Plasma membrane domains enriched in cortical endoplasmic reticulum function as membrane protein trafficking hubs

Molecular Biology of the Cell

Volumn 24, Issue 17, 2013, Pages 2703-2713

  Fox, Philip D ^a   Haberkorn, Christopher J ^a   Weigel, Aubrey V ^b   Higgins, Jenny L ^b   Akin, Elizabeth J ^a   Kennedy, Matthew J ^c   Krapf, Diego ^b   Tamkun, Michael M ^a  

^a Department of Environmental and Radiological Health Sciences   (United States)

^b Engineering Research Center and Hydraulics Laboratory   (United States)

^c UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURFACE PROTEIN; MEMBRANE PROTEIN;

ARTICLE; CELL FUNCTION; CELL MEMBRANE; CELL MIGRATION; CELL STRAIN HEK293; CONTROLLED STUDY; ELECTRON MICROSCOPY; ENDOCYTOSIS; ENDOPLASMIC RETICULUM; EXOCYTOSIS; FLUORESCENCE MICROSCOPY; INTERNAL REFLECTANCE FLUORESCENCE MICROSCOPY; MOLECULAR BIOLOGY; PRIORITY JOURNAL;

CELL MEMBRANE; CELL MOVEMENT; CLATHRIN; ENDOCYTOSIS; ENDOPLASMIC RETICULUM; EXOCYTOSIS; HEK293 CELLS; HUMANS; KV1.4 POTASSIUM CHANNEL; MEMBRANE PROTEINS; MICROSCOPY, FLUORESCENCE; PROTEIN TRANSPORT; RECEPTORS, TRANSFERRIN; SHAB POTASSIUM CHANNELS;

EID: 84883418325     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E12-12-0895     Document Type: Article

References (58)

1. Antonucci DE, Lim ST, Vassanelli S, Trimmer JS (2001). Dynamic localization and clustering of dendritic Kv2.1 voltage-dependent potassium channels in developing hippocampal neurons. Neuroscience 108, 69-81.
2. Barlow AL, Macleod A, Noppen S, Sanderson J, Guerin CJ (2010). Colocalization analysis in fluorescence micrographs: verification of a more accurate calculation of Pearson's correlation coefficient. Microsc Microanal 16, 710-724.
3. Bellve KD, Leonard D, Standley C, Lifshitz LM, Tuft RA, Hayakawa A, Corvera S, Fogarty KE (2006). Plasma membrane domains specialized for clathrin-mediated endocytosis in primary cells. J Biol Chem 281, 16139-16146.
4. Cao H, Krueger EW, McNiven MA (2011). Hepatocytes internalize trophic receptors at large endocytic "hot spots." Hepatology 54, 1819-1829.
5. Carrasco S, Meyer T (2011). STIM proteins and the endoplasmic reticulum-plasma membrane junctions. Annu Rev Biochem 80, 973-1000.
6. Chivers CE, Crozat E, Chu C, Moy VT, Sherratt DJ, Howarth M (2010). A streptavidin variant with slower biotin dissociation and increased mechanostability. Nat Methods 7, 391-393.
7. Deutsch E, Weigel AV, Akin EJ, Fox P, Hansen G, Haberkorn CJ, Loftus R, Krapf D, Tamkun MM (2012). Kv2.1 cell surface clusters are insertion platforms for ion channel delivery to the plasma membrane. Mol Biol Cell 23, 2917-2929.
8. + channel, Kv2.1, is apposed to astrocytic processes and is associated with inhibitory postsynaptic membranes in hippocampal and cortical principal neurons and inhibitory interneurons. Neuroscience 84, 37-48.
9. Ehrlich M, Boll W, Van Oijen A, Hariharan R, Chandran K, Nibert ML, Kirchhausen T (2004). Endocytosis by random initiation and stabilization of clathrin-coated pits. Cell 118, 591-605.
10. Gaidarov I, Santini F, Warren RA, Keen JH (1999). Spatial control of coated-pit dynamics in living cells. Nat Cell Bio 1, 1-7.
11. Hopkins CR (1985). The appearance and internalization of transferrin receptors at the margins of spreading human tumor cells. Cell 40, 199-208.
12. Howarth M, Chinnapen DJ-F, Gerrow K, Dorrestein PC, Grandy MR, Kelleher NL, El-Husseini A, Ting AY (2006). A monovalent streptavidin with a single femtomolar biotin binding site. Nat Methods 3, 267-273.
13. Jahn R, Sudhof TC (1999). Membrane fusion and exocytosis. Annu Rev Biochem 68, 863-911.
14. Jaiswal JK, Goldman ER, Mattoussi H, Simon SM (2004). Use of quantum dots for live cell imaging. Nat Methods 1, 73-78.
15. Jaiswal JK, Simon SM (2004). Potentials and pitfalls of fluorescent quantum dots for biological imaging. Trends Cell Biol 14, 497-504.
16. Jaqaman K, Loerke D, Mettlen M, Kuwata H, Grinstein S, Schmid SL, Danuser G (2008). Robust single-particle tracking in live-cell time-lapse sequences. Nat Methods 5, 695-702.
17. Jing SQ, Spencer T, Miller K, Hopkins C, Trowbridge IS (1990). Role of the human transferrin receptor cytoplasmic domain in endocytosis: localization of a specific signal sequence for internalization. J Cell Biol 110, 283-294.
18. Keller P, Toomre D, Diaz E, White J, Simons K (2001). Multicolour imaging of post-Golgi sorting and trafficking in live cells. Nat Cell Biol 3, 140-149.
19. Kennedy MJ, Davison IG, Robinson CG, Ehlers MD (2010). Syntaxin-4 defines a domain for activity-dependent exocytosis in dendritic spines. Cell 141, 524-535.
20. Klopfenstein DR, Kappeler F, Hauri HP (1998). A novel direct interaction of endoplasmic reticulum with microtubules. EMBO J 17, 6168-6177.
21. 2+ influx. Curr Biol 15, 1235-1241.
22. Loerke D, Mettlen M, Yarar D, Jaqaman K, Jaqaman H, Danuser G, Schmid SL (2009). Cargo and dynamin regulate clathrin-coated pit maturation. PLoS Biol 7, e57.
23. 2+ transients control exo-endocytosis of synaptic-like microvesicles in astrocytes. J Neurosci 28, 9122-9132.
24. McMahon HT, Boucrot E (2011). Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat Rev Mol Cell Biol 12, 517-533.
25. McNiven MA (2006). Big gulps: specialized membrane domains for rapid receptor-mediated endocytosis. Trends Cell Biol 16, 487-492.
26. Mettlen M, Loerke D, Yarar D, Danuser G, Schmid SL (2010). Cargo- and adaptor-specific mechanisms regulate clathrin-mediated endocytosis. J Cell Biol 188, 919-933.
27. Miesenbock G, De Angelis DA, Rothman JE (1998). Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394, 192-195.
28. Miller K, Shipman M, Trowbridge IS, Hopkins CR (1991). Transferrin receptors promote the formation of clathrin lattices. Cell 65, 621-632.
29. Motley A, Bright NA, Seaman MN, Robinson MS (2003). Clathrin-mediated endocytosis in AP-2-depleted cells. J Cell Biol 162, 909-918.
30. Muennich EAL, Fyffe REW (2004). Focal aggregation of voltage-gated, Kv2.1 subunit-containing, potassium channels at synaptic sites in rat spinal motoneurones. J Physiol 554, 673-685.
31. Nunez D, Antonescu C, Mettlen M, Liu A, Schmid SL, Loerke D, Danuser G (2011). Hotspots organize clathrin-mediated endocytosis by efficient recruitment and retention of nucleating resources. Traffic 12, 1868-1878.
32. + channel. Proc Natl Acad Sci USA 107, 12351-12356.
33. O'Connell KM, Rolig AS, Whitesell JD, Tamkun MM (2006). Kv2.1 potassium channels are retained within dynamic cell surface microdomains that are defined by a perimeter fence. J Neurosci 26, 9609-9618.
34. O'Connell KM, Tamkun MM (2005). Targeting of voltage-gated potassium channel isoforms to distinct cell surface microdomains. J Cell Sci 118, 2155-2166.
35. Orci L, Gabbay KH, Malaisse WJ (1972). Pancreatic beta-cell web: its possible role in insulin secretion. Science 175, 1128-1130.
36. Orci L, Ravazzola M, Le Coadic M, Shen WW, Demaurex N, Cosson P (2009). From the cover: STIM1-induced precortical and cortical subdomains of the endoplasmic reticulum. Proc Natl Acad Sci USA 106, 19358-19362.
37. Petrini EM, Lu JY, Cognet L, Lounis B, Ehlers MD, Choquet D (2009). Endocytic trafficking and recycling maintain a pool of mobile surface AMPA receptors required for synaptic potentiation. Neuron 63, 92-105.
38. Presley JF, Cole NB, Schroer TA, Hirschberg K, Zaal KJ, Lippincott-Schwartz J (1997). ER-to-Golgi transport visualized in living cells. Nature 389, 81-85.
39. Rappoport JZ, Kemal S, Benmerah A, Simon SM (2006). Dynamics of clathrin and adaptor proteins during endocytosis. Am J Physiol Cell Physiol 291, C1072-C1081.
40. Robinson IM, Finnegan JM, Monck JR, Wightman RM, Fernandez JM (1995). Colocalization of calcium entry and exocytotic release sites in adrenal chromaffin cells. Proc Natl Acad Sci USA 92, 2474-2478.
41. Robinson IM, Yamada M, Carrion-Vazquez M, Lennon VA, Fernandez JM (1996). Specialized release zones in chromaffin cells examined with pulsed-laser imaging. Cell Calcium 20, 181-201.
42. Rosenbluth J (1962). Subsurface cisterns and their relationship to the neuronal plasma membrane. J Cell Biol 13, 405-421.
43. Russ JC (2007). The Image Processing Handbook, 5th ed., Boca Raton, FL: CRC.
44. Saffarian S, Cocucci E, Kirchhausen T (2009). Distinct dynamics of endocytic clathrin-coated pits and coated plaques. PLoS Biol 7, e1000191.
45. Schroeder TJ, Jankowski JA, Senyshyn J, Holz RW, Wightman RM (1994). Zones of exocytotic release on bovine adrenal medullary cells in culture. J Biol Chem 269, 17215-17220.
46. Sergé A, Bertaux N, Rigneault H, Marguet D (2008). Dynamic multiple-target tracing to probe spatiotemporal cartography of cell membranes. Nat Methods 5, 687-694.
47. Shaw G, Morse S, Ararat M, Graham FL (2002). Preferential transformation of human neuronal cells by human adenoviruses and the origin of HEK 293 cells. FASEB J 16, 869-871.
48. Spiliotis ET, Nelson WJ (2003). Spatial control of exocytosis. Curr Opin Cell Biol 15, 430-437.
49. Stenkula KG, Lizunov VA, Cushman SW, Zimmerberg J (2010). Insulin controls the spatial distribution of GLUT4 on the cell surface through regulation of its postfusion dispersal. Cell Metab 12, 250-259.
50. Sudhof TC (2004). The synaptic vesicle cycle. Annu Rev Neurosci 27, 509-547.
51. Sudhof TC, Rizo J (2011). Synaptic vesicle exocytosis. Cold Spring Harb Perspect Biol 3, a005637.
52. Stradalova V, Blazikova M, Grossmann G, Opekarova M, Tanner W, Malinsky J (2012). Distribution of cortical endoplasmic reticulum determines positioning of endocytic events in yeast plasma membrane. PLoS One 7, e35132.
53. Tamkun MM, O'Connell KM, Rolig AS (2007). A cytoskeletal-based perimeter fence selectively corrals a sub-population of cell surface Kv2.1 channels. J Cell Sci 120, 2413-2423.
54. Terasaki M, Chen LB, Fujiwara K (1986). Microtubules and the endoplasmic reticulum are highly interdependent structures. J Cell Biol 103, 1557-1568.
55. Toomre D, Steyer JA, Keller P, Almers W, Simons K (2000). Fusion of constitutive membrane traffic with the cell surface observed by evanescent wave microscopy. J Cell Biol 149, 33-40.
56. Waterman-Storer CM, Salmon ED (1998). Endoplasmic reticulum membrane tubules are distributed by microtubules in living cells using three distinct mechanisms. Curr Biol 8, 798-806.
57. Weigel AV, Simon B, Tamkun MM, Krapf D (2011). Ergodic and nonergodic processes coexist in the plasma membrane as observed by single-molecule tracking. Proc Natl Acad Sci USA 108, 6438-6443.
58. Wick PF, Trenkle JM, Holz RW (1997). Punctate appearance of dopamine-β-hydroxylase on the chromaffin cell surface reflects the fusion of individual chromaffin granules upon exocytosis. Neuroscience 80, 847-860.