Experimental Hematology
Volume 34, Issue 11 , Pages 1451-1461 , November 2006

Interferon-γ mediates suppression of erythropoiesis but not reduced red cell survival following CpG-ODN administration in vivo

  • Neeta Thawani

      Affiliations

    • Centre for the Study of Host Resistance, Research Institute of the McGill University Health Centre, Montreal, Quebec, Canada
    • Centre for Host-Parasite Interactions, Institute of Parasitology, McGill University, Montreal, Quebec, Canada
    • ,
  • Mifong Tam

      Affiliations

    • Centre for the Study of Host Resistance, Research Institute of the McGill University Health Centre, Montreal, Quebec, Canada
    • ,
  • Kai-Hsin Chang

      Affiliations

    • Centre for the Study of Host Resistance, Research Institute of the McGill University Health Centre, Montreal, Quebec, Canada
    • Division of Hematology, Department of Medicine, University of Washington, Seattle, Wash., USA
    • ,
  • Mary M. Stevenson

      Affiliations

    • Centre for the Study of Host Resistance, Research Institute of the McGill University Health Centre, Montreal, Quebec, Canada
    • Centre for Host-Parasite Interactions, Institute of Parasitology, McGill University, Montreal, Quebec, Canada
    • Corresponding Author InformationOffprint requests to: Mary M. Stevenson Ph.D., Centre for the Study of Host Resistance, Research Institute of the McGill University Health Centre, Rm. L11-409, 1650 Cedar Ave, Montreal, Quebec, Canada H3G 1A4

Received 10 March 2006 ,Revised 14 June 2006 ,Accepted 21 June 2006.

References 

  1. Rudin W, Quesniaux V, Favre N, Bordmann G. Malaria toxins from P. chabaudi chabaudi AS and P. berghei ANKA cause dyserythropoiesis in C57BL/6 mice. Parasitology. 1997;115:467–474
  2. Miller KL, Schooley JC, Smith KL, Kullgren B, Mahlmann LJ, Silverman PH. Inhibition of erythropoiesis by a soluble factor in murine malaria. Exp Hematol. 1989;17:379–385
  3. Yap GS, Stevenson MM. Production of soluble inhibitor of erythropoiesis during Plasmodium chabaudi AS infection in resistant and susceptible mice. Ann N Y Acad Sci. 1991;628:279–281
  4. McDevitt MA, Xie J, Gordeuk V, Bucala R. The anemia of malaria infection: role of inflammatory cytokines. Curr Hematol Rep. 2004;3:97–106
  5. Means RT, Krantz SB. Progress in understanding the pathogenesis of the anemia of chronic disease. Blood. 1992;80:1639–1647
  6. Alvarez-Hernandez X, Licega J, McKay I, Brock JH. Induction of hypoferremia and modulation of macrophage iron metabolism by tumor necrosis factor. Lab Invest. 1989;61:319–322
  7. Weiss G, Goodnough LT. Anemia of chronic disease. N Engl J Med. 2005;352:1011–1023
  8. Byrd T, Horwitz MA. Regulation of transferrin receptor expression and ferritin content in human mononuclear macrophages. Coordinate upregulation by iron transferrin and downregulation by interferon γ. J Clin Invest. 1993;91:969–976
  9. Klinman DM, Currie D, Gursel I, Verthelyi D. Use of CpG oligodeoxynucleotides as immune adjuvants. Immunol Rev. 2004;199:201–216
  10. Bafica A, Scanga CA, Feng CG, Leifer C, Cheever A, Sher A. TLR9 regulates Th1 responses and cooperates with TLR2 in mediating optimal resistance to Mycobacterium tuberculosis. J Exp Med. 2005;202:1715–1724
  11. Kalis C, Gumenscheimer M, Freudenberg N, et al. Requirement for TLR9 in the immunomodulatory activity of Propionibacterium acnes. J Immunol. 2005;174:4295–4300
  12. Coban C, Ishii KJ, Kawai T, et al. Toll-like receptor 9 mediates innate immune activation by the malaria pigment hemozoin. J Exp Med. 2005;201:19–25
  13. Milon G, Gheorghiu M, Lagranderie M, Lebastard M, Marchal G. BCG-induced anaemia in mice: no direct effect of the growth of bacilli. Ann Immunol (Paris). 1984;135:195–204
  14. Chang KH, Stevenson MM. Malarial anaemia: mechanisms and implications of insufficient erythropoiesis during blood-stage malaria. Int J Parasitol. 2004;34:1501–1516
  15. Brozovic B, Sljivic VS, Warr GW. Haematological changes and iron metabolism in rats after administration of Corynebacterium parvum. Br J Exp Pathol. 1975;56:183–192
  16. Rehli M. Of mice and men: species variations of Toll-like receptor expression. Trends Immunol. 2002;23:375–378
  17. Su Z, Tam MF, Jankovic D, Stevenson MM. Vaccination with novel immunostimulatory adjuvants against blood-stage malaria in mice. Infect Immun. 2003;71:5178–5187
  18. Apte RN, Galanos C, Pluznik DH. Lipid A, the active part of bacterial endotoxins in inducing serum colony-stimulating activity and proliferation of splenic granulocyte/macrophage progenitor cells. J. Cell Physiol. 1976;87:71–78
  19. Apte RN, Pluznik DH. Control mechanisms of endotoxin and particulate material stimulation of hemopoietic colony-forming cell differentiation. Exp Hematol. 1976;4:10–18
  20. Staber FG, Metcalf D. Cellular and molecular basis of the increased splenic hemopoiesis in mice treated with bacterial cell wall components. Proc Natl Acad Sci U S A. 1980;77:4322–4325
  21. Sparwasser T, Hultner L, Koch ES, Luz A, Lipford GB, Wagner H. Immunostimulatory CpG-oligodeoxynucleotides cause extramedullary murine hemopoiesis. J Immunol. 1999;162:2368–2374
  22. Cano LE, Kashino SS, Arruda C, et al. Protective role of γ interferon in experimental pulmonary paracoccidioidomycosis. Infect Immun. 1998;66:800–806
  23. de Jong K, Emerson RK, Butler J, Bastacky J, Mohandas N, Kuypers FA. Short survival of phosphatidylserine-exposing red blood cells in murine sickle cell anemia. Blood. 2001;98:1577–1584
  24. Zhang D, Johnson MM, Miller CP, Pircher TJ, Geiger JN, Wojchowski DM. An optimized system for studies of EPO-dependent murine pro-erythroblast development. Exp Hematol. 2001;29:1278–1288
  25. Means RT, Krantz SB, Luna J, Marsters SA, Ashkenazi A. Inhibition of murine erythroid colony formation in vitro by interferon γ and correction by interferon receptor immunoadhesin. Blood. 1994;83:911–915
  26. Quesniaux VF, Ryffel B. Interleukin-12-induced interferon-γ inhibits hematopoiesis in vivo in mice. Ann N Y Acad Sci. 1996;795:189–195
  27. Johnson CS, Cook CA, Furmanski P. In vivo suppression of erythropoiesis by tumor necrosis factor-α (TNF-α): reversal with exogenous erythropoietin (EPO). Exp Hematol. 1990;18:109–113
  28. Chang KH, Tam M, Stevenson MM. Modulation of the course and outcome of blood-stage malaria by erythropoietin-induced reticulocytosis. J Infect Dis. 2004;189:735–743
  29. Nijhof W, Goris H, Dontje B, Dresz J, Loeffler M. Optimal erythroid cell production during erythropoietin treatment of mice occurs by exploiting the splenic microenvironment. Exp Hematol. 1993;21:496–501
  30. Broudy VC, Lin N, Brice M, Nakamoto B, Papayannopoulou T. Erythropoietin receptor characteristics on primary human erythroid cells. Blood. 1991;77:2583–2590
  31. Kina T, Ikuta K, Takayama E. The monoclonal antibody TER-119 recognizes a molecule associated with glycophorin A and specifically marks the late stages of murine erythroid lineage. Br J Haematol. 2000;109:280–287
  32. Chang KH, Tam M, Stevenson MM. Inappropriately low reticulocytosis in severe malarial anemia correlates with suppression in the development of late erythroid precursors. Blood. 2004;103:3727–3735
  33. Lok CN, Loh TT. Regulation of transferrin function and expression: review and update. Biol Signals Recept. 1998;7:157–178
  34. Konijn AM, Carmel N, Levy R, Hershko C. Ferritin synthesis in inflammation. II. Mechanism of increased ferritin synthesis. Br J Haematol. 1981;49:361–368
  35. Socolovsky M, Nam HS, Lodish HF. Ineffective erythropoiesis in Stat 5α-/-5β-/- mice due to decreased survival of early erythroblasts. Blood. 2001;98:3261–3273
  36. May Lai CM, Swaminathan N, Klinken SP. IFN-α inhibits erythropoietin-induced proliferation but not differentiation, and restricts erythroleukemia development. J Interferon Cytokine Res. 1995;15:669–675
  37. Johnson CS, Keckler DJ, Furmanski PN. In vivo hematopoietic effects of rIL-1α: stimulation of granulocytic, monocytic, megakaryocytic and early erythroid progenitors, suppression of late-stage erythropoiesis and reversal of erythroid suppression with Epo. Blood. 1989;73:678–683
  38. Johnson C, Cook CA, Furmanski P. In vivo suppression of erythropoiesis by TNF-α: reversal with exogenous Epo. Exp Hematol. 1990;18:109–113
  39. Weiss G. Pathogenesis and treatment of anemia of chronic disease. Blood Rev. 2002;16:87–96
  40. Zermati Y, Fichelson S, Hermine O. TGF-β inhibits erythropoiesis by blocking proliferation and accelerating differentiation of erythroid progenitors. Exp Hematol. 2000;28:885–894
  41. Felli N, Pedini F, Zeuner A, et al. Multiple members of the TNF superfamily contribute to IFN-γ-mediated inhibition of erythropoiesis. J Immunol. 2005;175:1464–1472
  42. Ludwiczek S, Aigner E, Theurl I, Weiss G. Cytokine-mediated regulation of iron-transport in human monocytic cells. Blood. 2002;101:4148–4154
  43. Moldawer LL, Marano MA, Wei H, et al. Cachectin/tumour necrosis factor alters red blood cell kinetics and induces anemia in vivo. FASEB J. 1989;3:1637–1643

PII: S0301-472X(06)00409-7

doi: 10.1016/j.exphem.2006.06.014

Experimental Hematology
Volume 34, Issue 11 , Pages 1451-1461 , November 2006

Article Tools

* Image Usage & Resolution