Ribosome and Ribosome Biogenesis: Comparison
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The ribosome represents a complex macromolecular structure composed of RNA and proteins, interacting through an intricate and interlinked network to sustain its fundamental ancient functionalities. The synthesis of ribosomes entails a sophisticated and energetically demanding process that induced cells during their evolution to select a range of stringent control mechanisms across diverse cellular signalling pathways. In actively dividing cells, there's a stimulation to generate new ribosomes to cope with heightened biosynthetic requirements. Nevertheless, when signals of cellular stress emerge or disruptions arise within the ribosome biogenesis process, there is a rapid cessation of rRNA transcription, leading to interruptions at various stages of ribosome assembly. The impairment of the accurate construction and function of ribosomes characterises a range of dysfunctions commonly identified as ribosomopathies.

  • ribosomal origins and evolution
  • RNA-binding proteins
  • ribosomal RNA

1. Introduction

RNA-binding proteins (RBPs) are a broad group of proteins that specifically bind to RNA molecules, forming ribonucleoprotein particles (RNPs) through interactions with their RNA-binding domains (RBDs), including RNA recognition motifs (RRMs), K homology (KH) domains, double-stranded RNA-binding domains (dsRBDs), intrinsically disordered regions (IDRs) and others [1]. RBPs play a crucial role in numerous biological processes of all living organisms, ranging from transcription to splicing, from modification to intracellular trafficking, and from translation to decay. To date, more than 1500 RBPs have been identified in humans [2],[3] and their activity and regulation are essential for the proper function of many biological processes. Therefore, it is not surprising that the impaired function of RBPs can lead to the development of a wide range of diseases, ranging from genetic disorders to cancer [4],[5],[6],[7]. Among the plethora of RNPs, ribosomes can be considered their archetype, having appeared in their archaic form about 4 billion years ago and remaining highly conserved throughout extant life (Figure 1) [8],[9],[10]. Current ribosomes are macromolecules composed of ribosomal RNA (rRNA) and ribosomal proteins (RPs), whose composition is believed to have been selected during evolution to contribute to the improved fitness of RNA molecules with peptidyl transferase activity (PTA) and to ensure accurate and efficient reading of the genetic code. Numerous ribosome biogenesis factors (RBFs), also represented among themselves by RBPs, participate in the proper assembly and function of the mature ribosome. Nowadays, ribosomes control the expression of almost all proteins present in living organisms, and the impairment of their functions results in the emergence of a set of diseases, including ribosomopathies and cancer.
Figure 1. Schematic depiction of the evolutionary distribution of ribosomal proteins across superkingdoms. Universal ribosomal proteins are depicted in white within the central area of the three intersecting circles. Ribosomal proteins specific to bacteria are located within the purple section of the lower circle, while those specific to eukaryotes can be found in the light blue section on the left. Ribosomal proteins exclusive to archaea are situated within the region emerging from the overlapping light blue and green circles. Notably, all archaea-specific ribosomal proteins are also present in eukarya, indicating the absence of any ribosomal proteins unique to archaea. The nomenclature of ribosomal proteins is consistent with the literature criteria [11].

2. Overview of Ribosome and Ribosome Biogenesis

The present-day ribosomes consist of both small (30S and 40S) and large (50S and 60S) subunits in prokaryotes and eukaryotes, respectively, and they exhibit a highly conserved three-dimensional structure in all living cells, as shown in Figure 2 [12].
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Figure 2. The structure of ribosomes. A side-by-side comparison of the structures of prokaryotic (E. coli, pdb ID 7K00) and eukaryotic (H. sapiens, pdb ID: 6QZP) ribosomes. Ribosomes consist of the large (blue) and the small (red) subunit which comprise a combination of ribosomal RNA (rRNA) molecules and proteins. The rRNA molecules provide the basic building block of the ribosome, establishing its basic structure and functional characteristics. The ribosomal proteins contribute to the overall stability and integrity of the ribosome by bridging structural gaps and promoting the efficient synthesis of proteins. At the center of the figure, rRNA backbone ribbons extracted from superimposed large ribosomal subunits display noticeable variations in size compared to their conserved three-dimensional conformation. The bacterium (E. coli) is green, and the eukaryote (H. sapiens) is blue.
Their reciprocal association forms the 70S complex in prokaryotes and the 80S complex in eukaryotes, creating the integral A (aminoacyl), P (peptidyl) and E (exit) sites. The A site accepts incoming aminoacyl-tRNA, the P site holds the tRNA with the growing peptide chain and the E site accommodates the deacylated tRNA before it departs from the ribosome. The precise order in which amino acids are incorporated into nascent polypeptide chains depends on the accuracy with which the genetic information in the mRNA is encoded by the ribosomes through the coordinate action of the mRNA, tRNA and various translation factors. Achieving this accuracy requires the ribosomes to undergo a complex and energy-intensive process of biogenesis. In eukaryotes, ribosome biogenesis initiates in the nucleolus, which is a specialized nuclear region for ribosome production that involves all three primary RNA polymerases. RNA polymerase I transcribes rDNA to produce the 47S polycistronic precursor pre-rRNA (35S in yeast), which undergoes further processing to yield mature rRNAs: 18S, 5.8S and 28S. RNA polymerase II generates a class of messenger RNAs (mRNA) known as 5′-Terminal-Oligo-Pyrimidine (TOP)-mRNAs, encoding ribosomal proteins (RPs) and ribosome biogenesis factors (RBFs). These motifs help coordinate the regulation of all ribosome biogenesis and translation components [13]. RNA polymerase III synthesizes the 5S rRNA, which becomes part of the large ribosomal subunit [14]. The sequential assembly of RPs and rRNAs relies on a series of transient factors referred to as ribosomal assembly factors (RAFs) or ribosome biogenesis factors (RBFs). These factors include small nucleolar ribonucleoproteins (snoRNPs), nucleases, ATPases, GTPases, RNA helicases and other proteins without predicted enzymatic activity. In eukaryotes, more than 200 of these factors have been identified, and their coordinated interaction is essential for functional ribosome formation [15],[16]. Some of these factors are associated with the pre-rRNA 47S to form the 90S pre-ribosome, inducing specific exo- and endonucleolytic cleavages in premature rRNA [17],[18]. Others participate in concurrent post-transcriptional modifications of approximately 200 rRNA nucleotides. These modifications include pseudouridylation and 2′-O-ribose methylation. They are catalyzed by two types of small nucleolar ribonucleoprotein complexes: H/ACA box snoRNPs and C/D box snoRNPs, respectively [19],[20],[21], that together cover around 95% of identified rRNA post-transcriptional modifications, with the remaining 5% involving acetylation or other types of changes [22],[23],[24],[25]. It is worth noting that the nucleotides targeted by snoRNPs are in crucial regions of the ribosome, including the peptidyl transferase and decoding centers. These modifications contribute to both the correct folding of rRNA and, consequently, the proper functioning of ribosomes [26],[27],[28],[29]. Additional ribosome biogenesis factors known as “placeholders” temporarily bind to specific sites on nascent ribosomes until these sites are structurally ready for other factors to take over and prevent premature recruitment of subsequent factors, early formation of structures and potential folding issues [30]. The initial stages of ribosome biogenesis in the nucleolus yield the pre-40S and pre-60S subunits, which are then exported to the cytoplasm for final maturation. The list of factors involved in the correct assembly of functional ribosomes is extensive and the detailed description for all of them is beyond the scope of this revisewarch, although their high number gives an idea of the complexity of the process, making it one of the most energy-intensive for cell growth [31]. As a result, rigorous control mechanisms have evolved to ensure the quality of ribosome biogenesis through various cell signaling pathways, including c-Myc, MAPK/ERK and mTORC1. These pathways allow ribosome biogenesis rates to adapt to changing environmental conditions [32],[33],[34],[35]. When normal mammalian cells receive stimuli promoting cell proliferation, they respond by increasing ribosome biogenesis and protein synthesis. The gained ribosome production enables them to meet the increased biosynthetic demands associated with cell division, ensuring that daughter cells possess the necessary cellular machinery for survival and normal function [36],[37]. Conversely, exposure to various stressors (such as doxorubicin, replication stress, hypoxia and growth factor deprivation), or the compromised functioning of ribosomes themselves, leads to an immediate arrest of rRNA transcription and subsequent disruption of various steps in ribosome biogenesis. This is accomplished through the activation of nucleolar stress by various routes, involving factors like p53, ARF, PTEN and pRB [38],[39],[40],[41],[42],[43],[44]. In the context of cancer cells, the dysregulation of tumor suppressor genes and proto-oncogenes results in the upregulation of ribosome biogenesis [45]. This, in turn, accelerates cell growth by altering the rate of cell cycle progression. Therefore, changes in ribosome biogenesis rates can be considered a consequence of neoplastic transformation [46]. However, even alterations in protein synthesis levels per se can induce neoplastic transformation. Increased expression of proteins involved in the control of translation initiation, such as eIF4E, leads to changes in mRNA translation, resulting in tumor formation [47],[48]. Additionally, evidence from ribosomal disorders suggests that changes in both the quantity and quality of ribosomes can, on their own, shift the pool of translated mRNAs toward promoting neoplastic transformation [49]. However, despite stringent quality controls of ribosome biogenesis, since their first identification, ribosomes appear to be different [50]. The next progressive technical improvements made to their study confirmed the marked diversity of ribosomal particles between different types of cells of the same organism or during the different stages of organism development to such an extent that today we speak of heterogeneous ribosomes [51],[52],[53]. Sources of diversity arise both from RP content and post-translational modifications (PTMs) of RPs [54] and from rRNA sequences and their post-transcriptional modifications [55],[56],[57], as well as the type of non-ribosomal proteins bound to them [58] and the substitution of RP paralogs [59],[60]. To date there is no univocal and definitive vision regarding the role of the heterogeneous ribosomal architecture and the physiological role for some of their modifications is not yet fully known. However, ribosomes can be perceived as a hub for the integration of a set of spatiotemporal intra- and extracellular signals that would lead to dynamic variations in their composition [61],[62],[63],[64]. At any time, the different combination of PTMs and/or RBPs bound to the ribosomes could change their binding affinity for specific structures or sequence motifs of specific mRNA resulting in alterations of their translational activity [65],[66].

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