In vivo xenogeneic scaffold fate is determined by residual antigenicity and extracellular matrix preservation
Abstract The immunological potential of animal-derived tissues and organs is the critical hurdle to increasing their clinical implementation. Glutaraldehyde-fixation cross-links proteins in xenogeneic tissues (e.g., bovine pericardium) to delay immune rejection, but also compromises the regenerative...
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| Veröffentlicht in: | Biomaterials 2016-06, Vol.92, p.1-12 |
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| creator | Wong, Maelene L Wong, Janelle L Vapniarsky, Natalia Griffiths, Leigh G |
| description | Abstract The immunological potential of animal-derived tissues and organs is the critical hurdle to increasing their clinical implementation. Glutaraldehyde-fixation cross-links proteins in xenogeneic tissues (e.g., bovine pericardium) to delay immune rejection, but also compromises the regenerative potential of the resultant biomaterial. Unfixed xenogeneic biomaterials in which xenoantigenicity has been ameliorated and native extracellular matrix (ECM) architecture has been maintained have the potential to overcome limitations of current clinically utilized glutaraldehyde-fixed biomaterials. The objective of this work was to determine how residual antigenicity and ECM architecture preservation modulate recipient immune and regenerative responses towards unfixed bovine pericardium (BP) ECM scaffolds. Disruption of ECM architecture during scaffold generation, with either SDS-decellularization or glutaraldehyde-fixation, stimulated recipient foreign body response and resultant fibrotic encapsulation following leporine subpannicular implantation. Conversely, BP scaffolds subjected to stepwise removal of hydrophilic and lipophilic antigens using amidosulfobetaine-14 (ASB-14) maintained native ECM architecture and thereby avoided fibrotic encapsulation. Removal of hydrophilic and lipophilic antigens significantly decreased local and systemic graft-specific, adaptive immune responses and subsequent calcification of BP scaffolds compared to scaffolds undergoing hydrophile removal only. Critically, removal of antigenic components and preservation of ECM architecture with ASB-14 promoted full-thickness recipient non-immune cellular repopulation of the BP scaffold. Further, unlike clinically utilized fixed BP, ASB-14-treated scaffolds fostered rapid intimal and medial vessel wall regeneration in a porcine carotid patch angioplasty model. This work highlights the importance of residual antigenicity and ECM architecture preservation in modulating recipient immune and regenerative responses towards xenogeneic biomaterial generation. |
| doi_str_mv | 10.1016/j.biomaterials.2016.03.024 |
| format | Article |
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Glutaraldehyde-fixation cross-links proteins in xenogeneic tissues (e.g., bovine pericardium) to delay immune rejection, but also compromises the regenerative potential of the resultant biomaterial. Unfixed xenogeneic biomaterials in which xenoantigenicity has been ameliorated and native extracellular matrix (ECM) architecture has been maintained have the potential to overcome limitations of current clinically utilized glutaraldehyde-fixed biomaterials. The objective of this work was to determine how residual antigenicity and ECM architecture preservation modulate recipient immune and regenerative responses towards unfixed bovine pericardium (BP) ECM scaffolds. Disruption of ECM architecture during scaffold generation, with either SDS-decellularization or glutaraldehyde-fixation, stimulated recipient foreign body response and resultant fibrotic encapsulation following leporine subpannicular implantation. Conversely, BP scaffolds subjected to stepwise removal of hydrophilic and lipophilic antigens using amidosulfobetaine-14 (ASB-14) maintained native ECM architecture and thereby avoided fibrotic encapsulation. Removal of hydrophilic and lipophilic antigens significantly decreased local and systemic graft-specific, adaptive immune responses and subsequent calcification of BP scaffolds compared to scaffolds undergoing hydrophile removal only. Critically, removal of antigenic components and preservation of ECM architecture with ASB-14 promoted full-thickness recipient non-immune cellular repopulation of the BP scaffold. Further, unlike clinically utilized fixed BP, ASB-14-treated scaffolds fostered rapid intimal and medial vessel wall regeneration in a porcine carotid patch angioplasty model. This work highlights the importance of residual antigenicity and ECM architecture preservation in modulating recipient immune and regenerative responses towards xenogeneic biomaterial generation.</description><identifier>ISSN: 0142-9612</identifier><identifier>EISSN: 1878-5905</identifier><identifier>DOI: 10.1016/j.biomaterials.2016.03.024</identifier><identifier>PMID: 27031928</identifier><language>eng</language><publisher>Netherlands: Elsevier Ltd</publisher><subject>adaptive immunity ; Adaptive Immunity - drug effects ; Advanced Basic Science ; Animals ; Antigen removal ; antigens ; Antigens, Heterophile - metabolism ; Architecture ; biobased products ; biocompatible materials ; Biocompatible Materials - pharmacology ; Biomaterials ; Biomedical materials ; calcification ; Calcification, Physiologic - drug effects ; Cattle ; Collagen - metabolism ; crosslinking ; Decellularization ; Dentistry ; Electrochemical machining ; encapsulation ; Extracellular matrix ; Extracellular Matrix - drug effects ; Extracellular Matrix - metabolism ; Foreign-Body Reaction - pathology ; hydrophilicity ; Hydrophobic and Hydrophilic Interactions ; Immune response ; Immunity, Humoral - drug effects ; lipophilicity ; Neovascularization, Physiologic - drug effects ; pericardium ; Pericardium - drug effects ; Preservation ; proteins ; Rabbits ; Regeneration - drug effects ; Regenerative ; Scaffolds ; Surgical implants ; Sus scrofa ; swine ; Tissue Scaffolds - chemistry ; Vascular regenerative medicine ; Xenogeneic scaffold</subject><ispartof>Biomaterials, 2016-06, Vol.92, p.1-12</ispartof><rights>2016</rights><rights>Copyright © 2016. Published by Elsevier Ltd.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c641t-829145d4d6a5957f8af509cd6de26100a64fbd5e56cd1aa92af7400e9bc0b36f3</citedby><cites>FETCH-LOGICAL-c641t-829145d4d6a5957f8af509cd6de26100a64fbd5e56cd1aa92af7400e9bc0b36f3</cites><orcidid>0000-0003-3639-5561</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.biomaterials.2016.03.024$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>230,314,780,784,885,3550,27924,27925,45995</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/27031928$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Wong, Maelene L</creatorcontrib><creatorcontrib>Wong, Janelle L</creatorcontrib><creatorcontrib>Vapniarsky, Natalia</creatorcontrib><creatorcontrib>Griffiths, Leigh G</creatorcontrib><title>In vivo xenogeneic scaffold fate is determined by residual antigenicity and extracellular matrix preservation</title><title>Biomaterials</title><addtitle>Biomaterials</addtitle><description>Abstract The immunological potential of animal-derived tissues and organs is the critical hurdle to increasing their clinical implementation. Glutaraldehyde-fixation cross-links proteins in xenogeneic tissues (e.g., bovine pericardium) to delay immune rejection, but also compromises the regenerative potential of the resultant biomaterial. Unfixed xenogeneic biomaterials in which xenoantigenicity has been ameliorated and native extracellular matrix (ECM) architecture has been maintained have the potential to overcome limitations of current clinically utilized glutaraldehyde-fixed biomaterials. The objective of this work was to determine how residual antigenicity and ECM architecture preservation modulate recipient immune and regenerative responses towards unfixed bovine pericardium (BP) ECM scaffolds. Disruption of ECM architecture during scaffold generation, with either SDS-decellularization or glutaraldehyde-fixation, stimulated recipient foreign body response and resultant fibrotic encapsulation following leporine subpannicular implantation. Conversely, BP scaffolds subjected to stepwise removal of hydrophilic and lipophilic antigens using amidosulfobetaine-14 (ASB-14) maintained native ECM architecture and thereby avoided fibrotic encapsulation. Removal of hydrophilic and lipophilic antigens significantly decreased local and systemic graft-specific, adaptive immune responses and subsequent calcification of BP scaffolds compared to scaffolds undergoing hydrophile removal only. Critically, removal of antigenic components and preservation of ECM architecture with ASB-14 promoted full-thickness recipient non-immune cellular repopulation of the BP scaffold. Further, unlike clinically utilized fixed BP, ASB-14-treated scaffolds fostered rapid intimal and medial vessel wall regeneration in a porcine carotid patch angioplasty model. This work highlights the importance of residual antigenicity and ECM architecture preservation in modulating recipient immune and regenerative responses towards xenogeneic biomaterial generation.</description><subject>adaptive immunity</subject><subject>Adaptive Immunity - drug effects</subject><subject>Advanced Basic Science</subject><subject>Animals</subject><subject>Antigen removal</subject><subject>antigens</subject><subject>Antigens, Heterophile - metabolism</subject><subject>Architecture</subject><subject>biobased products</subject><subject>biocompatible materials</subject><subject>Biocompatible Materials - pharmacology</subject><subject>Biomaterials</subject><subject>Biomedical materials</subject><subject>calcification</subject><subject>Calcification, Physiologic - drug effects</subject><subject>Cattle</subject><subject>Collagen - metabolism</subject><subject>crosslinking</subject><subject>Decellularization</subject><subject>Dentistry</subject><subject>Electrochemical machining</subject><subject>encapsulation</subject><subject>Extracellular matrix</subject><subject>Extracellular Matrix - drug effects</subject><subject>Extracellular Matrix - metabolism</subject><subject>Foreign-Body Reaction - pathology</subject><subject>hydrophilicity</subject><subject>Hydrophobic and Hydrophilic Interactions</subject><subject>Immune response</subject><subject>Immunity, Humoral - drug effects</subject><subject>lipophilicity</subject><subject>Neovascularization, Physiologic - drug effects</subject><subject>pericardium</subject><subject>Pericardium - drug effects</subject><subject>Preservation</subject><subject>proteins</subject><subject>Rabbits</subject><subject>Regeneration - drug effects</subject><subject>Regenerative</subject><subject>Scaffolds</subject><subject>Surgical implants</subject><subject>Sus scrofa</subject><subject>swine</subject><subject>Tissue Scaffolds - chemistry</subject><subject>Vascular regenerative medicine</subject><subject>Xenogeneic scaffold</subject><issn>0142-9612</issn><issn>1878-5905</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNUstuEzEUHSEQDYVfQBYrNgnXHnvGZlEJtTwqVWIBSOwsj32nOEzsYs9Eyd_wLXwZHqVUhQ3xxrr2Oee-TlW9oLCiQJtX61Xn48aMmLwZ8oqVtxXUK2D8QbWgspVLoUA8rBZAOVuqhrKT6knOaygxcPa4OmEt1FQxuajCZfj1c-u3kewwxGsM6C3J1vR9HBzpSxLiM3FYkm18QEe6PUmYvZvMQEwYfaF468d9CRzB3ZiMxWGYBpNIKTH5HbkpeExbM_oYnlaP-lIzPru9T6sv795-Pv-wvPr4_vL8zdXSNpyOS8kU5cJx1xihRNtL0wtQ1jUOWUMBTMP7zgkUjXXUGMVM33IAVJ2Frm76-rQ6O-jeTN0GncVQChv0TfIbk_Y6Gq___gn-m76OWy2YVNC0ReDlrUCKPybMo974PHdmAsYpa1Y2UXNe0-a_UCpBgpCKHwFtZasklHMMlIpa1KAK9PUBalPMOWF_1ycFPTtGr_V9x-jZMRpqXRxTyM_vT-qO-sciBXBxAGDZ19Zj0tl6DBadT2hH7aI_Ls_ZPzJ28MU6ZviOe8zrOKUwc6jOTIP-NHt3tm4ZMAAXX-vfyjvxdg</recordid><startdate>20160601</startdate><enddate>20160601</enddate><creator>Wong, Maelene L</creator><creator>Wong, Janelle L</creator><creator>Vapniarsky, Natalia</creator><creator>Griffiths, Leigh G</creator><general>Elsevier Ltd</general><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>7X8</scope><scope>7QO</scope><scope>8FD</scope><scope>FR3</scope><scope>P64</scope><scope>7SR</scope><scope>7TB</scope><scope>7U5</scope><scope>8BQ</scope><scope>F28</scope><scope>JG9</scope><scope>L7M</scope><scope>7S9</scope><scope>L.6</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-3639-5561</orcidid></search><sort><creationdate>20160601</creationdate><title>In vivo xenogeneic scaffold fate is determined by residual antigenicity and extracellular matrix preservation</title><author>Wong, Maelene L ; Wong, Janelle L ; Vapniarsky, Natalia ; Griffiths, Leigh G</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c641t-829145d4d6a5957f8af509cd6de26100a64fbd5e56cd1aa92af7400e9bc0b36f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>adaptive immunity</topic><topic>Adaptive Immunity - drug effects</topic><topic>Advanced Basic Science</topic><topic>Animals</topic><topic>Antigen removal</topic><topic>antigens</topic><topic>Antigens, Heterophile - metabolism</topic><topic>Architecture</topic><topic>biobased products</topic><topic>biocompatible materials</topic><topic>Biocompatible Materials - pharmacology</topic><topic>Biomaterials</topic><topic>Biomedical materials</topic><topic>calcification</topic><topic>Calcification, Physiologic - drug effects</topic><topic>Cattle</topic><topic>Collagen - metabolism</topic><topic>crosslinking</topic><topic>Decellularization</topic><topic>Dentistry</topic><topic>Electrochemical machining</topic><topic>encapsulation</topic><topic>Extracellular matrix</topic><topic>Extracellular Matrix - drug effects</topic><topic>Extracellular Matrix - metabolism</topic><topic>Foreign-Body Reaction - pathology</topic><topic>hydrophilicity</topic><topic>Hydrophobic and Hydrophilic Interactions</topic><topic>Immune response</topic><topic>Immunity, Humoral - drug effects</topic><topic>lipophilicity</topic><topic>Neovascularization, Physiologic - drug effects</topic><topic>pericardium</topic><topic>Pericardium - drug effects</topic><topic>Preservation</topic><topic>proteins</topic><topic>Rabbits</topic><topic>Regeneration - drug effects</topic><topic>Regenerative</topic><topic>Scaffolds</topic><topic>Surgical implants</topic><topic>Sus scrofa</topic><topic>swine</topic><topic>Tissue Scaffolds - chemistry</topic><topic>Vascular regenerative medicine</topic><topic>Xenogeneic scaffold</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Wong, Maelene L</creatorcontrib><creatorcontrib>Wong, Janelle L</creatorcontrib><creatorcontrib>Vapniarsky, Natalia</creatorcontrib><creatorcontrib>Griffiths, Leigh G</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Biotechnology Research Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Engineered Materials Abstracts</collection><collection>Mechanical & Transportation Engineering Abstracts</collection><collection>Solid State and Superconductivity Abstracts</collection><collection>METADEX</collection><collection>ANTE: Abstracts in New Technology & Engineering</collection><collection>Materials Research Database</collection><collection>Advanced Technologies Database with Aerospace</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Biomaterials</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wong, Maelene L</au><au>Wong, Janelle L</au><au>Vapniarsky, Natalia</au><au>Griffiths, Leigh G</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>In vivo xenogeneic scaffold fate is determined by residual antigenicity and extracellular matrix preservation</atitle><jtitle>Biomaterials</jtitle><addtitle>Biomaterials</addtitle><date>2016-06-01</date><risdate>2016</risdate><volume>92</volume><spage>1</spage><epage>12</epage><pages>1-12</pages><issn>0142-9612</issn><eissn>1878-5905</eissn><abstract>Abstract The immunological potential of animal-derived tissues and organs is the critical hurdle to increasing their clinical implementation. Glutaraldehyde-fixation cross-links proteins in xenogeneic tissues (e.g., bovine pericardium) to delay immune rejection, but also compromises the regenerative potential of the resultant biomaterial. Unfixed xenogeneic biomaterials in which xenoantigenicity has been ameliorated and native extracellular matrix (ECM) architecture has been maintained have the potential to overcome limitations of current clinically utilized glutaraldehyde-fixed biomaterials. The objective of this work was to determine how residual antigenicity and ECM architecture preservation modulate recipient immune and regenerative responses towards unfixed bovine pericardium (BP) ECM scaffolds. Disruption of ECM architecture during scaffold generation, with either SDS-decellularization or glutaraldehyde-fixation, stimulated recipient foreign body response and resultant fibrotic encapsulation following leporine subpannicular implantation. Conversely, BP scaffolds subjected to stepwise removal of hydrophilic and lipophilic antigens using amidosulfobetaine-14 (ASB-14) maintained native ECM architecture and thereby avoided fibrotic encapsulation. Removal of hydrophilic and lipophilic antigens significantly decreased local and systemic graft-specific, adaptive immune responses and subsequent calcification of BP scaffolds compared to scaffolds undergoing hydrophile removal only. Critically, removal of antigenic components and preservation of ECM architecture with ASB-14 promoted full-thickness recipient non-immune cellular repopulation of the BP scaffold. Further, unlike clinically utilized fixed BP, ASB-14-treated scaffolds fostered rapid intimal and medial vessel wall regeneration in a porcine carotid patch angioplasty model. This work highlights the importance of residual antigenicity and ECM architecture preservation in modulating recipient immune and regenerative responses towards xenogeneic biomaterial generation.</abstract><cop>Netherlands</cop><pub>Elsevier Ltd</pub><pmid>27031928</pmid><doi>10.1016/j.biomaterials.2016.03.024</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0003-3639-5561</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | adaptive immunity Adaptive Immunity - drug effects Advanced Basic Science Animals Antigen removal antigens Antigens, Heterophile - metabolism Architecture biobased products biocompatible materials Biocompatible Materials - pharmacology Biomaterials Biomedical materials calcification Calcification, Physiologic - drug effects Cattle Collagen - metabolism crosslinking Decellularization Dentistry Electrochemical machining encapsulation Extracellular matrix Extracellular Matrix - drug effects Extracellular Matrix - metabolism Foreign-Body Reaction - pathology hydrophilicity Hydrophobic and Hydrophilic Interactions Immune response Immunity, Humoral - drug effects lipophilicity Neovascularization, Physiologic - drug effects pericardium Pericardium - drug effects Preservation proteins Rabbits Regeneration - drug effects Regenerative Scaffolds Surgical implants Sus scrofa swine Tissue Scaffolds - chemistry Vascular regenerative medicine Xenogeneic scaffold |
| title | In vivo xenogeneic scaffold fate is determined by residual antigenicity and extracellular matrix preservation |
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