Single Amino Acid Variation Underlies Species-Specific Sensitivity to Amphibian Skin-Derived Opioid-like Peptides

Chemistry and Biology

Volumn 22, Issue 6, 2015, Pages 764-775

  Vardy, Eyal ^a   Sassano, Maria F ^a   Rennekamp, Andrew J ^b,c   Kroeze, Wesley K ^a   Mosier, Philip D ^d   Westkaemper, Richard B ^d   Stevens, Craig W ^e   Katritch, Vsevolod ^f   Stevens, Raymond C ^f   Peterson, Randall T ^b,c   Roth, Bryan L ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^d VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^e OKLAHOMA STATE UNIVERSITY   (United States)

^f UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA NEOENDORPHIN; AMINO ACID; DELTA OPIATE RECEPTOR; DELTORPHIN; DELTORPHIN C; DELTORPHIN II; DERMORPHIN; DYNORPHIN A; DYNORPHIN B; ENDOMORPHIN 1; ENDOMORPHIN 2; ENKEPHALIN[2 DEXTRO ALANINE 4 METHYLPHENYLALANINE 5 GLYCINE]; ENKEPHALIN[2 DEXTRO ALANINE 5 DEXTRO LEUCINE]; L5 ENKEPHALIN; LEUCINE; M5 ENKEPHALIN; OPIATE AGONIST; OPIATE PEPTIDE; OPIATE RECEPTOR; SALVINORIN A; UNCLASSIFIED DRUG; XENDORPHIN; NARCOTIC ANALGESIC AGENT; OLIGOPEPTIDE; PEPTIDE;

AMPHIBIA; ANURA; ARTICLE; CONTROLLED STUDY; EMBRYO; FEMALE; FISH; HUMAN; HUMAN CELL; LAMPREY; MOLECULAR MODEL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SKIN SECRETION; AMINO ACID SEQUENCE; ANIMAL; ANIMAL BEHAVIOR; BINDING SITE; CHEMISTRY; DRUG EFFECTS; KINETICS; METABOLISM; MOLECULAR DYNAMICS; MOLECULAR GENETICS; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; SEQUENCE ALIGNMENT; SKIN; SPECIES DIFFERENCE; ZEBRA FISH;

AMPHIBIA; ANURA; MAMMALIA; PETROMYZONTIDAE; VERTEBRATA;

AMINO ACID SEQUENCE; AMPHIBIANS; ANALGESICS, OPIOID; ANIMALS; BEHAVIOR, ANIMAL; BINDING SITES; HUMANS; KINETICS; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; OLIGOPEPTIDES; OPIOID PEPTIDES; PEPTIDES; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, OPIOID; SEQUENCE ALIGNMENT; SKIN; SPECIES SPECIFICITY; ZEBRAFISH;

EID: 84934953131     PISSN: 10745521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chembiol.2015.05.012     Document Type: Article

References (66)

1. J.A. Allen, J.M. Yost, V. Setola, X. Chen, M.F. Sassano, M. Chen, S. Peterson, P.N. Yadav, X.P. Huang, and B. Feng Discovery of beta-arrestin-biased dopamine D2 ligands for probing signal transduction pathways essential for antipsychotic efficacy Proc. Natl. Acad. Sci. USA 108 2011 18488 18493
2. F.A. Alvarez, I. Rodriguez-Martin, V. Gonzalez-Nunez, E.M. de Velasco, R. Gonzalez-Sarmiento, and R.E. Rodriguez New kappa opioid receptor from zebrafish Danio rerio Neurosci. Lett. 405 2006 94 99
3. J.A. Ballesteros, and H. Weinstein Integrated methods for the construction of three-dimensional models and computational probing of structure-function relations in G protein-coupled receptors Methods Neurosci. 25 1995 366 428
4. A. Barrallo, R. Gonzalez-Sarmiento, A. Porteros, M. Garcia-Isidoro, and R.E. Rodriguez Cloning, molecular characterization, and distribution of a gene homologous to delta opioid receptor from zebrafish (Danio rerio) Biochem. Biophys. Res. Commun. 245 1998 544 548
5. A. Barrallo, R. Gonzalez-Sarmiento, F. Alvar, and R.E. Rodriguez ZFOR2, a new opioid receptor-like gene from the teleost zebrafish (Danio rerio) Brain Res. Mol. Brain Res. 84 2000 1 6
6. S. Benyhe, E. Varga, A. Borsodi, and M. Wollemann The occurrence of different kappa opioid receptors (K1 and K2) in frog (Rana esculenta) brain membranes Acta Physiol. Hung. 76 1990 291 294
7. S. Benyhe, E. Varga, J. Hepp, A. Magyar, A. Borsodi, and M. Wollemann Characterization of kappa 1 and kappa 2 opioid binding sites in frog (Rana esculenta) brain membrane preparation Neurochem. Res. 15 1990 899 904
8. 3H]ethylketocyclazocine Life Sci. 51 1992 1647 1655
9. C. Bond, K.S. LaForge, M. Tian, D. Melia, S. Zhang, L. Borg, J. Gong, J. Schluger, J.A. Strong, and S.M. Leal Single-nucleotide polymorphism in the human mu opioid receptor gene alters beta-endorphin binding and activity: possible implications for opiate addiction Proc. Natl. Acad. Sci. USA 95 1998 9608 9613
10. G. Bonner, F. Meng, and H. Akil Selectivity of mu-opioid receptor determined by interfacial residues near third extracellular loop Eur. J. Pharmacol. 403 2000 37 44
11. C.S. Bradford, E.A. Walthers, B.T. Searcy, and F.L. Moore Cloning, heterologous expression and pharmacological characterization of a kappa opioid receptor from the brain of the rough-skinned newt, Taricha granulosa J. Mol. Endocrinol. 34 2005 809 823
12. C.S. Bradford, E.A. Walthers, D.J. Stanley, M.M. Baugh, and F.L. Moore Delta and mu opioid receptors from the brain of a urodele amphibian, the rough-skinned newt Taricha granulosa: cloning, heterologous expression, and pharmacological characterization Gen. Comp. Endocrinol. 146 2006 275 290
13. C.M. Brasel, G.W. Sawyer, and C.W. Stevens A pharmacological comparison of the cloned frog and human mu opioid receptors reveals differences in opioid affinity and function Eur. J. Pharmacol. 599 2008 36 43
14. H.A. Burgess, and M. Granato Modulation of locomotor activity in larval zebrafish during light adaptation J. Exp. Biol. 210 2007 2526 2539
15. K. Chaturvedi, M. Shahrestanifar, and R.D. Howells mu Opioid receptor: role for the amino terminus as a determinant of ligand binding affinity Brain Res. Mol. Brain Res. 76 2000 64 72
16. L.S. Chervova, D.N. Lapshin, and A.A. Kamenskii Pain sensitivity of trout and analgesia caused by intranasally administered dermorphin Dokl. Akad. Nauk 338 1994 836 837
17. M.G. Darlison, F.R. Greten, R.J. Harvey, H.J. Kreienkamp, T. Stuhmer, H. Zwiers, K. Lederis, and D. Richter Opioid receptors from a lower vertebrate (Catostomus commersoni): sequence, pharmacology, coupling to a G-protein-gated inward-rectifying potassium channel (GIRK1), and evolution Proc. Natl. Acad. Sci. USA 94 1997 8214 8219
18. S. Dreborg, G. Sundstrom, T.A. Larsson, and D. Larhammar Evolution of vertebrate opioid receptors Proc. Natl. Acad. Sci. USA 105 2008 15487 15492
19. R.H. Ehrensing, G.F. Michell, and A.J. Kastin Similar antagonism of morphine analgesia by MIF-1 and naloxone in Carassius auratus Pharmacol. Biochem. Behav. 17 1982 757 761
20. V. Erspamer, P. Melchiorri, G. Falconieri-Erspamer, L. Negri, R. Corsi, C. Severini, D. Barra, M. Simmaco, and G. Kreil Deltorphins: a family of naturally occurring peptides with high affinity and selectivity for delta opioid binding sites Proc. Natl. Acad. Sci. USA 86 1989 5188 5192
21. H.D. Fabing, and J.R. Hawkins Intravenous bufotenine injection in the human being Science 123 1956 886 887
22. G. Fenalti, P.M. Giguere, V. Katritch, X.P. Huang, A.A. Thompson, V. Cherezov, B.L. Roth, and R.C. Stevens Molecular control of delta-opioid receptor signalling Nature 506 2014 191 196
23. G. Fenalti, N.A. Zatsepin, C. Betti, P. Giguere, G.W. Han, A. Ishchenko, W. Liu, K. Guillemyn, H. Zhang, and D. James Structural basis for bifunctional peptide recognition at human delta-opioid receptor Nat. Struct. Mol. Biol. 22 2015 265 268
24. M. Filizola, and L.A. Devi Grand opening of structure-guided design for novel opioids Trends Pharmacol. Sci. 34 2013 6 12
25. S. Granier, A. Manglik, A.C. Kruse, T.S. Kobilka, F.S. Thian, W.I. Weis, and B.K. Kobilka Structure of the delta-opioid receptor bound to naltrindole Nature 485 2012 400 404
26. M.D. Hillis, L.K. Ammerman, M.T. Dixon, and R.O. de Sá Ribosomal DNA and the phylogeny of frogs Herpetol. Monogr. 7 1993 118 131
27. R. Inger The development of a phylogeny of frogs Evolution 21 1967 369 384
28. G.A. Jansen, and N.M. Greene Morphine metabolism and morphine tolerance in goldfish Anesthesiology 32 1970 231 235
29. M. Jordan, A. Schallhorn, and F.M. Wurm Transfecting mammalian cells: optimization of critical parameters affecting calcium-phosphate precipitate formation Nucleic Acids Res. 24 1996 596 601
30. S.E. Jordt, and D. Julius Molecular basis for species-specific sensitivity to "hot" chili peppers Cell 108 2002 421 430
31. L.H. Lazarus, and M. Attila The toad, ugly and venomous, wears yet a precious jewel in his skin Prog. Neurobiol. 41 1993 473 507
32. L.H. Lazarus, S.D. Bryant, M. Attila, and S. Salvadori Frog skin opioid peptides: a case for environmental mimicry Environ. Health Perspect. 102 1994 648 654
33. L.H. Lazarus, S.D. Bryant, P.S. Cooper, and S. Salvadori What peptides these deltorphins be Prog. Neurobiol. 57 1999 377 420
34. A. Manglik, A.C. Kruse, T.S. Kobilka, F.S. Thian, J.M. Mathiesen, R.K. Sunahara, L. Pardo, W.I. Weis, B.K. Kobilka, and S. Granier Crystal structure of the mu-opioid receptor bound to a morphinan antagonist Nature 485 2012 321 326
35. P.C. Montecucchi, R. de Castiglione, S. Piani, L. Gozzini, and V. Erspamer Amino acid composition and sequence of dermorphin, a novel opiate-like peptide from the skin of Phyllomedusa sauvagei Int. J. Pept. Protein Res. 17 1981 275 283
36. 3H]naloxone binding in amphibian brain Eur. J. Pharmacol. 397 2000 255 262
37. 3H]-naloxone binding in amphibian spinal cord Brain Res. 884 2000 184 191
38. P. Pattee, A.E. Ilie, S. Benyhe, G. Toth, A. Borsodi, and S.R. Nagalla Cloning and characterization of Xendorphin prohormone from Xenopus laevis: a new opioid-like prohormone distinct from proenkephalin and prodynorphin J. Biol. Chem. 278 2003 53098 53104
39. M.C. Peeters, G.J. van Westen, Q. Li, and A.P. IJzerman Importance of the extracellular loops in G protein-coupled receptors for ligand recognition and receptor activation Trends Pharmacol. Sci. 32 2011 35 42
40. M.C. Pepin, S.Y. Yue, E. Roberts, C. Wahlestedt, and P. Walker Novel "restoration of function" mutagenesis strategy to identify amino acids of the delta-opioid receptor involved in ligand binding J. Biol. Chem. 272 1997 9260 9267
41. V.E. Prince, and F.B. Pickett Splitting pairs: the diverging fates of duplicated genes Nat. Rev. Genet. 3 2002 827 837
42. R.E. Rodriguez, A. Barrallo, F. Garcia-Malvar, I.J. McFadyen, R. Gonzalez-Sarmiento, and J.R. Traynor Characterization of ZFOR1, a putative delta-opioid receptor from the teleost zebrafish (Danio rerio) Neurosci. Lett. 288 2000 207 210
43. A.H. Rowe, Y. Xiao, M.P. Rowe, T.R. Cummins, and H.H. Zakon Voltage-gated sodium channel in grasshopper mice defends against bark scorpion toxin Science 342 2013 441 446
44. L.U. Sneddon Evolution of nociception in vertebrates: comparative analysis of lower vertebrates Brain Res. Brain Res. Rev. 46 2004 123 130
45. S.H. Snyder, and G.W. Pasternak Historical review: opioid receptors Trends Pharmacol. Sci. 24 2003 198 205
46. C.W. Stevens Relative analgesic potency of mu, delta and kappa opioids after spinal administration in amphibians J. Pharmacol. Exp. Ther. 276 1996 440 448
47. C.W. Stevens The evolution of vertebrate opioid receptors Front. Biosci. 14 2009 1247 1269
48. C.W. Stevens, and T.L. Yaksh Spinal action of dermorphin, an extremely potent opioid peptide from frog skin Brain Res. 385 1986 300 304
49. C.W. Stevens, and L.C. Newman Spinal administration of selective opioid antagonists in amphibians: evidence for an opioid unireceptor Life Sci. 64 1999 PL125 PL130
50. C.W. Stevens, A.J. Klopp, and J.A. Facello Analgesic potency of mu and kappa opioids after systemic administration in amphibians J. Pharmacol. Exp. Ther. 269 1994 1086 1093
51. C.W. Stevens, G. Toth, A. Borsodi, and S. Benyhe Xendorphin B1, a novel opioid-like peptide determined from a Xenopus laevis brain cDNA library, produces opioid antinociception after spinal administration in amphibians Brain Res. Bull. 71 2007 628 632
52. C.W. Stevens, C.M. Brasel, and S. Mohan Cloning and bioinformatics of amphibian mu, delta, kappa, and nociceptin opioid receptors expressed in brain tissue: evidence for opioid receptor divergence in mammals Neurosci. Lett. 419 2007 189 194
53. R. Straight, J.L. Glenn, and C.C. Snyder Antivenom activity of rattlesnake blood plasma Nature 261 1976 259 260
54. G. Sundstrom, S. Dreborg, and D. Larhammar Concomitant duplications of opioid peptide and receptor genes before the origin of jawed vertebrates PLoS One 5 2010 e10512
55. Z. Takacs, K.C. Wilhelmsen, and S. Sorota Snake alpha-neurotoxin binding site on the Egyptian cobra (Naja haje) nicotinic acetylcholine receptor is conserved Mol. Biol. Evol. 18 2001 1800 1809
56. Z. Takacs, K.C. Wilhelmsen, and S. Sorota Cobra (Naja spp.) nicotinic acetylcholine receptor exhibits resistance to Erabu sea snake (Laticauda semifasciata) short-chain alpha-neurotoxin J. Mol. Evol. 58 2004 516 526
57. C. Ulens, M. Van Boven, P. Daenens, and J. Tytgat Interaction of p-fluorofentanyl on cloned human opioid receptors and exploration of the role of Trp-318 and His-319 in mu-opioid receptor selectivity J. Pharmacol. Exp. Ther. 294 2000 1024 1033
58. E. Vardy, P.D. Mosier, K.J. Frankowski, H. Wu, V. Katritch, R.B. Westkaemper, J. Aube, R.C. Stevens, and B.L. Roth Chemotype-selective modes of action of kappa-opioid receptor agonists J. Biol. Chem. 288 2013 34470 34483
59. T.A. Vortherms, P.D. Mosier, R.B. Westkaemper, and B.L. Roth Differential helical orientations among related G protein-coupled receptors provide a novel mechanism for selectivity. Studies with salvinorin A and the kappa-opioid receptor J. Biol. Chem. 282 2007 3146 3156
60. E.A. Walthers, C.S. Bradford, and F.L. Moore Cloning, pharmacological characterization and tissue distribution of an ORL1 opioid receptor from an amphibian, the rough-skinned newt Taricha granulosa J. Mol. Endocrinol. 34 2005 247 256
61. M. Wheatley, D. Wootten, M.T. Conner, J. Simms, R. Kendrick, R.T. Logan, D.R. Poyner, and J. Barwell Lifting the lid on GPCRs: the role of extracellular loops Br. J. Pharmacol. 165 2012 1688 1703
62. K.L. White, A.P. Scopton, M.L. Rives, R.V. Bikbulatov, P.R. Polepally, P.J. Brown, T. Kenakin, J.A. Javitch, J.K. Zjawiony, and B.L. Roth Identification of novel functionally selective k-opioid receptor scaffolds Mol. Pharmacol. 85 2014 83 90
63. K.L. White, J.E. Robinson, H. Zhu, J.F. DiBerto, P.R. Polepally, J.K. Zjawiony, D.E. Nichols, C.J. Malanga, and B.L. Roth The G protein-biased kappa-opioid receptor agonist RB-64 is analgesic with a unique spectrum of activities in vivo J. Pharmacol. Exp. Ther. 352 2015 98 109
64. H. Wu, D. Wacker, M. Mileni, V. Katritch, G.W. Han, E. Vardy, W. Liu, A.A. Thompson, X.P. Huang, and F.I. Carroll Structure of the human kappa-opioid receptor in complex with JDTic Nature 485 2012 327 332
65. H. Xu, Y.F. Lu, J.S. Partilla, Q.X. Zheng, J.B. Wang, G.A. Brine, F.I. Carroll, K.C. Rice, K.X. Chen, and Z.Q. Chi Opioid peptide receptor studies, 11: involvement of Tyr148, Trp318 and His319 of the rat mu-opioid receptor in binding of mu-selective ligands Synapse 32 1999 23 28
66. F. Yan, P.D. Mosier, R.B. Westkaemper, J. Stewart, J.K. Zjawiony, T.A. Vortherms, D.J. Sheffler, and B.L. Roth Identification of the molecular mechanisms by which the diterpenoid salvinorin A binds to kappa-opioid receptors Biochemistry 44 2005 8643 8651