IL-17A Activates ERK1/2 and Enhances Differentiation of Oligodendrocyte Progenitor Cells

Overview

Journal Glia

Specialty Neurology

Date 2015 Jan 6

PMID 25557204

Citations 32

Authors

Jane M Rodgers

Andrew P Robinson

Elen S Rosler

Karen Lariosa-Willingham

Rachael E Persons

Jason C Dugas

Stephen D Miller

Affiliations

Soon will be listed here.

Abstract

Inflammatory signals present in demyelinated multiple sclerosis lesions affect the reparative remyelination process conducted by oligodendrocyte progenitor cells (OPCs). Interferon-γ (IFN-γ), tumor necrosis factor-α (TNF-α), and interleukin (IL)-6 have differing effects on the viability and growth of OPCs, however the effects of IL-17A are largely unknown. Primary murine OPCs were stimulated with IL-17A and their viability, proliferation, and maturation were assessed in culture. IL-17A-stimulated OPCs exited the cell cycle and differentiated with no loss in viability. Expression of the myelin-specific protein, proteolipid protein, increased in a cerebellar slice culture assay in the presence of IL-17A. Downstream, IL-17A activated ERK1/2 within 15 min and induced chemokine expression in 2 days. These results demonstrate that IL-17A exposure stimulates OPCs to mature and participate in the inflammatory response.

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References

Wolswijk G . Oligodendrocyte survival, loss and birth in lesions of chronic-stage multiple sclerosis. Brain. 1999; 123 ( Pt 1):105-15. DOI: 10.1093/brain/123.1.105. View

Maeda Y, Solanky M, Menonna J, Chapin J, Li W, Dowling P . Platelet-derived growth factor-alpha receptor-positive oligodendroglia are frequent in multiple sclerosis lesions. Ann Neurol. 2001; 49(6):776-85. DOI: 10.1002/ana.1015. View

Lock C, Hermans G, Pedotti R, Brendolan A, Schadt E, Garren H . Gene-microarray analysis of multiple sclerosis lesions yields new targets validated in autoimmune encephalomyelitis. Nat Med. 2002; 8(5):500-8. DOI: 10.1038/nm0502-500. View

Vela J, Molina-Holgado E, Arevalo-Martin A, Almazan G, Guaza C . Interleukin-1 regulates proliferation and differentiation of oligodendrocyte progenitor cells. Mol Cell Neurosci. 2002; 20(3):489-502. DOI: 10.1006/mcne.2002.1127. View

Valerio A, Ferrario M, Dreano M, Garotta G, Spano P, Pizzi M . Soluble interleukin-6 (IL-6) receptor/IL-6 fusion protein enhances in vitro differentiation of purified rat oligodendroglial lineage cells. Mol Cell Neurosci. 2002; 21(4):602-15. DOI: 10.1006/mcne.2002.1208. View

Pizzi M, Sarnico I, Boroni F, Benarese M, Dreano M, Garotta G . Prevention of neuron and oligodendrocyte degeneration by interleukin-6 (IL-6) and IL-6 receptor/IL-6 fusion protein in organotypic hippocampal slices. Mol Cell Neurosci. 2004; 25(2):301-11. DOI: 10.1016/j.mcn.2003.10.022. View

Barres B, Hart I, Coles H, Burne J, Voyvodic J, Richardson W . Cell death and control of cell survival in the oligodendrocyte lineage. Cell. 1992; 70(1):31-46. DOI: 10.1016/0092-8674(92)90531-g. View

McKinnon R, Piras G, Ida Jr J, Dubois-Dalcq M . A role for TGF-beta in oligodendrocyte differentiation. J Cell Biol. 1993; 121(6):1397-407. PMC: 2119703. DOI: 10.1083/jcb.121.6.1397. View

Corbin J, Kelly D, Rath E, Baerwald K, Suzuki K, Popko B . Targeted CNS expression of interferon-gamma in transgenic mice leads to hypomyelination, reactive gliosis, and abnormal cerebellar development. Mol Cell Neurosci. 1996; 7(5):354-70. DOI: 10.1006/mcne.1996.0026. View

10.

Pang Y, Cai Z, Rhodes P . Effect of tumor necrosis factor-alpha on developing optic nerve oligodendrocytes in culture. J Neurosci Res. 2005; 80(2):226-34. DOI: 10.1002/jnr.20450. View

11.

Lin W, Harding H, Ron D, Popko B . Endoplasmic reticulum stress modulates the response of myelinating oligodendrocytes to the immune cytokine interferon-gamma. J Cell Biol. 2005; 169(4):603-12. PMC: 2171696. DOI: 10.1083/jcb.200502086. View

12.

Chew L, King W, Kennedy A, Gallo V . Interferon-gamma inhibits cell cycle exit in differentiating oligodendrocyte progenitor cells. Glia. 2005; 52(2):127-43. DOI: 10.1002/glia.20232. View

13.

Hovelmeyer N, Hao Z, Kranidioti K, Kassiotis G, Buch T, Frommer F . Apoptosis of oligodendrocytes via Fas and TNF-R1 is a key event in the induction of experimental autoimmune encephalomyelitis. J Immunol. 2005; 175(9):5875-84. DOI: 10.4049/jimmunol.175.9.5875. View

14.

Kang Z, Altuntas C, Gulen M, Liu C, Giltiay N, Qin H . Astrocyte-restricted ablation of interleukin-17-induced Act1-mediated signaling ameliorates autoimmune encephalomyelitis. Immunity. 2010; 32(3):414-25. PMC: 3073618. DOI: 10.1016/j.immuni.2010.03.004. View

15.

Fyffe-Maricich S, Karlo J, Landreth G, Miller R . The ERK2 mitogen-activated protein kinase regulates the timing of oligodendrocyte differentiation. J Neurosci. 2011; 31(3):843-50. PMC: 3568938. DOI: 10.1523/JNEUROSCI.3239-10.2011. View

16.

Paintlia M, Paintlia A, Singh A, Singh I . Synergistic activity of interleukin-17 and tumor necrosis factor-α enhances oxidative stress-mediated oligodendrocyte apoptosis. J Neurochem. 2010; 116(4):508-21. PMC: 3033460. DOI: 10.1111/j.1471-4159.2010.07136.x. View

17.

Hofstetter H, Ibrahim S, Koczan D, Kruse N, Weishaupt A, Toyka K . Therapeutic efficacy of IL-17 neutralization in murine experimental autoimmune encephalomyelitis. Cell Immunol. 2006; 237(2):123-30. DOI: 10.1016/j.cellimm.2005.11.002. View

18.

Komiyama Y, Nakae S, Matsuki T, Nambu A, Ishigame H, Kakuta S . IL-17 plays an important role in the development of experimental autoimmune encephalomyelitis. J Immunol. 2006; 177(1):566-73. DOI: 10.4049/jimmunol.177.1.566. View

19.

Setzu A, Lathia J, Zhao C, Wells K, Rao M, ffrench-Constant C . Inflammation stimulates myelination by transplanted oligodendrocyte precursor cells. Glia. 2006; 54(4):297-303. DOI: 10.1002/glia.20371. View

20.

Cahoy J, Emery B, Kaushal A, Foo L, Zamanian J, Christopherson K . A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. J Neurosci. 2008; 28(1):264-78. PMC: 6671143. DOI: 10.1523/JNEUROSCI.4178-07.2008. View