Solution structure of an RNA fragment with the P7/P9.0 region and the 3′-terminal guanosine of the Tetrahymena group I intron

Aya Kitamura, Yutaka Muto, Satoru Watanabe, Insil Kim, Takuhiro Ito, Yoichi Nishiya, Kensaku Sakamoto, Takashi Ohtsuki, Gota Kawai, Kimitsuna Watanabe, Kazumi Hosono, Hiroshi Takaku, Etsuko Katoh, Toshimasa Yamazaki, Tan Inoue, Shigeyuki Yokoyama

Research output: Contribution to journalArticle

14 Citations (Scopus)

Abstract

In the second step of the two consecutive transesterifications of the self-splicing reaction of the group I intron, the conserved guanosine at the 3′ terminus of the intron (ωG) binds to the guanosine-binding site (GBS) in the intron. In the present study, we designed a 22-nt model RNA (GBS/ωG) including the GBS and ωG from the Tetrahymena group I intron, and determined the solution structure by NMR methods. In this structure, ωG is recognized by the formation of a base triple with the G264·C311 base pair, and this recognition is stabilized by the stacking interaction between ωG and C262. The bulged structure at A263 causes a large helical twist angle (40 ± 8°) between the G264·C311 and C262·G312 base pairs. We named this type of binding pocket with a bulge and a large twist, formed on the major groove, a "Bulge-and-Twist" (BT) pocket. With another twist angle between the C262·G312 and G413·C313 base pairs (45 ± 10°), the axis of GBS/ωG is kinked at the GBS region. This kinked axis superimposes well on that of the corresponding region in the structure model built on a 5.0 Å resolution electron density map (Golden et al., Science, 1998, 282:345-358). This compact structure of the GBS is also consistent with previous biochemical studies on group I introns. The BT pockets are also found in the arginine-binding site of the HIV-TAR RNA, and within the 16S rRNA and the 23S rRNA.

Original languageEnglish
Pages (from-to)440-451
Number of pages12
JournalRNA
Volume8
Issue number4
DOIs
Publication statusPublished - 2002
Externally publishedYes

Fingerprint

Tetrahymena
Guanosine
Introns
Binding Sites
RNA
Base Pairing
Arginine
HIV
Electrons

Keywords

  • NMR
  • Ribozyme
  • RNA structure
  • Self-splicing

ASJC Scopus subject areas

  • Genetics
  • Molecular Biology

Cite this

Solution structure of an RNA fragment with the P7/P9.0 region and the 3′-terminal guanosine of the Tetrahymena group I intron. / Kitamura, Aya; Muto, Yutaka; Watanabe, Satoru; Kim, Insil; Ito, Takuhiro; Nishiya, Yoichi; Sakamoto, Kensaku; Ohtsuki, Takashi; Kawai, Gota; Watanabe, Kimitsuna; Hosono, Kazumi; Takaku, Hiroshi; Katoh, Etsuko; Yamazaki, Toshimasa; Inoue, Tan; Yokoyama, Shigeyuki.

In: RNA, Vol. 8, No. 4, 2002, p. 440-451.

Research output: Contribution to journalArticle

Kitamura, A, Muto, Y, Watanabe, S, Kim, I, Ito, T, Nishiya, Y, Sakamoto, K, Ohtsuki, T, Kawai, G, Watanabe, K, Hosono, K, Takaku, H, Katoh, E, Yamazaki, T, Inoue, T & Yokoyama, S 2002, 'Solution structure of an RNA fragment with the P7/P9.0 region and the 3′-terminal guanosine of the Tetrahymena group I intron', RNA, vol. 8, no. 4, pp. 440-451. https://doi.org/10.1017/S1355838202026043
Kitamura, Aya ; Muto, Yutaka ; Watanabe, Satoru ; Kim, Insil ; Ito, Takuhiro ; Nishiya, Yoichi ; Sakamoto, Kensaku ; Ohtsuki, Takashi ; Kawai, Gota ; Watanabe, Kimitsuna ; Hosono, Kazumi ; Takaku, Hiroshi ; Katoh, Etsuko ; Yamazaki, Toshimasa ; Inoue, Tan ; Yokoyama, Shigeyuki. / Solution structure of an RNA fragment with the P7/P9.0 region and the 3′-terminal guanosine of the Tetrahymena group I intron. In: RNA. 2002 ; Vol. 8, No. 4. pp. 440-451.
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abstract = "In the second step of the two consecutive transesterifications of the self-splicing reaction of the group I intron, the conserved guanosine at the 3′ terminus of the intron (ωG) binds to the guanosine-binding site (GBS) in the intron. In the present study, we designed a 22-nt model RNA (GBS/ωG) including the GBS and ωG from the Tetrahymena group I intron, and determined the solution structure by NMR methods. In this structure, ωG is recognized by the formation of a base triple with the G264·C311 base pair, and this recognition is stabilized by the stacking interaction between ωG and C262. The bulged structure at A263 causes a large helical twist angle (40 ± 8°) between the G264·C311 and C262·G312 base pairs. We named this type of binding pocket with a bulge and a large twist, formed on the major groove, a {"}Bulge-and-Twist{"} (BT) pocket. With another twist angle between the C262·G312 and G413·C313 base pairs (45 ± 10°), the axis of GBS/ωG is kinked at the GBS region. This kinked axis superimposes well on that of the corresponding region in the structure model built on a 5.0 {\AA} resolution electron density map (Golden et al., Science, 1998, 282:345-358). This compact structure of the GBS is also consistent with previous biochemical studies on group I introns. The BT pockets are also found in the arginine-binding site of the HIV-TAR RNA, and within the 16S rRNA and the 23S rRNA.",
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T1 - Solution structure of an RNA fragment with the P7/P9.0 region and the 3′-terminal guanosine of the Tetrahymena group I intron

AU - Kitamura, Aya

AU - Muto, Yutaka

AU - Watanabe, Satoru

AU - Kim, Insil

AU - Ito, Takuhiro

AU - Nishiya, Yoichi

AU - Sakamoto, Kensaku

AU - Ohtsuki, Takashi

AU - Kawai, Gota

AU - Watanabe, Kimitsuna

AU - Hosono, Kazumi

AU - Takaku, Hiroshi

AU - Katoh, Etsuko

AU - Yamazaki, Toshimasa

AU - Inoue, Tan

AU - Yokoyama, Shigeyuki

PY - 2002

Y1 - 2002

N2 - In the second step of the two consecutive transesterifications of the self-splicing reaction of the group I intron, the conserved guanosine at the 3′ terminus of the intron (ωG) binds to the guanosine-binding site (GBS) in the intron. In the present study, we designed a 22-nt model RNA (GBS/ωG) including the GBS and ωG from the Tetrahymena group I intron, and determined the solution structure by NMR methods. In this structure, ωG is recognized by the formation of a base triple with the G264·C311 base pair, and this recognition is stabilized by the stacking interaction between ωG and C262. The bulged structure at A263 causes a large helical twist angle (40 ± 8°) between the G264·C311 and C262·G312 base pairs. We named this type of binding pocket with a bulge and a large twist, formed on the major groove, a "Bulge-and-Twist" (BT) pocket. With another twist angle between the C262·G312 and G413·C313 base pairs (45 ± 10°), the axis of GBS/ωG is kinked at the GBS region. This kinked axis superimposes well on that of the corresponding region in the structure model built on a 5.0 Å resolution electron density map (Golden et al., Science, 1998, 282:345-358). This compact structure of the GBS is also consistent with previous biochemical studies on group I introns. The BT pockets are also found in the arginine-binding site of the HIV-TAR RNA, and within the 16S rRNA and the 23S rRNA.

AB - In the second step of the two consecutive transesterifications of the self-splicing reaction of the group I intron, the conserved guanosine at the 3′ terminus of the intron (ωG) binds to the guanosine-binding site (GBS) in the intron. In the present study, we designed a 22-nt model RNA (GBS/ωG) including the GBS and ωG from the Tetrahymena group I intron, and determined the solution structure by NMR methods. In this structure, ωG is recognized by the formation of a base triple with the G264·C311 base pair, and this recognition is stabilized by the stacking interaction between ωG and C262. The bulged structure at A263 causes a large helical twist angle (40 ± 8°) between the G264·C311 and C262·G312 base pairs. We named this type of binding pocket with a bulge and a large twist, formed on the major groove, a "Bulge-and-Twist" (BT) pocket. With another twist angle between the C262·G312 and G413·C313 base pairs (45 ± 10°), the axis of GBS/ωG is kinked at the GBS region. This kinked axis superimposes well on that of the corresponding region in the structure model built on a 5.0 Å resolution electron density map (Golden et al., Science, 1998, 282:345-358). This compact structure of the GBS is also consistent with previous biochemical studies on group I introns. The BT pockets are also found in the arginine-binding site of the HIV-TAR RNA, and within the 16S rRNA and the 23S rRNA.

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KW - Ribozyme

KW - RNA structure

KW - Self-splicing

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