Role of the locus coeruleus in enhanced orexin A-induced spontaneous physical activity in obesity-resistant rats

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 305, Issue 11, 2013, Pages

  Teske, Jennifer A ^a,b,d,e   Perez Leighton, Claudio E ^f   Billington, Charles J ^b,d,e,g   Kotz, Catherine M ^b,c,d,e,g  

^a UNIVERSITY OF ARIZONA   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c GERIATRIC RESEARCH EDUCATION AND CLINICAL CENTER   (United States)

^d University of Minnesota   (United States)

^e UNIVERSITY OF MINNESOTA   (United States)

^f UNIVERSIDAD ANDRÉS BELLO   (Chile)

^g UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

Brain; Diet induced obesity

Indexed keywords

OREXIN A;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY COMPOSITION; CONTROLLED STUDY; ENERGY EXPENDITURE; FEEDING; LOCUS CERULEUS; MALE; NONHUMAN; OBESITY; PHYSICAL ACTIVITY; PRIORITY JOURNAL; RAT;

BRAIN; DIET-INDUCED OBESITY;

ADIPOSITY; ANIMALS; BODY COMPOSITION; ENERGY METABOLISM; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LOCUS COERULEUS; MALE; MOTOR ACTIVITY; NEUROPEPTIDES; OBESITY; PHENOTYPE; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84889560905     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00229.2013     Document Type: Article

References (56)

1. Adamantidis AR, Zhang F, Aravanis AM, Deisseroth K, de Lecea L. Neural substrates of awakening probed with optogenetic control of hypocretin neurons. Nature 450: 420-424, 2007.
2. Arch JR, Hislop D, Wang SJ, Speakman JR. Some mathematical and technical issues in the measurement and interpretation of open-circuit indirect calorimetry in small animals. Int J Obes (Lond) 30: 1322-1331, 2006.
3. Bernard R, Lydic R, Baghdoyan HA. Hypocretin-1 activates G proteins in arousal-related brainstem nuclei of rat. Neuroreport 13: 447-450, 2002.
4. Berridge CW, Schmeichel BE, Espana RA. Noradrenergic modulation of wakefulness/arousal. Sleep Med Rev 16: 187-197, 2012.
5. Bourgin P, Huitron-Resendiz S, Spier AD, Fabre V, Morte B, Criado JR, Sutcliffe JG, Henriksen SJ, de Lecea L. Hypocretin-1 modulates rapid eye movement sleep through activation of locus coeruleus neurons. J Neurosci 20: 7760-7765, 2000.
6. Butler AA, Kozak LP. A recurring problem with the analysis of energy expenditure in genetic models expressing lean and obese phenotypes. Diabetes 59: 323-329, 2010.
7. Chu N, Bloom FE. Norepinephrine-containing neurons: changes in spontaneous discharge patterns during sleeping and waking. Science 179: 908-910, 1973.
8. D'Haeseleer P. How does gene expression clustering work? Nat Biotechnol 23: 1499-1501, 2005.
9. de Araujo IE, Ferreira JG, Tellez LA, Ren X, Yeckel CW. The gut-brain dopamine axis: a regulatory system for caloric intake. Physiol Behav 106: 394-399, 2012.
10. de Lecea L, Kilduff TS, Peyron C, Gao X, Foye PE, Danielson PE, Fukuhara C, Battenberg EL, Gautvik VT, Bartlett FS, 2nd Frankel WN, van den Pol AN, Bloom FE, Gautvik KM, Sutcliffe JG. The hypocretins: hypothalamus-specific peptides with neuroexcitatory activity. Proc Natl Acad Sci USA 95: 322-327, 1998.
11. Even PC, Nadkarni NA. Indirect calorimetry in laboratory mice and rats: principles, practical considerations, interpretation and perspectives. Am J Physiol Regul Integr Comp Physiol 303: R459-R476, 2012.
12. Greco MA, Shiromani PJ. Hypocretin receptor protein and mRNA expression in the dorsolateral pons of rats. Brain Res Mol Brain Res 88: 176-182, 2001.
13. Hagan JJ, Leslie RA, Patel S, Evans ML, Wattam TA, Holmes S, Benham CD, Taylor SG, Routledge C, Hemmati P, Munton RP, Ashmeade TE, Shah AS, Hatcher JP, Hatcher PD, Jones DN, Smith MI, Piper DC, Hunter AJ, Porter RA, Upton N. Orexin A activates locus coeruleus cell firing and increases arousal in the rat. Proc Natl Acad Sci USA 96: 10911-10916, 1999.
14. Hara J, Beuckmann CT, Nambu T, Willie JT, Chemelli RM, Sinton CM, Sugiyama F, Yagami K, Goto K, Yanagisawa M, Sakurai T. Genetic ablation of orexin neurons in mice results in narcolepsy, hypophagia, and obesity. Neuron 30: 345-354, 2001.
15. Horvath TL, Peyron C, Diano S, Ivanov A, Aston-Jones G, Kilduff TS, van Den Pol AN. Hypocretin (orexin) activation and synaptic innervation of the locus coeruleus noradrenergic system. J Comp Neurol 415: 145-159, 1999.
16. Hunter GR, Byrne NM. Physical activity and muscle function but not resting energy expenditure impact on weight gain. J Strength Cond Res 19: 225-230, 2005.
17. Kiyashchenko LI, Mileykovskiy BY, Maidment N, Lam HA, Wu MF, John J, Peever J, Siegel JM. Release of hypocretin (orexin) during waking and sleep states. J Neurosci 22: 5282-5286, 2002.
18. Kotz C, Nixon J, Butterick T, Perez-Leighton C, Teske J, Billington C. Brain orexin promotes obesity resistance. Ann NY Acad Sci 1264: 72-86, 2012.
19. Kotz CM, Levine AS, Billington CJ. Effect of naltrexone on feeding, neuropeptide Y and uncoupling protein gene expression during lactation. Neuroendocrinology 65: 259-264, 1997.
20. Kotz CM, Teske JA, Billington CJ. Neuroregulation of nonexercise activity thermogenesis and obesity resistance. Am J Physiol Regul Integr Comp Physiol 294: R699-R710, 2008.
21. Kotz CM, Teske JA, Levine JA, Wang C. Feeding and activity induced by orexin A in the lateral hypothalamus in rats. Regul Pept 104: 27-32, 2002.
22. Kotz CM, Wang C, Teske JA, Thorpe AJ, Novak CM, Kiwaki K, Levine JA. Orexin A mediation of time spent moving in rats: neural mechanisms. Neuroscience 142: 29-36, 2006.
23. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2[-delta delta C(T)] method. Methods 25: 402-408, 2001.
24. MacLean PS, Higgins JA, Johnson GC, Fleming-Elder BK, Donahoo WT, Melanson EL, Hill JO. Enhanced metabolic efficiency contributes to weight regain after weight loss in obesity-prone rats. Am J Physiol Regul Integr Comp Physiol 287: R1306-R1315, 2004.
25. Mavanji V, Teske JA, Billington CJ, Kotz CM. Elevated sleep quality and orexin receptor mRNA in obesity-resistant rats. Int J Obes (Lond) 34: 1576-1588, 2010.
26. Miller GA, Chapman JP. Misunderstanding analysis of covariance. J Abnorm Psychol 110: 40-48, 2001.
27. Nelson MC, Story M, Larson NI, Neumark-Sztainer D, Lytle LA. Emerging adulthood and college-aged youth: an overlooked age for weight-related behavior change. Obesity (Silver Spring) 16: 2205-2211, 2008.
28. Nicholson C. Diffusion from an injected volume of a substance in brain tissue with arbitrary volume fraction and tortuosity. Brain Res 333: 325-329, 1985.
29. Nixon JP, Kotz CM, Novak CM, Billington CJ, Teske JA. Neuropeptides controlling energy balance: orexins and neuromedins. Hand Exp Pharmacol 209: 77-109, 2012.
30. Novak CM, Escande C, Burghardt PR, Zhang M, Barbosa MT, Chini EN, Britton SL, Koch LG, Akil H, Levine JA. Spontaneous activity, economy of activity, and resistance to diet-induced obesity in rats bred for high intrinsic aerobic capacity. Horm Behav 58: 355-367, 2010.
31. Novak CM, Jiang X, Wang C, Teske JA, Kotz CM, Levine JA. Caloric restriction and physical activity in zebrafish (Danio rerio). Neurosci Lett 383: 99-104, 2005.
32. Novak CM, Kotz CM, Levine JA. Central orexin sensitivity, physical activity, and obesity in diet-induced obese and diet-resistant rats. Am J Physiol Endocrinol Metab 290: E396-E403, 2006.
33. Novak CM, Levine JA. Daily intraparaventricular orexin-A treatment induces weight loss in rats. Obesity (Silver Spring) 17: 1493-1498, 2009.
34. Overton JM. Phenotyping small animals as models for the human metabolic syndrome: thermoneutrality matters. Int J Obes (Lond) 34, Suppl 2: S53-S58, 2010.
35. Paxinos G, Watson C, Pennisi M, Topple A. Bregma, lambda and the interaural midpoint in stereotaxic surgery with rats of different sex, strain and weight. J Neurosci Methods 13: 139-143, 1985.
36. Perez-Leighton CE, Boland K, Teske JA, Billington C, Kotz CM. Behavioral responses to orexin, orexin receptor gene expression, and spontaneous physical activity contribute to individual sensitivity to obesity. Am J Physiol Endocrinol Metab 303: E865-E874, 2012.
37. Peyron C, Tighe DK, van den Pol AN, de Lecea L, Heller HC, Sutcliffe JG, Kilduff TS. Neurons containing hypocretin (orexin) project to multiple neuronal systems. J Neurosci 18: 9996-10015, 1998.
38. Picker MJ, Allen RM, Morgan D, Levine AS, O'Hare E, Cleary JP. Effects of neuropeptide Y on the discriminative stimulus and antinociceptive properties of morphine. Pharmacol Biochem Behav 64: 161-164, 1999.
39. Ricci MR, Levin BE. Ontogeny of diet-induced obesity in selectively bred Sprague-Dawley rats. Am J Physiol Regul Integr Comp Physiol 285: R610-R618, 2003.
40. Ringner M. What is principal component analysis? Nat Biotechnol 26: 303-304, 2008.
41. Sakata T, Yoshimatsu H, Kurokawa M. Hypothalamic neuronal histamine: implications of its homeostatic control of energy metabolism. Nutrition 13: 403-411, 1997.
42. Sakurai T, Amemiya A, Ishii M, Matsuzaki I, Chemelli RM, Tanaka H, Williams SC, Richardson JA, Kozlowski GP, Wilson S, Arch JR, Buckingham RE, Haynes AC, Carr SA, Annan RS, McNulty DE, Liu WS, Terrett JA, Elshourbagy NA, Bergsma DJ, Yanagisawa M. Orexins and orexin receptors: a family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior. Cell 92: 573-585, 1998.
43. Stacklies W, Redestig H, Scholz M, Walther D, Selbig J. pcaMethods-a bioconductor package providing PCA methods for incomplete data. Bioinformatics 23: 1164-1167, 2007.
44. Sunter D, Morgan I, Edwards CM, Dakin CL, Murphy KG, Gardiner J, Taheri S, Rayes E, Bloom SR. Orexins: effects on behavior and localisation of orexin receptor 2 messenger ribonucleic acid in the rat brainstem. Brain Res 907: 27-34, 2001.
45. Tallett AJ, Blundell JE, Rodgers RJ. Sibutramine-induced anorexia: potent, dose-dependent and behaviourally-selective profile in male rats. Behav Brain Res 198: 359-365, 2009.
46. Team RC. R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing, 2013.
47. Teske JA, Billington CJ, Kuskowski MA, Kotz CM. Spontaneous physical activity protects against fat mass gain. Int J Obes (Lond) 36: 603-613, 2012.
48. Teske JA, Kotz CM. Effect of acute and chronic caloric restriction and metabolic glucoprivation on spontaneous physical activity in obesityprone and obesity-resistant rats. Am J Physiol Regul Integr Comp Physiol 297: R176-R184, 2009.
49. Teske JA, Levine AS, Kuskowski M, Levine JA, Kotz CM. Elevated hypothalamic orexin signaling, sensitivity to orexin A, and spontaneous physical activity in obesity-resistant rats. Am J Physiol Regul Integr Comp Physiol 291: R889-R899, 2006.
50. Thorpe AJ, Mullett MA, Wang C, Kotz CM. Peptides that regulate food intake: regional, metabolic, and circadian specificity of lateral hypothalamic orexin A feeding stimulation. Am J Physiol Regul Integr Comp Physiol 284: R1409-R1417, 2003.
51. Troyanskaya O, Cantor M, Sherlock G, Brown P, Hastie T, Tibshirani R, Botstein D, Altman RB. Missing value estimation methods for DNA microarrays. Bioinformatics 17: 520-525, 2001.
52. Tschop MH, Speakman JR, Arch JR, Auwerx J, Bruning JC, Chan L, Eckel RH, Farese RV Jr, Galgani JE, Hambly C, Herman MA, Horvath TL, Kahn BB, Kozma SC, Maratos-Flier E, Muller TD, Munzberg H, Pfluger PT, Plum L, Reitman ML, Rahmouni K, Shulman GI, Thomas G, Kahn CR, Ravussin E. A guide to analysis of mouse energy metabolism. Nat Methods 9: 57-63, 2012.
53. Tsunematsu T, Kilduff TS, Boyden ES, Takahashi S, Tominaga M, Yamanaka A. Acute optogenetic silencing of orexin/hypocretin neurons induces slow-wave sleep in mice. J Neurosci 31: 10529-10539, 2011.
54. van den Pol AN, Ghosh PK, Liu RJ, Li Y, Aghajanian GK, Gao XB. Hypocretin (orexin) enhances neuron activity and cell synchrony in developing mouse GFP-expressing locus coeruleus. J Physiol 541: 169-185, 2002.
55. Wang C, Bomberg E, Billington C, Levine A, Kotz CM. Brain-derived neurotrophic factor in the hypothalamic paraventricular nucleus increases energy expenditure by elevating metabolic rate. Am J Physiol Regul Integr Comp Physiol 293: R992-R1002, 2007.
56. Wellman PJ. Norepinephrine and the control of food intake. Nutrition 16: 837-842, 2000.