Abstract
Author SummaryEukaryotes—fungi, plants, animals, and many unicellular organisms—are defined by the presence of a cell nucleus that contains the chromosomes and is enveloped by a lipid membrane lined on the inner face with a protein network called the lamina. Among other functions, the lamina serves as an anchorage site for the ends of chromosomes. In multicellular animals (metazoa), the lamina comprises a few related proteins called lamins, which are very important for many functions related to the nucleus; abnormal lamins result in multiple nuclear defects and diseases, including inappropriate gene expression and premature aging. Until now, however, lamins had been found only in metazoa; no protein of equivalent function had been identified in plants, fungi, or unicellular organisms. Here, we describe a protein from African trypanosomes—the single-cell parasites that cause sleeping sickness—that fulfils many lamin-like roles, including maintaining nuclear structure and organizing the chromosomes of this organism. We show that this protein, which we call NUP-1 for nuclear periphery protein-1, is vital for the antigenic variation mechanisms that allow the parasite to escape the host immune response. We propose that NUP-1 is a lamin analogue that performs similar functions in trypanosomes to those of authentic lamins in metazoa. These findings, we believe, have important implications for understanding the evolution of the nucleus.
Highlights
Eukaryotic genomes are primarily organized as linear chromosomes and further segregated into transcriptionally active euchromatin and repressed heterochromatin [1,2,3]
A single NUP-1 syntenic orthologue was present in each trypanosomatid genome examined (Figure 1, Table S1), each exhibiting the same structure as NUP-1 but varying in size and number of repeats; the repeats within each NUP-1 orthologue are nearly identical but diverge significantly between species
While structures that resemble the nucleoskeletal metazoan lamina and heterochromatin are recognized in many eukaryotic lineages, the lamin proteins themselves are clearly restricted to the metazoa [7,15], and no lamina components have been unequivocally identified to date in any non-metazoan organism
Summary
Eukaryotic genomes are primarily organized as linear chromosomes and further segregated into transcriptionally active euchromatin and repressed heterochromatin [1,2,3]. In metazoa such chromatin organization requires the coiled-coil lamins, intermediate filament proteins that form a stable meshwork between the nuclear envelope (NE) and nuclear matrix, physically associating with peripheral heterochromatin [2,4,5]. Lamins directly participate in nuclear pore complex (NPC) positioning, maintenance of nuclear structure, spindle assembly, and control of developmental gene expression programs [6,7,8,9].
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