Mechanisms of melanocortin-2 receptor (MC2R) internalization and recycling in human embryonic kidney (HEK) cells: Identification of key Ser/Thr (S/T) amino acids

Molecular Endocrinology

Volumn 25, Issue 11, 2011, Pages 1961-1977

  Roy, Simon ^a   Roy, Sébastien Jean ^a   Pinard, Sandra ^a   Taillefer, Louis Daniel ^a   Rached, Mohamed ^a   Parent, Jean Luc ^a   Gallo Payet, Nicole ^a  

^a UNIVERSITY OF SHERBROOKE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CLATHRIN; CYCLIC AMP; DYNAMIN; MELANOCORTIN 2 RECEPTOR; MELANOCORTIN 2 RECEPTOR ACCESSORY PROTEIN 1; MELANOCORTIN 2 RECEPTOR ACCESSORY PROTEIN 2; PEPTIDES AND PROTEINS; RETINA S ANTIGEN; SERINE; THREONINE; UNCLASSIFIED DRUG;

ARTICLE; CELL MEMBRANE; CELL SURFACE; ENDOSOME; HUMAN; KIDNEY CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION;

ARRESTINS; BLOTTING, WESTERN; CELL LINE; CELL MEMBRANE; CYCLIC AMP; DYNAMINS; ENDOSOMES; ENZYME-LINKED IMMUNOSORBENT ASSAY; HUMANS; IMMUNOPRECIPITATION; MICROSCOPY, FLUORESCENCE; PROTEIN BINDING; RECEPTOR, MELANOCORTIN, TYPE 2; SERINE; THREONINE;

EID: 80054972845     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2011-0018     Document Type: Article

References (63)

1. Sewer MB, Waterman MR 2003 ACTH modulation of transcription factors responsible for steroid hydroxylase gene expression in the adrenal cortex. Microsc Res Tech 61:300-307
2. Gallo-Payet N, Payet MD 2003 Mechanism of action of ACTH: beyond cAMP. Microsc Res Tech 61:275-287
3. Forti FL, Dias MH, Armelin HA 2006 ACTH receptor: ectopic expression, activity and signaling. Mol Cell Biochem 293:147-160
4. Mountjoy KG, Robbins LS, Mortrud MT, Cone RD 1992 The cloning of a family of genes that encode the melanocortin receptors. Science 257:1248-1251
5. Chida D, Nakagawa S, Nagai S, Sagara H, Katsumata H, Imaki T, Suzuki H, Mitani F, Ogishima T, Shimizu C, Kotaki H, Kakuta S, Sudo K, Koike T, Kubo M, Iwakura Y 2007 Melanocortin 2 receptor is required for adrenal gland development, steroidogenesis, and neonatal gluconeogenesis. Proc Natl Acad Sci USA 104:18205-18210
6. Chung TT, Webb TR, Chan LF, Cooray SN, Metherell LA, King PJ, Chapple JP, Clark AJ 2008 The majority of adrenocorticotropin receptor (melanocortin 2 receptor) mutations found in familial glu-cocorticoid deficiency type 1 lead to defective trafficking of the receptorto the cell surface. J Clin Endocrinol Metab 93:4948-4954
7. Clark AJ, Chan LF, Chung TT, Metherell LA 2009 The genetics of familial glucocorticoid deficiency. Best Pract Res Clin Endocrinol Metab 23:159-165
8. Clark AJ, McLoughlin L, Grossman A 1993 Familial glucocorticoid deficiency associated with point mutation in the adrenocorticotro-pin receptor. Lancet 341:461-462
9. Metherell LA, Chapple JP, Cooray S, David A, Becker C, Rüschen-dorf F, Naville D, Begeot M, Khoo B, Nürnberg P, Huebner A, Cheetham ME, Clark AJ 2005 Mutations in MRAP, encoding a new interacting partner of the ACTH receptor, cause familial glucocorticoid deficiency type 2. Nat Genet 37:166-170
10. Lefkowitz RJ, Roth J, Pricer W, Pastan I 1970 ACTH receptors in the adrenal: specific binding of ACTH-125I and its relation to ad-enyl cyclase. Proc Natl Acad Sci USA 65:745-752
11. Penhoat A, Naville D, Begeot M 2001 The adrenocorticotrophic hormone receptor. Current Opinion Endocrinol Diabetes 8:112-117
12. Roy S, Rached M, Gallo-Payet N 2007 Differential regulation of the human adrenocorticotropin receptor [melanocortin-2 receptor (MC2R)] by human MC2R accessory protein isoforms α and β in isogenic human embryonic kidney 293 cells. Mol Endocrinol 21: 1656-1669
13. Cooray SN, Clark AJ 2010 Melanocortin receptors and their accessory proteins. Mol Cell Endocrinol 331:215-221
14. Hinkle PM, Sebag JA 2009 Structure and function of the melano-cortin2 receptor accessory protein (MRAP). Mol Cell Endocrinol 300:25-31
15. Dores RM 2009 Adrenocorticotropic hormone, melanocyte-stim-ulating hormone, and the melanocortin receptors: revisiting the work of Robert Schwyzer: a thirty-year retrospective. Ann NY Acad Sci 1163:93-100
16. Baig AH, Swords FM, Szaszak M, King PJ, Hunyady L, Clark AJ 2002 Agonist activated adrenocorticotropin receptor internalizes via a clathrin-mediated G protein receptor kinase dependent mechanism. Endocr Res 28:281-289
17. Clark AJ, Baig AH, Noon L, Swords FM, Hunyady L, King PJ 2003 Expression, desensitization, and internalization of the ACTH receptor (MC2R). Ann NY Acad Sci 994:111-117
18. Kilianova Z, Basora N, Kilian P, Payet MD, Gallo-Payet N 2006 Human MC2R expression and functionality. Effect of PKA and PKC on desensitization and internalization. Endocrinology 147: 2325-2337
19. Laporte SA, Oakley RH, Holt JA, Barak LS, Caron MG 2000 The interaction of β-arrestin with the AP-2 adaptor is required for the clustering of β 2-adrenergic receptor into clathrin-coated pits. J Biol Chem 275:23120-23126
20. Oakley RH, Laporte SA, Holt JA, Barak LS, Caron MG 2001 Molecular determinants underlying the formation of stable intracellular G protein-coupled receptor- β -arrestin complexes after receptor endocytosis. J Biol Chem 276:19452-19460
21. Lefkowitz RJ, Shenoy SK 2005 Transduction of receptor signals by β -arrestins. Science 308:512-517
22. Marchese A, Paing MM, Temple BR, Trejo J 2008 G protein-coupled receptor sorting to endosomes and lysosomes. Annu Rev Pharmacol Toxicol 48:601-629
23. Gaborik Z, Hunyady L 2004 Intracellular trafficking of hormone receptors. Trends Endocrinol Metab 15:286-293
24. Seachrist JL, Ferguson SS 2003 Regulation of G protein-coupled receptor endocytosis and trafficking by Rab GTPases. Life Sci 74: 225-235
25. Schwartz SL, Cao C, Pylypenko O, Rak A, Wandinger-Ness A 2007 Rab GTPases at a glance. J Cell Sci 120:3905-3910
26. Noon LA, Franklin JM, King PJ, Goulding NJ, Hunyady L, Clark AJ 2002 Failed export of the adrenocorticotrophin receptor from the endoplasmic reticulum in non-adrenal cells: evidence in support of a requirement for a specific adrenal accessory factor. J Endocrinol 174:17-25
27. Rached M, El Mourabit H, Buronfosse A, Blondet A, Naville D, Begeot M, Penhoat A 2005 Expression of the human melanocortin-2 receptor in different eukaryotic cells. Peptides 26:1842-1847
28. Webb TR, Clark AJ 2010 Minireview: the melanocortin 2 receptor accessory proteins. Mol Endocrinol 24:475-484
29. Gallo-Payet N, Payet MD 1989 Excitation-secretion coupling: involvement of potassium channels in ACTH-stimulated rat adrenocortical cells. J Endocrinol 120:409-421
30. Gallo-Payet N, Grazzini E, Cote M, Chouinard L, Chorvatova A, Bilodeau L, Payet MD, Guillon G 1996 Role of calcium in the mechanism of action of ACTH in human adrenocortical cells. J Clin Invest 98:460-466
31. Roy S, Perron B, Gallo-Payet N 2010 Role of asparagine-linked glycosylation in cell surface expression and function of the human adrenocorticotropin receptor (melanocortin 2 receptor) in 293/ FRT cells. Endocrinology 151:660-670
32. Sebag JA, Hinkle PM 2009 Regions of melanocortin 2 (MC2) receptor accessory protein necessary for dual topology and MC2 receptor trafficking and signaling. J Biol Chem 284:610-618
33. Orsini MJ, Benovic JL 1998 Characterization of dominant negative arrestins that inhibit β 2-adrenergic receptor internalization by distinct mechanisms. J Biol Chem 273:34616-34622
34. Mundell SJ, Orsini MJ, Benovic JL 2002 Characterization of arres-tin expression and function. Methods Enzymol 343:600-611
35. Takei K, Slepnev VI, De Camilli P 2001 Interactions of dynamin and amphiphysin with liposomes. Methods Enzymol 329:478-486
36. Jean-Alphonse F, Hanyaloglu AC 2011 Regulation of GPCR signal networks via membrane trafficking. Mol Cell Endocrinol 331:205-214
37. Donaldson JG, Finazzi D, Klausner RD 1992 Brefeldin A inhibits Golgi membrane-catalysed exchange of guanine nucleotide onto ARF protein. Nature 360:350-352
38. Dinter A, Berger EG 1998 Golgi-disturbing agents. Histochem Cell Biol 109:571-590
39. Lichtshtein D, Dunlop K, Kaback HR, Blume AJ 1979 Mechanism of monensin-induced hyperpolarization of neuroblastoma-glioma hybrid NG108-15. Proc Natl Acad Sci USA 76:2580-2584
40. Stein BS, Bensch KG, Sussman HH 1984 Complete inhibition of transferrin recycling by monensin in K562 cells. J Biol Chem 259: 14762-14772
41. Sanchez-Laorden BL, Jiménez-Cervantes C, García-Borrón JC 2007 Regulation of human melanocortin 1 receptor signaling and trafficking by Thr-308 and Ser-316 and its alteration in variant alleles associated with red hair and skin cancer. J Biol Chem 282: 3241-3451
42. Sánchez-Laorden BL, Herraiz C, Valencia JC, Hearing VJ, Jiménez-Cervantes C, García-Borrón JC 2009 Aberrant trafficking of human melanocortin 1 receptor variants associated with red hair and skin cancer: steady-state retention of mutant forms in the proximal golgi. J Cell Physiol 220:640-654
43. Roy SJ, Parent A, Gallant MA, de Brum-Fernandes AJ, Stankova ́ J, Parent JL 2010 Characterization of C-terminal tail determinants involved in CRTH2 receptor trafficking: identification of a recycling motif. Eur J Pharmacol 630:10-18
44. Sever S, Damke H, Schmid SL 2000 Dynamin:GTP controls the formation of constricted coated pits, the rate limiting step in clath-rin-mediated endocytosis. J Cell Biol 150:1137-1148
45. Hansen SH, Sandvig K, van Deurs B 1993 Clathrin and HA2 adaptors: effects of potassium depletion, hypertonic medium, and cyto-sol acidification. J Cell Biol 121:61-72
46. Cai M, Varga EV, Stankova M, Mayorov A, Perry JW, Yamamura HI, Trivedi D, Hruby VJ 2006 Cell signaling and trafficking of human melanocortin receptors in real time using two-photon fluorescence and confocal laser microscopy: differentiation of agonists and antagonists. Chem Biol Drug Des 68:183-193
47. Sebag JA, Hinkle PM 2007 Melanocortin-2 receptor accessory protein MRAP forms antiparallel homodimers. Proc Natl Acad Sci USA 104:20244-20249
48. Côté M, Guillon G, Payet MD, Gallo-Payet N 2001 Expression and regulation of adenylyl cyclase isoforms in the human adrenal gland. J Clin Endocrinol Metab 86:4495-4503
49. Tremblay E, Payet MD, Gallo-Payet N 1991 Effects of ACTH and angiotensin II on cytosolic calcium in cultured adrenal glomerulosa cells. Role of cAMP production in the ACTH effect. Cell Calcium 12:655-673
50. Fridmanis D, Petrovska R, Kalnina I, Slaidina M, Peculis R, Schioth HB, Klovins J 2010 Identification of domains responsible for specific membrane transport and ligand specificity of the ACTH receptor (MC2R). Mol Cell Endocrinol 321:175-183
51. Moore SA, Patel AS, Huang N, Lavin BC, Grammatopoulos TN, Andres RD, Weyhenmeyer JA 2002 Effects of mutations in the highly conserved DRY motif on binding affinity, expression, and G-protein recruitment of the human angiotensin II type-2 receptor. Brain Res Mol Brain Res 109:161-167
52. Yamano Y, Kamon R, Yoshimizu T, Toda Y, Oshida Y, Chaki S, Yoshioka M, Morishima I 2004 The role of the DRY motif of human MC4R for receptor activation. Biosci Biotechnol Biochem 68:1369-1371
53. Lembo PM, Ghahremani MH, Morris SJ, Albert PR 1997 A conserved threonine residue in the second intracellular loop of the 5-hydroxytryptamine 1A receptor directs signaling specificity. Mol Pharmacol 52:164-171
54. Prado GN, Mierke DF, Pellegrini M, Taylor L, Polgar P 1998 Motif mutation of bradykinin B2 receptor second intracellular loop and proximal C terminus is critical for signal transduction, internalization, and resensitization. J Biol Chem 273:33548-33555
55. Kushwaha N, Harwood SC, Wilson AM, Berger M, Tecott LH, Roth BL, Albert PR 2006 Molecular determinants in the second intracellular loop of the 5-hydroxytryptamine-1A receptor for G-protein coupling. Mol Pharmacol 69:1518-1526
56. Slavotinek AM, Hurst JA, Dunger D, Wilkie AO 1998 ACTH receptor mutation in a girl with familial glucocorticoid deficiency. Clin Genet 53:57-62
57. Elias LL, Huebner A, Pullinger GD, Mirtella A, Clark AJ 1999 Functional characterization of naturally occurring mutations of the human adrenocorticotropin receptor: poor correlation of pheno-type and genotype. J Clin Endocrinol Metab 84:2766-2770
58. Chan LF, Webb TR, Chung TT, Meimaridou E, Cooray SN, Guasti L, Chapple JP, Egertova M, Elphick MR, Cheetham ME, Metherell LA, Clark AJ 2009 MRAP and MRAP2 are bidirectional regulators of the melanocortin receptor family. Proc Natl Acad Sci USA 106:6146-6151
59. Sebag JA, Hinkle PM 2009 Opposite effects of the melanocortin-2 (MC2) receptor accessory protein MRAP on MC2 and MC5 receptor dimerization and trafficking. J Biol Chem 284:22641-22648
60. Hwang GW, Oh SE, Takahashi T, Lee JY, Naganuma A 2010 siRNA-mediated knockdown of the melanocortin 2 receptor accessory protein 2 (MRAP2) gene confers resistance to methylmercury on HEK293 cells. J Toxicol Sci 35:947-950
61. Parent A, Hamelin E, Germain P, Parent JL 2009 Rab11 regulates the recycling of the /32-adrenergic receptor through a direct interaction. Biochem J 418:163-172
62. Zinchuk V, Zinchuk O, Okada T 2007 Quantitative colocalization analysis of multicolor confocal immunofluorescence microscopy images: pushing pixels to explore biological phenomena. Acta Histochem Cytochem 40:101-111
63. Clark AJ, Cammas FM 1996 The ACTH receptor. Baillieres Clin Endocrinol Metab 10:29-47