ELK1 transcription factor linked to dysregulated striatal mu opioid receptor signaling network and oprm1 polymorphism in human heroin abusers

Biological Psychiatry

Volumn 74, Issue 7, 2013, Pages 511-519

  Daws, Stephanie E ^a   Whittard, John D ^a   Jacobs, Michelle M ^a   Ren, Yanhua ^a   Mazloom, Amin R ^a   Caputi, Francesca F ^a   Horvath, Monika ^c,d   Keller, Eva ^d   Ma'Ayan, Avi ^a   Pan, Ying Xian ^f   Chiang, Lillian W ^e   Hurd, Yasmin L ^a,b  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c UPPSALA UNIVERSITY   (Sweden)

^d SEMMELWEIS UNIVERSITY OF MEDICINE   (Hungary)

^e MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^f PURDUE PHARMA L P   (United States)

Author keywords

Addiction; MAPK; opioid; rat; self administration; transcriptome

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; DIAMORPHINE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MORPHINE 6 ACETATE; MU OPIATE RECEPTOR; SERUM RESPONSE FACTOR; TRANSCRIPTION FACTOR ELK 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CAUDATE NUCLEUS; CELLULAR DISTRIBUTION; CHROMATIN; CONTROLLED STUDY; DESENSITIZATION; DRUG ABUSE; DRUG USE; GENE; GENE EXPRESSION; GENETIC ASSOCIATION; GENOTYPE; HUMAN; HUMAN TISSUE; INTERNALIZATION; INTRON; LASER CAPTURE MICRODISSECTION; MALE; NERVE CELL PLASTICITY; NONHUMAN; NUCLEUS ACCUMBENS; ONSET AGE; OPRM1 GENE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PUTAMEN; RAT; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; TRANSCRIPTION REGULATION;

ADDICTION; MAPK; OPIOID; RAT; SELF-ADMINISTRATION; TRANSCRIPTOME;

ANIMALS; CORPUS STRIATUM; ETS-DOMAIN PROTEIN ELK-1; FEMALE; HEROIN DEPENDENCE; HUMANS; MALE; NUCLEUS ACCUMBENS; POLYMORPHISM, GENETIC; RATS; RATS, LONG-EVANS; RECEPTORS, OPIOID, MU; SIGNAL TRANSDUCTION;

EID: 84883745879     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2013.04.012     Document Type: Article

References (80)

1. Substance Abuse and Mental Health Services Administration Results from the 2009 National Survey on Drug Use and Health: National Findings 2010 Office of Applied Studies, National Survey on Drug Use and Health Series H-32, Department of Health and Human Services Publication No. SMA 07-4293 Rockville, MD
2. G.K. Hulse, D.R. English, E. Milne, and C.D. Holman The quantification of mortality resulting from the regular use of illicit opiates Addiction 94 1999 221 229
3. H.W. Matthes, R. Maldonado, F. Simonin, O. Valverde, S. Slowe, and I. Kitchen Loss of morphine-induced analgesia, reward effect and withdrawal symptoms in mice lacking the mu-opioid-receptor gene Nature 383 1996 819 823
4. I. Sora, G. Elmer, M. Funada, J. Pieper, X.F. Li, F.S. Hall, and G.R. Uhl Mu opiate receptor gene dose effects on different morphine actions: evidence for differential in vivo mu receptor reserve Neuropsychopharmacology 25 2001 41 54
5. S.K. Sharma, M. Nirenberg, and W.A. Klee Morphine receptors as regulators of adenylate cyclase activity Proc Natl Acad Sci U S A 72 1975 590 594
6. R.A. Gross, and R.L. Macdonald Dynorphin A selectively reduces a large transient (N-type) calcium current of mouse dorsal root ganglion neurons in cell culture Proc Natl Acad Sci U S A 84 1987 5469 5473
7. M. Tallent, M.A. Dichter, G.I. Bell, and T. Reisine The cloned kappa opioid receptor couples to an N-type calcium current in undifferentiated PC-12 cells Neuroscience 63 1994 1033 1040
8. K. Fukuda, S. Kato, H. Morikawa, T. Shoda, and K. Mori Functional coupling of the delta-, mu-, and kappa-opioid receptors to mitogen-activated protein kinase and arachidonate release in Chinese hamster ovary cells J Neurochem 67 1996 1309 1316
9. E.J. Nestler Molecular mechanisms of drug addiction Neuropharmacology 47 suppl 1 2004 24 32
10. C. Luscher, and R.C. Malenka Drug-evoked synaptic plasticity in addiction: From molecular changes to circuit remodeling Neuron 69 2011 650 663
11. M.J. Christie Cellular neuroadaptations to chronic opioids: Tolerance, withdrawal and addiction Br J Pharmacol 154 2008 384 396
12. H. Haberstock-Debic, K.A. Kim, Y.J. Yu, and M. von Zastrow Morphine promotes rapid, arrestin-dependent endocytosis of mu-opioid receptors in striatal neurons J Neurosci 25 2005 7847 7857
13. M.T. Tsuang, M.J. Lyons, J.M. Meyer, T. Doyle, S.A. Eisen, and J. Goldberg Co-occurrence of abuse of different drugs in men: The role of drug-specific and shared vulnerabilities Arch Gen Psychiatry 55 1998 967 972
14. L. Bevilacqua, and D. Goldman Genes and addictions Clin Pharmacol Ther 85 2009 359 361
15. E.C. Nelson, M.T. Lynskey, A.C. Heath, N. Wray, A. Agrawal, and F.L. Shand Association of OPRD1 polymorphisms with heroin dependence in a large case-control series [published online ahead of print April 13] Addict Biol 2012
16. J. Shi, L. Hui, Y. Xu, F. Wang, W. Huang, and G. Hu Sequence variations in the mu-opioid receptor gene (OPRM1) associated with human addiction to heroin Hum Mutat 19 2002 459 460
17. V. Yuferov, D. Fussell, K.S. LaForge, D.A. Nielsen, D. Gordon, and A. Ho Redefinition of the human kappa opioid receptor gene (OPRK1) structure and association of haplotypes with opiate addiction Pharmacogenetics 14 2004 793 804
18. K. Drakenberg, A. Nikoshkov, M.C. Horvath, P. Fagergren, A. Gharibyan, and K. Saarelainen Mu opioid receptor A118G polymorphism in association with striatal opioid neuropeptide gene expression in heroin abusers Proc Natl Acad Sci U S A 103 2006 7883 7888
19. K. Befort, D. Filliol, F.M. Decaillot, C. Gaveriaux-Ruff, M.R. Hoehe, and B.L. Kieffer A single nucleotide polymorphic mutation in the human mu-opioid receptor severely impairs receptor signaling J Biol Chem 276 2001 3130 3137
20. C. Bond, K.S. LaForge, M. Tian, D. Melia, S. Zhang, and L. Borg 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 U S A 95 1998 9608 9613
21. D. Wang, J.M. Quillan, K. Winans, J.L. Lucas, and W. Sadee Single nucleotide polymorphisms in the human mu opioid receptor gene alter basal G protein coupling and calmodulin binding J Biol Chem 276 2001 34624 34630
22. Y. Zhang, D. Wang, A.D. Johnson, A.C. Papp, and W. Sadee Allelic expression imbalance of human mu opioid receptor (OPRM1) caused by variant A118G J Biol Chem 280 2005 32618 32624
23. M.R. Delgado Reward-related responses in the human striatum Ann N Y Acad Sci 1104 2007 70 88
24. S.N. Haber, K.S. Kim, P. Mailly, and R. Calzavara Reward-related cortical inputs define a large striatal region in primates that interface with associative cortical connections, providing a substrate for incentive-based learning J Neurosci 26 2006 8368 8376
25. M.S. Jog, Y. Kubota, C.I. Connolly, V. Hillegaart, and A.M. Graybiel Building neural representations of habits Science 286 1999 1745 1749
26. M. Ellgren, S.M. Spano, and Y.L. Hurd Adolescent cannabis exposure alters opiate intake and opioid limbic neuronal populations in adult rats Neuropsychopharmacology 32 2007 607 615
27. Y. Ren, J. Whittard, A. Higuera-Matas, C.V. Morris, and Y.L. Hurd Cannabidiol, a nonpsychotropic component of cannabis, inhibits cue-induced heroin seeking and normalizes discrete mesolimbic neuronal disturbances J Neurosci 29 2009 14764 14769
28. M.S. Spano, M. Ellgren, X. Wang, and Y.L. Hurd Prenatal cannabis exposure increases heroin seeking with allostatic changes in limbic enkephalin systems in adulthood Biol Psychiatry 61 2007 554 563
29. S. Dai, W.A. Corrigall, K.M. Coen, and H. Kalant Heroin self-administration by rats: Influence of dose and physical dependence Pharmacol Biochem Behav 32 1989 1009 1015
30. M.M. Jacobs, A. Okvist, M. Horvath, E. Keller, M.J. Bannon, S. Morgello, and Y.L. Hurd Dopamine receptor D1 and postsynaptic density gene variants associate with opiate abuse and striatal expression levels [published online ahead of print October 9] Mol Psychiatry 2012
31. S. Purcell, B. Neale, K. Todd-Brown, L. Thomas, M.A. Ferreira, and D. Bender PLINK: A tool set for whole-genome association and population-based linkage analyses Am J Hum Genet 81 2007 559 575
32. A. Okvist, P. Fagergren, J. Whittard, A. Garcia-Osta, K. Drakenberg, and M.C. Horvath Dysregulated postsynaptic density and endocytic zone in the amygdala of human heroin and cocaine abusers Biol Psychiatry 69 2010 245 252
33. M.D. Abramoff, P.J. Magalhaes, and S.J. Ram Image Processing with ImageJ Biophotonics International 11 2004 36 42
34. W.S. Rasband ImageJ 1997-2011 U.S. National Institutes of Health Bethesda, MD
35. G.M. Aldridge, D.M. Podrebarac, W.T. Greenough, and I.J. Weiler The use of total protein stains as loading controls: An alternative to high-abundance single-protein controls in semi-quantitative immunoblotting J Neurosci Methods 172 2008 250 254
36. M.E. Levin, J.G. Jin, R.R. Ji, J. Tong, J.D. Pomonis, and D.J. Lavery Complement activation in the peripheral nervous system following the spinal nerve ligation model of neuropathic pain Pain 137 2008 182 201
37. R.A. Irizarry, B.M. Bolstad, F. Collin, L.M. Cope, B. Hobbs, and T.P. Speed Summaries of Affymetrix GeneChip probe level data Nucleic Acids Res 31 2003 e15
38. Y. Benjamini, and Y. Hochberg Controlling the false discovery rate: A practical and powerful approach to multiple testing J Royal Stat Soc 57 1995 289 300
39. A. Lachmann, H. Xu, J. Krishnan, S.I. Berger, A.R. Mazloom, and A. Ma'ayan ChEA: Transcription factor regulation inferred from integrating genome-wide ChIP-X experiments Bioinformatics 26 2010 2438 2444
40. W.J. Kent, C.W. Sugnet, T.S. Furey, K.M. Roskin, T.H. Pringle, A.M. Zahler, and D. Haussler The human genome browser at UCSC Genome Res 12 2002 996 1006
41. G.K. Geiss, R.E. Bumgarner, B. Birditt, T. Dahl, N. Dowidar, and D.L. Dunaway Direct multiplexed measurement of gene expression with color-coded probe pairs Nat Biotechnol 26 2008 317 325
42. J.A. DiNieri, X. Wang, H. Szutorisz, S.M. Spano, J. Kaur, and P. Casaccia Maternal cannabis use alters ventral striatal dopamine D2 gene regulation in the offspring Biol Psychiatry 70 2011 763 769
43. L.M. Bohn, R.J. Lefkowitz, R.R. Gainetdinov, K. Peppel, M.G. Caron, and F.T. Lin Enhanced morphine analgesia in mice lacking beta-arrestin 2 Science 286 1999 2495 2498
44. H. Gille, M. Kortenjann, O. Thomae, C. Moomaw, C. Slaughter, M.H. Cobb, and P.E. Shaw ERK phosphorylation potentiates Elk-1-mediated ternary complex formation and transactivation EMBO J 14 1995 951 962
45. S. Impey, K. Obrietan, S.T. Wong, S. Poser, S. Yano, and G. Wayman Cross talk between ERK and PKA is required for Ca2+ stimulation of CREB-dependent transcription and ERK nuclear translocation Neuron 21 1998 869 883
46. G. Boglari, and J. Szeberenyi Nuclear translocation of p90Rsk and phosphorylation of CREB is induced by ionomycin in a Ras-independent manner in PC12 cells Acta Biol Hung 53 2002 325 334
47. K. Brami-Cherrier, J. Lavaur, C. Pages, J.S. Arthur, and J. Caboche Glutamate induces histone H3 phosphorylation but not acetylation in striatal neurons: role of mitogen- and stress-activated kinase-1 J Neurochem 101 2007 697 708
48. K. Brami-Cherrier, E. Valjent, D. Herve, J. Darragh, J.C. Corvol, and C. Pages Parsing molecular and behavioral effects of cocaine in mitogen- and stress-activated protein kinase-1-deficient mice J Neurosci 25 2005 11444 11454
49. R. Marais, J. Wynne, and R. Treisman The SRF accessory protein Elk-1 contains a growth factor-regulated transcriptional activation domain Cell 73 1993 381 393
50. H.C. Tomasiewicz, M.M. Jacobs, M.B. Wilkinson, S.P. Wilson, E.J. Nestler, and Y.L. Hurd Proenkephalin mediates the enduring effects of adolescent cannabis exposure associated with adult opiate vulnerability Biol Psychiatry 72 2012 803 810
51. F.J. Vaccarino, F.E. Bloom, and G.F. Koob Blockade of nucleus accumbens opiate receptors attenuates intravenous heroin reward in the rat Psychopharmacology (Berl) 86 1985 37 42
52. S.D. Mague, and J.A. Blendy OPRM1 SNP (A118G): Involvement in disease development, treatment response, and animal models Drug Alcohol Depend 108 2010 172 182
53. S.A. Shabalina, D.V. Zaykin, P. Gris, A.Y. Ogurtsov, J. Gauthier, and K. Shibata Expansion of the human mu-opioid receptor gene architecture: Novel functional variants Hum Mol Gen 18 2009 1037 1051
54. L. Zhang, K.S. Kendler, and X. Chen The mu-opioid receptor gene and smoking initiation and nicotine dependence Behav Brain Funct 2 2006 28
55. A. Lachmann, and A. Ma'ayan Lists2Networks: Integrated analysis of gene/protein lists BMC Bioinformatics 11 2010 87
56. J. Boros, I.J. Donaldson, A. O'Donnell, Z.A. Odrowaz, L. Zeef, and M. Lupien Elucidation of the ELK1 target gene network reveals a role in the coordinate regulation of core components of the gene regulation machinery Genome Res 19 2009 1963 1973
57. X. Zhang, D.T. Odom, S.H. Koo, M.D. Conkright, G. Canettieri, and J. Best Genome-wide analysis of cAMP-response element binding protein occupancy, phosphorylation, and target gene activation in human tissues Proc Natl Acad Sci U S A 102 2005 4459 4464
58. A. Besnard, B. Galan-Rodriguez, P. Vanhoutte, and J. Caboche Elk-1 a transcription factor with multiple facets in the brain Front Neurosci 5 2011 35
59. G.F. Koob A role for brain stress systems in addiction Neuron 59 2008 11 34
60. F. Weiss, R. Ciccocioppo, L.H. Parsons, S. Katner, X. Liu, and E.P. Zorrilla Compulsive drug-seeking behavior and relapse. Neuroadaptation, stress, and conditioning factors Ann N Y Acad Sci 937 2001 1 26
61. M. Gutierrez-Mecinas, A.F. Trollope, A. Collins, H. Morfett, S.A. Hesketh, F. Kersante, and J.M. Reul Long-lasting behavioral responses to stress involve a direct interaction of glucocorticoid receptors with ERK1/2-MSK1-Elk-1 signaling Proc Natl Acad Sci U S A 108 2011 13806 13811
62. J. Lavaur, F. Bernard, P. Trifilieff, V. Pascoli, V. Kappes, and C. Pages A TAT-DEF-Elk-1 peptide regulates the cytonuclear trafficking of Elk-1 and controls cytoskeleton dynamics J Neurosci 27 2007 14448 14458
63. S. Salinas, A. Briancon-Marjollet, G. Bossis, M.A. Lopez, M. Piechaczyk, and I. Jariel-Encontre SUMOylation regulates nucleo-cytoplasmic shuttling of Elk-1 J Cell Biol 165 2004 767 773
64. A. Besnard, N. Bouveyron, V. Kappes, V. Pascoli, C. Pages, and N. Heck Alterations of molecular and behavioral responses to cocaine by selective inhibition of Elk-1 phosphorylation J Neurosci 31 2011 14296 14307
65. S. Jenab, E.D. Festa, A. Nazarian, H.B. Wu, W.L. Sun, and R. Hazim Cocaine induction of ERK proteins in dorsal striatum of Fischer rats Brain Res Mol Brain Res 142 2005 134 138
66. E. Valjent, J.C. Corvol, C. Pages, M.J. Besson, R. Maldonado, and J. Caboche Involvement of the extracellular signal-regulated kinase cascade for cocaine-rewarding properties J Neurosci 20 2000 8701 8709
67. E. Valjent, C. Pages, M. Rogard, M.J. Besson, R. Maldonado, and J. Caboche Delta 9-tetrahydrocannabinol-induced MAPK/ERK and Elk-1 activation in vivo depends on dopaminergic transmission Eur J Neurosci 14 2001 342 352
68. C. Paratore, G. Brugnoli, H.Y. Lee, U. Suter, and L. Sommer The role of the Ets domain transcription factor Erm in modulating differentiation of neural crest stem cells Dev Biol 250 2002 168 180
69. Y. Yuasa, M. Okabe, S. Yoshikawa, K. Tabuchi, W.C. Xiong, Y. Hiromi, and H. Okano Drosophila homeodomain protein REPO controls glial differentiation by cooperating with ETS and BTB transcription factors Development 130 2003 2419 2428
70. H. Hasegawa, S. Ashigaki, M. Takamatsu, R. Suzuki-Migishima, N. Ohbayashi, and N. Itoh Laminar patterning in the developing neocortex by temporally coordinated fibroblast growth factor signaling J Neurosci 24 2004 8711 8719
71. O. Demir, N. Aysit, Z. Onder, N. Turkel, G. Ozturk, A.D. Sharrocks, and I.A. Kurnaz ETS-domain transcription factor Elk-1 mediates neuronal survival: SMN as a potential target Biochim Biophys Acta 1812 2011 652 662
72. P. Kermer, M.H. Digicaylioglu, M. Kaul, J.M. Zapata, M. Krajewska, and F. Stenner-Liewen BAG1 over-expression in brain protects against stroke Brain Pathol 13 2003 495 506
73. P. Kermer, M. Krajewska, J.M. Zapata, S. Takayama, J. Mai, S. Krajewski, and J.C. Reed Bag1 is a regulator and marker of neuronal differentiation Cell Death Differ 9 2002 405 413
74. V. Planchamp, C. Bermel, L. Tonges, T. Ostendorf, S. Kugler, and J.C. Reed BAG1 promotes axonal outgrowth and regeneration in vivo via Raf-1 and reduction of ROCK activity Brain 131 2008 2606 2619
75. T. Uemura, T. Sato, T. Aoki, A. Yamamoto, T. Okada, and R. Hirai p31 deficiency influences endoplasmic reticulum tubular morphology and cell survival Mol Cell Biol 29 2009 1869 1881
76. A. Aichem, C. Pelzer, S. Lukasiak, B. Kalveram, P.W. Sheppard, and N. Rani USE1 is a bispecific conjugating enzyme for ubiquitin and FAT10, which FAT10ylates itself in cis Nat Commun 1 2010 13
77. N. Marie, B. Aguila, and S. Allouche Tracking the opioid receptors on the way of desensitization Cell Signal 18 2006 1815 1833
78. L.M. Bohn, R.R. Gainetdinov, T.D. Sotnikova, I.O. Medvedev, R.J. Lefkowitz, L.A. Dykstra, and M.G. Caron Enhanced rewarding properties of morphine, but not cocaine, in beta(arrestin)-2 knock-out mice J Neurosci 23 2003 10265 10273
79. M. Ferrer-Alcon, R. La Harpe, and J.A. Garcia-Sevilla Decreased immunodensities of micro-opioid receptors, receptor kinases GRK 2/6 and beta-arrestin-2 in postmortem brains of opiate addicts Brain Res Mol Brain Res 121 2004 114 122
80. C. Mazzucchelli, C. Vantaggiato, A. Ciamei, S. Fasano, P. Pakhotin, and W. Krezel Knockout of ERK1 MAP kinase enhances synaptic plasticity in the striatum and facilitates striatal-mediated learning and memory Neuron 34 2002 807 820