Home LiteratureArticle Details
PMID: 9848652 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

A polysomal ribonuclease involved in the destabilization of albumin mRNA is a novel member of the peroxidase gene family.

RNA (New York, N.Y.) ·Vol. 4 ·No. 12 ·1998-12-00 ·Pages 1537-48

Chernokalskaya E, Dubell AN, Cunningham KS, Hanson MN, Dompenciel RE, Schoenberg DR

Abstract

We have purified an approximately 60 kDa endoribonuclease from Xenopus liver polysomes with properties expected for a messenger RNase involved in the estrogen-regulated destabilization of serum protein mRNAs (Dompenciel et al., 1995, J Biol Chem 270:6108-6118). The present report describes the cloning of this protein and its identification as a novel member of the peroxidase gene family. This novel enzyme, named polysomal RNase 1, or PMR-1 has 57% sequence identity with myeloperoxidase, and like that protein, appears to be processed from a larger precursor. Unlike myeloperoxidase, however, PMR-1 lacks N-linked oligosaccharide, heme, and peroxidase activity. Western blot and immunoprecipitation experiments using epitope-specific antibodies to the derived protein sequence confirm the identity of the cloned cDNA to the protein originally isolated from polysomes. The 80 kDa pre-PMR-1 expressed in a recombinant baculovirus was not processed to the 60 kDa form in Sf9 cells and lacks RNase activity. However, the baculovirus-expressed mature 60-kDa form of the enzyme has RNase activity. The recombinant protein is an endonuclease that shows selectivity for albumin versus ferritin mRNA. While it does not cleave at consensus APyrUGA elements, recombinant PMR-1 generates the same minor cleavage products from albumin mRNA as PMR-1 purified from liver. Finally, we show estrogen induces only a small increase in the amount of PMR-1. This result is consistent with earlier data suggesting estrogen activates mRNA decay through a posttranslational pathway.

MeSH Terms
Albumins/genetics Amino Acid Sequence Base Sequence Endoribonucleases/genetics,metabolism Estrogens/physiology Gene Expression Regulation, Enzymologic/physiology Liver/enzymology Molecular Sequence Data Multigene Family Peroxidases/metabolism RNA, Messenger/genetics,metabolism Recombinant Proteins/metabolism Sequence Homology, Amino Acid
Chemicals
Albumins Estrogens RNA, Messenger Recombinant Proteins Peroxidases Endoribonucleases polysomal RNase 1
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Chernokalskaya E
Department of Pharmacology and the Comprehensive Cancer Center, Ohio State University, Columbus 43210-1239, USA.
Dubell A N
Cunningham K S
Hanson M N
Dompenciel R E
Schoenberg D R
References (38)
38 references, click to expand
  1. Sequence-specific endonucleolytic cleavage and protection of mRNA in Xenopus and Drosophila.
    Genes Dev. 1993 Aug;7(8):1620-31 PMID: 8339937
  2. Unique autolytic cleavage of human myeloperoxidase. Implications for the involvement of active site MET409.
    J Biol Chem. 1992 Dec 15;267(35):25282-8 PMID: 1334087
  3. Mutational analysis of the [4Fe-4S]-cluster converting iron regulatory factor from its RNA-binding form to cytoplasmic aconitase.
    EMBO J. 1994 Jan 15;13(2):453-61 PMID: 7508861
  4. Purification and properties of a protein that binds to the C-terminal coding region of human c-myc mRNA.
    J Biol Chem. 1994 Mar 25;269(12):9261-9 PMID: 8132663
  5. Evidence that the pathway of transferrin receptor mRNA degradation involves an endonucleolytic cleavage within the 3' UTR and does not involve poly(A) tail shortening.
    EMBO J. 1994 Apr 15;13(8):1969-80 PMID: 7909515
  6. Iron regulatory protein prevents binding of the 43S translation pre-initiation complex to ferritin and eALAS mRNAs.
    EMBO J. 1994 Aug 15;13(16):3882-91 PMID: 8070415
  7. Estrogen action via the cAMP signaling pathway: stimulation of adenylate cyclase and cAMP-regulated gene transcription.
    Proc Natl Acad Sci U S A. 1994 Aug 30;91(18):8517-21 PMID: 8078914
  8. Purification of a human polyribosome-associated 3' to 5' exoribonuclease.
    J Biol Chem. 1994 Dec 16;269(50):31814-21 PMID: 7989354
  9. A guanosine quadruplex and two stable hairpins flank a major cleavage site in insulin-like growth factor II mRNA.
    Nucleic Acids Res. 1994 Dec 25;22(25):5709-16 PMID: 7838726
  10. Structure of the green heme in myeloperoxidase.
    Arch Biochem Biophys. 1995 Jan 10;316(1):653-6 PMID: 7840679
  11. Glyceraldehyde-3-phosphate dehydrogenase selectively binds AU-rich RNA in the NAD(+)-binding region (Rossmann fold).
    J Biol Chem. 1995 Feb 10;270(6):2755-63 PMID: 7531693
  12. Purification and characterization of an estrogen-regulated Xenopus liver polysomal nuclease involved in the selective destabilization of albumin mRNA.
    J Biol Chem. 1995 Mar 17;270(11):6108-18 PMID: 7890744
  13. AUH, a gene encoding an AU-specific RNA binding protein with intrinsic enoyl-CoA hydratase activity.
    Proc Natl Acad Sci U S A. 1995 Mar 14;92(6):2051-5 PMID: 7892223
  14. The mRNA-binding protein COLBP is glutamate dehydrogenase.
    FEBS Lett. 1995 Jul 3;367(3):291-6 PMID: 7607326
  15. mRNA stability in mammalian cells.
    Microbiol Rev. 1995 Sep;59(3):423-50 PMID: 7565413
  16. The cis-acting elements involved in endonucleolytic cleavage of the 3' UTR of human IGF-II mRNAs bind a 50 kDa protein.
    Nucleic Acids Res. 1996 Mar 15;24(6):1000-7 PMID: 8604329
  17. Tyrosine kinase/p21ras/MAP-kinase pathway activation by estradiol-receptor complex in MCF-7 cells.
    EMBO J. 1996 Mar 15;15(6):1292-300 PMID: 8635462
  18. Spectral analysis of lactoperoxidase. Evidence for a common heme in mammalian peroxidases.
    J Biol Chem. 1996 Feb 16;271(7):3406-12 PMID: 8631940
  19. ProMod and Swiss-Model: Internet-based tools for automated comparative protein modelling.
    Biochem Soc Trans. 1996 Feb;24(1):274-9 PMID: 8674685
  20. Cleavage properties of an estrogen-regulated polysomal ribonuclease involved in the destabilization of albumin mRNA.
    Nucleic Acids Res. 1997 Feb 15;25(4):735-42 PMID: 9016622
  21. A mouse cytoplasmic exoribonuclease (mXRN1p) with preference for G4 tetraplex substrates.
    J Cell Biol. 1997 Feb 24;136(4):761-73 PMID: 9049243
  22. Poly(A) tail shortening by a mammalian poly(A)-specific 3'-exoribonuclease.
    J Biol Chem. 1997 Apr 18;272(16):10448-56 PMID: 9099687
  23. Messenger RNA deadenylylation precedes decapping in mammalian cells.
    Proc Natl Acad Sci U S A. 1997 May 27;94(11):5628-33 PMID: 9159123
  24. Estrogen stabilizes vitellogenin mRNA against cytoplasmic degradation.
    Cell. 1983 Aug;34(1):207-14 PMID: 6192932
  25. H4 histone messenger RNA decay in cell-free extracts initiates at or near the 3' terminus and proceeds 3' to 5'.
    J Mol Biol. 1986 Apr 20;188(4):579-93 PMID: 3525849
  26. Posttranscriptional regulation of albumin gene expression in Xenopus liver: evidence for an estrogen receptor-dependent mechanism.
    Mol Endocrinol. 1987 Feb;1(2):160-7 PMID: 3454873
  27. Extranuclear estrogen-regulated destabilization of Xenopus laevis serum albumin mRNA.
    Mol Endocrinol. 1989 May;3(5):805-14 PMID: 2547154
  28. Estrogen regulation of gene transcription and mRNA stability.
    Recent Prog Horm Res. 1989;45:29-58; discussion 58-64 PMID: 2682843
  29. Estrogen-induced destabilization and associated degradation intermediates of apolipoprotein II mRNA.
    Prog Clin Biol Res. 1990;322:227-40 PMID: 2304937
  30. Endonucleolytic cleavage of a maternal homeo box mRNA in Xenopus oocytes.
    Genes Dev. 1990 Nov;4(11):1925-35 PMID: 1980477
  31. The estrogen-regulated destabilization of Xenopus albumin mRNA is independent of translation.
    Biochem Biophys Res Commun. 1991 Jan 31;174(2):825-30 PMID: 1993075
  32. In vitro deadenylation of mammalian mRNA by a HeLa cell 3' exonuclease.
    EMBO J. 1991 Oct;10(10):3067-71 PMID: 1717259
  33. Coordinate estrogen-regulated instability of serum protein-coding messenger RNAs in Xenopus laevis.
    Mol Endocrinol. 1991 Apr;5(4):461-8 PMID: 1922078
  34. Estrogen-induced ribonuclease activity in Xenopus liver.
    Biochemistry. 1991 Oct 29;30(43):10490-8 PMID: 1931972
  35. Removal of a 3' non-coding sequence is an initial step in degradation of gro alpha mRNA and is regulated by interleukin-1.
    Nucleic Acids Res. 1992 Mar 11;20(5):1123-7 PMID: 1549476
  36. The rate-limiting step in yeast PGK1 mRNA degradation is an endonucleolytic cleavage in the 3'-terminal part of the coding region.
    Mol Cell Biol. 1992 Jul;12(7):2986-96 PMID: 1320194
  37. Properties of a HeLa cell 3' exonuclease specific for degrading poly(A) tails of mammalian mRNA.
    J Biol Chem. 1992 Sep 5;267(25):18154-9 PMID: 1355481
  38. The nuclease that selectively degrades albumin mRNA in vitro associates with Xenopus liver polysomes through the 80S ribosome complex.
    Arch Biochem Biophys. 1993 Sep;305(2):313-9 PMID: 8373169
Article Info
Journal
RNA (New York, N.Y.)
Abbr.
RNA
ISSN
1355-8382
Published
1998-12-00
Pages
1537-48
Language
English
Region
United States
NLM ID
9509184
PMCID
PMC1369724
Subset
IM
Grants
NIGMS NIH HHS · F32 GM19350 · United States
NIGMS NIH HHS · R01 GM38277 · United States
Databases
GENBANK
U68724
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]