Temperature dependent photolabeling of the human angiotensin II type 1 receptor reveals insights into its conformational landscape and its activation mechanism

Biochemical Pharmacology

Volumn 80, Issue 7, 2010, Pages 990-999

  Arsenault, Jason ^a   Cabana, Jérôme ^a   Fillion, Dany ^a   Leduc, Richard ^a   Guillemette, Gaétan ^a   Lavigne, Pierre ^a   Escher, Emanuel ^a  

^a UNIVERSITY OF SHERBROOKE   (Canada)

Author keywords

Angiotensin II; Constitutive activity; GPCR; Molecular modeling; Photolabeling

Indexed keywords

4 BENZOYL LEVO PHENYLALANINE; ANGIOTENSIN 1 RECEPTOR; ANGIOTENSIN II; ASPARAGINE; CYANOGEN BROMIDE; GLYCINE; GUANOSINE TRIPHOSPHATASE; IODINE 125; LIGAND; METHIONINE; PHENYLALANINE DERIVATIVE; PROTEIN SAR1; RECEPTOR; UNCLASSIFIED DRUG; 4-BENZOYLPHENYLALANINE; BENZOPHENONE DERIVATIVE; PHENYLALANINE; PROTEIN BINDING;

ANIMAL CELL; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; DENSITOMETRY; DRUG MECHANISM; FRAGMENTATION REACTION; MUTAGENESIS; MUTANT; NONHUMAN; NUCLEOTIDE SEQUENCE; PHOTOAFFINITY LABELING; PHOTOLYSIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; RADIOACTIVITY; TEMPERATURE DEPENDENCE; ANALOGS AND DERIVATIVES; BINDING SITE; CHEMISTRY; CONFORMATION; GENETICS; HUMAN; METABOLISM; TEMPERATURE;

ANGIOTENSIN II; BENZOPHENONES; BINDING SITES; CYANOGEN BROMIDE; HUMANS; LIGANDS; METHIONINE; MOLECULAR CONFORMATION; PHENYLALANINE; PROTEIN BINDING; RECEPTOR, ANGIOTENSIN, TYPE 1; TEMPERATURE;

EID: 77955655743     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcp.2010.06.004     Document Type: Article

References (52)

1. Cherezov V., Rosenbaum D.M., Hanson M.A., Rasmussen S.G., Thian F.S., Kobilka T.S., et al. High-resolution crystal structure of an engineered human beta2-adrenergic G protein-coupled receptor. Science 2007, 318:1258-1265.
2. Day P.W., Rasmussen S.G., Parnot C., Fung J.J., Masood A., Kobilka T.S., et al. A monoclonal antibody for G protein-coupled receptor crystallography. Nat Methods 2007, 4:927-929.
3. Scheerer P., Park J.H., Hildebrand P.W., Kim Y.J., Krauss N., Choe H.W., et al. Crystal structure of opsin in its G-protein-interacting conformation. Nature 2008, 455:497-502.
4. Cozzini P., Kellogg G.E., Spyrakis F., Abraham D.J., Costantino G., Emerson A., et al. Target flexibility: an emerging consideration in drug discovery and design. J Med Chem 2008, 51:6237-6255.
5. Kenakin T. Allosteric theory: taking therapeutic advantage of the malleable nature of GPCRs. Curr Neuropharmacol 2007, 5:149-156.
6. Leach K., Sexton P.M., Christopoulos A. Allosteric GPCR modulators: taking advantage of permissive receptor pharmacology. Trends Pharmacol Sci 2007, 28:382-389.
7. May L.T., Leach K., Sexton P.M., Christopoulos A. Allosteric modulation of G protein-coupled receptors. Annu Rev Pharmacol Toxicol 2007, 47:1-51.
8. Vauquelin G., Van Liefde I. G protein-coupled receptors: a count of 1001 conformations. Fundam Clin Pharmacol 2005, 19:45-56.
9. Kobilka B., Schertler G.F. New G-protein-coupled receptor crystal structures: insights and limitations. Trends Pharmacol Sci 2008, 29:79-83.
10. Urban J.D., Clarke W.P., von Zastrow M., Nichols D.E., Kobilka B., Weinstein H., et al. Functional selectivity and classical concepts of quantitative pharmacology. J Pharmacol Exp Ther 2007, 320:1-13.
11. de Gasparo M., Catt K.J., Inagami T., Wright J.W., Unger T. International union of pharmacology. XXIII. The angiotensin II receptors. Pharmacol Rev 2000, 52:415-472.
12. Hunyady L., Catt K.J. Pleiotropic AT1 receptor signaling pathways mediating physiological and pathogenic actions of angiotensin II. Mol Endocrinol 2006, 20:953-970.
13. Kenakin T. Functional selectivity through protean and biased agonism: who steers the ship?. Mol Pharmacol 2007, 72:1393-1401.
14. Auger-Messier M., Clement M., Lanctot P.M., Leclerc P.C., Leduc R., Escher E., et al. The constitutively active N111G-AT1 receptor for angiotensin II maintains a high affinity conformation despite being uncoupled from its cognate G protein Gq/11alpha. Endocrinology 2003, 144:5277-5284.
15. Nikiforovich G.V., Mihalik B., Catt K.J., Marshall G.R. Molecular mechanisms of constitutive activity: mutations at position 111 of the angiotensin AT1 receptor. J Pept Res 2005, 66:236-248.
16. Clement M., Cabana J., Holleran B.J., Leduc R., Guillemette G., Lavigne P., et al. Activation induces structural changes in the liganded angiotensin II type 1 receptor. J Biol Chem 2009, 284:26603-26612.
17. Arsenault J., Renaud M.P., Clement M., Fillion D., Guillemette G., Leduc R., et al. Temperature-induced ligand contact point variations of the hAT1 receptor and of the constitutively active mutant N111G-hAT1. Adv Exp Med Biol 2009, 611:339-340.
18. Ruoho A.E., Kiefer H., Roeder P.E., Singer S.J. The mechanism of photoaffinity labeling. Proc Natl Acad Sci USA 1973, 70:2567-2571.
19. Clement M., Martin S.S., Beaulieu M.E., Chamberland C., Lavigne P., Leduc R., et al. Determining the environment of the ligand binding pocket of the human angiotensin II type I (hAT1) receptor using the methionine proximity assay. J Biol Chem 2005, 280:27121-27129.
20. Clement M., Chamberland C., Perodin J., Leduc R., Guillemette G., Escher E. The active and the inactive form of the hAT1 receptor have an identical ligand-binding environment: an MPA study on a constitutively active angiotensin II receptor mutant. J Recept Signal Transduct Res 2006, 26:417-433.
21. Rihakova L., Deraet M., Auger-Messier M., Perodin J., Boucard A.A., Guillemette G., et al. Methionine proximity assay, a novel method for exploring peptide ligand-receptor interaction. J Recept Signal Transduct Res 2002, 22:297-313.
22. Perodin J., Deraet M., Auger-Messier M., Boucard A.A., Rihakova L., Beaulieu M.E., et al. Residues 293 and 294 are ligand contact points of the human angiotensin type 1 receptor. Biochemistry 2002, 41:14348-14356.
23. Saviano M., Improta R., Benedetti E., Carrozzini B., Cascarano G.L., Didierjean C., et al. Benzophenone photophore flexibility and proximity: molecular and crystal-state structure of a Bpa-containing trichogin dodecapeptide analogue. Chembiochem 2004, 5:541-544.
24. Marciniak B., Bobrowski K., Hug G.L. Quenching of triplet states of aromatic ketones by sulfur-containing amino acids in solution. Evidence for electron transfer. J Am Chem Soc 1993, 97:11937-11943.
25. Arsenault J., Renaud M.P., Clement M., Fillion D., Guillemette G., Leduc R., et al. Temperature-dependent variations of ligand-receptor contact points in hAT(1). J Pept Sci 2007, 13:575-580.
26. Wittelsberger A., Thomas B.E., Mierke D.F., Rosenblatt M. Methionine acts as a " magnet" in photoaffinity crosslinking experiments. FEBS Lett 2006, 580:1872-1876.
27. Kawamura A., Hindi S., Mihai D.M., James L., Aminova O. Binding is not enough: flexibility is needed for photocrosslinking of Lck kinase by benzophenone photoligands. Bioorg Med Chem 2008, 16:8824-8829.
28. Souto M.L., Borhan B., Nakanishi K. Low-temperature photoaffinity labeling of rhodopsin and intermediates along transduction path. Methods Enzymol 2000, 316:425-435.
29. Dong M., Miller L.J. Effects of pH and temperature on photoaffinity labeling of Family B G protein-coupled receptors. Regul Pept 2009, 158:110-115.
30. Bosse R., Servant G., Zhou L.M., Boulay G., Guillemette G., Escher E. Sar1-p-benzoylphenylalanine-angiotensin, a new photoaffinity probe for selective labeling of the type 2 angiotensin receptor. Regul Pept 1993, 44:215-223.
31. Fraker P.J., Speck J.C. Protein and cell membrane iodinations with a sparingly soluble chloroamide, 1,3,4,6-tetrachloro-3a,6a-diphrenylglycoluril. Biochem Biophys Res Commun 1978, 80:849-857.
32. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227:680-685.
33. Blanton M.P., Cohen J.B. Identifying the lipid-protein interface of the Torpedo nicotinic acetylcholine receptor: secondary structure implications. Biochemistry 1994, 33:2859-2872.
34. Okada T., Sugihara M., Bondar A.N., Elstner M., Entel P., Buss V. The retinal conformation and its environment in rhodopsin in light of a new 2.2 A crystal structure. J Mol Biol 2004, 342:571-583.
35. Shenkin P.S., Yarmush D.L., Fine R.M., Wang H.J., Levinthal C. Predicting antibody hypervariable loop conformation. I. Ensembles of random conformations for ringlike structures. Biopolymers 1987, 26:2053-2085.
36. Cornell W.D., Cieplak P., Bayly C.I., Gould I.R., Merz K.M., Ferguson D.M., et al. A second generation force field for the simulation of proteins, nucleic acids, and organic molecules (vol. 117, p. 5179, 1995). J Am Chem Soc 1996, 118:2309.
37. Spyroulias G.A., Nikolakopoulou P., Tzakos A., Gerothanassis I.P., Magafa V., Manessi-Zoupa E., et al. Comparison of the solution structures of angiotensin I & II. Implication for structure-function relationship. Eur J Biochem 2003, 270:2163-2173.
38. Charest G., Lavigne P. Simple and versatile restraints for the accurate modeling of alpha-helical coiled-coil structures of multiple strandedness, orientation and composition. Biopolymers 2006, 81:202-214.
39. 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. Meth Neurosci 1995, 25:366-428.
40. Ballesteros J.A., Shi L., Javitch J.A. Structural mimicry in G protein-coupled receptors: implications of the high-resolution structure of rhodopsin for structure-function analysis of rhodopsin-like receptors. Mol Pharmacol 2001, 60:1-19.
41. Lanctot P.M., Leclerc P.C., Clement M., Auger-Messier M., Escher E., Leduc R., et al. Importance of N-glycosylation positioning for cell-surface expression, targeting, affinity and quality control of the human AT1 receptor. Biochem J 2005, 390:367-376.
42. Lanctot P.M., Leclerc P.C., Escher E., Leduc R., Guillemette G. Role of N-glycosylation in the expression and functional properties of human AT1 receptor. Biochemistry 1999, 38:8621-8627.
43. Donald A.S. Partial deglycosylation of blood-group-specific glycoproteins. Biochem J 1980, 185:327-337.
44. Domazet I., Holleran B.J., Martin S.S., Lavigne P., Leduc R., Escher E., et al. The second transmembrane domain of the human type 1 angiotensin II receptor participates in the formation of the ligand binding pocket and undergoes integral pivoting movement during the process of receptor activation. J Biol Chem 2009, 284:11922-11929.
45. Martin S.S., Boucard A.A., Clement M., Escher E., Leduc R., Guillemette G. Analysis of the third transmembrane domain of the human type 1 angiotensin II receptor by cysteine scanning mutagenesis. J Biol Chem 2004, 279:51415-51423.
46. Domazet I., Martin S.S., Holleran B.J., Morin M.E., Lacasse P., Lavigne P., et al. The fifth transmembrane domain of angiotensin II Type 1 receptor participates in the formation of the ligand-binding pocket and undergoes a counterclockwise rotation upon receptor activation. J Biol Chem 2009, 284:31953-31961.
47. Martin S.S., Holleran B.J., Escher E., Guillemette G., Leduc R. Activation of the angiotensin II type 1 receptor leads to movement of the sixth transmembrane domain: analysis by the substituted cysteine accessibility method. Mol Pharmacol 2007, 72:182-190.
48. Shi L., Liapakis G., Xu R., Guarnieri F., Ballesteros J.A., Javitch J.A. Beta2 adrenergic receptor activation. Modulation of the proline kink in transmembrane 6 by a rotamer toggle switch. J Biol Chem 2002, 277:40989-40996.
49. Ahuja S., Smith S.O. Multiple switches in G protein-coupled receptor activation. Trends Pharmacol Sci 2009, 30:494-502.
50. Bhattacharya S., Hall S.E., Vaidehi N. Agonist-induced conformational changes in bovine rhodopsin: insight into activation of G-protein-coupled receptors. J Mol Biol 2008, 382:539-555.
51. Salom D., Lodowski D.T., Stenkamp R.E., Le Trong I., Golczak M., Jastrzebska B., et al. Crystal structure of a photoactivated deprotonated intermediate of rhodopsin. Proc Natl Acad Sci USA 2006, 103:16123-16128.
52. Park J.H., Scheerer P., Hofmann K.P., Choe H.W., Ernst O.P. Crystal structure of the ligand-free G-protein-coupled receptor opsin. Nature 2008, 454:183-187.