Deficiency in surface expression of E-selectin ligand promotes lung colonization in a mouse model of breast cancer

International Journal of Cancer

Volumn 117, Issue 3, 2005, Pages 398-408

  Monzavi Karbassi, Behjatolah ^a   Whitehead, Tracy L ^a   Jousheghany, Fariba ^a   Artaud, Cecile ^a   Hennings, Leah ^a   Shaaf, Saeid ^a   Slaughter, Aubrey ^a   Korourian, Soheila ^a   Kelly, Thomas ^a   Blaszczyk Thurin, Magdalena ^b   Kieber Emmons, Thomas ^a  

^a UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

4T1 cells; Breast cancer; Metastasis; Sialyl Lewisx antigen

Indexed keywords

ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; LIGAND; OLIGOSACCHARIDE; PADGEM PROTEIN; SIALYL LEWIS A ANTIGEN; SIALYL LEWIS X ANTIGEN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CARCINOMA; CANCER CELL CULTURE; CANCER GROWTH; CANCER MODEL; CARCINOMA CELL; CELL ADHESION; CELL ASSAY; CELL MOTILITY; CELL STRUCTURE; CELL SURFACE; CONTROLLED STUDY; FEMALE; LUNG METASTASIS; MOUSE; MOUSE STRAIN; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; SUBCUTANEOUS FAT; TUMOR GROWTH; VASCULAR ENDOTHELIUM; WOUND SCRATCH ASSAY;

ANIMALS; E-SELECTIN; FEMALE; LIGANDS; LUNG NEOPLASMS; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; MICE, INBRED BALB C; NEOPLASM METASTASIS; OLIGOSACCHARIDES;

EID: 26444515544     PISSN: 00207136     EISSN: None     Source Type: Journal    
DOI: 10.1002/ijc.21192     Document Type: Article

References (69)

1. Liotta LA, Steeg PS, Stetler-Stevenson WG. Cancer metastasis and angiogenesis: an imbalance of positive and negative regulation. Cell 1991;64:327-36.
2. Fidler IJ. The pathogenesis of cancer metastasis: the "seed and soil" hypothesis revisited. Nature Rev Cancer 2003;3:453-8.
3. Dennis JW, Granovsky M, Warren CE. Protein glycosylation in development and disease. Bioessays 1999;21:412-21.
4. Granovsky M, Fata J, Pawling J, Muller WJ, Khokha R, Dennis JW. Suppression of tumor growth and metastasis in Mgat5-deficient mice. Nat Med 2000;6:306-12.
5. Nelson RM, Venot A, Bevilacqua MP, Linhardt RJ, Stamenkovic I. Carbohydrate-protein interactions in vascular biology. Annu Rev Cell Dev Biol 1995;11:601-31.
6. a in lesions of breast carcinoma. Int J Cancer 1997;74:296-300.
7. Kim YJ, Varki A. Perspectives on the significance of altered glycosylation of glycoproteins in cancer. Glycoconj J 1997;14:569-76.
8. x oligosaccharides in tumor metastasis and rejection by natural killer cells. EMBO J 1999;18:1516-25.
9. Kim YJ, Borsig L, Varki NM, Varki A. P-selectin deficiency attenuates tumor growth and metastasis. Proc Natl Acad Sci USA 1998;95:9325-30.
10. Majuri ML, Niemela R, Tiisala S, Renkonen O, Renkonen R. Expression and function of α2, 3-sialyl- and α1,3/1,4-fucosyltransferases in colon adenocarcinoma cell lines: role in synthesis of E-selectin counter-receptors. Int J Cancer 1995;63:551-9.
11. McEver RP, Moore KL, Cummings RD. Leukocyte trafficking mediated by selectin-carbohydrate interactions. J Biol Chem 1995;270:11025-8.
12. Kansas GS. Selectins and their ligands: current concepts and controversies. Blood 1996;88:3259-87.
13. Varki A. Selectin ligands: will the real ones please stand up? J Clin Invest 1997;100:S31-5.
14. Lowe JB, Ward PA. Therapeutic inhibition of carbohydrate-protein interactions in vivo. J Clin Invest 1997;100:S47-51.
15. McEver RP, Cummings RD. Role of PSGL-1 binding to selectins in leukocyte recruitment. J Clin Invest 1997;100:S97-103.
16. Kannagi R, Izawa M, Koike T, Miyazaki K, Kimura N. Carbohydrate-mediated cell adhesion in cancer metastasis and angiogenesis. Cancer Sci 2004;95:377-84.
17. a and E-selectin in metastasis assessed with peptide antagonist. Peptides 2002;23:999-1010.
18. x-dependent lung colonization of B16 melanoma cells through a selectin-like endothelial receptor distinct from E- or P-selectin. Cancer Res 2002;62:4194-8.
19. a antigen. Int J Cancer 1996;69:290-4.
20. x/a underexpression and E-cadherin overexpression in the lymphovascular embolus of inflammatory breast carcinoma. Am J Pathol 2002;161:619-28.
21. Miller FR, Miller BE, Heppner GH. Characterization of metastatic heterogeneity among subpopulations of a single mouse mammary tumor: heterogeneity in phenotypic stability. Invasion Metastasis 1983;3:22-31.
22. Pulaski BA, Ostrand-Rosenberg S. Reduction of established spontaneous mammary carcinoma metastases following immunotherapy with major histocompatibility complex class II and B7.1 cell-based tumor vaccines. Cancer Res 1998;58:1486-93.
23. Parviz M, Chin CS, Graham LJ, Miller C, Lee C, George K, Bear HD. Successful adoptive immunotherapy with vaccine-sensitized T cells, despite no effect with vaccination alone in a weakly immunogenic tumor model. Cancer Immunol Immunother 2003;52:739-50.
24. x, α1,3 fucosyltransferase VII, and metastatic potential. J Cancer Res Clin Oncol 2002;128:189-96.
25. Guo P, Zhang Y, Zhang XY, Chen HL, Wang H, Narimatsu H. Analysis of Lewis antigens on cell surface and α1-, 3-fucosyltransferase subtypes in H7721 human hepatocarcinoma cells. J Exp Clin Cancer Res 2003;22:135-9.
26. x antigens and their E-selectin-dependent adhesion. Clin Exp Metastasis 1998;16:569-76.
27. x-dependent lung colonization of tumor cells. Cancer Res 2000;60:450-6.
28. Aslakson CJ, Miller FR. Selective events in the metastatic process defined by analysis of the sequential dissemination of subpopulations of a mouse mammary tumor. Cancer Res 1992;52:1399-405.
29. Pulaski BA, Ostrand-Rosenberg S. Mouse 4T1 breast tumor model. In: Coligan JE, Kruisbeek AM, Margulies DH, Shevach E, Strober W, eds.Current protocols in immunology, vol. 3. New York: John Wiley & Sons, 2000.20.2.1-20.2.16.
30. Monzavi-Karbassi B, Cunto-Amesty G, Luo P, Shamloo S, Blaszcyk-Thurin M, Kieber-Emmons T. Immunization with a carbohydrate mimicking peptide augments tumor-specific cellular responses. Int Immunol 2001;13:1361-71.
31. x to adhesion of human cancer cells to vascular endothelium. Cancer Res 1993;53:354-61.
32. x-deficient variant of HL60 cells exhibits high levels of adhesion to vascular selectins: further evidence that HECA-452 and CSLEX1 monoclonal antibody epitopes are not essential for high avidity binding to vascular selectins. J Immunol 1998;160:5122-9.
33. Wagers AJ, Stoolman LM, Kannagi R, Craig R, Kansas GS. Expression of leukocyte fucosyltransferases regulates binding to E-selectin: relationship to previously implicated carbohydrate epitopes. J Immunol 1997;159:1917-29.
34. Hanai N, Shitara K, Yoshida H. Generation of monoclonal antibodies against human lung squamous cell carcinoma and adenocarcinoma using mice rendered tolerant to normal human lung. Cancer Res 1986;46:4438-43.
35. x glycolipids in a gastric cancer cell line and normal stomach tissue Anticancer Res 1993;13:1277-82.
36. Hakomori S. Tumor malignancy defined by aberrant glycosylation and sphingo(glyco)lipid metabolism. Cancer Res 1996;56:5309-18.
37. Hakomori S. Glycosylation defining cancer malignancy: new wine in an old bottle. Proc Natl Acad Sci USA 2002;99:10231-3.
38. Dennis JW, Laferte S, Waghome C, Breitman ML, Kerbel RS. β1-6 branching of Asn-linked oligosaccharides is directly associated with metastasis. Science 1987;236:582-5.
39. Yagel S, Feinmesser R, Waghorne C, Lala PK, Breitman ML, Dennis JW. Evidence that β1-6 branched Asn-linked oligosaccharides on metastatic tumor cells facilitate invasion of basement membranes. Int J Cancer 1989;44:685-90.
40. Seberger PJ, Chaney WG. Control of metastasis by Asn-linked, β1-6 branched oligosaccharides in mouse mammary cancer cells. Glycobiology 1999;9:235-41.
41. Nemoto-Sasaki Y, Mitsuki M, Morimoto-Tomita M, Maeda A, Tsuiji M, Irimura T. Correlation between the sialylation of cell surface Thomsen-Friedenreich antigen and the metastatic potential of colon carcinoma cells in a mouse model. Glycoconj J 2001;18:895-906.
42. x-related carbohydrate antigens with distinct properties in cell adhesion. Biochem Biophys Res Commun 2003;303:896-901.
43. x moiety on rat polymorphonuclear leukocytes responsible for binding to rat E-selectin. Biochem Biophys Res Commun 1995;215:547-54.
44. x, α1,3-fucosyltransferase VII, and metastatic potential in a human hepatocarcinoma cell line. Eur J Biochem 2001;268:3501-12.
45. Wong CW, Song C, Grimes MM, Fu W, Dewhirst MW, Muschel RJ, Al-Mehdi AB. Intravascular location of breast cancer cells after spontaneous metastasis to the lung. Am J Pathol 2002;161:749-53.
46. x/a-deficient MUC1 in the passive dissemination of tumor emboli in inflammatory breast carcinoma. Oncogene 2002;21:3631-43.
47. Behrens J. The role of cell adhesion molecules in cancer invasion and metastasis. Breast Cancer Res Treat 1993;24:175-84.
48. Cavallaro U, Christofori G. Cell adhesion in tumor invasion and metastasis: loss of the glue is not enough. Biochim Biophys Acta 2001;1552:39-45.
49. Hirohashi S, Kanai Y. Cell adhesion system and human cancer morphogenesis. Cancer Sci 2003;94:575-81.
50. Wyckoff JB, Jones JG, Condeelis JS, Segall JE. A critical step in metastasis: in vivo analysis of intravasation at the primary tumor. Cancer Res 2000;60:2504-11.
51. Yoshimura M, Nishikawa A, Ihara Y, Taniguchi S, Taniguchi N. Suppression of lung metastasis of B16 mouse melanoma by N-acetylglucosaminyltransferase III gene transfection. Proc Natl Acad Sci USA 1995;92:8754-8.
52. Yoshimura M, Ihara Y, Matsuzawa Y, Taniguchi N. Aberrant glycosylation of E-cadherin enhances cell-cell binding to suppress metastasis. J Biol Chem 1996;271:13811-5.
53. 1 integrin and vascular laminin-5 mediate pulmonary arrest and metastasis. J Cell Biol 2004;164:935-41.
54. 1 changes with melanoma progression. Biochim Biophys Acta 2003;1643:113-23.
55. 1 reduces ligand binding and down-regulates cell adhesion and cell migration. J Biol Chem 2004;279:19747-54.
56. y, CA19-9, and CSLEX1 in early cancer, intestinal metaplasia, and uninvolved mucosa of the stomach. Am J Clin Pathol 1992;98:67-75.
57. x antigen defined by MAb AM-3 is an independent prognostic marker in colorectal carcinoma patients. Int J Cancer 2000;88:281-6.
58. x antigen as a prognostic factor in patients with stage O, I, and II gastric cancer. Cancer Lett 2002;175:213-21.
59. Nakagoe T, Fukushima K, Itoyanagi N, Ikuta Y, Oka T, Nagayasu T, Ayabe H, Hara S, Ishikawa H, Minami H. Expression of ABH/Lewis-related antigens as prognostic factors in patients with breast cancer. J Cancer Res Clin Oncol 2002;128:257-64.
60. x antigen in breast cancer. Oncology 1998;55:357-62.
61. Sumikura S, Ishigami S, Natsugoe S, Miyazono F, Tokuda K, Nakajo A, Okumura H, Matsumoto M, Hokita S, Aikou T. Disseminated cancer cells in the blood and expression of sialylated antigen in gastric cancer. Cancer Lett 2003;200:77-83.
62. Friederichs J, Zeller Y, Hafezi-Moghadam A, Grone HJ, Ley K, Altevogt P. The CD24/P-selectin binding pathway initiates lung arrest of human A125 adenocarcinoma cells. Cancer Res 2000;60:6714-22.
63. Aigner S, Ramos CL, Hafezi-Moghadam A, Lawrence MB, Friederichs J, Altevogt P, Ley K. CD24 mediates rolling of breast carcinoma cells on P-selectin. FASEB J 1998;12:1241-51.
64. Aigner S, Sthoeger ZM, Fogel M, Weber E, Zarn J, Ruppert M, Zeller Y, Vestweber D, Stahel R, Sammar M, Altevogt P. CD24, a mucin-type glycoprotein, is a ligand for P-selectin on human tumor cells. Blood 1997;89:3385-95.
65. Kristiansen G, Winzer KJ, Mayordomo E, Bellach J, Schluns K, Denkert C, Dahl E, Pilarsky C, Altevogt P, Guski H, Dietel M. CD24 expression is a new prognostic marker in breast cancer. Clin Cancer Res 2003;9:4906-13.
66. Zijlstra A, Mellor R, Panzarella G, Aimes RT, Hooper JD, Marchenko ND, Quigley JP. A quantitative analysis of rate-limiting steps in the metastatic cascade using human-specific real-time polymerase chain reaction. Cancer Res 2002;62:7083-92.
67. Mannori G, Crottet P, Cecconi O, Hanasaki K, Aruffo A, Nelson RM, Varki A, Bevilacqua MP. Differential colon cancer cell adhesion to E-, P-, and L-selectin: role of mucin-type glycoproteins. Cancer Res 1995;55:4425-31.
68. Stone JP, Wagner DD. P-selectin mediates adhesion of platelets to neuroblastoma and small cell lung cancer. J Clin Invest 1993;92:804-13.
69. Varki NM, Varki A. Heparin inhibition of selectin-mediated interactions during the hematogenous phase of carcinoma metastasis: rationale for clinical studies in humans. Semin Thromb Hemost 2002;28:53-66.