DOI: 10.1002/jbmr.5650071111. Regulation of cytoplasmic calcium concentration in tetracycline-treated osteoclasts

Regulation of cytoplasmic calcium concentration in tetracycline-treated osteoclasts

10.1002/jbmr.5650071111

Crossref journal-article

Oxford University Press (OUP)

Journal of Bone and Mineral Research (286)

Abstract

Abstract The ability of low-dose tetracyclines to inhibit collagenase activity and inactivate osteoclasts suggests that these compounds have great potential as a prophylaxis for metabolic bone disease. However, the cellular mechanism by which tetracyclines interact with skeletal tissue is not yet clear. To better understand the effects of tetracyclines on bone metabolism, we examined their effect on osteoclast activity in vitro. Because tetracyclines can enter the cell and bind calcium and have been reported to directly interact with osteoclasts, we postulated that exposure to either of two tetracyclines, minocycline or doxycycline, would alter cytosolic Ca2+ regulation in rat osteoclasts. [Ca2+]i was measured in single rat osteoclasts utilizing fura-2. Addition of extracellular Ca2+ (5 mM CaCl2), a potent osteoclast inhibitor, increased [Ca2+]i in all osteoclasts, but 10−6 M salmon calcitonin (sCT) did so only in a subpopulation of osteoclasts. Neither minocycline nor doxycycline (10 μg/ml) altered steady-state osteoclast [Ca2+]i. Further, neither minocycline nor doxycycline pretreatment affected the sCT-mediated increases in [Ca2+]i. However, tetracycline pretreatment significantly decreased the cytosolic Ca2+ response to extracellular CaCl2. Our results strongly suggest that tetracyclines have a specific effect on extracellular Ca2+-stimulated cytosolic Ca2+ mobilization in osteoclasts, which is not solely dependent on their ability to buffer Ca2+. Furthermore, these results point to the potential use of tetracyclines as probes to study cytosolic Ca2+ regulation. However, that tetracyclines attenuate a signal response associated with decreased osteoclastic resorption suggests that the reported antiresorptive attributes of tetracyclines must be achieved independently of an effect on osteoclastic cytosolic Ca2+.

Bibliography

Donahue, H. J., Iijima, K., Goligorsky, M. S., Rubin, C. T., & Rifkin, B. R. (1992). Regulation of cytoplasmic calcium concentration in tetracycline-treated osteoclasts. Journal of Bone and Mineral Research, 7(11), 1313â1318.

Authors 5

Henry J. Donahue (first)
Kazumoto Iijima (additional)
Michael S. Goligorsky (additional)
Clinton T. Rubin (additional)
Barry R. Rifkin (additional)

References 30 Referenced 26

{'issue': '1', 'key': '2024013112171225600_bib1', 'first-page': '27', 'article-title': 'Tetracycline administration prevents diabetes-induced osteopenia in the rat: Initial observations', 'volume': '68', 'author': 'Golub', 'year': '1990', 'journal-title': 'Res Commun Chem Pathol Pharmacol'} / Res Commun Chem Pathol Pharmacol / Tetracycline administration prevents diabetes-induced osteopenia in the rat: Initial observations by Golub (1990)
10.1002/jor.1100060512 / J Orthop Res / Inhibition of epiphyseal cartilage collagenase by tetracyclines in low phosphate rickets in rats by Greenwald (1988)
{'issue': '3', 'key': '2024013112171225600_bib3', 'first-page': '323', 'article-title': 'The effect of tetracyclines on collagenase activity in UMR 106–01 rat osteoblastic osteosarcoma cells', 'volume': '70', 'author': 'Ramamurthy', 'year': '1990', 'journal-title': 'Res Commun Chem Pathol Pharmacol'} / Res Commun Chem Pathol Pharmacol / The effect of tetracyclines on collagenase activity in UMR 106–01 rat osteoblastic osteosarcoma cells by Ramamurthy (1990)
10.1007/BF01946671 / Experientia / Tetracyclines inhibit parathyroid hormone-induced bone resorption in organ culture by Gomes (1984)
{'key': '2024013112171225600_bib5', 'first-page': '85', 'volume-title': 'The Biological Mechanisms of Tooth Movement and Craniofacial Adaptation', 'author': 'Rifkin', 'year': '1992'} / The Biological Mechanisms of Tooth Movement and Craniofacial Adaptation by Rifkin (1992)
10.1016/S0021-9258(18)68273-0 / J Biol Chem / Differential effects of parathyroid hormone and its analogues on cytosolic calcium ion and cAMP levels in cultured rat osteoblast-like cells by Donahue (1988)
{'key': '2024013112171225600_bib7', 'first-page': 'E45', 'article-title': 'Parathyroid hormone acutely elevates intracellular calcium in osteoblast-like cells', 'volume': '253', 'author': 'Reid', 'year': '1987', 'journal-title': 'Am J Physiol'} / Am J Physiol / Parathyroid hormone acutely elevates intracellular calcium in osteoblast-like cells by Reid (1987)
10.1016/0006-291X(87)91058-8 / Biochem Biophys Res Commun / 1,25-(OH)2D3 increases cytosolic Ca2+ concentration of osteoblastic cell clone MC3T3–E1 by Oshima (1987)
{'key': '2024013112171225600_bib9', 'first-page': 'F755', 'article-title': 'Modulation of osteoblast function by prostaglandins', 'volume': '257', 'author': 'Yamaguchi', 'year': '1989', 'journal-title': 'Am J Physiol'} / Am J Physiol / Modulation of osteoblast function by prostaglandins by Yamaguchi (1989)
10.1016/S0021-9258(18)71683-9 / J Biol Chem / Control of cytosolic free calcium in rat and chicken osteoclasts by Malgaroli (1989)
10.1016/0006-291X(89)91143-1 / Biochem Biophys Res Commun / Calcium-activated intracellular calcium elevation: A novel mechanism of osteoclast regulation by Zaidi (1989)
10.1172/JCI114235 / J Clin Invest / Extracellular proton acidify osteoclasts, reduce cytosolic calcium, and promote expression of cell-matrix attachment structures by Teti (1989)
10.1210/endo-120-2-602 / Endocrinology / A comparative study of disaggregated chick and rat osteoclasts in vitro: Effect of calcitonin and prostaglandin by Arnett (1987)
10.1016/S0091-679X(08)60770-0 / Methods Cell Biol / Dermal fibroblasts by Ham (1980)
10.1016/S0021-9258(19)83641-4 / J Biol Chem / A new generation of Ca2+ indicators with greatly improved fluorescence properties by Grynkiewicz (1985)
10.1016/0143-4160(85)90041-7 / Cell Calcium / Measurement of cytosolic free Ca2+ in individual cells using fluorescence microscopy with dual excitation wavelengths by Tsien (1985)
10.1038/318558a0 / Nature / Calcium gradients in single smooth muscle cells revealed by the digital imaging microscope using fura-2 by Williams (1985)
10.1677/joe.0.1260473 / J Endocrinol / Evidence that the action of calcitonin on rat osteoclasts is mediated by two G proteins acting via separate post-receptor pathways by Zaidi (1990)
10.1126/science.1847755 / Science / Cell cycle-dependent coupling of the calcitonin receptor to different G proteins by Chakraborty (1991)
10.1016/0006-291X(91)91345-D / Biochem Biophys Res Commun / Selective antagonism of calcitonin-induced osteoclastic quiescence (Q effect) by human calcitonin gene-related peptide-(Val8Phe37) by Alam (1991)
10.1126/science.1658940 / Science / Expression cloning of an adenylate cyclase-coupled calcitonin receptor by Lin (1991)
10.1152/physrev.1991.71.2.371 / Physiol Rev / Extracellular Ca2+ sensing, regulation of parathyroid cell function, and role of Ca2+ and other ions as extracellular (first) messengers by Brown (1991)
10.1146/annurev.bb.20.060191.001101 / Annu Rev Biophys Chem / Calcium spiking by Meyer (1991)
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10.1016/0006-291X(89)92405-4 / Biochem Biophys Res Commun / Inhibition of osteoclastic acid phosphatase abolishes bone resorption by Zaidi (1989)
10.1083/jcb.111.6.2543 / J Cell Biol / Osteoclast cytosolic calcium, regulated by voltage-gated calcium channels and extracellular calcium, controls podosome assembly and bone resorption by Miyauchi (1990)
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Dates

Type	When
Created	15 years, 7 months ago (Feb. 3, 2010, 11:54 a.m.)
Deposited	1 year, 5 months ago (March 13, 2024, 10:55 a.m.)
Indexed	4 months, 4 weeks ago (April 8, 2025, 12:44 p.m.)
Issued	32 years, 10 months ago (Nov. 1, 1992)
Published	32 years, 10 months ago (Nov. 1, 1992)
Published Online	32 years, 10 months ago (Nov. 1, 1992)
Published Print	32 years, 10 months ago (Nov. 1, 1992)

Funders 2

NIH
Awards3
1. DK41573 (MSG)
2. AG10199 (HJD)
3. DE09576 (BRR)
American Federation of Aging Research 10.13039/100000965 American Federation for Aging Research
Region: Americas
gov (Trusts, charities, foundations (both public and private))
Labels2
1. American Federation for Aging Research, Inc.
2. AFAR

BibTeX

@article{Donahue_1992, title={Regulation of cytoplasmic calcium concentration in tetracycline-treated osteoclasts}, volume={7}, ISSN={1523-4681}, url={http://dx.doi.org/10.1002/jbmr.5650071111}, DOI={10.1002/jbmr.5650071111}, number={11}, journal={Journal of Bone and Mineral Research}, publisher={Oxford University Press (OUP)}, author={Donahue, Henry J. and Iijima, Kazumoto and Goligorsky, Michael S. and Rubin, Clinton T. and Rifkin, Barry R.}, year={1992}, month=nov, pages={1313–1318} }

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  "abstract": "<jats:title>Abstract</jats:title>\n               <jats:p>The ability of low-dose tetracyclines to inhibit collagenase activity and inactivate osteoclasts suggests that these compounds have great potential as a prophylaxis for metabolic bone disease. However, the cellular mechanism by which tetracyclines interact with skeletal tissue is not yet clear. To better understand the effects of tetracyclines on bone metabolism, we examined their effect on osteoclast activity in vitro. Because tetracyclines can enter the cell and bind calcium and have been reported to directly interact with osteoclasts, we postulated that exposure to either of two tetracyclines, minocycline or doxycycline, would alter cytosolic Ca2+ regulation in rat osteoclasts. [Ca2+]i was measured in single rat osteoclasts utilizing fura-2. Addition of extracellular Ca2+ (5 mM CaCl2), a potent osteoclast inhibitor, increased [Ca2+]i in all osteoclasts, but 10\u22126 M salmon calcitonin (sCT) did so only in a subpopulation of osteoclasts. Neither minocycline nor doxycycline (10 \u03bcg/ml) altered steady-state osteoclast [Ca2+]i. Further, neither minocycline nor doxycycline pretreatment affected the sCT-mediated increases in [Ca2+]i. However, tetracycline pretreatment significantly decreased the cytosolic Ca2+ response to extracellular CaCl2. Our results strongly suggest that tetracyclines have a specific effect on extracellular Ca2+-stimulated cytosolic Ca2+ mobilization in osteoclasts, which is not solely dependent on their ability to buffer Ca2+. Furthermore, these results point to the potential use of tetracyclines as probes to study cytosolic Ca2+ regulation. However, that tetracyclines attenuate a signal response associated with decreased osteoclastic resorption suggests that the reported antiresorptive attributes of tetracyclines must be achieved independently of an effect on osteoclastic cytosolic Ca2+.</jats:p>",
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