Structures of active melanocortin-4 receptor-Gs-protein complexes with NDP-α-MSH and setmelanotide.


Journal

Cell research
ISSN: 1748-7838
Titre abrégé: Cell Res
Pays: England
ID NLM: 9425763

Informations de publication

Date de publication:
11 2021
Historique:
received: 08 05 2021
accepted: 31 08 2021
pubmed: 26 9 2021
medline: 27 1 2022
entrez: 25 9 2021
Statut: ppublish

Résumé

The melanocortin-4 receptor (MC4R), a hypothalamic master regulator of energy homeostasis and appetite, is a class A G-protein-coupled receptor and a prime target for the pharmacological treatment of obesity. Here, we present cryo-electron microscopy structures of MC4R-Gs-protein complexes with two drugs recently approved by the FDA, the peptide agonists NDP-α-MSH and setmelanotide, with 2.9 Å and 2.6 Å resolution. Together with signaling data from structure-derived MC4R mutants, the complex structures reveal the agonist-induced origin of transmembrane helix (TM) 6-regulated receptor activation. The ligand-binding modes of NDP-α-MSH, a high-affinity linear variant of the endogenous agonist α-MSH, and setmelanotide, a cyclic anti-obesity drug with biased signaling toward Gq/11, underline the key role of TM3 in ligand-specific interactions and of calcium ion as a ligand-adaptable cofactor. The agonist-specific TM3 interplay subsequently impacts receptor-Gs-protein interfaces at intracellular loop 2, which also regulates the G-protein coupling profile of this promiscuous receptor. Finally, our structures reveal mechanistic details of MC4R activation/inhibition, and provide important insights into the regulation of the receptor signaling profile which will facilitate the development of tailored anti-obesity drugs.

Identifiants

pubmed: 34561620
doi: 10.1038/s41422-021-00569-8
pii: 10.1038/s41422-021-00569-8
pmc: PMC8563958
doi:

Substances chimiques

Receptor, Melanocortin, Type 4 0
setmelanotide 0
alpha-MSH 581-05-5
MSH, 4-Nle-7-Phe-alpha- 75921-69-6

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1176-1189

Subventions

Organisme : Deutsche Forschungsgemeinschaft (German Research Foundation)
ID : CRC1423 - project number 421152132, Z03
Organisme : Deutsche Forschungsgemeinschaft (German Research Foundation)
ID : CRC1423 - project number 394046635, A03
Organisme : Deutsche Forschungsgemeinschaft (German Research Foundation)
ID : Germany's Excellence Strategies - EXC2008/1 (UniSysCat) - 390540038
Organisme : Deutsche Forschungsgemeinschaft (German Research Foundation)
ID : CRC1423 - project number 421152132, A05

Informations de copyright

© 2021. The Author(s).

Références

Science. 2020 Apr 24;368(6489):428-433
pubmed: 32327598
J Pharmacol Exp Ther. 2003 Mar;304(3):1217-27
pubmed: 12604699
Front Endocrinol (Lausanne). 2019 Jul 31;10:515
pubmed: 31417496
J Mol Endocrinol. 2016 Jul;57(1):R59-80
pubmed: 27151573
Acta Crystallogr D Biol Crystallogr. 2010 Apr;66(Pt 4):486-501
pubmed: 20383002
Nat Methods. 2020 Dec;17(12):1214-1221
pubmed: 33257830
Proc Natl Acad Sci U S A. 2004 Jan 27;101(4):959-63
pubmed: 14732697
Nature. 2008 Sep 25;455(7212):497-502
pubmed: 18818650
Science. 2021 May 21;372(6544):808-814
pubmed: 33858992
Lancet Diabetes Endocrinol. 2020 Dec;8(12):960-970
pubmed: 33137293
Acta Crystallogr D Biol Crystallogr. 1994 Sep 1;50(Pt 5):760-3
pubmed: 15299374
Nat Med. 2018 May;24(5):551-555
pubmed: 29736023
Science. 2019 May 10;364(6440):552-557
pubmed: 31073061
Acta Crystallogr D Biol Crystallogr. 2011 Apr;67(Pt 4):235-42
pubmed: 21460441
Int J Mol Sci. 2020 Feb 12;21(4):
pubmed: 32059383
Biochemistry. 2000 Dec 5;39(48):14900-11
pubmed: 11101306
Proc Natl Acad Sci U S A. 1980 Oct;77(10):5754-8
pubmed: 6777774
Nature. 2008 Jul 10;454(7201):183-7
pubmed: 18563085
J Comput Chem. 2004 Oct;25(13):1605-12
pubmed: 15264254
J Pediatr Endocrinol Metab. 2020 Jul 3;:
pubmed: 32619193
Nat Methods. 2015 Jul;12(7):661-663
pubmed: 26030448
Peptides. 2009 Oct;30(10):1892-900
pubmed: 19646498
Life Sci. 1996;58(20):1777-84
pubmed: 8637402
Trends Pharmacol Sci. 2011 Apr;32(4):213-8
pubmed: 21414670
Cell Metab. 2006 Feb;3(2):141-6
pubmed: 16459315
Acta Crystallogr D Biol Crystallogr. 2010 Jan;66(Pt 1):12-21
pubmed: 20057044
Acta Crystallogr D Biol Crystallogr. 1999 Jan;55(Pt 1):191-205
pubmed: 10089410
Acta Crystallogr D Biol Crystallogr. 2004 Dec;60(Pt 12 Pt 1):2184-95
pubmed: 15572771
N Engl J Med. 2016 Jul 21;375(3):240-6
pubmed: 27468060
N Engl J Med. 2015 Jul 2;373(1):48-59
pubmed: 26132941
J Med Chem. 1995 Sep 1;38(18):3454-61
pubmed: 7658432
Nature. 2011 Jul 19;477(7366):549-55
pubmed: 21772288
J Clin Endocrinol Metab. 2015 Apr;100(4):1639-45
pubmed: 25675384
J Mol Biol. 1994 May 20;238(5):777-93
pubmed: 8182748
Acta Crystallogr D Struct Biol. 2018 Jun 1;74(Pt 6):531-544
pubmed: 29872004
J Biol Chem. 2002 Jun 7;277(23):20328-35
pubmed: 11912210
Nature. 2015 Aug 13;524(7564):173-179
pubmed: 26147082
Biochemistry. 2005 Aug 30;44(34):11329-41
pubmed: 16114870
J Biol Chem. 1993 Oct 25;268(30):22273-6
pubmed: 8226735
Methods Enzymol. 2002;343:329-71
pubmed: 11665578
Nat Rev Drug Discov. 2008 Apr;7(4):307-23
pubmed: 18323849
Science. 2007 Nov 23;318(5854):1258-65
pubmed: 17962520
Biochim Biophys Acta Mol Basis Dis. 2017 Oct;1863(10 Pt A):2414-2435
pubmed: 28363699
Handb Exp Pharmacol. 2012;(209):47-75
pubmed: 22249810
Endocr Rev. 2010 Aug;31(4):506-43
pubmed: 20190196
Biochemistry. 2006 Jun 13;45(23):7277-88
pubmed: 16752916
Nature. 2014 Jan 9;505(7482):234-8
pubmed: 24336198
Nature. 2011 Mar 31;471(7340):651-5
pubmed: 21389988
Mol Endocrinol. 2001 Jan;15(1):164-71
pubmed: 11145747
J Clin Endocrinol Metab. 2006 May;91(5):1761-9
pubmed: 16492696
Acta Crystallogr D Biol Crystallogr. 2010 Feb;66(Pt 2):213-21
pubmed: 20124702
J Clin Invest. 2000 Jul;106(2):253-62
pubmed: 10903341
Biochemistry. 2005 Mar 8;44(9):3418-31
pubmed: 15736952
Eur J Pharmacol. 2005 Apr 11;512(2-3):85-95
pubmed: 15840392
Mol Cell Endocrinol. 2017 Jul 5;449:3-11
pubmed: 27899324
Mol Cell Endocrinol. 1990 Apr 17;70(2):139-45
pubmed: 2161361
Cell. 2020 Sep 17;182(6):1574-1588.e19
pubmed: 32946782
Cell Res. 2021 Oct;31(10):1061-1071
pubmed: 34453129
Nature. 2017 Jun 8;546(7657):248-253
pubmed: 28538729
Nucleic Acids Res. 2003 Jan 15;31(2):E6-6
pubmed: 12527795
Int J Mol Sci. 2020 Oct 15;21(20):
pubmed: 33076233
Neuropeptides. 1999 Jun;33(3):191-6
pubmed: 10657491
J Chem Inf Model. 2011 Oct 24;51(10):2778-86
pubmed: 21919503
Biochim Biophys Acta Mol Basis Dis. 2017 Oct;1863(10 Pt A):2462-2467
pubmed: 28499989
Nat Neurosci. 2016 Feb;19(2):206-19
pubmed: 26814590

Auteurs

Nicolas A Heyder (NA)

Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Institute of Medical Physics and Biophysics, Group Protein X-ray Crystallography and Signal Transduction, Charitéplatz 1, Berlin, Germany.

Gunnar Kleinau (G)

Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Institute of Medical Physics and Biophysics, Group Protein X-ray Crystallography and Signal Transduction, Charitéplatz 1, Berlin, Germany.

David Speck (D)

Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Institute of Medical Physics and Biophysics, Group Protein X-ray Crystallography and Signal Transduction, Charitéplatz 1, Berlin, Germany.

Andrea Schmidt (A)

Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Institute of Medical Physics and Biophysics, Group Protein X-ray Crystallography and Signal Transduction, Charitéplatz 1, Berlin, Germany.

Sarah Paisdzior (S)

Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Institute for Experimental Pediatric Endocrinology, Berlin, Germany.

Michal Szczepek (M)

Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Institute of Medical Physics and Biophysics, Group Protein X-ray Crystallography and Signal Transduction, Charitéplatz 1, Berlin, Germany.

Brian Bauer (B)

Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Institute of Medical Physics and Biophysics, Group Protein X-ray Crystallography and Signal Transduction, Charitéplatz 1, Berlin, Germany.

Anja Koch (A)

Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Institute of Medical Physics and Biophysics, Group Protein X-ray Crystallography and Signal Transduction, Charitéplatz 1, Berlin, Germany.

Monique Gallandi (M)

Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Institute of Medical Physics and Biophysics, Group Protein X-ray Crystallography and Signal Transduction, Charitéplatz 1, Berlin, Germany.

Dennis Kwiatkowski (D)

Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Institute of Medical Physics and Biophysics, Group Protein X-ray Crystallography and Signal Transduction, Charitéplatz 1, Berlin, Germany.

Jörg Bürger (J)

Charité - Universitätsmedizin Berlin, Institute of Medical Physics and Biophysics, Berlin, Germany.
Microscopy and Cryo-Electron Microscopy Service Group, Max-Planck-Institut für Molekulare Genetik, Berlin, Germany.

Thorsten Mielke (T)

Microscopy and Cryo-Electron Microscopy Service Group, Max-Planck-Institut für Molekulare Genetik, Berlin, Germany.

Annette G Beck-Sickinger (AG)

Faculty of Life Sciences, Institute of Biochemistry, Leipzig University, Leipzig, Germany.

Peter W Hildebrand (PW)

Charité - Universitätsmedizin Berlin, Institute of Medical Physics and Biophysics, Berlin, Germany.
Institute for Medical Physics and Biophysics, Medical Faculty, Leipzig University, Leipzig, Germany.
Berlin Institute of Health at Charité - Universitätsmedizin Berlin, Core Facility Genomics, Charitéplatz 1, Berlin, Germany.

Christian M T Spahn (CMT)

Charité - Universitätsmedizin Berlin, Institute of Medical Physics and Biophysics, Berlin, Germany.

Daniel Hilger (D)

Department of Pharmaceutical Chemistry, Philipps-University Marburg, Marburg, Germany.

Magdalena Schacherl (M)

Charité - Universitätsmedizin Berlin, Institute of Medical Physics and Biophysics, Berlin, Germany.

Heike Biebermann (H)

Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Institute for Experimental Pediatric Endocrinology, Berlin, Germany.

Tarek Hilal (T)

Research Center of Electron Microscopy and Core Facility BioSupraMol, Institute of Chemistry and Biochemistry, Freie Universität Berlin, Berlin, Germany.

Peter Kühnen (P)

Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Institute for Experimental Pediatric Endocrinology, Berlin, Germany.

Brian K Kobilka (BK)

Berlin Institute of Health at Charité - Universitätsmedizin Berlin, Core Facility Genomics, Charitéplatz 1, Berlin, Germany.
Department of Molecular and Cellular Physiology, Stanford University School of Medicine, Stanford, CA, USA.

Patrick Scheerer (P)

Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Institute of Medical Physics and Biophysics, Group Protein X-ray Crystallography and Signal Transduction, Charitéplatz 1, Berlin, Germany. patrick.scheerer@charite.de.
DZHK (German Centre for Cardiovascular Research), partner site Berlin, Berlin, Germany. patrick.scheerer@charite.de.

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Classifications MeSH