Rescue of defective G protein - Coupled receptor function in vivo by intermolecular cooperation

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 5, 2010, Pages 2319-2324

  Rivero Müller, Adolfo ^a   Chou, Yen Yin ^b,c   Ji, Inhae ^d   Lajic, Svetlana ^b   Hanyaloglu, Aylin C ^b   Jonas, Kim ^b   Rahman, Nafis ^a   Ji, Tae H ^d   Huhtaniemi, Ilpo ^a,b  

^a UNIVERSITY OF TURKU   (Finland)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^d UNIVERSITY OF KENTUCKY   (United States)

Author keywords

di oligomerization; Fertility; Luteinizing hormone receptor; Testis; Transgenic mice

Indexed keywords

G PROTEIN COUPLED RECEPTOR; LUTEINIZING HORMONE RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CONTROLLED STUDY; HUMAN; HUMAN CELL; INTERNALIZATION; MOUSE; NONHUMAN; OLIGOMERIZATION; PHENOTYPE; PRIORITY JOURNAL; TRANSGENIC MOUSE;

ANIMALS; CELL LINE; CHORIONIC GONADOTROPIN; GENETIC COMPLEMENTATION TEST; HUMANS; MALE; MICE; MICE, KNOCKOUT; MICE, MUTANT STRAINS; MICE, TRANSGENIC; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MUTATION; PHENOTYPE; PROTEIN BINDING; PROTEIN MULTIMERIZATION; RECEPTORS, G-PROTEIN-COUPLED; RECEPTORS, LH; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; TESTIS;

MUS MUSCULUS;

EID: 76649114492     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0906695106     Document Type: Article

References (48)

1. Drews J (2000) Drug discovery: a historical perspective. Science 287:1960-1964.
2. Bulenger S, Marullo S, Bouvier M (2005) Emerging role of homo- and heterodimerization in G-protein-coupled receptor biosynthesis and maturation. Trends Pharmacol Sci 26:131-137.
3. Pin JP, et al. (2004) The activation mechanism of class-C G-protein coupled receptors. Biol Cell 96:335-342.
4. Kaupmann K, et al. (1998) GABA(B)-receptor subtypes assemble into functional heteromeric complexes. Nature 396:683-687.
5. Whorton MR, et al. (2007) A monomeric G protein-coupled receptor isolated in a high-density lipoprotein particle efficiently activates its G protein. Proc Natl Acad Sci USA 104:7682-7687.
6. Margeta-Mitrovic M, Jan YN, Jan LY (2000) A trafficking checkpoint controls GABA(B) receptor heterodimerization. Neuron 27:97-106.
7. Salahpour A, et al. (2004) Homodimerization of the beta2-adrenergic receptor as a prerequisite for cell surface targeting. J Biol Chem 279:33390-33397.
8. GuanR, etal. (2009) Bioluminescence resonance energytransfer studies reveal constitutive dimerization of the human lutropin receptor and a lack of correlation between receptor activation and the propensity for dimerization. J Biol Chem284:7483-7494.
9. Pin JP, Galvez T, Prézeau L (2003) Evolution, structure, and activation mechanism of family 3/C G-protein-coupled receptors. Pharmacol Ther 98:325-354.
10. Thomas RM, et al. (2007) Follice-stimulating hormone receptor forms oligomers and shows evidence of carboxyl-terminal proteolytic processing. Endocrinology 148: 1987-1995.
11. Jordan BA, Trapaidze N, Gomes I, Nivarthi R, Devi LA (2001) Oligomerization of opioid receptors with beta 2-adrenergic receptors: a role in trafficking and mitogena-ctivated protein kinase activation. Proc Natl Acad Sci USA 98:343-348.
12. Terrillon S, Bouvier M (2004) Roles of G-protein-coupled receptor dimerization. EMBO Rep 5:30-34.
13. El-Asmar L, et al. (2005) Evidence for negative binding cooperativity within CCR5-CCR2b heterodimers. Mol Pharmacol 67:460-469.
14. Urizar E, et al. (2005) Glycoprotein hormone receptors: link between receptor homodimerization and negative cooperativity. EMBO J 24:1954-1964.
15. Lee C, Ji IJ, Ji TH (2002) Use of defined-function mutants to access receptor-receptor interactions. Methods 27:318-323.
16. Monnot C, et al. (1996) Polar residues in the transmembrane domains of the type 1 angiotensin II receptor are required for binding and coupling. Reconstitution of the binding site by co-expression of two deficient mutants. J Biol Chem 271:1507-1513.
17. Costagliola S, Urizar E, Mendive F, Vassart G (2005) Specificity and promiscuity of gonadotropin receptors. Reproduction 130:275-281.
18. Ray K, Hauschild BC (2000) Cys-140 is critical for metabotropic glutamate receptor-1 dimerization. J Biol Chem 275:34245-34251.
19. Bazarsuren A, et al. (2002) In vitro folding, functional characterization, and disulfide pattern of the extracellular domain of human GLP-1 receptor. Biophys Chem 96:305-318.
20. Giguére V, Gallant MA, de Brum-Fernandes AJ, Parent JL (2004) Role of extracellular cysteine residues in dimerization/oligomerization of the human prostacyclin receptor. Eur J Pharmacol 494:11-22.
21. Kunishima N, et al. (2000) Structural basis of glutamate recognition by a dimeric metabotropic glutamate receptor. Nature 407:971-977.
22. Romano C, Yang WL, O'Malley KL (1996) Metabotropic glutamate receptor 5 is a disulfide-linked dimer. J Biol Chem 271:28612-28616.
23. Kroeger KM, Pfleger KD, Eidne KA (2003) G-protein coupled receptor oligomerization in neuroendocrine pathways. Front Neuroendocrinol 24:254-278.
24. Romano C, et al. (2001) Covalent and noncovalent interactions mediate metabotropic glutamate receptor mGlu5 dimerization. Mol Pharmacol 59:46-53.
25. Fonseca JM, Lambert NA (2009) Instability of a class a G protein-coupled receptor oligomer interface. Mol Pharmacol 75:1296-1299.
26. James JR, Oliveira MI, Carmo AM, Iaboni A, Davis SJ (2006) A rigorous experimental framework for detecting protein oligomerization using bioluminescence resonance energy transfer. Nat Methods 3:1001-1006.
27. Bouvier M, Heveker N, Jockers R, Marullo S, Milligan G (2007) BRET analysis of GPCR oligomerization: newer does not mean better. Nat Methods 4:3-4, author reply 4.
28. Salahpour A, Masri B (2007) Experimental challenge to a 'rigorous' BRET analysis of GPCR oligomerization. Nat Methods 4:599-600, author reply 601.
29. Gurevich VV, Gurevich EV (2008) GPCR monomers and oligomers: it takes all kinds. Trends Neurosci 31:74-81.
30. Parnot C, Kobilka B (2004) Toward understanding GPCR dimers. Nat Struct Mol Biol 11: 691-692.
31. Kniazeff J, et al. (2004) Closed state of both binding domains of homodimeric mGlu receptors is required for full activity. Nat Struct Mol Biol 11:706-713.
32. Jeoung M, Lee C, Ji I, Ji TH (2007) Trans-activation, cis-activation and signal selection of gonadotropin receptors. Mol Cell Endocrinol 260-262:137-143.
33. Ji I, Lee C, Song Y, Conn PM, Ji TH (2002) Cis- and trans-activation of hormone receptors: the LH receptor. Mol Endocrinol 16:1299-1308.
34. Ng GY, et al. (1996) Dopamine D2 receptor dimers and receptor-blocking peptides. Biochem Biophys Res Commun 227:200-204.
35. Lee C, et al. (2002) Two defective heterozygous luteinizing hormone receptors can rescue hormone action. J Biol Chem 277:15795-15800.
36. Ji I, et al. (2004) Trans-activation of mutant follicle-stimulating hormone receptors selectively generates only one of two hormone signals. Mol Endocrinol 18:968-978.
37. Sangkuhl K, Schulz A, Schultz G, Schöneberg T (2002) Structural requirements for mutational lutropin/choriogonadotropin receptor activation. J Biol Chem 277: 47748-47755.
38. Huhtaniemi IT, Themmen APN (2000) Mutations of gonadotropins and gonadotropin receptors: elucidating the physiology and pathophysiology of pituitary-gonadal function. Endocr Rev 21:551-583.
39. Zhang FP, Poutanen M, Wilbertz J, Huhtaniemi I (2001) Normal prenatal but arrested postnatal sexual development of luteinizing hormone receptor knockout (LuRKO) mice. Mol Endocrinol 15:172-183.
40. Lei ZM, Rao CV, Kornyei JL, Licht P, Hiatt ES (1993) Novel expression of human chorionic gonadotropin/luteinizinghormonereceptorgeneinbrain. Endocrinology 132:2262-2270.
41. Ahtiainen P, et al. (2007) Phenotypic characterisation of mice with exaggerated and missing LH/hCG action. Mol Cell Endocrinol 260-262:255-263.
42. Huhtaniemi I, et al. (2006) Genetically modified mouse models in studies of luteinising hormone action. Mol Cell Endocrinol 252:126-135.
43. Wu C, Narayan P, Puett D (1996) Protein engineering of a novel constitutively active hormone-receptor complex. J Biol Chem 271:31638-31642.
44. Kanda M, et al. (1999) Genetic fusion of an alpha-subunit gene to the follicle-stimulating hormone and chorionic gonadotropin-beta subunit genes: production of a bifunctional protein. Mol Endocrinol 13:1873-1881.
45. Xing Y, et al. (2001) Alternatively folded choriogonadotropin analogs. Implications for hormone folding and biological activity. J Biol Chem 276:46953-46960.
46. Lee C, Ji I, Ji TH (2004) Distinctmechanisms of cAMP induction by constitutively activating LH receptor and wild-type LH receptor activated by hCG. Endocrine 25:111-115.
47. Catt KJ, Dufau ML (1973) Spare gonadotrophin receptors in rat testis. Nat New Biol 244:219-221.
48. Zhang Y, Buchholz F, Muyrers JP, Stewart AF (1998) A new logic for DNA engineering using recombination in Escherichia coli. Nat Genet 20:123-128.