Intratumoral Cancer Cell Intravasation Can Occur Independent of Invasion into the Adjacent Stroma

Cell Reports

Volumn 19, Issue 3, 2017, Pages 601-616

  Deryugina, Elena I ^a   Kiosses, William B ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

animal models of cancer; cancer metastasis; cell intravasation; chorioallantoic membrane model; EGFR; mouse ear tumor model; stromal invasion; tumor angiogenesis; tumor cell migration; tumor invasion

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; GREEN FLUORESCENT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL; CANCER CELL; CANCER CELL CULTURE; CANCER GROWTH; CANCER STAGING; CARCINOGENESIS; CELL FUNCTION; CELL INVASION; CHICKEN; CONFOCAL MICROSCOPY; CONTROLLED STUDY; EMBRYO; FIBROSARCOMA CELL LINE; HUMAN; HUMAN CELL; IMAGE ANALYSIS; INTRAVASATION; MELANOMA CELL LINE; METASTASIS POTENTIAL; MOUSE; NONHUMAN; QUANTITATIVE ANALYSIS; STROMA; TUMOR LOCALIZATION; TUMOR VASCULARIZATION; ANIMAL; C57BL MOUSE; CELL MOTION; CHICK EMBRYO; DISEASE MODEL; EAR; HYPOXIA; METABOLISM; METASTASIS; NEOPLASM; NEOVASCULARIZATION (PATHOLOGY); NONOBESE DIABETIC MOUSE; PATHOLOGY; PERMEABILITY; SCID MOUSE; STROMA CELL; TUMOR CELL LINE; TUMOR INVASION;

ANIMALS; CELL LINE, TUMOR; CELL MOVEMENT; CHICK EMBRYO; DISEASE MODELS, ANIMAL; EAR; GREEN FLUORESCENT PROTEINS; HUMANS; HYPOXIA; MICE, INBRED C57BL; MICE, INBRED NOD; MICE, SCID; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; PERMEABILITY; RECEPTOR, EPIDERMAL GROWTH FACTOR; STROMAL CELLS;

EID: 85017663855     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2017.03.064     Document Type: Article

References (41)

1. Arteaga, C.L., Engelman, J.A., ERBB receptors: From oncogene discovery to basic science to mechanism-based cancer therapeutics. Cancer Cell 25 (2014), 282–303.
2. Blouw, B., Patel, M., Iizuka, S., Abdullah, C., You, W.K., Huang, X., Li, J.L., Diaz, B., Stallcup, W.B., Courtneidge, S.A., The invadopodia scaffold protein Tks5 is required for the growth of human breast cancer cells in vitro and in vivo. PLoS ONE, 10, 2015, e0121003.
3. Bobek, V., Kolostova, K., Pinterova, D., Kacprzak, G., Adamiak, J., Kolodziej, J., Boubelik, M., Kubecova, M., Hoffman, R.M., A clinically relevant, syngeneic model of spontaneous, highly metastatic B16 mouse melanoma. Anticancer Res. 30 (2010), 4799–4803.
4. Chiang, S.P., Cabrera, R.M., Segall, J.E., Tumor cell intravasation. Am. J. Physiol. Cell Physiol. 311 (2016), C1–C14.
5. 18F-FDG PET/CT provides powerful prognostic stratification in the primary staging of large breast cancer when compared with conventional explorations. Eur. J. Nucl. Med. Mol. Imaging 41 (2014), 428–437.
6. Conn, E.M., Botkjaer, K.A., Kupriyanova, T.A., Andreasen, P.A., Deryugina, E.I., Quigley, J.P., Comparative analysis of metastasis variants derived from human prostate carcinoma cells: Roles in intravasation of VEGF-mediated angiogenesis and uPA-mediated invasion. Am. J. Pathol. 175 (2009), 1638–1652.
7. Coumans, F.A., Siesling, S., Terstappen, L.W., Detection of cancer before distant metastasis. BMC Cancer, 13, 2013, 283.
8. Deryugina, E.I., Chorioallantoic membrane microtumor model to study the mechanisms of tumor angiogenesis, vascular permeability, and tumor cell intravasation. Methods Mol. Biol. 1430 (2016), 283–298.
9. Deryugina, E.I., Quigley, J.P., Chick embryo chorioallantoic membrane model systems to study and visualize human tumor cell metastasis. Histochem. Cell Biol. 130 (2008), 1119–1130.
10. Deryugina, E.I., Quigley, J.P., Tumor angiogenesis: MMP-mediated induction of intravasation- and metastasis-sustaining neovasculature. Matrix Biol. 44-46 (2015), 94–112.
11. Deryugina, E.I., Zijlstra, A., Partridge, J.J., Kupriyanova, T.A., Madsen, M.A., Papagiannakopoulos, T., Quigley, J.P., Unexpected effect of matrix metalloproteinase down-regulation on vascular intravasation and metastasis of human fibrosarcoma cells selected in vivo for high rates of dissemination. Cancer Res. 65 (2005), 10959–10969.
12. Deryugina, E.I., Zajac, E., Juncker-Jensen, A., Kupriyanova, T.A., Welter, L., Quigley, J.P., Tissue-infiltrating neutrophils constitute the major in vivo source of angiogenesis-inducing MMP-9 in the tumor microenvironment. Neoplasia 16 (2014), 771–788.
13. Egeblad, M., Nakasone, E.S., Werb, Z., Tumors as organs: Complex tissues that interface with the entire organism. Dev. Cell 18 (2010), 884–901.
14. Fibla, J.J., Cassivi, S.D., Decker, P.A., Allen, M.S., Darling, G.E., Landreneau, R.J., McKenna, R.J., Putnam, J.B., ACOSOG Z0030 Study Group. Validation of the lung cancer staging system revisions using a large prospective clinical trial database (ACOSOG Z0030). Eur. J. Cardiothorac. Surg. 43 (2013), 911–914.
15. Folkman, J., Role of angiogenesis in tumor growth and metastasis. Semin. Oncol. 29:6, Suppl 16 (2002), 15–18.
16. Giampieri, S., Manning, C., Hooper, S., Jones, L., Hill, C.S., Sahai, E., Localized and reversible TGFbeta signalling switches breast cancer cells from cohesive to single cell motility. Nat. Cell Biol. 11 (2009), 1287–1296.
17. Gligorijevic, B., Wyckoff, J., Yamaguchi, H., Wang, Y., Roussos, E.T., Condeelis, J., N-WASP-mediated invadopodium formation is involved in intravasation and lung metastasis of mammary tumors. J. Cell Sci. 125 (2012), 724–734.
18. Hanahan, D., Weinberg, R.A., Hallmarks of cancer: The next generation. Cell 144 (2011), 646–674.
19. Harney, A.S., Arwert, E.N., Entenberg, D., Wang, Y., Guo, P., Qian, B.Z., Oktay, M.H., Pollard, J.W., Jones, J.G., Condeelis, J.S., Real-time imaging reveals local, transient vascular permeability, and tumor cell intravasation stimulated by TIE2hi macrophage-derived VEGFA. Cancer Discov. 5 (2015), 932–943.
20. Hölzel, D., Eckel, R., Emeny, R.T., Engel, J., Distant metastases do not metastasize. Cancer Metastasis Rev. 29 (2010), 737–750.
21. Hüsemann, Y., Geigl, J.B., Schubert, F., Musiani, P., Meyer, M., Burghart, E., Forni, G., Eils, R., Fehm, T., Riethmüller, G., Klein, C.A., Systemic spread is an early step in breast cancer. Cancer Cell 13 (2008), 58–68.
22. Juncker-Jensen, A., Deryugina, E.I., Rimann, I., Zajac, E., Kupriyanova, T.A., Engelholm, L.H., Quigley, J.P., Tumor MMP-1 activates endothelial PAR1 to facilitate vascular intravasation and metastatic dissemination. Cancer Res. 73 (2013), 4196–4211.
23. Kalluri, R., Weinberg, R.A., The basics of epithelial-mesenchymal transition. J. Clin. Invest. 119 (2009), 1420–1428.
24. Kedrin, D., Gligorijevic, B., Wyckoff, J., Verkhusha, V.V., Condeelis, J., Segall, J.E., van Rheenen, J., Intravital imaging of metastatic behavior through a mammary imaging window. Nat. Methods 5 (2008), 1019–1021.
25. Kim, J., Yu, W., Kovalski, K., Ossowski, L., Requirement for specific proteases in cancer cell intravasation as revealed by a novel semiquantitative PCR-based assay. Cell 94 (1998), 353–362.
26. Klein, C.A., Parallel progression of primary tumours and metastases. Nat. Rev. Cancer 9 (2009), 302–312.
27. Kovacs, E., Zorn, J.A., Huang, Y., Barros, T., Kuriyan, J., A structural perspective on the regulation of the epidermal growth factor receptor. Annu. Rev. Biochem. 84 (2015), 739–764.
28. Massagué, J., Obenauf, A.C., Metastatic colonization by circulating tumour cells. Nature 529 (2016), 298–306.
29. Minder, P., Zajac, E., Quigley, J.P., Deryugina, E.I., EGFR regulates the development and microarchitecture of intratumoral angiogenic vasculature capable of sustaining cancer cell intravasation. Neoplasia 17 (2015), 634–649.
30. Partridge, J.J., Madsen, M.A., Ardi, V.C., Papagiannakopoulos, T., Kupriyanova, T.A., Quigley, J.P., Deryugina, E.I., Functional analysis of matrix metalloproteinases and tissue inhibitors of metalloproteinases differentially expressed by variants of human HT-1080 fibrosarcoma exhibiting high and low levels of intravasation and metastasis. J. Biol. Chem. 282 (2007), 35964–35977.
31. Podsypanina, K., Du, Y.C., Jechlinger, M., Beverly, L.J., Hambardzumyan, D., Varmus, H., Seeding and propagation of untransformed mouse mammary cells in the lung. Science 321 (2008), 1841–1844.
32. 1 integrin is a metastasis suppressor in mouse models and human cancer. J. Clin. Invest. 121 (2011), 226–237.
33. Rhim, A.D., Mirek, E.T., Aiello, N.M., Maitra, A., Bailey, J.M., McAllister, F., Reichert, M., Beatty, G.L., Rustgi, A.K., Vonderheide, R.H., et al. EMT and dissemination precede pancreatic tumor formation. Cell 148 (2012), 349–361.
34. Riedl, C.C., Slobod, E., Jochelson, M., Morrow, M., Goldman, D.A., Gonen, M., Weber, W.A., Ulaner, G.A., Retrospective analysis of 18F-FDG PET/CT for staging asymptomatic breast cancer patients younger than 40 years. J. Nucl. Med. 55 (2014), 1578–1583.
35. Suh, D.H., Kim, T.H., Kim, J.W., Kim, S.Y., Kim, H.S., Lee, T.S., Chung, H.H., Kim, Y.B., Park, N.H., Song, Y.S., Improvements to the FIGO staging for ovarian cancer: Reconsideration of lymphatic spread and intraoperative tumor rupture. J. Gynecol. Oncol. 24 (2013), 352–358.
36. Turajlic, S., Swanton, C., Metastasis as an evolutionary process. Science 352 (2016), 169–175.
37. Weinberg, R.A., The Biology of Cancer. 2013, Taylor & Francis Group.
38. Wyckoff, J.B., Wang, Y., Lin, E.Y., Li, J.F., Goswami, S., Stanley, E.R., Segall, J.E., Pollard, J.W., Condeelis, J., Direct visualization of macrophage-assisted tumor cell intravasation in mammary tumors. Cancer Res. 67 (2007), 2649–2656.
39. Xue, C., Wyckoff, J., Liang, F., Sidani, M., Violini, S., Tsai, K.L., Zhang, Z.Y., Sahai, E., Condeelis, J., Segall, J.E., Epidermal growth factor receptor overexpression results in increased tumor cell motility in vivo coordinately with enhanced intravasation and metastasis. Cancer Res. 66 (2006), 192–197.
40. Ye, X., Weinberg, R.A., Epithelial-mesenchymal plasticity: A central regulator of cancer progression. Trends Cell Biol. 25 (2015), 675–686.
41. Yoshida, Y., Murayama, T., Sato, Y., Suzuki, Y., Saito, H., Tanaka, N., Validation of 7th TNM staging system for lung cancer, based on surgical outcomes. Asian Cardiovasc. Thorac. Ann. 21 (2013), 693–699.