Abstract
Separation of functions within the cytoplasm of the eukaryotic cell has resulted in the development of a highly dynamic network of membranous compartments. Among them, the endosomes represent a crossing point for the major cellular trafficking pathways. Indeed, they are responsible for the communication between the cellular compartments, as well as between the cell and its environment, through the regulation of signalling networks and transport of material. The proteins from the sorting nexin (SNX) family have an established role as major regulators of endosomal protein transport in mammals, insects, worms, and yeast. By contrast, research on plant SNXs has been initiated relatively recently. Despite that, the accumulated knowledge suggests that plant SNXs may have evolved different mechanisms of action and might work in a different protein complex environment, compared to their yeast and animal counterparts. In this chapter, we highlight both common and specific characteristics of plant SNX protein function and regulation in comparison to the well-studied mammalian SNX machinery.
Enric Zelazny and Rumen Ivanov have contributed equally to this work
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Abbreviations
- BAR:
-
Bin/Amphiphysin/Rvs domain
- C-ter:
-
Nexin C-terminal domain
- MIT:
-
Microtubule interacting domain
- F:
-
Forkhead-associated domain
- FERM:
-
4.1/Ezrin/Radixin/Moesin domain
- Kinesin:
-
Kinesin motor domain
- PDZ:
-
PSD95/Dlg1/Zo-1 domain
- PIN:
-
Pin-formed
- PX:
-
PHOX homology domain
- PXA:
-
PHOX associated domain
- RAB:
-
Rab5-binding domain
- RAS :
-
Ras-association domain
- RGS:
-
Regulator of G-protein signalling domain
- RHO:
-
RhoGAP domain
- SH3:
-
Src Homology 3 domain
- SNX:
-
Sorting nexin
- SRK:
-
S locus receptor kinase
- VPS:
-
Vacuolar protein sorting
References
Abas L, Benjamins R, Malenica N, Paciorek T, Wirniewska 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
Arighi CN, Hartnell LM, Aguilar RC, Haft CR, Bonifacino JS (2004) Role of the mammalian retromer in sorting of the cation-independent mannose 6-phosphate receptor. J Cell Biol 165:123–133
Barberon M, Zelazny E, Robert S, Conejero 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 U S A 108:E450–E458
Bravo J, Karathanassis D, Pacold CM, Pacold ME, Ellson CD, Anderson KE, Butler PJ, Lavenir I, Perisic O, Hawkins PT, Stephens L, Williams RL (2001) The crystal structure of the PX domain from p40(phox) bound to phosphatidylinositol 3-phosphate. Mol Cell 8:829–839
Carlton J, Bujny M, Peter BJ, Oorschot VM, Rutherford A, Mellor H, Klumperman J, McMahon HT, Cullen PJ (2004) Sorting nexin-1 mediates tubular endosome-to-TGN transport through coincidence sensing of high-curvature membranes and 3-phosphoinositides. Curr Biol 14:1791–1800
Carlton J, Bujny M, Rutherford A, Cullen P (2005a) Sorting nexins–unifying trends and new perspectives. Traffic 6:75–82
Carlton JG, Bujny MV, Peter BJ, Oorschot VM, Rutherford A, Arkell RS, Klumperman J, McMahon HT, Cullen PJ (2005b) Sorting nexin-2 is associated with tubular elements of the early endosome, but is not essential for retromer-mediated endosome-to-TGN transport. J Cell Sci 118:4527–4539
Cozier GE, Carlton J, McGregor AH, Gleeson PA, Teasdale RD, Mellor H, Cullen PJ (2002) The phox homology (PX) domain-dependent, 3-phosphoinositide-mediated association of sorting nexin-1 with an early sorting endosomal compartment is required for its ability to regulate epidermal growth factor receptor degradation. J Biol Chem 277:48730–48736
Cullen PJ (2008) Endosomal sorting and signalling: an emerging role for sorting nexins. Nat Rev Mol Cell Biol 9:574–582
Cullen PJ, Korswagen HC (2012) Sorting nexins provide diversity for retromer-dependent trafficking events. Nat Cell Biol 14:29–37
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
Dislich B, Than ME, Lichtenthaler SF (2011) Specific amino acids in the BAR domain allow homodimerization and prevent heterodimerization of sorting nexin 33. Biochem J 433:75–83
Franch-Marro X, Wendler F, Guidato S, Griffith J, Baena-Lopez A, Itasaki N, Maurice MM, Vincent JP (2008) Wingless secretion requires endosome-to-golgi retrieval of Wntless/Evi/Sprinter by the retromer complex. Nat Cell Biol 10:170–177
Frost A, Perera R, Roux A, Spasov K, Destaing O, Egelman EH, De Camilli P, Unger VM (2008) Structural basis of membrane invagination by F-BAR domains. Cell 132:807–817
Geldner N, Friml J, Stierhof YD, Jurgens G, Palme K (2001) Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature 413:425–428
Geldner N, Hyman DL, Wang X, Schumacher K, Chory J (2007) Endosomal signaling of plant steroid receptor kinase BRI1. Genes Dev 21:1598–1602
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
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
Haberg K, Lundmark R, Carlsson SR (2008) SNX18 is an SNX9 paralog that acts as a membrane tubulator in AP-1-positive endosomal trafficking. J Cell Sci 121:1495–1505
Haft CR, de la Luz Sierra M, Barr VA, Haft DH, Taylor SI (1998) Identification of a family of sorting nexin molecules and characterization of their association with receptors. Mol Cell Biol 18:7278–7287
Hettema EH, Lewis MJ, Black MW, Pelham HR (2003) Retromer and the sorting nexins Snx4/41/42 mediate distinct retrieval pathways from yeast endosomes. EMBO J 22:548–557
Horazdovsky BF, Davies BA, Seaman MN, McLaughlin SA, Yoon S, Emr SD (1997) A sorting nexin-1 homologue, Vps5p, forms a complex with Vps17p and is required for recycling the vacuolar protein-sorting receptor. Mol Biol Cell 8:1529–1541
Jaillais Y, Fobis-Loisy I, Miege C, Gaude T (2008) Evidence for a sorting endosome in Arabidopsis root cells. Plant J 53:237–247
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
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
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
Kleine-Vehn J, Leitner J, Zwiewka M, Sauer M, Abas L, Luschnig C, Friml J (2008) Differential degradation of PIN2 auxin efflux carrier by retromer-dependent vacuolar targeting. Proc Natl Acad Sci USA 105:17812–17817
Koumandou VL, Klute MJ, Herman EK, Nunez-Miguel R, Dacks JB, Field MC (2011) Evolutionary reconstruction of the retromer complex and its function in Trypanosoma brucei. J Cell Sci 124:1496–1509
Kurten RC, Cadena DL, Gill GN (1996) Enhanced degradation of EGF receptors by a sorting nexin, SNX1. Science 272:1008–1010
Kurten RC, Eddington AD, Chowdhury P, Smith RD, Davidson AD, Shank BB (2001) Self-assembly and binding of a sorting nexin to sorting endosomes. J Cell Sci 114:1743–1756
Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and clustal X version 2.0. Bioinformatics 23:2947–2948
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
Lundmark R, Carlsson SR (2003) Sorting nexin 9 participates in clathrin-mediated endocytosis through interactions with the core components. J Biol Chem 278:46772–46781
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
Niemes S, Labs M, Scheuring D, Krueger F, Langhans M, Jesenofsky B, Robinson DG, Pimpl P (2010a) Sorting of plant vacuolar proteins is initiated in the ER. Plant J 62:601–614
Niemes S, Langhans M, Viotti C, Scheuring D, San Wan Yan M, Jiang L, Hillmer S, Robinson DG, Pimpl P (2010b) Retromer recycles vacuolar sorting receptors from the trans-Golgi network. Plant J 61:107–121
Nisar S, Kelly E, Cullen PJ, Mundell SJ (2010) Regulation of P2Y1 receptor traffic by sorting Nexin 1 is retromer independent. Traffic 11:508–519
Nothwehr SF, Hindes AE (1997) The yeast VPS5/GRD2 gene encodes a sorting nexin-1-like protein required for localizing membrane proteins to the late golgi. J Cell Sci 110(Pt 9):1063–1072
Paciorek T, Zazimalova E, Ruthardt N, Petrasek J, Stierhof YD, Kleine-Vehn J, Morris DA, Emans N, Jurgens G, Geldner N, Friml J (2005) Auxin inhibits endocytosis and promotes its own efflux from cells. Nature 435:1251–1256
Perrière G, Gouy M (1996) WWW-query: an on-line retrieval system for biological sequence banks. Biochimie 78:364–369
Peter BJ, Kent HM, Mills IG, Vallis Y, Butler PJ, Evans PR, McMahon HT (2004) BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science 303:495–499
Phan NQ, Kim SJ, Bassham DC (2008) overexpression of Arabidopsis sorting nexin AtSNX2b inhibits endocytic trafficking to the vacuole. Mol Plant 1:961–976
Ponting CP (1996) Novel domains in NADPH oxidase subunits, sorting nexins, and PtdIns 3-kinases: binding partners of SH3 domains? Protein Sci 5:2353–2357
Pourcher M, Santambrogio M, Thazar N, Thierry AM, Fobis-Loisy I, Miege C, Jaillais Y, Gaude T (2010) Analyses of sorting nexins reveal distinct retromer-subcomplex functions in development and protein sorting in Arabidopsis thaliana. Plant Cell 22:3980–3991
Pylypenko O, Lundmark R, Rasmuson E, Carlsson SR, Rak A (2007) The PX-BAR membrane-remodeling unit of sorting nexin 9. EMBO J 26:4788–4800
Rahman A, Takahashi M, Shibasaki K, Wu S, Inaba T, Tsurumi S, Baskin TI (2010) Gravitropism of Arabidopsis thaliana roots requires the polarization of PIN2 toward the root tip in meristematic cortical cells. Plant Cell 22:1762–1776
Reddy JV, Seaman MN (2001) Vps26p, a component of retromer, directs the interactions of Vps35p in endosome-to-golgi retrieval. Mol Biol Cell 12:3242–3256
Reyes FC, Buono R, Otegui MS (2011) Plant endosomal trafficking pathways. Curr Opin Plant Biol 14:666–673
Robinson DG, Pimpl P, Scheuring D, Stierhof YD, Sturm S, Viotti C (2012) Trying to make sense of retromer. Trends Plant Sci 17:431–439
Roepstorff K, Grandal MV, Henriksen L, Knudsen SL, Lerdrup M, Grovdal L, Willumsen BM, van Deurs B (2009) Differential effects of EGFR ligands on endocytic sorting of the receptor. Traffic 10:1115–1127
Rojas R, Kametaka S, Haft CR, Bonifacino JS (2007) Interchangeable but essential functions of SNX1 and SNX2 in the association of retromer with endosomes and the trafficking of mannose 6-phosphate receptors. Mol Cell Biol 27:1112–1124
Seaman MN (2004) Cargo-selective endosomal sorting for retrieval to the Golgi requires retromer. J Cell Biol 165:111–122
Seaman MN, Marcusson EG, Cereghino JL, Emr SD (1997) Endosome to Golgi retrieval of the vacuolar protein sorting receptor, Vps10p, requires the function of the VPS29, VPS30, and VPS35 gene products. J Cell Biol 137:79–92
Seet LF, Hong W (2006) The phox (PX) domain proteins and membrane traffic. Biochim Biophys Acta 1761:878–896
Shibasaki K, Uemura M, Tsurumi S, Rahman A (2009) Auxin response in Arabidopsis under cold stress: underlying molecular mechanisms. Plant Cell 21:3823–3838
Shin N, Lee S, Ahn N, Kim SA, Ahn SG, YongPark Z, Chang S (2007) Sorting nexin 9 interacts with dynamin 1 and N-WASP and coordinates synaptic vesicle endocytosis. J Biol Chem 282:28939–28950
Soulet F, Yarar D, Leonard M, Schmid SL (2005) SNX9 regulates dynamin assembly and is required for efficient clathrin-mediated endocytosis. Mol Biol Cell 16:2058–2067
Stierhof YD, Viotti C, Scheuring D, Sturm S, Robinson DG (2012) Sorting nexins 1 and 2a locate mainly to the TGN. Protoplasma. doi:10.1007/s00709-012-0399-1
Strochlic TI, Setty TG, Sitaram A, Burd CG (2007) Grd19/Snx3p functions as a cargo-specific adapter for retromer-dependent endocytic recycling. J Cell Biol 177:115–125
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
Teasdale RD, Collins BM (2012) Insights into the PX (phox-homology) domain and SNX (sorting nexin) protein families: structures, functions and roles in disease. Biochem J 441:39–59
Teasdale RD, Loci D, Houghton F, Karlsson L, Gleeson PA (2001) A large family of endosome-localized proteins related to sorting nexin 1. Biochem J 358:7–16
Traer CJ, Rutherford AC, Palmer KJ, Wassmer T, Oakley J, Attar N, Carlton JG, Kremerskothen J, Stephens DJ, Cullen PJ (2007) SNX4 coordinates endosomal sorting of TfnR with dynein-mediated transport into the endocytic recycling compartment. Nat Cell Biol 9:1370–1380
van Leeuwen W, Okresz L, Bogre L, Munnik T (2004) Learning the lipid language of plant signalling. Trends Plant Sci 9:378–384
van Weering JR, Verkade P, Cullen PJ (2010) SNX-BAR proteins in phosphoinositide-mediated, tubular-based endosomal sorting. Semin Cell Dev Biol 21:371–380
van Weering JR, Verkade P, Cullen PJ (2012) SNX-BAR-mediated endosome tubulation is co-ordinated with endosome maturation. Traffic 13:94–107
Vanoosthuyse V, Tichtinsky G, Dumas C, Gaude T, Cock JM (2003) Interaction of calmodulin, a sorting nexin and kinase-associated protein phosphatase with the Brassica oleracea S locus receptor kinase. Plant Physiol 133:919–929
Voigt B, Timmers AC, Šamaj J, Hlavacka A, Ueda T, Preuss M, Nielsen E, Mathur J, Emans N, Stenmark H, Nakano A, Baluška F, Menzel D (2005) Actin-based motility of endosomes is linked to the polar tip growth of root hairs. Eur J Cell Biol 84:609–621
Wang Q, Kaan HY, Hooda RN, Goh SL, Sondermann H (2008) Structure and plasticity of endophilin and sorting nexin 9. Structure 16:1574–1587
Wassmer T, Attar N, Harterink M, van Weering JR, Traer CJ, Oakley J, Goud B, Stephens DJ, Verkade P, Korswagen HC, Cullen PJ (2009) The retromer coat complex coordinates endosomal sorting and dynein-mediated transport, with carrier recognition by the trans-Golgi network. Dev Cell 17:110–122
Worby CA, Dixon JE (2002) Sorting out the cellular functions of sorting nexins. Nat Rev Mol Cell Biol 3:919–931
Xu Y, Hortsman H, Seet L, Wong SH, Hong W (2001) SNX3 regulates endosomal function through its PX-domain-mediated interaction with PtdIns(3)P. Nat Cell Biol 3:658–666
Yamazaki M, Shimada T, Takahashi H, Tamura K, Kondo M, Nishimura M, Hara-Nishimura I (2008) Arabidopsis VPS35, a retromer component, is required for vacuolar protein sorting and involved in plant growth and leaf senescence. Plant Cell Physiol 49:142–156
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
Zhong Q, Watson MJ, Lazar CS, Hounslow AM, Waltho JP, Gill GN (2005) Determinants of the endosomal localization of sorting nexin 1. Mol Biol Cell 16:2049–2057
Zhou CZ, de La Sierra-Gallay IL, Quevillon-Cheruel S, Collinet B, Minard P, Blondeau K, Henckes G, Aufrere R, Leulliot N, Graille M, Sorel I, Savarin P, de la Torre F, Poupon A, Janin J, van Tilbeurgh H (2003) Crystal structure of the yeast phox homology (PX) domain protein Grd19p complexed to phosphatidylinositol-3-phosphate. J Biol Chem 278:50371–50376
Zimmerberg J, McLaughlin S (2004) Membrane curvature: how BAR domains bend bilayers. Curr Biol 14:R250–R252
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2012 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
Zelazny, E., Ivanov, R., Gaude, T. (2012). The Plant SNX Family and Its Role in Endocytosis. In: Šamaj, J. (eds) Endocytosis in Plants. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-32463-5_12
Download citation
DOI: https://doi.org/10.1007/978-3-642-32463-5_12
Published:
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-642-32462-8
Online ISBN: 978-3-642-32463-5
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)