Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Original Article
  • Published:

Stem Cells

Rapid mobilization of hematopoietic progenitors by AMD3100 and catecholamines is mediated by CXCR4-dependent SDF-1 release from bone marrow stromal cells

Leukemia volume 25, pages 1286–1296 (2011)Cite this article

Subjects

A Corrigendum to this article was published on 10 August 2011

Abstract

Steady-state egress of hematopoietic progenitor cells can be rapidly amplified by mobilizing agents such as AMD3100, the mechanism, however, is poorly understood. We report that AMD3100 increased the homeostatic release of the chemokine stromal cell derived factor-1 (SDF-1) to the circulation in mice and non-human primates. Neutralizing antibodies against CXCR4 or SDF-1 inhibited both steady state and AMD3100-induced SDF-1 release and reduced egress of murine progenitor cells over mature leukocytes. Intra-bone injection of biotinylated SDF-1 also enhanced release of this chemokine and murine progenitor cell mobilization. AMD3100 directly induced SDF-1 release from CXCR4+ human bone marrow osteoblasts and endothelial cells and activated uPA in a CXCR4/JNK-dependent manner. Additionally, ROS inhibition reduced AMD3100-induced SDF-1 release, activation of circulating uPA and mobilization of progenitor cells. Norepinephrine treatment, mimicking acute stress, rapidly increased SDF-1 release and progenitor cell mobilization, whereas β2-adrenergic antagonist inhibited both steady state and AMD3100-induced SDF-1 release and progenitor cell mobilization in mice. In conclusion, this study reveals that SDF-1 release from bone marrow stromal cells to the circulation emerges as a pivotal mechanism essential for steady-state egress and rapid mobilization of hematopoietic progenitor cells, but not mature leukocytes.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6

Similar content being viewed by others

References

  1. Spiegel A, Kalinkovich A, Shivtiel S, Kollet O, Lapidot T . Stem cell regulation via dynamic interactions of the nervous and immune systems with the microenvironment. Cell Stem Cell 2008; 3: 484–492.

    Article  CAS  PubMed  Google Scholar 

  2. Lapidot T, Kollet O . The Brain-Bone-Blood Triad: Traffic Lights for Stem-Cell Homing and Mobilization. Hematology Am Soc Hematol Educ Program 2010; 1–6.

    Article  PubMed  Google Scholar 

  3. Wright DE, Wagers AJ, Gulati AP, Johnson FL, Weissman IL . Physiological migration of hematopoietic stem and progenitor cells. Science 2001; 294: 1933–1936.

    Article  CAS  PubMed  Google Scholar 

  4. Kollet O, Dar A, Lapidot T . The multiple roles of osteoclasts in host defense: bone remodeling and hematopoietic stem cell mobilization. Annu Rev Immunol 2007; 25: 51–69.

    Article  CAS  PubMed  Google Scholar 

  5. Lapid K, Vagima Y, Kollet O, Lapidot T . Egress and mobilization of hematopoietic progenitor cells. StemBook, Harvard Stem Cell Institute 2009; 1.39.1.

  6. Lapidot T, Petit I . Current understanding of stem cell mobilization: the roles of chemokines, proteolytic enzymes, adhesion molecules, cytokines, and stromal cells. Exp Hematol 2002; 30: 973–981.

    Article  CAS  PubMed  Google Scholar 

  7. Petit I, Szyper-Kravitz M, Nagler A, Lahav M, Peled A, Habler L et al. G-CSF induces stem cell mobilization by decreasing bone marrow SDF-1 and up-regulating CXCR4. Nat Immunol 2002; 3: 687–694.

    Article  CAS  PubMed  Google Scholar 

  8. Papayannopoulou T, Scadden DT . Stem-cell ecology and stem cells in motion. Blood 2008; 111: 3923–3930.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Dar A, Kollet O, Lapidot T . Mutual, reciprocal SDF-1/CXCR4 interactions between hematopoietic and bone marrow stromal cells regulate human stem cell migration and development in NOD/SCID chimeric mice. Exp Hematol 2006; 34: 967–975.

    Article  CAS  PubMed  Google Scholar 

  10. Ponomaryov T, Peled A, Petit I, Taichman RS, Habler L, Sandbank J et al. Induction of the chemokine stromal-derived factor-1 following DNA damage improves human stem cell function. J Clin Invest 2000; 106: 1331–1339.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Dar A, Goichberg P, Shinder V, Kalinkovich A, Kollet O, Netzer N et al. Chemokine receptor CXCR4-dependent internalization and resecretion of functional chemokine SDF-1 by bone marrow endothelial and stromal cells. Nat Immunol 2005; 6: 1038–1046.

    Article  CAS  PubMed  Google Scholar 

  12. Sugiyama T, Kohara H, Noda M, Nagasawa T . Maintenance of the hematopoietic stem cell pool by CXCL12-CXCR4 chemokine signaling in bone marrow stromal cell niches. Immunity 2006; 25: 977–988.

    Article  CAS  PubMed  Google Scholar 

  13. Hattori K, Heissig B, Tashiro K, Honjo T, Tateno M, Shieh JH et al. Plasma elevation of stromal cell-derived factor-1 induces mobilization of mature and immature hematopoietic progenitor and stem cells. Blood 2001; 97: 3354–3360.

    Article  CAS  PubMed  Google Scholar 

  14. Shen H, Cheng T, Olszak I, Garcia-Zepeda E, Lu Z, Herrmann S et al. CXCR-4 desensitization is associated with tissue localization of hemopoietic progenitor cells. J Immunol 2001; 166: 5027–5033.

    Article  CAS  PubMed  Google Scholar 

  15. Frenette PS, Weiss L . Sulfated glycans induce rapid hematopoietic progenitor cell mobilization: evidence for selectin-dependent and independent mechanisms. Blood 2000; 96: 2460–2468.

    CAS  PubMed  Google Scholar 

  16. Sweeney EA, Lortat-Jacob H, Priestley GV, Nakamoto B, Papayannopoulou T . Sulfated polysaccharides increase plasma levels of SDF-1 in monkeys and mice: involvement in mobilization of stem/progenitor cells. Blood 2002; 99: 44–51.

    Article  CAS  PubMed  Google Scholar 

  17. Tchernychev B, Ren Y, Sachdev P, Janz JM, Haggis L, O'Shea A et al. Discovery of a CXCR4 agonist pepducin that mobilizes bone marrow hematopoietic cells. Proc Natl Acad Sci USA 2010; 107: 22255–22259.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Mendez-Ferrer S, Lucas D, Battista M, Frenette PS . Haematopoietic stem cell release is regulated by circadian oscillations. Nature 2008; 452: 442–447.

    Article  CAS  PubMed  Google Scholar 

  19. Katayama Y, Battista M, Kao WM, Hidalgo A, Peired AJ, Thomas SA et al. Signals from the sympathetic nervous system regulate hematopoietic stem cell egress from bone marrow. Cell 2006; 124: 407–421.

    Article  CAS  PubMed  Google Scholar 

  20. Spiegel A, Shivtiel S, Kalinkovich A, Ludin A, Netzer N, Goichberg P et al. Catecholaminergic neurotransmitters regulate migration and repopulation of immature human CD34+ cells through Wnt signaling. Nat Immunol 2007; 8: 1123–1131.

    Article  CAS  PubMed  Google Scholar 

  21. Selleri C, Montuori N, Ricci P, Visconte V, Carriero MV, Sidenius N et al. Involvement of the urokinase-type plasminogen activator receptor in hematopoietic stem cell mobilization. Blood 2005; 105: 2198–2205.

    Article  CAS  PubMed  Google Scholar 

  22. Tjwa M, Janssens S, Carmeliet P . Plasmin therapy enhances mobilization of HPCs after G-CSF. Blood 2008; 112: 4048–4050.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Tesio M, Golan K, Corso S, Giordano S, Schajnovitz A, Vagima Y et al. Enhanced c-Met activity promotes G-CSF induced mobilization of hematopoietic progenitor cells via ROS signaling. Blood 2011; 117: 419–428.

    Article  CAS  PubMed  Google Scholar 

  24. Abraham M, Beider K, Wald H, Weiss ID, Zipori D, Galun E et al. The CXCR4 antagonist 4F-benzoyl-TN14003 stimulates the recovery of the bone marrow after transplantation. Leukemia 2009; 23: 1378–1388.

    Article  CAS  PubMed  Google Scholar 

  25. Hatse S, Princen K, Bridger G, De Clercq E, Schols D . Chemokine receptor inhibition by AMD3100 is strictly confined to CXCR4. FEBS Lett 2002; 527: 255–262.

    Article  CAS  PubMed  Google Scholar 

  26. Devine SM, Vij R, Rettig M, Todt L, McGlauchlen K, Fisher N et al. Rapid mobilization of functional donor hematopoietic cells without G-CSF using AMD3100, an antagonist of the CXCR4/SDF-1 interaction. Blood 2008; 112: 990–998.

    Article  CAS  PubMed  Google Scholar 

  27. Broxmeyer HE, Orschell CM, Clapp DW, Hangoc G, Cooper S, Plett PA et al. Rapid mobilization of murine and human hematopoietic stem and progenitor cells with AMD3100, a CXCR4 antagonist. J Exp Med 2005; 201: 1307–1318.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Larochelle A, Krouse A, Metzger M, Orlic D, Donahue RE, Fricker S et al. AMD3100 mobilizes hematopoietic stem cells with long-term repopulating capacity in nonhuman primates. Blood 2006; 107: 3772–3778.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Liles WC, Broxmeyer HE, Rodger E, Wood B, Hubel K, Cooper S et al. Mobilization of hematopoietic progenitor cells in healthy volunteers by AMD3100, a CXCR4 antagonist. Blood 2003; 102: 2728–2730.

    Article  CAS  PubMed  Google Scholar 

  30. Hess DA, Bonde J, Craft TP, Wirthlin L, Hohm S, Lahey R et al. Human progenitor cells rapidly mobilized by AMD3100 repopulate NOD/SCID mice with increased frequency in comparison to cells from the same donor mobilized by granulocyte colony stimulating factor. Biol Blood Marrow Transplant 2007; 13: 398–411.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Gazitt Y, Freytes CO, Akay C, Badel K, Calandra G . Improved mobilization of peripheral blood CD34+ cells and dendritic cells by AMD3100 plus granulocyte-colony-stimulating factor in non-Hodgkin's lymphoma patients. Stem Cells Dev 2007; 16: 657–666.

    Article  CAS  PubMed  Google Scholar 

  32. Cashen A, Lopez S, Gao F, Calandra G, MacFarland R, Badel K et al. A phase II study of plerixafor (AMD3100) plus G-CSF for autologous hematopoietic progenitor cell mobilization in patients with Hodgkin lymphoma. Biol Blood Marrow Transplant 2008; 14: 1253–1261.

    Article  CAS  PubMed  Google Scholar 

  33. Bennett BL, Sasaki DT, Murray BW, O'Leary EC, Sakata ST, Xu W et al. SP600125, an anthrapyrazolone inhibitor of Jun N-terminal kinase. Proc Natl Acad Sci USA 2001; 98: 13681–13686.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Reca R, Cramer D, Yan J, Laughlin MJ, Janowska-Wieczorek A, Ratajczak J et al. A novel role of complement in mobilization: immunodeficient mice are poor granulocyte-colony stimulating factor mobilizers because they lack complement-activating immunoglobulins. Stem Cells 2007; 25: 3093–3100.

    Article  CAS  PubMed  Google Scholar 

  35. Amara A, Lorthioir O, Valenzuela A, Magerus A, Thelen M, Montes M et al. Stromal cell-derived factor-1alpha associates with heparan sulfates through the first beta-strand of the chemokine. J Biol Chem 1999; 274: 23916–23925.

    Article  CAS  PubMed  Google Scholar 

  36. Nagasawa T, Hirota S, Tachibana K, Takakura N, Nishikawa S, Kitamura Y et al. Defects of B-cell lymphopoiesis and bone-marrow myelopoiesis in mice lacking the CXC chemokine PBSF/SDF-1. Nature 1996; 382: 635–638.

    Article  CAS  PubMed  Google Scholar 

  37. Lavi E, Strizki JM, Ulrich AM, Zhang W, Fu L, Wang Q et al. CXCR-4 (Fusin), a co-receptor for the type 1 human immunodeficiency virus (HIV-1), is expressed in the human brain in a variety of cell types, including microglia and neurons. Am J Pathol 1997; 151: 1035–1042.

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Zou YR, Kottmann AH, Kuroda M, Taniuchi I, Littman DR . Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development. Nature 1998; 393: 595–599.

    Article  CAS  PubMed  Google Scholar 

  39. Serrati S, Margheri F, Fibbi G, Di Cara G, Minafra L, Pucci-Minafra I et al. Endothelial cells and normal breast epithelial cells enhance invasion of breast carcinoma cells by CXCR-4-dependent up-regulation of urokinase-type plasminogen activator receptor (uPAR, CD87) expression. J Pathol 2008; 214: 545–554.

    Article  CAS  PubMed  Google Scholar 

  40. Jin DK, Shido K, Kopp HG, Petit I, Shmelkov SV, Young LM et al. Cytokine-mediated deployment of SDF-1 induces revascularization through recruitment of CXCR4+ hemangiocytes. Nat Med 2006; 12: 557–567.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Kollet O, Dar A, Shivtiel S, Kalinkovich A, Lapid K, Sztainberg Y et al. Osteoclasts degrade endosteal components and promote mobilization of hematopoietic progenitor cells. Nat Med 2006; 12: 657–664.

    Article  CAS  PubMed  Google Scholar 

  42. Massberg S, Konrad I, Schurzinger K, Lorenz M, Schneider S, Zohlnhoefer D et al. Platelets secrete stromal cell-derived factor 1alpha and recruit bone marrow-derived progenitor cells to arterial thrombi in vivo. J Exp Med 2006; 203: 1221–1233.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Petit I, Jin D, Rafii S . The SDF-1-CXCR4 signaling pathway: a molecular hub modulating neo-angiogenesis. Trends Immunol 2007; 28: 299–307.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Wang Y, Cui L, Gonsiorek W, Min SH, Anilkumar G, Rosenblum S et al. CCR2 and CXCR4 regulate peripheral blood monocyte pharmacodynamics and link to efficacy in experimental autoimmune encephalomyelitis. J Inflamm (Lond) 2009; 6: 32.

    Article  Google Scholar 

  45. Tepper OM, Carr J, Allen Jr RJ, Chang CC, Lin CD, Tanaka R et al. Decreased circulating progenitor cell number and failed mechanisms of stromal cell-derived factor-1alpha mediated bone marrow mobilization impair diabetic tissue repair. Diabetes 2010; 59: 1974–1983.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Bonig H, Chudziak D, Priestley G, Papayannopoulou T . Insights into the biology of mobilized hematopoietic stem/progenitor cells through innovative treatment schedules of the CXCR4 antagonist AMD3100. Exp Hematol 2009; 37: 402–415 e1.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Allende ML, Tuymetova G, Lee BG, Bonifacino E, Wu YP, Proia RL . S1P1 receptor directs the release of immature B cells from bone marrow into blood. J Exp Med 2010; 207: 1113–1124.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Downey N, Thien M, Juares J, Bradstock K, Bendall L . Sphingosine-1-phosphate mediates the egress of hematopoietic stem cells from the bone marrow into the peripheral blood. Exp Hematol ISEH Ann Meet 2010; 38: Abstract 122.

  49. Golan K, Vagima Y, Ludin A, Itkin T, Kalinkovich A, Cohen-Gur S et al. The lipid chemokine S1P regulates hematopoietic progenitor cell egress and mobilization via its major receptor S1P1 and by SDF-1 inhibition, in a p38/Akt/mTOR dependent manner. ASH Ann Meeting Abstr 2010; 116: Abstract 553.

  50. Ratajczak MZ, Lee H, Wysoczynski M, Wan W, Marlicz W, Laughlin MJ et al. Novel insight into stem cell mobilization-plasma sphingosine-1-phosphate is a major chemoattractant that directs the egress of hematopoietic stem progenitor cells from the bone marrow and its level in peripheral blood increases during mobilization due to activation of complement cascade/membrane attack complex. Leukemia 2010; 24: 976–985.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Ratajczak MZ, Kim CH, Wojakowski W, Janowska-Wieczorek A, Kucia M, Ratajczak J . Innate immunity as orchestrator of stem cell mobilization. Leukemia 2010; 24: 1667–1675.

    Article  CAS  PubMed  Google Scholar 

  52. Ross J . FGFR1 Is Required for and Elucidates Multiple Mechanisms of HSC Mobilization. ASH Ann Meet Abstr 2009; 114: Abstract 2532.

  53. Donzella GA, Schols D, Lin SW, Este JA, Nagashima KA, Maddon PJ et al. AMD3100, a small molecule inhibitor of HIV-1 entry via the CXCR4 co-receptor. Nat Med 1998; 4: 72–77.

    Article  CAS  PubMed  Google Scholar 

  54. Schols D, Struyf S, Van Damme J, Este JA, Henson G, De Clercq E . Inhibition of T-tropic HIV strains by selective antagonization of the chemokine receptor CXCR4. J Exp Med 1997; 186: 1383–1388.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Hendrix CW, Collier AC, Lederman MM, Schols D, Pollard RB, Brown S et al. Safety, pharmacokinetics, and antiviral activity of AMD3100, a selective CXCR4 receptor inhibitor, in HIV-1 infection. J Acquir Immune Defic Syndr 2004; 37: 1253–1262.

    Article  CAS  PubMed  Google Scholar 

  56. Zabel BA, Wang Y, Lewen S, Berahovich RD, Penfold ME, Zhang P et al. Elucidation of CXCR7-mediated signaling events and inhibition of CXCR4-mediated tumor cell transendothelial migration by CXCR7 ligands. J Immunol 2009; 183: 3204–3211.

    Article  CAS  PubMed  Google Scholar 

  57. Yamazaki K, Allen TD . Ultrastructural morphometric study of efferent nerve terminals on murine bone marrow stromal cells, and the recognition of a novel anatomical unit: the ‘neuro-reticular complex’. Am J Anat 1990; 187: 261–276.

    Article  CAS  PubMed  Google Scholar 

  58. Aiuti A, Webb IJ, Bleul C, Springer T, Gutierrez-Ramos JC . 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 1997; 185: 111–120.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Semerad CL, Christopher MJ, Liu F, Short B, Simmons PJ, Winkler I et al. G-CSF potently inhibits osteoblast activity and CXCL12 mRNA expression in the bone marrow. Blood 2005; 106: 3020–3027.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Christopher MJ, Liu F, Hilton MJ, Long F, Link DC . Suppression of CXCL12 production by bone marrow osteoblasts is a common and critical pathway for cytokine-induced mobilization. Blood 2009; 114: 1331–1339.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Lee HM, Wysoczynski M, Liu R, Shin DM, Kucia M, Botto M et al. Mobilization studies in complement-deficient mice reveal that optimal AMD3100 mobilization of hematopoietic stem cells depends on complement cascade activation by AMD3100-stimulated granulocytes. Leukemia 2009; 24: 573–582.

    Article  PubMed  PubMed Central  Google Scholar 

  62. Heissig B, Hattori K, Dias S, Friedrich M, Ferris B, Hackett NR et al. Recruitment of stem and progenitor cells from the bone marrow niche requires MMP-9 mediated release of kit-ligand. Cell 2002; 109: 625–637.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Pelus LM, Bian H, King AG, Fukuda S . Neutrophil-derived MMP-9 mediates synergistic mobilization of hematopoietic stem and progenitor cells by the combination of G-CSF and the chemokines GRObeta/CXCL2 and GRObetaT/CXCL2delta4. Blood 2004; 103: 110–119.

    Article  CAS  PubMed  Google Scholar 

  64. Jujo K, Hamada H, Iwakura A, Thorne T, Sekiguchi H, Clarke T et al. CXCR4 blockade augments bone marrow progenitor cell recruitment to the neovasculature and reduces mortality after myocardial infarction. Proc Natl Acad Sci USA 2010; 107: 11008–11013.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Heissig B, Lund LR, Akiyama H, Ohki M, Morita Y, Romer J et al. The plasminogen fibrinolytic pathway is required for hematopoietic regeneration. Cell Stem Cell 2007; 1: 658–670.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Binder BR, Mihaly J, Prager GW . uPAR-uPA-PAI-1 interactions and signaling: a vascular biologist's view. Thromb Haemost 2007; 97: 336–342.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This study was partially supported by the Helen and Martin Kimmel Institute for Stem Cell Research at the Weizmann Institute, Israeli Science Foundation grant 544/09, the European Union (Advance Cell-based Therapies for the Treatment of Primary Immunodeficiency HEALTH-F5-2010-261387) and the Legacy Heritage Fund (TL). PSF is an established investigator of the American Heart Association supported by the National Institutes of Health. This work was also partially supported by Grant-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science, and Technology of Japan (SO and NF). TL holds The Edith Arnoff Stein Professorial Chair in Stem Cell Research. We would like to thank Dr Abraham Avigdor for supplying us with human BM aspirations from healthy donors and to Dr Scott Cooper for performing experiments with Anormed-derived AMD3100. Our special thanks to Drs Sara Rankin, Isabelle Petit, Shoham Shivtiel and Jonathan Canaani for fruitful discussions and for critically reviewing the manuscript.

Author information

Author notes

  1. A Dar, A Schajnovitz and K Lapid: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Immunology, Weizmann Institute of Science, Rehovot, Israel

    A Dar, A Schajnovitz, K Lapid, A Kalinkovich, T Itkin, A Ludin, M Tesio, O Kollet, N N Cohen, R Margalit, E C Buss & T Lapidot

  2. Department of Medicine, Immunology Institute, and Black Family Stem Cell Institute, Mount Sinai School of Medicine, New York, NY, USA

    W-M Kao, M Battista & P S Frenette

  3. Institute Pasteur, Paris, France

    F Baleux

  4. Graduate School of Pharmaceutical Sciences, Kyoto University, Sakyo-ku, Kyoto, Japan,

    S Oishi & N Fujii

  5. Molecular Hematopoiesis Section, Hematology Branch, National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, MA, USA

    A Larochelle & C E Dunbar

  6. Department of Microbiology and Immunology, Indiana University School of Medicine, Indianapolis, IN, USA

    H E Broxmeyer

Authors
  1. A Dar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A Schajnovitz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. K Lapid
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. A Kalinkovich
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. T Itkin
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. A Ludin
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. W-M Kao
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. M Battista
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. M Tesio
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. O Kollet
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. N N Cohen
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. R Margalit
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. E C Buss
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. F Baleux
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. S Oishi
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. N Fujii
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. A Larochelle
    View author publications

    You can also search for this author in PubMed Google Scholar

  18. C E Dunbar
    View author publications

    You can also search for this author in PubMed Google Scholar

  19. H E Broxmeyer
    View author publications

    You can also search for this author in PubMed Google Scholar

  20. P S Frenette
    View author publications

    You can also search for this author in PubMed Google Scholar

  21. T Lapidot
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to T Lapidot.

Ethics declarations

Competing interests

The authors declare no conflict of interest.

Additional information

Supplementary Information accompanies the paper on the Leukemia website

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dar, A., Schajnovitz, A., Lapid, K. et al. Rapid mobilization of hematopoietic progenitors by AMD3100 and catecholamines is mediated by CXCR4-dependent SDF-1 release from bone marrow stromal cells. Leukemia 25, 1286–1296 (2011). https://doi.org/10.1038/leu.2011.62

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/leu.2011.62

Keywords

This article is cited by

Search

Advanced search

Quick links