Phosphorylation-dependent trafficking of plasma membrane proteins in animal and plant cells

Journal of Integrative Plant Biology

Volumn 55, Issue 9, 2013, Pages 789-808

  Offringa, Remko ^a   Huang, Fang ^a,b  

^a LEIDEN UNIVERSITY   (Netherlands)

^b UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

Cell polarity; Endosomal trafficking; Phosphorylation; PIN auxin efflux carriers; Plasmamembrane localized transmembrane proteins

Indexed keywords

HORMONE; MEMBRANE; PLASMA; PROTEIN; SIGNALING; TRANSPORT PROCESS;

MEMBRANE PROTEIN;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; CELL MEMBRANE; CELL POLARITY; CHEMISTRY; ENDOSOMAL TRAFFICKING; METABOLISM; MOLECULAR GENETICS; PHOSPHORYLATION; PIN AUXIN EFFLUX CARRIERS; PLANT CELL; PLASMAMEMBRANE-LOCALIZED TRANSMEMBRANE PROTEINS; PROTEIN TRANSPORT;

CELL POLARITY; ENDOSOMAL TRAFFICKING; PHOSPHORYLATION; PIN AUXIN EFFLUX CARRIERS; PLASMAMEMBRANE-LOCALIZED TRANSMEMBRANE PROTEINS;

AMINO ACID SEQUENCE; ANIMALS; CELL MEMBRANE; CELL POLARITY; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; PLANT CELLS; PROTEIN TRANSPORT;

EID: 84883675751     PISSN: 16729072     EISSN: 17447909     Source Type: Journal    
DOI: 10.1111/jipb.12096     Document Type: Article

References (174)

1. Abas L, Benjamins R, Malenica N, Paciorek T, Wisniewska J, Moulinier-Anzola JC, 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. Ambrose C, Ruan Y, Gardiner J, Tamblyn LM, Catching A, Kirik V, Marc J, Overall R, Wasteneys GO (2013) CLASP interacts with sorting nexin 1 to link microtubules and auxin transport via PIN2 recycling in Arabidopsis thaliana. Dev. Cell 24, 649-659.
3. Apodaca G (2001) Endocytic traffic in polarized epithelial cells: Role of the actin and microtubule cytoskeleton. Traffic 2, 149-159.
4. Barbez E, Kubes M, Rolcik J, Beziat C, Pencik A, Wang B, Rosquete MR, Zhu J, Dobrev PI, Lee Y, Zazimalova E, Petrasek J, Geisler M, Friml J, Kleine-Vehn J (2012) A novel putative auxin carrier family regulates intracellular auxin homeostasis in plants. Nature 485, 119-122.
5. Baskin TI, Peret B, Baluska F, Benfey PN, Bennett M, Forde BG, Gilroy S, Helariutta Y, Hepler PK, Leyser O, Masson PH, Muday GK, Murphy AS, Poethig S, Rahman A, Roberts K, Scheres B, Sharp RE, Somerville C (2010) Shootward and rootward: Peak terminology for plant polarity. Trends Plant Sci. 15, 593-594.
6. Beck M, Zhou J, Faulkner C, MacLean D, Robatzek S (2012) Spatio-temporal cellular dynamics of the Arabidopsis flagellin receptor reveal activation status-dependent endosomal sorting. Plant Cell 24, 4205-4219.
7. Benjamins R, Quint A, Weijers D, Hooykaas P, Offringa R (2001) The PINOID protein kinase regulates organ development in Arabidopsis by enhancing polar auxin transport. Development 128, 4057-4067.
8. Benkova E, Michniewicz M, Sauer M, Teichmann T, Seifertova D, Jürgens G, Friml J (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115, 591-602.
9. Benschop JJ, Mohammed S, O'Flaherty M, Heck AJ, Slijper M, Menke FL (2007) Quantitative phosphoproteomics of early elicitor signaling in Arabidopsis. Mol. Cell Proteomics 6, 1198-1214.
10. Bogre L, Okresz L, Henriques R, Anthony RG (2003) Growth signalling pathways in Arabidopsis and the AGC protein kinases. Trends Plant Sci. 8, 424-431.
11. Boone M, Kortenoeven ML, Robben JH, Tamma G, Deen PM (2011) Counteracting vasopressin-mediated water reabsorption by ATP, dopamine, and phorbol esters: Mechanisms of action. Am. J. Physiol. Renal Physiol. 300, F761-F771.
12. Boursiac Y, Prak S, Boudet J, Postaire O, Luu DT, Tournaire-Roux C, Santoni V, Maurel C (2008) The response of Arabidopsis root water transport to a challenging environment implicates reactive oxygen species- and phosphorylation-dependent internalization of aquaporins. Plant Signal. Behav. 3, 1096-1098.
13. Cadena DL, Chan CL, Gill GN (1994) The intracellular tyrosine kinase domain of the epidermal growth factor receptor undergoes a conformational change upon autophosphorylation. J. Biol. Chem. 269, 260-265.
14. Cardone MH, Smith BL, Song W, Mochly-Rosen D, Mostov KE (1994) Phorbol myristate acetate-mediated stimulation of transcytosis and apical recycling in MDCK cells. J. Cell Biol. 124, 717-727.
15. Carneiro AM, Blakely RD (2006) Serotonin-, protein kinase C-, and Hic-5-associated redistribution of the platelet serotonin transporter. J. Biol. Chem. 281, 24769-24780.
16. Carneiro AM, Ingram SL, Beaulieu JM, Sweeney A, Amara SG, Thomas SM, Caron MG, Torres GE (2002) The multiple LIM domain-containing adaptor protein Hic-5 synaptically colocalizes and interacts with the dopamine transporter. J. Neurosci. 22, 7045-7054.
17. Casanova JE, Apodaca G, Mostov KE (1991) An autonomous signal for basolateral sorting in the cytoplasmic domain of the polymeric immunoglobulin receptor. Cell 66, 65-75.
18. Casanova JE, Breitfeld PP, Ross SA, Mostov KE (1990) Phosphorylation of the polymeric immunoglobulin receptor required for its efficient transcytosis. Science 248, 742-745.
19. Chen R, Hilson P, Sedbrook J, Rosen E, Caspar T, Masson PH (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.
20. Chen Y, Hoehenwarter W, Weckwerth W (2010) Comparative analysis of phytohormone-responsive phosphoproteins in Arabidopsis thaliana using TiO2-phosphopeptide enrichment and mass accuracy precursor alignment. Plant J. 63, 1-17.
21. Cheng Y, Qin G, Dai X, Zhao Y (2008) NPY genes and AGC kinases define two key steps in auxin-mediated organogenesis in Arabidopsis. Proc. Natl. Acad. Sci. USA 105, 21017-21022.
22. Craddock C, Lavagi I, Yang Z (2012) New insights into Rho signaling from plant ROP/Rac GTPases. Trends Cell Biol. 22, 492-501.
23. Cui Y, Li X, Chen Q, He X, Yang Q, Zhang A, Yu X, Chen H, Liu N, Xie Q, Yang W, Zuo J, Palme K, Li W (2010) BLOS1, a putative BLOC-1 subunit, interacts with SNX1 and modulates root growth in Arabidopsis. J. Cell Sci. 123, 3727-3733.
24. Dai M, Zhang C, Kania U, Chen F, Xue Q, McCray T, Li G, Qin G, Wakeley M, Terzaghi W, Wan J, Zhao Y, Xu J, Friml J, Deng XW, Wang H (2012) A PP6-type phosphatase holoenzyme directly regulates PIN phosphorylation and auxin efflux in Arabidopsis. Plant Cell 24, 2497-2514.
25. De Matteis MA, Luini A (2008) Exiting the Golgi complex. Nat. Rev. Mol. Cell Biol. 9, 273-284.
26. De Smet I, Voss U, Lau S, Wilson M, Shao N, Timme RE, Swarup R, Kerr I, Hodgman C, Bock R, Bennett M, Jürgens G, Beeckman T (2011) Unraveling the evolution of auxin signaling. Plant Physiol. 155, 209-221.
27. Deborde S, Perret E, Gravotta D, Deora A, Salvarezza S, Schreiner R, Rodriguez-Boulan E (2008) Clathrin is a key regulator of basolateral polarity. Nature 452, 719-723.
28. Delbarre A, Muller P, Guern J (1998) Short-Lived and phosphorylated proteins contribute to carrier-mediated efflux, but not to influx, of auxin in suspension-cultured tobacco cells. Plant Physiol. 116, 833-844.
29. Dettmer J, Friml J (2011) Cell polarity in plants: When two do the same, it is not the same. Curr. Opin. Cell Biol. 23, 686-696.
30. Dhonukshe P, Aniento F, Hwang I, Robinson DG, Mravec J, Stierhof YD, Friml J (2007) Clathrin-mediated constitutive endocytosis of PIN auxin efflux carriers in Arabidopsis. Curr. Biol. 17, 520-527.
31. Dhonukshe P, Huang F, Galvan-Ampudia CS, Mahonen AP, Kleine-Vehn J, Xu J, Quint A, Prasad K, Friml J, Scheres B, Offringa R (2010) Plasma membrane-bound AGC3 kinases phosphorylate PIN auxin carriers at TPRXS(N/S) motifs to direct apical PIN recycling. Development 137, 3245-3255.
32. Dhonukshe P, Tanaka H, Goh T, Ebine K, Mahonen AP, Prasad K, Blilou I, Geldner N, Xu J, Uemura T, Chory J, Ueda T, Nakano A, Scheres B, Friml J (2008) Generation of cell polarity in plants links endocytosis, auxin distribution and cell fate decisions. Nature 456, 962-966.
33. Ding Z, Galvan-Ampudia CS, Demarsy E, Langowski L, Kleine-Vehn J, Fan Y, Morita MT, Tasaka M, Fankhauser C, Offringa R, Friml J (2011) Light-mediated polarization of the PIN3 auxin transporter for the phototropic response in Arabidopsis. Nat. Cell Biol. 13, 447-452.
34. Dong J, MacAlister CA, Bergmann DC (2009) BASL controls asymmetric cell division in Arabidopsis. Cell 137, 1320-1330.
35. Eto K, Noda Y, Horikawa S, Uchida S, Sasaki S (2010) Phosphorylation of aquaporin-2 regulates its water permeability. J. Biol. Chem. 285, 40777-40784.
36. Feraru E, Feraru MI, Kleine-Vehn J, Martiniere A, Mouille G, Vanneste S, Vernhettes S, Runions J, Friml J (2011) PIN polarity maintenance by the cell wall in Arabidopsis. Curr. Biol. 21, 338-343.
37. Feraru E, Vosolsobe S, Feraru MI, Petrasek J, Kleine-Vehn J (2012) Evolution and structural diversification of PILS putative auxin carriers in plants. Front. Plant Sci. 3, 227.
38. Friml J, Benfey P, Benkova E, Bennett M, Berleth T, Geldner N, Grebe M, Heisler M, Hejatko J, Jürgens G, Laux T, Lindsey K, Lukowitz W, Luschnig C, Offringa R, Scheres B, Swarup R, Torres-Ruiz R, Weijers D, Zazimalova E (2006) Apical-basal polarity: Why plant cells don't stand on their heads. Trends Plant Sci. 11, 12-114.
39. Friml J, Jones AR (2010) Endoplasmic reticulum: The rising compartment in auxin biology. Plant Physiol. 154, 458-462.
40. Friml J, Vieten A, Sauer M, Weijers D, Schwarz H, Hamann T, Offringa R, Jürgens G (2003) Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426, 147-153.
41. Friml J, Wisniewska J, Benkova E, Mendgen K, Palme K (2002) Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 415, 806-809.
42. Friml J, Yang X, Michniewicz M, Weijers D, Quint A, Tietz O, Benjamins R, Ouwerkerk PB, Ljung K, Sandberg G, Hooykaas PJ, Palme K, Offringa R (2004) A PINOID-dependent binary switch in apical-basal PIN polar targeting directs auxin efflux. Science 306, 862-865.
43. Fujiwara T, Ritchie K, Murakoshi H, Jacobson K, Kusumi A (2002) Phospholipids undergo hop diffusion in compartmentalized cell membrane. J. Cell Biol. 157, 1071-1081.
44. Furutani M, Kajiwara T, Kato T, Treml BS, Stockum C, Torres-Ruiz RA, Tasaka M (2007) The gene MACCHI-BOU 4/ENHANCER OF PINOID encodes a NPH3-like protein and reveals similarities between organogenesis and phototropism at the molecular level. Development 134, 3849-3859.
45. Furutani M, Sakamoto N, Yoshida S, Kajiwara T, Robert HS, Friml J, Tasaka M (2011) Polar-localized NPH3-like proteins regulate polarity and endocytosis of PIN-FORMED auxin efflux carriers. Development 138, 2069-2078.
46. Fushimi K, Sasaki S, Marumo F (1997) Phosphorylation of serine 256 is required for cAMP-dependent regulatory exocytosis of the aquaporin-2 water channel. J. Biol. Chem. 272, 14800-14804.
47. Galvan-Ampudia CS, Offringa R (2007) Plant evolution: AGC kinases tell the auxin tale. Trends Plant Sci. 12, 541-547.
48. 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.
49. Ganguly A, Lee SH, Cho HT (2012) Functional identification of the phosphorylation sites of Arabidopsis PIN-FORMED3 for its subcellular localization and biological role. Plant J. 71, 810-823.
50. Geldner N (2009) Cell polarity in plants: A PARspective on PINs. Curr. Opin. Plant Biol. 12, 42-48.
51. Geldner N, Anders N, Wolters H, Keicher J, Kornberger W, Muller P, Delbarre A, Ueda T, Nakano A, Jürgens G (2003) The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell 112, 219-230.
52. Geldner N, Friml J, Stierhof YD, Jürgens G, Palme K (2001) Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature 413, 425-428.
53. Geldner N, Hyman DL, Wang X, Schumacher K, Chory J (2007) Endosomal signaling of plant steroid receptor kinase BRI1. Genes Dev. 21, 1598-1602.
54. Geldner N, Robatzek S (2008) Plant receptors go endosomal: A moving view on signal transduction. Plant Physiol. 147, 1565-1574.
55. Gomez-Gomez L, Bauer Z, Boller T (2001) Both the extracellular leucine-rich repeat domain and the kinase activity of FSL2 are required for flagellin binding and signaling in Arabidopsis. Plant Cell 13, 1155-1163.
56. Gravotta D, Carvajal-Gonzalez JM, Mattera R, Deborde S, Banfelder JR, Bonifacino JS, Rodriguez-Boulan E (2012) The clathrin adaptor AP-1A mediates basolateral polarity. Dev. Cell 22, 811-823.
57. Grefen C, Blatt MR (2008) SNAREs-molecular governors in signalling and development. Curr. Opin. Plant Biol. 11, 600-609.
58. Gullapalli A, Garrett TA, Paing MM, Griffin CT, Yang Y, Trejo J (2004) A role for sorting nexin 2 in epidermal growth factor receptor down-regulation: Evidence for distinct functions of sorting nexin 1 and 2 in protein trafficking. Mol. Biol. Cell 15, 2143-2155.
59. Gullapalli A, Wolfe BL, Griffin CT, Magnuson T, Trejo J (2006) An essential role for SNX1 in lysosomal sorting of protease-activated receptor-1: Evidence for retromer-, Hrs-, and Tsg101-independent functions of sorting nexins. Mol. Biol. Cell 17, 1228-1238.
60. Harrison BR, Masson PH (2008) ARL2, ARG1 and PIN3 define a gravity signal transduction pathway in root statocytes. Plant J. 53, 380-392.
61. Heisler MG, Ohno C, Das P, Sieber P, Reddy GV, Long JA, Meyerowitz EM (2005) Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem. Curr. Biol. 15, 1899-1911.
62. Hirokawa N, Noda Y, Tanaka Y, Niwa S (2009) Kinesin superfamily motor proteins and intracellular transport. Nat. Rev. Mol. Cell Biol. 10, 682-696.
63. Hirt RP, Hughes GJ, Frutiger S, Michetti P, Perregaux C, Poulain-Godefroy O, Jeanguenat N, Neutra MR, Kraehenbuhl JP (1993) Transcytosis of the polymeric Ig receptor requires phosphorylation of serine 664 in the absence but not the presence of dimeric IgA. Cell 74, 245-255.
64. Hoffert JD, Fenton RA, Moeller HB, Simons B, Tchapyjnikov D, McDill BW, Yu MJ, Pisitkun T, Chen F, Knepper MA (2008) Vasopressin-stimulated increase in phosphorylation at Ser269 potentiates plasma membrane retention of aquaporin-2. J. Biol. Chem. 283, 24617-24627.
65. Honigmann A, van den Bogaart G, Iraheta E, Risselada HJ, Milovanovic D, Mueller V, Mullar S, Diederichsen U, Fasshauer D, Grubmuller H, Hell SW, Eggeling C, Kuhnel K, Jahn R (2013) Phosphatidylinositol 4, 5-bisphosphate clusters act as molecular beacons for vesicle recruitment. Nat. Struct. Mol. Biol. 20, 679-686.
66. Huang F, Zago MK, Abas L, van MA, Galvan-Ampudia CS, Offringa R (2010) Phosphorylation of conserved PIN motifs directs Arabidopsis PIN1 polarity and auxin transport. Plant Cell 22, 1129-1142.
67. Iden S, Collard JG (2008) Crosstalk between small GTPases and polarity proteins in cell polarization. Nat. Rev. Mol. Cell Biol. 9, 846-859.
68. Jaillais Y, Fobis-Loisy I, Miege C, Gaude T (2008) Evidence for a sorting endosome in Arabidopsis root cells. Plant J. 53, 237-247.
69. 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.
70. Jaillais Y, Santambrogio M, Rozier F, Fobis-Loisy I, Miege C, Gaude T (2007) The retromer protein VPS29 links cell polarity and organ initiation in plants. Cell 130, 1057-1070.
71. Jayanthi LD, Samuvel DJ, Blakely RD, Ramamoorthy S (2005) Evidence for biphasic effects of protein kinase C on serotonin transporter function, endocytosis, and phosphorylation. Mol. Pharmacol. 67, 2077-2087.
72. Jiang J, Zhang C, Wang X (2013) Ligand perception, activation, and early signaling of plant steroid receptor BRI1. J. Integr. Plant Biol. DOI: 10.1111/jipb.12081
73. Kamsteeg EJ, Bichet DG, Konings IB, Nivet H, Lonergan M, Arthus MF, van Os CH, Deen PM (2003) Reversed polarized delivery of an aquaporin-2 mutant causes dominant nephrogenic diabetes insipidus. J. Cell Biol. 163, 1099-1109.
74. Katsura T, Gustafson CE, Ausiello DA, Brown D (1997) Protein kinase A phosphorylation is involved in regulated exocytosis of aquaporin-2 in transfected LLC-PK1 cells. Am. J. Physiol. 272, F817-F822.
75. Kitakura S, Vanneste S, Robert S, Lofke C, Teichmann T, Tanaka H, Friml J (2011) Clathrin mediates endocytosis and polar distribution of PIN auxin transporters in Arabidopsis. Plant Cell 23, 1920-1931.
76. Kleine-Vehn J, Dhonukshe P, Sauer M, Brewer PB, Wisniewska J, Paciorek T, Benkova E, Friml J (2008a) ARF GEF-dependent transcytosis and polar delivery of PIN auxin carriers in Arabidopsis. Curr. Biol. 18, 526-531.
77. Kleine-Vehn J, Huang F, Naramoto S, Zhang J, Michniewicz M, Offringa R, Friml J (2009) PIN auxin efflux carrier polarity is regulated by PINOID kinase-mediated recruitment into GNOM-independent trafficking in Arabidopsis. Plant Cell 21, 3839-3849.
78. Kleine-Vehn J, Leitner J, Zwiewka M, Sauer M, Abas L, Luschnig C, Friml J (2008b) Differential degradation of PIN2 auxin efflux carrier by retromer-dependent vacuolar targeting. Proc. Natl. Acad. Sci. USA 105, 17812-17817.
79. Kleine-Vehn J, Wabnik K, Martiniere A, Langowski L, Willig K, Naramoto S, Leitner J, Tanaka H, Jakobs S, Robert S, Luschnig C, Govaerts W, Hell SW, Runions J, Friml J (2011) Recycling, clustering, and endocytosis jointly maintain PIN auxin carrier polarity at the plasma membrane. Mol. Syst. Biol. 7, 540.
80. Korbei B, Luschnig C (2013) Plasma membrane protein ubiquitylation and degradation as determinants of positional growth in plants. J. Integr. Plant Biol. 55, 809-823.
81. Kost B, Chua NH (2002) The plant cytoskeleton: Vacuoles and cell walls make the difference. Cell 108, 9-912.
82. Krecek P, Skupa P, Libus J, Naramoto S, Tejos R, Friml J, Zazimalova E (2009) The PIN-FORMED (PIN) protein family of auxin transporters. Genome Biol. 10, 249.
83. Kurten RC (2003) Sorting motifs in receptor trafficking. Adv. Drug Deliv. Rev. 55, 1405-1419.
84. Kurten RC, Cadena DL, Gill GN (1996) Enhanced degradation of EGF receptors by a sorting nexin, SNX1. Science 272, 1008-1010.
85. Langowski L, Ruzicka K, Naramoto S, Kleine-Vehn J, Friml J (2010) Trafficking to the outer polar domain defines the root-soil interface. Curr. Biol. 20, 904-908.
86. 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.
87. Leitner J, Petrasek J, Tomanov K, Retzer K, Parezova M, Korbei B, Bachmair A, Zazimalova E, Luschnig C (2012) Lysine63-linked ubiquitylation of PIN2 auxin carrier protein governs hormonally controlled adaptation of Arabidopsis root growth. Proc. Natl. Acad. Sci. USA 109, 8322-8327.
88. Lenne PF, Wawrezinieck L, Conchonaud F, Wurtz O, Boned A, Guo XJ, Rigneault H, He HT, Marguet D (2006) Dynamic molecular confinement in the plasma membrane by microdomains and the cytoskeleton meshwork. EMBO J. 25, 3245-3256.
89. Leto D, Saltiel AR (2012) Regulation of glucose transport by insulin: Traffic control of GLUT4. Nat. Rev. Mol. Cell Biol. 13, 383-396.
90. Levkowitz G, Waterman H, Ettenberg SA, Katz M, Tsygankov AY, Alroy I, Lavi S, Iwai K, Reiss Y, Ciechanover A, Lipkowitz S, Yarden Y (1999) Ubiquitin ligase activity and tyrosine phosphorylation underlie suppression of growth factor signaling by c-Cbl/Sli-1. Mol. Cell 4, 1029-1040.
91. Li H, Lin D, Dhonukshe P, Nagawa S, Chen D, Friml J, Scheres B, Guo H, Yang Z (2011a) Phosphorylation switch modulates the interdigitated pattern of PIN1 localization and cell expansion in Arabidopsis leaf epidermis. Cell Res. 21, 970-978.
92. Li R, Liu P, Wan Y, Chen T, Wang Q, Mettbach U, Baluska F, Samaj J, Fang X, Lucas WJ, Lin J (2012) A membrane microdomain-associated protein, Arabidopsis Flot1, is involved in a clathrin-independent endocytic pathway and is required for seedling development. Plant Cell 24, 2105-2122.
93. Li W, Zhang Q, Oiso N, Novak EK, Gautam R, O'Brien EP, Tinsley CL, Blake DJ, Spritz RA, Copeland NG, Jenkins NA, Amato D, Roe BA, Starcevic M, Dell'Angelica EC, Elliott RW, Mishra V, Kingsmore SF, Paylor RE, Swank RT (2003) Hermansky-Pudlak syndrome type 7 (HPS-7) results from mutant dysbindin, a member of the biogenesis of lysosome-related organelles complex 1 (BLOC-1). Nat. Genet. 35, 84-89.
94. Li X, Wang X, Yang Y, Li R, He Q, Fang X, Luu DT, Maurel C, Lin J (2011b) Single-molecule analysis of PIP2;1 dynamics and partitioning reveals multiple modes of Arabidopsis plasma membrane aquaporin regulation. Plant Cell 23, 3780-3797.
95. Lu D, Lin W, Gao X, Wu S, Cheng C, Avila J, Heese A, Devarenne TP, He P, Shan L (2011) Direct ubiquitination of pattern recognition receptor FLS2 attenuates plant innate immunity. Science 332, 1439-1442.
96. Lu D, Wu S, Gao X, Zhang Y, Shan L, He P (2010) A receptor-like cytoplasmic kinase, BIK1, associates with a flagellin receptor complex to initiate plant innate immunity. Proc. Natl. Acad. Sci. USA 107, 496-501.
97. Luschnig C, Gaxiola RA, Grisafi P, Fink GR (1998) EIR1, a root-specific protein involved in auxin transport, is required for gravitropism in Arabidopsis thaliana. Genes Dev. 12, 2175-2187.
98. Luton F, Cardone MH, Zhang M, Mostov KE (1998) Role of tyrosine phosphorylation in ligand-induced regulation of transcytosis of the polymeric Ig receptor. Mol. Biol. Cell 9, 1787-1802.
99. Luton F, Hexham MJ, Zhang M, Mostov KE (2009) Identification of a cytoplasmic signal for apical transcytosis. Traffic 10, 1128-1142.
100. Luton F, Verges M, Vaerman JP, Sudol M, Mostov KE (1999) The SRC family protein tyrosine kinase p62yes controls polymeric IgA transcytosis in vivo. Mol. Cell 4, 627-632.
101. Malinska K, Zazimalova E (2011) Uniform structure of eukaryotic plasma membrane: Lateral domains in plants. Curr. Protein Pept. Sci. 12, 148-155.
102. Martiniere A, Lavagi I, Nageswaran G, Rolfe DJ, Maneta-Peyret L, Luu DT, Botchway SW, Webb SE, Mongrand S, Maurel C, Martin-Fernandez ML, Kleine-Vehn J, Friml J, Moreau P, Runions J (2012) Cell wall constrains lateral diffusion of plant plasma-membrane proteins. Proc. Natl. Acad. Sci. USA 109, 12805-12810.
103. Mellman I, Nelson WJ (2008) Coordinated protein sorting, targeting and distribution in polarized cells. Nat. Rev. Mol. Cell Biol. 9, 833-845.
104. Michniewicz M, Zago MK, Abas L, Weijers D, Schweighofer A, Meskiene I, Heisler MG, Ohno C, Zhang J, Huang F, Schwab R, Weigel D, Meyerowitz EM, Luschnig C, Offringa R, Friml J (2007) Antagonistic regulation of PIN phosphorylation by PP2A and PINOID directs auxin flux. Cell 130, 1044-1056.
105. Moeller HB, Olesen ET, Fenton RA (2011) Regulation of the water channel aquaporin-2 by posttranslational modification. Am. J. Physiol. Renal Physiol. 300, F1062-F1073.
106. Moeller HB, Praetorius J, Rutzler MR, Fenton RA (2010) Phosphorylation of aquaporin-2 regulates its endocytosis and protein-protein interactions. Proc. Natl. Acad. Sci. USA 107, 424-429.
107. Mostowy S, Cossart P (2012) Septins: The fourth component of the cytoskeleton. Nat. Rev. Mol. Cell Biol. 13, 183-194.
108. Mravec J, Petrasek J, Li N, Boeren S, Karlova R, Kitakura S, Parezova M, Naramoto S, Nodzynski T, Dhonukshe P, Bednarek SY, Zazimalova E, de VS, Friml J (2011) Cell plate restricted association of DRP1A and PIN proteins is required for cell polarity establishment in Arabidopsis. Curr. Biol. 21, 1055-1060.
109. Mravec J, Skupa P, Bailly A, Hoyerova K, Krecek P, Bielach A, Petrasek J, Zhang J, Gaykova V, Stierhof YD, Dobrev PI, Schwarzerova K, Rolcik J, Seifertova D, Luschnig C, Benkova E, Zazimalova E, Geisler M, Friml J (2009) Subcellular homeostasis of phytohormone auxin is mediated by the ER-localized PIN5 transporter. Nature 459, 1136-1140.
110. Muller A, Guan C, Galweiler L, Tanzler P, Huijser P, Marchant A, Parry G, Bennett M, Wisman E, Palme K (1998) AtPIN2 defines a locus of Arabidopsis for root gravitropism control. EMBO J. 17, 6903-6911.
111. Munnik T, Testerink C (2009) Plant phospholipid signaling: "In a nutshell". J. Lipid Res. 50 (Suppl), S260-S265.
112. Nesterov A, Kurten RC, Gill GN (1995a) Association of epidermal growth factor receptors with coated pit adaptins via a tyrosine phosphorylation-regulated mechanism. J. Biol. Chem. 270, 6320-6327.
113. Nesterov A, Wiley HS, Gill GN (1995b) Ligand-induced endocytosis of epidermal growth factor receptors that are defective in binding adaptor proteins. Proc. Natl. Acad. Sci. USA 92, 8719-8723.
114. Noda Y, Horikawa S, Kanda E, Yamashita M, Meng H, Eto K, Li Y, Kuwahara M, Hirai K, Pack C, Kinjo M, Okabe S, Sasaki S (2008) Reciprocal interaction with G-actin and tropomyosin is essential for aquaporin-2 trafficking. J. Cell Biol. 182, 587-601.
115. Normanly J (2010) Approaching cellular and molecular resolution of auxin biosynthesis and metabolism. Cold Spring Harb. Perspect. Biol. 2, a001594.
116. Nuhse TS, Stensballe A, Jensen ON, Peck SC (2004) Phosphoproteomics of the Arabidopsis plasma membrane and a new phosphorylation site database. Plant Cell 16, 2394-2405.
117. Okamoto CT, Song W, Bomsel M, Mostov KE (1994) Rapid internalization of the polymeric immunoglobulin receptor requires phosphorylated serine 726. J. Biol. Chem. 269, 15676-15682.
118. Opresko LK, Chang CP, Will BH, Burke PM, Gill GN, Wiley HS (1995) Endocytosis and lysosomal targeting of epidermal growth factor receptors are mediated by distinct sequences independent of the tyrosine kinase domain. J. Biol. Chem. 270, 4325-4333.
119. Paciorek T, Zazimalova E, Ruthardt N, Petrasek J, Stierhof YD, Kleine-Vehn J, Morris DA, Emans N, Jürgens G, Geldner N, Friml J (2005) Auxin inhibits endocytosis and promotes its own efflux from cells. Nature 435, 1251-1256.
120. Petrasek J, Mravec J, Bouchard R, Blakeslee JJ, Abas M, Seifertova D, Wisniewska J, Tadele Z, Kubes M, Covanova M, Dhonukshe P, Skupa P, Benkova E, Perry L, Krecek P, Lee OR, Fink GR, Geisler M, Murphy AS, Luschnig C, Zazimalova E, Friml J (2006) PIN proteins perform a rate-limiting function in cellular auxin efflux. Science 312, 914-918.
121. Pillitteri LJ, Peterson KM, Horst RJ, Torii KU (2011) Molecular profiling of stomatal meristemoids reveals new component of asymmetric cell division and commonalities among stem cell populations in Arabidopsis. Plant Cell 23, 3260-3275.
122. Prak S, Hem S, Boudet J, Viennois G, Sommerer N, Rossignol M, Maurel C, Santoni V (2008) Multiple phosphorylations in the C-terminal tail of plant plasma membrane aquaporins: Role in subcellular trafficking of AtPIP2;1 in response to salt stress. Mol. Cell Proteomics 7, 1019-1030.
123. Rakusova H, Gallego-Bartolome J, Vanstraelen M, Robert HS, Alabadi D, Blazquez MA, Benkova E, Friml J (2011) Polarization of PIN3-dependent auxin transport for hypocotyl gravitropic response in Arabidopsis thaliana. Plant J. 67, 817-826.
124. Ramamoorthy S, Shippenberg TS, Jayanthi LD (2011) Regulation of monoamine transporters: Role of transporter phosphorylation. Pharmacol. Ther. 129, 220-238.
125. Rashotte AM, DeLong A, Muday GK (2001) Genetic and chemical reductions in protein phosphatase activity alter auxin transport, gravity response, and lateral root growth. Plant Cell 13, 1683-1697.
126. Reinhardt D, Pesce ER, Stieger P, Mandel T, Baltensperger K, Bennett M, Traas J, Friml J, Kuhlemeier C (2003) Regulation of phyllotaxis by polar auxin transport. Nature 426, 255-260.
127. Richter S, Geldner N, Schrader J, Wolters H, Stierhof YD, Rios G, Koncz C, Robinson DG, Jürgens G (2007) Functional diversification of closely related ARF-GEFs in protein secretion and recycling. Nature 448, 488-492.
128. Rigo G, Ayaydin F, Tietz O, Zsigmond L, Kovacs H, Pay A, Salchert K, Darula Z, Medzihradszky KF, Szabados L, Palme K, Koncz C, Cseplo A (2013) Inactivation of plasma membrane-localized CDPK-RELATED KINASE5 decelerates PIN2 exocytosis and root gravitropic response in Arabidopsis. Plant Cell 25, 1592-1608.
129. Robatzek S, Chinchilla D, Boller T (2006) Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis. Genes Dev. 20, 537-542.
130. Robinson DG, Jiang L, Schumacher K (2008) The endosomal system of plants: Charting new and familiar territories. Plant Physiol. 147, 1482-1492.
131. Rodriguez-Boulan E, Powell SK (1992) Polarity of epithelial and neuronal cells. Annu. Rev. Cell Biol. 8, 395-427.
132. Sabatini S, Beis D, Wolkenfelt H, Murfett J, Guilfoyle T, Malamy J, Benfey P, Leyser O, Bechtold N, Weisbeek P, Scheres B (1999) An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99, 463-472.
133. Sauer M, Balla J, Luschnig C, Wisniewska J, Reinohl V, Friml J, Benkova E (2006) Canalization of auxin flow by Aux/IAA-ARF-dependent feedback regulation of PIN polarity. Genes Dev. 20, 2902-2911.
134. Sawchuk MG, Edgar A, Scarpella E (2013) Patterning of leaf vein networks by convergent auxin transport pathways. PLoS Genet. 9, e1003294.
135. Schulze B, Mentzel T, Jehle AK, Mueller K, Beeler S, Boller T, Felix G, Chinchilla D (2010) Rapid heteromerization and phosphorylation of ligand-activated plant transmembrane receptors and their associated kinase BAK1. J. Biol. Chem. 285, 9444-9451.
136. Schwessinger B, Roux M, Kadota Y, Ntoukakis V, Sklenar J, Jones A, Zipfel C (2011) Phosphorylation-dependent differential regulation of plant growth, cell death, and innate immunity by the regulatory receptor-like kinase BAK1. PLoS Genet. 7, e1002046.
137. Setty SR, Tenza D, Truschel ST, Chou E, Sviderskaya EV, Theos AC, Lamoreux ML, Di Pietro SM, Starcevic M, Bennett DC, Dell'Angelica EC, Raposo G, Marks MS (2007) BLOC-1 is required for cargo-specific sorting from vacuolar early endosomes toward lysosome-related organelles. Mol. Biol. Cell 18, 768-780.
138. Shah K, Russinova E, Gadella TW, Jr., Willemse J, de Vries SC (2002) The Arabidopsis kinase-associated protein phosphatase controls internalization of the somatic embryogenesis receptor kinase 1. Genes Dev. 16, 1707-1720.
139. 2+ entry. Nature 499, 238-242.
140. Shewan AM, Marsh BJ, Melvin DR, Martin S, Gould GW, James DE (2000) The cytosolic C-terminus of the glucose transporter GLUT4 contains an acidic cluster endosomal targeting motif distal to the dileucine signal. Biochem. J. 350, 99-107.
141. Shirakawa M, Ueda H, Shimada T, Nishiyama C, Hara-Nishimura I (2009) Vacuolar SNAREs function in the formation of the leaf vascular network by regulating auxin distribution. Plant Cell Physiol. 50, 1319-1328.
142. Sigismund S, Argenzio E, Tosoni D, Cavallaro E, Polo S, Di Fiore PP (2008) Clathrin-mediated internalization is essential for sustained EGFR signaling but dispensable for degradation. Dev. Cell 15, 209-219.
143. Sigismund S, Woelk T, Puri C, Maspero E, Tacchetti C, Transidico P, Di Fiore PP, Polo S (2005) Clathrin-independent endocytosis of ubiquitinated cargos. Proc. Natl. Acad. Sci. USA 102, 2760-2765.
144. Skirpan A, Culler AH, Gallavotti A, Jackson D, Cohen JD, McSteen P (2009) BARREN INFLORESCENCE2 interaction with ZmPIN1a suggests a role in auxin transport during maize inflorescence development. Plant Cell Physiol. 50, 652-657.
145. Song W, Bomsel M, Casanova J, Vaerman JP, Mostov K (1994) Stimulation of transcytosis of the polymeric immunoglobulin receptor by dimeric IgA. Proc. Natl. Acad. Sci. USA 91, 163-166.
146. Steinborn K, Maulbetsch C, Priester B, Trautmann S, Pacher T, Geiges B, Kuttner F, Lepiniec L, Stierhof YD, Schwarz H, Jürgens G, Mayer U (2002) The Arabidopsis PILZ group genes encode tubulin-folding cofactor orthologs required for cell division but not cell growth. Genes Dev. 16, 959-971.
147. Steiner JA, Carneiro AM, Blakely RD (2008) Going with the flow: Trafficking-dependent and -independent regulation of serotonin transport. Traffic 9, 1393-1402.
148. Steinmann T, Geldner N, Grebe M, Mangold S, Jackson CL, Paris S, Galweiler L, Palme K, Jürgens G (1999) Coordinated polar localization of auxin efflux carrier PIN1 by GNOM ARF GEF. Science 286, 316-318.
149. Sukumar P, Edwards KS, Rahman A, Delong A, Muday GK (2009) PINOID kinase regulates root gravitropism through modulation of PIN2-dependent basipetal auxin transport in Arabidopsis thaliana. Plant Physiol. 150, 722-735.
150. Takano J, Tanaka M, Toyoda A, Miwa K, Kasai K, Fuji K, Onouchi H, Naito S, Fujiwara T (2010) Polar localization and degradation of Arabidopsis boron transporters through distinct trafficking pathways. Proc. Natl. Acad. Sci. USA 107, 5220-5225.
151. Tamma G, Robben JH, Trimpert C, Boone M, Deen PM (2011) Regulation of AQP2 localization by S256 and S261 phosphorylation and ubiquitination. Am. J. Physiol. Cell Physiol. 300, C636-C646.
152. Tanaka H, Dhonukshe P, Brewer PB, Friml J (2006) Spatiotemporal asymmetric auxin distribution: A means to coordinate plant development. Cell Mol. Life Sci. 63, 2738-2754.
153. Tanaka H, Kitakura S, Rakusova H, Uemura T, Feraru MI, De RR, Robert S, Kakimoto T, Friml J (2013) Cell Polarity and patterning by PIN trafficking through early endosomal compartments in Arabidopsis thaliana. PLoS Genet. 9, e1003540.
154. Treml BS, Winderl S, Radykewicz R, Herz M, Schweizer G, Hutzler P, Glawischnig E, Ruiz RA (2005) The gene ENHANCER OF PINOID controls cotyledon development in the Arabidopsis embryo. Development 132, 4063-4074.
155. Tse YC, Mo B, Hillmer S, Zhao M, Lo SW, Robinson DG, Jiang L (2004) Identification of multivesicular bodies as prevacuolar compartments in Nicotiana tabacum BY-2 cells. Plant Cell 16, 672-693.
156. Tuma P, Hubbard AL (2003) Transcytosis: Crossing cellular barriers. Physiol. Rev. 83, 871-932.
157. van Balkom BW, Savelkoul PJ, Markovich D, Hofman E, Nielsen S, van der SP, Deen PM (2002) The role of putative phosphorylation sites in the targeting and shuttling of the aquaporin-2 water channel. J. Biol. Chem. 277, 41473-41479.
158. Vanneste S, Friml J (2009) Auxin: A trigger for change in plant development. Cell 136, 1005-1016.
159. Verhey KJ, Yeh JI, Birnbaum MJ (1995) Distinct signals in the GLUT4 glucose transporter for internalization and for targeting to an insulin-responsive compartment. J. Cell Biol. 130, 1071-1079.
160. Viotti C, Bubeck J, Stierhof YD, Krebs M, Langhans M, van den Berg W, van DW, Richter S, Geldner N, Takano J, Jürgens G, de Vries SC, Robinson DG, Schumacher K (2010) Endocytic and secretory traffic in Arabidopsis merge in the trans-Golgi network/early endosome, an independent and highly dynamic organelle. Plant Cell 22, 1344-1357.
161. Wabnik K, Kleine-Vehn J, Govaerts W, Friml J (2011) Prototype cell-to-cell auxin transport mechanism by intracellular auxin compartmentalization. Trends Plant Sci. 16, 468-475.
162. Wiley HS (2003) Trafficking of the ErbB receptors and its influence on signaling. Exp. Cell Res. 284, 78-88.
163. Willige BC, Ahlers S, Zourelidou M, Barbosa IC, Demarsy E, Trevisan M, Davis PA, Roelfsema MR, Hangarter R, Fankhauser C, Schwechheimer C (2013) D6PK AGCVIII kinases are required for auxin transport and phototropic hypocotyl bending in Arabidopsis. Plant Cell 25, 1674-1688.
164. Wisniewska J, Xu J, Seifertova D, Brewer PB, Ruzicka K, Blilou I, Rouquie D, Benkova E, Scheres B, Friml J (2006) Polar PIN localization directs auxin flow in plants. Science 312, 883.
165. Yalovsky S, Bloch D, Sorek N, Kost B (2008) Regulation of membrane trafficking, cytoskeleton dynamics, and cell polarity by ROP/RAC GTPases. Plant Physiol. 147, 1527-1543.
166. Yang H, Murphy AS (2009) Functional expression and characterization of Arabidopsis ABCB, AUX 1 and PIN auxin transporters in Schizosaccharomyces pombe. Plant J. 59, 179-191.
167. Yui N, Lu HA, Chen Y, Nomura N, Bouley R, Brown D (2013) Basolateral targeting and microtubule-dependent transcytosis of the aquaporin-2 water channel. Am. J. Physiol. Cell Physiol. 304, C38-C48.
168. Yui N, Lu HJ, Bouley R, Brown D (2012) AQP2 is necessary for vasopressin- and forskolin-mediated filamentous actin depolymerization in renal epithelial cells. Biol. Open. 1, 101-108.
169. 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.
170. Zhang J, Nodzynski T, Pencik A, Rolcik J, Friml J (2010) PIN phosphorylation is sufficient to mediate PIN polarity and direct auxin transport. Proc. Natl. Acad. Sci. USA 107, 918-922.
171. Zhang Z, Thomma BP (2013) Structure-function aspects of extracellular leucine-rich repeat-containing cell surface receptors in plants. J. Integr. Plant Biol. doi: 10.1111/jipb.12080
172. Zhong Q, Lazar CS, Tronchere H, Sato T, Meerloo T, Yeo M, Songyang Z, Emr SD, Gill GN (2002) Endosomal localization and function of sorting nexin 1. Proc. Natl. Acad. Sci. USA 99, 6767-6772.
173. Zourelidou M, Muller I, Willige BC, Nill C, Jikumaru Y, Li H, Schwechheimer C (2009) The polarly localized D6 PROTEIN KINASE is required for efficient auxin transport in Arabidopsis thaliana. Development 136, 627-636.
174. Zwiewka M, Feraru E, Moller B, Hwang I, Feraru MI, Kleine-Vehn J, Weijers D, Friml J (2011) The AP-3 adaptor complex is required for vacuolar function in Arabidopsis. Cell Res. 12, 1711-1722.