Experimental Hematology
Volume 36, Issue 9 , Pages 1157-1166 , September 2008

Parathyroid hormone effectively induces mobilization of progenitor cells without depletion of bone marrow

  • Stefan Brunner

      Affiliations

    • Ludwig-Maximilians University, Klinikum Grosshadern, Medical Department I, Munich, Germany
    • ,
  • Marc-Michael Zaruba

      Affiliations

    • Ludwig-Maximilians University, Klinikum Grosshadern, Medical Department I, Munich, Germany
    • ,
  • Bruno Huber

      Affiliations

    • Ludwig-Maximilians University, Klinikum Grosshadern, Medical Department I, Munich, Germany
    • ,
  • Robert David

      Affiliations

    • Ludwig-Maximilians University, Klinikum Grosshadern, Medical Department I, Munich, Germany
    • ,
  • Marcus Vallaster

      Affiliations

    • Ludwig-Maximilians University, Klinikum Grosshadern, Medical Department I, Munich, Germany
    • ,
  • Gerald Assmann

      Affiliations

    • Ludwig-Maximilians University, Institute of Pathology, Munich, Germany
    • ,
  • Josef Mueller-Hoecker

      Affiliations

    • Ludwig-Maximilians University, Institute of Pathology, Munich, Germany
    • ,
  • Wolfgang-Michael Franz

      Affiliations

    • Ludwig-Maximilians University, Klinikum Grosshadern, Medical Department I, Munich, Germany
    • Corresponding Author InformationOffprint requests to: Wolfgang-Michael Franz, M.D., Medizinische Klinik und Poliklinik I, Klinikum Großhadern, Marchioninistr. 15, 81377 Munich, Germany

Received 27 April 2007 ,Revised 18 March 2008 ,Accepted 19 March 2008.

References 

  1. Brown EM. Four-parameter model of the sigmoidal relationship between parathyroid hormone release and extracellular calcium concentration in normal and abnormal parathyroid tissue. J Clin Endocrinol Metab. 1983;56:572–581
  2. Brown EM. Mechanisms underlying the regulation of parathyroid hormone secretion in vivo and in vitro. Curr Opin Nephrol Hypertens. 1993;2:541–551
  3. Diaz R, El-Hajj Fuleihan G, Brown EM. Regulation of parathyroid function. In:  Fray GGS editors. Handbook of Physiology, Section 7: Endocrinology. New York: Oxford University Press; 1999;p. 183–213
  4. Madore GR, Sherman PJ, Lane JM. Parathyroid hormone. J Am Acad Orthop Surg. 2004;12:67–71
  5. Potts JT, Juppner H. Parathyroid hormone: molecular biology and regulation. In:  Bilezikian JP,  Raisz LG,  Rodan GA editor. Principles of Bone Biology. New York: Academic Press; 1996;325
  6. Qian J, Colbert MC, Witte D, et al. Midgestational lethality in mice lacking the parathyroid hormone (PTH)/PTH-related peptide receptor is associated with abrupt cardiomyocyte death. Endocrinology. 2003;144:1053–1061
  7. Tian J, Smogorzewski M, Kedes L, Massry SG. Parathyroid hormone-parathyroid hormone related protein receptor messenger RNA is present in many tissues besides the kidney. Am J Nephrol. 1993;13:210–213
  8. Calvi LM, Adams GB, Weibrecht KW, et al. Osteoblastic cells regulate the haematopoietic stem cell niche. Nature. 2003;425:841–846
  9. Weber JM, Forsythe SR, Christianson CA, et al. Parathyroid hormone stimulates expression of the Notch ligand Jagged1 in osteoblastic cells. Bone. 2006;39:485–493
  10. Marie PJ. Role of N-cadherin in bone formation. J Cell Physiol. 2002;190:297–305
  11. Reya T. Regulation of hematopoietic stem cell self-renewal. Recent Prog Horm Res. 2003;58:283–295
  12. Reya T, Duncan AW, Ailles L, et al. A role for Wnt signalling in self-renewal of haematopoietic stem cells. Nature. 2003;423:409–414
  13. Tobimatsu T, Kaji H, Sowa H, et al. Parathyroid hormone increases beta-catenin levels through Smad3 in mouse osteoblastic cells. Endocrinology. 2006;147:2583–2590
  14. Zhu J, Emerson SG. A new bone to pick: osteoblasts and the haematopoietic stem-cell niche. Bioessays. 2004;26:595–596
  15. Yamane T, Kunisada T, Tsukamoto H, et al. Wnt signaling regulates hemopoiesis through stromal cells. J Immunol. 2001;167:765–772
  16. Murdoch B, Chadwick K, Martin M, et al. Wnt-5A augments repopulating capacity and primitive hematopoietic development of human blood stem cells in vivo. Proc Natl Acad Sci U S A. 2003;100:3422–3427
  17. Willert K, Brown JD, Danenberg E, et al. Wnt proteins are lipid-modified and can act as stem cell growth factors. Nature. 2003;423:448–452
  18. Varnum-Finney B, Purton LE, Yu M, et al. The Notch ligand, Jagged-1, influences the development of primitive hematopoietic precursor cells. Blood. 1998;91:4084–4091
  19. Varnum-Finney B, Brashem-Stein C, Bernstein ID. Combined effects of Notch signaling and cytokines induce a multiple log increase in precursors with lymphoid and myeloid reconstituting ability. Blood. 2003;101:1784–1789
  20. Karanu FN, Murdoch B, Gallacher L, et al. The notch ligand jagged-1 represents a novel growth factor of human hematopoietic stem cells. J Exp Med. 2000;192:1365–1372
  21. Burns CE, Traver D, Mayhall E, Shepard JL, Zon LI. Hematopoietic stem cell fate is established by the Notch-Runx pathway. Genes Dev. 2005;19:2331–2342
  22. Adams GB, Martin RP, Alley IR, et al. Therapeutic targeting of a stem cell niche. Nat Biotechnol. 2007;25:238–243
  23. Lindemann A, Herrmann F, Oster W, et al. Hematologic effects of recombinant human granulocyte colony-stimulating factor in patients with malignancy. Blood. 1989;74:2644–2651
  24. Jansen J, Hanks S, Thompson JM, Dugan MJ, Akard LP. Transplantation of hematopoietic stem cells from the peripheral blood. J Cell Mol Med. 2005;9:37–50
  25. Asahara T, Murohara T, Sullivan A, et al. Isolation of putative progenitor endothelial cells for angiogenesis. Science. 1997;275:964–967
  26. Beltrami AP, Barlucchi L, Torella D, et al. Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell. 2003;114:763–776
  27. Oh H, Bradfute SB, Gallardo TD, et al. Cardiac progenitor cells from adult myocardium: homing, differentiation, and fusion after infarction. Proc Natl Acad Sci U S A. 2003;100:12313–12318
  28. Orlic D, Kajstura J, Chimenti S, et al. Mobilized bone marrow cells repair the infarcted heart, improving function and survival. Proc Natl Acad Sci U S A. 2001;98:10344–10349
  29. Shi Q, Rafii S, Wu MH, et al. Evidence for circulating bone marrow-derived endothelial cells. Blood. 1998;92:362–367
  30. Abbott JD, Huang Y, Liu D, Hickey R, Krause DS, Giordano FJ. Stromal cell-derived factor-1alpha plays a critical role in stem cell recruitment to the heart after myocardial infarction but is not sufficient to induce homing in the absence of injury. Circulation. 2004;110:3300–3305
  31. Ito T, Tajima F, Ogawa M. Developmental changes of CD34 expression by murine hematopoietic stem cells. Exp Hematol. 2000;28:1269–1273
  32. Ogawa M. Changing phenotypes of hematopoietic stem cells. Exp Hematol. 2002;30:3–6
  33. Werner N, Priller J, Laufs U, et al. Bone marrow-derived progenitor cells modulate vascular reendothelialization and neointimal formation: effect of 3-hydroxy-3-methylglutaryl coenzyme a reductase inhibition. Arterioscler Thromb Vasc Biol. 2002;22:1567–1572
  34. Asahara T, Takahashi T, Masuda H, et al. VEGF contributes to postnatal neovascularization by mobilizing bone marrow-derived endothelial progenitor cells. EMBO J. 1999;18:3964–3972
  35. 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
  36. Jung Y, Wang J, Schneider A, et al. Regulation of SDF-1 (CXCL12) production by osteoblasts; a possible mechanism for stem cell homing. Bone. 2006;38:497–508
  37. McClelland P, Onyia JE, Miles RR, et al. Intermittent administration of parathyroid hormone (1-34) stimulates matrix metalloproteinase-9 (MMP-9) expression in rat long bone. J Cell Biochem. 1998;70:391–401
  38. Taichman RS, Emerson SG. Human osteoblasts support hematopoiesis through the production of granulocyte colony-stimulating factor. J Exp Med. 1994;179:1677–1682
  39. Taichman RS, Reilly MJ, Emerson SG. Human osteoblasts support human hematopoietic progenitor cells in vitro bone marrow cultures. Blood. 1996;87:518–524
  40. Taichman R, Reilly M, Verma R, Ehrenman K, Emerson S. Hepatocyte growth factor is secreted by osteoblasts and cooperatively permits the survival of haematopoietic progenitors. Br J Haematol. 2001;112:438–448
  41. Duarte RF, Frank DA. SCF and G-CSF lead to the synergistic induction of proliferation and gene expression through complementary signaling pathways. Blood. 2000;96:3422–3430
  42. Duarte RF, Franf DA. The synergy between stem cell factor (SCF) and granulocyte colony-stimulating factor (G-CSF): molecular basis and clinical relevance. Leuk Lymphoma. 2002;43:1179–1187
  43. Hematti P, Tuchman S, Larochelle A, Metzger ME, Donahue RE, Tisdale JF. Comparison of retroviral transduction efficiency in CD34+ cells derived from bone marrow versus G-CSF-mobilized or G-CSF plus stem cell factor-mobilized peripheral blood in nonhuman primates. Stem Cells. 2004;22:1062–1069
  44. Hess DA, Levac KD, Karanu FN, et al. Functional analysis of human hematopoietic repopulating cells mobilized with granulocyte colony-stimulating factor alone versus granulocyte colony-stimulating factor in combination with stem cell factor. Blood. 2002;100:869–878
  45. van Os R, Robinson S, Sheridan T, Mislow JM, Dawes D, Mauch PM. Granulocyte colony-stimulating factor enhances bone marrow stem cell damage caused by repeated administration of cytotoxic agents. Blood. 1998;92:1950–1956
  46. van Os R, Robinson S, Sheridan T, Mauch PM. Granulocyte-colony stimulating factor impedes recovery from damage caused by cytotoxic agents through increased differentiation at the expense of self-renewal. Stem Cells. 2000;18:120–127
  47. Freedman A, Neuberg D, Mauch P, et al. Cyclophosphamide, doxorubicin, vincristine, prednisone dose intensification with granulocyte colony-stimulating factor markedly depletes stem cell reserve for autologous bone marrow transplantation. Blood. 1997;90:4996–5001
  48. Gazitt Y, Freytes CO, Callander N, et al. Successful PBSC mobilization with high-dose G-CSF for patients failing a first round of mobilization. J Hematother. 1999;8:173–183
  49. Deindl E, Zaruba MM, Brunner S, et al. G-CSF administration after myocardial infarction in mice attenuates late ischemic cardiomyopathy by enhanced arteriogenesis. FASEB J. 2006;20:956–958
  50. Engelmann MG, Theiss HD, Hennig-Theiss C, et al. Autologous bone marrow stem cell mobilization induced by granulocyte colony-stimulating factor after subacute ST-segment elevation myocardial infarction undergoing late revascularization: final results from the G-CSF-STEMI (Granulocyte Colony-Stimulating Factor ST-Segment Elevation Myocardial Infarction) trial. J Am Coll Cardiol. 2006;48:1712–1721
  51. Engelmann MG, Franz WM. Stem cell therapy after myocardial infarction: ready for clinical application?. Curr Opin Mol Ther. 2006;8:396–414

PII: S0301-472X(08)00128-8

doi: 10.1016/j.exphem.2008.03.014

Experimental Hematology
Volume 36, Issue 9 , Pages 1157-1166 , September 2008

Article Tools

* Image Usage & Resolution