Receptor heteromeric assembly - How it works and why it matters: The case of ionotropic glutamate receptors

Progress in Molecular Biology and Translational Science

Volumn 117, Issue , 2013, Pages 361-386

  Herguedas, Beatriz ^a   Krieger, James ^a   Greger, Ingo H ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

Assembly domain; Assembly interface; Glutamate receptor tetramer; iGluR N terminal domain; Ion channels; Receptor oligomerization

Indexed keywords

CATION CHANNEL; GLUTAMATE RECEPTOR; GLUTAMIC ACID; ION CHANNEL; IONOTROPIC RECEPTOR; OLIGOMER; TETRAMER; VOLTAGE GATED POTASSIUM CHANNEL;

ANIMAL; ARTICLE; BINDING AFFINITY; BIOGENESIS; CELL TYPE; CHANNEL GATING; CHEMICAL STRUCTURE; CRYSTAL STRUCTURE; ENDOPLASMIC RETICULUM; HUMAN; METABOLISM; NEUROTRANSMISSION; NONHUMAN; PHYSIOLOGY; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN MULTIMERIZATION; STOICHIOMETRY; SYNAPTIC TRANSMISSION;

EID: 84896729678     PISSN: 18771173     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-386931-9.00013-1     Document Type: Chapter

References (127)

1. M. Lynch The evolution of multimeric protein assemblages Mol Biol Evol 29 5 2012 1353 1366
2. J.B. Pereira-Leal, E.D. Levy, C. Kamp, and S.A. Teichmann Evolution of protein complexes by duplication of homomeric interactions Genome Biol 8 4 2007 R51
3. M.E. Call, and K.W. Wucherpfennig Common themes in the assembly and architecture of activating immune receptors Nat Rev Immunol 7 11 2007 841 850
4. M.E. Call, J. Pyrdol, and K.W. Wucherpfennig Stoichiometry of the T-cell receptor-CD3 complex and key intermediates assembled in the endoplasmic reticulum EMBO J 23 12 2004 2348 2357
5. K.A. Jones, B. Borowsky, J.A. Tamm, D.A. Craig, M.M. Durkin, and M. Dai GABA(B) receptors function as a heteromeric assembly of the subunits GABA(B)R1 and GABA(B)R2 Nature 396 6712 1998 674 679
6. Y. Geng, D. Xiong, L. Mosyak, D.L. Malito, J. Kniazeff, and Y. Chen Structure and functional interaction of the extracellular domain of human GABA(B) receptor GBR2 Nat Neurosci 15 7 2012 970 978
7. C.P. Wanamaker, J.C. Christianson, and W.N. Green Regulation of nicotinic acetylcholine receptor assembly Ann N Y Acad Sci 998 2003 66 80
8. S. Cull-Candy, S. Brickley, and M. Farrant NMDA receptor subunits: diversity, development and disease Curr Opin Neurobiol 11 2001 327 335
9. V. Tsetlin, D. Kuzmin, and I. Kasheverov Assembly of nicotinic and other Cys-loop receptors J Neurochem 116 5 2011 734 741
10. L.J. Wu, T.B. Sweet, and D.E. Clapham International Union of Basic and Clinical Pharmacology. LXXVI. Current progress in the mammalian TRP ion channel family Pharmacol Rev 62 3 2010 381 404
11. J. Zheng, and W.N. Zagotta Stoichiometry and assembly of olfactory cyclic nucleotide-gated channels Neuron 42 3 2004 411 421
12. W. Lu, Y. Shi, A.C. Jackson, K. Bjorgan, M.J. During, and R. Sprengel Subunit composition of synaptic AMPA receptors revealed by a single-cell genetic approach Neuron 62 2 2009 254 268
13. J.T. Isaac, M. Ashby, and C.J. McBain The role of the GluR2 subunit in AMPA receptor function and synaptic plasticity Neuron 54 2007 859 871
14. J.A. Kauer, and R.C. Malenka Synaptic plasticity and addiction Nat Rev Neurosci 8 11 2007 844 858
15. M.A. Sutton, H.T. Ito, P. Cressy, C. Kempf, J.C. Woo, and E.M. Schuman Miniature neurotransmission stabilizes synaptic function via tonic suppression of local dendritic protein synthesis Cell 125 4 2006 785 799
16. S.F. Traynelis, L.P. Wollmuth, C.J. McBain, F.S. Menniti, K.M. Vance, and K.K. Ogden Glutamate receptor ion channels: structure, regulation, and function Pharmacol Rev 62 3 2010 405 496
17. T. Cui-Wang, C. Hanus, T. Cui, T. Helton, J. Bourne, and D. Watson Local zones of endoplasmic reticulum complexity confine cargo in neuronal dendrites Cell 148 1-2 2012 309 321
18. L. Ellgaard, and A. Helenius Quality control in the endoplasmic reticulum Nat Rev Mol Cell Biol 4 2003 181 191
19. S. Nehls, E.L. Snapp, N.B. Cole, K.J. Zaal, A.K. Kenworthy, and T.H. Roberts Dynamics and retention of misfolded proteins in native ER membranes Nat Cell Biol 2 5 2000 288 295
20. N.G. Shuart, Y. Haitin, S.S. Camp, K.D. Black, and W.N. Zagotta Molecular mechanism for 3:1 subunit stoichiometry of rod cyclic nucleotide-gated ion channels Nat Commun 2 2012 457
21. J. Kumar, and M.L. Mayer Functional insights from glutamate receptor ion channel structures Annu Rev Physiol 75 2013 313 337
22. M.L. Mayer Structure and mechanism of glutamate receptor ion channel assembly, activation and modulation Curr Opin Neurobiol 21 2 2011 283 290
23. A.C. Penn, and I.H. Greger Sculpting AMPA receptor formation and function by alternative RNA processing RNA Biol 6 5 2009 517 522
24. M. Sukumaran, A.C. Penn, and I.H. Greger AMPA receptor assembly: atomic determinants and built-in modulators Adv Exp Med Biol 970 2012 241 264
25. 2 +-permeable AMPA receptors: synaptic plasticity and beyond Curr Opin Neurobiol 16 2006 288 297
26. S. Kwak, and J.H. Weiss Calcium-permeable AMPA channels in neurodegenerative disease and ischemia Curr Opin Neurobiol 16 3 2006 281 287
27. 2 +-permeable AMPA receptors in synaptic plasticity and neuronal death Trends Neurosci 30 2007 126 134
28. A.M. Batchelor, T. Knopfel, F. Gasparini, and J. Garthwaite Pharmacological characterization of synaptic transmission through mGluRs in rat cerebellar slices Neuropharmacology 36 3 1997 401 403
29. M. Yuzaki New (but old) molecules regulating synapse integrity and plasticity: Cbln1 and the delta2 glutamate receptor Neuroscience 162 3 2009 633 643
30. B.A. Copits, and G.T. Swanson Dancing partners at the synapse: auxiliary subunits that shape kainate receptor function Nat Rev Neurosci 13 10 2012 675 686
31. S.J. Guzman, and P. Jonas Beyond TARPs: the growing list of auxiliary AMPAR subunits Neuron 66 1 2010 8 10
32. A.C. Jackson, and R.A. Nicoll The expanding social network of ionotropic glutamate receptors: TARPs and other transmembrane auxiliary subunits Neuron 70 2 2011 178 199
33. J. Schwenk, N. Harmel, A. Brechet, G. Zolles, H. Berkefeld, and C.S. Müller High-resolution proteomics unravel architecture and molecular diversity of native AMPA receptor complexes Neuron 74 4 2012 621 633
34. N.F. Shanks, J.N. Savas, T. Maruo, O. Cais, A. Hirao, and S. Oe Differences in AMPA and kainate receptor interactomes facilitate identification of AMPA receptor auxiliary subunit GSG1L Cell Rep 1 6 2012 590 598
35. A.J. Norris, N.C. Foeger, and J.M. Nerbonne Neuronal voltage-gated K + (Kv) channels function in macromolecular complexes Neurosci Lett 486 2 2010 73 77
36. J. Schwenk, N. Harmel, G. Zolles, W. Bildl, A. Kulik, and B. Heimrich Functional proteomics identify cornichon proteins as auxiliary subunits of AMPA receptors Science 323 5919 2009 1313 1319
37. S. Tomita, H. Adesnik, M. Sekiguchi, W. Zhang, K. Wada, and J.R. Howe Stargazin modulates AMPA receptor gating and trafficking by distinct domains Nature 435 7045 2005 1052 1058
38. J. von Engelhardt, V. Mack, R. Sprengel, N. Kavenstock, K.W. Li, and Y. Stern-Bach CKAMP44: a brain-specific protein attenuating short-term synaptic plasticity in the dentate gyrus Science 327 5972 2010 1518 1522
39. W. Zhang, Y. Cho, E. Lolis, and J.R. Howe Structural and single-channel results indicate that the rates of ligand binding domain closing and opening directly impact AMPA receptor gating J Neurosci 28 4 2008 932 943
40. G. Ayalon, and Y. Stern-Bach Functional assembly of AMPA and kainate receptors is mediated by several discrete protein-protein interactions Neuron 31 2001 103 113
41. + channel assembly Biophys J 76 4 1999 2004 2017
42. T. Nakagawa The biochemistry, ultrastructure, and subunit assembly mechanism of AMPA receptors Mol Neurobiol 42 3 2010 161 184
43. N.F. Shanks, T. Maruo, A.N. Farina, M.H. Ellisman, and T. Nakagawa Contribution of the global subunit structure and stargazin on the maturation of AMPA receptors J Neurosci 30 7 2010 2728 2740
44. C. Rosenmund, Y. Stern-Bach, and C.F. Stevens The tetrameric structure of a glutamate receptor channel Science 280 1998 1596 1599
45. I.H. Greger, L. Khatri, X. Kong, and E.B. Ziff AMPA receptor tetramerization is mediated by Q/R editing Neuron 40 2003 763 774
46. M.L. Mayer Glutamate receptors at atomic resolution Nature 440 7083 2006 456 462
47. T. Nakagawa, Y. Cheng, E. Ramm, M. Sheng, and T. Walz Structure and different conformational states of native AMPA receptor complexes Nature 433 7025 2005 545 549
48. W. Tichelaar, M. Safferling, K. Keinanen, H. Stark, and D.R. Madden The three-dimensional structure of an ionotropic glutamate receptor reveals a dimer-of-dimers assembly J Mol Biol 344 2 2004 435 442
49. A. Reiner, R.J. Arant, and E.Y. Isacoff Assembly stoichiometry of the GluK2/GluK5 kainate receptor complex Cell Rep 1 3 2012 234 240
50. A.I. Sobolevsky, M.P. Rosconi, and E. Gouaux X-ray structure, symmetry and mechanism of an AMPA-subtype glutamate receptor Nature 462 2009 745 756
51. N. Armstrong, Y. Sun, G.Q. Chen, and E. Gouaux Structure of a glutamate-receptor ligand-binding core in complex with kainate Nature 395 1998 913 917
52. I.H. Greger, E.B. Ziff, and A.C. Penn Molecular determinants of AMPA receptor subunit assembly Trends Neurosci 30 2007 407 416
53. M. Rossmann, M. Sukumaran, A.C. Penn, D.B. Veprintsev, M.M. Babu, and I.H. Greger Subunit-selective N-terminal domain associations organize the formation of AMPA receptor heteromers EMBO J 30 2011 959 971
54. H. Zhao, A.J. Berger, P.H. Brown, J. Kumar, A. Balbo, and C.A. May Analysis of high-affinity assembly for AMPA receptor amino-terminal domains J Gen Physiol 139 5 2012 371 388
55. E. Karakas, N. Simorowski, and H. Furukawa Subunit arrangement and phenylethanolamine binding in GluN1/GluN2B NMDA receptors Nature 475 7355 2012 249 253
56. F.A. Quiocho, and P.S. Ledvina Atomic structure and specificity of bacterial periplasmic receptors for active transport and chemotaxis: variation of common themes Mol Microbiol 20 1996 17 25
57. A. Clayton, C. Siebold, R.J. Gilbert, G.C. Sutton, K. Harlos, and R.A. McIlhinney Crystal structure of the GluR2 amino-terminal domain provides insights into the architecture and assembly of ionotropic glutamate receptors J Mol Biol 392 5 2009 1125 1132
58. R. Jin, S.K. Singh, S. Gu, H. Furukawa, A.I. Sobolevsky, and J. Zhou Crystal structure and association behaviour of the GluR2 amino-terminal domain EMBO J 28 12 2009 1812 1823
59. J. Kumar, and M.L. Mayer Crystal structures of the glutamate receptor ion channel GluK3 and GluK5 amino-terminal domains J Mol Biol 404 4 2010 680 696
60. J. Kumar, P. Schuck, R. Jin, and M.L. Mayer The N-terminal domain of GluR6-subtype glutamate receptor ion channels Nat Struct Mol Biol 16 6 2009 631 638
61. A. Dutta, I.H. Shrivastava, M. Sukumaran, I.H. Greger, and I. Bahar Comparative dynamics of NMDA- and AMPA-glutamate receptor N-terminal domains Structure 20 11 2012 1838 1849
62. R.P. Bahadur, P. Chakrabarti, F. Rodier, and J. Janin A dissection of specific and non-specific protein-protein interfaces J Mol Biol 336 4 2004 943 955
63. M. Sukumaran, M. Rossmann, I. Shrivastava, A. Dutta, I. Bahar, and I.H. Greger Dynamics and allosteric potential of the AMPA receptor N-terminal domain EMBO J 30 5 2011 972 982
64. J. Kumar, P. Schuck, and M.L. Mayer Structure and assembly mechanism for heteromeric kainate receptors Neuron 71 2 2011 319 331
65. A.N. Farina, K.Y. Blain, T. Maruo, W. Kwiatkowski, S. Choe, and T. Nakagawa Separation of domain contacts is required for heterotetrameric assembly of functional NMDA receptors J Neurosci 31 10 2011 3565 3579
66. P.T. Atlason, M.L. Garside, E. Meddows, P. Whiting, and R.A. McIlhinney N-Methyl-D-aspartate (NMDA) receptor subunit NR1 forms the substrate for oligomeric assembly of the NMDA receptor J Biol Chem 282 35 2007 25299 25307
67. J.P. Pin, T. Galvez, and L. Prezeau Evolution, structure, and activation mechanism of family 3/C G-protein-coupled receptors Pharmacol Ther 98 3 2003 325 354
68. X. He, D. Chow, M.M. Martick, and K.C. Garcia Allosteric activation of a spring-loaded natriuretic peptide receptor dimer by hormone Science 293 5535 2001 1657 1662
69. N. Kunishima, Y. Shimada, Y. Tsuji, T. Sato, M. Yamamoto, and T. Kumasaka Structural basis of glutamate recognition by a dimeric metabotropic glutamate receptor Nature 407 6807 2000 971 977
70. L. Mony, S. Zhu, S. Carvalho, and P. Paoletti Molecular basis of positive allosteric modulation of GluN2B NMDA receptors by polyamines EMBO J 30 15 2011 3134 3146
71. E. Doumazane, P. Scholler, J.M. Zwier, E. Trinquet, P. Rondard, and J.P. Pin A new approach to analyze cell surface protein complexes reveals specific heterodimeric metabotropic glutamate receptors FASEB J 25 1 2011 66 77
72. C. Cui, and M.L. Mayer Heteromeric kainate receptors formed by the coassembly of GluR5, GluR6, and GluR7 J Neurosci 19 19 1999 8281 8291
73. M. Gielen, B. Siegler Retchless, L. Mony, J.W. Johnson, and P. Paoletti Mechanism of differential control of NMDA receptor activity by NR2 subunits Nature 459 7247 2009 703 707
74. D. Perrais, J. Veran, and C. Mulle Gating and permeation of kainate receptors: differences unveiled Trends Pharmacol Sci 31 11 2010 516 522
75. G.T. Swanson, T. Green, R. Sakai, A. Contractor, W. Che, H. Kamiya, and S.F. Heinemann Differential activation of individual subunits in heteromeric kainate receptors Neuron 34 4 2002 589 598
76. U. Das, J. Kumar, M.L. Mayer, and A.J. Plested Domain organization and function in GluK2 subtype kainate receptors Proc Natl Acad Sci USA 107 18 2010 8463 8468
77. I.H. Greger, P. Akamine, L. Khatri, and E.B. Ziff Developmentally regulated, combinatorial RNA processing modulates AMPA receptor biogenesis Neuron 51 2006 85 97
78. A.C. Penn, S.R. Williams, and I.H. Greger Gating motions underlie AMPA receptor secretion from the endoplasmic reticulum EMBO J 27 22 2008 3056 3068
79. P.H. Seeburg The role of RNA editing in controlling glutamate receptor channel properties J Neurochem 66 1996 1 5
80. S.K. Coleman, T. Moykkynen, A. Jouppila, S. Koskelainen, C. Rivera, E.R. Korpi, and K. Keinänen Agonist occupancy is essential for forward trafficking of AMPA receptors J Neurosci 29 2 2009 303 312
81. M.B. Gill, P. Vivithanaporn, and G.T. Swanson Glutamate binding and conformational flexibility of ligand-binding domains are critical early determinants of efficient kainate receptor biogenesis J Biol Chem 284 21 2009 14503 14512
82. S.J. Mah, E. Cornell, N.A. Mitchell, and M.W. Fleck Glutamate receptor trafficking: endoplasmic reticulum quality control involves ligand binding and receptor function J Neurosci 25 9 2005 2215 2225
83. A.V. Kenny, S.L. Cousins, L. Pinho, and F.A. Stephenson The integrity of the glycine co-agonist binding site of N-methyl-D-aspartate receptors is a functional quality control checkpoint for cell surface delivery J Biol Chem 284 1 2009 324 333
84. K. She, J.S. Ferreira, A.L. Carvalho, and A.M. Craig Glutamate binding to the GluN2B subunit controls surface trafficking of N-methyl-D-aspartate (NMDA) receptors J Biol Chem 287 33 2012 27432 27445
85. A.C. Penn, A. Balik, C. Wozny, O. Cais, and I.H. Greger Activity-mediated AMPA receptor remodeling, driven by alternative splicing in the ligand-binding domain Neuron 76 3 2012 503 510
86. A. Balik, A.C. Penn, Z. Nemoda, and I.H. Greger Activity-regulated RNA editing in select neuronal subfields in hippocampus Nucleic Acids Res 41 2 2013 1124 1134
87. C.L. Salussolia, and L.P. Wollmuth Flip-flopping to the membrane Neuron 76 3 2012 463 465
88. C. Chaudhry, A.J. Plested, P. Schuck, and M.L. Mayer Energetics of glutamate receptor ligand binding domain dimer assembly are modulated by allosteric ions Proc Natl Acad Sci USA 106 30 2009 12329 12334
89. K.B. Hansen, P. Naur, N.L. Kurtkaya, A.S. Kristensen, M. Gajhede, J.S. Kastrup, and S.F. Traynelis Modulation of the dimer interface at ionotropic glutamate-like receptor delta2 by D-serine and extracellular calcium J Neurosci 29 4 2009 907 917
90. A.J. Plested, and M.L. Mayer Structure and mechanism of kainate receptor modulation by anions Neuron 53 2007 829 841
91. P. Vivithanaporn, L.L. Lash, W. Marszalec, and G.T. Swanson Critical roles for the M3-S2 transduction linker domain in kainate receptor assembly and postassembly trafficking J Neurosci 27 39 2007 10423 10433
92. C.H. Lee, and E. Gouaux Amino terminal domains of the NMDA receptor are organized as local heterodimers PLoS One 6 4 2011 e19180
93. M. Mansour, N. Nagarajan, R.B. Nehring, J.D. Clements, and C. Rosenmund Heteromeric AMPA receptors assemble with a preferred subunit stoichiometry and spatial arrangement Neuron 32 5 2001 841 853
94. M. Riou, D. Stroebel, J.M. Edwardson, and P. Paoletti An alternating GluN1-2-1-2 subunit arrangement in mature NMDA receptors PLoS One 7 4 2012 e35134
95. A. Pasternack, S.K. Coleman, A. Jouppila, D.G. Mottershead, M. Lindfors, M. Pasternack, and K. Keinäznen Alpha-amino-3-hydroxy-5-methyl-4- isoxazolepropionic acid (AMPA) receptor channels lacking the N-terminal domain J Biol Chem 277 51 2002 49662 49667
96. C.L. Salussolia, M.L. Prodromou, P. Borker, and L.P. Wollmuth Arrangement of subunits in functional NMDA receptors J Neurosci 31 31 2011 11295 11304
97. G.Q. Chen, C. Cui, M.L. Mayer, and E. Gouaux Functional characterization of a potassium-selective prokaryotic glutamate receptor Nature 402 6763 1999 817 821
98. T. Kuner, P.H. Seeburg, and H.R. Guy A common architecture for K + channels and ionotropic glutamate receptors? Trends Neurosci 26 1 2003 27 32
99. L.P. Wollmuth, and A.I. Sobolevsky Structure and gating of the glutamate receptor ion channel Trends Neurosci 27 6 2004 321 328
100. + conduction and selectivity Science 280 5360 1998 69 77
101. + channel Science 309 5736 2005 897 903
102. R. Sprengel, R. Aronoff, M. Volkner, B. Schmitt, R. Mosbach, and T. Kuner Glutamate receptor channel signatures Trends Pharmacol Sci 22 1 2001 7 10
103. M.S. Washburn, M. Numberger, S. Zhang, and R. Dingledine Differential dependence on GluR2 expression of three characteristic features of AMPA receptors J Neurosci 17 24 1997 9393 9406
104. D. Bowie Redefining the classification of AMPA-selective ionotropic glutamate receptors J Physiol 590 Pt 1 2012 49 61
105. 2 + permeability in both TM1 and TM2 of high affinity kainate receptor channels: diversity by RNA editing Neuron 10 3 1993 491 500
106. B. Sommer, M. Kohler, R. Sprengel, and P.H. Seeburg RNA editing in brain controls a determinant of ion flow in glutamate-gated channels Cell 67 1 1991 11 19
107. N. Burnashev, H. Monyer, P.H. Seeburg, and B. Sakmann Divalent ion permeability of AMPA receptor channels is dominated by the edited form of a single subunit Neuron 8 1 1992 189 198
108. I.H. Greger, L. Khatri, and E.B. Ziff RNA editing at Arg607 controls AMPA receptor exit from the endoplasmic reticulum Neuron 34 2002 759 772
109. R.I. Hume, R. Dingledine, and S.F. Heinemann Identification of a site in glutamate receptor subunits that controls calcium permeability Science 253 5023 1991 1028 1031
110. S.M. Ball, P.T. Atlason, O.O. Shittu-Balogun, and E. Molnar Assembly and intracellular distribution of kainate receptors is determined by RNA editing and subunit composition J Neurochem 114 6 2010 1805 1818
111. A. Bernard, L. Ferhat, F. Dessi, G. Charton, A. Repressa, Y. Ben-Ari, and M. Khrestchatisky Q/R editing of the rat GluR5 and GluR6 kainate receptors in vivo and in vitro: evidence for independent developmental, pathological and cellular regulation Eur J Neurosci 11 2 1999 604 616
112. N. Sans, B. Vissel, R.S. Petralia, Y.X. Wang, K. Chang, and G.A. Royle Aberrant formation of glutamate receptor complexes in hippocampal neurons of mice lacking the GluR2 AMPA receptor subunit J Neurosci 23 28 2003 9367 9373
113. R. Brusa, F. Zimmermann, D.S. Koh, D. Feldmeyer, P. Gass, P.H. Seeburg, and R. Sprengel Early-onset epilepsy and postnatal lethality associated with an editing-deficient GluR-B allele in mice Science 270 5242 1995 1677 1680
114. C.L. Salussolia, A. Corrales, I. Talukder, R. Kazi, G. Akgul, M. Bowen, and L.P. Wollmuth Interaction of the M4 segment with other transmembrane segments is required for surface expression of mammalian alpha-amino-3-hydroxy- 5-methyl-4-isoxazolepropionic acid (AMPA) receptors J Biol Chem 286 46 2011 40205 40218
115. M. Kaniakova, K. Lichnerova, L. Vyklicky, and M. Horak Single amino acid residue in the M4 domain of GluN1 subunit regulates the surface delivery of NMDA receptors J Neurochem 123 3 2012 385 395
116. O.B. Clarke, and J.M. Gulbis Oligomerization at the membrane: potassium channel structure and function Adv Exp Med Biol 747 2012 122 136
117. Z. Wang, Y. Jiang, L. Lu, R. Huang, Q. Hou, and F. Shi Molecular mechanisms of cyclic nucleotide-gated ion channel gating J Genet Genomics 34 6 2007 477 485
118. M. Li, Y.N. Jan, and L.Y. Jan Specification of subunit assembly by the hydrophilic amino-terminal domain of the Shaker potassium channel Science 257 5074 1992 1225 1230
119. J. Lu, J.M. Robinson, D. Edwards, and C. Deutsch T1-T1 interactions occur in ER membranes while nascent Kv peptides are still attached to ribosomes Biochemistry 40 37 2001 10934 10946
120. C. Deutsch Potassium channel ontogeny Annu Rev Physiol 64 2002 19 46
121. M. Schwake, D. Athanasiadu, C. Beimgraben, J. Blanz, C. Beck, and T.J. Jentsch Structural determinants of M-type KCNQ (Kv7) K + channel assembly J Neurosci 26 14 2006 3757 3766
122. J.C. Gomez-Posada, A. Etxeberria, M. Roura-Ferrer, P. Areso, M. Masin, R.D. Murrell-Lagnado, and A. Villarroel A pore residue of the KCNQ3 potassium M-channel subunit controls surface expression J Neurosci 30 27 2010 9316 9323
123. A.P. Stewart, J.C. Gomez-Posada, J. McGeorge, M.J. Rouhani, A. Villarroel, R.D. Murrell-Lagnado, and J.M. Edwardson The Kv7.2/Kv7.3 heterotetramer assembles with a random subunit arrangement J Biol Chem 287 15 2012 11870 11877
124. J. Ludwig, D. Owen, and O. Pongs Carboxy-terminal domain mediates assembly of the voltage-gated rat ether-a-go-go potassium channel EMBO J 16 21 1997 6337 6345
125. I.H. Chen, J.H. Hu, G.M. Jow, C.C. Chuang, T.T. Lee, D.J. Liu, and C.J. Jeng Distal end of carboxyl terminus is not essential for the assembly of rat Eag1 potassium channels J Biol Chem 286 31 2011 27183 27196
126. C. Peng, E.D. Rich, and M.D. Varnum Subunit configuration of heteromeric cone cyclic nucleotide-gated channels Neuron 42 3 2004 401 410
127. D. Weitz, N. Ficek, E. Kremmer, P.J. Bauer, and U.B. Kaupp Subunit stoichiometry of the CNG channel of rod photoreceptors Neuron 36 5 2002 881 889