Tumour exosome integrins determine organotropic metastasis
Open accessAbstract
Ever since Stephen Paget's 1889 hypothesis, metastatic organotropism has remained one of cancer's greatest mysteries. Here we demonstrate that exosomes from mouse and human lung-, liver- and brain-tropic tumour cells fuse preferentially with resident cells at their predicted destination, namely lung fibroblasts and epithelial cells, liver Kupffer cells and brain endothelial cells. We show that tumour-derived exosomes uptaken by organ-specific cells prepare the pre-metastatic niche. Treatment with exosomes from lung-tropic models redirected the metastasis of bone-tropic tumour cells. Exosome proteomics revealed distinct integrin expression patterns, in which the exosomal integrins α6β4 and α6β1 were associated with lung metastasis, while exosomal integrin αvβ5 was linked to liver metastasis. Targeting the integrins α6β4 and αvβ5 decreased exosome uptake, as well as lung and liver metastasis, respectively. We demonstrate that exosome integrin uptake by resident cells activates Src phosphorylation and pro-inflammatory S100 gene expression. Finally, our clinical data indicate that exosomal integrins could be used to predict organ-specific metastasis.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Exosomes from mouse and human lung-, brain-, and liver-tropic tumor cells fuse preferentially with resident cells, namely lung fibroblasts and epithelial cells, brain endothelial cells, and liver Kupffer cells, at their predicted destination.
“In this perspective, exosomes from mouse and human lung-, brain- and liver-tropic tumor cells fuse preferentially with resident cells namely lung fibroblasts and epithelial cells, brain endothelial cells and liver Kupffer cells at their predicted destination.”
From Tumor microenvironment complexity and therapeutic implications at a glance (2020) · cites this paper as [176]
The 'Distinct cells uptake tropic exosomes' section identifies the claimed lung, liver and brain resident-cell targets for exosomes from human tumour cell lines. It describes fusion with Kupffer cells, but only co-localization with lung cells and interaction with brain endothelial cells. The 'Future metastatic sites uptake exosomes' section reports organ-specific uptake for mouse exosomes, not preferential fusion with those particular resident cells. (LLM, conf=0.86)
Experimental — accuracy not yet measuredUptake of tumor-derived exosomes prepares organ-specific cells to serve as a pre-metastatic niche.
“Furthermore, uptake of tumor-derived exosomes prepares organ-specific cells to serve as pre-metastatic niche.”
From Tumor microenvironment complexity and therapeutic implications at a glance (2020) · cites this paper as [176]
Experimental — accuracy not yet measuredIntegrin-mediated uptake of exosomes activates Src phosphorylation and pro-inflammatory S100 gene expression in resident cells.
“Finally, integrin-mediated uptake of exosome activates Src phosphorylation and pro-inflammatory S100 gene expression in resident cells [176].”
From Tumor microenvironment complexity and therapeutic implications at a glance (2020) · cites this paper as [176]
Exosomes display differential integrin expression, and blockade of integrins αvβ5 and α6β4 dampens exosome uptake and liver and lung metastasis, respectively.
“Moreover, these exosomes display differential integrin expression, and blockade of integrins αvβ5 and α6β4 dampen exosome uptake, as well as liver and lung metastasis, respectively.”
From Tumor microenvironment complexity and therapeutic implications at a glance (2020) · cites this paper as [176]
Injection of exosomes from lung-tropic models can redirect the metastasis of bone-tropic tumor cells.
“Notably, the injection of exosomes from lung-tropic models can redirect the metastasis of bone-tropic tumor cells.”
From Tumor microenvironment complexity and therapeutic implications at a glance (2020) · cites this paper as [176]
Exosomes precondition specific organs for metastatic invasion.
“Recently published article by Lyden et al (Hoshino et al., 2015), showed that exosomes precondition specific organs for metastatic invasion.”
From Tumor microenvironment derived exosomes pleiotropically modulate cancer cell metabolism (2016) · cites this paper as Hoshino et al., 2015
Tumor-derived exosomes preferentially localize to sites of metastasis including liver, lung, and bone marrow, where they promote vascular permeability and increase BMDC recruitment.
“Moreover, tumor-derived exosomes preferentially localize to sites of metastasis, including liver, lung, and bone marrow, where they promote vascular permeability and increase BMDC recruitment (101–104).”
From Hypoxic control of metastasis (2016) · cites this paper as [103]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
1 retracted
Cox, T. R., Rumney, R. M. H., Schoof, E. M., Perryman, L., Høye, A. M., Agrawal, A., Bird, D., Latif, N. A., Forrest, H., Evans, H. R., et al. (2015) · Nature · doi:10.1038/nature14492 · Cited by 482 · see citing works
RetractedValadi, H., Ekström, K., Bossios, A., Sjöstrand, M., Lee, J. J., & Lötvall, J. O. (2007) · Nature Cell Biology · doi:10.1038/ncb1596 · Cited by 12,834 · see citing works
Extracellular vesicles: Exosomes, microvesicles, and friends
Raposo, G., & Stoorvogel, W. (2013) · Journal of Cell Biology · doi:10.1083/jcb.201211138 · Cited by 8,099 · see citing works
Involvement of chemokine receptors in breast cancer metastasis
Müller, A., Homey, B., Soto, H., Ge, N., Catron, D., Buchanan, M. E., McClanahan, T., Murphy, E., Yuan, W., Wagner, S. N., et al. (2001) · Nature · doi:10.1038/35065016 · Cited by 5,340 · see citing works
The distribution of secondary growths in cancer of the breast.
Paget, S. (1889) · The Lancet · doi:10.1016/s0140-6736(00)49915-0 · Cited by 5,277 · see citing works
Cox, J., Hein, M. Y., Luber, C. A., Paron, I., Nagaraj, N., & Mann, M. (2014) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m113.031591 · Cited by 5,180 · see citing works
Skog, J., Würdinger, T., van Rijn, S., Meijer, D. H., Gainche, L., Curry, W. T., Carter, B. S., Krichevsky, A. M., & Breakefield, X. O. (2008) · Nature Cell Biology · doi:10.1038/ncb1800 · Cited by 5,001 · see citing works
Membrane vesicles as conveyors of immune responses
Théry, C., Ostrowski, M., & Segura, É. (2009) · Nature reviews. Immunology · doi:10.1038/nri2567 · Cited by 3,869 · see citing works
Integrins in cancer: biological implications and therapeutic opportunities
Desgrosellier, J. S., & Cheresh, D. A. (2009) · Nature reviews. Cancer · doi:10.1038/nrc2748 · Cited by 3,721 · see citing works
Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET
Peinado, H., Alečković, M., Lavotshkin, S., Matei, I., Costa-Silva, B., Moreno-Bueno, G., Hergueta-Redondo, M., Williams, C., García-Santos, G., Ghajar, C. M., et al. (2012) · Nature Medicine · doi:10.1038/nm.2753 · Cited by 3,715 · see citing works
Self-citationVEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche
Kaplan, R. N., Riba, R. D., Zacharoulis, S., Bramley, A. H., Vincent, L., Costa, C., MacDonald, D. D., Jin, D. K., Shido, K., Kerns, S. A., et al. (2005) · Nature · doi:10.1038/nature04186 · Cited by 3,288 · see citing works
Self-citationGenes that mediate breast cancer metastasis to lung
Minn, A. J., Gupta, G. P., Siegel, P. M., Bos, P. D., Shu, W., Giri, D. D., Viale, A., Olshen, A. B., Gerald, W. L., & Massagué, J. (2005) · Nature · doi:10.1038/nature03799 · Cited by 2,922 · see citing works
Self-citationPancreatic cancer exosomes initiate pre-metastatic niche formation in the liver
Costa-Silva, B., Aiello, N. M., Ocean, A. J., Singh, S., Zhang, H., Thakur, B. K., Becker, A., Hoshino, A., Mark, M. T., Molina, H., et al. (2015) · Nature Cell Biology · doi:10.1038/ncb3169 · Cited by 2,692 · see citing works
Self-citationRappsilber, J., Ishihama, Y., & Mann, M. (2002) · Analytical Chemistry · doi:10.1021/ac026117i · Cited by 2,589 · see citing works
A multigenic program mediating breast cancer metastasis to bone
Kang, Y., Siegel, P. M., Shu, W., Drobnjak, M., Käkönen, S.-M., Cordon‐Cardo, C., Guise, T. A., & Massagué, J. (2003) · Cancer Cell · doi:10.1016/s1535-6108(03)00132-6 · Cited by 2,562 · see citing works
Self-citationSemi-supervised learning for peptide identification from shotgun proteomics datasets
Käll, L., Canterbury, J. D., Weston, J., Noble, W. S., & MacCoss, M. J. (2007) · Nature Methods · doi:10.1038/nmeth1113 · Cited by 2,424 · see citing works
Genes that mediate breast cancer metastasis to the brain
Bos, P. D., Zhang, X. H.-F., Nadal, C., Shu, W., Gomis, R. R., Nguyen, D. X., Minn, A. J., van de Vijver, M. J., Gerald, W. L., Foekens, J. A., et al. (2009) · Nature · doi:10.1038/nature08021 · Cited by 1,863 · see citing works
Self-citationDouble-stranded DNA in exosomes: a novel biomarker in cancer detection
Thakur, B. K., Zhang, H., Becker, A., Matei, I. R., Huang, Y., Costa‐Silva, B., Zheng, Y., Hoshino, A., Brazier, H., Xiang, J., et al. (2014) · Cell Research · doi:10.1038/cr.2014.44 · Cited by 1,592 · see citing works
Self-citationAbsolute Quantification of Proteins by LCMSE
Silva, J. C., Gorenstein, M. V., Li, G.-Z., Vissers, J. P. C., & Geromanos, S. J. (2006) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m500230-mcp200 · Cited by 1,529 · see citing works
Weaver, V. M., Petersen, O. W., Wang, F., Larabell, C. A., Briand, P., Damsky, C., & Bissell, M. J. (1997) · The Journal of Cell Biology · doi:10.1083/jcb.137.1.231 · Cited by 1,483 · see citing works
Self-citationCancer-secreted miR-105 destroys vascular endothelial barriers to promote metastasis
Zhou, W., Fong, M. Y., Min, Y., Somlo, G., Liu, L., Palomares, M. R., Yu, Y., Chow, A., O’Connor, S. T. F., Chin, A. R., et al. (2014) · Cancer Cell · doi:10.1016/j.ccr.2014.03.007 · Cited by 1,476 · see citing works
Arg-Gly-Asp: A versatile cell recognition signal
Ruoslahti, E. I., & Pierschbacher, M. D. (1986) · Cell · doi:10.1016/0092-8674(86)90259-x · Cited by 1,406 · see citing works
Cancer to bone: a fatal attraction
Weilbaecher, K. N., Guise, T. A., & McCauley, L. K. (2011) · Nature reviews. Cancer · doi:10.1038/nrc3055 · Cited by 1,283 · see citing works
Tumour microvesicles contain retrotransposon elements and amplified oncogene sequences
Balaj, L., Lessard, R., Dai, L., Cho, Y., Pomeroy, S. L., Breakefield, X. O., & Skog, J. (2011) · Nature Communications · doi:10.1038/ncomms1180 · Cited by 1,185 · see citing works
Hiratsuka, S., Nakamura, K., Iwai, S., Murakami, M., Itoh, T., Kijima, H., Shipley, J. M., Senior, R. M., & Shibuya, M. (2002) · Cancer Cell · doi:10.1016/s1535-6108(02)00153-8 · Cited by 910 · see citing works
Breast cancer cells produce tenascin C as a metastatic niche component to colonize the lungs
Oskarsson, T., Acharyya, S., Zhang, X. H.-F., Vanharanta, S., Tavazoie, S. F., Morris, P. G., Downey, R. J., Manova-Todorova, K., Brogi, E., & Massagué, J. (2011) · Nature Medicine · doi:10.1038/nm.2379 · Cited by 869 · see citing works
Weaver, V. M., Lelièvre, S. A., Lakins, J. N., Chrenek, M. A., Jones, J., Giancotti, F. G., Werb, Z., & Bissell, M. J. (2002) · Cancer Cell · doi:10.1016/s1535-6108(02)00125-3 · Cited by 794 · see citing works
Self-citationDistinct organ-specific metastatic potential of individual breast cancer cells and primary tumors
Minn, A. J., Kang, Y., Serganova, I. S., Gupta, G. P., Giri, D. D., Doubrovin, M., Ponomarev, V., Gerald, W. L., Blasberg, R. G., & Massagué, J. (2005) · Journal of Clinical Investigation · doi:10.1172/jci22320 · Cited by 743 · see citing works
Self-citationTominaga, N., Kosaka, N., Ono, M., Katsuda, T., Yoshioka, Y., Tamura, K., Lötvall, J., Nakagama, H., & Ochiya, T. (2015) · Nature Communications · doi:10.1038/ncomms7716 · Cited by 724 · see citing works
The secreted factors responsible for pre-metastatic niche formation: Old sayings and new thoughts
Peinado, H., Lavotshkin, S., & Lyden, D. C. (2011) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2011.01.002 · Cited by 657 · see citing works
Self-citationProteomics, transcriptomics and lipidomics of exosomes and ectosomes
Choi, D., Kim, D., Kim, Y., & Gho, Y. S. (2013) · PROTEOMICS · doi:10.1002/pmic.201200329 · Cited by 513 · see citing works
The IL-6/JAK/Stat3 feed-forward loop drives tumorigenesis and metastasis
Chang, Q., Bournazou, E., Sansone, P., Berishaj, M., Gao, S. P., Daly, L., Wels, J., Theilen, T., Granitto, S., Zhang, X., et al. (2013) · Neoplasia · doi:10.1593/neo.13706 · Cited by 494 · see citing works
Self-citationRole of organ selectivity in the determination of metastatic patterns of B16 melanoma.
Hart, I. R., & Fidler, I. J. (1980) · PubMed · Cited by 428 · see citing works
Organotropism of Breast Cancer Metastasis
Lü, X., & Kang, Y. (2007) · Journal of Mammary Gland Biology and Neoplasia · doi:10.1007/s10911-007-9047-3 · Cited by 259 · see citing works
Self-citationSuppression of Tumor Development and Metastasis Formation in Mice Lacking the S100A4(mts1) Gene
Grum-Schwensen, B., Klingelhöfer, J., Berg, C. H., El-Naaman, C., Grigorian, M., Lukanidin, E. M., & Ambartsumian, N. S. (2005) · Cancer Research · doi:10.1158/0008-5472.can-04-4510 · Cited by 235 · see citing works
Tumor αvβ3 Integrin Is a Therapeutic Target for Breast Cancer Bone Metastases
Zhao, Y., Bachelier, R., Treilleux, I., Pujuguet, P., Peyruchaud, O., Baron, R., Clément-Lacroix, P., & Clézardin, P. (2007) · Cancer Research · doi:10.1158/0008-5472.can-06-4499 · Cited by 210 · see citing works
Weaver, V. M., Lelièvre, S. A., Lakins, J. N., Chrenek, M. A., Jones, J., Giancotti, F. G., Werb, Z., & Bissell, M. J. (2002) · University of North Texas Digital Library (University of North Texas) · doi:10.1016/s1535-6108%2802%2900125-3 · Cited by 208 · see citing works
Self-citationChen, M., Sinha, M., Luxon, B. A., et al. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m803997200 · Cited by 155 · see citing works
Building the niche: The role of the S100 proteins in metastatic growth
Lukanidin, E. M., & Sleeman, J. P. (2012) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2012.02.006 · Cited by 151 · see citing works
Nikolopoulos, S. N., Blaikie, P., Yoshioka, T., Guo, W., Puri, C., Tacchetti, C., & Giancotti, F. G. (2005) · Molecular and Cellular Biology · doi:10.1128/mcb.25.14.6090-6102.2005 · Cited by 131 · see citing works
Order and Disorder: The Role of Extracellular Matrix in Epithelial Cancer
Radisky, D. C., Muschler, J. L., & Bissell, M. J. (2002) · Cancer Investigation · doi:10.1081/cnv-120000374 · Cited by 109 · see citing works
Self-citationFocal Adhesion Kinase Activated by β4 Integrin Ligation to mCLCA1 Mediates Early Metastatic Growth
Abdel‐Ghany, M., Cheng, H.-C., Elble, R. C., & Pauli, B. U. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m205307200 · Cited by 109 · see citing works
Identifying Site-specific Metastasis Genes and FunctionsPreprint
Gupta, G. P., Minn, A. J., Kang, Y., Siegel, P. M., Serganova, I. S., Cordon‐Cardo, C., Olshen, A. B., Gerald, W. L., & Massagué, J. (2005) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.2005.70.018 · Cited by 108 · see citing works
Self-citationGrum-Schwensen, B., Klingelhöfer, J., Grigorian, M., Almholt, K., Nielsen, B. S., Lukanidin, E. M., & Ambartsumian, N. S. (2010) · Cancer Research · doi:10.1158/0008-5472.can-09-3220 · Cited by 87 · see citing works
Bäuerle, T., Komljenovic, D., Merz, M., Berger, M. R., Goodman, S. L., & Semmler, W. (2010) · International Journal of Cancer · doi:10.1002/ijc.25563 · Cited by 84 · see citing works
Bunkenborg, J., García, G. E., Paz, M. I. P., Andersen, J., & Molina, H. (2010) · PROTEOMICS · doi:10.1002/pmic.201000103 · Cited by 60 · see citing works
Self-citationPeriostin Is a Key Niche Component for Wound Metastasis of Melanoma
Fukuda, K., Sugihara, E., Ohta, S., et al. (2015) · PLoS ONE · doi:10.1371/journal.pone.0129704 · Cited by 54 · see citing works
Wu, Y., Muldoon, L. L., Gahramanov, S., et al. (2012) · Journal of Neuro-Oncology · doi:10.1007/s11060-012-0942-0 · Cited by 50 · see citing works
Kim, T. H., Kim, H. I., Soung, Y. H., et al. (2009) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-09-0102 · Cited by 49 · see citing works
Mainiero, F., Colombara, M., Antonini, V., et al. (2003) · European Journal of Immunology · doi:10.1002/eji.200323931 · Cited by 33 · see citing works
The minimum element of a synthetic peptide required to block prostate tumor cell migration
Sroka, T. C., Mařı́k, J., Pennington, M. E., et al. (2006) · Cancer Biology & Therapy · doi:10.4161/cbt.5.11.3461 · Cited by 14 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- [46]Peinado H Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET Nature Med 18 883 891 2012 22635005 PMC3645291
Cited by
Sorted by citations
The biology <b>,</b> function <b>,</b> and biomedical applications of exosomes
Kalluri, R., & LeBleu, V. S. (2020) · Science · doi:10.1126/science.aau6977 · Cited by 10,770 · see citing works
Shedding light on the cell biology of extracellular vesicles
van Niel, G., D'Angelo, G., & Raposo, G. (2018) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2017.125 · Cited by 8,369 · see citing works
Nieto, M. A., Huang, R. Y.-J., Jackson, R. A., & Thiery, J. P. (2016) · Cell · doi:10.1016/j.cell.2016.06.028 · Cited by 4,492 · see citing works
The evolving tumor microenvironment: From cancer initiation to metastatic outgrowth
de Visser, K. E., & Joyce, J. A. (2023) · Cancer Cell · doi:10.1016/j.ccell.2023.02.016 · Cited by 4,059 · see citing works
Communication by Extracellular Vesicles: Where We Are and Where We Need to Go
Tkach, M., & Théry, C. (2016) · Cell · doi:10.1016/j.cell.2016.01.043 · Cited by 3,444 · see citing works
Reassessment of exosome composition
Jeppesen, D. K., Fenix, A. M., Franklin, J. L., Higginbotham, J. N., Zhang, Q., Zimmerman, L. J., Liebler, D. C., Ping, J., Liu, Q., Evans, R., et al. (2019) · Cell · doi:10.1016/j.cell.2019.02.029 · Cited by 2,975 · see citing works
Concepts of extracellular matrix remodelling in tumour progression and metastasis
Winkler, J., Abisoye-Ogunniyan, A., Metcalf, K. J., & Werb, Z. (2020) · Nature Communications · doi:10.1038/s41467-020-18794-x · Cited by 2,296 · see citing works
Extracellular Vesicles in Cancer: Cell-to-Cell Mediators of Metastasis
Becker, A., Thakur, B. K., Weiss, J. M., Kim, H. S., Peinado, H., & Lyden, D. (2016) · Cancer Cell · doi:10.1016/j.ccell.2016.10.009 · Cited by 2,003 · see citing works
Self-citationMetastatic colonization by circulating tumour cells
Massagué, J., & Obenauf, A. C. (2016) · Nature · doi:10.1038/nature17038 · Cited by 2,062 · see citing works
Pre-metastatic niches: organ-specific homes for metastases
Peinado, H., Zhang, H., Matei, I. R., Costa-Silva, B., Hoshino, A., Rodrigues, G., Psaila, B., Kaplan, R. N., Bromberg, J. F., Kang, Y., et al. (2017) · Nature Reviews Cancer · doi:10.1038/nrc.2017.6 · Cited by 1,889 · see citing works
Self-citationCell Membrane Coating Nanotechnology
Fang, R. H., Kroll, A. V., Gao, W., & Zhang, L. (2018) · Advanced Materials · doi:10.1002/adma.201706759 · Cited by 1,885 · see citing works
Tumor microenvironment complexity and therapeutic implications at a glance
Baghban, R., Roshangar, L., Jahanban-Esfahlan, R., Seidi, K., Ebrahimi-Kalan, A., Jaymand, M., Kolahian, S., Javaheri, T., & Zare, P. (2020) · Cell Communication and Signaling · doi:10.1186/s12964-020-0530-4 · Cited by 1,784 · see citing works
“Finally, integrin-mediated uptake of exosome activates Src phosphorylation and pro-inflammatory S100 gene expression in resident cells [176].”
BackgroundRNA delivery by extracellular vesicles in mammalian cells and its applications
O’Brien, K., Breyne, K., Ughetto, S., Laurent, L. C., & Breakefield, X. O. (2020) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-020-0251-y · Cited by 1,811 · see citing works
Every step of the way: integrins in cancer progression and metastasis
Hamidi, H., & Ivaska, J. (2018) · Nature Reviews Cancer · doi:10.1038/s41568-018-0038-z · Cited by 1,493 · see citing works
Current and future perspectives of liquid biopsies in genomics-driven oncology
Heitzer, E., Haque, I. S., Roberts, C. E. S., & Speicher, M. R. (2019) · Nature Reviews Genetics · doi:10.1038/s41576-018-0071-5 · Cited by 1,557 · see citing works
Endoplasmic reticulum stress signals in the tumour and its microenvironment
Chen, X., & Cubillos-Ruiz, J. R. (2021) · Nature Reviews Cancer · doi:10.1038/s41568-020-00312-2 · Cited by 1,356 · see citing works
Suppression of Exosomal PD-L1 Induces Systemic Anti-tumor Immunity and Memory
Poggio, M., Hu, T., Pai, C.-C., Chu, B., Belair, C. D., Chang, A., Montabana, E., Lang, U. E., Fu, Q., Fong, L., et al. (2019) · Cell · doi:10.1016/j.cell.2019.02.016 · Cited by 1,376 · see citing works
Clinical Applications of Circulating Tumor Cells and Circulating Tumor DNA as Liquid Biopsy
Alix-Panabières, C., & Pantel, K. (2016) · Cancer Discovery · doi:10.1158/2159-8290.cd-15-1483 · Cited by 1,394 · see citing works
Self-citationRankin, E. B., & Giaccia, A. J. (2016) · Science · doi:10.1126/science.aaf4405 · Cited by 1,340 · see citing works
Challenges and directions in studying cell–cell communication by extracellular vesicles
van Niel, G., Carter, D. R. F., Clayton, A., Lambert, D. W., Raposo, G., & Vader, P. (2022) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-022-00460-3 · Cited by 1,229 · see citing works
Exosomes: key players in cancer and potential therapeutic strategy
Dai, J., Su, Y., Zhong, S., Cong, L., Liu, B., Yang, J., Tao, Y., He, Z., Chen, C., & Jiang, Y. (2020) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-020-00261-0 · Cited by 1,186 · see citing works
Lipids in exosomes: current knowledge and the way forward
Skotland, T., Sandvig, K., & Llorente, A. (2017) · Progress in Lipid Research · doi:10.1016/j.plipres.2017.03.001 · Cited by 1,030 · see citing works
Tumor microenvironment derived exosomes pleiotropically modulate cancer cell metabolism
Zhao, H., Yang, L., Baddour, J., Achreja, A., Bernard, V., Moss, T., Marini, J. C., Tudawe, T., Seviour, E. G., San Lucas, F. A., et al. (2016) · eLife · doi:10.7554/elife.10250 · Cited by 927 · see citing works
Role of Glutathione in Cancer: From Mechanisms to Therapies
Kennedy, L., Sandhu, J. K., Harper, M.-E., & Cuperlovic-Culf, M. (2020) · Biomolecules · doi:10.3390/biom10101429 · Cited by 880 · see citing works
Exosomes maintain cellular homeostasis by excreting harmful DNA from cells
Takahashi, A., Okada, R., Nagao, K., Kawamata, Y., Hanyu, A., Yoshimoto, S., Takasugi, M., Watanabe, S., Kanemaki, M. T., Obuse, C., et al. (2017) · Nature Communications · doi:10.1038/ncomms15287 · Cited by 761 · see citing works
Therapeutically harnessing extracellular vesicles
Cheng, L., & Hill, A. F. (2022) · Nature Reviews Drug Discovery · doi:10.1038/s41573-022-00410-w · Cited by 737 · see citing works
Haraszti, R. A., Didiot, M., Sapp, E., Leszyk, J., Shaffer, S. A., Rockwell, H. E., Gao, F., Narain, N. R., DiFiglia, M., Kiebish, M. A., et al. (2016) · Journal of Extracellular Vesicles · doi:10.3402/jev.v5.32570 · Cited by 746 · see citing works
Extracellular Vesicles and Nanoparticles: Emerging Complexities
Jeppesen, D. K., Zhang, Q., Franklin, J. L., & Coffey, R. J. (2023) · Trends in Cell Biology · doi:10.1016/j.tcb.2023.01.002 · Cited by 705 · see citing works
Application of exosomes as liquid biopsy in clinical diagnosis
Zhou, B., Xu, K., Zheng, X., Chen, T., Wang, J., Song, Y., Shao, Y., & Zheng, S. (2020) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-020-00258-9 · Cited by 685 · see citing works
Exosome–Liposome Hybrid Nanoparticles Deliver CRISPR/Cas9 System in MSCs
Lin, Y., Wu, J., Gu, W., Huang, Y., Tong, Z., Huang, L., & Tan, J. (2018) · Advanced Science · doi:10.1002/advs.201700611 · Cited by 625 · see citing works
The extracellular matrix in tumor progression and metastasis
Eble, J. A., & Niland, S. (2019) · Clinical & Experimental Metastasis · doi:10.1007/s10585-019-09966-1 · Cited by 613 · see citing works
Epigenetic inheritance of acquired traits through sperm RNAs and sperm RNA modifications
Chen, Q., Yan, W., & Duan, E. (2016) · Nature Reviews Genetics · doi:10.1038/nrg.2016.106 · Cited by 576 · see citing works
A history of exploring cancer in context
Maman, S., & Witz, I. P. (2018) · Nature Reviews Cancer · doi:10.1038/s41568-018-0006-7 · Cited by 502 · see citing works
Bertocchi, A., Carloni, S., Ravenda, P. S., Bertalot, G., Spadoni, I., Lo Cascio, A., Gandini, S., Lizier, M., Braga, D., Asnicar, F., et al. (2021) · Cancer Cell · doi:10.1016/j.ccell.2021.03.004 · Cited by 515 · see citing works
The Use of Alternative Strategies for Enhanced Nanoparticle Delivery to Solid Tumors
Izci, M., Maksoudian, C., Manshian, B. B., & Soenen, S. J. (2021) · Chemical Reviews · doi:10.1021/acs.chemrev.0c00779 · Cited by 506 · see citing works
Song, Y., Li, Z., He, T., Qu, M., Jiang, L., Li, W., Shi, X., Pan, J., Zhang, L., Wang, Y., et al. (2019) · Theranostics · doi:10.7150/thno.30879 · Cited by 487 · see citing works
Liquid Biopsies, What We Do Not Know (Yet)
Bardelli, A., & Pantel, K. (2017) · Cancer Cell · doi:10.1016/j.ccell.2017.01.002 · Cited by 482 · see citing works
Self-citationExosomes in cancer development and clinical applications
Tai, Y., Chen, K., Hsieh, J., & Shen, T. (2018) · Cancer Science · doi:10.1111/cas.13697 · Cited by 426 · see citing works
Self-citationEngineered Extracellular Vesicles for Cancer Therapy
Zhang, X., Zhang, H., Gu, J., Zhang, J., Shi, H., Qian, H., Wang, D., Xu, W., Pan, J., & Santos, H. A. (2021) · Advanced Materials · doi:10.1002/adma.202005709 · Cited by 428 · see citing works
Self-citationTakasugi, M., Okada, R., Takahashi, A., Virya Chen, D., Watanabe, S., & Hara, E. (2017) · Nature Communications · doi:10.1038/ncomms15728 · Cited by 410 · see citing works
Linkage between endosomal escape of LNP-mRNA and loading into EVs for transport to other cells
Maugeri, M., Nawaz, M., Papadimitriou, A., Angerfors, A., Camponeschi, A., Na, M., Hölttä, M., Skantze, P., Johansson, S., Sundqvist, M., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-12275-6 · Cited by 428 · see citing works
Exosomes in the tumor microenvironment as mediators of cancer therapy resistance
Li, I., & Nabet, B. Y. (2019) · Molecular Cancer · doi:10.1186/s12943-019-0975-5 · Cited by 416 · see citing works
Mechanisms associated with biogenesis of exosomes in cancer
McAndrews, K. M., & Kalluri, R. (2019) · Molecular Cancer · doi:10.1186/s12943-019-0963-9 · Cited by 394 · see citing works
Qiao, L., Hu, S., Huang, K., Su, T., Li, Z., Vandergriff, A., Cores, J., Dinh, P.-U., Allen, T., Shen, D., et al. (2020) · Theranostics · doi:10.7150/thno.39434 · Cited by 404 · see citing works
Hepatocytes direct the formation of a pro-metastatic niche in the liver
Lee, J. W., Stone, M. L., Porrett, P. M., Thomas, S. K., Komar, C. A., Li, J. H., Delman, D., Graham, K., Gladney, W. L., Hua, X., et al. (2019) · Nature · doi:10.1038/s41586-019-1004-y · Cited by 402 · see citing works
Wang, S., Zheng, Y., Yang, F., Zhu, L., Zhu, X.-Q., Wang, Z.-F., Wu, X.-L., Zhou, C.-H., Yan, J.-Y., Hu, B.-Y., et al. (2021) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-021-00659-4 · Cited by 369 · see citing works
Exosome biogenesis, bioactivities and functions as new delivery systems of natural compounds
Farooqi, A. A., Desai, N. N., Qureshi, M. Z., Librelotto, D. R. N., Gasparri, M. L., Bishayee, A., Nabavi, S. M., Curti, V., & Daglia, M. (2018) · Biotechnology Advances · doi:10.1016/j.biotechadv.2017.12.010 · Cited by 359 · see citing works
Borghesan, M., Fafián-Labora, J., Eleftheriadou, O., Carpintero-Fernández, P., Paez-Ribes, M., Vizcay-Barrena, G., Swisa, A., Kolodkin-Gal, D., Ximénez-Embún, P., Lowe, R., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.05.095 · Cited by 315 · see citing works
“, 2015), indicators of cancer metastasis (Hoshino et al., 2015), and therapeutic carriers (Kamerkar et al.”
BackgroundSelf-citationWei, H., Chen, J., Wang, S., Fu, F., Zhu, X., Wu, C., Liu, Z., Zhong, G., & Lin, J. (2019) · International Journal of Nanomedicine · doi:10.2147/ijn.s218988 · Cited by 317 · see citing works
KLF4-dependent perivascular cell plasticity mediates pre-metastatic niche formation and metastasis
Murgai, M., Ju, W., Eason, M., Kline, J., Beury, D. W., Kaczanowska, S., Miettinen, M. M., Kruhlak, M., Lei, H., Shern, J. F., et al. (2017) · Nature Medicine · doi:10.1038/nm.4400 · Cited by 263 · see citing works
Internalization of Exosomes through Receptor-Mediated Endocytosis
Gonda, A., Kabagwira, J., Senthil, G. N., & Wall, N. R. (2019) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-18-0891 · Cited by 296 · see citing works
Engineering and physical sciences in oncology: challenges and opportunities
Mitchell, M. J., Jain, R. K., & Langer, R. (2017) · Nature Reviews Cancer · doi:10.1038/nrc.2017.83 · Cited by 273 · see citing works
Glioblastoma: exosome and microRNA as novel diagnosis biomarkers
Saadatpour, L., Fadaee, E., Fadaei, S., Nassiri Mansour, R., Mohammadi, M., Mousavi, S. M., Goodarzi, M., Verdi, J., & Mirzaei, H. (2016) · Cancer Gene Therapy · doi:10.1038/cgt.2016.48 · Cited by 244 · see citing works
Extracellular Vesicles in Liver Pathobiology: Small Particles With Big Impact
Hirsova, P., Ibrahim, S. H., Verma, V. K., Morton, L. A., Shah, V. H., LaRusso, N. F., Gores, G. J., & Malhi, H. (2016) · Hepatology · doi:10.1002/hep.28814 · Cited by 229 · see citing works
TGF-&beta; signaling in cancer metastasis
Xie, F., Ling, L., Van Dam, H., Zhou, F., & Zhang, L. (2018) · Acta Biochimica et Biophysica Sinica · doi:10.1093/abbs/gmx123 · Cited by 231 · see citing works
KRAS Oncogenic Signaling Extends beyond Cancer Cells to Orchestrate the Microenvironment
Dias Carvalho, P., Guimarães, C. F., Cardoso, A. P., Mendonça, S., Costa, Â. M., Oliveira, M. J., & Velho, S. (2018) · Cancer Research · doi:10.1158/0008-5472.can-17-2084 · Cited by 202 · see citing works
Nishida-Aoki, N., Tominaga, N., Takeshita, F., Sonoda, H., Yoshioka, Y., & Ochiya, T. (2017) · Molecular Therapy · doi:10.1016/j.ymthe.2016.10.009 · Cited by 208 · see citing works
Increased Circulating Exosomal miRNA-223 Is Associated with Acute Ischemic Stroke
Chen, Y., Song, Y., Huang, J., Qu, M., Zhang, Y., Geng, J., Zhang, Z., Liu, J., & Yang, G.-Y. (2017) · Frontiers in Neurology · doi:10.3389/fneur.2017.00057 · Cited by 207 · see citing works
The crosstalk: exosomes and lipid metabolism
Wang, W., Zhu, N., Yan, T., Shi, Y.-N., Chen, J., Zhang, C.-J., Xie, X.-J., Liao, D.-F., & Qin, L. (2020) · Cell Communication and Signaling · doi:10.1186/s12964-020-00581-2 · Cited by 203 · see citing works
Exosomes as Mediators of the Systemic Adaptations to Endurance Exercise
Safdar, A., & Tarnopolsky, M. A. (2018) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a029827 · Cited by 203 · see citing works
Liu, Q., Li, D., Pan, X., & Liang, Y. (2023) · Journal of Nanobiotechnology · doi:10.1186/s12951-023-02081-0 · Cited by 201 · see citing works
Sakha, S., Muramatsu, T., Ueda, K., & Inazawa, J. (2016) · Scientific Reports · doi:10.1038/srep38750 · Cited by 201 · see citing works
Emerging tumor spheroids technologies for 3D in vitro cancer modeling
Rodrigues, T., Kundu, B., Silva-Correia, J., Kundu, S. C., Oliveira, J. M., Reis, R. L., & Correlo, V. M. (2018) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2017.10.018 · Cited by 178 · see citing works
You, Y., Borgmann, K., Edara, V. V., Stacy, S., Ghorpade, A., & Ikezu, T. (2020) · Journal of Extracellular Vesicles · doi:10.1080/20013078.2019.1706801 · Cited by 176 · see citing works
Chen, Y.-A., Lu, C.-H., Ke, C.-C., Chiu, S.-J., Jeng, F.-S., Chang, C.-W., Yang, B.-H., & Liu, R.-S. (2021) · Biomedicines · doi:10.3390/biomedicines9060594 · Cited by 167 · see citing works
Liang, Y., Iqbal, Z., Lu, J., Wang, J., Zhang, H., Chen, X., Duan, L., & Xia, J. (2023) · Molecular Therapy · doi:10.1016/j.ymthe.2022.10.008 · Cited by 162 · see citing works
Self-citationBhome, R., Goh, R. W., Bullock, M. D., Pillar, N., Thirdborough, S. M., Mellone, M., Mirnezami, R., Galea, D., Veselkov, K., Gu, Q., et al. (2017) · Aging · doi:10.18632/aging.101355 · Cited by 155 · see citing works
Wang, J., Zhu, M., & Nie, G. (2021) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2021.113974 · Cited by 153 · see citing works
Cancer-Associated Fibroblasts and Tumor-Associated Macrophages in Cancer and Cancer Immunotherapy
Raskov, H., Orhan, A., Gaggar, S., & Gögenur, I. (2021) · Frontiers in Oncology · doi:10.3389/fonc.2021.668731 · Cited by 150 · see citing works
Emerging roles and therapeutic value of exosomes in cancer metastasis
Wu, M., Wang, G., Hu, W., Yao, Y., & Yu, X.-F. (2019) · Molecular Cancer · doi:10.1186/s12943-019-0964-8 · Cited by 140 · see citing works
Liquid biopsy in the clinical management of hepatocellular carcinoma
von Felden, J., Garcia-Lezana, T., Schulze, K., Losic, B., & Villanueva, A. (2020) · Gut · doi:10.1136/gutjnl-2019-320282 · Cited by 141 · see citing works
Exosomes in cancer: Use them or target them?
Bastos, N., Ruivo, C. F., da Silva, S., & Melo, S. A. (2018) · Seminars in Cell & Developmental Biology · doi:10.1016/j.semcdb.2017.08.009 · Cited by 140 · see citing works
Garofalo, M., Saari, H., Somersalo, P., Crescenti, D., Kuryk, L., Aksela, L., Capasso, C., Madetoja, M., Koskinen, K., Oksanen, T., et al. (2018) · Journal of Controlled Release · doi:10.1016/j.jconrel.2018.05.015 · Cited by 138 · see citing works
Osteoclast-derived apoptotic bodies couple bone resorption and formation in bone remodeling
Ma, Q., Liang, M., Wu, Y., Luo, F., Ma, Z., Dong, S., Xu, J., & Dou, C. (2021) · Bone Research · doi:10.1038/s41413-020-00121-1 · Cited by 117 · see citing works
Extracellular Vesicles in Brain Tumors and Neurodegenerative Diseases
Ciregia, F., Urbani, A., & Palmisano, G. (2017) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2017.00276 · Cited by 110 · see citing works
Sullivan, R., Maresh, G., Zhang, X., Salomon, C., Hooper, J., Margolin, D., & Li, L. (2017) · Frontiers in Endocrinology · doi:10.3389/fendo.2017.00194 · Cited by 112 · see citing works
Strategies for the use of Extracellular Vesicles for the Delivery of Therapeutics
Sil, S., Dagur, R. S., Liao, K., Peeples, E. S., Hu, G., Periyasamy, P., & Buch, S. (2020) · Journal of Neuroimmune Pharmacology · doi:10.1007/s11481-019-09873-y · Cited by 109 · see citing works
Dar, G. H., Mendes, C. C., Kuan, W.-L., Speciale, A. A., Conceição, M., Görgens, A., Uliyakina, I., Lobo, M. J., Lim, W. F., EL Andaloussi, S., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-27056-3 · Cited by 100 · see citing works
Molecular alterations of cancer cell and tumour microenvironment in metastatic gastric cancer
Li, W., Ng, J. M.-K., Wong, C. C., Ng, E. K. W., & Yu, J. (2018) · Oncogene · doi:10.1038/s41388-018-0341-x · Cited by 87 · see citing works
Engineering strategies for customizing extracellular vesicle uptake in a therapeutic context
Esmaeili, A., Alini, M., Baghaban Eslaminejad, M., & Hosseini, S. (2022) · Stem Cell Research & Therapy · doi:10.1186/s13287-022-02806-2 · Cited by 94 · see citing works
Current advances in non‐viral gene delivery systems: Liposomes versus extracellular vesicles
Belhadj, Z., Qie, Y., Carney, R. P., Li, Y., & Nie, G. (2023) · BMEMat · doi:10.1002/bmm2.12018 · Cited by 79 · see citing works
Engineered extracellular vesicles as brain therapeutics
Lino, M. M., Simões, S., Tomatis, F., Albino, I., Barrera, A., Vivien, D., Sobrino, T., & Ferreira, L. (2021) · Journal of Controlled Release · doi:10.1016/j.jconrel.2021.08.037 · Cited by 68 · see citing works
Fuller, O. K., Whitham, M., Mathivanan, S., & Febbraio, M. A. (2020) · Cells · doi:10.3390/cells9102182 · Cited by 60 · see citing works
Roles of Macrophages and Exosomes in Liver Diseases
Shen, M., Shen, Y., Fan, X., Men, R., Ye, T., & Yang, L. (2020) · Frontiers in Medicine · doi:10.3389/fmed.2020.583691 · Cited by 61 · see citing works
Bezdan, D., Grigorev, K., Meydan, C., Pelissier Vatter, F. A., Cioffi, M., Rao, V., MacKay, M., Nakahira, K., Burnham, P., Afshinnekoo, E., et al. (2020) · iScience · doi:10.1016/j.isci.2020.101844 · Cited by 59 · see citing works
Self-citationMazumdar, A., Urdinez, J., Boro, A., Arlt, M. J. E., Egli, F. E., Niederöst, B., Jaeger, P. K., Moschini, G., Muff, R., Fuchs, B., et al. (2020) · Cancers · doi:10.3390/cancers12113457 · Cited by 40 · see citing works
Network approach in liquidomics landscape
Santini, D., Botticelli, A., Galvano, A., Iuliani, M., Incorvaia, L., Gristina, V., Taffon, C., Foderaro, S., Paccagnella, E., Simonetti, S., et al. (2023) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-023-02743-9 · Cited by 37 · see citing works
Engineering exosomes for bone defect repair
Ma, S., Zhang, Y., Li, S., Li, A., Li, Y., & Pei, D. (2022) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2022.1091360 · Cited by 38 · see citing works
Ma, Y., Nenkov, M., Chen, Y., & Gaßler, N. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25158352 · Cited by 28 · see citing works
Kortüm, B., Radhakrishnan, H., Zincke, F., Sachse, C., Burock, S., Keilholz, U., Dahlmann, M., Walther, W., Dittmar, G., Kobelt, D., et al. (2022) · Oncogene · doi:10.1038/s41388-022-02407-6 · Cited by 26 · see citing works
Post-COVID-19 Parkinsonism and Parkinson’s Disease Pathogenesis: The Exosomal Cargo Hypothesis
Mysiris, D. S., Vavougios, G. D., Karamichali, E., Papoutsopoulou, S., Stavrou, V. T., Papayianni, E., Boutlas, S., Mavridis, T., Foka, P., Zarogiannis, S. G., et al. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23179739 · Cited by 25 · see citing works
Han, S., Xue, L., Wei, Y., Yong, T., Jia, W., Qi, Y., Luo, Y., Liang, J., Wen, J., Bie, N., et al. (2023) · Advanced Science · doi:10.1002/advs.202207080 · Cited by 24 · see citing works
Li, Z., Ma, L., Chen, M., Chen, X., Sha, M., & Hang, H. (2025) · JHEP Reports · doi:10.1016/j.jhepr.2024.101275 · Cited by 11 · see citing works
Molecular Regulation and Oncogenic Functions of TSPAN8
Yang, J., Zhang, Z., Lam, J. S. W., Fan, H., & Fu, N. Y. (2024) · Cells · doi:10.3390/cells13020193 · Cited by 11 · see citing works
Extracellular Vesicles and Their Interplay with Biological Membranes
Yeo Xian Ping, J., Raj Neupane, Y., & Pastorin, G. (2022) · Physiology · doi:10.5772/intechopen.101297 · Cited by 9 · see citing works
- Authors
- Hoshino, A., Costa-Silva, B., Shen, T.-L., Rodrigues, G., Hashimoto, A., Tesic Mark, M., Molina, H., Kohsaka, S., Di Giannatale, A., Ceder, S., Singh, S., Williams, C., Soplop, N., Uryu, K., Pharmer, L., King, T., Bojmar, L., Davies, A. E., Ararso, Y., Zhang, T., Zhang, H., Hernandez, J., Weiss, J. M., Dumont-Cole, V. D., Kramer, K., Wexler, L. H., Narendran, A., Schwartz, G. K., Healey, J. H., Sandstrom, P., Jørgen Labori, K., Kure, E. H., Grandgenett, P. M., Hollingsworth, M. A., de Sousa, M., Kaur, S., Jain, M., Mallya, K., Batra, S. K., Jarnagin, W. R., Brady, M. S., Fodstad, O., Muller, V., Pantel, K., Minn, A. J., Bissell, M. J., Garcia, B. A., Kang, Y., Rajasekhar, V. K., Ghajar, C. M., Matei, I., Peinado, H., Bromberg, J., & Lyden, D.
- Affiliations
- Children's Cancer and Blood Foundation (US)
- National Taiwan University (TW)
- Rockefeller University (US)
- Memorial Sloan Kettering Cancer Center (US)
- Karolinska Institutet (SE)
- Linköping University (SE)
- Lawrence Berkeley National Laboratory (US)
- Weill Cornell Medicine (US)
- Alberta Children's Hospital (CA)
- Columbia University Irving Medical Center (US)
- Oslo University Hospital (NO)
- University of Nebraska Medical Center (US)
- Universität Hamburg (DE)
- University Medical Center Hamburg-Eppendorf (DE)
- University of Pennsylvania (US)
- Princeton University (US)
- Fred Hutch Cancer Center (US)
- Corresponding author
- Bromberg, Jacqueline
- Lyden, David
- ORCID
- Hoshino, Ayuko
- Shen, Tang-Long
- Hashimoto, Ayako
- Molina, Henrik
- Kohsaka, Shinji
- Ceder, Sophia
- Singh, Swarnima
- Soplop, Nadine
- Uryu, Kunihiro
- King, Tari
- Bojmar, Linda
- Davies, Alexander E.
- Zhang, Tuo
- Zhang, Haiying
- Hernandez, Jonathan
- Weiss, Joshua M.
- Wexler, Leonard H.
- Narendran, Aru
- Schwartz, Gary K.
- Healey, John H.
- Kure, Elin H.
- Grandgenett, Paul M.
- Hollingsworth, Michael A.
- Kaur, Sukhwinder
- Jain, Maneesh
- Mallya, Kavita
- Batra, Surinder K.
- Jarnagin, William R.
- Brady, Mary S.
- Pantel, Klaus
- Minn, Andy J.
- Bissell, Mina J.
- Garcia, Benjamin A.
- Kang, Yibin
- Rajasekhar, Vinagolu K.
- Ghajar, Cyrus M.
- Matei, Irina
- Bromberg, Jacqueline
- Lyden, David
- Venue
- Nature
- Published
- 2015-10-28
- Volume
- 527
- Issue
- 7578
- Pages
- 329-335
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC4788391
- OpenAlex
- W1950118853
- Cited by
- 5,101
- References
- 51
- Citations by year
- 2026: 416 · 2025: 455 · 2024: 491 · 2023: 517 · 2022: 566 · 2021: 611 · 2020: 577 · 2019: 470 · 2018: 413 · 2017: 346 · 2016: 228 · 2015: 9 · 2014: 1
- FWCI
- 144.23
- Type
- journal article
- Language
- en
- Update notices
- expression_of_concern (2026-08-05)
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- OSTI OAI (U.S. Department of Energy Office of Scientific and Technical Information) (submittedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- U.S. Department of Defense (P30CA008748, W81XWH, W81XWH-13)
- Breast Cancer Alliance (P30 CA008748)
- Ira Sohn Research Conference Foundation
- Melanoma Research Alliance
- Hartwell Foundation
- Memorial Sloan-Kettering Cancer Center (CA008748, P30 CA008748)
- Hospital for Special Surgery
- National Institutes of Health (W81XWH, CA008748)
- Japan Society for the Promotion of Science
- National Cancer Institute (CA169416, CA008748, U01CA169538, CA169538, R01CA169416, P30CA008748, R50CA211462)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Extracellular vesicles in disease
- Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
- Health Sciences › Medicine › Immunology and Allergy › Cell Adhesion Molecules Research
- Keywords
- organotropic metastasis, integrins, exosome uptake, pre-metastatic niche, alpha6beta4 integrin, integrin αvβ5, alpha6beta1 integrin, extracellular vesicles, lung metastasis, liver metastasis, brain metastases, Src phosphorylation, integrin-targeted therapy, metastasis prediction
- MeSH terms
- Animals, Brain, Epithelial Cells, Female, Fibroblasts, Humans, Kupffer Cells, Liver, Lung, Mice, Inbred C57BL, Neoplasm Metastasis, S100 Proteins, Organ Specificity, Phosphorylation, Biomarkers, Integrins, Genes, src, Tropism, Receptors, Vitronectin, Integrin alpha6beta1, Integrin alpha6beta4, Integrin beta Chains, Integrin beta4, Endothelial Cells, Cell Line, Tumor, Mice, Exosomes
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
