L1CAM defines the regenerative origin of metastasis-initiating cells in colorectal cancer.

Animals Colorectal Neoplasms / pathology Humans Mice Neoplasm Metastasis Neural Cell Adhesion Molecule L1 / genetics

Journal

Nature cancer
ISSN: 2662-1347
Titre abrégé: Nat Cancer
Pays: England
ID NLM: 101761119

Informations de publication

Date de publication:
01 2020
Historique:
entrez: 14 7 2020
pubmed: 14 7 2020
medline: 14 7 2020
Statut: ppublish

Résumé

Metastasis-initiating cells with stem-like properties drive cancer lethality, yet their origins and relationship to primary-tumor-initiating stem cells are not known. We show that L1CAM

Identifiants

DOI: 10.1038/s43018-019-0006-x PMID: 32656539 PMC: PMC7351134
pubmed: 32656539
doi: 10.1038/s43018-019-0006-x
pmc: PMC7351134
mid: NIHMS1595275
pii: 10.1038/s43018-019-0006-x
doi:

Substances chimiques

L1CAM protein, human 0
Neural Cell Adhesion Molecule L1 0

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Pagination

28-45

Subventions

Organisme : NIH HHS
ID : U54 OD020355
Pays : United States
Organisme : NCI NIH HHS
ID : T32 CA009207
Pays : United States
Organisme : NCI NIH HHS
ID : P30 CA008748
Pays : United States
Organisme : NCI NIH HHS
ID : K08 CA230213
Pays : United States
Organisme : NCI NIH HHS
ID : P01 CA094060
Pays : United States
Organisme : NCATS NIH HHS
ID : KL2 TR002385
Pays : United States
Organisme : NIGMS NIH HHS
ID : T32 GM007739
Pays : United States
Organisme : NCI NIH HHS
ID : P01 CA129243
Pays : United States
Organisme : NCI NIH HHS
ID : R25 CA020449
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA182551
Pays : United States
Organisme : NCI NIH HHS
ID : U54 CA209975
Pays : United States
Organisme : NCI NIH HHS
ID : F30 CA203238
Pays : United States

Commentaires et corrections

Type : CommentIn
Type : ErratumIn

Déclaration de conflit d'intérêts

Competing interests J.M. is a science advisor for and owns company stock in Scholar Rock.

Références

Batlle, E. & Clevers, H. Cancer stem cells revisited. Nat. Med. 23, 1124–1134 (2017).
pubmed: 28985214
Celia-Terrassa, T. & Kang, Y. Distinctive properties of metastasis-initiating cells. Genes Dev. 30, 892–908 (2016).
pubmed: 27083997 pmcid: 4840296
Lambert, A. W., Pattabiraman, D. R. & Weinberg, R. A. Emerging biological principles of metastasis. Cell 168, 670–691 (2017).
pubmed: 5308465 pmcid: 5308465
Massague, J. & Obenauf, A. C. Metastatic colonization by circulating tumour cells. Nature 529, 298–306 (2016).
pubmed: 26791720 pmcid: 5029466
Reya, T., Morrison, S. J., Clarke, M. F. & Weissman, I. L. Stem cells, cancer, and cancer stem cells. Nature 414, 105–111 (2001).
pubmed: 11689955 pmcid: 11689955
Hanahan, D. & Weinberg, R. A. Hallmarks of cancer: the next generation. Cell 144, 646–674 (2011).
pubmed: 21376230
Rathjen, F. G. & Schachner, M. Immunocytological and biochemical characterization of a new neuronal cell surface component (L1 antigen) which is involved in cell adhesion. EMBO J. 3, 1–10 (1984).
pubmed: 6368220 pmcid: 557289
Valiente, M. et al. Serpins promote cancer cell survival and vascular co-option in brain metastasis. Cell 156, 1002–1016 (2014).
pubmed: 24581498 pmcid: 3988473
Er, E. E. et al. Pericyte-like spreading by disseminated cancer cells activates YAP and MRTF for metastatic colonization. Nat. Cell Biol. 20, 966–978 (2018).
pubmed: 30038252 pmcid: 6467203
Altevogt, P., Doberstein, K. & Fogel, M. L1CAM in human cancer. Int. J. Cancer 138, 1565–1576 (2016).
pubmed: 26111503
Sato, T. et al. Long-term expansion of epithelial organoids from human colon, adenoma, adenocarcinoma, and Barrett’s epithelium. Gastroenterology 141, 1762–1772 (2011).
pubmed: 21889923
Jung, P. et al. Isolation and in vitro expansion of human colonic stem cells. Nat. Med. 17, 1225–1227 (2011).
pubmed: 21892181
Barker, N. et al. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 449, 1003–1007 (2007).
pubmed: 17934449
Barker, N. et al. Crypt stem cells as the cells-of-origin of intestinal cancer. Nature 457, 608–611 (2009).
pubmed: 19092804
Ayyaz, A. et al. Single-cell transcriptomes of the regenerating intestine reveal a revival stem cell. Nature 569, 121–125 (2019).
pubmed: 31019301
Pascual, G. et al. Targeting metastasis-initiating cells through the fatty acid receptor CD36. Nature 541, 41–45 (2017).
Hallmann, R. et al. Expression and function of laminins in the embryonic and mature vasculature. Physiol. Rev. 85, 979–1000 (2005).
pubmed: 15987800
Simon-Assmann, P. et al. The laminins: role in intestinal morphogenesis and differentiation. Ann. NY Acad. Sci. 859, 46–64 (1998).
pubmed: 9928369
Kleinman, H. K. et al. Basement membrane complexes with biological activity. Biochemistry 25, 312–318 (1986).
pubmed: 2937447
Lemmon, V., Farr, K. L. & Lagenaur, C. L1-mediated axon outgrowth occurs via a homophilic binding mechanism. Neuron 2, 1597–1603 (1989).
pubmed: 2627381
Hall, H., Carbonetto, S. & Schachner, M. L1/HNK-1 carbohydrate- and β
pubmed: 9003039
Oskarsson, T. et al. Breast cancer cells produce tenascin C as a metastatic niche component to colonize the lungs. Nat. Med. 17, 867–874 (2011).
pubmed: 21706029 pmcid: 4020577
Okayasu, I. et al. A novel method in the induction of reliable experimental acute and chronic ulcerative colitis in mice. Gastroenterology 98, 694–702 (1990).
pubmed: 1688816 pmcid: 1688816
Dahme, M. et al. Disruption of the mouse L1 gene leads to malformations of the nervous system. Nat. Genet. 17, 346–349 (1997).
pubmed: 9354804
Madison, B. B. et al. Cis elements of the villin gene control expression in restricted domains of the vertical (crypt) and horizontal (duodenum, cecum) axes of the intestine. J. Biol. Chem. 277, 33275–33283 (2002).
Ge, Y. et al. Stem cell lineage infidelity drives wound repair and cancer. Cell 169, 636–650 (2017).
pubmed: 28434617 pmcid: 5510746
Dvorak, H. F. Tumors: wounds that do not heal. Similarities between tumor stroma generation and wound healing. N. Engl. J. Med. 315, 1650–1659 (1986).
pubmed: 3537791
Cheung, A. F. et al. Complete deletion of Apc results in severe polyposis in mice. Oncogene 29, 1857–1864 (2010).
pubmed: 20010873
O’Rourke, K. P. et al. Transplantation of engineered organoids enables rapid generation of metastatic mouse models of colorectal cancer. Nat. Biotechnol. 35, 577–582 (2017).
pubmed: 28459450 pmcid: 5462850
Ghidini, M., Petrelli, F. & Tomasello, G. Right versus left colon cancer: resectable and metastatic disease. Curr. Treat. Options Oncol. 19, 31 (2018).
pubmed: 29796712
Bettington, M. et al. The serrated pathway to colorectal carcinoma: current concepts and challenges. Histopathology 62, 367–386 (2013).
pubmed: 23339363
Chen, J. et al. A restricted cell population propagates glioblastoma growth after chemotherapy. Nature 488, 522–526 (2012).
pubmed: 22854781 pmcid: 3427400
Driessens, G., Beck, B., Caauwe, A., Simons, B. D. & Blanpain, C. Defining the mode of tumour growth by clonal analysis. Nature 488, 527–530 (2012).
pubmed: 22854777 pmcid: 5553110
Schepers, A. G. et al. Lineage tracing reveals Lgr5
pubmed: 22855427
He, X. et al. Promotion of spinal cord regeneration by neural stem cell-secreted trimerized cell adhesion molecule L1. PLoS One 7, e46223 (2012).
pubmed: 23049984 pmcid: 3458024
Guseva, D., Loers, G. & Schachner, M. Function-triggering antibodies to the adhesion molecule L1 enhance recovery after injury of the adult mouse femoral nerve. PLoS One 9, e112984 (2014).
pubmed: 25393007 pmcid: 4231121
Schoenherr, C. J. & Anderson, D. J. The neuron-restrictive silencer factor (NRSF): a coordinate repressor of multiple neuron-specific genes. Science 267, 1360–1363 (1995).
pubmed: 7871435
Mukherjee, S., Brulet, R., Zhang, L. & Hsieh, J. REST regulation of gene networks in adult neural stem cells. Nat. Commun. 7, 13360 (2016).
pubmed: 27819263 pmcid: 5103073
Westbrook, T. F. et al. A genetic screen for candidate tumor suppressors identifies REST. Cell 121, 837–848 (2005).
pubmed: 15960972
Kourtidis, A., Lu, R., Pence, L. J. & Anastasiadis, P. Z. A central role for cadherin signaling in cancer. Exp. Cell Res. 358, 78–85 (2017).
pubmed: 28412244 pmcid: 5544584
Chong, J. A. et al. REST: a mammalian silencer protein that restricts sodium channel gene expression to neurons. Cell 80, 949–957 (1995).
pubmed: 7697725
Lim, J. S. et al. Intratumoural heterogeneity generated by Notch signalling promotes small-cell lung cancer. Nature 545, 360–364 (2017).
pubmed: 28489825 pmcid: 5776014
Lapuk, A. V. et al. From sequence to molecular pathology, and a mechanism driving the neuroendocrine phenotype in prostate cancer. J. Pathol. 227, 286–297 (2012).
pubmed: 22553170 pmcid: 3659819
Lin, T. P. et al. REST reduction is essential for hypoxia-induced neuroendocrine differentiation of prostate cancer cells by activating autophagy signaling. Oncotarget 7, 26137–26151 (2016).
pubmed: 27034167 pmcid: 5041970
Denny, S. K. et al. Nfib promotes metastasis through a widespread increase in chromatin accessibility. Cell 166, 328–342 (2016).
pubmed: 27374332 pmcid: 5004630
Roe, J. S. et al. Enhancer reprogramming promotes pancreatic cancer metastasis. Cell 170, 875–888 (2017).
pubmed: 28757253 pmcid: 5726277
Naik, S. et al. Inflammatory memory sensitizes skin epithelial stem cells to tissue damage. Nature 550, 475–480 (2017).
pubmed: 29045388 pmcid: 5808576
Tian, H. et al. A reserve stem cell population in small intestine renders Lgr5-positive cells dispensable. Nature 478, 255–259 (2011).
pubmed: 21927002 pmcid: 4251967
Schwitalla, S. et al. Intestinal tumorigenesis initiated by dedifferentiation and acquisition of stem-cell-like properties. Cell 152, 25–38 (2013).
pubmed: 23273993
Shimokawa, M. et al. Visualization and targeting of LGR5
pubmed: 28355176
Rompolas, P. et al. Spatiotemporal coordination of stem cell commitment during epidermal homeostasis. Science 352, 1471–1474 (2016).
pubmed: 27229141 pmcid: 4958018
Tata, P. R. et al. Dedifferentiation of committed epithelial cells into stem cells in vivo. Nature 503, 218–223 (2013).
pubmed: 24196716 pmcid: 4035230
Stange, D. E. et al. Differentiated Troy
pubmed: 24120136 pmcid: 4094146
Varga, J. & Greten, F. R. Cell plasticity in epithelial homeostasis and tumorigenesis. Nat. Cell Biol. 19, 1133–1141 (2017).
pubmed: 28945230
Yui, S. et al. YAP/TAZ-dependent reprogramming of colonic epithelium links ECM remodeling to tissue regeneration. Cell Stem Cell 22, 35–49 (2018).
pubmed: 29249464 pmcid: 5766831
Blanpain, C., Lowry, W. E., Geoghegan, A., Polak, L. & Fuchs, E. Self-renewal, multipotency, and the existence of two cell populations within an epithelial stem cell niche. Cell 118, 635–648 (2004).
pubmed: 15339667
Stingl, J. et al. Purification and unique properties of mammary epithelial stem cells. Nature 439, 993–997 (2006).
pubmed: 16395311
Shackleton, M. et al. Generation of a functional mammary gland from a single stem cell. Nature 439, 84–88 (2006).
pubmed: 16397499
Ito, M. et al. Stem cells in the hair follicle bulge contribute to wound repair but not to homeostasis of the epidermis. Nat. Med. 11, 1351–1354 (2005).
pubmed: 16288281
Van Keymeulen, A. et al. Distinct stem cells contribute to mammary gland development and maintenance. Nature 479, 189–193 (2011).
pubmed: 21983963
Cheng, D. T. et al. Memorial Sloan Kettering–Integrated Mutation Profiling of Actionable Cancer Targets (MSK-IMPACT): a hybridization capture-based next-generation sequencing clinical assay for solid tumor molecular oncology. J. Mol. Diagn. 17, 251–264 (2015).
pubmed: 25801821 pmcid: 5808190
Chakravarty, D. et al. OncoKB: a precision oncology knowledge base. JCO Precis. Oncol. https://doi.org/10.1200/PO.17.00011 (2017).
Maru, Y., Orihashi, K. & Hippo, Y. Lentivirus-based stable gene delivery into intestinal organoids. Methods Mol. Biol. 1422, 13–21 (2016).
pubmed: 27246018
Jackson, E. L. et al. Analysis of lung tumor initiation and progression using conditional expression of oncogenic K-ras. Genes Dev. 15, 3243–3248 (2001).
pubmed: 11751630 pmcid: 312845
Marino, S., Vooijs, M., van Der Gulden, H., Jonkers, J. & Berns, A. Induction of medulloblastomas in p53-null mutant mice by somatic inactivation of Rb in the external granular layer cells of the cerebellum. Genes Dev. 14, 994–1004 (2000).
pubmed: 10783170 pmcid: 316543
Kim, J. J., Shajib, M. S., Manocha, M. M. & Khan, W. I. Investigating intestinal inflammation in DSS-induced model of IBD. J. Vis. Exp. https://doi.org/10.3791/3678 (2012).
Kreyberg, L. Main histological types of primary epithelial lung tumours. Br. J. Cancer 15, 206–210 (1961).
pubmed: 13754309 pmcid: 2070911
Shultz, L. D. et al. NOD/LtSz-Rag1
pubmed: 14557749
Cespedes, M. V. et al. Orthotopic microinjection of human colon cancer cells in nude mice induces tumor foci in all clinically relevant metastatic sites. Am. J. Pathol. 170, 1077–1085 (2007).
pubmed: 17322390 pmcid: 1864873
Azizi, E. et al. Single-cell map of diverse immune phenotypes in the breast tumor microenvironment. Cell 174, 1293–1308 (2018).
pubmed: 29961579 pmcid: 6348010
van Dijk, D. et al. Recovering gene interactions from single-cell data using data diffusion. Cell 174, 716–729 (2018).
pubmed: 29961576 pmcid: 6771278
Fellmann, C. et al. An optimized microRNA backbone for effective single-copy RNAi. Cell Rep. 5, 1704–1713 (2013).
pubmed: 24332856
Basnet, H. et al. Tyrosine phosphorylation of histone H2A by CK2 regulates transcriptional elongation. Nature 516, 267–271 (2014).
pubmed: 25252977 pmcid: 4461219
Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J. 17, 10–12 (2011).
Andrews, S. FASTQC. A quality control tool for high throughput sequence data. Babrahan Bioinformatics http://www.bioinformatics.babraham.ac.uk/projects/fastqc/ (2010).
Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012).
pubmed: 22388286 pmcid: 22388286
Zhang, Y. et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9, R137 (2008).
pubmed: 18798982 pmcid: 2592715
Heinz, S. et al. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell 38, 576–589 (2010).
pubmed: 20513432 pmcid: 2898526
Quinlan, A. R. & Hall, I. M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841–842 (2010).
pubmed: 20110278 pmcid: 2832824

Auteurs

Karuna Ganesh (K)

Cancer Biology and Genetics Program, Sloan Kettering Institute, Memorial Sloan Kettering Cancer Center, New York, NY, USA.
Department of Medicine, Memorial Sloan Kettering Cancer Center, New York, NY, USA.
Molecular Pharmacology Program, Sloan Kettering Institute, Memorial Sloan Kettering Cancer Center, New York, NY, USA.

Harihar Basnet (H)

Cancer Biology and Genetics Program, Sloan Kettering Institute, Memorial Sloan Kettering Cancer Center, New York, NY, USA.

Yasemin Kaygusuz (Y)

Cancer Biology and Genetics Program, Sloan Kettering Institute, Memorial Sloan Kettering Cancer Center, New York, NY, USA.
Louis V. Gerstner, Jr. Graduate School of Biomedical Sciences, Memorial Sloan Kettering Cancer Center, New York, NY, USA.

Ashley M Laughney (AM)

Cancer Biology and Genetics Program, Sloan Kettering Institute, Memorial Sloan Kettering Cancer Center, New York, NY, USA.
Institute for Computational Biomedicine, Department of Physiology and Biophysics, Weill Cornell Medicine, New York, NY, USA.

Lan He (L)

Cancer Biology and Genetics Program, Sloan Kettering Institute, Memorial Sloan Kettering Cancer Center, New York, NY, USA.

Roshan Sharma (R)

Computational and Systems Biology Program, Sloan Kettering Institute, Memorial Sloan Kettering Cancer Center, New York, NY, USA.
Department of Applied Physics and Applied Math, Columbia University, New York, NY, USA.
New York Genome Center, New York, NY, USA.

Kevin P O'Rourke (KP)

Cancer Biology and Genetics Program, Sloan Kettering Institute, Memorial Sloan Kettering Cancer Center, New York, NY, USA.
Weill Cornell/Rockefeller/Sloan Kettering Tri-Institutional MD-PhD Program, New York, NY, USA.

Vincent P Reuter (VP)

Center for Epigenetics Research, Memorial Sloan Kettering Cancer Center, New York, NY, USA.

Yun-Han Huang (YH)

Cancer Biology and Genetics Program, Sloan Kettering Institute, Memorial Sloan Kettering Cancer Center, New York, NY, USA.
Louis V. Gerstner, Jr. Graduate School of Biomedical Sciences, Memorial Sloan Kettering Cancer Center, New York, NY, USA.
Weill Cornell/Rockefeller/Sloan Kettering Tri-Institutional MD-PhD Program, New York, NY, USA.

Mesruh Turkekul (M)

Molecular Cytology Core Facility, Memorial Sloan Kettering Cancer Center, New York, NY, USA.

Ekrem Emrah Er (EE)

Cancer Biology and Genetics Program, Sloan Kettering Institute, Memorial Sloan Kettering Cancer Center, New York, NY, USA.
Department of Physiology and Biophysics, University of Illinois at Chicago, Chicago, IL, USA.

Ignas Masilionis (I)

Computational and Systems Biology Program, Sloan Kettering Institute, Memorial Sloan Kettering Cancer Center, New York, NY, USA.

Katia Manova-Todorova (K)

Molecular Cytology Core Facility, Memorial Sloan Kettering Cancer Center, New York, NY, USA.

Martin R Weiser (MR)

Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, NY, USA.

Leonard B Saltz (LB)

Department of Medicine, Memorial Sloan Kettering Cancer Center, New York, NY, USA.

Julio Garcia-Aguilar (J)

Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, NY, USA.
ORCID: 0000-0003-2451-0948

Richard Koche (R)

Center for Epigenetics Research, Memorial Sloan Kettering Cancer Center, New York, NY, USA.
ORCID: 0000-0002-6820-5083

Scott W Lowe (SW)

Cancer Biology and Genetics Program, Sloan Kettering Institute, Memorial Sloan Kettering Cancer Center, New York, NY, USA.
ORCID: 0000-0002-5284-9650

Dana Pe'er (D)

Computational and Systems Biology Program, Sloan Kettering Institute, Memorial Sloan Kettering Cancer Center, New York, NY, USA.

Jinru Shia (J)

Department of Pathology, Memorial Sloan Kettering Cancer Center, New York, NY, USA.
ORCID: 0000-0002-4351-2511

Joan Massagué (J)

Cancer Biology and Genetics Program, Sloan Kettering Institute, Memorial Sloan Kettering Cancer Center, New York, NY, USA. j-massague@ski.mskcc.org.
ORCID: 0000-0001-9324-8408

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female

Evaluation of Low-Value Services Across Major Medicare Advantage Insurers and Traditional Medicare.

Ciara Duggan, Adam L Beckman, Ishani Ganguli et al.
1.00
Humans United States Aged Cross-Sectional Studies Medicare Part C

Effectiveness of Virtual Yoga for Chronic Low Back Pain: A Randomized Clinical Trial.

Hallie Tankha, Devyn Gaskins, Amanda Shallcross et al.
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH

questionsmedicales.fr › Eucaryotes › Animaux › L1CAM defines the regenerative origin of...
questionsmedicales.fr › Maladies de l'appareil digestif › Maladies gastro-intestinales › Maladies intestinales › Maladies du rectum › Tumeurs colorectales › L1CAM defines the regenerative origin of...
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Primates › Haplorhini › Catarrhini › Hominidae › Humains › L1CAM defines the regenerative origin of...
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Rodentia › Muridae › Murinae › Souris › L1CAM defines the regenerative origin of...
questionsmedicales.fr › États, signes et symptômes pathologiques › Processus pathologiques › Processus néoplasiques › Métastase tumorale › L1CAM defines the regenerative origin of...
questionsmedicales.fr › Facteurs biologiques › Antigènes › Antigènes de surface › Molécules d'adhérence cellulaire › Molécules d'adhérence cellulaire neuronale › Molécules d'adhérence cellulaire neurales › Molécule d'adhérence cellulaire neurale L-1 › L1CAM defines the regenerative origin of...