Blocking IGF signaling in adult neurons alleviates alzheimer’s disease pathology through amyloid-β clearance

Journal of Neuroscience

Volumn 35, Issue 33, 2015, Pages 11500-11513

  Gontier, Géraldine ^a,b   George, Caroline ^a,b   Chaker, Zayna ^a,c   Holzenberger, Martin ^a,b   Aïd, Saba ^a,b  

^a HÔPITAL SAINT ANTOINE   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

Alzheimer s disease; Amyloid ; Conditional mutagenesis; Insulin like growth factor; Mouse model; Neuron

Indexed keywords

AMYLOID BETA PROTEIN; SOMATOMEDIN C; SOMATOMEDIN C RECEPTOR;

ADULT; AGING; ALZHEIMER DISEASE; AMYLOID PLAQUE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTOPHAGY; BARNES MAZE TEST; CELL BODY; CELL SIZE; CELL STRUCTURE; CELL VACUOLE; CONNECTOME; CONTROLLED STUDY; DENDRITE; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GENOTYPE; GLIA CELL; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; INTRACELLULAR SIGNALING; MALE; MEMORY; MOUSE; NERVE CELL; NERVE CELL PLASTICITY; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; OPEN FIELD TEST; PLASMA CLEARANCE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; WESTERN BLOTTING; Y-MAZE TEST; ANIMAL; ANIMAL BEHAVIOR; CELL CULTURE; DOWN REGULATION; FOREBRAIN; GENETICS; KNOCKOUT MOUSE; MAZE TEST; METABOLIC CLEARANCE RATE; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; BEHAVIOR, ANIMAL; CELL SIZE; CELLS, CULTURED; DOWN-REGULATION; FEMALE; INSULIN-LIKE GROWTH FACTOR I; MALE; MAZE LEARNING; METABOLIC CLEARANCE RATE; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; NEURONS; PROSENCEPHALON; RECEPTOR, IGF TYPE 1; SIGNAL TRANSDUCTION;

EID: 84939824081     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0343-15.2015     Document Type: Article

References (63)

1. Attar A, Liu T, Chan WT, Hayes J, Nejad M, Lei K, Bitan G (2013) A shortened Barnes maze protocol reveals memory deficits at 4-months of age in the triple-transgenic mouse model of Alzheimer's disease. PLoS One 8:e80355. CrossRef Medline
2. Backman SA, Stambolic V, Suzuki A, Haight J, Elia A, Pretorius J, Tsao MS, Shannon P, Bolon B, Ivy GO, MakTW (2001) Deletion of Pten in mouse brain causes seizures, ataxia and defects in soma size resembling Lhermitte-Duclos disease. Nat Genet 29:396-403. CrossRef Medline
3. Barnes CA (1979) Memory deficits associated with senescence: a neurophysiological and behavioral study in the rat. J Comp Physiol Psychol 93:74 -104. CrossRef Medline
4. Biondi O, Branchu J, Ben Salah A, Houdebine L, Bertin L, Chali F, Desseille C, Weill L, Sanchez G, Lancelin C, Aı¨d S, Lopes P, Pariset C, Le´colle S, Coˆte´ J, Holzenberger M, Chanoine C, Massaad C, Charbonnier F (2015) IGF-1R reduction triggers neuroprotective signaling pathways in spinalmuscular- atrophy mice. J Neurosci. In press.
5. Bomfim TR, Forny-Germano L, Sathler LB, Brito-Moreira J, Houzel JC, Decker H, Silverman MA, Kazi H, Melo HM, McClean PL, Holscher C, Arnold SE, Talbot K, Klein WL, Munoz DP, Ferreira ST, De Felice FG (2012) An anti-diabetes agent protects the mouse brain from defective insulin signaling caused by Alzheimer's disease-associated Abeta oligomers. J Clin Invest 122:1339 -1353. CrossRef Medline
6. Brouillette J, Caillierez R, Zommer N, Alves-Pires C, Benilova I, Blum D, De Strooper B, Bue´e L (2012) Neurotoxicity and memory deficits induced by soluble low-molecular-weight amyloid-_1-42 oligomers are revealed in vivo by using a novel animal model. J Neurosci 32:7852-7861. CrossRef Medline
7. Caccamo A, Majumder S, Richardson A, Strong R, Oddo S (2010) Molecular interplay between mammalian target of rapamycin (mTOR), amyloid-beta, and Tau: effects on cognitive impairments. J Biol Chem 285:13107-13120. CrossRef Medline
8. Carro E, Trejo JL, Gomez-Isla T, LeRoith D, Torres-Aleman I (2002) Serum insulin-like growth factor I regulates brain amyloid-beta levels. Nat Med 8:1390 -1397. CrossRef Medline
9. Choi SH, Aid S, Caracciolo L, Minami SS, Niikura T, Matsuoka Y, Turner RS, Mattson MP, Bosetti F (2013) Cyclooxygenase-1 inhibition reduces amyloid pathology and improves memory deficits in a mouse model of Alzheimer's disease. J Neurochem 124:59-68. CrossRef Medline
10. Chva´tal A, Anderova´ M, Hock M, Prajerova´ I, Neprasova´ H, Chva´tal V, Kirchhoff F, Sykova´ E (2007) Three-dimensional confocal morphometry reveals structural changes in astrocyte morphology in situ. J Neurosci Res 85:260 -271. CrossRef Medline
11. Cloe¨tta D, Thomanetz V, Baranek C, Lustenberger RM, Lin S, Oliveri F, Atanasoski S, Ru¨egg MA (2013) Inactivation of mTORC1 in the developing brain causes microcephaly and affects gliogenesis. J Neurosci 33: 7799-7810. CrossRef Medline
12. Cohen E, Bieschke J, Perciavalle RM, Kelly JW, Dillin A (2006) Opposing activities protect against age-onset proteotoxicity. Science 313:1604- 1610. CrossRef Medline
13. Cohen E, Paulsson JF, Blinder P, Burstyn-Cohen T, Du D, Estepa G, Adame A, Pham HM, Holzenberger M, Kelly JW, Masliah E, Dillin A (2009) Reduced IGF-1 signaling delays age-associated proteotoxicity in mice. Cell 139:1157-1169. CrossRef Medline
14. Cooper KL, Oh S, Sung Y, Dasari RR, Kirschner MW, Tabin CJ (2013) Multiple phases of chondrocyte enlargement underlie differences in skeletal proportions. Nature 495:375-378. CrossRef Medline
15. Erdmann G, Schu¨tz G, Berger S (2007) Inducible gene inactivation in neurons of the adult mouse forebrain.BMCNeurosci 8:63. CrossRef Medline
16. Florez-McClure ML, Hohsfield LA, Fonte G, Bealor MT, Link CD (2007) Decreased insulin-receptor signaling promotes the autophagic degradation of beta-amyloid peptide in C. elegans. Autophagy 3:569-580. CrossRef Medline
17. Freude S, Hettich MM, Schumann C, Sto¨hr O, Koch L, Ko¨hler C, Udelhoven M, Leeser U, Mu¨ller M, Kubota N, Kadowaki T, Krone W, Schro¨der H, Bru¨ning JC, Schubert M (2009) Neuronal IGF-1 resistance reduces Abeta accumulation and protects against premature death in a model of Alzheimer's disease. FASEB J 23:3315-3324. CrossRef Medline
18. Fricano CJ, Despenza T Jr, Frazel PW, Li M, O'Malley AJ, Westbrook GL, Luikart BW (2014) Fatty acids increase neuronal hypertrophy of Pten knockdown neurons. Front Mol Neurosci 7:30. CrossRef Medline
19. Ghazi-Noori S, Froud KE, Mizielinska S, Powell C, Smidak M, Fernandez de Marco M, O'Malley C, Farmer M, Parkinson N, Fisher EM, Asante EA, Brandner S, Collinge J, Isaacs AM (2012) Progressive neuronal inclusion formation and axonal degeneration in CHMP2B mutant transgenic mice. Brain 135:819-832. CrossRef Medline
20. Gunji H, Little RA, Hiraiwa K (2002) Interleukin-6 deficiency increases blood volume without altering body composition in young mice. Cytokine 20:30 -37. CrossRef Medline
21. Heneka MT, Kummer MP, Stutz A, Delekate A, Schwartz S, Vieira-Saecker A, Griep A, Axt D, Remus A, Tzeng TC, Gelpi E, Halle A, Korte M, Latz E, Golenbock DT (2013) NLRP3 is activated in Alzheimer's disease and contributes to pathology in APP/PS1 mice. Nature 493:674-678. CrossRef Medline
22. Herculano-Houzel S, Watson C, Paxinos G (2013) Distribution of neurons in functional areas of the mouse cerebral cortex reveals quantitatively different cortical zones. Front Neuroanat 7:35. CrossRef Medline
23. Hirata-Fukae C, Li HF, Hoe HS, Gray AJ, Minami SS, Hamada K, Niikura T, Hua F, Tsukagoshi-Nagai H, Horikoshi-Sakuraba Y, Mughal M, Rebeck GW, LaFerla FM, Mattson MP, Iwata N, Saido TC, Klein WL, Duff KE, Aisen PS, Matsuoka Y (2008) Females exhibit more extensive amyloid, but not tau, pathology in an Alzheimer transgenic model. Brain Res 1216: 92-103. CrossRef Medline
24. Holzenberger M, Dupont J, Ducos B, Leneuve P, Ge´loe¨n A, Even PC, Cervera P, Le Bouc Y (2003) IGF-1 receptor regulates lifespan and resistance to oxidative stress in mice. Nature 421:182-187. CrossRef Medline
25. Iliadi KG, Knight D, Boulianne GL (2012) Healthy aging-insights from Drosophila. Front Physiol 3:106. CrossRef Medline
26. Jankowsky JL, Fadale DJ, Anderson J, Xu GM, Gonzales V, Jenkins NA, Copeland NG, Lee MK, Younkin LH, Wagner SL, Younkin SG, Borchelt DR (2004) Mutant presenilins specifically elevate the levels of the 42 residue beta-amyloid peptide in vivo: evidence for augmentation of a 42-specific gamma secretase. Hum Mol Genet 13:159 -170. Medline
27. Kappeler L, De Magalhaes Filho C, Dupont J, Leneuve P, Cervera P, Pe´rin L, Loudes C, Blaise A, Klein R, Epelbaum J, Le Bouc Y, Holzenberger M (2008) Brain IGF-1 receptors control mammalian growth and lifespan through a neuroendocrine mechanism. PLoS Biol 6:e254. CrossRef Medline
28. Kappeler L, De Magalhaes Filho C, Leneuve P, Xu J, Brunel N, Chatziantoniou C, Le Bouc Y, Holzenberger M (2009) Early postnatal nutrition determines somatotropic function in mice. Endocrinology 150:314 -323. CrossRef Medline
29. Kenyon CJ (2010) The genetics of ageing. Nature 464:504 -512. CrossRef Medline
30. Killick R, Scales G, Leroy K, Causevic M, Hooper C, Irvine EE, Choudhury AI, Drinkwater L, Kerr F, Al-Qassab H, Stephenson J, Yilmaz Z, Giese KP, Brion JP, Withers DJ, Lovestone S (2009) Deletion of Irs2 reduces amyloid deposition and rescues behavioural deficits in APP transgenic mice. Biochem Biophys Res Commun 386:257-262. CrossRef Medline
31. Klionsky DJ, Abdalla FC, Abeliovich H, Abraham RT, Acevedo-Arozena A, Adeli K, Agholme L, Agnello M, Agostinis P, Aguirre-Ghiso JA, Ahn HJ, Ait-Mohamed O, Ait-Si-Ali S, Akematsu T, Akira S, Al-Younes HM, Al- Zeer MA, Albert ML, Albin RL, Alegre-Abarrategui J, et al. (2012) Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 8:445-544. CrossRef Medline
32. Koistinaho M, Lin S, Wu X, Esterman M, Koger D, Hanson J, Higgs R, Liu F, Malkani S, Bales KR, Paul SM (2004) Apolipoprotein E promotes astrocyte colocalization and degradation of deposited amyloid-_ peptides. Nat Med 10:719 -726. CrossRef Medline
33. KwonCH, Zhu X, Zhang J, Knoop LL, Tharp R, Smeyne RJ, Eberhart CG, Burger PC, Baker SJ (2001) Pten regulates neuronal soma size: a mouse model of Lhermitte-Duclos disease. Nat Genet 29:404-411. CrossRef Medline
34. Larson ME, Sherman MA, Greimel S, Kuskowski M, Schneider JA, Bennett DA, Lesne´ SE (2012) Soluble _-synuclein is a novel modulator of Alzheimer's disease pathophysiology. J Neurosci 32:10253-10266. CrossRef Medline
35. Longo VD, Antebi A, Bartke A, Barzilai N, Brown-Borg HM, Caruso C, Curiel TJ, de Cabo R, Franceschi C, Gems D, Ingram DK, Johnson TE, Kennedy BK, Kenyon C, Klein S, Kopchick JJ, Lepperdinger G, Madeo F, Mirisola MG, Mitchell JR, et al. (2015) Interventions to slow aging in humans: are we ready? Aging Cell. Advance online publication. Retrieved July 6, 2015. CrossRef Medline
36. Madisen L, Zwingman TA, Sunkin SM, Oh SW, Zariwala HA, Gu H, Ng LL, Palmiter RD, Hawrylycz MJ, Jones AR, Lein ES, ZengH (2010) A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat Neurosci 13:133-140. CrossRef Medline
37. McDonald JM, Savva GM, Brayne C, Welzel AT, Forster G, Shankar GM, Selkoe DJ, Ince PG, Walsh DM, Walsh DM (2010) The presence of sodium dodecyl sulphate-stable Abeta dimers is strongly associated with Alzheimer-type dementia. Brain 133:1328 -1341. CrossRef Medline
38. Minami SS, Sidahmed E, Aid S, Shimoji M, Niikura T, Mocchetti I, Rebeck GW, Prendergast JS, Dealwis C, Wetzel R, Bosetti F, Matsuoka Y, Hoe HS, Turner RS (2010) Therapeutic versus neuroinflammatory effects of passive immunization is dependent onA_/amyloid burden in a transgenic mouse model of Alzheimer's disease. J Neuroinflammation 7:57. CrossRef Medline
39. Moloney AM, Griffin RJ, Timmons S, O'Connor R, Ravid R, O'Neill C (2010) Defects in IGF-1 receptor, insulin receptor and IRS-1/2 in Alzheimer's disease indicate possible resistance to IGF-1 and insulin signalling. Neurobiol Aging 31:224 -243. CrossRef Medline
40. Nilsson P, Loganathan K, Sekiguchi M, Matsuba Y, Hui K, Tsubuki S, Tanaka M, Iwata N, Saito T, Saido TC (2013) A_ secretion and plaque formation depend on autophagy. Cell Rep 5:61- 69. CrossRef Medline
41. Nixon RA (2013) The role of autophagy in neurodegenerative disease. Nat Med 19:983-997. CrossRef Medline
42. O'Leary TP, Brown RE (2009) Visuo-spatial learning and memory deficits on the Barnes maze in the 16-month-old APPswe/PS1dE9 mouse model of Alzheimer's disease. Behav Brain Res 201:120 -127. CrossRef Medline
43. Paxinos G, Franklin KBJ (2001) The mouse brain in stereotaxic coordinates. San Diego: Academic.
44. Reiserer RS, Harrison FE, Syverud DC, McDonald MP (2007) Impaired spatial learning in the APPSwe_PSEN1DeltaE9 bigenic mouse model of Alzheimer's disease. Genes Brain Behav 6:54-65. CrossRef Medline
45. Rivera EJ, Goldin A, Fulmer N, Tavares R, Wands JR, de la Monte SM (2005) Insulin and insulin-like growth factor expression and function deteriorate with progression of Alzheimer's disease: link to brain reductions in acetylcholine. J Alzheimers Dis 8:247-268. Medline
46. Sebastiani P, Perls TT (2012) The genetics of extreme longevity: lessons from the New England Centenarian Study. Front Genet 3:277. CrossRef Medline
47. Serrano-Pozo A, William CM, Ferrer I, Uro-Coste E, Delisle MB, Maurage CA, Hock C, Nitsch RM, Masliah E, Growdon JH, Frosch MP, Hyman BT (2010) Beneficial effect of human anti-amyloid-beta active immunization on neurite morphology and tau pathology. Brain 133:1312-1327. CrossRef Medline
48. Shankar GM, Li S, Mehta TH, Garcia-Munoz A, Shepardson NE, Smith I, Brett FM, Farrell MA, Rowan MJ, Lemere CA, Regan CM, Walsh DM, Sabatini BL, Selkoe DJ (2008) Amyloid-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat Med 14:837- 842. CrossRef Medline
49. Steele JW, Lachenmayer ML, Ju S, Stock A, Liken J, Kim SH, Delgado LM, Alfaro IE, Bernales S, Verdile G, Bharadwaj P, Gupta V, Barr R, Friss A, Dolios G, Wang R, Ringe D, Fraser P, Westaway D, St George-Hyslop PH, et al. (2013) Latrepirdine improves cognition and arrests progression of neuropathology in an Alzheimer's mouse model. Mol Psychiatry 18:889- 897. CrossRef Medline
50. Steen E, Terry BM, Rivera EJ, Cannon JL, Neely TR, Tavares R, Xu XJ, Wands JR, de la Monte SM (2005) Impaired insulin and insulin-like growth factor expression and signaling mechanisms in Alzheimer's disease-is this type 3 diabetes? J Alzheimers Dis 7:63- 80. Medline
51. Stewart S, Cacucci F, Lever C (2011) Which memory task for my mouse? A systematic review of spatial memory performance in the Tg2576 Alzheimer's mouse model. J Alzheimers Dis 26:105-126. CrossRef Medline
52. Taguchi A, WartschowLM,WhiteMF (2007) Brain IRS2 signaling coordinates life span and nutrient homeostasis. Science 317:369-372. CrossRef Medline
53. Talbot K, Wang HY, Kazi H, Han LY, Bakshi KP, Stucky A, Fuino RL, Kawaguchi KR, Samoyedny AJ, Wilson RS, Arvanitakis Z, Schneider JA, Wolf BA, Bennett DA, Trojanowski JQ, Arnold SE (2012) Demonstrated brain insulin resistance in Alzheimer's disease patients is associated with IGF-1 resistance, IRS-1 dysregulation, and cognitive decline. J Clin Invest 122:1316 -1338. CrossRef Medline
54. Tavazoie SF, Alvarez VA, Ridenour DA, Kwiatkowski DJ, Sabatini BL (2005) Regulation of neuronal morphology and function by the tumor suppressors Tsc1 and Tsc2. Nat Neurosci 8:1727-1734. CrossRef Medline
55. Thomanetz V, Angliker N, Cloe¨tta D, Lustenberger RM, Schweighauser M, Oliveri F, Suzuki N, Ru¨egg MA (2013) Ablation of the mTORC2 component rictor in brain or Purkinje cells affects size and neuron morphology. J Cell Biol 201:293-308. CrossRef Medline
56. van Diepen MT, Parsons M, Downes CP, Leslie NR, Hindges R, Eickholt BJ (2009) MyosinV controls PTEN function and neuronal cell size. Nat Cell Biol 11:1191-1196. CrossRef Medline
57. Wang J, Zhou J, Bondy CA (1999) Igf1 promotes longitudinal bone growth by insulin-like actions augmenting chondrocyte hypertrophy. FASEB J 13:1985-1990. Medline
58. Wang J, Tanila H, Puoliva¨li J, Kadish I, van Groen T (2003) Gender differences in the amount and deposition of amyloidbeta in APPswe and PS1 double transgenic mice. Neurobiol Dis 14:318 -327. CrossRef Medline
59. Xie L, Kang H, Xu Q, Chen MJ, Liao Y, Thiyagarajan M, O'Donnell J, Christensen DJ, Nicholson C, Iliff JJ, Takano T, Deane R, Nedergaard M (2013) Sleep drives metabolite clearance from the adult brain. Science 342:373-377. CrossRef Medline
60. Xu J, Gontier G, Chaker Z, Lacube P, Dupont J, Holzenberger M (2014) Longevity effect of IGF-1R mutation depends on genetic backgroundspecific receptor activation. Aging Cell 13:19 -28. CrossRef Medline
61. Yang DS, Stavrides P, Mohan PS, Kaushik S, Kumar A, Ohno M, Schmidt SD, Wesson D, Bandyopadhyay U, Jiang Y, Pawlik M, Peterhoff CM, Yang AJ, Wilson DA, St George-Hyslop P, Westaway D, Mathews PM, Levy E, Cuervo AM, Nixon RA (2011) Reversal of autophagy dysfunction in the TgCRND8 mouse model of Alzheimer's disease ameliorates amyloid pathologies and memory deficits. Brain 134:258 -277. CrossRef Medline
62. Yang DS, Stavrides P, Saito M, Kumar A, Rodriguez-Navarro JA, Pawlik M, Huo C, Walkley SU, Saito M, Cuervo AM, Nixon RA (2014) Defective macroautophagic turnover of brain lipids in the TgCRND8 Alzheimer mouse model: prevention by correcting lysosomal proteolytic deficits. Brain 137:3300 -3318. CrossRef Medline
63. Zhang G, Li J, Purkayastha S, Tang Y, Zhang H, Yin Y, Li B, Liu G, Cai D (2013) Hypothalamic programming of systemic ageing involving IKKbeta, NF-kappaB and GnRH. Nature 497:211-216. CrossRef Medline