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Pulsating fluid flow affects pre‐osteoblast behavior and osteogenic differentiation through production of soluble factors
Bone mass increases after error‐loading, even in the absence of osteocytes. Loaded osteoblasts may produce a combination of growth factors affecting adjacent osteoblast differentiation. We hypothesized that osteoblasts respond to a single load in the short‐term (minutes) by changing F‐actin stress f...
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Published in: | Physiological reports 2021-06, Vol.9 (12), p.e14917-n/a |
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creator | Jin, Jianfeng Seddiqi, Hadi Bakker, Astrid D. Wu, Gang Verstappen, Johanna F. M. Haroon, Mohammad Korfage, Joannes A. M. Zandieh‐Doulabi, Behrouz Werner, Arie Klein‐Nulend, Jenneke Jaspers, Richard T. |
description | Bone mass increases after error‐loading, even in the absence of osteocytes. Loaded osteoblasts may produce a combination of growth factors affecting adjacent osteoblast differentiation. We hypothesized that osteoblasts respond to a single load in the short‐term (minutes) by changing F‐actin stress fiber distribution, in the intermediate‐term (hours) by signaling molecule production, and in the long‐term (days) by differentiation. Furthermore, growth factors produced during and after mechanical loading by pulsating fluid flow (PFF) will affect osteogenic differentiation. MC3T3‐E1 pre‐osteoblasts were either/not stimulated by 60 min PFF (amplitude, 1.0 Pa; frequency, 1 Hz; peak shear stress rate, 6.5 Pa/s) followed by 0–6 h, or 21/28 days of post‐incubation without PFF. Computational analysis revealed that PFF immediately changed distribution and magnitude of fluid dynamics over an adherent pre‐osteoblast inside a parallel‐plate flow chamber (immediate impact). Within 60 min, PFF increased nitric oxide production (5.3‐fold), altered actin distribution, but did not affect cell pseudopodia length and cell orientation (initial downstream impact). PFF transiently stimulated Fgf2, Runx2, Ocn, Dmp1, and Col1⍺1 gene expression between 0 and 6 h after PFF cessation. PFF did not affect alkaline phosphatase nor collagen production after 21 days, but altered mineralization after 28 days. In conclusion, a single bout of PFF with indirect associated release of biochemical factors, stimulates osteoblast differentiation in the long‐term, which may explain enhanced bone formation resulting from mechanical stimuli.
Pulsating fluid flow has distinct temporal impact on pre‐osteoblast behavior and osteogenic differentiation. Initially, PFF increased nitric oxide production, followed in the short‐term by F‐actin stress fiber changes. In the long‐term, PFF did not enhance collagen production, but increased mineralization. This indicates that a single bout of mechanical loading, triggering release of soluble factors, stimulates mineralization in the long‐term. |
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Pulsating fluid flow has distinct temporal impact on pre‐osteoblast behavior and osteogenic differentiation. Initially, PFF increased nitric oxide production, followed in the short‐term by F‐actin stress fiber changes. In the long‐term, PFF did not enhance collagen production, but increased mineralization. This indicates that a single bout of mechanical loading, triggering release of soluble factors, stimulates mineralization in the long‐term.</description><identifier>EISSN: 2051-817X</identifier><identifier>DOI: 10.14814/phy2.14917</identifier><identifier>PMID: 34174021</identifier><language>eng</language><publisher>United States: John Wiley & Sons, Inc</publisher><subject>Actin ; Actins - metabolism ; Actins - physiology ; Alkaline phosphatase ; Alkaline Phosphatase - metabolism ; Animals ; Bone growth ; Bone mass ; Boundary conditions ; Cbfa-1 protein ; Cell Differentiation - physiology ; Cell Line ; Collagen ; Collagen - metabolism ; Computer applications ; Cytoskeleton ; Fibroblast growth factor 2 ; Fibroblasts ; Finite Element Analysis ; finite element modeling ; Fluid dynamics ; Fluid flow ; F‐actin stress fiber ; Gene Expression ; Growth factors ; Mechanical loading ; Mechanical stimuli ; Metabolism ; Mice ; Mineralization ; Morphology ; Nitric oxide ; Nitric Oxide - metabolism ; Original ; Osteoblastogenesis ; Osteoblasts ; Osteoblasts - metabolism ; Osteoblasts - physiology ; Osteocytes ; Osteogenesis ; Osteogenesis - physiology ; osteogenic differentiation ; Physiology ; pre‐osteoblast ; Pseudopodia ; Pulsatile Flow - physiology ; Shear stress</subject><ispartof>Physiological reports, 2021-06, Vol.9 (12), p.e14917-n/a</ispartof><rights>2021 The Authors. published by Wiley Periodicals LLC on behalf of The Physiological Society and the American Physiological Society</rights><rights>2021 The Authors. Physiological Reports published by Wiley Periodicals LLC on behalf of The Physiological Society and the American Physiological Society.</rights><rights>2021. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4527-e4783ffa39ee219e27f2e08306242e62853c4011b9cc5183475b516a2dd0c72f3</citedby><cites>FETCH-LOGICAL-c4527-e4783ffa39ee219e27f2e08306242e62853c4011b9cc5183475b516a2dd0c72f3</cites><orcidid>0000-0001-7661-199X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/2545864705/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/2545864705?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,315,733,786,790,891,11589,25783,27957,27958,37047,37048,44625,46087,46511,53827,53829,75483</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34174021$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Jin, Jianfeng</creatorcontrib><creatorcontrib>Seddiqi, Hadi</creatorcontrib><creatorcontrib>Bakker, Astrid D.</creatorcontrib><creatorcontrib>Wu, Gang</creatorcontrib><creatorcontrib>Verstappen, Johanna F. M.</creatorcontrib><creatorcontrib>Haroon, Mohammad</creatorcontrib><creatorcontrib>Korfage, Joannes A. M.</creatorcontrib><creatorcontrib>Zandieh‐Doulabi, Behrouz</creatorcontrib><creatorcontrib>Werner, Arie</creatorcontrib><creatorcontrib>Klein‐Nulend, Jenneke</creatorcontrib><creatorcontrib>Jaspers, Richard T.</creatorcontrib><title>Pulsating fluid flow affects pre‐osteoblast behavior and osteogenic differentiation through production of soluble factors</title><title>Physiological reports</title><addtitle>Physiol Rep</addtitle><description>Bone mass increases after error‐loading, even in the absence of osteocytes. Loaded osteoblasts may produce a combination of growth factors affecting adjacent osteoblast differentiation. We hypothesized that osteoblasts respond to a single load in the short‐term (minutes) by changing F‐actin stress fiber distribution, in the intermediate‐term (hours) by signaling molecule production, and in the long‐term (days) by differentiation. Furthermore, growth factors produced during and after mechanical loading by pulsating fluid flow (PFF) will affect osteogenic differentiation. MC3T3‐E1 pre‐osteoblasts were either/not stimulated by 60 min PFF (amplitude, 1.0 Pa; frequency, 1 Hz; peak shear stress rate, 6.5 Pa/s) followed by 0–6 h, or 21/28 days of post‐incubation without PFF. Computational analysis revealed that PFF immediately changed distribution and magnitude of fluid dynamics over an adherent pre‐osteoblast inside a parallel‐plate flow chamber (immediate impact). Within 60 min, PFF increased nitric oxide production (5.3‐fold), altered actin distribution, but did not affect cell pseudopodia length and cell orientation (initial downstream impact). PFF transiently stimulated Fgf2, Runx2, Ocn, Dmp1, and Col1⍺1 gene expression between 0 and 6 h after PFF cessation. PFF did not affect alkaline phosphatase nor collagen production after 21 days, but altered mineralization after 28 days. In conclusion, a single bout of PFF with indirect associated release of biochemical factors, stimulates osteoblast differentiation in the long‐term, which may explain enhanced bone formation resulting from mechanical stimuli.
Pulsating fluid flow has distinct temporal impact on pre‐osteoblast behavior and osteogenic differentiation. Initially, PFF increased nitric oxide production, followed in the short‐term by F‐actin stress fiber changes. In the long‐term, PFF did not enhance collagen production, but increased mineralization. This indicates that a single bout of mechanical loading, triggering release of soluble factors, stimulates mineralization in the long‐term.</description><subject>Actin</subject><subject>Actins - metabolism</subject><subject>Actins - physiology</subject><subject>Alkaline phosphatase</subject><subject>Alkaline Phosphatase - metabolism</subject><subject>Animals</subject><subject>Bone growth</subject><subject>Bone mass</subject><subject>Boundary conditions</subject><subject>Cbfa-1 protein</subject><subject>Cell Differentiation - physiology</subject><subject>Cell Line</subject><subject>Collagen</subject><subject>Collagen - metabolism</subject><subject>Computer applications</subject><subject>Cytoskeleton</subject><subject>Fibroblast growth factor 2</subject><subject>Fibroblasts</subject><subject>Finite Element Analysis</subject><subject>finite element modeling</subject><subject>Fluid dynamics</subject><subject>Fluid flow</subject><subject>F‐actin stress fiber</subject><subject>Gene Expression</subject><subject>Growth factors</subject><subject>Mechanical loading</subject><subject>Mechanical stimuli</subject><subject>Metabolism</subject><subject>Mice</subject><subject>Mineralization</subject><subject>Morphology</subject><subject>Nitric oxide</subject><subject>Nitric Oxide - metabolism</subject><subject>Original</subject><subject>Osteoblastogenesis</subject><subject>Osteoblasts</subject><subject>Osteoblasts - metabolism</subject><subject>Osteoblasts - physiology</subject><subject>Osteocytes</subject><subject>Osteogenesis</subject><subject>Osteogenesis - physiology</subject><subject>osteogenic differentiation</subject><subject>Physiology</subject><subject>pre‐osteoblast</subject><subject>Pseudopodia</subject><subject>Pulsatile Flow - physiology</subject><subject>Shear stress</subject><issn>2051-817X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>WIN</sourceid><sourceid>PIMPY</sourceid><recordid>eNp9kc1qFTEYhgdBbKlduZeAG0GO5neS2QhSqi0U7EJBVyGT-XImJWdyTCYtBzdegtfolTSdU4u6cJOEL08e3vA2zTOCXxOuCH-zHXe0HjsiHzWHFAuyUkR-OWiOc77CGBPMWIf5k-aAcSI5puSw-X5ZQjazn9bIheKHusYbZJwDO2e0TfDrx8-YZ4h9MHlGPYzm2seEzDSgZb6GyVs0-PoiwTT76ooTmscUy3qsgjgUu4yiQzmG0gdAztg5pvy0eexMyHB8vx81n9-ffjo5W118_HB-8u5iZbmgcgVcKuacYR0AJR1Q6ShgxXBLOYWWKsEsx4T0nbWCKMal6AVpDR0GbCV17Kh5u_duS7-BwdaYyQS9TX5j0k5H4_XfN5Mf9Tpea0UZ51JWwct7QYrfCuRZb3y2EIKZIJasqeCixaqVoqIv_kGvYklT_d5CqZZLfEe92lM2xZwTuIcwBOulS33XpV66rPTzP_M_sL9brADdAzc-wO5_Ln159pXurbfRHa9n</recordid><startdate>202106</startdate><enddate>202106</enddate><creator>Jin, Jianfeng</creator><creator>Seddiqi, Hadi</creator><creator>Bakker, Astrid D.</creator><creator>Wu, Gang</creator><creator>Verstappen, Johanna F. 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M. ; Haroon, Mohammad ; Korfage, Joannes A. M. ; Zandieh‐Doulabi, Behrouz ; Werner, Arie ; Klein‐Nulend, Jenneke ; Jaspers, Richard T.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4527-e4783ffa39ee219e27f2e08306242e62853c4011b9cc5183475b516a2dd0c72f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Actin</topic><topic>Actins - metabolism</topic><topic>Actins - physiology</topic><topic>Alkaline phosphatase</topic><topic>Alkaline Phosphatase - metabolism</topic><topic>Animals</topic><topic>Bone growth</topic><topic>Bone mass</topic><topic>Boundary conditions</topic><topic>Cbfa-1 protein</topic><topic>Cell Differentiation - physiology</topic><topic>Cell Line</topic><topic>Collagen</topic><topic>Collagen - metabolism</topic><topic>Computer applications</topic><topic>Cytoskeleton</topic><topic>Fibroblast growth factor 2</topic><topic>Fibroblasts</topic><topic>Finite Element Analysis</topic><topic>finite element modeling</topic><topic>Fluid dynamics</topic><topic>Fluid flow</topic><topic>F‐actin stress fiber</topic><topic>Gene Expression</topic><topic>Growth factors</topic><topic>Mechanical loading</topic><topic>Mechanical stimuli</topic><topic>Metabolism</topic><topic>Mice</topic><topic>Mineralization</topic><topic>Morphology</topic><topic>Nitric oxide</topic><topic>Nitric Oxide - metabolism</topic><topic>Original</topic><topic>Osteoblastogenesis</topic><topic>Osteoblasts</topic><topic>Osteoblasts - metabolism</topic><topic>Osteoblasts - physiology</topic><topic>Osteocytes</topic><topic>Osteogenesis</topic><topic>Osteogenesis - physiology</topic><topic>osteogenic differentiation</topic><topic>Physiology</topic><topic>pre‐osteoblast</topic><topic>Pseudopodia</topic><topic>Pulsatile Flow - physiology</topic><topic>Shear stress</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Jin, Jianfeng</creatorcontrib><creatorcontrib>Seddiqi, Hadi</creatorcontrib><creatorcontrib>Bakker, Astrid D.</creatorcontrib><creatorcontrib>Wu, Gang</creatorcontrib><creatorcontrib>Verstappen, Johanna F. 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M.</au><au>Haroon, Mohammad</au><au>Korfage, Joannes A. M.</au><au>Zandieh‐Doulabi, Behrouz</au><au>Werner, Arie</au><au>Klein‐Nulend, Jenneke</au><au>Jaspers, Richard T.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Pulsating fluid flow affects pre‐osteoblast behavior and osteogenic differentiation through production of soluble factors</atitle><jtitle>Physiological reports</jtitle><addtitle>Physiol Rep</addtitle><date>2021-06</date><risdate>2021</risdate><volume>9</volume><issue>12</issue><spage>e14917</spage><epage>n/a</epage><pages>e14917-n/a</pages><eissn>2051-817X</eissn><notes>Funding information</notes><notes>This work was granted by the China Scholarship Council [CSC, No. 201608530156]. This work was also granted by Health‐Holland (Project No. LSHM19016, “BB”).</notes><notes>Jenneke Klein‐Nulend and Richard T. Jaspers shared last authorship.</notes><notes>ObjectType-Article-1</notes><notes>SourceType-Scholarly Journals-1</notes><notes>ObjectType-Feature-2</notes><notes>content type line 23</notes><abstract>Bone mass increases after error‐loading, even in the absence of osteocytes. Loaded osteoblasts may produce a combination of growth factors affecting adjacent osteoblast differentiation. We hypothesized that osteoblasts respond to a single load in the short‐term (minutes) by changing F‐actin stress fiber distribution, in the intermediate‐term (hours) by signaling molecule production, and in the long‐term (days) by differentiation. Furthermore, growth factors produced during and after mechanical loading by pulsating fluid flow (PFF) will affect osteogenic differentiation. MC3T3‐E1 pre‐osteoblasts were either/not stimulated by 60 min PFF (amplitude, 1.0 Pa; frequency, 1 Hz; peak shear stress rate, 6.5 Pa/s) followed by 0–6 h, or 21/28 days of post‐incubation without PFF. Computational analysis revealed that PFF immediately changed distribution and magnitude of fluid dynamics over an adherent pre‐osteoblast inside a parallel‐plate flow chamber (immediate impact). Within 60 min, PFF increased nitric oxide production (5.3‐fold), altered actin distribution, but did not affect cell pseudopodia length and cell orientation (initial downstream impact). PFF transiently stimulated Fgf2, Runx2, Ocn, Dmp1, and Col1⍺1 gene expression between 0 and 6 h after PFF cessation. PFF did not affect alkaline phosphatase nor collagen production after 21 days, but altered mineralization after 28 days. In conclusion, a single bout of PFF with indirect associated release of biochemical factors, stimulates osteoblast differentiation in the long‐term, which may explain enhanced bone formation resulting from mechanical stimuli.
Pulsating fluid flow has distinct temporal impact on pre‐osteoblast behavior and osteogenic differentiation. Initially, PFF increased nitric oxide production, followed in the short‐term by F‐actin stress fiber changes. In the long‐term, PFF did not enhance collagen production, but increased mineralization. This indicates that a single bout of mechanical loading, triggering release of soluble factors, stimulates mineralization in the long‐term.</abstract><cop>United States</cop><pub>John Wiley & Sons, Inc</pub><pmid>34174021</pmid><doi>10.14814/phy2.14917</doi><tpages>18</tpages><orcidid>https://orcid.org/0000-0001-7661-199X</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Actin Actins - metabolism Actins - physiology Alkaline phosphatase Alkaline Phosphatase - metabolism Animals Bone growth Bone mass Boundary conditions Cbfa-1 protein Cell Differentiation - physiology Cell Line Collagen Collagen - metabolism Computer applications Cytoskeleton Fibroblast growth factor 2 Fibroblasts Finite Element Analysis finite element modeling Fluid dynamics Fluid flow F‐actin stress fiber Gene Expression Growth factors Mechanical loading Mechanical stimuli Metabolism Mice Mineralization Morphology Nitric oxide Nitric Oxide - metabolism Original Osteoblastogenesis Osteoblasts Osteoblasts - metabolism Osteoblasts - physiology Osteocytes Osteogenesis Osteogenesis - physiology osteogenic differentiation Physiology pre‐osteoblast Pseudopodia Pulsatile Flow - physiology Shear stress |
title | Pulsating fluid flow affects pre‐osteoblast behavior and osteogenic differentiation through production of soluble factors |
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