Pharmacogenomics of GPCR Drug Targets

Cell

Volumn 172, Issue 1-2, 2018, Pages 41-54.e19

  Hauser, Alexander S ^a,b   Chavali, Sreenivas ^a   Masuho, Ikuo ^c   Jahn, Leonie J ^d   Martemyanov, Kirill A ^c   Gloriam, David E ^b   Babu, M Madan ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

^d Chalmers University of Technology   (Denmark)

Author keywords

clinical trial; drug response; economic burden; FDA approved drugs; GPCR; natural variation; opioid receptor; personalized medicine; pharmacogenomics; polymorphism

Indexed keywords

AMITRIPTYLINE; BIMATOPROST; BUPRENORPHINE; CANDESARTAN HEXETIL; CERULETIDE; CLOPIDOGREL; DOXAZOSIN; DYNORPHIN A; ENDOMORPHIN 1; EXENDIN 4; G PROTEIN COUPLED RECEPTOR; GOSERELIN; LIRAGLUTIDE; MELATONIN; MONTELUKAST; MORPHINE; NALOXONE; PRAMIPEXOLE; QUETIAPINE; ROPINIROLE; SALBUTAMOL; SALMETEROL; SOLIFENACIN; SUMATRIPTAN; TICAGRELOR; TIOTROPIUM BROMIDE; TOLTERODINE; TRAMADOL; TRAZODONE; UNINDEXED DRUG; PROTEIN BINDING;

ARTICLE; CONTROLLED STUDY; DRUG APPROVAL; DRUG BINDING SITE; DRUG COST; DRUG RECEPTOR BINDING; DRUG RESPONSE; DRUG STRUCTURE; DRUG TARGETING; FEMALE; FOOD AND DRUG ADMINISTRATION; GENE MUTATION; GENETIC VARIATION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PHARMACOGENOMICS; PRIORITY JOURNAL; RAT; ANTAGONISTS AND INHIBITORS; BINDING SITE; CHEMISTRY; GENETICS; HEK293 CELL LINE; METABOLISM; PHARMACOGENETIC VARIANT; PHARMACOGENETICS; PRESCRIPTION; PROCEDURES; SOFTWARE; STANDARDS;

BINDING SITES; DRUG PRESCRIPTIONS; HEK293 CELLS; HUMANS; PHARMACOGENETICS; PHARMACOGENOMIC VARIANTS; PROTEIN BINDING; RECEPTORS, G-PROTEIN-COUPLED; SOFTWARE;

EID: 85039034321     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2017.11.033     Document Type: Article

References (72)

1. Adzhubei, I., Jordan, D.M., Sunyaev, S.R., Predicting functional effect of human missense mutations using PolyPhen-2. Curr. Protoc. Hum. Genet., Chapter 7, 2013 Unit 7.20.
2. Allen, J.A., Roth, B.L., Strategies to discover unexpected targets for drugs active at G protein-coupled receptors. Annu. Rev. Pharmacol. Toxicol. 51 (2011), 117–144.
3. Auton, A., Brooks, L.D., Durbin, R.M., Garrison, E.P., Kang, H.M., Korbel, J.O., Marchini, J.L., McCarthy, S., McVean, G.A., Abecasis, G.R., 1000 Genomes Project Consortium. A global reference for human genetic variation. Nature 526 (2015), 68–74.
4. Boucrot, E., Ferreira, A.P.A., Almeida-Souza, L., Debard, S., Vallis, Y., Howard, G., Bertot, L., Sauvonnet, N., McMahon, H.T., Endophilin marks and controls a clathrin-independent endocytic pathway. Nature 517 (2015), 460–465.
5. Boyer, E.W., Management of opioid analgesic overdose. N. Engl. J. Med. 367 (2012), 146–155.
6. Chen, B., Brinkmann, K., Chen, Z., Pak, C.W., Liao, Y., Shi, S., Henry, L., Grishin, N.V., Bogdan, S., Rosen, M.K., The WAVE regulatory complex links diverse receptors to the actin cytoskeleton. Cell 156 (2014), 195–207.
7. Congreve, M., Oswald, C., Marshall, F.H., Applying structure-based drug design approaches to allosteric modulators of GPCRs. Trends Pharmacol. Sci. 38 (2017), 837–847.
8. Costa-Neto, C.M., Parreiras-E-Silva, L.T., Bouvier, M., A pluridimensional view of biased agonism. Mol. Pharmacol. 90 (2016), 587–595.
9. DataLab-EBM (2017). https://openprescribing.net/.
10. Dolfin, E., Guani, B., Lussiana, C., Mari, C., Restagno, G., Revelli, A., FSH-receptor Ala307Thr polymorphism is associated to polycystic ovary syndrome and to a higher responsiveness to exogenous FSH in Italian women. J. Assist. Reprod. Genet. 28 (2011), 925–930.
11. Dufresne, M., Seva, C., Fourmy, D., Cholecystokinin and gastrin receptors. Physiol. Rev. 86 (2006), 805–847.
12. Evans, W.E., McLeod, H.L., Pharmacogenomics—drug disposition, drug targets, and side effects. N. Engl. J. Med. 348 (2003), 538–549.
13. FDA (2014). Drugs Table of Pharmacogenomic Biomarkers in Drug Labeling, https://www.fda.gov/Drugs/ScienceResearch/ucm572698.htm.
14. Flock, T., Ravarani, C.N.J., Sun, D., Venkatakrishnan, A.J., Kayikci, M., Tate, C.G., Veprintsev, D.B., Babu, M.M., Universal allosteric mechanism for Gα activation by GPCRs. Nature 524 (2015), 173–179.
15. Flock, T., Hauser, A.S., Lund, N., Gloriam, D.E., Balaji, S., Babu, M.M., Selectivity determinants of GPCR-G-protein binding. Nature 545 (2017), 317–322.
16. Gahbauer, S., Böckmann, R.A., Membrane-mediated oligomerization of G protein coupled receptors and its implications for GPCR function. Front. Physiol., 7, 2016, 494.
17. Gallion, J., Koire, A., Katsonis, P., Schoenegge, A.-M., Bouvier, M., Lichtarge, O., Predicting phenotype from genotype: Improving accuracy through more robust experimental and computational modeling. Hum. Mutat. 38 (2017), 569–580.
18. Giacomini, K.M., Krauss, R.M., Roden, D.M., Eichelbaum, M., Hayden, M.R., Nakamura, Y., When good drugs go bad. Nature 446 (2007), 975–977.
19. Gupta, K., Donlan, J.A.C., Hopper, J.T.S., Uzdavinys, P., Landreh, M., Struwe, W.B., Drew, D., Baldwin, A.J., Stansfeld, P.J., Robinson, C.V., The role of interfacial lipids in stabilizing membrane protein oligomers. Nature 541 (2017), 421–424.
20. Hauser, A.S., Misty, A., Mathias, R.-A., Schiöth, H.B., Gloriam, D.E., Trends in GPCR drug discovery: new agents, targets and indications. Nat. Rev. Drug Disc. 16 (2017), 829–842.
21. Hollins, B., Kuravi, S., Digby, G.J., Lambert, N.A., The c-terminus of GRK3 indicates rapid dissociation of G protein heterotrimers. Cell. Signal. 21 (2009), 1015–1021.
22. Hornbeck, P.V., Zhang, B., Murray, B., Kornhauser, J.M., Latham, V., Skrzypek, E., PhosphoSitePlus, 2014: mutations, PTMs and recalibrations. Nucleic Acids Res. 43 (2015), D512–D520.
23. Huang, K.Y., Su, M.G., Kao, H.J., Hsieh, Y.C., Jhong, J.H., Cheng, K.H., Huang, H.D., Lee, T.Y., dbPTM 2016: 10-year anniversary of a resource for post-translational modification of proteins. Nucleic Acids Res. 44:D1 (2016), D435–D446.
24. Isberg, V., de Graaf, C., Bortolato, A., Cherezov, V., Katritch, V., Marshall, F.H., Mordalski, S., Pin, J.-P.P., Stevens, R.C., Vriend, G., Gloriam, D.E., Generic GPCR residue numbers—aligning topology maps while minding the gaps. Trends Pharmacol. Sci. 36 (2015), 22–31.
25. Johnson, J.A., Ethnic differences in cardiovascular drug response: Potential contribution of pharmacogenetics. Circulation 118 (2008), 1383–1393.
26. Jubb, H.C., Higueruelo, A.P., Ochoa-Montaño, B., Pitt, W.R., Ascher, D.B., Blundell, T.L., Arpeggio: A web server for calculating and visualising interatomic interactions in protein structures. J. Mol. Biol. 429 (2017), 365–371.
27. Kang, Y., Zhou, X.E., Gao, X., He, Y., Liu, W., Ishchenko, A., Barty, A., White, T.A., Yefanov, O., Han, G.W., et al. Crystal structure of rhodopsin bound to arrestin by femtosecond X-ray laser. Nature 523 (2015), 561–567.
28. Katritch, V., Fenalti, G., Abola, E.E., Roth, B.L., Cherezov, V., Stevens, R.C., Allosteric sodium in class A GPCR signaling. Trends Biochem. Sci. 39 (2014), 233–244.
29. Koscielny, G., An, P., Carvalho-Silva, D., Cham, J.A., Fumis, L., Gasparyan, R., Hasan, S., Karamanis, N., Maguire, M., Papa, E., et al. Open Targets: A platform for therapeutic target identification and validation. Nucleic Acids Res. 45 (2017), D985–D994.
30. Kukurba, K.R., Zhang, R., Li, X., Smith, K.S., Knowles, D.A., How Tan, M., Piskol, R., Lek, M., Snyder, M., Macarthur, D.G., et al. Allelic expression of deleterious protein-coding variants across human tissues. PLoS Genet., 10, 2014, 10.1371/journal.pgen.1004304 Published online May 1, 2014.
31. Lappalainen, T., Montgomery, S.B., Nica, A.C., Dermitzakis, E.T., Epistatic selection between coding and regulatory variation in human evolution and disease. Am. J. Hum. Genet. 89 (2011), 459–463.
32. Lauschke, V.M., Milani, L., Ingelman-Sundberg, M., Pharmacogenomic Biomarkers for Improved Drug Therapy-Recent Progress and Future Developments. 2017, 10.1208/s12248-017-0161-x Published online November 27, 2017.
33. Law, V., Knox, C., Djoumbou, Y., Jewison, T., Guo, A.C., Liu, Y., Maciejewski, A., Arndt, D., Wilson, M., Neveu, V., et al. DrugBank 4.0: shedding new light on drug metabolism. Nucleic Acids Res. 42 (2014), D1091–D1097.
34. Lek, M., Karczewski, K.J., Minikel, E.V., Samocha, K.E., Banks, E., Fennell, T., O'Donnell-Luria, A.H., Ware, J.S., Hill, A.J., Cummings, B.B., et al., Exome Aggregation Consortium. Analysis of protein-coding genetic variation in 60,706 humans. Nature 536 (2016), 285–291.
35. Liang, Y.-L., Khoshouei, M., Radjainia, M., Zhang, Y., Glukhova, A., Tarrasch, J., Thal, D.M., Furness, S.G.B., Christopoulos, G., Coudrat, T., et al. Phase-plate cryo-EM structure of a class B GPCR-G-protein complex. Nature 546 (2017), 118–123.
36. Liggett, S.B., Mialet-Perez, J., Thaneemit-Chen, S., Weber, S.A., Greene, S.M., Hodne, D., Nelson, B., Morrison, J., Domanski, M.J., Wagoner, L.E., et al. A polymorphism within a conserved beta(1)-adrenergic receptor motif alters cardiac function and beta-blocker response in human heart failure. Proc. Natl. Acad. Sci. USA 103 (2006), 11288–11293.
37. Masuho, I., Ostrovskaya, O., Kramer, G.M., Jones, C.D., Xie, K., Martemyanov, K.A., Distinct profiles of functional discrimination among G proteins determine the actions of G protein-coupled receptors. Sci. Signal., 8, 2015, ra123.
38. Masuho, I., Martemyanov, K.A., Lambert, N.A., Monitoring G protein activation in cells with BRET. Methods Mol. Biol. 1335 (2015), 107–113.
39. Mialet Perez, J., Rathz, D.A., Petrashevskaya, N.N., Hahn, H.S., Wagoner, L.E., Schwartz, A., Dorn, G.W., Liggett, S.B., β 1-adrenergic receptor polymorphisms confer differential function and predisposition to heart failure. Nat. Med. 9 (2003), 1300–1305.
40. Miosge, L.A., Field, M.A., Sontani, Y., Cho, V., Johnson, S., Palkova, A., Balakishnan, B., Liang, R., Zhang, Y., Lyon, S., et al. Comparison of predicted and actual consequences of missense mutations. Proc. Natl. Acad. Sci. USA 112 (2015), E5189–E5198.
41. Munk, C., Isberg, V., Mordalski, S., Harpsøe, K., Rataj, K., Hauser, A.S., Kolb, P., Bojarski, A.J., Vriend, G., Gloriam, D.E., GPCRdb: the G protein-coupled receptor database - an introduction. Br. J. Pharmacol. 173 (2016), 2195–2207.
42. Munk, C., Harpsøe, K., Hauser, A.S., Isberg, V., Gloriam, D.E., Integrating structural and mutagenesis data to elucidate GPCR ligand binding. Curr. Opin. Pharmacol. 30 (2016), 51–58.
43. Ng, P.C., Henikoff, S., SIFT: Predicting amino acid changes that affect protein function. Nucleic Acids Res. 31 (2003), 3812–3814.
44. Orman, J.S., Keating, G.M., Spotlight on buprenorphine/naloxone in the treatment of opioid dependence. CNS Drugs 23 (2009), 899–902.
45. Pándy-Szekeres, G., Munk, C., Tsonkov, T.M., Mordalski, S., Harpsøe, K., Hauser, A.S., Gloriam, D.E., GPCRdb in 2018: adding GPCR structure models and ligands. Nucleic Acids Res., 2017, 10.1093/nar/gkx1109 Published online November 16, 2017.
46. Raimondi, F., Betts, M.J., Lu, Q., Inoue, A., Gutkind, J.S., Russell, R.B., Genetic variants affecting equivalent protein family positions reflect human diversity. Sci. Rep., 7, 2017, 12771.
47. Rask-Andersen, M., Masuram, S., Schiöth, H.B., The druggable genome: Evaluation of drug targets in clinical trials suggests major shifts in molecular class and indication. Annu. Rev. Pharmacol. Toxicol. 54 (2014), 9–26.
48. Rasmussen, S.G.F., DeVree, B.T., Zou, Y., Kruse, A.C., Chung, K.Y., Kobilka, T.S., Thian, F.S., Chae, P.S., Pardon, E., Calinski, D., et al. Crystal structure of the β2 adrenergic receptor-Gs protein complex. Nature 477 (2011), 549–555.
49. Raveh, A., Cooper, A., Guy-David, L., Reuveny, E., Nonenzymatic rapid control of GIRK channel function by a G protein-coupled receptor kinase. Cell 143 (2010), 750–760.
50. Relling, M.V., Evans, W.E., Pharmacogenomics in the clinic. Nature 526 (2015), 343–350.
51. Rieck, M., Schumacher-Schuh, A.F., Altmann, V., Callegari-Jacques, S.M., Rieder, C.R.M., Hutz, M.H., Association between DRD2 and DRD3 gene polymorphisms and gastrointestinal symptoms induced by levodopa therapy in Parkinson's disease. Pharmacogenomics J., 2016.
52. Roden, D.M., George, A.L. Jr., The genetic basis of variability in drug responses. Nat. Rev. Drug Discov. 1 (2002), 37–44.
53. Ruderfer, D.M., Hamamsy, T., Lek, M., Karczewski, K.J., Kavanagh, D., Samocha, K.E., Daly, M.J., MacArthur, D.G., Fromer, M., Purcell, S.M., Exome Aggregation Consortium. Patterns of genic intolerance of rare copy number variation in 59,898 human exomes. Nat. Genet. 48 (2016), 1107–1111.
54. Santos, R., Ursu, O., Gaulton, A., Bento, A.P., Donadi, R.S., Bologa, C.G., Karlsson, A., Al-Lazikani, B., Hersey, A., Oprea, T.I., Overington, J.P., A comprehensive map of molecular drug targets. Nat. Rev. Drug Discov. 16 (2017), 19–34.
55. Savova, V., Chun, S., Sohail, M., McCole, R.B., Witwicki, R., Gai, L., Lenz, T.L., Wu, C.T., Sunyaev, S.R., Gimelbrant, A.A., Genes with monoallelic expression contribute disproportionately to genetic diversity in humans. Nat. Genet. 48 (2016), 231–237.
56. Sim, S.C., Ingelman-Sundberg, M., Pharmacogenomic biomarkers: new tools in current and future drug therapy. Trends Pharmacol. Sci. 32 (2011), 72–81.
57. Smedley, D., Haider, S., Durinck, S., Pandini, L., Provero, P., Allen, J., Arnaiz, O., Awedh, M.H., Baldock, R., Barbiera, G., et al. The BioMart community portal: an innovative alternative to large, centralized data repositories. Nucleic Acids Res. 43 (2015), W589–W598.
58. Southan, C., Sharman, J.L., Benson, H.E., Faccenda, E., Pawson, A.J., Alexander, S.P.H., Buneman, O.P., Davenport, A.P., McGrath, J.C., Peters, J.A., et al., NC-IUPHAR. The IUPHAR/BPS Guide to PHARMACOLOGY in 2016: towards curated quantitative interactions between 1300 protein targets and 6000 ligands. Nucleic Acids Res. 44:D1 (2016), D1054–D1068.
59. Sultana, J., Cutroneo, P., Trifirò G., Clinical and economic burden of adverse drug reactions. J. Pharmacol. Pharmacother. 4:Suppl 1 (2013), S73–S77.
60. The IDG Knowledge Management Center (2016). Unexplored opportunities in the druggable human genome. Nature Reviews, https://www.nature.com/nrd/posters/druggablegenome/index.html.
61. Thompson, M.D., Cole, D.E.C., Capra, V., Siminovitch, K.A., Rovati, G.E., Burnham, W.M., Rana, B.K., Pharmacogenetics of the G protein-coupled receptors. Methods Mol. Biol. 1175 (2014), 189–242.
62. Trzaskowski, B., Latek, D., Yuan, S., Ghoshdastider, U., Debinski, A., Filipek, S., Action of molecular switches in GPCRs—theoretical and experimental studies. Curr. Med. Chem. 19 (2012), 1090–1109.
63. Turner, T.N., Yi, Q., Krumm, N., Huddleston, J., Hoekzema, K., F Stessman, H.A., Doebley, A.L., Bernier, R.A., Nickerson, D.A., Eichler, E.E., denovo-db: A compendium of human de novo variants. Nucleic Acids Res. 45 (2017), D804–D811.
64. US Food and Drug Administration (2013). Clinical Pharmacogenomics: Premarket Evaluation in Early-Phase Clinical Studies and Recommendations for Labeling, https://www.fda.gov/downloads/Drugs/GuidanceComplianceRegulatoryInformation/Guidances/UCM337169.pdf.
65. van der Lee, R., Buljan, M., Lang, B., Weatheritt, R.J., Daughdrill, G.W., Dunker, A.K., Fuxreiter, M., Gough, J., Gsponer, J., Jones, D.T., et al. Classification of intrinsically disordered regions and proteins. Chem. Rev. 114 (2014), 6589–6631.
66. Venkatakrishnan, A.J., Deupi, X., Lebon, G., Tate, C.G., Schertler, G.F., Babu, M.M., Molecular signatures of G-protein-coupled receptors. Nature 494 (2013), 185–194.
67. Venkatakrishnan, A.J., Flock, T., Prado, D.E., Oates, M.E., Gough, J., Madan Babu, M., Structured and disordered facets of the GPCR fold. Curr. Opin. Struct. Biol. 27 (2014), 129–137.
68. Venkatakrishnan, A.J., Deupi, X., Lebon, G., Heydenreich, F.M., Flock, T., Miljus, T., Balaji, S., Bouvier, M., Veprintsev, D.B., Tate, C.G., et al. Diverse activation pathways in class A GPCRs converge near the G-protein-coupling region. Nature 536 (2016), 484–487.
69. Wacker, D., Wang, C., Katritch, V., Han, G.W., Huang, X.-P., Vardy, E., McCorvy, J.D., Jiang, Y., Chu, M., Siu, F.Y., et al. Structural features for functional selectivity at serotonin receptors. Science 340 (2013), 615–619.
70. Wacker, D., Stevens, R.C., Roth, B.L., How ligands illuminate GPCR molecular pharmacology. Cell 170 (2017), 414–427.
71. Ward, L.D., Kellis, M., Interpreting noncoding genetic variation in complex traits and human disease. Nat. Biotechnol. 30 (2012), 1095–1106.
72. Zhang, Y., Sun, B., Feng, D., Hu, H., Chu, M., Qu, Q., Tarrasch, J.T., Li, S., Sun Kobilka, T., Kobilka, B.K., Skiniotis, G., Cryo-EM structure of the activated GLP-1 receptor in complex with a G protein. Nature 546 (2017), 248–253.