• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of rnaThe RNA SocietyeTOC AlertsSubscriptionsJournal HomeCSHL PressRNA
RNA. Dec 1998; 4(12): 1537–1548.
PMCID: PMC1369724

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

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.

Full Text

The Full Text of this article is available as a PDF (1.0M).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Dompenciel RE, Garnepudi VR, Schoenberg DR. 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):6108–6118. [PubMed]
  • Andersson LA, Bylkas SA, Wilson AE. Spectral analysis of lactoperoxidase. Evidence for a common heme in mammalian peroxidases. J Biol Chem. 1996 Feb 16;271(7):3406–3412. [PubMed]
  • Aronica SM, Kraus WL, Katzenellenbogen BS. 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):8517–8521. [PMC free article] [PubMed]
  • Aström J, Aström A, Virtanen A. Properties of a HeLa cell 3' exonuclease specific for degrading poly(A) tails of mammalian mRNA. J Biol Chem. 1992 Sep 5;267(25):18154–18159. [PubMed]
  • Aström J, Aström A, Virtanen A. In vitro deadenylation of mammalian mRNA by a HeLa cell 3' exonuclease. EMBO J. 1991 Oct;10(10):3067–3071. [PMC free article] [PubMed]
  • Bashkirov VI, Scherthan H, Solinger JA, Buerstedde JM, Heyer WD. A mouse cytoplasmic exoribonuclease (mXRN1p) with preference for G4 tetraplex substrates. J Cell Biol. 1997 Feb 24;136(4):761–773. [PMC free article] [PubMed]
  • Binder R, Gordon DA, Hwang SP, Williams DL. Estrogen-induced destabilization and associated degradation intermediates of apolipoprotein II mRNA. Prog Clin Biol Res. 1990;322:227–240. [PubMed]
  • Binder R, Horowitz JA, Basilion JP, Koeller DM, Klausner RD, Harford JB. 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):1969–1980. [PMC free article] [PubMed]
  • Brock ML, Shapiro DJ. Estrogen stabilizes vitellogenin mRNA against cytoplasmic degradation. Cell. 1983 Aug;34(1):207–214. [PubMed]
  • Brown BD, Harland RM. Endonucleolytic cleavage of a maternal homeo box mRNA in Xenopus oocytes. Genes Dev. 1990 Nov;4(11):1925–1935. [PubMed]
  • Brown BD, Zipkin ID, Harland RM. Sequence-specific endonucleolytic cleavage and protection of mRNA in Xenopus and Drosophila. Genes Dev. 1993 Aug;7(8):1620–1631. [PubMed]
  • Caruccio N, Ross J. Purification of a human polyribosome-associated 3' to 5' exoribonuclease. J Biol Chem. 1994 Dec 16;269(50):31814–31821. [PubMed]
  • Chernokalskaya E, Dompenciel R, Schoenberg DR. Cleavage properties of an estrogen-regulated polysomal ribonuclease involved in the destabilization of albumin mRNA. Nucleic Acids Res. 1997 Feb 15;25(4):735–742. [PMC free article] [PubMed]
  • Christiansen J, Kofod M, Nielsen FC. 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):5709–5716. [PMC free article] [PubMed]
  • Couttet P, Fromont-Racine M, Steel D, Pictet R, Grange T. Messenger RNA deadenylylation precedes decapping in mammalian cells. Proc Natl Acad Sci U S A. 1997 May 27;94(11):5628–5633. [PMC free article] [PubMed]
  • Dompenciel RE, Garnepudi VR, Schoenberg DR. 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):6108–6118. [PubMed]
  • Fenna R, Zeng J, Davey C. Structure of the green heme in myeloperoxidase. Arch Biochem Biophys. 1995 Jan 10;316(1):653–656. [PubMed]
  • Gray NK, Hentze MW. Iron regulatory protein prevents binding of the 43S translation pre-initiation complex to ferritin and eALAS mRNAs. EMBO J. 1994 Aug 15;13(16):3882–3891. [PMC free article] [PubMed]
  • Hirling H, Henderson BR, Kühn LC. 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):453–461. [PMC free article] [PubMed]
  • Körner CG, Wahle E. Poly(A) tail shortening by a mammalian poly(A)-specific 3'-exoribonuclease. J Biol Chem. 1997 Apr 18;272(16):10448–10456. [PubMed]
  • Migliaccio A, Di Domenico M, Castoria G, de Falco A, Bontempo P, Nola E, Auricchio F. Tyrosine kinase/p21ras/MAP-kinase pathway activation by estradiol-receptor complex in MCF-7 cells. EMBO J. 1996 Mar 15;15(6):1292–1300. [PMC free article] [PubMed]
  • Moskaitis JE, Buzek SW, Pastori RL, Schoenberg DR. The estrogen-regulated destabilization of Xenopus albumin mRNA is independent of translation. Biochem Biophys Res Commun. 1991 Jan 31;174(2):825–830. [PubMed]
  • Nagy E, Rigby WF. Glyceraldehyde-3-phosphate dehydrogenase selectively binds AU-rich RNA in the NAD(+)-binding region (Rossmann fold). J Biol Chem. 1995 Feb 10;270(6):2755–2763. [PubMed]
  • Nakagawa J, Waldner H, Meyer-Monard S, Hofsteenge J, Jenö P, Moroni C. 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):2051–2055. [PMC free article] [PubMed]
  • Pastori RL, Moskaitis JE, Buzek SW, Schoenberg DR. Coordinate estrogen-regulated instability of serum protein-coding messenger RNAs in Xenopus laevis. Mol Endocrinol. 1991 Apr;5(4):461–468. [PubMed]
  • Pastori RL, Moskaitis JE, Schoenberg DR. Estrogen-induced ribonuclease activity in Xenopus liver. Biochemistry. 1991 Oct 29;30(43):10490–10498. [PubMed]
  • Pastori RL, Schoenberg DR. 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):313–319. [PubMed]
  • Peitsch MC. ProMod and Swiss-Model: Internet-based tools for automated comparative protein modelling. Biochem Soc Trans. 1996 Feb;24(1):274–279. [PubMed]
  • Preiss T, Sang AE, Chrzanowska-Lightowlers ZM, Lightowlers RN. The mRNA-binding protein COLBP is glutamate dehydrogenase. FEBS Lett. 1995 Jul 3;367(3):291–296. [PubMed]
  • Prokipcak RD, Herrick DJ, Ross J. 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):9261–9269. [PubMed]
  • Riegel AT, Aitken SC, Martin MB, Schoenberg DR. Posttranscriptional regulation of albumin gene expression in Xenopus liver: evidence for an estrogen receptor-dependent mechanism. Mol Endocrinol. 1987 Feb;1(2):160–167. [PubMed]
  • Ross J. mRNA stability in mammalian cells. Microbiol Rev. 1995 Sep;59(3):423–450. [PMC free article] [PubMed]
  • Ross J, Kobs G. 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):579–593. [PubMed]
  • Scheper W, Holthuizen PE, Sussenbach JS. 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):1000–1007. [PMC free article] [PubMed]
  • Schoenberg DR, Moskaitis JE, Smith LH, Jr, Pastori RL. Extranuclear estrogen-regulated destabilization of Xenopus laevis serum albumin mRNA. Mol Endocrinol. 1989 May;3(5):805–814. [PubMed]
  • Shapiro DJ, Barton MC, McKearin DM, Chang TC, Lew D, Blume J, Nielsen DA, Gould L. Estrogen regulation of gene transcription and mRNA stability. Recent Prog Horm Res. 1989;45:29–64. [PubMed]
  • Stoeckle MY. 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):1123–1127. [PMC free article] [PubMed]
  • Taylor KL, Pohl J, Kinkade JM., Jr Unique autolytic cleavage of human myeloperoxidase. Implications for the involvement of active site MET409. J Biol Chem. 1992 Dec 15;267(35):25282–25288. [PubMed]
  • Vreken P, Raué HA. 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):2986–2996. [PMC free article] [PubMed]

Articles from RNA are provided here courtesy of The RNA Society

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...