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Background: Huntington's disease is caused by a CAG repeat expansion in the huntingtin gene, HTT. Age at onset has been used as a quantitative phenotype in genetic analysis looking for Huntington's disease modifiers, but is hard to define and not always available. Therefore, we aimed to generate a novel measure of disease progression and to identify genetic markers associated with this progression measure. Methods: We generated a progression score on the basis of principal component analysis of prospectively acquired longitudinal changes in motor, cognitive, and imaging measures in the 218 indivduals in the TRACK-HD cohort of Huntington's disease gene mutation carriers (data collected 2008-11). We generated a parallel progression score using data from 1773 previously genotyped participants from the European Huntington's Disease Network REGISTRY study of Huntington's disease mutation carriers (data collected 2003-13). We did a genome-wide association analyses in terms of progression for 216 TRACK-HD participants and 1773 REGISTRY participants, then a meta-analysis of these results was undertaken. Findings: Longitudinal motor, cognitive, and imaging scores were correlated with each other in TRACK-HD participants, justifying use of a single, cross-domain measure of disease progression in both studies. The TRACK-HD and REGISTRY progression measures were correlated with each other (r=0·674), and with age at onset (TRACK-HD, r=0·315; REGISTRY, r=0·234). The meta-analysis of progression in TRACK-HD and REGISTRY gave a genome-wide significant signal (p=1·12 × 10-10) on chromosome 5 spanning three genes: MSH3, DHFR, and MTRNR2L2. The genes in this locus were associated with progression in TRACK-HD (MSH3 p=2·94 × 10-8DHFR p=8·37 × 10-7 MTRNR2L2 p=2·15 × 10-9) and to a lesser extent in REGISTRY (MSH3 p=9·36 × 10-4DHFR p=8·45 × 10-4MTRNR2L2 p=1·20 × 10-3). The lead single nucleotide polymorphism (SNP) in TRACK-HD (rs557874766) was genome-wide significant in the meta-analysis (p=1·58 × 10-8), and encodes an aminoacid change (Pro67Ala) in MSH3. In TRACK-HD, each copy of the minor allele at this SNP was associated with a 0·4 units per year (95% CI 0·16-0·66) reduction in the rate of change of the Unified Huntington's Disease Rating Scale (UHDRS) Total Motor Score, and a reduction of 0·12 units per year (95% CI 0·06-0·18) in the rate of change of UHDRS Total Functional Capacity score. These associations remained significant after adjusting for age of onset. Interpretation: The multidomain progression measure in TRACK-HD was associated with a functional variant that was genome-wide significant in our meta-analysis. The association in only 216 participants implies that the progression measure is a sensitive reflection of disease burden, that the effect size at this locus is large, or both. Knockout of Msh3 reduces somatic expansion in Huntington's disease mouse models, suggesting this mechanism as an area for future therapeutic investigation. Funding: The European Commission FP7 NeurOmics project; CHDI Foundation; the Medical Research Council UK; the Brain Research Trust; and the Guarantors of Brain.
Identification of genetic variants associated with Huntington's disease progression: a genome-wide association study
Davina J Hensman Moss;Antonio F Pardiñas;Douglas Langbehn;Kitty Lo;Blair R Leavitt;Raymund Roos;Alexandra Durr;Simon Mead;Peter Holmans;Lesley Jones;Sarah J Tabrizi;A Coleman;R Dar Santos;J Decolongon;A Sturrock;E Bardinet;C Jauff Ret;D Justo;S Lehericy;C Marelli;K Nigaud;R Valabrègue;SJA van den Bogaard;E M Dumas;J van der Grond;EP t'Hart;C Jurgens;M-N Witjes-Ane;N Arran;J Callaghan;C Stopford;C Frost;R Jones;N Hobbs;N Lahiri;R Ordidge;G Owen;T Pepple;J Read;M Say;E Wild;A Patel;N C Fox;C Gibbard;I Malone;H Crawford;D Whitehead;S Keenan;D M Cash;C Berna;N Bechtel;S Bohlen;A Hoff Man;P Kraus;E Axelson;C Wang;T Acharya;S Lee;W Monaco;C Campbell;S Queller;K Whitlock;C Campbell;M Campbell;E Frajman;C Milchman;A O'Regan;I Labuschagne;J Stout;B Landwehrmeyer;D Craufurd;R Scahill;S Hicks;C Kennard;H Johnson;A Tobin;HD Rosas;R Reilmann;B Borowsky;C Pourchot;S C Andrews;Anne-Catherine Bachoud-Lévi;Anna Rita Bentivoglio;Ida Biunno;Raphael Bonelli;Jean-Marc Burgunder;Stephen Dunnett;Joaquim Ferreira;Olivia Handley;Arvid Heiberg;Torsten Illmann;G. Bernhard Landwehrmeyer;Jamie Levey;Maria A. Ramos-Arroyo;Jørgen Nielsen;Susana Pro Koivisto;Markku Päivärinta;Raymund A. C. Roos;A Rojo Sebastián;Sarah Tabrizi;Wim Vandenberghe;Christine Verellen-Dumoulin;Tereza Uhrova;Jan Wahlström;Jacek Zaremba;Verena Baake;Katrin Barth;Monica Bascuñana Garde;Sabrina Betz;Reineke Bos;Jenny Callaghan;Adrien Come;Leonor Correia Guedes;Daniel Ecker;Ana Maria Finisterra;Ruth Fullam;Mette Gilling;Lena Gustafsson;Olivia J Handley;Carina Hvalstedt;Christine Held;Kerstin Koppers;Claudia Lamanna;Matilde Laurà;Asunción Martínez Descals;Saül Martinez-Horta;Tiago Mestre;Sara Minster;Daniela Monza;Lisanne Mütze;Martin Oehmen;Michael Orth;Hélène Padieu;Laurent Paterski;Nadia Peppa;Susana Pro Koivisto;Martina Di Renzo;Amandine Rialland;Niini Røren;Pavla Šašinková;Erika Timewell;Jenny Townhill;Patricia Trigo Cubillo;Wildson Vieira da Silva;Marleen R van Walsem;Carina Whalstedt;Marie-Noelle Witjes-Ané;Grzegorz Witkowski;Abigail Wright;Daniel Zielonka;Eugeniusz Zielonka;Paola Zinzi;Raphael M. Bonelli;Sabine Lilek;Karen Hecht;Brigitte Herranhof;Anna Holl;Hans-Peter Kapfhammer;Michael Koppitz;Markus Magnet;Nicole Müller;Daniela Otti;Annamaria Painold;Karin Reisinger;Monika Scheibl;Helmut Schöggl;Jasmin Ullah;Eva-Maria Braunwarth;Florian Brugger;Lisa Buratti;Eva-Maria Hametner;Caroline Hepperger;Christiane Holas;Anna Hotter;Anna Hussl;Christoph Müller;Werner Poewe;Klaus Seppi;Fabienne Sprenger;Gregor Wenning;Andrea Boogaerts;Godelinde Calmeyn;Isabelle Delvaux;Dirk Liessens;Nele Somers;Michel Dupuit;Cécile Minet;Dominique van Paemel;Pascale Ribaï;Christine Verellen-Dumoulin;Andrea Boogaerts;Wim Vandenberghe;Dimphna van Reijen;Jirí Klempír;Veronika Majerová;Jan Roth;Irena Stárková;Lena E. Hjermind;Oda Jacobsen;Jørgen E. Nielsen;Ida Unmack Larsen;Tua Vinther-Jensen;Heli Hiivola;Hannele Hyppönen;Kirsti Martikainen;Katri Tuuha;Philippe Allain;Dominique Bonneau;Marie Bost;Bénédicte Gohier;Marie-Anne Guérid;Audrey Olivier;Adriana Prundean;Clarisse Scherer-Gagou;Christophe Verny;Blandine Babiloni;Sabrina Debruxelles;Charlotte Duché;Cyril Goizet;Laetitia Jameau;Danielle Lafoucrière;Umberto Spampinato;Rekha Barthélémy;Christelle De Bruycker;Maryline Cabaret Anne-Sophie Carette;Eric Decorte Luc Defebvre;Marie Delliaux;Arnaud Delval;Alain Destee;Kathy Dujardin;Marie-Hélène Lemaire;Sylvie Manouvrier;Mireille Peter;Lucie Plomhouse;Bernard Sablonnière;Clémence Simonin;Stéphanie Thibault-Tanchou;Isabelle Vuillaume;Marcellin Bellonet;Hassan Berrissoul;Stéphanie Blin;Françoise Courtin;Cécile Duru;Véronique Fasquel;Olivier Godefroy;Pierre Krystkowiak;Béatrice Mantaux;Martine Roussel;Sandrine Wannepain;Jean-Philippe Azulay;Marie Delfini;Alexandre Eusebio;Frédérique Fluchere;Laura Mundler;Mathieu Anheim;Celine Julié;Ouhaid Lagha Boukbiza;Nadine Longato;Gabrielle Rudolf;Christine Tranchant;Marie-Agathe Zimmermann;Christoph Michael Kosinski;Eva Milkereit;Daniela Probst;Kathrin Reetz;Christian Sass;Johannes Schiefer;Christiane Schlangen;Cornelius J. Werner;Harald Gelderblom;Josef Priller;Harald Prüß;Eike Jakob Spruth;Gisa Ellrichmann;Lennard Herrmann;Rainer Hoffmann;Barbara Kaminski;Peter Kotz;Christian Prehn;Carsten Saft;Herwig Lange;Robert Maiwald;Matthias Löhle;Antonia Maass;Simone Schmidt;Cecile Bosredon;Alexander Storch;Annett Wolz;Martin Wolz;Philipp Capetian;Johann Lambeck;Birgit Zucker;Kai Boelmans;Christos Ganos;Walburgis Heinicke;Ute Hidding;Jan Lewerenz;Alexander Münchau;Michael Orth;Jenny Schmalfeld;Lars Stubbe;Simone Zittel;Gabriele Diercks;Dirk Dressler;Heike Gorzolla;Christoph Schrader;Pawel Tacik;Michael Ribbat;Bernhard Longinus;Katrin Bürk;Jens Carsten Möller;Ida Rissling;Mark Mühlau;Alexander Peinemann;Michael Städtler;Adolf Weindl;Juliane Winkelmann;Cornelia Ziegler;Natalie Bechtel;Heike Beckmann;Stefan Bohlen;Eva Hölzner;Herwig Lange;Ralf Reilmann;Stefanie Rohm;Silke Rumpf;Sigrun Schepers;Natalia Weber;Matthias Dose;Gabriele Leythäuser;Ralf Marquard;Tina Raab;Alexandra Wiedemann;Katrin Barth;Andrea Buck;Julia Connemann;Daniel Ecker;Carolin Geitner;Christine Held;Andrea Kesse;Bernhard Landwehrmeyer;Christina Lang;Jan Lewerenz;Franziska Lezius;Solveig Nepper;Anke Niess;Michael Orth;Ariane Schneider;Daniela Schwenk;Sigurd Süßmuth;Sonja Trautmann;Patrick Weydt;Claudia Cormio;Vittorio Sciruicchio;Claudia Serpino;Marina de Tommaso;Sabina Capellari;Pietro Cortelli;Roberto Galassi;Giovanni Rizzo;Roberto Poda;Cesa Scaglione;Elisabetta Bertini;Elena Ghelli;Andrea Ginestroni;Francesca Massaro;Claudia Mechi;Marco Paganini;Silvia Piacentini;Silvia Pradella;Anna Maria Romoli;Sandro Sorbi;Giovanni Abbruzzese;Monica Bandettini di Poggio;Giovanna Ferrandes;Paola Mandich;Roberta Marchese;Alberto Albanese;Daniela Di Bella;Anna Castaldo;Stefano Di Donato;Cinzia Gellera;Silvia Genitrini;Caterina Mariotti;Daniela Monza;Lorenzo Nanetti;Dominga Paridi;Paola Soliveri;Chiara Tomasello;Giuseppe De Michele;Luigi Di Maio;Marco Massarelli;Silvio Peluso;Alessandro Roca;Cinzia Valeria Russo;Elena Salvatore;Pierpaolo Sorrentino;Enrico Amico;Mariagrazia Favellato;Annamaria Griguoli;Irene Mazzante;Martina Petrollini;Ferdinando Squitieri;Barbara D'Alessio;Chiara Esposito;Rita Bentivoglio;Marina Frontali;Arianna Guidubaldi;Tamara Ialongo;Gioia Jacopini;Carla Piano;Silvia Romano;Francesco Soleti;Maria Spadaro;Paola Zinzi;Monique S. E. van Hout;Marloes E. Verhoeven;Jeroen P. P. van Vugt;A. Marit de Weert;J. J. W. Bolwijn;M. Dekker;B. Kremer;K. L. Leenders;J. C. H. van Oostrom;Simon J. A. van den Bogaard;Reineke Bos;Eve M. Dumas;Ellen P. 't Hart;Raymund A. C. Roos;Berry Kremer;C. C. P. Verstappen;Olaf Aaserud;Jan Frich C;Arvid Heiberg;Marleen R van Walsem;Ragnhild Wehus;Kathrine Bjørgo;Madeleine Fannemel;Per F. Gørvell;Eirin Lorentzen;Susana Pro Koivisto;Lars Retterstøl;Bodil Stokke;Inga Bjørnevoll;Sigrid Botne Sando;Artur Dziadkiewicz;Malgorzata Nowak;Piotr Robowski;Emilia Sitek;Jaroslaw Slawek;Witold Soltan;Michal Szinwelski;Magdalena Blaszcyk;Magdalena Boczarska-Jedynak;Ewelina Ciach-Wysocka;Agnieszka Gorzkowska;Barbara Jasinska-Myga;Gabriela Klodowska-Duda;Gregorz Opala;Daniel Stompel;Krzysztof Banaszkiewicz;Dorota Bocwinska;Kamila Bojakowska-Jaremek;Malgorzata Dec;Malgorzata Krawczyk;Monika Rudzinska;Elzbieta Szczygiel;Andrzej Szczudlik;Anna Wasielewska;Magdalena Wójcik;Anna Bryl;Anna Ciesielska;Aneta Klimberg;Jerzy Marcinkowski;Husam Samara;Justyna Sempolowicz;Daniel Zielonka;Anna Gogol;Piotr Janik;Hubert Kwiecinski;Zygmunt Jamrozik;Jakub Antczak;Katarzyna Jachinska;Wioletta Krysa;Maryla Rakowicz;Przemyslaw Richter;Rafal Rola;Danuta Ryglewicz;Halina Sienkiewicz-Jarosz;Iwona Stepniak;Anna Sulek;Grzegorz Witkowski;Jacek Zaremba;Elzbieta Zdzienicka;Karolina Zieora-Jakutowicz;Joaquim J Ferreira;Miguel Coelho;Leonor Correia Guedes;Tiago Mendes;Tiago Mestre;Anabela Valadas;Carlos Andrade;Miguel Gago;Carolina Garrett;Maria Rosália Guerra;Carmen Durán Herrera;Patrocinio Moreno Garcia;Miquel Aguilar Barbera;Dolors Badenes Guia;Laura Casas Hernanz;Judit López Catena;Pilar Quiléz Ferrer;Ana Rojo Sebastián;Gemma Tome Carruesco;Jordi Bas;Núria Busquets;Matilde Calopa;Misericordia Floriach Robert;Celia Mareca Viladrich;Jesús Miguel Ruiz Idiago;Antonio Villa Riballo;Esther Cubo;Cecilia Gil Polo;Natividad Mariscal;Perez Jessica Rivadeneyra;Francisco Barrero;Blas Morales;María Fenollar;Rocío García-Ramos García;Paloma Ortega;Clara Villanueva;Javier Alegre;Mónica Bascuñana;Juan Garcia Caldentey;Marta Fatás Ventura;Guillermo García Ribas;Justo García de Yébenes;José Luis López-Sendón Moreno;Patricia Trigo Cubillo;Javier Alegre;Fernando Alonso Frech;Justo García de Yébenes;Pedro J García Ruíz;Asunción Martínez-Descals;Rosa Guerrero;María José Saiz Artiga;Vicenta Sánchez;María Fuensanta Noguera Perea;Lorenza Fortuna;Salvadora Manzanares;Gema Reinante;María Martirio Antequera Torres;Laura Vivancos Moreau;Sonia González González;Luis Menéndez Guisasola;Carlos Salvador;Esther Suaréz San Martín;Inés Legarda Ramirez;Aranzazú Gorospe;Mónica Rodriguez Lopera;Penelope Navas Arques;María José Torres Rodríguez;Barbara Vives Pastor;Itziar Gaston;Maria Dolores Martinez-Jaurrieta;Maria A. Ramos-Arroyo;Jose Manuel Garcia Moreno;Carolina Mendez Lucena;Fatima Damas;Hermoso Eva Pacheco Cortegana;José Chacón Peña;Luis Redondo;Fátima Carrillo;María Teresa Cáceres;Pablo Mir;María José Lama Suarez;Laura Vargas-González;Maria E. Bosca;Francisco Castera Brugada;Juan Andres Burguera;Anabel Campos;Garcia Carmen Peiró Vilaplana;Peter Berglund;Radu Constantinescu;Gunnel Fredlund;Ulrika Høsterey-Ugander;Petra Linnsand;Liselotte Neleborn-Lingefjärd;Jan Wahlström;Magnus Wentzel;Ghada Loutfi;Carina Olofsson;Eva-Lena Stattin;Laila Westman;Birgitta Wikström;Jean-Marc Burgunder;Yanik Stebler;Alain Kaelin;Irene Romero;Michael Schüpbach;Sabine Weber Zaugg;Maria Hauer;Roman Gonzenbach;Hans H. Jung;Violeta Mihaylova;Jens Petersen;Roisin Jack;Kirsty Matheson;Zosia Miedzybrodzka;Daniela Rae;Sheila A Simpson;Fiona Summers;Alexandra Ure;Vivien Vaughan;Shahbana Akhtar;Jenny Crooks;Adrienne Curtis;Jenny de Souza;John Piedad;Hugh Rickards;Jan Wright;Elizabeth Coulthard;Louise Gethin;Beverley Hayward;Kasia Sieradzan;Abigail Wright;Matthew Armstrong;Roger A. Barker;Deidre O'Keefe;Anna Di Pietro;Kate Fisher;Anna Goodman;Susan Hill;Ann Kershaw;Sarah Mason;Nicole Paterson;Lucy Raymond;Rachel Swain;Natalie Valle Guzman;Monica Busse;Cynthia Butcher;Jenny Callaghan;Stephen Dunnett;Catherine Clenaghan;Ruth Fullam;Olivia Handley;Sarah Hunt;Lesley Jones;Una Jones;Hanan Khalil;Sara Minster;Michael Owen;Kathleen Price;Anne Rosser;Jenny Townhill;Maureen Edwards;Carrie Ho;Teresa Hughes;Marie McGill;Pauline Pearson;Mary Porteous;Paul Smith;Peter Brockie;Jillian Foster;Nicola Johns;Sue McKenzie;Jean Rothery;Gareth Thomas;Shona Yates;Liz Burrows;Carol Chu;Amy Fletcher;Deena Gallantrae;Stephanie Hamer;Alison Harding;Stefan Klöppel;Alison Kraus;Fiona Laver;Monica Lewis;Mandy Longthorpe;Ivana Markova;Ashok Raman;Nicola Robertson;Mark Silva;Aileen Thomson;Sue Wild;Pam Yardumian;Carol Chu;Carole Evans;Deena Gallentrae;Stephanie Hamer;Alison Kraus;Ivana Markova;Ashok Raman;Carol Chu;Stephanie Hamer;Emma Hobson;Stuart Jamieson;Alison Kraus;Ivana Markova;Ashok Raman;Hannah Musgrave;Liz Rowett;Jean Toscano;Sue Wild;Pam Yardumian;Colin Bourne;Jackie Clapton;Carole Clayton;Heather Dipple;Dawn Freire-Patino;Janet Grant;Diana Gross;Caroline Hallam;Julia Middleton;Ann Murch;Catherine Thompson;Sundus Alusi;Rhys Davies;Kevin Foy;Emily Gerrans;Louise Pate;Thomasin Andrews;Andrew Dougherty;Charlotte Golding;Fred Kavalier;Hana Laing;Alison Lashwood;Dene Robertson;Deborah Ruddy;Alastair Santhouse;Anna Whaite;Thomasin Andrews;Stefania Bruno;Karen Doherty;Charlotte Golding;Salman Haider;Davina Hensman;Nayana Lahiri;Monica Lewis;Marianne Novak;Aakta Patel;Nicola Robertson;Elisabeth Rosser;Sarah Tabrizi;Rachel Taylor;Thomas Warner;Edward Wild;Natalie Arran;Judith Bek;Jenny Callaghan;David Craufurd;Ruth Fullam;Marianne Hare;Liz Howard;Susan Huson;Liz Johnson;Mary Jones;Helen Murphy;Emma Oughton;Lucy Partington-Jones;Dawn Rogers;Andrea Sollom;Julie Snowden;Cheryl Stopford;Jennifer Thompson;Iris Trender-Gerhard;Nichola Verstraelen;Leann Westmoreland;Richard Armstrong;Kathryn Dixon;Andrea H Nemeth;Gill Siuda;Ruth Valentine;David Harrison;Max Hughes;Andrew Parkinson;Beverley Soltysiak;Oliver Bandmann;Alyson Bradbury;Paul Gill;Helen Fairtlough;Kay Fillingham;Isabella Foustanos;Mbombe Kazoka;Kirsty O'Donovan;Nadia Peppa;Cat Taylor;Katherine Tidswell;Oliver Quarrell;Jean-Marc Burgunder;Puay Ngoh Lau;Emmanul Pica;Louis Tan
2017-01-01
Abstract
Background: Huntington's disease is caused by a CAG repeat expansion in the huntingtin gene, HTT. Age at onset has been used as a quantitative phenotype in genetic analysis looking for Huntington's disease modifiers, but is hard to define and not always available. Therefore, we aimed to generate a novel measure of disease progression and to identify genetic markers associated with this progression measure. Methods: We generated a progression score on the basis of principal component analysis of prospectively acquired longitudinal changes in motor, cognitive, and imaging measures in the 218 indivduals in the TRACK-HD cohort of Huntington's disease gene mutation carriers (data collected 2008-11). We generated a parallel progression score using data from 1773 previously genotyped participants from the European Huntington's Disease Network REGISTRY study of Huntington's disease mutation carriers (data collected 2003-13). We did a genome-wide association analyses in terms of progression for 216 TRACK-HD participants and 1773 REGISTRY participants, then a meta-analysis of these results was undertaken. Findings: Longitudinal motor, cognitive, and imaging scores were correlated with each other in TRACK-HD participants, justifying use of a single, cross-domain measure of disease progression in both studies. The TRACK-HD and REGISTRY progression measures were correlated with each other (r=0·674), and with age at onset (TRACK-HD, r=0·315; REGISTRY, r=0·234). The meta-analysis of progression in TRACK-HD and REGISTRY gave a genome-wide significant signal (p=1·12 × 10-10) on chromosome 5 spanning three genes: MSH3, DHFR, and MTRNR2L2. The genes in this locus were associated with progression in TRACK-HD (MSH3 p=2·94 × 10-8DHFR p=8·37 × 10-7 MTRNR2L2 p=2·15 × 10-9) and to a lesser extent in REGISTRY (MSH3 p=9·36 × 10-4DHFR p=8·45 × 10-4MTRNR2L2 p=1·20 × 10-3). The lead single nucleotide polymorphism (SNP) in TRACK-HD (rs557874766) was genome-wide significant in the meta-analysis (p=1·58 × 10-8), and encodes an aminoacid change (Pro67Ala) in MSH3. In TRACK-HD, each copy of the minor allele at this SNP was associated with a 0·4 units per year (95% CI 0·16-0·66) reduction in the rate of change of the Unified Huntington's Disease Rating Scale (UHDRS) Total Motor Score, and a reduction of 0·12 units per year (95% CI 0·06-0·18) in the rate of change of UHDRS Total Functional Capacity score. These associations remained significant after adjusting for age of onset. Interpretation: The multidomain progression measure in TRACK-HD was associated with a functional variant that was genome-wide significant in our meta-analysis. The association in only 216 participants implies that the progression measure is a sensitive reflection of disease burden, that the effect size at this locus is large, or both. Knockout of Msh3 reduces somatic expansion in Huntington's disease mouse models, suggesting this mechanism as an area for future therapeutic investigation. Funding: The European Commission FP7 NeurOmics project; CHDI Foundation; the Medical Research Council UK; the Brain Research Trust; and the Guarantors of Brain.
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Utilizza questo identificativo per citare o creare un link a questo documento: https://hdl.handle.net/11388/343089
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