Adhesion receptors as therapeutic targets for circulating tumor cells

Frontiers in Oncology

Volumn 2 JUL, Issue , 2012, Pages

  Li, Jiahe ^a   King, Michael R ^a  

^a School of Chemical and Molecular Engineering   (United States)

Author keywords

Adhesion; Cancer therapy; CTCs; Receptors

Indexed keywords

ADHESION RECEPTOR; BETA INTEGRIN; EPIDERMAL GROWTH FACTOR; FUCOSYLTRANSFERASE; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 1; LECTIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; RECEPTOR; SELECTIN; TUMOR MARKER; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UNCLASSIFIED DRUG; VASCULAR CELL ADHESION MOLECULE 1;

APOPTOSIS; CANCER THERAPY; CELL GROWTH; CELL INTERACTION; CELL PROLIFERATION; CELL VIABILITY; CIRCULATING TUMOR CELL; ENDOTHELIUM; GENE SILENCING; HUMAN; INTRACELLULAR SIGNALING; METASTASIS; REVIEW; SURVIVAL; THROMBOCYTE AGGLUTINATION; TUMOR INVASION; TUMOR MICROENVIRONMENT;

EID: 84872773111     PISSN: None     EISSN: 2234943X     Source Type: Journal    
DOI: 10.3389/fonc.2012.00079     Document Type: Review

References (105)

1. Aktas, B., Tewes, M., Fehm, T., Hauch, S., Kimmig, R., and Kasimir-Bauer, S. (2009). Stem cell and epithelial-mesenchymal transition markers are frequently overexpressed in circulating tumor cells of metastatic breast cancer patients. Breast Cancer Res. 11, R46.
2. Allard, W. J., Matera, J., Miller, M. C., Repollet, M., Connelly, M. C., Rao, C., Tibbe, A. G., Uhr, J. W., and Terstappen, L. W. (2004). Tumor cells circulate in the peripheral blood of all major carcinomas but not in healthy subjects or patients with nonmalignant diseases. Clin. Cancer Res. 10, 6897-6904.
3. Amirkhosravi, A., Meyer, T., Amaya, M., Davila, M., Mousa, S. A., Robson, T., and Francis, J. L. (2007). The role of tissue factor pathway inhibitor in tumor growth and metastasis. Semin. Thromb. Hemost. 33, 643-652.
4. Amirkhosravi, A., Meyer, T., Chang, J. Y., Amaya, M., Siddiqui, F., Desai, H., and Francis, J. L. (2002). Tissue factor pathway inhibitor reduces experimental lung metastasis of B16 melanoma. Thromb. Haemost. 87, 930-936.
5. Bagge, U., Blixt, A., and Strid, K. G. (1983). The initiation of post-capillary margination of leukocytes: studies in vitro on the influence of erythrocyte concentration and flow velocity. Int. J. Microcirc. Clin. Exp. 2, 215-227.
6. Barthel, S. R., Gavino, J. D., Wiese, G. K., Jaynes, J. M., Siddiqui, J., and Dimitroff, C. J. (2008). Analysis of glycosyltransferase expression in metastatic prostate cancer cells capable of rolling activity on microvascular endothelial (E)-selectin. Glycobiology 18, 806-817.
7. Borsig, L., Wang, L., Cavalcante, M. C., Cardilo-Reis, L., Ferreira, P. L., Mourao, P. A., Esko, J. D., and Pavao, M. S. (2007). Selectin blocking activity of a fucosylated chondroitin sulfate glycosaminoglycan from sea cucumber. Effect on tumor metastasis and neutrophil recruitment. J. Biol. Chem. 282, 14984-14991.
8. Borsig, L., Wong, R., Feramisco, J., Nadeau, D. R., Varki, N. M., and Varki, A. (2001). Heparin and cancer revisited: mechanistic connections involving platelets, P-selectin, carcinoma mucins, and tumor metastasis. Proc. Natl. Acad. Sci. U.S.A. 98, 3352-3357.
9. Brown, J. R., Yang, F., Sinha, A., Ramakrishnan, B., Tor, Y., Qasba, P. K., and Esko, J. D. (2009). Deoxygenated disaccharide analogs as specific inhibitors of beta1-4-galactosyltransferase 1 and selectin-mediated tumor metastasis. J. Biol. Chem. 284, 4952-4959.
10. Buerke, M., Weyrich, A. S., Zheng, Z., Gaeta, F. C., Forrest, M. J., and Lefer, A. M. (1994). Sialyl Lewisx-containing oligosaccharide attenuates myocardial reperfusion injury in cats. J. Clin. Invest. 93, 1140-1148.
11. Camerer, E., Qazi, A. A., Duong, D. N., Cornelissen, I., Advincula, R., and Coughlin, S. R. (2004). Platelets, protease-activated receptors, and fibrinogen in hematogenous metastasis. Blood 104, 397-401.
12. Chambers, A. F., Groom, A. C., and Macdonald, I. C. (2002). Dissemination and growth of cancer cells in metastatic sites. Nat. Rev. Cancer 2, 563-572.
13. Chen, Q., Zhang, X. H., and Massague, J. (2011). Macrophage binding to receptor VCAM-1 transmits survival signals in breast cancer cells that invade the lungs. Cancer Cell 20, 538-549.
14. Coumans, F. A., Doggen, C. J., Attard, G., De Bono, J. S., and Terstappen, L. W. (2010). All circulating EpCAM+CK+CD45-objects predict overall survival in castration-resistant prostate cancer. Ann. Oncol. 21, 1851-1857.
15. Coussens, L. M., and Werb, Z. (2002). Inflammation and cancer. Nature 420, 860-867.
16. Criscitiello, C., Sotiriou, C., and Ignatiadis, M. (2010). Circulating tumor cells and emerging blood biomarkers in breast cancer. Curr. Opin. Oncol. 22, 552-558.
17. 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.
18. Cristofanilli, M., Hayes, D. F., Budd, G. T., Ellis, M. J., Stopeck, A., Reuben, J. M., Doyle, G. V., Matera, J., Allard, W. J., Miller, M. C., Fritsche, H. A., Hortobagyi, G. N., and Terstappen, L. W. (2005). Circulating tumor cells: a novel prognostic factor for newly diagnosed metastatic breast cancer. J. Clin. Oncol. 23, 1420-1430.
19. Danila, D. C., Fleisher, M., and Scher, H. I. (2011). Circulating tumor cells as biomarkers in prostate cancer. Clin. Cancer Res. 17, 3903-3912.
20. Ding, K. F., and Zheng, S. (2004). [Study on relationship of fucosyltransferase gene types in breast cancer with metastasis and prognosis]. Zhonghua Wai Ke Za Zhi 42, 546-550.
21. Elices, M. J., Osborn, L., Takada, Y., Crouse, C., Luhowskyj, S., Hemler, M. E., and Lobb, R. R. (1990). VCAM-1 on activated endothelium interacts with the leukocyte integrin VLA-4 at a site distinct from the VLA-4/fibronectin binding site. Cell 60, 577-584.
22. Frisch, S. M., and Ruoslahti, E. (1997). Integrins and anoikis. Curr. Opin. Cell Biol. 9, 701-706.
23. Geng, Y., Marshall, J. R., and King, M. R. (2012). Glycomechanics of the metastatic cascade: tumor cell-endothelial cell interactions in the circulation. Ann. Biomed. Eng. 40, 790-805.
24. Geng, Y., Narasipura, S., Seigel, G. M., and King, M. R. (2010). Vascular recruitment of human retinoblastoma cells by multi-cellular adhesive interactions with circulating leukocytes. Cell. Mol. Bioeng. 3, 361-368.
25. Ghiaur, G., Gerber, J. M., Matsui, W., and Jones, R. J. (2012). Cancer stem cells: relevance to clinical transplantation. Curr. Opin. Oncol. 24, 170-175.
26. Goldsmith, H. L., and Spain, S. (1984). Margination of leukocytes in blood flow through small tubes. Microvasc. Res. 27, 204-222.
27. Grailer, J. J., Kodera, M., and Steeber, D. A. (2009). L-selectin: role in regulating homeostasis and cutaneous inflammation. J. Dermatol. Sci. 56, 141-147.
28. Guo, Q., Guo, B., Wang, Y., Wu, J., Jiang, W., Zhao, S., Qiao, S., and Wu, Y. (2012). Functional analysis of alpha1, 3/4-fucosyltransferase VI in human hepatocellular carcinoma cells. Biochem. Biophys. Res. Commun. 417, 311-317.
29. Guo, W., and Giancotti, F. G. (2004). Integrin signalling during tumour progression. Nat. Rev. Mol. Cell Biol. 5, 816-826.
30. Gupta, G. P., and Massague, J. (2004). Platelets and metastasis revisited: a novel fatty link. J. Clin. Invest. 114, 1691-1693.
31. Hennet, T. (2002). The galactosyltransferase family. Cell. Mol. Life Sci. 59, 1081-1095.
32. Hoskins, M. H., and Dong, C. (2006). Kinetics analysis of binding between melanoma cells and neutrophils. Mol. Cell. Biomech. 3, 79-87.
33. Hostettler, N., Naggi, A., Torri, G., Ishai-Michaeli, R., Casu, B., Vlodavsky, I., and Borsig, L. (2007). P-selectin-and heparanase-dependent antimetastatic activity of non-anticoagulant heparins. FASEB J. 21, 3562-3572.
34. Hou, J. M., Greystoke, A., Lancashire, L., Cummings, J., Ward, T., Board, R., Amir, E., Hughes, S., Krebs, M., Hughes, A., Ranson, M., Lorigan, P., Dive, C., and Blackhall, F. H. (2009). Evaluation of circulating tumor cells and serological cell death biomarkers in small cell lung cancer patients undergoing chemotherapy. Am. J. Pathol. 175, 808-816.
35. Huang, Z., and King, M. R. (2009). An immobilized nanoparticle-based platform for efficient gene knockdown of targeted cells in the circulation. Gene Ther. 16, 1271-1282.
36. Hughes, A. D., and King, M. R. (2010). Use of naturally occurring halloysite nanotubes for enhanced capture of flowing cells. Langmuir 26, 12155-12164.
37. Hughes, A. D., Mattison, J., Western, L. T., Powderly, J. D., Greene, B. T., and King, M. R. (2012a). Microtube device for selectin-mediated capture of viable circulating tumor cells from blood. Clin. Chem. 58, 846-853.
38. Hughes, A. D., Mattison, J., Powderly, J. D., Greene, B. T., and King, M. R. (2012b). Rapid isolation of viable circulating tumor cells from patient blood samples. J. Vis. Exp. pii: 4248.
39. Huh, S. J., Liang, S., Sharma, A., Dong, C., and Robertson, G. P. (2010). Transiently entrapped circulating tumor cells interact with neutrophils to facilitate lung metastasis development. Cancer Res. 70, 6071-6082.
40. Iadocicco, K., Monteiro, L. H., and Chaui-Berlinck, J. G. (2002). A theoretical model for estimating the margination constant of leukocytes. BMC Physiol. 2, 3.
41. Iinuma, H., Watanabe, T., Mimori, K., Adachi, M., Hayashi, N., Tamura, J., Matsuda, K., Fukushima, R., Okinaga, K., Sasako, M., and Mori, M. (2011). Clinical significance of circulating tumor cells, including cancer stem-like cells, in peripheral blood for recurrence and prognosis in patients with Dukes' stage B and C colorectal cancer. J. Clin. Oncol. 29, 1547-1555.
42. Joyce, J. A., and Pollard, J. W. (2009). Microenvironmental regulation of metastasis. Nat. Rev. Cancer 9, 239-252.
43. Kang, Y., Siegel, P. M., Shu, W., Drobnjak, M., Kakonen, S. M., Cordon-Cardo, C., Guise, T. A., and Massague, J. (2003). A multigenic program mediating breast cancer metastasis to bone. Cancer Cell 3, 537-549.
44. Kasimir-Bauer, S., Hoffmann, O., Wallwiener, D., Kimmig, R., and Fehm, T. (2012). Expression of stem cell and epithelial-mesenchymal transition markers in primary breast cancer patients with circulating tumor cells. Breast Cancer Res. 14, R15.
45. Kasthuri, R. S., Taubman, M. B., and Mackman, N. (2009). Role of tissue factor in cancer. J. Clin. Oncol. 27, 4834-4838.
46. Kim, M. Y., Oskarsson, T., Acharyya, S., Nguyen, D. X., Zhang, X. H., Norton, L., and Massague, J. (2009). Tumor self-seeding by circulating cancer cells. Cell 139, 1315-1326.
47. Koenig, A., Norgard-Sumnicht, K., Linhardt, R., and Varki, A. (1998). Differential interactions of heparin and heparan sulfate glycosaminoglycans with the selectins. Implications for the use of unfractionated and low molecular weight heparins as therapeutic agents. J. Clin. Invest. 101, 877-889.
48. Kohler, S., Ullrich, S., Richter, U., and Schumacher, U. (2010). E-/P-selectins and colon carcinoma metastasis: first in vivo evidence for their crucial role in a clinically relevant model of spontaneous metastasis formation in the lung. Br. J. Cancer 102, 602-609.
49. Konstantopoulos, K., and Thomas, S. N. (2009). Cancer cells in transit: the vascular interactions of tumor cells. Annu. Rev. Biomed. Eng. 11, 177-202.
50. Kopp, H. G., Placke, T., and Salih, H. R. (2009). Platelet-derived transforming growth factor-beta down-regulates NKG2D thereby inhibiting natural killer cell antitumor reactivity. Cancer Res. 69, 7775-7783.
51. Koschny, R., Walczak, H., and Ganten, T. M. (2007). The promise of TRAIL-potential and risks of a novel anticancer therapy. J. Mol. Med. (Berl.) 85, 923-935.
52. Labelle, M., Begum, S., and Hynes, R. O. (2011). Direct signaling between platelets and cancer cells induces an epithelial-mesenchymal-like transition and promotes metastasis. Cancer Cell 20, 576-590.
53. Lanier, L. L. (2005). NK cell recognition. Annu. Rev. Immunol. 23, 225-274.
54. Larsen, G. R., Sako, D., Ahern, T. J., Shaffer, M., Erban, J., Sajer, S. A., Gibson, R. M., Wagner, D. D., Furie, B. C., and Furie, B. (1992). P-selectin and E-selectin. Distinct but overlapping leukocyte ligand specificities. J. Biol. Chem. 267, 11104-11110.
55. Lawrence, M. B., and Springer, T. A. (1991). Leukocytes roll on a selectin at physiologic flow rates: distinction from and prerequisite for adhesion through integrins. Cell 65, 859-873.
56. Lee, D. Y., Park, K., Kim, S. K., Park, R. W., Kwon, I. C., Kim, S. Y., and Byun, Y. (2008). Antimetastatic effect of an orally active heparin derivative on experimentally induced metastasis. Clin. Cancer Res. 14, 2841-2849.
57. Lefer, D. J., Flynn, D. M., Phillips, M. L., Ratcliffe, M., and Buda, A. J. (1994). A novel sialyl LewisX analog attenuates neutrophil accumulation and myocardial necrosis after ischemia and reperfusion. Circulation 90, 2390-2401.
58. Ley, K. (2003). The role of selectins in inflammation and disease. Trends Mol. Med. 9, 263-268.
59. Liang, S., Fu, C., Wagner, D., Guo, H., Zhan, D., Dong, C., and Long, M. (2008). Two-dimensional kinetics of beta 2-integrin and ICAM-1 bindings between neutrophils and melanoma cells in a shear flow. Am. J. Physiol. Cell Physiol. 294, C743-C753.
60. Liang, S., Slattery, M. J., and Dong, C. (2005). Shear stress and shear rate differentially affect the multi-step process of leukocyte-facilitated melanoma adhesion. Exp. Cell Res. 310, 282-292.
61. Lianidou, E. S., and Markou, A. (2011). Circulating tumor cells as emerging tumor biomarkers in breast cancer. Clin. Chem. Lab. Med. 49, 1579-1590.
62. Liu, Y., Jiang, P., Capkova, K., Xue, D., Ye, L., Sinha, S. C., Mackman, N., Janda, K. D., and Liu, C. (2011). Tissue factor-activated coagulation cascade in the tumor microenvironment is critical for tumor progression and an effective target for therapy. Cancer Res. 71, 6492-6502.
63. Lowes, L. E., Goodale, D., Keeney, M., and Allan, A. L. (2011). Image cytometry analysis of circulating tumor cells. Methods Cell Biol. 102, 261-290.
64. Lu, J., Steeg, P. S., Price, J. E., Krishnamurthy, S., Mani, S. A., Reuben, J., Cristofanilli, M., Dontu, G., Bidaut, L., Valero, V., Hortobagyi, G. N., and Yu, D. (2009). Breast cancer metastasis: challenges and opportunities. Cancer Res. 69, 4951-4953.
65. Lu, X., Mu, E., Wei, Y., Riethdorf, S., Yang, Q., Yuan, M., Yan, J., Hua, Y., Tiede, B. J., Haffty, B. G., Pantel, K., Massague, J., and Kang, Y. (2011). VCAM-1 promotes osteolytic expansion of indolent bone micrometastasis of breast cancer by engaging alpha4beta1-positive osteoclast progenitors. Cancer Cell 20, 701-714.
66. Matsuura, N., Narita, T., Hiraiwa, N., Hiraiwa, M., Murai, H., Iwase, T., Funahashi, H., Imai, T., Takagi, H., and Kannagi, R. (1998). Gene expression of fucosyl-and sialyl-transferases which synthesize sialyl Lewisx, the carbohydrate ligands for E-selectin, in human breast cancer. Int. J. Oncol. 12, 1157-1164.
67. Minn, A. J., Gupta, G. P., Siegel, P. M., Bos, P. D., Shu, W., Giri, D. D., Viale, A., Olshen, A. B., Gerald, W. L., and Massague, J. (2005). Genes that mediate breast cancer metastasis to lung. Nature 436, 518-524.
68. Mohammad, K. S., Javelaud, D., Fournier, P. G., Niewolna, M., McKenna, C. R., Peng, X. H., Duong, V., Dunn, L. K., Mauviel, A., and Guise, T. A. (2011). TGF-beta-RI kinase inhibitor SD-208 reduces the development and progression of melanoma bone metastases. Cancer Res. 71, 175-184.
69. Moreira, I. S., Fernandes, P. A., and Ramos, M. J. (2007). Vascular endothelial growth factor (VEGF) inhibition-a critical review. Anticancer Agents Med. Chem. 7, 223-245.
70. Moretta, L., and Moretta, A. (2004). Unravelling natural killer cell function: triggering and inhibitory human NK receptors. EMBO J. 23, 255-259.
71. Nagrath, S., Sequist, L. V., Maheswaran, S., Bell, D. W., Irimia, D., Ulkus, L., Smith, M. R., Kwak, E. L., Digumarthy, S., Muzikansky, A., Ryan, P., Balis, U. J., Tompkins, R. G., Haber, D. A., and Toner, M. (2007). Isolation of rare circulating tumour cells in cancer patients by microchip technology. Nature 450, 1235-1239.
72. Nieswandt, B., Hafner, M., Echtenacher, B., and Mannel, D. N. (1999). Lysis of tumor cells by natural killer cells in mice is impeded by platelets. Cancer Res. 59, 1295-1300.
73. Ogawa, J., Inoue, H., and Koide, S. (1996). Expression of alpha-1, 3-fucosyltransferase type IV and VII genes is related to poor prognosis in lung cancer. Cancer Res. 56, 325-329.
74. Osborn, L., Hession, C., Tizard, R., Vassallo, C., Luhowskyj, S., Chi-Rosso, G., and Lobb, R. (1989). Direct expression cloning of vascular cell adhesion molecule 1, a cytokine-induced endothelial protein that binds to lymphocytes. Cell 59, 1203-1211.
75. Petretti, T., Schulze, B., Schlag, P. M., and Kemmner, W. (1999). Altered mRNA expression of glycosyltransferases in human gastric carcinomas. Biochim. Biophys. Acta 1428, 209-218.
76. Placke, T., Orgel, M., Schaller, M., Jung, G., Rammensee, H. G., Kopp, H. G., and Salih, H. R. (2012). Platelet-derived MHC class I confers a pseudonormal phenotype to cancer cells that subverts the antitumor reactivity of natural killer immune cells. Cancer Res. 72, 440-448.
77. Rana, K., Liesveld, J. L., and King, M. R. (2009). Delivery of apoptotic signal to rolling cancer cells: a novel biomimetic technique using immobilized TRAIL and E-selectin. Biotechnol. Bioeng. 102, 1692-1702.
78. Rana, K., Reinhart-King, C. A., and King, M. R. (2012). Inducing apoptosis in rolling cancer cells: a combined therapy with aspirin and immobilized TRAIL and E-selectin. Mol. Pharm. doi: 10.1021/mp300073j. [Epub ahead of print].
79. Roberts, W. G., Whalen, P. M., Soderstrom, E., Moraski, G., Lyssikatos, J. P., Wang, H. F., Cooper, B., Baker, D. A., Savage, D., Dalvie, D., Atherton, J. A., Ralston, S., Szewc, R., Kath, J. C., Lin, J., Soderstrom, C., Tkalcevic, G., Cohen, B. D., Pollack, V., Barth, W., Hungerford, W., and Ung, E. (2005). Antiangiogenic and antitumor activity of a selective PDGFR tyrosine kinase inhibitor, CP-673, 451. Cancer Res. 65, 957-966.
80. Roland, C. L., Dineen, S. P., Toombs, J. E., Carbon, J. G., Smith, C. W., Brekken, R. A., and Barnett, C. C. Jr. (2010). Tumor-derived intercellular adhesion molecule-1 mediates tumor-associated leukocyte infiltration in orthotopic pancreatic xenografts. Exp. Biol. Med. (Maywood) 235, 263-270.
81. Rosette, C., Roth, R. B., Oeth, P., Braun, A., Kammerer, S., Ekblom, J., and Denissenko, M. F. (2005). Role of ICAM1 in invasion of human breast cancer cells. Carcinogenesis 26, 943-950.
82. Scher, H. I., Morris, M. J., Basch, E., and Heller, G. (2011). End points and outcomes in castration-resistant prostate cancer: from clinical trials to clinical practice. J. Clin. Oncol. 29, 3695-3704.
83. Shirota, K., Kato, Y., Irimura, T., Kondo, H., and Sugiyama, Y. (2001). Anti-metastatic effect of the sialyl Lewis-X analog GSC-150 on the human colon carcinoma derived cell line KM12-HX in the mouse. Biol. Pharm. Bull. 24, 316-319.
84. Sierko, E., and Wojtukiewicz, M. Z. (2007). Inhibition of platelet function: does it offer a chance of better cancer progression control? Semin. Thromb. Hemost. 33, 712-721.
85. Slattery, M. J., and Dong, C. (2003). Neutrophils influence melanoma adhesion and migration under flow conditions. Int. J. Cancer 106, 713-722.
86. Stevenson, J. L., Choi, S. H., and Varki, A. (2005). Differential metastasis inhibition by clinically relevant levels of heparins-correlation with selectin inhibition, not antithrombotic activity. Clin. Cancer Res. 11, 7003-7011.
87. Theodoropoulos, P. A., Polioudaki, H., Agelaki, S., Kallergi, G., Saridaki, Z., Mavroudis, D., and Georgoulias, V. (2010). Circulating tumor cells with a putative stem cell phenotype in peripheral blood of patients with breast cancer. Cancer Lett. 288, 99-106.
88. Toloudi, M., Apostolou, P., Chatziioannou, M., and Papasotiriou, I. (2011). Correlation between cancer stem cells and circulating tumor cells and their value. Case Rep. Oncol. 4, 44-54.
89. Toso, C., Mentha, G., and Majno, P. (2011). Liver transplantation for hepatocellular carcinoma: five steps to prevent recurrence. Am. J. Transplant. 11, 2031-2035.
90. Valastyan, S., and Weinberg, R. A. (2011). Tumor metastasis: molecular insights and evolving paradigms. Cell 147, 275-292.
91. Vermeulen, L., De Sousa E Melo, F., Richel, D. J., and Medema, J. P. (2012). The developing cancer stem-cell model: clinical challenges and opportunities. Lancet Oncol. 13, e83-e89.
92. Wang, J., Cao, M. G., You, C. Z., Wang, C. L., Liu, S. L., Kai, C., and Dou, J. (2012). A preliminary investigation of the relationship between circulating tumor cells and cancer stem cells in patients with breast cancer. Cell. Mol. Biol. (Noisy-le-grand) 58(Suppl.), OL1641-OL1645.
93. Wang, S. (2008). The promise of cancer therapeutics targeting the TNF-related apoptosis-inducing ligand and TRAIL receptor pathway. Oncogene 27, 6207-6215.
94. Wang, Q. Y., Wu, S. L., Chen, J. H., Liu, F., and Chen, H. L. (2003). Expressions of Lewis antigens in human non-small cell pulmonary cancer and primary liver cancer with different pathological conditions. J. Exp. Clin. Cancer Res. 22, 431-440.
95. Wang, Y., Klijn, J. G., Zhang, Y., Sieuwerts, A. M., Look, M. P., Yang, F., Talantov, D., Timmermans, M., Meijer-Van Gelder, M. E., Yu, J., Jatkoe, T., Berns, E. M., Atkins, D., and Foekens, J. A. (2005). Gene-expression profiles to predict distant metastasis of lymph-node-negative primary breast cancer. Lancet 365, 671-679.
96. Wei, M., Tai, G., Gao, Y., Li, N., Huang, B., Zhou, Y., Hao, S., and Zeng, X. (2004). Modified heparin inhibits P-selectin-mediated cell adhesion of human colon carcinoma cells to immobilized platelets under dynamic flow conditions. J. Biol. Chem. 279, 29202-29210.
97. Weninger, W., Ulfman, L. H., Cheng, G., Souchkova, N., Quackenbush, E. J., Lowe, J. B., and Von Andrian, U. H. (2000). Specialized contributions by alpha(1,3)-fucosyltransferase-IV and FucT-VII during leukocyte rolling in dermal microvessels. Immunity 12, 665-676.
98. Wenzel, J., Zeisig, R., Haider, W., Habedank, S., and Fichtner, I. (2010). Inhibition of pulmonary metastasis in a human MT3 breast cancer xenograft model by dual liposomes preventing intravasal fibrin clot formation. Breast Cancer Res. Treat. 121, 13-22.
99. Weroha, S. J., and Haluska, P. (2008). IGF-1 receptor inhibitors in clinical trials-early lessons. J. Mammary Gland Biol. Neoplasia 13, 471-483.
100. Wild, M. K., Huang, M. C., Schulze-Horsel, U., Van Der Merwe, P. A., and Vestweber, D. (2001). Affinity, kinetics, and thermodynamics of E-selectin binding to E-selectin ligand-1. J. Biol. Chem. 276, 31602-31612.
101. Wu, Q. D., Wang, J. H., Condron, C., Bouchier-Hayes, D., and Redmond, H. P. (2001). Human neutrophils facilitate tumor cell transendothelial migration. Am. J. Physiol. Cell Physiol. 280, C814-C822.
102. Yalcin, S., Kilickap, S., Portakal, O., Arslan, C., Hascelik, G., and Kutluk, T. (2010). Determination of circulating tumor cells for detection of colorectal cancer progression or recurrence. Hepatogastroenterology 57, 1395-1398.
103. Yang, X. S., Liu, S., Liu, Y. J., Liu, J. W., Liu, T. J., Wang, X. Q., and Yan, Q. (2010). Overexpression of fucosyltransferase IV promotes A431 cell proliferation through activating MAPK and PI3K/Akt signaling pathways. J. Cell. Physiol. 225, 612-619.
104. Yin, X., Rana, K., Ponmudi, V., and King, M. R. (2010). Knockdown of fucosyltransferase III disrupts the adhesion of circulating cancer cells to E-selectin without affecting hematopoietic cell adhesion. Carbohydr. Res. 345, 2334-2342.
105. Zacharowski, K., Otto, M., Hafner, G., Marsh, H. C. Jr., and Thiemermann, C. (1999). Reduction of myocardial infarct size with sCR1sLe(x), an alternatively glycosylated form of human soluble complement receptor type 1 (sCR1), possessing sialyl Lewis x. Br. J. Pharmacol. 128, 945-952.