Age-impaired fluid homeostasis depends on the balance of IL-6/IGF-I in the rat supraoptic nuclei

Neurobiology of Aging

Volumn 30, Issue 10, 2009, Pages 1677-1692

  Palin, K ^a   Moreau, M L ^a   Orcel, H ^b   Duvoid Guillou, A ^b   Rabie A ^b   Kelley, K W ^c   Moos, F ^a  

^a UNIVERSITÉ DE BORDEAUX   (France)

^b INSTITUT DE GÉNOMIQUE FONCTIONNELLE   (France)

^c Laboratory of Integrative Immunophysiology   (United States)

Author keywords

Cytokine; Growth factor; Hormone; Lipopolysaccharide; Neurohypophyseal system; Vasopressin; Water balance

Indexed keywords

ARGIPRESSIN; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; MESSENGER RNA; PROTEIN C FOS; SOMATOMEDIN;

AGE DISTRIBUTION; AGED; AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIURESIS; FLUID BALANCE; GENE EXPRESSION; HORMONE BLOOD LEVEL; MALE; NERVE CELL STIMULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SUPRAOPTIC NUCLEUS;

EID: 69249220390     PISSN: 01974580     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2007.12.006     Document Type: Article

References (76)

1. Armstrong W.E. Morphological and electrophysiological classification of hypothalamic supraoptic neurons. Prog. Neurobiol. 47 4-5 (1995) 291-339
2. Beishuizen A., and Thijs L.G. Endotoxin and the hypothalamo-pituitary-adrenal (HPA) axis. J. Endotoxin Res. 9 1 (2003) 3-24
3. Ben-Barak Y., Russell J.T., Whitnall M.H., Ozato K., and Gainer H. Neurophysin in the hypothalamo-neurohypophysial system. I. Production and characterization of monoclonal antibodies. J. Neurosci. 5 1 (1985) 81-97
4. Bourque C.W., Ciura S., Trudel E., Stachniak T.J., and Sharif-Naeini R. Neurophysiological characterization of mammalian osmosensitive neurones. Exp. Physiol. 92 3 (2007) 499-505
5. Cappola A.R., Xue Q.L., Ferrucci L., Guralnik J.M., Volpato S., and Fried L.P. Insulin-like growth factor I and interleukin-6 contribute synergistically to disability and mortality in older women. J. Clin. Endocrinol. Metab. 88 5 (2003) 2019-2025
6. Chakfe Y., Zhang Z., and Bourque C.W. IL-1beta directly excites isolated rat supraoptic neurons via upregulation of the osmosensory cation current. Am. J. Physiol. 290 5 (2006) R1183-R1190
7. Ciura S., and Bourque C.W. Transient receptor potential vanilloid 1 is required for intrinsic osmoreception in organum vasculosum lamina terminalis neurons and for normal thirst responses to systemic hyperosmolality. J. Neurosci. 26 35 (2006) 9069-9075
8. Corman B., Roinel N., and Geelen G. Plasma vasopressin and cortical nephron function in aging rats. Mech. Ageing Dev. 62 3 (1992) 263-277
9. Cunningham Jr. E.T., and Sawchenko P.E. Reflex control of magnocellular vasopressin and oxytocin secretion. Trends Neurosci. 14 9 (1991) 406-410
10. Curran T., and Morgan J.I. Memories of fos. Bioessays 7 6 (1987) 255-258
11. Daynes R.A., Araneo B.A., Ershler W.B., Maloney C., Li G.Z., and Ryu S.Y. Altered regulation of IL-6 production with normal aging. Possible linkage to the age-associated decline in dehydroepiandrosterone and its sulfated derivative. J. Immunol. 150 12 (1993) 5219-5230
12. De Benedetti F., Alonzi T., Moretta A., Lazzaro D., Costa P., Poli V., Martini A., Ciliberto G., and Fattori E. Interleukin 6 causes growth impairment in transgenic mice through a decrease in insulin-like growth factor-I. A model for stunted growth in children with chronic inflammation. J. Clin. Invest. 99 4 (1997) 643-650
13. De Simoni M.G., Terreni L., Chiesa R., Mangiarotti F., and Forloni G.L. Interferon-gamma potentiates interleukin (IL)-6 and tumor necrosis factor-alpha but not IL-1beta induced by endotoxin in the brain. Endocrinology 138 12 (1997) 5220-5226
14. Desson S.E., and Ferguson A.V. Interleukin 1beta modulates rat subfornical organ neurons as a result of activation of a non-selective cationic conductance. J. Physiol. 550 Pt 1 (2003) 113-122
15. Ershler W.B. Interleukin-6: a cytokine for gerontologists. J. Am. Geriatr. Soc. 41 2 (1993) 176-181
16. Fliers E., and Swaab D.F. Activation of vasopressinergic and oxytocinergic neurons during aging in the Wistar rat. Peptides 4 2 (1983) 165-170
17. Fliers E., Swaab D.F., Pool C.W., and Verwer R.W. The vasopressin and oxytocin neurons in the human supraoptic and paraventricular nucleus: changes with aging and in senile dementia. Brain Res. 342 1 (1985) 45-53
18. Fong A.C., Hardman J.M., and Porta E.A. Immunocytochemical hormonal features of pituitary adenomas of aging Wistar male rats. Mech. Ageing Dev. 20 2 (1982) 141-154
19. Frolkis V.V., Golovchenko S.F., Medved V.I., and Frolkis R.A. Vasopressin and cardiovascular system in aging. Gerontology 28 5 (1982) 290-302
20. Ghorbel M.T., Sharman G., Leroux M., Barrett T., Donovan D.M., Becker K.G., and Murphy D. Microarray analysis reveals interleukin-6 as a novel secretory product of the hypothalamo-neurohypophyseal system. J. Biol. Chem. 278 21 (2003) 19280-19285
21. Giusti-Paiva A., Branco L.G., de Castro M., Antunes-Rodrigues J., and Carnio E.C. Role of nitric oxide in thermoregulation during septic shock: involvement of vasopressin. Pflugers Arch. 447 2 (2003) 175-180
22. Godbout J.P., and Johnson R.W. Interleukin-6 in the aging brain. J. Neuroimmunol. 147 1-2 (2004) 141-144
23. Gonzalez-Hernandez T., Afonso-Oramas D., Cruz-Muros I., Barroso-Chinea P., Abreu P., del Mar Perez-Delgado M., Rancel-Torres N., and del Carmen Gonzalez M. Interleukin-6 and nitric oxide synthase expression in the vasopressin and corticotrophin-releasing factor systems of the rat hypothalamus. J. Histochem. Cytochem. 54 4 (2006) 427-441
24. Goudsmit E., Fliers E., and Swaab D.F. Vasopressin and oxytocin excretion in the Brown-Norway rat in relation to aging, water metabolism and testosterone. Mech. Ageing Dev. 44 3 (1988) 241-252
25. Harre E.M., Roth J., Pehl U., Kueth M., Gerstberger R., and Hubschle T. Selected contribution: role of IL-6 in LPS-induced nuclear STAT3 translocation in sensory circumventricular organs during fever in rats. J. Appl. Physiol. 92 6 (2002) 2657-2666
26. Hoogendijk J.E., Fliers E., Swaab D.F., and Verwer R.W. Activation of vasopressin neurons in the human supraoptic and paraventricular nucleus in senescence and senile dementia. J. Neurol. Sci. 69 3 (1985) 291-299
27. Hubschle T., Thorn E., Watson A., Roth J., Klaus S., and Meyerhof W. Leptin-induced nuclear translocation of STAT3 immunoreactivity in hypothalamic nuclei involved in body weight regulation. J. Neurosci. 21 7 (2001) 2413-2424
28. Inoue T., Saito H., Fukushima R., Inaba T., Lin M.T., Fukatsu K., and Muto T. Growth hormone and insulin like growth factor I enhance host defense in a murine sepsis model. Arch. Surg. 130 10 (1995) 1115-1122
29. Ishunina T.A., Salehi A., Hofman M.A., and Swaab D.F. Activity of vasopressinergic neurones of the human supraoptic nucleus is age- and sex-dependent. J. Neuroendocrinol. 11 4 (1999) 251-258
30. Ishunina T.A., and Swaab D.F. Neurohypophyseal peptides in aging and Alzheimer's disease. Ageing Res. Rev. 1 3 (2002) 537-558
31. Ishunina T.A., and Swaab D.F. Vasopressin and oxytocin neurons of the human supraoptic and paraventricular nucleus: size changes in relation to age and sex. J. Clin. Endocrinol. Metab. 84 12 (1999) 4637-4644
32. Itoh H., Kaneko M., Ohshima S., Shumiya S., and Sakaguchi E. Effect of low protein and low energy diet on physiological status and digestibility of F344 rats. Exp. Anim. 51 5 (2002) 485-491
33. Kasting N.W. Characteristics of body temperature, vasopressin, and oxytocin responses to endotoxin in the rat. Can. J. Physiol. Pharmacol. 64 12 (1986) 1575-1578
34. Kasting N.W., Mazurek M.F., and Martin J.B. Endotoxin increases vasopressin release independently of known physiological stimuli. Am. J. Physiol. 248 4 Pt 1 (1985) E420-E424
35. Khan A.S., Sane D.C., Wannenburg T., and Sonntag W.E. Growth hormone, insulin-like growth factor-1 and the aging cardiovascular system. Cardiovasc. Res. 54 1 (2002) 25-35
36. Konsman J.P., Kelley K., and Dantzer R. Temporal and spatial relationships between lipopolysaccharide-induced expression of Fos, interleukin-lbeta and inducible nitric oxide synthase in rat brain. Neuroscience 89 2 (1999) 535-548
37. Landgraf R., Neumann I., Holsboer F., and Pittman Q.J. Interleukin-1 beta stimulates both central and peripheral release of vasopressin and oxytocin in the rat. Eur. J. Neurosci. 7 4 (1995) 592-598
38. Li Z., Inenage K., Kawano S., Kannan H., and Yamashita H. Interleukin-1 beta directly excites hypothalamic supraoptic neurons in rats in vitro. Neuroreport 3 1 (1992) 91-93
39. Lucassen P.J., Ravid R., Gonatas N.K., and Swaab D.F. Activation of the human supraoptic and paraventricular nucleus neurons with aging and in Alzheimer's disease as judged from increasing size of the Golgi apparatus. Brain Res. 632 1-2 (1993) 105-113
40. Lucassen P.J., Salehi A., Pool C.W., Gonatas N.K., and Swaab D.F. Activation of vasopressin neurons in aging and Alzheimer's disease. J. Neuroendocrinol. 6 6 (1994) 673-679
41. Mastorakos G., Weber J.S., Magiakou M.A., Gunn H., and Chrousos G.P. Hypothalamic-pituitary-adrenal axis activation and stimulation of systemic vasopressin secretion by recombinant interleukin-6 in humans: potential implications for the syndrome of inappropriate vasopressin secretion. J. Clin. Endocrinol. Metab. 79 4 (1994) 934-939
42. Matsunaga W., Miyata S., Takamata A., Bun H., Nakashima T., and Kiyohara T. LPS-induced Fos expression in oxytocin and vasopressin neurons of the rat hypothalamus. Brain Res. 858 1 (2000) 9-18
43. McKinley M.J., Mathai M.L., McAllen R.M., McClear R.C., Miselis R.R., Pennington G.L., Vivas L., Wade J.D., and Oldfield B.J. Vasopressin secretion: osmotic and hormonal regulation by the lamina terminalis. J. Neuroendocrinol. 16 4 (2004) 340-347
44. Miller M. Nocturnal polyuria in older people: pathophysiology and clinical implications. J. Am. Geriatr. Soc. 48 10 (2000) 1321-1329
45. Morgan J.I., and Curran T. Stimulus-transcription coupling in neurons: role of cellular immediate-early genes. Trends Neurosci. 12 11 (1989) 459-462
46. Paxinos G., and Watson C. The Rat Brain in Stereotaxic Coordinates (2005), Elsevier
47. Perlstein R.S., Whitnall M.H., Abrams J.S., Mougey E.H., and Neta R. Synergistic roles of interleukin-6, interleukin-1, and tumor necrosis factor in the adrenocorticotropin response to bacterial lipopolysaccharide in vivo. Endocrinology 132 3 (1993) 946-952
48. Prechel M.M., Halbur L., Devata S., Vaidya A.M., and Young M.R. Increased interleukin-6 production by cerebral cortical tissue of adult versus young mice. Mech. Ageing Dev. 92 2-3 (1996) 185-194
49. Ravid R., Fliers E., Swaab D.F., and Zurcher C. Changes in vasopressin and testosterone in the senescent Brown-Norway (BN/BiRij) rat. Gerontology 33 2 (1987) 87-98
50. Rink L., Cakman I., and Kirchner H. Altered cytokine production in the elderly. Mech. Ageing Dev. 102 2-3 (1998) 199-209
51. Rivest S., and Laflamme N. Neuronal activity and neuropeptide gene transcription in the brains of immune-challenged rats. J. Neuroendocrinol. 7 7 (1995) 501-525
52. Rummel C., Hubschle T., Gerstberger R., and Roth J. Nuclear translocation of the transcription factor STAT3 in the guinea pig brain during systemic or localized inflammation. J. Physiol. 557 Pt 2 (2004) 671-687
53. Serri O., St-Jacques P., Sartippour M., and Renier G. Alterations of monocyte function in patients with growth hormone (GH) deficiency: effect of substitutive GH therapy. J. Clin. Endocrinol. Metab. 84 1 (1999) 58-63
54. Sesmilo G., Biller B.M., Llevadot J., Hayden D., Hanson G., Rifai N., and Klibanski A. Effects of growth hormone administration on inflammatory and other cardiovascular risk markers in men with growth hormone deficiency. A randomized, controlled clinical trial. Ann. Intern. Med. 133 2 (2000) 111-122
55. Sharif Naeini R., Ciura S., and Bourque C.W. TRPVs: ion channels that make you thirsty!. Med. Sci. (Paris) 22 12 (2006) 1035-1037
56. Sheehy C.M., Perry P.A., and Cromwell S.L. Dehydration: biological considerations, age-related changes, and risk factors in older adults. Biol. Res. Nurs. 1 1 (1999) 30-37
57. Shi L., Linville M.C., Tucker E.W., Sonntag W.E., and Brunso-Bechtold J.K. Differential effects of aging and insulin-like growth factor-1 on synapses in CA1 of rat hippocampus. Cereb. Cortex 15 5 (2005) 571-577
58. Smale L., Castleberry C., and Nunez A.A. Fos rhythms in the hypothalamus of Rattus and Arvicanthis that exhibit nocturnal and diurnal patterns of rhythmicity. Brain Res. 899 1-2 (2001) 101-105
59. Sonntag W.E., Lynch C.D., Bennett S.A., Khan A.S., Thornton P.L., Cooney P.T., Ingram R.L., McShane T., and Brunso-Bechtold J.K. Alterations in insulin-like growth factor-1 gene and protein expression and type 1 insulin-like growth factor receptors in the brains of ageing rats. Neuroscience 88 1 (1999) 269-279
60. Spies M., Nesic O., Barrow R.E., Perez-Polo J.R., and Herndon D.N. Liposomal IGF-1 gene transfer modulates pro- and anti-inflammatory cytokine mRNA expression in the burn wound. Gene Ther. 8 18 (2001) 1409-1415
61. Ster J., Colomer C., Monzo C., Duvoid-Guillou A., Moos F., Alonso G., and Hussy N. Insulin-like growth factor-1 inhibits adult supraoptic neurons via complementary modulation of mechanoreceptors and glycine receptors. J. Neurosci. 25 9 (2005) 2267-2276
62. Swanson L.W. Brain Maps: Structure of the Rat Brain (2004), Elsevier Academic Press
63. Swanson L.W., and Sawchenko P.E. Hypothalamic integration: organization of the paraventricular and supraoptic nuclei. Annu. Rev. Neurosci. 6 (1983) 269-324
64. Terrazzino S., Perego C., De Luigi A., and De Simoni M.G. Interleukin-6, tumor necrosis factor and corticosterone induction by central lipopolysaccharide in aged rats. Life Sci. 61 7 (1997) 695-701
65. Terwel D., Markerink M., and Jo lles J. Age-related changes in concentrations of vasopressin in the central nervous system and plasma of the male Wistar rat. Mech. Ageing Dev. 65 2-3 (1992) 127-136
66. van Enckevort F.H., Sweep C.G., Span P.N., Demacker P.N., Hermsen C.C., and Hermus A.R. Reduced adrenal response to bacterial lipopolysaccharide in interleukin-6-deficient mice. J. Endocrinol. Invest. 24 10 (2001) 786-795
67. Van Wagoner N.J., and Benveniste E.N. Interleukin-6 expression and regulation in astrocytes. J. Neuroimmunol. 100 1-2 (1999) 124-139
68. Van Wagoner N.J., Oh J.W., Repovic P., and Benveniste E.N. Interleukin-6 (IL-6) production by astrocytes: autocrine regulation by IL-6 and the soluble IL-6 receptor. J. Neurosci. 19 13 (1999) 5236-5244
69. Wainwright A., Rutter A.R., Seabrook G.R., Reilly K., and Oliver K.R. Discrete expression of TRPV2 within the hypothalamo-neurohypophysial system: implications for regulatory activity within the hypothalamic-pituitary-adrenal axis. J. Comp. Neurol. 474 1 (2004) 24-42
70. Whitnall M.H., Key S., Ben-Barak Y., Ozato K., and Gainer H. Neurophysin in the hypothalamo-neurohypophysial system. II. Immunocytochemical studies of the ontogeny of oxytocinergic and vasopressinergic neurons. J. Neurosci. 5 1 (1985) 98-109
71. Windle R.J., Forsling M.L., and Guzek J.W. Daily rhythms in the hormone content of the neurohypophysial system and release of oxytocin and vasopressin in the male rat: effect of constant light. J. Endocrinol. 133 2 (1992) 283-290
72. Yaghmaie F., Saeed O., Garan S.A., Voelker M.A., Gouw A.M., Freitag W., Sternberg H., and Timiras P.S. Age-dependent loss of insulin-like growth factor-1 receptor immunoreactive cells in the supraoptic hypothalamus is reduced in calorically restricted mice. Int. J. Dev. Neurosci. 24 7 (2006) 431-436
73. Ye P., Price W., Kassiotis G., Kollias G., and D'Ercole A.J. Tumor necrosis factor-alpha regulation of insulin-like growth factor-I, type 1 IGF receptor, and IGF binding protein expression in cerebellum of transgenic mice. J. Neurosci. Res. 71 5 (2003) 721-731
74. Ye S.M., and Johnson R.W. Increased interleukin-6 expression by microglia from brain of aged mice. J. Neuroimmunol. 93 1-2 (1999) 139-148
75. Ye S.M., and Johnson R.W. Regulation of interleukin-6 gene expression in brain of aged mice by nuclear factor kappaB. J. Neuroimmunol. 117 1-2 (2001) 87-96
76. Zhou X., Herman J.P., and Paden C.M. Evidence that IGF-I acts as an autocrine/paracrine growth factor in the magnocellular neurosecretory system: neuronal synthesis and induction of axonal sprouting. Exp. Neurol. 159 2 (1999) 419-432