Experimental Hematology
Volume 38, Issue 7 , Pages 540-547 , July 2010

Hematopoietic stem cell origin of connective tissues

  • Makio Ogawa

      Affiliations

    • Department of Pathology and Laboratory Medicine, Medical University of South Carolina, Charleston, SC., USA
    • Research Service, Department of Veterans Affairs Medical Center, Charleston, SC., USA
    • Corresponding Author InformationOffprint requests to: Makio Ogawa, M.D., Ph.D., Department of Veterans Affairs Medical Center, 109 Bee Street, Charleston, SC 29401-5799
  • ,
  • Amanda C. LaRue

      Affiliations

    • Department of Pathology and Laboratory Medicine, Medical University of South Carolina, Charleston, SC., USA
    • Research Service, Department of Veterans Affairs Medical Center, Charleston, SC., USA
  • ,
  • Patricia M. Watson

      Affiliations

    • Department of Medicine, Medical University of South Carolina, Charleston, SC., USA
  • ,
  • Dennis K. Watson

      Affiliations

    • Department of Pathology and Laboratory Medicine, Medical University of South Carolina, Charleston, SC., USA
    • Department of Biochemistry and Molecular Biology, Medical University of South Carolina, Charleston, SC., USA

Received 6 April 2010 ,Revised 6 April 2010 ,Accepted 8 April 2010.

References 

  1. Ashton BA, Allen TD, Howlett CR, Eaglesom CC, Hattori A, Owen M. Formation of bone and cartilage by marrow stromal cells in diffusion chambers in vivo. Clin Orthop Relat Res. 1980;294–307
  2. Prockop DJ. Marrow stromal cells as stem cells for nonhematopoietic tissues. Science. 1997;276:71–74
  3. Pittenger MF, Mackay AM, Beck SC, et al. Multilineage potential of adult human mesenchymal stem cells. Science. 1999;284:143–147
  4. Bianco P, Robey PG, Simmons PJ. Mesenchymal stem cells: revisiting history, concepts, and assays. Cell Stem Cell. 2008;2:313–319
  5. Studeny M, Marini FC, Champlin RE, Zompetta C, Fidler IJ, Andreeff M. Bone marrow-derived mesenchymal stem cells as vehicles for interferon-beta delivery into tumors. Cancer Res. 2002;62:3603–3608
  6. Verfaillie CM, Schwartz R, Reyes M, Jiang Y. Unexpected potential of adult stem cells. Ann N Y Acad Sci. 2003;996:231–234
  7. Gregory CA, Prockop DJ, Spees JL. Non-hematopoietic bone marrow stem cells: molecular control of expansion and differentiation. Exp Cell Res. 2005;306:330–335
  8. Caplan AI. Mesenchymal stem cells. J Orthop Res. 1991;9:641–650
  9. Friedenstein AJ, Chailakhjan RK, Lalykina KS. The development of fibroblast colonies in monolayer cultures of guinea-pig bone marrow and spleen cells. Cell Tissue Kinet. 1970;3:393–403
  10. Friedenstein AJ, Chailakhyan RK, Gerasimov UV. Bone marrow osteogenic stem cells: in vitro cultivation and transplantation in diffusion chambers. Cell Tissue Kinet. 1987;20:263–272
  11. Friedenstein AJ, Gorskaja JF, Kulagina NN. Fibroblast precursors in normal and irradiated mouse hematopoietic organs. Exp Hematol. 1976;4:267–274
  12. Caplan AI, Bruder SP. Mesenchymal stem cells: building blocks for molecular medicine in the 21st century. Trends Mol Med. 2001;7:259–264
  13. Dazzi F, Horwood NJ. Potential of mesenchymal stem cell therapy. Curr Opin Oncol. 2007;19:650–655
  14. Prockop DJ, Olson SD. Clinical trials with adult stem/progenitor cells for tissue repair: let's not overlook some essential precautions. Blood. 2007;109:3147–3151
  15. Okabe M, Ikawa M, Kominami K, Nakanishi T, Nishimune Y. ‘Green mice’ as a source of ubiquitous green cells. FEBS Lett. 1997;407:313–319
  16. Osawa M, Hanada K, Hamada H, Nakauchi H. Long-term lymphohematopoietic reconstitution by a single CD34-low/negative hematopoietic stem cell. Science. 1996;273:242–245
  17. Masuya M, Drake CJ, Fleming PA, et al. Hematopoietic origin of glomerular mesangial cells. Blood. 2003;101:2215–2218
  18. Hess DC, Abe T, Hill WD, et al. Hematopoietic origin of microglial and perivascular cells in brain. Exp Neurol. 2004;186:134–144
  19. Abe T, Masuya M, Ogawa M. An efficient method for single hematopoietic stem cell engraftment in mice based on cell-cycle dormancy of hematopoietic stem cells. Exp Hematol. 2010;38:603–608
  20. Matsuzaki Y, Kinjo K, Mulligan RC, Okano H. Unexpectedly efficient homing capacity of purified murine hematopoietic stem cells. Immunity. 2004;20:87–93
  21. Musashi M, Yang YC, Paul SR, Clark SC, Sudo T, Ogawa M. Direct and synergistic effects of interleukin 11 on murine hemopoiesis in culture. Proc Natl Acad Sci U S A. 1991;88:765–769
  22. Ikebuchi K, Clark SC, Ihle JN, Souza LM, Ogawa M. Granulocyte colony-stimulating factor enhances interleukin 3-dependent proliferation of multipotential hemopoietic progenitors. Proc Natl Acad Sci U S A. 1988;85:3445–3449
  23. Ogawa M, LaRue AC, Drake CJ. Hematopoietic origin of fibroblasts/myofibroblasts: its pathophysiologic implications. Blood. 2006;108:2893–2896
  24. Eckes B, Zigrino P, Kessler D, et al. Fibroblast-matrix interactions in wound healing and fibrosis. Matrix Biol. 2000;19:325–332
  25. Gabbiani G. The myofibroblast in wound healing and fibrocontractive diseases. J Pathol. 2003;200:500–503
  26. Powell DW, Mifflin RC, Valentich JD, Crowe SE, Saada JI, West AB. Myofibroblasts. I. Paracrine cells important in health and disease. Am J Physiol Cell Physiol. 1999;277:C1–C19
  27. Tomasek JJ, Gabbiani G, Hinz B, Chaponnier C, Brown RA. Myofibroblasts and mechano-regulation of connective tissue remodelling. Nat Rev Mol Cell Biol. 2002;3:349–363
  28. LaRue AC, Masuya M, Ebihara Y, et al. Hematopoietic origins of fibroblasts: I. In vivo studies of fibroblasts associated with solid tumors. Exp Hematol. 2006;34:208–218
  29. Ziegelhoeffer T, Fernandez B, Kostin S, et al. Bone marrow-derived cells do not incorporate into the adult growing vasculature. Circ Res. 2004;94:230–238
  30. Rajantie I, Ilmonen M, Alminaite A, Ozerdem U, Alitalo K, Salven P. Adult bone marrow-derived cells recruited during angiogenesis comprise precursors for periendothelial vascular mural cells. Blood. 2004;104:2084–2086
  31. Lang H, Ebihara Y, Schmiedt RA, et al. Contribution of bone marrow hematopoietic stem cells to adult mouse inner ear: mesenchymal cells and fibrocytes. J Comp Neurol. 2006;496:187–201
  32. Visconti RP, Ebihara Y, LaRue AC, et al. An in vivo analysis of hematopoietic stem cell potential: hematopoietic origin of cardiac valve interstitial cells. Circ Res. 2006;98:690–696
  33. Fujita J, Mori M, Kawada H, et al. Administration of granulocyte colony-stimulating factor after myocardial infarction enhances the recruitment of hematopoietic stem cell-derived myofibroblasts and contributes to cardiac repair. Stem Cells. 2007;25:2750–2759
  34. Miyata E, Masuya M, Yoshida S, et al. Hematopoietic origin of hepatic stellate cells in the adult liver. Blood. 2008;111:2427–2435
  35. Ebihara Y, Masuya M, Larue AC, et al. Hematopoietic origins of fibroblasts: II. In vitro studies of fibroblasts, CFU-F, and fibrocytes. Exp Hematol. 2006;34:219–229
  36. Abe R, Donnelly SC, Peng T, Bucala R, Metz CN. Peripheral blood fibrocytes: differentiation pathway and migration to wound sites. J Immunol. 2001;166:7556–7562
  37. Luria EA, Panasyuk AF, Friedenstein AY. Fibroblast colony formation from monolayer cultures of blood cells. Transfusion. 1971;11:345–349
  38. Penn PE, Jiang DZ, Fei RG, Sitnicka E, Wolf NS. Dissecting the hematopoietic microenvironment. IX. Further characterization of murine bone marrow stromal cells. Blood. 1993;81:1205–1213
  39. Ntambi JM, Young-Cheul K. Adipocyte differentiation and gene expression. J Nutr. 2000;130:3122S–3126S
  40. Gregoire FM. Adipocyte differentiation: from fibroblast to endocrine cell. Exp Biol Med (Maywood). 2001;226:997–1002
  41. Tholpady SS, Aojanepong C, Llull R, et al. The cellular plasticity of human adipocytes. Ann Plast Surg. 2005;54:651–656
  42. Sera Y, LaRue AC, Moussa O, et al. Hematopoietic stem cell origin of adipocytes. Exp Hematol. 2009;37:1108–1120
  43. Crossno JT, Majka SM, Grazia T, Gill RG, Klemm DJ. Rosiglitazone promotes development of a novel adipocyte population from bone marrow-derived circulating progenitor cells. J Clin Invest. 2006;116:3220–3228
  44. Koh YJ, Kang S, Lee HJ, et al. Bone marrow-derived circulating progenitor cells fail to transdifferentiate into adipocytes in adult adipose tissues in mice. J Clin Invest. 2007;117:3684–3695
  45. Nuttall ME, Gimble JM. Controlling the balance between osteoblastogenesis and adipogenesis and the consequent therapeutic implications. Curr Opin Pharmacol. 2004;4:290–294
  46. Gimble JM, Zvonic S, Floyd ZE, Kassem M, Nuttall ME. Playing with bone and fat. J Cell Biochem. 2006;98:251–266
  47. Meunier P, Aaron J, Edouard C, Vignon G. Osteoporosis and the replacement of cell populations of the marrow by adipose tissue. A quantitative study of 84 iliac bone biopsies. Clin Orthop Relat Res. 1971;80:147–154
  48. Bennett JH, Joyner CJ, Triffitt JT, Owen ME. Adipocytic cells cultured from marrow have osteogenic potential. J Cell Sci. 1991;99(Pt 1):131–139
  49. Beresford JN, Bennett JH, Devlin C, Leboy PS, Owen ME. Evidence for an inverse relationship between the differentiation of adipocytic and osteogenic cells in rat marrow stromal cell cultures. J Cell Sci. 1992;102(Pt 2):341–351
  50. Levine JA, Jensen MD, Eberhardt NL, O'Brien T. Adipocyte macrophage colony-stimulating factor is a mediator of adipose tissue growth. J Clin Invest. 1998;101:1557–1564
  51. Wiktor-Jedrzejczak W, Bartocci A, Ferrante AW, et al. Total absence of colony-stimulating factor 1 in the macrophage-deficient osteopetrotic (op/op) mouse. Proc Natl Acad Sci U S A. 1990;87:4828–4832
  52. Dai XM, Ryan GR, Hapel AJ, et al. Targeted disruption of the mouse colony-stimulating factor 1 receptor gene results in osteopetrosis, mononuclear phagocyte deficiency, increased primitive progenitor cell frequencies, and reproductive defects. Blood. 2002;99:111–120
  53. Wei S, Lightwood D, Ladyman H, et al. Modulation of CSF-1-regulated post-natal development with anti-CSF-1 antibody. Immunobiology. 2005;210:109–119
  54. Olmsted-Davis EA, Gugala Z, Camargo F, et al. Primitive adult hematopoietic stem cells can function as osteoblast precursors. Proc Natl Acad Sci U S A. 2003;100:15877–15882
  55. Dominici M, Pritchard C, Garlits JE, Hofmann TJ, Persons DA, Horwitz EM. Hematopoietic cells and osteoblasts are derived from a common marrow progenitor after bone marrow transplantation. Proc Natl Acad Sci U S A. 2004;101:11761–11766
  56. Mehrotra M, Rosol M, Ogawa M, LaRue AC. Amelioration of a mouse model of osteogenesis imperfecta with hematopoietic stem cell transplantation: Microcomputed tomography studies. Exp Hematol. 2010;38:593–602
  57. Gao J, Dennis JE, Muzic RF, Lundberg M, Caplan AI. The dynamic in vivo distribution of bone marrow-derived mesenchymal stem cells after infusion. Cells Tissues Organs. 2001;169:12–20
  58. Javazon EH, Beggs KJ, Flake AW. Mesenchymal stem cells: paradoxes of passaging. Exp Hematol. 2004;32:414–425
  59. Horwitz EM, Le Blanc K, Dominici M, et al. Clarification of the nomenclature for MSC: The International Society for Cellular Therapy position statement. Cytotherapy. 2005;7:393–395
  60. Sudo K, Kanno M, Miharada K, et al. Mesenchymal progenitors able to differentiate into osteogenic, chondrogenic, and/or adipogenic cells in vitro are present in most primary fibroblast-like cell populations. Stem Cells. 2007;25:1610–1617
  61. Haniffa MA, Wang XN, Holtick U, et al. Adult human fibroblasts are potent immunoregulatory cells and functionally equivalent to mesenchymal stem cells. J Immunol. 2007;179:1595–1604
  62. Jones EA, Kinsey SE, English A, et al. Isolation and characterization of bone marrow multipotential mesenchymal progenitor cells. Arthritis Rheum. 2002;46:3349–3360
  63. Kuwana M, Okazaki Y, Kodama H, et al. Human circulating CD14+ monocytes as a source of progenitors that exhibit mesenchymal cell differentiation. J Leukoc Biol. 2003;74:833–845
  64. Abe T, Fleming PA, Masuya M, et al. Granulocyte/macrophage origin of glomerular mesangial cells. Int J Hematol. 2005;82:115–118
  65. Bucala R, Spiegel LA, Chesney J, Hogan M, Cerami A. Circulating fibrocytes define a new leukocyte subpopulation that mediates tissue repair. Mol Med. 1994;1:71–81
  66. Schmidt M, Sun G, Stacey MA, Mori L, Mattoli S. Identification of circulating fibrocytes as precursors of bronchial myofibroblasts in asthma. J Immunol. 2003;171:380–389
  67. Pabst R, Sterzel RB. Cell renewal of glomerular cell types in normal rats. An autoradiographic analysis. Kidney Int. 1983;24:626–631
  68. Spalding KL, Arner E, Westermark PO, et al. Dynamics of fat cell turnover in humans. Nature. 2008;453:783–787
  69. Manolagas SC. Birth and death of bone cells: basic regulatory mechanisms and implications for the pathogenesis and treatment of osteoporosis. Endocr Rev. 2000;21:115–137
  70. Shirai K, Sera Y, Bulkeley W, et al. Hematopoietic stem cell origin of human fibroblasts: cell culture studies of female recipients of gender-mismatched stem cell transplantation and patients with chronic myelogenous leukemia. Exp Hematol. 2009;37:1464–1471
  71. Saito N, Ishikawa F, Shimoda K, et al. Xenotransplantation of primary CD34+CD38- hematopoietic stem cells results in an in vivo model of idiopathic myelofibrosis. Blood (ASH Annual Meeting Abstracts). 2006;108:Abstract 666
  72. Goan SR, Junghahn I, Wissler M, et al. Donor stromal cells from human blood engraft in NOD/SCID mice. Blood. 2000;96:3971–3978
  73. Horwitz EM, Prockop DJ, Fitzpatrick LA, et al. Transplantability and therapeutic effects of bone marrow-derived mesenchymal cells in children with osteogenesis imperfecta. Nat Med. 1999;5:309–313
  74. Horwitz EM, Prockop DJ, Gordon PL, et al. Clinical responses to bone marrow transplantation in children with severe osteogenesis imperfecta. Blood. 2001;97:1227–1231
  75. Horwitz EM, Gordon PL, Koo WK, et al. Isolated allogeneic bone marrow-derived mesenchymal cells engraft and stimulate growth in children with osteogenesis imperfecta: Implications for cell therapy of bone. Proc Natl Acad Sci U S A. 2002;99:8932–8937
  76. Tolar J, Ishida-Yamamoto A, Riddle M, et al. Amelioration of epidermolysis bullosa by transfer of wild-type bone marrow cells. Blood. 2009;113:1167–1174
  77. Klebanov S, Astle CM, DeSimone O, Ablamunits V, Harrison DE. Adipose tissue transplantation protects ob/ob mice from obesity, normalizes insulin sensitivity and restores fertility. J Endocrinol. 2005;186:203–211
  78. Sugimoto H, Mundel TM, Sund M, Xie L, Cosgrove D, Kalluri R. Bone-marrow-derived stem cells repair basement membrane collagen defects and reverse genetic kidney disease. Proc Natl Acad Sci U S A. 2006;103:7321–7326
  79. Prodromidi EI, Poulsom R, Jeffery R, et al. Bone marrow-derived cells contribute to podocyte regeneration and amelioration of renal disease in a mouse model of Alport syndrome. Stem Cells. 2006;24:2448–2455

PII: S0301-472X(10)00148-7

doi: 10.1016/j.exphem.2010.04.005

Experimental Hematology
Volume 38, Issue 7 , Pages 540-547 , July 2010