Antagonism of sigma-1 receptors blocks compulsive-like eating

Neuropsychopharmacology

Volumn 37, Issue 12, 2012, Pages 2593-2604

  Cottone, Pietro ^a   Wang, Xiaofan ^a   Park, Jin Won ^a   Valenza, Marta ^a,b   Blasio, Angelo ^a,c   Kwak, Jina ^a   Iyer, Malliga R ^d   Steardo, Luca ^c   Rice, Kenner C ^d   Hayashi, Teruo ^d   Sabino, Valentina ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF BARI MEDICAL SCHOOL   (Italy)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

^d NATIONAL INSTITUTE ON DRUG ABUSE   (United States)

Author keywords

addiction; binge eating disorder; eating disorders; food intake; palatability; risk taking behavior

Indexed keywords

ANOREXIGENIC AGENT; BD 1063; MESSENGER RNA; OPIATE ANTAGONIST; SIGMA 1 OPIATE RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTERIOR CINGULATE; ARTICLE; BINGE EATING DISORDER; CONTROLLED STUDY; DIET; DOSE RESPONSE; DRUG ANTAGONISM; DRUG EFFECT; DRUG MECHANISM; EXPERIMENTAL TEST; INSTRUMENTAL CONDITIONING; MALE; MOTOR ACTIVITY; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

ANIMALS; BINGE-EATING DISORDER; BLOTTING, WESTERN; CONDITIONING, OPERANT; DOSE-RESPONSE RELATIONSHIP, DRUG; EMOTIONS; MALE; MOTIVATION; MOTOR ACTIVITY; PIPERAZINES; RATS; RATS, WISTAR; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, SIGMA; RISK-TAKING; RNA, MESSENGER; RNA, SMALL INTERFERING;

EID: 84867572610     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2012.89     Document Type: Article

References (86)

1. Akritas MG (1990). The rank transform method in some two-factor designs. J Am Statist Assoc 85: 73-78.
2. APA (2000). Diagnostic and Statistical Manual of Mental Disorders (4th ed.FText Revision. American Psychiatric Association: Washington, DC.
3. Avena NM, Rada P, Hoebel BG (2008). Evidence for sugar addiction: behavioral and neurochemical effects of intermittent, excessive sugar intake. Neurosci Biobehav Rev 32: 20-39.
4. Aydar E, Palmer CP, Klyachko VA, Jackson MB (2002). The sigma receptor as a ligand-regulated auxiliary potassium channel subunit. Neuron 34: 399-410.
5. Belin D, Mar AC, Dalley JW, Robbins TW, Everitt BJ (2008). High impulsivity predicts the switch to compulsive cocaine-taking. Science 320: 1352-1355.
6. Blasio A, Narayan AR, Kaminski BJ, Steardo L, Sabino V, Cottone P (2012). A modified adjusting delay task to assess impulsive choice between isocaloric reinforcers in non-deprived male rats: effects of 5-HT(2A/C) and 5-HT (1A) receptor agonists. Psychopharmacology (Berl) 219: 377-386.
7. Boeka AG, Lokken KL (2011). Prefrontal systems involvement in binge eating. Eating Weight Disord 16: e121-e126.
8. Brammer MK, Gilmore DL, Matsumoto RR (2006). Interactions between 3,4-methylenedioxymethamphetamine and sigma1 receptors. Eur J Pharmacol 553: 141-145.
9. Colorado RA, Shumake J, Conejo NM, Gonzalez-Pardo H, Gonzalez-Lima F (2006). Effects of maternal separation, early handling, and standard facility rearing on orienting and impulsive behavior of adolescent rats. Behav Process 71: 51-58.
10. Cooper SJ (2004). Endocannabinoids and food consumption: comparisons with benzodiazepine and opioid palatabilitydependent appetite. Eur J Pharmacol 500: 37-49.
11. Corwin RL (2004). Binge-type eating induced by limited access in rats does not require energy restriction on the previous day. Appetite 42: 139-142.
12. Corwin RL (2006). Bingeing rats: a model of intermittent excessive behavior? Appetite 46: 11-15.
13. Corwin RL, Avena NM, Boggiano MM (2011). Feeding and reward: perspectives from three rat models of binge eating. Physiol Behav 104: 87-97.
14. Corwin RL, Buda-Levin A (2004). Behavioral models of binge-type eating. Physiol Behav 82: 123-130.
15. Corwin RL, Grigson PS (2009). Symposium overviewFfood addiction: fact or fiction? J Nutr 139: 617-619.
16. Cottone P, Sabino V, Nagy TR, Coscina DV, Zorrilla EP (2007a). Feeding microstructure in diet-induced obesity susceptible vs resistant rats: central effects of urocortin 2. J Physiol 583(Part 2): 487-504.
17. Cottone P, Sabino V, Roberto M, Bajo M, Pockros L, Frihauf JB et al (2009a). CRF system recruitment mediates dark side of compulsive eating. Proc Natl Acad Sci USA 106: 20016-20020.
18. Cottone P, Sabino V, Steardo L, Zorrilla EP (2007b). FG 7142 specifically reduces meal size and the rate and regularity of sustained feeding in female rats: evidence that benzodiazepine inverse agonists reduce food palatability. Neuropsychopharmacology 32: 1069-1081.
19. Cottone P, Sabino V, Steardo L, Zorrilla EP (2008a). Intermittent access to preferred food reduces the reinforcing efficacy of chow in rats. Am J Physiol 295: R1066-R1076.
20. Cottone P, Sabino V, Steardo L, Zorrilla EP (2008b). Opioiddependent anticipatory negative contrast and binge-like eating in rats with limited access to highly preferred food. Neuropsychopharmacology 33: 524-535.
21. Cottone P, Sabino V, Steardo L, Zorrilla EP (2009b). Consummatory, anxiety-related and metabolic adaptations in female rats with alternating access to preferred food. Psychoneuroendocrinology 34: 38-49.
22. Davis JF, Loos M, Di Sebastiano AR, Brown JL, Lehman MN, Coolen LM (2010). Lesions of the medial prefrontal cortex cause maladaptive sexual behavior in male rats. Biol Psychiatry 67: 1199-1204.
23. de Costa BR, He XS, Linders JT, Dominguez C, Gu ZQ, Williams W et al (1993). Synthesis and evaluation of conformationally restricted N-[2-(3,4-dichlorophenyl)ethyl]-N-methyl-2-(1-pyrrolidinyl) ethylamines at sigma receptors. 2. Piperazines, bicyclic amines, bridged bicyclic amines, and miscellaneous compounds. J Med Chem 36: 2311-2320.
24. Dong LY, Cheng ZX, Fu YM, Wang ZM, Zhu YH, Sun JL et al (2007). Neurosteroid dehydroepiandrosterone sulfate enhances spontaneous glutamate release in rat prelimbic cortex through activation of dopamine D1 and sigma-1 receptor. Neuropharmacology 52: 966-974.
25. Dong Y, Fu YM, Sun JL, Zhu YH, Sun FY, Zheng P (2005). Neurosteroid enhances glutamate release in rat prelimbic cortex via activation of alpha1-adrenergic and sigma1 receptors. Cell Mol Life Sci 62: 1003-1014.
26. Fontanilla D, Johannessen M, Hajipour AR, Cozzi NV, Jackson MB, Ruoho AE (2009). The hallucinogen N,N-dimethyltryptamine (DMT) is an endogenous sigma-1 receptor regulator. Science 323: 934-937.
27. Fournier ML, Paulson A, Pavelka N, Mosley AL, Gaudenz K, Bradford WD et al (2010). Delayed correlation of mRNA and protein expression in rapamycin-treated cells and a role for Ggc1 in cellular sensitivity to rapamycin. Mol Cell Proteomics 9: 271-284.
28. Garces-Ramirez L, Green JL, Hiranita T, Kopajtic TA, Mereu M, Thomas AM et al (2011). Sigma receptor agonists: receptor binding and effects on mesolimbic dopamine neurotransmission assessed by microdialysis. Biol Psychiatry 69: 208-217.
29. Greenbaum D, Colangelo C, Williams K, Gerstein M (2003). Comparing protein abundance and mRNA expression levels on a genomic scale. Genome Biol 4: 117.
30. Gundlach AL, Largent BL, Snyder SH (1986). Autoradiographic localization of sigma receptor binding sites in guinea pig and rat central nervous system with (+)3H-3-(3-hydroxyphenyl)-N-(1-propyl)piperidine. J Neurosci 6: 1757-1770.
31. Hanner M, Moebius FF, Flandorfer A, Knaus HG, Striessnig J, Kempner E et al (1996). Purification, molecular cloning, and expression of the mammalian sigma1-binding site. Proc Natl Acad Sci USA 93: 8072-8077.
32. Hartz SM, Ben-Shahar Y, Tyler M (2001). Logistic growth curve analysis in associative learning data. Anim Cogn 3: 185-189.
33. Hayashi T, Su TP (2003). Intracellular dynamics of sigma-1 receptors (sigma binding sites) in NG108-15 cells. J Pharmacol Exp Ther 306: 726-733.
34. Hayashi T, Su TP (2007). Sigma-1 receptor chaperones at the ER-mitochondrion interface regulate Ca(2+) signaling and cell survival. Cell 131: 596-610.
35. Hayashi T, Su TP (2008). An update on the development of drugs for neuropsychiatric disorders: focusing on the sigma 1 receptor ligand. Expert Opin Therap Targets 12: 45-58.
36. Hayashi T, Tsai SY, Mori T, Fujimoto M, Su TP (2011). Targeting ligand-operated chaperone sigma-1 receptors in the treatment of neuropsychiatric disorders. Expert Opin Therap Targets 15: 557-577.
37. Hellewell SB, Bowen WD (1990). A sigma-like binding site in rat pheochromocytoma (PC12) cells: decreased affinity for (+)-benzomorphans and lower molecular weight suggest a different sigma receptor form from that of guinea pig brain. Brain Res 527: 244-253.
38. Herrera Y, Katnik C, Rodriguez JD, Hall AA, Willing A, Pennypacker KR et al (2008). Sigma-1 receptor modulation of acid-sensing ion channel a (ASIC1a) and ASIC1a-induced Ca2+ influx in rat cortical neurons. J Pharmacol Exp Ther 327: 491-502.
39. Heyne A, Kiesselbach C, Sahun I, McDonald J, Gaiffi M, Dierssen M et al (2009). An animal model of compulsive food-taking behaviour. Addict Biol 14: 373-383.
40. Hiranita T, Soto PL, Tanda G, Katz JL (2010). Reinforcing effects of sigma-receptor agonists in rats trained to self-administer cocaine. J Pharmacol Exp Ther 332: 515-524.
41. Hiranita T, Soto PL, Tanda G, Katz JL (2011). Lack of cocaine-like discriminative-stimulus effects of sigma-receptor agonists in rats. Behav Pharmacol 22: 525-530.
42. Hiranita T, Tanda G, Kopajtic TA, Newman AH, Katz JL (2009). Reinforcing Effects of Sigma-Receptor Agonists in Cocaine-Experienced and Naive Rats Program No 496.1. Neuroscience Meeting Planner Society for Neuroscience, Chicago, IL.
43. Hopf FW, Chang SJ, Sparta DR, Bowers MS, Bonci A (2010). Motivation for alcohol becomes resistant to quinine adulteration after 3 to 4 months of intermittent alcohol self-administration. Alcohol Clin Exp Res 34: 1565-1573.
44. Hudson JI, Hiripi E, Pope Jr HG., Kessler RC (2007). The prevalence and correlates of eating disorders in the National Comorbidity Survey Replication. Biol Psychiatry 61: 348-358.
45. Javaras KN, Pope HG, Lalonde JK, Roberts JL, Nillni YI, Laird NM et al (2008). Co-occurrence of binge eating disorder with psychiatric and medical disorders. J Clin Psychiatry 69: 266-273.
46. Johnson PM, Kenny PJ (2010). Dopamine D2 receptors in addiction-like reward dysfunction and compulsive eating in obese rats. Nat Neurosci 13: 635-641.
47. Kalivas PW, Volkow ND (2005). The neural basis of addiction: a pathology of motivation and choice. Am J Psychiatry 162: 1403-1413.
48. Kalivas PW, Volkow ND (2011). New medications for drug addiction hiding in glutamatergic neuroplasticity. Mol Psychiatry 16: 974-986.
49. Katz JL, Su TP, Hiranita T, Hayashi T, Tanda G, Kopajtic T et al (2011). A role for sigma receptors in stimulant self administration and addiction. Pharmaceuticals (Basel) 4: 880-914.
50. Koob GF (2009). Neurobiological substrates for the dark side of compulsivity in addiction. Neuropharmacology 56(Suppl 1): 18-31.
51. Koob GF, Volkow ND (2010). Neurocircuitry of addiction. Neuropsychopharmacology 35: 217-238.
52. Martin-Fardon R, Maurice T, Aujla H, Bowen WD, Weiss F (2007). Differential effects of sigma1 receptor blockade on self-administration and conditioned reinstatement motivated by cocaine vs natural reward. Neuropsychopharmacology 32: 1967-1973.
53. Martin WR, Eades CG, Thompson JA, Huppler RE, Gilbert PE (1976). The effects of morphine-and nalorphine-like drugs in the nondependent and morphine-dependent chronic spinal dog. J Pharmacol Exp Ther 197: 517-532.
54. Matsumoto RR, Liu Y, Lerner M, Howard EW, Brackett DJ (2003). Sigma receptors: potential medications development target for anti-cocaine agents. Eur J Pharmacol 469: 1-12.
55. Maurice T, Casalino M, Lacroix M, Romieu P (2003). Involvement of the sigma 1 receptor in the motivational effects of ethanol in mice. Pharmacol Biochem Behav 74: 869-876.
56. Maurice T, Martin-Fardon R, Romieu P, Matsumoto RR (2002). Sigma(1) (sigma(1)) receptor antagonists represent a new strategy against cocaine addiction and toxicity. Neurosci Biobehav Rev 26: 499-527.
57. Maurice T, Phan VL, Urani A, Kamei H, Noda Y, Nabeshima T (1999). Neuroactive neurosteroids as endogenous effectors for the sigma1 (sigma1) receptor: pharmacological evidence and therapeutic opportunities. Jpn J Pharmacol 81: 125-155.
58. Maurice T, Romieu P (2004). Involvement of the sigma1 receptor in the appetitive effects of cocaine. Pharmacopsychiatry 37(Suppl 3): S198-S207.
59. Maurice T, Su TP (2009). The pharmacology of sigma-1 receptors. Pharmacol Ther 124: 195-206.
60. McCracken KA, Bowen WD, de Costa BR, Matsumoto RR (1999). Two novel sigma receptor ligands, BD1047 and LR172, attenuate cocaine-induced toxicity and locomotor activity. Eur J Pharmacol 370: 225-232.
61. Melendez RI, Kalivas PW (2003). Metabotropic glutamate receptor regulation of extracellular glutamate levels in the prefrontal cortex. Ann N Y Acad Sci 1003: 443-444.
62. Melendez RI, Vuthiganon J, Kalivas PW (2005). Regulation of extracellular glutamate in the prefrontal cortex: focus on the cystine glutamate exchanger and group I metabotropic glutamate receptors. J Pharmacol Exp Ther 314: 139-147.
63. Menkel M, Terry P, Pontecorvo M, Katz JL, Witkin JM (1991). Selective sigma ligands block stimulant effects of cocaine. Eur J Pharmacol 201: 251-252.
64. Moebius FF, Burrows GG, Hanner M, Schmid E, Striessnig J, Glossmann H (1993). Identification of a 27-kDa high affinity phenylalkylamine-binding polypeptide as the sigma 1 binding site by photoaffinity labeling and ligand-directed antibodies. Mol Pharmacol 44: 966-971.
65. Narayanan S, Mesangeau C, Poupaert JH, McCurdy CR (2011). Sigma receptors and cocaine abuse. Curr Top Med Chem 11: 1128-1150.
66. Nguyen EC, McCracken KA, Liu Y, Pouw B, Matsumoto RR (2005). Involvement of sigma (sigma) receptors in the acute actions of methamphetamine: receptor binding and behavioral studies. Neuropharmacology 49: 638-645.
67. Perry JL, Joseph JE, Jiang Y, Zimmerman RS, Kelly TH, Darna M et al (2011). Prefrontal cortex and drug abuse vulnerability: translation to prevention and treatment interventions. Brain Res Rev 65: 124-149.
68. Quirion R, Bowen WD, Itzhak Y, Junien JL, Musacchio JM, Rothman RB et al (1992). A proposal for the classification of sigma binding sites. Trends Pharmacol Sci 13: 85-86.
69. Rawls SM, Baron DA, Geller EB, Adler MW (2002). Sigma sites mediate DTG-evoked hypothermia in rats. Pharmacol Biochem Behav 73: 779-786.
70. Robbins TW, Ersche KD, Everitt BJ (2008). Drug addiction and the memory systems of the brain. Ann N Y Acad Sci 1141: 1-21.
71. Rodvelt KR, Miller DK (2010). Could sigma receptor ligands be a treatment for methamphetamine addiction? Curr Drug Abuse Rev 3: 156-162.
72. Romieu P, Martin-Fardon R, Maurice T (2000). Involvement of the sigma1 receptor in the cocaine-induced conditioned place preference. NeuroReport 11: 2885-2888.
73. Romieu P, Phan VL, Martin-Fardon R, Maurice T (2002). Involvement of the sigma receptor in cocaine-induced conditioned place preference: possible dependence on dopamine uptake blockade. Neuropsychopharmacology 26: 444-455.
74. Sabino V, Cottone P, Blasio A, Iyer MR, Steardo L, Rice KC et al (2011). Activation of sigma-receptors induces binge-like drinking in sardinian alcohol-preferring rats. Neuropsychopharmacology 36: 1207-1218.
75. Sabino V, Cottone P, Parylak SL, Steardo L, Zorrilla EP (2009a). Sigma-1 receptor knockout mice display a depressive-like phenotype. Behav Brain Res 198: 472-476.
76. Sabino V, Cottone P, Zhao Y, Iyer MR, Steardo Jr L, Steardo L et al (2009b). The sigma-receptor antagonist BD-1063 decreases ethanol intake and reinforcement in animal models of excessive drinking. Neuropsychopharmacology 34: 1482-1493.
77. Sabino V, Cottone P, Zhao Y, Steardo L, Koob GF, Zorrilla EP (2009c). Selective reduction of alcohol drinking in Sardinian alcohol-preferring rats by a sigma-1 receptor antagonist. Psychopharmacology (Berl) 205: 327-335.
78. Su TP (1993). Delineating biochemical and functional properties of sigma receptors: emerging concepts. Critl Rev Neurobiol 7: 187-203.
79. Takahashi S, Miwa T, Horikomi K (2000). Involvement of sigma 1 receptors in methamphetamine-induced behavioral sensitization in rats. Neurosci Lett 289: 21-24.
80. Teegarden SL, Bale TL (2007). Decreases in dietary preference produce increased emotionality and risk for dietary relapse. Biol Psychiatry 61: 1021-1029.
81. Volkow ND, Wang GJ, Telang F, Fowler JS, Thanos PK, Logan J et al (2008). Low dopamine striatal D2 receptors are associated with prefrontal metabolism in obese subjects: possible contributing factors. NeuroImage 42: 1537-1543.
82. Walker JM, Bowen WD, Walker FO, Matsumoto RR, De Costa B, Rice KC (1990). Sigma receptors: biology and function. Pharmacol Rev 42: 355-402.
83. Wilfley D, Berkowitz R, Goebel-Fabbri A, Hirst K, Ievers-Landis C, Lipman TH et al (2011). Binge eating, mood, and quality of life in youth with type 2 diabetes: baseline data from the today study. Diabet Care 34: 858-860.
84. Witkin JM, Terry P, Menkel M, Hickey P, Pontecorvo M, Ferkany J et al (1993). Effects of the selective sigma receptor ligand, 6-[6-(4- hydroxypiperidinyl)hexyloxy]-3-methylflavone (NPC 16377), on behavioral and toxic effects of cocaine. J Pharmacol Exp Ther 266: 473-482.
85. Yanovski SZ (2003). Binge eating disorder and obesity in 2003: could treating an eating disorder have a positive effect on the obesity epidemic? Int J Eat Disord 34(Suppl): S117-S120.
86. Yeomans MR (1996). Palatability and the micro-structure of feeding in humans: the appetizer effect. Appetite 27: 119-133.