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Network structure and transcriptomic vulnerability shape atrophy in frontotemporal dementia

Title:	Network structure and transcriptomic vulnerability shape atrophy in frontotemporal dementia
Authors:	Shafiei, Golia; Bazinet, Vincent; Dadar, Mahsa; Manera, Ana L; Collins, D Louis; Dagher, Alain; Borroni, Barbara; Sanchez-Valle, Raquel; Moreno, Fermin; Laforce, Robert; Graff, Caroline; Synofzik, Matthis; Galimberti, Daniela; Rowe, James B; Masellis, Mario; Tartaglia, Maria Carmela; Finger, Elizabeth; Vandenberghe, Rik; de Mendonça, Alexandre; Tagliavini, Fabrizio; Santana, Isabel; Butler, Chris; Gerhard, Alex; Danek, Adrian; Levin, Johannes; Otto, Markus; Sorbi, Sandro; Jiskoot, Lize C; Seelaar, Harro; van Swieten, John C; Rohrer, Jonathan D; Misic, Bratislav; Ducharme, Simon; Frontotemporal Lobar Degeneration Neuroimaging Initiative (FTLDNI); GENetic Frontotemporal dementia Initiative (GENFI); Howard Rosen; Bradford C Dickerson; Kimoko Domoto-Reilly; David Knopman; Bradley F Boeve; Adam L Boxer; John Kornak; Bruce L Miller; William W Seeley; Maria-Luisa Gorno-Tempini; Scott McGinnis; Maria Luisa Mandelli; Aitana Sogorb Esteve; Annabel Nelson; Arabella Bouzigues; Carolin Heller; Caroline V Greaves; David Cash; David L Thomas; Emily Todd; Hanya Benotmane; Henrik Zetterberg; Imogen J Swift; Jennifer Nicholas; Kiran Samra; Lucy L Russell; Martina Bocchetta; Rachelle Shafei; Rhian S Convery; Carolyn Timberlake; Thomas Cope; Timothy Rittman; Alberto Benussi; Enrico Premi; Roberto Gasparotti; Silvana Archetti; Stefano Gazzina; Valentina Cantoni; Andrea Arighi; Chiara Fenoglio; Elio Scarpini; Giorgio Fumagalli; Vittoria Borracci; Giacomina Rossi; Giorgio Giaccone; Giuseppe Di Fede; Paola Caroppo; Pietro Tiraboschi; Sara Prioni; Veronica Redaelli; David Tang-Wai; Ekaterina Rogaeva; Miguel Castelo-Branco; Morris Freedman; Ron Keren; Sandra Black; Sara Mitchell; Christen Shoesmith; Robart Bartha; Rosa Rademakers; Emma van der Ende; Jackie Poos; Janne M Papma; Lucia Giannini; Rick van Minkelen; Yolande Pijnenburg; Benedetta Nacmias; Camilla Ferrari; Cristina Polito; Gemma Lombardi; Valentina Bessi; Michele Veldsman; Christin Andersson; Hakan Thonberg; Linn Öijerstedt; Vesna Jelic; Paul Thompson; Tobias Langheinrich; Albert Lladó; Anna Antonell; Jaume Olives; Mircea Balasa; Nuria Bargalló; Sergi Borrego-Ecija; Ana Verdelho; Carolina Maruta; Catarina B Ferreira; Gabriel Miltenberger; Frederico Simões do Couto; Alazne Gabilondo; Ana Gorostidi; Jorge Villanua; Marta Cañada; Mikel Tainta; Miren Zulaica; Myriam Barandiaran; Patricia Alves; Benjamin Bender; Carlo Wilke; Lisa Graf; Annick Vogels; Mathieu Vandenbulcke; Philip Van Damme; Rose Bruffaerts; Pedro Rosa-Neto; Serge Gauthier; Agnès Camuzat; Alexis Brice; Anne Bertrand; Aurélie Funkiewiez; Daisy Rinaldi; Dario Saracino; Olivier Colliot; Sabrina Sayah; Catharina Prix; Elisabeth Wlasich; Olivia Wagemann; Sandra Loosli; Sonja Schönecker; Tobias Hoegen; Jolina Lombardi; Sarah Anderl-Straub; Adeline Rollin; Gregory Kuchcinski; Maxime Bertoux; Thibaud Lebouvier; Vincent Deramecourt; Beatriz Santiago; Diana Duro; Maria João Leitão; Maria Rosario Almeida; Miguel Tábuas-Pereira; Sónia Afonso; Annerose Engel; Maryna Polyakova
Contributors:	Golia, Shafiei; Vincent, Bazinet; Mahsa, Dadar; Ana L, Manera; D Louis, Collin; Alain, Dagher; Barbara, Borroni; Raquel, Sanchez-Valle; Fermin, Moreno; Robert, Laforce; Caroline, Graff; Matthis, Synofzik; Daniela, Galimberti; James B, Rowe; Mario, Maselli; Maria Carmela, Tartaglia; Elizabeth, Finger; Rik, Vandenberghe; Alexandre, De Mendonça; Fabrizio, Tagliavini; Isabel, Santana; Chris, Butler; Alex, Gerhard; Adrian, Danek; Johannes, Levin; Markus, Otto; Sandro, Sorbi; Lize C, Jiskoot; Harro, Seelaar; John C, Van Swieten; Jonathan D, Rohrer; Bratislav, Misic; Simon, Ducharme; Lobar Degeneration Neuroimaging Initiative (FTLDNI), Frontotemporal; Frontotemporal dementia Initiative (GENFI), Genetic; Rosen, Howard; C Dickerson, Bradford; Domoto-Reilly, Kimoko; Knopman, David; F Boeve, Bradley; L Boxer, Adam; Kornak, John; L Miller, Bruce; W Seeley, William; Gorno-Tempini, Maria-Luisa; Mcginnis, Scott; Luisa Mandelli, Maria; Sogorb Esteve, Aitana; Nelson, Annabel; Bouzigues, Arabella; Heller, Carolin; V Greaves, Caroline; Cash, David; L Thomas, David; Todd, Emily; Benotmane, Hanya; Zetterberg, Henrik; J Swift, Imogen; Nicholas, Jennifer; Samra, Kiran; L Russell, Lucy; Bocchetta, Martina; Shafei, Rachelle; S Convery, Rhian; Timberlake, Carolyn; Cope, Thoma; Rittman, Timothy; Benussi, Alberto; Premi, Enrico; Gasparotti, Roberto; Archetti, Silvana; Gazzina, Stefano; Cantoni, Valentina; Arighi, Andrea; Fenoglio, Chiara; Scarpini, Elio; Fumagalli, Giorgio; Borracci, Vittoria; Rossi, Giacomina; Giaccone, Giorgio; Di Fede, Giuseppe; Caroppo, Paola; Tiraboschi, Pietro; Prioni, Sara; Redaelli, Veronica; Tang-Wai, David; Rogaeva, Ekaterina; Castelo-Branco, Miguel; Freedman, Morri; Keren, Ron; Black, Sandra; Mitchell, Sara; Shoesmith, Christen; Bartha, Robart; Rademakers, Rosa; Van Der Ende, Emma; Poos, Jackie; M Papma, Janne; Giannini, Lucia; Van Minkelen, Rick
Publication Year:	2023
Collection:	Università degli studi di Trieste: ArTS (Archivio della ricerca di Trieste)
Subject Terms:	connectome; disease epicentre; frontotemporal dementia; gene expression; network spreading
Description:	Connections among brain regions allow pathological perturbations to spread from a single source region to multiple regions. Patterns of neurodegeneration in multiple diseases, including behavioural variant of frontotemporal dementia (bvFTD), resemble the large-scale functional systems, but how bvFTD-related atrophy patterns relate to structural network organization remains unknown. Here we investigate whether neurodegeneration patterns in sporadic and genetic bvFTD are conditioned by connectome architecture. Regional atrophy patterns were estimated in both genetic bvFTD (75 patients, 247 controls) and sporadic bvFTD (70 patients, 123 controls). First, we identified distributed atrophy patterns in bvFTD, mainly targeting areas associated with the limbic intrinsic network and insular cytoarchitectonic class. Regional atrophy was significantly correlated with atrophy of structurally- and functionally-connected neighbours, demonstrating that network structure shapes atrophy patterns. The anterior insula was identified as the predominant group epicentre of brain atrophy using data-driven and simulation-based methods, with some secondary regions in frontal ventromedial and antero-medial temporal areas. We found that FTD-related genes, namely C9orf72 and TARDBP, confer local transcriptomic vulnerability to the disease, modulating the propagation of pathology through the connectome. Collectively, our results demonstrate that atrophy patterns in sporadic and genetic bvFTD are jointly shaped by global connectome architecture and local transcriptomic vulnerability, providing an explanation as to how heterogenous pathological entities can lead to the same clinical syndrome.
Document Type:	article in journal/newspaper
Language:	English
Relation:	info:eu-repo/semantics/altIdentifier/pmid/35188955; info:eu-repo/semantics/altIdentifier/wos/WOS:000898821500001; volume:146; issue:1; firstpage:321; lastpage:336; numberofpages:16; journal:BRAIN; https://hdl.handle.net/11368/3097190; https://academic.oup.com/brain/article/146/1/321/6533638?login=true
DOI:	10.1093/brain/awac069
Availability:	https://hdl.handle.net/11368/3097190; https://doi.org/10.1093/brain/awac069; https://academic.oup.com/brain/article/146/1/321/6533638?login=true
Rights:	info:eu-repo/semantics/openAccess ; license:Creative commons ; license:Digital Rights Management non definito ; license uri:http://creativecommons.org/licenses/by-nc/4.0/ ; license uri:iris.PRI00
Accession Number:	edsbas.3F9FDB3C
Database:	BASE