Thirst deficits in aged rats are reversed by dietary omega-3 fatty acid supplementation

Neurobiology of Aging

Volumn 33, Issue 10, 2012, Pages 2422-2430

  Begg, Denovan P ^a,b   Sinclair, Andrew J ^b   Weisinger, Richard S ^a  

^a LA TROBE UNIVERSITY   (Australia)

^b DEAKIN UNIVERSITY   (Australia)

Author keywords

Aging; Arachidonic acid; Cyclooxygenase; Dehydration; Docosahexaenoic acid; Fluid intake; Omega 3 polyunsaturated fatty acids; Prostaglandin E; Thirst

Indexed keywords

ANGIOTENSIN II; ARGIPRESSIN; ATRIAL NATRIURETIC FACTOR; CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; CYTOSOLIC PHOSPHOLIPASE A2; HYPERTONIC SOLUTION; MESSENGER RNA; OMEGA 3 FATTY ACID; PROSTAGLANDIN E SYNTHASE; PROSTAGLANDIN E2; PROSTANOID;

AGED; AGING; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTONOMIC NEUROPATHY; BODY WEIGHT; BRAIN LEVEL; CONTROLLED STUDY; CYTOSOLIC PHOSPHOLIPASE A2 GENE; DEHYDRATION; DIET SUPPLEMENTATION; DRINKING BEHAVIOR; FATTY ACID SYNTHESIS; GENE; GENE EXPRESSION REGULATION; HYPEROSMOTIC STRESS; HYPOTHALAMUS; MALE; METABOLITE; NONHUMAN; PRIORITY JOURNAL; PROSTAGLANDIN E SYNTHASE GENE; PROTEIN BLOOD LEVEL; RAT; THERAPY EFFECT; THIRST DEFICIT;

AGE FACTORS; ANGIOTENSIN II; ANIMALS; ARGININE VASOPRESSIN; ATRIAL NATRIURETIC FACTOR; CYCLOOXYGENASE 2; DEHYDRATION; DIETARY SUPPLEMENTS; DINOPROSTONE; DRINKING; FATTY ACIDS, OMEGA-3; HYPOTHALAMUS; INTRAMOLECULAR OXIDOREDUCTASES; MALE; PHOSPHOLIPASES A2, CYTOSOLIC; RATS; SALINE SOLUTION, HYPERTONIC; THIRST;

EID: 84864384268     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2011.12.001     Document Type: Article

References (56)

1. Aïd S., Bosetti F. Gene expression of cyclooxygenase-1 and Ca(2+)-independent phospholipase A(2) is altered in rat hippocampus during normal aging. Brain Res. Bull 2007, 73:108-113.
2. Attar-Bashi N.M., Weisinger R.S., Begg D.P., Li D., Sinclair A.J. Failure of conjugated linoleic acid supplementation to enhance biosynthesis of docosahexaenoic acid from alpha-linolenic acid in healthy human volunteers. Prostaglandins Leukot. Essent. Fatty Acids 2007, 76:121-130.
3. Baylis C., Corman B. The aging kidney: insights from experimental studies. J. Am. Soc. Nephrol 1998, 9:699-709.
4. Begg D.P., Sinclair A.J., Stahl L.A., Garg M.L., Jois M., Weisinger R.S. Dietary protein level interacts with omega-3 polyunsaturated fatty acid deficiency to induce hypertension. Am. J. Hypertens 2010, 23:125-128.
5. Begg D.P., Sinclair A.J., Stahl L.A., Premaratna S.D., Hafandi A., Jois M., Weisinger R.S. Hypertension induced by omega-3 polyunsaturated fatty acid deficiency is alleviated by a-linolenic acid regardless of dietary source. Hypertens. Res 2010, 33:808-813.
6. Begg D.P., Weisinger R.S. The role of adrenal or testicular hormones in voluntary ethanol and NaCl intake of crowded and individually housed rats. Physiol. Behav 2008, 93:408-413.
7. Bengele H.H., Mathias R.S., Perkins J.H., Alexander E.A. Urinary concentrating defect in the aged rat. Am. J. Physiol. Ren. Physiol 1981, 240:F147-F150.
8. Chun A.L., Wallace L.J., Gerald M.C., Levin R.M., Wein A.J. Effect of age on in vivo urinary bladder function in the rat. J. Urol 1988, 139:625-627.
9. Combet S., Teillet L., Geelen G., Pitrat B., Gobin R., Nielsen S., Trinh-Trang-Tan M.M., Corman B., Verbavatz J.M. Food restriction prevents age-related polyuria by vasopressin-dependent recruitment of aquaporin-2. Am. J. Physiol. Ren. Physiol 2001, 281:F1123-F1131.
10. Crowe M.J., Forsling M.L., Rolls B.J., Phillips P.A., Ledingham J.G., Smith R.F. Altered water excretion in healthy elderly men. Age Ageing 1987, 16:285-293.
11. January 2009 Heatwave in Victoria: an Assessment of Health Impacts 2009, D.H.S., In: Services, D.o.H. (Ed.), Victorian Government, Melbourne.
12. Davis K.M., Fish L.C., Minaker K.L., Elahi D. Atrial natriuretic peptide levels in the elderly: differentiating normal aging changes from disease. J. Gerontol. A Biol. Sci. Med. Sci 1996, 51:M95-M101.
13. Deloof S., De Seze C., Montel V., Chatelain A. Effects of water deprivation on atrial natriuretic peptide secretion and density of binding sites in adrenal glands and kidneys of maternal and fetal rats in late gestation. Eur. J. Endocrinol 1999, 141:160-168.
14. Donadio J.V., Bergstralh E.J., Offord K.P., Spencer D.C., Holley K.E. A controlled trial of fish oil in IgA nephropathy. Mayo Nephrology Collaborative Group. N Engl J. Med 1994, 331:1194-1199.
15. Ehrlich K.J., Fitts D.A. Atrial natriuretic peptide in the subfornical organ reduces drinking induced by angiotensin or in response to water deprivation. Behav. Neurosci 1990, 104:365-372.
16. Farrell M.J., Zamarripa F., Shade R., Phillips P.A., McKinley M., Fox P.T., Blair-West J., Denton D.A., Egan G.F. Effect of aging on regional cerebral blood flow responses associated with osmotic thirst and its satiation by water drinking: a PET study. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:382-387.
17. Focà A., Matera G., Mastroeni P., Caputi A.P. Evidence that prostaglandins within preoptic area (POA) may mediate the antidipsogenic effect of Escherichia coli endotoxin in the rat. Circ. Shock 1985, 17:137-145.
18. Goldstein D.J., Marante Perez D.J., Gunst J.P., Halperin J.A. Prostaglandins E1 inhibits acute cell dehydration thirst. Pharmacol. Biochem. Behav 1979, 10:895-898.
19. Grynszpan D. Lessons from the French heatwave. Lancet 2003, 362:1169-1170.
20. Hodgkinson B., Evans D., Wood J. Maintaining oral hydration in older adults: a systematic review. Int. J. Nurs. Pract 2003, 9:S19-S28.
21. Hrelia S., Bordoni A., Celadon M., Turchetto E., Biagi P.L., Rossi C.A. Age-related changes in linoleate and alpha-linolenate desaturation by rat liver microsomes. Biochem. Biophys. Res. Commun 1989, 163:348-355.
22. Jakobsson P.J., Thorén S., Morgenstern R., Samuelsson B. Identification of human prostaglandin E synthase: a microsomal, glutathione-dependent, inducible enzyme, constituting a potential novel drug target. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:7220-7225.
23. Jayasooriya A.P., Ackland M.L., Mathai M.L., Sinclair A.J., Weisinger H.S., Weisinger R.S., Halver J.E., Kitajka K., Puskás L.G. Perinatal omega-3 polyunsaturated fatty acid supply modifies brain zinc homeostasis during adulthood. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:7133-7138.
24. Jayasooriya A.P., Mathai M.L., Walker L.L., Begg D.P., Denton D.A., Cameron-Smith D., Egan G.F., McKinley M.J., Rodger P.D., Sinclair A.J., Wark J.D., Weisinger H.S., Jois M., Weisinger R.S. Mice lacking angiotensin-converting enzyme have increased energy expenditure, with reduced fat mass and improved glucose clearance. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:6531-6536.
25. Kaysen G.A., Myers B.D. The aging kidney. Clin. Geriatr. Med 1985, 1:207-222.
26. Kobayashi Y., Lederis K., Kawashima S. Neural lobe function in aged Wistar/Tw strain rats showing polydipsia and polyuria. Endocrinol. Jpn 1986, 33:617-627.
27. Kysely J., Kim J. Mortality during heat waves in South Korea, 1991-2005: How exceptional was the 1994 heat wave?. Clim. Res 2009, 38:105-116.
28. Ledingham J.G., Crowe M.J., Forsling M.L., Phillips P.A., Rolls B.J. Effects of aging on vasopressin secretion, water excretion, and thirst in man. Kidney Int. Suppl 1987, 21:S90-S92.
29. Mackenbach J.P., Borst V., Schols J.M. Heat-related mortality among nursing-home patients. Lancet 1997, 349:1297-1298.
30. McKinley M.J., Denton D.A., Thomas C.J., Woods R.L., Mathai M.L. Differential effects of aging on fluid intake in response to hypovolemia, hypertonicity, and hormonal stimuli in Munich Wistar rats. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:3450-3455.
31. McMichael A.J., Woodruff R.E., Hales S. Climate change and human health: present and future risks. Lancet 2006, 367:859-869.
32. Meydani M., Meydani S.N., Macauley J.B., Blumberg J.R. Influence of dietary vitamin E and selenium on the ex-vivo synthesis of prostaglandin E2 in brain regions of young and old rats. Prostaglandins Leukot. Med 1985, 18:337-346.
33. Nava F., Carta G. Repeated lipopolysaccharide administration produces tolerance to anorexia and fever but not to inhibition of thirst in rat. Int. J. Immunopharmacol 2000, 22:943-953.
34. O'Neill P.A., Duggan J., Davies I. Response to dehydration in elderly patients in long-term care. Aging (Milano) 1997, 9:372-377.
35. Palin K., Moreau M.L., Orcel H., Duvoid-Guillou A., Rabié A., Kelley K.W., Moos F. Age-impaired fluid homeostasis depends on the balance of IL-6/IGF-I in the rat supraoptic nuclei. Neurobiol. Aging 2009, 30:1677-1692.
36. Pérez Guaita M.F., Chiaraviglio E. Effect of prostaglandin E1 and its biosynthesis inhibitor indomethacin on drinking in the rat. Pharmacol. Biochem. Behav 1980, 13:787-792.
37. Phillips P.A., Bretherton M., Johnston C.I., Gray L. Reduced osmotic thirst in healthy elderly men. Am. J. Physiol 1991, 261:R166-R171.
38. Phillips P.A., Johnston C.I., Gray L. Disturbed fluid and electrolyte homoeostasis following dehydration in elderly people. Age Ageing 1993, 22:S26-S33.
39. Phillips P.A., Rolls B.J., Ledingham J.G., Forsling M.L., Morton J.J., Crowe M.J., Wollner L. Reduced thirst after water deprivation in healthy elderly men. N Engl J. Med 1984, 311:753-759.
40. Qiu D., Tanihata T., Aoyama H., Fujita T., Inaba Y., Minowa M. Relationship between a high mortality rate and extreme heat during the summer of 1999 in Hokkaido Prefecture, Japan. J. Epidemiol 2002, 12:254-257.
41. Rao J.S., Ertley R.N., DeMar J.C., Rapoport S.I., Bazinet R.P., Lee H.J. Dietary n-3 PUFA deprivation alters expression of enzymes of the arachidonic and docosahexaenoic acid cascades in rat frontal cortex. Mol. Psychiatry 2007, 12:151-157.
42. Rolls B.J., Phillips P.A. Aging and disturbances of thirst and fluid balance. Nutr. Rev 1990, 48:137-144.
43. Rowland N.E., Morien A., Garcea M., Fregly M.J. Aging and fluid homeostasis in rats. Am. J. Physiol 1997, 273:R1441-R1450.
44. Silver A.J., Flood J.F., Morley J.E. Effect of aging on fluid ingestion in mice. J. Gerontol 1991, 46:B117-B121.
45. Silver A.J., Morley J.E., Ishimaru-Tseng T.V., Morley P.M. Angiotensin II and fluid ingestion in old rats. Neurobiol. Aging 1993, 14:519-522.
46. Song C., Manku M.S., Horrobin D.F. Long-chain polyunsaturated fatty acids modulate interleukin-1beta-induced changes in behavior, monoaminergic neurotransmitters, and brain inflammation in rats. J. Nutr 2008, 138:954-963.
47. Tang E.H., Vanhoutte P.M. Gene expression changes of prostanoid synthases in endothelial cells and prostanoid receptors in vascular smooth muscle cells caused by aging and hypertension. Physiol. Genomics 2008, 32:409-418.
48. Thomas C.J., McAllen R.M., Salo L.M., Woods R.L. Restorative effect of atrial natriuretic peptide or chronic neutral endopeptidase inhibition on blunted cardiopulmonary vagal reflexes in aged rats. Hypertension 2008, 52:696-701.
49. Thunhorst R.L., Beltz T.G., Johnson A.K. Hypotension- and osmotically induced thirst in old Brown Norway rats. Am. J. Physiol. Regul. Integr. Comp. Physiol 2009, 297:R149-R157.
50. Thunhorst R.L., Johnson A.K. Thirst and salt appetite responses in young and old Brown Norway rats. Am. J. Physiol. Regul. Integr. Comp. Physiol 2003, 284:R317-R327.
51. Touqui L., Rothhut B., Shaw A.M., Fradin A., Vargaftig B.B., Russo-Marie F. Platelet activation-a role for a 40K anti-phospholipase A2 protein indistinguishable from lipocortin. Nature 1986, 321:177-180.
52. Weisinger R.S., Armitage J.A., Chen N., Begg D.P., Mathai M.L., Jayasooriya A.P., Sinclair A.J., Weisinger H.S. Sodium appetite in adult rats following ω-3 polyunsaturated fatty acid deficiency in early development. Appetite 2010, 55:393-397.
53. Weisinger R.S., Blair-West J.R., Denton D.A., Tarjan E. Central administration of atrial natriuretic peptide suppresses sodium and water intake of sheep. Brain Res 1992, 579:113-118.
54. Whitman S., Good G., Donoghue E.R., Benbow N., Shou W., Mou S. Mortality in Chicago attributed to the July 1995 heat wave. Am. J. Public Health 1997, 87:1515-1518.
55. Whyte D.G., Thunhorst R.L., Johnson A.K. Reduced thirst in old, thermally dehydrated rats. Physiol. Behav 2004, 81:569-576.
56. Wu S.Q., Kwan C.Y., Tang F. The effect of aging on ANP levels in the plasma, heart, and brain of rats. J. Gerontol. A Biol. Sci. Med. Sci 1997, 52:B250-B254.