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Tudor Domain Proteins in Development Jun Wei Pek1,*,‡, Amit Anand1 and Toshie Kai1,2,*

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Tudor Domain Proteins in Development Jun Wei Pek1,*,‡, Amit Anand1 and Toshie Kai1,2,* PRIMER 2255 Development 139, 2255-2266 (2012) doi:10.1242/dev.073304 © 2012. Published by The Company of Biologists Ltd Tudor domain proteins in development Jun Wei Pek1,*,‡, Amit Anand1 and Toshie Kai1,2,* Summary However, the factors that determine this specificity are still poorly Tudor domain proteins function as molecular adaptors, binding understood (Kim et al., 2006; Chen et al., 2011). Here, we focus methylated arginine or lysine residues on their substrates to primarily on the methyl-arginine-binding Tudor domain proteins promote physical interactions and the assembly of and their roles in RNA metabolism. The roles of lysine methylation macromolecular complexes. Here, we discuss the emerging in regulating histone and non-histone proteins have been recently roles of Tudor domain proteins during development, most reviewed (Zhang et al., 2012), so we will discuss only some notably in the Piwi-interacting RNA pathway, but also in other functions for methyl-lysine-binding Tudor domains. A list of Tudor aspects of RNA metabolism, the DNA damage response and domain proteins discussed here is given in Table 1. chromatin modification. Tudor domain proteins involved in RNA metabolism have been studied extensively, especially for their functions in germline and Key words: Tudor domain, RNA metabolism, Chromatin, piRNA gonadal development. These Tudor domain proteins harbor an ‘extended Tudor domain’ of ~180 amino acids, containing the 60 Introduction amino acid core Tudor domain, and interact with methylated The tudor gene was originally discovered in Drosophila arginines on target proteins. Structural analysis has shown that the melanogaster in 1985 in a screen for maternal factors that regulate Tudor domain binds to symmetrically dimethylated arginines with embryonic development or fertility (for a timeline, see Box 1) a higher affinity than its binding to asymmetrically dimethylated (Boswell and Mahowald, 1985). The Tudor protein contains 11 arginines (Liu et al., 2010a; Liu et al., 2010b). Arginine residue repeats of a domain, later termed the Tudor domain, that was methylation is catalyzed by enzymes known as protein arginine subsequently found to be present in many other proteins that methyltransferases (PRMTs) (Fig. 1B). Arginine can be methylated function in RNA metabolism (Ponting, 1997; Callebaut and by Type I and II PRMTs to form mono-methylated arginine. This Mornon, 1997). Over the past two decades, Tudor domain proteins mono-methylated form can then be further methylated by either a have emerged as a class of proteins that regulate not only multiple Type I or Type II PRMT to form an asymmetric or symmetric di- aspects of RNA metabolism – including RNA splicing and small methyl-arginine, respectively (Gary and Clarke, 1998; Bedford and RNA pathways – but also a number of other processes, such as Richard, 2005; Bedford and Clarke, 2009; Boulanger et al., 2004). histone modification and the DNA damage response (reviewed by Thus, PRMTs establish the methyl-arginine marks that are Chen et al., 2011; Siomi et al., 2010; Lasko, 2010; Thomson and recognized and bound by Tudor domain proteins. Recently, JMJ20 Lasko, 2005). Through these activities, Tudor domain proteins and JMJ22 (Jumonji domain-containing proteins) have been shown affect a wide variety of processes during development, including to function as histone arginine demethylases in Arabidopsis (Cho cell division, differentiation, genome stability and gametogenesis. et al., 2012); however, it remains unclear whether such an eraser of We present the current knowledge gained from studies in arginine methylation exists in animals. Lysine methylation and Drosophila melanogaster, mice and human cell lines regarding how demethylation are catalyzed by lysine methyltransferases (KMTs) the Tudor domain functions and the roles of different Tudor domain and demethylases (LSDs), respectively (Fig. 1C) (Zhang and proteins in biological pathways. Reinberg, 2001; Zhang et al., 2012). A common function of Tudor domain proteins is to act as an Tudor domain proteins function as adaptor ‘adaptor’ that links methylated arginine or lysine marks to proteins ‘effectors’ with specific catalytic activities. A minority of Tudor The Tudor domain is a conserved protein structural motif of ~60 domain proteins containing only Tudor domains function as amino acids that is characterized by a strongly bent anti-parallel - adaptors that recruit downstream effectors (Table 1). The rest of the sheet composed of five -strands with a barrel-like fold (Sprangers family contain additional catalytic, enzymatic or functional et al., 2003). The Tudor domain has been reported to recognize and domains (e.g. nuclease or RNA helicase domains) and may bind methylated lysines and arginines of target substrates (Fig. 1A), themselves also function as effectors. This theme will be seen and this is thought to be the key in their ability to facilitate the recurrently in the following sections, as we discuss the functions of assembly of protein complexes at discrete cellular compartments different Tudor domain proteins in various biological processes. (Friberg et al., 2009; Liu et al., 2010a; Liu et al., 2010b; Tripsianes et al., 2011). A subset of Tudor domain proteins bind methylated Tudor domain proteins in RNA metabolism lysines, whereas the rest have methyl-arginine-binding capacity. Tudor domain proteins have been found to be involved in many processes that regulate the metabolism of RNA molecules, such as RNA processing, stability and translation. To target RNAs, Tudor 1Temasek Life Sciences Laboratory, 1 Research Link, National University of Singapore, Singapore 117604. 2Department of Biological Sciences, National University of domain proteins typically contain RNA-binding motifs themselves Singapore, 14 Science Drive 4, Singapore 117604. or bind to di-methylated arginines of proteins that are directly bound to RNAs. Below, we discuss prominent examples that *Authors for correspondence ([email protected]; [email protected]) ‡Present address: Carnegie Institute for Science, Department of Embryology, 3250 display the diversity of Tudor domain functions in RNA San Martin Drive, Baltimore, MD 21218, USA. metabolism. DEVELOPMENT 2256 PRIMER Development 139 (13) miRNA and siRNA pathways Box 1. Timeline of the major discoveries on Tudor The miRNA pathway regulates cellular functions ranging from cell domains division, differentiation and embryogenesis to regeneration 1985. Discovery of tudor in Drosophila. The gene was named after (Hatfield et al., 2005; Li and Carthew, 2005; Bushati et al., 2008; an extinct English royal family, the Tudors, for its grandchildless Pek et al., 2009; Yin et al., 2008). In this pathway, endogenous phenotype in which mutant females produce embryos with defects in primordial germ cell specification (Boswell and Mahowald, 1985). hairpin transcripts are processed into mature 22-nucleotide 1997. Identification of conserved Tudor domain (Ponting, 1997; miRNAs. These short single-stranded RNAs target mRNAs via Callebaut and Mornon, 1997). base pairing between the seed sequence of the miRNA and the 2001. SMN binds symmetric dimethylated arginines in spliceosomal mRNA – most often but not always at the 3Ј UTR. This results in SM proteins (Friesen et al., 2001; Brahms et al., 2001). Tudor inhibition of gene expression, by either translational repression or domain structure solved (Selenko et al., 2001). mRNA degradation (Fig. 3) (Liu et al., 2005; Guo et al., 2010). 2003. Tudor domain ‘royal’ family defined to also include Tudor, Another form of small RNA regulation occurs via the siRNA MBT, PWWP, chromo and plant Agenet domains (Maurer-Stroh et pathway. Double-stranded RNAs, either exogenous or from al., 2003). endogenous double-stranded RNA encoding loci, are processed 2005. Tudor domain proposed to recognize methyl-arginines (Cote into exo- or endo-siRNAs of a specific length (between 20 and 25 and Richard, 2005). 2006. Tudor domain proposed to recognize methyl-lysine (Kim et nucleotides, depending on species), which silence their targets by al., 2006). post-transcriptional and transcriptional means (Fig. 3). The 2006. Structure of Tudor domain bound to methyl-lysine solved siRNA/endo-siRNA pathways are important for combating (Huang et al., 2006; Botuyan et al., 2006). exogenous viral infections and endogenous retrotransposon 2009. Germline Tudor domain proteins shown to recognize activities, robust embryonic development and mitotic chromosome methylated Piwi proteins (Kirino et al., 2009; Reuter et al., 2009; segregation (Chung et al., 2008; Czech et al., 2008; Ghildiyal et al., Wang et al., 2009; Vagin et al., 2009; Chen et al., 2009; Nishida et 2008; Kawamura et al., 2008; van Rij et al., 2006; Wang et al., al., 2009). 2006; Galiana-Arnoux et al., 2006; Lucchetta et al., 2009; Pek and 2010. Structure of Tudor domain bound to methyl-arginine solved Kai, 2011a). (Liu et al., 2010a; Liu et al., 2010b). The effector of both the miRNA and siRNA pathways is the RNA-induced silencing complex (RISC), which contains the protein Argonaute as a key catalytic component. In Drosophila, Splicing mammals and Caenorhabditis elegans, RISC also contains the In higher eukaryotes, splicing to remove introns from pre-mRNAs is Tudor-SN protein, which contains a Tudor domain and four a highly coordinated and regulated event catalyzed by small nuclear nuclease domains (Table 1) (Caudy et al., 2003). Structural studies ribonucleoproteins (snRNPs) (Han et al., 2011). snRNPs are on Drosophila Tudor-SN have shown
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