Identification of urocortin 3 afferent projection to the ventromedial nucleus of the hypothalamus in rat brain

Journal of Comparative Neurology

Volumn 519, Issue 10, 2011, Pages 2023-2042

  Chen, Peilin ^a   Lin, David ^a   Giesler, Jessica ^a   Li, Chien ^a  

^a UNIVERSITY OF VIRGINIA HEALTH SYSTEM   (United States)

Author keywords

CRF; CRF receptors; Enkephalin; Feeding; Stress

Indexed keywords

ENKEPHALIN; UROCORTIN III;

AMYGDALOID NUCLEUS; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CONTROLLED STUDY; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; HYPOTHALAMUS VENTROMEDIAL NUCLEUS; MALE; NEUROANATOMY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SENSORY NERVE; STRIA TERMINALIS;

AFFERENT PATHWAYS; ANIMALS; ENKEPHALINS; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; UROCORTINS; VENTROMEDIAL HYPOTHALAMIC NUCLEUS;

EID: 79956265028     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.22620     Document Type: Article

References (54)

1. Abercrombie M. 1946. Estimation of nuclear population from microtome sections. Anat Rec 94: 239-247.
2. Berk ML, Finkelstein JA. 1981. Afferent projections to the preoptic area and hypothalamic regions in the rat brain. Neuroscience 6: 1601-1624.
3. Bilkei-Gorzo A, Racz I, Michel K, Mauer D, Zimmer A, Klingmuller D, Zimmer A. 2008. Control of hormonal stress reactivity by the endogenous opioid system. Psychoneuroendocrinology 33: 425-436.
4. Cecchi M, Khoshbouei H, Javors M, Morilak DA. 2002. Modulatory effects of norepinephrine in the lateral bed nucleus of the stria terminalis on behavioral and neuroendocrine responses to acute stress. Neuroscience 112: 13-21.
5. Chalmers DT, Lovenberg TW, De Souza EB. 1995. Localization of novel corticotrophin-releasing factor receptor (CRF2) mRNA expression to specific subcortical nuclei in rat brain: comparison with CRF1 receptor mRNA expression. J Neurosci 15:6340-6350.
6. Chen P, Vaughan J, Donaldson C, Vale WW, Li C. 2009. Injection of Urocortin 3 into the ventromedial hypothalamus modulates feeding, blood glucose levels and hypothalamic POMC gene expression but not the HPA axis. Am J Physiol Endocrinol Metab. 2010 Feb;298:E337-45.
7. Ciccocioppo R, Fedeli A, Economidou D, Policani F, Weiss F, Massi M. 2003. The bed nucleus is a neuroanatomical substrate for the anorectic effect of corticotropin-releasing factor and for its reversal by nociceptin/orphanin FQ. J Neurosci 23: 9445-9451.
8. Cuello AC, Milstein C, Couture R, Wright B, Priestley JV, Jarvis J. 1984. Characterization and immunocytochemical application of monoclonal antibodies against enkephalins. J Histochem Cytochem 32: 947-957.
9. Davis M, Walker DL, Lee Y. 1997. Roles of the amygdala and bed nucleus of the stria terminalis in fear and anxiety measured with the acoustic startle reflex. Possible relevance to PTSD. Ann N Y Acad Sci 821: 305-331.
10. Dong HW, Petrovich GD, Swanson LW. 2001. Topography of projections from amygdala to bed nuclei of the stria terminalis. Brain Res Brain Res Rev 38: 192-246.
11. Drolet G, Dumont EC, Gosselin I, Kinkead R, Laforest S, Trottier JF. 2001. Role of endogenous opioid system in the regulation of the stress response. Prog Neuropsychopharmacol Biol Psychiatry 25: 729-741.
12. Fahrbach SE, Morrell JI, Pfaff DW. 1989. Studies of ventromedial hypothalamic afferents in the rat using three methods of HRP application. ExpBrain Res 77: 221-233.
13. Fekete EM, Inoue K, Zhao Y, Rivier JE, Vale WW, Szucs A, Koob GF, Zorrilla EP. 2007. Delayed satiety-like actions and altered feeding microstructure by a selective type 2 corticotropin-releasing factor agonist in rats: intra-hypothalamic urocortin 3 administration reduces food intake by prolonging the post-meal interval. Neuropsychopharmacology 32: 1052-1068.
14. Hsu SY, Hsueh AJ. 2001. Human stresscopin and stresscopin-related peptide are selective ligands for the type 2 corticotropin-releasing hormone receptor. Nat Med 7: 605-611.
15. Jamieson PM, Li C, Kukura C, Vaughan J, Vale W. 2006. Urocortin 3 modulates the neuroendocrine stress response and is regulated in rat amygdala and hypothalamus by stress and glucocorticoids. Endocrinology 147: 4578-4588.
16. Janecka A, Fichna J, Janecki T. 2004. Opioid receptors and their ligands. Curr Top Med Chem 4: 1-17.
17. Khoshbouei H, Cecchi M, Morilak DA. 2002. Modulatory effects of galanin in the lateral bed nucleus of the stria terminalis on behavioral and neuroendocrine responses to acute stress. Neuropsychopharmacology 27: 25-34.
18. King BM, Cook JT, Dallman MF. 1996. Hyperinsulinemia in rats with obesity-inducing amygdaloid lesions. Am J Physiol 271: R1156-1159.
19. King BM, Cook JT, Rossiter KN, Rollins BL. 2003. Obesity-inducing amygdala lesions: examination of anterograde degeneration and retrograde transport. Am J Physiol Regul Integr Comp Physiol 284: R965-982.
20. Kita H, Oomura Y. 1982. An HRP study of the afferent connections to rat medial hypothalamic region. Brain Res Bull 8: 53-62.
21. Kuperman Y, Issler O, Regev L, Musseri I, Navon I, Neufeld-Cohen A, Gil S, Chen A. 2010. Perifornical Urocortin-3 mediates the link between stress-induced anxiety and energy homeostasis. Proc Natl Acad Sci U S A 107: 8393-8398.
22. Larsen PJ, Hay-Schmidt A, Mikkelsen JD. 1994. Efferent connections from the lateral hypothalamic region and the lateral preoptic area to the hypothalamic paraventricular nucleus of the rat. J Comp Neurol 342: 299-319.
23. Lechan RM, Fekete C. 2006. The TRH neuron: a hypothalamic integrator of energy metabolism. Prog Brain Res 153: 209-235.
24. Lewis K, Li C, Perrin MH, Blount A, Kunitake K, Donaldson C, Vaughan J, Reyes TM, Gulyas J, Fischer W, Bilezikjian L, Rivier J, Sawchenko PE, Vale WW. 2001. Identification of urocortin III, an additional member of the corticotropin-releasing factor (CRF) family with high affinity for the CRF2 receptor. Proc Natl Acad Sci U S A 98: 7570-7575.
25. Li CS, Cho YK. 2006. Efferent projection from the bed nucleus of the stria terminalis suppresses activity of taste-responsive neurons in the hamster parabrachial nuclei. Am J Physiol Regul Integr Comp Physiol 291: R914-926.
26. Li C, Chen P, Smith MS. 1999. Identification of neuronal input to the arcuate nucleus (ARH) activated during lactation: implications in the activation of neuropeptide Y neurons. Brain Res 824: 267-276.
27. Li C, Vaughan J, Sawchenko PE, Vale WW. 2002. Urocortin III-immunoreactive projections in rat brain: partial overlap with sites of type 2 corticotrophin-releasing factor receptor expression. J Neurosci 22: 991-1001.
28. Li C, Chen P, Vaughan J, Blount A, Chen A, Jamieson PM, Rivier J, Smith MS, Vale W. 2003. Urocortin III is expressed in pancreatic beta-cells and stimulates insulin and glucagon secretion. Endocrinology 144: 3216-3224.
29. Luiten PG, Room P. 1980. Interrelations between lateral, dorsomedial and ventromedial hypothalamic nuclei in the rat. An HRP study. Brain Res 190: 321-332.
30. McBride RL, Sutin J. 1977. Amygdaloid and pontine projections to the ventromedial nucleus of the hypothalamus. J Comp Neurol 174: 377-396.
31. Merchenthaler I. 1991. Co-localization of enkephalin and TRH in perifornical neurons of the rat hypothalamus that project to the lateral septum. Brain Res 544: 177-180.
32. Merchenthaler I, Maderdrut JL, Altschuler RA, Petrusz P. 1986. Immunocytochemical localization of proenkephalin-derived peptides in the central nervous system of the rat. Neuroscience 17: 325-348.
33. Merchenthaler I, Csernus V, Csontos C, Petrusz P, Mess B. 1988. New data on the immunocytochemical localization of thyrotropin-releasing hormone in the rat central nervous system. Am J Anat 181: 359-376.
34. Merchenthaler I, Meeker M, Petrusz P, Kizer JS. 1989. Identification and immunocytochemical localization of a new thyrotropin-releasing hormone precursor in rat brain. Endocrinology 124: 1888-1897.
35. Numan M, Numan M. 1996. A lesion and neuroanatomical tract-tracing analysis of the role of the bed nucleus of the stria terminalis in retrieval behavior and other aspects of maternal responsiveness in rats. Dev Psychobiol 29: 23-51.
36. Numan M, Numan MJ, Marzella SR, Palumbo A. 1998. Expression of c-fos, fos B, and egr-1 in the medial preoptic area and bed nucleus of the stria terminalis during maternal behavior in rats. Brain Res 792: 348-352.
37. Ohata H, Shibasaki T. 2004. Effects of urocortin 2 and 3 on motor activity and food intake in rats. Peptides 25: 1703-1709.
38. Onteniente B, Menetrey D, Arai R, Calas A. 1989. Origin of the met-enkephalinergic innervation of the lateral septum in the rat. Cell Tissue Res 256: 585-592.
39. Pelleymounter MA, Joppa M, Ling N, Foster AC. 2004. Behavioral and neuroendocrine effects of the selective CRF2 receptor agonists urocortin II and urocortin III. Peptides 25: 659-666.
40. Poulain P, Martin-Bouyer L, Beauvillain JC, Tramu G. 1984. Study of the efferent connections of the enkephalinergic magnocellular dorsal nucleus in the guinea-pig hypothalamus using lesions, retrograde tracing and immunohistochemistry: evidence for a projection to the lateral septum. Neuroscience 11: 331-343.
41. Radulovic J, Ruhmann A, Liepold T, Spiess J. 1999. Modulation of learning and anxiety by corticotropin-releasing factor (CRF) and stress: differential roles of CRF receptors 1 and 2. J Neurosci 19: 5016-5025.
42. Ragnauth A, Schuller A, Morgan M, Chan J, Ogawa S, Pintar J, Bodnar RJ, Pfaff DW. 2001. Female preproenkephalin-knockout mice display altered emotional responses. Proc Natl Acad Sci U S A 98: 1958-1963.
43. Reilly JJ, Maki R, Nardozzi J, Schulkin J. 1994. The effects of lesions of the bed nucleus of the stria terminalis on sodium appetite. Acta Neurobiol Exp 54: 253-257.
44. Sakanaka M, Magari S. 1989. Reassessment of enkephalin (ENK)-containing afferents to the rat lateral septum with reference to the fine structures of septal ENK fibers. Brain Res 479: 205-216.
45. Sawchenko PE. 1987. Evidence for differential regulation of corticotropin-releasing factor and vasopressin immunoreactivities in parvocellular neurosecretory and autonomic-related projections of the paraventricular nucleus. Brain Res 437: 253-263.
46. Swanson LW, Sawchenko PE, Rivier J, Vale WW. 1983. Organization of ovine corticotropin-releasing factor immunoreactive cells and fibers in the rat brain: an immunohistochemical study. Neuroendocrinology 36: 165-186.
47. Szeidemann Z, Shanabrough M, Leranth C. 1995. Hypothalamic Leu-enkephalin-immunoreactive fibers terminate on calbindin-containing somatospiny cells in the lateral septal area of the rat. J Comp Neurol 358: 573-583.
48. Thompson BL, Rosen JB. 2000. Effects of TRH on acoustic startle, conditioned fear and active avoidance in rats. Neuropeptides 34: 38-44.
49. Todorovic C, Radulovic J, Jahn O, Radulovic M, Sherrin T, Hippel C, Spiess J. 2007. Differential activation of CRF receptor subtypes removes stress-induced memory deficit and anxiety. Eur J Neurosci 25: 3385-3397.
50. Van Pett K, Viau V, Bittencourt JC, Chan RK, Li HY, Arias C, Prins GS, Perrin M, Vale W, Sawchenko PE. 2000. Distribution of mRNAs encoding CRF receptors in brain and pituitary of rat and mouse. J Comp Neurol 428:191-212.
51. Wittmann G, Fuzesi T, Liposits Z, Lechan RM, Fekete C. 2009. Distribution and axonal projections of neurons coexpressing thyrotropin-releasing hormone and urocortin 3 in the rat brain. J Comp Neurol 517: 825-840.
52. Wood RI, Newman SW. 1995. Integration of chemosensory and hormonal cues is essential for mating in the male Syrian hamster. J Neurosci 15: 7261-7269.
53. Zaborszky L. 1982. Afferent connections of the medial basal hypothalamus. Adv Anat Embryol Cell Biol 69: 1-107.
54. Zardetto-Smith AM, Beltz TG, Johnson AK. 1994. Role of the central nucleus of the amygdala and bed nucleus of the stria terminalis in experimentally-induced salt appetite. Brain Res 645: 123-134.