Leptin is involved in age-dependent changes in response to systemic inflammation in the rat

Brain, Behavior, and Immunity

Volumn 36, Issue , 2014, Pages 128-138

  Koenig, Sandy ^a   Luheshi, Giamal N ^b   Wenz, Tina ^c   Gerstberger, Rüdiger ^a   Roth, Joachim ^a   Rummel, Christoph ^a  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

^b DOUGLAS MENTAL HEALTH UNIVERSITY INSTITUTE   (Canada)

^c UNIVERSITY OF COLOGNE   (Germany)

Author keywords

Aging; Cytokines; Fever; Inflammatory transcription factors; Leptin; Lipopolysaccharide; MicroRNA; Microsomal prostaglandin E synthase; Obesity; White adipose tissue

Indexed keywords

CYCLOOXYGENASE 2; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 6; LEPTIN; LIPOPOLYSACCHARIDE; PROSTAGLANDIN SYNTHASE; SODIUM CHLORIDE; TUMOR NECROSIS FACTOR ALPHA;

ADIPOSE TISSUE; ADIPSIA; AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANOREXIA; ARTICLE; CONTROLLED STUDY; CORE TEMPERATURE; CYTOKINE RELEASE; DISEASES; ENZYME LINKED IMMUNOSORBENT ASSAY; EX VIVO STUDY; FEVER; INFLAMMATION; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TELEMETRY; WEIGHT REDUCTION; WHITE ADIPOSE TISSUE;

ADIPOSE TISSUE; AGING; ANIMALS; CYCLOOXYGENASE 2; CYTOKINES; HYPOTHALAMUS; INFLAMMATION; LEPTIN; LIPOPOLYSACCHARIDES; LIVER; MALE; MICRORNAS; OXIDATIVE STRESS; RATS; RATS, WISTAR;

EID: 84891825307     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2013.10.019     Document Type: Article

References (56)

1. Alvarez-Rodriguez L., Lopez-Hoyos M., Munoz-Cacho P., Martinez-Taboada V.M. Aging is associated with circulating cytokine dysregulation. Cell. Immunol. 2012, 273:124-132.
2. Barrientos R.M., Watkins L.R., Rudy J.W., Maier S.F. Characterization of the sickness response in young and aging rats following E. coli infection. Brain Behav. Immun. 2009, 23:450-454.
3. Baumgartner R.N., Waters D.L., Morley J.E., Patrick P., Montoya G.D., Garry P.J. Age-related changes in sex hormones affect the sex difference in serum leptin independently of changes in body fat. Metabolism 1999, 48:378-384.
4. Bhaumik D., Scott G.K., Schokrpur S., Patil C.K., Orjalo A.V., Rodier F., Lithgow G.J., Campisi J. MicroRNAs miR-146a/b negatively modulate the senescence-associated inflammatory mediators IL-6 and IL-8. Aging (Albany NY) 2009, 1:402-411.
5. Bruunsgaard H., Andersen-Ranberg K., Jeune B., Pedersen A.N., Skinhoj P., Pedersen B.K. A high plasma concentration of TNF-alpha is associated with dementia in centenarians. J. Gerontol. A Biol. Sci. Med. Sci. 1999, 54:M357-364.
6. Bruunsgaard H., Pedersen M., Pedersen B.K. Aging and proinflammatory cytokines. Curr. Opin. Hematol. 2001, 8:131-136.
7. Buchanan J.B., Peloso E., Satinoff E. Thermoregulatory and metabolic changes during fever in young and old rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2003, 285:R1165-1169.
8. Carrascosa J.M., Ros M., Andres A., Fernandez-Agullo T., Arribas C. Changes in the neuroendocrine control of energy homeostasis by adiposity signals during aging. Exp. Gerontol. 2009, 44:20-25.
9. Chung H.Y., Lee E.K., Choi Y.J., Kim J.M., Kim D.H., Zou Y., Kim C.H., Lee J., Kim H.S., Kim N.D., Jung J.H., Yu B.P. Molecular inflammation as an underlying mechanism of the aging process and age-related diseases. J. Dent. Res. 2011, 90:830-840.
10. Damm J., Luheshi G.N., Gerstberger R., Roth J., Rummel C. Spatiotemporal nuclear factor interleukin-6 expression in the rat brain during lipopolysaccharide-induced fever is linked to sustained hypothalamic inflammatory target gene induction. J. Comp. Neurol. 2011, 519:480-505.
11. Damm J., Harden L.M., Gerstberger R., Roth J., Rummel C. The putative JAK-STAT inhibitor AG490 exacerbates LPS-fever, reduces sickness behavior, and alters the expression of pro- and anti-inflammatory genes in the rat brain. Neuropharmacology 2013, 71:98-111.
12. Dantzer R., O'Connor J.C., Freund G.G., Johnson R.W., Kelley K.W. From inflammation to sickness and depression: when the immune system subjugates the brain. Nat. Rev. Neurosci. 2008, 9:46-56.
13. Fantuzzi G., Faggioni R. Leptin in the regulation of immunity, inflammation, and hematopoiesis. J. Leukoc. Biol. 2000, 68:437-446.
14. Ferrucci L., Corsi A., Lauretani F., Bandinelli S., Bartali B., Taub D.D., Guralnik J.M., Longo D.L. The origins of age-related proinflammatory state. Blood 2005, 105:2294-2299.
15. Foster K.D., Conn C.A., Kluger M.J. Fever, tumor necrosis factor, and interleukin-6 in young, mature, and aged Fischer 344 rats. Am. J. Physiol. 1992, 262:R211-215.
16. Gabriely I., Ma X.H., Yang X.M., Rossetti L., Barzilai N. Leptin resistance during aging is independent of fat mass. Diabetes 2002, 51:1016-1021.
17. Godbout J.P., Johnson R.W. Age and neuroinflammation: a lifetime of psychoneuroimmune consequences. Immunol. Allergy Clin. North Am. 2009, 29:321-337.
18. Godbout J.P., Chen J., Abraham J., Richwine A.F., Berg B.M., Kelley K.W., Johnson R.W. Exaggerated neuroinflammation and sickness behavior in aged mice following activation of the peripheral innate immune system. FASEB J. 2005, 19:1329-1331.
19. Gupta S., Agrawal S., Gollapudi S. Increased activation and cytokine secretion in B cells stimulated with leptin in aged humans. Immun. Ageing 2013, 10:3.
20. Halaas J.L., Gajiwala K.S., Maffei M., Cohen S.L., Chait B.T., Rabinowitz D., Lallone R.L., Burley S.K., Friedman J.M. Weight-reducing effects of the plasma protein encoded by the obese gene. Science 1995, 269:543-546.
21. Harden L.M., du Plessis I., Poole S., Laburn H.P. Interleukin-6 and leptin mediate lipopolysaccharide-induced fever and sickness behavior. Physiol. Behav. 2006, 89:146-155.
22. Huang Y., Henry C.J., Dantzer R., Johnson R.W., Godbout J.P. Exaggerated sickness behavior and brain proinflammatory cytokine expression in aged mice in response to intracerebroventricular lipopolysaccharide. Neurobiol. Aging 2008, 29:1744-1753.
23. Inoue W., Poole S., Bristow A.F., Luheshi G.N. Leptin induces cyclooxygenase-2 via an interaction with interleukin-1beta in the rat brain. Eur. J. Neurosci. 2006, 24:2233-2245.
24. Isidori A.M., Strollo F., More M., Caprio M., Aversa A., Moretti C., Frajese G., Riondino G., Fabbri A. Leptin and aging: correlation with endocrine changes in male and female healthy adult populations of different body weights. J. Clin. Endocrinol. Metab. 2000, 85:1954-1962.
25. Jiang M., Xiang Y., Wang D., Gao J., Liu D., Liu Y., Liu S., Zheng D. Dysregulated expression of miR-146a contributes to age-related dysfunction of macrophages. Aging Cell 2012, 11:29-40.
26. Kozak W., Kozak A. Genetic models in applied physiology. Differential role of nitric oxide synthase isoforms in fever of different etiologies: studies using Nos gene-deficient mice. J. Appl. Physiol. 2003, 94:2534-2544.
27. Laflamme N., Rivest S. Effects of systemic immunogenic insults and circulating proinflammatory cytokines on the transcription of the inhibitory factor kappaB alpha within specific cellular populations of the rat brain. J. Neurochem. 1999, 73:309-321.
28. Laupland K.B., Church D.L., Mucenski M., Sutherland L.R., Davies H.D. Population-based study of the epidemiology of and the risk factors for invasive Staphylococcus aureus infections. J. Infect. Dis. 2003, 187:1452-1459.
29. Lebel E., Vallieres 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 2000, 141:3749-3763.
30. Lezza A.M., Pesce V., Cormio A., Fracasso F., Vecchiet J., Felzani G., Cantatore P., Gadaleta M.N. Increased expression of mitochondrial transcription factor A and nuclear respiratory factor-1 in skeletal muscle from aged human subjects. FEBS Lett. 2001, 501:74-78.
31. Luheshi G.N., Gardner J.D., Rushforth D.A., Loudon A.S., Rothwell N.J. Leptin actions on food intake and body temperature are mediated by IL-1. Proc. Natl. Acad. Sci. USA 1999, 96:7047-7052.
32. Maury E., Brichard S.M. Adipokine dysregulation, adipose tissue inflammation and metabolic syndrome. Mol. Cell. Endocrinol. 2010, 314:1-16.
33. Nadjar A., Bluthe R.M., May M.J., Dantzer R., Parnet P. Inactivation of the cerebral NFkappaB pathway inhibits interleukin-1beta-induced sickness behavior and c-Fos expression in various brain nuclei. Neuropsychopharmacology 2005, 30:1492-1499.
34. Peralta S., Carrascosa J.M., Gallardo N., Ros M., Arribas C. Ageing increases SOCS-3 expression in rat hypothalamus: effects of food restriction. Biochem. Biophys. Res. Commun. 2002, 296:425-428.
35. Picca A., Fracasso F., Pesce V., Cantatore P., Joseph A.M., Leeuwenburgh C., Gadaleta M.N., Lezza A.M. Age- and calorie restriction-related changes in rat brain mitochondrial DNA and TFAM binding. Age (Dordr) 2013, 35:1607-1620.
36. Pohl J., Woodside B., Luheshi G.N. Changes in hypothalamically mediated acute-phase inflammatory responses to lipopolysaccharide in diet-induced obese rats. Endocrinology 2009, 150:4901-4910.
37. Quinn S.R., O'Neill L.A. A trio of microRNAs that control Toll-like receptor signalling. Int. Immunol. 2011, 23:421-425.
38. Romanovsky A.A., Ivanov A.I., Shimansky Y.P. Selected contribution: ambient temperature for experiments in rats: a new method for determining the zone of thermal neutrality. J. Appl. Physiol. 2002, 92:2667-2679.
39. Roth J., Rummel C., Barth S.W., Gerstberger R., Hübschle T. Molecular aspects of fever and hyperthermia. Immunol. Allergy Clin. North Am. 2009, 29:229-245.
40. Rummel C., Sachot C., Poole S., Luheshi G.N. Circulating interleukin-6 induces fever through a STAT3-linked activation of COX-2 in the brain. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2006, 291:R1316-R1326.
41. Rummel C., Gerstberger R., Roth J., Hubschle T. Parthenolide attenuates LPS-induced fever, circulating cytokines and markers of brain inflammation in rats. Cytokine 2011, 56:739-748.
42. Rummel C., Matsumura K., Luheshi G.N. Circulating IL-6 contributes to peripheral LPS-induced mPGES-1 expression in the rat brain. Brain Res. Bull. 2011, 86:319-325.
43. Sachot C., Poole S., Luheshi G.N. Circulating leptin mediates lipopolysaccharide-induced anorexia and fever in rats. J. Physiol. 2004, 561:263-272.
44. Sandhir R., Berman N.E. Age-dependent response of CCAAT/enhancer binding proteins following traumatic brain injury in mice. Neurochem. Int. 2010, 56:188-193.
45. Scarpace P.J., Tumer N. Peripheral and hypothalamic leptin resistance with age-related obesity. Physiol. Behav. 2001, 74:721-727.
46. Scarpace P.J., Borst S.E., Bender B.S. The association of E. coli peritonitis with an impaired and delayed fever response in senescent rats. J. Gerontol. 1992, 47:B142-145.
47. Scarpace P.J., Matheny M., Moore R.L., Tumer N. Impaired leptin responsiveness in aged rats. Diabetes 2000, 49:431-435.
48. Schautz B., Later W., Heller M., Peters A., Muller M.J., Bosy-Westphal A. Impact of age on leptin and adiponectin independent of adiposity. Br. J. Nutr. 2012, 108:363-370.
49. Sonkoly E., Stahle M., Pivarcsi A. MicroRNAs and immunity: novel players in the regulation of normal immune function and inflammation. Semin. Cancer Biol. 2008, 18:131-140.
50. Suliman H.B., Carraway M.S., Welty-Wolf K.E., Whorton A.R., Piantadosi C.A. Lipopolysaccharide stimulates mitochondrial biogenesis via activation of nuclear respiratory factor-1. J. Biol. Chem. 2003, 278:41510-41518.
51. Suliman H.B., Welty-Wolf K.E., Carraway M., Tatro L., Piantadosi C.A. Lipopolysaccharide induces oxidative cardiac mitochondrial damage and biogenesis. Cardiovasc. Res. 2004, 64:279-288.
52. Taganov K.D., Boldin M.P., Chang K.J., Baltimore D. NF-kappaB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses. Proc. Natl. Acad. Sci. USA 2006, 103:12481-12486.
53. Trayhurn P., Wood I.S. Signalling role of adipose tissue: adipokines and inflammation in obesity. Biochem. Soc. Trans. 2005, 33:1078-1081.
54. Wei J., Xu H., Davies J.L., Hemmings G.P. Increase of plasma IL-6 concentration with age in healthy subjects. Life Sci. 1992, 51:1953-1956.
55. Welsch J., Hubschle T., Murgott J., Kirschning C., Rummel C., Gerstberger R., Roth J. Fever induction by systemic stimulation with macrophage-activating lipopeptide-2 depends upon TLR2 but not CD36. Innate Immun. 2012, 18:541-559.
56. Wu D., Ren Z., Pae M., Guo W., Cui X., Merrill A.H., Meydani S.N. Aging up-regulates expression of inflammatory mediators in mouse adipose tissue. J. Immunol. 2007, 179:4829-4839.