Intramolecular allosteric communication in dopamine D2 receptor revealed by evolutionary amino acid covariation

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 13, 2016, Pages 3539-3544

  Sung, Yun Min ^a   Wilkins, Angela D ^a   Rodriguez, Gustavo J ^a   Wensel, Theodore G ^a   Lichtarge, Olivier ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Allostery; Evolutionary Trace; G protein coupled receptors; Residue covariation

Indexed keywords

AMINO ACID; DOPAMINE 2 RECEPTOR; G PROTEIN COUPLED RECEPTOR; DOPAMINE; GUANINE NUCLEOTIDE BINDING PROTEIN; LIGAND; RECOMBINANT PROTEIN; SEROTONIN;

ALGORITHM; ALLOSTERISM; ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; EC50; EVOLUTIONARY ALGORITHM; LIGAND BINDING; LOSS OF FUNCTION MUTATION; MUTAGENESIS; PREDICTION; PRIORITY JOURNAL; PROTEIN STRUCTURE; AMINO ACID SUBSTITUTION; BINDING SITE; CHEMISTRY; GENETIC VARIATION; GENETICS; HEK293 CELL LINE; HUMAN; METABOLISM; MOLECULAR EVOLUTION; MOLECULAR MODEL; PROTEIN DOMAIN; SITE DIRECTED MUTAGENESIS; THERMODYNAMICS;

ALGORITHMS; AMINO ACID SUBSTITUTION; AMINO ACIDS; BINDING SITES; DOPAMINE; EVOLUTION, MOLECULAR; GENETIC VARIATION; GTP-BINDING PROTEINS; HEK293 CELLS; HUMANS; LIGANDS; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; PROTEIN INTERACTION DOMAINS AND MOTIFS; RECEPTORS, DOPAMINE D2; RECOMBINANT PROTEINS; SEROTONIN; THERMODYNAMICS;

EID: 84962054908     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1516579113     Document Type: Article

References (62)

1. Ortlund EA, Bridgham JT, Redinbo MR, Thornton JW (2007) Crystal structure of an ancient protein: Evolution by conformational epistasis. Science 317(5844):1544-1548.
2. Jones DT, Buchan DW, Cozzetto D, Pontil M (2012) PSICOV: Precise structural contact prediction using sparse inverse covariance estimation on large multiple sequence alignments. Bioinformatics 28(2):184-190.
3. Nemoto W, Imai T, Takahashi T, Kikuchi T, Fujita N (2004) Detection of pairwise residue proximity by covariation analysis for 3D-structure prediction of G-proteincoupled receptors. Protein J 23(6):427-435.
4. Fuchs A, et al. (2007) Co-evolving residues in membrane proteins. Bioinformatics 23(24):3312-3319.
5. Dunn SD, Wahl LM, Gloor GB (2008) Mutual information without the influence of phylogeny or entropy dramatically improves residue contact prediction. Bioinformatics 24(3):333-340.
6. Burger L, van Nimwegen E (2010) Disentangling direct from indirect co-evolution of residues in protein alignments. PLOS Comput Biol 6(1):e1000633.
7. Morcos F, et al. (2011) Direct-coupling analysis of residue coevolution captures native contacts across many protein families. Proc Natl Acad Sci USA 108(49):E1293-E1301.
8. Marks DS, et al. (2011) Protein 3D structure computed from evolutionary sequence variation. PLoS One 6(12):e28766.
9. Hopf TA, et al. (2012) Three-dimensional structures of membrane proteins from genomic sequencing. Cell 149(7):1607-1621.
10. Nugent T, Jones DT (2012) Accurate de novo structure prediction of large transmembrane protein domains using fragment-assembly and correlated mutation analysis. Proc Natl Acad Sci USA 109(24):E1540-E1547.
11. Sułkowska JI, Morcos F, Weigt M, Hwa T, Onuchic JN (2012) Genomics-aided structure prediction. Proc Natl Acad Sci USA 109(26):10340-10345.
12. Weigt M, White RA, Szurmant H, Hoch JA, Hwa T (2009) Identification of direct residue contacts in protein-protein interaction by message passing. Proc Natl Acad Sci USA 106(1):67-72.
13. Livesay DR, Kreth KE, Fodor AA (2012) A critical evaluation of correlated mutation algorithms and coevolution within allosteric mechanisms. Methods Mol Biol 796: 385-398.
14. Lockless SW, Ranganathan R (1999) Evolutionarily conserved pathways of energetic connectivity in protein families. Science 286(5438):295-299.
15. Gloor GB, Martin LC, Wahl LM, Dunn SD (2005) Mutual information in protein multiple sequence alignments reveals two classes of coevolving positions. Biochemistry 44(19):7156-7165.
16. Chakrabarti S, Panchenko AR (2009) Coevolution in defining the functional specificity. Proteins 75(1):231-240.
17. Süel GM, Lockless SW, Wall MA, Ranganathan R (2003) Evolutionarily conserved networks of residues mediate allosteric communication in proteins. Nat Struct Biol 10(1):59-69.
18. Halabi N, Rivoire O, Leibler S, Ranganathan R (2009) Protein sectors: Evolutionary units of three-dimensional structure. Cell 138(4):774-786.
19. Chi CN, et al. (2008) Reassessing a sparse energetic network within a single protein domain. Proc Natl Acad Sci USA 105(12):4679-4684.
20. Teşileanu T, Colwell LJ, Leibler S (2015) Protein sectors: Statistical coupling analysis versus conservation. PLOS Comput Biol 11(2):e1004091.
21. Madabushi S, et al. (2004) Evolutionary trace of G protein-coupled receptors reveals clusters of residues that determine global and class-specific functions. J Biol Chem 279(9):8126-8132.
22. Shenoy SK, et al. (2006) beta-arrestin-dependent, G protein-independent ERK1/2 activation by the beta2 adrenergic receptor. J Biol Chem 281(2):1261-1273.
23. Rodriguez GJ, Yao R, Lichtarge O, Wensel TG (2010) Evolution-guided discovery and recoding of allosteric pathway specificity determinants in psychoactive bioamine receptors. Proc Natl Acad Sci USA 107(17):7787-7792.
24. Kang HJ, Wilkins AD, Lichtarge O, Wensel TG (2015) Determinants of endogenous ligand specificity divergence among metabotropic glutamate receptors. J Biol Chem 290(5):2870-2878.
25. Lichtarge O, Bourne HR, Cohen FE (1996) An evolutionary trace method defines binding surfaces common to protein families. J Mol Biol 257(2):342-358.
26. Katsonis P, Lichtarge O (2014) A formal perturbation equation between genotype and phenotype determines the Evolutionary Action of protein-coding variations on fitness. Genome Res 24(12):2050-2058.
27. Wilkins AD, et al. (2013) Accounting for epistatic interactions improves the functional analysis of protein structures. Bioinformatics 29(21):2714-2721.
28. Bonci A, Hopf FW (2005) The dopamine D2 receptor: New surprises from an old friend. Neuron 47(3):335-338.
29. Yan Z, Song WJ, Surmeier J (1997) D2 dopamine receptors reduce N-type Ca2+ currents in rat neostriatal cholinergic interneurons through a membrane-delimited, protein-kinase-C-insensitive pathway. J Neurophysiol 77(2):1003-1015.
30. Einhorn LC, Oxford GS (1993) Guanine nucleotide binding proteins mediate D2 dopamine receptor activation of a potassium channel in rat lactotrophs. J Physiol 462: 563-578.
31. Luo Y, Kokkonen GC, Wang X, Neve KA, Roth GS (1998) D2 dopamine receptors stimulate mitogenesis through pertussis toxin-sensitive G proteins and Ras-involved ERK and SAP/JNK pathways in rat C6-D2L glioma cells. J Neurochem 71(3):980-990.
32. Hernandez-Lopez S, et al. (2000) D2 dopamine receptors in striatal medium spiny neurons reduce L-type Ca2+ currents and excitability via a novel PLC[beta]1-IP3- calcineurin-signaling cascade. J Neurosci 20(24):8987-8995.
33. Enjalbert A, Bockaert J (1983) Pharmacological characterization of the D2 dopamine receptor negatively coupled with adenylate cyclase in rat anterior pituitary. Mol Pharmacol 23(3):576-584.
34. Sunahara RK, et al. (1991) Cloning of the gene for a human dopamine D5 receptor with higher affinity for dopamine than D1. Nature 350(6319):614-619.
35. Van Tol HH, et al. (1991) Cloning of the gene for a human dopamine D4 receptor with high affinity for the antipsychotic clozapine. Nature 350(6319):610-614.
36. Sokoloff P, Giros B, Martres MP, Bouthenet ML, Schwartz JC (1990) Molecular cloning and characterization of a novel dopamine receptor (D3) as a target for neuroleptics. Nature 347(6289):146-151.
37. Baldassi C, et al. (2014) Fast and accurate multivariate Gaussian modeling of protein families: Predicting residue contacts and protein-interaction partners. PLoS One 9(3): e92721.
38. Shannon CE (1997) The mathematical theory of communication. 1963. MD Comput 14(4):306-317.
39. Mani R, St Onge RP, Hartman JL, 4th, Giaever G, Roth FP (2008) Defining genetic interaction. Proc Natl Acad Sci USA 105(9):3461-3466.
40. Araya CL, et al. (2012) A fundamental protein property, thermodynamic stability, revealed solely from large-scale measurements of protein function. Proc Natl Acad Sci USA 109(42):16858-16863.
41. Oliveira L, Paiva AC, Vriend G (2002) Correlated mutation analyses on very large sequence families. ChemBioChem 3(10):1010-1017.
42. Palczewski K, et al. (2000) Crystal structure of rhodopsin: A G protein-coupled receptor. Science 289(5480):739-745.
43. Ballesteros JA, et al. (2001) Activation of the beta 2-adrenergic receptor involves disruption of an ionic lock between the cytoplasmic ends of transmembrane segments 3 and 6. J Biol Chem 276(31):29171-29177.
44. Choe HW, et al. (2011) Crystal structure of metarhodopsin II. Nature 471(7340): 651-655.
45. Rasmussen SG, et al. (2011) Structure of a nanobody-stabilized active state of the β(2) adrenoceptor. Nature 469(7329):175-180.
46. Rasmussen SG, et al. (2011) Crystal structure of the β2 adrenergic receptor-Gs protein complex. Nature 477(7366):549-555.
47. Standfuss J, et al. (2011) The structural basis of agonist-induced activation in constitutively active rhodopsin. Nature 471(7340):656-660.
48. Deupi X, Standfuss J (2011) Structural insights into agonist-induced activation of G-protein-coupled receptors. Curr Opin Struct Biol 21(4):541-551.
49. Fritze O, et al. (2003) Role of the conserved NPxxY(x)5, 6F motif in the rhodopsin ground state and during activation. Proc Natl Acad Sci USA 100(5):2290-2295.
50. Chien EY, et al. (2010) Structure of the human dopamine D3 receptor in complex with a D2/D3 selective antagonist. Science 330(6007):1091-1095.
51. Wang C, et al. (2013) Structural basis for molecular recognition at serotonin receptors. Science 340(6132):610-614.
52. Vanni S, Neri M, Tavernelli I, Rothlisberger U (2009) Observation of "ionic lock" formation in molecular dynamics simulations of wild-type beta 1 and beta 2 adrenergic receptors. Biochemistry 48(22):4789-4797.
53. Trzaskowski B, et al. (2012) Action of molecular switches in GPCRs-Theoretical and experimental studies. Curr Med Chem 19(8):1090-1109.
54. Li J, Edwards PC, Burghammer M, Villa C, Schertler GF (2004) Structure of bovine rhodopsin in a trigonal crystal form. J Mol Biol 343(5):1409-1438.
55. Cherezov V, et al. (2007) High-resolution crystal structure of an engineered human beta2-adrenergic G protein-coupled receptor. Science 318(5854):1258-1265.
56. Hanson MA, et al. (2008) A specific cholesterol binding site is established by the 2.8 A structure of the human β2-adrenergic receptor. Structure 16(6):897-905.
57. Guo W, Shi L, Filizola M, Weinstein H, Javitch JA (2005) Crosstalk in G protein-coupled receptors: Changes at the transmembrane homodimer interface determine activation. Proc Natl Acad Sci USA 102(48):17495-17500.
58. Guo W, Shi L, Javitch JA (2003) The fourth transmembrane segment forms the interface of the dopamine D2 receptor homodimer. J Biol Chem 278(7):4385-4388.
59. Zocher M, Zhang C, Rasmussen SG, Kobilka BK, Müller DJ (2012) Cholesterol increases kinetic, energetic, and mechanical stability of the human β2-adrenergic receptor. Proc Natl Acad Sci USA 109(50):E3463-E3472.
60. Han Y, Moreira IS, Urizar E, Weinstein H, Javitch JA (2009) Allosteric communication between protomers of dopamine class A GPCR dimers modulates activation. Nat Chem Biol 5(9):688-695.
61. Suzek BE, Huang H, McGarvey P, Mazumder R, Wu CH (2007) UniRef: Comprehensive and non-redundant UniProt reference clusters. Bioinformatics 23(10):1282-1288.
62. Kang HJ, et al. (2014) Selectivity and evolutionary divergence of metabotropic glutamate receptors for endogenous ligands and G proteins coupled to phospholipase C or TRP channels. J Biol Chem 289(43):29961-29974.