Summary
The complex development of the metanephric kidney illustrates the decisive role of sequential morphogenetic interactions of varying type in organogenesis. In this review the following steps were singled out from this continuous, strictly controlled organogenesis: determination of the mesoderm during the blastula stage, induction of pronephric nephrons during gastrulation, guided migration of the pronephric duct, mesenchyme-controlled branching of the ureter, induced aggregation of the mesenchymal cells of the metanephric blastema, homotypically controlled polarization of the cells in the renal vesicle and remodelling of the vesicle into the S-shaped body, guided migration of endothelial cells into the nephric blastema and the glomerular crevice, and the matrix interaction(s) completing the formation of the glomerular basement membrane with dual origin.
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References
Abrahamson DR (1985) Origin of the glomerular basement membrane visualized after in vivo labeling of laminin in newborn rat kidney. J Cell Biol 100:1988–2000
Ekblom P, Alitalo K, Vaheri A, Timpl R, Saxén L (1980) Induction of a basement membrane glycoprotein: Possible role of laminin in morphogenesis. Proc Natl Acad Sci USA 77:485–489
Ekblom P, Lehtonen E, Saxén L, Timpl R (1981) Shift in collagen type as an early response to induction of the metanephric mesenchyme. J Cell Biol 89:276–283
Gospodarowicz D, Neufeld G, Schweigerer L (1986) Molecular and biological characterization of fibroblast growth factor, an angiogenic factor which also controls the proliferation and diferentiation of mesoderm and neuroectoderm derived cells. Cell Differ 19:1–17
Grobstein C (1955) Inductive interactions in the development of the mouse metanephros. J Exp Zool 130:319–340
Grobstein C (1956a) Trans-filter induction of tubules in mouse metanephrogenic mesenchyme. Exp Cell Res 10:424–440
Grobstein C (1956b) Inductive tissue interaction in development. Adv Cancer Res 4:187–236
Grobstein C (1967) Mechanisms of organogenetic tissue interaction. Natl Cancer Inst Monogr 26:279–299
Grover A, Andrews G, Adamson ED (1983) Role of laminin in epithelium formation by F9 aggregates. J Cell Biol 97:137–144
Gurdon JB, Fairman S, Mohun TJ, Breman S (1985) Activation of muscle-specific actin genes in Xenopus development by an induction between animal and vegetal cells of the blastula. Cell 41:913–922
Gustafson T, Wolpert L (1963) The cellular basis of morphogenesis and sea urchin development. Int Rev Cytol 15:139–214
Lehtonen E (1976) Transmission of signals in embryonic induction. Med Biol 54:108–128
Poole TJ, Steinberg MS (1981) Amphibian pronephric duct morphogenesis: segregation, cell rearrangement and directed migration of the Ambystoma duct rudiment. J Embryol Exp Morphol 63:1–16
Poole TJ, Steinberg MS (1982) Evidence for the guidance of pronephric duct migration by a craniocaudally travelling adhesion gradient. Dev Biol 92:144–158
Sariola H (1985) Incomplete fusion of the epithelial and endothelial basement membranes in interspecies hybrid glomeruli. Cell Differ 14:189–195
Sariola H, Ekblom P, Lehtonen E, Saxén L (1983) Differentiation and vascularization of the metanephric kidney grafted on chorioallantoic membrane. Dev Biol 86:427–435
Sariola H, Timpl R, von der Mark K, Mayne R, Fitch JM, Linsenmayer TF, Ekblom P (1984a) Dual origin of glomerular basement membrane. Dev Biol 101:86–96
Sariola H, Peault B, Le Douarin N, Buck C, Dieterlen-Lievre F, Saxén L (1984b) Extracellular matrix and capillary ingrowth in interspecies chimeric kidneys. Cell Differ 15:43–52
Saxén L (1970) The determination and differentiation of the metanephric nephron. In: N Alwall, F Berglund, B Josephson (eds) Proc Fourth Int Congr Nephrol Vol I. S. Karger, Basel, pp 29–38
Saxén L (1972) Interactive mechanisms in morphogenesis. In: D Tarin (ed) Tissue interactions and carcinogenesis. Academic Press, London, pp 49–80
Saxén L (1984) Implementation of a developmental program. In: C Changas (ed) Modern biological experimentation. Pontificia Acad Sci, Citta del Vaticano, pp 155–163
Saxén L (1987) Organogenesis of the kidney. Cambridge Univ Press, Cambridge (in press)
Saxén L, Toivonen S (1962) Primary embryonic induction. Academic Press, London
Saxén L, Wartiovaara J (1966) Cell contact and cell adhesion during tissue organogenesis. Int J Cancer 1:271–290
Saxén L, Koskimies O, Lahti A, Miettinen H, Rapola J, Wartiovaara J (1968) Differentiation of kidney mesenchyme in an experimental model system. Adv Morphol 7:251–293
Saxén L, Karkinen-Jääskeläinen M, Lehtonen E, Nordling S, Wartiovaara J (1976) Inductive tissue interactions. In: G Poste, GL Nicolson (eds) The cell surface in animal embryogenesis and development. North-Holland Publ. Co, Amsterdam, pp 331–407
Slack JMW (1983) From egg to embryo. Cambridge Univ Press, Cambridge
Spemann H (1901) Über Korrelationen in der Entwicklung des Auges. Verh Anat Ges (Jena) 15:61–79
Thesleff I, Ekblom P (1984) Role of transferrin in branching morphogenesis, growth and differentiation of the embryonic kidney. J Embryol Exp Morphol 82:147–161
Thiery J-P, Duband JL, Rutishauser U, Edelman GM (1982) Cell adhesion molecules in early chicken embryogenesis. Proc Natl Acad Sci USA 79:6737–6741
Tiedemann H (1984) Neural embryonic induction. In: A-M Duprat, AC Kato, M Weber (eds) The role of cell interactions in early neurogenesis. Plenum Press, New York, pp 89–105
Toivonen S, Saxén L (1955) The simultaneous inductive action of liver and bonemarrow of the guinea pig in implantation and explantation experiments with embryos of Triturus. Exp Cell Res (Suppl) 3:346–357
Vestweber K, Kemler R, Ekblom P (1985) Cell-adhesíon molecule uvomorulin during kidney development. Dev Biol 112:213–221
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Saxén, L., Sariola, H. & Lehtonen, E. Sequential cell and tissue interactions governing organogenesis of the kidney. Anat Embryol 175, 1–6 (1986). https://doi.org/10.1007/BF00315450
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DOI: https://doi.org/10.1007/BF00315450