Experimental Hematology
Volume 38, Issue 11 , Pages 1087-1098 , November 2010

Activation of ephrin A proteins influences hematopoietic stem cell adhesion and trafficking patterns

  • Michael J. Ting

      Affiliations

    • Leukaemia Foundation of Queensland Research Unit, Queensland Institute of Medical Research, Brisbane, Australia
    • School of Medicine, Faculty of Health Sciences, University of Queensland, Brisbane, Australia
    • Corresponding Author InformationOffprint requests to: Michael J. Ting, Ph.D., University of Queensland Centre for Clinical Research, Tissue Repair and Inflammation Laboratory (Level 8), Building 71/918, RWBH Herston Campus, Herston, Queensland 4029, Australia
  • ,
  • Bryan W. Day

      Affiliations

    • Leukaemia Foundation of Queensland Research Unit, Queensland Institute of Medical Research, Brisbane, Australia
  • ,
  • Mark D. Spanevello

      Affiliations

    • Leukaemia Foundation of Queensland Research Unit, Queensland Institute of Medical Research, Brisbane, Australia
  • ,
  • Andrew W. Boyd

      Affiliations

    • Leukaemia Foundation of Queensland Research Unit, Queensland Institute of Medical Research, Brisbane, Australia
    • School of Medicine, Faculty of Health Sciences, University of Queensland, Brisbane, Australia

Received 21 June 2009 ,Revised 9 July 2010 ,Accepted 14 July 2010.

References 

  1. Avecilla S, Hattori K, Heissig B, et al. Chemokine-mediated interaction of hematopoietic progenitors with bone marrow vascular niches is required for thrombopoiesis. Nat Med. 2004;10:64–71
  2. Vermeulen M, Le Pesteur F, Gagnerault M, Mary J, 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
  3. 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
  4. Oates A, Lackmann M, Power M, et al. An early developmental role for eph-ephrin interaction during vertebrate gastrulation. Mech Dev. 1999;83:77–94
  5. Durbin L, Brennan C, Shiomi K, et al. Eph signaling is required for segmentation and differentiation of the somites. Genes Dev. 1998;12:3096–3109
  6. Lackmann M, Boyd AW. Eph, a protein family coming of age: more confusion, insight, or complexity?. Sci Signal. 2008;1:re2
  7. Himanen JP, Saha N, Nikolov DB. Cell-cell signaling via Eph receptors and ephrins. Curr Opin Cell Biol. 2007;19:534–542
  8. Eberhart J, Swartz M, Koblar SA, Pasquale EB, Tanaka H, Krull CE. Expression of EphA4, ephrin-A2 and ephrin-A5 during axon outgrowth to the hindlimb indicates potential roles in pathfinding. Dev Neurosci. 2000;22:237–250
  9. Coonan J, Greferath U, Messenger J, et al. Development and reorganization of corticospinal projections in EphA4 deficient mice. J Comp Neurol. 2001;436:248–262
  10. Birgbauer E, Oster SF, Severin CG, Sretavan DW. Retinal axon growth cones respond to EphB extracellular domains as inhibitory axon guidance cues. Development. 2001;128:3041–3048
  11. Adams R, Wilkinson G, Weiss C, et al. Roles of ephrinB ligands and EphB receptors in cardiovascular development: demarcation of arterial/venous domains, vascular morphogenesis, and sprouting angiogenesis. Genes Dev. 1999;13:295–306
  12. Batlle E, Henderson J, Beghtel H, et al. Beta-catenin and TCF mediate cell positioning in the intestinal epithelium by controlling the expression of EphB/ephrinB. Cell. 2002;111:251–263
  13. Holmberg J, Genander M, Halford M, et al. EphB receptors coordinate migration and proliferation in the intestinal stem cell niche. Cell. 2006;125:1151–1163
  14. Yu G, Luo H, Wu Y, Wu J. Mouse ephrinB3 augments T-cell signaling and responses to T-cell receptor ligation. J Biol Chem. 2003;278:47209–47216
  15. Freywald A, Sharfe N, Rashotte C, Grunberger T, Roifman CM. The EphB6 receptor inhibits JNK activation in T lymphocytes and modulates T cell receptor-mediated responses. J Biol Chem. 2003;278:10150–10156
  16. Ogawa K, Pasqualini R, Lindberg RA, Kain R, Freeman AL, Pasquale EB. The ephrin-A1 ligand and its receptor, EphA2, are expressed during tumor neovascularization. Oncogene. 2000;19:6043–6052
  17. Foo SS, Turner CJ, Adams S, et al. Ephrin-B2 controls cell motility and adhesion during blood-vessel-wall assembly. Cell. 2006;124:161–173
  18. Prevost N, Woulfe D, Tanaka T, Brass LF. Interactions between Eph kinases and ephrins provide a mechanism to support platelet aggregation once cell-to-cell contact has occurred. Pro Natl Acad Sci U S A. 2002;99:9219–9224
  19. Prevost N, Woulfe D, Jiang H, et al. Eph kinases and ephrins support thrombus growth and stability by regulating integrin outside-in signaling in platelets. Proc Natl Acad Sci U S A. 2005;102:9820–9825
  20. Dottori M, Down M, Huttmann A, Fitzpatrick DR, Boyd AW. Cloning and characterization of EphA3 (Hek) gene promoter: DNA methylation regulates expression in hematopoietic tumor cells. Blood. 1999;94:2477–2486
  21. Lazarova P, Wu Q, Kvalheim , et al. Growth factor receptors in hematopoietic stem cells: EPH family expression in CD34+ and CD133+ cell populations from mobilized peripheral blood. Int J Immunopathol Pharmacol. 2006;19:49–56
  22. Steube KG, Meyer C, Habig S, Uphoff CC, Drexler HG. Expression of receptor tyrosine kinase HTK (hepatoma transmembrane kinase) and HTK ligand by human leukemia-lymphoma cell lines. Leuk Lymphoma. 1999;33:371–376
  23. Inada T, Iwama A, Sakano S, Ohno M, Sawada K, Suda T. Selective expression of the receptor tyrosine kinase, HTK, on human erythroid progenitor cells. Blood. 1997;89:2757–2765
  24. Suenobu S, Takabura N, Inada T, et al. A role of EphB4 receptor and its ligand, ephrin-B2, in erythropoiesis. Biochem Biophys Res Commun. 2002;293:1124–1131
  25. Okubo T, Yanai N, Obinata M. Stromal cells modulate ephrinB2 expression and transmigration of hematopoietic cells. Exp Hematol. 2006;34:330–338
  26. Sharfe N, Feywald A, Toro A, Dadi H, Roifman C. Ephrin stimulation modulates T cell chemotaxis. Eur J Immunol. 2002;32:3745–3755
  27. Aasheim H, Delabie J, Finne E. Ephrin-A1 binding to CD4+ T lymphocytes stimulates migration and induces tyrosine phosphorylation of PYK2. Blood. 2004;105:2869–2876
  28. Duhrsen U, Novotny J, Boyd AW. Self-renewal of a transplantable murine leukemia induced by co-culture with human stromal cell lines. Leukemia. 1994;8:490–497
  29. Novotny JR, Duehrsen U, Welch K, Layton JE, Cebon JS, Boyd AW. Cloned stromal cell lines derived from human Whitlock/Witte-type long-term bone marrow cultures. Exp Hematol. 1990;18:775–784
  30. Leung LC, Johnson GR. In vitro maintenance of hemopoietic stem cells with lymphoid and myeloid repopulating ability by a cloned murine adherent bone marrow cell line. Exp Hematol. 1987;15:989–994
  31. Boyd AW, Ward LD, Wicks IP, et al. Isolation and characterization of a novel receptor-type protein tyrosine kinase (hek) from a human pre-B cell line. J Biol Chem. 1992;267:3262–3267
  32. Day B, Smith F, Chen K, et al. Eph/Ephrin membrane proteins: a mammalian expression vector pTIg-BOS-Fc allowing rapid protein purification. Protein Pept Lett. 2006;13:193–196
  33. Pfaffl MW. XXXX. In:  Bustin SA editors. Quantification Strategies in Real-Time PCR A-Z of Quantitative PCR. La Jolla, CA: International University Line; 2004;p. 87–120
  34. Goodell M, Brose K, Paradis G, Conner A, Mulligan R. Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J Exp Med. 1996;183:1797–1806
  35. Duffy SL, Steiner KA, Tam PP, Boyd AW. Expression analysis of the Epha1 receptor tyrosine kinase and its high-affinity ligands Efna1 and Efna3 during early mouse development. Gene Expr Patterns. 2006;6:719–723
  36. Flanagan JG, Vanderhaeghen P. The ephrins and Eph receptors in neural development. Annu Rev Neurosci. 1998;21:309–345
  37. Huai J, Drescher U. An ephrin-A-dependent signaling pathway controls integrin function and is linked to the tyrosine phosphorylation of a 120-kDa protein. J Biol Chem. 2001;276:6689–6694
  38. Davy A, Robbins SM. Ephrin-A5 modulates cell adhesion and morphology in an integrin-dependent manner. EMBO J. 2000;19:5396–53405
  39. Papayannopoulou T, Nakamoto B. Peripheralization of hemopoietic progenitors in primates treated with anti-VLA4 integrin. Proc Natl Acad Sci U S A. 1993;90:9374–9378
  40. Prosper F, Verfaillie CM. Regulation of hematopoiesis through adhesion receptors. J Leuk Biol. 2001;69:307–316
  41. Vearing C, Lee F, Wimmer-Kleikamp S, et al. Concurrent binding of anti-EphA3 antibody and ephrin-A5 amplifies EphA3 signaling and downstream responses: potential as EphA3-specific tumor-targeting reagents. Cancer Res. 2005;65:6745–6754
  42. Lackmann M, Mann R, Kravets L, et al. Ligand for EPH-related kinase (LERK) 7 is the preferred high affinity ligand for the HEK receptor. J Biol Chem. 1997;272:16521–16530
  43. Stier S, Ko Y, Forkett R, et al. Osteopontin is a hematopoietic stem cell niche component that negatively regulates stem cell pool size. J Exp Med. 2005;201:1781–1791
  44. Carlesso N, Aster J, Sklar J, Scadden D. Notch-1 induced delay of human hematopoietic progenitor cell differentiation is associated with altered cell cycle kinetics. Blood. 1999;93:838–848
  45. Sugiyama T, Kohara H, Noda M, et al. Maintenance of the hematopoietic stem cell pool by CXCL12-CXCR4 chemokine signaling in bone marrow stromal cell niches. Immunity. 2006;25:977–988
  46. Potocnik A, Brakebusch C, Fassler R. Fetal and adult hematopoietic stem cells require β1 integrin function for colonizing fetal liver, spleen, and bone marrow. Blood. 2000;12:653–663
  47. Prosper F, Stroncek D, McCarthy JB, Verfaillie CM. Mobilization and homing of peripheral blood progenitors is related to reversible downregulation of alpha4 beta1 integrin expression and function. J Clin Invest. 1998;101:2456–2467
  48. Lichterfeld M, Martin S, Burkly L, Haas R, Kronenwett R. Mobilization of CD34+ haematopoietic stem cells is associated with a functional inactivation of the integrin very late antigen 4. Br J Haematol. 2000;110:71–81
  49. Davy A, Gale N, Murray E, et al. Compartmentalized signaling by GPI-anchored ephrin-A5 requires the Fyn tyrosine kinase to regulate cellular adhesion. Genes Dev. 1999;13:3125–3135
  50. Aoki M, Yamashita T, Tohyama M. EphA receptors direct the differentiation of mammalian neural precursor cells through a mitogen-activated protein kinase-dependent pathway. J Biol Chem. 2004;279:32643–32650
  51. Depaepe V, Suarez-Gonzalez N, Dufour A, et al. Ephrin signalling controls brain size by regulating apoptosis of neural progenitors. Nature. 2005;435:1244–1250
  52. Holmberg J, Armulik A, Senti K, et al. Ephrin-A2 reverse signaling negatively regulates neural progenitor proliferation and neurogenesis. Genes Dev. 2005;19:462–471
  53. Ricard J, Salinas J, Garcia L, Liebl DJ. EphrinB3 regulates cell proliferation and survival in adult neurogenesis. Mol Cell Neurosci. 2006;31:713–722
  54. Conover J, Doetsch F, Garcia-Verdugo J, Gale N, Yancopoulos G, Alvarez-Bullya A. Disruption of Eph/ephrin signaling affects migration and proliferation in the adult subventricular zone. Nat Neurosci. 2000;3:1091–1097
  55. Stokowski A, Shi S, Sun T, Bartold P, Koblar S, Gronthos S. EphB/ephrin-B interaction mediates adult stem cell attachment, spreading, and migration: implications for dental tissue repair. Stem Cells. 2007;25:156–164
  56. Arthur A, Koblar S, Shi S, Gronthos S. Eph/ephrinB mediate dental pulp stem cell mobilization and function. J Dent Res. 2009;88:829–834

PII: S0301-472X(10)00288-2

doi: 10.1016/j.exphem.2010.07.007

Experimental Hematology
Volume 38, Issue 11 , Pages 1087-1098 , November 2010