Insights from the HuR-interacting transcriptome: NcRNAs, ubiquitin pathways, and patterns of secondary structure dependent RNA interactions

Molecular Genetics and Genomics

Volumn 287, Issue 11-12, 2012, Pages 867-879

  St Laurent III, Georges ^a,b   Shtokalo, Dmitry ^b,c,d   Heydarian, Mohammad ^e   Palyanov, Andrey ^c,d   Babiy, Dmitry ^c   Zhou, Jianhua ^b   Kumar, Ajit ^f   Urcuqui Inchima, Silvio ^a  

^a UNIVERSIDAD DE ANTIOQUIA   (Colombia)

^b St Laurent Institute   (United States)

^c AcademGene Ltd   (Russian Federation)

^d A P ERSHOV INSTITUTE OF INFORMATICS SYSTEMS   (Russian Federation)

^e JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f GEORGE WASHINGTON UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

HuR; Protein RNA interaction; RNA; Secondary structure; Transcriptome

Indexed keywords

COMPLEMENTARY RNA; HUR PROTEIN; NUCLEOTIDE; TRANSCRIPTOME; UBIQUITIN PROTEIN LIGASE; UNTRANSLATED RNA;

ARTICLE; CONTROLLED STUDY; EXON; GENE LOCUS; GENETIC CODE; IMMUNOPRECIPITATION; MICROARRAY ANALYSIS; PRIORITY JOURNAL; PROTEIN RNA BINDING; PROTEIN SECONDARY STRUCTURE; RNA ANALYSIS; RNA SEQUENCE; RNA SPLICING; RNA STABILITY; RNA TRANSCRIPTION; SIGNAL TRANSDUCTION;

HU PARANEOPLASTIC ENCEPHALOMYELITIS ANTIGENS; HUMANS; IMMUNOPRECIPITATION; RNA, ANTISENSE; RNA, MESSENGER; TRANSCRIPTOME; UBIQUITIN;

EID: 84870400323     PISSN: 16174615     EISSN: 16174623     Source Type: Journal    
DOI: 10.1007/s00438-012-0722-8     Document Type: Article

References (86)

1. Abdelmohsen K, Lal A, Kim HH, Gorospe M (2007) Posttranscriptional orchestration of an anti-apoptotic program by HuR. Cell Cycle 6(11):1288-1292 (Pubitemid 47327958)
2. Abdelmohsen K, Srikantan S, Yang X, Lal A, Kim HH, Kuwano Y, Galban S, Becker KG, Kamara D, de Cabo R, Gorospe M (2009) Ubiquitin-mediated proteolysis of HuR by heat shock. EMBO J 28(9):1271-1282
3. Abdelmohsen K, Kim MM, Srikantan S, Mercken EM, Brennan SE, Wilson GM, Cabo R, Gorospe M (2010) miR-519 suppresses tumor growth by reducing HuR levels. Cell Cycle 9(7):1354-1359
4. Amadio M, Scapagnini G, Laforenza U, Intrieri M, Romeo L, Govoni S, Pascale A (2008) Post-transcriptional regulation of HSP70 expression following oxidative stress in SH-SY5Y cells: the potential involvement of the RNA-binding protein HuR. Curr Pharm Des 14(26):2651-2658
5. Auweter SD, Oberstrass FC, Allain FH (2006) Sequence-specific binding of single-stranded RNA: is there a code for recognition? Nucleic Acids Res 34(17):4943-4959 (Pubitemid 44605637)
6. Brennan CM, Steitz JA (2001) HuR and mRNA stability. Cell Mol Life Sci 58(2):266-277 (Pubitemid 32217358)
7. Brennan CM, Gallouzi IE, Steitz JA (2000) Protein ligands to HuR modulate its interaction with target mRNAs in vivo. J Cell Biol 151(1):1-14
8. Calaluce R, Gubin MM, Davis JW, Magee JD, Chen J, Kuwano Y, Gorospe M, Atasoy U (2010) The RNA binding protein HuR differentially regulates unique subsets of mRNAs in estrogen receptor negative and estrogen receptor positive breast cancer. BMC Cancer 10:126
9. Cao X, Yeo G, Muotri AR, Kuwabara T, Gage FH (2006) Noncoding RNAs in the mammalian central nervous system. Annu Rev Neurosci 29:77-103 (Pubitemid 44476840)
10. Chang N, Yi J, Guo G, Liu X, Shang Y, Tong T, Cui Q, Zhan M, Gorospe M, Wang W (2010) HuR uses AUF1 as a cofactor to promote p16INK4 mRNA decay. Mol Cell Biol 30(15): 3875-3886
11. Chen C, Okayama H (1987) High-efficiency transformation of mammalian cells by plasmid DNA. Mol Cell Biol 7(8): 2745-2752
12. Chen CY, Xu N, Shyu AB (2002) Highly selective actions of HuR in antagonizing AU-rich element-mediated mRNA destabilization. Mol Cell Biol 22(20):7268-7278
13. Cherry J, Karschner V, Jones H, Pekala PH (2006) HuR, an RNAbinding protein, involved in the control of cellular differentiation. In Vivo 20(1):17-23
14. Cho SJ, Zhang J, Chen X (2010) RNPC1 modulates the RNA-binding activity of, and cooperates with, HuR to regulate p21 mRNA stability. Nucleic Acids Res 38(7):2256-2267
15. Christov CP, Trivier E, Krude T (2008) Noncoding human Y RNAs are overexpressed in tumours and required for cell proliferation. Br J Cancer 98(5):981-988 (Pubitemid 351341611)
16. Cook KB, Kazan H, Zuberi K, Morris Q, Hughes TR (2011) RBPDB: a database of RNA-binding specificities. Nucleic Acids Res 39 (Database issue):D301-D308
17. Costantino CL, Witkiewicz AK, Kuwano Y, Cozzitorto JA, Kennedy EP, Dasgupta A, Keen JC, Yeo CJ, Gorospe M, Brody JR (2009) The role of HuR in gemcitabine efficacy in pancreatic cancer: HuR up-regulates the expression of the gemcitabine metabolizing enzyme deoxycytidine kinase. Cancer Res 69(11):4567-4572
18. Durie D, Lewis SM, Liwak U, Kisilewicz M, Gorospe M, Holcik M (2011) RNA-binding protein HuR mediates cytoprotection through stimulation of XIAP translation. Oncogene 30(12): 1460-1469
19. Faghihi MA, Wahlestedt C (2009) Regulatory roles of natural antisense transcripts. Nat Rev Mol Cell Biol 10(9):637-643
20. Faghihi MA, Modarresi F, Khalil AM, Wood DE, Sahagan BG, Morgan TE, Finch CE, St Laurent G 3rd, Kenny PJ, Wahlestedt C (2008) Expression of a noncoding RNA is elevated in Alzheimer's disease and drives rapid feed-forward regulation of beta-secretase. Nat Med 14(7):723-730
21. Faghihi MA, Kocerha J, Modarresi F, Engstrom PG, Chalk AM, Brothers SP, Koesema E, St Laurent G, Wahlestedt C (2010) RNAi screen indicates widespread biological function for human natural antisense transcripts. PLoS One 5(10):e13177
22. Fan XC, Steitz JA (1998) Overexpression of HuR, a nuclearcytoplasmic shuttling protein, increases the in vivo stability of ARE-containing mRNAs. EMBO J 17(12):3448-3460 (Pubitemid 28279517)
23. Fan J, Ishmael FT, Fang X, Myers A, Cheadle C, Huang SK, Atasoy U, Gorospe M, Stellato C (2011) Chemokine transcripts as targets of the RNA-binding protein HuR in human airway epithelium. J Immunol 186(4):2482-2494
24. Galban S, Kuwano Y, Pullmann R Jr, Martindale JL, Kim HH, Lal A, Abdelmohsen K, Yang X, Dang Y, Liu JO, Lewis SM, Holcik M, Gorospe M (2008) RNA-binding proteins HuR and PTB promote the translation of hypoxia-inducible factor 1alpha. Mol Cell Biol 28(1):93-107
25. Gardiner TJ, Christov CP, Langley AR, Krude T (2009) A conserved motif of vertebrate Y RNAs essential for chromosomal DNA replication. RNA 15(7):1375-1385
26. Gorospe M, Tominaga K, Wu X, Fahling M, Ivan M (2011) Posttranscriptional control of the hypoxic response by RNA-binding proteins and microRNAs. Front Mol Neurosci 4:7
27. Gruber AR, Lorenz R, Bernhart SH, Neubock R, Hofacker IL (2008) The Vienna RNA websuite. Nucleic Acids Res 36 (Web Server issue):W70-W74
28. Guide (2009) GeneChip Expression Analysis Technical Manual http://media.affymetrix.com/support/downloads/manuals/expression-analysis- technical-manual.pdf. Accessed 10 Sept 2012
29. Guo F, Li Y, Liu Y, Wang J, Li Y, Li G (2010) Inhibition of metastasis-associated lung adenocarcinoma transcript 1 in CaSki human cervical cancer cells suppresses cell proliferation and invasion. Acta Biochim Biophys Sin (Shanghai) 42(3):224-229
30. Hinman MN, Lou H (2008) Diverse molecular functions of Hu proteins. Cell Mol Life Sci 65(20):3168-3181
31. Hofacker IL, Fontana W, Stadler PF, Bonhoeffer S, Tacker M, Schuster P (1994) Fast folding and comparison of RNA secondary structures. Monatshefte f Chemie 125:167-188
32. Hogan DJ, Riordan DP, Gerber AP, Herschlag D, Brown PO (2008) Diverse RNA-binding proteins interact with functionally related sets of RNAs, suggesting an extensive regulatory system. PLoS Biol 6(10):e255
33. Huarte M, Guttman M, Feldser D, Garber M, Koziol MJ, Kenzelmann- Broz D, Khalil AM, Zuk O, Amit I, Rabani M, Attardi LD, Regev A, Lander ES, Jacks T, Rinn JL (2010) A large intergenic noncoding RNA induced by p53 mediates global gene repression in the p53 response. Cell 142(3):409-419
34. Iyaguchi D, Yao M, Tanaka I, Toyota E (2009) Cloning, expression, purification and preliminary crystallographic studies of the adenylate/uridylate-rich element-binding protein HuR complexed with its target RNA. Acta Crystallogr Sect F Struct Biol Cryst Commun 65(Pt 3):285-287
35. Kazan H, Ray D, Chan ET, Hughes TR, Morris Q (2010) RNAcontext: a new method for learning the sequence and structure binding preferences of RNA-binding proteins. PLoS Comput Biol 6:e1000832
36. Kedde M, Agami R (2008) Interplay between microRNAs and RNAbinding proteins determines developmental processes. Cell Cycle 7(7):899-903 (Pubitemid 351573784)
37. Kim HH, Gorospe M (2008) Phosphorylated HuR shuttles in cycles. Cell Cycle 7(20):3124-3126
38. Kim HH, Kuwano Y, Srikantan S, Lee EK, Martindale JL, Gorospe M (2009) HuR recruits let-7/RISC to repress c-Myc expression. Genes Dev 23(15):1743-1748
39. Kim HH, Abdelmohsen K, Gorospe M (2010) Regulation of HuR by DNA damage response kinases. J Nucleic Acids. doi: 10.4061/2010/981487
40. Kishore S, Jaskiewicz L, Burger L, Hausser J, Khorshid M, Zavolan M (2011) A quantitative analysis of CLIP methods for identifying binding sites of RNA-binding proteins. Nat Methods 8(7):559-564
41. Kohn M, Lederer M, Wachter K, Huttelmaier S (2010) Near-infrared (NIR) dye-labeled RNAs identify binding of ZBP1 to the noncoding Y3-RNA. RNA 16(7):1420-1428
42. Krude T, Christov CP, Hyrien O, Marheineke K (2009) Y RNA functions at the initiation step of mammalian chromosomal DNA replication. J Cell Sci 122(Pt 16):2836-2845
43. Kullmann M, Gopfert U, Siewe B, Hengst L (2002) ELAV/Hu proteins inhibit p27 translation via an IRES element in the p27 50UTR. Genes Dev 16(23):3087-3099 (Pubitemid 35424195)
44. Kuwano Y, Kim HH, Abdelmohsen K, Pullmann R Jr, Martindale JL, Yang X, Gorospe M (2008) MKP-1 mRNA stabilization and translational control by RNA-binding proteins HuR and NF90. Mol Cell Biol 28(14):4562-4575 (Pubitemid 351977754)
45. Lal A, Kawai T, Yang X, Mazan-Mamczarz K, Gorospe M (2005) Antiapoptotic function of RNA-binding protein HuR effected through prothymosin alpha. EMBO J 24(10):1852-1862 (Pubitemid 40769504)
46. Lebedeva S, Jens M, Theil K, Schwanhausser B, Selbach M, Landthaler M, Rajewsky N (2011) Transcriptome-wide analysis of regulatory interactions of the RNA-binding protein HuR. Mol Cell 43(3):340-352
47. Leulliot N, Varani G (2001) Current topics in RNA-protein recognition: control of specificity and biological function through induced fit and conformational capture. Biochemistry 40(27): 7947-7956 (Pubitemid 32641191)
48. Li M, Gu W (2011) A critical role for noncoding 5S rRNA in regulating Mdmx stability. Mol Cell 43(6):1023-1032
49. Lopez de Silanes I, Zhan M, Lal A, Yang X, Gorospe M (2004) Identification of a target RNA motif for RNA-binding protein HuR. Proc Natl Acad Sci USA 101(9):2987-2992 (Pubitemid 38327723)
50. Lopez de Silanes I, Gorospe M, Taniguchi H, Abdelmohsen K, Srikantan S, Alaminos M, Berdasco M, Urdinguio RG, Fraga MF, Jacinto FV, Esteller M (2009) The RNA-binding protein HuR regulates DNA methylation through stabilization of DNMT3b mRNA. Nucleic Acids Res 37(8):2658-2671
51. Ma WJ, Cheng S, Campbell C, Wright A, Furneaux H (1996) Cloning and characterization of HuR, a ubiquitously expressed Elav-like protein. J Biol Chem 271(14):8144-8151 (Pubitemid 26108641)
52. Masuda K, Abdelmohsen K, Gorospe M (2009) RNA-binding proteins implicated in the hypoxic response. J Cell Mol Med 13 (9A):2759-2769
53. Masuda K, Abdelmohsen K, Kim MM, Srikantan S, Lee EK, Tominaga K, Selimyan R, Martindale JL, Yang X, Lehrmann E, Zhang Y, Becker KG, Wang JY, Kim HH, Gorospe M (2011) Global dissociation of HuR-mRNA complexes promotes cell survival after ionizing radiation. EMBO J 30(6):1040-1053
54. Mattick JS, Makunin IV (2006) Non-coding RNA. Hum Mol Genet 15(Spec No 1):R17-R29
55. Mazan-Mamczarz K, Galban S, Lopez de Silanes I, Martindale JL, Atasoy U, Keene JD, Gorospe M (2003) RNA-binding protein HuR enhances p53 translation in response to ultraviolet light irradiation. Proc Natl Acad Sci USA 100(14):8354-8359 (Pubitemid 36842549)
56. Mazan-Mamczarz K, Hagner PR, Corl S, Srikantan S, Wood WH, Becker KG, Gorospe M, Keene JD, Levenson AS, Gartenhaus RB (2008) Post-transcriptional gene regulation by HuR promotes a more tumorigenic phenotype. Oncogene 27(47):6151-6163
57. Millard SS, Vidal A, Markus M, Koff A (2000) A U-rich element in the 50 untranslated region is necessary for the translation of p27 mRNA. Mol Cell Biol 20(16):5947-5959 (Pubitemid 30613044)
58. Morrissey JH (1981) Silver stain for proteins in polyacrylamide gels: a modified procedure with enhanced uniform sensitivity. Anal Biochem 117(2):307-310 (Pubitemid 12189968)
59. Mukherjee N, Corcoran DL, Nusbaum JD, Reid DW, Georgiev S, Hafner M, Ascano M Jr, Tuschl T, Ohler U, Keene JD (2011) Integrative regulatory mapping indicates that the RNA-binding protein HuR couples pre-mRNA processing and mRNA stability. Mol Cell 43(3):327-339
60. Nadar M, Chan MY, Huang SW, Huang CC, Tseng JT, Tsai CH (2011) HuR binding to AU-rich elements present in the 30 untranslated region of classical swine fever virus. Virol J 8(1):340
61. Nakamura H, Kawagishi H, Watanabe A, Sugimoto K, Maruyama M, Sugimoto M (2011) Cooperative role of the RNA-binding proteins Hzf and HuR in p53 activation. Mol Cell Biol 31(10):1997-2009
62. Oeffinger M, Wei KE, Rogers R, DeGrasse JA, Chait BT, Aitchison JD, Rout MP (2007) Comprehensive analysis of diverse ribonucleoprotein complexes. Nat Methods 4(11):951-956 (Pubitemid 350042385)
63. Peng S, Chen LL, Lei XX, Yang L, Lin H, Carmichael GG, Huang Y (2011) Genome-wide studies reveal that Lin28 enhances the translation of genes important for growth and survival of human embryonic stem cells. Stem Cells 29(3):496-504
64. Poliseno L, Salmena L, Riccardi L, Fornari A, Song MS, Hobbs RM, Sportoletti P, Varmeh S, Egia A, Fedele G, Rameh L, Loda M, Pandolfi PP (2010) Identification of the miR-106b*25 microRNA cluster as a proto-oncogenic PTEN-targeting intron that cooperates with its host gene MCM7 in transformation. Sci Signal 3 (117):ra29
65. Raspaglio G, De Maria I, Filippetti F, Martinelli E, Zannoni GF, Prislei S, Ferrandina G, Shahabi S, Scambia G, Ferlini C (2010) HuR regulates beta-tubulin isotype expression in ovarian cancer. Cancer Res 70(14):5891-5900
66. Ray D, Kazan H, Chan ET, Pena Castillo L, Chaudhry S, Talukder S, Blencowe BJ, Morris Q, Hughes TR (2009) Rapid and systematic analysis of the RNA recognition specificities of RNAbinding proteins. Nat Biotechnol 27(7):667-670
67. Richards NG, Rittenhouse DW, Freydin B, Cozzitorto JA, Grenda D, Rui H, Gonye G, Kennedy EP, Yeo CJ, Brody JR, Witkiewicz AK (2010) HuR status is a powerful marker for prognosis and response to gemcitabine-based chemotherapy for resected pancreatic ductal adenocarcinoma patients. Ann Surg 252 (3):499-505; discussion 505-506
68. Rzymski T, Paantjens A, Bod J, Harris AL (2008) Multiple pathways are involved in the anoxia response of SKIP3 including HuRregulated RNA stability, NF-kappaB and ATF4. Oncogene 27(33):4532-4543
69. Scheele C, Petrovic N, Faghihi MA, Lassmann T, Fredriksson K, Rooyackers O, Wahlestedt C, Good L, Timmons JA (2007) The human PINK1 locus is regulated in vivo by a non-coding natural antisense RNA during modulation of mitochondrial function. BMC Genomics 8:74
70. Scott GK, Marx C, Berger CE, Saunders LR, Verdin E, Schafer S, Jung M, Benz CC (2008) Destabilization of ERBB2 transcripts by targeting 30 untranslated region messenger RNA associated HuR and histone deacetylase-6. Mol Cancer Res 6(7):1250-1258
71. Sharp PA (2009) The centrality of RNA. Cell 136(4):577-580
72. Shtokalo DN, Palyanov AY, Babiy DP, Heydarian M, St Laurent G 3rd (2010) Identification of protein binding motifs in rna considering both primary sequence and secondary structure. BGRS Conference Abstract
73. Topisirovic I, Siddiqui N, Orolicki S, Skrabanek LA, Tremblay M, Hoang T, Borden KL (2009) Stability of eukaryotic translation initiation factor 4E mRNA is regulated by HuR, and this activity is dysregulated in cancer. Mol Cell Biol 29(5):1152-1162
74. Ule J, Jensen KB, Ruggiu M, Mele A, Ule A, Darnell RB (2003) CLIP identifies Nova-regulated RNA networks in the brain. Science 302(5648):1212-1215 (Pubitemid 37421026)
75. Wang W, Caldwell MC, Lin S, Furneaux H, Gorospe M (2000a) HuR regulates cyclin A and cyclin B1 mRNA stability during cell proliferation. EMBO J 19(10):2340-2350 (Pubitemid 30259015)
76. Wang W, Furneaux H, Cheng H, Caldwell MC, Hutter D, Liu Y, Holbrook N, Gorospe M (2000b) HuR regulates p21 mRNA stabilization by UV light. Mol Cell Biol 20(3):760-769 (Pubitemid 30044212)
77. Wang W, Yang X, Cristofalo VJ, Holbrook NJ, Gorospe M (2001) Loss of HuR is linked to reduced expression of proliferative genes during replicative senescence. Mol Cell Biol 21(17): 5889-5898 (Pubitemid 32737806)
78. Wang J, Zhao W, Guo Y, Zhang B, Xie Q, Xiang D, Gao J, Wang B, Chen Z (2009) The expression of RNA-binding protein HuR in non-small cell lung cancer correlates with vascular endothelial growth factor-C expression and lymph node metastasis. Oncology 76(6):420-429
79. Wang PY, Rao JN, Zou T, Liu L, Xiao L, Yu TX, Turner DJ, Gorospe M, Wang JY (2010) Post-transcriptional regulation of MEK-1 by polyamines through the RNA-binding protein HuR modulating intestinal epithelial apoptosis. Biochem J 426(3):293-306
80. Xiao L, Rao JN, Zou T, Liu L, Marasa BS, Chen J, Turner DJ, Zhou H, Gorospe M, Wang JY (2007) Polyamines regulate the stability of activating transcription factor-2 mRNA through RNA-binding protein HuR in intestinal epithelial cells. Mol Biol Cell 18(11):4579-4590 (Pubitemid 350060183)
81. Yi X, Zhou Y, Zheng W, Chambers SK (2009) HuR expression in the nucleus correlates with high histological grade and poor diseasefree survival in ovarian cancer. Aust N Z J Obstet Gynaecol 49(1):93-98
82. Yuan Z, Sanders AJ, Ye L, Jiang WG (2010) HuR, a key posttranscriptional regulator, and its implication in progression of breast cancer. Histol Histopathol 25(10):1331-1340
83. Yuan Z, Sanders AJ, Ye L, Wang Y, Jiang WG (2011) Prognostic value of the human antigen R (HuR) in human breast cancer: high level predicts a favourable prognosis. Anticancer Res 31(1):303-310
84. Zhang Q, Wu J, Nguyen A, Wang BD, He P, Laurent GS, Rennert OM, Su YA (2008) Molecular mechanism underlying differential apoptosis between human melanoma cell lines UACC903 and UACC903(+6) revealed by mitochondria-focused cDNA microarrays. Apoptosis 13(8):993-1004
85. Zhang X, Zou T, Rao JN, Liu L, Xiao L, Wang PY, Cui YH, Gorospe M, Wang JY (2009) Stabilization of XIAP mRNA through the RNA binding protein HuR regulated by cellular polyamines. Nucleic Acids Res 37(22):7623-7637
86. Zhao J, Ohsumi TK, Kung JT, Ogawa Y, Grau DJ, Sarma K, Song JJ, Kingston RE, Borowsky M, Lee JT (2011) Genome-wide identification of polycomb-associated RNAs by RIP-seq. Mol Cell 40(6):939-953