Altered PLP1 splicing causes hypomyelination of early myelinating structures

Annals of Clinical and Translational Neurology

Volumn 2, Issue 6, 2015, Pages 648-661

  Kevelam, Sietske H ^a,b   Taube, Jennifer R ^c   van Spaendonk, Rosalina M L ^a   Bertini, Enrico ^d   Sperle, Karen ^c   Tarnopolsky, Mark ^e   Tonduti, Davide ^f   Valente, Enza Maria ^g,h   Travaglini, Lorena ^d   Sistermans, Erik A ^a   Bernard, Geneviève ⁱ   Catsman Berrevoets, Coriene E ^j   van Karnebeek, Clara D M ^k   Østergaard, John R ^l   Friederich, Richard L ^m   Fawzi Elsaid, Mahmoud ⁿ   Schieving, Jolanda H ^o   Tarailo Graovac, Maja ^k   Orcesi, Simona ^p   Steenweg, Marjan E ^a,b   van Berkel, Carola G M ^a   Waisfisz, Quinten ^a   Abbink, Truus E M ^a,b   van der Knaap, Marjo S ^a,b   Hobson, Grace M ^c,q,r   Wolf, Nicole I ^a,b   more..

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b VU UNIVERSITY AMSTERDAM   (Netherlands)

^c NEMOURS ALFRED I DUPONT HOSPITAL FOR CHILDREN   (United States)

^d BAMBINO GESÙ CHILDREN S HOSPITAL   (Italy)

^e MCMASTER CHILDREN S HOSPITAL   (Canada)

^f UNIVERSITY OF PAVIA   (Italy)

^g UNIVERSITY OF SALERNO   (Italy)

^h CASA SOLLIEVO DELLA SOFFERENZA HOSPITAL   (Italy)

ⁱ MONTREAL CHILDREN S HOSPITAL   (Canada)

^j SOPHIA CHILDREN S HOSPITAL   (Netherlands)

^k UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^l AARHUS UNIVERSITY HOSPITAL   (Denmark)

^m KAISER PERMANENTE   (United States)

ⁿ HAMAD MEDICAL CORPORATION   (Qatar)

^o RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^p C MONDINO NATIONAL NEUROLOGICAL INSTITUTE   (Italy)

^q UNIVERSITY OF DELAWARE   (United States)

^r THOMAS JEFFERSON UNIVERSITY   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CLINICAL ARTICLE; COMPUTER MODEL; EXOME; GENE; GENE DELETION; GENE MUTATION; GENE SEQUENCE; GENE SILENCING; GENETIC ANALYSIS; HUMAN; HYPOMYELINATION; MALE; MISSENSE MUTATION; MYELINATION; NUCLEAR MAGNETIC RESONANCE IMAGING; PLP1 GENE; PRIORITY JOURNAL; RNA SPLICING; X CHROMOSOME LINKED DISORDER;

EID: 84991209261     PISSN: None     EISSN: 23289503     Source Type: Journal    
DOI: 10.1002/acn3.203     Document Type: Article

References (53)

1. Steenweg ME, Wolf NI, Schieving JH, et al. Novel hypomyelinating leukoencephalopathy affecting early myelinating structures. Arch Neurol 2012;69:125-128.
2. Steenweg ME, Vanderver A, Blaser S, et al. Magnetic resonance imaging pattern recognition in hypomyelinating disorders. Brain 2010;133:2971-2982.
3. van der Knaap MS, Breiter SN, Naidu S, et al. Defining and categorizing leukoencephalopathies of unknown origin: MR imaging approach. Radiology 1999;213:121-133.
4. Pouwels PJ, Vanderver A, Bernard G, et al. Hypomyelinating leukodystrophies: translational research progress and prospects. Ann Neurol 2014;76:5-19.
5. van der Knaap MS, Valk J. Pelizaeus-Merzbacher disease and X-linked spastic paraplegia type 2. In Magnetic resonance of myelination and myelin disorders. 3rd ed. Berlin: Springer, 2005. p. 272-280.
6. Tonduti D, Pichiecchio A, Wolf NI, et al. Novel hypomyelinating leukoencephalopathy affecting early myelinating structures: clinical course in two brothers. Neuropediatrics 2013;44:213-217.
7. Woodward KJ. The molecular and cellular defects underlying Pelizaeus-Merzbacher disease. Expert Rev Mol Med 2008;10:e14.
8. Inoue K. PLP1-related inherited dysmyelinating disorders: Pelizaeus-Merzbacher disease and spastic paraplegia type 2. Neurogenetics 2005;6:1-16.
9. Hudson LD. Pelizaeus-Merzbacher disease and spastic paraplegia type 2: two faces of myelin loss from mutations in the same gene. J Child Neurol 2003;18:616-624.
10. Kevelam SH, Bugiani M, Salomons GS, et al. Exome sequencing reveals mutated SLC19A3 in patients with an early-infantile, lethal encephalopathy. Brain 2013;136:1534-1543.
11. Dallabona C, Diodato D, Kevelam SH, et al. Novel (ovario) leukodystrophy related to AARS2 mutations. Neurology 2014;82:2063-2071.
12. Taft RJ, Vanderver A, Leventer RJ, et al. Mutations in DARS cause hypomyelination with brain stem and spinal cord involvement and leg spasticity. Am J Hum Genet 2013;92:774-780.
13. Nave KA, Lai C, Bloom FE, et al. Splice site selection in the proteolipid protein (PLP) gene transcript and primary structure of the DM-20 protein of central nervous system myelin. Proc Natl Acad Sci USA 1987;84:5665-5669.
14. Wolf NI, Salomons GS, Rodenburg RJ, et al. Mutations in RARS cause hypomyelination. Ann Neurol 2014;76:134-139.
15. Ameziane N, Sie D, Dentro S, et al. Diagnosis of fanconi anemia: mutation analysis by next-generation sequencing. Anemia 2012;2012:132856.
16. Untergasser A, Cutcutache I, Koressaar T, et al. Primer3-new capabilities and interfaces. Nucleic Acids Res 2012;40:e115.
17. Koressaar T, Remm M. Enhancements and modifications of primer design program Primer3. Bioinformatics 2007;23:1289-1291.
18. Ng PC, Henikoff S. Predicting deleterious amino acid substitutions. Genome Res 2001;11:863-874.
19. Adzhubei I, Jordan DM, Sunyaev SR. Predicting functional effect of human missense mutations using PolyPhen-2. Curr Protoc Hum Genet 2013;Chapter 7:Unit7.20. doi: 10.1002/0471142905.hg0720s76:Unit7
20. Schwarz JM, Cooper DN, Schuelke M, et al. MutationTaster2: mutation prediction for the deep-sequencing age. Nat Methods 2014;11:361-362.
21. Wallis Y, Payne S, McAnulty C, et al. Practice guidelines for the evaluation of pathogenicity and the reporting of sequence variants in clinical molecular genetics. Available at: http://www.acgs.uk.com/media/774853/evaluation_and_reporting_of_sequence:variants_bpgs_june_2013_-_finalpdf.pdf. Accessed May, 2014.
22. Zuker M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 2003;31:3406-3415.
23. Taube JR, Sperle K, Banser L, et al. PMD patient mutations reveal a long-distance intronic interaction that regulates PLP1/DM20 alternative splicing. Hum Mol Genet 2014;23:5464-5478.
24. Hobson GM, Huang Z, Sperle K, et al. A PLP splicing abnormality is associated with an unusual presentation of PMD. Ann Neurol 2002;52:477-488.
25. Pratt VM, Dlouhy SR, Hodes ME. Possible cryptic splice site found in the PLP gene in a patient with Pelizaeus-Merzbacher disease. Am J Hum Genet 1991;49(suppl):393-451.
26. Eng LF, Chao FC, Gerstl B, et al. The maturation of human white matter myelin. Fractionation of the myelin membrane proteins. Biochemistry 1968;7:4455-4465.
27. Sistermans EA, de Coo RF, De Wijs IJ, et al. Duplication of the proteolipid protein gene is the major cause of Pelizaeus-Merzbacher disease. Neurology 1998;50:1749-1754.
28. Cailloux F, Gauthier-Barichard F, Mimault C, et al. Genotype-phenotype correlation in inherited brain myelination defects due to proteolipid protein gene mutations. Clinical European Network on Brain Dysmyelinating Disease. Eur J Hum Genet 2000;8:837-845.
29. Wolf NI, Sistermans EA, Cundall M, et al. Three or more copies of the proteolipid protein gene PLP1 cause severe Pelizaeus-Merzbacher disease. Brain 2005;128:743-751.
30. Shy ME, Hobson G, Jain M, et al. Schwann cell expression of PLP1 but not DM20 is necessary to prevent neuropathy. Ann Neurol 2003;53:354-365.
31. Osaka H, Kawanishi C, Inoue K, et al. Novel nonsense proteolipid protein gene mutation as a cause of X-linked spastic paraplegia in twin males. Biochem Biophys Res Commun 1995;215:835-841.
32. Hodes ME, Blank CA, Pratt VM, et al. Nonsense mutation in exon 3 of the proteolipid protein gene (PLP) in a family with an unusual form of Pelizaeus-Merzbacher disease. Am J Med Genet 1997;69:121-125.
33. Nance MA, Boyadjiev S, Pratt VM, et al. Adult-onset neurodegenerative disorder due to proteolipid protein gene mutation in the mother of a man with Pelizaeus-Merzbacher disease. Neurology 1996;47:1333-1335.
34. Laukka JJ, Stanley JA, Garbern JY, et al. Neuroradiologic correlates of clinical disability and progression in the X-linked leukodystrophy Pelizaeus-Merzbacher disease. J Neurol Sci 2013;335:75-81.
35. Saugier-Veber P, Munnich A, Bonneau D, et al. X-linked spastic paraplegia and Pelizaeus-Merzbacher disease are allelic disorders at the proteolipid protein locus. Nat Genet 1994;6:257-262.
36. Sivakumar K, Sambuughin N, Selenge B, et al. Novel exon 3B proteolipid protein gene mutation causing late-onset spastic paraplegia type 2 with variable penetrance in female family members. Ann Neurol 1999;45:680-683.
37. Gorman MP, Golomb MR, Walsh LE, et al. Steroid-responsive neurologic relapses in a child with a proteolipid protein-1 mutation. Neurology 2007;68:1305-1307.
38. Grossi S, Regis S, Biancheri R, et al. Molecular genetic analysis of the PLP1 gene in 38 families with PLP1-related disorders: identification and functional characterization of 11 novel PLP1 mutations. Orphanet J Rare Dis 2011;6:40-46.
39. Osaka H, Koizume S, Aoyama H, et al. Mild phenotype in Pelizaeus-Merzbacher disease caused by a PLP1-specific mutation. Brain Dev 2010;32:703-707.
40. Pratt VM, Trofatter JA, Larsen MB, et al. New variant in exon 3 of the proteolipid protein (PLP) gene in a family with Pelizaeus-Merzbacher disease. Am J Med Genet 1992;43:642-646.
41. Pretorius E, Naude H, Ribbens C, et al. Pelizaeus-Merzbacher disease: a developmental disorder affecting myelin formation in the nervous system. J Dev Phys Disabil 2005;17:173-183.
42. Hobson GM, Huang Z, Sperle K, et al. Splice-site contribution in alternative splicing of PLP1 and DM20: molecular studies in oligodendrocytes. Hum Mutat 2006;27:69-77.
43. Pratt VM, Naidu S, Dlouhy SR, et al. A novel mutation in exon 3 of the proteolipid protein gene in Pelizaeus-Merzbacher disease. Neurology 1995;45:394-395.
44. Lassuthova P, Zaliova M, Inoue K, et al. Three new PLP1 splicing mutations demonstrate pathogenic and phenotypic diversity of Pelizaeus-Merzbacher disease. J Child Neurol 2014;29:924-931.
45. Hobson GM, Davis AP, Stowell NC, et al. Mutations in noncoding regions of the proteolipid protein gene in Pelizaeus-Merzbacher disease. Neurology 2000;55:1089-1096.
46. Hubner CA, Orth U, Senning A, et al. Seventeen novel PLP1 mutations in patients with Pelizaeus-Merzbacher disease. Hum Mutat 2005;25:321-322.
47. Bridge PJ, Wilkens PJ. The role of proteolipid protein gene in Pelizaeus-Merzbacher disease. Am J Hum Genet 1992;51(suppl):A209.
48. Bonnet-Dupeyron MN, Combes P, Santander P, et al. PLP1 splicing abnormalities identified in Pelizaeus-Merzbacher disease and SPG2 fibroblasts are associated with different types of mutations. Hum Mutat 2008;29:1028-1036.
49. Wang E, Huang Z, Hobson GM, et al. PLP1 alternative splicing in differentiating oligodendrocytes: characterization of an exonic splicing enhancer. J Cell Biochem 2006;97:999-1016.
50. Wang E, Dimova N, Cambi F. PLP/DM20 ratio is regulated by hnRNPH and F and a novel G-rich enhancer in oligodendrocytes. Nucleic Acids Res 2007;35:4164-4178.
51. Warf MB, Berglund JA. Role of RNA structure in regulating pre-mRNA splicing. Trends Biochem Sci 2010;35:169-178.
52. Regis S, Corsolini F, Grossi S, et al. Restoration of the normal splicing pattern of the PLP1 gene by means of an antisense oligonucleotide directed against an exonic mutation. PLoS One 2013;8:e73633.
53. van der Knaap MS, Valk J. Myelination and retarded myelination. In: Magnetic resonance of myelination and myelin disorders. 3rd ed. Berlin: Springer, 2005. p. 37-65.