Table 1. Crystal structures solved for Lsm assemblies (to 2010)1Proteins are named by the first letters of the species, followed by the type of protein. Asterisked entries indicate structures solved in the presence of RNA. 2Hypothetical protein adopting an Lsm fold.3Structure deposited without supporting publication.
1. Introduction
It is today recognized that the vast majority of the cellular pool of RNA (nearly 98% in humans) comprises non-coding RNA (ncRNA) species (Mattick, 2001), with only a small proportion serving as direct template for protein synthesis. The diverse ncRNA forms are themselves capable of function, involved in a plethora of tasks such as protein scaffolding,
Various types of ncRNA, as well as RNPs containing tRNA, rRNA or snRNA, directly interact with mRNA at different stages of its life. Figure 1 presents an overview of the maturation of pre-mRNA and the fate of the mRNA generated. Pre-mRNA initially undergoes modification to enhance its stability: a 5’ methyl guanosine (m7G) cap added during transcription (Wen & Shatkin, 1999) and a poly(A)-tail placed in the 3’ region by the polyadenylation machinery (Proudfoot et al., 2002; Balbo & Bohm, 2007). Following initiation of spliceosomal assembly by recruitment of core particles in the cytoplasm, non-coding introns are spliced from the pre-mRNA sequence by the mature spliceosome in the nucleus (Crick, 1979; Pozzoli et al., 2002). This multi-megadalton complex itself contains 170 protein components and various types of snRNA, rivaling the ribosome in molecular complexity (Wahl et al., 2009).
Within the spliceosome, several distinct small nuclear RNP (snRNP) core complexes each contain snRNA organized around specific ring-structured protein assemblies. For those known as U1-, U2-, U4- and U5-snRNPs, these ring scaffolds are provided by members of the Sm protein family (Luhrmann et al., 1990), recruited to their specific snRNA partners in the cytoplasm at a distinct Sm-site of bases (Urlaub et al., 2001; Peng & Gallwitz 2004). The core snRNPs are reimported into the nucleus for further processing and spliceosome assembly (Will & Luhrmann, 2001; Patel & Bellini 2008). In contrast, U6 snRNA is first modified within the nucleoli and then engages with a related protein ring, in this case containing Lsm (“Sm-like”) proteins Lsm2-Lsm8. Together with the U1-U5 particles, the U6 snRNP is translocated to Cajal bodies for formation of the U4/U6*U5 tri-snRNP (Patel & Bellini, 2008). The mature snRNPs eventually assemble on pre-mRNA for intron removal steps (Will & Luhrmann, 2001; Patel & Bellini 2008).
Following excision of introns, mRNA enters the cytoplasm via the nuclear pore complex to be either translated or degraded. In eukaryotes, two pathways are utilized for mRNA decay: i) 3’-to-5’ degradation by the exosome or ii) 5’-decapping, followed by 5’-to-3’ exonuclease degradation (Garneau et al., 2007). In either event, decay is initiated by shortening of the poly(A)-tail by deadenylases (Tucker et al., 2001; Garneau et al., 2007; Nissan et al., 2010). Protein machinery required for the 5’-decapping pathway is found enriched in cytoplasmic foci known as processing or P-bodies (Sheth & Parker 2003), which appear to control the sorting and storage of mRNA. Within P-bodies, a specific assembly of Lsm proteins (Lsm1-Lsm7) and ancilliary protein factors expedites mRNA decapping and subsequent breakdown by ribonuclease (Nissan et al., 2010). While the extent to which mRNA decay is restricted to P-bodies is unclear, sequestered mRNA species are observed to leave P-bodies and may re-enter translation (Brengues et al., 2005).
2. Phylogeny of Lsm protein sequences
The Lsm proteins recur as molecular chaperones for RNA during the many steps of its processing, sorting and regulation (Beggs, 2005). While Sm proteins were first found enriched in a patient with systemic lupus erythematosis (Lerner & Steitz 1979), the wider protein family has since been described across all domains of life (Beggs, 2005; Ma et al., 2005). Members include eukaryotic Lsm (Salgado-Garrido et al., 1999), Sm (Kambach et al., 1999) and SMN/Gemin proteins (Selenko et al., 2001; Ma et al., 2005), archaeal Lsm proteins (Collins et al., 2001), the bacterial protein Hfq (Schumacher et al., 2002) and a recently identified Lsm homolog of cyanophage origin (Das et al., 2009). Eukaryotic genomes can contain up to 16 Lsm and 7 Sm proteins (Albrecht & Lengauer 2004), yet 2-3 Lsm proteins are generally encoded in archaea (Collins et al., 2001; Toro et al., 2002; Mura et al., 2003) and only a single form is evident in bacteria and cyanophage (Schumacher et al., 2002; Das et al., 2009).
A characteristic feature of the Lsm proteins is their natural tendency to form ring-shaped quaternary complexes, each of a precise composition related to cellular location and RNA target (Beggs, 2005; Spiller et al., 2007). In prokaryotes and archaea, homomeric complexes of six or seven Lsm protomers appear to be functional, whilst discrete heteromeric assemblies of seven distinct Lsm proteins are found in eukaryotes. The individual Lsm proteins vary in size from 8-25 kDa (78-240 amino acids); representative sequences are depicted in Figure 2. Within each, a bipartite consensus sequence (designated Sm1 and Sm2 motifs) can be identified. These motifs arise from strands 1-3 and 4-5 of the core -sheet structure, respectively. A variable stretch of residues between these conserved segments is created by a surface-exposed interconnecting loop (Kambach et al., 1999; Collins et al., 2001).
The N- and C-terminal tail regions of each Lsm sequence are often highly charged and differ markedly between members; these are considered to provide contact points for additional protein or RNA interactions (Reijns et al., 2008; Reijns et al., 2009; Weber et al., 2010). In the case of the eukaryotic Lsm1 and Lsm4 proteins, these tail segments are notably elongated.
The most highly conserved sequence segments across the Lsm family include specific amino acid sidechains implicated in RNA-binding. These are localized to two specific loop features, as outlined in Figure 2. For archaeal and eukaryotic Lsm proteins, sequence motifs Asp-x---Asn ( = hydrophobic) and Arg-Gly-(Asp) (Kambach et al., 1999; Collins et al., 2001; Toro et al., 2001) are characteristic of loops L3 and L5, respectively. In bacterial Hfq, these RNA-binding segments occur as Asp-x--- (L3) and Tyr-Lys-His (L5) (Schumacher et al., 2002).
For this bacterial ortholog, a highly conserved Gln residue on the N-terminal -helix is also implicated in RNA-binding (Schumacher et al., 2002).
Overall, the bacterial protein Hfq shows little sequence conservation with its archaeal and eukaryotic orthologs, yet the archaeal and eukaryotic Lsm proteins share some limited sequence similarity (20 %). The following Lsm-Sm protein paralogs are identifiable: Lsm1-SmB, Lsm2-SmD1, Lsm3-SmD2, Lsm4-SmD3, Lsm5-SmE, Lsm6-SmF, Lsm7-SmG, Lsm8-SmB (Fromont-Racine et al., 2000). These specific sequence relationships suggest the eukaryotic Lsm proteins to have evolved from a common archaeal ancestor in two waves (Khusial et al., 2005; Veretnik et al., 2009). A first gene duplication event likely created eight distinct Lsm proteins, from which later evolved the Sm protein group. The diversity of biological activities of Lsm proteins compared to their more specialized Sm counterparts supports this two-step evolution model (Beggs, 2005; Khusial et al., 2005). The presence of up to three Lsm proteins in archaea, as well as an Hfq-like protein in archaeal
A few multidomain proteins incorporating Lsm components have been observed (summarized, Figure 2). Lsm12 includes t-RNA and methyltransferase domains (Albrecht & Lengauer, 2004), and Lsm13, Lsm14 and Lsm15 all contain a central DFDF-x(7)-F domain (Albrecht & Lengauer, 2004; Anantharaman & Aravind, 2004). Lsm16 features a remarkably disrupted Lsm variant (lacking both the N-terminal -helix and a complete 4 strand) in addition to FDF and YjeF-N domains (Albrecht & Lengauer, 2004; Tritschler et al., 2007). This protein is suggested to be dimeric in solution (Ling et al., 2008). The archaeal protein Pa-Sm3 contains an Lsm-like domain in addition to a C-terminal domain of unknown function adopting an /-fold (Mura et al., 2003).
3. Structures of Lsm protein ring complexes
Crystal structures of Lsm and Sm proteins from diverse sources today provide many high-resolution views of the ring morphology of their assemblies. As shown in Figure 3, Lsm rings have been observed to range 58-75 Å in diameter and to contain a central pore of 6-15 Å. Some crystal structures solved to date (Table 1) have been obtained in the presence of specific RNA partners. The recent solving of the human U1-snRNP structures containing the Sm assembly bound together with U1 snRNA and proteins U1-70K and U1-A have been significant and exciting advances (Pomeranz Krummel et al., 2009; Weber et al., 2010). These provide the first molecular detail of L/Sm rings bound to the highly intertwined protein-RNA network within RNP complexes.
Within the various Lsm ring assemblies, each protomer occurs as a highly bent five-stranded antiparallel -sheet overlaid in most cases by an N-terminal -helix (Figure 4A). The pronounced twist of the -sheet aligns strand 5 against 1, so forming an SH3-type barrel loosely related to the OB-fold (Kambach et al., 1999; Collins et al. 2001). Strands 4 and 5 each present on opposite ends of the module, so providing interaction sites for adjacent Lsm subunits via 4-5’ pairing (Figure 4). Stacking of five to eight protomers in such a manner ultimately results in the formation of the toroid assembly characteristic of all Lsm assemblies (Figure 4).
Within this ring organisation, the N-terminal amphipathic -helices of each Lsm component are gathered across one face of the toroid, from which also project the unstructured N- and
Hexameric | 1D3B | 2.00 | Kambach et al., 1999 | ||
1KQ1 | 1.55 | Schumacher et al., 2002 | |||
1KQ2 | 2.71 | Schumacher et al., 2002 | |||
1LJO | 1.95 | Toro et al., 2002 | |||
1HK9 | 2.15 | Sauter et al., 2003 | |||
1U1S | 1.60 | Nikulin et al., 2003 | |||
1U1T | 1.90 | Nikulin et al., 2003 | |||
2QTX | 2.50 | Nielsen et al., 2007 | |||
3PGG | 2.14 | Vedadi et al., 2007 | |||
3HFN | 2.31 | Boggild et al., 2009 | |||
3GIB | 2.40 | Link et al., 2009 | |||
3HFO | 1.30 | Boggild et al., 2009 | |||
3INZ | 1.70 | Moskaleva et al., 2010 | |||
3M4G | 2.05 | Moskaleva et al., 2010 | |||
3HSB | 2.20 | Someya et al., 20103 | |||
Heptameric | 1I81, 1MGQ | 2.00, 1.70 | Collins et al., 2001 | ||
1I8F | 1.75 | Mura et al., 2001 | |||
1I4K | 2.50 | Toro et al., 2001 | |||
1I5L | 2.75 | Toro et al., 2001 | |||
1JBM | 1.85 | Mura et al., 2003b | |||
1JRI | 1.75 | Mura et al., 2003b | |||
1LNX | 2.05 | Mura et al., 2003b | |||
1H64 | 1.90 | Thore et al., 2003 | |||
1M8V | 2.60 | Thore et al., 2003 | |||
1M5Q | 2.00 | Mura et al., 2003a | |||
1LOJ | 1.90 | Mura et al., 2003b | |||
1N9R | 2.80 | Collins et al., 2003 | |||
1N9S | 3.50 | Collins et al., 2003 | |||
1TH7 | 1.68 | Kilic et al., 2005 | |||
U1-snRNP* | 3CW1 | 5.49 | Pomeranz Krummel et al., 2009 | ||
U1-snRNP* | 3PGW | 4.40 | Weber et al., 2010 | ||
Other | 3BY7 | 2.60 | Das et al., 2009 | ||
3BW1 | 2.50 | Naidoo et al., 2008 | |||
1YCY | 2.80 | Huang et al., 20043 |
C-terminal extensions. The opposite face of the ring, named the distal face, is predominantly composed of residues of the variable loop L4 segments. All the Lsm ring structures (across eukarya, archaea and bacteria) reveal clusters of positive residues lining the internal pore, as well as pronounced positive elements on the distal face (Toro et al., 2001; Brennan & Link, 2007; Naidoo et al., 2008).
The body of structural data adds to biochemical understanding concerning L/Sm-RNA interactions, and distinct RNA sites within the protein oligomer. These include i) a binding site within the lumen of the ring, ii) an external contact site on the helix face and iii) residues located on the distal face of the complex (Figure 4). The first of these sites engages residues from loops L3 and L5, contributed from all Lsm components to create a nucleotide-binding pocket running around the inner rim (Weber et al., 2010). The specific architecture and repeated circular location of these specific, highly conserved, sidechains enables one nucleotide base to be bound per L/Sm protomer. Crystal structures of archaeal and bacterial Lsm complexed with RNA clearly show the oligonucleotides to be threaded around this rim of the toroid (Toro et al., 2001; Schumacher et al., 2002). Each binding “slot” allows specific base stacking to a hydrophobic sidechain of loop L3, as well as contact with the signature Arg residues of loop L5 and H-bonding with Asn residues (strand 4). Further electrostatic contacts (involving conserved Asp (strand 2), Arg (loop L5) and Gly (loop L5) residues) enhance the stability of the Lsm-RNA complex (Toro et al., 2001). Figure 5 displays these relevant binding interactions for U5 within the lumen site of archaeal
An external contact site for RNA at the helix face of the Lsm toroid (site ii) is suggested by the crystal structure of
A third distinct RNA-binding site (iii) is likely to be unique to the bacterial Hfq assembly, and its tripartite form has been detailed in the crystal structure of Hfq bound to poly(A) RNA (Link et al. 2009). The protein Hfq engages poly(A) sequences on its distal face via specific residues exposed from strands 2 and 4. There is, however, no evidence for poly(A) binding by eukaryotic Lsm proteins. In the structure of the Hfq/RNA complex, RNA contacts include electrostatic interactions from Lys (strand 2) and Gln (strand 4) sidechains, as well as stacking of bases between Tyr, Leu (strand 2) and Leu and Ile (strand 2’) of adjacent subunits. It is in this region of the toroid that sequence variability of the loop L4 across the Lsm family results in non-conservation of distal face chemistry, so explaining the unique binding properties of Hfq.
Within the crystal structures of the human U1-snRNP complex, multiple RNA interactions made by the ring of Sm proteins include binding sites i) and ii) outlined above (Weber et al., 2010). However, the U1-snRNP structure also clearly demonstrates the role of the Sm sequence extensions and loop regions as additional interaction sites, particularly the C-terminal extensions of SmD3 and SmB. In the lumen of the toroid (i.e. site i), snRNA threads
to stack single nucleotides of the Sm site against the key loop L3 and L5 residues, noteably the aromatic sidechains. From the helix face of the ring are projected residues of the N-terminal -helix and loop L3 of SmD2, forming an external contact site (reminiscent of site ii) that guides the snRNA into the ring pore. Residues from the loop L2 regions of SmD1 and SmD2 appear to guide RNA out from the Sm ring. Protruding beyond the distal face, residues of the elongated L4 loops of SmD2 and SmB provide another important interaction point to clamp and secure a stem-loop of the snRNA.
The majority of crystal structures of Lsm obtained to date portray the hexa- and heptameric protein assemblies that correspond to fully functional homomeric or heteromeric protein groupings. It is, for instance, assumed that complexes of SmD1-SmD2, SmD3-SmB and SmE-SmF-SmG can exist independently in the cytoplasm, yet rearrange into mixed heptamers in the presence of RNA during snRNP formation (Peng & Gallwitz, 2004). However, a few crystal structures suggest that other compositions, e.g. pentamers and octamers, may be stable for eukaryotic Lsm (Naidoo et al., 2008; Das et al., 2009). While it is currently not clear if these organizations are peculiar to recombinant preparations of the Lsm family, they suggest possibilities for a variety of multimeric assemblies
4. Functional roles for Lsm proteins
Sm and Lsm proteins are known to interact with a diversity of RNA partner species. Specific RNA sequences recognized by various Lsm complexes include the Sm-site (A2U5GA) (Raker et al., 1999) and U-rich stretches at the 3’ end of oligoadenylated mRNA (Chowdhury et al., 2007) and RNA polymerase III transcripts, including snRNA (Achsel et al., 1999). Other binding partners include snoRNA (Kufel et al., 2003a), P RNA (Kufel et al., 2002), tRNA (Kufel et al., 2002) and rRNA (Kufel et al., 2003b). Depletion of Lsm proteins 2-5 and 8 in yeast results in defects in post-transcriptional processing of tRNA, P RNA, rRNA, snoRNA and snRNA precursors (Kufel et al., 2002; Kufel et al., 2003b; Kufel et al., 2003a). Yet only minor (or no) effects are observed on depletion of Lsm6 and Lsm7. A summary of some specific Lsm-ncRNA interactions is presented in Table 2.
The Lsm2-Lsm8 complex plays a key role in U6 snRNA maturation, so impacting on the formation of spliceosomal snRNPs (Karaduman et al., 2006). U6 snRNA is the most conserved of all snRNA species and key to the catalytic activity of the spliceosome (Brow, 2002). Newly transcribed U6 pre-snRNA is targeted to the nucleoli following binding of the La protein (Lhp1 in yeast) at its U-rich 3’ region (Wolin & Cedervall, 2002). Following cyclic phosphorylation, La (or Lhp1) is displaced from the U6 snRNA by the Lsm2-Lsm8 assembly (Achsel et al., 1999; Licht et al., 2008), which induces conformational changes that stimulate binding of a recycling factor (p110 or Prp24) (Rader & Guthrie, 2002; Ryan et al., 2002; Karaduman et al., 2006). These conformational changes have been suggested to assist in the formation and recycling of the U4/U6 di-snRNP by exposing single stranded nucleotides for base pairing (Beggs, 2005; Karaduman et al., 2006; Karaduman et al., 2008). The Lsm2-Lsm8 complex is also implicated in decapping steps of mRNA in the nucleus. This was suggested by the finding that Lsm6 and Lsm8 were required for nuclear mRNA decay (Kufel et al., 2004).
A specific role for Lsm1-Lsm7 concerns activation of mRNA decay in P-bodies; depletion of individual yeast Lsm proteins results in the accumulation of capped, oligoadenylated mRNA transcripts (Boeck et al., 1998; Bonnerot et al., 2000; Bouveret et al., 2000; Tharun et al., 2000). This specific Lsm complex is recruited alongside other decay factors to U-rich tracts by the protein Pat1, after its displacement of cap-binding translation factors (Parker & Sheth, 2007). It is likely that Pat1 and Lsm1-Lsm7 are then involved in subsequent activation of the Dcp1-Dcp2 enzyme (Nissan et al., 2010). A variety of studies have demonstrated the interaction of Lsm1-Lsm7 with decapping factors and exoribonuclease Xrn1 (Bonnerot et al., 2000; Bouveret et al., 2000; Tharun et al., 2000; Coller et al., 2001).
RNAspecies | Lsm function | Selected experimental evidence | References |
snRNA | assembly, processing and nuclear localization | Lsm2-8 binds 3’ end of U6 snRNA | Achsel et al., 1999 |
Lsm2-8 initiates structural rearrangements of U6 snRNA | Karaduman et al., 2006; 2008 | ||
Depletion of Lsm2-Lsm8 results in splicing defects | Mayes et al., 1999 | ||
Splicing activity recovered through recombinant Lsm proteins | Verdone et al., 2004 | ||
Lsm2-8 localizes U6 snRNA to the nucleus | Spiller et al., 2007 | ||
tRNA | splicing, 3’ and 5’ end-processing | Accumulation of unprocessed pre-tRNA and reduced La/Lhp1 binding upon Lsm2-Lsm5 and Lsm8 depletion | Kufel et al., 2002 |
Direct interaction of Lsm3 with tRNA and its splicing factors | Fromont-Racine et al., 1997 | ||
P RNA | chaperone | Depletion of Lsm2-Lsm5 and Lsm8 reduces pre-PRNA levels | Mayes et al., 1999 |
Reduced La/Lhp1 binding upon Lsm2-Lsm5 and Lsm8 depletion | Kufel et al., 2002 | ||
Lsm2-Lsm7 proteins coprecipitate with pre-PRNA | Salgado-Garrido et al., 1999 | ||
rRNA | 3’ and 5’ end-processing | Depletion of Lsm2-Lsm5 and Lsm8 delays pre-rRNA processing and increases rRNA decay rate | Kufel et al., 2003b |
Pre-rRNA coprecipitates with Lsm3 but not Lsm1 | Kufel et al., 2003b | ||
Deletion of Lsm6 and Lsm7 genes impairs 20S pre-rRNA processing | Li et al., 2009 | ||
snoRNA | 3’ end-processing | Lsm2-Lsm5 and Lsm8 depletion results in U3-snoRNA degradation and loss of its 3’ extended precursor | Kufel et al., 2003a |
Reduced La/Lhp1 binding upon Lsm3 or Lsm5 depletion | Kufel et al., 2003a | ||
Lsm2-Lsm7 but not Lsm1 or Lsm8 coprecipitate with snR5 snoRNA | Fernandez et al., 2004 | ||
Lsm2-4 and 6-8 but not Lsm5 coprecipitate with U8 snoRNA | Tomasevic & Peculis, 2002 |
In contrast to its enhancement of mRNA decay, however, the Lsm1-Lsm7 complex can also protect mRNA against 3’ end trimming (He & Parker, 2001). This may involve steric hindrance of nuclease attack at mRNA locations on which Lsm1-Lsm7 and Pat1 proteins are bound.
5. Specific functions of bacterial Hfq
Bacterial Hfq is observed to interact with bacterial sRNA and so promote the formation of sRNA-mRNA complexes (Wassarman et al., 2001; Gottesman & Storz, 2010). Bacterial sRNAs are small non-coding RNA species (50-500 nucleotides), which regulate gene expression via base pairing with mRNA transcripts in a similar mechanism to eukaryotic siRNA or miRNA (Storz et al., 2004; Majdalani et al., 2005; Livny & Waldor, 2007; Gottesman & Storz, 2010). Hfq controls gene expression either by rearranging the RNA secondary structure, or by increasing the concentration of RNA locally to promote RNA-RNA interactions (Moll et al., 2003; Lease & Woodson, 2004; Afonyushkin et al., 2005). A similar mode of binding to sRNA was recently observed for the archaeal Lsm from
As for the eukaryotic Lsm proteins, Hfq is required for deadenylation-dependent mRNA decay. An RNase E-Hfq-sRNA complex is thought to function in translational repression and subsequent mRNA destabilization and degradation (Morita et al., 2005; Morita et al., 2006). Additional functions of Hfq include ATPase activity (Sukhodolets & Garges, 2003), cellular stress response and modulation of virulence in some bacterial strains (Tsui et al., 1994; Fantappie et al., 2009; Liu et al., 2010). Interestingly, the virulence of the multi-drug resistant human pathogen
6. Lsm proteins in human disease and viral replication
Aberrations in functions of Lsm proteins have been associated with a number of human diseases. Sm proteins are known to be targeted by auto-antibodies in systemic lupus erythematosis (Lerner & Steitz, 1979). In fact, the proteins were first identified in nuclear extracts of a patient suffering from this disease. A mutation of the SMN gene resulting in diminished assembly of snRNPs is the cause of spinal muscular atrophy (Lefebvre et al., 1995; Wan et al., 2005). Three Lsm proteins (Lsm1, Lsm3 and Lsm7) have now been directly connected to different cancer types. Lsm1 (also named cancer associated Sm-like protein, CaSm) was upregulated in pancreatic, prostate and breast cancer, as well as in several cancer-derived cell lines (Schweinfest et al., 1997; Fraser et al., 2005; Streicher et al., 2007). Remarkably, overexpression of antisense Lsm1 has been demonstrated to promote tumor reduction (Kelley et al., 2000; Kelley et al., 2001; Yan et al., 2006). Elevated levels of Lsm7 have been identified in malignant thyroid tumors, and a reduction in Lsm7 expression was observed in breast cancers (Conte et al., 2002; Rosen et al., 2005). The copy number and expression for the Lsm3 gene was found to be elevated in cervical cancer (Lyng et al., 2006).
Observations concerning Lsm proteins in viral replication underlines some interesting functional diversity. Bacterial Hfq was initially described as a host factor required for phage Qß replication (Franze de Fernandez et al., 1968). A role for Lsm1 as an effector of HIV replication has been reported (Chable-Bessia et al., 2009). It has also been suggested more recently that positive-strand RNA viruses may directly bind to the host Lsm1-7 protein complex via tRNA-like structures and A-rich stretches, so diverting normal mRNA regulation (Galao et al., 2010). The requirement of host Lsm proteins for the replication of this class of virus has additionally been demonstrated in plant brome mosaic virus (Diez et al., 2000; Noueiry et al., 2003; Mas et al., 2006) and human hepatitis C virus (Scheller et al., 2009).
References
- 1.
Achsel T. Brahms H. Kastner B. Bachi A. Wilm M. Luerhmann R. 1999 A doughnut-shaped heteromer of human Sm-like proteins binds to the 3’ end of U6 snRNA, thereby facilitating U4/U6 duplex formation in vitro’, 18 (20),5789 EOF 802 EOF - 2.
Afonyushkin T. Vecerek B. Moll I. Blasi U. Kaberdin V. R. 2005 Both RNase E and RNase III control the stability of sodB mRNA upon translational inhibition by the small regulatory RNA RyhB’, 33 (5),1678 EOF 1689 EOF - 3.
Albrecht M. Lengauer T. 2004 Novel Sm-like proteins with long C-terminal tails and associated methyltransferases’, 569 (1-3),18 EOF 26 EOF - 4.
Anantharaman V. Aravind L. 2004 Novel conserved domains in proteins with predicted roles in eukaryotic cell-cycle regulation, decapping and RNA stability’, 5 (1),45 EOF - 5.
Balbo P. B. Bohm A. 2007 Mechanism of poly(A) polymerase: structure of the enzyme-MgATP-RNA ternary complex and kinetic analysis’, 15 (9), 1117-31. - 6.
Beggs J. D. 2005 Lsm proteins and RNA processing’, Biochem Soc Trans33 439 501 - 7.
Boeck R. Lapeyre B. Brown C. E. Sachs A. B. 1998 Capped mRNA degradation intermediates accumulate in the yeast spb8 2 mutant’, 18 (9), 5062-72. - 8.
Bonnerot C. Boeck R. Lapeyre B. 2000 The two proteins Pat1Mrt1p and Spb8p interact in vivo, are required for mRNA decay, and are functionally linked to Pab1p.’, 20. - 9.
Bouveret E. Rigaut G. Shevchenko A. Wilm M. Seraphin B. 2000 A Sm-like protein complex that participates in mRNA degradation’, 19 (7),1661 EOF 71 EOF - 10.
Brengues M. Teixeira D. Parker R. 2005 Movement of eukaryotic mRNAs between polysomes and cytoplasmic processing bodies’, 310 (5747),486 EOF 9 EOF - 11.
Brennan R. G. Link T. M. 2007 Hfq structure, function and ligand binding’, 10 (2),125 EOF 133 EOF - 12.
Brow D. A. 2002 Allosteric cascade of spliceosome activation’,36 333 60 - 13.
Chable-Bessia C. Meziane O. Latreille D. Triboulet R. Zamborlini A. Wagschal A. Jacquet J. M. Reynes J. Levy Y. Saib A. Bennasser Y. Benkirane M. 2009 Suppression of HIV-1 replication by microRNA effectors’, 6,26 EOF Retrovirology EOF - 14.
Chowdhury A. Mukhopadhyay J. Tharun S. 2007 The decapping activator Lsm17p Pat1p complex has the intrinsic ability to distinguish between oligoadenylated and polyadenylated RNAs’, 13. - 15.
Coller J. M. Tucker M. Sheth U. MA Valencia-Sanchez Parker R. 2001 The DEAD box helicase, Dhh1p, functions in mRNA decapping and interacts with both the decapping and deadenylase complexes. 7. - 16.
BM Collins Harrop S. J. Kornfeld G. D. Ian D. W. Curmi P. M. G. Mabbutt B. C. 2001 Crystal Structure of a Heptameric Sm-like Protein Complex from Archea: Implications for the Structure and Evolution of snRNPs’,309 915 23 - 17.
Conte N. Charafe-Jauffret E. Delaval B. Adelaide J. Ginestier C. Geneix J. Isnardon D. Jacquemier J. Birnbaum D. 2002 Carcinogenesis and translational controls: TACC1 is down-regulated in human cancers and associates with mRNA regulators’, 21 (36),5619 EOF 30 EOF - 18.
Crick F. 1979 Split genes and RNA splicing’, 204 (4390),264 EOF 71 EOF - 19.
Das D. Kozbial P. Axelrod H. L. Miller M. D. Mc Mullan D. Krishna S. S. Abdubek P. Acosta C. Astakhova T. Burra P. Carlton D. Chen C. Chiu H. J. Clayton T. Deller M. C. Duan L. Elias Y. Elsliger M. A. Ernst D. Farr C. Feuerhelm J. Grzechnik A. Grzechnik S. K. Hale J. Han G. W. Jaroszewski L. Jin K. K. Johnson H. A. Klock H. E. Knuth M. W. Kumar A. Marciano D. Morse A. T. Murphy K. D. Nigoghossian E. Nopakun A. Okach L. Oommachen S. Paulsen J. Puckett C. Reyes R. Rife C. L. Sefcovic N. Sudek S. Tien H. Trame C. Trout C. V. van den Bedem. H. Weekes D. White A. Xu Q. Hodgson K. O. Wooley J. Deacon A. M. Godzik A. Lesley S. A. Wilson I. A. 2009 Crystal structure of a novel Sm-like protein of putative cyanophage origin at 2.60 A resolution’, 75 (2),296 EOF 307 EOF - 20.
Diez J. Ishikawa M. Kaido M. Ahlquist P. 2000 Identification and characterization of a host protein required for efficient template selection in viral RNA replication’, 97 (8),3913 EOF 3918 EOF - 21.
Eddy S. R. 2001 Non-coding RNA genes and the modern RNA world’, 2 (12),919 EOF 29 EOF - 22.
Fantappie L. Metruccio M. M. Seib K. L. Oriente F. Cartocci E. Ferlicca F. Giuliani M. M. Scarlato V. Delany I. 2009 The RNA chaperone Hfq is involved in stress response and virulence in Neisseria meningitidis and is a pleiotropic regulator of protein expression’, 77 (5),1842 EOF 1853 EOF - 23.
Fernandez C. F. Pannone B. K. Chen X. Fuchs G. Wolin S. L. 2004 An Lsm2 Lsm7 complex in Saccharomyces cerevisiae associates with the small nucleolar RNA snR5’, 15 (6), 2842-52. - 24.
Fischer S. Benz J. Spath B. Maier L. K. Straub J. Granzow M. Raabe M. Urlaub H. Hoffmann J. Brutschy B. Allers T. Soppa J. Marchfelder A. 2011 The archaeal Lsm protein binds to small RNAs’, 285 (45),34429 EOF 34438 EOF - 25.
Franze de Fernandez. M. T. Eoyang L. August J. T. 1968 Factor fraction required for the synthesis of bacteriophage Qbeta-RNA’, 219 (5154),588 EOF 90 EOF - 26.
Fraser M. M. Watson P. M. Fraig M. M. Kelley J. R. Nelson P. S. Boylan A. M. Cole D. J. Watson D. K. 2005 CaSm-mediated cellular transformation is associated with altered gene expression and messenger RNA stability’, 65 (14),6228 EOF 36 EOF - 27.
Fromont-Racine M. Rain J. C. Legrain P. 1997 Toward a functional analysis of the yeast genome through exhaustive two-hybrid screens.’, 16. - 28.
Fromont-Racine M. Mayes A. E. Brunet-Simon A. Rain J. C. Colley A. Dix I. Decourty L. Joly N. Ricard F. Beggs J. D. Legrain P. 2000 Genome-wide protein interaction screens reveal functional networks involving Sm-like proteins’, 17 (2),95 EOF 110 EOF - 29.
Galao R. P. Chari A. Alves-Rodrigues I. Lobao D. Mas A. Kambach C. Fischer U. Diez J. 2010 LSm1 7 complexes bind to specific sites in viral RNA genomes and regulate their translation and replication’, 16 (4), 817-27. - 30.
Garneau Nicole. L. Wilusz Jeffrey. Wilusz Carol. J. 2007 The highways and byways of mRNA decay’,8 113 26 - 31.
Gottesman S. Storz G. 2010 Bacterial Small RNA Regulators: Versatile Roles and Rapidly Evolving Variations’, . - 32.
He W. Parker R. 2001 The yeast cytoplasmic LsmI/Pat1p complex protects mRNA 3’ termini from partial degradation’, 158 (4),1445 EOF 55 EOF - 33.
Kambach Christian. Walke Stefan. Young Robert. Avis Johanna. M. de la Fortelle Eric. Raker Veronica. A. Luerhmann Reinhard. Li Jade. Nagai Kiyoshi. 1999 Crystal Structures of Two Sm Protein Complexes and Their Implications for the Assembly of the Spliceosomal snRNPs’,96 375 87 - 34.
Karaduman R. Fabrizio P. Hartmuth K. Urlaub H. Luerhmann R. 2006 RNA structure and RNA-Protein interactions in Purified Yeast U6 snRNPs’,356 1248 62 - 35.
Karaduman R. Dube P. Stark H. Fabrizio P. Kastner B. Luhrmann R. 2008 Structure of yeast U6 snRNPs: arrangement of Prp24p and the LSm complex as revealed by electron microscopy’, 14 (12),2528 EOF 2537 EOF - 36.
Kelley J. R. Fraser M. M. Schweinfest C. W. Vournakis J. N. Watson D. K. Cole D. J. 2001 CaSm/gemcitabine chemo-gene therapy leads to prolonged survival in a murine model of pancreatic cancer’, 130 (2),280 EOF 288 EOF - 37.
Kelley J. R. Brown J. M. Frasier M. M. Baron P. L. Schweinfest C. W. Vournakis J. N. Watson D. K. Cole D. J. 2000 The cancer-associated Sm-like oncogene: a novel target for the gene therapy of pancreatic cancer’, 128 (2), 353-60. - 38.
Khusial P. Plaag R. Zieve G. W. 2005 LSm proteins form heptameric rings that bind to RNA via repeating motifs’, 30 (9). - 39.
Kufel J. Bousquet-Antonelli C. Beggs J. D. Tollervey D. 2004 Nuclear pre-mRNA decapping and 5’ degradation in yeast require the Lsm2 8 p complex’, 24 (21), 9646-57. - 40.
Kufel J. Allmang C. Verdone L. Beggs J. D. Tollervey D. 2002 Lsm proteins are required for normal processing of pre-tRNAs and their efficient association with La-homologous protein Lhp1p’, 22 (14),5248 EOF 56 EOF - 41.
Kufel J. Allmang C. Verdone L. Beggs J. Tollervey D. 2003a A complex pathway for 3’ processing of the yeast U3 snoRNA’, 31 (23),6788 EOF 97 EOF - 42.
Kufel J. Allmang C. Petfalski E. Beggs J. Tollervey D. 2003b Lsm Proteins are required for normal processing and stability of ribosomal RNAs’, 278 (4),2147 EOF 56 EOF - 43.
Lease R. A. Woodson S. A. 2004 Cycling of the Sm-like protein Hfq on the DsrA small regulatory RNA’, 344 (5),1211 EOF 23 EOF - 44.
Lefebvre S. Burglen L. Reboullet S. Clermont O. Burlet P. Viollet L. Benichou B. Cruaud C. Millasseau P. Zeviani M. et al. 1995 Identification and characterization of a spinal muscular atrophy-determining gene’, 80 (1),155 EOF 65 EOF - 45.
Lerner M. R. Steitz J. A. 1979 Antibodies to small nuclear RNAs complexed with proteins are produced by patients with systemic lupus erythematosus’, 76 (11),5495 EOF 5499 EOF - 46.
Li Z. Lee I. Moradi E. Hung N. J. Johnson A. W. Marcotte E. M. 2009 Rational extension of the ribosome biogenesis pathway using network-guided genetics’, 7 (10),e1000213 EOF - 47.
Licht K. Medenbach J. Luerhmann R. Kambach C. Bindereif A. 2008 cyclic phosphorylation of U6 snRNA leads to recruitment of recycling factor110 through LSm proteins’, 14 (8), 1-7. - 48.
Lilley D. M. 2005 Structure, folding and mechanisms of ribozymes’, 15 (3), 313-23. - 49.
Ling S. H. Decker C. J. Walsh M. A. She M. Parker R. Song H. 2008 Crystal structure of human Edc3 and its functional implications’, 28 (19),5965 EOF 5976 EOF - 50.
Link T. M. Valentin-Hansen P. Brennan R. G. 2009 Structure of Escherichia coli Hfq bound to polyriboadenylate RNA’, 106 (46),19292 EOF 19297 EOF - 51.
Liu Y. Wu N. Dong J. Gao Y. Zhang X. Mu C. Shao N. Yang G. 2010 Hfq is a global regulator that controls the pathogenicity of Staphylococcus aureus’, 5 (9):e13069 EOF - 52.
Livny J. Waldor M. K. 2007 Identification of small RNAs in diverse bacterial species’, 10 (2),96 EOF 101 EOF - 53.
Luhrmann R. Kastner B. Bach M. 1990 Structure of spliceosomal snRNPs and their role in pre-mRNA splicing’, 1087 (3),265 EOF 92 EOF - 54.
Lyng H. Brovig R. S. Svendsrud D. H. Holm R. Kaalhus O. Knutstad K. Oksefjell H. Sundfor K. Kristensen G. B. Stokke T. 2006 Gene expressions and copy numbers associated with metastatic phenotypes of uterine cervical cancer’, 7,268 EOF - 55.
Ma Y. Dostie J. Dreyfuss G. Van Duyne G. D. 2005 The Gemin6 Gemin7 heterodimer from the survival of motor neurons complex has an Sm protein-like structure’, 13 (6), 883-92. - 56.
Majdalani N. Vanderpool C. K. Gottesman S. 2005 Bacterial small RNA regulators’, 40 (2),93 EOF 113 EOF - 57.
Mas A. Alves-Rodrigues I. Noueiry A. Ahlquist P. Diez J. 2006 Host deadenylation-dependent mRNA decapping factors are required for a key step in brome mosaic virus RNA replication’, 80 (1),246 EOF 51 EOF - 58.
Mattick J. S. 2001 Non-coding RNAs: the architects of eukaryotic complexity’, 2 (11),986 EOF 91 EOF - 59.
Mattick J. S. Makunin I. V. 2006 Non-coding RNA’, 15 Spec1 R17 29 - 60.
Mayes A. E. Verdone L. Legraine P. JD Beggs 1999 Characerization of Sm-like proteins in yeast and their association with U6 snRNA ‘, 18 (15), 4321-31. - 61.
Moll I. Leitsch D. Steinhauser T. Blasi U. 2003 RNA chaperone activity of the Sm-like Hfq protein’, 4 (3),284 EOF 9 EOF - 62.
Morita T. Maki K. Aiba H. 2005 RNase E-based ribonucleoprotein complexes: mechanical basis of mRNA destabilization mediated by bacterial noncoding RNAs’, 19 (18),2176 EOF 86 EOF - 63.
Morita T. Mochizuki Y. Aiba H. 2006 Translational repression is sufficient for gene silencing by bacterial small noncoding RNAs in the absence of mRNA destruction’, 103 (13),4858 EOF 4863 EOF - 64.
Mura C. Phillips M. Kozhukhovsky A. Eisenberg D. 2003 Structure and assembly of an augmented Sm-like archaeal protein14 mer’, 100 (8), 4539-44. - 65.
Naidoo N. Harrop S. J. Sobti M. Haynes P. A. Szymczyna B. R. Williamson J. R. Curmi P. M. G. Mabbutt B. C. 2008 Crystal Structure of Lsm3 Octamer from Saccharomyces cerevisiae: Implications for Lsm Ring Organisation and Recruitment’,377 1357 71 - 66.
Nissan T. Rajyaguru P. She M. Song H. Parker R. 2010 Decapping activators in Saccharomyces cerevisiae act by multiple mechanisms’, 39 (5),773 EOF 783 EOF - 67.
Noueiry A. O. Diez J. Falk S. P. Chen J. Ahlquist P. 2003 Yeast Lsm17p Pat1p deadenylation-dependent mRNA-decapping factors are required for brome mosaic virus genomic RNA translation’, 23 (12), 4094-106. - 68.
Parker R. Sheth U. 2007 P Bodies and the control of mRNA Translation and Degradation’, 25 (5),635 EOF 646 EOF - 69.
Patel S. B. Bellini M. 2008 The assembly of a spliceosomal small nuclear ribonucleoprotein particle’, 36 (20),6482 EOF 6493 EOF - 70.
Peng R. Gallwitz D. 2004 Multiple SNARE interactions of an SM protein: Sed5Sly1p binding is dispensable for transport’, 23 (20), 3939-49. - 71.
Pomeranz Krummel. D. A. Oubridge C. Leung A. K. Li J. Nagai K. 2009 Crystal structure of human spliceosomal U1 snRNP at 5.5 A resolution’, 458 (7237),475 EOF 480 EOF - 72.
Pozzoli U. Sironi M. Cagliani R. Comi G. P. Bardoni A. Bresolin N. 2002 Comparative analysis of the human dystrophin and utrophin gene structures’, 160 (2),793 EOF 8 EOF - 73.
Proudfoot N. J. Furger A. Dye M. J. 2002 Integrating mRNA processing with transcription’, 108 (4),501 EOF 12 EOF - 74.
Rader S. D. Guthrie C. 2002 A conserved Lsm-interaction motif in Prp24 required for efficient U4/U6 di-snRNP formation’, 8 (11),1378 EOF 1392 EOF - 75.
Raker V. A. Hartmuth K. Kastner B. Luhrmann R. 1999 Spliceosomal U snRNP core assembly: Sm proteins assemble onto an Sm site RNA nonanucleotide in a specific and thermodynamically stable manner’, 19 (10),6554 EOF 65 EOF - 76.
Reijns M. A. Auchynnikava T. Beggs J. D. 2009 Analysis of Lsm1p and Lsm8p domains in the cellular localization of Lsm complexes in budding yeast’, 276 (13),3602 EOF 3617 EOF - 77.
Reijns M. A. Alexander R. D. Spiller M. P. Beggs J. D. 2008 A role for Q/N-rich aggregation-prone regions in P-body localization’, 121 (Pt 15),2463 EOF 2472 EOF - 78.
Rosen J. He M. Umbricht C. Alexander H. R. Dackiw A. P. Zeiger M. A. Libutti S. K. 2005 A six-gene model for differentiating benign from malignant thyroid tumors on the basis of gene expression’, 138 (6), 1050-6; discussion56 7 - 79.
Ryan D. E. Stevens S. W. Abelson J. 2002 The 5’ and 3’ domains of yeast U6 snRNA: Lsm proteins facilitate binding of Prp24 protein to the U6 telestem region’, 8 (8),1011 EOF 33 EOF - 80.
Salgado-Garrido J. Bragado-Nielsson E. Kandels-Lewis S. Seraphin B. 1999 Sm and Sm-like proteins assemble in two related complexes of deep evolutionary origin’, 18 (12),3451 EOF 62 EOF - 81.
Scheller N. Mina L. B. Galao R. P. Chari A. Gimenez-Barcons M. Noueiry A. Fischer U. Meyerhans A. Diez J. 2009 Translation and replication of hepatitis C virus genomic RNA depends on ancient cellular proteins that control mRNA fates’, 106 (32),13517 EOF 13522 EOF - 82.
Schumacher Pearson R. F. Moller T. Valentin-Hansen P. Brennan R. G. 2002 Structures of the pleiotropic translational regulator Hfq and an Hfq-RNA complex: a bacterial Sm-like protein’, 21 (13),3546 EOF 56 EOF - 83.
Schweinfest C. W. Graber M. W. Chapman J. M. Papas T. S. Baron P. L. Watson D. K. 1997 CaSm: an Sm-like protein that contributes to the transformed state in cancer cells’, 57 (14),2961 EOF 5 EOF - 84.
Selenko P. Sprangers R. Stier G. Buhler D. Fischer U. Sattler M. 2001 SMN tudor domain structure and its interaction with the Sm proteins’, 8 (1),27 EOF 31 EOF - 85.
Sheth U. Parker R. 2003 Decapping and decay of messenger RNA occur in cytoplasmic processing bodies’, 300 (5620),805 EOF 8 EOF - 86.
Sobti M. Cubeddu L. Haynes P. A. Mabbutt B. C. 2010 Engineered rings of mixed yeast Lsm proteins show differential interactions with translation factors and U-rich RNA’, 49 (11),2335 EOF 2345 EOF - 87.
Song M. G. Kiledjian M. 2007 Terminal oligo U-tract-mediated stimulation of decapping’, 13 (12),2356 EOF 65 EOF - 88.
Spiller M. P. Boon K. L. Reijns M. A. Beggs J. D. 2007 The Lsm2 8 complex determines nuclear localization of the spliceosomal U6 snRNA’, 35 (3), 923-9. - 89.
Storz G. Opdyke J. A. Zhang A. 2004 Controlling mRNA stability and translation with small, noncoding RNAs’, 7 (2),140 EOF 4 EOF - 90.
Streicher K. L. Yang Z. Q. Draghici S. Ethier S. P. 2007 Transforming function of the LSM1 oncogene in human breast cancers with the 811 12 amplicon’, 26 (14), 2104-14. - 91.
Sukhodolets M. V. Garges S. 2003 Interaction of Escherichia coli RNA polymerase with the ribosomal protein S1 and the Sm-like ATPase Hfq’, 42 (26),8022 EOF 34 EOF - 92.
Tharun S. He W. Mayes A. E. Lennertz P. Beggs J. D. Parker R. 2000 Yeast Sm-like proteins function in mRNA decapping and decay’, 404 (6777),515 EOF 8 EOF - 93.
Thore S. Mayer C. Sauter C. Weeks S. Suck D. 2003 Crystal structures of the Pyrococcus abyssi Sm core and its complex with RNA. Common features of RNA binding in archaea and eukarya’, 278 (2),1239 EOF 47 EOF - 94.
Tomasevic N. Peculis B. A. 2002 Xenopus LSm proteins bind U8 snoRNA via an internal evolutionarily conserved octamer sequence’, 22 (12),4101 EOF 12 EOF - 95.
Toro I. Basquin J. Teo-Dreher H. Suck D. 2002 Archaeal Sm proteins form heptameric and hexameric complexes: crystal structures of the Sm1 and Sm2 proteins from the hyperthermophile Archaeoglobus fulgidus’, 320 (1),129 EOF 42 EOF - 96.
Toro I. Thore Stephane. Mayer Claudine. Basquin Jerome. Seraphin Bertrand. Suck Dietrich. 2001 RNA binding in an Sm core domain: X-ray structure and functional analysis of an archeal Sm protein complex’, 20 (9), 2293-303. - 97.
Tritschler F. Eulalio A. Truffault V. Hartmann M. D. Helms S. Schmidt S. Coles M. Izaurralde E. Weichenrieder O. 2007 A divergent Sm fold in EDC3 proteins mediates DCP1 binding and P-body targeting’, 27 (24),8600 EOF 11 EOF - 98.
Tsui H. C. Leung H. C. Winkler M. E. 1994 Characterization of broadly pleiotropic phenotypes caused by an hfq insertion mutation in Escherichia coli K-12’, 13 (1),35 EOF 49 EOF - 99.
Tucker M. Valencia-Sanchez M. A. Staples R. R. Chen J. Denis C. L. Parker R. 2001 The transcription factor associated Ccr4 and Caf1 proteins are components of the major cytoplasmic mRNA deadenylase in Saccharomyces cerevisiae’, 104 (3),377 EOF 86 EOF - 100.
Urlaub H. Raker V. A. Kostka S. Luhrmann R. 2001 Sm protein-Sm site RNA interactions within the inner ring of the spliceosomal snRNP core structure’, 20 (1-2),187 EOF 96 EOF - 101.
Verdone L. Galardi S. Page D. Beggs J. D. 2004 Lsm proteins promote regeneration of pre-mRNA splicing activity’, 14 (16),1487 EOF 1491 EOF - 102.
Veretnik S. Wills C. Youkharibache P. Valas R. E. Bourne P. E. 2009 Sm/Lsm genes provide a glimpse into the early evolution of the spliceosome’, 5 (3),e1000315 EOF - 103.
Wahl M. C. Will C. L. Luhrmann R. 2009 The spliceosome: design principles of a dynamic RNP machine’, 136 (4),701 EOF 718 EOF - 104.
Wan L. Battle D. J. Yong J. Gubitz A. K. Kolb S. J. Wang J. Dreyfuss G. 2005 The survival of motor neurons protein determines the capacity for snRNP assembly: biochemical deficiency in spinal muscular atrophy’, 25 (13),5543 EOF 51 EOF - 105.
Wassarman K. M. Repoila F. Rosenow C. Storz G. Gottesman S. 2001 Identification of novel small RNAs using comparative genomics and microarrays’, 15 (13),1637 EOF 51 EOF - 106.
Weber G. Trowitzsch S. Kastner B. Luhrmann R. Wahl M. C. 2010 Functional organization of the Sm core in the crystal structure of human U1 snRNP’, 29 (24),4172 EOF 4184 EOF - 107.
Wen Y. Shatkin A. J. 1999 Transcription elongation factor hSPT5 stimulates mRNA capping’, 13 (14),1774 EOF 9 EOF - 108.
Will C. L. Luhrmann R. 2001 Spliceosomal UsnRNP biogenesis, structure and function’, 13 (3),290 EOF 301 EOF - 109.
Wolin S. L. Cedervall T. 2002 The La protein’,71 375 403 - 110.
Yan Y. Rubinchik S. Wood A. L. Gillanders W. E. Dong J. Y. Watson D. K. Cole D. J. 2006 Bystander effect contributes to the antitumor efficacy of CaSm antisense gene therapy in a preclinical model of advanced pancreatic cancer’, 13 (2),357 EOF 65 EOF