Regulation of the Actin Cytoskeleton via Rho GTPase Signalling in Dictyostelium and Mammalian Cells: A Parallel Slalom

Vedrana Filić; Lucija Mijanović; Darija Putar; Antea Talajić; Helena Ćetković; Igor Weber

doi:10.3390/cells10071592

journal article Open Access Jun 24, 2021

Regulation of the Actin Cytoskeleton via Rho GTPase Signalling in Dictyostelium and Mammalian Cells: A Parallel Slalom

Vedrana Filić Lucija Mijanović Darija Putar Antea Talajić Helena Ćetković

Igor Weber

Cells Vol. 10 No. 7 pp. 1592 · MDPI AG

View at Publisher Save 10.3390/cells10071592

Abstract

Both Dictyostelium amoebae and mammalian cells are endowed with an elaborate actin cytoskeleton that enables them to perform a multitude of tasks essential for survival. Although these organisms diverged more than a billion years ago, their cells share the capability of chemotactic migration, large-scale endocytosis, binary division effected by actomyosin contraction, and various types of adhesions to other cells and to the extracellular environment. The composition and dynamics of the transient actin-based structures that are engaged in these processes are also astonishingly similar in these evolutionary distant organisms. The question arises whether this remarkable resemblance in the cellular motility hardware is accompanied by a similar correspondence in matching software, the signalling networks that govern the assembly of the actin cytoskeleton. Small GTPases from the Rho family play pivotal roles in the control of the actin cytoskeleton dynamics. Indicatively, Dictyostelium matches mammals in the number of these proteins. We give an overview of the Rho signalling pathways that regulate the actin dynamics in Dictyostelium and compare them with similar signalling networks in mammals. We also provide a phylogeny of Rho GTPases in Amoebozoa, which shows a variability of the Rho inventories across different clades found also in Metazoa.

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References

365

[1]

Ridley "The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors" Cell (1992) 10.1016/0092-8674(92)90163-7

[2]

Ridley "The small GTP-binding protein rac regulates growth factor-induced membrane ruffling" Cell (1992) 10.1016/0092-8674(92)90164-8

[3]

Ridley "Historical Overview of Rho GTPases" Methods Mol. Biol. (2012) 10.1007/978-1-61779-442-1_1

[4]

Boureux "Evolution of the Rho Family of Ras-Like GTPases in Eukaryotes" Mol. Biol. Evol. (2007) 10.1093/molbev/msl145

[5]

Eme "On the Age of Eukaryotes: Evaluating Evidence from Fossils and Molecular Clocks" Cold Spring Harb. Perspect. Biol. (2014) 10.1101/cshperspect.a016139

[6]

Kang "Between a Pod and a Hard Test: The Deep Evolution of Amoebae" Mol. Biol. Evol. (2017) 10.1093/molbev/msx162

[7]

Artemenko "Moving towards a paradigm: Common mechanisms of chemotactic signaling in Dictyostelium and mammalian leukocytes" Cell. Mol. Life Sci. (2014) 10.1007/s00018-014-1638-8

[8]

Bozzaro "Phagocytosis and Host-Pathogen Interactions in Dictyostelium with a Look at Macrophages" Int. Rev. Cell Mol. Biol. (2008) 10.1016/s1937-6448(08)01206-9

[9]

Eat Prey, Live: Dictyostelium discoideum As a Model for Cell-Autonomous Defenses

Joe Dan Dunn, Cristina Bosmani, Caroline Barisch et al.

Frontiers in Immunology 2018 10.3389/fimmu.2017.01906

[10]

Dickinson "Studying Epithelial Morphogenesis in Dictyostelium" Methods Mol. Biol. (2015) 10.1007/978-1-4939-1164-6_18

[11]

Loomis "Genetic control of morphogenesis in Dictyostelium" Dev. Biol. (2015) 10.1016/j.ydbio.2015.03.016

[12]

Weijer "Dictyostelium morphogenesis" Curr. Opin. Genet. Dev. (2004) 10.1016/j.gde.2004.06.006

[13]

Alexandrova "Actin Cytoskeleton in Mesenchymal-to-Amoeboid Transition of Cancer Cells" Int. Rev. Cell Mol. Biol. (2020) 10.1016/bs.ircmb.2020.06.002

[14]

Macropinocytosis of protein is an amino acid supply route in Ras-transformed cells

Cosimo Commisso, Shawn M. Davidson, Rengin G. Soydaner-Azeloglu et al.

Nature 2013 10.1038/nature12138

[15]

King "The origins and evolution of macropinocytosis" Philos. Trans. R. Soc. B Biol. Sci. (2019) 10.1098/rstb.2018.0158

[16]

Palm "Nutrient acquisition strategies of mammalian cells" Nature (2017) 10.1038/nature22379

[17]

Stuelten "Cell motility in cancer invasion and metastasis: Insights from simple model organisms" Nat. Rev. Cancer (2018) 10.1038/nrc.2018.15

[18]

Williams "Function of small GTPases in Dictyostelium macropinocytosis" Philos. Trans. R. Soc. B Biol. Sci. (2019) 10.1098/rstb.2018.0150

[19]

Liu "Confinement and Low Adhesion Induce Fast Amoeboid Migration of Slow Mesenchymal Cells" Cell (2015) 10.1016/j.cell.2015.01.007

[20]

Mechanisms of 3D cell migration

Kenneth M. Yamada, Michael Sixt

Nature Reviews Molecular Cell Biology 2019 10.1038/s41580-019-0172-9

[21]

Miao "Altering the threshold of an excitable signal transduction network changes cell migratory modes" Nat. Cell Biol. (2017) 10.1038/ncb3495

[22]

Medalia "Organization of Actin Networks in Intact Filopodia" Curr. Biol. (2007) 10.1016/j.cub.2006.11.022

[23]

Schirenbeck "The Diaphanous-related formin dDia2 is required for the formation and maintenance of filopodia" Nat. Cell Biol. (2005) 10.1038/ncb1266

[24]

Zatulovskiy "Bleb-driven chemotaxis of Dictyostelium cells" J. Cell Biol. (2014) 10.1083/jcb.201306147

[25]

Weber "Is there a pilot in a pseudopod?" Eur. J. Cell Biol. (2006) 10.1016/j.ejcb.2006.05.002

[26]

Cardelli "Phagocytosis and Macropinocytosis in Dictyostelium: Phosphoinositide-Based Processes, Biochemically Distinct" Traffic (2001) 10.1034/j.1600-0854.2001.002005311.x

[27]

Rivero "Endocytosis and the Actin Cytoskeleton in Dictyostelium discoideum" Int. Rev. Cell Mol. Biol. (2008) 10.1016/s1937-6448(08)00633-3

[28]

Lee "The regulation of actin polymerization and cross-linking in Dictyostelium" Biochim. Biophys. Acta (BBA) Gen. Subj. (2001) 10.1016/s0304-4165(01)00107-6

[29]

Noegel "The actin cytoskeleton of Dictyostelium: A story told by mutants" J. Cell Sci. (2000) 10.1242/jcs.113.5.759

[30]

Rosenblum "The Molecular Basis of Phenotypic Convergence" Annu. Rev. Ecol. Evol. Syst. (2014) 10.1146/annurev-ecolsys-120213-091851

[31]

Speed "Quantification provides a conceptual basis for convergent evolution" Biol. Rev. (2016) 10.1111/brv.12257

[32]

Fort, P., and Blangy, A. (2018). Rho signaling: An historical and evolutionary perspective. Rho Signaling: Molecular Biology in Health and Disease, World Scientific. 10.1142/9789813228795_0001

[33]

Klimes "Rho GTPases: Deciphering the Evolutionary History of a Complex Protein Family" Methods Mol. Biol. (2012) 10.1007/978-1-61779-442-1_2

[34]

Beljan, S., Bosnar, M.H., and Ćetković, H. (2020). Rho Family of Ras-Like GTPases in Early-Branching Animals. Cells, 9. 10.3390/cells9102279

[35]

Vlahou "Rho GTPase signaling in Dictyostelium discoideum: Insights from the genome" Eur. J. Cell Biol. (2006) 10.1016/j.ejcb.2006.04.011

[36]

An Improved General Amino Acid Replacement Matrix

S. Q. Le, O. Gascuel

Molecular Biology and Evolution 2008 10.1093/molbev/msn067

[37]

MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms

Sudhir Kumar, Glen Stecher, Michael Li et al.

Molecular Biology and Evolution 2018 10.1093/molbev/msy096

[38]

Wennerberg "The Ras superfamily at a glance" J. Cell Sci. (2005) 10.1242/jcs.01660

[39]

The Guanine Nucleotide-Binding Switch in Three Dimensions

Ingrid R. Vetter, Alfred Wittinghofer

Science 2001 10.1126/science.1062023

[40]

Bourne "The GTPase superfamily: Conserved structure and molecular mechanism" Nature (1991) 10.1038/349117a0

[41]

Dever "GTP-binding domain: Three consensus sequence elements with distinct spacing" Proc. Natl. Acad. Sci. USA (1987) 10.1073/pnas.84.7.1814

[42]

Bos "GEFs and GAPs: Critical Elements in the Control of Small G Proteins" Cell (2007) 10.1016/j.cell.2007.05.018

[43]

Molecular Switch for Signal Transduction: Structural Differences Between Active and Inactive Forms of Protooncogenic ras Proteins

Michael V. Milburn, Liang Tong, Abraham M. deVos et al.

Science 1990 10.1126/science.2406906

[44]

"Fast-cycling Rho GTPases" Small GTPases (2020) 10.1080/21541248.2017.1391365

[45]

Colicelli "Human RAS Superfamily Proteins and Related GTPases" Sci. STKE (2004) 10.1126/stke.2502004re13

[46]

Ahmadian "Always look on the bright site of Rho: Structural implications for a conserved intermolecular interface" EMBO Rep. (2004) 10.1038/sj.embor.7400293

[47]

Schaefer "Toward understanding RhoGTPase specificity: Structure, function and local activation" Small GTPases (2014) 10.4161/21541248.2014.968004

[48]

Dovas "RhoGDI: Multiple functions in the regulation of Rho family GTPase activities" Biochem. J. (2005) 10.1042/bj20050104

[49]

Boulter "The ‘invisible hand’: Regulation of RHO GTPases by RHOGDIs" Nat. Rev. Mol. Cell Biol. (2011) 10.1038/nrm3153

[50]

Mott "Structures of Ras superfamily effector complexes: What have we learnt in two decades?" Crit. Rev. Biochem. Mol. Biol. (2015) 10.3109/10409238.2014.999191

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Published: Jun 24, 2021
Vol/Issue: 10(7)
Pages: 1592
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Vedrana Filić