Glucagon-like peptide 1 receptor activation regulates cocaine actions and dopamine homeostasis in the lateral septum by decreasing arachidonic acid levels

Translational Psychiatry

Volumn 6, Issue 5, 2016, Pages

  Reddy, I A ^a   Pino, J A ^b,c   Weikop, P ^d,e   Osses, N ^b   Sorensen G ^d,e   Bering, T ^d   Valle, C ^f   Bluett, R J ^a,g   Erreger, K ^a   Wortwein, G ^d   Reyes, J G ^b   Graham, D ^h   Stanwood, G D ^h   Hackett, T A ^a,g   Patel, S ^g   Fink Jensen, A ^d,e   Torres, G E ^c   Galli, A ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b PONTIFICIA UNIVERSIDAD CATÓLICA DE VALPARAÍSO   (Chile)

^c UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^d UNIVERSITY OF COPENHAGEN   (Denmark)

^e Mental Health Services CPH   (Denmark)

^f UNIVERSIDAD VIÑA DEL MAR   (Chile)

^g VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^h FLORIDA STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACYLGLYCEROL; ARACHIDONIC ACID; ARACHIDONIC ACID DERIVATIVE; COCAINE; DOPAMINE; DOPAMINE TRANSPORTER; DOPAMINE UPTAKE INHIBITOR; ENDOCANNABINOID; EXENDIN 4; GLP1R PROTEIN, MOUSE; GLUCAGON LIKE PEPTIDE 1 RECEPTOR; GLYCERYL 2-ARACHIDONATE; INCRETIN; PEPTIDE; PROTEIN C FOS; SLC6A3 PROTEIN, MOUSE; VENOM;

AGONISTS; ANIMAL; DRUG EFFECTS; HOMEOSTASIS; METABOLISM; MICRODIALYSIS; MOUSE; SEPTUM NUCLEUS;

ANIMALS; ARACHIDONIC ACID; ARACHIDONIC ACIDS; COCAINE; DOPAMINE; DOPAMINE PLASMA MEMBRANE TRANSPORT PROTEINS; DOPAMINE UPTAKE INHIBITORS; ENDOCANNABINOIDS; GLUCAGON-LIKE PEPTIDE-1 RECEPTOR; GLYCERIDES; HOMEOSTASIS; INCRETINS; MICE; MICRODIALYSIS; PEPTIDES; PROTO-ONCOGENE PROTEINS C-FOS; SEPTAL NUCLEI; VENOMS;

EID: 85019999570     PISSN: None     EISSN: 21583188     Source Type: Journal    
DOI: 10.1038/TP.2016.86     Document Type: Article

References (94)

1. Erreger K, Davis AR, Poe AM, Greig NH, Stanwood GD, Galli A. Exendin-4 decreases amphetamine-induced locomotor activity. Physiol Behav 2012; 106: 574–578.
2. Reddy IA, Stanwood GD, Galli A. Moving beyond energy homeostasis: new roles for glucagon-like peptide-1 in food and drug reward. Neurochem Int 2014; 73: 49–55.
3. Harasta AE, Power JM, von Jonquieres G, Karl T, Drucker DJ, Housley GD et al. Septal glucagon-like peptide 1 receptor expression determines suppression of cocaine-induced behavior. Neuropsychopharmacology 2015; 40: 1969–1978.
4. Sorensen G, Reddy IA, Weikop P, Graham DL, Stanwood GD, Wortwein G et al. The glucagon-like peptide 1 (GLP-1) receptor agonist exendin-4 reduces cocaine self-administration in mice. Physiol Behav 2015; 149: 262–268.
5. Baggio LL, Drucker DJ. Biology of incretins: GLP-1 and GIP. Gastroenterology 2007; 132: 2131–2157.
6. Alhadeff AL, Rupprecht LE, Hayes MR. GLP-1 neurons in the nucleus of the solitary tract project directly to the ventral tegmental area and nucleus accumbens to control for food intake. Endocrinology 2012; 153: 647–658.
7. Drucker DJ, Nauck MA. The incretin system: glucagon-like peptide-1 receptor agonists and dipeptidyl peptidase-4 inhibitors in type 2 diabetes. Lancet 2006; 368: 1696–1705.
8. Pi-Sunyer X, Astrup A, Fujioka K, Greenway F, Halpern A, Krempf M et al. A randomized, controlled trial of 3.0 mg of liraglutide in weight management. N Engl J Med 2015; 373: 11–22.
9. Kastin AJ, Akerstrom V. Entry of exendin-4 into brain is rapid but may be limited at high doses. Int J Obes Relat Metab Disord 2003; 27: 313–318.
10. Merchenthaler I, Lane M, Shughrue P. Distribution of pre-pro-glucagon and glucagon-like peptide-1 receptor messenger RNAs in the rat central nervous system. J Comp Neurol 1999; 403: 261–280.
11. Dickson SL, Shirazi RH, Hansson C, Bergquist F, Nissbrandt H, Skibicka KP. The glucagon-like peptide 1 (GLP-1) analogue, exendin-4, decreases the rewarding value of food: a new role for mesolimbic GLP-1 receptors. J Neurosci 2012; 32: 4812–4820.
12. Shirazi RH, Dickson SL, Skibicka KP. Gut peptide GLP-1 and its analogue, exendin-4, decrease alcohol intake and reward. PLoS One 2013; 8: e61965.
13. Egecioglu E, Engel JA, Jerlhag E. The glucagon-like peptide 1 analogue exendin-4 attenuates the nicotine-induced locomotor stimulation, accumbal dopamine release, conditioned place preference as well as the expression of locomotor sensitization in mice. PLoS One 2013; 8: e77284.
14. Egecioglu E, Engel JA, Jerlhag E. The glucagon-like peptide 1 analogue, exendin-4, attenuates the rewarding properties of psychostimulant drugs in mice. PLoS One 2013; 8: e69010.
15. Egecioglu E, Steensland P, Fredriksson I, Feltmann K, Engel JA, Jerlhag E. The glucagon-like peptide 1 analogue Exendin-4 attenuates alcohol mediated beha-viors in rodents. Psychoneuroendocrinology 2013; 38: 1259–1270.
16. Graham DL, Erreger K, Galli A, Stanwood GD. GLP-1 analog attenuates cocaine reward. Mol Psychiatry 2013; 18: 961–962.
17. Suchankova P, Yan J, Schwandt ML, Stangl BL, Caparelli EC, Momenan R et al. The glucagon-like peptide-1 receptor as a potential treatment target in alcohol use disorder: evidence from human genetic association studies and a mouse model of alcohol dependence. Transl Psychiatry 2015; 5: e583.
18. Volkow ND, Wise RA. How can drug addiction help us understand obesity? Nat Neurosci 2005; 8: 555–560.
19. Berridge KC, Robinson TE. What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? Brain Res Brain Res Rev 1998; 28: 309–369.
20. Olds J, Milner P. Positive reinforcement produced by electrical stimulation of septal area and other regions of rat brain. J Comp Physiol Psychol 1954; 47: 419–427.
21. Sheehan TP, Chambers RA, Russell DS. Regulation of affect by the lateral septum: implications for neuropsychiatry. Brain Res Brain Res Rev 2004; 46: 71–117.
22. Luo AH, Tahsili-Fahadan P, Wise RA, Lupica CR, Aston-Jones G. Linking context with reward: a functional circuit from hippocampal CA3 to ventral tegmental area. Science 2011; 333: 353–357.
23. Sartor GC, Aston-Jones GS. A septal-hypothalamic pathway drives orexin neurons, which is necessary for conditioned cocaine preference. J Neurosci 2012; 32: 4623–4631.
24. Dadalko OI, Siuta M, Poe A, Erreger K, Matthies HJ, Niswender K et al. mTORC2/ rictor signaling disrupts dopamine-dependent behaviors via defects in striatal dopamine neurotransmission. J Neurosci 2015; 35: 8843–8854.
25. Sorensen G, Jensen M, Weikop P, Dencker D, Christiansen SH, Loland CJ et al. Neuropeptide Y Y5 receptor antagonism attenuates cocaine-induced effects in mice. Psychopharmacology (Berl) 2012; 222: 565–577.
26. Franklin K, Paxinos G. The Mouse Brain in Stereotaxic Coordinates. Academic Press: New York, NY, USA, 2007.
27. Weikop P, Egestad B, Kehr J. Application of triple-probe microdialysis for fast pharmacokinetic/pharmacodynamic evaluation of dopamimetic activity of drug candidates in the rat brain. J Neurosci Methods 2004; 140: 59–65.
28. Robertson SD, Matthies HJ, Owens WA, Sathananthan V, Christianson NS, Kennedy JP et al. Insulin reveals Akt signaling as a novel regulator of norepinephrine transporter trafficking and norepinephrine homeostasis. J Neurosci 2010; 30: 11305–11316.
29. Shonesy BC, Bluett RJ, Ramikie TS, Baldi R, Hermanson DJ, Kingsley PJ et al. Genetic disruption of 2-arachidonoylglycerol synthesis reveals a key role for endocannabinoid signaling in anxiety modulation. Cell Rep 2014; 9: 1644–1653.
30. Bronfman FC, Tcherpakov M, Jovin TM, Fainzilber M. Ligand-induced inter-nalization of the p75 neurotrophin receptor: a slow route to the signaling endosome. J Neurosci 2003; 23: 3209–3220.
31. Egana LA, Cuevas RA, Baust TB, Parra LA, Leak RK, Hochendoner S et al. Physical and functional interaction between the dopamine transporter and the synaptic vesicle protein synaptogyrin-3. J Neurosci 2009; 29: 4592–4604.
32. Ciliax BJ, Heilman C, Demchyshyn LL, Pristupa ZB, Ince E, Hersch SM et al. The dopamine transporter: immunochemical characterization and localization in brain. J Neurosci 1995; 15(3 Pt 1): 1714–1723.
33. Kuhar MJ, Ritz MC, Boja JW. The dopamine hypothesis of the reinforcing properties of cocaine. Trends Neurosci 1991; 14: 299–302.
34. Chen R, Tilley MR, Wei H, Zhou F, Zhou FM, Ching S et al. Abolished cocaine reward in mice with a cocaine-insensitive dopamine transporter. Proc Natl Acad Sci USA 2006; 103: 9333–9338.
35. Giros B, Jaber M, Jones SR, Wightman RM, Caron MG. Hyperlocomotion and indifference to cocaine and amphetamine in mice lacking the dopamine trans-porter. Nature 1996; 379: 606–612.
36. Speed N, Saunders C, Davis A, Owens W, Matthies H, Saadat S et al. Impaired striatal Akt signaling disrupts dopamine homeostasis and increases feeding. PLoS One 2011; 6: 1–10.
37. Williams JM, Owens WA, Turner GH, Saunders C, Dipace C, Blakely RD et al. Hypoinsulinemia regulates amphetamine-induced reverse transport of dopamine. PLoS Biol 2007; 5: 2369–2378.
38. Owens WA, Williams JM, Saunders C, Avison MJ, Galli A, Daws LC. Rescue of dopamine transporter function in hypoinsulinemic rats by a D2 receptor-ERK-dependent mechanism. J Neurosci 2012; 32: 2637–2647.
39. Gulley JM, Zahniser NR. Rapid regulation of dopamine transporter function by substrates, blockers and presynaptic receptor ligands. Eur J Pharmacol 2003; 479: 139–152.
40. Zahniser NR, Sorkin A. Rapid regulation of the dopamine transporter: role in stimulant addiction? Neuropharmacology 2004; 47: 80–91.
41. Rao A, Sorkin A, Zahniser NR. Mice expressing markedly reduced striatal dopamine transporters exhibit increased locomotor activity, dopamine uptake turnover rate, and cocaine responsiveness. Synapse 2013; 67: 668–677.
42. Tilley MR, Cagniard B, Zhuang X, Han DD, Tiao N, Gu HH. Cocaine reward and locomotion stimulation in mice with reduced dopamine transporter expression. BMC Neurosci 2007; 8: 42.
43. Robertson SD, Matthies HJ, Sathananthan V, Christianson NSB, Kennedy JP, Lindsley CW et al. Insulin reveals Akt signaling as a novel regulator of nor-epinephrine transporter trafficking and norepinephrine homeostasis. J Neurosci 2010; 30: 11305–11316.
44. Göke R, Fehmann HC, Linn T, Schmidt H, Krause M, Eng J et al. Exendin-4 is a high potency agonist and truncated exendin-(9-39)-amide an antagonist at the glucagon-like peptide 1-(7-36)-amide receptor of insulin-secreting beta-cells. J Biol Chem 1993; 268: 19650–19655.
45. Horder J, Harmer CJ, Cowen PJ, McCabe C. Reduced neural response to reward following 7 days treatment with the cannabinoid CB1 antagonist rimonabant in healthy volunteers. Int J Neuropsychopharmacol 2010; 13: 1103–1113.
46. Labouebe G, Liu S, Dias C, Zou H, Wong JC, Karunakaran S et al. Insulin induces long-term depression of ventral tegmental area dopamine neurons via endo-cannabinoids. Nat Neurosci 2013; 16: 300–308.
47. Parsons LH, Hurd YL. Endocannabinoid signalling in reward and addiction. Nat Rev Neurosci 2015; 16: 579–594.
48. Xi ZX, Peng XQ, Li X, Song R, Zhang HY, Liu QR et al. Brain cannabinoid CB(2) receptors modulate cocaine's actions in mice. Nat Neurosci 2011; 14: 1160–1166.
49. Xi ZX, Spiller K, Pak AC, Gilbert J, Dillon C, Li X et al. Cannabinoid CB1 receptor antagonists attenuate cocaine's rewarding effects: experiments with self-administration and brain-stimulation reward in rats. Neuropsychopharmacology 2008; 33: 1735–1745.
50. Nomura DK, Morrison BE, Blankman JL, Long JZ, Kinsey SG, Marcondes MC et al. Endocannabinoid hydrolysis generates brain prostaglandins that promote neu-roinflammation. Science 2011; 334: 809–813.
51. L'Hirondel M, Cheramy A, Godeheu G, Glowinski J. Effects of arachidonic acid on dopamine synthesis, spontaneous release, and uptake in striatal synaptosomes from the rat. J Neurochem 1995; 64: 1406–1409.
52. Chen N, Appell M, Berfield JL, Reith ME. Inhibition by arachidonic acid and other fatty acids of dopamine uptake at the human dopamine transporter. Eur J Pharmacol 2003; 478: 89–95.
53. Zhang L, Reith ME. Regulation of the functional activity of the human dopamine transporter by the arachidonic acid pathway. Eur J Pharmacol 1996; 315: 345–354.
54. Westerink RH, Ewing AG. The PC12 cell as model for neurosecretion. Acta Physiol (Oxf) 2008; 192: 273–285.
55. Kovacic P. Role of oxidative metabolites of cocaine in toxicity and addiction: oxidative stress and electron transfer. Med Hypotheses 2005; 64: 350–356.
56. Poon HF, Abdullah L, Mullan MA, Mullan MJ, Crawford FC. Cocaine-induced oxi-dative stress precedes cell death in human neuronal progenitor cells. Neurochem Int 2007; 50: 69–73.
57. Ng F, Berk M, Dean O, Bush AI. Oxidative stress in psychiatric disorders: evidence base and therapeutic implications. Int J Neuropsychopharmacol 2008; 11: 851–876.
58. Teramoto S, Miyamoto N, Yatomi K, Tanaka Y, Oishi H, Arai H et al. Exendin-4, a glucagon-like peptide-1 receptor agonist, provides neuroprotection in mice transient focal cerebral ischemia. J Cereb Blood Flow Metab 2011; 31: 1696–1705.
59. Brame CJ, Salomon RG, Morrow JD, Roberts LJ 2nd. Identification of extremely reactive gamma-ketoaldehydes (isolevuglandins) as products of the isoprostane pathway and characterization of their lysyl protein adducts. J Biol Chem 1999; 274: 13139–13146.
60. Davies SS, Amarnath V, Brame CJ, Boutaud O, Roberts LJ 2nd. Measurement of chronic oxidative and inflammatory stress by quantification of isoketal/levu-glandin gamma-ketoaldehyde protein adducts using liquid chromatography tandem mass spectrometry. Nat Protoc 2007; 2: 2079–2091.
61. Davies SS, Amarnath V, Roberts LJ 2nd. Isoketals: highly reactive gamma-ketoaldehydes formed from the H2-isoprostane pathway. Chem Phys Lipids 2004; 128: 85–99.
62. Davies SS, Brantley EJ, Voziyan PA, Amarnath V, Zagol-Ikapitte I, Boutaud O et al. Pyridoxamine analogues scavenge lipid-derived gamma-ketoaldehydes and protect against H2O2-mediated cytotoxicity. Biochemistry 2006; 45: 15756–15767.
63. Morel P, Tallineau C, Pontcharraud R, Piriou A, Huguet F. Effects of 4-hydro-xynonenal, a lipid peroxidation product, on dopamine transport and Na+/K+ ATPase in rat striatal synaptosomes. Neurochem Int 1998; 33: 531–540.
64. Park SU, Ferrer JV, Javitch JA, Kuhn DM. Peroxynitrite inactivates the human dopamine transporter by modification of cysteine 342: potential mechanism of neurotoxicity in dopamine neurons. J Neurosci 2002; 22: 4399–4405.
65. Huang CL, Huang NK, Shyue SK, Chern Y. Hydrogen peroxide induces loss of dopamine transporter activity: a calcium-dependent oxidative mechanism. J Neurochem 2003; 86: 1247–1259.
66. Robertson SD, Matthies HJ, Galli A. A closer look at amphetamine-induced reverse transport and trafficking of the dopamine and norepinephrine transporters. Mol Neurobiol 2009; 39: 73–80.
67. Mortensen OV, Amara SG. Dynamic regulation of the dopamine transporter. Eur J Pharmacol 2003; 479: 159–170.
68. Pike LJ, Han X, Chung KN, Gross RW. Lipid rafts are enriched in arachidonic acid and plasmenylethanolamine and their composition is independent of caveolin-1 expression: a quantitative electrospray ionization/mass spectrometric analysis. Biochemistry 2002; 41: 2075–2088.
69. Cremona ML, Matthies HJ, Pau K, Bowton E, Speed N, Lute BJ et al. Flotillin-1 is essential for PKC-triggered endocytosis and membrane microdomain localization of DAT. Nat Neurosci 2011; 14: 469–477.
70. Gabriel LR, Wu S, Kearney P, Bellve KD, Standley C, Fogarty KE et al. Dopamine transporter endocytic trafficking in striatal dopaminergic neurons: differential dependence on dynamin and the actin cytoskeleton. J Neurosci 2013; 33: 17836–17846.
71. Heath RG. Electrical self-stimulation of the brain in man. Am J Psychiatry 1963; 120: 571–577.
72. Prado-Alcala R, Streather A, Wise RA. Brain stimulation reward and dopamine terminal fields. II. Septal and cortical projections. Brain Res 1984; 301: 209–219.
73. Zahm DS, Parsley KP, Schwartz ZM, Cheng AY. On lateral septum-like character-istics of outputs from the accumbal hedonic "hotspot" of Pecina and Berridge with commentary on the transitional nature of basal forebrain "boundaries". J Comp Neurol 2013; 521: 50–68.
74. Ahmed SH, Koob GF. Transition from moderate to excessive drug intake: change in hedonic set point. Science 1998; 282: 298–300.
75. Calipari ES, Ferris MJ, Jones SR. Extended access of cocaine self-administration results in tolerance to the dopamine-elevating and locomotor-stimulating effects of cocaine. J Neurochem 2014; 128: 224–232.
76. Ferris MJ, Calipari ES, Mateo Y, Melchior JR, Roberts DC, Jones SR. Cocaine self-administration produces pharmacodynamic tolerance: differential effects on the potency of dopamine transporter blockers, releasers, and methylphenidate. Neuropsychopharmacology 2012; 37: 1708–1716.
77. Calipari ES, Ferris MJ, Melchior JR, Bermejo K, Salahpour A, Roberts DC et al. Methylphenidate and cocaine self-administration produce distinct dopamine terminal alterations. Addict Biol 2014; 19: 145–155.
78. Ferris MJ, Calipari ES, Rose JH, Siciliano CA, Sun H, Chen R et al. A single amphetamine infusion reverses deficits in dopamine nerve-terminal function caused by a history of cocaine self-administration. Neuropsychopharmacology 2015; 40: 1826–1836.
79. Chen N, Reith ME. Substrates and inhibitors display different sensitivity to expression level of the dopamine transporter in heterologously expressing cells. J Neurochem 2007; 101: 377–388.
80. Volkow ND, Wang GJ, Fischman MW, Foltin RW, Fowler JS, Abumrad NN et al. Relationship between subjective effects of cocaine and dopamine transporter occupancy. Nature 1997; 386: 827–830.
81. Mazei-Robison MS, Koo JW, Friedman AK, Lansink CS, Robison AJ, Vinish M et al. Role for mTOR signaling and neuronal activity in morphine-induced adaptations in ventral tegmental area dopamine neurons. Neuron 2011; 72: 977–990.
82. Perry T, Greig NH. The glucagon-like peptides: a double-edged therapeutic sword? Trends Pharmacol Sci 2003; 24: 377–383.
83. Ye Y, Birnbaum Y. Cyclic AMP-mediated pleiotropic effects of glucagon-like peptide-1 receptor activation. Focus on "Exendin-4 attenuates high glucose-induced cardiomyocyte apoptosis via inhibition of endoplasmic reticulum stress and activation of SERCA2a". Am J Physiol Cell Physiol 2013; 304: C505–C507.
84. El Manira A, Kyriakatos A. The role of endocannabinoid signaling in motor control. Physiology (Bethesda) 2010; 25: 230–238.
85. Bhattacharjee AK, Chang L, White L, Bazinet RP, Rapoport SI. D-Amphetamine stimulates D2 dopamine receptor-mediated brain signaling involving arachidonic acid in unanesthetized rats. J Cereb Blood Flow Metab 2006; 26: 1378–1388.
86. Farooqui AA, Horrocks LA, Farooqui T. Modulation of inflammation in brain: a matter of fat. J Neurochem 2007; 101: 577–599.
87. Abbas T, Faivre E, Holscher C. Impairment of synaptic plasticity and memory formation in GLP-1 receptor KO mice: Interaction between type 2 diabetes and Alzheimer's disease. Behav Brain Res 2009; 205: 265–271.
88. Holscher C. Central effects of GLP-1: new opportunities for treatments of neuro-degenerative diseases. J Endocrinol 2014; 221: T31–T41.
89. Holscher C, Li L. New roles for insulin-like hormones in neuronal signalling and protection: new hopes for novel treatments of Alzheimer's disease? Neurobiol Aging 2010; 31: 1495–1502.
90. Harkavyi A, Abuirmeileh A, Lever R, Kingsbury AE, Biggs CS, Whitton PS. Glucagon-like peptide 1 receptor stimulation reverses key deficits in distinct rodent models of Parkinson's disease. J Neuroinflammation 2008; 5: 19.
91. Brame CJ, Boutaud O, Davies SS, Yang T, Oates JA, Roden D et al. Modification of proteins by isoketal-containing oxidized phospholipids. J Biol Chem 2004; 279: 13447–13451.
92. Rivera P, Miguens M, Coria SM, Rubio L, Higuera-Matas A, Bermudez-Silva FJ et al. Cocaine self-administration differentially modulates the expression of endogenous cannabinoid system-related proteins in the hippocampus of Lewis vs. Fischer 344 rats. Int J Neuropsychopharmacol 2013; 16: 1277–1293.
93. Mietlicki-Baase EG, Ortinski PI, Reiner DJ, Sinon CG, McCutcheon JE, Pierce RC et al. Glucagon-like peptide-1 receptor activation in the nucleus accumbens core suppresses feeding by increasing glutamatergic AMPA/kainate signaling. J Neurosci 2014; 34: 6985–6992.
94. Mietlicki-Baase EG, Ortinski PI, Rupprecht LE, Olivos DR, Alhadeff AL, Pierce RC et al. The food intake-suppressive effects of glucagon-like peptide-1 receptor signaling in the ventral tegmental area are mediated by AMPA/kainate receptors. Am J Physiol Endocrinol Metab 2013; 305: E1367–E1374.