Identification of endothelin 2 as an inflammatory factor that promotes central nervous system remyelination

Brain

Volumn 136, Issue 4, 2013, Pages 1035-1047

  Yuen, Tracy J ^a,b,c,e   Johnson, Kory R ^d   Miron, Veronique E ^a   Zhao, Chao ^b   Quandt, Jacqueline ^c,f   Harrisingh, Marie C ^a   Swire, Matthew ^a   Williams, Anna ^a   McFarland, Henry F ^c   Franklin, Robin J M ^b   Ffrench Constant, Charles ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

^d NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

endothelin; inflammation; multiple sclerosis; oligodendrocytes; regeneration; remyelination

Indexed keywords

CXCL13 CHEMOKINE; CXCL2 CHEMOKINE; ENDOTHELIN 2; ENDOTHELIN RECEPTOR; ENDOTHELIN RECEPTOR TYPE B; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; UNCLASSIFIED DRUG; ZYMOSAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOPSY; BRAIN SLICE; CELL LINEAGE; CONTROLLED STUDY; HUMAN; HUMAN TISSUE; IN VIVO STUDY; INNATE IMMUNITY; MACROPHAGE; MICROARRAY ANALYSIS; MULTIPLE SCLEROSIS; MYELIN SHEATH; MYELINATION; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; RAT; REGENERATION; REMYELINIZATION; RETINA; STEM CELL; UPREGULATION;

EID: 84876066645     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awt024     Document Type: Article

References (51)

1. Arai H, Hori S, Aramori I, Ohkubo H, Nakanishi S. Cloning and expression of a cDNA encoding an endothelin receptor. Nature 1990; 348: 730-2.
2. Aramori I, Nakanishi S. Coupling of two endothelin receptor subtypes to differing signal transduction in transfected Chinese hamster ovary cells. J Biol Chem 1992; 267: 12468-74.
3. Arnett HA, Mason J, Marino M, Suzuki K, Matsushima GK, Ting JP. TNF alpha promotes proliferation of oligodendrocyte progenitors and remyelination. Nat Neurosci 2001; 4: 1116-22.
4. Buttery PC, French-Constant C. Laminin-2/integrin interactions enhance myelin membrane formation by oligodendrocytes. Mol Cell Neurosci 1999; 14: 199-212.
5. Chan JR, Watkins TA, Cosgaya JM, Zhang C, Chen L, Reichardt LF, et al. NGF controls axonal receptivity to myelination by Schwann cells or oligodendrocytes. Neuron 2004; 43: 183-91.
6. Chari DM, Zhao C, Kotter MR, Blakemore WF, Franklin RJM. Corticosteroids delay remyelination of experimental demyelination in the rodent central nervous system. J Neurosci Res 2006; 83: 594-605.
7. Colello RJ, Devey LR, Imperato E, Pott U. The chronology of oligodendrocyte differentiation in the rat optic nerve: evidence for a signaling step initiating myelination in the CNS. J Neurosci 1995; 15: 7665-72.
8. Davenport AP. International Union of Pharmacology. XXIX. Update on endothelin receptor nomenclature. Pharmacol Rev 2002; 54: 219-26.
9. Ehrenreich H, Anderson RW, Fox CH, Rieckmann P, Hoffman GS, Travis WD, et al. Endothelins, peptides with potent vasoactive properties, are produced by human macrophages. J Exp Med 1990; 172: 1741-8.
10. Eisenbach M, Kartvelishvily E, Eshed-Eisenbach Y, Watkins T, Sorensen A, Thomson C, et al. Differential clustering of Caspr by oligodendrocytes and Schwann cells. J Neurosci Res 2009; 87: 3492-501.
11. Fancy SP, Harrington EP, Yuen TJ, Silbereis JC, Zhao C, Baranzini SE, et al. Axin2 as regulatory and therapeutic target in newborn brain injury and remyelination. Nat Neurosci 2011; 14: 1009-16.
12. Felts PA, Smith KJ. Blood-brain barrier permeability in astrocyte-free regions of the central nervous system remyelinated by Schwann cells. Neuroscience 1996; 75: 643-55.
13. Fyffe-Maricich SL, Karlo JC, Landreth GE, Miller RH. The ERK2 mitogen-activated protein kinase regulates the timing of oligodendrocyte differentiation. J Neurosci 2011; 31: 843-50.
14. Gadea A, Aguirre A, Haydar TF, Gallo V. Endothelin-1 regulates oligodendrocyte development. J Neurosci 2009; 29: 10047-62.
15. Gadea A, Schinelli S, Gallo V. Endothelin-1 regulates astrocyte proliferation and reactive gliosis via a JNK/c-Jun signaling pathway. J Neurosci 2008; 28: 2394-408.
16. Glezer I, Lapointe A, Rivest S. Innate immunity triggers oligodendrocyte progenitor reactivity and confines damages to brain injuries. FASEB J 2006; 20: 750-2.
17. Huang JK, Jarjour AA, Nait Oumesmar B, Kerninon C, Williams A, Krezel W, et al. Retinoid X receptor gamma signaling accelerates CNS remyelination. Nat Neurosci 2011; 14: 45-53.
18. Ihara M, Saeki T, Fukuroda T, Kimura S, Ozaki S, Patel AC, et al. A novel radioligand [125I]BQ-3020 selective for endothelin (ETB) receptors. Life Sci 1992; 51: PL47-52.
19. Ishikawa K, Ihara M, Noguchi K, Mase T, Mino N, Saeki T, et al. Biochemical and pharmacological profile of a potent and selective endothelin B-receptor antagonist, BQ-788. Proc Natl Acad Sci USA 1994; 91: 4892-6.
20. Jung KJ, Kim DW, Lee HN, Lee YS, Lee SJ, Che JH, et al. The role of endothelin receptor A during myelination of developing oligodendrocytes. J Korean Med Sci 2011; 26: 92-9.
21. Kawanabe Y, Nauli SM. Endothelin. Cell Mol Life Sci 2011; 68: 195-203.
22. Khodorova A, Richter J, Vasko MR, Strichartz G. Early and late contributions of glutamate and CGRP to mechanical sensitization by endothelin-1. J Pain 2009; 10: 740-9.
23. Kotter MR, Li WW, Zhao C, Franklin RJM. Myelin impairs CNS remyelination by inhibiting oligodendrocyte precursor cell differentiation. J Neurosci 2006; 26: 328-32.
24. Kotter MR, Setzu A, Sim FJ, Van Rooijen N, Franklin RJM. Macrophage depletion impairs oligodendrocyte remyelination following lysolecithininduced demyelination. Glia 2001; 35: 204-12.
25. Kotter MR, Zhao C, van Rooijen N, Franklin RJM. Macrophage-depletion induced impairment of experimental CNS remyelination is associated with a reduced oligodendrocyte progenitor cell response and altered growth factor expression. Neurobiol Dis 2005; 18: 166-75.
26. Koyama Y, Takemura M, Fujiki K, Ishikawa N, Shigenaga Y, Baba A. BQ788, an endothelin ET(B) receptor antagonist, attenuates stab wound injury-induced reactive astrocytes in rat brain. Glia 1999; 26: 268-71.
27. Laursen LS, Chan CW, French-Constant C. An integrin-contactin complex regulates CNS myelination by differential Fyn phosphorylation. J Neurosci 2009; 29: 9174-85.
28. Li WW, Setzu A, Zhao C, Franklin RJM. Minocycline-mediated inhibition of microglia activation impairs oligodendrocyte progenitor cell responses and remyelination in a non-immune model of demyelination. J Neuroimmunol 2005; 158: 58-66.
29. MacCumber MW, Ross CA, Snyder SH. Endothelin in brain: receptors, mitogenesis, and biosynthesis in glial cells. Proc Natl Acad Sci USA 1990; 87: 2359-63.
30. Mason JL, Suzuki K, Chaplin DD, Matsushima GK. Interleukin-1beta promotes repair of the CNS. J Neurosci 2001; 21: 7046-52.
31. McCarthy KD, de Vellis J. Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J Cell Biol 1980; 85: 890-902.
32. McKinnon RD, Waldron S, Kiel ME. PDGF alpha-receptor signal strength controls an RTK rheostat that integrates phosphoinositol 30-kinase and phospholipase Cgamma pathways during oligodendrocyte maturation. J Neurosci 2005; 25: 3499-508.
33. Miron VE, Ludwin SK, Darlington PJ, Jarjour AA, Soliven B, Kennedy TE, et al. Fingolimod (FTY720) enhances remyelination following demyelination of organotypic cerebellar slices. Am J Pathol 2010; 176: 2682-94.
34. Pomonis JD, Rogers SD, Peters CM, Ghilardi JR, Mantyh PW. Expression and localization of endothelin receptors: implications for the involvement of peripheral glia in nociception. J Neurosci 2001; 21: 999-1006.
35. Rogers SD, Peters CM, Pomonis JD, Hagiwara H, Ghilardi JR, Mantyh PW. Endothelin B receptors are expressed by astrocytes and regulate astrocyte hypertrophy in the normal and injured CNS. Glia 2003; 41: 180-90.
36. Rosano L, Cianfrocca R, Masi S, Spinella F, Di Castro V, Biroccio A, et al. Beta-arrestin links endothelin A receptor to beta-catenin signaling to induce ovarian cancer cell invasion and metastasis. Proc Natl Acad Sci USA 2009; 106: 2806-11.
37. Rosenberg SS, Kelland EE, Tokar E, De la Torre AR, Chan JR. The geometric and spatial constraints of the microenvironment induce oligodendrocyte differentiation. Proc Natl Acad Sci USA 2008; 105: 14662-7.
38. Ruckh JM, Zhao JW, Shadrach JL, van Wijngaarden P, Rao TN, Wagers AJ, et al. Rejuvenation and regeneration in the aging central nervous system. Cell Stem Cell 2012; 10: 96-103.
39. Said N, Smith S, Sanchez-Carbayo M, Theodorescu D. Tumor endothelin-1 enhances metastatic colonization of the lung in mouse xenograft models of bladder cancer. J Clin Invest 2011; 121: 132-47.
40. Sakurai T, Yanagisawa M, Takuwa Y, Miyazaki H, Kimura S, Goto K, et al. Cloning of a cDNA encoding a non-isopeptide-selective subtype of the endothelin receptor. Nature 1990; 348: 732-5.
41. Setzu A, ffrench-Constant C, Franklin RJM. CNS axons retain their competence for myelination throughout life. Glia 2004; 45: 307-11.
42. Setzu A, Lathia JD, Zhao C, Wells K, Rao MS, ffrench-Constant C, et al. Inflammation stimulates myelination by transplanted oligodendrocyte precursor cells. Glia 2006; 54: 297-303.
43. Shin T, Kang B, Tanuma N, Matsumoto Y, Wie M, Ahn M, et al. Intrathecal administration of endothelin-1 receptor antagonist ameliorates autoimmune encephalomyelitis in Lewis rats. Neuroreport 2001; 12: 1465-8.
44. Sim FJ, McClain CR, Schanz SJ, Protack TL, Windrem MS, Goldman SA. CD140a identifies a population of highly myelinogenic, migrationcompetent and efficiently engrafting human oligodendrocyte progenitor cells. Nat Biotechnol 2011; 29: 934-41.
45. Sim FJ, Zhao C, Penderis J, Franklin RJM. The age-related decrease in CNS remyelination efficiency is attributable to an impairment of both oligodendrocyte progenitor recruitment and differentiation. J Neurosci 2002; 22: 2451-9.
46. Wang Z, Colognato H, ffrench-Constant C. Contrasting effects of mitogenic growth factors on myelination in neuron-oligodendrocyte co-cultures. Glia 2007; 55: 537-45.
47. Woodruff RH, Franklin RJM. Demyelination and remyelination of the caudal cerebellar peduncle of adult rats following stereotaxic injections of lysolecithin, ethidium bromide, and complement/antigalactocerebroside: a comparative study. Glia 1999; 25: 216-28.
48. Yanagisawa M, Kurihara H, Kimura S, Tomobe Y, Kobayashi M, Mitsui Y, et al. A novel potent vasoconstrictor peptide produced by vascular endothelial cells. Nature 1988; 332: 411-5.
49. Yin Y, Cui Q, Gilbert HY, Yang Y, Yang Z, Berlinicke C, et al. Oncomodulin links inflammation to optic nerve regeneration. Proc Natl Acad Sci USA 2009; 106: 19587-92.
50. Yin Y, Henzl MT, Lorber B, Nakazawa T, Thomas TT, Jiang F, et al. Oncomodulin is a macrophage-derived signal for axon regeneration in retinal ganglion cells. Nat Neurosci 2006; 9: 843-52.
51. Zhang H, Jarjour AA, Boyd A, Williams A. Central nervous system remyelination in culture-a tool for multiple sclerosis research. Exp Neurol 2011; 230: 138-48.