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Effect of vitamin D status on the activity of carbonic anhydrase in chicken epiphysis and kidney

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Chickens were raised for 6 weeks from the date of hatch under red light on a vitamin D-free diet; controls were given an oral vitamin D supplement. Vitamin D-deficient animals showed decreased total serum calcium concentration and decreased DNA content in epiphysis and kidney homogenates. In calcifying epiphysis, total carbonic anhydrase (CA) activity was decreased, but activity per μg DNA was slightly increased and specific activity was double that of the controls. Polyacrylamide gel isoelectric focusing after preparation of the enzyme showed a picture similar to that seen after parathyroid hormone (PTH) administration in chicks; therefore, this could be considered a secondary hyperparathyroidism. The CA activation was not seen in the kidney which can be explained by induction of an endogenous inhibitor protein of the cyclic AMP-dependent protein kinase exclusively in the kidney in vitamin D deficiency. In an additional experiment, chickens were raised for 3 weeks from the date of hatch under red light on a vitamin D-free diet. Daily oral substitution by different vitamin D metabolites (1,25 (OH)2D3, 25OHD3, 24, 25(OH)2D3) over 7 days led to CA activation compared with controls probably by restoring protein kinase activity in the kidney. Our results show that CA activity is inversely correlated with serum calcium concentrations which is in agreement with a regulatory mechanism recently proposed by us.

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References

  1. Arey LB (1920) The origin, growth and fate of osteoclasts and their relation to bone resorption. Am J Anat 26:315–345

    Article  Google Scholar 

  2. Vaes G (1968) On the mechanisms of bone resportion. The action of parathyroid hormone on the excretion and synthesis of lysosomal enzymes on the extracellular release of acid by bone cells. J Cell Biol 39:676–679

    Article  PubMed  CAS  Google Scholar 

  3. Fallon MD (1984) Bone-resorbing fluid from osteoclasts is acid: an in vitro micropuncture study. In: Cohn DV, Fujita P, Potts Jr, JT, Talmage RV (eds) Endocrine control of bone and calcium metabolism. Elsevier Science Publisher BV, Amsterdam

    Google Scholar 

  4. Blair HC, Ghandur-Mnaymneh L (1985) Macrophage-mediated bone resorption occurs in an acidic environment. Calcif Tissue Int 37:547–550

    PubMed  CAS  Google Scholar 

  5. Janowitz HD, Colcher H, Hollander F (1952) Inhibition of gastric secretion of acids in dogs by carbonic-anhydrase inhibitors: 2-acetyl-amino-1.3.4-thiodizole-5-sulfonamide. Am J Physiol 171:325

    PubMed  CAS  Google Scholar 

  6. Siegmund P, Dulce HJ, Koerber F, Schuette E (1959) Ueber den Einfluss von Carboanhydrase-Inhibitoren auf erhoehte Plasma-Calcium-Werte und das Vorkommen von Carboanhydrase im Epiphysenknorpel und Knochen. Naturwiss 46:358

    Article  CAS  Google Scholar 

  7. Siegmund P, Dulce HJ (1960) Zur Biochemie der Knochenaufloesung I. Einfluss des Carboanhydrase-Inhibitors 2-Acetamino 1.3.4.-thiodiazol-sulfonamid-(5) (DIAMOX) auf den Calciumstoffwechsel bei Legehennen. Hoppe-Seyler's Z Physiol Chem 300:149–159

    Google Scholar 

  8. Dulce HJ, Siegmund P, Schuette E (1960) Zur Biochemie der Knochenaufloesung II. Der Einfluss von DIAMOX auf das Plasma-Calcium oestron-behandelter Haehne. Hoppe-Seyler's Z Physiol Chem 320:160–162

    PubMed  CAS  Google Scholar 

  9. Dulce HJ, Siegmund P, Schuette E (1960) Zur Biochemie der Knochenaufloesung III. Ueber das Vorkommen der Carboanhydrase im Knochen Hoppe-Seyler's Z Physiol Chem 320:160–162

    PubMed  CAS  Google Scholar 

  10. Siegmund P, Bauditz W (1965) Die Wirkung von Azetazolamid auf den Anstieg der Plasma-Calcium-Werte nach Parathormon. Arch Exp Pathol Pharmak 251:288–294

    CAS  Google Scholar 

  11. Waite LC, Volkert WA, Kenny AD (1970) Inhibition of bone resorption by acetazolamide in the rat. Endocrinology 87:1129–1139

    PubMed  CAS  Google Scholar 

  12. Minkin C, Jennings JM (1972) Carbonic anhydrase and bone remodeling: sulfonamide inhibition of bone resorption in organ culture. Science 176:1031–1033

    Article  PubMed  CAS  Google Scholar 

  13. Waite LC (1972) Carbonic anhydrase inhibitors, parathyroid hormone and calcium metabolism. Endocrinology 91:1160–1165

    PubMed  CAS  Google Scholar 

  14. Maren TH (1967) Carbonic anhydrase: chemistry, physiology and inhibition. Physiol Reviews 47 (reprint) 595–781

    CAS  Google Scholar 

  15. Maren TH (1984) The general physiology of reactions catalyzed by carbonic anhydrase and their inhibition by sulfonamides. Ann NY Acad Sci 429:568–579

    Article  PubMed  CAS  Google Scholar 

  16. Conaway HH, Waite LC, Kenny AD (1973) Immobilization and bone mass in rats. Effects of parathyroidectomy and acetazolamide. Calcif Tissue Res 11:323–330

    Article  PubMed  CAS  Google Scholar 

  17. Kenny AD (1985) Role of carbonic anhydrase in bone: partial inhibition of disuse atrophy of bone by parenteral acetazolamide. Calcif Tissue Int 37:126–133

    PubMed  CAS  Google Scholar 

  18. Holke ME (1974) Die Wirkungen von Parathormon auf die Carboanhydrase-Aktivitaet in der Niere, thesis. Free Universität Berlin

  19. Anderson RE, Jee WSS, Woodbury DM (1985) Stimulation of carbonic anhydrase in osteoclasts by parathyroid hormone. Calcif Tissue Int 37:646–650

    PubMed  CAS  Google Scholar 

  20. Siegmund P, Tuellmann A, Holke M (1974) The cyclic AMP-mediated action of epinephrine on the activity of carbonic anhydrase in avian erythrocytes. Horm Metab Res 6:158–161

    PubMed  CAS  Google Scholar 

  21. Narumi S, Kanno M (1973) Effects of gastric acid stimulants and inhibitors on the activity of HCO3-stimulated, Mg2+-dependent ATPase and carbonic anhydrase in rat gastric mucosa. Biochim Biophys Acta 311:80–89

    Article  PubMed  CAS  Google Scholar 

  22. Narumi S, Maki Y (1973) Possible role of cyclic AMP in gastric acid secretion in rat. Biochim Biophys Acta 311:90–97

    Article  PubMed  CAS  Google Scholar 

  23. Narumi S, Miyamoto E (1974) Activation and phosphorylation of carbonic anhydrase by adenosine 3′, 5′-monophosphate-dependent protein kinase. Biochim Biophys Acta 350:215–224

    PubMed  CAS  Google Scholar 

  24. Dietsch P, Siegmund P (1978) Mechanism of activation of carbonic anhydrase by parathyroid hormone. In: Copp DV, Talmage RV (eds) Endocrinology of calcium metabolism. Excerpta Medica, Amsterdam-Oxford

    Google Scholar 

  25. Dietsch P, Siegmund P (1984) Carbonic anhydrase—an interconvertible enzyme. Ann NY Acad Sci 429:243–244

    Article  CAS  Google Scholar 

  26. Brommage P, Neuman WF (1979) Mechanism of mobilization of bone mineral by 1,25-dihydroxyvitamin D3. Am J Physiol 237:E113-E120

    PubMed  CAS  Google Scholar 

  27. Anderson RE, Gay CV, Schraer H (1981) Ultrastructural localization of carbonic anhydrase in active and inactive osteoclasts Calcif Tissue Int 33:290

    Article  Google Scholar 

  28. Tanaka Y, DeLuca HF (1971) Bone mineral mobilization activity of 1,25-dihydroxycholecalciferol, a metabolite of vitamin D. Arch Biochem Biophys 146:574–578

    Article  PubMed  CAS  Google Scholar 

  29. Gebauer U, Fleisch H (1978) Effect of 1,25-dihydroxycholecalciferol on adenosine 3′, 5′-cyclic monophosphate production in calvaria of mice. Calcif Tissue Res 25:223–225

    Article  PubMed  CAS  Google Scholar 

  30. Pierce WM, Lineberry MD, Waite LC (1982) Effects of sulfonamides on the hypercalcemic response to vitamin D. Horm Metab Res 14:670–673

    Article  PubMed  CAS  Google Scholar 

  31. Hall GE, Kenny AD (1985) Carbonic anhydrase and 1,25-dihydroxycholecalciferol-induced bone resorption. Calcif Tissue Int 37:134–142

    PubMed  CAS  Google Scholar 

  32. Narbaitz R, Kacew S, Sitwell L (1984) The role of vitamin D3 metabolites on the regulation of carbonic anhydrase activity in the chorionic epithelium of the chick. Ann NY Acad 429:479–480

    Article  CAS  Google Scholar 

  33. Stahl PD, Kenny AD (1969) Studies on the mechanism of action of thyreocalcitonin: inhibition with acetazolamide. Endocrinology 85:16–18

    Google Scholar 

  34. Gay CV, Schraer H, Anderson RE, Cao H (1984) Current studies of the localization and function of carbonic anhydrase in osteoclasts. Ann NY Acad Sci 429:473–478

    Article  PubMed  CAS  Google Scholar 

  35. Anderson RE, Schraer H, Gay CV (1982) Ultrastructural immunocytochemical localization of carbonic anhydrase in normal and calcitonin-treated chick osteoclasts. Ann Rech Vet 204:9–20

    CAS  Google Scholar 

  36. Gay CV (1980) Recent developments in carbonic anhydrase localization: occurrence of carbonic anhydrase in calcium-mobilizing tissues. In: Bauer C, Gros G, Bartels H (eds) Biophysics and physiology of carbon dioxide. Springer Verlag, Berlin, Heidelberg, New York

    Google Scholar 

  37. Kumpulainen T, Vaeaenaenen HK (1982) Immunohistochemical demonstration of extracellular carbonic anhydrase in epiphyseal growth cartilage. Calcif Tissue Int 34:428–430

    Article  PubMed  CAS  Google Scholar 

  38. Gay CV, Ito MB, Schraer H (1983) Carbonic anhydrase activity in isolated osteoclasts. Metab Bone Dis Rel 5:33–39

    Article  CAS  Google Scholar 

  39. Warshawsky H, Goltzman D, Rouleau MF, Bergerow JJM (1980) Direct in vivo demonstration by autoradiography of specific binding sites for calcitonin in skeletal and renal tissues of the rat. J Cell Biol 85:682–694

    Article  PubMed  CAS  Google Scholar 

  40. Rao LG, Heersche JNM, Marchuk LS, Sturtridge E (1981) Immunohistochemical demonstration of calcitonin binding to specific cell types in fixed rat bone tissue. Endocrinology 108:1972–1979

    Article  PubMed  CAS  Google Scholar 

  41. Sly WS, Hewett-Emmett D, Whyte MP, Yu Y-SL, Tashian RE (1983) 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 USA 80:2752–2756

    Article  PubMed  CAS  Google Scholar 

  42. Sly WS, Whyte MP, Sundaram V, Tashian RE, Hewett-Emmett D, Guibaud P, Vainsel M, Baluarte HJ, Gruskin A, Al-Mosawi M, Sakati N, Ohlsson A (1985) Carbonic anhydrase II deficiency in 12 families with the autosomal recessive syndrome of osteopetrosis with renal tubular acidosis and cerebral calcification. N Engl J Med 313:139–145

    Article  PubMed  CAS  Google Scholar 

  43. Rasmussen H, DeLuca HF, Arnaud C, Hawker C, von Stedingk M (1963) The relationship between vitamin D and parathyroid hormone. J Clin Invest 42:1940–1946

    PubMed  CAS  Google Scholar 

  44. Rasmussen H, DeLuca HF, Arnaud C, Hawker C, v. Stedingk M (1963) The relationship between vitamin D and parathyroid hormone. J Clin Invest 42:1940–1946

    Article  PubMed  CAS  Google Scholar 

  45. Crowell JA, Cooper CW, Toverud SU, Boass A (1981) Influence of vitamin D on parathyroid hormone-induced adenosine 3′, 5′-monophosphate production by bone cells isolated from rat calvaria. Endocrinology 109:1715–1722

    Article  PubMed  CAS  Google Scholar 

  46. Crowell JA Jr, Cooper CW, Toverud SU Boass A (1981) Influence of vitamin D on parathyroid hormone-induced accumulation in bone cells from rat calvaria. Calcif Tissue Int 33:333

    Google Scholar 

  47. Wilbur KM, Anderson NG (1948) Electrometric and colorimetric determination of carbonic anhydrase. J Biol Chem 176:147–154

    CAS  PubMed  Google Scholar 

  48. Brunk CF, Jones KC, James TW (1979) Assay for nanogram quantities of DNA in cellular homogenates. Anal Biochem 92:497–500

    Article  PubMed  CAS  Google Scholar 

  49. Siegmund P, Koerber F, Dietsch P (1976) Praktikum der physiologischen Chemie, De Gruyter, Berlin-New York

    Google Scholar 

  50. Rudack-Garcia D, Henry HL (1981) Effect of vitamin D status on cyclic AMP-dependent protein kinase activity and its heat-stable inhibitor in chick kidney. J Biol Chem 256:10781–10785

    PubMed  CAS  Google Scholar 

  51. Liang CT, Balakir RA, Barnes J, Sacktor B (1984) Responses of chick renal cells to parathyroid hormone: effect of vitamin D. Am J Physiol 246:C401-C406

    PubMed  CAS  Google Scholar 

  52. Henry HL, Al-Abdaly F, Noland TA Jr (1983) Cyclic AMP-dependent protein kinase and its endogenous inhibitor protein—tissue distribution and effect of vitamin D status in the chick. Comp Biochem Physiol 74B:715–718

    CAS  Google Scholar 

  53. Henry HL, Rudack-Garcia D, Al-Abdaly F (1981) Increased levels of an inhibitor of cyclic AMP-dependent protein kinase in kidney from vitamin D-deficient chicks. Calcif Tissue Int 33:335

    Google Scholar 

  54. Drewe J, Dietsch P, Keck E (1985) Influence of vitamin D status on the activity of carbonic anhydrase in the chick kidney. In: Norman AW, Schaefer K, Grigoleit HG, von Herrath D (eds) Vitamin D: a chemical, biochemical and clinical update. Walter de Gruyter Berlin, New York, 451–452

    Google Scholar 

  55. Pochhammer C, Dietsch P, Siegmund P (1979) Histochemical detection of carbonic anhydrase with dimethylaminonaphtalene-5′-sulfonamide. J Histochem Cytochem 27:1103–1107

    PubMed  CAS  Google Scholar 

  56. Wong GL, Kent GN, Ku KY, Cohn DV (1978) The interaction on the hormone-regulated synthesis of hyaluronic acids and citrate decarboxylation in isolated bone cells. Endocrinology 103:2274–2282

    Article  PubMed  CAS  Google Scholar 

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Drewe, J., Dietsch, P. & Keck, E. Effect of vitamin D status on the activity of carbonic anhydrase in chicken epiphysis and kidney. Calcif Tissue Int 43, 26–32 (1988). https://doi.org/10.1007/BF02555164

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  • DOI: https://doi.org/10.1007/BF02555164

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