Novel, gel-free proteomics approach identifies RNF5 and JAMP as modulators of GPCR stability

Molecular Endocrinology

Volumn 27, Issue 8, 2013, Pages 1245-1266

  Roy, Sébastien J ^a   Glazkova, Irina ^b   Fréchette, Louis ^a   Iorio Morin, Christian ^a   Binda, Chantal ^a   Pétrin, Darlaine ^b   Trieu, Phan ^b   Robitaille, Mélanie ^c   Angers, Stéphane ^c   Hébert, Terence E ^b   Parent, Jean Luc ^a  

^a Centre Hospitalier Universitaire de Sherbrooke   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOCRINE MOTILITY FACTOR RECEPTOR; BETA 2 ADRENERGIC RECEPTOR; G PROTEIN COUPLED RECEPTOR; JNK ASSOCIATED MEMBRANE PROTEIN; MEMBRANE PROTEIN; PROSTAGLANDIN D2 RECEPTOR; PROSTAGLANDIN RECEPTOR; PROTEASOME; RING FINGER PROTEIN 5; SMALL INTERFERING RNA; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

ARTICLE; CELL SURFACE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MASS SPECTROMETRY; OUTER MEMBRANE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN STABILITY; PROTEOMICS; UBIQUITINATION;

CARRIER PROTEINS; CELL LINE; DNA-BINDING PROTEINS; ENDOPLASMIC RETICULUM; HEK293 CELLS; HUMANS; MEMBRANE GLYCOPROTEINS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN TRANSPORT; PROTEOMICS; RECEPTORS, ADRENERGIC, BETA-2; RECEPTORS, IMMUNOLOGIC; RECEPTORS, PROSTAGLANDIN; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84880768521     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2013-1091     Document Type: Article

References (79)

1. Galès C, Van Durm JJ, Schaak S, et al. Probing the activationpromoted structural rearrangements in preassembled receptor-G protein complexes. Nat Struct Mol Biol. 2006;13:778-786
2. Gaès C, Rebois RV, Hogue M, et al. Real-time monitoring of receptor and G-protein interactions in living cells. Nat Meth. 2005; 2:177-184
3. Dupré DJ, Robitaille M, Éthier N, et al. Seven transmembrane receptor core signaling complexes are assembled prior to plasma membrane trafficking. J Biol Chem. 2006;281:34561-34573
4. Dupré DJ, Baragli A, Rebois RV, Éthier N, Hébert TE. Signalling complexes associated with adenylyl cyclase II are assembled during their biosynthesis. Cell Signal. 2007;19:481-489
5. Dupré DJ, Robitaille M, Rebois RV, Hébert TE. The role of Gβγ subunits in the organization, assembly, and function of GPCR signaling complexes. Ann Rev Pharmacol Toxicol. 2009;49:31-56
6. Nobles M, Benians A, Tinker A. Heterotrimeric G proteins precouple with G protein-coupled receptors in living cells. Proc Natl Acad Sci USA. 2005;102:18706-18711
7. Lavine N, Ethier N, Oak JN, et al. Gprotein-coupled receptors form stable complexes with inwardly rectifying potassium channels and adenylyl cyclase. J Biol Chem. 2002;277:46010-46019
8. Floyd DH, Geva A, Bruinsma SP, Overton MC, Blumer KJ, Baranski TJ. C5a receptor oligomerization. J Biol Chem. 2003;278: 35354-35361
9. Marshall FH, Jones KA, Kaupmann K, Bettler B. GABAB receptors- the first 7TM heterodimers. Trends Pharmacol Sci. 1999;20: 396-399
10. Issafras H, Angers S, Bulenger S, et al. Constitutive agonist-independent CCR5 oligomerization and antibody-mediated clustering occurring at physiological levels of receptors. J Biol Chem. 2002; 277:34666-34673
11. Overton MC, Blumer KJ. The extracellular N-terminal domain and transmembrane domains 1 and 2 mediate oligomerization of a yeast Gprotein-coupled receptor. J Biol Chem. 2002;277:41463-41472
12. Terrillon S, Durroux T, Mouillac B, et al. Oxytocin and vasopressin V1a and V2 receptors form constitutive homo- and heterodimers during biosynthesis. Mol Endocrinol. 2003;17:677-691
13. Salahpour A, Angers S, Mercier J-F, Lagacé M, Marullo S, Bouvier M. Homodimerization of the β2-adrenergic receptor as a prerequisite for cell surface targeting. J Biol Chem. 2004;279:33390-33397
14. Hegde RS, Ploegh HL. Quality and quantity control at the endoplasmic reticulum. Curr Opin Cell Biol. 2010;22:437-446
15. Vembar SS, Brodsky JL. One step at a time: endoplasmic reticulumassociated degradation. Nat Rev Mol Cell Biol. 2008;9:944-957
16. Haack KK, Tougas MR, Jones KT, El-Dahr SS, Radhakrishna H, McCarty NA. A novel bioassay for detecting GPCR heterodimerization: transactivation of β2 adrenergic receptor by bradykinin receptor. J Biomol Screen. 2010;15:251-260
17. Cook LB, Zhu CC, Hinkle PM. Thyrotropin-releasing hormone receptor processing: role of ubiquitination and proteasomal degradation. Mol Endocrinol. 2003;17:1777-1791
18. Lu M, Echeverri F, Moyer BD. Endoplasmic reticulum retention, degradation, and aggregation of olfactory G-protein coupled receptors. Traffic. 2003;4:416-433
19. Illing ME, Rajan RS, Bence NF, Kopito RR. A rhodopsin mutant linked to autosomal dominant retinitis pigmentosa is prone to aggregate and interacts with the ubiquitin proteasome system. J Biol Chem. 2002;277:34150-34160
20. Huang Y, Niwa J, Sobue G, Breitwieser GE. Calcium-sensing receptor ubiquitination and degradation mediated by the E3 ubiquitin ligase dorfin. J Biol Chem. 2006;281:11610-11617
21. Petaja-Repo UE, Hogue M, Laperriere A, Bhalla S, Walker P, Bouvier M. Newly synthesized human delta opioid receptors retained in the endoplasmic reticulum are retrotranslocated to the cytosol, deglycosylated, ubiquitinated, and degraded by the proteasome. J Biol Chem. 2001;276:4416-4423
22. Kotlikoff MI, Kamm KE. Molecular mechanisms of β-adrenergic relaxation of airway smooth muscle. Ann Rev Physiol. 1996;58: 115-141
23. Ecker PM, Lin CC, Powers J, Kobilka BK, Dubin AM, Bernstein D. Effect of targeted deletions of β1- and β2-adrenergic-receptor subtypes on heart rate variability. Am J Physiol Heart Circ Physiol. 2006;290:H192-H199
24. Parent A, Roy SJ, Iorio-Morin C, et al. ANKRD13C acts as a molecular chaperone for G protein-coupled receptors. J Biol Chem. 2010;285:40838-40851
25. Nagata K, Hirai H. The second PGD(2) receptor CRTH2: structure, properties, and functions in leukocytes. Prostaglandins Leukot Essent Fatty Acids. 2003;69:169-177
26. Joazeiro CA, Weissman AM. RING finger proteins: mediators of ubiquitin ligase activity. Cell. 2000;102:549-552
27. Didier C, Broday L, Bhoumik A, et al. RNF5, a RING finger protein that regulates cell motility by targeting paxillin ubiquitination and altered localization. Mol Cell Biol. 2003;23:5331-5345
28. Tcherpakov M, Broday L, Delaunay A, et al. JAMP optimizes ERAD to protect cells from unfolded proteins. Mol Biol Cell. 2008; 19:5019-5028
29. Younger JM, Chen L, Ren HY, et al. Sequential quality-control checkpoints triage misfolded cystic fibrosis transmembrane conductance regulator. Cell. 2006;126:571-582
30. Morito D, Hirao K, Oda Y, et al. Gp78 cooperates with RMA1 in endoplasmic reticulum-associated degradation of CFTRDeltaF508. Mol Biol Cell. 2008;19:1328-1336
31. Lee K, Hong TJ, Hahn JS. Roles of 17-AAG-induced molecular chaperones and Rma1 E3 ubiquitin ligase in folding and degradation of Pendrin. FEBS Lett. 2012;586:2535-2541
32. Angers S, Thorpe CJ, Biechele TL, et al. The KLHL12-Cullin-3 ubiquitin ligase negatively regulates the Wnt-β-catenin pathway by targeting Dishevelled for degradation. Nat Cell Biol. 2006;8:348-357
33. Masri B, Salahpour A, Didriksen M, et al. Antagonism of dopamine D2 receptor/β-arrestin 2 interaction is a common property of clinically effective antipsychotics. Proc Natl Acad Sci USA. 2008;105: 13656-13661
34. Roy SJ, Parent A, Gallant MA, de Brum-Fernandes AJ, Stanková J, Parent JL. Characterization of C-terminal tail determinants involved in CRTH2 receptor trafficking: identification of a recycling motif. Eur J Pharmacol. 2010;630:10-18
35. Parent JL, Labrecque P, Orsini MJ, Benovic JL. Internalization of the TXA2 receptor alpha and beta isoforms: role of the differentially spliced cooh terminus in agonist-promoted receptor internalization. J Biol Chem. 1999;274:8941-8948
36. Goupil E, Tassy D, Bourguet C, et al. A novel biased allosteric compound inhibitor of parturition selectively impedes the prostaglandin F2_-mediated Rho/ROCK signaling pathway. J Biol Chem. 2010;285:25624-25636
37. Ahmed SM, Daulat AM, Angers S. G protein βγ subunits regulate cell adhesion through Rap1a and its effector Radil. J. Biol. Chem. 2010;285:6538-6551
38. Angers S. Proteomic Analyses of Protein Complexes in the Wnt Pathway, Wnt Signaling. In: Vincan, E, ed. Totowa, NJ: Humana Press; 2008:223-230
39. Xiao K, Shenoy SK. β2-adrenergic receptor lysosomal trafficking is regulated by ubiquitination of lysyl residues in two distinct receptor domains. J Biol Chem. 2011;286:12785-12795
40. Martin NP, Lefkowitz RJ, Shenoy SK. Regulation of V2 vasopressin receptor degradation by agonist-promoted ubiquitination. J Biol Chem. 2003;278:45954-45959
41. Berthouze M, Venkataramanan V, Li Y, Shenoy SK. The deubiquitinases USP33 and USP20 coordinate beta2 adrenergic receptor recycling and resensitization. EMBO J. 2009;28:1684-1696
42. Shenoy SK, Modi AS, Shukla AK, et al. Beta-arrestin-dependent signaling and trafficking of 7-transmembrane receptors is reciprocally regulated by the deubiquitinase USP33 and the E3 ligase Mdm2. Proc Natl Acad Sci USA. 2009;106:6650-6655
43. Marchese A, Benovic JL. Ubiquitination of G-protein-coupled receptors. Methods Mol Biol. 2004;259:299-305
44. Lavoie C, Mercier JF, Salahpour A, et al. β1/β2-adrenergic receptor heterodimerization regulates β2-adrenergic receptor internalization and ERK signaling efficacy. J Biol Chem. 2002;277:35402-35410
45. Gallant MA, Slipetz D, Hamelin E, et al. Differential regulation of the signaling and trafficking of the two prostaglandin D2 receptors, prostanoid DP receptor and CRTH2. Eur J Pharmacol. 2007;557: 115-123
46. Parent JL, Labrecque P, Driss Rochdi M, Benovic JL. Role of the differentially spliced carboxyl terminus in thromboxane A2 receptor trafficking: identification of a distinct motif for tonic internalization. J Biol Chem. 2001;276:7079-7085
47. Lachance V, Cartier A, Génier S, et al. Regulation of beta2-adrenergic receptor maturation and anterograde trafficking by an interaction with Rab geranylgeranyltransferase: modulation of Rab geranylgeranylation by the receptor. J Biol Chem. 2011;286:40802-40813
48. Linke D. Detergents: An Overview. In: Richard RB, Murray PD, eds. Methods in Enzymology. Waltham, MA: Academic Press; 2009:603-617
49. Oner SS, Kaya AI, Onaran HO, Ozcan G, Ugur Ö. β2-Adrenoceptor, Gs and adenylate cyclase coupling in purified detergent-resistant, low density membrane fractions. Eur J Pharmacol. 2010;630: 42-52
50. Cerione RA., Codina J, Benovic JL, Lefkowitz RJ, Birnbaumer L, Caron MG. Mammalian beta.2-adrenergic receptor: reconstitution of functional interactions between pure receptor and pure stimulatory nucleotide binding protein of the adenylate cyclase system. Biochemistry. 1984;23:4519-4525
51. Yeung Y-G, Stanley E R. Rapid detergent removal from peptide samples with ethyl acetate for mass spectrometry analysis. In: Current Protocols in Protein Science. John Wiley, Sons, Inc; 2010:59: 16.12.1-16.12.5
52. Daulat AM, Maurice P, Froment C, et al. Purification and identification of G protein-coupled receptor protein complexes under native conditions. Mol Cell Proteomics. 2007;6:835-844
53. Cong M, Perry SJ, Hu LA, Hanson PI, Claing A, Lefkowitz RJ. Binding of the β2 adrenergic receptor to N-ethylmaleimide-sensitive factor regulates receptor recycling. J Biol Chem. 2001;276: 45145-45152
54. Daaka Y, Luttrell LM, Lefkowitz RJ. Switching of the coupling of the β2-adrenergic receptor to different G proteins by protein kinase A. Nature. 1997;390:88-91
55. Hall RA, Ostedgaard LS, Premont RT, et al. A C-terminal motif found in the β2-adrenergic receptor, P2Y1 receptor and cystic fibrosis transmembrane conductance regulator determines binding to the Na+/H+ exchanger regulatory factor family of PDZ proteins. Proc Natl Acad Sci USA. 1998;95:8496-8501
56. Park S-H, Bolender N, Eisele F, et al. The cytoplasmic Hsp70 chaperone machinery subjects misfolded and endoplasmic reticulum import- incompetent proteins to degradation via the ubiquitin-proteasome system. Mol Biol Cell. 2007;18:153-165
57. Bukau B, Weissman J, Horwich A. Molecular chaperones and protein quality control. Cell. 2006;125:443-451
58. Caramelo JJ, Parodi AJ. Getting in and out from calnexin/calreticulin cycles. J Biol Chem. 2008;283:10221-10225
59. Gorbea C, Goellner GM, Teter K, Holmes RK, Rechsteiner M. Characterization of mammalian Ecm29, a 26 S proteasome-associated protein that localizes to the nucleus and membrane vesicles. J Biol Chem. 2004;279:54849-54861
60. Zhong B, Zhang Y, Tan B, Liu TT, Wang YY, Shu HB. The E3 ubiquitin ligase RNF5 targets virus-induced signaling adaptor for ubiquitination and degradation. J Immunol. 2010;184:6249-6255
61. Pilon M, Schekman R, Römisch K. Sec61p mediates export of a misfolded secretory protein from the endoplasmic reticulum to the cytosol for degradation. EMBO J. 1997;16:4540-4548
62. Ye Y, Shibata Y, Kikkert M, van Voorden S, Wiertz E, Rapoport TA. Recruitment of the p97 ATPase and ubiquitin ligases to the site of retrotranslocation at the endoplasmic reticulum membrane. Proc Natl Acad Sci USA. 2005;102:14132-14138
63. Schubert U, Antón LC, Gibbs J, Norbury CC, Yewdell JW, Bennink JR. Rapid degradation of a large fraction of newly synthesized proteins by proteasomes. Nature. 2000;404:770-774
64. Zhong X, Shen Y, Ballar P, Apostolou A, Agami R, Fang S. AAA ATPase p97/valosin-containing protein interacts with gp78, a ubiquitin ligase for endoplasmic reticulum-associated degradation. J Biol Chem. 2004;279:45676-45684
65. Zhong B, Zhang L, Lei C, et al. The ubiquitin ligase RNF5 regulates antiviral responses by mediating degradation of the adaptor protein MITA. Immunity. 2009;30:397-407
66. Tcherpakov M, Delaunay A, Toth J, Kadoya T, Petroski MD, Ronai ZA. Regulation of endoplasmic reticulum-associated degradation by RNF5-dependent ubiquitination of JNK-associated membrane protein (JAMP). J Biol Chem. 2009;284:12099-12109
67. Francesconi A, Kumari R, Zukin RS. Proteomic analysis reveals novel binding partners of metabotropic glutamate receptor 1. J Neurochem. 2009;108:1515-1525
68. Bartoi T, Rigbolt KT, Du D, Köhr G, Blagoev B, Kornau HC. GABAB receptor constituents revealed by tandem affinity purification from transgenic mice. J Biol Chem. 2010;285:20625-20633
69. Wacker JL, Feller DB, Tang XB, et al. Disease-causing mutation in GPR54 reveals the importance of the second intracellular loop for class A G-protein-coupled receptor function. J Biol Chem. 2008; 283:31068-31078
70. Lyssand JS, DeFino MC, Tang XB, et al. Blood pressure is regulated by an _1D-adrenergic receptor/dystrophin signalosome. J Biol Chem. 2008;283:18792-18800
71. Free RB, Hazelwood LA, Cabrera DM, et al. D1 and D2 dopamine receptor expression is regulated by direct interaction with the chaperone protein calnexin. J Biol Chem. 2007;282:21285-21300
72. He F, Qiao Z-H, Cai J, Pierce W, He D-C, Song Z-H. Involvement of the 90-kDa heat shock protein (Hsp-90) in CB2 cannabinoid receptor-mediated cell migration: a new role of Hsp-90 in migration signaling of a G protein-coupled receptor. Mol Pharmacol. 2007; 72:1289-1300
73. Nilsson J, Ståhl S, Lundeberg J, Uhlén M, Nygren P-å. Affinity fusion strategies for detection, purification, and immobilization of recombinant proteins. Prot Expr Purif. 1997;11:1-16
74. Puig O, Caspary F, Rigaut G, et al. The tandem affinity purification (TAP) method: a general procedure of protein complex purification. Methods. 2001;24:218-229
75. Vanaken T, Foxall-Vanaken S, Castleman S, Ferguson-Miller S. [3] Alkyl glycoside detergents: Synthesis and applications to the study of membrane proteins. In: Sidney Fleischer BF, ed. Methods in Enzymology. Waltham, MA: Academic Press; 1986:27-35
76. Wisniewski JR, Zougman A, Nagaraj N, Mann M. Universal sample preparation method for proteome analysis. Nat Methods. 2009; 6:359-362
77. Speers AE, Wu CC. Proteomics of integral membrane proteins: theory and application. Chem Rev. 2007;107:3687-3714
78. Alonso V, Friedman PA. Minireview: ubiquitination-regulated G protein-coupled receptor signaling and trafficking. Mol Endocrinol. 2013;27:558-572
79. Alonso V, Magyar CE, Wang B, Bisello A, Friedman PA. Ubiquitination- deubiquitination balance dictates ligand-stimulated PTHR sorting. J Bone Mineral Res. 2011;26:2923-2934.