In vivo efficacy of endothelial growth medium stimulated mesenchymal stem cells derived from patients with critical limb ischemia

Cell therapy has been proposed for patients with critical limb ischemia (CLI). Autologous bone marrow derived cells (BMCs) have been mostly used, mesenchymal stem cells (MSCs) being an alternative. The aim of this study was to characterize two types of MSCs and evaluate their efficacy. MSCs were obt...

Full description

Saved in:
Bibliographic Details
Published inJournal of translational medicine Vol. 17; no. 1; pp. 261 - 21
Main Authors Al-Rifai, Rida, Nguyen, Philippe, Bouland, Nicole, Terryn, Christine, Kanagaratnam, Lukshe, Poitevin, Gaël, François, Caroline, Boisson-Vidal, Catherine, Sevestre, Marie-Antoinette, Tournois, Claire
Format Journal Article
LanguageEnglish
Published England BioMed Central Ltd 09.08.2019
BioMed Central
BMC
Subjects
Amputation
Angiogenesis
B cells
Biotechnology
Blood flow
Cardiology and cardiovascular system
Care and treatment
Cell therapy
Cellular Biology
Critical limb ischemia
Cytokines
Diagnosis
Endothelial growth factors
Endothelium
Genes
Hematology
Human health and pathology
Ischemia
Life Sciences
Limb salvage
Mesenchymal stem cells
Stem cell research
Stem cell transplantation
Stem cells
Testing
France
Angiogenesis
Cell therapy
Critical limb ischemia
Mesenchymal stem cells
Online AccessGet full text

Cover

Abstract Cell therapy has been proposed for patients with critical limb ischemia (CLI). Autologous bone marrow derived cells (BMCs) have been mostly used, mesenchymal stem cells (MSCs) being an alternative. The aim of this study was to characterize two types of MSCs and evaluate their efficacy. MSCs were obtained from CLI-patients BMCs. Stimulated- (S-) MSCs were cultured in endothelial growth medium. Cells were characterized by the expression of cell surface markers, the relative expression of 6 genes, the secretion of 10 cytokines and the ability to form vessel-like structures. The cell proangiogenic properties was analysed in vivo, in a hindlimb ischemia model. Perfusion of lower limbs and functional tests were assessed for 28 days after cell infusion. Muscle histological analysis (neoangiogenesis, arteriogenesis and muscle repair) was performed. S-MSCs can be obtained from CLI-patients BMCs. They do not express endothelial specific markers but can be distinguished from MSCs by their secretome. S-MSCs have the ability to form tube-like structures and, in vivo, to induce blood flow recovery. No amputation was observed in S-MSCs treated mice. Functional tests showed improvement in treated groups with a superiority of MSCs and S-MSCs. In muscles, CD31+ and αSMA+ labelling were the highest in S-MSCs treated mice. S-MSCs induced the highest muscle repair. S-MSCs exert angiogenic potential probably mediated by a paracrine mechanism. Their administration is associated with flow recovery, limb salvage and muscle repair. The secretome from S-MSCs or secretome-derived products may have a strong potential in vessel regeneration and muscle repair. Trial registration NCT00533104.
AbstractList Background: Cell therapy has been proposed for patients with critical limb ischemia (CLI). Autologous bone marrow derived cells (BMCs) have been mostly used, mesenchymal stem cells (MSCs) being an alternative. The aim of this study was to characterize two types of MSCs and evaluate their efficacy.Methods: MSCs were obtained from CLI-patients BMCs. Stimulated-(S-) MSCs were cultured in endothelial growth medium. Cells were characterized by the expression of cell surface markers, the relative expression of 6 genes, the secretion of 10 cytokines and the ability to form vessel-like structures. The cell proangiogenic properties was analysed in vivo, in a hindlimb ischemia model. Perfusion of lower limbs and functional tests were assessed for 28 days after cell infusion. Muscle histological analysis (neoangiogenesis, arteriogenesis and muscle repair) was performed.Results: S-MSCs can be obtained from CLI-patients BMCs. They do not express endothelial specific markers but can be distinguished from MSCs by their secretome. S-MSCs have the ability to form tube-like structures and, in vivo, to induce blood flow recovery. No amputation was observed in S-MSCs treated mice. Functional tests showed improvement in treated groups with a superiority of MSCs and S-MSCs. In muscles, CD31+ and αSMA+ labelling were the highest in S-MSCs treated mice. S-MSCs induced the highest muscle repair.Conclusions: S-MSCs exert angiogenic potential probably mediated by a paracrine mechanism. Their administration is associated with flow recovery, limb salvage and muscle repair. The secretome from S-MSCs or secretome-derived products may have a strong potential in vessel regeneration and muscle repair. Trial registration NCT00533104
Background Cell therapy has been proposed for patients with critical limb ischemia (CLI). Autologous bone marrow derived cells (BMCs) have been mostly used, mesenchymal stem cells (MSCs) being an alternative. The aim of this study was to characterize two types of MSCs and evaluate their efficacy. Methods MSCs were obtained from CLI-patients BMCs. Stimulated- (S-) MSCs were cultured in endothelial growth medium. Cells were characterized by the expression of cell surface markers, the relative expression of 6 genes, the secretion of 10 cytokines and the ability to form vessel-like structures. The cell proangiogenic properties was analysed in vivo, in a hindlimb ischemia model. Perfusion of lower limbs and functional tests were assessed for 28 days after cell infusion. Muscle histological analysis (neoangiogenesis, arteriogenesis and muscle repair) was performed. Results S-MSCs can be obtained from CLI-patients BMCs. They do not express endothelial specific markers but can be distinguished from MSCs by their secretome. S-MSCs have the ability to form tube-like structures and, in vivo, to induce blood flow recovery. No amputation was observed in S-MSCs treated mice. Functional tests showed improvement in treated groups with a superiority of MSCs and S-MSCs. In muscles, CD31+ and [alpha]SMA+ labelling were the highest in S-MSCs treated mice. S-MSCs induced the highest muscle repair. Conclusions S-MSCs exert angiogenic potential probably mediated by a paracrine mechanism. Their administration is associated with flow recovery, limb salvage and muscle repair. The secretome from S-MSCs or secretome-derived products may have a strong potential in vessel regeneration and muscle repair. Trial registration NCT00533104 Keywords: Angiogenesis, Cell therapy, Critical limb ischemia, Mesenchymal stem cells
Cell therapy has been proposed for patients with critical limb ischemia (CLI). Autologous bone marrow derived cells (BMCs) have been mostly used, mesenchymal stem cells (MSCs) being an alternative. The aim of this study was to characterize two types of MSCs and evaluate their efficacy.BACKGROUNDCell therapy has been proposed for patients with critical limb ischemia (CLI). Autologous bone marrow derived cells (BMCs) have been mostly used, mesenchymal stem cells (MSCs) being an alternative. The aim of this study was to characterize two types of MSCs and evaluate their efficacy.MSCs were obtained from CLI-patients BMCs. Stimulated- (S-) MSCs were cultured in endothelial growth medium. Cells were characterized by the expression of cell surface markers, the relative expression of 6 genes, the secretion of 10 cytokines and the ability to form vessel-like structures. The cell proangiogenic properties was analysed in vivo, in a hindlimb ischemia model. Perfusion of lower limbs and functional tests were assessed for 28 days after cell infusion. Muscle histological analysis (neoangiogenesis, arteriogenesis and muscle repair) was performed.METHODSMSCs were obtained from CLI-patients BMCs. Stimulated- (S-) MSCs were cultured in endothelial growth medium. Cells were characterized by the expression of cell surface markers, the relative expression of 6 genes, the secretion of 10 cytokines and the ability to form vessel-like structures. The cell proangiogenic properties was analysed in vivo, in a hindlimb ischemia model. Perfusion of lower limbs and functional tests were assessed for 28 days after cell infusion. Muscle histological analysis (neoangiogenesis, arteriogenesis and muscle repair) was performed.S-MSCs can be obtained from CLI-patients BMCs. They do not express endothelial specific markers but can be distinguished from MSCs by their secretome. S-MSCs have the ability to form tube-like structures and, in vivo, to induce blood flow recovery. No amputation was observed in S-MSCs treated mice. Functional tests showed improvement in treated groups with a superiority of MSCs and S-MSCs. In muscles, CD31+ and αSMA+ labelling were the highest in S-MSCs treated mice. S-MSCs induced the highest muscle repair.RESULTSS-MSCs can be obtained from CLI-patients BMCs. They do not express endothelial specific markers but can be distinguished from MSCs by their secretome. S-MSCs have the ability to form tube-like structures and, in vivo, to induce blood flow recovery. No amputation was observed in S-MSCs treated mice. Functional tests showed improvement in treated groups with a superiority of MSCs and S-MSCs. In muscles, CD31+ and αSMA+ labelling were the highest in S-MSCs treated mice. S-MSCs induced the highest muscle repair.S-MSCs exert angiogenic potential probably mediated by a paracrine mechanism. Their administration is associated with flow recovery, limb salvage and muscle repair. The secretome from S-MSCs or secretome-derived products may have a strong potential in vessel regeneration and muscle repair. Trial registration NCT00533104.CONCLUSIONSS-MSCs exert angiogenic potential probably mediated by a paracrine mechanism. Their administration is associated with flow recovery, limb salvage and muscle repair. The secretome from S-MSCs or secretome-derived products may have a strong potential in vessel regeneration and muscle repair. Trial registration NCT00533104.
Abstract Background Cell therapy has been proposed for patients with critical limb ischemia (CLI). Autologous bone marrow derived cells (BMCs) have been mostly used, mesenchymal stem cells (MSCs) being an alternative. The aim of this study was to characterize two types of MSCs and evaluate their efficacy. Methods MSCs were obtained from CLI-patients BMCs. Stimulated- (S-) MSCs were cultured in endothelial growth medium. Cells were characterized by the expression of cell surface markers, the relative expression of 6 genes, the secretion of 10 cytokines and the ability to form vessel-like structures. The cell proangiogenic properties was analysed in vivo, in a hindlimb ischemia model. Perfusion of lower limbs and functional tests were assessed for 28 days after cell infusion. Muscle histological analysis (neoangiogenesis, arteriogenesis and muscle repair) was performed. Results S-MSCs can be obtained from CLI-patients BMCs. They do not express endothelial specific markers but can be distinguished from MSCs by their secretome. S-MSCs have the ability to form tube-like structures and, in vivo, to induce blood flow recovery. No amputation was observed in S-MSCs treated mice. Functional tests showed improvement in treated groups with a superiority of MSCs and S-MSCs. In muscles, CD31+ and αSMA+ labelling were the highest in S-MSCs treated mice. S-MSCs induced the highest muscle repair. Conclusions S-MSCs exert angiogenic potential probably mediated by a paracrine mechanism. Their administration is associated with flow recovery, limb salvage and muscle repair. The secretome from S-MSCs or secretome-derived products may have a strong potential in vessel regeneration and muscle repair. Trial registration NCT00533104
Cell therapy has been proposed for patients with critical limb ischemia (CLI). Autologous bone marrow derived cells (BMCs) have been mostly used, mesenchymal stem cells (MSCs) being an alternative. The aim of this study was to characterize two types of MSCs and evaluate their efficacy. MSCs were obtained from CLI-patients BMCs. Stimulated- (S-) MSCs were cultured in endothelial growth medium. Cells were characterized by the expression of cell surface markers, the relative expression of 6 genes, the secretion of 10 cytokines and the ability to form vessel-like structures. The cell proangiogenic properties was analysed in vivo, in a hindlimb ischemia model. Perfusion of lower limbs and functional tests were assessed for 28 days after cell infusion. Muscle histological analysis (neoangiogenesis, arteriogenesis and muscle repair) was performed. S-MSCs can be obtained from CLI-patients BMCs. They do not express endothelial specific markers but can be distinguished from MSCs by their secretome. S-MSCs have the ability to form tube-like structures and, in vivo, to induce blood flow recovery. No amputation was observed in S-MSCs treated mice. Functional tests showed improvement in treated groups with a superiority of MSCs and S-MSCs. In muscles, CD31+ and αSMA+ labelling were the highest in S-MSCs treated mice. S-MSCs induced the highest muscle repair. S-MSCs exert angiogenic potential probably mediated by a paracrine mechanism. Their administration is associated with flow recovery, limb salvage and muscle repair. The secretome from S-MSCs or secretome-derived products may have a strong potential in vessel regeneration and muscle repair. Trial registration NCT00533104.
Cell therapy has been proposed for patients with critical limb ischemia (CLI). Autologous bone marrow derived cells (BMCs) have been mostly used, mesenchymal stem cells (MSCs) being an alternative. The aim of this study was to characterize two types of MSCs and evaluate their efficacy. MSCs were obtained from CLI-patients BMCs. Stimulated- (S-) MSCs were cultured in endothelial growth medium. Cells were characterized by the expression of cell surface markers, the relative expression of 6 genes, the secretion of 10 cytokines and the ability to form vessel-like structures. The cell proangiogenic properties was analysed in vivo, in a hindlimb ischemia model. Perfusion of lower limbs and functional tests were assessed for 28 days after cell infusion. Muscle histological analysis (neoangiogenesis, arteriogenesis and muscle repair) was performed. S-MSCs can be obtained from CLI-patients BMCs. They do not express endothelial specific markers but can be distinguished from MSCs by their secretome. S-MSCs have the ability to form tube-like structures and, in vivo, to induce blood flow recovery. No amputation was observed in S-MSCs treated mice. Functional tests showed improvement in treated groups with a superiority of MSCs and S-MSCs. In muscles, CD31+ and [alpha]SMA+ labelling were the highest in S-MSCs treated mice. S-MSCs induced the highest muscle repair. S-MSCs exert angiogenic potential probably mediated by a paracrine mechanism. Their administration is associated with flow recovery, limb salvage and muscle repair. The secretome from S-MSCs or secretome-derived products may have a strong potential in vessel regeneration and muscle repair.
ArticleNumber 261
Audience Academic
Author Kanagaratnam, Lukshe
François, Caroline
Nguyen, Philippe
Sevestre, Marie-Antoinette
Boisson-Vidal, Catherine
Al-Rifai, Rida
Terryn, Christine
Tournois, Claire
Bouland, Nicole
Poitevin, Gaël
Author_xml – sequence: 1
  givenname: Rida
  surname: Al-Rifai
  fullname: Al-Rifai, Rida
– sequence: 2
  givenname: Philippe
  surname: Nguyen
  fullname: Nguyen, Philippe
– sequence: 3
  givenname: Nicole
  surname: Bouland
  fullname: Bouland, Nicole
– sequence: 4
  givenname: Christine
  surname: Terryn
  fullname: Terryn, Christine
– sequence: 5
  givenname: Lukshe
  surname: Kanagaratnam
  fullname: Kanagaratnam, Lukshe
– sequence: 6
  givenname: Gaël
  surname: Poitevin
  fullname: Poitevin, Gaël
– sequence: 7
  givenname: Caroline
  surname: François
  fullname: François, Caroline
– sequence: 8
  givenname: Catherine
  surname: Boisson-Vidal
  fullname: Boisson-Vidal, Catherine
– sequence: 9
  givenname: Marie-Antoinette
  surname: Sevestre
  fullname: Sevestre, Marie-Antoinette
– sequence: 10
  givenname: Claire
  orcidid: 0000-0002-9946-837X
  surname: Tournois
  fullname: Tournois, Claire
BackLink https://www.ncbi.nlm.nih.gov/pubmed/31399109$$D View this record in MEDLINE/PubMed
https://hal.science/hal-02326058$$DView record in HAL
BookMark eNp9Uk1v1DAQjVAR_YAfwAVZ4gKHFNtx_HFBWlVAV1qJC5wtx7E3rpJ4sbNb9dh_zoSUqlsh5IOtmTfvzYzfeXEyxtEVxVuCLwmR_FMmVHFRYqJKinFVVi-KM8KEKmsp-MmT92lxnvMNxpTVTL0qTitSKUWwOivu1yM6hENEzvtgjb1D0SM3tnHqXB9Mj7Yp3k4dGlwb9gPKUxj2vZlcC5HsRtvdDQDKkxuQdX2fUetSOEDapzignZmCG6eMbgNw2BQm0OhRH4YGhWw7NwTzunjpTZ_dm4f7ovj59cuPq-ty8_3b-mq1KW3N-VTCFDW10pGaGEUJMw31TFRMWuaVJdYQwZwhvhZNZZ2yjbCqVp7JlnJjnKwuivXC20Zzo3cpDCbd6WiC_hOIaatNgv56pz1phJeGt41SzEtnuKWNaqgULSfQAHB9Xrh2-wY2Y2HGZPoj0uPMGDq9jQfNuZRUUiD4uBB0z8quVxs9xzCtKMe1PMxiHx7EUvy1d3nSA-wOlm1GF_dZUyqIZJIoAdD3C3RrYIww-gjqdobrVa04xxi0AXX5DxScFv7DgsV8gPhRwbun4z42_NdGACALwKaYc3L-EUKwnq2qF6tqsKqerapnUvGsxoYJ_BLnjYX-P5W_AfG97mk
CitedBy_id crossref_primary_10_1016_j_heliyon_2023_e18245
crossref_primary_10_1021_acsnano_2c02898
crossref_primary_10_1155_2020_2830565
crossref_primary_10_1016_j_jconrel_2021_01_034
crossref_primary_10_1242_dmm_050632
crossref_primary_10_1186_s13287_024_03634_2
crossref_primary_10_1016_j_ejphar_2020_173354
crossref_primary_10_1210_clinem_dgaa403
crossref_primary_10_1007_s11906_020_1034_8
crossref_primary_10_3389_fcell_2020_00471
crossref_primary_10_1155_2020_3150716
crossref_primary_10_1016_j_bbadis_2019_165624
Cites_doi 10.1634/stemcells.2007-0197
10.1186/1479-5876-11-143
10.1016/j.surg.2017.11.018
10.1161/CIRCRESAHA.108.175943
10.1016/j.jcyt.2013.11.011
10.1007/s00259-016-3480-8
10.3390/ijms18091852
10.1111/j.1743-6109.2008.01172.x
10.1371/journal.pone.0049447
10.1253/circj.CJ-17-0045
10.1111/ahe.12318
10.1016/j.semcdb.2017.11.005
10.1038/nprot.2009.185
10.15283/ijsc.2013.6.1.37
10.1002/stem.1198
10.1016/j.jcyt.2016.10.013
10.1161/CIRCRESAHA.116.303849
10.1161/CIRCRESAHA.116.309045
10.1177/0003319710364213
10.1007/s11886-013-0447-2
10.1002/cyto.a.23242
10.1016/j.jacc.2009.06.058
10.1080/19491034.2015.1090073
10.1038/mt.2014.161
10.1016/j.jss.2010.04.025
10.1155/2018/8179075
10.1016/j.jss.2014.06.041
10.1634/stemcells.2005-0365
10.1016/j.jvs.2006.12.037
10.1111/j.1538-7836.2010.03936.x
10.1634/stemcells.22-3-377
10.1016/j.jvs.2011.04.006
10.1161/ATVBAHA.109.186189
10.1253/circj.CJ-11-1135
10.1016/j.jcyt.2016.02.009
10.1016/j.jss.2015.02.011
10.1016/j.acthis.2016.11.009
10.1016/j.biocel.2012.12.001
10.1161/CIRCRESAHA.116.304710
10.2174/1573403X113099990001
10.1016/j.jtcvs.2011.08.053
10.1038/icb.2015.94
10.1111/j.1538-7836.2007.02381.x
10.1177/0003319715595172
10.1016/j.cardiores.2005.02.006
10.1215/S1152851705000232
10.1089/rej.2009.0872
10.1016/j.ejvs.2017.10.012
10.1002/term.359
10.1016/S0140-6736(02)09670-8
10.1016/j.yjmcc.2010.08.010
10.1038/bmt.2011.196
10.1177/1538574413518119
10.1371/journal.pone.0096161
10.1016/j.diabres.2010.12.010
10.1148/radiol.2432060491
10.1007/s00268-012-1892-6
10.1155/2018/9415367
10.1038/mt.2012.52
10.1016/j.ejvs.2015.08.018
10.1083/jcb.144.6.1113
10.1371/journal.pone.0046842
10.1007/s10238-013-0238-5
10.1016/j.bbrc.2010.08.029
10.1016/j.stem.2009.05.003
10.1016/j.jvs.2012.04.067
ContentType Journal Article
Copyright COPYRIGHT 2019 BioMed Central Ltd.
Distributed under a Creative Commons Attribution 4.0 International License
The Author(s) 2019
Copyright_xml – notice: COPYRIGHT 2019 BioMed Central Ltd.
– notice: Distributed under a Creative Commons Attribution 4.0 International License
– notice: The Author(s) 2019
DBID AAYXX
CITATION
NPM
7X8
1XC
VOOES
5PM
DOA
DOI 10.1186/s12967-019-2003-3
DatabaseName CrossRef
PubMed
MEDLINE - Academic
Hyper Article en Ligne (HAL)
Hyper Article en Ligne (HAL) (Open Access)
PubMed Central (Full Participant titles)
DOAJ - Directory of Open Access Journals
DatabaseTitle CrossRef
PubMed
MEDLINE - Academic
DatabaseTitleList

MEDLINE - Academic

PubMed
Database_xml – sequence: 1
  dbid: DOA
  name: DOAJ Directory of Open Access Journals
  url: https://www.doaj.org/
  sourceTypes: Open Website
– sequence: 2
  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 Medicine
EISSN 1479-5876
EndPage 21
ExternalDocumentID oai_doaj_org_article_f1b7f8a6db994f8ea6c2b9b287d61151
PMC6688282
oai_HAL_hal_02326058v1
A596600823
31399109
10_1186_s12967_019_2003_3
Genre Research Support, Non-U.S. Gov't
Journal Article
GeographicLocations France
GeographicLocations_xml – name: France
GroupedDBID ---
0R~
29L
2WC
53G
5VS
6PF
7X7
88E
8FI
8FJ
AAFWJ
AAJSJ
AASML
AAWTL
AAYXX
ABDBF
ABUWG
ACGFO
ACGFS
ACIHN
ACIWK
ACPRK
ACUHS
ADBBV
ADUKV
AEAQA
AENEX
AFKRA
AFPKN
AFRAH
AHBYD
AHMBA
AHYZX
ALIPV
ALMA_UNASSIGNED_HOLDINGS
AMKLP
AMTXH
AOIJS
BAPOH
BAWUL
BCNDV
BENPR
BFQNJ
BMC
BPHCQ
BVXVI
C6C
CCPQU
CITATION
CS3
DIK
DU5
E3Z
EBD
EBLON
EBS
EJD
ESX
F5P
FYUFA
GROUPED_DOAJ
GX1
H13
HMCUK
HYE
IAO
IHR
INH
INR
ITC
KQ8
M1P
M48
M~E
O5R
O5S
OK1
OVT
P2P
PGMZT
PHGZM
PHGZT
PIMPY
PQQKQ
PROAC
PSQYO
RBZ
RNS
ROL
RPM
RSV
SBL
SOJ
TR2
TUS
UKHRP
WOQ
WOW
XSB
~8M
-A0
3V.
ACRMQ
ADINQ
C24
NPM
PMFND
7X8
PPXIY
1XC
2VQ
4.4
ADRAZ
AHSBF
IPNFZ
RIG
VOOES
5PM
PJZUB
PUEGO
ID FETCH-LOGICAL-c566t-87652c8e151a9214ab2f47348c4f9c1ca174ea1f57b3ce9cb7c959f48d26aae83
IEDL.DBID M48
ISSN 1479-5876
IngestDate Wed Aug 27 01:08:20 EDT 2025
Thu Aug 21 13:43:03 EDT 2025
Fri May 09 12:24:42 EDT 2025
Thu Jul 10 18:01:41 EDT 2025
Tue Jun 17 20:51:30 EDT 2025
Tue Jun 10 20:24:49 EDT 2025
Thu Jan 02 22:59:03 EST 2025
Tue Jul 01 03:51:12 EDT 2025
Thu Apr 24 22:53:33 EDT 2025
IsDoiOpenAccess true
IsOpenAccess true
IsPeerReviewed true
IsScholarly true
Issue 1
Keywords Angiogenesis
Cell therapy
Critical limb ischemia
Mesenchymal stem cells
Language English
License Distributed under a Creative Commons Attribution 4.0 International License: http://creativecommons.org/licenses/by/4.0
Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-c566t-87652c8e151a9214ab2f47348c4f9c1ca174ea1f57b3ce9cb7c959f48d26aae83
Notes ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 23
ORCID 0000-0002-9946-837X
0000-0001-6651-4926
0000-0002-1779-6936
0000-0002-6976-0011
0000-0002-3954-5919
OpenAccessLink http://journals.scholarsportal.info/openUrl.xqy?doi=10.1186/s12967-019-2003-3
PMID 31399109
PQID 2271848197
PQPubID 23479
PageCount 21
ParticipantIDs doaj_primary_oai_doaj_org_article_f1b7f8a6db994f8ea6c2b9b287d61151
pubmedcentral_primary_oai_pubmedcentral_nih_gov_6688282
hal_primary_oai_HAL_hal_02326058v1
proquest_miscellaneous_2271848197
gale_infotracmisc_A596600823
gale_infotracacademiconefile_A596600823
pubmed_primary_31399109
crossref_primary_10_1186_s12967_019_2003_3
crossref_citationtrail_10_1186_s12967_019_2003_3
ProviderPackageCode CITATION
AAYXX
PublicationCentury 2000
PublicationDate 2019-08-09
PublicationDateYYYYMMDD 2019-08-09
PublicationDate_xml – month: 08
  year: 2019
  text: 2019-08-09
  day: 09
PublicationDecade 2010
PublicationPlace England
PublicationPlace_xml – name: England
– name: London
PublicationTitle Journal of translational medicine
PublicationTitleAlternate J Transl Med
PublicationYear 2019
Publisher BioMed Central Ltd
BioMed Central
BMC
Publisher_xml – name: BioMed Central Ltd
– name: BioMed Central
– name: BMC
References E Tateishi-Yuyama (2003_CR4) 2002; 360
AJ Friedenstein (2003_CR12) 1976; 4
AD Morris (2003_CR49) 2018; 163
G Bergers (2003_CR51) 2005; 7
N van Royen (2003_CR52) 2009; 55
W Tancharoen (2003_CR39) 2017; 119
A Liew (2003_CR8) 2016; 67
RJ Powell (2003_CR62) 2012; 20
A Limbourg (2003_CR30) 2009; 4
JR Beauchamp (2003_CR55) 1999; 144
HC Lee (2003_CR64) 2012; 76
MH Criqui (2003_CR1) 2015; 116
W Cuccuini (2003_CR28) 2010; 8
TM Gaafar (2003_CR26) 2014; 14
D Mushahary (2003_CR13) 2018; 93
GP Lasala (2003_CR63) 2012; 144
NR Dash (2003_CR60) 2009; 12
S Roura (2003_CR25) 2012; 7
RH Lee (2003_CR56) 2009; 5
W Roman (2003_CR35) 2018; 82
JW Liu (2003_CR21) 2007; 5
A Bura (2003_CR19) 2014; 16
SW Kim (2003_CR59) 2006; 24
GS Teo (2003_CR43) 2012; 30
A Bayes-Genis (2003_CR24) 2010; 49
J Phelps (2003_CR70) 2018; 2018
A Goedecke (2003_CR45) 2011; 5
H Gremmels (2003_CR29) 2014; 22
L Chen (2003_CR42) 2014; 9
SS Yang (2003_CR66) 2013; 6
J Oswald (2003_CR38) 2004; 22
Y Seo (2003_CR69) 2019; 2019
M Konno (2003_CR23) 2010; 400
D Lu (2003_CR17) 2011; 92
AK Das (2003_CR65) 2013; 37
LJ Harris (2003_CR46) 2010; 163
RA Brenes (2003_CR31) 2012; 56
FJ Vizoso (2003_CR15) 2017; 18
PE Reis (2003_CR33) 2014; 48
K Janeczek Portalska (2003_CR40) 2012; 7
M Ai (2003_CR5) 2016; 18
N Hakimzadeh (2003_CR53) 2014; 10
PK Gupta (2003_CR18) 2013; 11
M Simons (2003_CR47) 2015; 116
R El Omar (2003_CR68) 2016; 94
L Brewster (2003_CR50) 2017; 65
S Dimmeler (2003_CR9) 2008; 102
AM Heemskerk (2003_CR58) 2007; 243
SM Peeters Weem (2003_CR7) 2015; 50
S Belmadani (2003_CR44) 2009; 29
G Chamberlain (2003_CR14) 2007; 25
B Pignon (2003_CR10) 2017; 81
H Ning (2003_CR22) 2009; 6
C Wang (2003_CR37) 2018; 55
T Iwase (2003_CR48) 2005; 66
M Rigato (2003_CR6) 2017; 120
B Cadot (2003_CR34) 2015; 6
P Koutakis (2003_CR57) 2015; 196
L Norgren (2003_CR2) 2007; 45
C Tournois (2003_CR11) 2017; 19
KW Yong (2003_CR16) 2018; 2018
RJ Powell (2003_CR67) 2011; 54
V Cannella (2003_CR27) 2018; 47
NK Gupta (2003_CR3) 2014; 16
M Choi (2003_CR32) 2013; 45
DM Smadja (2003_CR36) 2012; 47
E Barreto-Duran (2003_CR20) 2018; 7
G Hendrikx (2003_CR54) 2016; 43
GP Lasala (2003_CR61) 2010; 61
A Policha (2003_CR41) 2014; 192
References_xml – volume: 25
  start-page: 2739
  year: 2007
  ident: 2003_CR14
  publication-title: Stem Cells
  doi: 10.1634/stemcells.2007-0197
– volume: 11
  start-page: 143
  year: 2013
  ident: 2003_CR18
  publication-title: J Transl Med
  doi: 10.1186/1479-5876-11-143
– volume: 163
  start-page: 870
  year: 2018
  ident: 2003_CR49
  publication-title: Surgery
  doi: 10.1016/j.surg.2017.11.018
– volume: 102
  start-page: 1319
  year: 2008
  ident: 2003_CR9
  publication-title: Circ Res
  doi: 10.1161/CIRCRESAHA.108.175943
– volume: 16
  start-page: 245
  year: 2014
  ident: 2003_CR19
  publication-title: Cytotherapy
  doi: 10.1016/j.jcyt.2013.11.011
– volume: 43
  start-page: 2433
  year: 2016
  ident: 2003_CR54
  publication-title: Eur J Nucl Med Mol Imaging
  doi: 10.1007/s00259-016-3480-8
– volume: 4
  start-page: 267
  year: 1976
  ident: 2003_CR12
  publication-title: Exp Hematol
– volume: 18
  start-page: 1852
  year: 2017
  ident: 2003_CR15
  publication-title: Int J Mol Sci.
  doi: 10.3390/ijms18091852
– volume: 6
  start-page: 967
  year: 2009
  ident: 2003_CR22
  publication-title: J Sex Med
  doi: 10.1111/j.1743-6109.2008.01172.x
– volume: 7
  start-page: e49447
  year: 2012
  ident: 2003_CR25
  publication-title: PLoS ONE
  doi: 10.1371/journal.pone.0049447
– volume: 81
  start-page: 1713
  year: 2017
  ident: 2003_CR10
  publication-title: Circ J
  doi: 10.1253/circj.CJ-17-0045
– volume: 47
  start-page: 11
  year: 2018
  ident: 2003_CR27
  publication-title: Anat Histol Embryol
  doi: 10.1111/ahe.12318
– volume: 82
  start-page: 51
  year: 2018
  ident: 2003_CR35
  publication-title: Semin Cell Dev Biol
  doi: 10.1016/j.semcdb.2017.11.005
– volume: 4
  start-page: 1737
  year: 2009
  ident: 2003_CR30
  publication-title: Nat Protoc
  doi: 10.1038/nprot.2009.185
– volume: 6
  start-page: 37
  year: 2013
  ident: 2003_CR66
  publication-title: Int J Stem Cells
  doi: 10.15283/ijsc.2013.6.1.37
– volume: 30
  start-page: 2472
  year: 2012
  ident: 2003_CR43
  publication-title: Stem Cells
  doi: 10.1002/stem.1198
– volume: 19
  start-page: 299
  year: 2017
  ident: 2003_CR11
  publication-title: Cytotherapy
  doi: 10.1016/j.jcyt.2016.10.013
– volume: 116
  start-page: 1509
  year: 2015
  ident: 2003_CR1
  publication-title: Circ Res
  doi: 10.1161/CIRCRESAHA.116.303849
– volume: 120
  start-page: 1326
  year: 2017
  ident: 2003_CR6
  publication-title: Circ Res
  doi: 10.1161/CIRCRESAHA.116.309045
– volume: 61
  start-page: 551
  year: 2010
  ident: 2003_CR61
  publication-title: Angiology
  doi: 10.1177/0003319710364213
– volume: 16
  start-page: 447
  year: 2014
  ident: 2003_CR3
  publication-title: Curr Cardiol Rep
  doi: 10.1007/s11886-013-0447-2
– volume: 93
  start-page: 19
  year: 2018
  ident: 2003_CR13
  publication-title: Cytom A
  doi: 10.1002/cyto.a.23242
– volume: 55
  start-page: 17
  year: 2009
  ident: 2003_CR52
  publication-title: J Am Coll Cardiol
  doi: 10.1016/j.jacc.2009.06.058
– volume: 6
  start-page: 373
  year: 2015
  ident: 2003_CR34
  publication-title: Nucleus
  doi: 10.1080/19491034.2015.1090073
– volume: 22
  start-page: 1960
  year: 2014
  ident: 2003_CR29
  publication-title: Mol Ther
  doi: 10.1038/mt.2014.161
– volume: 163
  start-page: e105
  year: 2010
  ident: 2003_CR46
  publication-title: J Surg Res
  doi: 10.1016/j.jss.2010.04.025
– volume: 2018
  start-page: 8179075
  year: 2018
  ident: 2003_CR16
  publication-title: Stem Cells Int
  doi: 10.1155/2018/8179075
– volume: 192
  start-page: 656
  year: 2014
  ident: 2003_CR41
  publication-title: J Surg Res
  doi: 10.1016/j.jss.2014.06.041
– volume: 24
  start-page: 1620
  year: 2006
  ident: 2003_CR59
  publication-title: Stem Cells
  doi: 10.1634/stemcells.2005-0365
– volume: 45
  start-page: S5
  issue: Suppl S
  year: 2007
  ident: 2003_CR2
  publication-title: J Vasc Surg
  doi: 10.1016/j.jvs.2006.12.037
– volume: 8
  start-page: 2042
  year: 2010
  ident: 2003_CR28
  publication-title: J Thromb Haemost
  doi: 10.1111/j.1538-7836.2010.03936.x
– volume: 22
  start-page: 377
  year: 2004
  ident: 2003_CR38
  publication-title: Stem Cells
  doi: 10.1634/stemcells.22-3-377
– volume: 54
  start-page: 1032
  year: 2011
  ident: 2003_CR67
  publication-title: J Vasc Surg
  doi: 10.1016/j.jvs.2011.04.006
– volume: 29
  start-page: 802
  year: 2009
  ident: 2003_CR44
  publication-title: Arterioscler Thromb Vasc Biol
  doi: 10.1161/ATVBAHA.109.186189
– volume: 76
  start-page: 1750
  year: 2012
  ident: 2003_CR64
  publication-title: Circ J
  doi: 10.1253/circj.CJ-11-1135
– volume: 18
  start-page: 712
  year: 2016
  ident: 2003_CR5
  publication-title: Cytotherapy
  doi: 10.1016/j.jcyt.2016.02.009
– volume: 196
  start-page: 172
  year: 2015
  ident: 2003_CR57
  publication-title: J Surg Res
  doi: 10.1016/j.jss.2015.02.011
– volume: 119
  start-page: 113
  year: 2017
  ident: 2003_CR39
  publication-title: Acta Histochem
  doi: 10.1016/j.acthis.2016.11.009
– volume: 45
  start-page: 560
  year: 2013
  ident: 2003_CR32
  publication-title: Int J Biochem Cell Biol
  doi: 10.1016/j.biocel.2012.12.001
– volume: 116
  start-page: e99
  year: 2015
  ident: 2003_CR47
  publication-title: Circ Res
  doi: 10.1161/CIRCRESAHA.116.304710
– volume: 10
  start-page: 73
  year: 2014
  ident: 2003_CR53
  publication-title: Curr Cardiol Rev
  doi: 10.2174/1573403X113099990001
– volume: 144
  start-page: 377
  year: 2012
  ident: 2003_CR63
  publication-title: J Thorac Cardiovasc Surg
  doi: 10.1016/j.jtcvs.2011.08.053
– volume: 94
  start-page: 342
  year: 2016
  ident: 2003_CR68
  publication-title: Immunol Cell Biol
  doi: 10.1038/icb.2015.94
– volume: 5
  start-page: 826
  year: 2007
  ident: 2003_CR21
  publication-title: J Thromb Haemost
  doi: 10.1111/j.1538-7836.2007.02381.x
– volume: 67
  start-page: 444
  year: 2016
  ident: 2003_CR8
  publication-title: Angiology
  doi: 10.1177/0003319715595172
– volume: 66
  start-page: 543
  year: 2005
  ident: 2003_CR48
  publication-title: Cardiovasc Res
  doi: 10.1016/j.cardiores.2005.02.006
– volume: 7
  start-page: 114
  year: 2018
  ident: 2003_CR20
  publication-title: Am J Stem Cells
– volume: 7
  start-page: 452
  year: 2005
  ident: 2003_CR51
  publication-title: Neuro Oncol
  doi: 10.1215/S1152851705000232
– volume: 65
  start-page: e821
  issue: 826–838
  year: 2017
  ident: 2003_CR50
  publication-title: J Vasc Surg
– volume: 12
  start-page: 359
  year: 2009
  ident: 2003_CR60
  publication-title: Rejuvenation Res
  doi: 10.1089/rej.2009.0872
– volume: 55
  start-page: 257
  year: 2018
  ident: 2003_CR37
  publication-title: Eur J Vasc Endovasc Surg
  doi: 10.1016/j.ejvs.2017.10.012
– volume: 5
  start-page: 648
  year: 2011
  ident: 2003_CR45
  publication-title: J Tissue Eng Regen Med
  doi: 10.1002/term.359
– volume: 360
  start-page: 427
  year: 2002
  ident: 2003_CR4
  publication-title: Lancet
  doi: 10.1016/S0140-6736(02)09670-8
– volume: 49
  start-page: 771
  year: 2010
  ident: 2003_CR24
  publication-title: J Mol Cell Cardiol
  doi: 10.1016/j.yjmcc.2010.08.010
– volume: 47
  start-page: 997
  year: 2012
  ident: 2003_CR36
  publication-title: Bone Marrow Transplant
  doi: 10.1038/bmt.2011.196
– volume: 48
  start-page: 207
  year: 2014
  ident: 2003_CR33
  publication-title: Vasc Endovasc Surg
  doi: 10.1177/1538574413518119
– volume: 9
  start-page: e96161
  year: 2014
  ident: 2003_CR42
  publication-title: PLoS ONE
  doi: 10.1371/journal.pone.0096161
– volume: 92
  start-page: 26
  year: 2011
  ident: 2003_CR17
  publication-title: Diabetes Res Clin Pract
  doi: 10.1016/j.diabres.2010.12.010
– volume: 243
  start-page: 413
  year: 2007
  ident: 2003_CR58
  publication-title: Radiology
  doi: 10.1148/radiol.2432060491
– volume: 37
  start-page: 915
  year: 2013
  ident: 2003_CR65
  publication-title: World J Surg
  doi: 10.1007/s00268-012-1892-6
– volume: 2018
  start-page: 9415367
  year: 2018
  ident: 2003_CR70
  publication-title: Stem Cells Int
  doi: 10.1155/2018/9415367
– volume: 20
  start-page: 1280
  year: 2012
  ident: 2003_CR62
  publication-title: Mol Ther
  doi: 10.1038/mt.2012.52
– volume: 50
  start-page: 775
  year: 2015
  ident: 2003_CR7
  publication-title: Eur J Vasc Endovasc Surg
  doi: 10.1016/j.ejvs.2015.08.018
– volume: 2019
  start-page: 5126156
  year: 2019
  ident: 2003_CR69
  publication-title: Stem Cells Int
– volume: 144
  start-page: 1113
  year: 1999
  ident: 2003_CR55
  publication-title: J Cell Biol
  doi: 10.1083/jcb.144.6.1113
– volume: 7
  start-page: e46842
  year: 2012
  ident: 2003_CR40
  publication-title: PLoS ONE
  doi: 10.1371/journal.pone.0046842
– volume: 14
  start-page: 177
  year: 2014
  ident: 2003_CR26
  publication-title: Clin Exp Med
  doi: 10.1007/s10238-013-0238-5
– volume: 400
  start-page: 461
  year: 2010
  ident: 2003_CR23
  publication-title: Biochem Biophys Res Commun
  doi: 10.1016/j.bbrc.2010.08.029
– volume: 5
  start-page: 54
  year: 2009
  ident: 2003_CR56
  publication-title: Cell Stem Cell
  doi: 10.1016/j.stem.2009.05.003
– volume: 56
  start-page: 1669
  year: 2012
  ident: 2003_CR31
  publication-title: J Vasc Surg
  doi: 10.1016/j.jvs.2012.04.067
SSID ssj0024549
Score 2.3092754
Snippet Cell therapy has been proposed for patients with critical limb ischemia (CLI). Autologous bone marrow derived cells (BMCs) have been mostly used, mesenchymal...
Background Cell therapy has been proposed for patients with critical limb ischemia (CLI). Autologous bone marrow derived cells (BMCs) have been mostly used,...
Background: Cell therapy has been proposed for patients with critical limb ischemia (CLI). Autologous bone marrow derived cells (BMCs) have been mostly used,...
Abstract Background Cell therapy has been proposed for patients with critical limb ischemia (CLI). Autologous bone marrow derived cells (BMCs) have been mostly...
SourceID doaj
pubmedcentral
hal
proquest
gale
pubmed
crossref
SourceType Open Website
Open Access Repository
Aggregation Database
Index Database
Enrichment Source
StartPage 261
SubjectTerms Amputation
Angiogenesis
B cells
Biotechnology
Blood flow
Cardiology and cardiovascular system
Care and treatment
Cell therapy
Cellular Biology
Critical limb ischemia
Cytokines
Diagnosis
Endothelial growth factors
Endothelium
Genes
Hematology
Human health and pathology
Ischemia
Life Sciences
Limb salvage
Mesenchymal stem cells
Stem cell research
Stem cell transplantation
Stem cells
Testing
SummonAdditionalLinks – databaseName: DOAJ - Directory of Open Access Journals
  dbid: DOA
  link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwrV3Pi9QwFA66B_Eirj-rq0QRBKHsNE3T5DiKyyiuJxf2FpL0xSlMO2JnBvbof77vtZ1hq6AXr0k6zeR9Sb7XvHyPsTelwzUuSp9GYcpUQgyp8UGkkAOyB-1hFuly8vlXtbiQny-LyxupvigmbJAHHgbuNGa-jNqpyhsjowangvDGI9GvFLKZ3vHBPW_vTO1V9tDtGc8wM61OO9zVFIVYmrQPxsonu1Av1n9Ykm8vKSLyT7r5e9TkjW3o7D67N_JHPh_6fcxuQfuA3TkfT8gfsl-fWr6rd2sOpA3hwhVfRw5tRRetVog1_h397s2S05n6tuE4wRtK4AUVlnSI2OVVg41I3ZnTN_2OVwjRHVbTPRQ-qrB2nD7f8jCmSeCruvG8Rj8Zmto9YhdnH799WKRjmoU0IJfb0HpYiKABB9MZkUnnRZQkehNkNCELDp0WcFksSp8HMMGXwRRoX10J5Rzo_DE7atctPGVcQTULyHBw05tJNLYrhSpyKQ2AVE75hM32w27DqEFOqTBWtvdFtLKDpSxaihJk5jZP2LvDIz8GAY6_NX5Ptjw0JO3svgARZUdE2X8hKmFvCQmWZjh2Dk01XFTAv0haWXZekKIpnVAm7GTSEmdmmFS_RixNOrOYf7FUhkyJHEm9w7e92kPN0vMU89bCettZIZA3SGRsZcKeDNA7_FaOxB2JnklYOQHl5GXTmrZe9urhSqFTpcWz_zFUz9ldQZOqD6E5YUebn1t4gSRt41_28_EahTk6vQ
  priority: 102
  providerName: Directory of Open Access Journals
Title In vivo efficacy of endothelial growth medium stimulated mesenchymal stem cells derived from patients with critical limb ischemia
URI https://www.ncbi.nlm.nih.gov/pubmed/31399109
https://www.proquest.com/docview/2271848197
https://hal.science/hal-02326058
https://pubmed.ncbi.nlm.nih.gov/PMC6688282
https://doaj.org/article/f1b7f8a6db994f8ea6c2b9b287d61151
Volume 17
hasFullText 1
inHoldings 1
isFullTextHit
isPrint
link http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwjV1bixMxFA7bXRBfxPvOupYogiCMdjKZZPIg0souVewii4XiS0gymW2hnbqdtthH_7nnTKfV0UV8mYckc0u-k3wnl-8Q8kIa6ONybsOcKRlyn7tQWcdCH3tgD6n1nRwPJw8uRH_IP46S0QHZhbeqK7C80bXDeFLDxfT19-vNOzD4t5XBp-JNCWOWwA2UKqy2WsUtcgQDk0Q7HfD0l_ReUrHhiEsVJtAL1IucNz6iMUxVav77Prs1xi2Tf_PRP7dV_jZOnd8ld2qCSbtbRNwjB764T24N6iX0B-THh4KuJ-s59SgeYdyGznPqiwxPYk0BjPQKHPPlmOKi-2pGoQeYYYQvn0FKCZAeb2ZQCOWfKU76lzQDDK8hGw-q0FqmtaQ4v0tdHUeBTiczSydQ2342MQ_J8Pzsy_t-WMdhCB2QvSV2mAlzqQdyYBSLuLEs56iK43iuXOQMeDXeRHkibey8clY6lQAA0owJY3waPyKHxbzwx4QKn3UcUCAYFTsc0GAkE0nMufKeCyNsQDq7ateuFinHWBlTXTkrqdDbltLQUhhBM9ZxQF7tb_m2Vej4V-EetuW-IIprVwnzxZWubVXnkZV5akRmleJ56o1wzCoLvmUmgEBHAXmJSNAISvg4aKrtSQb4RRTT0t0EJU9xCTMgp42SYLqukf0csNT4mH73k8Y0oFLoaaZreNuzHdQ03o-b4go_X5WaMSAWHCidDMjjLfT2z4qB2QMTVAGRDVA2XtbMKSbjSl5cCPC6Unby33_5hNxmaDnVRppTcrhcrPxToGpL2yYtOZJtctQ7u_h82a4mPNqVUcL1svf1J9DQPzA
linkProvider Scholars Portal
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=In+vivo+efficacy+of+endothelial+growth+medium+stimulated+mesenchymal+stem+cells+derived+from+patients+with+critical+limb+ischemia&rft.jtitle=Journal+of+translational+medicine&rft.au=Al-Rifai%2C+Rida&rft.au=Nguyen%2C+Philippe&rft.au=Bouland%2C+Nicole&rft.au=Terryn%2C+Christine&rft.date=2019-08-09&rft.pub=BioMed+Central+Ltd&rft.issn=1479-5876&rft.eissn=1479-5876&rft.volume=17&rft.issue=1&rft_id=info:doi/10.1186%2Fs12967-019-2003-3&rft.externalDocID=A596600823
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=1479-5876&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=1479-5876&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=1479-5876&client=summon