Direct and indirect effects of immune and central nervous system-resident cells on human oligodendrocyte progenitor cell differentiation

Journal of Immunology

Volumn 194, Issue 2, 2015, Pages 761-772

  Moore, Craig S ^a   Cui, Qiao Ling ^a   Warsi, Nebras M ^a   Durafourt, Bryce A ^a   Zorko, Nika ^a   Owen, David R ^b   Antel, Jack P ^a   Bar Or, Amit ^a  

^a MCGILL UNIVERSITY   (Canada)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON INDUCIBLE PROTEIN 10; TUMOR NECROSIS FACTOR ALPHA; CULTURE MEDIUM; CXCL10 PROTEIN, MOUSE;

ADULT; ARTICLE; ASTROCYTE; BONE MARROW CELL; CELL DEATH; CELL DIFFERENTIATION; CELL LINEAGE; CELL MATURATION; CELL SURVIVAL; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; CULTURE MEDIUM; CYTOKINE RELEASE; CYTOTOXICITY; FETUS; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNE SYSTEM; IMMUNOCOMPETENT CELL; MACROPHAGE; MICROGLIA; MULTIPLE SCLEROSIS; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; OLIGODENDROCYTE PRECURSOR CELL; OLIGODENDROGLIA; TH1 CELL; TH17 CELL; TH2 CELL; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; FEMALE; IMMUNOLOGY; MALE; PHARMACOLOGY;

ASTROCYTES; CELL DIFFERENTIATION; CELLS, CULTURED; CENTRAL NERVOUS SYSTEM; CHEMOKINE CXCL10; CULTURE MEDIA, CONDITIONED; FEMALE; HUMANS; MACROPHAGES; MALE; NEURAL STEM CELLS; OLIGODENDROGLIA; TH1 CELLS; TH17 CELLS; TH2 CELLS;

EID: 84920410942     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1401156     Document Type: Article

References (60)

1. Lassmann, H., and J. van Horssen. 2011. The molecular basis of neurodegeneration in multiple sclerosis. FEBS Lett. 585: 3715-3723.
2. Oreja-Guevara, C., J. Ramos-Cejudo, L. S. Aroeira, B. Chamorro, and E. Diez-Tejedor. 2012. TH1/TH2 Cytokine profile in relapsing-remitting multiple sclerosis patients treated with Glatiramer acetate or Natalizumab. BMC Neurol. 12: 95.
3. Cui, Q. L., T. Kuhlmann, V. E. Miron, S. Y. Leong, J. Fang, P. Gris, T. E. Kennedy, G. Almazan, and J. Antel. 2013. Oligodendrocyte progenitor cell susceptibility to injury in multiple sclerosis. Am. J. Pathol. 183: 516-525.
4. D'Souza, S., K. Alinauskas, E. McCrea, C. Goodyer, and J. P. Antel. 1995. Differential susceptibility of human CNS-derived cell populations to TNFdependent and independent immune-mediated injury. J. Neurosci. 15: 7293- 7300.
5. Selmaj, K., and C. S. Raine. 1988. Tumor necrosis factor mediates myelin damage in organotypic cultures of nervous tissue. Ann. N. Y. Acad. Sci. 540: 568-570.
6. Selmaj, K. W., and C. S. Raine. 1988. Tumor necrosis factor mediates myelin and oligodendrocyte damage in vitro. Ann. Neurol. 23: 339-346.
7. Louis, J. C., E. Magal, S. Takayama, and S. Varon. 1993. CNTF protection of oligodendrocytes against natural and tumor necrosis factor-induced death. Science 259: 689-692.
8. Bennett, J. L., and O. Stüve. 2009. Update on inflammation, neurodegeneration, and immunoregulation in multiple sclerosis: Therapeutic implications. Clin. Neuropharmacol. 32: 121-132.
9. Kuhlmann, T., V. Miron, Q. Cui, C. Wegner, J. Antel, and W. Brück. 2008. Differentiation block of oligodendroglial progenitor cells as a cause for remyelination failure in chronic multiple sclerosis. [Published erratum appears in 2009 Brain 132: 1118.] Brain 131: 1749-1758.
10. Sica, A., and A. Mantovani. 2012. Macrophage plasticity and polarization: In vivo veritas. J. Clin. Invest. 122: 787-795.
11. Durafourt, B. A., C. S. Moore, D. A. Zammit, T. A. Johnson, F. Zaguia, M. C. Guiot, A. Bar-Or, and J. P. Antel. 2012. Comparison of polarization properties of human adult microglia and blood-derived macrophages. Glia 60: 717-727.
12. Moore, C. S., V. T. Rao, B. A. Durafourt, B. J. Bedell, S. K. Ludwin, A. Bar-Or, and J. P. Antel. 2013. miR-155 as a multiple sclerosis-relevant regulator of myeloid cell polarization. Ann. Neurol. 74: 709-720.
13. Séguin, R., K. Biernacki, A. Prat, K. Wosik, H. J. Kim, M. Blain, E. McCrea, A. Bar-Or, and J. P. Antel. 2003. Differential effects of Th1 and Th2 lymphocyte supernatants on human microglia. Glia 42: 36-45.
14. Kim, H. J., I. Ifergan, J. P. Antel, R. Seguin, M. Duddy, Y. Lapierre, F. Jalili, and A. Bar-Or. 2004. Type 2 monocyte and microglia differentiation mediated by glatiramer acetate therapy in patients with multiple sclerosis. J. Immunol. 172: 7144-7153.
15. Vogel, D. Y., E. J. Vereyken, J. E. Glim, P. D. Heijnen, M. Moeton, P. van der Valk, S. Amor, C. E. Teunissen, J. van Horssen, and C. D. Dijkstra. 2013. Macrophages in inflammatory multiple sclerosis lesions have an intermediate activation status. J. Neuroinflammation 10: 35.
16. Miron, V. E., A. Boyd, J. W. Zhao, T. J. Yuen, J. M. Ruckh, J. L. Shadrach, P. van Wijngaarden, A. J. Wagers, A. Williams, R. J. Franklin, and C. ffrench-Constant. 2013. M2 microglia and macrophages drive oligodendrocyte differentiation during CNS remyelination. Nat. Neurosci. 16: 1211-1218.
17. Williams, A., G. Piaton, and C. Lubetzki. 2007. Astrocytes-friends or foes in multiple sclerosis? Glia 55: 1300-1312.
18. Moore, C. S., S. L. Abdullah, A. Brown, A. Arulpragasam, and S. J. Crocker. 2011. How factors secreted from astrocytes impact myelin repair. J. Neurosci. Res. 89: 13-21.
19. Durafourt, B. A., C. S. Moore, M. Blain, and J. P. Antel. 2013. Isolating, culturing, and polarizing primary human adult and fetal microglia. Methods Mol. Biol. 1041: 199-211.
20. Wu, C., S. Y. Leong, C. S. Moore, Q. L. Cui, P. Gris, L. P. Bernier, T. A. Johnson, P. Séguéla, T. E. Kennedy, A. Bar-Or, and J. P. Antel. 2013. Dual effects of daily FTY720 on human astrocytes in vitro: relevance for neuroinflammation. J. Neuroinflammation 10: 41.
21. Livak, K. J., and T. D. Schmittgen. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(2Delta Delta C(T)) Method. Methods 25: 402-408.
22. Lisak, R. P., J. A. Benjamins, L. Nedelkoska, J. L. Barger, S. Ragheb, B. Fan, N. Ouamara, T. A. Johnson, S. Rajasekharan, and A. Bar-Or. 2012. Secretory products of multiple sclerosis B cells are cytotoxic to oligodendroglia in vitro. J. Neuroimmunol. 246: 85-95.
23. Zhang, Y., F. Jalili, N. Ouamara, A. Zameer, G. Cosentino, M. Mayne, L. Hayardeny, J. P. Antel, A. Bar-Or, and G. R. John. 2010. Glatiramer acetatereactive T lymphocytes regulate oligodendrocyte progenitor cell number in vitro: role of IGF-2. J. Neuroimmunol. 227: 71-79.
24. Selmaj, K., C. S. Raine, B. Cannella, and C. F. Brosnan. 1991. Identification of lymphotoxin and tumor necrosis factor in multiple sclerosis lesions. J. Clin. Invest. 87: 949-954.
25. Su, Z., Y. Yuan, J. Chen, Y. Zhu, Y. Qiu, F. Zhu, A. Huang, and C. He. 2011. Reactive astrocytes inhibit the survival and differentiation of oligodendrocyte precursor cells by secreted TNF-a. J. Neurotrauma 28: 1089-1100.
26. Paintlia, M. K., A. S. Paintlia, A. K. Singh, and I. Singh. 2011. Synergistic activity of interleukin-17 and tumor necrosis factor-a enhances oxidative stressmediated oligodendrocyte apoptosis. J. Neurochem. 116: 508-521.
27. Kim, S., A. J. Steelman, H. Koito, and J. Li. 2011. Astrocytes promote TNFmediated toxicity to oligodendrocyte precursors. J. Neurochem. 116: 53-66.
28. Theibich, A., L. Dreyer, M. Magyari, and H. Locht. 2014. Demyelinizing neurological disease after treatment with tumor necrosis factor alpha-inhibiting agents in a rheumatological outpatient clinic: description of six cases. Clin. Rheumatol. 33: 719-723.
29. Seror, R., C. Richez, C. Sordet, S. Rist, L. Gossec, G. Direz, E. Houvenagel, J. M. Berthelot, C. Pagnoux, E. Dernis, et al; Club Rhumatismes et Inflammation Section of the SFR. 2013. Pattern of demyelination occurring during anti-TNF-a therapy: A French national survey. Rheumatology (Oxford) 52: 868-874.
30. Matsumoto, T., I. Nakamura, A. Miura, G. Momoyama, and K. Ito. 2013. Newonset multiple sclerosis associated with adalimumab treatment in rheumatoid arthritis: A case report and literature review. Clin. Rheumatol. 32: 271-275.
31. Maier, O., R. Fischer, C. Agresti, and K. Pfizenmaier. 2013. TNF receptor 2 protects oligodendrocyte progenitor cells against oxidative stress. Biochem. Biophys. Res. Commun. 440: 336-341.
32. Arnett, H. A., J. Mason, M. Marino, K. Suzuki, G. K. Matsushima, and J. P. Ting. 2001. TNF alpha promotes proliferation of oligodendrocyte progenitors and remyelination. Nat. Neurosci. 4: 1116-1122.
33. Fischer, R., H. Wajant, R. Kontermann, K. Pfizenmaier, and O. Maier. 2014. Astrocyte-specific activation of TNFR2 promotes oligodendrocyte maturation by secretion of leukemia inhibitory factor. Glia 62: 272-283.
34. Patel, J. R., J. L. Williams, M. M. Muccigrosso, L. Liu, T. Sun, J. B. Rubin, and R. S. Klein. 2012. Astrocyte TNFR2 is required for CXCL12-mediated regulation of oligodendrocyte progenitor proliferation and differentiation within the adult CNS. Acta Neuropathol. 124: 847-860.
35. Schafer, D. P., E. K. Lehrman, A. G. Kautzman, R. Koyama, A. R. Mardinly, R. Yamasaki, R. M. Ransohoff, M. E. Greenberg, B. A. Barres, and B. Stevens. 2012. Microglia sculpt postnatal neural circuits in an activity and complementdependent manner. Neuron 74: 691-705.
36. Plemel, J. R., S. B. Manesh, J. S. Sparling, and W. Tetzlaff. 2013. Myelin inhibits oligodendroglial maturation and regulates oligodendrocytic transcription factor expression. Glia 61: 1471-1487.
37. Nielsen, H. H., R. Ladeby, C. Fenger, H. Toft-Hansen, A. A. Babcock, T. Owens, and B. Finsen. 2009. Enhanced microglial clearance of myelin debris in T cellinfiltrated central nervous system. J. Neuropathol. Exp. Neurol. 68: 845-856.
38. Mantovani, A., S. K. Biswas, M. R. Galdiero, A. Sica, and M. Locati. 2013. Macrophage plasticity and polarization in tissue repair and remodelling. J. Pathol. 229: 176-185.
39. Zhang, Z., Z. Y. Zhang, J. Schittenhelm, Y. Wu, R. Meyermann, and H. J. Schluesener. 2011. Parenchymal accumulation of CD163+ macrophages/microglia in multiple sclerosis brains. J. Neuroimmunol. 237: 73-79.
40. Hu, X., P. Li, Y. Guo, H. Wang, R. K. Leak, S. Chen, Y. Gao, and J. Chen. 2012. Microglia/macrophage polarization dynamics reveal novel mechanism of injury expansion after focal cerebral ischemia. Stroke 43: 3063-3070.
41. Shechter, R., O. Miller, G. Yovel, N. Rosenzweig, A. London, J. Ruckh, K. W. Kim, E. Klein, V. Kalchenko, P. Bendel, et al. 2013. Recruitment of beneficial M2 macrophages to injured spinal cord is orchestrated by remote brain choroid plexus. Immunity 38: 555-569.
42. Butovsky, O., M. P. Jedrychowski, C. S. Moore, R. Cialic, A. J. Lanser, G. Gabriely, T. Koeglsperger, B. Dake, P. M. Wu, C. E. Doykan, et al. 2014. Identification of a unique TGF-b-dependent molecular and functional signature in microglia. Nat. Neurosci. 17: 131-143.
43. Taylor, D. L., G. Pirianov, S. Holland, C. J. McGinnity, A. L. Norman, C. Reali, L. T. Diemel, D. Gveric, D. Yeung, and H. Mehmet. 2010. Attenuation of proliferation in oligodendrocyte precursor cells by activated microglia. J. Neurosci. Res. 88: 1632-1644.
44. Bai, L., D. P. Lennon, V. Eaton, K. Maier, A. I. Caplan, S. D. Miller, and R. H. Miller. 2009. Human bone marrow-derived mesenchymal stem cells induce Th2-polarized immune response and promote endogenous repair in animal models of multiple sclerosis. Glia 57: 1192-1203.
45. Moore, C. S., R. Milner, A. Nishiyama, R. F. Frausto, D. R. Serwanski, R. R. Pagarigan, J. L. Whitton, R. H. Miller, and S. J. Crocker. 2011. Astrocytic tissue inhibitor of metalloproteinase-1 (TIMP-1) promotes oligodendrocyte differentiation and enhances CNS myelination. J. Neurosci. 31: 6247-6254.
46. Silberstein, F. C., R. De Simone, G. Levi, and F. Aloisi. 1996. Cytokineregulated expression of platelet-derived growth factor gene and protein in cultured human astrocytes. J. Neurochem. 66: 1409-1417.
47. Aloisi, F., S. Rosa, U. Testa, P. Bonsi, G. Russo, C. Peschle, and G. Levi. 1994. Regulation of leukemia inhibitory factor synthesis in cultured human astrocytes. J. Immunol. 152: 5022-5031.
48. Su, J. J., M. Osoegawa, T. Matsuoka, M. Minohara, M. Tanaka, T. Ishizu, F. Mihara, T. Taniwaki, and J. Kira. 2006. Upregulation of vascular growth factors in multiple sclerosis: correlation with MRI findings. J. Neurol. Sci. 243: 21-30.
49. Cuzner, M. L., D. Gveric, C. Strand, A. J. Loughlin, L. Paemen, G. Opdenakker, and J. Newcombe. 1996. The expression of tissue-type plasminogen activator, matrix metalloproteases and endogenous inhibitors in the central nervous system in multiple sclerosis: comparison of stages in lesion evolution. J. Neuropathol. Exp. Neurol. 55: 1194-1204.
50. Slaets, H., J. J. Hendriks, C. Van den Haute, F. Coun, V. Baekelandt, P. Stinissen, and N. Hellings. 2010. CNS-targeted LIF expression improves therapeutic efficacy and limits autoimmune-mediated demyelination in a model of multiple sclerosis. Mol. Ther. 18: 684-691.
51. McKinnon, R. D., T. Matsui, M. Dubois-Dalcq, and S. A. Aaronson. 1990. FGF modulates the PDGF-driven pathway of oligodendrocyte development. Neuron 5: 603-614.
52. McKinnon, R. D., C. Smith, T. Behar, T. Smith, and M. Dubois-Dalcq. 1993. Distinct effects of bFGF and PDGF on oligodendrocyte progenitor cells. Glia 7: 245-254.
53. Cui, Q. L., G. Fragoso, V. E. Miron, P. J. Darlington, W. E. Mushynski, J. Antel, and G. Almazan. 2010. Response of human oligodendrocyte progenitors to growth factors and axon signals. J. Neuropathol. Exp. Neurol. 69: 930-944.
54. Sui, Y., R. Potula, N. Dhillon, D. Pinson, S. Li, A. Nath, C. Anderson, J. Turchan, D. Kolson, O. Narayan, and S. Buch. 2004. Neuronal apoptosis is mediated by CXCL10 overexpression in simian human immunodeficiency virus encephalitis. Am. J. Pathol. 164: 1557-1566.
55. Sui, Y., L. Stehno-Bittel, S. Li, R. Loganathan, N. K. Dhillon, D. Pinson, A. Nath, D. Kolson, O. Narayan, and S. Buch. 2006. CXCL10-induced cell death in neurons: role of calcium dysregulation. Eur. J. Neurosci. 23: 957-964.
56. Balashov, K. E., J. B. Rottman, H. L. Weiner, and W. W. Hancock. 1999. CCR5 (+) and CXCR3(+) T cells are increased in multiple sclerosis and their ligands MIP-1alpha and IP-10 are expressed in demyelinating brain lesions. Proc. Natl. Acad. Sci. USA 96: 6873-6878.
57. Simpson, J. E., J. Newcombe, M. L. Cuzner, and M. N. Woodroofe. 2000. Expression of the interferon-gamma-inducible chemokines IP-10 and Mig and their receptor, CXCR3, in multiple sclerosis lesions. Neuropathol. Appl. Neurobiol. 26: 133-142.
58. Sørensen, T. L., C. Trebst, P. Kivisäkk, K. L. Klaege, A. Majmudar, R. Ravid, H. Lassmann, D. B. Olsen, R. M. Strieter, R. M. Ransohoff, and F. Sellebjerg. 2002. Multiple sclerosis: A study of CXCL10 and CXCR3 co-localization in the inflamed central nervous system. J. Neuroimmunol. 127: 59-68.
59. Tanuma, N., H. Sakuma, A. Sasaki, and Y. Matsumoto. 2006. Chemokine expression by astrocytes plays a role in microglia/macrophage activation and subsequent neurodegeneration in secondary progressive multiple sclerosis. Acta Neuropathol. 112: 195-204.
60. Tirotta, E., R. M. Ransohoff, and T. E. Lane. 2011. CXCR2 signaling protects oligodendrocyte progenitor cells from IFN-g/CXCL10-mediated apoptosis. Glia 59: 1518-1528.