Loss-of-Function Variants in CUL3 Cause a Syndromic Neurodevelopmental Disorder

被引：2

作者：

Blackburn, Patrick R. ^{[1
]}

Ebstein, Frederic ^{[2
,3
]}

Hsieh, Tzung-Chien ^{[4
]}

Motta, Marialetizia ^{[5
]}

Radio, Francesca Clementina ^{[5
]}

Herkert, Johanna C. ^{[6
]}

Rinne, Tuula ^{[7
]}

Thiffault, Isabelle ^{[8
,9
]}

Rapp, Michele ^{[10
]}

Alders, Mariel ^{[11
]}

Maas, Saskia ^{[11
]}

Gerard, Benedicte ^{[12
]}

Smol, Thomas ^{[13
]}

Vincent-Delorme, Catherine ^{[14
]}

Cogne, Benjamin ^{[3
,15
]}

Isidor, Bertrand ^{[3
,15
]}

Vincent, Marie ^{[3
,15
]}

Bachmann-Gagescu, Ruxandra ^{[16
,17
]}

Rauch, Anita ^{[16
]}

Joset, Pascal ^{[18
]}

Ferrero, Giovanni Battista ^{[19
]}

Ciolfi, Andrea ^{[5
]}

Husson, Thomas ^{[20
,21
]}

Guerrot, Anne-Marie ^{[21
]}

Bacino, Carlos ^{[22
]}

Macmurdo, Colleen ^{[23
]}

Thompson, Stephanie S. ^{[23
]}

Rosenfeld, Jill A. ^{[24
]}

Faivre, Laurence ^{[25
,26
]}

Mau-Them, Frederic Tran ^{[26
,27
]}

Deb, Wallid ^{[3
]}

Vignard, Virginie ^{[3
]}

Agrawal, Pankaj B. ^{[28
,29
]}

Madden, Jill A. ^{[28
,29
]}

Goldenberg, Alice ^{[21
]}

Lecoquierre, Francois ^{[21
]}

Zech, Michael ^{[30
,31
,32
]}

Prokisch, Holger ^{[30
,31
,32
]}

Necpal, Jan ^{[33
,34
]}

Jech, Robert ^{[35
]}

Winkelmann, Juliane ^{[36
,37
,38
,39
]}

Koprusakova, Monika Turcanova ^{[40
]}

Konstantopoulou, Vassiliki ^{[41
]}

Younce, John R. ^{[42
]}

Shinawi, Marwan ^{[43
,44
]}

Mighton, Chloe ^{[45
,46
]}

Fung, Charlotte ^{[47
,48
]}

Morel, Chantal F. ^{[47
,49
]}

Lerner-Ellis, Jordan ^{[50
,51
,52
]}

Ditroia, Stephanie ^{[53
]}

机构：

[1] St Jude Childrens Res Hosp, Dept Pathol, 262 Danny Thomas Pl, Memphis, TN 38105 USA

[2] Univ Med Greifswald, Inst Med Biochem & Mol Biol, Greifswald, Germany

[3] Nantes Univ, Inst Thorax, CHU Nantes, CNRS,INSERM, Nantes, France

[4] Univ Bonn, Inst Genom Stat & Bioinformat, Bonn, Germany

[5] Osped Pediatr Bambino Gesu, IRCCS, Mol Genet & Funct Genom, Rome, Italy

[6] Univ Groningen, Univ Med Ctr Groningen, Dept Genet, Groningen, Netherlands

[7] Radboud Univ Nijmegen, Med Ctr, Dept Human Genet, Nijmegen, Netherlands

[8] Childrens Mercy Hosp, Ctr Pediat Genom Med, Kansas City, MO 64108 USA

[9] Childrens Mercy Hosp, Dept Pathol & Lab Med, Kansas City, MO USA

[10] Childrens Hosp Colorado, Dept Clin Nutr, Aurora, CO USA

[11] Univ Amsterdam, Amsterdam Univ Med Ctr, Dept Clin Genet, Amsterdam, Netherlands

[12] Ctr Hosp Univ Strasbourg, Unite Biol & Genet Mol, Strasbourg, France

[13] Univ Lille, Inst Genet Med, RADEME Team, CHU Lille, Lille, France

[14] CHU Lille, Hop Jeanne Flandre, Dept Clin Genet, Lille, France

[15] Nantes Univ, Serv Genet Med, CHU Nantes, Nantes, France

[16] Univ Zurich, Inst Med Genet, Schlieren, Switzerland

[17] Univ Zurich, Dept Mol Life Sci, Zurich, Switzerland

[18] Univ Hosp Basel, Inst Med Genet & Pathol, Med Genet, Basel, Switzerland

[19] Univ Torino, San Luigi Gonzaga Univ Hosp, Dept Clin & Biol Sci, Turin, Italy

[20] Ctr Hosp Rouvray, Dept Res, Rouen, France

[21] Normandie Univ, Reference Ctr Dev Disorders, Dept Genet, UNIROUEN, Rouen, France

[22] Baylor Coll Med, Dept Mol & Human Genet, Houston, TX USA

[23] Baylor Scott & White Med Ctr, Dept Internal Med, Div Med Genet, Temple, TX USA

[24] Baylor Genet, Houston, TX USA

[25] Ctr Genet, Ctr Reference Anomalies Dev & Syndromes Malformat, FHU TRANSLAD CHU, Dijon, France

[26] Univ Bourgogne Franche Comte, Equipe GAD, INSERM UMR1231, Dijon, France

[27] CHU Dijon Bourgogne, Unite Fonct Innovat Diagnost Genom Malad Rares, FHU TRANSLAD, Dijon, France

[28] Manton Ctr Orphan Dis Res, Div Genet & Genom, Boston, MA USA

[29] Univ Miami, Holtz Childrens Hosp, Dept Pediat, Div Neonatol,Miller Sch Med, Miami, FL USA

[30] Helmholtz Zentrum Munchen, Inst Neurogenom, Munich, Germany

[31] Tech Univ Munich, Inst Human Genet, Sch Med, Munich, Germany

[32] Tech Univ Munich, Inst Adv Study, Garching, Germany

[33] Zvolen Hosp, Dept Neurol, Zvolen, Slovakia

[34] Comenius Univ, Fac Med, Dept Neurol, Bratislava, Slovakia

[35] Charles Univ Prague, Gen Univ Hosp, Fac Med 1, Dept Neurol, Prague, Czech Republic

[36] Helmholtz Zentrum Muenchen, Inst Neurogenom, Neuherberg, Germany

[37] Tech Univ Muenchen, Neurogenet, Munich, Germany

[38] Klinikum Rechts Isar TUM, Inst Human Genet, Munich, Germany

[39] Munich Cluster Syst Neurol SyNergy, Munich, Germany

[40] Comenius Univ, Jessenius Fac Med Martin, Martin, Slovakia

[41] Med Univ Vienna, Dept Pediat & Adolescent Med, Vienna, Austria

[42] Univ North Carolina Chapel Hill, Dept Neurol, Chapel Hill, NC USA

[43] St Louis Childrens Hosp, Div Genet & Genom Med, St. Louis, MO USA

[44] Washington Univ, Sch Med, Dept Neurol, St. Louis, MO USA

[45] Univ Toronto, Inst Hlth Policy Management & Evaluat, Toronto, ON, Canada

[46] St Michaels Hosp, Li Ka Shing Knowledge Inst, Policy Res Program, Genom Hlth Serv, Toronto, ON, Canada

[47] Univ Hlth Network & Sinai Hlth Syst, Fred A Litwin Family Ctr Genet Med, Toronto, ON, Canada

[48] Univ Toronto, Dept Mol Genet, Toronto, ON, Canada

[49] Univ Toronto, Dept Med, Toronto, ON, Canada

[50] Mt Sinai Hosp, Pathol & Lab Med, Sinai Hlth, Toronto, ON, Canada

来源：

ANNALS OF NEUROLOGY | 2024年

基金：

中国国家自然科学基金; 美国国家卫生研究院;

关键词：

DE-NOVO MUTATIONS; PROTEIN NETWORK; CULLIN; 3; SUBUNIT; GENES; PHENOTYPE; ENCODES;

D O I：

10.1002/ana.27077

中图分类号：

R74 [神经病学与精神病学];

学科分类号：

摘要：

Purpose: De novo variants in CUL3 (Cullin-3 ubiquitin ligase) have been strongly associated with neurodevelopmental disorders (NDDs), but no large case series have been reported so far. Here we aimed to collect sporadic cases carrying rare variants in CUL3, describe the genotype-phenotype correlation, and investigate the underlying pathogenic mechanism. Methods: Genetic data and detailed clinical records were collected via multi-center collaboration. Dysmorphic facial features were analyzed using GestaltMatcher. Variant effects on CUL3 protein stability were assessed using patient-derived T-cells. Results: We assembled a cohort of 35 individuals with heterozygous CUL3 variants presenting a syndromic NDD characterized by intellectual disability with or without autistic features. Of these, 33 have loss-of-function (LoF) and two have missense variants. CUL3 LoF variants in patients may affect protein stability leading to perturbations in protein homeostasis, as evidenced by decreased ubiquitin-protein conjugates in vitro . Specifically, we show that cyclin E1 (CCNE1) and 4E-BP1 (EIF4EBP1), two prominent substrates of CUL3, fail to be targeted for proteasomal degradation in patient-derived cells. Conclusion: Our study further refines the clinical and mutational spectrum of CUL3 -associated NDDs, expands the spectrum of cullin RING E3 ligase-associated neuropsychiatric disorders, and suggests haploinsufficiency via LoF variants is the predominant pathogenic mechanism.

引用

页码：76 / 89

页数：14

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[25] Further evidence for de novo variants in SYNCRIP as the cause of a neurodevelopmental disorder [J].

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共 50 条

[21] Loss-of-function variants in UBAP1L cause autosomal recessive retinal degeneration [J].

Han, Ji Hoon ;

Rodenburg, Kim ;

Hayman, Tamar ;

Calzetti, Giacomo ;

Kaminska, Karolina ;

Quinodoz, Mathieu ;

Marra, Molly ;

Wallerich, Sandrine ;

Allon, Gilad ;

Nagy, Zoltan Z. ;

Knezy, Krisztina ;

Li, Yumei ;

Chen, Rui ;

Barboni, Mirella Telles Salgueiro ;

Yang, Paul ;

Pennesi, Mark E. ;

van den Born, L. Ingeborgh ;

Varsanyi, Balazs ;

Szabo, Viktoria ;

Sharon, Dror ;

Banin, Eyal ;

Ben-Yosef, Tamar ;

Roosing, Susanne ;

Koenekoop, Robert K. ;

Rivolta, Carlo .

GENETICS IN MEDICINE, 2024, 26 (06)

[22] Missense variants in RPH3A cause defects in excitatory synaptic function and are associated with a clinically variable neurodevelopmental disorder [J].

Pavinato, Lisa ;

Stanic, Jennifer ;

Barzasi, Marta ;

Gurgone, Antonia ;

Chiantia, Giuseppe ;

Cipriani, Valentina ;

Eberini, Ivano ;

Palazzolo, Luca ;

Di Luca, Monica ;

Costa, Alex ;

Marcantoni, Andrea ;

Biamino, Elisa ;

Spada, Marco ;

Hiatt, Susan M. ;

Kelley, Whitley, V ;

Vestito, Letizia ;

Efthymiou, Stephanie ;

Chand, Prem ;

Kaiyrzhanov, Rauan ;

Bruselles, Alessandro ;

Cardaropoli, Simona ;

Tartaglia, Marco ;

De Rubies, Silvia ;

Buxbaum, Joseph D. ;

Smedley, Damian ;

Ferrero, Giovanni Battista ;

Giustetto, Maurizio ;

Gardoni, Fabrizio ;

Brusco, Alfredo .

GENETICS IN MEDICINE, 2023, 25 (11)

[23] Loss-of-function of KMT5B leads to neurodevelopmental disorder and impairs neuronal development and neurogenesis [J].

Chen, Guodong ;

Han, Lin ;

Tan, Senwei ;

Jia, Xiangbin ;

Wu, Huidan ;

Quan, Yingting ;

Zhang, Qiumeng ;

Yu, Bin ;

Hu, Zhengmao ;

Xia, Kun ;

Guo, Hui .

JOURNAL OF GENETICS AND GENOMICS, 2022, 49 (09) :881-890

[24] Pathogenic variants in SMARCA5, a chromatin remodeler, cause a range of syndromic neurodevelopmental features [J].

Li, Dong ;

Wang, Qin ;

Gong, Naihua N. ;

Kurolap, Alina ;

Feldman, Hagit Baris ;

Boy, Nikolas ;

Brugger, Melanie ;

Grand, Katheryn ;

McWalter, Kirsty ;

Sacoto, Maria J. Guillen ;

Wakeling, Emma ;

Hurst, Jane ;

March, Michael E. ;

Bhoj, Elizabeth J. ;

Nowaczyk, Malgorzata J. M. ;

Gonzaga-Jauregui, Claudia ;

Mathew, Mariam ;

Dava-Wala, Ashita ;

Siemon, Amy ;

Bartholomew, Dennis ;

Huang, Yue ;

Lee, Hane ;

Martinez-Agosto, Julian A. ;

Schwaibold, Eva M. C. ;

Brunet, Theresa ;

Choukair, Daniela ;

Pais, Lynn S. ;

White, Susan M. ;

Christodoulou, John ;

Brown, Dana ;

Lindstrom, Kristin ;

Grebe, Theresa ;

Tiosano, Dov ;

Kayser, Matthew S. ;

Tan, Tiong Yang ;

Deardorff, Matthew A. ;

Song, Yuanquan ;

Hakonarson, Hakon .

SCIENCE ADVANCES, 2021, 7 (20)

[25] Further evidence for de novo variants in SYNCRIP as the cause of a neurodevelopmental disorder [J].

Semino, Francesca ;

Schroeter, Julian ;

Willemsen, Marjolein H. ;

Bast, Thomas ;

Biskup, Saskia ;

Beck-Woedl, Stefanie ;

Brennenstuhl, Heiko ;

Schaaf, Christian P. ;

Koelker, Stefan ;

Hoffmann, Georg F. ;

Haack, Tobias B. ;

Syrbe, Steffen .

HUMAN MUTATION, 2021, 42 (09) :1094-1100

[26] De novo variants in TCF7L2 are associated with a syndromic neurodevelopmental disorder [J].

Dias, Caroline ;

Pfundt, Rolph ;

Kleefstra, Tjitske ;

Shuurs-Hoeijmakers, Janneke ;

Boon, Elles M. J. ;

van Hagen, Johanna M. ;

Zwijnenburg, Petra ;

Weiss, Marjan M. ;

Keren, Boris ;

Mignot, Cyril ;

Isapof, Arnaud ;

Weiss, Karin ;

Hershkovitz, Tova ;

Iascone, Maria ;

Maitz, Silvia ;

Feichtinger, Rene G. ;

Kotzot, Dieter ;

Mayr, Johannes A. ;

Ben-Omran, Tawfeg ;

Mahmoud, Laila ;

Pais, Lynn S. ;

Walsh, Christopher A. ;

Shashi, Vandana ;

Sullivan, Jennifer A. ;

Stong, Nicholas ;

Lecoquierre, Francois ;

Guerrot, Anne-Marie ;

Charollais, Aude ;

Rodan, Lance H. .

AMERICAN JOURNAL OF MEDICAL GENETICS PART A, 2021, 185 (08) :2384-2390

[27] Consolidating the association of biallelic MAPKAPK5 pathogenic variants with a distinct syndromic neurodevelopmental disorder [J].

Maroofian, Reza ;

Efthymiou, Stephanie ;

Suri, Mohnish ;

Rahman, Fatima ;

Zaki, Maha S. ;

Maqbool, Shazia ;

Anwa, Najwa ;

Ruiz-Perez, Victor L. ;

Yanovsky-Dagan, Shira ;

Elpeleg, Orly ;

Sudhakar, Sniya ;

Mankad, Kshitij ;

Harel, Tamar ;

Houlden, Henry .

JOURNAL OF MEDICAL GENETICS, 2023, 60 (08) :791-796

[28] Gain and loss of function variants in EZH1 disrupt neurogenesis and cause dominant and recessive neurodevelopmental disorders [J].

Gracia-Diaz, Carolina ;

Zhou, Yijing ;

Yang, Qian ;

Maroofian, Reza ;

Espana-Bonilla, Paula ;

Lee, Chul-Hwan ;

Zhang, Shuo ;

Padilla, Natalia ;

Fueyo, Raquel ;

Waxman, Elisa ;

Lei, Sunyimeng ;

Otrimski, Garrett ;

Li, Dong ;

Sheppard, Sarah ;

Mark, Paul ;

Harr, Margaret ;

Hakonarson, Hakon ;

Rodan, Lance ;

Jackson, Adam ;

Vasudevan, Pradeep ;

Powel, Corrina ;

Mohammed, Shehla ;

Maddirevula, Sateesh ;

Alzaidan, Hamad ;

Faqeih, Eissa ;

Efthymiou, Stephanie ;

Turchetti, Valentina ;

Rahman, Fatima ;

Maqbool, Shazia ;

Salpietro, Vincenzo ;

Ibrahim, Shahnaz ;

di Rosa, Gabriella ;

Houlden, Henry ;

Alharbi, Maha Nasser ;

Al-Sannaa, Nouriya Abbas ;

Bauer, Peter ;

Zifarelli, Giovanni ;

Estaras, Conchi ;

Hurst, Anna C. E. ;

Thompson, Michelle ;

Chassevent, Anna ;

Smith-Hicks, Constance ;

de la Cruz, Xavier ;

Holtz, Alexander ;

Elloumi, Houda Zghal ;

Hajianpour, M. J. L. ;

Rieubland, Claudine A. ;

Braun, Dominique ;

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