Experimental Hematology
Volume 38, Issue 4 , Pages 321-332 , April 2010

Fifth complement cascade protein (C5) cleavage fragments disrupt the SDF-1/CXCR4 axis: Further evidence that innate immunity orchestrates the mobilization of hematopoietic stem/progenitor cells

  • Ali Jalili

      Affiliations

    • Canadian Blood Services R & D, University of Alberta, Edmonton, Alberta, Canada
    • Department of Medicine, University of Alberta, Edmonton, Alberta, Canada
    • ,
  • Neeta Shirvaikar

      Affiliations

    • Canadian Blood Services R & D, University of Alberta, Edmonton, Alberta, Canada
    • Department of Medicine, University of Alberta, Edmonton, Alberta, Canada
    • ,
  • Leah Marquez-Curtis

      Affiliations

    • Canadian Blood Services R & D, University of Alberta, Edmonton, Alberta, Canada
    • ,
  • Yuanyuan Qiu

      Affiliations

    • Canadian Blood Services R & D, University of Alberta, Edmonton, Alberta, Canada
    • ,
  • Chris Korol

      Affiliations

    • Department of Medicine, University of Alberta, Edmonton, Alberta, Canada
    • ,
  • HakMo Lee

      Affiliations

    • University of Louisville, Louisville, Ky., USA
    • ,
  • A. Robert Turner

      Affiliations

    • Department of Medicine, University of Alberta, Edmonton, Alberta, Canada
    • ,
  • Mariusz Z. Ratajczak

      Affiliations

    • University of Louisville, Louisville, Ky., USA
    • ,
  • Anna Janowska-Wieczorek

      Affiliations

    • Canadian Blood Services R & D, University of Alberta, Edmonton, Alberta, Canada
    • Department of Medicine, University of Alberta, Edmonton, Alberta, Canada
    • Corresponding Author InformationOffprint requests to: Anna Janowska-Wieczorek, M.D., Ph.D., Department of Medicine, University of Alberta, CBS Edmonton Centre, 8249-114 Street NW, Edmonton, Alberta T6G 2R8, Canada

Received 18 September 2009 ,Revised 15 January 2010 ,Accepted 5 February 2010.

References 

  1. Levesque JP, Winkler IG. Mobilization of hematopoietic stem cells: state of the art. Curr Opin Organ Transplant. 2008;13:53–58
  2. Pelus LM. Peripheral blood stem cell mobilization: new regimens, new cells, where do we stand. Curr Opin Hematol. 2008;15:285–292
  3. 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
  4. Lee H, Ratajczak MZ. Innate immunity: a key player in the mobilization of hematopoietic stem/progenitor cells. Arch Immunol Ther Exp. 2009;57:1–9
  5. 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
  6. Guo R-F, Ward PA. Role of C5a in inflammatory responses. Annu Rev Immunol. 2005;23:821–852
  7. Lee H, Whitfield PL, Mackay CR. Receptors for complement C5a. The importance of C5aR and the enigmatic role of C5L2. Immunol Cell Biol. 2008;86:153–160
  8. Monk PN, Scola A-M, Madala P, Fairlie DP. Function, structure and therapeutic potential of complement C5a receptors. Br J Pharmacol. 2007;152:429–448
  9. Burger R, Zilow G. Complement-derived anaphylatoxins in natural immunity. In:  Sim E editors. The Natural Immune System: Humoral Factors. New York: Oxford; 1993;p. 209
  10. Sekhsaria S, Fleisher TA, Vowells S, et al. Granulocyte colony-stimulating factor recruitment of CD34+ progenitors to peripheral blood: impaired mobilization in chronic granulomatous disease and adenosine deaminase-deficient severe combined immunodeficiency disease patients. Blood. 1996;88:1104–1112
  11. Reca R, Mastellos D, Majka M, et al. Functional receptor for C3a anaphylatoxin is expressed by normal hematopoietic stem/progenitor cells, and C3a enhances their homing-related responses to SDF-1. Blood. 2003;101:3784–3793
  12. Ratajczak MZ, Reca R, Wysoczynski M, Yan J, Ratajczak J. Modulation of the SDF-1−CXCR4 axis by third complement component (C3)—Implications for trafficking of CXCR4+ stem cells. Exp Hematol. 2006;34:986–995
  13. Ratajczak J, Reca R, Kucia M, et al. Mobilization studies in mice deficient in either C3 or C3a receptor (C3aR) reveal a novel role for complement in retention of hematopoietic stem/progenitor cells in bone marrow. Blood. 2004;103:2071–2078
  14. Reca R, Cramer D, Yan 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
  15. McQuibban GA, Butler GS, Gong JH, et al. Matrix metalloproteinase activity inactivates the CXC chemokine stromal cell-derived factor-1. J Biol Chem. 2001;276:43503–43508
  16. Marquez-Curtis L, Jalili A, Deiteren K, et al. Carboxypeptidase M expressed by human bone marrow cells cleaves the C-terminal lysine of stromal cell-derived factor 1 alpha: another player in hematopoietic stem/progenitor cell mobilization?. Stem Cells. 2008;26:1211–1220
  17. Majka M, Janowska-Wieczorek A, Ratajczak J, et al. Numerous growth factors, cytokines, and chemokines are secreted by human CD34+ cells, myeloblasts, erythroblasts, and megakaryoblasts and regulate normal hematopoiesis in an autocrine/paracrine manner. Blood. 2001;97:3075–3085
  18. Son BR, Marquez-Curtis LA, Kucia M, et al. Migration of bone marrow and cord blood mesenchymal stem cells in vitro is regulated by stromal-derived factor-1-CXCR4 and hepatocyte growth factor-c-met axes and involves matrix metalloproteinases. Stem Cells. 2006;24:1254–1264
  19. Lee HM, Wu W, Wysoczynski M, et al. Impaired mobilization of hematopoietic stem/progenitor cells in C5-deficient mice supports the pivotal involvement of innate immunity in this process and reveals novel promobilization effects of granulocytes. Leukemia. 2009;23:2052–2062
  20. 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
  21. Janowska-Wieczorek A, Marquez LA, Nabholtz JM, et al. Growth factors and cytokines upregulate gelatinase expression in bone marrow CD34+ cells and their transmigration through reconstituted basement membrane. Blood. 1999;93:3379–3390
  22. Kim HK, De La Luz Sierra M, Williams CK, Gulino AV, Tosato G. G-CSF down-regulation of CXCR4 expression identified as a mechanism for mobilization of myeloid cells. Blood. 2006;108:812–820
  23. Bensinger W, DiPersio JF, McCarty JM. Improving stem cell mobilization strategies: future directions. Bone Marrow Transplant. 2009;43:181–195
  24. Wysoczynski M, Reca R, Lee H, Wu W, Ratajczak J, Ratajczak MZ. Defective engraftment of C3aR-/- hematopoietic stem cells reveals a novel role of the C3a-C3aR axis in bone marrow homing. Leukemia. 2009;23:1455–1461
  25. Prujit JF, Verzaal P, van Os R, et al. Neutrophils are indispensable for hematopoietic stem cell mobilization induced by interleukin-8 in mice. Proc Natl Acad Sci U S A. 2002;99:6228–6233
  26. Molineux G, McCrea C, Yan XQ, Kerzic P, McNiece I. Flt-3 ligand synergizes with granulocyte colony-stimulating factor to increase neutrophil numbers and to mobilize peripheral blood stem cells with long-term repopulating potential. Blood. 1997;89:3998–4004
  27. Furze RC, Rankin SM. Neutrophil mobilization and clearance in the bone marrow. Immunology. 2008;125:281–288
  28. 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;3:687–694
  29. Winkler IG, Levesque J-P. Mechanisms of hematopoietic stem cell mobilization: when innate immunity assails the cells that make blood and bone. Exp Hematol. 2006;34:996–1009
  30. Valenzuela-Fernandez A, Planchenault T, Baleux F, et al. Leukocyte elastase negatively regulates stromal cell-derived factor-1 (SDF-1)/CXCR4 binding and functions by amino-terminal processing of SDF-1 and CXCR4. J Biol Chem. 2002;277:15677–15689
  31. Delgado MB, Clark-Lewis I, Loetscher P, et al. Rapid inactivation of stromal cell-derived factor-1 by cathepsin G associated with lymphocytes. Eur J Immunol. 2001;31:699–707
  32. Christopherson KW. 2nd, Cooper S, Broxmeyer HE. Cell surface peptidase CD26/DPPIV mediates G-CSF mobilization of mouse progenitor cells. Blood. 2003;101:4680–4686
  33. DiScipio RG, Schraufstatter IU, Sikora L, Zuraw BL, Srimarao P. C5a mediates secretion and activation of matrix metalloproteinase 9 from human eosinophils and neutrophils. Int Immunopharmacol. 2006;6:1109–1118
  34. Jin F, Zhai Q, Qiu L, et al. Degradation of BM SDF-1 by MMP-9: the role in G-CSF-induced hematopoietic stem/progenitor cell mobilization. Bone Marrow Transplant. 2008;42:581–588
  35. Barbolina MV, Stack MS. Membrane type 1-matrix metalloproteinase: substrate diversity in pericellular proteolysis. Semin Cell Dev Biol. 2008;19:24–33
  36. Shirvaikar N, Reca R, Jalili A, et al. CFU-Meg progenitors ex vivo-expanded from cord blood maintain their in vitro homing potential and express matrix metalloproteinases. Cytotherapy. 2008;10:182–192
  37. Gálvez BG, Matías Román S, Albar JP, et al. Membrane type 1-matrix metalloproteinase is activated during migration of human endothelial cells and modulates endothelial motility and matrix remodelling. J Biol Chem. 2001;276:37491–37500
  38. Matías Román S, Gálvez BG, Genis L, et al. Membrane type 1-matrix metalloproteinase is involved in migration of human monocytes and is regulated through their interaction with fibronectin or endothelium. Blood. 2005;105:3956–3964
  39. Vagima Y, Avigdor A, Goichberg P, et al. MT1-MMP and RECK are involved in human CD34+ progenitor cell retention, egress and mobilization. J Clin Invest. 2009;119:492–503
  40. De La Luz Sierra MD, Yang FQ, Narazaki M, et al. Differential processing of stromal-derived factor 1-alpha and stromal-derived factor-1 beta explains functional diversity. Blood. 2004;103:2452–2459
  41. Levesque JP, Hendy J, Takamatsu Y, Williams B, Winkler IG, Simmons PJ. Mobilization by either cyclophosphamide or granulocyte colony-stimulating factor transforms the bone marrow into a highly proteolytic environment. Exp Hematol. 2002;5:440–449
  42. Velders GA, Fibbe WE. Involvement of proteases in cytokine-induced hematopoietic stem cell mobilization. Ann NY Acad Sci. 2005;1044:60–69
  43. Christopher MJ, Liu F, Hilton MJ, Long F, Link DC. Suppression of CXCL12 production by BM osteoblasts is a common and critical pathway for cytokine-induced mobilization. Blood. 2009;114:1331–1339

PII: S0301-472X(10)00046-9

doi: 10.1016/j.exphem.2010.02.002

Experimental Hematology
Volume 38, Issue 4 , Pages 321-332 , April 2010

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