Cell wall constrains lateral diffusion of plant plasma-membrane proteins

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 31, 2012, Pages 12805-12810

  Martinière, Alexandre ^a   Lavagi, Irene ^a   Nageswaran, Gayathri ^a   Rolfe, Daniel J ^b   Maneta Peyret, Lilly ^c   Luu, Doan Trung ^d   Botchway, Stanley W ^b   Webb, Stephen E D ^b   Mongrand, Sebastien ^c   Maurel, Christophe ^d   Martin Fernandez, Marisa L ^b   Kleine Vehn, Jürgen ^e   Friml, Jirí ^f   Moreau, Patrick ^c   Runions, John ^a  

^a OXFORD BROOKES UNIVERSITY   (United Kingdom)

^b RUTHERFORD APPLETON LABORATORY   (United Kingdom)

^c University Victor Segalen   (France)

^d CNRS   (France)

^e UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

^f GHENT UNIVERSITY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MEMBRANE PROTEIN; CELLULOSE; GREEN FLUORESCENT PROTEIN;

ARTICLE; CELL WALL; CYTOSKELETON; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; PLANT CELL; PRIORITY JOURNAL; PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL WALL; CYTOSKELETON; MEMBRANE MICRODOMAINS; MEMBRANE PROTEINS; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; TOBACCO;

ANIMALIA;

EID: 84864497608     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1202040109     Document Type: Article

References (49)

1. Schwacke R, et al. (2003) ARAMEMNON, a novel database for Arabidopsis integral membrane proteins. Plant Physiol 131:16-26. (Pubitemid 36141203)
2. Engelman DM (2005) Membranes are more mosaic than fluid. Nature 438:578-580.
3. Singer SJ, Nicolson GL (1972) The fluid mosaic model of the structure of cell membranes. Science 175:720-731.
4. Saffman PG, Delbrück M (1975) Brownian motion in biological membranes. Proc Natl Acad Sci USA 72:3111-3113.
5. Thompson NL, Axelrod D (1980) Reduced lateral mobility of a fluorescent lipid probe in cholesterol-depleted erythrocyte membrane. Biochim Biophys Acta 597:155-165.
6. Yechiel E, Edidin M (1987) Micrometer-scale domains in fibroblast plasma membranes. J Cell Biol 105:755-760. (Pubitemid 18043838)
7. Kwik J, et al. (2003) Membrane cholesterol, lateral mobility, and the phosphatidylinositol 4,5-bisphosphate-dependent organization of cell actin. Proc Natl Acad Sci USA 100:13964-13969. (Pubitemid 37499174)
8. Lenne PF, et al. (2006) Dynamic molecular confinement in the plasma membrane by microdomains and the cytoskeleton meshwork. EMBO J 25:3245-3256.
9. Sieber JJ, et al. (2007) Anatomy and dynamics of a supramolecular membrane protein cluster. Science 317:1072-1076. (Pubitemid 47330189)
10. Kusumi A, et al. (2005) Paradigm shift of the plasma membrane concept from the two-dimensional continuum fluid to the partitioned fluid: High-speed single-molecule tracking of membrane molecules. Annu Rev Biophys Biomol Struct 34:351-378. (Pubitemid 40847729)
11. Simons K, Ikonen E (1997) Functional rafts in cell membranes. Nature 387:569-572. (Pubitemid 27248754)
12. Owen DM, Williamson D, Rentero C, Gaus K (2009) Quantitative microscopy: Protein dynamics and membrane organisation. Traffic 10:962-971.
13. Mongrand S, Stanislas T, Bayer EM, Lherminier J, Simon-Plas F (2010) Membrane rafts in plant cells. Trends Plant Sci 15:656-663.
14. Borner GH, et al. (2005) Analysis of detergent-resistant membranes in Arabidopsis. Evidence for plasma membrane lipid rafts. Plant Physiol 137:104-116. (Pubitemid 43034293)
15. Morel J, et al. (2006) Proteomics of plant detergent-resistant membranes. Mol Cell Proteomics 5:1396-1411. (Pubitemid 44323294)
16. Lefebvre B, et al. (2007) Characterization of lipid rafts from Medicago truncatula root plasma membranes: A proteomic study reveals the presence of a raft-associated redox system. Plant Physiol 144:402-418. (Pubitemid 46941606)
17. Grossmann G, Opekarova M, Novakova L, Stolz J, Tanner W (2006) Lipid raft-based membrane compartmentation of a plant transport protein expressed in Saccharomyces cerevisiae. Eukaryot Cell 5:945-953. (Pubitemid 43895024)
18. Raffaele S, et al. (2009) Remorin, a solanaceae protein resident in membrane rafts and plasmodesmata, impairs potato virus X movement. Plant Cell 21:1541-1555.
19. Men S, et al. (2008) Sterol-dependent endocytosis mediates post-cytokinetic acquisition of PIN2 auxin efflux carrier polarity. Nat Cell Biol 10:237-244. (Pubitemid 351194054)
20. Liu P, et al. (2009) Lipid microdomain polarization is required for NADPH oxidase-dependent ROS signaling in Picea meyeri pollen tube tip growth. Plant J 60:303-313.
21. Takano J, et al. (2010) Polar localization and degradation of Arabidopsis boron transporters through distinct trafficking pathways. Proc Natl Acad Sci USA 107: 5220-5225.
22. Feraru E, et al. (2011) PIN polarity maintenance by the cell wall in Arabidopsis. Curr Biol 21:338-343.
23. Martinière A, Gayral P, Hawes C, Runions J (2011) Building bridges: Formin1 of Arabidopsis forms a connection between the cell wall and the actin cytoskeleton. Plant J 66:354-365.
24. Runions J, Brach T, Kühner S, Hawes C (2006) Photoactivation of GFP reveals protein dynamics within the endoplasmic reticulum membrane. J Exp Bot 57:43-50. (Pubitemid 43007126)
25. Graumann K, Runions J, Evans DE (2010) Characterization of SUN-domain proteins at the higher plant nuclear envelope. Plant J 61:134-144.
26. Sparkes I, Runions J, Hawes C, Griffing L (2009) Movement and remodeling of the endoplasmic reticulum in nondividing cells of tobacco leaves. Plant Cell 21:3937-3949.
27. Sutter JU, Campanoni P, Tyrrell M, Blatt MR (2006) Selective mobility and sensitivity to SNAREs is exhibited by the Arabidopsis KAT1 K+ channel at the plasma membrane. Plant Cell 18:935-954. (Pubitemid 43956146)
28. Sorieul M, Santoni V, Maurel C, Luu DT (2011) Mechanisms and effects of retention of over-expressed aquaporin AtPIP2;1 in the endoplasmic reticulum. Traffic 12:473-482.
29. Sparkes IA, Runions J, Kearns A, Hawes C (2006) Rapid, transient expression of fluorescent fusion proteins in tobacco plants and generation of stably transformed plants. Nat Protoc 1:2019-2025. (Pubitemid 46773326)
30. Luu DT, et al. (2012) Fluorescence recovery after photobleaching reveals high cycling dynamics of plasma membrane aquaporins in Arabidopsis roots under salt stress. Plant J 69:894-905.
31. Umenishi F, Verbavatz JM, Verkman AS (2000) cAMP regulated membrane diffusion of a green fluorescent protein-aquaporin 2 chimera. Biophys J 78:1024-1035. (Pubitemid 30211861)
32. Vermeer JE, et al. (2009) Imaging phosphatidylinositol 4-phosphate dynamics in living plant cells. Plant J 57:356-372.
33. Brandizzi F, et al. (2002) The destination for single-pass membrane proteins is influenced markedly by the length of the hydrophobic domain. Plant Cell 14:1077-1092. (Pubitemid 34609218)
34. Grebe M, et al. (2003) Arabidopsis sterol endocytosis involves actin-mediated trafficking via ARA6-positive early endosomes. Curr Biol 13:1378-1387. (Pubitemid 37029427)
35. Bonneau L, et al. (2010) Plasma membrane sterol complexation, generated by filipin, triggers signaling responses in tobacco cells. Biochim Biophys Acta 1798: 2150-2159.
36. 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. (Pubitemid 34839781)
37. Li X, et al. (2011) Single-molecule analysis of PIP2;1 dynamics and partitioning reveals multiple modes of Arabidopsis plasma membrane aquaporin regulation. Plant Cell 23: 3780-3797.
38. Vizcay-Barrena G, Webb SE, Martin-Fernandez ML, Wilson ZA (2011) Subcellular and single-molecule imaging of plant fluorescent proteins using total internal reflection fluorescence microscopy (TIRFM). J Exp Bot 62:5419-5428.
39. Patterson GH, Lippincott-Schwartz J (2002) A photoactivatable GFP for selective photolabeling of proteins and cells. Science 297:1873-1877. (Pubitemid 35024347)
40. Holtzer L, Schmidt T (2010) The tracking of individual molecules in cells and tissues. Single Particle Tracking and Single Molecule Energy Transfer, eds Brauchle C, Lamb D, Michaelis J (Wiley-VCH, Weinheim, Germany).
41. Homann U, Meckel T, Hewing J, Hütt MT, Hurst AC (2007) Distinct fluorescent pattern of KAT1:GFP in the plasma membrane of Vicia faba guard cells. Eur J Cell Biol 86:489-500. (Pubitemid 47099510)
42. Carpita NC (2011) Update on mechanisms of plant cell wall biosynthesis: How plants make cellulose and other (1->4)-β-D-glycans. Plant Physiol 155:171-184.
43. Giddings TH, Jr., Brower DL, Staehelin LA (1980) Visualization of particle complexes in the plasma membrane of Micrasterias denticulata associated with the formation of cellulose fibrils in primary and secondary cell walls. J Cell Biol 84:327-339. (Pubitemid 10147870)
44. Mueller SC, Brown RM, Jr. (1980) Evidence for an intramembrane component associated with a cellulose microfibril-synthesizing complex in higher plants. J Cell Biol 84: 315-326. (Pubitemid 10147869)
45. Wang L, Hukin D, Pritchard J, Thomas C (2006) Comparison of plant cell turgor pressure measurement by pressure probe and micromanipulation. Biotechnol Lett 28: 1147-1150. (Pubitemid 44078503)
46. Kleine-Vehn J, et al. (2011) Recycling, clustering, and endocytosis jointly maintain PIN auxin carrier polarity at the plasma membrane. Mol Syst Biol 7:540.
47. Bischoff V, Cookson SJ, Wu S, Scheible WR (2009) Thaxtomin A affects CESA-complex density, expression of cell wall genes, cell wall composition, and causes ectopic lignification in Arabidopsis thaliana seedlings. J Exp Bot 60:955-965.
48. Clarke DT, et al. (2011) Optics clustered to output unique solutions: A multi-laser facility for combined single molecule and ensemble microscopy. Review of Scientific Instruments 82, 093705.
49. Rolfe DJ, et al. (2011) Automated multidimensional single molecule fluorescence microscopy feature detection and tracking. Eur Biophys J 40:1167-1186.