Skip to main content
PMC home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1982 Nov 1;95(2):394–402. doi: 10.1083/jcb.95.2.394

Alterations in alveolar basement membranes during postnatal lung growth

PMCID: PMC2112950  PMID: 7142296

Abstract

We studied the ultrastructural characteristics of alveolar basement membranes (ABM) and capillary basement membranes (CBM) in rat lungs at birth, at 8-10 d of age, during alveolar formation, and at 6-10 wk of age, after most alveoli have formed. We also measured in vitro lung proteoglycan and heparan sulfate synthesis at each age. We noted three major age-related changes in pulmonary basement membranes. (a) Discontinuities in the ABM through which basilar cytoplasmic foot processes extend are present beneath alveolar type-2 cells but not alveolar type-1 cells. These discontinuities are most prevalent at birth but also exist in the adult. (b) Discontinuities are also present in CBM at the two earliest time points but are maximal at 8 d of age rather than at birth. Fusions between ABM and CBM are often absent at 8 d of age, but CBM and CBM/ABM fusions were complete in the adult. (c) Heparan sulfate proteoglycans identified with ruthenium red and selective enzyme degradation are distributed equally on epithelial and interstitial sides of the ABM lamina densa at birth, but decrease on the interstitial side with age. In vitro proteoglycan and heparan sulfate accumulation at birth was two times that at 8 d and five times that in the adult. Discontinuities in ABM allow epithelial-mesenchymal interactions that may influence type-2 cells cytodifferentiation. Discontinuities in CBM suggest that capillary proliferation and neovascularization are associated with alveolar formation at 8 d. When CBM becomes complete and forms junctions with ABM, lung neovascularization likely ends as does the ability to form new alveoli.

Full Text

The Full Text of this article is available as a PDF (4.2 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. ALESCIO T., CASSINI A. Induction in vitro of tracheal buds by pulmonary mesenchyme grafted on tracheal epithelium. J Exp Zool. 1962 Jul;150:83–94. doi: 10.1002/jez.1401500202. [DOI] [PubMed] [Google Scholar]
  2. Alquier C., Fayet G., Hovsepian S., Michel-Béchet M. Biosynthesis of the basal lamina as a result of interaction between thyroid and mesenchymal cells in culture. Cell Tissue Res. 1979 Aug 3;200(1):69–81. doi: 10.1007/BF00236888. [DOI] [PubMed] [Google Scholar]
  3. Ausprunk D. H., Boudreau C. L., Nelson D. A. Proteoglycans in the microvascular. II. Histochemical localization in proliferating capillaries of the rabbit cornea. Am J Pathol. 1981 Jun;103(3):367–375. [PMC free article] [PubMed] [Google Scholar]
  4. Ausprunk D. H., Folkman J. Migration and proliferation of endothelial cells in preformed and newly formed blood vessels during tumor angiogenesis. Microvasc Res. 1977 Jul;14(1):53–65. doi: 10.1016/0026-2862(77)90141-8. [DOI] [PubMed] [Google Scholar]
  5. Banerjee S. D., Cohn R. H., Bernfield M. R. Basal lamina of embryonic salivary epithelia. Production by the epithelium and role in maintaining lobular morphology. J Cell Biol. 1977 May;73(2):445–463. doi: 10.1083/jcb.73.2.445. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bluemink J. G., Van Maurik P., Lawson K. A. Intimate cell contacts at the epithelial/mesenchymal interface in embryonic mouse lung. J Ultrastruct Res. 1976 May;55(2):257–270. doi: 10.1016/s0022-5320(76)80071-8. [DOI] [PubMed] [Google Scholar]
  7. Brody J. S., Burki R., Kaplan N. Deoxyribonucleic acid synthesis in lung cells during compensatory lung growth after pneumonectomy. Am Rev Respir Dis. 1978 Feb;117(2):307–316. doi: 10.1164/arrd.1978.117.2.307. [DOI] [PubMed] [Google Scholar]
  8. Buhain W. J., Brody J. S. Compensatory growth of the lung following pneumonectomy. J Appl Physiol. 1973 Dec;35(6):898–902. doi: 10.1152/jappl.1973.35.6.898. [DOI] [PubMed] [Google Scholar]
  9. Burri P. H., Dbaly J., Weibel E. R. The postnatal growth of the rat lung. I. Morphometry. Anat Rec. 1974 Apr;178(4):711–730. doi: 10.1002/ar.1091780405. [DOI] [PubMed] [Google Scholar]
  10. Burri P. H. The postnatal growth of the rat lung. 3. Morphology. Anat Rec. 1974 Sep;180(1):77–98. doi: 10.1002/ar.1091800109. [DOI] [PubMed] [Google Scholar]
  11. Culp L. A., Rollins B. J., Buniel J., Hitri S. Two functionally distinct pools of glycosaminoglycan in the substrate adhesion site of murine cells. J Cell Biol. 1978 Dec;79(3):788–801. doi: 10.1083/jcb.79.3.788. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Cutler L. S. The dependent and independent relationships between cytodifferentiation and morphogenesis in developing salivary gland secretory cells. Anat Rec. 1980 Mar;196(3):341–347. doi: 10.1002/ar.1091960310. [DOI] [PubMed] [Google Scholar]
  13. David G., Bernfield M. R. Collagen reduces glycosaminoglycan degradation by cultured mammary epithelial cells: possible mechanism for basal lamina formation. Proc Natl Acad Sci U S A. 1979 Feb;76(2):786–790. doi: 10.1073/pnas.76.2.786. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Evans M. J., Cabral L. J., Stephens R. J., Freeman G. Transformation of alveolar type 2 cells to type 1 cells following exposure to NO2. Exp Mol Pathol. 1975 Feb;22(1):142–150. doi: 10.1016/0014-4800(75)90059-3. [DOI] [PubMed] [Google Scholar]
  15. Gill P. J., Adler J., Silbert C. K., Silbert J. E. Removal of glycosaminoglycans from cultures of human skin fibroblasts. Biochem J. 1981 Jan 15;194(1):299–307. doi: 10.1042/bj1940299. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Haies D. M., Gil J., Weibel E. R. Morphometric study of rat lung cells. I. Numerical and dimensional characteristics of parenchymal cell population. Am Rev Respir Dis. 1981 May;123(5):533–541. doi: 10.1164/arrd.1981.123.5.533. [DOI] [PubMed] [Google Scholar]
  17. Hay E. D., Meier S. Stimulation of corneal differentiation by interaction between cell surface and extracellular matrix. II. Further studies on the nature and site of transfilter "induction". Dev Biol. 1976 Aug;52(1):141–157. doi: 10.1016/0012-1606(76)90014-2. [DOI] [PubMed] [Google Scholar]
  18. Kauffman S. L., Burri P. H., Weibel E. R. The postnatal growth of the rat lung. II. Autoradiography. Anat Rec. 1974 Sep;180(1):63–76. doi: 10.1002/ar.1091800108. [DOI] [PubMed] [Google Scholar]
  19. Kleinman H. K., Klebe R. J., Martin G. R. Role of collagenous matrices in the adhesion and growth of cells. J Cell Biol. 1981 Mar;88(3):473–485. doi: 10.1083/jcb.88.3.473. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Lilja S., Barrach H. J. An electron microscopical study of the influence of different glycosaminoglycans on the fibrillogenesis of collagen type I and II in vitro. Virchows Arch A Pathol Anat Histol. 1981;390(3):325–338. doi: 10.1007/BF00496562. [DOI] [PubMed] [Google Scholar]
  21. Merrilees M. J., Scott L. Interaction of epithelial cells and fibroblasts in culture: effect on glycosaminoglycan levels. Dev Biol. 1980 May;76(2):396–409. doi: 10.1016/0012-1606(80)90388-7. [DOI] [PubMed] [Google Scholar]
  22. Oegema T. R., Jr, Laidlaw J., Hascall V. C., Dziewiatkowski D. D. The effect of proteoglycans on the formation of fibrils from collagen solutions. Arch Biochem Biophys. 1975 Oct;170(2):698–709. doi: 10.1016/0003-9861(75)90167-8. [DOI] [PubMed] [Google Scholar]
  23. Saxén L., Lehtonen E. Transfilter induction of kidney tubules as a function of the extent and duration of intercellular contacts. J Embryol Exp Morphol. 1978 Oct;47:97–109. [PubMed] [Google Scholar]
  24. Schubert D., LaCorbiere M. A role of secreted glycosaminoglycans in cell-substratum adhesion. J Biol Chem. 1980 Dec 10;255(23):11564–11569. [PubMed] [Google Scholar]
  25. Smith B. T., Galaugher W., Thurlbeck W. M. Serum from pneumonectomized rabbits stimulates alveolar type II cell proliferation in vitro. Am Rev Respir Dis. 1980 Apr;121(4):701–707. doi: 10.1164/arrd.1980.121.4.701. [DOI] [PubMed] [Google Scholar]
  26. Smith B. T. Lung maturation in the fetal rat: acceleration by injection of fibroblast-pneumonocyte factor. Science. 1979 Jun 8;204(4397):1094–1095. doi: 10.1126/science.582216. [DOI] [PubMed] [Google Scholar]
  27. Solursh M., Singley C. T., Reiter R. S. The influence of epithelia on cartilage and loose connective tissue formation by limb mesenchyme cultures. Dev Biol. 1981 Sep;86(2):471–482. doi: 10.1016/0012-1606(81)90205-0. [DOI] [PubMed] [Google Scholar]
  28. Strang L. B. Growth and development of the lung: fetal and postnatal. Annu Rev Physiol. 1977;39:253–276. doi: 10.1146/annurev.ph.39.030177.001345. [DOI] [PubMed] [Google Scholar]
  29. Sugrue S. P., Hay E. D. Response of basal epithelial cell surface and Cytoskeleton to solubilized extracellular matrix molecules. J Cell Biol. 1981 Oct;91(1):45–54. doi: 10.1083/jcb.91.1.45. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Thesleff I., Barrach H. J., Foidart J. M., Vaheri A., Pratt R. M., Martin G. R. Changes in the distribution of type IV collagen, laminin, proteoglycan, and fibronectin during mouse tooth development. Dev Biol. 1981 Jan 15;81(1):182–192. doi: 10.1016/0012-1606(81)90361-4. [DOI] [PubMed] [Google Scholar]
  31. Vaccaro C. A., Brody J. S. Structural features of alveolar wall basement membrane in the adult rat lung. J Cell Biol. 1981 Nov;91(2 Pt 1):427–437. doi: 10.1083/jcb.91.2.427. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Vaccaro C. A., Brody J. S. Ultrastructural localization and characterization of proteoglycans in the pulmonary alveolus. Am Rev Respir Dis. 1979 Oct;120(4):901–910. doi: 10.1164/arrd.1979.120.4.901. [DOI] [PubMed] [Google Scholar]
  33. Wicha M. S., Liotta L. A., Vonderhaar B. K., Kidwell W. R. Effects of inhibition of basement membrane collagen deposition on rat mammary gland development. Dev Biol. 1980 Dec;80(2):253–256. doi: 10.1016/0012-1606(80)90402-9. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES