Coatomer in the universe of cellular complexity
Jazyk angličtina Země Spojené státy americké Médium print
Typ dokumentu časopisecké články, Research Support, N.I.H., Extramural, práce podpořená grantem
Grantová podpora
P41 GM109824
NIGMS NIH HHS - United States
R01 CA228351
NCI NIH HHS - United States
R01 GM112108
NIGMS NIH HHS - United States
204697/Z/16/Z
Wellcome Trust - United Kingdom
PubMed
36399624
PubMed Central
PMC9727805
DOI
10.1091/mbc.e19-01-0012
Knihovny.cz E-zdroje
- MeSH
- biologická evoluce MeSH
- COP-vezikuly MeSH
- endozomální třídící komplexy pro transport metabolismus MeSH
- Eukaryota * genetika MeSH
- eukaryotické buňky * metabolismus MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Research Support, N.I.H., Extramural MeSH
- Názvy látek
- endozomální třídící komplexy pro transport MeSH
Eukaryotic cells possess considerable internal complexity, differentiating them from prokaryotes. Eukaryogenesis, an evolutionary transitional period culminating in the last eukaryotic common ancestor (LECA), marked the origin of the eukaryotic endomembrane system. LECA is reconstructed as possessing intracellular complexity akin to modern eukaryotes. Construction of endomembrane compartments involved three key gene families: coatomer, BAR-domain proteins, and ESCRT. Each has a distinct evolutionary origin, but of these coatomer and BAR proteins are eukaryote specific, while ESCRT has more ancient origins. We discuss the structural motifs defining these three membrane-coating complexes and suggest that compared with BAR and ESCRT, the coatomer architecture had a unique ability to be readily and considerably modified, unlocking functional diversity and enabling the development of the eukaryotic cell.
Institute of Parasitology Biology Center Czech Academy of Sciences 37005 Ceske Budejovice Czechia
Laboratory of Cellular and Structural Biology The Rockefeller University New York NY10021
School of Life Sciences University of Dundee Dundee DD1 5EH UK
Zobrazit více v PubMed
Akey CW, Singh D, Ouch C, Echeverria I, Nudelman I, Varberg JM, Yu Z, Fang F, Shi Y, Wang J, et al. (2022). Comprehensive structure and functional adaptations of the yeast nuclear pore complex. Cell 185, 361–378.e325. PubMed PMC
Bar-Peled L, Chantranupong L, Cherniack AD, Chen WW, Ottina KA, Grabiner BC, Spear ED, Carter SL, Meyerson M, Sabatini DM (2013). A Tumor suppressor complex with GAP activity for the Rag GTPases that signal amino acid sufficiency to mTORC1. Science 340, 1100–1106. PubMed PMC
Beck M, Mosalaganti S, Kosinski J (2018). From the resolution revolution to evolution: structural insights into the evolutionary relationships between vesicle coats and the nuclear pore. Curr Opin Struct Biol 52, 32–40. PubMed
Bethune J, Wieland FT (2018). Assembly of COPI and COPII Vesicular Coat Proteins on Membranes. Annu Rev Biophys 47, 63–83. PubMed
Bley CJ, Nie S, Mobbs GW, Petrovic S, Gres AT, Liu X, Mukherjee S, Harvey S, Huber FM, Lin DH, et al. (2022). Architecture of the cytoplasmic face of the nuclear pore. Science 376, eabm9129. PubMed PMC
Carman PJ, Dominguez R (2018). BAR domain proteins-a linkage between cellular membranes, signaling pathways, and the actin cytoskeleton. Biophys Rev 10, 1587–1604. PubMed PMC
Caspi Y, Dekker C (2018). Dividing the archaeal way: the ancient Cdv cell-division machinery. Front Microbiol 9, 174. PubMed PMC
D’Angelo MA (2018). Nuclear pore complexes as hubs for gene regulation. Nucleus (Austin, Tex.) 9, 142–148. PubMed PMC
Dacks JB, Field MC (2007). Evolution of the eukaryotic membrane-trafficking system: origin, tempo and mode. J Cell Sci 120, 2977–2985. PubMed
Dacks JB, Robinson MS (2017). Outerwear through the ages: evolutionary cell biology of vesicle coats. Curr Opin Cell Biol 47, 108–116. PubMed
De Magistris P (2021). The great escape: mRNA export through the nuclear pore complex. Int J Mol Sci 22, 11767. PubMed PMC
Devos D, Dokudovskaya S, Alber F, Williams R, Chait BT, Sali A, Rout MP (2004). Components of coated vesicles and nuclear pore complexes share a common molecular architecture. PLoS Biol 2, e380. PubMed PMC
Devos D, Dokudovskaya S, Williams R, Alber F, Eswar N, Chait BT, Rout MP, Sali A (2006). Simple fold composition and modular architecture of the nuclear pore complex. Proc Natl Acad Sci USA 103, 2172–2177. PubMed PMC
Dokudovskaya S, Waharte F, Schlessinger A, Pieper U, Devos DP, Cristea IM, Williams R, Salamero J, Chait BT, Sali A, et al. (2011). A conserved coatomer-related complex containing Sec13 and Seh1 dynamically associates with the vacuole in Saccharomyces cerevisiae. Mol Cell Proteomics 10, M110 006478. PubMed PMC
Fernandez-Martinez J, Rout MP (2021). One ring to rule them all? structural and functional diversity in the nuclear pore complex. Trends Biochem Sci 46, 595–607. PubMed PMC
Field MC, Rout MP (2019). Pore timing: the evolutionary origins of the nucleus and nuclear pore complex. F1000Res 8, 16402.1. PubMed PMC
Field MC, Sali A, Rout MP (2011). Evolution: On a bender–BARs, ESCRTs, COPs, and finally getting your coat. J Cell Biol 193, 963–972. PubMed PMC
Fontana P, Dong Y, Pi X, Tong AB, Hecksel CW, Wang L, Fu TM, Bustamante C, Wu H (2022). Structure of cytoplasmic ring of nuclear pore complex by integrative cryo-EM and AlphaFold. Science 376, eabm9326. PubMed PMC
Grant CR, Wan J, Komeili A (2018). Organelle formation in bacteria and archaea. Annu Rev Cell Dev Biol 34, 217–238. PubMed
Hayama R, Rout MP, Fernandez-Martinez J (2017). The nuclear pore complex core scaffold and permeability barrier: variations of a common theme. Curr Opin Cell Biol 46, 110–118. PubMed PMC
Holzer G, Antonin W (2018). Nuclear pore complexes: global conservation and local variation. Curr Biol 28, R674–R677. PubMed
Junglas B, Huber ST, Heidler T, Schlosser L, Mann D, Hennig R, Clarke M, Hellmann N, Schneider D, Sachse C (2021). PspA adopts an ESCRT-III-like fold and remodels bacterial membranes. Cell 184, 3674–3688.e3618. PubMed
Kim SJ, Fernandez-Martinez J, Nudelman I, Shi Y, Zhang W, Raveh B, Herricks T, Slaughter BD, Hogan JA, Upla P, et al. (2018). Integrative structure and functional anatomy of a nuclear pore complex. Nature 555, 475–482. PubMed PMC
Koumandou VL, Klute MJ, Herman EK, Nunez-Miguel R, Dacks JB, Field MC (2011). Evolutionary reconstruction of the retromer complex and its function in Trypanosoma brucei. J Cell Sci 124, 1496–1509. PubMed PMC
Kuzmin E, Taylor JS, Boone C (2021). Retention of duplicated genes in evolution. Trends Genet 38, 59–72. PubMed PMC
Leung KF, Dacks JB, Field MC (2008). Evolution of the multivesicular body ESCRT machinery; retention across the eukaryotic lineage. Traffic 9, 1698–1716. PubMed
Lin DH, Hoelz A (2019). The structure of the nuclear pore complex (an update). Annu Rev Biochem 88, 725–783. PubMed PMC
Liu J, Tassinari M, Souza DP, Naskar S, Noel JK, Bohuszewicz O, Buck M, Williams TA, Baum B, Low HH (2021). Bacterial Vipp1 and PspA are members of the ancient ESCRT-III membrane-remodeling superfamily. Cell 184, 3660–3673.e3618. PubMed PMC
Loissell-Baltazar YA, Dokudovskaya S (2021). SEA and GATOR 10 years later. Cells 10, 2689. PubMed PMC
Makarov AA, Padilla-Mejia NE, Field MC (2021). Evolution and diversification of the nuclear pore complex. Biochem Soc Trans 49, 1601–1619. PubMed PMC
McCullough J, Clippinger AK, Talledge N, Skowyra ML, Saunders MG, Naismith TV, Colf LA, Afonine P, Arthur C, Sundquist WI, et al. (2015). Structure and membrane remodeling activity of ESCRT-III helical polymers. Science 350, 1548–1551. PubMed PMC
McCullough J, Frost A, Sundquist WI (2018). Structures, functions, and dynamics of ESCRT-III/Vps4 membrane remodeling and fission complexes. Annu Rev Cell Dev Biol 34, 85–109. PubMed PMC
Mosalaganti S, Obarska-Kosinska A, Siggel M, Taniguchi R, Turonova B, Zimmerli CE, Buczak K, Schmidt FH, Margiotta E, Mackmull MT, et al. (2022). AI-based structure prediction empowers integrative structural analysis of human nuclear pores. Science 376, eabm9506. PubMed
Mosalaganti S, Kosinski J, Albert S, Schaffer M, Strenkert D, Salomé PA, Merchant SS, Plitzko JM, Baumeister W, Engel BD, Beck M (2018). In situ architecture of the algal nuclear pore complex. Nat Commun 9, 2361. PubMed PMC
Paci G, Caria J, Lemke EA (2021). Cargo transport through the nuclear pore complex at a glance. J Cell Sci 134, jcs247874. PubMed
Petrovic S, Samanta D, Perriches T, Bley CJ, Thierbach K, Brown B, Nie S, Mobbs GW, Stevens TA, Liu X, et al. (2022). Architecture of the linker-scaffold in the nuclear pore. Science 376, eabm9798. PubMed PMC
Phillips DA, Zacharoff LA, Hampton CM, Chong GW, Malanoski AP, Metskas LA, Xu S, Bird LJ, Eddie BJ, Miklos AE, et al. (2021). A bacterial membrane sculpting protein with BAR domain-like activity. Elife 10, e60049. PubMed PMC
Rout MP, Field MC (2017). The evolution of organellar coat complexes and organization of the eukaryotic cell. Annu Rev Biochem 86, 637–657. PubMed
Samson RY, Obita T, Hodgson B, Shaw MK, Chong PL, Williams RL, Bell SD (2011). Molecular and structural basis of ESCRT-III recruitment to membranes during archaeal cell division. Mol Cell 41, 186–196. PubMed PMC
Simunovic M, Evergren E, Callan-Jones A, Bassereau P (2019). Curving cells inside and out: roles of BAR domain proteins in membrane shaping and its cellular implications. Annu Rev Cell Dev Biol 35, 111–129. PubMed
Sochacki KA, Dickey AM, Strub MP, Taraska JW (2017). Endocytic proteins are partitioned at the edge of the clathrin lattice in mammalian cells. Nat Cell Biol 19, 352–361. PubMed PMC
Suetsugu S, Toyooka K, Senju Y (2010). Subcellular membrane curvature mediated by the BAR domain superfamily proteins. Semin Cell Dev Biol 21, 340–349. PubMed
Traub LM (2009). Clathrin couture: fashioning distinctive membrane coats at the cell surface. PLoS Biol 7, e1000192. PubMed PMC
Valenstein ML, Rogala KB, Lalgudi PV, Brignole EJ, Gu X, Saxton RA, Chantranupong L, Kolibius J, Quast JP, Sabatini DM (2022). Structure of the nutrient-sensing hub GATOR2. Nature 607, 610–616. PubMed PMC
van Dam TJ, Townsend MJ, Turk M, Schlessinger A, Sali A, Field MC, Huynen MA (2013). Evolution of modular intraflagellar transport from a coatomer-like progenitor. Proc Natl Acad Sci USA 110, 6943–6948. PubMed PMC
Vietri M, Radulovic M, Stenmark H (2020). The many functions of ESCRTs. Nat Rev Mol Cell Biol 21, 25–42. PubMed
von Appen A, Kosinski J, Sparks L, Ori A, DiGuilio AL, Vollmer B, Mackmull MT, Banterle N, Parca L, Kastritis P, et al. (2015). In situ structural analysis of the human nuclear pore complex. Nature 526, 140–143. PubMed PMC
Zimmerli CE, Allegretti M, Rantos V, Goetz SK, Obarska-Kosinska A, Zagoriy I, Halavatyi A, Hummer G, Mahamid J, Kosinski J, Beck M (2021). Nuclear pores dilate and constrict in cellulo. Science 374, eabd9776. PubMed
Zhu X, Huang G, Zeng C, Zhan X, Liang K, Xu Q, Zhao Y, Wang P, Wang Q, Zhou Q, et al. (2022). Structure of the cytoplasmic ring of the Xenopus laevis nuclear pore complex. Science 376, eabl8280. PubMed