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Scanning Electrochemical Microscopy at the Surface of Bone‐Resorbing Osteoclasts: Evidence for Steady‐State Disposal and Intracellular Functional Compartmentalization of Calcium
Osteoclast resorptive activity occurs despite the presence of extremely high levels of ionized calcium ([Ca2+]) within the osteoclast hemivacuole, which is generated as a by‐product of its resorptive activity. Previous in vitro observations have shown that increases in extracellular [Ca2+] ([Ca2+]e)...
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Published in: | Journal of bone and mineral research 2001-11, Vol.16 (11), p.2092-2102 |
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description | Osteoclast resorptive activity occurs despite the presence of extremely high levels of ionized calcium ([Ca2+]) within the osteoclast hemivacuole, which is generated as a by‐product of its resorptive activity. Previous in vitro observations have shown that increases in extracellular [Ca2+] ([Ca2+]e) in the surrounding medium can inhibit the osteoclast resorptive activity. Therefore, it has been suggested that the osteoclast acts as a “sensor” for [Ca2+]e, and that high [Ca2+]e leads to an increase in intracellular [Ca2+] ([Ca2+]i), thereby inhibiting osteoclasts in a negative feedback manner. In this report we have carried out an experimental and theoretical analysis of calcium disposal during osteoclast activity to evaluate how in vitro models relate to in vivo osteoclast activity, where it is possible that high [Ca2+]e may be present in the hemivacuole but not over the nonresorbing surface of the cell. Scanning electrochemical microscopy (SECM) studies of [Ca2+] and superoxide anion () generation by bone‐resorbing osteoclasts on the surface of a bovine cortical bone slice were compared with microspectofluorometric measurements of the levels of [Ca2+]i in single osteoclasts and the effect of [Ca2+]i on various aspects of osteoclast function. The generation of by the osteoclasts has been shown to be positively correlated with osteoclast resorptive function and can therefore serve as an index of acute changes in osteoclast activity. The SECM of bone‐resorbing osteoclasts at the surface of a bone slice revealed a continuous steady‐state release of Ca2+. Even after prolonged incubation lasting 3 h the near‐surface [Ca2+]e in the solution above the cell remained |
doi_str_mv | 10.1359/jbmr.2001.16.11.2092 |
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M. ; Rathod, Hersha ; Gillespie, James I. ; Horrocks, Benjamin R. ; Datta, Harish K.</creator><creatorcontrib>Berger, Christine E. M. ; Rathod, Hersha ; Gillespie, James I. ; Horrocks, Benjamin R. ; Datta, Harish K.</creatorcontrib><description>Osteoclast resorptive activity occurs despite the presence of extremely high levels of ionized calcium ([Ca2+]) within the osteoclast hemivacuole, which is generated as a by‐product of its resorptive activity. Previous in vitro observations have shown that increases in extracellular [Ca2+] ([Ca2+]e) in the surrounding medium can inhibit the osteoclast resorptive activity. Therefore, it has been suggested that the osteoclast acts as a “sensor” for [Ca2+]e, and that high [Ca2+]e leads to an increase in intracellular [Ca2+] ([Ca2+]i), thereby inhibiting osteoclasts in a negative feedback manner. In this report we have carried out an experimental and theoretical analysis of calcium disposal during osteoclast activity to evaluate how in vitro models relate to in vivo osteoclast activity, where it is possible that high [Ca2+]e may be present in the hemivacuole but not over the nonresorbing surface of the cell. Scanning electrochemical microscopy (SECM) studies of [Ca2+] and superoxide anion () generation by bone‐resorbing osteoclasts on the surface of a bovine cortical bone slice were compared with microspectofluorometric measurements of the levels of [Ca2+]i in single osteoclasts and the effect of [Ca2+]i on various aspects of osteoclast function. The generation of by the osteoclasts has been shown to be positively correlated with osteoclast resorptive function and can therefore serve as an index of acute changes in osteoclast activity. The SECM of bone‐resorbing osteoclasts at the surface of a bone slice revealed a continuous steady‐state release of Ca2+. Even after prolonged incubation lasting 3 h the near‐surface [Ca2+]e in the solution above the cell remained <2 mM. The SECM real‐time measurement data were consistent with the osteoclast acting as a conduit for continuous Ca2+ disposal from the osteoclast‐bone interface. We conclude that the osteoclast distinguishes [Ca2+]e in the hemivacuole and in the extracellular fluid above the cell which we denote [Ca2+]e′. We found that an increase in [Ca2+]i may be associated with activation; inhibition; or be without effect on generation, bone‐matrix, or bone resorption. Similarly, osteoclast adhesion and bone‐resorbing activity was affected by [Ca2+]e′ but showed no correlation with [Ca2+]i. The data suggest the existence of functional compartmentalization of [Ca2+]i within the osteoclast, where elevated calcium may have an inhibitory, excitatory, or no effect on the overall osteoclast activity while exerting a selective effect on different functional modalities. These observations lead to the conclusion that far from being inhibited by Ca2+ generated, the osteoclast by virtue of the observed functional compartmentalization is highly adapted at carrying out its activity even when the level of [Ca2+] in resorptive lacunae is elevated.</description><identifier>ISSN: 0884-0431</identifier><identifier>EISSN: 1523-4681</identifier><identifier>DOI: 10.1359/jbmr.2001.16.11.2092</identifier><identifier>PMID: 11697806</identifier><identifier>CODEN: JBMREJ</identifier><language>eng</language><publisher>Washington, DC: John Wiley and Sons and The American Society for Bone and Mineral Research (ASBMR)</publisher><subject>Animals ; Biological and medical sciences ; Bone Resorption - metabolism ; Bone Resorption - pathology ; Calcium - metabolism ; Cattle ; Cell Adhesion ; Cell Compartmentation ; cytosolic calcium ; Electrochemistry - methods ; Fundamental and applied biological sciences. Psychology ; In Vitro Techniques ; Microscopy, Electron, Scanning - methods ; osteoclast activity ; Osteoclasts - metabolism ; Osteoclasts - ultrastructure ; Rats ; Rats, Wistar ; scanning electrochemical microscopy ; Skeleton and joints ; superoxide anion ; Superoxides - metabolism ; Vertebrates: osteoarticular system, musculoskeletal system</subject><ispartof>Journal of bone and mineral research, 2001-11, Vol.16 (11), p.2092-2102</ispartof><rights>Copyright © 2001 ASBMR</rights><rights>2002 INIST-CNRS</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5338-3615039c80d87bc3bfdd7e20421086dc9d5179273d16cb2084d422685846d28c3</citedby><cites>FETCH-LOGICAL-c5338-3615039c80d87bc3bfdd7e20421086dc9d5179273d16cb2084d422685846d28c3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=14107482$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/11697806$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Berger, Christine E. M.</creatorcontrib><creatorcontrib>Rathod, Hersha</creatorcontrib><creatorcontrib>Gillespie, James I.</creatorcontrib><creatorcontrib>Horrocks, Benjamin R.</creatorcontrib><creatorcontrib>Datta, Harish K.</creatorcontrib><title>Scanning Electrochemical Microscopy at the Surface of Bone‐Resorbing Osteoclasts: Evidence for Steady‐State Disposal and Intracellular Functional Compartmentalization of Calcium</title><title>Journal of bone and mineral research</title><addtitle>J Bone Miner Res</addtitle><description>Osteoclast resorptive activity occurs despite the presence of extremely high levels of ionized calcium ([Ca2+]) within the osteoclast hemivacuole, which is generated as a by‐product of its resorptive activity. Previous in vitro observations have shown that increases in extracellular [Ca2+] ([Ca2+]e) in the surrounding medium can inhibit the osteoclast resorptive activity. Therefore, it has been suggested that the osteoclast acts as a “sensor” for [Ca2+]e, and that high [Ca2+]e leads to an increase in intracellular [Ca2+] ([Ca2+]i), thereby inhibiting osteoclasts in a negative feedback manner. In this report we have carried out an experimental and theoretical analysis of calcium disposal during osteoclast activity to evaluate how in vitro models relate to in vivo osteoclast activity, where it is possible that high [Ca2+]e may be present in the hemivacuole but not over the nonresorbing surface of the cell. Scanning electrochemical microscopy (SECM) studies of [Ca2+] and superoxide anion () generation by bone‐resorbing osteoclasts on the surface of a bovine cortical bone slice were compared with microspectofluorometric measurements of the levels of [Ca2+]i in single osteoclasts and the effect of [Ca2+]i on various aspects of osteoclast function. The generation of by the osteoclasts has been shown to be positively correlated with osteoclast resorptive function and can therefore serve as an index of acute changes in osteoclast activity. The SECM of bone‐resorbing osteoclasts at the surface of a bone slice revealed a continuous steady‐state release of Ca2+. Even after prolonged incubation lasting 3 h the near‐surface [Ca2+]e in the solution above the cell remained <2 mM. The SECM real‐time measurement data were consistent with the osteoclast acting as a conduit for continuous Ca2+ disposal from the osteoclast‐bone interface. We conclude that the osteoclast distinguishes [Ca2+]e in the hemivacuole and in the extracellular fluid above the cell which we denote [Ca2+]e′. We found that an increase in [Ca2+]i may be associated with activation; inhibition; or be without effect on generation, bone‐matrix, or bone resorption. Similarly, osteoclast adhesion and bone‐resorbing activity was affected by [Ca2+]e′ but showed no correlation with [Ca2+]i. The data suggest the existence of functional compartmentalization of [Ca2+]i within the osteoclast, where elevated calcium may have an inhibitory, excitatory, or no effect on the overall osteoclast activity while exerting a selective effect on different functional modalities. These observations lead to the conclusion that far from being inhibited by Ca2+ generated, the osteoclast by virtue of the observed functional compartmentalization is highly adapted at carrying out its activity even when the level of [Ca2+] in resorptive lacunae is elevated.</description><subject>Animals</subject><subject>Biological and medical sciences</subject><subject>Bone Resorption - metabolism</subject><subject>Bone Resorption - pathology</subject><subject>Calcium - metabolism</subject><subject>Cattle</subject><subject>Cell Adhesion</subject><subject>Cell Compartmentation</subject><subject>cytosolic calcium</subject><subject>Electrochemistry - methods</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>In Vitro Techniques</subject><subject>Microscopy, Electron, Scanning - methods</subject><subject>osteoclast activity</subject><subject>Osteoclasts - metabolism</subject><subject>Osteoclasts - ultrastructure</subject><subject>Rats</subject><subject>Rats, Wistar</subject><subject>scanning electrochemical microscopy</subject><subject>Skeleton and joints</subject><subject>superoxide anion</subject><subject>Superoxides - metabolism</subject><subject>Vertebrates: osteoarticular system, musculoskeletal system</subject><issn>0884-0431</issn><issn>1523-4681</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2001</creationdate><recordtype>article</recordtype><recordid>eNqNkcFuFCEYxydGY7fVNzCGi95m5YMZhvGk3W61pk2Trp4JA4ylmYEtMJr15CP4Mr6QTyKT3aRHPUHg9_99hH9RvAC8BFq3b-66MSwJxrAEtgTI25Y8KhZQE1pWjMPjYoE5r0pcUTgqjmO8wxizmrGnxREAaxuO2aL4vVHSOeu-ovVgVApe3ZrRKjmgK6uCj8pvd0gmlG4N2kyhl8og36NT78yfn79uTPShm9PXMRmvBhlTfIvW36w2LpO9D2iTjNS7DG-STAad2bj1Mful0-jCpZCNwzANMqDzyalkvcuXKz9uZUijcUkO9oecj-e5KzkoO43Piie9HKJ5flhPii_n68-rj-Xl9YeL1fvLUtWU8pIyqDFtFceaN52iXa91YwiuCGDOtGp1DU1LGqqBqY5gXumKEMZrXjFNuKInxeu9dxv8_WRiEqON83ulM36KoiGk5iQL_gUCJ5RRDhms9uD8uTGYXmyDHWXYCcBi7lXMvYq5VwFMAIi51xx7efBP3Wj0Q-hQZAZeHQAZc3t9kE7Z-MBVgJuKz6J3e-67Hczuv4aLT6dXNzWrMTAA4PQv-DfEPA</recordid><startdate>200111</startdate><enddate>200111</enddate><creator>Berger, Christine E. M.</creator><creator>Rathod, Hersha</creator><creator>Gillespie, James I.</creator><creator>Horrocks, Benjamin R.</creator><creator>Datta, Harish K.</creator><general>John Wiley and Sons and The American Society for Bone and Mineral Research (ASBMR)</general><general>American Society for Bone and Mineral Research</general><scope>IQODW</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QP</scope><scope>7X8</scope></search><sort><creationdate>200111</creationdate><title>Scanning Electrochemical Microscopy at the Surface of Bone‐Resorbing Osteoclasts: Evidence for Steady‐State Disposal and Intracellular Functional Compartmentalization of Calcium</title><author>Berger, Christine E. M. ; Rathod, Hersha ; Gillespie, James I. ; Horrocks, Benjamin R. ; Datta, Harish K.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5338-3615039c80d87bc3bfdd7e20421086dc9d5179273d16cb2084d422685846d28c3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2001</creationdate><topic>Animals</topic><topic>Biological and medical sciences</topic><topic>Bone Resorption - metabolism</topic><topic>Bone Resorption - pathology</topic><topic>Calcium - metabolism</topic><topic>Cattle</topic><topic>Cell Adhesion</topic><topic>Cell Compartmentation</topic><topic>cytosolic calcium</topic><topic>Electrochemistry - methods</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>In Vitro Techniques</topic><topic>Microscopy, Electron, Scanning - methods</topic><topic>osteoclast activity</topic><topic>Osteoclasts - metabolism</topic><topic>Osteoclasts - ultrastructure</topic><topic>Rats</topic><topic>Rats, Wistar</topic><topic>scanning electrochemical microscopy</topic><topic>Skeleton and joints</topic><topic>superoxide anion</topic><topic>Superoxides - metabolism</topic><topic>Vertebrates: osteoarticular system, musculoskeletal system</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Berger, Christine E. M.</creatorcontrib><creatorcontrib>Rathod, Hersha</creatorcontrib><creatorcontrib>Gillespie, James I.</creatorcontrib><creatorcontrib>Horrocks, Benjamin R.</creatorcontrib><creatorcontrib>Datta, Harish K.</creatorcontrib><collection>Pascal-Francis</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Journal of bone and mineral research</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Berger, Christine E. M.</au><au>Rathod, Hersha</au><au>Gillespie, James I.</au><au>Horrocks, Benjamin R.</au><au>Datta, Harish K.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Scanning Electrochemical Microscopy at the Surface of Bone‐Resorbing Osteoclasts: Evidence for Steady‐State Disposal and Intracellular Functional Compartmentalization of Calcium</atitle><jtitle>Journal of bone and mineral research</jtitle><addtitle>J Bone Miner Res</addtitle><date>2001-11</date><risdate>2001</risdate><volume>16</volume><issue>11</issue><spage>2092</spage><epage>2102</epage><pages>2092-2102</pages><issn>0884-0431</issn><eissn>1523-4681</eissn><coden>JBMREJ</coden><abstract>Osteoclast resorptive activity occurs despite the presence of extremely high levels of ionized calcium ([Ca2+]) within the osteoclast hemivacuole, which is generated as a by‐product of its resorptive activity. Previous in vitro observations have shown that increases in extracellular [Ca2+] ([Ca2+]e) in the surrounding medium can inhibit the osteoclast resorptive activity. Therefore, it has been suggested that the osteoclast acts as a “sensor” for [Ca2+]e, and that high [Ca2+]e leads to an increase in intracellular [Ca2+] ([Ca2+]i), thereby inhibiting osteoclasts in a negative feedback manner. In this report we have carried out an experimental and theoretical analysis of calcium disposal during osteoclast activity to evaluate how in vitro models relate to in vivo osteoclast activity, where it is possible that high [Ca2+]e may be present in the hemivacuole but not over the nonresorbing surface of the cell. Scanning electrochemical microscopy (SECM) studies of [Ca2+] and superoxide anion () generation by bone‐resorbing osteoclasts on the surface of a bovine cortical bone slice were compared with microspectofluorometric measurements of the levels of [Ca2+]i in single osteoclasts and the effect of [Ca2+]i on various aspects of osteoclast function. The generation of by the osteoclasts has been shown to be positively correlated with osteoclast resorptive function and can therefore serve as an index of acute changes in osteoclast activity. The SECM of bone‐resorbing osteoclasts at the surface of a bone slice revealed a continuous steady‐state release of Ca2+. Even after prolonged incubation lasting 3 h the near‐surface [Ca2+]e in the solution above the cell remained <2 mM. The SECM real‐time measurement data were consistent with the osteoclast acting as a conduit for continuous Ca2+ disposal from the osteoclast‐bone interface. We conclude that the osteoclast distinguishes [Ca2+]e in the hemivacuole and in the extracellular fluid above the cell which we denote [Ca2+]e′. We found that an increase in [Ca2+]i may be associated with activation; inhibition; or be without effect on generation, bone‐matrix, or bone resorption. Similarly, osteoclast adhesion and bone‐resorbing activity was affected by [Ca2+]e′ but showed no correlation with [Ca2+]i. The data suggest the existence of functional compartmentalization of [Ca2+]i within the osteoclast, where elevated calcium may have an inhibitory, excitatory, or no effect on the overall osteoclast activity while exerting a selective effect on different functional modalities. These observations lead to the conclusion that far from being inhibited by Ca2+ generated, the osteoclast by virtue of the observed functional compartmentalization is highly adapted at carrying out its activity even when the level of [Ca2+] in resorptive lacunae is elevated.</abstract><cop>Washington, DC</cop><pub>John Wiley and Sons and The American Society for Bone and Mineral Research (ASBMR)</pub><pmid>11697806</pmid><doi>10.1359/jbmr.2001.16.11.2092</doi><tpages>11</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Animals Biological and medical sciences Bone Resorption - metabolism Bone Resorption - pathology Calcium - metabolism Cattle Cell Adhesion Cell Compartmentation cytosolic calcium Electrochemistry - methods Fundamental and applied biological sciences. Psychology In Vitro Techniques Microscopy, Electron, Scanning - methods osteoclast activity Osteoclasts - metabolism Osteoclasts - ultrastructure Rats Rats, Wistar scanning electrochemical microscopy Skeleton and joints superoxide anion Superoxides - metabolism Vertebrates: osteoarticular system, musculoskeletal system |
title | Scanning Electrochemical Microscopy at the Surface of Bone‐Resorbing Osteoclasts: Evidence for Steady‐State Disposal and Intracellular Functional Compartmentalization of Calcium |
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