Western-type diet modulates inflammatory responses and impairs functional outcome following permanent middle cerebral artery occlusion in aged mice expressing the human apolipoprotein E4 allele

Journal of Neuroinflammation

Volumn 10, Issue , 2013, Pages

  Dhungana, Hiramani ^a   Rolova, Taisia ^a   Savchenko, Ekaterina ^a   Wojciechowski, Sara ^a   Savolainen, Kaisa ^a   Ruotsalainen, Anna Kaisa ^a   Sullivan, Patrick M ^b   Koistinaho, Jari ^a,c   Malm, Tarja ^a  

^a UNIVERSITY OF EASTERN FINLAND   (Finland)

^b DUKE UNIVERSITY   (United States)

^c KUOPIO UNIVERSITY HOSPITAL   (Finland)

Author keywords

Aging; Apolipoprotein E; Atherosclerosis; Brain ischemia; Inflammation; Western diet

Indexed keywords

APOLIPOPROTEIN E3; APOLIPOPROTEIN E4; CYCLOOXYGENASE 2; INTERLEUKIN 6; ISOPROTEIN;

AGING; ALLELE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN INFARCTION; BRAIN ISCHEMIA; CELL ACTIVATION; CHOLESTEROL BLOOD LEVEL; CHOLESTEROL DIET; CONTROLLED STUDY; DISEASE PREDISPOSITION; FUNCTIONAL STATUS; IMMUNOREACTIVITY; MACROGLIA; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; MOTOR DYSFUNCTION; MOUSE; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM INFLAMMATION; NEUROMODULATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; SENSORY DYSFUNCTION;

AGING; ALLELES; ANIMALS; APOLIPOPROTEIN E4; ATHEROSCLEROSIS; COMORBIDITY; DIET, HIGH-FAT; DISEASE MODELS, ANIMAL; GENOTYPE; HUMANS; IMMUNOHISTOCHEMISTRY; INFARCTION, MIDDLE CEREBRAL ARTERY; INFLAMMATION; MAGNETIC RESONANCE IMAGING; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MOTOR ACTIVITY; RECOVERY OF FUNCTION;

EID: 84883541769     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/1742-2094-10-102     Document Type: Article

References (48)

1. Iadecola C, Anrather J. The immunology of stroke: from mechanisms to translation. Nat Med 2011, 17:796-808. 10.1038/nm.2399, 3137275, 21738161.
2. Endres M, Engelhardt B, Koistinaho J, Lindvall O, Meairs S, Mohr JP, Planas A, Rothwell N, Schwaninger M, Schwab ME, Vivien D, Wieloch T, Dirnagl U. Improving outcome after stroke: overcoming the translational roadblock. Cerebrovasc Dis 2008, 25:268-278. 10.1159/000118039, 18292653.
3. Mahley RW, Huang Y. Apolipoprotein E: from atherosclerosis to Alzheimer's disease and beyond. Curr Opin Lipidol 1999, 10:207-217. 10.1097/00041433-199906000-00003, 10431657.
4. Huang Y. Mechanisms linking apolipoprotein E isoforms with cardiovascular and neurological diseases. Curr Opin Lipidol 2010, 21:337-345. 10.1097/MOL.0b013e32833af368, 20531185.
5. Mahley RW, Rall SC. Apolipoprotein E: far more than a lipid transport protein. Annu Rev Genomics Hum Genet 2000, 1:507-537. 10.1146/annurev.genom.1.1.507, 11701639.
6. Huang Y. Roles of apolipoprotein E4 (ApoE4) in the pathogenesis of Alzheimer's disease: lessons from ApoE mouse models. Biochem Soc Trans 2011, 39:924-932. 10.1042/BST0390924, 21787325.
7. Dik MG, Deeg DJ, Bouter LM, Corder EH, Kok A, Jonker C. Stroke and apolipoprotein E ε{lunate}4 are independent risk factors for cognitive decline: a population-based study. Stroke 2000, 31:2431-2436. 10.1161/01.STR.31.10.2431, 11022076.
8. Lynch JR, Tang W, Wang H, Vitek MP, Bennett ER, Sullivan PM, Warner DS, Laskowitz DT. APOE genotype and an ApoE-mimetic peptide modify the systemic and central nervous system inflammatory response. J Biol Chem 2003, 278:48529-48533. 10.1074/jbc.M306923200, 14507923.
9. Sieber MW, Claus RA, Witte OW, Frahm C. Attenuated inflammatory response in aged mice brains following stroke. PLoS One 2011, 6:e26288. 10.1371/journal.pone.0026288, 3196544, 22028848.
10. Laskowitz DT, Sheng H, Bart RD, Joyner KA, Roses AD, Warner DS. Apolipoprotein E-deficient mice have increased susceptibility to focal cerebral ischemia. J Cereb Blood Flow Metab 1997, 17:753-758.
11. Sheng H, Laskowitz DT, Bennett E, Schmechel DE, Bart RD, Saunders AM, Pearlstein RD, Roses AD, Warner DS. Apolipoprotein E isoform-specific differences in outcome from focal ischemia in transgenic mice. J Cereb Blood Flow Metab 1998, 18:361-366.
12. Slooter AJ, Tang MX, van Duijn CM, Stern Y, Ott A, Bell K, Breteler MM, Van Broeckhoven C, Tatemichi TK, Tycko B, Hofman A, Mayeux R. Apolipoprotein E epsilon4 and the risk of dementia with stroke. A population-based investigation. JAMA 1997, 277:818-821. 10.1001/jama.1997.03540340052032, 9052712.
13. Sheng H, Laskowitz DT, Mackensen GB, Kudo M, Pearlstein RD, Warner DS. Apolipoprotein E deficiency worsens outcome from global cerebral ischemia in the mouse. Stroke 1999, 30:1118-1124. 10.1161/01.STR.30.5.1118, 10229753.
14. Sullivan PM, Mezdour H, Aratani Y, Knouff C, Najib J, Reddick RL, Quarfordt SH, Maeda N. Targeted replacement of the mouse apolipoprotein E gene with the common human APOE3 allele enhances diet-induced hypercholesterolemia and atherosclerosis. J Biol Chem 1997, 272:17972-17980. 10.1074/jbc.272.29.17972, 9218423.
15. Koistinaho M, Kettunen MI, Goldsteins G, Keinanen R, Salminen A, Ort M, Bures J, Liu D, Kauppinen RA, Higgins LS, Koistinaho J. Beta-amyloid precursor protein transgenic mice that harbor diffuse A beta deposits but do not form plaques show increased ischemic vulnerability: role of inflammation. Proc Natl Acad Sci U S A 2002, 99:1610-1615. 10.1073/pnas.032670899, 122238, 11818564.
16. Shuaib A, Xu Wang C, Yang T, Noor R. Effects of nonpeptide V(1) vasopressin receptor antagonist SR-49059 on infarction volume and recovery of function in a focal embolic stroke model. Stroke 2002, 33:3033-3037. 10.1161/01.STR.0000039405.31526.06, 12468809.
17. Bouet V, Boulouard M, Toutain J, Divoux D, Bernaudin M, Schumann-Bard P, Freret T. The adhesive removal test: a sensitive method to assess sensorimotor deficits in mice. Nat Protoc 2009, 4:1560-1564. 10.1038/nprot.2009.125, 19798088.
18. Li G, Bien-Ly N, Andrews-Zwilling Y, Xu Q, Bernardo A, Ring K, Halabisky B, Deng C, Mahley RW, Huang Y. GABAergic interneuron dysfunction impairs hippocampal neurogenesis in adult apolipoprotein E4 knockin mice. Cell Stem Cell 2009, 5:634-645. 10.1016/j.stem.2009.10.015, 2992822, 19951691.
19. Crawford F, Wood M, Ferguson S, Mathura V, Gupta P, Humphrey J, Mouzon B, Laporte V, Margenthaler E, O'Steen B, Hayes R, Roses A, Mullan M. Apolipoprotein E-genotype dependent hippocampal and cortical responses to traumatic brain injury. Neuroscience 2009, 159:1349-1362. 10.1016/j.neuroscience.2009.01.033, 19409232.
20. James ML, Sullivan PM, Lascola CD, Vitek MP, Laskowitz DT. Pharmacogenomic effects of apolipoprotein e on intracerebral hemorrhage. Stroke 2009, 40:632-639. 10.1161/STROKEAHA.108.530402, 2699752, 19109539.
21. Mannix RC, Zhang J, Park J, Zhang X, Bilal K, Walker K, Tanzi RE, Tesco G, Whalen MJ. Age-dependent effect of apolipoprotein E4 on functional outcome after controlled cortical impact in mice. J Cereb Blood Flow Metab 2011, 31:351-361. 10.1038/jcbfm.2010.99, 3049498, 20588316.
22. Mori T, Town T, Kobayashi M, Tan J, Fujita SC, Asano T. Augmented delayed infarct expansion and reactive astrocytosis after permanent focal ischemia in apolipoprotein E4 knock-in mice. J Cereb Blood Flow Metab 2004, 24:646-656.
23. Horsburgh K, McCulloch J, Nilsen M, Roses AD, Nicoll JA. Increased neuronal damage and apoE immunoreactivity in human apolipoprotein E, E4 isoform-specific, transgenic mice after global cerebral ischaemia. Eur J Neurosci 2000, 12:4309-4317.
24. Wagle J, Farner L, Flekkoy K, Wyller TB, Sandvik L, Eiklid KL, Fure B, Stensrod B, Engedal K. Association between ApoE epsilon4 and cognitive impairment after stroke. Dement Geriatr Cogn Disord 2009, 27:525-533. 10.1159/000223230, 19494491.
25. Klein RC, Mace BE, Moore SD, Sullivan PM. Progressive loss of synaptic integrity in human apolipoprotein E4 targeted replacement mice and attenuation by apolipoprotein E2. Neuroscience 2010, 171:1265-1272. 10.1016/j.neuroscience.2010.10.027, 2991419, 20951774.
26. Trommer BL, Shah C, Yun SH, Gamkrelidze G, Pasternak ES, Ye GL, Sotak M, Sullivan PM, Pasternak JF, LaDu MJ. ApoE isoform affects LTP in human targeted replacement mice. Neuroreport 2004, 15:2655-2658. 10.1097/00001756-200412030-00020, 15570172.
27. Bour A, Grootendorst J, Vogel E, Kelche C, Dodart JC, Bales K, Moreau PH, Sullivan PM, Mathis C. Middle-aged human apoE4 targeted-replacement mice show retention deficits on a wide range of spatial memory tasks. Behav Brain Res 2008, 193:174-182. 10.1016/j.bbr.2008.05.008, 18572260.
28. Buchman AS, Boyle PA, Wilson RS, Beck TL, Kelly JF, Bennett DA. Apolipoprotein E e4 allele is associated with more rapid motor decline in older persons. Alzheimer Dis Assoc Disord 2009, 23:63-69. 10.1097/WAD.0b013e31818877b5, 2662708, 19266700.
29. Molteni R, Barnard RJ, Ying Z, Roberts CK, Gomez-Pinilla F. A high-fat, refined sugar diet reduces hippocampal brain-derived neurotrophic factor, neuronal plasticity, and learning. Neuroscience 2002, 112:803-814. 10.1016/S0306-4522(02)00123-9, 12088740.
30. Pistell PJ, Morrison CD, Gupta S, Knight AG, Keller JN, Ingram DK, Bruce-Keller AJ. Cognitive impairment following high fat diet consumption is associated with brain inflammation. J Neuroimmunol 2010, 219:25-32. 10.1016/j.jneuroim.2009.11.010, 2823983, 20004026.
31. Li N, Kong X, Ye R, Yang Q, Han J, Xiong L. Age-related differences in experimental stroke: possible involvement of mitochondrial dysfunction and oxidative damage. Rejuvenation Res 2011, 14:261-273. 10.1089/rej.2010.1115, 21466386.
32. Duan YL, Wang SY, Zeng QW, Su DS, Li W, Wang XR, Zhao Z. Astroglial reaction to delta opioid peptide [D-Ala2, D-Leu5] enkephalin confers neuroprotection against global ischemia in the adult rat hippocampus. Neuroscience 2011, 192:81-90.
33. Faulkner JR, Herrmann JE, Woo MJ, Tansey KE, Doan NB, Sofroniew MV. Reactive astrocytes protect tissue and preserve function after spinal cord injury. J Neurosci 2004, 24:2143-2155. 10.1523/JNEUROSCI.3547-03.2004, 14999065.
34. Szydlowska K, Zawadzka M, Kaminska B. Neuroprotectant FK506 inhibits glutamate-induced apoptosis of astrocytes in vitro and in vivo. J Neurochem 2006, 99:965-975. 10.1111/j.1471-4159.2006.04136.x, 17076660.
35. Zhao Y, Rempe DA. Targeting astrocytes for stroke therapy. Neurotherapeutics 2010, 7:439-451. 10.1016/j.nurt.2010.07.004, 20880507.
36. Crisby M, Rahman SM, Sylven C, Winblad B, Schultzberg M. Effects of high cholesterol diet on gliosis in apolipoprotein E knockout mice. Implications for Alzheimer's disease and stroke. Neurosci Lett 2004, 369:87-92. 10.1016/j.neulet.2004.05.057, 15450674.
37. Candelario-Jalil E, Fiebich BL. Cyclooxygenase inhibition in ischemic brain injury. Curr Pharm Des 2008, 14:1401-1418. 10.2174/138161208784480216, 18537663.
38. Zhang X, Dong F, Ren J, Driscoll MJ, Culver B. High dietary fat induces NADPH oxidase-associated oxidative stress and inflammation in rat cerebral cortex. Exp Neurol 2005, 191:318-325. 10.1016/j.expneurol.2004.10.011, 15649487.
39. Denes A, Humphreys N, Lane TE, Grencis R, Rothwell N. Chronic systemic infection exacerbates ischemic brain damage via a CCL5 (regulated on activation, normal T-cell expressed and secreted)-mediated proinflammatory response in mice. J Neurosci 2010, 30:10086-10095. 10.1523/JNEUROSCI.1227-10.2010, 3044869, 20668193.
40. McColl BW, Rothwell NJ, Allan SM. Systemic inflammatory stimulus potentiates the acute phase and CXC chemokine responses to experimental stroke and exacerbates brain damage via interleukin-1- and neutrophil-dependent mechanisms. J Neurosci 2007, 27:4403-4412. 10.1523/JNEUROSCI.5376-06.2007, 17442825.
41. Schram MT, Euser SM, de Craen AJ, Witteman JC, Frolich M, Hofman A, Jolles J, Breteler MM, Westendorp RG. Systemic markers of inflammation and cognitive decline in old age. J Am Geriatr Soc 2007, 55:708-716. 10.1111/j.1532-5415.2007.01159.x, 17493190.
42. Suzuki S, Tanaka K, Suzuki N. Ambivalent aspects of interleukin-6 in cerebral ischemia: inflammatory versus neurotrophic aspects. J Cereb Blood Flow Metab 2009, 29:464-479. 10.1038/jcbfm.2008.141, 19018268.
43. Grocott HP, Newman MF, El-Moalem H, Bainbridge D, Butler A, Laskowitz DT. Apolipoprotein E genotype differentially influences the proinflammatory and anti-inflammatory response to cardiopulmonary bypass. J Thorac Cardiovasc Surg 2001, 122:622-623. 10.1067/mtc.2001.115152, 11547323.
44. Grunenfelder J, Umbehr M, Plass A, Bestmann L, Maly FE, Zund G, Turina M. Genetic polymorphisms of apolipoprotein E4 and tumor necrosis factor beta as predisposing factors for increased inflammatory cytokines after cardiopulmonary bypass. J Thorac Cardiovasc Surg 2004, 128:92-97. 10.1016/j.jtcvs.2004.02.022, 15224026.
45. Moretti EW, Morris RW, Podgoreanu M, Schwinn DA, Newman MF, Bennett E, Moulin VG, Mba UU, Laskowitz DT. APOE polymorphism is associated with risk of severe sepsis in surgical patients. Crit Care Med 2005, 33:2521-2526. 10.1097/01.CCM.0000186368.96146.FB, 16276176.
46. Colton CA, Needham LK, Brown C, Cook D, Rasheed K, Burke JR, Strittmatter WJ, Schmechel DE, Vitek MP. APOE genotype-specific differences in human and mouse macrophage nitric oxide production. J Neuroimmunol 2004, 147:62-67. 10.1016/j.jneuroim.2003.10.015, 14741429.
47. Knouff C, Hinsdale ME, Mezdour H, Altenburg MK, Watanabe M, Quarfordt SH, Sullivan PM, Maeda N. Apo E structure determines VLDL clearance and atherosclerosis risk in mice. J Clin Invest 1999, 103:1579-1586. 10.1172/JCI6172, 408371, 10359567.
48. Jin K, Minami M, Lan JQ, Mao XO, Batteur S, Simon RP, Greenberg DA. Neurogenesis in dentate subgranular zone and rostral subventricular zone after focal cerebral ischemia in the rat. Proc Natl Acad Sci USA 2001, 98:4710-4715. 10.1073/pnas.081011098, 31899, 11296300.