The 90-kDa heat shock protein stabilizes the polysomal ribonuclease 1 mRNA endonuclease to degradation by the 26S proteasome

Molecular Biology of the Cell

Volumn 19, Issue 2, 2008, Pages 546-552

  Peng, Yong ^a,b   Liu, Xiaoqiang ^a   Schoenberg, Daniel R ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b College of Physicians and Surgeons ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

C SRC PROTEIN; ENDONUCLEASE; GELDANAMYCIN; HEAT SHOCK PROTEIN 90; MESSENGER RNA; POLYSOMAL RIBONUCLEASE 1; PROTEASOME; PROTEIN TYROSINE KINASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CATALYSIS; CONTROLLED STUDY; HUMAN; HUMAN CELL; NONHUMAN; POLYSOME; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION;

ANIMALS; BENZOQUINONES; BINDING SITES; CELL LINE, TUMOR; CERCOPITHECUS AETHIOPS; COS CELLS; ENDONUCLEASES; HSP90 HEAT-SHOCK PROTEINS; HUMANS; LACTAMS, MACROCYCLIC; MODELS, BIOLOGICAL; POLYRIBOSOMES; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, TERTIARY; RNA STABILITY; RNA, MESSENGER; SEQUENCE DELETION;

EID: 39449133370     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E07-08-0774     Document Type: Article

References (31)

1. Bonvini, P., Dalla Rosa, H., Vignes, N., and Rosolen, A. (2004). Ubiquitination and proteasomal degradation of nucleophosmin-anaplastic lymphoma kinase induced by 17-allylamino-demethoxygeldanamycin: role of the co-chaperone carboxyl heat shock protein 70-interacting protein. Cancer Res. 64, 3256-3264.
2. Bremer, K. A., Stevens, A., and Schoenberg, D. R. (2003). An endonuclease activity similar to Xenopus PMR1 catalyzes the degradation of normal and nonsense-containing human β-globin mRNA in erythroid cells. RNA 9, 1157-1167.
3. Chernokalskaya, E., DuBell, A. N., Cunningham, K. S., Hanson, M. N., Dompenciel, R. E., and Schoenberg, D. R. (1998). A polysomal ribonuclease involved in the destabilization of albumin mRNA is a novel member of the peroxidase gene family. RNA 4, 1537-1548.
4. Cunningham, K. S., Hanson, M. N., and Schoenberg, D. R. (2001). Polysomal ribonuclease 1 exists in a latent form on polysomes prior to estrogen activation of mRNA decay. Nucleic Acids Res. 29, 1156-1162.
5. Dompenciel, R. E., Garnepudi, V. R., and Schoenberg, D. R. (1995). Purification and characterization of an estrogen-regulated Xenopus liver polysomal nuclease involved in the selective destabilization of albumin mRNA. J. Biol. Chem. 270, 6108-6118.
6. Doong, H., Rizzo, K., Fang, S., Kulpa, V., Weissman, A. M., and Kohn, E. C. (2003). CAIR-1/BAG-3 abrogates heat shock protein-70 chaperone complex-mediated protein degradation: accumulation of poly-ubiquitinated Hsp90 client proteins. J. Biol. Chem. 278, 28490-28500.
7. Gallouzi, I., Parker, F., Chebli, K., Maurier, F., Labourier, E., Barlat, I., Capony, J. P., Tocque, B., and Tazi, J. (1998). A novel phosphorylation-dependent RNase activity of GAP-SH3 binding protein: a potential link between signal transduction and RNA stability. Mol. Cell. Biol. 18, 3956-3965.
8. Garneau, N. L., Wilusz, J., and Wilusz, C. J. (2007). The highways and byways of mRNA decay. Nat. Rev. Mol. Cell Biol. 8, 113-126.
9. Hollien, J., and Weissman, J. S. (2006). Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response. Science 313, 104-107.
10. Kim, T. S., Jang, C. Y., Kim, H. D., Lee, J. Y., Ahn, B. Y., and Kim, J. (2006). Interaction of Hsp90 with ribosomal proteins protects from ubiquitination and proteasome-dependent degradation. Mol. Biol. Cell 17, 824-833.
11. Kisselev, A. F., and Goldberg, A. L. (2001). Proteasome inhibitors: from research tools to drug candidates. Chem. Biol. 8, 739-758.
12. Kisselev, A. F., Callard, A., and Goldberg, A. L. (2006). Importance of the different proteolytic sites of the proteasome and the efficacy of inhibitors varies with the protein substrate. J. Biol. Chem. 281, 8582-8590.
13. Laroia, G., Cuesta, R., Brewer, G., and Schneider, R. J. (1999). Control of mRNA decay by heat shock-ubiquitin-proteasome pathway. Science 284, 499-502.
14. Laroia, G., Sarkar, B., and Schneider, R. J. (2002). Ubiquitin-dependent mechanism regulates rapid turnover of AU-rich cytokine mRNAs. Proc. Natl. Acad. Sci. USA 99, 1842-1846.
15. Lawson, B., Brewer, J. W., and Hendershot, L. M. (1998). Geldanamycin an Hsp90/GRP94-binding drug, induces increased transcription of endoplasmic reticulum (ER) chaperones via the ER stress pathway. J. Cell Physiol. 174, 170-178.
16. Loo, M. A., Jensen, T. J., Cui, L., Hou, Y., Chang, X. B., and Riordan, J. R. (1998). Perturbation of Hsp90 interaction with nascent CFTR prevents its maturation and accelerates its degradation by the proteasome. EMBO J. 17, 6879-6887.
17. Murray, E. L., and Schoenberg, D. R. (2007). A + U-rich instability elements differentially activate 5′-3′ and 3′-5′ mRNA decay. Mol. Cell Biol. 27, 2791-2799.
18. Pastori, R. L., Moskaitis, J. E., Buzek, S. W., and Schoenberg, D. R. (1991a). Coordinate estrogen-regulated instability of serum protein-coding messenger RNAs in Xenopus laevis. Mol. Endocrinol. 5, 461-468.
19. Pastori, R. L., Moskaitis, J. E., and Schoenberg, D. R. (1991b). Estrogen-induced ribonuclease activity in Xenopus liver. Biochemistry 30, 10490-10498.
20. Peng, Y., and Schoenberg, D. R. (2007). c-Src activates endonuclease-mediated mRNA decay. Mol. Cell 25, 779-787.
21. Prodromou, C., Roe, S. M., O'Brien, R., Ladbury, J. E., Piper, P. W., and Pearl, L. H. (1997). Identification and structural characterization of the ATP/ADP-binding site in the Hsp90 molecular chaperone. Cell 90, 65-75.
22. Sheth, U., and Parker, R. (2003). Decapping and decay of messenger RNA occur in cytoplasmic processing bodies. Science 300, 805-808.
23. Stancato, L. F., Silverstein, A. M., Owens-Grillo, J. K., Chow, Y. H., Jove, R., and Pratt, W. B. (1997). The Hsp90-binding antibiotic geldanamycin decreases Raf levels and epidermal growth factor signaling without disrupting formation of signaling complexes or reducing the specific enzymatic activity of Raf kinase. J. Biol. Chem. 272, 4013-4020.
24. Stebbins, C. E., Russo, A. A., Schneider, C., Rosen, N., Hartl, F. U., and Pavletich, N. P. (1997). Crystal structure of an Hsp90-geldanamycin complex: targeting of a protein chaperone by an antitumor agent. Cell 89, 239-250.
25. Stevens, A., Wang, Y., Bremer, K., Zhang, J., Hoepfner, R., Antoniou, M., Schoenberg, D. R., and Maquat, L. E. (2002). Beta-globin mRNA decay in erythroid cells: UG site-preferred endonucleolytic cleavage that is augmented by a premature termination codon. Proc. Natl. Acad. Sci. USA 99, 12741-12746.
26. Stoecklin, G., Mayo, T., and Anderson, P. (2005). ARE-mRNA degradation requires the 5′-3′ decay pathway. EMBO Rep. 7, 72-77.
27. Wang, Z., and Kiledjian, M. (2000). Identification of an erythroid-enriched endoribonuclease activity involved in specific mRNA cleavage. EMBO J. 19, 295-305.
28. Xu, Y., Singer, M. A., and Lindquist, S. (1999). Maturation of the tyrosine kinase c-src as a kinase and as a substrate depends on the molecular chaperone Hsp90. Proc. Natl. Acad. Sci. USA 96, 109-114.
29. Yang, F., Peng, Y., Murray, E. L., Otsuka, Y., Kedersha, N., and Schoenberg, D. R. (2006). Polysome-bound endonuclease PMR1 Is targeted to stress granules via stress-specific binding to TIA-1. Mol. Cell. Biol. 26, 8803-8813.
30. Yang, F., Peng, Y., and Schoenberg, D. R. (2004). Endonuclease-mediated mRNA decay requires tyrosine phosphorylation of polysomal ribonuclease 1 (PMR1) for the targeting and degradation of polyribosome-bound substrate mRNA. J. Biol. Chem. 279, 48993-49002.
31. Yang, F., and Schoenberg, D. R. (2004). Endonuclease-mediated mRNA decay involves the selective targeting of PMR1 to polyribosome-bound substrate mRNA. Mol. Cell 14, 435-445.