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Front. Biol.    2017, Vol. 12 Issue (1) : 19-48    https://doi.org/10.1007/s11515-017-1439-1
REVIEW
Putting it all together: intrinsic and extrinsic mechanisms governing proteasome biogenesis
Lauren A. Howell1,Robert J. Tomko Jr.1(),Andrew R. Kusmierczyk2()
1. Department of Biomedical Sciences, Florida State University College of Medicine, Tallahassee, FL 32306, USA
2. Department of Biology, Indiana University-Purdue University Indianapolis, Indianapolis, IN 46202, USA
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Abstract

BACKGROUND: The 26S proteasome is at the heart of the ubiquitin-proteasome system, which is the key cellular pathway for the regulated degradation of proteins and enforcement of protein quality control. The 26S proteasome is an unusually large and complicated protease comprising a 28-subunit core particle (CP) capped by one or two 19-subunit regulatory particles (RP). Multiple activities within the RP process incoming ubiquitinated substrates for eventual degradation by the barrel-shaped CP. The large size and elaborate architecture of the proteasome have made it an exceptional model for understanding mechanistic themes in macromolecular assembly.

OBJECTIVE: In the present work, we highlight the most recent mechanistic insights into proteasome assembly, with particular emphasis on intrinsic and extrinsic factors regulating proteasome biogenesis. We also describe new and exciting questions arising about how proteasome assembly is regulated and deregulated in normal and diseased cells.

METHODS: A comprehensive literature search using the PubMed search engine was performed, and key findings yielding mechanistic insight into proteasome assembly were included in this review.

RESULTS: Key recent studies have revealed that proteasome biogenesis is dependent upon intrinsic features of the subunits themselves as well as extrinsic factors, many of which function as dedicated chaperones.

CONCLUSION: Cells rely on a diverse set of mechanistic strategies to ensure the rapid, efficient, and faithful assembly of proteasomes from their cognate subunits. Importantly, physiological as well as pathological changes to proteasome assembly are emerging as exciting paradigms to alter protein degradation in vivo.
Keywords proteasome assembly      assembly chaperones      ubiquitin-proteasome system      proteolysis      macromolecular complex     
Corresponding Author(s): Robert J. Tomko Jr.,Andrew R. Kusmierczyk   
Just Accepted Date: 09 January 2017   Online First Date: 16 February 2017    Issue Date: 28 February 2017
 Cite this article:   
Lauren A. Howell,Robert J. Tomko Jr.,Andrew R. Kusmierczyk. Putting it all together: intrinsic and extrinsic mechanisms governing proteasome biogenesis[J]. Front. Biol., 2017, 12(1): 19-48.
 URL:  
https://academic.hep.com.cn/fib/EN/10.1007/s11515-017-1439-1
https://academic.hep.com.cn/fib/EN/Y2017/V12/I1/19
Fig.1  Architecture and composition of the proteasome. (A) The 26S proteasome consists of a 20S core particle (CP), shown in gray, capped on one or both ends by the 19S regulatory particle (RP). The RP can be further divided into lid and base subcomplexes, shown in yellow and blue, respectively. (B) Architecture of the CP α ring. (C) Architecture of the β ring. The three β subunits harboring peptidase activity are in red, whereas the noncatalytic β subunits are in light gray. (D) Subunit arrangement and domain architecture of the RP lid. The lid consists of non-ATPase subunits Rpn3, 5-9, 11, 12, and Rpn15/Sem1. Rpn11, shown in red, harbors the lone intrinsic deubiquitinating (DUB) activity within the proteasome. (E) Subunit composition and architecture of the RP base. The six Rpt ATPases are shown in blue, and the four non-ATPase subunits, Rpn1, 2, 10, and 13, are shown in green. Non-ATPase subunits are shown in their relative positions within the RP. Note that Rpn10 does not directly contact Rpt3 and Rpt4, but rather is suspended above them via subunits of the lid.
Fig.2  Framework of CP assembly. For clarity, assembly factors have been omitted and β subunit propeptides (squiggly lines) are shown only on the catalytically active subunits. CP assembly begins when α subunits coalesce into an α-ring. Early β subunits (β2, β3, β4) bind to the α-ring to form the 13S intermediate. Subsequent entry of the late β subunits (β5, β6, β1) results in the formation of the 15S intermediate. Incorporation of β7 is the rate limiting step of CP assembly and gives rise to a complete half-proteasome. Dimerization of two half-proteasomes forms a transient species, the preholoproteasome (PHP), which undergoes processing of the β subunit propeptides to form the mature CP.
Fig.3  The lid and base assembly pathways. (A) Lid assembly pathway in yeast. (B) Overview of base assembly. Assembly chaperones are omitted for clarity and are addressed in Fig. 7.
Fig.4  Pba1-Pba2 and CP assembly. (A) Pba1-Pba2 functions as a safety. Pba1-Pba2 is shown bound to a series of CP assembly intermediates containing a complete α-ring and various β subunits. The intermediates are shown inverted, relative to their orientation in Fig. 2, to better visualize the binding of the assembly factor. The α-ring in the intermediates prior to the preholoproteasome (PHP) stage is distended, which allows Pba1-Pba2 to lie partially embedded in the axial channel formed by the ring. This is the high affinity state of Pba1-Pba2 bound to an α-ring and makes it impossible for RP to occupy the ring. Following dimerization of half-proteasomes, each α-ring undergoes a conformational change which tightens its radius as the α subunits move closer to the central axis. The resulting narrowing of the axial channel evicts Pba1-Pba2 which assumes a more surface-bound location. As the propeptides are processed and a mature CP forms, Pba1-Pba2 binding switches to a low affinity state which allows it to be easily displaced from the now-functional CP by the RP. (B) Additional functions of Pba1-Pba2. The formation of α-rings is promoted, in an unknown fashion, by Pba1-Pba2. At the same time, Pba1-Pba2 binding to α subunits and/or isolated α-rings prevents these entities from misassembly into non-productive species.
Fig.5  HbYX motif docking into the CP α-ring. (A) A view of the Rpt2, Rpt3, and Rpt5 HbYX motifs docked into the intra-subunit pockets on the outside surface of the CP α ring. The HbYX motifs of Rpt2, Rpt3, and Rpt5 are shown as red spheres, and lie at the interfaces between α1-α2, α3-α4, and α5-α6, respectively. (B) A close-up view of the HbYX motif of Rpt5 docked into the α5-α6 pocket. Rpt5 (beige) inserts its three most C-terminal residues, Phe-Tyr-Ala, into the pocket. The C-terminal carboxylate of the alanine residue (red spheres) interacts with the positively charged side chain of the pocket lysine (blue) contributed by α6, whereas the Phe and Tyr residues (green spheres) make hydrophobic contacts with the interior of the pocket.
Fig.6  Pba3-Pba4 and α-ring assembly. The formation of α-rings is shown in the presence, or absence, of Pba3-Pba4. In both cases, the early events of α-ring assembly are similar and may involve the formation of species containing α5, α6, α7 and α1. However, via a poorly understood mechanism, the presence of Pba3-Pba4 influences the entry of the remaining α subunits (α2, α3 and α4) in an order that generates only canonical α-rings and thus only canonical proteasomes. Arrival of early β subunits displaces Pba3-Pba4, forming the 13S intermediate. In the absence of Pba3-Pba4, the remaining α subunits are not restricted in their order of assembly and (at least) three possible α-rings are formed. One of these is the canonical α-ring which is bound by β subunits to produce canonical proteasomes. Another is an α-ring in which α3 is replaced by a second copy of α4; this gives rise to α4-α4 proteasomes. The third ring, which lacks α4 and has two copies of α2, might form a 13S-like species that is not competent for further assembly.
Fig.7  Overview of base assembly and chaperone eviction. Non-ATPase subunits are omitted for clarity. (A) and (B), Two non-exclusive pathways have been proposed for assembly of the RP base. In the first (A), the base forms independently of the CP. In the second (B), The CP acts as a template or scaffold for the incoming chaperone modules, and each chaperone is released as its respective module docks onto the CP. A gray dotted arrow with question mark indicates the as-yet untested possibility of crosstalk between these two proposed pathways. (C) Proposed mechanism of coupling between ATP hydrolysis and chaperone eviction by the base. The base assumes “down” or “out” conformations according to the nature of the nucleotide bound (ADP-bound vs. ATP-bound). In the ADP-bound, “down” state, the AAA+ small domains (shown as small circles) that are bound by the chaperones point downward, generating steric clash (T-bars) between the chaperones and the CP. In the ATP-bound state, the chaperones are positioned outward, relieving steric hindrance and allowing formation of a metastable chaperone-base-CP complex. Subsequent ATP hydrolysis forcefully repositions the small domains to the down position, which shears the chaperones from the small domains (eviction). Although a full base is shown in this model, the same concept could in principle allow for shearing of chaperones from ATPase-active intermediates as they dock on the CP (B).
Fig.8  Intrinsic regulatory features of the lid important for proteasome biogenesis. (A) Sequence alignment of select Sem1/DSS1 homologs. Conserved binding regions Site 1 and Site 2, as well as the poorly conserved linker region and indicated below the alignment. The region that forms a helix in available EM structures of the proteasome is indicated above the alignment. The acidic residues characteristic of Site 1 and Site 2 are highlighted in red, whereas the conserved tryptophan residues present in Site 2 are highlighted in blue. (B) The cryo-EM structure of the isolated lid from yeast (PDB ID 3JCK) is shown, highlighting the positioning of Sem1 between Rpn3 and Rpn7. Lid subunits Rpn5, 6, 8, 9, 11, and 12 are colored gray, whereas Rpn3 and Rpn7 are colored magenta and cyan, respectively. Only portions of Sem1 are clearly resolved in this structure, but they are shown as green and orange. Site 1 is located within the green segment, and Site 2 within the orange. Inset, conserved acidic residues in Site 1 and Site 2 are shown in space-filling mode as spheres to illustrate their roles in docking Sem1 onto Rpn3 and Rpn7. Conserved tryptophan residues are shown in stick mode in blue and indicated with blue arrows. (C) Conformational changes associated with lid assembly and attachment to the base. In a low-resolution EM structure of LP2, the N-termini of Rpn6 (and potentially Rpn5) are closed inward toward the Rpn8-Rpn11 heterodimer. Lid subunit coloring is the same as in Fig. 3A.
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