Pooled analysis of patients with inherited prion disease caused by two- to twelve-octapeptide repeat insertions in the prion protein gene (PRNP).
Creutzfeldt–Jakob disease
Genetics
Gerstmann–Sträussler–Scheinker syndrome
Octapeptide repeat insertion
Prion disease
Journal
Journal of neurology
ISSN: 1432-1459
Titre abrégé: J Neurol
Pays: Germany
ID NLM: 0423161
Informations de publication
Date de publication:
09 Sep 2023
09 Sep 2023
Historique:
received:
19
07
2023
accepted:
24
08
2023
revised:
21
08
2023
medline:
10
9
2023
pubmed:
10
9
2023
entrez:
9
9
2023
Statut:
aheadofprint
Résumé
Inherited prion diseases caused by two- to twelve-octapeptide repeat insertions (OPRIs) in the prion protein gene (PRNP) show significant clinical heterogeneity. This study describes a family with two new cases with a 4-OPRI mutation and two asymptomatic mutation carriers. The pooled analysis summarizes all cases reported in the literature to date and describes the relation between survival, age of onset, number of OPRI and codon 129 polymorphism. MEDLINE and Google Scholar were queried from database inception up to December 31, 2022. Age of onset was compared per number of OPRI and per codon 129 polymorphism using the Kruskal-Wallis and Wilcoxon-Mann-Whitney tests, respectively. Disease duration was modeled non-parametrically by a Kaplan-Meier model and semi-parametrically by a Cox model. This study comprised 164 patients. Lower number of OPRI and presence of valine (cis-V) versus methionine (cis-M) on codon 129 were associated with an older age of onset (P < 0.001 and P = 0.025, respectively) and shorter disease duration (P < 0.001 and P = 0.003, respectively). Within patients with 5- or more OPRI codon cis-V remained significantly associated with a shorter disease duration. Codon 129 homozygosity versus heterozygosity was not significantly associated with age of onset or disease duration (P = 0.076 and P = 0.409, respectively). This study summarized the largest cohort of patients with two- to twelve-OPRI to date. Lower number of OPRI and codon 129 cis-V is associated with an older age of onset and shorter disease duration, while homozygosity or heterozygosity on codon 129 was not.
Identifiants
pubmed: 37689591
doi: 10.1007/s00415-023-11968-9
pii: 10.1007/s00415-023-11968-9
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Fonds Wetenschappelijk Onderzoek
ID : 3G0H8318
Organisme : Bijzonder Onderzoeksfonds UGent
ID : 01N10319
Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany.
Références
Takada LT, Kim MO, Cleveland RW, Wong K, Forner SA, Gala II (2017) Genetic prion disease: experience of a rapidly progressive dementia center in the United States and a review of the literature. Am J Med Genet B Neuropsychiatr Genet. 174(1):36–69
pubmed: 27943639
pmcid: 7207989
doi: 10.1002/ajmg.b.32505
Mead S (2006) Inherited prion disease with six octapeptide repeat insertional mutation–molecular analysis of phenotypic heterogeneity. Brain. 129(9):2297–317
pubmed: 16923955
doi: 10.1093/brain/awl226
Areškevičiūtė A, Høgh P, Bartoletti-Stella A, Melchior LC, Nielsen PR, Parchi P (2019) A novel eight octapeptide repeat insertion in PRNP causing prion disease in a Danish family. j neuropathol exp neurol. 78(7):595–604
pubmed: 31107536
doi: 10.1093/jnen/nlz037
Chen Z, Nan H, Kong Y, Chu M, Liu L, Zhang J (2022) Amino acid substitution within seven-octapeptide repeat insertions in the prion protein gene associated with short-term course. Viruses. 14(10):2245
pubmed: 36298800
pmcid: 9609758
doi: 10.3390/v14102245
Yu SL, Jin L, Sy MS, Mei FH, Kang SL, Sun GH (2004) Polymorphisms of the PRNP gene in Chinese populations and the identification of a novel insertion mutation. Eur J Hum Genet. 12(10):867–70
pubmed: 15266305
doi: 10.1038/sj.ejhg.5201245
Rossi G, Giaccone G, Giampaolo L, Iussich S, Puoti G, Frigo M (2000) Creutzfeldt-Jakob disease with a novel four extra-repeat insertional mutation in the PrP gene. Neurology. 55(3):405–10
pubmed: 10932276
doi: 10.1212/WNL.55.3.405
Martinez-Saez E, Gelpi E, Rey MJ, Ferrer I, Ribalta T, Botta-Orfila T (2012) Hirano body-rich subtypes of Creutzfeldt-Jakob disease. Neuropathol Appl Neurobiol. 38(2):153–61
pubmed: 21726270
doi: 10.1111/j.1365-2990.2011.01208.x
Clift K, Guthrie K, Klee EW, Boczek N, Cousin M, Blackburn P (2016) Familial Creutzfeldt-Jakob disease: case report and role of genetic counseling in post mortem testing. Prion. 10(6):502–6
pubmed: 27929804
pmcid: 5161295
doi: 10.1080/19336896.2016.1254858
Kovács GG, Puopolo M, Ladogana A, Pocchiari M, Budka H, van Duijn C (2005) Genetic prion disease: the EUROCJD experience. Hum Genet. 118(2):166–74
pubmed: 16187142
doi: 10.1007/s00439-005-0020-1
Mead S, Uphill J, Beck J, Poulter M, Campbell T, Lowe J (2012) Genome-wide association study in multiple human prion diseases suggests genetic risk factors additional to PRNP. Hum Mol Genet. 21(8):1897–906
pubmed: 22210626
doi: 10.1093/hmg/ddr607
Capellari S, Strammiello R, Saverioni D, Kretzschmar H, Parchi P (2011) Genetic Creutzfeldt-Jakob disease and fatal familial insomnia: insights into phenotypic variability and disease pathogenesis. Acta Neuropathol (Berl). 121(1):21–37
pubmed: 20978903
doi: 10.1007/s00401-010-0760-4
McVean GA, Altshuler DM, Durbin RM, Abecasis GR, Bentley DR, Chakravarti A (2012) An integrated map of genetic variation from 1092 human genomes. Nature. 491(7422):56–65
pubmed: 23128226
doi: 10.1038/nature11632
R Core Team. R: A Language and Environment for Statistical Computing. Vienna, Austria; 2016. Available from: https://www.R-project.org/ . Accessed on 1 Mar 2023
Capellari S, Vital C, Parchi P, Petersen RB, Ferrer X, Jarnier D (1997) Familial prion disease with a novel 144-bp insertion in the prion protein gene in a Basque family. Neurology. 49(1):133–41
pubmed: 9222181
doi: 10.1212/WNL.49.1.133
Laplanche LJ, Tre NDL, Brandel PJ, Dussaucy M, Chatelain J, Launay JM (1995) Two novel insertions in the prion protein gene in patients with lateonset dementia. Hum Mol Genet. 4(6):1109–11
pubmed: 7655470
doi: 10.1093/hmg/4.6.1109
Brennecke N, Cali I, Mok TH, Speedy H, Hosszu LLP, Genomics England Research Consortium (2021) characterization of prion disease associated with a two-octapeptide repeat insertion. Viruses. 13(9):1794
pubmed: 34578375
pmcid: 8473248
doi: 10.3390/v13091794
Goldfarb LG, Brown P, Little BW, Cervenáková L, Kenney K, Gibbs CJ (1993) A new (two-repeat) octapeptide coding insert mutation in Creutzfeldt-Jakob disease. Neurology. 43(11):2392–2392
pubmed: 8232966
doi: 10.1212/WNL.43.11.2392
Croes EA, Theuns J, Houwing-Duistermaat JJ, Dermaut B, Sleegers K, Roks G (2004) Octapeptide repeat insertions in the prion protein gene and early onset dementia. J Neurol Neurosurg Psychiatry. 75(8):1166–70
pubmed: 15258222
pmcid: 1739180
doi: 10.1136/jnnp.2003.020198
van Harten B, van Gool WA, van Langen IM, Deekman JM, Meijerink PHS, Weinstein HC (2000) A new mutation in the prion protein gene: a patient with dementia and white matter changes. Neurology. 55(7):1055–7
pubmed: 11061272
doi: 10.1212/WNL.55.7.1055
Grasbon-Frodl E, Schmalzbauer R, Weber P, Krebs B, Windl O, Zerr I (2004) A novel three extra-repeat insertion in the prion protein gene (PRNP) in a patient with Creutzfeldt-Jakob disease. Neurogenetics. 5(4):249–50
pubmed: 15480878
doi: 10.1007/s10048-004-0196-x
Nishida Y, Sodeyama N, Toru Y, Toru S, Kitamoto T, Mizusawa H (2004) Creutzfeldt-Jakob disease with a novel insertion and codon 219 Lys/Lys polymorphism in PRNP. Neurology. 63(10):1978–9
pubmed: 15557533
doi: 10.1212/01.WNL.0000144196.43430.E1
Kaski DN, Pennington C, Beck J, Poulter M, Uphill J, Bishop MT (2011) Inherited prion disease with 4-octapeptide repeat insertion: disease requires the interaction of multiple genetic risk factors. Brain. 134(6):1829–38
pubmed: 21616973
doi: 10.1093/brain/awr079
Campbell TA, Palmer MS, Will RG, Gibb WRG, Luthert PJ, Collinge J (1996) A prion disease with a novel 96-base pair insertional mutation in the prion protein gene. Neurology. 46(3):761–6
pubmed: 8618679
doi: 10.1212/WNL.46.3.761
Yanagihara C, Yasuda M, Maeda K, Miyoshi K, Nishimura Y (2002) Rapidly progressive dementia syndrome associated with a novel four extra repeat mutation in the prion protein gene. J Neurol Neurosurg Psychiatry. 72(6):788–91
pubmed: 12023426
pmcid: 1737919
doi: 10.1136/jnnp.72.6.788
Goldfarb LG, Brown P, McCombie WR, Goldgaber D, Swergold GD, Wills PR (1991) Transmissible familial Creutzfeldt-Jakob disease associated with five, seven, and eight extra octapeptide coding repeats in the PRNP gene. Proc Natl Acad Sci. 88(23):10926–30
pubmed: 1683708
pmcid: 53045
doi: 10.1073/pnas.88.23.10926
Depaz R, Haik S, Peoc’h K, Seilhean D, Grabli D, Vicart S (2012) Long-standing prion dementia manifesting as posterior cortical atrophy. Alzheimer Dis Assoc Disord. 26(3):289
pubmed: 21959360
doi: 10.1097/WAD.0b013e318231e449
Cochran EJ, Bennett DA, Cervenakova L, Kenney K, Bernard B, Foster NL (1996) Familial Creutzfeldt-Jakob disease with a five-repeat octapeptide insert mutation. Neurology. 47(3):727–33
pubmed: 8797471
doi: 10.1212/WNL.47.3.727
Skworc KH, Windl O, Schulz-Schaeffer WJ, Giese A, Bergk J, Nägele A (1999) Familial Creutzfeldt-Jakob disease with a novel 120-bp insertion in the prion protein gene. Ann Neurol. 46(5):693–700
pubmed: 10553985
doi: 10.1002/1531-8249(199911)46:5<693::AID-ANA3>3.0.CO;2-Z
Beck G, Kawano T, Naba I, Nishimura T, Sawada J, Hazama T (2005) A case with a 120 base pair insertional mutation in the prion protein gene: the first case in Japan. J Neurol Neurosurg Psychiatry. 76(5):756–7
pubmed: 15834045
pmcid: 1739617
doi: 10.1136/jnnp.2004.048553
Mead S, Webb TEF, Campbell TA, Beck J, Linehan JM, Rutherfoord S (2007) Inherited prion disease with 5-OPRI: phenotype modification by repeat length and codon 129. Neurology. 69(8):730–8
pubmed: 17709704
doi: 10.1212/01.wnl.0000267642.41594.9d
Jansen C, van Swieten JC, Capellari S, Strammiello R, Parchi P, Rozemuller AJM (2009) Inherited Creutzfeldt-Jakob disease in a Dutch patient with a novel five octapeptide repeat insertion and unusual cerebellar morphology. J Neurol Neurosurg Psychiatry. 80(12):1386–9
pubmed: 19917818
doi: 10.1136/jnnp.2008.169359
McKnight K, Herron B, Turkington J, Haffey S, Mead S, McMonagle P (2013) Inherited prion disease due to 5-octapeptide repeat insertion. J Neurol Sci. 333:e334-5
doi: 10.1016/j.jns.2013.07.1239
Nicholl D, Windl O, de Silva R, Sawcer S, Dempster M, Ironside JW (1995) Inherited Creutzfeldt-Jakob disease in a British family associated with a novel 144 base pair insertion of the prion protein gene. J Neurol Neurosurg Psychiatry. 58(1):65–9
pubmed: 7823070
pmcid: 1073270
doi: 10.1136/jnnp.58.1.65
Oda T, Kitamoto T, Tateishi J, Mitsuhashi T, Iwabuchi K, Haga C (1995) Prion disease with 144 base pair insertion in a Japanese family line. Acta Neuropathol (Berl). 90(1):80–6
pubmed: 7572084
doi: 10.1007/BF00294463
Vital C, Gray F, Vital A, Parchi P, Capellari S, Petersen RB (1998) Prion encephalopathy with insertion of octapeptide repeats: the number of repeats determines the type of cerebellar deposits. Neuropathol Appl Neurobiol. 24(2):125–30
pubmed: 9634208
doi: 10.1046/j.1365-2990.1998.00098.x
Gelpi E, Kovacs GG, Ströbel T, Koperek O, Voigtländer T, Liberski PP (2005) Prion disease with a 144 base pair insertion: unusual cerebellar prion protein immunoreactivity. Acta Neuropathol (Berl). 110(5):513–9
pubmed: 16155763
doi: 10.1007/s00401-005-1073-x
Doughty C, Lyons J. A Case of Familial Prion Disease Caused by a Six-Octapeptide Repeat Insertion Mutation (P5.185). Neurology [Internet]. 5 april 2016 [geciteerd 14 maart 2023];86(16 Supplement). Beschikbaar op: https://n.neurology.org/content/86/16_Supplement/P5.185 . Accessed 1 Feb 2023
Tateishi J (1991) Recent advances in the research of Creutzfeldt-Jakob disease (CJD) and Gerstmann-Strüssler syndrome (GSS). Rinsho Shinkeigaku. 31(12):1306–8
pubmed: 1687809
Dermaut B, Cruts M, Backhovens H, Lübcke U, Van Everbroeck B, Sciot R (2000) Familial Creutzfeldt-Jakob disease in a patient carrying both a presenilin 1 missense substitution and a prion protein gene insertion. J Neurol. 247(5):364–8
pubmed: 10896268
doi: 10.1007/s004150050603
Lewis V, Collins S, Hill AF, Boyd A, McLean CA, Smith M (2003) Novel prion protein insert mutation associated with prolonged neurodegenerative illness. Neurology. 60(10):1620–4
pubmed: 12771252
doi: 10.1212/01.WNL.0000065887.14609.0E
Cannella M, Martino T, Simonelli M, Ciammola A, Gradini R, Ciarmiello A (2009) De novo seven extra repeat expanded mutation in the PRNP gene in an Italian patient with early onset dementia. Case Rep. 2009:bcr0820080711
King A, Doey L, Rossor M, Mead S, Collinge J, Lantos P (2003) Phenotypic variability in the brains of a family with a prion disease characterized by a 144-base pair insertion in the prion protein gene. Neuropathol Appl Neurobiol 29(2):98–105
pubmed: 12662318
doi: 10.1046/j.1365-2990.2003.00423.x
Collinge J, Brown J, Hardy J, Mullan M, Rossor MN, Baker H (1992) Inherited prion disease with 144 base pair gene insertion: 2. Clinical and pathological features. Brain. 115(3):687–710
pubmed: 1352725
doi: 10.1093/brain/115.3.687
Brown P, Goldfarb LG, McCombie WR, Nieto A, Squillacote D, Sheremata W (1992) Atypical Creutzfeldt-Jakob disease in an American family with an insert mutation in the PRNP amyloid precursor gene. Neurology. 42(2):422–422
pubmed: 1736177
doi: 10.1212/WNL.42.2.422
van Gool WA, Hensels GW, Hoogerwaard EM, Wiezer JHA, Wesseling P, Bolhuis PA (1995) Hypokinesia and presenile dementia in a Dutch family with a novel insertion in the prion protein gene. Brain. 118(6):1565–71
pubmed: 8595485
doi: 10.1093/brain/118.6.1565
Paucar M, Xiang F, Moore R, Walker RH, Winnberg E, Svenningsson S (2013) Genotype-phenotype analysis in inherited prion disease with eight octapeptide repeat insertional mutation. Landes Biosci december 7(6):501–510
Owen F, Poulter M, Collinge J, Leach M, Lofthouse R, Crow TJ (1992) A dementing illness associated with a novel insertion in the prion protein gene. Mol Brain Res. 13(1):155–7
pubmed: 1349721
doi: 10.1016/0169-328X(92)90056-H
Duchen LW, Poulter M, Harding AE (1993) Dementia associated with a 216 base pair insertion in the prion protein gene: clinical and neuropathological features. Brain. 116(3):555–67
pubmed: 8513392
doi: 10.1093/brain/116.3.555
Krasemann S, Zerr I, Weber T, Poser S, Kretzschmar H, Hunsmann G (1995) Prion disease associated with a novel nine octapeptide repeat insertion in the PRNP gene. Mol Brain Res. 34(1):173–6
pubmed: 8750875
doi: 10.1016/0169-328X(95)00175-R
Ritter A, Reed MU, Campbell T, Gentle P, Wint D (2021) Early onset dementia with early and prominent behavioral features due to prion disease associated with nine octapeptide repeat insertion in the PRNP gene. Journal neuropsychiatry clinical neuroscience. AMER Psychiatric Publishing Inc, Washington, pp 253–253
Townley RA, Polsinelli AJ, Fields JA, Machulda MM, Jones DT, Graff-Radford J (2020) Longitudinal clinical, neuropsychological, and neuroimaging characterization of a kindred with a 12-octapeptide repeat insertion in PRNP: the next generation. Neurocase. 26(4):211–9
pubmed: 32602775
pmcid: 7426006
doi: 10.1080/13554794.2020.1787458
Kumar N, Boeve BF, Boot BP, Orr CF, Duffy J, Woodruff BK (2011) Clinical characterization of a kindred with a novel 12-octapeptide repeat insertion in the prion protein gene. Arch Neurol. 68(9):1165–70
pubmed: 21911696
pmcid: 3326586
doi: 10.1001/archneurol.2011.187
Sánchez-Valle R, Yagüe J, Turón A, Aróstegui JI, Nos C, Rey M (2012) Inherited prion disease with 4-octapeptide repeat insertion linked to valine at codon 129. Brain. 135(4):e212
pubmed: 22300874
doi: 10.1093/brain/awr358
Sánchez-Valle R, Aróstegui JI, Yagüe J, Rami L, Lladó A, Molinuevo JL (2008) First demonstrated de novo insertion in the prion protein gene in a young patient with dementia. J Neurol Neurosurg Psychiatry. 79(7):845–6
pubmed: 18559465
doi: 10.1136/jnnp.2007.137463
Jansen C, Voet W, Head MW, Parchi P, Yull H, Verrips A (2011) A novel seven-octapeptide repeat insertion in the prion protein gene (PRNP) in a Dutch pedigree with Gerstmann–Sträussler–Scheinker disease phenotype: comparison with similar cases from the literature. Acta Neuropathol (Berl). 121(1):59–68
pubmed: 20198483
doi: 10.1007/s00401-010-0656-3
Laplanche JL, Hachimi KHE, Durieux I, Thuillet P, Defebvre L, Delasnerie-Lauprêtre N (1999) Prominent psychiatric features and early onset in an inherited prion disease with a new insertional mutation in the prion protein gene. Brain. 122(12):2375–86
pubmed: 10581230
doi: 10.1093/brain/122.12.2375