Crystal structure of group II intron domain 1 reveals a template for RNA assembly

Zhao, Chen; Rajashankar, Kanagalaghatta R.; Marcia, Marco; Pyle, Anna Marie

doi:10.1038/nchembio.1949

Title: Crystal structure of group II intron domain 1 reveals a template for RNA assembly

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Abstract

Although the importance of large noncoding RNAs is increasingly appreciated, our understanding of their structures and architectural dynamics remains limited. In particular, we know little about RNA folding intermediates and how they facilitate the productive assembly of RNA tertiary structures. In this paper, we report the crystal structure of an obligate intermediate that is required during the earliest stages of group II intron folding. Composed of domain 1 from the Oceanobacillus iheyensis group II intron (266 nucleotides), this intermediate retains native-like features but adopts a compact conformation in which the active site cleft is closed. Transition between this closed and the open (native) conformation is achieved through discrete rotations of hinge motifs in two regions of the molecule. Finally, the open state is then stabilized by sequential docking of downstream intron domains, suggesting a 'first come, first folded' strategy that may represent a generalizable pathway for assembly of large RNA and ribonucleoprotein structures.

Authors:

Zhao, Chen ^[1]; Rajashankar, Kanagalaghatta R. ^[2];

^[3]; Pyle, Anna Marie ^[4]

Yale Univ., New Haven, CT (United States). Dept. of Molecular Biophysics and Biochemistry
Argonne National Lab. (ANL), Argonne, IL (United States). Northeastern Collaborative Access Team (NE-CAT); Cornell Univ., Ithaca, NY (United States). Dept. of Chemistry and Chemical Biology
Yale Univ., New Haven, CT (United States). Dept. of Molecular, Cellular, and Developmental Biology
Yale Univ., New Haven, CT (United States). Dept. of Molecular, Cellular, and Developmental Biology. Dept. of Chemistry; Howard Hughes Medical Inst., Chevy Chase, MD (United States)

Publication Date:: Mon Oct 26 00:00:00 EDT 2015

Research Org.:: Yale Univ., New Haven, CT (United States); Argonne National Lab. (ANL), Argonne, IL (United States)

Sponsoring Org.:: USDOE Office of Science (SC); National Inst. of Health (NIH) (United States)

Contributing Org.:: Howard Hughes Medical Inst., Chevy Chase, MD (United States); Cornell Univ., Ithaca, NY (United States)

OSTI Identifier:: 1227028

Grant/Contract Number:: AC02-06CH11357; RO1GM50313; P41 GM103403; S10 RR029205

Resource Type:: Accepted Manuscript

Journal Name:: Nature Chemical Biology

Additional Journal Information:: Journal Volume: 11; Journal Issue: 12; Journal ID: ISSN 1552-4450

Publisher:: Nature Publishing Group

Country of Publication:: United States

Language:: ENGLISH

Subject:: 59 BASIC BIOLOGICAL SCIENCES; 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; Biochemistry; Ribozymes; RNA; X-ray crystallography

Citation Formats


                    Zhao, Chen, Rajashankar, Kanagalaghatta R., Marcia, Marco, and Pyle, Anna Marie. Crystal structure of group II intron domain 1 reveals a template for RNA assembly.  United States: N. p., 2015. 
Web.  doi:10.1038/nchembio.1949.

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                    Zhao, Chen, Rajashankar, Kanagalaghatta R., Marcia, Marco, & Pyle, Anna Marie. Crystal structure of group II intron domain 1 reveals a template for RNA assembly.  United States.  https://doi.org/10.1038/nchembio.1949

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                    Zhao, Chen, Rajashankar, Kanagalaghatta R., Marcia, Marco, and Pyle, Anna Marie. Mon .  
"Crystal structure of group II intron domain 1 reveals a template for RNA assembly".  United States.  https://doi.org/10.1038/nchembio.1949.  https://www.osti.gov/servlets/purl/1227028.

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@article{osti_1227028,

  title        = {Crystal structure of group II intron domain 1 reveals a template for RNA assembly},

  author       = {Zhao, Chen and Rajashankar, Kanagalaghatta R. and Marcia, Marco and Pyle, Anna Marie},

  abstractNote = {Although the importance of large noncoding RNAs is increasingly appreciated, our understanding of their structures and architectural dynamics remains limited. In particular, we know little about RNA folding intermediates and how they facilitate the productive assembly of RNA tertiary structures. In this paper, we report the crystal structure of an obligate intermediate that is required during the earliest stages of group II intron folding. Composed of domain 1 from the Oceanobacillus iheyensis group II intron (266 nucleotides), this intermediate retains native-like features but adopts a compact conformation in which the active site cleft is closed. Transition between this closed and the open (native) conformation is achieved through discrete rotations of hinge motifs in two regions of the molecule. Finally, the open state is then stabilized by sequential docking of downstream intron domains, suggesting a 'first come, first folded' strategy that may represent a generalizable pathway for assembly of large RNA and ribonucleoprotein structures.},

  doi          = {10.1038/nchembio.1949},

  journal      = {Nature Chemical Biology},

  number       = 12,

  volume       = 11,

  place        = {United States},

  year         = {Mon Oct 26 00:00:00 EDT 2015},

  month        = {Mon Oct 26 00:00:00 EDT 2015}

}

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