Crossref journal-article
The Company of Biologists
Development (237)
Abstract

Abstract Developing kidneys of human and murine fetuses have been stained with monoclonal antibodies to desmosomal proteins 1 and 2 (desmoplakins) (dp 1&2), desmosomal glycoprotein 1 (desmoglein) and a polyclonal antiserum to desmosomal glycoproteins 2 and 3 (desmocollins). All three antibodies stain the mesenchymal condensates that represent the first stage in kidney tubule development, indicating that desmosomal antigens are expressed very early in tubule morphogenesis. Desmosomal antigens are continuously expressed throughout the developing tubule being concentrated at the apical and basal regions of the lateral membranes of cells. Staining is also present in both visceral and parietal membranes of the developing Bowman’s capsule. In the mature tubule, desmosomal staining becomes restricted to a discontinuous apico-lateral ring around the cells. Staining is completely lost from the visceral membrane of the mature Bowman’s capsule (the podocytes) but persists in the parietal membrane. At the condensate stage, staining for dpl&2 is much more intense than staining for simple epithelial keratin. Electron microscopy showed the presence of small (ca 0.1 μm) punctate junctions in the developing tubule. These may be immature desmosomes. No fully mature desmosomes such as are present in mature kidney were found. The results suggest that desmosomal proteins and glycoproteins are involved in the early development of adhesive contacts between cells of the kidney tubule. The changing pattern of antigen expression, the loss of desmosomal staining from the podocytes and the immaturity of junctions suggest that desmosomal adhesion is labile during tubule morphogenesis, perhaps in order to facilitate changes of cell-cell contact.

Bibliography

Garrod, D. R., & Fleming, S. (1990). Early expression of desmosomal components during kidney tubule morphogenesis in human and murine embryos. Development, 108(2), 313–321.

Authors 2
  1. D. R. Garrod (first)
  2. S. Fleming (additional)
References 50 Referenced 58
  1. 10.1083/jcb.108.4.1477 / J. Cell Biol. / Expression of mutant keratin cDNA in epithelial cells reveals possible mechanisms for initiation and assembly of intermediate filaments by Albers (1989)
  2. 10.1007/BF00490899 / Histochemistry / Differentiation of cell types in the mammalian kidney by immunofluorescence microscopy using antibodies to intermediate filament proteins and desmoplakins by Bachman (1983)
  3. 10.1083/jcb.102.2.560 / J. Cell Biol. / Organization of cytokeratin bundles by desmosomes in rat mammary epithelial cells by Bologna (1986)
  4. {'key': '2023050311341351000_DEVELOP_108_2_313C4', 'first-page': '427', 'article-title': 'The desmosome-intermediate filament complex', 'volume-title': 'The Cell in Contact. Adhesions and Junctions as Morphogenetic Determinants', 'author': 'Cowin', 'year': '1985'} / The Cell in Contact. Adhesions and Junctions as Morphogenetic Determinants / The desmosome-intermediate filament complex by Cowin (1985)
  5. 10.1038/302148a0 / Nature, Lond. / Antibodies to epithelial desmosomes show wide tissue and species cross reactivity by Cowin (1983)
  6. 10.1242/jcs.66.1.119 / J. Cell Sci. / Distribution of desmosomal components in the tissues of vertebrates, studied by fluorescent antibody staining by Cowin (1984)
  7. 10.1083/jcb.85.3.695 / J. Cell Biol. / Desmosome development in an in vitro model by Dembitzer (1980)
  8. 10.1111/j.1432-0436.1985.tb00297.x / Differentiation / Distribution of vimentin, cytokeratins and desmosomal-plaque proteins in human nephroblastoma as revealed by specific antibodies: co-existence of cell groups of different degrees of epithelial differentiation by Denk (1985)
  9. 10.1083/jcb.102.5.1843 / J. Cell Biol. / Identification of actin-, -actinin-, and vinculin-containing plaques at the lateral membranes of epithelial cells by Drenkhann (1986)
  10. 10.1242/dev.103.2.325 / Development / Spatial and temporal distribution of the adherens-junction-associated adhesion molecule A-CAM during avian embryogenesis by Duband (1988)
  11. 10.1016/0012-1606(75)90063-9 / Devl Biol. / The preimplantation mammalian embryo: Characterisation of intercellular junctions and their appearance during development by Ducibella (1975)
  12. 10.1073/pnas.81.18.5763 / Proc. natn. Acad. Sci. U.S.A. / Lumen formation and redistribution of intramembranous proteins during differentiation of ducts in the rat mammary gland by Dulbecco (1984)
  13. 10.1021/bi00410a001 / Biochemistry / Morphoregulatory molecules by Edelman (1988)
  14. 10.1083/jcb.91.1.1 / J. Cell Biol. / Formation of basement membranes in the embryonic kidney: an immunohistological study by Ekblom (1981)
  15. 10.1073/pnas.77.1.485 / Proc. natn. Acad. Sci. U.S.A. / Induction of a basement membrane glycoprotein in embryonic kidney: possible role of laminin in morphogenesis by Ekblom (1980)
  16. {'key': '2023050311341351000_DEVELOP_108_2_313C16', 'first-page': '109', 'article-title': 'Basement membrane and organogenesis', 'volume-title': 'Developmental Mechanisms: Normal and Abnormal. Alan R. Liss, Inc', 'author': 'Ekblom', 'year': '1985'} / Developmental Mechanisms: Normal and Abnormal. Alan R. Liss, Inc / Basement membrane and organogenesis by Ekblom (1985)
  17. {'key': '2023050311341351000_DEVELOP_108_2_313C17', 'first-page': '191', 'article-title': 'Immunohistochemical evidence transferrin, dependent proliferation during renal tubulogenesis', 'volume': '153', 'author': 'Fleming', 'year': '1987', 'journal-title': 'J. Anat.'} / J. Anat. / Immunohistochemical evidence transferrin, dependent proliferation during renal tubulogenesis by Fleming (1987)
  18. 10.1111/j.1365-2559.1987.tb02619.x / Histopathology / The distribution of cytokeratin antigens in the kidney and in renal tumours by Fleming (1987)
  19. {'key': '2023050311341351000_DEVELOP_108_2_313C19', 'article-title': 'Loss of desmosomes in sarcomatoid renal tumours. Submitted for publication', 'volume-title': 'J. Pathol (submitted)', 'author': 'Fleming', 'year': '1989'} / J. Pathol (submitted) / Loss of desmosomes in sarcomatoid renal tumours. Submitted for publication by Fleming (1989)
  20. 10.1111/j.1432-0436.1981.tb01178.x / Differentiation / Antibodies to high molecular weight polypeptides of desmosomes: specific localisation of a class of junctional proteins in cells and tissues by Franke (1981)
  21. 10.1007/978-1-4684-5092-7_3 / Cellular and Molecular Control of Direct Cell Interactions / The adhesions of epithelial cells by Garrod (1985)
  22. 10.1042/bst0140172 / Biochem. Soc. Trans. / Formation of desmosomes in polarized and non-polarized epithelial cells: implications for epithelial morphogenesis by Garrod (1986)
  23. 10.1242/jcs.1986.Supplement_4.14 / J. Cell Sci. Suppl. / Desmosomes, cell adhesion molecules and the adhesive properties of cells in tissues by Garrod (1986)
  24. {'key': '2023050311341351000_DEVELOP_108_2_313C24', 'article-title': '‘Desmosomes’', 'volume-title': 'Morphoregulatory Molecules', 'author': 'Garrod', 'year': '1989'} / Morphoregulatory Molecules / ‘Desmosomes’ by Garrod (1989)
  25. {'key': '2023050311341351000_DEVELOP_108_2_313C25', 'first-page': '552', 'article-title': 'Expression of vimentin and cytokeratin types of intermediate filament proteins in developing and adult human kidneys', 'volume': '50', 'author': 'Holthofer', 'year': '1984', 'journal-title': 'Lab. Invest.'} / Lab. Invest. / Expression of vimentin and cytokeratin types of intermediate filament proteins in developing and adult human kidneys by Holthofer (1984)
  26. 10.1242/dev.102.4.749 / Development / Neural cell adhesion molecules during embryonic induction and development of the kidney by Klein (1988)
  27. 10.1016/S0022-5320(75)80013-X / J. Ultrastruct. Res. / The ultrastructure of the developing proximal tubule of the rat kidney by Larson (1975)
  28. 10.1016/0012-1606(85)90051-X / Devl Biol. / Reorganization of intermediate filament cytoskeleton in induced metanephric mesenchyme cells is independent of tubule morphogenesis by Lehtonen (1985)
  29. 10.1083/jcb.48.3.455 / J. Cell Biol. / Differentiation of the junctional complex of surface cells in the developing Fundulus blastoderm by Lentz (1971)
  30. 10.1136/jcp.37.9.975 / J. Clin. Pathol. / Monoclonal antibody to cytokeratin for use in routine histopathology by Makin (1984)
  31. 10.1136/jcp.31.5.454 / J. Clin. Pathol. / Alkaline phosphatase and peroxidase for double immunoenzymatic labelling of cellular constituents by Mason (1981)
  32. 10.1242/jcs.85.1.95 / J. Cell Sci. / Calcium-induced desmosome formation in cultured kidney epithelial cells by Mattey (1986)
  33. 10.1242/jcs.85.1.113 / J. Cell Sci. / Splitting and internalization of the desmosomes of cultured kidney epithelial cells by reduction in calcium concentrations by Mattey (1986)
  34. 10.1002/j.1460-2075.1987.tb04834.x / EMBO J. / Localization of the protein and glycoprotein components of bovine nasal epithelial desmosomes by immunoelectron microscopy by Miller (1987)
  35. 10.1007/BF00315707 / Anat. Embryol. / The development of cell junctions during nephrogenesis by Minuth (1981)
  36. {'key': '2023050311341351000_DEVELOP_108_2_313C36', 'first-page': '4', 'article-title': 'Desmosomal proteins: new markers for identification and classification of tumours', 'volume': '54', 'author': 'Moll', 'year': '1986', 'journal-title': 'Lab. Invest.'} / Lab. Invest. / Desmosomal proteins: new markers for identification and classification of tumours by Moll (1986)
  37. {'key': '2023050311341351000_DEVELOP_108_2_313C37', 'first-page': '290', 'article-title': 'Development of human kidney as shown by microdissection. III. Formation and interrelationships of collecting tubules and nephrons', 'volume': '76', 'author': 'Osathanondh', 'year': '1963', 'journal-title': 'Arch. Pathol.'} / Arch. Pathol. / Development of human kidney as shown by microdissection. III. Formation and interrelationships of collecting tubules and nephrons by Osathanondh (1963)
  38. 10.1016/0012-1606(62)90056-8 / Devi Biol / Desmosome development in normal and reassociating cells of the early chick blastoderm by Overton (1962)
  39. 10.1002/path.1711530311 / J. Pathol. / Antidesmosomal monoclonal antibody in the diagnosis of intracranial tumours by Parrish (1987)
  40. 10.1083/jcb.106.3.677 / J. Cell Biol. / Kinetics of desmosome assembly in Madin-Darby canine kidney epithelial cells: Temporal and spatial regulation of desmoplakin organisation and stabilisation upon cell-cell contact I. Biochemical analysis by Pasdar (1988)
  41. 10.1083/jcb.106.3.687 / J. Cell Biol. / Kinetics of desmosome assembly in Madin-Darby canine kidney epithelial cells: Temporal and spatial regulation of desmoplakin organisation and stabilisation upon cell-cell contact II. Morphological analysis by Pasdar (1988)
  42. 10.1083/jcb.105.5.2327 / J. Cell Biol. / Structure and assembly of desmosome junctions: Biosynthesis and turnover of the major desmosome components of MDCK cells in low calcium medium by Penn (1987)
  43. 10.1083/jcb.105.1.57 / J. Cell Biol. / Structure and assembly of desmosome junctions: Biosynthesis, processing and glycoprotein components in cultured epithelial cells by Penn (1987)
  44. 10.1017/CBO9780511565083 / Organogenesis of the Kidney. by Saxen (1987)
  45. 10.1002/ijc.2910010307 / Int. J. Cancer / Cell contact and cell adhesion during tissue organization by Saxen (1966)
  46. 10.1016/S0074-7696(08)60940-7 / Int. Rev. Cytol. / Structure and function of intercellular junctions by Staehlin (1974)
  47. 10.1016/0012-1606(84)90175-1 / Dev! Biol. / Ontogenetic expression of cell adhesion molecules: L-CAM is found in epithelia derived from the three primary germ layers by Thiery (1984)
  48. 10.1073/pnas.79.21.6737 / Proc. natn. Acad. Sci. U.S.A. / Cell adhesion molecules in early chicken embryogenesis by Thiery (1982)
  49. 10.1016/0012-1606(85)90135-6 / Devi Biol. / Cell adhesion molecule uvomorulin during kidney development by Vestweber (1985)
  50. 10.1002/path.1711530410 / J. Pathol. / Monoclonal antibody to desmosomal glycoprotein 1-A new epithelial marker for diagnostic pathology by Vilela (1987)
Dates
Type When
Created 4 years, 4 months ago (April 25, 2021, 8:40 p.m.)
Deposited 2 years, 4 months ago (May 3, 2023, 7:41 a.m.)
Indexed 2 days, 14 hours ago (Sept. 3, 2025, 6:47 a.m.)
Issued 35 years, 7 months ago (Feb. 1, 1990)
Published 35 years, 7 months ago (Feb. 1, 1990)
Published Online 35 years, 7 months ago (Feb. 1, 1990)
Published Print 35 years, 7 months ago (Feb. 1, 1990)
Funders 0

None

@article{Garrod_1990, title={Early expression of desmosomal components during kidney tubule morphogenesis in human and murine embryos}, volume={108}, ISSN={1477-9129}, url={http://dx.doi.org/10.1242/dev.108.2.313}, DOI={10.1242/dev.108.2.313}, number={2}, journal={Development}, publisher={The Company of Biologists}, author={Garrod, D. R. and Fleming, S.}, year={1990}, month=feb, pages={313–321} }