Extracellular vesicles secreted by triple-negative breast cancer stem cells trigger premetastatic niche remodeling and metastatic growth in the lungs.


Journal

International journal of cancer
ISSN: 1097-0215
Titre abrégé: Int J Cancer
Pays: United States
ID NLM: 0042124

Informations de publication

Date de publication:
15 05 2023
Historique:
revised: 11 11 2022
received: 28 07 2022
accepted: 13 12 2022
pubmed: 28 1 2023
medline: 15 3 2023
entrez: 27 1 2023
Statut: ppublish

Résumé

Tumor secreted extracellular vesicles (EVs) are potent intercellular signaling platforms. They are responsible for the accommodation of the premetastatic niche (PMN) to support cancer cell engraftment and metastatic growth. However, complex cancer cell composition within the tumor increases also the heterogeneity among cancer secreted EVs subsets, a functional diversity that has been poorly explored. This phenomenon is particularly relevant in highly plastic and heterogenous triple-negative breast cancer (TNBC), in which a significant representation of malignant cancer stem cells (CSCs) is displayed. Herein, we selectively isolated and characterized EVs from CSC or differentiated cancer cells (DCC; EVs

Identifiants

pubmed: 36705298
doi: 10.1002/ijc.34447
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

2153-2165

Informations de copyright

© 2023 The Authors. International Journal of Cancer published by John Wiley & Sons Ltd on behalf of UICC.

Références

Fragomeni SM, Sciallis A, Jeruss JS. Molecular subtypes and local-regional control of breast cancer. Surg Oncol Clin N Am. 2018;27:95-120.
Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68:394-424.
Wahl GM, Spike BT. Cell state plasticity, stem cells, EMT, and the generation of intra-tumoral heterogeneity. NPJ Breast Cancer. 2017;3:14.
Coates JT, Sun S, Leshchiner I, et al. Parallel genomic alterations of antigen and payload targets mediate polyclonal acquired clinical resistance to Sacituzumab Govitecan in triple-negative breast cancer. Cancer Discov. 2021;11:2436-2445.
Ma F, Li H, Wang H, et al. Enriched CD44(+)/CD24(−) population drives the aggressive phenotypes presented in triple-negative breast cancer (TNBC). Cancer Lett. 2014;353:153-159.
Ginestier C, Hur MH, Charafe-Jauffret E, et al. ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell. 2007;1:555-567.
Acharyya S, Oskarsson T, Vanharanta S, et al. A CXCL1 paracrine network links cancer chemoresistance and metastasis. Cell. 2012;150:165-178.
Albrengues J, Shields MA, Ng D, et al. Neutrophil extracellular traps produced during inflammation awaken dormant cancer cells in mice. Science. 2018;361:eaao4227. doi:10.1126/science.aao4227
Najafi M, Mortezaee K, Majidpoor J. Cancer stem cell (CSC) resistance drivers. Life Sci. 2019;234:116781.
Zomer A, Ellenbroek SIJ, Ritsma L, Beerling E, Vrisekoop N, Van Rheenen J. Intravital imaging of cancer stem cell plasticity in mammary tumors. Stem Cells. 2013;31:602-606. doi:10.1002/stem.1296
Fumagalli A, Oost KC, Kester L, et al. Plasticity of Lgr5-negative cancer cells drives metastasis in colorectal cancer. Cell Stem Cell. 2020;26:569-578.e7.
Gener P, Rafael D, Seras-Franzoso J, et al. Pivotal role of AKT2 during dynamic phenotypic change of breast cancer stem cells. Cancers. 2019;11:1058.
Su S, Chen J, Yao H, et al. CD10+GPR77+ cancer-associated fibroblasts promote cancer formation and chemoresistance by sustaining cancer stemness. Cell. 2018;172:841-856.e16.
Tsuyada A, Chow A, Wu J, et al. CCL2 mediates cross-talk between cancer cells and stromal fibroblasts that regulates breast cancer stem cells. Cancer Res. 2012;72:2768-2779.
Bartosh TJ, Ullah M, Zeitouni S, Beaver J, Prockop DJ. Cancer cells enter dormancy after cannibalizing mesenchymal stem/stromal cells (MSCs). Proc Natl Acad Sci USA. 2016;113:E6447-E6456.
Ji Z, He L, Regev A, Struhl K. Inflammatory regulatory network mediated by the joint action of NF-kB, STAT3, and AP-1 factors is involved in many human cancers. Proc Natl Acad Sci USA. 2019;116:9453-9462.
Bliss SA, Sinha G, Sandiford OA, et al. Mesenchymal stem cell-derived exosomes stimulate cycling quiescence and early breast cancer dormancy in bone marrow. Cancer Res. 2016;76:5832-5844.
Binenbaum Y, Fridman E, Yaari Z, et al. Transfer of miRNA in macrophage-derived exosomes induces drug resistance in pancreatic adenocarcinoma. Cancer Res. 2018;78:5287-5299.
Becker A, Thakur BK, Weiss JM, Kim HS, Peinado H, Lyden D. Extracellular vesicles in cancer: cell-to-cell mediators of metastasis. Cancer Cell. 2016;30:836-848.
Russell AE, Sneider A, Witwer KW, et al. Biological membranes in EV biogenesis, stability, uptake, and cargo transfer: an ISEV position paper arising from the ISEV membranes and EVs workshop. J Extracell Vesicles. 2019;8:1684862. doi:10.1080/20013078.2019.1684862
Chowdhury R, Webber JP, Gurney M, Mason MD, Tabi Z, Clayton A. Cancer exosomes trigger mesenchymal stem cell differentiation into pro-angiogenic and pro-invasive myofibroblasts. Oncotarget. 2015;6:715-731.
Fang T, Lv H, Lv G, et al. Tumor-derived exosomal miR-1247-3p induces cancer-associated fibroblast activation to foster lung metastasis of liver cancer. Nat Commun. 2018;9:191.
Tang MKS, Yue PYK, Ip PP, et al. Soluble E-cadherin promotes tumor angiogenesis and localizes to exosome surface. Nat Commun. 2018;9:2270.
Chen G, Huang AC, Zhang W, et al. Exosomal PD-L1 contributes to immunosuppression and is associated with anti-PD-1 response. Nature. 2018;560:382-386.
Li C, Qiu S, Jin K, et al. Tumor-derived microparticles promote the progression of triple-negative breast cancer via PD-L1-associated immune suppression. Cancer Lett. 2021;523:43-56.
Wendler F, Stamp GW, Giamas G. Tumor-stromal cell communication: small vesicles signal big changes. Trends Cancer. 2016;2:326-329.
Ji Q, Zhou L, Sui H, et al. Primary tumors release ITGBL1-rich extracellular vesicles to promote distal metastatic tumor growth through fibroblast-niche formation. Nat Commun. 2020;11:1211.
Wu SZ, Roden DL, Wang C, et al. Stromal cell diversity associated with immune evasion in human triple-negative breast cancer. EMBO J. 2020;39:e104063. doi:10.15252/embj.2019104063
Gaggioli C, Hooper S, Hidalgo-Carcedo C, et al. Fibroblast-led collective invasion of carcinoma cells with differing roles for RhoGTPases in leading and following cells. Nat Cell Biol. 2007;9:1392-1400.
Costa A, Kieffer Y, Scholer-Dahirel A, et al. Fibroblast heterogeneity and immunosuppressive environment in human breast cancer. Cancer Cell. 2018;33:463-479.e10.
Pelon F, Bourachot B, Kieffer Y, et al. Cancer-associated fibroblast heterogeneity in axillary lymph nodes drives metastases in breast cancer through complementary mechanisms. Nat Commun. 2020;11:404.
Wen SW, Lima LG, Lobb RJ, et al. Breast cancer-derived exosomes reflect the cell-of-origin phenotype. Proteomics. 2019;19:e1800180.
Gener P, Gouveia LP, Sabat GR, et al. Fluorescent CSC models evidence that targeted nanomedicines improve treatment sensitivity of breast and colon cancer stem cells. Nanomedicine. 2015;11:1883-1892.
Seras-Franzoso J, Díaz-Riascos ZV, Corchero JL, et al. Extracellular vesicles from recombinant cell factories improve the activity and efficacy of enzymes defective in lysosomal storage disorders. J Extracell Vesicles. 2021;10:e12058. doi:10.1002/jev2.12058
Conti S, Kato T, Park D, Sahai E, Trepat X, Labernadie A. CAFs and cancer cells co-migration in 3D spheroid invasion assay. Methods Mol Biol. 2021;2179:243-256.
Labernadie A, Kato T, Brugués A, et al. A mechanically active heterotypic E-cadherin/N-cadherin adhesion enables fibroblasts to drive cancer cell invasion. Nat Cell Biol. 2017;19:224-237.
Morancho A, Hernández-Guillamon M, Boada C, et al. Cerebral ischaemia and matrix metalloproteinase-9 modulate the angiogenic function of early and late outgrowth endothelial progenitor cells. J Cell Mol Med. 2013;17:1543-1553.
Cámara-Sánchez P, Díaz-Riascos ZV, García-Aranda N, et al. Selectively targeting breast cancer stem cells by 8-Quinolinol and Niclosamide. Int J Mol Sci. 2022;23:11760.
Lázaro-Ibánez E, Al-Jamal KT, Dekker N, et al. Selection of fluorescent, bioluminescent, and radioactive tracers to accurately reflect extracellular vesicle biodistribution in vivo. ACS Nano. 2021;15:3212-3227.
Hoshino A, Costa-Silva B, Shen T-L, et al. Tumour exosome integrins determine organotropic metastasis. Nature. 2015;527:329-335.
Kolář M, Szabo P, Dvořánková B, et al. Upregulation of IL-6, IL-8 and CXCL-1 production in dermal fibroblasts by normal/malignant epithelial cells in vitro: Immunohistochemical and transcriptomic analyses. Biol Cell. 2012;104:738-751. doi:10.1111/boc.201200018
van der Zee M, Sacchetti A, Cansoy M, et al. IL6/JAK1/STAT3 signaling blockade in endometrial cancer affects the ALDHhi/CD126+ stem-like component and reduces tumor burden. Cancer Res. 2015;75:3608-3622.
Singh JK, Farnie G, Bundred NJ, et al. Targeting CXCR1/2 significantly reduces breast cancer stem cell activity and increases the efficacy of inhibiting HER2 via HER2-dependent and -independent mechanisms. Clin Cancer Res. 2013;19:643-656.
Korkaya H, Liu S, Wicha MS. Regulation of cancer stem cells by cytokine networks: attacking Cancer's inflammatory roots: figure 1. Clin Cancer Res. 2011;17:6125-6129. doi:10.1158/1078-0432.CCR-10-2743
Iliopoulos D, Hirsch HA, Wang G, Struhl K. Inducible formation of breast cancer stem cells and their dynamic equilibrium with non-stem cancer cells via IL6 secretion. Proc Natl Acad Sci USA. 2011;108:1397-1402. doi:10.1073/pnas.1018898108
Lu H, Clauser KR, Tam WL, et al. A breast cancer stem cell niche supported by juxtacrine signalling from monocytes and macrophages. Nat Cell Biol. 2014;16:1105-1117.
Fan Q-M, Jing Y-Y, Yu G-F, et al. Tumor-associated macrophages promote cancer stem cell-like properties via transforming growth factor-beta1-induced epithelial-mesenchymal transition in hepatocellular carcinoma. Cancer Lett. 2014;352:160-168.
Glentis A, Oertle P, Mariani P, et al. Cancer-associated fibroblasts induce metalloprotease-independent cancer cell invasion of the basement membrane. Nat Commun. 2017;8:924.
Wang L, Yang G, Zhao D, et al. CD103-positive CSC exosome promotes EMT of clear cell renal cell carcinoma: role of remote MiR-19b-3p. Mol Cancer. 2019;18:86.
Öhlund D, Handly-Santana A, Biffi G, et al. Distinct populations of inflammatory fibroblasts and myofibroblasts in pancreatic cancer. J Exp Med. 2017;214:579-596.

Auteurs

Patricia González-Callejo (P)

Drug Delivery & Targeting, Vall d'Hebron Institut de Recerca (VHIR), Universitat Autònoma de Barcelona (UAB), Barcelona, Spain.
Networking Research Center on Bioengineering, Biomaterials and Nanomedicine (CIBER-BBN), Instituto de Salud Carlos III, Madrid, Spain.

Petra Gener (P)

Drug Delivery & Targeting, Vall d'Hebron Institut de Recerca (VHIR), Universitat Autònoma de Barcelona (UAB), Barcelona, Spain.
Networking Research Center on Bioengineering, Biomaterials and Nanomedicine (CIBER-BBN), Instituto de Salud Carlos III, Madrid, Spain.

Zamira V Díaz-Riascos (ZV)

Drug Delivery & Targeting, Vall d'Hebron Institut de Recerca (VHIR), Universitat Autònoma de Barcelona (UAB), Barcelona, Spain.
Networking Research Center on Bioengineering, Biomaterials and Nanomedicine (CIBER-BBN), Instituto de Salud Carlos III, Madrid, Spain.
Functional Validation & Preclinical Research (FVPR), Vall d‧Hebron Institut de Recerca (VHIR), Universitat Autònoma de Barcelona (UAB), Passeig de la Vall d'Hebron, Barcelona, Spain.

Sefora Conti (S)

Integrative Cell and Tissue Dynamics Group, Institute for Bioengineering of Catalonia (IBEC), Barcelona, Spain.

Patricia Cámara-Sánchez (P)

Drug Delivery & Targeting, Vall d'Hebron Institut de Recerca (VHIR), Universitat Autònoma de Barcelona (UAB), Barcelona, Spain.
Networking Research Center on Bioengineering, Biomaterials and Nanomedicine (CIBER-BBN), Instituto de Salud Carlos III, Madrid, Spain.
Functional Validation & Preclinical Research (FVPR), Vall d‧Hebron Institut de Recerca (VHIR), Universitat Autònoma de Barcelona (UAB), Passeig de la Vall d'Hebron, Barcelona, Spain.

Roger Riera (R)

Nanoscopy for Nanomedicine Group, Institute for Bioengineering of Catalonia (IBEC), Barcelona, Spain.
Department of Biomedical Engineering, Institute for Complex Molecular Systems (ICMS), Eindhoven University of Technology, Eindhoven, Netherlands.

Sandra Mancilla (S)

Drug Delivery & Targeting, Vall d'Hebron Institut de Recerca (VHIR), Universitat Autònoma de Barcelona (UAB), Barcelona, Spain.
Networking Research Center on Bioengineering, Biomaterials and Nanomedicine (CIBER-BBN), Instituto de Salud Carlos III, Madrid, Spain.
Functional Validation & Preclinical Research (FVPR), Vall d‧Hebron Institut de Recerca (VHIR), Universitat Autònoma de Barcelona (UAB), Passeig de la Vall d'Hebron, Barcelona, Spain.

Miguel García-Gabilondo (M)

Neurovascular Research Laboratory, Vall d‧Hebron Institut de Recerca (VHIR), Universitat Autònoma de Barcelona (UAB), Passeig Vall d'Hebron, Barcelona, Spain.

Vicente Peg (V)

Department of Pathology, Vall d'Hebron University Hospital, Universitat Autònoma de Barcelona (UAB), Barcelona, Spain.
Spanish Biomedical Research Network Centre in Oncology (CIBERONC), Instituto de Salud Carlos III, Madrid, Spain.

Diego Arango (D)

Department of Molecular Oncology, Biomedical Research Institute of Lleida, Lleida, Spain.
Biomedical Research in Digestive Tract Tumors, Vall d'Hebron Research Institute (VHIR), Universitat Autònoma de Barcelona (UAB), Passeig de la Vall d'Hebron, Barcelona, Spain.

Anna Rosell (A)

Neurovascular Research Laboratory, Vall d‧Hebron Institut de Recerca (VHIR), Universitat Autònoma de Barcelona (UAB), Passeig Vall d'Hebron, Barcelona, Spain.

Anna Labernadie (A)

Integrative Cell and Tissue Dynamics Group, Institute for Bioengineering of Catalonia (IBEC), Barcelona, Spain.

Xavier Trepat (X)

Networking Research Center on Bioengineering, Biomaterials and Nanomedicine (CIBER-BBN), Instituto de Salud Carlos III, Madrid, Spain.
Integrative Cell and Tissue Dynamics Group, Institute for Bioengineering of Catalonia (IBEC), Barcelona, Spain.
Catalan Institution for Research and Advanced Studies (ICREA), Passeig Lluís Companys, Barcelona, Spain.

Lorenzo Albertazzi (L)

Nanoscopy for Nanomedicine Group, Institute for Bioengineering of Catalonia (IBEC), Barcelona, Spain.
Department of Biomedical Engineering, Institute for Complex Molecular Systems (ICMS), Eindhoven University of Technology, Eindhoven, Netherlands.

Simó Schwartz (S)

Drug Delivery & Targeting, Vall d'Hebron Institut de Recerca (VHIR), Universitat Autònoma de Barcelona (UAB), Barcelona, Spain.
Networking Research Center on Bioengineering, Biomaterials and Nanomedicine (CIBER-BBN), Instituto de Salud Carlos III, Madrid, Spain.

Joaquin Seras-Franzoso (J)

Drug Delivery & Targeting, Vall d'Hebron Institut de Recerca (VHIR), Universitat Autònoma de Barcelona (UAB), Barcelona, Spain.
Networking Research Center on Bioengineering, Biomaterials and Nanomedicine (CIBER-BBN), Instituto de Salud Carlos III, Madrid, Spain.
Department of Genetics and Microbiology, Universitat Autònoma de Barcelona (UAB), Bellaterra, Spain.

Ibane Abasolo (I)

Drug Delivery & Targeting, Vall d'Hebron Institut de Recerca (VHIR), Universitat Autònoma de Barcelona (UAB), Barcelona, Spain.
Networking Research Center on Bioengineering, Biomaterials and Nanomedicine (CIBER-BBN), Instituto de Salud Carlos III, Madrid, Spain.
Functional Validation & Preclinical Research (FVPR), Vall d‧Hebron Institut de Recerca (VHIR), Universitat Autònoma de Barcelona (UAB), Passeig de la Vall d'Hebron, Barcelona, Spain.

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
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH