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Deletion of Drosophila Nopp140 induces subcellular ribosomopathies

Abstract

The nucleolar and Cajal body phosphoprotein of 140 kDa (Nopp140) is considered a ribosome assembly factor, but its precise functions remain unknown. To approach this problem, we deleted the Nopp140 gene in Drosophila using FLP-FRT recombination. Genomic PCR, reverse transcriptase-PCR (RT-PCR), and immunofluorescence microscopy confirmed the loss of Nopp140, its messenger RNA (mRNA), and protein products from all tissues examined. Nopp140-/- larvae arrested in the second instar stage and most died within 8 days. While nucleoli appeared intact in Nopp140-/- cells, the C/D small nucleolar ribonucleoprotein (snoRNP) methyltransferase, fibrillarin, redistributed to the nucleoplasm in variable amounts depending on the cell type; RT-PCRs showed that 2′-O-methylation of ribosomal RNA (rRNA) in Nopp140-/- cells was reduced at select sites within both the 18S and 28S rRNAs. Ultrastructural analysis showed that Nopp140-/- cells were deficient in cytoplasmic ribosomes, but instead contained abnormal electron-dense cytoplasmic granules. Immunoblot analysis showed a loss of RpL34, and metabolic labeling showed a significant drop in protein translation, supporting the loss of functional ribosomes. Northern blots showed that pre-RNA cleavage pathways were generally unaffected by the loss of Nopp140, but that R2 retrotransposons that naturally reside within the 28S region of normally silent heterochromatic Drosophila ribosomal DNA (rDNA) genes were selectively expressed in Nopp140-/- larvae. Unlike copia elements and the related R1 retrotransposon, R2 expression appeared to be preferentially dependent on the loss of Nopp140 and not on environmental stresses. We believe the phenotypes described here define novel intracellular ribosomopathies resulting from the loss of Nopp140.

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Acknowledgments

This work was supported by the National Science Foundation, award MCB0919709. We thank Ying Xiao of LSU’s Socolofsky Microscopy Center for thick and thin sectioning Drosophila tissues. We thank Jim Wilhelm for providing the antibody against Drosophila DCP-1. We also thank high school student Molly Lieux of St. Joseph’s Academy of Baton Rouge for her assistance in the environmental stress, RT-PCR experiments.

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Correspondence to Patrick DiMario.

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Fang He and Allison James contributed equally and are co-first authors.

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He, F., James, A., Raje, H. et al. Deletion of Drosophila Nopp140 induces subcellular ribosomopathies. Chromosoma 124, 191–208 (2015). https://doi.org/10.1007/s00412-014-0490-9

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