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. 1977 May 1;73(2):445–463. doi: 10.1083/jcb.73.2.445

Basal lamina of embryonic salivary epithelia. Production by the epithelium and role in maintaining lobular morphology

PMCID: PMC2109925  PMID: 858743

Abstract

The role of the basal lamina in maintaining the normal morphology of mouse embryo submandibular epithelia was assessed by examining its production as well as the cellular and organ culture changes associated with its removal and replacement. The lamina was removed from epithelia isolated free of mesenchyme by brief treatment with testicular hyaluronidase in the absence of calcium. The treatment causes rounding- up of the cells, loss of cellular cohesion, appearance of microvilli, and changes in the organization of cytoskeletal structures. The lamina is not removed and the cellular alterations do not occur in the absence of hyaluronidase in calcium-free medium or when both enzyme and calcium are present, possibly because digestion of chondroitin sulfate, a component of the lamina, is inhibited by calcium. Within 2 h after treatment, in the absence of mesenchyme or biological substrata, the epithelia deposits a new lamina, which is identical by several criteria to the preexisting lamina, and reverses the cellular alterations. Epithelia treated with hyaluronidase lose lobular morphology during culture with mesenchyme. Delaying culture with mesenchyme, to allow restoration of the lamina and of normal cellular architecture, prevents the loss of lobular morphology. The results indicate that the basal lamina imposes morphologic stability on the epithelium, while the mesenchyme apparently affects processes involved in changes in morphology, possibly by selective degradation of the basal lamina.

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Selected References

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  1. Ash J. F., Spooner B. S., Wessells N. K. Effects of papaverine and calcium-free medium on salivary gland morphogenesis. Dev Biol. 1973 Aug;33(2):463–469. doi: 10.1016/0012-1606(73)90151-6. [DOI] [PubMed] [Google Scholar]
  2. Bernfield M. R., Banerjee S. D. Acid mucopolysaccharide (glycosaminoglycan) at the epithelial-mesenchymal interface of mouse embryo salivary glands. J Cell Biol. 1972 Mar;52(3):664–673. doi: 10.1083/jcb.52.3.664. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bernfield M. R. Collagen synthesis during epitheliomesenchymal interactions. Dev Biol. 1970 Jun;22(2):213–231. doi: 10.1016/0012-1606(70)90151-x. [DOI] [PubMed] [Google Scholar]
  4. Clark C. C., Tomichek E. A., Koszalka T. R., Minor R. R., Kefalides N. A. The embryonic rat parietal yolk sac. The role of the parietal endoderm in the biosynthesis of basement membrane collagen and glycoprotein in vitro. J Biol Chem. 1975 Jul 10;250(13):5259–5267. [PubMed] [Google Scholar]
  5. Cohen A. M., Hay E. D. Secretion of collagen by embryonic neuroepithelium at the time of spinal cord--somite interaction. Dev Biol. 1971 Dec;26(4):578–605. doi: 10.1016/0012-1606(71)90142-4. [DOI] [PubMed] [Google Scholar]
  6. Cohn R. H., Cassiman J. J., Bernfield M. R. Relationship of transformation, cell density, and growth control to the cellular distribution of newly synthesized glycosaminoglycan. J Cell Biol. 1976 Oct;71(1):280–294. doi: 10.1083/jcb.71.1.280. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Coughlin M. D. Early development of parasympathetic nerves in the mouse submandibular gland. Dev Biol. 1975 Mar;43(1):123–139. doi: 10.1016/0012-1606(75)90136-0. [DOI] [PubMed] [Google Scholar]
  8. Culp L. A. Substrate-attached glycoproteins mediating adhesion of normal and virus-transformed mouse fibroblasts. J Cell Biol. 1974 Oct;63(1):71–83. doi: 10.1083/jcb.63.1.71. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cutler L. S., Chaudhry A. P. Intercellular contacts at the epithelial-mesenchymal interface during the prenatal development of the rat submandibular gland. Dev Biol. 1973 Aug;33(2):229–240. doi: 10.1016/0012-1606(73)90133-4. [DOI] [PubMed] [Google Scholar]
  10. Dodson J. W., Hay E. D. Secretion of collagen by corneal epithelium. II. Effect of the underlying substratum on secretion and polymerization of epithelial products. J Exp Zool. 1974 Jul;189(1):51–72. doi: 10.1002/jez.1401890106. [DOI] [PubMed] [Google Scholar]
  11. Dodson J. W., Hay E. D. Secretion of collagenous stroma by isolated epithelium grown in vitro. Exp Cell Res. 1971 Mar;65(1):215–220. doi: 10.1016/s0014-4827(71)80069-1. [DOI] [PubMed] [Google Scholar]
  12. Dunstone J. R. Ion-exchange reactions between acid mucopolysaccharides and various cations. Biochem J. 1962 Nov;85(2):336–351. doi: 10.1042/bj0850336. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Goldman R. D. The use of heavy meromyosin binding as an ultrastructural cytochemical method for localizing and determining the possible functions of actin-like microfilaments in nonmuscle cells. J Histochem Cytochem. 1975 Jul;23(7):529–542. doi: 10.1177/23.7.1095652. [DOI] [PubMed] [Google Scholar]
  14. Grobstein C., Cohen J. Collagenase: effect on the morphogenesis of embryonic salivary epithelium in vitro. Science. 1965 Oct 29;150(3696):626–628. doi: 10.1126/science.150.3696.626. [DOI] [PubMed] [Google Scholar]
  15. Hay E. D., Dodson J. W. Secretion of collagen by corneal epithelium. I. Morphology of the collagenous products produced by isolated epithelia grown on frozen-killed lens. J Cell Biol. 1973 Apr;57(1):190–213. doi: 10.1083/jcb.57.1.190. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hay E. D., Meier S. Glycosaminoglycan synthesis by embryonic inductors: neural tube, notochord, and lens. J Cell Biol. 1974 Sep;62(3):889–898. doi: 10.1083/jcb.62.3.889. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hendrix R. W., Zwaan J. The matrix of the optic vesicle-presumptive lens interface during induction of the lens in the chicken embryo. J Embryol Exp Morphol. 1975 Jul;33(4):1023–1049. [PubMed] [Google Scholar]
  18. Johnson R. C., Manasek F. J., Vinson W. C., Seyer J. M. The biochemical and ultrastructural demonstration of collagen during early heart development. Dev Biol. 1974 Feb;36(2):252–271. doi: 10.1016/0012-1606(74)90049-9. [DOI] [PubMed] [Google Scholar]
  19. KALLMAN F., GROBSTEIN C. SOURCE OF COLLAGEN AT EPITHELIOMESENCHYMAL INTERFACES DURING INDUCTIVE INTERACTION. Dev Biol. 1965 Apr;11:169–183. doi: 10.1016/0012-1606(65)90055-2. [DOI] [PubMed] [Google Scholar]
  20. Kefalides N. A. Structure and biosynthesis of basement membranes. Int Rev Connect Tissue Res. 1973;6:63–104. doi: 10.1016/b978-0-12-363706-2.50008-8. [DOI] [PubMed] [Google Scholar]
  21. Kosher R. A., Lash J. W. Notochordal stimulation of in vitro somite chondrogenesis before and after enzymatic removal of perinotochordal materials. Dev Biol. 1975 Feb;42(2):362–378. doi: 10.1016/0012-1606(75)90340-1. [DOI] [PubMed] [Google Scholar]
  22. Lehtonen E., Wartiovaara J., Nordling S., Saxén L. Demonstration of cytoplasmic processes in Millipore filters permitting kidney tubule induction. J Embryol Exp Morphol. 1975 Feb;33(1):187–203. [PubMed] [Google Scholar]
  23. Mathan M., Hermos J. A., Trier J. S. Structural features of the epithelio-mesenchymal interface of rat duodenal mucosa during development. J Cell Biol. 1972 Mar;52(3):577–588. doi: 10.1083/jcb.52.3.577. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Meier L., Hay E. D. Stimulation of corneal differentiation by interaction between cell surface and extracellular matrix. I. Morphometric analysis of transfilter "induction". J Cell Biol. 1975 Aug;66(2):275–291. doi: 10.1083/jcb.66.2.275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Meier S., Hay E. D. Control of corneal differentiation by extracellular materials. Collagen as a promoter and stabilizer of epithelial stroma production. Dev Biol. 1974 Jun;38(2):249–270. doi: 10.1016/0012-1606(74)90005-0. [DOI] [PubMed] [Google Scholar]
  26. Meier S., Hay E. D. Synthesis of sulfated glycosaminoglycans by embryonic corneal epithelium. Dev Biol. 1973 Dec;35(2):318–331. doi: 10.1016/0012-1606(73)90027-4. [DOI] [PubMed] [Google Scholar]
  27. Nadol J. B., Jr, Gibbins J. R. Autoradiographic evidence for epithelial origin of glucose-rich components of the basement membrane (basal lamina) and basement lamella in the skin of Fundulus heteroclitus. Z Zellforsch Mikrosk Anat. 1970;106(3):398–411. doi: 10.1007/BF00335781. [DOI] [PubMed] [Google Scholar]
  28. Newsome D. A., Kenyon K. R. Collagen production in vitro by the retinal pigmented epithelium of the chick embryo. Dev Biol. 1973 Jun;32(2):387–400. doi: 10.1016/0012-1606(73)90249-2. [DOI] [PubMed] [Google Scholar]
  29. Pierce G. B. The development of basement membranes of the mouse embryo. Dev Biol. 1966 Apr;13(2):231–249. doi: 10.1016/0012-1606(66)90066-2. [DOI] [PubMed] [Google Scholar]
  30. Pollard T. D., Weihing R. R. Actin and myosin and cell movement. CRC Crit Rev Biochem. 1974 Jan;2(1):1–65. doi: 10.3109/10409237409105443. [DOI] [PubMed] [Google Scholar]
  31. Roblin R., Albert S. O., Gelb N. A., Black P. H. Cell surface changes correlated with density-dependent growth inhibition. Glycosaminoglycan metabolism in 3T3, SV3T3, and con A selected revertant cells. Biochemistry. 1975 Jan 28;14(2):347–357. doi: 10.1021/bi00673a022. [DOI] [PubMed] [Google Scholar]
  32. Slavkin H. C. Embryonic tooth formation. A tool for developmental biology. Oral Sci Rev. 1974;4(0):7–136. [PubMed] [Google Scholar]
  33. Spooner B. S., Ash J. F., Wrenn J. T., Frater R. B., Wessells N. K. Heavy meromyosin binding to microfilaments involved in cell and morphogenetic movements. Tissue Cell. 1973;5(1):37–46. doi: 10.1016/s0040-8166(73)80004-7. [DOI] [PubMed] [Google Scholar]
  34. Spooner B. S., Wessells N. K. An analysis of salivary gland morphogenesis: role of cytoplasmic microfilaments and microtubules. Dev Biol. 1972 Jan;27(1):38–54. doi: 10.1016/0012-1606(72)90111-x. [DOI] [PubMed] [Google Scholar]
  35. Terry A. H., Culp L. A. Substrate-attached glycoproteins from normal and virus-transformed cells. Biochemistry. 1974 Jan 29;13(3):414–425. doi: 10.1021/bi00700a004. [DOI] [PubMed] [Google Scholar]
  36. Trelstad R. L., Hayashi K., Toole B. P. Epithelial collagens and glycosaminoglycans in the embryonic cornea. Macromolecular order and morphogenesis in the basement membrane. J Cell Biol. 1974 Sep;62(3):815–830. doi: 10.1083/jcb.62.3.815. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Trelstad R. L., Kang A. H., Cohen A. M., Hay E. D. Collagen synthesis in vitro by embryonic spinal cord epithelium. Science. 1973 Jan 19;179(4070):295–297. doi: 10.1126/science.179.4070.295. [DOI] [PubMed] [Google Scholar]
  38. Vracko R. Basal lamina scaffold-anatomy and significance for maintenance of orderly tissue structure. Am J Pathol. 1974 Nov;77(2):314–346. [PMC free article] [PubMed] [Google Scholar]
  39. Wartiovaara J., Nordling S., Lehtonen E., Saxén L. Transfilter induction of kidney tubles: correlation with cytoplasmic penetration into nucleopore filters. J Embryol Exp Morphol. 1974 Jun;31(3):667–682. [PubMed] [Google Scholar]
  40. von der Mark H., von der Mark K., Gay S. Study of differential collagen synthesis during development of the chick embryo by immunofluorescence. I. Preparation of collagen type I and type II specific antibodies and their application to early stages of the chick embryo. Dev Biol. 1976 Feb;48(2):237–249. doi: 10.1016/0012-1606(76)90088-9. [DOI] [PubMed] [Google Scholar]

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