Peripheral osmotic stimulation inhibits the brain's innate immune response to microdialysis of acidic perfusion fluid adjacent to supraoptic nucleus

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 297, Issue 5, 2009, Pages

  Summy Long, Joan Y ^a   Hu, Sanmei ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

Acidosis; c Fos; Hypertonic saline; Interleukin 1 ; Magnocellular neurons

Indexed keywords

COMPLEMENT RECEPTOR; CYCLOOXYGENASE 2; GLIAL FIBRILLARY ACIDIC PROTEIN; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 1BETA; OXYTOCIN; PROTEIN C FOS; PROTEIN OX 42; UNCLASSIFIED DRUG; VASOPRESSIN;

ACIDOSIS; ANIMAL TISSUE; ARTICLE; BRAIN VENTRICLE; CELL DAMAGE; CONTROLLED STUDY; CYTOKINE RELEASE; EPENDYMA CELL; HYPOTHALAMUS; IMMUNOHISTOCHEMISTRY; INNATE IMMUNITY; MACROGLIA; MAGNOCELLULAR NUCLEUS; MALE; MICRODIALYSIS; MICROGLIA; NEUROENDOCRINE SYSTEM; NONHUMAN; ONCOGENE C FOS; PERFUSION; PREOPTIC NUCLEUS; PRIORITY JOURNAL; RAT; SUPRAOPTIC NUCLEUS; THALAMUS MIDLINE NUCLEUS; VASCULARIZATION;

ACIDOSIS; ANIMALS; BRAIN; DISEASE MODELS, ANIMAL; EPENDYMA; IMMUNITY, INNATE; INTERLEUKIN-1BETA; MALE; MICRODIALYSIS; MICROGLIA; MIDLINE THALAMIC NUCLEI; OSMOSIS; OXYTOCIN; RATS; RATS, SPRAGUE-DAWLEY; SALINE SOLUTION, HYPERTONIC; SUPRAOPTIC NUCLEUS; VASOPRESSINS;

EID: 70449631603     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00340.2009     Document Type: Article

References (126)

1. Arend WP, Weigus HG, Thompson RC, Eisenberg SP. Biological properties of recombinant human monocyte-derived interleukin 1 receptor antagonist. J Clin Invest 85: 1694-1697, 1990. (Pubitemid 20176469)
2. Ayoub AE, Salm AK. Increased morphological diversity of microglia in the activated hypothalamic supraoptic nucleus. J Neurosci 23: 7759-7766, 2003.
3. Benveniste H. Brain microdialysis. J Neurochem 52: 1667-1679, 1989.
4. Berkowitz BA, Sherman S. Characterization of vasopressin analgesia. J Pharmacol Exp Ther 220: 329-334, 1982.
5. Besedovsky HO, del Rey A. Immune-neuroendocrine circuits: integrative role of cytokines. Front Neuroendocrinol 13: 61-94, 1992.
6. Bjugn R, Gunderson HJG. Estimate of the total number of neurons and glial and endothelial cells in the rat spinal cord by means of the optical disector. J Comp Neurol 328: 406-414, 1993. (Pubitemid 23040109)
7. Bobak JB, Salm AK. Plasticity of astrocytes of the ventral glial limitans subjacent to the supraoptic nucleus. J Comp Neurol 376: 188-197, 1996.
8. Bourque CW. Osmoregulation of vasopressin neurons: a synergy of intrinsic and synaptic processes. Prog Brain Res 119: 59-76, 1998.
9. Bourque CW. Central mechanisms of osmosensation and systemic osmoregulation. Nat Rev Neurosci 9: 519-531, 2008.
10. Bourque CW, Ciura S, Trudel E, Stachniak TJE, Sharif-Naeini. Hydromineral neuroendocrinology: neurophysiological characterization of mammalian osmosensitive neurones. Exp Physiol 92: 499-505, 2007.
11. Bourque CW, Richard D. Axonal projections from the organum vasculosum lamina terminalis to the supraoptic nucleus: functional analysis and presynaptic modulation. Clin Exp Pharmacol Physiol 28: 570-574, 2001. (Pubitemid 32588434)
12. Bulger EM, Cuschieri J, Warner K, Maier RV. Hypertonic resuscitation modulates the inflammatory response in patients with traumatic hemorrhagic shock. Ann Surg 245: 635-641, 2007. (Pubitemid 46555669)
13. Cammermeyer J. The hypependymal microglia cell. Z Anat Entwicklungsgesch 124: 543-561, 1965.
14. Cao C, Matsumura K, Shirakawa N, Maeda M, Jikihara I, Kobayashi S, Watanabe Y. Pyrogenic cytokines injected into the rat cerebral ventricle induce cyclooxygenase-2 in brain endothelial cells and also upregulate their receptors. Eur J Neurosci 13: 1781-1790, 2001. (Pubitemid 32488067)
15. Cartmell T, Poole S, Turnbull A, Rothwell N, Luheshi G. Circulating interleukin-6 mediates the febrile response to localized inflammation in rats. J Physiol 526: 653-661, 2000. (Pubitemid 30654768)
16. Chakfe Y, Zhang Z, Bourque CW. IL-1β directly excites isolated rat supraoptic neurons via upregulation of the osmosensory cation current. Am J Physiol Regul Integr Comp Physiol 290: R1183-R1190, 2006.
17. Chang SL, Ren T, Zadina JE. Interleukin-1 activation of Fos protooncogene protein in the rat hypothalamus. Brain Res 617: 123-130, 1993. (Pubitemid 23201733)
18. Chappell PB, Smith MA, Kilts CD, Bissette G, Ritchie J, Anderson C, Nemeroff CB. Alterations in corticotropin-releasing factor-like immunoreactivity in discrete rat brain regions after acute and chronic stress. J Neurosci 6: 2908-2914, 1986.
19. Chassin C, Hornef MW, Bens M, Lotz M, Goujon JM, Vimont S, Arlet G, Hertig A, Rondeau E, Vandewalle A. Hormonal control of the renal immune response and antibacterial host defense by arginine vasopressin. J Exp Med 204: 2837-2852, 2007. (Pubitemid 350179554)
20. Chinenov Y, Rogatsky I. Glucocorticoids and the innate immune system: crosstalk with the toll-like receptor signaling network. Mol Cell Endocrinol 275: 30-42, 2007. (Pubitemid 47260712)
21. Chu C, Kato K, Jin Q, Qiu D, Yu N, Oiso Y, Kannan H. Enhanced cardiovascular alteration and Fos expression induced by central salt loading in a conscious rat transgenic for the metallothionein-vasopressin fusion gene. Neurosci Res 53: 147-155, 2005. (Pubitemid 41219530)
22. Chung S, Lee MY, Soh H, Jung W, Joe E. Modulation of membrane potential by extracellular pH in activated microglia in rats. Neurosci Lett 249: 139-142, 1998. (Pubitemid 28331535)
23. Clausen T, Khaldi A, Zuaner A, Reinert M, Doppenberg E, Menzel M, Soukup J, Alves OL, Bullock MR. Cerebral acid-base homeostasis after severe traumatic brain injury. J Neurosurg 103: 597-607, 2005. (Pubitemid 43193865)
24. Clodi M, Vila G, Geyeregger R, Riedl M, Stulnig TM, Struck J, Luger TA, Luger A. Oxytocin alleviates the neuroendocrine and cytokine response to bacterial endotoxin in healthy men. Am J Physiol Endocrinol Metab 295: E686-E691, 2008.
25. Cunningham ET Jr, Sawchenko PE. Reflex control of magnocellular vasopressin and oxytocin secretion. Trends Neurosci 14: 406-411, 1991.
26. Del Bigio MR. The ependyma: a protective barrier between brain and cerebrospinal fluid. Glia 14: 1-13, 1995.
27. Desson SE, Ferguson AV. Interleukin-1β modulates rat subfornical organ neurons as a result of activation of a non-selective cationic conductance. J Physiol 550 (Pt.1): 113-122, 2003.
28. Di Chiara G. In-vivo brain dialysis of neurotransmitters. Trends Pharmacol Sci 11: 116-121, 1990.
29. Diana A, van Dam AM, Winblad B, Schultzberg M. Co-localization of interleukin-1 receptor type I and interleukin-1 receptor antagonist with vasopressin in magnocellular neurons of the paraventricular and supraoptic nuclei of the rat hypothalamus. Neuroscience 89: 137-147, 1999. (Pubitemid 29049033)
30. Dinarello CA. ELISA kits based on monoclonal antibodies do not measure total IL-1 beta synthesis. J Immunol Methods 148: 255-259, 1992.
31. Dragunow M, Goulding M, Faull RLM, Ralph R, Mee E, Frith R. Induction of c-fos mRNA and protein in neurons and glia after traumatic brain injury: Pharmacological characterization. Exp Neurol 107: 236-248, 1990. (Pubitemid 20085705)
32. 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 14: 897-913, 1994. (Pubitemid 24043940)
33. Ericsson A, Liu C, Hart RP, Sawchenko PE. Type 1 interleukin-1 receptor in the rat brain: distribution, regulation, and relationship to sites of IL-1-induced cellular activation. J Comp Neurol 361: 681-698, 1995.
34. Eriksson C, Van Dam AM, Lucassen PJ, Bol JG, Winblad B, Schultzberg M. Immunohistochemical localization of interleukin-1β, interleukin-1 receptor antagonist and interleukin-1β converting enzyme/ caspase-1 in the rat brain after peripheral administration of kainic acid. Neuroscience 93: 915-930, 1999. (Pubitemid 29341639)
35. Faggioni R, Fantuzzi G, Fuller J, Dinarello CA, Feingold KR, Grunfeld C. IL-1 beta mediates leptin induction during inflammation. Am J Physiol Regul Integr Comp Physiol 274: R204-R208, 1998. (Pubitemid 28092634)
36. Feldberg W, Rocha e Silva M, Jr. Vasopressin release produced in anaesthetized cats by antagonists of gamma-aminobutyric acid and glycine. Br J Pharmacol 62: 99-106, 1978. (Pubitemid 8251903)
37. Ferri C, Ferguson AV. Interleukin-1 beta depolarizes paraventricular nucleus parvocellular neurones. J Neuroendocrinol 15: 126-133, 2003. (Pubitemid 36193025)
38. Ferri C, Yuill EA, Ferguson A. Interleukin-1β depolarizes magnocellular neurons in the paraventricular nucleus of the hypothalamus through prostaglandin-mediated activation of a nonselective cationic conductance. Regul Pept 129: 63-71, 2005. (Pubitemid 40775787)
39. French RA, VanHoy RW, Chizzonite R, Zachary JF, Dantzer R, Parnet P, Bluthe RM, Kelley KW. Expression and localization of p80 and p68 interleukin-1 receptor proteins in the brain of adult mice. J Neuroimmunol 93: 194-202, 1999. (Pubitemid 29051565)
40. Ghorbel MT, Sharman G, Leroux M, Barrett T, Donovan DM, Becker KG, Murphy D. Microarray analysis reveals interleukin-6 as a novel secretory product of the hypothalamo-neurohypophyseal system. J Biol Chem 278: 19280-19285, 2003. (Pubitemid 36799320)
41. Graeber M, Streit W. Perivascular microglia defined. Trends Neurosci 13: 366, 1990.
42. Hannum CH, Wilcox CJ, Arend WP, Joslin FG, Dripps DJ, Heimdal PL, Armes LG, Sommer A, Eisenberg SP, Thompson RC. Interleukin- 1 receptor antagonist activity of a human interleukin-1 inhibitor. Nature 343: 336-340, 1990. (Pubitemid 120028524)
43. Hatanaka E, Shimomi FM, Curi R, Campa A. Sodium chloride inhibits cytokine production by lipopolysaccharide-stimulated human neutrophils and mononuclear cells. Shock 27: 32-35, 2007. (Pubitemid 44968007)
44. Hatton GI, Perlmutter LS, Salm AK, Tweedle CD. Dynamic neuronalglial interactions in hypothalamus and pituitary: implication for control of synthesis and release. Peptides 5: 121-138, 1984.
45. Herx LM, Rivest S, Yong VW. Central nervous system-initiated inflammation and neurotrophism in trauma: IL-1B is required for the production of ciliary neurotrophic factor. J Immunol 165: 2232-2239, 2000. (Pubitemid 30643173)
46. Honda K, Negoro H, Dyball REJ, Higuchi T, Takano S. The osmoreceptor complex in the rat: evidence for interactions between the supraoptic and other diencephalic nuclei. J Physiol (Lond) 431: 225-241, 1990.
47. Hosoi T, Okuma Y, Nomura Y. Leptin induces IL-1 receptor antagonist expression in the brain. Biochem Biophys Res Commun 294: 215-219, 2002. (Pubitemid 34694079)
48. Hsu SM, Raine L, Fanger H. Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: A comparison between ABC and unlabeled antibody (PAP) procedures. J Histochem Cytochem 29: 577-580, 1981. (Pubitemid 11147380)
49. Hwang AS, Wilcox GL. Intradermal hypertonic saline-induced behavior as a nociceptive test in mice. Life Sci 38: 2389-2396, 1986.
50. Ip NY, Wiegand SJ, Morse J, Rudge JS. Injury-induced regulation of ciliary neurotrophic factor mRNA in the adult rat brain. Eur J Neurosci 5: 25-33, 1993. (Pubitemid 23079495)
51. Johnson AK, Zardetto-Smith AM, Edwards GL. Integrative mechanisms and the maintenance of cardiovascular and body fluid homeostasis: the central processing of sensory input derived from the circumventricular organs of the lamina terminalis. Prog Brain Res 91: 381-393, 1992.
52. Keil LC, Rosella-Dampman LM, Emmert S, Chee O, Summy-Long JY. Enkephalin inhibition of angiotensin-stimulated release of oxytocin and vasopressin. Brain Res 297: 329-336, 1984. (Pubitemid 14136576)
53. Keil LC, Severs WB. Reduction in plasma vasopressin levels of dehydrated rats following acute stress. Endocrinology 100: 30-38, 1977.
54. Kelly JF, Elias CF, Lee CE, Ahima RS, Seeley RJ, Bjørbaek C, Oka T, Saper CB, Flier JS, Elmquist JK. Ciliary neurotrophic factor and leptin induce distinct patterns of immediate early gene expression in the brain. Diabetes 53: 911-920, 2004. (Pubitemid 38436602)
55. Kent S, Bluthe RM, Dantzer R, Hardwick AJ, Kelley KW, Rothwell NJ, Vannice JL. Different receptor mechanisms mediate the pyrogenic and behavioral effects of interleukin 1. Proc Natl Acad Sci USA 89: 9117-9120, 1992.
56. 2+ influx by acidic extracellular pH in cultured human microglia. Glia 36: 22-30, 2001.
57. Kis B, Isse T, Snipes JA, Chen L, Yamashita H, Ueta Y, Busija DW. Effects of LPS stimulation on the expression of prostaglandin carriers in the cells of the blood-brain and blood-cerebrospinal fluid barriers. Appl Physiol 100: 1392-1399, 2006. (Pubitemid 43671500)
58. Kølsen-Petersen JA. Immune effect of hypertonic saline: fact or fiction? Acta Anaesthesiol Scand 48: 667-678, 2004.
59. Konsman JP, Drukarch B, van Dam AM. (Peri)vascular production and action of pro-inflammatory cytokines in brain pathology. Clin Sci (Lond) 112: 1-25, 2007. (Pubitemid 46127195)
60. Konsman JP, Tridon V, Dantzer R. Diffusion and action of intracerebroventricularly injected interleukin-1 in the CNS. Neuroscience 101: 957-967, 2000. (Pubitemid 30952919)
61. Konsman JP, Vigues S, Mackerlova L, Bristow A, Blomqvist A. Rat brain vascular distribution of interleukin-1 type-1 receptor immunoreactivity: relationship to patterns of inducible cyclooxygenase expression by peripheral inflammatory stimuli. J Comp Neurol 472: 113-129, 2004. (Pubitemid 38393311)
62. Kovacs KJ. c-Fos as a transcription factor: a stressful (re)view from a functional map. Neurochem Int 33: 287-297, 1998.
63. Kovacs KJ, Sawchenko PE. Mediation of osmoregulatory influences on neuroendocrine corticotropin-releasing factor expression by the ventral lamina terminalis. Proc Natl Acad Sci USA 90: 7681-7685, 1993. (Pubitemid 23250014)
64. Kreutzberg GW. Microglia: a censor for pathological events in the CNS. Trends Neurosci 19: 312-318, 1996.
65. Lacroix S, Rivest S. Effect of acute systemic inflammatory response and cytokines on the transcription of the genes encoding cyclooxygenase enzymes (COX-1 and COX-2) in the rat brain. J Neurochem 70: 452-466, 1998. (Pubitemid 28079333)
66. Larsen PJ, Mikkelsen JD. Functional identification of central afferent projection conveying information of acute "stress" to the hypothalamic paraventricular nucleus. J Neurosci 15: 2609-2627, 1995.
67. Lebel E, Vallières L, Rivest S. Selective involvement of interleukin-6 in the transcriptional activation of the suppressor of cytokine signaling-3 in the brain during systemic immune challenges. Endocrinology 141: 3749-3763. 2000. (Pubitemid 30815700)
68. Ludwig M. Dendritic release of vasopressin and oxytocin. J Neuroendocrinol 10: 881-895, 1998.
69. Mander TH, Morris JF. Immunophenotypic evidence for distinct populations of microglia in the rat hypothalamo-neurohypophysial system. Cell Tissue Res 280: 665-673, 1995.
70. Marcoux J, McArthur DA, Miller C, Glenn TC, Villablance P, Martin NA, Hovda DA, Alger JR, Vespa PM. Persistent metabolic crisis as measured by elevated cerebral microdialysis lactate-pyruvate ratio predicts chronic frontal lobe brain atrophy after traumatic brain injury. Crit Care Med 36: 2871-2877, 2008.
71. Mercier F, Kitasako JT, Hatton GI. Fractones and other basal laminae in the hypothalamus. J Comp Neurol 455: 324-340, 2003. (Pubitemid 36076500)
72. Nadeau S, Rivest S. Glucocorticoids play a fundamental role in protecting the brain during innate immune response. J Neurosci 23: 5536-5544, 2003. (Pubitemid 36807829)
73. Neumann I, Ludwig M, Engelmann M, Pittman QJ, Landgraf R. Simultaneous microdialysis in blood and brain: oxytocin and vasopressin release in response to central and peripheral osmotic stimulation and suckling in the rat. Neuroendocrinology 58: 637-645, 1993. (Pubitemid 24008622)
74. Nguyen MD, Julien JP, Rivest S. Innate immunity: The missing link in neuroprotection and neurodegeneration? Nat Rev Neurosci 3: 216-227, 2002. (Pubitemid 135706591)
75. Niimi M, Sato M, Wada Y, Takahara J, Kawanishi K. Effect of central and continuous intravenous injection of interleukin-1 beta on brain c-fos expression in the rat: involvement of prostaglandins. Neuroimmunomodulation 3: 87-92, 1996. (Pubitemid 26373863)
76. Oldfield BJ, Bicknell RJ, McAllen RM, Weisinger RS, McKinley MJ. Intravenous hypertonic saline induces Fos immunoreactivity in neurons throughout the lamina terminalis. Brain Res 561: 151-156, 1991.
77. Oliet SH, Bourque CW. Gadolinium uncouples mechanical detection and osmoreceptor potential in supraoptic neurons. Neuron 16: 175-181, 1996.
78. Olivadoti M, Opp M. Effects of i.c.v. administration of interleukin-1 on sleep and body temperature of interleukin-6-deficient mice. Neuroscience 153: 338-348, 2008.
79. Palkovits M, Deli M, Gallatz K, Toth Z, Buzas E, Falus A. Highly activated c-fos expression in specific brain regions (ependyma, circumventricular organs, choroid plexus) of histidine decarboxylase deficient mice in response to formalin-induced acute pain. Neuropharmacology 53: 101-112, 2007. (Pubitemid 47125949)
80. Pellegrino LJ, Pellegrino AS, Cushman AJ. A Stereotaxic Atlas of the Rat Brain. New York: Plenum, 1981.
81. Petersson M, Wiberg U, Lundeberg T, Uvnäs-Moberg K. Oxytocin decreases carrageenan induced inflammation in rats. Peptides 22: 1479-1484, 2001. (Pubitemid 32770021)
82. Pinteaux E, Inoue W, Schmidt L, Molina-Holgado F, Rothwell NJ, Luheshi GN. Leptin induces interleukin-1beta release from rat microglial cells through a caspase 1-independent mechanism. J Neurochem 102: 826-833, 2007. (Pubitemid 47057280)
83. Pirnik Z, Mravec B, Kiss A. Fos protein expression in mouse hypothalamic paraventricular (PVN) and supraoptic (SON) nuclei upon osmotic stimulus: colocalization with vasopressin, oxytocin, and tyrosine hydroxylase. Neurochem Int 45: 597-607, 2004. (Pubitemid 38844880)
84. Pittman QJ, Chen X, Mouihate A, Hirasawa M, Martin S. Arginine vasopressin, fever and temperature regulation. Prog Brain Res 119: 383-392, 1998. (Pubitemid 29099984)
85. Proescholdt MG, Hutto B, Brady LS, Herkenham M. Studies of cerebrospinal fluid flow and penetration into brain following lateral ventricle and cisterna magna injections of the tracer [14C]inulin in rat. Neuroscience 95: 577-592, 2000.
86. Proescholdt MG, Chakravarty S, Foster JA, Foti SB, Briley EM, Herkenham M. Intracerebroventricular but not intravenous interleukin-1β induces widespread vascular-mediated leukocyte infiltration and immune signal mRNA expression followed by brain-wide glial activation. Neuroscience 112: 731-749, 2002. (Pubitemid 34634166)
87. Raivich G, Bohatschek M, Kloss CUA, Werner A, Jones LL, Kreutzberg GW. Neuroglial activation repertoire in the injured brain: graded response, molecular mechanisms and cues to physiological function. Brain Res Rev 30: 77-105, 1999. (Pubitemid 29331517)
88. Richard D, Bourque CW. Synaptic control of rat supraoptic neurones during osmotic stimulation of the organum vasculosum lamina terminalis in vitro. J Physiol 489: 567-577, 1995. (Pubitemid 26009885)
89. Rinaman L, Stricker EM, Hoffman GE, Verbalis JG. Central c-Fos expression in neonatal and adult rats after subcutaneous injection of hypertonic saline. Neuroscience 79: 1165-1175, 1997. (Pubitemid 27293766)
90. Rizoli SB, Rhind SG, Shek PN, Inaba K, Filips D, Tien H, Brenneman F, Rotstein O. The immunomodulatory effects of hypertonic saline resuscitation in patients sustaining traumatic hemorrhagic shock: a randomized, controlled, double-blinded trial. Ann Surg 243: 47-57, 2006. (Pubitemid 43054054)
91. Robinson AP, White TM, Mason DW. Macrophage heterogeneity in the rat as delineated by two monoclonal antibodies MRC OX-41 and MRC OX-42, the latter recognizing complement receptor type 3. Immunology 57: 239-247, 1986.
92. Rusnak M, House SB, Arima H, Gainer H. Ciliary neurotrophic factor increases the survival of magnocellular vasopressin and oxytocin neurons in rat supraoptic nucleus in organotypic cultures. Micro Res Tech 56: 101-112, 2002. (Pubitemid 34087760)
93. Sawchenko PE, Swanson LW. The organization of forebrain afferents to the paraventricular and supraoptic nuclei of the rat. J Comp Neurol 218: 121-144, 1983.
94. Scarlett JM, Jobst EE, Enriori PJ, Bowe DD, Batra AK, Grant WF, Cowley MA, Marks DL. Regulation of central melanocortin signaling by interleukin-1β. Endocrinology 148: 4217-4225, 2007.
95. Schiltz JC, Sawchenko PE. Specificity and generality of the involvement of catecholaminergic afferents in hypothalamic responses to immune insults. J Comp Neurol 502: 455-467, 2007.
96. Schobitz B, de Kloet ER, Sutanto W, Holsboer F. Cellular localization of interleukin 6 mRNA and interleukin 6 receptor mRNA in rat brain. Eur J Neurosci 5: 1426-1435, 1993. (Pubitemid 23325225)
97. Sharp FR, Sagar SM, Hicks K, Lowenstein D, Hisanaga K. c-Fos mRNA, Fos, and Fos-related antigen induction by hypertonic saline and stress. J Neurosci 11: 2321-2331, 1991.
98. Shukla A, Hashiguchi N, Chen Y, Coimbra R, Hoyt DB, Junger WG. Osmotic regulation of cell function and possible clinical applications. Shock 21: 391-400, 2004.
99. Siesjö BK, Katsura K, Mellergård P, Ekholm A, Lundgren J, Smith ML. Acidosis-related brain damage. Prog Brain Res 96: 23-48, 1993.
100. Siesjö BK. Pathophysiology and treatment of focal cerebral ischemia. Part I: Pathophysiology. J Neurosurg 77: 169-184, 1992.
101. Sims JE, Gayle MA, Slack JL, Alderson MR, Bird TA, Giri JG, Colotta F, Re F, Mantovani A, Shanebeck K, Grabstein KH, Dower SK. Interleukin 1 signaling occurs exclusively via type I receptor. Proc Natl Acad Sci USA 90: 6155-6159, 1993. (Pubitemid 23191473)
102. Srinivasan D, Yen J, Joseph DJ, Friedman W. Cell type-specific interleukin-1β signaling in the CNS. J Neurosci 24: 6482-6488, 2004. (Pubitemid 38971695)
103. Staudenmayer KL, Maier RV, Jelacic S, Bulger EM. Hypertonic saline modulates innate immunity in a model of systemic inflammation. Shock 23: 459-463, 2005. (Pubitemid 40571670)
104. Sternberg E. Neural regulation of innate immunity: a coordinated nonspecific host response to pathogens. Nature 6: 318-328, 2006.
105. Summy-Long JY, Hu S, Pruss A, Chen X, Phillips TM. Response of Interleukin-1β in the magnocellular system to salt-loading. J Neuroendocrinol 18: 926-937, 2006. (Pubitemid 44660626)
106. Summy-Long JY, Hu S, Long A, Phillips TM. Interleukin-1β release in the supraoptic nucleus area during osmotic stimulation requires neural function. J Neuroendocrinol 20: 1224-1232, 2008.
107. Sundar SK, Becker KJ, Cierpial MA, Carpenter MD, Rankin LA, Fleener SL, Ritchie JC, Simson PE, Weiss JM. Intracerebroventricular infusion of interleukin 1 rapidly decreases peripheral cellular immune responses. Proc Natl Acad Sci USA 86: 6398-6402, 1989.
108. Swanson LW, Sawchenko PE. Hypothalamic integration: Organization of the paraventricular and supraoptic nuclei. Annu Rev Neurosci 6: 269-324, 1983.
109. Tonelli L, Webster JI, Rapp KL, Sternberg E. Neuroendocrine responses regulating susceptibility and resistance to autoimmune/inflammatory disease in inbred rat strains. Immunol Rev 184: 203-211, 2001. (Pubitemid 34123776)
110. Uvnas-Moberg K. Oxytocin linked antistress effects-the relaxation and growth response. Acta Physiol Scand 640: 38-42, 1997. (Pubitemid 27496277)
111. Uvnas-Moberg K, Ahlenius S, Hillegaart V, Alster P. High doses of oxytocin cause sedation and low doses cause an anxiolytic-like effect in male rats. Pharmacol Biochem Behav 49: 101-106, 1994. (Pubitemid 2136891)
112. Vallières L, Lacroix S, Rivest S. Influence of interleukin-6 on neural activity and transcription of the gene encoding corticotrophin-releasing factor in the rat brain: an effect depending upon the route of administration. Eur J Neurosci 9: 1461-1472, 1997. (Pubitemid 27303246)
113. Van Dam AM, Bauer J, Tilders FJH, Berkenbosch F. Endotoxin-induced appearance of immunoreactive interleukin-1β in ramified microglia in rat brain: a light and electron microscopic study. Neuroscience 65: 815-826, 1995.
114. Verbalis JG, Mangione MP, Stricker EM. Oxytocin produces natriuresis in rats at physiological plasma concentrations. Endocrinology 128: 1317-1322, 1991.
115. Watkins LR, Thurston CL, Fleshner M. Phenylephrine-induced antinociception: investigations of potential neural and endocrine bases. Brain Res 528: 273-284, 1990. (Pubitemid 20318206)
116. Watt JA, Bone S, Pressler M, Cranston HJ, Paden CM. Ciliary neurotrophic factor is expressed in the magnocellular neurosecretory system of the rat in vivo: evidence for injury- and activity-induced upregulation. Exp Neurol 197: 206-214, 2006. (Pubitemid 41819088)
117. Watt JA, Cranston HJ, Paden CM. Interleukin-1 receptor type 1 expression in the magnocellular neurosecretory system of the rat: Evidence for activity-dependent regulation. Soc Neurosci Abstr Program No 73.2. 2004, Abstract Viewer/Itinerary Planner, Washington, DC: Society for Neuroscience, 2004.
118. Watt JA, Hobbs NK. Interleukin-1β immunoreactivity in identified neurons of the rat magnocellular neurosecretory system: evidence for activity-dependent release. J Neurosci Res 60: 478-489, 2000.
119. Watts AG, Sanchez-Watts, G. Interactions between heterotypic stressors and corticosterone reveal integrative mechanisms for controlling corticotropin-releasing hormone gene expression in the rat paraventricular nucleus. J Neurosci 22: 6282-6289, 2002. (Pubitemid 35387669)
120. Wessel TC, Joh TH, Volpe BR. In situ hybridization analysis of c-fos and c-jun expression in the rat brain following transient forebrain ischemia. Brain Res 567: 231-240. 1991.
121. Woodroofe MN, Sarna GS, Wadhwa M, Hayes GM, Loughlin AJ, Tinker A, Cuzner ML. Detection of interleukin-1 and interleukin-6 in adult rat brain, following mechanical injury, by in vivo microdialysis: evidence of a role for microglia in cytokine production. J Neuroimmunol 33: 227-236, 1991.
122. Xiong JJ, Hatton GI. Differential responses of oxytocin and vasopressin neurons to the osmotic and stressful components of hypertonic saline injections: a Fos protein double-labeling study. Brain Res 719: 143-153, 1996.
123. Yabuuchi K, Minami M, Katsumata S, Satoh M. Localization of type I interleukin-1 receptor mRNA in the rat brain. Mol Brain Res 27: 27-36, 1994. (Pubitemid 24324085)
124. Yang H, Wang L, Ju G. Evidence for hypothalamic paraventricular nucleus as an integrative center of neuroimmunomodulation. Neuroimmunomodulation 4: 120-127, 2009.
125. Yao J, Keri JE, Taffs RE, Colton CA. Characterization of interleukin-1 production by microglia in culture. Brain Res 591: 88-93, 1992.
126. Yasuda K, Churchill L, Yasuda T, Blindheim K, Falter M, Krueger JM. Unilateral cortical appication of interleukin-1β (IL1β) induces asymmetry in fos, IL1β and nerve growth factor immunoreactivity: implications for sleep regulation. Brain Res 1131: 44-59, 2007. (Pubitemid 46075115)