Specialized eRpL22 paralogue-specific ribosomes regulate specific mRNA translation in spermatogenesis in<i>Drosophila melanogaster</i>

Mageeney, Catherine M.; Ware, Vassie C.

doi:10.1091/mbc.e19-02-0086

Cited by 29 publications

(29 citation statements)

References 76 publications

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…The function of the RpL22 and RpL22-like paralog pair in Drosophila testis has been explored and it has been suggested that the two proteins are not functionally redundant in development or spermatogenesis. However, knockdown of RpL22 is partially rescued by RpL22-like and vice versa [34, 35]. Further work is needed to directly link effects on ribosome composition and mRNA translational output, as the two paralogs may interact with different pools of mRNA in the testis [35].…”

Section: Discussionmentioning

confidence: 99%

See 1 more Smart Citation

Ribosome heterogeneity inDrosophila melanogastergonads through paralog-switching

Aspden

Fontana

O’Connell

et al. 2020

Preprint

View full text Add to dashboard Cite

13Ribosomes have long been thought of as homogeneous, macromolecular machines but 14 recent evidence suggests they are heterogeneous and their specialisation can regulate translation. 15Here, we have characterised ribosomal protein heterogeneity across 5 tissues of Drosophila 16 melanogaster. We find that testis and ovary contain the most heterogeneous ribosome populations, 17 and that specialisation in these tissues occurs through paralog-switching. For the first time, we have 18 solved structures of ribosomes purified from in vivo tissues by cryo-EM, revealing differences in 19 precise ribosomal arrangement for testis and ovary 80S ribosomes. Differences in the amino acid 20 composition of paralog pairs and their localisation on the ribosome exterior indicate paralog-21 switching could alter the ribosome surface, enabling different proteins to regulate translation. One 22 testis-specific paralog-switching pair is also found in humans, suggesting this is a conserved site of 23 ribosome specialisation. Overall, this work allows us to propose possible mechanisms by which 24 ribosome specialisation can regulate translation. 25 26 27 48 effects [1], whilst RpL38 mutants in D. melanogaster exhibit large wings, small bristles, delayed 49 development and disorganised wing hair polarity [14]. 50 2 Human cytoplasmic ribosomes usually comprise of 80 RPs and 4 rRNAs. This is similar across 51 the majority of multicellular eukaryotes including D. melanogaster with 80 RPs and 5 rRNAs. 52 However, annotated in FlyBase there are 93 cytoplasmic RP genes, including 39 small subunit 53 proteins and 54 large subunit proteins [15]. These additional genes code for 13 paralogs in D. 54 melanogaster. In fact, across eukaryotes many RP genes possess paralogs, for example human RpL3 55 and RpL3L [11] and Arabidopsis RpS8A and RpS8B [13]. In total, there are 19 pairs of paralogs in 56 humans [4] and all 80 RPs in Arabidopsis thaliana have paralogs [16].57 To dissect the function of ribosome heterogeneity it is necessary to understand biological 58 importance within context of whole organisms. Within the developmental biology field, a large 59 proportion of research focuses on the contribution of transcription to gene expression control.60 However, during development a variety of processes and key time points are highly dependent on 61 the regulation of mRNA translation (oogenesis in Xenopus [17], early embryo development in 62 Drosophila [18] and mammalian erythropoiesis [19]). The balance between self-renewal and 63 differentiation at the stem cell niche is highly dependent on translation in both the ovary and the 64 testis [20]. This is exemplified by disruptions to the stem cell niche in the testis when RPs are 65 knocked down e.g. RpL19 RNAi results in over-proliferation of early germ cells in D. melanogaster 66 [21]. During the meiotic phase of gametogenesis, transcription does not occur [22]; therefore 67 meiotic cells rely on post-transcriptional gene regulation [23]. The translational machinery has 68 evolved to become specialise...

show abstract

Section: Discussionmentioning

confidence: 99%

“…However, knockdown of RpL22 is partially rescued by RpL22-like and vice versa [34, 35]. Further work is needed to directly link effects on ribosome composition and mRNA translational output, as the two paralogs may interact with different pools of mRNA in the testis [35].…”

Section: Discussionmentioning

confidence: 99%

Ribosome heterogeneity inDrosophila melanogastergonads through paralog-switching

Aspden

Fontana

O’Connell

et al. 2020

Preprint

View full text Add to dashboard Cite

show abstract

“…Co-expression of eRpL22 along with eRpL22-like within eye tissue cell types is consistent with the hypothesis that eRpL22 and eRpL22-like have functionally distinct roles within these cells. These roles may include distinctive ribosome-related functions, including their assembly into specialized ribosomes (eg, 1,11,12,22 ) or roles that are independent of ribosomal processes (eg, reviewed by 9,35 ). We used IHC and confocal microscopy to assess eRpL22-like localization relative to other large subunit Rps, RpL9 and RpL23a or to the nucleolar marker fibrillarin.…”

Section: Ribosomal Roles Are Implicated For Erpl22-like In Eye Devementioning

confidence: 99%

“…In fact, we have recently demonstrated unique patterns of specific translation on eRpL22 ribosomes and eRpL22-like ribosomes in the germline. 22 A complete developmental eRpL22-like expression profile within the developing eye is necessary to understand functional contributions of this Rp to developmental and differentiation processes required to build an eye.…”

Section: Introductionmentioning

confidence: 99%

Tissue‐specific expression of ribosomal protein paralogue eRpL22‐like in Drosophila melanogaster eye development

Gershman

Pritchard

Chaney

et al. 2020

Developmental Dynamics

Self Cite

View full text Add to dashboard Cite

Background Differences in core or tissue‐specific ribosomal protein (Rp) composition within ribosomes contribute to ribosome heterogeneity and functional variability. Yet, the degree to which ribosome heterogeneity modulates development is unknown. The Drosophila melanogaster eRpL22 family contains structurally diverse paralogues, eRpL22 and eRpL22‐like. Unlike ubiquitously expressed eRpL22, eRpL22‐like expression is tissue‐specific, notably within the male germline and the eye. We investigated expression within the developing eye to uncover tissue/cell types where specific paralogue roles might be defined. Results Immunohistochemistry analysis confirms ubiquitous eRpL22 expression throughout eye development. In larvae, eRpL22‐like is ubiquitously expressed, but highly enriched in the peripodial epithelium (PE). In early pupae, eRpL22‐like is broadly distributed in multiple cell types, but later, is primarily enriched in interommatidial hair cells (IoHC). Adult patterns include the ring of accessory cells around ommatidia. Adult retinae IoHC patterning phenotypes (shown by scanning electron microscopy) may be linked to RNAi‐mediated eRpL22‐like depletion within larval PE. Immunoblots and polysome profile analyses show multiple variants of eRpL22‐like across development, with the variant at the expected molecular mass co‐sedimenting with active ribosomes. Conclusion Our data reveal differential patterns of eRpL22‐like expression relative to eRpL22 and suggest a specific role for eRpL22‐like in developmental patterning of the eye.

show abstract

“…Brian McStay (National University of Ireland, Galway) described nucleolar formation and subsequent fusion in human cells from a chromosomal perspective. Using monochromosomal cell hybrids to engineer individual NOR 3 -bearing acrocentric chromosomes, he showed that their p-arms with fused proximal and distal junctions lacking intervening rDNA still associate with nucleoli. He also showed that individual NORs occupy distinct territories within large mature nucleoli.…”

Section: Rdna Dynamicsmentioning

confidence: 99%

Emerging Roles for the Nucleolus 2019

Baserga

Duncan

2020

Journal of Biological Chemistry

View full text Add to dashboard Cite

The nucleolus is the central organelle within eukaryotic cells whose primary function is to generate ribosomes, the major protein producing machines within all cells. New roles for the nucleolus are continuously emerging as we explore its molecular intricacies. Despite the central and fundamental role of the nucleolus in cell biology, there has previously been no single official meeting that enables the gathering of scientists whose research converges on the nucleolus. As a result, the community of researchers who study this organelle risks fragmentation across disciplines. The Emerging Roles for the Nucleolus Symposium, which has now taken place twice on a biennial basis, first in 2017 (1) and again in 2019, therefore, represents the first of its kind. The overarching goals of this symposium are (a) to convene researchers who study the nucleolus across model systems (yeast, nematodes, fruit flies, mouse, human cell lines) and biological perspectives (structural, biophysical, molecular, cellular, pathophysiology), (b) to share and disseminate the latest research breakthroughs in nucleolar biology, (c) to promote interaction, engagement, and collaboration centered on the nucleolus across disciplines, and (d) to provide trainees and early career investigators with an organelle-specific scientific community of support.

show abstract

Specialized eRpL22 paralogue-specific ribosomes regulate specific mRNA translation in spermatogenesis inDrosophila melanogaster

Cited by 29 publications

References 76 publications

Ribosome heterogeneity inDrosophila melanogastergonads through paralog-switching

Ribosome heterogeneity inDrosophila melanogastergonads through paralog-switching

Tissue‐specific expression of ribosomal protein paralogue eRpL22‐like in Drosophila melanogaster eye development

Emerging Roles for the Nucleolus 2019

Contact Info

Product

Resources

About