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

Journal of Clinical Investigation

Volumn 101, Issue 4, 1998, Pages 877-889

  Koenig, Andrea ^b   Norgard Sumnicht, Karin ^b   Linhardt, Robert ^a   Varki, Ajit ^b  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Affinity chromatography; Endothelium; Proteoglycans; Selectin inhibition; Sulfate

Indexed keywords

CALCIUM; CARBOHYDRATE; CATION; DALTEPARIN; EDETIC ACID; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; ENOXAPARIN; GLYCOSAMINOGLYCAN; HEPARIN; L SELECTIN; LOW MOLECULAR WEIGHT HEPARIN; PADGEM PROTEIN; PROTEOHEPARAN SULFATE; SELECTIN;

AFFINITY CHROMATOGRAPHY; ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN INTERACTION;

EID: 0032519957     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI1509     Document Type: Article

References (109)

1. Bevilacqua, M.P., und R.M. Nelson. 1993. Selcclins. J. Clin. Invest. 91: 379-387.
2. Alhelda, S.M., C.W. Smith, and P.A. Ward. 1994. Adhesion molecules and inflammatory injury. FASEB (Fed. Am. Soc. Exp. Biol.) J. 8:504-512.
3. Varki, A. 1994. Seleetin ligands. Proc: Natl. Acad. Sci. USA. 91:7390-7397.
4. Furie, B., and B.C. Furic. 1995. The molecular basis of platelet and endothelial cell interaction with neulrophils and nionocytes: role of P-seleclin and the P-seleclin ligand, PSGL-1. Tliromh. Haemosiasis. 74:224-227.
5. Lasky, L.A. 1995. Selectin-carbohydrate interactions and the initiation of the inflammalory response. Annu. Rev. Biochem. 64:113-139.
6. McEver, R.P., K.L. Moore, and R.D. Cummings. 1995. Leukocyte trafficking mediated by selectin-carhohydrate interactions. J. Biol. Chem. 270 11025-11028.
7. Nelson, R.M., A. Venol, M.P. Bevilaequa, R.J. Linhardt, and I. Stamenkovic. 1995. Carbohydrate-protein interactions in vascular biology. Annn. Rev. Cell Biol. 11:601-631.
8. Springer, T.A. 1995. Traffic signals on endolhelium for lymphocyte recirculation and leukocyte emigration. Anna. Rev. Physiol. 57:827-872.
9. Tedder, T.F., D.A. Stecher, A. Chen, and P. Engel. 1995. The sclectins: vascular adhesion molecules. FASEB (Fed. Am. Soc. Exp. Biol.) J. 9:866-873.
10. Butcher, E.C., and L.J. Picker. 1996. Lymphocyte homing and homeostasis. Science. 272:60-66.
11. Crocker, P.R., and T. Feizi. 1996. Carbohydrate recognition systems: functional triads in cell-cell interactions. Curr. Opin. Struct. Biol. 6:679-691.
12. Hynes, R.O., and D.D. Wagner. 1996. Genetic manipulation of vascular adhesion molecules in mice. J. Clin. Invest. 98:2193-2195.
13. Kansas, G.S. 1996. Selectins and their ligands: current concepts and controversies. Blood. 88:3259-3287.
14. Rosen, S.D., and C.R. Bertozzi. 1996. Leukocyte adhesion: two sclectins converge on sulphate. Curr. Biol. 6:261-264.
15. Vestweher, D. 1996. Ligand-speciticity of the selectins. J. Cell. Biochem. 61:585-091.
16. Zimmcrman, G.A., T.M. McInlyre, and S.M. Prescott. 1996. Adhesion and signaling in vascular cell-cell interactions. J. Clin, Invest. 98:1699-1702.
17. Frenette, P.S., and D.D. Wagner. 1997. Insights into selectin function from knockout mice. Thromb. Haemostasis. 78:60-64.
18. Lowe, J.B., and P.A. Ward. 1997. Therapeutic inhibition of carbohydrate-protein interactions in vivo. J. Clin. Invest. 99:822-826.
19. Varki, A. 1997. Selectin ligands: will the real ones please stand up? J. Clin. Invest. 99:158-162.
20. McEver, R.P., and R.D. Cummings. 1997. Role of PSGL-1 binding to selectins in leukocyte recruitment. J. Clin. Invest. 100:485-492.
21. x antigen. is associated with metastatic potential of transitional cell carcinoma of the human urinary bladder. Biochem. Biophys. Res. Commun. 181:1218-1222.
22. Aruffo, A., M.T. Dictsch, H. Wan, K.E. Hellsiröm. and I. Hellström. 1992. Granule membrane protein 140 (GMP140) binds to carcinomas and carcinoma-derived cell lines. Proc: Natl. Acad. Sci. USA. 89:2292-2296.
23. x antigen correlates with poor survival in patients with colorectal carcinoma: clinicopaihological and immunohistochemical study. Cancer. 53:3632-3637.
24. Takada, A., K. Ohmori, T. Yoneda, K. Tsuyuoka, A. Hascgawa M. Kiso, and R. Kannagi. 1993. Contribution of carbohydrate antigens sialyl Lewis A and sialyl Lewis X to adhesion of human cancer cells to vascular endothelium. Cancer Res. 53:354-361.
25. Ogawa, J., H. Inoue, and S. Koide. 1996. Expression of α-1.3-Fucosyl-transferase type IV and VII genes is related to poor prognosis in lung cancer. Cancer Res: 56:325-329.
26. x in colorectal cancer metastasis. Dis. Colon Rectum. 40:420-431.
27. x. Science. 25(1:1130-1132.
28. x determinant on myeloid and tumor cells. Science. 250:1132-1135.
29. x. Proc. Natl. Acad. Sci. USA. 88:6224-6228.
30. x is recognized by the endothelial cell leukocyte adhesion molecule ELAM-1. J. Biol. Chem. 266:14869-14872.
31. Tyrrell, D., P. James, N. Rao, C. Foxall, S. Abbas, F. Dasgupta, M. Nashed, A. Hasegawa, M. Kiso, D. Asa, et al. 1991. Structural requirements for the carbohydrate ligand of E-selectin. Proc. Natl. Acad. Sci. USA. 88:10372-10376.
32. a. Biochem. Biophys. Res. Commun. 184:1048-1055.
33. x oligosaccharide. J. Cell Biol. 117:895-902.
34. Larkin, M., T.J. Ahern, M.S. Stoll, M. Shaffcr, D. Sako, J. O'Brien, C.-T. Yuen, A.M. Lawson, R.A. Childs, K.M. Barone. et al. 1992. Spectrum of sialylated and nonsialylated tuco-oligosaccharides bound by the endothelial-leukocytc adhesion molecule E-selectin. Dependence of the carbohydrate binding activity on E-selectin density. J. Biol. Chem. 267:13661-13668.
35. Philips, M.L., B.R. Schwanz, A. Etzioni, R. Bayer, H.D. Ochs, J.C. Paulson, and J.M. Harlan. 1995. Neutrophil adhesion in leukocyte adhesion deficiency syndrome type 2. J. Clin. Invest. 96:2898-2906.
36. Maly, P., A.D. Thall, B. Petrvniak, G.E. Rogers. P.L. Smith, R.M. Marks, R.J. Kelly, K.M. Gersten, G.Y. Cheng, T.L. Saunders, et al. 1996. The α(1,3)Fucosyltransferase Fuc-TVII controls leukocyte trafficking through an essential role in L-, E-, and P-selectin ligand biosynthesis. Cell. 86:643-653.
37. Norgard, K.E., K.L. Moore, S. Diaz, N.L. Stults, S. Ushiyama, R.P. McEver, R.D. Cummings, and A, Varki. 1993. Characterization of a specific ligand for P-selectin on myeloid cells. A minor glycoprotein with sialylaled O-linked oligosaccharides. J. Biol. Chem. 268:12764-12774.
38. Sako, D., X.-J. Chang, K.M. Barone, G. Vachino, H.M. While, G. Shaw, G.M. Veldman, K.M. Bean, T.J, Ahern, B. Furie, et al. 1993. Expression cloning of a functional glycoprotein ligand for P-selectin. Cell. 75:1179-1186.
39. Weyrich, A.S., X. Ma, D.J. Lefer, K.H. Albertine, and A.M. Lefer. 1993. In vivo neutralization of P-selectin protects feline heart and endothelium in myocardial ischemia and reperfusion injury. J. Clin. Invest. 91:2620-2629.
40. Ridings, P.C., S. Holloway, G.L. Bloomfield, M.L. Phillips, B.J. Fisher, C.R. Blocher, H.J. Sugerman, and A.A. Fowler, III. 1997. Protective role of synthetic sialylated oligosaccharide in sepsis-induced acute lung injury. J. Appl. Physiol. 82:644-651.
41. Bevilacqua, M.P., R.M. Nelson, G. Mannori, and O. Cecconi. 1994. Endothelial-leukocyte adhesion molecules in human disease. Annn. Rev. Med. 45: 361-378.
42. x-containing oligosaccharide exerts beneficial effects in murine traumaticshock. Am. J. Pliysiol. (Heart Cirr. Physiol.). 267:H2124-H2131.
43. Lefer, A.M. 1995. Role of selectins in myocardtal ischemia reperfusion injury. Ann. Thorac. Surg. 60:773-777.
44. Seekamp, A., and P.A. Ward. 1993. Ischemia-reperfusion injury. Agents Actions. 41:137-152.
45. O'Connell, D., A. Koenig, S. Jennings, B. Hicke, H.L. Han, T. Fitzwater, Y.F. Chang, N. Varki, D. Parma, and A. Varki. 1996. Calcium-dependent oligonucleotide antagonists specific for L-selectin. Proc. Natl. Acad. Sci. USA. 93:5883-5887.
46. Hicke, B.J., S.R. Watson, A. Koenig, C.K. Lynott, R.F. Bargatze, Y.F. Chang, S. Ringquist, L. Moon-McDermot, S. Jennings, T. Fitzwater, et al. 1996. DNA aptamers block L-selectin function in vivo. Inhibition of human lymphocyte trafficking in SCID mice. J. Clin. Invest. 98:2688-2692.
47. Yednock, T.A., L.M. Stoolman, and S.D. Rosen. 1987. Phosphomannosyl-derivatized beads detect a receptor involved in lymphocyte homing. J. Cell Biol. 104:713-723.
48. Skinner, M.P., D.J. Fournier, R.K. Andrews, J.J. Gorman, C.N. Chesterman, and M.C. Berndt. 1989. Characterization of human platelet GMP-140 as a heparin-binding protein. Bioehem. Biophys. Res. Commun. 164:1373-1379.
49. Aruffo, A., W. Kolanus, G. Walz, P. Fredman, and B. Seed. 1991. CD62/P-selectin recognition of myeloid and tumor cell sulfalides. Cell. 67:35-44.
50. x, and sulfated glycans modulate this binding. Biochem. Biophys. Res. Commun. 181:1223-1230.
51. Skinner, M.P., C.M. Lucas, G.F. Burns, C.N. Chesterman, and M.C Berndl. 1991. GMP-140 binding to neulrophils is inhibited by sulfated glycans. J. Biol. Chem. 266:5371-5374.
52. Needham, L.K., and R.L. Schnaar. 1993. The HNK-1 reactive sultoglucuronyl glycolipids are ligands for L-selectin and P-selectin but not E-selectin. Proc. Natl. Acad. Sci. USA. 90:1359-1363.
53. Nelson, R.M., O. Cecconi, W.G. Roberts, A. Aruffo, R.J. Linhardt, and M.P. Bevilacqua. 1993. Heparin oligosaccharides bind L- and P-selectin and inhibit acute inflammation. Blood. 82:3253-3258.
54. a. A superior oligosaccharide ligand tor human E-selectin. J. Biol. Chem. 269:1595-1598.
55. Mitsuoka, C., N. Kawakami-Kimura, M. Kasugai-Sawada, N. Hiraiwa, K. Toda, H. Ishida, M. Kiso, A. Hasegawa, and R. Kannagi. 1997. Sulfated sialyl Lewis X, the putative L-selectin ligand, detected on endothelial cells of high endothelial venules by a distinct set of anti-sialyl Lewis X antibodies. Biochem. Biophys. Res. Commun. 230:546-551.
56. Yoshino, K., H. Ohmoto, N. Kondo, H. Tsujishila, Y. Hiramatsu, Y. Inoue, and H. Kondo. 1997. Studies on selectin blockers. IV. Structure-function relationships of sulfated sialyl Lewis X hexasaccharide ceramides toward E-, P-, and L-selectin binding. J. Med. Chem. 40:455-462.
57. Norgard-Sumnicht, K.E., N.M. Varki, and A. Varki. 1993. Calcium-dependent heparin-like ligands for L-selectin in nonlymphoid endolhelial cells. Science. 261:480-483.
58. Norgard-Sumnicht, K., and A. Varki. 1995. Endolhelial heparan sulfate proteoglycans that bind to L-selectin have glucosamine residues with unsuhstituted amino groups. J. Biol. Chem. 270:12012-12024.
59. Zakrzewicz, A., M. Gräfe, D. Terbeek, M. Bongrazio, W. AuchSchwelk. B. Walzog. K. Graf. E. Fleck, K. Ley, and P. Gaehtgens. 1997. L-selec(in-dependent leukocyte adhesion to microvascular but not to macrovascular endothelial cells of the human coronary system. Blood. 89:3228-3235.
60. Giuffre, L., A.S. Cordey, N. Monai, Y. Tardy, M. Schapira, and O. Spertini. 1997. Monocyte adhesion to activated aortic endothelium: role of L-selectin and heparan sulfate proteoglycans. J. Cell Biol. 136:945-956.
61. Ginsberg, J.S. 1996. Management of venous thromboembolism. N. Engl. J. Med 335:1816-1828.
62. Hirsh, J. 1996. Comparison of the relative efficacy and safety of lowmolecular-weight heparin and unfractionated heparin for the treatment of venous thrombosis. Semin. Thromb. Hemost. 22(Suppl. 2):7-12.
63. Fareed, J., J.M. Walenga, D. Hoppensteadt, X. Huan, and A. Racanelli. 1988. Comparative study on the in vitro and in vivo activities of seven lowmolecular-weight heparins [published erratum appears in Haemostasis. 1988. 18:following 389]. Haemostasis. 18(Suppl. 3):3-15.
64. Coccheri, S. 1990. Low molecular weight heparins: an introduction. Haemostasis. 20(Suppl. S1):74-80.
65. Lane, D.A., and K. Ryan. 1990. The importance of anti-factor Xa and antithrombin activities of low molecular weight heparins. J. Lab. Clin. Med. 116:269-270.
66. Mammen, E.F. 1990. Fragmin: the new generation antithrombotic agent. Why low molecular weight heparin? Semin. Thromh. Hemoslasis. 16(Suppl.):1-4
67. Sakuragawa, N., and K. Takahashi. 1990. Comparative studies on properties of unfractionated and low molecular weight heparin. Semin. Thromb. Hemostasis. 16(Suppl.):5-11.
68. Freedman, M.D. 1991. Low molecular weight heparins: an emerging new class of glycosaminoglycan antithrombotics. J. Clin. Pharmacol. 31:298-306.
69. Hamano, S., M. Nishiyama, H. Komatsu, H. Miyata, S. Ikeda, and N. Sakuragawa. 1992. Study of anticoagulant mechanism of low molecular weight heparin. Thromb. Res. 65:801-808.
70. Nurmohamed, M.T., H. Ten Cate, and J.W. Ten Cate. 1997. Low molecular weight heparin(oid)s: clinical investigations and practical recommendations. Drugs. 53:736-751.
71. Pineo, G.F., and R.D. Hull. 1997. Low-mulccular-weight heparin: prophylaxis and treatment of venous thromboembolism. Annu. Rev. Med. 48:79-91.
72. Lohse, D.L., and R.J. Linhardt. 1992. Purification and characterization of heparin lyases from Flavobuetcium heparinum. J. Biol. Chem. 267:24347-24355.
73. Pervin, A., C. Gullo, K.A. Jandik, X.-J. Han, and R.J. Linhardt. 1995. Preparation and structural charactcrization of large hcparin-derived oligosaccharides. Glycobiology. 5:83-95.
74. Norgard, K.E., H. Han, L. Powell, M. Kriegler, A. Varki, and N.M. Varki. 1993. Enhanced interaction of L-selectin with the high endothelial venule ligand via selectively oxidized sialic acids. Proc. Natl. Acad. Sci. USA. 90:1068-1072.
75. Nelson, R.M., S. Dolich, A. Aruffo, O. Cecconi, and M.P. Bevilacqua. 1993. Higher-affinity oligosaccharide ligands for E-selectin. J. Clin. Invest. 91: 1157-1166.
76. Roux, L., S. Holovda, G. Sundblad, H.H. Freeze, and A. Varki. 1988. Sulfaled N-linked oligosaccharides in mammalian cells. I. Complex-type chains with sialic acids and O-sulfate esters. J. Biol. Chem. 263:8879-8889.
77. Kocnig, A., R. Jain, R. Vig, K.E. Norgard-Sumnicht, K.L. Matta, and A. Varki. 1997. Selectin inhibition: synthesis and evaluation of novel sialylaled, sulfated and tucosylated oligosaccharides, including the major capping group of GlyCAM-1. Glymhiohgy. 7:79-93.
78. Conrad, H.E. 1996. Nitrous acid degradation of glycosaminoglvcans. In Current Protocols in Molecular Biology. F.M. Ausubel, R. Brent, R.E. Kingston, D.D. Moore, J.G. Seidman, J.A. Smith, K. Struhl, L.M. Albright, D.M. Coen, and A. Varki, editors. John Wiley & Sons, New York. Unit 17-22A.
79. Desai, U.R., H. Wang, and R.J. Linhardt. 1993. Specificity studies on the heparin lyases from Flavobacteriuni hepurinum. Bioehemistry. 32:8140-8145.
80. Jandik, K.A., K. Gu, and R.J. Linhardt. 1994. Action pattern of polysaccharide lyases on glycosaminoglycans. Glycohinlogy. 4:289-296.
81. Linhardt, R.J. 1996. Analysis of glycosaminoglycans with polysaccharide lyases. In Current Protocols in Molecular Biology. F.M. Ausubel, R. Brent, R.E. Kingston, D.D. Moore, J.G. Seidman, J.A. Smith, K. Struhl, L.M. Albright, D.M. Coen, and A. Varki, editors. John Wiley & Sons, New York. Unit 17-13B.
82. 2+-induced eonformational change in the lectin domain of GMP-140. J. Biol. Chem. 266:22313-22318.
83. Graves, B.J., R.L. Crowther, C. Chandran, J.M. Rumberger, S. Li, K.-S. Huang, D.H. Presky, P.C. Familletti, B.A. Wolitzky, and D.K. Burns. 1994. Insight into E-selectin/ligand interaction from the crystal structure and mulagcnesis of the lec/EGF domains. Nature. 367:532-538.
84. Geng, J.G., M.P. Bevilacqua, K.L. Moore, T.M. Mclnlyre, S.M. Preseott, J.M. Kim, G.A. Bliss, G.A. Zimmerman, and R.P. McEver. 1990. Rapid neutrophil adhesion to activated endothelium mediated by GMP-140. Nature. 343:757-760.
85. Rosen, S.D., and C.R. Bertozzi. 1994. The selectins and their ligands. Curr. Opin. Cell. Biol. 6:663-673.
86. Weis, W.I., K. Drickamer, and W.A. Hendrickson. 1992. Structure of a C-type mannose-binding protein complexed with an oligosaccharide. Nature. 360:127-134.
87. Varki, A., and S. Kornfeld. 1983. The spectrum of anionic oligosaccharides released by endo-beta-N-acetylglucosaminidase H from glycoproteins. Structural studies and interactions with the phosphomannosyl receptor. J. Biol. Chem. 258:2808-2818.
88. Powell, L.D., R.K. Jain, K.L. Malta, S. Sabesan, and A. Varki. 1995. Characterization of sialyloligosaccharide binding by recombinant soluble and native cell-associated CD22. Evidence for a minimal structural recognition motif and the potential importance of multisite binding. J. Biol. Chem. 270:7523-7532.
89. Boneu, B. 1996. Glycosaminoglycans: clinical use. Semin. Thromb. Hemosiasis. 22:209-212.
90. El Habbal, M.H., L. Smith, M.J. Elliotl, and S. Strobel. 1995. Effect of heparin anticoagulation on neutrophil adhesion molecules and release of IL8: C3 is not essential. Cardiovasc. Res. 30:676-681.
91. Leculier, C., O. Benzerara, N. Couprie, A. Francina, Y. Lasne, E. Archimbaud, and D. Fiere. 1992. Specific binding between human neutrophils and heparin. Br. J. Haemutol. 81:81-85.
92. Salzman, E.W., R.D. Rosenberg, M.H. Smith, J.N. Lindon, and L. Favreau. 1980. Effect of heparin and heparin fractions on platelet aggregation. J. Clin. Invest. 65:64-73.
93. Home, M.K., III, and E.S. Chao. 1989. Heparin binding to resting and activated platelets. Blood. 74:238-243.
94. Home, M.K., III. 1991. Heparin binds normally to platelets digested with Strepiomyces griseus praiease. Thromb. Res. 61:155-158.
95. Dawes, J. 1993. Interactions of heparins in the vascular environment. Haemostasis. 23(Suppl. 1):212-219.
96. Hemmerich, S., H. Leffler, and S.D. Rosen. 1995. Structure of the O-glycans in GlyCAM-1, an endothelial-derived ligand for L-selectin. J. Biol. Chem. 270:12035-12047.
97. Pouyani, T., and B. Seed. 1995. PSGL-1 recognition of P-selectin is controlled by a tyrosine sulfntion consensus at the PSGL-1 amino terminus. Cell. 83:333-343.
98. Wilkins, P.P., K.L. Moore, R.P. McEver, and R.D. Cummings. 1995. Tyrosine sulfalion of P-selectin glycoprotein ligand-1 is required for high affinity binding to P-selectin. J. Biol. Chem. 270:22677-22680.
99. Wilkins, P.P., R.P. McEver, and R.D. Cummings. 1996. Structures of the O-glycans on P-selectin glycoprolein ligand-1 from HL-60 cells. J. Biol. Chem. 271:18732-18742.
100. Lincoff, A.M., J.E. Tchcng, R.M. Califf, T. Bass, J.J. Popma, P.S. Toirstoin, N.S. Kleiman, L.J. Hattel. H.V. Anderson, J.J. Ferguson, et al. 1997. Standard versus low-dose weight-adjusted heparin in patients treated with the platelet glycoprotein IIb/IIIa receptor antibody fragment abciximab (c7E3 Fab) during percutaneous coronary rcvascularization. PROLOG Investigators. Am. J. Cardiol. 79:286-291.
101. Granger, C.B., J. Hirsch, R.M. Califf, J. Col, H.D. White, A. Betriu, L.H. Woodlief, K.L. Lee, E.G. Bovill, R.J. Simes, and E.J. Topol. 1996. Activated partial thromhoplastin time and outcome after thrombolytic therapy for acute myocardial infarction: results from the GUSTO-I trial. Circultion. 93: 870-878.
102. Sobel, B.E. 1997. Heparin and slreptokinase. Cartdiovasc. Drugs Ther. 11:97-100.
103. Commcrford, P.J. 1997. Heparin after acute myocardial infarction. cardiovasc. Drugs Ther. 11:101-109.
104. White, H.D. 1997. Is hepurin of value in the management of acute myocardial infarction? Cardiovasc. Drugs Ther. 11:111-119.
105. Mulligan, M.S., J.B. Lowe, R.D. Larsen, J. Paulson, Z. Zheng, S. DeFrees, K. Maemura, M. Fukuda, and P.A. Ward. 1993. Protective effects of sialylated oligosaccharides in immune complex-induced acute lung injury. J. Exp. Med. 178:623-631.
106. x-containing oligosaccharide attenuates myocardial reperfusion injury in cats. J. Clin. Invest. 93:1140-1148.
107. x analog attenuates neutrophil accumulation and myocardial necrosis after ischemia and reperfusion. Circulation. 90:2390-2401.
108. x-containng carbohydrate reduces infarct sizc: rolc of sclcctins in myocardial repcrfusion injury. Am. J. Physiol. (Heart Circ. Physiol.). 271H20S6-H2096.
109. Tojo, S.J., S. Yokota, H. Koike, J. Schultz, Y. Hamazume, E. Misugi, K. Yamada, M. Hayashi, J.C. Paulson, and S. Morooka. 1996. Reduction of rat myocardial ischemia and reperfusion injury by sialyl Lewis x oligosaccharide and anti-rat P-seleetin antibodies. Glycobiolagy. 6:463-169.