Preferential β-arrestin signalling at low receptor density revealed by functional characterization of the human FSH receptor A189 V mutation

Molecular and Cellular Endocrinology

Volumn 331, Issue 1, 2011, Pages 109-118

  Tranchant, Thibaud ^a,b,c,d,f   Durand, Guillaume ^a,b,c,d   Gauthier, Christophe ^a,b,c,d   Crépieux, Pascale ^a,b,c,d   Ulloa Aguirre, Alfredo ^a,b,c,d,e   Royère, Dominique ^a,b,c,d,f   Reiter, Eric ^a,b,c,d  

^a UMR85 PHYSIOLOGIE DE LA REPRODUCTION ET DES COMPORTEMENTS   (France)

^b CNRS   (France)

^c UNIVERSITÉ DE TOURS   (France)

^d Haras Nationaux   (France)

^e Le Studium   (France)

^f UNIVERSITY HOSPITAL OF TOURS   (France)

Author keywords

Arrestin; A189 V mutation; FSH; FSH receptor; Selective signalling

Indexed keywords

BETA ARRESTIN; CYCLIC AMP DEPENDENT PROTEIN KINASE; FOLLITROPIN RECEPTOR; RECOMBINANT FOLLITROPIN; SMALL INTERFERING RNA;

ARTICLE; CELL COUNT; CELL MEMBRANE; CONTROLLED STUDY; HUMAN; HUMAN CELL; MUTATION; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

AMINO ACID SUBSTITUTION; ANIMALS; ARRESTINS; CELL MEMBRANE; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; FOLLICLE STIMULATING HORMONE; HEK293 CELLS; HUMANS; KINETICS; MALE; MUTANT PROTEINS; MUTATION; PHOSPHORYLATION; RECEPTORS, FSH; SIGNAL TRANSDUCTION; SWINE; TRANSFECTION;

EID: 78149416205     PISSN: 03037207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mce.2010.08.016     Document Type: Article

References (43)

1. Aittomaki K., Lucena J.L., Pakarinen P., Sistonen P., Tapanainen J., Gromoll J., Kaskikari R., Sankila E.M., Lehvaslaiho H., Engel A.R., Nieschlag E., Huhtaniemi I., de la Chapelle A. Mutation in the follicle-stimulating hormone receptor gene causes hereditary hypergonadotropic ovarian failure. Cell 1995, 82(6):959-968.
2. Allen M.D, Zhang J. Subcellular dynamics of protein kinase A activity visualized by FRET-based reporters. Biochem. Biophys. Res. Commun. 2006, 348(2):716-721.
3. Azzi M., Charest P.G., Angers S., Rousseau G., Kohout T., Bouvier M., Pineyro G. Beta-arrestin-mediated activation of MAPK by inverse agonists reveals distinct active conformations for G protein-coupled receptors. Proc. Natl. Acad. Sci. U.S.A. 2003, 100(20):11406-11411.
4. Crepieux P., Marion S., Martinat N., Fafeur V., Vern Y.L., Kerboeuf D., Guillou F., Reiter E. The ERK-dependent signalling is stage-specifically modulated by FSH, during primary Sertoli cell maturation. Oncogene 2001, 20(34):4696-4709.
5. DeFea K.A, Zalevsky J., Thoma M.S., Dery O., Mullins R.D., Bunnett N.W. beta-Arrestin-dependent endocytosis of proteinase-activated receptor 2 is required for intracellular targeting of activated ERK1/2. J. Cell Biol. 2000, 148(6):1267-1281.
6. DeFea K.A., Vaughn Z.D., O'Bryan E.M., Nishijima D., Dery O., Bunnett N.W. The proliferative and antiapoptotic effects of substance P are facilitated by formation of a beta-arrestin-dependent scaffolding complex. Proc. Natl. Acad. Sci. U.S.A. 2000, 97(20):11086-11091.
7. Dierich A., Sairam M.R., Monaco L., Fimia G.M., Gansmuller A., LeMeur M., Sassone-Corsi P. Impairing follicle-stimulating hormone (FSH) signaling in vivo: targeted disruption of the FSH receptor leads to aberrant gametogenesis and hormonal imbalance. Proc. Natl. Acad. Sci. U.S.A. 1998, 95(23):13612-13617.
8. DiPilato L.M., Cheng X., Zhang J. Fluorescent indicators of cAMP and Epac activation reveal differential dynamics of cAMP signaling within discrete subcellular compartments. Proc. Natl. Acad. Sci. U.S.A. 2004, 101(47):16513-16518.
9. Drake M.T., Violin J.D., Whalen E.J., Wisler J.W., Shenoy S.K., Lefkowitz R.J. beta-Arrestin-biased agonism at the beta2-adrenergic receptor. J. Biol. Chem. 2008, 283(9):5669-5676.
10. Gesty-Palmer D., Chen M., Reiter E., Ahn S., Nelson C.D., Wang S., Eckhardt A.E., Cowan C.L., Spurney R.F., Luttrell L.M., Lefkowitz R.J. Distinct beta-arrestin- and G protein-dependent pathways for parathyroid hormone receptor-stimulated ERK1/2 activation. J. Biol. Chem. 2006, 281(16):10856-10864.
11. Gesty-Palmer D., Flannery P., Yuan L., Corsino L., Spurney R., Lefkowitz R.J., Luttrell L.M. A beta-arrestin-biased agonist of the parathyroid hormone receptor (PTH1R) promotes bone formation independent of G protein activation. Sci. Transl. Med. 2009, 1(1). ra1.
12. Ghadami M., Salama S.A., Khatoon N., Chilvers R., Nagamani M., Chedrese P.J., Al-Hendy A. Toward gene therapy of primary ovarian failure: adenovirus expressing human FSH receptor corrects the Finnish C566T mutation. Mol. Hum. Reprod. 2008, 14(1):9-15.
13. Huhtaniemi I. Mutations along the pituitary-gonadal axis affecting sexual maturation: novel information from transgenic and knockout mice. Mol. Cell. Endocrinol. 2006, 254-255:84-90.
14. Janovick J.A., Maya-Nunez G., Ulloa-Aguirre A., Huhtaniemi I.T., Dias J.A., Verbost P., Conn P.M. Increased plasma membrane expression of human follicle-stimulating hormone receptor by a small molecule thienopyr(im)idine. Mol. Cell. Endocrinol. 2009, 298(1-2):84-88.
15. Kara E., Crepieux P., Gauthier C., Martinat N., Piketty V., Guillou F., Reiter E. A phosphorylation cluster of five serine and threonine residues in the C-terminus of the follicle-stimulating hormone receptor is important for desensitization but not for beta-arrestin-mediated ERK activation. Mol. Endocrinol. 2006, 20(11):3014-3026.
16. Krishnamurthy H., Danilovich N., Morales C.R., Sairam M.R. Qualitative and quantitative decline in spermatogenesis of the follicle-stimulating hormone receptor knockout (FORKO) mouse. Biol. Reprod. 2000, 62(5):1146-1159.
17. Kumar T.R., Wang Y., Lu N., Matzuk M.M. Follicle stimulating hormone is required for ovarian follicle maturation but not male fertility. Nat. Genet. 1997, 15(2):201-204.
18. Layman L.C., Lee E.J., Peak D.B., Namnoum A.B., Vu K.V., van Lingen B.L., Gray M.R., McDonough P.G., Reindollar R.H., Jameson J.L. Delayed puberty and hypogonadism caused by mutations in the follicle-stimulating hormone beta-subunit gene. N. Engl. J. Med. 1997, 337(9):607-611.
19. Layman L.C., Porto A.L., Xie J., da Motta A., da Motta L.D., Weiser W., Sluss P.M. FSH beta gene mutations in a female with partial breast development and a male sibling with normal puberty and azoospermia. J. Clin. Endocrinol. Metab. 2002, 87(8):3702-3707.
20. Lazari M.F., Liu X., Nakamura K., Benovic J.L., Ascoli M. Role of G protein-coupled receptor kinases on the agonist-induced phosphorylation and internalization of the follitropin receptor. Mol. Endocrinol. 1999, 13(6):866-878.
21. Lindstedt G., Nystrom E., Matthews C., Ernest I., Janson P.O., Chatterjee K. Follitropin (FSH) deficiency in an infertile male due to FSHbeta gene mutation A syndrome of normal puberty and virilization but underdeveloped testicles with azoospermia, low FSH but high lutropin and normal serum testosterone concentrations. Clin. Chem. Lab. Med. 1998, 36(8):663-665.
22. Luttrell L.M., Ferguson S.S., Daaka Y., Miller W.E., Maudsley S., Della Rocca G.J., Lin F., Kawakatsu H., Owada K., Luttrell D.K., Caron M.G., Lefkowitz R.J. Beta-arrestin-dependent formation of beta2 adrenergic receptor-Src protein kinase complexes. Science 1999, 283(5402):655-661.
23. Luttrell L.M., Roudabush F.L., Choy E.W., Miller W.E., Field M.E., Pierce K.L., Lefkowitz R.J. Activation and targeting of extracellular signal-regulated kinases by beta-arrestin scaffolds. Proc. Natl. Acad. Sci. U.S.A. 2001, 98(5):2449-2454.
24. Matthews C.H., Borgato S., Beck-Peccoz P., Adams M., Tone Y., Gambino G., Casagrande S., Tedeschini G., Benedetti A., Chatterjee V.K. Primary amenorrhoea and infertility due to a mutation in the beta-subunit of follicle-stimulating hormone. Nat. Genet. 1993, 5(1):83-86.
25. McNatty K.P., Lun S., Heath D.A., Hudson N.L., O'Keeffe L.E., Henderson K.M. Binding characteristics of 125I-labelled human FSH to granulosa cells from Booroola ewes which were homozygous, heterozygous or non-carriers of a major gene(s) influencing their ovulation rate. J. Reprod. Fertil. 1989, 86(1):27-38.
26. Musnier A., Heitzler D., Boulo T., Tesseraud S., Durand G., Lecureuil C., Guillou H., Poupon A., Reiter E., Crepieux P. Developmental regulation of p70 S6 kinase by a G protein-coupled receptor dynamically modelized in primary cells. Cell. Mol. Life Sci. 2009, 66(21):3487-3503.
27. Neer E.J. Heterotrimeric G proteins: organizers of transmembrane signals. Cell 1995, 80(2):249-257.
28. Phillip M., Arbelle J.E., Segev Y., Parvari R. Male hypogonadism due to a mutation in the gene for the beta-subunit of follicle-stimulating hormone. N. Engl. J. Med. 1998, 338(24):1729-1732.
29. Premont R.T., Gainetdinov R.R. Physiological roles of G protein-coupled receptor kinases and arrestins. Annu. Rev. Physiol. 2007, 69:511-534.
30. Rannikko A., Pakarinen P., Manna P.R., Beau I., Misrahi M., Aittomaki K., Huhtaniemi I. Functional characterization of the human FSH receptor with an inactivating Ala189Val mutation. Mol. Hum. Reprod. 2002, 8(4):311-317.
31. Reiter E., Lefkowitz R.J. GRKs and beta-arrestins: roles in receptor silencing, trafficking and signaling. Trends Endocrinol. Metab. 2006, 17(4):159-165.
32. Reiter E., Marion S., Robert F., Troispoux C., Boulay F., Guillou F., Crepieux P. Kinase-inactive G-protein-coupled receptor kinases are able to attenuate follicle-stimulating hormone-induced signaling. Biochem. Biophys. Res. Commun. 2001, 282(1):71-78.
33. Shenoy S.K., Drake M.T., Nelson C.D., Houtz D.A., Xiao K., Madabushi S., Reiter E., Premont R.T., Lichtarge O., Lefkowitz R.J. beta-Arrestin-dependent G protein-independent ERK1/2 activation by the beta2 adrenergic receptor. J. Biol. Chem. 2006, 281(2):1261-1273.
34. Simoni M., Gromoll J., Nieschlag E. The follicle-stimulating hormone receptor: biochemistry, molecular biology, physiology, and pathophysiology. Endocr. Rev. 1997, 18(6):739-773.
35. Tapanainen J.S., Aittomaki K., Min J., Vaskivuo T., Huhtaniemi I.T. Men homozygous for an inactivating mutation of the follicle-stimulating hormone (FSH) receptor gene present variable suppression of spermatogenesis and fertility. Nat. Genet. 1997, 15(2):205-206.
36. Tena-Sempere M., Manna P.R., Huhtaniemi I. Molecular cloning of the mouse follicle-stimulating hormone receptor complementary deoxyribonucleic acid: functional expression of alternatively spliced variants and receptor inactivation by a C566T transition in exon 7 of the coding sequence. Biol. Reprod. 1999, 60(6):1515-1527.
37. Troispoux C., Guillou F., Elalouf J.M., Firsov D., Iacovelli L., De Blasi A., Combarnous Y., Reiter E. Involvement of G protein-coupled receptor kinases and arrestins in desensitization to follicle-stimulating hormone action. Mol. Endocrinol. 1999, 13(9):1599-1614.
38. Violin J.D., Lefkowitz R.J. Beta-arrestin-biased ligands at seven-transmembrane receptors. Trends Pharmacol. Sci. 2007, 28(8):416-422.
39. Wehbi V., Tranchant T., Durand G., Musnier A., Decourtye J., Piketty V., Butnev V.Y., Bousfield G.R., Crepieux P., Maurel M.C., Reiter E. Partially deglycosylated equine LH preferentially activates beta-arrestin-dependent signaling at the follicle-stimulating hormone receptor. Mol. Endocrinol. 2010, 24(3):561-573.
40. Wehbi V., Decourtye J., Piketty V., Durand G., Reiter E., Maurel M.C. Selective modulation of follicle-stimulating hormone signaling pathways with enhancing equine chorionic gonadotropin/antibody immune complexes. Endocrinology 2010, 151(6):2788-2799.
41. Wei H., Ahn S., Shenoy S.K., Karnik S.S., Hunyady L., Luttrell L.M., Lefkowitz R.J. Independent beta-arrestin 2 and G protein-mediated pathways for angiotensin II activation of extracellular signal-regulated kinases 1 and 2. Proc. Natl. Acad. Sci. U.S.A. 2003, 100(19):10782-10787.
42. Wisler J.W., DeWire S.M., Whalen E.J., Violin J.D., Drake M.T., Ahn S., Shenoy S.K., Lefkowitz R.J. A unique mechanism of beta-blocker action: carvedilol stimulates beta-arrestin signaling. Proc. Natl. Acad. Sci. U.S.A. 2007, 104(42):16657-16662.
43. Zhang J., Ma Y., Taylor S.S., Tsien R.Y. Genetically encoded reporters of protein kinase A activity reveal impact of substrate tethering. Proc. Natl. Acad. Sci. U.S.A. 2001, 98(26):14997-15002.