Abstract
Recent experiments to derive a thermally stable mutant of turkey beta-1-adrenergic receptor (beta1AR) have shown that a combination of six single point mutations resulted in a 20 degrees C increase in thermal stability in mutant beta1AR. Here we have used the all-atom force-field energy function to calculate a stability score to detect stabilizing point mutations in G-protein coupled receptors. The calculated stability score shows good correlation with the measured thermal stability for 76 single point mutations and 22 multiple mutants in beta1AR. We have demonstrated that conformational sampling of the receptor for various mutants improve the prediction of thermal stability by 50%. Point mutations Y227A5.58, V230A5.61, and F338M7.48 in the thermally stable mutant m23-beta1AR stabilizes key microdomains of the receptor in the inactive conformation. The Y227A5.58 and V230A5.61 mutations stabilize the ionic lock between R139(3.50) on transmembrane helix3 and E285(6.30) on transmembrane helix6. The mutation F338M7.48 on TM7 alters the interaction of the conserved motif NPxxY(x)5,6F with helix8 and hence modulates the interaction of TM2-TM7-helix8 microdomain. The D186-R317 salt bridge (in extracellular loops 2 and 3) is stabilized in the cyanopindolol-bound wild-type beta1AR, whereas the salt bridge between D184-R317 is preferred in the mutant m23. We propose that this could be the surrogate to a similar salt bridge found between the extracellular loop 2 and TM7 in beta2AR reported recently. We show that the binding energy difference between the inactive and active states is less in m23 compared to the wild-type, which explains the activation of m23 at higher norepinephrine concentration compared to the wild-type. Results from this work throw light into the mechanism behind stabilizing mutations. The computational scheme proposed in this work could be used to design stabilizing mutations for other G-protein coupled receptors.
MeSH Terms
Adrenergic beta-1 Receptor Agonists
Amino Acid Substitution/genetics
Animals
Models, Molecular
Mutant Proteins/chemistry
Mutation/genetics
Norepinephrine/metabolism
Pindolol/analogs & derivatives,pharmacology
Protein Stability/drug effects
Protein Structure, Secondary
Receptors, Adrenergic, beta-1/chemistry
Salts/metabolism
Transition Temperature/drug effects
Turkeys
Chemicals
Adrenergic beta-1 Receptor Agonists
Mutant Proteins
Receptors, Adrenergic, beta-1
Salts
cyanopindolol
Pindolol
Norepinephrine
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Balaraman Gouthaman S
Division of Immunology, Beckman Research Institute of the City of Hope, Duarte, California, USA.
Bhattacharya Supriyo
Vaidehi Nagarajan
References (30)
30 references, click to expand
-
Crystal structure of the ligand-free G-protein-coupled receptor opsin.
Nature. 2008 Jul 10;454(7201):183-7
PMID: 18563085
-
Flat-Bottom Strategy for Improved Accuracy in Protein Side-Chain Placements.
J Chem Theory Comput. 2008 Dec 9;4(12):2160-9
PMID: 26620487
-
All-atom empirical potential for molecular modeling and dynamics studies of proteins.
J Phys Chem B. 1998 Apr 30;102(18):3586-616
PMID: 24889800
-
Conserved aspartic acid residues 79 and 113 of the beta-adrenergic receptor have different roles in receptor function.
J Biol Chem. 1988 Jul 25;263(21):10267-71
PMID: 2899076
-
Conformational thermostabilization of the beta1-adrenergic receptor in a detergent-resistant form.
Proc Natl Acad Sci U S A. 2008 Jan 22;105(3):877-82
PMID: 18192400
-
GPCR engineering yields high-resolution structural insights into beta2-adrenergic receptor function.
Science. 2007 Nov 23;318(5854):1266-73
PMID: 17962519
-
Exploring folding free energy landscapes using computational protein design.
Curr Opin Struct Biol. 2004 Feb;14(1):89-95
PMID: 15102454
-
Rational protein design: combining theory and experiment.
Proc Natl Acad Sci U S A. 1997 Sep 16;94(19):10015-7
PMID: 9294154
-
Computational mapping of the conformational transitions in agonist selective pathways of a G-protein coupled receptor.
J Am Chem Soc. 2010 Apr 14;132(14):5205-14
PMID: 20235532
-
Involvement of Asn-293 in stereospecific agonist recognition and in activation of the beta 2-adrenergic receptor.
Proc Natl Acad Sci U S A. 1996 Aug 20;93(17):9276-81
PMID: 8799191
-
Designing proteins for therapeutic applications.
Curr Opin Struct Biol. 2003 Aug;13(4):513-8
PMID: 12948782
-
Role of the conserved NPxxY(x)5,6F motif in the rhodopsin ground state and during activation.
Proc Natl Acad Sci U S A. 2003 Mar 4;100(5):2290-5
PMID: 12601165
-
Identification of two distinct inactive conformations of the beta2-adrenergic receptor reconciles structural and biochemical observations.
Proc Natl Acad Sci U S A. 2009 Mar 24;106(12):4689-94
PMID: 19258456
-
Transferability of thermostabilizing mutations between beta-adrenergic receptors.
Mol Membr Biol. 2009 Dec;26(8):385-96
PMID: 19883298
-
Agonist-induced conformational changes in bovine rhodopsin: insight into activation of G-protein-coupled receptors.
J Mol Biol. 2008 Oct 3;382(2):539-55
PMID: 18638482
-
G-protein-coupled receptor structures were not built in a day.
Protein Sci. 2009 Jul;18(7):1335-42
PMID: 19536805
-
VMD: visual molecular dynamics.
J Mol Graph. 1996 Feb;14(1):33-8, 27-8
PMID: 8744570
-
Structural and dynamic effects of cholesterol at preferred sites of interaction with rhodopsin identified from microsecond length molecular dynamics simulations.
Proteins. 2009 Aug 1;76(2):403-17
PMID: 19173312
-
Design, structure and stability of a hyperthermophilic protein variant.
Nat Struct Biol. 1998 Jun;5(6):470-5
PMID: 9628485
-
Extra precision glide: docking and scoring incorporating a model of hydrophobic enclosure for protein-ligand complexes.
J Med Chem. 2006 Oct 19;49(21):6177-96
PMID: 17034125
-
Crystal structure of the human beta2 adrenergic G-protein-coupled receptor.
Nature. 2007 Nov 15;450(7168):383-7
PMID: 17952055
-
Ligand-stabilized conformational states of human beta(2) adrenergic receptor: insight into G-protein-coupled receptor activation.
Biophys J. 2008 Mar 15;94(6):2027-42
PMID: 18065472
-
Scalable molecular dynamics with NAMD.
J Comput Chem. 2005 Dec;26(16):1781-802
PMID: 16222654
-
A graph-theory algorithm for rapid protein side-chain prediction.
Protein Sci. 2003 Sep;12(9):2001-14
PMID: 12930999
-
Computer-based design of novel protein structures.
Annu Rev Biophys Biomol Struct. 2006;35:49-65
PMID: 16689627
-
The forgotten serine. A critical role for Ser-2035.42 in ligand binding to and activation of the beta 2-adrenergic receptor.
J Biol Chem. 2000 Dec 1;275(48):37779-88
PMID: 10964911
-
Ligand-specific regulation of the extracellular surface of a G-protein-coupled receptor.
Nature. 2010 Jan 7;463(7277):108-12
PMID: 20054398
-
Structure of a beta1-adrenergic G-protein-coupled receptor.
Nature. 2008 Jul 24;454(7203):486-91
PMID: 18594507
-
Predicting free energy changes using structural ensembles.
Nat Methods. 2009 Jan;6(1):3-4
PMID: 19116609
-
The structure and function of G-protein-coupled receptors.
Nature. 2009 May 21;459(7245):356-63
PMID: 19458711