SIRT1 knockdown promotes neural differentiation and attenuates the heat shock response

Journal of Cellular Physiology

Volumn 229, Issue 9, 2014, Pages 1224-1235

  Liu, Diana J ^a   Hammer, David ^a   Komlos, Daniel ^a   Chen, Kuang Yu ^a   Firestein, Bonnie L ^a   Liu, Alice Y C ^a  

^a RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; HEAT SHOCK COGNATE PROTEIN 70; HEAT SHOCK PROTEIN 70; HEAT SHOCK TRANSCRIPTION FACTOR 1; RETROVIRUS VECTOR; SHORT HAIRPIN RNA; SIRTUIN 1;

ANIMAL CELL; ARTICLE; BRAIN CELL CULTURE; CELL MATURATION; CONTROLLED STUDY; EMBRYO; EMBRYO CULTURE; GENE OVEREXPRESSION; GENE SILENCING; HEAT SHOCK RESPONSE; MOLECULAR WEIGHT; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; NEUROPROGENITOR CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN PROTEIN INTERACTION; RAT; REGULATORY MECHANISM; REPORTER GENE; STEM CELL;

ANIMALS; CELL LINE, TUMOR; CELL PROLIFERATION; CEREBRAL CORTEX; DNA-BINDING PROTEINS; DOWN-REGULATION; GENE KNOCKDOWN TECHNIQUES; GESTATIONAL AGE; HEAT-SHOCK PROTEINS; HEAT-SHOCK RESPONSE; HSP70 HEAT-SHOCK PROTEINS; MICE; NEURAL STEM CELLS; NEUROGENESIS; NEURONS; PROTEIN BINDING; RATS; RATS, SPRAGUE-DAWLEY; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SIRTUIN 1; TIME FACTORS; TRANSCRIPTION FACTORS; TRANSFECTION;

EID: 84901236321     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.24556     Document Type: Article

References (71)

1. Akerfelt M, Morimoto RI, Sistonen L. 2010. Heat shock factors: Integrators of cell stress, development and lifespan. Nat Rev Mol Cell Biol 11:545-555.
2. Anckar J, Sistonen L. 2011. Regulation of HSF1 function in the heat stress response: Implications in aging and disease. Annu Rev Biochem 80:1089-1115.
3. Aranha MM, Santos DM, Sola S, Steer CJ, Rodrigues CM. 2011. MiR-34a regulates mouse neural stem cell differentiation. PLoS ONE 6:e21396.
4. Baler R, Dahl G, Voellmy R. 1993. Activation of human heat shock genes is accompanied by oligomerization, modification, and rapid translocation of heat shock transcription factor HSF1. Mol Cell Biol 13:2486-2496.
5. Batulan Z, Shinder GA, Minotti S, He BP, Doroudchi MM, Nalbantoglu J, Strong MJ, Durham HD. 2003. High threshold for induction of the stress response in motor neurons is associated with failure to activate HSF1. J Neurosci 23:5789-5798.
6. Baur JA, Pearson KJ, Price NL, Jamieson HA, Lerin C, Kalra A, Prabhu VV, Allard JS, Lopez-Lluch G, Lewis K, Pistell PJ, Poosala S, Becker KG, Boss O, Gwinn D, Wang M, Ramaswamy S, Fishbein KW, Spencer RG, Lakatta EG, Le Couteur D, Shaw RJ, Navas P, Puigserver P, Ingram DK, de Cabo R, Sinclair DA, 2006. Resveratrol improves health and survival of mice on a high-calorie diet. Nature 444:337-342.
7. Baur JA, Sinclair DA. 2006. Therapeutic potential of resveratrol: The in vivo evidence. Nat Rev Drug Discov 5:493-506.
8. Blander G, Bhimavarapu A, Mammone T, Maes D, Elliston K, Reich C, Matsui MS, Guarente L, Loureiro JJ. 2009. SIRT1 promotes differentiation of normal human keratinocytes. J Invest Dermatol 129:41-49.
9. Blander G, Guarente L. 2004. The Sir2 family of protein deacetylases. Annu Rev Biochem 73:417-435.
10. Brown IR, Rush SJ. 1999. Cellular localization of the heat shock transcription factors HSF1 and HSF2 in the rat brain during postnatal development and following hyperthermia. Brain Res 821:333-340.
11. Brunet A, Sweeney LB, Sturgill JF, Chua KF, Greer PL, Lin Y, Tran H, Ross SE, Mostoslavsky R, Cohen HY, Hu LS, Cheng H-L, 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.
12. Calvanese V, Lara E, Suárez-Álvarez B, Abu Dawud R, Vázquez-Chantada M, Martínez-Chantar ML, Embade N, López-Nieva P, Horrillo A, Hmadcha A, Soria B, Piazzolla D, Herranz D, Serrano M, Mato JM, Andrews PW, López-Larrea C, Esteller M, Fraga MF. 2010. Sirtuin 1 regulation of developmental genes during differentiation of stem cells. Proc Natl Acad Sci 107:13736-13741.
13. Caviness VS, Takahashi T, Nowakowski RS. 1995. Numbers, time and neocortical neuronogenesis: A general developmental and evolutionary model. Trends Neurosci 18:379-383.
14. Cheng HL, Mostoslavsky R, Saito S, Manis JP, Gu Y, Patel P, Bronson R, Appella E, Alt FW, Chua KF. 2003. Developmental defects and p53 hyperacetylation in Sir2 homolog (SIRT1)-deficient mice. Proc Natl Acad Sci USA 100:10794-10799.
15. Codocedo JF, Allard C, Godoy JA, Varela-Nallar L, Inestrosa NC. 2012. SIRT1 regulates dendritic development in hippocampal neurons. PLoS ONE 7:e47073.
16. Cohen HY, Miller C, Bitterman KJ, Wall NR, Hekking B, Kessler B, Howitz KT, Gorospe M, de Cabo R, Sinclair DA. 2004. Calorie restriction promotes mammalian cell survival by inducing the SIRT1 deacetylase. Science 305:390-392.
17. Di Giovanni S, Knights CD, Rao M, Yakovlev A, Beers J, Catania J, Avantaggiati ML, Faden AI. 2006. The tumor suppressor protein p53 is required for neurite outgrowth and axon regeneration. EMBO J 25:4084-4096.
18. Donmez G, Wang D, Cohen DE, Guarente L. 2010. SIRT1 suppresses [beta]-amyloid production by activating the [alpha]-secretase gene ADAM10. Cell 142:320-332.
19. Du Y, Chen CP, Tseng CY, Eisenberg Y, Firestein BL. 2007. Astroglia-mediated effects of uric acid to protect spinal cord neurons from glutamate toxicity. Glia 55:463-472.
20. Feige JN, Auwerx J. 2008. Transcriptional targets of sirtuins in the coordination of mammalian physiology. Curr Opin Cell Biol 20:303-309.
21. Forman MS, Trojanowski JQ, Lee VM. 2004. Neurodegenerative diseases: A decade of discoveries paves the way for therapeutic breakthroughs. Nat Med 10:1055-1063.
22. Foster JA, Brown IR. 1997. Differential induction of heat shock mRNA in oligodendrocytes, microglia, and astrocytes following hyperthermia. Brain Res Mol Brain Res 45:207-218.
23. Foster JA, Rush SJ, Brown IR. 1995. Localization of constitutive and hyperthermia-inducible heat shock mRNAs (hsc70 and hsp70) in the rabbit cerebellum and brainstem by non-radioactive in situ hybridization. J Neurosci Res 41:603-612.
24. Fulco M, Schiltz RL, Iezzi S, King MT, Zhao P, Kashiwaya Y, Hoffman E, Veech RL, Sartorelli V. 2003. Sir2 regulates skeletal muscle differentiation as a potential sensor of the redox state. Mol Cell 12:51-62.
25. Gohlke JM, Griffith WC, Faustman EM. 2007. Computational models of neocortical neuronogenesis and programmed cell death in the developing mouse, monkey, and human. Cereb Cortex 17:2433-2442.
26. Guarente L. 2005. Calorie restriction and SIR2 genes-Towards a mechanism. Mech Ageing Dev 126:923-928.
27. Guarente L. 2007. Sirtuins in aging and disease. Cold Spring Harb Symp Quant Biol 72:483-488.
28. Guo W, Qian L, Zhang J, Zhang W, Morrison A, Hayes P, Wilson S, Chen T, Zhao J. 2011. Sirt1 overexpression in neurons promotes neurite outgrowth and cell survival through inhibition of the mTOR signaling. J Neurosci Res 89:1723-1736.
29. Guzhova I, Kislyakova K, Moskaliova O, Fridlanskaya I, Tytell M, Cheetham M, Margulis B. 2001. In vitro studies show that Hsp70 can be released by glia and that exogenous Hsp70 can enhance neuronal stress tolerance. Brain Res 914:66-73.
30. Hasegawa K, Yoshikawa K. 2008. Necdin regulates p53 acetylation via sirtuin1 to modulate DNA damage response in cortical neurons. J Neurosci 28:8772-8784.
31. Hisahara S, Chiba S, Matsumoto H, Tanno M, Yagi H, Shimohama S, Sato M, Horio Y. 2008. Histone deacetylase SIRT1 modulates neuronal differentiation by its nuclear translocation. Proc Natl Acad Sci 105:15599-15604.
32. Homma S, Jin X, Wang G, Tu N, Min J, Yanasak N, Mivechi NF. 2007. Demyelination, astrogliosis, and accumulation of ubiquitinated proteins, hallmarks of CNS disease in hsf1-deficient mice. J Neurosci 27:7974-7986.
33. Howitz KT, Bitterman KJ, Cohen HY, Lamming DW, Lavu S, Wood JG, Zipkin RE, Chung P, Kisielewski A, Zhang LL, Scherer B, Sinclair DA. 2003. Small molecule activators of sirtuins extend Saccharomyces cerevisiae lifespan. Nature 425:191-196.
34. Huang LE, Zhang H, Bae SW, Liu AY. 1994. Thiol reducing reagents inhibit the heat shock response. Involvement of a redox mechanism in the heat shock signal transduction pathway. J Biol Chem 269:30718-30725.
35. Imai S. 2007. Is Sirt1 a miracle bullet for longevity? Aging Cell 6:735-737.
36. Johnson MB, Kawasawa YI, Mason CE, Krsnik Z, Coppola G, Bogdanovic D, Geschwind DH, Mane SM, State MW, Sestan N. 2009. Functional and evolutionary insights into human brain development through global transcriptome analysis. Neuron 62:494-509.
37. Kim D, Nguyen MD, Dobbin MM, Fischer A, Sananbenesi F, Rodgers JT, Delalle I, Baur JA, Sui G, Armour SM, Puigserver P, Sinclair DA, Tsai LH. 2007. SIRT1 deacetylase protects against neurodegeneration in models for Alzheimer's disease and amyotrophic lateral sclerosis. EMBO J 26:3169-3179.
38. Kim MJ, Ahn K, Park SH, Kang HJ, Jang BG, Oh SJ, Oh SM, Jeong YJ, Heo JI, Suh JG, Lim SS, Ko YJ, Huh SO, Kim SC, Park JB, Kim J, Kim JI, Jo SA, Lee JY. 2009. SIRT1 regulates tyrosine hydroxylase expression and differentiation of neuroblastoma cells via FOXO3a. FEBS Lett 583:1183-1188.
39. Knights CD, Catania J, Giovanni SD, Muratoglu S, Perez R, Swartzbeck A, Quong AA, Zhang X, Beerman T, Pestell RG, Avantaggiati ML. 2006. Distinct p53 acetylation cassettes differentially influence gene-expression patterns and cell fate. J Cell Biol 173:533-544.
40. Lansbury PT, Lashuel HA. 2006. A century-old debate on protein aggregation and neurodegeneration enters the clinic. Nature 443:774-779.
41. Lavu S, Boss O, Elliott PJ, Lambert PD. 2008. Sirtuins [mdash] novel therapeutic targets to treat age-associated diseases. Nat Rev Drug Discov 7:841-853.
42. Li Y, Yokota T, Gama V, Yoshida T, Gomez JA, Ishikawa K, Sasaguri H, Cohen HY, Sinclair DA, Mizusawa H, Matsuyama S. 2007. Bax-inhibiting peptide protects cells from polyglutamine toxicity caused by Ku70 acetylation. Cell Death Differ 14:2058-2067.
43. Libert S, Cohen D, Guarente L. 2008. Neurogenesis directed by Sirt1. Nat Cell Biol 10:373-374.
44. Liu AYC, Mathur R, Mei N, Langhammer CG, Babiarz B, Firestein BL. 2011. Neuroprotective drug riluzole amplifies the heat shock factor 1 (HSF1)- and glutamate transporter 1 (GLT1)-dependent cytoprotective mechanisms for neuronal survival. J Biol Chem 286:2785-2794.
45. Magby JP, Bi C, Chen ZY, Lee FS, Plummer MR. 2006. Single-cell characterization of retrograde signaling by brain-derived neurotrophic factor. J Neurosci 26:13531-13536.
46. Manzerra P, Rush SJ, Brown IR. 1993. Temporal and spatial distribution of heat shock mRNA and protein (hsp70) in the rabbit cerebellum in response to hyperthermia. J Neurosci Res 36:480-490.
47. Manzerra P, Rush SJ, Brown IR. 1997. Tissue-specific differences in heat shock protein hsc70 and hsp70 in the control and hyperthermic rabbit. J Cell Physiol 170:130-137.
48. Marcuccilli CJ, Mathur SK, Morimoto RI, Miller RJ. 1996. Regulatory differences in the stress response of hippocampal neurons and glial cells after heat shock. J Neurosci 16:478-485.
49. McBurney MW, Yang X, Jardine K, Hixon M, Boekelheide K, Webb JR, Lansdorp PM, Lemieux M. 2003. The mammalian SIR2alpha protein has a role in embryogenesis and gametogenesis. Mol Cell Biol 23:38-54.
50. Morimoto RI. 2008. Proteotoxic stress and inducible chaperone networks in neurodegenerative disease and aging. Genes Dev 22:1427-1438.
51. Muchowski PJ, Wacker JL. 2005. Modulation of neurodegeneration by molecular chaperones. Nat Rev Neurosci 6:11-22.
52. Nelson P, Christian C, Nirenberg M. 1976. Synapse formation between clonal neuroblastoma X glioma hybrid cells and striated muscle cells. Proc Natl Acad Sci USA 73:123-127.
53. Ng F, Tang BL. 2013. Sirtuins' modulation of autophagy. J Cell Physiol 228:2262-2270.
54. Nicot A, DiCicco-Bloom E. 2001. Regulation of neuroblast mitosis is determined by PACAP receptor isoform expression. Proc Natl Acad Sci USA 98:4758-4763.
55. Nirenberg M, Wilson S, Higashida H, Rotter A, Krueger K, Busis N, Ray R, Kenimer JG, Adler M. 1983. Modulation of synapse formation by cyclic adenosine monophosphate. Science 222:794-799.
56. Nishimura RN, Dwyer BE. 1996. Evidence for different mechanisms of induction of HSP70i: A comparison of cultured rat cortical neurons with astrocytes. Brain Res Mol Brain Res 36:227-239.
57. Oza J, Yang J, Chen KY, Liu AY. 2008. Changes in the regulation of heat shock gene expression in neuronal cell differentiation. Cell Stress Chaperones 13:73-84.
58. Picard F, Kurtev M, Chung N, Topark-Ngarm A, Senawong T, Machado De Oliveira R, Leid M, McBurney MW, Guarente L. 2004. Sirt1 promotes fat mobilization in white adipocytes by repressing PPAR-gamma. Nature 429:771-776.
59. Prozorovski T, Schulze-Topphoff U, Glumm R, Baumgart J, Schroter F, Ninnemann O, Siegert E, Bendix I, Brustle O, Nitsch R, Zipp F, Aktas O. 2008. Sirt1 contributes critically to the redox-dependent fate of neural progenitors. Nat Cell Biol 10:385-394.
60. Sakamoto J, Miura T, Shimamoto K, Horio Y. 2003. Predominant expression of Sir2a, an NAD-dependent histone deacetylase, in the embryonic mouse heart and brain. FEBS Lett 556:281-286.
61. Sansone L, Reali V, Pellegrini L, Villanova L, Aventaggiato M, Marfe G, Rosa R, Nebbioso M, Tafani M, Fini M, Russo MA, Pucci B. 2013. SIRT1 silencing confers neuroprotection through IGF-1 pathway activation. J Cell Physiol 228:1754-1761.
62. Santos SD, Saraiva MJ. 2004. Enlarged ventricles, astrogliosis and neurodegeneration in heat shock factor 1 null mouse brain. Neuroscience 126:657-663.
63. Sarge KD, Murphy SP, Morimoto RI. 1993. Activation of heat shock gene transcription by heat shock factor 1 involves oligomerization, acquisition of DNA-binding activity, and nuclear localization and can occur in the absence of stress. Mol Cell Biol 13:1392-1407.
64. Soto C. 2003. Unfolding the role of protein misfolding in neurodegenerative diseases. Nat Rev Neurosci 4:49-60.
65. Teng FYH, Hor CHH, Tang BL. 2009. Emerging cues mediating astroglia lineage restriction of progenitor cells in the injured/diseased adult CNS. Differentiation 77:121-127.
66. Vaccarino FM, Schwartz ML, Raballo R, Nilsen J, Rhee J, Zhou M, Doetschman T, Coffin JD, Wyland JJ, Hung YT. 1999. Changes in cerebral cortex size are governed by fibroblast growth factor during embryogenesis. Nat Neurosci 2:848.
67. Westerheide SD, Anckar J, Stevens SM, Sistonen L, Morimoto RI. 2009. Stress-inducible regulation of heat shock factor 1 by the deacetylase SIRT1. Science 323:1063-1066.
68. Yamamoto H, Schoonjans K, Auwerx J. 2007. Sirtuin functions in health and disease. Mol Endocrinol 21:1745-1755.
69. Yang J, Bridges K, Chen KY, Liu AY. 2008. Riluzole increases the amount of latent HSF1 for an amplified heat shock response and cytoprotection. PLoS ONE 3:e2864.
70. Yang J, Oza J, Bridges K, Chen KY, Liu AY. 2008. Neural differentiation and the attenuated heat shock response. Brain Res 1203:39-50.
71. Zhang Y, Wang J, Chen G, Fan D, Deng M. 2011. Inhibition of Sirt1 promotes neural progenitors toward motoneuron differentiation from human embryonic stem cells. Biochem Biophys Res Commun 404:610-614.