Neuroadaptations in the striatal proteome of the rat following prolonged excessive sucrose intake

Neurochemical Research

Volumn 39, Issue 5, 2014, Pages 815-824

  Ahmed, Selina ^a   Kashem, Mohammed Abul ^a   Sarker, Ranjana ^a   Ahmed, Eakhlas U ^a   Hargreaves, Garth A ^a   McGregor, Iain S ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Craving; Dopamine; Obesity; Proteomics; Rat; Striatum; Sucrose

Indexed keywords

3,4 DIHYDROXYPHENYLACETIC ACID; 5 HYDROXYINDOLEACETIC ACID; ADIPOPHILIN; BINDING PROTEIN; C H RAS 1 PROTEIN; CATECHOL METHYLTRANSFERASE; DOPAMINE; GLUTATHIONE TRANSFERASE; HOMOVANILLIC ACID; LAMIN; LAMIN B1; MALATE DEHYDROGENASE; NEUROFILAMENT L PROTEIN; NEUROFILAMENT PROTEIN; NORADRENALIN; PHOSPHATASE; PHOSPHOPROTEIN PHOSPHATASE 1; PROLACTIN; PROLINE DIPEPTIDASE; PROTEIN 14 3 3; PROTEIN PHOSPHATASE 1 REGULATORY SUBUNIT 7; PROTEOME; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; PYRIDOXAL PHOSPHATE PHOSPHATASE; PYRUVATE DEHYDROGENASE; RAB PROTEIN; RAB3B PROTEIN; SEPIAPTERIN REDUCTASE; SEROTONIN; SUCROSE; UNCLASSIFIED DRUG; GLUTATHIONE;

3,4 DIHYDROXYPHENYLACETIC ACID BRAIN LEVEL; 5 HYDROXYINDOLEACETIC ACID BRAIN LEVEL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; BRAIN LEVEL; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINE BRAIN LEVEL; DOWN REGULATION; FOOD ADDICTION; HOMOVANILLIC ACID BRAIN LEVEL; LONG TERM EXPOSURE; MALE; NEUROADAPTATION; NONHUMAN; NORADRENALIN BRAIN LEVEL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEOMICS; RAT; SEROTONIN BRAIN LEVEL; SUGAR INTAKE; UPREGULATION; WEIGHT GAIN; ANIMAL; APOPTOSIS; CALORIC INTAKE; DRUG EFFECTS; METABOLISM; OBESITY; WISTAR RAT;

RATTUS; RATTUS NORVEGICUS;

ANIMALS; APOPTOSIS; CORPUS STRIATUM; DOPAMINE; ENERGY INTAKE; GLUTATHIONE; MALE; OBESITY; PROTEOME; RATS, WISTAR; SUCROSE;

EID: 84905408792     PISSN: 03643190     EISSN: 15736903     Source Type: Journal    
DOI: 10.1007/s11064-014-1274-6     Document Type: Article

References (65)

1. Swinburn BA, Sacks G, Hall KD, McPherson K, Finegood DT, Moodie ML, Gortmaker SL (2011) The global obesity pandemic: shaped by global drivers and local environments. Lancet 378(9793):804-814
2. Avena NM, Long KA, Hoebel BG (2005) Sugar-dependent rats show enhanced responding for sugar after abstinence: evidence of a sugar deprivation effect. Physiol Behav 84(3):359-362 (Pubitemid 40342589)
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(1):20-39 (Pubitemid 350160955)
4. Bocarsly ME, Berner LA, Hoebel BG, Avena NM (2011) Rats that binge eat fat-rich food do not show somatic signs or anxiety associated with opiate-like withdrawal: implications for nutrient-specific food addiction behaviors. Physiol Behav 104(5):865-872
5. Corwin RL, Avena NM, Boggiano MM (2011) Feeding and reward: perspectives from three rat models of binge eating. Physiol Behav 104(1):87-97
6. Geiger BM, Haburcak M, Avena NM, Moyer MC, Hoebel BG, Pothos EN (2009) Deficits of mesolimbic dopamine neurotransmission in rat dietary obesity. Neuroscience 159(4):1193-1199
7. Baldo BA, Pratt WE, Will MJ, Hanlon EC, Bakshi VP, Cador M (2013) Principles of motivation revealed by the diverse functions of neuropharmacological and neuroanatomical substrates underlying feeding behavior. Neurosci Biobehav Rev 37(9):1985-1998
8. Carnell S, Gibson C, Benson L, Ochner CN, Geliebter A (2012) Neuroimaging and obesity: current knowledge and future directions. Obes Rev 13(1):43-56
9. O'Doherty JP, Deichmann R, Critchley HD, Dolan RJ (2002) Neural responses during anticipation of a primary taste reward. Neuron 33(5):815-826 (Pubitemid 34219251)
10. Hajnal A, Smith GP, Norgren R (2004) Oral sucrose stimulation increases accumbens dopamine in the rat. Am J Physiol Regul Integr Comp Physiol 286(1):R31-37 (Pubitemid 38055888)
11. Bassareo V, Di Chiara G (1997) Differential influence of associative and nonassociative learning mechanisms on the responsiveness of prefrontal and accumbal dopamine transmission to food stimuli in rats fed ad libitum. J Neurosci 17(2):851-861 (Pubitemid 27024596)
12. Liang NC, Hajnal A, Norgren R (2006) Sham feeding corn oil increases accumbens dopamine in the rat. Am J Physiol Regul Integr Comp Physiol 291(5):R1236-1239
13. Schur EA, Kleinhans NM, Goldberg J, Buchwald D, Schwartz MW, Maravilla K (2009) Activation in brain energy regulation and reward centers by food cues varies with choice of visual stimulus. Int J Obes (Lond) 33(6):653-661
14. Yoganathan P, Karunakaran S, Ho MM, Clee SM (2012) Nutritional regulation of genome-wide association obesity genes in a tissue-dependent manner. Nutr Metab (Lond) 9(1):65
15. Vucetic Z, Kimmel J, Totoki K, Hollenbeck E, Reyes TM (2010) Maternal high-fat diet alters methylation and gene expression of dopamine and opioid-related genes. Endocrinology 151(10):4756-4764
16. Lee SK, Park SO, Joe CO, Kim YS (2007) Interaction of HCV core protein with 14-3-3epsilon protein releases Bax to activate apoptosis. Biochem Biophys Res Commun 352(3):756-762 (Pubitemid 44880320)
17. Matsuda-Matsumoto H, Iwazaki T, Kashem MA, Harper C, Matsumoto I (2007) Differential protein expression profiles in the hippocampus of human alcoholics. Neurochem Int 51(6-7):370-376 (Pubitemid 47503457)
18. Kashem MA, Sarker R, Des Etages H, Machaalani R, King N, McGregor IS, Matsumoto I (2009) Comparative proteomics in the corpus callosal sub-regions of postmortem human brain. Neurochem Int 55(7):483-490
19. Kashem MA, James G, Harper C, Wilce P, Matsumoto I (2007) Differential protein expression in the corpus callosum (splenium) of human alcoholics: a proteomics study. Neurochem Int 50(2):450-459 (Pubitemid 46097176)
20. Kashem MA, Harper C, Matsumoto I (2008) Differential protein expression in the corpus callosum (genu) of human alcoholics. Neurochem Int 53(1-2):1-11
21. Quinn HR, Matsumoto I, Callaghan PD, Long LE, Arnold JC, Gunasekaran N, Thompson MR, Dawson B, Mallet PE, Kashem MA, Matsuda-Matsumoto H, Iwazaki T, McGregor IS (2008) Adolescent rats find repeated Delta(9)-THC less aversive than adult rats but display greater residual cognitive deficits and changes in hippocampal protein expression following exposure. Neuropsychopharmacology 33(5):1113-1126 (Pubitemid 351367534)
22. Hargreaves GA, Quinn H, Kashem MA, Matsumoto I, McGregor IS (2009) Proteomic analysis demonstrates adolescent vulnerability to lasting hippocampal changes following chronic alcohol consumption. Alcohol Clin Exp Res 33(1):86-94
23. van Nieuwenhuijzen PS, Kashem MA, Matsumoto I, Hunt GE, McGregor IS (2010) A long hangover from party drugs: residual proteomic changes in the hippocampus of rats 8 weeks after gamma-hydroxybutyrate (GHB), 3,4-methylenedioxymethamphetamine (MDMA) or their combination. Neurochem Int 56(8):871-877
24. Motbey CP, Karanges E, Li KM, Wilkinson S, Winstock AR, Ramsay J, Hicks C, Kendig MD, Wyatt N, Callaghan PD, McGregor IS (2012) Mephedrone in adolescent rats: residual memory impairment and acute but not lasting 5-HT depletion. PLoS ONE 7(9):e45473
25. Kashem MA, Ummehany R, Ukai W, Hashimoto E, Saito T, McGregor IS, Matsumoto I (2009) Effects of typical (haloperidol) and atypical (risperidone) antipsychotic agents on protein expression in rat neural stem cells. Neurochem Int 55(7):558-565
26. Ahmed EU, Ahmed S, Ukai W, Matsumoto I, Kemp A, McGregor IS, Kashem MA (2012) Antipsychotic induced alteration of growth and proteome of rat neural stem cells. Neurochem Res 37(8):1649-1659
27. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254
28. Kashem MA, Etages HD, Kopitar-Jerala N, McGregor IS, Matsumoto I (2009) Differential protein expression in the corpus callosum (body) of human alcoholic brain. J Neurochem 110(2):486-495
29. Zabel C, Andreew A, Mao L, Hartl D (2008) Protein expression overlap: more important than which proteins change in expression? Expert Rev Proteom 5(2):187-205 (Pubitemid 351670925)
30. Stanta G, Mucelli SP, Petrera F, Bonin S, Bussolati G (2006) A novel fixative improves opportunities of nucleic acids and proteomic analysis in human archive's tissues. Diagn Mol Pathol 15(2):115-123 (Pubitemid 44350489)
31. Grimm JW, Barnes J, North K, Collins S, Weber R (2011) A general method for evaluating incubation of sucrose craving in rats. J Vis Exp 57:e3335
32. Kendig MD, Boakes RA, Rooney KB, Corbit LH (2013) Chronic restricted access to 10% sucrose solution in adolescent and young adult rats impairs spatial memory and alters sensitivity to outcome devaluation. Physiol Behav 120C:164-172
33. Lombardo YB, D'Alessandro ME, Chicco AG (2006) A long-term sucrose-rich diet increases diacylglycerol content and membrane nPKC theta expression and alters glucose metabolism in skeletal muscle of rats. Nutr Res 26(6):289-296 (Pubitemid 44142803)
34. Charlet K, Beck A, Heinz A (2013) The dopamine system in mediating alcohol effects in humans. Curr Top Behav Neurosci 13:461-488
35. Rada P, Avena NM, Hoebel BG (2005) Daily bingeing on sugar repeatedly releases dopamine in the accumbens shell. Neuroscience 134(3):737-744 (Pubitemid 41133378)
36. Doyon WM, Ramachandra V, Samson HH, Czachowski CL, Gonzales RA (2004) Accumbal dopamine concentration during operant self-administration of a sucrose or a novel sucrose with ethanol solution. Alcohol 34(2-3):261-271 (Pubitemid 40292785)
37. Hajnal A, Margas WM, Covasa M (2008) Altered dopamine D2 receptor function and binding in obese OLETF rat. Brain Res Bull 75(1):70-76 (Pubitemid 350297644)
38. Rauhut AS, Fenton L, Bardo MT (2010) Renewal of sucrose-seeking behavior in rats: role of D(2) dopamine receptors. Pharmacol Biochem Behav 96(3):354-362
39. Pan Y, Berman Y, Haberny S, Meller E, Carr KD (2006) Synthesis, protein levels, activity, and phosphorylation state of tyrosine hydroxylase in mesoaccumbens and nigrostriatal dopamine pathways of chronically food-restricted rats. Brain Res 1122(1):135-142 (Pubitemid 44708112)
40. Wallace LJ (2007) A small dopamine permeability of storage vesicle membranes and end product inhibition of tyrosine hydroxylase are sufficient to explain changes occurring in dopamine synthesis and storage after inhibition of neuron firing. Synapse 61(9):715-723
41. Kashem MA, Ahmed S, Sarker R, Ahmed EU, Hargreaves GA, McGregor IS (2012) Long-term daily access to alcohol alters dopamine-related synthesis and signalling proteins in the rat striatum. Neurochem Int 61(8):1280-1288
42. Ben-Jonathan N, LaPensee CR, LaPensee EW (2008) What can we learn from rodents about prolactin in humans? Endocr Rev 29(1):1-41 (Pubitemid 351252745)
43. Shelly S, Boaz M, Orbach H (2012) Prolactin and autoimmunity. Autoimmun Rev 11(6-7):A465-470
44. Angelier F, Chastel O (2009) Stress, prolactin and parental investment in birds: a review. Gen Comp Endocrinol 163(1-2):142-148
45. Meaney AM, O'Keane V (2002) Prolactin and schizophrenia: clinical consequences of hyperprolactinemia. Life Sci 71(9):979-992 (Pubitemid 34667104)
46. Tse MC, Wong GK, Xiao P, Cheng CH, Chan KM (2008) Down-regulation of goldfish (Carassius auratus) prolactin gene expression by dopamine and thyrotropin releasing hormone. Gen Comp Endocrinol 155(3):729-741 (Pubitemid 351191909)
47. Gonzalez-Iglesias AE, Murano T, Li S, Tomic M, Stojilkovic SS (2008) Dopamine inhibits basal prolactin release in pituitary lactotrophs through pertussis toxin-sensitive and -insensitive signalling pathways. Endocrinology 149(4):1470-1479 (Pubitemid 351468341)
48. Ben-Jonathan N, Hugo ER, Brandebourg TD, LaPensee CR (2006) Focus on prolactin as a metabolic hormone. Trends Endocrinol Metab 17(3):110-116
49. Ellingboe J, Mendelson JH, Kuehnle JC (1980) Effects of heroin and naltrexone on plasma prolactin levels in man. Pharmacol Biochem Behav 12(1):163-165 (Pubitemid 10103033)
50. Brown TT, Dobs AS (2002) Endocrine effects of marijuana. J Clin Pharmacol 42(11 Suppl):90S-96S (Pubitemid 35205051)
51. Wu LY, Huang EY, Tao PL (2010) Coadministration of dextromethorphan during pregnancy and throughout lactation prevents morphine-induced hyperprolactinemia in female rats. Fertil Steril 93(5):1686-1694
52. Rideout HJ, Parker LA (1996) Morphine enhancement of sucrose palatability: analysis by the taste reactivity test. Pharmacol Biochem Behav 53(3):731-734 (Pubitemid 26086457)
53. Da Silva LA, De Marcucci OL, Carmona A (1992) Adaptive changes in total pyruvate dehydrogenase activity in lipogenic tissues of rats fed high-sucrose or high-fat diets. Comp Biochem Physiol Comp Physiol 103(2):407-411
54. Pape ME, Lopez-Casillas F, Kim KH (1988) Physiological regulation of acetyl-CoA carboxylase gene expression: effects of diet, diabetes, and lactation on acetyl-CoA carboxylase mRNA. Arch Biochem Biophys 267(1):104-109 (Pubitemid 19001015)
55. Fantino M (2011) Role of lipids in the control of food intake. Curr Opin Clin Nutr Metabol Care 14(2):138-144
56. Fortino MA, Lombardo YB, Chicco A (2007) The reduction of dietary sucrose improves dyslipidemia, adiposity, and insulin secretion in an insulin-resistant rat model. Nutrition 23(6):489-497 (Pubitemid 46901013)
57. Basciano H, Federico L, Adeli K (2005) Fructose, insulin resistance, and metabolic dyslipidemia. Nutr Metab (Lond) 2(1):5
58. Boone C, Mourot J, Gregoire F, Remacle C (2000) The adipose conversion process: regulation by extracellular and intracellular factors. Reprod Nutr Dev 40(4):325-358
59. Kutsuna M, Kodama T, Sumida M, Nagai A, Higashine M, Zhang W, Hayashi Y, Shiraishi A, Ohashi Y (2007) Presence of adipose differentiation-related protein in rat meibomian gland cells. Exp Eye Res 84(4):687-693 (Pubitemid 46400635)
60. Chirico V, Cannavo S, Lacquaniti A, Salpietro V, Mandolfino M, Romeo PD, Cotta O, Munafo C, Giorgianni G, Salpietro C, Arrigo T (2013) Prolactin in obese children: a bridge between inflammation and metabolic-endocrine dysfunction. Clin Endocrinol (Oxf) 79(4):537-544
61. Maria Ines PM, Maria LG, Cecilia RM, Daniela N, Maria OA, Marcelo R, Damasia BV (2014) Selective disruption of dopamine D2 receptors in pituitary lactotropes increases body weight and adiposity in female mice. Endocrinology 155(3):829-839
62. Zhao X, Zhu Q, Wang Y, Yang Z, Liu Y (2010) Tissue-specific expression of the chicken adipose differentiation-related protein (ADP) gene. Mol Biol Rep 37(6):2839-2845
63. Feillet-Coudray C, Sutra T, Fouret G, Ramos J, Wrutniak-Cabello C, Cabello G, Cristol JP, Coudray C (2009) Oxidative stress in rats fed a high-fat high-sucrose diet and preventive effect of polyphenols: involvement of mitochondrial and NAD(P)H oxidase systems. Free Radic Biol Med 46(5):624-632
64. Saiki R, Okazaki M, Iwai S, Kumai T, Kobayashi S, Oguchi K (2007) Effects of pioglitazone on increases in visceral fat accumulation and oxidative stress in spontaneously hypertensive hyperlipidemic rats fed a high-fat diet and sucrose solution. J Pharmacol Sci 105(2):157-167 (Pubitemid 350106805)
65. Hansen M, Baunsgaard D, Autrup H, Vogel UB, Moller P, Lindecrona R, Wallin H, Poulsen HE, Loft S, Dragsted LO (2008) Sucrose, glucose and fructose have similar genotoxicity in the rat colon and affect the metabolome. Food Chem Toxicol 46(2):752-760 (Pubitemid 350297555)