Proteoglycans guide SDF-1-induced migration of hematopoietic progenitor cells

Journal of Leukocyte Biology

Volumn 72, Issue 2, 2002, Pages 353-362

  Netelenbos, Tanja ^a   Zuijderduijn, Suzanne ^a   Van Den Born, Jacob ^a   Kessler, Floortje L ^a   Zweegman, Sonja ^a   Huijgens, Peter C ^a   Dräger, Angelika M ^a,b  

^a ACADEMIC MEDICAL CENTER   (Netherlands)

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Bone marrow endothelial cells; Chemokines; Glycosaminoglycans; Homing; Transmigration

Indexed keywords

CHEMOATTRACTANT; CHEMOKINE RECEPTOR CXCR4; GLYCOSAMINOGLYCAN; HEPARAN SULFATE; PROTEOGLYCAN; STROMAL CELL DERIVED FACTOR 1;

ANTIGEN PRESENTATION; ARTICLE; BONE MARROW; CELL MIGRATION; DOSE RESPONSE; ENDOTHELIUM CELL; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; PRIORITY JOURNAL;

BONE MARROW; CELL ADHESION; CELL MOVEMENT; CELLS, CULTURED; CHEMOKINES, CXC; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOTHELIUM, VASCULAR; EXTRACELLULAR MATRIX; FIBRONECTINS; HEMATOPOIETIC STEM CELLS; HEPARIN; HEPARITIN SULFATE; HL-60 CELLS; HUMANS; MACROMOLECULAR SUBSTANCES; OSMOLAR CONCENTRATION; PROTEIN BINDING; PROTEOGLYCANS; RECEPTORS, CXCR4; SOLUBILITY; STRUCTURE-ACTIVITY RELATIONSHIP; VASCULAR CELL ADHESION MOLECULE-1;

EID: 0036697301     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (60)

1. Papayannopoulou, T., Craddock, C. (1997) Homing and trafficking of hemopoietic progenitor cells. Acta Haematol. 97, 97-104.
2. Mazo, I. B., von Andrian, U. H. (1999) Adhesion and homing of bloodborne cells in bone marrow microvessels. J. Leukoc. Biol. 66, 25-32.
3. Dimitroff, C. J., Lee, J. Y., Rafii, S., Fuhlbrigge, R. C., Sackstein, R. (2001) Cd44 is a major E-selectin ligand on human hematopoietic progenitor cells. J. Cell Biol. 153, 1277-1286.
4. Frenette, P. S., Subbarao, S., Mazo, I. B., von Andrian, U. H., Wagner, D. D. (1998) Endothelial selectins and vascular cell adhesion molecule-1 promote hematopoietic progenitor homing to bone marrow. Proc. Natl. Acad. Sci. USA 95, 14423-14428.
5. Schweitzer, C. M., Vicart, P., Delouis, C., Paulin, D., Dräger, A. M., Langenhuijsen, M. M., Weksler, B. B. (1997) Characterization of a newly established human bone marrow endothelial cell line: distinct adhesive properties for hematopoietic progenitors compared with human umbilical vein endothelial cells. Lab. Investig. 76, 25-36.
6. Peled, A., Grabovsky, V., Habler, L., Sandbank, J., Arenzana-Seisdedos, F., Petit, I., Ben-Hur, H., Lapidot, T. (1999) The chemokine SDF-1 stimulates integrin-mediated arrest of CD34(+) cells on vascular endothelium under shear flow. J. Clin. Investig. 104, 1199-1211.
7. Rood, P. M., Dercksen, M. W., Cazemier, H., Kerst, J. M., von dem, B., Gerritsen, W. R., van der Schoot, C. E. (2000) E-selectin and very late activation antigen-4 mediate adhesion of hematopoietic progenitor cells to bone marrow endothelium. Ann. Hematol. 79, 477-484.
8. Voermans, C., Rood, P. M., Hordijk, P. L., Gerritsen, W. R., van der Schoot, C. E. (2000) Adhesion molecules involved in transendothelial migration of human hematopoietic progenitor cells. Stem Cells 18, 435-443.
9. Naiyer, A. J., Jo, D. Y., Ahn, J., Mohle, R., Peichev, M., Lam, G., Silverstein, R. L., Moore, M. A., Rafii, S. (1999) Stromal derived factor-1-induced chemokinesis of cord blood CD34(+) cells (long-term culture-initiating cells) through endothelial cells is mediated by E-selectin. Blood 94, 4011-4019.
10. Yong, K. L., Watts, M., Shaun, T. N., Sullivan, A., Ings, S., Linch, D. C. (1998) Transmigration of CD34+ cells across specialized and nonspecialized endothelium requires prior activation by growth factors and is mediated by PECAM-1 (CD31). Blood 91, 1196-1205.
11. Janowska-Wieczorek, A., Marquez, L. A., Dobrowsky, A., Ratajezak, M. Z., Cabuhat, M. L. (2000) Differential MMP and TIMP production by human marrow and peripheral blood CD34(+) cells in response to chemokines. Exp. Hematol. 28, 1274-1285.
12. Mackay, C. R. (2001) Chemokines: immunology's high impact factors. Nat. Immunol. 2, 95-101.
13. Bleul, C. C., Fuhlbrigge, R. C., Casasnovas, J. M., Aiuti, A., Springer, T. A. (1996) A highly efficacious lymphocyte chemoattractant, stromal cell-derived factor 1 (SDF-1). J. Exp. Med. 184, 1101-1109.
14. Zlotnik, A., Yoshie, O. (2000) Chemokines: a new classification system and their role in immunity. Immunity 12, 121-127.
15. Kim, C. H., Broxmeyer, H. E. (1998) In vitro behavior of hematopoietic progenitor cells under the influence of chemoattractants: stromal cell-derived factor-1, steel factor, and the bone marrow environment. Blood 91, 100-110.
16. Aiuti, A., Webb, I. J., Bleul, C., Springer, T., Gutierrez-Ramos, J. C. (1997) The chemokine SDF-1 is a chemoattractant for human CD34+ hematopoietic progenitor cells and provides a new mechanism to explain the mobilization of CD34+ progenitors to peripheral blood. J. Exp. Med. 185, 111-120.
17. Ponomaryov, T., Peled, A., Petit, I., Taichman, R. S., Habler, L., Sandbank, J., Arenzana-Seisdedos, F., Magerus, A., Caruz, A., Fujii, N., Nagler, A., Lahav, M., Szyper-Kravitz, M., Zipori, D., Lapidot, T. (2000) Induction of the chemokine stromal-derived factor-1 following DNA damage improves human stem cell function. J. Clin. Investig. 106, 1331-1339.
18. Imai, K., Kobayashi, M., Wang, J., Shinobu, N., Yoshida, H., Hamada, J., Shindo, M., Higashino, F., Tanaka, J., Asaka, M., Hosokawa, M. (1999) Selective secretion of chemoattractants for haemopoietic progenitor cells by bone marrow endothelial cells: a possible role in homing of haemopoietic progenitor cells to bone marrow. Br. J. Haematol. 106, 905-911.
19. Peled, A., Kollet, O., Ponomaryov, T., Petit, I., Franitza, S., Grabovsky, V., Slav, M. M., Nagler, A., Lider, O., Alon, R., Zipori, D., Lapidot, T. (2000) The chemokine SDF-1 activates the integrins LFA-1, VLA-4, and VLA-5 on immature human CD34(+) cells: role in transendothelial/stromal migration and engraftment of NOD/SCID mice. Blood 95, 3289-3296.
20. Ma, Q., Jones, D., Borghesani, P. R., Segal, R. A., Nagasawa, T., Kishimoto, T., Bronson, R. T., Springer, T. A. (1998) Impaired B-lymphopoiesis, myelopoiesis, and derailed cerebellar neuron migration in CXCR4-and SDF-1-deficient mice. Proc. Natl. Acad. Sci. USA 95, 9448-9453.
21. Zou, Y. R., Kottmann, A. H., Kuroda, M., Taniuchi, I., Littman, D. R. (1998) Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development. Nature 393, 595-599.
22. Peled, A., Petit, I., Kollet, O., Magid, M., Ponomaryov, T., Byk, T., Nagler, A., Ben-Hur, H., Many, A., Shultz, L., Lider, O., Alon, R., Zipori, D., Lapidot, T. (1999) Dependence of human stem cell engraftment and repopulation of NOD/SCID mice on CXCR4. Science 283, 845-848.
23. Netelenbos, T., Dräger, A. M., Van het Hof, B., Kessler, F. L., Delouis, C., Huijgens, P. C., van den Born, J., Van Dijk, W. (2001). Differences in sulfation patterns of heparan sulfate derived from human bone marrow and umbilical vein endothelial cells. Exp. Hematol. 29, 884-893.
24. Amara, A., Lorthioir, O., Valenzuela, A., Magerus, A., Thelen, M., Montes, M., Virelizier, J. L., Delepierre, M., Baleux, F., Lortat-Jacob, H., Arenzana-Seisdedos, F. (1999) Stromal cell-derived factor-1alpha associates with heparan sulfates through the first beta-strand of the chemokine. J. Biol. Chem. 274, 23916-23925.
25. Mbemba, E., Gluckman, J. C., Gattegno, L. (2000) Glycan and glycosaminoglycan binding properties of stromal cell-derived factor (SDF)-1alpha. Glycobiology 10, 21-29.
26. Jackson, R. L., Busch, S. J., Cardin, A. D. (1991) Glycosaminoglycans: molecular properties, protein interactions, and role in physiological processes. Physiol. Rev. 71, 481-539.
27. Bernfield, M., Gotte, M., Park, P. W., Reizes, O., Fitzgerald, M. L., Lincecum, J., Zako, M. (1999) Functions of cell surface heparan sulfate proteoglycans. Annu. Rev. Biochem. 68, 729-777.
28. Gallagher, J. T., Turnbull, J. E., Lyon, M. (1992) Patterns of sulphation in heparan sulphate: polymorphism based on a common structural theme. Int. J. Biochem. 24, 553-560.
29. Esko, J. D., Lindahl, U. (2001) Molecular diversity of heparan sulfate. J. Clin. Investig. 108, 169-173.
30. Maciag, T., Cerundolo, J., Ilsley, S., Kelley, P. R., Forand, R. (1979) An endothelial cell growth factor from bovine hypothalamus: identification and partial characterization. Proc. Natl. Acad. Sci. USA 76, 5674-5678.
31. Schmid, I., Krall, W. J., Uittenbogaart, C. H., Braun, J., Giorgi, J. V. (1992) Dead cell discrimination with 7-amino-actinomycin D in combination with dual color immunofluorescence in single laser flow cytometry. Cytometry 13, 204-208.
32. Kuijper, P. H., Gallardo, T. H., van der Linden, J. A., Lammers, J. W., Sixma, J. J., Koenderman, L., Zwaginga, J. J. (1996) Platelet-dependent primary hemostasis promotes selectin- and integrin-mediated neutrophil adhesion to damaged endothelium under flow conditions. Blood 87, 3271-3281.
33. Bianchi, G., D'Amico, G., Varone, L., Sozzani, S., Mantovani, A., Allavena, P. (2000) In vitro studies on the trafficking of dendritic cells through endothelial cells and extra-cellular matrix. Dev. Immunol. 7, 143-153.
34. Frey, T. (1995) Nucleic acid dyes for detection of apoptosis in live cells. Cytometry 21, 265-274.
35. Mohle, R., Bautz, F., Rafii, S., Moore, M. A., Brugger, W., Kanz, L. (1998) The chemokine receptor CXCR-4 is expressed on CD34+ hematopoietic progenitors and leukemic cells and mediates transendothelial migration induced by stromal cell-derived factor-1. Blood 91, 4523-4530.
36. Voermans, C., Gerritsen, W. R., von dem Borne, A. E., van der Schoot, C. E. (1999) Increased migration of cord blood-derived CD34+ cells, as compared to bone marrow and mobilized peripheral blood CD34+ cells across uncoated or fibronectin-coated filters. Exp. Hematol. 27, 1806-1814.
37. Humphries, D. E., Silbert, J. E. (1988) Chlorate: a reversible inhibitor of proteoglycan sulfation. Biochem. Biophys. Res. Commun. 154, 365-371.
38. van den Born, J., Gunnarsson, K., Bakker, M. A., Kjellen, L., Kusche-3Gullberg, M., Maccarana, M., Berden, J. H., Lindahl, U. (1995) Presence of N-unsubstituted glucosamine units in native heparan sulfate revealed by a monoclonal antibody. J. Biol. Chem. 270, 31303-31309.
39. Pelletier, A. J., van der Laan, L. J., Hildbrand, P., Siani, M. A., Thompson, D. A., Dawson, P. E., Torbett, B. E., Salomon, D. R. (2000) Presentation of chemokine SDF-1 alpha by fibronectin mediates directed migration of T cells. Blood 96, 2682-2690.
40. Rot, A. (1993) Neutrophil attractant/activation protein-1 (interleukin-8) induces in vitro neutrophil migration by haptotactic mechanism. Eur. J. Immunol. 23, 303-306.
41. Drexler, H. G., Matsuo, Y. (1999) Guidelines for the characterization and publication of human malignant hematopoietic cell lines. Leukemia 13, 835-842.
42. Cinamon, G., Grabovsky, V., Winter, E., Franitza, S., Feigelson, S., Shamri, R., Dwir, O., Alon, R. (2001) Novel chemokine functions in lymphocyte migration through vascular endothelium under shear flow. J. Leukoc. Biol. 69, 860-866.
43. Cinamon, G., Shinder, V., Alon, R. (2001) Shear forces promote lymphocyte migration across vascular endothelium bearing apical chemokines. Nat. Immunol. 2, 515-522.
44. Verfaillie, C., Hurley, R., Bhatia, R., McCarthy, J. B. (1994) Role of bone marrow matrix in normal and abnormal hematopoiesis. Crit. Rev. Oncol. Hematol. 16, 201-224.
45. Wight, T. N., Kinsella, M. G., Qwarnstrom, E. E. (1992) The role of proteoglycans in cell adhesion, migration and proliferation. Curr. Opin. Cell Biol. 4, 793-801.
46. Rot, A. (1992) Endothelial cell binding of NAP-1/IL-8: role in neutrophil emigration. Immunol. Today 13, 291-294.
47. Wiedermann, C. J., Reinisch, N., Bellmann, R., Schratzberger, P., Kowald, E., Kahler, C. M. (1995) Different patterns of deactivation of chemotaxis and haptotaxis of human peripheral blood mononuclear leukocytes by soluble and surface-bound attractants. J. Leukoc. Biol. 58, 438-444.
48. Pye, D. A., Gallagher, J. T. (1999) Monomer complexes of basic fibroblast growth factor and heparan sulfate oligosaccharides are the minimal functional unit for cell activation. J. Biol. Chem. 274, 13456-13461.
49. Gallagher, J. T. (2001) Heparan sulfate: growth control with a restricted sequence menu. J. Clin. Investig. 108, 357-361.
50. Rodriguez-Frade, J. M., Mellado, M., Martinez, A. (2001) Chemokine receptor dimerization: two are better than one. Trends Immunol. 22, 612-617.
51. Hoogewerf, A. J., Kuschert, G. S., Proudfoot, A. E., Borlat, F., ClarkLewis, I., Power, C. A., Wells, T. N. (1997) Glycosaminoglycans mediate cell surface oligomerization of chemokines. Biochemistry 36, 13570-13578.
52. Ali, S., Palmer, A. C., Fritchley, S. J., Maley, Y., Kirby, J. A. (2001) Multimerization of monocyte chemoattractant protein-1 is not required for glycosaminoglycan-dependent transendothelial chemotaxis. Biochem. J. 358, 737-745.
53. Sadir, R., Baleux, F., Grosdidier, A., Imberty, A., Lortat-Jacob, H. (2001) Characterization of the stromal cell-derived factor-1alpha-heparin complex. J. Biol. Chem. 276, 8288-8296.
54. Vila-Coro, A. J., Rodriguez-Frade, J. M., Martin, D. A., Moreno-Ortiz, M. C., Martinez, A., Mellado, M. (1999) The chemokine SDF-1alpha triggers CXCR4 receptor dimerization and activates the JAK/STAT pathway. FASEB J. 13, 1699-1710.
55. Valenzuela-Fernandez, A., Palanche, T., Amara, A., Magerus, A., Altmeyer, R., Delaunay, T., Virelizier, J. L., Baleux, F., Galzi, J. L., Arenzana-Seisdedos, F. (2001) Optimal inhibition of X4 HIV isolates by the CXC chemokine stromal cell-derived factor 1 alpha requires interaction with cell surface heparan sulfate proteoglycans. J. Biol. Chem. 276, 26550-26558.
56. Spivak-Kroizman, T., Lemmon, M. A., Dikic, I., Ladbury, J. E., Pinchasi, D., Huang, J., Jaye, M., Crumley, G., Schlessinger, J., Lax, I. (1994) Heparin-induced oligomerization of FGF molecules is responsible for FGF receptor dimerization, activation, and cell proliferation. Cell 79, 1015-1024.
57. Webb, L. M., Ehrengruber, M. U., Clark-Lewis, I., Baggiolini, M., Rot, A. (1993) Binding to heparan sulfate or heparin enhances neutrophil responses to interleukin 8. Proc. Natl. Acad. Sci. USA 90, 7158-7162.
58. Dias-Baruffi, M., Pereira-da-Silva, G., Jamur, M. C., Roque-Barreira, M. C. (1998) Heparin potentiates in vivo neutrophil migration induced by IL-8. Glycoconj. J. 15, 523-526.
59. Ramdin, L., Perks, B., Sheron, N., Shute, J. K. (1998) Regulation of interleukin-8 binding and function by heparin and alpha2-macroglobulin. Clin. Exp. Allergy 28, 616-624.
60. Kuschert, G. S., Coulin, F., Power, C. A., Proudfoot, A. E., Hubbard, R. E., Hoogewerf, A. J., Wells, T. N. (1999) Glycosaminoglycans interact selectively with chemokines and modulate receptor binding and cellular responses. Biochemistry 38, 12959-12968.