Ubiquitination of MBNL1 Is Required for Its Cytoplasmic Localization and Function in Promoting Neurite Outgrowth

被引:42
作者
Wang, Pei-Ying [1 ,2 ,3 ]
Chang, Kuei-Ting [3 ]
Lin, Yu-Mei [3 ]
Kuo, Ting-Yu [3 ]
Wang, Guey-Shin [1 ,2 ,3 ,4 ]
机构
[1] Natl Yang Ming Univ, Program Mol Med, Taipei, Taiwan
[2] Acad Sinica, Taipei, Taiwan
[3] Acad Sinica, Inst Biomed Sci, Taipei, Taiwan
[4] Natl Yang Ming Univ, Taiwan Int Grad Program Interdisciplinary Neurosc, Taipei, Taiwan
关键词
MYOTONIC-DYSTROPHY; MUSCLEBLIND PROTEINS; MESSENGER-RNA; MOUSE MODEL; EARLY EVENT; BRAIN; ACTIVATION; SEQUESTRATION; ASSOCIATION; EXPRESSION;
D O I
10.1016/j.celrep.2018.02.025
中图分类号
Q2 [细胞生物学];
学科分类号
071009 ; 090102 ;
摘要
The Muscleblind-like protein family (MBNL) plays an important role in regulating the transition between differentiation and pluripotency and in the pathogenesis of myotonic dystrophy type 1 (DM1), a CTG expansion disorder. How different MBNL isoforms contribute to the differentiation and are affected in DM1 has not been investigated. Here, we show that the MBNL1 cytoplasmic, but not nuclear, isoform promotes neurite morphogenesis and reverses the morphological defects caused by expanded CUG RNA. Cytoplasmic MBNL1 is polyubiquitinated by lysine 63 (K63). Reduced cytoplasmic MBNL1 in the DM1 mouse brain is consistent with the reduced extent of K63 ubiquitination. Expanded CUG RNA induced the deubiqutination of cytoplasmic MBNL1, which resulted in nuclear translocation and morphological impairment that could be ameliorated by inhibiting K63-linked polyubiquitin chain degradation. Our results suggest that K63-linked ubiquitination of MBNL1 is required for its cytoplasmic localization and that deubiquitination of cytoplasmic MBNL1 is pathogenic in the DM1 brain.
引用
收藏
页码:2294 / 2306
页数:13
相关论文
共 42 条
[1]   The muscleblind gene participates in the organization of Z-bands and epidermal attachments of Drosophila muscles and is regulated by Dmef2 [J].
Artero, R ;
Prokop, A ;
Paricio, N ;
Begemann, G ;
Pueyo, I ;
Mlodzik, M ;
Perez-Alonso, M ;
Baylies, MK .
DEVELOPMENTAL BIOLOGY, 1998, 195 (02) :131-143
[2]   Loss of MBNL Leads to Disruption of Developmentally Regulated Alternative Polyadenylation in RNA-Mediated Disease [J].
Batra, Ranjan ;
Charizanis, Konstantinos ;
Manchanda, Mini ;
Mohan, Apoorva ;
Li, Moyi ;
Finn, Dustin J. ;
Goodwin, Marianne ;
Zhang, Chaolin ;
Sobczak, Krzysztof ;
Thornton, Charles A. ;
Swanson, Maurice S. .
MOLECULAR CELL, 2014, 56 (02) :311-322
[3]   Ubiquitin and the control of protein fate in the secretory and endocytic pathways [J].
Bonifacino, JS ;
Weissman, AM .
ANNUAL REVIEW OF CELL AND DEVELOPMENTAL BIOLOGY, 1998, 14 :19-57
[4]   Muscleblind-like 2-Mediated Alternative Splicing in the Developing Brain and Dysregulation in Myotonic Dystrophy [J].
Charizanis, Konstantinos ;
Lee, Kuang-Yung ;
Batra, Ranjan ;
Goodwin, Marianne ;
Zhang, Chaolin ;
Yuan, Yuan ;
Shiue, Lily ;
Cline, Melissa ;
Scotti, Marina M. ;
Xia, Guangbin ;
Kumar, Ashok ;
Ashizawa, Tetsuo ;
Clark, H. Brent ;
Kimura, Takashi ;
Takahashi, Masanori P. ;
Fujimura, Harutoshi ;
Jinnai, Kenji ;
Yoshikawa, Hiroo ;
Gomes-Pereira, Mario ;
Gourdon, Genevieve ;
Sakai, Noriaki ;
Nishino, Seiji ;
Foster, Thomas C. ;
Ares, Manuel, Jr. ;
Darnell, Robert B. ;
Swanson, Maurice S. .
NEURON, 2012, 75 (03) :437-450
[5]   Muscleblind-like 1 (Mbnl1) regulates pre-mRNA alternative splicing during terminal erythropoiesis [J].
Cheng, Albert W. ;
Shi, Jiahai ;
Wong, Piu ;
Luo, Katherine L. ;
Trepman, Paula ;
Wang, Eric T. ;
Choi, Heejo ;
Burge, Christopher B. ;
Lodish, Harvey F. .
BLOOD, 2014, 124 (04) :598-610
[6]   Candidate tumor suppressor BTG3 maintains genomic stability by promoting Lys63-linked ubiquitination and activation of the checkpoint kinase CHK1 [J].
Cheng, Yu-Che ;
Lin, Tsong-Yu ;
Shieh, Sheau-Yann .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2013, 110 (15) :5993-5998
[7]   Induction and reversal of myotonic dystrophy type 1 pre-mRNA splicing defects by small molecules [J].
Childs-Disney, Jessica L. ;
Stepniak-Konieczna, Ewa ;
Tuan Tran ;
Yildirim, Ilyas ;
Park, HaJeung ;
Chen, Catherine Z. ;
Hoskins, Jason ;
Southall, Noel ;
Marugan, Juan J. ;
Patnaik, Samarjit ;
Zheng, Wei ;
Austin, Chris P. ;
Schatz, George C. ;
Sobczak, Krzysztof ;
Thornton, Charles A. ;
Disney, Matthew D. .
NATURE COMMUNICATIONS, 2013, 4
[8]   Reducing Levels of Toxic RNA with Small Molecules [J].
Coonrod, Leslie A. ;
Nakamori, Masayuki ;
Wang, Wenli ;
Carrell, Samuel ;
Hilton, Cameron L. ;
Bodner, Micah J. ;
Siboni, Ruth B. ;
Docter, Aaron G. ;
Haley, Michael M. ;
Thornton, Charles A. ;
Berglund, J. Andrew .
ACS CHEMICAL BIOLOGY, 2013, 8 (11) :2528-2537
[9]   Activation of the IκB kinase complex by TRAF6 requires a dimeric ubiquitin-conjugating enzyme complex and a unique polyubiquitin chain [J].
Deng, L ;
Wang, C ;
Spencer, E ;
Yang, LY ;
Braun, A ;
You, JX ;
Slaughter, C ;
Pickart, C ;
Chen, ZJ .
CELL, 2000, 103 (02) :351-361
[10]   Aberrant alternative splicing and extracellular matrix gene expression in mouse models of myotonic dystrophy [J].
Du, Hongqing ;
Cline, Melissa S. ;
Osborne, Robert J. ;
Tuttle, Daniel L. ;
Clark, Tyson A. ;
Donohue, John Paul ;
Hall, Megan P. ;
Shiue, Lily ;
Swanson, Maurice S. ;
Thornton, Charles A. ;
Ares, Manuel, Jr. .
NATURE STRUCTURAL & MOLECULAR BIOLOGY, 2010, 17 (02) :187-U8