Phylogenetic reconstruction and evolution of the Rab GTPase gene family in Amoebozoa
Jazyk angličtina Země Spojené státy americké Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
33779495
PubMed Central
PMC9707542
DOI
10.1080/21541248.2021.1903794
Knihovny.cz E-zdroje
- Klíčová slova
- Phylogenomics, Rab therapeutic intervention, cellular biology, eukaryotic evolution,
- MeSH
- Amoebozoa * genetika metabolismus MeSH
- Eukaryota metabolismus MeSH
- fylogeneze MeSH
- molekulární evoluce MeSH
- Rab proteiny vázající GTP * genetika metabolismus MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- Rab proteiny vázající GTP * MeSH
Rab GTPase is a paralog-rich gene family that controls the maintenance of the eukaryotic cell compartmentalization system. Diverse eukaryotes have varying numbers of Rab paralogs. Currently, little is known about the evolutionary pattern of Rab GTPase in most major eukaryotic 'supergroups'. Here, we present a comprehensive phylogenetic reconstruction of the Rab GTPase gene family in the eukaryotic 'supergroup' Amoebozoa, a diverse lineage represented by unicellular and multicellular organisms. We demonstrate that Amoebozoa conserved 20 of the 23 ancestral Rab GTPases predicted to be present in the last eukaryotic common ancestor and massively expanded several 'novel' in-paralogs. Due to these 'novel' in-paralogs, the Rab family composition dramatically varies between the members of Amoebozoa; as a consequence, 'supergroup'-based studies may significantly change our current understanding of the evolution and diversity of this gene family. The high diversity of the Rab GTPase gene family in Amoebozoa makes this 'supergroup' a key lineage to study and advance our knowledge of the evolution of Rab in Eukaryotes.
Department of Biological Sciences Mississippi State University Starkville Mississippi USA
Department of Zoology Institute of Biosciences University of São Paulo São Paulo Brazil
Institute of Parasitology Biology Centre Czech Academy of Sciences České Budějovice Czech Republic
Zobrazit více v PubMed
Stenmark H, Olkkonen VM.. The rab gtpase family. Genome Biol. 2001;2(5):reviews3007–1. PubMed PMC
Zhen Y, Stenmark H.. Cellular functions of Rab GTPases at a glance. J Cell Sci. 2015;128(17):3171–3176. PubMed
Hutagalung AH, Novick PJ. Role of Rab GTPases in membrane traffic and cell physiology. Physiol Rev. 2011;91(1):119–149. PubMed PMC
Zerial M, McBride H. Rab proteins as membrane organizers. Nat Rev Mol Cell Biol. 2001;2(2):107–117. PubMed
Pfeffer S. A model for Rab GTPase localization. Biochem Soc Trans. 2005;33(4):627–630. PubMed
Colicelli J. Human RAS superfamily proteins and related GTPases. Science’s STKE. 2004;2004(250):re13–re13. PubMed PMC
Asaoka R, Uemura T, Ito J, et al. Arabidopsis RABA1 GTPases are involved in transport between the trans‐Golgi network and the plasma membrane, and are required for salinity stress tolerance. Plant J. 2013;73(2):240–249. PubMed
Gurkan C, Lapp H, Alory C, et al. Large-scale profiling of Rab GTPase trafficking networks: the membrome. Mol Biol Cell. 2005;16(8):3847–3864. PubMed PMC
Rutherford S, Moore I. The Arabidopsis Rab GTPase family: another enigma variation. Curr Opin Plant Biol. 2002;5(6):518–528. PubMed
Vernoud V, Horton AC, Yang Z, et al. Analysis of the small GTPase gene superfamily of Arabidopsis. Plant Physiol. 2003;131(3):1191–1208. PubMed PMC
Brighouse A, Dacks JB, Field MC. Rab protein evolution and the history of the eukaryotic endomembrane system. Cell Mol Life Sci. 2010;67(20):3449–3465. PubMed PMC
Pereira‐Leal JB. The Ypt/Rab family and the evolution of trafficking in fungi. Traffic. 2008;9(1):27–38. PubMed
Bright LJ, Kambesis N, Nelson SB, et al. Comprehensive analysis reveals dynamic and evolutionary plasticity of Rab GTPases and membrane traffic in Tetrahymena thermophila. PLoS Genet. 2010;6(10):e1001155. PubMed PMC
Eisen JA, Coyne RS, Wu M, et al. Macronuclear genome sequence of the ciliate Tetrahymena thermophila, a model eukaryote. PLoS Biol. 2006;4(9):e286. PubMed PMC
Ezougou CN, Ben-Rached F, Moss DK, et al. Plasmodium falciparum Rab5B is an N-terminally myristoylated Rab GTPase that is targeted to the parasite’s plasma and food vacuole membranes. PloS One. 2014;9(2):e87695. PubMed PMC
Quevillon E, Spielmann T, Brahimi K, et al. The Plasmodiumfalciparum family of Rab GTPases. Gene. 2003;306:13–25. PubMed
Langsley G, Van Noort V, Carret C, et al. Comparative genomics of the Rab protein family in Apicomplexan parasites. Microbes Infect. 2008;10(5):462–470. PubMed PMC
Ackers JP, Dhir V, Field MC. A bioinformatic analysis of the RAB genes of Trypanosoma brucei. Mol Biochem Parasitol. 2005;141(1):89–97. PubMed
Field MC. Signalling the genome: the Ras-like small GTPase family of trypanosomatids. Trends Parasitol. 2005;21(10):447–450. PubMed
Fritz-Laylin LK, Prochnik SE, Ginger ML, et al. The genome of Naegleria gruberi illuminates early eukaryotic versatility. Cell. 2010;140(5):631–642. PubMed
Carlton JM, Hirt RP, Silva JC, et al. Draft genome sequence of the sexually transmitted pathogen Trichomonas vaginalis. Science. 2007;315(5809):207–212. PubMed PMC
Lal K, Field MC, Carlton JM, et al. Identification of a very large Rab GTPase family in the parasitic protozoan Trichomonas vaginalis. Mol Biochem Parasitol. 2005;143(2):226–235. PubMed
Eliáš M, Brighouse A, Gabernet-Castello C, et al. Sculpting the endomembrane system in deep time: high resolution phylogenetics of Rab GTPases. J Cell Sci. 2012;125(10):2500–2508. PubMed PMC
Petrželková R, Eliáš M. Contrasting patterns in the evolution of the Rab GTPase family in Archaeplastida. Acta Societatis Botanicorum Poloniae. 2014;83:4.
Kang S, Tice AK, Spiegel FW, et al. Between a pod and a hard test: the deep evolution of amoebae. Mol Biol Evol. 2017;34(9):2258–2270. PubMed PMC
Nakada-Tsukui K, Saito-Nakano Y, Husain A, et al. Conservation and function of Rab small GTPases in Entamoeba: annotation of E. invadens Rab and its use for the understanding of Entamoeba biology. Exp Parasitol. 2010;126(3):337–347. PubMed
Lahr DJ, Kosakyan A, Lara E, et al. Phylogenomics and morphological reconstruction of Arcellinida testate amoebae highlight diversity of microbial eukaryotes in the Neoproterozoic. Curr Biol. 2019;29(6):991–1001. PubMed
Diekmann Y, Seixas E, Gouw M, et al. Thousands of rab GTPases for the cell biologist. PLoS Comput Biol. 2011;7(10):e1002217. PubMed PMC
Saito-Nakano Y, Loftus BJ, Hall N, et al. The diversity of Rab GTPases in Entamoeba histolytica. Exp Parasitol. 2005;110(3):244–252. PubMed
Wennerberg K, Rossman KL, Der CJ. The Ras superfamily at a glance. J Cell Sci. 2005;118(5):843–846. PubMed
Huet D, Blisnick T, Perrot S, et al. The GTPase IFT27 is involved in both anterograde and retrograde intraflagellar transport. Elife. 2014;3:e02419. PubMed PMC
Eguether T, San Agustin JT, Keady BT, et al. IFT27 links the BBSome to IFT for maintenance of the ciliary signaling compartment. Dev Cell. 2014;31(3):279–290. PubMed PMC
Kanie T, Abbott KL, Mooney NA, et al. The CEP19-RABL2 GTPase complex binds IFT-B to initiate intraflagellar transport at the ciliary base. Dev Cell. 2017;42(1):22–36. PubMed PMC
Lim YS, Tang BL. A role for Rab23 in the trafficking of Kif17 to the primary cilium. J Cell Sci. 2015;128(16):2996–3008. PubMed
Lo JC, Jamsai D, O’Connor AE, et al. (2012). RAB-like 2 has an essential role in male fertility, sperm intra-flagellar transport, and tail assembly. PubMed PMC
Lumb JH, Field MC. Rab23 is a flagellar protein in Trypanosoma brucei. BMC Res Notes. 2011;4(1):190. PubMed PMC
Qin H, Wang Z, Diener D, et al. Intraflagellar transport protein 27 is a small G protein involved in cell-cycle control. Curr Biol. 2007;17(3):193–202. PubMed PMC
Wang Y, Ng EL, Tang BL. Rab23: what exactly does it traffic? Traffic. 2006;7(6):746–750. PubMed
Yoshimura SI, Egerer J, Fuchs E, et al. Functional dissection of Rab GTPases involved in primary cilium formation. J Cell Biol. 2007;178(3):363–369. PubMed PMC
Hess S, Eme L, Roger AJ, et al. A natural toroidal microswimmer with a rotary eukaryotic flagellum. Nat Microbiol. 2019;4(10):1620–1626. PubMed
Fiore‐Donno AM, Tice AK, Brown MW. A non‐flagellated member of the myxogastria and expansion of the echinosteliida. J Eukaryotic Microbiol. 2019;66(4):538–544. PubMed
Reinhardt DJ, Olive LS. Echinosteliopsis, a new genus of the Mycetozoa. Mycologia. 1966;58(6):966–970.
Field MC, Carrington M. Intracellular membrane transport systems in Trypanosoma brucei. Traffic. 2004;5(12):905–913. PubMed
Field MC, Natesan SKA, Gabernet‐Castello C, et al. Intracellular trafficking in the trypanosomatids. Traffic. 2007;8(6):629–639. PubMed
Eichinger L, Pachebat JA, Glöckner G, et al. The genome of the social amoeba Dictyostelium discoideum. Nature. 2005;435(7038):43–57. PubMed PMC
Loftus B, Anderson I, Davies R, et al. The genome of the protist parasite Entamoeba histolytica. Nature. 2005;433(7028):865–868. PubMed
Lorenzi HA, Puiu D, Miller JR, et al. New assembly, reannotation and analysis of the Entamoeba histolytica genome reveal new genomic features and protein content information. PLoS Negl Trop Dis. 2010;4(6):e716. PubMed PMC
Žárský V, Klimeš V, Pačes J, et al. (2021). The Mastigamoeba balamuthi genome and the nature of the free-living ancestor of Entamoeba. Molecular biology and evolution, msab020. PubMed PMC
Mitra BN, Saito‐Nakano Y, Nakada‐Tsukui K, et al. Rab11B small GTPase regulates secretion of cysteine proteases in the enteric protozoan parasite Entamoeba histolytica. Cell Microbiol. 2007;9(9):2112–2125. PubMed
Verma K, Srivastava VK, Datta S. Rab GTPases take centre stage in understanding Entamoeba histolytica biology. Small GTPases. 2020;11(5):320–333. PubMed PMC
McGugan GC, Temesvari LA. Characterization of a Rab11-like GTPase, EhRab11, of entamoeba histolytica. Mol Biochem Parasitol. 2003;129(2):137–146. PubMed
Okada M, Nozaki T. New insights into molecular mechanisms of phagocytosis in Entamoeba histolytica by proteomic analysis. Arch Med Res. 2006;37(2):244–251. PubMed
Saito-Nakano Y, Yasuda T, Nakada-Tsukui K, et al. Rab5-associated vacuoles play a unique role in phagocytosis of the enteric protozoan parasite Entamoeba histolytica. J Biol Chem. 2004;279(47):49497–49507. PubMed
Rupper A, Grove B, Cardelli J. Rab7 regulates phagosome maturation in Dictyostelium. J Cell Sci. 2001;114(13):2449–2460. PubMed
Saito‐Nakano Y, Wahyuni R, Nakada‐Tsukui K, et al. Rab7D small GTPase is involved in phago‐, trogocytosis and cytoskeletal reorganization in the enteric protozoan Entamoeba histolytica. Cell Microbiol. 2021;23(1):e13267. PubMed PMC
Stein MP, Dong J, Wandinger-Ness A. Rab proteins and endocytic trafficking: potential targets for therapeutic intervention. Adv Drug Deliv Rev. 2003;55(11):1421–1437. PubMed
Seppey M, Manni M, Zdobnov EM. BUSCO: assessing genome assembly and annotation completeness. In: Gene prediction. Humana: New York, NY; 2019. p. 227–245. PubMed
Altschul SF, Madden TL, Schäffer AA, et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997;25(17):3389–3402. PubMed PMC
Surkont J, Diekmann Y, Pereira-Leal JB. Rabifier2: an improved bioinformatic classifier of Rab GTPases. Bioinformatics. 2017;33(4):568–570. PubMed
Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30(4):772–780. PubMed PMC
Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics. 2009;25(15):1972–1973. PubMed PMC
Kalyaanamoorthy S, Minh BQ, Wong TK, et al. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods. 2017;14(6):587–589. PubMed PMC
Hoang DT, Chernomor O, Von Haeseler A, et al. UFBoot2: improving the ultrafast bootstrap approximation. Mol Biol Evol. 2018;35(2):518–522. PubMed PMC
Nguyen LT, Schmidt HA, Von Haeseler A, et al. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol. 2015;32(1):268–274. PubMed PMC
Adl SM, Bass D, Lane CE, et al. Revisions to the classification, nomenclature, and diversity of eukaryotes. J Eukaryotic Microbiol. 2019;66(1):4–119. PubMed PMC
Schilde C, Lawal HM, Kin K, et al. A well supported multi gene phylogeny of 52 dictyostelia. Mol Phylogenet Evol. 2019;134:66–73. PubMed PMC
Cui Z, Li J, Chen Y, et al. Molecular epidemiology, evolution, and phylogeny of Entamoeba spp. Genetics and Evolution: Infection; 2019. p. 75, 104018. PubMed