Competitive binding of CUGBP1 and HuR to occludin mRNA controls its translation and modulates epithelial barrier function

Molecular Biology of the Cell

Volumn 24, Issue 2, 2013, Pages 85-99

  Yu, Ting Xi ^a   Rao, Jaladanki N ^a   Zou, Tongtong ^a   Liu, Lan ^a   Xiao, Lan ^a   Ouyang, Miao ^a   Cao, Shan ^a   Gorospe, Myriam ^b   Wang, Jian Ying ^a,c  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b BALTIMORE VA MEDICAL CENTER   (United States)

^c NATIONAL INSTITUTE ON AGING   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CUG BINDING PROTEIN 1; HUR PROTEIN; MESSENGER RNA; OCCLUDIN; PROTEIN ZO1; RNA BINDING PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ARTICLE; BINDING COMPETITION; CELL POLARITY; CONTROLLED STUDY; GENE DISRUPTION; GENE EXPRESSION REGULATION; GENE LOCATION; GENE OVEREXPRESSION; GENE REPRESSION; GENETIC ASSOCIATION; HUMAN; HUMAN CELL; INTESTINE EPITHELIUM CELL; PRIORITY JOURNAL; PROTEIN BINDING; RNA PROCESSING; RNA TRANSLATION; TIGHT JUNCTION; WESTERN BLOTTING;

3' UNTRANSLATED REGIONS; BASE SEQUENCE; BINDING SITES; BINDING, COMPETITIVE; CACO-2 CELLS; ELECTRIC IMPEDANCE; EPITHELIAL CELLS; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; GENES, REPORTER; HU PARANEOPLASTIC ENCEPHALOMYELITIS ANTIGENS; HUMANS; INTESTINES; LUCIFERASES, RENILLA; OCCLUDIN; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; RNA, MESSENGER; RNA, SMALL INTERFERING; RNA-BINDING PROTEINS; TIGHT JUNCTIONS;

EID: 84872291506     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E12-07-0531     Document Type: Article

References (58)

1. Abdelmohsen K et al. (2007). Phosphorylation of HuR by Chk2 regulates SIRT1 expression. Mol Cell 25, 543-557. (Pubitemid 46274441)
2. Bartel DP (2009). MicroRNAs: target recognition and regulatory functions. Cell 136, 215-233.
3. Bhattacharyya SN, Habermacher R, Martine U, Closs El, Filipowicz W (2006). Relief of microRNA-mediated translational repression in human cells subjected to stress. Cell 125, 1111-1124. (Pubitemid 43866197)
4. Buchan JR, Parker R (2009). Eukaryotic stress granules: the ins and outs of translation. Mol Cell 36, 932-941.
5. Chen J, Xiao L, Rao JN, Zou T, Liu L, Bellavance E, Gorospe M, Wang JY (2008). JunD represses transcription and translation of the tight junction protein zona occludens-1 modulating intestinal epithelial barrier function. Mol Biol Cell 19, 3701-3712.
6. Chen Y, Merzdorf C, Paul DL, Goodenough DA (1997). COOH terminus of occludin is required for tight junction barrier function in early Xenopus embryos. J Cell Biol 138, 891-899. (Pubitemid 27365050)
7. Chu CY, Rana TM (2006). Translation repression in human cells by microRNA-induced gene silencing requires RCK/p54. PLoS Biol 4, e210.
8. Cui YH, Xiao L, Rao JN, Zou T, Liu L, Chen Y, Turner DJ, Gorospe M, Wang JY (2012). miR-503 represses CUG-binding protein 1 translation by recruiting CUGBP1 mRNA to processing bodies. Mol Biol Cell 23, 151-162.
9. Cummins PM (2012). Occludin: one protein, many forms. Mol Cell Biol 32, 242-250.
10. Du D et al. (2010). The tight junction protein, occludin, regulates the directional migration of epithelial cells. Dev Cell 18, 52-63.
11. Forster C (2008). Tight junctions and the modulation of barrier function in disease. Histochem Cell Biol 130, 55-70.
12. Furuse M, Hirase T, Itoh M, Nagafuchi A, Yonemura S, Tsukita S, Tsukita S (1993). Occludin: a novel integral membrane protein localizing at tight junctions. J Cell Biol 123, 1777-1788. (Pubitemid 24012933)
13. Gherzi R, Lee KY, Briata P, Wegmuller D, Moroni C, Karin M, Chen CY (2004). A KH domain RNA binding protein, KSRP, promotes ARE-directed mRNA turnover by recruiting the degradation machinery. Mol Cell 14, 571-583. (Pubitemid 38739081)
14. Guo X, Rao JN, Liu L, Zou T, Turner DJ, Bass BL, Wang JY (2003). Regulation of adherens junctions and epithelial paracellular permeability: a novel function for polyamines. Am J Physiol Cell Physiol 285, C1174-C1187. (Pubitemid 37296294)
15. Harter JL (1960). Critical values for Duncan's new multiple range test.
16. Houseley J, Tollervey D (2009). The many pathways of RNA degradation. Cell 136, 763-776.
17. Huichalaf C et al. (2010). Expansion of CUG RNA repeats causes stress and inhibition of translation in myotonic dystrophy 1 (DM1) cells. FASEB J 24, 3706-3719.
18. Iakova P, Wang GL, Timchenko L, Michalak M, Pereira-Smith OM, Smith JR, Timchenko NA (2004). Competition of CUGBP1 and calreticulin for the regulation of p21 translation determines cell fate. EMBO J 23, 406-417. (Pubitemid 38294505)
19. Kawai T, Lal A, Yang X, Galban S, Mazan-Mamczarz K, Gorospe M (2006). Translational control of cytochrome c by RNA-binding proteins TIA-1 and HuR. Mol Cell Biol 26, 3295-3307.
20. Keene JD (2007). RNA regulons: coordination of post-transcriptional events. Nature Rev Genet 8, 533-543.
21. Kress C, Gautier-Courteille C, Osborne HB, Babinet C, Paillard L (2007). Inactivation of CUG-BP1/CELF1 causes growth, viability, and spermatogenesis defects in mice. Mol Cell Biol 27, 1146-1157. (Pubitemid 46174574)
22. Kulkarni M., Ozgur S, Stoecklin G (2010). On track with P-bodies. Biochem Soc Trans 38, 242-251.
23. Lal A, Mazan-Mamczarz K, Kawai T, Yang X, Martindale JL, Gorospe M (2004). Concurrent versus individual binding of HuR and AUF1 to common labile target mRNAs. EMBO J 23, 3092-3102. (Pubitemid 39093603)
24. Lee EK et al. (2010). hnRNP C promotes APP translation by competing with FMRP for APP mRNA recruitment to P bodies. Nature Struct Mol Biol 17, 732-739.
25. Lee JE, Lee JY, Wilusz J, Tian B, Wilusz CJ (2010). Systematic analysis of cis-elements in unstable mRNAs demonstrates that CUGBP1 is a key regulator of mRNA decay in muscle cells. PloS One 5, e11201.
26. Liao B, Hu Y, Brewer G (2007). Competitive binding of AUF1 and TIAR to MYC mRNA controls its translation. Nature Struct Mol Biol 14, 511-518. (Pubitemid 46871812)
27. Liu L, Rao JN, Zou T, Xiao L, Wang PY, Turner DJ, Gorospe M, Wang JY (2009). Polyamines regulate c-Myc translation through Chk2-dependent HuR phosphorylation. Mol Biol Cell 20, 4885-4898.
28. Marchiando AM et al. (2010). Caveolin-1-dependent occludin endocytosis is required for TNF-induced tight junction regulation in vivo. J Cell Biol 189, 111-126.
29. McCarthy KM, Skare IB, Stankewich MC, Furuse M, Tsukita S, Rogers RA, Lynch RD, Schneeberger EE (1996). Occludin is a functional component of the tight junction. J Cell Sci 1, 2287-2298. (Pubitemid 26325491)
30. Milne CA, Hodgkin J (1999). ETR-1, a homologue of a protein linked to myotonic dystrophy, is essential for muscle development in Caenorhabditis elegans. Curr Biol 9, 1243-1246. (Pubitemid 29527149)
31. Paillard L, Omilli F, Legagneux V, Bassez T, Maniey D, Osborne HB (1998). EDEN and EDEN-BP, a cis element and an associated factor that mediate sequence-specific mRNA deadenylation in Xenopus embryos. EMBO J 17, 278-287. (Pubitemid 28041068)
32. Raleigh DR, Marchiando AM, Zhang Y, Shen L, Sasaki H, Wang Y, Long M, Turner JR (2010). Tight junction-associated MARVEL proteins marveld3, tricellulin, and occludin have distinct but overlapping functions. Mol Biol Cell 21, 1200-1213.
33. Raleigh DR et al. (2011). Occludin S408 phosphorylation regulates tight junction protein interactions and barrier function. J Cell Biol 193, 565-582.
34. Rattenbacher B, Beisang D, Wiesner DL, Jeschke JC, von Hohenberg M, St Louis-Vlasova IA, Bohjanen PR (2010). Analysis of CUGBP1 targets identifies GU-repeat sequences that mediate rapid mRNA decay. Mol Cell Biol 30, 3970-3980.
35. Saito K, Kondo E, Matsushita M (2011). microRNA 130 family regulates the hypoxia response signal through the P-body protein DDX6. Nucleic Acids Res 39, 6086-6099.
36. Saitou M, Furuse M, Sasaki H, Schulzke JD, Fromm M, Takano H, Noda T, Tsukita S (2000). Complex phenotype of mice lacking occludin, a component of tight junction strands. Mol Biol Cell 11, 4131-4142.
37. Schulzke JD, Fromm M (2009). Tight junctions: molecular structure meets function. Ann NY Acad Sci 1165, 1-6.
38. Seth A, Sheth P, Elias BC, Rao RK (2007). Protein phosphatases 2A and 1 interact with occludin and negatively regulate the assembly of tight junctions in the CACO-2 cell monolayer. J Biol Chem 282, 11487-11498. (Pubitemid 47100808)
39. Shen L, Pili R (2008). Posttranscription regulation of prostate cancer growth. Cancer J 14, 46-53.
40. Su L, Mruk DD, Lui WY, Lee WM, Cheng CY (2011). P-glycoprotein regulates blood-testis barrier dynamics via its effects on the occludin/zonula occludens 1 (ZO-1) protein complex mediated by focal adhesion kinase (FAK). Proc Natl Acad Sci USA 108, 19623-19628.
41. Suh E, Traber PG (1996). An intestine-specific homeobox gene regulates proliferation and differentiation. Mol Cell Biol 16, 619-625. (Pubitemid 26029101)
42. Suzuki T, Elias BC, Seth A, Shen L, Turner JR, Giorgianni F, Desiderio D, Guntaka R, Rao R (2009). PKCη regulates occludin phosphorylation and epithelial tight junction integrity. Proc Natl Acad Sci USA 106, 61-66.
43. Tsuda K et al. (2009). Structural basis for the seqeunce-specific RNA-recognition mechanism of human CUGB-BP1 RRM3. Nucleic Acids Res 37, 5151-5166.
44. Turner JR (2009). Intestinal mucosal barrier function in health and disease. Nature Rev Immunol 9, 799-809.
45. Vlasova IA, Bohjanen PR (2008). Posttranscriptional regulation of gene networks by GU-rich elements and CELF proteins. RNA Biol 5, 201-207.
46. 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, 293-306.
47. Wang Z, Wade P, Mandell KJ, Akyildiz A, Parkos CA, Mrsny RJ, Nusrat A (2007). Raf 1 represses expression of the tight junction protein occludin via activation of the zinc-finger transcription factor slug. Oncogene 26, 1222-1230.
48. Wong V, Gumbiner BM (1997). A synthetic peptide corresponding to the extracellular domain of occludin perturbs the tight junction permeability barrier. J Cell Biol 136, 399-409. (Pubitemid 27063089)
49. Xiao L, Cui YH, Rao JN, Zou T, Liu L, Smith A, Turner DJ, Gorospe M, Wang JY (2011). Regulation of cyclin-dependent kinase 4 translation through CUG-binding protein 1 and microRNA-222 by polyamines. Mol Biol Cell 22, 3055-3069.
50. Xiao L, Rao JN, Zou T, Liu L, Marasa BS, Chen J, Turner DJ, Passaniti A, Wang JY (2007a). Induced JunD in intestinal epithelial cells represses CDK4 transcription through its proximal promoter region following polyamine depletion. Biochem J 403, 573-581. (Pubitemid 46706986)
51. Xiao L, Rao JN, Zou T, Liu L, Marasa BS, Chen J, Turner DJ, Zhou H, Gorospe H, Wang JY (2007b). Polyamines regulate the stability of activating transcription factor-2 mRNA through RNA-binding protein HuR in intestinal epithelial cells. Mol Biol Cell 18, 4579-4590. (Pubitemid 350060183)
52. Ye D, Guo S, Al-Sadi R, Ma TY (2011). MicroRNA regulation of intestinal epithelial tight junction permeability. Gastroenterology 141, 1323-1333.
53. Yu AS, McCarthy KM, Francis SA, McCormack JM, Lai J, Rogers RA, Lynch RD, Schneeberger EE (2005). Knockdown of occludin expression leads to diverse phenotypic alterations in epithelial cells. Am J Physiol Cell Physiol 288, C1231-C1241. (Pubitemid 40991060)
54. Yu TX, Wang PY, Rao JN, Zou T, Liu L, Xiao L, Gorospe M, Wang JY (2011). Chk2-dependent HuR phosphorylation regulates occludin mRNA translation and epithelial barrier function. Nucleic Acids Res 39, 8472-8487.
55. Zhang L, Lee JE, Wilusz J, Wilusz CJ (2008). The RNA-binding protein CUGBP1 regulates stability of tumor necrosis factor mRNA in muscle cells: implications for myotonic dystrophy. J Biol Chem 283, 22457-22463.
56. 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, 7623-7637.
57. Zou T, Mazan-Mamczarz K, Rao JN, Liu L, Marasa BS, Zhang AH, Xiao L, Pullmann R, Gorospe M, Wang JY (2006). Polyamine depletion increases cytoplasmic levels of RNA-binding protein HuR leading to stabilization of nucleophosmin and p53 mRNAs. J Biol Chem 281, 19387-19394. (Pubitemid 44035444)
58. Zou T, Rao JN, Liu L, Xiao L, Yu TX, Jiang P, Gorospe M, Wang JY (2010). Polyamines regulate the stability of JunD mRNA by modulating the competitive binding of its 32 untranslated region to HuR and AUF1. Mol Cell Biol 30, 5021-5032.