J. Exp. Med.
© The Rockefeller University Press
0022-1007/97/01/111/10 $2.00
Volume 185 January 1997 111-120

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

By A. Aiuti,^* I.J. Webb,^¶ C. Bleul, T. Springer, and J.C. Gutierrez-Ramos^***

From the ^* Center for Blood Research, Inc., and the  Department of Genetics, ^§ Department of Pathology, and  Department of Medicine, Harvard Medical School, Boston, Massachusetts 02115; ^¶ Blood Component Laboratory, Dana-Farber Cancer Institute, Boston, Massachusetts 02115; and ^** Millennium Pharmaceuticals, Inc., Cambridge, Massachusetts 02139

Hematopoietic progenitor cells migrate in vitro and in vivo towards a gradient of the chemotactic factor stromal cell-derived factor-1 (SDF-1) produced by stromal cells. This is the first chemoattractant reported for human CD34⁺ progenitor cells. Concentrations of SDF-1 that elicit chemotaxis also induce a transient elevation of cytoplasmic calcium in CD34⁺ cells. SDF-1-induced chemotaxis is inhibited by pertussis toxin, suggesting that its signaling in CD34⁺ cells is mediated by seven transmembrane receptors coupled to G_i proteins. CD34⁺ cells migrating to SDF-1 include cells with a more primitive (CD34⁺/CD38 or CD34⁺/DR) phenotype as well as CD34⁺ cells phenotypically committed to the erythroid, lymphoid and myeloid lineages, including functional BFU-E, CFU-GM, and CFU-MIX progenitors. Chemotaxis of CD34⁺ cells in response to SDF-1 is increased by IL-3 in vitro and is lower in CD34⁺ progenitors from peripheral blood than in CD34⁺ progenitors from bone marrow, suggesting that an altered response to SDF-1 may be associated with CD34 progenitor mobilization.

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• Katayama, Y., Hidalgo, A., Peired, A., Frenette, P. S. (2004). Integrin {alpha}4{beta}7 and its counterreceptor MAdCAM-1 contribute to hematopoietic progenitor recruitment into bone marrow following transplantation. Blood 104: 2020-2026 [Abstract] [Full Text]  
• Hidalgo, A., Peired, A. J., Weiss, L. A., Katayama, Y., Frenette, P. S. (2004). The integrin {alpha}M{beta}2 anchors hematopoietic progenitors in the bone marrow during enforced mobilization. Blood 104: 993-1001 [Abstract] [Full Text]  
• Rombouts, E. J. C., Pavic, B., Lowenberg, B., Ploemacher, R. E. (2004). Relation between CXCR-4 expression, Flt3 mutations, and unfavorable prognosis of adult acute myeloid leukemia. Blood 104: 550-557 [Abstract] [Full Text]  
• Suratt, B. T., Petty, J. M., Young, S. K., Malcolm, K. C., Lieber, J. G., Nick, J. A., Gonzalo, J.-A., Henson, P. M., Worthen, G. S. (2004). Role of the CXCR4/SDF-1 chemokine axis in circulating neutrophil homeostasis. Blood 104: 565-571 [Abstract] [Full Text]  
• Fischer, A. M., Mercer, J. C., Iyer, A., Ragin, M. J., August, A. (2004). Regulation of CXC Chemokine Receptor 4-mediated Migration by the Tec Family Tyrosine Kinase ITK. J. Biol. Chem. 279: 29816-29820 [Abstract] [Full Text]  
• Levesque, J.-P., Liu, F., Simmons, P. J., Betsuyaku, T., Senior, R. M., Pham, C., Link, D. C. (2004). Characterization of hematopoietic progenitor mobilization in protease-deficient mice. Blood 104: 65-72 [Abstract] [Full Text]  
• Kimura, T., Boehmler, A. M., Seitz, G., Kuci, S., Wiesner, T., Brinkmann, V., Kanz, L., Mohle, R. (2004). The sphingosine 1-phosphate receptor agonist FTY720 supports CXCR4-dependent migration and bone marrow homing of human CD34+ progenitor cells. Blood 103: 4478-4486 [Abstract] [Full Text]  
• Hiasa, K.-i., Ishibashi, M., Ohtani, K., Inoue, S., Zhao, Q., Kitamoto, S., Sata, M., Ichiki, T., Takeshita, A., Egashira, K. (2004). Gene Transfer of Stromal Cell-Derived Factor-1{alpha} Enhances Ischemic Vasculogenesis and Angiogenesis via Vascular Endothelial Growth Factor/Endothelial Nitric Oxide Synthase-Related Pathway: Next-Generation Chemokine Therapy for Therapeutic Neovascularization. Circulation 109: 2454-2461 [Abstract] [Full Text]  
• Evans, C. A., Tonge, R., Blinco, D., Pierce, A., Shaw, J., Lu, Y., Hamzah, H. G., Gray, A., Downes, C. P., Gaskell, S. J., Spooncer, E., Whetton, A. D. (2004). Comparative proteomics of primitive hematopoietic cell populations reveals differences in expression of proteins regulating motility. Blood 103: 3751-3759 [Abstract] [Full Text]  
• Oonakahara, K.-i., Matsuyama, W., Higashimoto, I., Kawabata, M., Arimura, K., Osame, M. (2004). Stromal-Derived Factor-1{alpha}/CXCL12-CXCR 4 Axis Is Involved in the Dissemination of NSCLC Cells into Pleural Space. Am. J. Respir. Cell Mol. Bio. 30: 671-677 [Abstract] [Full Text]  
• van Buul, J. D., Hordijk, P. L. (2004). Signaling in Leukocyte Transendothelial Migration. Arterioscler. Thromb. Vasc. Bio. 24: 824-833 [Abstract] [Full Text]  
• Tavor, S., Petit, I., Porozov, S., Avigdor, A., Dar, A., Leider-Trejo, L., Shemtov, N., Deutsch, V., Naparstek, E., Nagler, A., Lapidot, T. (2004). CXCR4 Regulates Migration and Development of Human Acute Myelogenous Leukemia Stem Cells in Transplanted NOD/SCID Mice. Cancer Res. 64: 2817-2824 [Abstract] [Full Text]  
• Spiegel, A., Kollet, O., Peled, A., Abel, L., Nagler, A., Bielorai, B., Rechavi, G., Vormoor, J., Lapidot, T. (2004). Unique SDF-1-induced activation of human precursor-B ALL cells as a result of altered CXCR4 expression and signaling. Blood 103: 2900-2907 [Abstract] [Full Text]  
• Kahn, J., Byk, T., Jansson-Sjostrand, L., Petit, I., Shivtiel, S., Nagler, A., Hardan, I., Deutsch, V., Gazit, Z., Gazit, D., Karlsson, S., Lapidot, T. (2004). Overexpression of CXCR4 on human CD34+ progenitors increases their proliferation, migration, and NOD/SCID repopulation. Blood 103: 2942-2949 [Abstract] [Full Text]  
• Avigdor, A., Goichberg, P., Shivtiel, S., Dar, A., Peled, A., Samira, S., Kollet, O., Hershkoviz, R., Alon, R., Hardan, I., Ben-Hur, H., Naor, D., Nagler, A., Lapidot, T. (2004). CD44 and hyaluronic acid cooperate with SDF-1 in the trafficking of human CD34+ stem/progenitor cells to bone marrow. Blood 103: 2981-2989 [Abstract] [Full Text]  
• Bartolome, R. A., Galvez, B. G., Longo, N., Baleux, F., van Muijen, G. N. P., Sanchez-Mateos, P., Arroyo, A. G., Teixido, J. (2004). Stromal Cell-Derived Factor-1{alpha} Promotes Melanoma Cell Invasion across Basement Membranes Involving Stimulation of Membrane-Type 1 Matrix Metalloproteinase and Rho GTPase Activities. Cancer Res. 64: 2534-2543 [Abstract] [Full Text]  
• Hamon, M., Mbemba, E., Charnaux, N., Slimani, H., Brule, S., Saffar, L., Vassy, R., Prost, C., Lievre, N., Starzec, A., Gattegno, L. (2004). A syndecan-4/CXCR4 complex expressed on human primary lymphocytes and macrophages and HeLa cell line binds the CXC chemokine stromal cell-derived factor-1 (SDF-1). Glycobiology 14: 311-323 [Abstract] [Full Text]  
• Abeyta, M. J., Clark, A. T., Rodriguez, R. T., Bodnar, M. S., Pera, R. A. R., Firpo, M. T. (2004). Unique gene expression signatures of independently-derived human embryonic stem cell lines. Hum Mol Genet 13: 601-608 [Abstract] [Full Text]  
• Monaco, G., Konopleva, M., Munsell, M., Leysath, C., Wang, R.-Y., Jackson, C. E., Korbling, M., Estey, E., Belmont, J., Andreeff, M. (2004). Engraftment of Acute Myeloid Leukemia in NOD/SCID Mice Is Independent of CXCR4 and Predicts Poor Patient Survival. Stem Cells 22: 188-201 [Abstract] [Full Text]  
• Papayannopoulou, T. (2004). Current mechanistic scenarios in hematopoietic stem/progenitor cell mobilization. Blood 103: 1580-1585 [Abstract] [Full Text]  
• Ueda, Y., Yang, K., Foster, S. J., Kondo, M., Kelsoe, G. (2004). Inflammation Controls B Lymphopoiesis by Regulating Chemokine CXCL12 Expression. JEM 199: 47-58 [Abstract] [Full Text]  
• Yao, L., Salvucci, O., Cardones, A. R., Hwang, S. T., Aoki, Y., De La Luz Sierra, M., Sajewicz, A., Pittaluga, S., Yarchoan, R., Tosato, G. (2003). Selective expression of stromal-derived factor-1 in the capillary vascular endothelium plays a role in Kaposi sarcoma pathogenesis. Blood 102: 3900-3905 [Abstract] [Full Text]  

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