International Journal of Hematology

, Volume 74, Issue 1, pp 9–17

Regulation of Hematopoiesis by Chemokine Family Members

Progress in hematology


Chemokines, originally designated as chemoattractant cytokines, comprise a large family of molecules that have been implicated in a number of different functions mediated through chemokine receptors. Among these functions are regulatory roles in hematopoiesis that encompass effects on the proliferation, survival, and homing/migration of myeloid progenitor cells. This article reviews the field of chemokine regulation of hematopoiesis at the level of myeloid progenitor cells.

Key words

Chemokines Stem/progenitor cells Proliferation Survival Migration/homing 


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  1. 1.
    Broxmeyer HE. Role of cytokines in hematopoiesis. In: Oppenheim JJ, Rossio JL,Gearing AJH, eds.Clinical Aspects of Cytokines: Role in Pathogenesis, Diagnosis and Therapy. New York, NY: Oxford University Press; 1993:201–206.Google Scholar
  2. 2.
    Broxmeyer HE. The hematopoietic system: principles of therapy with hematopoietically active cytokines. In: Ganser A, Hoelzer D, eds.Cytokines in the Treatment of Hematopoietic Failure. 1999. New York, NY: Marcel Dekker; 1999:1–37.Google Scholar
  3. 3.
    Cooper S, Broxmeyer HE. Measurement of interleukin-3 and other hematopoietic growth factors, such as GM-CSF, G-CSF, M-CSF, erythropoietin and the potent co-stimulating cytokines Steel factor and Flt-3 ligand. In: Coligan JE, Kruisbeek AM, Margulies DH, Shevach EM, Strober W, Coico R, eds.Current Protocols in Immunology. Suppl 18. New York, NY: John Wiley & Sons; 1996:6.4.1–6.4.12.Google Scholar
  4. 4.
    Broxmeyer HE, Maze R, Miyazawa K, et al. The Kit receptor and its ligand, Steel factor, as regulators of hemopoiesis.Cancer Cells. 1991;3:480–487.PubMedGoogle Scholar
  5. 5.
    Broudy V. Stem cell factor and hematopoiesis.Blood. 1997;90:1345–1364.PubMedGoogle Scholar
  6. 6.
    Lyman SD, Jacobsen SEW. c-kit ligand and Flt3 ligand: stem/progenitor cell factors with overlapping but distinct activities.Blood. 1998;91:1101–1134.PubMedGoogle Scholar
  7. 7.
    Williams DE, Hangoc G, Cooper S, et al. The in vivo effects of purified recombinant IL-3 and purified natural CSF-1 on murine high proliferative potential colony forming cells: demonstration of in vivo synergism.Blood. 1987;70:401–403.PubMedGoogle Scholar
  8. 8.
    Broxmeyer HE, Williams DE, Hangoc G, et al. Synergistic myelopoietic action in vivo of combinations of purified natural murine colony stimulating factor-1, recombinant murine interleukin-3, and recombinant murine granulocyte-macrophage colony stimulating factor administered to mice.Proc Natl Acad Sci U S A. 1987;84:3871–3875.PubMedCrossRefGoogle Scholar
  9. 9.
    Broxmeyer HE, Williams DE, Cooper S, Hangoc G, Ralph P. Recombinant human granulocyte-colony stimulating factor and recombinant human macrophage-colony stimulating factor synergize in vivo to enhance proliferation of granulocyte-macrophage, erythroid and multipotential progenitor cells in mice.J Cell Biochem. 1988;38:127–136.PubMedCrossRefGoogle Scholar
  10. 10.
    Broxmeyer HE, Kim CH. Chemokines and hematopoiesis. In: Rollins BJ, ed.Chemokines and Cancer. Totowa, NJ: Humana Press; 1999:263–291.Google Scholar
  11. 11.
    Broxmeyer HE, Kim CH. Regulation of hematopoiesis in a sea of chemokine family members with a plethora of redundant activities.Exp Hematol. 1999;27:1113–1123.PubMedCrossRefGoogle Scholar
  12. 12.
    Rollins BJ. Chemokines.Blood. 1997;90:909–928.PubMedGoogle Scholar
  13. 13.
    Baggiolini M, Dewald B, Moser B. Human chemokines: an update.Annu Rev Immunol. 1997;15:675–705.PubMedCrossRefGoogle Scholar
  14. 14.
    Luster AD. Chemokines-chemotactic cytokines that mediate inflammation.N Engl J Med. 1998;12:436–445.CrossRefGoogle Scholar
  15. 15.
    Kim CH, Broxmeyer HE. Chemokines: signal lamps for trafficking of T- and B-cells for development and effector function.J Leuk Biol. 1999;65:6–15.Google Scholar
  16. 16.
    Zlotnik A, Yoshie O. Chemokines: a new classification system and their role in immunity.Immunity. 2000;12:121–127.PubMedCrossRefGoogle Scholar
  17. 17.
    Broxmeyer HE. Suppressor cytokines and regulation of myelopoiesis: biology and possible clinical uses.Am J Pediatr Hematol Oncol. 1992;14:22–30.PubMedCrossRefGoogle Scholar
  18. 18.
    Broxmeyer HE. Myelosuppressive cytokines and peptides. In: Whetton T, Gordon T, eds.Hemopoietic Growth Factors. London, UK: Plenum; 1996:121–150.Blood Cell Biochemistry; vol. 7.Google Scholar
  19. 19.
    Broxmeyer HE, Sherry B, Lu L, et al. Myelopoietic enhancing effects of murine macrophage inflammatory proteins 1 and 2 in vitro on colony formation by murine and human bone marrow granulocyte-macrophage progenitor cells.J Exp Med. 1989;170:1583–1594.PubMedCrossRefGoogle Scholar
  20. 20.
    Graham GJ, Wright EG, Hewick R, et al. Identification and characterization of an inhibitor of haemopoietic stem cell proliferation.Nature. 1990;344:442–444.PubMedCrossRefGoogle Scholar
  21. 21.
    Broxmeyer HE, Sherry B, Lu L, et al. Enhancing and suppressing effects of recombinant murine macrophage inflammatory proteins on colony formation in vitro by bone marrow myeloid progenitor cells.Blood. 1990;76:1110–1116.PubMedGoogle Scholar
  22. 22.
    Broxmeyer HE, Sherry B, Cooper S, et al. Macrophage inflammatory protein (MIP)-1α abrogates the capacity of MIP-1α to suppress myeloid progenitor cell growth.J Immunol. 1991;147:2586–2594.PubMedGoogle Scholar
  23. 23.
    Clements JM, Craig S, Gearing AJH, et al. Biological and structural properties of MIP-1α expressed in yeast.Cytokine. 1992;4:76–82.PubMedCrossRefGoogle Scholar
  24. 24.
    Maze R, Sherry B, Kwon BS, Cerami A, Broxmeyer HE. Myelosuppressive effects in vivo of purified recombinant murine macrophage inflammatory protein-1 alpha.J Immunol. 1992;149:1004–1009.PubMedGoogle Scholar
  25. 25.
    Cooper S, Mantel C, Broxmeyer HE. Myelosuppressive effects in vivo with very low dosage of monomeric recombinant murine macrophage inflammatory protein-1α.Exp Hematol. 1994;22:186–193.PubMedGoogle Scholar
  26. 26.
    Dunlop DJ, Wright EG, Lorimore S, et al. Demonstration of stem cell inhibition and myeloprotective effects of SCI/rhuMIP-1α in vivo.Blood. 1992;79:2221–2225.PubMedGoogle Scholar
  27. 27.
    Lord BI, Dexter TM, Clements JM, Hunter MA, Gearing AJH. Macrophage-inflammatory protein protects multipotent hematopoietic cells from the cytotoxic effects of hydroxyurea in vivo.Blood. 1992;79:2605–2609.PubMedGoogle Scholar
  28. 28.
    Broxmeyer HE, Sherry B, Cooper S, et al. Comparative analysis of the suppressive effects of the human macrophage inflammatory protein family of cytokines (chemokines) on proliferation of human myeloid progenitor cells.J Immunol. 1993;150:3448–3458.PubMedGoogle Scholar
  29. 29.
    Lu L, Xiao M, Grigsby S, et al. Comparative effects of suppressive cytokines on isolated single CD34+++ stem/progenitor cells from human bone marrow and umbilical cord blood plated with and without serum.Exp Hematol. 1993;21:1442–1446.PubMedGoogle Scholar
  30. 30.
    Mantel C, Kim Y-J, Cooper S, Kwon B, Broxmeyer HE. Polymerization of murine macrophage inflammatory protein-1α inactivates its myelosuppressive effects in vitro. The active form is monomer.Proc Natl Acad Sci U S A. 1993;90:2232–2236.PubMedCrossRefGoogle Scholar
  31. 31.
    Broxmeyer HE, Cooper S, Hague N, et al. Human chemokines: enhancement of specific activity and effects in vitro on normal and leukemic progenitors and a factor dependent cell line and in vivo in mice.Ann Hematol. 1995;71:235–246.PubMedCrossRefGoogle Scholar
  32. 32.
    Hunter MG, Bawden L, Brotherton D, et al. BB10010: an active variant of human macrophage inflammatory protein-1α with improved pharmaceutical properties.Blood. 1995;86:4400–4408.PubMedGoogle Scholar
  33. 33.
    Broxmeyer HE, Orazi A, Hague NL, Sledge GW Jr, Rasmussen H, Gordon MS. Myeloid progenitor cell proliferation and mobilization effects of BB10010, a genetically engineered variant of human macrophage inflammatory protein-1α, in a phase I clinical trial in patients with relapsed/refractory breast cancer.Blood Cells Mol Dis. 1998;24:14–30.PubMedCrossRefGoogle Scholar
  34. 34.
    Daly TJ, LaRosa GJ, Dolich S, Maione TE, Cooper S, Broxmeyer HE. High activity suppression of myeloid progenitor proliferation by chimeric mutants of interleukin 8 and platelet factor 4.J Biol Chem. 1995;270:23282–23292.PubMedCrossRefGoogle Scholar
  35. 35.
    Crow M, Taub DD, Cooper S, Broxmeyer HE, Sarris AH. Human recombinant interferon-inducible protein-10: intact disulfide bridges are not required for inhibition of hematopoietic progenitors and chemotaxis of T lymphocytes and monocytes.J Hematother Stem Cell Res. 2001;10:147–156.PubMedCrossRefGoogle Scholar
  36. 36.
    Broxmeyer HE. Regulation of myelopoiesis as assessed by gene deletion and gene transduction. In: Zon LI, ed.Hematopoiesis. A Developmental Approach. New York, NY: Oxford University Press; 2001:247–257.Google Scholar
  37. 37.
    Broxmeyer HE, Cooper S, Cacalano G, Hague NL, Bailish E, Moore MW Interleukin-8 receptor is involved in negative regulation of myeloid progenitor cells in vivo: evidence from mice lacking the murine IL-8 receptor homolog.J Exp Med. 1996;184:1825–1832.PubMedCrossRefGoogle Scholar
  38. 38.
    Boring L, Gosling J, Chensue SW, et al. Impaired monocyte migration and reduced Type 1 (Th1) cytokine responses in CCR2 knockout mice.J Clin Invest. 1997;100:2552–2561.PubMedCrossRefGoogle Scholar
  39. 39.
    Reid S, Ritchie A, Boring L, et al. Enhanced myeloid progenitor cell cycling and apoptosis in mice lacking the chemokine receptor, CCR2.Blood. 1999;93:1524–1533.PubMedGoogle Scholar
  40. 40.
    Gao JL, Wynn TA, Chang Y, et al. Impaired host defense, hematopoiesis, granulomatous inflammation and type 1/type 2 cytokine balance in mice lacking cc chemokine receptor 1.J Exp Med. 1997;185:1959–1968.PubMedCrossRefGoogle Scholar
  41. 41.
    Broxmeyer HE, Cooper S, Hangoc G, Gao J-L, Murphy PM. Dominant myelopoietic effector functions mediated by chemokine receptor CCR1.J Exp Med. 1999;189:1987–1992.PubMedCrossRefGoogle Scholar
  42. 42.
    Broxmeyer HE, Youn BS, Kim CH, Hangoc G, Cooper S, Mantel C. Chemokine regulation of hematopoiesis and the involvement of pertussis toxin-sensitive Gai proteins.NY Acad Sci. 2001;938:117–128.CrossRefGoogle Scholar
  43. 43.
    Hall RA, Premont RT, Lefkowitz RJ. Heptahelical receptor signaling: beyond the G-protein paradigm.J Cell Biol. 1999;145:927–932.PubMedCrossRefGoogle Scholar
  44. 44.
    Aronica SM, Mantel C, Gonin R, et al. Interferon-inducible protein 10 and macrophage inflammatory protein-1α inhibit growth factor stimulation of Raf-1 kinase activity and protein synthesis in a human growth factor-dependent hematopoietic cell line.J Biol Chem. 1995;270:21998–22007.PubMedCrossRefGoogle Scholar
  45. 45.
    Kim CH, Qu CK, Hangoc G, Cooper S, Feng GS, Broxmeyer HE. Abnormal chemokine-induced responses of immature and mature hematopoietic cells from motheaten mice implicates the protein tyrosine phosphatase SHP-1 in chemokine responses.J Exp Med. 1999;190:681–690.PubMedCrossRefGoogle Scholar
  46. 46.
    Kim CH, Hangoc G, Cooper S, et al. Altered responsiveness to chemokines due to targeted disruption of SHIP.J Clin Invest. 1999;104:1751–1759.PubMedCrossRefGoogle Scholar
  47. 47.
    Williams GT, Smith CA, Spooncer E, Dexter TM, Taylor DR. Haemopoietic colony stimulating factors promote cell survival by suppressing apoptosis.Nature. 1990;343:76–79.PubMedCrossRefGoogle Scholar
  48. 48.
    Blalock WL, Weinstein-Oppenheimer C, Chang F, et al. Signal transduction, cell regulatory, and anti-apoptotic pathways regulated by IL-3 in hematopoietic cells: possible sites for intervention with anti-neoplastic drugs.Leukemia. 1999;13:1109–1166.PubMedCrossRefGoogle Scholar
  49. 49.
    Ritchie A, Broxmeyer HE. Suppression of P53-mediated growth factor withdrawal induced apoptosis in the myeloid compartment by hematopoietic cytokines: an overview of hematopoiesis and apoptosis with a presentation of thrombopoietin and the MO7e cell line as a model.Crit Rev Oncol Hematol. 1999;31:169–191.PubMedCrossRefGoogle Scholar
  50. 50.
    Israels LG, Israels ED. Apoptosis.Stem Cells. 1999;17:306–313.PubMedCrossRefGoogle Scholar
  51. 51.
    Wyllie AH. Apoptosis: cell death in tissue regulation.J Pathol. 1987;153:313–316.PubMedCrossRefGoogle Scholar
  52. 52.
    Cotter TG, Lennon SV, Glynn JM, Green DR. Microfilament-disrupting agents prevent formation of apoptotic bodies in tumor cells undergoing apoptosis.Cancer Res. 1992;52:997–1005.PubMedGoogle Scholar
  53. 53.
    Gorman AM, McGowan A, O’Neill C, Cotter T. Oxidative stress and apoptosis in neurodegeneration.J Neurol Sci. 1996;139:45–52.PubMedCrossRefGoogle Scholar
  54. 54.
    Thompson HJ, Strange R, Schedin PJ. Apoptosis in the generation and prevention of cancer.Cancer Epidemiol Biomarkers Prev. 1992;1:597–602.PubMedGoogle Scholar
  55. 55.
    Thompson CB. Apoptosis in the pathogenesis and treatment of disease.Science. 1995;267:1456–1462.PubMedCrossRefGoogle Scholar
  56. 56.
    Tashiro K, Tada H, Heilker R, Shirozu M, Nakano T, Honjo T. Signal sequence trap: a cloning strategy for secreted protein and type 1 membrane proteins.Science. 1993;261:600–603.PubMedCrossRefGoogle Scholar
  57. 57.
    Nagasawa T, Kikutani H, Kishimoto T. Molecular cloning and structure of a pre-B-cell growth stimulating factor.Proc Natl Acad Sci U S A. 1994;91:2305–2309.PubMedCrossRefGoogle Scholar
  58. 58.
    Zlotnik A, Morales J, Hedrick JA. Recent advances in chemokines and chemokine receptors.Crit Rev Immunol. 1999;19:1–47.PubMedGoogle Scholar
  59. 59.
    Nagasawa T, Hirota S, Tachibana K, et al. Defects of B lymphopoiesis and bone marrow myelopoiesis in mice lacking the CXC chemokine PBSF/SDF-1.Nature. 1996;382:635–638.PubMedCrossRefGoogle Scholar
  60. 60.
    Ma Q, Jones D, Borghesani PR, et al. Impaired B lymphopoiesis, myelopoiesis and derailed cerebellar neuron migration in CXCR4-and SDF-deficient mice.Proc Natl Acad Sci U S A. 1998;95:9448–9453.PubMedCrossRefGoogle Scholar
  61. 61.
    Zou YR, Kohmann AH, Kuroda M,Taniuchi L, Littman DR. Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development.Nature. 1998;393:595–599.PubMedCrossRefGoogle Scholar
  62. 62.
    Shirozu M, Nakano T, Inazawa J, et al. Structure and chromosomal localization of the human stromal cell-derived factor 1 (SDF1) gene.Genomics. 1995;28:495–500.PubMedCrossRefGoogle Scholar
  63. 63.
    Bleul CC, Fuhlbrigge RC, Casasnovas JM, Aiuti A, Springer TA. A highly efficacious lymphocyte chemoattractant, stromal cell-derived factor-1 (SDF-1).J Exp Med. 1996;184:1101–1109.PubMedCrossRefGoogle Scholar
  64. 64.
    Dealwis C, Fernandez EJ, Thompson DA, Simon RJ, Siani MA, Lolis E. Crystal structure of chemically synthesized (N33A) stromal-cell derived factor alpha, a potent ligand for the HIV-1 “fusion” coreceptor.Proc Natl Acad Sci U S A. 1998;95:6941–6946.PubMedCrossRefGoogle Scholar
  65. 65.
    Broxmeyer HE, Hangoc G, Cooper S, Kim CH. Enhanced myelopoiesis in SDF-1 transgenic mice: SDF-1 modulates myelopoiesis by regulating progenitor cell survival and inhibitory effects of myelosuppressive chemokines [abstract].Blood. 1999;94(suppl 1):650a.Google Scholar
  66. 66.
    Aiuti A, Webb IJ, 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.PubMedCrossRefGoogle Scholar
  67. 67.
    Kim CH, Broxmeyer HE. 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. 1998;91:100–110.PubMedGoogle Scholar
  68. 68.
    Mohle R, Bautz F, Rafii S, Moore MAS, Brugger W, Kanz L. 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. 1998;91:4523.PubMedGoogle Scholar
  69. 69.
    Gotoh A, Reid S, Miyazawa K, Broxmeyer HE. SDF-1 suppresses cytokine-induced adhesion of human hematopoietic progenitor cells to immobilized fibronectin.Brit J Haematol. 1999;106:171–174.CrossRefGoogle Scholar
  70. 70.
    Peled A, Kollet O, Ponomaryov T, et al. 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. 2000;95:3289–3296.PubMedGoogle Scholar
  71. 71.
    Peled A, Grabovsky V, Habler L, et al. The chemokine SDF-1 stimulates integrin-mediated arrest of CD34+ cells on vascular endothelium under shear flow.J Clin Invest. 1999;104:1199–1211.PubMedCrossRefGoogle Scholar
  72. 72.
    Ma Q, Jones D, Springer TA. The chemokine receptor CXCR4 is required for the retention of B lineage and granulocytic precursors within the bone marrow microenvironment.Immunity. 1999;10:463–471.PubMedCrossRefGoogle Scholar
  73. 73.
    Peled A, Petit I, Kollet O, et al. Dependence of human stem cell engraftment and repopulation of NOD/SCID mice on CXCR4.Science. 1999;283:845–848.PubMedCrossRefGoogle Scholar
  74. 74.
    Kim CH, Pelus LM, White JR, Broxmeyer HE. Differential chemotactic behavior of developing T cells in response to thymic chemokines.Blood. 1998;91:4434–4443.PubMedGoogle Scholar
  75. 75.
    Ganju RK, Brubaker SA, Meyer J, et al. The α-chemokine, stromal cell derived factor-1α, binds to the transmembrane G-protein-coupled CXCR4 receptor and activates multiple signal transduction pathways.J Biol Chem. 1998;273:23169–23175.PubMedCrossRefGoogle Scholar
  76. 76.
    Dutt P, Wang J-F, Groopman JE. Stromal cell-derived factor 1α and stem cell factor/kit ligand share signaling pathways in hematopoietic progenitors: a potential mechanism for cooperative induction of chemotaxis.J Immunol. 1998;161:3652–3658.PubMedGoogle Scholar
  77. 77.
    Vicente-Mannzannares M, Rey M, Jones DR, et al. Involvement of phosphatidylinositol 3-kinase in stromal cell-derived factor-1α-induced lymphocyte polarization and chemotaxis.J Immunol. 1999;163:4001–4012.Google Scholar
  78. 78.
    Vila-Coro AJ, Rodriguez-Frade JM, Marin de Ana A, Moreno-Ortiz MC, Martinez C, Mellado M. The chemokine SDF-1α triggers CXCR4 receptor dimerization and activates the Jak/Stat pathway.FASEB J. 1999;13:1699–1710.PubMedGoogle Scholar
  79. 79.
    Sotsias Y, Whittaker GC, Westwick J, Ward SG. The CXC chemokine stromal cell-derived factor activates a Gi-coupled phosphoinositide 3-kinase in T-lymphocytes.J Immunol. 1999;163:5954–5963.Google Scholar
  80. 80.
    Haddad E, Zugaza JL, Louache F, et al. The interaction between Cdc42 and WASP is required for SDF-1-induced T-lymphocyte chemotaxis.Blood. 2001;97:33–38.PubMedCrossRefGoogle Scholar
  81. 81.
    Chernock RD, Cerla RP, Ganju RK. SHP2 and cbl participate in α-chemokine receptor CXCR4-mediated signaling pathways.Blood. 2001;97:608–615.PubMedCrossRefGoogle Scholar
  82. 82.
    Cherla RP, Ganju RK. Stromal cell-derived factor 1α-induced chemotaxis in T cells is mediated by nitric oxide signaling pathways.J Immunol. 2001;166:3067–3074.PubMedGoogle Scholar
  83. 83.
    Kim CH, Pelus LM, White JR, Broxmeyer HE. CKβ-11/MIP-3β/ELC, a CC chemokine, is a chemoattractant with a specificity for macrophage progenitors amongst myeloid progenitor cells.J Immunol. 1998;161:2580–2585.PubMedGoogle Scholar
  84. 84.
    Kim CH, Broxmeyer HE. CCR7 and CXCR3 ligand SLC/Exodus 2/6 Ckine induces chemotaxis of hematopoietic progenitor cells: differential activity of ligands of CCR7, CXCR3, or CXCR4 in chemotaxis/actin polymerization vs. suppression of progenitor proliferation.J Leuk Biol. 1999;66:455–461.Google Scholar
  85. 85.
    Tilton B, Ho L, Oberlin E, et al. Signal transduction by CXC chemokine receptor 4: stromal cell-derived factor 1 stimulates prolonged protein kinase B and extracellular signal-regulated kinase 2 activation in T lymphocytes.J Exp Med. 2000;192:313–324.PubMedCrossRefGoogle Scholar
  86. 86.
    Sullivan SK, McGrath DA, Grigoriadis D, Bacon KB. Pharmacological and signaling analysis of human chemokine receptor CCR-7 stably expressed in HEK-293 cells: high affinity binding of recombinant ligands MIP-3beta and SLC stimulates multiple signaling cascades.Biochem Biophys Res Comm. 1999;263:685–690.PubMedCrossRefGoogle Scholar
  87. 87.
    Fagarasan S, Shinkura R, Kamata T, et al. Alymphosplasia (aly)-type nuclear factor kB-inducing kinase (NIK) causes defects in secondary lymphoid tissue chemokine receptor signaling and homing of peritoneal cells to the gut-associated lymphatic tissue system.J Exp Med. 2000;191:1477–1486.PubMedCrossRefGoogle Scholar
  88. 88.
    Jinquan T, Quan S, Jacobi HH, et al. CXC chemokine receptor 3 expression on CD34+ hematopoietic progenitors from human cord blood induced by granulocyte-macrophage colony-stimulating factor: chemotaxis and adhesion induced by its ligands, interferon γ-inducible protein 10 and monokine induced by interferon γ.Blood. 2000;96:1230–1238.PubMedGoogle Scholar
  89. 89.
    Hromas R, Cripe L, Hangoc G, Cooper S, Broxmeyer HE. The exodus subfamily of CC chemokines inhibit the proliferation of chronic myelogenous leukemia progenitors.Blood. 2000;95:1506–1508.PubMedGoogle Scholar

Copyright information

© The Japanese Society of Hematology 2001

Authors and Affiliations

  1. 1.Department of Microbiology and Immunology and the Walther Oncology CenterIndiana University School of Medicine and the Walther Cancer InstituteIndianapolis, IndianaUSA
  2. 2.Walther Oncology CenterIndiana University School of MedicineIndianapolisUSA

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