Missense mutations in TENM4, a regulator of axon guidance and central myelination, cause essential tremor


Por: Hor, H, Francescatto, L, Bartesaghi, L, Ortega-Cubero, S, Kousi, M, Lorenzo-Betancor, O, Jimenez-Jimenez, FJ, Gironell, A, Clarimon, J, Drechsel, O, Agundez, JAG, Broz, DK, Chiquet-Ehrismann, R, Lleo, A, Coria, F, Garcia-Martin, E, Alonso-Navarro, H, Marti, MJ, Kulisevsky, J, Hor, CN, Ossowski, S, Chrast, R, Katsanis, N, Pastor, P, Estivill, X

Publicada: 15 oct 2015
Resumen:
Essential tremor (ET) is a common movement disorder with an estimated prevalence of 5% of the population aged over 65 years. In spite of intensive efforts, the genetic architecture of ET remains unknown. We used a combination of whole-exome sequencing and targeted resequencing in three ET families. In vitro and in vivo experiments in oligodendrocyte precursor cells and zebrafish were performed to test our findings. Whole-exome sequencing revealed a missense mutation in TENM4 segregating in an autosomal-dominant fashion in an ET family. Subsequent targeted resequencing of TENM4 led to the discovery of two novel missense mutations. Not only did these two mutations segregate with ET in two additional families, but we also observed significant over transmission of pathogenic TENM4 alleles across the three families. Consistent with a dominant mode of inheritance, in vitro analysis in oligodendrocyte precursor cells showed that mutant proteins mislocalize. Finally, expression of human mRNA harboring any of three patient mutations in zebrafish embryos induced defects in axon guidance, confirming a dominant-negative mode of action for these mutations. Our genetic and functional data, which is corroborated by the existence of a Tenm4 knockout mouse displaying an ET phenotype, implicates TENM4 in ET. Together with previous studies of TENM4 in model organisms, our studies intimate that processes regulating myelination in the central nervous system and axon guidance might be significant contributors to the genetic burden of this disorder.

Filiaciones:
Hor, H:
 CRG, Bioinformat & Genom Program, Barcelona, Spain

 UPF, Barcelona, Spain

 Hosp Mar Med Res Inst IMIM, Barcelona, Spain

 CRG CIBER Epidemiol & Salud Publ CIBERESP, Barcelona 08003, Catalonia, Spain

Francescatto, L:
 Duke Univ, Med Ctr, Ctr Human Dis Modeling, Durham, NC 27710 USA

Bartesaghi, L:
 Univ Lausanne, Dept Med Genet, CH-1005 Lausanne, Switzerland

 Karolinska Inst, Dept Neurosci, S-17177 Stockholm, Sweden

 CIBERNED, Pamplona 31008, Navarra, Spain

Ortega-Cubero, S:
 Karolinska Inst, Dept Clin Neurosci, S-17177 Stockholm, Sweden

 Univ Navarra, Sch Med, Ctr Appl Med Res CIMA, Div Neurosci,Neurogenet Lab, Pamplona 31008, Navarra, Spain

Kousi, M:
 Duke Univ, Med Ctr, Ctr Human Dis Modeling, Durham, NC 27710 USA

 Univ Navarra, Sch Med, Clin Univ Navarra, Dept Neurol, Pamplona 31008, Navarra, Spain

Lorenzo-Betancor, O:
 Karolinska Inst, Dept Clin Neurosci, S-17177 Stockholm, Sweden

 Univ Navarra, Sch Med, Ctr Appl Med Res CIMA, Div Neurosci,Neurogenet Lab, Pamplona 31008, Navarra, Spain

 Univ Navarra, Sch Med, Clin Univ Navarra, Dept Neurol, Pamplona 31008, Navarra, Spain

 CIBERNED, Pamplona 31008, Navarra, Spain

Jimenez-Jimenez, FJ:
 Hosp Univ Sureste, Neurol Sect, Madrid 28030, Spain

Gironell, A:
 Hosp Santa Creu & Sant Pau, Dept Neurol, Movement Disorders Unit, Barcelona, Spain

 St Pau Biomed Res Inst, Barcelona, Spain

Clarimon, J:
 St Pau Biomed Res Inst, Barcelona, Spain

 Univ Autonoma Barcelona, Barcelona 08026, Catalonia, Spain

 CIBERNED, Barcelona 08026, Catalonia, Spain

Drechsel, O:
 CRG, Bioinformat & Genom Program, Barcelona, Spain

 UPF, Barcelona, Spain

Agundez, JAG:
 Univ Extremadura, Dept Pharmacol, Caceres 10071, Spain

Broz, DK:
 Novartis Res Fdn, Friedrich Miescher Inst Biomed Res, Fac Sci, CH-4058 Basel, Switzerland

 Novartis Res Fdn, Friedrich Miescher Inst Biomed Res, Dept Biomed, CH-4058 Basel, Switzerland

 Univ Basel, CH-4058 Basel, Switzerland

Chiquet-Ehrismann, R:
 Novartis Res Fdn, Friedrich Miescher Inst Biomed Res, Fac Sci, CH-4058 Basel, Switzerland

 Novartis Res Fdn, Friedrich Miescher Inst Biomed Res, Dept Biomed, CH-4058 Basel, Switzerland

 Univ Basel, CH-4058 Basel, Switzerland

Lleo, A:
 St Pau Biomed Res Inst, Barcelona, Spain

Coria, F:
 Son Espases Univ Hosp, Serv Neurol, Clin Nervous Disorders, Palma De Mallorca 07120, Spain

Garcia-Martin, E:
 Univ Extremadura, Dept Biochem & Mol Biol, Caceres 10071, Spain

 CIBERNED, Hosp Clin, Neurol Serv, Movement Disorders Unit, Barcelona 08036, Catalonia, Spain

Marti, MJ:
 Inst Invest Biomed August Pi i Sunyer IDIBAPS, Barcelona 08036, Catalonia, Spain

Kulisevsky, J:
 Hosp Santa Creu & Sant Pau, Dept Neurol, Movement Disorders Unit, Barcelona, Spain

 Univ Autonoma Barcelona, Barcelona 08026, Catalonia, Spain

 CIBERNED, Barcelona 08026, Catalonia, Spain

Hor, CN:
 CRG, Bioinformat & Genom Program, Barcelona, Spain

 UPF, Barcelona, Spain

 Hosp Mar Med Res Inst IMIM, Barcelona, Spain

 CRG CIBER Epidemiol & Salud Publ CIBERESP, Barcelona 08003, Catalonia, Spain

Ossowski, S:
 CRG, Bioinformat & Genom Program, Barcelona, Spain

 UPF, Barcelona, Spain

Chrast, R:
 Univ Lausanne, Dept Med Genet, CH-1005 Lausanne, Switzerland

 Karolinska Inst, Dept Neurosci, S-17177 Stockholm, Sweden

Pastor, P:
 UPF, Barcelona, Spain

 Karolinska Inst, Dept Clin Neurosci, S-17177 Stockholm, Sweden

 Univ Navarra, Sch Med, Ctr Appl Med Res CIMA, Div Neurosci,Neurogenet Lab, Pamplona 31008, Navarra, Spain

 Univ Navarra, Sch Med, Clin Univ Navarra, Dept Neurol, Pamplona 31008, Navarra, Spain

 CIBERNED, Pamplona 31008, Navarra, Spain

Estivill, X:
 CRG, Bioinformat & Genom Program, Barcelona, Spain

 Hosp Mar Med Res Inst IMIM, Barcelona, Spain

 CRG CIBER Epidemiol & Salud Publ CIBERESP, Barcelona 08003, Catalonia, Spain

 Univ Hosp Quiron Dexeus, Dexeus Womens Hlth, Barcelona 08028, Catalonia, Spain
ISSN: 09646906





HUMAN MOLECULAR GENETICS
Editorial
OXFORD UNIV PRESS, GREAT CLARENDON ST, OXFORD OX2 6DP, ENGLAND, Reino Unido
Tipo de documento: Article
Volumen: 24 Número: 20
Páginas: 5677-5686
WOS Id: 000363022600002
ID de PubMed: 26188006
imagen Green Published, Bronze

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