FRET-detectable interactions between the ARE binding proteins, HuR and p37AUF1

RNA

Volumn 13, Issue 9, 2007, Pages 1453-1468

  David, Pamela S ^a   Tanveer, Rasheeda ^a   Port, J David ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

ARE; AUF1; FRET; HuR; Protein protein interaction

Indexed keywords

ANISOMYCIN; BINDING PROTEIN; HETERODIMER; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN D; HOMODIMER; HUR PROTEIN; HYBRID PROTEIN; MESSENGER RNA; PROTEIN P37;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL COMPARTMENTALIZATION; CELL GRANULE; CELL LINE; CELL STRESS; CONTROLLED STUDY; FLUORESCENCE RESONANCE ENERGY TRANSFER; IMMUNOCYTOCHEMISTRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; VAS DEFERENS;

ANIMALS; ANTIGENS, SURFACE; CELL LINE; CELL NUCLEUS; CRICETINAE; CYTOPLASM; FLUORESCENCE RESONANCE ENERGY TRANSFER; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEIN D; HUMANS; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; RNA, MESSENGER; RNA-BINDING PROTEINS;

EID: 34548348186     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.501707     Document Type: Article

References (94)

1. Abdelmohsen, K., Pullmann Jr., R., 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.
2. Abraham, W.T., Gilbert, E.M., Lowes, B.D., Minobe, W.A., Larrabee, P., Roden, R.L., Dutcher, D., Sederberg, J., Lindenfeld, J.A., Wolfel, E.E., et al. 2002. Coordinate changes in Myosin heavy chain isoform gene expression are selectively associated with alterations in dilated cardiomyopathy phenotype. Mol. Med. 8: 750-760.
3. Anderson, P. and Kedersha, N. 2006. RNA granules. J. Cell Biol. 172: 803-808.
4. Atasoy, U., Watson, J., Patel, D., and Keene, J.D. 1998. ELAV protein HuA (HuR) can redistribute between nucleus and cytoplasm and is upregulated during serum stimulation and T cell activation. J. Cell Sci. 111: 3145-3156.
5. Bakheet, T., Williams, B.R., and Khabar, K.S. 2006. ARED 3.0: The large and diverse AU-rich transcriptome. Nucleic Acids Res. 34: D111-D114.
6. Blaxall, B.C., Dwyer-Nield, L.D., Bauer, A.K., Bohlmeyer, T.J., Malkinson, A.M., and Port, J.D. 2000a. Differential expression and localization of the mRNA binding proteins, AU-rich element mRNA binding protein (AUF1) and Hu antigen R (HuR), in neoplastic lung tissue. Mol. Carcinog. 28: 76-83.
7. Blaxall, B.C., Pellett, A.C., Wu, S.C., Pende, A., and Port, J.D. 2000b. Purification and characterization of β-adrenergic receptor mRNA-binding proteins. J. Biol. Chem. 275: 4290-4297.
8. Blaxall, B.C., Pende, A., Wu, S.C., and Port, J.D. 2002. Correlation between intrinsic mRNA stability and the affinity of AUF1 (hnRNP D) and HuR for A+U-rich mRNAs. Mol. Cell. Biochem. 232: 1-11.
9. Brengues, M., Teixeira, D., and Parker, R. 2005. Movement of eukaryotic mRNAs between polysomes and cytoplasmic processing bodies. Science 310: 486-489.
10. Brook, M., Tchen, C.R., Santalucia, T., McIlrath, J., Arthur, J.S., Saklatvala, J., and Clark, A.R. 2006. Posttranslational regulation of tristetraprolin subcellular localization and protein stability by p38 mitogen-activated protein kinase and extracellular signal-regulated kinase pathways. Mol. Cell. Biol. 26: 2408-2418.
11. Buzby, J.S., Lee, S.M., Van Winkle, P., DeMaria, C.T., Brewer, G., and Cairo, M.S. 1996. Increased granulocyte-macrophage colony-stimulating factor mRNA instability in cord versus adult mononuclear cells is translation dependent and associated with increased levels of A+U-rich element binding factor. Blood 88: 2889-2897.
12. Carballo, E., Lai, W.S., and Blackshear, P.J. 2000. Evidence that tristetraprolin is a physiological regulator of granulocyte-macrophage colony-stimulating factor messenger RNA deadenylation and stability. Blood 95: 1891-1899.
13. Chen, C.-Y., Xu, N., and Shyu, A.-B. 1995. mRNA decay is mediated by two distinct AU-rich elements from the c-fos and granulocyte-macrophage colony-stimulating factor transcripts: Different deadenylation kinetics and uncoupling from translation. Mol. Cell. Biol. 15: 5777-5788.
14. Cherradi, N., Lejczak, C., Desroches-Castan, A., and Feige, J.J. 2006. Antagonistic functions of tetradecanoyl phorbol acetate-inducible-sequence 11b and HuR in the hormonal regulation of vascular endothelial growth factor messenger ribonucleic acid stability by adrenocorticotropin. Mol. Endocrinol. 20: 916-930.
15. Chilibeck, K.A., Wu, T., Liang, C., Schellenberg, M.J., Gesner, E.M., Lynch, J.M., and MacMillan, A.M. 2006. FRET analysis of in vivo dimerization by RNA-editing enzymes. J. Biol. Chem. 281: 16530-16535.
16. Cougot, N., Babajko, S., and Seraphin, B. 2004. Cytoplasmic foci are sites of mRNA decay in human cells. J. Cell Biol. 165: 31-40.
17. Dean, J.L., Wait, R., Mahtani, K.R., Sully, G., Clark, A.R., and Saklatvala, J. 2001. The 3′-untranslated region of tumor necrosis factor α mRNA is a target of the mRNA-stabilizing factor HuR. Mol. Cell. Biol. 21: 721-730.
18. Dean, J.L.E., Sarsfield, S.J., Tsounakou, E., and Saklatvala, J. 2003. p38 mitogen-activated protein kinase stabilizes mRNAs that contain cyclooxygenase-2 and tumor necrosis factor AU-rich elements by inhibiting deadenylation. J. Biol. Chem. 278: 39470-39476.
19. DeMaria, C.T. and Brewer, G. 1996. AUF1 binding affinity to A+U-rich elements correlates with rapid mRNA degradation. J. Biol. Chem. 271: 12179-12184.
20. DeMaria, C.T., Sun, Y., Long, L., Wagner, B.J., and Brewer, G. 1997. Structural determinants in AUF1 required for high affinity binding to A+U-rich elements. J. Biol. Chem. 272: 27635-27643.
21. Doller, A., Huwiler, A., Muller, R., Radeke, H.H., Pfeilschifter, J., and Eberhardt, W. 2007. PKCα-dependent phosphorylation of the mRNA stabilizing factor HuR: Implications for posttranscriptional regulation of cyclooxygenase-2. Mol. Biol. Cell 18: 2137-2148.
22. Dreyfuss, G. 1986. Structure and function of nuclear and cytoplasmic ribonucleoprotein particles. Annu. Rev. Cell Biol. 2: 459-498.
23. Eulalio, A., Behm-Ansmant, I., and Izaurralde, E. 2007. P bodies: At the crossroads of post-transcriptional pathways. Nat. Rev. Mol. Cell Biol. 8: 9-22.
24. Fan, X.C. and Steitz, J.A. 1998a. HNS, a nuclear-cytoplasmic shuttling sequence in HuR. Proc. Natl. Acad. Sci. 95: 15293-15298.
25. Fan, X.C. and Steitz, J.A. 1998b. Overexpression of HuR, a nuclear-cytoplasmic shuttling protein, increases the in vivo stability of ARE-containing mRNAs. EMBO J. 17: 3448-3460.
26. Fawal, M., Armstrong, F., Ollier, S., Dupont, H., Touriol, C., Monsarrat, B., Delsol, G., Payrastre, B., and Morello, D. 2006. A "liaison dangereuse" between AUF1/hnRNPD and the oncogenic tyrosine kinase NPM-ALK. Blood 108: 2780-2788.
27. Fialcowitz, E.J., Brewer, B.Y., Keenan, B.P., and Wilson, G.M. 2005. A hairpin-like structure within an AU-rich mRNA-destabilizing element regulates trans-factor binding selectivity and mRNA decay kinetics. J. Biol. Chem. 280: 22406-22417.
28. Figueroa, A., Cuadrado, A., Fan, J., Atasoy, U., Muscat, G.E., Munoz-Canoves, P., Gorospe, M., and Munoz, A. 2003. Role of HuR in skeletal myogenesis through coordinate regulation of muscle differentiation genes. Mol. Cell. Biol. 23: 4991-5004.
29. Forster, T. 1948. Zwischenmolekulare energiewanderung und fluoreszenz. Ann. Phys. 2: 57-75.
30. Fries, B., Heukeshoven, J., Hauber, I., Gruttner, C., Stocking, C., Kehlenbach, R.H., Hauber, J., and Chemnitz, J. 2006. Analysis of nucleocytoplasmic trafficking of the Hur ligand APRIL and its influence on CD83 expression. J. Biol. Chem. 282: 4504-4515.
31. Gallouzi, I.E., Brennan, C.M., and Steitz, J.A. 2001. Protein ligands mediate the CRM1-dependent export of HuR in response to heat shock. RNA 7: 1348-1361.
32. Galperin, E. and Sorkin, A. 2003. Visualization of Rab5 activity in living cells by FRET microscopy and influence of plasma-membrane-targeted RAB5 on clathrin-dependent endocytosis. J. Cell Sci. 116: 4799-4810.
33. Galperin, E., Verkhusha, V.V., and Sorkin, A. 2004. Three-chromophore FRET microscopy to analyze multiprotein interactions in living cells. Nat. Methods 1: 209-217.
34. 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.
35. Gordon, G.W., Berry, G., Liang, X.H., Levine, B., and Herman, B. 1998. Quantitative fluorescence resonance energy transfer measurements using fluorescence microscopy. Biophys. J. 74: 2702-2713.
36. Gouble, A. and Morello, D. 2000. Synchronous and regulated expression of two AU-binding proteins, AUF1 and HuR, throughout murine development. Oncogene 19: 5377-5384.
37. Headley, V., Tanveer, R., Greene, S.M., Zweifach, A., and Port, J.D. 2004. Reciprocal regulation of β-adrenergic receptor mRNA stability by mitogen activated protein kinase activation and inhibition. Mol. Cell. Biochem. 285: 109-119.
38. Higashino, F., Aoyagi, M., Takahashi, A., Ishino, M., Taoka, M., Isobe, T., Kobayashi, M., Totsuka, Y., Kohgo, T., and Shindoh, M. 2005. Adenovirus E4orf6 targets pp32/LANP to control the fate of ARE-containing mRNAs by perturbing the CRM1-dependent mechanism. J. Cell Biol. 170: 15-20.
39. Kawamura, H., Tomozoe, Y., Akagi, T., Kamei, D., Ochiai, M., and Yamada, M. 2002. Identification of the nucleocytoplasmic shuttling sequence of heterogeneous nuclear ribonucleoprotein D-like protein JKTBP and its interaction with mRNA. J. Biol. Chem. 277: 2732-2739.
40. Kedersha, N. and Anderson, P. 2002. Stress granules: Sites of mRNA triage that regulate mRNA stability and translatability. Biochem. Soc. Trans. 30: 963-969.
41. Kedersha, N.L., Gupta, M., Li, W., Miller, I., and Anderson, P. 1999. RNA-binding proteins TIA-1 and TIAR link the phosphorylation of eIF-2 α to the assembly of mammalian stress granules. J. Cell Biol. 147: 1431-1442.
42. Kedersha, N., Cho, M.R., Li, W., Yacono, P.W., Chen, S., Gilks, N., Golan, D.E., and Anderson, P. 2000. Dynamic shuttling of TIA-1 accompanies the recruitment of mRNA to mammalian stress granules. J. Cell Biol. 151: 1257-1268.
43. 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.
44. Keene, J.D. and Lager, P.J. 2005. Post-transcriptional operons and regulons co-ordinating gene expression. Chromosome Res. 13: 327-337.
45. Kimura, T., Hashimoto, I., Nagase, T., and Fujisawa, J. 2004. CRM1-dependent, but not ARE-mediated, nuclear export of IFN-α1 mRNA. J. Cell Sci. 117: 2259-2270.
46. Kuersten, S. and Goodwin, E.B. 2005. Linking nuclear mRNP assembly and cytoplasmic destiny. Biol. Cell. 97: 469-478.
47. Lafon, I., Carballes, F., Brewer, G., Poiret, M., and Morello, D. 1998. Developmental expression of AUF1 and HuR, two c-myc mRNA binding proteins. Oncogene 16: 3413-3421.
48. Lal, A., Mazan-Mamczarz, K., Kawai, T., Yang, X., Martindale, J.L., and Gorospe, M. 2004. Concurrent versus individual binding of HuR and AUF1 to common labile target mRNAs. EMBO J. 23: 3092-3102.
49. Laroia, G. and Schneider, R.J. 2002. Alternate exon insertion controls selective ubiquitination and degradation of different AUF1 protein isoforms. Nucleic Acids Res. 30: 3052-3058.
50. Laroia, G., Cuesta, R., Brewer, G., and Schneider, R.J. 1999. Control of mRNA decay by heat shock-ubiquitin-proteasome pathway. Science 284: 499-502.
51. Lian, S., Jakymiw, A., Eystathioy, T., Hamel, J.C., Fritzler, M.J., and Chan, E.K. 2006. GW bodies, microRNAs and the cell cycle. Cell Cycle 5: 242-245.
52. Linker, K., Pautz, A., Fechir, M., Hubrich, T., Greeve, J., and Kleinert, H. 2005. Involvement of KSRP in the post-transcriptional regulation of human iNOS expression-complex interplay of KSRP with TTP and HuR. Nucleic Acids Res. 33: 4813-4827.
53. Lu, J.Y. and Schneider, R.J. 2004. Tissue distribution of AU-rich mRNA binding proteins involved in regulation of mRNA decay. J. Biol. Chem. 279: 12974-12979.
54. Ma, W.-J., Cheng, S., Campbell, C., Wright, A., and Furneaux, H. 1996. Cloning and characterization of HuR, a ubiquitously expressed elav-like protein. J. Biol. Chem. 271: 8144-8151.
55. Mahtani, K.R., Brook, M., Dean, J.L., Sully, G., Saklatvala, J., and Clark, A.R. 2001. Mitogen-activated protein kinase p38 controls the expression and posttranslational modification of tristetraprolin, a regulator of tumor necrosis factor a mRNA stability. Mol. Cell. Biol. 21: 6461-6469.
56. Maison, C., Bailly, D., Peters, A.H., Quivy, J.P., Roche, D., Taddei, A., Lachner, M., Jenuwein, T., and Almouzni, G. 2002. Higher-order structure in pericentric heterochromatin involves a distinct pattern of histone modification and an RNA component. Nat. Genet. 30: 329-334.
57. Martinez-Chantar, M.L., Vazquez-Chantada, M., Garnacho, M., Latasa, M.U., Varela-Rey, M., Dotor, J., Santamaria, M., Martinez-Cruz, L.A., Parada, L.A., Lu, S.C., et al. 2006. S-adenosylmethionine regulates cytoplasmic HuR via AMP-activated kinase. Gastroenterology 131: 223-232.
58. Mazan-Mamczarz, K., Galban, S., Lopez de Silanes, I., 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. 100: 8354-8359.
59. Ming, X.F., Stoecklin, G., Lu, M., Looser, R., and Moroni, C. 2001. Parallel and independent regulation of interleukin-3 mRNA turnover by phosphatidylinositol 3-kinase and p38 mitogen-activated protein kinase. Mol. Cell. Biol. 21: 5778-5789.
60. Moore, M.J. 2005. From birth to death: The complex lives of eukaryotic mRNAs. Science 309: 1514-1518.
61. Neininger, A., Kontoyiannis, D., Kotlyarov, A., Winzen, R., Eckert, R., Volk, H.-D., Holtmann, H., Kollias, G., and Gaestel, M. 2002. MK2 targets AU-rich elements and regulates biosynthesis of tumor necrosis factor and interleukin-6 independently at different post-transcriptional levels. J. Biol. Chem. 277: 3065-3068.
62. Newbury, S.F., Muhlemann, O., and Stoecklin, G. 2006. Turnover in the Alps: An mRNA perspective. Workshops on mechanisms and regulation of mRNA turnover. EMBO Rep. 7: 143-148.
63. Ogilvie, R.L., Abelson, M., Hau, H.H., Vlasova, I., Blackshear, P.J., and Bohjanen, P.R. 2005. Tristetraprolin down-regulates IL-2 gene expression through AU-rich element-mediated mRNA decay. J. Immunol. 174: 953-961.
64. Parker, R. and Song, H. 2004. The enzymes and control of eukaryotic mRNA turnover. Nat. Struct. Mol. Biol. 11: 121-127.
65. Pende, A., Tremmel, K.D., DeMaria, C.T., Blaxall, B.C., Minobe, W., Sherman, J.A., Bisognano, J., Bristow, M.R., Brewer, G., and Port, J.D. 1996. Regulation of the mRNA-binding protein AUF1 by activation of the b-adrenergic receptor signal transduction pathway. J. Biol. Chem. 271: 8493-8501.
66. Peng, S.S., Chen, C.Y., Xu, N., and Shyu, A.B. 1998. RNA stabilization by the AU-rich element binding protein, HuR, an ELAV protein. EMBO J. 17: 3461-3470.
67. Prechtel, A.T., Chemnitz, J., Schirmer, S., Ehlers, C., Langbein-Detsch, I., Stulke, J., Dabauvalle, M.C., Kehlenbach, R.H., and Hauber, J. 2006. Expression of CD83 is regulated by HuR via a novel cis-active coding region RNA element. J. Biol. Chem. 281: 10912-10925.
68. Raineri, I., Wegmueller, D., Gross, B., Certa, U., and Moroni, C. 2004. Roles of AUF1 isoforms, HuR and BRF1 in ARE-dependent mRNA turnover studied by RNA interference. Nucleic Acids Res. 32: 1279-1288.
69. Robinow, S. and White, K. 1988. The locus elav of Drosophila melanogaster is expressed in neurons at all developmental stages. Dev. Biol. 126: 294-303.
70. Sarkar, B., Lu, J.Y., and Schneider, R.J. 2003a. Nuclear import and export functions in the different isoforms of the AUF1/heterogeneous nuclear ribonucleoprotein protein family. J. Biol. Chem. 278: 20700-20707.
71. Sarkar, B., Xi, Q., He, C., and Schneider, R.J. 2003b. Selective degradation of AU-rich mRNAs promoted by the p37 AUF1 protein isoform. Mol. Cell. Biol. 23: 6685-6693.
72. Schmidlin, M., Lu, M., Leuenberger, S.A., Stoecklin, G., Mallaun, M., Gross, B., Gherzi, R., Hess, D., Hemmings, B.A., and Moroni, C. 2004. The ARE-dependent mRNA-destabilizing activity of BRF1 is regulated by protein kinase B. EMBO J. 23: 4760-4769.
73. Seko, Y., Azmi, H., Fariss, R., and Ragheb, J.A. 2004. Selective cytoplasmic translocation of HuR and site-specific binding to the interleukin-2 mRNA are not sufficient for CD28-mediated stabilization of the mRNA. J. Biol. Chem. 279: 33359-33367.
74. Shen, Z.J., Esnault, S., and Malter, J.S. 2005. The peptidyl-prolyl isomerase Pin1 regulates the stability of granulocyte-macrophage colony-stimulating factor mRNA in activated eosinophils. Nat. Immunol. 6: 1280-1287.
75. Sirenko, O.I., Lofquist, A.K., DeMaria, C.T., Morris, J.S., Brewer, G., and Haskill, J.S. 1997. Adhesion-dependent regulation of an A+U-rich element-binding activity associated with AUF1. Mol. Cell. Biol. 17: 3898-3906.
76. Soller, M. and White, K. 2005. ELAV multimerizes on conserved AU4-6 motifs important for ewg splicing regulation. Mol. Cell. Biol. 25: 7580-7591.
77. Stoecklin, G., Stoeckle, P., Lu, M., Muehlemann, O., and Moroni, C. 2001. Cellular mutants define a common mRNA degradation pathway targeting cytokine AU-rich elements. RNA 7: 1578-1588.
78. Stoecklin, G., Colombi, M., Raineri, I., Leuenberger, S., Mallaun, M., Schmidlin, M., Gross, B., Lu, M., Kitamura, T., and Moroni, C. 2002. Functional cloning of BRF1, a regulator of ARE-dependent mRNA turnover. EMBO J. 21: 4709-4718.
79. Stoecklin, G., Stubbs, T., Kedersha, N., Wax, S., Rigby, W.F., Blackwell, T.K., and Anderson, P. 2004. MK2-induced tristetraprolin: 14-3-3 complexes prevent stress granule association and ARE-mRNA decay. EMBO J. 23: 1313-1324.
80. Suzuki, M., Iijima, M., Nishimura, A., Tomozoe, Y., Kamei, D., and Yamada, M. 2005. Two separate regions essential for nuclear import of the hnRNP D nucleocytoplasmic shuttling sequence. FEBS J. 272: 3975-3987.
81. Taylor, G.A. and Blackshear, P.J. 1995. Zinc inhibits turnover of labile mRNAs in intact cells. J. Cell. Physiol. 162: 378-387.
82. Taylor, G.A., Carballo, E., Lee, D.M., Lai, W.S., Thompson, M.J., Patel, D.D., Schenkman, D.I., Gilkeson, G.S., Broxmeyer, H.E., Haynes, B.F., et al. 1996. A pathogenetic role for TNF α in the syndrome of cachexia, arthritis, and autoimmunity resulting from tristetraprolin (TTP) deficiency. Immunity 4: 445-454.
83. Tenenbaum, S.A., Lager, P.J., Carson, C.C., and Keene, J.D. 2002. Ribonomics: Identifying mRNA subsets in mRNP complexes using antibodies to RNA-binding proteins and genomic arrays. Methods 26: 191-198.
84. Vogel, S.S., Thaler, C., and Koushik, S.V. 2006. Fanciful FRET. Sci. STKE 2006: re2. doi: 10.1126/stke.3312006re2.
85. Wagner, B.J., DeMaria, C.T., Sun, Y., Wilson, G.M., and Brewer, G. 1998. Structure and genomic organization of the human AUF1 gene: Alternative pre-mRNA splicing generates four protein isoforms. Genomics 48: 195-202.
86. Wang, W., Caldwell, M.C., Lin, S., Furneaux, H., and Gorospe, M. 2000a. HuR regulates cyclin A and cyclin B1 mRNA stability during cell proliferation. EMBO J. 19: 2340-2350.
87. Wang, W., Furneaux, H., Cheng, H., Caldwell, M.C., Hutter, D., Liu, Y., Holbrook, N., and Gorospe, M. 2000b. HuR regulates p21 mRNA stabilization by UV light. Mol. Cell. Biol. 20: 760-769.
88. Wilson, G.M., Sun, Y., Lu, H., and Brewer, G. 1999. Assembly of AUF1 oligomers on U-rich RNA targets by sequential dimer association. J. Biol. Chem. 274: 33374-33381.
89. Wilson, G.M., Sutphen, K., Chuang, K., and Brewer, G. 2001a. Folding of A+U-rich RNA elements modulates AUF1 binding. Potential roles in regulation of mRNA turnover. J. Biol. Chem. 276: 8695-8704.
90. Wilson, G.M., Sutphen, K., Moutafis, M., Sinha, S., and Brewer, G. 2001b. Structural re-modeling of an A+U-rich RNA element by cation or AUF1 binding. J. Biol. Chem. 276: 38400-38409.
91. Wilson, G.M., Lu, J., Sutphen, K., Suarez, Y., Sinha, S., Brewer, B., Villanueva-Feliciano, E.C., Ysla, R.M., Charles, S., and Brewer, G. 2003a. Phosphorylation of p40AUF1 regulates binding to A+U-rich mRNA-destabilizing elements and protein-induced changes in ribonucleoprotein structure. J. Biol. Chem. 278: 33039-33048.
92. Wilson, G.M., Lu, J., Sutphen, K., Sun, Y., Huynh, Y., and Brewer, G. 2003b. Regulation of A+U-rich element-directed mRNA turnover involving reversible phosphorylation of AUF1. J. Biol. Chem. 278: 33029-33038.
93. Winzen, R., Kracht, M., Ritter, B., Wilhelm, A., Chen, C.Y., Shyu, A.B., Muller, M., Gaestel, M., Resch, K., and Holtmann, H. 1999. The p38 MAP kinase pathway signals for cytokine-induced mRNA stabilization via MAP kinase-activated protein kinase 2 and an AU-rich region-targeted mechanism. EMBO J. 18: 4969-4980.
94. Yang, E., van Nimwegen, E., Zavolan, M., Rajewsky, N., Schroeder, M., Magnasco, M., and Darnell Jr., J.E. 2003. Decay rates of human mRNAs: Correlation with functional characteristics and sequence attributes. Genome Res. 13: 1863-1872.