Experimental Hematology
Volume 37, Issue 12 , Pages 1445-1453 , December 2009

Mesenchymal stem cell–educated macrophages: A novel type of alternatively activated macrophages

  • Jaehyup Kim

      Affiliations

    • Department of Medicine, University of Wisconsin-Madison, School of Medicine and Public Health, Madison, Wis., USA
    • ,
  • Peiman Hematti

      Affiliations

    • Department of Medicine, University of Wisconsin-Madison, School of Medicine and Public Health, Madison, Wis., USA
    • University of Wisconsin Carbone Cancer Center, Madison, Wis., USA
    • Corresponding Author InformationOffprint requests to: Peiman Hematti, M.D., Hematology Office, Department of Medicine, University of Wisconsin-Madison, School of Medicine and Public Health, 4033-WIMR, 1111 Highland Avenue, Madison, WI 53705-2275

Received 5 June 2009 ,Revised 25 August 2009 ,Accepted 16 September 2009.

References 

  1. Friedenstein AJ, Petrakova KV, Kurolesova AI, Frolova GP. Heterotopic of bone marrow. Analysis of precursor cells for osteogenic and hematopoietic tissues. Transplantation. 1968;6:230–247
  2. Caplan AI. Mesenchymal stem cells. J Orthop Res. 1991;9:641–650
  3. Pittenger MF, Mackay AM, Beck SC, et al. Multilineage potential of adult human mesenchymal stem cells. Science. 1999;284:143–147
  4. 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
  5. Crisan M, Yap S, Casteilla L, et al. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell. 2008;3:301–313
  6. Covas DT, Panepucci RA, Fontes AM, et al. Multipotent mesenchymal stromal cells obtained from diverse human tissues share functional properties and gene-expression profile with CD146+ perivascular cells and fibroblasts. Exp Hematol. 2008;36:642–654
  7. da Silva Meirelles L, Chagastelles PC, Nardi NB. Mesenchymal stem cells reside in virtually all post-natal organs and tissues. J Cell Sci. 2006;119:2204–2213
  8. Lennon DP, Caplan AI. Isolation of rat marrow-derived mesenchymal stem cells. Exp Hematol. 2006;34:1606–1607
  9. Bartholomew A, Sturgeon C, Siatskas M, et al. Mesenchymal stem cells suppress lymphocyte proliferation in vitro and prolong skin graft survival in vivo. Exp Hematol. 2002;30:42–48
  10. Tse WT, Pendleton JD, Beyer WM, Egalka MC, Guinan EC. Suppression of allogeneic T-cell proliferation by human marrow stromal cells: implications in transplantation. Transplantation. 2003;75:389–397
  11. Le Blanc K, Tammik C, Rosendahl K, Zetterberg E, Ringden O. HLA expression and immunologic properties of differentiated and undifferentiated mesenchymal stem cells. Exp Hematol. 2003;31:890–896
  12. Rasmusson I, Ringden O, Sundberg B, Le Blanc K. Mesenchymal stem cells inhibit the formation of cytotoxic T lymphocytes, but not activated cytotoxic T lymphocytes or natural killer cells. Transplantation. 2003;76:1208–1213
  13. Di Ianni M, Del Papa B, De Ioanni M, et al. Mesenchymal cells recruit and regulate T regulatory cells. Exp Hematol. 2008;36:309–318
  14. Horwitz E, Dominici M. How do mesenchymal stromal cells exert their therapeutic benefit?. Cytotherapy. 2008;10:771–774
  15. Caplan AI. Why are MSCs therapeutic? New data: new insight. J Pathol. 2009;217:318–324
  16. Le Blanc K, Pittenger M. Mesenchymal stem cells: progress toward promise. Cytotherapy. 2005;7:36–45
  17. Jones BJ, McTaggart SJ. Immunosuppression by mesenchymal stromal cells: from culture to clinic. Exp Hematol. 2008;36:733–741
  18. Javazon EH, Beggs KJ, Flake AW. Mesenchymal stem cells: paradoxes of passaging. Exp Hematol. 2004;32:414–425
  19. Giordano A, Galderisi U, Marino IR. From the laboratory bench to the patient's bedside: an update on clinical trials with mesenchymal stem cells. J Cell Physiol. 2007;211:27–35
  20. Nauta AJ, Fibbe WE. Immunomodulatory properties of mesenchymal stromal cells. Blood. 2007;110:3499–3506
  21. Sundin M, Remberger M, Lonnies H, Sundberg B, Ringden O, Le Blanc K. No increased trapping of multipotent mesenchymal stromal cells in bone marrow filters compared with other bone marrow cells. Cytotherapy. 2008;10:238–242
  22. Trivedi P, Hematti P. Derivation and immunological characterization of mesenchymal stromal cells from human embryonic stem cells. Exp Hematol. 2008;36:350–359
  23. Mellor-Pita S, Citores MJ, Castejon R, et al. Monocytes and T lymphocytes contribute to a predominance of interleukin 6 and interleukin 10 in systemic lupus erythematosus. Cytometry. 2009;76B:261–270
  24. Stephens SA, Brownlie J, Charleston B, Howard CJ. Differences in cytokine synthesis by the sub-populations of dendritic cells from afferent lymph. Immunology. 2003;110:48–57
  25. Kryczek I, Banerjee M, Cheng P, et al. Phenotype, distribution, generation, and functional and clinical relevance of Th17 cells in the human tumor environments. Blood. 2009;114:1141–1149
  26. Sachdeva N, Asthana D. Cytokine quantitation: technologies and applications. Front Biosci. 2007;12:4682–4695
  27. Porcheray F, Viaud S, Rimaniol AC, et al. Macrophage activation switching: an asset for the resolution of inflammation. Clin Exp Immunol. 2005;142:481–489
  28. Hoffman RA. Standardization and quantitation in flow cytometry. Methods Cell Biol. 2001;63:299–340
  29. Geijtenbeek TB, Torensma R, van Vliet SJ, et al. Identification of DC-SIGN, a novel dendritic cell-specific ICAM-3 receptor that supports primary immune responses. Cell. 2000;100:575–585
  30. Carter LL, Swain SL. Single cell analyses of cytokine production. Curr Opin Immunol. 1997;9:177–182
  31. Schultz C. Intracytoplasmic detection of proinflammatory cytokines and chemokines in monocytes by flow cytometry. Methods Mol Biol. 2003;215:29–39
  32. Harvath L, Terle DA. Assay for phagocytosis. Methods Mol Biol. 1999;115:281–290
  33. Gordon S. The macrophage: past, present and future. Eur J Immunol. 2007;37(Suppl 1):S9–S17
  34. Pollard JW. Trophic macrophages in development and disease. Nat Rev. 2009;9:259–270
  35. Stout RD, Jiang C, Matta B, Tietzel I, Watkins SK, Suttles J. Macrophages sequentially change their functional phenotype in response to changes in microenvironmental influences. J Immunol. 2005;175:342–349
  36. Martinez FO, Helming L, Gordon S. Alternative activation of macrophages: an immunologic functional perspective. Annu Rev Immunol. 2009;27:451–483
  37. Mosser DM, Edwards JP. Exploring the full spectrum of macrophage activation. Nat Rev. 2008;8:958–969
  38. Mantovani A, Sica A, Sozzani S, Allavena P, Vecchi A, Locati M. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 2004;25:677–686
  39. Mosser DM. The many faces of macrophage activation. J Leukoc Biol. 2003;73:209–212
  40. Le Blanc K, Rasmusson I, Sundberg B, et al. Treatment of severe acute graft-versus-host disease with third party haploidentical mesenchymal stem cells. Lancet. 2004;363:1439–1441
  41. Le Blanc K, Frassoni F, Ball L, et al. Mesenchymal stem cells for treatment of steroid-resistant, severe, acute graft-versus-host disease: a phase II study. Lancet. 2008;371:1579–1586
  42. Chen SL, Fang WW, Ye F, et al. Effect on left ventricular function of intracoronary transplantation of autologous bone marrow mesenchymal stem cell in patients with acute myocardial infarction. Am J Cardiol. 2004;94:92–95
  43. Deda H, Inci MC, Kurekci AE, et al. Treatment of amyotrophic lateral sclerosis patients by autologous bone marrow-derived hematopoietic stem cell transplantation: a 1-year follow-up. Cytotherapy. 2009;11:18–25
  44. Bang OY, Lee JS, Lee PH, Lee G. Autologous mesenchymal stem cell transplantation in stroke patients. Ann Neurol. 2005;57:874–882
  45. Taupin P. OTI-010 Osiris therapeutics/jcr pharmaceuticals. Curr Opin Investig Drugs. 2006;7:473–481
  46. Abdi R, Fiorina P, Adra CN, Atkinson M, Sayegh MH. Immunomodulation by mesenchymal stem cells: a potential therapeutic strategy for type 1 diabetes. Diabetes. 2008;57:1759–1767
  47. Yoshikawa T, Mitsuno H, Nonaka I, et al. Wound therapy by marrow mesenchymal cell transplantation. Plast Reconstr Surg. 2008;121:860–877
  48. Charo IF, Ransohoff RM. The many roles of chemokines and chemokine receptors in inflammation. N Engl J Med. 2006;354:610–621
  49. Seager Danciger J, Lutz M, Hama S, et al. Method for large scale isolation, culture and cryopreservation of human monocytes suitable for chemotaxis, cellular adhesion assays, macrophage and dendritic cell differentiation. J Immunol Methods. 2004;288:123–134
  50. Martinez FO, Gordon S, Locati M, Mantovani A. Transcriptional profiling of the human monocyte-to-macrophage differentiation and polarization: new molecules and patterns of gene expression. J Immunol. 2006;177:7303–7311
  51. Fadok VA, Bratton DL, Konowal A, Freed PW, Westcott JY, Henson PM. Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/paracrine mechanisms involving TGF-beta, PGE2, and PAF. J Clin Invest. 1998;101:890–898
  52. Sallusto F, Lanzavecchia A. Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/macrophage colony-stimulating factor plus interleukin 4 and downregulated by tumor necrosis factor alpha. J Exp Med. 1994;179:1109–1118
  53. Jiang XX, Zhang Y, Liu B, et al. Human mesenchymal stem cells inhibit differentiation and function of monocyte-derived dendritic cells. Blood. 2005;105:4120–4126
  54. Nauta AJ, Kruisselbrink AB, Lurvink E, Willemze R, Fibbe WE. Mesenchymal stem cells inhibit generation and function of both CD34+-derived and monocyte-derived dendritic cells. J Immunol. 2006;177:2080–2087
  55. Ramasamy R, Fazekasova H, Lam EW, Soeiro I, Lombardi G, Dazzi F. Mesenchymal stem cells inhibit dendritic cell differentiation and function by preventing entry into the cell cycle. Transplantation. 2007;83:71–76
  56. Tiemessen MM, Jagger AL, Evans HG, van Herwijnen MJ, John S, Taams LS. CD4+CD25+Foxp3+ regulatory T cells induce alternative activation of human monocytes/macrophages. Proc Natl Acad Sci U S A. 2007;104:19446–19451
  57. Ortiz LA, Dutreil M, Fattman C, et al. Interleukin 1 receptor antagonist mediates the antiinflammatory and antifibrotic effect of mesenchymal stem cells during lung injury. Proc Natl Acad Sci U S A. 2007;104:11002–11007
  58. Nemeth K, Leelahavanichkul A, Yuen PS, et al. Bone marrow stromal cells attenuate sepsis via prostaglandin E(2)-dependent reprogramming of host macrophages to increase their interleukin-10 production. Nat Med. 2009;15:42–49
  59. Peister A, Mellad JA, Larson BL, Hall BM, Gibson LF, Prockop DJ. Adult stem cells from bone marrow (MSCs) isolated from different strains of inbred mice vary in surface epitopes, rates of proliferation, and differentiation potential. Blood. 2004;103:1662–1668
  60. Schneemann M, Schoeden G. Macrophage biology and immunology: man is not a mouse. J Leukoc Biol. 2007;81:579;discussion 580
  61. Tilg H, Trehu E, Atkins MB, Dinarello CA, Mier JW. Interleukin-6 (IL-6) as an anti-inflammatory cytokine: induction of circulating IL-1 receptor antagonist and soluble tumor necrosis factor receptor p55. Blood. 1994;83:113–118
  62. Xing Z, Gauldie J, Cox G, et al. IL-6 is an antiinflammatory cytokine required for controlling local or systemic acute inflammatory responses. J Clin Invest. 1998;101:311–320
  63. Gallucci RM, Simeonova PP, Matheson JM, et al. Impaired cutaneous wound healing in interleukin-6-deficient and immunosuppressed mice. FASEB J. 2000;14:2525–2531
  64. Gallucci RM, Sugawara T, Yucesoy B, et al. Interleukin-6 treatment augments cutaneous wound healing in immunosuppressed mice. J Interferon Cytokine Res. 2001;21:603–609
  65. Danon D, Madjar J, Edinov E, et al. Treatment of human ulcers by application of macrophages prepared from a blood unit. Exp Gerontol. 1997;32:633–641
  66. Zuloff-Shani A, Kachel E, Frenkel O, Orenstein A, Shinar E, Danon D. Macrophage suspensions prepared from a blood unit for treatment of refractory human ulcers. Transfus Apher Sci. 2004;30:163–167

PII: S0301-472X(09)00365-8

doi: 10.1016/j.exphem.2009.09.004

Experimental Hematology
Volume 37, Issue 12 , Pages 1445-1453 , December 2009

Article Tools

* Image Usage & Resolution