ABSTRACT
The functional relevance and the evolution of two parallel mRNA splicing systems in eukaryotes--a major and minor spliceosome that differ in abundance and splicing rate--are poorly understood. We report here that partially spliced pre-mRNAs containing minor-class introns undergo nuclear export and that minor-class snRNAs are predominantly cytoplasmic in vertebrates. Cytoplasmic interference with the minor spliceosome further indicated its functional segregation from the nucleus. In keeping with this, minor splicing was only weakly affected during mitosis. By selectively interfering with snRNA function in zebrafish development and in mammalian cells, we revealed a conserved role for minor splicing in cell-cycle progression. We argue that the segregation of the splicing systems allows for processing of partially unspliced cytoplasmic transcripts, emerging as a result of different splicing rates. The segregation offers a mechanism accounting for spliceosome evolution in a single lineage and provides a means for nucleus-independent control of gene expression.
Subject(s)
Cell Nucleus/metabolism , Cell Proliferation , RNA Precursors/metabolism , RNA Splicing , RNA, Small Nuclear/metabolism , Spliceosomes/metabolism , Animals , Apoptosis , Cytoplasm/metabolism , Gene Expression Regulation , In Situ Hybridization , Introns/genetics , Mice , Mitosis/physiology , NIH 3T3 Cells , RNA, Messenger/genetics , RNA, Messenger/metabolism , RNA, Small Nuclear/genetics , Zebrafish/anatomy & histology , Zebrafish/embryology , Zebrafish/genetics , Zebrafish/growth & developmentABSTRACT
The hugin gene of Drosophila encodes a neuropeptide with homology to mammalian neuromedin U. The hugin-expressing neurons are localized exclusively to the subesophageal ganglion of the central nervous system and modulate feeding behavior in response to nutrient signals. These neurons send neurites to the protocerebrum, the ventral nerve cord, the ring gland, and the pharynx and may interact with the gustatory sense organs. In this study, we have investigated the morphology of the hugin neurons at a single-cell level by using clonal analysis. We show that single cells project to only one of the four major targets. In addition, the neurites of the different hugin cells overlap in a specific brain region lateral to the foramen of the esophagus, which could be a new site of neuropeptide release for feeding regulation. Our study reveals novel complexity in the morphology of individual hugin neurons, which has functional implication for how they coordinate feeding behavior and growth.
Subject(s)
Drosophila Proteins/metabolism , Drosophila/anatomy & histology , Feeding Behavior/physiology , Nerve Net/cytology , Neurons/metabolism , Neuropeptides/metabolism , Animals , Animals, Genetically Modified , Behavior, Animal , Drosophila Proteins/genetics , Ganglia, Invertebrate/cytology , Green Fluorescent Proteins/metabolism , Neurites/physiology , Neurons/cytology , Neuropeptides/geneticsABSTRACT
The Drosophila hugin gene encodes a prepropeptide that can potentially generate several neuropeptides.(1) The gene is expressed in 20 cells of the subesophageal ganglion (SOG) that are involved in modulating feeding behavior.(2) One of the hugin neuropeptides shares homology with mammalian neuromedin U8 (NmU8), which has been shown to regulate feeding behavior in rodents.(3,4) Recent clonal analysis indicated that each hugin expressing neuron projects to one of four main targets: the protocerebrum, the ventral nerve cord, the pharynx and the corpora cardiaca.(5) In addition all hugin neurons send short neurites to a novel region ventro-lateral to the foramen, which we suggested could be the tritocerebrum. In this short article, we discuss two specific issues brought up by these analyses. One concerns the polarity of hugin neurons. The other is an evolutionary perspective on the processing of hugin neuropeptides in light of new data from mass spectrometric and genomic analyses.
