Cellular extrusion bioprinting improves kidney organoid reproducibility and conformation
Directed differentiation of human pluripotent stem cells to kidney organoids brings the prospect of drug screening, disease modelling and the generation of tissue for renal replacement. Currently, these applications are hampered by organoid variability, nephron immaturity, low throughput and limited...
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| Veröffentlicht in: | Nature materials 2021-02, Vol.20 (2), p.260-271 |
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| creator | Lawlor, Kynan T. Vanslambrouck, Jessica M. Higgins, J. William Chambon, Alison Bishard, Kristina Arndt, Derek Er, Pei Xuan Wilson, Sean B. Howden, Sara E. Tan, Ker Sin Li, Fanyi Hale, Lorna J. Shepherd, Benjamin Pentoney, Stephen Presnell, Sharon C. Chen, Alice E. Little, Melissa H. |
| description | Directed differentiation of human pluripotent stem cells to kidney organoids brings the prospect of drug screening, disease modelling and the generation of tissue for renal replacement. Currently, these applications are hampered by organoid variability, nephron immaturity, low throughput and limited scale. Here, we apply extrusion-based three-dimensional cellular bioprinting to deliver rapid and high-throughput generation of kidney organoids with highly reproducible cell number and viability. We demonstrate that manual organoid generation can be replaced by 6- or 96-well organoid bioprinting and evaluate the relative toxicity of aminoglycosides as a proof of concept for drug testing. In addition, three-dimensional bioprinting enables precise manipulation of biophysical properties, including organoid size, cell number and conformation, with modification of organoid conformation substantially increasing nephron yield per starting cell number. This facilitates the manufacture of uniformly patterned kidney tissue sheets with functional proximal tubular segments. Hence, automated extrusion-based bioprinting for kidney organoid production delivers improvements in throughput, quality control, scale and structure, facilitating in vitro and in vivo applications of stem cell-derived human kidney tissue.
Extrusion-based bioprinting has been shown to rapidly and reproducibly generate kidney organoids from a cell-only paste, with the number and maturation of functional units within the kidney tissue capable of being further improved by bioprinting tissue sheets. |
| doi_str_mv | 10.1038/s41563-020-00853-9 |
| format | Article |
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Extrusion-based bioprinting has been shown to rapidly and reproducibly generate kidney organoids from a cell-only paste, with the number and maturation of functional units within the kidney tissue capable of being further improved by bioprinting tissue sheets.</description><identifier>ISSN: 1476-1122</identifier><identifier>EISSN: 1476-4660</identifier><identifier>DOI: 10.1038/s41563-020-00853-9</identifier><identifier>PMID: 33230326</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>631/80/83 ; 639/166/985 ; 639/301/54/2295 ; 692/308/2171 ; Aminoglycosides ; Automation ; Biocompatibility ; Biomaterials ; Bioprinting ; Chemistry and Materials Science ; Condensed Matter Physics ; Extrusion ; Gene expression ; Genetic engineering ; Humans ; Hydrogels ; In vivo methods and tests ; Kidney Tubules, Proximal - cytology ; Kidney Tubules, Proximal - metabolism ; Kidneys ; Materials Science ; Nanotechnology ; Optical and Electronic Materials ; Organoids - cytology ; Organoids - metabolism ; Pluripotent Stem Cells - cytology ; Pluripotent Stem Cells - metabolism ; Quality control ; Reproducibility ; Sheets ; Stem cells ; Three dimensional printing ; Tissue engineering ; Tissues ; Toxicity</subject><ispartof>Nature materials, 2021-02, Vol.20 (2), p.260-271</ispartof><rights>The Author(s), under exclusive licence to Springer Nature Limited 2020</rights><rights>The Author(s), under exclusive licence to Springer Nature Limited 2020.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c598t-23c34943a1dca7ce33102a431831c0d43be50f62c3f3a96a69b4b75145d06a1f3</citedby><cites>FETCH-LOGICAL-c598t-23c34943a1dca7ce33102a431831c0d43be50f62c3f3a96a69b4b75145d06a1f3</cites><orcidid>0000-0003-0380-2263 ; 0000-0003-4080-5439</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,315,781,785,886,27925,27926</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33230326$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Lawlor, Kynan T.</creatorcontrib><creatorcontrib>Vanslambrouck, Jessica M.</creatorcontrib><creatorcontrib>Higgins, J. William</creatorcontrib><creatorcontrib>Chambon, Alison</creatorcontrib><creatorcontrib>Bishard, Kristina</creatorcontrib><creatorcontrib>Arndt, Derek</creatorcontrib><creatorcontrib>Er, Pei Xuan</creatorcontrib><creatorcontrib>Wilson, Sean B.</creatorcontrib><creatorcontrib>Howden, Sara E.</creatorcontrib><creatorcontrib>Tan, Ker Sin</creatorcontrib><creatorcontrib>Li, Fanyi</creatorcontrib><creatorcontrib>Hale, Lorna J.</creatorcontrib><creatorcontrib>Shepherd, Benjamin</creatorcontrib><creatorcontrib>Pentoney, Stephen</creatorcontrib><creatorcontrib>Presnell, Sharon C.</creatorcontrib><creatorcontrib>Chen, Alice E.</creatorcontrib><creatorcontrib>Little, Melissa H.</creatorcontrib><title>Cellular extrusion bioprinting improves kidney organoid reproducibility and conformation</title><title>Nature materials</title><addtitle>Nat. Mater</addtitle><addtitle>Nat Mater</addtitle><description>Directed differentiation of human pluripotent stem cells to kidney organoids brings the prospect of drug screening, disease modelling and the generation of tissue for renal replacement. Currently, these applications are hampered by organoid variability, nephron immaturity, low throughput and limited scale. Here, we apply extrusion-based three-dimensional cellular bioprinting to deliver rapid and high-throughput generation of kidney organoids with highly reproducible cell number and viability. We demonstrate that manual organoid generation can be replaced by 6- or 96-well organoid bioprinting and evaluate the relative toxicity of aminoglycosides as a proof of concept for drug testing. In addition, three-dimensional bioprinting enables precise manipulation of biophysical properties, including organoid size, cell number and conformation, with modification of organoid conformation substantially increasing nephron yield per starting cell number. This facilitates the manufacture of uniformly patterned kidney tissue sheets with functional proximal tubular segments. Hence, automated extrusion-based bioprinting for kidney organoid production delivers improvements in throughput, quality control, scale and structure, facilitating in vitro and in vivo applications of stem cell-derived human kidney tissue.
Extrusion-based bioprinting has been shown to rapidly and reproducibly generate kidney organoids from a cell-only paste, with the number and maturation of functional units within the kidney tissue capable of being further improved by bioprinting tissue sheets.</description><subject>631/80/83</subject><subject>639/166/985</subject><subject>639/301/54/2295</subject><subject>692/308/2171</subject><subject>Aminoglycosides</subject><subject>Automation</subject><subject>Biocompatibility</subject><subject>Biomaterials</subject><subject>Bioprinting</subject><subject>Chemistry and Materials Science</subject><subject>Condensed Matter Physics</subject><subject>Extrusion</subject><subject>Gene expression</subject><subject>Genetic engineering</subject><subject>Humans</subject><subject>Hydrogels</subject><subject>In vivo methods and tests</subject><subject>Kidney Tubules, Proximal - cytology</subject><subject>Kidney Tubules, Proximal - metabolism</subject><subject>Kidneys</subject><subject>Materials Science</subject><subject>Nanotechnology</subject><subject>Optical and Electronic Materials</subject><subject>Organoids - cytology</subject><subject>Organoids - metabolism</subject><subject>Pluripotent Stem Cells - cytology</subject><subject>Pluripotent Stem Cells - metabolism</subject><subject>Quality control</subject><subject>Reproducibility</subject><subject>Sheets</subject><subject>Stem cells</subject><subject>Three dimensional printing</subject><subject>Tissue engineering</subject><subject>Tissues</subject><subject>Toxicity</subject><issn>1476-1122</issn><issn>1476-4660</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNp9kU1P3DAQhq2Kqnz1D3CoInHhEurx2E5yQUIrSpGQuIDEzXIcZzFN7K2doO6_r-luaeHAyZbmmdeeeQg5AnoKFOuviYOQWFJGS0prgWXzgewBr2TJpaQ72zsAY7tkP6VHShkIIT-RXUSGFJncI_cLOwzzoGNhf01xTi74onVhFZ2fnF8WblzF8GRT8cN13q6LEJfaB9cV0eZCNxvXusFN60L7rjDB9yGOesoph-Rjr4dkP2_PA3L37eJ28b28vrm8Wpxfl0Y09VQyNMgbjho6oytjEYEyzRFqBEM7jq0VtJfMYI-6kVo2LW8rAVx0VGro8YCcbXJXczvazlg_RT2oPMCo41oF7dTrincPahmeVFULgRXkgJNtQAw_Z5smNbpk8la0t2FOinHJgeeFiYwev0Efwxx9Hi9TNXBgVFSZYhvKxJBStP3LZ4CqZ3FqI05lceqPONXkpi__j_HS8tdUBnADpGc3Sxv_vf1O7G-Gw6Wi</recordid><startdate>20210201</startdate><enddate>20210201</enddate><creator>Lawlor, Kynan T.</creator><creator>Vanslambrouck, Jessica M.</creator><creator>Higgins, J. 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William ; Chambon, Alison ; Bishard, Kristina ; Arndt, Derek ; Er, Pei Xuan ; Wilson, Sean B. ; Howden, Sara E. ; Tan, Ker Sin ; Li, Fanyi ; Hale, Lorna J. ; Shepherd, Benjamin ; Pentoney, Stephen ; Presnell, Sharon C. ; Chen, Alice E. ; Little, Melissa H.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c598t-23c34943a1dca7ce33102a431831c0d43be50f62c3f3a96a69b4b75145d06a1f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>631/80/83</topic><topic>639/166/985</topic><topic>639/301/54/2295</topic><topic>692/308/2171</topic><topic>Aminoglycosides</topic><topic>Automation</topic><topic>Biocompatibility</topic><topic>Biomaterials</topic><topic>Bioprinting</topic><topic>Chemistry and Materials Science</topic><topic>Condensed Matter Physics</topic><topic>Extrusion</topic><topic>Gene expression</topic><topic>Genetic engineering</topic><topic>Humans</topic><topic>Hydrogels</topic><topic>In vivo methods and tests</topic><topic>Kidney Tubules, Proximal - cytology</topic><topic>Kidney Tubules, Proximal - metabolism</topic><topic>Kidneys</topic><topic>Materials Science</topic><topic>Nanotechnology</topic><topic>Optical and Electronic Materials</topic><topic>Organoids - cytology</topic><topic>Organoids - metabolism</topic><topic>Pluripotent Stem Cells - cytology</topic><topic>Pluripotent Stem Cells - metabolism</topic><topic>Quality control</topic><topic>Reproducibility</topic><topic>Sheets</topic><topic>Stem cells</topic><topic>Three dimensional printing</topic><topic>Tissue engineering</topic><topic>Tissues</topic><topic>Toxicity</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Lawlor, Kynan T.</creatorcontrib><creatorcontrib>Vanslambrouck, Jessica M.</creatorcontrib><creatorcontrib>Higgins, J. 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William</au><au>Chambon, Alison</au><au>Bishard, Kristina</au><au>Arndt, Derek</au><au>Er, Pei Xuan</au><au>Wilson, Sean B.</au><au>Howden, Sara E.</au><au>Tan, Ker Sin</au><au>Li, Fanyi</au><au>Hale, Lorna J.</au><au>Shepherd, Benjamin</au><au>Pentoney, Stephen</au><au>Presnell, Sharon C.</au><au>Chen, Alice E.</au><au>Little, Melissa H.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Cellular extrusion bioprinting improves kidney organoid reproducibility and conformation</atitle><jtitle>Nature materials</jtitle><stitle>Nat. Mater</stitle><addtitle>Nat Mater</addtitle><date>2021-02-01</date><risdate>2021</risdate><volume>20</volume><issue>2</issue><spage>260</spage><epage>271</epage><pages>260-271</pages><issn>1476-1122</issn><eissn>1476-4660</eissn><abstract>Directed differentiation of human pluripotent stem cells to kidney organoids brings the prospect of drug screening, disease modelling and the generation of tissue for renal replacement. Currently, these applications are hampered by organoid variability, nephron immaturity, low throughput and limited scale. Here, we apply extrusion-based three-dimensional cellular bioprinting to deliver rapid and high-throughput generation of kidney organoids with highly reproducible cell number and viability. We demonstrate that manual organoid generation can be replaced by 6- or 96-well organoid bioprinting and evaluate the relative toxicity of aminoglycosides as a proof of concept for drug testing. In addition, three-dimensional bioprinting enables precise manipulation of biophysical properties, including organoid size, cell number and conformation, with modification of organoid conformation substantially increasing nephron yield per starting cell number. This facilitates the manufacture of uniformly patterned kidney tissue sheets with functional proximal tubular segments. Hence, automated extrusion-based bioprinting for kidney organoid production delivers improvements in throughput, quality control, scale and structure, facilitating in vitro and in vivo applications of stem cell-derived human kidney tissue.
Extrusion-based bioprinting has been shown to rapidly and reproducibly generate kidney organoids from a cell-only paste, with the number and maturation of functional units within the kidney tissue capable of being further improved by bioprinting tissue sheets.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>33230326</pmid><doi>10.1038/s41563-020-00853-9</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0003-0380-2263</orcidid><orcidid>https://orcid.org/0000-0003-4080-5439</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | 631/80/83 639/166/985 639/301/54/2295 692/308/2171 Aminoglycosides Automation Biocompatibility Biomaterials Bioprinting Chemistry and Materials Science Condensed Matter Physics Extrusion Gene expression Genetic engineering Humans Hydrogels In vivo methods and tests Kidney Tubules, Proximal - cytology Kidney Tubules, Proximal - metabolism Kidneys Materials Science Nanotechnology Optical and Electronic Materials Organoids - cytology Organoids - metabolism Pluripotent Stem Cells - cytology Pluripotent Stem Cells - metabolism Quality control Reproducibility Sheets Stem cells Three dimensional printing Tissue engineering Tissues Toxicity |
| title | Cellular extrusion bioprinting improves kidney organoid reproducibility and conformation |
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