Modeling metastasis biology and therapy in real time in the mouse lung
Open accessAbstract
Pulmonary metastasis remains the leading ca use of death for cancer patients. Opportunities to improve treatment outcomes for patients require new methods to study and view the biology of metastatic progression. Here, we describe an ex vivo pulmonary metastasis assay (PuMA) in which the metastatic progression of GFP-expressing cancer cells, from a single cell to the formation of multicellular colonies, in the mouse lung microenvironment was assessed in real time for up to 21 days. The biological validity of this assay was confirmed by its prediction of the in vivo behavior of a variety of high- and low-metastatic human and mouse cancer cell lines and the discrimination of tumor microenvironments in the lung that were most permissive to metastasis. Using this approach, we provide what we believe to be new insights into the importance of tumor cell interactions with the stromal components of the lung microenvironment. Finally, the translational utility of this assay was demonstrated through its use in the evaluation of therapeutics at discrete time points during metastatic progression. We believe that this assay system is uniquely capable of advancing our understanding of both metastasis biology and therapeutic strategies.
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Ex vivo culture methods permit investigation of tumour cells that grow within an intact lung environment.
“Ex vivo culture systems are useful to study tumour cells growing within an intact lung environment 214,215 .”
From Osteosarcoma (2022) · cites this paper as [214]
Cites
Hsu, S. M., Raine, L., & Fanger, H. (1981) · Journal of Histochemistry & Cytochemistry · doi:10.1177/29.4.6166661 · Cited by 14,248 · see citing works
Aslakson, C. J., & Miller, F. R. (1992) · PubMed · Cited by 1,234 · see citing works
Metastasis: recent discoveries and novel treatment strategies
Eccles, S. A., & Welch, D. R. (2007) · The Lancet · doi:10.1016/s0140-6736(07)60781-8 · Cited by 721 · see citing works
The membrane-cytoskeleton linker ezrin is necessary for osteosarcoma metastasis
Khanna, C., Wan, X., Bose, S., Cassaday, R., Olomu, O., Mendoza, A., Yeung, C., Gorlick, R., Hewitt, S. M., & Helman, L. J. (2004) · Nature Medicine · doi:10.1038/nm982 · Cited by 705 · see citing works
Self-citationAl‐Mehdi, A., Tozawa, K., Fisher, A. B., Shientag, L., Lee, A., & Muschel, R. J. (2000) · Nature Medicine · doi:10.1038/71429 · Cited by 703 · see citing works
Inhibition of Metastatic Outgrowth from Single Dormant Tumor Cells by Targeting the Cytoskeleton
Barkan, D., Kleinman, H. K., Simmons, J. L., Asmussen, H., Kamaraju, A. K., Hoenorhoff, M. J., Liu, Z.-Y., Costes, S. V., Cho, E. H., Lockett, S., et al. (2008) · Cancer Research · doi:10.1158/0008-5472.can-07-6849 · Cited by 426 · see citing works
Self-citationCameron, M. D., Schmidt, E. E., Kerkvliet, N. I., Nadkarni, K. V., Morris, V. L., Groom, A. C., Chambers, A. F., & MacDonald, I. C. (2000) · PubMed · Cited by 400 · see citing works
Metastasis-associated differences in gene expression in a murine model of osteosarcoma.
Khanna, C., Khan, J. I., Nguyen, P., Prehn, J., Caylor, J., Yeung, C. L., Trepel, J. B., Meltzer, P. S., & Helman, L. J. (2001) · PubMed · Cited by 282 · see citing works
Self-citationSteps in tumor metastasis: new concepts from intravital videomicroscopy
Chambers, A. F., MacDonald, I. C., Schmidt, E. E., Koop, S., Morris, V. L., Khokha, R., & Groom, A. C. (1995) · Cancer and Metastasis Reviews · doi:10.1007/bf00690599 · Cited by 265 · see citing works
Demonstration of all connective tissue elements in a single section; pentachrome stains.
Hz, M. (1955) · PubMed · Cited by 265 · see citing works
Cifone, M. A., & Fidler, I. J. (1980) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.77.2.1039 · Cited by 243 · see citing works
Influence of sun exposures during childhood and during adulthood on melanoma risk
Autier, P., & Doré, J. (1998) · International Journal of Cancer · doi:10.1002/(sici)1097-0215(19980812)77:4 · Cited by 235 · see citing works
Self-citationRapamycin Inhibits Ezrin-Mediated Metastatic Behavior in a Murine Model of Osteosarcoma
Wan, X., Mendoza, A., Khanna, C., & Helman, L. J. (2005) · Cancer Research · doi:10.1158/0008-5472.can-04-3135 · Cited by 215 · see citing works
Self-citationKhanna, C., Prehn, J., Yeung, C., Caylor, J., Tsokos, M., & Helman, L. (2000) · Clinical & Experimental Metastasis · doi:10.1023/a:1006767007547 · Cited by 207 · see citing works
Self-citationBorowsky, A. D., Namba, R., Young, L. J. T., Hunter, K. W., Hodgson, J., Tepper, C. G., McGoldrick, E. T., Muller, W. J., Cardiff, R. D., & Gregg, J. P. (2005) · Clinical & Experimental Metastasis · doi:10.1007/s10585-005-2908-5 · Cited by 195 · see citing works
Self-citationTechnical considerations for studying cancer metastasis in vivo
Welch, D. R. (1997) · Clinical & Experimental Metastasis · doi:10.1023/a:1018477516367 · Cited by 192 · see citing works
ARF functions as a melanoma tumor suppressor by inducing p53-independent senescence
Ha, L., Ichikawa, T., Anver, M. R., Dickins, R. A., Lowe, S. W., Sharpless, N. E., Krimpenfort, P., DePinho, R. A., Bennett, D. C., Sviderskaya, E. V., et al. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0611638104 · Cited by 144 · see citing works
Self-citationAdvances in optical imaging and novel model systems for cancer metastasis research
Henriquez, N. V., van Overveld, P. G. M., Que, I., Buijs, J. T., Bachelier, R., Kaijzel, E. L., Löwik, C. W. G. M., Clézardin, P., & van der Pluijm, G. (2007) · Clinical & Experimental Metastasis · doi:10.1007/s10585-007-9115-5 · Cited by 60 · see citing works
Characterization of human cells transformed in vitro by n‐methyl‐n'‐nitro‐n‐nitrosoguanidine
Rhim, J. S., Putman, D. L., Arnstein, P., Huebner, R. J., & McAllister, R. M. (1977) · International Journal of Cancer · doi:10.1002/ijc.2910190411 · Cited by 46 · see citing works
Long-term maintenance of mature pulmonary parenchyma cultured in serum-free conditions
Siminski, J., Kavanagh, T. J., Chi, E. Y., & Raghu, G. (1992) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.1992.262.1.l105 · Cited by 35 · see citing works
The Molecular Biology of Pulmonary Metastasis
Krishnan, K., Khanna, C., & Helman, L. J. (2006) · Thoracic surgery clinics/Thorac. surg. clin. · doi:10.1016/j.thorsurg.2005.12.003 · Cited by 33 · see citing works
Self-citationNovel targets with potential therapeutic applications in osteosarcoma
Khanna, C. (2008) · Current Oncology Reports · doi:10.1007/s11912-008-0054-3 · Cited by 29 · see citing works
Self-citationPreclinical studies of treosulfan demonstrate potent activity in Ewing’s sarcoma
Werner, S., Mendoza, A., Hilger, R. A., Erlacher, M., Reichardt, W., Lissat, A., Konanz, C., Uhl, M., Niemeyer, C. M., Khanna, C., et al. (2007) · Cancer Chemotherapy and Pharmacology · doi:10.1007/s00280-007-0566-9 · Cited by 27 · see citing works
Self-citationThree-dimensional type I collagen cell culture systems for the study of bone pathophysiology.
Themistocleous, G. S., Katopodis, H., Sourla, A., Lembessis, P., Doillon, C. J., Soucacos, P. N., & Koutsilieris, M. (2004) · PubMed · Cited by 25 · see citing works
Breast cancer metastasis progression as revealed by intravital videomicroscopy
MacDonald, I. C., & Chambers, A. F. (2006) · Expert Review of Anticancer Therapy · doi:10.1586/14737140.6.9.1271 · Cited by 12 · see citing works
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Tsai, J. H., & Yang, J. (2013) · Genes & Development · doi:10.1101/gad.225334.113 · Cited by 1,132 · see citing works
Tsai, J. H., Donaher, J. L., Murphy, D. A., Chau, S., & Yang, J. (2012) · Cancer Cell · doi:10.1016/j.ccr.2012.09.022 · Cited by 1,073 · see citing works
Preclinical Mouse Cancer Models: A Maze of Opportunities and Challenges
Day, C.-P., Merlino, G., & Van Dyke, T. (2015) · Cell · doi:10.1016/j.cell.2015.08.068 · Cited by 676 · see citing works
Self-citationBeird, H. C., Bielack, S. S., Flanagan, A. M., Gill, J., Heymann, D., Janeway, K. A., Livingston, J. A., Roberts, R. D., Strauss, S. J., & Gorlick, R. (2022) · Nature Reviews Disease Primers · doi:10.1038/s41572-022-00409-y · Cited by 660 · see citing works
Visualization of immediate immune responses to pioneer metastatic cells in the lung
Headley, M. B., Bins, A. D., Nip, A., Roberts, E. W., Looney, M. R., Gérard, A., & Krummel, M. F. (2016) · Nature · doi:10.1038/nature16985 · Cited by 442 · see citing works
Small molecule inhibitors of ezrin inhibit the invasive phenotype of osteosarcoma cells
Bulut, G., Hong, S.-H., Chen, K., Beauchamp, E. M., Rahim, S., Kosturko, G. W., Glasgow, E., Dakshanamurthy, S., Lee, H.-S., Daar, I., et al. (2012) · Oncogene · doi:10.1038/onc.2011.245 · Cited by 179 · see citing works
Self-citationToward a Drug Development Path That Targets Metastatic Progression in Osteosarcoma
Khanna, C., Fan, T. M., Gorlick, R., Helman, L. J., Kleinerman, E. S., Adamson, P. C., Houghton, P. J., Tap, W. D., Welch, D. R., Steeg, P. S., et al. (2014) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-13-2574 · Cited by 178 · see citing works
Self-citationPositively selected enhancer elements endow osteosarcoma cells with metastatic competence
Morrow, J. J., Bayles, I., Funnell, A. P. W., Miller, T. E., Saiakhova, A., Lizardo, M. M., Bartels, C. F., Kapteijn, M. Y., Hung, S., Mendoza, A., et al. (2018) · Nature Medicine · doi:10.1038/nm.4475 · Cited by 161 · see citing works
Self-citationTGF-β Signaling in Myeloid Cells Is Required for Tumor Metastasis
Pang, Y., Gara, S. K., Achyut, B. R., Li, Z., Yan, H. H., Day, C., Weiss, J. M., Trinchieri, G., Morris, J. C., & Li, Y. (2013) · Cancer Discovery · doi:10.1158/2159-8290.cd-12-0527 · Cited by 155 · see citing works
Guha, M., Srinivasan, S., Ruthel, G. T., Kashina, A., Carstens, R. P., Mendoza, A., Khanna, C., Winkle, T. V., & Avadhani, N. G. (2013) · Oncogene · doi:10.1038/onc.2013.467 · Cited by 154 · see citing works
Self-citationCombined SFK/MEK inhibition prevents metastatic outgrowth of dormant tumor cells
Touny, L. H. E., Vieira, A., Mendoza, A., Khanna, C., Hoenerhoff, M. J., & Green, J. E. (2013) · Journal of Clinical Investigation · doi:10.1172/jci70259 · Cited by 144 · see citing works
Self-citationHurst, D. R., & Welch, D. R. (2011) · International review of cytology · doi:10.1016/b978-0-12-385859-7.00003-3 · Cited by 136 · see citing works
Neri, S., Ishii, G., Hashimoto, H., Kuwata, T., Nagai, K., Date, H., & Ochiai, A. (2015) · International Journal of Cancer · doi:10.1002/ijc.29464 · Cited by 132 · see citing works
Roberts, R. D., Lizardo, M. M., Reed, D. R., Hingorani, P., Glover, J., Allen‐Rhoades, W., Fan, T., Khanna, C., Sweet‐Cordero, E. A., Cash, T., et al. (2019) · Cancer · doi:10.1002/cncr.32351 · Cited by 127 · see citing works
Self-citationCharacterization of the metastatic phenotype of a panel of established osteosarcoma cells
Ren, L., Mendoza, A., Zhu, J., Briggs, J., Halsey, C., Hong, E. S., Burkett, S. S., Morrow, J. J., Lizardo, M. M., Osborne, T. S., et al. (2015) · Oncotarget · doi:10.18632/oncotarget.5177 · Cited by 119 · see citing works
Self-citationTegavivint and the β-Catenin/ALDH Axis in Chemotherapy-Resistant and Metastatic Osteosarcoma
Nomura, M., Rainusso, N., Lee, Y.-C., Dawson, B., Coarfa, C., Han, R., Larson, J. L., Shuck, R., Kurenbekova, L., & Yustein, J. T. (2019) · JNCI: Journal of the National Cancer Institute · doi:10.1093/jnci/djz026 · Cited by 99 · see citing works
Blocking Surgically Induced Lysyl Oxidase Activity Reduces the Risk of Lung Metastases
Rachman-Tzemah, C., Zaffryar‐Eilot, S., Grossman, M., Ribero, D., Timaner, M., Mäki, J. M., Myllyharju, J., Bertolini, F., Hershkovitz, D., Sagi, I., et al. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.04.005 · Cited by 96 · see citing works
Fan, T. M., Roberts, R. D., & Lizardo, M. M. (2020) · Frontiers in Oncology · doi:10.3389/fonc.2020.00013 · Cited by 90 · see citing works
Twenty Years on: What Do We Really Know about Ewing Sarcoma and What Is the Path Forward?
Lawlor, E. R., & Sorensen, P. H. B. (2015) · Critical Reviews™ in Oncogenesis · doi:10.1615/critrevoncog.2015013553 · Cited by 87 · see citing works
Yan, H. H., Jiang, J. D., Pang, Y., Achyut, B. R., Lizardo, M. M., Liang, X., Hunter, K. W., Khanna, C., Hollander, C. M., & Li, Y. (2015) · Cancer Research · doi:10.1158/0008-5472.can-15-2282-t · Cited by 81 · see citing works
Self-citationDuquet, A., Melotti, A., Mishra, S., Malerba, M., Seth, C., Conod, A., & Altaba, A. R. I. (2014) · EMBO Molecular Medicine · doi:10.15252/emmm.201303799 · Cited by 77 · see citing works
T Cells Promote Metastasis by Regulating Extracellular Matrix Remodeling following Chemotherapy
Haj-Shomaly, J., Vorontsova, A., Barenholz‐Cohen, T., Levi-Galibov, O., Devarasetty, M., Timaner, M., Raviv, Z., Cooper, T. J., Söker, S., Hasson, P., et al. (2021) · Cancer Research · doi:10.1158/0008-5472.can-21-1012 · Cited by 72 · see citing works
LZTFL1 suppresses lung tumorigenesis by maintaining differentiation of lung epithelial cells
Wei, Q., Chen, Z.-H., Wang, L., Zhang, T., Duan, L., Behrens, C., Wistuba, I. I., Minna, J. D., Gao, B., Luo, J.-H., et al. (2015) · Oncogene · doi:10.1038/onc.2015.328 · Cited by 62 · see citing works
Garg, M. (2017) · Expert Reviews in Molecular Medicine · doi:10.1017/erm.2017.6 · Cited by 60 · see citing works
Alsarraj, J., Faraji, F., Geiger, T. R., Mattaini, K. R., Williams, M. F., Wu, J. J., Ha, N., Merlino, T., Walker, R. C., Bosley, A. D., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0080746 · Cited by 58 · see citing works
Self-citationRen, L., Hong, S.-H., Chen, Q.-R., Briggs, J., Cassavaugh, J., Srinivasan, S., Lizardo, M. M., Mendoza, A., Xia, A. Y., Avadhani, N., et al. (2012) · Cancer Research · doi:10.1158/0008-5472.can-11-0210 · Cited by 50 · see citing works
Self-citationLizardo, M. M., Morrow, J. J., Miller, T. E., Hong, E. S., Ren, L., Mendoza, A., Halsey, C. H., Scacheri, P. C., Helman, L. J., & Khanna, C. (2016) · Neoplasia · doi:10.1016/j.neo.2016.09.001 · Cited by 50 · see citing works
Self-citationMetabolomics uncovers a link between inositol metabolism and osteosarcoma metastasis
Ren, L., Hong, E. S., Mendoza, A., Issaq, S. H., Hoang, C. T., Lizardo, M. M., LeBlanc, A. K., & Khanna, C. (2017) · Oncotarget · doi:10.18632/oncotarget.15872 · Cited by 46 · see citing works
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Bayles, I., Krajewska, M., Pontius, W. D., Saiakhova, A., Morrow, J. J., Bartels, C., Lu, J., Faber, Z. J., Fedorov, Y., Hong, E. S., et al. (2019) · Journal of Clinical Investigation · doi:10.1172/jci127718 · Cited by 46 · see citing works
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Barkan, D., & Green, J. E. (2011) · Journal of Visualized Experiments · doi:10.3791/2914 · Cited by 39 · see citing works
Self-citationPIK3CAH1047R Accelerates and Enhances KRASG12D-Driven Lung Tumorigenesis
Green, S., Trejo, C. L., & McMahon, M. (2015) · Cancer Research · doi:10.1158/0008-5472.can-15-1249 · Cited by 38 · see citing works
The First European Interdisciplinary Ewing Sarcoma Research Summit
Kovar, H., Alonso, J., Åman, P., Aryee, D. N. T., Ban, J., Burchill, S. A., Burdach, S. E. G., de Álava, E., Delattre, O., Dirksen, U., et al. (2012) · Frontiers in Oncology · doi:10.3389/fonc.2012.00054 · Cited by 38 · see citing works
Ezrin Binds to DEAD-Box RNA Helicase DDX3 and Regulates Its Function and Protein Level
Çelik, H., Sajwan, K. P., Selvanathan, S. P., Marsh, B. J., Pai, A. V., Saygıdeğer, Y., Han, J. J., Minas, T. Z., Rahim, S., Erkizan, H. V., et al. (2015) · Molecular and Cellular Biology · doi:10.1128/mcb.00332-15 · Cited by 38 · see citing works
Lü, M., Huang, X. P., Cai, X., Sun, J., Liu, X., Weng, L., Zhu, L., Luo, Q., & Chen, Z. (2022) · ACS Applied Materials & Interfaces · doi:10.1021/acsami.1c23737 · Cited by 36 · see citing works
KISS1 in metastatic cancer research and treatment: potential and paradoxes
Ly, T., Harihar, S., & Welch, D. R. (2020) · Cancer and Metastasis Reviews · doi:10.1007/s10555-020-09868-9 · Cited by 35 · see citing works
Targeting dormant micrometastases: rationale, evidence to date and clinical implications
Hurst, R. E., Bastian, A., Bailey‐Downs, L. C., & Ihnat, M. A. (2016) · Therapeutic Advances in Medical Oncology · doi:10.1177/1758834015624277 · Cited by 29 · see citing works
Schott, C. R., Shah, A. T., & Sweet-Cordero, A. (2020) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-43085-6_1 · Cited by 30 · see citing works
Disruption of STAT5A and NMI signaling axis leads to ISG20-driven metastatic mammary tumors
Alsheikh, H. A., Metge, B. J., Pruitt, H. C., Kammerud, S. C., Chen, D., Wei, S., Shevde, L. A., & Samant, R. S. (2021) · Oncogenesis · doi:10.1038/s41389-021-00333-y · Cited by 30 · see citing works
Reddy, G. B., Kerr, D. L., Spasojević, I., Tovmasyan, A. G., Hsu, D. S., Brigman, B. E., Somarelli, J. A., Needham, D., & Eward, W. C. (2020) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-19-0689 · Cited by 28 · see citing works
Apoptosis Resistance and PKC Signaling: Distinguishing Features of High and Low Metastatic Cells
Hong, S.-H., Ren, L., Mendoza, A., Eleswarapu, A. S., & Khanna, C. (2012) · Neoplasia · doi:10.1593/neo.111498 · Cited by 28 · see citing works
Self-citationMorrow, J. J., Mendoza, A., Koyen, A., Lizardo, M. M., Ren, L., Waybright, T. J., Hansen, R. J., Gustafson, D. L., Zhou, M., Fan, T. M., et al. (2016) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-16-0326 · Cited by 27 · see citing works
Self-citationIntravital microscopy in the mouse dorsal chamber model for the study of solid tumors.
Baron, V. T., Welsh, J., Abedinpour, P., & Borgström, P. (2011) · PubMed Central · Cited by 24 · see citing works
Silver, K. I., Patkar, S., Mazcko, C. N., Berger, E. P., Beck, J. A., & LeBlanc, A. K. (2023) · Veterinary and Comparative Oncology · doi:10.1111/vco.12927 · Cited by 22 · see citing works
The spatiotemporal cellular dynamics of lung immunity
Lelkes, E., Headley, M. B., Thornton, E. E., Looney, M. R., & Krummel, M. F. (2014) · Trends in Immunology · doi:10.1016/j.it.2014.05.005 · Cited by 20 · see citing works
Evans, C. E., Palazón, A., Sim, J., Tyrakis, P. A., Prodger, A., Xiao, L., Chan, S., Bendahl, P., Belting, M., Euler, L. V., et al. (2017) · Biology Open · doi:10.1242/bio.024653 · Cited by 20 · see citing works
Çelik, H., Hong, S.-H., Colón-López, D. D., Han, J. J., Saygıdeğer, Y., Minas, T. Z., Swift, M. R., Paige, M. A., Glasgow, E. F., Toretsky, J. A., et al. (2015) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-15-0511 · Cited by 20 · see citing works
Self-citationLizardo, M. M., & Sorensen, P. H. (2018) · Journal of Visualized Experiments · doi:10.3791/56332 · Cited by 19 · see citing works
Novel role of the dietary flavonoid fisetin in suppressing rRNA biogenesis
Kammerud, S. C., Metge, B. J., Elhamamsy, A. R., Weeks, S. E., Alsheikh, H. A., Mattheyses, A. L., Shevde, L. A., & Samant, R. S. (2021) · Laboratory Investigation · doi:10.1038/s41374-021-00642-1 · Cited by 18 · see citing works
Yu, P. Y., Gardner, H. L., Roberts, R., Cam, H., Hariharan, S., Ren, L., LeBlanc, A. K., Xiao, H., Lin, J., Guttridge, D. C., et al. (2017) · PLOS ONE · doi:10.1371/journal.pone.0181885 · Cited by 17 · see citing works
Self-citationPharmacologic Inhibition of EIF4A Blocks NRF2 Synthesis to Prevent Osteosarcoma Metastasis
Lizardo, M. M., Hughes, C. S., Huang, Y. Z., Shyp, T., Delaidelli, A., Zhang, H., Shaool, S. S., Renner, A. F., Burwag, F., Sayles, L. C., et al. (2024) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-24-1317 · Cited by 18 · see citing works
Live imaging of the pulmonary immune environment
Looney, M. R., & Headley, M. B. (2018) · Cellular Immunology · doi:10.1016/j.cellimm.2018.09.007 · Cited by 16 · see citing works
Pontius, W., Hong, E. S., Faber, Z. J., Gray, J., Peacock, C. D., Bayles, I., Lovrenert, K., Chin, D. H., Gryder, B. E., Bartels, C. F., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-42656-x · Cited by 14 · see citing works
Kravtsova‐Ivantsiv, Y., Goldhirsh, G., & Ciechanover, A. J. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2416909121 · Cited by 15 · see citing works
Fleten, K. G., Flørenes, V. A., Prasmickaite, L., Hill, O., Sykora, J., Mælandsmo, G. M., & Engesæter, B. (2016) · Cell Death Discovery · doi:10.1038/cddiscovery.2016.81 · Cited by 14 · see citing works
Kaurenoic acid nanocarriers regulates cytokine production and inhibit breast cancer cell migration
Ferreira, K. C. B., Valle, A. B. C. D. S., Gualberto, A. C. M., Aleixo, D. T., Silva, L. M., Santos, M. M., Costa, D. D. S., Oliveira, L. L., Gameiro, J., Tavares, G. D., et al. (2022) · Journal of Controlled Release · doi:10.1016/j.jconrel.2022.10.048 · Cited by 14 · see citing works
Ren, L., Huang, S., Beck, J. A., & LeBlanc, A. K. (2021) · Scientific Reports · doi:10.1038/s41598-021-04018-9 · Cited by 13 · see citing works
Self-citationMetge, B. J., Alsheikh, H. A., Kammerud, S. C., Chen, D., Das, D., Nebane, N. M., Bostwick, J. R., Shevde, L. A., & Samant, R. S. (2024) · Cell Death and Disease · doi:10.1038/s41419-024-06694-7 · Cited by 13 · see citing works
Photopharmacological modulation of native CRAC channels using azoboronate photoswitches
Udasin, R. G., Sil, A., Zomot, E., Cohen, H. A., Haj-Shomaly, J., Engelmayer, N., Lev, S., Binshtok, A. M., Shaked, Y., Kienzler, M. A., et al. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2118160119 · Cited by 13 · see citing works
Metge, B. J., Alsheikh, H. A., Chen, D., Elhamamsy, A. R., Hinshaw, D. C., Chen, B.-R., Sleckman, B. P., Samant, R. S., & Shevde, L. A. (2023) · npj Precision Oncology · doi:10.1038/s41698-023-00410-y · Cited by 13 · see citing works
Szmulewitz, R. Z., Clark, R., Lotan, T. L., Otto, K. B., Veneris, J. T., Macleod, K. F., & Rinker-Schaeffer, C. W. (2011) · International Journal of Cancer · doi:10.1002/ijc.26005 · Cited by 13 · see citing works
Systemic Influences of Mammary Cancer on Monocytes in Mice
Robinson, A., Burgess, M. O., Webb, S., Louwe, P. A., Ouyang, Z., Skola, D., Han, C. Z., Batada, N. N., González‐Huici, V., Cassetta, L., et al. (2022) · Cancers · doi:10.3390/cancers14030833 · Cited by 12 · see citing works
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Nuckhir, M., Withey, D., Cabral, S. C. M., Harrison, H., & Clarke, R. B. (2024) · Journal of Mammary Gland Biology and Neoplasia · doi:10.1007/s10911-024-09567-z · Cited by 12 · see citing works
Shechter, D., Harel, M., Mukherjee, A., Muñoz‐Sagredo, L., Loven, D., Prinz, E., Avraham, S., Orian‐Rousseau, V., Geiger, T., Shaked, Y., et al. (2020) · Cells · doi:10.3390/cells9102269 · Cited by 12 · see citing works
Lung-Derived Selectins Enhance Metastatic Behavior of Triple Negative Breast Cancer Cells
Khan, S. U., Xia, Y., Goodale, D. B., Schoettle, G., & Allan, A. L. (2021) · Biomedicines · doi:10.3390/biomedicines9111580 · Cited by 10 · see citing works
Knopeke, M. T., Ritschdorff, E. T., Clark, R., Griend, D. J. V., Khan, S., Thobe, M. N., Shear, J. B., & Rinker-Schaeffer, C. W. (2011) · FEBS Letters · doi:10.1016/j.febslet.2011.09.007 · Cited by 10 · see citing works
Young, E. D., Strom, K. B., Tsue, A. F., Usset, J. L., MacPherson, S., McGuire, J. T., & Welch, D. R. (2018) · Clinical & Experimental Metastasis · doi:10.1007/s10585-018-9882-1 · Cited by 9 · see citing works
Selective enhancer changes in osteosarcoma lung metastasis
Kovar, H. (2018) · Nature Medicine · doi:10.1038/nm.4487 · Cited by 8 · see citing works
Assessing a Novel 3D Assay System for Drug Screening against OS Metastasis
Koons, N., Amato, N., Sauer, S. J., Warshawsky, D., Barkan, D., & Khanna, C. (2021) · Pharmaceuticals · doi:10.3390/ph14100971 · Cited by 7 · see citing works
Self-citationEffects of spatial diffusion on nonequilibrium steady states in a model for prebiotic evolution
Intoy, B., Wynveen, A., & Halleý, J. W. (2016) · Physical review. E · doi:10.1103/physreve.94.042424 · Cited by 8 · see citing works
Targetable Intercellular Signaling Pathways Facilitate Lung Colonization in Osteosarcoma
Reinecke, J. B., & Roberts, R. D. (2020) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-43085-6_7 · Cited by 7 · see citing works
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Scopim‐Ribeiro, R., Lizardo, M. M., Zhang, H., Dhez, A.-C., Hughes, C. S., & Sorensen, P. H. B. (2021) · Frontiers in Oncology · doi:10.3389/fonc.2021.645757 · Cited by 6 · see citing works
Ex vivo Live Imaging of Lung Metastasis and Their Microenvironment
van den Bijgaart, R. J. E., Kong, N., Maynard, C., & Plaks, V. (2016) · Journal of Visualized Experiments · doi:10.3791/53741 · Cited by 6 · see citing works
Wang, J., Liu, H., & Zheng, K. (2017) · Journal of Cancer Research and Therapeutics · doi:10.4103/jcrt.jcrt_323_17 · Cited by 6 · see citing works
Lin, T.-C., Liao, Y., Chang, W., Yang, C.-H., Cheng, L.-H., Cheng, M., & Cheng, H.-C. (2018) · Journal of Visualized Experiments · doi:10.3791/56761 · Cited by 6 · see citing works
Preclinical models for the study of pediatric solid tumors: focus on bone sarcomas
Petrescu, D. I., Yustein, J. T., & Dasgupta, A. (2024) · Frontiers in Oncology · doi:10.3389/fonc.2024.1388484 · Cited by 5 · see citing works
Bhat, V., Piaseczny, M. M., Goodale, D. B., Patel, U., Sadri, A., & Allan, A. L. (2024) · Clinical & Experimental Metastasis · doi:10.1007/s10585-024-10284-4 · Cited by 5 · see citing works
Elhamamsy, A. R., Metge, B. J., Swain, C. A., Elbahoty, M. H., Hinshaw, D. C., Kammerud, S. C., Chen, D., Samant, R. S., & Shevde, L. A. (2025) · Nature Communications · doi:10.1038/s41467-025-63315-3 · Cited by 4 · see citing works
Advancing Preclinical Biology for Ewing Sarcoma: An International Effort
Cruz, F. S. D., Stewart, E. A., Surdez, D., Daley, J. D., Soragni, A., Tomazou, E. M., Alvarez-Perez, J., Feinberg, T. Y., Amatruda, J. F., Ganapathi, S. S., et al. (2025) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-25-0428 · Cited by 6 · see citing works
Yu, Y., Mendoza, A., & Merlino, G. T. (2023) · STAR Protocols · doi:10.1016/j.xpro.2023.102349 · Cited by 4 · see citing works
Self-citationA new semiquantitative method for evaluation of metastasis progression.
Volarevic, A., Ljujić, B., Volarević, V., Milovanović, M., Kanjevac, T., Lukić, A., & Arsenijević, N. (2012) · PubMed · Cited by 3 · see citing works
Takashima, Y., Murakami, T., Inoué, T., Hagiyama, M., Yoneshige, A., Nishimura, S., Akagi, M., & Ito, A. (2017) · Tumor Biology · doi:10.1177/1010428317704365 · Cited by 2 · see citing works
Gatz, S. A., SHIPLEY, J. M., Keller, C., & Linardic, C. M. (2020) · Pediatric oncology · doi:10.1007/978-3-030-51160-9_10 · Cited by 2 · see citing works
Breast Cancer Invasion and Metastasis
Stecklein, S. R., Elsarraj, H. S., Valdez, K. E., Paul, A., & Behbod, F. (2013) · Springer eBooks · doi:10.1007/978-94-007-7835-1_3 · Cited by 2 · see citing works
Li, Y., Gong, H., Chen, X., Su, J., Yang, Y., Luo, Y., Cheng, T., Pan, C., Li, H., Jiang, Z., et al. (2025) · International Immunopharmacology · doi:10.1016/j.intimp.2025.116032 · Cited by 1 · see citing works
Needham, D. (2020) · Elsevier eBooks · doi:10.1016/b978-0-08-102983-1.00022-3 · Cited by 1 · see citing works
Positively Selected Enhancer Elements Endow Tumor Cells with Metastatic CompetencePreprint
Morrow, J. J., Bayles, I., Funnell, A. P. W., Miller, T. E., Saiakhova, A., Lizardo, M. M., Bartels, C. F., Kapteijn, M. Y., Hung, S., Mendoza, A., et al. (2017) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/155416 · Cited by 1 · see citing works
Self-citationYoung, E. D. (2018) · KU ScholarWorks (University of Kansas)
Malek, A. V. (2013) · Springer eBooks · doi:10.1007/978-94-007-7835-1_6
Gaspar, N. (2020) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.736286746.793579340
Haj-Shomaly, J., Vorontsova, A., Barenholz‐Cohen, T., Levi-Galibov, O., Devarasetty, M., Timaner, M., Raviv, Z., Cooper, T. J., Söker, S., Hasson, P., et al. (2023) · doi:10.1158/0008-5472.22582427
Haj-Shomaly, J., Vorontsova, A., Barenholz‐Cohen, T., Levi-Galibov, O., Devarasetty, M., Timaner, M., Raviv, Z., Cooper, T. J., Söker, S., Hasson, P., et al. (2023) · doi:10.1158/0008-5472.22582427.v1
Mooney, B., Chu, X., Negri, G. L., Lizardo, M. M., Song, H., Marsh, A., Delaidelli, A., Huang, Y. Z., Rouleau, M., Spencer, S. E., et al. (2026) · Cell Reports · doi:10.1016/j.celrep.2026.117884
- Authors
- Mendoza, A., Hong, S.-H., Osborne, T., Khan, M. A., Campbell, K., Briggs, J., Eleswarapu, A., Buquo, L., Ren, L., Hewitt, S. M., Dakir, E.-H., Garfield, S., Walker, R., Merlino, G., Green, J. E., Hunter, K. W., Wakefield, L. M., & Khanna, C.
- Affiliations
- National Institutes of Health (US)
- Corresponding author
- Khanna, Chand
- ORCID
- Venue
- Journal of Clinical Investigation
- Published
- 2010-08-02
- Volume
- 120
- Issue
- 8
- Pages
- 2979-2988
- ISSN
- 0021-9738 (ISSN-L)
- PMC
- PMC2912183
- OpenAlex
- W1992891544
- Cited by
- 92
- References
- 25
- Citations by year
- 2026: 1 · 2025: 3 · 2024: 6 · 2023: 6 · 2022: 5 · 2021: 7 · 2020: 9 · 2019: 3 · 2018: 7 · 2017: 8 · 2016: 7 · 2015: 9 · 2014: 3 · 2013: 7 · 2012: 4
- FWCI
- 2.85
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Clinical Investigation (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Howard Hughes Medical Institute
- Topics
- Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mechanisms of cancer metastasis
- Health Sciences › Medicine › Immunology and Allergy › Cell Adhesion Molecules Research
- Keywords
- lung metastasis, metastatic progression, lung microenvironment, tumor stroma, metastatic cell lines, real-time imaging, tumor spheroids
- MeSH terms
- Animals, Disease Models, Animal, Female, Humans, Lung Neoplasms, Mice, Inbred Strains, Disease Progression, Cell Line, Tumor, Mice
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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.
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