MOR Is Not Enough: Identification of Novel mu-Opioid Receptor Interacting Proteins Using Traditional and Modified Membrane Yeast Two-Hybrid Screens

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Petko, Jessica ^a   Justice Bitner, Stephanie ^a   Jin, Jay ^a,d   Wong, Victoria ^b,d   Kittanakom, Saranya ^b   Ferraro, Thomas N ^c   Stagljar, Igor ^b   Levenson, Robert ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DELTA OPIATE RECEPTOR; KAPPA OPIATE RECEPTOR; MORPHINE; MU OPIATE RECEPTOR; SEVEN IN ABSENTIA HOMOLOG 1; SEVEN IN ABSENTIA HOMOLOG 2; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BRAIN REGION; CELL MIGRATION; CONTROLLED STUDY; EMBRYO; FEMALE; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MODIFIED MEMBRANE YEAST TWO HYBRID SCREENING METHOD; MOUSE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; SCREENING TEST; SIGNAL TRANSDUCTION; TISSUE SPECIFICITY; TWO HYBRID SYSTEM; UBIQUITINATION;

ANALGESICS, OPIOID; ANIMALS; BRAIN; CELL LINE; FEMALE; HEK293 CELLS; HUMANS; IMMUNOPRECIPITATION; MICE; MICE, INBRED C57BL; MORPHINE; NUCLEAR PROTEINS; RECEPTORS, OPIOID, DELTA; RECEPTORS, OPIOID, KAPPA; RECEPTORS, OPIOID, MU; SIGNAL TRANSDUCTION; TWO-HYBRID SYSTEM TECHNIQUES; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION; YEASTS;

RODENTIA;

EID: 84879508959     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0067608     Document Type: Article

References (76)

1. Matthes HW, Maldonado R, Simonin F, Valverde O, Slowe S, et al. (1996) Loss of morphine-induced analgesia, reward effect and withdrawal symptoms in mice lacking the mu-opioid-receptor gene. Nature 383: 819-823.
2. Raehal KM, Bohn LM, (2005) Mu opioid receptor regulation and opiate responsiveness. Aaps J 7: E587-591.
3. von Zastrow M, Svingos A, Haberstock-Debic H, Evans C, (2003) Regulated endocytosis of opioid receptors: cellular mechanisms and proposed roles in physiological adaptation to opiate drugs. Curr Opin Neurobiol 13: 348-353.
4. Koch T, Hollt V, (2008) Role of receptor internalization in opioid tolerance and dependence. Pharmacol Ther 117: 199-206.
5. Koch T, Widera A, Bartzsch K, Schulz S, Brandenburg LO, et al. (2005) Receptor endocytosis counteracts the development of opioid tolerance. Mol Pharmacol 67: 280-287.
6. Berger AC, Whistler JL, (2011) Morphine-induced mu opioid receptor trafficking enhances reward yet prevents compulsive drug use. EMBO Mol Med 3: 385-397.
7. Finn AK, Whistler JL, (2001) Endocytosis of the mu opioid receptor reduces tolerance and a cellular hallmark of opiate withdrawal. Neuron 32: 829-839.
8. He L, Fong J, von Zastrow M, Whistler JL, (2002) Regulation of opioid receptor trafficking and morphine tolerance by receptor oligomerization. Cell 108: 271-282.
9. He L, Kim JA, Whistler JL, (2009) Biomarkers of morphine tolerance and dependence are prevented by morphine-induced endocytosis of a mutant mu-opioid receptor. FASEB J 23: 4327-4334.
10. Martini L, Whistler JL, (2007) The role of mu opioid receptor desensitization and endocytosis in morphine tolerance and dependence. Curr Opin Neurobiol 17: 556-564.
11. Whistler JL, Chuang HH, Chu P, Jan LY, von Zastrow M, (1999) Functional dissociation of mu opioid receptor signaling and endocytosis: implications for the biology of opiate tolerance and addiction. Neuron 23: 737-746.
12. Mayer BJ, (2006) Protein-protein interactions in signaling cascades. Methods Mol Biol 332: 79-99.
13. Mayer BJ, Blinov ML, Loew LM, (2009) Molecular machines or pleiomorphic ensembles: signaling complexes revisited. J Biol 8: 81.
14. Bockaert J, Perroy J, Becamel C, Marin P, Fagni L, (2010) GPCR interacting proteins (GIPs) in the nervous system: Roles in physiology and pathologies. Annu Rev Pharmacol Toxicol 50: 89-109.
15. Magalhaes AC, Dunn H, Ferguson SS, (2012) Regulation of GPCR activity, trafficking and localization by GPCR-interacting proteins. Br J Pharmacol 165: 1717-1736.
16. Maurice P, Guillaume JL, Benleulmi-Chaachoua A, Daulat AM, Kamal M, et al. (2011) GPCR-interacting proteins, major players of GPCR function. Adv Pharmacol 62: 349-380.
17. Kabbani N, Hannan MA, Levenson R, (2005) Unraveling the Dopamine Receptor Signalplex by DRIPs and DRAPs. Current Proteomics 2: 209-223.
18. Georgoussi Z, Georganta EM, Milligan G, (2012) The other side of opioid receptor signalling: regulation by protein-protein interaction. Curr Drug Targets 13: 80-102.
19. Jin J, Kittanakom S, Wong V, Reyes BA, Van Bockstaele EJ, et al. (2010) Interaction of the mu-opioid receptor with GPR177 (Wntless) inhibits Wnt secretion: potential implications for opioid dependence. BMC Neurosci 11: 33.
20. Reyes BA, Vakharia K, Ferraro TN, Levenson R, Berrettini WH, et al. (2012) Opiate agonist-induced re-distribution of Wntless, a mu-opioid receptor interacting protein, in rat striatal neurons. Exp Neurol 233: 205-213.
21. Chien CT, Bartel PL, Sternglanz R, Fields S, (1991) The two-hybrid system: a method to identify and clone genes for proteins that interact with a protein of interest. Proc Natl Acad Sci U S A 88: 9578-9582.
22. Lin R, Kabbani N, Binda A, Canfield V, Levenson R (2005) Use of the yeast two-hybrid system to detect receptor-protein interactions. In: George SR, O'Dowd BF, editors. G Protein-Coupled Receptor-Protein Interactions: John Wiley & Sons, Inc.
23. Lin R, Karpa K, Kabbani N, Goldman-Rakic P, Levenson R, (2001) Dopamine D2 and D3 receptors are linked to the actin cytoskeleton via interaction with filamin A. Proc Natl Acad Sci U S A. 98: 5258-5263.
24. Fetchko M, Stagljar I, (2004) Application of the split-ubiquitin membrane yeast two-hybrid system to investigate membrane protein interactions. Methods 32: 349-362.
25. Stagljar I, Korostensky C, Johnsson N, te Heesen S, (1998) A genetic system based on split-ubiquitin for the analysis of interactions between membrane proteins in vivo. Proc Natl Acad Sci U S A 95: 5187-5192.
26. Auerbach D, Galeuchet-Schenk B, Hottiger MO, Stagljar I, (2002) Genetic approaches to the identification of interactions between membrane proteins in yeast. J Recept Signal Transduct Res 22: 471-481.
27. Stagljar I, Fields S, (2002) Analysis of membrane protein interactions using yeast-based technologies. Trends Biochem Sci 27: 559-563.
28. De Cotiis DA, Woll MP, Fox TE, Hill RB, Levenson R, et al. (2008) Optimized expression and purification of myristoylated human neuronal calcium sensor 1 in E. coli. Protein Expr Purif 61: 103-112.
29. Studier FW, (2005) Protein production by auto-induction in high density shaking cultures. Protein Expr Purif 41: 207-234.
30. Keith DE, Murray SR, Zaki PA, Chu PC, Lissin DV, et al. (1996) Morphine activates opioid receptors without causing their rapid internalization. J Biol Chem 271: 19021-19024.
31. Li JG, Zhang F, Jin XL, Liu-Chen LY, (2003) Differential regulation of the human kappa opioid receptor by agonists: etorphine and levorphanol reduced dynorphin A- and U50,488H-induced internalization and phosphorylation. J Pharmacol Exp Ther 305: 531-540.
32. Hislop JN, Henry AG, von Zastrow M, (2011) Ubiquitination in the first cytoplasmic loop of mu-opioid receptors reveals a hierarchical mechanism of lysosomal down-regulation. J Biol Chem 286: 40193-40204.
33. Paxinos G, Franklin KBJ (2001) The Mouse Brain in Stereotaxic Coordinates. 2nd Edition.: Academic Press.
34. Abramoff MD, Magalhaes PJ, Ram SJ, (2004) Image Processing with ImageJ. Biophotonics International 11: 36-42.
35. Liu Y, Shah SV, Xiang X, Wang J, Deng ZB, et al. (2009) COP9-associated CSN5 regulates exosomal protein deubiquitination and sorting. Am J Pathol 174: 1415-1425.
36. Mueller B, Klemm EJ, Spooner E, Claessen JH, Ploegh HL, (2008) SEL1L nucleates a protein complex required for dislocation of misfolded glycoproteins. Proc Natl Acad Sci U S A 105: 12325-12330.
37. Hu G, Chung YL, Glover T, Valentine V, Look AT, et al. (1997) Characterization of human homologs of the Drosophila seven in absentia (sina) gene. Genomics 46: 103-111.
38. Kittanakom S, Chuk M, Wong V, Snyder J, Edmonds D, et al. (2009) Analysis of membrane protein complexes using the split-ubiquitin membrane yeast two-hybrid (MYTH) system. Methods Mol Biol 548: 247-271.
39. Lentze N, Auerbach D (2008) Membrane-based yeast two-hybrid system to detect protein interactions. Curr Protoc Protein Sci Chapter 19: Unit 19 17.
40. Petschnigg J, Wong V, Snider J, Stagljar I, (2012) Investigation of membrane protein interactions using the split-ubiquitin membrane yeast two-hybrid system. Methods Mol Biol 812: 225-244.
41. Snider J, Kittanakom S, Curak J, Stagljar I (2010) Split-ubiquitin based membrane yeast two-hybrid (MYTH) system: a powerful tool for identifying protein-protein interactions. J Vis Exp.
42. Hausmann G, Banziger C, Basler K, (2007) Helping Wingless take flight: how WNT proteins are secreted. Nat Rev Mol Cell Biol 8: 331-336.
43. Peretti D, Dahan N, Shimoni E, Hirschberg K, Lev S, (2008) Coordinated lipid transfer between the endoplasmic reticulum and the Golgi complex requires the VAP proteins and is essential for Golgi-mediated transport. Mol Biol Cell 19: 3871-3884.
44. Wyles JP, McMaster CR, Ridgway ND, (2002) Vesicle-associated membrane protein-associated protein-A (VAP-A) interacts with the oxysterol-binding protein to modify export from the endoplasmic reticulum. J Biol Chem 277: 29908-29918.
45. Haefliger JA, Bruzzone R, Jenkins NA, Gilbert DJ, Copeland NG, et al. (1992) Four novel members of the connexin family of gap junction proteins. Molecular cloning, expression, and chromosome mapping. J Biol Chem 267: 2057-2064.
46. Kramer JW, Post MA, Brown AM, Kirsch GE, (1998) Modulation of potassium channel gating by coexpression of Kv2.1 with regulatory Kv5.1 or Kv6.1 alpha-subunits. Am J Physiol 274: C1501-1510.
47. Talbot JN, Skifter DA, Bianchi E, Monaghan DT, Toews ML, et al. (2009) Regulation of mu opioid receptor internalization by the scaffold protein RanBPM. Neurosci Lett 466: 154-158.
48. Groer CE, Schmid CL, Jaeger AM, Bohn LM, (2011) Agonist-directed interactions with specific beta-arrestins determine mu-opioid receptor trafficking, ubiquitination, and dephosphorylation. J Biol Chem 286: 31731-31741.
49. Moriyoshi K, Iijima K, Fujii H, Ito H, Cho Y, et al. (2004) Seven in absentia homolog 1A mediates ubiquitination and degradation of group 1 metabotropic glutamate receptors. Proc Natl Acad Sci U S A 101: 8614-8619.
50. Yun S, Moller A, Chae SK, Hong WP, Bae YJ, et al. (2008) Siah proteins induce the epidermal growth factor-dependent degradation of phospholipase Cepsilon. J Biol Chem 283: 1034-1042.
51. Wheeler TC, Chin LS, Li Y, Roudabush FL, Li L, (2002) Regulation of synaptophysin degradation by mammalian homologues of seven in absentia. J Biol Chem 277: 10273-10282.
52. Szargel R, Rott R, Eyal A, Haskin J, Shani V, et al. (2009) Synphilin-1A inhibits seven in absentia homolog (SIAH) and modulates alpha-synuclein monoubiquitylation and inclusion formation. J Biol Chem 284: 11706-11716.
53. Polekhina G, House CM, Traficante N, Mackay JP, Relaix F, et al. (2002) Siah ubiquitin ligase is structurally related to TRAF and modulates TNF-alpha signaling. Nat Struct Biol 9: 68-75.
54. Liu J, Stevens J, Rote CA, Yost HJ, Hu Y, et al. (2001) Siah-1 mediates a novel beta-catenin degradation pathway linking p53 to the adenomatous polyposis coli protein. Mol Cell 7: 927-936.
55. Famulski JK, Trivedi N, Howell D, Yang Y, Tong Y, et al. (2010) Siah regulation of Pard3A controls neuronal cell adhesion during germinal zone exit. Science 330: 1834-1838.
56. Dimitrova YN, Li J, Lee YT, Rios-Esteves J, Friedman DB, et al. (2010) Direct ubiquitination of beta-catenin by Siah-1 and regulation by the exchange factor TBL1. J Biol Chem 285: 13507-13516.
57. Chaturvedi K, Bandari P, Chinen N, Howells RD, (2001) Proteasome involvement in agonist-induced down-regulation of mu and delta opioid receptors. J Biol Chem 276: 12345-12355.
58. Tanowitz M, von Zastrow M, (2003) A novel endocytic recycling signal that distinguishes the membrane trafficking of naturally occurring opioid receptors. J Biol Chem 278: 45978-45986.
59. Lorick KL, Jensen JP, Fang S, Ong AM, Hatakeyama S, et al. (1999) RING fingers mediate ubiquitin-conjugating enzyme (E2)-dependent ubiquitination. Proc Natl Acad Sci U S A 96: 11364-11369.
60. Jin J, Morse M, Frey C, Petko J, Levenson R, (2010) Expression of GPR177 (Wntless/Evi/Sprinter), a highly conserved Wnt-transport protein, in rat tissues, zebrafish embryos, and cultured human cells. Dev Dyn 239: 2426-2434.
61. Reyes AR, Levenson R, Berrettini W, Van Bockstaele EJ, (2010) Ultrastructural relationship between the mu opioid receptor and its interacting protein, GPR177, in striatal neurons. Brain Res 1358: 71-80.
62. Kabbani N, Levenson R, (2007) A proteomic approach to receptor signaling: molecular mechanisms and therapeutic implications derived from discovery of the dopamine D2 receptor signalplex. Eur J Pharmacol 572: 83-93.
63. Blugeon C, Le Crom S, Richard L, Vallat JM, Charnay P, et al. (2011) Dok4 is involved in Schwann cell myelination and axonal interaction in vitro. Glia 59: 351-362.
64. Uchida M, Enomoto A, Fukuda T, Kurokawa K, Maeda K, et al. (2006) Dok-4 regulates GDNF-dependent neurite outgrowth through downstream activation of Rap1 and mitogen-activated protein kinase. J Cell Sci 119: 3067-3077.
65. Shi L, Yue J, You Y, Yin B, Gong Y, et al. (2006) Dok5 is substrate of TrkB and TrkC receptors and involved in neurotrophin induced MAPK activation. Cell Signal 18: 1995-2003.
66. Pezet S, McMahon SB, (2006) Neurotrophins: mediators and modulators of pain. Annu Rev Neurosci 29: 507-538.
67. Pardon MC, (2010) Role of neurotrophic factors in behavioral processes: implications for the treatment of psychiatric and neurodegenerative disorders. Vitam Horm 82: 185-200.
68. Ren K, Dubner R, (2007) Pain facilitation and activity-dependent plasticity in pain modulatory circuitry: role of BDNF-TrkB signaling and NMDA receptors. Mol Neurobiol 35: 224-235.
69. Marcol W, Kotulska K, Larysz-Brysz M, Kowalik JL (2007) BDNF contributes to animal model neuropathic pain after peripheral nerve transection. Neurosurg Rev 30: 235-243; discussion 243.
70. Obata K, Noguchi K, (2006) BDNF in sensory neurons and chronic pain. Neurosci Res 55: 1-10.
71. Ghitza UE, Zhai H, Wu P, Airavaara M, Shaham Y, et al. (2010) Role of BDNF and GDNF in drug reward and relapse: a review. Neurosci Biobehav Rev 35: 157-171.
72. Choo YY, Boh BK, Lou JJ, Eng J, Leck YC, et al. (2011) Characterization of the role of COP9 signalosome in regulating cullin E3 ubiquitin ligase activity. Mol Biol Cell 22: 4706-4715.
73. Henry AG, Hislop JN, Grove J, Thorn K, Marsh M, et al. (2012) Regulation of endocytic clathrin dynamics by cargo ubiquitination. Dev Cell 23: 519-532.
74. Hu G, Zhang S, Vidal M, Baer JL, Xu T, et al. (1997) Mammalian homologs of seven in absentia regulate DCC via the ubiquitin-proteasome pathway. Genes Dev 11: 2701-2714.
75. Liao D, Lin H, Law PY, Loh HH, (2005) Mu-opioid receptors modulate the stability of dendritic spines. Proc Natl Acad Sci U S A 102: 1725-1730.
76. Eisch AJ, Barrot M, Schad CA, Self DW, Nestler EJ, (2000) Opiates inhibit neurogenesis in the adult rat hippocampus. Proc Natl Acad Sci U S A 97: 7579-7584.