Chk2-dependent HuR phosphorylation regulates occludin mRNA translation and epithelial barrier function

Nucleic Acids Research

Volumn 39, Issue 19, 2011, Pages 8472-8487

  Yu, Ting Xi ^a,b   Wang, Peng Yuan ^a,b   Rao, Jaladanki N ^a,b   Zou, Tongtong ^a,b   Liu, Lan ^a,b   Xiao, Lan ^a,b   Gorospe, Myriam ^c   Wang, Jian Ying ^a,b  

^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

BETA CATENIN; CHECKPOINT KINASE 2; CLAUDIN 1; HUR PROTEIN; JUNCTIONAL ADHESION MOLECULE A; MESSENGER RNA; OCCLUDIN; POLYAMINE; PROTEIN ZO1; PROTEIN ZO2; SMALL INTERFERING RNA; UVOMORULIN;

3' UNTRANSLATED REGION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GENE OVEREXPRESSION; GENE SILENCING; INHIBITION KINETICS; INTESTINE EPITHELIUM; INTESTINE MUCOSA; INTESTINE MUCOSA PERMEABILITY; MALE; MOUSE; NONHUMAN; PERMEABILITY BARRIER; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; RAT; RNA INTERFERENCE; RNA TRANSLATION; SEPSIS;

3' UNTRANSLATED REGIONS; ANIMALS; CELL MEMBRANE PERMEABILITY; CELLS, CULTURED; GENE EXPRESSION REGULATION; HU PARANEOPLASTIC ENCEPHALOMYELITIS ANTIGENS; INTESTINAL MUCOSA; MALE; MEMBRANE PROTEINS; MICE; PHOSPHORYLATION; POLYAMINES; PROTEIN BIOSYNTHESIS; PROTEIN-SERINE-THREONINE KINASES; RATS; RNA, MESSENGER; SEPSIS;

MUS;

EID: 80455129693     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkr567     Document Type: Article

References (64)

1. Turner, J.R. (2009) Intestinal mucosal barrier function in health and disease. Nat. Rev. Immunol., 9, 799-809.
2. Schulzke, J.D. and Fromm, M. (2009) Tight junctions: molecular structure meets function. Ann. NY Acad. Sci., 1165, 1-6.
3. Förster, C. (2008) Tight junctions and the modulation of barrier function in disease. Histochem. Cell Biol., 130, 55-70.
4. Funke, L., Dakoji, S. and Bredt, D.S. (2005) Membrane-associated guanylate kinases regulate adhesion and plasticity at cell junctions. Annu. Rev. Biochem., 74, 219-245.
5. Nejsum, L.N. and Nelson, W.J. (2007) A molecular mechanism directly linking E-cadherin adhesion to initiation of epithelial cell surface polarity. J. Cell Biol., 178, 323-335.
6. Schneeberger, E.E. and Lynch, R.D. (2004) The tight junction: a multifunctional complex. Am. J. Physiol. Cell Physiol., 286, 1213-1228.
7. Liu, L., Guo, X., Rao, J.N., Zou, T., Xiao, L., Yu, T., Timmons, J.A., Turner, D.J. and Wang, J.Y. (2009) Polyamines regulate E-cadherin transcription through c-Myc modulating intestinal epithelial barrier function. Am. J. Physiol. Cell Physiol., 296, C801-C810.
8. Guo, X., Rao, J.N., Liu, L., Zou, T., Turner, D.J., Bass, B.L. and Wang, J.Y. (2003) Regulation of adherens junctions and epithelial paracellular permeability: a novel function for polyamines. Am. J. Physiol. Cell Physiol., 285, C1174-C1187.
9. Raleigh, D.R., Marchiando, A.M., Zhang, Y., Shen, L., Sasaki, H., Wang, Y., Long, M. and Turner, J.R. (2010) Tight junction-associated MARVEL proteins marveld3, tricellulin, and occludin have distinct but overlapping functions. Mol. Biol. Cell, 21, 1200-1213.
10. Suzuki, T., Elias, B.C., Seth, A., Shen, L., Turner, J.R., Giorgianni, F., Desiderio, D., Guntaka, R. and Rao, R. (2009) PKCZ regulates occludin phosphorylation and epithelial tight junction integrity. Proc. Natl Acad. Sci. USA, 106, 61-66.
11. Marchiando, A.M., Shen, L., Graham, W.V., Weber, C.R., Schwarz, B.T., Austin, J.R. 2nd, Raleigh, D.R., Guan, Y., Watson, A.J., Montrose, M.H. et al. (2010) Caveolin-1-dependent occludin endocytosis is required for TNF-induced tight junction regulation in vivo. J. Cell Biol., 189, 111-126.
12. Chen, Y., Merzdorf, C., Paul, D.L. and Goodenough, D.A. (1997) COOH terminus of occludin is required for tight junction barrier function in early Xenopus embryos. J. Cell Biol., 138, 891-899.
13. Lacaz-Vieira, F., Jaeger, M.M., Farshori, P. and Kachar, B. (1999) Small synthetic peptides homologous to segments of the first external loop of occludin impair tight junction resealing. J. Membr. Biol., 168, 289-297.
14. Rao, R. (2009) Occludin phosphorylation in regulation of epithelial tight junctions. Ann. NY Acad. Sci., 1165, 62-68.
15. Du, D. Xu, F., Yu, L., Zhang, C., Lu, X., Yuan, H., Huang, Q., Zhang, F., Bao, H., Jia, L. et al. (2010) The tight junction protein, occludin, regulates the directional migration of epithelial cells. Dev. Cell, 18, 52-63.
16. McCarthy, K.M., Skare, I.B., Stankewich, M.C., Furuse, M., Tsukita, S., Rogers, R.A., Lynch, R.D. and Schneeberger, E.E. (1996) Occludin is a functional component of the tight junction. J. Cell Sci., 109, 2287-2298.
17. Bamforth, S.D., Kniesel, U., Wolburg, H., Engelhardt, B. and Risau, W. (1999) A dominant mutant of occludin disrupts tight junction structure and function. J. Cell Sci., 112, 1879-1888.
18. Krishnan, M., Singh, A.B., Smith, J.J., Sharma, A., Chen, X., Eschrich, S., Yeatman, T.J., Beauchamp, R.D. and Dhawan, P. (2010) HDAC inhibitors regulate claudin-1 expression in colon cancer cells through modulation of mRNA stability. Oncogene, 29, 305-312.
19. Chen, J., Xiao, L., Rao, J.N., Zou, T., Liu, L., Bellavance, E., Gorospe, M. and Wang, J.Y. (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.
20. Guo, X., Rao, J.N., Liu, L., Zou, T., Keledjian, K.M., Boneva, D., Marasa, B.S. and Wang, J.Y. (2005) Polyamines are necessary for synthesis and stability of occludin protein in intestinal epithelial cells. Am. J. Physiol. Gastrointest. Liver Physiol., 288, G1159-G1169.
21. Wang, P.Y., Rao, J.N., Zou, T., Liu, L., Xiao, L., Yu, T.X., Turner, D.J., Gorospe, M. and Wang, J.Y. (2010) Post-transcriptional regulation of MEK-1 by polyamines through the RNA-binding protein HuR modulating intestinal epithelial apoptosis. Biochem. J., 426, 293-306.
22. Liu, L., Rao, J.N., Zou, T., Xiao, L., Wang, P.Y., Turner, D.J., Gorospe, M. and Wang, J.Y. (2009) Polyamines regulate c-Myc translation through Chk2-dependent HuR phosphorylation. Mol. Biol. Cell, 20, 4885-4898.
23. Xiao, L., Rao, J.N., Zou, T., Liu, L., Marasa, B.S., Chen, J., Turner, D.J., Zhou, H., Gorospe, M. and Wang, J.Y. (2007) 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.
24. Li, L., Liu, L., Rao, J.N., Esmaili, A., Strauch, E.D., Bass, B.L. and Wang, J.Y. (2002) JunD stabilization results in inhibition of normal intestinal epithelial cell growth through p21 after polyamine depletion. Gastroenterology, 123, 764-779.
25. Keene, J.D. (2007) RNA regulons: coordination of post-transcriptional events. Nat. Rev. Genet., 8, 533-543.
26. Abdelmohsen, K., Kuwano, Y., Kim, H.H. and Gorospe, M. (2008) Posttranscriptional gene regulation by RNA-binding proteins during oxidative stress: implications for cellular senescence. Biol. Chem., 389, 243-255.
27. Zhang, X., Zou, T., Rao, J.N., Liu, L., Xiao, L., Wang, P.Y., Cui, Y.H., Gorospe, M. and Wang, J.Y. (2009) Stabilization of XIAP mRNA through the RNA binding protein HuR regulated by cellular polyamines. Nucleic Acids Res., 37, 7623-7637.
28. Yeh, C.H., Hung, L.Y., Hsu, C., Le, S.Y., Lee, P.T., Liao, W.L., Lin, Y.T., Chang, W.C. and Tseng, J.T. (2008) RNA-binding protein HuR interacts with thrombomodulin 50 untranslated region and represses internal ribosome entry site-mediated translation under IL-3 treatment. Mol. Biol. Cell, 19, 3812-3822.
29. Bhattacharyya, S.N., Habermacher, R., Martine, U., Closs, E.I. and Filipowicz, W. (2006) Relief of microRNA-mediated translational repression in human cells subjected to stress. Cell, 125, 1111-1124.
30. Kim, H.H., Kuwano, Y., Srikantan, S., Lee, E.K., Martindale, J.L. and Gorospe, M. (2009) HuR recruits let-7/RISC to repress c-Myc expression. Genes Dev., 23, 1743-1748.
31. Chen, C.Y. and Shyu, A.B. (1995) AU-rich elements: characterization and importance in mRNA degradation. Trends Biochem. Sci., 20, 465-470.
32. Wilusz, C.J., Wormington, M. and Peltz, S.W. (2001) The cap-to-tail guide to mRNA turnover. Nat. Rev. Mol. Cell Biol., 2, 237-246.
33. Wilusz, C.J. and Wiluszm, J. (2004) Bringing the role of mRNA decay in the control of gene expression into focus. Trends Genet., 20, 491-497.
34. Kedersha, N., Stoecklin, G., Ayodele, M., Yacono, P., Lykke-Andersen, J., Fitzler, M.J., Scheuner, D., Kaufman, R.J., Golan, D.E. and Anderson, P. (2005) Stress granules and processing bodies are dynamically linked sites of mRNP remodeling. J. Cell Biol., 169, 871-884.
35. Gherzi, R., Lee, K.Y., Briata, P., Wegmuller, D., Moroni, C., Karin, M. and Chen, C.Y. (2004) A KH domain RNA binding protein, KSRP, promotes ARE-directed mRNA turnover by recruiting the degradation machinery. Mol. Cell, 14, 571-583.
36. Pan, Y.X., Chen, H. and Kilberg, M.S. (2005) Interaction of RNA-binding proteins HuR and AUF1 with the human ATF3 mRNA 3-untranslated region regulates its amino acid limitation-induced stabilization. J. Biol. Chem., 280, 34609-34616.
37. Liao, B., Hu, Y. and Brewer, G. (2007) Competitive binding of AUF1 and TIAR to MYC mRNA controls its translation. Nat. Struct. Mol. Biol., 14, 511-518.
38. Doller, A., Huwiler, A., Müller, R., Radeke, H.H., Pfeilschifter, J. and Eberhardt, W. (2007) Protein kinase C alpha-dependent phosphorylation of the mRNA-stabilizing factor HuR: implications for posttranscriptional regulation of cyclooxygenase-2. Mol. Biol. Cell, 18, 2137-2148.
39. Gorospe, M. (2003) HuR in the mammalian genotoxic response: post-transcriptional multitasking. Cell Cycle, 2, 412-414.
40. Wang, J.Y. (2007) Polyamines and mRNA stability in regulation of intestinal mucosal growth. Amino Acids, 33, 241-252.
41. Fan, X.C. and Steitz, J.A. (1998) Overexpression of HuR, a nuclear-cytoplasmic shuttling protein, increases the in vivo stability of ARE-containing mRNAs. EMBO J., 17, 3448-3460.
42. Abdelmohsen, K., Pullmann, R. Jr, Lal, A., Kim, H.H., Galban, S., Yang, X., Blethrow, J.D., Walker, M., Shubert, J., Gillespie, D.A. et al. (2007) Phosphorylation of HuR by Chk2 regulates SIRT1 expression. Mol. Cell, 25, 543-557.
43. Zou, T., Mazan-Mamczarz, K., Rao, J.N., Liu, L., Marasa, B.S., Zhang, A.H., Xiao, L., Pullmann, R., Gorospe, M. and Wang, J.Y. (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.
44. Kim, H.H. (2008) Nuclear HuR accumulation through phosphorylation by Cdk1. Genes Dev., 22, 1804-1815.
45. Suh, E. and Traber, P.G. (1996) An intestine-specific homeobox gene regulates proliferation and differentiation. Mol. Cell Biol., 16, 619-625.
46. Quaroni, A., Wands, J., Trelstad, R.L. and Isselbacher, K.J. (1979) Epithelioid cell cultures from rat small intestine. Characterization by morphologic and immunologic criteria. J. Cell Biol., 80, 248-265.
47. Rao, J.N., Liu, S.V., Zou, T., Liu, L., Xiao, L., Zhang, X., Bellavance, E., Yuan, J.X. and Wang, J.Y. (2008) Rac1 promotes intestinal epithelial restitution by increasing Ca2+ influx through interaction with phospholipase C-g1 after wounding. Am. J. Physiol. Cell Physiol., 295, C1499-C1509.
48. Kawai, T., Lal, A., Yang, X., Galban, S., Mazan-Mamczarz, K. and Gorospe, M. (2006) Translational control of cytochrome c by RNA-binding proteins TIA-1 and HuR. Mol. Cell. Biol., 26, 3295-3307.
49. Mazan-Mamczarz, K., Galban, S., de Silanes, I.L., Martindale, J.L., Atasoy, U., Keene, J.D. and Gorospe, M. (2003) RNA-binding protein HuR enhances p53 translation in response to ultraviolet light irradiation. Proc. Natl Acad. Sci. USA, 100, 8354-8359.
50. Guo, X., Rao, J.N., Liu, L., Zou, T.T., Turner, D.J., Bas, B.L. and Wang, J.Y. (2003) Regulation of adherens junctions and epithelial paracellular permeability: a novel function for polyamines. Am. J. Physiol. Cell Physiol., 285, C1174-C1187.
51. Hubbard, W.J., Choudhry, M., Schwacha, M.G., Kerby, J.D., Rue, L.W. 3rd, Bland, K.I. and Chaudry, I.H. (2005) Cecal ligation and puncture. Shock, 24, S52-S57.
52. Napolitano, L.M., Koruda, M.J., Meyer, A.A. and Baker, C.C. (1996) The impact of femur fracture with associated soft tissue injury on immune function and intestinal permeability. Shock, 5, 202-207.
53. Harter, J.L. (1960) Critical values for Duncan's new multiple range test. Biometrics, 16, 671-685.
54. López de Silanes, I., Zhan, M., Lal, A., Yang, X. and Gorospe, M. (2004) Identification of a target RNA motif for RNA-binding protein HuR. Proc. Natl Acad. Sci. USA, 101, 2987-2992.
55. Patel, A.R. and Wang, J.Y. (1999) Polyamine depletion is associated with an increase in JunD/AP-1 activity in small intestinal crypt cells. Am. J. Physiol. Gastrointest. Liver Physiol., 276, G441-G450.
56. Zou, T., Liu, L., Rao, J.N., Marasa, B.S., Chen, J., Xiao, L., Zhou, H., Gorospe, M. and Wang, J.Y. (2008) Polyamines modulate the subcellular localization of RNA-binding protein HuR through AMP-activated protein kinase-regulated phosphorylation and acetylation of importin-1. Biochem. J., 409, 389-398.
57. Wang, J.Y. and Johnson, L.R. (1991) Polyamines and ornithine decarboxylase during repair of duodenal mucosa after stress in rats. Gastroenterology, 100, 333-343.
58. Li, L., Rao, J.N., Guo, X., Liu, L., Santora, R., Bass, B.L. and Wang, J.Y. (2001) Polyamine depletion stabilizes p53 resulting in inhibition of normal intestinal epithelial cell proliferation. Am. J. Physiol. Cell Physiol., 281, C941-C953.
59. Mazan-Mamczarz, K., Hagner, P.R., Corl, S., Srikantan, S., Wood, W.H., Becker, K.G., Gorospe, M., Keene, J.D., Levenson, A.S. and Gartenhaus, R.B. (2008) Post-transcriptional gene regulation by HuR promotes a more tumorigenic phenotype. Oncogene, 27, 6151-6163.
60. Galbán, S., Kuwano, Y., Pullmann, R. Jr, Martindale, J.L., Kim, H.H., Lal, A., Abdelmohsen, K., Yang, X., Dang, Y., Liu, J.O. et al. (2008) RNA-binding proteins HuR and PTB promote the translation of hypoxia-inducible factor 1alpha. Mol. Cell. Biol., 28, 93-107.
61. Kuwano, Y., Kim, H.H., Abdelmohsen, K., Pullmann, R. Jr, Martindale, J.L., Yang, X. and Gorospe, M. (2008) MKP-1 mRNA stabilization and translational control by RNA-binding proteins HuR and NF90. Mol. Cell. Biol., 28, 4562-4575.
62. Lal, A., Kawai, T., Yang, X., Mazan-Mamczarz, K. and Gorospe, M. (2005) Antiapoptotic function of RNA-binding protein HuR effected through prothymosin-a. EMBO J., 24, 1852-1862.
63. Levy, N.S., Chung, S., Furneaux, H. and Levy, A.P. (1998) Hypoxic stabilization of vascular endothelial growth factor mRNA by the RNA-binding protein HuR. J. Biol. Chem., 273, 6417-6423.
64. Casero, R.A. Jr and Marton, L.J. (2007) Targeting polyamine metabolism and function in cancer and other hyperproliferative diseases. Nat. Rev. Drug Discov., 6, 373-390.