Alternative 3′ UTRs act as scaffolds to regulate membrane protein localization

Nature

Volumn 522, Issue 7556, 2015, Pages 363-367

  Berkovits, Binyamin D ^a   Mayr, Christine ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD47 ANTIGEN; MEMBRANE PROTEIN; MESSENGER RNA; PROTEOME; RNA; RNA BINDING PROTEIN; RNA BINDING PROTEIN HUR; RNA BINDING PROTEIN SET; UNCLASSIFIED DRUG; 3' UNTRANSLATED REGION; CD47 PROTEIN, HUMAN; CHAPERONE; ELAV LIKE PROTEIN 1; ELAV PROTEIN; ELAVL1 PROTEIN, HUMAN; RAC1 PROTEIN; RAC1 PROTEIN, HUMAN; RNA ISOFORM; SET PROTEIN, HUMAN; TRANSCRIPTION FACTOR;

CYTOPLASM; GENE EXPRESSION; GERM CELL; MEMBRANE; PROTEIN; RNA;

3' UNTRANSLATED REGION; AMINO ACID SEQUENCE; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; GENE TRANSLOCATION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN TRANSPORT; REGULATORY MECHANISM; RNA BINDING; CELL LINE; CHEMISTRY; GENETICS; METABOLISM; POLYADENYLATION; REPORTER GENE;

3' UNTRANSLATED REGIONS; ANTIGENS, CD47; CELL LINE; CELL MEMBRANE; ELAV PROTEINS; ELAV-LIKE PROTEIN 1; ENDOPLASMIC RETICULUM; GENES, REPORTER; HISTONE CHAPERONES; HUMANS; MEMBRANE PROTEINS; POLYADENYLATION; PROTEIN TRANSPORT; RAC1 GTP-BINDING PROTEIN; RNA ISOFORMS; RNA, MESSENGER; TRANSCRIPTION FACTORS;

EID: 84930052197     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature14321     Document Type: Article

References (40)

1. Sandberg, R., Neilson, J. R., Sarma, A., Sharp, P. A. & Burge, C. B. Proliferating cells express mRNAs with shortened 39 untranslated regions and fewer microRNA target sites. Science 320, 1643-1647 (2008).
2. Mayr, C. & Bartel, D. P. Widespread shortening of 39UTRs by alternative cleavage and polyadenylation activates oncogenes in cancer cells. Cell 138, 673-684 (2009).
3. Lianoglou, S., Garg, V., Yang, J. L., Leslie, C. S. & Mayr, C. Ubiquitously transcribed genes use alternative polyadenylation to achieve tissue-specific expression. Genes Dev. 27, 2380-2396 (2013).
4. Brennan, C. M., Gallouzi, I. E. & Steitz, J. A. Protein ligands to HuR modulate its interaction with target mRNAs in vivo. J. Cell Biol. 151, 1-14 (2000).
5. ten Klooster, J. P., Leeuwen, I., Scheres, N., Anthony, E. C. & Hordijk, P. L. Rac1-induced cell migration requires membrane recruitment of the nuclear oncogene SET. EMBO J. 26, 336-345 (2007).
6. Kishore, S. et al. A quantitative analysis of CLIP methods for identifying binding sites of RNA-binding proteins. Nature Methods 8, 559-564 (2011).
7. Lebedeva, S. et al. Transcriptome-wide analysis of regulatory interactions of the RNA-binding protein HuR. Mol. Cell 43, 340-352 (2011).
8. Mukherjee,N. et al. Integrative regulatorymapping indicates that the RNA-binding protein HuR couples pre-mRNA processing and mRNA stability. Mol. Cell 43, 327-339 (2011).
9. Uren, P. J. et al. Genomic analyses of the RNA-binding protein Hu antigen R (HuR) identify a complex network of target genes and novel characteristics of its binding sites. J. Biol. Chem. 286, 37063-37066 (2011).
10. An, J. J. et al. Distinct role of long 39 UTR BDNF mRNA in spine morphology and synaptic plasticity in hippocampal neurons. Cell 134, 175-187 (2008).
11. Oldenborg, P. A. et al. Role of CD47 as a marker of self on red blood cells. Science 288, 2051-2054 (2000).
12. Jaiswal, S. et al. CD47 is upregulated on circulating hematopoietic stem cells and leukemia cells to avoid phagocytosis. Cell 138, 271-285 (2009).
13. Fan, X. C. & Steitz, J. A. Overexpression of HuR, a nuclear-cytoplasmic shuttling protein, increases the in vivo stability of ARE-containing mRNAs. EMBO J. 17, 3448-3460 (1998).
14. Mazan-Mamczarz, K. et al. RNA-binding protein HuR enhances p53 translation in response to ultraviolet light irradiation. Proc. Natl Acad. Sci. USA 100, 8354-8359 (2003).
15. Seo, S. B. et al. Regulation of histone acetylation and transcription by INHAT, a human cellular complex containing the set oncoprotein. Cell 104, 119-130 (2001).
16. Fan, Z., Beresford, P. J., Oh, D. Y., Zhang, D. & Lieberman, J. Tumor suppressor NM23-H1 is a granzyme A-activated DNase during CTL-mediated apoptosis, and the nucleosome assembly protein SET is its inhibitor. Cell 112, 659-672 (2003).
17. Miller, J. D., Wilhelm, H., Gierasch, L., Gilmore, R. & Walter, P. GTP binding and hydrolysis by the signal recognition particle during initiation of protein translocation. Nature 366, 351-354 (1993).
18. Schneider, R., Bannister, A. J., Weise, C.& Kouzarides, T.Direct binding of INHAT to H3 tails disrupted by modifications. J. Biol. Chem. 279, 23859-23862 (2004).
19. Zerangue, N., Schwappach, B., Jan, Y. N. & Jan, L. Y. A new ER trafficking signal regulates the subunit stoichiometry of plasma membrane K(ATP) channels. Neuron 22, 537-548 (1999).
20. Walmsley, M. J. et al. Critical roles for Rac1 and Rac2 GTPases in B cell development and signaling. Science 302, 459-462 (2003).
21. Reinhold, M. I., Green, J. M., Lindberg, F. P., Ticchioni, M. & Brown, E. J. Cell spreading distinguishes the mechanism of augmentation of T cell activation by integrin-associated protein/CD47 and CD28. Int. Immunol. 11, 707-718 (1999).
22. Lamy, L. et al. CD47 and the 19 kDa interacting protein-3 (BNIP3) in T cell apoptosis. J. Biol. Chem. 278, 23915-23921 (2003).
23. Lindberg, F. P. et al. Decreased resistance to bacterial infection and granulocyte defects in IAP-deficient mice. Science 274, 795-798 (1996).
24. Isenberg, J. S. et al. Thrombospondin-1 and CD47 limit cell and tissue survival of radiation injury. Am. J. Pathol. 173, 1100-1112 (2008).
25. Soto-Pantoja, D. R., Isenberg, J. S.&Roberts,D.D. Therapeutic targeting ofCD47 to modulate tissue responses to ischemia and radiation. J. Genet. Syndr.Gene Ther. 2, 1000105 (2011).
26. Frazier, W. A., Isenberg, J. S., Kaur, S. & Roberts, D. D. in UCSD Nature Molecule Pages (University of California, San Diego, 2010).
27. Avet, C. et al. SET protein interacts with intracellular domains of the gonadotropinreleasing hormone receptor and differentially regulates receptor signaling to cAMP and calcium in gonadotrope cells. J. Biol. Chem. 288, 2641-2654 (2013).
28. Nilsson, J., Persson, B. & von Heijne, G. Comparative analysis of amino acid distributions in integral membrane proteins from 107 genomes. Proteins 60, 606-616 (2005).
29. Lau, A. G. et al. Distinct 39UTRs differentially regulate activity-dependent translation of brain-derived neurotrophic factor (BDNF). Proc. Natl Acad. Sci. USA 107, 15945-15950 (2010).
30. Yoon, J. H. et al. Scaffold function of long non-coding RNA HOTAIR in protein ubiquitination. Nature Commun. 4, 2939 (2013).
31. Neviani, P. et al. The tumor suppressor PP2A is functionally inactivated in blast crisis CML through the inhibitory activity of the BCR/ABL-regulated SET protein. Cancer Cell 8, 355-368 (2005).
32. Nho, R. S. et al. PTEN regulates fibroblast elimination during collagen matrix contraction. J. Biol. Chem. 281, 33291-33301 (2006).
33. Reinhold, M. I. et al. In vivo expression of alternatively spliced forms of integrinassociated protein (CD47). J. Cell Sci. 108, 3419-3425 (1995).
34. Slobodin, B. & Gerst, J. E. A novel mRNA affinity purification technique for the identification of interacting proteins and transcripts in ribonucleoprotein complexes. RNA 16, 2277-2290 (2010).
35. Bertrand, E. et al. Localization of ASH1 mRNA particles in living yeast. Mol. Cell 2, 437-445 (1998).
36. Ridley, A. J., Paterson, H. F., Johnston, C. L., Diekmann, D. & Hall, A. The small GTPbinding protein rac regulates growth factor-induced membrane ruffling. Cell 70, 401-410 (1992).
37. Niranjanakumari, S., Lasda, E., Brazas, R. & Garcia-Blanco, M. A. Reversible crosslinking combined with immunoprecipitation to study RNA-protein interactions in vivo. Methods 26, 182-190 (2002).
38. Mili, S. & Steitz, J. A. Evidence for reassociation of RNA-binding proteins after cell lysis:implications for the interpretationofimmunoprecipitationanalyses.RNA 10, 1692-1694 (2004).
39. Huang, daW., Sherman, B. T. & Lempicki, R. A. Systematic and integrative analysis of large gene lists usingDAVIDbioinformatics resources.Nature Protocols 4,44-57 (2009).
40. Stagljar, I. & Fields, S. Analysis of membrane protein interactions using yeastbased technologies. Trends Biochem. Sci. 27, 559-563 (2002). RESEARCH