Experimental Hematology
Volume 35, Issue 2 , Pages 314-325 , February 2007

Adhesion of hematopoietic progenitor cells to human mesenchymal stem cells as a model for cell−cell interaction

  • Wolfgang Wagner

      Affiliations

    • Department of Medicine V, University of Heidelberg, Heidelberg, Germany
    • Department of Physiology and Pathophysiology, University of Heidelberg, Heidelberg, Germany
  • ,
  • Frederik Wein

      Affiliations

    • Department of Medicine V, University of Heidelberg, Heidelberg, Germany
  • ,
  • Christoph Roderburg

      Affiliations

    • Department of Medicine V, University of Heidelberg, Heidelberg, Germany
  • ,
  • Rainer Saffrich

      Affiliations

    • Department of Medicine V, University of Heidelberg, Heidelberg, Germany
  • ,
  • Anne Faber

      Affiliations

    • Department of Medicine V, University of Heidelberg, Heidelberg, Germany
  • ,
  • Ulf Krause

      Affiliations

    • Department of Medicine V, University of Heidelberg, Heidelberg, Germany
  • ,
  • Mario Schubert

      Affiliations

    • Department of Medicine V, University of Heidelberg, Heidelberg, Germany
  • ,
  • Vladimir Benes

      Affiliations

    • Genomics Core Facility, European Molecular Biology Laboratory, Heidelberg, Germany
  • ,
  • Volker Eckstein

      Affiliations

    • Department of Medicine V, University of Heidelberg, Heidelberg, Germany
  • ,
  • Holger Maul

      Affiliations

    • Department of Obstetrics and Gynecology, University of Heidelberg, Heidelberg, Germany
  • ,
  • Anthony D. Ho

      Affiliations

    • Department of Medicine V, University of Heidelberg, Heidelberg, Germany
    • Corresponding Author InformationOffprint requests to: Anthony D. Ho, M.D., Department of Medicine V, University of Heidelberg, Im Neuenheimer Feld 410, 69120 Heidelberg, Germany

Received 22 June 2006 ,Revised 30 August 2006 ,Accepted 5 October 2006.

References 

  1. Schofield R. The relationship between the spleen colony-forming cell and the haemopoietic stem cell. Blood Cells. 1978;4:7–25
  2. Punzel M, Liu D, Zhang T, et al. The symmetry of initial divisions of human hematopoietic progenitors is altered only by the cellular microenvironment. Exp Hematol. 2003;31:339–347
  3. Ho AD, Punzel M. Hematopoietic stem cells: can old cells learn new tricks?. J Leukoc Biol. 2003;73:547–555
  4. Zhang J, Niu C, Ye L, et al. Identification of the haematopoietic stem cell niche and control of the niche size. Nature. 2003;425:836–841
  5. Wilson A, Trumpp A. Bone-marrow haematopoietic-stem-cell niches. Nat Rev Immunol. 2006;6:93–106
  6. Forsberg EC, Prohaska SS, Katzman S, et al. Differential expression of novel potential regulators in hematopoietic stem cells. PLoS Genet. 2005;1:e28
  7. Dexter TM, Allen TD, Lajtha LG. Conditions controlling the proliferation of haemopoietic stem cells in vitro. J Cell Physiol. 1977;91:335–344
  8. Kadereit S, Deeds LS, Haynesworth SE, et al. Expansion of LTC-ICs and maintenance of p21 and BCL-2 expression in cord blood CD34(+)/CD38(-) early progenitors cultured over human MSCs as a feeder layer. Stem Cells. 2002;20:573–582
  9. Yamaguchi M, Hirayama F, Murahashi H, et al. Ex vivo expansion of human UC blood primitive hematopoietic progenitors and transplantable stem cells using human primary BM stromal cells and human AB serum. Cytotherapy. 2002;4:109–118
  10. Horwitz EM, Le BK, Dominici M, et al. Clarification of the nomenclature for MSC: The International Society for Cellular Therapy position statement. Cytotherapy. 2005;7:393–395
  11. Wineman J, Moore K, Lemischka I, Muller-Sieburg C. Functional heterogeneity of the hematopoietic microenvironment: rare stromal elements maintain long-term repopulating stem cells. Blood. 1996;87:4082–4090
  12. Gan OI, Murdoch B, Larochelle A, Dick JE. Differential maintenance of primitive human SCID-repopulating cells, clonogenic progenitors, and long-term culture-initiating cells after incubation on human bone marrow stromal cells. Blood. 1997;90:641–650
  13. Jang YK, Jung DH, Jung MH, et al. Mesenchymal stem cells feeder layer from human umbilical cord blood for ex vivo expanded growth and proliferation of hematopoietic progenitor cells. Ann Hematol. 2006;85:212–225
  14. Robinson SN, Ng J, Niu T, et al. Superior ex vivo cord blood expansion following co-culture with bone marrow-derived mesenchymal stem cells. Bone Marrow Transplant. 2006;37:359–366
  15. Moore KA, Ema H, Lemischka IR. In vitro maintenance of highly purified, transplantable hematopoietic stem cells. Blood. 1997;89:4337–4347
  16. Thiemann FT, Moore KA, Smogorzewska EM, Lemischka IR, Crooks GM. The murine stromal cell line AFT024 acts specifically on human CD34+CD38- progenitors to maintain primitive function and immunophenotype in vitro. Exp Hematol. 1998;26:612–619
  17. Punzel M, Gupta P, Verfaillie CM. The microenvironment of AFT024 cells maintains primitive human hematopoiesis by counteracting contact mediated inhibition of proliferation. Cell Commun Adhes. 2002;9:149–159
  18. Huang S, Law P, Francis K, Palsson BO, Ho AD. Symmetry of initial cell divisions among primitive hematopoietic progenitors is independent of ontogenic age and regulatory molecules. Blood. 1999;94:2595–2604
  19. Wagner W, Saffrich R, Wirkner U, et al. Hematopoietic progenitor cells and cellular microenvironment: behavioral and molecular changes upon interaction. Stem Cells. 2005;23:1180–1191
  20. Sagvolden G, Giaever I, Pettersen EO, Feder J. Cell adhesion force microscopy. Proc Natl Acad Sci U S A. 1999;96:471–476
  21. Lotz MM, Burdsal CA, Erickson HP, McClay DR. Cell adhesion to fibronectin and tenascin: quantitative measurements of initial binding and subsequent strengthening response. J Cell Biol. 1989;109:1795–1805
  22. McClay DR, Wessel GM, Marchase RB. Intercellular recognition: quantitation of initial binding events. Proc Natl Acad Sci U S A. 1981;78:4975–4979
  23. Wagner W, Ansorge A, Wirkner U, et al. Molecular evidence for stem cell function of the slow-dividing fraction among human hematopoietic progenitor cells by genome-wide analysis. Blood. 2004;104:675–686
  24. Reyes M, Lund T, Lenvik T, et al. Purification and ex vivo expansion of postnatal human marrow mesodermal progenitor cells. Blood. 2001;98:2615–2625
  25. Wagner W, Wein F, Seckinger A, et al. Comparative characteristics of mesenchymal stem cells from human bone marrow, adipose tissue, and umbilical cord blood. Exp Hematol. 2005;33:1402–1416
  26. Wagner W, Feldmann RE, Seckinger A, et al. The heterogeneity of human mesenchymal stem cell preparations—evidence from simultaneous analysis of proteomes and transcriptomes. Exp Hematol. 2006;34:536–548
  27. Holloway W, Martinez AR, Oh DJ, et al. Key adhesion molecules are present on long podia extended by hematopoietic cells. Cytometry. 1999;37:171–177
  28. Oh DJ, Martinez AR, Lee GM, Francis K, Palsson BO. Intercellular adhesion can be visualized using fluorescently labeled fibrosarcoma HT1080 cells cocultured with hematopoietic cell lines or CD34(+) enriched human mobilized peripheral blood cells. Cytometry. 2000;40:119–125
  29. Frimberger AE, McAuliffe CI, Werme KA, et al. The fleet feet of haematopoietic stem cells: rapid motility, interaction and proteopodia. Br J Haematol. 2001;112:644–654
  30. Sutherland HJ, Eaves CJ, Eaves AC, Dragowska W, Lansdorp PM. Characterization and partial purification of human marrow cells capable of initiating long-term hematopoiesis in vitro. Blood. 1989;74:1563–1570
  31. Punzel M, Gupta P, Roodell M, Mortari F, Verfaillie CM. Factor(s) secreted by AFT024 fetal liver cells following stimulation with human cytokines are important for human LTC-IC growth. Leukemia. 1999;13:1079–1084
  32. Giebel B, Zhang T, Beckmann J, et al. Primitive human hematopoietic cells give rise to differentially specified daughter cells upon their initial cell division. Blood. 2006;107:2146–2152
  33. Brazma A, Hingamp P, Quackenbush J, et al. Minimum information about a microarray experiment (MIAME)-toward standards for microarray data. Nat Genet. 2001;29:365–371
  34. Rossmann H, Bachmann O, Vieillard-Baron D, Gregor M, Seidler U. Na+/. Gastroenterology. 1999;116:1389–1398
  35. Zeeberg BR, Feng W, Wang G, et al. GoMiner: a resource for biological interpretation of genomic and proteomic data. Genome Biol. 2003;4:R28
  36. Francis K, Ramakrishna R, Holloway W, Palsson BO. Two new pseudopod morphologies displayed by the human hematopoietic KG1a progenitor cell line and by primary human CD34(+) cells. Blood. 1998;92:3616–3623
  37. Hattori K, Heissig B, Tashiro K, et al. Plasma elevation of stromal cell-derived factor-1 induces mobilization of mature and immature hematopoietic progenitor and stem cells. Blood. 2001;97:3354–3360
  38. Punzel M, Zhang T, Liu D, Eckstein V, Ho AD. Functional analysis of initial cell divisions defines the subsequent fate of individual human CD34(+)CD38(−) cells. Exp Hematol. 2002;30:464–472
  39. Koller MR, Manchel I, Smith AK. Quantitative long-term culture-initiating cell assays require accessory cell depletion that can be achieved by CD34-enrichment or 5-fluorouracil exposure. Blood. 1998;91:4056–4064
  40. Borovecki F, Lovrecic L, Zhou J, et al. Genome-wide expression profiling of human blood reveals biomarkers for Huntington's disease. Proc Natl Acad Sci U S A. 2005;102:11023–11028
  41. Choong ML, Luo B, Lodish HF. Microenvironment-driven changes in the expression profile of hematopoietic cobblestone area-forming cells. Ann Hematol. 2004;83:160–169
  42. Hackney JA, Charbord P, Brunk BP, et al. A molecular profile of a hematopoietic stem cell niche. Proc Natl Acad Sci U S A. 2002;99:13061–13066
  43. Charbord P, Moore K. Gene expression in stem cell-supporting stromal cell lines. Ann N Y Acad Sci. 2005;1044:159–167
  44. Teixido J, Hemler ME, Greenberger JS, Anklesaria P. Role of beta 1 and beta 2 integrins in the adhesion of human CD34hi stem cells to bone marrow stroma. J Clin Invest. 1992;90:358–367
  45. 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
  46. Cancelas JA, Koevoet WL, de Koning AE, et al. Connexin-43 gap junctions are involved in multiconnexin-expressing stromal support of hemopoietic progenitors and stem cells. Blood. 2000;96:498–505
  47. Durig J, Rosenthal C, Halfmeyer K, et al. Intercellular communication between bone marrow stromal cells and CD34+ haematopoietic progenitor cells is mediated by connexin 43-type gap junctions. Br J Haematol. 2000;111:416–425
  48. Straub BK, Eckstein V, Grund C, et al. Expression of complex junction proteins in hematopoietic progenitor cells. Blood. (ASH Annual Meeting Abstracts); 2004:1282.
  49. Wuchter P, Boda-Heggemann J, Straub B, et al. Molecular characterization of unique junctional complexes as communication pathways among mesenchymal stem cells. Blood. (ASH Annual Meeting Abstracts);2005:1399.
  50. Sovalat H, Racadot E, Ojeda M, et al. CD34+ cells and CD34+CD38—subset from mobilized blood show different patterns of adhesion molecules compared to those from steady-state blood, bone marrow, and cord blood. J Hematother Stem Cell Res. 2003;12:473–489
  51. Gigant C, Latger-Cannard V, Bensoussan D, et al. Quantitative expression of adhesion molecules on granulocyte colony-stimulating factor-mobilized peripheral blood, bone marrow, and cord blood CD34+ cells. J Hematother Stem Cell Res. 2001;10:807–814

PII: S0301-472X(06)00656-4

doi: 10.1016/j.exphem.2006.10.003

Experimental Hematology
Volume 35, Issue 2 , Pages 314-325 , February 2007