Extracellular Matrix Remodeling at Implantation: Role of Hyaluronan

  • Jeremy J. G. Brown
  • Virginia E. Papaioannou
Conference paper
Part of the Serono Symposia USA book series (SERONOSYMP)

Abstract

The establishment of pregnancy in species with interstitial, hemochorial placentation (e.g., mouse and human) requires that following displacement of the uterine epithelium, trophoblast cells of the periimplantation blastocyst penetrate the underlying stroma. There, they tap into the maternal vasculature, generating a fetomaternal interface for nutrient and waste exchange. That trophoblast is an intrinsically invasive tissue in these species has been convincingly demonstrated by its behavior in ectopic sites or in the lumen of a nonreceptive uterus from which the epithelium has been stripped (1, 2). In the absence of an appropriate remodeling response by the host tissue, proliferation and invasion proceed in an uncontrolled and unrestricted manner, resulting in choriocarcinoma. In the normal in vivo condition, however, the attachment of a blastocyst to the luminal epithelium of a receptive uterus initiates a cascade of new gene transcription events, resulting in differentiation, or decidualization, of the underlying stroma, such that the maternal tissue becomes resistant to invasion. The trophoblast’s proliferative and invasive potential is consequently limited by the uterine microenvironment, and appropriate differentiative programs are set in motion for the development of a normal, functioning placenta.

Keywords

Polysaccharide Luminal Progesterone Streptomyces Oligosaccharide 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Kirby DRS. The “invasiveness” of trophoblast. In: Park WW, ed. The early conceptus, normal and abnormal. Edinburgh: St. Andrews Press, 1965:68–74.Google Scholar
  2. 2.
    Sherman MI, Wudl LW. The implanting mouse blastocyst. In: Poste G, Nicolson GL, eds. The cell surface in animal embryogenesis and development. Amsterdam: Elsevier/North Holland, 1976:81–125.Google Scholar
  3. 3.
    Hunt JS, Pollard JW. Macrophages in the uterus and placenta. In: Gordon S, Russell SW, eds. Macrophages and macrophage activation, current topics in microbiology and immunology. New York: Springer-Verlag, 1992:36–63.Google Scholar
  4. 4.
    Nose A, Takeichi M. A novel cadherin cell adhesion molecule: its expression patterns associated with implantation and organogenesis of mouse embryos. J Cell Biol 1986;103:2649–58.PubMedCrossRefGoogle Scholar
  5. 5.
    Winterhager E, Grummer R, Jahn E, Willecke K, Traub O. Spatial and temporal expression of connexin26 and connexin43 in rat endometrium during trophoblast invasion. Dev Biol 1993;157:399–409.PubMedCrossRefGoogle Scholar
  6. 6.
    Lala PK, Graham CH. Mechanisms of trophoblast invasiveness and their control: the role of proteases and protease inhibitors. Cancer Metastasis Rev 1990;9:369–79.PubMedCrossRefGoogle Scholar
  7. 7.
    Behrendsten O, Alexander CM, Werb Z. Metalloproteinases mediate extra-cellular matrix degradation by cells from mouse blastocyst outgrowths. Development 1992;114:447–56.Google Scholar
  8. 8.
    Bischof P, Martelli M, Campana A. Matrix metalloproteinases and inhibitors dialog: potential role in the implantation process. In: Gianaroli L, Campana A, Trounson AO, eds. Implantation in mammals. New York: Raven Press, 1993;91:151–65.Google Scholar
  9. 9.
    Grinnel F, Head JR, Hoffpauir J. Fibronectin and cell shape in vivo: studies on the endometrium during pregnancy. J Cell Biol 1982;94:597–606.CrossRefGoogle Scholar
  10. 10.
    Wewer UM, Damjanov A, Weiss J, Liotta LA, Damjanov I. Mouse endo­metrial stromal cells produce basement membrane components. Differentia­tion 1986;32:49–58.CrossRefGoogle Scholar
  11. 11.
    Glasser SR, Lampelo S, Munir MI, Julian JA. Expression of desmin, laminin and fibronectin during in situ differentiation (decidualization) of rat uterine stromal cells. Differentiation 1987;35:132–42.PubMedCrossRefGoogle Scholar
  12. 12.
    Karkavelas G, Kefalides NA, Amenta PS, Martinez-Hernandez A. Com­parative ultrastructural localization of collagen types III, IV, VI and laminin in rat uterus and kidney. J Ultrastruct Mol Struct Res 1988;100:137–55.PubMedCrossRefGoogle Scholar
  13. 13.
    Mulholland J, Aplin JD, Ayad S, Hong L, Glasser SR. Loss of collagen type VI from rat endometrial stroma during decidualization. Biol Reprod 1992; 46:1136–43.PubMedCrossRefGoogle Scholar
  14. 14.
    Aplin JD, Charlton AK, Ayad S. An immunohistochemical study of human endometrial extracellular matrix during the menstrual cycle and the first trimester of pregnancy. Cell Tissue Res 1988;253:231–40.PubMedCrossRefGoogle Scholar
  15. 15.
    Farrar JD, Carson DD. Differential temporal and spatial expression of mRNA encoding extracellular matrix components in decidua during the periimplantation period. Biol Reprod 1992;46:1095–108.PubMedCrossRefGoogle Scholar
  16. 16.
    Senior PV, Crichley DR, Beck F, Walker RA, Varley JM. The localization of laminin mRNA and protein in the postimplantation embryo and placenta of the mouse: an in situ hybridization and immunohistochemical study. Development 1988;104:431–46.PubMedGoogle Scholar
  17. 17.
    Julian JA, Chiquet-Ehrismann R, Erickson HP, Carson DD. Tenascin is induced at implantation sites in the mouse uterus and interferes with epithelial cell adhesion. Development 1994;120:661–71.PubMedGoogle Scholar
  18. 18.
    Michie HJ, Head JR. Tenascin in pregnant and non-pregnant rat uterus: unique spatio-temporal expression during decidualization. Biol Reprod 1994; 50:1277–86.PubMedCrossRefGoogle Scholar
  19. 19.
    Aplin JD, Charlton AK. The role of matrix macromolecules in the invasion of decidua by trophoblast: model studies using BeWo cells. Troph Res 1990;4:139–58.Google Scholar
  20. 20.
    Glasser SR, Mulholland J, Mani SK, et al. Blastocyst-endometrial relation­ships: reciprocal interactions between uterine epithelium and stromal cells and blastocysts. Troph Res 1991;5:229–80.Google Scholar
  21. 21.
    Brown JJG, Papaioannou VE. Distribution of hyaluronan in the mouse endometrium during the periimplantation period of pregnancy. Differentiation 1992;52:61–8.PubMedCrossRefGoogle Scholar
  22. 22.
    Papaioannou VE, Ebert KM. Comparative aspects of embryo manipulation in mammals. In: Rossant J, Pedersen R, eds. Experimental approaches to mammalian embryonic development. Cambridge: Cambridge University Press, 1986:67–96.Google Scholar
  23. 23.
    Redline RW, Shea CM, Papaioannou VE, Lu CY. Defective anti-listerial responses in deciduoma of pseudopregnant mice. Am J Pathol 1988;133: 485–97.PubMedGoogle Scholar
  24. 24.
    Redline RW, McKay DB, Vasquez MA, Papaioannou VE, Lu CY. Macrophage functions are regulated by the substratum of murine decidual stromal cells. J Clin Invest 1990;85:1951–8.PubMedCrossRefGoogle Scholar
  25. 25.
    Balazs EA, Laurent TC, Jeanloz RW. Nomenclature of hyaluronic acid. Biochem J 1986;235:903.PubMedGoogle Scholar
  26. 26.
    Comper WD, Laurent TC. Physiological function of connective tissue polysac­charides. Physiol Rev 1978;58:255–315.PubMedGoogle Scholar
  27. 27.
    Gallagher JT. The extended family of proteoglycans: social residents of the pericellular zone. Curr Opin Cell Biol 1989;1:1201–18.PubMedCrossRefGoogle Scholar
  28. 28.
    Toole BP. Glycosaminoglycans in morphogenesis. In: Hay E, ed. Cell biology of extracellular matrix. New York: Plenum Press, 1981:259–94.Google Scholar
  29. 29.
    Toole BP. Hyaluronan and its binding proteins, the hyaladherins. Curr Opin Cell Biol 1990;2:839–44.PubMedCrossRefGoogle Scholar
  30. 30.
    Toole BP. Proteoglycans and hyaluronan in morphogenesis and differentiation. In: Hay E, ed. Cell biology of extracellular matrix. 2nd ed. New York: Plenum Press, 1991:305–41.CrossRefGoogle Scholar
  31. 31.
    Iozzo RV. Proteoglycans: structure, function and role in neoplasia. Lab Invest 1985;53:373–96.PubMedGoogle Scholar
  32. 32.
    Carson DD, Dutt A, Tang JP. Glycoconjugate synthesis during early pregnancy: hyaluronate synthesis and function. Dev Biol 1987;120:228–35.PubMedCrossRefGoogle Scholar
  33. 33.
    Jacobs AL, Carson DD. Proteoglycan synthesis and metabolism by mouse uterine stroma cultured in vitro. J Biol Chem 1991;266:15464–73.PubMedGoogle Scholar
  34. 34.
    Enders AC, Chavez DJ, Schlafke S. Comparisons of implantation in utero and in vitro. In: Glasser SR, Bullock DW, eds. Cellular and molecular aspects of implantation. New York: Plenum Press, 1981:365–82.Google Scholar
  35. 35.
    Glasser SR. Biochemical and structural changes in uterine and endometrial cell types following natural or artificial deciduogenic stimuli. Troph Res 1990;4:377–416.Google Scholar
  36. 36.
    Sunderland CA, Redman CWG, Stirrat GM. Monoclonal antibodies to human syncytiotrophoblast. Immunology 1981;43:541–6.PubMedGoogle Scholar
  37. 37.
    Sunderland CA, Bulmer JN, Luscombe M, Redman CWG, Stirrat GM. Immunohistological and biochemical evidence for a role for hyaluronic acid in the growth and development of the placenta. J Reprod Immunol 1985;8: 197–212.PubMedCrossRefGoogle Scholar
  38. 38.
    Cidadao AJ, Thorsteinsdottir S, David-Ferreira JF. Immunocytochemical study of tissue distribution and hormonal control of chondroitin-, dermatan- and keratan-sulfates from rodent uterus. Eur J Cell Biol 1990;52:105–16.PubMedGoogle Scholar
  39. 39.
    Ohya T, Kaneko Y. Novel hyaluronidase from Streptomyces. Biochim Biophys Acta 1970;198:607–9.PubMedGoogle Scholar
  40. 40.
    Derby MA, Pintar JE. The histochemical specificity of Streptomyces hyaluronidase and chondroitinase ABC. Histochem J 1978;10:529–47.PubMedCrossRefGoogle Scholar
  41. 41.
    Ripellino JA, Kilinger MM, Margolis RU, Margolis RK. The hyaluronic acid binding region as a specific probe for the localization of hyaluronic acid in tissue sections. J Histochem Cytochem 1985;33:1066–86.CrossRefGoogle Scholar
  42. 42.
    Green SJ, Tarone G, Underhill CB. Distribution of hyaluronate and hyaluronate receptors in the adult lung. J Cell Sci 1988;89:145–56.Google Scholar
  43. 43.
    Girard N, Courel MN, Delpech A, Bruckner G, Delpech B. Staining of hyaluronan in rat cerebellum with a hyaluronectin-antihyaluronectin immune complex. Histochem J 1992;24:21–4.PubMedCrossRefGoogle Scholar
  44. 44.
    Krehbiel RH. Cytological studies of the decidual reaction in the rat during early pregnancy and in the production of deciduomata. Physiol Zool 1937; 10:212–23.Google Scholar
  45. 45.
    Finn CA, Martin L. Patterns of cell division in the mouse uterus during early pregnancy. J Endocrinol 1967;39:593–7.PubMedCrossRefGoogle Scholar
  46. 46.
    Patan S, Alvarez MJ, Schittny JC, Burri PH. Intussusceptive microvascular growth: a common alternative to capillary sprouting. Arch Histol Cytol 1992 ; 55 (suppl) : 65–75.PubMedCrossRefGoogle Scholar
  47. 47.
    Gross JL, Moscetelli D, Rifkin DB. Increased capillary endothelial cell protease activity in response to angiogenic stimuli. Proc Natl Acad Sci USA 1983;80:2623–7.PubMedCrossRefGoogle Scholar
  48. 48.
    Folkman J, Klagsbrun M. Angiogenic factors. Science 1987;235:442–7.PubMedCrossRefGoogle Scholar
  49. 49.
    Klagsbrun M, D’Amore PA. Regulators of angiogenesis. Annu Rev Physiol 1991;53:217–39.PubMedCrossRefGoogle Scholar
  50. 50.
    Ausprunk DH. Distribution of hyaluronic acid and sulfated glycosaminogly­cans during blood-vessel development in the chick chorioallantoic membrane. Am J Anat 1986;177:313–31.PubMedCrossRefGoogle Scholar
  51. 51.
    Brecht M, Mayer U, Schlosser E, Prehm P. Increased hyaluronate synthesis is required for fibroblast detachment and mitosis. Biochem J 1986;239:445–50.PubMedGoogle Scholar
  52. 52.
    West DC, Kumar S. Hyaluronan and angiogenesis. Ciba Found Symp 1989; 143:187–207.PubMedGoogle Scholar
  53. 53.
    Bernfield M, Banerjee SD, Koda JE, Rapraeger AC. Remodeling of the basement membrane: morphogenesis and maturation. Ciba Found Symp 1984;108:179–96.PubMedGoogle Scholar
  54. 54.
    Fraser JRE, Laurent TC. Turnover and metabolism of hyaluronan. Ciba Found Symp 1989;143:41–53.PubMedGoogle Scholar
  55. 55.
    Culty M, Nguyen HA, Underhill CB. The hyaluronan receptor (CD44) participates in the uptake and degradation of hyaluronan. J Cell Biol 1992; 116:1055–62.PubMedCrossRefGoogle Scholar
  56. 56.
    Turley EA. Hyaluronan and cell locomotion. Cancer Metastasis Rev 1992; 11:21–30.PubMedCrossRefGoogle Scholar
  57. 57.
    Stern M, Chang A, Stern R. Liver hyaluronidase localized to endothelial cells. Mol Cell Biol 1992;3(suppl):67a.Google Scholar
  58. 58.
    Aruffo A, Stamenkovic I, Melnick M, Underhill CB, Seed B. CD44 is the principal cell surface receptor for hyaluronate. Cell 1990;61:1303–13.PubMedCrossRefGoogle Scholar
  59. 59.
    Underhill CB. CD44: the hyaluronan receptor. J Cell Sci 1992;103:293–8.PubMedGoogle Scholar
  60. 60.
    Lesley J, Hyman R, Kincade PW. CD44 and its interaction with extracellular matrix. Adv Immunol 1993;54:271–335.PubMedCrossRefGoogle Scholar
  61. 61.
    Wheatley SC, Isacke CM, Crossley PH. Restricted expression of the hyaluronan receptor, CD44, during postimplantation mouse embryogenesis suggests key roles in tissue formation and patterning. Development 1993; 119:295–306.PubMedGoogle Scholar
  62. 62.
    Brown JJG, Papaioannou VE. Ontogeny of hyaluronan secretion during early mouse development. Development 1993;117:483–92.PubMedGoogle Scholar
  63. 63.
    Faassen AE, Schrager JA, Klein DJ, Oegema TR, Couchman JR, McCarthy JB. A cell surface chondroitin sulphate proteoglycan, immunologically related to CD44, is involved in type I collagen-mediated melanoma cell motility and invasion. J Cell Biol 1992;116:521–31.PubMedCrossRefGoogle Scholar
  64. 64.
    Jalkanen S, Jalkanen M. Lymphocyte CD44 binds the COOH-terminal heparin-binding domain of fibronectin. J Cell Biol 1992;116:817–25.PubMedCrossRefGoogle Scholar
  65. 65.
    Mijake K, Underhill CB, Lesley J, Kincade PW. Hyaluronate can function as a cell adhesion molecule and CD44 participates in hyaluronate recognition. J Exp Med 1990;172:69–75.CrossRefGoogle Scholar
  66. 66.
    Stewart CL, Kaspar P, Brunet LJ, et al. Blastocyst implantation depends on maternal expression of leukaemia inhibitory factor. Nature 1992;359:76–9.PubMedCrossRefGoogle Scholar
  67. 67.
    Ruoslahti E, Yamaguchi Y. Proteoglycans as modulators of growth factor activities. Cell 1991;64:867–9.PubMedCrossRefGoogle Scholar
  68. 68.
    Nathan C, Sporn M. Cytokines in context. J Cell Biol 1991;113:981–6.PubMedCrossRefGoogle Scholar
  69. 69.
    Klagsbrun M, Baird A. A dual receptor system is required for basic fibroblast growth factor activity. Cell 1991;67:229–31.PubMedCrossRefGoogle Scholar
  70. 70.
    Tanaka Y, Adams DH, Hubscher S, Hirano H, Siebenlist U, Shaw S. T-cell adhesion induced by proteoglycan-immobilized cytokine MIP-1ß. Nature 1993;361:79–82.PubMedCrossRefGoogle Scholar
  71. 71.
    Alho AM, Underhill CB. The hyaluronate receptor is preferentially expressed on proliferating epithelial cells. J Cell Biol 1989;108:1557–65.PubMedCrossRefGoogle Scholar
  72. 72.
    Turley EA, Moore D. Hyaluronate binding proteins also bind to fibronectin, laminin and collagen. Biochem Biophys Res Commun 1984;121:808–14.PubMedCrossRefGoogle Scholar
  73. 73.
    Turley EA. Hyaluronic acid stimulates protein kinase activity in intact cells and in an isolated protein complex. J Biol Chem 1989;264:8951–5.PubMedGoogle Scholar
  74. 74.
    Prehm P. Identification and regulation of the eukaryotic hyaluronate synthase. Ciba Found Symp 1989;149:21–40.Google Scholar
  75. 75.
    Klewes L, Turley EA, Prehm P. The hyaluronate synthase from a eukaryotic cell line. Biochem J 1993;290:791–5.PubMedGoogle Scholar
  76. 76.
    Hayashi M, Nakajima Y, Fishman WH. The cytologic demonstration of ß­glucuronidase employing napthol AS-BI glucuronide and hexazonium pararosanilin; a preliminary report. J Histochem Cytochem 1964;12:293–7.PubMedCrossRefGoogle Scholar
  77. 77.
    Hayashi M. Histochemical demonstration of N-acetyl-(3-glucosaminidase employing napthol AS-BI N-acetyl-(3-glucosaminide as substrate. J Histochem Cytochem 1965;13:355–60.PubMedCrossRefGoogle Scholar
  78. 78.
    Feder N. Solitary cells and enzyme exchange in tetraparental mice. Nature 1976;263:67–9.PubMedCrossRefGoogle Scholar
  79. 79.
    Underhill CB, Nguyen HA, Shizari M, Culty M. CD44 positive macro­phages take up hyaluronan during lung development. Dev Biol 1993;155: 324–36.PubMedCrossRefGoogle Scholar
  80. 80.
    Schlafke S, Welsh AO, Enders AC. Penetration of the basal lamina of the uterine luminal epithelium during implantation in the rat. Anat Rec 1985; 212:47–56.PubMedCrossRefGoogle Scholar
  81. 81.
    Welsh AO, Enders AC. Light and electron microscopic examination of the mature decidual cells of the rat with emphasis on the antimesometrial decidua and its degeneration. Am J Anat 1985;172:1–29.PubMedCrossRefGoogle Scholar
  82. 82.
    Bourguignon LYW, Kalomiris EL, Lokeshwar VB. Acylation of the lymphoma transmembrane glycoprotein, GP85, may be required for GP85­ankyrin interaction. J Biol Chem 1991;266:11761–5.PubMedGoogle Scholar
  83. 83.
    Kielty CM, Whittaker SP, Grant ME, Shuttleworth CA. Type VI collagen microfibrils: evidence for a structural association with hyaluronan. J Cell Biol 1992;118:979–90.PubMedCrossRefGoogle Scholar
  84. 84.
    Linsenmayer TF. Collagen. In: Hay ED, ed. Cell biology of extracellular matrix. 2nd ed. New York: Plenum Press, 1991:7–44.CrossRefGoogle Scholar
  85. 85.
    Jeffrey JJ. Collagen synthesis and degradation in the uterine deciduoma: regulation of collagenase activity by progesterone. Collagen Relat Res 1981; 1:257–68.Google Scholar
  86. 86.
    Myers DB, Clark DE, Hurst PR. Decreased collagen concentration in rat uterine implantation sites compared with non-implantation tissue at days 6–11 of pregnancy Reprod Fertil Dev 1990;2:607–12.Google Scholar
  87. 87.
    Inoue S. Ultrastructure of basement membranes. Int Rev Cytol 1989;117: 57–98.PubMedCrossRefGoogle Scholar
  88. 88.
    Rider V, Carlone DL, Witrock D, Cai C, Oliver N. Uterine fibronectin mRNA content and localization are modulated during implantation. Dev Dynam 1992;195:1–14.CrossRefGoogle Scholar
  89. 89.
    Thomas T, Dziadek M. Expression of laminin and nidogen genes during the postimplantation development of the mouse placenta. Biol Reprod 1993; 49:1251–9.PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag New York, Inc. 1995

Authors and Affiliations

  • Jeremy J. G. Brown
  • Virginia E. Papaioannou

There are no affiliations available

Personalised recommendations