Selectin-mucin interactions as a probable molecular explanation for the association of Trousseau syndrome with mucinous adenocarcinomas

Journal of Clinical Investigation

Volumn 112, Issue 6, 2003, Pages 853-862

  Wahrenbrock, Mark ^a,c   Borsig, Lubor ^a,b   Le, Dzung ^c   Varki, Nissi ^a,c   Varki, Ajit ^a,b,d  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIVITAMIN K; HEPARIN; L SELECTIN; MUCIN; PADGEM PROTEIN; RECOMBINANT HIRUDIN; SELECTIN; THROMBIN; THROMBOPLASTIN; TUMOR PROTEIN; ANTIFIBRINOLYTIC AGENT; FIBRINOLYTIC AGENT; VITAMIN K GROUP;

ADENOCARCINOMA; ANIMAL MODEL; ARTICLE; BLOOD; CONTROLLED STUDY; HUMAN; HUMAN CELL; MICROANGIOPATHY; MICROTHROMBUS; MOLECULAR RECOGNITION; MOUSE; MUCINOUS ADENOCARCINOMA; NONHUMAN; OCCULT CANCER; PRIORITY JOURNAL; PROTEIN PURIFICATION; THROMBOCYTE ACTIVATION; THROMBOCYTE AGGREGATION; THROMBOCYTE RICH PLASMA; THROMBOPHLEBITIS; TROUSSEAU SYNDROME; ANIMAL; C57BL MOUSE; CANCER TRANSPLANTATION; CELL CULTURE; CHEMISTRY; COLLOID CARCINOMA; COMORBIDITY; CYTOLOGY; GENETICS; ISOLATION AND PURIFICATION; LUNG; METABOLISM; PARANEOPLASTIC SYNDROME; SYNDROME; THROMBOCYTE; THROMBOSIS; XENOGRAFT;

ADENOCARCINOMA, MUCINOUS; ANIMALS; ANTIFIBRINOLYTIC AGENTS; BLOOD PLATELETS; COMORBIDITY; FIBRINOLYTIC AGENTS; HEPARIN; HUMANS; L-SELECTIN; LUNG; MICE; MICE, INBRED C57BL; MUCINS; NEOPLASM TRANSPLANTATION; P-SELECTIN; PARANEOPLASTIC SYNDROMES; PLATELET ACTIVATION; SYNDROME; THROMBIN; THROMBOPHLEBITIS; THROMBOSIS; TRANSPLANTATION, HETEROLOGOUS; TUMOR CELLS, CULTURED; VITAMIN K;

EID: 0142155574     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI200318882     Document Type: Article

References (89)

1. Trousseau, A. 1868. Lectures on clinical medicine, delivered at the Hotel-Dieu, Paris. P.V. Bazire, editor and translator. The New Sydenham Society Publications. London, United Kingdom. 55:281-332.
2. Samuels, M.A., King, M.E., and Balis, U. 2002. Case records of the Massachusetts General Hospital. Weekly clinicopathological exercises. Case 31-2002. A 61-year-old man with headache and multiple infarcts. N. Engl. J. Med. 347:1187-1194.
3. Sack, G.H., Jr., Levin, J., and Bell, W.R. 1977. Trousseau's syndrome and other manifestations of chronic disseminated coagulopathy in patients with neoplasms: clinical, pathophysiologic, and rherapeutic features. Medicine (Baltimore). 56:1-37.
4. Callander, N., and Rapaport, S.I. 1993. Trousseau's syndrome. West. J. Med. 158:364-371.
5. Rigdon, E.E. 2000. Trousseau's syndrome and acute arterial thrombosis. Cardiovasc. Surg. 8:214-218.
6. Arkel, Y.S. 2000. Thrombosis and cancer. Semin. Oncol. 27:362-374.
7. Rickles, F.R., and Falanga, A. 2001. Molecular basis for the relationship between thrombosis and cancer. Thromb. Res. 102:V215-V224.
8. Gale, A.J., and Gordon, S.G. 2001. Update on tumor cell procoagulant factors. Acta Haematol. 106:25-32.
9. Lee, A. 2002. Cancer and thromboembolic disease: pathogenic mechanisms. Cancer Treat. Rev. 28:137-140.
10. Lip, G.Y., Chin, B.S., and Blann, A.D. 2002. Cancer and the prothrombotic state. Lancet Oncol. 3:27-34.
11. Gordon, S.G. 1992. Cancer cell procoagulants and their implications. Hematol. Oncol. Clin. North Am. 6:1359-1374.
12. Bani, M.R., et al. 1992. Blood coagulation changes in nude mice bearing human colon carcinomas. Int. J. Cancer. 50:75-79.
13. Mielicki, W.P., Tenderenda, M., Rutkowski, P., and Chojnowski, K. 1999. Activation of blood coagulation and the activity of cancer procoagulant (EC 3.4.22.26) in breast cancer patients. Cancer Lett. 146:61-66.
14. Callander, N.S., Varki, N., and Rao, L.V. 1992. Immunohistochemical identification of tissue factor in solid tumors. Cancer. 70:1194-1201.
15. Zacharski, L.R., Schned, A.R., and Sorenson, G.D. 1983. Occurrence of fibrin and tissue factor antigen in human small cell carcinoma of the lung. Cancer Res. 43:3963-3968.
16. Kakkar, A.K., DeRuvo, N., Chinswangwatanakul, V., Tebbutt, S., and Williamson, R.C. 1995. Extrinsic-pathway activation in cancer with high factor VIIa and tissue factor. Lancet. 346:1004-1005.
17. Bell, W.R., Starksen N.F., Tong, S., and Porterfield, J.K. 1985. Trousseau's syndrome. Devastating coagulopathy in the absence of heparin. Am. J. Med. 79:423-430.
18. Krauth, D., Holden, A., Knapic, N., Liepman, M., and Ansell, J. 1987. Safety and efficacy of long-term oral anticoagulation in cancer patients. Cancer. 59:983-985.
19. Walsh-McMonagle, D., and Green, D. 1997. Low-molecular-weight heparin in the management of Trousseau's syndrome. Cancer. 80:649-655.
20. Meyer, G., et al. 2002. Comparison of low-molecular-weight heparin and warfarin for the secondary prevention of venous thromboembolism in patients with cancer: a randomized controlled study. Arch. Intern. Med. 162:1729-1735.
21. Levine, M. 2002. Managing thromboembotic disease in the cancer patient: efficacy and safety of antithrombotic treatment options in patients with cancer. Cancer Treat. Rev. 28:145-149.
22. Carraway, K.L., Fregien, N., Carraway, K. L., III, and Carraway, C.A. 1992. Tumor sialomucin complexes as tumor antigens and modulators of cellular interactions and proliferation. J. Cell Sci. 103:299-307.
23. Kim, Y.S., Gum, J., and Brockhause, I. 1996. Mucin glycoproteins in neoplasia. Glycoconj. J. 13:693-707.
24. Perez-Vilar, J., and Hill, R.L. 1999. The structure and assembly of secreted mucins. J. Biol. Chem. 274:31751-31754.
25. Hanisch, F.G., and Muller, S. 2000. MUC1: the polymorphic appearance of human mucin. Glycobiology. 10:439-449.
26. Fukuda, M., and Tsuboi, S.T. 1999. Mucin-type O-glycans and leukosialin. Biochim. Biophys. Acta. 1455:205-217.
27. Nakamori, S., Ota, D.M., Cleary, K.R., Shirotani, K., and Irimura, T. 1994. MUC1 mucin expression as a marker of progression and metastasis of human colorectal carcinoma. Gastroenterology. 106:353-361.
28. Perrais, M., Pigny, P., Copin, M.C., Aubert, J.P., and Van, S.I. 2002. Induction of MUC2 and MUC5AC mucins by factors of the epidermal growth factor (EGF) family is mediated by EGF receptor/Ras/Raf/extracellular signal-regulated kinase cascade and Sp1. J. Biol. Chem. 277:32258-32267.
29. Yin, B.W., Dnistrian, T.A., and Lloyd, K.O. 2002. Ovarian cancer antigen CA125 is encoded by the MUC16 mucin gene. Int. J. Cancer. 98:737-740.
30. McCool, D.J., Forstner, J.F., and Forsmer, G.G. 1995. Regulated and unregulated pathways for MUC2 mucin secretion in human colonic LS180 adenocarcinoma cells are distinct. Biochem. J. 312:125-133.
31. Enss, M.L., et al. 2000. Proinflammatory cytokines trigger MUC gene expression and mucin release in the intestinal cancer cell line LS180. Inflamm. Res. 49:162-169.
32. Komatsu, M., Arango, M.E., and Carraway, K.L. 2002. Synthesis and secretion of Muc4/sialomucin complex: implication of intracellular proteolysis. Biochem. J. 368:41-48.
33. Kim, Y.J., Borsig, L., Han, H.L., Varki, N.M., and Varki, A. 1999. Distinct selectin ligands on colon carcinoma mucins can mediate pathological interactions among platelets, leukocytes, and endothelium. Am. J. Pathol. 155:461-472.
34. Kim, Y.J., Borsig, L., Varki, N.M., and Varki, A. 1998. P-selectin deficiency attenuates tumor growth and metastasis. Proc. Natl. Acad. Sci. U. S. A. 95:9325-9330.
35. Borsig, L., et al. 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.
36. Borsig, L., Wong, R., Hynes, R.O., Varki, N.M., and Varki, A. 2002. Synergistic effects of L- and P-selectin in facilitating tumor metastasis can involve non-mucin ligands and implicate leukocytes as enhancers of metastasis. Proc. Natl. Acad. Sci. U. S. A. 99:2193-2198.
37. Singhal, A.K. et al. 1990. Profiles of Lewisx-containing glycoproteins and glycolipids in sera of patients with adenocarcinoma. Cancer Res. 50:1375-1380.
38. Kawa, S., et al. 1991. Preparation of pancreatic cancer-associated mucin expressing CA 19-9, CA50, Span-1, SSEA-1, and Dupan-2. Scand. J. Gastroenterol. 26:981-992.
39. Hanski, C., et al. 1995. Characterization of the major sialyl-Lex-positive mucins present in colon, colon carcinoma, and sera of patients with colorectal cancer. Cancer Res. 55:928-933.
40. Zhang, K, Baeckström, D., Brevinge, H., and Hansson, G.C. 1996. Secreted MUC1 mucins lacking their cytoplasmic part and carrying sialyl-Lewis a and x epitopes from a tumor cell line and sera of colon carcinoma patients can inhibit HL-60 leukocyte adhesion to E-selectin-expressing endothelial cells. J. Cell Biochem. 60:538-549.
41. Yiannakou, J.Y., Newland, P., Calder, F., Kingsnorth, A.N., and Rhodes, J.M. 1997. Prospective study of CAM 17.1/WGA mucin assay for serological diagnosis of pancreatic cancer. Lancet. 349:389-392.
42. Rhodes, J.M. 1999. Usefulness of novel tumour markers. Ann. Oncol. 4(Suppl. 10):118-121.
43. Yin, B.W., and Lloyd, K.O. 2001. Molecular cloning of the CA125 ovarian cancer antigen: identification as a new mucin, MUC16. J. Biol. Chem. 276:27371-27375.
44. Pineo, G.F., Regoeczi, E., Hatton, M.W., and Brain, M.C. 1973. The activation of coagulation by extracts of mucus: a possible pathway of intravascular coagulation accompanying adenocarcinomas. J. Lab. Clin. Med. 82:255-266.
45. Pineo, G.F., et al. 1974. Tumors, mucus production, and hypercoagulability. Ann. N. Y. Acad. Sci. 230:262-270.
46. Hemmerich, S., and Rosen, S.D. 2000. Carbohydrate sulfotransferases in lymphocyte homing. Glycobiology. 10:849-856.
47. Furie, B., Furie, B.C., and Flaumenhaf, R. 2001. A journey with platelet P-selectin: the molecular basis of granule secretion, signalling and cell adhesion. Thromb. Haemost. 86:214-221.
48. Tsuboi, S., and Fukuda, M. 2001. Roles of O-linked oligosaccharides in immune responses. Bioessays. 23:46-53.
49. McEver, R.P. 2002. Selectins: lectins that initiate cell adhesion under flow. Curr Opin. Cell Biol. 14:581-586.
50. Varki, A. 1994. Selectin ligands. Proc. Natl. Acad. Sci. U. S. A. 91:7390-7397.
51. Kansas, G.S. 1996. Setectins and their ligands: current concepts and controversies. Blood. 88:3259-3287.
52. Epperson, T.R., Patel, K.D., McEver, R.P., and Cummings, R.D. 2000. Noncovalent association of P-selectin glycoprotein ligand-1 and minimal determinants for binding to P-selectin. J. Biol. Chem. 275:7839-7853.
53. Leppänen, A., Penttilä, L., Renkonen, O., McEver, R.P., and Cummings, R.D. 2002. Glycosulfopeptides with O-glycans containing sialylated and polyfucosylated polylactosamine bind with low affinity to P-selectin. J. Biol. Chem. 277:39749-39759.
54. Nelson, R.M. et al. 1993. Heparin oligosaccharides bind L- and P-selectin and inhibit acute inflammation. Blood. 82:3253-3258.
55. Notgard-Sumnicht, K.E., Varki, N.M., and Varki, A. 1993. Calcium-dependent heparin-like ligands for L-selectin in nonlymphoid endothelial cells. Science. 261:480-483.
56. Notgard-Sumnicht, K.E., and Varki, A. 1995. Endothelial heparan sulfate proteoglycans that bind to L-selectin have glucosamine residues with unsubstituted amino groups. J. Biol. Chem. 270:12012-12024.
57. Koenig, A., Norgard-Sumnicht, K.E., 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.
58. Xie, X., et al. 2000. Inhibition selectin-mediated cell adhesion and prevention of acute inflammation by nonanticoagulant sulfated saccharides. Studies with carboxyl-reduced and sulfated heparin and with trestarin A sulfate. J. Biol. Chem. 275:34818-34825.
59. Wang, L., Brown, J.R., Varki, A., and Esko, J.D. 2002. Heparin's anti-inflammatory effects require glucosamine 6-O-sulfation and are mediated by blockade of L- and P-selectins. J. Clin. Invest. 110:127-136. doi:10.1172/JCI200214996.
60. Varki, N.M., and Varki, A. 2002. Heparin inhibition of selectin-mediated interactions during the hematogenous phase of carcinoma metastasis: Rationale for clinical studies in humans. Semin. Thromb. Hemost. 28:53-66.
61. Beeley, J.G. 1985. Glycoprotein and proteoglycan techniques. Elsevier. New York, New York, USA. 73-78.
62. Manzi, A.E., Diaz, S., and Varki, A 1990. High-pressure liquid chromatography of sialic acids on a pellicular resin anion-exchange column with pulsed amperometric detection: a comparison with six other systems. Anal. Biocbem. 188:20-32.
63. Corriveau, D., and Fritsma, J. 1988. Hemostasis and thrombosis in the clinical taboratory. 1988. J.P. Lippincott Co. Philadelphia, Pennsylvania, USA. 443 pp.
64. Lehr, H.A., Mankoff, D.A., Corwin, D., Santeusanio, G., and Gown, A.M. 1997. Application of Photoshop-based image analysis to quantification of hormone receptor expression in breast cancer. J. Histochem. Cytochem. 45:1559-1565.
65. Capon, C., et al. 1997. Sulfated Lewis X determinants as a major structural motif in glycans from LS174T-HM7 human colon carcinoma mucin. J. Biol. Chem. 272:31957-31968.
66. Moesby, L., Hansen, E.W., and Christensen, J.D. 2000. Endotoxin testing of proteins for parenteral administration using the Mono Mac 6 assay. J. Clin. Pharm. Ther. 25:283-289.
67. Tian, F., Appert, H.E., Myles, J., and Howard, J.M. 1992. Prognostic value of serum CA 19-9 levels in pancreatic adenocarcinoma. Ann. Surg. 215:350-355.
68. Harmenberg, U., Wahren, B., and Wiechel, K.L. 1988. Tumor markers carbohydrate antigens CA 19-9 and CA-50 and carcinoembryonic antigen in pancreatic cancer and benign diseases of the pancreatobiliary tract. Cancer Res. 48:1985-1988.
69. Bevilacqua, M.P., Stengelin, S., Gimbrone, M.A., and Seed, B. 1989. Endothelial leukocyte adhesion molecule 1: an inducible receptor for neutrophils related to complement regulatory proteins and lectins. Science. 243:1160-1165.
70. Li, N., et al. 2000. Platelet-leukocyce cross talk in whole blood. Arterioscler. Thromb. Vasc. Biol. 20:2702-2708.
71. Laudanna, C., et al. 1994. Sulfatides trigger increase of cytosolic free calcium and enhanced expression of tumor necrosis factor-alpha and interleukin-8 mRNA in human neutrophils. Evidence for a role of L-selectin as a signaling molecule. J. Biol. Chem. 269:4021-4026.
72. Waddell, T.K., Fialkow, L., Chan, C.K., Kishimoto, T.K., and Downey, G.P. 1994. Potentiation of the oxidative burst of human neutrophils. A signaling role for L-selectin. J. Biol. Chem. 269:18485-18491.
73. Waddell, T.K., Fialkow, L., Chan, C.K., Kishimoto, T.K., and Downey, G.P. 1995. Signaling functions of L-selectin. Enhancement of tyrosine phosphorylation and activation of MAP kinase. J. Biol. Chem. 270:15403-15411.
74. Brenner, B., et al. 1996. L-selectin activates the Ras pathway via the tyrosine kinase p561ck. Proc. Natl. Acad. Sci. U. S. A. 93:15376-15381.
75. Malhotra, R., and Bird, M.I. 1997. L-selectin: a novel receptor for lipopolysaccharide and its potential role in bacterial sepsis. Bioessays. 19:919-923.
76. Crockect-Torabi, E., Sulenbarger, B., Smith, C.W., and Fantone, J.C. 1995. Activation of human neutrophils through L-selectin and Mac-1 molecules. J. Immunol. 154:2291-2302.
77. Crockett-Torabi, E., and Fantone, J.C. 1997. L-selectin stimulation of canine neutrophil initiates calcium signal secondary to tyrosine kinase activation. Am. J. Physiol. Heart. Circ. Physiol. 272:H1302-H1308.
78. Simon, S.I., et al. 1999. Signaling functions of L-selectin in neutrophils: alterations in the cytoskeleton and colocalization with CD18. J. Immunol. 163:2891-2901.
79. Wize, J., Sopata, I., Smerdel, A., and Maslinski, S. 1998. Ligation of selectin L and integrin CD11b/CD18 (Mac-1) induces release of gelatinase B (MMP-9) from human neutrophils. Inflamm. Res. 47:325-327.
80. Smolen, J.E., et al. 2000. L-selectin signaling of neutrophil adhesion and degranulation involves p38 mitogen-activated protein kinase. J. Biol. Chem. 275:15876-15884.
81. Hidari, K.I., Weyrich, A.S., Zimmerman, G.A., and McEver, R.P. 1997. Engagement of P-selectin glycoprotein ligand-1 enhances tyrosine phosphorylation and activates mitogen-activated protein kinases in human neutrophils. J. Biol. Chem. 272:28750-28756.
82. Evangelista, V., et al. 1999. Platelet/polymorphonuclear leukocyte interaction: P-selectin triggers protein-tyrosine phosphorylation-dependent CD11b/CD18 adhesion: Role of PSGL-1 as a signaling molecule. Blood. 93:876-885.
83. Marcus, A.J. 1990. Stratton lecture 1989. Thrombosis and inflammation as multicellular processes: pathophysiologic significance of transcellular metabolism. Blood. 76:1903-1907.
84. De Gaetano, G., Cerletti, C., and Evangelista, V., 1999. Recent advances in platelet-polymorphonuclear leukocyte interaction. Haemostasis. 29:41-49.
85. Celi, A., et al. 1994. P-selectin induces the expression of tissue factor on monocytes. Proc. Natl. Acad. Sci. U. S. A. 91:8767-8771.
86. Giesen, P.L., and Nemerson, Y. 2000. Tissue factor on the loose. Semin. Thromb. Hemost. 26:379-384.
87. Osterud, B. 2001. The role of platelets in decrypting monocyte tissue factor. Semin. Hematol. 38(Suppl. 12):2-5.
88. Zimmerman, G.A., McIntyre, T.M., Prescott, S.M., and Stafforini, D.M. 2002. The platelet-activating factor signaling system and its regulators in syndromes of inflammation and thrombosis. Crit. Care Med. 30(Suppl.):S294-S301.
89. Merten, M., and Thiagarajan, P. 2001. Role for sulfatides in platelet aggregation. Circulation. 104:2955-2960.