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PMID: 2910910 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Cytoplasmic pH regulation and chloride/bicarbonate exchange in avian osteoclasts.

The Journal of clinical investigation ·Vol. 83 ·No. 1 ·1989-01-00 ·Pages 227-33

Teti A, Blair HC, Teitelbaum SL, Kahn AJ, Koziol C, Konsek J, Zambonin-Zallone A, Schlesinger PH

Abstract

Osteoclasts resorb bone by first attaching to the bone surface and then secreting protons into an isolated extracellular compartment formed at the cell-bone attachment site. This secretion of protons (local acidification) is required to solubilize bone hydroxyapatite crystals and for activity of bone collagen-degrading acid proteases. However, the large quantity of protons required, 2 mol/mol of calcium, would result in an equal accumulation of cytosolic base equivalents. This alkaline load must be corrected to maintain cytosolic pH within physiologic limits. In this study, we have measured cytoplasmic pH with pH-sensitive fluorescent compounds, while varying the extracellular ionic composition of the medium, to determine the nature of the compensatory mechanism used by osteoclasts during bone resorption. Our data show that osteoclasts possess a chloride/bicarbonate exchanger that enables them to maintain normal intracellular pH in the face of a significant proton efflux. This conclusion follows from the demonstration of a dramatic cytoplasmic acidification when osteoclasts that have been incubated in bicarbonate-containing medium are transferred into bicarbonate-free medium. This acidification is absolutely dependent on and proportional to medium [Cl-]. Furthermore, acidification is inhibited by the classic inhibitor of red cell anion exchange, 4,4'-diisothiocyanatostilbene-2,2'-disulfonate, and by diphenylamine-2-carboxylate, an inhibitor of chloride specific channels. However, the acidification process is neither energy nor sodium dependent. The physiologic importance of chloride/bicarbonate exchange is demonstrated by the chloride dependence of recovery from an endogenous or exogenous alkaline load in osteoclasts. We conclude that chloride/bicarbonate exchange is in large part responsible for cytoplasmic pH homeostasis of active osteoclasts, showing that these cells are similar to renal tubular epithelial cells in their regulation of intracellular pH.

MeSH Terms
Animals Bicarbonates/pharmacology Carrier Proteins/metabolism Chickens Chloride-Bicarbonate Antiporters Cytoplasm/metabolism Hydrogen-Ion Concentration Osteoclasts/metabolism
Chemicals
Bicarbonates Carrier Proteins Chloride-Bicarbonate Antiporters
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Teti A
Institute of Human Anatomy, University of Bari Medical School, Italy.
Blair H C
Teitelbaum S L
Kahn A J
Koziol C
Konsek J
Zambonin-Zallone A
Schlesinger P H
References (32)
32 references, click to expand
  1. On the mechanisms of bone resorption. The action of parathyroid hormone on the excretion and synthesis of lysosomal enzymes and on the extracellular release of acid by bone cells.
    J Cell Biol. 1968 Dec;39(3):676-97 PMID: 5699937
  2. Physiologic and pharmacologic regulation of bone resorption.
    N Engl J Med. 1970 Apr 16;282(16):909-16 PMID: 4314044
  3. Acid phosphatase of osteoclasts demonstrated by electron microscopic histochemistry.
    Histochemie. 1971;28(2):103-17 PMID: 5137661
  4. Fine structural localization of acid phosphomonoesterase in the brush border region of osteoclasts.
    Histochemie. 1971;28(4):337-44 PMID: 5159900
  5. Electron microscopic localization of hydrolytic enzymes in osteoclasts.
    Histochem J. 1972 May;4(3):245-58 PMID: 4340739
  6. Intracellular pH transients in squid giant axons caused by CO2, NH3, and metabolic inhibitors.
    J Gen Physiol. 1976 Jan;67(1):91-112 PMID: 1460
  7. Fluorescence probe measurement of the intralysosomal pH in living cells and the perturbation of pH by various agents.
    Proc Natl Acad Sci U S A. 1978 Jul;75(7):3327-31 PMID: 28524
  8. Comparison of the effects of stimulators and inhibitors of resorption on the release of lysosomal enzymes and radioactive calcium from fetal bone in organ culture.
    Endocrinology. 1978 Dec;103(6):1969-75 PMID: 748028
  9. Intracellular pH measurements in Ehrlich ascites tumor cells utilizing spectroscopic probes generated in situ.
    Biochemistry. 1979 May 29;18(11):2210-8 PMID: 36128
  10. Rodent peritoneal macrophages as bone resorbing cells.
    Calcif Tissue Int. 1979 Jul 3;27(3):255-61 PMID: 114287
  11. Electrogenic proton transport in epithelial membranes.
    J Membr Biol. 1982;65(3):155-74 PMID: 6460866
  12. Cytoplasmic pH and free Mg2+ in lymphocytes.
    J Cell Biol. 1982 Oct;95(1):189-96 PMID: 6815204
  13. Isolated osteoclasts in primary culture: first observations on structure and survival in culture media.
    Anat Embryol (Berl). 1982 Dec;165(3):405-13 PMID: 7158821
  14. Bicarbonate transport in cortical and outer medullary collecting tubules.
    Am J Physiol. 1983 Mar;244(3):F289-96 PMID: 6829761
  15. Carbonic anhydrase II deficiency identified as the primary defect in the autosomal recessive syndrome of osteopetrosis with renal tubular acidosis and cerebral calcification.
    Proc Natl Acad Sci U S A. 1983 May;80(9):2752-6 PMID: 6405388
  16. Anion dependence of rabbit medullary collecting duct acidification.
    J Clin Invest. 1983 May;71(5):1505-8 PMID: 6853724
  17. Activation of Na+/H+ exchange by epidermal growth factor elevates intracellular pH in A431 cells.
    J Biol Chem. 1983 Oct 25;258(20):12644-53 PMID: 6195155
  18. Carbonic anhydrase activity in isolated osteoclasts.
    Metab Bone Dis Relat Res. 1983-1984;5(1):33-9 PMID: 6423928
  19. An electrogenic proton-translocating adenosine triphosphatase from bovine kidney medulla.
    J Clin Invest. 1984 Jun;73(6):1704-10 PMID: 6327769
  20. Electrophysiological analysis of bicarbonate permeation across the peritubular cell membrane of rat kidney proximal tubule. II. Exclusion of HCO3(-)-effects on other ion permeabilities and of coupled electroneutral HCO3(-)-transport.
    Pflugers Arch. 1984 May;401(1):43-51 PMID: 6089091
  21. Cell-substratum interaction of cultured avian osteoclasts is mediated by specific adhesion structures.
    J Cell Biol. 1984 Nov;99(5):1696-705 PMID: 6436255
  22. Transient increase in intracellular pH during Dictyostelium differentiation.
    J Cell Biol. 1984 Nov;99(5):1883-7 PMID: 6092389
  23. Conductive properties of the rabbit outer medullary collecting duct: inner stripe.
    Am J Physiol. 1985 Apr;248(4 Pt 2):F500-6 PMID: 3985156
  24. Role of carbonic anhydrase in bone resorption induced by 1,25 dihydroxyvitamin D3 in vitro.
    Calcif Tissue Int. 1985 Mar;37(2):134-42 PMID: 3924369
  25. Cell-mediated extracellular acidification and bone resorption: evidence for a low pH in resorbing lacunae and localization of a 100-kD lysosomal membrane protein at the osteoclast ruffled border.
    J Cell Biol. 1985 Dec;101(6):2210-22 PMID: 3905822
  26. Intracellular pH regulation and proton transport by rabbit renal medullary collecting duct cells. Role of plasma membrane proton adenosine triphosphatase.
    J Clin Invest. 1986 Jan;77(1):113-20 PMID: 2418058
  27. A perspective on antimalarial action: effects of weak bases on Plasmodium falciparum.
    Biochem Pharmacol. 1986 Feb 15;35(4):547-52 PMID: 3511916
  28. Isolated osteoclasts resorb the organic and inorganic components of bone.
    J Cell Biol. 1986 Apr;102(4):1164-72 PMID: 3457013
  29. Intracellular pH regulation in rabbit renal medullary collecting duct cells. Role of chloride-bicarbonate exchange.
    J Clin Invest. 1986 May;77(5):1682-8 PMID: 2871045
  30. Rous sarcoma virus-transformed fibroblasts and cells of monocytic origin display a peculiar dot-like organization of cytoskeletal proteins involved in microfilament-membrane interactions.
    Exp Cell Res. 1987 Mar;169(1):202-14 PMID: 3028844
  31. Diphenylamine-2-carboxylate blocks Cl(-)-HCO3- exchange in Necturus gallbladder epithelium.
    Am J Physiol. 1987 Jul;253(1 Pt 1):C79-89 PMID: 3605330
  32. [Histochemical contribution to the study of bone construction and destruction].
    Presse Med. 1951 Sep 22;59(60):1240-42 PMID: 14875726
Article Info
Journal
The Journal of clinical investigation
Abbr.
J Clin Invest
ISSN
0021-9738
Published
1989-01-00
Pages
227-33
Language
English
Region
United States
NLM ID
7802877
PMCID
PMC303666
Subset
IM
Grants
NIADDK NIH HHS · AM-32788 · United States
NIAMS NIH HHS · AR-01631 · United States
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