Cellular and Molecular Life Sciences

, Volume 69, Issue 9, pp 1415–1423

Regulation of neutrophil trafficking from the bone marrow

Review

Abstract

Neutrophils are an essential component of the innate immune response and a major contributor to inflammation. Consequently, neutrophil homeostasis in the blood is highly regulated. Neutrophil number in the blood is determined by the balance between neutrophil production in the bone marrow and release from the bone marrow to blood with neutrophil clearance from the circulation. This review will focus on mechanisms regulating neutrophil release from the bone marrow. In particular, recent data demonstrating a central role for the chemokines CXCL12 and CXCL2 in regulating neutrophil egress from the bone marrow will be discussed.

Keywords

Neutrophils Granulocyte colony-stimulating factor (G-CSF) CXCR4 CXCR2 CXCL12 (stromal derived factor-1; SDF-1) CXCL1 CXCL2 Leukocyte trafficking WHIM syndrome 

References

  1. 1.
    Grau AJ, Boddy AW, Dukovic DA, Buggle F, Lichy C, Brandt T, Hacke W (2004) Leukocyte count as an independent predictor of recurrent ischemic events. Stroke 35(5):1147–1152PubMedCrossRefGoogle Scholar
  2. 2.
    Madjid M, Awan I, Willerson JT, Casscells SW (2004) Leukocyte count and coronary heart disease: implications for risk assessment. J Am Coll Cardiol 44(10):1945–1956PubMedCrossRefGoogle Scholar
  3. 3.
    Demetri GD, Griffin JD (1991) Granulocyte colony-stimulating factor and its receptor. Blood 78(11):2791–2808PubMedGoogle Scholar
  4. 4.
    Semerad CL, Liu F, Gregory AD, Stumpf K, Link DC (2002) G-CSF is an essential regulator of neutrophil trafficking from the bone marrow to the blood. Immunity 17(4):413–423PubMedCrossRefGoogle Scholar
  5. 5.
    Lieschke GJ, Grail D, Hodgson G, Metcalf D, Stanley E, Cheers C, Fowler KJ, Basu S, Zhan YF, Dunn AR (1994) Mice lacking granulocyte colony-stimulating factor have chronic neutropenia, granulocyte and macrophage progenitor cell deficiency, and impaired neutrophil mobilization. Blood 84(6):1737–1746PubMedGoogle Scholar
  6. 6.
    Liu F, Wu HY, Wesselschmidt R, Kornaga T, Link DC (1996) Impaired production and increased apoptosis of neutrophils in granulocyte colony-stimulating factor receptor-deficient mice. Immunity 5(5):491–501PubMedCrossRefGoogle Scholar
  7. 7.
    Molineux G, Migdalska A, Szmitkowski M, Zsebo K, Dexter TM (1991) The effects on hematopoiesis of recombinant stem cell factor (ligand for c-kit) administered in vivo to mice either alone or in combination with granulocyte colony-stimulating factor. Blood 78(4):961–966PubMedGoogle Scholar
  8. 8.
    Seymour JF, Lieschke GJ, Grail D, Quilici C, Hodgson G, Dunn AR (1997) Mice lacking both granulocyte colony-stimulating factor (CSF) and granulocyte-macrophage CSF have impaired reproductive capacity, perturbed neonatal granulopoiesis, lung disease, amyloidosis, and reduced long-term survival. Blood 90(8):3037–3049PubMedGoogle Scholar
  9. 9.
    Liu F, Poursine-Laurent J, Wu HY, Link DC (1997) Interleukin-6 and the granulocyte colony-stimulating factor receptor are major independent regulators of granulopoiesis in vivo but are not required for lineage commitment or terminal differentiation. Blood 90(7):2583–2590PubMedGoogle Scholar
  10. 10.
    Rosmarin AG, Yang Z, Resendes KK (2005) Transcriptional regulation in myelopoiesis: hematopoietic fate choice, myeloid differentiation, and leukemogenesis. Exp Hematol 33(2):131–143PubMedCrossRefGoogle Scholar
  11. 11.
    Cartwright GE, Athens JW, Wintrobe MM (1964) The kinetics of granulopoiesis in normal man. Blood 24:780–803PubMedGoogle Scholar
  12. 12.
    Dancey JT, Deubelbeiss KA, Harker LA, Finch CA (1976) Neutrophil kinetics in man. J Clin Invest 58(3):705–715PubMedCrossRefGoogle Scholar
  13. 13.
    Pillay J, den Braber I, Vrisekoop N, Kwast LM, de Boer RJ, Borghans JA, Tesselaar K, Koenderman L (2010) In vivo labeling with 2H2O reveals a human neutrophil lifespan of 5.4 days. Blood 116 (4):625–627Google Scholar
  14. 14.
    Rankin SM (2010) The bone marrow: a site of neutrophil clearance. J Leukoc Biol 88(2):241–251PubMedCrossRefGoogle Scholar
  15. 15.
    Thakur ML, Lavender JP, Arnot RN, Silvester DJ, Segal AW (1977) Indium-111-labeled autologous leukocytes in man. J Nucl Med 18(10):1014–1021PubMedGoogle Scholar
  16. 16.
    Suratt BT, Young SK, Lieber J, Nick JA, Henson PM, Worthen GS (2001) Neutrophil maturation and activation determine anatomic site of clearance from circulation. Am J Physiol Lung Cell Mol Physiol 281(4):L913–L921PubMedGoogle Scholar
  17. 17.
    Furze RC, Rankin SM (2008) Neutrophil mobilization and clearance in the bone marrow. Immunology 125(3):281–288PubMedCrossRefGoogle Scholar
  18. 18.
    Nagase H, Miyamasu M, Yamaguchi M, Imanishi M, Tsuno NH, Matsushima K, Yamamoto K, Morita Y, Hirai K (2002) Cytokine-mediated regulation of CXCR4 expression in human neutrophils. J Leukoc Biol 71(4):711–717PubMedGoogle Scholar
  19. 19.
    Martin C, Burdon PCE, Bridger G, Gutierrez-Ramos JC, Williams TJ, Rankin SM (2003) Chemokines acting via CXCR2 and CXCR4 control the release of neutrophils from the bone marrow and their return following senescence. Immunity 19(4):583–593PubMedCrossRefGoogle Scholar
  20. 20.
    Suratt BT, Petty JM, Young SK, Malcolm KC, Lieber JG, Nick JA, Gonzalo J-A, Henson PM, Worthen GS (2004) Role of the CXCR4/SDF-1 chemokine axis in circulating neutrophil homeostasis. Blood 104(2):565–571PubMedCrossRefGoogle Scholar
  21. 21.
    Eash KJ, Means JM, White DW, Link DC (2009) CXCR4 is a key regulator of neutrophil release from the bone marrow under basal and stress granulopoiesis conditions. Blood 113(19):4711–4719PubMedCrossRefGoogle Scholar
  22. 22.
    Campbell FR (1972) Ultrastructural studies of transmural migration of blood cells in the bone marrow of rats, mice and guinea pigs. Am J Anat 135(4):521–535PubMedCrossRefGoogle Scholar
  23. 23.
    Inoue S, Osmond DG (2001) Basement membrane of mouse bone marrow sinusoids shows distinctive structure and proteoglycan composition: a high resolution ultrastructural study. Anat Rec 264(3):294–304PubMedCrossRefGoogle Scholar
  24. 24.
    Burdon PCE, Martin C, Rankin SM (2008) Migration across the sinusoidal endothelium regulates neutrophil mobilization in response to ELR + CXC chemokines. Br J Haematol 142(1):100–108PubMedCrossRefGoogle Scholar
  25. 25.
    Lévesque JP, Hendy J, Takamatsu Y, Williams B, Winkler IG, Simmons PJ (2002) Mobilization by either cyclophosphamide or granulocyte colony-stimulating factor transforms the bone marrow into a highly proteolytic environment. Exp Hematol 30(5):440–449PubMedCrossRefGoogle Scholar
  26. 26.
    Opdenakker G, Fibbe WE, Van Damme J (1998) The molecular basis of leukocytosis. Immunol Today 19(4):182–189PubMedCrossRefGoogle Scholar
  27. 27.
    Etzioni A (2009) Genetic etiologies of leukocyte adhesion defects. Curr Opin Immunol 21(5):481–486PubMedCrossRefGoogle Scholar
  28. 28.
    Simmons PJ, Masinovsky B, Longenecker BM, Berenson R, Torok-Storb B, Gallatin WM (1992) Vascular cell adhesion molecule-1 expressed by bone marrow stromal cells mediates the binding of hematopoietic progenitor cells. Blood 80(2):388–395PubMedGoogle Scholar
  29. 29.
    Schweitzer KM, Dräger AM, van der Valk P, Thijsen SF, Zevenbergen A, Theijsmeijer AP, van der Schoot CE, Langenhuijsen MM (1996) Constitutive expression of E-selectin and vascular cell adhesion molecule-1 on endothelial cells of hematopoietic tissues. Am J Pathol 148(1):165–175PubMedGoogle Scholar
  30. 30.
    Scott LM, Priestley GV, Papayannopoulou T (2003) Deletion of alpha4 integrins from adult hematopoietic cells reveals roles in homeostasis, regeneration, and homing. Mol Cell Biol 23(24):9349–9360PubMedCrossRefGoogle Scholar
  31. 31.
    Burdon PCE, Martin C, Rankin SM (2005) The CXC chemokine MIP-2 stimulates neutrophil mobilization from the rat bone marrow in a CD49d-dependent manner. Blood 105(6):2543–2548PubMedCrossRefGoogle Scholar
  32. 32.
    Ley K, Laudanna C, Cybulsky MI, Nourshargh S (2007) Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat Rev Immunol 7(9):678–689PubMedCrossRefGoogle Scholar
  33. 33.
    Larangeira AP, Silva AR, Gomes RN, Penido C, Henriques MG, Castro-Faria-Neto HC, Bozza PT (2001) Mechanisms of allergen- and LPS-induced bone marrow eosinophil mobilization and eosinophil accumulation into the pleural cavity: a role for CD11b/CD18 complex. Inflamm Res 50(6):309–316PubMedCrossRefGoogle Scholar
  34. 34.
    Scharffetter-Kochanek K, Lu H, Norman K, van Nood N, Munoz F, Grabbe S, McArthur M, Lorenzo I, Kaplan S, Ley K, Smith CW, Montgomery CA, Rich S, Beaude AL (1998) Spontaneous skin ulceration and defective T cell function in CD18 null mice. J Exp Med 188(1):119–131PubMedCrossRefGoogle Scholar
  35. 35.
    Forlow SB, Schurr JR, Kolls JK, Bagby GJ, Schwarzenberger PO, Ley K (2001) Increased granulopoiesis through interleukin-17 and granulocyte colony-stimulating factor in leukocyte adhesion molecule-deficient mice. Blood 98(12):3309–3314PubMedCrossRefGoogle Scholar
  36. 36.
    Stark MA, Huo Y, Burcin TL, Morris MA, Olson TS, Ley K (2005) Phagocytosis of apoptotic neutrophils regulates granulopoiesis via IL-23 and IL-17. Immunity 22(3):285–294PubMedCrossRefGoogle Scholar
  37. 37.
    Rogowski O, Sasson Y, Kassirer M, Zeltser D, Maharshak N, Arber N, Halperin P, Serrov J, Sorkin P, Eldor A, Berliner S (1998) Down-regulation of the CD62L antigen as a possible mechanism for neutrophilia during inflammation. Br J Haematol 101(4):666–669PubMedCrossRefGoogle Scholar
  38. 38.
    Kassirer M, Zeltser D, Gluzman B, Leibovitz E, Goldberg Y, Roth A, Keren G, Rotstein R, Shapira I, Arber N, Berliner AS (1999) The appearance of L-selectin (low) polymorphonuclear leukocytes in the circulating pool of peripheral blood during myocardial infarction correlates with neutrophilia and with the size of the infarct. Clin Cardiol 22(11):721–726PubMedCrossRefGoogle Scholar
  39. 39.
    Robinson SD, Frenette PS, Rayburn H, Cummiskey M, Ullman-Culleré M, Wagner DD, Hynes RO (1999) Multiple, targeted deficiencies in selectins reveal a predominant role for P-selectin in leukocyte recruitment. Proc Natl Acad Sci USA 96(20):11452–11457PubMedCrossRefGoogle Scholar
  40. 40.
    Arbonés ML, Ord DC, Ley K, Ratech H, Maynard-Curry C, Otten G, Capon DJ, Tedder TF (1994) Lymphocyte homing and leukocyte rolling and migration are impaired in L-selectin-deficient mice. Immunity 1(4):247–260PubMedCrossRefGoogle Scholar
  41. 41.
    Heissig B, Hattori K, Dias S, Friedrich M, Ferris B, Hackett NR, Crystal RG, Besmer P, Lyden D, Moore MAS, Werb Z, Rafii S (2002) Recruitment of stem and progenitor cells from the bone marrow niche requires MMP-9 mediated release of kit-ligand. Cell 109(5):625–637PubMedCrossRefGoogle Scholar
  42. 42.
    Petit I, Szyper-Kravitz M, Nagler A, Lahav M, Peled A, Habler L, Ponomaryov T, Taichman RS, Arenzana-Seisdedos F, Fujii N, Sandbank J, Zipori D, Lapidot T (2002) G-CSF induces stem cell mobilization by decreasing bone marrow SDF-1 and up-regulating CXCR4. Nat Immunol 3(7):687–694PubMedCrossRefGoogle Scholar
  43. 43.
    Lévesque J-P, Hendy J, Winkler IG, Takamatsu Y, Simmons PJ (2003) Granulocyte colony-stimulating factor induces the release in the bone marrow of proteases that cleave c-KIT receptor (CD117) from the surface of hematopoietic progenitor cells. Exp Hematol 31(2):109–117PubMedCrossRefGoogle Scholar
  44. 44.
    Lévesque J-P, Hendy J, Takamatsu Y, Simmons PJ, Bendall LJ (2003) Disruption of the CXCR4/CXCL12 chemotactic interaction during hematopoietic stem cell mobilization induced by GCSF or cyclophosphamide. J Clin Invest 111(2):187–196PubMedGoogle Scholar
  45. 45.
    Levesque J, Liu F, Simmons PJ, Betsuyaku T, Senior RM, Pham C, Link DC (2004) Characterization of hematopoietic progenitor mobilization in protease-deficient mice. Blood 104(1):65–72PubMedCrossRefGoogle Scholar
  46. 46.
    Aiuti A, Webb IJ, Bleul C, Springer T, Gutierrez-Ramos JC (1997) 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 185(1):111–120PubMedCrossRefGoogle Scholar
  47. 47.
    Kawabata K, Ujikawa M, Egawa T, Kawamoto H, Tachibana K, Iizasa H, Katsura Y, Kishimoto T, Nagasawa T (1999) A cell-autonomous requirement for CXCR4 in long-term lymphoid and myeloid reconstitution. Proc Natl Acad Sci USA 96(10):5663–5667PubMedCrossRefGoogle Scholar
  48. 48.
    Shirozu M, Nakano T, Inazawa J, Tashiro K, Tada H, Shinohara T, Honjo T (1995) Structure and chromosomal localization of the human stromal cell-derived factor 1 (SDF1) gene. Genomics 28(3):495–500PubMedCrossRefGoogle Scholar
  49. 49.
    Semerad CL, Christopher MJ, Liu F, Short B, Simmons PJ, Winkler I, Levesque J, Chappel J, Ross FP, Link DC (2005) G-CSF potently inhibits osteoblast activity and CXCL12 mRNA expression in the bone marrow. Blood 106(9):3020–3027PubMedCrossRefGoogle Scholar
  50. 50.
    Ara T, Nakamura Y, Egawa T, Sugiyama T, Abe K, Kishimoto T, Matsui Y, Nagasawa T (2003) Impaired colonization of the gonads by primordial germ cells in mice lacking a chemokine, stromal cell-derived factor-1 (SDF-1). Proc Natl Acad Sci USA 100(9):5319–5323PubMedCrossRefGoogle Scholar
  51. 51.
    Sugiyama T, Kohara H, Noda M, Nagasawa T (2006) Maintenance of the hematopoietic stem cell pool by CXCL12-CXCR4 chemokine signaling in bone marrow stromal cell niches. Immunity 25(6):977–988PubMedCrossRefGoogle Scholar
  52. 52.
    Christopher MJ, Liu F, Hilton MJ, Long F, Link DC (2009) Suppression of CXCL12 production by bone marrow osteoblasts is a common and critical pathway for cytokine-induced mobilization. Blood 114(7):1331–1339PubMedCrossRefGoogle Scholar
  53. 53.
    Sierro F, Biben C, Martínez-Muñoz L, Mellado M, Ransohoff RM, Li M, Woehl B, Leung H, Groom J, Batten M, Harvey RP, Martínez-A C, Mackay CR, Mackay F (2007) Disrupted cardiac development but normal hematopoiesis in mice deficient in the second CXCL12/SDF-1 receptor, CXCR7. Proc Natl Acad Sci USA 104(37):14759–14764PubMedCrossRefGoogle Scholar
  54. 54.
    Berahovich RD, Zabel BA, Penfold MET, Lewén S, Wany Y, Miao Z, Gan L, Pereda J, Dias J, Slukvin II, McGrath KE, Jaen JC, Schall TJ (2010) CXCR7 protein is not expressed on human or mouse leukocytes. J Immunol 185(9):5130–5139PubMedCrossRefGoogle Scholar
  55. 55.
    Nagasawa T, Hirota S, Tachibana K, Takakura N, Nishikawa S, Kitamura Y, Yoshida N, Kikutani H, Kishimoto T (1996) Defects of B-cell lymphopoiesis and bone-marrow myelopoiesis in mice lacking the CXC chemokine PBSF/SDF-1. Nature 382(6592):635–638PubMedCrossRefGoogle Scholar
  56. 56.
    Zou YR, Kottmann AH, Kuroda M, Taniuchi I, Littman DR (1998) Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development. Nature 393(6685):595–599PubMedCrossRefGoogle Scholar
  57. 57.
    Tachibana K, Hirota S, Iizasa H, Yoshida H, Kawabata K, Kataoka Y, Kitamura Y, Matsushima K, Yoshida N, Nishikawa S, Kishimoto T, Nagasawa T (1998) The chemokine receptor CXCR4 is essential for vascularization of the gastrointestinal tract. Nature 393(6685):591–594PubMedCrossRefGoogle Scholar
  58. 58.
    Ma Q, Jones D, Borghesani PR, Segal RA, Nagasawa T, Kishimoto T, Bronson RT, Springer TA (1998) Impaired B-lymphopoiesis, myelopoiesis, and derailed cerebellar neuron migration in CXCR4- and SDF-1-deficient mice. Proc Natl Acad Sci USA 95(16):9448–9453PubMedCrossRefGoogle Scholar
  59. 59.
    Ma Q, Jones D, Springer TA (1999) The chemokine receptor CXCR4 is required for the retention of B lineage and granulocytic precursors within the bone marrow microenvironment. Immunity 10(4):463–471PubMedCrossRefGoogle Scholar
  60. 60.
    Tzeng Y, Li H, Kang Y, Chen W, Cheng W, Lai D (2011) Loss of Cxcl12/Sdf-1 in adult mice decreases the quiescent state of hematopoietic stem/progenitor cells and alters the pattern of hematopoietic regeneration after myelosuppression. Blood 117(2):429–439PubMedCrossRefGoogle Scholar
  61. 61.
    Liles WC, Broxmeyer HE, Rodger E, Wood B, Hübel K, Cooper S, Hangoc G, Bridger GJ, Henson GW, Calandra G, Dale DC (2003) Mobilization of hematopoietic progenitor cells in healthy volunteers by AMD3100, a CXCR4 antagonist. Blood 102(8):2728–2730PubMedCrossRefGoogle Scholar
  62. 62.
    Broxmeyer HE, Orschell CM, Clapp DW, Hangoc G, Cooper S, Plett PA, Liles WC, Li X, Graham-Evans B, Campbell TB, Calandra G, Bridger G, Dale DC, Srour EF (2005) Rapid mobilization of murine and human hematopoietic stem and progenitor cells with AMD3100, a CXCR4 antagonist. J Exp Med 201(8):1307–1318PubMedCrossRefGoogle Scholar
  63. 63.
    Hernandez PA, Gorlin RJ, Lukens JN, Taniuchi S, Bohinjec J, Francois F, Klotman ME, Diaz GA (2003) Mutations in the chemokine receptor gene CXCR4 are associated with WHIM syndrome, a combined immunodeficiency disease. Nat Genet 34(1):70–74PubMedCrossRefGoogle Scholar
  64. 64.
    Kawai T, Malech HL (2009) WHIM syndrome: congenital immune deficiency disease. Curr Opin Hematol 16(1):20–26PubMedCrossRefGoogle Scholar
  65. 65.
    Kawai T, Choi U, Cardwell L, DeRavin SS, Naumann N, Whiting-Theobald NL, Linton GF, Moon J, Murphy PM, Malech HL (2007) WHIM syndrome myelokathexis reproduced in the NOD/SCID mouse xenotransplant model engrafted with healthy human stem cells transduced with C-terminus-truncated CXCR4. Blood 109(1):78–84PubMedCrossRefGoogle Scholar
  66. 66.
    Walters KB, Green JM, Surfus JC, Yoo SK, Huttenlocher A (2010) Live imaging of neutrophil motility in a zebrafish model of WHIM syndrome. Blood 116(15):2803–2811PubMedCrossRefGoogle Scholar
  67. 67.
    Gulino AV, Moratto D, Sozzani S, Cavadini P, Otero K, Tassone L, Imberti L, Pirovano S, Notarangelo LD, Soresina R, Mazzolari E, Nelson DL, Notarangelo LD, Badolato R (2004) Altered leukocyte response to CXCL12 in patients with warts hypogammaglobulinemia, infections, myelokathexis (WHIM) syndrome. Blood 104(2):444–452PubMedCrossRefGoogle Scholar
  68. 68.
    Balabanian K, Lagane B, Pablos JL, Laurent L, Planchenault T, Verola O, Lebbe C, Kerob D, Dupuy A, Hermine O, Nicolas J, Latger-Cannard V, Bensoussan D, Bordigoni P, Baleux F, Le Deist F, Virelizier J, Arenzana-Seisdedos F, Bachelerie F (2005) WHIM syndromes with different genetic anomalies are accounted for by impaired CXCR4 desensitization to CXCL12. Blood 105(6):2449–2457PubMedCrossRefGoogle Scholar
  69. 69.
    Kawai T, Choi U, Whiting-Theobald NL, Linton GF, Brenner S, Sechler JMG, Murphy PM, Malech HL (2005) Enhanced function with decreased internalization of carboxy-terminus truncated CXCR4 responsible for WHIM syndrome. Exp Hematol 33(4):460–468PubMedCrossRefGoogle Scholar
  70. 70.
    Lagane B, Chow KYC, Balabanian K, Levoye A, Harriague J, Planchenault T, Baleux F, Gunera-Saad N, Arenzana-Seisdedos F, Bachelerie F (2008) CXCR4 dimerization and beta-arrestin-mediated signaling account for the enhanced chemotaxis to CXCL12 in WHIM syndrome. Blood 112(1):34–44PubMedCrossRefGoogle Scholar
  71. 71.
    McCormick PJ, Segarra M, Gasperini P, Gulino AV, Tosato G (2009) Impaired recruitment of Grk6 and beta-Arrestin 2 causes delayed internalization and desensitization of a WHIM syndrome-associated CXCR4 mutant receptor. PLoS ONE 4(12):e8102PubMedCrossRefGoogle Scholar
  72. 72.
    Busillo JM, Armando S, Sengupta R, Meucci O, Bouvier M, Benovic JL (2010) Site-specific phosphorylation of CXCR4 is dynamically regulated by multiple kinases and results in differential modulation of CXCR4 signaling. J Biol Chem 285(10):7805–7817PubMedCrossRefGoogle Scholar
  73. 73.
    Laterveer L, Lindley IJ, Hamilton MS, Willemze R, Fibbe WE (1995) Interleukin-8 induces rapid mobilization of hematopoietic stem cells with radioprotective capacity and long-term myelolymphoid repopulating ability. Blood 85(8):2269–2275PubMedGoogle Scholar
  74. 74.
    King AG, Horowitz D, Dillon SB, Levin R, Farese AM, MacVittie TJ, Pelus LM (2001) 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 GRObeta. Blood 97(6):1534–1542PubMedCrossRefGoogle Scholar
  75. 75.
    Eash KJ, Greenbaum AM, Gopalan PK, Link DC (2010) CXCR2 and CXCR4 antagonistically regulate neutrophil trafficking from murine bone marrow. J Clin Invest 120(7):2423–2431PubMedCrossRefGoogle Scholar
  76. 76.
    Köhler A, De Filippo K, Hasenberg M, van den Brandt C, Nye E, Hosking MP, Lane TE, Männ L, Ransohoff RM, Hauser AE, Winter O, Schraven B, Geiger H, Hogg N, Gunzer M (2011) G-CSF-mediated thrombopoietin release triggers neutrophil motility and mobilization from bone marrow via induction of Cxcr2 ligands. Blood 117(16):4349–4357PubMedCrossRefGoogle Scholar
  77. 77.
    Wengner AM, Pitchford SC, Furze RC, Rankin SM (2008) The coordinated action of G-CSF and ELR + CXC chemokines in neutrophil mobilization during acute inflammation. Blood 111(1):42–49PubMedCrossRefGoogle Scholar
  78. 78.
    Cacalano G, Lee J, Kikly K, Ryan AM, Pitts-Meek S, Hultgren B, Wood WI, Moore MW (1994) Neutrophil and B cell expansion in mice that lack the murine IL-8 receptor homolog. Science 265(5172):682–684PubMedCrossRefGoogle Scholar
  79. 79.
    Shuster DE, Kehrli ME, Ackermann MR (1995) Neutrophilia in mice that lack the murine IL-8 receptor homolog. Science 269(5230):1590–1591PubMedCrossRefGoogle Scholar
  80. 80.
    Broxmeyer HE, Cooper S, Cacalano G, Hague NL, Bailish E, Moore MW (1996) Involvement of Interleukin (IL) 8 receptor in negative regulation of myeloid progenitor cells in vivo: evidence from mice lacking the murine IL-8 receptor homologue. J Exp Med 184(5):1825–1832PubMedCrossRefGoogle Scholar
  81. 81.
    Kawakami M, Tsutsumi H, Kumakawa T, Abe H, Hirai M, Kurosawa S, Mori M, Fukushima M (1990) Levels of serum granulocyte colony-stimulating factor in patients with infections. Blood 76(10):1962–1964PubMedGoogle Scholar
  82. 82.
    Delano MJ, Kelly-Scumpia KM, Thayer TC, Winfield RD, Scumpia PO, Cuenca AG, Harrington PB, O’Malley KA, Warner E, Gabrilovich S, Mathews CE, Laface D, Heyworth PG, Ramphal R, Strieter RM, Moldawer LL, Efron PA (2011) Neutrophil mobilization from the bone marrow during polymicrobial sepsis is dependent on CXCL12 signaling. J Immunol 187(2):911–918PubMedCrossRefGoogle Scholar
  83. 83.
    Richardson RM, Tokunaga K, Marjoram R, Sata T, Snyderman R (2003) Interleukin-8-mediated heterologous receptor internalization provides resistance to HIV-1 infectivity: Role of signal strength and receptor desensitization. J Biol Chem 278(18):15867–15873PubMedCrossRefGoogle Scholar
  84. 84.
    Christopher MJ, Rao M, Liu F, Woloszynek JR, Link DC (2011) Expression of the G-CSF receptor in monocytic cells is sufficient to mediate hematopoietic progenitor mobilization by G-CSF in mice. J Exp Med 208(2):251–260PubMedCrossRefGoogle Scholar
  85. 85.
    Balabanian K, Levoye A, Klemm L, Lagane B, Hermine O, Harriague J, Baleux F, Arenzana-Seisdedos F, Bachelerie F (2008) Leukocyte analysis from WHIM syndrome patients reveals a pivotal role for GRK3 in CXCR4 signaling. J Clin Invest 118(3):1074–1084PubMedGoogle Scholar
  86. 86.
    Bradley ME, Bond ME, Manini J, Brown Z, Charlton SJ (2009) SB265610 is an allosteric, inverse agonist at the human CXCR2 receptor. Br J Pharmacol 158(1):328–338PubMedCrossRefGoogle Scholar
  87. 87.
    Holz O, Khalilieh S, Ludwig-Sengpiel A, Watz H, Stryszak P, Soni P, Tsai M, Sadeh J, Magnussen H (2010) SCH527123, a novel CXCR2 antagonist, inhibits ozone-induced neutrophilia in healthy subjects. Eur Respir J 35(3):564–570PubMedCrossRefGoogle Scholar
  88. 88.
    Lazaar AL, Sweeney LE, Macdonald AJ, Alexis NE, Chen C, Tal-Singer R (2011) SB-656933, a novel CXCR2 selective antagonist, inhibits ex vivo neutrophil activation and ozone-induced airway inflammation in humans. Br J Clin Pharmacol 72(2):282–293PubMedCrossRefGoogle Scholar
  89. 89.
    Burger JA, Peled A (2009) CXCR4 antagonists: targeting the microenvironment in leukemia and other cancers. Leukemia 23(1):43–52PubMedCrossRefGoogle Scholar
  90. 90.
    Lazennec G, Richmond A (2010) Chemokines and chemokine receptors: new insights into cancer-related inflammation. Trends Mol Med 16(3):133–144PubMedCrossRefGoogle Scholar
  91. 91.
    Hendrix CW, Flexner C, MacFarland RT, Giandomenico C, Fuchs EJ, Redpath E, Bridger G, Henson GW (2000) Pharmacokinetics and safety of AMD-3100, a novel antagonist of the CXCR-4 chemokine receptor, in human volunteers. Antimicrob Agents Chemother 44(6):1667–1673PubMedCrossRefGoogle Scholar
  92. 92.
    Hendrix CW, Collier AC, Lederman MM, Schols D, Pollard RB, Brown S, Jackson JB, Coombs RW, Glesby MJ, Flexner CW, Bridger GJ, Badel K, MacFarland RT, Henson GW, Calandra G (2004) Safety, pharmacokinetics, and antiviral activity of AMD3100, a selective CXCR4 receptor inhibitor, in HIV-1 infection. J Acquir Immune Defic Syndr 37(2):1253–1262PubMedCrossRefGoogle Scholar
  93. 93.
    McCandless EE, Wang Q, Woerner BM, Harper JM, Klein RS (2006) CXCL12 limits inflammation by localizing mononuclear infiltrates to the perivascular space during experimental autoimmune encephalomyelitis. J Immunol 177(11):8053–8064PubMedGoogle Scholar
  94. 94.
    Matthys P, Hatse S, Vermeire K, Wuyts A, Bridger G, Henson GW, De Clercq E, Billiau A, Schols D (2001) AMD3100, a potent and specific antagonist of the stromal cell-derived factor-1 chemokine receptor CXCR4, inhibits autoimmune joint inflammation in IFN-gamma receptor-deficient mice. J Immunol 167(8):4686–4692PubMedGoogle Scholar
  95. 95.
    Lukacs NW, Berlin A, Schols D, Skerlj RT, Bridger GJ (2002) AMD3100, a CxCR4 antagonist, attenuates allergic lung inflammation and airway hyperreactivity. Am J Pathol 160(4):1353–1360PubMedCrossRefGoogle Scholar
  96. 96.
    Xia X-M, Wang F-Y, Xu W-A, Wang Z-K, Liu J, Lu Y-K, Jin X-X, Lu H, Shen Y-Z (2010) CXCR4 antagonist AMD3100 attenuates colonic damage in mice with experimental colitis. World J Gastroenterol 16(23):2873–2880PubMedCrossRefGoogle Scholar

Copyright information

© Springer Basel AG 2011

Authors and Affiliations

  1. 1.Division of Oncology, Department of Internal MedicineWashington University School of MedicineSaint LouisUSA

Personalised recommendations