Intranasal deferoxamine attenuates synapse loss via up-regulating the P38/HIF-1α pathway on the brain of APP/PS1 transgenic mice

Frontiers in Aging Neuroscience

Volumn 7, Issue JUN, 2015, Pages

  Guo, Chuang ^a   Zhang, Yu Xin ^b   Wang, Tao ^a   Zhong, Man Li ^a   Yang, Zhao Hui ^a   Hao, Li Juan ^a   Chai, Rui ^a   Zhang, Shuai ^a  

^a NORTHEASTERN UNIVERSITY   (China)

^b HEBEI UNITED UNIVERSITY   (China)

Author keywords

Alzheimer's disease; Deferoxamine; Hypoxia inducible factor; Iron; Synapse; Transgenic mouse

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; BRAIN DERIVED NEUROTROPHIC FACTOR; DEFEROXAMINE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; IRON; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE P38; NATURAL RESISTANCE ASSOCIATED MACROPHAGE PROTEIN 2; PRESENILIN 1; TRANSFERRIN RECEPTOR;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL LOSS; CONTROLLED STUDY; DRUG EFFICACY; FENTON REACTION; GENE EXPRESSION REGULATION; HIF ALPHA GENE; HIPPOCAMPAL CA3 REGION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR SIGNALING; MALE; MOUSE; NERVE CELL NECROSIS; NEUROBLASTOMA CELL LINE; NEUROPROTECTION; NONHUMAN; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS INHIBITION; SYNAPSE; TRANSGENIC MOUSE; WESTERN BLOTTING;

EID: 84936118142     PISSN: None     EISSN: 16634365     Source Type: Journal    
DOI: 10.3389/fnagi.2015.00104     Document Type: Article

References (55)

1. Atkins, C. M., Selcher, J. C., Petraitis, J. J., Trzaskos, J. M., and Sweatt, J. D. (1998). The MAPK cascade is required for mammalian associative learning. Nat. Neurosci. 1, 602-609. doi: 10.1038/2836
2. Avramovich-Tirosh, Y., Bar-Am, O., Amit, T., Youdim, M. B., and Weinreb, O. (2010). Up-regulation of hypoxia-inducible factor (HIF)-1alpha and HIF-target genes in cortical neurons by the novel multifunctional iron chelator anti-Alzheimer drug, M30. Curr. Alzheimer Res. 7, 300-306. doi: 10.2174/156720510791162403
3. Bandyopadhyay, S., Huang, X., Lahiri, D. K., and Rogers, J. T. (2010). Novel drug targets based on metallobiology of Alzheimer's disease. Expert Opin. Ther. Targets 14, 1177-1197. doi: 10.1517/14728222.2010.525352
4. Bergeron, M., Yu, A. Y., Solway, K. E., Semenza, G. L., and Sharp, F. R. (1999). Induction of hypoxia-inducible factor-1 (HIF-1) and its target genes following focal ischaemia in rat brain. Eur. J. Neurosci. 11, 4159-4170. doi: 10.1046/j.1460-9568.1999.00845.x
5. Bianchi, L., Tacchini, L., and Cairo, G. (1999). HIF-1-mediated activation of transferrin receptor gene transcription by iron chelation. Nucleic Acids Res. 27, 4223-4227. doi: 10.1093/nar/27.21.4223
6. Blancher, C., Moore, J. W., Robertson, N., and Harris, A. L. (2001). Effects of ras and von Hippel-Lindau (VHL) gene mutations on hypoxia-inducible factor (HIF)-1alpha, HIF-2alpha and vascular endothelial growth factor expression and their regulation by the phosphatidylinositol 3′-kinase/Akt signaling pathway. Cancer Res. 61, 7349-7355.
7. Cho, H. J., Kim, S. K., Jin, S. M., Hwang, E. M., Kim, Y. S., Huh, K., et al. (2007). IFN-gamma-induced BACE1 expression is mediated by activation of JAK2 and ERK1/2 signaling pathways and direct binding of STAT1 to BACE1 promoter in astrocytes. Glia 55, 253-262. doi: 10.1002/glia.20451
8. Crapper McLachlan, D. R., Dalton, A. J., Kruck, T. P., Bell, M. Y., Smith, W. L., Kalow, W., et al. (1991). Intramuscular desferrioxamine in patients with alzheimer's disease. Lancet 337, 1304-1308. doi: 10.1016/0140-6736(91)92978-b
9. Cuajungco, M. P., Fagét, K. Y., Huang, X., Tanzi, R. E., and Bush, A. I. (2000). Metal chelation as a potential therapy for alzheimer's disease. Ann. N Y Acad. Sci. 920, 292-304. doi: 10.1111/j.1749-6632.2000.tb06938.x
10. de Lima, M. N., Dias, C. P., Torres, J. P., Dornelles, A., Garcia, V. A., Scalco, F. S., et al. (2008). Reversion of age-related recognition memory impairment by iron chelation in rats. Neurobiol. Aging 29, 1052-1059. doi: 10.1016/j.neurobiolaging.2007.02.006
11. Epstein, A. C., Gleadle, J. M., McNeill, L. A., Hewitson, K. S., O'Rourke, J., Mole, D. R., et al. (2001). C. elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell 107, 43-54. doi: 10.1016/S0092-8674(01)00507-4
12. Fine, J. M., Baillargeon, A. M., Renner, D. B., Hoerster, N. S., Tokarev, J., Colton, S., et al. (2012). Intranasal deferoxamine improves performance in radial arm water maze, stabilizes HIF-1alpha and phosphorylates GSK3beta in P301L tau transgenic mice. Exp. Brain Res. 219, 381-390. doi: 10.1007/s00221-012-3101-0
13. Guo, C., Wang, T., Zheng, W., Shan, Z. Y., Teng, W. P., and Wang, Z. Y. (2013a). Intranasal deferoxamine reverses iron-induced memory deficits and inhibits amyloidogenic APP processing in a transgenic mouse model of Alzheimer's disease. Neurobiol. Aging 34, 562-575. doi: 10.1016/j.neurobiolaging.2012.05.009
14. Guo, C., Wang, P., Zhong, M. L., Wang, T., Huang, X. S., Li, J. Y., et al. (2013b). Deferoxamine inhibits iron induced hippocampal tau phosphorylation in the Alzheimer transgenic mouse brain. Neurochem. Int. 62, 165-172. doi: 10.1016/j.neuint.2012.12.005
15. Haleagrahara, N., Siew, C. J., and Ponnusamy, K. (2013). Effect of quercetin and desferrioxamine on 6-hydroxydopamine (6-OHDA) induced neurotoxicity in striatum of rats. J. Toxicol. Sci. 38, 25-33. doi: 10.2131/jts.38.25
16. Hanson, L. R., Roeytenberg, A., Martinez, P. M., Coppes, V. G., Sweet, D. C., Rao, R. J., et al. (2009). Intranasal deferoxamine provides increased brain exposure and significant protection in rat ischemic stroke. J. Pharmacol. Exp. Ther. 330, 679-686. doi: 10.1124/jpet.108.149807
17. Honda, K., Smith, M. A., Zhu, X., Baus, D., Merrick, W. C., Tartakoff, A. M., et al. (2005). Ribosomal RNA in alzheimer disease is oxidized by bound redox-active iron. J. Biol. Chem. 280, 20978-20986. doi: 10.1074/jbc.m500526200
18. Ivan, M., Kondo, K., Yang, H., Kim, W., Valiando, J., Ohh, M., et al. (2001). HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing. Science 292, 464-468. doi: 10.1126/science.1059817
19. Jaakkola, P., Mole, D. R., Tian, Y. M., Wilson, M. I., Gielbert, J., Gaskell, S. J., et al. (2001). Targeting of HIF-alpha to the von hippel-lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science 292, 468-472. doi: 10.1126/science.1059796
20. Jiang, B. H., Jiang, G., Zheng, J. Z., Lu, Z., Hunter, T., and Vogt, P. K. (2001). Phosphatidylinositol 3-kinase signaling controls levels of hypoxia-inducible factor 1. Cell Growth Differ. 12, 363-369.
21. Kim, S. K., Park, H. J., Hong, H. S., Baik, E. J., Jung, M. W., and Mook-Jung, I. (2006). ERK1/2 is an endogenous negative regulator of the gamma-secretase activity. FASEB J. 20, 157-159. doi: 10.1096/fj.05-4055fje
22. Lando, D., Peet, D. J., Whelan, D. A., Gorman, J. J., and Whitelaw, M. L. (2002). Asparagine hydroxylation of the HIF transactivation domain a hypoxic switch. Science 295, 858-861. doi: 10.1126/science.1068592
23. Lee, D. W., and Andersen, J. K. (2006). Role of HIF-1 in iron regulation: potential therapeutic strategy for neurodegenerative disorders. Curr. Mol. Med. 6, 883-893. doi: 10.2174/156652406779010849
24. Lee, P. J., Jiang, B. H., Chin, B. Y., Iyer, N. V., Alam, J., Semenza, G. L., et al. (1997). Hypoxia-inducible factor-1 mediates transcriptional activation of the heme oxygenase-1 gene in response to hypoxia. J. Biol. Chem. 272, 5375-5381. doi: 10.1074/jbc.272.9.5375
25. Lee, J. W., Lee, Y. K., Ban, J. O., Ha, T. Y., Yun, Y. P., Han, S. B., et al. (2009). Green tea (-)-epigallocatechin-3-gallate inhibits beta-amyloid-induced cognitive dysfunction through modification of secretase activity via inhibition of ERK and NF-kappaB pathways in mice. J. Nutr. 139, 1987-1993. doi: 10.3945/jn.109.109785
26. Li, J., Davidson, G., Huang, Y., Jiang, B. H., Shi, X., Costa, M., et al. (2004). Nickel compounds act through phosphatidylinositol-3-kinase/Akt-dependent, p70(S6k)-independent pathway to induce hypoxia inducible factor transactivation and Cap43 expression in mouse epidermal Cl41 cells. Cancer Res. 64, 94-101. doi: 10.1158/0008-5472.can-03-0737
27. Lim, H. J., Shim, S. B., Jee, S. W., Lee, S. H., Lim, C. J., Hong, J. T., et al. (2013). Green tea catechin leads to global improvement among Alzheimer's disease-related phenotypes in NSE/hAPP-C105 Tg mice. J. Nutr. Biochem. 24, 1302-1313. doi: 10.1016/j.jnutbio.2012.10.005
28. Lonati, E., Brambilla, A., Milani, C., Masserini, M., Palestini, P., and Bulbarelli, A. (2014). Pin1, a new player in the fate of HIF-1alpha degradation: an hypothetical mechanism inside vascular damage as Alzheimer's disease risk factor. Front. Cell. Neurosci. 8:1. doi: 10.3389/fncel.2014.00001
29. Mecklenburgh, K. I., Walmsley, S. R., Cowburn, A. S., Wiesener, M., Reed, B. J., Upton, P. D., et al. (2002). Involvement of a ferroprotein sensor in hypoxia-mediated inhibition of neutrophil apoptosis. Blood 100, 3008-3016. doi: 10.1182/blood-2002-02-0454
30. Migliore, L., and Coppedè, F. (2009). Environmental-induced oxidative stress in neurodegenerative disorders and aging. Mutat. Res. 674, 73-84. doi: 10.1016/j.mrgentox.2008.09.013
31. Moreira, P. I., Sayre, L. M., Zhu, X., Nunomura, A., Smith, M. A., and Perry, G. (2010). Detection and localization of markers of oxidative stress by in situ methods: application in the study of Alzheimer disease. Methods Mol. Biol. 610, 419-434. doi: 10.1007/978-1-60327-029-8_25
32. Morse, L. J., Payton, S. M., Cuny, G. D., and Rogers, J. T. (2004). FDA-preapproved drugs targeted to the translational regulation and processing of the amyloid precursor protein. J. Mol. Neurosci. 24, 129-136. doi: 10.1385/jmn:24:1:129
33. Reznichenko, L., Amit, T., Zheng, H., Avramovich-Tirosh, Y., Youdim, M. B., Weinreb, O., et al. (2006). Reduction of iron-regulated amyloid precursor protein and beta-amyloid peptide by (-)-epigallocatechin-3-gallate in cell cultures: implications for iron chelation in Alzheimer's disease. J. Neurochem. 97, 527-536. doi: 10.1111/j.1471-4159.2006.03770.x
34. Rolfs, A., Kvietikova, I., Gassmann, M., and Wenger, R. H. (1997). Oxygen-regulated transferrin expression is mediated by hypoxia-inducible factor-1. J. Biol. Chem. 272, 20055-20062. doi: 10.1074/jbc.272.32.20055
35. Roux, P. P., and Blenis, J. (2004). ERK and p38 MAPK-activated protein kinases: a family of protein kinases with diverse biological functions. Microbiol. Mol. Biol. Rev. 68, 320-344. doi: 10.1128/mmbr.68.2.320-344.2004
36. Ruscher, K., Freyer, D., Karsch, M., Isaev, N., Megow, D., Sawitzki, B., et al. (2002). Erythropoietin is a paracrine mediator of ischemic tolerance in the brain: evidence from an in vitro model. J. Neurosci. 22, 10291-10301.
37. Savage, M. J., Lin, Y. G., Ciallella, J. R., Flood, D. G., and Scott, R. W. (2002). Activation of c-Jun N-terminal kinase and p38 in an Alzheimer's disease model is associated with amyloid deposition. J. Neurosci. 22, 3376-3385.
38. Savory, J., Huang, Y., Wills, M. R., and Herman, M. M. (1998). Reversal by desferrioxamine of tau protein aggregates following two days of treatment in aluminum-induced neurofibrillary degeneration in rabbit: implications for clinical trials in Alzheimer's disease. Neurotoxicology 19, 209-214.
39. Schaeffer, H. J., and Weber, M. J. (1999). Mitogen-activated protein kinases: specific messages from ubiquitous messengers. Mol. Cell. Biol. 19, 2435-2444.
40. Schinder, A. F., and Poo, M. (2000). The neurotrophin hypothesis for synaptic plasticity. Trends Neurosci. 23, 639-645. doi: 10.1016/s0166-2236(00)01672-6
41. Schubert, D., and Chevion, M. (1995). The role of iron in beta amyloid toxicity. Biochem. Biophys. Res. Commun. 216, 702-707. doi: 10.1006/bbrc.1995.2678
42. Schubert, D., Soucek, T., and Blouw, B. (2009). The induction of HIF-1 reduces astrocyte activation by amyloid beta peptide. Eur. J. Neurosci. 29, 1323-1334. doi: 10.1111/j.1460-9568.2009.06712.x
43. Semenza, G. L. (1998). Hypoxia-inducible factor 1, master regulator of O2 homeostasis. Curr. Opin. Genet. Dev. 8, 588-594. doi: 10.1016/s0959-437x(98)80016-6
44. Semenza, G. L. (1999). Regulation of mammalian O2 homeostasis by hypoxia-inducible factor 1. Annu. Rev. Cell Dev. Biol. 15, 551-578. doi: 10.1146/annurev.cellbio.15.1.551
45. Siddiq, A., Ayoub, I. A., Chavez, J. C., Aminova, L., Shah, S., LaManna, J. C., et al. (2005). Hypoxia-inducible factor prolyl 4-hydroxylase inhibition. A target for neuroprotection in the central nervous system. J. Biol. Chem. 280, 41732-41743. doi: 10.1074/jbc.m504963200
46. Soucek, T., Cumming, R., Dargusch, R., Maher, P., and Schubert, D. (2003). The regulation of glucose metabolism by HIF-1 mediates a neuroprotective response to amyloid beta peptide. Neuron 39, 43-56. doi: 10.1016/s0896-6273(03)00367-2
47. Tacchini, L., Gammella, E., De Ponti, C., Recalcati, S., and Cairo, G. (2008). Role of HIF-1 and NF-kappaB transcription factors in the modulation of transferrin receptor by inflammatory and anti-inflammatory signals. J. Biol. Chem. 283, 20674-20686. doi: 10.1074/jbc.M800365200
48. Thoenen, H. (1995). Neurotrophins and neuronal plasticity. Science 270, 593-598. doi: 10.1126/science.270.5236.593
49. Thoenen, H. (2000). Neurotrophins and activity-dependent plasticity. Prog. Brain Res. 128, 183-191. doi: 10.1016/s0079-6123(00)28016-3
50. Wang, G. L., Jiang, B. H., Rue, E. A., and Semenza, G. L. (1995). Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension. Proc. Natl. Acad. Sci. U S A 92, 5510-5514. doi: 10.1073/pnas.92.12.5510
51. Weinreb, O., Amit, T., and Youdim, M. B. (2008). The application of proteomics for studying the neurorescue activity of the polyphenol (-)-epigallocatechin-3-gallate. Arch. Biochem. Biophys. 476, 152-160. doi: 10.1016/j.abb.2008.01.004
52. Yue, P., Tao, T., Zhao, Y., Ren, J., and Chai, X. (2007). Huperzine A in rat plasma and CSF following intranasal administration. Int. J. Pharm. 337, 127-132. doi: 10.1016/j.ijpharm.2006.12.029
53. Zaman, K., Ryu, H., Hall, D., O'Donovan, K., Lin, K. I., Miller, M. P., et al. (1999). Protection from oxidative stress-induced apoptosis in cortical neuronal cultures by iron chelators is associated with enhanced DNA binding of hypoxia-inducible factor-1 and ATF-1/CREB and increased expression of glycolytic enzymes, p21(waf1/cip1) and erythropoietin. J. Neurosci. 19, 9821-9830.
54. Zecca, L., Youdim, M. B., Riederer, P., Connor, J. R., and Crichton, R. R. (2004). Iron, brain ageing and neurodegenerative disorders. Nat. Rev. Neurosci. 5, 863-873. doi: 10.1038/nrn1537
55. Zelzer, E., Levy, Y., Kahana, C., Shilo, B. Z., Rubinstein, M., and Cohen, B. (1998). Insulin induces transcription of target genes through the hypoxia-inducible factor HIF-1alpha/ARNT. EMBO J. 17, 5085-5094. doi: 10.1093/emboj/17.17.5085