Astrocytes are central in the pathomechanisms of vanishing white matter

Journal of Clinical Investigation

Volumn 126, Issue 4, 2016, Pages 1512-1524

  Dooves, Stephanie ^a   Bugiani, Marianna ^a   Postma, Nienke L ^a   Polder, Emiel ^a   Land, Niels ^a   Horan, Stephen T ^a   Van Deijk, Anne Lieke F ^b   Van De Kreeke, Aleid ^a   Jacobs, Gerbren ^a   Vuong, Caroline ^a   Klooster, Jan ^c   Kamermans, Maarten ^c   Wortel, Joke ^b   Loos, Maarten ^d   Wisse, Lisanne E ^a   Scheper, Gert C ^a   Abbink, Truus E M ^a   Heine, Vivi M ^a,b   Van Der Knaap, Marjo S ^a,b  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b VU UNIVERSITY AMSTERDAM   (Netherlands)

^c NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

^d Sylics (Synaptologics BV)   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

GUANINE NUCLEOTIDE EXCHANGE FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; CELL MATURATION; CONTROLLED STUDY; DISEASE COURSE; DISEASE SEVERITY; GENOTYPE; HUMAN; HUMAN TISSUE; LEUKODYSTROPHY; MALE; MOUSE; MUELLER CELL; NONHUMAN; OLIGODENDROGLIA; PHENOTYPE; PRIORITY JOURNAL; VANISHING WHITE MATTER; WHITE MATTER; ANIMAL; CELL CULTURE; COCULTURE; DISEASE MODEL; GENETICS; LEUKOENCEPHALOPATHY; METABOLISM; MUTANT MOUSE STRAIN; PATHOLOGY; PATHOPHYSIOLOGY;

ANIMALS; ASTROCYTES; CELLS, CULTURED; COCULTURE TECHNIQUES; DISEASE MODELS, ANIMAL; EUKARYOTIC INITIATION FACTOR-2B; HUMANS; LEUKOENCEPHALOPATHIES; MICE; MICE, MUTANT STRAINS; OLIGODENDROGLIA; WHITE MATTER;

EID: 84964692080     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI83908     Document Type: Article

References (60)

1. van der Knaap MS, Pronk JC, Scheper GC. Vanishing white matter disease. Lancet Neurol. 2006;5(5):413-423.
2. Leegwater PA, et al. Subunits of the translation initiation factor eIF2B are mutant in leukoencephalopathy with vanishing white matter. Nat Genet. 2001;29(4):383-388.
3. van der Knaap MS, et al. Mutations in each of the five subunits of translation initiation factor eIF2B can cause leukoencephalopathy with vanishing white matter. Ann Neurol. 2002;51(2):264-270.
4. Labauge P, et al. Natural history of adult-onset eIF2B-related disorders: A multi-centric survey of 16 cases. Brain. 2009;132(pt 8):2161-2169.
5. van der Lei HDW, et al. Genotype-phenotype correlation in vanishing white matter disease. Neurology. 2010;75(17):1555-1559.
6. Fogli A, et al. The effect of genotype on the natural history of eIF2B-related leukodystrophies. Neurology. 2004;62(9):1509-1517.
7. van der Knaap MS, et al. eIF2B-related disorders: antenatal onset and involvement of multiple organs. Am J Hum Genet. 2003;73(5):1199-1207.
8. Scheper GC, Proud CG, van der Knaap MS. Defective translation initiation causes vanishing of cerebral white matter. Trends Mol Med. 2006;12(4):159-166.
9. Liu R, et al. Severity of Vanishing White Matter disease does not correlate with deficits in eIF2B activity or the integrity of eIF2B complexes. Hum Mutat. 2011;32(9):1036-1045.
10. Li W, Wang XM, van der Knaap MS, Proud CG. Mutations linked to leukoencephalopathy with vanishing white matter impair the function of the eukaryotic initiation factor 2B complex in diverse ways. Mol Cell Biol. 2004;24(8):3295-3306.
11. Richardson JP, Mohammad SS, Pavitt GD. Mutations causing childhood ataxia with central nervous system hypomyelination reduce eukaryotic initiation factor 2B complex formation and activity. Mol Cell Biol. 2004;24(6):2352-2363.
12. Horzinski L, et al. Eukaryotic initiation factor 2B (eIF2B) GEF activity as a diagnostic tool for EIF2B-related disorders. PLoS One. 2009;4(12):e8318.
13. van Kollenburg B, et al. egulation of protein synthesis in lymphoblasts from vanishing white matter patients. Neurobiol Dis. 2006;21(3):496-504.
14. Kantor L, et al. Heightened stress response in primary fibroblasts expressing mutant eIF2B genes from CACH/VWM leukodystrophy patients. Hum Genet. 2005;118(1):99-106.
15. Fogli A, et al. Decreased guanine nucleotide exchange factor activity in eIF2B-mutated patients. Eur J Hum Genet. 2004;12(7):561-566.
16. Bugiani M, Boor I, Powers JM, Scheper GC, van der Knaap MS. Leukoencephalopathy with Vanishing White Matter: A review. J Neuropathol Exp Neurol. 2010;69(10):987-996.
17. Wong K, et al. Foamy cells with oligodendroglial phenotype in childhood ataxia with diffuse central nervous system hypomyelination syndrome. Acta Neuropathol. 2000;100(6):635-646.
18. Dietrich J, et al. EIF2B5 mutations compromise GFAP(+) astrocyte generation in vanishing white matter leukodystrophy. Nat Med. 2005;11(3):277-283.
19. Rodriguez D, et al. Increased density of oligodendrocytes in childhood ataxia with diffuse central hypomyelination (CACH) syndrome: neuropathological and biochemical study of two cases. Acta Neuropathol. 1999;97(5):469-480.
20. Bugiani M, et al. Defective glial maturation in Vanishing White Matter disease. J Neuropathol Exp Neurol. 2011;70(1):69-82.
21. Bugiani M, et al. Hyaluronan accumulation and arrested oligodendrocyte progenitor maturation in vanishing white matter disease. Brain. 2013;136(pt 1):209-222.
22. Back SA, et al. Hyaluronan accumulates in demyelinated lesions and inhibits oligodendrocyte progenitor maturation. Nat Med. 2005;11(9):966-972.
23. Fogli A, et al. Cree leukoencephalopathy and CACH/VWM disease are allelic at the EIF2B5 locus. Ann Neurol. 2002;52(4):506-510.
24. Sofroniew MV. Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci. 2009;32(12):638-647.
25. Jennings MD, Zhou Y, Mohammad-Qureshi SS, Bennett D, Pavitt GD. eIF2B promotes eIF5 dissociation from eIF2 center dot GDP to facilitate guanine nucleotide exchange for translation initiation. Genes Dev. 2013;27(24):2696-2707.
26. Marom L, Ulitsky I, Cabilly Y, Shamir R, Elroy-Stein O. A point mutation in translation initiation factor eIF2B leads to function-and time-specific changes in brain gene expression. PLoS One. 2011;6(10):e26992.
27. van der Knaap MS, Kamphorst M, Barth PG, Kraaijeveld CL, Gut E, Valk J. Phenotypic variation in leukoencephalopathy with vanishing white matter. Neurology. 1998;51(2):540-547.
28. Hata Y, et al. An autopsy case of infantile-onset vanishing white matter disease related to an EIF2B2 mutation (V85E) in a hemizygous region. Int J Clin Exp Pathol. 2014;7(6):3355-3362.
29. Depienne C, et al. Brain white matter oedema due to ClC-2 chloride channel deficiency: an observational analytical study. Lancet Neurol. 2013;12(7):659-668.
30. Geva M, et al. A mouse model for eukaryotic translation initiation factor 2B-leucodystrophy reveals abnormal development of brain white matter. Brain. 2010;133(pt 8):2448-2461.
31. Bjartmar C, Yin XH, Trapp BD. Axonal pathology in myelin disorders. J Neurocytol. 1999;28(4-5):383-395.
32. Robain O. The jimpy mouse. Acta Zool Pathol Antverp. 1977;68(68):68-92.
33. Rosenfeld J, Freidrich VL. Axonal swellings in jimpy mice - does lack of myelin cause neuronal abnormalities. Neuroscience. 1983;10(3):959-966.
34. Kamphuis W, et al. GFAP isoforms in adult mouse brain with a focus on neurogenic astrocytes and reactive astrogliosis in mouse models of Alzheimer disease. PLoS One. 2012;7(8):e42823.
35. Middeldorp J, Hol EM. GFAP in health and disease. Prog Neurobiol. 2011;93(3):421-443.
36. Mamber C, Kamphuis W, Haring NL, Peprah N, Middeldorp J, Hol EM. GFAPΔ expression in glia of the developmental and adolescent mouse brain. PLoS One. 2012;7(12):e52659.
37. Huyghe A, et al. Developmental splicing deregulation in leukodystrophies related to EIF2B mutations. PLoS One. 2012;7(6):e38264.
38. Xu HW, et al. Bergmann glia function in granule cell migration during cerebellum development. Mol Neurobiol. 2013;47(2):833-844.
39. Metea MR, Newman EA. Calcium signaling in specialized glial cells. Glia. 2006;54(7):650-655.
40. Eckstein AK, Reichenbach A, Jacobi P, Weber P, Gregor M, Zrenner E. Hepatic retinopathia. Changes in retinal function. Vision Res. 1997;37(12):1699-1706.
41. Hammond TR, et al. Astrocyte-derived endothelin-1 inhibits remyelination through notch activation. Neuron. 2014;81(3):588-602.
42. Wang YP, et al. Astrocytes from the contused spinal cord inhibit oligodendrocyte differentiation of adult oligodendrocyte precursor cells by increasing the expression of bone morphogenetic proteins. J Neurosci. 2011;31(16):6053-6058.
43. Arai K, Lo EH. Astrocytes protect oligodendrocyte precursor cells via MEK/ERK and PI3K/Akt signaling. J Neurosci Res. 2010;88(4):758-763.
44. Chernoff GF. Shiverer - an autosomal recessive mutant mouse with myelin deficiency. J Hered. 1981;72(2):128.
45. Lu JF, et al. A mouse model for X-linked adrenoleukodystrophy. Proc Natl Acad Sci U S A. 1997;94(17):9366-9371.
46. Hess B, et al. Phenotype of arylsulfatase Adeficient mice: Relationship to human metachromatic leukodystrophy. Proc Natl Acad Sci U S A. 1996;93(25):14821-14826.
47. Behrendt R, Roers A. Mouse models for Aicardi-Goutieres syndrome provide clues to the molecular pathogenesis of systemic autoimmunity. Clin Exp Immunol. 2014;175(1):9-16.
48. Hagemann TL, Connor JX, Messing A. Alexander disease-associated glial fibrillary acidic protein mutations in mice induce rosenthal fiber formation and a white matter stress response. J Neurosci. 2006;26(43):11162-11173.
49. Verheijden S, et al. Peroxisomal multifunctional protein-2 deficiency causes neuroinflammation and degeneration of Purkinje cells independent of very long chain fatty acid accumulation. Neurobiol Dis. 2013;58:258-269.
50. Ramakrishnan H, et al. Increasing sulfatide synthesis in myelin-forming cells of arylsulfatase A-deficient mice causes demyelination and neurological symptoms reminiscent of human metachromatic leukodystrophy. J Neurosci. 2007;27(35):9482-9490.
51. Messing A, Head MW, Galles K, Galbreath EJ, Goldman JE, Brenner M. Fatal encephalopathy with astrocyte inclusions in GFAP transgenic mice. Am J Pathol. 1998;152(2):391-398.
52. Lin Y, et al. Impaired eukaryotic translation initiation factor 2B activity specifically in oligodendrocytes reproduces the pathology of vanishing white matter disease in mice. J Neurosci. 2014;34(36):12182-12191.
53. Cabilly Y, et al. Poor cerebral inflammatory response in eIF2B knock-in mice: implications for the aetiology of vanishing white matter disease. Plos One. 2012;7(10):e46715.
54. Dever TE. Gene-specific regulation by general translation factors. Cell. 2002;108(4):545-556.
55. Turon-Vinas E, et al. Vanishing white matter disease in a spanish population. J Cent Nerv Syst Dis. 2014;6:59-68.
56. Oberheim NA, Goldman SA, Nedergaard M. Heterogeneity of astrocytic form and function. Methods Mol Biol. 2012;814:23-45.
57. Matyash V, Kettenmann H. Heterogeneity in astrocyte morphology and physiology. Brain Res Rev. 2010;63(1-2):2-10.
58. Loos M, et al. Sheltering behavior and locomotor activity in 11 genetically diverse common inbred mouse strains using home-cage monitoring. PLoS One. 2014;9(9):e108563.
59. Sim FJ, McClain CR, Schanz SJ, Protack TL, Windrem MS, Goldman SA. CD140a identifies a population of highly myelinogenic, migration-competent and efficiently engrafting human oligodendrocyte progenitor cells. Nat Biotechnol. 2011;29(10):934-941.
60. Heine VM, Rowitch DH. Hedgehog signaling has a protective effect in glucocorticoid-induced mouse neonatal brain injury through an 11 beta HSD2-dependent mechanism. J Clin Invest. 2009;119(2):267-277.