Adipokines: A link between obesity and dementia?

The Lancet Neurology

Volumn 13, Issue 9, 2014, Pages 913-923

  Kiliaan, Amanda J ^a   Arnoldussen, Ilse A C ^a   Gustafson, Deborah R ^b,c,d  

^a RADBOUD UNIVERSITY   (Netherlands)

^b STATE UNIVERSITY OF NEW YORK   (United States)

^c UNIVERSITY OF GOTHENBURG   (Sweden)

^d UMS 011   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPOCYTOKINE; ADIPONECTIN; COMPLEMENT FACTOR D; LEPTIN; NERVE GROWTH FACTOR; PLASMINOGEN ACTIVATOR INHIBITOR 1; SCATTER FACTOR;

ADIPOSE TISSUE; BLOOD BRAIN BARRIER; BODY MASS; COGNITIVE DEFECT; DEMENTIA; DISEASE ASSOCIATION; ENDOCRINE FUNCTION; ENERGY BALANCE; ENERGY METABOLISM; HUMAN; HYPERTENSION; INFLAMMATION; NERVE DEGENERATION; OBESITY; PRIORITY JOURNAL; REVIEW; THROMBOSIS; ALZHEIMER DISEASE; BRAIN ATROPHY; BRAIN SIZE; NONHUMAN; WAIST CIRCUMFERENCE; WHITE MATTER; METABOLISM;

ADIPOKINES; DEMENTIA; HUMANS; OBESITY;

EID: 84906077008     PISSN: 14744422     EISSN: 14744465     Source Type: Journal    
DOI: 10.1016/S1474-4422(14)70085-7     Document Type: Review

References (146)

1. Gustafson D, Rothenberg E, Blennow K, Steen B, Skoog I An 18-year follow-up of overweight and risk of Alzheimer disease. Arch Intern Med 2003, 163:1524. 1518.
2. Whitmer RA, Gunderson EP, Quesenberry CP, Zhou J, Yaffe K Body mass index in midlife and risk of Alzheimer disease and vascular dementia. Curr Alzheimer Res 2007, 4:103-109.
3. Whitmer RA, Gustafson DR, Barrett-Connor E, Haan MN, Gunderson EP, Yaffe K Central obesity and increased risk of dementia more than three decades later. Neurology 2008, 71:1057-1064.
4. Fitzpatrick AL, Kuller LH, Lopez OL, et al. Midlife and late-life obesity and the risk of dementia: cardiovascular health study. Arch Neurol 2009, 66:336-342.
5. Kivipelto M, Ngandu T, Fratiglioni L, et al. Obesity and vascular risk factors at midlife and the risk of dementia and Alzheimer disease. Arch Neurol 2005, 62:1556-1560.
6. Gustafson DR, Backman K, Waern M, et al. Adiposity indicators and dementia over 32 years in Sweden. Neurology 2009, 73:1559-1566.
7. Hayden KM, Zandi PP, Lyketsos CG, et al. Vascular risk factors for incident Alzheimer disease and vascular dementia: the Cache County study. Alzheimer Dis Assoc Disord 2006, 20:93-100.
8. Besser LM, Gill DP, Monsell SE, et al. Body mass index, weight change, and clinical progression in mild cognitive impairment and Alzheimer's disease. Alzheimer Dis Assoc Disord 2014, 28:36-43.
9. Gustafson DR Adiposity and cognitive decline: underlying mechanisms. J Alzheimers Dis 2012, 30(suppl 2):S97-112.
10. Arnoldussen IAC, Kiliaan AJ, Gustafson DR Obesity and dementia: adipokines interact with the brain. Eur J Neuropsychopharmacol 2014, published online Mar 20. 10.1016/j.euroneuro.2014.03.002.
11. Chen JH, Lin KP, Chen YC Risk factors for dementia. J Formos Med Assoc 2009, 108:754-764.
12. Prunet-Marcassus B, Cousin B, Caton D, Andre M, Penicaud L, Casteilla L From heterogeneity to plasticity in adipose tissues: site-specific differences. Exp Cell Res 2006, 312:727-736.
13. Vindigni V, Tonello C, Lancerotto L, et al. Preliminary report of in vitro reconstruction of a vascularized tendon-like structure: a novel application for adipose-derived stem cells. Ann Plastic Surg 2013, 71:664-670.
14. Adipose tissue protocols 2010, Humana Press, New York. K. Yang (Ed.).
15. Lehr S, Hartwig S, Lamers D, et al. Identification and validation of novel adipokines released from primary human adipocytes. Mol Cell Proteomics 2012, 11. M111.010504.
16. Avram AS, Avram MM, James WD Subcutaneous fat in normal and diseased states: 2. Anatomy and physiology of white and brown adipose tissue. J Am Acad Dermatol 2005, 53:671-683.
17. Sbarbati A, Accorsi D, Benati D, et al. Subcutaneous adipose tissue classification. Eur J Histochem 2010, 54:e48.
18. Villarroya J, Cereijo R, Villarroya F An endocrine role for brown adipose tissue?. Am J Physiol Endocrinol Metab 2013, 305:E567-E572.
19. Esteve Rafols M Adipose tissue: cell heterogeneity and functional diversity. Endocrinol Nutr 2014, 61:100-112. [in English, Spanish].
20. Feng B, Zhang T, Xu H Human adipose dynamics and metabolic health. Ann N Y Acad Sci 2013, 1281:160-177.
21. Ferland M, Despres JP, Tremblay A, et al. Assessment of adipose tissue distribution by computed axial tomography in obese women: association with body density and anthropometric measurements. Br J Nutr 1989, 61:139-148.
22. Pouliot MC, Despres JP, Lemieux S, et al. Waist circumference and abdominal sagittal diameter: best simple anthropometric indexes of abdominal visceral adipose tissue accumulation and related cardiovascular risk in men and women. Am J Cardiol 1994, 73:460-468.
23. Seidell JC, Oosterlee A, Deurenberg P, Hautvast JG, Ruijs JH Abdominal fat depots measured with computed tomography: effects of degree of obesity, sex, and age. Eur J Clin Nutr 1988, 42:805-815.
24. Gallagher D, Visser M, Sepulveda D, Pierson RN, Harris T, Heymsfield SB How useful is body mass index for comparison of body fatness across age, sex, and ethnic groups?. Am J Epidemiol 1996, 143:228-239.
25. Campbell DR, Kurzer MS Flavonoid inhibition of aromatase enzyme activity in human preadipocytes. J Steroid Biochem Mol Biol 1993, 46:381-388.
26. Gustafson DR Adiposity hormones and dementia. J Neurol Sci 2010, 299:30-34.
27. Stedman's medical dictionary 2006, Lippincott Williams & Wilkins, Philadelphia. 25th edn.
28. Myelin formation, structure, and biochemistry. In: Basic neurochemistry: molecular, cellular, and medical aspects 1999, Lippincott Williams & Wilkins, Philadelphia. 5th edn. G.J. Siegel, B.W. Agranoff, R.W. Albers, S.K. Fisher, M.D. Uhler (Eds.).
29. Erta M, Quintana A, Hidalgo J Interleukin-6, a major cytokine in the central nervous system. Int J Biol Sci 2012, 8:1254-1266.
30. Wenk GL Neuropathologic changes in Alzheimer's disease. J Clin Psychiatry 2003, 64(suppl 9):7-10.
31. Michaud M, Balardy L, Moulis G, et al. Proinflammatory cytokines, aging, and age-related diseases. J Am Med Dir Assoc 2013, 14:877-882.
32. Van de Voorde J, Pauwels B, Boydens C, Decaluwe K Adipocytokines in relation to cardiovascular disease. Metabolism 2013, 62:1513-1521.
33. Bays HE Adiposopathy is "sick fat" a cardiovascular disease?. J Am Coll Cardiol 2011, 57:2461-2473.
34. Catindig JA, Venketasubramanian N, Ikram MK, Chen C Epidemiology of dementia in Asia: insights on prevalence, trends and novel risk factors. J Neurol Sci 2012, 321:11-16.
35. Balistreri CR, Caruso C, Candore G The role of adipose tissue and adipokines in obesity related inflammatory diseases. Mediators Inflamm 2010, 2010:802078.
36. Duvnjak L, Duvnjak M The metabolic syndrome-an ongoing story. J Physiol Pharmacol 2009, 60(suppl 7):19-24.
37. Figlewicz DP Adiposity signals and food reward: expanding the CNS roles of insulin and leptin. Am J Physiol Regul Integr Comp Physiol 2003, 284:R882-R892.
38. Hill JW, Elias CF, Fukuda M, et al. Direct insulin and leptin action on pro-opiomelanocortin neurons is required for normal glucose homeostasis and fertility. Cell Metab 2010, 11:286-297.
39. Gustafson D, Bäckman K, Lissner L, et al. Leptin and dementia over 32 years-The Prospective Population Study of Women. Alzheimers Dement 2012, 8:272-277.
40. Lieb W, Beiser AS, Vasan RS, et al. Association of plasma leptin levels with incident Alzheimer's disease and MRI measures of brain aging. JAMA 2009, 302:2565-2572.
41. Zeki Al Hazzouri A, Stone KL, Haan MN, Yaffe K Leptin, mild cognitive impairment, and dementia among elderly women. J Gerontol A Biol Sci Med Sci 2013, 68:175-180.
42. Holden KF, Lindquist K, Tylavsky FA, Rosano C, Harris TB, Yaffe K Serum leptin level and cognition in the elderly: findings from the Health ABC Study. Neurobiol Aging 2009, 30:1483-1489.
43. Ban Y, Watanabe T, Miyazaki A, et al. Impact of increased plasma serotonin levels and carotid atherosclerosis on vascular dementia. Atherosclerosis 2007, 195:153-159.
44. van Himbergen TM, Beiser AS, Ai M, et al. Biomarkers for insulin resistance and inflammation and the risk for all-cause dementia and Alzheimer disease: results from the Framingham Heart Study. Arch Neurol 2012, 69:594-600.
45. Roberts RO, Geda YE, Knopman DS, et al. Association of C-reactive protein with mild cognitive impairment. Alzheimers Dement 2009, 5:398-405.
46. Une K, Takei YA, Tomita N, et al. Adiponectin in plasma and cerebrospinal fluid in MCI and Alzheimer's disease. Eur J Neurol 2011, 18:1006-1009.
47. Teixeira AL, Diniz BS, Campos AC, et al. Decreased levels of circulating adiponectin in mild cognitive impairment and Alzheimer's disease. Neuromolecular Med 2013, 15:115-121.
48. Tan ZS, Beiser AS, Vasan RS, et al. Inflammatory markers and the risk of Alzheimer disease: the Framingham Study. Neurology 2007, 68:1902-1908.
49. Yaffe K, Kanaya A, Lindquist K, et al. The metabolic syndrome, inflammation, and risk of cognitive decline. JAMA 2004, 292:2237-2242.
50. van Exel E, Eikelenboom P, Comijs H, et al. Vascular factors and markers of inflammation in offspring with a parental history of late-onset Alzheimer disease. Arch Gen Psychiatry 2009, 66:1263-1270.
51. Zhang Y, Proenca R, Maffel M, Barone M, Leopold L, Friedman J Positional cloning of the mouse obese gene and its human homologue. Nature 1994, 372:425-432.
52. Maffei M, Halaas J, Ravussin E, et al. Leptin levels in human and rodent: measurement of plasma leptin and ob RNA in obese and weight-reduced subjects. Nat Med 1995, 1:1155-1161.
53. Banks W Is obesity a disease of the blood-brain barrier? Physiological, pathological, and evolutionary considerations. Curr Pharm Des 2003, 9:801-809.
54. Friedman J, Halaas L Leptin and the regulation of body weight in mammals. Nature 1998, 22:763-770.
55. Lissner L, Karlsson C, Lindroos AK, et al. Birth weight, adulthood BMI, and subsequent weight gain in relation to leptin levels in Swedish women. Obes Res 1999, 7:150-154.
56. Gustafson DR, Backman K, Joas E, et al. 37 years of body mass index and dementia: observations from the prospective population study of women in Gothenburg, Sweden. J Alzheimers Dis 2012, 28:163-171.
57. Peiser C, McGregor GP, Lang RE Binding and internalization of leptin by porcine choroid plexus cells in culture. Neurosci Lett 2000, 283:209-212.
58. Zlokovic BV, Jovanovic S, Miao W, Samara S, Verma S, Farrell CL Differential regulation of leptin transport by the choroid plexus and blood-brain barrier and high affinity transport systems for entry into hypothalamus and across the blood-cerebrospinal fluid barrier. Endocrinology 2000, 141:1434-1441.
59. Wiesner G, Vaz M, Collier G, et al. Leptin is released from the human brain: influence of adiposity and gender. J Clin Endocrinol Metab 1999, 84:2270-2274.
60. Morash B, Li A, Murphy PR, Wilkinson M, Ur E Leptin gene expression in the brain and pituitary gland. Endocrinology 1999, 140:5995-5998.
61. Brown R, Imran SA, Belsham DD, Ur E, Wilkinson M Adipokine gene expression in a novel hypothalamic neuronal cell line: resistin-dependent regulation of fasting-induced adipose factor and SOCS-3. Neuroendocrinology 2007, 85:232-241.
62. Brown R, Thompson HJ, Imran SA, Ur E, Wilkinson M Traumatic brain injury induces adipokine gene expression in rat brain. Neurosci Lett 2008, 432:73-78.
63. Wilkinson M, Brown R, Imran SA, Ur E Adipokine gene expression in brain and pituitary gland. Neuroendocrinology 2007, 86:191-209.
64. Schulz C, Paulus K, Lehnert H Adipocyte-brain: crosstalk. Results Probl Cell Differ 2010, 52:189-201.
65. Bluher M Adipose tissue dysfunction in obesity. Exp Clin Endocrinol Diabet 2009, 117:241-250.
66. Abizaid A, Horvath TL Brain circuits regulating energy homeostasis. Regul Pept 2008, 149:3-10.
67. Bluher S, Mantzoros CS Leptin in humans: lessons from translational research. Am J Clin Nutr 2009, 89:991S-997S.
68. Harvey J, Shanley LJ, O'Malley D, Irving AJ Leptin: a potential cognitive enhancer?. Biochem Soc Trans 2005, 33:1029-1032.
69. Davidson TL, Kanoski SE, Walls EK, Jarrard LE Memory inhibition and energy regulation. Physiol Behav 2005, 86:731-746.
70. Oomura Y, Aou S, Fukunaga K Prandial increase of leptin in the brain activates spatial learning and memory. Pathophysiology 2010, 17:119-127.
71. Fewlass DC, Noboa K, Pi-Sunyer FX, Johnston JM, Yan SD, Tezapsidis N Obesity-related leptin regulates Alzheimer's Abeta. FASEB J 2004, 18:1870-1878.
72. Kishi T, Elmquist JK Body weight is regulated by the brain: a link between feeding and emotion. Mol Psychiatry 2005, 10:132-146.
73. Qi Y, Takahashi N, Hileman SM, et al. Adiponectin acts in the brain to decrease body weight. Nat Med 2004, 10:524-529.
74. Carro EM Therapeutic approaches of leptin in Alzheimer's disease. Recent Pat CNS Drug Discov 2009, 4:200-208.
75. Sinha MK, Songer T, Xiao Q, et al. Analytical validation and biological evaluation of a high molecular-weight adiponectin ELISA. Clin Chem 2007, 53:2144-2151.
76. Chandran M, Phillips SA, Ciaraldi T, Henry RR Adiponectin: more than just another fat cell hormone?. Diabet Care 2003, 26:2442-2450.
77. Kubota N, Yano W, Kubota T, et al. Adiponectin stimulates AMP-activated protein kinase in the hypothalamus and increases food intake. Cell Metab 2007, 6:55-68.
78. Kusminski CM, McTernan PG, Schraw T, et al. Adiponectin complexes in human cerebrospinal fluid: distinct complex distribution from serum. Diabetologia 2007, 50:634-642.
79. Kos K, Harte AL, da Silva NF, et al. Adiponectin and resistin in human cerebrospinal fluid and expression of adiponectin receptors in the human hypothalamus. J Clin Endocrinol Metab 2007, 92:1129-1136.
80. Kang KH, Higashino A, Kim HS, Lee YT, Kageyama T Molecular cloning, gene expression, and tissue distribution of adiponectin and its receptors in the Japanese monkey, Macaca fuscata. J Med Primatol 2009, 38:77-85.
81. Angelidis G, Dafopoulos K, Messini CI, et al. The emerging roles of adiponectin in female reproductive system-associated disorders and pregnancy. Reprod Sci 2013, 20:872-881.
82. Qiu G, Wan R, Hu J, et al. Adiponectin protects rat hippocampal neurons against excitotoxicity. Age (Dordr) 2011, 33:155-165.
83. Fry M, Smith PM, Hoyda TD, et al. Area postrema neurons are modulated by the adipocyte hormone adiponectin. J Neurosci 2006, 26:9695-9702.
84. Buchman AS, Wilson RS, Bienias JL, Shah RC, Evans DA, Bennett DA Change in body mass index and risk of incident Alzheimer disease. Neurology 2005, 65:892-897.
85. Lenchik L, Register TC, Hsu FC, et al. Adiponectin as a novel determinant of bone mineral density and visceral fat. Bone 2003, 33:646-651.
86. Ryan AS, Berman DM, Nicklas BJ, et al. Plasma adiponectin and leptin levels, body composition, and glucose utilization in adult women with wide ranges of age and obesity. Diabetes Care 2003, 26:2383-2388.
87. Drolet R, Belanger C, Fortier M, et al. Fat depot-specific impact of visceral obesity on adipocyte adiponectin release in women. Obesity 2009, 17:424-430.
88. Blogowski W, Budkowska M, Salata D, et al. Clinical analysis of selected complement-derived molecules in human adipose tissue. J Transl Med 2013, 11:11.
89. Searfoss GH, Jordan WH, Calligaro DO, et al. Adipsin, a biomarker of gastrointestinal toxicity mediated by a functional gamma-secretase inhibitor. J Biol Chem 2003, 278:46107-46116.
90. Giordano P, Del Vecchio GC, Cecinati V, et al. Metabolic, inflammatory, endothelial and haemostatic markers in a group of Italian obese children and adolescents. Eur J Pediatr 2011, 170:845-850.
91. Mantovani RM, Rios DR, Moura LC, et al. Childhood obesity: evidence of an association between plasminogen activator inhibitor-1 levels and visceral adiposity. J Pediatr Endocrinol Metab 2011, 24:361-367.
92. Singh A, Foster GD, Gunawardana J, et al. Elevated circulating tissue factor procoagulant activity, factor VII, and plasminogen activator inhibitor-1 in childhood obesity: evidence of a procoagulant state. Br J Haematol 2012, 158:523-527.
93. Greenberg AS, Obin MS Obesity and the role of adipose tissue in inflammation and metabolism. Am J Clin Nutr 2006, 83:461S-465S.
94. Guerre-Millo M Adipose tissue and adipokines: for better or worse. Diabetes Metab 2004, 30:13-19.
95. Loskutoff DJ, Sawdey M, Mimuro J Type 1 plasminogen activator inhibitor. Prog Hemost Thromb 1989, 9:87-115.
96. Skurk T, Hauner H Obesity and impaired fibrinolysis: role of adipose production of plasminogen activator inhibitor-1. Int J Obes Relat Metab Disord 2004, 28:1357-1364.
97. Ahn MY, Zhang ZG, Tsang W, Chopp M Endogenous plasminogen activator expression after embolic focal cerebral ischemia in mice. Brain Res 1999, 837:169-176.
98. Jeon H, Kim JH, Kim JH, Lee WH, Lee MS, Suk K Plasminogen activator inhibitor type 1 regulates microglial motility and phagocytic activity. J Neuroinflammation 2012, 9:149.
99. Soeda S, Koyanagi S, Kuramoto Y, et al. Anti-apoptotic roles of plasminogen activator inhibitor-1 as a neurotrophic factor in the central nervous system. Thrombosis Haemostasis 2008, 100:1014-1020.
100. Soeda S, Oda M, Ochiai T, Shimeno H Deficient release of plasminogen activator inhibitor-1 from astrocytes triggers apoptosis in neuronal cells. Brain Res Mol Brain Res 2001, 91:96-103.
101. Ciccone A, Valvassori L, Nichelatti M, et al. Endovascular treatment for acute ischemic stroke. N Engl J Med 2013, 368:904-913.
102. Kasza A, Kowanetz M, Poslednik K, Witek B, Kordula T, Koj A Epidermal growth factor and pro-inflammatory cytokines regulate the expression of components of plasminogen activation system in U373-MG astrocytoma cells. Cytokine 2001, 16:187-190.
103. Murakami K, Suzuki M, Suzuki N, Hamajo K, Tsukamoto T, Shimojo M Cerebroprotective effects of TAK-937, a novel cannabinoid receptor agonist, in permanent and thrombotic focal cerebral ischemia in rats: therapeutic time window, combination with t-PA and efficacy in aged rats. Brain Res 2013, 1526:84-93.
104. Melchor JP, Pawlak R, Strickland S The tissue plasminogen activator-plasminogen proteolytic cascade accelerates amyloid-b (Ab) degradation and inhibits Ab-induced neurodegeneration. J Neurosci 2003, 23:8867-8871.
105. Medina MG, Ledesma MD, Dominguez JE, et al. Tissue plasminogen activator mediates amyloid-induced neurotoxicity via Erk1/2 activation. EMBO J 2005, 24:1706-1716.
106. Barker R, Kehoe PG, Love S Activators and inhibitors of the plasminogen system in Alzheimer's disease. J Cell Mol Med 2012, 16:865-876.
107. Das UN Is obesity an inflammatory condition?. Nutrition 2001, 17:953-966.
108. Boulanger MJ, Chow DC, Brevnova EE, Garcia KC Hexameric structure and assembly of the interleukin-6/IL-6 alpha-receptor/gp130 complex. Science 2003, 300:2101-2104.
109. Banks WA, Kastin AJ, Gutierrez EG Penetration of interleukin-6 across the murine blood-brain barrier. Neurosci Lett 1994, 179:53-56.
110. Frei K, Malipiero UV, Leist TP, Zinkernagel RM, Schwab ME, Fontana A On the cellular source and function of interleukin 6 produced in the central nervous system in viral diseases. Eur J Immunol 1989, 19:689-694.
111. Lieberman AP, Pitha PM, Shin HS, Shin ML Production of tumor necrosis factor and other cytokines by astrocytes stimulated with lipopolysaccharide or a neurotropic virus. Proc Natl Acad Sci USA 1989, 86:6348-6352.
112. Fabry Z, Fitzsimmons KM, Herlein JA, Moninger TO, Dobbs MB, Hart MN Production of the cytokines interleukin 1 and 6 by murine brain microvessel endothelium and smooth muscle pericytes. J Neuroimmunol 1993, 47:23-34.
113. Balschun D, Wetzel W, Del Rey A, et al. Interleukin-6: a cytokine to forget. FASEB J 2004, 18:1788-1790.
114. Nelson TE, Olde Engberink A, Hernandez R, et al. Altered synaptic transmission in the hippocampus of transgenic mice with enhanced central nervous systems expression of interleukin-6. Brain Behav Immun 2012, 26:959-971.
115. Richwine AF, Parkin AO, Buchanan JB, et al. Architectural changes to CA1 pyramidal neurons in adult and aged mice after peripheral immune stimulation. Psychoneuroendocrinology 2008, 33:1369-1377.
116. Tancredi V, D'Antuono M, Cafe C, et al. The inhibitory effects of interleukin-6 on synaptic plasticity in the rat hippocampus are associated with an inhibition of mitogen-activated protein kinase ERK. J Neurochem 2000, 75:634-643.
117. Ropelle ER, Flores MB, Cintra DE, et al. IL-6 and IL-10 anti-inflammatory activity links exercise to hypothalamic insulin and leptin sensitivity through IKKβ and ER stress inhibition. PLoS Biol 2010, 8:e1000465.
118. Marsland AL, Gianaros PJ, Abramowitch SM, Manuck SB, Hariri AR Interleukin-6 covaries inversely with hippocampal grey matter volume in middle-aged adults. Biol Psychiatry 2008, 64:484-490.
119. Sartipy P, Loskutoff DJ Monocyte chemoattractant protein 1 in obesity and insulin resistance. Proc Natl Acad Sci USA 2003, 100:7265-7270.
120. Samad F, Pandey M, Bell PA, Loskutoff DJ Insulin continues to induce plasminogen activator inhibitor 1 gene expression in insulin-resistant mice and adipocytes. Mol Med 2000, 6:680-692.
121. Shimomura I, Matsuda M, Hammer RE, Bashmakov Y, Brown MS, Goldstein JL Decreased IRS-2 and increased SREBP-1c lead to mixed insulin resistance and sensitivity in livers of lipodystrophic and ob/ob mice. Mol Cell 2000, 6:77-86.
122. Cusi K, Maezono K, Osman A, et al. Insulin resistance differentially affects the PI 3-kinase- and MAP kinase-mediated signaling in human muscle. J Clin Invest 2000, 105:311-320.
123. Jiang ZY, Lin YW, Clemont A, et al. Characterization of selective resistance to insulin signaling in the vasculature of obese Zucker (fa/fa) rats. J Clin Invest 1999, 104:447-457.
124. Kanda H, Tateya S, Tamori Y, et al. MCP-1 contributes to macrophage infiltration into adipose tissue, insulin resistance, and hepatic steatosis in obesity. J Clin Invest 2006, 116:1494-1505.
125. Ho L, Zhao W, Dams-O'Connor K, et al. Elevated plasma MCP-1 concentration following traumatic brain injury as a potential "predisposition" factor associated with an increased risk for subsequent development of Alzheimer's disease. J Alzheimers Dis 2012, 31:301-313.
126. Jung C, Fritzenwanger M, Fischer N, Figulla HR Hepatocyte growth factor is elevated in obese adolescents. J Pediatr Endocrinol Metab 2009, 22:645-651.
127. Bell LN, Ward JL, Degawa-Yamauchi M, et al. Adipose tissue production of hepatocyte growth factor contributes to elevated serum HGF in obesity. Am J Physiol Endocrinol Metabol 2006, 291:E843-E848.
128. Jung W, Castren E, Odenthal M, et al. Expression and functional interaction of hepatocyte growth factor-scatter factor and its receptor c-met in mammalian brain. J Cell Biol 1994, 126:485-494.
129. Powell EM, Campbell DB, Stanwood GD, Davis C, Noebels JL, Levitt P Genetic disruption of cortical interneuron development causes region- and GABA cell type-specific deficits, epilepsy, and behavioral dysfunction. J Neurosci 2003, 23:622-631.
130. Nagayama T, Nagayama M, Kohara S, et al. Post-ischemic delayed expression of hepatocyte growth factor and c-Met in mouse brain following focal cerebral ischemia. Brain Res 2004, 999:155-166.
131. Fenton H, Finch PW, Rubin JS, et al. Hepatocyte growth factor (HGF/SF) in Alzheimer's disease. Brain Res 1998, 779:262-270.
132. Akimoto M, Baba A, Ikeda-Matsuo Y, et al. Hepatocyte growth factor as an enhancer of nmda currents and synaptic plasticity in the hippocampus. Neuroscience 2004, 128:155-162.
133. Date I, Takagi N, Takagi K, et al. Hepatocyte growth factor improved learning and memory dysfunction of microsphere-embolized rats. J Neurosci Res 2004, 78:442-453.
134. Shimamura M, Sato N, Nakagami H, Taniyama Y, Morishita R Development of nucleic acid drugs for neurological disorders. Curr Top Med Chem 2012, 12:1621-1629.
135. Manni L, Rocco ML, Bianchi P, et al. Nerve growth factor: basic studies and possible therapeutic applications. Growth Factors 2013, 31:115-122.
136. Cattaneo A, Calissano P Nerve growth factor and Alzheimer's disease: new facts for an old hypothesis. Mol Neurobiol 2012, 46:588-604.
137. Fragkouli A, Tzinia AK, Charalampopoulos I, Gravanis A, Tsilibary EC Matrix metalloproteinase-9 participates in NGF-induced alpha-secretase cleavage of amyloid-beta protein precursor in PC12 cells. J Alzheimers Dis 2011, 24:705-719.
138. Giacobini E, Becker RE One hundred years after the discovery of Alzheimer's disease. A turning point for therapy?. J Alzheimers Dis 2007, 12:37-52.
139. Konukoglu D, Andican G, Firtina S, Erkol G, Kurt A Serum brain-derived neurotrophic factor, nerve growth factor and neurotrophin-3 levels in dementia. Acta Neurol Belg 2012, 112:255-260.
140. Blasko I, Lederer W, Oberbauer H, et al. Measurement of thirteen biological markers in CSF of patients with Alzheimer's disease and other dementias. Dement Geriatr Cogn Disord 2006, 21:9-15.
141. Tian L, Guo R, Yue X, et al. Intranasal administration of nerve growth factor ameliorate beta-amyloid deposition after traumatic brain injury in rats. Brain Res 2012, 1440:47-55.
142. Lee SA, Kallianpur A, Xiang YB, et al. Intra-individual variation of plasma adipokine levels and utility of single measurement of these biomarkers in population-based studies. Cancer Epidemiol Biomarkers Prev 2007, 16:2464-2470.
143. Azrad M, Gower BA, Hunter GR, Nagy TR Racial differences in adiponectin and leptin in healthy premenopausal women. Endocrine 2013, 43:586-592.
144. Khan UI, Wang D, Sowers MR, et al. Race-ethnic differences in adipokine levels: the Study of Women's Health Across the Nation (SWAN). Metab Clin Exp 2012, 61:1261-1269.
145. Cruz-Jentoft AJ, Baeyens JP, Bauer JM, et al. Sarcopenia: European consensus on definition and diagnosis: report of the European Working Group on Sarcopenia in Older People. Age Ageing 2010, 39:412-423.
146. Stevens J, Cai J, Pamuk ER, Williamson DF, Thun MJ, Wood JL The effect of age on the association between body-mass index and mortality. N Engl J Med 1998, 338:1-7.