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Article: Epithelial to Mesenchymal Transition in a Clinical Perspective.

Pasquier, Jennifer / Abu-Kaoud, Nadine / Al Thani, Haya / Rafii, Arash

2015 Volume 2015, Page(s) 792182

Abstract: Tumor growth and metastatic dissemination rely on cellular plasticity. Among the different phenotypes acquired by cancer cells, epithelial to mesenchymal transition (EMT) has been extensively illustrated. Indeed, this transition allows an epithelial ... ...

Abstract	Tumor growth and metastatic dissemination rely on cellular plasticity. Among the different phenotypes acquired by cancer cells, epithelial to mesenchymal transition (EMT) has been extensively illustrated. Indeed, this transition allows an epithelial polarized cell to acquire a more mesenchymal phenotype with increased mobility and invasiveness. The role of EMT is quite clear during developmental stage. In the neoplastic context in many tumors EMT has been associated with a more aggressive tumor phenotype including local invasion and distant metastasis. EMT allows the cell to invade surrounding tissues and survive in the general circulation and through a stem cell phenotype grown in the host organ. The molecular pathways underlying EMT have also been clearly defined and their description is beyond the scope of this review. Here we will summarize and analyze the attempts made to block EMT in the therapeutic context. Indeed, till today, most of the studies are made in animal models. Few clinical trials are ongoing with no obvious benefits of EMT inhibitors yet. We point out the limitations of EMT targeting such tumor heterogeneity or the dynamics of EMT during disease progression.
Language	English
Publishing date	2015-09-06
Publishing country	Egypt
Document type	Journal Article ; Review
ZDB-ID	2461349-6
ISSN	1687-8469 ; 1687-8450
ISSN (online)	1687-8469
ISSN	1687-8450
DOI	10.1155/2015/792182
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Article ; Online: VE-cadherin cleavage by ovarian cancer microparticles induces β-catenin phosphorylation in endothelial cells.

Al Thawadi, Hamda / Abu-Kaoud, Nadine / Al Farsi, Haleema / Hoarau-Véchot, Jessica / Rafii, Shahin / Rafii, Arash / Pasquier, Jennifer

Oncotarget

2016 Volume 7, Issue 5, Page(s) 5289–5305

Abstract: Microparticles (MPs) are increasingly recognized as important mediators of cell-cell communication in tumour growth and metastasis by facilitating angiogenesis-related processes. While the effects of the MPs on recipient cells are usually well described ... ...

Abstract	Microparticles (MPs) are increasingly recognized as important mediators of cell-cell communication in tumour growth and metastasis by facilitating angiogenesis-related processes. While the effects of the MPs on recipient cells are usually well described in the literature, the leading process remains unclear. Here we isolated MPs from ovarian cancer cells and investigated their effect on endothelial cells. First, we demonstrated that ovarian cancer MPs trigger β-catenin activation in endothelial cells, inducing the upregulation of Wnt/β-catenin target genes and an increase of angiogenic properties. We showed that this MPs mediated activation of β-catenin in ECs was Wnt/Frizzled independent; but dependent on VE-cadherin localization disruption, αVβ3 integrin activation and MMP activity. Finally, we revealed that Rac1 and AKT were responsible for β-catenin phosphorylation and translocation to the nucleus. Overall, our results indicate that MPs released from cancer cells could play a major role in neo-angiogenesis through activation of beta catenin pathway in endothelial cells.
MeSH term(s)	Cadherins/metabolism ; Endothelial Cells/metabolism ; Endothelial Cells/physiology ; Female ; Humans ; Ovarian Neoplasms/metabolism ; Ovarian Neoplasms/pathology ; Phosphorylation ; Signal Transduction ; Tumor Microenvironment ; beta Catenin/metabolism
Chemical Substances	Cadherins ; beta Catenin
Language	English
Publishing date	2016-02-02
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2560162-3
ISSN	1949-2553 ; 1949-2553
ISSN (online)	1949-2553
ISSN	1949-2553
DOI	10.18632/oncotarget.6677
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Article ; Online: Evidence for P-Glycoprotein Involvement in Cell Volume Regulation Using Coulter Sizing in Flow Cytometry.

Pasquier, Jennifer / Rioult, Damien / Abu-Kaoud, Nadine / Hoarau-Véchot, Jessica / Marin, Matthieu / Le Foll, Frank

International journal of molecular sciences

2015 Volume 16, Issue 7, Page(s) 14318–14337

Abstract: The regulation of cell volume is an essential function that is coupled to a variety of physiological processes such as receptor recycling, excitability and contraction, cell proliferation, migration, and programmed cell death. Under stress, cells undergo ...

Abstract	The regulation of cell volume is an essential function that is coupled to a variety of physiological processes such as receptor recycling, excitability and contraction, cell proliferation, migration, and programmed cell death. Under stress, cells undergo emergency swelling and respond to such a phenomenon with a regulatory volume decrease (RVD) where they release cellular ions, and other osmolytes as well as a concomitant loss of water. The link between P-glycoprotein, a transmembrane transporter, and cell volume regulation is controversial, and changes in cells volume are measured using microscopy or electrophysiology. For instance, by using the patch-clamp method, our team demonstrated that chloride currents activated in the RVD were more intense and rapid in a breast cancer cell line overexpressing the P-glycoprotein (P-gp). The Cell Lab Quanta SC is a flow cytometry system that simultaneously measures electronic volume, side scatter and three fluorescent colors; altogether this provides unsurpassed population resolution and accurate cell counting. Therefore, here we propose a novel method to follow cellular volume. By using the Coulter-type channel of the cytometer Cell Lab Quanta SC MPL (multi-platform loading), we demonstrated a role for the P-gp during different osmotic treatments, but also a differential activity of the P-gp through the cell cycle. Altogether, our data strongly suggests a role of P-gp in cell volume regulation.
MeSH term(s)	ATP-Binding Cassette, Sub-Family B, Member 1/genetics ; ATP-Binding Cassette, Sub-Family B, Member 1/metabolism ; Cell Size ; Chloride Channels/metabolism ; Flow Cytometry/methods ; Humans ; MCF-7 Cells
Chemical Substances	ATP-Binding Cassette, Sub-Family B, Member 1 ; Chloride Channels
Language	English
Publishing date	2015-06-24
Publishing country	Switzerland
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2019364-6
ISSN	1422-0067 ; 1422-0067 ; 1661-6596
ISSN (online)	1422-0067
ISSN	1422-0067 ; 1661-6596
DOI	10.3390/ijms160714318
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Article ; Online: Breast cancer cells promote a notch-dependent mesenchymal phenotype in endothelial cells participating to a pro-tumoral niche.

Ghiabi, Pegah / Jiang, Jie / Pasquier, Jennifer / Maleki, Mahtab / Abu-Kaoud, Nadine / Halabi, Najeeb / Guerrouahen, Bella S / Rafii, Shahin / Rafii, Arash

Journal of translational medicine

2015 Volume 13, Page(s) 27

Abstract: Background: Endothelial cells (ECs) are responsible for creating a tumor vascular niche as well as producing angiocrine factors. ECs demonstrate functional and phenotypic heterogeneity when located under different microenvironments. Here, we describe a ... ...

Abstract	Background: Endothelial cells (ECs) are responsible for creating a tumor vascular niche as well as producing angiocrine factors. ECs demonstrate functional and phenotypic heterogeneity when located under different microenvironments. Here, we describe a tumor-stimulated mesenchymal phenotype in ECs and investigate its impact on tumor growth, stemness, and invasiveness. Methods: Xenograft tumor assay in NOD/SCID mice and confocal imaging were conducted to show the acquisition of mesenchymal phenotype in tumor-associated ECs in vivo. Immunocytochemistry, qPCR and flow cytometry techniques showed the appearance of mesenchymal traits in ECs after contact with breast tumor cell lines MDA-MB231 or MCF-7. Cell proliferation, cell migration, and sphere formation assays were applied to display the functional advantages of mesenchymal ECs in tumor growth, invasiveness, and enrichment of tumor initiating cells. qPCR and western blotting were used to investigate the mechanisms underlying EC mesenchymal transition. Results: Our results showed that co-injection of ECs and tumor cells in NOD/SCID mice significantly enhanced tumor growth in vivo with tumor-associated ECs expressing mesenchymal markers while maintaining their intrinsic endothelial trait. We also showed that a mesenchymal phenotype is possibly detectable in human neoplastic breast biopsies as well as ECs pre-exposed to tumor cells (ECs(Mes)) in vitro. The ECs(Mes) acquired prolonged survival, increased migratory behavior and enhanced angiogenic properties. In return, ECs(Mes) were capable of enhancing tumor survival and invasiveness. The mesenchymal phenotypes in ECs(Mes) were the result of a contact-dependent transient phenomenon and reversed upon removal of the neoplastic contexture. We showed a synergistic role for TGFβ and notch pathways in this phenotypic change, as simultaneous inhibition of notch and TGFβ down-regulated Smad1/5 phosphorylation and Jag1(KD) tumor cells were unable to initiate the process. Conclusions: Overall, our data proposed a crosstalk mechanism between tumor and microenvironment where tumor-stimulated mesenchymal modulation of ECs enhanced the constitution of a transient mesenchymal/endothelial niche leading to significant increase in tumor proliferation, stemness, and invasiveness. The possible involvement of notch and TGFβ pathways in the initiation of mesenchymal phenotype may propose new stromal targets.
MeSH term(s)	Animals ; Breast Neoplasms/genetics ; Breast Neoplasms/metabolism ; Breast Neoplasms/pathology ; Cell Line, Tumor ; Cell Proliferation ; Female ; Gene Expression Regulation, Neoplastic ; Human Umbilical Vein Endothelial Cells/metabolism ; Human Umbilical Vein Endothelial Cells/pathology ; Humans ; Mesoderm/metabolism ; Mesoderm/pathology ; Mice ; Mice, Inbred NOD ; Mice, SCID ; Phenotype ; Receptors, Notch/metabolism ; Signal Transduction/genetics ; Transcriptome/genetics ; Transforming Growth Factor beta/metabolism ; Tumor Microenvironment ; Xenograft Model Antitumor Assays
Chemical Substances	Receptors, Notch ; Transforming Growth Factor beta
Language	English
Publishing date	2015-01-27
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ISSN	1479-5876
ISSN (online)	1479-5876
DOI	10.1186/s12967-015-0386-3
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Article ; Online: Endothelial cells provide a notch-dependent pro-tumoral niche for enhancing breast cancer survival, stemness and pro-metastatic properties.

Ghiabi, Pegah / Jiang, Jie / Pasquier, Jennifer / Maleki, Mahtab / Abu-Kaoud, Nadine / Rafii, Shahin / Rafii, Arash

PloS one

2014 Volume 9, Issue 11, Page(s) e112424

Abstract: Treating metastasis has been challenging due to tumors complexity and heterogeneity. This complexity is partly related to the crosstalk between tumor and its microenvironment. Endothelial cells -the building blocks of tumor vasculature- have been shown ... ...

Abstract	Treating metastasis has been challenging due to tumors complexity and heterogeneity. This complexity is partly related to the crosstalk between tumor and its microenvironment. Endothelial cells -the building blocks of tumor vasculature- have been shown to have additional roles in cancer progression than angiogenesis and supplying oxygen and nutrients. Here, we show an alternative role for endothelial cells in supporting breast cancer growth and spreading independent of their vascular functions. Using endothelial cells and breast cancer cell lines MDA-MB231 and MCF-7, we developed co-culture systems to study the influence of tumor endothelium on breast tumor development by both in vitro and in vivo approaches. Our results demonstrated that endothelial cells conferred survival advantage to tumor cells under complete starvation and enriched the CD44HighCD24Low/- stem cell population in tumor cells. Moreover, endothelial cells enhanced the pro-metastatic potential of breast cancer cells. The in vitro and in vivo results concordantly confirmed a role for endothelial Jagged1 to promote breast tumor through notch activation. Here, we propose a role for endothelial cells in enhancing breast cancer progression, stemness, and pro-metastatic traits through a perfusion-independent manner. Our findings may be beneficial in developing novel therapeutic approaches.
MeSH term(s)	Animals ; Basic Helix-Loop-Helix Transcription Factors/genetics ; Basic Helix-Loop-Helix Transcription Factors/metabolism ; Breast Neoplasms/metabolism ; Breast Neoplasms/pathology ; CD24 Antigen/metabolism ; Calcium-Binding Proteins/genetics ; Calcium-Binding Proteins/metabolism ; Cell Line, Tumor ; Cell Survival ; Cells, Cultured ; Cellular Microenvironment ; Coculture Techniques ; Endothelial Cells/cytology ; Endothelial Cells/metabolism ; Homeodomain Proteins/genetics ; Homeodomain Proteins/metabolism ; Humans ; Hyaluronan Receptors/metabolism ; Intercellular Signaling Peptides and Proteins/genetics ; Intercellular Signaling Peptides and Proteins/metabolism ; Jagged-1 Protein ; MCF-7 Cells ; Membrane Proteins/genetics ; Membrane Proteins/metabolism ; Mice, Inbred NOD ; Mice, Knockout ; Mice, SCID ; Microscopy, Confocal ; Neoplasm Metastasis ; Neoplastic Stem Cells/metabolism ; Neoplastic Stem Cells/pathology ; Receptors, Notch/metabolism ; Reverse Transcriptase Polymerase Chain Reaction ; Serrate-Jagged Proteins ; Transcription Factor HES-1 ; Transplantation, Heterologous
Chemical Substances	Basic Helix-Loop-Helix Transcription Factors ; CD24 Antigen ; Calcium-Binding Proteins ; Homeodomain Proteins ; Hyaluronan Receptors ; Intercellular Signaling Peptides and Proteins ; JAG1 protein, human ; Jag1 protein, mouse ; Jagged-1 Protein ; Membrane Proteins ; Receptors, Notch ; Serrate-Jagged Proteins ; Transcription Factor HES-1 ; HES1 protein, human (149348-15-2)
Language	English
Publishing date	2014
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ISSN	1932-6203
ISSN (online)	1932-6203
DOI	10.1371/journal.pone.0112424
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Article ; Online: P-glycoprotein-activity measurements in multidrug resistant cell lines: single-cell versus single-well population fluorescence methods.

Pasquier, Jennifer / Rioult, Damien / Abu-Kaoud, Nadine / Marie, Sabine / Rafii, Arash / Guerrouahen, Bella S / Le Foll, Frank

BioMed research international

2013 Volume 2013, Page(s) 676845

Abstract: Background: P-gp expression has been linked to the efflux of chemotherapeutic drugs in human cancers leading to multidrug resistance. Fluorescence techniques have been widely applied to measure the P-gp activity. In this paper, there is a comparison ... ...

Abstract	Background: P-gp expression has been linked to the efflux of chemotherapeutic drugs in human cancers leading to multidrug resistance. Fluorescence techniques have been widely applied to measure the P-gp activity. In this paper, there is a comparison between the advantages of two fluorescence approaches of commonly available and affordable instruments: the microplate reader (MPR) and the flow cytometer to detect the P-gp efflux activity using calcein-AM. Results: The selectivity, sensibility, and reproducibility of the two methods have been defined. Our results showed that the MPR is more powerful for the detection of small inhibition, whereas the flow cytometry method is more reliable at higher concentrations of the inhibitors. We showed that to determine precisely the inhibition efficacy the flow cytometry is better; hence, to get the correct E max and EC50 values, we cannot only rely on the MPR. Conclusion: Both techniques can potentially be used extensively in the pharmaceutical industry for high-throughput drug screening and in biology laboratories for academic research, monitoring the P-gp efflux in specific assays.
MeSH term(s)	ATP Binding Cassette Transporter, Subfamily B/metabolism ; Cell Line, Tumor ; Drug Resistance, Multiple/physiology ; Drug Resistance, Neoplasm/physiology ; Fluoresceins/metabolism ; Fluorescence ; Humans ; MCF-7 Cells ; Reproducibility of Results
Chemical Substances	ATP Binding Cassette Transporter, Subfamily B ; Fluoresceins ; calcein AM (148504-34-1)
Language	English
Publishing date	2013-11-17
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2698540-8
ISSN	2314-6141 ; 2314-6133
ISSN (online)	2314-6141
ISSN	2314-6133
DOI	10.1155/2013/676845
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Article ; Online: SDF-1alpha concentration dependent modulation of RhoA and Rac1 modifies breast cancer and stromal cells interaction.

Pasquier, Jennifer / Abu-Kaoud, Nadine / Abdesselem, Houari / Madani, Aisha / Hoarau-Véchot, Jessica / Thawadi, Hamda Al / Vidal, Fabien / Couderc, Bettina / Favre, Gilles / Rafii, Arash

BMC cancer

2015 Volume 15, Page(s) 569

Abstract: Background: The interaction of SDF-1alpha with its receptor CXCR4 plays a role in the occurrence of distant metastasis in many solid tumors. This interaction increases migration from primary sites as well as homing at distant sites.: Methods: Here we ...

Abstract	Background: The interaction of SDF-1alpha with its receptor CXCR4 plays a role in the occurrence of distant metastasis in many solid tumors. This interaction increases migration from primary sites as well as homing at distant sites. Methods: Here we investigated how SDF-1α could modulate both migration and adhesion of cancer cells through the modulation of RhoGTPases. Results: We show that different concentrations of SDF-1α modulate the balance of adhesion and migration in cancer cells. Increased migration was obtained at 50 and 100 ng/ml of SDF-1α; however migration was reduced at 200 ng/ml. The adhesion between breast cancer cells and BMHC was significantly increased by SDF-1α treatment at 200 ng/ml and reduced using a blocking monoclonal antibody against CXCR4. We showed that at low SDF-1α concentration, RhoA was activated and overexpressed, while at high concentration Rac1 was promoting SDF-1α mediating-cell adhesion. Conclusion: We conclude that SDF-1α concentration modulates migration and adhesion of breast cancer cells, by controlling expression and activation of RhoGTPases.
MeSH term(s)	Breast Neoplasms/metabolism ; Cell Adhesion ; Cell Line, Tumor ; Cell Movement ; Chemokine CXCL12/metabolism ; Chemokine CXCL12/pharmacology ; Coculture Techniques ; Female ; Humans ; MCF-7 Cells ; Stromal Cells/cytology ; Stromal Cells/physiology ; rac1 GTP-Binding Protein/metabolism ; rhoA GTP-Binding Protein/metabolism
Chemical Substances	CXCL12 protein, human ; Chemokine CXCL12 ; RAC1 protein, human ; RHOA protein, human (124671-05-2) ; rac1 GTP-Binding Protein (EC 3.6.5.2) ; rhoA GTP-Binding Protein (EC 3.6.5.2)
Language	English
Publishing date	2015-08-01
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ISSN	1471-2407
ISSN (online)	1471-2407
DOI	10.1186/s12885-015-1556-7
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Article: Microparticles mediated cross-talk between tumoral and endothelial cells promote the constitution of a pro-metastatic vascular niche through Arf6 up regulation.

Pasquier, Jennifer / Thawadi, Hamda Al / Ghiabi, Pegah / Abu-Kaoud, Nadine / Maleki, Mahtab / Guerrouahen, Bella S / Vidal, Fabien / Courderc, Bettina / Ferron, Gwenael / Martinez, Alejandra / Al Sulaiti, Haya / Gupta, Renuka / Rafii, Shahin / Rafii, Arash

Cancer microenvironment : official journal of the International Cancer Microenvironment Society

2014 Volume 7, Issue 1-2, Page(s) 41–59

Abstract: The tumor stroma plays an essential role in tumor growth, resistance to therapy and occurrence of metastatic phenotype. Tumor vessels have been considered as passive conducts for nutrients but several studies have demonstrated secretion of pro-tumoral ... ...

Abstract	The tumor stroma plays an essential role in tumor growth, resistance to therapy and occurrence of metastatic phenotype. Tumor vessels have been considered as passive conducts for nutrients but several studies have demonstrated secretion of pro-tumoral factors by endothelial cells. The failure of anti-angiogenic therapies to meet expectations raised by pre-clinical studies prompt us to better study the cross-talk between endothelial and cancer cells. Here, we hypothesized that tumor cells and the endothelium secrete bio-active microparticles (MPs) participating to a functional cross-talk. We characterized the cancer cells MPs, using breast and ovarian cancer cell lines (MCF7, MDA-MB231, SKOV3, OVCAR3 and a primary cell lines, APOCC). Our data show that MPs from mesenchymal-like cell lines (MDA-MB231, SKOV3 and APOCC) were able to promote an activation of endothelial cells through Akt phosphorylation, compared to MPs from epithelial-like cell lines (OVCAR3 and MCF7). The MPs from mesenchymal-like cells contained increased angiogenic molecules including PDGF, IL8 and angiogenin. The endothelial activation was associated to increased Arf6 expression and MPs secretion. Endothelial activation functionalized an MP dependent pro-tumoral vascular niche promoting cancer cells proliferation, invasiveness, stem cell phenotype and chemoresistance. MPs from cancer and endothelial cells displayed phenotypic heterogeneity, and participated to a functional cross-talk where endothelial activation by cancer MPs resulted in increased secretion of EC-MPs sustaining tumor cells. Such cross-talk may play a role in perfusion independent role of the endothelium.
Language	English
Publishing date	2014-01-15
Publishing country	Netherlands
Document type	Journal Article
ZDB-ID	2422345-1
ISSN	1875-2284 ; 1875-2292
ISSN (online)	1875-2284
ISSN	1875-2292
DOI	10.1007/s12307-013-0142-2
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Article ; Online: Preferential transfer of mitochondria from endothelial to cancer cells through tunneling nanotubes modulates chemoresistance.

Pasquier, Jennifer / Guerrouahen, Bella S / Al Thawadi, Hamda / Ghiabi, Pegah / Maleki, Mahtab / Abu-Kaoud, Nadine / Jacob, Arthur / Mirshahi, Massoud / Galas, Ludovic / Rafii, Shahin / Le Foll, Frank / Rafii, Arash

Journal of translational medicine

2013 Volume 11, Page(s) 94

Abstract: Our vision of cancer has changed during the past decades. Indeed tumors are now perceived as complex entities where tumoral and stromal components interact closely. Among the different elements of tumor stroma the cellular component play a primordial ... ...

Abstract	Our vision of cancer has changed during the past decades. Indeed tumors are now perceived as complex entities where tumoral and stromal components interact closely. Among the different elements of tumor stroma the cellular component play a primordial role. Bone Marrow derived mesenchymal cells (MSCs) are attracted to tumor sites and support tumor growth. Endothelial cells (ECs) play a major role in angiogenesis. While the literature documents many aspects of the cross talk between stromal and cancer cells, the role of direct hetero-cellular contact is not clearly established. Recently, Tunneling nanotubes (TnTs) have been shown to support cell-to-cell transfers of plasma membrane components, cytosolic molecules and organelles within cell lines. Herein, we have investigated the formation of heterocellular TnTs between stromal (MSCs and ECs) and cancer cells. We demonstrate that TnTs occur between different cancer cells, stromal cells and cancer-stromal cell lines. We showed that TnTs-like structure occurred in 3D anchorage independent spheroids and also in tumor explant cultures. In our culture condition, TnTs formation occurred after large membrane adhesion. We showed that intercellular transfers of cytoplasmic content occurred similarly between cancer cells and MSCs or ECs, but we highlighted that the exchange of mitochondria occurred preferentially between endothelial cells and cancer cells. We illustrated that the cancer cells acquiring mitochondria displayed chemoresistance. Our results illustrate the perfusion-independent role of the endothelium by showing a direct endothelial to cancer cell mitochondrial exchange associated to phenotypic modulation. This supports another role of the endothelium in the constitution of the metastatic niche.
MeSH term(s)	Bone Marrow Cells/cytology ; Cell Adhesion ; Cell Line, Tumor ; Cell Membrane/metabolism ; Cell Survival ; Coculture Techniques/methods ; Drug Resistance, Neoplasm ; Female ; Green Fluorescent Proteins/metabolism ; Humans ; MCF-7 Cells ; Mesenchymal Stem Cells/cytology ; Mitochondria/metabolism ; Nanotubes/chemistry ; Neoplasms/drug therapy ; Neoplasms/metabolism ; Neovascularization, Pathologic ; Ovarian Neoplasms/drug therapy ; Ovarian Neoplasms/metabolism
Chemical Substances	Green Fluorescent Proteins (147336-22-9)
Language	English
Publishing date	2013-04-10
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ISSN	1479-5876
ISSN (online)	1479-5876
DOI	10.1186/1479-5876-11-94
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