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. 1989 Sep 1;109(3):1279–1288. doi: 10.1083/jcb.109.3.1279

Cellular remodeling of HCO3(-)-secreting cells in rabbit renal collecting duct in response to an acidic environment

PMCID: PMC2115759  PMID: 2549077

Abstract

The renal cortical collecting duct (CCD) consists of principal and intercalated cells. Two forms of intercalated cells, those cells involved in H+/HCO3- transport, have recently been described. H+- secreting cells are capable of apical endocytosis and have H+ATPase on the apical membrane and a basolateral Cl-/HCO3- exchanger. HCO3(-)- secreting cells bind peanut agglutinin (PNA) to apical membrane receptors and have diffuse or basolateral distribution of H+ATPase; their Cl-/HCO3- exchanger is on the apical membrane. We found that 20 h after acid feeding of rabbits, there was a fourfold increase in number of cells showing apical endocytosis and a numerically similar reduction of cells binding PNA. Incubation of CCDs at pH 7.1 for 3-5 h in vitro led to similar, albeit less pronounced, changes. Evidence to suggest internalization and degradation of the PNA binding sites included a reduction in apical binding of PNA, decrease in pH in the environment of PNA binding, and incorporation of electron-dense PNA into cytoplasmic vesicles. Such remodeling was dependent on protein synthesis. There was also functional evidence for loss of apical Cl- /HCO3- exchange on PNA-labeled cells. Finally, net HCO3- flux converted from secretion to absorption after incubation at low pH. Thus, exposure of CCDs to low pH stimulates the removal/inactivation of apical Cl- /HCO3- exchangers and the internalization of other apical membrane components. Remodeling of PNA-labeled cells may mediate the change in polarity of HCO3- flux observed in response to acid treatment.

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Selected References

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  1. Al-Awqati Q. Proton-translocating ATPases. Annu Rev Cell Biol. 1986;2:179–199. doi: 10.1146/annurev.cb.02.110186.001143. [DOI] [PubMed] [Google Scholar]
  2. Alper S. L., Kopito R. R., Libresco S. M., Lodish H. F. Cloning and characterization of a murine band 3-related cDNA from kidney and from a lymphoid cell line. J Biol Chem. 1988 Nov 15;263(32):17092–17099. [PubMed] [Google Scholar]
  3. Alpern R. J. Mechanism of basolateral membrane H+/OH-/HCO-3 transport in the rat proximal convoluted tubule. A sodium-coupled electrogenic process. J Gen Physiol. 1985 Nov;86(5):613–636. doi: 10.1085/jgp.86.5.613. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Brown D., Gluck S., Hartwig J. Structure of the novel membrane-coating material in proton-secreting epithelial cells and identification as an H+ATPase. J Cell Biol. 1987 Oct;105(4):1637–1648. doi: 10.1083/jcb.105.4.1637. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Brown D., Hirsch S., Gluck S. An H+-ATPase in opposite plasma membrane domains in kidney epithelial cell subpopulations. Nature. 1988 Feb 18;331(6157):622–624. doi: 10.1038/331622a0. [DOI] [PubMed] [Google Scholar]
  6. Brown D., Weyer P., Orci L. Nonclathrin-coated vesicles are involved in endocytosis in kidney collecting duct intercalated cells. Anat Rec. 1987 Jul;218(3):237–242. doi: 10.1002/ar.1092180303. [DOI] [PubMed] [Google Scholar]
  7. Burg M., Green N. Bicarbonate transport by isolated perfused rabbit proximal convoluted tubules. Am J Physiol. 1977 Oct;233(4):F307–F314. doi: 10.1152/ajprenal.1977.233.4.F307. [DOI] [PubMed] [Google Scholar]
  8. Cannon C., van Adelsberg J., Kelly S., Al-Awqati Q. Carbon-dioxide-induced exocytotic insertion of H+ pumps in turtle-bladder luminal membrane: role of cell pH and calcium. Nature. 1985 Apr 4;314(6010):443–446. doi: 10.1038/314443a0. [DOI] [PubMed] [Google Scholar]
  9. Cosson P., de Curtis I., Pouysségur J., Griffiths G., Davoust J. Low cytoplasmic pH inhibits endocytosis and transport from the trans-Golgi network to the cell surface. J Cell Biol. 1989 Feb;108(2):377–387. doi: 10.1083/jcb.108.2.377. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Dani C., Blanchard J. M., Piechaczyk M., El Sabouty S., Marty L., Jeanteur P. Extreme instability of myc mRNA in normal and transformed human cells. Proc Natl Acad Sci U S A. 1984 Nov;81(22):7046–7050. doi: 10.1073/pnas.81.22.7046. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Daukas G., Zigmond S. H. Inhibition of receptor-mediated but not fluid-phase endocytosis in polymorphonuclear leukocytes. J Cell Biol. 1985 Nov;101(5 Pt 1):1673–1679. doi: 10.1083/jcb.101.5.1673. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Dobyan D. C., Bulger R. E. Renal carbonic anhydrase. Am J Physiol. 1982 Oct;243(4):F311–F324. doi: 10.1152/ajprenal.1982.243.4.F311. [DOI] [PubMed] [Google Scholar]
  13. Drenckhahn D., Schlüter K., Allen D. P., Bennett V. Colocalization of band 3 with ankyrin and spectrin at the basal membrane of intercalated cells in the rat kidney. Science. 1985 Dec 13;230(4731):1287–1289. doi: 10.1126/science.2933809. [DOI] [PubMed] [Google Scholar]
  14. Gluck S., Cannon C., Al-Awqati Q. Exocytosis regulates urinary acidification in turtle bladder by rapid insertion of H+ pumps into the luminal membrane. Proc Natl Acad Sci U S A. 1982 Jul;79(14):4327–4331. doi: 10.1073/pnas.79.14.4327. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kaissling B., Kriz W. Structural analysis of the rabbit kidney. Adv Anat Embryol Cell Biol. 1979;56:1–123. doi: 10.1007/978-3-642-67147-0. [DOI] [PubMed] [Google Scholar]
  16. Koeppen B. M., Biagi B. A., Giebisch G. H. Intracellular microelectrode characterization of the rabbit cortical collecting duct. Am J Physiol. 1983 Jan;244(1):F35–F47. doi: 10.1152/ajprenal.1983.244.1.F35. [DOI] [PubMed] [Google Scholar]
  17. Lombard W. E., Kokko J. P., Jacobson H. R. Bicarbonate transport in cortical and outer medullary collecting tubules. Am J Physiol. 1983 Mar;244(3):F289–F296. doi: 10.1152/ajprenal.1983.244.3.F289. [DOI] [PubMed] [Google Scholar]
  18. Lotspeich W. D. Metabolic aspects of acid-base change. Science. 1967 Mar 3;155(3766):1066–1075. doi: 10.1126/science.155.3766.1066. [DOI] [PubMed] [Google Scholar]
  19. McKinney T. D., Burg M. B. Bicarbonate absorption by rabbit cortical collecting tubules in vitro. Am J Physiol. 1978 Feb;234(2):F141–F145. doi: 10.1152/ajprenal.1978.234.2.F141. [DOI] [PubMed] [Google Scholar]
  20. McKinney T. D., Burg M. B. Bicarbonate transport by rabbit cortical collecting tubules. Effect of acid and alkali loads in vivo on transport in vitro. J Clin Invest. 1977 Sep;60(3):766–768. doi: 10.1172/JCI108830. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Ridderstrale Y., Kashgarian M., Koeppen B., Giebisch G., Stetson D., Ardito T., Stanton B. Morphological heterogeneity of the rabbit collecting duct. Kidney Int. 1988 Nov;34(5):655–670. doi: 10.1038/ki.1988.230. [DOI] [PubMed] [Google Scholar]
  22. Satlin L. M., Schwartz G. J. Postnatal maturation of rabbit renal collecting duct: intercalated cell function. Am J Physiol. 1987 Oct;253(4 Pt 2):F622–F635. doi: 10.1152/ajprenal.1987.253.4.F622. [DOI] [PubMed] [Google Scholar]
  23. Schuster V. L., Bonsib S. M., Jennings M. L. Two types of collecting duct mitochondria-rich (intercalated) cells: lectin and band 3 cytochemistry. Am J Physiol. 1986 Sep;251(3 Pt 1):C347–C355. doi: 10.1152/ajpcell.1986.251.3.C347. [DOI] [PubMed] [Google Scholar]
  24. Schwartz G. J., Al-Awqati Q. Carbon dioxide causes exocytosis of vesicles containing H+ pumps in isolated perfused proximal and collecting tubules. J Clin Invest. 1985 May;75(5):1638–1644. doi: 10.1172/JCI111871. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Schwartz G. J., Barasch J., Al-Awqati Q. Plasticity of functional epithelial polarity. 1985 Nov 28-Dec 4Nature. 318(6044):368–371. doi: 10.1038/318368a0. [DOI] [PubMed] [Google Scholar]
  26. Star R. A., Burg M. B., Knepper M. A. Bicarbonate secretion and chloride absorption by rabbit cortical collecting ducts. Role of chloride/bicarbonate exchange. J Clin Invest. 1985 Sep;76(3):1123–1130. doi: 10.1172/JCI112067. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Verlander J. W., Madsen K. M., Tisher C. C. Effect of acute respiratory acidosis on two populations of intercalated cells in rat cortical collecting duct. Am J Physiol. 1987 Dec;253(6 Pt 2):F1142–F1156. doi: 10.1152/ajprenal.1987.253.6.F1142. [DOI] [PubMed] [Google Scholar]
  28. Wade J. B., O'Neil R. G., Pryor J. L., Boulpaep E. L. Modulation of cell membrane area in renal collecting tubules by corticosteroid hormones. J Cell Biol. 1979 May;81(2):439–445. doi: 10.1083/jcb.81.2.439. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. van Adelsberg J., Al-Awqati Q. Regulation of cell pH by Ca+2-mediated exocytotic insertion of H+-ATPases. J Cell Biol. 1986 May;102(5):1638–1645. doi: 10.1083/jcb.102.5.1638. [DOI] [PMC free article] [PubMed] [Google Scholar]

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