Components of Coated Vesicles and Nuclear Pore Complexes Share a Common Molecular Architecture

Abstract

Numerous features distinguish prokaryotes from eukaryotes, chief among which are the distinctive internal membrane systems of eukaryotic cells. These membrane systems form elaborate compartments and vesicular trafficking pathways, and sequester the chromatin within the nuclear envelope. The nuclear pore complex is the portal that specifically mediates macromolecular trafficking across the nuclear envelope. Although it is generally understood that these internal membrane systems evolved from specialized invaginations of the prokaryotic plasma membrane, it is not clear how the nuclear pore complex could have evolved from organisms with no analogous transport system. Here we use computational and biochemical methods to perform a structural analysis of the seven proteins comprising the yNup84/vNup107–160 subcomplex, a core building block of the nuclear pore complex. Our analysis indicates that all seven proteins contain either a β-propeller fold, an α-solenoid fold, or a distinctive arrangement of both, revealing close similarities between the structures comprising the yNup84/vNup107–160 subcomplex and those comprising the major types of vesicle coating complexes that maintain vesicular trafficking pathways. These similarities suggest a common evolutionary origin for nuclear pore complexes and coated vesicles in an early membrane-curving module that led to the formation of the internal membrane systems in modern eukaryotes.

Integrative structure and functional anatomy of a nuclear pore complex

“…11), which led us to hypothesize that they share a common evolutionary ancestor termed the “protocoatomer” 34 . Two major families of coating complexes exist: COPI/clathrin and COPII, with each having discrete vesicle recognition and trafficking roles 35,36 .…”

Evolution and persistence of the cilium

“…IFT-52 possesses a GIFT domain, also found in the flavobacterial gliding protein GldG and certain other bacterial proteins [Beatson and Ponting, 2004]. Ciliary necklace and nuclear pore Coated vesicle scaffold proteins share a common molecular architecture, not only with the IFT proteins, but also with the nuclear pore complex proteins [Devos et al, 2004], suggesting that the barrier function of the nuclear pore and selectivity of the ciliary necklace may have a common origin. Nuclear pore selectivity requires nuclear localization signals and a transport mechanism.…”

Regarding the presence of membrane coat proteins in bacteria: Confusion? What confusion?

“…The protocoatomer theory states that the MC architecture is composed of an Nt-beta-propeller followed by a Ct-alpha-solenoid [8]. There is no doubt that all proteins we have detected in PVC members do have the MC architecture (Table 2 in ref.…”

“…It is important to state here that despite the homology between eukaryotic MCs, their sequences and structures have diverged almost beyond the point of recognition. Notwithstanding this divergence, it is now broadly accepted that the eukaryotic MCs have a common origin, a prediction we made four years before the first crystallographic support was obtained [8,9]. A structural comparison of the alpha-helical repeats using one of the most accurate tools available today, COPS (topsearch.services.came.sbg.ac.at, [10]), reveals that the predicted structures of the bacterial MCs do not differ more from the eukaryotic MCs than the eukaryotic MCs do between themselves.…”