Chemokine receptor CXCR4-dependent internalization and resecretion of functional chemokine SDF-1 by bone marrow endothelial and stromal cells

Nature Immunology

Volumn 6, Issue 10, 2005, Pages 1038-1046

  Dar, Ayelet ^a   Goichberg, Polina ^a   Shinder, Vera ^a   Kalinkovich, Alexander ^a   Kollet, Orit ^a   Netzer, Neta ^a   Margalit, Raanan ^a   Zsak, Marion ^b   Nagler, Arnon ^c   Hardan, Izhar ^c   Resnick, Igor ^d   Rot, Antal ^b   Lapidot, Tsvee ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b Novartis Institute for Biomedical Research   (Austria)

^c SHEBA MEDICAL CENTER   (Israel)

^d HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

CD34 ANTIGEN; CHEMOKINE RECEPTOR CXCR4; STROMAL CELL DERIVED FACTOR 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; CELL FUNCTION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENDOTHELIUM CELL; HEMATOPOIETIC CELL; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HOMEOSTASIS; HUMAN; HUMAN CELL; HUMAN TISSUE; INTRACELLULAR TRANSPORT; LYMPHOCYTE HOMING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN SECRETION; PROTEIN TRANSPORT; STROMA CELL;

ANIMALS; ANTIGENS, CD34; BONE MARROW; CELL MOVEMENT; CELLS, CULTURED; CHEMOKINES, CXC; ENDOTHELIAL CELLS; HEMATOPOIETIC STEM CELLS; HOMEOSTASIS; HUMANS; IMMUNITY, ACTIVE; MICE; MICE, INBRED NOD; MICE, SCID; RECEPTORS, CXCR4; STROMAL CELLS;

EID: 27144443385     PISSN: 15292908     EISSN: None     Source Type: Journal    
DOI: 10.1038/ni1251     Document Type: Article

References (53)

1. Nagasawa, T. et al. Defects of B-cell lymphopoiesis and bone-marrow myelopoiesis in mice lacking the CXC chemokine PBSF/SDF-1. Nature 382, 635-638 (1996).
2. Tachibana, K. et al. The chemokine receptor CXCR4 is essential for vascularization of the gastrointestinal tract. Nature 393, 591-594 (1998).
3. Zou, Y.R., Kottmann, A.H., Kuroda, M., Taniuchi, I. & Littman, D.R. Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development. Nature 393, 5955-599 (1998).
4. Peled, A. et al. Dependence of human stem cell engrafment and repopulation of NOD/SCID mice on CXCR4. Science 283, 845-848 (1999).
5. Muller, A. et al. Involvement of chemokine receptors in breast cancer metastasis. Nature 410, 50-56 (2001).
6. Sun, Y.X. et al. Expression of CXCR4 and CXCL12 (SDF-1) in human prostate cancers (PCa) in vivo. J. Cell. Biochem. 89, 462-473 (2003).
7. Imai, K. et al. 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 (1999).
8. + cells on vascular endothelium under shear flow. J. Clin. Invest. 104, 1199-1211 (1999).
9. Ponomaryov, T. et al. Induction of the chemokine stromal-derived factor-1 following DNA damage improves human stem cell function. J. Clin. Invest. 106, 1331-1339 (2000).
10. Kortesidis, A. Stromal-derived factor-1 promotes the growth, survival, and development of human bone marrow stromal stem cells. Blood 105, 3793-3801 (2005).
11. + cells: Role in transendothelial/stromal migration and engrafment of NOD/SCID mice. Blood 95, 3289-3296 (2000).
12. + T cells. Immunity 22, 259-270 (2005).
13. Ceradini, D.J. et al. Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nat. Med. 10, 858-564 (2004).
14. + stem cell recruitment to the liver. J. Clin. Invest. 112, 160-169 (2003).
15. De La Luz Sierra, M. et al. Differential processing of stromal-derived factor-1α and stromal-derived factor-1β explains functional diversity. Blood 103, 2452-2459 (2004).
16. Petit, I. et al. G-CSF induces stem cell mobilization by decreasing bone marrow SDF-1 and up-regulating CXCR4. Nat. Immunol. 3, 687-694 (2002).
17. Levesque, J.P., Hendy, J., Takamatsu, Y., Simmons, P.J. & Bendall, L.J. Disruption of the CXCR4/CXCL12 chemotactic interaction during hematopoietic stem cell mobilization induced by GCSF or cyclophosphamide. J. Clin. Invest. 111, 187-196 (2003).
18. Hattori, K. et al. Plasma elevation of stromal-cell-derived factor-1 induces mobilization of mature and immature hematopoietic progenitor and stem cells. Blood 97, 3354-3360 (2001).
19. Shen, H. et al. CXCR-4 desensitization is associated with tissue localization of hematopoietic progenitor cells. J. Immunol. 166 5027-5033 (2001).
20. Middleton, J. et al. Transcytosis and surface presentation of IL-8 by venular endothelial cells. Cell 91, 385-395 (1997).
21. Horuk, R. et al. The duffy antigen receptor for chemokines: structural analysis and expression in the brain. J. Leukoc. Biol. 59, 29-38 (1996).
22. Rot, A. & von Andrian, U.H. Chemokines in innate and adaptive host defense: Basic chemokinese grammar for immune cells. Annu. Rev. Immunol. 22, 891-928 (2004).
23. Jamieson, T. et al. The chemokine receptor D6 limits the inflammatory response in vivo. Nat. Immunol. 6, 403-411 (2005).
24. Fra, A.M. et al. Scavenging of inflammatory CC chemokines by the promiscuous putatively silent chemokine receptor D6. J. Immunol. 170, 2279-2282 (2003).
25. Chaudhuri, A. et al. Detection of Duffy antigen in the plasma membranes and caveolae of vascular endothelial and epithelial cells of nonerythroid organs. Blood 89, 701-712 (1997).
26. Amara, A. et al. Stromal cell-derived factor-1α associates with heparan sulfates through the first β-strand of the chemokine. J. Biol. Chem. 274, 23916-23925 (1999).
27. Suzuki, G. et al. Loss of SDF-1 receptor expression during positive selection in the thymus. Int. Immunol. 10, 1049-1056 (1998).
28. Signoret, N. et al. Phorbol esters and SDF-1 induce rapid endocytosis and down modulation of the chemokine receptor CXCR4. J. Cell Biol. 139, 651-664 (1997).
29. Minshall, R.D., Sessa, W.C., Stan, R.V, Anderson, R.G.W. & Malik, A.B. Caveolin regulation of endothelial function. Am. J. Physiol. Lung Cell. Mol. Physiol. 285, L1179-L1183 (2003).
30. Rafii, S. Isolation and characterization of human bone marrow microvascular endothelial cells: Hematopoietic progenitor cell adhesion. Blood 84, 10-19 (1994).
31. Chaussalet, M. et al. Homocysteine modulates the proteolytic potential of human vascular endothelial cells. Biochem. Biophys. Res. Commun. 316, 170-176 (2004).
32. Netelenbos, T. et al. Proteoglycans on bone marrow endothelial cells bind and present SDF-1 towards hematopoietic progenitor cells. Leukemia 17, 175-184 (2003).
33. null mice. Blood 97, 3283-3291 (2001).
34. Amara, A. et al. HIV coreceptor downregulation as antiviral principle: SDF-1 α-dependent internalization of the chemokine receptor CXCR4 contributes to inhibition of HIV replication. J. Exp. Med. 186, 139-146 (1997).
35. Stumm, R.K. et al. A dual role for the SDF-1/CXCR4 chemokine receptor system in adult brain: Isoform-selective regulation of SDF-1 expression modulates CXCR4-dependent neuronal plasticity and cerebral leukocyte recruitment after focal ischemia. J. Neurosci. 22, 5865-5878 (2002).
36. Askari, A.T. et al. Effect of stromal-cell-derived-factor 1 on stem-cell homing and tissue regeneration in ischaemic cardiomyopathy. Lancet 362, 697-703 (2003).
37. Dzenko, K.A., Andjelkovic, A.V., Kuziel, W.A. & Pachter, J.S. The chemokine receptor CCR2 mediates the binding and internalization of monocyte chemoattractant protein-1 along brain microvessels. J. Neurosci. 21, 9214-9223 (2001).
38. Pablos, J.L. et al. Synoviocyte-derived CXCL12 is displayed on endothelium and induces angiogenesis in rheumatoid arthritis. J. Immunol. 170, 2147-2152 (2003).
39. Hitchon, C. et al. Hypoxia-induced production of stromal cell-derived factor 1(CXCL12) and vascular endothelial growth factor by synovial fibroblasts. Arthritis Rheum. 46, 2587-2597 (2002).
40. Salvucci, O. et al. Regulation of endothelial cell branching morphogenesis by endogenous chemokine stromal-derived factor-1. Blood 99, 2703-2711 (2002).
41. Lambertsen, R.H. & Weiss, L. A model of intramedullary hematopoietic microenvironments based on stereologic study of the distribution of endocloned marrow colonies. Blood 63, 287-297 (1984).
42. Lord, B.I. The architecture of bone marrow cell populations. Int. J. Cell Cloning 8, 317-331 (1990).
43. Calvi, L.M. et al. Osteoblastic cells regulate the haematopoietic stem cell niche. Nature 425, 841-846 (2003).
44. Kollet, O. et al. Osteoclasts are involved in stem cell mobilization: Cleavage of SDF-1 by cathepsin K. Blood 104, 364A-364A.
45. Sipkins, D.A. et al. In vivo imaging of specialized bone marrow endothelial microdomains for tumour engraftment. Nature 435, 969-973 (2005).
46. Kiel, M.J. et al. SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell 121, 1109-1121 (2005).
47. Mack, M. et al. Aminooxypentane-RANTES induces CCR5 internalization but inhibits recycling: A novel inhibitory mechanism of HIV infectivity. J. Exp. Med. 187, 1215-1224 (1998).
48. Oynebraten, I., Bakke, O., Brandtzaeg, P., Johansen, F.E. & Haraldsen, G. Rapid chemokine secretion from endothelial cells originates from two distinct compartments. Blood 104, 314-320 (2004).
49. Wolff, B., Burns, A.R., Middleton, J. & Rot, A. Endothelial cells "memory" of inflammatory stimulation: Human venular endothelial cells store interleukin 8 in weibel-palade bodies. J. Exp. Med. 188 1757-1762 (1998).
50. Rafii, S. et al. isolation and characterization of human bone marrow microvascular endothelial cells: Hematopoietic progenitor cell adhesion. Blood 84, 10-19 (1994).
51. Spiegel, A. et al. Unique SDF-1 induced activation of human precursor-B ALL cells as a result of altered CXCR4 expression and signaling. Blood 103, 2900-2907 (2004).
52. Song, L. & Pachter, S. Monocyte chemoattractant protein-1 alters expression of tight junction-associated proteins in brain microvascular endothelial cells. Microvasc. Res. 67, 78-89 (2004).
53. Pelletier, A.J. et al. Presentation of chemokine SDF-1α by fibronectin mediates directed migration of T cells. Blood 96 2682-2690 (2000).