Centromeric and pericentric transcription and transcripts: their intricate relationships, regulation, and functions

Abstract

Centromeres are no longer considered to be silent. Both centromeric and pericentric transcription have been discovered, and their RNA transcripts have been characterized and probed for functions in numerous monocentric model organisms recently. Here, we will discuss the challenges in centromere transcription studies due to the repetitive nature and sequence similarity in centromeric and pericentric regions. Various technological breakthroughs have helped to tackle these challenges and reveal unique features of the centromeres and pericentromeres. We will briefly introduce these techniques, including third-generation long-read DNA and RNA sequencing, protein-DNA and RNA–DNA interaction detection methods, and epigenomic and nucleosomal mapping techniques. Interestingly, some newly analyzed repeat-based holocentromeres also resemble the architecture and the transcription behavior of monocentromeres. We will summarize evidences that support the functions of the transcription process and stalling, and those that support the functions of the centromeric and pericentric RNAs. The processing of centromeric and pericentric RNAs into multiple variants and their diverse structures may also provide clues to their functions. How future studies may address the separation of functions of specific centromeric transcription steps, processing pathways, and the transcripts themselves will also be discussed.

The first chicken oocyte nucleus whole transcriptomic profile defines the spectrum of maternal mRNA and non-coding RNA genes transcribed by the lampbrush chromosomes

“…In our oocyte nuclear RNA-seq data, both Kronos and adjacent CNM repeat arrays on GGA32 undergo transcription during the lampbrush stage of oogenesis (Figure 8 g). In line with this, centromeric and pericentromeric RNAs have many functions at the centromeres and in the heterochromatin of the pericentromeres (Zhu et al . 2023).…”

The role of RNA in the maintenance of chromatin domains as revealed by antibody-mediated proximity labelling coupled to mass spectrometry

“…For instance, dosage compensatory RNA Xist in mammals or Rox in Drosophila specifically associate with the inactive female X or the hyperactive male X chromosome in vivo ( Grimaud and Becker, 2010 ; Galupa and Heard, 2018 ; Samata and Akhtar, 2018 ; Plath et al, 2002 ). RNA transcribed from pericentromeric or centromeric chromatin bind plays a key role in setting up the structure of the centromere and the clustering of distinct centromeres in interphase ( Corless et al, 2020 ; Zhu et al, 2023 ). To investigate the RNA-dependent proteomic neighbourhood of distinct nuclear domains like the hyperactive X chromosome or the chromocenter, we performed AMPL-MS for MSL2 and CID in the presence or absence of RNase A ( Figure 4a and Supplementary files 9–12 ).…”

RepEnTools: an automated repeat enrichment analysis package for ChIP-seq data reveals hUHRF1 Tandem-Tudor domain enrichment in young repeats

“…For humans there are already available a haploid (chm13v2) and most recently a diploid male T2T genome [ 2 , 3 , 7 ], and the human pangenome project will continue to broaden these horizons [ 6 ]. These new tools have already generated a wealth of new information and given valuable insights into some epigenetic processes on REs [ 4 , 13 , 14 , 63 ]. At the same time, our understanding of RE function and their important influence on epigenetic regulation during development [ 48 ], in health [ 64 , 65 ] and disease [ 66 – 69 ] increases.…”