Mice with selective elimination of striatal acetylcholine release are lean, show altered energy homeostasis and changed sleep/wake cycle

Journal of Neurochemistry

Volumn 124, Issue 5, 2013, Pages 658-669

  Guzman, Monica S ^a,b   De Jaeger, Xavier ^a,b   Drangova, Maria ^a,b   Prado, Marco A M ^a,b   Gros, Robert ^a,b   Prado, Vania F ^a,b  

^a ROBARTS RESEARCH INSTITUTE   (Canada)

^b WESTERN UNIVERSITY   (Canada)

Author keywords

body weight; insulin; leptin; metabolism; striatum; VAChT

Indexed keywords

ACETYLCHOLINE; INSULIN; LEPTIN; VESICULAR ACETYLCHOLINE TRANSPORTER;

ACETYLCHOLINE RELEASE; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CHOLINERGIC ACTIVITY; CONTROLLED STUDY; ENERGY BALANCE; ENERGY EXPENDITURE; FOOD INTAKE; GROWTH RATE; HORMONE BLOOD LEVEL; INSULIN BLOOD LEVEL; LEAN BODY WEIGHT; LEPTIN BLOOD LEVEL; MALE; METABOLIC REGULATION; MOUSE MUTANT; NONHUMAN; PHENOTYPE; PHYSICAL ACTIVITY; PRIORITY JOURNAL; SLEEP WAKING CYCLE; STRIATE CORTEX; WAKEFULNESS;

ACETYLCHOLINE; ANIMALS; BODY WEIGHT; CORPUS STRIATUM; ENERGY METABOLISM; HOMEOSTASIS; IMMUNOHISTOCHEMISTRY; MICE; MICE, KNOCKOUT; POLYMERASE CHAIN REACTION; SLEEP; VESICULAR ACETYLCHOLINE TRANSPORT PROTEINS;

MUS;

EID: 84874118295     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.12128     Document Type: Article

References (45)

1. Avena N. M., and, Rada P. V., (2012) Cholinergic modulation of food and drug satiety and withdrawal. Physiol. Behav. 106, 332-336.
2. Avena N. M., Rada P., Moise N., and, Hoebel B. G., (2006) Sucrose sham feeding on a binge schedule releases accumbens dopamine repeatedly and eliminates the acetylcholine satiety response. Neuroscience 139, 813-820.
3. Balthasar N., Dalgaard L. T., Lee C. E., et al,. (2005) Divergence of melanocortin pathways in the control of food intake and energy expenditure. Cell 123, 493-505. (Pubitemid 41546678)
4. Benoit S. C., Air E. L., Coolen L. M., Strauss R., Jackman A., Clegg D. J., Seeley R. J., and, Woods S. C., (2002) The catabolic action of insulin in the brain is mediated by melanocortins. J. Neurosci. 22, 9048-9052. (Pubitemid 35379074)
5. Bi S., Robinson B. M., and, Moran T. H., (2003) Acute food deprivation and chronic food restriction differentially affect hypothalamic NPY mRNA expression. Am. J. Physiol. Regul. Integr. Comp. Physiol. 285, R1030-R1036. (Pubitemid 37296354)
6. de Castro B. M., De J. X, Martins-Silva C., et al,. (2009a) The vesicular acetylcholine transporter is required for neuromuscular development and function. Mol. Cell. Biol. 29, 5238-5250.
7. de Castro B. M., Pereira G. S., Magalhaes V., et al,. (2009b) Reduced expression of the vesicular acetylcholine transporter causes learning deficits in mice. Genes Brain Behav. 8, 23-35.
8. Comella C. L., (2007) Sleep disorders in Parkinson's disease: an overview. Mov. Disord. 22 (Suppl 17), S367-S373. (Pubitemid 350134190)
9. Dankner R., Chetrit A., Shanik M. H., Raz I., and, Roth J., (2009) Basal-state hyperinsulinemia in healthy normoglycemic adults is predictive of type 2 diabetes over a 24-year follow-up: a preliminary report. Diabetes Care 32, 1464-1466.
10. Detombe S. A., Dunmore-Buyze J., and, Drangova M., (2012) Evaluation of eXIA 160 cardiac-related enhancement in C57BL/6 and BALB/c mice using micro-CT. Contrast Media Mol. Imaging 7, 240-246.
11. Elmquist J. K., Elias C. F., and, Saper C. B., (1999) From lesions to leptin: hypothalamic control of food intake and body weight. Neuron 22, 221-232. (Pubitemid 29109657)
12. Gadea-Ciria M., Stadler H., Lloyd K. G., and, Bartholini G., (1973) Acetylcholine release within the cat striatum during the sleep-wakefulness cycle. Nature 243, 518-519.
13. Granton P. V., Norley C. J., Umoh J., Turley E. A., Frier B. C., Noble E. G., and, Holdsworth D. W., (2010) Rapid in vivo whole body composition of rats using cone beam muCT. J. Appl. Physiol. 109, 1162-1169.
14. Gras C., Amilhon B., Lepicard E. M., et al,. (2008) The vesicular glutamate transporter VGLUT3 synergizes striatal acetylcholine tone. Nat. Neurosci. 11, 292-300. (Pubitemid 351311799)
15. Guzman M. S., De Jaeger X., Raulic S., et al,. (2011) Elimination of the vesicular acetylcholine transporter in the striatum reveals regulation of behaviour by cholinergic-glutamatergic co-transmission. PLoS Biol. 9, e1001194. doi: 10.1371/journal.pbio.1001194.
16. Hajnal A., Szekely M., Galosi R., and, Lenard L., (2000) Accumbens cholinergic interneurons play a role in the regulation of body weight and metabolism. Physiol. Behav. 70, 95-103.
17. Hanin I., (1996) The AF64A model of cholinergic hypofunction: an update. Life Sci. 58, 1955-1964. (Pubitemid 26160433)
18. Hernandez-Peon R., O'Flaherty J. J., and, Mazzuchelli O. 'F., (1967) Sleep and other behavioural effects induced by acetylcholinic stimulation of basal temporal cortex and striate structures. Brain Res. 4, 243-267.
19. Higley M. J., Gittis A. H., Oldenburg I. A., Balthasar N., Seal R. P., Edwards R. H., Lowell B. B., Kreitzer A. C., and, Sabatini B. L., (2011) Cholinergic interneurons mediate fast VGluT3-dependent glutamatergic transmission in the striatum. PLoS ONE 6, e19155.
20. Hikida T., Kitabatake Y., Pastan I., and, Nakanishi S., (2003) Acetylcholine enhancement in the nucleus accumbens prevents addictive behaviors of cocaine and morphine. Proc. Natl Acad. Sci. USA 100, 6169-6173. (Pubitemid 36576949)
21. Hoebel B. G., Avena N. M., and, Rada P., (2007) Accumbens dopamine-acetylcholine balance in approach and avoidance. Curr. Opin. Pharmacol. 7, 617-627. (Pubitemid 350177561)
22. Kaneko S., Hikida T., Watanabe D., Ichinose H., Nagatsu T., Kreitman R. J., Pastan I., and, Nakanishi S., (2000) Synaptic integration mediated by striatal cholinergic interneurons in basal ganglia function. Science 289, 633-637. (Pubitemid 30622070)
23. Lima R. F., Prado V. F., Prado M. A., and, Kushmerick C., (2010) Quantal release of acetylcholine in mice with reduced levels of the vesicular acetylcholine transporter. J. Neurochem. 113, 943-951.
24. Mark G. P., Rada P., Pothos E., and, Hoebel B. G., (1992) Effects of feeding and drinking on acetylcholine release in the nucleus accumbens, striatum, and hippocampus of freely behaving rats. J. Neurochem. 58, 2269-2274.
25. Mark G. P., Shabani S., Dobbs L. K., and, Hansen S. T., (2011) Cholinergic modulation of mesolimbic dopamine function and reward. Physiol. Behav. 104, 76-81.
26. Martins-Silva C., De J. X, Guzman M. S., Lima R. D., Santos M. S., Kushmerick C., Gomez M. V., Caron M. G., Prado M. A., and, Prado V. F., (2011) Novel strains of mice deficient for the vesicular acetylcholine transporter: insights on transcriptional regulation and control of locomotor behavior. PLoS ONE 6, e17611.
27. McGaughy J., Everitt B. J., Robbins T. W., and, Sarter M., (2000) The role of cortical cholinergic afferent projections in cognition: impact of new selective immunotoxins. Behav. Brain Res. 115, 251-263.
28. Mena-Segovia J., Cintra L., Prospero-Garcia O., and, Giordano M., (2002) Changes in sleep-waking cycle after striatal excitotoxic lesions. Behav. Brain Res. 136, 475-481. (Pubitemid 35333263)
29. Nonogaki K., (2000) New insights into sympathetic regulation of glucose and fat metabolism. Diabetologia 43, 533-549. (Pubitemid 30322070)
30. Pack A. I., Galante R. J., Maislin G., et al,. (2007) Novel method for high-throughput phenotyping of sleep in mice. Physiol. Genomics 28, 232-238. (Pubitemid 46702010)
31. Palmiter R. D., (2007) Is dopamine a physiologically relevant mediator of feeding behavior? Trends Neurosci. 30, 375-381. (Pubitemid 47088716)
32. Pisani A., Bernardi G., Ding J., and, Surmeier D. J., (2007) Re-emergence of striatal cholinergic interneurons in movement disorders. Trends Neurosci. 30, 545-553. (Pubitemid 47513239)
33. Plum L., Lin H. V., Dutia R., et al,. (2009) The obesity susceptibility gene Cpe links FoxO1 signaling in hypothalamic pro-opiomelanocortin neurons with regulation of food intake. Nat. Med. 15, 1195-1201.
34. Prado V. F., Martins-Silva C., de Castro B. M., et al,. (2006) Mice deficient for the vesicular acetylcholine transporter are myasthenic and have deficits in object and social recognition. Neuron 51, 601-612. (Pubitemid 44314080)
35. Pratt W. E., and, Blackstone K., (2009) Nucleus accumbens acetylcholine and food intake: decreased muscarinic tone reduces feeding but not food-seeking. Behav. Brain Res. 198, 252-257.
36. Pratt W. E., and, Kelley A. E., (2005) Striatal muscarinic receptor antagonism reduces 24-h food intake in association with decreased preproenkephalin gene expression. Eur. J. Neurosci. 22, 3229-3240. (Pubitemid 43002006)
37. Qiu M. H., Vetrivelan R., Fuller P. M., and, Lu J., (2010) Basal ganglia control of sleep-wake behavior and cortical activation. Eur. J. Neurosci. 31, 499-507.
38. Rossi J., Balthasar N., Olson D., Scott M., Berglund E., Lee C. E., Choi M. J., Lauzon D., Lowell B. B., and, Elmquist J. K., (2011) Melanocortin-4 receptors expressed by cholinergic neurons regulate energy balance and glucose homeostasis. Cell Metab. 13, 195-204.
39. Schwartz M. W., Seeley R. J., Woods S. C., Weigle D. S., Campfield L. A., Burn P., and, Baskin D. G., (1997) Leptin increases hypothalamic pro-opiomelanocortin mRNA expression in the rostral arcuate nucleus. Diabetes 46, 2119-2123. (Pubitemid 27512108)
40. Schwartz M. W., Woods S. C., Porte D. Jr, Seeley R. J., and, Baskin D. G., (2000) Central nervous system control of food intake. Nature 404, 661-671. (Pubitemid 30205071)
41. Shanik M. H., Xu Y., Skrha J., Dankner R., Zick Y., and, Roth J., (2008) Insulin resistance and hyperinsulinemia: is hyperinsulinemia the cart or the horse? Diabetes Care 31 (Suppl 2), S262-S268.
42. Tepper J. M., Sharpe N. A., Koos T. Z., and, Trent F., (1998) Postnatal development of the rat neostriatum: electrophysiological, light- and electron-microscopic studies. Dev. Neurosci. 20, 125-145. (Pubitemid 28349869)
43. Yamada M., Miyakawa T., Duttaroy A., et al,. (2001) Mice lacking the M3 muscarinic acetylcholine receptor are hypophagic and lean. Nature 410, 207-212. (Pubitemid 32216592)
44. Yeo G. S., and, Heisler L. K., (2012) Unraveling the brain regulation of appetite: lessons from genetics. Nat. Neurosci. 15, 1343-1349.
45. Yin F. C., Spurgeon H. A., Rakusan K., Weisfeldt M. L., and, Lakatta E. G., (1982) Use of tibial length to quantify cardiac hypertrophy: application in the aging rat. Am. J. Physiol. 243, H941-H947. (Pubitemid 13169525)