Journal of Neuroimmunology
Volume 173, Issue 1 , Pages 166-173 , April 2006

Cytokine profile of iron-laden macrophages: Implications for cellular magnetic resonance imaging

  • Ines Siglienti

      Affiliations

    • Department of Neurology, Julius-Maximilians-Universität, Josef-Schneider-Str. 11, 97080 Würzburg, Germany
    • Current address: Institute for MS-Research, Georg-August-Universität and Gemeinnützige Hertie-Stiftung, Waldweg 33, D-37073 Göttingen, Germany.
  • ,
  • Martin Bendszus

      Affiliations

    • Department of Neuroradiology, Julius-Maximilians-Universität, Josef-Schneider-Str. 11, 97080 Würzburg, Germany
  • ,
  • Christoph Kleinschnitz

      Affiliations

    • Department of Neurology, Julius-Maximilians-Universität, Josef-Schneider-Str. 11, 97080 Würzburg, Germany
  • ,
  • Guido Stoll

      Affiliations

    • Department of Neurology, Julius-Maximilians-Universität, Josef-Schneider-Str. 11, 97080 Würzburg, Germany
    • Corresponding Author InformationCorresponding author. Tel.: +49 931 20123769; fax: +49 931 20123489.

Received 17 August 2005 ,Accepted 15 November 2005.

References 

  1. Arbab AS, Bashaw LA, Miller BR, Jordan EK, Lewis BK, Kalish H, et al. Characterization of biophysical and metabolic properties of cells labeled with superparamagnetic iron oxide nanoparticles and transfection agent for cellular MR imaging. Radiology. 2003;229:838–846
  2. Arbab AS, Yocum GT, Kalish H, Jordan EK, Anderson SA, Khakoo AY, et al. Efficient magnetic cell labeling with protamine sulfate complexed to ferumoxides for cellular MRI. Blood. 2004;104:1217–1223
  3. Beckmann N, Falk R, Zurbrugg S, Dawson J, Engelhardt P. Macrophage infiltration into the rat knee detected by MRI in a model of antigen-induced arthritis. Magn. Reson. Med. 2003;49:1047–1055
  4. Bendszus M, Stoll G. Caught in the act: In vivo mapping of macrophage infiltration in nerve injury by magnetic resonance imaging. J. Neurosci. 2003;23:10892–10896
  5. Benveniste EN. Role of macrophages/microglia in multiple sclerosis and experimental allergic encephalomyelitis. J. Mol. Med. 1997;75:165–173
  6. Chen F, Ward J, Robinson PJ. MR imaging of the liver and spleen: A comparison of the effects on signal intensity of two superparamagnetic iron oxide agents. Magn. Reson. Imaging. 1999;17:549–556
  7. Chung IY, Norris JG, Benveniste EN. Differential tumor necrosis factor alpha expression by astrocytes from EAE-susceptible and -resistant rat strains. J. Exp. Med. 1991;173:801–811
  8. Cooke KR, Hill GR, Crawford JM, Bungard D, Brinson YS, Delmonte J, et al. Tumor necrosis factor-alpha production to lipopolysaccharide stimulation by donor cells predicts the severity of experimental acute graft-versus-host disease. J. Clin. Invest. 1998;102:1882–1891
  9. Corot C, Petry KG, Trivedi R, Saleh A, Jonkmanns C, Le Bas JF, et al. Macrophage imaging in central nervous system and in carotid atherosclerotic plaque using ultrasmall superparamagnetic iron oxide in magnetic resonance imaging. Invest. Radiol. 2004;39:619–625
  10. Donnelly RP, Freeman SL, Hayes MP. Inhibition of IL-10 expression by IFN-gamma up-regulates transcription of TNF-alpha in human monocytes. J. Immunol. 1995;155:1420–1427
  11. Dousset V, Delalande C, Ballarino L, Quesson B, Seilhan D, Coussemacq M, et al. In vivo macrophage activity imaging in the central nervous system detected by magnetic resonance. Magn. Res. Med. 1999;41:329–333
  12. 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
  13. Fearon DT, Locksley RM. The instructive role of innate immunity in the acquired immune response. Science. 1996;272:50–54
  14. Fiorentino DF, Zlotnik A, Mosmann TR, Howard M, Ogarra A. IL-10 inhibits cytokine production by activated macrophages. J. Immunol. 1991;147:3815–3822
  15. Floris S, Blezer ELA, Schreibelt G, Dopp E, van der Pol SMA, Schadee-Eestermans IL, et al. Blood–brain barrier permeability and monocyte infiltration in experimental allergic encephalomyelitis—a quantitative MRI study. Brain. 2004;127:616–627
  16. Huitinga I, Vanrooijen N, Degroot CJA, Uitdehaag BMJ, Dijkstra CD. Suppression of experimental allergic encephalomyelitis in Lewis rats after elimination of macrophages. J. Exp. Med. 1990;172:1025–1033
  17. Jander S, Pohl J, D'Urso D, Gillen C, Stoll G. Time course and cellular localization of interleukin-10 mRNA and protein expression in autoimmune inflammation of the rat central nervous system. Am. J. Pathol. 1998;152:975–982
  18. Jander S, Pohl J, Gillen C, Stoll G. Differential expression of interleukin-10 mRNA in Wallerian degeneration and immune-mediated inflammation of the rat peripheral nervous system. J. Neurosci. Res. 1996;43:254–259
  19. Juedes AE, Hjelmstrom P, Bergman CM, Neild AL, Ruddle NH. Kinetics and cellular origin of cytokines in the central nervous system: Insight into mechanisms of myelin oligodendrocyte glycoprotein-induced experimental autoimmune encephalomyelitis. J. Immunol. 2000;164:419–426
  20. Jung S, Siglienti I, Grauer O, Magnus T, Scarlato G, Toyka K. Induction of IL-10 in rat peritoneal macrophages and dendritic cells by glatiramer acetate. J. Neuroimmunol. 2004;148:63–73
  21. Kanno S, Wu YJL, Lee PC, Dodd SJ, Williams M, Griffith BP, et al. Macrophage accumulation associated with rat cardiac allograft rejection detected by magnetic resonance imaging with ultrasmall superparamagnetic iron oxide particles. Circulation. 2001;104:934–938
  22. Kim JG, Hahn YS. IFN-gamma inhibits the suppressive effects of PGE(2) on the production of tumor necrosis factor-alpha by mouse macrophages. Immunol. Invest. 2000;29:257–269
  23. Kleinschnitz C, Bendszus M, Frank M, Solymosi L, Toyka KV, Stoll G. In vivo monitoring of macrophage infiltration in experimental ischemic brain lesions by magnetic resonance imaging. J. Cereb. Blood Flow Metab. 2003;23:1356–1361
  24. Kostura L, Kraitchman DL, Mackay AM, Pittenger MF, Bulte JW. Feridex labeling of mesenchymal stem cells inhibits chondrogenesis but not adipogenesis or osteogenesis. NMR Biomed. 2004;17:513–517
  25. Magnus T, Chan A, Grauer O, Toyka KV, Gold R. Microglial phagocytosis of apoptotic inflammatory T cells leads to down-regulation of microglial immune activation. J. Immunol. 2001;167:5004–5010
  26. Malefyt RD, Abrams J, Bennett B, Figdor CG, Devries JE. Interleukin-10 (IL-10) inhibits cytokine synthesis by human monocytes—an autoregulatory role of IL-10 produced by monocytes. J. Exp. Med. 1991;174:1209–1220
  27. Rausch M, Hiestand P, Baumann D, Cannet C, Rudin M. MRI-based monitoring of inflammation and tissue damage in acute and chronic relapsing EAE. Magn. Reson. Med. 2003;50:309–314
  28. Raynal I, Prigent P, Peyramaure S, Najid A, Rebuzzi C, Corot C. Macrophage endocytosis of superparamagnetic iron oxide nanoparticles—mechanisms and comparison of Ferumoxides and Ferumoxtran-10. Invest. Radiol. 2004;39:56–63
  29. Renno T, Krakowski M, Piccirillo C, Lin JY, Owens T. TNF-alpha expression by resident microglia and infiltrating leukocytes in the central nervous system of mice with experimental allergic encephalomyelitis—regulation by Th1 cytokines. J. Immunol. 1995;154:944–953
  30. Saleh A, Schroeter M, Jonkmanns C, Hartung HP, Modder U, Jander S. In vivo MRI of brain inflammation in human ischaemic stroke. Brain. 2004;127:1670–1677
  31. Selmaj K, Raine CS, Cannella B, Brosnan CF. Identification of lymphotoxin and tumor-necrosis-factor in multiple sclerosis lesions. J. Clin. Invest. 1991;87:949–954
  32. Shamsi K, Balzer T, Saini S, Ros PR, Nelson RC, Carter EC, et al. Superparamagnetic iron oxide particles (SH U 555 A): Evaluation of efficacy in three doses for hepatic MR imaging. Radiology. 1998;206:365–371
  33. Stoll G, Jander S. The role of microglia and macrophages in the pathophysiology of the CNS. Prog. Neurobiol. 1999;58:233–247
  34. Stoll G, Jander S, Schroeter M. Detrimental and beneficial effects of injury-induced inflammation and cytokine expression in the nervous system. In:  Alzheimer C editors. Molecular and Cellular Biology of Neuroprotection in the CNS. vol. 513:2002;p. 87–113
  35. Stoll G, Wesemeier C, Gold R, Solymosi L, Toyka KV, Bendszus M. In vivo monitoring of macrophage infiltration in experimental autoimmune neuritis by magnetic resonance imaging. J. Neuroimmunol. 2004;149:142–146
  36. Trivedi RA, U-King-Im JM, Graves MJ, Cross JJ, Horsley J, Goddard MJ, et al. In vivo detection of macrophages in human carotid atheroma: temporal dependence of ultrasmall superparamagnetic particles of iron oxide-enhanced MRI. Stroke. 2004;35:1631–1635
  37. Voll RE, Herrmann M, Roth EA, Stach C, Kalden JR, Girkontaite I. Immunosuppressive effects of apoptotic cells. Nature. 1997;390:350–351
  38. Wanidworanun C, Strober W. Predominant role of tumor necrosis factor-alpha in human monocyte IL-10 synthesis. J. Immunol. 1993;151:6853–6861

PII: S0165-5728(05)00495-9

doi: 10.1016/j.jneuroim.2005.11.011

Journal of Neuroimmunology
Volume 173, Issue 1 , Pages 166-173 , April 2006