تقرير
A single-domain intrabody targeting the follicle-stimulating hormone receptor impacts FSH-induced G protein-dependent signalling.
العنوان: | A single-domain intrabody targeting the follicle-stimulating hormone receptor impacts FSH-induced G protein-dependent signalling. |
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المؤلفون: | Raynaud P; Physiologie de la Reproduction et des Comportements (PRC), Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement (INRAE), Centre National de la Recherche Scientifique (CNRS), Institut Français du Cheval et de l'Equitation (IFCE), Université de Tours, Nouzilly, France., Jugnarain V; Physiologie de la Reproduction et des Comportements (PRC), Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement (INRAE), Centre National de la Recherche Scientifique (CNRS), Institut Français du Cheval et de l'Equitation (IFCE), Université de Tours, Nouzilly, France., Vaugrente O; Physiologie de la Reproduction et des Comportements (PRC), Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement (INRAE), Centre National de la Recherche Scientifique (CNRS), Institut Français du Cheval et de l'Equitation (IFCE), Université de Tours, Nouzilly, France., Vallet A; Physiologie de la Reproduction et des Comportements (PRC), Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement (INRAE), Centre National de la Recherche Scientifique (CNRS), Institut Français du Cheval et de l'Equitation (IFCE), Université de Tours, Nouzilly, France., Boulo T; Physiologie de la Reproduction et des Comportements (PRC), Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement (INRAE), Centre National de la Recherche Scientifique (CNRS), Institut Français du Cheval et de l'Equitation (IFCE), Université de Tours, Nouzilly, France., Gauthier C; Physiologie de la Reproduction et des Comportements (PRC), Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement (INRAE), Centre National de la Recherche Scientifique (CNRS), Institut Français du Cheval et de l'Equitation (IFCE), Université de Tours, Nouzilly, France., Inoue A; Graduate School of Pharmaceutical Sciences, Tohoku University, Sendai, Japan., Sibille N; Centre de Biologie Structurale (CBS), CNRS, University Montpellier, Inserm, France., Gauthier C; Physiologie de la Reproduction et des Comportements (PRC), Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement (INRAE), Centre National de la Recherche Scientifique (CNRS), Institut Français du Cheval et de l'Equitation (IFCE), Université de Tours, Nouzilly, France., Jean-Alphonse F; Physiologie de la Reproduction et des Comportements (PRC), Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement (INRAE), Centre National de la Recherche Scientifique (CNRS), Institut Français du Cheval et de l'Equitation (IFCE), Université de Tours, Nouzilly, France.; Inria, Inria Saclay-Ile-de-France, Palaiseau, France., Reiter E; Physiologie de la Reproduction et des Comportements (PRC), Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement (INRAE), Centre National de la Recherche Scientifique (CNRS), Institut Français du Cheval et de l'Equitation (IFCE), Université de Tours, Nouzilly, France.; Inria, Inria Saclay-Ile-de-France, Palaiseau, France., Crépieux P; Physiologie de la Reproduction et des Comportements (PRC), Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement (INRAE), Centre National de la Recherche Scientifique (CNRS), Institut Français du Cheval et de l'Equitation (IFCE), Université de Tours, Nouzilly, France.; Inria, Inria Saclay-Ile-de-France, Palaiseau, France., Bruneau G; Physiologie de la Reproduction et des Comportements (PRC), Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement (INRAE), Centre National de la Recherche Scientifique (CNRS), Institut Français du Cheval et de l'Equitation (IFCE), Université de Tours, Nouzilly, France. |
المصدر: | FEBS letters [FEBS Lett] 2024 Jan; Vol. 598 (2), pp. 220-232. Date of Electronic Publication: 2023 Nov 03. |
نوع المنشور: | Letter; Research Support, Non-U.S. Gov't; Comment |
اللغة: | English |
بيانات الدورية: | Publisher: John Wiley & Sons Ltd Country of Publication: England NLM ID: 0155157 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1873-3468 (Electronic) Linking ISSN: 00145793 NLM ISO Abbreviation: FEBS Lett Subsets: MEDLINE |
أسماء مطبوعة: | Publication: Jan. 2016- : West Sussex : John Wiley & Sons Ltd. Original Publication: Amsterdam, North-Holland on behalf of the Federation of European Biochemical Societies. |
مواضيع طبية MeSH: | Receptors, FSH*/genetics , Receptors, FSH*/chemistry , Receptors, FSH*/metabolism , Follicle Stimulating Hormone*/chemistry , Follicle Stimulating Hormone*/metabolism , Follicle Stimulating Hormone*/pharmacology, GTP-Binding Proteins/metabolism ; Signal Transduction |
مستخلص: | Intracellular variable fragments of heavy-chain antibody from camelids (intra-VHH) have been successfully used as chaperones to solve the 3D structure of active G protein-coupled receptors bound to their transducers. However, their effect on signalling has been poorly explored, although they may provide a better understanding of the relationships between receptor conformation and activity. Here, we isolated and characterized iPRC1, the first intra-VHH recognizing a member of the large glycoprotein hormone receptor family, the follicle-stimulating hormone receptor (FSHR). This intra-VHH recognizes the FSHR third intracellular loop and decreases cAMP production in response to FSH, without altering Gαs recruitment. Hence, iPRC1 behaves as an allosteric modulator and provides a new tool to complete structure/activity studies performed thus far on this receptor. (© 2023 The Authors. FEBS Letters published by John Wiley & Sons Ltd on behalf of Federation of European Biochemical Societies.) |
التعليقات: | Comment on: Front Endocrinol (Lausanne). 2022 Nov 16;13:1048601. (PMID: 36465650) |
References: | Latorraca NR, Venkatakrishnan AJ and Dror RO (2017) GPCR dynamics: structures in motion. Chem Rev 117, 139-155. De Pascali F, Ayoub MA, Benevelli R, Sposini S, Lehoux J, Gallay N, Raynaud P, Landomiel F, Jean-Alphonse F, Gauthier C et al. (2021) Pharmacological characterization of low molecular weight biased agonists at the follicle stimulating hormone receptor. Int J Mol Sci 22, 9850. Stijlemans B, Conrath K, Cortez-Retamozo V, Van Xong H, Wyns L, Senter P, Revets H, De Baetselier P, Muyldermans S and Magez S (2004) Efficient targeting of conserved cryptic epitopes of infectious agents by single domain antibodies. J Biol Chem 279, 1256-1261. Liu H, Schittny V and Nash MA (2019) Removal of a conserved disulfide bond does not compromise mechanical stability of a VHH antibody complex. Nano Lett 19, 5524-5529. Manglik A and Kobilka B (2014) The role of protein dynamics in GPCR function: insights from the β2AR and rhodopsin. Curr Opin Cell Biol 27, 136-143. Rasmussen SGF, Choi HJ, Fung JJ, Pardon E, Casarosa P, Chae PS, DeVree BT, Rosenbaum DM, Thian FS, Kobilka TS et al. (2011) Structure of a nanobody-stabilized active state of the β2 adrenoceptor. Nature 469, 175-180. Kruse AC, Ring AM, Manglik A, Hu J, Hu K, Eitel K, Hübner H, Pardon E, Valant C, Sexton PM et al. (2013) Activation and allosteric modulation of a muscarinic acetylcholine receptor. Nature 504, 101-106. Huang W, Manglik A, Venkatakrishnan AJ, Laeremans T, Feinberg EN, Sanborn AL, Kato HE, Livingston KE, Thorsen TS, Kling RC et al. (2015) Structural insights into μ-opioid receptor activation. Nature 524, 315-321. Masureel M, Zou Y, Picard LP, van der Westhuizen E, Mahoney JP, Rodrigues JPGLM, Mildorf TJ, Dror RO, Shaw DE, Bouvier M et al. (2018) Structural insights into binding specificity, efficacy and bias of a β2AR partial agonist. Nat Chem Biol 14, 1059-1066. Staus DP, Strachan RT, Manglik A, Pani B, Kahsai AW, Kim TH, Wingler LM, Ahn S, Chatterjee A, Masoudi A et al. (2016) Allosteric nanobodies reveal the dynamic range and diverse mechanisms of G protein-coupled receptor activation. Nature 535, 448-452. Irannejad R, Tomshine JC, Tomshine JR, Chevalier M, Mahoney JP, Steyaert J, Rasmussen SGF, Sunahara RK, el-Samad H, Huang B et al. (2013) Conformational biosensors reveal GPCR signalling from endosomes. Nature 495, 534-538. Raynaud P, Gauthier C, Jugnarain V, Jean-Alphonse F, Reiter E, Bruneau G and Crépieux P (2022) Intracellular VHHs to monitor and modulate GPCR signaling. Front Endocrinol 13, 1048601. Staus DP, Wingler LM, Strachan RT, Rasmussen SGF, Pardon E, Ahn S, Steyaert J, Kobilka BK and Lefkowitz RJ (2014) Regulation of β2-adrenergic receptor function by Conformationally selective single-domain Intrabodies. Mol Pharmacol 85, 472-481. McMahon C, Baier AS, Pascolutti R, Wegrecki M, Zheng S, Ong JX, Erlandson SC, Hilger D, Rasmussen SGF, Ring AM et al. (2018) Yeast surface display platform for rapid discovery of conformationally selective nanobodies. Nat Struct Mol Biol 25, 289-296. Gromoll J, Simoni M, Nordhoff V, Behre HM, De Geyter C and Nieschlag E (1996) Functional and clinical consequences of mutations in the FSH receptor. Mol Cell Endocrinol 125, 177-182. Duan J, Xu P, Zhang H, Luan X, Yang J, He X, Mao C, Shen DD, Ji Y, Cheng X et al. (2023) Mechanism of hormone and allosteric agonist mediated activation of follicle stimulating hormone receptor. Nat Commun 14, 519. Marion S, Robert F, Crepieux P, Martinat N, Troispoux C, Guillou F and Reiter E (2002) G protein-coupled receptor kinases and Beta Arrestins are Relocalized and attenuate cyclic 3′,5′-adenosine monophosphate response to follicle-stimulating hormone in rat primary Sertoli cells. Biol Reprod 66, 70-76. Marion S, Kara E, Crepieux P, Piketty V, Martinat N, Guillou F and Reiter E (2006) G protein-coupled receptor kinase 2 and β-arrestins are recruited to FSH receptor in stimulated rat primary Sertoli cells. J Endocrinol 190, 341-350. Reiter E and Lefkowitz RJ (2006) GRKs and beta-arrestins: roles in receptor silencing, trafficking and signaling. Trends Endocrinol Metab 17, 159-165. Sposini S, Jean-Alphonse FG, Ayoub MA, Oqua A, West C, Lavery S, Brosens JJ, Reiter E and Hanyaloglu AC (2017) Integration of GPCR signaling and sorting from very early endosomes via opposing APPL1 mechanisms. Cell Rep 21, 2855-2867. Ulloa-Aguirre A, Zariñán T, Jardón-Valadez E, Gutiérrez-Sagal R and Dias JA (2018) Structure-function relationships of the follicle-stimulating hormone receptor. Front Endocrinol 9, 707. Stallaert W, Van Der Westhuizen ET, Schönegge AM, Plouffe B, Hogue M, Lukashova V, Inoue A, Ishida S, Aoki J, Le Gouill C et al. (2017) Purinergic receptor transactivation by the β2-adrenergic receptor increases intracellular Ca2+ in nonexcitable cells. Mol Pharmacol 91, 533-544. Devost D, Sleno R, Pétrin D, Zhang A, Shinjo Y, Okde R, Aoki J, Inoue A and Hébert TE (2017) Conformational profiling of the AT1 angiotensin II receptor reflects biased Agonism, G protein coupling, and cellular context. J Biol Chem 292, 5443-5456. Ayoub MA, Landomiel F, Gallay N, Jégot G, Poupon A, Crépieux P and Reiter E (2015) Assessing gonadotropin receptor function by resonance energy transfer-based assays. Front Endocrinol 6, 130. Wan Q, Okashah N, Inoue A, Nehmé R, Carpenter B, Tate CG and Lambert NA (2018) Mini G protein probes for active G protein-coupled receptors (GPCRs) in live cells. J Biol Chem 293, 7466-7473. Tranchant T, Durand G, Gauthier C, Crépieux P, Ulloa-Aguirre A, Royère D and Reiter E (2011) Preferential β-arrestin signalling at low receptor density revealed by functional characterization of the human FSH receptor A189 V mutation. Mol Cell Endocrinol 331, 109-118. Heitzler D, Durand G, Gallay N, Rizk A, Ahn S, Kim J, Violin JD, Dupuy L, Gauthier C, Piketty V et al. (2012) Competing G protein-coupled receptor kinases balance G protein and β-arrestin signaling. Mol Syst Biol 8, 590. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B et al. (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9, 676-682. Bertoni M, Kiefer F, Biasini M, Bordoli L and Schwede T (2017) Modeling protein quaternary structure of homo- and hetero-oligomers beyond binary interactions by homology. Sci Rep 7, 10480. Bienert S, Waterhouse A, de Beer TAP, Tauriello G, Studer G, Bordoli L and Schwede T (2017) The SWISS-MODEL repository-new features and functionality. Nucleic Acids Res 45, D313-D319. Waterhouse A, Bertoni M, Bienert S, Studer G, Tauriello G, Gumienny R, Heer FT, de Beer TAP, Rempfer C, Bordoli L et al. (2018) SWISS-MODEL: homology modelling of protein structures and complexes. Nucleic Acids Res 46, W296-W303. Studer G, Rempfer C, Waterhouse AM, Gumienny R, Haas J and Schwede T (2020) QMEANDisCo-distance constraints applied on model quality estimation. Bioinformatics 36, 1765-1771. Van Zundert GCP, Rodrigues JPGLM, Trellet M, Schmitz C, Kastritis PL, Karaca E, Melquiond ASJ, van Dijk M, de Vries SJ and Bonvin AMJJ (2016) The HADDOCK2.2 web server: user-friendly integrative modeling of biomolecular complexes. J Mol Biol 428, 720-725. Honorato RV, Koukos PI, Jiménez-García B, Tsaregorodtsev A, Verlato M, Giachetti A, Rosato A and Bonvin AMJJ (2021) Structural biology in the clouds: the WeNMR-EOSC ecosystem. Front Mol Biosci 8, 729513. Timossi C, Ortiz-Elizondo C, Pineda DB, Dias JA, Conn PM and Ulloa-Aguirre A (2004) Functional significance of the BBXXB motif reversed present in the cytoplasmic domains of the human follicle-stimulating hormone receptor. Mol Cell Endocrinol 223, 17-26. Sadler F, Ma N, Ritt M, Sharma Y, Vaidehi N and Sivaramakrishnan S (2023) Autoregulation of GPCR signalling through the third intracellular loop. Nature 615, 734-741. Pardon E, Betti C, Laeremans T, Chevillard F, Guillemyn K, Kolb P, Ballet S and Steyaert J (2018) Nanobody-enabled reverse pharmacology on G-protein-coupled receptors. Angew Chem Int Ed 57, 5292-5295. |
معلومات مُعتمدة: | Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement; ANR-10-LABX-53 LabEx MAbImprove; Région Centre Val de Loire RD2020 Biomédicaments SELMAT; INTACT Région Centre Val de Loire APR-IR; Centre National de la Recherche Scientifique (CNRS) |
فهرسة مساهمة: | Keywords: FSH receptor; G protein-coupled receptors; cell signalling; intracellular VHH |
المشرفين على المادة: | 0 (Receptors, FSH) 9002-68-0 (Follicle Stimulating Hormone) EC 3.6.1.- (GTP-Binding Proteins) |
تواريخ الأحداث: | Date Created: 20231103 Date Completed: 20240130 Latest Revision: 20240206 |
رمز التحديث: | 20240206 |
DOI: | 10.1002/1873-3468.14765 |
PMID: | 37923554 |
قاعدة البيانات: | MEDLINE |
تدمد: | 1873-3468 |
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DOI: | 10.1002/1873-3468.14765 |