PACAP gene expression in neurons of the rat hypothalamo-pituitary-adrenocortical axis is induced by endotoxin and interleukin-1β

Neuroendocrinology

Volumn 70, Issue 1, 1999, Pages 73-82

  Hannibal, Jens ^b   Jessop, David S ^c   Fahrenkrug, Jan ^c   Harbuz, Michael S ^c   Larsen, Philip J ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b BISPEBJERG HOSPITAL   (Denmark)

^c NONE

Author keywords

Adrenal steroids; Cytokines; Immunocytochemistry; In situ hybridization; Interleukins; Lipopolysaccharide; Neuroimmune interactions; Paraventricular nucleus; Pituitary adenylate cyclase activating polypeptide; Vagotomy

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; ENDOTOXIN; HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE; INTERLEUKIN 1BETA; MESSENGER RNA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; GENE INDUCTION; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IMMUNOREACTIVITY; IN SITU HYBRIDIZATION; MALE; MEDIAN EMINENCE; NONHUMAN; PRIORITY JOURNAL; RAT; THALAMUS MIDLINE NUCLEUS; VAGUS NERVE;

ANIMALS; ARTHRITIS, EXPERIMENTAL; CORTICOSTERONE; ENDOTOXINS; GENE EXPRESSION REGULATION; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; INTERLEUKIN-1; LIPOPOLYSACCHARIDES; MALE; NEURONS; NEUROPEPTIDES; PARAVENTRICULAR HYPOTHALAMIC NUCLEUS; PITUITARY ADENYLATE CYCLASE-ACTIVATING POLYPEPTIDE; PITUITARY-ADRENAL SYSTEM; RATS; RATS, WISTAR; RNA, MESSENGER; VAGOTOMY;

EID: 0005739565     PISSN: 00283835     EISSN: None     Source Type: Journal    
DOI: 10.1159/000054461     Document Type: Article

References (49)

1. Vale W, Spiess J, Rivier C, Rivier J: Characterization of a 41-residue ovine hypothalamic peptide that stimulates secretion of corticotropin and beta-endorphin. Science 1981;213: 1394-1397.
2. Rivest S, Rivier C: Influence of the paraventricular nucleus of the hypothalamus in the alteration of neuroendocrine functions induced by intermittent footshock or interleukin. Endocrinology 1991;129:2049-2057.
3. Rivier C: Effect of peripheral and central cytokines on the hypothalamic-pituitary-adrenal axis of the rat. Ann NY Acad Sci 1993;697:97-105.
4. Dunn AJ: Infection as a stressor: A cytokine-mediated activation of the hypothalamo-pituitary-adrenal axis? Ciba Found Symp 1993; 172:226-239.
5. Dunn AJ: The role of interleukin-1 and tumor necrosis factor alpha in the neurochemical and neuroendocrine responses to endotoxin. Brain Res Bull 1992;29:807-812.
6. Dunn AJ: Role of cytokines in infection-induced stress. Ann NY Acad Sci 1993;697:189-202.
7. Rivier C, Rivest S: Mechanisms mediating the effects of cytokines on neuroendocrine functions in the rat. Ciba Found Symp 1993;172: 204-220.
8. Harbuz MS, Lightman SL: Stress and the hypothalamo-pituitary-adrenal axis: Acute, chronic and immunological activation. J Endocrinol 1992;134:327-339.
9. Antoni FA: Hypothalamic control of adrenocorticotropin secretion: Advance since the discovery of 41-residue corticotropin-releasing factor. Endocrine Rev 1986;7:351-378.
10. Gillies GE, Linton EA, Lowry PJ: Corticotropin releasing activity of the new CRF is potentiated several times by vasopressin, Nature 1982;229:355-357.
11. Schmidt ED, Janszen AW, Wouterlood FG, Tilders FJ: Interleukin-induced long-lasting changes in hypothalamic corticotropin-releasing hormone (CRH)-neurons and hyperresponsiveness of the hypothalamus-pituitary-adrenal axis. J Neurosci 1995;15:7417-7426.
12. Schmidt ED, Binnekade R, Janszen AW, Tilders FJ: Short stressor induced long-lasting increases of vasopressin stores in hypothalamic corticotropin-releasing hormone (CRH) neurons in adult rats. J Neuroendocrinol, 1996;8: 703-712.
13. Arimura A, Shioda S: Pituitary adenylate cyclase activating polypeptide (PACAP) and its receptors: Neuroendocrine and endocrine interaction. Front Neuroendocrinol 1995;16:53-88.
14. Hannibal J, Mikkelsen JD, Fahrenkrug J, Larsen PJ: Pituitary adenylate cyclase-activating peptide gene expression in corticotropin-releasing factor-containing parvicellular neurons of the rat hypothalamic paraventricular nucleus is induced by colchicine, but not by adrenalectomy, acute osmotic, ether, or restraint stress. Endocrinology 1995;136:4116-4124.
15. Ceccatelli S, Villar MJ, Goldstein M, Hökfelt T: Expression of c-fos immunoreactivity in transmitter characterized neurons after stress. Proc Natl Acad Sci USA 1989;86:9569-9573.
16. Gaykema RP, Dijkstra I, Tilders FJ: Subdiaphragmatic vagotomy suppresses endotoxin-induced activation of hypothalamic corticotropin-releasing hormone neurons and ACTH secretion. Endocrinology 1995;136:4717-4720.
17. Tilders FJ, DeRijk RH, Van Dam AM, Vincent VA, Schotanus K, Persoons JH: Activation of the hypothalamus-pituitary-adrenal axis by bacterial endotoxins: Routes and intermediates signals. Psychoneuroendocrinol 1994;19:209-232.
18. Zuckerman SH, Shellhaas J, Butler LD: Differential regulation of lipopolysaccaride-induced interleukin-1 and tumor necrosis factor-alpha synthesis: Effects of endogenous and exogenous glucocorticoids and the role of the pituitary-adrenal axis. Eur J Immunol 1989;19:301-305.
19. Harbuz MS, Rees RG, Eckland DJ, Jessop DS, Brewerton D, Lightman SL: Paradoxical responses of hypothalamic corticotropin-releasing factor (CRF) messenger ribonucleic acid (mRNA) and CRF-41 peptide and adenohypophysial proopiomelanocortin mRNA during chronic inflammatory stress. Endocrinology 1992;130:1394-1400.
20. Shinmei M, Masuda K, Kikushi T, Shinomura Y: Interleukin 1, tumor necrosis factor and interleukin 6 as mediators of cartilage destruction. Semin Arthritis Rheum 1989;(18(suppl): 27-31.
21. Leisten JC, Gaarde WA, Scholz W: Interleukin-6 serum levels correlate with footpad swelling in adjuvant-induced arthritic Lewis rats treated with cyclosporin A or indomethacin. Clin Immunol Immonopathol 1990;56:108-114.
22. Watkins LR, Wiertelak EP, Goehler LE, Mooney-Heiberger K, Martinez J, Furness L, Smith KP, Maier SF: Neurocircuitry of illness-induced hyperalgesia. Brain Res 1994;639:283-299.
23. Hannibal J, Mikkelsen JD, Clausen H, Holst JJ, Wulff BS, Fahrenkrug J: Gene expression of pituitary adenlyate cyclase activating polypeptide (PACAP) in the rat hypothalamus. Regul Pept 1995;55:133-148.
24. Hannibal J, Ding JM, Chen D, Gillette MU, Fahrenkrug J, Larsen PJ, Mikkelsen JD: Pituitary adenylate cyclase activating peptide (PACAP) in the retinohypothalamic tract. A daytime regulator of the biological clock. J Neurosci 1997;17:2637-2644.
25. Fahrenkrug J, Hannibal J: PACAP immunore-activity in capsaicin-sensitive nerve fibers supplying the rat urinary tract. Neuroscience 1998; 83:1261-1272.
26. Chover-Gonzalez AJ, Harbuz MS, Lightman SL: Effect of adrenalectomy and stress on interleukin-1 beta-mediated activation of hypothalamic corticotropin-releasing factor mRNA. 5 Neuroimmunol 1993;42:155-160.
27. Harbuz MS, Stephanou A, Sarlis N, Lightman SL: The effects of recombinant human interleukin (IL)-1 alpha, IL-1 beta or IL-6 on hypothalamo-pituitary-adrenal axis activation. J Endocrinol 1992;133:349-355.
28. Rivest S, Laflamme N: Neuronal activily and neuropeptide gene transcription in the brains of immune-challenged rats. J Neuroendocrinol 1998;7:501-525.
29. Rivest S, Laflamme N, Nappi RE: Immune challenge and immobilization stress induce transcription of the gene encoding the CRF receptor in selective nuclei of the rat hypothalamus. J Neurosci 1995;15:2680-2695.
30. Dow RC, Bennie J, Fink G: Pituitary adenylate cyclase-activating peptide-38 (PACAP)-38 is released into hypophysial portal blood in the normal male and female rat. J Endocrinol 1994;142:R1-R4.
31. Rawlings SR, Hezareh M: Pituitary adenylate cyclase-activating polypeptide (PACAP) and PACAP/vasoactive intestinal polypeptide receptors: Actions on the anterior pituitary gland. Endocr Rev 1996;17:4-29.
32. Gottschall PE, Tatsuno I, Miyata A, Arimura A: Characterization and distribution of binding sites for the hypothalamic peptide, pituitary adenylate cyclase-activating polypeptide. Endocrinology 1990;127:272-277.
33. Spengler D, Waeber C, Pantaloni C, Holsboer F, Bockaert J, Seeburg PH, Journot L: Differential signal transduction by five splice variants of the PACAP receptor. Nature 1993;365: 170-175.
34. Miyata A, Arimura A, Dahl RR, Minamino N, Uehara A, Jiang L, Culler MD, Coy DH: Isolation of a novel 38 residue-hypothalamic polypeptide which stimulates adenylate cyclase in pituitary cells. Biochem Biophys Res Commun 1989;164:567-574.
35. Propato Mussafiri R, Kanse SM, Ghatei MA, Bloom SR: Pituitary adenylate cycylase-activating polypeptide releases 7B2, adrenocorticotrophin, growth hormone and prolactin from the mouse and rat clonal pituitary cell lines AtT-20 and GH3. J Endocrinol 1992;132:107-113.
36. Chiodera P, Volpi R, Capretti L, Caffarri G, Magotti MG, Coiro V: Effects of intravenously infused pituitary adenylate cyclase activating polypeptide on adenohypophyseal hormone secretion in normal men. Neuroendocrinology 1996;64:242-246.
37. Grinevich V, Fournier A, Pelletier G: Effects of pituitary adenylate cyclase-activating polypeptide (PACAP) on corticotropin-releasing hormone (CRH) gene expression in the rat hypothalamic paraventricular nucleus. Brain Res 1997;773:190-196.
38. Legradi G, Hannibal J, Lechan RM: Pituitary adenylate cyclase-activating polypeptide-nerve terminals densely innervate corticotropin-releasing hormone-neurons in the hypothalamic paraventricular nucleus of the rat. Neurosci Lett 1998;246:145-148.
39. Nomura M, Ueta Y, Serino R, Kabashima N, Shibuya I, Yamashita H: PACAP type I receptor gene expression in the paraventricular and supraoptic nuclei of rats. NeuroReport 1996;8: 67-70.
40. Hashimoto H, Nogi H, Mori K, Ohishi H, Shigemoto R, Yamamoto K, Matsuda T, Mizuno N, Nagata S, Baba A: Distribution of the mRNA for a pituitary adenylate cyclase-activating polypeptide receptor in the rat brain: An in situ hybridization study. J Comp Neurol 1996;371:567-577.
41. Banks WA, Ortiz L, Plotkin SR, Kastin AJ: Human interleukin (IL) 1α, murine IL-1α and murine IL-1β are transported from blood to brain in the mouse by a shared saturable mechanism. J Pharmacol Exp Ther 1991;259:988-996.
42. Hansen MK, Taishi P, Chen Z, Krueger JM: Vagotomy blocks the induction of interleukin-1beta (IL-1beta) mRNA in the brain of rats in response to systemic IL-1beta. J Neurosci 1998;18:2247-2253.
43. Hansen MK, Krueger JM: Subdiaphragmatic vagotomy blocks the sleep-and fever-promoting effects of interleukin-1beta. Am J Physiol 1997;273:R1246-R1253.
44. Romanovsky AA, Simons CT, Szekely M, Kulchitsky VA: The vagus nerve in the thermoregulatory response to systemic inflammation. Am J Physiol 1997;273:R407-R413.
45. Fleshner M, Silbert L, Deak T, Goehler LE, Martin D, Watkins LR, Maier SF: TNF-alpha-induced corticosterone elevation but not serum protein or corticosteroid binding globulin reduction is vagally mediated. Brain Res Bull 1997;44:701-706.
46. Milligan ED, McGorry MM, Fleshner M, Gaykema RP, Goehler LE. Watkins LR, Maier SF: Subdiaphragmatic vagotomy does not prevent fever following intracerebroventricular prostaglandin E2: Further evidence for the importance of vagal afferents in immune-to-brain communication. Brain Res 1997;766:240-243.
47. Goehler LE, Relton JK, Dripps D, Kiechle R, Tartaglia N, Maier SF, Watkins LR: Vagal paraganglia bind biotinylated interleukin-1 receptor antagonist: A possible mechanism for immune-to-brain communication. Brain Res Bull 1997;43:357-364.
48. Ericsson A, Kovacs KJ, Sawchenko PE: A functional anatomical analysis of central pathways subserving the effects of interleukin-1 on stress-related neuroendocrine neurons. J Neurosci 1994;14:897-913.
49. Ericsson A, Arias C, Sawchenko PE: Evidence for an intramedullary prostaglandin-dependent mechanism in the activation of stress-related neuroendocrine circuitry by intravenous interleukin-1. J Neurosci 1997;17:7166-7179.