Modulation of pre-mRNA structure by hnRNP proteins regulates alternative splicing of MALT1

被引:25
作者
Jones, Alisha N. [1 ,2 ]
Grass, Carina [3 ]
Meininger, Isabel [3 ]
Geerlof, Arie [1 ]
Klostermann, Melina [4 ,5 ]
Zarnack, Kathi [4 ,5 ]
Krappmann, Daniel [3 ]
Sattler, Michael [1 ,2 ]
机构
[1] Helmholtz Zentrum Munchen, Inst Struct Biol, Mol Targets & Therapeut Ctr, D-85764 Munich, Germany
[2] Tech Univ Munich, Bavarian NMR Ctr, Dept Chem, D-85748 Munich, Germany
[3] Helmholtz Zentrum Munchen, Inst Mol Toxicol & Pharmacol, Res Unit Cellular Signal Integrat, Mol Targets & Therapeut Ctr, D-85764 Munich, Germany
[4] Goethe Univ Frankfurt, Buchmann Inst Mol Life Sci BMLS, Max Laue Str 15, D-60438 Frankfurt, Germany
[5] Goethe Univ Frankfurt, Fac Biol Sci, Max Von Laue Str 15, D-60438 Frankfurt, Germany
关键词
SELECTIVE 2'-HYDROXYL ACYLATION; SECONDARY STRUCTURE; NMR-SPECTROSCOPY; BINDING; MECHANISMS; MOTIF; SITE; RECOGNITION; ACTIVATION; INSIGHTS;
D O I
10.1126/sciadv.abp9153
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
Alternative splicing plays key roles for cell type-specific regulation of protein function. It is controlled by cis-regulatory RNA elements that are recognized by RNA binding proteins (RBPs). The MALT1 paracaspase is a key factor of signaling pathways that mediate innate and adaptive immune responses. Alternative splicing of MALT1 is critical for controlling optimal T cell activation. We demonstrate that MALT1 splicing depends on RNA structural elements that sequester the splice sites of the alternatively spliced exon7. The RBPs hnRNP U and hnRNP L bind competitively to stem-loop RNA structures that involve the 5' and 3' splice sites flanking exon7. While hnRNP U stabilizes RNA stem-loop conformations that maintain exon7 skipping, hnRNP L disrupts these RNA elements to facilitate recruitment of the essential splicing factor U2AF2, thereby promoting exon7 inclusion. Our data represent a paradigm for the control of splice site selection by differential RBP binding and modulation of pre-mRNA structure.
引用
收藏
页数:14
相关论文
共 70 条
[31]   RNA structure and the mechanisms of alternative splicing [J].
McManus, C. Joel ;
Graveley, Brenton R. .
CURRENT OPINION IN GENETICS & DEVELOPMENT, 2011, 21 (04) :373-379
[32]   Alternative splicing of MALT1 controls signalling and activation of CD4+ T cells [J].
Meininger, Isabel ;
Griesbach, Richard A. ;
Hu, Desheng ;
Gehring, Torben ;
Seeholzer, Thomas ;
Bertossi, Arianna ;
Kranich, Jan ;
Oeckinghaus, Andrea ;
Eitelhuber, Andrea C. ;
Greczmiel, Ute ;
Gewies, Andreas ;
Schmidt-Supprian, Marc ;
Ruland, Juergen ;
Brocker, Thomas ;
Heissmeyer, Vigo ;
Heyd, Florian ;
Krappmann, Daniel .
NATURE COMMUNICATIONS, 2016, 7
[33]   RNA structure analysis at single nucleotide resolution by selective 2′-hydroxyl acylation and primer extension (SHAPE) [J].
Merino, EJ ;
Wilkinson, KA ;
Coughlan, JL ;
Weeks, KM .
JOURNAL OF THE AMERICAN CHEMICAL SOCIETY, 2005, 127 (12) :4223-4231
[34]   Expansion of the eukaryotic proteome by alternative splicing [J].
Nilsen, Timothy W. ;
Graveley, Brenton R. .
NATURE, 2010, 463 (7280) :457-463
[35]   A novel TRAF6 binding site in MALT1 defines distinct mechanisms of NF-κB activation by API2•MALT1 fusions [J].
Noels, Heidi ;
van Loo, Geert ;
Hagens, Sofie ;
Broeckx, Vicky ;
Beyaert, Rudi ;
Marynen, Peter ;
Baens, Mathijs .
JOURNAL OF BIOLOGICAL CHEMISTRY, 2007, 282 (14) :10180-10189
[36]   3S: Shotgun secondary structure determination of long non-coding RNAs [J].
Novikova, Irina V. ;
Dharap, Ashutosh ;
Hennelly, Scott P. ;
Sanbonmatsu, Karissa Y. .
METHODS, 2013, 63 (02) :170-177
[37]   TRAF6 prevents fatal inflammation by homeostatic suppression of MALT1 protease [J].
O'Neill, Thomas J. ;
Seeholzer, Thomas ;
Gewies, Andreas ;
Gehring, Torben ;
Giesert, Florian ;
Hamp, Isabel ;
Grass, Carina ;
Schmidt, Henrik ;
Kriegsmann, Katharina ;
Tofaute, Marie J. ;
Demski, Katrin ;
Poth, Tanja ;
Rosenbaum, Marc ;
Schnalzger, Theresa ;
Ruland, Juergen ;
Goettlicher, Martin ;
Kriegsmann, Mark ;
Naumann, Ronald ;
Heissmeyer, Vigo ;
Plettenburg, Oliver ;
Wurst, Wolfgang ;
Krappmann, Daniel .
SCIENCE IMMUNOLOGY, 2021, 6 (65)
[38]   Structure of PTB bound to RNA: Specific binding and implications for splicing regulation [J].
Oberstrass, FC ;
Auweter, SD ;
Erat, M ;
Hargous, Y ;
Henning, A ;
Wenter, P ;
Reymond, L ;
Amir-Ahmady, B ;
Pitsch, S ;
Black, DL ;
Allain, FHT .
SCIENCE, 2005, 309 (5743) :2054-2057
[39]   Intrinsically disordered RGG/RG domains mediate degenerate specificity in RNA binding [J].
Ozdilek, Bagdeser A. ;
Thompson, Valery F. ;
Ahmed, Nasiha S. ;
White, Connor I. ;
Batey, Robert T. ;
Schwartz, Jacob C. .
NUCLEIC ACIDS RESEARCH, 2017, 45 (13) :7984-7996
[40]   SR proteins: a foot on the exon before the transition from intron to exon definition [J].
Ram, Oren ;
Ast, Gil .
TRENDS IN GENETICS, 2007, 23 (01) :5-7