Table of Contents Author Guidelines Submit a Manuscript
Journal of Immunology Research
Volume 2016, Article ID 2414906, 12 pages
http://dx.doi.org/10.1155/2016/2414906
Research Article

F4/80+ Host Macrophages Are a Barrier to Murine Embryonic Stem Cell-Derived Hematopoietic Progenitor Engraftment In Vivo

1Quantitative and Systems Biology Graduate Group, School of Natural Sciences, University of California-Merced, Merced, CA 95340, USA
2Department of Molecular Cell Biology, Vrije University, Amsterdam, Netherlands
3Molecular and Cell Biology Unit, School of Natural Sciences, University of California-Merced, Merced, CA 95340, USA

Received 22 May 2016; Revised 3 September 2016; Accepted 4 October 2016

Academic Editor: Xiao-Feng Yang

Copyright © 2016 Heather L. Thompson et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. J. A. Bradley, E. M. Bolton, and R. A. Pedersen, “Stem cell medicine encounters the immune system,” Nature Reviews Immunology, vol. 2, no. 11, pp. 859–871, 2002. View at Publisher · View at Google Scholar · View at Scopus
  2. A. P. Chidgey and R. L. Boyd, “Immune privilege for stem cells: not as simple as it looked,” Cell Stem Cell, vol. 3, no. 4, pp. 357–358, 2008. View at Publisher · View at Google Scholar · View at Scopus
  3. H. L. Thompson and J. O. Manilay, “Embryonic Stem cell-derived hematopoietic stem cells: challenges in development, differentiation, and immunogenicity,” Current Topics in Medicinal Chemistry, vol. 11, no. 13, pp. 1621–1637, 2011. View at Publisher · View at Google Scholar · View at Scopus
  4. P. J. Fairchild, “Taming the lion: the challenge of immunity in regenerative medicine,” Regenerative Medicine, vol. 10, no. 3, pp. 227–229, 2015. View at Publisher · View at Google Scholar · View at Scopus
  5. T. Wekerle and M. Sykes, “Induction of tolerance,” Surgery, vol. 135, no. 4, pp. 359–364, 2004. View at Publisher · View at Google Scholar · View at Scopus
  6. T. M. Schmitt, R. F. de Pooter, M. A. Gronski, S. K. Cho, P. S. Ohashi, and J. C. Zúñiga-Pflücker, “Induction of T cell development and establishment of T cell competence from embryonic stem cells differentiated in vitro,” Nature Immunology, vol. 5, no. 4, pp. 410–417, 2004. View at Publisher · View at Google Scholar · View at Scopus
  7. E. M. Kim, R. Stultz, S. Bonde, and N. Zavazava, “Embryonic stem cell-derived T cells induce lethal graft-versus-host disease and reject allogenic skin grafts upon thymic selection,” American Journal of Transplantation, vol. 12, no. 3, pp. 600–609, 2012. View at Publisher · View at Google Scholar · View at Scopus
  8. S. L. McKinney-Freeman, O. Naveiras, F. Yates et al., “Surface antigen phenotypes of hematopoietic stem cells from embryos and murine embryonic stem cells,” Blood, vol. 114, no. 2, pp. 268–278, 2009. View at Publisher · View at Google Scholar · View at Scopus
  9. H. L. Thompson, B. T. McLelland, and J. O. Manilay, “Indirect immune recognition of mouse embryonic stem cell-derived hematopoietic progenitors in vitro,” Experimental Hematology, vol. 42, no. 5, pp. 347–359.e5, 2014. View at Publisher · View at Google Scholar · View at Scopus
  10. T. Yamane, N. Hosen, H. Yamazaki, and I. L. Weissman, “Expression of AA4.1 marks lymphohematopoietic progenitors in early mouse development,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 22, pp. 8953–8958, 2009. View at Publisher · View at Google Scholar · View at Scopus
  11. L. Verda, D. A. Kim, S. Ikehara et al., “Hematopoietic mixed chimerism derived from allogeneic embryonic stem cells prevents autoimmune diabetes mellitus in NOD mice,” Stem Cells, vol. 26, no. 2, pp. 381–386, 2008. View at Publisher · View at Google Scholar · View at Scopus
  12. S. Bonde, A. M. Dowden, K.-M. Chan, W. B. Tabayoyong, and N. Zavazava, “HOXB4 but not BMP4 confers self-renewal properties to ES-derived hematopoietic progenitor cells,” Transplantation, vol. 86, no. 12, pp. 1803–1809, 2008. View at Publisher · View at Google Scholar · View at Scopus
  13. C. A. Koch, P. Geraldes, and J. L. Platt, “Immunosuppression by embryonic stem cells,” Stem Cells, vol. 26, no. 1, pp. 89–98, 2008. View at Publisher · View at Google Scholar · View at Scopus
  14. N. J. Robertson, F. A. Brook, R. L. Gardner, S. P. Cobbold, H. Waldmann, and P. J. Fairchild, “Embryonic stem cell-derived tissues are immunogenic but their inherent immune privilege promotes the induction of tolerance,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 52, pp. 20920–20925, 2007. View at Publisher · View at Google Scholar · View at Scopus
  15. R.-J. Swijnenburg, M. Tanaka, H. Vogel et al., “Embryonic stem cell immunogenicity increases upon differentiation after transplantation into ischemic myocardium,” Circulation, vol. 112, no. 9, pp. I166–I172, 2005. View at Publisher · View at Google Scholar · View at Scopus
  16. R. Dressel, J. Schindehütte, T. Kuhlmann et al., “The tumorigenicity of mouse embryonic stem cells and in vitro differentiated neuronal cells is controlled by the recipients' immune response,” PLoS ONE, vol. 3, no. 7, Article ID e2622, 2008. View at Publisher · View at Google Scholar · View at Scopus
  17. W. B. Tabayoyong, J. G. Salas, S. Bonde, and N. Zavazava, “HOXB4-transduced embryonic stem cell-derived Lin-c-kit + and Lin-Sca-1+ hematopoietic progenitors express H60 and are targeted by NK cells,” Journal of Immunology, vol. 183, no. 9, pp. 5449–5457, 2009. View at Publisher · View at Google Scholar · View at Scopus
  18. R. V. Sionov, S. Yagel, R. Har-Nir, and R. Gallily, “Trophoblasts protect the inner cell mass from macrophage destruction,” Biology of Reproduction, vol. 49, no. 3, pp. 588–595, 1993. View at Publisher · View at Google Scholar · View at Scopus
  19. M. Molcanyi, B. Bosche, K. Kraitsy et al., “Pitfalls and fallacies interfering with correct identification of embryonic stem cells implanted into the brain after experimental traumatic injury,” Journal of Neuroscience Methods, vol. 215, no. 1, pp. 60–70, 2013. View at Publisher · View at Google Scholar · View at Scopus
  20. K. O. Lui, A. S. Boyd, S. P. Cobbold, H. Waldmann, and P. J. Fairchild, “A role for regulatory T cells in acceptance of ESC-derived tissues transplanted across an major histocompatibility complex barrier,” Stem Cells, vol. 28, no. 10, pp. 1905–1914, 2010. View at Publisher · View at Google Scholar · View at Scopus
  21. H. L. Thompson, B. T. McLelland, and J. O. Manilay, “Indirect immune recognition of mouse embryonic stem cell-derived hematopoietic progenitors in vitro,” Experimental Hematology, vol. 42, no. 5, pp. 347–359, 2014. View at Publisher · View at Google Scholar · View at Scopus
  22. M. Kennedy and G. M. Keller, “Hematopoietic commitment of ES cells in culture,” Methods in Enzymology, vol. 365, pp. 39–59, 2003. View at Publisher · View at Google Scholar · View at Scopus
  23. L. D. Shultz, B. L. Lyons, L. M. Burzenski et al., “Human lymphoid and myeloid cell development in NOD/LtSz-scid IL2Rγnull mice engrafted with mobilized human hemopoietic stem cells,” Journal of Immunology, vol. 174, no. 10, pp. 6477–6489, 2005. View at Publisher · View at Google Scholar · View at Scopus
  24. N. van Rooijen and E. van Kesteren-Hendrikx, “Clodronate liposomes: perspectives in research and therapeutics,” Journal of Liposome Research, vol. 12, no. 1-2, pp. 81–94, 2002. View at Publisher · View at Google Scholar · View at Scopus
  25. M. J. Ferkowicz, M. Starr, X. Xie et al., “CD41 expression defines the onset of primitive and definitive hematopoiesis in the murine embryo,” Development, vol. 130, no. 18, pp. 4393–4403, 2003. View at Publisher · View at Google Scholar · View at Scopus
  26. H. K. A. Mikkola, Y. Fujiwara, T. M. Schlaeger, D. Traver, and S. H. Orkin, “Expression of CD41 marks the initiation of definitive hematopoiesis in the mouse embryo,” Blood, vol. 101, no. 2, pp. 508–516, 2003. View at Publisher · View at Google Scholar · View at Scopus
  27. P. J. Murray and T. A. Wynn, “Protective and pathogenic functions of macrophage subsets,” Nature Reviews Immunology, vol. 11, no. 11, pp. 723–737, 2011. View at Publisher · View at Google Scholar · View at Scopus
  28. N. Van Rooijen and A. Sanders, “Liposome mediated depletion of macrophages: mechanism of action, preparation of liposomes and applications,” Journal of Immunological Methods, vol. 174, no. 1-2, pp. 83–93, 1994. View at Publisher · View at Google Scholar · View at Scopus
  29. P. R. Taylor, L. Martinez-Pomares, M. Stacey, H.-H. Lin, G. D. Brown, and S. Gordon, “Macrophage receptors and immune recognition,” Annual Review of Immunology, vol. 23, pp. 901–944, 2005. View at Publisher · View at Google Scholar · View at Scopus
  30. A. J. Mitchell, L. C. Pradel, L. Chasson et al., “Autofluorescence as a tool for myeloid cell analysis,” Journal of Leukocyte Biology, vol. 88, no. 3, pp. 597–603, 2010. View at Publisher · View at Google Scholar · View at Scopus
  31. A. Diefenbach, J. K. Hsia, M.-Y. B. Hsiung, and D. H. Raulet, “A novel ligand for the NKG2D receptor activates NK cells and macrophages and induces tumor immunity,” European Journal of Immunology, vol. 33, no. 2, pp. 381–391, 2003. View at Publisher · View at Google Scholar · View at Scopus
  32. D. H. Raulet, “Roles of the NKG2D immunoreceptor and its ligands,” Nature Reviews Immunology, vol. 3, no. 10, pp. 781–790, 2003. View at Publisher · View at Google Scholar · View at Scopus
  33. B. R. Blazar, F. P. Lindberg, E. Ingulli et al., “CD47 (Integrin-associated Protein) engagement of dendritic cell and macrophage counterreceptors is required to prevent the clearance of donor lymphohematopoietic cells,” Journal of Experimental Medicine, vol. 194, no. 4, pp. 541–549, 2001. View at Publisher · View at Google Scholar · View at Scopus
  34. S. Jaiswal, C. H. M. Jamieson, W. W. Pang et al., “CD47 is upregulated on circulating hematopoietic stem cells and leukemia cells to avoid phagocytosis,” Cell, vol. 138, no. 2, pp. 271–285, 2009. View at Publisher · View at Google Scholar · View at Scopus
  35. P. Oldenborg, “CD47: a cell surface glycoprotein which regulates multiple functions of hematopoietic cells in health and disease,” ISRN Hematology, vol. 2013, Article ID 614619, 19 pages, 2013. View at Publisher · View at Google Scholar
  36. M. Olsson and P.-A. Oldenborg, “CD47 on experimentally senescent murine RBCs inhibits phagocytosis following Fcγ receptor-mediated but not scavenger receptor-mediated recognition by macrophages,” Blood, vol. 112, no. 10, pp. 4259–4267, 2008. View at Publisher · View at Google Scholar · View at Scopus
  37. D. Holmannová, M. Kolácková, K. Kondélková, P. Kunes, J. Krejsek, and C. Andrýs, “CD200/CD200R paired potent inhibitory molecules regulating immune and inflammatory responses; Part I: CD200/CD200R structure, activation, and function,” Acta Medica (Hradec Králové), vol. 55, no. 1, pp. 12–17, 2012. View at Google Scholar · View at Scopus
  38. T. A. M. Steevels and L. Meyaard, “Immune inhibitory receptors: essential regulators of phagocyte function,” European Journal of Immunology, vol. 41, no. 3, pp. 575–587, 2011. View at Publisher · View at Google Scholar · View at Scopus
  39. M. F. Cesta, “Normal structure, function, and histology of the spleen,” Toxicologic Pathology, vol. 34, no. 5, pp. 455–465, 2006. View at Publisher · View at Google Scholar · View at Scopus
  40. N. Arora, P. L. Wenzel, S. L. McKinney-Freeman et al., “Effect of developmental stage of HSC and recipient on transplant outcomes,” Developmental Cell, vol. 29, no. 5, pp. 621–628, 2014. View at Publisher · View at Google Scholar · View at Scopus
  41. J. Ciriza, H. Thompson, R. Petrosian, J. O. Manilay, and M. E. García-Ojeda, “The migration of hematopoietic progenitors from the fetal liver to the fetal bone marrow: lessons learned and possible clinical applications,” Experimental Hematology, vol. 41, no. 5, pp. 411–423, 2013. View at Publisher · View at Google Scholar · View at Scopus
  42. R. K. Burt, L. Verda, D.-A. Kim, Y. Oyama, K. Luo, and C. Link, “Embryonic stem cells as an alternate marrow donor source: engraftment without graft-versus-host disease,” Journal of Experimental Medicine, vol. 199, no. 7, pp. 895–904, 2004. View at Publisher · View at Google Scholar · View at Scopus
  43. A. Chow, D. Lucas, A. Hidalgo et al., “Bone marrow CD169+ macrophages promote the retention of hematopoietic stem and progenitor cells in the mesenchymal stem cell niche,” The Journal of Experimental Medicine, vol. 208, no. 2, pp. 261–271, 2011. View at Publisher · View at Google Scholar · View at Scopus
  44. J. C. Frith, J. Mönkkönen, G. M. Blackburn, R. G. G. Russell, and M. J. Rogers, “Clodronate and liposome-encapsulated clodronate are metabolized to a toxic ATP analog, adenosine 5'-(β,γ-dichloromethylene) triphosphate, by mammalian cells in vitro,” Journal of Bone and Mineral Research, vol. 12, no. 9, pp. 1358–1367, 1997. View at Publisher · View at Google Scholar · View at Scopus
  45. P. J. M. Leenen, K. Radošević, J. S. A. Voerman et al., “Heterogeneity of mouse spleen dendritic cells: in vivo phagocytic activity, expression of macrophage markers, and subpopulation turnover,” The Journal of Immunology, vol. 160, no. 5, pp. 2166–2173, 1998. View at Google Scholar · View at Scopus
  46. D. E. Hughes, K. R. Wright, H. L. Uy et al., “Bisphosphonates promote apoptosis in murine osteoclasts in vitro and in vivo,” Journal of Bone and Mineral Research, vol. 10, no. 10, pp. 1478–1487, 1995. View at Google Scholar · View at Scopus
  47. G. W. Feith, M. J. J. T. Bogman, K. J. M. Assmann et al., “Decreased PMN accumulation and glomerular damage by clodronate liposome treatment in PMN-dependent anti-GBM nephritis in mice,” Experimental Nephrology, vol. 5, no. 4, pp. 301–304, 1997. View at Google Scholar · View at Scopus
  48. S. McKinney-Freeman, P. Cahan, H. Li et al., “The transcriptional landscape of hematopoietic stem cell ontogeny,” Cell Stem Cell, vol. 11, no. 5, pp. 701–714, 2012. View at Publisher · View at Google Scholar · View at Scopus
  49. R. Das, P. Guan, L. Sprague et al., “Janus kinase inhibition lessens inflammation and ameliorates disease in murine models of hemophagocytic lymphohistiocytosis,” Blood, vol. 127, no. 13, pp. 1666–1675, 2016. View at Publisher · View at Google Scholar
  50. G. S. Schulert and A. A. Grom, “Macrophage activation syndrome and cytokine-directed therapies,” Best Practice and Research: Clinical Rheumatology, vol. 28, no. 2, pp. 277–292, 2014. View at Publisher · View at Google Scholar · View at Scopus
  51. A. Hayden, S. Park, D. Giustini, A. Y. Lee, and L. Y. Chen, “Hemophagocytic syndromes (HPSs) including hemophagocytic lymphohistiocytosis (HLH) in adults: a systematic scoping review,” Blood Reviews, 2016. View at Publisher · View at Google Scholar
  52. F. O. Martinez and S. Gordon, “The M1 and M2 paradigm of macrophage activation: time for reassessment,” F1000Prime Reports, vol. 6, article 13, 2014. View at Publisher · View at Google Scholar · View at Scopus
  53. C. Iwamoto, K. Takenaka, S. Urata et al., “The BALB/c-specific polymorphic SIRPA enhances its affinity for human CD47, inhibiting phagocytosis against human cells to promote xenogeneic engraftment,” Experimental Hematology, vol. 42, no. 3, pp. 163–171, 2014. View at Publisher · View at Google Scholar · View at Scopus