Protein diffusion in plant cell plasma membranes: The cell-wall corral

Frontiers in Plant Science

Volumn 4, Issue DEC, 2013, Pages

  Martiniere, Alexandre ^a   Runions, John ^b  

^a UNIV MONTPELLIER   (France)

^b OXFORD BROOKES UNIVERSITY   (United Kingdom)

Author keywords

Cell wall; Corral; Cytoskeleton; Diffusion; Lateral mobility; Plasma membrane microdomains

Indexed keywords

EID: 84901011441     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2013.00515     Document Type: Article

References (47)

1. Alassimone, J., Naseer, S., and Geldner, N. (2010). A developmental framework for endodermal differentiation and polarity. Proc. Natl. Acad. Sci. U.S.A. 107, 5214-5219. doi: 10.1073/pnas.0910772107
2. Ali, G. S., Prasad, K. V., Day, I., and Reddy, A. S. (2007). Ligand-dependent reduction in the membrane mobility of FLAGELLIN SENSITIVE2, an arabidopsis receptor-like kinase. Plant Cell Physiol. 48, 1601-1611. doi: 10.1093/pcp/pcm132
3. Axelrod, D. (1983). Lateral motion of membrane proteins and biological function. J. Membr. Biol. 75, 1-10. doi: 10.1007/BF01870794
4. Borner, G. H., Sherrier, D. J., Weimar, T., Michaelson, L. V., Hawkins, N. D. MacAskill, A., et al. (2005). Analysis of detergent-resistant membranes in Arabidopsis. Evidence for plasma membrane lipid rafts. Plant Physiol. 137, 104-116. doi: 10.1104/pp.104.053041
5. Boutte, Y., Frescatada-Rosa, M., Men, S., Chow, C. M., Ebine, K., Gustavsson, A., et al. (2010). Endocytosis restricts Arabidopsis KNOLLE syntaxin to the cell division plane during late cytokinesis. EMBO J. 29, 546-558. doi: 10.1038/emboj.2009.363
6. Choquet, D., and Triller, A. (2003). The role of receptor diffusion in the organization of the postsynaptic membrane. Nat. Rev. Neurosci. 4, 251-265. doi: 10.1038/nrn1077
7. Demir, F., Horntrich, C., Blachutzik, J. O., Scherzer, S., Reinders, Y., Kierszniowska, A et al. (2013). Arabidopsis nanodomain-delimited ABA signaling pathway regulates the anion channel SLAH3. Proc. Natl. Acad. Sci. U.S.A. 20, 8296-8301 doi: 10.1073/pnas.1211667110
8. Engelman, D. M. (2005). Membranes are more mosaic than fluid. Nature. 438, 578-580. doi: 10.1038/nature04394
9. Feder, T. J., Brust-Mascher, I., Slattery, J. P., Baird, B., and Webb, W. W. (1996). Constrained diffusion or immobile fraction on cell surfaces: a new interpretation. Biophys. J. 70, 2767-73. doi: 10.1016/S0006-3495(96) 79846-6
10. Feraru, E., Feraru, M. I., Kleine-Vehn, J., Martiniere, A., Mouille, G., Vanneste, S., et al. (2011). PIN polarity maintenance by the cell wall in Arabidopsis. Curr. Biol. 21, 338-343. doi: 10.1016/j.cub.2011. 01.036
11. Frischknecht, R., Heine, M., Perrais, D., Seidenbecher, C. I., Choquet, D., and Gundelfinger, E. D. (2009). Brain extracellular matrix affects AMPA receptor lateral mobility and short-term synaptic plasticity. Nat. Neurosci. 12, 897-904. doi: 10.1038/nn.2338
12. Geldner, N. (2013). The endodermis. Annu. Rev. Plant Biol. 64, 531-558. doi: 10.1146/annurev-arplant-050312-120050
13. Greenberg, M. L., and Axelrod, D. (1993). Anomalously slow mobility of fluorescent lipid probes in the plasma membrane of the yeast Saccharomyces cerevisiae. J. Membr. Biol. 131, 115-127. doi: 10.1007/BF027 91320
14. Hammond, G. R., Sim, Y., Lagnado, L., and Irvine, R. F. (2009). Reversible binding and rapid diffusion of proteins in complex with inositol lipids serves to coordinate free movement with spatial information. J. Cell Biol. 184, 297-308 doi: 10.1083/jcb.200809073
15. Hematy, K. and Hofte, H. (2008). Novel receptor kinases involved in growth regulation. Curr. Opin. Plant Biol. 11, 321-328. doi: 10.1016/j.pbi.2008. 02.008
16. Keinath, N. F., Kierszniowska, S., Lorek, J. Bourdais, G. Kessler, S. A. Shimosato- Asano, H., et al. (2010). PAMP (pathogen-associated molecular pattern)- induced changes in plasma membrane compartmentalization reveal novel components of plant immunity. J Biol. Chem. 285, 39140-43919. doi: 10.1074/jbc.M110.160531
17. Kleine-Vehn, J., Wabnik, K., Martiniere, A., Langowski, L., Willig, K., Naramoto, A., et al. (2011). Recycling, clustering, and endocytosis jointly maintain PIN auxin carrier polarity at the plasma membrane. Mol. Syst. Biol. 7, 540. doi: 10.1038/msb.2011.72
18. Li, R., Liu, P., Wan, Y., Chen, T., Wang, Q., Mettbach, U., et al. (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 doi: 10.1105/tpc.112. 095695
19. Li, X., Wang, X., Yang, Y., Li, R., He, Q., Fang, X., et al. (2011). Single-molecule analysis of PIP2;1 dynamics and partitioning reveals multiple modes of Arabidopsis plasmamembrane aquaporinregulation. PlantCell. 23, 3780-3797. doi: 10.1105/tpc.111.091454
20. Luu, D. T., Martiniere, A., Sorieul, M., Runions, J., and Maurel, C. (2012). Fluorescence recovery after photobleaching reveals high cycling dynamics of plasma membrane aquaporins in Arabidopsis roots under salt stress. Plant J. 69, 894-905. doi: 10.1111/j.1365-313X.2011. 04841.x
21. Maglione, M. and Sigrist, S. J. (2013). Seeing the forest tree by tree: super-resolution light microscopy meets the neurosciences. Nat. Neurosci. 16, 790-797. doi: 10.1038/nn.3403
22. Mai, J., Trump, S., Lehmann, I., and Attinger, S. (2013). Parameter importance in FRAP acquisition and analysis: a simulation approach. Biophys. J. 104, 2089-2097. doi: 10.1016/j.bpj.2013.03.036
23. Malinsky, J., Opekarova, M., Grossmann, G., and Tanner, W. (2013). Membrane microdomains, rafts, and detergent-resistant membranes in plants and fungi. Annu. Rev. Plant Biol. 64, 501-529. doi: 10.1146/annurev-arplant-050312- 120103
24. Martiniere, A., Gayral, P., Hawes, C., and Runions, J. (2011). Building bridges: formin1 of Arabidopsis forms a connection between the cell wall and the actin cytoskeleton. Plant J. 66, 354-365. doi: 10.1111/j.1365-313X.2011. 04497.x
25. Martiniere, A., Lavagi, I., Nageswaran, G., Rolfe, D. J., Maneta-Peyret, L., Luu, D. T., et al. (2012). Cell wall constrains lateral diffusion of plant plasmamembrane proteins. Proc. Natl. Acad. Sci. U.S.A. 109, 12805-12810. doi: 10.1073/pnas.1202040109
26. Men, S., Boutte, Y., Ikeda, Y., Li, X., Palme, K., Stierhof, Y. D., et al. (2008). Sterol-dependent endocytosis mediates post-cytokinetic acquisition of PIN2 auxin efflux carrier polarity. Nat. Cell Biol. 10, 237-244. doi: 10.1038/ ncb1686
27. Nicolson, G. L. (2013). The Fluid-Mosaic Model of Membrane Structure: Still relevant to understanding the structure, function and dynamics of biological membranes after more than 40 years. Biochim. Biophys. Acta doi: 10.1016/j. bbamem.2013.10.019. [Epub ahead of print].
28. Oancea, E., Teruel, M. N., Quest, A. F. G., and Meyer, T. (1998). Green fluorescent protein (GFP)-tagged cysteine-rich domains from protein kinase C as fluorescent indicators for diacylglycerol signaling in living cells. J. Cell. Biol. 140, 485-498 doi: 10.1083/jcb.140.3.485
29. Owen, D. M., Williamson, D., Rentero, C., and Gaus, K. (2009). Quantitative microscopy: protein dynamics and membrane organisation. Traffic. 10, 962-971. doi: 10.1111/j.1600-0854.2009.00908.x
30. Raffaele, S., Bayer, E., Lafarge, D., Cluzet, S., German Retana, S., Boubekeur, T., et al. (2009). Remorin, a solanaceae protein resident in membrane rafts and plasmodesmata, impairs potato virus X movement. Plant Cell. 21, 1541-1555. doi: 10.1105/tpc.108.064279
31. Roppolo, D., De Rybel, B., Tendon, V. D., Pfister, A., Alassimone, J., Vermeer, J. E., et al. (2011). A novel protein family mediates Casparian strip formation in the endodermis. Nature. 473, 380-383. doi: 10.1038/nature10070
32. Roppolo, D., and Geldner, N. (2012). Membrane and walls: who is master, who is servant? Curr. Opin. Plant Biol. 15, 608-617 doi: 10.1016/j.pbi.2012.09.009
33. Saffman, P. G. and Delbruck, M. (1975). Brownian motion in biological membranes. Proc. Natl. Acad. Sci. U.S.A. 72, 3111-3113. doi: 10.1073/pnas.72. 8.3111
34. Simons, K., and Gerl, M. J. (2010). Revitalizing membrane rafts: new tools and insights. Nat. Rev. Mol. Cell Biol. 11, 688-699. doi: 10.1038/nrm2977
35. Simons, K., and Ikonen, E. (1997). Functional rafts in cell membranes. Nature. 387, 569-572. doi: 10.1038/42408
36. Simon-Plas, F., Perraki, A., Bayer, E., Gerbeau-Pissot, P., and Mongrand, S. (2011). An upadte on plant membrane rafts. Curr. Opin. Plant. Biol. 14, 642-649. doi: 10.1016/j.pbi.2011.08.003
37. Singer, S. G., and Nicolson, G. L. (1972). The fluid mosaic model of the structure of cell membranes. Science, 18, 720-731. doi: 10.1126/science.175.4023.720
38. Sorieul, M., Santoni, V., Maurel, C. and Luu, D. T. (2011). Mechanisms and effects of retention of over-expressed aquaporin AtPIP2;1 in the endoplasmic reticulum. Traffic. 12, 473-482. doi: 10.1111/j.1600-0854.2010.01154.x
39. Spira, F., Mueller, N. S., Beck, G. Von Olshausen, P., Beig, J., and Wedlich- Soldner, R. (2012). Patchwork organization of the yeast plasma membrane into numerous coexisting domains. Nat. Cell Biol. 14, 640-648. doi: 10.1038/ ncb2487
40. Sprague, B., Pego, R. L., Stavreva, D. A., and McNally, J. G. (2004). Analysis of binding reactions by fluorescence recovery after photobleaching. Biophys J. 86, 3473-3495. doi: 10.1529/biophysj.103.026765
41. Steinwand, B. J., and Kieber, J. J. (2010). The role of receptor-like kinases in regulating cell wall function. Plant Physiol. 153, 479-484. doi: 10.1104/pp.110. 155887
42. Sutter, J. U., Campanoni, P., Tyrrell, M., and Blatt, M. R. (2006). Selective mobility and sensitivity to SNAREs is exhibited by the Arabidopsis KAT1 K+ channel at the plasma membrane. Plant Cell. 18, 935-954. doi: 10.1105/tpc.105. 038950
43. Takano, J., Tanaka, M., Toyoda, A., Miwa, K., Kasai, K., Fuji, K., et al. (2010). Polar localization and degradation of Arabidopsis boron transporters through distinct trafficking pathways. Proc. Natl. Acad. Sci. U.S.A. 107, 5220-5225. doi: 10.1073/pnas.0910744107
44. Tomishige, M., Sako, Y., and Kusumi, A. (1998). Regulation mechanism of the lateral diffusion of band 3 in erythrocyte membranes by the membrane skeleton. J. Cell. Biol. 142, 989-1000. doi: 10.1083/jcb.142.4.989
45. Umenishi, F., Verbavatz, J. M., and Verkman, A. S. (2000). cAMP regulated membrane diffusion of a green fluorescent protein-aquaporin chimera. Biophys. J. 78, 1024-1035. doi: 10.1016/S0006-3495(00) 76661-6
46. Wang, Q., Zhao, Y., Luo, W., Li, R., He, Q., Fang, X., et al. (2013). Single-particle analysis reveals shutoff control of the Arabidopsis ammonium transporter AMT1;3 by clustering and internalization. Proc. Natl. Acad. Sci. U.S.A. 110, 13204-13209. doi: 10.1073/pnas. 1301160110
47. Yang, J., Kohler, K., Davis, D. M., and Burroughs, N. J. (2010). An improved strip FRAP method for estimating diffusion coefficients: correcting for the degree of photobleaching. J. Microsc. 238, 240-253. doi: 10.1111/j.1365- 2818.2009.03347.x