Skip to main content
Log in

Apical plasma membrane-bound enzymes of rabbit uterine epithelium

Pattern changes during the periimplantation phase

  • Published:
Histochemistry Aims and scope Submit manuscript

Summary

In order to monitor changes in the apical cell membrane of rabbit uterine epithelium which are postulated to be a precondition for trophoblast attachment, the marker enzymes: alkaline phosphatase, aminopeptidase M, γ-glutamyl transferase and dipeptidyl peptidase IV were investigated during the periimplantation phase. Endometrium of early pregnancy (implantation chamber, interblastocyst endometrium; 5–8 days post coitum, d p.c.) was compared with specimens obtained at hCG-induced pseudopregnancy (p. hCG) to distinguish between membrane changes regulated by maternal plasma steroid hormones and such which might be induced locally by blastocyst-derived signals.

All enzymes tested showed their main activity at 5 d p.c./p. hCG. The weakest reaction in this series of stages was generally found at 8 d p.c. (interblastocyst segments) or at 8 d p. hCG. In contrast to the rest of the epithelium, the implantation chamber retained high activity of dipeptidyl peptidase IV, and the activity of alkaline phosphatase even raised here again at 7 and 8 d p.c. indicating a direct local influence of the blastocyst on the luminal epithelium. The results suggest that 1) considerable changes occur in the composition of the apical plasma membrane of the uterine epithelium when the endometrium enters the “receptive state”, 2) the overall trend is towards a loss of apical-type characteristics of this membrane domain and 3) the changes are modulated both systemically (by plasma steroid hormone levels) and locally by signals from the implanting blastocyst.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

d p.c.:

days post coitum

d. p. hCG:

days post hCG injection

hCG:

human chorionic gonadotropin

aP:

alkaline phosphatase

ATPase:

adenosine triphosphatase

Ca2+-ATPase:

Ca2+-activated adenosine triphosphatase

APM:

aminopeptidase M

GGT:

γ-glutamyl transferase

DPP IV:

dipeptidyl peptidase IV

PCMB:

p-chloromercuric benzoate

DFP:

di-isopropylfluorophosphate

DMF:

dimethylformamide

References

  • Anderson TL, Hoffman LH (1984) Alterations in epithelial glycocalyx of rabbit uteri during early pseudopregnancy and pregnancy, and following ovariectomy. Am J Anat 171:321–334

    Google Scholar 

  • Anderson TL, Olson GE, Hoffman LH (1986) Stage-specific alterations in the apical membrane glycoproteins of endometrial epithelial cells related to implantation in rabbits. Biol Reprod 34:701–720

    Google Scholar 

  • Ando T, Fujimoto K, Mayahara H, Miyajima H, Ogawa K (1981) A new one-step method for the histochemistry and cytochemistry of Ca2+-ATPase activity. Acta Histochem Cytochem 14:705–726

    Google Scholar 

  • Beier HM (1973) Die hormonelle Steuerung der Uterussekretion und frühen Embryonalentwicklung des Kaninchens. Habilitationsschrift, Universität Kiel

  • Beier HM, Kühnel W, Petry G (1970) Uterine secretion proteins as extrinsic factors in preimplantation development. Adv Biosci 6:165–189

    Google Scholar 

  • Birge SJ (1981) Intestinal phosphate transport and alkaline phosphatase. In: Calcium and phosphate transport across biomembranes. Academic Press, New York, pp 181–184

    Google Scholar 

  • Blanke H-J, Graf R (1985) Zytochemische Untersuchungen von Hydrolasen im Genitale weiblicher Marmosets (Callithrix jacchus) und Ratten. Acta Histochem (Suppl) 31:171–184

    Google Scholar 

  • Blanke H-J, Gossrau R, Graf R (1984) Zur Zytochemie von Membranhydrolasen im weiblichen Genitale von Marmosets (Callithrix jacchus). Verh Anat Ges 78:359–360

    Google Scholar 

  • Busch LC (1982) Ultrastrukturelle Untersuchungen zur Transformation des Endometriums. Habilitationsschrift, Medizinische Fakultät, RWTH Aachen

  • Christie GA (1967) Histochemistry of implantation in the rabbit. Histochemie 9:13–29

    Google Scholar 

  • Conti CJ, Gimenez-Conti IB, Conner EA, Lehman JM, Gerschenson LE (1984) Estrogen and progesterone regulation of proliferation, migration, and loss in different target cells of rabbit uterine epithelium. Endocrinology 114:345–351

    Google Scholar 

  • Davies J, Hoffman LH (1973) Studies on the progestational endometrium of the rabbit. I. Light microscopy, day 0 to day 13 of gonadotrophin-induced pseudopregnancy. Am J Anat 137:423–446

    Google Scholar 

  • Davies J, Hoffman LH (1975) Studies on the progestational endometrium of the rabbit. II. Electron microscopy, day 0 to day 13 of gonadotrophin-induced pseudopregnancy. Am J Anat 142:335–366

    Google Scholar 

  • Denker H-W (1969) Zur Enzym-Topochemie von Frühentwicklung und Implantation des Kaninchens. Dissertation, Med Fak Marburg

  • Denker H-W (1970) Topochemie hochmolekularer Kohlenhydratsubstanzen in Frühentwicklung und Implantation des Kaninchens. Zool Jahrb Abt Allgem Zool und Physiol 75:141–145

    Google Scholar 

  • Denker H-W (1971) Enzym-Topochemie von Frühentwicklung und Implantation des Kaninchens. III. Proteasen. Histochemie 25:344–360

    Google Scholar 

  • Denker H-W (1977) Implantation. The role of proteinases, and blockage of implantation by proteinase inhibitors. Adv Anat Embryol Cell Biol 53 Fasc 5.

  • Denker H-W (1980) Endometrial arylamidase secretion: a sensitive parameter of steroid hormone action and of embryo-maternal interrelationships in the rabbit. In: Beato M (ed) Steroid induced uterine proteins. Elsevier, North-Holland Biomedical Press, Amsterdam, pp 121–131

    Google Scholar 

  • Denker H-W, Stangl R (1976) Versuche zur Lokalisierung und Abgrenzung verschiedener Aminosäure-Arylamidasen in Uterus und Blastozyste des Kaninchens. Acta Histochem (Suppl) 16:249–257

    Google Scholar 

  • Dickman Z, Dey SK, Sen Gupta J (1976) A new concept: control of early pregnancy by steroid hormones originating in the preimplantation embryo. Vitam Horm 34:215–242

    Google Scholar 

  • Enders AC, Schlafke S (1971) Penetration of the uterine epithelium during implantation in the rabbit. Am J Anat 132:219–240

    Google Scholar 

  • Feracci H, Bernadac A, Hovsépian S, Fayct G, Maroux S (1981) Aminopeptidase N is a marker for the apical pole of porcine thyroid epithelial cells in vivo and in culture. Cell Tissue Res 221:137–146

    Google Scholar 

  • Finn CA, Hinchliffe JR (1964) Reaction of the mouse uterus during implantation and deciduoma formation as demonstrated by changes in the distribution of alkaline phosphatase. J Reprod Fertil 8:331–338

    Google Scholar 

  • Fischer B, Winterhager E, Busch LC, Beier HM (1985) Die Pseudogravidität des Kaninchens als reproduktionsbiologisches Modell. Fertilität 1:101–109

    Google Scholar 

  • Fuhrmann K (1959) Kolorimetrische Bestimmung und histochemischer Nachweis der Aminopeptidase an Geweben weiblicher Genitalorgane. Zentralbl Gynäkol 28:1105–1123

    Google Scholar 

  • Gossrau R (1979) Peptidasen II. Zur Lokalisation der Dipeptidylpeptidase IV (DPP IV). Histochemische und biochemische Untersuchung. Histochemistry 60:231–248

    Google Scholar 

  • Hanski C, Huhle T, Reutter W (1985) Involvement of plasma membrane dipeptidyl peptidase IV in fibronectin-mediated adhesion of cells on collagen. Biol Chem Hoppe-Seyler 366:1169–1176

    Google Scholar 

  • Izquierdo L, Marticorena P (1975) Alkaline phosphatase in preimplantation mouse embryos. Exp Cell Res 92:399–402

    Google Scholar 

  • Kennedy TG (1983) Embryonic signals and the initiation of blastocyst implantation. Aust J Biol Sci 36:531–543

    Google Scholar 

  • Kinne R (1976) Membrane-molecular aspects of tubular transport. Int Rev Physiol 11:169–210

    Google Scholar 

  • Kugler P (1981) Localization of aminopeptidase A (angiotensinase A) in the rat and mouse kidney. Histochemistry 72:269–278

    Google Scholar 

  • Kugler P (1984) Zur Enzymhistochemic transportierender Epithelien. Verh Anat Ges 78:41–54

    Google Scholar 

  • Kühnel W, Beier HM, Petry G (1971) Untersuchungen zur hormonellen Regulation der Praeimplantationsphase der Gravidität. II. Histologische, topochemische und biochemische Analysen am hormonbehandelten, pseudograviden Kaninchenuterus. Cytobiologie 4:9–40

    Google Scholar 

  • Kyte J (1976) Immunoferritin determination of the distribution of (Na++K+)ATPase over the plasma membranes of renal convoluted tubules. I. Distal segment. J Cell Biol 68:287–303

    Google Scholar 

  • Lampelo SA, Ricketts AP, Bullock DW (1985) Purification of rabbit endometrial plasma membranes from receptive and nonreceptive uteri. J Reprod Fertil 75:475–484

    Google Scholar 

  • Lehninger AL (1977) Biochemie. Verlag Chemie, Weinheim New York, pp 649–650

    Google Scholar 

  • Lewis PR, Knight DR (1977) Staining methods for sectioned materials. In: Glauert AM (ed) Practical methods in electron microscopy, vol 5. Elsevier/North-Holland, Amsterdam, pp 184–185

    Google Scholar 

  • Lin C, Sasaki M, Orcutt ML, Miyayama H, Singer RM (1976) Plasma membrane localization of alkaline phosphatase in HeLa cells. J Histochem Cytochem 24:659–667

    Google Scholar 

  • Lojda Z, Gossrau R, Schiebler TH (1979) Enzyme histochemistry. A laboratory manual. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Louvard D (1980) Apical membrane aminopeptidase appears at site of cell-cell contact in cultured kidney epithelial cells. Proc Natl Acad Sci USA 77:4132–4136

    Google Scholar 

  • Mancarella DA, Mahaboob Basha SM, Mullins DE, Mansfield E, Bazer FW, Roberts RM (1981) Properties of a membrane-associated l-leucine β-naphthylamidase (leucine aminopeptidase) from the porcine uterus. Biol Reprod 24:879–887

    Google Scholar 

  • Manning JP, Steinetz BG, Giannina T (1969) Decidual alkaline phosphatase activity in the pregnant and pseudopregnant rat. Ann NY Acad Sci 166:482–509

    Google Scholar 

  • McDonald UK, Barrett AJ (1986) Mammalian proteases. A glossary and bibliography, vol 2, Exopeptidases. Academic Press, New York

    Google Scholar 

  • McDonald JK, Schwabe C (1977) Intracellular exopeptidases. In: Barrett AJ (ed) Proteinases in mammalian cells and tissues. North-Holland, Amsterdam, New York, Oxford, pp 311–391

    Google Scholar 

  • Meister A, Tate SS (1976) Glutathione and related γ-glutamyl compounds. Biosynthesis and utilization. Annu Rev Biochem 45:559–604

    Google Scholar 

  • Murphy CR, Swift JG, Mukherjee TM, Rogers AW (1982) Changes in the fine structure of the apical plasma membrane of endometrial epithelial cells during implantation in the rat. J Cell Sci 55:1–12

    Google Scholar 

  • Nachlas MM, Monis B, Rosenblatt D, Seligman AM (1960) Improvement in the histochemical localization of leucine aminopeptidase with a new substrate, l-leucyl-4-methoxy-2-naphthylamide. J Biophys Biochem Cytol 7:261–264

    Google Scholar 

  • Nalbach BP, Denker H-W (1983) Stage-dependent changes in lectin binding patterns in rabbit uterus and blastocyst during the preimplantation period and implantation. Eur J Cell Biol Suppl 4:13

    Google Scholar 

  • Oledzka-Slotwińska H, Creemers J, Desmet V (1967) Cytidine monophosphate as substrate for the electron microscopic visualization of alkaline phosphatase activity. Histochemie 9:320–326

    Google Scholar 

  • Orlowski M, Meister A (1970) The γ-glutamyl cycle: a possible transport system for amino acids. Proc Natl Acad Sci USA 67:1248–1255

    Google Scholar 

  • Petry G, Kühnel W, Beier HM (1970) Untersuchungen zur hormonellen Regulation der Praeimplantationsphase der Gravidität. I. Histologische, topochemische und biochemische Analysen am normalen Kaninchenuterus. Cytobiologie 2:1–32

    Google Scholar 

  • Pisam M, Pipoche P (1976) Redistribution of surface macromolecules in dissociated epithelial cells. J Cell Biol 71:907–920

    Google Scholar 

  • Rabito CA, Kreisberg JI, Wight D (1984) Alkaline phosphatase and γ-glutamyl transpeptidase as polarization markers during the organization of LLC-PK1 cells into an epithelial membrane. J Biol Chem 259:574–582

    Google Scholar 

  • Rodriguez-Boulan E, Paskiet KT, Sabatini DD (1983) Assembly of enveloped viruses in MDCK cells: polarized budding from single attached cells and from clusters of cells in suspension. J Cell Biol 96:866–874

    Google Scholar 

  • Rutenburg AM, Kim H, Fischbein JW, Hanker JS, Wasserkrug HL, Seligman AM (1969) γ-Glutamyl transpeptidase activity. J Histochem Cytochem 17:517–526

    Google Scholar 

  • Spicer SS, Baron DA, Sato A, Schulte BA (1981) Variability of cell surface glycoconjugates — relation to differences in cell function. J Histochem Cytochem 29:994–1002

    Google Scholar 

  • Suzuki H, Tsutsumi Y (1980) Morphological changes of uterine and cervical epithelium during early pregnancy in rabbits. J Fac Agr Hokkaido Univ 60:47–61

    Google Scholar 

  • Suzuki H, Tsutsumi Y (1981) Morphological studies of uterine and cervical epithelium in pseudopregnant rabbits. J Fac Agr Hokkaido Univ 60:123–132

    Google Scholar 

  • Suzuki M, Kuramoto H, Izumi S, Shirane H, Watanabe K (1981) Cyclic changes of alkaline phosphatase in the human endometrium: histochemical and biochemical analyses. Acta Histochem Cytochem 14:524–533

    Google Scholar 

  • Tanaka K, Omori K, Tashiro Y (1986) Quantitative immunoferritin localization of leucine aminopeptidase on canine hepatocyte cell surface. J Histochem Cytochem 34:775–784

    Google Scholar 

  • Tarachand U, Sivabalan R, Eapen J (1981) Enhanced gamma glutamyl transpeptidase activity in rat uterus following deciduoma induction and implantation. Biochem Biophys Res Commun 101:1152–1157

    Google Scholar 

  • van Hoorn G, Denker H-W (1975) Effect of the blastocyst on a uterine amino acid arylamidase in the rabbit. J Reprod Fertil 45:359–362

    Google Scholar 

  • Wachstein M, Meisel E (1957) Histochemistry of hepatic phosphatases at a physiologic pH with special reference to the demonstration of bile canaliculi. Am J Clin Pathol 27:13–23

    Google Scholar 

  • Winterhager E (1985) Dynamik der Zellmembran: Modellstudien während der Implantationsreaktion beim Kaninchen. Habilitationsschrift, Medizinische Fakultät, RWTH Aachen

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Classen-Linke, I., Denker, H.W. & Winterhager, E. Apical plasma membrane-bound enzymes of rabbit uterine epithelium. Histochemistry 87, 517–529 (1987). https://doi.org/10.1007/BF00492466

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00492466

Keywords

Navigation