Novel Long Noncoding RNAs (lncRNAs) in Myogenesis: a miR-31 Overlapping lncRNA Transcript Controls Myoblast Differentiation

被引:82
作者
Ballarino, Monica [1 ]
Cazzella, Valentina [1 ]
D'Andrea, Daniel [2 ]
Grassi, Luigi [2 ]
Bisceglie, Lavinia [1 ]
Cipriano, Andrea [1 ]
Santini, Tiziana [3 ]
Pinnaro, Chiara [1 ]
Morlando, Mariangela [1 ]
Tramontano, Anna [2 ,3 ]
Bozzoni, Irene [1 ,3 ,4 ,5 ]
机构
[1] Univ Roma La Sapienza, Dept Biol & Biotechnol Charles Darwin, I-00185 Rome, Italy
[2] Univ Roma La Sapienza, Dept Phys, I-00185 Rome, Italy
[3] Ist Italiano Tecnol, Ctr Life Nano Sci Sapienza, Rome, Italy
[4] Univ Roma La Sapienza, Inst Pasteur Fdn Cenci Bolognetti, I-00185 Rome, Italy
[5] Univ Roma La Sapienza, IBPM, I-00185 Rome, Italy
关键词
DUCHENNE MUSCULAR-DYSTROPHY; MUSCLE DIFFERENTIATION; EXPRESSION ANALYSIS; SKELETAL MYOGENESIS; MDX MOUSE; CELLS; GENE; THERAPY; SEQ; REGENERATION;
D O I
10.1128/MCB.01394-14
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
Transcriptome analysis allowed the identification of new long noncoding RNAs differentially expressed during murine myoblast differentiation. These transcripts were classified on the basis of their expression under proliferating versus differentiated conditions, muscle-restricted activation, and subcellular localization. Several species displayed preferential expression in dystrophic (mdx) versus wild-type muscles, indicating their possible link with regenerative processes. One of the identified transcripts, lnc-31, even if originating from the same nuclear precursor of miR-31, is produced by a pathway mutually exclusive. We show that lnc-31 and its human homologue hsa-lnc-31 are expressed in proliferating myoblasts, where they counteract differentiation. In line with this, both species are more abundant in mdx muscles and in human Duchenne muscular dystrophy (DMD) myoblasts, than in their normal counterparts. Altogether, these data suggest a crucial role for lnc-31 in controlling the differentiation commitment of precursor myoblasts and indicate that its function is maintained in evolution despite the poor sequence conservation with the human counterpart.
引用
收藏
页码:728 / 736
页数:9
相关论文
共 45 条
[1]   Screening non-coding RNAs in transcriptomes from neglected species using PORTRAIT: case study of the pathogenic fungus Paracoccidioides brasiliensis Software [J].
Arrial, Roberto T. ;
Togawa, Roberto C. ;
Brigido, Marcelo de M. .
BMC BIOINFORMATICS, 2009, 10
[2]   miR-31 and its host gene lncRNA LOC554202 are regulated by promoter hypermethylation in triple-negative breast cancer [J].
Augoff, Katarzyna ;
McCue, Brian ;
Plow, Edward F. ;
Sossey-Alaoui, Khalid .
MOLECULAR CANCER, 2012, 11
[3]   Identification of small ORFs in vertebrates using ribosome footprinting and evolutionary conservation [J].
Bazzini, Ariel A. ;
Johnstone, Timothy G. ;
Christiano, Romain ;
Mackowiak, Sebastian D. ;
Obermayer, Benedikt ;
Fleming, Elizabeth S. ;
Vejnar, Charles E. ;
Lee, Miler T. ;
Rajewsky, Nikolaus ;
Walther, Tobias C. ;
Giraldez, Antonio J. .
EMBO JOURNAL, 2014, 33 (09) :981-993
[4]   miR-31 modulates dystrophin expression: new implications for Duchenne muscular dystrophy therapy [J].
Cacchiarelli, Davide ;
Incitti, Tania ;
Martone, Julie ;
Cesana, Marcella ;
Cazzella, Valentina ;
Santini, Tiziana ;
Sthandier, Olga ;
Bozzoni, Irene .
EMBO REPORTS, 2011, 12 (02) :136-141
[5]   MicroRNAs Involved in Molecular Circuitries Relevant for the Duchenne Muscular Dystrophy Pathogenesis Are Controlled by the Dystrophin/nNOS Pathway [J].
Cacchiarelli, Davide ;
Martone, Julie ;
Girardi, Erika ;
Cesana, Marcella ;
Incitti, Tania ;
Morlando, Mariangela ;
Nicoletti, Carmine ;
Santini, Tiziana ;
Sthandier, Olga ;
Barberi, Laura ;
Auricchio, Alberto ;
Musaro, Antonio ;
Bozzoni, Irene .
CELL METABOLISM, 2010, 12 (04) :341-351
[6]   Exon 45 Skipping Through U1-snRNA Antisense Molecules Recovers the Dys-nNOS Pathway and Muscle Differentiation in Human DMD Myoblasts [J].
Cazzella, Valentina ;
Martone, Julie ;
Pinnaro, Chiara ;
Santini, Tiziana ;
Twayana, Shyam Sundar ;
Sthandier, Olga ;
D'Amico, Adele ;
Ricotti, Valeria ;
Bertini, Enrico ;
Muntoni, Francesco ;
Bozzoni, Irene .
MOLECULAR THERAPY, 2012, 20 (11) :2134-2142
[7]   A Long Noncoding RNA Controls Muscle Differentiation by Functioning as a Competing Endogenous RNA [J].
Cesana, Marcella ;
Cacchiarelli, Davide ;
Legnini, Ivano ;
Santini, Tiziana ;
Sthandier, Olga ;
Chinappi, Mauro ;
Tramontano, Anna ;
Bozzoni, Irene .
CELL, 2011, 147 (02) :358-369
[8]   Cellular and molecular regulation of muscle regeneration [J].
Chargé, SBP ;
Rudnicki, MA .
PHYSIOLOGICAL REVIEWS, 2004, 84 (01) :209-238
[9]   The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation [J].
Chen, JF ;
Mandel, EM ;
Thomson, JM ;
Wu, QL ;
Callis, TE ;
Hammond, SM ;
Conlon, FL ;
Wang, DZ .
NATURE GENETICS, 2006, 38 (02) :228-233
[10]   Muscle Satellite Cells Are Primed for Myogenesis but Maintain Quiescence with Sequestration of Myf5 mRNA Targeted by microRNA-31 in mRNP Granules [J].
Crist, Colin G. ;
Montarras, Didier ;
Buckingham, Margaret .
CELL STEM CELL, 2012, 11 (01) :118-126