Experimental Hematology
Volume 34, Issue 8 , Pages 1010-1020 , August 2006

Peripheral blood stem cell mobilization: The CXCR2 ligand GROβ rapidly mobilizes hematopoietic stem cells with enhanced engraftment properties

  • Louis M. Pelus

      Affiliations

    • Corresponding Author InformationOffprint requests to: Louis M. Pelus, Ph.D., Department of Microbiology and Immunology and Walther Oncology Center, Indiana University School of Medicine, 950 West Walnut Street, Indianapolis, IN 46202
  • ,
  • Seiji Fukuda

References 

  1. McCredie KB, Hersch EM, Freireich EJ. Cells capable of colony formation in the peripheral blood of man. Science. 1971;171:293–294
  2. Kurnick JE, Robinson WA. Colony growth of human peripheral white blood cells in vitro. Blood. 1971;37:136–141
  3. Chervenick PA, Boggs DR. In vitro growth of granulocytic and mononuclear cell colonies from blood of normal individuals. Blood. 1971;37:131–135
  4. To LB, Haylock DN, Simmons PJ, Juttner CA. The biology and clinical uses of blood stem cells. Blood. 1997;89:2233–2258
  5. Papayannopoulou T. Current mechanistic scenarios in hematopoietic stem/progenitor cell mobilization. Blood. 2004;103:1580–1585
  6. Fruehauf S, Seggewiss R. Its moving day: factors affecting peripheral blood stem cell mobilization and strategies for improvement. Br J Haematol. 2003;122:360–375
  7. Thomas J, Liu F, Link DC. Mechanisms of mobilization of hematopoietic progenitors with granulocyte colony-stimulating factor. Curr Opin Hematol. 2002;9:183–189
  8. Kessinger A, Armitage JO. The evolving role of autologous peripheral blood stem cell transplantation following high-dose therapy for malignancies. Blood. 1991;77:211–213
  9. Goldman JM, Horowitz MM. The international bone marrow registry. Int J Hematol. 2002;76:393–397
  10. Ringden O, Remberger M, Runde V, et al. Faster engraftment of neutrophils and platelets with peripheral blood stem cells from unrelated donors: a comparison with marrow transplantation. Bone Marrow Transplant. 2000;26:6–8
  11. Benito AI, Diaz MA, Gonzales-Vicent M, Sevilla J, Madero L. Hematopoietic stem cell transplantation using umbilical cord blood progenitors: review of current clinical results. Bone Marrow Transplant. 2004;33:675–690
  12. Bensinger W, Singer J, Appelbaum FR, et al. Autologous transplantation with peripheral blood mononuclear cells collected after administration of recombinant granulocyte stimulating factor. Blood. 1993;81:3158–3163
  13. Blume KG, Thomas ED. A review of autologous hematopoietic cell transplantation. Biol Bone Marrow Transplant. 2000;6:1–12
  14. Kennedy J. Peripheral blood progenitor cell mobilization: a clinical review. Pharmacotherapy. 1998;18:3–8
  15. Welte K, Gabrilove J, Bronchud MH, Platzer E, Morstyn G. Filgrastim (r-metHuG-CSF): the first 10 years. Blood. 1996;88:1907–1929
  16. Stiff P, Gingrich R, Luger S, et al. A randomized phase 2 study of PBPC mobilization by stem cell factor and filgrastim in heavily pretreated patients with Hodgkin's disease or non-Hodgkin's lymphoma. Bone Marrow Transplant. 2000;26:471–481
  17. Croop JM, Cooper R, Fernandez C, et al. Mobilization and collection of peripheral blood CD34+ cells from patients with Fanconi anemia. Blood. 2001;98:2917–2921
  18. Anderlini P, Przepiorka D, Seong C, et al. Factors affecting mobilization of CD34+ cells in normal donors treated with filgrastim. Transfusion. 1997;37:507–512
  19. Schmitz N, Dreger P, Suttorp M, et al. Primary transplantation of allogeneic peripheral blood progenitor cells mobilized by Filgrastim (granulocyte colony-stimulating factor). Blood. 1995;85:1666–1672
  20. Aversa F, Tabilio A, Velardi A, et al. Treatment of high risk acute leukemia with T-cell-depleted stem cells from related donors with one fully mismatched HLA haplotype. N Eng J Med. 1998;339:1186–1193
  21. Reisner Y, Martelli MF. Transplantation tolerance induced by “mega dose” CD34+ cell transplants. Exp Hematol. 2000;28:119–127
  22. Lataillade JJ, Clay D, Dupuy C, et al. Chemokine SDF-1 enhances circulating CD34+ cell proliferation in synergy with cytokines: possible role in progenitor survival. Blood. 2000;95:756–768
  23. Broxmeyer HE, Kohli L, Kim CH. Stromal cell-derived factor-1/CXCL12 directly enhances survival/antiapoptosis of myeloid progenitor cells through CXCR4 and G(alpha)i proteins and enhances engraftment of competitive, repopulating stem cells. J Leukocyte Biol. 2003;73:630–638
  24. Broxmeyer HE, Cooper S, Kohli L, et al. Transgenic expression of stromal cell derived factor-1/CXCL12 enhances myeloid progenitor cell survival/anti-apoptosis in vitro in response to growth factor withdrawal and enhances myelopoiesis. J Immunol. 2003;170:421–429
  25. Lee Y, Gotoh A, Kwon HJ, et al. Enhancement of intracellular signaling associated with hematopoietic progenitor cell survival in response to SDF-1/CXCL12 in synergy with other cytokines. Blood. 2002;99:4307–4317
  26. Lataillade JJ, Clay D, Bourin P, et al. Stromal cell-derived factor 1 regulates primitive hematopoiesis by suppressing apoptosis and by promoting G0/G1 transition in CD34+ cells: evidence for an autocrine/paracrine mechanism. Blood. 2002;99:1117–1129
  27. Broxmeyer HE, Cooper S, Hangoc G, Kim KC. Stromal cell-derived factor-1/CXCL12 selectively counteracts inhibitory effects of myelosuppressive chemokines on hematopoietic progenitor cell proliferation in vitro. Stem Cells Dev. 2005;14:199–203
  28. 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
  29. 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
  30. Möhle R, Bautz F, Rafi S, Moore MAS, Brugger W, Kanz L. The chemokine receptor CXCR4 is expressed on CD34+ hematopoietic progenitors and leukemic cells and mediates transendothelial migration induced by stromal cell-derived factor-1. Blood. 1998;91:4523–4530
  31. 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
  32. Lapidot T, Kollet O. The essential roles of the chemokine SDF-1 and its receptor CXCR4 in human stem cell homing and repopulation of transplanted immune-deficient NOD/SCID and NOD/SCID/ß2mnull mice. Leukemia. 2002;16:1992–2203
  33. Christopherson KW, Hangoc G, Mantel CR, Broxmeyer HE. Modulation of hematopoietic stem cell homing and engraftment by CD26. Science. 2004;305:1000–1003
  34. Pelus LM, Broxmeyer HE. Chemokine axes in hematopoietic stem cell mobilization. 2006; Progress in Inflammation (In press).
  35. Lord BI, Woolford LB, Wood LM, et al. Mobilization of early hematopoietic progenitor cells with BB-10010: a genetically engineered variant of human macrophage inflammatory protein-1a. Blood. 1995;85:3412–3415
  36. Broxmeyer HE, Orazi A, Hague NL, Sledge GW, Rasmussen H, Gordon MS. Myeloid progenitor cell proliferation and mobilization effects of BB10010, a genetically engineered variant of human macrophage inflammatory protein-1a, in a phase I clinical trial in patients with relapsed/refractory breast cancer. Blood Cells, Molec, and Dis. 1998;24:14–30
  37. 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
  38. Pelus LM, Bian H, Fukuda S, Wong D, Merzouk A, Salari H. The CXCR4 agonist peptide, CTCE-0021, rapidly mobilizes polymorphonuclear neutrophils and hematopoietic progenitor cells into peripheral blood and synergizes with granulocyte colony-stimulating factor. Exp Hematol. 2005;33:295–307
  39. Merzouk A, Wong D, Salari H, Bian H, Fukuda S, Pelus LM. Rational design of chemokine SDF-1 analogs with agonist activity for the CXCR4 receptor and the capacity to rapidly mobilize PMN and hematopoietic progenitor cells in mice. Letters in Drug Design & Discovery. 2004;1:126–134
  40. Broxmeyer HE, Clapp DW, Orschell CM, 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
  41. Liles WC, Broxmeyer HE, Rodger E, et al. Mobilization of hematopoietic progenitor cells in healthy volunteers by AMD3100, a CXCR4 antagonist. Blood. 2003;102:2728–2730
  42. Hubel K, Liles WC, Broxmeyer HE, et al. Leukocytosis and mobilization of CD34+ hematopoietic progenitor cells by AMD3100, a CXCR4 antagonist. Supportive Cancer Therapy. 2004;1:165–172
  43. Devine SM, Flomenberg N, Vesole DH, et al. Rapid mobilization of CD34+ cells following administration of the CXCR4 antagonist AMD3100 to patients with multiple myeloma and Non-Hodgkin's lymphoma. J Clin Oncol. 2004;22:1095–1102
  44. Liles WC, Rodger E, Broxmeyer HE, et al. Augmented mobilization and collection of CD34+ hematopoietic cells from normal human volunteers stimulated with G-CSF by single-dose administration of AMD3100, a CXCR4 antagonist. Transfusion. 2004;45:295–300
  45. Shen H, Cheng T, Olszak I, et al. CXCR-4 desensitization is associated with tissue localization of hematopoietic progenitor cells. J Immunol. 2001;166:5027–5033
  46. Yang OO, Swanberg SL, Lu Z, et al. Enhanced inhibition of human immunodeficiency virus type 1 by met-stromal-derived factor 1b correlates with down-modulation of CXCR4. J Virol. 1999;73:4582–4589
  47. Laterveer L, Lindley IJD, Hamilton MS, Willemze R, Fibbe WE. Interleukin-8 induces rapid mobilization of hematopoietic stem cells with radioprotective capacity and long-term myelolymphoid repopulating ability. Blood. 1995;85:2269–2275
  48. Fibbe WE, Pruijt JFM, Velders G, et al. Biology of IL-8-induced stem cell mobilization. Ann N Y Acad Sci. 1999;872:71–82
  49. Laterveer L, Zijlmans JM, Lindley IJD, Hamilton MS, Willemze R, Fibbe WE. Improved survival of lethally irradiated recipient mice transplanted with circulating progenitor cells mobilized by IL-8 after pretreatment with stem cell factor. Exp Hematol. 1996;24:1387–1393
  50. King AG, Horowitz D, Levin SB, Farese AM, MacVittie TJ, Pelus LM. Rapid mobilization of murine hematopoietic stem cells with enhanced engraftment properties and evaluation of hematopoietic progenitor cell mobilization in rhesus monkeys by a single injection of SB-251353, a specific truncated form of the human CXC chemokine GROb. Blood. 2001;97:1534–1542
  51. Pelus LM, Horowitz D, Cooper SC, King AG. Peripheral blood stem cell mobilization. A role for CXC chemokines. Crit Rev Oncol Hematol. 2002;43:257–275
  52. King AG, Johanson K, Frey CA, et al. Identification of unique truncated KC/GROb chemokines with potent hematopoietic and anti-infective activities. J Immunol. 2000;164:3774–3782
  53. 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 GROb/CXCL2 and GRObT/CXCL2des4. Blood. 2004;103:110–119
  54. Wang J-B, Mukaida N, Zhang Y, Ito T, Nakao S, Matsushima K. Enhanced mobilization of hematopoietic progenitor cells by mouse MIP-2 and granulocyte colony-stimulating factor in mice. J Leukoc Biol. 1997;62:503–509
  55. Fukuda S, Bian H, King AG, Pelus LM. The CXC chemokine GROb mobilizes PBSC with enhanced homing capacity independent of the SDF-1/CXCR4 axis. Submitted. 2005;
  56. Ino K, Ageitos AG, Singh RK, Talmadge JE. Activation-induced T cell apoptosis by monocytes from stem cell products. Int Immunopharmacol. 2001;1:1307–1319
  57. Osawa M, Hanada K, Hamada H, Nakauchi H. Long-term lymphohematopoietic reconstitution by a single CD34-low/negative hematopoietic stem cell. Science. 1996;273:242–245
  58. Matsuzaki Y, Kinjo K, Mulligan RC, Okano H. Unexpectedly efficient homing capacity of purified murine hematopoietic stem cells. Immunity. 2004;20:87–93
  59. Liu B, Buckley SM, Lewis ID, Goldman AI, Wagner JE, van der Loo JC. Homing defect of cultured human hematopoietic cells in the NOD/SCID mouse is mediated by Fas/CD95. Exp Hematol. 2003;31:824–832
  60. 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
  61. Katayama Y, Hidalgo A, Furie BC, Vestweber D, Furie B, Frenette PS. PSGL-1 participates in E-selectin mediated progenitor homing to bone marrow: evidence for cooperation between E-selectin ligands and a4 integrin. Blood. 2003;102:2060–2067
  62. Papayannopoulou T, Priestly GV, Nakamoto B, Zafiropoulos V, Scott LM. Molecular pathways in bone marrow homing: dominant role of a4b1 over b2-integrins and selectins. Blood. 2001;98:2403–2411
  63. Vermeulen M, LePasteur F, Gagnerault M-C, Mary J-Y, Sainteny F, Lepault F. Role of adhesion molecules in the homing and mobilization of murine hematopoietic stem and progenitor cells. Blood. 1998;92:894–900
  64. Frenette PS, Subbarao S, Mazo IB, von Adrian UH, Wagner DD. Endothelial selectins and vascular cell adhesion molecule-1 promote hematopoietic progenitor homing to bone marrow. Proc Natl Acad Sci U S A. 1998;95:14423–14428
  65. Dercksen MW, Gerritsen WR, Rodenhuis S, et al. Expression of adhesion molecules on CD34+ cells: CD34+L-selectin+ cells predict a rapid platelet recovery after peripheral blood stem cell transplantation. Blood. 1995;85:3313–3319
  66. Voermans C, Kooi ML, Rodenhuis S, van der Lelie H, van der Schoot CE, Gerritsen WR. In vitro migratory capacity of CD34+ cells is related to hematopoietic recovery after autologous stem cell transplantation. Blood. 2001;91:100–110
  67. Foudi A, Zhang Y, Geay JF, et al. The hematopoietic reconstitution defect of mice lacking CXCR4 is related to an altered retention of hematopoietic cells in the bone marrow. Blood. 2004;104:38a
  68. Okada Y, Morodomi T, Enghid JJ, et al. Matrix metalloproteinase 2 from rheumatoid synovial fibroblasts. Purification and activation of the precursor and enzymic properties. Eur J Biochem. 1990;194:721–730
  69. Bonig H, Priestly GV, Nilsson SK, Jiang Y, Papayannopoulou T. PTX-sensitive signals in bone marrow homing of fetal and adult progenitor cells. Blood. 2004;104:2299–2306
  70. Wiesmann A, Spangrude GJ. Marrow engraftment of hematopoietic stem and progenitor cells is independent of Galphai-coupled chemokine receptors. Exp Hematol. 1999;27:946–955
  71. Kovach NL, Lin N, Yednock T, Harlan JM, Broudy VC. Stem cell factor modulates avidity of a4b1 and a5b1 integrins expressed on hematopoietic cell lines. Blood. 1995;85:159–167
  72. Solanilla A, Grosset C, Duchez P, et al. Flt3-ligand induces adhesion of haematopoietic progenitor cells via a very late antigen (VLA)-4- and VLA-5-dependent mechanism. Br J Haematol. 2003;120:782–786
  73. Lévesque J-P, Leavesley DI, Niutta S, Vadas M, Simmons PJ. Cytokines increase human hemopoietic cell adhesiveness by activation of very late antigen (VLA)-4 and VLA-5 integrins. J Exp Med. 1995;181:1815–1914
  74. Herrera C, Sanchez J, Torres A, Pascual A, Rueda A, Alvarez MA. Pattern of expression of CXCR4 and adhesion molecules by human CD34+ cells from different sources: role in homing efficiency in NOD/SCID mice. Hematologica. 2004;89:1037–1045
  75. Leone DR, Giza KGA, Dolinski BM, et al. An assessment of the mechanistic differences between two integrin a4b1 inhibitors, the monoclonal antibody TA-2 and the small molecule BIO5192, in rat experimental autoimmune encephalomyelitis. J Pharmacol Exp Ther. 2003;305:1150–1162
  76. Holyoake T, Jiang X, Eaves C, Eaves A. Isolation of a highly quiescent subpopulation of primitive leukemic cells in chronic myeloid leukemia. Blood. 1999;96:2056–2064
  77. Schluter C, Duchrow M, Wohlenberg C, et al. The cell-proliferation antigen of antibody Ki-67: a very large, ubiquitous nuclear protein with numerous repeated elements, representing a new kind of cell cycle-maintaining proteins. J Cell Biol. 1993;123:513–522
  78. Ramos-Desimone N, Moll UM, Quigley JP, French DL. Inhibition of matrix metalloproteinase-9 activation by a specific monoclonal antibody. Hybridoma. 1993;12:349–363
  79. Robinson SN, Pisarev VM, Chavez JM, Singh RK, Talmadge JE. Use of matrix metalloproteinase (MMP)-9 knockout mice demonstrates that MMP-9 activity is not absolutely required for G-CSF or Flt-3 ligand-induced hematopoietic progenitor cell mobilization or engraftment. Stem Cells. 2003;21:417–427
  80. Papayannopoulou T, Priestly GV, Bonig H, Nakamoto B. The role of G-protein signaling in hematopoietic stem/progenitor cell mobilization. Blood. 2003;101:4739–4747
  81. Dubois B, Masure S, Hurtenbach U, et al. Resistance of young gelatinase B-deficient mice to experimental autoimmune encephalomyelitis and necrotizing tail lesions. J Clin Invest. 1999;104:1507–1515
  82. Borregaard N, Cowland JB. Granules of the human neutrophilic polymorphonuclear leukocyte. Blood. 2000;89:3503–3521
  83. Masure S, Proost P, Van Damme J, Opdenakker G. Purification and identification of a 91-kDa neutrophil gelatinase. Release by the activating peptide interleukin-8. Eur J Biochem. 1991;198:391–398
  84. Fridman R, Re Bird , Hoyhtya M, et al. Expression of human recombinant 72 kDa gelatinase and tissue inhibitor of metalloproteinase-2 (TIMP-2): characterization of complex and free enzyme. Biochem J. 1993;289:411–416
  85. Goldberg GI, Strongin A, Collier IE, Genrich LT, Marmer BL. Interaction of 92-kDA type IV collagenase with the tissue inhibitor of metalloproteinases prevents dimerization, complex formation with interstitial collagenase, and activation of the proenzyme with stromelysin. J Biol Chem. 1992;267:4583–4591
  86. Olson MW, Gervasi DC, Mobashery S, Fridman R. Kinetic analysis of the binding of human matrix metalloproteinase-2 and -9 to tissue inhibitor of metalloproteinase (TIMP)-1 and TIMP-2. J Biol Chem. 1997;272:29975–29983
  87. Massova I, Kotra LP, Fridman R, Mobashery S. Matrix metalloproteinases: structures, evolution, and diversification. FASEB J. 1998;12:1075–1095
  88. Bode W, Fernandez-Catalan C, Tschesche H, Grams F, Nagase H, Maskos K. Structural properties of matrix metalloproteinases. Cell Mol Life Sci. 1999;55:639–652
  89. Visse R, Nagrase H. Matrix metalloproteinases and tissue inhibitors of metalloproteinases. Structure, function, and biochemistry. Circ Res. 2003;92:827–839
  90. Janowska-Wieczorek A, Marquez LA, Dobrowsky A, Ratajczak MZ, Cabuhat ML. Differential MMP and TIMP production by human marrow and peripheral blood CD34+ cells in response to chemokines. Exp Hematol. 2000;28:1274–1285
  91. Zaoui P, Barro C, Morel F. Differential expression and secretion of gelatinases and tissue inhibitor of metalloproteinase-1 during neutrophil adhesion. Biochim Biophys Acta. 1996;1290:101–112
  92. Kjeldsen L, Sengelov H, Lollike K, Nielsen MH, Borregaard N. Isolation and characterization of gelatinase granules from human neutrophils. Blood. 1994;83:1640–1649
  93. Itoh Y, Nagase H. Preferential inactivation of tissue inhibitor of metalloproteinase-1 that is bound to the precursor of matrix metalloproteinase 9 (progelatinase B) by human neutrophil elastase. J Biol Chem. 1995;270:16518–16521
  94. Alexander CM, Howard EW, Bissell MJ, Werb Z. Rescue of mammary epithelial cell apoptosis and entactin degradation by a TIMP-1 transgene. J Cell Biol. 1996;135:1669–1677
  95. Moore MAS, Hattori K, Heissig B, et al. Mobilization of endothelial and hematopoietic stem and progenitor cells by adenovector-mediated elevation of serum levels of SDF-1, VEGF and angiopoietin-1. Ann N Y Acad Sci. 2001;938:36–45

PII: S0301-472X(06)00242-6

doi: 10.1016/j.exphem.2006.04.004

Experimental Hematology
Volume 34, Issue 8 , Pages 1010-1020 , August 2006