Leptin attenuates BACE1 expression and amyloid-β genesis via the activation of SIRT1 signaling pathway

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1842, Issue 9, 2014, Pages 1587-1595

  Marwarha, Gurdeep ^a   Raza, Shaneabbas ^a   Meiers, Craig ^a   Ghribi, Othman ^a  

^a UNIVERSITY OF NORTH DAKOTA   (United States)

Author keywords

Alzheimer's disease; Amyloid ; BACE 1; Leptin; NF B; SIRT1

Indexed keywords

AMYLOID BETA PROTEIN; BETA SECRETASE 1; LEPTIN; SIRTUIN 1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; SYNAPTOTAGMIN I;

ACETYLATION; ARTICLE; ATTENUATION; CONTROLLED STUDY; DEACETYLATION; ENZYME LINKED IMMUNOSORBENT ASSAY; HOMOGENATE; HUMAN; HUMAN CELL; NEUROBLASTOMA CELL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; UBIQUITINATION; WESTERN BLOTTING;

ALZHEIMER'S DISEASE; AMYLOID-Β; BACE-1; LEPTIN; NF-ΚB; SIRT1;

AMYLOID BETA-PEPTIDES; AMYLOID PRECURSOR PROTEIN SECRETASES; ASPARTIC ACID ENDOPEPTIDASES; BLOTTING, WESTERN; CHROMATIN IMMUNOPRECIPITATION; ENZYME-LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LEPTIN; NEUROBLASTOMA; NF-KAPPA B; PROMOTER REGIONS, GENETIC; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNAL TRANSDUCTION; SIRTUIN 1; TUMOR CELLS, CULTURED;

EID: 84903851215     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2014.05.015     Document Type: Article

References (75)

1. Tanzi R.E., Bertram L. Twenty years of the Alzheimer's disease amyloid hypothesis: a genetic perspective. Cell 2005, 120:545-555.
2. Forman M.S., Trojanowski J.Q., Lee V.M. Neurodegenerative diseases: a decade of discoveries paves the way for therapeutic breakthroughs. Nat. Med. 2004, 10:1055-1063.
3. Selkoe D.J. Cell biology of protein misfolding: the examples of Alzheimer's and Parkinson's diseases. Nat. Cell Biol. 2004, 6:1054-1061.
4. Kaeberlein M., McVey M., Guarente L. The SIR2/3/4 complex and SIR2 alone promote longevity in Saccharomyces cerevisiae by two different mechanisms. Genes Dev. 1999, 13:2570-2580.
5. Imai S., Armstrong C.M., Kaeberlein M., Guarente L. Transcriptional silencing and longevity protein Sir2 is an NAD-dependent histone deacetylase. Nature 2000, 403:795-800.
6. Anderson R.M., Bitterman K.J., Wood J.G., Medvedik O., Sinclair D.A. Nicotinamide and PNC1 govern lifespan extension by calorie restriction in Saccharomyces cerevisiae. Nature 2003, 423:181-185.
7. Anderson R.M., Latorre-Esteves M., Neves A.R., Lavu S., Medvedik O., Taylor C., et al. Yeast life-span extension by calorie restriction is independent of NAD fluctuation. Science 2003, 302:2124-2126.
8. Cohen H.Y., Miller C., Bitterman K.J., Wall N.R., Hekking B., Kessler B., et al. Calorie restriction promotes mammalian cell survival by inducing the SIRT1 deacetylase. Science 2004, 305:390-392.
9. Luo J., Nikolaev A.Y., Imai S., Chen D., Su F., Shiloh A., et al. Negative control of p53 by Sir2alpha promotes cell survival under stress. Cell 2001, 107:137-148.
10. Picard F., Kurtev M., Chung N., Topark-Ngarm A., Senawong T., Machado De O.R., et al. Sirt1 promotes fat mobilization in white adipocytes by repressing PPAR-gamma. Nature 2004, 429:771-776.
11. Li X., Zhang S., Blander G., Tse J.G., Krieger M., Guarente L. SIRT1 deacetylates and positively regulates the nuclear receptor LXR. Mol. Cell 2007, 28:91-106.
12. Chen J., Zhou Y., Mueller-Steiner S., Chen L.F., Kwon H., Yi S., et al. SIRT1 protects against microglia-dependent amyloid-beta toxicity through inhibiting NF-kappaB signaling. J. Biol. Chem. 2005, 280:40364-40374.
13. Kaltschmidt B., Uherek M., Volk B., Baeuerle P.A., Kaltschmidt C. Transcription factor NF-kappaB is activated in primary neurons by amyloid beta peptides and in neurons surrounding early plaques from patients with Alzheimer disease. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:2642-2647.
14. Kaltschmidt B., Uherek M., Wellmann H., Volk B., Kaltschmidt C. Inhibition of NF-kappaB potentiates amyloid beta-mediated neuronal apoptosis. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:9409-9414.
15. Camandola S., Poli G., Mattson M.P. The lipid peroxidation product 4-hydroxy-2,3-nonenal inhibits constitutive and inducible activity of nuclear factor kappa B in neurons. Brain Res. Mol. Brain Res. 2000, 85:53-60.
16. Tamagno E., Bardini P., Obbili A., Vitali A., Borghi R., Zaccheo D., et al. Oxidative stress increases expression and activity of BACE in NT2 neurons. Neurobiol. Dis. 2002, 10:279-288.
17. Tamagno E., Parola M., Bardini P., Piccini A., Borghi R., Guglielmotto M., et al. Beta-site APP cleaving enzyme up-regulation induced by 4-hydroxynonenal is mediated by stress-activated protein kinases pathways. J. Neurochem. 2005, 92:628-636.
18. Bourne K.Z., Ferrari D.C., Lange-Dohna C., Rossner S., Wood T.G., Perez-Polo J.R. Differential regulation of BACE1 promoter activity by nuclear factor-kappaB in neurons and glia upon exposure to beta-amyloid peptides. J. Neurosci. Res. 2007, 85:1194-1204.
19. Buggia-Prevot V., Sevalle J., Rossner S., Checler F. NFkappaB-dependent control of BACE1 promoter transactivation by Abeta42. J. Biol. Chem. 2008, 283:10037-10047.
20. Guglielmotto M., Aragno M., Tamagno E., Vercellinatto I., Visentin S., Medana C., et al. AGEs/RAGE complex upregulates BACE1 via NF-kappaB pathway activation. Neurobiol. Aging 2012, 33(1):196.e13-27.
21. Donmez G., Wang D., Cohen D.E., Guarente L. SIRT1 suppresses beta-amyloid production by activating the alpha-secretase gene ADAM10. Cell 2010, 142:320-332.
22. Kim D., Nguyen M.D., Dobbin M.M., Fischer A., Sananbenesi F., Rodgers J.T., et al. SIRT1 deacetylase protects against neurodegeneration in models for Alzheimer's disease and amyotrophic lateral sclerosis. EMBO J. 2007, 26:3169-3179.
23. Qian H., Hausman G.J., Compton M.M., Azain M.J., Hartzell D.L., Baile C.A. Leptin regulation of peroxisome proliferator-activated receptor-gamma, tumor necrosis factor, and uncoupling protein-2 expression in adipose tissues. Biochem. Biophys. Res. Commun. 1998, 246:660-667.
24. Fewlass D.C., Noboa K., Pi-Sunyer F.X., Johnston J.M., Yan S.D., Tezapsidis N. Obesity-related leptin regulates Alzheimer's Abeta. FASEB J. 2004, 18:1870-1878.
25. Greco S.J., Bryan K.J., Sarkar S., Zhu X., Smith M.A., Ashford J.W., et al. Chronic leptin supplementation ameliorates pathology and improves cognitive performance in a transgenic mouse model of Alzheimer's disease. J. Alzheimers Dis. 2010, 19(4):1155-1167.
26. Tezapsidis N., Johnston J.M., Smith M.A., Ashford J.W., Casadesus G., Robakis N.K., et al. Leptin: a novel therapeutic strategy for Alzheimer's disease. J. Alzheimers Dis. 2009, 16:731-740.
27. Marwarha G., Dasari B., Prasanthi J.R., Schommer J., Ghribi O. Leptin reduces the accumulation of Abeta and phosphorylated tau induced by 27-hydroxycholesterol in rabbit organotypic slices. J. Alzheimers Dis. 2010, 19:1007-1019.
28. Marwarha G., Prasanthi J.R., Schommer J., Dasari B., Ghribi O. Molecular interplay between leptin, insulin-like growth factor-1, and beta-amyloid in organotypic slices from rabbit hippocampus. Mol. Neurodegener. 2011, 6:41.
29. Marwarha G., Ghribi O. Leptin signaling and Alzheimer's disease. Am. J. Neurodegener. Dis. 2012, 1:245-265.
30. Marwarha G., Ghribi O. Cellular model of Alzheimer's disease-relevance to therapeutic testing. Exp. Neurol. 2012, 233:733-739.
31. Lieb W., Beiser A.S., Vasan R.S., Tan Z.S., Au R., Harris T.B., et al. Association of plasma leptin levels with incident Alzheimer disease and MRI measures of brain aging. JAMA 2009, 302:2565-2572.
32. Power D.A., Noel J., Collins R., O'Neill D. Circulating leptin levels and weight loss in Alzheimer's disease patients. Dement. Geriatr. Cogn. Disord. 2001, 12:167-170.
33. Ramadori G., Fujikawa T., Fukuda M., Anderson J., Morgan D.A., Mostoslavsky R., et al. SIRT1 deacetylase in POMC neurons is required for homeostatic defenses against diet-induced obesity. Cell Metab. 2010, 12:78-87.
34. Ramadori G., Lee C.E., Bookout A.L., Lee S., Williams K.W., Anderson J., et al. Brain SIRT1: anatomical distribution and regulation by energy availability. J. Neurosci. 2008, 28:9989-9996.
35. Sasaki T., Kim H.J., Kobayashi M., Kitamura Y.I., Yokota-Hashimoto H., Shiuchi T., et al. Induction of hypothalamic Sirt1 leads to cessation of feeding via agouti-related peptide. Endocrinology 2010, 151:2556-2566.
36. Marwarha G., Dasari B., Prabhakara J.P., Schommer J., Ghribi O. Beta-amyloid regulates leptin expression and tau phosphorylation through the mTORC1 signaling pathway. J. Neurochem. 2010, 115:373-384.
37. Marwarha G., Raza S., Prasanthi J.R., Ghribi O. Gadd153 and NF-kappaB crosstalk regulates 27-hydroxycholesterol-induced increase in BACE1 and beta-amyloid production in human neuroblastoma SH-SY5Y cells. PLoS One 2013, 8:e70773.
38. Marwarha G., Rhen T., Schommer T., Ghribi O. The oxysterol 27-hydroxycholesterol regulates alpha-synuclein and tyrosine hydroxylase expression levels in human neuroblastoma cells through modulation of liver X receptors and estrogen receptors - relevance to Parkinson's disease. J. Neurochem. 2011, 119:1119-1136.
39. Marwarha G., Dasari B., Ghribi O. Endoplasmic reticulum stress-induced CHOP activation mediates the down-regulation of leptin in human neuroblastoma SH-SY5Y cells treated with the oxysterol 27-hydroxycholesterol. Cell. Signal. 2012, 24:484-492.
40. Grozinger C.M., Chao E.D., Blackwell H.E., Moazed D., Schreiber S.L. Identification of a class of small molecule inhibitors of the sirtuin family of NAD-dependent deacetylases by phenotypic screening. J. Biol. Chem. 2001, 276:38837-38843.
41. Mai A., Massa S., Lavu S., Pezzi R., Simeoni S., Ragno R., et al. Design, synthesis, and biological evaluation of sirtinol analogues as class III histone/protein deacetylase (sirtuin) inhibitors. J. Med. Chem. 2005, 48:7789-7795.
42. Kahyo T., Ichikawa S., Hatanaka T., Yamada M.K., Setou M. A novel chalcone polyphenol inhibits the deacetylase activity of SIRT1 and cell growth in HEK293T cells. J. Pharmacol. Sci. 2008, 108:364-371.
43. Jung-Hynes B., Nihal M., Zhong W., Ahmad N. Role of sirtuin histone deacetylase SIRT1 in prostate cancer. A target for prostate cancer management via its inhibition?. J. Biol. Chem. 2009, 284:3823-3832.
44. Rossner S., Sastre M., Bourne K., Lichtenthaler S.F. Transcriptional and translational regulation of BACE1 expression-implications for Alzheimer's disease. Prog. Neurobiol. 2006, 79:95-111.
45. Baeuerle P.A., Baltimore D. I kappa B: a specific inhibitor of the NF-kappa B transcription factor. Science 1988, 242:540-546.
46. Baeuerle P.A., Baltimore D. A 65-kappaD subunit of active NF-kappaB is required for inhibition of NF-kappaB by I kappaB. Genes Dev. 1989, 3:1689-1698.
47. Beg A.A., Baldwin A.S. The I kappa B proteins: multifunctional regulators of Rel/NF-kappa B transcription factors. Genes Dev. 1993, 7:2064-2070.
48. Chen L., Fischle W., Verdin E., Greene W.C. Duration of nuclear NF-kappaB action regulated by reversible acetylation. Science 2001, 293:1653-1657.
49. Gerritsen M.E., Williams A.J., Neish A.S., Moore S., Shi Y., Collins T. CREB-binding protein/p300 are transcriptional coactivators of p65. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:2927-2932.
50. Perkins N.D., Felzien L.K., Betts J.C., Leung K., Beach D.H., Nabel G.J. Regulation of NF-kappaB by cyclin-dependent kinases associated with the p300 coactivator. Science 1997, 275:523-527.
51. Zhong H., Voll R.E., Ghosh S. Phosphorylation of NF-kappa B p65 by PKA stimulates transcriptional activity by promoting a novel bivalent interaction with the coactivator CBP/p300. Mol. Cell 1998, 1:661-671.
52. Sheppard K.A., Rose D.W., Haque Z.K., Kurokawa R., McInerney E., Westin S., et al. Transcriptional activation by NF-kappaB requires multiple coactivators. Mol. Cell. Biol. 1999, 19:6367-6378.
53. Vanden B.W., De B.K., Boone E., Plaisance S., Haegeman G. The nuclear factor-kappaB engages CBP/p300 and histone acetyltransferase activity for transcriptional activation of the interleukin-6 gene promoter. J. Biol. Chem. 1999, 274:32091-32098.
54. Ashburner B.P., Westerheide S.D., Baldwin A.S. The p65 (RelA) subunit of NF-kappaB interacts with the histone deacetylase (HDAC) corepressors HDAC1 and HDAC2 to negatively regulate gene expression. Mol. Cell. Biol. 2001, 21:7065-7077.
55. Chen L.F., Mu Y., Greene W.C. Acetylation of RelA at discrete sites regulates distinct nuclear functions of NF-kappaB. EMBO J. 2002, 21:6539-6548.
56. Zhong H., May M.J., Jimi E., Ghosh S. The phosphorylation status of nuclear NF-kappa B determines its association with CBP/p300 or HDAC-1. Mol. Cell 2002, 9:625-636.
57. Yeung F., Hoberg J.E., Ramsey C.S., Keller M.D., Jones D.R., Frye R.A., et al. Modulation of NF-kappaB-dependent transcription and cell survival by the SIRT1 deacetylase. EMBO J. 2004, 23:2369-2380.
58. Sasaki T., Kikuchi O., Shimpuku M., Susanti V.Y., Yokota-Hashimoto H., Taguchi R., et al. Hypothalamic SIRT1 prevents age-associated weight gain by improving leptin sensitivity in mice. Diabetologia 2014 Apr, 57:819-831.
59. Minokoshi Y., Kim Y.B., Peroni O.D., Fryer L.G., Muller C., Carling D., et al. Leptin stimulates fatty-acid oxidation by activating AMP-activated protein kinase. Nature 2002, 415:339-343.
60. Minokoshi Y., Alquier T., Furukawa N., Kim Y.B., Lee A., Xue B., et al. AMP-kinase regulates food intake by responding to hormonal and nutrient signals in the hypothalamus. Nature 2004, 428:569-574.
61. Ceddia R.B. Direct metabolic regulation in skeletal muscle and fat tissue by leptin: implications for glucose and fatty acids homeostasis. Int. J. Obes. (Lond.) 2005, 29:1175-1183.
62. Greco S.J., Sarkar S., Johnston J.M., Tezapsidis N. Leptin regulates tau phosphorylation and amyloid through AMPK in neuronal cells. Biochem. Biophys. Res. Commun. 2009, 380:98-104.
63. Greco S.J., Hamzelou A., Johnston J.M., Smith M.A., Ashford J.W., Tezapsidis N. Leptin boosts cellular metabolism by activating AMPK and the sirtuins to reduce tau phosphorylation and beta-amyloid in neurons. Biochem. Biophys. Res. Commun. 2011, 414(1):170-174.
64. Canto C., Auwerx J. PGC-1alpha, SIRT1 and AMPK, an energy sensing network that controls energy expenditure. Curr. Opin. Lipidol. 2009, 20:98-105.
65. Fulco M., Cen Y., Zhao P., Hoffman E.P., McBurney M.W., Sauve A.A., et al. Glucose restriction inhibits skeletal myoblast differentiation by activating SIRT1 through AMPK-mediated regulation of Nampt. Dev. Cell 2008, 14:661-673.
66. Canto C., Gerhart-Hines Z., Feige J.N., Lagouge M., Noriega L., Milne J.C., et al. AMPK regulates energy expenditure by modulating NAD+metabolism and SIRT1 activity. Nature 2009, 458:1056-1060.
67. Ruderman N.B., Xu X.J., Nelson L., Cacicedo J.M., Saha A.K., Lan F., et al. AMPK and SIRT1: a long-standing partnership?. Am. J. Physiol. Endocrinol. Metab. 2010, 298:E751-E760.
68. Brooks C.L., Gu W. How does SIRT1 affect metabolism, senescence and cancer?. Nat. Rev. Cancer 2009, 9:123-128.
69. Guarente L., Franklin H. Epstein lecture: sirtuins, aging, and medicine. N. Engl. J. Med. 2011, 364:2235-2244.
70. Lange-Dohna C., Zeitschel U., Gaunitz F., Perez-Polo J.R., Bigl V., Rossner S. Cloning and expression of the rat BACE1 promoter. J. Neurosci. Res. 2003, 73:73-80.
71. Sastre M., Dewachter I., Rossner S., Bogdanovic N., Rosen E., Borghgraef P., et al. Nonsteroidal anti-inflammatory drugs repress beta-secretase gene promoter activity by the activation of PPARgamma. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:443-448.
72. Katsouri L., Parr C., Bogdanovic N., Willem M., Sastre M. PPARgamma co-activator-1alpha (PGC-1alpha) reduces amyloid-beta generation through a PPARgamma-dependent mechanism. J. Alzheimers Dis. 2011, 25:151-162.
73. Kakuma T., Wang Z.W., Pan W., Unger R.H., Zhou Y.T. Role of leptin in peroxisome proliferator-activated receptor gamma coactivator-1 expression. Endocrinology 2000, 141:4576-4582.
74. Crunkhorn S., Dearie F., Mantzoros C., Gami H., da Silva W.S., Espinoza D., et al. Peroxisome proliferator activator receptor gamma coactivator-1 expression is reduced in obesity: potential pathogenic role of saturated fatty acids and p38 mitogen-activated protein kinase activation. J. Biol. Chem. 2007, 282:15439-15450.
75. Roman E.A., Reis D., Romanatto T., Maimoni D., Ferreira E.A., Santos G.A., et al. Central leptin action improves skeletal muscle AKT, AMPK, and PGC1 alpha activation by hypothalamic PI3K-dependent mechanism. Mol. Cell. Endocrinol. 2010, 314:62-69.