Heparin-induced leukocytosis requires 6-O-sulfation and is caused by blockade of selectin- and CXCL12 protein-mediated leukocyte trafficking in mice

Journal of Biological Chemistry

Volumn 287, Issue 8, 2012, Pages 5542-5553

  Zhang, Siyuan ^a   Condac, Eduard ^a   Qiu, Hong ^a   Jiang, Junlin ^a   Gutierrez Sanchez, Gerardo ^a   Bergmann, Carl ^a   Handel, Tracy ^b   Wang, Lianchun ^a  

^a UNIVERSITY OF GEORGIA   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTICOAGULANT ACTIVITIES; BONE MARROW; CHEMOKINES; L-SELECTIN; MECHANISTIC STUDIES; P-SELECTIN; SELECTINS; SIDE EFFECT; STRUCTURAL DETERMINANTS; THYMOCYTES; UNDERLYING MECHANISM; VASCULATURE;

BIOCHEMISTRY; BIOLOGY;

POLYSACCHARIDES;

GLUCOSAMINE; HEPARIN; L SELECTIN; PADGEM PROTEIN; STROMAL CELL DERIVED FACTOR 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW; CELL ACTIVITY; CELL DIFFERENTIATION; CELL MIGRATION; CELL POPULATION; CONTROLLED STUDY; ENZYME INHIBITION; HUMAN; HUMAN CELL; LEUKOCYTE; LEUKOCYTOSIS; LYMPHOCYTOSIS; MOUSE; NEUTROPHIL; NEUTROPHILIA; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SULFATION; THYMOCYTE; THYMUS;

ANIMALS; BONE MARROW CELLS; CHEMOKINE CXCL12; GLUCOSAMINE; HEPARIN; HEPARITIN SULFATE; HUMANS; LEUKOCYTE ROLLING; LEUKOCYTOSIS; LYMPHOCYTOSIS; MICE; NEUTROPHILS; SELECTINS; SULFATES; THYMOCYTES;

EID: 84863174876     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.314716     Document Type: Article

References (56)

1. Opdenakker, G., Fibbe, W. E., and Van Damme, J. (1998) The molecular basis of leukocytosis. Immunol. Today 19, 182-189 (Pubitemid 28216059)
2. Abramson, N., and Melton, B. (2000) Leukocytosis. Basics of clinical assessment. Am. Fam. Physician 62, 2053-2060
3. Bradfield, J. W., and Born, G. V. (1974) Lymphocytosis produced by heparin and other sulfated polysaccharides in mice and rats. Cell. Immunol. 14, 22-32
4. Godlowski, Z. Z. (1951) Prevention of hormona eosinopenia and lymphopenia by inhibition of clotting in blood; preliminary report. Br. Med. J. 1, 854-855
5. Sasaki, S. (1967) Production of lymphocytosis by polysaccharide polysulfates (heparinoids). Nature 214, 1041-1042
6. Esko, J. D., and Selleck, S. B. (2002) Order out of chaos. Assembly of ligand-binding sites in heparan sulfate. Annu. Rev. Biochem. 71, 435-471 (Pubitemid 34800227)
7. Nelson, R. M., Cecconi, O., Roberts, W. G., Aruffo, A., Linhardt, R. J., and Bevilacqua, M. P. (1993) Heparin oligosaccharides bind L- and P-selectin and inhibit acute inflammation. Blood 82, 3253-3258 (Pubitemid 23356692)
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 (Pubitemid 32220849)
9. 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 (Pubitemid 34743473)
10. Fahey, V. A. (1995) Heparin-induced thrombocytopenia. J. Vasc. Nurs. 13, 112-116
11. Weninger, W., Ulfman, L. H., Cheng, G., Souchkova, N., Quackenbush, E. J., Lowe, J. B., and von Andrian, U. H. (2000) Specialized contributions by α(1,3)-fucosyltransferase-IV and FucT-VII during leukocyte rolling in dermal microvessels. Immunity 12, 665-676
12. Sweeney, E. A., Lortat-Jacob, H., Priestley, G. V., Nakamoto, B., and Papayannopoulou, T. (2002) Sulfated polysaccharides increase plasma levels of SDF-1 in monkeys and mice. Involvement in mobilization of stem/progenitor cells. Blood 99, 44-51
13. Albanese, P., Caruelle, D., Frescaline, G., Delbé, J., Petit-Cocault, L., Huet, E., Charnaux, N., Uzan, G., Papy-Garcia, D., and Courty, J. (2009) Glycosaminoglycan mimetics-induced mobilization of hematopoietic progenitors and stem cells into mouse peripheral blood. Structure/function insights. Exp. Hematol. 37, 1072-1083
14. Wang, L., Fuster, M., Sriramarao, P., and Esko, J. D. (2005) Endothelial heparan sulfate deficiency impairs L-selectin- and chemokine-mediated neutrophil trafficking during inflammatory responses. Nat. Immunol. 6, 902-910 (Pubitemid 43090445)
15. Scollay, R. G., Butcher, E. C., and Weissman, I. L. (1980) Thymus cell migration. Quantitative aspects of cellular traffic from the thymus to the periphery in mice. Eur. J. Immunol. 10, 210-218 (Pubitemid 10150634)
16. Horwitz, B. H., Mizgerd, J. P., Scott, M. L., and Doerschuk, C. M. (2001) Mechanisms of granulocytosis in the absence of CD18. Blood 97, 1578-1583 (Pubitemid 32217220)
17. Basu, S., Hodgson, G., Katz, M., and Dunn, A. R. (2002) Evaluation of role of G-CSF in the production, survival, and release of neutrophils from bone marrow into circulation. Blood 100, 854-861 (Pubitemid 34832610)
18. Suratt, B. T., Petty, J. M., Young, S. K., Malcolm, K. C., Lieber, J. G., Nick, J. A., Gonzalo, J. A., Henson, P. M., and Worthen, G. S. (2004) Role of the CXCR4/SDF-1 chemokine axis in circulating neutrophil homeostasis. Blood 104, 565-571 (Pubitemid 38900043)
19. Nakagawa, M., Terashima, T., D'yachkova, Y., Bondy, G. P., Hogg, J. C., and van Eeden, S. F. (1998) Glucocorticoid-induced granulocytosis. Contribution of marrow release and demargination of intravascular granulocytes. Circulation 98, 2307-2313 (Pubitemid 28533851)
20. Netelenbos, T., Zuijderduijn, S., Van Den Born, J., Kessler, F. L., Zweegman, S., Huijgens, P. C., and Dräger, A. M. (2002) Proteoglycans guide SDF-1-induced migration of hematopoietic progenitor cells. J. Leukocyte Biol. 72, 353-362
21. Netelenbos, T., van den Born, J., Kessler, F. L., Zweegman, S., Merle, P. A., van Oostveen, J. W., Zwaginga, J. J., Huijgens, P. C., and Dräger, A. M. (2003) Proteoglycans on bone marrow endothelial cells bind and present SDF-1 towards hematopoietic progenitor cells. Leukemia 17, 175-184 (Pubitemid 36175904)
22. Wijelath, E., Namekata, M., Murray, J., Furuyashiki, M., Zhang, S., Coan, D., Wakao, M., Harris, R. B., Suda, Y., Wang, L., and Sobel, M. (2010) Multiple mechanisms for exogenous heparin modulation of vascular endothelial growth factor activity. J. Cell. Biochem. 111, 461-468
23. Zhou, B., Honor, L. B., He, H., Ma, Q., Oh, J. H., Butterfield, C., Lin, R. Z., Melero-Martin, J. M., Dolmatova, E., Duffy, H. S., Gise, A., Zhou, P., Hu, Y. W., Wang, G., Zhang, B., Wang, L., Hall, J. L., Moses, M. A., McGowan, F. X., and Pu, W. T. (2011) Adult mouse epicardium modulates myocardial injury by secreting paracrine factors. J. Clin. Invest. 121, 1894-1904
24. Osmond, R. I., Kett, W. C., Skett, S. E., and Coombe, D. R. (2002) Protein-heparin interactions measured by BIAcore 2000 are affected by the method of heparin immobilization. Anal. Biochem. 310, 199-207 (Pubitemid 35388262)
25. Amara, A., Lorthioir, O., Valenzuela, A., Magerus, A., Thelen, M., Montes, M., Virelizier, J. L., Delepierre, M., Baleux, F., Lortat-Jacob, H., and Arenzana-Seisdedos, F. (1999) Stromal cell-derived factor-1α associates with heparan sulfates through the first β-strand of the chemokine. J. Biol. Chem. 274, 23916-23925
26. Bradfield, J. W., and Born, G. V. (1969) Inhibition of lymphocyte recirculation by heparin. Nature 222, 1183-1184
27. Ford, W. L., and Gowans, J. L. (1969) The traffic of lymphocytes. Semin. Hematol. 6, 67-83
28. Christopher, M. J., and Link, D. C. (2007) Regulation of neutrophil homeostasis. Curr. Opin. Hematol. 14, 3-8 (Pubitemid 44885605)
29. Furze, R. C., and Rankin, S. M. (2008) Neutrophil mobilization and clearance in the bone marrow. Immunology 125, 281-288
30. Johnson, R. C., Mayadas, T. N., Frenette, P. S., Mebius, R. E., Subramaniam, M., Lacasce, A., Hynes, R. O., and Wagner, D. D. (1995) Blood cell dynamics in P-selectin-deficient mice. Blood 86, 1106-1114
31. Springer, T. A. (1994) Traffic signals for lymphocyte recirculation and leukocyte emigration. The multistep paradigm. Cell 76, 301-314
32. Malý, P., Thall, A., Petryniak, B., Rogers, C. E., Smith, P. L., Marks, R. M., Kelly, R. J., Gersten, K. M., Cheng, G., Saunders, T. L., Camper, S. A., Camphausen, R. T., Sullivan, F. X., Isogai, Y., Hindsgaul, O., von Andrian, U. H., and Lowe, J. B. (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 (Pubitemid 26299495)
33. Martin, C., Burdon, P. C., Bridger, G., Gutierrez-Ramos, J. C., Williams, T. J., and Rankin, S. M. (2003) Chemokines acting via CXCR2 and CXCR4 control the release of neutrophils from the bone marrow and their return following senescence. Immunity 19, 583-593 (Pubitemid 37311439)
34. Wang, J., Mukaida, N., Zhang, Y., Ito, T., Nakao, S., and Matsushima, K. (1997) Enhanced mobilization of hematopoietic progenitor cells by mouse MIP-2 and granulocyte colony-stimulating factor in mice. J. Leukocyte Biol. 62, 503-509 (Pubitemid 27459780)
35. Zhang, P., Quinton, L. J., Gamble, L., Bagby, G. J., Summer, W. R., and Nelson, S. (2005) The granulopoietic cytokine response and enhancement of granulopoiesis in mice during endotoxemia. Shock 23, 344-352 (Pubitemid 40463628)
36. Eash, K. J., Greenbaum, A. M., Gopalan, P. K., and Link, D. C. (2010) CXCR2 and CXCR4 antagonistically regulate neutrophil trafficking from murine bone marrow. J. Clin. Invest. 120, 2423-2431
37. Frenette, P. S., and Weiss, L. (2000) Sulfated glycans induce rapid hematopoietic progenitor cell mobilization. Evidence for selectin-dependent and -independent mechanisms. Blood 96, 2460-2468
38. Handel, T. M., Johnson, Z., Crown, S. E., Lau, E. K., and Proudfoot, A. E. (2005) Regulation of protein function by glycosaminoglycans, as exemplified by chemokines. Annu. Rev. Biochem. 74, 385-410 (Pubitemid 40995512)
39. Shen, H., Cheng, T., Olszak, I., Garcia-Zepeda, E., Lu, Z., Herrmann, S., Fallon, R., Luster, A. D., and Scadden, D. T. (2001) CXCR-4 desensitization is associated with tissue localization of hemopoietic progenitor cells. J. Immunol. 166, 5027-5033 (Pubitemid 32280715)
40. Dar, A., Schajnovitz, A., Lapid, K., Kalinkovich, A., Itkin, T., Ludin, A., Kao, W. M., Battista, M., Tesio, M., Kollet, O., Cohen, N. N., Margalit, R., Buss, E. C., Baleux, F., Oishi, S., Fujii, N., Larochelle, A., Dunbar, C. E., Broxmeyer, H. E., Frenette, P. S., and Lapidot, T. (2011) Rapid mobilization of hematopoietic progenitors by AMD3100 and catecholamines is mediated by CXCR4-dependent SDF-1 release from bone marrow stromal cells. Leukemia 25, 1378
41. Petit, I., Szyper-Kravitz, M., Nagler, A., Lahav, M., Peled, A., Habler, L., Ponomaryov, T., Taichman, R. S., Arenzana-Seisdedos, F., Fujii, N., Sandbank, J., Zipori, D., and Lapidot, T. (2002) G-CSF induces stem cell mobilization by decreasing bone marrow SDF-1 and up-regulating CXCR4. Nat. Immunol. 3, 687-694 (Pubitemid 34752479)
42. Netelenbos, T., van den Born, J., Kessler, F. L., Zweegman, S., Huijgens, P. C., and Drager, A. M. (2003) In vitro model for hematopoietic progenitor cell homing reveals endothelial heparan sulfate proteoglycans as direct adhesive ligands. J. Leukocyte Biol. 74, 1035-1044 (Pubitemid 38040325)
43. Sadir, R., Baleux, F., Grosdidier, A., Imberty, A., and Lortat-Jacob, H. (2001) Characterization of the stromal cell-derived factor-1α-heparin complex. J. Biol. Chem. 276, 8288-8296
44. Hattori, K., Heissig, B., Tashiro, K., Honjo, T., Tateno, M., Shieh, J. H., Hackett, N. R., Quitoriano, M. S., Crystal, R. G., Rafii, S., and Moore, M. A. (2001) Plasma elevation of stromal cell-derived factor-1 induces mobilization of mature and immature hematopoietic progenitor and stem cells. Blood 97, 3354-3360
45. De La Luz Sierra, M., Yang, F., Narazaki, M., Salvucci, O., Davis, D., Yarchoan, R., Zhang, H. H., Fales, H., and Tosato, G. (2004) Differential processing of stromally derived factor-1α and stromal-derived factor-1β explains functional diversity. Blood 103, 2452-2459 (Pubitemid 38392993)
46. Zhang, F., Yang, B., Ly, M., Solakyildirim, K., Xiao, Z., Wang, Z., Beaudet, J. M., Torelli, A. Y., Dordick, J. S., and Linhardt, R. J. (2011) Structural characterization of heparins from different commercial sources. Anal. Bioanal. Chem. 401, 2793-2803
47. Stekel, D. J., Parker, C. E., and Nowak, M. A. (1997)Amodel of lymphocyte recirculation. Immunol. Today 18, 216-221
48. Leppänen, A., White, S. P., Helin, J., McEver, R. P., and Cummings, R. D. (2000) Binding of glycosulfopeptides to P-selectin requires stereospecific contributions of individual tyrosine sulfate and sugar residues. J. Biol. Chem. 275, 39569-39578 (Pubitemid 32058983)
49. Stevenson, J. L., Varki, A., and Borsig, L. (2007) Heparin attenuates metastasis mainly due to inhibition of P- and L-selectin, but non-anticoagulant heparins can have additional effects. Thromb. Res. 120, S107-S111 (Pubitemid 350101778)
50. 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 (Pubitemid 41428760)
51. Kim, C. H., and Broxmeyer, H. E. (1999) Chemokines. Signal lamps for trafficking of T and B cells for development and effector function. J. Leukocyte Biol. 65, 6-15 (Pubitemid 29024912)
52. Tyrrell, D. J., Horne, A. P., Holme, K. R., Preuss, J. M., and Page, C. P. (1999) Heparin in inflammation. Potential therapeutic applications beyond anticoagulation. Adv. Pharmacol. 46, 151-208
53. Papayannopoulou, T. (2004) Current mechanistic scenarios in hematopoietic stem/progenitor cell mobilization. Blood 103, 1580-1585
54. Lapidot, T., and Petit, I. (2002) Current understanding of stem cell mobilization. The roles of chemokines, proteolytic enzymes, adhesion molecules, cytokines, and stromal cells. Exp. Hematol. 30, 973-981 (Pubitemid 35286613)
55. de Haan, G., Ausema, A., Wilkens, M., Molineux, G., and Dontje, B. (2000) Efficient mobilization of hematopoietic progenitors after a single injection of pegylated recombinant human granulocyte colony-stimulating factor in mouse strains with distinct marrow-cell pool sizes. Br. J. Haematol. 110, 638-646
56. Thelen, M., and Stein, J. V. (2008) How chemokines invite leukocytes to dance. Nat. Immunol. 9, 953-959