Actin-sorting nexin 27 (SNX27)-retromer complex mediates rapid parathyroid hormone receptor recycling

Journal of Biological Chemistry

Volumn 291, Issue 21, 2016, Pages 10986-11002

  McGarvey, Jennifer C ^a   Xiao, Kunhong ^a   Bowman, Shanna L ^b   Mamonova, Tatyana ^a   Zhan, Qiangmin ^a   Bisello, Alessandro ^a   Bruce Sneddon, W ^a   Ardura, Juan A ^a   Jean Alphonse, Frederic ^a   Vilardaga, Jean Pierre ^a   Puthenveedu, Manojkumar A ^b   Friedman, Peter A ^a,c  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b CARNEGIE MELLON UNIVERSITY   (United States)

^c UNIVERSIDAD SAN PABLO CEU   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BINS; BIOCHEMISTRY; ENDOCRINOLOGY; LIGANDS; MASS SPECTROMETRY; MOLECULAR DYNAMICS; RECYCLING;

BINDING PARTNERS; CO-IMMUNOPRECIPITATIONS; DOMAIN-CONTAINING PROTEINS; ION HOMEOSTASIS; PARATHYROID HORMONE RECEPTORS; PARATHYROID HORMONES; PROTEIN BINDING; SURFACE RECEPTORS;

PROTEINS;

ACTIN; N ETHYLMALEIMIDE SENSITIVE FACTOR; PARATHYROID HORMONE; PARATHYROID HORMONE RECEPTOR; PROTEIN SERINE THREONINE KINASE; SORTING NEXIN; SORTING NEXIN 27; UNCLASSIFIED DRUG; VPS 26 PROTEIN; VPS29 PROTEIN; VPS35 PROTEIN; MULTIPROTEIN COMPLEX; PARATHYROID HORMONE RECEPTOR 1; PROTEIN BINDING; PROTEIN SUBUNIT; RECOMBINANT PROTEIN; SNX27 PROTEIN, HUMAN;

ARTICLE; CELL MEMBRANE; COMPLEX FORMATION; CONTROLLED STUDY; DEPOLYMERIZATION; ENDOSOME; HUMAN; HUMAN CELL; MASS SPECTROMETRY; MOLECULAR DYNAMICS; PDZ DOMAIN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; ANIMAL; CHEMISTRY; CHO CELL LINE; CRICETULUS; GENETICS; HEK293 CELL LINE; METABOLISM; PROTEIN DEGRADATION; PROTEIN SUBUNIT; PROTEIN TRANSPORT;

ACTINS; ANIMALS; CHO CELLS; CRICETULUS; ENDOSOMES; HEK293 CELLS; HUMANS; METABOLIC NETWORKS AND PATHWAYS; MOLECULAR DYNAMICS SIMULATION; MULTIPROTEIN COMPLEXES; N-ETHYLMALEIMIDE-SENSITIVE PROTEINS; PDZ DOMAINS; PROTEIN BINDING; PROTEIN SUBUNITS; PROTEIN TRANSPORT; PROTEOLYSIS; RECEPTOR, PARATHYROID HORMONE, TYPE 1; RECOMBINANT PROTEINS; SORTING NEXINS;

EID: 84971384350     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.697045     Document Type: Article

References (90)

1. Ferguson, S. S. (2001) Evolving concepts in G protein-coupled receptor endocytosis: the role in receptor desensitization and signaling. Pharmacol. Rev. 53, 1-24
2. Hanyaloglu, A. C., and von Zastrow, M. (2008) Regulation of GPCRs by endocytic membrane trafficking and its potential implications. Annu. Rev. Pharmacol. Toxicol. 48, 537-568
3. Tsvetanova, N. G., Irannejad, R., and von Zastrow, M. (2015) G proteincoupled receptor (GPCR) signaling via heterotrimeric G proteins from endosomes. J. Biol. Chem. 290, 6689-6696
4. Temkin, P., Lauffer, B., Jäger, S., Cimermancic, P., Krogan, N. J., and von Zastrow, M. (2011) SNX27 mediates retromer tubule entry and endosome-to-plasma membrane trafficking of signalling receptors. Nat. Cell Biol. 13, 715-721
5. Harbour, M. E., Breusegem, S. Y., Antrobus, R., Freeman, C., Reid, E., and Seaman, M. N. (2010) The cargo-selective retromer complex is a recruiting hub for protein complexes that regulate endosomal tubule dynamics. J. Cell Sci. 123, 3703-3717
6. Wassmer, T., Attar, N., Harterink, M., van Weering, J. R., Traer, C. J., Oakley, J., Goud, B., Stephens, D. J., Verkade, P., Korswagen, H. C., and Cullen, P. J. (2009) The retromer coat complex coordinates endosomal sorting and dynein-mediated transport, with carrier recognition by the trans-Golgi network. Dev. Cell 17, 110-122
7. Haft, C. R., de la Luz Sierra, M., Bafford, R., Lesniak, M. A., Barr, V. A., and Taylor, S. I. (2000) Human orthologs of yeast vacuolar protein sorting proteins Vps26, 29, and 35: assembly into multimeric complexes. Mol. Biol. Cell 11, 4105-4116
8. Hierro, A., Rojas, A. L., Rojas, R., Murthy, N., Effantin, G., Kajava, A. V., Steven, A. C., Bonifacino, J. S., and Hurley, J. H. (2007) Functional architecture of the retromer cargo-recognition complex. Nature 449, 1063-1067
9. Rojas, R., Kametaka, S., Haft, C. R., and Bonifacino, J. S. (2007) Interchangeable but essential functions of SNX1 and SNX2 in the association of retromer with endosomes and the trafficking of mannose 6-phosphate receptors. Mol. Cell. Biol. 27, 1112-1124
10. Linardopoulou, E. V., Parghi, S. S., Friedman, C., Osborn, G. E., Parkhurst, S. M., and Trask, B. J. (2007) Human subtelomeric WASH genes encode a new subclass of the WASP family. PLoS Genet. 3, e237
11. Derivery, E., Sousa, C., Gautier, J. J., Lombard, B., Loew, D., and Gautreau, A. (2009) The Arp2/3 activator WASH controls the fission of endosomes through a large multiprotein complex. Dev. Cell 17, 712-723
12. Gomez, T. S., and Billadeau, D. D. (2009) A FAM21-containing WASH complex regulates retromer-dependent sorting. Dev. Cell 17, 699-711
13. Helfer, E., Harbour, M. E., Henriot, V., Lakisic, G., Sousa-Blin, C., Volceanov, L., Seaman, M. N., and Gautreau, A. (2013) Endosomal recruitment of the WASH complex: active sequences and mutations impairing interaction with the retromer. Biol. Cell 105, 191-207
14. van Weering, J. R., and Cullen, P. J. (2014) Membrane-associated cargo recycling by tubule-based endosomal sorting. Semin. Cell Dev. Biol. 31, 40-47
15. Ghai, R., Bugarcic, A., Liu, H., Norwood, S. J., Skeldal, S., Coulson, E. J., Li, S. S., Teasdale, R. D., and Collins, B. M. (2013) Structural basis for endosomal trafficking of diverse transmembrane cargos by PX-FERM proteins. Proc. Natl. Acad. Sci. U.S.A. 110, E643- 652
16. Steinberg, F., Gallon, M., Winfield, M., Thomas, E. C., Bell, A. J., Heesom, K. J., Tavaré, J. M., and Cullen, P. J. (2013) A global analysis of SNX27-retromer assembly and cargo specificity reveals a function in glucose and metal ion transport. Nat. Cell Biol. 15, 461-471
17. Gallon, M., Clairfeuille, T., Steinberg, F., Mas, C., Ghai, R., Sessions, R. B., Teasdale, R. D., Collins, B. M., and Cullen, P. J. (2014) A unique PDZ domain and arrestin-like fold interaction reveals mechanistic details of endocytic recycling by SNX27-retromer. Proc. Natl. Acad. Sci. U.S.A. 111, E3604-E3613
18. Lauffer, B. E., Melero, C., Temkin, P., Lei, C., Hong, W., Kortemme, T., and von Zastrow, M. (2010) SNX27 mediates PDZ-directed sorting from endosomes to the plasma membrane. J. Cell Biol. 190, 565-574
19. Nakagawa, T., and Asahi, M. (2013) β1 -Adrenergic receptor recycles via a membranous organelle, recycling endosome, by binding with sorting nexin27. J. Membr. Biol. 246, 571-579
20. Bauch, C., Koliwer, J., Buck, F., Hönck, H. H., and Kreienkamp, H. J. (2014) Subcellular sorting of the G-protein coupled mouse somatostatin receptor 5 by a network of PDZ-domain containing proteins. PLoS One 9, e88529
21. Lin, T. B., Lai, C. Y., Hsieh, M. C., Wang, H. H., Cheng, J. K., Chau, Y. P., Chen, G. D., and Peng, H. Y. (2015) VPS26A-SNX27 interaction-dependent mGluR5 recycling in dorsal horn neurons mediates neuropathic pain in rats. J. Neurosci. 35, 14943-14955
22. Puthenveedu, M. A., Lauffer, B., Temkin, P., Vistein, R., Carlton, P., Thorn, K., Taunton, J., Weiner, O. D., Parton, R. G., and von Zastrow, M. (2010) Sequence-dependent sorting of recycling proteins by actin-stabilized endosomal microdomains. Cell 143, 761-773
23. Vistein, R., and Puthenveedu, M. A. (2013) Reprogramming of G proteincoupled receptor recycling and signaling by a kinase switch. Proc. Natl. Acad. Sci. U.S.A. 110, 15289-15294
24. Cao, T. T., Deacon, H. W., Reczek, D., Bretscher, A., and von Zastrow, M. (1999) A kinase-regulated PDZ-domain interaction controls endocytic sorting of the β2 -adrenergic receptor. Nature 401, 286-290
25. Gage, R. M., Matveeva, E. A., Whiteheart, S. W., and von Zastrow, M. (2005) Type I PDZ ligands are sufficient to promote rapid recycling of G protein-coupled receptors independent of binding to N-ethylmaleimidesensitive factor. J. Biol. Chem. 280, 3305-3313
26. Cheloha, R. W., Gellman, S. H., Vilardaga, J. P., and Gardella, T. J. (2015) PTH receptor-1 signalling: mechanistic insights and therapeutic prospects. Nat. Rev. Endocrinol. 11, 712-724
27. Drake, M. T., Shenoy, S. K., and Lefkowitz, R. J. (2006) Trafficking of G protein-coupled receptors. Circ. Res. 99, 570-582
28. Srivastava, A., Gupta, B., Gupta, C., and Shukla, A. K. (2015) Emerging functional divergence of β-arrestin isoforms in GPCR function. Trends Endocrinol. Metab. 26, 628-642
29. Walther, C., and Ferguson, S. S. (2013) Arrestins: role in the desensitization, sequestration, and vesicular trafficking of G protein-coupled receptors. Prog. Mol. Biol. Transl. Sci. 118, 93-113
30. Vilardaga, J. P., Jean-Alphonse, F. G., and Gardella, T. J. (2014) Endosomal generation of cAMP in GPCR signaling. Nat. Chem. Biol. 10, 700-706
31. Kotowski, S. J., Hopf, F. W., Seif, T., Bonci, A., and von Zastrow, M. (2011) Endocytosis promotes rapid dopaminergic signaling. Neuron 71, 278-290
32. 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., and von Zastrow, M. (2013) Conformational biosensors reveal GPCR signalling from endosomes. Nature 495, 534-538
33. Chauvin, S., Bencsik, M., Bambino, T., and Nissenson, R. A. (2002) Parathyroid hormone receptor recycling: role of receptor dephosphorylation and β-arrestin. Mol. Endocrinol. 16, 2720-2732
34. Ferrari, S. L., Behar, V., Chorev, M., Rosenblatt, M., and Bisello, A. (1999) Endocytosis of ligand-human parathyroid hormone receptor 1 complexes is protein kinase C-dependent and involves β-arrestin2: real-time monitoring by fluorescence microscopy. J. Biol. Chem. 274, 29968-29975
35. Sneddon, W. B., Bisello, A., Magyar, C. E., Willick, G. E., Syme, C. A., Galbiati, F., and Friedman, P. A. (2004) Ligand-selective dissociation of activation and internalization of the parathyroid hormone (PTH) receptor: conditional efficacy of PTH peptide fragments. Endocrinology 145, 2815-2823
36. Vilardaga, J. P., Krasel, C., Chauvin, S., Bambino, T., Lohse, M. J., and Nissenson, R. A. (2002) Internalization determinants of the parathyroid hormone receptor differentially regulate β-arrestin/receptor association. J. Biol. Chem. 277, 8121-8129
37. Ferrandon, S., Feinstein, T. N., Castro, M., Wang, B., Bouley, R., Potts, J. T., Gardella, T. J., and Vilardaga, J. P. (2009) Sustained cyclic AMP production by parathyroid hormone receptor endocytosis. Nat. Chem. Biol. 5, 734-742
38. Calebiro, D., Nikolaev, V. O., Gagliani, M. C., de Filippis, T., Dees, C., Tacchetti, C., Persani, L., and Lohse, M. J. (2009) Persistent cAMP-signals triggered by internalized G-protein-coupled receptors. PLoS Biol. 7, e1000172
39. 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., and Vilardaga, J. P. (2013) Noncanonical control of vasopressin receptor type 2 signaling by retromer and arrestin. J. Biol. Chem. 288, 27849-27860
40. Tsvetanova, N. G., and von Zastrow, M. (2014) Spatial encoding of cyclic AMP signaling specificity by GPCR endocytosis. Nat. Chem. Biol. 10, 1061-1065
41. Gidon, A., Al-Bataineh, M. M., Jean-Alphonse, F. G., Stevenson, H. P., Watanabe, T., Louet, C., Khatri, A., Calero, G., Pastor-Soler, N. M., Gardella, T. J., and Vilardaga, J. P. (2014) Endosomal GPCR signaling turned off by negative feedback actions of PKA and v-ATPase. Nat. Chem. Biol. 10, 707-709
42. Feinstein, T. N., Wehbi, V. L., Ardura, J. A., Wheeler, D. S., Ferrandon, S., Gardella, T. J., and Vilardaga, J. P. (2011) Retromer terminates the generation of cAMP by internalized PTH receptors. Nat. Chem. Biol. 7, 278-284
43. Seaman, M. N. J. (2012) The retromer complex: endosomal protein recycling and beyond. J. Cell Sci. 125, 4693-4702
44. Conway, B. R., Minor, L. K., Xu, J. Z., D'Andrea, M. R., Ghosh, R. N., and Demarest, K. T. (2001) Quantitative analysis of agonist-dependent parathyroid hormone receptor trafficking in whole cells using a functional green fluorescent protein conjugate. J. Cell. Physiol. 189, 341-355
45. Huang, Z., Chen, Y., and Nissenson, R. A. (1995) The cytoplasmic tail of the G-protein-coupled receptor for parathyroid hormone and parathyroid hormone-related protein contains positive and negative signals for endocytosis. J. Biol. Chem. 270, 151-156
46. Tawfeek, H. A., Qian, F., and Abou-Samra, A. B. (2002) Phosphorylation of the receptor for PTH and PTHrP is required for internalization and regulates receptor signaling. Mol. Endocrinol. 16, 1-13
47. Alonso, V., Magyar, C. E., Wang, B., Bisello, A., and Friedman, P. A. Ubiquitination-deubiquitination balance dictates ligand-stimulated PTHR sorting. (2011) Ubiquitination-deubiquitination balance dictates ligandstimulated PTHR sorting. J. Bone Miner. Res. 26, 2923-2934
48. Romero, G., von Zastrow, M., and Friedman, P. A. (2011) Role of PDZ proteins in regulating trafficking, signaling, and function of GPCRs: means, motif, and opportunity. Adv. Pharmacol. 62, 279-314
49. + exchanger regulatory factor-1 association and dissociation regulate parathyroid hormone receptor trafficking at membrane microdomains. J. Biol. Chem. 286, 35020-35029
50. Wang, B., Bisello, A., Yang, Y., Romero, G. G., and Friedman, P. A. (2007) NHERF1 regulates parathyroid hormone receptor membrane retention without affecting recycling. J. Biol. Chem. 282, 36214-36222
51. Geiser, M., Cèbe, R., Drewello, D., and Schmitz, R. (2001) Integration of PCR fragments at any specific site within cloning vectors without the use of restriction enzymes and DNA ligase. BioTechniques 31, 88-92
52. Chaudhary, S., Pak, J. E., Gruswitz, F., Sharma, V., and Stroud, R. M. (2012) Overexpressing human membrane proteins in stably transfected and clonal human embryonic kidney 293S cells. Nat. Protoc. 7, 453-466
53. Valdes, J. L., Tang, J., McDermott, M. I., Kuo, J. C., Zimmerman, S. P., Wincovitch, S. M., Waterman, C. M., Milgram, S. L., and Playford, M. P. (2011) Sorting nexin 27 protein regulates trafficking of a p21-activated kinase (PAK) interacting exchange factor (β-Pix)-G protein-coupled receptor kinase interacting protein (GIT) complex via a PDZ domain interaction. J. Biol. Chem. 286, 39403-39416
54. Shi, H., Rojas, R., Bonifacino, J. S., and Hurley, J. H. (2006) The retromer subunit Vps26 has an arrestin fold and binds Vps35 through its C-terminal domain. Nat. Struct. Mol. Biol. 13, 540-548
55. Ghai, R., Mobli, M., Norwood, S. J., Bugarcic, A., Teasdale, R. D., King, G. F., and Collins, B. M. (2011) Phox homology band 4.1/ezrin/radixin/moesin-like proteins function as molecular scaffolds that interact with cargo receptors and Ras GTPases. Proc. Natl. Acad. Sci. U.S.A. 108, 7763-7768
56. Kahsai, A. W., Rajagopal, S., Sun, J., and Xiao, K. (2014) Monitoring protein conformational changes and dynamics using stable-isotope labeling and mass spectrometry. Nat. Protoc. 9, 1301-1319
57. 2-adrenergic receptor establish a barcode that encodes differential functions of β-arrestin. Sci. Signal. 4, ra51
58. Haas, W., Faherty, B. K., Gerber, S. A., Elias, J. E., Beausoleil, S. A., Bakalarski, C. E., Li, X., Villén, J., and Gygi, S. P. (2006) Optimization and use of peptide mass measurement accuracy in shotgun proteomics. Mol. Cell. Proteomics 5, 1326-1337
59. Balana, B., Maslennikov, I., Kwiatkowski, W., Stern, K. M., Bahima, L., Choe, S., and Slesinger, P. A. (2011) 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, 5831-5836
60. Case, D. A., Darden, T. A., Cheatham, T. E., 3rd, Simmerling, C. L., Wang, J., Duke, R. E., Luo, R., Merz, K. M., Pearlman, D. A., Crowley, M., Walker, R. C., Zhang, W., Wang, B., Hayik, S., Roitberg, A., et al. (2006) AMBER 9, University of California, San Francisco
61. Case, D. A., Darden, T. A., Cheatham, T. E., 3rd, Simmerling, C. L., Wang, J., Duke, R. E., Luo, R., Walker, R. C., Zhang, W., Merz, K. M., Roberts, B., Wang, B., Hayik, S., Roitberg, A., Seabra, G., et al. (2010) AMBER 11, University of California, San Francisco
62. Hornak, V., Abel, R., Okur, A., Strockbine, B., Roitberg, A., and Simmerling, C. (2006) Comparison of multiple Amber force fields and development of improved protein backbone parameters. Proteins 65, 712-725
63. Berendsen, H. J. C., Postma, J. P. M., Vangunsteren, W. F., Dinola, A., and Haak, J. R. (1984) Molecular dynamics with coupling to an external bath. J. Chem. Phys. 81, 3684-3690
64. Darden, T., York, D., and Pedersen, L. (1993) Particle mesh Ewald: an N•log(N) method for Ewald sums in large systems. J. Chem. Phys. 98, 10089-10092
65. Ryckaert, J. P., Ciccotti, G., and Berendsen, H. J. C. (1977) Numerical integration of Cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes. J. Comp. Phys. 23, 327-341
66. Wang, B., Yang, Y., and Friedman, P. A. (2008) Na/H exchange regulatory factor 1, a novel AKT-associating protein, regulates extracellular signalregulated kinase signaling through a B-Raf-mediated pathway. Mol. Biol. Cell 19, 1637-1645
67. Cushing, P. R., Fellows, A., Villone, D., Boisguérin, P., and Madden, D. R. (2008) The relative binding affinities of PDZ partners for CFTR: a biochemical basis for efficient endocytic recycling. Biochemistry 47, 10084-10098
68. Roehrl, M. H. A., Wang, J. Y., and Wagner, G. (2004) A general framework for development and data analysis of competitive high-throughput screens for small-molecule inhibitors of protein-protein interactions by fluorescence polarization. Biochemistry 43, 16056-16066
69. Syme, C. A., Friedman, P. A., and Bisello, A. (2005) Parathyroid hormone receptor trafficking contributes to the activation of extracellular signalregulated kinases but is not required for regulation of cAMP signaling. J. Biol. Chem. 280, 11281-11288
70. Bowman, S. L., Soohoo, A. L., Shiwarski, D. J., Schulz, S., Pradhan, A. A., and Puthenveedu, M. A. (2015) Cell-autonomous regulation of μ-opioid receptor recycling by substance P. Cell Rep. 10, 1925-1936
71. Bowman, S. L., Soohoo, A. L., and Puthenveedu, M. A. (2015) Visualizing and quantitating sequence-dependent GPCR recycling. Methods Cell Biol. 130, 333-345
72. Mahon, M. J. (2009) The parathyroid hormone 1 receptor directly binds to the FERM domain of ezrin, an interaction that supports apical receptor localization and signaling in LLC-PK1 cells. Mol. Endocrinol. 23, 1691-1701
73. Vilardaga, J. P., Romero, G., Friedman, P. A., and Gardella, T. J. (2011) Molecular basis of parathyroid hormone receptor signaling and trafficking: a family B GPCR paradigm. Cell Mol. Life Sci. 68, 1-13
74. Sneddon, W. B., Syme, C. A., Bisello, A., Magyar, C. E., Weinman, E. J., Rochdi, M. D., Parent, J. L., Abou-Samra, A. B., and Friedman, P. A. (2003) Activation-independent parathyroid hormone receptor internalization is regulated by NHERF1 (EBP50). J. Biol. Chem. 278, 43787-43796
75. Zimmerman, S. P., Hueschen, C. L., Malide, D., Milgram, S. L., and Playford, M. P. (2013) Sorting nexin 27 (SNX27) associates with zonula occludens-2 (ZO-2) and modulates the epithelial tight junction. Biochem. J. 455, 95-106
76. Miesenböck, G. (2012) Synapto-pHluorins: genetically encoded reporters of synaptic transmission. Cold Spring Harb. Protoc. 2012, 213-217
77. Mayle, K. M., Le, A. M., and Kamei, D. T. (2012) The intracellular trafficking pathway of transferrin. Biochim. Biophys. Acta 1820, 264-281
78. 2-adrenergic receptor to N-ethylmaleimide-sensitive factor regulates receptor recycling. J. Biol. Chem. 276, 45145-45152
79. Song, I., Kamboj, S., Xia, J., Dong, H., Liao, D., and Huganir, R. L. (1998) Interaction of the N-ethylmaleimide-sensitive factor with AMPA receptors. Neuron 21, 393-400
80. Nishimune, A., Isaac, J. T., Molnar, E., Noel, J., Nash, S. R., Tagaya, M., Collingridge, G. L., Nakanishi, S., and Henley, J. M. (1998) NSF binding to GluR2 regulates synaptic transmission. Neuron 21, 87-97
81. 2 adrenoceptor trafficking and signaling in cardiomyocytes. Mol. Pharmacol. 72, 429-439
82. +-ATPase and the Golgi apparatus in the recycling of PTH/PTHrP receptor. Am. J. Physiol. Endocrinol. Metab. 286, E704-E710
83. Garrido, J. L., Wheeler, D., Vega, L. L., Friedman, P. A., and Romero, G. (2009) Role of phospholipase D in parathyroid hormone type 1 receptor signaling and trafficking. Mol. Endocrinol. 23, 2048-2059
84. van Dam, E. M., Ten Broeke, T., Jansen, K., Spijkers, P., and Stoorvogel, W. (2002) Endocytosed transferrin receptors recycle via distinct dynamin and phosphatidylinositol 3-kinase-dependent pathways. J. Biol. Chem. 277, 48876-48883
85. Arighi, C. N., Hartnell, L. M., Aguilar, R. C., Haft, C. R., and Bonifacino, J. S. (2004) Role of the mammalian retromer in sorting of the cation-independent mannose 6-phosphate receptor. J. Cell Biol. 165, 123-133
86. Alonso, V., and Friedman, P. A. (2013) Minireview: ubiquitination-regulated G protein-coupled receptor signaling and trafficking. Mol. Endocrinol. 27, 558-572
87. Ryu, J. K., Min, D., Rah, S. H., Kim, S. J., Park, Y., Kim, H., Hyeon, C., Kim, H. M., Jahn, R., and Yoon, T. Y. (2015) Spring-loaded unraveling of a single SNARE complex by NSF in one round of ATP turnover. Science 347, 1485-1489
88. Chan, A. S. M., 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., and Pavlos, N. J. (2016) Sorting Nexin 27 couples PTHR trafficking to retromer for signal regulation in osteoblasts during bone growth. Mol. Biol. Cell 27, 1367-1382
89. Lee, S., Chang, J., and Blackstone, C. (2016) FAM21 directs SNX27-retromer cargoes to the plasma membrane by preventing transport to the Golgi apparatus. Nat. Commun. 7, 10939
90. Peng, Y., Ayaz-Guner, S., Yu, D., and Ge, Y. (2014) Top-down mass spectrometry of cardiac myofilament proteins in health and disease. Proteomics Clin. Appl. 8, 554-568