Pancreatic cancer exosomes initiate pre-metastatic niche formation in the liver

Costa-Silva, Bruno; Aiello, Nicole M.; Ocean, Allyson J.; Singh, Swarnima; Zhang, Haiying; Thakur, Basant Kumar; Becker, Annette; Hoshino, Ayuko; Mark, Milica Tešić; Molina, Henrik; Xiang, Jenny; Zhang, Tuo; Theilen, Till-Martin; García-Santos, Guillermo; Williams, Caitlin; Ararso, Yonathan; Huang, Yujie; Rodrigues, Gonçalo; Shen, Tang-Long; Labori, Knut Jørgen; Lothe, Inger Marie Bowitz; Kure, Elin H.; Hernandez, Jonathan; Doussot, Alexandre; Ebbesen, Saya H.; Grandgenett, Paul M.; Hollingsworth, Michael A.; Jain, Maneesh; Mallya, Kavita; Batra, Surinder K.; Jarnagin, William R.; Schwartz, Robert E.; Matei, Irina; Peinado, Héctor; Stanger, Ben Z.; Bromberg, Jacqueline; Lyden, David

doi:10.1038/ncb3169

Cited by 2,692Extracellular vesicles in diseasePancreatic and Hepatic Oncology ResearchCancer Cells and Metastasis

Pancreatic cancer exosomes initiate pre-metastatic niche formation in the liver

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Costa-Silva, Bruno, Aiello, Nicole M., Ocean, Allyson J., Singh, Swarnima, Zhang, Haiying, Thakur, Basant Kumar, Becker, Annette, Hoshino, Ayuko +29 more·2015·Nature Cell Biology

DOI 10.1038/ncb3169PMC PMC5769922

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Abstract

Pancreatic ductal adenocarcinomas (PDACs) are highly metastatic with poor prognosis, mainly due to delayed detection. We hypothesized that intercellular communication is critical for metastatic progression. Here, we show that PDAC-derived exosomes induce liver pre-metastatic niche formation in naive mice and consequently increase liver metastatic burden. Uptake of PDAC-derived exosomes by Kupffer cells caused transforming growth factor β secretion and upregulation of fibronectin production by hepatic stellate cells. This fibrotic microenvironment enhanced recruitment of bone marrow-derived macrophages. We found that macrophage migration inhibitory factor (MIF) was highly expressed in PDAC-derived exosomes, and its blockade prevented liver pre-metastatic niche formation and metastasis. Compared with patients whose pancreatic tumours did not progress, MIF was markedly higher in exosomes from stage I PDAC patients who later developed liver metastasis. These findings suggest that exosomal MIF primes the liver for metastasis and may be a prognostic marker for the development of PDAC liver metastasis.

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Exosomes contain proteins, nucleic acids, and miRNAs.
“Recent studies indicate that they contain proteins, nucleic acids and miRNAs (Ekström et al., 2012; Costa-Silva et al., 2015; Simons and Raposo, 2009).”
From Tumor microenvironment derived exosomes pleiotropically modulate cancer cell metabolism (2016) · cites this paper as Costa-Silva et al., 2015
Exosomes carry a complex cargo that includes proteins, lipids, and miRNAs.
“Exosomes are known to carry a complex cargo that includes proteins, lipids, and miRNAs (Costa-Silva et al., 2015; Simons and Raposo, 2009).”
From Tumor microenvironment derived exosomes pleiotropically modulate cancer cell metabolism (2016) · cites this paper as Costa-Silva 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 [102]

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Aziz, J., Shezali, H., Radzi, Z., Yahya, N. A., Abu Kassim, N. H., Czernuszka, J., & Rahman, M. T. (2016) · Skin Pharmacology and Physiology · doi:10.1159/000447017 · Cited by 7,323 · see citing works
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Noy, R., & Pollard, J. W. (2014) · Immunity · doi:10.1016/j.immuni.2014.06.010 · Cited by 4,089 · see citing works
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Pickup, M. W., Novitskiy, S. V., & Moses, H. L. (2013) · Nature reviews. Cancer · doi:10.1038/nrc3603 · Cited by 915 · see citing works
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Record, M., Carayon, K., Poirot, M., & Silvente‐Poirot, S. (2013) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2013.10.004 · Cited by 853 · see citing works
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Wight, T. N., & Potter‐Perigo, S. (2011) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00132.2011 · Cited by 669 · see citing works
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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
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Zhong, S., Joung, J., Zheng, Y., Chen, Y.-R., Liu, B., Shao, Y., Xiang, J., Fei, Z., & Giovannoni, J. J. (2011) · Cold Spring Harbor Protocols · doi:10.1101/pdb.prot5652 · Cited by 471 · see citing works
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Sceneay, J., Smyth, M. J., & Möller, A. (2013) · Cancer and Metastasis Reviews · doi:10.1007/s10555-013-9420-1 · Cited by 422 · see citing works
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Ijichi, H., Chytil, A., Gorska, A. E., Aakre, M. E., Fujitani, Y., Fujitani, S., Wright, C. V. E., & Moses, H. L. (2006) · Genes & Development · doi:10.1101/gad.1475506 · Cited by 379 · see citing works
Extracellular vesicles as an emerging mechanism of cell-to-cell communication
Tetta, C., Ghigo, E., Silengo, L., Deregibus, M. C., & Camussi, G. (2012) · Endocrine · doi:10.1007/s12020-012-9839-0 · Cited by 377 · see citing works
In vivo selection of highly metastatic cells from surgical specimens of different primary human colon carcinomas implanted into nude mice.
Morikawa, K., Walker, S. M., Jessup, J. M., & Fidler, I. J. (1988) · PubMed · Cited by 364 · see citing works
Plasma fibronectin supports neuronal survival and reduces brain injury following transient focal cerebral ischemia but is not essential for skin-wound healing and hemostasis.
Sakai, T., Johnson, K. J., Murozono, M., Sakai, K., Magnuson, M. A., Wieloch, T. W., Cronberg, T., Isshiki, A., Erickson, H., & Fässler, R. (2001) · Nature Medicine · doi:10.1038/85471 · Cited by 359 · see citing works
Induction and chemotherapeutic response of two transplantable ductal adenocarcinomas of the pancreas in C57BL/6 mice.
Corbett, T. H., Roberts, B. J., Leopold, W. R., Peckham, J. C., Wilkoff, L. J., Griswold, D. P., & Schabel, F. M. (1984) · PubMed · Cited by 356 · see citing works
The ALK‐5 inhibitor A‐83‐01 inhibits Smad signaling and epithelial‐to‐mesenchymal transition by transforming growth factor‐β
Tojo, M., Hamashima, Y., Hanyu, A., Kajimoto, T., Saitoh, M., Miyazono, K., Node, M., & Imamura, T. (2005) · Cancer Science · doi:10.1111/j.1349-7006.2005.00103.x · Cited by 340 · see citing works
LY2109761, a novel transforming growth factor β receptor type I and type II dual inhibitor, as a therapeutic approach to suppressing pancreatic cancer metastasis
Melisi, D., Ishiyama, S., Sclabas, G. M., Fleming, J. B., Xia, Q., Tortora, G., Abbruzzese, J. L., & Chiao, P. J. (2008) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-07-0337 · Cited by 324 · see citing works
Pancreatic adenocarcinoma induces bone marrow mobilization of myeloid-derived suppressor cells which promote primary tumor growth
Porembka, M. R., Mitchem, J. B., Belt, B. A., Hsieh, C., Lee, H.-M., Herndon, J. M., Gillanders, W. E., Linehan, D. C., & Goedegebuure, P. S. (2012) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-011-1178-0 · Cited by 278 · see citing works
Differences in Survival by Histologic Type of Pancreatic Cancer
Fesinmeyer, M. D., Austin, M. A., Li, C. I., Roos, A. J. D., & Bowen, D. J. (2005) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-05-0120 · Cited by 270 · see citing works
Role of Pancreatic Cancer-derived Exosomes in Salivary Biomarker Development
Lau, C., Kim, Y., Chia, D., Spielmann, N., Eibl, G., Elashoff, D., Wei, F., Lin, Y.-L., Moro, A., Grogan, T., et al. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.452458 · Cited by 256 · see citing works
Direct lineage tracing reveals the ontogeny of pancreatic cell fates during mouse embryogenesis.
Gu, G.-Q., Brown, J. R., & Melton, D. (2003) · Mechanisms of Development · doi:10.1016/s0925-4773(02)00330-1 · Cited by 236 · see citing works
Tissue inhibitor of metalloproteinases (TIMP)‐1 creates a premetastatic niche in the liver through SDF‐1/CXCR4‐dependent neutrophil recruitment in mice
Seubert, B., Grünwald, B. T., Kobuch, J., Cui, H., Schelter, F., Schaten, S., Siveke, J. T., Lim, N. H., Nagase, H., Simonavicius, N., et al. (2014) · Hepatology · doi:10.1002/hep.27378 · Cited by 213 · see citing works
Tumor-cell-derived microvesicles as carriers of molecular information in cancer
Martins, V. R., Dias, M. S., & Hainaut, P. L. (2012) · Current Opinion in Oncology · doi:10.1097/cco.0b013e32835b7c81 · Cited by 211 · see citing works
Transforming Growth Factor-β in the Gastrointestinal and Hepatic Tumor Microenvironment
Achyut, B. R., & Yang, H. H. (2011) · Gastroenterology · doi:10.1053/j.gastro.2011.07.048 · Cited by 200 · see citing works
Control of Tumor-Associated Macrophage Alternative Activation by Macrophage Migration Inhibitory Factor
Yaddanapudi, K., Putty, K., Rendon, B. E., Lamont, G. J., Faughn, J., Satoskar, A. R., Lasnik, A. B., Eaton, J. W., & Mitchell, R. A. (2013) · The Journal of Immunology · doi:10.4049/jimmunol.1201650 · Cited by 184 · see citing works
Macrophage migration inhibitory factor (MIF) exerts antifibrotic effects in experimental liver fibrosis via CD74
Heinrichs, D., Knauel, M., Offermanns, C., Berres, M., Nellen, A., Leng, L., Schmitz, P., Bucala, R., Trautwein, C., Weber, C., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1107023108 · Cited by 158 · see citing works
Therapeutic Efficacy of Bifunctional siRNA Combining TGF-β1 Silencing with RIG-I Activation in Pancreatic Cancer
Ellermeier, J., Wei, J., Duewell, P., Hoves, S., Stieg, M. R., Adunka, T., Noerenberg, D., Anders, H., Mayr, D. C., Poeck, H., et al. (2013) · Cancer Research · doi:10.1158/0008-5472.can-11-3850 · Cited by 155 · see citing works
Role of Kupffer cells in arresting circulating tumor cells and controlling metastatic growth in the liver
Bayón, L. G., Izquierdo, M. A., Sirovich, I., van Rooijen, N., Beelen, R. H. J., & Meijer, S. (1996) · Hepatology · doi:10.1002/hep.510230542 · Cited by 150 · see citing works
The association between tumour progression and vascularity in the oral mucosa
Pazouki, S., CHISHOLM, D. M., Adi, M. M., Carmichael, G., Farquharson, M., Ogden, G. R., Schor, S. L., & Schor, A. M. (1997) · The Journal of Pathology · doi:10.1002/(sici)1096-9896(199709)183:1 · Cited by 149 · see citing works
Macrophage migration inhibitory factor induces epithelial to mesenchymal transition, enhances tumor aggressiveness and predicts clinical outcome in resected pancreatic ductal adenocarcinoma
Funamizu, N., Hu, C., Lacy, C., Schetter, A. J., Zhang, G., He, P., Gaedcke, J., Ghadimi, M. B., Ghadimi, Β. M., Yfantis, H. G., et al. (2012) · International Journal of Cancer · doi:10.1002/ijc.27736 · Cited by 133 · see citing works
Biomarkers of TGF-β Signaling Pathway and Prognosis of Pancreatic Cancer
Javle, M. M., Li, Y., Tan, D., Dong, X., Chang, P., Kar, S., & Li, D. (2014) · PLoS ONE · doi:10.1371/journal.pone.0085942 · Cited by 130 · see citing works
Inhibition of Transforming Growth Factor β Signaling Reduces Pancreatic Adenocarcinoma Growth and Invasiveness
Gaspar, N. J., Li, L., Kapoun, A. M., Medicherla, S., Reddy, M., Li, G., O’Young, G., Quon, D. H., Henson, M., Damm, D. L., et al. (2007) · Molecular Pharmacology · doi:10.1124/mol.106.029025 · Cited by 120 · see citing works
Biological Significance of Local TGF-β Activation in Liver Diseases
Hayashi, H., & Sakai, T. (2012) · Frontiers in Physiology · doi:10.3389/fphys.2012.00012 · Cited by 110 · see citing works
TSU68 Prevents Liver Metastasis of Colon Cancer Xenografts by Modulating the Premetastatic Niche
Yamamoto, M., Kikuchi, H., Ohta, M., Kawabata, T., Hiramatsu, Y., Kondo, K., Baba, M., Kamiya, K., Tanaka, T., Kitagawa, M., et al. (2008) · Cancer Research · doi:10.1158/0008-5472.can-08-1748 · Cited by 105 · see citing works
Knockdown of the β 1 integrin subunit reduces primary tumor growth and inhibits pancreatic cancer metastasis
Grzesiak, J. J., Cao, H. S. T., Burton, D. W., Kaushal, S., Vargas, F., Clopton, P., Snyder, C. S., Deftos, L. J., Hoffman, R. M., & Bouvet, M. (2011) · International Journal of Cancer · doi:10.1002/ijc.25942 · Cited by 104 · see citing works
TGF-β and αvβ6 Integrin Act in a Common Pathway to Suppress Pancreatic Cancer Progression
Hezel, A. F., Deshpande, V., Zimmerman, S. M., Contino, G., Alagesan, B., O’Dell, M. R., Rivera, L. B., Harper, J. W., Lonning, S. M., Brekken, R. A., et al. (2012) · Cancer Research · doi:10.1158/0008-5472.can-12-0634 · Cited by 99 · see citing works
Targeting the transforming growth factor-β signalling pathway in metastatic cancer
Korpal, M., & Kang, Y. (2010) · European Journal of Cancer · doi:10.1016/j.ejca.2010.02.040 · Cited by 92 · see citing works
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Saif, M. W. (2015) · PubMed · doi:10.6092/1590-8577/3071 · Cited by 89 · see citing works
Fibronectin Protects from Excessive Liver Fibrosis by Modulating the Availability of and Responsiveness of Stellate Cells to Active TGF-β
Kawelke, N., Vasel, M., Sens, C., von Au, A., Dooley, S., & Nakchbandi, I. A. (2011) · PLoS ONE · doi:10.1371/journal.pone.0028181 · Cited by 84 · see citing works
Bimodal role of Kupffer cells during colorectal cancer liver metastasis
Wen, S., Ager, E. I., & Christophi, C. (2013) · Cancer Biology & Therapy · doi:10.4161/cbt.24593 · Cited by 81 · see citing works
Macrophage migration inhibitory factor contributes to ethanol-induced liver injury by mediating cell injury, steatohepatitis, and steatosis
Barnes, M. A., McMullen, M. R., Roychowdhury, S., Pisano, S. G., Liu, X., Stavitsky, A. B., & Nagy, L. E. (2012) · Hepatology · doi:10.1002/hep.26169 · Cited by 79 · see citing works
Pancreatic cancer diagnosis by free and exosomal miRNA
Zöller, M. (2013) · World Journal of Gastrointestinal Pathophysiology · doi:10.4291/wjgp.v4.i4.74 · Cited by 78 · see citing works
Cell Signals Influencing Hepatic Fibrosis
Cong, M., Iwaisako, K., Jiang, C., & Kisseleva, T. (2012) · International Journal of Hepatology · doi:10.1155/2012/158547 · Cited by 70 · see citing works
Development and characterization of a reliable mouse model of colorectal cancer metastasis to the liver
Zhang, Y., Davis, C., Ryan, J. C., Janney, C., & Peña, M. M. O. (2013) · Clinical & Experimental Metastasis · doi:10.1007/s10585-013-9591-8 · Cited by 67 · see citing works
Prevention of Lethal Acute Hepatic Failure by Antimacrophage Migration Inhibitory Factor Antibody in Mice Treated With Bacille Calmette–Guerin and Lipopolysaccharide
Kobayashi, S., Nishihira, J., Watanabe, S., et al. (1999) · Hepatology · doi:10.1002/hep.510290610 · Cited by 65 · see citing works
Strategies for discovering novel pancreatic cancer biomarkers
Chan, A., Diamandis, E. P., & Blasutig, I. M. (2012) · Journal of Proteomics · doi:10.1016/j.jprot.2012.09.025 · Cited by 59 · see citing works
ISO-1, a Macrophage Migration Inhibitory Factor Antagonist, Inhibits Airway Remodeling in a Murine Model of Chronic Asthma
Chen, P., Luo, Y.-L., Wang, W., et al. (2010) · Molecular Medicine · doi:10.2119/molmed.2009.00128 · Cited by 56 · see citing works
Macrophage Migration Inhibitory Factor Enzymatic Activity, Lung Inflammation, and Cystic Fibrosis
Adamali, H. I., Armstrong, M. E., McLaughlin, A. M., Cooke, G., McKone, E. F., Costello, C. M., Gallagher, C. G., Leng, L., Baugh, J. A., Fingerle‐Rowson, G., et al. (2012) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.201110-1864oc · Cited by 51 · see citing works
Macrophages promote tumour growth and liver metastasis in an orthotopic syngeneic mouse model of colon cancer
Kruse, J., von Bernstorff, W., Evert, K., et al. (2013) · International Journal of Colorectal Disease · doi:10.1007/s00384-013-1703-z · Cited by 49 · see citing works
Chimeric scFv/γ receptor-mediated T-cell lysis of tumor cells is coregulated by adhesion and accessory molecules
Weijtens, M. E. M., Willemsen, R. A., Krimpen, B. A. V., & Bolhuis, R. L. H. (1998) · International Journal of Cancer · doi:10.1002/(sici)1097-0215(19980717)77:2 · Cited by 45 · see citing works
A new type of antimetastatic peptide derived from fibronectin.
Kato, R., Ishikawa, T., Kamiya, S., et al. (2002) · PubMed · Cited by 40 · see citing works
Stromal cell-derived factor-1α and macrophage migration-inhibitory factor induce metastatic behavior in CXCR4-expressing colon cancer cells
SHIN, H.-N., Moon, H., & Ku, J. (2012) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2012.1141 · Cited by 31 · see citing works
Exosome characterization from ascitic fluid holds promise for identifying markers of colorectal cancer.
Arscott, W. T., & Camphausen, K. A. (2011) · PubMed · Cited by 26 · see citing works
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Arscott, W. T., & Camphausen, K. A. (2011) · Biomarkers in Medicine · doi:10.2217/bmm.11.80 · Cited by 24 · see citing works
Analysis of urinary exosomes to identify new markers of non-small-cell lung cancer.
Arscott, W. T., & Camphausen, K. A. (2011) · PubMed · Cited by 22 · see citing works
Novel Immunocompetent Murine Models Representing Advanced Local and Metastatic Pancreatic Cancer
Little, E. C., Wang, C., Watson, P. M., Watson, D. K., Cole, D. J., & Camp, E. R. (2011) · Journal of Surgical Research · doi:10.1016/j.jss.2011.10.025 · Cited by 21 · see citing works
Macrophage migration inhibitory factor expression correlates with inflammatory changes in human chronic hepatitis B infection
Zhang, H., Nanji, A. A., Luk, J. M., Huang, X., Lo, C., Chen, Y. X., Yuen, S., Lan, H. Y., & Lau, G. K. K. (2005) · Liver International · doi:10.1111/j.1478-3231.2005.01047.x · Cited by 20 · see citing works
Self-citation
Macrophage Migration Inhibitory Factor Expression in Male and Female Ethanol-Fed Rats
Nanji, A. A., Lau, G. K. K., Tipoe, G. L., Yuen, S. T., Chen, Y. X., Thomas, P., & Lan, H. Y. (2001) · Journal of Interferon & Cytokine Research · doi:10.1089/107999001317205187 · Cited by 14 · see citing works
Inhibition of hepatic metastasis in mice treated with cell-binding domain of human fibronectin and angiogenesis inhibitor TNP-470
Saito, N., Mitsuhashi, M., Hayashi, T., et al. (2001) · International Journal of Clinical Oncology · doi:10.1007/pl00012108 · Cited by 13 · see citing works
Therapy for hepatic fibrosis: Revisiting the preclinical models
Bissell, D. M. (2011) · Clinics and Research in Hepatology and Gastroenterology · doi:10.1016/j.clinre.2011.03.009 · Cited by 13 · see citing works
A Versatile Technique for the In Vivo Imaging of Human Tumor Xenografts Using Near-Infrared Fluorochrome-Conjugated Macromolecule Probes
Suemizu, H., Kawai, K., Higuchi, Y., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0082708 · Cited by 8 · see citing works

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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
Roles of the immune system in cancer: From tumor initiation to metastatic progression
Gonzalez, H., Hagerling, C., & Werb, Z. (2018) · Genes & Development · doi:10.1101/gad.314617.118 · Cited by 2,111 · 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-citation
Metastatic 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-citation
Targeting metastasis
Steeg, P. S. (2016) · Nature Reviews Cancer · doi:10.1038/nrc.2016.25 · Cited by 1,363 · see citing works
Hypoxic control of metastasis
Rankin, E. B., & Giaccia, A. J. (2016) · Science · doi:10.1126/science.aaf4405 · Cited by 1,340 · see citing works
Adipose tissue macrophage-derived exosomal miRNAs can modulate in vivo and in vitro insulin sensitivity
Ying, W., Riopel, M., Bandyopadhyay, G., Dong, Y., Birmingham, A., Seo, J. B., Ofrecio, J. M., Wollam, J., Hernandez-Carretero, A., Fu, W., et al. (2017) · Cell · doi:10.1016/j.cell.2017.08.035 · Cited by 1,191 · 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
Single-cell RNA sequencing reveals stromal evolution into LRRC15(+) myofibroblasts as a determinant of patient response to cancer immunotherapy
Dominguez, C. X., Müller, S., Keerthivasan, S., Koeppen, H., Hung, J., Gierke, S., Breart, B., Foreman, O., Bainbridge, T. W., Castiglioni, A., et al. (2020) · Cancer Discovery · doi:10.1158/2159-8290.cd-19-0644 · Cited by 857 · see citing works
Cancer stem cells as key drivers of tumour progression
Ayob, A. Z., & Ramasamy, T. S. (2018) · Journal of Biomedical Science · doi:10.1186/s12929-018-0426-4 · Cited by 910 · see citing works
CAFs secreted exosomes promote metastasis and chemotherapy resistance by enhancing cell stemness and epithelial-mesenchymal transition in colorectal cancer
Hu, J. L., Wang, W., Lan, X. L., Zeng, Z. C., Liang, Y. S., Yan, Y. R., Song, F. Y., Wang, F. F., Zhu, X. H., Liao, W. J., et al. (2019) · Molecular Cancer · doi:10.1186/s12943-019-1019-x · Cited by 773 · 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
Macrophage Polarization in Chronic Inflammatory Diseases: Killers or Builders?
Parisi, L., Gini, E., Baci, D., Tremolati, M., Fanuli, M., Bassani, B., Farronato, G., Bruno, A., & Mortara, L. (2018) · Journal of Immunology Research · doi:10.1155/2018/8917804 · Cited by 508 · 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
Gut vascular barrier impairment leads to intestinal bacteria dissemination and colorectal cancer metastasis to liver
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
Fibroblast-macrophage reciprocal interactions in health, fibrosis, and cancer
Buechler, M. B., Fu, W., & Turley, S. J. (2021) · Immunity · doi:10.1016/j.immuni.2021.04.021 · Cited by 494 · see citing works
Spatial architecture of the immune microenvironment orchestrates tumor immunity and therapeutic response
Fu, T., Dai, L.-J., Wu, S.-Y., Xiao, Y., Ma, D., Jiang, Y.-Z., & Shao, Z.-M. (2021) · Journal of Hematology & Oncology · doi:10.1186/s13045-021-01103-4 · Cited by 480 · see citing works
Macrophage-secreted granulin supports pancreatic cancer metastasis by inducing liver fibrosis
Nielsen, S. R., Quaranta, V., Linford, A., Emeagi, P., Rainer, C., Santos, A., Ireland, L., Sakai, T., Sakai, K., Kim, Y.-S., et al. (2016) · Nature Cell Biology · doi:10.1038/ncb3340 · Cited by 441 · see citing works
Exosomes 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-citation
Small extracellular vesicles secreted from senescent cells promote cancer cell proliferation through EphA2
Takasugi, 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
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
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
Tumor restriction by type I collagen opposes tumor-promoting effects of cancer-associated fibroblasts
Bhattacharjee, S., Hamberger, F., Ravichandra, A., Miller, M., Nair, A., Affo, S., Filliol, A., Chin, L., Savage, T. M., Yin, D., et al. (2021) · Journal of Clinical Investigation · doi:10.1172/jci146987 · Cited by 367 · see citing works
Self-citation
The molecular biology of pancreatic adenocarcinoma: Translational challenges and clinical perspectives
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
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
Ticket to a bubble ride: Cargo sorting into exosomes and extracellular vesicles
Anand, S., Samuel, M., Kumar, S., & Mathivanan, S. (2019) · Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics · doi:10.1016/j.bbapap.2019.02.005 · Cited by 284 · see citing works
Combining Machine Learning and Nanofluidic Technology To Diagnose Pancreatic Cancer Using Exosomes
Ko, J., Bhagwat, N., Yee, S. S., Ortiz, N., Sahmoud, A., Black, T., Aiello, N. M., McKenzie, L., O’Hara, M., Redlinger, C., et al. (2017) · ACS Nano · doi:10.1021/acsnano.7b05503 · Cited by 249 · see citing works
Self-citation
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
Cancer stem cell secretome in the tumor microenvironment: a key point for an effective personalized cancer treatment
López de Andrés, J., Griñán-Lisón, C., Jiménez, G., & Marchal, J. A. (2020) · Journal of Hematology & Oncology · doi:10.1186/s13045-020-00966-3 · Cited by 207 · see citing works
Employing mesenchymal stem cells to support tumor-targeted delivery of extracellular vesicle (EV)-encapsulated microRNA-379
O’Brien, K. P., Khan, S., Gilligan, K. E., Zafar, H., Lalor, P., Glynn, C., O’Flatharta, C., Ingoldsby, H., Dockery, P., De Bhulbh, A., et al. (2018) · Oncogene · doi:10.1038/s41388-017-0116-9 · Cited by 215 · see citing works
Disruption of Circulating Extracellular Vesicles as a Novel Therapeutic Strategy against Cancer Metastasis
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
Proteomic analysis of urinary extracellular vesicles reveal biomarkers for neurologic disease
Wang, S., Kojima, K., Mobley, J. A., & West, A. B. (2019) · EBioMedicine · doi:10.1016/j.ebiom.2019.06.021 · Cited by 145 · see citing works
Exosomal microRNAs derived from colorectal cancer-associated fibroblasts: role in driving cancer progression
Bhome, 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
Cyp4a in tumor-associated macrophages promotes pre-metastatic niche formation and metastasis
Chen, X. W., Yu, T. J., Zhang, J., Li, Y., Chen, H. L., Yang, G. F., Yu, W., Liu, Y. Z., Liu, X. X., Duan, C. F., et al. (2017) · Oncogene · doi:10.1038/onc.2017.118 · Cited by 143 · 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
The Emerging Roles of Extracellular Vesicles As Communication Vehicles within the Tumor Microenvironment and Beyond
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
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
Regulation and Function of Matrix Metalloproteinase-13 in Cancer Progression and Metastasis
Li, S., Pritchard, D. M., & Yu, L.-G. (2022) · Cancers · doi:10.3390/cancers14133263 · Cited by 82 · see citing works
Retinoic Acid Receptor‐β Is Downregulated in Hepatocellular Carcinoma and Cirrhosis and Its Expression Inhibits Myosin‐Driven Activation and Durotaxis in Hepatic Stellate Cells
Cortes, E., Lachowski, D., Rice, A., Chronopoulos, A., Robinson, B., Thorpe, S., Lee, D. A., Possamai, L. A., Wang, H., Pinato, D. J., et al. (2019) · Hepatology · doi:10.1002/hep.30193 · Cited by 64 · see citing works
Analysis of extracellular vesicles as emerging theranostic nanoplatforms
Xing, Y., Cheng, Z., Wang, R., Lv, C., James, T. D., & Yu, F. (2020) · Coordination Chemistry Reviews · doi:10.1016/j.ccr.2020.213506 · Cited by 67 · 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
Transgenerational paternal transmission of acquired traits: stress-induced modification of the sperm regulatory transcriptome and offspring phenotypes
Pang, T. Y., Short, A. K., Bredy, T. W., & Hannan, A. J. (2017) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2017.02.007 · Cited by 61 · see citing works
Recent advances in microfluidic methods in cancer liquid biopsy
Iliescu, F. S., Poenar, D. P., Yu, F., Ni, M., Chan, K. H., Cima, I., Taylor, H. K., Cima, I., & Iliescu, C. (2019) · Biomicrofluidics · doi:10.1063/1.5087690 · Cited by 51 · see citing works
Exosomes: a tool for bone tissue engineering
Huber, J., Griffin, M. F., Longaker, M. T., & Quarto, N. (2022) · Tissue Engineering Part B Reviews · doi:10.1089/ten.teb.2020.0246 · Cited by 41 · see citing works
NetrinG1(+) cancer-associated fibroblasts generate unique extracellular vesicles that support the survival of pancreatic cancer cells under nutritional stress
Raghavan, K. S., Francescone, R., Franco-Barraza, J., Gardiner, J. C., Vendramini-Costa, D. B., Luong, T., Pourmandi, N., Andren, A., Kurimchak, A., Ogier, C., et al. (2022) · Cancer Research Communications · doi:10.1158/2767-9764.crc-21-0147 · Cited by 40 · see citing works
Exploring the Role of Osteosarcoma-Derived Extracellular Vesicles in Pre-Metastatic Niche Formation and Metastasis in the 143-B Xenograft Mouse Osteosarcoma Model
Mazumdar, 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
Lung endothelium exploits susceptible tumor cell states to instruct metastatic latency
Jakab, M., Lee, K. H., Uvarovskii, A., Ovchinnikova, S., Kulkarni, S. R., Jakab, S., Rostalski, T., Spegg, C., Anders, S., & Augustin, H. G. (2024) · Nature Cancer · doi:10.1038/s43018-023-00716-7 · Cited by 39 · see citing works
3D microperfusion of mesoscale human microphysiological liver models improves functionality and recapitulates hepatic zonation
Wesseler, M. F., Taebnia, N., Harrison, S., Youhanna, S., Preiss, L. C., Kemas, A. M., Vegvari, A., Mokry, J., Sullivan, G. J., Lauschke, V. M., et al. (2023) · Acta Biomaterialia · doi:10.1016/j.actbio.2023.09.022 · Cited by 39 · see citing works
Implementing biological markers as a tool to guide clinical care of patients with pancreatic cancer
Iovanna, J. (2021) · Translational Oncology · doi:10.1016/j.tranon.2020.100965 · Cited by 18 · see citing works
Primary breast tumours but not lung metastases induce protective anti-tumour immune responses after Treg-depletion
Hughes, E., Lauder, S. N., Smart, K., Bloom, A., Scott, J., Jones, E., Somerville, M., Browne, M., Blainey, A., Godkin, A., et al. (2020) · Cancer Immunology, Immunotherapy · doi:10.1007/s00262-020-02603-x · Cited by 15 · see citing works
Drug repurposing of 6-AZA-UTP and itraconazole reveals novel B3GALT5 inhibitors for pancreatic cancer
Botcha, L., Sehar, M., Cheng, Y.-C., Zhang, S.-C., Khan Jadoon, M. S., & Chuang, P.-K. (2025) · Bioorganic Chemistry · doi:10.1016/j.bioorg.2025.108464 · Cited by 1 · see citing works

P106 Active macrophage migration inhibitory factor (MIF) is a previously unrecognized isoform of MIF and a potential new biomarker for inflammatory bowel diseases
Völkel, D., Thiele, M., Douillard, P., et al. (2013) · Journal of Crohn s and Colitis · doi:10.1016/s1873-9946(13)60128-2
Announcing Exosomes and Microvesicles, the Official Journal of the American Society for Exosomes and Microvesicles
Gould, S. J., Taylor, D., Chiesi, A., et al. (2013) · Journal of Circulating Biomarkers · doi:10.33393/jcb.2013.2034 · Cited by 1 · see citing works
Exosomes and communication between tumours and the immune system: are all exosomes equal?
Bobrie, A., & Théry, C. (2013) · Biochemical Society Transactions · doi:10.1042/bst20120245 · Cited by 122 · see citing works
Serum macrophage migration inhibitory factor (MIF) in the intercritical phase of hereditary periodic fevers and its relationship with theMIF‐173G/C polymorphism
Rigante, D., Flex, A., Federico, G., et al. (2007) · Scandinavian Journal of Rheumatology · doi:10.1080/03009740701218816 · Cited by 6 · see citing works
Microvesicles and Exosomes in Cancer
Harrison, P., Gardiner, C., & Sargent, I. L. (2014) · doi:10.1201/b15647-15

Authors: 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., Xiang, J., Zhang, T., Theilen, T.-M., García-Santos, G., Williams, C., Ararso, Y., Huang, Y., Rodrigues, G., Shen, T.-L., Labori, K. J., Lothe, I. M. B., Kure, E. H., Hernandez, J., Doussot, A., Ebbesen, S. H., Grandgenett, P. M., Hollingsworth, M. A., Jain, M., Mallya, K., Batra, S. K., Jarnagin, W. R., Schwartz, R. E., Matei, I., Peinado, H., Stanger, B. Z., Bromberg, J., & Lyden, D.
Affiliations: University of Pennsylvania (US)
NewYork–Presbyterian Hospital (US)
Children's Cancer and Blood Foundation (US)
Medizinische Hochschule Hannover (DE)
Rockefeller University (US)
Weill Cornell Medicine (US)
Universidade do Porto (PT)
National Taiwan University (TW)
Oslo University Hospital (NO)
Memorial Sloan Kettering Cancer Center (US)
University of Nebraska Medical Center (US)
Spanish National Cancer Research Centre (ES)
Corresponding author: Stanger, Ben Z.
Bromberg, Jacqueline
Lyden, David
ORCID: Aiello, Nicole M.
Ocean, Allyson J.
Singh, Swarnima
Zhang, Haiying
Becker, Annette
Hoshino, Ayuko
Molina, Henrik
Xiang, Jenny
Zhang, Tuo
Theilen, Till-Martin
Huang, Yujie
Rodrigues, Gonçalo
Shen, Tang-Long
Labori, Knut Jørgen
Lothe, Inger Marie Bowitz
Kure, Elin H.
Doussot, Alexandre
Grandgenett, Paul M.
Hollingsworth, Michael A.
Jain, Maneesh
Mallya, Kavita
Batra, Surinder K.
Jarnagin, William R.
Schwartz, Robert E.
Matei, Irina
Peinado, Héctor
Stanger, Ben Z.
Bromberg, Jacqueline
Lyden, David
Venue: Nature Cell Biology
Publisher: Springer Science and Business Media LLC
Published: 2015-05-18
Volume: 17
Issue: 6
Pages: 816-826
ISSN: 1465-7392 (ISSN-L)
1476-4679
DOI: 10.1038/ncb3169
PMC: PMC5769922
OpenAlex: W1601681275
Cited by: 2,692
References: 70
Citations by year: 2026: 154 · 2025: 191 · 2024: 226 · 2023: 282 · 2022: 286 · 2021: 317 · 2020: 287 · 2019: 264 · 2018: 273 · 2017: 208 · 2016: 166 · 2015: 34 · 2014: 1
FWCI: 98.52
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
Locations: Nature Cell Biology (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: Hospital for Special Surgery
National Cancer Institute (U54CA163120, P50CA127297, U01CA111294, P30CA008748, R50CA211462)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Extracellular vesicles in disease
Health Sciences › Medicine › Oncology › Pancreatic and Hepatic Oncology Research
Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
Keywords: pancreatic ductal adenocarcinoma, exosomes, pre-metastatic niche, liver metastasis, Kupffer cells, TGF-beta, hepatic stellate cells, fibronectin, macrophage recruitment, macrophage migration inhibitory factor, tumor microenvironment, prognostic factors, intercellular communication
MeSH terms: Animals, Base Sequence, Bone Marrow Cells, Cell Movement, Female, Fibronectins, Humans, Liver, Liver Neoplasms, Macrophage Migration-Inhibitory Factors, Macrophages, Mice, Inbred C57BL, Pancreatic Neoplasms, Precancerous Conditions, Signal Transduction, Gene Expression Regulation, Neoplastic, Transforming Growth Factor beta, Sequence Analysis, RNA, Mice, Knockout, Carcinoma, Pancreatic Ductal, RNA Interference, RNA, Small Interfering, Cell Line, Tumor, Mice, Hepatic Stellate Cells, Exosomes

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Pancreatic cancer exosomes initiate pre-metastatic niche formation in the liver

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