FOXO3a is broadly neuroprotective in vitro and in vivo against insults implicated in motor neuron diseases

Journal of Neuroscience

Volumn 29, Issue 25, 2009, Pages 8236-8247

  Mojsilovic Petrovic, Jelena ^a   Nedelsky, Natalia ^b,g   Boccitto, Marco ^a   Mano, Itzhak ^c,j   Georgiades, Savvas N ^d,h   Zhou, Weiguo ^a   Liu, Yuhong ^e   Neve, Rachael L ^f,i   Taylor, J Paul ^b,g   Driscoll, Monica ^c   Clardy, Jon ^d   Merry, Diane ^e   Kalb, Robert G ^a,b  

^a CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c RUTGERS UNIVERSITY   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

^e THOMAS JEFFERSON UNIVERSITY   (United States)

^f MCLEAN HOSPITAL   (United States)

^g ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^h IMPERIAL COLLEGE LONDON   (United Kingdom)

ⁱ MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^j CITY UNIVERSITY OF NEW YORK   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN RECEPTOR; TRANSCRIPTION FACTOR DAF 16; TRANSCRIPTION FACTOR FKHRL1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; EXCITOTOXICITY; IN VITRO STUDY; IN VIVO STUDY; MALE; MOTOR NEURON DISEASE; MOUSE; NERVE CELL NECROSIS; NERVE DEGENERATION; NEUROPROTECTION; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION;

ANIMALS; BLOTTING, WESTERN; CELL COUNT; CELL CULTURE TECHNIQUES; CELL DEATH; COMPUTATIONAL BIOLOGY; DISEASE MODELS, ANIMAL; DROSOPHILA; EMBRYO, MAMMALIAN; EXCITATORY AMINO ACID AGONISTS; FEMALE; FLUORESCENCE; FORKHEAD TRANSCRIPTION FACTORS; IMMUNOHISTOCHEMISTRY; KAINIC ACID; MICE; MICE, INBRED C57BL; MOTOR NEURON DISEASE; MOTOR NEURONS; NEUROPROTECTIVE AGENTS; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; SPINAL CORD; TYROSINE;

EID: 67649366086     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1805-09.2009     Document Type: Article

References (63)

1. Barthélémy C, Henderson CE, Pettmann B (2004) Foxo3a induces motoneuron death through the Fas pathway in cooperation with JNK. BMC Neurosci 5:48. (Pubitemid 40177033)
2. Berdichevsky A, Viswanathan M, Horvitz HR, Guarente L (2006) C. elegans SIR-2.1 interacts with 14-3-3 proteins to activate DAF-16 and extend life span. Cell 125:1165-1177.
3. s-induced neurodegeneration in Caenorhabditis elegans. J Neurosci 18:2871-2880.
4. Birkenkamp KU, Coffer PJ (2003) Regulation of cell survival and proliferation by the FOXO (Forkhead box, class O) subfamily of Forkhead transcription factors. Biochem Soc Trans 31:292-297. (Pubitemid 36241447)
5. Boillée S, Vande Velde C, Cleveland DW (2006) ALS: a disease of motor neurons and their nonneuronal neighbors. Neuron 52:39-59. (Pubitemid 44466358)
6. Bruijn LI, Becher MW, Lee MK, Anderson KL, Jenkins NA, Copeland NG, Sisodia SS, Rothstein JD, Borchelt DR, Price DL, Cleveland DW (1997) ALS-linked SOD1 mutant G85R mediates damage to astrocytes and promotes rapidly progressive disease with SOD1-containing inclusions. Neuron 18:327-338. (Pubitemid 27111114)
7. Bruijn LI, Miller TM, Cleveland DW (2004) Unraveling the mechanisms involved in motor neuron degeneration in ALS. Annu Rev Neurosci 27:723-749. (Pubitemid 39050419)
8. Brunet A, Bonni A, Zigmond MJ, Lin MZ, Juo P, Hu LS, Anderson MJ, Arden KC, Blenis J, Greenberg ME (1999) Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96:857-868. (Pubitemid 29165088)
9. Brunet A, Park J, Tran H, Hu LS, Hemmings BA, Greenberg ME (2001) Protein kinase SGK mediates survival signals by phosphorylating the Forkhead Transcription Facotr FKHRL1 (FOXO3a). Mol Cell Biol 21:952-965. (Pubitemid 32104742)
10. Brunet A, Sweeney LB, Sturgill JF, Chua KF, Greer PL, Lin Y, Tran H, Ross SE, Mostoslavsky R, Cohen HY, Hu LS, Cheng HL, Jedrychowski MP, Gygi SP, Sinclair DA, Alt FW, Greenberg ME (2004) Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science 303:2011-2015. (Pubitemid 38393275)
11. Chevalier-Larsen ES, O'Brien CJ, Wang H, Jenkins SC, Holder L, Lieberman AP, Merry DE (2004) Castration restores function and neurofilament alterations of aged symptomatic males in a transgenic mouse model of spinal and bulbar muscular atrophy. J Neurosci 24:4778-4786.
12. Cleveland DW, Rothstein JD (2001) From Charcot to Lou Gehrig: deciphering selective motor neuron death in ALS. Nat Rev Neurosci 2:806-819. (Pubitemid 33674062)
13. Cohen E, Bieschke J, Perciavalle RM, Kelly JW, Dillin A (2006) Opposing activities protect against age-onset proteotoxicity. Science 313:1604-1610. (Pubitemid 44414028)
14. Dionne MS, Pham LN, Shirasu-Hiza M, Schneider DS (2006) Akt and FOXOdysregulation contribute to infection-induced wasting in Drosophila. Curr Biol 16:1977-1985. (Pubitemid 44573814)
15. Dunckley T, Huentelman MJ, Craig DW, Pearson JV, Szelinger S, Joshipura K, Halperin RF, Stamper C, Jensen KR, Letizia D, Hesterlee SE, Pestronk A, Levine T, Bertorini T, Graves MC, Mozaffar T, Jackson CE, Bosch P, McVey A, Dick A, et al. (2007) Whole-genome analysis of sporadic amyotrophic lateral sclerosis. N Engl J Med 357:775-788. (Pubitemid 47295644)
16. Ernfors P, Lee KF, Jaenisch R (1994) Mice lacking brain-derived neurotrophic factor develop with sensory deficits. Nature 368:147-150. (Pubitemid 24101525)
17. Finkel T, Holbrook NJ (2000) Oxidants, oxidative stress and the biology of ageing. Nature 408:239-247. (Pubitemid 30839429)
18. Frey D, Schneider C, Xu L, Borg J, Spooren W, Caroni P (2000) Early and selective loss of neuromuscular synapse subtypes with low sprouting competence in motoneuron diseases. J Neurosci 20:2534-2542. (Pubitemid 30220340)
19. Friedman DB, Johnson TE (1988) A mutation in the age-1 gene in Caenorhabditis elegans lengthens life and reduces hermaphrodite fertility. Genetics 118:75-86.
20. Fryer HJ, Knox RJ, Strittmatter SM, Kalb RG (1999) Excitotoxic death of a subset of embryonic rat motor neurons in vitro. J Neurochem 72:500-513. (Pubitemid 29055211)
21. Fryer HJ, Wolf DH, Knox RJ, Strittmatter SM, Pennica D, O'Leary RM, Russell DS, Kalb RG (2000) Brain-derived neurotrophic factor induces excitotoxic sensitivity in cultured embryonic rat spinal motor neurons through activation of the phosphatidylinositol 3-kinase pathway. J Neurochem 74:582-595. (Pubitemid 30053730)
22. Georgiades SN, Clardy J (2005) Total synthesis of psammaplysenes A and B, naturally occurring inhibitors of FOXO1a nuclear export. Org Lett 7:4091-4094. (Pubitemid 41361536)
23. Georgiades SN, Clardy J (2006) Preparation of a psammaplysene-based library. Org Lett 8:4251-4254. (Pubitemid 44449954)
24. Greer EL, Brunet A (2005) FOXO transcription factors at the interface between longevity and tumor suppression. Oncogene 24:7410-7425. (Pubitemid 41637981)
25. Greer EL, Oskoui PR, Banko MR, Maniar JM, Gygi MP, Gygi SP, Brunet A (2007a) The energy sensor AMP-activated protein kinase directly regulates the mammalian FOXO3 transcription factor. J Biol Chem 282:30107-30119. (Pubitemid 350035296)
26. Greer EL, Dowlatshahi D, Banko MR, Villen J, Hoang K, Blanchard D, Gygi SP, Brunet A (2007b) An AMPK-FOXO pathway mediates longevity induced by a novel method of dietary restriction in C. elegans. Curr Biol 17:1646-1656. (Pubitemid 47503807)
27. Hekimi S, Guarente L (2003) Genetics and the specificity of the aging process. Science 299:1351-1354. (Pubitemid 36254640)
28. Hsu AL, Murphy CT, Kenyon C (2003) Regulation of aging and age-related disease by DAF-16 and heat-shock factor. Science 300:1142-1145. (Pubitemid 36583098)
29. Hu JH, Chernoff K, Pelech S, Krieger C (2003) Protein kinase and protein phosphatase expression in the central nervous system of G93A mSOD over-expressing mice. J Neurochem 85:422-431. (Pubitemid 36438337)
30. Hu MC, Lee DF, Xia W, Golfman LS, Ou-Yang F, Yang JY, Zou Y, Bao S, Hanada N, Saso H, Kobayashi R, Hung MC (2004) IkappaB kinase promotes tumorigenesis through inhibition of forkhead FOXO3a. Cell 117:225-237. (Pubitemid 38496242)
31. Hu P, Kalb RG (2003) BDNF heightens the sensitivity of motor neurons to excitotoxic insults through activation of TrkB. J Neurochem 84:1421-1430. (Pubitemid 36343608)
32. Jünger MA, Rintelen F, Stocker H, Wasserman JD, Végh M, Radimerski T, Greenberg ME, Hafen E (2003) The Drosophila forkhead transcription factor FOXO mediates the reduction in cell number associated with reduced insulin signaling. J Biol 2:20.
33. Kasperaviciute D, Weale ME, Shianna KV, Banks GT, Simpson CL, Hansen VK, Turner MR, Shaw CE, Al-Chalabi A, Pall HS, Goodall EF, Morrison KE, Orrell RW, Beck M, Jablonka S, Sendtner M, Brockington A, Ince PG, Hartley J, Nixon H, Shaw PJ, Schiavo G, Wood NW, Goldstein DB, Fisher EM (2007) Large-scale pathways-based association study in amyotrophic lateral sclerosis. Brain 130:2292-2301. (Pubitemid 47327621)
34. Kau TR, Schroeder F, Ramaswamy S, Wojciechowski CL, Zhao JJ, Roberts TM, Clardy J, Sellers WR, Silver PA (2003) A chemical genetic screen identifies inhibitors of regulated nuclear export of a Forkhead transcription factor in PTEN-deficient tumor cells. Cancer Cell 4:463-476. (Pubitemid 38050043)
35. Klöcker N, Cellerino A, Bähr M (1998) Free radical scavenging and inhibition of nitric oxide synthase potentiates the neurotrophic effects of brain-derived neurotrophic factor on axotomized retinal ganglion cells in vivo. J Neurosci 18:1038-1046. (Pubitemid 28112925)
36. Koh JY, Gwag BJ, Lobner D, Choi DW (1995) Potentiated necrosis of cultured cortical neurons by neurotrophins. Science 268:573-575.
37. Koliatsos VE, Clatterbuck RE, Winslow JW, Cayouette MH, Price DL (1993) Evidence that brain-derived neurotrophic factor is a trophic factor for motor neurons in vivo. Neuron 10:359-367. (Pubitemid 23111729)
38. Kops GJ, Dansen TB, Polderman PE, Saarloos I, Wirtz KW, Coffer PJ, Huang TT, Bos JL, Medema RH, Burgering BM (2002) Forkhead transcription factor FOXO3a protects quiescent cells from oxidative stress. Nature 419:316-321.
39. La Spada AR, Wilson EM, Lubahn DB, Harding AE, Fischbeck KH (1991) Androgen receptor gene mutations in X-linked spinal and bulbar muscular atrophy. Nature 352:77-79. (Pubitemid 21896702)
40. Leenders H, Whiffield S, Benoist C, Mathis D (2000) Role of the forkhead transcription family member, FKHR, in thymocyte differentiation. Eur J Immunol 30:2980-2990. (Pubitemid 30786029)
41. Lin MT, Beal MF (2006) Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 443:787-795. (Pubitemid 44622683)
42. Lobsiger CS, Cleveland DW (2007) Glial cells as intrinsic components of non-cell-autonomous neurodegenerative disease. Nat Neurosci 10:1355-1360. (Pubitemid 350014678)
43. Longo VD, Finch CE (2003) Evolutionary medicine: from dwarf model systems to healthy centenarians? Science 299:1342-1346.
44. Mano I, Driscoll M (2009) Caenorhabditis elegans glutamate transporter deletion induces AMPA-receptor/adenylyl cyclase 9-dependent excitotoxicity. J Neurochem 108:1373-1384.
45. Mojsilovic-Petrovic J, Jeong GB, Crocker A, Arneja A, David S, Russell DS, Russell D, Kalb RG (2006) Protecting motor neurons from toxic insult by antagonism of adenosine A2a and Trk receptors. J Neurosci 26:9250-9263. (Pubitemid 44359851)
46. Morley JF, Morimoto RI (2004) Regulation of longevity in Caenorhabditis elegans by heat shock factor and molecular chaperones. Mol Biol Cell 15:657-664.
47. Mourelatos Z, Gonatas NK, Stieber A, Gurney ME, Dal Canto MC (1996) The Golgi apparatus of spinal cord motor neurons in transgenic mice expressing mutant Cu, Zn superoxide dismutase becomes fragmented in early, preclinical stages of the disease. Proc Natl Acad Sci U S A 93:5472-5477. (Pubitemid 26159474)
48. Nakamura N, Ramaswamy S, Vazquez F, Signoretti S, Loda M, Sellers WR (2000) Forkhead transcription factors are critical effectors of cell death and cell cycle arrest downstream of PTEN. Mol Cell Biol 20:8969-8982. (Pubitemid 32245927)
49. Nemoto S, Finkel T (2002) Redox regulation of forkhead proteins through a p66shc-dependent signaling pathway. Science 295:2450-2452. (Pubitemid 34270258)
50. Neve RL, Howe JR, Hong S, Kalb RG (1997) Introduction of the glutamate receptor subunit 1 into motor neurons in vitro and in vivo using a recombinant herpes simplex virus. Neuroscience 79:435-447. (Pubitemid 27232401)
51. Pandey UB, Nie Z, Batlevi Y, McCray BA, Ritson GP, Nedelsky NB, Schwartz SL, DiProspero NA, Knight MA, Schuldiner O, Padmanabhan R, Hild M, Berry DL, Garza D, Hubbert CC, Yao TP, Baehrecke EH, Taylor JP (2007) HDAC6rescues neurodegeneration and provides an essential link between autophagy and the UPS. Nature 447:859-863. (Pubitemid 46920134)
52. Pasinelli P, Brown RH (2006) Molecular biology of amyotrophic lateral sclerosis: insights from genetics. Nat Rev Neurosci 7:710-723. (Pubitemid 44267495)
53. Pun S, Santos AF, Saxena S, Xu L, Caroni P (2006) Selective vulnerability and pruning of phasic motoneuron axons in motoneuron disease alleviated by CNTF. Nat Neurosci 9:408-419. (Pubitemid 43290971)
54. Ramaswamy S, Nakamura N, Sansal I, Bergeron L, Sellers WR (2002) A novel mechanism of gene regulation and tumor suppression by the transcription factor FKHR. Cancer Cell 2:81-91. (Pubitemid 41043990)
55. Rao SD, Weiss JH (2004) Excitotoxic and oxidative cross-talk between motor neurons and glia in ALS pathogenesis. Trends Neurosci 27:17-23. (Pubitemid 38036974)
56. Schroeder FC, Kau TR, Silver PA, Clardy J (2005) The psammaplysenes, specific inhibitors of FOXO1a nuclear export. J Nat Prod 68:574-576. (Pubitemid 40586322)
57. Storkebaum E, Lambrechts D, Dewerchin M, Moreno-Murciano MP, Appelmans S, Oh H, Van Damme P, Rutten B, Man WY, De Mol M, Wyns S, Manka D, Vermeulen K, Van Den Bosch L, Mertens N, Schmitz C, Robberecht W, Conway EM, Collen D, Moons L, Carmeliet P (2005) Treatment of motoneuron degeneration by intracerebroventricular delivery of VEGF in a rat model of ALS. Nat Neurosci 8:85-92. (Pubitemid 41236736)
58. Takeyama K, Ito S, Yamamoto A, Tanimoto H, Furutani T, Kanuka H, Miura M, Tabata T, Kato S (2002) Androgen-dependent neurodegeneration by polyglutamine-expanded human androgen receptor in Drosophila. Neuron 35:855-864.
59. Tatar M, Bartke A, Antebi A (2003) The endocrine regulation of aging by insulin-like signals. Science 299:1346-1351. (Pubitemid 36254639)
60. Thibault ST, Singer MA, Miyazaki WY, Milash B, Dompe NA, Singh CM, Buchholz R, Demsky M, Fawcett R, Francis-Lang HL, Ryner L, Cheung LM, Chong A, Erickson C, Fisher WW, Greer K, Hartouni SR, Howie E, Jakkula L, Joo D, et al. (2004) A complementary transposon tool kit for Drosophila melanogaster using P and piggyBac. Nat Genet 36:283-287.
61. Wagey R, Pelech SL, Duronio V, Krieger C (1998) Phosphatidylinositol 3-kinase: increased activity and protein level in amyotrophic lateral sclerosis. J Neurochem 71:716-722. (Pubitemid 28480419)
62. Watanabe M, Dykes-Hoberg M, Culotta VC, Price DL, Wong PC, Rothstein JD (2001) Histological evidence of protein aggregation in mutant SOD1 transgenic mice and in amyotrophic lateral sclerosis neural tissues. Neurobiol Dis 8:933-941. (Pubitemid 34017087)
63. Willcox BJ, Donlon TA, He Q, Chen R, Grove JS, Yano K, Masaki KH, Willcox DC, Rodriguez B, Curb JD (2008) FOXO3A genotype is strongly associated with human longevity. Proc Natl Acad Sci U S A 105:13987-13992.