Rapamycin suppresses brain aging in senescence-accelerated OXYS rats

Aging

Volumn 5, Issue 6, 2013, Pages 474-484

  Kolosova, Nataliya G ^a   Vitovtov, Anton O ^a   Muraleva, Natalia A ^a   Akulov, Andrey E ^a   Stefanova, Natalia A ^a   Blagosklonny, Mikhail V ^b  

^a INSTITUTE OF CYTOLOGY AND GENETICS   (Russian Federation)

^b ROSWELL PARK CANCER INSTITUTE   (United States)

Author keywords

Age related diseases; Aging; brain; MTOR; mTOR

Indexed keywords

EID: 84880634185     PISSN: 19454589     EISSN: None     Source Type: Journal    
DOI: 10.18632/aging.100573     Document Type: Article

References (56)

1. Loewith R, Hall MN. Target of rapamycin (TOR) in nutrient signaling and growth control. Genetics. 2011; 189: 1177-1201.
2. Sengupta S, Peterson TR, Sabatini DM. Regulation of the mTOR complex 1 pathway by nutrients, growth factors, and stress. Mol Cell. 2010; 40: 310-322.
3. Sarbassov dos D, Ali SM, Sabatini DM. Growing roles for the mTOR pathway. Curr Opin Cell Biol. 2005; 17: 596-603.
4. Duran RV, Hall MN. Glutaminolysis feeds mTORC1. Cell Cycle. 2012; 11: 4107-4108.
5. Demidenko ZN, Blagosklonny MV. Growth stimulation leads to cellular senescence when the cell cycle is blocked. Cell Cycle. 2008; 7: 3355-3361.
6. Leontieva OV, Blagosklonny MV. DNA damaging agents and p53 do not cause senescence in quiescent cells, while consecutive re-activation of mTOR is associated with conversion to senescence. Aging (Albany NY). 2010; 2: 924-935.
7. Chen C, Liu Y, Zheng P. mTOR regulation and therapeutic rejuvenation of aging hematopoietic stem cells. Sci Signal. 2009; 2: ra75.
8. Mercier I, Camacho J, Titchen K, Gonzales DM, Quann K, Bryant KG, Molchansky A, Milliman JN, Whitaker-Menezes D, Sotgia F, Jasmin JF, Schwarting R, Pestell RG, Blagosklonny MV, Lisanti MP. Caveolin-1 and accelerated host aging in the breast tumor microenvironment: chemoprevention with rapamycin, an mTOR inhibitor and anti-aging drug. Am J Pathol. 2012; 181: 278-293.
9. Blagosklonny MV. Cell cycle arrest is not yet senescence, which is not just cell cycle arrest: terminology for TOR-driven aging. Aging (Albany NY). 2012; 4: 159-165.
10. Kapahi P, Zid BM, Harper T, Koslover D, Sapin V, Benzer S. Regulation of lifespan in Drosophila by modulation of genes in the TOR signaling pathway. Curr Biol. 2004; 14: 885-890.
11. Selman C, Tullet JM, Wieser D, Irvine E, Lingard SJ, Choudhury AI, Claret M, Al-Qassab H, Carmignac D, Ramadani F, Woods A, Robinson IC, Schuster E, Batterham RL, Kozma SC, Thomas G et al. Ribosomal protein S6 kinase 1 signaling regulates mammalian life span. Science. 2009; 326: 140-144.
12. Harrison DE, Strong R, Sharp ZD, Nelson JF, Astle CM, Flurkey K, Nadon NL, Wilkinson JE, Frenkel K, Carter CS, Pahor M, Javors MA, Fernandezr E, Miller RA. Rapamycin fed late in life extends lifespan in genetically heterogenous mice. Nature. 2009; 460: 392-396.
13. Miller RA, Harrison DE, Astle CM, Baur JA, Boyd AR, de Cabo R, Fernandez E, Flurkey K, Javors MA, Nelson JF, Orihuela CJ, Pletcher S, Sharp ZD, Sinclair D, Starnes JW, Wilkinson JE et al. Rapamycin, but not resveratrol or simvastatin, extends life span of genetically heterogeneous mice. J Gerontol A Biol Sci Med Sci. 2011; 66: 191-201.
14. Anisimov VN, Zabezhinski MA, Popovich IG, Piskunova TS, Semenchenko AV, Tyndyk ML, Yurova MN, Antoch MP, Blagosklonny MV. Rapamycin extends maximal lifespan in cancer-prone mice. Am J Pathol. 2010; 176: 2092-2097.
15. Anisimov VN, Zabezhinski MA, Popovich IG, Piskunova TS, Semenchenko AV, Tyndyk ML, Yurova MN, Rosenfeld SV, Blagosklonny MV. Rapamycin increases lifespan and inhibits spontaneous tumorigenesis in inbred female mice. Cell Cycle. 2011; 10: 4230-4236.
16. Wilkinson JE, Burmeister L, Brooks SV, Chan CC, Friedline S, Harrison DE, Hejtmancik JF, Nadon N, Strong R, Wood LK, Woodward MA, Miller RA. Rapamycin slows aging in mice. Aging Cell. 2012; 11: 675-682.
17. Spong A, Bartke A. Rapamycin slows aging in mice. Cell Cycle. 2012; 11: 845.
18. Moskalev AA, Shaposhnikov MV. Pharmacological Inhibition of Phosphoinositide 3 and TOR Kinases Improves Survival of Drosophila melanogaster. Rejuvenation Res. 2010; 13: 246-247.
19. Bjedov I, Toivonen JM, Kerr F, Slack C, Jacobson J, Foley A, Partridge L. Mechanisms of life span extension by rapamycin in the fruit fly Drosophila melanogaster. Cell Metab. 2010; 11: 35-46.
20. Stanfel MN, Shamieh LS, Kaeberlein M, Kennedy BK. The TOR pathway comes of age. Biochim Biophys Acta. 2009; 1790: 1067-1074.
21. Johnson SC, Rabinovitch PS, Kaeberlein M. mTOR is a key modulator of ageing and age-related disease. Nature. 2013; 493:338-345.
22. Khanna A, Kapahi P. Rapamycin: killing two birds with one stone. Aging (Albany NY). 2011; 3: 1043-1044.
23. Spilman P, Podlutskaya N, Hart MJ, Debnath J, Gorostiza O, Bredesen D, Richardson A, Strong R, Galvan V. Inhibition of mTOR by rapamycin abolishes cognitive deficits and reduces amyloid-beta levels in a mouse model of Alzheimer's disease. PLoS One. 2010; 5: e9979.
24. Majumder S, Caccamo A, Medina DX, Benavides AD, Javors MA, Kraig E, Strong R, Richardson A, Oddo S. Lifelong rapamycin administration ameliorates age-dependent cognitive deficits by reducing IL-1beta and enhancing NMDA signaling. Aging Cell. 2012; 11: 326-335.
25. Halloran J, Hussong SA, Burbank R, Podlutskaya N, Fischer KE, Sloane LB, Austad SN, Strong R, Richardson A, Hart MJ, Galvan V. Chronic inhibition of mammalian target of rapamycin by rapamycin modulates cognitive and non-cognitive components of behavior throughout lifespan in mice. Neuroscience. 2012; 223: 102-113.
26. Lang UE, Heger J, Willbring M, Domula M, Matschke K, Tugtekin SM. Immunosuppression using the mammalian target of rapamycin (mTOR) inhibitor everolimus: pilot study shows significant cognitive and affective improvement. Transplant Proc. 2009; 41: 4285-4288.
27. Lhotellier L, Perez-Diaz F, Cohen-Salmon C. Locomotor and exploratory activity in three inbred strains of mice from young adulthood to senescence. Exp Aging Res. 1993; 19: 177-187.
28. Frussa-Filho R, Otoboni JR, Giannotti AD, Amaral AC, Conceicao IM. Effect of age on antinociceptive effects of elevated plus-maze exposure. Braz J Med Biol Res. 1992; 25: 827-829.
29. Chen GH, Wang C, Yangcheng HY, Liu RY, Zhou JN. Agerelated changes in anxiety are task-specific in the senescenceaccelerated prone mouse 8. Physiol Behav. 2007; 91: 644-651.
30. Kolosova NG, Trofimova NA, Fursova A. Opposite effects of antioxidants on anxiety in Wistar and OXYS rats. Bull Exp Biol Med. 2006; 141: 734-737.
31. Sergeeva S, Bagryanskaya E, Korbolina E, Kolosova N. Development of behavioural dysfunctions in acceleratedsenescence OXYS rats is associated with early postnatal alterations in brain phosphate metabolism. Exp Gerontol. 2006; 41: 141-150.
32. Kolosova NG, Stefanova NA, Muraleva NA, Skulachev VP. The mitochondria-targeted antioxidant SkQ1 but not Nacetylcysteine reverses aging-related biomarkers in rats. Aging (Albany NY). 2012; 4: 686-694.
33. Stefanova NA, Fursova A, Sarsenbaev KN, Kolosova NG. Effects of Cistanche deserticola on behavior and signs of cataract and retinopathy in senescence-accelerated OXYS rats. J Ethnopharmacol. 2011; 138: 624-632.
34. Stefanova NA, Fursova A, Kolosova NG. Behavioral effects induced by mitochondria-targeted antioxidant SkQ1 in Wistarand senescence-accelerated OXYS rats. J Alzheimers Dis. 2010; 21: 479-491.
35. Kolosova NG, Muraleva NA, Zhdankina AA, Stefanova NA, Fursova AZ, Blagosklonny MV. Prevention of age-related macular degeneration-like retinopathy by rapamycin in rats. Am J Pathol. 2012; 181: 472-477.
36. Loskutova LV, Kolosova NG. Emotional state and one-trial learning in OXYS rats with hereditarily elevated production of oxygen radicals. Bull Exp Biol Med. 2000; 130: 746-748.
37. Markova EV, Obukhova LA, Kolosova NG. Parameters of cell immune response in Wistar and OXYS rats and their behavior in the open field test. Bull Exp Biol Med. 2003; 136: 588-590.
38. Markova EV, Kozlov VA, Trofimova NA, Kolosova NG. Stimulation of cell component of the immune response activates exploratory behavior in senescence accelerated OXYS rats. Bull Exp Biol Med. 2005; 140: 345-347.
39. Agafonova IG, Kotel'nikov VN, Mischenko NP, Kolosova NG. Evaluation of effects of histochrome and mexidol on structural and functional characteristics of the brain in senescenceaccelerated OXYS rats by magnetic resonance imaging. Bull Exp Biol Med. 2011; 150: 739-743.
40. Beregovoy NA, Sorokina NS, Starostina MV, Kolosova NG. Age-specific peculiarities of formation of long-term posttetanic potentiation in OXYS rats. Bull Exp Biol Med. 2011; 151: 71-73.
41. Iijima Y, Laser M, Shiraishi H, Willey CD, Sundaravadivel B, Xu L, McDermott PJ, Kuppuswamy D. c-Raf/MEK/ERK pathway controls protein kinase C-mediated p70S6K activation in adult cardiac muscle cells. J Biol Chem. 2002; 277: 23065-23075.
42. Salmond RJ, Emery J, Okkenhaug K, Zamoyska R. MAPK, phosphatidylinositol 3-kinase, and mammalian target of rapamycin pathways converge at the level of ribosomal protein S6 phosphorylation to control metabolic signaling in CD8 T cells. J Immunol. 2009; 183: 7388-7397.
43. Abe Y, Yoon SO, Kubota K, Mendoza MC, Gygi SP, Blenis J. p90 ribosomal S6 kinase and p70 ribosomal S6 kinase link phosphorylation of the eukaryotic chaperonin containing TCP-1 to growth factor, insulin, and nutrient signaling. J Biol Chem. 2009; 284: 14939-14948.
44. Chiu C, Miller MC, Caralopoulos IN, Worden MS, Brinker T, Gordon ZN, Johanson CE, Silverberg GD. Temporal course of cerebrospinal fluid dynamics and amyloid accumulation in the aging rat brain from three to thirty months. Fluids Barriers CNS. 2012; 9: 3.
45. Chambraud B, Sardin E, Giustiniani J, Dounane O, Schumacher M, Goedert M, Baulieu EE. A role for FKBP52 in Tau protein function. Proc Natl Acad Sci U S A. 2010; 107: 2658-2663.
46. Avila J, de Barreda EG, Pallas-Bazarra N, Hernandez F. Tau and neuron aging. Aging Dis. 2013; 4: 23-28.
47. Dassie E, Andrews MR, Bensadoun JC, Cacquevel M, Schneider BL, Aebischer P, Wouters FS, Richardson JC, Hussain I, Howlett DR, Spillantini MG, Fawcett JW. Focal expression of adeno-associated viral-mutant tau induces widespread impairment in an APP mouse model. Neurobiol Aging. 2013; 34: 1355-1368.
48. Steinhilb ML, Dias-Santagata D, Fulga TA, Felch DL, Feany MB. Tau phosphorylation sites work in concert to promote neurotoxicity in vivo. Mol Biol Cell. 2007; 18: 5060-5068.
49. Inoue K, Rispoli J, Kaphzan H, Klann E, Chen EI, Kim J, Komatsu M, Abeliovich A. Macroautophagy deficiency mediates age-dependent neurodegeneration through a phospho-tau pathway. Mol Neurodegener. 7: 48.
50. Lenart N, Szegedi V, Juhasz G, Kasztner A, Horvath J, Bereczki E, Toth ME, Penke B, Santha M. Increased tau phosphorylation and impaired presynaptic function in hypertriglyceridemic ApoB-100 transgenic mice. PLoS One. 7: e46007.
51. Caccamo A, Magri A, Medina DX, Wisely EV, Lopez-Aranda MF, Silva AJ, Oddo S. mTOR regulates tau phosphorylation and degradation: implications for Alzheimer's disease and other tauopathies. Aging Cell. 2013; 12: 370-380.
52. Li X, Alafuzoff I, Soininen H, Winblad B, Pei JJ. Levels of mTOR and its downstream targets 4E-BP1, eEF2, and eEF2 kinase in relationships with tau in Alzheimer's disease brain. Febs J. 2005; 272: 4211-4220.
53. Meske V, Albert F, Ohm TG. Coupling of mammalian target of rapamycin with phosphoinositide 3-kinase signaling pathway regulates protein phosphatase 2A- and glycogen synthase kinase-3 -dependent phosphorylation of Tau. J Biol Chem. 2008; 283: 100-109.
54. Tang Z, Bereczki E, Zhang H, Wang S, Li C, Ji X, Branca RM, Lehtio J, Guan Z, Filipcik P, Xu S, Winblad B, Pei JJ. Mammalian Target of Rapamycin (mTor) Mediates Tau Protein Dyshomeostasis: IMPLICATION FOR ALZHEIMER DISEASE. J Biol Chem. 2013; 288: 15556-15570.
55. Khurana V, Lu Y, Steinhilb ML, Oldham S, Shulman JM, Feany MB. TOR-mediated cell-cycle activation causes neurodegeneration in a Drosophila tauopathy model. Curr Biol. 2006; 16: 230-241.
56. Blagosklonny MV. An anti-aging drug today: from senescence-promoting genes to anti-aging pill. Drug Disc Today. 2007; 12: 218-224.