The Arabidopsis thaliana tandem zinc finger 1 (AtTZF1) protein in RNA binding and decay

Plant Journal

Volumn 78, Issue 3, 2014, Pages 452-467

  Qu, Jie ^a   Kang, Shin Gene ^a   Wang, Wei ^a   Musier Forsyth, Karin ^a   Jang, Jyan Chyun ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

Arabidopsis thaliana; arginine rich (RR) motif; AtTZF1; AU rich elements; protein RNA interaction; RNA turnover; tandem CCCH zinc finger (TZF) motif

Indexed keywords

ARGININE; ELECTROPHORETIC MOBILITY; GENE EXPRESSION; HTTP; PLANTS (BOTANY); PROTEINS; ZINC;

ARABIDOPSIS THALIANA; ARGININE-RICH (RR) MOTIF; ATTZF1; AU-RICH ELEMENTS; PROTEIN-RNA INTERACTION; ZINC FINGER;

RNA;

ARABIDOPSIS THALIANA;

ARABIDOPSIS PROTEIN; GLUTATHIONE TRANSFERASE; HYBRID PROTEIN; PLANT RNA; TRANSCRIPTION FACTOR; TRISTETRAPROLIN; TZF1 PROTEIN, ARABIDOPSIS; ZFP36 PROTEIN, HUMAN; ZINC FINGER PROTEIN;

ARABIDOPSIS; AU RICH ELEMENT; BINDING SITE; FLUORESCENCE POLARIZATION; GENETICS; METABOLISM; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; PROTEIN MOTIF; RNA STABILITY;

AMINO ACID MOTIFS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; AU RICH ELEMENTS; BASE SEQUENCE; BINDING SITES; FLUORESCENCE POLARIZATION; GLUTATHIONE TRANSFERASE; MOLECULAR SEQUENCE DATA; MUTATION; RECOMBINANT FUSION PROTEINS; RNA STABILITY; RNA, PLANT; TRANSCRIPTION FACTORS; TRISTETRAPROLIN; ZINC FINGERS;

EID: 84899652722     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12485     Document Type: Article

References (78)

1. Barreau, C., Paillard, L., and, Osborne, H.B., (2005) AU-rich elements and associated factors: are there unifying principles? Nucleic Acids Res. 33, 7138-7150.
2. Bayer, T.S., Booth, L.N., Knudsen, S.M., and, Ellington, A.D., (2005) Arginine-rich motifs present multiple interfaces for specific binding by RNA. RNA, 11, 1848-1857.
3. Berg, J.M., and, Shi, Y., (1996) The galvanization of biology: a growing appreciation for the roles of zinc. Science, 271, 1081-1085.
4. Blackshear, P.J., (1984) Systems for polyacrylamide gel electrophoresis. Methods Enzymol. 104, 237-255.
5. Blackshear, P.J., (2002) Tristetraprolin and other CCCH tandem zinc-finger proteins in the regulation of mRNA turnover. Biochem. Soc. Trans. 30, 945-952.
6. Blackshear, P.J., Lai, W.S., Kennington, E.A., Brewer, G., Wilson, G.M., Guan, X., and, Zhou, P., (2003) Characteristics of the interaction of a synthetic human tristetraprolin tandem zinc finger peptide with AU-rich element-containing RNA substrates. J. Biol. Chem. 278, 19947-19955.
7. Blackshear, P.J., Phillips, R.S., and, Lai, W.S., (2005) Tandem CCCH Zinc Finger Proteins in mRNA Binding Georgetown. New York: Kluwer Academic/Plenum Publishers.
8. 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.
9. Brooks, S.A., and, Blackshear, P.J., (2013) Tristetraprolin (TTP): interactions with mRNA and proteins, and current thoughts on mechanisms of action. Biochim. Biophys. Acta 1829, 666-679.
10. 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.
11. Cuenca, A.A., Schetter, A., Aceto, D., Kemphues, K., and, Seydoux, G., (2003) Polarization of the C. elegans zygote proceeds via distinct establishment and maintenance phases. Development, 130, 1255-1265.
12. Czechowski, T., Stitt, M., Altmann, T., Udvardi, M.K., and, Scheible, W.R., (2005) Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol. 139, 5-17.
13. Dannull, J., Surovoy, A., Jung, G., and, Moelling, K., (1994) Specific binding of HIV-1 nucleocapsid protein to PSI RNA in vitro requires N-terminal zinc finger and flanking basic amino acid residues. EMBO J. 13, 1525-1533.
14. Delaney, K.J., Xu, R., Zhang, J., Li, Q.Q., Yun, K.Y., Falcone, D.L., and, Hunt, A.G., (2006) Calmodulin interacts with and regulates the RNA-binding activity of an Arabidopsis polyadenylation factor subunit. Plant Physiol. 140, 1507-1521.
15. DeRenzo, C., Reese, K.J., and, Seydoux, G., (2003) Exclusion of germ plasm proteins from somatic lineages by cullin-dependent degradation. Nature, 424, 685-689.
16. DuBois, R.N., McLane, M.W., Ryder, K., Lau, L.F., and, Nathans, D., (1990) A growth factor-inducible nuclear protein with a novel cysteine/histidine repetitive sequence. J. Biol. Chem. 265, 19185-19191.
17. Fabian, M.R., Frank, F., Rouya, C., Siddiqui, N., Lai, W.S., Karetnikov, A., Blackshear, P.J., Nagar, B., and, Sonenberg, N., (2013) Structural basis for the recruitment of the human CCR4-NOT deadenylase complex by tristetraprolin. Nat. Struct. Mol. Biol. 20, 735-739.
18. Farley, B.M., Pagano, J.M., and, Ryder, S.P., (2008) RNA target specificity of the embryonic cell fate determinant POS-1. RNA, 14, 2685-2697.
19. Garneau, N.L., Wilusz, J., and, Wilusz, C.J., (2007) The highways and byways of mRNA decay. Nat. Rev. Mol. Cell Biol. 8, 113-126.
20. Guan, K.L., and, Dixon, J.E., (1991) Eukaryotic proteins expressed in Escherichia coli: an improved thrombin cleavage and purification procedure of fusion proteins with glutathione S-transferase. Anal. Biochem. 192, 262-267.
21. Gutierrez, R.A., Ewing, R.M., Cherry, J.M., and, Green, P.J., (2002) Identification of unstable transcripts in Arabidopsis by cDNA microarray analysis: rapid decay is associated with a group of touch- and specific clock-controlled genes. Proc. Natl Acad. Sci. USA, 99, 11513-11518.
22. Heximer, S.P., and, Forsdyke, D.R., (1993) A human putative lymphocyte G0/G1 switch gene homologous to a rodent gene encoding a zinc-binding potential transcription factor. DNA Cell Biol. 12, 73-88.
23. Heyduk, T., Ma, Y., Tang, H., and, Ebright, R.H., (1996) Fluorescence anisotropy: rapid, quantitative assay for protein-DNA and protein-protein interaction. Methods Enzymol. 274, 492-503.
24. 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.
25. Jan, A., Maruyama, K., Todaka, D., Kidokoro, S., Abo, M., Yoshimura, E., Shinozaki, K., Nakashima, K., and, Yamaguchi-Shinozaki, K., (2013) OsTZF1, a CCCH-tandem zinc finger protein, confers delayed senescence and stress tolerance in rice by regulating stress-related genes. Plant Physiol. 161, 1202-1216.
26. Jang, J.C., Fujioka, S., Tasaka, M., Seto, H., Takatsuto, S., Ishii, A., Aida, M., Yoshida, S., and, Sheen, J., (2000) A critical role of sterols in embryonic patterning and meristem programming revealed by the fackel mutants of Arabidopsis thaliana. Genes Dev., 14, 1485-1497.
27. Jenkins, T.H., Li, J., Scutt, C.P., and, Gilmartin, P.M., (2005) Analysis of members of the Silene latifolia Cys2/His2 zinc-finger transcription factor family during dioecious flower development and in a novel stamen-defective mutant ssf1. Planta, 220, 559-571.
28. Kim, J., and, Somers, D.E., (2010) Rapid assessment of gene function in the circadian clock using artificial microRNA in Arabidopsis mesophyll protoplasts. Plant Physiol. 154, 611-621.
29. Kim, D.H., Yamaguchi, S., Lim, S., Oh, E., Park, J., Hanada, A., Kamiya, Y., and, Choi, G., (2008) SOMNUS, a CCCH-type zinc finger protein in Arabidopsis, negatively regulates light-dependent seed germination downstream of PIL5. Plant Cell, 20, 1260-1277.
30. Klug, A., and, Schwabe, J.W., (1995) Protein motifs 5. Zinc fingers. FASEB J. 9, 597-604.
31. Kong, Z., Li, M., Yang, W., Xu, W., and, Xue, Y., (2006) A novel nuclear-localized CCCH-type zinc finger protein, OsDOS, is involved in delaying leaf senescence in rice. Plant Physiol. 141, 1376-1388.
32. Kruger, N.J., (2002) The Bradford Method for Protein Quantification. In The Protein Protocols Handbook, 2nd edn (, Walker, J.M., ed.). Totowa: Humana Press Inc, pp. 15-21.
33. 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.
34. Lai, W.S., Stumpo, D.J., and, Blackshear, P.J., (1990) Rapid insulin-stimulated accumulation of an mRNA encoding a proline-rich protein. J. Biol. Chem. 265, 16556-16563.
35. 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 alpha mRNA. Mol. Cell. Biol. 19, 4311-4323.
36. 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.
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. Lai, W.S., Perera, L., Hicks, S.N., and, Blackshear, P.J., (2013) Mutational and structural analysis of the tandem zinc finger domain of tristetraprolin. J. Biol. Chem. 289, 565-580.
39. Laity, J.H., Lee, B.M., and, Wright, P.E., (2001) Zinc finger proteins: new insights into structural and functional diversity. Curr. Opin. Struct. Biol. 11, 39-46.
40. Lee, S.J., Jung, H.J., Kang, H., and, Kim, S.Y., (2012) Arabidopsis zinc finger proteins AtC3H49/AtTZF3 and AtC3H20/AtTZF2 are involved in ABA and JA responses. Plant Cell Physiol. 53, 673-686.
41. Li, Z., and, Thomas, T.L., (1998) PEI1, an embryo-specific zinc finger protein gene required for heart-stage embryo formation in Arabidopsis. Plant Cell, 10, 383-398.
42. Licatalosi, D.D., and, Darnell, R.B., (2010) RNA processing and its regulation: global insights into biological networks. Nat. Rev. Genet. 11, 75-87.
43. Lin, P.C., Pomeranz, M.C., Jikumaru, Y., Kang, S.G., Hah, C., Fujioka, S., Kamiya, Y., and, Jang, J.C., (2011) The Arabidopsis tandem zinc finger protein AtTZF1 affects ABA- and GA-mediated growth, stress and gene expression responses. Plant J. 65, 253-268.
44. Livak, K.J., and, Schmittgen, T.D., (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods, 25, 402-408.
45. Lunde, B.M., Moore, C., and, Varani, G., (2007) RNA-binding proteins: modular design for efficient function. Nat. Rev. Mol. Cell Biol. 8, 479-490.
46. Ma, Q., and, Herschman, H.R., (1991) A corrected sequence for the predicted protein from the mitogen-inducible TIS11 primary response gene. Oncogene, 6, 1277-1278.
47. Martin, K.C., and, Ephrussi, A., (2009) mRNA localization: gene expression in the spatial dimension. Cell, 136, 719-730.
48. Mathieu, O., Yukawa, Y., Prieto, J.L., Vaillant, I., Sugiura, M., and, Tourmente, S., (2003) Identification and characterization of transcription factor IIIA and ribosomal protein L5 from Arabidopsis thaliana. Nucleic Acids Res. 31, 2424-2433.
49. Moore, M., and, Ullman, C., (2003) Recent developments in the engineering of zinc finger proteins. Brief. Funct. Genomic. Proteomic. 1, 342-355.
50. Muench, D.G., Zhang, C., and, Dahodwala, M., (2012) Control of cytoplasmic translation in plants. Wiley Interdiscip. Rev. RNA, 3, 178-194.
51. Narsai, R., Howell, K.A., Millar, A.H., O'Toole, N., Small, I., and, Whelan, J., (2007) Genome-wide analysis of mRNA decay rates and their determinants in Arabidopsis thaliana. Plant Cell, 19, 3418-3436.
52. Pagano, J.M., Farley, B.M., McCoig, L.M., and, Ryder, S.P., (2007) Molecular basis of RNA recognition by the embryonic polarity determinant MEX-5. J. Biol. Chem. 282, 8883-8894.
53. Pedro-Segura, E., Vergara, S.V., Rodriguez-Navarro, S., Parker, R., Thiele, D.J., and, Puig, S., (2008) The Cth2 ARE-binding protein recruits the Dhh1 helicase to promote the decay of succinate dehydrogenase SDH4 mRNA in response to iron deficiency. J. Biol. Chem. 283, 28527-28535.
54. Pomeranz, M.C., Hah, C., Lin, P.C., Kang, S.G., Finer, J.J., Blackshear, P.J., and, Jang, J.C., (2010) The Arabidopsis tandem zinc finger protein AtTZF1 traffics between the nucleus and cytoplasmic foci and binds both DNA and RNA. Plant Physiol. 152, 151-165.
55. Pomeranz, M., Finer, J., and, Jang, J.C., (2011a) Putative molecular mechanisms underlying tandem CCCH zinc finger protein mediated plant growth, stress, and gene expression responses. Plant Signal. Behav. 6, 647-651.
56. Pomeranz, M., Zhang, L., Finer, J., and, Jang, J.C., (2011b) Can AtTZF1 act as a transcriptional activator or repressor in plants? Plant Signal. Behav. 6, 719-722.
57. Puig, S., Askeland, E., and, Thiele, D.J., (2005) Coordinated remodeling of cellular metabolism during iron deficiency through targeted mRNA degradation. Cell, 120, 99-110.
58. Puig, S., Vergara, S.V., and, Thiele, D.J., (2008) Cooperation of two mRNA-binding proteins drives metabolic adaptation to iron deficiency. Cell Metab. 7, 555-564.
59. Raghavan, A., Robison, R.L., McNabb, J., Miller, C.R., Williams, D.A., and, Bohjanen, P.R., (2001) HuA and tristetraprolin are induced following T cell activation and display distinct but overlapping RNA binding specificities. J. Biol. Chem. 276, 47958-47965.
60. Ross, J., (1995) mRNA stability in mammalian cells. Microbiol. Rev. 59, 423-450.
61. Schmalzbauer, E., Strack, B., Dannull, J., Guehmann, S., and, Moelling, K., (1996) Mutations of basic amino acids of NCp7 of human immunodeficiency virus type 1 affect RNA binding in vitro. J. Virol. 70, 771-777.
62. Schubert, C.M., Lin, R., de Vries, C.J., Plasterk, R.H., and, Priess, J.R., (2000) MEX-5 and MEX-6 function to establish soma/germline asymmetry in early C. elegans embryos. Mol. Cell, 5, 671-682.
63. Schumann, U., Prestele, J., O'Geen, H., Brueggeman, R., Wanner, G., and, Gietl, C., (2007) Requirement of the C3HC4 zinc RING finger of the Arabidopsis PEX10 for photorespiration and leaf peroxisome contact with chloroplasts. Proc. Natl Acad. Sci. USA, 104, 1069-1074.
64. Sheen, J., (2001) Signal transduction in maize and Arabidopsis mesophyll protoplasts. Plant Physiol. 127, 1466-1475.
65. Stewart-Maynard, K.M., Cruceanu, M., Wang, F., Vo, M.N., Gorelick, R.J., Williams, M.C., Rouzina, I., and, Musier-Forsyth, K., (2008) Retroviral nucleocapsid proteins display nonequivalent levels of nucleic acid chaperone activity. J. Virol. 82, 10129-10142.
66. Sun, J., Jiang, H., Xu, Y., Li, H., Wu, X., Xie, Q., and, Li, C., (2007) The CCCH-type zinc finger proteins AtSZF1 and AtSZF2 regulate salt stress responses in Arabidopsis. Plant Cell Physiol. 48, 1148-1158.
67. Takatsuji, H., (1998) Zinc-finger transcription factors in plants. Cell. Mol. Life Sci. 54, 582-596.
68. Tam, P.P., Barrette-Ng, I.H., Simon, D.M., Tam, M.W., Ang, A.L., and, Muench, D.G., (2010) The Puf family of RNA-binding proteins in plants: phylogeny, structural modeling, activity and subcellular localization. BMC Plant Biol. 10, 44.
69. Vargas, D.Y., Raj, A., Marras, S.A., Kramer, F.R., and, Tyagi, S., (2005) Mechanism of mRNA transport in the nucleus. Proc. Natl Acad. Sci. USA, 102, 17008-17013.
70. Vergara, S.V., Puig, S., and, Thiele, D.J., (2011) Early recruitment of AU-rich element-containing mRNAs determines their cytosolic fate during iron deficiency. Mol. Cell. Biol. 31, 417-429.
71. Walia, R.R., Caragea, C., Lewis, B.A., Towfic, F., Terribilini, M., El-Manzalawy, Y., Dobbs, D., and, Honavar, V., (2012) Protein-RNA interface residue prediction using machine learning: an assessment of the state of the art. BMC Bioinformatics, 13, 89.
72. Wang, L., and, Brown, S.J., (2006) BindN: a web-based tool for efficient prediction of DNA and RNA binding sites in amino acid sequences. Nucleic Acids Res. 34, W243-W248.
73. Wang, D., Guo, Y., Wu, C., Yang, G., Li, Y., and, Zheng, C., (2008) Genome-wide analysis of CCCH zinc finger family in Arabidopsis and rice. BMC Genomics, 9, 44.
74. Wells, D.G., (2012) mRNA translation: regulating an out of soma experience. Curr. Opin. Cell Biol. 24, 554-557.
75. Westermeier, R., (2006) Sensitive, quantitative, and fast modifications for Coomassie Blue staining of polyacrylamide gels. Proteomics, 6 (Suppl 2), 61-64.
76. Worthington, M.T., Amann, B.T., Nathans, D., and, Berg, J.M., (1996) Metal binding properties and secondary structure of the zinc-binding domain of Nup475. Proc. Natl Acad. Sci. USA 93, 13754-13759.
77. Worthington, M.T., Pelo, J.W., Sachedina, M.A., Applegate, J.L., Arseneau, K.O., and, Pizarro, T.T., (2002) RNA binding properties of the AU-rich element-binding recombinant Nup475/TIS11/tristetraprolin protein. J. Biol. Chem. 277, 48558-48564.
78. Zhang, C., Zhang, F., Zhou, J., Fan, Z., Chen, F., Ma, H., and, Xie, X., (2012) Overexpression of a phytochrome-regulated tandem zinc finger protein gene, OsTZF1, confers hypersensitivity to ABA and hyposensitivity to red light and far-red light in rice seedlings. Plant Cell Rep. 31, 1333-1343.