Barcoding of GPCR trafficking and signaling through the various trafficking roadmaps by compartmentalized signaling networks

Cellular Signalling

Volumn 36, Issue , 2017, Pages 42-55

  Bahouth, Suleiman W ^a   Nooh, Mohammed M ^b  

^a UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^b CAIRO UNIVERSITY   (Egypt)

Author keywords

Endosomes; GPCR; GRK; PKA; Signaling; SNX27; Trafficking

Indexed keywords

ACTIN; BETA 1 ADRENERGIC RECEPTOR; BETA 2 ADRENERGIC RECEPTOR; BETA ARRESTIN; CHEMOKINE RECEPTOR CXCR4; CYCLIC AMP DEPENDENT PROTEIN KINASE; G PROTEIN COUPLED RECEPTOR; PARATHYROID HORMONE RECEPTOR 1; SORTING NEXIN;

CELL COMPARTMENTALIZATION; CLATHRIN-COATED VESICLE; DESENSITIZATION; ENDOCYTOSIS; ENDOSOME; GENETIC PROCEDURES; HUMAN; INTERNALIZATION; INTRACELLULAR SIGNALING; NONHUMAN; PRIORITY JOURNAL; PROTEIN BARCODING; PROTEIN PHOSPHORYLATION; REVIEW; SIGNAL TRANSDUCTION; UBIQUITINATION; ANIMAL; METABOLISM; PHYSIOLOGICAL FEEDBACK; PROTEIN PROCESSING; PROTEIN TRANSPORT;

ANIMALS; ENDOSOMES; FEEDBACK, PHYSIOLOGICAL; HUMANS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION;

EID: 85018866455     PISSN: 08986568     EISSN: 18733913     Source Type: Journal    
DOI: 10.1016/j.cellsig.2017.04.015     Document Type: Review

References (172)

1. [1] Katritch, V., Cherezov, V., Stevens, R.C., Structure-function of the G protein-coupled receptor superfamily. Annu. Rev. Pharmacol. Toxicol. 53 (2013), 531–556.
2. [2] Ellisdon, A.M., Halls, M.L., Compartmentalization of GPCR signalling controls unique cellular responses. Biochem. Soc. Trans. 44 (2016), 562–567.
3. [3] Langeberg, L.K., Scott, J.D., Signalling scaffolds and local organization of cellular behaviour. Nat. Rev. Mol. Cell Biol. 16 (2015), 232–244.
4. [4] Hanyaloglu, A.C., von Zastrow, M., Regulation of GPCRs by endocytic membrane trafficking and its potential implications. Annu. Rev. Pharmacol. Toxicol. 48 (2008), 537–568.
5. [5] Ferguson, S.S., Evolving concepts in G protein-coupled receptor endocytosis: the role in receptor desensitization and signaling. Pharmacol. Rev. 53 (2001), 1–24.
6. [6] Mohan, M.L., Vasudevan, N.T., Gupta, M.K., Martelli, E.E., Naga Prasad, S.V., G-protein coupled receptor resensitization-appreciating the balancing act of receptor function. Curr. Mol. Pharmacol. 5 (2012), 350–361.
7. [7] Irannejad, R., von Zastrow, M., GPCR signaling along the endocytic pathway. Curr. Opin. Cell Biol. 27 (2014), 109–116.
8. [8] Lefkowitz, R.J., Pitcher, J., Krueger, K., Daaka, Y., Mechanisms of β-adrenergic receptor desensitization and resensitization. Adv. Pharmacol. 42:1998 (1998), 416–420.
9. [9] Claing, A., Laporte, S.A., Caron, M.G., Lefkowitz, R.J., Endocytosis of G protein-coupled receptors: roles of G protein-coupled receptor kinases and β-arrestin proteins. Prog. Neurobiol. 66 (2002), 61–79.
10. [10] Shenoy, S.K., Lefkowitz, R.J., β-Arrestin-mediated receptor trafficking and signal transduction. Trends Pharmacol. Sci. 32 (2011), 521–533.
11. [11] Kendall, R.T., Strungs, E.G., Rachidi, S.M., Lee, M.H., El-Shewy, H.M., Luttrell, D.K., Janech, M.G., Luttrell, The β-arrestin pathway-selective type 1A angiotensin receptor (AT1A) agonist [Sar1, Ile4, Ile8] angiotensin II regulates a robust G protein-independent signaling network. J. Biol. Chem. 286 (2011), 19880–19891.
12. [12] Ferguson, S.S.G., Downey, W.E. III, Calapierto, A.M., Barak, L.S., Menard, L., Caron, M.G., Role of β-arrestin in mediating agonist-promoted G-protein-coupled receptor internalization. Science 271 (1996), 363–366.
13. [13] Maxfield, F.R., McGraw, T.E., Endocytic recycling. Nat. Rev. Mol. Cell Biol. 5 (2004), 121–132.
14. [14] Le Roy, C., Wrana, J.L., Clathrin- and non-clathrin-mediated endocytic regulation of cell signalling. Nat. Rev. Mol. Cell Biol. 6 (2005), 112–126.
15. [15] Gruenberg, J., The endocytic pathway: a mosaic of domains. Nat. Rev. Mol. Cell Biol. 2 (2001), 721–730.
16. [16] Conner, S.D., Schmid, S.L., Regulated portals of entry into the cell. Nature 422 (2003), 37–44.
17. [17] Miller, W.E., Lefkowitz, R.J., Expanding roles for β-arrestins as scaffolds and adapters in GPCR signaling and trafficking. Curr. Opin. Cell Biol. 13 (2001), 139–145.
18. [18] Cheng, Z.J., Singh, R.D., Marks, D.L., Pagano, R.E., Membrane microdomains, caveolae, and caveolar endocytosis of sphingolipids. Mol. Membr. Biol. 23 (2006), 101–110.
19. [19] Parton, R.G., Simons, K., The multiple faces of caveolae. Nat. Rev. Mol. Cell Biol. 8 (2007), 185–194.
20. [20] Henley, J.R., Krueger, E.W., Oswald, J., McNiven, M.A., Dynamin-mediated internalization of caveolae. J. Cell Biol. 141 (1998), 85–99.
21. [21] Oh, P., McIntosh, D.P., Schnitzer, J.E., Dynamin at the neck of caveolae mediates their budding to form transport vesicles by GTP-driven fission from the plasma membrane of endothelium. J. Cell Biol. 141 (1998), 101–114.
22. [22] Pelkmans, L., Burli, T., Zerial, M., Helenius, A., Caveolin-stabilized membrane domains as multifunctional transport and sorting devices in endocytic membrane traffic. Cell 118 (2004), 767–780.
23. [23] Pelkmans, L., Zerial, M., M. Kinase-regulated quantal assemblies and kiss-and-run recycling of caveolae. Nature 436 (2005), 128–133.
24. [24] Pavlos, N.J., Friedman, P.A., GPCR signaling and trafficking: the long and short of it. Trends Endocrinol. Metab., 2016 (S1043-2760(16)30146-1).
25. [25] Hinkle, P.M., Puskas, J.A., Detection of G protein-coupled receptors by immunofluorescence microscopy. Methods Mol. Biol. 237 (2004), 127–134.
26. [26] Marchese, A., Monitoring chemokine receptor trafficking by confocal immunofluorescence microscopy. Methods Enzymol. 570 (2016), 281–292.
27. 1-adrenergic receptor. J. Biol. Chem. 279 (2004), 21135–21143.
28. 2-Adrenergic receptor desensitization, internalization, and phosphorylation in response to full and partial agonists. J. Biol. Chem. 272 (1997), 23871–23879.
29. 2-adrenergic receptor phosphorylation and internalization. Am. J. Respir. Cell Mol. Biol. 36 (2007), 254–261.
30. 2-adrenergic receptor. Nature 383 (1996), 447–450.
31. 1-Adrenergic receptor recycles via a membranous organelle, recycling endosome, by binding with sorting nexin27. J. Membr. Biol. 246 (2013), 571–579.
32. 1-adrenergic receptor that are involved in coupling the receptor to G proteins. J. Biol. Chem. 281 (2006), 12896–12907.
33. 1 adrenergic receptor endocytosis through different pathways. J. Biol. Chem. 278 (2003), 35403–35411.
34. s. J. Recept. Signal Transduct. Res. 33 (2013), 79–88.
35. 1-adrenergic receptor for β-arrestins explains the resistance to agonist-induced internalization. Life Sci. 68:2001 (2001), 2251–2257.
36. 2-adrenergic receptors following clathrin-mediated endocytosis. J. Cell Sci. 117 (2004), 723–734.
37. 2-adrenergic receptor establish a barcode that encodes differential functions of β-arrestin. Sci. Signal., 4, 2011, ra51.
38. [38] Butcher, A.J., Prihandoko, R., Kong, K.C., McWilliams, P., Edwards, J.M., Bottrill, A., Mistry, S., Tobin, A.B., Differential G-protein-coupled receptor phosphorylation provides evidence for a signaling bar code. J. Biol. Chem. 286 (2011), 11506–11518.
39. [39] Zindel, D., Engel, S., Bottrill, A.R., Pin, J.P., Prézeau, L., Tobin, A.B., Bünemann, M., Krasel, C., Butcher, A.J., Identification of key phosphorylation sites in PTH1R that determine arrestin3 binding and fine-tune receptor signaling. Biochem. J. 473 (2016), 4173–4192.
40. [40] Butcher, A.J., Hudson, B.D., Shimpukade, B., Alvarez-Curto, E., Prihandoko, R., Ulven, T. et al., Concomitant action of structural elements and receptor phosphorylation determines arrestin-3 interaction with the free fatty acid receptor FFA4. J. Biol. Chem. 289 (2014), 18451–18465.
41. [41] Busillo, J.M., Armando, S., Sengupta, R., Meucci, O., Bouvier, M., Benovic, J.L., Site-specific phosphorylation of CXCR4 is dynamically regulated by multiple kinases and results in differential modulation of CXCR4 signaling. J. Biol. Chem. 285 (2010), 7805–7817.
42. [42] Bouzo-Lorenzo, M., Santo-Zas, I., Lodeiro, M., Nogueiras, R., Casanueva, F.F., Castro, M. et al., Distinct phosphorylation sites on the ghrelin receptor, GHSR1a, establish a code that determines the functions of β-arrestins. Sci. Rep., 6(2016), 2016, 22495, 10.1038/srep22495.
43. [43] Kong, K.C., Butcher, A.J., McWilliams, P., Jones, D., Wess, J., Hamdan, F.F., Werry, T., Rosethorne, E.M., Charlton, S.J., Munson, S.E., Cragg, A.A., Smart, A.D., Tobin, A.B., M3-muscarinic receptor promotes insulin release via receptor phosphorylation/arrestin-dependent activation of protein kinase D1. Proc. Natl. Acad. Sci. U. S. A. 107 (2010), 21181–21186.
44. [44] Poulin, B., Butcher, A., McWilliams, P., Bourgognon, J.M., Pawlak, R., Kong, K.C., Bottrill, A., Mistry, S., Wess, J., Rosethorne, E.M., Charltonand, S.J., Tobin, A.B., The M3-muscarinic receptor regulates learning and memory in a receptor phosphorylation/arrestin-dependent manner. Proc. Natl. Acad. Sci. U. S. A. 107:2010 (2010), 9440–9445.
45. [45] Bradley, S.J., Wiegman, C.H., Iglesias, M.M., Kong, K.C., Butcher, A.J., Plouffe, B., Goupil, E., Bourgognon, J.M., Macedo-Hatch, T., LeGouill, C., Russell, K., Laporte, S.A., Konig, G.M., Kostenis, E., Bouvier, M., Chung, K.F., Amrani, Y., Tobin, A.B., Mapping physiological G protein-coupled receptor signaling pathways reveals a role for receptor phosphorylation in airway contraction. Proc. Natl. Acad. Sci. U. S. A. 113 (2016), 4524–4529.
46. 2-adrenergic receptor. Nature 401 (1999), 286–290.
47. [47] Whistler, J.L., Enquist, J., Marley, A., Fong, J., Gladher, F., Tsuruda, J., Murray, S.R., von Zastrow, M., Modulation of postendocytic sorting of G protein-coupled receptors. Science 297 (2002), 615–620.
48. 1-adrenergic receptors is mediated by pathways that are either dependent or independent of type-I PDZ, protein kinase A (PKA) and SAP97. J. Biol. Chem. 289 (2014), 2277–2294.
49. [49] Romero, G., von Zastrow, M., Friedman, P.A., Role of PDZ proteins in regulating trafficking, signaling, and function of GPCRs: means, motif, and opportunity. Adv. Pharmacol. 62 (2011), 279–314.
50. [50] Gage, R.M., Kim, K.A., Cao, T.T., von Zastrow, M., A transplantable sorting signal that is sufficient to mediate rapid recycling of G protein-coupled receptors. J. Biol. Chem. 276 (2001), 44712–44720.
51. [51] Gage, R.M., Matveeva, E.A., Whiteheart, S.W., von Zastrow, M., Type I PDZ ligands are sufficient to promote rapid recycling of G protein-coupled receptors independent of binding to NSF. J. Biol. Chem. 280 (2005), 2205–3313.
52. [52] Alpern, R.J., Moe, O.W., Caplan, M., Chapter 46: polyuria and diabetes insipidus. Seldin and Giebisch's The Kidney, fifth ed., 2013, Elsevier Inc, NY, NY, 1571–1600.
53. [53] Fushimi, K., Sasaki, S., Marumo, F., Phosphorylation of serine 256 is required for cAMP-dependent regulatory exocytosis of the aquaporin-2 water channel. J. Biol. Chem. 272:1997 (1997), 14800–14804.
54. [54] Noda, Y., Horikawa, S., Furukawa, T., Hirai, K., Katayama, Y., Asai, T., Kuwahara, M., Katagiri, K., Kinashi, T., Hattori, M., Nimato, N., Sasaki, S., Aquaporin-2 trafficking is regulated by PDZ domain containing protein SPA-1. FEBS Lett. 568 (2004), 139–145.
55. [55] Orsini, M.J., Parent, J.L., Mundell, S.J., Marchese, A., Benovic, J.L., Trafficking of the HIV coreceptor CXCR4. Role of arrestins and identification of residues in the c-terminal tail that mediate receptor internalization. J. Biol. Chem. 274 (1999), 31076–31086.
56. [56] Marchese, A., Benovic, J.L., Agonist-promoted ubiquitination of the G protein-coupled receptor CXCR4 mediates lysosomal sorting. J. Biol. Chem. 276 (2001), 45509–45512.
57. [57] J.M. Busillo JM, Armando S, Sengupta R, Meucci O, Bouvier M, Benovic JL., Site-specific phosphorylation of CXCR4 is dynamically regulated by multiple kinases and results in differential modulation of CXCR4 signaling. J. Biol. Chem. 285 (2010), 7805–7817.
58. [58] Marchese, A., Trejo, J.A., Ubiquitin-dependent regulation of G protein-coupled receptor trafficking and signaling. Cell. Signal. 25 (2013), 707–716.
59. [59] Shenoy, S.K., McDonald, P.H., Kohout, T.A., Lefkowitz, R.J., Regulation of receptor fate by ubiquitination of activated beta 2-adrenergic receptor and beta-arrestin. Science 294 (2001), 1307–1313.
60. 2-adrenergic receptor trafficking. EMBO Rep. 14:2013 (2013), 164–171.
61. [61] Shenoy, S.K., Xiao, K., Venkataramanan, V., Snyder, P.M., Freedman, N.J., Weissman, A.M., Nedd4 mediates agonist-dependent ubiquitination, lysosomal targeting, and degradation of the beta2-adrenergic receptor. J. Biol. Chem. 283 (2008), 22166–22176.
62. 2-adrenergic receptor. J. Biol. Chem. 291 (2016), 14510–14525.
63. [63] Tanowitz, M., von Zastrow, M., A novel endocytic recycling signal that distinguishes the membrane trafficking of naturally occurring opioid receptors. J. Biol. Chem. 278 (2003), 45978–45986.
64. [64] Vargas, G.A., Von Zastrow, M., Identification of a novel endocytic recycling signal in the D1 dopamine receptor. J. Biol. Chem. 279 (2004), 37461–37469.
65. [65] Nooh, M.M., Mancarella, S., Bahouth, S.W., Identification of novel transplantable GPCR recycling motif for drug discovery. Biochem. Pharmacol. 120 (2016), 22–32.
66. [66] Kallal, L., Gagnon, A.W., Penn, R.B., Benovic, J.L., Visualization of agonist-inducedsequestration and down-regulation of a green fluorescent protein-tagged beta2-adrenergic receptor. J. Biol. Chem. 273 (1998), 322–328.
67. [67] Kallal, L., Benovic, J.L., Using green fluorescent proteins to study G-protein coupled receptor localization and trafficking. Trends Pharmacol. Sci. 21 (2000), 175–180.
68. 1-adrenergic receptor generates a receptosome involved in receptor recycling and networking. J. Biol. Chem. 282 (2007), 5085–5099.
69. [69] Bowman, S.L., Shiwarski, D.J., Puthenveedu, M.A., Distinct G–protein coupled receptor recycling pathways allow spatial control of downstream G protein signaling. J. Cell Biol. 214 (2016), 797–806.
70. [70] Klauck, T.M., Faux, M.C., Labudda, K., Langeberg, L.K., Jaken, S., Scott, J.D., Coordination of three signaling enzymes by AKAP79, a mammalian scaffold protein. Science 271 (1996), 1589–1592.
71. 1-adrenergic receptor promotes recycling and functional resensitization of the receptor. J. Biol. Chem. 281 (2006), 33537–33553.
72. 1-adrenergic receptor trafficking and signaling in mammalian cells. J. Biol. Chem. 288 (2013), 33797–33812.
73. [73] Jo, I., Ward, D.T., Baum, M.A., Scott, J.D., Coghlan, V.M., Hammond, T.G., Harris, H.W., AQP2 is a substrate for endogenous PP2B activity within an inner medullary AKAP-signaling complex. Am. J. Physiol. Ren. Physiol. 281 (2001), F958–F965.
74. [74] Li, X., Matta, S.M., Sullivan, R.D., Bahouth, S.W., Carvedilol reverses cardiac hypertrophy and insufficiency in AKAP5 knockout mice by normalizing the activities of calcineurin and calmodulin kinase-II. Cardiovasc. Res. 104 (2014), 270–279.
75. [75] Kim, E., Sheng, M., PDZ domain proteins of synapses. Nat. Rev. Neurosci. 5 (2004), 771–781.
76. [76] Zhu, J., Shang, Y., Zhang, M., Mechanistic basis of MAGUK-organized complexes in synaptic development and signalling. Nat. Rev. Neurosci. 17 (2016), 209–223.
77. [77] Bredt, D.S., Nicoll, R.A., AMPA receptor trafficking at excitatory synapses. Neuron 40 (2003), 361–379.
78. [78] Joubert, L., Hanson, B., Barthet, G., Sebben, M., Claeysen, S., Hong, W., Marin, P., Dumuis, A., Bockaert, J., New sorting nexin (SNX27) and NHERF specifically interact with the 5-HT4a receptor splice variant: roles in receptor targeting. J. Cell Sci. 117 (2004), 5367–5379.
79. + exchange. Nature 392 (1998), 626–630.
80. [80] Lauffer, B.E., Chen, S., Melero, C., Kortemme, T., von Zastrow, M., Vargas, G.A., Engineered protein connectivity to actin mimics PDZ-dependent recycling of G protein-coupled receptors but not its regulation by Hrs. J. Biol. Chem. 284 (2009), 2448–2458.
81. [81] Lauffer, B.E., Melero, C., Temkin, P., Lei, C., Hong, W., Kortemme, T., von Zastrow, M., SNX27 mediates PDZ-directed sorting from endosomes to the plasma membrane. J. Cell Biol. 190 (2010), 565–574.
82. 1-adrenergic receptor interaction with N-methyl-D-aspartate receptors. J. Biol. Chem. 275 (2000), 38659–38666.
83. 1-Adrenergic receptor association with the synaptic scaffolding protein membrane-associated guanylate kinase inverted-2 (MAGI-2). Differential regulation of receptor internalization by MAGI-2 and PSD-95. J. Biol. Chem. 276 (2001), 41310–41317.
84. [84] Hu, L.A., Chen, W., Martin, N.P., Whalen, E.J., Premont, R.T., Lefkowitz, R.J., GIPC interacts with the beta1-adrenergic receptor and regulates beta1-adrenergic receptor-mediated ERK activation. J. Biol. Chem. 278 (2003), 26295–26301.
85. [85] He, J., Bellini, M., Inuzuka, H., Xu, J., Xiong, Y., Yang, X., Castleberry, A.M., Hall, R.A., Proteomic analysis of beta1-adrenergic receptor interactions with PDZ scaffold proteins. J. Biol. Chem. 281 (2006), 2820–2827.
86. 1-adrenergic receptor surface expression. J. Biol. Chem. 279 (2004), 50190–50196.
87. 1-adrenergic receptor modulates receptor trafficking and signaling in cardiac myocytes. J. Biol. Chem. 277 (2002), 33783–33790.
88. 1-adrenergic receptor in intracellular compartments after internalization. J. Biol. Chem. 290 (2015), 6120–6129.
89. [89] Wu, H., Reuver, S.M., Kuhlendahl, S., Chung, W.J., Garner, C.C., Subcellular targeting and cytoskeletal attachment of SAP97 to the epithelial lateral membrane. J. Cell Sci. 111 (1998), 2365–2376.
90. +/calmodulin-dependent protein kinase II binds to and phosphorylates a specific SAP97 splice variant to disrupt association with AKAP79/150 and modulate alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid-type glutamate receptor (AMPAR) activity. J. Biol. Chem. 285 (2010), 923–934.
91. [91] Fujita, A., Kurachi, Y., SAP family proteins. Biochem. Biophys. Res. Commun. 269 (2000), 1–6.
92. [92] Müller, B.M., Kistner, U., Veh, R.W., Cases-Langhoff, C., Becker, B., Gundelfinger, E.D., Garner, C.C., Molecular characterization and spatial distribution of SAP97, a novel presynaptic protein homologous to SAP90 and the Drosophila discs-large tumor suppressor protein. J. Neurosci. 15 (1995), 2354–2366.
93. 1-adrenergic receptor through its PDZ2 and i3 domains. PLos One, 8, 2013, e63379.
94. [94] Heydorn, A., Søndergaard, B.P., Ersbøll, B., Holst, B., Nielsen, F.C., Haft, C.R., Whistler, J., Schwartz, T.W., A library of 7TM receptor C-terminal tails. Interactions with the proposed postendocytic sorting proteins ERM-binding phosphoprotein 50 (EBP50), N-ethylmaleimidesensitive factor (NSF), sorting nexin 1 (SNX1), and G protein-coupled receptor-associated sorting protein (GASP). J. Biol. Chem. 279 (2004), 54291–54303.
95. [95] Sorkin, A., von Zastrow, M., Endocytosis and signalling: intertwining molecular networks. Nat. Rev. Mol. Cell Biol. 10 (2009), 609–622.
96. 1-adrenergic receptor from endosomes to the plasma membrane. Cell. Signal. 29 (2017), 192–208.
97. [97] Houslay, M.D., Underpinning compartmentalised cAMP signalling through targeted cAMP breakdown. Trends Biochem. Sci. 35 (2010), 91–100.
98. [98] McCahill, A.C., Huston, E., Li, X., Houslay, M.D., PDE4 associates with different scaffolding proteins: modulating interactions as treatment for certain diseases. Handb. Exp. Pharmacol. 186:2008 (2008), 125–166.
99. [99] Stangherlin, A., Zaccolo, M., Phosphodiesterases and subcellular compartmentalized cAMP signaling in the cardiovascular system. Am. J. Physiol. Heart Circ. Physiol. 302 (2012), H379–H390.
100. [100] Conti, M., Mika, D., Richter, W., Cyclic AMP compartments and signaling specificity: role of cyclic nucleotide phospho-diesterases. J. Gen. Physiol. 143 (2014), 29–38.
101. 2-adrenergic receptors is defined by differential interactions with PDE4. EMBO J. 27 (2008), 384–393.
102. 1 adrenergic receptor stimulation of cAMP/PKA signals in cardiac myocytes. J. Biol. Chem. 289 (2014), 14771–14781.
103. [103] Zerial, M., McBride, H., Rab proteins as membrane organizers. Nat. Rev. Mol. Cell Biol. 2 (2001), 107–117.
104. [104] Pereira-Leal, J.B., Seabra, M.C., The mammalian Rab family of small GTPases: definition of family and subfamily sequence motifs suggests a mechanism for functional specificity in the Rab superfamily. J. Mol. Biol. 301 (2002), 1077–1087.
105. [105] Stenmark, H., Rab GTPases as coordinators of vesicle traffic. Nat. Rev. Mol. Cell Biol. 10 (2009), 513–525.
106. [106] Wandinger-Ness, A., Zerial, M., Rab proteins and the compartmentalization of the endosomal system. Cold Spring Harb. Perspect. Biol., 6, 2014, a022616.
107. [107] Ehlers, M.D., Reinsertion or degradation of AMPA receptors determined by activity-dependent endocytic sorting. Neuron 28 (2000), 511–525.
108. 1-adrenergic receptor. Cell. Signal. 23 (2011), 46–57.
109. [109] Puthenveedu, M.A., Laufer, B., Temkin, P., Vistein, R., Carlton, P., Thorn, K., Taunton, J., Weiner, O.D., Parton, R.G., Von Zastrow, M., Sequence-dependent sorting of recycling proteins by actin-stabilized endosomal microdomains. Cell 143 (2010), 761–767.
110. [110] Frederic, J.-A., Bowersox, S., Chen, S., Beard, G., Puthenveedu, M.A., Hanyaloglu, A.C., Spacially restricted G protein-coupled receptor activity via divergent endocytic compartments. J. Biol. Chem. 289 (2013), 3936–3977.
111. [111] Lunn, M.L., Nassirpour, R., Arrabit, C., Tan, J., McLeod, I., Arias, C.M., Sawchenko, P.E., Yates, J.R. 3rd, Slesinger, P.A., A unique sorting nexin regulates trafficking of potassium channels via a PDZ domain interaction. Nat. Neurosci. 10 (2007), 1249–1259.
112. [112] Rincón, E., Santos, T., Avila-Flores, A., Albar, J.P., Lalioti, V., Lei, C., Hong, W., Mérida, I., Proteomics identification of sorting nexin 27 as a diacylglycerol kinase zeta-associated protein: new diacylglycerol kinase roles in endocytic recycling. Mol. Cell. Proteomics 6 (2007), 1073–1087.
113. [113] Temkin, P., Lauffer, B., Jager, S., Cimermancic, P., Krogan, N.J., von Zastrow, M., SNX27 mediates retromer tubule entry and endosome-to-plasma membrane trafficking of signaling receptors. Nat. Cell Biol. 13 (2010), 715–721.
114. [114] Chan, A.S., Clairfeuille, T., Landao-Bassonga, E., Kinna, G., Ng, P.Y., Loo, L.S., Cheng, T.S., Zheng, M., Hong, W., Teasdale, R.D., Collins, B.M., Pavlos, N.J., Sorting nexin 27 couples PTHR trafficking to retromer for signal regulation in osteoblasts during bone growth. Mol. Biol. Cell 27 (2016), 1367–1382.
115. [115] McGarvey, J.C., Xiao, K., Bowman, S.L., Mamonova, T., Zhang, Q., Bisello, A., Sneddon, W.B., Ardura, J.A., Jean-Alphonse, F., Vilardaga, J.P., Puthenveedu, M.A., Friedman, P.A., Actin-sorting nexin 27 (SNX27)-retromer complex mediates rapid parathyroid hormone receptor recycling. J. Biol. Chem. 291:2016 (2016), 10986–11002.
116. [116] Hussain, N.K., Diering, G.H., Sole, J., Anggono, V., Huganir, R.L., Sorting nexin 27 regulates basal and activity-dependent trafficking of AMPARs. Proc. Natl. Acad. Sci. U. S. A. 111 (2014), 11840–11845.
117. [117] Loo, L.S., Tang, N., Al-Haddawi, M., Dawe, G.S., Hong, W., A role for sorting nexin 27 in AMPA receptor trafficking. Nat. Commun., 5, 2014, 3176.
118. [118] Wang, X., Zhao, Y., Zhang, X., Badie, H., Zhou, Y., Mu, Y., Loo, L.S., Cai, L., Thompson, R.C., Yang, B., Chen, Y., Johnson, P.F., Wu, C., Bu, G., Mobley, W.C., Zhang, D., Gage, F.H., Ranscht, B., Zhang, Y.W., Lipton, S.A., Hong, W., Xu, H., Loss of sorting nexin-27 contributes to excitatory synaptic dysfunction by modulating glutamate receptor recycling in Down's syndrome. Nat. Med. 19 (2013), 473–480.
119. [119] Balana, B., Maslennikov, I., Kwiatkowski, W., Stern, K.M., Bahima, L., Choe, S., Slesinger, P.A., Mechanism underlying selective regulation of G protein-gated inwardly rectifying potassium channels by the psychostimulant-sensitive sorting nexin 27. Proc. Natl. Acad. Sci. U. S. A. 108 (2011), 5831–5836.
120. [120] Clairfeuille, T., Mas, C., Chan, A.S., Yang, Z., Tello-Lafoz, M., Chandra, M., Widagdo, J., Kerr, M.C., Paul, B., Mérida, I., Teasdale, R.D., Pavlos, N.J., Anggono, V., Collins, B.M., A molecular code for endosomal recycling of phosphorylated cargos by the SNX27-retromer complex. Nat. Struct. Mol. Biol. 23 (2016), 921–932.
121. 2-adrenergic receptor. J. Biol. Chem. 271 (1996), 13796–13803.
122. 1-adrenergic receptor association with PSD-95. J. Biol. Chem. 277 (2002), 1607–1613.
123. [123] Harbour, M.E., Breusegem, S.Y., Antrobus, R., Freeman, C., Reid, E., Seaman, M.N., The cargo-selective retromer complex is a recruiting hub for protein complexes that regulate endosomal tubule dynamics. J. Cell Sci. 123 (2010), 3703–3717.
124. [124] Carlton, J., Bujny, M., Peter, B.J., Oorschot, V.M., Rutherford, A., Mellor, H., Klumperman, J., McMahon, H.T., Cullen, P.J., Sorting nexin-1 mediates tubular endosome-to-TGN transport through coincidence sensing of high- curvature membranes and 3-phosphoinositides. Curr. Biol. 14 (2004), 1791–1800.
125. [125] Seaman, M.N.J., Cargo-selective endosomal sorting for retrieval to the Golgi requires retromer. J. Cell Biol. 165 (2004), 111–122.
126. [126] Derivery, E., Sousa, C., Gautier, J.J., Lombard, B., Loew, D., Gautreau, A., The Arp2/3 activator WASH controls the fission of endosomes through a large multi protein complex. Dev. Cell 17 (2009), 712–723.
127. [127] McGough, J.J., Steinberg, F., Gallon, M., Yatsu, A., Ohbayashi, N., Heesom, K.J., Fukuda, M., Cullen, P.J., Identification of molecular heterogeneity in SNX27-retromer-mediated endosome-to-plasma-membrane recycling. J. Cell Sci. 127 (2014), 4940–4953.
128. [128] Steinberg, F., Gallon, F.M., Winfield, M., Thomas, E.C., Bell, A.J., Heesom, K.J., Tavare, J.M., Cullen, P.J., A global analysis of SNX27-retromer assembly and cargo specificity reveals a function in glucose and metal ion transport. Nat. Cell Biol. 15 (2013), 461–471.
129. [129] Lee, S., Chang, J., Blackstone, C., FAM21 directs SNX27-retromer cargoes to the plasma membrane by preventing transport to the Golgi apparatus. Nat. Commun., 7, 2016, 10939.
130. [130] Harbour, M.E., Breusegem, S.Y., Seaman, N.J., Recruitment of the endosomal WASH complex is mediated by the extended “tail” of FAM21 binding to the retromer protein Vps35. Biochem. J. 442 (2012), 209–220.
131. [131] Jia, D., Gomez, T.S., Billadeau, D.D., Rosen, M.K., Multiple repeat elements within FAM21 tail link the WASH actin regulatory complex to the retromer. Mol. Biol. Cell 23 (2012), 2352–2361.
132. [132] Viklund, I.M., Aspenström, P., Meas-Yedid, V., Zhang, B., Kopec, J., Agren, D., Schneider, G., D'Amato, M., Olivo-Marin, J.C., Sansonetti, P. et al., WAFL, a new protein involved in regulation of early endocytic transport at the intersection of actin and microtubule dynamics. Exp. Cell Res. 315 (2009), 1040–1052.
133. [133] Nakajima, O., Nakamura, F., Yamashita, N., Tomita, Y., Suto, F., Okada, T., Iwamatsu, A., Kondo, E., Fujisawa, H., Takei, K., Goshima, Y., FKBP133: a novel mouse FK506-binding protein homolog alters growth cone morphology. Biochem. Biophys. Res. Commun. 346 (2006), 140–149.
134. [134] Pan, Y.F., Viklund, I.M., Tsai, H.H., Pettersson, S., Maruyama, I.N., The ulcerative colitis marker protein WAFL interacts with accessory proteins in endocytosis. Int. J. Biol. Sci. 6 (2010), 163–171.
135. [135] Eichel, K., Jullie, D., von Zastrow, M., β-Arrestin drives MAP kinase signalling from clathrin-coated structures after GPCR dissociation. Nat. Cell Biol. 18 (2016), 303–310.
136. [136] Shukla, A.K., Manglik, A., Kruse, A.C. et al., Structure of active β-arrestin-1 bound to a G-protein-coupled receptor phosphopeptide. Nature 497 (2013), 137–141.
137. [137] Kang, Y., Zhou, X.E., Gao, X. et al., Crystal structure of Rhodopsin bound to arrestin by femtosecond X-ray laser. Nature 523 (2015), 561–567.
138. [138] Gurevich, V.V., Gurevich, E.V., The structural basis of arrestin-mediated regulation of G-protein-coupled receptors. Pharmacol. Ther. 110 (2006), 465–502.
139. [139] Shukla, A.K., Westfield, G.H., Xiao, K. et al., Visualization of arrestin recruitment by a G-protein-coupled receptor. Nature 512:2014 (2014), 218–222.
140. [140] Cahill, T.J. 3rd, Thomsen, A.R., Tarrasch, J.T. et al., Distinct conformations of GPCR-β-arrestin complexes mediate desensitization, signaling, and endocytosis. Proc. Natl. Acad. Sci. U. S. A. 114 (2017), 2562–2567.
141. [141] Feinstein, T.N., Yui, N., Webber, M.J., Wehbi, V.L., Stevenson, H.P., King, J.D. Jr., Hallows, K.R., Brown, D., Bouley, R., Vilardaga, J.P., Noncanonical control of vasopressin receptor type2 signaling by retromer and arrestin. J. Biol. Chem. 288 (2013), 27849–27860.
142. [142] Ferrandon, S., Feinstein, T.N., Castro, M., Wang, B., Bouley, R., Potts, J.T., Gardella, T.J., Vilardaga, J.P., Sustained cyclic AMP production by parathyroid hormone receptor endocytosis. Nat. Chem. Biol. 5 (2009), 734–742.
143. [143] Inda, C., Dos Santos Claro, P.A., Bonfiglio, J.J., Senin, S.A., Maccarrone, G., Turck, C.W., Silberstein, S., Different cAMP sources are critically involved in G protein coupled receptor CRHR1 signaling. J. Cell Biol. 214 (2016), 181–195.
144. [144] Vilardage, J.-P., Jean-Alphonse, F.G., Endosomal generation of cAMP in GPCR signaling. Nat. Chem. Biol. 10 (2014), 700–706.
145. [145] Irannejad, R., Tomshine, J.C., Tomshine, J.R., Chevalier, M., Mahoney, J.P., Steyaert, J., Rasmussen, S.G., Sunahara, R.K., El-Samad, H., Huang, B., von Zastrow, M., Conformational biosensors reveal GPCR signalling from endosomes. Nature 495 (2013), 534–538.
146. [146] Oakley, R.H., Laporte, S.A., Holt, J.A., Barak, L.S., Caron, M.G., Association of β-arrestin with G protein-coupled receptors during clathrin-mediated endocytosis dictates the profile of receptor resensitization. J. Biol. Chem. 274 (1999), 32248–32257.
147. [147] Shukla, A.K., Violin, J.D., Whalen, E.J., Gesty-Palmer, D., Shenoy, S.K., Lefkowitz, R.J., Distinct conformational changes in β-arrestin report biased agonism at seven-transmembrane receptors. Proc. Natl. Acad. Sci. U. S. A. 105:2008 (2008), 9988–9993.
148. [148] Nuber, S., Zabel, U., Lorenz, K., Nuber, A., Milligan, G., Tobin, A.B., Lohse, M.J., Hoffmann, C., β-Arrestin biosensors reveal a rapid, receptor-dependent activation/deactivation cycle. Nature 531 (2016), 661–664.
149. [149] Lee, M.H., Appleton, K.M., Strungs, E.G., Kwon, J.Y., Morinelli, T.A., Peterson, Y.K., Laporte, S.A., Luttrell, L.M., The conformational signature of β-arrestin2 predicts its trafficking and signalling functions. Nature 531 (2016), 665–668.
150. [150] Yang, F., Yu, X., Liu, C., Qu, C.X., Gong, Z., Liu, H.D., Li, F.H., Wang, H.M., He, D.F., Yi, F., Song, C., Tian, C.L., Xiao, K.H., Wang, J.Y., Sung, J.P., Selective mechanisms of arrestin conformations and functions revealed by unnatural amino acid incorporation and (19)F-NMR. Nat. Commun., 6, 2015, 8202, 10.1038/ncomms9202.
151. [151] Thomsen, A.R., Plouffe, B., Cahill, T.J. 3rd, Shukla, A.K., Tarrasch, J.T., Dosey, A.M., Kahsai, A.W., Strachan, R.T., Pani, B., Mahoney, J.P., Huang, L., Breton, B., Heydenreich, F.M., Sunahara, R.K., Skiniotis, G., Bouvier, M., Lefkowitz, R.J., GPCR-G protein-β-arrestin super-complex mediates sustained G protein signaling. Cell 166 (2016), 907–919.
152. 2-adrenergic receptor. J. Biol. Chem. 281 (2006), 1261–1273.
153. [153] Tsvetanova, N.G., von Zastrow, M., Spatial encoding of cyclic AMP signaling specificity by GPCR endocytosis. Nat. Chem. Biol. 10 (2014), 1061–1066.
154. [154] Xiong, L., Xia, W.F., Tang, F.L., Pan, J.X., Mei, L., Xiong, C.W., Retromer in Osteoblasts Interacts With Protein Phosphatase 1 Regulator Subunit 14C, Terminates Parathyroid Hormone's Signaling, and Promotes Its Catabolic Response. EBioMedicine 2016:9 (2016), 45–60.
155. [155] Wehbi, V.L., Stevenson, H.P., Feinstein, T.N., Calero, G., Romero, G., Vilardaga, J.P., Noncanonical GPCR signaling arising from a PTH receptor-arrestin-Gβγ complex. Proc. Natl. Acad. Sci. U. S. A. A110 (2013), 1530–1535.
156. [156] Feinstein, T.N., Wehbi, V.L., Ardura, J.A., Wheeler, D.S., Ferrandon, S., Gardella, T.J., Vilardaga, J.P., Retromer terminates the generation of cAMP by internalized PTH receptors. Nat. Chem. Biol. 7 (2011), 278–284.
157. [157] Huotari, J., Helenius, A., Endosome maturation. EMBO J. 30 (2011), 3481–3500.
158. [158] Seaman, M.N., The retromer complex-endosomal protein recycling and beyond. J. Cell Sci. 125 (2012), 4693–4702.
159. [159] Hartenik, M., Port, F., Lorenowicz, M.J., McGough, I.J., Silhankova, M., Betist, M.C., van Weering, J.R., van Heesbeen, R.G., Middlekoop, T.C., Basler, K., Cullen, P.J., Korswagen, H.C., A SNX3 dependent retromer pathway mediates retrograde transport of the Wnt sorting receptor Wntless and is required for Wnt secretion. Nat. Cell Biol. 13 (2011), 914–923.
160. [160] Vistein, R., Puthenveedu, M.A., Reprogramming of G protein-coupled receptor recycling recycling and signaling by a kinase switch. Proc. Natl. Acad. Sci. U. S. A. 110 (2013), 15289–15294.
161. 2-adrenergic receptor to different G proteins by PKA. Nature 390 (1997), 88–91.
162. [162] Martin, N.P., Whalen, E.J., Zamah, M.A., Pierce, K.L., Lefkowitz, R.J., PKA-mediated phosphorylation of the beta1-adrenergic receptor promotes Gs/Gi switching. Cell. Signal. 16 (2004), 1397–1403.
163. [163] Liang, W., Fishman, P.H., Resistance of the human beta1-adrenergic receptor to agonist-induced ubiquitination: a mechanism for impaired receptor degradation. J. Biol. Chem. 279 (2004), 46882–46889.
164. 1-adrenoceptor density. Int. J. Cardiol. 72 (2000), 137–141.
165. [165] Molinoff, P.B., Alpha- and beta-adrenergic receptor subtypes properties, distribution and regulation. Drugs 28 (1984), 1–15.
166. 2 adrenoceptors in guinea pig atrium: functional and receptor binding studies. J. Pharmacol. Exp. Ther. 241 (1987), 1041–1047.
167. [167] Bristow, M.R., Ginsburg, R., Minobe, W., Cubicciotti, R.S., Sageman, W.S., Lurie, K., Billingham, M.E., Harrison, D.C., Stinson, E.B., Decreased catecholamine sensitivity and beta-adrenergic-receptor density in failing human hearts. N. Engl. J. Med. 307 (1982), 205–211.
168. 1-receptor messenger RNA abundance in the failing human heart. J. Clin. Invest. 92 (1993), 2737–2745.
169. [169] Brodde, O.E., Beta-adrenoceptors in cardiac disease. Pharmacol. Ther. 60 (1993), 405–430.
170. 2-adrenergic receptor-mediated adenylate cyclase stimulation in nonfailing and failing human ventricular myocardium. Mol. Pharmacol., 1989, 295–303.
171. [171] Fajardo, G., Zhao, M., Powers, J., Bernstein, D., Differential cardiotoxic/cardioprotective effects of β-adrenergic receptor subtypes in myocytes and fibroblasts in doxorubicin cardiomyopathy. J. Mol. Cell. Cardiol. 40 (2006), 375–383.
172. [172] Bernstein, D., Fajardo, G., Zhao, M., Urashima, T., Powers, J., Berry, G., Kobilka, B.K., Differential cardioprotective/cardiotoxic effects mediated by beta-adrenergic receptor subtypes. Am. J. Physiol. Heart Circ. Physiol. 289 (2005), H2441–H2449.