Integration of stress and leptin signaling by CART producing neurons in the rodent midbrain centrally projecting Edinger-Westphal nucleus

Frontiers in Neuroanatomy

Volumn 8, Issue MAR, 2014, Pages

  Xu, Lu ^a   Janssen, Donny ^a   van der Knaap, Noortje ^a   Roubos, Eric W ^a   Leshan, Rebecca L ^b   Myers Jr , Martin G ^b   Gaszner, Balazs ^c   Kozicz, Tamás ^a  

^a RADBOUD UNIVERSITY   (Netherlands)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF PÉCS   (Hungary)

Author keywords

Centrally projecting Edinger Westphal nucleus; db db mice; Depression; Fasting; Obesity; Restraint

Indexed keywords

COCAINE AND AMPHETAMINE REGULATED TRANSCRIPT PEPTIDE; LEPTIN; LEPTIN RECEPTOR; MESSENGER RNA;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIET RESTRICTION; EDINGER WESTPHAL NUCLEUS; ENERGY METABOLISM; GENE EXPRESSION; IMAGE ANALYSIS; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; MESENCEPHALON; MOUSE; NERVE CELL; NERVE CELL STIMULATION; NONHUMAN; ONCOGENE C FOS; PROTEIN EXPRESSION; RAT; STRESS;

EID: 84896930584     PISSN: 16625129     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnana.2014.00008     Document Type: Article

References (52)

1. Ahima, R. S., and Osei, S. Y. (2004). Leptin signaling. Physiol. Behav. 81, 223-241. doi: 10.1016/j.physbeh.2004.02.014
2. Bittencourt, J. C., Vaughan, J., Arias, C., Rissman, R. A., Vale, W. W., and Sawchenko, P. E. (1999). Urocortin expression in rat brain: evidence against a pervasive relationship of urocortin-containing projections with targets bearing type 2 CRF receptors. J. Comp. Neurol. 415, 285-312. doi: 10.1002/(SICI)1096- 9861(19991220)415:3<285::AID-CNE1>3.0.C0;2-0
3. Bloem, B., Xu, L., Morava, E., Faludi, G., Palkovits, M., Roubos, E. W., et al. (2012). Sex-specific differences in the dynamics of cocaine- and amphetamine-regulated transcript and nesfatin-1 expressions in the midbrain of depressed suicide victims vs. controls. Neuropharmacology 62, 297-303. doi: 10.1016/j.neuropharm.2011.07.023
4. Campfield, L.A., Smith, F. J., Guisez, Y., Devos, R., and Burn, P. (1995). Recombinant mouse OB protein: evidence for a peripheral signal linking adiposity and central neural networks. Science 269, 546-549. doi: 10.1126/science.7624778
5. Cespedes, I. C., de Oliveira, A. R., da Silva, J. M., da Silva, A. V., Sita, L. V., and Bittencourt, J. C. (2010). mRNA expression of corticotropin-releasing factor and urocortin 1 after restraint and foot shock together with alprazolam administration. Peptides 31, 2200-2208. doi: 10.1016/j.peptides.2010. 08.022
6. Chrousos, G. P., and Gold, P. W. (1992). The concepts of stress and stress system disorders. Overview of physical and behavioral homeostasis. JAMA 267, 1244-1252. doi: 10.1001/jama.1992.03480090092034
7. Dandekar, M. P., Singru, P. S., Kokare, D. M., and Subhedar, N. K. (2009). Cocaine- and amphetamine-regulated transcript peptide plays a role in the manifestation of depression: social isolation and olfactory bulbectomy models reveal unifying principles. Neuropsychopharmacology 34, 1288-1300. doi: 10.1038/npp. 2008.201
8. Da Silva, A. V., Torres, K. R., Haemmerle, C. A., Cespedes, I. C., and Bittencourt, J. C. (2013). The Edinger-Westphal nucleus II: hypothalamic afferents in the rat. J. Chem. Neuroanat. 54, 5-19. doi: 10.1016/j.jchemneu.2013.04.001
9. Date, Y., Kojima, M., Hosoda, H., Sawaguchi, A., Mondal, M. S., Suganuma, T., et al. (2000). Ghrelin, a novel growth hormone-releasing acylated peptide, is synthesized in a distinct endocrine cell type in the gastrointestinal tracts of rats and humans. Endocrinology 141, 4255-4261. doi: 10.1210/endo.141. 11.7757
10. Dietrich, M. O., and Horvath, T. L. (2009). Feeding signals and brain circuitry. Eur. J. Neurosci. 30, 1688-1696. doi: 10.1111/j.1460-9568.2009.06963.x
11. Dominguez, G., Lakatos, A., and Kuhar, M. J. (2002). Characterization of the cocaine- and amphetamine-regulated transcript (CART) peptide gene promoter and its activation by a cyclic AMP-dependent signaling pathway in GH3 cells. J. Neurochem. 80, 885-893. doi: 10.1046/j.0022-3042.2002.00775.x
12. Gaszner, B., Csernus, V., and Kozicz, T. (2004). Urocortinergic neurons respond in a differentiated manner to various acute stressors in the Edinger-Westphal nucleus in the rat. J. Comp. Neurol. 480, 170-179. doi: 10.1002/cne.20343
13. Gorska, E., Popko, K., Stelmaszczyk-Emmel, A., Ciepiela, O., Kucharska, A., and Wasik, M. (2010). Leptin receptors. Eur. J. Med. Res. 15(Suppl. 2), 50-54.
14. Hakansson, M. L., and Meister, B. (1998). Transcription factor STAT3 in leptin target neurons of the rat hypothalamus. Neuroendocrinology 68, 420-427. doi: 10.1159/000054392
15. Haque, Z., Akbar, N., Yasmin, F., Haleem, M. A., and Haleem, D. J. (2013). Inhibition of immobilization stress-induced anorexia, behavioral deficits, and plasmacorticosterone secretion by injected leptin in rats. Stress 16, 353-362. doi: 10.3109/10253890.2012.736047
16. Heiman, M. L., Ahima, R. S., Craft, L. S., Schoner, B., Stephens, T. W., and Flier, J. S. (1997). Leptin inhibition of the hypothalamic-pituitary-adrenal axis in response to stress. Endocrinology 138, 3859-3863. doi: 10.1210/endo.138.9.5366
17. Huo, L., Munzberg, H., Nillni, E. A., and Bjørbaek, C. (2004). Role of signal transducer and activator of transcription 3 in regulation of hypothalamic trh gene expression by leptin. Endocrinology 145, 2516-2523. doi: 10.1210/en.2003-1242
18. Kalra, S. P., Dube, M. G., Pu, S., Xu, B., Horvath, T. L., and Kalra, P. S. (1999). Interacting appetite-regulating pathways in the hypothalamic regulation of body weight. Endocr. Rev. 20, 68-100. doi: 10.1210/edrv.20.1.0357
19. Korosi, A., Schotanus, S., Olivier, B., Roubos, E. W., and Kozicz, T. (2005). Chronic ether stress-induced response of urocortin 1 neurons in the Edinger-Westphal nucleus in the mouse. Brain Res. 1046, 172-179. doi: 10.1016/j.brainres.2005.04.012
20. Koylu, E. O., Couceyro, P. R., Lambert, P. D., Ling, N. C., DeSouza, E. B., and Kuhar, M. J. (1997). Immunohistochemical localization of novel CART peptides in rat hypothalamus, pituitary and adrenal gland. J. Neuroendocrinol. 9, 823-833. doi: 10.1046/j.1365-2826.1997.00651.x
21. Kozicz, T. (2003). Neurons colocalizing urocortin and cocaine and amphetamine- regulated transcript immunoreactivities are induced by acute lipopolysaccharide stress in the Edinger-Westphal nucleus in the rat. Neuroscience 116, 315-320. doi: 10.1016/S0306-4522(02)00772-8
22. Kozicz, T. (2007). On the role of urocortin 1 in the non-preganglionic Edinger- Westphal nucleus in stress adaptation. Gen. Comp. Endocrinol. 153,235-240. doi: 10.1016/j.ygcen.2007.04.005
23. Kozicz, T., Li, M., and Arimura, A. (2001). The activation of urocortin immunore- active neurons in the Einger-Westphal nucleus following stress in rats. Stress 4, 85-90. doi: 10.3109/10253890109115724
24. Kozicz, T., Sterrenburg, L., and Xu, L. (2011). Does midbrain urocortin 1 matter? A 15-year journey from stress (mal)adaptation to energy metabolism. Stress 14, 376-383. doi: 10.3109/10253890.2011.563806
25. Levene, H. (1960). Robust tests for equality of variances, in Contributions to Probability and Statistics: Essays in Honor of Harold Hotelling, eds I. Olkin, S. G. Ghurye, W. Hoeffding, W. G. Madow, and H. B. Mann (Menlo Park, CA: Stanford University Press), 278-292.
26. Liu, J., Garza, J. C., Bronner, J., Kim, C. S., Zhang, W., and Lu, X. Y. (2010). Acute administration of leptin produces anxiolytic-like effects: a comparison with fluoxetine. Psychopharmacology (Berl.) 207, 535-545. doi: 10.1007/s00213- 009-1684-3
27. Lu, X. Y. (2007). The leptin hypothesis of depression: a potential link between mood disorders and obesity? Curr. Opin. Pharmacol. 7, 648-652. doi: 10.1016/j.coph.2007.10.010
28. Lu, X. Y., Kim, C. S., Frazer, A., and Zhang, W. (2006). Leptin: a potential novel antidepressant. Proc. Natl. Acad. Sci. U.S.A. 103, 1593-1598. doi: 10.1073/pnas.0508901103
29. Malendowicz, L. K., Rucinski, M., Belloni, A. S., Ziolkowska, A., and Nussdorfer, G. G. (2007). Leptin and the regulation of the hypothalamic-pituitary-adrenal axis. Int. Rev. Cytol. 263, 63-102. doi: 10.1016/S0074-7696(07)63002-2
30. Meier, U., and Gressner, A. M. (2004). Endocrine regulation of energy metabolism: review of pathobiochemical and clinical chemical aspects of lep- tin, ghrelin, adiponectin, and resistin. Clin. Chem. 50, 1511-1525. doi: 10.1373/clinchem.2004.032482
31. Morava, E., and Kozicz, T. (2013). Mitochondria and the economy of stress (mal)adaptation. Neurosci. Biobehav. Rev. 37, 668-680. doi: 10.1016/j.neubiorev.2013.02.005
32. Munzberg, H., Huo, L., Nillni, E. A., Hollenberg, A. N., and Bjørbaek, C. (2003). Role of signal transducer and activator of transcription 3 in regulation of hypothalamic proopiomelanocortin gene expression by leptin. Endocrinology 144 2121-2131. doi: 10.1210/en.2002-221037
33. Ohata, H., Suzuki, K., Oki, Y., and Shibasaki, T. (2000). Urocortin in the ventromedial hypothalamic nucleus acts as an inhibitor of feeding behavior in rats. Brain Res. 861, 1-7. doi: 10.1016/S0006-8993(99)02378-1
34. Okere, B., Xu, L., Roubos, E. W., Sonetti, D., and Kozicz, T. (2010). Restraint stress alters the secretory activity of neurons co-expressing urocortin-1, cocaine- and amphetamine-regulated transcript peptide and nesfatin-1 in the mouse Edinger-Westphal nucleus. Brain Res. 1317, 92-99. doi: 10.1016/j.brainres.2009. 12.053
35. Paxinos, G., and Franklin, K. B. J. (2001). TheMouseBrain in Stereotaxic Coordinates, 3rd Edn. NewYork: Academic Press.
36. Rogge, G., Jones, D., Hubert, G. W., Lin, Y., and Kuhar, M. J. (2008). CART peptides: regulators of body weight, reward and other functions. Nat. Rev. Neurosci. 9, 747-758. doi: 10.1038/nrn2493
37. Roubos, E. W., Dahmen, M., Kozicz, T., and Xu, L. (2012). Leptin and the hypothalamo-pituitary-adrenal stress axis. Gen. Comp. Endocrinol. 177, 28-36. doi: 10.1016/j.ygcen.2012.01.009
38. Rouwette, T., Klemann, K., Gaszner, B., Scheffer, G. J., Roubos, E. W., Scheenen, W. J., et al. (2011). Differential responses of corticotropin-releasing factor and urocortin 1 to acute pain stress in the rat brain. Neuroscience 183, 15-24. doi: 10.1016/j.neuroscience.2011.03.054
39. Sapolsky, R. M., Romero, L. M., and Munck, A. U. (2000). How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr. Rev. 21, 55-89. doi: 10.1210/edrv.21.1.0389
40. Spencer, S. J., Xu, L., Clarke, M. A., Lemus, M., Reichenbach, A., Geenen, B., et al. (2012). Ghrelin regulates the hypothalamic-pituitary-adrenal axis and restricts anxiety after acute stress. Biol. Psychiatry 72, 457-465. doi: 10.1016/j.biopsych.2012.03.010
41. Tschop, M., Smiley, D. L., and Heiman, M. L. (2000). Ghrelin induces adiposity in rodents. Nature 407, 908-913. doi: 10.1038/35038090
42. Weitemier, A. Z., and Ryabinin, A. E. (2005). Lesions of the Edinger-Westphal nucleus alter food andwater consumption. Behav. Neurosci. 119,1235-1243. doi: 10.1037/0735-7044.119.5.1235
43. Weitemier, A. Z., Tsivkovskaia, N. O., and Ryabinin, A. E. (2005). Urocortin 1 distribution in mouse brain is strain-dependent. Neuroscience 132, 729-740. doi: 10.1016/j.neuroscience.2004.12.047
44. Wiehager, S., Beiderbeck, D. I., Gruber, S. H., El-Khoury, A., Wamsteeker, J., Neumann, I. D., et al. (2009). Increased levels of cocaine and amphetamine regulated transcript in two animal models of depression and anxiety. Neurobiol. Dis. 34, 375-380. doi: 10.1016/j.nbd.2009.02.010
45. Williams, K.W., and Elmquist, J.K. (2012).Fromneuroanatomytobehavior:central integration of peripheral signals regulating feeding behavior. Nat. Neurosci. 15, 1350-1355. doi: 10.1038/nn.3217
46. Xu, L., Bloem, B., Gaszner, B., Roubos, E. W., and Kozicz, T. (2009). Sex-specific effects of fasting on urocortin 1, cocaine- and amphetamine-regulated transcript peptide and nesfatin-1 expression in the rat Edinger-Westphal nucleus. Neuroscience 162, 1141-1149. doi: 10.1016/j.neuroscience.2009.05.003
47. Xu, L., Bloem, B., Gaszner, B., Roubos, E. W., and Kozicz, T. (2010). Stress- related changes in the activity of cocaine- and amphetamine-regulated transcript and nesfatin neurons in the midbrain non-preganglionic Edinger-Westphal nucleus in the rat. Neuroscience 170, 478-488. doi: 10.1016/j.neuroscience.2010. 07.001
48. Xu, L., Scheenen, W. J., Leshan, R. L., Patterson, C. M., Elias, C. F., Bouwhuis, S., et al. (2011). Leptin signaling modulates the activity of urocortin 1 neurons in the mouse nonpreganglionic Edinger-Westphal nucleus. Endocrinology 152, 979-988. doi: 10.1210/en.2010-1143
49. Xu, L., Scheenen, W. J., Roubos, E. W., and Kozicz, T. (2012). Peptidergic Edinger-Westphal neurons and the energy-dependent stress response. Gen. Comp. Endocrinol. 177, 296-304. doi: 10.1016/j.ygcen.2011.11.039
50. Zhang, Y., Kerman, I. A., Laque, A., Nguyen, P., Faouzi, M., Louis, G. W., et al. (2011). Leptin-receptor-expressing neurons in the dorsomedial hypothalamus and median preoptic area regulate sympathetic brown adipose tissue circuits. J. Neurosci. 31, 1873-1884. doi: 10.1523/JNEUR0SCI.3223-10.2011
51. Zhang, Y., Proenca, R., Maffei, M., Barone, M., Leopold, L., and Friedman, J. M. (1994). Positional cloning of the mouse obese gene and its human homologue. Nature 372, 425-432. doi: 10.1038/372425a0
52. Zigman, J. M., Jones, J. E., Lee, C. E., Saper, C. B., and Elmquist, J. K. (2006). Expression of ghrelin receptor mRNA in the rat and the mouse brain. J. Comp. Neurol. 494, 528-548. doi: 10.1002/cne.20823