2003). Trophoblast L-selectin-mediated adhesion at the maternal–foetal interface. Science, New York 299, 405–408.

Kumar S. , Zhu L.J. , Polihronis M. , Cameron S.T. , Baird D.T. , Schatz F. , Dua A. , Ying Y.K. , Bagchi M.K. , & Bagchi I.C. (1998). Progesterone induces calcitonin gene expression in human endometrium within the putative window of implantation. Journal of Clinical Endocrinology and Metabolism 83, 4443–4450.

Sharkey A.M. , & Smith S.K. (2003). The endometrium as a cause of implantation failure. Best practice & research. Clinical Obstetrics & Gynaecology 17, 289–307.

Makrigiannakis A. , Zoumakis E. , Kalantaridou S. , & Chrousos G. (2004). Endometrial and placental CRH as regulators of human embryo implantation. Journal of Reproductive Immunology 62, 53–59.

Minas V. , Loutradis D. , & Makrigiannakis A. (2004). Factors controlling blastocyst implantation. Reproductive BioMedicine Online 10, 205–216.

Kimber S.J. (2005). Leukaemia inhibitory factor in implantation and uterine biology. Reproduction 130, 131–145.

Jabbour H.N. , Kelly R.W. , Fraser H.M. , & Critchley H.D. (2006). Endocrine regulation of menstruation. Endocrine Reviews 27, 17–46.

Padilla L. , Reinicke K. , Montesino H. , Villena F. , Asencio H. , Cruz M. , & Rudolph M.I. (1990). Histamine content and mast cells distribution in mouse uterus: the effect of sexual hormones, gestation and labor. Cell and Molecular Biology 36, 93–100.

Chakraborty I. , Das S.K. , Wang J. , & Dey S.K. (1996). Developmental expression of the cyclo-oxy-genase-1 and cyclo-oxygenase-2 genes in the periimplantation mouse uterus and their differential regulation by the blastocyst and ovarian steroids. Journal of Molecular Endocrinology 16, 107–122.

Charpigny G. , Reinaud P. , Tamby J.P. , Creminon C. , & Guillomot M. (1997). Cyclooxygenase-2 unlike cyclooxygenase-1 is highly expressed in ovine embryos during the implantation period. Biology of Reproduction 57, 1032–1040.

Das S.K. , Wang J. , Dey S.K. , & Mead R.A. (1999). Spatiotemporal expression of cyclooxygenase 1 and cyclooxygenase 2 during delayed implantation and the periimplantation period in the Western spotted skunk. Biology of Reproduction 60, 893–899.

Song J.H. , Sirois J. , Houde A. , & Murphy B.D. (1998). Cloning, developmental expression, and immunohistochemistry of cyclooxygenase 2 in the endometrium during embryo implantation and gestation in the mink (Mustela vison). Endocrinology 139, 3629–3636.

Kim J. , Wang J. , Bambra C. , Das S.K. , Dey S.K. , & Fazleabas A.T. (1999). Expression of cyclooxygenase-1 and -2 in the baboon endometrium during the menstrual cycle and pregnancy. Endocrinology 140, 2672–2678.

Critchley H.O. , Jones R.L. , Lea R.G. , Drudy T.A. , Kelly R.W. , Williams A.R. , & Baird D.T. (1999). Role of inflammatory mediators in human endometrium during progesterone withdrawal and early pregnancy. Journal of Clinical Endocrinology & Metabolism 84, 240–248.

Marions L. , & Danielsson K.G. (1999). Expression of cyclo-oxygenase in human endometrium during the implantation period. Molecular Human Reproduction 5, 961–965.

Spaziani E. (1963). Relationship between early vascular responses and growth in the rat uterus: stimulation of cell division by estradiol and vasodilating amines. Endocrinology 72, 180–188.

Dey S.K. , Villanueva C. , Chien S.M. , & Crist R.D. (1978). The role of histamine in implantation in the rabbit. Journal of Reproduction and Fertility 53, 23–26.

Paria B.C. , Reese J. , Das S.K. , & Dey S.K. (2002). Deciphering the cross-talk of implantation: advances and challenges. Science, New York 296, 2185–2218.

Lim H. , Song H. , Paria B.C. , Reese J. , Das S.K. , & Dey S.K. (2002). Molecules in blastocyst implantation: uterine and embryonic perspectives. Vitamins and Hormones 64, 43–76.

Tazuke S.I. , & Giudice L.C. (1996). Growth factors and cytokines in endometrium, embryonic development, and maternal: embryonic interactions. Seminars in Reproductive Endocrinology 14, 231–245.

Martin K.L. , Barlow D.H. , & Sargent I.L. (1998). Heparin-binding epidermal growth factor significantly improves human blastocyst development and hatching in serum-free medium. Human Reproduction 13, 1645–1652.

Chard T. (1995). Cytokines in implantation. Human Reproduction Update 1, 385–396.

Stewart C.L. , Kaspar P. , Brunet L.J. , Bhatt H. , Gadi I. , Kontgen F. , & Abbondanzo S.J. (1992). Blastocyst implantation depends on maternal expression of leukaemia inhibitory factor. Nature, London 359, 76–79.

Harvey M.B. , Leco K.J. , Arcellana P. , Zhang X. , Edwards D.R. , & Schultz G.A. (1995). Roles of growth factors during peri-implantation development. Human Reproduction 10, 712–718.

Rappolee D.A. , Brenner C.A. , Schultz R. , Mark D. , & Werb Z. (1988). Developmental expression of PDGF, TGF-alpha, and TGF-beta genes in preimplantation mouse embryos. Science, New York 241, 1823–1825.

Wang H. , Xie H. , & Dey S.K. (2006). Endocannabinoid signalling directs periimplantation events. American Association of Pharmaceutical Scientists — AAPS Journal 8, 425–432.

Guo Y. , Wang H. , Okamoto Y. , Ueda N. , Kingsley P.J. , Marnett L.J. , Schmid H.H. , Das S.K. , & Dey S.K. (2005). N-acylphosphatidylethanolamine-hydrolyzing phospholipase D is an important determinant of uterine anandamide levels during implantation. Journal of Biological Chemistry 280, 23429–23432.

Audus K.L. (1999). Controlling drug delivery across the placenta. European Journal of Pharmaceutical Sciences 8, 161–165.

Pacifici G.M. , & Nottoli R. (1995). Placental transfer of drugs administered to the mother. Clinical Pharmacokinetics 28, 235–269.

Schinkel A.H. , & Jonker J.W. (2003). Mammalian drug efflux transporters of the ATP binding cassette (ABC) family: an overview. Advanced Drug Delivery Reviews 55, 3–29.

Mizuno N. , Niwa T. , Yotsumoto Y. , & Sugiyama Y. (2003). Impact of drug transporter studies on drug discovery and development. Pharmacological Reviews 55, 425–461.

Leslie E.M. , Deeley R.G. , & Cole S.P. (2005). Multidrug resistance proteins: role of P–glycoprotein, MRP1, MRP2, and BCRP (ABCG2) in tissue defence. Toxicology and Applied Pharmacology 204, 216–237.

Ceckova-Novotna M. , Pavek P. , & Staud F. (2006). P–glycoprotein in the placenta: expression, localization, regulation and function. Reproductive Toxicology 22, 400–410.

Cordon-Cardo C. , O'Brien J.P. , Casals D. , Rittman-Grauer L. , Biedler J.L. , Melamed M.R. , & Bertino J.R. (1989). Multidrug-resistance gene (P–glycoprotein) is expressed by endothelial cells at blood–brain barrier sites. Proceedings of the National Academy of Sciences, USA 86, 695–698.

Bremer S. , Hoof T. , Wilke M. , Busche R. , Scholte B. , Riordan J.R. , Maass G. , & Tummler B. (1992). Quantitative expression patterns of multidrug-resistance P–glycoprotein (MDR1) and differentially spliced cystic-fibrosis transmembrane-conductance regulator mRNA transcripts in human epithelia. European Journal of Biochemistry 206, 137–149.

Nakamura Y. , Ikeda S. , Furukawa T. , Sumizawa T. , Tani A. , Akiyama S. , & Nagata Y. (1997). Function of P–glycoprotein expressed in placenta and mole. Biochemical and Biophysical Research Communications 235, 849–853.

Ushigome F. , Takanaga H. , Matsuo H. , Yanai S. , Tsukimori K. , Nakano H. , Uchiumi T. , Nakamura T. , Kuwano M. , Ohtani H. , & Sawada Y. (2000). Human placental transport of vinblastine, vincristine, digoxin and progesterone: contribution of P–glycoprotein. European Journal of Pharmaceutical Sciences 408, 1–10.

Utoguchi N. , Chandorkar G.A. , Avery M. , & Audus K.L. (2000). Functional expression of P–glycoprotein in primary cultures of human cytotrophoblasts and BeWo cells. Reproductive Toxicology 14, 217–224.

Lankas G.R. , Wise L.D. , Cartwright M.E. , Pippert T. , & Umbenhauer D.R. (1998). Placental P–glycoprotein deficiency enhances susceptibility to chemically induced birth defects in mice. Reproductive Toxicology 12, 457–463.

Pavek P. , Fendrich Z. , Staud F. , Malakova J. , Brozmanova H. , Laznicek M. , Semecky V. , Grundmann M. , & Palicka V. (2001). Influence of P–glycoprotein on the transplacental passage of cyclosporine. Journal of Pharmaceutical Sciences 90, 1583–1592.

Pavek P. , Staud F. , Fendrich Z. , Slenarova H. , Libra A. , Novotna M. , Kopecky M. , Nobilis M. , & Semecky V. (2003). Examination of the functional activity of P–glycoprotein in the rat placental barrier using rhodamine 123. Journal of Pharmacology and Experimental Therapeutics 305, 1239–1250.

Molsa M. , Heikkinen T. , Hakkola J. , Hakala K. , Wallerman O. , Wadelius M. , Wadelius C. , & Laine K. (2005). Functional role of P–glycoprotein in the human blood–placental barrier. Journal of Pharmacology and Experimental Therapeutics 78, 123–131.

Nanovskaya T. , Nekhayeva I. , Karunaratne N. , Audus K. , Hankins G.D. , & Ahmed M.S. (2005). Role of P–glycoprotein in transplacental transfer of methadone. Biochemical Pharmacology 69, 1869–1878.

Sudhakaran S. , Ghabrial H. , Nation R.L. , Kong D.C. , Gude N.M. , Angus P.W. , & Rayner C.R. (2005). Differential bidirectional transfer of indinavir in the isolated perfused human placenta. Antimicrobial Agents and Chemotherapy 49, 1023–1028.

Allikmets R. , Schriml L.M. , Hutchinson A. , Romano-Spica V. , & Dean M. (1998). A human placenta-specific ATP-binding cassette gene (ABCP) on chromosome 4q22 that is involved in multidrug resistance. Cancer Research 58, 5337–5339.

Litman T. , Jensen U. , Hansen A. , Covitz K.M. , Zhan Z. , Fetsch P. , Abati A. , Hansen P.R. , Horn T. , Skovsgaard T. , & Bates S.E. (2002). Use of peptide antibodies to probe for the mitoxantrone resistance-associated protein MXR/BCRP/ABCP/ABCG2. Biochimica et Biophysica Acta 1565, 6–16.

Maliepaard M. , Scheffer G.L. , Faneyte I.F. , van Gastelen M.A. , Pijnenborg A.C. , Schinkel A.H. , van De Vijver M.J. , Scheper R.J. , & Schellens J.H. (2001). Subcellular localization and distribution of the breast cancer resistance protein transporter in normal human tissues. Cancer Research 61, 3458–3464.

Jonker J.W. , Buitelaar M. , Wagenaar E. , Van Der Valk M.A. , Scheffer G.L. , Scheper R.J. , Plosch T. , Kuipers F. , Elferink R.P. , Rosing H. , Beijnen J.H. , & Schinkel A.H. (2002). The breast cancer resistance protein protects against a major chlorophyll-derived dietary phototoxin and protoporphyria. Proceedings of the National Academy of Sciences, USA 99, 15649–15654.

Jonker J.W. , Smit J.W. , Brinkhuis R.F. , Maliepaard M. , Beijnen J.H. , Schellens J.H. , & Schinkel A.H. (2000). Role of breast cancer resistance protein in the bioavailability and foetal penetration of topotecan. Journal of the National Cancer Institute 92, 1651–1656.

Kolwankar D. , Glover D.D. , Ware J.A. , & Tracy T.S. (2005). Expression and function of ABCB1 and ABCG2 in human placental tissue. Drug Metabolism and Disposition: The Biological Fate of Chemicals 33, 524–529.

Ceckova M. , Libra A. , Pavek P. , Nachtigal P. , Brabec M. , Fuchs R. , & Staud F. (2006). Expression and functional activity of breast cancer resistance protein (bcrp, abcg2) transporter in the human choriocarcinoma cell line BeWo. Clinical and Experimental Pharmacology & Physiology 33, 58–65.

Staud F. , Vackova Z. , Pospechova K. , Pavek P. , Ceckova M. , Libra A. , Cygalova L. , Nachtigal P. , & Fendrich Z. (2006). Expression and transport activity of breast cancer resistance protein (Bcrp/Abcg2) in dually perfused rat placenta and HRP-1 cell line. Journal of Pharmacology and Experimental Therapeutics 319, 53–62.

Borst P. , Evers R. , Kool M. , & Wijnholds J. (1999). The multidrug resistance protein family. Biochimica et Biophysica Acta 1461, 347–357.

Bodo A. , Bakos E. , Szeri F. , Varadi A. , & Sarkadi B. (2003). The role of multidrug transporters in drug availability, metabolism and toxicity. Toxicology Letters 140, 133–143.

Kruh G.D. , & Belinsky M.G. (2003). The MRP family of drug efflux pumps. Oncogene 22, 7537–7552.

Haimeur A. , Conseil G. , Deeley R.G. , & Cole S.P. (2004). The MRP-related and BCRP/ABCG2 multidrug resistance proteins: biology, substrate specificity and regulation. Current Drug Metabolism 5, 21–53.

Langmann T. , Mauerer R. , Zahn A. , Moehle C. , Probst M. , Stremmel W. , & Schmitz G. (2003). Real-time reverse transcription-PCR expression profiling of the complete human ATP-binding cassette transporter superfamily in various tissues. Clinical Chemistry 49, 230–238.

Leazer T.M. , & Klaassen C.D. (2003). The presence of xenobiotic transporters in rat placenta. Drug Metabolism and Disposition: The Biological Fate of Chemicals 31, 153–167.

Nagashige M. , Ushigome F. , Koyabu N. , Hirata K. , Kawabuci M. , Hirakawa T. , Satoh S. , Tsukimori K. , Nakano H. , Uchiumi T. , Kuwano M. , Ohtani H. , & Sawada Y. (2003). Basal membrane localization of MRP1 in human placental trophoblast. Placenta 24, 951–958.

Atkinson D.E. , Greenwood S.L. , Sibley C.P. , Glazier J.D. , & Fairbairn L.J. (2003). Role of MDR1 and MRP1 in trophoblast cells, elucidated using retroviral gene transfer. American Journal of Physiology — Cell Physiology 285, 584–591.

St-Pierre M.V. , Serrano M.A. , Macias R.I. , Dubs U. , Hoechli M. , Lauper U. , Meier P.J. , & Marin J.J. (2000). Expression of members of the multidrug resistance protein family in human term placenta. American Journal of Physiology — Regulatory, Integrative and Comparative Physiology 279, 1495–1503.

Meyer Z. , Schwabedissen H.E. , Grube M. , Heydrich B. , Linnemann K. , Fusch C. , Kroemer H.K. , & Jedlitschky G. (2005). Expression, localization, and function of MRP5 (ABCC5), a transporter for cyclic nucleotides, in human placenta and cultured human trophoblasts: effects of gestational age and cellular differentiation. American Journal of Pathology 166, 39–48.

Pasanen M. (1999). The expression and regulation of drug metabolism in human placenta. Advanced Drug Delivery Reviews 38, 81–97.

Staud F. , Mazancova K. , Miksik I. , Pavek P. , Fendrich Z. , & Pacha J. (2006). Corticosterone transfer and metabolism in the dually perfused rat placenta: effect of 11beta-hydroxysteroid dehydrogenase type 2. Placenta 27, 171–180.

Sharma M. , Shubert D.E. , Sharma M. , Lewis J. , McGarrigle B.P. , Bofinger D.P. , & Olson J.R. (2003). Biotransformation of tamoxifen in a human endometrial explant culture model. Chemico– Biological Interactions 146, 237–249.

Kim S.Y. , Suzuki N. , Laxmi Y.R. , & Shibutani S. (2004). Genotoxic mechanism of tamoxifen in developing endometrial cancer. Drug Metabolism Reviews 36, 199–218.

Hukkanen J. , Mantyla M. , Kangas L. , Wirta P. , Hakkola J. , Paakki P. , Evisalmi S. , Pelkonen O. , & Raunio H. (1998). Expression of cytochrome P450 genes encoding enzymes active in the metabolism of tamoxifen in human uterine endometrium. Pharmacology & Toxicology 82, 93–97.

Nebert D.W. , Dalton T.P. , Okey A.B. , & Gonzalez F.J. (2004). Role of aryl hydrocarbon receptor-mediated induction of the CYP1 enzymes in environmental toxicity and cancer. Journal of Biological Chemistry 279, 23847–23850.

Igarashi T. , Osuga U. , Tsutsumi O. , Momoeda M. , Ando K. , Matsumi H. , Takai Y. , Okagaki R. , Hiroi H. , Fujiwara O. , Yano T. , & Taketani Y. (1999). Expression of Ah receptor and dioxin-related genes in human uterine endometrium in women with or without endometriosis. Endocrine Journal 46, 765–772.

Bofinger D.P. , Feng L. , Chi L.H. , Love J. , Stephen F.D. , Sutter T.R. , Osteen K.G. , Costich T.G. , Batt R.E. , Koury S.T.M. , & Olson J.R. (2001). Effect of TCDD exposure on CYP1A1 and CYP1B1 expression in explant cultures of human endometrium. Toxicological Science 62, 299–314.

Vadlamuri S.V. , Glover D.D. , Turner T. , & Sarkar M.A. (1998). Regiospecific expression of cytochrome P4501A1 and 1B1 in human uterine tissue. Cancer Letters 122, 143–150.

Kikkawa F. , Nawa A. , Oguchi H. , Kawai M. , Maeda O. , Suganuma N. , Aoyama T. , & Tomoda Y. (1994). Positive correlation between cytochrome P450 2E1 mRNA level and serum estradiol level in human uterine endometrium. Oncology 51, 52–58.

Sarkar M.A. , Vadlamuri V. , Ghosh S. , & Glover D.D. (2003). Expression and cyclic variability of CYP3A4 and CYP3A7 isoforms in human endometrium and cervix during the menstrual cycle. Drug Metabolism and Disposition: The Biological Fate of Chemicals 31, 1–6.

Garzon P. , Navarro-Ruiz A. , Garcia-Estrada J. , & Gallegos A. (1989). Steroid conjugate formed by human endometrium. Archivos de Investigacion Medica 20, 113–122.

Lepine J. , Bernard O. , Plante M. , Tetu B. , Pelletier G. , Labrie F. , Belanger A. , & Guillemette C. (2004). Specificity and regioselectivity of the conjugation of estradiol, estrone, and their catecholestrogen and methoxyestrogen metabolites by human uridine diphospho-glucuronosyltransferases expressed in endometrium. Journal of Clinical Endocrinology and Metabolism 89, 5222–5232.

Falany J.L. , Azziz R. , & Falany C.N. (1998). Identification and characterization of cytosolic sulfotransferases in normal human endometrium. Chemico–Biological Interactions 109, 329–339.

Rubin G.L. , Harrold A.J. , Mills J.A. , Falany C.N. , & Coughtrie M.W. (1999). Regulation of sulphotransferase expression in the endometrium during the menstrual cycle, by oral contraceptives and during early pregnancy. Molecular Human Reproduction 5, 995–1002.

Wolffe A.P. , & Tata J.R. (1984). Primary culture, cellular stress and differentiated function. FEBS Letters 176, 8–15.

Valbuena D. , Martin J. , de Pablo J.L. , Remohi J. , Pellecier A. , & Simon C. (2001). Increasing levels of estradiol are deleterious to embryonic implantation because they directly affect the embryo. Fertility and Sterility 76, 962–968.

Iwase A. , Ando H. , Nagasaka T. , Shibata D. , Harata T. , Shimomura Y. , Goto M. , & Kikkawa F. (2006). Neutral endopeptidase expressed by decidualized stromal cells suppresses phosphorylation and deoxyribonucleic acid synthesis induced by endothelin-1 in human endometrium. Endocrinology 147, 5153–5159.

Rinehart C.A. , Laundon C.H. , Mayben J.P. , Lyn-Cook B.D. , & Kaufman D.G. (1993). Conditional immortalization of human endometrial stromal cells with a temperature-sensitive simian virus 40. Carcinogenesis 14, 993–999.

Krikun G. , Mar G. , Alvaro A. , Guller S. , Schatz F. , Sapi E. , Rahman M. , Caze R. , Qumsiyeh M. , & Lockwood C.J. (2004). A novel immortalized human endometrial stromal cell line with normal progestational response. Endocrinology 145, 2291–2296.

Wooenhaupt K. , Jonas L. , Tiemann U. , & Tornek W. (2004). Influence of the mycotoxins alpha and beta-zearealenol (ZOL) on regulators of cap-dependent translation control in pig endometrial cells. Reproductive Toxicology 19, 189–199.

Bentin-Ley U. , Pedersen B. , Lindenberg S. , Larsen J.F. , Hamberger L. , & Horn T. (1994). Isolation and culture of human endometrial cells in a three-dimensional culture system. Journal of Reproduction and Fertility 101, 327–332.

Petersen A. , Bentin-Ley U. , Ravn V. , Ovortrup K. , Sørensen S. , Islin H. , Sjögren A. , Mosselmann S. , & Hamberger L. (2005). The antiprogesterone Org 31710 inhibits human blastocyst–endometrial interactions in vitro. Fertility and Sterility 83, 1255–1263.

Arnold J.T. , Kaufman D.G. , Seppala M. , & Lessey B.A. (2001). Endometrial stromal cells regulate epithelial cell growth in vitro: a new co-culture model. Human Reproduction 16, 836–845.

Classen-Linke I. , Alfer J. , Krusche C.A. , Chwalisz K. , Rath W. , & Beier H.M. (2000). Progestins, progesterone receptor modulators, and progesterone antagonists change VEGF release of endometrial cells in culture. Steroids 65, 763–771.

Yang H. , Han S. , Kim H. , Choi Y.M. , Hwang K.J. , Kwo H.C. , Kim S.K. , & Cho D.J. (2002). Expression of integrins, cyclooxygenases and matrix metalloproteinases in three-dimensional human endometrial cell culture system. Experimental & Molecular Medicine 34, 75–82.

Landgren B.M. , Hamberger L. , Johannisson E. , Eriksson H. , & Stavreus-Evers A. (1996). A new method to study the process of implantation of a human blastocyst in vitro. Fertility and Sterility 65, 1067–1070.

Staphreus-Evers A. , Hovatta O. , Eriksson H. , Landgren B.M. (2003). Development and characterization of an endometrial tissue culture system. Reproductive BioMedicine Online 7, 243–249.

Fasciani A. , Bocci G. , Xu J. , Bielecki R. , Greenblatt E. , Leyland N. , & Casper R.F. (2003). Three-dimensional in vitro culture of endometrial explants mimics the early stages of endometriosis. Fertility and Sterility 80, 1137–1143.

Pitt J.A. , Feng L. , Abbott B.D. , Schmid J. , Batt R.E. , Costich T.G. , Koury S.T. , & Bofinger D.P. (2001). Expression of AhR and ARNT mRNA in cultured human endometrial explants exposed to TCDD. Toxicological Sciences 62, 289–298.

Catalano R.D. , Yanaihara A. , Evans A.L. , Rocha D. , Prentice A. , Saidi S. , Print C.G. , Charnock-Jones D.S. , Sharkey A.M. , & Smith S.K. (2003). The effect of RU486 on the gene expression profile in an endometrial explant model. Molecular Human Reproduction 9, 465–473.

Jain J.K. , Li A. , Minoo P. , Nucatola D.L. , Felix J.C. (2005). The effect of nonoxynol-9 on human endometrium. Contraception 71, 137–142.

Kim S.Y. , Suzuki N. , Santosh Laxmi Y.R. , McGarrigle B.P. , Olson J.R. , Sharma M. , Sharma M. , & Shibutani S. (2005). Formation of tamoxifen-DNA adducts in human endometrial explants exposed to α-hydroxytamoxifen. Chemical Research in Toxicology 18, 889–895.

Cornet P.B. , Picquet C. , Lemoine P. , Osteen K.G. , Bruner-Tran K.L. , Tabibzadeh S. , Courtoy P.J. , Eeckhout Y. , Marbaix E. , & Henriet P. (2002). Regulation and function of LEFTY-A/EBAF in the human endometrium. Journal of Biological Chemistry 277, 42496–42504.

Punyadeera C. , Dunselman G. , Marbaix E. , Kamps R. , Galant C. , Nap A. , de Goeij A. , Ederveen A. , & Groothius P. (2004). Triphasic pattern in ex vivo response of human proliferative phase endometrium to oestrogens. Journal of Steroid Biochemistry & Molecular Biology 92, 175–185.

Vassilev V. , Pretto C.M. , Cornet P.B. , Delvaux D. , Eckhout Y. , Courtoy P.J. , Marbaix E. , & Henriet P. (2005). Response of matrix metalloproteinase and tissue inhibitors of metalloproteinases messenger ribonucleic acids to ovarian steroids in human endometrial explants mimics their gene- and phase-specific differential control in vivo. Journal of Clinical Endocrinology & Metabolism 90, 5848–5857.

Bellehumeur C. , Collette T. , Maheux R. , Mailloux J. , Villeneuve M. , & Akoum A. (2005). Increased soluble interleukin-1 receptor type II proteolysis in the endometrium of women with endometriosis. Human Reproduction 20, 1177–1184.

Noyes R.W. , Hertig A.T. , & Rock J. (1950). Dating the endometrial biopsy. Fertility and Sterility 1, 3–25.

Johannisson E. , Landgren B.M. , Rohr H.P. , & Diczfalusy E. (1987). Endometrial morphology and peripheral hormone levels in women with regular menstrual cycles. Fertility and Sterility 48, 401–408.

Murray M.J. , Meyer W.R. , Zaino R.J. , Lessey B.A. , Novotny D.B. , Ireland K. , Zeng D. , & Fritz M.A. (2004). A critical analysis of the accuracy reproducibility, and clinical utility of histologic endometrial dating in fertile women. Fertility and Sterility 81, 1333–1134.

McGovern P.G. , Myers E.R. , Silva S. , Coutifaris C. , Carson S.A. , Legro R.S. , Schlaff W.D. , Carr B.R. , Steinkampf M.P. , Giudice L.C. , Leppert P.C. , & Diamond M.P. (2004). Absence of secretory endometrium after false-positive home urine luteinizing hormone testing. Fertility and Sterility 82, 1273–1277.

Talbi S. , Hamilton A.E. , Vo K.C. , Tulac S. , Overgaard M.T. , Dosiou C. , Le Shay N. , Nezhat C.N. , Kempson R. , Lessey B.A. , Nayak N.R. , & Giudice L.C. (2006). Molecular phenotyping of human endometrium distinguishes menstrual cycle phases and underlying biological processes in normo-ovulatory women. Endocrinology 147, 1097–1121.

Herrler A. , von Rango U. , & Beier H.M. (2002). Embryo–maternal signalling: how the embryo starts talking to its mother to accomplish implantation. Reproductive BioMedicine Online 6, 244–256.

Folkman J. (1985). Tumor angiogenesis. Advances in Cancer Research 43, 175–203.

Folkman J. , & Shing Y. (1992). Control of angiogenesis by heparin and other sulfated polysaccharides. Advances in Experimental Medicine and Biology 313, 355–364.

Gordon J.D. , Mesiano S. , Zaloudek C.J. , & Jaffe R.B. (1996). Vascular endothelial growth factor localization in human ovary and fallopian tubes: possible role in reproductive function and ovarian cyst formation. Journal of Clinical Endocrinology and Metabolism 81, 353–359.

Iruela-Arispe M.L. , Rodriguez-Manzaneque J.C. , & Abu-Jawdeh G. (1999). Endometrial endothelial cells express estrogen and progesterone receptors and exhibit a tissue specific response to angiogenic growth factors. Microcirculation 6, 127–140.

Critchley H.O. , Brenner R.M. , Henderson T.A. , Williams K. , Nayak N.R. , Slayden O.D. , Millar M.R. , & Saunders P.T. (2001). Estrogen receptor beta, but not estrogen receptor alpha, is present in the vascular endothelium of the human and nonhuman primate endometrium. Journal of Clinical Endocrinology and Metabolism 86, 1370–1378.

Krikun G. , Schatz F. , Taylor R. , Critchley H.O. , Rogers P.A. , Huang J. , & Lockwood C.J. (2005). Endometrial endothelial cell steroid receptor expression and steroid effects on gene expression. Journal of Clinical Endocrinology and Metabolism 90, 1812–1818.

Giudice L.C. (1994). Growth factors and growth modulators in human uterine endometrium: their potential relevance to reproductive medicine. Fertility and Sterility 61, 1–17.

Gargett C.E. , Lederman F.L. , Lau T.M. , Taylor N.H. , & Rogers P.A. (1999). Lack of correlation between vascular endothelial growth factor production and endothelial cell proliferation in the human endometrium. Human Reproduction 14, 2080–2088.

Gargett C.E. , & Rogers P.A. (2001). Human endometrial angiogenesis. Reproduction 121, 181–186.

Rogers P.A. , & Gargett C.E. (1998). Endometrial angiogenesis. Angiogenesis 2, 287–294.

Henning B. , Meerarani P. , Slim R. , Toborek M. , Daugherty A. , Silverstone A.E. , & Robertson L.W. (2002). Proinflammatory properties of coplanar PCBs: in vitro and in vivo evidence. Toxicology and Applied Pharmacology 181, 174–183.

Jokinen M.P. , Walker N.J. , Brix A.E. , Sells D.M. , Haseman J.K. , & Nyska A. (2003). Increase in cardiovascular pathology in female Sprague-Dawley rats following chronic treatment with 2,3,7,8-tetra-chlorodibenzo-p-dioxin and 3,3’,4,4’,5-pentachloro-biphenyl. Cardiovascular Toxicology 3, 299–310.

Revankar C.M. , Cimino D.F. , Sklar L.A. , Arterburn J.B. , & Prossnitz E.R. (2005). A transmembrane intracellular estrogen receptor mediates rapid cell signaling. Science, New York 307, 1625–1630.

Möller B. , Rönnerdag M. , Wang G. , Odlind V. , & Olovsson M. (2005). Expression of vascular endothelial growth factors and their receptors in human endometrium from women experiencing abnormal bleeding patterns after prolonged use of a levonorgestrel-releasing intrauterine system. Human Reproduction 20, 1410–1417.

Wingfield M. , Macpherson A. , Healy D.L. , & Rogers P.A. (1995). Cell proliferation is increased in the endometrium of women with endometriosis. Fertility and Sterility 64, 340–346.

Huppert B. , & Peeters L.L.H. (2005). Vascular biology in implantation and placentation. Angiogenesis 8, 157–167.

Betsholtz C. , Lindholm P. , & Gerhardt H. (2005). Role of pericytes in vascular morphogenesis. EXS 94, 115–125.

Leveen P. , Pekny M. , Gebre-Medhin S. , Swolin B. , Larsson E. , & Betsholtz C. (1994). Mice deficient for PDGF B show renal, cardiovascular, and haematological abnormalities. Genes & Development 8, 1875–1887.

Armulik A. , Abramsson A. , & Betsholtz C. (2005). Endothelial/pericyte interactions. Circulation Research 97, 512–523.

Loeffler M. , & Potten C.S. (1997). Stem cells and cellular pedigrees — a conceptual introduction. In Stem Cells (ed. Potten C.S. ), pp. 1–2. London, UK: Academic Press.

King A. , Thomas L. , & Bischof P. (2000). Cell culture models of trophoblast II: trophoblast cell lines — a workshop report. Placenta 21, S113–S119.

Miller R.K. , Genbacev O. , Turner M.A. , Aplin J.D. , Caniggia I. , & Huppertz B. (2005). Human placental explants in culture: approaches and assessments. Placenta 26, 439–448.

Burleigh D.W. , Kendziorski C.M. , Choi Y.Y. , Grindle K.M. , Grendel R.L. , Magness R.R. , & Golos T.G. (2007). Microarray analysis of BeWo and JEG3 trophoblast cell lines: identification of differentially expressed transcripts. Placenta 28, 383–389.

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, 439–461.

Caniggia I. , Taylor C.V. , Ritchie J.W. , Lye S.J. , & Letarte M. (1997). Endoglin regulates trophoblast differentiation along the invasive pathway in human placental villous explants. Endocrinology 138, 4977–4988.

Bechi N. , Letta F. , Romagnoli R. , Focardi S. , Corsi I. , Buffi C. , & Paulesu L. (2006). Estrogenlike response to p-nonylphenol in human first trimester placenta and BeWo choriocarcinoma cells. Toxicological Sciences 93, 75–81.

Ala-Kokko T.I. , Myllynen P. , & Vähäkangas K. (2000). Ex vivo perfusion of the human placental cotyledon: implications for anesthetic pharmacology. International Journal of Obstetric Anaesthesia 9, 26–38.

Vähäkangas K. , & Myllynen P. (2006). Experimental methods to study human transplacental exposure to genotoxic agents. Mutation Research 608, 129–135.

Mose T. , Mortensen G.K. , Hedegaard M. , & Knudsen L. (2007). Phthalate monoesters in perfusate from a dual placenta perfusion system, the placenta tissue and umbilical cord blood. Reproductive Toxicology 23, 83–89.

Mose T. , Knudsen L.E. , Hedegaard M. , & Mortensen G. (2007). Transplacental transfer of monomethyl phthalate and mono (2-ethylhexyl) phthalate in a human placenta perfusion system. International Journal of Toxicology 26, 221–229.

Polliotti B.M. , Holmes R. , Cornish J.D. , Hulsey M. , Keesling S. , Schwartz D. , Abramowsky C.R. , Huddleston J. , Panigel M. , & Nahmias A.J. (1996). Long-term dual perfusion of isolated human placental lobules with improved oxygenation for infectious diseases research. Placenta 17, 57–68. Erratum in: Placenta 17, 267–268.

Heikkila A. , Myllynen P. , Keski-Nisula L. , Heinonen S. , Vähäkangas K. , & Yla-Herttuala S. (2002). Gene transfer to human placenta ex vivo: a novel application of dual perfusion of human placental cotyledon. American Journal of Obstetrics and Gynecology 186, 1046–1051.

Myllynen P. , Pienimaki P. , & Vähäkangas K. (2005). Human placental perfusion method in the assessment of transplacental passage of antiepileptic drugs. Toxicology and Applied Pharmacology 207, 489–494.

Myllynen P. , & Vähäkangas K. (2002). An examination of whether human placental perfusion allows accurate prediction of placental drug transport: studies with diazepam. Journal of Pharmacological and Toxicological Methods 48, 131–138.

Pienimäki P. , Hartikainen A-L. , Arvela P. , Partanen T. , Herva R. , Pelkonen O. , & Vähäkangas K. (1995). Carbamazepine and its metabolites in human perfused placenta and in maternal and cord plasma. Epilepsia 36, 241–248.

Hoffmann S. , & Hartung T. (2006). Toward an evidence-based toxicology. Human & Experimental Toxicology 25, 497–513.

Anon. (1984). Biosafety in Microbiological and Bio-medical Laboratories. DHHS (Centers for Disease Control) Publication No. 84-8395 (ed. Richmond J.Y. , & McKinney R.W. ), pp. 88–199. Atlanta, GA, USA: US Government Printing Office.

World Health Organization (WHO) (2003). Laboratory Safety Manual, 2nd edn, pp. 45–50. Geneva, Switzerland: WHO.

Walker D. , & Campbell D. (1999). A survey of infections in United Kingdom laboratories, 1994–1995. Journal of Clinical Pathology 52, 415–418.

Fisker N. , Mygind L.H. , Krarup H.B. , Licht D. , Georgsen J. , & Christensen P.B. (2004). Blood borne viral infections among Danish Health Care Workers — frequent blood exposure but low prevalence of infection. European Journal of Epidemiology 19, 61–67.

Tarantola A. , Golliot F. , Astagneau P. , Fleury L. , Brücker G. , & Bouvet E. (2003). Occupational blood fluids exposures in health care workers: four-year surveillance from the Northern France network. American Journal of Infection Control 31, 357–363.

Hanrahan A. , & Reutter L. (1997). A critical review of the literature on sharps injuries: epidemiology, management of exposures and prevention. Journal of Advanced Nursing 25, 144–154.

Wilburn S.Q. (2004). Needle stick and sharp injury prevention. The Online Journal of Issues in Nursing 9, 5.

Mahn J.W. (1991). Fundamentals of Laboratory Safety: Physical Hazards in the Academic Laboratory, 2nd edn, 300 pp. New York, NY, USA: Van Nostrand Reinhold.

Stricoff R.S. , & Walters D.B. (1995). Handbook of Laboratory Health and Safety, 2nd edn, pp. 59–68. Hoboken, NJ, USA: John Wiley and Sons Inc.

Anon. (2005). Ethics — Ethical Scientific Research — Respect of Fundamental Principles. Website http://ec.europa.eu/research/science-society/page_en.cfm?id=3203 (Accessed 20.12.06).