Optical and SPION-Enhanced MR imaging shows that trans-stilbene inhibitors of NF-κB concomitantly lower alzheimer's disease plaque formation and microglial activation in AβPP/PS-1 transgenic mouse brain

Journal of Alzheimer's Disease

Volumn 40, Issue 1, 2014, Pages 191-212

  Solberg, Nathan O ^a   Chamberlin, Ryan ^d   Vigil, Jenette R ^a   Deck, Lorraine M ^b   Heidrich, John E ^c   Brown, David C ^a   Brady, Christina I ^a   Vander Jagt, Thomas A ^c   Garwood, Michael ^d   Bisoffi, Marco ^a   Severns, Virginia ^a   Jagt, David L Vander ^a,c   Sillerud, Laurel O ^a  

^a UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NEW MEXICO   (United States)

^c Quatros   (United States)

^d UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

LD55; magnetic resonance imaging; microglia; neuroinflammation; NF B; resveratrol; SPIONs; transgenic mice

Indexed keywords

AMYLOID PRECURSOR PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LD 55; PRESENILIN 1; PROTEIN INHIBITOR; RESVERATROL; STILBENE; SUPERPARAMAGNETIC IRON OXIDE NANOPARTICLE; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; AMYLOID PLAQUE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BRAIN CORTEX; BRAIN SIZE; BRAIN TISSUE; CELL ACTIVATION; CEREBELLUM; CONFOCAL MICROSCOPE; CONTRAST ENHANCEMENT; CONTRAST TO NOISE RATIO; CONTROLLED STUDY; CORPUS STRIATUM; EX VIVO STUDY; FLUORESCENCE MICROSCOPY; HIPPOCAMPUS; HISTOPATHOLOGY; IMMUNOFLUORESCENCE; MICROGLIA; MOUSE; NERVOUS SYSTEM INFLAMMATION; NEUROIMAGING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; OLFACTORY BULB; PRIORITY JOURNAL; PUTAMEN; QUANTITATIVE ANALYSIS; SUPPLEMENTATION; THALAMUS; TISSUE SECTION;

LD55; MAGNETIC RESONANCE IMAGING; MICROGLIA; NEUROINFLAMMATION; NF-ΚB; RESVERATROL; SPIONS; TRANSGENIC MICE;

AGE FACTORS; ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; BRAIN; DISEASE MODELS, ANIMAL; ENZYME INHIBITORS; FERRIC COMPOUNDS; HUMANS; IMAGING, THREE-DIMENSIONAL; METAL NANOPARTICLES; MICE; MICE, TRANSGENIC; MICROGLIA; MUTATION; NEUROPROTECTIVE AGENTS; NF-KAPPA B; PLAQUE, AMYLOID; PRESENILIN-1; STILBENES;

EID: 84900002249     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-131031     Document Type: Article

References (63)

1. Alzheimer's Association (2011) Alzheimer's disease facts and figures. Alzheimer's Association, Washington, D.C., http://www.alz.org/downloads/facts- figures-2011.pdf
2. Hebert LE, Scherr PA, Bienias JL, Bennett DA, Evans DA (2003) Alzheimer's disease in the U.S. population: Prevalence estimates using the 2000 census. Arch Neurol 60, 1119-1122.
3. Fodero-Tavoletti AT, Villemagn VL, Rowe CC, Masters CL, Barnham KJ, Cappai R (2011) Amyloid-β : The seeds of darkness. Int J Biochem Cell Biol 43, 1247-1251.
4. McLean CA, Cherny RA, Fraser FW, Fuller SJ, Smith MJ, Beyreuther K, Bush AI, Masters CL (1999) Soluble pool of Abeta amyloid as a determinant of severity of neurodegener-ation in Alzheimer's disease. Ann Neurol 46, 860-866.
5. Liu Z, Condello C, Schain A, Harb R, Grutzendler J (2010) CX3CR1 in microglia regulates brain amyloid deposition through selective protofibrillar amyloid-β phagocytosis. J Neurosci30, 17091-17101.
6. Selkoe DJ (1991) The molecular pathology of Alzheimer's disease. Neuron 6, 487-498.
7. Selkoe DJ, Schenk D (2003) Alzheimer's disease: Molecular understanding predicts amyloid-based therapeutics. Annu Rev Pharmacol Toxicol 43, 545-584.
8. Urbanc B, Betnel M, Cruz L, Bitan G, Teplow D (2010) Elucidation of amyloid β-protein oligomerization mechanisms: Discrete molecular dynamics study. J Am Chem Soc 132, 4266-4280.
9. Khandelwal PJ, Herman AM, Moussa CE (2011) Inflammation in the early stages of neurodegenerative pathology. J Neuroimmunol 238, 1-11.
10. Doré V, Villemagne VL, Bourgeat P, Fripp J, Acosta O, Chetélat G, Zhou L, Martins R, Ellis KA, Masters CL, Ames D, Salvado O, Rowe CC (2013) Cross-sectional and longitudinal analysis of the relationship between Aβ deposition, cortical thickness, and memory in cognitively unimpaired individuals and in Alzheimer disease. JAMA Neurol 27, 1-9.
11. Jack CR Jr, Lowe VJ, Senjem ML, Weigand SD, Kemp BJ, Shiung MM, Knopman DS, Boeve BF, Klunk WE, Mathis CA, Petersen RC (2008) 11C PiB and structural MRI provide complementary information in imaging of Alzheimer's disease and amnestic mild cognitive impairment. Brain 131, 665-680.
12. Choi SR, Golding G, Zhuang Z, Zhang W, Lim N, Hefti F, Benedum TE, Kilbourn MR, Skovronsky D, Kung HF (2009) Preclinical properties of 18F-AV-45: A PET agent for Abeta plaques in the brain. J Nucl Med 50, 1887-1894.
13. Yang L, Rieves D, Ganley C (2012) Brain amyloid imaging-FDA approval of florbetapir F18 injection. N Engl J Med 367, 885-887.
14. Chamberlain R, Reyes D, Curran GL, Marjanska M, Wen-genack TM, Poduslo JF, Garwood M, Jack CR (2009) Comparison of amyloid plaque contrast generated by T2-weighted, T2-weighted, and susceptibility-weighted imaging methods in transgenic mouse models of Alzheimer's disease. Magn Reson Med 61, 1158-1164.
15. Jack CR, Wengenack TM, Reyes DA, Garwood M, Curran GL, Borowsk BJ, Lin J, Preboske GM, Holasek SS, Adriany G, Poduslo JF (2005) In vivo magnetic resonance microimaging of individual amyloid plaques in Alzheimer's transgenic mice. J Neurosci 25, 10041-10048.
16. Benveniste H, Einstein G, Kim KR, Hulette C, Johnson GA (1999) Detection of neuritic plaques in Alzheimer's disease by magnetic resonance microscopy. Proc Natl Acad Sci USA 96, 14079-14084.
17. Borthakur A, Gur T, Wheaton AJ, Corbo M, Trojanowski JQ, Lee VM, Reddy R (2006) In vivo measurement of plaque burden in a mouse model of Alzheimer's disease. J Magn Reson Imag 24, 1011-1017.
18. Braakman N, Matysik J, vanDuinen SG, Verbeek F, Schliebs R, de Groot HJ, Alia A (2006) Longitudinal assessment of Alzheimer's beta-amyloid plaque development in transgenic mice monitored by in vivo magnetic resonance microimaging. J Magn Reson Imaging 24, 530-536.
19. Benveniste H, Ma Y, Dhawan J, Gifford A, Smith SD, Fein-stein I, Du C, Grant SC, Hof PR (2007) Anatomical and functional phenotyping of mice models of Alzheimer's disease by MR microscopy. Ann N Y Acad Sci 1097, 12-29.
20. Sillerud LO, Solberg NO, Chamberlin R, Heidrich JE, Brown DC, Brady CI, Vander Jagt TA, Garwood M, Vander Jagt DL (2013) SPION-enhanced magnetic resonance imaging of Alzheimer's plaques in AβPP/PS-1 transgenic mouse brain. J Alzheimers Dis 34, 349-365.
21. Kim YS, Joh TH (2006) Microglia, major player in the brain inflammation: Their roles in the pathogenesis of Parkinson's disease. Exp Mol Med 38, 333-347.
22. El Khoury J, Luster AD (2008) Mechanisms of microglia accumulation in Alzheimer's disease: Therapeutic implications. Trends Pharmacol Sci 29, 626-632.
23. Graeber MB (2010) Changing face of microglia. Science 330, 783-788.
24. Schlachetzki JC, Hüll M (2009) Microglial activation in Alzheimer's disease. Curr Alzheimer Res 6, 554-563.
25. Heneka MT, O'Banion MK (2007) Inflammatory processes in Alzheimer's disease. J Neuroimmunol 184, 69-91.
26. Nimmerjahn A, Kirchoff F, Helmchen F (2005) Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 308, 1314-1318.
27. Takeuchi O, Akira S (2010) Pattern recognition receptors and inflammation. Cell 140, 805-820.
28. Tahara K, Kim HD, Jin JJ, Maxwell JA, Li L, Fukuchi KI (2006) Role of toll-like receptor signaling in Aβ uptake and clearance. Brain 129, 3006-3019.
29. Rhee SH, Hwang D (2000) Murine TOLL-like receptor 4 confers lipopolysaccharide responsiveness as determined by activation of NF-/cB and expression of the inducible cyclooxy-genase. J Biol Chem 275, 34035-34040.
30. Capiralla H, Vingtdeux V, Zhao H, Sankowski R, Al-Abed Y, Davies P, Marambaud P (2012) Resveratrol mitigates lipopolysaccharide-and Aβ-mediated microglial inflammation by inhibiting the TLR4/NF-/cB/STAT signaling cascade. J Neurochem 120, 461-472.
31. Bornemann KD, Wiederhold KH, Pauli C, Ermini F, Stalder M, Schnell L, Sommer B, Jucker M, Staufenbiel M (2001) Abeta-induced inflammatory processes in microglia cells of AβPP23 transgenic mice. Am J Pathol 158, 63-73.
32. Pan XD, Zhu YG, Lin N, Zhang J, Ye QY, Huang HP, Chen XC (2011) Microglial phagocytosis induced by fibrillar β-amyloid is attenuated by oligomeric β-amyloid: Implications for Alzheimer's disease. Mol Neurodegener 6, 45.
33. Neher JJ, Neniskyte U, Brown GC (2012) Primary phagocytosis of neurons by inflamed microglia: Potential roles in neurodegeneration. Front Pharmacol 3, 27.
34. Granic I, Dolga AM, Nijholt IM, van Dijk G, Eisel ULM (2009) Inflammation and NF-/cB in Alzheimer's disease and diabetes. J Alzheimers Dis 16, 809-821.
35. Kaltschmidt B, Uherek M, Volk B, Baeuerle PA, Kaltschmidt C (1997) 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 USA 94, 2642-2647.
36. Mattson MP (2005) NF-/cB in the survival and plasticity of neurons. Neurochem Res 30, 883-893.
37. Kaltschmidt B, Kaltschmidt C (2009) NF-/cB in the nervous system. Cold Spring Harb Perspect Biol 1, a001271.
38. Lee Y-J, Han SB, Nam S-Y, Oh K-W, Hong JT (2010) Inflammation and Alzheimer's disease. Arch Pharm Res 33, 1539-1556.
39. Sovak M (2001) Grape extract, resveratrol, and its analogs: A review. J Med Food 4, 93-105.
40. Leiro J, Arranz JA, Fraiz N, Sanmartin ML, Quezada E, Orallo F (2005) Effect of cis-resveratrol on genes involved in nuclear factor kappa B signaling. Int Immunopharmacol 5, 393-406.
41. Storz P, Doppler H, Toker A (2004) Activation loop phosphorylation controls protein kinase D-dependent activation of nuclear factor kappaB. Mol Pharmacol 66, 870-879.
42. Ulrich S, Wolter F, Stein JM (2005) Molecular mechanisms of the chemopreventive effects of resveratrol and its analogs in carcinogenesis. Mol Nutr Food Res 49, 452-461.
43. Heynekamp JJ, Weber WM, Hunsaker LA, Gonzales AM, Orlando RA, Deck LM, Vander Jagt DL (2006) Substituted trans-stilbenes, including analogues of the natural product resveratrol, inhibit the human tumor necrosis factor alpha-induced activation of transcription factor nuclear factor kappaB. J Med Chem 49, 7182-7189.
44. Bi XL, Yang JY, Dong YX, Wang JM, Cui YH, Ikeshima T, Zhao YQ, Wu CF (2005) Resveratrol inhibits nitric oxide and TNF-alpha production by lipopolysaccharide-activated microglia. Int Immunopharmacol 5, 185-193.
45. Boberin LD, Quincozes-Santos A, Guerra MC, Leite MC, Souza DO, Goncalves CA, Gottfried C (2012) Resveratrol prevents ammonia toxicity in astroglial cells. PLoS One 7, e52164.
46. Kim J, Lee HJ, Lee KW (2010) Naturally occurring phy-tochemicals for the prevention of Alzheimer's disease. J Neurochem 112, 1415-1430.
47. Kotha A, Sekharam M, Cilenti L, Siddiquee K, Khaled A, Zervos AS, Carter B, Turkson J, Jove R (2006) Resveratrol inhibits Src and Stat3 signaling and induces the apoptosis of malignant cells containing activated Stat3 protein. Mol Cancer Res 5, 621-629.
48. Faber AC, Dufort FJ, Blair D, Wagoer D, Roberts MF, Chikes TC (2006) Inhibition of phosphatidylinositol 3-kinase-mediated glucose metabolism coincides with resveratrol-induced cell cycle arrest in human diffuse large B-cell lymphomas. Biochem Pharmacol 72, 1246-1256.
49. Feng L, Jin J, Zhang LF, Yan T, Tao WY (2006) Analysis of the resveratrol-binding protein using phage-displayed random peptide library. Acta Biochim Biophys Sin (Shanghai) 38, 342-348.
50. Kundu JK, Shin YK, Kim SH, Surh YJ (2006) Resveratrol inhibits phorbol ester-induced expression of COX-2 and activation of NF-kappaB in mouse skin by blocking IkappaB kinase activity. Carcinogenesis 27, 1465-1474.
51. Hardy J, Allsop D (1991) Amyloid deposition as the central event in the aetiology of Alzheimer's disease. Trends Pharmacol Sci 12, 383-388.
52. Hardy J (1997) Amyloid, the presenilins and Alzheimer's disease. Trends Neurosci 20, 154-159.
53. Hsaio K, Chapman P, Nilsen S, Eckman C, Harigaya Y, Younkin S, Yang F, Cole G (1996) Correlative memory deficits, Aβ elevation, and amyloid plaques in transgenic mice. Science 274, 99-102.
54. Holcomb L, Gordon MN, McGowan E, Yo X, Benkovic S, Jantzen P, Wright K, Saad I, Mueller R, Morgan D, Sanders S, Zehr C, O'Campo K, Hardy J, Prada CM, Eckman C, Younkin S, Hsaio K, Duff K (1998) Accelerated Azlheimer-type phe-notype in transgenic mice carrying both mutant amyloid precursor protein and presenilin 1 transgenes. Nat Med 4, 97-100.
55. Karuppagounder SS, Pinto JT, Xu H, Chen HL, Beal MF, Gibson GE (2009) Dietary supplementation with resveratrol reduces plaque pathology in a transgenic model of Alzheimer's disease. Neurochem Int 54, 111-118.
56. Vingtdeux V, Giliberto L, Zhao H, Chandakkar P, Wu Q, Simon JE, Janle EM, Lobo J, Ferruzzi MG, Davies P, Marambaud P (2010) AMP-activated protein kinase signaling activation by resveratrol modulates amyloid-β peptide metabolism. J Biol Chem 285, 9100-9113.
57. Stookey LL (1970) Ferrozine-a new spectrophotometric reagent for iron. Anal Chem 42, 779-781.
58. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH image to ImageJ: 25 years of image analysis. Nat Methods 9, 671-675.
59. Lu X, Ma L, Ruan L, Kong Y, Mou H, Zhang Z, Wang Z, Wang JM, Le Y (2010) Resveratrol differentially modulates inflammatory responses of microglia and astrocytes. J Neuroinflammation 7, 46-60.
60. Zhang F, Liu J, Shi JS (2010) Anti-inflammatory activities of resveratrol in the brain: Role of resveratrol in microglial activation. Eur J Pharmacol 636, 1-7.
61. Yan P, Bero AW, Cirrito JR, Xiao Q, Hu X, Wang Y, Gonzales E, Holtzman DM, Lee J (2009) Characterizing the appearance and growth of amyloid plaques in AβPP/PS1 mice. J Neurosci 29, 10706-10714.
62. Masters CL, Cappai R, Barnham KJ, Villemagne VL (2006) Molecular mechanisms for Alzheimer's disease: Implications for neuroimaging and therapeutics. J Neurochem 106, 1700-1725.
63. Taylor RM, Huber DL, Monson TC, Ali AS, Bisoffi M, Sillerud LO (2011) Multifunctional iron platinum stealth immunomicelles: Targeted detection of human prostate cancer cells using both fluorescence and magnetic resonance imaging. J Nanopart Res 13, 4717-4729.