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Crystal structure of human myosin 1c--the motor in GLUT4 exocytosis: implications for Ca2+ regulation and 14-3-3 binding.

Münnich S, Taft MH, Manstein DJ
J Mol Biol 426 2070-81 (2014)
Cited: 42 times
EuropePMC logo PMID: 24636949

Abstract

Myosin 1c (Myo1c) plays a key role in supporting motile events that underlie cell migration, vesicle trafficking, insulin-stimulated glucose uptake and hearing. Here, we present the crystal structure of the human Myo1c motor in complex with its light chain calmodulin. Our structure reveals tight interactions of the motor domain with calmodulin bound to the first IQ motif in the neck region. Several of the calmodulin residues contributing to this interaction are also involved in Ca(2+) binding. Contact residues in the motor domain are linked to the central β-sheet and the HO helix, suggesting a mechanism for communicating changes in Ca(2+) binding in the neck region to the actin and nucleotide binding regions of the motor domain. The structural context and the chemical environment of Myo1c mutations that are involved in sensorineural hearing loss in humans are described and their impact on motor function is discussed. We show that a construct consisting of the motor domain of Myo1c and the first IQ motif is sufficient to establish a tight interaction with 14-3-3β (KD=0.9 μM) and present the model of a double-headed Myo1c-14-3-3 complex. This complex has been implicated in the exocytosis of glucose transporter 4 storage vesicles during insulin-stimulated glucose uptake.

Reviews - 4byf mentioned but not cited (1)

  1. Kinetic Adaptations of Myosins for Their Diverse Cellular Functions. Heissler SM, Sellers JR. Traffic 17 839-859 (2016)

Articles - 4byf mentioned but not cited (13)

  1. Force-producing ADP state of myosin bound to actin. Wulf SF, Ropars V, Fujita-Becker S, Oster M, Hofhaus G, Trabuco LG, Pylypenko O, Sweeney HL, Houdusse AM, Schröder RR. Proc Natl Acad Sci U S A 113 E1844-52 (2016)
  2. Conformational heterogeneity of the calmodulin binding interface. Shukla D, Peck A, Pande VS. Nat Commun 7 10910 (2016)
  3. Catalytic strategy used by the myosin motor to hydrolyze ATP. Kiani FA, Fischer S. Proc Natl Acad Sci U S A 111 E2947-56 (2014)
  4. Structural and mechanistic insights into the function of the unconventional class XIV myosin MyoA from Toxoplasma gondii. Powell CJ, Ramaswamy R, Kelsen A, Hamelin DJ, Warshaw DM, Bosch J, Burke JE, Ward GE, Boulanger MJ. Proc Natl Acad Sci U S A 115 E10548-E10555 (2018)
  5. N-terminal splicing extensions of the human MYO1C gene fine-tune the kinetics of the three full-length myosin IC isoforms. Zattelman L, Regev R, Ušaj M, Reinke PYA, Giese S, Samson AO, Taft MH, Manstein DJ, Henn A. J Biol Chem 292 17804-17818 (2017)
  6. Structural Analysis of the Myo1c and Neph1 Complex Provides Insight into the Intracellular Movement of Neph1. Arif E, Sharma P, Solanki A, Mallik L, Rathore YS, Twal WO, Nath SK, Gandhi D, Holzman LB, Ostap EM, Ashish, Nihalani D. Mol Cell Biol 36 1639-1654 (2016)
  7. 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)
  8. Structure of the Single-lobe Myosin Light Chain C in Complex with the Light Chain-binding Domains of Myosin-1C Provides Insights into Divergent IQ Motif Recognition. Langelaan DN, Liburd J, Yang Y, Miller E, Chitayat S, Crawley SW, Côté GP, Smith SP. J Biol Chem 291 19607-19617 (2016)
  9. The regulatory protein 14-3-3β binds to the IQ motifs of myosin-IC independent of phosphorylation. Ji HH, Ostap EM. J Biol Chem 295 3749-3756 (2020)
  10. Alternative N-terminal regions of Drosophila myosin heavy chain II regulate communication of the purine binding loop with the essential light chain. Bloemink MJ, Hsu KH, Geeves MA, Bernstein SI. J Biol Chem 295 14522-14535 (2020)
  11. The role of motor proteins in photoreceptor protein transport and visual function. Radhakrishnan R, Dronamraju VR, Leung M, Gruesen A, Solanki AK, Walterhouse S, Roehrich H, Song G, da Costa Monsanto R, Cureoglu S, Martin R, Kondkar AA, van Kuijk FJ, Montezuma SR, Knöelker HJ, Hufnagel RB, Lobo GP. Ophthalmic Genet 43 285-300 (2022)
  12. Mechanochemical properties of human myosin-1C are modulated by isoform-specific differences in the N-terminal extension. Giese S, Reindl T, Reinke PYA, Zattelman L, Fedorov R, Henn A, Taft MH, Manstein DJ. J Biol Chem 296 100128 (2021)
  13. Physiologically Relevant Free Ca2+ Ion Concentrations Regulate STRA6-Calmodulin Complex Formation via the BP2 Region of STRA6. Young BD, Varney KM, Wilder PT, Costabile BK, Pozharski E, Cook ME, Godoy-Ruiz R, Clarke OB, Mancia F, Weber DJ. J Mol Biol 433 167272 (2021)


Reviews citing this publication (9)

  1. Myosin light chains: Teaching old dogs new tricks. Heissler SM, Sellers JR. Bioarchitecture 4 169-188 (2014)
  2. The ever changing moods of calmodulin: how structural plasticity entails transductional adaptability. Villarroel A, Taglialatela M, Bernardo-Seisdedos G, Alaimo A, Agirre J, Alberdi A, Gomis-Perez C, Soldovieri MV, Ambrosino P, Malo C, Areso P. J Mol Biol 426 2717-2735 (2014)
  3. The many structural faces of calmodulin: a multitasking molecular jackknife. Kursula P. Amino Acids 46 2295-2304 (2014)
  4. The Role of Calmodulin in Tumor Cell Migration, Invasiveness, and Metastasis. Villalobo A, Berchtold MW. Int J Mol Sci 21 E765 (2020)
  5. Unconventional Myosins: How Regulation Meets Function. Fili N, Toseland CP. Int J Mol Sci 21 E67 (2019)
  6. Structural Basis of Cargo Recognition by Unconventional Myosins in Cellular Trafficking. Li J, Li J, Lu Q, Zhang M. Traffic 17 822-838 (2016)
  7. Mechanics and Activation of Unconventional Myosins. Batters C, Veigel C. Traffic 17 860-871 (2016)
  8. ATP Analogues for Structural Investigations: Case Studies of a DnaB Helicase and an ABC Transporter. Lacabanne D, Wiegand T, Wili N, Kozlova MI, Cadalbert R, Klose D, Mulkidjanian AY, Meier BH, Böckmann A. Molecules 25 E5268 (2020)
  9. Does the Actin Network Architecture Leverage Myosin-I Functions? Pernier J, Schauer K. Biology (Basel) 11 989 (2022)

Articles citing this publication (19)

  1. Comprehensive identification of RNA-protein interactions in any organism using orthogonal organic phase separation (OOPS). Queiroz RML, Smith T, Villanueva E, Marti-Solano M, Monti M, Pizzinga M, Mirea DM, Ramakrishna M, Harvey RF, Dezi V, Thomas GH, Willis AE, Lilley KS. Nat Biotechnol 37 169-178 (2019)
  2. How actin initiates the motor activity of Myosin. Llinas P, Isabet T, Song L, Ropars V, Zong B, Benisty H, Sirigu S, Morris C, Kikuti C, Safer D, Sweeney HL, Houdusse A. Dev Cell 33 401-412 (2015)
  3. 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)
  4. Loss of functional MYO1C/myosin 1c, a motor protein involved in lipid raft trafficking, disrupts autophagosome-lysosome fusion. Brandstaetter H, Kishi-Itakura C, Tumbarello DA, Manstein DJ, Buss F. Autophagy 10 2310-2323 (2014)
  5. Structure of myosin-1c tail bound to calmodulin provides insights into calcium-mediated conformational coupling. Lu Q, Li J, Li J, Ye F, Zhang M. Nat Struct Mol Biol 22 81-88 (2015)
  6. 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)
  7. Mechanochemical tuning of myosin-I by the N-terminal region. Greenberg MJ, Lin T, Shuman H, Ostap EM. Proc Natl Acad Sci U S A 112 E3337-44 (2015)
  8. Multiscale modelling of relationships between protein classes and drug behavior across all diseases using the CANDO platform. Sethi G, Chopra G, Samudrala R. Mini Rev Med Chem 15 705-717 (2015)
  9. Lowered Expression of Tumor Suppressor Candidate MYO1C Stimulates Cell Proliferation, Suppresses Cell Adhesion and Activates AKT. Visuttijai K, Pettersson J, Mehrbani Azar Y, van den Bout I, Örndal C, Marcickiewicz J, Nilsson S, Hörnquist M, Olsson B, Ejeskär K, Behboudi A. PLoS One 11 e0164063 (2016)
  10. Crystal structure of the rigor-like human non-muscle myosin-2 motor domain. Münnich S, Pathan-Chhatbar S, Manstein DJ. FEBS Lett 588 4754-4760 (2014)
  11. 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)
  12. Myosin-1C uses a novel phosphoinositide-dependent pathway for nuclear localization. Nevzorov I, Sidorenko E, Wang W, Zhao H, Vartiainen MK. EMBO Rep 19 290-304 (2018)
  13. Mutations in MYO1H cause a recessive form of central hypoventilation with autonomic dysfunction. Spielmann M, Hernandez-Miranda LR, Ceccherini I, Weese-Mayer DE, Kragesteen BK, Harabula I, Krawitz P, Birchmeier C, Leonard N, Mundlos S. J Med Genet 54 754-761 (2017)
  14. Calcium-regulated import of myosin IC into the nucleus. Maly IV, Hofmann WA. Cytoskeleton (Hoboken) 73 341-350 (2016)
  15. Phenamacril is a reversible and noncompetitive inhibitor of Fusarium class I myosin. Wollenberg RD, Taft MH, Giese S, Thiel C, Balázs Z, Giese H, Manstein DJ, Sondergaard TE. J Biol Chem 294 1328-1337 (2019)
  16. NYX-2925 induces metabotropic N-methyl-d-aspartate receptor (NMDAR) signaling that enhances synaptic NMDAR and α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor. Bowers MS, Cacheaux LP, Sahu SU, Schmidt ME, Sennello JA, Leaderbrand K, Khan MA, Kroes RA, Moskal JR. J Neurochem 152 523-541 (2020)
  17. Distinct actin-tropomyosin cofilament populations drive the functional diversification of cytoskeletal myosin motor complexes. Reindl T, Giese S, Greve JN, Reinke PY, Chizhov I, Latham SL, Mulvihill DP, Taft MH, Manstein DJ. iScience 25 104484 (2022)
  18. Putting the brakes on a myosin motor. Eddington C, Titus MA. J Biol Chem 295 3757-3758 (2020)
  19. Redox regulation of KV7 channels through EF3 hand of calmodulin. Nuñez E, Jones F, Muguruza-Montero A, Urrutia J, Aguado A, Malo C, Bernardo-Seisdedos G, Domene C, Millet O, Gamper N, Villarroel A. Elife 12 e81961 (2023)


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