A Systematic comparison of in vitro cell uptake and in vivo biodistribution for three classes of gold nanoparticles with saturated PEG coatings
A great deal of attention has been focused on nanoparticles for cancer therapy, with the promise of tumor-selective delivery. However, despite intense work in the field over many years, the biggest obstacle to this vision remains extremely low delivery efficiency of nanoparticles into tumors. Due to...
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| description | A great deal of attention has been focused on nanoparticles for cancer therapy, with the promise of tumor-selective delivery. However, despite intense work in the field over many years, the biggest obstacle to this vision remains extremely low delivery efficiency of nanoparticles into tumors. Due to the cost, time, and impact on the animals for in vivo studies, the nanoparticle field predominantly uses cellular uptake assays as a proxy to predict in vivo outcomes. Extensive research has focused on decreasing macrophage uptake in vitro as a proxy to delay nanoparticle accumulation in the mononuclear phagocytic system (MPS), mainly the liver and spleen, and thereby increase tumor accumulation. We have recently reported novel synthetic methods employing small molecule crosslinkers for the controlled assembly of small nanoparticles into larger aggregates and found that these nanoaggregates had remarkably high surface coverage and low cell uptake, even in macrophages. We further found that this extremely low cellular uptake could be recapitulated on solid gold nanoparticles by densely coating their surface with small molecules. Here we report our studies on the biodistribution and clearance of these materials in comparison to more conventional PEGylated gold nanoparticles. It was expected that the remarkably low macrophage uptake in vitro would translate to extended blood circulation time in vivo, but instead we found no correlation between either surface coverage or in vitro macrophage cell uptake and in vivo blood circulation. Gold nanoaggregates accumulate more rapidly and to a higher level in the liver compared to control gold nanoparticles. The lack of correlation between in vitro macrophage uptake and in vivo blood circulation suggests that the field must find other in vitro assays to use as a primary proxy for in vivo outcomes or use direct in vivo experimentation as a primary assay. |
| doi_str_mv | 10.1371/journal.pone.0234916 |
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However, despite intense work in the field over many years, the biggest obstacle to this vision remains extremely low delivery efficiency of nanoparticles into tumors. Due to the cost, time, and impact on the animals for in vivo studies, the nanoparticle field predominantly uses cellular uptake assays as a proxy to predict in vivo outcomes. Extensive research has focused on decreasing macrophage uptake in vitro as a proxy to delay nanoparticle accumulation in the mononuclear phagocytic system (MPS), mainly the liver and spleen, and thereby increase tumor accumulation. We have recently reported novel synthetic methods employing small molecule crosslinkers for the controlled assembly of small nanoparticles into larger aggregates and found that these nanoaggregates had remarkably high surface coverage and low cell uptake, even in macrophages. We further found that this extremely low cellular uptake could be recapitulated on solid gold nanoparticles by densely coating their surface with small molecules. Here we report our studies on the biodistribution and clearance of these materials in comparison to more conventional PEGylated gold nanoparticles. It was expected that the remarkably low macrophage uptake in vitro would translate to extended blood circulation time in vivo, but instead we found no correlation between either surface coverage or in vitro macrophage cell uptake and in vivo blood circulation. Gold nanoaggregates accumulate more rapidly and to a higher level in the liver compared to control gold nanoparticles. The lack of correlation between in vitro macrophage uptake and in vivo blood circulation suggests that the field must find other in vitro assays to use as a primary proxy for in vivo outcomes or use direct in vivo experimentation as a primary assay.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0234916</identifier><identifier>PMID: 32614882</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Accumulation ; Animals ; Assaying ; Biodistribution ; Biology and Life Sciences ; Blood ; Blood circulation ; Cell interactions ; Cell surface ; Coated Materials, Biocompatible - pharmacokinetics ; Comparative analysis ; Correlation ; Crosslinking ; Endocytosis ; Engineering and Technology ; Ethanol ; Experimentation ; Experiments ; Fasting - metabolism ; Female ; Gold ; Gold - administration & dosage ; Gold - blood ; Gold - pharmacokinetics ; Half-Life ; Health aspects ; In vivo methods and tests ; Kidney - metabolism ; Liver ; Liver - metabolism ; Macrophages ; Macrophages - physiology ; Medicine ; Medicine and Health Sciences ; Metal Nanoparticles - administration & dosage ; Metal Nanoparticles - classification ; Mice ; Nanoparticles ; Organ Specificity ; Phagocytes ; Physical Sciences ; Physiological aspects ; Pilot Projects ; Polyethylene glycol ; Polyethylene Glycols ; RAW 264.7 Cells ; Specific Pathogen-Free Organisms ; Spleen ; Spleen - metabolism ; Tissue Distribution ; Tumors</subject><ispartof>PloS one, 2020-07, Vol.15 (7), p.e0234916</ispartof><rights>COPYRIGHT 2020 Public Library of Science</rights><rights>2020 Zhang et al. 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We further found that this extremely low cellular uptake could be recapitulated on solid gold nanoparticles by densely coating their surface with small molecules. Here we report our studies on the biodistribution and clearance of these materials in comparison to more conventional PEGylated gold nanoparticles. It was expected that the remarkably low macrophage uptake in vitro would translate to extended blood circulation time in vivo, but instead we found no correlation between either surface coverage or in vitro macrophage cell uptake and in vivo blood circulation. Gold nanoaggregates accumulate more rapidly and to a higher level in the liver compared to control gold nanoparticles. The lack of correlation between in vitro macrophage uptake and in vivo blood circulation suggests that the field must find other in vitro assays to use as a primary proxy for in vivo outcomes or use direct in vivo experimentation as a primary assay.</description><subject>Accumulation</subject><subject>Animals</subject><subject>Assaying</subject><subject>Biodistribution</subject><subject>Biology and Life Sciences</subject><subject>Blood</subject><subject>Blood circulation</subject><subject>Cell interactions</subject><subject>Cell surface</subject><subject>Coated Materials, Biocompatible - pharmacokinetics</subject><subject>Comparative analysis</subject><subject>Correlation</subject><subject>Crosslinking</subject><subject>Endocytosis</subject><subject>Engineering and Technology</subject><subject>Ethanol</subject><subject>Experimentation</subject><subject>Experiments</subject><subject>Fasting - metabolism</subject><subject>Female</subject><subject>Gold</subject><subject>Gold - administration & dosage</subject><subject>Gold - blood</subject><subject>Gold - pharmacokinetics</subject><subject>Half-Life</subject><subject>Health aspects</subject><subject>In vivo methods and tests</subject><subject>Kidney - metabolism</subject><subject>Liver</subject><subject>Liver - metabolism</subject><subject>Macrophages</subject><subject>Macrophages - physiology</subject><subject>Medicine</subject><subject>Medicine and Health Sciences</subject><subject>Metal Nanoparticles - administration & dosage</subject><subject>Metal Nanoparticles - classification</subject><subject>Mice</subject><subject>Nanoparticles</subject><subject>Organ Specificity</subject><subject>Phagocytes</subject><subject>Physical Sciences</subject><subject>Physiological aspects</subject><subject>Pilot Projects</subject><subject>Polyethylene glycol</subject><subject>Polyethylene Glycols</subject><subject>RAW 264.7 Cells</subject><subject>Specific Pathogen-Free Organisms</subject><subject>Spleen</subject><subject>Spleen - metabolism</subject><subject>Tissue Distribution</subject><subject>Tumors</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><sourceid>DOA</sourceid><recordid>eNqNk1FrFDEQxxdRbK1-A9GAIPhwZ7LJZpMX4Si1HhQqVn0Ns9nsXure5ppkT_sp_MrmettyCwqShw2T3_8_s8NMlr0keE5oSd5fu8H30M03rjdznFMmCX-UHRNJ8xnPMX18cD_KnoVwjXFBBedPsyOac8KEyI-z3wt0dRuiWUO0Gmm33oC3wfXINcj2aGujd0ibrkPDJsIPg6Cv9w9bhyrrahuit9UQbdI0zqO48sYg3UEIJuxcWtfVqIfeJeeUo0vRnzauUIA4eIimRp_PzlPmVEDfhufZkwa6YF6M35Ps28ezr6efZheX58vTxcVMc1zyWaM5I0DyojKVrqCWXHImSlKWVDLTMClxVUgtTcUZx9rUBQghKGlyUTXCGHqSvd77bjoX1NjLoHJGJBeSMpGI5Z6oHVyrjbdr8LfKgVV3AedbNf6QIhIXHBhgCjXTRSVIKqfAtOACGl7kyevDmG2o1qbWpo8euonp9KW3K9W6rSopzTEnyeDNaODdzWBC_EfJI9VCqsr2jUtmem2DVgueC5qMCp6o-V-odGqztjpNU2NTfCJ4NxEkJppfsYUhBLW8-vL_7OX3Kfv2gF0Z6OIquO5ulsIUZHtQexeCN81D5whWu2W474baLYMalyHJXh12_UF0P_30D4PSBlQ</recordid><startdate>20200702</startdate><enddate>20200702</enddate><creator>Zhang, Yijia</creator><creator>Liu, Alice T</creator><creator>Cornejo, Yvonne R</creator><creator>Van Haute, Desiree</creator><creator>Berlin, Jacob M</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</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>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0001-7498-766X</orcidid></search><sort><creationdate>20200702</creationdate><title>A Systematic comparison of in vitro cell uptake and in vivo biodistribution for three classes of gold nanoparticles with saturated PEG coatings</title><author>Zhang, Yijia ; Liu, Alice T ; Cornejo, Yvonne R ; Van Haute, Desiree ; Berlin, Jacob M</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c6076-fc641a125bebcbad9696487177394ef4990b59c9eb6460ced5a88831f28bf8ee3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Accumulation</topic><topic>Animals</topic><topic>Assaying</topic><topic>Biodistribution</topic><topic>Biology and Life Sciences</topic><topic>Blood</topic><topic>Blood circulation</topic><topic>Cell interactions</topic><topic>Cell surface</topic><topic>Coated Materials, Biocompatible - 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However, despite intense work in the field over many years, the biggest obstacle to this vision remains extremely low delivery efficiency of nanoparticles into tumors. Due to the cost, time, and impact on the animals for in vivo studies, the nanoparticle field predominantly uses cellular uptake assays as a proxy to predict in vivo outcomes. Extensive research has focused on decreasing macrophage uptake in vitro as a proxy to delay nanoparticle accumulation in the mononuclear phagocytic system (MPS), mainly the liver and spleen, and thereby increase tumor accumulation. We have recently reported novel synthetic methods employing small molecule crosslinkers for the controlled assembly of small nanoparticles into larger aggregates and found that these nanoaggregates had remarkably high surface coverage and low cell uptake, even in macrophages. We further found that this extremely low cellular uptake could be recapitulated on solid gold nanoparticles by densely coating their surface with small molecules. Here we report our studies on the biodistribution and clearance of these materials in comparison to more conventional PEGylated gold nanoparticles. It was expected that the remarkably low macrophage uptake in vitro would translate to extended blood circulation time in vivo, but instead we found no correlation between either surface coverage or in vitro macrophage cell uptake and in vivo blood circulation. Gold nanoaggregates accumulate more rapidly and to a higher level in the liver compared to control gold nanoparticles. The lack of correlation between in vitro macrophage uptake and in vivo blood circulation suggests that the field must find other in vitro assays to use as a primary proxy for in vivo outcomes or use direct in vivo experimentation as a primary assay.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>32614882</pmid><doi>10.1371/journal.pone.0234916</doi><tpages>e0234916</tpages><orcidid>https://orcid.org/0000-0001-7498-766X</orcidid><oa>free_for_read</oa></addata></record> |
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| source | Public Library of Science (PLoS) Journals Open Access; MEDLINE; DOAJ Directory of Open Access Journals; EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Accumulation Animals Assaying Biodistribution Biology and Life Sciences Blood Blood circulation Cell interactions Cell surface Coated Materials, Biocompatible - pharmacokinetics Comparative analysis Correlation Crosslinking Endocytosis Engineering and Technology Ethanol Experimentation Experiments Fasting - metabolism Female Gold Gold - administration & dosage Gold - blood Gold - pharmacokinetics Half-Life Health aspects In vivo methods and tests Kidney - metabolism Liver Liver - metabolism Macrophages Macrophages - physiology Medicine Medicine and Health Sciences Metal Nanoparticles - administration & dosage Metal Nanoparticles - classification Mice Nanoparticles Organ Specificity Phagocytes Physical Sciences Physiological aspects Pilot Projects Polyethylene glycol Polyethylene Glycols RAW 264.7 Cells Specific Pathogen-Free Organisms Spleen Spleen - metabolism Tissue Distribution Tumors |
| title | A Systematic comparison of in vitro cell uptake and in vivo biodistribution for three classes of gold nanoparticles with saturated PEG coatings |
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