Dual Role for the RNA-binding Domain of Xenopus Laevis SLBP1 in Histone Pre-mRNA Processing

Overview

Journal RNA

Specialty Molecular Biology

Date 2000 Dec 6

PMID 11105762

Citations 12

Authors

T C Ingledue 3rd

Z Dominski

R Sanchez

J A Erkmann

W F Marzluff

Affiliations

Soon will be listed here.

Abstract

The replication-dependent histone mRNAs end in a conserved 26-nt sequence that forms a stem-loop structure. This sequence is required for histone pre-mRNA processing and plays a role in multiple aspects of histone mRNA metabolism. Two proteins that bind the 3' end of histone mRNA are found in Xenopus oocytes. xSLBP1 is found in the nucleus, where it functions in histone pre-mRNA processing, and in the cytoplasm, where it may control histone mRNA translation and stability. xSLBP2 is a cytoplasmic protein, inactive in histone pre-mRNA processing, whose expression is restricted to oogenesis and early development. These proteins are similar only in their RNA-binding domains (RBD). A chimeric protein (1-2-1) in which the RBD of xSLBP1 has been replaced with the RBD of xSLBP2 binds the stem-loop with an affinity similar to the original protein. The 1-2-1 protein efficiently localizes to the nucleus of the frog oocyte, but is not active in processing of histone pre-mRNA in vivo. This protein does not support processing in a nuclear extract, but inhibits processing by competing with the active SLBP by binding to the substrate. The 1-2-1 protein also inhibits processing of synthetic histone pre-mRNA injected into frog oocytes, but has no effect on processing of histone pre-mRNA transcribed from an injected histone gene. This result suggests that sequences in the RBD of xSLBP1 give it preferential access to histone pre-mRNA transcribed in vivo.

Citing Articles

U7 snRNP is recruited to histone pre-mRNA in a FLASH-dependent manner by two separate regions of the stem-loop binding protein.

Skrajna A, Yang X, Bucholc K, Zhang J, Hall T, Dadlez M RNA. 2017; 23(6):938-951.

PMID: 28289156 PMC: 5435866. DOI: 10.1261/rna.060806.117.

SLIP1, a factor required for activation of histone mRNA translation by the stem-loop binding protein.

Cakmakci N, Lerner R, Wagner E, Zheng L, Marzluff W Mol Cell Biol. 2007; 28(3):1182-94.

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Formation of the 3' end of histone mRNA: getting closer to the end.

Dominski Z, Marzluff W Gene. 2007; 396(2):373-90.

PMID: 17531405 PMC: 2888136. DOI: 10.1016/j.gene.2007.04.021.

Nuclear export of metazoan replication-dependent histone mRNAs is dependent on RNA length and is mediated by TAP.

Erkmann J, Sanchez R, Treichel N, Marzluff W, Kutay U RNA. 2004; 11(1):45-58.

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The oligo(A) tail on histone mRNA plays an active role in translational silencing of histone mRNA during Xenopus oogenesis.

Sanchez R, Marzluff W Mol Cell Biol. 2004; 24(6):2513-25.

PMID: 14993288 PMC: 355835. DOI: 10.1128/MCB.24.6.2513-2525.2004.

References

Frey M, Matera A . Coiled bodies contain U7 small nuclear RNA and associate with specific DNA sequences in interphase human cells. Proc Natl Acad Sci U S A. 1995; 92(13):5915-9. PMC: 41612. DOI: 10.1073/pnas.92.13.5915. View

Pandey N, Williams A, Sun J, Brown V, Bond U, Marzluff W . Point mutations in the stem-loop at the 3' end of mouse histone mRNA reduce expression by reducing the efficiency of 3' end formation. Mol Cell Biol. 1994; 14(3):1709-20. PMC: 358529. DOI: 10.1128/mcb.14.3.1709-1720.1994. View

Cho D, Scharl E, Steitz J . Decreasing the distance between the two conserved sequence elements of histone pre-messenger RNA interferes with 3' processing in vitro. RNA. 1995; 1(9):905-14. PMC: 1369339. View

Dominski Z, Sumerel J, Hanson R, Marzluff W . The polyribosomal protein bound to the 3' end of histone mRNA can function in histone pre-mRNA processing. RNA. 1995; 1(9):915-23. PMC: 1369340. View

Hanson R, Sun J, Willis D, Marzluff W . Efficient extraction and partial purification of the polyribosome-associated stem-loop binding protein bound to the 3' end of histone mRNA. Biochemistry. 1996; 35(7):2146-56. DOI: 10.1021/bi9521856. View

Gallie D, Lewis N, Marzluff W . The histone 3'-terminal stem-loop is necessary for translation in Chinese hamster ovary cells. Nucleic Acids Res. 1996; 24(10):1954-62. PMC: 145863. DOI: 10.1093/nar/24.10.1954. View

Wu C, Murphy C, Gall J . The Sm binding site targets U7 snRNA to coiled bodies (spheres) of amphibian oocytes. RNA. 1996; 2(8):811-23. PMC: 1369417. View

Wang Z, Krasikov T, Frey M, Wang J, Matera A, Marzluff W . Characterization of the mouse histone gene cluster on chromosome 13: 45 histone genes in three patches spread over 1Mb. Genome Res. 1996; 6(8):688-701. DOI: 10.1101/gr.6.8.688. View

Wang Z, Tisovec R, Debry R, Frey M, Matera A, Marzluff W . Characterization of the 55-kb mouse histone gene cluster on chromosome 3. Genome Res. 1996; 6(8):702-14. DOI: 10.1101/gr.6.8.702. View

10.

Meric F, Searfoss A, Wormington M, Wolffe A . Masking and unmasking maternal mRNA. The role of polyadenylation, transcription, splicing, and nuclear history. J Biol Chem. 1996; 271(48):30804-10. DOI: 10.1074/jbc.271.48.30804. View

11.

Longo F, Mathews L, Gururajan R, Chen J, Weeks D . Changes in nuclear localization of An3, a RNA helicase, during oogenesis and embryogenesis in Xenopus laevis. Mol Reprod Dev. 1996; 45(4):491-502. DOI: 10.1002/(SICI)1098-2795(199612)45:4<491::AID-MRD12>3.0.CO;2-#. View

12.

Wang Z, Whitfield M, Ingledue 3rd T, Dominski Z, Marzluff W . The protein that binds the 3' end of histone mRNA: a novel RNA-binding protein required for histone pre-mRNA processing. Genes Dev. 1996; 10(23):3028-40. DOI: 10.1101/gad.10.23.3028. View

13.

Scharl E, Steitz J . Length suppression in histone messenger RNA 3'-end maturation: processing defects of insertion mutant premessenger RNAs can be compensated by insertions into the U7 small nuclear RNA. Proc Natl Acad Sci U S A. 1996; 93(25):14659-64. PMC: 26191. DOI: 10.1073/pnas.93.25.14659. View

14.

McCracken S, Fong N, Yankulov K, Ballantyne S, Pan G, GREENBLATT J . The C-terminal domain of RNA polymerase II couples mRNA processing to transcription. Nature. 1997; 385(6614):357-61. DOI: 10.1038/385357a0. View

15.

Martin F, Schaller A, Eglite S, Schumperli D, Muller B . The gene for histone RNA hairpin binding protein is located on human chromosome 4 and encodes a novel type of RNA binding protein. EMBO J. 1997; 16(4):769-78. PMC: 1169678. DOI: 10.1093/emboj/16.4.769. View

16.

Matsumoto K, Wassarman K, Wolffe A . Nuclear history of a pre-mRNA determines the translational activity of cytoplasmic mRNA. EMBO J. 1998; 17(7):2107-21. PMC: 1170555. DOI: 10.1093/emboj/17.7.2107. View

17.

Bellini M, Gall J . Coilin can form a complex with the U7 small nuclear ribonucleoprotein. Mol Biol Cell. 1998; 9(10):2987-3001. PMC: 25576. DOI: 10.1091/mbc.9.10.2987. View

18.

Wang Z, Ingledue T, Dominski Z, Sanchez R, Marzluff W . Two Xenopus proteins that bind the 3' end of histone mRNA: implications for translational control of histone synthesis during oogenesis. Mol Cell Biol. 1998; 19(1):835-45. PMC: 83940. DOI: 10.1128/MCB.19.1.835. View

19.

Abbott J, Marzluff W, Gall J . The stem-loop binding protein (SLBP1) is present in coiled bodies of the Xenopus germinal vesicle. Mol Biol Cell. 1999; 10(2):487-99. PMC: 25182. DOI: 10.1091/mbc.10.2.487. View

20.

Dominski Z, Zheng L, Sanchez R, Marzluff W . Stem-loop binding protein facilitates 3'-end formation by stabilizing U7 snRNP binding to histone pre-mRNA. Mol Cell Biol. 1999; 19(5):3561-70. PMC: 84148. DOI: 10.1128/MCB.19.5.3561. View