Tandem RNA isolation reveals functional rearrangement of RNA-binding proteins on CDKN1B/p27^Kip1 3’UTRs in cisplatin treated cells

References

• Neelamraju Y, Hashemikhabir S, Janga SC. The human RBPome: from genes and proteins to human disease. J Proteomics. 2015;127:61–70.
   PubMed Web of Science ®Google Scholar
• Blagden S, Abdel Mouti M, Chettle J. Ancient and modern: hints of a core post-transcriptional network driving chemotherapy resistance in ovarian cancer. Wiley Interdiscip Rev RNA. 2018;9:e1432.
   PubMed Web of Science ®Google Scholar
• Iadevaia V, Gerber AP. Combinatorial control of mRNA fates by RNA-binding proteins and non-coding RNAs. Biomolecules. 2015;5:2207–2222.
   PubMed Web of Science ®Google Scholar
• Hentze MW, Castello A, Schwarzl T, et al. A brave new world of RNA-binding proteins. Nat Rev Mol Cell Biol. 2018;19:327–341.
   PubMed Web of Science ®Google Scholar
• Matia-Gonzalez AM, Laing EE, Gerber AP. Conserved mRNA-binding proteomes in eukaryotic organisms. Nat Struct Mol Biol. 2015;22:1027–1033.
   PubMed Web of Science ®Google Scholar
• Sysoev VO, Fischer B, Frese CK, et al. Global changes of the RNA-bound proteome during the maternal-to-zygotic transition in Drosophila. Nat Commun. 2016;7:12128.
   PubMed Web of Science ®Google Scholar
• Liepelt A, Naarmann-de Vries IS, Simons N, et al. Identification of RNA-binding proteins in macrophages by interactome capture. Mol Cell Proteomics. 2016;15:2699–2714.
   PubMed Web of Science ®Google Scholar
• Milek M, Imami K, Mukherjee N, et al. DDX54 regulates transcriptome dynamics during DNA damage response. Genome Res. 2017;27:1344–1359.
   PubMed Web of Science ®Google Scholar
• Hassan T, Smith SG, Gaughan K, et al. Isolation and identification of cell-specific microRNAs targeting a messenger RNA using a biotinylated anti-sense oligonucleotide capture affinity technique. Nucleic Acids Res. 2013;41:e71.
   PubMed Web of Science ®Google Scholar
• Matia-Gonzalez AM, Iadevaia V, Gerber AP. A versatile tandem RNA isolation procedure to capture in vivo formed mRNA-protein complexes. Methods. 2017;118-119:93–100.
   PubMed Web of Science ®Google Scholar
• Iadevaia V, Matia-Gonzalez AM, Gerber AP. An oligonucleotide-based tandem RNA isolation procedure to recover eukaryotic mRNA-protein complexes. J Vis Exp. 2018;138:e58223.
   PubMed Web of Science ®Google Scholar
• Hartmuth K, Vornlocher HP, Luhrmann R. Tobramycin affinity tag purification of spliceosomes. Methods Mol Biol. 2004;257:47–64.
   PubMedGoogle Scholar
• Slobodin B, Gerst JE. RaPID: an aptamer-based mRNA affinity purification technique for the identification of RNA and protein factors present in ribonucleoprotein complexes. Methods Mol Biol. 2011;714:387–406.
   PubMedGoogle Scholar
• Shen DW, Pouliot LM, Hall MD, et al. Cisplatin resistance: a cellular self-defense mechanism resulting from multiple epigenetic and genetic changes. Pharmacol Rev. 2012;64:706–721.
   PubMed Web of Science ®Google Scholar
• Galluzzi L, Senovilla L, Vitale I, et al. Molecular mechanisms of cisplatin resistance. Oncogene. 2012;31:1869–1883.
   PubMed Web of Science ®Google Scholar
• Dasari S, Tchounwou PB. Cisplatin in cancer therapy: molecular mechanisms of action. Eur J Pharmacol. 2014;740:364–378.
   PubMed Web of Science ®Google Scholar
• Beli P, Lukashchuk N, Wagner SA, et al. Proteomic investigations reveal a role for RNA processing factor THRAP3 in the DNA damage response. Mol Cell. 2012;46:212–225.
   PubMed Web of Science ®Google Scholar
• Chavez JD, Hoopmann MR, Weisbrod CR, et al. Quantitative proteomic and interaction network analysis of cisplatin resistance in HeLa cells. PLoS One. 2011;6:e19892.
   PubMed Web of Science ®Google Scholar
• Pines A, Kelstrup CD, Vrouwe MG, et al. Global phosphoproteome profiling reveals unanticipated networks responsive to cisplatin treatment of embryonic stem cells. Mol Cell Biol. 2011;31:4964–4977.
   PubMed Web of Science ®Google Scholar
• Tamura K. Development of cell-cycle checkpoint therapy for solid tumors. Jpn J Clin Oncol. 2015;45:1097–1102.
   PubMed Web of Science ®Google Scholar
• Visconti R, Della Monica R, Grieco D. Cell cycle checkpoint in cancer: a therapeutically targetable double-edged sword. J Exp Clin Cancer Res. 2016;35:153.
   PubMed Web of Science ®Google Scholar
• Roy A, Banerjee S. p27 and leukemia: cell cycle and beyond. J Cell Physiol. 2015;230:504–509.
   PubMed Web of Science ®Google Scholar
• Sharma SS, Pledger WJ. The non-canonical functions of p27(Kip1) in normal and tumor biology. Cell Cycle. 2016;15:1189–1201.
   PubMed Web of Science ®Google Scholar
• Cannell IG, Merrick KA, Morandell S, et al. A pleiotropic RNA-binding protein controls distinct cell cycle checkpoints to drive resistance of p53-defective tumors to chemotherapy. Cancer Cell. 2015;28:623–637.
   PubMed Web of Science ®Google Scholar
• Stephens PJ, Tarpey PS, Davies H, et al. The landscape of cancer genes and mutational processes in breast cancer. Nature. 2012;486:400–404.
   PubMed Web of Science ®Google Scholar
• Le TV, Seo Y, Ryu CJ, et al. Increased expression of p27 is associated with the cisplatin resistance in gastric cancer cell line YCC-3. Arch Pharm Res. 2010;33:1127–1132.
   PubMed Web of Science ®Google Scholar
• Lim J, Lee SH, Cho S, et al. 4-methoxychalcone enhances cisplatin-induced oxidative stress and cytotoxicity by inhibiting the Nrf2/ARE-mediated defense mechanism in A549 lung cancer cells. Mol Cells. 2013;36:340–346.
   PubMed Web of Science ®Google Scholar
• Xie Q, Wang S, Zhao Y, et al. MiR-519d impedes cisplatin-resistance in breast cancer stem cells by down-regulating the expression of MCL-1. Oncotarget. 2017;8:22003–22013.
   PubMedGoogle Scholar
• Davaadelger B, Duan L, Perez RE, et al. Crosstalk between the IGF-1R/AKT/mTORC1 pathway and the tumor suppressors p53 and p27 determines cisplatin sensitivity and limits the effectiveness of an IGF-1R pathway inhibitor. Oncotarget. 2016;7:27511–27526.
   PubMedGoogle Scholar
• Huang Y, Jeong JS, Okamura J, et al. Global tumor protein p53/p63 interactome: making a case for cisplatin chemoresistance. Cell Cycle. 2012;11:2367–2379.
   PubMed Web of Science ®Google Scholar
• Casalini P, Iorio MV, Berno V, et al. Relationship between p53 and p27 expression following HER2 signaling. Breast. 2007;16:597–605.
   PubMed Web of Science ®Google Scholar
• Chen CS, Ho DR, Chen FY, et al. AKT mediates actinomycin D-induced p53 expression. Oncotarget. 2014;5:693–703.
   PubMedGoogle Scholar
• Huo Y, Iadevaia V, Yao Z, et al. Stable isotope-labelling analysis of the impact of inhibition of the mammalian target of rapamycin on protein synthesis. Biochem J. 2012;444:141–151.
   PubMed Web of Science ®Google Scholar
• Protter DSW, Parker R. Principles and properties of stress granules. Trends Cell Biol. 2016;26:668–679.
   PubMed Web of Science ®Google Scholar
• Lemm I, Ross J. Regulation of c-myc mRNA decay by translational pausing in a coding region instability determinant. Mol Cell Biol. 2002;22:3959–3969.
   PubMed Web of Science ®Google Scholar
• Karapetyan AR, Buiting C, Kuiper RA, et al. Regulatory roles for long ncRNA and mRNA. Cancers (Basel). 2013;5:462–490.
   PubMedGoogle Scholar
• Hamasaki K, Killian J, Cho J, et al. Minimal RNA constructs that specifically bind aminoglycoside antibiotics with high affinities. Biochemistry. 1998;37:656–663.
   PubMed Web of Science ®Google Scholar
• Baltz AG, Munschauer M, Schwanhausser B, et al. The mRNA-bound proteome and its global occupancy profile on protein-coding transcripts. Mol Cell. 2012;46:674–690.
   PubMed Web of Science ®Google Scholar
• Castello A, Fischer B, Eichelbaum K, et al. Insights into RNA biology from an atlas of mammalian mRNA-binding proteins. Cell. 2012;149:1393–1406.
   PubMed Web of Science ®Google Scholar
• Ziegeler G, Ming J, Koseki JC, et al. Embryonic lethal abnormal vision-like HuR-dependent mRNA stability regulates post-transcriptional expression of cyclin-dependent kinase inhibitor p27Kip1. J Biol Chem. 2010;285:15408–15419.
   PubMed Web of Science ®Google Scholar
• Mukherjee N, Corcoran DL, Nusbaum JD, et al. Integrative regulatory mapping indicates that the RNA-binding protein HuR couples pre-mRNA processing and mRNA stability. Mol Cell. 2011;43:327–339.
   PubMed Web of Science ®Google Scholar
• Yoon JH, De S, Srikantan S, et al. PAR-CLIP analysis uncovers AUF1 impact on target RNA fate and genome integrity. Nat Commun. 2014;5:5248.
   PubMed Web of Science ®Google Scholar
• Zheng Y, Miskimins WK. CUG-binding protein represses translation of p27Kip1 mRNA through its internal ribosomal entry site. RNA Biol. 2011;8:365–371.
   PubMed Web of Science ®Google Scholar
• Cox J, Hein MY, Luber CA, et al. Accurate proteome-wide label-free quantification by delayed normalization and maximal peptide ratio extraction, termed MaxLFQ. Mol Cell Proteomics. 2014;13:2513–2526.
   PubMed Web of Science ®Google Scholar
• Davis AP, Grondin CJ, Johnson RJ, et al. The comparative toxicogenomics database: update 2019. Nucleic Acids Res. 2018;47:D948–954.
   Web of Science ®Google Scholar
• Kondrashov N, Pusic A, Stumpf CR, et al. Ribosome-mediated specificity in Hox mRNA translation and vertebrate tissue patterning. Cell. 2011;145:383–397.
   PubMed Web of Science ®Google Scholar
• Albihlal WS, Gerber AP. Unconventional RNA-binding proteins: an uncharted zone in RNA biology. FEBS Lett. 2018;592:2917–2931.
   PubMed Web of Science ®Google Scholar
• Garcia-Maurino SM, Rivero-Rodriguez F, Velazquez-Cruz A, et al. RNA binding protein regulation and cross-talk in the control of AU-rich mRNA fate. Front Mol Biosci. 2017;4:71.
   PubMed Web of Science ®Google Scholar
• Biswas A, Brown CM. Scan for Motifs: a webserver for the analysis of post-transcriptional regulatory elements in the 3ʹ untranslated regions (3ʹ UTRs) of mRNAs. BMC Bioinformatics. 2014;15:174.
   PubMed Web of Science ®Google Scholar
• Fallmann J, Sedlyarov V, Tanzer A, et al. AREsite2: an enhanced database for the comprehensive investigation of AU/GU/U-rich elements. Nucleic Acids Res. 2016;44:D90–95.
   PubMed Web of Science ®Google Scholar
• Gherzi R, Chen CY, Ramos A, et al. KSRP controls pleiotropic cellular functions. Semin Cell Dev Biol. 2014;34:2–8.
   PubMed Web of Science ®Google Scholar
• Bracken CP, Wall SJ, Barre B, et al. Regulation of cyclin D1 RNA stability by SNIP1. Cancer Res. 2008;68:7621–7628.
   PubMed Web of Science ®Google Scholar
• Yim EK, Lee SB, Lee KH, et al. Analysis of the in vitro synergistic effect of 5-fluorouracil and cisplatin on cervical carcinoma cells. Int J Gynecol Cancer. 2006;16:1321–1329.
   PubMed Web of Science ®Google Scholar
• Dormoy-Raclet V, Menard I, Clair E, et al. The RNA-binding protein HuR promotes cell migration and cell invasion by stabilizing the beta-actin mRNA in a U-rich-element-dependent manner. Mol Cell Biol. 2007;27:5365–5380.
   PubMed Web of Science ®Google Scholar
• Li H, Chen W, Zhou Y, et al. Identification of mRNA binding proteins that regulate the stability of LDL receptor mRNA through AU-rich elements. J Lipid Res. 2009;50:820–831.
   PubMed Web of Science ®Google Scholar
• Hopkins TG, Mura M, Al-Ashtal HA, et al. The RNA-binding protein LARP1 is a post-transcriptional regulator of survival and tumorigenesis in ovarian cancer. Nucleic Acids Res. 2016;44:1227–1246.
   PubMed Web of Science ®Google Scholar
• Rukov JL, Shomron N. MicroRNA pharmacogenomics: post-transcriptional regulation of drug response. Trends Mol Med. 2011;17:412–423.
   PubMed Web of Science ®Google Scholar
• Mayr C. Regulation by 3ʹ-Untranslated Regions. Annu Rev Genet. 2017;51:171–194.
   PubMed Web of Science ®Google Scholar
• Smillie CL, Sirey T, Ponting CP. Complexities of post-transcriptional regulation and the modeling of ceRNA crosstalk. Crit Rev Biochem Mol Biol. 2018;53:231–245.
   PubMed Web of Science ®Google Scholar
• Srisawat C, Engelke DR. RNA affinity tags for purification of RNAs and ribonucleoprotein complexes. Methods. 2002;26:156–161.
   PubMed Web of Science ®Google Scholar
• Galgano A, Forrer M, Jaskiewicz L, et al. Comparative analysis of mRNA targets for human PUF-family proteins suggests extensive interaction with the miRNA regulatory system. PLoS One. 2008;3:e3164.
   PubMed Web of Science ®Google Scholar
• Imig J, Kanitz A, Gerber AP. RNA regulons and the RNA-protein interaction network. BioMol Concepts. 2012;2:403–414.
   Google Scholar
• Keene JD. RNA regulons: coordination of post-transcriptional events. Nat Rev Genet. 2007;8:533–543.
   PubMed Web of Science ®Google Scholar
• Chang JF, Lin ST, Hung E, et al. Nuclear proteomics with XRCC3 knockdown to reveal the development of doxorubicin-resistant uterine cancer. Toxicol Sci. 2014;139:396–406.
   PubMed Web of Science ®Google Scholar
• Fukunaga S, Kakehashi A, Sumida K, et al. Integrative analyses of miRNA and proteomics identify potential biological pathways associated with onset of pulmonary fibrosis in the bleomycin rat model. Toxicol Appl Pharmacol. 2015;286:188–197.
   PubMed Web of Science ®Google Scholar
• Boucas J, Fritz C, Schmitt A, et al. Label-free protein-RNA interactome analysis identifies khsrp signaling downstream of the p38/Mk2 kinase complex as a critical modulator of cell cycle progression. PLoS One. 2015;10:e0125745.
   PubMed Web of Science ®Google Scholar
• Piskareva O, Harvey H, Nolan J, et al. The development of cisplatin resistance in neuroblastoma is accompanied by epithelial to mesenchymal transition in vitro. Cancer Lett. 2015;364:142–155.
   PubMed Web of Science ®Google Scholar
• Wu W, Yan C, Gan T, et al. Nuclear proteome analysis of cisplatin-treated HeLa cells. Mutat Res. 2010;691:1–8.
   PubMed Web of Science ®Google Scholar
• Hernandez Losa J, Parada Cobo C, Guinea Viniegra J, et al. Role of the p38 MAPK pathway in cisplatin-based therapy. Oncogene. 2003;22:3998–4006.
   PubMed Web of Science ®Google Scholar
• Briata P, Forcales SV, Ponassi M, et al. p38-dependent phosphorylation of the mRNA decay-promoting factor KSRP controls the stability of select myogenic transcripts. Mol Cell. 2005;20:891–903.
   PubMed Web of Science ®Google Scholar
• Vlasova IA, Tahoe NM, Fan D, et al. Conserved GU-rich elements mediate mRNA decay by binding to CUG-binding protein 1. Mol Cell. 2008;29:263–270.
   PubMed Web of Science ®Google Scholar
• Iadevaia V, Wang X, Yao Z, et al. Evaluation of mTOR-regulated mRNA translation. Methods Mol Biol. 2012;821:171–185.
   PubMedGoogle Scholar
• King HA, El-Sharif HF, Matia-Gonzalez AM, et al. Generation of ribosome imprinted polymers for sensitive detection of translational responses. Sci Rep. 2017;7:6542.
   PubMed Web of Science ®Google Scholar
• Hartmuth K, Urlaub H, Vornlocher HP, et al. Protein composition of human prespliceosomes isolated by a tobramycin affinity-selection method. Proc Natl Acad Sci U S A. 2002;99:16719–16724.
   PubMed Web of Science ®Google Scholar
• Cox J, Mann M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol. 2008;26:1367–1372.
   PubMed Web of Science ®Google Scholar
• Vizcaino JA, Deutsch EW, Wang R, et al. ProteomeXchange provides globally coordinated proteomics data submission and dissemination. Nat Biotechnol. 2014;32:223–226.
   PubMed Web of Science ®Google Scholar
• Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001;29:e45.
   PubMed Web of Science ®Google Scholar
• Scherrer T, Femmer C, Schiess R, et al. Defining potentially conserved RNA regulons of homologous zinc-finger RNA-binding proteins. Genome Biol. 2011;12:R3.
   PubMed Web of Science ®Google Scholar
• Boyle EI, Weng S, Gollub J, et al. GO::termFinder–open source software for accessing Gene Ontology information and finding significantly enriched Gene Ontology terms associated with a list of genes. Bioinformatics. 2004;20:3710–3715.
   PubMed Web of Science ®Google Scholar
• Szklarczyk D, Morris JH, Cook H, et al. The STRING database in 2017: quality-controlled protein-protein association networks, made broadly accessible. Nucleic Acids Res. 2017;45:D362–D368.
   PubMed Web of Science ®Google Scholar