Single and local blockade of interleukin-6 signaling promotes neuronal differentiation from transplanted embryonic stem cell-derived neural precursor cells

Journal of Neuroscience Research

Volumn 89, Issue 9, 2011, Pages 1388-1399

  Gomi, Masanori ^a,b   Aoki, Tomohiro ^b   Takagi, Yasushi ^b   Nishimura, Masaki ^b   Ohsugi, Yoshiyuki ^c   Mihara, Masahiko ^c   Nozaki, Kazuhiko ^b,d   Hashimoto, Nobuo ^b   Miyamoto, Susumu ^b   Takahashi, Jun ^a,b  

^a KYOTO UNIVERSITY   (Japan)

^b KYOTO UNIVERSITY   (Japan)

^c CHUGAI PHARMACEUTICAL CO LTD   (Japan)

^d SHIGA UNIVERSITY OF MEDICAL SCIENCE   (Japan)

Author keywords

Embryonic stem cells; IL 6; Immune response; Inflammation; Transplantation

Indexed keywords

CYCLOSPORIN A; INTERLEUKIN 1BETA; INTERLEUKIN 4; INTERLEUKIN 6; INTERLEUKIN 6 ANTIBODY;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN; CELL SURVIVAL; EMBRYONIC STEM CELL; GLIA CELL; IMMUNE RESPONSE; LEUKOCYTE; MACROPHAGE; MICROGLIA; MOUSE; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NEUROLOGIC DISEASE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PRIORITY JOURNAL; STROMA CELL;

ANIMALS; ANTIBODIES, BLOCKING; ANTIBODIES, MONOCLONAL; BRAIN; CELL DIFFERENTIATION; CELL SURVIVAL; CELLS, CULTURED; EMBRYONIC STEM CELLS; GRAFT SURVIVAL; INTERLEUKIN-6; MALE; MICE; MICE, INBRED C57BL; NEURAL STEM CELLS; STEM CELL TRANSPLANTATION;

EID: 79960035168     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.22667     Document Type: Article

References (44)

1. Barker RA, Widner H. 2004. Immune problems in central nervous system cell therapy. NeuroRx 1: 472-481.
2. Bryan D, Walker KB, Ferguson M, Thorpe R. 2005. Cytokine gene expression in a murine wound healing model. Cytokine 31: 429-438.
3. Carpenter LR, Yancopoulos GD, Stahl N. 1998. General mechanisms of cytokine receptor signaling. Adv Protein Chem 52: 109-140.
4. Chojnacki A, Shimazaki T, Gregg C, Weinmaster G, Weiss S. 2003. Glycoprotein 130 signaling regulates Notch1 expression and activation in the self-renewal of mammalian forebrain neural stem cells. J Neurosci 23: 1730-1741.
5. Fassbender K, Rossol S, Kammer T, Daffertshofer M, Wirth S, Dollman M, Hennerici M. 1994. Proinflammatory cytokines in serum of patients with acute cerebral ischemia: kinetics of secretion and relation to theextent of brain damage and outcome of disease. J Neurol Sci 122: 135-139.
6. Ferrari CC, Depino AM, Prada F, Muraro N, Campbell S, Podhajcer O, Perry VH, Anthony DC, Pitossi FJ. 2004. Reversible demyelination, blood-brain barrier breakdown, and pronounced neutrophil recruitment induced by chronic IL-1 expression in the brain. Am J Pathol 165: 1827-1837.
7. Gadient RA, Otten UH. 1997. Interleukin-6 (IL-6)-a molecule with both beneficial and destructive potentials. Prog Neurobiol 52: 379-390.
8. Gaiano N, Nye JS, Fishell G. 2000. Radial glial identity is promoted by Notch1 signaling in the murine forebrain. Neuron 26: 395-404.
9. Guo J, Zeng Y, Liang Y, Wang L, Su H, Wu W. 2007. Cyclosporine affects the proliferation and differentiation of neural stem cells in culture. Neuroreport 18: 863-868.
10. Ideguchi M, Shinoyama M, Gomi M, Hayashi H, Hashimoto N, Takahashi J. 2008. Immune or inflammatory response by the host brain suppresses neuronal differentiation of transplanted ES cell-derived neural precursor cells. J Neurosci Res 86: 1936-1943.
11. Ishibashi M, Moriyoshi K, Sasai Y, Shiota K, Nakanishi S, Kageyama R. 1994. Persistent expression of helix-loop-helix factor HES-1 prevents mammalian neural differentiation in the central nervous system. EMBO J 13: 1799-1805.
12. Ishibashi M, Ang SL, Shiota K, Nakanishi S, Kageyama R, Guillemot F. 1995. Targeted disruption of mammalian hairy and enhancer of split homolog-1 (HES-1) leads to up-regulation of neural helix-loop-helix factors, premature neurogenesis, and severe neural tube defects. Genes Dev 9: 3136-3148.
13. Kageyama R, Ohtsuka T, Hatakeyama J, Ohsawa R. 2005. Roles of bHLH genes in neural stem cell differentiation. Exp Cell Res 306: 343-348.
14. Kawasaki H, Mizuseki K, Nishikawa S, Kaneko S, Kuwana Y, Nakanishi S, Nishikawa SI, Sasai Y. 2000. Induction of midbrain dopaminergic neurons from ES cells by stromal cell-derived inducing activity. Neuron 28: 31-40.
15. Kishimoto T, Akira S, Narazaki M, Taga T. 1995. Interleukin-6 family of cytokines and gp130. Blood 86: 1243-1254.
16. Kossmann T, Hans VH, Imhof HG, Stocker R, Grob P, Trentz O, Morganti-Kossmann C. 1995. Intrathecal and serum interleukin-6 and the acute-phase response in patients with severe traumatic brain injuries. Shock 4: 311-317.
17. Li JY, Christophersen NS, Hall V, Soulet D, Brundin P. 2008. Critical issues of clinical human embryonic stem cell therapy for brain repair. Trends Neurosci 31: 146-153.
18. Maimone D, Guazzi GC, Annunziata P. 1997. IL-6 detection in multiple sclerosis brain. J Neurol Sci 146: 59-65.
19. McLoughlin RM, Hurst SM, Nowell MA, Harris DA, Horiuchi S, Morgan LW, Wilkinson TS, Yamamoto N, Topley N, Jones SA. 2004. Differential regulation of neutrophil-activating chemokines by IL-6 and its soluble receptor isoforms. J Immunol 172: 5676-5683.
20. McLoughlin RM, Jenkins BJ, Grail D, Williams AS, Fielding CA, Parker CR, Ernst M, Topley N, Jones SA. 2005. IL-6 trans-signaling via STAT3 directs T cell infiltration in acute inflammation. Proc Natl Acad Sci U S A 102: 9589-9594.
21. Meier-Kriesche HU, Li S, Gruessner RW, Fung JJ, Bustami RT, Barr ML, Leichtman AB. 2006. Immunosuppression: evolution in practice and trends, 1994-2004. Am J Transplant 6: 1111-1131.
22. Mima T, Nishimoto N. 2009. Clinical value of blocking IL-6 receptor. Curr Opin Rheumatol 21: 224-230.
23. Mirza B, Krook H, Andersson P, Larsson LC, Korsgren O, Widner H. 2004. Intracerebral cytokine profiles in adult rats grafted with neural tissue of different immunological disparity. Brain Res Bull 63: 105-118.
24. Monje ML, Toda H, Palmer TD. 2003. Inflammatory blockade restores adult hippocampal neurogenesis. Science 302: 1760-1765.
25. Nakanishi M, Niidome T, Matsuda S, Akaike A, Kihara T, Sugimoto H. 2007. Microglia-derived interleukin-6 and leukaemia inhibitory factor promote astrocytic differentiation of neural stem/progenitor cells. Eur J Neurosci 25: 649-658.
26. Nakashima K, Taga T. 2002. Mechanisms underlying cytokine-mediated cell-fate regulation in the nervous system. Mol Neurobiol 25: 233-244.
27. Newman MB, Bakay RA. 2008. Therapeutic potentials of human embryonic stem cells in Parkinson's disease. Neurotherapeutics 5: 237-251.
28. Nishimoto N, Kishimoto T. 2004. Inhibition of IL-6 for the treatment of inflammatory diseases. Curr Opin Pharmacol 4: 386-391.
29. Nishimoto N, Yoshizaki K, Maeda K, Kuritani T, Deguchi H, Sato B, Imai N, Suemura M, Kakehi T, Takagi N, Kishimoto T. 2003. Toxicity, pharmacokinetics, and dose-finding study of repetitive treatment with the humanized anti-interleukin 6 receptor antibody MRA in rheumatoid arthritis. Phase I/II clinical study. J Rheumatol 30: 1426-1435.
30. Okada S, Nakamura M, Mikami Y, Shimazaki T, Mihara M, Ohsugi Y, Iwamoto Y, Yoshizaki K, Kishimoto T, Toyama Y, Okano H. 2004. Blockade of interleukin-6 receptor suppresses reactive astrogliosis and ameliorates functional recovery in experimental spinal cord injury. J Neurosci Res 76: 265-276.
31. Okazaki M, Yamada Y, Nishimoto N, Yoshizaki K, Mihara M. 2002. Characterization of anti-mouse interleukin-6 receptor antibody. Immunol Lett 84: 231-240.
32. Olanow CW, Goetz CG, Kordower JH, Stoessl AJ, Sossi V, Brin MF, Shannon KM, Nauert GM, Perl DP, Godbold J, Freeman TB. 2003. A double-blind controlled trial of bilateral fetal nigral transplantation in Parkinson's disease. Ann Neurol 54: 403-414.
33. Preynat-Seauve O, Suter DM, Tirefort D, Turchi L, Virolle T, Chneiweiss H, Foti M, Lobrinus JA, Stoppini L, Feki A, Dubois-Dauphin M, Krause KH. 2009. Development of human nervous tissue upon differentiation of embryonic stem cells in three-dimensional culture. Stem Cells 27: 509-520.
34. Probert L, Akassoglou K, Pasparakis M, Kontogeorgos G, Kollias G. 1995. Spontaneous inflammatory demyelinating disease in transgenic mice showing central nervous system-specific expression of tumor necrosis factor alpha. Proc Natl Acad Sci U S A 92: 11294-11298.
35. Quagliarello V, Scheld WM. 1992. Bacterial meningitis: pathogenesis, pathophysiology, and progress. N Engl J Med 327: 864-872.
36. Quintana A, Muller M, Frausto RF, Ramos R, Getts DR, Sanz E, Hofer MJ, Krauthausen M, King NJ, Hidalgo J, Campbell IL. 2009. Site-specificproduction of IL-6 in the central nervous system retargets and enhances the inflammatory response in experimental autoimmune encephalomyelitis. J Immunol 183: 2079-2088.
37. Robel S, Mori T, Zoubaa S, Schlegel J, Sirko S, Faissner A, Goebbels S, Dimou L, Gotz M. 2009. Conditional deletion of beta1-integrin in astroglia causes partial reactive gliosis. Glia 57: 1630-1647.
38. Saijo K, Winner B, Carson CT, Collier JG, Boyer L, Rosenfeld MG, Gage FH, Glass CK. 2009. A Nurr1/CoREST pathway in microglia and astrocytes protects dopaminergic neurons from inflammation-induced death. Cell 137: 47-59.
39. Schobitz B, Voorhuis DA, De Kloet ER. 1992. Localization of interleukin 6 mRNA and interleukin 6 receptor mRNA in rat brain. Neurosci Lett 136: 189-192.
40. Tamura T, Udagawa N, Takahashi N, Miyaura C, Tanaka S, Yamada Y, Koishihara Y, Ohsugi Y, Kumaki K, Taga T, et al. 1993. Soluble interleukin-6 receptor triggers osteoclast formation by interleukin 6. Proc Natl Acad Sci U S A 90: 11924-11928.
41. Tanigaki K, Nogaki F, Takahashi J, Tashiro K, Kurooka H, Honjo T. 2001. Notch1 and Notch3 instructively restrict bFGF-responsive multipotent neural progenitor cells to an astroglial fate. Neuron 29: 45-55.
42. Vallieres L, Campbell IL, Gage FH, Sawchenko PE. 2002. Reduced hippocampal neurogenesis in adult transgenic mice with chronic astrocytic production of interleukin-6. J Neurosci 22: 486-492.
43. Van Assche G, Dalle I, Noman M, Aerden I, Swijsen C, Asnong K, Maes B, Ceuppens J, Geboes K, Rutgeerts P. 2003. A pilot study on the use of the humanized anti-interleukin-2 receptor antibody daclizumab in active ulcerative colitis. Am J Gastroenterol 98: 369-376.
44. Wright LS, Li J, Caldwell MA, Wallace K, Johnson JA, Svendsen CN. 2003. Gene expression in human neural stem cells: effects of leukemia inhibitory factor. J Neurochem 86: 179-195.