Epigenomic analysis reveals a unique DNA methylation program of metastasis-competent circulating tumor cells in colorectal cancer

Circulating tumor cells (CTCs) and epigenetic alterations are involved in the development of metastasis from solid tumors, such as colorectal cancer (CRC). The aim of this study was to characterize the DNA methylation profile of metastasis-competent CTCs in CRC. The DNA methylome of the human CRC-de...

Full description

Saved in:
Bibliographic Details
Published inScientific reports Vol. 13; no. 1; p. 15401
Main Authors Bao-Caamano, Aida, Costa-Fraga, Nicolás, Cayrefourcq, Laure, Jácome, María Amalia, Rodriguez-Casanova, Aitor, Muinelo-Romay, Laura, López-López, Rafael, Alix-Panabières, Catherine, Díaz-Lagares, Angel
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 16.09.2023
Nature Publishing Group
Nature Portfolio
Subjects
631/67/322
692/4028/67
Cancer
Colorectal cancer
Colorectal carcinoma
CpG islands
Deoxyribonucleic acid
DNA
DNA methylation
Epigenetics
Gene regulation
Humanities and Social Sciences
Metastases
Metastasis
multidisciplinary
Science
Science (multidisciplinary)
Solid tumors
Therapeutic targets
Tumor cells
Wnt protein
Online AccessGet full text

Cover

Abstract Circulating tumor cells (CTCs) and epigenetic alterations are involved in the development of metastasis from solid tumors, such as colorectal cancer (CRC). The aim of this study was to characterize the DNA methylation profile of metastasis-competent CTCs in CRC. The DNA methylome of the human CRC-derived cell line CTC-MCC-41 was analyzed and compared with primary (HT29, Caco2, HCT116, RKO) and metastatic (SW620 and COLO205) CRC cells. The association between methylation and the transcriptional profile of CTC-MCC-41 was also evaluated. Differentially methylated CpGs were validated with pyrosequencing and qMSP. Compared to primary and metastatic CRC cells, the methylation profile of CTC-MCC-41 was globally different and characterized by a slight predominance of hypomethylated CpGs mainly distributed in CpG-poor regions. Promoter CpG islands and shore regions of CTC-MCC-41 displayed a unique methylation profile that was associated with the transcriptional program and relevant cancer pathways, mainly Wnt signaling. The epigenetic regulation of relevant genes in CTC-MCC-41 was validated. This study provides new insights into the epigenomic landscape of metastasis-competent CTCs, revealing biological information for metastasis development, as well as new potential biomarkers and therapeutic targets for CRC patients.
AbstractList Circulating tumor cells (CTCs) and epigenetic alterations are involved in the development of metastasis from solid tumors, such as colorectal cancer (CRC). The aim of this study was to characterize the DNA methylation profile of metastasis-competent CTCs in CRC. The DNA methylome of the human CRC-derived cell line CTC-MCC-41 was analyzed and compared with primary (HT29, Caco2, HCT116, RKO) and metastatic (SW620 and COLO205) CRC cells. The association between methylation and the transcriptional profile of CTC-MCC-41 was also evaluated. Differentially methylated CpGs were validated with pyrosequencing and qMSP. Compared to primary and metastatic CRC cells, the methylation profile of CTC-MCC-41 was globally different and characterized by a slight predominance of hypomethylated CpGs mainly distributed in CpG-poor regions. Promoter CpG islands and shore regions of CTC-MCC-41 displayed a unique methylation profile that was associated with the transcriptional program and relevant cancer pathways, mainly Wnt signaling. The epigenetic regulation of relevant genes in CTC-MCC-41 was validated. This study provides new insights into the epigenomic landscape of metastasis-competent CTCs, revealing biological information for metastasis development, as well as new potential biomarkers and therapeutic targets for CRC patients.
Abstract Circulating tumor cells (CTCs) and epigenetic alterations are involved in the development of metastasis from solid tumors, such as colorectal cancer (CRC). The aim of this study was to characterize the DNA methylation profile of metastasis-competent CTCs in CRC. The DNA methylome of the human CRC-derived cell line CTC-MCC-41 was analyzed and compared with primary (HT29, Caco2, HCT116, RKO) and metastatic (SW620 and COLO205) CRC cells. The association between methylation and the transcriptional profile of CTC-MCC-41 was also evaluated. Differentially methylated CpGs were validated with pyrosequencing and qMSP. Compared to primary and metastatic CRC cells, the methylation profile of CTC-MCC-41 was globally different and characterized by a slight predominance of hypomethylated CpGs mainly distributed in CpG-poor regions. Promoter CpG islands and shore regions of CTC-MCC-41 displayed a unique methylation profile that was associated with the transcriptional program and relevant cancer pathways, mainly Wnt signaling. The epigenetic regulation of relevant genes in CTC-MCC-41 was validated. This study provides new insights into the epigenomic landscape of metastasis-competent CTCs, revealing biological information for metastasis development, as well as new potential biomarkers and therapeutic targets for CRC patients.
Abstract Circulating tumor cells (CTCs) and epigenetic alterations are involved in the development of metastasis from solid tumors, such as colorectal cancer (CRC). The aim of this study was to characterize the DNA methylation profile of metastasis-competent CTCs in CRC. The DNA methylome of the human CRC-derived cell line CTC-MCC-41 was analyzed and compared with primary (HT29, Caco2, HCT116, RKO) and metastatic (SW620 and COLO205) CRC cells. The association between methylation and the transcriptional profile of CTC-MCC-41 was also evaluated. Differentially methylated CpGs were validated with pyrosequencing and qMSP. Compared to primary and metastatic CRC cells, the methylation profile of CTC-MCC-41 was globally different and characterized by a slight predominance of hypomethylated CpGs mainly distributed in CpG-poor regions. Promoter CpG islands and shore regions of CTC-MCC-41 displayed a unique methylation profile that was associated with the transcriptional program and relevant cancer pathways, mainly Wnt signaling. The epigenetic regulation of relevant genes in CTC-MCC-41 was validated. This study provides new insights into the epigenomic landscape of metastasis-competent CTCs, revealing biological information for metastasis development, as well as new potential biomarkers and therapeutic targets for CRC patients.
ArticleNumber 15401
Author Jácome, María Amalia
Cayrefourcq, Laure
Bao-Caamano, Aida
Costa-Fraga, Nicolás
Díaz-Lagares, Angel
López-López, Rafael
Rodriguez-Casanova, Aitor
Alix-Panabières, Catherine
Muinelo-Romay, Laura
Author_xml – sequence: 1
  givenname: Aida
  surname: Bao-Caamano
  fullname: Bao-Caamano, Aida
  organization: Epigenomics Unit, Cancer Epigenomics, Translational Medical Oncology Group (ONCOMET), Health Research Institute of Santiago de Compostela (IDIS), University Clinical Hospital of Santiago (CHUS/SERGAS), Universidade de Santiago de Compostela (USC), Galician Precision Oncology Research Group (ONCOGAL), Medicine and Dentistry School, Universidade de Santiago de Compostela (USC)
– sequence: 2
  givenname: Nicolás
  surname: Costa-Fraga
  fullname: Costa-Fraga, Nicolás
  organization: Epigenomics Unit, Cancer Epigenomics, Translational Medical Oncology Group (ONCOMET), Health Research Institute of Santiago de Compostela (IDIS), University Clinical Hospital of Santiago (CHUS/SERGAS), Universidade de Santiago de Compostela (USC), Galician Precision Oncology Research Group (ONCOGAL), Medicine and Dentistry School, Universidade de Santiago de Compostela (USC), Centro de Investigación Biomédica en Red Cáncer (CIBERONC), ISCIII
– sequence: 3
  givenname: Laure
  surname: Cayrefourcq
  fullname: Cayrefourcq, Laure
  organization: Laboratory of Rare Human Circulating Cells, University Medical Center of Montpellier, IURC, CREEC, MIVEGEC, University of Montpellier, CNRS, IRD
– sequence: 4
  givenname: María Amalia
  surname: Jácome
  fullname: Jácome, María Amalia
  organization: Department of Mathematics, MODES Group, CITIC, Faculty of Science, Universidade da Coruña
– sequence: 5
  givenname: Aitor
  surname: Rodriguez-Casanova
  fullname: Rodriguez-Casanova, Aitor
  organization: Epigenomics Unit, Cancer Epigenomics, Translational Medical Oncology Group (ONCOMET), Health Research Institute of Santiago de Compostela (IDIS), University Clinical Hospital of Santiago (CHUS/SERGAS), Universidade de Santiago de Compostela (USC), Galician Precision Oncology Research Group (ONCOGAL), Medicine and Dentistry School, Universidade de Santiago de Compostela (USC), Roche-Chus Joint Unit, Translational Medical Oncology Group (ONCOMET), Health Research Institute of Santiago (IDIS), Centro de Investigación Biomédica en Red Cáncer (CIBERONC), ISCIII
– sequence: 6
  givenname: Laura
  surname: Muinelo-Romay
  fullname: Muinelo-Romay, Laura
  organization: Galician Precision Oncology Research Group (ONCOGAL), Medicine and Dentistry School, Universidade de Santiago de Compostela (USC), Liquid Biopsy Analysis Unit, Translational Medical Oncology Group (ONCOMET), Health Research Institute of Santiago de Compostela (IDIS), Centro de Investigación Biomédica en Red Cáncer (CIBERONC), ISCIII
– sequence: 7
  givenname: Rafael
  surname: López-López
  fullname: López-López, Rafael
  email: rafael.lopez.lopez@sergas.es
  organization: Galician Precision Oncology Research Group (ONCOGAL), Medicine and Dentistry School, Universidade de Santiago de Compostela (USC), Roche-Chus Joint Unit, Translational Medical Oncology Group (ONCOMET), Health Research Institute of Santiago (IDIS), Centro de Investigación Biomédica en Red Cáncer (CIBERONC), ISCIII, Translational Medical Oncology Group (ONCOMET), Health Research Institute of Santiago de Compostela (IDIS), University Clinical Hospital of Santiago (CHUS/SERGAS)
– sequence: 8
  givenname: Catherine
  surname: Alix-Panabières
  fullname: Alix-Panabières, Catherine
  email: c-panabieres@chu-montpellier.fr
  organization: Laboratory of Rare Human Circulating Cells, University Medical Center of Montpellier, IURC, CREEC, MIVEGEC, University of Montpellier, CNRS, IRD, European Liquid Biopsy Society (ELBS)
– sequence: 9
  givenname: Angel
  surname: Díaz-Lagares
  fullname: Díaz-Lagares, Angel
  email: angel.diaz.lagares@sergas.es
  organization: Epigenomics Unit, Cancer Epigenomics, Translational Medical Oncology Group (ONCOMET), Health Research Institute of Santiago de Compostela (IDIS), University Clinical Hospital of Santiago (CHUS/SERGAS), Galician Precision Oncology Research Group (ONCOGAL), Medicine and Dentistry School, Universidade de Santiago de Compostela (USC), Centro de Investigación Biomédica en Red Cáncer (CIBERONC), ISCIII, Department of Clinical Analysis, University Hospital Complex of Santiago de Compostela (CHUS)
BookMark eNp9ks1u1TAQhSNUREvpC7CyxIZNwPF_VqhqC1SqYANra-LYqa8SO9hJq7vkzfFtKqAssCzZGp_5bM-cl9VRiMFW1esGv2swVe8za3irakxozQimsr5_Vp0QzHhNKCFHf-2Pq7Ocd7gMTlrWtC-qYyplI3ErTqqfV7MfbIiTNwgCjPvsM0r2zsKYEaA1-B-rRZdfztFkl9v9CIuPAc0pDgkmFN0hDLlMn2sTp9kuNizI-GTWgzYMaFmnmJCxYwH6gEwcY7JmgREZCMamV9VzVy6zZ4_rafX949W3i8_1zddP1xfnN7XhjVrq1lDHXPmy47TDplOcUgWWKyI5dkrKFnNupRFEAFa4dUoZwYQQ4JxocU9Pq-uN20fY6Tn5CdJeR_D6IRDToCEt3oxWE4qZ7XHXgeoYSNXx3ioiRMscGCYPrA8ba167yfam_DnB-AT69CT4Wz3EO91gjnnDSCG8fSSkWCqcFz35fCgSBBvXrIkSXCrMWlWkb_6R7uKaSq82Vel-Q0VRkU1lUsw5Wff7NQ3WB8fozTG6OEY_OEbflyS6JeUiDoNNf9D_yfoFOmTGow
CitedBy_id crossref_primary_10_1038_s41598_023_48501_x
Cites_doi 10.1016/j.cell.2017.05.016
10.1016/j.cell.2006.11.001
10.1093/bioinformatics/btw313
10.3322/caac.21660
10.1158/2159-8290.CD-21-1059
10.1186/s13148-022-01302-x
10.1111/j.1349-7006.2012.02222.x
10.1186/s12943-022-01616-7
10.3389/fcell.2021.622459
10.1002/ijc.24981
10.1084/jem.97.5.695
10.1038/s41416-022-01819-1
10.1016/j.cell.2018.11.046
10.1200/JCO.2007.15.8923
10.4161/cc.6.21.4880
10.21873/anticanres.11423
10.1186/s12943-021-01326-6
10.1158/1940-6207.CAPR-15-0349
10.1038/sj.onc.1209439
10.3892/ol.2019.10400
10.1016/j.tranon.2021.101174
10.1101/sqb.2005.70.010
10.1007/s10637-019-00824-1
10.1056/NEJMra072067
10.1158/0008-5472.CAN-14-2613
10.15252/emmm.201911908
10.1073/pnas.0914018107
10.1158/1078-0432.CCR-04-1810
10.1101/gr.197194.115
10.3322/caac.21492
10.3390/cancers13153693
10.1373/clinchem.2016.263582
10.1158/1078-0432.CCR-20-3471
10.1126/science.1203543
10.1038/srep28010
10.1038/leu.2009.86
10.3390/cancers11081098
10.1002/path.4011
10.18632/oncotarget.26676
10.1007/s12032-014-0966-8
10.1016/j.juro.2007.01.010
10.1016/S0021-9258(18)61420-6
10.1038/s41392-021-00817-8
10.3390/cancers8070060
10.1038/ng.298
10.1158/1078-0432.CCR-18-0421
10.1016/j.addr.2020.12.010
10.1073/pnas.1608585113
ContentType Journal Article
Copyright The Author(s) 2023. corrected publication 2023
The Author(s) 2023. corrected publication 2023. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
Springer Nature Limited 2023
Copyright_xml – notice: The Author(s) 2023. corrected publication 2023
– notice: The Author(s) 2023. corrected publication 2023. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
– notice: Springer Nature Limited 2023
DBID C6C
AAYXX
CITATION
3V.
7X7
7XB
88A
88E
88I
8FE
8FH
8FI
8FJ
8FK
ABUWG
AFKRA
AZQEC
BBNVY
BENPR
BHPHI
CCPQU
DWQXO
FYUFA
GHDGH
GNUQQ
HCIFZ
K9.
LK8
M0S
M1P
M2P
M7P
PIMPY
PQEST
PQQKQ
PQUKI
Q9U
7X8
5PM
DOA
DOI 10.1038/s41598-023-42037-w
DatabaseName Springer Open Access
CrossRef
ProQuest Central (Corporate)
Health & Medical Collection
ProQuest Central (purchase pre-March 2016)
Biology Database (Alumni Edition)
Medical Database (Alumni Edition)
Science Database (Alumni Edition)
ProQuest SciTech Collection
ProQuest Natural Science Collection
Hospital Premium Collection
Hospital Premium Collection (Alumni Edition)
ProQuest Central (Alumni) (purchase pre-March 2016)
ProQuest Central (Alumni)
ProQuest Central
ProQuest Central Essentials
Biological Science Collection
ProQuest Central
Natural Science Collection
ProQuest One Community College
ProQuest Central Korea
Health Research Premium Collection
Health Research Premium Collection (Alumni)
ProQuest Central Student
SciTech Premium Collection
ProQuest Health & Medical Complete (Alumni)
ProQuest Biological Science Collection
Health & Medical Collection (Alumni Edition)
Medical Database
Science Database
Biological Science Database
Publicly Available Content Database
ProQuest One Academic Eastern Edition (DO NOT USE)
ProQuest One Academic
ProQuest One Academic UKI Edition
ProQuest Central Basic
MEDLINE - Academic
PubMed Central (Full Participant titles)
DOAJ Directory of Open Access Journals
DatabaseTitle CrossRef
Publicly Available Content Database
ProQuest Central Student
ProQuest Central Essentials
ProQuest Health & Medical Complete (Alumni)
ProQuest Central (Alumni Edition)
SciTech Premium Collection
ProQuest One Community College
ProQuest Natural Science Collection
ProQuest Biology Journals (Alumni Edition)
ProQuest Central
Health Research Premium Collection
Health and Medicine Complete (Alumni Edition)
Natural Science Collection
ProQuest Central Korea
Biological Science Collection
ProQuest Medical Library (Alumni)
ProQuest Science Journals (Alumni Edition)
ProQuest Biological Science Collection
ProQuest Central Basic
ProQuest Science Journals
ProQuest One Academic Eastern Edition
ProQuest Hospital Collection
Health Research Premium Collection (Alumni)
Biological Science Database
ProQuest SciTech Collection
ProQuest Hospital Collection (Alumni)
ProQuest Health & Medical Complete
ProQuest Medical Library
ProQuest One Academic UKI Edition
ProQuest One Academic
ProQuest Central (Alumni)
MEDLINE - Academic
DatabaseTitleList Publicly Available Content Database
MEDLINE - Academic


CrossRef
Database_xml – sequence: 1
  dbid: C6C
  name: Springer Open Access
  url: http://www.springeropen.com/
  sourceTypes: Publisher
– sequence: 2
  dbid: DOA
  name: DOAJ Directory of Open Access Journals
  url: https://www.doaj.org/
  sourceTypes: Open Website
– sequence: 3
  dbid: BENPR
  name: ProQuest Central
  url: https://www.proquest.com/central
  sourceTypes: Aggregation Database
DeliveryMethod fulltext_linktorsrc
Discipline Biology
EISSN 2045-2322
EndPage 15401
ExternalDocumentID oai_doaj_org_article_2304ed0bba8b4a78b5de826694fac47d
10_1038_s41598_023_42037_w
GrantInformation_xml – fundername: ISCIII and the European Regional Development Fund (FEDER), reference number PI18/00307. Instituto de Salud Carlos III (ISCII), reference number CP20/00129
– fundername: Xunta de Galicia, reference number IN606A-2020/004
– fundername: Axencia Galega de Innovación (GAIN), Vicepresidencia Segunda e Consellería de Economía, Empresa e Innovación. Reference number IN853B 2018/03
– fundername: PFIS, Instituto de Salud Carlos III (ISCIII) and Fondo Social Europeo, reference number FI19/00240
– fundername: ISCIII and the European Regional Development Fund (FEDER), reference number PI18/00307. Juan Rodés, Instituto de Salud Carlos III (ISCIII) and Servizo Galego de Saúde (SERGAS), reference number JR17/00016
– fundername: European Union Horizon 2020 Research and Innovation program under the Marie Skłodowska-Curie grant agreement No. 765492, The National Institute of Cancer (INCa, http://www.e-cancer.fr), SIRIC Montpellier Cancer Grant INCa_Inserm_DGOS_12553, and the ERA-NET TRANSCAN 2 JTC 2016 PROLIPSY, la Fondation ARC pour la Recherche sur le cancer and les Fonds de dotation AFER pour la recherche médicale
– fundername: ;
GroupedDBID 0R~
3V.
4.4
53G
5VS
7X7
88A
88E
88I
8FE
8FH
8FI
8FJ
AAFWJ
AAJSJ
AAKDD
ABDBF
ABUWG
ACGFS
ACSMW
ADBBV
ADRAZ
AENEX
AFKRA
AJTQC
ALIPV
ALMA_UNASSIGNED_HOLDINGS
AOIJS
AZQEC
BAWUL
BBNVY
BCNDV
BENPR
BHPHI
BPHCQ
BVXVI
C6C
CCPQU
DIK
DWQXO
EBD
EBLON
EBS
ESX
FYUFA
GNUQQ
GROUPED_DOAJ
GX1
HCIFZ
HH5
HMCUK
HYE
KQ8
LK8
M0L
M1P
M2P
M48
M7P
M~E
NAO
OK1
PIMPY
PQQKQ
PROAC
PSQYO
RIG
RNT
RNTTT
RPM
SNYQT
UKHRP
AAYXX
AFPKN
CITATION
7XB
8FK
K9.
PQEST
PQUKI
Q9U
7X8
5PM
ID FETCH-LOGICAL-c518t-9c3f4f598f53b0cb85338ae582750f8779055e7c626a0809f88c64666aff690d3
IEDL.DBID RPM
ISSN 2045-2322
IngestDate Tue Oct 22 15:16:05 EDT 2024
Tue Sep 17 21:29:33 EDT 2024
Fri Oct 25 04:01:35 EDT 2024
Sat Nov 09 11:22:11 EST 2024
Fri Aug 23 03:38:37 EDT 2024
Fri Oct 11 20:47:56 EDT 2024
IsDoiOpenAccess true
IsOpenAccess true
IsPeerReviewed true
IsScholarly true
Issue 1
Language English
License Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-c518t-9c3f4f598f53b0cb85338ae582750f8779055e7c626a0809f88c64666aff690d3
Notes ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 23
OpenAccessLink https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10505142/
PMID 37717096
PQID 2865420136
PQPubID 2041939
PageCount 1
ParticipantIDs doaj_primary_oai_doaj_org_article_2304ed0bba8b4a78b5de826694fac47d
pubmedcentral_primary_oai_pubmedcentral_nih_gov_10505142
proquest_miscellaneous_2865780498
proquest_journals_2865420136
crossref_primary_10_1038_s41598_023_42037_w
springer_journals_10_1038_s41598_023_42037_w
PublicationCentury 2000
PublicationDate 2023-09-16
PublicationDateYYYYMMDD 2023-09-16
PublicationDate_xml – month: 09
  year: 2023
  text: 2023-09-16
  day: 16
PublicationDecade 2020
PublicationPlace London
PublicationPlace_xml – name: London
PublicationTitle Scientific reports
PublicationTitleAbbrev Sci Rep
PublicationYear 2023
Publisher Nature Publishing Group UK
Nature Publishing Group
Nature Portfolio
Publisher_xml – name: Nature Publishing Group UK
– name: Nature Publishing Group
– name: Nature Portfolio
References Santiago, Daniels, Wang, Deng, Lee (CR48) 2017; 7
Tan (CR37) 2019; 18
Cowling, Cole (CR38) 2007; 6
Cohen (CR7) 2008; 26
Hughes (CR16) 1987; 262
Shinozaki (CR13) 2005; 11
Diaz-Lagares (CR21) 2016; 113
Chaffer, Weinberg (CR23) 2011; 331
Lee (CR42) 2018; 24
Scherer, Syverton, Gey (CR25) 1953; 97
Hanssen (CR32) 2016; 6
Ericson (CR26) 2010; 107
Qi (CR39) 2012; 103
Aguilera (CR40) 2006; 25
Lin (CR6) 2021; 6
Xi, Xu (CR2) 2021; 14
Husni (CR20) 2019; 10
Gupta, Massague (CR24) 2006; 127
Mirabelli, Coppola, Salvatore (CR28) 2019
Zhao (CR49) 2022; 21
Eslami, Cortes-Hernandez, Thomas, Pantel, Alix-Panabieres (CR5) 2022; 127
Alix-Panabieres (CR10) 2017; 63
Bray (CR1) 2018; 68
Lyberopoulou (CR14) 2017; 37
Irizarry (CR35) 2009; 41
de Sousa, Vermeulen (CR36) 2016
Cottrell (CR18) 2007; 177
Brown (CR31) 2021; 27
Cayrefourcq (CR15) 2021; 20
Esteller (CR29) 2008; 358
Valencia (CR44) 2009; 23
Hanahan (CR22) 2022; 12
Gu, Eils, Schlesner (CR17) 2016; 32
Bell (CR34) 2016; 26
Huang (CR43) 2014; 31
Dujon (CR4) 2021
Koch (CR8) 2020; 12
Baylin, Chen (CR19) 2005; 70
Sheaffer, Elliott, Kaestner (CR30) 2016; 9
Cayrefourcq (CR9) 2015; 75
Nusse, Clevers (CR46) 2017; 169
Sung (CR3) 2021; 71
Davis (CR47) 2020; 38
Ruiz-Banobre (CR27) 2022; 14
Caspi, Wittenstein, Kazelnik, Shor-Nareznoy, Rosin-Arbesfeld (CR45) 2021; 169
Rodriguez-Casanova (CR11) 2021; 9
Gkountela (CR33) 2019; 176
Carmona (CR12) 2012; 228
Gotze, Wolter, Reifenberger, Muller, Sievers (CR41) 2010; 126
P Mirabelli (42037_CR28) 2019
KL Sheaffer (42037_CR30) 2016; 9
Y Xi (42037_CR2) 2021; 14
C Alix-Panabieres (42037_CR10) 2017; 63
AM Dujon (42037_CR4) 2021
TE Hughes (42037_CR16) 1987; 262
Z Gu (42037_CR17) 2016; 32
R Nusse (42037_CR46) 2017; 169
SJ Cohen (42037_CR7) 2008; 26
M Caspi (42037_CR45) 2021; 169
SZ Eslami (42037_CR5) 2022; 127
WF Scherer (42037_CR25) 1953; 97
L Cayrefourcq (42037_CR15) 2021; 20
SB Baylin (42037_CR19) 2005; 70
H Sung (42037_CR3) 2021; 71
GP Gupta (42037_CR24) 2006; 127
A Valencia (42037_CR44) 2009; 23
A Rodriguez-Casanova (42037_CR11) 2021; 9
H Zhao (42037_CR49) 2022; 21
EMF de Sousa (42037_CR36) 2016
J Ruiz-Banobre (42037_CR27) 2022; 14
RE Husni (42037_CR20) 2019; 10
F Bray (42037_CR1) 2018; 68
FJ Carmona (42037_CR12) 2012; 228
S Gotze (42037_CR41) 2010; 126
K Ericson (42037_CR26) 2010; 107
RE Bell (42037_CR34) 2016; 26
M Shinozaki (42037_CR13) 2005; 11
Y Huang (42037_CR43) 2014; 31
S Cottrell (42037_CR18) 2007; 177
S Gkountela (42037_CR33) 2019; 176
V Lee (42037_CR42) 2018; 24
X Tan (42037_CR37) 2019; 18
CL Chaffer (42037_CR23) 2011; 331
LC Brown (42037_CR31) 2021; 27
C Koch (42037_CR8) 2020; 12
L Cayrefourcq (42037_CR9) 2015; 75
A Diaz-Lagares (42037_CR21) 2016; 113
A Lyberopoulou (42037_CR14) 2017; 37
D Hanahan (42037_CR22) 2022; 12
L Qi (42037_CR39) 2012; 103
L Santiago (42037_CR48) 2017; 7
O Aguilera (42037_CR40) 2006; 25
RA Irizarry (42037_CR35) 2009; 41
M Esteller (42037_CR29) 2008; 358
VH Cowling (42037_CR38) 2007; 6
A Hanssen (42037_CR32) 2016; 6
D Lin (42037_CR6) 2021; 6
SL Davis (42037_CR47) 2020; 38
References_xml – volume: 169
  start-page: 985
  year: 2017
  end-page: 999
  ident: CR46
  article-title: Wnt/beta-catenin signaling, disease, and emerging therapeutic modalities
  publication-title: Cell
  doi: 10.1016/j.cell.2017.05.016
  contributor:
    fullname: Clevers
– volume: 127
  start-page: 679
  year: 2006
  end-page: 695
  ident: CR24
  article-title: Cancer metastasis: Building a framework
  publication-title: Cell
  doi: 10.1016/j.cell.2006.11.001
  contributor:
    fullname: Massague
– volume: 32
  start-page: 2847
  year: 2016
  end-page: 2849
  ident: CR17
  article-title: Complex heatmaps reveal patterns and correlations in multidimensional genomic data
  publication-title: Bioinformatics
  doi: 10.1093/bioinformatics/btw313
  contributor:
    fullname: Schlesner
– volume: 71
  start-page: 209
  year: 2021
  end-page: 249
  ident: CR3
  article-title: Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries
  publication-title: CA Cancer J. Clin.
  doi: 10.3322/caac.21660
  contributor:
    fullname: Sung
– volume: 12
  start-page: 31
  year: 2022
  end-page: 46
  ident: CR22
  article-title: Hallmarks of cancer: New dimensions
  publication-title: Cancer Discov.
  doi: 10.1158/2159-8290.CD-21-1059
  contributor:
    fullname: Hanahan
– volume: 14
  start-page: 86
  year: 2022
  ident: CR27
  article-title: Noninvasive early detection of colorectal cancer by hypermethylation of the LINC00473 promoter in plasma cell-free DNA
  publication-title: Clin. Epigenet.
  doi: 10.1186/s13148-022-01302-x
  contributor:
    fullname: Ruiz-Banobre
– volume: 103
  start-page: 828
  year: 2012
  end-page: 835
  ident: CR39
  article-title: Dickkopf-1 inhibits epithelial-mesenchymal transition of colon cancer cells and contributes to colon cancer suppression
  publication-title: Cancer Sci.
  doi: 10.1111/j.1349-7006.2012.02222.x
  contributor:
    fullname: Qi
– volume: 7
  start-page: 1389
  year: 2017
  end-page: 1406
  ident: CR48
  article-title: Wnt signaling pathway protein LEF1 in cancer, as a biomarker for prognosis and a target for treatment
  publication-title: Am. J. Cancer Res.
  contributor:
    fullname: Lee
– volume: 21
  start-page: 144
  year: 2022
  ident: CR49
  article-title: Wnt signaling in colorectal cancer: pathogenic role and therapeutic target
  publication-title: Mol. Cancer
  doi: 10.1186/s12943-022-01616-7
  contributor:
    fullname: Zhao
– volume: 9
  start-page: 622459
  year: 2021
  ident: CR11
  article-title: Epigenetic landscape of liquid biopsy in colorectal cancer
  publication-title: Front. Cell Dev. Biol.
  doi: 10.3389/fcell.2021.622459
  contributor:
    fullname: Rodriguez-Casanova
– volume: 126
  start-page: 2584
  year: 2010
  end-page: 2593
  ident: CR41
  article-title: Frequent promoter hypermethylation of Wnt pathway inhibitor genes in malignant astrocytic gliomas
  publication-title: Int. J. Cancer
  doi: 10.1002/ijc.24981
  contributor:
    fullname: Sievers
– volume: 97
  start-page: 695
  year: 1953
  end-page: 710
  ident: CR25
  article-title: Studies on the propagation in vitro of poliomyelitis viruses. IV. Viral multiplication in a stable strain of human malignant epithelial cells (strain HeLa) derived from an epidermoid carcinoma of the cervix
  publication-title: J. Exp. Med.
  doi: 10.1084/jem.97.5.695
  contributor:
    fullname: Gey
– volume: 127
  start-page: 800
  year: 2022
  end-page: 810
  ident: CR5
  article-title: Functional analysis of circulating tumour cells: The KEY to understand the biology of the metastatic cascade
  publication-title: Br. J. Cancer
  doi: 10.1038/s41416-022-01819-1
  contributor:
    fullname: Alix-Panabieres
– volume: 176
  start-page: 98
  year: 2019
  end-page: 112
  ident: CR33
  article-title: Circulating tumor cell clustering shapes DNA methylation to enable metastasis seeding
  publication-title: Cell
  doi: 10.1016/j.cell.2018.11.046
  contributor:
    fullname: Gkountela
– volume: 26
  start-page: 3213
  year: 2008
  end-page: 3221
  ident: CR7
  article-title: Relationship of circulating tumor cells to tumor response, progression-free survival, and overall survival in patients with metastatic colorectal cancer
  publication-title: J. Clin. Oncol.
  doi: 10.1200/JCO.2007.15.8923
  contributor:
    fullname: Cohen
– volume: 6
  start-page: 2625
  year: 2007
  end-page: 2627
  ident: CR38
  article-title: Turning the tables: Myc activates Wnt in breast cancer
  publication-title: Cell Cycle
  doi: 10.4161/cc.6.21.4880
  contributor:
    fullname: Cole
– volume: 37
  start-page: 1105
  year: 2017
  end-page: 1112
  ident: CR14
  article-title: Identification of methylation profiles of cancer-related genes in circulating tumor cells population
  publication-title: Anticancer Res.
  doi: 10.21873/anticanres.11423
  contributor:
    fullname: Lyberopoulou
– volume: 20
  start-page: 30
  year: 2021
  ident: CR15
  article-title: Selective treatment pressure in colon cancer drives the molecular profile of resistant circulating tumor cell clones
  publication-title: Mol. Cancer
  doi: 10.1186/s12943-021-01326-6
  contributor:
    fullname: Cayrefourcq
– volume: 9
  start-page: 534
  year: 2016
  end-page: 546
  ident: CR30
  article-title: DNA hypomethylation contributes to genomic instability and intestinal cancer initiation
  publication-title: Cancer Prev. Res.
  doi: 10.1158/1940-6207.CAPR-15-0349
  contributor:
    fullname: Kaestner
– volume: 25
  start-page: 4116
  year: 2006
  end-page: 4121
  ident: CR40
  article-title: Epigenetic inactivation of the Wnt antagonist DICKKOPF-1 (DKK-1) gene in human colorectal cancer
  publication-title: Oncogene
  doi: 10.1038/sj.onc.1209439
  contributor:
    fullname: Aguilera
– volume: 18
  start-page: 1278
  year: 2019
  end-page: 1286
  ident: CR37
  article-title: Hypermethylation of the PTTG1IP promoter leads to low expression in early-stage non-small cell lung cancer
  publication-title: Oncol. Lett.
  doi: 10.3892/ol.2019.10400
  contributor:
    fullname: Tan
– volume: 14
  start-page: 101174
  year: 2021
  ident: CR2
  article-title: Global colorectal cancer burden in 2020 and projections to 2040
  publication-title: Transl. Oncol.
  doi: 10.1016/j.tranon.2021.101174
  contributor:
    fullname: Xu
– volume: 70
  start-page: 427
  year: 2005
  end-page: 433
  ident: CR19
  article-title: Aberrant gene silencing in tumor progression: implications for control of cancer
  publication-title: Cold Spring Harb. Symp. Quant. Biol.
  doi: 10.1101/sqb.2005.70.010
  contributor:
    fullname: Chen
– volume: 38
  start-page: 821
  year: 2020
  end-page: 830
  ident: CR47
  article-title: A phase 1b dose escalation study of Wnt pathway inhibitor vantictumab in combination with nab-paclitaxel and gemcitabine in patients with previously untreated metastatic pancreatic cancer
  publication-title: Invest. New Drugs
  doi: 10.1007/s10637-019-00824-1
  contributor:
    fullname: Davis
– volume: 358
  start-page: 1148
  year: 2008
  end-page: 1159
  ident: CR29
  article-title: Epigenetics in cancer
  publication-title: N. Engl. J. Med.
  doi: 10.1056/NEJMra072067
  contributor:
    fullname: Esteller
– volume: 75
  start-page: 892
  year: 2015
  end-page: 901
  ident: CR9
  article-title: Establishment and characterization of a cell line from human circulating colon cancer cells
  publication-title: Can. Res.
  doi: 10.1158/0008-5472.CAN-14-2613
  contributor:
    fullname: Cayrefourcq
– volume: 12
  start-page: e11908
  year: 2020
  ident: CR8
  article-title: Characterization of circulating breast cancer cells with tumorigenic and metastatic capacity
  publication-title: EMBO Mol. Med.
  doi: 10.15252/emmm.201911908
  contributor:
    fullname: Koch
– volume: 107
  start-page: 2598
  year: 2010
  end-page: 2603
  ident: CR26
  article-title: Genetic inactivation of AKT1, AKT2, and PDPK1 in human colorectal cancer cells clarifies their roles in tumor growth regulation
  publication-title: Proc. Natl. Acad. Sci. USA
  doi: 10.1073/pnas.0914018107
  contributor:
    fullname: Ericson
– volume: 11
  start-page: 2156
  year: 2005
  end-page: 2162
  ident: CR13
  article-title: Distinct hypermethylation profile of primary breast cancer is associated with sentinel lymph node metastasis
  publication-title: Clin. Cancer Res.
  doi: 10.1158/1078-0432.CCR-04-1810
  contributor:
    fullname: Shinozaki
– volume: 26
  start-page: 601
  year: 2016
  end-page: 611
  ident: CR34
  article-title: Enhancer methylation dynamics contribute to cancer plasticity and patient mortality
  publication-title: Genome Res.
  doi: 10.1101/gr.197194.115
  contributor:
    fullname: Bell
– volume: 68
  start-page: 394
  year: 2018
  end-page: 424
  ident: CR1
  article-title: Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries
  publication-title: CA Cancer J. Clin.
  doi: 10.3322/caac.21492
  contributor:
    fullname: Bray
– year: 2021
  ident: CR4
  article-title: Is there one key step in the metastatic cascade?
  publication-title: Cancers
  doi: 10.3390/cancers13153693
  contributor:
    fullname: Dujon
– volume: 63
  start-page: 700
  year: 2017
  end-page: 713
  ident: CR10
  article-title: Molecular portrait of metastasis-competent circulating tumor cells in colon cancer reveals the crucial role of genes regulating energy metabolism and DNA repair
  publication-title: Clin. Chem.
  doi: 10.1373/clinchem.2016.263582
  contributor:
    fullname: Alix-Panabieres
– volume: 27
  start-page: 4077
  year: 2021
  end-page: 4088
  ident: CR31
  article-title: Circulating tumor cell chromosomal instability and neuroendocrine phenotype by immunomorphology and poor outcomes in men with mCRPC treated with abiraterone or enzalutamide
  publication-title: Clin. Cancer Res.
  doi: 10.1158/1078-0432.CCR-20-3471
  contributor:
    fullname: Brown
– volume: 331
  start-page: 1559
  year: 2011
  end-page: 1564
  ident: CR23
  article-title: A perspective on cancer cell metastasis
  publication-title: Science
  doi: 10.1126/science.1203543
  contributor:
    fullname: Weinberg
– volume: 6
  start-page: 28010
  year: 2016
  ident: CR32
  article-title: Characterization of different CTC subpopulations in non-small cell lung cancer
  publication-title: Sci. Rep.
  doi: 10.1038/srep28010
  contributor:
    fullname: Hanssen
– volume: 23
  start-page: 1658
  year: 2009
  end-page: 1666
  ident: CR44
  article-title: Wnt signaling pathway is epigenetically regulated by methylation of Wnt antagonists in acute myeloid leukemia
  publication-title: Leukemia
  doi: 10.1038/leu.2009.86
  contributor:
    fullname: Valencia
– year: 2019
  ident: CR28
  article-title: Cancer cell lines are useful model systems for medical research
  publication-title: Cancers
  doi: 10.3390/cancers11081098
  contributor:
    fullname: Salvatore
– volume: 228
  start-page: 230
  year: 2012
  end-page: 240
  ident: CR12
  article-title: Epigenetic disruption of cadherin-11 in human cancer metastasis
  publication-title: J. Pathol.
  doi: 10.1002/path.4011
  contributor:
    fullname: Carmona
– volume: 10
  start-page: 1625
  year: 2019
  end-page: 1636
  ident: CR20
  article-title: DNA hypomethylation-related overexpression of SFN, GORASP2 and ZYG11A is a novel prognostic biomarker for early stage lung adenocarcinoma
  publication-title: Oncotarget
  doi: 10.18632/oncotarget.26676
  contributor:
    fullname: Husni
– volume: 31
  start-page: 966
  year: 2014
  ident: CR43
  article-title: Overexpression of Dickkopf-1 predicts poor prognosis for patients with hepatocellular carcinoma after orthotopic liver transplantation by promoting cancer metastasis and recurrence
  publication-title: Med. Oncol.
  doi: 10.1007/s12032-014-0966-8
  contributor:
    fullname: Huang
– volume: 177
  start-page: 1753
  year: 2007
  end-page: 1758
  ident: CR18
  article-title: Discovery and validation of 3 novel DNA methylation markers of prostate cancer prognosis
  publication-title: J. Urol.
  doi: 10.1016/j.juro.2007.01.010
  contributor:
    fullname: Cottrell
– volume: 262
  start-page: 3762
  year: 1987
  end-page: 3767
  ident: CR16
  article-title: A novel cell line (Caco-2) for the study of intestinal lipoprotein synthesis
  publication-title: J. Biol. Chem.
  doi: 10.1016/S0021-9258(18)61420-6
  contributor:
    fullname: Hughes
– volume: 6
  start-page: 404
  year: 2021
  ident: CR6
  article-title: Circulating tumor cells: Biology and clinical significance
  publication-title: Signal Transduct. Target. Ther.
  doi: 10.1038/s41392-021-00817-8
  contributor:
    fullname: Lin
– year: 2016
  ident: CR36
  article-title: Wnt signaling in cancer stem cell biology
  publication-title: Cancers
  doi: 10.3390/cancers8070060
  contributor:
    fullname: Vermeulen
– volume: 41
  start-page: 178
  year: 2009
  end-page: 186
  ident: CR35
  article-title: The human colon cancer methylome shows similar hypo- and hypermethylation at conserved tissue-specific CpG island shores
  publication-title: Nat. Genet.
  doi: 10.1038/ng.298
  contributor:
    fullname: Irizarry
– volume: 24
  start-page: 6160
  year: 2018
  end-page: 6167
  ident: CR42
  article-title: A phase I trial of a guadecitabine (SGI-110) and irinotecan in metastatic colorectal cancer patients previously exposed to irinotecan
  publication-title: Clin. Cancer Res.
  doi: 10.1158/1078-0432.CCR-18-0421
  contributor:
    fullname: Lee
– volume: 169
  start-page: 118
  year: 2021
  end-page: 136
  ident: CR45
  article-title: Therapeutic targeting of the oncogenic Wnt signaling pathway for treating colorectal cancer and other colonic disorders
  publication-title: Adv. Drug Deliv. Rev.
  doi: 10.1016/j.addr.2020.12.010
  contributor:
    fullname: Rosin-Arbesfeld
– volume: 113
  start-page: E7535
  year: 2016
  end-page: E7544
  ident: CR21
  article-title: Epigenetic inactivation of the p53-induced long noncoding RNA TP53 target 1 in human cancer
  publication-title: Proc. Natl. Acad. Sci. USA
  doi: 10.1073/pnas.1608585113
  contributor:
    fullname: Diaz-Lagares
– volume: 228
  start-page: 230
  year: 2012
  ident: 42037_CR12
  publication-title: J. Pathol.
  doi: 10.1002/path.4011
  contributor:
    fullname: FJ Carmona
– volume: 169
  start-page: 118
  year: 2021
  ident: 42037_CR45
  publication-title: Adv. Drug Deliv. Rev.
  doi: 10.1016/j.addr.2020.12.010
  contributor:
    fullname: M Caspi
– volume: 177
  start-page: 1753
  year: 2007
  ident: 42037_CR18
  publication-title: J. Urol.
  doi: 10.1016/j.juro.2007.01.010
  contributor:
    fullname: S Cottrell
– volume: 11
  start-page: 2156
  year: 2005
  ident: 42037_CR13
  publication-title: Clin. Cancer Res.
  doi: 10.1158/1078-0432.CCR-04-1810
  contributor:
    fullname: M Shinozaki
– year: 2021
  ident: 42037_CR4
  publication-title: Cancers
  doi: 10.3390/cancers13153693
  contributor:
    fullname: AM Dujon
– volume: 32
  start-page: 2847
  year: 2016
  ident: 42037_CR17
  publication-title: Bioinformatics
  doi: 10.1093/bioinformatics/btw313
  contributor:
    fullname: Z Gu
– volume: 21
  start-page: 144
  year: 2022
  ident: 42037_CR49
  publication-title: Mol. Cancer
  doi: 10.1186/s12943-022-01616-7
  contributor:
    fullname: H Zhao
– volume: 41
  start-page: 178
  year: 2009
  ident: 42037_CR35
  publication-title: Nat. Genet.
  doi: 10.1038/ng.298
  contributor:
    fullname: RA Irizarry
– volume: 68
  start-page: 394
  year: 2018
  ident: 42037_CR1
  publication-title: CA Cancer J. Clin.
  doi: 10.3322/caac.21492
  contributor:
    fullname: F Bray
– volume: 169
  start-page: 985
  year: 2017
  ident: 42037_CR46
  publication-title: Cell
  doi: 10.1016/j.cell.2017.05.016
  contributor:
    fullname: R Nusse
– volume: 18
  start-page: 1278
  year: 2019
  ident: 42037_CR37
  publication-title: Oncol. Lett.
  doi: 10.3892/ol.2019.10400
  contributor:
    fullname: X Tan
– volume: 25
  start-page: 4116
  year: 2006
  ident: 42037_CR40
  publication-title: Oncogene
  doi: 10.1038/sj.onc.1209439
  contributor:
    fullname: O Aguilera
– volume: 23
  start-page: 1658
  year: 2009
  ident: 42037_CR44
  publication-title: Leukemia
  doi: 10.1038/leu.2009.86
  contributor:
    fullname: A Valencia
– volume: 12
  start-page: e11908
  year: 2020
  ident: 42037_CR8
  publication-title: EMBO Mol. Med.
  doi: 10.15252/emmm.201911908
  contributor:
    fullname: C Koch
– volume: 6
  start-page: 2625
  year: 2007
  ident: 42037_CR38
  publication-title: Cell Cycle
  doi: 10.4161/cc.6.21.4880
  contributor:
    fullname: VH Cowling
– volume: 176
  start-page: 98
  year: 2019
  ident: 42037_CR33
  publication-title: Cell
  doi: 10.1016/j.cell.2018.11.046
  contributor:
    fullname: S Gkountela
– volume: 331
  start-page: 1559
  year: 2011
  ident: 42037_CR23
  publication-title: Science
  doi: 10.1126/science.1203543
  contributor:
    fullname: CL Chaffer
– volume: 70
  start-page: 427
  year: 2005
  ident: 42037_CR19
  publication-title: Cold Spring Harb. Symp. Quant. Biol.
  doi: 10.1101/sqb.2005.70.010
  contributor:
    fullname: SB Baylin
– volume: 97
  start-page: 695
  year: 1953
  ident: 42037_CR25
  publication-title: J. Exp. Med.
  doi: 10.1084/jem.97.5.695
  contributor:
    fullname: WF Scherer
– volume: 71
  start-page: 209
  year: 2021
  ident: 42037_CR3
  publication-title: CA Cancer J. Clin.
  doi: 10.3322/caac.21660
  contributor:
    fullname: H Sung
– volume: 31
  start-page: 966
  year: 2014
  ident: 42037_CR43
  publication-title: Med. Oncol.
  doi: 10.1007/s12032-014-0966-8
  contributor:
    fullname: Y Huang
– volume: 38
  start-page: 821
  year: 2020
  ident: 42037_CR47
  publication-title: Invest. New Drugs
  doi: 10.1007/s10637-019-00824-1
  contributor:
    fullname: SL Davis
– volume: 24
  start-page: 6160
  year: 2018
  ident: 42037_CR42
  publication-title: Clin. Cancer Res.
  doi: 10.1158/1078-0432.CCR-18-0421
  contributor:
    fullname: V Lee
– volume: 37
  start-page: 1105
  year: 2017
  ident: 42037_CR14
  publication-title: Anticancer Res.
  doi: 10.21873/anticanres.11423
  contributor:
    fullname: A Lyberopoulou
– volume: 7
  start-page: 1389
  year: 2017
  ident: 42037_CR48
  publication-title: Am. J. Cancer Res.
  contributor:
    fullname: L Santiago
– volume: 75
  start-page: 892
  year: 2015
  ident: 42037_CR9
  publication-title: Can. Res.
  doi: 10.1158/0008-5472.CAN-14-2613
  contributor:
    fullname: L Cayrefourcq
– volume: 126
  start-page: 2584
  year: 2010
  ident: 42037_CR41
  publication-title: Int. J. Cancer
  doi: 10.1002/ijc.24981
  contributor:
    fullname: S Gotze
– volume: 262
  start-page: 3762
  year: 1987
  ident: 42037_CR16
  publication-title: J. Biol. Chem.
  doi: 10.1016/S0021-9258(18)61420-6
  contributor:
    fullname: TE Hughes
– volume: 9
  start-page: 622459
  year: 2021
  ident: 42037_CR11
  publication-title: Front. Cell Dev. Biol.
  doi: 10.3389/fcell.2021.622459
  contributor:
    fullname: A Rodriguez-Casanova
– volume: 12
  start-page: 31
  year: 2022
  ident: 42037_CR22
  publication-title: Cancer Discov.
  doi: 10.1158/2159-8290.CD-21-1059
  contributor:
    fullname: D Hanahan
– volume: 14
  start-page: 86
  year: 2022
  ident: 42037_CR27
  publication-title: Clin. Epigenet.
  doi: 10.1186/s13148-022-01302-x
  contributor:
    fullname: J Ruiz-Banobre
– volume: 10
  start-page: 1625
  year: 2019
  ident: 42037_CR20
  publication-title: Oncotarget
  doi: 10.18632/oncotarget.26676
  contributor:
    fullname: RE Husni
– year: 2016
  ident: 42037_CR36
  publication-title: Cancers
  doi: 10.3390/cancers8070060
  contributor:
    fullname: EMF de Sousa
– volume: 127
  start-page: 800
  year: 2022
  ident: 42037_CR5
  publication-title: Br. J. Cancer
  doi: 10.1038/s41416-022-01819-1
  contributor:
    fullname: SZ Eslami
– volume: 103
  start-page: 828
  year: 2012
  ident: 42037_CR39
  publication-title: Cancer Sci.
  doi: 10.1111/j.1349-7006.2012.02222.x
  contributor:
    fullname: L Qi
– volume: 14
  start-page: 101174
  year: 2021
  ident: 42037_CR2
  publication-title: Transl. Oncol.
  doi: 10.1016/j.tranon.2021.101174
  contributor:
    fullname: Y Xi
– volume: 27
  start-page: 4077
  year: 2021
  ident: 42037_CR31
  publication-title: Clin. Cancer Res.
  doi: 10.1158/1078-0432.CCR-20-3471
  contributor:
    fullname: LC Brown
– volume: 26
  start-page: 3213
  year: 2008
  ident: 42037_CR7
  publication-title: J. Clin. Oncol.
  doi: 10.1200/JCO.2007.15.8923
  contributor:
    fullname: SJ Cohen
– volume: 20
  start-page: 30
  year: 2021
  ident: 42037_CR15
  publication-title: Mol. Cancer
  doi: 10.1186/s12943-021-01326-6
  contributor:
    fullname: L Cayrefourcq
– volume: 113
  start-page: E7535
  year: 2016
  ident: 42037_CR21
  publication-title: Proc. Natl. Acad. Sci. USA
  doi: 10.1073/pnas.1608585113
  contributor:
    fullname: A Diaz-Lagares
– volume: 127
  start-page: 679
  year: 2006
  ident: 42037_CR24
  publication-title: Cell
  doi: 10.1016/j.cell.2006.11.001
  contributor:
    fullname: GP Gupta
– volume: 107
  start-page: 2598
  year: 2010
  ident: 42037_CR26
  publication-title: Proc. Natl. Acad. Sci. USA
  doi: 10.1073/pnas.0914018107
  contributor:
    fullname: K Ericson
– volume: 358
  start-page: 1148
  year: 2008
  ident: 42037_CR29
  publication-title: N. Engl. J. Med.
  doi: 10.1056/NEJMra072067
  contributor:
    fullname: M Esteller
– volume: 6
  start-page: 404
  year: 2021
  ident: 42037_CR6
  publication-title: Signal Transduct. Target. Ther.
  doi: 10.1038/s41392-021-00817-8
  contributor:
    fullname: D Lin
– volume: 26
  start-page: 601
  year: 2016
  ident: 42037_CR34
  publication-title: Genome Res.
  doi: 10.1101/gr.197194.115
  contributor:
    fullname: RE Bell
– volume: 6
  start-page: 28010
  year: 2016
  ident: 42037_CR32
  publication-title: Sci. Rep.
  doi: 10.1038/srep28010
  contributor:
    fullname: A Hanssen
– volume: 9
  start-page: 534
  year: 2016
  ident: 42037_CR30
  publication-title: Cancer Prev. Res.
  doi: 10.1158/1940-6207.CAPR-15-0349
  contributor:
    fullname: KL Sheaffer
– volume: 63
  start-page: 700
  year: 2017
  ident: 42037_CR10
  publication-title: Clin. Chem.
  doi: 10.1373/clinchem.2016.263582
  contributor:
    fullname: C Alix-Panabieres
– year: 2019
  ident: 42037_CR28
  publication-title: Cancers
  doi: 10.3390/cancers11081098
  contributor:
    fullname: P Mirabelli
SSID ssj0000529419
Score 2.469655
Snippet Circulating tumor cells (CTCs) and epigenetic alterations are involved in the development of metastasis from solid tumors, such as colorectal cancer (CRC). The...
Abstract Circulating tumor cells (CTCs) and epigenetic alterations are involved in the development of metastasis from solid tumors, such as colorectal cancer...
Abstract Circulating tumor cells (CTCs) and epigenetic alterations are involved in the development of metastasis from solid tumors, such as colorectal cancer...
SourceID doaj
pubmedcentral
proquest
crossref
springer
SourceType Open Website
Open Access Repository
Aggregation Database
Publisher
StartPage 15401
SubjectTerms 631/67/322
692/4028/67
Cancer
Colorectal cancer
Colorectal carcinoma
CpG islands
Deoxyribonucleic acid
DNA
DNA methylation
Epigenetics
Gene regulation
Humanities and Social Sciences
Metastases
Metastasis
multidisciplinary
Science
Science (multidisciplinary)
Solid tumors
Therapeutic targets
Tumor cells
Wnt protein
SummonAdditionalLinks – databaseName: DOAJ Directory of Open Access Journals
  dbid: DOA
  link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwrV3NbxUhECemiYkX42dcbQ0m3nTTx8KycGy1TeOhJ5v0RoAd9B26r3lvX5oe_c-dgX2128R48Qq7AeaDGWDmN4x9jAaEbgFqCBpqZYWvjRakV1J20VNVkRwge67PLtS3y_byXqkvigkr8MCFcId0aQn9IgRvgvKdCW0P6BJrq5KPquvz7ruw9w5TBdW7sUrYKUtmIc3hBi0VZZM1slYN5cbdzCxRBuyfeZkPYyQfPJRm-3P6jD2dHEd-VCb8nD2C4QV7XEpJ3r5kv06uM97q1TJyPwGNcIJnQvHinm8zTiv_en7EqWb0bYmA41N0Fl8lavboKeJvdZx86ZHH5Trm-l7DDz5ur1ZrThf9G74cOKFd026Jc4okOetX7OL05PuXs3oqr1DHVpixtlEmlZAoqZVhEQMabmk8tIYg35MhIMK2hS7ikcejX2mTMVErPO74lPBM3cvXbG9YDfCGcdklBUYBpCYo0SdLXPNaCFCALkBXsU87UrvrgqLh8uu3NK4wxiFjXGaMu6nYMXHj7ktCwM4NKBdukgv3L7mo2P6Ol25Sy42jNFwcREhdsQ933ahQRDw_wGpbviFUJmsqZmYyMJvQvGdY_szQ3IIKAwrVVOzzTlz-jP73Fb_9Hyt-x540JN5U30Lvs71xvYUD9JjG8D4rx28_uRXG
  priority: 102
  providerName: Directory of Open Access Journals
– databaseName: Health & Medical Collection
  dbid: 7X7
  link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwfV1Nb9QwELWgCIkL4lMECjISN7C6jh3bOaECrSoOPVFpb5bjjMsemmyzWVU98s_xON6tUgmudhI7nrE9Mx6_R8gnb4CrCoBBo4DJmjtmFMd5JYT2DllFUoLsuTq7kD-X1TIH3DY5rXK3JqaFuu09xsiP8AalLBFh7Ov6miFrFJ6uZgqNh-QRLxcKU7r0Uu9jLHiKJXmd78oshDnaxP0K75SVgsWPCc1uZvtRgu2f2Zr3MyXvHZemXej0GXmazUd6PMn7OXkA3QvyeCKUvH1J_pysE-rq1cpTl-FGKII0RSWjjm4TWiv9cX5MkTn6dsqDozlHi_YBi120F-NrzGeLeqR-NfjE8tVd0nF71Q8Uw_0buuooYl7jmhn75FF_hlfk4vTk1_czlkkWmK-4GVntRZAhDkqoRLPwTdy-hXFQGQR-DwbhCKsKtI-Oj4vWZR2M8UpGp8eFED3rVrwmB13fwRtChQ4SjAQIZSN5G2oMODvFOUiIhoAuyOfdUNv1hKVh0xm4MHYSjI2CsUkw9qYg31Aa-ycRBzsV9MOlzdPKYgvQLprGmUY6bZqqhegwqVoG56VuC3K4k6XNk3Nj71SpIB_31XFa4eC5Dvrt9AxiM9WmIGamA7MOzWu61e8E0M2RHpDLsiBfdupy1_q___jt_zv7jjxBrntMVuHqkByMwxbeR4tobD4ktf8LYEMMYg
  priority: 102
  providerName: ProQuest
– databaseName: Scholars Portal Open Access Journals
  dbid: M48
  link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwjV1Lb9QwEB6VIiQuFeUhUgoyEjcI1LGTOAeESmlVceiJlXqzHMcuK9GkZLMqe-SfM-M4RamKxDW25ceM4xl75vsA3ljleJE7l7q6cKmsuElVwWlfCVFaQ6wiIUD2rDhdyK_n-fkWTHRHcQFXd7p2xCe16H-8__Vz8wk3_McxZVx9WOEhRIlimUhlRmlv1_fgfibRU6dQvmjuj1jfWSV5FXNn7m46O58CjP_M9rwdOXnr-TScSiePYCeak-xwlP8ubLn2MTwYCSY3T-D38VVAYb1cWmYi_Agj0CacPDNsHdBb2ZezQ0ZM0psxLo7FmC3Wefps0H7EZqmNFvbA7LK3gfWrvWDD-rLrGV3_r9iyZYSBTf9QHJMlfeqfwuLk-NvRaRpJF1KbczWklRVeelwUn4v6wNZ4nAtlXK4ICN4rgifMc1dadIQMWpuVV8oWEp0g4z162o14Bttt17rnwETppVPSOZ_Vkje-ogtoU3DupEPDoEzg7bTU-mrE1tDhTVwoPQpGo2B0EIy-TuAzSeOmJuFihw9df6HjNtPUg2sO6tqoWppS1Xnj0IEqKumNlWWTwP4kSz3pmqbkXOyEiyKB1zfFuM1o8UzruvVYh7CaKpWAmunAbEDzknb5PQB2c6IL5DJL4N2kLn97__eM9_5jNC_gYUbaS6QWxT5sD_3avUQzaahfBd3_A_ZzEfc
  priority: 102
  providerName: Scholars Portal
– databaseName: Springer Open Access
  dbid: C6C
  link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwlV3Nb9UwDLdgCInLxKcoDJRJ3KBieUnT9Dgem6YddmLSblGSOvAO65ve69O0I__57LTvoU5w4NokTRrbtZ3YPwN8ihalqRBLDAZL3UhfWiNZrpSqo-eqIjlA9sKcXerzq-pqhMnhXJjJ_b2yX9ekYDgJbKZKPeOUttvH8IReYDl8a27mu_MUvrHSshnzYv4-dKJ7MkT_xK58GBX54Go0a5zT57A_morieKDtC3iE3Ut4OhSPvHsFv09uMsLq9SIKP0KLCAZkIoYSXmwyMqv4fnEsuEr03RDzJsZ4LLFM_NiTbUjDyjhaz72Ii1XMFb26n6LfXC9Xgo_212LRCca35v8jrSkyr6xew-XpyY_5WTkWVChjJW1fNlElnWhTUqXCUQykqpX1WFkGeU-WoQerCutITo4nS7JJ1kajycHxKZEX3ao3sNctO3wLQtVJo9WIaRa0bFPDh8veSIkaSenXBXzebrW7GXAzXL7vVtYNhHFEGJcJ424L-MbU2PVkzOv8gFjBjSLkeAZsj0LwNmhf21C1SM6RaXTyUddtAQdbWrpRENeOE29pEqlMAYe7ZhIh3jzf4XIz9GEcpsYWYCc8MFnQtKVb_Mpg3JJLAUo9K-DLll3-zP7vL373f93fwzOuc8-BKtIcwF6_2uAHsob68DGLwT3tUQXe
  priority: 102
  providerName: Springer Nature
Title Epigenomic analysis reveals a unique DNA methylation program of metastasis-competent circulating tumor cells in colorectal cancer
URI https://link.springer.com/article/10.1038/s41598-023-42037-w
https://www.proquest.com/docview/2865420136
https://search.proquest.com/docview/2865780498
https://pubmed.ncbi.nlm.nih.gov/PMC10505142
https://doaj.org/article/2304ed0bba8b4a78b5de826694fac47d
Volume 13
hasFullText 1
inHoldings 1
isFullTextHit
isPrint
link http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV3da9swED_ajo2-jH0yb13QYG-bm8iSZfmxzVLKoKGMFfJmZEVqA4sTHIfSx_3nu5PtrinsZS8GfyFZ9zvrTrr7HcBnqx1XqXOxK5WLZc5NrBUnvRIis4aqioQA2ak6v5LfZ-lsD1SfCxOC9m25OK5-LY-rxU2IrVwv7bCPExteXow5lV_jMhnuwz4i9IGP3jJ6J7nkeZchMxJ6uMFZijLJEhHLhPLibg_hmcjQkxkRWf-DCSnw9u8Ym49DJR_tl4Zp6OwFPO_sR3bS9vMl7LnqFTxtK0revYbfk3WgXV0uLDMd3wgjliZEGTNsG-ha2bfpCaPS0XdtIBzrgrTYytNlgwYjvhbbzqRumF3UNpT5qq5Zs12uakbr_Ru2qBiRXtNPE_tkCUD1G7g6m_wcn8ddlYXYplw3cW6Flx7Hx6eiHNkS52-hjUs1Mb97TXyEaeoyi56PQfMy91pbJdHrMd6jaz0Xb-GgWlXuHTCReem0dM4npeRzn9OKs1GcO-nQEsgi-NIPdbFuyTSKsAkudNHKqEAZFUFGxW0EpySN-yeJCDtcWNXXRQeHglpw81FZGl1Kk-kynTv0mFQuvbEym0dw1Muy6LRzU1A2LjbChYrg0_1t1CsaPFO51bZ9hsiZch2B3sHATod27yBgA0N3D9AIvvZw-dv6v7_4_f-39AEOE8I3FbdQR3DQ1Fv3Ec2lphygjsyyATw5nUwvf-DZWI0HYekBjxdSD4L2_AFGRhrc
link.rule.ids 230,315,730,783,787,867,888,2109,12068,21400,24330,27936,27937,31731,31732,33756,33757,41132,42201,43322,43817,51588,53804,53806,74073,74630
linkProvider National Library of Medicine
linkToHtml http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwfV1Lb9QwEB5BKwQXxFMNFDASN7C6jp3EOaEWtlqgrBBqpd4sx7HLHpos2ayqHvnneBzvVqkEV-fleGbsmfH4-wDeGWlZnllLbZVbKkqmqcwZ2hXnhdHIKhIKZOf57Ex8Pc_OY8JtFcsqN3NimKjr1mCO_ABPUIoUEcY-Ln9TZI3C3dVIoXEXdhGqygdfu0fT-Y-f2ywL7mMJVsbTMhMuD1Z-xcJTZSmn_nW8oFejFSkA94-8zdu1krc2TMM6dPwIHkYHkhwOEn8Md2zzBO4NlJLXT-HPdBlwVy8XhugIOEIQpsmrGdFkHfBayef5IUHu6OuhEo7EKi3SOmzW3mP0j1ETfeqemEVnAs9Xc0H69WXbEUz4r8iiIYh6jbOm75NBDeqewdnx9PTTjEaaBWoyJntaGu6E84PiMl5NTOUXcC61zSRCvzuJgIRZZgvjQx_t_cvSSWly4cMe7ZyPrWv-HHaatrF7QHjhhJXCWpdWgtWuxJSzzhmzwnpXoEjg_Wao1XJA01BhF5xLNQhGecGoIBh1lcARSmN7JyJhh4a2u1DRsBR-wdaTqtKyErqQVVZbHzLlpXDaiKJOYH8jSxXNc6VulCmBt9vL3rBw8HRj2_VwD6IzlTIBOdKBUYfGV5rFrwDRzZAgkIk0gQ8bdbn5-r__-MX_O_sG7s9Ov5-oky_zby_hQYpKjGwW-T7s9N3avvL-UV-9jkbwF69BELg
linkToPdf http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwfV3db9MwED9BJxAviE-RbYCReAOrde0kzhPaWKvxoWpCTNqb5Tj26MOSkqaa9sh_js9xO2USvNpJ7Pju7Dv7_PsBvDfSsiy1ltoys1QUTFOZMbQrznOjkVUkJMgustNz8fUivYj5T-uYVrmdE8NEXTUG98jHeINSTBFhbOxiWsTZyfzT6jdFBik8aY10GvdhLxcZn4xg73i2OPux23HBMy3BinhzZsLleO1XL7xhNuXUf5rn9HqwOgUQ_4HneTdv8s7haViT5k_gcXQmyVEv_adwz9bP4EFPL3nzHP7MVgGD9WppiI7gIwQhm7zKEU02AbuVnCyOCPJI3_RZcSRmbJHGYbH23qN_jZroX3fELFsTOL_qS9JtrpqW4Ob_mixrggjYOIP6PhnUpvYFnM9nPz-f0ki5QE3KZEcLw51wflBcysuJKf1izqW2qUQYeCcRnDBNbW58GKS9r1k4KU0mfAiknfNxdsVfwqhuavsKCM-dsFJY66alYJUrcPtZZ4xZYb1bkCfwYTvUatUja6hwIs6l6gWjvGBUEIy6TuAYpbF7ElGxQ0HTXqpoZApbsNWkLLUshc5lmVbWh09ZIZw2Iq8SONzKUkVTXatbxUrg3a7aGxkOnq5ts-mfQaSmQiYgBzow6NCwpl7-CnDdDMkCmZgm8HGrLret__uP9__f2bfw0Ou_-v5l8e0AHk1Rh5HYIjuEUddu7GvvKnXlm2gDfwFN3xTm
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=Epigenomic+analysis+reveals+a+unique+DNA+methylation+program+of+metastasis-competent+circulating+tumor+cells+in+colorectal+cancer&rft.jtitle=Scientific+reports&rft.au=Bao-Caamano%2C+Aida&rft.au=Costa-Fraga%2C+Nicol%C3%A1s&rft.au=Cayrefourcq%2C+Laure&rft.au=J%C3%A1come%2C+Mar%C3%ADa+Amalia&rft.date=2023-09-16&rft.eissn=2045-2322&rft.volume=13&rft.issue=1&rft.spage=15401&rft.epage=15401&rft_id=info:doi/10.1038%2Fs41598-023-42037-w&rft.externalDBID=NO_FULL_TEXT
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=2045-2322&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=2045-2322&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=2045-2322&client=summon