Coiled bodies are predisposed to a spatial association with genes that contain snoRNA sequences in their introns

Abstract

Small nucleolar RNAs (snoRNAs) constitute a group of more than 100 different stable RNA molecules that are found concentrated in the nucleolus where they are involved in the maturation of ribosomal RNA. Most snoRNAs are not produced from their own genes but are encoded in the introns of other genes, referred to as snoRNA host genes. Little is known about the mechanisms by which the snoRNAs are produced from introns and how the snoRNAs mature to functional snoRNP complexes in the nucleolus. One class of intron-encoded snoRNAs binds with high specificity to the protein fibrillarin which is found concentrated in the nucleolus, but also in small nuclear domains known as coiled bodies. It has become clear that genes that code for small stable RNAs, e.g., U1, U2 snRNA, and the U3 snoRNA, are often found adjacent to coiled bodies. High concentrations of transcription factors and RNA processing factors in and around coiled bodies indicate that they may be involved in the expression of the adjacent genes. In order to investigate whether coiled bodies could play a role in the synthesis of intron-encoded snoRNAs the distribution of coiled bodies was studied relative to three different snoRNA host genes, i.e., hsc70, RPS3, UHG. All three were found adjacent to coiled bodies at significantly high frequencies (11-19%), compared to control sequences (0-2%), to conclude a preferential association between the snoRNA host genes and coiled bodies. This association could point to a possible role for coiled bodies in the synthesis and/or maturation of snoRNAs. An involvement in snoRNA production could explain the presence of transcription factors, splicing factors, and fibrillarin in coiled bodies.

Coilin: The first 25 years

“…Genes encoding snRNAs, snoRNAs and histone mRNAs were found closely associated with CBs in cytological assays. [61][62][63][64][65][66][67] Coilin association with snRNA and histone genes was recently reexamined by genome-wide ChIP-Seq, which detected coilin peaks at most of these genes. 33 CBs contain pre-U2 snRNA 68 and contact between CBs and chromatin is maintained by active snRNA gene transcription.…”

The Coilin Interactome Identifies Hundreds of Small Noncoding RNAs that Traffic through Cajal Bodies

“…Coilin Binds Hundreds of Small ncRNAs In Vivo (Boulon et al, 2004;Narayanan et al, 1999;Schul et al, 1999;Weinstein and Steitz, 1999). Perhaps for historical reasons, CBs have instead emerged as a center of snRNA modification and spliceosomal snRNP assembly.…”

U3 snoRNA genes are multi-copy and frequently linked to U5 snRNA genes in Euglena gracilis§

“…Such an arrangement could conceivably lead to the formation of a tRNA transcription and processing center enriched in RNAP III, transcription, and processing factors [71,73]. Experimental evidence suggests that U3 snoRNA genes in human cells may associate in three-dimensional space with coiled bodies in the nucleus [39,74]. Thus, the three-dimensional clustering of genes transcribed by RNAP III could promote the formation of 'transcription territories' [75] that function to more efficiently recruit transcription complexes to the region, thereby maintaining a high level of gene expression.…”