Functional role of the c-terminal amphipathic helix 8 of olfactory receptors and other g protein-coupled receptors

International Journal of Molecular Sciences

Volumn 17, Issue 11, 2016, Pages

  Sato, Takaaki ^a   Kawasaki, Takashi ^a   Mine, Shouhei ^a   Matsumura, Hiroyoshi ^b  

^a NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

^b RITSUMEIKAN UNIVERSITY   (Japan)

Author keywords

Activation; Ca2+imaging; G protein coupled receptor; Homology model; Interaction; Olfactory receptor; Response kinetics

Indexed keywords

G PROTEIN COUPLED RECEPTOR; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANOSINE DIPHOSPHATE; GUANOSINE TRIPHOSPHATE; MUTANT PROTEIN; G PROTEIN ALPHA 16; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; OLFACTORY RECEPTOR; PROTEIN BINDING;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; CARBOXY TERMINAL SEQUENCE; DIMERIZATION; DNA HELIX; HUMAN; INTERNALIZATION; KINETICS; MODEL; MOLECULAR INTERACTION; MUTAGENESIS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; OLFACTORY RECEPTOR; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; REVIEW; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; ANIMAL; BINDING SITE; CHEMICAL PHENOMENA; CHEMISTRY; GENETICS; METABOLISM; MOLECULAR MODEL; MOUSE; MUTATION; PROTEIN DOMAIN; PROTEIN SECONDARY STRUCTURE;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; GTP-BINDING PROTEIN ALPHA SUBUNITS, GQ-G11; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MICE; MODELS, MOLECULAR; MUTATION; PROTEIN BINDING; PROTEIN DOMAINS; PROTEIN STRUCTURE, SECONDARY; RECEPTORS, ODORANT; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84996486886     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms17111930     Document Type: Review

References (47)

1. Bjarnadóttir,T.K.; Gloriam,D.E.; Hellstrand,S.H.; Kristiansson,H.; Fredriksson,R.; Schiöth,H.B. Comprehensive repertoire and phylogenetic analysis of the G protein-coupled receptors in human and mouse. Genomics 2006,88,263–273.
2. Overington,J.P.; Al-Lazikani,B.; Hopkins,A.L. How many drug targets are there? Nat. Rev. 2006,5,993–996.
3. Huang,W.; Manglik,A.; Venkatakrishnan,A.J.; Laeremans,T.; Feinberg,E.N.; Sanborn,A.L.; Kato,H.E.; Livingston,K.E.; Thorsen,T.S.; Kling,R.C.; et al. Structural insights into µ opioid receptor activation. Nature 2015,524,315–321.
4. 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 2016,536,484–487.
5. s protein complex. Nature 2011,477,549–555.
6. Kling,R.C.; Lanig,H.; Clark,T.; Gmeiner,P. Active-state models of ternary GPCR complexes: Determinants of selective receptor-G protein coupling. PLoS ONE 2013,8,e67244.
7. Kawasaki,T.; Saka,T.; Mine,S.; Mizohata,E.; Inoue,T.; Matsumura,H.; Sato,T. The N-terminal acidic residue of the cytosoloc helix 8 of an odorant receptor is responsible for different response dynamics via G protein. FEBS Lett. 2015,589,1136–1142.
8. Bruno,A.; Costantino,G.; de Fabritiis,G.; Pastor,M.; Selent,J. Membrane-sensitive conformational states of helix 8 in the metabotropic Glu2 receptor,a class C GPCR. PLoS ONE 2012,7,e42023.
9. Krishna,A.G.; Menon,S.T.; Terry,T.J.; Sakmar,T.P. Evidence that helix 8 of rhodopsin acts as a membrane-dependent conformational switch. Biochemistry 2002,41,8298–8309.
10. Kuwasako,K.; Kitamura,K.; Nagata,S.; Hikosaka,T.; Kato,J. Structure-function analysis of helix 8 of human calcitonin receptor-like receptor within the adrenomedullin 1 receptor. Peptides 2011,32,144–149.
11. Knepp,A.M.; Periole,X.; Marrink,S.J.; Sakmar,T.P.; Huber,T. Rhodopsin forms a dimer with cytoplasmic helix 8 contacts in native membranes. Biochemistry 2012,51,1819–1821.
12. 1 -adrenergic receptor that are involved in coupling the receptor to G proteins. J. Biol. Chem. 2006,281,12896–12907.
13. 2 -adrenergic G protein-coupled receptor. Science 2007,318,1258–1265.
14. Palczewski,K.; Kumasaka,T.; Hori,T.; Behnke,C.A.; Motoshima,H.; Fox,B.A.; Le Trong,I.; Teller,D.C.; Okada,T.; Stenkamp,R.E.; et al. Crystal structure of rhodopsin: A G protein-coupled receptor. Science 2000,289,739–745.
15. Fritze,O.; Filipek,S.; Kuksa,V.; Palczewski,K.; Hofmann,K.P.; Ernst,O.P. Role of the conserved NPxxY(x)5,6F motif in the rhodopsin ground state and during activation. Proc. Natl. Acad. Sci. USA 2003,100,2290–2295.
16. Hamamoto,A.; Horikawa,M.; Saho,T.; Saito,Y. Mutation of Phe318 within the NPxxY(x)(5,6)F motif in melanin-concentrating hormone receptor 1 results in an efficient signaling activity. Front. Endocrinol. 2012,3,147.
17. Buck,L.; Axel,R. A novel multigene family may encode odorant receptors: A molecular basis for odor recognition. Cell 1991,65,175–187.
18. Sali,A.; Blundell,T.L. Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 1993,234,779–815.
19. Laskowski,R.; MacArthur,M.; Moss,D.; Thornton,J. PROCHECK: A program to check the stereochemical quality of protein structures. J. Appl. Cryst. 1993,26,283–291.
20. Kaye,R.G.; Saldanha,J.W.; Lu,Z.L.; Hulme,E.C. helix 8 of the M1 muscarinic acetylcholine receptor: Scanning mutagenesis delineates a G protein recognition site. Mol. Pharmacol. 2011,79,701–709.
21. 2 adrenergic G protein-coupled receptor. Nature 2007,450,383–387.
22. Choe,H.W.; Kim,Y.J.; Park,J.H.; Morizumi,T.; Pai,E.F.; Krauss,N.; Hofmann,K.P.; Scheerer,P.; Ernst,O.P. Crystal structure of metarhodopsin II. Nature 2011,471,651–655.
23. Hamana,H.; Shou-Xin,L.; Breuils,L.; Hirono,J.; Sato,T. Heterologous functional expression system for odorant receptors. J. Neurosci. Methods 2010,185,213–220.
24. 2 -adrenergic receptor activation. Cell 2013,152,532–542.
25. Ballesteros,J.A.; Weinstein,H. Integrated methods for the construction of three-dimensional models and computational probing of structure-function relations in G protein-coupled receptors. Method Neurosci. 1995,25,366–428.
26. Kruse,A.C.; Ring,A.M.; Manglik,A.; Hu,J.; Hu,K.; Eitel,K.; Hübner,H.; Pardon,E.; Valant,C.; Sexton,P.M.; et al. Activation and allosteric modulation of a muscarinic acetylcholine receptor. Nature 2013,504,101–106.
27. Sounier,R.; Mas,C.; Steyaert,J.; Laeremans,T.; Manglik,A.; Huang,W.; Kobilka,B.K.; Déméné,H.; Granier,S. Propagation of conformational changes during µ opioid receptor activation. Nature 2015,524,375–378.
28. Ernst,O.P.; Meyer,C.K.; Marin,E.P.; Henklein,P.; Fu,W.Y.; Sakmar,T.P.; Hofmann,K.P. Mutation of the fourth cytoplasmic loop of rhodopsin affects binding of transducin subunits. J. Biol. Chem. 2000,275,1937–1943.
29. Marin,E.P.; Krishna,A.G.; Zvyaga,T.A.; Isele,J.; Siebert,F.; Sakmar,T.P. The amino terminus of the fourth cytoplasmic loop of rhodopsin modulates rhodopsin-transducin interaction. J. Biol. Chem. 2000,275,1930–1936.
30. Scheerer,P.; Park,J.H.; Hildebrand,P.W.; Kim,Y.J.; Krauß,N.; Choe,H.W.; Hofmann,K.P.; Ernst,O.P. Crystal structural of opsin in its G protein-interacting conformation. Nature 2008,455,497–502.
31. Scheerer,P.; Heck,M.; Goede,A.; Park,J.H.; Choe,H.W.; Ernst,O.P.; Hofmann,K.P.; Hildebrand,P.W. Structural and kinetic modeling of an activating helix switch in the rhodopsin-transducin interface. Proc. Natl. Acad. Sci. USA 2009,106,10660–10665.
32. Hu,J.; Wang,Y.; Zhang,X.; Lloyd,J.R.; Li,J.H.; Karpiak,J.; Costanzi,S.; Wess,J. Structural basis of G protein-coupled receptor-G protein interactions. Nat. Chem. Biol. 2010,6,541–548.
33. Katada,S.; Tanaka,M.; Touhara,K. Structural determinants for membrane trafficking and G protein selectivity of a mouse olfactory receptor. J. Neurochem. 2004,90,1453–1463.
34. i. J. Biol. Chem. 2013,288,32449–32465.
35. 2 -adrenergic receptors. Mol. Endocrinol. 2011,25,1416–1430.
36. Sato,T.; Kobayakawa,R.; Kobayakawa,K.; Emura,M.; Itohara,S.; Kawasaki,T.; Tsuboi,A.; Matsumura,H. Supersensitive odor discrimination is controlled in part by initial transient interactions between the most sensitive dorsal olfactory receptors and G proteins. Recept. Clin. Investig. 2016,3,e1117.
37. Sato,T.; Kobayakawa,R.; Kobayakawa,K.; Emura,M.; Itohara,S.; Kizumi,M.; Hamana,H.; Tsuboi,A.; Hirono,J. Supersensitive detection and discrimination of enantiomers by dorsal olfactory receptors: Evidence for hierarchical odour coding. Sci. Rep. 2015,5,14073.
38. Hamana,H.; Hirono,J.; Kizumi,M.; Sato,T. Sensitivity-dependent hierarchical receptor codes for odours. Chem. Senses 2003,28,87–104.
39. Sato,T.; Kajiwara,R.; Takashima,I.; Iijima,T. A novel method for quantifying similarities between oscillatory neural responses in wavelet time-frequency power profiles. Brain Res. 2016,1636,107–117.
40. Ishikawa,T.; Sato,T.; Shimizu,A.; de Curtis,M.; Kakei,T.; Iijima,T. Odour-driven activity in the olfactory cortex of an in vitro isolated guinea-pig whole brain with olfactory epithelium. J. Neurophysiol. 2007,97,670–679.
41. Stopfer,M.; Bhagavan,S.; Smith,B.H.; Laurent,G. Impaired odour discrimination on desynchronization of odour-encoding neural assemblies. Nature 1997,390,70–74. [PubMed]
42. Matsukawa,M.; Imada,M.; Murakami,T.; Aizawa,S.; Sato,T. Rose odour can innately counteract predator odour. Brain Res. 2011,1381,117–123.
43. Gehret,A.U.; Jones,B.W.; Tran,P.N.; Cook,L.B.; Greuber,E.K.; Hinkle,P.M. Role of helix 8 of the thyrotropin-releasing hormone receptor in phosphorylation by G protein-coupled receptor kinase. Mol. Pharmacol. 2010,77,288–297.
44. Kirchberg,K.; Kim,T.Y.; Möller,M.; Skegro,D.; Dasara Raju,G.; Granzin,J.; Büldt,G.; Schlesinger,R.; Alexiev,U. Conformational dynamics of helix 8 in the GPCR rhodopsin controls arrestin activation in the desensitization process. Proc. Natl. Acad. Sci. USA 2011,108,18690–18695.
45. Tetsuka,M.; Saito,Y.; Imai,K.; Doi,H.; Maruyama,K. The basic residues in the membrane-proximal C-terminal tail of the rat melanin-concentrating hormone receptor 1 are required for receptor function. Endocrinology 2004,145,3712–3723.
46. Huynh,J.; Thomas,W.G.; Aguilar,M.-I.; Pattenden,L.K. Role of helix 8 in G protein-coupled receptors based on structure-function studies on the type 1 angiotensin receptor. Mol. Cell. Endocrinol. 2009,302,118–127.
47. Borroto-Escuela,D.O.; Romero-Fernandez,W.; Mudó,G.; Pérez-Alea,M.; Ciruela,F.; Tarakanov,A.O.; Narvaez,M.; di Liberto,V.; Agnati,L.F.; Belluardo,N.; et al. R Fibroblast growth factor receptor 1–5-hydroxytryptamine 1A heteroreceptor complexes and their enhancement of hippocampal plasticity. Biol. Psychiatry 2012,71,84–91.