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Near-atomic structure of jasplakinolide-stabilized malaria parasite F-actin reveals the structural basis of filament instability.

Pospich S, Kumpula EP, von der Ecken J, Vahokoski J, Kursula I, Raunser S
Proc Natl Acad Sci U S A 114 10636-10641 (2017)
Cited: 40 times
EuropePMC logo PMID: 28923924

Abstract

During their life cycle, apicomplexan parasites, such as the malaria parasite Plasmodium falciparum, use actomyosin-driven gliding motility to move and invade host cells. For this process, actin filament length and stability are temporally and spatially controlled. In contrast to canonical actin, P. falciparum actin 1 (PfAct1) does not readily polymerize into long, stable filaments. The structural basis of filament instability, which plays a pivotal role in host cell invasion, and thus infectivity, is poorly understood, largely because high-resolution structures of PfAct1 filaments were missing. Here, we report the near-atomic structure of jasplakinolide (JAS)-stabilized PfAct1 filaments determined by electron cryomicroscopy. The general filament architecture is similar to that of mammalian F-actin. The high resolution of the structure allowed us to identify small but important differences at inter- and intrastrand contact sites, explaining the inherent instability of apicomplexan actin filaments. JAS binds at regular intervals inside the filament to three adjacent actin subunits, reinforcing filament stability by hydrophobic interactions. Our study reveals the high-resolution structure of a small molecule bound to F-actin, highlighting the potential of electron cryomicroscopy for structure-based drug design. Furthermore, our work serves as a strong foundation for understanding the structural design and evolution of actin filaments and their function in motility and host cell invasion of apicomplexan parasites.

Articles - 5ogw mentioned but not cited (9)

  1. Near-atomic structure of jasplakinolide-stabilized malaria parasite F-actin reveals the structural basis of filament instability. Pospich S, Kumpula EP, von der Ecken J, Vahokoski J, Kursula I, Raunser S. Proc Natl Acad Sci U S A 114 10636-10641 (2017)
  2. Density modification of cryo-EM maps. Terwilliger TC, Sobolev OV, Afonine PV, Adams PD, Read RJ. Acta Crystallogr D Struct Biol 76 912-925 (2020)
  3. The actomyosin interface contains an evolutionary conserved core and an ancillary interface involved in specificity. Robert-Paganin J, Xu XP, Swift MF, Auguin D, Robblee JP, Lu H, Fagnant PM, Krementsova EB, Trybus KM, Houdusse A, Volkmann N, Hanein D. Nat Commun 12 1892 (2021)
  4. High-resolution structures of malaria parasite actomyosin and actin filaments. Vahokoski J, Calder LJ, Lopez AJ, Molloy JE, Kursula I, Rosenthal PB. PLoS Pathog 18 e1010408 (2022)
  5. Divergent Plasmodium actin residues are essential for filament localization, mosquito salivary gland invasion and malaria transmission. Yee M, Walther T, Frischknecht F, Douglas RG. PLoS Pathog 18 e1010779 (2022)
  6. Structure and function of Plasmodium actin II in the parasite mosquito stages. Lopez AJ, Andreadaki M, Vahokoski J, Deligianni E, Calder LJ, Camerini S, Freitag A, Bergmann U, Rosenthal PB, Sidén-Kiamos I, Kursula I. PLoS Pathog 19 e1011174 (2023)
  7. In silico approach to understand epigenetics of POTEE in ovarian cancer. Qazi S, Raza K. J Integr Bioinform 18 (2021)
  8. Sulfonylpiperazine compounds prevent Plasmodium falciparum invasion of red blood cells through interference with actin-1/profilin dynamics. Dans MG, Piirainen H, Nguyen W, Khurana S, Mehra S, Razook Z, Geoghegan ND, Dawson AT, Das S, Parkyn Schneider M, Jonsdottir TK, Gabriela M, Gancheva MR, Tonkin CJ, Mollard V, Goodman CD, McFadden GI, Wilson DW, Rogers KL, Barry AE, Crabb BS, de Koning-Ward TF, Sleebs BE, Kursula I, Gilson PR. PLoS Biol 21 e3002066 (2023)
  9. Structure and function of an atypical homodimeric actin capping protein from the malaria parasite. Bendes ÁÁ, Kursula P, Kursula I. Cell Mol Life Sci 79 125 (2022)


Reviews citing this publication (4)

  1. Towards a structural understanding of the remodeling of the actin cytoskeleton. Merino F, Pospich S, Raunser S. Semin Cell Dev Biol 102 51-64 (2020)
  2. Polymerization and depolymerization of actin with nucleotide states at filament ends. Fujiwara I, Takeda S, Oda T, Honda H, Narita A, Maéda Y. Biophys Rev 10 1513-1519 (2018)
  3. Electron cryomicroscopy as a powerful tool in biomedical research. Quentin D, Raunser S. J Mol Med (Berl) 96 483-493 (2018)
  4. Therapeutic Potential of Marine-Derived Cyclic Peptides as Antiparasitic Agents. Ribeiro R, Costa L, Pinto E, Sousa E, Fernandes C. Mar Drugs 21 609 (2023)

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  2. High-resolution cryo-EM structures of actin-bound myosin states reveal the mechanism of myosin force sensing. Mentes A, Huehn A, Liu X, Zwolak A, Dominguez R, Shuman H, Ostap EM, Sindelar CV. Proc Natl Acad Sci U S A 115 1292-1297 (2018)
  3. Structural insights into actin filament recognition by commonly used cellular actin markers. Kumari A, Kesarwani S, Javoor MG, Vinothkumar KR, Sirajuddin M. EMBO J 39 e104006 (2020)
  4. Structural basis of αE-catenin-F-actin catch bond behavior. Xu XP, Pokutta S, Torres M, Swift MF, Hanein D, Volkmann N, Weis WI. Elife 9 e60878 (2020)
  5. Structural basis of actin filament assembly and aging. Oosterheert W, Klink BU, Belyy A, Pospich S, Raunser S. Nature 611 374-379 (2022)
  6. Differential requirements for cyclase-associated protein (CAP) in actin-dependent processes of Toxoplasma gondii. Hunt A, Russell MRG, Wagener J, Kent R, Carmeille R, Peddie CJ, Collinson L, Heaslip A, Ward GE, Treeck M. Elife 8 e50598 (2019)
  7. In situ ultrastructures of two evolutionarily distant apicomplexan rhoptry secretion systems. Mageswaran SK, Guérin A, Theveny LM, Chen WD, Martinez M, Lebrun M, Striepen B, Chang YW. Nat Commun 12 4983 (2021)
  8. Optical Manipulation of F-Actin with Photoswitchable Small Molecules. Borowiak M, Küllmer F, Gegenfurtner F, Peil S, Nasufovic V, Zahler S, Thorn-Seshold O, Trauner D, Arndt HD. J Am Chem Soc 142 9240-9249 (2020)
  9. Actin stabilizing compounds show specific biological effects due to their binding mode. Wang S, Crevenna AH, Ugur I, Marion A, Antes I, Kazmaier U, Hoyer M, Lamb DC, Gegenfurtner F, Kliesmete Z, Ziegenhain C, Enard W, Vollmar A, Zahler S. Sci Rep 9 9731 (2019)
  10. Apicomplexan actin polymerization depends on nucleation. Kumpula EP, Pires I, Lasiwa D, Piirainen H, Bergmann U, Vahokoski J, Kursula I. Sci Rep 7 12137 (2017)
  11. High-resolution structures of the actomyosin-V complex in three nucleotide states provide insights into the force generation mechanism. Pospich S, Sweeney HL, Houdusse A, Raunser S. Elife 10 e73724 (2021)
  12. Inter-subunit interactions drive divergent dynamics in mammalian and Plasmodium actin filaments. Douglas RG, Nandekar P, Aktories JE, Kumar H, Weber R, Sattler JM, Singer M, Lepper S, Sadiq SK, Wade RC, Frischknecht F. PLoS Biol 16 e2005345 (2018)
  13. Conserved actin machinery drives microtubule-independent motility and phagocytosis in Naegleria. Velle KB, Fritz-Laylin LK. J Cell Biol 219 e202007158 (2020)
  14. Activation of Cofilin Increases Intestinal Permeability via Depolymerization of F-Actin During Hypoxia in vitro. Song H, Zhang J, He W, Wang P, Wang F. Front Physiol 10 1455 (2019)
  15. Unusual dynamics of the divergent malaria parasite PfAct1 actin filament. Lu H, Fagnant PM, Trybus KM. Proc Natl Acad Sci U S A 116 20418-20427 (2019)
  16. Cryo-EM Structure of Actin Filaments from Zea mays Pollen. Ren Z, Zhang Y, Zhang Y, He Y, Du P, Wang Z, Sun F, Ren H. Plant Cell 31 2855-2867 (2019)
  17. 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)
  18. Cryo-EM Resolves Molecular Recognition Of An Optojasp Photoswitch Bound To Actin Filaments In Both Switch States. Pospich S, Küllmer F, Nasufović V, Funk J, Belyy A, Bieling P, Arndt HD, Raunser S. Angew Chem Int Ed Engl 60 8678-8682 (2021)
  19. Origin and arrangement of actin filaments for gliding motility in apicomplexan parasites revealed by cryo-electron tomography. Martinez M, Mageswaran SK, Guérin A, Chen WD, Thompson CP, Chavin S, Soldati-Favre D, Striepen B, Chang YW. Nat Commun 14 4800 (2023)
  20. Structural basis of rapid actin dynamics in the evolutionarily divergent Leishmania parasite. Kotila T, Wioland H, Selvaraj M, Kogan K, Antenucci L, Jégou A, Huiskonen JT, Romet-Lemonne G, Lappalainen P. Nat Commun 13 3442 (2022)
  21. Ice thickness monitoring for cryo-EM grids by interferometry imaging. Hohle MM, Lammens K, Gut F, Wang B, Kahler S, Kugler K, Till M, Beckmann R, Hopfner KP, Jung C. Sci Rep 12 15330 (2022)
  22. Synthesis of the polyketide section of seragamide A and related cyclodepsipeptides via Negishi cross coupling. Lang JH, Lindel T. Beilstein J Org Chem 15 577-583 (2019)
  23. A new method for the construction of coarse-grained models of large biomolecules from low-resolution cryo-electron microscopy data. Zhang Y, Xia K, Cao Z, Gräter F, Xia F. Phys Chem Chem Phys 21 9720-9727 (2019)
  24. Total Synthesis and Bioactivity Mapping of Geodiamolide H. Nasufović V, Küllmer F, Bößneck J, Dahse HM, Görls H, Bellstedt P, Stallforth P, Arndt HD. Chemistry 27 11633-11642 (2021)
  25. Toxoplasma gondii actin filaments are tuned for rapid disassembly and turnover. Hvorecny KL, Sladewski TE, De La Cruz EM, Kollman JM, Heaslip AT. Nat Commun 15 1840 (2024)
  26. Cell softness renders cytotoxic T lymphocytes and T leukemic cells resistant to perforin-mediated killing. Zhou Y, Wang D, Zhou L, Zhou N, Wang Z, Chen J, Pang R, Fu H, Huang Q, Dong F, Cheng H, Zhang H, Tang K, Ma J, Lv J, Cheng T, Fiskesund R, Zhang X, Huang B. Nat Commun 15 1405 (2024)
  27. Comment Mightier Than Muscle: A Near-Atomic View of Pollen Actin Filaments. Farquharson KL. Plant Cell 31 2817-2818 (2019)


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