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The myosin X motor is optimized for movement on actin bundles.

<div class='caption-title'>Myosin X dimerization region.</div>
<div class='caption-title'>Histogram and density plots of myosin X full length and HMM step-size data.</div>
<div class='caption-title'>Pre-powerstroke and rigor states of myosin X.</div>
Ropars V, Yang Z, Isabet T, Blanc F, Zhou K, Lin T, Liu X, Hissier P, Samazan F, Amigues B, Yang ED, Park H, Pylypenko O, Cecchini M, Sindelar CV, Sweeney HL, Houdusse A
OpenAccess logo Nat Commun 7 12456 (2016)
Related entries: 5hmo, 5hmp, 5i0h, 5i0i

Cited: 40 times
EuropePMC logo PMID: 27580874

Abstract

Myosin X has features not found in other myosins. Its structure must underlie its unique ability to generate filopodia, which are essential for neuritogenesis, wound healing, cancer metastasis and some pathogenic infections. By determining high-resolution structures of key components of this motor, and characterizing the in vitro behaviour of the native dimer, we identify the features that explain the myosin X dimer behaviour. Single-molecule studies demonstrate that a native myosin X dimer moves on actin bundles with higher velocities and takes larger steps than on single actin filaments. The largest steps on actin bundles are larger than previously reported for artificially dimerized myosin X constructs or any other myosin. Our model and kinetic data explain why these large steps and high velocities can only occur on bundled filaments. Thus, myosin X functions as an antiparallel dimer in cells with a unique geometry optimized for movement on actin bundles.

Articles - 5kg8 mentioned but not cited (3)

  1. The myosin X motor is optimized for movement on actin bundles. Ropars V, Yang Z, Isabet T, Blanc F, Zhou K, Lin T, Liu X, Hissier P, Samazan F, Amigues B, Yang ED, Park H, Pylypenko O, Cecchini M, Sindelar CV, Sweeney HL, Houdusse A. Nat Commun 7 12456 (2016)
  2. Structural basis of Fusarium myosin I inhibition by phenamacril. Zhou Y, Zhou XE, Gong Y, Zhu Y, Cao X, Brunzelle JS, Xu HE, Zhou M, Melcher K, Zhang F. PLoS Pathog 16 e1008323 (2020)
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Reviews citing this publication (9)

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  2. The many roles of myosins in filopodia, microvilli and stereocilia. Houdusse A, Titus MA. Curr Biol 31 R586-R602 (2021)
  3. Actin-Associated Proteins and Small Molecules Targeting the Actin Cytoskeleton. Gao J, Nakamura F. Int J Mol Sci 23 2118 (2022)
  4. Myosins in Osteoclast Formation and Function. Lee BS. Biomolecules 8 E157 (2018)
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  7. TGF-β1 signalling in Alzheimer's pathology and cytoskeletal reorganization: a specialized Tau perspective. Kapoor M, Chinnathambi S. J Neuroinflammation 20 72 (2023)
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  9. Toward physics-based precision medicine: Exploiting protein dynamics to design new therapeutics and interpret variants. Meller A, Kelly D, Smith LG, Bowman GR. Protein Sci 33 e4902 (2024)

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  3. Myosin-X knockout is semi-lethal and demonstrates that myosin-X functions in neural tube closure, pigmentation, hyaloid vasculature regression, and filopodia formation. Heimsath EG, Yim YI, Mustapha M, Hammer JA, Cheney RE. Sci Rep 7 17354 (2017)
  4. Drug specificity and affinity are encoded in the probability of cryptic pocket opening in myosin motor domains. Meller A, Lotthammer JM, Smith LG, Novak B, Lee LA, Kuhn CC, Greenberg L, Leinwand LA, Greenberg MJ, Bowman GR. Elife 12 e83602 (2023)
  5. Ca2+-Induced Rigidity Change of the Myosin VIIa IQ Motif-Single α Helix Lever Arm Extension. Li J, Li J, Chen Y, Deng Y, Unarta IC, Lu Q, Huang X, Zhang M. Structure 25 579-591.e4 (2017)
  6. A binding protein regulates myosin-7a dimerization and actin bundle assembly. Liu R, Billington N, Yang Y, Bond C, Hong A, Siththanandan V, Takagi Y, Sellers JR. Nat Commun 12 563 (2021)
  7. Kinetic adaptation of human Myo19 for active mitochondrial transport to growing filopodia tips. Ušaj M, Henn A. Sci Rep 7 11596 (2017)
  8. Full-length Plasmodium falciparum myosin A and essential light chain PfELC structures provide new anti-malarial targets. Moussaoui D, Robblee JP, Auguin D, Krementsova EB, Haase S, Blake TCA, Baum J, Robert-Paganin J, Trybus KM, Houdusse A. Elife 9 e60581 (2020)
  9. Kinetic signatures of myosin-5B, the motor involved in microvillus inclusion disease. Heissler SM, Chinthalapudi K, Sellers JR. J Biol Chem 292 18372-18385 (2017)
  10. The ATPase mechanism of myosin 15, the molecular motor mutated in DFNB3 human deafness. Jiang F, Takagi Y, Shams A, Heissler SM, Friedman TB, Sellers JR, Bird JE. J Biol Chem 296 100243 (2021)
  11. Activated full-length myosin-X moves processively on filopodia with large steps toward diverse two-dimensional directions. Sato O, Jung HS, Komatsu S, Tsukasaki Y, Watanabe TM, Homma K, Ikebe M. Sci Rep 7 44237 (2017)
  12. Optical control of fast and processive engineered myosins in vitro and in living cells. Ruijgrok PV, Ghosh RP, Zemsky S, Nakamura M, Gong R, Ning L, Chen R, Vachharajani VT, Chu AE, Anand N, Eguchi RR, Huang PS, Lin MZ, Alushin GM, Liphardt JT, Bryant Z. Nat Chem Biol 17 540-548 (2021)
  13. Optimized filopodia formation requires myosin tail domain cooperation. Arthur AL, Songster LD, Sirkia H, Bhattacharya A, Kikuti C, Borrega FP, Houdusse A, Titus MA. Proc Natl Acad Sci U S A 116 22196-22204 (2019)
  14. The Antiparallel Dimerization of Myosin X Imparts Bundle Selectivity for Processive Motility. Caporizzo MA, Fishman CE, Sato O, Jamiolkowski RM, Ikebe M, Goldman YE. Biophys J 114 1400-1410 (2018)
  15. Dynamic ion pair behavior stabilizes single α-helices in proteins. Batchelor M, Wolny M, Baker EG, Paci E, Kalverda AP, Peckham M. J Biol Chem 294 3219-3234 (2019)
  16. Molecular assemblies built with the artificial protein Pizza. Vrancken JPM, Aupič J, Addy C, Jerala R, Tame JRH, Voet ARD. J Struct Biol X 4 100027 (2020)
  17. Filopodia powered by class x myosin promote fusion of mammalian myoblasts. Hammers DW, Hart CC, Matheny MK, Heimsath EG, Lee YI, Hammer JA, Cheney RE, Sweeney HL. Elife 10 e72419 (2021)
  18. Protrusion growth driven by myosin-generated force. Fitz GN, Weck ML, Bodnya C, Perkins OL, Tyska MJ. Dev Cell 58 18-33.e6 (2023)
  19. Chiral growth of adherent filopodia. Li W, Chung WL, Kozlov MM, Medalia O, Geiger B, Bershadsky AD. Biophys J 122 3704-3721 (2023)
  20. Mllt11 Regulates Migration and Neurite Outgrowth of Cortical Projection Neurons during Development. Stanton-Turcotte D, Hsu K, Moore SA, Yamada M, Fawcett JP, Iulianella A. J Neurosci 42 3931-3948 (2022)
  21. VASP-mediated actin dynamics activate and recruit a filopodia myosin. Arthur AL, Crawford A, Houdusse A, Titus MA. Elife 10 e68082 (2021)
  22. A peptide interfering with the dimerization of oncogenic KITENIN protein and its stability suppresses colorectal tumour progression. Kim SJ, Sun EG, Bae JA, Park S, Hong CS, Park ZY, Kim H, Kim KK. Clin Transl Med 12 e871 (2022)
  23. Simultaneous tracking of two motor domains reveals near simultaneous steps and stutter steps of myosin 10 on actin filament bundles. Qin X, Yoo H, Man Cheng HC, Nguyen QQ, Li J, Liu X, Prunetti L, Chen X, Liu T, Sweeney HL, Park H. Biochem Biophys Res Commun S0006-291X(20)30305-3 (2020)
  24. Comparative analysis of the MyTH4-FERM myosins reveals insights into the determinants of actin track selection in polarized epithelia. Matoo S, Graves MJ, Acharya P, Choi MS, Storad ZA, Idris RAES, Pickles BK, Arvay TO, Shinder PE, Gerts A, Papish JP, Crawley SW. Mol Biol Cell 32 ar30 (2021)
  25. The Antiparallel Coiled-Coil Domain Allows Multiple Forward Step Sizes of Myosin X. Nguyen QQ, Zhou Y, Cheng MS, Qin X, Cheng HCM, Liu X, Sweeney HL, Park H. J Phys Chem Lett 14 4914-4922 (2023)
  26. How myosin VI traps its off-state, is activated and dimerizes. Canon L, Kikuti C, Planelles-Herrero VJ, Lin T, Mayeux F, Sirkia H, Lee YI, Heidsieck L, Velikovsky L, David A, Liu X, Moussaoui D, Forest E, Höök P, Petersen KJ, Morgan TE, Di Cicco A, Sirés-Campos J, Derivery E, Lévy D, Delevoye C, Sweeney HL, Houdusse A. Nat Commun 14 6732 (2023)
  27. Lysyl hydroxylase 2 deficiency promotes filopodia formation and fibroblast migration. Nozaki R, Kasamatsu A, Moss J, Uzawa K. Biochem Biophys Res Commun 587 146-152 (2022)
  28. Myo10 tail is crucial for promoting long filopodia. Chen X, Arciola JM, Lee YI, Wong PHP, Yin H, Tao Q, Jin Y, Qin X, Sweeney HL, Park H. J Biol Chem 300 105523 (2024)


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