A constitutively active mutant of the human lutropin receptor (hLHR-L457R) escapes lysosomal targeting and degradation

Molecular Endocrinology

Volumn 20, Issue 11, 2006, Pages 2931-2945

  Galet, Colette ^a   Ascoli, Mario ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURFACE RECEPTOR; LEUPEPTIN; LUTEINIZING HORMONE RECEPTOR;

ARTICLE; CELL CYCLE; CELL HYPERPLASIA; CELL MUTANT; CELL STRAIN HEK293; CELL SURFACE; CELL TRANSPORT; CELLULAR DISTRIBUTION; GENE MUTATION; HORMONE ACTION; HORMONE BINDING; HUMAN; HUMAN CELL; LEYDIG CELL; LYSOSOME; MALE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN TARGETING; PUBERTY; SIGNAL TRANSDUCTION;

AMINO ACID SUBSTITUTION; ANIMALS; ANTIGENS, SURFACE; CELLS, CULTURED; CHORIONIC GONADOTROPIN; ENDOCYTOSIS; HUMANS; LYSOSOMES; MICE; MUTANT PROTEINS; PROTEIN DENATURATION; PROTEIN TRANSPORT; RECEPTORS, LH; TRANSFECTION;

EID: 33751542453     PISSN: 08888809     EISSN: 08888809     Source Type: Journal    
DOI: 10.1210/me.2006-0138     Document Type: Article

References (52)

1. Pierce KL, Lefkowitz RJ 2001 Classical and new roles of β-arrestins in the regulation of G-protein-coupled receptors. Nat Rev Neurosci 2:727-733
2. Miller WE, Lefkowitz RJ 2001 Expanding roles for β-arrestins as scaffolds and adapters in GPCR signaling and trafficking. Curr Opin Cell Biol 13:139-145
3. Ferguson SSG 2001 Evolving concepts in G protein-coupled receptor endocytosis: the role in receptor desensitization and signaling. Pharmacol Rev 53:1-24
4. Perry SJ, Lefkowitz RJ 2002 Arresting developments in heptahelical receptor signaling and regulation. Trends Cell Biol 12:130-138
5. Sorkin A, von Zastrow M 2002 Signal transduction and endocytosis: close encounters of many kinds. Nat Rev Mol Cell Biol 3:600-614
6. Marchese A, Chen C, Kim Y-M, Benovic JL 2003 The ins and outs of G protein-coupled receptor trafficking. Trends Biochem Sci 28:369-376
7. Tsao P, Cao T, von Zastrow M 2001 Role of endocytosis in mediating downregulation of G-protein-coupled receptors. Trends Pharmacol Sci 22:91-96
8. Hicke L 2001 Protein regulation by monoubiquitin. Nat Rev Mol Cell Biol 2:195-201
9. Hicke L 2001 A new ticket for entry into budding vesicles-ubiquitin. Cell 106:527-530
10. Ascoli M 1984 Lysosomal accumulation of the hormone-receptor complex during receptor-mediated endocytosis of human choriogonadotropin. J Cell Biol 99:1242-1250
11. Wang H, Segaloff DL, Ascoli M 1991 Lutropin/choriogonadotropin down-regulates its receptor by both receptor mediated endocytosis and a cAMP-dependent reduction in receptor mRNA. J Biol Chem 266:780-785
12. Bhaskaran RS, Ascoli M 2005 The post-endocytotic fate of the gonadotropin receptors is an important determinant of the desensitization of gonadotropin responses. J Mol Endocrinol 34:447-457
13. Trejo J, Hammes SR, Coughlin SR 1998 Termination of signaling by protease-activated receptor-1 is linked to lysosomal sorting. Proc Natl Acad Sci USA 95:13698-13702
14. Trejo J, Coughlin SR 1999 The cytoplasmic tails of protease-activated receptor-1 and substance P receptor specify sorting to lysosomes versus recycling. J Biol Chem 274:2216-2224
15. Bremnes T, Paasche JD, Mehlum A, Sandberg C, Bremnes B, Attramadal H 2000 Regulation and intracellular trafficking pathways of the endothelin receptors. J Biol Chem 275:17596-17604
16. Kishi M, Liu X, Hirakawa T, Reczek D, Bretscher A, Ascoli M 2001 Identification of two distinct structural motifs that, when added to the C-terminal tail of the rat lutropin receptor, redirect the internalized hormone-receptor complex from a degradation to a recycling pathway. Mol Endocrinol 15:1624-1635
17. Galet C, Min L, Narayanan R, Kishi M, Weigel NL, Ascoli M 2003 Identification of a transferable two amino acid motif (GT) present in the C-terminal tail of the human lutropin receptor that redirects internalized G protein-coupled receptors from a degradation to a recycling pathway. Mol Endocrinol 17:411-422
18. Hirakawa T, Galet C, Kishi M, Ascoli M 2003 GIPC binds to the human lutropin receptor (LHR) through an unusual PDZ domain binding motif and it regulates the sorting of the internalized human choriogonadotropin (hCG) and the density of cell surface LHR. J Biol Chem 278:49348-49357
19. Galet C, Hirakawa T, Ascoli M 2004 The postendocytotic trafficking of the hLHR is mediated by a transferable motif consisting of the C-terminal cysteine and an upstream leucine. Mol Endocrinol 18:434-446
20. Ascoli M, Fanelli F, Segaloff DL 2002 The lutropin/choriogonadotropin receptor. A 2002 perspective. Endocr Rev 23:141-174
21. Themmen APN 2005 An update of the pathophysiology of human gonadotrophin subunit and receptor gene mutations and polymorphisms. Reproduction 130:263-274
22. Min K-S, Liu X, Fabritz J, Jaquette J, Abell AN, Ascoli M 1998 Mutations that induce constitutive activation and mutations that impair signal transduction modulate the basal and/or agonist-stimulated internalization of the lutropin/choriogonadotropin receptor. J Biol Chem 273:34911-34919
23. Min L, Ascoli M 2000 Effect of activating and inactivating mutations on the phosphorylation and trafficking of the human lutropin/choriogonadotropin receptor. Mol Endocrinol 14:1797-1810
24. Min L, Galet C, Ascoli M 2002 The association of arrestin-3 with the human lutropin/choriogonadotropin receptor depends mostly on receptor activation rather than on receptor phosphorylation. J Biol Chem 277:702-710
25. Bradbury FA, Menon KMJ 1999 Evidence that constitutively active luteinizing hormone/human chorionic gonadotropin receptors are rapidly internalized. Biochemistry 38:8703-8712
26. Munshi UM, Clouser CL, Peegel H, Menon KMJ 2005 Evidence that palmitoylation of carboxyl terminus cysteine residues of the human luteinizing hormone receptor regulates postendocytic processing. Mol Endocrinol 19:749-758
27. Latronico AC, Abell AN, Arnhold IJP, Liu X, Lins TSS, Brito VN, Bilerbeck AE, Segaloff DL, Mendonica BB 1998 A unique constitutively activating mutation in third transmbembrane helix of luteinizing hormone receptor causes sporadic male gonadotropin-independent precocious puberty. J Clin Endocrinol Metab 83:2435-2440
28. Shinozaki H, Fanelli F, Liu X, Butterbrodt J, Nakamura K, Segaloff DL 2001 Pleiotropic effects of substitutions of a highly conserved leucine in transmembrane helix III of the human lutropin/choriogonadotropin receptor with respect to constitutive activation and hormone responsiveness. Mol Endocrinol 15:972-984
29. Hirakawa T, Ascoli M 2003 A constitutively active somatic mutation of the human lutropin receptor found in Leydig cell tumors activates the same families of G proteins as germ line mutations associated with Leydig cell hyperplasia. Endocrinology 144:3872-3878
30. Hirakawa T, Galet C, Ascoli M 2002 MA-10 cells transfected with the human lutropin/choriogonadotropin receptor (hLHR). A novel experimental paradigm to study the functional properties of the hLHR. Endocrinology 143:1026-1035
31. Nakamura K, Lazari MFM, Li S, Korgaonkar C, Ascoli M 1999 Role of the rate of internalization of the agonist-receptor complex on the agonist-induced down-regulation of the lutropin/choriogonadotropin receptor. Mol Endocrinol 13:1295-1304
32. Nakamura K, Liu X, Ascoli M 1999 The rate of internalization of the gonadotropin receptors is greatly affected by the origin of the extracellular domain. J Biol Chem 274:25426-25432
33. Nakamura K, Ascoli M 1999 A dileucine-based motif in the C-terminal tail of the lutropin/choriogonadotropin receptor inhibits endocytosis of the agonist-receptor complex. Mol Pharmacol 56:728-736
34. Nakamura K, Liu X, Ascoli M 2000 Seven non-contiguous intracellular residues of the lutropin/choriogonadotropin receptor dictate the rate of agonist-induced internalization and its sensitivity to non-visual arrestins. J Biol Chem 275:241-247
35. Kishi M, Ascoli M 2000 The C-terminal tail of the rat lutropin/choriogonadotropin receptor independently modulates hCG-induced internalization of the cell surface receptor and the lysosomal targeting of the internalized hCG-receptor complex. Mol Endocrinol 14:926-936
36. Ghinea N, Vuhai MT, Groyer-Picard M-T, Houllier A, Schoëvaërt D, Milgrom E 1992 Pathways of internalization of the hCG/LH receptor: immunoelectron micro-scopic studies in Leydig cells and transfected L cells. J Cell Biol 118:1347-1358
37. Baratti-Elbaz C, Chinea N, Lahuna O, Loosfelt H, Pichon C, Milgrom E 1999 Internalization and recycling pathways of the thyrotropin receptor. Mol Endocrinol 13:1751-1765
38. Graeve L, Drickamer K, Rodriguez-Boulan E 1989 Polarized endocytosis by Madin-Darby canine kidney cells transfected with functional chicken liver glycoprotein receptor. J Cell Biol 109:2809-2816
39. Gage RM, Kim K-A, Cao TT, von Zastrow M 2001 A transplantable sorting signal that is sufficient to mediate rapid recycling of G protein-coupled receptors. J Biol Chem 276:44712-44720
40. Tanowitz M, von Zastrow M 2003 A novel endocytic recycling signal that distinguishes the membrane trafficking of naturally occurring opioid receptors. J Biol Chem 278:45978-45986
41. Ascoli M, Puett D 1978 Inhibition of the degradation of receptor-bound human choriogonadotropin by lysosomotropic agents, protease inhibitors, and metabolic inhibitors. J Biol Chem 253:7832-7838
42. Paasche JD, Attramadal T, Kristiansen K, Oksvold MP, Johansen HK, Huitfeldt HS, Dahl SG, Attramadal H 2005 Subtype-specific sorting of the ETA endothelin receptor by a novel endocytic recycling signal for G protein-coupled receptors. Mol Pharmacol 67:1581-1590
43. Gaborik Z, Hunyady L 2004 Intracellular trafficking of hormone receptors. Trends Endocrinol Metab 15:286-293
44. Quintana J, Wang H, Ascoli M 1993 The regulation of the binding affinity of the luteinizing hormone/choriogonadotropin receptor by sodium ions is mediated by a highly conserved aspartate located in the second transmembrane domain of G protein-coupled receptors. Mol Endocrinol 7:767-775
45. Costagliola S, Urizar E, Mendive F, Vassart G 2005 Specificity and promiscuity of gonadotropin receptors. Reproduction 130:275-281
46. Fabritz J, Ryan S, Ascoli M 1998 Transfected cells express mostly the intracellular precursor of the lutropin/ choriogonadotropin receptor but this precursor binds choriogonadotropin with high affinity. Biochemistry 37:664-672
47. Chen C, Okayama H 1987 High-efficiency transformation of mammalian cells by plasmid DNA. Mol Cell Biol 7:2745-2752
48. Ascoli M 1982 Internalization and degradation of receptor-bound human choriogonadotropin in Leydig tumor cells. Fate of the hormone subunits. J Biol Chem 257:13306-13311
49. Quintana J, Hipkin RW, Ascoli M 1993 A polyclonal antibody to a synthetic peptide derived from the rat FSH receptor reveals the recombinant receptor as a 74 kDa protein. Endocrinology 133:2098-2104
50. Sheff DR, Daro EA, Hull M, Mellman I 1999 The receptor recycling pathway contains two distinct populations of early endosomes with different sorting functions. J Cell Biol 145:123-139
51. Margolskee R, McHenry-Rinde B, Horn R 1993 Panning transfected cells for electrophysiological studies. Biotechniques 15:906-911
52. Ascoli M, Puett D 1978 Gonadotropin binding and stimulation of steroidogenesis in Leydig tumor cells. Proc Natl Acad Sci USA 75:99-102