Dietary restriction mitigates cocaine-induced alterations of olfactory bulb cellular plasticity and gene expression, and behavior

Journal of Neurochemistry

Volumn 114, Issue 1, 2010, Pages 323-334

  Xu, Xiangru ^a,b   Mughal, Mohamed R ^a   Scott Hall, F ^c   Perona, Maria T G ^c   Pistell, Paul J ^a,d   Lathia, Justin D ^a   Chigurupati, Srinivasulu ^a   Becker, Kevin G ^a   Ladenheim, Bruce ^c   Niklason, Laura E ^b   Uhl, George R ^c   Cadet, Jean Lud ^c   Mattson, Mark P ^a,e  

^a NATIONAL INSTITUTE ON AGING   (United States)

^b YALE UNIVERSITY   (United States)

^c NATIONAL INSTITUTE ON DRUG ABUSE   (United States)

^d PENNINGTON BIOMEDICAL RESEARCH CENTER   (United States)

^e JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Addiction; Caloric restriction; CREB; Neurogenesis; Nucleus accumbens; Obesity

Indexed keywords

3,4 DIHYDROXYPHENYLACETIC ACID; 5 HYDROXYINDOLEACETIC ACID; AMINE OXIDASE (FLAVIN CONTAINING) ISOENZYME A; AMINE OXIDASE (FLAVIN CONTAINING) ISOENZYME B; CALCIUM; CATECHOL METHYLTRANSFERASE; COCAINE; CYCLIC AMP; DOPAMINE; HOMOVANILLIC ACID; SEROTONIN; TYROSINE 3 MONOOXYGENASE;

ACUTE DRUG ADMINISTRATION; ADDICTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALCIUM SIGNALING; CALORIC INTAKE; CELL PROLIFERATION; CELLULAR STRESS RESPONSE; CHRONIC DRUG ADMINISTRATION; CONDITIONING; CONTROLLED STUDY; DIET RESTRICTION; DOPAMINE METABOLISM; DOWN REGULATION; ENERGY METABOLISM; GENE EXPRESSION REGULATION; LOCOMOTION; MALE; MITOCHONDRIAL RESPIRATION; MOUSE; NERVE CELL PLASTICITY; NEURAL STEM CELL; NONHUMAN; OLFACTORY BULB; OLFACTORY RECEPTOR; PLACE PREFERENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR GENE; SENSITIZATION; UPREGULATION;

ANIMALS; BEHAVIOR, ANIMAL; CELL PROLIFERATION; COCAINE; DIET; DOPAMINE; ENERGY INTAKE; FASTING; GENE EXPRESSION; MALE; MICE; MICE, INBRED C57BL; MOTOR ACTIVITY; NEURONS; OLFACTORY BULB; STEM CELLS;

MUS;

EID: 77953306087     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2010.06782.x     Document Type: Article

References (76)

1. Alburges M. E. Wamsley J. K. (1993) Effects on monoamine levels in rat CNS after chronic administration of cocaine. Invest. Clin. 34, 181 192.
2. Andersen M. L., Perry J. C., Bignotto M., Perez-Mendes P., Cinini S. M., Mello L. E. Tufik S. (2007) Influence of chronic cocaine treatment and sleep deprivation on sexual behavior and neurogenesis of the male rat. Prog. Neuropsychopharmacol. Biol. Psychiatry 31, 1224 1229.
3. Arumugam T. V., Phillips T. M., Cheng A., Morrell C. H., Mattson M. P. Wan R. (2010) Age and energy intake interact to modify cell stress pathways and stroke outcome. Ann. Neurol. 67, 41 52.
4. Atianjoh F. E., Ladenheim B., Krasnova I. N. Cadet J. L. (2008) Amphetamine causes dopamine depletion and cell death in the mouse olfactory bulb. Eur. J. Pharmacol. 589, 94 97.
5. Barness L. A., Opitz J. M. Gilbert-Barness E. (2007) Obesity: genetic, molecular, and environmental aspects. Am. J. Med. Genet. A 143A, 3016 3034.
6. Bauer L. O. Mott A. E. (1996) Differential effects of cocaine, alcohol, and nicotine dependence on olfactory evoked potentials. Drug Alcohol Depend. 42, 21 26.
7. Baxter L. R. Jr., Schwartz J. M., Phelps M. E., Mazziotta J. C., Barrio J., Rawson R. A., Engel J., Guze B. H., Selin C. Sumida R. (1988) Localization of neurochemical effects of cocaine and other stimulants in the human brain. J. Clin. Psychiatry 49 (Suppl 23 26.
8. Bergström A., Jayatissa M. N., Thykjaer T. Wiborg O. (2007) Molecular pathways associated with stress resilience and drug resistance in the chronic mild stress rat model of depression: a gene expression study. J. Mol. Neurosci. 33, 201 215.
9. Blanchard D. C. Blanchard R. J. (1999) Cocaine potentiates defensive behaviors related to fear and anxiety. Neurosci. Biobehav. Rev. 23, 981 991.
10. Breton-Provencher V., Lemasson M., Peralta M. R. III. Saghatelyan A. (2009) Interneurons produced in adulthood are required for the normal functioning of the olfactory bulb network and for the execution of selected olfactory behaviors. J. Neurosci. 29, 15245 15257.
11. Bruce-Keller A. J., Umberger G., McFall R. Mattson M. P. (1999) Food restriction reduces brain damage and improves behavioral outcome following excitotoxic and metabolic insults. Ann. Neurol. 45, 8 15.
12. Calcagnetti D. J., Quatrella L. A. Schechter M. D. (1996) Olfactory bulbectomy disrupts the expression of cocaine-induced conditioned place preference. Physiol. Behav. 59, 597 604.
13. Costall B., Kelly M. E., Naylor R. J. Onaivi E. S. (1989) The actions of nicotine and cocaine in a mouse model of anxiety. Pharmacol. Biochem. Behav. 33, 197 203.
14. Crawford F. C., Wood M. L., Wilson S. E., Mathura V. S., Hollen T. R., Geall F., Kolippakkam D. N. Mullan M. J. (2006) Cocaine induced inflammatory response in human neuronal progenitor cells. J. Neurochem. 97, 662 674.
15. Dey S. Snow D. M. (2007) Cocaine exposure in vitro induces apoptosis in fetal locus coeruleus neurons through TNF-alpha-mediated induction of Bax and phosphorylated c-Jun NH(2)-terminal kinase. J. Neurochem. 103, 542 556. (Pubitemid 47498012)
16. Di Chiara G., Bassareo V., Fenu S., De Luca M. A., Spina L., Cadoni C., Acquas E., Carboni E., Valentini V. Lecca D. (2004) Dopamine and drug addiction: the nucleus accumbens shell connection. Neuropharmacology 47 (Suppl 1 227 241.
17. Diao L. H., Bickford P. C., Stevens J. O., Cline E. J. Gerhardt G. A. (1997) Caloric restriction enhances evoked DA overflow in striatum and nucleus accumbens of aged Fischer 344 rats. Brain Res. 763, 276 280.
18. Dominguez-Escriba L., Hernandez-Rabaza V., Soriano-Navarro M., Barcia J. A., Romero F. J., Garcia-Verdugo J. M. Canales J. J. (2006) Chronic cocaine exposure impairs progenitor proliferation but spares survival and maturation of neural precursors in adult rat dentate gyrus. Eur. J. Neurosci. 24, 586 594.
19. Duan W. Mattson M. P. (1999) Dietary restriction and 2-deoxyglucose administration improve behavioral outcome and reduce degeneration of dopaminergic neurons in models of Parkinson's disease. J. Neurosci. Res. 57, 195 206.
20. Duan W., Guo Z., Jiang H., Ware M., Li X. J. Mattson M. P. (2003) Dietary restriction normalizes glucose metabolism and BDNF levels, slows disease progression, and increases survival in huntingtin mutant mice. Proc. Natl Acad. Sci. USA 100, 2911 2916.
21. van Duuren E., Lankelma J. Pennartz C. M. (2008) Population coding of reward magnitude in the orbitofrontal cortex of the rat. J. Neurosci. 28, 8590 8603.
22. Everitt B. J., Belin D., Economidou D., Pelloux Y., Dalley J. W. Robbins T. W. (2008) Review. Neural mechanisms underlying the vulnerability to develop compulsive drug-seeking habits and addiction. Philos. Trans. R. Soc. Lond. B Biol. Sci. 363, 3125 3135.
23. Ferriday D. Brunstrom J. M. (2008) How does food-cue exposure lead to larger meal sizes? Br. J. Nutr. 100, 1325 1332.
24. Fumagalli F., Di Pasquale L., Caffino L., Racagni G. Riva M. A. (2007) Repeated exposure to cocaine differently modulates BDNF mRNA and protein levels in rat striatum and prefrontal cortex. Eur. J. Neurosci. 26, 2756 2763.
25. Geiger B. M., Haburcak M., Avena N. M., Moyer M. C., Hoebel B. G. Pothos E. N. (2009) Deficits of mesolimbic dopamine neurotransmission in rat dietary obesity. Neuroscience 159, 1193 1199.
26. Gelegen C., van den Heuvel J., Collier D. A., Campbell I. C., Oppelaar H., Hessel E. Kas M. J. (2008) Dopaminergic and brain-derived neurotrophic factor signalling in inbred mice exposed to a restricted feeding schedule. Genes Brain Behav. 7, 552 559.
27. Gheusi G., Cremer H., McLean H., Chazal G., Vincent J. D. Lledo P. M. (2000) Importance of newly generated neurons in the adult olfactory bulb for odor discrimination. Proc. Natl Acad. Sci. USA 97, 1823 1828.
28. Gordon A. S., Moran D. T., Jafek B. W., Eller P. M. Strahan R. C. (1990) The effect of chronic cocaine abuse on human olfaction. Arch. Otolaryngol. Head Neck Surg. 116, 1415 1418.
29. Hadfield M. G. Milio C. (1992) Cocaine and regional brain monoamines in mice. Pharmacol. Biochem. Behav. 43, 395 403.
30. Halagappa V. K., Guo Z., Pearson M., Matsuoka Y., Cutler R. G., Laferla F. M. Mattson M. P. (2007) Intermittent fasting and caloric restriction ameliorate age-related behavioral deficits in the triple-transgenic mouse model of Alzheimer's disease. Neurobiol. Dis. 26, 212 220.
31. Hall F. S., Li X. F., Sora I., Xu F., Caron M., Lesch K. P., Murphy D. L. Uhl G. R. (2002) Cocaine mechanisms: enhanced cocaine, fluoxetine and nisoxetine place preferences following monoamine transporter deletions. Neuroscience 115, 153 161.
32. Hall F. S., Goeb M., Li X. F., Sora I. Uhl G. R. (2004) μ-Opioid receptor knockout mice display reduced cocaine conditioned place preference but enhanced sensitization of cocaine-induced locomotion. Brain Res. Mol. Brain Res. 121, 123 130.
33. Havrda M. C., Harris B. T., Mantani A., Ward N. M., Paolella B. R., Cuzon V. C., Yeh H. H. Israel M. A. (2008) Id2 is required for specification of dopaminergic neurons during adult olfactory neurogenesis. J. Neurosci. 28, 14074 14086.
34. Hayase T., Yamamoto Y., Yamamoto K., Muso E., Shiota K. Hayashi T. (2003) Similar effects of cocaine and immobilization stress on the levels of heat-shock proteins and stress-activated protein kinases in the rat hippocampus, and on swimming behaviors: the contribution of dopamine and benzodiazepine receptors. Behav. Pharmacol. 14, 551 562.
35. Heilbronn L. K., Smith S. R., Martin C. K., Anton S. D. Ravussin E. (2005) Alternate-day fasting in nonobese subjects: effects on body weight, body composition, and energy metabolism. Am. J. Clin. Nutr. 81, 69 73.
36. Horne M. K., Lee J., Chen F., Lanning K., Tomas D. Lawrence A. J. (2008) Long-term administration of cocaine or serotonin reuptake inhibitors results in anatomical and neurochemical changes in noradrenergic, dopaminergic, and serotonin pathways. J. Neurochem. 106, 1731 1744.
37. Ikemoto S. (2007) Dopamine reward circuitry: two projection systems from the ventral midbrain to the nucleus accumbens-olfactory tubercle complex. Brain Res. Rev. 56, 27 78.
38. Johnson J. B., Summer W., Cutler R. G. et al. (2007) Alternate day calorie restriction improves clinical findings and reduces markers of oxidative stress and inflammation in overweight adults with moderate asthma. Free Radic. Biol. Med. 42, 665 674.
39. Kalivas P. W., Duffy P., DuMars L. A. Skinner C. (1988) Behavioral and neurochemical effects of acute and daily cocaine administration in rats. J. Pharmacol. Exp. Ther. 245, 485 492.
40. Kornetsky C., Huston-Lyons D. Porrino L. J. (1991) The role of the olfactory tubercle in the effects of cocaine, morphine and brain-stimulation reward. Brain Res. 541, 75 81.
41. Krasnova I. N., Ladenheim B., Jayanthi S., Oyler J., Moran T. H., Huestis M. A. Cadet J. L. (2001) Amphetamine-induced toxicity in dopamine terminals in CD-1 and C57BL/6J mice: complex roles for oxygen-based species and temperature regulation. Neuroscience 107, 265 274.
42. Lee J., Duan W. Mattson M. P. (2002) Evidence that brain-derived neurotrophic factor is required for basal neurogenesis and mediates, in part, the enhancement of neurogenesis by dietary restriction in the hippocampus of adult mice. J. Neurochem. 82, 1367 1375.
43. Lee K. J., Kim S. J., Kim S. W. et al. (2006) Chronic mild stress decreases survival, but not proliferation, of new-born cells in adult rat hippocampus. Exp. Mol. Med. 38, 44 54.
44. Lemaire V., Aurousseau C., Le Moal M. Abrous D. N. (1999) Behavioural trait of reactivity to novelty is related to hippocampal neurogenesis. Eur. J. Neurosci. 11, 4006 4014.
45. Li X., Tang X., Jablonska B., Aguirre A., Gallo V. Luskin M. B. (2009) p27(KIP1) regulates neurogenesis in the rostral migratory stream and olfactory bulb of the postnatal mouse. J. Neurosci. 29, 2902 2914.
46. Lutter M. Nestler E. J. (2009) Homeostatic and hedonic signals interact in the regulation of food intake. J. Nutr. 139, 629 632.
47. Lyons D., Friedman D. P., Nader M. A. Porrino L. J. (1996) Cocaine alters cerebral metabolism within the ventral striatum and limbic cortex of monkeys. J. Neurosci. 16, 1230 1238. (Pubitemid 26140879)
48. Martin B., Pearson M., Kebejian L. et al. (2007) Sex-dependent metabolic, neuroendocrine, and cognitive responses to dietary energy restriction and excess. Endocrinology 148, 4318 4333.
49. Martin B., Pearson M., Brenneman R. et al. (2008) Conserved and differential effects of dietary energy intake on the hippocampal transcriptomes of females and males. PLoS ONE 3, e2398.
50. Martin B., Maudsley S., White C. M. Egan J. M. (2009) Hormones in the naso-oropharynx: endocrine modulation of taste and smell. Trends Endocrinol. Metab. 20, 163 170.
51. Maswood N., Young J., Tilmont E. et al. (2004) Caloric restriction increases neurotrophic factor levels and attenuates neurochemical and behavioral deficits in a primate model of Parkinson's disease. Proc. Natl Acad. Sci. USA 101, 18171 18176.
52. McIntyre R. S., McElroy S. L., Konarski J. Z., Soczynska J. K., Bottas A., Castel S., Wilkins K. Kennedy S. H. (2007) Substance use disorders and overweight/obesity in bipolar I disorder: preliminary evidence for competing addictions. J. Clin. Psychiatry 68, 1352 1357.
53. Mennicken F., Savasta M., Peretti-Renucci R. Feuerstein C. (1992) Autoradiographic localization of dopamine uptake sites in the rat brain with 3H-GBR 12935. J. Neural Transm. Gen. Sect. 87, 1 14.
54. Mineur Y. S., Belzung C. Crusio W. E. (2007) Functional implications of decreases in neurogenesis following chronic mild stress in mice. Neuroscience 150, 251 259.
55. Mouret A., Lepousez G., Gras J., Gabellec M. M. Lledo P. M. (2009) Turnover of newborn olfactory bulb neurons optimizes olfaction. J. Neurosci. 29, 12302 12314.
56. Mucignat-Caretta C., Bondi M. Caretta A. (2004) Animal models of depression: olfactory lesions affect amygdala, subventricular zone, and aggression. Neurobiol. Dis. 16, 386 395.
57. Noonan M. A., Choi K. H., Self D. W. Eisch A. J. (2008) Withdrawal from cocaine self-administration normalizes deficits in proliferation and enhances maturity of adult-generated hippocampal neurons. J. Neurosci. 28, 2516 2526.
58. Noonan M. A., Bulin S. E., Fuller D. C. Eisch A. J. (2010) Reduction of adult hippocampal neurogenesis confers vulnerability in an animal model of cocaine addiction. J. Neurosci. 30, 304 315.
59. Parihar V. K., Hattiangady B., Kuruba R., Shuai B. Shetty A. K. (2009) Predictable chronic mild stress improves mood, hippocampal neurogenesis and memory. Mol. Psychiatry [Epub ahead of print].
60. Quach L. A., Wanke C. A., Schmid C. H., Gorbach S. L., Mwamburi D. M., Mayer K. H., Spiegelman D. Tang A. M. (2008) Drug use and other risk factors related to lower body mass index among HIV-infected individuals. Drug Alcohol Depend. 95, 30 36.
61. Rolls E. T. (2006) Brain mechanisms underlying flavour and appetite. Philos. Trans. R. Soc. Lond. B Biol. Sci. 361, 1123 1136.
62. Saunders C., Ferrer J. V., Shi L., Chen J., Merrill G., Lamb M. E., Leeb-Lundberg L. M., Carvelli L., Javitch J. A. Galli A. (2000) Amphetamine-induced loss of human dopamine transporter activity: an internalization-dependent and cocaine-sensitive mechanism. Proc. Natl Acad. Sci. USA 97, 6850 6855.
63. Schifano F. Corkery J. (2008) Cocaine/crack cocaine consumption, treatment demand, seizures, related offences, prices, average purity levels and deaths in the UK (1990-2004). J. Psychopharmacol. 22, 71 79.
64. Sellings L. H., McQuade L. E. Clarke P. B. (2006) Evidence for multiple sites within rat ventral striatum mediating cocaine-conditioned place preference and locomotor activation. J. Pharmacol. Exp. Ther. 317, 1178 1187.
65. Sinha R., Talih M., Malison R., Cooney N., Anderson G. M. Kreek M. J. (2003) Hypothalamic-pituitary-adrenal axis and sympatho-adreno-medullary responses during stress-induced and drug cue-induced cocaine craving states. Psychopharmacology (Berl) 170, 62 72.
66. Stamp J. A., Mashoodh R., van Kampen J. M. Robertson H. A. (2008) Food restriction enhances peak corticosterone levels, cocaine-induced locomotor activity, and DeltaFosB expression in the nucleus accumbens of the rat. Brain Res. 1204, 94 101.
67. Stoeckel L. E., Weller R. E., Cook E. W. III., Twieg D. B., Knowlton R. C. Cox J. E. (2008) Widespread reward-system activation in obese women in response to pictures of high-calorie foods. Neuroimage 41, 636 647.
68. Stranahan A. M., Arumugam T. V., Cutler R. G., Lee K., Egan J. M. Mattson M. P. (2008) Diabetes impairs hippocampal function through glucocorticoid- mediated effects on new and mature neurons. Nat. Neurosci. 11, 309 317.
69. Stranahan A. M., Lee K., Martin B., Maudsley S., Golden E., Cutler R. G. Mattson M. P. (2009) Voluntary exercise and caloric restriction enhance hippocampal dendritic spine density and BDNF levels in diabetic mice. Hippocampus 19, 951 961.
70. Szczypka M. S., Rainey M. A. Palmiter R. D. (2000) Dopamine is required for hyperphagia in Lep(ob/ob) mice. Nat. Genet. 25, 102 104.
71. Teegarden S. L., Scott A. N. Bale T. L. (2009) Early life exposure to a high fat diet promotes long-term changes in dietary preferences and central reward signaling. Neuroscience 162, 924 932.
72. Volkow N. D., Wang G. J., Fowler J. S. Telang F. (2008) Overlapping neuronal circuits in addiction and obesity: evidence of systems pathology. Philos. Trans. R. Soc. Lond. B Biol. Sci. 363, 3191 3200.
73. Wan R., Camandola S. Mattson M. P. (2003) Intermittent food deprivation improves cardiovascular and neuroendocrine responses to stress in rats. J. Nutr. 133, 1921 1929.
74. Whitman M. C. Greer C. A. (2009) Adult neurogenesis and the olfactory system. Prog. Neurobiol. 89, 162 175.
75. Xu X., Zhan M., Duan W. et al. (2007) Gene expression atlas of the mouse central nervous system: impact and interactions of age, energy intake and gender. Genome Biol. 8, R234.
76. Yamaguchi M., Suzuki T., Seki T., Namba T., Juan R., Arai H., Hori T. Asada T. (2004) Repetitive cocaine administration decreases neurogenesis in adult rat hippocampus. Ann. N Y Acad. Sci. 1025, 351 362.