ABCB19/PGP19 stabilises PIN1 in membrane microdomains in Arabidopsis

Plant Journal

Volumn 57, Issue 1, 2009, Pages 27-44

  Titapiwatanakun, Boosaree ^b   Blakeslee, Joshua J ^a,b   Bandyopadhyay, Anindita ^b   Yang, Haibing ^b   Mravec, Jozef ^c   Sauer, Michael ^c   Cheng, Yan ^b   Adamec, Jiri ^d   Nagashima, Akitomo ^e   Geisler, Markus ^f   Sakai, Tatsuya ^e   Friml, Jiri ^c   Peer, Wendy Ann ^b   Murphy, Angus S ^b,g  

^a BROWN UNIVERSITY   (United States)

^b PURDUE UNIVERSITY   (United States)

^c GHENT UNIVERSITY   (Belgium)

^d Purdue Discovery Park   (United States)

^e RIKEN Center for Sustainable Resource Science   (Japan)

^f UNIVERSITY OF ZURICH   (Switzerland)

^g UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Auxin transport; Detergent resistant membrane; Lipid raft; Multi drug resistance protein; P glycoprotein; PIN1; Trafficking

Indexed keywords

ABC TRANSPORTER; ABCB19 PROTEIN, ARABIDOPSIS; ARABIDOPSIS PROTEIN; CARRIER PROTEIN; INDOLEACETIC ACID DERIVATIVE; PGP19 PROTEIN, ARABIDOPSIS; PIN1 PROTEIN, ARABIDOPSIS; STEROL;

ARABIDOPSIS; ARTICLE; CELL MEMBRANE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; SCHIZOSACCHAROMYCES;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; ATP-BINDING CASSETTE TRANSPORTERS; GENE EXPRESSION REGULATION, PLANT; INDOLEACETIC ACIDS; MEMBRANE MICRODOMAINS; MEMBRANE TRANSPORT PROTEINS; SCHIZOSACCHAROMYCES; STEROLS;

ARABIDOPSIS; SCHIZOSACCHAROMYCES POMBE;

EID: 58149117560     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2008.03668.x     Document Type: Article

References (102)

1. Abas, L., Benjamins, R., Malenica, N., Paciorek, T., Wisniewska, J., Moulinier-Anzola, J.C., Sieberer, T., Friml, J. Luschnig, C. (2006) Intracellular trafficking and proteolysis of the Arabidopsis auxin-efflux facilitator PIN2 are involved in root gravitropism. Nat. Cell Biol. 8, 249 256.
2. Ambudkar, S.V., Dey, S., Hrycyna, C.A., Ramachandra, M., Pastan, I. Gottesman, M.M. (1999) Biochemical, cellular, and pharmacological aspects of the multidrug transporter. Annu. Rev. Pharmacol. Toxicol. 39, 361 398.
3. Babiychuk, E.B. Draeger, A. (2006) Biochemical characterization of detergent-resistant membranes: a systematic approach. Biochem. J. 397, 407 416.
4. Bahler, J., Wu, J.Q., Longtine, M.S., Shah, N.G., McKenzie, A. 3rd., Steever, A.B., Wach, A., Philippsen, P. Pringle, J.R. (1998) Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe. Yeast, 14, 943 951.
5. Bailly, A., Sovero, V., Vincenzetti, V., Santelia, D., Bartnik, D., Koenig, B.W., Mancuso, S., Martinoia, E. Geisler, M. (2008) Modulation of P-glycoproteins by auxin transport inhibitors is mediated by interaction with immunophilins. J. Biol. Chem. 283, 21817 21826.
6. Bandyopadhyay, A., Blakeslee, J.J., Lee, O.R. et al. (2007) Interactions of PIN and PGP auxin transport mechanisms. Biochem. Soc. Trans. 35, 137 141.
7. Bennett, M.J., Marchant, A., Green, H.G., May, S.T., Ward, S.P., Millner, P.A., Walker, A.R., Schulz, B. Feldmann, K.A. (1996) Arabidopsis AUX1 gene: a permease-like regulator of root gravitropism. Science, 273, 948 950.
8. Betz, W.J., Mao, F. Smith, C.B. (1996) Imaging exocytosis and endocytosis. Curr. Opin. Neurobiol. 6, 365 371.
9. Blakeslee, J.J., Peer, W.A. Murphy, A.S. (2005) Auxin transport. Curr. Opin. Plant Biol. 8, 494 500.
10. Blakeslee, J.J., Bandyopadhyay, A., Lee, O.R. et al. (2007) Interactions among PIN-FORMED and P-glycoprotein auxin transporters in Arabidopsis. Plant Cell, 19, 131 147.
11. Blilou, I., Xu, J., Wildwater, M., Willemsen, V., Paponov, I., Friml, J., Heidstra, R., Aida, M., Palme, K. Scheres, B. (2005) The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature, 433, 39 44.
12. Borner, G.H., Sherrier, D.J., Weimar, T., Michaelson, L.V., Hawkins, N.D., Macaskill, A., Napier, J.A., Beale, M.H., Lilley, K.S. Dupree, P. (2005) Analysis of detergent-resistant membranes in Arabidopsis. Evidence for plasma membrane lipid rafts. Plant Physiol. 137, 104 116.
13. Bouchard, R., Bailly, A., Blakeslee, J.J. et al. (2006) Immunophilin-like TWISTED DWARF1 modulates auxin efflux activities of Arabidopsis P-glycoproteins. J. Biol. Chem. 281, 30603 30612.
14. Chen, R., Hilson, P., Sedbrook, J., Rosen, E., Caspar, T. Masson, P.H. (1998) The arabidopsis thaliana AGRAVITROPIC 1 gene encodes a component of the polar-auxin-transport efflux carrier. Proc. Natl. Acad. Sci. USA, 95, 15112 15117.
15. Cho, M., Lee, S.H. Cho, H.T. (2007) P-glycoprotein4 displays auxin efflux transporter-like action in Arabidopsis root hair cells and tobacco cells. Plant Cell, 19, 3930 3943.
16. Dhonukshe, P., Grigoriev, I., Fischer, R. et al. (2008) Auxin transport inhibitors impair vesicle motility and actin cytoskeleton dynamics in diverse eukaryotes. Proc. Natl. Acad. Sci. USA, 105, 4489 4494.
17. Dijkhuis, A.J., Douwes, J., Kamps, W., Sietsma, H. Kok, J.W. (2003) Differential expression of sphingolipids in P-glycoprotein or multidrug resistance-related protein 1 expressing human neuroblastoma cell lines. FEBS Lett. 548, 28 32.
18. Doerner, P. (2008) Plant roots: recycled auxin energizes patterning and growth. Curr. Biol. 18, R72 R74.
19. Duenas, E., Vazquez de Aldana, C.R., de Cos, T., Castro, C. Henar Valdivieso, M. (1999) Generation of null alleles for the functional analysis of six genes from the right arm of Saccharomyces cerevisiae chromosome II. Yeast, 15, 615 623.
20. Friml, J., Vieten, A., Sauer, M., Weijers, D., Schwarz, H., Hamann, T., Offringa, R. Jurgens, G. (2003) Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature, 426, 147 153.
21. Fu, D. Roufogalis, B.D. (2007) Actin disruption inhibits endosomal traffic of P-glycoprotein-EGFP and resistance to daunorubicin accumulation. Am. J. Physiol. Cell Physiol. 292, C1543 C1552.
22. Galvan-Ampudia, C.S. Offringa, R. (2007) Plant evolution: AGC kinases tell the auxin tale. Trends Plant Sci. 12, 541 547.
23. Galweiler, L., Guan, C., Muller, A., Wisman, E., Mendgen, K., Yephremov, A. Palme, K. (1998) Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science, 282, 2226 2230.
24. Garrigues, A., Escargueil, A.E. Orlowski, S. (2002) The multidrug transporter, P-glycoprotein, actively mediates cholesterol redistribution in the cell membrane. Proc. Natl. Acad. Sci. USA, 99, 10347 10352.
25. Gayet, L., Dayan, G., Barakat, S., Labialle, S., Michaud, M., Cogne, S., Mazane, A., Coleman, A.W., Rigal, D. Baggetto, L.G. (2005) Control of P-glycoprotein activity by membrane cholesterol amounts and their relation to multidrug resistance in human CEM leukemia cells. Biochemistry, 44, 4499 4509.
26. Geisler, M. Murphy, A.S. (2006) The ABC of auxin transport: the role of p-glycoproteins in plant development. FEBS Lett. 580, 1094 1102.
27. Geisler, M., Kolukisaoglu, H.U., Bouchard, R. et al. (2003) TWISTED DWARF1, a unique plasma membrane-anchored immunophilin-like protein, interacts with Arabidopsis multidrug resistance-like transporters AtPGP1 and AtPGP19. Mol. Biol. Cell 14, 4238 4249.
28. Geisler, M., Blakeslee, J.J., Bouchard, R. et al. (2005) Cellular efflux of auxin catalyzed by the Arabidopsis MDR/PGP transporter AtPGP1. Plant J. 44, 179 194.
29. Geldner, N., Friml, J., Stierhof, Y.D., Jurgens, G. Palme, K. (2001) Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature, 413, 425 428.
30. Geldner, N., Anders, N., Wolters, H., Keicher, J., Kornberger, W., Muller, P., Delbarre, A., Ueda, T., Nakano, A. Jurgens, G. (2003) The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell, 112, 219 230.
31. Gemmill, T.R. Trimble, R.B. (1998) All pyruvylated galactose in Schizosaccharomyces pombe N-glycans is present in the terminal disaccharide, 4, 6-O-[(R)-(1-carboxyethylidine)]-Galbeta1,3Galalpha1. Glycobiology, 8, 1087 1095.
32. Gil, P., Dewey, E., Friml, J., Zhao, Y., Snowden, K.C., Putterill, J., Palme, K., Estelle, M. Chory, J. (2001) BIG: a calossin-like protein required for polar auxin transport in Arabidopsis. Genes Dev. 15, 1985 1997.
33. Gillmor, C.S., Lukowitz, W., Brininstool, G., Sedbrook, J.C., Hamann, T., Poindexter, P. Somerville, C. (2005) Glycosylphosphatidylinositol-anchored proteins are required for cell wall synthesis and morphogenesis in Arabidopsis. Plant Cell. 17, 1128 1140.
34. Gomez-Mouton, C., Abad, J.L., Mira, E., Lacalle, R.A., Gallardo, E., Jimenez-Baranda, S., Illa, I., Bernad, A., Manes, S. Martinez, A.C. (2001) Segregation of leading-edge and uropod components into specific lipid rafts during T cell polarization. Proc. Natl. Acad. Sci. USA, 98, 9642 9647.
35. Grieneisen, V.A., Xu, J., Maree, A.F., Hogeweg, P. Scheres, B. (2007) Auxin transport is sufficient to generate a maximum and gradient guiding root growth. Nature, 449, 1008 1013.
36. Heese-Peck, A., Pichler, H., Zanolari, B., Watanabe, R., Daum, G. Riezman, H. (2002) Multiple functions of sterols in yeast endocytosis. Mol. Biol. Cell. 13, 2664 2680.
37. Illinger, D. Kuhry, J.G. (1994) The kinetic aspects of intracellular fluorescence labeling with TMA-DPH support the maturation model for endocytosis in L929 cells. J. Cell. Biol. 125, 783 794.
38. Jaillais, Y., Fobis-Loisy, I., Miege, C., Rollin, C. Gaude, T. (2006) AtSNX1 defines an endosome for auxin-carrier trafficking in Arabidopsis. Nature, 443, 106 109.
39. Kamau, S.W., Kramer, S.D., Gunthert, M. Wunderli-Allenspach, H. (2005) Effect of the modulation of the membrane lipid composition on the localization and function of P-glycoprotein in MDR1-MDCK cells. In Vitro Cell. Dev. Biol. Anim. 41, 207 216.
40. Kleine-Vehn, J., Dhonukshe, P., Swarup, R., Bennett, M. Friml, J. (2006) Subcellular trafficking of the Arabidopsis auxin influx carrier AUX1 uses a novel pathway distinct from PIN1. Plant Cell. 18, 3171 3181.
41. Laloi, M., Perret, A.M., Chatre, L. et al. (2007) Insights into the role of specific lipids in the formation and delivery of lipid microdomains to the plasma membrane of plant cells. Plant Physiol. 143, 461 472.
42. Lambert, D., O'Neill, C.A. Padfield, P.J. (2007) Methyl-beta-cyclodextrin increases permeability of Caco-2 cell monolayers by displacing specific claudins from cholesterol rich domains associated with tight junctions. Cell. Physiol. Biochem. 20, 495 506.
43. Laxmi, A., Pan, J., Morsy, M. Chen, R. (2008) Light plays an essential role in intracellular distribution of auxin efflux carrier PIN2 in Arabidopsis thaliana. PLoS ONE, 3, e1510.
44. Lefebvre, B., Furt, F., Hartmann, M.A. et al. (2007) Characterization of lipid rafts from Medicago truncatula root plasma membranes: a proteomic study reveals the presence of a raft-associated redox system. Plant Physiol. 144, 402 418.
45. Lewis, D.R., Miller, N.D., Splitt, B.L., Wu, G. Spalding, E.P. (2007) Separating the roles of acropetal and basipetal auxin transport on gravitropism with mutations in two Arabidopsis multidrug resistance-like ABC transporter genes. Plant Cell. 19, 1838 1850.
46. Li, G. Xue, H.W. (2007) Arabidopsis PLDzeta2 regulates vesicle trafficking and is required for auxin response. Plant Cell. 19, 281 295.
47. Lin, R. Wang, H. (2005) Two homologous ATP-binding cassette transporter proteins, AtMDR1 and AtPGP1, regulate Arabidopsis photomorphogenesis and root development by mediating polar auxin transport. Plant Physiol. 138, 949 964.
48. Luker, G.D., Pica, C.M., Kumar, A.S., Covey, D.F. Piwnica-Worms, D. (2000) Effects of cholesterol and enantiomeric cholesterol on P-glycoprotein localization and function in low-density membrane domains. Biochemistry, 39, 7651 7661.
49. Madore, N., Smith, K.L., Graham, C.H., Jen, A., Brady, K., Hall, S. Morris, R. (1999) Functionally different GPI proteins are organized in different domains on the neuronal surface. EMBO J. 18, 6917 6926.
50. Magee, A.I. Parmryd, I. (2003) Detergent-resistant membranes and the protein composition of lipid rafts. Genome Biol. 4, 234.
51. Malenica, N., Abas, L., Benjamins, R., Kitakura, S., Sigmund, H.F., Jun, K.S., Hauser, M.T., Friml, J. Luschnig, C. (2007) MODULATOR OF PIN genes control steady-state levels of Arabidopsis PIN proteins. Plant J. 51, 537 550.
52. Martens, J.R., Navarro-Polanco, R., Coppock, E.A., Nishiyama, A., Parshley, L., Grobaski, T.D. Tamkun, M.M. (2000) Differential targeting of Shaker-like potassium channels to lipid rafts. J. Biol. Chem. 275, 7443 7446.
53. Men, S., Boutte, Y., Ikeda, Y., Li, X., Palme, K., Stierhof, Y.D., Hartmann, M.A., Moritz, T. Grebe, M. (2008) Sterol-dependent endocytosis mediates post-cytokinetic acquisition of PIN2 auxin efflux carrier polarity. Nat. Cell Biol. 10, 237 244.
54. Mongrand, S., Morel, J., Laroche, J., Claverol, S., Carde, J.P., Hartmann, M.A., Bonneu, M., Simon-Plas, F., Lessire, R. Bessoule, J.J. (2004) Lipid rafts in higher plant cells: purification and characterization of Triton X-100-insoluble microdomains from tobacco plasma membrane. J. Biol. Chem. 279, 36277 36286.
55. Morel, J., Claverol, S., Mongrand, S., Furt, F., Fromentin, J., Bessoule, J.J., Blein, J.P. Simon-Plas, F. (2006) Proteomics of plant detergent-resistant membranes. Mol. Cell Proteomics. 5, 1396 1411.
56. Multani, D.S., Briggs, S.P., Chamberlin, M.A., Blakeslee, J.J., Murphy, A.S. Johal, G.S. (2003) Loss of an MDR transporter in compact stalks of maize br2 and sorghum dw3 mutants. Science, 302, 81 84.
57. Murphy, A.S., Hoogner, K.R., Peer, W.A. Taiz, L. (2002) Identification, purification, and molecular cloning of N-1-naphthylphthalmic acid-binding plasma membrane-associated aminopeptidases from Arabidopsis. Plant Physiol. 128, 935 950.
58. Nagashima, A., Suzuki, G., Uehara, Y. et al. (2008) Phytochromes and cryptochromes regulate the differential growth of Arabidopsis hypocotyls in both a PGP19-dependent and a PGP19-independent manner. Plant J. 53, 516 529.
59. Nebenfuhr, A., Ritzenthaler, C. Robinson, D.G. (2002) Brefeldin A: deciphering an enigmatic inhibitor of secretion. Plant Physiol. 130, 1102 1108.
60. Noh, B., Murphy, A.S. Spalding, E.P. (2001) Multidrug resistance-like genes of Arabidopsis required for auxin transport and auxin-mediated development. Plant Cell, 13, 2441 2454.
61. Noh, B., Bandyopadhyay, A., Peer, W.A., Spalding, E.P. Murphy, A.S. (2003) Enhanced gravi- and phototropism in plant mdr mutants mislocalizing the auxin efflux protein PIN1. Nature, 423, 999 1002.
62. Nusrat, A., Parkos, C.A., Verkade, P., Foley, C.S., Liang, T.W., Innis-Whitehouse, W., Eastburn, K.K. Madara, J.L. (2000) Tight junctions are membrane microdomains. J. Cell Sci. 113 (Pt 10 1771 1781.
63. Orlowski, S., Martin, S. Escargueil, A. (2006) P-glycoprotein and 'lipid rafts': some ambiguous mutual relationships (floating on them, building them or meeting them by chance?). Cell. Mol. Life Sci. 63, 1038 1059.
64. Paciorek, T., Zazimalova, E., Ruthardt, N. et al. (2005) Auxin inhibits endocytosis and promotes its own efflux from cells. Nature, 435, 1251 1256.
65. Peer, W.A. Murphy, A.S. (2007) Flavonoids and auxin transport: modulators or regulators? Trends Plant Sci. 12, 556 563.
66. Peer, W.A., Bandyopadhyay, A., Blakeslee, J.J., Makam, S.N., Chen, R.J., Masson, P.H. Murphy, A.S. (2004) Variation in expression and protein localization of the PIN family of auxin efflux facilitator proteins in flavonoid mutants with altered auxin transport in Arabidopsis thaliana. Plant Cell, 16, 1898 1911.
67. Perez-Perez, J.M., Ponce, M.R. Micol, J.L. (2004) The ULTRACURVATA2 gene of Arabidopsis encodes an FK506-binding protein involved in auxin and brassinosteroid signaling. Plant Physiol. 134, 101 117.
68. Petrasek, J., Mravec, J., Bouchard, R. et al. (2006) PIN proteins perform a rate-limiting function in cellular auxin efflux. Science, 312, 914 918.
69. Raven, J.A. (1975) Transport of indoleacetic-acid in plant-cells in relation to Ph and electrical potential gradients, and its significance for polar Iaa transport. New Phytol. 74, 163 172.
70. Richter, S., Geldner, N., Schrader, J., Wolters, H., Stierhof, Y.D., Rios, G., Koncz, C., Robinson, D.G. Jurgens, G. (2007) Functional diversification of closely related ARF-GEFs in protein secretion and recycling. Nature, 448, 488 492.
71. Rojas-Pierce, M., Titapiwatanakun, B., Sohn, E.J. et al. (2007) Arabidopsis P-glycoprotein19 participates in the inhibition of gravitropism by gravacin. Chem. Biol. 14, 1366 1376.
72. Sadler, S.E. Jacobs, N.D. (2004) Stimulation of Xenopus laevis oocyte maturation by methyl-beta-cyclodextrin. Biol. Reprod. 70, 1685 1692.
73. Saint-Jore, C.M., Evins, J., Batoko, H., Brandizzi, F., Moore, I. Hawes, C. (2002) Redistribution of membrane proteins between the golgi apparatus and endoplasmic reticulum in plants is reversible and not dependent on cytoskeletal networks. Plant J. 29, 661 678.
74. Santelia, D., Vincenzetti, V., Azzarello, E., Bovet, L., Fukao, Y., Duchtig, P., Mancuso, S., Martinoia, E. Geisler, M. (2005) MDR-like ABC transporter AtPGP4 is involved in auxin-mediated lateral root and root hair development. FEBS Lett. 579, 5399 5406.
75. Schaller, H., Bouvier-Nave, P. Benveniste, P. (1998) Overexpression of an Arabidopsis cDNA encoding a sterol-C24(1)-methyltransferase in tobacco modifies the ratio of 24-methyl cholesterol to sitosterol and is associated with growth reduction. Plant Physiol. 118, 461 469.
76. Sharom, F.J. Lehto, M.T. (2002) Glycosylphosphatidylinositol-anchored proteins: structure, function, and cleavage by phosphatidylinositol-specific phospholipase C. Biochem. Cell Biol. 80, 535 549.
77. Shin, H., Shin, H.S., Guo, Z., Blancaflor, E.B., Masson, P.H. Chen, R. (2005) Complex regulation of Arabidopsis AGR1/PIN2-mediated root gravitropic response and basipetal auxin transport by cantharidin-sensitive protein phosphatases. Plant J. 42, 188 200.
78. Shogomori, H. Brown, D.A. (2003) Use of detergents to study membrane rafts: the good, the bad, and the ugly. Biol. Chem. 384, 1259 1263.
79. Sidler, M., Hassa, P., Hasan, S., Ringli, C. Dudler, R. (1998) Involvement of an ABC transporter in a developmental pathway regulating hypocotyl cell elongation in the light. Plant Cell. 10, 1623 1636.
80. Sieburth, L.E., Muday, G.K., King, E.J., Benton, G., Kim, S., Metcalf, K.E., Meyers, L., Seamen, E. Van Norman, J.M. (2006) SCARFACE encodes an ARF-GAP that is required for normal auxin efflux and vein patterning in Arabidopsis. Plant Cell, 18, 1396 1411.
81. Steinmann, T., Geldner, N., Grebe, M., Mangold, S., Jackson, C.L., Paris, S., Galweiler, L., Palme, K. Jurgens, G. (1999) Coordinated polar localization of auxin efflux carrier PIN1 by GNOM ARF GEF. Science, 286, 316 318.
82. Swarup, R., Friml, J., Marchant, A., Ljung, K., Sandberg, G., Palme, K. Bennett, M. (2001) Localization of the auxin permease AUX1 suggests two functionally distinct hormone transport pathways operate in the Arabidopsis root apex. Genes Dev. 15, 2648 2653.
83. Swarup, R., Kargul, J., Marchant, A. et al. (2004) Structure-function analysis of the presumptive Arabidopsis auxin permease AUX1. Plant Cell. 16, 3069 3083.
84. Swarup, R., Kramer, E.M., Perry, P., Knox, K., Leyser, H.M., Haseloff, J., Beemster, G.T., Bhalerao, R. Bennett, M.J. (2005) Root gravitropism requires lateral root cap and epidermal cells for transport and response to a mobile auxin signal. Nat. Cell Biol. 7, 1057 1065.
85. Taylor, J.E. Fernandez-Patron, C. (2003) Delivery of bioactive, gel-isolated proteins into live cells. Electrophoresis, 24, 1331 1337.
86. Teh, O.K. Moore, I. (2007) An ARF-GEF acting at the golgi and in selective endocytosis in polarized plant cells. Nature, 448, 493 496.
87. Terasaka, K., Blakeslee, J.J., Titapiwatanakun, B. et al. (2005) PGP4, an ATP binding cassette P-glycoprotein, catalyzes auxin transport in Arabidopsis thaliana roots. Plant Cell. 17, 2922 2939.
88. Troost, J., Lindenmaier, H., Haefeli, W.E. Weiss, J. (2004) Modulation of cellular cholesterol alters P-glycoprotein activity in multidrug-resistant cells. Mol. Pharmacol. 66, 1332 1339.
89. Tse, Y.C., Lo, S.W., Hillmer, S., Dupree, P. Jiang, L. (2006) Dynamic response of prevacuolar compartments to brefeldin a in plant cells. Plant Physiol. 142, 1442 1459.
90. Ueda, T., Yamaguchi, M., Uchimiya, H. Nakano, A. (2001) Ara6, a plant-unique novel type Rab GTPase, functions in the endocytic pathway of Arabidopsis thaliana. EMBO J. 20, 4730 4741.
91. Ueda, T., Uemura, T., Sato, M.H. Nakano, A. (2004) Functional differentiation of endosomes in Arabidopsis cells. Plant J. 40, 783 789.
92. Wachtler, V. Balasubramanian, M.K. (2006) Yeast lipid rafts? - an emerging view. Trends Cell Biol. 16, 1 4.
93. Wachtler, V., Rajagopalan, S. Balasubramanian, M.K. (2003) Sterol-rich plasma membrane domains in the fission yeast Schizosaccharomyces pombe. J. Cell Sci. 116, 867 874.
94. Wang, Y., Loo, T.W., Bartlett, M.C. Clarke, D.M. (2007a) Additive effect of multiple pharmacological chaperones on maturation of CFTR processing mutants. Biochem. J. 406, 257 263.
95. Wang, Y., Loo, T.W., Bartlett, M.C. Clarke, D.M. (2007b) Correctors promote maturation of cystic fibrosis transmembrane conductance regulator (CFTR)-processing mutants by binding to the protein. J. Biol. Chem. 282, 33247 33251.
96. Willemsen, V., Friml, J., Grebe, M., van den Toorn, A., Palme, K. Scheres, B. (2003) Cell polarity and PIN protein positioning in Arabidopsis require STEROL METHYLTRANSFERASE1 function. Plant Cell. 15, 612 625.
97. Wojtal, K.A., de Vries, E., Hoekstra, D. van Ijzendoorn, S.C. (2006) Efficient trafficking of MDR1/P-glycoprotein to apical canalicular plasma membranes in HepG2 cells requires PKA-RIIalpha anchoring and glucosylceramide. Mol. Biol. Cell. 17, 3638 3650.
98. Worrall, D., Ng, C.K. Hetherington, A.M. (2003) Sphingolipids, new players in plant signaling. Trends Plant Sci. 8, 317 320.
99. Wu, G., Lewis, D.R. Spalding, E.P. (2007) Mutations in Arabidopsis multidrug resistance-like ABC transporters separate the roles of acropetal and basipetal auxin transport in lateral root development. Plant Cell. 19, 1826 1837.
100. Yang, Y., Hammes, U.Z., Taylor, C.G., Schachtman, D.P. Nielsen, E. (2006) High-affinity auxin transport by the AUX1 influx carrier protein. Curr. Biol. 16, 1123 1127.
101. Yasuhara, H., Sonobe, S. Shibaoka, H. (1995) Effects of brefeldin A on the formation of the cell plate in tobacco BY-2 cells. Eur. J. Cell Biol. 66, 274 281.
102. Zazimalova, E., Krecek, P., Skupa, P., Hoyerova, K. Petrasek, J. (2007) Polar transport of the plant hormone auxin - the role of PIN-FORMED (PIN) proteins. Cell. Mol. Life Sci. 64, 1621 1637.