CD36 upregulation mediated by intranasal lv-nrf2 treatment mitigates hypoxia-induced progression of Alzheimer's-like pathogenesis

Antioxidants and Redox Signaling

Volumn 21, Issue 16, 2014, Pages 2208-2230

  Wang, Chun Yan ^a,b,c   Wang, Zhan You ^a,b   Xie, Jing Wei ^a   Cai, Jian Hui ^c   Wang, Tao ^a,b   Xu, Ye ^c   Wang, Xu ^d   An, Li ^a  

^a CHINA MEDICAL UNIVERSITY   (China)

^b NORTHEASTERN UNIVERSITY   (China)

^c JILIN MEDICAL COLLEGE   (China)

^d LIAONING UNIVERSITY OF TRADITIONAL CHINESE MEDICINE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; CD36 ANTIGEN; LENTIVIRUS VECTOR; TRANSCRIPTION FACTOR NRF2; AMYLOID PRECURSOR PROTEIN; NFE2L2 PROTEIN, HUMAN;

AGING; ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DISEASE COURSE; GENE TARGETING; HYPOXIA; LEARNING DISORDER; MALE; MEMORY DISORDER; MICROGLIA; MOUSE; NERVOUS SYSTEM INFLAMMATION; NEUROPATHOLOGY; NONHUMAN; PROTEIN DEGRADATION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SPATIAL LEARNING; SPATIAL MEMORY; TRANSACTIVATION; UPREGULATION; ANIMAL; ANOXIA; DISEASE MODEL; ENZYMOLOGY; EXON; GENE THERAPY; GENETICS; HUMAN; LENTIVIRINAE; METABOLISM; OXIDATIVE STRESS; TRANSGENIC MOUSE;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; ANOXIA; ANTIGENS, CD36; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; EXONS; GENETIC THERAPY; HUMANS; LENTIVIRUS; MICE; MICE, TRANSGENIC; MICROGLIA; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; UP-REGULATION;

EID: 84913591310     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2014.5845     Document Type: Article

References (78)

1. Aliev G, Smith MA, Seyidov D, Neal ML, Lamb BT, Nunomura A, Gasimov EK, Vinters HV, Perry G, Lamanna JC, and Friedland RP. The role of oxidative stress in the pathophysiology of cerebrovascular lesions in Alzheimer's disease. Brain Pathol 12: 21-35, 2002.
2. Bao Y, Qin L, Kim E, Bhosle S, Guo H, Febbraio M, Haskew-Layton RE, Ratan R, and Cho S. CD36 is involved in astrocyte activation and astroglial scar formation. J Cereb Blood Flow Metab 32: 1567-1577, 2012.
3. Bard F, Cannon C, Barbour R, Burke RL, Games D, Grajeda H, Guido T, Hu K, Huang J, Johnson-Wood K, Khan K, Kholodenko D, Lee M, Lieberburg I, Motter R, Nguyen M, Soriano F, Vasquez N, Weiss K, Welch B, Seubert P, Schenk D, and Yednock T. Peripherally administered antibodies against amyloid beta-peptide enter the central nervous system and reduce pathology in a mouse model of Alzheimer disease. Nat Med 6: 916-919, 2000.
4. Barhwal K, Hota SK, Jain V, Prasad D, Singh SB, and Ilavazhagan G. Acetyl-l-carnitine (ALCAR) prevents hypobaric hypoxia-induced spatial memory impairment through extracellular related kinase-mediated nuclear factor erythroid 2-related factor 2 phosphorylation. Neuroscience 161: 501-514, 2009.
5. Barja G. Free radicals and aging. Trends Neurosci 27: 595-600, 2004.
6. Barnwell JW, Asch AS, Nachman RL, Yamaya M, Aikawa M, and Ingravallo P. A human 88-kD membrane glycoprotein (CD36) functions in vitro as a receptor for a cytoadherence ligand on Plasmodium falciparum-infected erythrocytes. J Clin Invest 84: 765-772, 1989.
7. Bazan NG and Lukiw WJ. Cyclooxygenase-2 and presenilin-1 gene expression induced by interleukin-1beta and amyloid beta 42 peptide is potentiated by hypoxia in primary human neural cells. J Biol Chem 277: 30359-30367, 2002.
8. Bazan NG, Palacios-Pelaez R, and Lukiw WJ. Hypoxia signaling to genes: significance in Alzheimer's disease. Mol Neurobiol 26: 283-298, 2002.
9. Bell EL, Klimova TA, Eisenbart J, Moraes CT, Murphy MP, Budinger GR, and Chandel NS. The Qo site of the mitochondrial complex III is required for the transduction of hypoxic signaling via reactive oxygen species production. J Cell Biol 177: 1029-1036, 2007.
10. Calabrese V, Cornelius C, Dinkova-Kostova AT, Calabrese EJ, and Mattson MP. Cellular stress responses, the hormesis paradigm, and vitagenes: novel targets for therapeutic intervention in neurodegenerative disorders. Antioxid Redox Signal 13: 1763-1811, 2010.
11. Carvalho C, Correia SC, Santos RX, Cardoso S, Moreira PI, Clark TA, Zhu X, Smith MA, and Perry G. Role of mitochondrial-mediated signaling pathways in Alzheimer disease and hypoxia. J Bioenerg Biomembr 41: 433-440, 2009.
12. Chang S, Jiang X, Zhao C, Lee C, and Ferriero DM. Exogenous low dose hydrogen peroxide increases hypoxiainducible factor-1alpha protein expression and induces preconditioning protection against ischemia in primary cortical neurons. Neurosci Lett 441: 134-138, 2008.
13. Coraci IS, Husemann J, Berman JW, Hulette C, Dufour JH, Campanella GK, Luster AD, Silverstein SC, and El-Khoury JB. CD36, a class B scavenger receptor, is expressed on microglia in Alzheimer's disease brains and can mediate production of reactive oxygen species in response to betaamyloid fibrils. Am J Pathol 160: 101-112, 2002.
14. Crouch PJ, Hung LW, Adlard PA, Cortes M, Lal V, Filiz G, Perez KA, Nurjono M, Caragounis A, Du T, Laughton K, Volitakis I, Bush AI, Li QX, Masters CL, Cappai R, Cherny RA, Donnelly PS, White AR, and Barnham KJ. Increasing Cu bioavailability inhibits Abeta oligomers and tau phosphorylation. Proc Natl Acad Sci U S A 106: 381-386, 2009.
15. D'archivio M, Scazzocchio B, Filesi C, Vari R, Maggiorella T, Sernicola L, Santangelo C, Giovannini C, and Masella R. Oxidised LDL up-regulate CD36 expression by the Nrf2 pathway in 3T3-L1 preadipocytes. FEBS Lett 582: 2291-2298, 2008.
16. Desmond DW, Moroney JT, Sano M, and Stern Y. Incidence of dementia after ischemic stroke: results of a longitudinal study. Stroke 33: 2254-2260, 2002.
17. Donovan EL, Mccord JM, Reuland DJ, Miller BF, and Hamilton KL. Phytochemical activation of Nrf2 protects human coronary artery endothelial cells against an oxidative challenge. Oxidative Med Cell Longev 2012: 132931, 2012.
18. Dröge W. Free radicals in the physiological control of cell function. Physiol Rev 82: 47-95, 2002.
19. Eba S, Hoshikawa Y, Moriguchi T, Mitsuishi Y, Satoh H, Ishida K, Watanabe T, Shimizu T, Shimokawa H, Okada Y, Yamamoto M, and Kondo T. The nuclear factor erythroid 2-related factor 2 activator oltipraz attenuates chronic hypoxia-induced cardiopulmonary alterations in mice. Am J Respir Cell Mol Biol 49: 324-333, 2013.
20. Eftekharzadeh B, Maghsoudi N, and Khodagholi F. Stabilization of transcription factor Nrf2 by tBHQ prevents oxidative stress-induced amyloid beta formation in NT2N neurons. Biochimie 92: 245-253, 2010.
21. El Khoury J, Hickman SE, Thomas CA, Loike JD, and Silverstein SC. Microglia, scavenger receptors, and the pathogenesis of Alzheimer's disease. Neurobiol Aging 19: S81-S84, 1998.
22. El Khoury JB, Moore KJ, Means TK, Leung J, Terada K, Toft M, Freeman MW, and Luster AD. CD36 mediates the innate host response to beta-Amyloid. J Exp Med 197: 1657-1666, 2003.
23. Febbraio M, Hajjar DP, and Silverstein RL. CD36: a class B scavenger receptor involved in angiogenesis, atherosclerosis, inflammation, and lipid metabolism. J Clin Invest 108: 785-791, 2001.
24. Floden AM and Combs CK. Microglia demonstrate agedependent interaction with amyloid-beta fibrils. J Alzheimer's Dis 25: 279-293, 2011.
25. Flora SJ, Bhatt K, and Mehta A. Arsenic moiety in gallium arsenide is responsible for neuronal apoptosis and behavioral alterations in rats. Toxicol Appl Pharmacol 240: 236-244, 2009.
26. Giordano FJ. Oxygen, oxidative stress, hypoxia, and heart failure. J Clin Invest 115: 500-508, 2005.
27. Heneka MT, Nadrigny F, Regen T, Martinez-Hernandez A, Dumitrescu-Ozimek L, Terwel D, Jardanhazi-Kurutz D, Walter J, Kirchhoff F, Hanisch UK, and Kummer MP. Locus ceruleus controls Alzheimer's disease pathology by modulating microglial functions through norepinephrine. Proc Natl Acad Sci U S A 107: 6058-6063, 2010.
28. Hickman SE, Allison EK, and El Khoury J. Microglial dysfunction and defective beta-Amyloid clearance pathways in aging Alzheimer's disease mice. J Neurosci 28: 8354-8360, 2008.
29. Hipkiss AR, Brownson C, and Carrier MJ. Carnosine, the anti-Ageing, anti-oxidant dipeptide, may react with protein carbonyl groups. Mech Ageing Dev 122: 1431-1445, 2001.
30. Hirano K, Kuwasako T, Nakagawa-Toyama Y, Janabi M, Yamashita S, and Matsuzawa Y. Pathophysiology of human genetic CD36 deficiency. Trends Cardiovasc Med 13: 136-141, 2003.
31. Hurttila H, Koponen JK, Kansanen E, Jyrkkänen HK, Kivela A, Kylätie R, Ylä-Herttuala S, and Levonen AL. Oxidative stress-inducible lentiviral vectors for gene therapy. Gene Ther 15: 1271-1279, 2008.
32. Ishii T, Itoh K, Ruiz E, Leake DS, Unoki H, Yamamoto M, and Mann GE. Role of Nrf2 in the regulation of CD36 and stress protein expression in murine macrophages: activation by oxidatively modified LDL and 4-hydroxynonenal. Circ Res 94: 609-616, 2004.
33. Itoh K, Chiba T, Takahashi S, Ishii T, Igarashi K, Katoh Y, Oyake T, Hayashi N, Satoh K, Hatayama I, Yamamoto M, and Nabeshima Y. An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem Biophys Res Commun 236: 313-322, 1997.
34. Kanninen K, Heikkinen R, Malm T, Rolova T, Kuhmonen S, Leinonen H, Ylä-Herttuala S, Tanila H, Levonen AL, Koistinaho M, and Koistinaho J. Intrahippocampal injection of a lentiviral vector expressing Nrf2 improves spatial learning in a mouse model of Alzheimer's disease. Proc Natl Acad Sci U S A 106: 16505-16510, 2009.
35. Kanninen K, Malm TM, Jyrkkänen HK, Goldsteins G, Keksa-Goldsteine V, Tanila H, Yamamoto M, Ylä-Herttuala S, Levonen AL, and Koistinaho J. Nuclear factor erythroid 2-related factor 2 protects against beta amyloid. Mol Cell Neurosci 39: 302-313, 2008.
36. Koponen JK, Kekarainen T, E Heinonen S, Laitinen A, Nystedt J, Laine J, and Ylä-Herttuala S. Umbilical cord blood-Derived progenitor cells enhance muscle regeneration in mouse hindlimb ischemia model. Mol Ther 15: 2172-2177, 2007.
37. Lee JM, Calkins MJ, Chan K, Kan YW, and Johnson JA. Identification of the NF-E2-related factor-2-Dependent genes conferring protection against oxidative stress in primary cortical astrocytes using oligonucleotide microarray analysis. J Biol Chem 278: 12029-12038, 2003.
38. Lee JM, Shih AY, Murphy TH, and Johnson JA. NF-E2-related factor-2 mediates neuroprotection against mitochondrial complex I inhibitors and increased concentrations of intracellular calcium in primary cortical neurons. J Biol Chem 278: 37948-37956, 2003.
39. Leissring MA, Farris W, Chang AY, Walsh DM, Wu X, Sun X, Frosch MP, and Selkoe DJ. Enhanced proteolysis of beta-Amyloid in APP transgenic mice prevents plaque formation, secondary pathology, and premature death. Neuron 40: 1087-1093, 2003.
40. Leuner K, Schütt T, Kurz C, Eckert SH, Schiller C, Occhipinti A, Mai S, Jendrach M, Eckert GP, Kruse SE, Palmiter RD, Brandt U, Drose S, Wittig I, Willem M, Haass C, Reichert AS, and Müller WE. Mitochondrion-Derived reactive oxygen species lead to enhanced amyloid beta formation. Antioxid Redox Signal 16: 1421-1433, 2012.
41. Levonen AL, Inkala M, Heikura T, Jauhiainen S, Jyrkkänen HK, Kansanen E, Maä K, Romppanen E, Turunen P, Rutanen J, and Ylä-Herttuala S. Nrf2 gene transfer induces antioxidant enzymes and suppresses smooth muscle cell growth in vitro and reduces oxidative stress in rabbit aorta in vivo. Arterioscler Thromb Vasc Biol 27: 741-747, 2007.
42. Li L, Zhang X, Yang D, Luo G, Chen S, and Le W. Hypoxia increases Abeta generation by altering beta-And gammacleavage of APP. Neurobiol Aging 30: 1091-1098, 2009.
43. Liu Y, Liu F, Iqbal K, Grundke-Iqbal I, and Gong CX. Decreased glucose transporters correlate to abnormal hyperphosphorylation of tau in Alzheimer disease. FEBS Lett 582: 359-364, 2008.
44. Maruyama A, Tsukamoto S, Nishikawa K, Yoshida A, Harada N, Motojima K, Ishii T, Nakane A, Yamamoto M, and Itoh K. Nrf2 regulates the alternative first exons of CD36 in macrophages through specific antioxidant response elements. Arch Biochem Biophys 477: 139-145, 2008.
45. Mattson MP. Cellular actions of beta-Amyloid precursor protein and its soluble and fibrillogenic derivatives. Physiol Rev 77: 1081-1132, 1997.
46. Mawuenyega KG, Sigurdson W, Ovod V, Munsell L, Kasten T, Morris JC, Yarasheski KE, and Bateman RJ. Decreased clearance of CNS beta-Amyloid in Alzheimer's disease. Science 330: 1774, 2010.
47. Mcmahon M, Itoh K, Yamamoto M, and Hayes JD. Keap1-Dependent proteasomal degradation of transcription factor Nrf2 contributes to the negative regulation of antioxidant response element-Driven gene expression. J Biol Chem 278: 21592-21600, 2003.
48. Meda L, Cassatella MA, Szendrei GI, Otvos L Jr., Baron P, Villalba M, Ferrari D, and Rossi F. Activation of microglial cells by beta-Amyloid protein and interferon-gamma. Nature 374: 647-650, 1995.
49. Olagnier D, Lavergne RA, Meunier E, Lefévre L, Dardenne C, Aubouy A, Benoit-Vical F, Ryffel B, Coste A, Berry A, and Pipy B. Nrf2, a PPARgamma alternative pathway to promote CD36 expression on inflammatory macrophages: implication for malaria. PLoS Pathog 7: e1002254, 2011.
50. Park L, Wang G, Zhou P, Zhou J, Pitstick R, Previti ML, Younkin L, Younkin SG, Van Nostrand WE, Cho S, Anrather J, Carlson GA, and Iadecola C. Scavenger receptor CD36 is essential for the cerebrovascular oxidative stress and neurovascular dysfunction induced by amyloid-beta. Proc Natl Acad Sci U S A 108: 5063-5068, 2011.
51. Patel SN, Lu Z, Ayi K, Serghides L, Gowda DC, and Kain KC. Disruption of CD36 impairs cytokine response to Plasmodium falciparum glycosylphosphatidylinositol and confers susceptibility to severe and fatal malaria in vivo. J Immunol 178: 3954-3961, 2007.
52. Peers C, Dallas ML, Boycott HE, Scragg JL, Pearson HA, and Boyle JP. Hypoxia and neurodegeneration. Ann N Y Acad Sci 1177: 169-177, 2009.
53. Peers C, Pearson HA, and Boyle JP. Hypoxia and Alzheimer's disease. Essays Biochem 43: 153-164, 2007.
54. Pialoux V, Mounier R, Brown AD, Steinback CD, Rawling JM, and Poulin MJ. Relationship between oxidative stress and HIF-1 alpha mRNA during sustained hypoxia in humans. Free Radic Biol Med 46: 321-326, 2009.
55. Qing H, He G, Ly PT, Fox CJ, Staufenbiel M, Cai F, Zhang Z, Wei S, Sun X, Chen CH, Zhou W, Wang K, and Song W. Valproic acid inhibits Abeta production, neuritic plaque formation, and behavioral deficits in Alzheimer's disease mouse models. J Exp Med 205: 2781-2789, 2008.
56. Querfurth HW and Laferla FM. Alzheimer's disease. N Engl J Med 362: 329-344, 2010.
57. Ramsey CP, Glass CA, Montgomery MB, Lindl KA, Ritson GP, Chia LA, Hamilton RL, Chu CT, and Jordan-Sciutto KL. Expression of Nrf2 in neurodegenerative diseases. J Neuropathol Exp Neurol 66: 75-85, 2007.
58. Sahin K, Tuzcu M, Gencoglu H, Dogukan A, Timurkan M, Sahin N, Aslan A, and Kucuk O. Epigallocatechin-3-gallate activates Nrf2/HO-1 signaling pathway in cisplatin-induced nephrotoxicity in rats. Life Sci 87: 240-245, 2010.
59. Sanchez A, Tripathy D, Yin X, Desobry K, Martinez J, Riley J, Gay D, Luo J, and Grammas P. p38 MAPK: a mediator of hypoxia-induced cerebrovascular inflammation. J Alzheimer's Dis 32: 587-597, 2012.
60. Schubert D, Soucek T, and Blouw B. The induction of HIF-1 reduces astrocyte activation by amyloid beta peptide. Eur J Neurosci 29: 1323-1334, 2009.
61. Selkoe DJ. Alzheimer's disease is a synaptic failure. Science 298: 789-791, 2002.
62. Semenza GL. HIF-1: mediator of physiological and pathophysiological responses to hypoxia. J Appl Physiol (1985) 88: 1474-1480, 2000.
63. Shao G, Gao CY, and Lu GW. Alterations of hypoxiainducible factor-1 alpha in the hippocampus of mice acutely and repeatedly exposed to hypoxia. Neurosignals 14: 255-261, 2005.
64. Silverstein RL and Febbraio M. CD36, a scavenger receptor involved in immunity, metabolism, angiogenesis, and behavior. Sci Signal 2: re3, 2009.
65. Skoog I and Gustafson D. Update on hypertension and Alzheimer's disease. Neurol Res 28: 605-611, 2006.
66. Stewart CR, Stuart LM, Wilkinson K, Van Gils JM, Deng J, Halle A, Rayner KJ, Boyer L, Zhong R, Frazier WA, Lacy-Hulbert A, El Khoury J, Golenbock DT, and Moore KJ. CD36 ligands promote sterile inflammation through assembly of a Toll-like receptor 4 and 6 heterodimer. Nat Immunol 11: 155-161, 2010.
67. Sun X, Erb H, and Murphy TH. Coordinate regulation of glutathione metabolism in astrocytes by Nrf2. Biochem Biophys Res Commun 326: 371-377, 2005.
68. Sun X, He G, Qing H, Zhou W, Dobie F, Cai F, Staufenbiel M, Huang LE, and Song W. Hypoxia facilitates Alzheimer's disease pathogenesis by up-regulating BACE1 gene expression. Proc Natl Acad Sci U S A 103: 18727-18732, 2006.
69. Sykiotis GP, Habeos IG, Samuelson AV, and Bohmann D. The role of the antioxidant and longevity-promoting Nrf2 pathway in metabolic regulation. Curr Opin Clin Nutr Metab Care 14: 41-48, 2011.
70. Tabner BJ, El-Agnaf OM, Turnbull S, German MJ, Paleologou KE, Hayashi Y, Cooper LJ, Fullwood NJ, and Allsop D. Hydrogen peroxide is generated during the very early stages of aggregation of the amyloid peptides impli-cated in Alzheimer disease and familial British dementia. J Biol Chem 280: 35789-35792, 2005.
71. Taylor CT. Mitochondria and cellular oxygen sensing in the HIF pathway. Biochem J 409: 19-26, 2008.
72. Wang CY, Xie JW, Wang T, Xu Y, Cai JH, Wang X, Zhao BL, An L, and Wang ZY. Hypoxia-triggered m-calpain activation evokes endoplasmic reticulum stress and neuropathogenesis in a transgenic mouse model of Alzheimer's disease. CNS Neurosci Ther 19: 820-833, 2013.
73. Wang CY, Xie JW, Xu Y, Wang T, Cai JH, Wang X, Zhao BL, An L, and Wang ZY. Trientine reduces BACE1 activity and mitigates amyloidosis via the AGE/RAGE/NFkappaB pathway in a transgenic mouse model of Alzheimer's disease. Antioxid Redox Signal 19: 2024-2039, 2013.
74. Wang J, Fields J, Zhao C, Langer J, Thimmulappa RK, Kensler TW, Yamamoto M, Biswal S, and Doré S. Role of Nrf2 in protection against intracerebral hemorrhage injury in mice. Free Radic Biol Med 43: 408-414, 2007.
75. Wild AC, Moinova HR, and Mulcahy RT. Regulation of gamma-glutamylcysteine synthetase subunit gene expression by the transcription factor Nrf2. J Biol Chem 274: 33627-33636, 1999.
76. Yamanaka M, Ishikawa T, Griep A, Axt D, Kummer MP, and Heneka MT. PPARgamma/RXRalpha-induced and CD36-mediated microglial amyloid-beta phagocytosis results in cognitive improvement in amyloid precursor protein/presenilin 1 mice. J Neurosci 32: 17321-17331, 2012.
77. Zhang X and Le W. Pathological role of hypoxia in Alzheimer's disease. Exp Neurol 223: 299-303, 2010.
78. Zhang X, Li L, Zhang X, Xie W, Li L, Yang D, Heng X, Du Y, Doody RS, and Le W. Prenatal hypoxia may aggravate the cognitive impairment and Alzheimer's disease neuropathology in APPSwe/PS1A246E transgenic mice. Neurobiol Aging 34: 663-678, 2013.