Skip to main content
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1971 Jun 1;49(3):582–594. doi: 10.1083/jcb.49.3.582

CORRELATION BETWEEN PINOCYTOSIS AND HYDROOSMOSIS INDUCED BY NEUROHYPOPHYSEAL HORMONES AND MEDIATED BY ADENOSINE 3',5'-CYCLIC MONOPHOSPHATE

Sandra K Masur 1, Eric Holtzman 1, Irving L Schwartz 1, Roderich Walter 1
PMCID: PMC2108495  PMID: 4326455

Abstract

The isolated urinary bladder of the toad responds to neurohypophyseal hormone with a net increase of water transport from the mucosal to the serosal solution in the presence of an osmotic gradient. This response is mediated intracellularly by cyclic 3',5'-adenosine monophosphate (AMP). The present study demonstrates that hydroosmotically active substances such as oxytocin, dibutyryl cyclic 3',5'-AMP, and theophylline, but not hydroosmotically inactive substances, induce the uptake of horseradish peroxidase from the mucosal solution. Peroxidase taken up by the mucosal cells is demonstrable in small tubules and vesicles, and eventually accumulates in lysosomes. The uptake of peroxidase from the serosal solution into similar bodies in the mucosal cells is not hormone-dependent. It is also shown that peroxidase does not penetrate the tight junction from either the mucosal or serosal solution. These results extend previous findings which implicated the apical membrane of the mucosal epithelium as the site affected by neurohypophyseal hormones. A mechanism based on secretory phenomena is proposed as a framework for future investigations of apical membrane permeability changes and pinocytosis.

Full Text

The Full Text of this article is available as a PDF (1.3 MB).

Selected References

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

  1. Amsterdam A., Ohad I., Schramm M. Dynamic changes in the ultrastructure of the acinar cell of the rat parotid gland during the secretory cycle. J Cell Biol. 1969 Jun;41(3):753–773. doi: 10.1083/jcb.41.3.753. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. BARRNETT R. J., BALL E. G. Metabolic and ultrastructural changes induced in adipose tissue by insulin. J Biophys Biochem Cytol. 1960 Sep;8:83–101. doi: 10.1083/jcb.8.1.83. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. BENTLEY P. J. The effects of neurohypophysial extracts on the water transfer across the wall of the isolated urinary bladder of the toad Bufo marinus. J Endocrinol. 1958 Sep;17(3):201–209. doi: 10.1677/joe.0.0170201. [DOI] [PubMed] [Google Scholar]
  4. BUTCHER R. W., SUTHERLAND E. W. Adenosine 3',5'-phosphate in biological materials. I. Purification and properties of cyclic 3',5'-nucleotide phosphodiesterase and use of this enzyme to characterize adenosine 3',5'-phosphate in human urine. J Biol Chem. 1962 Apr;237:1244–1250. [PubMed] [Google Scholar]
  5. Bentley P. J. Neurohypophysial function in Amphibia: hormone activity in the plasma. J Endocrinol. 1969 Mar;43(3):359–369. doi: 10.1677/joe.0.0430359. [DOI] [PubMed] [Google Scholar]
  6. Brandt P. W., Freeman A. R. Plasma membrane: substructural changes correlated with electrical resistance and pinocytosis. Science. 1967 Feb 3;155(3762):582–585. doi: 10.1126/science.155.3762.582. [DOI] [PubMed] [Google Scholar]
  7. CHOI J. K. ELECTRON MICROSCOPY OF ABSORPTION OF TRACER MATERIALS BY TOAD URINARY BLADDER EPITHELIUM. J Cell Biol. 1965 May;25:175–192. doi: 10.1083/jcb.25.2.175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Civan M. M., Frazier H. S. The site of the stimulatory action of vasopressin on sodium transport in toad bladder. J Gen Physiol. 1968 May;51(5):589–605. doi: 10.1085/jgp.51.5.589. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cushman S. W. Structure-function relationships in the adipose cell. II. Pinocytosis and factors influencing its activity in the isolated adipose cell. J Cell Biol. 1970 Aug;46(2):342–353. doi: 10.1083/jcb.46.2.342. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. DiBona D. R., Civan M. M., Leaf A. The anatomic site of the transepithelial permeability barriers of toad bladder. J Cell Biol. 1969 Jan;40(1):1–7. doi: 10.1083/jcb.40.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. DiBona D. R., Civan M. M. Toad urinary bladder: intercellular spaces. Science. 1969 Aug 1;165(3892):503–504. doi: 10.1126/science.165.3892.503. [DOI] [PubMed] [Google Scholar]
  12. Eggena P., Schwartz I. L., Walter R. A sensitive hydroosmotic toad bladder assay. Affinity and intrinsic activity of neurohypophyseal peptides. J Gen Physiol. 1968 Sep;52(3):465–481. doi: 10.1085/jgp.52.3.465. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Eggena P., Schwartz I. L., Walter R. Threshold and receptor reserve in the action of neurohypophyseal peptides. A study of synergists and antagonists of the hydroosmotic response of the toad urinary bladder. J Gen Physiol. 1970 Aug;56(2):250–271. doi: 10.1085/jgp.56.2.250. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. FARQUHAR M. G., PALADE G. E. Junctional complexes in various epithelia. J Cell Biol. 1963 May;17:375–412. doi: 10.1083/jcb.17.2.375. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Graham R. C., Jr, Karnovsky M. J. The early stages of absorption of injected horseradish peroxidase in the proximal tubules of mouse kidney: ultrastructural cytochemistry by a new technique. J Histochem Cytochem. 1966 Apr;14(4):291–302. doi: 10.1177/14.4.291. [DOI] [PubMed] [Google Scholar]
  16. Gulyassy P. F. Metabolism of adenosine 3',5'-monophosphate by epithelial cells of the toad bladder. J Clin Invest. 1969 Nov;47(11):2458–2468. doi: 10.1172/JCI105928. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. HAYS R. M., LEAF A. Studies on the movement of water through the isolated toad bladder and its modification by vasopressin. J Gen Physiol. 1962 May;45:905–919. doi: 10.1085/jgp.45.5.905. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Handler J. S., Butcher R. W., Sutherland E. W., Orloff J. The effect of vasopressin and of theophylline on the concentration of adenosine 3',5'-phosphate in the urinary bladder of the toad. J Biol Chem. 1965 Nov;240(11):4524–4526. [PubMed] [Google Scholar]
  19. Holtzman E., Dominitz R. Cytochemical studies of lysosomes, golgi apparatus and endoplasmic reticulum in secretion and protein uptake by adrenal medulla cells of the rat. J Histochem Cytochem. 1968 May;16(5):320–336. doi: 10.1177/16.5.320. [DOI] [PubMed] [Google Scholar]
  20. Karnovsky M. J. The ultrastructural basis of capillary permeability studied with peroxidase as a tracer. J Cell Biol. 1967 Oct;35(1):213–236. doi: 10.1083/jcb.35.1.213. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. LEAF A., HAYS R. M. Permeability of the isolated toad bladder to solutes and its modification by vasopressin. J Gen Physiol. 1962 May;45:921–932. doi: 10.1085/jgp.45.5.921. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. LUFT J. H. Improvements in epoxy resin embedding methods. J Biophys Biochem Cytol. 1961 Feb;9:409–414. doi: 10.1083/jcb.9.2.409. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Loewenstein W. R., Socolar S. J., Higashino S., Kanno Y., Davidson N. Intercellular Communication: Renal, Urinary Bladder, Sensory, and Salivary Gland Cells. Science. 1965 Jul 16;149(3681):295–298. doi: 10.1126/science.149.3681.295. [DOI] [PubMed] [Google Scholar]
  24. Manning M. Synthesis by the Merrifield method of a protected nonapeptide amide with the amino acid sequence of oxytocin. J Am Chem Soc. 1968 Feb 28;90(5):1348–1349. doi: 10.1021/ja01007a041. [DOI] [PubMed] [Google Scholar]
  25. Masur S. K., Holtzman E. Lysosomes and secretory granules in the normal and autotransplanted salmander pars distalis. Gen Comp Endocrinol. 1969 Feb;12(1):33–39. doi: 10.1016/0016-6480(69)90134-8. [DOI] [PubMed] [Google Scholar]
  26. Merrifield R. B. Solid-phase peptide synthesis. Adv Enzymol Relat Areas Mol Biol. 1969;32:221–296. doi: 10.1002/9780470122778.ch6. [DOI] [PubMed] [Google Scholar]
  27. NOVIKOFF A. B., ESSNER E., QUINTANA N. GOLGI APPARATUS AND LYSOSOMES. Fed Proc. 1964 Sep-Oct;23:1010–1022. [PubMed] [Google Scholar]
  28. ORLOFF J., HANDLER J. S. The similarity of effects of vasopressin, adenosine-3',5'-phosphate (cyclic AMP) and theophylline on the toad bladder. J Clin Invest. 1962 Apr;41:702–709. doi: 10.1172/JCI104528. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. PAK POY R. F., BENTLEY P. J. Fine structure of the epithelial cells of the toad urinary bladder. Exp Cell Res. 1960 Jun;20:235–237. doi: 10.1016/0014-4827(60)90246-9. [DOI] [PubMed] [Google Scholar]
  30. PALADE G. E. A study of fixation for electron microscopy. J Exp Med. 1952 Mar;95(3):285–298. doi: 10.1084/jem.95.3.285. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. PEACHEY L. D., RASMUSSEN H. Structure of the toad's urinary bladder as related to its physiology. J Biophys Biochem Cytol. 1961 Aug;10:529–553. doi: 10.1083/jcb.10.4.529. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Pastan I., Wollman S. H. Colloid droplet formation in dog thyroid in vitro. Induction by dibutyrl cyclic-AMP. J Cell Biol. 1967 Oct;35(1):262–266. doi: 10.1083/jcb.35.1.262. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. RASMUSSEN H., SCHWARTZ I. L., YOUNG R., MARC-AURELE J. STRUCTURAL REQUIREMENTS FOR THE ACTION OF NEUROHYPOPHYSEAL HORMONES UPON THE ISOLATED AMPHIBIAN URINARY BLADDER. J Gen Physiol. 1963 Jul;46:1171–1189. doi: 10.1085/jgp.46.6.1171. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. REYNOLDS E. S. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol. 1963 Apr;17:208–212. doi: 10.1083/jcb.17.1.208. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Rasmussen H. Cell communication, calcium ion, and cyclic adenosine monophosphate. Science. 1970 Oct 23;170(3956):404–412. doi: 10.1126/science.170.3956.404. [DOI] [PubMed] [Google Scholar]
  36. SABATINI D. D., BENSCH K., BARRNETT R. J. Cytochemistry and electron microscopy. The preservation of cellular ultrastructure and enzymatic activity by aldehyde fixation. J Cell Biol. 1963 Apr;17:19–58. doi: 10.1083/jcb.17.1.19. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Schwartz I. L., Walter R. Factors influencing the reactivity of the toad bladder to the hydro-osmotic action of vasopressin. Am J Med. 1967 May;42(5):769–776. doi: 10.1016/0002-9343(67)90094-0. [DOI] [PubMed] [Google Scholar]
  38. WATSON M. L. Staining of tissue sections for electron microscopy with heavy metals. J Biophys Biochem Cytol. 1958 Jul 25;4(4):475–478. doi: 10.1083/jcb.4.4.475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Walter R., Schwartz I. L. 5-Valine-oxytocin and 1-deamino-5-valine-oxytocin. Syntheses and some pharmacological properties. J Biol Chem. 1966 Dec 10;241(23):5500–5503. [PubMed] [Google Scholar]
  40. Wetzel B. K., Spicer S. S., Wollman S. H. Changes in fine structure and acid phosphatase localization in rat thyroid cells following thyrotropin administration. J Cell Biol. 1965 Jun;25(3):593–618. doi: 10.1083/jcb.25.3.593. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES