Mechanisms involved in dual vasopressin/apelin neuron dysfunction during aging

PLoS ONE

Volumn 9, Issue 2, 2014, Pages

  Sauvant, Julie ^a,b   Delpech, Jean Christophe ^a,b   Palin, Karine ^a,b   De Mota, Nadia ^c   Dudit, Jennifer ^a,b   Aubert, Agnès ^a,b   Orcel, Hélène ^d   Roux, Pascale ^a,b   Layé, Sophie ^a,b   Moos, Françoise ^a,b   Llorens Cortes, Catherine ^c   Nadjar, Agnès ^a,b  

^a NutriNeuro Bordeaux University   (France)

^b UNIVERSITÉ DE BORDEAUX   (France)

^c PSL RESEARCH UNIVERSITY   (France)

^d INSTITUT DE GÉNOMIQUE FONCTIONNELLE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

APELIN; ARGIPRESSIN; GLIAL FIBRILLARY ACIDIC PROTEIN; INTERLEUKIN 6; MESSENGER RNA; MINOCYCLINE; RUTHENIUM RED; VANILLOID RECEPTOR 2; VASOPRESSIN;

ADULT; AGED; AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; COMPARATIVE STUDY; CONTROLLED STUDY; CORRELATIONAL STUDY; CYTOKINE PRODUCTION; DEHYDRATION; HOMEOSTASIS; MALE; MICROGLIA; MORPHOLOGICAL ADAPTATION; NERVE CELL PLASTICITY; NERVOUS SYSTEM FUNCTION; NERVOUS SYSTEM INFLAMMATION; NEUROLOGIC DISEASE; NONHUMAN; OSMOSIS; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; RAT; SUPRAOPTIC NUCLEUS; VASOPRESSIN BLOOD LEVEL;

AGING; ANIMALS; ANTI-BACTERIAL AGENTS; ASTROCYTES; GENE EXPRESSION REGULATION; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; INTERLEUKIN-6; MALE; MINOCYCLINE; NEURONS; OSMOTIC PRESSURE; RATS; RATS, WISTAR; TRPV CATION CHANNELS; VASOPRESSINS;

EID: 84895549129     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0087421     Document Type: Article

References (74)

1. Jequier E, Constant F (2010) Water as an essential nutrient: the physiological basis of hydration. Eur J Clin Nutr 64: 115-123.
2. Phillips PA, Rolls BJ, Ledingham JG, Forsling ML, Morton JJ, et al. (1984) Reduced thirst after water deprivation in healthy elderly men. N Engl J Med 311: 753-759. (Pubitemid 14026225)
3. den Ouden DT, Meinders AE (2005) Vasopressin: physiology and clinical use in patients with vasodilatory shock: a review. Neth J Med 63: 4-13. (Pubitemid 40214673)
4. Robert J, Clauser ER (2005) [Vasopressin receptors: structure/function relationships and signal transduction in target cells]. J Soc Biol 199: 351-359.
5. De Mota N, Reaux-Le Goazigo A, El Messari S, Chartrel N, Roesch D, et al. (2004) Apelin, a potent diuretic neuropeptide counteracting vasopressin actions through inhibition of vasopressin neuron activity and vasopressin release. Proc Natl Acad Sci U S A 101: 10464-10469. (Pubitemid 38924948)
6. Reaux A, De Mota N, Skultetyova I, Lenkei Z, El Messari S, et al. (2001) Physiological role of a novel neuropeptide, apelin, and its receptor in the rat brain. J Neurochem 77: 1085-1096. (Pubitemid 32467063)
7. Reaux-Le Goazigo A, Morinville A, Burlet A, Llorens-Cortes C, Beaudet A (2004) Dehydration-induced cross-regulation of apelin and vasopressin immunoreactivity levels in magnocellular hypothalamic neurons. Endocrinology 145: 4392-4400. (Pubitemid 39120589)
8. Azizi M, Iturrioz X, Blanchard A, Peyrard S, De Mota N, et al. (2008) Reciprocal regulation of plasma apelin and vasopressin by osmotic stimuli. J Am Soc Nephrol 19: 1015-1024.
9. Llorens-Cortes C, Moos F (2008) Opposite potentiality of hypothalamic coexpressed neuropeptides, apelin and vasopressin in maintaining body-fluid homeostasis. Prog Brain Res 170: 559-570. (Pubitemid 352010251)
10. Fliers E, Swaab DF, Pool CW, Verwer RW (1985) The vasopressin and oxytocin neurons in the human supraoptic and paraventricular nucleus; changes with aging and in senile dementia. Brain Res 342: 45-53. (Pubitemid 16242863)
11. Palin K, Moreau ML, Sauvant J, Orcel H, Nadjar A, et al. (2009) Interleukin-6 activates arginine vasopressin neurons in the supraoptic nucleus during immune challenge in rats. Am J Physiol Endocrinol Metab 296: E1289-1299.
12. Hoogendijk JE, Fliers E, Swaab DF, Verwer RW (1985) Activation of vasopressin neurons in the human supraoptic and paraventricular nucleus in senescence and senile dementia. J Neurol Sci 69: 291-299. (Pubitemid 15074624)
13. Lucassen PJ, Ravid R, Gonatas NK, Swaab DF (1993) 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: 105-113. (Pubitemid 24015508)
14. Lucassen PJ, Salehi A, Pool CW, Gonatas NK, Swaab DF (1994) Activation of vasopressin neurons in aging and Alzheimer's disease. J Neuroendocrinol 6: 673-679.
15. Palin K, Moreau ML, Orcel H, Duvoid-Guillou A, Rabie A, et al. (2009) Age-impaired fluid homeostasis depends on the balance of IL-6/IGF-I in the rat supraoptic nuclei. Neurobiol Aging 30: 1677-1692.
16. Toth A, Boczan J, Kedei N, Lizanecz E, Bagi Z, et al. (2005) Expression and distribution of vanilloid receptor 1 (TRPV1) in the adult rat brain. Brain Res Mol Brain Res 135: 162-168. (Pubitemid 40602409)
17. Sudbury JR, Ciura S, Sharif-Naeini R, Bourque CW (2010) Osmotic and thermal control of magnocellular neurosecretory neurons - role of an N-terminal variant of trpv1. Eur J Neurosci 32: 2022-2030.
18. Wainwright A, Rutter AR, Seabrook GR, Reilly K, Oliver KR (2004) Discrete expression of TRPV2 within the hypothalamo-neurohypophysial system: Implications for regulatory activity within the hypothalamic-pituitary-adrenal axis. J Comp Neurol 474: 24-42. (Pubitemid 38685712)
19. Shimosato G, Amaya F, Ueda M, Tanaka Y, Decosterd I, et al. (2005) Peripheral inflammation induces up-regulation of TRPV2 expression in rat DRG. Pain 119: 225-232. (Pubitemid 41752983)
20. Miyata S, Hatton GI (2002) Activity-related, dynamic neuron-glial interactions in the hypothalamo-neurohypophysial system. Microsc Res Tech 56: 143-157. (Pubitemid 34087764)
21. Theodosis DT (2002) Oxytocin-secreting neurons: A physiological model of morphological neuronal and glial plasticity in the adult hypothalamus. Front Neuroendocrinol 23: 101-135.
22. Oliet SH, Bonfardin VD (2010) Morphological plasticity of the rat supraoptic nucleus - cellular consequences. Eur J Neurosci 32: 1989-1994.
23. Panatier A, Oliet SH (2006) Neuron-glia interactions in the hypothalamus. Neuron Glia Biol 2: 51-58. (Pubitemid 43248064)
24. Bonfanti L, Poulain DA, Theodosis DT (1993) Radial glia-like cells in the supraoptic nucleus of the adult rat. J Neuroendocrinol 5: 1-5. (Pubitemid 23189165)
25. Hawrylak N, Boone D, Salm AK (1999) The surface density of glial fibrillary acidic protein immunopositive astrocytic processes in the rat supraoptic nucleus is reversibly altered by dehydration and rehydration. Neurosci Lett 277: 57-60.
26. Hawrylak N, Fleming JC, Salm AK (1998) Dehydration and rehydration selectively and reversibly alter glial fibrillary acidic protein immunoreactivity in the rat supraoptic nucleus and subjacent glial limitans. Glia 22: 260-271. (Pubitemid 28159017)
27. Salm AK, Bobak JB (1999) Dehydration-associated changes in the ventral glial limitans subjacent to the supraoptic nucleus include a reduction in the extent of the basal lamina but not astrocytic process shrinkage. Exp Neurol 160: 425-432.
28. Ogura K, Ogawa M, Yoshida M (1994) Effects of ageing on microglia in the normal rat brain: immunohistochemical observations. Neuroreport 5: 1224-1226. (Pubitemid 24199801)
29. Peters A, Josephson K, Vincent SL (1991) Effects of aging on the neuroglial cells and pericytes within area 17 of the rhesus monkey cerebral cortex. Anat Rec 229: 384-398.
30. Castle SC (2000) Impact of age-related immune dysfunction on risk of infections. Z Gerontol Geriatr 33: 341-349.
31. Ginaldi L, Loreto MF, Corsi MP, Modesti M, De Martinis M (2001) Immunosenescence and infectious diseases. Microbes Infect 3: 851-857. (Pubitemid 32913168)
32. Straub RH, Miller LE, Scholmerich J, Zietz B (2000) Cytokines and hormones as possible links between endocrinosenescence and immunosenescence. J Neuroimmunol 109: 10-15.
33. Gehrmann J, Matsumoto Y, Kreutzberg GW (1995) Microglia: intrinsic immuneffector cell of the brain. Brain Res Brain Res Rev 20: 269-287.
34. Ciosek J (2002) Vasopressin and oxytocin release as influenced by thyrotropinreleasing hormone in euhydrated and dehydrated rats. J Physiol Pharmacol 53: 423-437.
35. Gottlieb HB, Ji LL, Jones H, Penny ML, Fleming T, et al. (2006) Differential effects of water and saline intake on water deprivation-induced c-Fos staining in the rat. Am J Physiol Regul Integr Comp Physiol 290: R1251-1261.
36. Paxinos G, Watson C, Pennisi M, Topple A (1985) Bregma, lambda and the interaural midpoint in stereotaxic surgery with rats of different sex, strain and weight. J Neurosci Methods 13: 139-143. (Pubitemid 15008633)
37. Henry CJ, Huang Y, Wynne A, Hanke M, Himler J, et al. (2008) Minocycline attenuates lipopolysaccharide (LPS)-induced neuroinflammation, sickness behavior, and anhedonia. J Neuroinflammation 5: 15.
38. Konsman JP, Kelley K, Dantzer R (1999) Temporal and spatial relationships between lipopolysaccharide-induced expression of Fos, interleukin-1beta and inducible nitric oxide synthase in rat brain. Neuroscience 89: 535-548. (Pubitemid 29044335)
39. Sharif-Naeini R, Ciura S, Zhang Z, Bourque CW (2008) Contribution of TRPV channels to osmosensory transduction, thirst, and vasopressin release. Kidney Int 73: 811-815. (Pubitemid 351398284)
40. Crawford DC, Moulder KL, Gereau RWt, Story GM, Mennerick S (2009) Comparative effects of heterologous TRPV1 and TRPM8 expression in rat hippocampal neurons. PLoS One 4: e8166.
41. Ishunina TA, Swaab DF (1999) Vasopressin and oxytocin neurons of the human supraoptic and paraventricular nucleus: size changes in relation to age and sex. J Clin Endocrinol Metab 84: 4637-4644.
42. Palin K, Cunningham C, Forse P, Perry VH, Platt N (2008) Systemic inflammation switches the inflammatory cytokine profile in CNS Wallerian degeneration. Neurobiol Dis 30: 19-29.
43. Fliers E, Swaab DF (1983) Activation of vasopressinergic and oxytocinergic neurons during aging in the Wistar rat. Peptides 4: 165-170. (Pubitemid 13047878)
44. Stachenfeld NS, Mack GW, Takamata A, DiPietro L, Nadel ER (1996) Thirst and fluid regulatory responses to hypertonicity in older adults. Am J Physiol 271: R757-765.
45. Terwel D, ten Haaf JA, Markerink M, Jolles J (1992) Changes in plasma vasopressin concentration and plasma osmolality in relation to age and time of day in the male Wistar rat. Acta Endocrinol (Copenh) 126: 357-362.
46. Sladek CD, Olschowka JA (1994) Dehydration induces Fos, but not increased vasopressin mRNA in the supraoptic nucleus of aged rats. Brain Res 652: 207-215. (Pubitemid 24227274)
47. Terwel D, Markerink M, Jolles J (1992) Age-related changes in concentrations of vasopressin in the central nervous system and plasma of the male Wistar rat. Mech Ageing Dev 65: 127-136.
48. Zbuzek VK, Wu WH (1982) Age-related vasopressin changes in rat plasma and the hypothalamo-hypophyseal system. Exp Gerontol 17: 133-138. (Pubitemid 12086309)
49. el Fazaa S, Mahmoud L, Gharbi N, Kamoun A, Gharib C (2000) [The effect of age and dehydration on the activity of the vasopressinergic system in rats]. Tunis Med 78: 132-138.
50. Swenson KL, Sands JM, Jacobs JD, Sladek CD (1997) Effect of aging on vasopressin and aquaporin responses to dehydration in Fischer 344-brown-Norway F1 rats. Am J Physiol 273: R35-40.
51. Sladek CD, McNeill TH, Gregg CM, Blair ML, Baggs RB (1981) Vasopressin and renin response to dehydration in aged rats. Neurobiol Aging 2: 293-302. (Pubitemid 12152576)
52. Catudioc-Vallero J, Sands JM, Klein JD, Sidorowicz HE, Sladek CD (2000) Effect of age and testosterone on the vasopressin and aquaporin responses to dehydration in Fischer 344/Brown-Norway F1 rats. J Gerontol A Biol Sci Med Sci 55: B26-34. (Pubitemid 30140727)
53. Hensellek S, Brell P, Schaible HG, Brauer R, Segond von Banchet G (2007) The cytokine TNFalpha increases the proportion of DRG neurones expressing the TRPV1 receptor via the TNFR1 receptor and ERK activation. Mol Cell Neurosci 36: 381-391. (Pubitemid 47633200)
54. Schaible HG, von Banchet GS, Boettger MK, Brauer R, Gajda M, et al. (2010) The role of proinflammatory cytokines in the generation and maintenance of joint pain. Ann N Y Acad Sci 1193: 60-69.
55. Li Z, Inenage K, Kawano S, Kannan H, Yamashita H (1992) Interleukin-1 beta directly excites hypothalamic supraoptic neurons in rats in vitro. Neuroreport 3: 91-93.
56. Chakfe Y, Zhang Z, Bourque CW (2006) IL-1beta directly excites isolated rat supraoptic neurons via upregulation of the osmosensory cation current. Am J Physiol Regul Integr Comp Physiol 290: R1183-1190.
57. Garcia-Segura LM, Chowen JA, Duenas M, Torres-Aleman I, Naftolin F (1994) Gonadal steroids as promoters of neuro-glial plasticity. Psychoneuroendocrinology 19: 445-453. (Pubitemid 24214316)
58. Alonso G, Runquist M, Hussy N, Duvoid A, Moos F (2003) Age-related modifications of the morphological organization of pituicytes are associated with alteration of the GABAergic and dopaminergic innervation afferent to the neurohypophysial lobe. Eur J Neurosci 18: 1889-1903. (Pubitemid 37372372)
59. Berciano MT, Andres MA, Calle E, Lafarga M (1995) Age-induced hypertrophy of astrocytes in rat supraoptic nucleus: a cytological, morphometric, and immunocytochemical study. Anat Rec 243: 129-144.
60. Jalenques I, Burette A, Albuisson E, Romand R (1997) Age-related changes in GFAP-immunoreactive astrocytes in the rat ventral cochlear nucleus. Hear Res 107: 113-124. (Pubitemid 27216486)
61. Kaur M, Sharma S, Kaur G (2008) Age-related impairments in neuronal plasticity markers and astrocytic GFAP and their reversal by late-onset short term dietary restriction. Biogerontology 9: 441-454.
62. Yoshida T, Goldsmith SK, Morgan TE, Stone DJ, Finch CE (1996) Transcription supports age-related increases of GFAP gene expression in the male rat brain. Neurosci Lett 215: 107-110. (Pubitemid 26313229)
63. Ghorbel MT, Sharman G, Leroux M, Barrett T, Donovan DM, et al. (2003) Microarray analysis reveals interleukin-6 as a novel secretory product of the hypothalamo-neurohypophyseal system. J Biol Chem 278: 19280-19285. (Pubitemid 36799320)
64. Moreau ML, Sauvant J, Moos F, Palin K (2010) Brain insulin growth factor-I induces diuresis increase through the inhibition of arginin-vasopressin release in aged rats. Neurobiol Aging 31: 532-536.
65. Rozovsky I, Finch CE, Morgan TE (1998) Age-related activation of microglia and astrocytes: in vitro studies show persistent phenotypes of aging, increased proliferation, and resistance to down-regulation. Neurobiol Aging 19: 97-103. (Pubitemid 28167802)
66. Sandhir R, Onyszchuk G, Berman NE (2008) Exacerbated glial response in the aged mouse hippocampus following controlled cortical impact injury. Exp Neurol 213: 372-380.
67. Campuzano O, Castillo-Ruiz MM, Acarin L, Castellano B, Gonzalez B (2009) Increased levels of proinflammatory cytokines in the aged rat brain attenuate injury-induced cytokine response after excitotoxic damage. J Neurosci Res 87: 2484-2497.
68. Casolini P, Catalani A, Zuena AR, Angelucci L (2002) Inhibition of COX-2 reduces the age-dependent increase of hippocampal inflammatory markers, corticosterone secretion, and behavioral impairments in the rat. J Neurosci Res 68: 337-343. (Pubitemid 34462539)
69. Krabbe KS, Pedersen M, Bruunsgaard H (2004) Inflammatory mediators in the elderly. Exp Gerontol 39: 687-699. (Pubitemid 38586809)
70. Vasto S, Candore G, Balistreri CR, Caruso M, Colonna-Romano G, et al. (2007) Inflammatory networks in ageing, age-related diseases and longevity. Mech Ageing Dev 128: 83-91. (Pubitemid 46073064)
71. Stirling DP, Koochesfahani KM, Steeves JD, Tetzlaff W (2005) Minocycline as a neuroprotective agent. Neuroscientist 11: 308-322. (Pubitemid 41040860)
72. Dyball REJ (1988) The importance of bursting in determining secretory response: how does a phasic firing pattern influence peptide release from neurohypophysial vasopressin terminals. in Pulsatility in neuroendocrine systems. ed Leng G (CRC, Boca Raton, FL): 181-196.
73. Hussy N, Deleuze C, Desarmenien MG, Moos FC (2000) Osmotic regulation of neuronal activity: a new role for taurine and glial cells in a hypothalamic neuroendocrine structure. Prog Neurobiol 62: 113-134. (Pubitemid 30316442)
74. Ma XY, Li HX, Ho SY (1995) [Vasopressin facilitates aortic baroreceptor activity in the rat]. Sheng Li Xue Bao 47: 394-400.