Inhibitors of myosin, but not actin, alter transport through Tradescantia plasmodesmata

Protoplasma

Volumn 248, Issue 1, 2011, Pages 205-216

  Radford, Janine E ^a,b   White, Rosemary G ^a,c  

^a MONASH UNIVERSITY   (Australia)

^b Computer Associates ^*  (Australia)

^c CSIRO   (Australia)

Author keywords

2,3 Butanedione monoxime (BDM); Actin; Cell to cell transport; Cytochalasin; Latrunculin; Myosin; N ethylmaleimide (NEM); Plasmodesmata; Tradescantia virginiana

Indexed keywords

TRADESCANTIA; TRADESCANTIA VIRGINIANA;

EID: 78751647935     PISSN: 0033183X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00709-010-0244-3     Document Type: Article

References (115)

1. Aaziz R, Dinant S, Epel BL (2001) Plasmodesmata and plant cytoskeleton. Trends Plant Sci 6: 326-330.
2. Adams W, Trafford AW, Eisner DA (1998) 2, 3-Butanedione monoxime (BDM) decreases sarcoplasmic reticulum Ca content by stimulating Ca release in isolated rat ventricular myocytes. Pflügers Archiv Eur J Physiol 436: 776-781.
3. Allen TJ, Mikala G, Wu X, Dolphin AC (1998) Effects of 2, 3-butanedione monoxime (BDM) on calcium channels expressed in Xenopus oocytes. J Physiol 508: 1-14.
4. Avisar A, Abu-Abied M, Belausov E, Sadot E, Hawes C, Sparkes IA (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.
5. Baron-Epel O, Hernandez D, Jiang L-W, Meiners S, Schindler M (1988) Dynamic continuity of cytoplasmic and membrane compartments between plant cells. J Cell Biol 106: 715-721.
6. Blackman LM, Overall RL (1998) Immunolocalisation of the cytoskeleton to plasmodesmata of Chara corallina. Plant J 14: 733-741.
7. Blanchard EM, Smith GL, Allen DG, Alpert NR (1990) The effects of 2, 3-butanedione monoxime on initial heat, tension, and aequorin light output of ferret papillary muscles. Pflügers Arch 416: 219-221.
8. Bonsignore CL, Hepler PK (1985) Caffeine inhibition of cytokinesis: dynamics of cell plate formation-deformation in vivo. Protoplasma 129: 28-35.
9. Bostrom TE, Walker NA (1976) Intercellular transport in plants. II. Cyclosis and the rate of intercellular transport of chloride in Chara. J Exp Bot 27: 347-357.
10. Brauer D, Uknalis J, Triana R, Shachar-Hill Y, Tu S-I (1997) Effects of bafilomycin A, and metabolic inhibitors on the maintenance of vacuolar acidity in maize root hair cells. Plant Physiol 113: 809-816.
11. 2+]I and contractile activity. Amer J Physiol 271: C1447-C1456.
12. Chen JC, Kamiya N (1975) Localization of myosin in the internodal cell of Nitella as suggested by differential treatment with N-ethylmaleimide. Cell Struct Funct 1: 1-9.
13. Chen S, Das P, Hari V (1994) In situ localization of ATPase activity in cells of plants infected by maize dwarf mosaic potyvirus. Arch Virol 134: 433-439.
14. Christensen NM, Faulkner CR, Oparka K (2009) Evidence for unidirectional flow through plasmodesmata. Plant Physiol 150: 96-104.
15. Cleland RE, Fujiwara T, Lucas WJ (1994) Plasmodesmal-mediated cell-to-cell transport in wheat roots is modulated by anaerobic stress. Protoplasma 178: 81-85.
16. Collings DA, Asada T, Allen NS, Shibaoka H (1998) Plasma membrane-associated actin in Bright Yellow 2 tobacco cells. Plant Physiol 118: 917-928.
17. Cooke R (1993) The actomyosin engine. FASEB J 9: 636-642.
18. 14 C in Characean cells: faster than visible streaming? J Exp Bot 34: 130-143.
19. Didhevar F, Baker DA (1986) Localization of ATPase in sink tissue of Ricinus. Ann Bot 57: 823-828.
20. Ding B, Kwon M-O, Warnberg L (1996) Evidence that actin filaments are involved in controlling the permeability of plasmodesmata in tobacco mesophyll. Plant J 10: 157-164.
21. Doberstein SK, Baines IC, Wiegand G, Korn ED, Pollard TD (1993) Inhibition of contractile vacuole function in vivo by antibodies against myosin-I. Nature 365: 841-843.
22. Eisfeld J, Mikala G, Varadi G, Schwartz A, Klockner U (1997) Inhibition of cloned human L-type cardiac calcium channels by 2, 3-butanedione monoxime does not require PKA-dependent phosphorylation sites. Biochem Biophys Res Commun 230: 489-492.
23. El-Mezgueldi M, Bagshaw CR (2008) The myosin family: biochemical and kinetic properties. In: Coluccio LM (ed) Chapter 3 Myosins: a superfamily of molecular motors. Springer, New York, pp 55-93.
24. Epel BL (1994) Plasmodesmata: composition, structure and trafficking. Plant Mol Biol 26: 1343-1356.
25. Erwee MG, Goodwin PB (1983) Characterisation of the Egeria densa planch. leaf symplast. Inhibition of the intercellular movement of fluorescent probes by group II ions. Planta 158: 320-328.
26. Esseling-Ozdoba A, Houtman D, van Lammeren AAM, Eiser E, Emons AMC (2008) Hydrodynamic flow in the cytoplasm of plant cells. J Microsc 231: 274-283.
27. Faulkner CR, Blackman LM, Collings DA, Cordwell SJ, Overall RL (2009) Anti-tropomyosin antibodies co-localise with actin microfilaments and label plasmodesmata. Eur J Cell Biol 88: 357-369.
28. Ferreira G, Artigas P, Pizarro G, Brum G (1997) Butanedione monoxime promotes voltage-dependent inactivation of L type calcium channels in heart. Effects on gating currents. J Mol Cell Cardiol 29: 777-787.
29. +-ATPase in plasmodesmata located in pit-fields of the young reactive pulvinus of Mimosa pudica L. Protoplasma 188: 180-185.
30. Forer A, Fabian L (2005) Does 2, 3-butanedione monoxime inhibit nonmuscle myosin? Protoplasma 225: 1-4.
31. Funaki K, Nagata A, Akimoto Y, Shimada K, Ito K, Yamamoto K (2004) The motility of Chara corallina myosin was inhibited reversibly by 2, 3-butanedione monoxime (BDM). Plant Cell Physiol 45: 1342-1345.
32. Furukawa-Stoffer T, Byers SD, Hodges DM, Laroche A, Weselake RJ (1998) Identification of N-ethylmaleimide-sensitive and -insensitive phosphatidate phosphatase activity in microspore-derived cultures of oilseed rape. Plant Sci 131: 139-147.
33. Gibbon BC, Kovar DR, Staiger CJ (1999) Latrunculin B has different effects on pollen germination and tube growth. Plant Cell 11: 2349-2363.
34. Golomb L, Abu-Abied M, Belausov E, Sadot (2008) Different subcellular localizations and functions of Arabidopsis myosin VIII. BMC Plant Biol 8: 3.
35. +-pumping inorganic pyrophosphatase. Plant Physiol 111: 195-202.
36. Grabski S, Arnoys E, Busch B, Schindler M (1998) Regulation of actin tension in plant cells by kinases and phosphatases. Plant Physiol 116: 279-290.
37. Grolig F, Schroder J, Sawitzky H, Lange U (1996) Partial characterization of a putative 110 kDa myosin from the green alga Chara corallina by in vitro binding of fluorescence F-actin. Cell Biol Int 20: 365-373.
38. 2+ release by 2, 3-butanedione monoxime in crustacean muscle. Pflügers Arch 424: 39-44.
39. Hayashi T (1960) Experimental studies on protoplasmic streaming in Characeae. Sci Pap Coll Gen Educ Univ Tokyo 10: 245-282.
40. Hepler PK, Valster A, Molchan T, Vos JW (2002) Roles for kinesin and myosin during cytokinesis. Philos Trans R Soc Lond B 357: 761-766.
41. Holdaway-Clarke TL, Walker NA, Hepler PK, Overall RL (2000) Physiological elevations in cytoplasmic free calcium by cold or ion injection result in transient closure of higher plant plasmodesmata. Planta 210: 329-335.
42. Holmes KC (2008) Myosin structure. In: Coluccio LM (ed) Chapter 2 in Myosins: a superfamily of molecular motors. Springer, New York, pp 35-54.
43. Islam K (1989) Thylakoid protein phosphorylation and associated photosystem II fluorescence changes: a study with the ATP analogue adenosine-5-O-thiotriphosphate (ATPγS). Biochim Biophys Acta 974: 267-273.
44. Kawakami S, Watanabe Y, Beachy RN (2004) Tobacco mosaic virus infection spreads cell to cell as intact replication complexes. Proc Natl Acad Sci USA 101: 6291-6296.
45. Kiehart DP, Mabuchi I, Inoué S (1982) Evidence that myosin does not contribute to force production in chromosome movement. J Cell Biol 94: 165-178.
46. Kim I, Kobayashi K, Cho E, Zambryski PC (2005) Subdomains for transport via plasmodesmata corresponding to the apical-basal axis are established during Arabidopsis embryogenesis. Proc Natl Acad Sci USA 102: 11945-11950.
47. Kohama K, Kohama T, Kendrick-Jones J (1987) Effect of N-ethylmaleimide on Ca-inhibition of Physarum myosin. J Biochem 102: 17-23.
48. 2+ inhibition of cytoplasmic streaming in lily pollen tubes. J Cell Sci 91: 501-509.
49. 2+ channel currents in single cells of the guinea-pig taenia caeci. J Physiol 433: 1-23.
50. Lew RR (1994) Regulation of electrical coupling between Arabidopsis root hairs. Planta 195: 67-73.
51. Liu J-Z, Blancaflor EB, Nelson RS (2005) The Tobacco mosaic virus 126-kilodalton protein, a constituent of the virus replication complex, alone or within the complex aligns with and traffics along microfilaments. Plant Physiol 138: 1877-1895.
52. Lucas WJ, Ham B-K, Kim J-K (2009) Plasmodesmata - bridging the gap between neighboring plant cells. Trends Cell Biol 19: 495-503.
53. +-pyrophosphatase maintain the vacuolar proton gradient in metabolic inhibitor-treated Acer pseudoplatanus cells. Biochim Biophys Acta 1229: 323-328.
54. Malec P, Ranaldi RA, Gabrys H (1996) Light-induced chloroplast movements in Lemma trisulca. Identification of the motile system. Plant Sci 120: 127-137.
55. McCurdy DW (1999) Is 2, 3-butanedione monoxime an effective inhibitor of myosin-based activities in plant cells? Protoplasma 209: 120-125.
56. Menzel D (1994) Dynamics and pharmacological perturbations of the endoplasmic reticulum in the unicellular green alga Acetabularia. Eur J Cell Biol 64: 113-119.
57. Mermall V, Post PL, Mooseker MS (1998) Unconventional myosins in cell movement, membrane traffic, and signal transduction. Science 279: 527-533.
58. Molchan TM, Valster AH, Hepler PK (2002) Actomyosin promotes cell plate alignment and late lateral expansion in Tradescantia stamen hair cells. Planta 214: 683-693.
59. Mooseker MS, Wolenski JS, Coleman TR, Hayden SM, Cheney RE, Espreafico E, Heintzelman MB, Peterson MD (1991) Structural and functional dissection of a membrane-bound mechanoenzyme: brush border myosin I. Curr Top Membr 38: 31-55.
60. Nagai R, Fukui S (1981) Differential treatment of Acetabularia with cytochalasin B and N-ethylmaleimide with special reference to their effects on cytoplasmic streaming. Protoplasma 109: 79-89.
61. Oiwa K, Kawakami T, Sugi H (1993) Unitary distance of actin-myosin sliding studied using an in vitro force-movement assay system combined with ATP iontophoresis. J Biochem 114: 28-32.
62. Oparka KJ (2004) Getting the message across: how do plant cells exchange macromolecular complexes? Trends Plant Sci 9: 33-41.
63. Patel JR, Diffee GM, Huang XP, Moss RL (1998) Phosphorylation of myosin regulatory light chain eliminates force-dependent changes in relaxation rates in skeletal muscle. Biophys J 74: 360-368.
64. Phillips RM, Altschuld RA (1996) 2, 3-butanedione 2-monoxime (BDM) induces calcium release from canine cardiac sarcoplasmic reticulum. Biochem Biophys Res Commun 229: 154-157.
65. Prokhnevsky AI, Peremyslov VV, Dolja VA (2005) Actin cytoskeleton is involved in targeting of a viral Hsp70 homolog to the cell periphery. J Virol 79: 14421-14428.
66. Radford JE, White RG (1998) Localization of a myosin-like protein to plasmodesmata. Plant J 14: 743-750.
67. Radford JE, White RG (2001) Effects of tissue-preparation-induced callose synthesis on estimates of plasmodesma size exclusion limits. Protoplasma 216: 47-55.
68. RayChaudhuri A, Hait NC, Dasgupta S, Bhaduri TJ, Deb R, Majumder AL (1997) L-myo-inositol 1-phosphate synthase from plant sources. Plant Physiol 115: 727-736.
69. Reichelt S, Knight AE, Hodge TP, Baluska F, Samja J, Volkmann D, 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.
70. Reisen D, Hanson MR (2007) Association of six YFP-myosin XI-tail fusions with mobile plant cell organelles BMC. Plant Biol 7: 6.
71. Robards AW, Kidwal P (1979) Cytochemical localization of phosphatase in differentiating secondary vascular cells. Planta 87: 227-238.
72. Roberts AG, Oparka KJ (2003) Plasmodesmata and the control of symplastic transport. Plant Cell Environ 26: 103-124.
73. Roopnarine O, Thomas DD (1996) Orientation of intermediate nucleotide states of indane dione spin-labeled myosin heads in muscle fibers. Biophys J 70: 2795-2806.
74. 2+-dependent proteinase from Arabidopsis roots. Arch Biochem Biophys 348: 143-151.
75. Salitz A, Schmitz K (1989) Influence of microfilament and microtubule inhibitors applied by immersion and microinjection on circulation streaming in the staminal hairs of Tradescantia blossfeldiana. Protoplasma 153: 37-45.
76. Sattarzadeh A, Krahmer J, Germain AD, Hanson MR (2009) A myosin XI tail domain homologous to the yeast myosin vacuole-binding domain interacts with plastids and stromules in Nicotiana benthamiana. Molec Plant 2: 1351-1358.
77. Schindler M, Jiang L (1986) Nuclear actin and myosin as control elements in nucleocytoplasmic transport. J Cell Biol 102: 859-862.
78. Schumaker KS, Gizinski MJ (1995) 1, 4-Dihydropyridine binding sites in moss plasma membranes. J Biol Chem 270: 23461-23467.
79. Seki M, Awata J-Y, Shimada K, Kashiyama T, Ito K, Yamamoto K (2003) Susceptibility of Chara myosin to SH reagents. Plant Cell Physiol 44: 201-205.
80. 2+ and cytochalasin B in permeabilized Characeae cells. Protoplasma 115: 18-24.
81. Spudich JA (1994) How molecular motors work. Nature 372: 515-518.
82. Spudich JA (2001) The myosin swinging cross-bridge model. Nat Rev Molec Cell Biol 2: 387-392.
83. Su S, Liu Z, Chen C, Zhang Y, Wang X, Zhu L, Miao L, Wang X-C, Yuan M (2010) Cucumber Mosaic Virus movement protein severs actin filaments to increase the plasmodesmal size exclusion limit in tobacco. Plant Cell 22: 1373-1387.
84. Sugimoto Y, Tokunaga M, Takezawa Y, Ikebe M, Wakabayashi K (1995) Conformational changes of the myosin heads during hydrolysis of ATP as analyzed by X-ray solution scattering. Biophys J 68: 29s-34s.
85. Tilney LG, Cooke TJ, Connelly PS, Tilney MS (1991) The structure of plasmodesmata as revealed by plasmolysis, detergent extraction, and protease digestion. J Cell Biol 112: 739-747.
86. Tirlapur UK, König K (1999) Near-infrared femtosecond laser pulses as a novel non-invasive means for dye-permeation and 3D imaging of localised dye-coupling in the Arabidopsis root meristem. Plant J 20: 363-370.
87. 2+-controlled cytoplasmic streaming of characean cells. Protoplasma 136: 161-169.
88. Tucker EB (1982) Translocation in the staminal hairs of Setcreasea purpurea. I. A study of cell ultrastructure and cell-to-cell passage of molecular probes. Protoplasma 113: 193-201.
89. Tucker EB (1987) Cytoplasmic streaming does not drive intercellular passage in staminal hairs of Setcreasea purpurea. Protoplasma 137: 140-144.
90. Tucker EB (1988) Inositol bisphosphate and inositol trisphosphate inhibit cell-to-cell passage of carboxyfluorescein in staminal hairs of Setcreasea purpurea. Planta 174: 358-363.
91. Tucker EB (1990) Calcium-loaded 1, 2-bis(2-aminophenoxy)ethane-N, N, N', N'-tetraacetic acid blocks cell-to-cell diffusion of carboxyfluorescein in staminal hairs of Setcreasea purpurea. Planta 182: 34-38.
92. Tucker EB (1993) Azide treatment enhances cell-to-cell diffusion in staminal hairs of Setcreasea purpurea. Protoplasma 174: 45-49.
93. 2+ fluxes may regulate cell-to-cell communication in plants. Plant Physiol 111: 459-467.
94. Tucker EB, Tucker JE (1993) Cell-to-cell diffusion selectivity in staminal hairs of Setcreasea purpurea. Protoplasma 174: 36-44.
95. Tucker JE, Mauzerall D, Tucker EB (1989) Symplastic transport of carboxyfluorescein in staminal hairs of Setcreasea purpurea is diffusive and includes loss to the vacuole. Plant Physiol 90: 1143-1147.
96. Turner A, Wells B, Roberts K (1994) Plasmodesmata of maize root tips: structure and composition. J Cell Science 107: 3351-3361.
97. Uyeda TQ, Abramson PD, Spudich JA (1996) The neck region of the myosin motor domain acts as a lever arm to generate movement. Proc Natl Acad Sci USA 93: 4459-4464.
98. Verrucchia F, Hervé JC (1997) Reversible blockade of gap junctional communication by 2, 3-butanedione monoxime in rat cardiac myocytes. Amer J Physiol 272: C875-C885.
99. Vidali L, McKenna ST, Hepler PK (2001) Actin polymerization is essential for pollen tube growth. Mol Biol Cell 12: 2534-2545.
100. + pumps. Plant Sci 96: 55-68.
101. Volkmann D, Mori T, Tirlapur UK, Konig K, Fujiwara T, Kendrick-Jones J, Baluska F (2003) Unconventional myosins of the plant-specific class VIII: endocytosis, cytokinesis, plasmodesmata/pit-fields, and cell-to-cell coupling. Cell Biol Int 27: 289-291.
102. Walter N, Holweg CL (2008) Head-neck domain of Arabidopsis myosin XI, MYA2, fused with GFP produces F-actin patterns that coincide with fast organelle streaming in different plant cells. BMC Plant Biol 8: 74.
103. 2+ and ATP or adenosine 5′-[γ-thio]-triphosphate (ATPγS) enhances intrinsic fluorescence and induces aggregation which increases the activity of spinach rubisco activase. Biochim Biophys Acta 1202: 47-55.
104. Watanabe M (1993) Effects of 2, 3-butanedione monoxime on smooth-muscle contraction of guinea-pig portal vein. Pflugers Arch 425: 462-468.
105. White RG, Badelt K, Overall RL, Vesk M (1994) Actin associated with plasmodesmata. Protoplasma 180: 169-184.
106. Williamson RE (1975) Cytoplasmic streaming in Chara: a cell model activated by ATP and inhibited by cytochalasin B. J Cell Sci 17: 655-668.
107. 2+, and organization. In: Melkonian M (ed) Algal cell motility. Chapman, Hall, New York, pp 73-98.
108. 2+ currents and action potentials of rats. Am J Hypertens 8: 1232-1240.
109. 2 burst, indicates mobilization of storage photosynthates. Photosynthetica 35: 107-119.
110. Yamamoto K (2008) Plant myosins VIII, XI, and XIII. In: Coluccio LM (ed) Chapter 12 in Myosins: a superfamily of molecular motors. Springer, New York, pp 375-390.
111. 14 C in Nitella flexilis. I. Tandem cells without applied pressure gradients. J Exp Bot 37: 1341-1352.
112. Zhang D, Wadsworth P, Hepler PK (1990) Microtubule dynamics in living dividing plant cells: confocal imaging of microinjected fluorescent brain tubulin. Proc Natl Acad Sci USA 87: 8820-8824.
113. +-pyrophosphatase. J Biol Chem 269: 23342-23350.
114. 2+ currents in adult rat sympathetic neurons does not involve 'chemical phosphatase' activity. Neurosci Lett 155: 24-28.
115. Zurek B, Sanger JM, Sanger JW, Jockusch BM (1990) Differential effects of myosin-antibody complexes on contractile rings and circumferential belts in epitheloid cells. J Cell Sci 97: 297-306.