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Cellular Biochemistry of the Endometrium

  • John D. Aplin

Abstract

Morphological alterations in endometrium during the reproductive cycle are increasingly well documented. A new era has now begun in which the molecular processes that underlie these structural changes will be elucidated. Ultimately, in the foreseeable future, the molecular interactions responsible for implantation and placentation will be understood, with undoubted benefits in the clinic. Progress will depend on a combination of biochemical, molecular biological, cell biological, and morphological approaches. This chapter summarizes current information on endometrial composition with emphasis on hormone-regulated alterations in endogenous glycoproteins, proteins, and proteoglycans that may be required for successful reproduction. The main focus of attention is on the human, but results of some animal studies are also included since they may facilitate the establishment of hypotheses for testing, insofar as ethics permit, in the human. New insights into function may be gained when a prominent constituent of one species is absent or modified in another. Emphasis is placed on structural components many of which represent the end products of metabolic processes that are controlled hormonally. The underlying endocrine and metabolic processes themselves are not considered. At the time of writing, few uninterrupted lines of connection can be drawn between morphology and biochemisry, so one function of this chapter is to draw attention to areas of research in which, with recent methodological advances, progress can now be expected.

Keywords

Human Endometrium Decidual Cell Diamine Oxidase Late Secretory Phase Glandular Epithelial Cell 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Abedin, M. Z., Ayad, S., and Weiss, J. B., 1981, Type V collagen: The presence of appreciable amounts of a3(V) chains in uterus, Biochem. Biophys. Res. Commun. 102: 1237–1245.PubMedCrossRefGoogle Scholar
  2. Abedin, M. Z., Ayad, S., and Weiss, J. B., 1982, Isolation and characterisation of cysteine-rich collagens from bovine placental tissues and uterus and their relationship to types IV and V collagens, Biosci. Rep. 2: 493–502.CrossRefGoogle Scholar
  3. Adams, C. E., 1958, Egg development in the rabbit: The influence of post-coital ligation of the uterine tube and of ovariectomy, J. Endocrinol. 16: 283–293.PubMedCrossRefGoogle Scholar
  4. Alden, R. H., 1942, Aspects of the egg-ovary-oviduct relationship in the albino rat. II. Egg development within the oviduct, J. Exp. Zool. 90: 171–175.CrossRefGoogle Scholar
  5. Anderson, T. L., and Hoffman, L. H., 1984, Alterations in epithelial glycocalyx of rabbit uteri during early pseudopregnancy and pregnancy, and following ovariectomy, Am. J. Anat. 171: 321–334.Google Scholar
  6. Anderson, T. L., Olson, G. E., and Hoffman, L. H., 1986, Stage-specific alterations in the apical membrane glycoproteins of endometrial epithelial cells related to implantation in rabbits, Biol. Reprod. 34: 701–720.PubMedCrossRefGoogle Scholar
  7. Aplin, J. D., and Hughes, R. C., 1982, Complex carbohydrates of the extracellular matrix, Biochim. Biophys. Acta 694: 375–418.PubMedGoogle Scholar
  8. Aplin, J. D., and Seif, M. W., 1985, Basally located epithelial cell surface component identified by a novel monoclonal antibody technique, Exp. Cell Res. 160: 550–555.PubMedCrossRefGoogle Scholar
  9. Aplin, J. D., and Seif, M. W., 1987, A monoclonal antibody to a cell surface determinant in human endometrial epithelium: Stage-specific expression in the menstrual cycle, Am. J. Obstet. Gynecol. 156: 250–255.PubMedGoogle Scholar
  10. Aplin, J. D., Campbell, S., and Allen, T. D., 1985, The extracellular matrix of human amniotic epithelium: Ultrastructure, composition and deposition, J. Cell Sci. 79: 119–136.PubMedGoogle Scholar
  11. Aplin, J. D., Charlton, A. K., and Ayad, S., 1988, An immunohistochemical study of human endometrial extracellular matrix during the menstrual cycle and first trimester of pregnancy, Cell Tissue Res. 253: 231–240.PubMedCrossRefGoogle Scholar
  12. Atger, M., Perricaudet, M., Toillais, P., and Milgrom, E., 1980, Bacterial cloning of the rabbit uteroglobin structural gene, Biochem. Biophys. Res. Commun. 93: 1082–1088.Google Scholar
  13. Atger, M., Atger, P., Toillais, P., and Milgrom, E., 1981, Cloning of rabbit genomic fragments containing the uteroglobin gene, J. Biol. Chem. 256: 5970–5972.Google Scholar
  14. Aumiiller, G., Seitz, J., Heyns, W., and Kirchner, C., 1985, Ultrastructural localisation of uteroglobin immu-noreactivity in rabbit lung and endometrium, and rat ventral prostate, Histochemistry 83: 413–417.CrossRefGoogle Scholar
  15. Ayad, S., Chambers, C. A., Shuttleworth, C. A., and Grant, M. E., 1985, Isolation from bovine elastic tissues of collagen type VI and characterisation of its form in vivo, Biochem. J. 230: 465–474.PubMedGoogle Scholar
  16. Barlow, D. P., Green, N. M., Kurkinen, M., and Hogan, B. L. M., 1984, Sequencing of laminin B chain cDNAs reveals C-terminal regions of coiled coil alpha helix, EMBO J. 3: 2355–2362.PubMedGoogle Scholar
  17. Baumbach, G. A., Saunders, P. T. K., Bazer, F. W., and Roberts, R. M., 1984, Uteroferrin has asparagine-linked high mannose-type oligosaccharides that contain mannose 6-phosphate, Proc. Natl. Acad. Sci. U. S. A. 81: 2985–2989.PubMedCrossRefGoogle Scholar
  18. Beato, M., and Beier, H. M., 1978, Characteristics of the purified uteroglobin-like protein from rabbit lung, J. Reprod. Fertil. 53: 305–314.PubMedCrossRefGoogle Scholar
  19. Beier, H. M., 1968, Uteroglobin: A hormone sensitive endometrial protein involved in blastocyst development, Biochim. Biophys. Acta 160: 289–291.PubMedGoogle Scholar
  20. Beier, H. M., 1976, Uteroglobin and related biochemical changes in the reproductive tract during early pregnancy in the rabbit, J. Reprod. Fertil. [Suppl.] 25: 53–69.Google Scholar
  21. Bell, S. C., 1979, Immunochemical identity of “decidua-associated protein” and a2 acute phase macroglobulin in the pregnant rat, J. Reprod. Immunol. 1: 193–206.CrossRefGoogle Scholar
  22. Bell, S. C., 1986, Secretory endometrial and decidual proteins: Studies and clinical significance of a maternally derived group of pregnancy-associated serum proteins, Hum. Reprod. 1: 129–143.Google Scholar
  23. Bell, S. C., and Bohn, H., 1986, Immunochemical and biochemical relationship between human pregnancy-associated secreted ar and a2-globulins (ar and a2-PEG) and the soluble placental proteins 12 and 14 (PP12 and PP14), Placenta 7: 283–294.PubMedCrossRefGoogle Scholar
  24. Bell, S. C., and Dore-Green, F., 1987, Detection and characterisation of human secretory “pregnancy-associ-ated” endometrial a2-globulin (a2-PEG) in uterine luminal fluid, J. Reprod. Immunol. 11: 13–29.Google Scholar
  25. Bell, S. C., and Patel, S. R., 1987, Immunochemical detection, physicochemical characterisation and levels of pregnancy-associated endometrial a2-globulin (a2-PEG) in seminal plasma of men, J. Reprod. Fertil. 80: 31–42.Google Scholar
  26. Bell, S. C., and Smith, S., 1988, The endometrium as a paracrine organ, in: Contemporary Obstetrics and Gynaecology, Vol. 17, part 2 ( G. V. P. Chamberlain, ed.), Butterworths, London, pp. 273–299.Google Scholar
  27. Bell, S. C., Patel, S., Hales, M. W., Kirwan, P. H., and Drife, J. O., 1985a, Immunochemical detection and characterisation of pregnancy-associated endometrial ar and a2-globulins secreted by human endometrium and decidua, J. Reprod. Fertil. 74: 261–270.PubMedCrossRefGoogle Scholar
  28. Bell, S. C., Hales, M. W., Patel, S., Kirwan, P. H., and Drife, J. O., 1985b, Protein synthesis and secretion by the human endometrium and decidua during early pregnancy, Br. J. Obstet. Gynaecol. 92: 793–803.PubMedCrossRefGoogle Scholar
  29. Bell, S. C., Patel, S. R., Kirwan, P. H., and Drife, J. O., 1986a, Protein synthesis and secretion by the human endometrium during the menstrual cycle and the effect of progesterone in vitro, J. Reprod. Fertil. 77: 221–231.PubMedCrossRefGoogle Scholar
  30. Bell, S. C., Hales, M. W., Patel, S. R., Kirwan, P. H., Drife, J. O., and Milford-Ward, A., 1986b, Amniotic fluid levels of secreted pregnancy-associated endometrial ar and a2-globulins (ar and a2-PEG), Br. J. Obstet. Gynaecol. 93: 909–915.Google Scholar
  31. Bell, S. C., Keyte, J. W., and Waites, G. T., 1987, Pregnancy-associated endometrial a2-globulin (a2-PEG), the major secretory protein of the luteal phase and first trimester pregnancy endometrium, is not glycosylated prolactin but related to P-lactoglobulins, J. Clin. Endocrinol. Metab. 65: 1–5.Google Scholar
  32. Bischof, P., Tseng, L., Brioschi, P. A., and Herrmann, W. L., 1986, Cancer antigen 125 is produced by human endometrial stromal cells, Hum. Reprod. 1: 423–426.Google Scholar
  33. Bissell, M. J., Hall, H. G., and Parry, G., 1982, How does the extracellular matrix direct gene expression? J. Theor. Biol. 99: 31–68.Google Scholar
  34. Blumberg, B., Mackrell, A. J., Olson, P. F., Kurkinen, M., Munson, J. M., Natzle, J. E., and Fessler, J. H., 1987, Basement membrane procollagen IV and its specialized carboxyl domain are conserved in Drosophila, mouse and human, J. Biol. Chem. 262: 5947–5950.PubMedGoogle Scholar
  35. Bohn, H., and Kraus, W., 1980, Isolierung und Characterisierung eines neuen plazentaspezifischen Proteins (PP12), Arch. Gynaecol. 229: 279–291.Google Scholar
  36. Bohn, H., Kraus, W., and Winckler, W., 1982, New soluble placental tissue proteins: Their isolation, characterisation, localization and quantification, Placenta (Suppl.) 4: 67–81.Google Scholar
  37. Bolton, A. E., Pockley, A. G., Clough, K. J., Mowles, E. A., Stoker, R. J., Westwood, O. M. R., and Chapman, M. G., 1987, Identification of placental protein 14 as an immunosuppressive factor in human reproduction, Lancet 1: 593–595.PubMedCrossRefGoogle Scholar
  38. Bruns, R. R., Press, W., Engvall, E., Timpl, R., and Gross, J., 1986, Type VI collagen in extracellular, 100 nm periodic filaments and fibrils: Identification by immunoelectron microscopy, J. Cell Biol. 103: 393–404.Google Scholar
  39. Bullock, D. W., and Conell, K. M., 1973, Occurrence and molecular weight of rabbit uterine “blastokinin,” Biol. Reprod. 9: 125–132.PubMedGoogle Scholar
  40. Bulmer, J. N., and Johnson, P. M., 1985, Antigen expression by trophoblast populations in the human placenta and their possible immunobiological relevance, Placenta 6: 127–140.PubMedCrossRefGoogle Scholar
  41. Bulmer, J. N., Wells, M., Bhabra, K., and Johnson, P. M., 1986, Immunohistological characterisation of endometrial gland epithelium and extravillous fetal trophoblast in third trimester human placental bed tissues, Br. J. Obstet. Gynaecol. 93: 823–832.PubMedCrossRefGoogle Scholar
  42. Bychkov, V., and Toto, P. D., 1986, Lectin binding to normal human endometrium, Gynecol. Obstet. Invest. 22: 29–33.PubMedCrossRefGoogle Scholar
  43. Campbell, S., Aplin, J. D., Seif, M. W., Richmond, S., Haynes, P., and Allen, T. D., 1988, Expression of a secretory product of microvillous and ciliated cells of the human endometrial epithelium in vivo and in vitro, Hum. Reprod. (in press).Google Scholar
  44. Carlin, B., Jaffe, R., Bender, B., and Chung, A. E., 1981, Entactin, a novel basal lamina-associated sulphated glycoprotein, J. Biol. Chem. 256: 5209–5216.PubMedGoogle Scholar
  45. Carson, D. D., Dutt, A., and Tang, J. -P., 1987, Glycoconjugate synthesis during early pregnancy: Hyaluronate synthesis and function, Dev. Biol. 120: 228–235.Google Scholar
  46. Chavez, D. J., and Anderson, T. L., 1985, The glycocalyx of the mouse uterine luminal epithelium during estrus, early pregnancy and the pre-implantation period and delayed implantation. 1. Acquisition of RCA-1 binding sites during pregnancy, Biol. Reprod. 32: 1135–1142.PubMedCrossRefGoogle Scholar
  47. Cheah, K. S., 1985, Collagen genes and inherited connective tissue disease, Biochem. J. 229: 287–303.PubMedGoogle Scholar
  48. Chegini, N., Rao, C. V., Wakim, N., and Sanfilippo, J., 1986, Binding of 125I-epidermal growth factor in human uterus, Cell Tissue Res. 246: 543–548.PubMedCrossRefGoogle Scholar
  49. Chemnitz, J., Folkerson, J., Teisner, B., Sinosich, M. J., Tornehave, D., Westergaard, J. G., Bolton, A. E., and Grudzinskas, J. G., 1986, Comparison of different antibody preparations against PAPP-A for use in localization and immunoassay studies, Br. J. Obstet. Bynaecol. 93: 916–923.CrossRefGoogle Scholar
  50. Chen, T. T., Bazer, F. W., Cetorelli, J. J., Pollard, W. E., and Roberts, R. M., 1973, Purification and properties of a progesterone-induced basic glycoprotein from the uterine fluid of pigs, J. Biol. Chem. 248: 8560–8566.PubMedGoogle Scholar
  51. Ciocca, D. R., Adams, D. J., Bjercke, R. J., Edwards, D. P., and McGuire, W. L., 1982, Immu-nohistochemical detection of an estrogen-related protein by monoclonal antibodies, Cancer Res. 42: 4256–4258.PubMedGoogle Scholar
  52. Ciocca, D. R., Adams, D. J., Edwards, D. P., Bjercke, R. J., and McGuire, W. L., 1983a, Distribution of an estrogen-induced protein with a molecular weight of 24, 000 in normal and malignant human tissues and cells, Cancer Res. 43: 1204–1210.Google Scholar
  53. Ciocca, D. R., Asch, R. H., Adams, D. J., and McGuire, W. L., 1983b, Evidence for modulation of a 24k protein in human endometrium during the menstrual cycle, J. Clin. Endocrinol. Metab. 57: 496–499.PubMedCrossRefGoogle Scholar
  54. Cooke, P. S., Uchima, F. A., Fujii, D. K., Bern, H. A., and Cunha, G. R., 1986, Restoration of normal morphology and estrogen responsiveness in cultured vaginal and uterine epithelia transplanted with stroma, Proc. NatL Acad Sci. U. S. A. 83: 2109–2113.PubMedCrossRefGoogle Scholar
  55. Cooke, P. S., Fujii, D. K., and Cunha, G. A., 1987, Vaginal and uterine stroma maintain their inductive properties following primary culture, In Vitro Cell Dev. Biol. 23: 159–166.Google Scholar
  56. Cornillie, F. J., Lauweryns, J. M., and Brosens, I. A., 1985, Normal human endometrium. An ultrastructural survey, Gynecol. Obstet. Invest. 20: 113–129.PubMedCrossRefGoogle Scholar
  57. Dallenbach-Hellweg, G., 1981, Histopathology of the Endometrium, 3rd ed., Springer-Verlag, Berlin.CrossRefGoogle Scholar
  58. Daly, D. C., Maslar, I. A., and Riddick, D. H., 1983, Prolactin production during in vitro decidualization of proliferative endometrium, Am. J. Obstet. Gynecol. 145: 672–678.PubMedGoogle Scholar
  59. Daniel, J. C., 1972, Preliminary attempts to terminate pregnancy by immunological attack on uterine protein, Experientia 28: 700–701.PubMedCrossRefGoogle Scholar
  60. Daniel, J. C., 1976, Blastokinin and analogous proteins, J. Reprod. Fertil. [Suppl.] 25: 71–83.Google Scholar
  61. Daya, S., Clark, D. A., Chaput, A., Devlin, C., and Jarrell, F., 1985, Suppressor cells in human decidua, Am. J. Obstet. Gynecol. 151: 267–270.PubMedGoogle Scholar
  62. Denker, H. -W., 1978, The role of trophoblastic factors in implantation, in: Novel Aspects of Reproductive Physiology ( C. H. Spilman and J. W. Wilks, eds.), Spectrum, New York, pp. 181–212.Google Scholar
  63. Denker, H. -W., 1982, Proteases of the blastocyst and of the uterus, in: Proteins and Steroids in Early Pregnan-cy ( H. M. Beier and P. Karlson, eds.), Springer-Verlag, Berlin, pp. 183–208.CrossRefGoogle Scholar
  64. Denker, H. -W., 1983, Basic aspects of ovoimplantation, Obstet. Gynecol. Annu. 12: 15–42.PubMedGoogle Scholar
  65. DiPasquale, A., 1975, Locomotory activity of epithelial cells in culture, Exp. Cell Res. 94: 191–215.CrossRefGoogle Scholar
  66. Dutt, A., Tang, J. -P., and Carson, D. D., 1987, Lactosaminoglycans are involved in uterine epithelial cell adhesion in vitro, Dev. Biol. 119: 27–37.PubMedCrossRefGoogle Scholar
  67. Dziadek, M., Paulsson, M., and Timpl, R., 1985, Identification and interactive repertoire of large forms of the basement membrane protein nidogen, EMBO J. 4: 2513–2518.PubMedGoogle Scholar
  68. Edwards, D. P., Adams, D. J., Savage, N., and McGuire, W. L., 1980, Estrogen induced synthesis of specific proteins in human breast cancer cells, Biochem. Biophys. Res. Commun. 93: 804–812.PubMedCrossRefGoogle Scholar
  69. Faber, M., Wewer, U. M., Berthelsen, J. G., Liotta, L. A., and Albrechtsen, R., 1986, Laminin production by human endometrial stromal cells relates to the cyclic and pathologic state of the endometrium, Am. J. Pathol. 124: 384–391.Google Scholar
  70. Frame, L. T., Wiley, L., and Rogol, A. D., 1979, Indirect immunofluorescent localisation of prolactin to the cytoplasm of decidua and trophoblast cells in human placental membranes at term, J. Clin. Endocrinol. Metab. 49: 435–437.PubMedCrossRefGoogle Scholar
  71. Gallagher, J. T., Lyon, M., and Steward, W. P., 1986, Structure and function of heparan sulphate pro-teoglycans, Biochem. J. 236: 313–325.PubMedGoogle Scholar
  72. Geuze, H. J., Slot, J. W., Strous, G. J. A. M., Hasilik, A., and von Figura, K., 1985, Possible pathways for lysosomal enzyme delivery, J. Cell Biol. 101: 2253–2262.PubMedCrossRefGoogle Scholar
  73. Glass, R. H., Aggeler, J., Spindle, A., Pedersen, R. A., and Werb, Z., 1983, Degradation of extracellular matrix by mouse trophoblast outgrowths: A model for implantation, J. Cell Biol. 96: 1108–1116.Google Scholar
  74. Glasser, S. R., 1985, Laboratory models of implantation, in: Reproductive Toxicology ( R. L. Dixon, ed.), Raven Press, New York, pp. 219–238.Google Scholar
  75. Glasser, S. R., and Julian, J., 1986, Intermediate filament protein as a marker of uterine stromal cell decid-ualisation, Biol. Reprod. 35: 463–474.Google Scholar
  76. Glasser, S. R., Lampelo, S., Munir, M. I., and Julian, J., 1987, Expression of desmin, laminin and fibronectin during in situ differentiation (decidualisation) of rat uterine stromal cells, Differentiation 35: 132–142.PubMedCrossRefGoogle Scholar
  77. Green, M. R., and Pastewka, J. V., 1978, Lactoferrin is a marker for prolactin response in mouse mammary explants, Endocrinology 103: 1510–1513.CrossRefGoogle Scholar
  78. Griepp, E. B., Dolan, W. J., Robbins, E. S., and Sabatini, D. D., 1983, Participation of plasma membrane proteins in formation of tight junctions by cultured epithelial cells, J. Cell Biol. 96: 693–702.PubMedCrossRefGoogle Scholar
  79. Grinnell, F., Head, J. R., and Hoffpanir, J., 1982, Fibronectin and cell shape in vivo. Studies on the endo-metrium during pregnancy, J. Cell Biol. 94: 597–606.Google Scholar
  80. Guest, J. F., Elder, M. G., and White, J. O., 1986, Application of two dimensional electrophoresis to characterise hormonally sensitive proteins in the normal and abnormal uterus, Electrophoresis 7: 512–518.CrossRefGoogle Scholar
  81. Handwerger, S., Barry, S., and Conn, P. M., 1984, Different subcellular storage sites for decidual and pituitary-derived prolactin: Possible explanation for differences in regulation, Mol. Cell. Endocrinol. 37: 83–87.PubMedCrossRefGoogle Scholar
  82. Handwerger, S., Hamman, I., Costello, A., and Markoff, E., 1987, cAMP inhibits the synthesis and release of prolactin from human decidual cells, Mol. Cell. Endocrinol. 50: 99–106.Google Scholar
  83. Hanisch, F. G., Uhlenbruck, G., Dienst, C., Stottrop, M., and Hippanf, E., 1985, Cal25 and Cal9–9: Two cancer-associated sialylsaccharide antigens on a mucus glycoprotein from human milk, Eur. J. Biochem. 149: 323–330.Google Scholar
  84. Hanley, M. R., and Jackson, T., 1987, The ras gene. Transformer and transducer, Nature 328: 668–669.Google Scholar
  85. Hassell, J. R., Kimwa, J. H., and Hascall, V. C., 1986, Proteoglycan core protein families, Annu. Rev. Biochem. 55: 539–567.PubMedCrossRefGoogle Scholar
  86. Hay, E. D., 1981, Extracellular matrix, J. Cell Biol. 91: 205s - 223s.PubMedCrossRefGoogle Scholar
  87. Healy, D. L., and Hodgen, G. D., 1983, The endocrinology of human endometrium, Obstet. Gynecol. Surv. 38: 509–530.PubMedCrossRefGoogle Scholar
  88. Healy, D. L., Muller, H. K., and Burger, H. G., 1977, Immunofluorescence localisation of prolactin to human amnion, Nature 265: 642–644.PubMedCrossRefGoogle Scholar
  89. Healy, D. L., Herington, A. L., and O’Herlihy, C., 1983, Chronic polyhydramnios: Evidence for a defect in the chorion laeve receptor for lactogenic hormones, J. Clin. Endocrinol. Metab. 56: 520–525.Google Scholar
  90. Heffner, L. J., Iddenden, D. A., and Lyttle, C. R., 1986, Electrophoretic analysis of secreted human endometrial proteins: Identification and characterisation of luteal phase products, J. Clin. Endocrinol. Metab. 62:1288–1295.CrossRefGoogle Scholar
  91. Heimann, R., Rice, R. H., Gross, M. K., and Coe, E. L., 1985, Estrogen receptor expression in serially cultivated rat endometrial cells: Stimulation by forskolin and cholera toxin, J. Cell. Physiol. 123: 197–200.PubMedCrossRefGoogle Scholar
  92. Heinegard, D., Bjdrne-Persson, A., Coster, L., Franzen, A., Gardell, S., Malmstrom, A., Paulsson, M., Sandfalk, R., and Vogel, K., 1985, The core proteins of large and small interstitial proteoglycans from various connective tissues form distinct subgroups, Biochem. J. 230: 181–194.Google Scholar
  93. Hembry, R. M., Murphy, G., Cawston, T. E., Dingle, J. T., and Reynolds, J. J., 1986, Characterisation of a specific antiserum for mammalian collagenase from several species: immunolocalisation of collagenase in rabbit chondrocytes and uterus, J. Cell Sci. 81: 105–123.PubMedGoogle Scholar
  94. Henkel, W., and Glanville, R. W., 1982, Covalent cross-linking between molecules of collagen types I and III. The involvement of the N-terminal non-helical regions of the a 1(1) and al(III) chains, Eur. J. Biochem. 122: 205–213.PubMedCrossRefGoogle Scholar
  95. Herington, A. C., Graham, J., and Healy, D. L., 1980, The presence of lactogen receptors in human chorion laeve, J. Clin. Endocrinol. Metab. 51: 1466–1468.PubMedCrossRefGoogle Scholar
  96. Hewitt, K., Beer, A. E., and Grinnell, F., 1979, Disappearance of anionic sites from the surface of the rat endometrial epithelium at the time of blastocyst implantation, Biol. Reprod. 21: 691–707.Google Scholar
  97. Hirsch, P. J., Fergusson, I. L. C., and King, R. J. B., 1976, Protein composition of human endometrium and its secretion at different stages of the menstrual cycle, Ann. N. Y. Acad. Sci. 286: 233–248.CrossRefGoogle Scholar
  98. Holinka, C. F., and Gurpide, E., 1984, Diamine oxidase activity in human decidua and endometrium, Am. J. Obstet. Gynecol. 150: 359–363.Google Scholar
  99. Home, C. H. W., Armstrong, S. S., Thomson, A. W., and Thompson, W. D., 1983, Detection of pregnancy-associated a2-glycoprotein (a2-PAG), an immunosuppressive agent, in IgA-producing plasma cells and in body secretions, Clin. Exp. Immunol. 51: 631–638.Google Scholar
  100. Huhtala, M. -L., Seppala, M., Narvanen, A., Palomaki, P., Julkunen, M., and Bohn, H., 1987, Amino acid sequence homology between human placental protein 14 and 0-lactoglobulins from various species, Endocrinology 120: 2620–2622.PubMedCrossRefGoogle Scholar
  101. Hynes, R. O., and Yamada, K. M., 1982, Fibronectins: Multifunctional modular glycoproteins, J. Cell Biol. 95: 369–377.PubMedCrossRefGoogle Scholar
  102. Jansen, R. P. S., Turner, M., Johannisson, E., Landgren, B. -M., and Diczfalusy, E., 1985, Cyclic changes in human endometrial surface glycoproteins: A quantitative histochemical study, Fertil. Steril. 44: 85–91.Google Scholar
  103. Joshi, S. G., 1983, A progestagen-associated protein of the human endometrium: Basic studies and potential clinical applications, J. Steroid. Biochem. 19: 751–757.PubMedCrossRefGoogle Scholar
  104. Joshi, S. G., Ebert, K. M., and Swartz, D. P., 1980a, Detection and synthesis of a progestagen-dependent protein in human endometrium, J. Reprod. Fertil. 59: 273–285.PubMedCrossRefGoogle Scholar
  105. Joshi, S. G., Ebert, K. M., and Smith, R. A., 1980b, Properties of the progestagen-dependent protein of the human endometrium, J. Reprod. Fertil. 59: 287–296.PubMedCrossRefGoogle Scholar
  106. Joshi, S. G., Smith, R. A., and Stokes, D. K., 1980c, A progestagen-dependent endometrial protein in human amniotic fluid, J. Reprod. Fertil. 60: 317–321.PubMedCrossRefGoogle Scholar
  107. Joshi, S. G., Bank, J. F., and Szarowski, D. H., 1981, Radioimmunoassay for a progestagen-associated protein of the human endometrium, J. Clin. Endocrinol. Metab. 52: 1185–1192.PubMedCrossRefGoogle Scholar
  108. Julkunen, M., Raikar, R. S., Joshi, S. G., Bohn, H., and Seppala, M., 1986, Placental protein 14 and progestagen-dependent endometrial protein are immunologically indistinguishable, Hum. Reprod. 1: 7–8.Google Scholar
  109. Jung, G., Helm, R. M., Carraway, C. A. C., and Carraway, K. L., 1984, Mechanism of con A-induced anchorage of the major cell surface-associated glycoproteins to the submembranous cytoskeleton in 13762 ascites mammary adenocarcinoma cells, J. Cell Biol. 98: 179–187.PubMedCrossRefGoogle Scholar
  110. Kabawat, W. E., Bast, R. C., Welch, W. R., Knapp, R. C., and Colvin, R. B., 1983, Immunopathologic characterization of a monoclonal antibody that recognizes common surface antigens of human ovarian tumors of serous endometrioid and clear cell types, Am. J. Clin. Pathol. 79: 98–104.PubMedGoogle Scholar
  111. Katz, J., Kirsch, L., Levitz, M., Nathoo, S. A., and Seiler, S., 1983, Estrogen-stimulated uptake of plasminogen by the mouse uterus, Endocrinology 112: 856–861.PubMedCrossRefGoogle Scholar
  112. Kauma, S., and Shapiro, S. S., 1986, Immunoperoxidase localisation of prolactin in endometrium during normal menstrual, luteal phase defect and corrected luteal phase defect cycles, Fertil. Steril. 46: 37–41.PubMedGoogle Scholar
  113. Khoiig, T. Y., Lane, E. B., and Robertson, W. B., 1986, An immunocytochemical study of fetal cells at the maternal-placental interface using monoclonal antibodies to keratin, vimentin and desmin, Cell Tissue Res. 246: 189–195.Google Scholar
  114. Kirchner, C., 1976, Uteroglobin in the rabbit. I. Intracellular localisation in the oviduct, uterus and preimplanta-tion blastocyst, Cell Tissue Res. 170: 415–424.PubMedCrossRefGoogle Scholar
  115. Kirchner, C., and Schroer, H. G., 1976, Uterine secretion-like proteins in the seminal plasma of the rabbit, J. Reprod. Fertil. 47: 325–330.PubMedCrossRefGoogle Scholar
  116. Kirk, D., and Alvarez, R. B., 1986, Morphologically stable epithelial vesicles cultured from normal human endometrium in defined media, In Vitro Cell Dev. Biol. 22: 604–614.Google Scholar
  117. Kirk, D., and Irwin, J. C., 1980, Normal human endometrium in cell culture, Methods Cell Biol. 21B: 51–77.CrossRefGoogle Scholar
  118. Kirk, D., King, R. J. B., Heyes, J., Peachey, L., Hirsch, P. J., and Taylor, R. W. T., 1978, Normal human endometrium in cell culture. I. Separation and characterisation of epithelial and stromal components in vitro, In Vitro 14: 651–662.PubMedCrossRefGoogle Scholar
  119. Kisalus, L. L., Herr, J. C., and Little, C. D., 1987a, Immunolocalisation of extracellular matrix proteins and collagen synthesis in first trimester human decidua, Anat. Rec. 218: 402–415.PubMedCrossRefGoogle Scholar
  120. Kisalus, L. L., Nunley, W. C., and Herr, J. C., 1987b, Protein synthesis and secretion in human decidua of early pregnancy, Biol. Reprod. 36: 785–798.PubMedCrossRefGoogle Scholar
  121. Kleinman, D., Sharon, Y., Sarov, I., and Insler, V., 1983, Human endometrium in cell culture: A new method for culturing human endometrium as separate epithelial and stromal components, Arch. Gynecol. 234: 103–112.Google Scholar
  122. Kleinman, H. K., Cannon, F. B., Laurie, G. W., Hassell, J. R., Aumailley, M., Terranova, V. P., Martin, G. R., and Dubois-Dalcq, M., 1985, Biological activities of laminin, J. Cell Biochem. 27: 317–326.PubMedCrossRefGoogle Scholar
  123. Koistinen, R., Kalkkinen, N., Huhtala, M. -L., Seppala, M., Bohn, H., and Rutanen, E. -M., 1986, Placental protein 12 is a decidual protein that binds somatomedin and has an identical N-terminal amino acid sequence with somatomedin-binding protein from human amniotic fluid, Endocrinology 118: 1375–1378.PubMedCrossRefGoogle Scholar
  124. Kornblihtt, A. R., Umezawa, K., Vibe-Pedersen, K., and Baralle, F. E., 1985, Primary structure of human fibronectin: Differential splicing may generate at least 10 polypeptides from a single gene, EMBO J. 4: 1755–1759.PubMedGoogle Scholar
  125. Lala, P. K., Kearns, M., Parhar, R. S., Scodrase, J., and Johnson, S., 1986, Immunological role of the cellular constituents of the decidua in the maintenance of semiallogeneic pregnancy, Ann. N. Y. Acad. Sci. 476: 183–205.Google Scholar
  126. Lampelo, S. A., Ricketts, A. P., and Bullock, D. W., 1985, Purification of rabbit endometrial plasma membranes from receptive and non-receptive uteri, J. Reprod. Fertil. 75: 475–484.PubMedCrossRefGoogle Scholar
  127. Lampelo, S. A., Anderson, T. L., and Bullock, D. W., 1986, Monoclonal antibodies recognise a cell surface marker of epithelial differentiation in rabbit endometrium, J. Reprod. Fertil. 78: 663–672.PubMedCrossRefGoogle Scholar
  128. Laurie, G. W., Bing, J. T., Kleinman, H. K., Hassell, J. R., Aumailley, M., Martin, G. R., and Feldman, R. J., 1986, Localisation of binding sites for laminin, heparan sulphate, proteoglycans and fibronectin in basement membrane (type IV) collagen, J. Mol. Biol. 189: 205–216.Google Scholar
  129. Ledbetter, S. R., Fisher, L. W., and Hassell, J. R., 1987, Domain structure of the basement membrane heparan sulphate proteolgycan, Biochemistry 26: 988–995.PubMedCrossRefGoogle Scholar
  130. Lee, D. W., and Markov, E., 1986, Synthesis and release of glycosylated prolactin by human decidua in vitro, J. Clin. Endocrinol. Metab. 62: 990–994.Google Scholar
  131. Lee, M. -C., and Damjanov, I., 1985, Pregnancy-related changes in the human endometrium revealed by lectin histochemistry, Histochemistry 82: 275–280.PubMedCrossRefGoogle Scholar
  132. Lee, M. -C., Wu, T. -C., Wai, Y. -J., and Damjanov, I., 1983, Pregnancy-related changes in mouse oviduct and uterus revealed by differential binding of fluoresceinated lectins, Histochemistry 79: 365–375.PubMedCrossRefGoogle Scholar
  133. Lin, C. -W., Chapman, C. M., DeLellis, R. A., and Kirley, S., 1978, Immunofluorescent staining of his-taminase (diamine oxidase) in human placenta, J. Histochem. Cytochem. 26: 1021–1025.Google Scholar
  134. Lin, T. M., and Halbert, S. P., 1976, Placental localization of human pregnancy-associated plasma proteins, Science 193: 1249–1252.PubMedCrossRefGoogle Scholar
  135. Lin, T. M., Halbert, S. P., Kiefer, D., Spellacy, W. N., and Gall, S., 1974, Characterization of four human pregnancy-associated plasma proteins, Am. J. Obstet. Gynecol. 118: 223–236.Google Scholar
  136. Lindenberg, S., Lauritsen, J. G., Nielsen, M. H., and Larsen, J. F., 1984, Isolation and culture of human endometrial cells, Fertil. Steril. 41: 650–652.PubMedGoogle Scholar
  137. Linsenmayer, T. F., Fitch, J. M., Schmid, T. M., Zak, N. B., Gibney, E., Sanderson, R., and Mayne, R., 1983, Monoclonal antibodies against chicken type V collagen: Production, specificity and use for immu-nocytochemical localization in embryonic cornea and other organs, J. Cell Biol. 96: 124–132.Google Scholar
  138. Loosfelt, H., Fridlansky, F., Savouret, J. -F., Atger, M., and Milgrom, E., 1981, Mechanism of action of progesterone in the rabbit endometrium. Induction of uteroglobin and its mRNA, J. Biol. Chem. 256: 3465–3470.Google Scholar
  139. MacLaughlin, D. T., Santoro, N. F., Bauer, H. H., Lawrence, D., and Richardson, G. S., 1986, Two-dimensional gel electrophoresis of endometrial protein in human uterine fluids: Qualitative and quantitative analysis, Biol. Reprod. 34: 579–585.PubMedCrossRefGoogle Scholar
  140. Marchi, F., and LeBlond, C. P., 1983, Collagen biogenesis and assembly into fibrils as shown by ultrastructural and [3H]proline radioautographic studies on the fibroblasts of the rat foot pad, Am. J. Anat. 168: 167–197.PubMedCrossRefGoogle Scholar
  141. Marshall, R. N., Underwood, L. E., Voina, S. J., Fonshee, D. B., and Van Wyke, J. J., 1974, Characterization of the insulin and somatomedin C receptors in human placental cell membranes, J. Clin. Endocrinol. Metab. 39: 283–289.PubMedCrossRefGoogle Scholar
  142. Martin, L., 1984, On the source of uterine “luminal fluid” proteins in the mouse, J. Reprod. Fertil. 71: 73–80.PubMedCrossRefGoogle Scholar
  143. Maslar, I. A., and Riddick, D. H., 1979, Prolactin production by human endometrium during the menstrual cycle, Am. J. Obstet. Gynecol. 135: 751–754.PubMedGoogle Scholar
  144. Málinski, C., Biegalski, T., Fogee, W. A., and Kitler, M. E., 1985, Diamine oxidase in developing tissues, in: Structure and Function of Amine Oxidases ( B. Mondovi, ed.), CRC Press, Boca Raton, FL, pp. 179–186.Google Scholar
  145. Masterson, R., Armstrong, E. M., and More, I. A. R., 1975, The cyclical variation in the percentage of ciliated cells in the normal human endometrium, J. Reprod. Fertil. 42: 537–540.CrossRefGoogle Scholar
  146. Matlin, K. S., and Simons, K., 1984, Sorting of an apical plasma membrane glycoprotein occurs before it reaches the cell surface in cultured epithelial cells, J. Cell Sci. 99: 2131–2139.Google Scholar
  147. Maudelonde, T., and Rochefort, H., 1987, A 51k progestin-regulated protein secreted by human endometrial cells in primary culture, J. Clin. Endocrinol. Metab. 64: 1294–1301.Google Scholar
  148. Mazurkiewicz, J. E., Bank, J. F., and Joshi, S. G., 1981, Immunocytochemical localization of a progestagen-associated endometrial protein in the human decidua, J. Clin. Endocrinol. Metab. 52: 1006–1008.PubMedCrossRefGoogle Scholar
  149. McRae, M. A., Newman, G. R., Walker, S. M., and Jasani, B., 1986, Immunohistochemical identification of prolactin and 24k protein in secretory phase endometrium, Fertil. Steril. 45: 643–648.Google Scholar
  150. Misrahi, M., Atger, M., and Milgrom, E., 1987, A novel progesterone-induced messenger RNA in rabbit and human endometria. Cloning and sequence analysis of the complementary DNA, Biochemistry 26: 3975–3982.Google Scholar
  151. Moll, R., Franke, W. W., Schiller, D. L., Geiger, B., and Krepler, R., 1982, The catalog of human cytokeratins: Patterns of expression in normal epithelia, tumors and cultured cells, Cell 31: 11–24.Google Scholar
  152. Moll, R., Levy, R., Czernobilsky, B., Hohlweg-Majert, P., Dallenbach-Hellweg, G., and Franke, W. W., 1983, Cytokeratins of normal epithelia and some neoplasms of the female genital tract, Lab. Invest. 49: 599–610.PubMedGoogle Scholar
  153. More, I. A. R., Armstrong, E. M., Larty, M., and McSeveney, D., 1974, Cyclical changes in the ultrastructure of the normal endometrial stromal cell, Br. J. Obstet. Gynaecol. 81: 337–347.Google Scholar
  154. Moretti-Rojas, I., Fuqua, S. A. W., Montgomery, R. A., and McGuire, W. L., 1988, A cDNA for the estradiol-regulated 24k protein: Control of mRNA levels in MCF-7 cells, Breast Cancer Res. Treat. 11: 155–164.PubMedCrossRefGoogle Scholar
  155. Morize, I., Surcouf, E., Vaney, M. C., Epelboim, Y., Buehner, M., Fridlansky, F., Milgrom, E., andMornon, J. P., 1987, Refinement of the L222j crystal form of oxidised uteroglobin at 1. 34 A resolution, J. Mol. Biol. 194: 725–741.PubMedCrossRefGoogle Scholar
  156. Morris, J. E., and Potter, S. W., 1984, A comparison of developmental changes in surface charge in mouse blastocysts and uterine epithelium using DEAE beads and dextran sulphate in vitro, Dev. Biol. 103: 190–199.PubMedCrossRefGoogle Scholar
  157. Mukherjee, A. B., Ulane, R. E., and Agrawal, A. K., 1982, Role of uteroglobin and transglutaminase in masking antigenicity of implanting rabbit embryos, Am. J. Reprod. Immunol. 2: 135–141.Google Scholar
  158. Mukherjee, D. C., Agrawal, A. K., Marjunath, R., and Mukherjee, A. B., 1983, Suppression of epididymal sperm antigenicity in the rabbit by uteroglobin and transglutaminase in vitro, Science 219: 989–991.PubMedCrossRefGoogle Scholar
  159. Mulholland, J., and Villee, C. A., 1984, Proteins synthesized by the rat endometrium during early pregnancy, J. Reprod. Fertil. 72: 395–400.PubMedCrossRefGoogle Scholar
  160. Muller, B., 1983, Genital tract proteins in the male rabbit. I. Localisation of uteroglobin, Andrologia 15: 380–384.CrossRefGoogle Scholar
  161. Murphy, L. J., Murphy, L. C., and Friesen, H. G., 1987, Estrogen induction of N-myc and c-myc proto-oncogene expression in the rat uterus, Endocrinology 120: 1882–1888.PubMedCrossRefGoogle Scholar
  162. Murray, F. A., Bazer, F. W., Rundell, J. W., Vincent, C. K., Wallace, H. D., and Warnick, A. C., 1971, Developmental failure of swine embryos restricted to the oviductal environment, J. Reprod. Fertil. 24: 445–448.PubMedCrossRefGoogle Scholar
  163. Murray, M. K., and Verhage, H. G., 1985, The immunocytochemical localisation of a cat uterine protein that is estrogen dependent ( CUPED ), Biol. Reprod. 32: 1229–1235.PubMedCrossRefGoogle Scholar
  164. Murray, M. K., Verhage, H. G., Buhi, W. C., and Jaffe, R. C., 1985, The detection and purification of a cat uterine secretory protein that is estrogen dependent ( CUPED ), Biol. Reprod. 32: 1219–1227.PubMedCrossRefGoogle Scholar
  165. Murray, M. K., Verhage, H. G., and Jaffe, R. C., 1986, Quantification of an estrogen-dependent cat uterine protein ( CUPED) in uterine flushings of estrogen-and progesterone-treated ovariectomised cats by radioimmunoassay, Biol. Reprod. 35: 531–536.PubMedCrossRefGoogle Scholar
  166. Nathan, C. F., 1987, Secretory products of macrophages, J. Clin. Invest. 79: 319–326.PubMedCrossRefGoogle Scholar
  167. Nissley, S. P., and Rechler, M. M., 1984, Insulin-like growth factors: Biosynthesis, receptors and carrier proteins, in: Hormonal Proteins and Peptides, Vol. XII ( C. Hoa Li, ed.), Academic Press, New York, pp. 127–203.Google Scholar
  168. O’Brien, T. J., Hardin, J. W., Bannon, G. A., Norris, J. S., and Quirk, J. G., 1986, CA125 antigen in human amniotic fluid and fetal membranes, Am. J. Obstet. Gynecol. 155: 50–55.PubMedGoogle Scholar
  169. Oksenberg, J. R., Mor-Yosef, S., Persitz, E., Schenker, Y., Mozes, E., and Brautbar, C., 1986, Antigen-presenting cells in human decidual tissue, Am. J. Reprod. Immunol. Microbiol. 11: 82–88.Google Scholar
  170. Owens, R. J., and Baralle, F. E., 1986, Exon structure of the collagen binding domain of human fibronectin, FEBS Lett. 204: 318–322.PubMedCrossRefGoogle Scholar
  171. Padykula, H., 1980, Uterine cell biology and phylogenetic considerations: An interpretation, in: Endometrium ( F. A. Kimball, ed.), Spectrum, New York, pp. 25–42.Google Scholar
  172. Panrucker, D. E., Lai, P. C. W., and Lorscheider, F. L., 1983, Distribution of acute phase a2 macroglobulin in rat fetomaternal compartments, Am. J. Physiol. 245: E138–E142.PubMedGoogle Scholar
  173. Papiz, M. Z., Sawyer, L., Eliopoulos, E. C., North, A. C. T., Findlay, J. B. C., Sivaprasadarao, R., Jones, T. A., Newcomer, M. E., and Kraulis, P. J., 1986, The struc ture of p-lactoglobulin and its similarity to plasma retinol-binding proteins, Nature 324: 383–385.PubMedCrossRefGoogle Scholar
  174. Parakkal, P., 1969, Involvement of macrophages in collagen resorption, J. Cell Biol. 41: 345–354.PubMedCrossRefGoogle Scholar
  175. Parr, M. B., and Parr, E. L., 1986, Endocytosis in the rat uterine epithelium at implantation, Ann. N. Y. Acad. Sci. 476: 110–121.PubMedCrossRefGoogle Scholar
  176. Parr, M. B., Tung, H. N., and Parr, E. L., 1986, The ultrastructure of the rat primary decidual zone, Am. J. Anat. 176: 423–436.PubMedCrossRefGoogle Scholar
  177. Pentecost, B. T., and Teng, C. T., 1987, Lactotransferrin is the major estrogen inducible protein of mouse uterine secretions, J. Biol. Chem. 262: 10134–10139.PubMedGoogle Scholar
  178. Perm, A., Sessa, A., and Desiderio, M. A., 1985, Diamine oxidase in regenerating and hypertrophic tissues, in: Structure and Function of Amine Oxidases ( B. Mondovi, ed.), CRC Press, Boca Raton, FL, pp. 179–186.Google Scholar
  179. Pervais, S., and Brew, K., 1985, Hology of 0-lactoglobulin, serum retinol-binding protein and protein HC, Science 228: 335–337.CrossRefGoogle Scholar
  180. Petrunin, D. D., Gryaznova, I. M., Petrunina, Y. A., and Tatarinov, Y. S., 1978, Comparative immu-nochemical and physiochemical characteristics of human chorionic ar and a2-microglobulins, Bull. Exp. Biol. Med. USSR 5: 658–661.CrossRefGoogle Scholar
  181. Petrunin, D. D., Kozljaeva, G. A., Mesrjankina, N. V., and Shevchenko, O. P., 1980, Detection of chorionic a2-microglobulin in the endometrium in the secretory phase of the menstrual cycle and in the male sperm, Akush. Ginekol. ( Mosk. ) 3: 22–23.Google Scholar
  182. Pinto da Silva, P., and Kachar, B., 1982, On tight junction structure, Cell 28: 441–450.CrossRefGoogle Scholar
  183. Ponstingl, H., Nieto, A., and Beato, M., 1978, Amino acid sequence of progesterone-induced rabbit uter-oglobin, Biochemistry 17: 3908–3912.PubMedCrossRefGoogle Scholar
  184. Povoa, G., Enberg, G., Jornvall, H., and Hall, K., 1984, Isolation and characterisation of a somatomedin-binding protein from midterm human amniotic fluid, Eur. J. Biochem. 144: 199–204.Google Scholar
  185. Prives, J., Fulton, A. B., Penman, S., Daniels, M. P., and Christian, C. N., 1982, Interaction of the cytoskeletal framework with acetylcholine receptor on the surface of embryonic muscle cells in culture, J. Cell Biol. 92: 231–236.PubMedCrossRefGoogle Scholar
  186. Psychoyos, A., 1986, Uterine receptivity for nidation, Ann. N. Y. Acad. Sci. 476: 36–42.PubMedCrossRefGoogle Scholar
  187. Rajkumar, K., Bigsby, R., Lieberman, R., and Gerschenson, L. E., 1983a, Uteroglobulin production by cultured rabbit uterine epithelial cells, Endocrinology 112: 1490–1498.PubMedCrossRefGoogle Scholar
  188. Rajkumar, K., Bigsby, R., Lieberman, R., and Gerschenson, L. E., 1983b, Effect of progesterone and 17(3-estradiol on production of uteroglobulin by cultured rabbit uterine epithelial cells, Endocrinology 112: 1499–1505.PubMedCrossRefGoogle Scholar
  189. Ramachandran, G. N., and Reddi, A. H. (eds.), 1976, Biochemistry of Collagen, Plenum Press, New York.Google Scholar
  190. Raub, T. J., Bazer, F. W., and Roberts, R. M., 1985, Localization of the iron transport glycoprotein, uteroferrin, in the porcine endometrium and placenta by using immunocolloidal gold, Anat. Embryol. 171: 253–258.Google Scholar
  191. Rauterberg, J., Jander, R., and Troyer, D., 1986, Type VI collagen. A structural glycoprotein with a collagenous domain, in: Frontiers of Matrix Biology, Vol. 11 ( L. Robert, ed.), S. Karger, Basel, pp. 90–109.Google Scholar
  192. Ricketts, A. P., Scott, D. W., and Bullock, D. W., 1984, Radioiodinated surface proteins of separated cell types from rabbit endometrium in relation to the time of implantation, Cell Tissue Res. 236: 421–429.PubMedCrossRefGoogle Scholar
  193. Riddick, D. H., and Daly, D. C., 1982, Decidual prolactin production in human gestation, Semin. Perinatol. 6: 229–237.Google Scholar
  194. Riddick, D. H., Luciano, A. A., Kusmik, W. E., and Maslar, I. P., 1978, De novo synthesis of prolactin by human decidua, Life Sci. 23: 1913–1921.PubMedCrossRefGoogle Scholar
  195. Rosen, S. W. (ed.), 1986, New placental proteins: Chemistry, physiology and clinical use, Placenta 7: 575–594.Google Scholar
  196. Rutanen, E. M., Koistinen, R., Wahlstrom, T., Bohn, H., Ranta, T., and Seppala, M., 1985, Synthesis of placental protein 12 by human decidua, Endocrinology 116: 1304–1309.PubMedCrossRefGoogle Scholar
  197. Rutanen, E. M., Koistinen, R., Sjoberg, J., Julkunen, M., Wahlstrom, T., Bohn, H., and Seppala, M., 1986, Synthesis of placental protein 12 by human endometrium, Endocrinology 118: 1067–1071.PubMedCrossRefGoogle Scholar
  198. Sakurai, Y., Sullivan, M., and Yamada, Y., 1986, arType IV collagen gene evolved differently from fibrillar collagen genes, J. Biol. Chem. 261: 6654–6657.Google Scholar
  199. Sananes, N., Weiller, S., Baulieu, E. -E., and Le Goascogne, C., 1978, In vitro decidualisation of rat endometrial cells, Endocrinology 103: 86–95.PubMedCrossRefGoogle Scholar
  200. Sasaki, M., Kato, S., Kohno, K., Martin, G. R., and Yamada, Y., 1987, Sequencing of the cDNA encoding the laminin Bx chain reveals a multidomain protein containing cysteine-rich repeats, Proc. Natl. Acad. Sci. U. S. A. 84: 935–939.Google Scholar
  201. Saunders, P. T. K., Renegar, R. H., Raub, T. J., Baumbach, G. A., Atkinson, P. H., Bazer, F. W., and Roberts, R. M., 1985, The carbohydrate structure of porcine uteroferrin and the role of the high mannose chains in promoting uptake by the RES cells of the fetal liver, J. Biol. Chem. 260: 3658–3663.PubMedGoogle Scholar
  202. Sawyer, L., 1987, One fold among many, Nature 327: 659.PubMedCrossRefGoogle Scholar
  203. Schlosnagle, D. C., Bazer, F. W., Tsibris, J. C. M., and Roberts, R. M., 1974, An iron-containing phosphatase induced by progesterone in the uterine fluids, J. Biol. Chem. 249: 7574–7579.PubMedGoogle Scholar
  204. Schmidt, G., Robenek, H., Harrach, B., Glossl, J., Nolte, V., Hormann, H., Richter, H., and Kresse, H., 1987, Interaction of small dermatan sulfate proteoglycan from fibroblasts with fibronectin, J. Cell Biol. 104: 1683–1691.PubMedCrossRefGoogle Scholar
  205. Scott, J. E., and Haigh, M., 1985, Proteoglycan-type I collagen fibril interactions in bone and non-calcifying connective tissues, Biosci. Rep. 5: 71–82.Google Scholar
  206. Seif, M. W., Aplin, J. D., Foden, L. J., and Tindall, V. R., 1988, A novel approach for monitoring the endometrial cycle and detecting ovulation, Am. J. Obstet. Gynecol, (in press).Google Scholar
  207. Seppala, M., Wahlstrom, T., Koskimies, A. I., Tenhunen, A., Rutanen, E. M., Koistinen, R., Huhtaniemi, I., Bohn, H., and Stenman, U. -H., 1984, Human pre-ovulatory follicular fluid, luteinized cells of hyperstimulated pre-ovulatory follicles and corpus luteum contain placental protein 12, J. Clin. Endocrinol. Metab. 58: 505–510.Google Scholar
  208. Sheets, E. E., Tsibris, J. C. M., Cook, N. I., Virgin, S. D., DeMay, R. M., and Spellacy, W. N., 1985, In vitro binding of insulin and epidermal growth factor to human endometrium and endocervix, Am. J. Obstet. Gynecol. 133: 60–65.Google Scholar
  209. Siegfried, J. M., Nelson, K. G., Martin, J. L., and Kaufman, D. G., 1984, Histochemical identification of cultured cells from human endometrium, In Vitro 20: 25–32.Google Scholar
  210. Skorstengaard, K., Jensen, M. S., Sahl, P., Petersen, T. E., and Magnusson, S., 1986, Complete primary structure of bovine plasma fibronectin, Eur. J. Biochem. 161: 441–453.Google Scholar
  211. Sottrup-Jensen, L., Folkerson, J., Kristensen, T., and Tack, B. F., 1984, Partial primary structure of human pregnancy zone protein: Extensive sequence homology with human a2-macroglobulin, Proc. Natl. Acad. Sci. U. S. A. 81: 7353–7357.PubMedCrossRefGoogle Scholar
  212. Southren, A. L., Kobayashi, Y., Brenner, P., and Weingold, A. B., 1965, Diamine oxidase activity in human maternal and fetal plasma and tissues at parturition, J. Appl. Physiol. 20: 1048–1051.PubMedGoogle Scholar
  213. Spiegel, S., Blumenthal, R., Fishman, P. H., and Handler, J. S., 1985, Gangliosides do not move from apical to basolateral plasma membrane in cultured epithelial cells, Biochim. Biophys. Acta 821: 310–318.PubMedCrossRefGoogle Scholar
  214. Steinert, P. M., Steven, A. C., and Roop, D. R., 1985, The molecular biology of intermediate filaments, Cell 42: 411–419.PubMedCrossRefGoogle Scholar
  215. Strinden, S. T., and Shapiro, S. S., 1983, Progesterone-altered secretory proteins from cultured human endometrium, Endocrinology 112: 862–870.PubMedCrossRefGoogle Scholar
  216. Surani, M. A. H., 1977, Qualitative and quantitative examination of the proteins of rat uterine luminal fluid during pro-oestrus and pregnancy and comparison with those of serum, J. Reprod. Fertil. 50: 281–287.PubMedCrossRefGoogle Scholar
  217. Sutcliffe, R. G., Brock, D. J. H., Nicholson, L. V. B., and Dunn, E., 1978, Fetal-and uterine-specific antigens in human amniotic fluid, J. Reprod. Fertil 54: 86–90.Google Scholar
  218. Sutcliffe, R. G., Bolton, A. E., Sharp, F., Nicholson, L. V. B., and Mackinnon, R., 1980a, Purification of human alpha uterine protein, J. Reprod. Fertil. 58: 435–442.Google Scholar
  219. Sutcliffe, R. G., Kukulska-Langlands, B. M., Coggins, J. R., Hunter, J. B., and Gore, C. H., 1980b, Studies on human pregnancy-associated plasma protein A. Purification by affinity chromatography and structural comparison with a2-macroglobulin, Biochem, J. 191: 799–809.Google Scholar
  220. Sutcliffe, R. G., Joshi, S. G., Paterson, W. F., and Bank, J. F., 1982, Serological identity between human alpha uterine protein and human progestagen-dependent endometrial protein, J. Reprod. Fertil. 65: 207–209.PubMedCrossRefGoogle Scholar
  221. Suzuki, M., Ogawa, M., Tamada, T., Nagura, H., and Watanabe, K., 1984, Immunohistochemical localisation of secretory components and Ig A in the human endometrium in relation to the menstrual cycle, Acta Histochem. Cytochem. 17: 223–229.Google Scholar
  222. Tabibzadeh, S. S., Gerber, M. A., and Satyaswaroop, P. G., 1986, Induction of HLA-DR antigen expression in human endometrial epithelial cells in vitro by recombinant 7-interferon, Am. J. Pathol. 125: 90–96.PubMedGoogle Scholar
  223. Takahashi, H., Nabeshima, Y., Ogata, K., and Takeuchi, S., 1984, Molecular cloning and nucleotide sequence of DNA complementary to human decidual prolactin mRNA, J. Biochem. ( Tokyo ) 95: 1491–1499.Google Scholar
  224. Takahashi, Y. I., Smith, J. E., Winick, M., and Goodman, D. S., 1975, Vitamin A deficiency and fetal growth and development in the rat, J. Nutr. 105: 1299–1310.PubMedGoogle Scholar
  225. Tancredi, T., Temussi, P. A., and Beato, M., 1982, Interaction of oxidised and reduced uteroglobin with progesterone, Eur. J. Biochem. 122: 101–104.Google Scholar
  226. Tansey, T. R., and Padykula, H. A., 1978, Cellular responses to experimental inhibition of collagen degrada-tion in the postpartum rat uterus, Anat. Ree. 191: 287–296.CrossRefGoogle Scholar
  227. Teng, C. T., Walker, M. P., Bhattacharyya, S. N., Klapper, D. G., DiAugustine, R. P., and McLachlan, J. A., 1986, Purification and properties of an oestrogen-stimulated mouse uterine glycoprotein, Biochem. J. 240: 413–422.PubMedGoogle Scholar
  228. Thie, M., Bochskanl, R., and Kirchner, C., 1984, Purification and immunohistology of a glycoprotein secreted from the rabbit uterus before implantation, Cell Tissue Res. 237: 155–160.PubMedCrossRefGoogle Scholar
  229. Thie, M., Bochskanl, R., and Kirchner, C., 1986, Glycoproteins in rabbit uterus during implantation, Histo-chemistry 84: 73–79.Google Scholar
  230. Tourville, D. R., Ogra, S. S., Lippes, J., and Tomasi, T. B., 1970, The human female reproductive tract: Immunohistological localization of 7A, 7G, 7M, secretory “pieces,” and lactoferrin, Am. J. Obstet. Gynecol. 108: 1102–1108.PubMedGoogle Scholar
  231. Travers, M. T., and Knowler, J. T., 1987, Estrogen-induced expression of oncogenes in the immature rat uterus, FEBS Lett. 211: 27–30.PubMedCrossRefGoogle Scholar
  232. Trüeb, B., and Winterhalter, K., 1986, Type VI collagen is composed of a 200 kd subunit and two 140 kd subunits, EMBO J. 5: 2815–2819.PubMedGoogle Scholar
  233. Tsai, M. -J., Bullock, D. W., and Woo, S. L. C., 1983, Hormonal regulation of rabbit uteroglobin gene transcription, Endocrinology 112: 871–876.PubMedCrossRefGoogle Scholar
  234. Van Leuven, F., Cassiman, J. J., and Van der Berghe, H., 1986, Human pregnancy zone protein and a2-macroglobulin. High affinity binding of complexes to the same receptor on fibroblasts and characterisation by monoclonal antibodies, J. Biol. Chem. 261: 16622–16625.PubMedGoogle Scholar
  235. Van Meer, G., and Simons, K., 1986, The function of tight junctions in maintaining differences in lipid composition between apical and basolateral cell surface domains of MDCK cells, EMBO J. 5: 1455–1464.PubMedGoogle Scholar
  236. van Veen, H. A., and Peereboom-Stegeman, J. H. J. C., 1987, The influence of the estrous cycle on the volume density and appearance of collagen containing vacuoles in fibroblasts of the rat uterus, Virchows Arch. [B] 53: 23–31.CrossRefGoogle Scholar
  237. Vladimirsky, F., Chen, L., Amsterdam, A., Zur, U., and Lindner, H. R., 1977, Differentiation of decidual cells in cultures of rat endometrium, J. Reprod. Fertil. 49: 61–68.PubMedCrossRefGoogle Scholar
  238. Von der Mark, K., and Kühl, U., 1985, Laminin and its receptor, Biochim. Biophys. Acta 823: 147–181.Google Scholar
  239. Wahlström, T., and Seppälä, M., 1984, PP12 is induced in the endometrium by progesterone, Fertil. Steril. 41: 781–784.Google Scholar
  240. Wahlström, T., Teisner, B., and Folkersen, J., 1981, Tissue localisation of pregnancy-associated plasma protein A ( PAPP-A) in normal placenta, Placenta 2: 253–258.Google Scholar
  241. Waites, G. T., Udagawa, Y., Armstrong, S. S., Sewell, H. F., Bell, S. C., and Thomson, A. W., 1985, Immunohistochemical localisation of mouse a j-pregnancy associated protein (arPAP) in pregnant mice: Relationship between serum a1-PAP levels and incidence of positive cells, J. Reprod. Immunol. 8: 173–185.CrossRefGoogle Scholar
  242. Weil, D., Bernard, M., Gargano, S., and Ramirez, F., 1987, The pro a2(V) collagen gene is evolutionarily related to the major fibril-forming collagens, Nucleic Acids Res. 15: 181–198.PubMedCrossRefGoogle Scholar
  243. Weisburger, W. R., Mendelsohn, G., Eggleston, J. C., and Baylin, S. B., 1978, Immunohistochemical localisation of histaminase (diamine oxidase) in decidual cells of human placenta, Lab. Invest. 38: 703–706.PubMedGoogle Scholar
  244. Wewer, U. M., Faber, M., Liotta, L. A., and Albrechtsen, R., 1985, Immunochemical and ultrastructural assessment of the nature of the pericellular basement membrane of human decidual cells, Lab. Invest. 53: 624–633.Google Scholar
  245. Wewer, U. M., Damjanov, A., Weiss, J., Liotta, L. A., and Damjanov, I., 1986, Mouse endometrial stromal cells produce basement membrane components, Differentiation 32: 49–58.PubMedCrossRefGoogle Scholar
  246. Wheeler, C., Komm, B. S., and Lyttle, C. R., 1987, Estrogen regulation of protein synthesis in the immature rat uterus: The effects of progesterone on proteins released into the medium during in vitro incubations, Endocrinology 120: 919–923.PubMedCrossRefGoogle Scholar
  247. Whyte, A., and Allen, W. R., 1985, Equine endometrium at preimplantation stages of pregnancy has specific glycosylated regions, Placenta 6: 537–542.PubMedCrossRefGoogle Scholar
  248. Whyte, A., and Robson, T., 1984, Saccharides localised by fluorescent lectins on trophectoderm and endometrium prior to implantation in pigs, sheep and equids, Placenta 5: 533–540.PubMedCrossRefGoogle Scholar
  249. Whyte, A., Tang, C., Rutter, F., and Heap, R. B., 1987, Lectin-binding characteristics of mouse oviduct and uterus associated with pregnancy block by autologous antiprogesterone monoclonal antibody, J. Reprod. Immunol. 11: 209–220.PubMedCrossRefGoogle Scholar
  250. Wienke, E. C., Cavazos, F., Hall, D. G., and Lucas, F. V., 1968, Ultrastructure of the human endometrial stromal cell during the menstrual cycle, Am. J. Obstet. Gynecol. 102: 65–77.PubMedGoogle Scholar
  251. Woessner, J. F., 1977, A latent form of collagenase in the involuting rat uterus and its activation by a serine proteinase, Biochem. J. 161: 535–543.PubMedGoogle Scholar
  252. Wynn, R. M., 1974, Ultrastructural development of the human decidua, Am. J. Obstet. Gynecol. 118: 652–670.PubMedGoogle Scholar
  253. Wynn, R. M., 1977, Histology and ultrastructure of the human endometrium, in: Biology of the Uterus ( R. M. Wynn, ed.), Plenum Press, New York, pp. 341–376.CrossRefGoogle Scholar
  254. Yen, Y., Lee, M. -C., Salzmann, M., and Damjanov, I., 1986, Lectin binding sites on human endocervix: A comparison with secretory and proliferative endometrium, Anat. Rec. 215: 262–266.Google Scholar
  255. Zimmerman, K. A., Yancopoulos, G. D., Collum, R. G., Smith, R. K., Kohl, N. E., Denis, K. A., Nau, M. M., Witte, O. N., Toran-Allerand, D., Gee, C. E., Minna, J. D., and Alt, F. W., 1986, Differential expression of myc family genes during development, Nature 319: 780–783.PubMedCrossRefGoogle Scholar
  256. Zorn, T. M. T., Bevilacqua, E. M. A. F., and Abrahamson, P. A., 1986, Collagen remodeling during decidualization in the mouse, Cell Tissue Res. 244: 443–448.PubMedCrossRefGoogle Scholar

Copyright information

© Plenum Publishing Corporation 1989

Authors and Affiliations

  • John D. Aplin
    • 1
    • 2
    • 3
  1. 1.Department of Obstetrics and GynaecologyUniversity of ManchesterManchesterEngland
  2. 2.Department of BiochemistryUniversity of ManchesterManchesterEngland
  3. 3.Department of Molecular BiologyUniversity of ManchesterManchesterEngland

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