Abstract
We have compared by immunocytochemistry and immunoblotting the expression and distribution of adhesion molecules participating in cell- matrix and cell-cell interactions during embryonic development and regeneration of rat liver. Fibronectin and the fibronectin receptor, integrin alpha 5 beta 1, were distributed pericellularly and expressed at a steady level during development from the 16th day of gestation and in neonate and adult liver. AGp110, a nonintegrin fibronectin receptor was first detected on the 17th day of gestation in a similar, nonpolarized distribution on parenchymal cell surfaces. At that stage of development haemopoiesis is at a peak in rat liver and fibronectin and receptors alpha 5 beta 1 and AGp110 were prominent on the surface of blood cell precursors. During the last 2 d of gestation (20th and 21st day) hepatocytes assembled around lumina. AGp110 was initially depolarized on the surface of these acinar cells but then confined to the lumen and to newly-formed bile canaliculi. At birth, a marked increase occurred in the canalicular expression of AGp110 and in the branching of the canalicular network. Simultaneously, there was enhanced expression of ZO-1, a protein component of tight junctions. On the second day postpartum, presence of AGp110 and of protein constituents of desmosomes and intermediate junctions, DGI and E- cadherin, respectively, was notably enhanced in cellular fractions insoluble in nonionic detergents, presumably signifying linkage of AGp110 with the cytoskeleton and assembly of desmosomal and intermediate junctions. During liver regeneration after partial hepatectomy, AGp110 remained confined to apical surfaces, indicating a preservation of basic polarity in parenchymal cells. A decrease in the extent and continuity of the canalicular network occurred in proliferating parenchyma, starting 24 h after resection in areas close to the terminal afferent blood supply of portal veins and spreading to the rest of the liver within the next 24 h. Distinct acinar structures, similar to the ones in prenatal liver, appeared at 72 h after hepatectomy. Restoration of the normal branching of the biliary tree commenced at 72 h. At 7 d postoperatively acinar formation declined and one-cell-thick hepatic plates, as in normal liver, were observed.
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- Adamson E. D., Baribault H., Kemler R. Altered uvomorulin expression in a noncompacting mutant cell line of F9 embryonal carcinoma cells. Dev Biol. 1990 Apr;138(2):338–347. doi: 10.1016/0012-1606(90)90201-s. [DOI] [PubMed] [Google Scholar]
- Alison M. R. Regulation of hepatic growth. Physiol Rev. 1986 Jul;66(3):499–541. doi: 10.1152/physrev.1986.66.3.499. [DOI] [PubMed] [Google Scholar]
- Bartles J. R., Hubbard A. L. Preservation of hepatocyte plasma membrane domains during cell division in situ in regenerating rat liver. Dev Biol. 1986 Nov;118(1):286–295. doi: 10.1016/0012-1606(86)90095-3. [DOI] [PubMed] [Google Scholar]
- Boller K., Vestweber D., Kemler R. Cell-adhesion molecule uvomorulin is localized in the intermediate junctions of adult intestinal epithelial cells. J Cell Biol. 1985 Jan;100(1):327–332. doi: 10.1083/jcb.100.1.327. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Edelman G. M. Cell adhesion molecules in the regulation of animal form and tissue pattern. Annu Rev Cell Biol. 1986;2:81–116. doi: 10.1146/annurev.cb.02.110186.000501. [DOI] [PubMed] [Google Scholar]
- Ekblom P., Vestweber D., Kemler R. Cell-matrix interactions and cell adhesion during development. Annu Rev Cell Biol. 1986;2:27–47. doi: 10.1146/annurev.cb.02.110186.000331. [DOI] [PubMed] [Google Scholar]
- Enrich C., Evans W. H., Gahmberg C. G. Fibronectin isoforms in plasma membrane domains of normal and regenerating rat liver. FEBS Lett. 1988 Feb 8;228(1):135–138. doi: 10.1016/0014-5793(88)80602-1. [DOI] [PubMed] [Google Scholar]
- Fabrikant J. I. The spatial distribution of parenchymal cell proliferation during regeneration of the liver. Johns Hopkins Med J. 1967 Mar;120(3):137–147. [PubMed] [Google Scholar]
- Garrod D. R., Fleming S. Early expression of desmosomal components during kidney tubule morphogenesis in human and murine embryos. Development. 1990 Feb;108(2):313–321. doi: 10.1242/dev.108.2.313. [DOI] [PubMed] [Google Scholar]
- Goodwin L., Hill J. E., Raynor K., Raszi L., Manabe M., Cowin P. Desmoglein shows extensive homology to the cadherin family of cell adhesion molecules. Biochem Biophys Res Commun. 1990 Dec 31;173(3):1224–1230. doi: 10.1016/s0006-291x(05)80917-9. [DOI] [PubMed] [Google Scholar]
- Gumbiner B., Simons K. A functional assay for proteins involved in establishing an epithelial occluding barrier: identification of a uvomorulin-like polypeptide. J Cell Biol. 1986 Feb;102(2):457–468. doi: 10.1083/jcb.102.2.457. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hughes R. C., Stamatoglou S. C. Adhesive interactions and the metabolic activity of hepatocytes. J Cell Sci Suppl. 1987;8:273–291. doi: 10.1242/jcs.1987.supplement_8.15. [DOI] [PubMed] [Google Scholar]
- Johansson S., Forsberg E., Lundgren B. Comparison of fibronectin receptors from rat hepatocytes and fibroblasts. J Biol Chem. 1987 Jun 5;262(16):7819–7824. [PubMed] [Google Scholar]
- Koch P. J., Walsh M. J., Schmelz M., Goldschmidt M. D., Zimbelmann R., Franke W. W. Identification of desmoglein, a constitutive desmosomal glycoprotein, as a member of the cadherin family of cell adhesion molecules. Eur J Cell Biol. 1990 Oct;53(1):1–12. [PubMed] [Google Scholar]
- Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
- Luzzatto A. C. Hepatocyte differentiation during early fetal development in the rat. Cell Tissue Res. 1981;215(1):133–142. doi: 10.1007/BF00236254. [DOI] [PubMed] [Google Scholar]
- Magee A. I., Buxton R. S. Transmembrane molecular assemblies regulated by the greater cadherin family. Curr Opin Cell Biol. 1991 Oct;3(5):854–861. doi: 10.1016/0955-0674(91)90060-c. [DOI] [PubMed] [Google Scholar]
- Montesano R., Friend D. S., Perrelet A., Orci L. In vivo assembly of tight junctions in fetal rat liver. J Cell Biol. 1975 Nov;67(2PT1):310–319. doi: 10.1083/jcb.67.2.310. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Moreau A., Maurice M., Feldmann G. Analysis of hepatocyte plasma membrane domains during rat development using monoclonal antibodies. J Histochem Cytochem. 1988 Jan;36(1):87–94. doi: 10.1177/36.1.3275714. [DOI] [PubMed] [Google Scholar]
- Nagafuchi A., Takeichi M. Cell binding function of E-cadherin is regulated by the cytoplasmic domain. EMBO J. 1988 Dec 1;7(12):3679–3684. doi: 10.1002/j.1460-2075.1988.tb03249.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nelson W. J., Shore E. M., Wang A. Z., Hammerton R. W. Identification of a membrane-cytoskeletal complex containing the cell adhesion molecule uvomorulin (E-cadherin), ankyrin, and fodrin in Madin-Darby canine kidney epithelial cells. J Cell Biol. 1990 Feb;110(2):349–357. doi: 10.1083/jcb.110.2.349. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Obrink B. C-CAM (cell-CAM 105)--a member of the growing immunoglobulin superfamily of cell adhesion proteins. Bioessays. 1991 May;13(5):227–234. doi: 10.1002/bies.950130505. [DOI] [PubMed] [Google Scholar]
- Odin P., Obrink B. The cell-surface expression of the cell adhesion molecule cellCAM 105 in rat fetal tissues and regenerating liver. Exp Cell Res. 1988 Nov;179(1):89–103. doi: 10.1016/0014-4827(88)90351-5. [DOI] [PubMed] [Google Scholar]
- Ogawa K., Medline A., Farber E. Sequential analysis of hepatic carcinogenesis: the comparative architecture of preneoplastic, malignant, prenatal, postnatal and regenerating liver. Br J Cancer. 1979 Nov;40(5):782–790. doi: 10.1038/bjc.1979.261. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pasdar M., Krzeminski K. A., Nelson W. J. Regulation of desmosome assembly in MDCK epithelial cells: coordination of membrane core and cytoplasmic plaque domain assembly at the plasma membrane. J Cell Biol. 1991 May;113(3):645–655. doi: 10.1083/jcb.113.3.645. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Patel V. P., Lodish H. F. The fibronectin receptor on mammalian erythroid precursor cells: characterization and developmental regulation. J Cell Biol. 1986 Feb;102(2):449–456. doi: 10.1083/jcb.102.2.449. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Penn E. J., Hobson C., Rees D. A., Magee A. I. The assembly of the major desmosome glycoproteins of Madin-Darby canine kidney cells. FEBS Lett. 1989 Apr 10;247(1):13–16. doi: 10.1016/0014-5793(89)81229-3. [DOI] [PubMed] [Google Scholar]
- Rabes H. M., Wirsching R., Tuczek H. V., Iseler G. Analysis of cell cycle compartments of hepatocytes after partial hepatecomy. Cell Tissue Kinet. 1976 Nov;9(6):517–532. doi: 10.1111/j.1365-2184.1976.tb01301.x. [DOI] [PubMed] [Google Scholar]
- Rappaport A. M. Hepatic blood flow: morphologic aspects and physiologic regulation. Int Rev Physiol. 1980;21:1–63. [PubMed] [Google Scholar]
- Schwarz M. A., Owaribe K., Kartenbeck J., Franke W. W. Desmosomes and hemidesmosomes: constitutive molecular components. Annu Rev Cell Biol. 1990;6:461–491. doi: 10.1146/annurev.cb.06.110190.002333. [DOI] [PubMed] [Google Scholar]
- Simons K., Fuller S. D. Cell surface polarity in epithelia. Annu Rev Cell Biol. 1985;1:243–288. doi: 10.1146/annurev.cb.01.110185.001331. [DOI] [PubMed] [Google Scholar]
- Stamatoglou S. C., Hughes R. C., Lindahl U. Rat hepatocytes in serum-free primary culture elaborate an extensive extracellular matrix containing fibrin and fibronectin. J Cell Biol. 1987 Nov;105(5):2417–2425. doi: 10.1083/jcb.105.5.2417. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Stamatoglou S. C., Manson M. M., Green J. A., Mayol X., Hughes R. C. Distribution of fibronectin and fibronectin-binding proteins, AGp110 and integrin alpha 5 beta 1, during chemically induced hepatocarcinogenesis in adult rats. J Cell Sci. 1991 Nov;100(Pt 3):599–604. doi: 10.1242/jcs.100.3.599. [DOI] [PubMed] [Google Scholar]
- Stamatoglou S. C., Sullivan K. H., Johansson S., Bayley P. M., Burdett I. D., Hughes R. C. Localization of two fibronectin-binding glycoproteins in rat liver and primary hepatocytes. Co-distribution in vitro of integrin (alpha 5 beta 1) and non-integrin (AGp110) receptors in cell-substratum adhesion sites. J Cell Sci. 1990 Dec;97(Pt 4):595–606. doi: 10.1242/jcs.97.4.595. [DOI] [PubMed] [Google Scholar]
- Stevenson B. R., Siliciano J. D., Mooseker M. S., Goodenough D. A. Identification of ZO-1: a high molecular weight polypeptide associated with the tight junction (zonula occludens) in a variety of epithelia. J Cell Biol. 1986 Sep;103(3):755–766. doi: 10.1083/jcb.103.3.755. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Stow J. L., Kjéllen L., Unger E., Hök M., Farquhar M. G. Heparan sulfate proteoglycans are concentrated on the sinusoidal plasmalemmal domain and in intracellular organelles of hepatocytes. J Cell Biol. 1985 Mar;100(3):975–980. doi: 10.1083/jcb.100.3.975. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Takeichi M. Cadherin cell adhesion receptors as a morphogenetic regulator. Science. 1991 Mar 22;251(5000):1451–1455. doi: 10.1126/science.2006419. [DOI] [PubMed] [Google Scholar]
- Wheeler G. N., Parker A. E., Thomas C. L., Ataliotis P., Poynter D., Arnemann J., Rutman A. J., Pidsley S. C., Watt F. M., Rees D. A. Desmosomal glycoprotein DGI, a component of intercellular desmosome junctions, is related to the cadherin family of cell adhesion molecules. Proc Natl Acad Sci U S A. 1991 Jun 1;88(11):4796–4800. doi: 10.1073/pnas.88.11.4796. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wiley L. M., Kidder G. M., Watson A. J. Cell polarity and development of the first epithelium. Bioessays. 1990 Feb;12(2):67–73. doi: 10.1002/bies.950120204. [DOI] [PubMed] [Google Scholar]
- Zeligs J. D., Wollman S. H. Mitosis in thyroid follicular epithelial cells in vivo. III. Cytokinesis. J Ultrastruct Res. 1979 Mar;66(3):288–303. doi: 10.1016/s0022-5320(79)90125-4. [DOI] [PubMed] [Google Scholar]