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Modulation of actin structure and function by phosphorylation of Tyr-53 and profilin binding.

Baek K, Liu X, Ferron F, Shu S, Korn ED, Dominguez R
Proc Natl Acad Sci U S A 105 11748-53 (2008)
Related entries: 3ci5, 3cip

Cited: 41 times
EuropePMC logo PMID: 18689676

Abstract

On starvation, Dictyostelium cells aggregate to form multicellular fruiting bodies containing spores that germinate when transferred to nutrient-rich medium. This developmental cycle correlates with the extent of actin phosphorylation at Tyr-53 (pY53-actin), which is low in vegetative cells but high in viable mature spores. Here we describe high-resolution crystal structures of pY53-actin and unphosphorylated actin in complexes with gelsolin segment 1 and profilin. In the structure of pY53-actin, the phosphate group on Tyr-53 makes hydrogen-bonding interactions with residues of the DNase I-binding loop (D-loop) of actin, resulting in a more stable conformation of the D-loop than in the unphosphorylated structures. A more rigidly folded D-loop may explain some of the previously described properties of pY53-actin, including its increased critical concentration for polymerization, reduced rates of nucleation and pointed end elongation, and weak affinity for DNase I. We show here that phosphorylation of Tyr-53 inhibits subtilisin cleavage of the D-loop and reduces the rate of nucleotide exchange on actin. The structure of profilin-Dictyostelium-actin is strikingly similar to previously determined structures of profilin-beta-actin and profilin-alpha-actin. By comparing this representative set of profilin-actin structures with other structures of actin, we highlight the effects of profilin on the actin conformation. In the profilin-actin complexes, subdomains 1 and 3 of actin close around profilin, producing a 4.7 degrees rotation of the two major domains of actin relative to each other. As a result, the nucleotide cleft becomes moderately more open in the profilin-actin complex, probably explaining the stimulation of nucleotide exchange on actin by profilin.

Articles - 3chw mentioned but not cited (9)

  1. Modulation of actin structure and function by phosphorylation of Tyr-53 and profilin binding. Baek K, Liu X, Ferron F, Shu S, Korn ED, Dominguez R. Proc Natl Acad Sci U S A 105 11748-11753 (2008)
  2. Structural basis for the slow dynamics of the actin filament pointed end. Narita A, Oda T, Maéda Y. EMBO J 30 1230-1237 (2011)
  3. Structural, Functional, and Immunological Characterization of Profilin Panallergens Amb a 8, Art v 4, and Bet v 2. Offermann LR, Schlachter CR, Perdue ML, Majorek KA, He JZ, Booth WT, Garrett J, Kowal K, Chruszcz M. J Biol Chem 291 15447-15459 (2016)
  4. Structural basis for profilin-mediated actin nucleotide exchange. Porta JC, Borgstahl GE. J Mol Biol 418 103-116 (2012)
  5. G65V Substitution in Actin Disturbs Polymerization Leading to Inhibited Cell Elongation in Cotton. Sun Y, Liang W, Shen W, Feng H, Chen J, Si Z, Hu Y, Zhang T. Front Plant Sci 10 1486 (2019)
  6. Specialization of actin isoforms derived from the loss of key interactions with regulatory factors. Boiero Sanders M, Toret CP, Guillotin A, Antkowiak A, Vannier T, Robinson RC, Michelot A. EMBO J 41 e107982 (2022)
  7. Crystal structure of timothy grass allergen Phl p 12.0101 reveals an unusual profilin dimer. O'Malley A, Kapingidza AB, Hyduke N, Dolamore C, Kowal K, Chruszcz M. Acta Biochim Pol 68 15-22 (2021)
  8. In silico studies reveal structural deviations of mutant profilin-1 and interaction with riluzole and edaravone in amyotrophic lateral sclerosis. Sadr AS, Eslahchi C, Ghassempour A, Kiaei M. Sci Rep 11 6849 (2021)
  9. Visualizing the Bohr effect in hemoglobin: neutron structure of equine cyanomethemoglobin in the R state and comparison with human deoxyhemoglobin in the T state. Dajnowicz S, Seaver S, Hanson BL, Fisher SZ, Langan P, Kovalevsky AY, Mueser TC. Acta Crystallogr D Struct Biol 72 892-903 (2016)


Reviews citing this publication (7)

  1. Tropomodulins and Leiomodins: Actin Pointed End Caps and Nucleators in Muscles. Fowler VM, Dominguez R. Biophys J 112 1742-1760 (2017)
  2. Conformational dynamics of actin: effectors and implications for biological function. Hild G, Bugyi B, Nyitrai M. Cytoskeleton (Hoboken) 67 609-629 (2010)
  3. New waves in dendritic spine actin cytoskeleton: From branches and bundles to rings, from actin binding proteins to post-translational modifications. Bertling E, Hotulainen P. Mol Cell Neurosci 84 77-84 (2017)
  4. Posttranslational modifications of the cytoskeleton. MacTaggart B, Kashina A. Cytoskeleton (Hoboken) 78 142-173 (2021)
  5. From amino-acid to disease: the effects of oxidation on actin-myosin interactions in muscle. Elkrief D, Matusovsky O, Cheng YS, Rassier DE. J Muscle Res Cell Motil 44 225-254 (2023)
  6. Microcysts: the third developmental pathway of social amoebozoans. Budniak AA, O'Day DH. Protist 163 2-14 (2012)
  7. Targeting cytoskeletal phosphorylation in cancer. Llorente-González C, González-Rodríguez M, Vicente-Manzanares M. Explor Target Antitumor Ther 2 292-308 (2021)

Articles citing this publication (25)

  1. Proteomics of MUC1-containing lipid rafts from plasma membranes and exosomes of human breast carcinoma cells MCF-7. Staubach S, Razawi H, Hanisch FG. Proteomics 9 2820-2835 (2009)
  2. Structural basis for actin assembly, activation of ATP hydrolysis, and delayed phosphate release. Murakami K, Yasunaga T, Noguchi TQ, Gomibuchi Y, Ngo KX, Uyeda TQ, Wakabayashi T. Cell 143 275-287 (2010)
  3. Near-atomic resolution for one state of F-actin. Galkin VE, Orlova A, Vos MR, Schröder GF, Egelman EH. Structure 23 173-182 (2015)
  4. A novel interplay between oncogenic PFTK1 protein kinase and tumor suppressor TAGLN2 in the control of liver cancer cell motility. Leung WK, Ching AK, Chan AW, Poon TC, Mian H, Wong AS, To KF, Wong N. Oncogene 30 4464-4475 (2011)
  5. Structural basis of thymosin-β4/profilin exchange leading to actin filament polymerization. Xue B, Leyrat C, Grimes JM, Robinson RC. Proc Natl Acad Sci U S A 111 E4596-605 (2014)
  6. Structural differences explain diverse functions of Plasmodium actins. Vahokoski J, Bhargav SP, Desfosses A, Andreadaki M, Kumpula EP, Martinez SM, Ignatev A, Lepper S, Frischknecht F, Sidén-Kiamos I, Sachse C, Kursula I. PLoS Pathog 10 e1004091 (2014)
  7. Structure of a longitudinal actin dimer assembled by tandem w domains: implications for actin filament nucleation. Rebowski G, Namgoong S, Boczkowska M, Leavis PC, Navaza J, Dominguez R. J Mol Biol 403 11-23 (2010)
  8. ATP and ADP actin states. Kudryashov DS, Reisler E. Biopolymers 99 245-256 (2013)
  9. Actin Tyrosine-53-Phosphorylation in Neuronal Maturation and Synaptic Plasticity. Bertling E, Englund J, Minkeviciene R, Koskinen M, Segerstråle M, Castrén E, Taira T, Hotulainen P. J Neurosci 36 5299-5313 (2016)
  10. Expression of Y53A-actin in Dictyostelium disrupts the cytoskeleton and inhibits intracellular and intercellular chemotactic signaling. Shu S, Liu X, Kriebel PW, Hong MS, Daniels MP, Parent CA, Korn ED. J Biol Chem 285 27713-27725 (2010)
  11. Mutation of actin Tyr-53 alters the conformations of the DNase I-binding loop and the nucleotide-binding cleft. Liu X, Shu S, Hong MS, Yu B, Korn ED. J Biol Chem 285 9729-9739 (2010)
  12. The effects of ADF/cofilin and profilin on the conformation of the ATP-binding cleft of monomeric actin. Kardos R, Pozsonyi K, Nevalainen E, Lappalainen P, Nyitrai M, Hild G. Biophys J 96 2335-2343 (2009)
  13. Human congenital myopathy actin mutants cause myopathy and alter Z-disc structure in Drosophila flight muscle. Sevdali M, Kumar V, Peckham M, Sparrow J. Neuromuscul Disord 23 243-255 (2013)
  14. Oxidative hotspots on actin promote skeletal muscle weakness in rheumatoid arthritis. Steinz MM, Persson M, Aresh B, Olsson K, Cheng AJ, Ahlstrand E, Lilja M, Lundberg TR, Rullman E, Möller KÄ, Sandor K, Ajeganova S, Yamada T, Beard N, Karlsson BC, Tavi P, Kenne E, Svensson CI, Rassier DE, Karlsson R, Friedman R, Gustafsson T, Lanner JT. JCI Insight 5 126347 (2019)
  15. STK16 regulates actin dynamics to control Golgi organization and cell cycle. Liu J, Yang X, Li B, Wang J, Wang W, Liu J, Liu Q, Zhang X. Sci Rep 7 44607 (2017)
  16. 14-3-3 Regulates Actin Filament Formation in the Deep-Branching Eukaryote Giardia lamblia. Krtková J, Xu J, Lalle M, Steele-Ogus M, Alas GCM, Sept D, Paredez AR. mSphere 2 e00248-17 (2017)
  17. ANGUSTIFOLIA Regulates Actin Filament Alignment for Nuclear Positioning in Leaves. Iwabuchi K, Ohnishi H, Tamura K, Fukao Y, Furuya T, Hattori K, Tsukaya H, Hara-Nishimura I. Plant Physiol 179 233-247 (2019)
  18. Atomic view into Plasmodium actin polymerization, ATP hydrolysis, and fragmentation. Kumpula EP, Lopez AJ, Tajedin L, Han H, Kursula I. PLoS Biol 17 e3000315 (2019)
  19. Actin R256 Mono-methylation Is a Conserved Post-translational Modification Involved in Transcription. Kumar A, Zhong Y, Albrecht A, Sang PB, Maples A, Liu Z, Vinayachandran V, Reja R, Lee CF, Kumar A, Chen J, Xiao J, Park B, Shen J, Liu B, Person MD, Trybus KM, Zhang KYJ, Pugh BF, Kamm KE, Milewicz DM, Shen X, Kapoor P. Cell Rep 32 108172 (2020)
  20. Mutant profilin suppresses mutant actin-dependent mitochondrial phenotype in Saccharomyces cerevisiae. Wen KK, McKane M, Stokasimov E, Rubenstein PA. J Biol Chem 286 41745-41757 (2011)
  21. Subunit Rtt102 controls the conformation of the Arp7/9 heterodimer and its interactions with nucleotide and the catalytic subunit of SWI/SNF remodelers. Turegun B, Kast DJ, Dominguez R. J Biol Chem 288 35758-35768 (2013)
  22. The effect of ADF/cofilin and profilin on the dynamics of monomeric actin. Kardos R, Nevalainen E, Nyitrai M, Hild G. Biochim Biophys Acta 1834 2010-2019 (2013)
  23. Tyrosine phosphorylation of actin during microcyst formation and germination in Polysphondylium pallidum. Budniak A, O'Day DH. Protist 162 490-502 (2011)
  24. A Catalog of Proteins Expressed in the AG Secreted Fluid during the Mature Phase of the Chinese Mitten Crabs (Eriocheir sinensis). He L, Li Q, Liu L, Wang Y, Xie J, Yang H, Wang Q. PLoS One 10 e0136266 (2015)
  25. Molecular Dynamics Study of Citrullinated Proteins Associated with the Development of Rheumatoid Arthritis. Taldaev A, Rudnev V, Kulikova L, Nikolsky K, Efimov A, Malsagova K, Kaysheva A. Proteomes 10 8 (2022)


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