The up-regulation of BACE1 mediated by hypoxia and ischemic injury: Role of oxidative stress and HIF1α

Journal of Neurochemistry

Volumn 108, Issue 4, 2009, Pages 1045-1056

  Guglielmotto, Michela ^a   Aragno, Manuela ^a   Autelli, Riccardo ^a   Giliberto, Luca ^b   Novo, Erica ^a   Colombatto, Sebastiano ^a   Danni, Oliviero ^a   Parola, Maurizio ^a   Smith, Mark A ^c   Perry, George ^d   Tamagno, Elena ^a   Tabaton, Massimo ^b,e  

^a UNIVERSITY OF TURIN   (Italy)

^b UNIVERSITY OF GENOA   (Italy)

^c CASE WESTERN RESERVE UNIVERSITY   (United States)

^d University of San Antonio   (United States)

^e Department of Neurosciences ^*  (Italy)

Author keywords

site APP cleaving enzyme; Alzheimer' disease; Hypoxia; Hypoxia inducible factor 1 ; Neuroblastoma cells; Oxidative stress

Indexed keywords

AMYLOID BETA PROTEIN; BETA SECRETASE; BETA SECRETASE 1; DIPHENYLIODONIUM SALT; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MITOGEN ACTIVATED PROTEIN KINASE P38; REACTIVE OXYGEN METABOLITE; ROTENONE; STRESS ACTIVATED PROTEIN KINASE 1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ISCHEMIA; CONTROLLED STUDY; ENZYME ACTIVATION; HUMAN; HUMAN CELL; MALE; NERVE CELL DIFFERENTIATION; NERVE CELL NECROSIS; NEUROBLASTOMA CELL; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; RESPIRATORY CHAIN; UPREGULATION;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN; AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; ASPARTIC ENDOPEPTIDASES; BRAIN; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; ELECTRON TRANSPORT COMPLEX I; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; HYPOXIA-ISCHEMIA, BRAIN; ISOENZYMES; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MALE; OXIDATIVE STRESS; RATS; RATS, WISTAR; REACTIVE OXYGEN SPECIES; UNCOUPLING AGENTS; UP-REGULATION;

RATTUS;

EID: 58549119790     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2008.05858.x     Document Type: Article

References (60)

1. 2-sensing pathway at the intersection of pulmonary hypertension and cancer. Am. J. Physiol. Heart Circ. Physiol. 294, H570 H578.
2. Arumugam T. V., Chan S. L., Jo D. G. et al. (2006) Gamma secretase-mediated Notch signaling worsens brain damage and functional outcome in ischemic stroke. Nature Med. 12, 621 623.
3. Bell E. L., Klimova T. A., Eisenbart J., Moraes C. T., Murphy M. P., Budinger G. R. Chandel N. S. (2007) 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.
4. Benjannet S., Elagoz A., Wickham L. et al. (2001) Post-translational processing of beta-secretase (beta-amyloid-converting enzyme) and its ectodomain shedding. The pro- and transmembrane/cytosolic domains affect its cellular activity and amyloid-beta production. J. Biol. Chem. 276, 10879 10887.
5. Borghi R., Patriarca S., Traverso N., Piccini A., Storace D., Garuti A., Cirmena G., Odetti P. Tabaton M. (2007) The increased activity of BACE1 correlates with oxidative stress in Alzheimer's disease. Neurobiol. Aging 28, 1009 1014.
6. Braak H., Braak E. Bohl J. (1993) Staging of Alzheimer-related cortical destruction. Eur. Neurol. 33, 403 408.
7. Chandel N. S., Maltepe E., Goldwasser E., Mathieu C. E., Simon M. C. Schumacker P. T. (1998) Mitochondrial reactive oxygen species trigger hypoxia-induced transcription. Proc. Natl Acad. Sci. USA 95, 11715 11720.
8. 2 sensing. J. Biol. Chem. 275, 25130 25138.
9. Chu K., Jung K. H., Kim S. J. et al. (2008) Transplantation of human neural stem cells protect against ischemia in a preventive mode via hypoxia-inducible factor-1alpha stabilization in the host brain. Brain Res. 1207, 182 192.
10. Collino M., Aragno M., Mastrocola R., Gallicchio M., Rosa A. C., Dianzani C., Danni O., Thiemermann C. Fantozzi R. (2006) Modulation of the oxidative stress and inflammatory response by PPAR gamma agonists in the hippocampus of rats exposed to cerebral ischemia/reperfusion. Eur. J. Pharmacol. 530, 70 80.
11. Faghihi M. A., Modarresi F., Khalil A. M., Wood D. E., Sahagan B. G., Morgan T. E., Finch C. E., St Laurent G. 3rd., Kenny P. J. Wahlestedt C. (2008) Expression of a noncoding RNA is elevated in Alzheimer's disease and drives rapid feed-forward regulation of beta-secretase. Nature Med. 14, 723 730.
12. Ferreiro E., Resende R., Costa R., Oliveira C. R. Pereira C. M. (2006) An endoplasmic-reticulum-specific apoptotic pathway is involved in prion and amyloid-beta peptides neurotoxicity. Neurobiol. Dis. 23, 669 678.
13. Fukumoto H., Cheung B. S., Hyman B. T. Irizarry M. C. (2002) Beta-secretase protein and activity are increased in the neocortex in Alzheimer disease. Arch. Neurol. 59, 1381 1389.
14. Guzy R. D. Schumacker P. T. (2006) Oxygen sensing by mitochondria at complex III: the paradox of increased reactive oxygen species during hypoxia. Exp. Physiol. 91, 807 819.
15. Hardy J. (2006) Alzheimer's disease: the amyloid cascade hypothesis: an update and reappraisal. J. Alzheimers Dis. 9, 151 153.
16. Hirai K., Aliev G., Nunomura A. et al. (2001) Mitochondrial abnormalities in Alzheimer's disease. J. Neurosci. 21, 3017 3023.
17. Holsinger R. M., McLean C. A., Beyreuther K., Masters C. L. Evin G. (2002) Increased expression of the amyloid precursor beta-secretase in Alzheimer's disease. Ann. Neurol. 51, 783 786.
18. Jellinger K. A. (1998) The neuropathological diagnosis of Alzheimer disease. J. Neural Transm. Suppl. 53, 97 118.
19. Jo D. G., Arumugam T. V., Woo H. N. et al. (2008) Evidence that γ-secretase mediates oxidative stress-induced β-secretase expression in Alzheimer's disease. Neurobiol. Aging [Epub ahead of print] doi :.
20. Kao S. C., Krichevsky A. M., Kosik K. S. Tsai L. H. (2004) BACE1 suppression by RNA interference in primary cortical neurons. J. Biol. Chem. 279, 1942 1949.
21. Lage J. M. (2006) 100 years of Alzheimer's disease (1906-2006). J. Alzheimers Dis. 9, 15 26.
22. Li Y. Trush M. A. (1998) Diphenyleniodonium, an NAD(P)H oxidase inhibitor, also potently inhibits mitochondrial reactive oxygen species production. Biochem. Biophys. Res. Commun. 253, 295 299.
23. Li R., Lindholm K., Yang L. B. et al. (2004) Amyloid beta peptide load is correlated with increased beta-secretase activity in sporadic Alzheimer's disease patients. Proc. Natl Acad. Sci. USA 101, 3632 3637.
24. Li L., Zhang X., Yang D., Luo G., Chen S. Le W. (2007) Hypoxia increases Aβ generation by altering β- and γ-cleavage of APP. Neurobiol. Aging [Epub ahead of print] doi :.
25. Mattson M. P. (2002) Oxidative stress, perturbed calcium homeostasis, and immune dysfunction in Alzheimer's disease. J. Neurovirol. 8, 539 550.
26. Meldrum D. R., Shenkar R., Sheridan B. C., Cain B. S., Abraham E. Harken A. H. (1997) Hemorrhage activates myocardial NFkappaB and increases TNF-alpha in the heart. J. Mol. Cell. Cardiol. 29, 2849 2854.
27. Mowrer K. R. Wolfe M. S. (2008) Promotion of BACE1 mRNA alternative splicing reduces amyloid beta-peptide production. J. Biol. Chem. 283, 18694 18701.
28. Murphy M. P., Hickman L. J., Eckman C. B., Uljon S. N., Wang R. Golde T. E. (1999) Gamma-secretase, evidence for multiple proteolytic activities and influence of membrane positioning of substrate on generation of amyloid beta peptides of varying length. J. Biol. Chem. 274, 11914 11923.
29. Pasternak S. H., Callahan J. W. Mahuran D. J. (2004) The role of the endosomal/lysosomal system in amyloid-beta production and the pathophysiology of Alzheimer's disease: reexamining the spatial paradox from a lysosomal perspective. J. Alzheimers Dis. 6, 53 65.
30. Pickford F., Masliah E., Britschgi M. et al. (2008) The autophagy-related protein beclin 1 shows reduced expression in early Alzheimer disease and regulates amyloid beta accumulation in mice. J. Clin. Invest. 118, 2190 2199.
31. Reddy P. H. Beal M. F. (2005) Are mitochondria critical in the pathogenesis of Alzheimer's disease? Brain Res. Brain Res. Rev. 49, 618 632.
32. Rezvani H. R., Dedieu S., North S., Belloc F., Rossignol R., Letellier T., de Verneuil H., Taïeb A. Mazurier F. (2007) Hypoxia-inducible factor-1alpha, a key factor in the keratinocyte response to UVB exposure. J. Biol. Chem. 282, 16413 16422.
33. Roberds S. L., Anderson J., Basi G. et al. (2001) BACE knockout mice are healthy despite lacking the primary beta-secretase activity in brain: implications for Alzheimer's disease therapeutics. Hum. Mol. Genet. 10, 1317 1324.
34. Schaeffer E. L. Gattaz W. F. (2008) Cholinergic and glutamatergic alterations beginning at the early stages of Alzheimer disease: participation of the phospholipase A(2) enzyme. Psychopharmacology 198, 1 27.
35. Selkoe D. J. (2001) Alzheimer's disease results from the cerebral accumulation and cytotoxicity of amyloid beta-protein. J. Alzheimers Dis. 3, 75 80.
36. Sharp F. R. Bernaudin M. (2004) HIF1 and oxygen sensing in the brain. Nat. Rev. Neurosci. 5, 437 448.
37. Stockley J. H. O'Neill C. (2007) The proteins BACE1 and BACE2 and beta-secretase activity in normal and Alzheimer's disease brain. Biochem. Soc. Trans. 35, 574 576.
38. Sun J. Trumpower B. L. (2003) Superoxide anion generation by the cytochrome bc1 complex. Arch. Biochem. Biophys. 419, 198 206.
39. Sun X., He G., Qing H., Zhou W., Dobie F., Cai F., Staufenbiel M., Huang L. E. Song W. (2006) Hypoxia facilitates Alzheimer's disease pathogenesis by up-regulating BACE1 gene expression. Proc. Natl Acad. Sci. USA 103, 18727 18732.
40. Tahirovic I., Sofic E., Sapcanin A., Gavrankapetanovic I., Bach-Rojecky L., Salkovic-Petrisic M., Lackovic Z., Hoyer S. Riederer P. (2007) Brain antioxidant capacity in rat models of betacytotoxic-induced experimental sporadic Alzheimer's disease and diabetes mellitus. J. Neural Transm. Suppl. 72, 235 240.
41. Tamagno E., Bardini P., Obbili A. et al. (2002) Oxidative stress increases expression and activity of BACE in NT2 neurons. Neurobiol. Dis. 10, 279 288.
42. 2 and 4-hydroxynonenal mediate amyloid beta-induced neuronal apoptosis by activating JNKs and p38MAPK. Exp. Neurol. 180, 144 155.
43. Tamagno E., Parola M., Bardini P. et al. (2005) Beta-site APP cleaving enzyme up-regulation induced by 4-hydroxynonenal is mediated by stress-activated protein kinases pathways. J. Neurochem. 92, 628 636.
44. Tamagno E., Guglielmotto M., Aragno M. et al. (2008a) Oxidative stress activates a positive feedback between the gamma- and beta-secretase cleavages of the beta-amyloid precursor protein. J. Neurochem. 104, 683 695.
45. Tamagno E., Guglielmotto M., Giliberto L., Vitali A., Borghi R., Autelli R., Danni O. Tabaton M. (2008b) JNK and ERK1/2 pathways have a dual opposite effect on the expression of BACE1. Neurobiol. Aging [Epub ahead of print] doi :.
46. Tesco G., Koh Y. H., Kang E. L. et al. (2007) Depletion of GGA3 stabilizes BACE and enhances beta-secretase activity. Neuron 54, 721 737.
47. Thakur A., Wang X., Siedlak S. L., Perry G., Smith M. A. Zhu X. (2007) c-Jun phosphorylation in Alzheimer disease. J. Neurosi. Res. 85, 1668 16673.
48. de la Torre J. C. (2008) Alzheimer's disease prevalence can be lowered with non-invasive testing. J Alzheimers Dis. 14, 353 359.
49. Turrens J. F. (2003) Mitochondrial formation of reactive oxygen species. J. Physiol. 552, 335 344.
50. Tyler S. J., Dawbarn D., Wilcock G. K. Allen S. J. (2002) Alpha- and beta-secretase: profound changes in Alzheimer's disease. Biochem. Biophys. Res. Commun. 299, 373 376.
51. Vassar R., Bennett B. D., Babu-Khan S. et al. (1999) Beta-secretase cleavage of Alzheimer's amyloid precursor protein by the transmembrane aspartic protease BACE. Science 286, 735 741.
52. Wallace D. C. (2001) Mouse models for mitochondrial disease. Am. J. Med. Genet. 106, 71 793.
53. Wang R., Zhang Y. W., Zhang X., Liu R., Zhang X., Hong S., Xia K., Xia J., Zhang Z. Xu H. (2006) Transcriptional regulation of APH-1A and increased gamma-secretase cleavage of APP and Notch by HIF-1 and hypoxia. FASEB J. 20, 1275 1277.
54. Yang L. B., Lindholm K., Yan R. et al. (2003) Elevated beta-secretase expression and enzymatic activity detected in sporadic Alzheimer disease. Nat. Med. 9, 3 4.
55. Yao S.-Y., Soutto M. Sriram S. (2008) Bacterial cell wall products increases stabilization of HIF-1 alpha in an oligodendrocyte cell line preconditioned by cobalt chloride or desferrioxamine. J. Neuroimmunol. 200, 17 26.
56. Yu W. H., Kumar A., Peterhoff C., Shapiro Kulnane L., Uchiyama Y., Lamb B. T., Cuervo A. M. Nixon R. A. (2004) Autophagic vacuoles are enriched in amyloid precursor protein-secretase activities: implications for beta-amyloid peptide over-production and localization in Alzheimer's disease. Int. J. Biochem. Cell Biol. 36, 2531 2540.
57. Yu W. H., Cuervo A. M., Kumar A. et al. (2005) Macroautophagy - a novel beta-amyloid peptide-generating pathway activated in Alzheimer's disease. J. Cell Biol. 171, 87 98.
58. Zhang X., Zhou K., Wang R., Cui J., Lipton S. A., Liao F. F., Xu H. Zhang Y. W. (2007) Hypoxia inducible factor 1alpha (HIF-1alpha)-mediated hypoxia increases BACE1 expression and beta-amyloid generation. J. Biol. Chem. 282, 10873 10880.
59. Zhu X., Sun Z., Lee H. G., Siedlak S. L., Perry G. Smith M. A. (2003) Distribution, levels, and activation of MEK1 in Alzheimer's disease. J. Neurochem. 86, 136 142.
60. Zhu X., Raina A. K., Perry G. Smith M. A. (2004) Alzheimer's disease: the two-hit hypothesis. Lancet Neurol. 3, 219 226.