Endothelin-converting enzyme 2 differentially regulates opioid receptor activity

British Journal of Pharmacology

Volumn 172, Issue 2, 2015, Pages 704-719

  Gupta, A ^a   Fujita, W ^a   Gomes, I ^a   Bobeck, E ^a   Devi, L A ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOTHELIN CONVERTING ENZYME; ENDOTHELIN CONVERTING ENZYME 2; ENDOTHELIN CONVERTING ENZYME INHIBITOR; MU OPIATE RECEPTOR; OPIATE RECEPTOR; S 136492; UNCLASSIFIED DRUG; ASPARTIC PROTEINASE; CYCLIC AMP; ENDOTHELIN-CONVERTING ENZYME; METALLOPROTEINASE; OPIATE PEPTIDE;

ANIMAL EXPERIMENT; ANTINOCICEPTION; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME REGULATION; HETEROLOGOUS EXPRESSION; IN VITRO STUDY; IN VIVO STUDY; MALE; MICROSCOPY; MOUSE; NEUROMODULATION; NONHUMAN; SIGNAL TRANSDUCTION; TAIL FLICK TEST; THIN LAYER CHROMATOGRAPHY; AGONISTS; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CHO CELL LINE; CRICETULUS; ENDOCYTOSIS; HYDROLYSIS; METABOLISM; PH; PROTEIN TRANSPORT;

ANIMALS; ASPARTIC ACID ENDOPEPTIDASES; CHO CELLS; CRICETULUS; CYCLIC AMP; ENDOCYTOSIS; HYDROGEN-ION CONCENTRATION; HYDROLYSIS; MALE; METALLOENDOPEPTIDASES; MICE, INBRED C57BL; OPIOID PEPTIDES; PROTEIN TRANSPORT; RECEPTORS, OPIOID, MU; SIGNAL TRANSDUCTION;

EID: 84920132543     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/bph.12833     Document Type: Article

References (68)

1. Alexander SPH, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Spedding M, et al. (2013a). The Concise Guide to PHARMACOLOGY 2013/14: G protein-coupled receptors. Br J Pharmacol 170: 1459-1581.
2. Alexander SPH, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Spedding M, et al. (2013b). The Concise Guide to PHARMACOLOGY 2013/14: Enzymes. Br J Pharmacol 170: 1797-1862.
3. Alt A, Mansour A, Akil H, Medzihradsky F, Traynor JR, Woods JH, (1998). Stimulation of guanosine-5'-O-(3-[35S]thio)triphosphate binding by endogenous opioids acting at a cloned mu receptor. J Pharmacol Exp Ther 286: 282-288.
4. Cattaruzza F, Cottrell GS, Vaksman N, Bunnett NW, (2009). Endothelin-converting enzyme 1 promotes re-sensitization of neurokinin 1 receptor-dependent neurogenic inflammation. Br J Pharmacol 156: 730-739.
5. Chavkin C, Henriksen SJ, Siggins GR, Bloom FE, (1985). Selective inactivation of opioid receptors in rat hippocampus demonstrates that dynorphin-A and -B may act on mu-receptors in the CA1 region. Brain Res 331: 366-370.
6. Chipkin RE, Latranyi MZ, Iorio LC, Barnett A, (1982). Potentiation of [D-ala2]enkephalinamide analgesia in rats by thiorphan. Eur J Pharmacol 83: 283-288.
7. Cottrell GS, Padilla BE, Amadesi S, Poole DP, Murphy JE, Hardt M, et al. (2009). Endosomal endothelin-converting enzyme-1: a regulator of beta-arrestin-dependent ERK signaling. J Biol Chem 284: 22411-22425.
8. Cox BM, Christie MJ, Devi L, Toll L, Traynor JR, (2015). Challenges for opioid receptor nomenclature: IUPHAR Review 9. Br J Pharmacol 172: 317-323.
9. Cvejic S, Trapaidze N, Cyr C, Devi LA, (1996). Thr353, located within the COOH-terminal tail of the delta opiate receptor, is involved in receptor down-regulation. J Biol Chem 271: 4073-4076.
10. Davis TP, Hoyer GL, Davis P, Burks TF, (1990). Proenkephalin A-derived peptide E and its fragments alter opioid contractility in the small intestine. Eur J Pharmacol 191: 253-261.
11. Devi LA, Miller LK, (2013). Endothelin-converting enzyme 2. In:, Rawlings ND, Salvesen G, (eds). Handbook of Proteolytic Enzymes, 3rd edn. Academic Press: Waltham, MA, pp. 632-635.
12. Emoto N, Yanagisawa M, (1995). Endothelin-converting enzyme-2 is a membrane-bound, phosphoramidon-sensitive metalloprotease with acidic pH optimum. J Biol Chem 270: 15262-15268.
13. Fan SF, Shen KF, Scheideler MA, Crain SM, (1992). F11 neuroblastoma x DRG neuron hybrid cells express inhibitory mu- and delta-opioid receptors which increase voltage-dependent K + currents upon activation. Brain Res 590: 329-333.
14. Fichter KM, Flajolet M, Greengard P, Vu TQ, (2010). Kinetics of G-protein-coupled receptor endosomal trafficking pathways revealed by single quantum dots. Proc Natl Acad Sci U S A 107: 18658-18663.
15. Fricker LD, (2012), Lloyd DF, Lakshmi D, (eds). Neuropeptides and Other Bioactive Peptides: From Discovery to Function, Vol. 2. Morgan & Claypool Life Sciences: Princeton, NJ, pp. 1-107.
16. Gagnidze K, Sachchidanand, Rozenfeld R, Mezei M, Zhou MM, Devi LA, (2008). Homology modeling and site-directed mutagenesis to identify selective inhibitors of endothelin-converting enzyme-2. J Med Chem 51: 3378-3387.
17. Gaudriault G, Nouel D, Dal Farra C, Beaudet A, Vincent JP, (1997). Receptor-induced internalization of selective peptidic mu and delta opioid ligands. J Biol Chem 272: 2880-2888.
18. Gomes I, Filipovska J, Devi LA, (2003). Opioid receptor oligomerization. Detection and functional characterization of interacting receptors. Methods Mol Med 84: 157-183.
19. Gomes I, Gupta A, Filipovska J, Szeto HH, Pintar JE, Devi LA, (2004). A role for heterodimerization of mu and delta opiate receptors in enhancing morphine analgesia. Proc Nat Acad Sci USA 101: 5135-5139.
20. Gomes I, Aryal DK, Wardman JH, Gupta A, Gagnidze K, Rodriguiz RM, et al. (2013a). GPR171 is a hypothalamic G protein-coupled receptor for BigLEN, a neuropeptide involved in feeding. Proc Nat Acad Sci USA 110: 16211-16216.
21. Gomes I, Gupta A, Devi LA, (2013b). G-protein-coupled heteromers: regulation in disease. Methods Enzymol 521: 219-238.
22. Gomes I, Wardman JH, Stockton SDJ, Devi LA, (2013c), Lakshmi D, Lloyd DF, (eds). Neuropeptide Receptors, Vol. 4. Morgan & Claypool Life Sciences: New Jersey, pp. 1-153.
23. Gomes I, Fujita W, Gupta A, Saldanha SA, Negri A, Pinello CE, et al. (2013d). Identification of a μ-δ opioid receptor heteromer-biased agonist with antinociceptive activity. Proc Natl Acad Sci U S A 110: 12072-12077.
24. Grunfelder CG, Engstler M, Weise F, Schwarz H, Stierhof YD, Morgan GW, et al. (2003). Endocytosis of a glycosylphosphatidylinositol-anchored protein via clathrin-coated vesicles, sorting by default in endosomes, and exocytosis via RAB11-positive carriers. Mol Biol Cell 14: 2029-2040.
25. Gupta A, Decaillot FM, Gomes I, Tkalych O, Heimann AS, Ferro ES, et al. (2007). Conformation state-sensitive antibodies to G-protein-coupled receptors. J Biol Chem 282: 5116-5124.
26. Gupta A, Rozenfeld R, Gomes I, Raehal KM, Decaillot FM, Bohn LM, et al. (2008). Post-activation-mediated changes in opioid receptors detected by N-terminal antibodies. J Biol Chem 283: 10735-10744.
27. Gupta A, Gomes I, Wardman J, Devi LA, (2014). Opioid receptor function is regulated by post-endocytic peptide processing. J Biol Chem 289: 19613-19626.
28. Hansen SH, Sandvig K, van Deurs B, (1991). The preendosomal compartment comprises distinct coated and noncoated endocytic vesicle populations. J Cell Biol 113: 731-741.
29. Hanyaloglu AC, von Zastrow M, (2008). Regulation of GPCRs by endocytic membrane trafficking and its potential implications. Annu Rev Pharmacol Toxicol 48: 537-568.
30. Hasdemir B, Mahajan S, Bunnett NW, Liao M, Bhargava A, (2012). Endothelin-converting enzyme-1 actions determine differential trafficking and signaling of corticotropin-releasing factor receptor 1 at high agonist concentrations. Mol Endocrinol 26: 681-695.
31. Ippoliti R, Ginobbi P, Lendaro E, D'Agostino I, Ombres D, Benedetti PA, et al. (1998). The effect of monensin and chloroquine on the endocytosis and toxicity of chimeric toxins. Cell Mol Life Sci 54: 866-875.
32. Jean-Alphonse F, Bowersox S, Chen S, Beard G, Puthenveedu MA, Hanyaloglu AC, (2014). Spatially restricted G protein-coupled receptor activity via divergent endocytic compartments. J Biol Chem 289: 3960-3977.
33. Jow F, He L, Kramer A, Hinson J, Bowlby MR, Dunlop J, et al. (2006). Validation of DRG-like F11 cells for evaluation of KCNQ/M-channel modulators. Assay Drug Dev Technol 4: 49-56.
34. Kilkenny C, Browne W, Cuthill IC, Emerson M, Altman DG, (2010). Animal research: reporting in vivo experiments: the ARRIVE guidelines. Br J Pharmacol 160: 1577-1579.
35. Kukkola PJ, Savage P, Sakane Y, Berry JC, Bilci NA, Ghai RD, et al. (1995). Differential structure-activity relationships of phosphoramidon analogues for inhibition of three metalloproteases: endothelin-converting enzyme, neutral endopeptidase, and angiotensin-converting enzyme. J Cardiovasc Pharmacol 26: S65-S68.
36. Law IK, Murphy JE, Bakirtzi K, Bunnett NW, Pothoulakis C, (2012). Neurotensin-induced proinflammatory signaling in human colonocytes is regulated by beta-arrestins and endothelin-converting enzyme-1-dependent endocytosis and resensitization of neurotensin receptor 1. J Biol Chem 287: 15066-15075.
37. Mansour A, Hoversten MT, Taylor LP, Watson SJ, Akil H, (1995). The cloned mu, delta and kappa receptors and their endogenous ligands: evidence for two opioid peptide recognition cores. Brain Res 700: 89-98.
38. McGrath J, Drummond G, McLachlan E, Kilkenny C, Wainwright C, (2010). Guidelines for reporting experiments involving animals: the ARRIVE guidelines. Br J Pharmacol 160: 1573-1576.
39. Mellman I, Fuchs R, Helenius A, (1986). Acidification of the endocytic and exocytic pathways. Annu Rev Biochem 55: 663-700.
40. Miller LK, Hou X, Rodriguiz RM, Gagnidze K, Sweedler JV, Wetsel WC, et al. (2011). Mice deficient in endothelin-converting enzyme-2 exhibit abnormal responses to morphine and altered peptide levels in the spinal cord. J Neurochem 119: 1074-1085.
41. Mittal N, Roberts K, Pal K, Bentolila LA, Fultz E, Minasyan A, et al. (2013). Select G-protein-coupled receptors modulate agonist-induced signaling via a ROCK, LIMK, and beta-arrestin 1 pathway. Cell Rep 5: 1010-1021.
42. Mizuno K, Minamino N, Kangawa K, Matsuo H, (1980a). A new endogenous opioid peptide from bovine adrenal medulla: isolation and amino acid sequence of a dodecapeptide (BAM-12P). Biochem Biophys Res Commun 95: 1482-1488.
43. Mizuno K, Minamino N, Kangawa K, Matsuo H, (1980b). A new family of endogenous 'big' Met-enkephalins from bovine adrenal medulla: purification and structure of docosa- (BAM-22P) and eicosapeptide (BAM-20P) with very potent opiate activity. Biochem Biophys Res Commun 97: 1283-1290.
44. Mzhavia N, Pan H, Che FY, Fricker LD, Devi LA, (2003). Characterization of endothelin-converting enzyme-2. Implication for a role in the nonclassical processing of regulatory peptides. J Biol Chem 278: 14704-14711.
45. Ouimet T, Orng SV, Poras H, Gagnidze K, Devi LA, Fournie-Zaluski MC, et al. (2010). Identification of an endothelin-converting enzyme-2-specific fluorigenic substrate and development of an in vitro and ex vivo enzymatic assay. J Biol Chem 285: 34390-34400.
46. Pacheco-Quinto J, Eckman EA, (2013). Endothelin-converting enzymes degrade intracellular beta-amyloid produced within the endosomal/lysosomal pathway and autophagosomes. J Biol Chem 288: 5606-5615.
47. Padilla BE, Cottrell GS, Roosterman D, Pikios S, Muller L, Steinhoff M, et al. (2007). Endothelin-converting enzyme-1 regulates endosomal sorting of calcitonin receptor-like receptor and beta-arrestins. J Cell Biol 179: 981-997.
48. Pasternak GW, (2011). The opiate receptors. In:, Pasternak GW, (ed.). The Receptors, Vol. 23. Humana Press: New York, pp. 1-528.
49. Pawson AJ, Sharman JL, Benson HE, Faccenda E, Alexander SP, Buneman OP, Davenport AP, McGrath JC, Peters JA, Southan C, Spedding M, Yu W, Harmar AJ,; NC-IUPHAR. (2014). The IUPHAR/BPS Guide to PHARMACOLOGY: an expert-driven knowledgebase of drug targets and their ligands. Nucl Acids Res 42 (Database Issue): D1098-1106.
50. Quirion R, Pert CB, (1981). Dynorphins: similar relative potencies on mu, delta- and kappa-opiate receptors. Eur J Pharmacol 76: 467-468.
51. Roman-Vendrell C, Yu YJ, Yudowski GA, (2012). Fast modulation of mu-opioid receptor (MOR) recycling is mediated by receptor agonists. J Biol Chem 287: 14782-14791.
52. Roosterman D, Cottrell GS, Padilla BE, Muller L, Eckman CB, Bunnett NW, et al. (2007). Endothelin-converting enzyme 1 degrades neuropeptides in endosomes to control receptor recycling. Proc Nat Acad Sci USA 104: 11838-11843.
53. Rozenfeld R, Devi LA, (2008). Regulation of CB1 cannabinoid receptor trafficking by the adaptor protein AP-3. FASEB J 22: 2311-2322.
54. Sanchez-Blazquez P, Chang JK, Garzon J, Lee NM, (1984). Dynorphin B-29: chemical synthesis and pharmacological properties in opioid systems in vitro. Neuropeptides 4: 369-374.
55. Schulz R, Wuster M, Herz A, (1984). Receptor preference of dynorphin A fragments in the mouse vas deferens determined by different techniques. J Pharmacol Exp Ther 230: 200-204.
56. Schulz R, Sakane Y, Berry C, Ghai R, (1991). Characterisation of neutral endopeptidase 3.4.24.11 (NEP) in the kidney: comparison between normotensive, genetically hypertensive and experimentally hypertensive rats. J Enzyme Inhib 4: 347-358.
57. Shirotani K, Tsubuki S, Iwata N, Takaki Y, Harigaya W, Maruyama K, et al. (2001). Neprilysin degrades both amyloid beta peptides 1-40 and 1-42 most rapidly and efficiently among thiorphan- and phosphoramidon-sensitive endopeptidases. J Biol Chem 276: 21895-21901.
58. Song B, Marvizon JC, (2003). Peptidases prevent mu-opioid receptor internalization in dorsal horn neurons by endogenously released opioids. J Neurosci 23: 1847-1858.
59. Stevens CW, Sangha S, Ogg BG, (1995). Analgesia produced by immobilization stress and an enkephalinase inhibitor in amphibians. Pharmacol Biochem Behav 51: 675-680.
60. Stoorvogel W, Oorschot V, Geuze HJ, (1996). A novel class of clathrin-coated vesicles budding from endosomes. J Cell Biol 132: 21-33.
61. Trapaidze N, Keith DE, Cvejic S, Evans CJ, Devi LA, (1996). Sequestration of the delta opioid receptor. Role of the C terminus in agonist-mediated internalization. J Biol Chem 271: 29279-29285.
62. Trapaidze N, Gomes I, Bansinath M, Devi LA, (2000). Recycling and resensitization of delta opioid receptors. DNA Cell Biol 19: 195-204.
63. Turner AJ, Murphy LJ, (1996). Molecular pharmacology of endothelin converting enzymes. Biochem Pharmacol 51: 91-102.
64. Vermeirssen V, Van Camp J, Verstraete W, (2002). Optimisation and validation of an angiotensin-converting enzyme inhibition assay for the screening of bioactive peptides. J Biochem Biophys Methods 51: 75-87.
65. Williams JT, Ingram SL, Henderson G, Chavkin C, von Zastrow M, Schulz S, et al. (2013). Regulation of mu-opioid receptors: desensitization, phosphorylation, internalization, and tolerance. Pharmacol Rev 65: 223-254.
66. Yanagisawa H, Hammer RE, Richardson JA, Emoto N, Williams SC, Takeda S, et al. (2000). Disruption of ECE-1 and ECE-2 reveals a role for endothelin-converting enzyme-2 in murine cardiac development. J Clin Invest 105: 1373-1382.
67. von Zastrow M, Williams JT, (2012). Modulating neuromodulation by receptor membrane traffic in the endocytic pathway. Neuron 76: 22-32.
68. Zhao P, Canals M, Murphy JE, Klingler D, Eriksson EM, Pelayo JC, et al. (2013). Agonist-biased trafficking of somatostatin receptor 2A in enteric neurons. J Biol Chem 288: 25689-25700.