Advertisement

Biochemistry (Moscow)

, Volume 84, Issue 7, pp 762–772 | Cite as

Intravasation as a Key Step in Cancer Metastasis

  • M. V. Zavyalova
  • E. V. Denisov
  • L. A. TashirevaEmail author
  • O. E. Savelieva
  • E. V. Kaigorodova
  • N. V. Krakhmal
  • V. M. Perelmuter
Review
  • 2 Downloads

Abstract

Intravasation is a key step in cancer metastasis during which tumor cells penetrate the vessel wall and enter circulation, thereby becoming circulating tumor cells and potential metastatic seeds. Understanding the molecular mechanisms of intravasation is critically important for the development of therapeutic strategies to prevent metastasis. In this article, we review current data on the mechanisms of cancer cell intravasation into the blood and lymphatic vessels. The entry of mature thymocytes into the circulation and of dendritic cells into the regional lymph nodes is considered as examples of intravasation under physiologically normal conditions. Intravasation in a pathophysiological state is illustrated by the reverse transendothelial migration of leukocytes into the bloodstream from the sites of inflammation mediated by the sphingosine 1-phosphate interaction with its receptors. Intravasation involves both invasion-dependent and independent mechanisms. In particular, mesenchymal and amoeboid cell invasion, as well as neoangiogenesis and vascular remodeling, are discussed to play a significant role in the entry of tumor cells to the circulation. Special attention is given to the contribution of macrophages to the intravasation via the CSF1/EGF (colony stimulating factor 1/epidermal growth factor) paracrine signaling pathway and the TMEM (tumor microenvironment of metastasis)-mediated mechanisms. Other mechanisms including intravasation of tumor cell clusters surrounded by the vessel wall elements, cooperative intravasation (entry of non-invasive tumor cells to the circulation following invasive tumor cells), and intravasation associated with the vasculogenic mimicry (formation of vascular channels by tumor cells) are also discussed. Novel intravasation-specific mechanisms that have not yet been described in the literature are suggested. The importance of targeted therapeutic strategies to prevent cancer intravasation is emphasized.

Keywords

intravasation invasion hematogenous metastasis carcinoma TMEM extrusion 

Abbreviations

CCL

CC chemokine ligand

CCR

CC chemokine receptor

CSF1

colony-stimulating factor 1

CSF1R

colony-stimulating factor 1 receptor

CTC

circulating tumor cell

CXCL

CXC chemokine ligand

CXCR

CXC chemokine receptor

DC

dendritic cell

EGF

epidermal growth factor

EGFR

epidermal growth factor receptor

EMT

epithelialmesenchymal transition

ICAM1

intercellular adhesion molecule 1

MDSC

myeloid-derived suppressor cell

MENA

mammalian enabled (actin regulator)

NACT

neoadjuvant chemotherapy

S1P

sphingosine-1-phosphate

S1PR

sphingosine-1-phosphate receptor

TGF-β

transforming growth factor β

TIE-2

angiopoietin-2 receptor

TMEM

tumor microenvironment of metastasis

VEGF-A

vascular endothelial growth factor A

VM

vasculogenic mimicry

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Dua, R. S., Gui, G. P., and Isacke, C. M. (2005) Endothelial adhesion molecules in breast cancer invasion into the vascular and lymphatic systems, Eur. J. Surg. Oncol., 31, 824–832; doi: 10.1016/j.ejso.2005.05.015.CrossRefGoogle Scholar
  2. 2.
    Chiang, S. P. H., Cabrera, R. M., and Segall, J. E. (2016) Tumor cell intravasation, Am. J. Physiol. Cell Physiol., 311, 1–14, doi: 10.1152/ajpcell.00238.2015.CrossRefGoogle Scholar
  3. 3.
    Gil-Henn, H., Patsialou, A., Wang, Y., Warren, M. S., Condeelis, J. S., and Koleske, A. J. (2012) Arg/Abl2 promotes invasion and attenuates proliferation of breast cancer in vivo, Oncogene, 32, 2622–2630; doi: 10.1038/onc. 2012.284.CrossRefGoogle Scholar
  4. 4.
    Roh-Johnson, M., Bravo- Cordero, J. J., Patsialou, A., Sharma, V. P., Guo, P., Liu, H., Hodgson, L., and Condeelis, J. (2014) Macrophage contact induces RhoA GTPase signaling to trigger tumor cell intravasation, Oncogene, 33, 4203–4212; doi: 10.1038/onc.2013.377.CrossRefGoogle Scholar
  5. 5.
    Cristofanilli, M., Budd, G. T., Ellis, M. J., Stopeck, A., Matera, J., Miller, M. C., Reuben, J. M., Doyle, G. V., Allard, W. J., Terstappen, L. W., and Hayes, D. F. (2004) Circulating tumor cells, disease progression, and survival in metastatic breast cancer, N. Engl. J. Med., 351, 781–791; doi: 10.1056/NEJMoa040766.CrossRefGoogle Scholar
  6. 6.
    Weinreich, M. A., and Hogquist, K. A. (2008) Thymic emigration: when and how T cells leave home, J. Immunol., 181, 2265–2270; doi: 10.4049/jimmunol.181.4.2265.CrossRefGoogle Scholar
  7. 7.
    Schwab, S. R., and Cyster, J. G. (2007) Finding a way out: lymphocyte egress from lymphoid organs, Nat. Immunol., 8, 1295–1301; doi: 10.1038/ni1545.CrossRefGoogle Scholar
  8. 8.
    Sanchez, T., and Hla, T. (2004) Structural and functional characteristics of S1P receptors, J. Cell. Biochem., 92, 913922; doi: 10.1002/jcb.20127.CrossRefGoogle Scholar
  9. 9.
    Rosen, H., Gonzalez-Cabrera, P. J., Sanna, M. G., and Brown, S. (2009) Sphingosine 1-phosphate receptor signaling, Annu. Rev. Biochem., 78, 743–768; doi: 10.1146/ annurev.biochem.78.072407.103733.CrossRefGoogle Scholar
  10. 10.
    Resop, R. S., Douaisi, M., Craft, J., Jachimowski, L. C., Blom, B., and Uittenbogaart, C. H. (2016) Sphingosine-1phosphate/sphingosine-1-phosphate receptor 1 signaling is required for migration of naive human T cells from the thymus to the periphery, J. Allergy Clin. Immunol., 138, 551557; doi: 10.1016/j.jaci.2015.12.1339.CrossRefGoogle Scholar
  11. 11.
    Zachariah, M. A., and Cyster, J. G. (2010) Neural crestderived pericytes promote egress of mature thymocytes at the corticomedullary junction, Science, 328, 1129-1135; doi: 10.1126/science.1188222.Google Scholar
  12. 12.
    Matloubian, M., Lo, C. G., Cinamon, G., Lesneski, M. J., Xu, Y., Brinkmann, V., Allende, M. L., Proia, R. L., and Cyster, J. G. (2004) Lymphocyte egress from thymus and peripheral lymphoid organs is dependent on S1P receptor, Nature, 427, 355–360; doi: 10.1038/nature02284.CrossRefGoogle Scholar
  13. 13.
    Maeda, Y., Seki, N., Sato, N., Sugahara, K., and Chiba, K. (2010) Sphingosine 1-phosphate receptor type 1 regulates egress of mature T cells from mouse bone marrow, Int. Immunol., 22, 515–525; doi: 10.1093/intimm/dxq036.CrossRefGoogle Scholar
  14. 14.
    Chiba, K., Matsuyuki, H., Maeda, Y., and Sugahara, K. (2006) Role of sphingosine 1-phosphate receptor type 1 in lymphocyte egress from secondary lymphoid tissues and thymus, Cell Mol. Immunol., 3, 11–19.Google Scholar
  15. 15.
    Ueno, H., Schmitt, N., Palucka, A. K., and Banchereau, J. (2010) Dendritic cells and humoral immunity in humans, Immunol. Cell Biol., 88, 376–380; doi: 10.1038/icb.2010.28.CrossRefGoogle Scholar
  16. 16.
    Seyfizadeh, N., Muthuswamy, R., Mitchell, D. A., Nierkens, S., and Seyfizadeh, N. (2016) Migration of dendritic cells to the lymph nodes and its enhancement to drive anti-tumor responses, Crit. Rev. Oncol. Hematol., 107, 100110.CrossRefGoogle Scholar
  17. 17.
    Eigenbrod, S., Derwand, R., Jakl, V., Endres, S., and Eigler, A. (2006) Sphingosine kinase and sphingosine-1phosphate regulate migration, endocytosis and apoptosis of dendritic cells, Immunol. Invest., 35, 149–165; doi: 10.1080/08820130600616490.CrossRefGoogle Scholar
  18. 18.
    Gollmann, G., Neuwirt, H., Tripp, C. H., Mueller, H., Konwalinka, G., Heufler, C., Romani, N., and Tiefenthaler, M. (2008) Sphingosine-1-phosphate receptor type-1 agonism impairs blood dendritic cell chemotaxis and skin dendritic cell migration to lymph nodes under inflammatory conditions, Int. Immunol., 20, 911–923; doi: 10.1093/intimm/dxn050.CrossRefGoogle Scholar
  19. 19.
    Rathinasamy, A., Czeloth, N., Pabst, O., Forster, R., and Bernhardt, G. (2010) The origin and maturity of dendritic cells determine the pattern of sphingosine 1-phosphate receptors expressed and required for efficient migration, J. Immunol., 185, 4072–4081; doi: 10.4049/jimmunol. 1000568.CrossRefGoogle Scholar
  20. 20.
    Tauzin, S., Starnes, T. W., Becker, F. B., Lam, P., and Huttenlocher, A. (2014) Redox and Src family kinase signaling control leukocyte wound attraction and neutrophil reverse migration, J. Cell Biol., 207, 589; doi: 10.1083/ jcb.201408090.Google Scholar
  21. 21.
    Buckley, C. D., Ross, E. A., McGettrick, H. M., Osborne, C. E., Haworth, O., Schmutz, C., Stone, P. C., Salmon, M., Matharu, N. M., Vohra, R. K., Nash, G. B., and Rainger, G. E. (2005) Identification of a phenotypically and functionally distinct population of long-lived neutrophils in a model of reverse endothelial migration, J. Leukoc. Biol., 79, 303–311; doi: 10.1189/jlb. 090549621.CrossRefGoogle Scholar
  22. 22.
    Joly, E., and Hudrisier, D. (2003) What is trogocytosis and what is its purpose? Nat. Immunol., 4, 815; doi: 10.1038/ ni0903-815.CrossRefGoogle Scholar
  23. 23.
    Burn, T., and Alvarez, J. I. (2017) Reverse transendothelial cell migration in inflammation: to help or to hinder? Cell. Mol. Life Sci., 74, 1871–1881; doi: 10.1007/s00018-0162444-2.CrossRefGoogle Scholar
  24. 24.
    Sleeman, J. P., Nazarenko, I., and Thiele, W. (2011) Do all roads lead to Rome? Routes to metastasis development, Int. J. Cancer, 128, 2511–2526; doi: 10.1002/ijc.26027.CrossRefGoogle Scholar
  25. 25.
    Giampieri, S., Manning, C., Hooper, S., Jones, L., Hill, C. S., and Sahai, E. (2009) Localized and reversible TGFβ signaling switches breast cancer cells from cohesive to single cell motility, Nat. Cell Biol., 11, 1287–1296; doi: 10.1038/ ncb1973.CrossRefGoogle Scholar
  26. 26.
    Spano, D., Heck, C., De Antonellis, P., Christofori, G., and Zollo, M. (2012) Molecular networks that regulate cancer metastasis, Semin. Cancer Biol., 22, 234–249; doi: 10.1016/j.semcancer.2012.03.006.CrossRefGoogle Scholar
  27. 27.
    Friedl, P., Locker, J., Sahai, E., and Segall, J. E. (2012) Classifying collective cancer cell invasion, Nat. Cell Biol., 14, 777–783, doi: 10.1038/ncb2548.CrossRefGoogle Scholar
  28. 28.
    Stoletov, K., Montel, V., Lester, R. D., Gonias, S. L., and Klemke, R. (2007) High-resolution imaging of the dynamic tumor cell vascular interface in transparent zebrafish, Proc. Natl. Acad. Sci. USA, 104, 17406–17411; doi: 10.1073/pnas.0703446104.CrossRefGoogle Scholar
  29. 29.
    Hana, W., Chenb, S., Yuanc, W., Fana, Q., Tianb, J., Wanga, X., Chend, L., Zhange, X., Weie, W., Liuf, R., Quc, J., Jiaob, Y., Austing, R. H., and Liuf, L. (2016) Oriented collagen fibers direct tumor cell intravasation, Proc. Natl. Acad. Sci. USA, 113, 11208–11213; doi: 10.1073/ pnas.1610347113.CrossRefGoogle Scholar
  30. 30.
    Pollard, J. W. (2008) Macrophages define the invasive microenvironment in breast cancer, J. Leukoc. Biol., 84, 623–630; doi: 10.1189/jlb.1107762.CrossRefGoogle Scholar
  31. 31.
    Lin, E. Y., Gouon-Evans, V., Nguyen, A. V., and Pollard, J. W. (2002) The macrophage growth factor CSF-1 in mammary gland development and tumor progression, J. Mamm. Gland Biol. Neoplasia, 7, 147–162; doi: 10.1023/ A:1020399802795.CrossRefGoogle Scholar
  32. 32.
    Wyckoff, J., Wang, W., Lin, E. Y., Wang, Y., Pixley, F., Stanley, E. R., Graf, T., Pollard, J. W., Segall, J., and Condeelis, J. (2004) A paracrine loop between tumor cells and macrophages is required for tumor cell migration in mammary tumors, Cancer Res., 64, 7022–7029; doi: 10.1158/0008-5472.CAN-04-1449.CrossRefGoogle Scholar
  33. 33.
    Van Nguyen, A., and Pollard, J. W. (2002) Colony stimulating factor-1 is required to recruit macrophages into the mammary gland to facilitate mammary ductal outgrowth, Dev. Biol., 247, 11–25; doi: 10.1006/dbio.2002.0669.CrossRefGoogle Scholar
  34. 34.
    Yamaguchi, H., Pixley, F., and Condeelis, J. (2006) Invadopodia and podosomes in tumor invasion, Eur. J. Cell Biol., 85, 213–218; doi: 10.1016/j.ejcb.2005.10.004.CrossRefGoogle Scholar
  35. 35.
    Arwert, E. N., Harney, A. S., Entenberg, D., Wang, Y., Sahai, E., Pollard, J. W., and Condeelis, J. S. (2018) A unidirectional transition from migratory to perivascular macrophage is required for tumor cell intravasation, Cell Rep., 23, 1239–1248; doi: 10.1016/j.celrep.2018.04.007.CrossRefGoogle Scholar
  36. 36.
    Ahirwar, D. K., Nasser, M. W., Ouseph, M. M., Elbaz, M., Cuitino, M. C., Kladney, R. D., Varikuti, S., Kaul, K., Satoskar, A. R., Ramaswamy, B., Zhang, X., Ostrowski, M. C., Leone, G., and Ganju, R. K. (2018) Fibroblast-derived CXCL12 promotes breast cancer metastasis by facilitating tumor cell intravasation, Oncogene, 37, 4428–4442; doi: 10.1038/s41388-018-0263-7.CrossRefGoogle Scholar
  37. 37.
    Leung, E., Xue, A., and Wang, Y. (2017) Blood vessel endothelium-directed tumor cell streaming in breast tumors requires the HGF/C-Met signaling pathway, Oncogene, 36, 2680–2692; doi: 10.1038/onc.2016.421.CrossRefGoogle Scholar
  38. 38.
    Robinson, B. D., Sica, G. L., Liu, Y., Rohan, T. E., Gertler, F. B., Condeelis, J. S., and Jones, J. G. (2009) Tumor microenvironment of metastasis in human breast carcinoma: a potential prognostic marker linked to hematogenous dissemination, Clin. Cancer Res., 15, 24332441; doi: 10.1158/1078-0432.CCR-08-2179.CrossRefGoogle Scholar
  39. 39.
    Harney, A. S., Arwert, E. N., Entenberg, D., Wang, Y., Guo, P., Qian, B. Z., Oktay, M. H., Pollard, J. W., Jones, J. G., and Condeelis, J. S. (2015) Real-time imaging reveals local, transient vascular permeability, and tumor cell intravasation stimulated by TIE2hi macrophage-derived VEGFA, Cancer Discov., 5, 932–943; doi: 10.1158/21598290.CD-15-0012.CrossRefGoogle Scholar
  40. 40.
    Rohan, T. E., Xue, X., Lin, H., D’Alfonso, T. M., Ginter, P. S., Oktay, M. H., Robinson, B. D., Ginsberg, M., Gertler, F. B., Glass, A. G., Sparano, J. A., Condeelis, J. S., and Jones, J. G. (2014) Tumor microenvironment of metastasis and risk of distant metastasis of breast cancer, J. Natl. Cancer Inst., 106, dju136; doi: 10.1093/jnci/dju136.Google Scholar
  41. 41.
    Saharinen, P., Eklund, L., Pulkki, K., Bono, P., and Alitalo, K. (2011) VEGF and angiopoietin signaling in tumor angiogenesis and metastasis, Trends Mol. Med., 17, 347–362; doi: 10.1016/j.molmed.2011.01.015.CrossRefGoogle Scholar
  42. 42.
    Wu, X., Giobbie-Hurder, A., Liao, X., Connelly, C., Connolly, E. M., and Li, J. (2017) Angiopoietin-2 as a biomarker and target for immune checkpoint therapy, Cancer Immunol. Res., 5, 17–28; doi: 10.1158/2326-6066.CIR-160206.CrossRefGoogle Scholar
  43. 43.
    Murdoch, C., Tazzyman, S., Webster, S., and Lewis, C. E. (2007) Expression of Tie-2 by human monocytes and their responses to angiopoietin-2, J. Immunol., 178, 7405–7411; doi: 10.4049/jimmunol.178.11.7405.CrossRefGoogle Scholar
  44. 44.
    De Palma, M., Venneri, M. A., Galli, R., Sergi Sergi, L., Politi, L. S., Sampaolesi, M., and Naldini, L. (2005) Tie2 identifies a hematopoietic lineage of proangiogenic monocytes required for tumor vessel formation and a mesenchymal population of pericyte progenitors, Cancer Cell, 8, 211226; doi: 10.1016/j.ccr.2005.08.002.CrossRefGoogle Scholar
  45. 45.
    Karagiannis, G. S., Pastoriza, J. M., Wang, Y., Harney, A. S., Entenberg, D., Pignatelli, J., Sharma, V. P., Xue, E. A., Cheng, E., D’Alfonso, T. M., Jones, J. G., Anampa, J., Rohan, T. E., Sparano, J. A., Condeelis, J. S., and Oktay, M. H. (2017) Neoadjuvant chemotherapy induces breast cancer metastasis through a TMEM-mediated mechanism, Sci. Transl. Med., 9, eaan0026; doi: 10.1126/scitranslmed.aan0026.CrossRefGoogle Scholar
  46. 46.
    Karagiannis, G. S., Condeelis, J. S., and Oktay, M. H. (2017) Chemotherapy-induced metastasis in breast cancer, Oncotarget, 8, 110733–110734; doi: 10.18632/oncotarget. 22717.CrossRefGoogle Scholar
  47. 47.
    Coffelt, S. B., Chen, Y. Y., Muthana, M., Welford, A. F., Tal, A. O., Scholz, A., Plate, K. H., Reiss, Y., Murdoch, C., De Palma, M., and Lewis, C. E. (2011) Angiopoietin 2 stimulates TIE2-expressing monocytes to suppress T cell activation and to promote regulatory T cell expansion, J. Immunol., 186, 4183–4190; doi: 10.4049/jimmunol.1002802.CrossRefGoogle Scholar
  48. 48.
    Ibberson, M., Bron, S., Guex, N., Faes-van’t Hull, E., Ifticene-Treboux, A., Henry, L., Lehr, H. A., Delaloye, J. F., Coukos, G., Xenarios, I., and Doucey, M. A. (2013) TIE-2 and VEGFR kinase activities drive immunosuppressive function of TIE-2-expressing monocytes in human breast tumors, Clin. Cancer Res., 19, 3439–3449; doi: 10.1158/1078-0432.CCR-12-3181.CrossRefGoogle Scholar
  49. 49.
    Si, Y., Tsou, C. L., Croft, K., and Charo, I. F. (2010) CCR2 mediates hematopoietic stem and progenitor cell trafficking to sites of inflammation in mice, J. Clin. Invest., 120, 1192–1203; doi: 10.1172/JCI40310.CrossRefGoogle Scholar
  50. 50.
    Johns, J. L., and Christopher, M. M. (2012) Extramedullary hematopoiesis: a new look at the underlying stem cell niche, theories of development, and occurrence in animals, Vet. Pathol., 49, 508–523; doi: 10.1177/ 0300985811432344.CrossRefGoogle Scholar
  51. 51.
    Matsubara, T., Kanto, T., Kuroda, S., Yoshio, S., Higashitani, K., Kakita, N., Miyazaki, M., Sakakibara, M., Hiramatsu, N., Kasahara, A., Tomimaru, Y., Tomokuni, A., Nagano, H., Hayashi, N., and Takehara, T. (2013) TIE2-expressing monocytes as a diagnostic marker for hepatocellular carcinoma correlates with angiogenesis, Hepatology, 57, 1416–1425; doi: 10.1002/hep.25965.CrossRefGoogle Scholar
  52. 52.
    Talmadge, J. E., and Gabrilovich, D. I. (2013) History of myeloid-derived suppressor cells, Nat. Rev. Cancer, 13, 739–752; doi: 10.1038/nrc3581.CrossRefGoogle Scholar
  53. 53.
    Yang, L., DeBusk, L. M., Fukuda, K., Fingleton, B., Green-Jarvis, B., Shyr, Y., Matrisian, L. M., Carbone, D. P., and Lin, P. C. (2004) Expansion of myeloid immune suppressor Gr+CD11b+ cells in tumor-bearing host directly promotes tumor angiogenesis, Cancer Cell, 6, 409–421; doi: 10.1016/j.ccr.2004.08.031.CrossRefGoogle Scholar
  54. 54.
    Yang, L., Huang, J., Ren, X., Gorska, A. E., Chytil, A., Aakre, M., Carbone, D. P., Matrisian, L. M., Richmond, A., Lin, P. C., and Moses, H. L. (2008) Abrogation of TGFβ signaling in mammary carcinomas recruits Gr1+CD11b+ myeloid cells that promote metastasis, Cancer Cell, 13, 23–35; doi: 10.1016/j.ccr.2007.12.004.CrossRefGoogle Scholar
  55. 55.
    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., Zhu, Z., Hicklin, D., Wu, Y., Port, J. L., Altorki, N., Port, E. R., Ruggero, D., Shmelkov, S. V., Jensen, K. K., Rafii, S., and Lyden, D. (2005) VEGFR1-positive hematopoietic bone marrow progenitors initiate the pre-metastatic niche, Nature, 438, 820–827; doi: 10.1038/nature04186.CrossRefGoogle Scholar
  56. 56.
    Peinado, H., Zhang, H., Matei, I. R., Costa-Silva, B., Hoshino, A., Rodrigues, G., Psaila, B., Kaplan, R. N., Bromberg, J. F., Kang, Y., Bissell, M. J., Cox, T. R., Giaccia, A. J., Erler, J. T., Hiratsuka, S., Ghajar, C. M., and Lyden, D. (2017) Pre-metastatic niches: organ-specific homes for metastases, Nat. Rev. Cancer, 17, 302–317; doi: 10.1038/nrc.2017.6.CrossRefGoogle Scholar
  57. 57.
    Okuno, Y., Nakamura-Ishizu, A., Kishi, K., Suda, T., and Kubota, Y. (2011) Bone marrow-derived cells serve as proangiogenic macrophages but not endothelial cells in wound healing, Blood, 117, 5264–5272; doi: 10.1182/ blood-2011-01-330720.CrossRefGoogle Scholar
  58. 58.
    Deryugina, E. I., and Kiosses, W. B. (2017) Intratumoral cancer cell intravasation can occur independent of invasion into the adjacent stroma, Cell Rep., 19, 601–616; doi: 10.1016/j.celrep.2017.03.064.CrossRefGoogle Scholar
  59. 59.
    Sugino, T., Kawaguchi, T., and Suzuki, T. (1993) Sequential process of blood-borne lung metastases of spontaneous mammary carcinoma in C3H mice, Int. J. Cancer, 55, 141–147; doi: 10.1002/ijc.2910550125.CrossRefGoogle Scholar
  60. 60.
    Sugino, T., Kusakabe, T., Hoshi, N., Yamaguchi, T., Kawaguchi, T., Goodison, S., Sekimata, M., Homma, Y., and Suzuki, T. (2002) An invasion-independent pathway of blood-borne metastasis: a new murine mammary tumor model, Am. J. Pathol., 160, 1973–1980; doi: 10.1016/ S0002-9440(10)61147-9.CrossRefGoogle Scholar
  61. 61.
    Weidner, N. (2002) New paradigm for vessel intravasation by tumor cells, Am. J. Pathol., 160, 1937–1939; doi: 10.1016/S0002-9440(10)61141-8.CrossRefGoogle Scholar
  62. 62.
    Kusters, B., Kats, G., Roodink, I., Verrijp, K., Wesseling, P., Ruiter, D. J., de Waal, R. M., and Leenders, W. P. (2007) Micronodular transformation as a novel mechanism of VEGF-A-induced metastasis, Oncogene, 26, 5808–5815; doi: 10.1038/sj.onc.1210360.CrossRefGoogle Scholar
  63. 63.
    Kats-Ugurlu, G., Roodink, I., de Weijert, M., Tiemessen, D., Maass, C., Verrijp, K., van der Laak, J., de Waal, R., Mulders, P., Oosterwijk, E., and Leenders, W. (2009) Circulating tumor tissue fragments in patients with pulmonary metastasis of clear cell renal cell carcinoma, J. Pathol., 219, 287–293; doi: 10.1002/path.2613.CrossRefGoogle Scholar
  64. 64.
    Aceto, N., Bardia, A., Miyamoto, D. T., Donaldson, M. C., Wittner, B. S., Spencer, J. A., Yu, M., Pely, A., Engstrom, A., Zhu, H., Brannigan, B. W., Kapur, R., Stott, S. L., Shioda, T., Ramaswamy, S., Ting, D. T., Lin, C. P., Toner, M., Haber, D. A., and Maheswaran, S. (2014) Circulating tumor cell clusters are oligoclonal precursors of breast cancer metastasis, Cell, 158, 1110–1122; doi: 10.1016/j.cell.2014.07.013.CrossRefGoogle Scholar
  65. 65.
    Tsuji, T., Ibaragi, S., and Hu, G. F. (2009) Epithelial-mesenchymal transition and cell cooperativity in metastasis, Cancer Res., 69, 7135–7139; doi: 10.1158/0008-5472. CAN-09-1618.CrossRefGoogle Scholar
  66. 66.
    Lyons, J. G., Lobo, E., Martorana, A. M., and Myerscough, M. R. (2008) Clonal diversity in carcinomas: its implications for tumor progression and the contribution made to it by epithelial-mesenchymal transitions, Clin. Exp. Metastasis, 25, 665–677; doi: 10.1007/s10585-0079134-2.CrossRefGoogle Scholar
  67. 67.
    Shen, Y., Quan, J., Wang, M., Li, S., Yang, J., Lv, M., Chen, Z., Zhang, L., Zhao, X., and Yang, J. (2017) Tumor vasculogenic mimicry formation as an unfavorable prognostic indicator in patients with breast cancer, Oncotarget, 8, 56408–56416; doi: 10.18632/oncotarget.16919.Google Scholar
  68. 68.
    Ge, H., and Luo, H. (2018) Overview of advances in vasculogenic mimicry–a potential target for tumor therapy, Cancer Manag. Res., 10, 2429–2437; doi: 10.2147/ CMAR.S164675.CrossRefGoogle Scholar
  69. 69.
    Gu, Y., Forostyan, T., Sabbadini, R., and Rosenblatt, J. (2011) Epithelial cell extrusion requires the sphingosine-1-phosphate receptor 2 pathway, J. Cell. Biol., 193, 667–676; doi: 10.1083/jcb.201010075.CrossRefGoogle Scholar
  70. 70.
    Gudipaty, S. A., and Rosenblatt, J. (2017) Epithelial cell extrusion: pathways and pathologies, Semin. Cell. Dev. Biol., 67, 132–140; doi: 10.1016/j.semcdb.2016.05.010.CrossRefGoogle Scholar
  71. 71.
    Slattum, G., Gu, Y., Sabbadini, R., and Rosenblatt, J. (2014) Autophagy in oncogenic K-Ras promotes basal extrusion of epithelial cells by degrading S1P, Curr. Biol., 24, 19–28; doi: 10.1016/j.cub.2013.11.029.CrossRefGoogle Scholar
  72. 72.
    Nakajima, M., Nagahashi, M., Rashid, O. M., Takabe, K., and Wakai, T. (2017) The role of sphingosine-1-phosphate in the tumor microenvironment and its clinical implications, Tumour Biol., 39, 1010428317699133; doi: 10.1177/ 1010428317699133.CrossRefGoogle Scholar
  73. 73.
    Waeber, C., Blondeau, N., and Salomone, S. (2004) Vascular sphingosine-1-phosphate S1P1 and S1P3 receptors, Drug News Perspect., 17, 365–382.CrossRefGoogle Scholar
  74. 74.
    Saito, H., Minamiya, Y., Kitamura, M., Saito, S., Enomoto, K., Terada, K., and Ogawa, J. (1998) Endothelial myosin light chain kinase regulates neutrophil migration across human umbilical vein endothelial cell monolayer, J. Immunol., 161, 1533–1540.Google Scholar
  75. 75.
    McVerry, B. J., and Garcia, J. G. (2004) Endothelial cell barrier regulation by sphingosine 1-phosphate, J. Cell Biochem., 92, 1075–1085; doi: 10.1002/jcb.20088.CrossRefGoogle Scholar
  76. 76.
    Lustberg, M. B., Balasubramanian, P., Miller, B., GarciaVilla, A., Deighan, C., Wu, Y., Carothers, S., Berger, M., Ramaswamy, B., Macrae, E. R., Wesolowski, R., Layman, R. M., Mrozek, E., Pan, X., Summers, T. A., Shapiro, C. L., and Chalmers, J. J. (2014) Heterogeneous atypical cell populations are present in blood of metastatic breast cancer patients, Breast Cancer Res., 16, R23; doi: 10.1186/bcr3622.CrossRefGoogle Scholar
  77. 77.
    Akhter, M. Z., Sharawat, S. K., Kumar, V., Kochat, V., Equbal, Z., Ramakrishnan, M., Kumar, U., Mathur, S., Kumar, L., and Mukhopadhyay, A. (2018) Aggressive serous epithelial ovarian cancer is potentially propagated by EpCAM+CD45+ phenotype, Oncogene, 37, 2089–2103; doi: 10.1038/s41388-017-0106-y.CrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2019

Authors and Affiliations

  • M. V. Zavyalova
    • 1
    • 2
  • E. V. Denisov
    • 1
  • L. A. Tashireva
    • 1
    Email author
  • O. E. Savelieva
    • 1
  • E. V. Kaigorodova
    • 1
    • 2
  • N. V. Krakhmal
    • 1
    • 2
  • V. M. Perelmuter
    • 1
  1. 1.Cancer Research Institute, Tomsk National Research Medical CenterRussian Academy of SciencesTomskRussia
  2. 2.Siberian State Medical UniversityMinistry of Health of the Russian FederationTomskRussia

Personalised recommendations