Selective benefits of simvastatin in bitransgenic APPSwe,Ind/TGF-β1 mice

Neurobiology of Aging

Volumn 35, Issue 1, 2014, Pages 203-212

  Papadopoulos, Panayiota ^a   Tong, Xin Kang ^a   Hamel, Edith ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

Alzheimer's disease; Amyloidosis; Memory; PI3 Akt pathway; Simvastatin; Transforming growth factor 1

Indexed keywords

AMYLOID BETA DEGRADING ENZYME NEPRILYSIN PROTEIN; AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; BETA SECRETASE; EARLY GROWTH RESPONSE FACTOR 1; NITRIC OXIDE SYNTHASE; SIMVASTATIN; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; AMNESIA; AMYLOID PLAQUE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL WALL; BRAIN LEVEL; CEREBROVASCULAR DISEASE; CONTROLLED STUDY; DRUG EFFICACY; FEMALE; HIPPOCAMPAL CA1 REGION; MALE; MOUSE; MOUSE MUTANT; NERVE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENSORY STIMULATION; SPATIAL LEARNING; TRANSGENIC MOUSE; VIBRISSA; WHISKER STIMULATION;

ALZHEIMER'S DISEASE; AMYLOIDOSIS; MEMORY; PI3/AKT PATHWAY; SIMVASTATIN; TRANSFORMING GROWTH FACTOR-Β1;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; CA1 REGION, HIPPOCAMPAL; DISEASE MODELS, ANIMAL; EARLY GROWTH RESPONSE PROTEIN 1; GENE EXPRESSION; HYDROXYMETHYLGLUTARYL-COA REDUCTASE INHIBITORS; LEARNING; MEMORY; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MOLECULAR TARGETED THERAPY; MUTATION; NITRIC OXIDE; SIMVASTATIN; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84885189956     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2013.07.010     Document Type: Article

References (71)

1. Aboulkassim T., Tong X.K., Tse Y.C., Wong T.P., Woo S.B., Neet K.E., Brahimi F., Hamel E., Saragovi H.U. Ligand-dependent TrkA activity in brain differentially affects spatial learning and long-term memory. Mol. Pharmacol. 2011, 80:498-508.
2. Arvanitakis Z., Schneider J.A., Wilson R.S., Bienias J.L., Kelly J.F., Evans D.A., Bennett D.A. Statins, incident Alzheimer disease, change in cognitive function, and neuropathology. Neurology 2008, 70:1795-1802.
3. Blanchard J., Martel G., Guillou J.L., Nogues X., Micheau J. Impairment of spatial memory consolidation in APP(751SL) mice results in cue-guided response. Neurobiol. Aging 2008, 29:1011-1021.
4. Bozon B., Davis S., Laroche S. Arequirement for the immediate early gene zif268 in reconsolidation of recognition memory after retrieval. Neuron 2003, 40:695-701.
5. Buckwalter M.S., Yamane M., Coleman B.S., Ormerod B.K., Chin J.T., Palmer T., Wyss-Coray T. Chronically increased transforming growth factor-beta1 strongly inhibits hippocampal neurogenesis in aged mice. Am. J. Pathol. 2006, 169:154-164.
6. Burton T., Liang B., Dibrov A., Amara F. Transcriptional activation and increase in expression of Alzheimer's beta-amyloid precursor protein gene is mediated by TGF-beta in normal human astrocytes. Biochem. Biophys. Res. Commun. 2002, 295:702-712.
7. Butterfield D.A., Barone E., Mancuso C. Cholesterol-independent neuroprotective and neurotoxic activities of statins: perspectives for statin use in Alzheimer disease and other age-related neurodegenerative disorders. Pharmacol. Res. 2011, 64:180-186.
8. Caraci F., Battaglia G., Busceti C., Biagioni F., Mastroiacovo F., Bosco P., Drago F., Nicoletti F., Sortino M.A., Copani A. TGF-beta 1 protects against Abeta-neurotoxicity via the phosphatidylinositol-3-kinase pathway. Neurobiol. Dis. 2008, 30:234-242.
9. Carlsson C.M., Gleason C.E., Hess T.M., Moreland K.A., Blazel H.M., Koscik R.L., Schreiber N.T., Johnson S.C., Atwood C.S., Puglielli L., Hermann B.P., McBride P.E., Stein J.H., Sager M.A., Asthana S. Effects of simvastatin on cerebrospinal fluid biomarkers and cognition in middle-aged adults at risk for Alzheimer's disease. J.Alzheimers Dis. 2008, 13:187-197.
10. Chen G., Rajkowska G., Du F., Seraji-Bozorgzad N., Manji H.K. Enhancement of hippocampal neurogenesis by lithium. J.Neurochem. 2000, 75:1729-1734.
11. Chen J., Zhang Z.G., Li Y., Wang Y., Wang L., Jiang H., Zhang C., Lu M., Katakowski M., Feldkamp C.S., Chopp M. Statins induce angiogenesis, neurogenesis, and synaptogenesis after stroke. Ann. Neurol. 2003, 53:743-751.
12. Cramer C., Haan M.N., Galea S., Langa K.M., Kalbfleisch J.D. Use of statins and incidence of dementia and cognitive impairment without dementia in a cohort study. Neurology 2008, 71:344-350.
13. Davis D.G., Schmitt F.A., Wekstein D.R., Markesbery W.R. Alzheimer neuropathologic alterations in aged cognitively normal subjects. J.Neuropathol. Exp. Neurol. 1999, 58:376-388.
14. Davis S., Bozon B., Laroche S. How necessary is the activation of the immediate early gene zif268 in synaptic plasticity and learning?. Behav. Brain Res. 2003, 142:17-30.
15. DeIpolyi A.R., Fang S., Palop J.J., Yu G.Q., Wang X., Mucke L. Altered navigational strategy use and visuospatial deficits in hAPP transgenic mice. Neurobiol. Aging 2008, 29:253-266.
16. Dickey C.A., Loring J.F., Montgomery J., Gordon M.N., Eastman P.S., Morgan D. Selectively reduced expression of synaptic plasticity-related genes in amyloid precursor protein+ presenilin-1 transgenic mice. J.Neurosci. 2003, 23:5219-5226.
17. Fassbender K., Simons M., Bergmann C., Stroick M., Lutjohann D., Keller P., Runz H., Kuhl S., Bertsch T., von Bergmann K., Hennerici M., Beyreuther K., Hartmann T. Simvastatin strongly reduces levels of Alzheimer's disease beta -amyloid peptides Abeta 42 and Abeta 40 invitro and invivo. Proc. Natl. Acad. Sci. U.S.A 2001, 98:5856-5861.
18. Ferretti M.T., Cuello A.C. Does a pro-inflammatory process precede Alzheimer's disease and mild cognitive impairment?. Curr. Alzheimer Res. 2011, 8:164-174.
19. Fiorentini A., Rosi M.C., Grossi C., Luccarini I., Casamenti F. Lithium improves hippocampal neurogenesis, neuropathology and cognitive functions in APP mutant mice. PloS One 2010, 5:e14382.
20. Flanders K.C., Lippa C.F., Smith T.W., Pollen D.A., Sporn M.B. Altered expression of transforming growth factor-beta in Alzheimer's disease. Neurology 1995, 45:1561-1569.
21. Frank-Cannon T.C., Alto L.T., McAlpine F.E., Tansey M.G. Does neuroinflammation fan the flame in neurodegenerative diseases?. Mol. Neurodegener. 2009, 4:47.
22. Grammas P., Ovase R. Cerebrovascular transforming growth factor-beta contributes to inflammation in the Alzheimer's disease brain. Am. J. Pathol. 2002, 160:1583-1587.
23. Haag M.D., Hofman A., Koudstaal P.J., Stricker B.H., Breteler M.M. Statins are associated with a reduced risk of Alzheimer disease regardless of lipophilicity. The Rotterdam Study. J.Neurol. Neurosurg. Psychiatry 2009, 80:13-17.
24. Iadecola C. Neurovascular regulation in the normal brain and in Alzheimer's disease. Nat. Rev. Neurosci. 2004, 5:347-360.
25. Jick H., Zornberg G.L., Jick S.S., Seshadri S., Drachman D.A. Statins and the risk of dementia. Lancet 2000, 356:1627-1631.
26. Jones M.W., Errington M.L., French P.J., Fine A., Bliss T.V., Garel S., Charnay P., Bozon B., Laroche S., Davis S. Arequirement for the immediate early gene Zif268 in the expression of late LTP and long-term memories. Nat. Neurosci. 2001, 4:289-296.
27. Karki K., Knight R.A., Han Y., Yang D., Zhang J., Ledbetter K.A., Chopp M., Seyfried D.M. Simvastatin and atorvastatin improve neurological outcome after experimental intracerebral hemorrhage. Stroke 2009, 40:3384-3389.
28. Koehler R.C., Roman R.J., Harder D.R. Astrocytes and the regulation of cerebral blood flow. Trends Neurosci. 2009, 32:160-169.
29. Kotilinek L.A., Westerman M.A., Wang Q., Panizzon K., Lim G.P., Simonyi A., Lesne S., Falinska A., Younkin L.H., Younkin S.G., Rowan M., Cleary J., Wallis R.A., Sun G.Y., Cole G., Frautschy S., Anwyl R., Ashe K.H. Cyclooxygenase-2 inhibition improves amyloid-beta-mediated suppression of memory and synaptic plasticity. Brain 2008, 131:651-664.
30. Kurata T., Miyazaki K., Kozuki M., Panin V.L., Morimoto N., Ohta Y., Nagai M., Ikeda Y., Matsuura T., Abe K. Atorvastatin and pitavastatin improve cognitive function and reduce senile plaque and phosphorylated tau in aged APP mice. Brain Res. 2011, 1371:161-170.
31. Lazarov O., Mattson M.P., Peterson D.A., Pimplikar S.W., van Praag H. When neurogenesis encounters aging and disease. Trends Neurosci. 2010, 33:569-579.
32. Lesne S., Kotilinek L., Ashe K.H. Plaque-bearing mice with reduced levels of oligomeric amyloid-beta assemblies have intact memory function. Neuroscience 2008, 151:745-749.
33. Li G., Shofer J.B., Rhew I.C., Kukull W.A., Peskind E.R., McCormick W., Bowen J.D., Schellenberg G.D., Crane P.K., Breitner J.C., Larson E.B. Age-varying association between statin use and incident Alzheimer's disease. J.Am. Geriatr. Soc. 2010, 58:1311-1317.
34. Li L., Cao D., Kim H., Lester R., Fukuchi K. Simvastatin enhances learning and memory independent of amyloid load in mice. Ann. Neurol. 2006, 60:729-739.
35. Lu D., Qu C., Goussev A., Jiang H., Lu C., Schallert T., Mahmood A., Chen J., Li Y., Chopp M. Statins increase neurogenesis in the dentate gyrus, reduce delayed neuronal death in the hippocampal CA3 region, and improve spatial learning in rat after traumatic brain injury. J.Neurotrauma 2007, 24:1132-1146.
36. Mucke L., Masliah E., Yu G.Q., Mallory M., Rockenstein E.M., Tatsuno G., Hu K., Kholodenko D., Johnson-Wood K., McConlogue L. High-level neuronal expression of abeta 1-42 in wild-type human amyloid protein precursor transgenic mice: synaptotoxicity without plaque formation. J.Neurosci. 2000, 20:4050-4058.
37. Nagaoka T., Hein T.W., Yoshida A., Kuo L. Simvastatin elicits dilation of isolated porcine retinal arterioles: role of nitric oxide and mevalonate-rho kinase pathways. Invest. Ophthalmol. Vis. Sci. 2007, 48:825-832.
38. Nicolakakis N., Aboulkassim T., Aliaga A., Tong X.K., Rosa-Neto P., Hamel E. Intact memory in TGF-beta1 transgenic mice featuring chronic cerebrovasculardeficit: recovery with pioglitazone. J.Cereb. Blood Flow Metab. 2011, 31:200-211.
39. Ongali B., Nicolakakis N., Lecrux C., Aboulkassim T., Rosa-Neto P., Papadopoulos P., Tong X.K., Hamel E. Transgenic mice overexpressing APP and transforming growth factor-beta1 feature cognitive and vascular hallmarks of Alzheimer's disease. Am. J. Pathol. 2010, 177:3071-3080.
40. Papadopoulos P., Ongali B., Hamel E. Selective invivo antagonism of endothelin receptors in transforming growth factor-beta1 transgenic mice that mimic the vascular pathology of Alzheimer's disease. Can. J. Physiol. Pharmacol. 2010, 88:652-660.
41. Park L., Zhou P., Pitstick R., Capone C., Anrather J., Norris E.H., Younkin L., Younkin S., Carlson G., McEwen B.S., Iadecola C. Nox2-derived radicals contribute to neurovascular and behavioral dysfunction in mice overexpressing the amyloid precursor protein. Proc. Natl. Acad. Sci. U.S.A 2008, 105:1347-1352.
42. Petanceska S.S., DeRosa S., Olm V., Diaz N., Sharma A., Thomas-Bryant T., Duff K., Pappolla M., Refolo L.M. Statin therapy for Alzheimer's disease: will it work?. J.Mol. Neurosci. 2002, 19:155-161.
43. Rao J.S., Kellom M., Kim H.W., Rapoport S.I., Reese E.A. Neuroinflammation and synaptic loss. Neurochem. Res. 2012, 37:903-910.
44. Rivest S. The promise of anti-inflammatory therapies for CNS injuries and diseases. Exp. Rev. Neurother. 2011, 11:783-786.
45. Sano M., Bell K.L., Galasko D., Galvin J.E., Thomas R.G., van Dyck C.H., Aisen P.S. Arandomized, double-blind, placebo-controlled trial of simvastatin to treat Alzheimer disease. Neurology 2011, 77:556-563.
46. Shepardson N.E., Shankar G.M., Selkoe D.J. Cholesterol level and statin use in Alzheimer disease: I. Review of epidemiological and preclinical studies. Arch. Neurol. 2011, 68:1239-1244.
47. Shepardson N.E., Shankar G.M., Selkoe D.J. Cholesterol level and statin use in Alzheimer disease: II. Review of human trials and recommendations. Arch. Neurol. 2011, 68:1385-1392.
48. Shinohara M., Sato N., Kurinami H., Takeuchi D., Takeda S., Shimamura M., Yamashita T., Uchiyama Y., Rakugi H., Morishita R. Reduction of brain beta-amyloid (Abeta) by fluvastatin, a hydroxymethylglutaryl-CoA reductase inhibitor, through increase in degradation of amyloid precursor protein C-terminal fragments (APP-CTFs) and Abeta clearance. J.Biol. Chem. 2010, 285:22091-22102.
49. Simons M., Schwarzler F., Lutjohann D., von Bergmann K., Beyreuther K., Dichgans J., Wormstall H., Hartmann T., Schulz J.B. Treatment with simvastatin in normocholesterolemic patients with Alzheimer's disease: a 26-week randomized, placebo-controlled, double-blind trial. Ann. Neurol. 2002, 52:346-350.
50. Sparks D.L. Alzheimer disease: statins in the treatment of Alzheimer disease. Nat. Rev. Neurol. 2011, 7:662-663.
51. Sparks D.L., Sabbagh M.N., Connor D.J., Lopez J., Launer L.J., Browne P., Wasser D., Johnson-Traver S., Lochhead J., Ziolwolski C. Atorvastatin for the treatment of mild to moderate Alzheimer disease: preliminary results. Arch. Neurol. 2005, 62:753-757.
52. Tamboli I.Y., Barth E., Christian L., Siepmann M., Kumar S., Singh S., Tolksdorf K., Heneka M.T., Lutjohann D., Wunderlich P., Walter J. Statins promote the degradation of extracellular amyloid {beta}-peptide by microglia via stimulation of exosome-associated insulin-degrading enzyme (IDE) secretion. J.Biol. Chem. 2010, 285:37405-37414.
53. Tesseur I., Wyss-Coray T. Arole for TGF-beta signaling in neurodegeneration: evidence from genetically engineered models. Curr. Alzheimer Res. 2006, 3:505-513.
54. Tesseur I., Zou K., Esposito L., Bard F., Berber E., Can J.V., Lin A.H., Crews L., Tremblay P., Mathews P., Mucke L., Masliah E., Wyss-Coray T. Deficiency in neuronal TGF-beta signaling promotes neurodegeneration and Alzheimer's pathology. J.Clin. Invest. 2006, 116:3060-3069.
55. Tong, X.K., Hamel, E., 2013. Simvastatin restored endothelial and smooth muscle cell function and reduced string vessel pathology in transgenic transforming growth factor-b1 mice Abstract # 620 Presented at: Brain 2013. May 20-23, 2013; Shanghai.
56. Tong X.K., Lecrux C., Hamel E. Age-dependent rescue by simvastatin of Alzheimer's disease cerebrovascular and memory deficits. J.Neurosci. 2012, 32:4705-4715.
57. Tong X.K., Nicolakakis N., Fernandes P., Ongali B., Brouillette J., Quirion R., Hamel E. Simvastatin improves cerebrovascular function and counters soluble amyloid-beta, inflammation and oxidative stress in aged APP mice. Neurobiol. Dis. 2009, 35:406-414.
58. Tong X.K., Nicolakakis N., Kocharyan A., Hamel E. Vascular remodeling versus amyloid beta-induced oxidative stress in the cerebrovascular dysfunctions associated with Alzheimer's disease. J.Neurosci. 2005, 25:11165-11174.
59. Trouche S., Bontempi B., Roullet P., Rampon C. Recruitment of adult-generated neurons into functional hippocampal networks contributes to updating and strengthening of spatial memory. Proc. Natl. Acad. Sci. U.S.A 2009, 106:5919-5924.
60. Valero J., Espana J., Parra-Damas A., Martin E., Rodriguez-Alvarez J., Saura C.A. Short-term environmental enrichment rescues adult neurogenesis and memory deficits in APP(Sw, Ind) transgenic mice. PloS One 2011, 6:e16832.
61. van der Wal E.A., Gomez-Pinilla F., Cotman C.W. Transforming growth factor-beta 1 is in plaques in Alzheimer and Down pathologies. Neuroreport 1993, 4:69-72.
62. Vedernikov Y.P., Fulep E.E., Saade G.R., Garfield R.E. Calcitonin gene-related peptide dilates the pregnant rat uterine vascular bed via guanylate cyclase, ATP- and Ca-sensitive potassium channels and gap junctions. Curr. Med. Res. Opin. 2002, 18:465-470.
63. Verret L., Jankowsky J.L., Xu G.M., Borchelt D.R., Rampon C. Alzheimer's-type amyloidosis in transgenic mice impairs survival of newborn neurons derived from adult hippocampal neurogenesis. J.Neurosci. 2007, 27:6771-6780.
64. Wolozin B., Kellman W., Ruosseau P., Celesia G.G., Siegel G. Decreased prevalence of Alzheimer disease associated with 3-hydroxy-3-methyglutaryl coenzyme A reductase inhibitors. Arch. Neurol. 2000, 57:1439-1443.
65. Wu H., Lu D., Jiang H., Xiong Y., Qu C., Li B., Mahmood A., Zhou D., Chopp M. Simvastatin-mediated upregulation of VEGF and BDNF, activation of the PI3K/Akt pathway, and increase of neurogenesis are associated with therapeutic improvement after traumatic brain injury. J.Neurotrauma 2008, 25:130-139.
66. Wyss-Coray T., Feng L., Masliah E., Ruppe M.D., Lee H.S., Toggas S.M., Rockenstein E.M., Mucke L. Increased central nervous system production of extracellular matrix components and development of hydrocephalus in transgenic mice overexpressing transforming growth factor-beta 1. Am. J. Pathol. 1995, 147:53-67.
67. Wyss-Coray T., Lin C., Sanan D.A., Mucke L., Masliah E. Chronic overproduction of transforming growth factor-beta1 by astrocytes promotes Alzheimer's disease-like microvascular degeneration in transgenic mice. Am. J. Pathol. 2000, 156:139-150.
68. Wyss-Coray T., Masliah E., Mallory M., McConlogue L., Johnson-Wood K., Lin C., Mucke L. Amyloidogenic role of cytokine TGF-beta1 in transgenic mice and in Alzheimer's disease. Nature 1997, 389:603-606.
69. Yaffe K., Barrett-Connor E., Lin F., Grady D. Serum lipoprotein levels, statin use, and cognitive function in older women. Arch. Neurol. 2002, 59:378-384.
70. Zhu Y., Culmsee C., Klumpp S., Krieglstein J. Neuroprotection by transforming growth factor-beta1 involves activation of nuclear factor-kappaB through phosphatidylinositol-3-OH kinase/Akt and mitogen-activated protein kinase-extracellular-signal regulated kinase1,2 signaling pathways. Neuroscience 2004, 123:897-906.
71. Zlokovic B.V. Neurovascular pathways to neurodegeneration in Alzheimer's disease and other disorders. Nat. Rev. Neurosci. 2011, 12:723-738.