Enhanced CLIP Uncovers IMP Protein-RNA Targets in Human Pluripotent Stem Cells Important for Cell Adhesion and Survival

Cell Reports

Volumn 15, Issue 3, 2016, Pages 666-679

  Conway, Anne E ^a,b   Van Nostrand, Eric L ^a   Pratt, Gabriel A ^a   Aigner, Stefan ^a   Wilbert, Melissa L ^a   Sundararaman, Balaji ^a   Freese, Peter ^c   Lambert, Nicole J ^c   Sathe, Shashank ^a   Liang, Tiffany Y ^a   Essex, Anthony ^b   Landais, Severine ^b   Burge, Christopher B ^c   Jones, D Leanne ^b,d   Yeo, Gene W ^a,e,f  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e AGENCY FOR SCIENCE   (Singapore)

^f NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; CELL PROTEIN; INSULIN LIKE GROWTH FACTOR 2 BINDING PROTEIN; INSULIN LIKE GROWTH FACTOR 2 MRNA BINDING PROTEIN; INSULIN LIKE GROWTH FACTOR 2 MRNA BINDING PROTEIN 1; INSULIN LIKE GROWTH FACTOR 2 MRNA BINDING PROTEIN 2; INTEGRIN; ITGB5 PROTEIN; MESSENGER RNA; PROTEIN BCL 2; RNA BINDING PROTEIN; UNCLASSIFIED DRUG; 3' UNTRANSLATED REGION; CROSS LINKING REAGENT; IMP-1 PROTEIN, HUMAN; IMP3 PROTEIN, HUMAN; PROTEIN BINDING; RNA;

3' UNTRANSLATED REGION; AMINO TERMINAL SEQUENCE; ANALYTIC METHOD; ARTICLE; BINDING AFFINITY; BINDING SITE; CELL ADHESION; CELL DEATH; CELL LEVEL; CELL SURVIVAL; CONTROLLED STUDY; ENHANCED CROSSLINKING AND IMMUNOPRECIPITATION; HUMAN; HUMAN CELL; MOLECULAR DYNAMICS; PHENOTYPE; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN TARGETING; RNA STABILITY; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; HUMAN EMBRYONIC STEM CELL; IMMUNOPRECIPITATION; METABOLISM; NUCLEOTIDE MOTIF; NUCLEOTIDE SEQUENCE; PROCEDURES;

3' UNTRANSLATED REGIONS; BASE SEQUENCE; CELL ADHESION; CELL SURVIVAL; CROSS-LINKING REAGENTS; GENE EXPRESSION REGULATION; HUMAN EMBRYONIC STEM CELLS; HUMANS; IMMUNOPRECIPITATION; INTEGRINS; NUCLEOTIDE MOTIFS; PLURIPOTENT STEM CELLS; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS C-BCL-2; RNA; RNA STABILITY; RNA, MESSENGER; RNA-BINDING PROTEINS;

EID: 84962757753     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2016.03.052     Document Type: Article

References (41)

1. Alipanahi B., Delong A., Weirauch M.T., Frey B.J. Predicting the sequence specificities of DNA- and RNA-binding proteins by deep learning. Nat. Biotechnol. 2015, 33:831-838.
2. Ardehali R., Inlay M.A., Ali S.R., Tang C., Drukker M., Weissman I.L. Overexpression of BCL2 enhances survival of human embryonic stem cells during stress and obviates the requirement for serum factors. Proc. Natl. Acad. Sci. USA 2011, 108:3282-3287.
3. Atlas R., Behar L., Sapoznik S., Ginzburg I. Dynamic association with polysomes during P19 neuronal differentiation and an untranslated-region-dependent translation regulation of the tau mRNA by the tau mRNA-associated proteins IMP1, HuD, and G3BP1. J. Neurosci. Res. 2007, 85:173-183.
4. Bell J.L., Wächter K., Mühleck B., Pazaitis N., Köhn M., Lederer M., Hüttelmaier S. Insulin-like growth factor 2 mRNA-binding proteins (IGF2BPs): post-transcriptional drivers of cancer progression?. Cell. Mol. Life Sci. 2013, 70:2657-2675.
5. Bernstein P.L., Herrick D.J., Prokipcak R.D., Ross J. Control of c-myc mRNA half-life in vitro by a protein capable of binding to a coding region stability determinant. Genes Dev. 1992, 6:642-654.
6. Braam S.R., Zeinstra L., Litjens S., Ward-van Oostwaard D., van den Brink S., van Laake L., Lebrin F., Kats P., Hochstenbach R., Passier R., et al. Recombinant vitronectin is a functionally defined substrate that supports human embryonic stem cell self-renewal via alphavbeta5 integrin. Stem Cells 2008, 26:2257-2265.
7. Chao J.A., Patskovsky Y., Patel V., Levy M., Almo S.C., Singer R.H. ZBP1 recognition of beta-actin zipcode induces RNA looping. Genes Dev. 2010, 24:148-158.
8. Dai N., Rapley J., Angel M., Yanik M.F., Blower M.D., Avruch J. mTOR phosphorylates IMP2 to promote IGF2 mRNA translation by internal ribosomal entry. Genes Dev. 2011, 25:1159-1172.
9. Dai N., Christiansen J., Nielsen F.C., Avruch J. mTOR complex 2 phosphorylates IMP1 cotranslationally to promote IGF2 production and the proliferation of mouse embryonic fibroblasts. Genes Dev. 2013, 27:301-312.
10. Dai N., Zhao L., Wrighting D., Krämer D., Majithia A., Wang Y., Cracan V., Borges-Rivera D., Mootha V.K., Nahrendorf M., et al. IGF2BP2/IMP2-Deficient mice resist obesity through enhanced translation of Ucp1 mRNA and Other mRNAs encoding mitochondrial proteins. Cell Metab. 2015, 21:609-621.
11. Dimitriadis E., Trangas T., Milatos S., Foukas P.G., Gioulbasanis I., Courtis N., Nielsen F.C., Pandis N., Dafni U., Bardi G., Ioannidis P. Expression of oncofetal RNA-binding protein CRD-BP/IMP1 predicts clinical outcome in colon cancer. Int. J. Cancer 2007, 121:486-494.
12. Farina K.L., Huttelmaier S., Musunuru K., Darnell R., Singer R.H. Two ZBP1 KH domains facilitate beta-actin mRNA localization, granule formation, and cytoskeletal attachment. J. Cell Biol. 2003, 160:77-87.
13. Gu W., Wells A.L., Pan F., Singer R.H. Feedback regulation between zipcode binding protein 1 and beta-catenin mRNAs in breast cancer cells. Mol. Cell. Biol. 2008, 28:4963-4974.
14. Gu W., Katz Z., Wu B., Park H.Y., Li D., Lin S., Wells A.L., Singer R.H. Regulation of local expression of cell adhesion and motility-related mRNAs in breast cancer cells by IMP1/ZBP1. J. Cell Sci. 2012, 125:81-91.
15. Hafner M., Landthaler M., Burger L., Khorshid M., Hausser J., Berninger P., Rothballer A., Ascano M., Jungkamp A.C., Munschauer M., et al. Transcriptome-wide identification of RNA-binding protein and microRNA target sites by PAR-CLIP. Cell 2010, 141:129-141.
16. Hammer N.A., Hansen Tv., Byskov A.G., Rajpert-De Meyts E., Grøndahl M.L., Bredkjaer H.E., Wewer U.M., Christiansen J., Nielsen F.C. Expression of IGF-II mRNA-binding proteins (IMPs) in gonads and testicular cancer. Reproduction 2005, 130:203-212.
17. Han H., Irimia M., Ross P.J., Sung H.K., Alipanahi B., David L., Golipour A., Gabut M., Michael I.P., Nachman E.N., et al. MBNL proteins repress ES-cell-specific alternative splicing and reprogramming. Nature 2013, 498:241-245.
18. Hansen T.V.O., Hammer N.A., Nielsen J., Madsen M., Dalbaeck C., Wewer U.M., Christiansen J., Nielsen F.C. Dwarfism and impaired gut development in insulin-like growth factor II mRNA-binding protein 1-deficient mice. Mol. Cell. Biol. 2004, 24:4448-4464.
19. Hüttelmaier S., Zenklusen D., Lederer M., Dictenberg J., Lorenz M., Meng X., Bassell G.J., Condeelis J., Singer R.H. Spatial regulation of beta-actin translation by Src-dependent phosphorylation of ZBP1. Nature 2005, 438:512-515.
20. Janiszewska M., Suvà M.L., Riggi N., Houtkooper R.H., Auwerx J., Clément-Schatlo V., Radovanovic I., Rheinbay E., Provero P., Stamenkovic I. Imp2 controls oxidative phosphorylation and is crucial for preserving glioblastoma cancer stem cells. Genes Dev. 2012, 26:1926-1944.
21. Jønson L., Vikesaa J., Krogh A., Nielsen L.K., Hansen Tv., Borup R., Johnsen A.H., Christiansen J., Nielsen F.C. Molecular composition of IMP1 ribonucleoprotein granules. Mol. Cell. Proteomics 2007, 6:798-811.
22. Konig J., Zarnack K., Rot G., Curk T., Kayikci M., Zupan B., Turner D.J., Luscombe N.M., Ule J. iCLIP--transcriptome-wide mapping of protein-RNA interactions with individual nucleotide resolution. J. Vis. Exp. 2011, (50):2638.
23. Lambert N., Robertson A., Jangi M., McGeary S., Sharp P.A., Burge C.B. RNA Bind-n-Seq: quantitative assessment of the sequence and structural binding specificity of RNA binding proteins. Mol. Cell 2014, 54:887-900.
24. Lee S.R., Pratt G.A., Martinez F.J., Yeo G.W., Lykke-Andersen J. Target discrimination in nonsense-mediated mRNA decay requires Upf1 ATPase activity. Mol. Cell 2015, 59:413-425.
25. Leeds P., Kren B.T., Boylan J.M., Betz N.A., Steer C.J., Gruppuso P.A., Ross J. Developmental regulation of CRD-BP, an RNA-binding protein that stabilizes c-myc mRNA in vitro. Oncogene 1997, 14:1279-1286.
26. Li Q., Brown J.B., Huang H., Bickel P.J. Measuring reproducibility of high-throughput experiments. Ann. Appl. Stat. 2011, 5:1752-1779.
27. Lovci M.T., Ghanem D., Marr H., Arnold J., Gee S., Parra M., Liang T.Y., Stark T.J., Gehman L.T., Hoon S., et al. Rbfox proteins regulate alternative mRNA splicing through evolutionarily conserved RNA bridges. Nat. Struct. Mol. Biol. 2013, 20:1434-1442.
28. Marchetto M.C., Narvaiza I., Denli A.M., Benner C., Lazzarini T.A., Nathanson J.L., Paquola A.C., Desai K.N., Herai R.H., Weitzman M.D., et al. Differential L1 regulation in pluripotent stem cells of humans and apes. Nature 2013, 503:525-529.
29. Nielsen J., Christiansen J., Lykke-Andersen J., Johnsen A.H., Wewer U.M., Nielsen F.C. A family of insulin-like growth factor II mRNA-binding proteins represses translation in late development. Mol. Cell. Biol. 1999, 19:1262-1270.
30. Nielsen F.C., Nielsen J., Kristensen M.A., Koch G., Christiansen J. Cytoplasmic trafficking of IGF-II mRNA-binding protein by conserved KH domains. J. Cell Sci. 2002, 115:2087-2097.
31. Nielsen J., Kristensen M.A., Willemoës M., Nielsen F.C., Christiansen J. Sequential dimerization of human zipcode-binding protein IMP1 on RNA: a cooperative mechanism providing RNP stability. Nucleic Acids Res. 2004, 32:4368-4376.
32. Ray D., Kazan H., Cook K.B., Weirauch M.T., Najafabadi H.S., Li X., Gueroussov S., Albu M., Zheng H., Yang A., et al. A compendium of RNA-binding motifs for decoding gene regulation. Nature 2013, 499:172-177.
33. Ross A.F., Oleynikov Y., Kislauskis E.H., Taneja K.L., Singer R.H. Characterization of a beta-actin mRNA zipcode-binding protein. Mol. Cell. Biol. 1997, 17:2158-2165.
34. Ross J., Lemm I., Berberet B. Overexpression of an mRNA-binding protein in human colorectal cancer. Oncogene 2001, 20:6544-6550.
35. Sugimoto Y., König J., Hussain S., Zupan B., Curk T., Frye M., Ule J. Analysis of CLIP and iCLIP methods for nucleotide-resolution studies of protein-RNA interactions. Genome Biol. 2012, 13:R67.
36. Van Nostrand E.L., Pratt G.A., Shishkin A.A., Gelboin-Burkhart C., Fang M.Y., Sundararaman B., Blue S.M., Nguyen T.B., Surka C., Elkins K., et al. Robust transcriptome-wide discovery of RNA binding protein binding sites with enhanced CLIP (eCLIP). Nat. Methods 2016, Published online March 28, 2016. 10.1038/nmeth.3810.
37. Vikesaa J., Hansen T.V., Jønson L., Borup R., Wewer U.M., Christiansen J., Nielsen F.C. RNA-binding IMPs promote cell adhesion and invadopodia formation. EMBO J. 2006, 25:1456-1468.
38. Wagenmakers A.J., Reinders R.J., van Venrooij W.J. Cross-linking of mRNA to proteins by irradiation of intact cells with ultraviolet light. Eur. J. Biochem. 1980, 112:323-330.
39. Wilbert M.L., Huelga S.C., Kapeli K., Stark T.J., Liang T.Y., Chen S.X., Yan B.Y., Nathanson J.L., Hutt K.R., Lovci M.T., et al. LIN28 binds messenger RNAs at GGAGA motifs and regulates splicing factor abundance. Mol. Cell 2012, 48:195-206.
40. Wu B., Buxbaum A.R., Katz Z.B., Yoon Y.J., Singer R.H. Quantifying protein-mRNA interactions in single live cells. Cell 2015, 162:211-220.
41. Yeo G.W., Coufal N.G., Liang T.Y., Peng G.E., Fu X.D., Gage F.H. An RNA code for the FOX2 splicing regulator revealed by mapping RNA-protein interactions in stem cells. Nat. Struct. Mol. Biol. 2009, 16:130-137.