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Digestive Diseases and Sciences

, Volume 55, Issue 2, pp 285–291 | Cite as

G-CSF Enhanced SDF-1 Gradient Between Bone Marrow and Liver Associated with Mobilization of Peripheral Blood CD34+ Cells in Rats with Acute Liver Failure

  • Yan Lei
  • Zhengwen LiuEmail author
  • Qunying Han
  • Wen Kang
  • Lei Zhang
  • Sai Lou
Original Article

Abstract

The role of stromal cell-derived factor-1 (SDF-1) in modulating massive liver damage is not well known. In this study, expression of SDF-1 in bone marrow and liver was investigated in rats with acute liver failure (ALF) when mobilized using granulocyte colony-stimulating factor (G-CSF). ALF was induced in rats by D-galactosamine (D-GalN). Starting after 2 hours following D-GalN induction, the animals were injected with G-CSF 50 μg/kg daily or saline as placebo for 5 days. The percentages of CD34+ cells in peripheral blood and the expression of SDF-1 in bone marrow and liver were then determined. The percentages of peripheral CD34+ cells demonstrated a transient increase in placebo rats following D-GalN induction and a significant increase in rats after G-CSF administration. SDF-1 expression showed a transient decrease in bone marrow and a transient increase in liver tissue from placebo rats. However, a significant decrease of SDF-1 expression in bone marrow and a remarkable increase in liver tissue were observed in animals from the G-CSF group. It was concluded that G-CSF can enhance the reduced expression of SDF-1 in bone marrow and increased expression in liver in ALF rats, forming a greater SDF-1 gradient, and chemoattracting CD34+ cells’ migration from bone marrow to an injured liver.

Keywords

Acute liver failure Granulocyte colony-stimulating factor Stem cell mobilization Stromal cell-derived factor-1 

Notes

Acknowledgments

This work was supported by Provincial Science and Technological Program of Shaanxi Province, PR China (2007K14-02). We are indebted to Dr. Xianling Liu from the Eastern Virginia Medical School in Virginia Beach, VA, USA, for her editorial assistance. We also thank Ms. Robin Solit and Mr. Perry Roland from USA for their helpful proofreading.

References

  1. 1.
    Bernuau J, Rueff B, Benhamou JP. Fulminant and subfulminant liver failure: definitions and causes. Semin Liver Dis. 1986;6(2):97–106. doi: 10.1055/s-2008-1040593.CrossRefPubMedGoogle Scholar
  2. 2.
    O’Grady JG, Schalm SW, Williams R. Acute liver failure: redefining the syndromes. Lancet. 1993;342(8866):273–275. doi: 10.1016/0140-6736(93)91818-7.CrossRefPubMedGoogle Scholar
  3. 3.
    Bernal W, Wendon J. Liver transplantation in adults with acute liver failure. J Hepatol. 2004;40(2):192–197. doi: 10.1016/j.jhep.2003.11.020.CrossRefPubMedGoogle Scholar
  4. 4.
    Kondo M, Wagers AJ, Manz MG, et al. Biology of hematopoietic stem cells and progenitors: implications for clinical application. Annu Rev Immunol. 2003;21:759–806. doi: 10.1146/annurev.immunol.21.120601.141007.CrossRefPubMedGoogle Scholar
  5. 5.
    Ferrari G, Cusella-De Angelis G, Coletta M, et al. Muscle regeneration by bone marrow-derived myogenic progenitors. Science. 1998;279(5356):1528–1530. doi: 10.1126/science.279.5356.1528.CrossRefPubMedGoogle Scholar
  6. 6.
    Hassink RJ, Brutel de la Rivière A, Mummery CL, Doevendans PA. Transplantation of cells for cardiac repair. J Am Coll Cardiol. 2003;41(5):711–717. doi: 10.1016/S0735-1097(02)02933-9.CrossRefPubMedGoogle Scholar
  7. 7.
    Mezey E, Chandross KJ, Harta G, Maki RA, McKercher SR. Turning blood into brain: cells bearing neuronal antigens generated in vivo from bone marrow. Science. 2000;290(5497):1779–1782. doi: 10.1126/science.290.5497.1779.CrossRefPubMedGoogle Scholar
  8. 8.
    Di Campli C, Zocco MA, Saulnier N, et al. Safety and efficacy profile of G-CSF therapy in patients with acute on chronic liver failure. Dig Liver Dis. 2007;39(12):1071–1076. doi: 10.1016/j.dld.2007.08.006.CrossRefPubMedGoogle Scholar
  9. 9.
    Theocharis SE, Papadimitriou LJ, Retsou ZP, Margeli AP, Ninos SS, Papadimitriou JD. Granulocyte-colony stimulating factor administration ameliorates liver regeneration in animal model of fulminant hepatic failure and encephalopathy. Dig Dis Sci. 2003;48(9):1797–1803. doi: 10.1023/A:1025463532521.CrossRefPubMedGoogle Scholar
  10. 10.
    Yannaki E, Athanasiou E, Xagorari A, et al. G-CSF-primed hematopoietic stem cells or G-CSF per se accelerate recovery and improve survival after liver injury, predominantly by promoting endogenous repair programs. Exp Hematol. 2005;33(1):108–119. doi: 10.1016/j.exphem.2004.09.005.CrossRefPubMedGoogle Scholar
  11. 11.
    Gaia S, Smedile A, Omedè P, et al. Feasibility and safety of G-CSF administration to induce bone marrow-derived cells mobilization in patients with end stage liver disease. J Hepatol. 2006;45(1):13–19. doi: 10.1016/j.jhep.2006.02.018.CrossRefPubMedGoogle Scholar
  12. 12.
    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(12):4307–4317. doi: 10.1182/blood.V99.12.4307.CrossRefPubMedGoogle Scholar
  13. 13.
    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(1):111–120. doi: 10.1084/jem.185.1.111.CrossRefPubMedGoogle Scholar
  14. 14.
    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(1):44–51. doi: 10.1182/blood.V99.1.44.CrossRefPubMedGoogle Scholar
  15. 15.
    Kortesidis A, Zannettino A, Isenmann S, Shi S, Lapidot T, Gronthos S. Stromal-derived factor-1 promotes the growth, survival, and development of human bone marrow stromal stem cells. Blood. 2005;105(10):3793–3801. doi: 10.1182/blood-2004-11-4349.CrossRefPubMedGoogle Scholar
  16. 16.
    Hatch HM, Zheng D, Jorgensen ML, Petersen BE. SDF-1alpha/CXCR4: a mechanism for hepatic oval cell activation and bone marrow stem cell recruitment to the injured liver of rats. Cloning Stem Cells. 2002;4(4):339–351. doi: 10.1089/153623002321025014.CrossRefPubMedGoogle Scholar
  17. 17.
    Petit I, Szyper-Kravitz M, Nagler A, et al. G-CSF induces stem cell mobilization by decreasing bone marrow SDF-1 and up-regulating CXCR4. Nat Immunol. 2002;3(7):687–694. doi: 10.1038/ni813.CrossRefPubMedGoogle Scholar
  18. 18.
    Stroncek DF, Clay ME, Petzoldt ML, et al. Treatment of normal individuals with granulocyte-colony-stimulating factor: donor experiences and the effects on peripheral blood CD34+ cell counts and on the collection of peripheral blood stem cells. Transfusion. 1996;36(7):601–610. doi: 10.1046/j.1537-2995.1996.36796323059.x.CrossRefPubMedGoogle Scholar
  19. 19.
    Rumi C, Rutella S, Teofili L, et al. RhG-CSF-mobilized CD34+ peripheral blood progenitors are myeloperoxidase-negative and noncycling irrespective of CD33 or CD13 coexpression. Exp Hematol. 1997;25(3):246–251.PubMedGoogle Scholar
  20. 20.
    Harada M, Qin Y, Takano H, et al. G-CSF prevents cardiac remodeling after myocardial infarction by activating the Jak-Stat pathway in cardiomyocytes. Nat Med. 2005;11(3):305–311. doi: 10.1038/nm1199.CrossRefPubMedGoogle Scholar
  21. 21.
    Rossi D, Zlotnik A. The biology of chemokines and their receptors. Annu Rev Immunol. 2000;18:217–242. doi: 10.1146/annurev.immunol.18.1.217.CrossRefPubMedGoogle Scholar
  22. 22.
    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(6685):595–599. doi: 10.1038/31269.CrossRefPubMedGoogle Scholar
  23. 23.
    Ponomaryov T, Peled A, Petit I, et al. Induction of the chemokine stromal-derived factor-1 following DNA damage improves human stem cell function. J Clin Invest. 2000;106(11):1331–1339. doi: 10.1172/JCI10329.CrossRefPubMedGoogle Scholar
  24. 24.
    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(9):1199–1211. doi: 10.1172/JCI7615.CrossRefPubMedGoogle Scholar
  25. 25.
    Sipkins DA, Wei X, Wu JW, et al. In vivo imaging of specialized bone marrow endothelial microdomains for tumour engraftment. Nature. 2005;435(7044):969–973. doi: 10.1038/nature03703.CrossRefPubMedGoogle Scholar
  26. 26.
    Kiel MJ, Yilmaz OH, Iwashita T, Yilmaz OH, Terhorst C, Morrison SJ. SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell. 2005;121(7):1109–1121. doi: 10.1016/j.cell.2005.05.026.CrossRefPubMedGoogle Scholar
  27. 27.
    Dar A, Goichberg P, Shinder V, 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(10):1038–1046. doi: 10.1038/ni1251.CrossRefPubMedGoogle Scholar
  28. 28.
    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(9):973–981. doi: 10.1016/S0301-472X(02)00883-4.CrossRefPubMedGoogle Scholar
  29. 29.
    Papayannopoulou T. Bone marrow homing: the players, the playfield, and their evolving roles. Curr Opin Hematol. 2003;10(3):214–219. doi: 10.1097/00062752-200305000-00004.CrossRefPubMedGoogle Scholar
  30. 30.
    Taichman RS. Blood and bone: two tissues whose fates are intertwined to create the hematopoietic stem-cell niche. Blood. 2005;105(7):2631–2639. doi: 10.1182/blood-2004-06-2480.CrossRefPubMedGoogle Scholar
  31. 31.
    Taichman RS, Emerson SG. The role of osteoblasts in the hematopoietic microenvironment. Stem Cells. 1998;16(1):7–15.CrossRefPubMedGoogle Scholar
  32. 32.
    Takahashi T, Kalka C, Masuda H, et al. Ischemia- and cytokine-induced mobilization of bone marrow-derived endothelial progenitor cells for neovascularization. Nat Med. 1999;5(4):434–438. doi: 10.1038/7434.CrossRefPubMedGoogle Scholar
  33. 33.
    Wang Y, Haider HK, Ahmad N, Zhang D, Ashraf M. Evidence for ischemia-induced host-derived bone marrow cell mobilization into cardiac allografts. J Mol Cell Cardiol. 2006;41(3):478–487. doi: 10.1016/j.yjmcc.2006.06.074.CrossRefPubMedGoogle Scholar
  34. 34.
    Ratajczak MZ, Kucia M, Reca R, Majka M, Janowska-Wieczorek A, Ratajczak J. Stem cell plasticity revisited: CXCR4-positive cells expressing mRNA for early muscle, liver and neural cells ‘hide out’ in the bone marrow. Leukemia. 2004;18(1):29–40. doi: 10.1038/sj.leu.2403184.CrossRefPubMedGoogle Scholar
  35. 35.
    Hu X, Dai S, Wu WJ, et al. Stromal cell derived factor-1 alpha confers protection against myocardial ischemia/reperfusion injury: role of the cardiac stromal cell derived factor-1 alpha CXCR4 axis. Circulation. 2007;116(6):654–663. doi: 10.1161/CIRCULATIONAHA.106.672451.CrossRefPubMedGoogle Scholar
  36. 36.
    Saxena A, Fish JE, White MD, et al. Stromal cell-derived factor-1alpha is cardioprotective after myocardial infarction. Circulation. 2008;117(17):2224–2231. doi: 10.1161/CIRCULATIONAHA.107.694992.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  • Yan Lei
    • 1
  • Zhengwen Liu
    • 1
    Email author
  • Qunying Han
    • 1
  • Wen Kang
    • 1
  • Lei Zhang
    • 1
  • Sai Lou
    • 1
  1. 1.Department of Infectious DiseasesFirst Affiliated Hospital, School of Medicine, Xi’an Jiaotong UniversityXi’anPeople’s Republic of China

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