Perfluorotributylamine-Loaded Albumin Nanoparticles Downregulate Platelet-Derived TGFβ to Inhibit Tumor Metastasis

Tumor metastasis contributes to the low overall survival of tumor patients, while transforming growth factor-β (TGFβ) has been recognized as a prominently promoting factor in the development of tumor metastasis. Platelets reserve abundant TGFβ, which will be secreted to peripheral blood after activa...

Full description

Saved in:
Bibliographic Details
Published inACS nano Vol. 17; no. 16; pp. 15388 - 15400
Main Authors Luo, Lifeng, Zhang, Baoli, Tao, Feng, Chen, Zhong, Ye, Qingsong, Zhao, Xiaozhi, Wu, Jinhui
Format Journal Article
LanguageEnglish
Published United States American Chemical Society 22.08.2023
Subjects
TGFβ
platelet
tumor metastasis
human serum albumin
perfluorotributylamine
Online AccessGet full text

Cover

Abstract Tumor metastasis contributes to the low overall survival of tumor patients, while transforming growth factor-β (TGFβ) has been recognized as a prominently promoting factor in the development of tumor metastasis. Platelets reserve abundant TGFβ, which will be secreted to peripheral blood after activation, and they are the dominant source of circulating TGFβ. Therefore, downregulation of platelet-derived TGFβ is expected to inhibit the metastasis of circulating tumor cells. Here, unfolded human serum albumin (HSA)-coated perfluorotributylamine (PFTBA) nanoparticles were constructed to display a favorable platelet delivery and an antiplatelet effect to downregulate platelet-derived TGFβ in vitro and in blood plasma. PFTBA@HSA-mediated TGFβ downregulation impaired epithelial-mesenchymal transition of tumor cells as well as their migration and invasion behaviors and enhanced immune surveillance of NK cells. Intravenous injection of PFTBA@HSA effectively reduced tumor metastasis on the lungs or liver to improve the survival rate of mice on multiple metastatic models, including CT26 colon cancer, B16F10 melanoma, and 4T1 breast cancer. Compared with the clinical antiplatelet drug ticagrelor, PFTBA@HSA reduced bleeding risk when displaying a favorable downregulation on platelet-derived TGFβ, thereby obtaining a higher therapy benefit. Together, this study confirmed that downregulation of platelet-derived TGFβ by PFTBA@HSA will be a potential approach and therapeutic candidate for the prevention of tumor metastasis.
AbstractList Tumor metastasis contributes to the low overall survival of tumor patients, while transforming growth factor-β (TGFβ) has been recognized as a prominently promoting factor in the development of tumor metastasis. Platelets reserve abundant TGFβ, which will be secreted to peripheral blood after activation, and they are the dominant source of circulating TGFβ. Therefore, downregulation of platelet-derived TGFβ is expected to inhibit the metastasis of circulating tumor cells. Here, unfolded human serum albumin (HSA)-coated perfluorotributylamine (PFTBA) nanoparticles were constructed to display a favorable platelet delivery and an antiplatelet effect to downregulate platelet-derived TGFβ and in blood plasma. PFTBA@HSA-mediated TGFβ downregulation impaired epithelial-mesenchymal transition of tumor cells as well as their migration and invasion behaviors and enhanced immune surveillance of NK cells. Intravenous injection of PFTBA@HSA effectively reduced tumor metastasis on the lungs or liver to improve the survival rate of mice on multiple metastatic models, including CT26 colon cancer, B16F10 melanoma, and 4T1 breast cancer. Compared with the clinical antiplatelet drug ticagrelor, PFTBA@HSA reduced bleeding risk when displaying a favorable downregulation on platelet-derived TGFβ, thereby obtaining a higher therapy benefit. Together, this study confirmed that downregulation of platelet-derived TGFβ by PFTBA@HSA will be a potential approach and therapeutic candidate for the prevention of tumor metastasis.
Tumor metastasis contributes to the low overall survival of tumor patients, while transforming growth factor-β (TGFβ) has been recognized as a prominently promoting factor in the development of tumor metastasis. Platelets reserve abundant TGFβ, which will be secreted to peripheral blood after activation, and they are the dominant source of circulating TGFβ. Therefore, downregulation of platelet-derived TGFβ is expected to inhibit the metastasis of circulating tumor cells. Here, unfolded human serum albumin (HSA)-coated perfluorotributylamine (PFTBA) nanoparticles were constructed to display a favorable platelet delivery and an antiplatelet effect to downregulate platelet-derived TGFβ in vitro and in blood plasma. PFTBA@HSA-mediated TGFβ downregulation impaired epithelial-mesenchymal transition of tumor cells as well as their migration and invasion behaviors and enhanced immune surveillance of NK cells. Intravenous injection of PFTBA@HSA effectively reduced tumor metastasis on the lungs or liver to improve the survival rate of mice on multiple metastatic models, including CT26 colon cancer, B16F10 melanoma, and 4T1 breast cancer. Compared with the clinical antiplatelet drug ticagrelor, PFTBA@HSA reduced bleeding risk when displaying a favorable downregulation on platelet-derived TGFβ, thereby obtaining a higher therapy benefit. Together, this study confirmed that downregulation of platelet-derived TGFβ by PFTBA@HSA will be a potential approach and therapeutic candidate for the prevention of tumor metastasis.
Author Zhang, Baoli
Wu, Jinhui
Ye, Qingsong
Luo, Lifeng
Chen, Zhong
Zhao, Xiaozhi
Tao, Feng
AuthorAffiliation State Key Laboratory of Pharmaceutical Biotechnology, Medical School
Department of Urology, Drum Tower Hospital, Medical School
Chemistry and Biomedicine Innovation Center
Jiangsu Key Laboratory for Nano Technology
Nanjing University
Wuxi Xishan NJU Institute of Applied Biotechnology
AuthorAffiliation_xml – name: Chemistry and Biomedicine Innovation Center
– name: Wuxi Xishan NJU Institute of Applied Biotechnology
– name: Jiangsu Key Laboratory for Nano Technology
– name: Nanjing University
– name: Department of Urology, Drum Tower Hospital, Medical School
– name: State Key Laboratory of Pharmaceutical Biotechnology, Medical School
Author_xml – sequence: 1
  givenname: Lifeng
  surname: Luo
  fullname: Luo, Lifeng
  organization: Department of Urology, Drum Tower Hospital, Medical School
– sequence: 2
  givenname: Baoli
  surname: Zhang
  fullname: Zhang, Baoli
  organization: State Key Laboratory of Pharmaceutical Biotechnology, Medical School
– sequence: 3
  givenname: Feng
  surname: Tao
  fullname: Tao, Feng
  organization: State Key Laboratory of Pharmaceutical Biotechnology, Medical School
– sequence: 4
  givenname: Zhong
  surname: Chen
  fullname: Chen, Zhong
  organization: State Key Laboratory of Pharmaceutical Biotechnology, Medical School
– sequence: 5
  givenname: Qingsong
  surname: Ye
  fullname: Ye, Qingsong
  organization: State Key Laboratory of Pharmaceutical Biotechnology, Medical School
– sequence: 6
  givenname: Xiaozhi
  orcidid: 0000-0002-4265-9730
  surname: Zhao
  fullname: Zhao, Xiaozhi
  organization: Department of Urology, Drum Tower Hospital, Medical School
– sequence: 7
  givenname: Jinhui
  orcidid: 0000-0001-8809-1290
  surname: Wu
  fullname: Wu, Jinhui
  email: wuj@nju.edu.cn
  organization: Nanjing University
BackLink https://www.ncbi.nlm.nih.gov/pubmed/37526429$$D View this record in MEDLINE/PubMed
BookMark eNp1kM1q3DAUhUVJaTJp190VLwPBM_qxbHkZkkw6ME2ymEJ3RrKvWwVZmugnIa-VB8kzVWGmsysI6Qq-cy7nzNCRdRYQ-krwnGBKFrIPVlo3Zz3GtOUf0AlpWV1iUf86OsycHKNZCA8Y80Y09Sd0zBpO64q2Jyjcgx9Nct5Fr1WKL0ZO2kK5dnKAobgwKuV_cZuXbKWPujcQiiv3bD38TkZGKO7fbwOxvAKvn7Jmc7N8ey2iK1b2j1Y6Fps0OV_8gChDPjp8Rh9HaQJ82b-n6OfyenP5vVzf3awuL9alZIzFEmpFscy5GOZAJBc9Vxwz0RLGRirboW0rqUZaC6jHYWwaIipOpRgVU2JQDTtFZzvfrXePCULsJh16MEZacCl0VFRVLQhmJKOLHdp7F4KHsdt6PUn_0hHcvTfd7Zvu9k1nxbe9eVITDAf-X7UZON8BWdk9uORtzvpfu7_jxI5D
CitedBy_id crossref_primary_10_1016_j_jconrel_2024_05_025
crossref_primary_10_1002_adma_202304328
crossref_primary_10_1016_j_ijbiomac_2023_129070
crossref_primary_10_1021_acsnano_3c12281
crossref_primary_10_1016_j_actbio_2024_05_016
crossref_primary_10_1021_acsami_3c13855
Cites_doi 10.2147/DDDT.S86621
10.1016/S1535-6108(03)00132-6
10.1016/j.canlet.2008.11.035
10.1254/jphs.09043FP
10.1182/blood.V122.21.SCI-31.SCI-31
10.1038/nri2808
10.1016/j.cell.2008.07.001
10.1152/jappl.2001.91.5.1941
10.1016/j.immuni.2019.03.024
10.1002/smll.201801694
10.1016/j.cca.2006.02.027
10.1007/s10753-013-9678-z
10.1016/j.ccell.2018.03.002
10.1182/blood.V128.22.3723.3723
10.1186/s13045-018-0669-2
10.1371/journal.pone.0173884
10.1126/scitranslmed.aay4860
10.1038/nature25501
10.1371/journal.pone.0067109
10.1182/blood.V116.21.3193.3193
10.1016/j.ccr.2011.09.009
10.1126/scitranslmed.aaz7287
10.1038/nrcardio.2017.206
10.1158/0008-5472.CAN-09-2123
10.1038/s41392-020-00436-9
10.1038/s41573-019-0052-1
10.1073/pnas.1901987116
10.1074/jbc.M112.443655
10.1111/j.1349-7006.2011.01917.x
10.1007/s00424-020-02482-2
10.3748/wjg.v16.i17.2080
10.3389/fimmu.2021.640578
10.1126/scisignal.2005189
10.1002/adma.201901513
10.1038/s41568-021-00413-6
10.1126/sciimmunol.aai7911
10.1021/acsnano.9b09827
10.1038/nature25492
10.1038/s41571-020-0403-1
10.1182/blood.V122.21.3488.3488
10.3390/ijms22094492
10.1038/ncomms9785
10.7150/thno.17908
ContentType Journal Article
Copyright 2023 American Chemical Society
Copyright_xml – notice: 2023 American Chemical Society
DBID NPM
AAYXX
CITATION
7X8
DOI 10.1021/acsnano.3c00295
DatabaseName PubMed
CrossRef
MEDLINE - Academic
DatabaseTitle PubMed
CrossRef
MEDLINE - Academic
DatabaseTitleList PubMed
Database_xml – sequence: 1
  dbid: NPM
  name: PubMed
  url: https://proxy.k.utb.cz/login?url=http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed
  sourceTypes: Index Database
DeliveryMethod fulltext_linktorsrc
Discipline Engineering
EISSN 1936-086X
EndPage 15400
ExternalDocumentID 10_1021_acsnano_3c00295
37526429
a541083221
Genre Journal Article
GroupedDBID ---
.K2
23M
4.4
55A
5GY
5VS
6J9
7~N
AABXI
ABFRP
ABMVS
ABQRX
ABUCX
ACGFO
ACGFS
ACS
ADHLV
AEESW
AENEX
AFEFF
AHGAQ
ALMA_UNASSIGNED_HOLDINGS
AQSVZ
CS3
EBS
ED~
F5P
GGK
GNL
IH9
IHE
JG~
P2P
RNS
ROL
UI2
VF5
VG9
W1F
XKZ
YZZ
AAHBH
ABJNI
ACBEA
BAANH
CUPRZ
NPM
AAYXX
CITATION
7X8
ID FETCH-LOGICAL-a333t-e6b20a002305e1a58c5b50389133f2a9d994abf268e6fdf7718452a8fb3b8db73
IEDL.DBID ACS
ISSN 1936-0851
IngestDate Fri Aug 16 10:10:01 EDT 2024
Fri Aug 23 02:52:09 EDT 2024
Tue Aug 27 13:54:02 EDT 2024
Thu Aug 24 08:24:00 EDT 2023
IsPeerReviewed true
IsScholarly true
Issue 16
Keywords TGFβ
platelet
tumor metastasis
human serum albumin
perfluorotributylamine
Language English
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-a333t-e6b20a002305e1a58c5b50389133f2a9d994abf268e6fdf7718452a8fb3b8db73
Notes ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 23
ORCID 0000-0001-8809-1290
0000-0002-4265-9730
PMID 37526429
PQID 2844681031
PQPubID 23479
PageCount 13
ParticipantIDs proquest_miscellaneous_2844681031
crossref_primary_10_1021_acsnano_3c00295
pubmed_primary_37526429
acs_journals_10_1021_acsnano_3c00295
PublicationCentury 2000
PublicationDate 2023-08-22
PublicationDateYYYYMMDD 2023-08-22
PublicationDate_xml – month: 08
  year: 2023
  text: 2023-08-22
  day: 22
PublicationDecade 2020
PublicationPlace United States
PublicationPlace_xml – name: United States
PublicationTitle ACS nano
PublicationTitleAlternate ACS Nano
PublicationYear 2023
Publisher American Chemical Society
Publisher_xml – name: American Chemical Society
References ref9/cit9
ref45/cit45
ref6/cit6
ref36/cit36
ref3/cit3
ref27/cit27
ref18/cit18
ref11/cit11
ref25/cit25
ref16/cit16
ref29/cit29
ref32/cit32
ref23/cit23
ref39/cit39
ref14/cit14
ref8/cit8
ref5/cit5
ref31/cit31
ref2/cit2
ref43/cit43
ref34/cit34
ref37/cit37
ref28/cit28
ref40/cit40
ref20/cit20
ref17/cit17
ref10/cit10
Kelly A. (ref24/cit24) 2017; 134
ref26/cit26
ref35/cit35
ref19/cit19
ref21/cit21
ref12/cit12
ref15/cit15
ref42/cit42
ref41/cit41
ref22/cit22
ref13/cit13
ref33/cit33
ref4/cit4
ref30/cit30
ref1/cit1
ref38/cit38
ref44/cit44
ref7/cit7
References_xml – ident: ref15/cit15
  doi: 10.2147/DDDT.S86621
– ident: ref4/cit4
  doi: 10.1016/S1535-6108(03)00132-6
– ident: ref13/cit13
  doi: 10.1016/j.canlet.2008.11.035
– ident: ref33/cit33
  doi: 10.1254/jphs.09043FP
– ident: ref41/cit41
  doi: 10.1182/blood.V122.21.SCI-31.SCI-31
– ident: ref23/cit23
  doi: 10.1038/nri2808
– ident: ref7/cit7
  doi: 10.1016/j.cell.2008.07.001
– ident: ref32/cit32
  doi: 10.1152/jappl.2001.91.5.1941
– ident: ref16/cit16
  doi: 10.1016/j.immuni.2019.03.024
– ident: ref29/cit29
  doi: 10.1002/smll.201801694
– ident: ref3/cit3
  doi: 10.1016/j.cca.2006.02.027
– ident: ref35/cit35
  doi: 10.1007/s10753-013-9678-z
– ident: ref36/cit36
  doi: 10.1016/j.ccell.2018.03.002
– ident: ref1/cit1
  doi: 10.1182/blood.V128.22.3723.3723
– volume: 134
  start-page: 137
  volume-title: Advances in Immunology
  year: 2017
  ident: ref24/cit24
  contributor:
    fullname: Kelly A.
– ident: ref18/cit18
  doi: 10.1186/s13045-018-0669-2
– ident: ref34/cit34
  doi: 10.1371/journal.pone.0173884
– ident: ref19/cit19
  doi: 10.1126/scitranslmed.aay4860
– ident: ref6/cit6
  doi: 10.1038/nature25501
– ident: ref12/cit12
  doi: 10.1371/journal.pone.0067109
– ident: ref22/cit22
  doi: 10.1182/blood.V116.21.3193.3193
– ident: ref38/cit38
  doi: 10.1016/j.ccr.2011.09.009
– ident: ref44/cit44
  doi: 10.1126/scitranslmed.aaz7287
– ident: ref45/cit45
  doi: 10.1038/nrcardio.2017.206
– ident: ref39/cit39
  doi: 10.1158/0008-5472.CAN-09-2123
– ident: ref10/cit10
  doi: 10.1038/s41392-020-00436-9
– ident: ref42/cit42
  doi: 10.1038/s41573-019-0052-1
– ident: ref27/cit27
  doi: 10.1073/pnas.1901987116
– ident: ref2/cit2
  doi: 10.1074/jbc.M112.443655
– ident: ref14/cit14
  doi: 10.1111/j.1349-7006.2011.01917.x
– ident: ref26/cit26
  doi: 10.1007/s00424-020-02482-2
– ident: ref17/cit17
  doi: 10.3748/wjg.v16.i17.2080
– ident: ref25/cit25
  doi: 10.3389/fimmu.2021.640578
– ident: ref9/cit9
  doi: 10.1126/scisignal.2005189
– ident: ref30/cit30
  doi: 10.1002/adma.201901513
– ident: ref40/cit40
  doi: 10.1038/s41568-021-00413-6
– ident: ref21/cit21
  doi: 10.1126/sciimmunol.aai7911
– ident: ref31/cit31
  doi: 10.1021/acsnano.9b09827
– ident: ref5/cit5
  doi: 10.1038/nature25492
– ident: ref8/cit8
  doi: 10.1038/s41571-020-0403-1
– ident: ref37/cit37
  doi: 10.1182/blood.V122.21.3488.3488
– ident: ref20/cit20
  doi: 10.3390/ijms22094492
– ident: ref28/cit28
  doi: 10.1038/ncomms9785
– ident: ref43/cit43
  doi: 10.7150/thno.17908
– ident: ref11/cit11
  doi: 10.1016/j.immuni.2019.03.024
SSID ssj0057876
Score 2.519721
Snippet Tumor metastasis contributes to the low overall survival of tumor patients, while transforming growth factor-β (TGFβ) has been recognized as a prominently...
SourceID proquest
crossref
pubmed
acs
SourceType Aggregation Database
Index Database
Publisher
StartPage 15388
Title Perfluorotributylamine-Loaded Albumin Nanoparticles Downregulate Platelet-Derived TGFβ to Inhibit Tumor Metastasis
URI http://dx.doi.org/10.1021/acsnano.3c00295
https://www.ncbi.nlm.nih.gov/pubmed/37526429
https://search.proquest.com/docview/2844681031
Volume 17
hasFullText 1
inHoldings 1
isFullTextHit
isPrint
link http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwjV3JTsMwELWgXODAvpRNRuqBS0pjJ258rFpKQRRVopV6i-zEERWQoCxI8Fl8CN_EOEnLUiG45JLEsjxjz3ue0RuEakAJuACSZjCfccMSgTQcBWRFNpRlWkoJnusU9G9Yb2Rdje3xp1j0zww-Mc-El4QijOrU0xkkexEtkWaD6y4Nrfbt9NDVfseKBDIQZEARMxWfuQF0GPKS72HoF2yZx5juWlGdleTShLq05L6epbLuvc4LN_49_XW0WiJN3CpcYwMtqHATrXzRH9xCyUDFwUMWxVHR9-oF3APeGteR8JWP8-v7SYjhBAZqXVbQ4Q7w9rjoYK_wQD_B9EYHhnyGf4YX3fc3nEb4MrybyEmKh9ljFOO-SgXg0GSSbKNR93zY7hllFwZDUEpTQzFJGiLnKrYyhe14tsxl-YDdBkRwn3NLyIAwR7HAD5oQ7CybCCeQVDq-bNIdVAmjUO0hrNXyfO6ZjvQk8EomuNWQJmMA0iSRDq2iGiyXW-6ixM0T5MR0yzV0yzWsotOp7dynQpPj909PprZ1Yd_oZIgIVZQlLoRlS2uxUbOKdgujzwajTRtwIuH7_5vPAVrWTej1TTMhh6iSxpk6AqiSyuPcST8ARQPl2g
link.rule.ids 315,783,787,2774,27090,27938,27939,57072,57122
linkProvider American Chemical Society
linkToHtml http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwlV1LT9wwEB4BPQAH-uKxfRqJQy9ZEjtx4iOCbpeyi0AsErfIThyxAhKUBxL8rP6Q_qaOney2pUKilxzyGDn2OPN9HucbgB2kBEIiSXN4yoXjy0w5kUayolzte77WUlidgvExH5773y-CiwVwZ__CYCMqtFTZJP5vdQFvF8_lMi_6LDGJpGARXgShG5qaBXv7Z7Nvr3E_3uaRkScjmJiL-fxjwESjpPo7Gj0BMW2oGbyE03kj7Q6Tq35Tq37y8Ei_8X_e4hWsdbiT7LWO8hoWdP4GVv9QI3wL1Ykus-umKIu2CtY9OgtedUaFTHVK7GL-NCf4PUai3e2nIwfI4su2nr0mJ-aIjuAcoMk7fGbybfDzB6kLcphfTtW0JpPmpijJWNcSUWk1rdbhfPB1sj90upoMjmSM1Y7mirrSMpdAezKIkkBZkT7kuhmVIhXClyqjPNI8S7MQQ58fUBlliqkoVSHbgKW8yPUWEKOdl4rEi1SikGVyKXxXeZwjZFNURawHO9hdcTenqtimy6kXd30Yd33Ygy-zIYxvW4WOp2_dng1xjLPIpEZkroumijFI-0aZjXk92GzHfm6MhQGiRirePa89n2F5OBmP4tHh8dF7WDHl6c0aNKUfYKkuG_0RQUytPlm__QVS-O5D
linkToPdf http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwlV1LT9wwEB61W6lqD6X0QRdocSUOvWS7sRMnPiKWFMpDK3VX4hbZiSMiaLLKA4n-rP4QfhNjJ7uiVEjtJYc8Rs547JnPY38DsIuQQEgEaQ5PuXA8mSkn1AhW1Fh7rqe1FJan4PSMH8697-f-eX8ozJyFwUbUKKm2SXwzqhdp1jMMuF_xfiGLcsQSk0zyn8IzP3CpqVuwt_9jOf8aE-RdLhmxMgYUK0KfvwQYj5TUf3qkR8JM626iNZivGmp3mVyO2kaNkl8POBz_909ew6s-_iR7ncGswxNdvIGX91gJ30I91VV21ZZV2VXDukGjwafOSSlTnRK7qJ8XBOdlBNz9vjoyQTRfdXXtNZmaKxqEM0GR1_jN7Ft0-5s0JTkqLnKVN2TW_iwrcqobidFpndfvYB4dzPYPnb42gyMZY42juaJjaRGMr13ph4mvLFkfYt6MSpEK4UmVUR5qnqVZgC7Q86kMM8VUmKqAvYdBURb6AxDDoZeKxA1VohBtcim8sXI5x9BNURWyIeyiuuJ-bNWxTZtTN-51GPc6HMKXZTfGi46p4_FXPy-7OcbRZFIkstBlW8forD3D0MbcIWx0_b8SxgIfo0cqNv-tPTvwfDqJ4pOjs-MteGGq1JulaEq3YdBUrf6IsUyjPlnTvQPxOvC9
openUrl ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Perfluorotributylamine-Loaded+Albumin+Nanoparticles+Downregulate+Platelet-Derived+TGF%CE%B2+to+Inhibit+Tumor+Metastasis&rft.jtitle=ACS+nano&rft.au=Luo%2C+Lifeng&rft.au=Zhang%2C+Baoli&rft.au=Tao%2C+Feng&rft.au=Chen%2C+Zhong&rft.date=2023-08-22&rft.eissn=1936-086X&rft.volume=17&rft.issue=16&rft.spage=15388&rft.epage=15400&rft_id=info:doi/10.1021%2Facsnano.3c00295&rft.externalDBID=NO_FULL_TEXT
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=1936-0851&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=1936-0851&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=1936-0851&client=summon