Current Genetics

, Volume 59, Issue 4, pp 207–230 | Cite as

Endocytic regulation of alkali metal transport proteins in mammals, yeast and plants

  • José Miguel Mulet
  • Vicent Llopis-Torregrosa
  • Cecilia Primo
  • Mª Carmen Marqués
  • Lynne Yenush
Research Article

Abstract

The relative concentrations of ions and solutes inside cells are actively maintained by several classes of transport proteins, in many cases against their concentration gradient. These transport processes, which consume a large portion of cellular energy, must be constantly regulated. Many structurally distinct families of channels, carriers, and pumps have been characterized in considerable detail during the past decades and defects in the function of some of these proteins have been linked to a growing list of human diseases. The dynamic regulation of the transport proteins present at the cell surface is vital for both normal cellular function and for the successful adaptation to changing environments. The composition of proteins present at the cell surface is controlled on both the transcriptional and post-translational level. Post-translational regulation involves highly conserved mechanisms of phosphorylation- and ubiquitylation-dependent signal transduction routes used to modify the cohort of receptors and transport proteins present under any given circumstances. In this review, we will summarize what is currently known about one facet of this regulatory process: the endocytic regulation of alkali metal transport proteins. The physiological relevance, major contributors, parallels and missing pieces of the puzzle in mammals, yeast and plants will be discussed.

Keywords

Ion homeostasis Endocytic regulation Ubiquitylation ESCRT 

References

  1. Abe F, Iida H (2003) Pressure-induced differential regulation of the two tryptophan permeases Tat1 and Tat2 by ubiquitin ligase Rsp5 and its binding proteins, Bul1 and Bul2. Mol Cell Biol 23:7566–7584PubMedGoogle Scholar
  2. Abriel H, Loffing J, Rebhun JF, Pratt JH, Schild L, Horisberger JD, Rotin D, Staub O (1999) Defective regulation of the epithelial Na+ channel by Nedd4 in Liddle’s syndrome. J Clin Invest 103:667–673. doi:10.1172/JCI5713 PubMedGoogle Scholar
  3. Alesutan I, Munoz C, Sopjani M, Dërmaku-Sopjani M, Michael D, Fraser S, Kemp BE, Seebohm G, Föller M, Lang F (2011) Inhibition of Kir2.1 (KCNJ2) by the AMP-activated protein kinase. Biochem Biophys Res Commun 408:505–510. doi:10.1016/j.bbrc.2011.04.015 PubMedGoogle Scholar
  4. Alvarez CE (2008) On the origins of arrestin and rhodopsin. BMC Evol Biol 8:222. doi:10.1186/1471-2148-8-222 PubMedGoogle Scholar
  5. Amerik AY, Nowak J, Swaminathan S, Hochstrasser M (2000) The Doa4 deubiquitinating enzyme is functionally linked to the vacuolar protein-sorting and endocytic pathways. Mol Biol Cell 11:3365–3380PubMedGoogle Scholar
  6. Anderson JA, Huprikar SS, Kochian LV, Lucas WJ, Gaber RF (1992) Functional expression of a probable Arabidopsis thaliana potassium channel in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 89:3736–3740PubMedGoogle Scholar
  7. Anderson JA, Nakamura RL, Gaber RF (1994) Heterologous expression of K+ channels in Saccharomyces cerevisiae: strategies for molecular analysis of structure and function. Symp Soc Exp Biol 48:85–97PubMedGoogle Scholar
  8. Aniento F, Gu F, Parton RG, Gruenberg J (1996) An endosomal beta COP is involved in the pH-dependent formation of transport vesicles destined for late endosomes. J Cell Biol 133:29–41PubMedGoogle Scholar
  9. Apse MP, Aharon GS, Snedden WA, Blumwald E (1999) Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science 285:1256–1258PubMedGoogle Scholar
  10. Arino J, Ramos J, Sychrova H (2010) Alkali metal cation transport and homeostasis in yeasts. Microbiol mol biol rev 74:95–120. doi:10.1128/mmbr.00042-09 PubMedGoogle Scholar
  11. Arnason TG, Pisclevich MG, Dash MD, Davies GF, Harkness TA (2005) Novel interaction between Apc5p and Rsp5p in an intracellular signaling pathway in Saccharomyces cerevisiae. Eukaryot Cell 4:134–146. doi:10.1128/EC.4.1.134-146.2005 PubMedGoogle Scholar
  12. Arroyo JP, Lagnaz D, Ronzaud C, Vázquez N, Ko BS, Moddes L, Ruffieux-Daidié D, Hausel P, Koesters R, Yang B, Stokes JB, Hoover RS, Gamba G, Staub O (2011) Nedd4-2 modulates renal Na+ –Cl– cotransporter via the aldosterone-SGK1-Nedd4-2 pathway. J Am Soc Nephrol 22:1707–1719. doi:10.1681/ASN.2011020132 PubMedGoogle Scholar
  13. Azmi IF, Davies BA, Xiao J, Babst M, Xu Z, Katzmann DJ (2008) ESCRT-III family members stimulate Vps4 ATPase activity directly or via Vta1. Dev Cell 14:50–61. doi:10.1016/j.devcel.2007.10.021 PubMedGoogle Scholar
  14. Babst M, Katzmann DJ, Estepa-Sabal EJ, Meerloo T, Emr SD (2002a) Escrt-III: an endosome-associated heterooligomeric protein complex required for mvb sorting. Dev Cell 3:271–282PubMedGoogle Scholar
  15. Babst M, Katzmann DJ, Snyder WB, Wendland B, Emr SD (2002b) Endosome-associated complex, ESCRT-II, recruits transport machinery for protein sorting at the multivesicular body. Dev Cell 3:283–289PubMedGoogle Scholar
  16. Bache KG, Slagsvold T, Cabezas A, Rosendal KR, Raiborg C, Stenmark H (2004) The growth-regulatory protein HCRP1/hVps37A is a subunit of mammalian ESCRT-I and mediates receptor down-regulation. Mol Biol Cell 15:4337–4346. doi:10.1091/mbc.E04-03-0250 PubMedGoogle Scholar
  17. Baietti MF, Zhang Z, Mortier E, Melchior A, Degeest G, Geeraerts A, Ivarsson Y, Depoortere F, Coomans C, Vermeiren E, Zimmermann P, David G (2012) Syndecan-syntenin-ALIX regulates the biogenesis of exosomes. Nat Cell Biol 14:677–685. doi:10.1038/ncb2502 PubMedGoogle Scholar
  18. Barajas D, Nagy PD (2010) Ubiquitination of tombusvirus p33 replication protein plays a role in virus replication and binding to the host Vps23p ESCRT protein. Virology 397:358–368. doi:10.1016/j.virol.2009.11.010 PubMedGoogle Scholar
  19. Barajas D, Jiang Y, Nagy PD (2009) A unique role for the host ESCRT proteins in replication of Tomato bushy stunt virus. PLoS Pathog 5:e1000705. doi:10.1371/journal.ppat.1000705 PubMedGoogle Scholar
  20. Barberon M, Zelazny E, Robert S, Conéjéro G, Curie C, Friml J, Vert G (2011) Monoubiquitin-dependent endocytosis of the iron-regulated transporter 1 (IRT1) transporter controls iron uptake in plants. Proc Natl Acad Sci USA 108:E450–E458. doi:10.1073/pnas.1100659108 PubMedGoogle Scholar
  21. Barragán V, Leidi EO, Andrés Z, Rubio L, De Luca A, Fernández JA, Cubero B, Pardo JM (2012) Ion exchangers NHX1 and NHX2 mediate active potassium uptake into vacuoles to regulate cell turgor and stomatal function in Arabidopsis. Plant Cell 24:1127–1142. doi:10.1105/tpc.111.095273 PubMedGoogle Scholar
  22. Bassil E, Ohto MA, Esumi T, Tajima H, Zhu Z, Cagnac O, Belmonte M, Peleg Z, Yamaguchi T, Blumwald E (2011) The Arabidopsis intracellular Na+/H+ antiporters NHX5 and NHX6 are endosome associated and necessary for plant growth and development. Plant Cell 23:224–239. doi:10.1105/tpc.110.079426 PubMedGoogle Scholar
  23. Beaudenon SL, Huacani MR, Wang G, McDonnell DP, Huibregtse JM (1999) Rsp5 ubiquitin-protein ligase mediates DNA damage-induced degradation of the large subunit of RNA polymerase II in Saccharomyces cerevisiae. Mol Cell Biol 19:6972–6979PubMedGoogle Scholar
  24. Becuwe M, Vieira N, Lara D, Gomes-Rezende J, Soares-Cunha C, Casal M, Haguenauer-Tsapis R, Vincent O, Paiva S, Léon S (2012) A molecular switch on an arrestin-like protein relays glucose signaling to transporter endocytosis. J Cell Biol 196:247–259. doi:10.1083/jcb.201109113 PubMedGoogle Scholar
  25. Belgareh-Touzé N, Léon S, Erpapazoglou Z, Stawiecka-Mirota M, Urban-Grimal D, Haguenauer-Tsapis R (2008) Versatile role of the yeast ubiquitin ligase Rsp5p in intracellular trafficking. Biochem Soc Trans 36:791–796. doi:10.1042/BST0360791 PubMedGoogle Scholar
  26. Bhalla V, Oyster NM, Fitch AC, Wijngaarden MA, Neumann D, Schlattner U, Pearce D, Hallows KR (2006) AMP-activated kinase inhibits the epithelial Na+ channel through functional regulation of the ubiquitin ligase Nedd4-2. J Biol Chem 281:26159–26169. doi:10.1074/jbc.M606045200 PubMedGoogle Scholar
  27. Blondel MO, Morvan J, Dupre S, Urban-Grimal D, Haguenauer-Tsapis R, Volland C (2004) Direct sorting of the yeast uracil permease to the endosomal system is controlled by uracil binding and Rsp5p-dependent ubiquitylation. Mol Biol Cell 15:883–895. doi:10.1091/mbc.E03-04-0202 PubMedGoogle Scholar
  28. Boase NA, Rychkov GY, Townley SL, Dinudom A, Candi E, Voss AK, Tsoutsman T, Semsarian C, Melino G, Koentgen F, Cook DI, Kumar S (2011) Respiratory distress and perinatal lethality in Nedd4-2-deficient mice. Nat Commun 2:287. doi:10.1038/ncomms1284 PubMedGoogle Scholar
  29. Boehmer C, Laufer J, Jeyaraj S, Klaus F, Lindner R, Lang F, Palmada M (2008) Modulation of the voltage-gated potassium channel Kv1.5 by the SGK1 protein kinase involves inhibition of channel ubiquitination. Cell Physiol Biochem 22:591–600. doi:10.1159/000185543 PubMedGoogle Scholar
  30. Bonifacino JS, Traub LM (2003) Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu Rev Biochem 72:395–447. doi:10.1146/annurev.biochem.72.121801.161800 PubMedGoogle Scholar
  31. Bowers K, Levi BP, Patel FI, Stevens TH (2000) The sodium/proton exchanger Nhx1p is required for endosomal protein trafficking in the yeast Saccharomyces cerevisiae. Mol Biol Cell 11:4277–4294PubMedGoogle Scholar
  32. Brett CL, Tukaye DN, Mukherjee S, Rao R (2005) The yeast endosomal Na+K+/H+ exchanger Nhx1 regulates cellular pH to control vesicle trafficking. Mol Biol Cell 16:1396–1405. doi:10.1091/mbc.E04-11-0999 PubMedGoogle Scholar
  33. Cao XR, Lill NL, Boase N, Shi PP, Croucher DR, Shan H, Qu J, Sweezer EM, Place T, Kirby PA, Daly RJ, Kumar S, Yang B (2008) Nedd4 controls animal growth by regulating IGF-1 signaling. Sci Signal 1:ra5. doi:10.1126/scisignal.1160940 PubMedGoogle Scholar
  34. Carrasquillo R, Tian D, Krishna S, Pollak MR, Greka A, Schlöndorff J (2012) SNF8, a member of the ESCRT-II complex, interacts with TRPC6 and enhances its channel activity. BMC Cell Biol 13:33. doi:10.1186/1471-2121-13-33 PubMedGoogle Scholar
  35. Chen L, Hellmann H (2013) Plant E3 Ligases: flexible enzymes in a sessile world1. Mol Plant. doi:10.1093/mp/sst005 Google Scholar
  36. Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nürnberger T, Jones JD, Felix G, Boller T (2007) A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448:497–500. doi:10.1038/nature05999 PubMedGoogle Scholar
  37. Christie KJ, Martinez JA, Zochodne DW (2012) Disruption of E3 ligase NEDD4 in peripheral neurons interrupts axon outgrowth: linkage to PTEN. Mol Cell Neurosci 50:179–192. doi:10.1016/j.mcn.2012.04.006 PubMedGoogle Scholar
  38. Clague MJ, Liu H, Urbé S (2012) Governance of endocytic trafficking and signaling by reversible ubiquitylation. Dev Cell 23:457–467. doi:10.1016/j.devcel.2012.08.011 PubMedGoogle Scholar
  39. Clancy JL, Henderson MJ, Russell AJ, Anderson DW, Bova RJ, Campbell IG, Choong DY, Macdonald GA, Mann GJ, Nolan T, Brady G, Olopade OI, Woollatt E, Davies MJ, Segara D, Hacker NF, Henshall SM, Sutherland RL, Watts CK (2003) EDD, the human orthologue of the hyperplastic discs tumour suppressor gene, is amplified and overexpressed in cancer. Oncogene 22:5070–5081. doi:10.1038/sj.onc.1206775 PubMedGoogle Scholar
  40. Coonrod EM, Stevens TH (2010) The yeast vps class E mutants: the beginning of the molecular genetic analysis of multivesicular body biogenesis. Mol Biol Cell 21:4057–4060. doi:10.1091/mbc.E09-07-0603 PubMedGoogle Scholar
  41. Crespo JL, Daicho K, Ushimaru T, Hall MN (2001) The GATA transcription factors GLN3 and GAT1 link TOR to salt stress in Saccharomyces cerevisiae. J Biol Chem 276:34441–34444. doi:10.1074/jbc.M103601200 PubMedGoogle Scholar
  42. Debonneville C, Flores SY, Kamynina E, Plant PJ, Tauxe C, Thomas MA, Münster C, Chraïbi A, Pratt JH, Horisberger JD, Pearce D, Loffing J, Staub O (2001) Phosphorylation of Nedd4-2 by Sgk1 regulates epithelial Na(+) channel cell surface expression. EMBO J 20:7052–7059. doi:10.1093/emboj/20.24.7052 PubMedGoogle Scholar
  43. Downes BP, Stupar RM, Gingerich DJ, Vierstra RD (2003) The HECT ubiquitin-protein ligase (UPL) family in Arabidopsis: UPL3 has a specific role in trichome development. Plant J 35:729–742PubMedGoogle Scholar
  44. Eisenach C, Chen ZH, Grefen C, Blatt MR (2012) The trafficking protein SYP121 of Arabidopsis connects programmed stomatal closure and K+ channel activity with vegetative growth. Plant J 69:241–251. doi:10.1111/j.1365-313X.2011.04786.x PubMedGoogle Scholar
  45. Ekberg J, Schuetz F, Boase NA, Conroy SJ, Manning J, Kumar S, Poronnik P, Adams DJ (2007) Regulation of the voltage-gated K(+) channels KCNQ2/3 and KCNQ3/5 by ubiquitination. Novel role for Nedd4-2. J Biol Chem 282:12135–12142. doi:10.1074/jbc.M609385200 PubMedGoogle Scholar
  46. Faresse N, Lagnaz D, Debonneville A, Ismailji A, Maillard M, Fejes-Toth G, Náray-Fejes-Tóth A, Staub O (2012) Inducible kidney-specific Sgk1 knockout mice show a salt-losing phenotype. Am J Physiol Renal Physiol 302:F977–F985. doi:10.1152/ajprenal.00535.2011 PubMedGoogle Scholar
  47. Field MC, Gabernet-Castello C, Dacks JB (2007) Reconstructing the evolution of the endocytic system: insights from genomics and molecular cell biology. Adv Exp Med Biol 607:84–96. doi:10.1007/978-0-387-74021-8_7 PubMedGoogle Scholar
  48. Fisk HA, Yaffe MP (1999) A role for ubiquitination in mitochondrial inheritance in Saccharomyces cerevisiae. J Cell Biol 145:1199–1208PubMedGoogle Scholar
  49. Flinn RJ, Yan Y, Goswami S, Parker PJ, Backer JM (2010) The late endosome is essential for mTORC1 signaling. Mol Biol Cell 21:833–841. doi:10.1091/mbc.E09-09-0756 PubMedGoogle Scholar
  50. Fotia AB, Ekberg J, Adams DJ, Cook DI, Poronnik P, Kumar S (2004) Regulation of neuronal voltage-gated sodium channels by the ubiquitin-protein ligases Nedd4 and Nedd4-2. J Biol Chem 279:28930–28935. doi:10.1074/jbc.M402820200 PubMedGoogle Scholar
  51. Futter CE, White IJ (2007) Annexins and endocytosis. Traffic 8:951–958. doi:10.1111/j.1600-0854.2007.00590.x PubMedGoogle Scholar
  52. Gabriely G, Kama R, Gerst JE (2007) Involvement of specific COPI subunits in protein sorting from the late endosome to the vacuole in yeast. Mol Cell Biol 27:526–540. doi:10.1128/MCB.00577-06 PubMedGoogle Scholar
  53. Gajewska B, Shcherbik N, Oficjalska D, Haines DS, Zoladek T (2003) Functional analysis of the human orthologue of the RSP5-encoded ubiquitin protein ligase, hNedd4, in yeast. Curr Genet 43:1–10. doi:10.1007/s00294-003-0371-x PubMedGoogle Scholar
  54. Galan JM, Moreau V, Andre B, Volland C, Haguenauer-Tsapis R (1996) Ubiquitination mediated by the Npi1p/Rsp5p ubiquitin-protein ligase is required for endocytosis of the yeast uracil permease. J Biol Chem 271:10946–10952PubMedGoogle Scholar
  55. Gao T, Liu Z, Wang Y, Cheng H, Yang Q, Guo A, Ren J, Xue Y (2013) UUCD: a family-based database of ubiquitin and ubiquitin-like conjugation. Nucleic Acids Res 41:D445–D451. doi:10.1093/nar/gks1103 PubMedGoogle Scholar
  56. Geldner N (2004) The plant endosomal system—its structure and role in signal transduction and plant development. Planta 219:547–560. doi:10.1007/s00425-004-1302-x PubMedGoogle Scholar
  57. Gitan RS, Eide DJ (2000) Zinc-regulated ubiquitin conjugation signals endocytosis of the yeast ZRT1 zinc transporter. Biochem J 346:329–336. doi:10.1042/0264-6021:3460329 PubMedGoogle Scholar
  58. Gitan RS, Luo H, Rodgers J, Broderius M, Eide D (1998) Zinc-induced inactivation of the yeast ZRT1 zinc transporter occurs through endocytosis and vacuolar degradation. J Biol Chem 273:28617–28624PubMedGoogle Scholar
  59. Gómez-Gómez L, Boller T (2000) FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol Cell 5:1003–1011PubMedGoogle Scholar
  60. Gong X, Chang A (2001) A mutant plasma membrane ATPase, Pma1-10, is defective in stability at the yeast cell surface. Proc Natl Acad Sci USA 98:9104–9109. doi:10.1073/pnas.161282998 PubMedGoogle Scholar
  61. Guo J, Wang T, Li X, Shallow H, Yang T, Li W, Xu J, Fridman MD, Yang X, Zhang S (2012) Cell surface expression of human ether-a-go–go-related gene (hERG) channels is regulated by caveolin-3 protein via the ubiquitin ligase Nedd4-2. J Biol Chem 287:33132–33141. doi:10.1074/jbc.M112.389643 PubMedGoogle Scholar
  62. Gwizdek C, Hobeika M, Kus B, Ossareh-Nazari B, Dargemont C, Rodriguez MS (2005) The mRNA nuclear export factor Hpr1 is regulated by Rsp5-mediated ubiquitylation. J Biol Chem 280:13401–13405. doi:10.1074/jbc.C500040200 PubMedGoogle Scholar
  63. Haas TJ, Sliwinski MK, Martínez DE, Preuss M, Ebine K, Ueda T, Nielsen E, Odorizzi G, Otegui MS (2007) The Arabidopsis AAA ATPase SKD1 is involved in multivesicular endosome function and interacts with its positive regulator LYST-INTERACTING PROTEIN5. Plant Cell 19:1295–1312. doi:10.1105/tpc.106.049346 PubMedGoogle Scholar
  64. Harkness TA, Davies GF, Ramaswamy V, Arnason TG (2002) The ubiquitin-dependent targeting pathway in Saccharomyces cerevisiae plays a critical role in multiple chromatin assembly regulatory steps. Genetics 162:615–632PubMedGoogle Scholar
  65. Hasenbrink G, Schwarzer S, Kolacna L, Ludwig J, Sychrova H, Lichtenberg-Fraté H (2005) Analysis of the mKir2.1 channel activity in potassium influx defective Saccharomyces cerevisiae strains determined as changes in growth characteristics. FEBS Lett 579:1723–1731. doi:10.1016/j.febslet.2005.02.025 PubMedGoogle Scholar
  66. Hatakeyama R, Kamiya M, Takahara T, Maeda T (2010) Endocytosis of the aspartic acid/glutamic acid transporter Dip5 is triggered by substrate-dependent recruitment of the Rsp5 ubiquitin ligase via the arrestin-like protein Aly2. Mol Cell Biol 30:5598–5607. doi:10.1128/MCB.00464-10 PubMedGoogle Scholar
  67. Hayashi M, Fukuzawa T, Sorimachi H, Maeda T (2005) Constitutive activation of the pH-responsive Rim101 pathway in yeast mutants defective in late steps of the MVB/ESCRT pathway. Mol Cell Biol 25:9478–9490. doi:10.1128/mcb.25.21.9478-9490.2005 PubMedGoogle Scholar
  68. He P, Lee SJ, Lin S, Seidler U, Lang F, Fejes-Toth G, Naray-Fejes-Toth A, Yun CC (2011) Serum- and glucocorticoid-induced kinase 3 in recycling endosomes mediates acute activation of Na+/H+ exchanger NHE3 by glucocorticoids. Mol Biol Cell 22:3812–3825. doi:10.1091/mbc.E11-04-0328 PubMedGoogle Scholar
  69. Heese A, Hann DR, Gimenez-Ibanez S, Jones AM, He K, Li J, Schroeder JI, Peck SC, Rathjen JP (2007) The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. Proc Natl Acad Sci USA 104:12217–12222. doi:10.1073/pnas.0705306104 PubMedGoogle Scholar
  70. Hein C, Springael JY, Volland C, Haguenauer-Tsapis R, André B (1995) NPl1, an essential yeast gene involved in induced degradation of Gap1 and Fur4 permeases, encodes the Rsp5 ubiquitin-protein ligase. Mol Microbiol 18:77–87PubMedGoogle Scholar
  71. Henke G, Maier G, Wallisch S, Boehmer C, Lang F (2004) Regulation of the voltage gated K+ channel Kv1.3 by the ubiquitin ligase Nedd4-2 and the serum and glucocorticoid inducible kinase SGK1. J Cell Physiol 199:194–199. doi:10.1002/jcp.10430 PubMedGoogle Scholar
  72. Herberth S, Shahriari M, Bruderek M, Hessner F, Müller B, Hülskamp M, Schellmann S (2012) Artificial ubiquitylation is sufficient for sorting of a plasma membrane ATPase to the vacuolar lumen of Arabidopsis cells. Planta 236:63–77. doi:10.1007/s00425-012-1587-0 PubMedGoogle Scholar
  73. Hicke L, Dunn R (2003) Regulation of membrane protein transport by ubiquitin and ubiquitin-binding proteins. Annu Rev Cell Dev Biol 19:141–172. doi:10.1146/annurev.cellbio.19.110701.154617 PubMedGoogle Scholar
  74. Hicke L, Riezman H (1996) Ubiquitination of a yeast plasma membrane receptor signals its ligand-stimulated endocytosis. Cell 84:277–287PubMedGoogle Scholar
  75. Hicke L, Zanolari B, Riezman H (1998) Cytoplasmic tail phosphorylation of the alpha-factor receptor is required for its ubiquitination and internalization. J Cell Biol 141:349–358PubMedGoogle Scholar
  76. Hoppe T, Matuschewski K, Rape M, Schlenker S, Ulrich HD, Jentsch S (2000) Activation of a membrane-bound transcription factor by regulated ubiquitin/proteasome-dependent processing. Cell 102:577–586PubMedGoogle Scholar
  77. Hsu C, Morohashi Y, Yoshimura S, Manrique-Hoyos N, Jung S, Lauterbach MA, Bakhti M, Grønborg M, Möbius W, Rhee J, Barr FA, Simons M (2010) Regulation of exosome secretion by Rab35 and its GTPase-activating proteins TBC1D10A-C. J Cell Biol 189:223–232. doi:10.1083/jcb.200911018 PubMedGoogle Scholar
  78. Hu G, Caza M, Cadieux B, Chan V, Liu V, Kronstad J (2013) Cryptococcus neoformans requires the ESCRT protein Vps23 for iron acquisition from heme, for capsule formation, and for virulence. Infect Immun 81:292–302. doi:10.1128/IAI.01037-12 PubMedGoogle Scholar
  79. Huang F, Kirkpatrick D, Jiang X, Gygi S, Sorkin A (2006) Differential regulation of EGF receptor internalization and degradation by multiubiquitination within the kinase domain. Mol Cell 21:737–748. doi:10.1016/j.molcel.2006.02.018 PubMedGoogle Scholar
  80. Huang F, Goh LK, Sorkin A (2007) EGF receptor ubiquitination is not necessary for its internalization. Proc Natl Acad Sci USA 104:16904–16909. doi:10.1073/pnas.0707416104 PubMedGoogle Scholar
  81. Huibregtse JM, Scheffner M, Beaudenon S, Howley PM (1995) A family of proteins structurally and functionally related to the E6-AP ubiquitin-protein ligase. Proc Natl Acad Sci USA 92:2563–2567PubMedGoogle Scholar
  82. Hurst AC, Meckel T, Tayefeh S, Thiel G, Homann U (2004) Trafficking of the plant potassium inward rectifier KAT1 in guard cell protoplasts of Vicia faba. Plant J 37:391–397PubMedGoogle Scholar
  83. Husnjak K, Dikic I (2012) Ubiquitin-binding proteins: decoders of ubiquitin-mediated cellular functions. Annu Rev Biochem 81:291–322. doi:10.1146/annurev-biochem-051810-094654 PubMedGoogle Scholar
  84. Ibl V, Csaszar E, Schlager N, Neubert S, Spitzer C, Hauser MT (2012) Interactome of the plant-specific ESCRT-III component AtVPS2.2 in Arabidopsis thaliana. J Proteome Res 11:397–411. doi:10.1021/pr200845n PubMedGoogle Scholar
  85. Ichimura T, Yamamura H, Sasamoto K, Tominaga Y, Taoka M, Kakiuchi K, Shinkawa T, Takahashi N, Shimada S, Isobe T (2005) 14-3-3 proteins modulate the expression of epithelial Na + channels by phosphorylation-dependent interaction with Nedd4-2 ubiquitin ligase. J Biol Chem 280:13187–13194. doi:10.1074/jbc.M412884200 PubMedGoogle Scholar
  86. Jegla TJ, Zmasek CM, Batalov S, Nayak SK (2009) Evolution of the human ion channel set. Comb Chem High Throughput Screen 12:2–23PubMedGoogle Scholar
  87. Jenness DD, Li Y, Tipper C, Spatrick P (1997) Elimination of defective alpha-factor pheromone receptors. Mol Cell Biol 17:6236–6245PubMedGoogle Scholar
  88. Jespersen T, Membrez M, Nicolas CS, Pitard B, Staub O, Olesen SP, Baró I, Abriel H (2007) The KCNQ1 potassium channel is down-regulated by ubiquitylating enzymes of the Nedd4/Nedd4-like family. Cardiovasc Res 74:64–74. doi:10.1016/j.cardiores.2007.01.008 PubMedGoogle Scholar
  89. Jolliffe CN, Harvey KF, Haines BP, Parasivam G, Kumar S (2000) Identification of multiple proteins expressed in murine embryos as binding partners for the WW domains of the ubiquitin-protein ligase Nedd4. Biochem J 351(Pt 3):557–565PubMedGoogle Scholar
  90. Kallay LM, Brett CL, Tukaye DN, Wemmer MA, Chyou A, Odorizzi G, Rao R (2011) Endosomal Na+(K+)/H+ exchanger Nhx1/Vps44 functions independently and downstream of multivesicular body formation. J Biol Chem 286:44067–44077. doi:10.1074/jbc.M111.282319 PubMedGoogle Scholar
  91. Kamsteeg EJ, Savelkoul PJ, Hendriks G, Konings IB, Nivillac NM, Lagendijk AK, van der Sluijs P, Deen PM (2008) Missorting of the Aquaporin-2 mutant E258K to multivesicular bodies/lysosomes in dominant NDI is associated with its monoubiquitination and increased phosphorylation by PKC but is due to the loss of E258. Pflugers Arch 455:1041–1054. doi:10.1007/s00424-007-0364-6 PubMedGoogle Scholar
  92. Kamynina E, Debonneville C, Bens M, Vandewalle A, Staub O (2001) A novel mouse Nedd4 protein suppresses the activity of the epithelial Na+ channel. FASEB J 15:204–214. doi:10.1096/fj.00-0191com PubMedGoogle Scholar
  93. Kasai K, Takano J, Miwa K, Toyoda A, Fujiwara T (2011) High boron-induced ubiquitination regulates vacuolar sorting of the BOR1 borate transporter in Arabidopsis thaliana. J Biol Chem 286:6175–6183. doi:10.1074/jbc.M110.184929 PubMedGoogle Scholar
  94. Katzmann DJ, Babst M, Emr SD (2001) Ubiquitin-dependent sorting into the multivesicular body pathway requires the function of a conserved endosomal protein sorting complex, ESCRT-I. Cell 106:145–155PubMedGoogle Scholar
  95. Katzmann DJ, Stefan CJ, Babst M, Emr SD (2003) Vps27 recruits ESCRT machinery to endosomes during MVB sorting. J Cell Biol 162:413–423. doi:10.1083/jcb.200302136 PubMedGoogle Scholar
  96. Kim JM, Wu H, Green G, Winkler CA, Kopp JB, Miner JH, Unanue ER, Shaw AS (2003) CD2-associated protein haploinsufficiency is linked to glomerular disease susceptibility. Science 300:1298–1300. doi:10.1126/science.1081068 PubMedGoogle Scholar
  97. Kim TH, Böhmer M, Hu H, Nishimura N, Schroeder JI (2010) Guard cell signal transduction network: advances in understanding abscisic acid, CO2, and Ca2+signaling. Annu Rev Plant Biol 61:561–591. doi:10.1146/annurev-arplant-042809-112226 PubMedGoogle Scholar
  98. Kölling R, Hollenberg CP (1994) The ABC-transporter Ste6 accumulates in the plasma membrane in a ubiquitinated form in endocytosis mutants. EMBO J 13:3261–3271PubMedGoogle Scholar
  99. Komander D, Rape M (2012) The ubiquitin code. Annu Rev Biochem 81:203–229. doi:10.1146/annurev-biochem-060310-170328 PubMedGoogle Scholar
  100. Kulathu Y, Komander D (2012) Atypical ubiquitylation—the unexplored world of polyubiquitin beyond Lys48 and Lys63 linkages. Nat Rev Mol Cell Biol 13:508–523. doi:10.1038/nrm3394 PubMedGoogle Scholar
  101. Kullmann DM (2010) Neurological channelopathies. Annu Rev Neurosci 33:151–172. doi:10.1146/annurev-neuro-060909-153122 PubMedGoogle Scholar
  102. Kumar S, Tomooka Y, Noda M (1992) Identification of a set of genes with developmentally down-regulated expression in the mouse brain. Biochem Biophys Res Commun 185:1155–1161PubMedGoogle Scholar
  103. Kumar S, Harvey KF, Kinoshita M, Copeland NG, Noda M, Jenkins NA (1997) cDNA cloning, expression analysis, and mapping of the mouse Nedd4 gene. Genomics 40:435–443. doi:10.1006/geno.1996.4582 PubMedGoogle Scholar
  104. Lafaurie-Janvore J, Maiuri P, Wang I, Pinot M, Manneville JB, Betz T, Balland M, Piel M (2013) ESCRT-III assembly and cytokinetic abscission are induced by tension release in the intercellular bridge. Science 339:1625–1629. doi:10.1126/science.1233866 PubMedGoogle Scholar
  105. Lam SK, Siu CL, Hillmer S, Jang S, An G, Robinson DG, Jiang L (2007) Rice SCAMP1 defines clathrin-coated, trans-golgi-located tubular-vesicular structures as an early endosome in tobacco BY-2 cells. Plant Cell 19:296–319. doi:10.1105/tpc.106.045708 PubMedGoogle Scholar
  106. Lamothe S, Zhang S (2013) The Serum- and Glucocorticoid-Inducible Kinase SGK1 and SGK3 Regulate hERG Channel Expression via Ubiquitin Ligase Nedd4-2 and GTPase Rab11. J Biol Chem. doi:10.1074/jbc.M113.453670 PubMedGoogle Scholar
  107. Langelier C, von Schwedler UK, Fisher RD, De Domenico I, White PL, Hill CP, Kaplan J, Ward D, Sundquist WI (2006) Human ESCRT-II complex and its role in human immunodeficiency virus type 1 release. J Virol 80:9465–9480. doi:10.1128/JVI.01049-06 PubMedGoogle Scholar
  108. Lauwers E, Erpapazoglou Z, Haguenauer-Tsapis R, André B (2010) The ubiquitin code of yeast permease trafficking. Trends Cell Biol 20:196–204. doi:10.1016/j.tcb.2010.01.004 PubMedGoogle Scholar
  109. Lawrence SP, Bright NA, Luzio JP, Bowers K (2010) The sodium/proton exchanger NHE8 regulates late endosomal morphology and function. Mol Biol Cell 21:3540–3551. doi:10.1091/mbc.E09-12-1053 PubMedGoogle Scholar
  110. Lee KB, Ptasienski JA, Bunemann M, Hosey MM (2000) Acidic amino acids flanking phosphorylation sites in the M2 muscarinic receptor regulate receptor phosphorylation, internalization, and interaction with arrestins. J Biol Chem 275:35767–35777. doi:10.1074/jbc.M002225200 PubMedGoogle Scholar
  111. Lee SM, Chin LS, Li L (2012) Charcot-Marie-Tooth disease-linked protein SIMPLE functions with the ESCRT machinery in endosomal trafficking. J Cell Biol 199:799–816. doi:10.1083/jcb.201204137 PubMedGoogle Scholar
  112. Lefkowitz RJ, Rajagopal K, Whalen EJ (2006) New roles for beta-arrestins in cell signaling: not just for seven-transmembrane receptors. Mol Cell 24:643–652. doi:10.1016/j.molcel.2006.11.007 PubMedGoogle Scholar
  113. Lin CH, MacGurn JA, Chu T, Stefan CJ, Emr SD (2008) Arrestin-related ubiquitin-ligase adaptors regulate endocytosis and protein turnover at the cell surface. Cell 135:714–725. doi:10.1016/j.cell.2008.09.025 PubMedGoogle Scholar
  114. Liu Y, Chang A (2006) Quality control of a mutant plasma membrane ATPase: ubiquitylation prevents cell-surface stability. J Cell Sci 119:360–369. doi:10.1242/jcs.02749 PubMedGoogle Scholar
  115. Liu J, Sitaram A, Burd CG (2007) Regulation of copper-dependent endocytosis and vacuolar degradation of the yeast copper transporter, Ctr1p, by the Rsp5 ubiquitin ligase. Traffic 8:1375–1384. doi:10.1111/j.1600-0854.2007.00616.x PubMedGoogle Scholar
  116. Liu Y, Oppenheim RW, Sugiura Y, Lin W (2009) Abnormal development of the neuromuscular junction in Nedd4-deficient mice. Dev Biol 330:153–166. doi:10.1016/j.ydbio.2009.03.023 PubMedGoogle Scholar
  117. Löfke C, Luschnig C, Kleine-Vehn J (2013) Posttranslational modification and trafficking of PIN auxin efflux carriers. Mech Dev 130:82–94. doi:10.1016/j.mod.2012.02.003 PubMedGoogle Scholar
  118. Lu PJ, Zhou XZ, Shen M, Lu KP (1999) Function of WW domains as phosphoserine- or phosphothreonine-binding modules. Science 283:1325–1328PubMedGoogle Scholar
  119. 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. doi:10.1073/pnas.0909705107 PubMedGoogle Scholar
  120. 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. doi:10.1126/science.1204903 PubMedGoogle Scholar
  121. Luhtala N, Odorizzi G (2004) Bro1 coordinates deubiquitination in the multivesicular body pathway by recruiting Doa4 to endosomes. J Cell Biol 166:717–729. doi:10.1083/jcb.200403139 PubMedGoogle Scholar
  122. MacGurn JA, Hsu PC, Smolka MB, Emr SD (2011) TORC1 regulates endocytosis via Npr1-mediated phosphoinhibition of a ubiquitin ligase adaptor. Cell 147:1104–1117. doi:10.1016/j.cell.2011.09.054 PubMedGoogle Scholar
  123. MacGurn JA, Hsu P-C, Emr SD (2012) Ubiquitin and Membrane Protein Turnover: from Cradle to Grave. Annu Rev Biochem 81(81):231–259. doi:10.1146/annurev-biochem-060210-093619 PubMedGoogle Scholar
  124. Mäser P, Thomine S, Schroeder JI, Ward JM, Hirschi K, Sze H, Talke IN, Amtmann A, Maathuis FJ, Sanders D, Harper JF, Tchieu J, Gribskov M, Persans MW, Salt DE, Kim SA, Guerinot ML (2001) Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiol 126:1646–1667PubMedGoogle Scholar
  125. Mayran N, Parton RG, Gruenberg J (2003) Annexin II regulates multivesicular endosome biogenesis in the degradation pathway of animal cells. EMBO J 22:3242–3253. doi:10.1093/emboj/cdg321 PubMedGoogle Scholar
  126. Meckel T, Hurst AC, Thiel G, Homann U (2004) Endocytosis against high turgor: intact guard cells of Vicia faba constitutively endocytose fluorescently labelled plasma membrane and GFP-tagged K-channel KAT1. Plant J 39:182–193. doi:10.1111/j.1365-313X.2004.02119.x PubMedGoogle Scholar
  127. Merhi A, André B (2012) Internal amino acids promote Gap1 permease ubiquitylation via TORC1/Npr1/14-3-3-dependent control of the Bul arrestin-like adaptors. Mol Cell Biol 32:4510–4522. doi:10.1128/MCB.00463-12 PubMedGoogle Scholar
  128. Metzger MB, Hristova VA, Weissman AM (2012) HECT and RING finger families of E3 ubiquitin ligases at a glance. J Cell Sci 125:531–537. doi:10.1242/jcs.091777 PubMedGoogle Scholar
  129. Miao Y, Zentgraf U (2010) A HECT E3 ubiquitin ligase negatively regulates Arabidopsis leaf senescence through degradation of the transcription factor WRKY53. Plant J 63:179–188. doi:10.1111/j.1365-313X.2010.04233.x PubMedGoogle Scholar
  130. Michelle C, Vourc’h P, Mignon L, Andres CR (2009) What was the set of ubiquitin and ubiquitin-like conjugating enzymes in the eukaryote common ancestor? J Mol Evol 68:616–628. doi:10.1007/s00239-009-9225-6 PubMedGoogle Scholar
  131. Mochida GH, Ganesh VS, de Michelena MI, Dias H, Atabay KD, Kathrein KL, Huang HT, Hill RS, Felie JM, Rakiec D, Gleason D, Hill AD, Malik AN, Barry BJ, Partlow JN, Tan WH, Glader LJ, Barkovich AJ, Dobyns WB, Zon LI, Walsh CA (2012) CHMP1A encodes an essential regulator of BMI1-INK4A in cerebellar development. Nat Genet 44:1260–1264. doi:10.1038/ng.2425 PubMedGoogle Scholar
  132. Morita E, Sandrin V, McCullough J, Katsuyama A, Baci Hamilton I, Sundquist WI (2011) ESCRT-III protein requirements for HIV-1 budding. Cell Host Microbe 9:235–242. doi:10.1016/j.chom.2011.02.004 PubMedGoogle Scholar
  133. Morrione A, Plant P, Valentinis B, Staub O, Kumar S, Rotin D, Baserga R (1999) mGrb10 interacts with Nedd4. J Biol Chem 274:24094–24099PubMedGoogle Scholar
  134. Mulet JM, Martin DE, Loewith R, Hall MN (2006) Mutual antagonism of target of rapamycin and calcineurin signaling. J Biol Chem 281:33000–33007. doi:10.1074/jbc.M604244200 PubMedGoogle Scholar
  135. Murdaca J, Treins C, Monthouël-Kartmann MN, Pontier-Bres R, Kumar S, Van Obberghen E, Giorgetti-Peraldi S (2004) Grb10 prevents Nedd4-mediated vascular endothelial growth factor receptor-2 degradation. J Biol Chem 279:26754–26761. doi:10.1074/jbc.M311802200 PubMedGoogle Scholar
  136. Muzioł T, Pineda-Molina E, Ravelli RB, Zamborlini A, Usami Y, Göttlinger H, Weissenhorn W (2006) Structural basis for budding by the ESCRT-III factor CHMP3. Dev Cell 10:821–830. doi:10.1016/j.devcel.2006.03.013 PubMedGoogle Scholar
  137. Nabhan JF, Pan H, Lu Q (2010) Arrestin domain-containing protein 3 recruits the NEDD4 E3 ligase to mediate ubiquitination of the beta2-adrenergic receptor. EMBO Rep 11:605–611. doi:10.1038/embor.2010.80 PubMedGoogle Scholar
  138. Naik N, Giannini E, Brouchon L, Boulay F (1997) Internalization and recycling of the C5a anaphylatoxin receptor: evidence that the agonist-mediated internalization is modulated by phosphorylation of the C-terminal domain. J Cell Sci 110(Pt 19):2381–2390PubMedGoogle Scholar
  139. Nakamura N, Tanaka S, Teko Y, Mitsui K, Kanazawa H (2005) Four Na+/H+ exchanger isoforms are distributed to Golgi and post-Golgi compartments and are involved in organelle pH regulation. J Biol Chem 280:1561–1572. doi:10.1074/jbc.M410041200 PubMedGoogle Scholar
  140. Nass R, Rao R (1998) Novel localization of a Na+/H+ exchanger in a late endosomal compartment of yeast. Implications for vacuole biogenesis. J Biol Chem 273:21054–21060PubMedGoogle Scholar
  141. Nass R, Cunningham KW, Rao R (1997) Intracellular sequestration of sodium by a novel Na+/H+ exchanger in yeast is enhanced by mutations in the plasma membrane H+-ATPase. Insights into mechanisms of sodium tolerance. J Biol Chem 272:26145–26152PubMedGoogle Scholar
  142. Navarrete C, Petrezselyova S, Barreto L, Martinez JL, Zahradka J, Arino J, Sychrova H, Ramos J (2010) Lack of main K plus uptake systems in Saccharomyces cerevisiae cells affects yeast performance in both potassium-sufficient and potassium-limiting conditions. FEMS Yeast Res 10:508–517. doi:10.1111/j.1567-1364.2010.00630.x PubMedGoogle Scholar
  143. Nickerson DP, West M, Odorizzi G (2006) Did2 coordinates Vps4-mediated dissociation of ESCRT-III from endosomes. J Cell Biol 175:715–720. doi:10.1083/jcb.200606113 PubMedGoogle Scholar
  144. Nijman SM, Luna-Vargas MP, Velds A, Brummelkamp TR, Dirac AM, Sixma TK, Bernards R (2005) A genomic and functional inventory of deubiquitinating enzymes. Cell 123:773–786. doi:10.1016/j.cell.2005.11.007 PubMedGoogle Scholar
  145. Nikko E, Pelham HR (2009) Arrestin-mediated endocytosis of yeast plasma membrane transporters. Traffic 10:1856–1867. doi:10.1111/j.1600-0854.2009.00990.x PubMedGoogle Scholar
  146. Nikko E, Sullivan JA, Pelham HR (2008) Arrestin-like proteins mediate ubiquitination and endocytosis of the yeast metal transporter Smf1. EMBO Rep 9:1216–1221. doi:10.1038/embor.2008.199 PubMedGoogle Scholar
  147. Núñez-Ramírez R, Sánchez-Barrena MJ, Villalta I, Vega JF, Pardo JM, Quintero FJ, Martinez-Salazar J, Albert A (2012) Structural insights on the plant salt-overly-sensitive 1 (SOS1) Na(+)/H(+) antiporter. J Mol Biol 424:283–294. doi:10.1016/j.jmb.2012.09.015 PubMedGoogle Scholar
  148. Obita T, Saksena S, Ghazi-Tabatabai S, Gill DJ, Perisic O, Emr SD, Williams RL (2007) Structural basis for selective recognition of ESCRT-III by the AAA ATPase Vps4. Nature 449:735–739. doi:10.1038/nature06171 PubMedGoogle Scholar
  149. Oliver PM, Cao X, Worthen GS, Shi P, Briones N, MacLeod M, White J, Kirby P, Kappler J, Marrack P, Yang B (2006) Ndfip1 protein promotes the function of itch ubiquitin ligase to prevent T cell activation and T helper 2 cell-mediated inflammation. Immunity 25:929–940. doi:10.1016/j.immuni.2006.10.012 PubMedGoogle Scholar
  150. O’Neill LA (2011) Plant science. Innate immunity in plants goes to the PUB. Science 332:1386–1387. doi:10.1126/science.1208448 PubMedGoogle Scholar
  151. Ostrowski M, Carmo NB, Krumeich S, Fanget I, Raposo G, Savina A, Moita CF, Schauer K, Hume AN, Freitas RP, Goud B, Benaroch P, Hacohen N, Fukuda M, Desnos C, Seabra MC, Darchen F, Amigorena S, Moita LF, Thery C (2010) Rab27a and Rab27b control different steps of the exosome secretion pathway. Nat Cell Biol 12: 19–30; sup pp 11–13. doi:10.1038/ncb2000 Google Scholar
  152. Otegui MS, Spitzer C (2008) Endosomal functions in plants. Traffic 9:1589–1598. doi:10.1111/j.1600-0854.2008.00787.x PubMedGoogle Scholar
  153. Pals-Rylaarsdam R, Hosey MM (1997) Two homologous phosphorylation domains differentially contribute to desensitization and internalization of the m2 muscarinic acetylcholine receptor. J Biol Chem 272:14152–14158PubMedGoogle Scholar
  154. Parikh H, Carlsson E, Chutkow WA, Johansson LE, Storgaard H, Poulsen P, Saxena R, Ladd C, Schulze PC, Mazzini MJ, Jensen CB, Krook A, Björnholm M, Tornqvist H, Zierath JR, Ridderstråle M, Altshuler D, Lee RT, Vaag A, Groop LC, Mootha VK (2007) TXNIP regulates peripheral glucose metabolism in humans. PLoS Med 4:e158. doi:10.1371/journal.pmed.0040158 PubMedGoogle Scholar
  155. Parkinson N, Ince PG, Smith MO, Highley R, Skibinski G, Andersen PM, Morrison KE, Pall HS, Hardiman O, Collinge J, Shaw PJ, Fisher EM, Study MPiA, Consortium F (2006) ALS phenotypes with mutations in CHMP2B (charged multivesicular body protein 2B). Neurology 67:1074–1077. doi:10.1212/01.wnl.0000231510.89311.8b PubMedGoogle Scholar
  156. Patra B, Pattanaik S, Yuan L (2013) Ubiquitin protein ligase 3 mediates the proteasomal degradation of GLABROUS 3 and ENHANCER OF GLABROUS 3, regulators of trichome development and flavonoid biosynthesis in Arabidopsis. Plant J 74:435–447. doi:10.1111/tpj.12132 PubMedGoogle Scholar
  157. Patwari P, Lee RT (2012) An expanded family of arrestins regulate metabolism. Trends Endocrinol Metab 23:216–222. doi:10.1016/j.tem.2012.03.003 PubMedGoogle Scholar
  158. Patwari P, Chutkow WA, Cummings K, Verstraeten VL, Lammerding J, Schreiter ER, Lee RT (2009) Thioredoxin-independent regulation of metabolism by the alpha-arrestin proteins. J Biol Chem 284:24996–25003. doi:10.1074/jbc.M109.018093 PubMedGoogle Scholar
  159. Pawliczek T, Crump CM (2009) Herpes simplex virus type 1 production requires a functional ESCRT-III complex but is independent of TSG101 and ALIX expression. J Virol 83:11254–11264. doi:10.1128/JVI.00574-09 PubMedGoogle Scholar
  160. Peer WA (2011) Plasma membrane protein trafficking. In: Murphy A, Peer W, Schultz B (eds) The plant plasma membrane. Springer-Verlag, Berlin, pp 31–56Google Scholar
  161. Perez-Valle J, Jenkins H, Merchan S, Montiel V, Ramos J, Sharma S, Serrano R, Yenush L (2007) Key role for intracellular K+ and protein kinases Sat4/Hal4 and Ha15 in the plasma membrane stabilization of yeast nutrient transporters. Mol Cell Biol 27:5725–5736. doi:10.1128/mcb.01375-06 PubMedGoogle Scholar
  162. Perez-Valle J, Rothe J, Primo C, Martinez Pastor M, Arino J, Pascual-Ahuir A, Miguel Mulet J, Serrano R, Yenush L (2010) Hal4 and Hal5 protein kinases are required for general control of carbon and nitrogen uptake and metabolism. Eukaryot Cell 9:1881–1890. doi:10.1128/ec.00184-10 PubMedGoogle Scholar
  163. Persaud A, Alberts P, Amsen EM, Xiong X, Wasmuth J, Saadon Z, Fladd C, Parkinson J, Rotin D (2009) Comparison of substrate specificity of the ubiquitin ligases Nedd4 and Nedd4-2 using proteome arrays. Mol Syst Biol 5:333. doi:10.1038/msb.2009.85 PubMedGoogle Scholar
  164. Peruzzi F, Prisco M, Morrione A, Valentinis B, Baserga R (2001) Anti-apoptotic signaling of the insulin-like growth factor-I receptor through mitochondrial translocation of c-Raf and Nedd4. J Biol Chem 276:25990–25996. doi:10.1074/jbc.M103188200 PubMedGoogle Scholar
  165. Philips JA, Porto MC, Wang H, Rubin EJ, Perrimon N (2008) ESCRT factors restrict mycobacterial growth. Proc Natl Acad Sci USA 105:3070–3075. doi:10.1073/pnas.0707206105 PubMedGoogle Scholar
  166. Pickart CM (2004) Back to the future with ubiquitin. Cell 116:181–190PubMedGoogle Scholar
  167. Pizzirusso M, Chang A (2004) Ubiquitin-mediated targeting of a mutant plasma membrane ATPase, Pma1-7, to the endosomal/vacuolar system in yeast. Mol Biol Cell 15:2401–2409. doi:10.1091/mbc.E03-10-0727 PubMedGoogle Scholar
  168. Poteryaev D, Datta S, Ackema K, Zerial M, Spang A (2010) Identification of the switch in early-to-late endosome transition. Cell 141:497–508. doi:10.1016/j.cell.2010.03.011 PubMedGoogle Scholar
  169. Prag G, Watson H, Kim YC, Beach BM, Ghirlando R, Hummer G, Bonifacino JS, Hurley JH (2007) The Vps27/Hse1 complex is a GAT domain-based scaffold for ubiquitin-dependent sorting. Dev Cell 12:973–986. doi:10.1016/j.devcel.2007.04.013 PubMedGoogle Scholar
  170. Qiu QS, Fratti RA (2010) The Na+/H+ exchanger Nhx1p regulates the initiation of Saccharomyces cerevisiae vacuole fusion. J Cell Sci 123:3266–3275. doi:10.1242/jcs.067637 PubMedGoogle Scholar
  171. Quintero FJ, Martinez-Atienza J, Villalta I, Jiang X, Kim WY, Ali Z, Fujii H, Mendoza I, Yun DJ, Zhu JK, Pardo JM (2011) Activation of the plasma membrane Na/H antiporter Salt-Overly-Sensitive 1 (SOS1) by phosphorylation of an auto-inhibitory C-terminal domain. Proc Natl Acad Sci USA 108:2611–2616. doi:10.1073/pnas.1018921108 PubMedGoogle Scholar
  172. Raymond CK, Howald-Stevenson I, Vater CA, Stevens TH (1992) Morphological classification of the yeast vacuolar protein sorting mutants: evidence for a prevacuolar compartment in class E vps mutants. Mol Biol Cell 3:1389–1402PubMedGoogle Scholar
  173. Reid E, Connell J, Edwards TL, Duley S, Brown SE, Sanderson CM (2005) The hereditary spastic paraplegia protein spastin interacts with the ESCRT-III complex-associated endosomal protein CHMP1B. Hum Mol Genet 14:19–38. doi:10.1093/hmg/ddi003 PubMedGoogle Scholar
  174. Reyes FC, Buono R, Otegui MS (2011) Plant endosomal trafficking pathways. Curr Opin Plant Biol 14:666–673. doi:10.1016/j.pbi.2011.07.009 PubMedGoogle Scholar
  175. Robatzek S, Chinchilla D, Boller T (2006) Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis. Genes Dev 20:537–542. doi:10.1101/gad.366506 PubMedGoogle Scholar
  176. Roberg KJ, Rowley N, Kaiser CA (1997) Physiological regulation of membrane protein sorting late in the secretory pathway of Saccharomyces cerevisiae. J Cell Biol 137:1469–1482PubMedGoogle Scholar
  177. Rodriguez MS, Gwizdek C, Haguenauer-Tsapis R, Dargemont C (2003) The HECT ubiquitin ligase Rsp5p is required for proper nuclear export of mRNA in Saccharomyces cerevisiae. Traffic 4:566–575PubMedGoogle Scholar
  178. Rodríguez-Rosales MP, Gálvez FJ, Huertas R, Aranda MN, Baghour M, Cagnac O, Venema K (2009) Plant NHX cation/proton antiporters. Plant Signal Behav 4:265–276PubMedGoogle Scholar
  179. Rolim AL, Lindsey SC, Kunii IS, Fujikawa AM, Soares FA, Chiamolera MI, Maciel RM, Silva MR (2010) Ion channelopathies in endocrinology: recent genetic findings and pathophysiological insights. Arq Bras Endocrinol Metabol 54:673–681PubMedGoogle Scholar
  180. Ronzaud C, Loffing-Cueni D, Hausel P, Debonneville A, Malsure SR, Fowler-Jaeger N, Boase NA, Perrier R, Maillard M, Yang B, Stokes JB, Koesters R, Kumar S, Hummler E, Loffing J, Staub O (2013) Renal tubular NEDD4-2 deficiency causes NCC-mediated salt-dependent hypertension. J Clin Invest 123:657–665. doi:10.1172/JCI61110 PubMedGoogle Scholar
  181. Rotin D, Kumar S (2009) Physiological functions of the HECT family of ubiquitin ligases. Nat Rev Mol Cell Biol 10:398–409. doi:10.1038/nrm2690 PubMedGoogle Scholar
  182. Rotin D, Staub O, Haguenauer-Tsapis R (2000) Ubiquitination and endocytosis of plasma membrane proteins: role of Nedd4/Rsp5p family of ubiquitin-protein ligases. J Membr Biol 176:1–17PubMedGoogle Scholar
  183. Rougier JS, van Bemmelen MX, Bruce MC, Jespersen T, Gavillet B, Apothéloz F, Cordonier S, Staub O, Rotin D, Abriel H (2005) Molecular determinants of voltage-gated sodium channel regulation by the Nedd4/Nedd4-like proteins. Am J Physiol Cell Physiol 288:C692–C701. doi:10.1152/ajpcell.00460.2004 PubMedGoogle Scholar
  184. Rue SM, Mattei S, Saksena S, Emr SD (2008) Novel Ist1-Did2 complex functions at a late step in multivesicular body sorting. Mol Biol Cell 19:475–484. doi:10.1091/mbc.E07-07-0694 PubMedGoogle Scholar
  185. Saksena S, Wahlman J, Teis D, Johnson AE, Emr SD (2009) Functional reconstitution of ESCRT-III assembly and disassembly. Cell 136:97–109. doi:10.1016/j.cell.2008.11.013 PubMedGoogle Scholar
  186. Samson RY, Obita T, Freund SM, Williams RL, Bell SD (2008) A role for the ESCRT system in cell division in archaea. Science 322:1710–1713. doi:10.1126/science.1165322 PubMedGoogle Scholar
  187. Sasaki T, Takagi H (2013) Phosphorylation of a conserved Thr357 in yeast Nedd4-like ubiquitin ligase Rsp5 is involved in down-regulation of the general amino acid permease Gap1. Genes Cells. doi:10.1111/gtc.12049 Google Scholar
  188. Schachtman DP, Schroeder JI, Lucas WJ, Anderson JA, Gaber RF (1992) Expression of an inward-rectifying potassium channel by the Arabidopsis KAT1 cDNA. Science 258:1654–1658PubMedGoogle Scholar
  189. Scheffner M, Huibregtse JM, Vierstra RD, Howley PM (1993) The HPV-16 E6 and E6-AP complex functions as a ubiquitin-protein ligase in the ubiquitination of p53. Cell 75:495–505PubMedGoogle Scholar
  190. Schellmann S, Pimpl P (2009) Coats of endosomal protein sorting: retromer and ESCRT. Curr Opin Plant Biol 12:670–676. doi:10.1016/j.pbi.2009.09.005 PubMedGoogle Scholar
  191. Schuetz F, Kumar S, Poronnik P, Adams DJ (2008) Regulation of the voltage-gated K(+) channels KCNQ2/3 and KCNQ3/5 by serum- and glucocorticoid-regulated kinase-1. Am J Physiol Cell Physiol 295:C73–C80. doi:10.1152/ajpcell.00146.2008 PubMedGoogle Scholar
  192. Schulman BA, Harper JW (2009) Ubiquitin-like protein activation by E1 enzymes: the apex for downstream signalling pathways. Nat Rev Mol Cell Biol 10:319–331. doi:10.1038/nrm2673 PubMedGoogle Scholar
  193. Schwarzer S, Kolacna L, Lichtenberg-Fraté H, Sychrova H, Ludwig J (2008) Functional expression of the voltage-gated neuronal mammalian potassium channel rat ether à go-go1 in yeast. FEMS Yeast Res 8:405–413. doi:10.1111/j.1567-1364.2007.00351.x PubMedGoogle Scholar
  194. Sentenac H, Bonneaud N, Minet M, Lacroute F, Salmon JM, Gaymard F, Grignon C (1992) Cloning and expression in yeast of a plant potassium ion transport system. Science 256:663–665PubMedGoogle Scholar
  195. Shcherbik N, Zoladek T, Nickels JT, Haines DS (2003) Rsp5p is required for ER bound Mga2p120 polyubiquitination and release of the processed/tethered transactivator Mga2p90. Curr Biol 13:1227–1233PubMedGoogle Scholar
  196. Shcherbik N, Kee Y, Lyon N, Huibregtse JM, Haines DS (2004) A single PXY motif located within the carboxyl terminus of Spt23p and Mga2p mediates a physical and functional interaction with ubiquitin ligase Rsp5p. J Biol Chem 279:53892–53898. doi:10.1074/jbc.M410325200 PubMedGoogle Scholar
  197. Shea FF, Rowell JL, Li Y, Chang TH, Alvarez CE (2012) Mammalian alpha arrestins link activated seven transmembrane receptors to Nedd4 family e3 ubiquitin ligases and interact with beta arrestins. PLoS ONE 7:e50557. doi:10.1371/journal.pone.0050557 PubMedGoogle Scholar
  198. Shearwin-Whyatt L, Dalton HE, Foot N, Kumar S (2006) Regulation of functional diversity within the Nedd4 family by accessory and adaptor proteins. BioEssays 28:617–628. doi:10.1002/bies.20422 PubMedGoogle Scholar
  199. Shen B, Li C, Min Z, Meeley RB, Tarczynski MC, Olsen OA (2003) sal1 determines the number of aleurone cell layers in maize endosperm and encodes a class E vacuolar sorting protein. Proc Natl Acad Sci USA 100:6552–6557. doi:10.1073/pnas.0732023100 PubMedGoogle Scholar
  200. Shi PP, Cao XR, Sweezer EM, Kinney TS, Williams NR, Husted RF, Nair R, Weiss RM, Williamson RA, Sigmund CD, Snyder PM, Staub O, Stokes JB, Yang B (2008) Salt-sensitive hypertension and cardiac hypertrophy in mice deficient in the ubiquitin ligase Nedd4-2. Am J Physiol Renal Physiol 295:F462–F470. doi:10.1152/ajprenal.90300.2008 PubMedGoogle Scholar
  201. Shiels A, Bennett TM, Knopf HL, Yamada K, Yoshiura K, Niikawa N, Shim S, Hanson PI (2007) CHMP4B, a novel gene for autosomal dominant cataracts linked to chromosome 20q. Am J Hum Genet 81:596–606. doi:10.1086/519980 PubMedGoogle Scholar
  202. Shimkets RA, Warnock DG, Bositis CM, Nelson-Williams C, Hansson JH, Schambelan M, Gill JR, Ulick S, Milora RV, Findling JW (1994) Liddle’s syndrome: heritable human hypertension caused by mutations in the beta subunit of the epithelial sodium channel. Cell 79:407–414PubMedGoogle Scholar
  203. Silvestri LS, Ruthel G, Kallstrom G, Warfield KL, Swenson DL, Nelle T, Iversen PL, Bavari S, Aman MJ (2007) Involvement of vacuolar protein sorting pathway in Ebola virus release independent of TSG101 interaction. J Infect Dis 196(Suppl 2):S264–S270. doi:10.1086/520610 PubMedGoogle Scholar
  204. Skibinski G, Parkinson NJ, Brown JM, Chakrabarti L, Lloyd SL, Hummerich H, Nielsen JE, Hodges JR, Spillantini MG, Thusgaard T, Brandner S, Brun A, Rossor MN, Gade A, Johannsen P, Sørensen SA, Gydesen S, Fisher EM, Collinge J (2005) Mutations in the endosomal ESCRTIII-complex subunit CHMP2B in frontotemporal dementia. Nat Genet 37:806–808. doi:10.1038/ng1609 PubMedGoogle Scholar
  205. Snyder PM, Olson DR, Thomas BC (2002) Serum and glucocorticoid-regulated kinase modulates Nedd4-2-mediated inhibition of the epithelial Na+ channel. J Biol Chem 277:5–8. doi:10.1074/jbc.C100623200 PubMedGoogle Scholar
  206. Snyder PM, Steines JC, Olson DR (2004) Relative contribution of Nedd4 and Nedd4-2 to ENaC regulation in epithelia determined by RNA interference. J Biol Chem 279:5042–5046. doi:10.1074/jbc.M312477200 PubMedGoogle Scholar
  207. Spitzer C, Schellmann S, Sabovljevic A, Shahriari M, Keshavaiah C, Bechtold N, Herzog M, Müller S, Hanisch FG, Hülskamp M (2006) The Arabidopsis elch mutant reveals functions of an ESCRT component in cytokinesis. Development 133:4679–4689. doi:10.1242/dev.02654 PubMedGoogle Scholar
  208. Spitzer C, Reyes FC, Buono R, Sliwinski MK, Haas TJ, Otegui MS (2009) The ESCRT-related CHMP1A and B proteins mediate multivesicular body sorting of auxin carriers in Arabidopsis and are required for plant development. Plant Cell 21:749–766. doi:10.1105/tpc.108.064865 PubMedGoogle Scholar
  209. Staub O, Dho S, Henry P, Correa J, Ishikawa T, McGlade J, Rotin D (1996) WW domains of Nedd4 bind to the proline-rich PY motifs in the epithelial Na+ channel deleted in Liddle’s syndrome. EMBO J 15:2371–2380PubMedGoogle Scholar
  210. Stauffer DR, Howard TL, Nyun T, Hollenberg SM (2001) CHMP1 is a novel nuclear matrix protein affecting chromatin structure and cell-cycle progression. J Cell Sci 114:2383–2393PubMedGoogle Scholar
  211. Sullivan JA, Lewis MJ, Nikko E, Pelham HR (2007) Multiple interactions drive adaptor-mediated recruitment of the ubiquitin ligase rsp5 to membrane proteins in vivo and in vitro. Mol Biol Cell 18:2429–2440. doi:10.1091/mbc.E07-01-0011 PubMedGoogle Scholar
  212. Sutter JU, Sieben C, Hartel A, Eisenach C, Thiel G, Blatt MR (2007) Abscisic acid triggers the endocytosis of the arabidopsis KAT1 K+ channel and its recycling to the plasma membrane. Curr Biol 17:1396–1402. doi:10.1016/j.cub.2007.07.020 PubMedGoogle Scholar
  213. Szaszi K, Paulsen A, Szabo EZ, Numata M, Grinstein S, Orlowski J (2002) Clathrin-mediated endocytosis and recycling of the neuron-specific Na+/H+ exchanger NHE5 isoform. Regulation by phosphatidylinositol 3′-kinase and the actin cytoskeleton. J Biol Chem 277:42623–42632. doi:10.1074/jbc.M206629200 PubMedGoogle Scholar
  214. Takahashi H, Nozawa A, Seki M, Shinozaki K, Endo Y, Sawasaki T (2009) A simple and high-sensitivity method for analysis of ubiquitination and polyubiquitination based on wheat cell-free protein synthesis. BMC Plant Biol 9:39. doi:10.1186/1471-2229-9-39 PubMedGoogle Scholar
  215. Takano J, Miwa K, Yuan L, von Wirén N, Fujiwara T (2005) Endocytosis and degradation of BOR1, a boron transporter of Arabidopsis thaliana, regulated by boron availability. Proc Natl Acad Sci USA 102:12276–12281. doi:10.1073/pnas.0502060102 PubMedGoogle Scholar
  216. 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. doi:10.1073/pnas.0910744107 PubMedGoogle Scholar
  217. Tang W, Ruknudin A, Yang WP, Shaw SY, Knickerbocker A, Kurtz S (1995) Functional expression of a vertebrate inwardly rectifying K+ channel in yeast. Mol Biol Cell 6:1231–1240PubMedGoogle Scholar
  218. Teis D, Saksena S, Emr SD (2008) Ordered assembly of the ESCRT-III complex on endosomes is required to sequester cargo during MVB formation. Dev Cell 15:578–589. doi:10.1016/j.devcel.2008.08.013 PubMedGoogle Scholar
  219. Tian M, Xie Q (2013) Non-26S proteasome proteolytic role of ubiquitin in plant endocytosis and endosomal trafficking(F). J Integr Plant Biol 55:54–63. doi:10.1111/jipb.12007 PubMedGoogle Scholar
  220. Tian Q, Olsen L, Sun B, Lid SE, Brown RC, Lemmon BE, Fosnes K, Gruis DF, Opsahl-Sorteberg HG, Otegui MS, Olsen OA (2007) Subcellular localization and functional domain studies of DEFECTIVE KERNEL1 in maize and Arabidopsis suggest a model for aleurone cell fate specification involving CRINKLY4 and SUPERNUMERARY ALEURONE LAYER1. Plant Cell 19:3127–3145. doi:10.1105/tpc.106.048868 PubMedGoogle Scholar
  221. Toyoshima M, Tanaka N, Aoki J, Tanaka Y, Murata K, Kyuuma M, Kobayashi H, Ishii N, Yaegashi N, Sugamura K (2007) Inhibition of tumor growth and metastasis by depletion of vesicular sorting protein Hrs: its regulatory role on E-cadherin and beta-catenin. Cancer Res 67:5162–5171. doi:10.1158/0008-5472.CAN-06-2756 PubMedGoogle Scholar
  222. Trajkovic K, Dhaunchak AS, Goncalves JT, Wenzel D, Schneider A, Bunt G, Nave KA, Simons M (2006) Neuron to glia signaling triggers myelin membrane exocytosis from endosomal storage sites. J Cell Biol 172:937–948. doi:10.1083/jcb.200509022 PubMedGoogle Scholar
  223. Tu C, Ahmad G, Mohapatra B, Bhattacharyya S, Ortega-Cava CF, Chung BM, Wagner KU, Raja SM, Naramura M, Band V, Band H (2011) ESCRT proteins: double-edged regulators of cellular signaling. Bioarchitecture 1:45–48. doi:10.4161/bioa.1.1.15173 PubMedGoogle Scholar
  224. Usami Y, Popov S, Popova E, Göttlinger HG (2008) Efficient and specific rescue of human immunodeficiency virus type 1 budding defects by a Nedd4-like ubiquitin ligase. J Virol 82:4898–4907. doi:10.1128/JVI.02675-07 PubMedGoogle Scholar
  225. Usami Y, Popov S, Popova E, Inoue M, Weissenhorn W, G Göttlinger H (2009) The ESCRT pathway and HIV-1 budding. Biochem Soc Trans 37:181–184. doi:10.1042/BST0370181 PubMedGoogle Scholar
  226. Vallier LG, Carlson M (1991) New SNF genes, GAL11 and GRR1 affect SUC2 expression in Saccharomyces cerevisiae. Genetics 129:675–684PubMedGoogle Scholar
  227. Van Belle D, André B (2001) A genomic view of yeast membrane transporters. Curr Opin Cell Biol 13:389–398PubMedGoogle Scholar
  228. van Bemmelen MX, Rougier JS, Gavillet B, Apothéloz F, Daidié D, Tateyama M, Rivolta I, Thomas MA, Kass RS, Staub O, Abriel H (2004) Cardiac voltage-gated sodium channel Nav1.5 is regulated by Nedd4-2 mediated ubiquitination. Circ Res 95:284–291. doi:10.1161/01.RES.0000136816.05109.89 PubMedGoogle Scholar
  229. Vecchione A, Marchese A, Henry P, Rotin D, Morrione A (2003) The Grb10/Nedd4 complex regulates ligand-induced ubiquitination and stability of the insulin-like growth factor I receptor. Mol Cell Biol 23:3363–3372PubMedGoogle Scholar
  230. Viotti C, Bubeck J, Stierhof YD, Krebs M, Langhans M, van den Berg W, van Dongen W, 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. doi:10.1105/tpc.109.072637 PubMedGoogle Scholar
  231. Waguri S, Dewitte F, Le Borgne R, Rouillé Y, Uchiyama Y, Dubremetz JF, Hoflack B (2003) Visualization of TGN to endosome trafficking through fluorescently labeled MPR and AP-1 in living cells. Mol Biol Cell 14:142–155. doi:10.1091/mbc.E02-06-0338 PubMedGoogle Scholar
  232. Wang X, Trotman LC, Koppie T, Alimonti A, Chen Z, Gao Z, Wang J, Erdjument-Bromage H, Tempst P, Cordon-Cardo C, Pandolfi PP, Jiang X (2007) NEDD4-1 is a proto-oncogenic ubiquitin ligase for PTEN. Cell 128:129–139. doi:10.1016/j.cell.2006.11.039 PubMedGoogle Scholar
  233. Wang J, Ding Y, Hillmer S, Miao Y, Lo SW, Wang X, Robinson DG, Jiang L (2010) EXPO, an exocyst-positive organelle distinct from multivesicular endosomes and autophagosomes, mediates cytosol to cell wall exocytosis in Arabidopsis and tobacco cells. Plant Cell 22:4009–4030. doi:10.1105/tpc.110.080697 PubMedGoogle Scholar
  234. Webster G, Berul CI (2013) An update on channelopathies: from mechanisms to management. Circulation 127:126–140. doi:10.1161/CIRCULATIONAHA.111.060343 PubMedGoogle Scholar
  235. Winter V, Hauser MT (2006) Exploring the ESCRTing machinery in eukaryotes. Trends Plant Sci 11:115–123. doi:10.1016/j.tplants.2006.01.008 PubMedGoogle Scholar
  236. Wittinger M, Vanhara P, El-Gazzar A, Savarese-Brenner B, Pils D, Anees M, Grunt TW, Sibilia M, Holcmann M, Horvat R, Schemper M, Zeillinger R, Schöfer C, Dolznig H, Horak P, Krainer M (2011) hVps37A Status affects prognosis and cetuximab sensitivity in ovarian cancer. Clin Cancer Res 17:7816–7827. doi:10.1158/1078-0432.CCR-11-0408 PubMedGoogle Scholar
  237. Wolfe DM, Pearce DA (2006) Channeling studies in yeast: yeast as a model for channelopathies? Neuromolecular Med 8:279–306. doi:10.1385/NMM:8:3:279 PubMedGoogle Scholar
  238. Wollert T, Wunder C, Lippincott-Schwartz J, Hurley JH (2009) Membrane scission by the ESCRT-III complex. Nature 458:172–177. doi:10.1038/nature07836 PubMedGoogle Scholar
  239. Woodman P (2009) ESCRT proteins, endosome organization and mitogenic receptor down-regulation. Biochem Soc Trans 37:146–150. doi:10.1042/BST0370146 PubMedGoogle Scholar
  240. Wright MH, Berlin I, Nash PD (2011) Regulation of endocytic sorting by ESCRT-DUB-mediated deubiquitination. Cell Biochem Biophys 60:39–46. doi:10.1007/s12013-011-9181-9 PubMedGoogle Scholar
  241. Wu N, Zheng B, Shaywitz A, Dagon Y, Tower C, Bellinger G, Shen CH, Wen J, Asara J, McGraw TE, Kahn BB, Cantley LC (2013) AMPK-dependent degradation of TXNIP upon energy stress leads to enhanced glucose uptake via GLUT1. Mol Cell 49:1167–1175. doi:10.1016/j.molcel.2013.01.035 PubMedGoogle Scholar
  242. Xinhan L, Matsushita M, Numaza M, Taguchi A, Mitsui K, Kanazawa H (2011) Na+/H+ exchanger isoform 6 (NHE6/SLC9A6) is involved in clathrin-dependent endocytosis of transferrin. Am J Physiol Cell Physiol 301:C1431–C1444. doi:10.1152/ajpcell.00154.2011 PubMedGoogle Scholar
  243. Yamaguchi T, Fukada-Tanaka S, Inagaki Y, Saito N, Yonekura-Sakakibara K, Tanaka Y, Kusumi T, Iida S (2001) Genes encoding the vacuolar Na+/H+ exchanger and flower coloration. Plant Cell Physiol 42:451–461PubMedGoogle Scholar
  244. Yang B, Kumar S (2010) Nedd4 and Nedd4-2: closely related ubiquitin-protein ligases with distinct physiological functions. Cell Death Differ 17:68–77. doi:10.1038/cdd.2009.84 PubMedGoogle Scholar
  245. Yang KS, Jin UH, Kim J, Song K, Kim SJ, Hwang I, Lim YP, Pai HS (2004) Molecular characterization of NbCHMP1 encoding a homolog of human CHMP1 in Nicotiana benthamiana. Mol Cells 17:255–261PubMedGoogle Scholar
  246. Yang B, Gay DL, MacLeod MK, Cao X, Hala T, Sweezer EM, Kappler J, Marrack P, Oliver PM (2008) Nedd4 augments the adaptive immune response by promoting ubiquitin-mediated degradation of Cbl-b in activated T cells. Nat Immunol 9:1356–1363. doi:10.1038/ni.1670 PubMedGoogle Scholar
  247. Ye Y, Rape M (2009) Building ubiquitin chains: E2 enzymes at work. Nat Rev Mol Cell Biol 10:755–764. doi:10.1038/nrm2780 PubMedGoogle Scholar
  248. Yoshida K, Kawachi M, Mori M, Maeshima M, Kondo M, Nishimura M, Kondo T (2005) The involvement of tonoplast proton pumps and Na+(K+)/H+ exchangers in the change of petal color during flower opening of Morning Glory, Ipomoea tricolor cv. Heavenly Blue. Plant Cell Physiol 46:407–415. doi:10.1093/pcp/pci057 PubMedGoogle Scholar
  249. Zaks-Makhina E, Kim Y, Aizenman E, Levitan ES (2004) Novel neuroprotective K+ channel inhibitor identified by high-throughput screening in yeast. Mol Pharmacol 65:214–219. doi:10.1124/mol.65.1.214 PubMedGoogle Scholar
  250. Zhang L, Anglesio MS, O’Sullivan M, Zhang F, Yang G, Sarao R, Mai PN, Cronin S, Hara H, Melnyk N, Li L, Wada T, Liu PP, Farrar J, Arceci RJ, Sorensen PH, Penninger JM (2007) The E3 ligase HACE1 is a critical chromosome 6q21 tumor suppressor involved in multiple cancers. Nat Med 13:1060–1069. doi:10.1038/nm1621 PubMedGoogle Scholar
  251. Zhang J, Li W, Xiang T, Liu Z, Laluk K, Ding X, Zou Y, Gao M, Zhang X, Chen S, Mengiste T, Zhang Y, Zhou JM (2010) Receptor-like cytoplasmic kinases integrate signaling from multiple plant immune receptors and are targeted by a Pseudomonas syringae effector. Cell Host Microbe 7:290–301. doi:10.1016/j.chom.2010.03.007 PubMedGoogle Scholar
  252. Zhang XQ, Hou P, Zhu HT, Li GD, Liu XG, Xie XM (2013) Knockout of the VPS22 component of the ESCRT-II complex in rice (Oryza sativa L.) causes chalky endosperm and early seedling lethality. Mol Biol Rep 40:3475–3481. doi:10.1007/s11033-012-2422-1 PubMedGoogle Scholar
  253. Zhou R, Kabra R, Olson DR, Piper RC, Snyder PM (2010) Hrs controls sorting of the epithelial Na+ channel between endosomal degradation and recycling pathways. J Biol Chem 285:30523–30530. doi:10.1074/jbc.M110.150755 PubMedGoogle Scholar
  254. Zoladek T, Tobiasz A, Vaduva G, Boguta M, Martin NC, Hopper AK (1997) MDP1, a Saccharomyces cerevisiae gene involved in mitochondrial/cytoplasmic protein distribution, is identical to the ubiquitin-protein ligase gene RSP5. Genetics 145:595–603PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • José Miguel Mulet
    • 1
  • Vicent Llopis-Torregrosa
    • 1
  • Cecilia Primo
    • 1
  • Mª Carmen Marqués
    • 1
  • Lynne Yenush
    • 1
  1. 1.Instituto de Biología Molecular y Celular de Plantas (IBMCP)Universitat Politècnica de València-Consejo Superior de Investigaciones CientíficasValenciaSpain

Personalised recommendations