Visceral adipose tissue inflammation is associated with age-related brain changes and ischemic brain damage in aged mice

Brain, Behavior, and Immunity

Volumn 50, Issue , 2015, Pages 221-231

  Shin, Jin A ^a   Jeong, Sae Im ^a   Kim, Minsuk ^a   Yoon, Joo Chun ^a   Kim, Hee Sun ^a   Park, Eun Mi ^a  

^a Ewha Womans University School of Medicine   (South Korea)

Author keywords

Adipose tissue inflammation; Aging; Blood brain barrier; Ischemic stroke; Macrophage; Microglia; Proinflammatory cytokine; Tight junction protein; Visceral fat removal

Indexed keywords

INTERLEUKIN 1BETA; INTERLEUKIN 6; TIGHT JUNCTION PROTEIN; TUMOR NECROSIS FACTOR ALPHA; AUTACOID; CYTOKINE;

ABDOMINAL OBESITY; ADULT; AGED; AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BRAIN DAMAGE; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; CONTROLLED STUDY; CYTOKINE RESPONSE; INTRAABDOMINAL FAT; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SOFT TISSUE INFLAMMATION; UPREGULATION; ANIMAL; C57BL MOUSE; COMPLICATION; INFLAMMATION; METABOLISM;

AGING; ANIMALS; BLOOD-BRAIN BARRIER; BRAIN ISCHEMIA; CYTOKINES; INFLAMMATION; INFLAMMATION MEDIATORS; INTERLEUKIN-1BETA; INTERLEUKIN-6; INTRA-ABDOMINAL FAT; MALE; MICE; MICE, INBRED C57BL; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84937239111     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2015.07.008     Document Type: Article

References (55)

1. Allen C.L., Bayraktutan U. Risk factors for ischaemic stroke. Int. J. Stroke 2008, 3:105-116.
2. Asdaghi N., Butcher K.S., Hill M.D. Risks and benefits of thrombolysis in the elderly. Int. J. Stroke 2012, 7:142-149.
3. Austad S. Recent advances in vertebrate aging research 2009. Aging Cell 2010, 9:297-303.
4. Badan I., Buchhold B., Hamm A., Gratz M., Walker L.C., Platt D., Kessler C., Popa-Wagner A. Accelerated glial reactivity to stroke in aged rats correlates with reduced functional recovery. J. Cereb. Blood Flow Metab. 2003, 23:845-854.
5. Banks W.A., Moinuddin A., Morley J.E. Regional transport of TNF-alpha across the blood-brain barrier in young ICR and young and aged SAMP8 mice. Neurobiol. Aging 2001, 22:671-676.
6. Beaufrere B., Morio B. Fat and protein redistribution with aging: metabolic considerations. Eur. J. Clin. Nutr. 2000, 54(Suppl 3):S48-S53.
7. Borst S.E., Conover C.F., Bagby G.J. Association of resistin with visceral fat and muscle insulin resistance. Cytokine 2005, 32:39-44.
8. Buckman L.B., Hasty A.H., Flaherty D.K., Buckman C.T., Thompson M.M., Matlock B.K., Weller K., Ellacott K.L. Obesity induced by a high-fat diet is associated with increased immune cell entry into the central nervous system. Brain Behav. Immun. 2014, 35:33-42.
9. Cevenini E., Caruso C., Candore G., Capri M., Nuzzo D., Duro G., Rizzo C., Colonna-Romano G., Lio D., Di Carlo D., Palmas M.G., Scurti M., Pini E., Franceschi C., Vasto S. Age-related inflammation: the contribution of different organs, tissues and systems. How to face it for therapeutic approaches. Curr. Pharm. Des. 2010, 16:609-618.
10. Coisne C., Engelhardt B. Tight junctions in brain barriers during central nervous system inflammation. Antioxid. Redox Signal. 2011, 15:1285-1303.
11. Corsonello A., Pedone C., Incalzi R.A. Age-related pharmacokinetic and pharmacodynamic changes and related risk of adverse drug reactions. Curr. Med. Chem. 2010, 17:571-584.
12. Debette S., Beiser A., Hoffmann U., Decarli C., O'Donnell C.J., Massaro J.M., Au R., Himali J.J., Wolf P.A., Fox C.S., Seshadri S. Visceral fat is associated with lower brain volume in healthy middle-aged adults. Ann. Neurol. 2010, 68:136-144.
13. Dhungana H., Malm T., Denes A., Valonen P., Wojciechowski S., Magga J., Savchenko E., Humphreys N., Grencis R., Rothwell N., Koistinaho J. Aging aggravates ischemic stroke-induced brain damage in mice with chronic peripheral infection. Aging Cell 2013, 12:842-850.
14. Dubrovsky Y.V., Samsa W.E., Kondratov R.V. Deficiency of circadian protein CLOCK reduces lifespan and increases age-related cataract development in mice. Aging (Albany NY) 2010, 2:936-944.
15. Fisher M., Feuerstein G., Howells D.W., Hurn P.D., Kent T.A., Savitz S.I., Lo E.H. Update of the stroke therapy academic industry roundtable preclinical recommendations. Stroke 2009, 40:2244-2250.
16. Gabriely I., Ma X.H., Yang X.M., Atzmon G., Rajala M.W., Berg A.H., Scherer P., Rossetti L., Barzilai N. Removal of visceral fat prevents insulin resistance and glucose intolerance of aging: an adipokine-mediated process?. Diabetes 2002, 51:2951-2958.
17. Harman-Boehm I., Bluher M., Redel H., Sion-Vardy N., Ovadia S., Avinoach E., Shai I., Kloting N., Stumvoll M., Bashan N., Rudich A. Macrophage infiltration into omental versus subcutaneous fat across different populations: effect of regional adiposity and the comorbidities of obesity. J. Clin. Endocrinol. Metab. 2007, 92:2240-2247.
18. Hart A.D., Wyttenbach A., Perry V.H., Teeling J.L. Age related changes in microglial phenotype vary between CNS regions: grey versus white matter differences. Brain Behav. Immun. 2012, 26:754-765.
19. Huffman D.M., Barzilai N. Role of visceral adipose tissue in aging. Biochim. Biophys. Acta 2009, 1790:1117-1123.
20. Ibrahim M.M. Subcutaneous and visceral adipose tissue: structural and functional differences. Obes. Rev. 2010, 11:11-18.
21. Isaac V., Sim S., Zheng H., Zagorodnov V., Tai E.S., Chee M. Adverse associations between visceral adiposity, brain structure, and cognitive performance in healthy elderly. Front. Aging Neurosci. 2011, 3:12.
22. Karcher H.S., Holzwarth R., Mueller H.P., Ludolph A.C., Huber R., Kassubek J., Pinkhardt E.H. Body fat distribution as a risk factor for cerebrovascular disease: an MRI-based body fat quantification study. Cerebrovasc. Dis. 2013, 35:341-348.
23. Knoflach M., Matosevic B., Rucker M., Furtner M., Mair A., Wille G., Zangerle A., Werner P., Ferrari J., Schmidauer C., Seyfang L., Kiechl S., Willeit J., Austrian Stroke Unit Registry C. Functional recovery after ischemic stroke - a matter of age: data from the Austrian Stroke Unit Registry. Neurology 2012, 78:279-285.
24. Koenig S., Luheshi G.N., Wenz T., Gerstberger R., Roth J., Rummel C. Leptin is involved in age-dependent changes in response to systemic inflammation in the rat. Brain Behav. Immun. 2014, 36:128-138.
25. Liu F., Yuan R., Benashski S.E., McCullough L.D. Changes in experimental stroke outcome across the life span. J. Cereb. Blood Flow Metab. 2009, 29:792-802.
26. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25:402-408.
27. Lonnqvist F., Thome A., Nilsell K., Hoffstedt J., Arner P. A pathogenic role of visceral fat beta 3-adrenoceptors in obesity. J. Clin. Invest. 1995, 95:1109-1116.
28. Manwani B., Liu F., Xu Y., Persky R., Li J., McCullough L.D. Functional recovery in aging mice after experimental stroke. Brain Behav. Immun. 2011, 25:1689-1700.
29. Manwani B., Liu F., Scranton V., Hammond M.D., Sansing L.H., McCullough L.D. Differential effects of aging and sex on stroke induced inflammation across the lifespan. Exp. Neurol. 2013, 249:120-131.
30. Matsumoto M., Ishikawa S., Kajii E. Association of adiponectin with cerebrovascular disease: a nested case-control study. Stroke 2008, 39:323-328.
31. Michaud A., Drolet R., Noel S., Paris G., Tchernof A. Visceral fat accumulation is an indicator of adipose tissue macrophage infiltration in women. Metabolism 2012, 61:689-698.
32. Murano I., Barbatelli G., Parisani V., Latini C., Muzzonigro G., Castellucci M., Cinti S. Dead adipocytes, detected as crown-like structures, are prevalent in visceral fat depots of genetically obese mice. J. Lipid Res. 2008, 49:1562-1568.
33. Naess H., Gjerde G., Waje-Andreassen U. Ischemic stroke in patients older and younger than 80 years. Acta Neurol. Scand. 2014, 129:399-404.
34. Nagura J., Nakagawa Y., Miyanaga M., Matsuoka K., Hayashi K., Ozasa K., Watanabe Y. Relationship between abdominal visceral fat and lacunar infarcts in Japanese men. Circ. J. 2004, 68:982-987.
35. Norden D.M., Godbout J.P. Review: microglia of the aged brain: primed to be activated and resistant to regulation. Neuropathol. Appl. Neurobiol. 2013, 39:19-34.
36. Olefsky J.M., Glass C.K. Macrophages, inflammation, and insulin resistance. Annu. Rev. Physiol. 2010, 72:219-246.
37. Park J.S., Shin J.A., Jung J.S., Hyun J.W., Van Le T.K., Kim D.H., Park E.M., Kim H.S. Anti-inflammatory mechanism of compound K in activated microglia and its neuroprotective effect on experimental stroke in mice. J. Pharmacol. Exp. Ther. 2012, 341:59-67.
38. Pistell P.J., Morrison C.D., Gupta S., Knight A.G., Keller J.N., Ingram D.K., Bruce-Keller A.J. Cognitive impairment following high fat diet consumption is associated with brain inflammation. J. Neuroimmunol. 2010, 219:25-32.
39. Pitombo C., Araujo E.P., De Souza C.T., Pareja J.C., Geloneze B., Velloso L.A. Amelioration of diet-induced diabetes mellitus by removal of visceral fat. J. Endocrinol. 2006, 191:699-706.
40. Popa-Wagner A., Badan I., Walker L., Groppa S., Patrana N., Kessler C. Accelerated infarct development, cytogenesis and apoptosis following transient cerebral ischemia in aged rats. Acta Neuropathol. 2007, 113:277-293.
41. Popescu B.O., Toescu E.C., Popescu L.M., Bajenaru O., Muresanu D.F., Schultzberg M., Bogdanovic N. Blood-brain barrier alterations in ageing and dementia. J. Neurol. Sci. 2009, 283:99-106.
42. Reed M.J., Karres N., Eyman D., Cruz A., Brekken R.A., Plymate S. The effects of aging on tumor growth and angiogenesis are tumor-cell dependent. Int. J. Cancer 2007, 120:753-760.
43. Salvioli S., Capri M., Valensin S., Tieri P., Monti D., Ottaviani E., Franceschi C. Inflamm-aging, cytokines and aging: state of the art, new hypotheses on the role of mitochondria and new perspectives from systems biology. Curr. Pharm. Des. 2006, 12:3161-3171.
44. Shi H., Sheng B., Zhang F., Wu C., Zhang R., Zhu J., Xu K., Kuang Y., Jameson S.C., Lin Z., Wang Y., Chen J., Jain M.K., Atkins G.B. Kruppel-like factor 2 protects against ischemic stroke by regulating endothelial blood brain barrier function. Am. J. Physiol. Heart Circ. Physiol. 2013, 304:H796-H805.
45. Shin J.A., Yang S.J., Jeong S.I., Park H.J., Choi Y.H., Park E.M. Activation of estrogen receptor beta reduces blood-brain barrier breakdown following ischemic injury. Neuroscience 2013, 235:165-173.
46. Shin J.A., Kim Y.A., Jeong S.I., Lee K.E., Kim H.S., Park E.M. Extracellular signal-regulated kinase1/2-dependent changes in tight junctions after ischemic preconditioning contributes to tolerance induction after ischemic stroke. Brain Struct. Funct. 2015, 220:13-26.
47. Skurk T., Alberti-Huber C., Herder C., Hauner H. Relationship between adipocyte size and adipokine expression and secretion. J. Clin. Endocrinol. Metab. 2007, 92:1023-1033.
48. Soderberg S., Stegmayr B., Ahlbeck-Glader C., Slunga-Birgander L., Ahren B., Olsson T. High leptin levels are associated with stroke. Cerebrovasc. Dis. 2003, 15:63-69.
49. Tan J.T., McLennan S.V., Williams P.F., Rezaeizadeh A., Lo L.W., Bonner J.G., Twigg S.M. Connective tissue growth factor/CCN-2 is upregulated in epididymal and subcutaneous fat depots in a dietary-induced obesity model. Am. J. Physiol. Endocrinol. Metab. 2013, 304:E1291-E1302.
50. Tchernof A., Despres J.P. Pathophysiology of human visceral obesity: an update. Physiol. Rev. 2013, 93:359-404.
51. Tucsek Z., Toth P., Sosnowska D., Gautam T., Mitschelen M., Koller A., Szalai G., Sonntag W.E., Ungvari Z., Csiszar A. Obesity in aging exacerbates blood-brain barrier disruption, neuroinflammation, and oxidative stress in the mouse hippocampus: effects on expression of genes involved in Beta-amyloid generation and Alzheimer's disease. J. Gerontol. A Biol. Sci. Med. Sci. 2014, 69:1212-1226.
52. Wang Y.Y., Lin S.Y., Chuang Y.H., Chen C.J., Tung K.C., Sheu W.H. Adipose proinflammatory cytokine expression through sympathetic system is associated with hyperglycemia and insulin resistance in a rat ischemic stroke model. Am. J. Physiol. Endocrinol. Metab. 2011, 300:E155-E163.
53. 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.
54. Yamashiro K., Tanaka R., Tanaka Y., Miyamoto N., Shimada Y., Ueno Y., Urabe T., Hattori N. Visceral fat accumulation is associated with cerebral small vessel disease. Eur. J. Neurol. 2014, 21:667-673.
55. Zhang X., Dong F., Ren J., Driscoll M.J., Culver B. High dietary fat induces NADPH oxidase-associated oxidative stress and inflammation in rat cerebral cortex. Exp. Neurol. 2005, 191:318-325.