Molecular characterization and subcellular localization of arabidopsis class viii myosin, ATM1

Journal of Biological Chemistry

Volumn 289, Issue 18, 2014, Pages 12343-12355

  Haraguchi, Takeshi ^a   Tominaga, Motoki ^b,c   Matsumoto, Rie ^a   Sato, Kei ^d   Nakano, Akihiko ^d   Yamamoto, Keiichi ^a   Ito, Kohji ^a  

^a CHIBA UNIVERSITY   (Japan)

^b Institute of Physical and Chemical Research   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^d UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; BIOLOGY;

ARABIDOPSIS; ENZYMATIC ACTIVITIES; HIGH AFFINITY; MOLECULAR CHARACTERIZATION; MOLECULAR PROPERTIES; SUBCELLULAR LOCALIZATIONS;

PROTEINS;

ACTIN; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATASE (MAGNESIUM); ARABIDOPSIS PROTEIN; MAGNESIUM; MYOSIN; MYOSIN VIII; PROTEIN ATM1; UNCLASSIFIED DRUG;

ARABIDOPSIS; ARTICLE; BACULOVIRUS EXPRESSION SYSTEM; BINDING AFFINITY; CELL STRUCTURE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; GENETIC REGULATION; MOLECULAR BIOLOGY; NONHUMAN; PLASMODESMA; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION;

ACTIN; ARABIDOPSIS; ATPASES; KINETICS; MOLECULAR MOTORS; MYOSIN;

ACTIN CYTOSKELETON; ACTINS; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; DINITROBENZENES; GREEN FLUORESCENT PROTEINS; KINETICS; MICROSCOPY, CONFOCAL; MYOSINS; PLANTS, GENETICALLY MODIFIED; PROTEIN BINDING; PROTOPLASTS; SULFANILAMIDES; TUBULIN MODULATORS;

EID: 84899727649     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.521716     Document Type: Article

References (92)

1. Odronitz, F., and Kollmar, M. (2007) Drawing the tree of eukaryotic life based on the analysis of 2,269 manually annotated myosins from 328 species. Genome Biol. 8, R196
2. Reddy, A. S., and Day, I. S. (2001) Analysis of the myosins encoded in the recently completed Arabidopsis thaliana genome sequence. Genome Biol. 2, RESEARCH0024
3. Tominaga, M., Kimura, A., Yokota, E., Haraguchi, T., Shimmen, T., Yamamoto, K., Nakano, A., and Ito, K. (2013) Cytoplasmic streaming velocity as a plant size determinant. Dev. Cell 27, 345-352
4. Avisar, D., Prokhnevsky, A. I., Makarova, K. S., Koonin, E. V., and Dolja, V. V. (2008) Myosin XI-K is required for rapid trafficking of Golgi stacks, peroxisomes, and mitochondria in leaf cells of Nicotiana benthamiana. Plant Physiol. 146, 1098-1108
5. Hashimoto, K., Igarashi, H., Mano, S., Nishimura, M., Shimmen, T., and Yokota, E. (2005) Peroxisomal localization of a myosin XI isoform in Arabidopsis thaliana. Plant Cell Physiol. 46, 782-789
6. Li, J. F., and Nebenführ, A. (2007) Organelle targeting of myosin XI is mediated by two globular tail subdomains with separate cargo binding sites. J. Biol. Chem. 282, 20593-20602
7. Reisen, D., and Hanson, M. R. (2007) Association of six YFP-myosin XItail fusions with mobile plant cell organelles. BMC Plant Biol. 7, 6
8. Avisar, D., Abu-Abied, M., Belausov, E., Sadot, E., Hawes, C., and Sparkes, I. A. (2009) A comparative study of the involvement of 17 Arabidopsis myosin family members on the motility of Golgi and other organelles. Plant Physiol. 150, 700-709
9. Peremyslov, V. V., Mockler, T. C., Filichkin, S. A., Fox, S. E., Jaiswal, P., Makarova, K. S., Koonin, E. V., and Dolja, V. V. (2011) Expression, splicing, and evolution of the myosin gene family in plants. Plant Physiol. 155, 1191-1204
10. Prokhnevsky, A. I., Peremyslov, V. V., and Dolja, V. V. (2008) Overlapping functions of the four class XI myosins in Arabidopsis growth, root hair elongation, and organelle motility. Proc. Natl. Acad. Sci. U.S.A. 105, 19744-19749
11. Sparkes, I. (2011) Recent advances in understanding plant myosin function: life in the fast lane. Mol. Plant 4, 805-812
12. Ueda, H., Yokota, E., Kutsuna, N., Shimada, T., Tamura, K., Shimmen, T., Hasezawa, S., Dolja, V. V., and Hara-Nishimura, I. (2010) Myosin-dependent endoplasmic reticulum motility and F-actin organization in plant cells. Proc. Natl. Acad. Sci. U.S.A. 107, 6894-6899
13. Ojangu, E. L., Järve, K., Paves, H., and Truve, E. (2007) Arabidopsis thaliana myosin XIK is involved in root hair as well as trichome morphogenesis on stems and leaves. Protoplasma 230, 193-202
14. Yokota, E., and Shimmen, T. (1994) Isolation and characterization of plant myosin from pollen tubes of lily. Protoplasma 177, 153-162
15. Tominaga, M., Kojima, H., Yokota, E., Orii, H., Nakamori, R., Katayama, E., Anson, M., Shimmen, T., and Oiwa, K. (2003) Higher plant myosin XI moves processively on actin with 35nmsteps at high velocity.EMBOJ. 22, 1263-1272
16. Yamamoto, K., Kikuyama, M., Sutoh-Yamamoto, N., and Kamitsubo, E. (1994) Purification of actin based motor protein from Chara corallina. Proc. Jpn. Acad. 70, 175-180
17. Hachikubo, Y., Ito, K., Schiefelbein, J., Manstein, D. J., and Yamamoto, K. (2007) Enzymatic activity and motility of recombinant Arabidopsis myosin XI, MYA1. Plant Cell Physiol. 48, 886-891
18. Ito, K., Kashiyama, T., Shimada, K., Yamaguchi, A., Awata Jy, Hachikubo, Y., Manstein, D. J., and Yamamoto, K. (2003) Recombinant motor domain constructs of Chara corallina myosin display fast motility and high ATPase activity. Biochem. Biophys. Res. Commun. 312, 958-964
19. Ito, K., Ikebe, M., Kashiyama, T., Mogami, T., Kon, T., and Yamamoto, K. (2007) Kinetic mechanism of the fastest motor protein, Chara myosin. J. Biol. Chem. 282, 19534-19545
20. Ito, K., Yamaguchi, Y., Yanase, K., Ichikawa, Y., and Yamamoto, K. (2009) Unique charge distribution in surface loops confers high velocity on the fast motor protein Chara myosin. Proc. Natl. Acad. Sci. U.S.A. 106, 21585-21590
21. Knight, A. E., and Kendrick-Jones, J. (1993) A myosin-like protein from a higher plant. J. Mol. Biol. 231, 148-154
22. Reichelt, S., Knight, A. E., Hodge, T. P., Baluska, F., Samaj, J., Volkmann, D., and Kendrick-Jones, J. (1999) Characterization of the unconventional myosin VIII in plant cells and its localization at the post-cytokinetic cell wall. Plant J. 19, 555-567
23. Golomb, L., Abu-Abied, M., Belausov, E., and Sadot, E. (2008) Different subcellular localizations and functions of Arabidopsis myosin VIII. BMC Plant Biol. 8, 3
24. Seki, M., Carninci, P., Nishiyama, Y., Hayashizaki, Y., and Shinozaki, K. (1998) High-efficiency cloning of Arabidopsis full-length cDNA by biotinylated CAP trapper. Plant J. 15, 707-720
25. Seki, M., Narusaka, M., Kamiya, A., Ishida, J., Satou, M., Sakurai, T., Nakajima, M., Enju, A., Akiyama, K., Oono, Y., Muramatsu, M., Hayashizaki, Y., Kawai, J., Carninci, P., Itoh, M., Ishii, Y., Arakawa, T., Shibata, K., Shinagawa, A., and Shinozaki, K. (2002) Functional annotation of a fulllength Arabidopsis cDNA collection. Science 296, 141-145
26. Geeves, M. A., Perreault-Micale, C., and Coluccio, L. M. (2000) Kinetic analyses of a truncated mammalian myosin I suggest a novel isomerization event preceding nucleotide binding. J. Biol. Chem. 275, 21624-21630
27. El Mezgueldi, M., Tang, N., Rosenfeld, S. S., and Ostap, E. M. (2002) The kinetic mechanism of Myo1e (human myosin-IC). J. Biol. Chem. 277, 21514-21521
28. De La Cruz, E. M., Wells, A. L., Rosenfeld, S. S., Ostap, E. M., and Sweeney, H. L. (1999) The kinetic mechanism of myosin V. Proc. Natl. Acad. Sci. U.S.A. 96, 13726-13731
29. Dosé, A. C., Ananthanarayanan, S., Moore, J. E., Burnside, B., and Yengo, C. M. (2007) Kinetic mechanism of human myosin IIIA. J. Biol. Chem. 282, 216-231
30. 2+-dependent regulation of the motor activity of myosin V. J. Biol. Chem. 275, 34766-34771
31. Wang, F., Chen, L., Arcucci, O., Harvey, E. V., Bowers, B., Xu, Y., Hammer, J. A., 3rd, and Sellers, J. R. (2000) Effect of ADP and ionic strength on the kinetic and motile properties of recombinant mouse myosin V. J. Biol. Chem. 275, 4329-4335
32. Trybus, K. M., Krementsova, E., and Freyzon, Y. (1999) Kinetic characterization of a monomeric unconventional myosinVconstruct. J. Biol. Chem. 274, 27448-27456
33. De La Cruz, E. M., Ostap, E. M., and Sweeney, H. L. (2001) Kinetic mechanism and regulation of myosin VI. J. Biol. Chem. 276, 32373-32381
34. Yang, Y., Kovács, M., Xu, Q., Anderson, J. B., and Sellers, J. R. (2005) Myosin VIIB from Drosophila is a high duty ratio motor. J. Biol. Chem. 280, 32061-32068
35. Henn, A., and De La Cruz, E. M. (2005) Vertebrate myosin VIIb is a high duty ratio motor adapted for generating and maintaining tension. J. Biol. Chem. 280, 39665-39676
36. Homma, K., and Ikebe, M. (2005) Myosin x is a high duty ratio motor. J. Biol. Chem. 280, 29381-29391
37. Kovács, M., Wang, F., and Sellers, J. R. (2005) Mechanism of action of myosin X, a membrane-associated molecular motor. J. Biol. Chem. 280, 15071-15083
38. Inoue, A., Saito, J., Ikebe, R., and Ikebe, M. (2002) Myosin IXb is a singleheaded minus-end-directed processive motor. Nat. Cell Biol. 4, 302-306
39. Haithcock, J., Billington, N., Choi, K., Fordham, J., Sellers, J. R., Stafford, W. F., White, H., and Forgacs, E. (2011) The kinetic mechanism of mouse myosin VIIA. J. Biol. Chem. 286, 8819-8828
40. Nakagawa, T., Suzuki, T., Murata, S., Nakamura, S., Hino, T., Maeo, K., Tabata, R., Kawai, T., Tanaka, K., Niwa, Y., Watanabe, Y., Nakamura, K., Kimura, T., and Ishiguro, S. (2007) Improved Gateway binary vectors: high-performance vectors for creation of fusion constructs in transgenic analysis of plants. Biosci. Biotechnol. Biochem. 71, 2095-2100
41. Tian, G. W., Mohanty, A., Chary, S. N., Li, S., Paap, B., Drakakaki, G., Kopec, C. D., Li, J., Ehrhardt, D., Jackson, D., Rhee, S. Y., Raikhel, N. V., and Citovsky, V. (2004) High-throughput fluorescent tagging of full-length Arabidopsis gene products in planta. Plant Physiol. 135, 25-38
42. Kodama, T., Fukui, K., and Kometani, K. (1986) The initial phosphate burst in ATP hydrolysis by myosin and subfragment-1 as studied by a modified Malachite Green method for determination of inorganic phosphate. J. Biochem. 99, 1465-1472
43. Kuhlman, P. A., and Bagshaw, C. R. (1998) ATPase kinetics of the Dictyostelium discoideum myosin II motor domain. J. Muscle Res. Cell Motil. 19, 491-504
44. Uyeda, T. Q., Abramson, P. D., and Spudich, J. A. (1996) The neck region of the myosin motor domain acts as a lever arm to generate movement. Proc. Natl. Acad. Sci. U.S.A. 93, 4459-4464
45. Tsiavaliaris, G., Fujita-Becker, S., Dürrwang, U., Diensthuber, R. P., Geeves, M. A., and Manstein, D. J. (2008) Mechanism, regulation, and functional properties of Dictyostelium myosin-1B. J. Biol. Chem. 283, 4520-4527
46. Ito, K., Uyeda, T. Q., Suzuki, Y., Sutoh, K., and Yamamoto, K. (2003) Requirement of domain-domain interaction for conformational change and functional ATP hydrolysis in myosin. J. Biol. Chem. 278, 31049-31057
47. Ito, K., Liu, X., Katayama, E., and Uyeda, T. Q. (1999) Cooperativity between two heads of Dictyostelium myosin II in in vitro motility and ATP hydrolysis. Biophys. J. 76, 985-992
48. Jontes, J. D., Milligan, R. A., Pollard, T. D., and Ostap, E. M. (1997) Kinetic characterization of brush border myosin-I ATPase. Proc. Natl. Acad. Sci. U.S.A. 94, 14332-14337
49. Goldstein, D. A. (1979) Calculation of the concentrations of free cations and cation-ligand complexes in solutions containing multiple divalent cations and ligands. Biophys. J. 26, 235-242
50. Mitsuda, N., Hisabori, T., Takeyasu, K., and Sato, M. H. (2004) VOZ; isolation and characterization of novel vascular plant transcription factors with a one-zinc finger from Arabidopsis thaliana. Plant Cell Physiol. 45, 845-854
51. Yoshimura, M., Homma, K., Saito, J., Inoue, A., Ikebe, R., and Ikebe, M. (2001) Dual regulation of mammalian myosin VI motor function. J. Biol. Chem. 276, 39600-39607
52. Homma, K., Saito, J., Ikebe, R., and Ikebe, M. (2001) Motor function and regulation of myosin X. J. Biol. Chem. 276, 34348-34354
53. 2+ ion concentration and heavy chain phosphorylation regulate the motor activity of a class I myosin. J. Biol. Chem. 280, 6064-6071
54. Rosenfeld, S. S., Houdusse, A., and Sweeney, H. L. (2005) Magnesium regulates ADP dissociation from myosin V. J. Biol. Chem. 280, 6072-6079
55. Hannemann, D. E., Cao, W., Olivares, A. O., Robblee, J. P., and De La Cruz, E. M. (2005) Magnesium, ADP, and actin binding linkage of myosin V: evidence for multiple myosin V-ADP and actomyosin V-ADP states. Biochemistry 44, 8826-8840
56. Heissler, S. M., and Manstein, D. J. (2012) Functional characterization of the human myosin-7a motor domain. Cell. Mol. Life Sci. 69, 299-311
57. 2+. Magnes. Res. 19, 225-236
58. Murphy, E., Freudenrich, C. C., Levy, L. A., London, R. E., and Lieberman, M. (1989) Monitoring cytosolic free magnesium in cultured chicken heart cells by use of the fluorescent indicator Furaptra. Proc. Natl. Acad. Sci. U.S.A. 86, 2981-2984
59. Raju, B., Murphy, E., Levy, L. A., Hall, R. D., and London, R. E. (1989) A fluorescent indicator for measuring cytosolic free magnesium. Am. J. Physiol. 256, C540-C548
60. 2+ in human erythrocytes. Biochim. Biophys. Acta 1035, 169-174
61. 2+ channel protein of Saccharomyces cerevisiae. FEBS J. 273, 1198-1209
62. 2+ concentration in Xenopus muscle fibres at rest, during fatigue and during metabolic blockade. Exp. Physiol. 77, 733-740
63. 2+]i in vascular smooth muscle cells. Am. J. Physiol. 263, C873-C878
64. 2+ in cerebral vascular smooth muscle cells. Eur. J. Pharmacol. 246, 299-301
65. Delva, P., Pastori, C., Degan, M., Montesi, G., and Lechi, A. (2004) Catecholamine-induced regulation in vitro and ex vivo of intralymphocyte ionized magnesium. J. Membr. Biol. 199, 163-171
66. 2+ concentration in smooth muscle cells of guinea pig tenia cecum: intracellular calibration of the fluorescent indicator furaptra. Biophys. J. 73, 3358-3370
67. 2+ in renal epithelial cells. Am. J. Physiol. 262, F1100-F1104
68. Singh, J., and Wisdom, D. M. (1995) Second messenger role of magnesium in pancreatic acinar cells of the rat. Mol. Cell. Biochem. 149, 175-182
69. 2+ in human brain and skeletal muscle by 31P-MRS. Magnes. Res. 21, 157-162
70. Rijkers, G. T., and Griffioen, A. W. (1993) Changes in free cytoplasmic magnesium following activation of human lymphocytes. Biochem. J. 289, 373-377
71. 2+ levels and phosphorylation potentials in mung bean root tips by in vivo 31P NMR spectroscopy. Plant Cell Physiol. 29, 919-924
72. Thaler, M. (1991) Lichtabhängige Anderungen cytoplasmatischer Ionenaktivitäten bei Eremosphaera viridis. Untersuchungen mit ionenselek-tiven Mikroelektroden. Ph.D. thesis, University of Würzburg, Germany
73. De La Cruz, E. M., Sweeney, H. L., and Ostap, E. M. (2000) ADP inhibition of myosin V ATPase activity. Biophys. J. 79, 1524-1529
74. Yengo, C. M., and Sweeney, H. L. (2004) Functional role of loop 2 in myosin V. Biochemistry 43, 2605-2612
75. Kambara, T., Komaba, S., and Ikebe, M. (2006) Human myosin III is a motor having an extremely high affinity for actin. J. Biol. Chem. 281, 37291-37301
76. Millar, N. C., and Geeves, M. A. (1983) The limiting rate of the ATPmediated dissociation of actin from rabbit skeletal muscle myosin subfragment 1. FEBS Lett. 160, 141-148
77. Siemankowski, R. F., Wiseman, M. O., and White, H. D. (1985) ADP dissociation from actomyosin subfragment 1 is sufficiently slow to limit the unloaded shortening velocity in vertebrate muscle. Proc. Natl. Acad. Sci. U.S.A. 82, 658-662
78. Geeves, M. A., and Jeffries, T. E. (1988) The effect of nucleotide upon a specific isomerization of actomyosin subfragment 1. Biochem. J. 256, 41-46
79. Yang, Y., Kovács, M., Sakamoto, T., Zhang, F., Kiehart, D. P., and Sellers, J. R. (2006) Dimerized drosophila myosin VIIa: a processive motor. Proc. Natl. Acad. Sci. U.S.A. 103, 5746-5751
80. Cremo, C. R., and Geeves, M. A. (1998) Interaction of actin and ADP with the head domain of smooth muscle myosin: implications for strain-dependent ADP release in smooth muscle. Biochemistry 37, 1969-1978
81. Watanabe, S., Ikebe, R., and Ikebe, M. (2006) Drosophila myosin VIIA is a high duty ratio motor with a unique kinetic mechanism. J. Biol. Chem. 281, 7151-7160
82. Wojtaszek, P., Anielska-Mazur, A., Gabrys, H., Baluska, F., and Volkmann, D. (2005) Recruitment of myosin VIII towards plastid surfaces is root-cap specific and provides the evidence for actomyosin involvement in root osmosensing. Funct. Plant Biol. 32, 721-736
83. Sattarzadeh, A., Franzen, R., and Schmelzer, E. (2008) The Arabidopsis class VIII myosin ATM2 is involved in endocytosis. Cell Motil. Cytoskeleton 65, 457-468
84. Lapierre, L. A., Kumar, R., Hales, C. M., Navarre, J., Bhartur, S. G., Burnette, J. O., Provance, D. W., Jr., Mercer, J. A., Bähler, M., and Goldenring, J. R. (2001) Myosin vb is associated with plasma membrane recycling systems. Mol. Biol. Cell 12, 1843-1857
85. Avisar, D., Prokhnevsky, A. I., and Dolja, V. V. (2008) Class VIII myosins are required for plasmodesmatal localization of a closterovirus Hsp70 homolog. J. Virol. 82, 2836-2843
86. Nyitrai, M., and Geeves, M. A. (2004) Adenosine diphosphate and strain sensitivity in myosin motors. Philos. Trans. R. Soc. Lond. B Biol. Sci. 359, 1867-1877
87. Jontes, J. D., Wilson-Kubalek, E. M., and Milligan, R. A. (1995) A 32° tail swing in brush border myosin I on ADP release. Nature 378, 751-753
88. Whittaker, M., Wilson-Kubalek, E. M., Smith, J. E., Faust, L., Milligan, R. A., and Sweeney, H. L. (1995) A 35-A movement of smooth muscle myosin on ADP release. Nature 378, 748-751
89. Veigel, C., Wang, F., Bartoo, M. L., Sellers, J. R., and Molloy, J. E. (2002) The gated gait of the processive molecular motor, myosin V. Nat. Cell Biol. 4, 59-65
90. Purcell, T. J., Morris, C., Spudich, J. A., and Sweeney, H. L. (2002) Role of the lever arm in the processive stepping of myosin V. Proc. Natl. Acad. Sci. U.S.A. 99, 14159-14164
91. Sakamoto, T., Wang, F., Schmitz, S., Xu, Y., Xu, Q., Molloy, J. E., Veigel, C., and Sellers, J. R. (2003) Neck length and processivity of myosin V. J. Biol. Chem. 278, 29201-29207
92. 2+ revealed by human T-cell immunodeficiency. Nature 475, 471-476