Live Microscopy of Multicellular Spheroids with the Multimodal Near-Infrared Nanoparticles Reveals Differences in Oxygenation Gradients

Assessment of hypoxia, nutrients, metabolite gradients, and other hallmarks of the tumor microenvironment within 3D multicellular spheroid and organoid models represents a challenging analytical task. Here, we report red/near-infrared (NIR) emitting cell staining with O2-sensitive nanoparticles, whi...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:ACS nano Jg. 18; H. 19; S. 12168 - 12186
Hauptverfasser: Debruyne, Angela C., Okkelman, Irina A., Heymans, Nina, Pinheiro, Cláudio, Hendrix, An, Nobis, Max, Borisov, Sergey M., Dmitriev, Ruslan I.
Format: Journal Article
Sprache:Englisch
Veröffentlicht: United States American Chemical Society 14.05.2024
Schlagworte:
ISSN:1936-0851, 1936-086X, 1936-086X
Online-Zugang:Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
Abstract Assessment of hypoxia, nutrients, metabolite gradients, and other hallmarks of the tumor microenvironment within 3D multicellular spheroid and organoid models represents a challenging analytical task. Here, we report red/near-infrared (NIR) emitting cell staining with O2-sensitive nanoparticles, which enable measurements of spheroid oxygenation on a conventional fluorescence microscope. Nanosensor probes, termed “MMIR” (multimodal infrared), incorporate an NIR O2-sensitive metalloporphyrin (PtTPTBPF) and deep red aza-BODIPY reference dyes within a biocompatible polymer shell, allowing for oxygen gradient quantification via fluorescence ratio and phosphorescence lifetime readouts. We optimized staining techniques and evaluated the nanosensor probe characteristics and cytotoxicity. Subsequently, we applied nanosensors to the live spheroid models based on HCT116, DPSCs, and SKOV3 cells, at rest, and treated with drugs affecting cell respiration. We found that the growth medium viscosity, spheroid size, and formation method influenced spheroid oxygenation. Some spheroids produced from HCT116 and dental pulp stem cells exhibited “inverted” oxygenation gradients, with higher core oxygen levels than the periphery. This contrasted with the frequently encountered “normal” gradient of hypoxia toward the core caused by diffusion. Further microscopy analysis of spheroids with an “inverted” gradient demonstrated metabolic stratification of cells within spheroids: thus, autofluorescence FLIM of NAD­(P)H indicated the formation of a glycolytic core and localization of OxPhos-active cells at the periphery. Collectively, we demonstrate a strong potential of NIR-emitting ratiometric nanosensors for advanced microscopy studies targeting live and quantitative real-time monitoring of cell metabolism and hypoxia in complex 3D tissue models.
AbstractList Assessment of hypoxia, nutrients, metabolite gradients, and other hallmarks of the tumor microenvironment within 3D multicellular spheroid and organoid models represents a challenging analytical task. Here, we report red/near-infrared (NIR) emitting cell staining with O2-sensitive nanoparticles, which enable measurements of spheroid oxygenation on a conventional fluorescence microscope. Nanosensor probes, termed “MMIR” (multimodal infrared), incorporate an NIR O2-sensitive metalloporphyrin (PtTPTBPF) and deep red aza-BODIPY reference dyes within a biocompatible polymer shell, allowing for oxygen gradient quantification via fluorescence ratio and phosphorescence lifetime readouts. We optimized staining techniques and evaluated the nanosensor probe characteristics and cytotoxicity. Subsequently, we applied nanosensors to the live spheroid models based on HCT116, DPSCs, and SKOV3 cells, at rest, and treated with drugs affecting cell respiration. We found that the growth medium viscosity, spheroid size, and formation method influenced spheroid oxygenation. Some spheroids produced from HCT116 and dental pulp stem cells exhibited “inverted” oxygenation gradients, with higher core oxygen levels than the periphery. This contrasted with the frequently encountered “normal” gradient of hypoxia toward the core caused by diffusion. Further microscopy analysis of spheroids with an “inverted” gradient demonstrated metabolic stratification of cells within spheroids: thus, autofluorescence FLIM of NAD(P)H indicated the formation of a glycolytic core and localization of OxPhos-active cells at the periphery. Collectively, we demonstrate a strong potential of NIR-emitting ratiometric nanosensors for advanced microscopy studies targeting live and quantitative real-time monitoring of cell metabolism and hypoxia in complex 3D tissue models.
Assessment of hypoxia, nutrients, metabolite gradients, and other hallmarks of the tumor microenvironment within 3D multicellular spheroid and organoid models represents a challenging analytical task. Here, we report red/near-infrared (NIR) emitting cell staining with O2-sensitive nanoparticles, which enable measurements of spheroid oxygenation on a conventional fluorescence microscope. Nanosensor probes, termed "MMIR" (multimodal infrared), incorporate an NIR O2-sensitive metalloporphyrin (PtTPTBPF) and deep red aza-BODIPY reference dyes within a biocompatible polymer shell, allowing for oxygen gradient quantification via fluorescence ratio and phosphorescence lifetime readouts. We optimized staining techniques and evaluated the nanosensor probe characteristics and cytotoxicity. Subsequently, we applied nanosensors to the live spheroid models based on HCT116, DPSCs, and SKOV3 cells, at rest, and treated with drugs affecting cell respiration. We found that the growth medium viscosity, spheroid size, and formation method influenced spheroid oxygenation. Some spheroids produced from HCT116 and dental pulp stem cells exhibited "inverted" oxygenation gradients, with higher core oxygen levels than the periphery. This contrasted with the frequently encountered "normal" gradient of hypoxia toward the core caused by diffusion. Further microscopy analysis of spheroids with an "inverted" gradient demonstrated metabolic stratification of cells within spheroids: thus, autofluorescence FLIM of NAD(P)H indicated the formation of a glycolytic core and localization of OxPhos-active cells at the periphery. Collectively, we demonstrate a strong potential of NIR-emitting ratiometric nanosensors for advanced microscopy studies targeting live and quantitative real-time monitoring of cell metabolism and hypoxia in complex 3D tissue models.Assessment of hypoxia, nutrients, metabolite gradients, and other hallmarks of the tumor microenvironment within 3D multicellular spheroid and organoid models represents a challenging analytical task. Here, we report red/near-infrared (NIR) emitting cell staining with O2-sensitive nanoparticles, which enable measurements of spheroid oxygenation on a conventional fluorescence microscope. Nanosensor probes, termed "MMIR" (multimodal infrared), incorporate an NIR O2-sensitive metalloporphyrin (PtTPTBPF) and deep red aza-BODIPY reference dyes within a biocompatible polymer shell, allowing for oxygen gradient quantification via fluorescence ratio and phosphorescence lifetime readouts. We optimized staining techniques and evaluated the nanosensor probe characteristics and cytotoxicity. Subsequently, we applied nanosensors to the live spheroid models based on HCT116, DPSCs, and SKOV3 cells, at rest, and treated with drugs affecting cell respiration. We found that the growth medium viscosity, spheroid size, and formation method influenced spheroid oxygenation. Some spheroids produced from HCT116 and dental pulp stem cells exhibited "inverted" oxygenation gradients, with higher core oxygen levels than the periphery. This contrasted with the frequently encountered "normal" gradient of hypoxia toward the core caused by diffusion. Further microscopy analysis of spheroids with an "inverted" gradient demonstrated metabolic stratification of cells within spheroids: thus, autofluorescence FLIM of NAD(P)H indicated the formation of a glycolytic core and localization of OxPhos-active cells at the periphery. Collectively, we demonstrate a strong potential of NIR-emitting ratiometric nanosensors for advanced microscopy studies targeting live and quantitative real-time monitoring of cell metabolism and hypoxia in complex 3D tissue models.
Assessment of hypoxia, nutrients, metabolite gradients, and other hallmarks of the tumor microenvironment within 3D multicellular spheroid and organoid models represents a challenging analytical task. Here, we report red/near-infrared (NIR) emitting cell staining with O2-sensitive nanoparticles, which enable measurements of spheroid oxygenation on a conventional fluorescence microscope. Nanosensor probes, termed “MMIR” (multimodal infrared), incorporate an NIR O2-sensitive metalloporphyrin (PtTPTBPF) and deep red aza-BODIPY reference dyes within a biocompatible polymer shell, allowing for oxygen gradient quantification via fluorescence ratio and phosphorescence lifetime readouts. We optimized staining techniques and evaluated the nanosensor probe characteristics and cytotoxicity. Subsequently, we applied nanosensors to the live spheroid models based on HCT116, DPSCs, and SKOV3 cells, at rest, and treated with drugs affecting cell respiration. We found that the growth medium viscosity, spheroid size, and formation method influenced spheroid oxygenation. Some spheroids produced from HCT116 and dental pulp stem cells exhibited “inverted” oxygenation gradients, with higher core oxygen levels than the periphery. This contrasted with the frequently encountered “normal” gradient of hypoxia toward the core caused by diffusion. Further microscopy analysis of spheroids with an “inverted” gradient demonstrated metabolic stratification of cells within spheroids: thus, autofluorescence FLIM of NAD­(P)H indicated the formation of a glycolytic core and localization of OxPhos-active cells at the periphery. Collectively, we demonstrate a strong potential of NIR-emitting ratiometric nanosensors for advanced microscopy studies targeting live and quantitative real-time monitoring of cell metabolism and hypoxia in complex 3D tissue models.
Assessment of hypoxia, nutrients, metabolite gradients, and other hallmarks of the tumor microenvironment within 3D multicellular spheroid and organoid models represents a challenging analytical task. Here, we report red/near-infrared (NIR) emitting cell staining with O -sensitive nanoparticles, which enable measurements of spheroid oxygenation on a conventional fluorescence microscope. Nanosensor probes, termed "MMIR" (multimodal infrared), incorporate an NIR O -sensitive metalloporphyrin (PtTPTBPF) and deep red aza-BODIPY reference dyes within a biocompatible polymer shell, allowing for oxygen gradient quantification via fluorescence ratio and phosphorescence lifetime readouts. We optimized staining techniques and evaluated the nanosensor probe characteristics and cytotoxicity. Subsequently, we applied nanosensors to the live spheroid models based on HCT116, DPSCs, and SKOV3 cells, at rest, and treated with drugs affecting cell respiration. We found that the growth medium viscosity, spheroid size, and formation method influenced spheroid oxygenation. Some spheroids produced from HCT116 and dental pulp stem cells exhibited "inverted" oxygenation gradients, with higher core oxygen levels than the periphery. This contrasted with the frequently encountered "normal" gradient of hypoxia toward the core caused by diffusion. Further microscopy analysis of spheroids with an "inverted" gradient demonstrated metabolic stratification of cells within spheroids: thus, autofluorescence FLIM of NAD(P)H indicated the formation of a glycolytic core and localization of OxPhos-active cells at the periphery. Collectively, we demonstrate a strong potential of NIR-emitting ratiometric nanosensors for advanced microscopy studies targeting live and quantitative real-time monitoring of cell metabolism and hypoxia in complex 3D tissue models.
Author Heymans, Nina
Nobis, Max
Borisov, Sergey M.
Pinheiro, Cláudio
Hendrix, An
Debruyne, Angela C.
Dmitriev, Ruslan I.
Okkelman, Irina A.
AuthorAffiliation Ghent University
Institute of Analytical Chemistry and Food Chemistry
Intravital Imaging Expertise Center, VIB Center for Cancer Biology
Cancer Research Institute Ghent (CRIG)
Tissue Engineering and Biomaterials Group, Department of Human Structure and Repair, Faculty of Medicine and Health Sciences
Laboratory of Experimental Cancer Research, Department of Human Structure and Repair
Ghent Light Microscopy Core
AuthorAffiliation_xml – name: Tissue Engineering and Biomaterials Group, Department of Human Structure and Repair, Faculty of Medicine and Health Sciences
– name: Cancer Research Institute Ghent (CRIG)
– name: Ghent University
– name: Laboratory of Experimental Cancer Research, Department of Human Structure and Repair
– name: Ghent Light Microscopy Core
– name: Institute of Analytical Chemistry and Food Chemistry
– name: Intravital Imaging Expertise Center, VIB Center for Cancer Biology
Author_xml – sequence: 1
  givenname: Angela C.
  surname: Debruyne
  fullname: Debruyne, Angela C.
  organization: Tissue Engineering and Biomaterials Group, Department of Human Structure and Repair, Faculty of Medicine and Health Sciences
– sequence: 2
  givenname: Irina A.
  surname: Okkelman
  fullname: Okkelman, Irina A.
  organization: Ghent University
– sequence: 3
  givenname: Nina
  surname: Heymans
  fullname: Heymans, Nina
  organization: Tissue Engineering and Biomaterials Group, Department of Human Structure and Repair, Faculty of Medicine and Health Sciences
– sequence: 4
  givenname: Cláudio
  surname: Pinheiro
  fullname: Pinheiro, Cláudio
  organization: Cancer Research Institute Ghent (CRIG)
– sequence: 5
  givenname: An
  surname: Hendrix
  fullname: Hendrix, An
  organization: Cancer Research Institute Ghent (CRIG)
– sequence: 6
  givenname: Max
  orcidid: 0000-0002-1861-1390
  surname: Nobis
  fullname: Nobis, Max
  organization: Intravital Imaging Expertise Center, VIB Center for Cancer Biology
– sequence: 7
  givenname: Sergey M.
  orcidid: 0000-0001-9318-8273
  surname: Borisov
  fullname: Borisov, Sergey M.
  email: sergey.borisov@tugraz.at
  organization: Institute of Analytical Chemistry and Food Chemistry
– sequence: 8
  givenname: Ruslan I.
  orcidid: 0000-0002-0347-8718
  surname: Dmitriev
  fullname: Dmitriev, Ruslan I.
  email: Ruslan.dmitriev@ugent.be
  organization: Ghent University
BackLink https://www.ncbi.nlm.nih.gov/pubmed/38687976$$D View this record in MEDLINE/PubMed
BookMark eNp9kVtvEzEQhS1URC_wzBvyIxLa1l7vzU8IFSiV0lbiIvFmzdrjxtXGDvZu2vwC_jYOCREgwZNHnu_MGZ05Jgc-eCTkOWennJX8DHTy4MOp0LyshXxEjrgUTcG65uvBvq75ITlO6Y6xuu3a5gk5FF3TtbJtjsj3mVshvXI6hqTDck2DpVfTMDqNwzANEOmn5RxjcCbRezfO6TjHLbAIBgZ6jRCLS28jRDT0Ou-yhJjVAyb6EVcIQ6JvnbUY0ev85zy9eVjfoofRBU8vIhiHfkxPyWObWXy2e0_Il_fvPp9_KGY3F5fnb2YFVIKNhRG2aVnZc8ZEVzcWEIy0pWBGlrJF2YPsy7IqZVVLW5uWddZoZoVm0AN2IE7I6-3c5dQv0OjsHWFQy-gWENcqgFN_drybq9uwUpxnz1KyPOHlbkIM3yZMo1q4tEkLPIYpKcEq2fJWVDyjL34327v8ij8DZ1tgE3-KaPcIZ2pzYLU7sNodOCvqvxTajT-zzNu64T-6V1tdbqi7MEWfU_4n_QPnHb9y
CitedBy_id crossref_primary_10_3390_cells13181536
crossref_primary_10_1021_acsnano_5c12854
crossref_primary_10_3389_fbioe_2025_1516482
crossref_primary_10_1021_acssensors_5c00180
crossref_primary_10_1177_20417314251345000
crossref_primary_10_1038_s41377_025_01949_0
crossref_primary_10_1038_s41598_025_88357_x
crossref_primary_10_1016_j_ccr_2025_217160
crossref_primary_10_1016_j_jorganchem_2024_123349
crossref_primary_10_1021_acsanm_5c01056
crossref_primary_10_1021_acs_biomac_4c01627
crossref_primary_10_1002_chem_202404188
crossref_primary_10_1021_cbmi_5c00021
Cites_doi 10.1007/978-3-319-26666-4_10
10.1039/B204317C
10.1152/ajpheart.00323.2002
10.1007/s10911-016-9359-2
10.1002/pro.3993
10.1101/2022.04.14.488402
10.1007/s40820-021-00653-z
10.1039/c3cs60131e
10.1021/nn200807g
10.1007/s00018-018-2840-x
10.1186/s12935-021-01853-8
10.1016/j.redox.2019.101420
10.1021/ja052947c
10.1021/ac900881z
10.1016/j.actbio.2019.02.014
10.1039/C4TC00983E
10.3791/63403
10.1126/sciimmunol.aal2861
10.1186/s13046-020-01583-1
10.3390/cancers12113324
10.1016/j.actbio.2022.03.010
10.1002/anie.201410646
10.1016/j.ceb.2009.11.015
10.2967/jnumed.107.045914
10.1038/cddis.2017.247
10.1021/acsnano.5b00771
10.1021/ja202902d
10.1117/1.JBO.25.7.071203
10.1021/acs.analchem.2c05126
10.1212/WNL.54.2.362
10.1016/j.freeradbiomed.2020.12.243
10.1039/D2LC00705C
10.1038/s41392-022-01080-1
10.1007/s10544-017-0200-5
10.1088/2050-6120/3/3/034001
10.1113/JP273309
10.1038/ncomms6262
10.1186/1471-2180-13-9
10.1002/bit.26845
10.1039/C6CS00092D
10.1038/nri.2017.103
10.1007/978-1-4615-3428-0_20
10.1016/j.biomaterials.2019.05.007
10.1038/bjc.1986.58
10.1039/c2an35907c
10.1126/science.aaf4405
10.1016/j.freeradbiomed.2005.02.010
10.3390/ijms22157954
10.1016/j.biomaterials.2022.121881
10.1002/adfm.201201387
10.1016/j.talanta.2009.05.041
10.1002/anie.200805894
10.1016/j.biomaterials.2013.08.065
10.1186/1476-4598-2-23
10.18632/oncotarget.7659
10.1080/05704928.2017.1363053
10.1186/1471-2407-11-167
10.1016/j.jphotochem.2008.10.003
10.1021/ja047649e
10.1126/sciadv.aau7314
10.1038/s41598-020-69026-7
10.1186/s13046-017-0570-9
10.1371/journal.pone.0204269
10.1038/s41586-022-05394-6
10.1016/S0006-3495(84)84030-8
10.1038/s41592-021-01291-4
10.3390/ijms21186806
10.1016/j.freeradbiomed.2016.12.004
10.1242/jcs.254763
10.1016/j.freeradbiomed.2016.08.010
10.1016/j.addr.2023.115081
10.3389/fendo.2021.742215
10.3389/fphys.2021.676782
10.1158/1078-0432.CCR-18-3590
10.1002/adfm.201400647
10.1016/S0002-9440(10)63058-1
10.1021/acssensors.5b00315
10.1111/febs.13270
10.1016/j.bios.2022.114917
10.3390/ijms20225565
10.1038/s41598-023-30403-7
10.1039/c8pp00122g
10.1038/s41567-022-01676-y
10.1002/jbio.202000472
10.1016/j.jneumeth.2013.04.005
10.1126/science.1126863
10.15252/embj.201592775
10.1016/j.biomaterials.2017.08.043
10.1038/s41598-018-30329-5
10.1016/j.febslet.2014.11.038
10.3390/antiox9060516
10.1146/annurev-anchem-061020-111458
10.1038/s44319-024-00089-7
10.1002/smll.202002494
10.1038/s41378-022-00442-7
10.1002/adom.202202720
10.1016/j.bbagen.2015.05.001
10.1016/j.ccell.2022.09.017
10.1038/s42255-020-00299-y
10.1021/ja105937q
10.1016/j.measurement.2022.112275
10.1039/c3ob42554a
10.1016/j.biomaterials.2011.11.048
10.1016/j.semcdb.2022.09.005
10.1016/j.pharmthera.2022.108186
10.1039/c1ib00050k
10.1007/s00018-014-1673-5
10.1016/j.tranon.2020.100845
ContentType Journal Article
Copyright 2024 The Authors. Published by American Chemical Society
2024 The Authors. Published by American Chemical Society 2024 The Authors
Copyright_xml – notice: 2024 The Authors. Published by American Chemical Society
– notice: 2024 The Authors. Published by American Chemical Society 2024 The Authors
DBID AAYXX
CITATION
CGR
CUY
CVF
ECM
EIF
NPM
7X8
5PM
DOI 10.1021/acsnano.3c12539
DatabaseName CrossRef
Medline
MEDLINE
MEDLINE (Ovid)
MEDLINE
MEDLINE
PubMed
MEDLINE - Academic
PubMed Central (Full Participant titles)
DatabaseTitle CrossRef
MEDLINE
Medline Complete
MEDLINE with Full Text
PubMed
MEDLINE (Ovid)
MEDLINE - Academic
DatabaseTitleList
MEDLINE - Academic

MEDLINE
Database_xml – sequence: 1
  dbid: NPM
  name: PubMed
  url: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed
  sourceTypes: Index Database
– sequence: 2
  dbid: 7X8
  name: MEDLINE - Academic
  url: https://search.proquest.com/medline
  sourceTypes: Aggregation Database
DeliveryMethod fulltext_linktorsrc
Discipline Engineering
EISSN 1936-086X
EndPage 12186
ExternalDocumentID PMC11100290
38687976
10_1021_acsnano_3c12539
b718913975
Genre Research Support, Non-U.S. Gov't
Journal Article
GroupedDBID ---
.K2
23M
4.4
55A
5GY
5VS
6J9
7~N
AABXI
ABFRP
ABJNI
ABMVS
ABQRX
ABUCX
ACBEA
ACGFO
ACGFS
ACS
ADHLV
AEESW
AENEX
AFEFF
AHGAQ
ALMA_UNASSIGNED_HOLDINGS
AQSVZ
BAANH
CS3
EBS
ED~
F5P
GGK
GNL
IH9
IHE
JG~
P2P
RNS
ROL
UI2
VF5
VG9
W1F
XKZ
YZZ
AAHBH
AAYXX
ABBLG
ABLBI
ADHGD
CITATION
CUPRZ
CGR
CUY
CVF
ECM
EIF
NPM
7X8
5PM
ID FETCH-LOGICAL-a430t-d3f6702b1003856faead9f230d9297e9ba9b22429459f5d708fdc0f3c0abae8a3
IEDL.DBID ACS
ISICitedReferencesCount 21
ISICitedReferencesURI http://www.webofscience.com/api/gateway?GWVersion=2&SrcApp=Summon&SrcAuth=ProQuest&DestLinkType=CitingArticles&DestApp=WOS_CPL&KeyUT=001228077200001&url=https%3A%2F%2Fcvtisr.summon.serialssolutions.com%2F%23%21%2Fsearch%3Fho%3Df%26include.ft.matches%3Dt%26l%3Dnull%26q%3D
ISSN 1936-0851
1936-086X
IngestDate Tue Sep 30 17:08:57 EDT 2025
Thu Jul 10 22:04:28 EDT 2025
Mon Jul 21 05:28:33 EDT 2025
Sat Nov 29 04:16:23 EST 2025
Tue Nov 18 21:31:37 EST 2025
Wed May 22 06:53:50 EDT 2024
IsDoiOpenAccess true
IsOpenAccess true
IsPeerReviewed true
IsScholarly true
Issue 19
Keywords hypoxia
nanoparticles
cancer
FLIM
oxygenation
fluorescence microscopy
multicellular spheroids
Language English
License https://creativecommons.org/licenses/by/4.0
Permits the broadest form of re-use including for commercial purposes, provided that author attribution and integrity are maintained (https://creativecommons.org/licenses/by/4.0/).
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-a430t-d3f6702b1003856faead9f230d9297e9ba9b22429459f5d708fdc0f3c0abae8a3
Notes ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 23
ORCID 0000-0002-0347-8718
0000-0002-1861-1390
0000-0001-9318-8273
OpenAccessLink https://pubmed.ncbi.nlm.nih.gov/PMC11100290
PMID 38687976
PQID 3049717341
PQPubID 23479
PageCount 19
ParticipantIDs pubmedcentral_primary_oai_pubmedcentral_nih_gov_11100290
proquest_miscellaneous_3049717341
pubmed_primary_38687976
crossref_primary_10_1021_acsnano_3c12539
crossref_citationtrail_10_1021_acsnano_3c12539
acs_journals_10_1021_acsnano_3c12539
PublicationCentury 2000
PublicationDate 2024-05-14
PublicationDateYYYYMMDD 2024-05-14
PublicationDate_xml – month: 05
  year: 2024
  text: 2024-05-14
  day: 14
PublicationDecade 2020
PublicationPlace United States
PublicationPlace_xml – name: United States
PublicationTitle ACS nano
PublicationTitleAlternate ACS Nano
PublicationYear 2024
Publisher American Chemical Society
Publisher_xml – name: American Chemical Society
References ref99/cit99
ref3/cit3
ref81/cit81
ref16/cit16
ref52/cit52
Papkovsky D. B. (ref45/cit45) 2018
ref114/cit114
ref115/cit115
ref116/cit116
ref110/cit110
ref111/cit111
ref2/cit2
ref112/cit112
ref77/cit77
ref113/cit113
ref71/cit71
ref117/cit117
ref20/cit20
ref48/cit48
ref74/cit74
ref10/cit10
ref35/cit35
ref89/cit89
ref19/cit19
ref93/cit93
ref42/cit42
ref96/cit96
ref107/cit107
ref109/cit109
ref13/cit13
ref105/cit105
ref61/cit61
ref67/cit67
ref38/cit38
ref90/cit90
ref64/cit64
ref54/cit54
ref6/cit6
ref18/cit18
ref65/cit65
ref97/cit97
ref101/cit101
ref11/cit11
ref102/cit102
ref29/cit29
ref76/cit76
ref86/cit86
ref32/cit32
ref39/cit39
ref5/cit5
ref43/cit43
ref80/cit80
ref28/cit28
ref91/cit91
Sutherland R. M. (ref24/cit24) 1986; 46
ref12/cit12
ref66/cit66
ref33/cit33
ref87/cit87
ref106/cit106
ref44/cit44
ref70/cit70
ref98/cit98
ref9/cit9
ref27/cit27
ref63/cit63
ref56/cit56
ref92/cit92
Casciari J. J. (ref23/cit23) 1988; 48
ref8/cit8
ref31/cit31
ref59/cit59
ref85/cit85
ref34/cit34
ref37/cit37
Filatov M. A. (ref55/cit55) 2018
ref60/cit60
ref88/cit88
Freyer J. P. (ref22/cit22) 1980; 40
ref82/cit82
ref53/cit53
Dmitriev R. I. (ref62/cit62) 2015; 9328
ref21/cit21
ref46/cit46
ref49/cit49
ref75/cit75
ref50/cit50
ref78/cit78
ref36/cit36
ref83/cit83
ref79/cit79
ref100/cit100
ref25/cit25
ref103/cit103
ref72/cit72
ref14/cit14
ref57/cit57
ref51/cit51
ref40/cit40
ref68/cit68
ref94/cit94
ref26/cit26
ref73/cit73
Hall E. J. (ref17/cit17) 2006; 6
ref69/cit69
ref15/cit15
ref41/cit41
ref58/cit58
ref95/cit95
ref108/cit108
ref104/cit104
ref4/cit4
ref30/cit30
ref47/cit47
ref84/cit84
ref1/cit1
ref7/cit7
References_xml – ident: ref21/cit21
  doi: 10.1007/978-3-319-26666-4_10
– ident: ref73/cit73
  doi: 10.1039/B204317C
– ident: ref114/cit114
  doi: 10.1152/ajpheart.00323.2002
– ident: ref82/cit82
  doi: 10.1007/s10911-016-9359-2
– ident: ref117/cit117
  doi: 10.1002/pro.3993
– ident: ref65/cit65
  doi: 10.1101/2022.04.14.488402
– ident: ref103/cit103
  doi: 10.1007/s40820-021-00653-z
– ident: ref51/cit51
  doi: 10.1039/c3cs60131e
– ident: ref56/cit56
  doi: 10.1021/nn200807g
– ident: ref42/cit42
  doi: 10.1007/s00018-018-2840-x
– ident: ref86/cit86
  doi: 10.1186/s12935-021-01853-8
– ident: ref89/cit89
  doi: 10.1016/j.redox.2019.101420
– ident: ref53/cit53
  doi: 10.1021/ja052947c
– ident: ref34/cit34
  doi: 10.1021/ac900881z
– ident: ref78/cit78
  doi: 10.1016/j.actbio.2019.02.014
– ident: ref111/cit111
  doi: 10.1039/C4TC00983E
– ident: ref63/cit63
  doi: 10.3791/63403
– ident: ref13/cit13
  doi: 10.1126/sciimmunol.aal2861
– ident: ref18/cit18
  doi: 10.1186/s13046-020-01583-1
– ident: ref85/cit85
  doi: 10.3390/cancers12113324
– ident: ref77/cit77
  doi: 10.1016/j.actbio.2022.03.010
– ident: ref54/cit54
  doi: 10.1002/anie.201410646
– ident: ref4/cit4
  doi: 10.1016/j.ceb.2009.11.015
– ident: ref28/cit28
  doi: 10.2967/jnumed.107.045914
– ident: ref46/cit46
  doi: 10.1038/cddis.2017.247
– ident: ref43/cit43
  doi: 10.1021/acsnano.5b00771
– ident: ref67/cit67
  doi: 10.1021/ja202902d
– ident: ref99/cit99
  doi: 10.1117/1.JBO.25.7.071203
– ident: ref102/cit102
  doi: 10.1021/acs.analchem.2c05126
– ident: ref5/cit5
  doi: 10.1212/WNL.54.2.362
– ident: ref1/cit1
  doi: 10.1016/j.freeradbiomed.2020.12.243
– ident: ref32/cit32
  doi: 10.1039/D2LC00705C
– ident: ref7/cit7
  doi: 10.1038/s41392-022-01080-1
– ident: ref90/cit90
  doi: 10.1007/s10544-017-0200-5
– ident: ref75/cit75
  doi: 10.1088/2050-6120/3/3/034001
– ident: ref15/cit15
  doi: 10.1113/JP273309
– ident: ref68/cit68
  doi: 10.1038/ncomms6262
– ident: ref93/cit93
  doi: 10.1186/1471-2180-13-9
– ident: ref20/cit20
  doi: 10.1002/bit.26845
– volume: 46
  start-page: 5320
  issue: 10
  year: 1986
  ident: ref24/cit24
  publication-title: Cancer Res.
– ident: ref57/cit57
  doi: 10.1021/acsnano.5b00771
– ident: ref52/cit52
  doi: 10.1039/C6CS00092D
– ident: ref10/cit10
  doi: 10.1038/nri.2017.103
– ident: ref50/cit50
  doi: 10.1007/978-1-4615-3428-0_20
– ident: ref70/cit70
  doi: 10.1016/j.biomaterials.2019.05.007
– ident: ref94/cit94
  doi: 10.1038/bjc.1986.58
– ident: ref69/cit69
  doi: 10.1039/c2an35907c
– ident: ref88/cit88
  doi: 10.1126/science.aaf4405
– ident: ref6/cit6
  doi: 10.1016/j.freeradbiomed.2005.02.010
– ident: ref11/cit11
  doi: 10.3390/ijms22157954
– ident: ref110/cit110
  doi: 10.1016/j.biomaterials.2022.121881
– ident: ref47/cit47
  doi: 10.1002/adfm.201201387
– ident: ref71/cit71
  doi: 10.1016/j.talanta.2009.05.041
– ident: ref58/cit58
  doi: 10.1002/anie.200805894
– ident: ref40/cit40
  doi: 10.1016/j.biomaterials.2013.08.065
– ident: ref3/cit3
  doi: 10.1186/1476-4598-2-23
– start-page: 50
  volume-title: Evolution of Cell-Penetrating Phosphorescent O2 Probes
  year: 2018
  ident: ref45/cit45
– ident: ref91/cit91
  doi: 10.18632/oncotarget.7659
– ident: ref95/cit95
  doi: 10.1080/05704928.2017.1363053
– ident: ref29/cit29
  doi: 10.1186/1471-2407-11-167
– ident: ref72/cit72
  doi: 10.1016/j.jphotochem.2008.10.003
– ident: ref74/cit74
  doi: 10.1021/ja047649e
– ident: ref80/cit80
  doi: 10.1126/sciadv.aau7314
– ident: ref87/cit87
  doi: 10.1038/s41598-020-69026-7
– ident: ref25/cit25
  doi: 10.1186/s13046-017-0570-9
– ident: ref92/cit92
  doi: 10.1371/journal.pone.0204269
– ident: ref84/cit84
  doi: 10.1038/s41586-022-05394-6
– ident: ref27/cit27
  doi: 10.1016/S0006-3495(84)84030-8
– ident: ref79/cit79
  doi: 10.1038/s41592-021-01291-4
– ident: ref19/cit19
  doi: 10.3390/ijms21186806
– ident: ref2/cit2
  doi: 10.1016/j.freeradbiomed.2016.12.004
– ident: ref104/cit104
  doi: 10.1242/jcs.254763
– ident: ref96/cit96
  doi: 10.1016/j.freeradbiomed.2016.08.010
– ident: ref97/cit97
  doi: 10.1016/j.addr.2023.115081
– ident: ref14/cit14
  doi: 10.3389/fendo.2021.742215
– ident: ref9/cit9
  doi: 10.3389/fphys.2021.676782
– ident: ref108/cit108
  doi: 10.1158/1078-0432.CCR-18-3590
– ident: ref60/cit60
  doi: 10.1002/adfm.201400647
– ident: ref76/cit76
  doi: 10.1016/S0002-9440(10)63058-1
– ident: ref113/cit113
  doi: 10.1021/acssensors.5b00315
– ident: ref12/cit12
  doi: 10.1111/febs.13270
– ident: ref30/cit30
  doi: 10.1016/j.bios.2022.114917
– ident: ref116/cit116
  doi: 10.3390/ijms20225565
– ident: ref100/cit100
  doi: 10.1038/s41598-023-30403-7
– ident: ref39/cit39
  doi: 10.1039/c8pp00122g
– volume: 40
  start-page: 3956
  issue: 11
  year: 1980
  ident: ref22/cit22
  publication-title: Cancer Res.
– ident: ref83/cit83
  doi: 10.1038/s41567-022-01676-y
– ident: ref101/cit101
  doi: 10.1002/jbio.202000472
– ident: ref64/cit64
  doi: 10.1016/j.jneumeth.2013.04.005
– ident: ref98/cit98
  doi: 10.1126/science.1126863
– ident: ref37/cit37
  doi: 10.15252/embj.201592775
– ident: ref44/cit44
  doi: 10.1016/j.biomaterials.2017.08.043
– ident: ref38/cit38
  doi: 10.1038/s41598-018-30329-5
– ident: ref112/cit112
  doi: 10.1016/j.febslet.2014.11.038
– ident: ref31/cit31
  doi: 10.3390/antiox9060516
– ident: ref41/cit41
  doi: 10.1146/annurev-anchem-061020-111458
– ident: ref26/cit26
  doi: 10.1038/s44319-024-00089-7
– ident: ref59/cit59
  doi: 10.1002/smll.202002494
– ident: ref33/cit33
  doi: 10.1038/s41378-022-00442-7
– volume: 9328
  volume-title: Progress in Biomedical Optics and Imaging - Proceedings of SPIE
  year: 2015
  ident: ref62/cit62
– ident: ref115/cit115
  doi: 10.1002/adom.202202720
– volume-title: Applications of Quenched Phosphorescence Detection of Molecular Oxygen in Life Sciences
  year: 2018
  ident: ref55/cit55
– ident: ref105/cit105
  doi: 10.1016/j.bbagen.2015.05.001
– ident: ref107/cit107
  doi: 10.1016/j.ccell.2022.09.017
– ident: ref81/cit81
  doi: 10.1038/s42255-020-00299-y
– ident: ref36/cit36
  doi: 10.1021/ja105937q
– ident: ref48/cit48
  doi: 10.1016/j.measurement.2022.112275
– ident: ref66/cit66
  doi: 10.1039/c3ob42554a
– ident: ref49/cit49
  doi: 10.1016/j.biomaterials.2011.11.048
– volume: 48
  start-page: 3905
  issue: 14
  year: 1988
  ident: ref23/cit23
  publication-title: Cancer Res.
– ident: ref109/cit109
  doi: 10.1016/j.semcdb.2022.09.005
– volume: 6
  volume-title: Radiobiology for the Radiologist
  year: 2006
  ident: ref17/cit17
– ident: ref8/cit8
  doi: 10.1016/j.pharmthera.2022.108186
– ident: ref35/cit35
  doi: 10.1039/c1ib00050k
– ident: ref61/cit61
  doi: 10.1007/s00018-014-1673-5
– ident: ref106/cit106
  doi: 10.1016/j.biomaterials.2019.05.007
– ident: ref16/cit16
  doi: 10.1016/j.tranon.2020.100845
SSID ssj0057876
Score 2.5434463
Snippet Assessment of hypoxia, nutrients, metabolite gradients, and other hallmarks of the tumor microenvironment within 3D multicellular spheroid and organoid models...
Assessment of hypoxia, nutrients, metabolite gradients, and other hallmarks of the tumor microenvironment within 3D multicellular spheroid and organoid models...
SourceID pubmedcentral
proquest
pubmed
crossref
acs
SourceType Open Access Repository
Aggregation Database
Index Database
Enrichment Source
Publisher
StartPage 12168
SubjectTerms Humans
Infrared Rays
Metalloporphyrins - chemistry
Metalloporphyrins - pharmacology
Microscopy, Fluorescence
Nanoparticles - chemistry
Oxygen - chemistry
Oxygen - metabolism
Spheroids, Cellular - drug effects
Spheroids, Cellular - metabolism
Title Live Microscopy of Multicellular Spheroids with the Multimodal Near-Infrared Nanoparticles Reveals Differences in Oxygenation Gradients
URI http://dx.doi.org/10.1021/acsnano.3c12539
https://www.ncbi.nlm.nih.gov/pubmed/38687976
https://www.proquest.com/docview/3049717341
https://pubmed.ncbi.nlm.nih.gov/PMC11100290
Volume 18
WOSCitedRecordID wos001228077200001&url=https%3A%2F%2Fcvtisr.summon.serialssolutions.com%2F%23%21%2Fsearch%3Fho%3Df%26include.ft.matches%3Dt%26l%3Dnull%26q%3D
hasFullText 1
inHoldings 1
isFullTextHit
isPrint
journalDatabaseRights – providerCode: PRVABC
  databaseName: American Chemical Society Journals
  customDbUrl:
  eissn: 1936-086X
  dateEnd: 99991231
  omitProxy: false
  ssIdentifier: ssj0057876
  issn: 1936-0851
  databaseCode: ACS
  dateStart: 20070801
  isFulltext: true
  titleUrlDefault: https://pubs.acs.org/action/showPublications?display=journals
  providerName: American Chemical Society
link http://cvtisr.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwlV1LT9wwEB4VyqE9lAKl3T6QkThwCSSxN7GPCEqLBFvEQ9pb5PghVgKn2iyo_IL-7c4k2S0LQmrPsa3E_jzzjWfyGWALvajSJe9HiU9MJLQRkUZWHgmpU2ulE8bJ5rKJfDCQw6E6_SsW_TiDnya72tRBh2qHG_TFXC3AyxRJLoF5b_98anQJd1mbQMYAGVnETMXnyQDkhkw974aecMvHJZIPfM7h8n-87Vt40xFLttciYQVeuLAKrx_IDa7B72M0beyESvDoZ5R7VnnW_IBLp_dUjsrOSWSgGtma0fksQ3LYNripLI49wF0RHQU_pqJ1hnYZA-6uro6duTuknDU76C5cQfPDRoH9-HWPCG1Wn30bN-Vlk_odXB5-vdj_HnUXMURa8HgSWe6zPE7LpMkjZl4j_JTH4MUiucqdKrUqkQqkSvSV79s8lt6a2HMT61I7qfk6LIYquA_A0M4jh8p5ZjCQUQ6jG6GlLm2WybxEZPRgC6ew6DZSXTQ58jQpunktunntwc50-QrTiZnTnRrXz3fYnnX42ep4PN90c4qHAvcaLYEOrrqtC0pJUtWCSHrwvsXHbDAu8QuQ2_VAziFn1oB0vOefhNFVo-edkGxfquKP__btn-BVisyKShgS8RkWJ-Nb9wWWzN1kVI83YCEfyo1mc_wB39wPfQ
linkProvider American Chemical Society
linkToHtml http://cvtisr.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwlV1NT9wwEB1RWqn0QOkHsLSlrsShl9Ak9ib2EdFSEMu2KlTiFjn-ECuBg9YLKr-gf7tjJ7uwRUjtNXGsxHmeeeMZPwNsoRcVsqb9JLOZSphULJHIyhPGZa41N0wZHg-bKIdDfnoqvi9AOt0Lgy_hsScfk_i36gLZJ7zmpGu2qUKXTMUjeNxH5xqQvbN7PLW9AX5Fm0fGOBnJxEzM514HwRspP--N7lHMvysl77ievef__9IrsNzRTLLT4uIFLBj3Ep7dER98Bb8HaOjIUSjIC1tTbkhjSdyOG9byQ3EqOQ6SA81IexJWawlSxbbBRaOx7yHOkeTA2XEoYSdopTH87qrsyA9zjQTUk8_d8StojMjIkW-_bhCvEQvk6zgWm038a_i59-Vkdz_pjmVIJKPpJNHUFmWa11nMKhZWIhiFxVBGI9UqjailqJEY5IL1he3rMuVWq9RSlcpaGi7pKiy6xpl1IGj1kVGVtFAY1giDsQ6TXNa6KHhZI056sIVDWHXTylcxY55nVTeuVTeuPdie_sVKddLm4YSN84cf-Dh74LJV9Xi46YcpLCqceeEXSGeaK1-FBGWoYWBZD9ZamMw6oxy_AJleD_gcgGYNgqr3_B03Oovq3lkQ8ctFuvFv3_4enu6fHA2qwcHw8A0s5ci5QnFDxt7C4mR8Zd7BE3U9GfnxZpwpfwDcNhb7
linkToPdf http://cvtisr.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV1Lb9QwEB5BQQgOvB_L00g9cElJ4mxiH6uWhYqyVBSk3iLHD7ESONV6W9FfwN9mxvGuulSVENddx0qcb2a-yYw_A2xiFJWq4-OscIXOKqWrTCErzyqhSmOErbQV8bCJZjoVR0fyIG0Ko70weBMBZwqxiE9WfWxcUhgo3uLvXvl-i2sMy1xehWtjDOeE7u2dw6X_JQjWQy0Zc2UkFCtBnwsTUETSYT0iXaCZf3dLngs_kzv_d-N34Xaim2x7wMc9uGL9fbh1ToTwAfzeR4fHPlFjHm1ROWO9Y3FbLn3TpyZVdkjSA_3MBEZfbRlSxmHAz97g3FO0lWzPuzm1sjP01piGp2479sWeIhENbDcdw4JOic08-_zrDHEbMcHez2PT2SI8hG-Td193PmTpeIZMVTxfZIa7usnLrojVxdopBKV0mNIYpFyNlZ2SHRKEUlZj6camyYUzOndc56pTVij-CDZ87-0TYOj9kVk1vNaY3kiLOU-lhOpMXYumQ7yMYBOXsE3mFdpYOS-LNq1rm9Z1BFvLN9nqJHFOJ238uPyCN6sLjgd1j8uHvl5Co0ULpFegvO1PQkuFSuplqIoRPB6gspqMC3wCZHwjEGsgWg0gde_1f_zse1T5LkjMr5T503979ldw42B30u7vTT8-g5slUi_qcSiq57CxmJ_YF3Bdny5mYf4yGssfkawZdQ
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=Live+Microscopy+of+Multicellular+Spheroids+with+the+Multimodal+Near-Infrared+Nanoparticles+Reveals+Differences+in+Oxygenation+Gradients&rft.jtitle=ACS+nano&rft.au=Debruyne%2C+Angela+C.&rft.au=Okkelman%2C+Irina+A.&rft.au=Heymans%2C+Nina&rft.au=Pinheiro%2C+Cl%C3%A1udio&rft.date=2024-05-14&rft.issn=1936-0851&rft.eissn=1936-086X&rft.volume=18&rft.issue=19&rft.spage=12168&rft.epage=12186&rft_id=info:doi/10.1021%2Facsnano.3c12539&rft.externalDBID=n%2Fa&rft.externalDocID=10_1021_acsnano_3c12539
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