Direct binding of specific AUF1 isoforms to tandem zinc finger domains of tristetraprolin (TTP) family proteins

Journal of Biological Chemistry

Volumn 287, Issue 8, 2012, Pages 5459-5471

  Kedar, Vishram P ^a   Zucconi, Beth E ^b   Wilson, Gerald M ^b   Blackshear, Perry J ^a,c  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

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

^c DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AU-RICH ELEMENTS; BINDING AFFINITIES; CELL EXTRACTS; COACTIVATORS; DEADENYLATION; ELEMENT-BINDING PROTEINS; GEL SHIFT ASSAYS; INTERACTION DOMAIN; ISOFORMS; MRNA BINDING; PROTEIN BINDING; RATE-LIMITING STEPS; RECOMBINANT PROTEIN; TRISTETRAPROLIN; ZINC FINGER DOMAINS; ZINC FINGER PROTEIN;

BINDING ENERGY; BIOCHEMISTRY; PROBES; RNA; ZINC;

PROTEINS;

AUF1P37 PROTEIN; AUF1P45 PROTEIN; CELL EXTRACT; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN D; ISOPROTEIN; MUTANT PROTEIN; RECOMBINANT PROTEIN; RNA; TRISTETRAPROLIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; FLUORESCENCE RESONANCE ENERGY TRANSFER; GEL MOBILITY SHIFT ASSAY; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN RNA BINDING; RNA PROBE; TANDEM ZINC FINGER DOMAIN; TWO HYBRID SYSTEM;

ANIMALS; HEK293 CELLS; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEIN D; HUMANS; MICE; MUTATION; PROTEIN BINDING; PROTEIN ISOFORMS; PROTEIN STRUCTURE, TERTIARY; RNA PROBES; RNA, MESSENGER; SUBSTRATE SPECIFICITY; TRISTETRAPROLIN; TUMOR NECROSIS FACTOR-ALPHA; ZINC FINGERS;

EID: 84857340173     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.312652     Document Type: Article

References (52)

1. 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., and Blackshear, P. J. (1996) A pathogenetic role for TNF-α in the syndrome of cachexia, arthritis, and autoimmunity resulting from tristetraprolin (TTP) deficiency. Immunity 4, 445-454
2. Carballo, E., and Blackshear, P. J. (2001) Roles of tumor necrosis factor-αreceptor subtypes in the pathogenesis of the tristetraprolin- deficiency syndrome. Blood 98, 2389-2395
3. -/- mice. Evidence that monocyte/macrophage progenitors may be responsible for TNFα overproduction. J. Clin. Invest. 100, 986-995
4. Carballo, E., Lai, W. S., and Blackshear, P. J. (1998) Feedback inhibition of macrophage tumor necrosis factor-α production by tristetraprolin. Science 281, 1001-1005
5. Lai, W. S., Carballo, E., Strum, J. R., Kennington, E. A., Phillips, R. S., and Blackshear, P. J. (1999) Evidence that tristetraprolin binds to AU-rich elements and promotes the deadenylation and destabilization of tumor necrosis factor α mRNA. Mol. Cell. Biol. 19, 4311-4323
6. Lai, W. S., Carballo, E., Thorn, J. M., Kennington, E. A., and Blackshear, P. J. (2000) Interactions of CCCH zinc finger proteins with mRNA. Binding of tristetraprolin-related zinc finger proteins to AU-rich elements and destabilization of mRNA. J. Biol. Chem. 275, 17827-17837
7. Lai, W. S., and Blackshear, P. J. (2001) Interactions of CCCH zinc finger proteins with mRNA. Tristetraprolin-mediated AU-rich element-dependent mRNA degradation can occur in the absence of a poly(A) tail. J. Biol. Chem. 276, 23144-23154
8. Carballo, E., Lai, W. S., and Blackshear, P. J. (2000) Evidence that tristetraprolin is a physiological regulator of granulocyte-macrophage colonystimulating factor messenger RNA deadenylation and stability. Blood 95, 1891-1899
9. Caponigro, G., and Parker, R. (1995) Multiple functions for the poly(A)-binding protein in mRNA decapping and deadenylation in yeast. Genes Dev. 9, 2421-2432
10. Decker, C. J., and Parker, R. (1993) A turnover pathway for both stable and unstable mRNAs in yeast: evidence for a requirement for deadenylation. Genes Dev. 7, 1632-1643
11. Funakoshi, Y., Doi, Y., Hosoda, N., Uchida, N., Osawa, M., Shimada, I., Tsujimoto, M., Suzuki, T., Katada, T., and Hoshino, S. (2007) Mechanism of mRNA deadenylation. Evidence for a molecular interplay between translation termination factor eRF3 and mRNA deadenylases. Genes Dev. 21, 3135-3148
12. Goldstrohm, A. C., and Wickens, M. (2008) Multifunctional deadenylase complexes diversify mRNA control. Nat. Rev. Mol. Cell Biol. 9, 337-344
13. Lai, W. S., Carrick, D. M., and Blackshear, P. J. (2005) Influence of nonameric AU-rich tristetraprolin-binding sites on mRNA deadenylation and turnover. J. Biol. Chem. 280, 34365-34377
14. Lai, W. S., Kennington, E. A., and Blackshear, P. J. (2003) Tristetraprolin and its family members can promote the cell-free deadenylation of AU-rich element-containing mRNAs by poly(A) ribonuclease. Mol. Cell. Biol. 23, 3798-3812
15. Stumpo, D. J., Byrd, N. A., Phillips, R. S., Ghosh, S., Maronpot, R. R., Castranio, T., Meyers, E. N., Mishina, Y., and Blackshear, P. J. (2004) Chorioallantoic fusion defects and embryonic lethality resulting from disruption of Zfp36L1, a gene encoding a CCCH tandem zinc finger protein of the tristetraprolin family. Mol. Cell. Biol. 24, 6445-6455
16. Stumpo, D. J., Broxmeyer, H. E., Ward, T., Cooper, S., Hangoc, G., Chung, Y. J., Shelley, W. C., Richfield, E. K., Ray, M. K., Yoder, M. C., Aplan, P. D., and Blackshear, P. J. (2009) Targeted disruption of Zfp36l2, encoding a CCCH tandem zinc finger RNA-binding protein, results in defective hematopoiesis. Blood 114, 2401-2410
17. Kedar, V. P., Darby, M. K., Williams, J. G., and Blackshear, P. J. (2010) Phosphorylation of human tristetraprolin in response to its interaction with the Cbl interacting protein CIN85. PLoS One 5, e9588
18. 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
19. Lu, J. Y., Bergman, N., Sadri, N., and Schneider, R. J. (2006) Assembly of AUF1 with eIF4G-poly(A) binding protein complex suggests a translation function in AU-rich mRNA decay. RNA 12, 883-893
20. Zhang, W., Wagner, B. J., Ehrenman, K., Schaefer, A. W., DeMaria, C. T., Crater, D., DeHaven, K., Long, L., and Brewer, G. (1993) Purification, characterization, and cDNA cloning of an AU-rich element RNA-binding protein, AUF1. Mol. Cell. Biol. 13, 7652-7665
21. Brewer, G. (1991) An A + U-rich element RNA binding factor regulates c-myc mRNA stability in vitro. Mol. Cell. Biol. 11, 2460-2466
22. Zucconi, B. E., and Wilson, G. M. (2012) Modulation of neoplastic gene regulatory pathways by the RNA binding factor AUF1. Front Biosci. 17, 2307-2325
23. Doi, A., Shiosaka, T., Takaoka, Y., Yanagisawa, K., and Fujita, S. (1998) Molecular cloning of the cDNA encoding A + U-rich element RNA binding factor. Biochim. Biophys. Acta 1396, 51-56
24. Garrus, J. E., von Schwedler, U. K., Pornillos, O. W., Morham, S. G., Zavitz, K. H., Wang, H. E., Wettstein, D. A., Stray, K. M., Côté, M., Rich, R. L., Myszka, D. G., and Sundquist, W. I. (2001) Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding. Cell 107, 55-65
25. DeGrado-Warren, J., Dufford, M., Chen, J., Bartel, P. L., Shattuck, D., and Frech, G. C. (2008) Construction and characterization of a normalized yeast two-hybrid library derived from a human protein-coding clone collection. Biotechniques 44, 265-273
26. Lu, J. Y., Sadri, N., and Schneider, R. J. (2006) Endotoxic shock in AUF1 knockout mice mediated by failure to degrade proinflammatory cytokine mRNAs. Genes Dev. 20, 3174-3184
27. Carrick, D. M., Lai, W. S., and Blackshear, P. J. (2004) The tandem CCCH zinc finger protein tristetraprolin and its relevance to cytokine mRNA turnover and arthritis. Arthritis Res. Ther. 6, 248-264
28. Phillips, R. S., Ramos, S. B., and Blackshear, P. J. (2002) Members of the tristetraprolin family of tandem CCCH zinc finger proteins exhibit CRM1-dependent nucleocytoplasmic shuttling. J. Biol. Chem. 277, 11606-11613
29. Kedar, V., McDonough, H., Arya, R., Li, H. H., Rockman, H. A., and Patterson, C. (2004) Muscle-specific RING finger 1 is a bona fide ubiquitin ligase that degrades cardiac troponin I. Proc. Natl. Acad. Sci. U.S.A. 101, 18135-18140
30. Zucconi, B. E., Ballin, J. D., Brewer, B. Y., Ross, C. R., Huang, J., Toth, E. A., and Wilson, G. M. (2010) Alternatively expressed domains of AU-rich element RNA-binding protein 1 (AUF1) regulate RNA binding affinity, RNA-induced protein oligomerization, and the local conformation of bound RNA ligands. J. Biol. Chem. 285, 39127-39139
31. Wilson, G. M., Sutphen, K., Chuang, K., and Brewer, G. (2001) Folding of A+U-rich RNA elements modulates AUF1 binding. Potential roles in regulation of mRNA turnover. J. Biol. Chem. 276, 8695-8704
32. Brewer, B. Y., Malicka, J., Blackshear, P. J., and Wilson, G. M. (2004) RNA sequence elements required for high affinity binding by the zinc finger domain of tristetraprolin. Conformational changes coupled to the bipartite nature of AU-rich mRNA-destabilizing motifs. J. Biol. Chem. 279, 27870-27877
33. Lakowicz, J. R. (1999) Principles of Fluorescence Spectroscopy, pp. 367-394, Kluwer Academic/Plenum, New York
34. Wilson, G. M. (2005) in Reviews in Fluorescence (Geddes, C.D., and Lakowicz, J. R., eds) pp. 223-243, Vol. 2., Springer Science+Business Media, Inc., New York
35. Sandler, H., and Stoecklin, G. (2008) Control ofmRNAdecay by phosphorylation of tristetraprolin. Biochem. Soc. Trans. 36, 491-496
36. Guhaniyogi, J., and Brewer, G. (2001) Regulation of mRNA stability in mammalian cells. Gene 265, 11-23
37. Lai, W. S., Kennington, E. A., and Blackshear, P. J. (2002) Interactions of CCCH zinc finger proteins with mRNA. Non-binding tristetraprolin mutants exert an inhibitory effect on degradation of AU-rich element-containing mRNAs. J. Biol. Chem. 277, 9606-9613
38. Cao, H., Deterding, L. J., and Blackshear, P. J. (2007) Phosphorylation site analysis of the anti-inflammatory and mRNA-destabilizing protein tristetraprolin. Expert Rev. Proteomics 4, 711-726
39. Frederick, E. D., Ramos, S. B., and Blackshear, P. J. (2008) A unique C-terminal repeat domain maintains the cytosolic localization of the placentaspecific tristetraprolin family member ZFP36L3. J. Biol. Chem. 283, 14792-14800
40. Körner, C. G., and Wahle, E. (1997) Poly(A) tail shortening by a mammalian poly(A)-specific 3′-exoribonuclease. J. Biol. Chem. 272, 10448-10456
41. Kahvejian, A., Svitkin, Y. V., Sukarieh, R., M'Boutchou, M. N., and Sonenberg, N. (2005) Mammalian poly(A)-binding protein is a eukaryotic translation initiation factor that acts via multiple mechanisms. Genes Dev. 19, 104-113
42. Körner, C. G., Wormington, M., Muckenthaler, M., Schneider, S., Dehlin, E., and Wahle, E. (1998) The deadenylating nuclease (DAN) is involved in poly(A) tail removal during the meiotic maturation of Xenopus oocytes. EMBO J. 17, 5427-5437
43. Chen, C. Y., Gherzi, R., Ong, S. E., Chan, E. L., Raijmakers, R., Pruijn, G. J., Stoecklin, G., Moroni, C., Mann, M., and Karin, M. (2001) AU binding proteins recruit the exosome to degrade ARE-containing mRNAs. Cell 107, 451-464
44. Mazan-Mamczarz, K., Kuwano, Y., Zhan, M., White, E. J., Martindale, J. L., Lal, A., and Gorospe, M. (2009) Identification of a signature motif in target mRNAs of RNA-binding protein AUF1. Nucleic Acids Res. 37, 204-214
45. Hudson, B. P., Martinez-Yamout, M. A., Dyson, H. J., and Wright, P. E. (2004) Recognition of the mRNA AU-rich element by the zinc finger domain of TIS11d. Nat. Struct. Mol. Biol. 11, 257-264
46. Sadri, N., and Schneider, R. J. (2009) Auf1/Hnrnpd-deficient mice develop pruritic inflammatory skin disease. J. Invest. Dermatol. 129, 657-670
47. Lykke-Andersen, J., and Wagner, E. (2005) Recruitment and activation of mRNA decay enzymes by two ARE-mediated decay activation domains in the proteins TTP and BRF-1. Genes Dev. 19, 351-361
48. 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 α mRNA stability. Mol. Cell. Biol. 21, 6461-6469
49. Johnson, B. A., Stehn, J. R., Yaffe, M. B., and Blackwell, T. K. (2002) Cytoplasmic localization of tristetraprolin involves 14-3-3-dependent and -independent mechanisms. J. Biol. Chem. 277, 18029-18036
50. Jing, Q., Huang, S., Guth, S., Zarubin, T., Motoyama, A., Chen, J., Di Padova, F., Lin, S. C., Gram, H., and Han, J. (2005) Involvement of microRNA in AU-rich element-mediated mRNA instability. Cell 120, 623-634
51. Carman, J. A., and Nadler, S. G. (2004) Direct association of tristetraprolin with the nucleoporin CAN/Nup214. Biochem. Biophys. Res. Commun. 315, 445-449
52. Sun, L., Stoecklin, G., Van Way, S., Hinkovska-Galcheva, V., Guo, R. F., Anderson, P., and Shanley, T. P. (2007) Tristetraprolin (TTP)-14-3-3 complex formation protects TTP from dephosphorylation by protein phosphatase 2a and stabilizes tumor necrosis factor-α mRNA. J. Biol. Chem. 282, 3766-3777