Structural insights into the lipid and ligand regulation of serotonin receptors

0
86


  • 1.

    Berger, M., Gray, J. A. & Roth, B. L. The expanded biology of serotonin. Annu. Rev. Med. 60, 355–366 (2009).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 2.

    Mohammad-Zadeh, L. F., Moses, L. & Gwaltney-Brant, S. M. Serotonin: a review. J. Vet. Pharmacol. Ther. 31, 187–199 (2008).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 3.

    Hannon, J. & Hoyer, D. Molecular biology of 5-HT receptors. Behav. Brain Res. 195, 198–213 (2008).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 4.

    Barnes, N. M. et al. International Union of Basic and Clinical Pharmacology. CX. Classification of receptors for 5-hydroxytryptamine; pharmacology and function. Pharmacol. Rev. 73, 310–520 (2021).

    PubMed 
    Article 

    Google Scholar
     

  • 5.

    Dawaliby, R. et al. Allosteric regulation of G protein-coupled receptor activity by phospholipids. Nat. Chem. Biol. 12, 35–39 (2016).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 6.

    Duncan, A. L., Song, W. & Sansom, M. S. P. Lipid-dependent regulation of ion channels and G protein-coupled receptors: insights from structures and simulations. Annu. Rev. Pharmacol. Toxicol. 60, 31–50 (2020).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 7.

    van Meer, G., Voelker, D. R. & Feigenson, G. W. Membrane lipids: where they are and how they behave. Nat. Rev. Mol. Cell Biol. 9, 112–124 (2008).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar
     

  • 8.

    Di Paolo, G. & De Camilli, P. Phosphoinositides in cell regulation and membrane dynamics. Nature 443, 651–657 (2006).

    ADS 
    PubMed 
    Article 
    CAS 

    Google Scholar
     

  • 9.

    de Rubio, R. G. et al. Phosphatidylinositol 4-phosphate is a major source of GPCR-stimulated phosphoinositide production. Sci. Signal. 11, eaan1210 (2018).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar
     

  • 10.

    Yen, H. Y. et al. PtdIns(4,5)P-2 stabilizes active states of GPCRs and enhances selectivity of G-protein coupling. Nature 559, 423–427 (2018).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 11.

    Falkenburger, B. H., Jensen, J. B., Dickson, E. J., Suh, B. C. & Hille, B. Phosphoinositides: lipid regulators of membrane proteins. J. Physiol. 588, 3179–3185 (2010).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 12.

    Seifert, R. & Wenzel-Seifert, K. Constitutive activity of G-protein-coupled receptors: cause of disease and common property of wild-type receptors. Naunyn Schmiedebergs Arch. Pharmacol. 366, 381–416 (2002).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 13.

    Teitler, M., Herrick-Davis, K. & Purohit, A. Constitutive activity of G-protein coupled receptors: emphasis on serotonin receptors. Curr. Top. Med. Chem. 2, 529–538 (2002).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 14.

    De Deurwaerdère, P., Bharatiya, R., Chagraoui, A. & Di Giovanni, G. Constitutive activity of 5-HT receptors: factual analysis. Neuropharmacology 168, 107967 (2020).

    PubMed 
    Article 
    CAS 

    Google Scholar
     

  • 15.

    Berg, K. A., Harvey, J. A., Spampinato, U. & Clarke, W. P. Physiological and therapeutic relevance of constitutive activity of 5-HT2A and 5-HT2C receptors for the treatment of depression. Prog. Brain Res. 172, 287–305 (2008).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 16.

    Gutierrez, M. G., Mansfield, K. S. & Malmstadt, N. The functional activity of the human serotonin 5-HT1A receptor is controlled by lipid bilayer composition. Biophys. J. 110, 2486–2495 (2016).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 17.

    Winner, P. Triptans for migraine management in adolescents. Headache 42, 675–679 (2002).

    PubMed 
    Article 

    Google Scholar
     

  • 18.

    Shimron-Abarbanell, D., Nöthen, M. M., Erdmann, J. & Propping, P. Lack of genetically determined structural variants of the human serotonin-1E (5-HT1E) receptor protein points to its evolutionary conservation. Brain Res. Mol. Brain Res. 29, 387–390 (1995).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 19.

    Liang, Y. L. et al. Dominant negative G proteins enhance formation and purification of agonist-GPCR-G protein complexes for structure determination. ACS Pharmacol Transl Sci 1, 12–20 (2018).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 20.

    Yin, W. et al. Crystal structure of the human 5-HT1B serotonin receptor bound to an inverse agonist. Cell Discov. 4, 12 (2018).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar
     

  • 21.

    García-Nafría, J., Nehmé, R., Edwards, P. C. & Tate, C. G. Cryo-EM structure of the serotonin 5-HT1B receptor coupled to heterotrimeric Go. Nature 558, 620–623 (2018).

    ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar
     

  • 22.

    Carlson, M. L. et al. The peptidisc, a simple method for stabilizing membrane proteins in detergent-free solution. eLife 7, e34085 (2018).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 23.

    Evans, K. L. J., Cropper, J. D., Berg, K. A. & Clarke, W. P. Mechanisms of regulation of agonist efficacy at the 5-HT1A receptor by phospholipid-derived signaling components. J. Pharmacol. Exp. Ther. 297, 1025–1035 (2001).

    CAS 
    PubMed 

    Google Scholar
     

  • 24.

    Pucadyil, T. J. & Chattopadhyay, A. Cholesterol modulates the antagonist-binding function of hippocampal serotonin1A receptors. Biochim. Biophys. Acta Biomembr. 1714, 35–42 (2005).

    CAS 
    Article 

    Google Scholar
     

  • 25.

    Kim, K. et al. Structure of a hallucinogen-activated Gq-coupled 5-HT2A serotonin receptor. Cell 182, 1574–1588 (2020).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 26.

    Forster, E. A. et al. A pharmacological profile of the selective silent 5-HT1A receptor antagonist, WAY-100635. Eur. J. Pharmacol. 281, 81–88 (1995).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 27.

    Zhou, Q. T. et al. Common activation mechanism of class A GPCRs. eLife 8, e50279 (2019).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 28.

    Kooistra, A.J. et al. GPCRdb in 2021: integrating GPCR sequence, structure and function. Nucleic Acids Res. 49, D335–D343 (2021).

    PubMed 
    Article 

    Google Scholar
     

  • 29.

    Klein, M. T., Dukat, M., Glennon, R. A. & Teitler, M. Toward selective drug development for the human 5-hydroxytryptamine 1E receptor: a comparison of 5-hydroxytryptamine 1E and 1F receptor structure-affinity relationships. J. Pharmacol. Exp. Ther. 337, 860–867 (2011).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 30.

    Xu, P. et al. Structures of the human dopamine D3 receptor-Gi complexes. Mol. Cell https://doi.org/10.1016/j.molcel.2021.01.003 (2021).

  • 31.

    Davies, M. A., Sheffler, D. J. & Roth, B. L. Aripiprazole: a novel atypical antipsychotic drug with a uniquely robust pharmacology. CNS Drug Rev. 10, 317–336 (2004).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 32.

    Sjögren, B., Csöregh, L. & Svenningsson, P. Cholesterol reduction attenuates 5-HT1A receptor-mediated signaling in human primary neuronal cultures. Naunyn Schmiedebergs Arch. Pharmacol. 378, 441–446 (2008).

    PubMed 
    Article 
    CAS 

    Google Scholar
     

  • 33.

    Chun, E. et al. Fusion partner toolchest for the stabilization and crystallization of G protein-coupled receptors. Structure 20, 967–976 (2012).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 34.

    Wang, C. et al. Structural basis for molecular recognition at serotonin receptors. Science 340, 610–614 (2013).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 35.

    Roth, C. B., Hanson, M. A. & Stevens, R. C. Stabilization of the human β2-adrenergic receptor TM4–TM3–TM5 helix interface by mutagenesis of Glu1223.41, a critical residue in GPCR structure. J. Mol. Biol. 376, 1305–1319 (2008).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 36.

    Maeda, S. et al. Development of an antibody fragment that stabilizes GPCR/G-protein complexes. Nat. Commun. 9, 3712 (2018).

    ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar
     

  • 37.

    Angiulli, G. et al. New approach for membrane protein reconstitution into peptidiscs and basis for their adaptability to different proteins. eLife 9, e53530 (2020).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 38.

    Zheng, S. Q. et al. MotionCor2: anisotropic correction of beam-induced motion for improved cryo-electron microscopy. Nat. Methods 14, 331–332 (2017).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 39.

    Zhang, K. Gctf: real-time CTF determination and correction. J. Struct. Biol. 193, 1–12 (2016).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 40.

    Scheres, S. H. RELION: implementation of a Bayesian approach to cryo-EM structure determination. J. Struct. Biol. 180, 519–530 (2012).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 41.

    Kato, H. E. et al. Conformational transitions of a neurotensin receptor 1-Gi1 complex. Nature 572, 80–85 (2019).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 42.

    Heymann, J. B. Guidelines for using Bsoft for high resolution reconstruction and validation of biomolecular structures from electron micrographs. Protein Sci. 27, 159–171 (2018).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 43.

    Kang, Y. Y. et al. Cryo-EM structure of human rhodopsin bound to an inhibitory G protein. Nature 558, 553–558 (2018).

    ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 44.

    Pettersen, E. F. et al. UCSF Chimera—a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605–1612 (2004).

    CAS 
    Article 

    Google Scholar
     

  • 45.

    Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D 60, 2126–2132 (2004).

    PubMed 
    Article 
    CAS 

    Google Scholar
     

  • 46.

    Croll, T. I. ISOLDE: a physically realistic environment for model building into low-resolution electron-density maps. Acta Crystallogr. D 74, 519–530 (2018).

    CAS 
    Article 

    Google Scholar
     

  • 47.

    Adams, P. D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D 66, 213–221 (2010).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 48.

    Williams, C. J. et al. MolProbity: more and better reference data for improved all-atom structure validation. Protein Sci. 27, 293–315 (2018).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 49.

    Pettersen, E. F. et al. UCSF ChimeraX: structure visualization for researchers, educators, and developers. Protein Sci. 30, 70–82 (2021).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 50.

    Halgren, T. A. et al. Glide: a new approach for rapid, accurate docking and scoring. 2. Enrichment factors in database screening. J. Med. Chem. 47, 1750–1759 (2004).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 51.

    Isberg, V. et al. Genetic GPCR residue numbers – aligning topology maps while minding the caps. Trends Pharmacol. Sci. 36, 22–31 (2015).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 52.

    Šali, A. & Blundell, T. L. Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234, 779–815 (1993).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 53.

    Wu, E. L. et al. CHARMM-GUI Membrane Builder toward realistic biological membrane simulations. J. Comput. Chem. 35, 1997–2004 (2014).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 54.

    Guvench, O. et al. CHARMM additive all-atom force field for carbohydrate derivatives and its utility in polysaccharide and carbohydrate-protein modeling. J. Chem. Theory Comput. 7, 3162–3180 (2011).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 55.

    MacKerell, A. D. et al. All-atom empirical potential for molecular modeling and dynamics studies of proteins. J. Phys. Chem. B 102, 3586–3616 (1998).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 56.

    Van Der Spoel, D. et al. GROMACS: fast, flexible, and free. J. Comput. Chem. 26, 1701–1718 (2005).

    Article 
    CAS 

    Google Scholar
     

  • 57.

    Hess, B., Kutzner, C., van der Spoel, D. & Lindahl, E. GROMACS 4: algorithms for highly efficient, load-balanced, and scalable molecular simulation. J. Chem. Theory Comput. 4, 435–447 (2008).

    CAS 
    Article 

    Google Scholar
     

  • 58.

    Bussi, G., Donadio, D. & Parrinello, M. Canonical sampling through velocity rescaling. J. Chem. Phys. 126, 014101 (2007).

    ADS 
    PubMed 
    Article 
    CAS 

    Google Scholar
     

  • 59.

    Aoki, K. M. & Yonezawa, F. Constant-pressure molecular-dynamics simulations of the crystal-smectic transition in systems of soft parallel spherocylinders. Phys. Rev. A 46, 6541–6549 (1992).

    ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 60.

    Hess, B. P-LINCS: a parallel linear constraint solver for molecular simulation. J. Chem. Theory Comput. 4, 116–122 (2008).

    CAS 
    PubMed 
    Article 

    Google Scholar
     



  • Source link