Heat shock and caloric restriction have a synergistic effect on the heat shock response in a sir2.1-dependent manner in Caenorhabditis elegans

Journal of Biological Chemistry

Volumn 287, Issue 34, 2012, Pages 29045-29053

  Raynes, Rachel ^a   Leckey, Bruce D ^a   Nguyen, Kevin ^a   Westerheide, Sandy D ^a  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENE EXPRESSION; MAMMALS;

CAENORHABDITIS ELEGANS; CALORIC RESTRICTION; CELLULARS; ELEGANS; GENES EXPRESSION; HEAT SHOCK RESPONSE; HEATSHOCKS; METABOLIC CONTROL; POLYGLUTAMINE; SYNERGISTIC EFFECT;

NEURODEGENERATIVE DISEASES;

HEAT SHOCK PROTEIN 70; MICROORGANISM PROTEIN; SIR2.1 PROTEIN; SIRTUIN 1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CAENORHABDITIS ELEGANS; CALORIC RESTRICTION; CONTROLLED STUDY; GENE ACTIVATION; GENE DELETION; GENE EXPRESSION REGULATION; GENE INDUCTION; HEAT SHOCK PROTEIN 70 GENE; HEAT SHOCK RESPONSE; HEAT TOLERANCE; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FUNCTION; REPORTER GENE; STRAIN DIFFERENCE; UPREGULATION;

EID: 84865246956     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.353714     Document Type: Article

References (54)

1. Akerfelt, M., Morimoto, R. I., and Sistonen, L. (2010) Heat shock factors: integrators of cell stress, development, and lifespan. Nat. Rev. Mol. Cell Biol. 11, 545-555
2. Anckar, J., and Sistonen, L. (2011) Regulation of HSF-1 function in the heat stress response: implications in aging and disease. Annu. Rev. Biochem. 80, 1089-1115
3. Chiang, W. C., Ching, T. T., Lee, H. C., Mousigian, C., and Hsu, A. L. (2012) HSF-1 regulators DDL-1/2 link insulin-like signaling to heat shock responses and modulation of longevity. Cell 148, 322-334
4. Sarge, K. D., Murphy, S. P., and Morimoto, R. I. (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 (Pubitemid 23068075)
5. von Koskull-Döring, P., Scharf, K. D., and Nover, L. (2007) The diversity of plant heat stress transcription factors. Trends Plant Sci. 12, 452-457
6. Yao, J., Munson, K. M., Webb, W. W., and Lis, J. T. (2006) Dynamics of heat shock factor association with native gene loci in living cells. Nature 442, 1050-1053 (Pubitemid 44330263)
7. Westerheide, S. D., and Morimoto, R. I. (2005) Heat shock response modulators as therapeutic tools for diseases of protein conformation. J. Biol. Chem. 280, 33097-33100 (Pubitemid 41397104)
8. Cypser, J. R., and Johnson, T. E. (2002) Multiple stressors in Caenorhabditis elegans induce stress hormesis and extended longevity. J. Gerontol. A Biol. Sci. Med. Sci. 57, B109-V114
9. Lithgow, G. J., White, T. M., Melov, S., and Johnson, T. E. (1995) Thermotolerance and extended lifespan conferred by single-gene mutations and induced by thermal stress. Proc. Natl. Acad. Sci. U.S.A. 92, 7540-7544
10. Bishop, N. A., and Guarente, L. (2007) Genetic links between diet and lifespan: shared mechanisms from yeast to humans. Nat. Rev. Genet. 8, 835-844 (Pubitemid 47609089)
11. McCay, C. M., Crowell, M. F., and Maynard, L. A. (1989) The effect of retarded growth upon the length of lifespan and upon the ultimate body size. Nutrition 5, 155-171; discussion 172
12. Kaeberlein, M., Powers, R. W., 3rd, Steffen, K. K., Westman, E. A., Hu, D., Dang, N., Kerr, E. O., Kirkland, K. T., Fields, S., and Kennedy, B. K. (2005) Regulation of yeast replicative lifespan by TOR and Sch9 in response to nutrients. Science 310, 1193-1196 (Pubitemid 41681747)
13. Fabrizio, P., Pozza, F., Pletcher, S. D., Gendron, C. M., and Longo, V. D. (2001) Regulation of longevity and stress resistance by Sch9 in yeast. Science 292, 288-290 (Pubitemid 32295387)
14. Johnson, T. E. (2008) Caenorhabditis elegans 2007: the premier model for the study of aging. Exp. Gerontol. 43, 1-4
15. Greer, E. L., and Brunet, A. (2009) Different dietary restriction regimens extend lifespan by both independent and overlapping genetic pathways in C. elegans. Aging Cell 8, 113-127
16. Giannakou, M. E., Goss, M., and Partridge, L. (2008) Role of dFOXO in lifespan extension by dietary restriction in Drosophila melanogaster: not required, but its activity modulates the response. Aging Cell 7, 187-198 (Pubitemid 351359652)
17. Min, K. J., Yamamoto, R., Buch, S., Pankratz, M., and Tatar, M. (2008) Drosophila lifespan control by dietary restriction independent of insulin-like signaling. Aging Cell 7, 199-206 (Pubitemid 351359653)
18. Anderson, R. M., Shanmuganayagam, D., and Weindruch, R. (2009) Caloric restriction and aging: studies in mice and monkeys. Toxicol. Pathol. 37, 47-51
19. Steinkraus, K. A., Smith, E. D., Davis, C., Carr, D., Pendergrass, W. R., Sutphin, G. L., Kennedy, B. K., and Kaeberlein, M. (2008) Dietary restriction suppresses proteotoxicity and enhances longevity by an hsf-1-dependent mechanism in Caenorhabditis elegans. Aging Cell 7, 394-404 (Pubitemid 351663908)
20. Donmez, G., and Guarente, L. (2010) Aging and disease: connections to sirtuins. Aging Cell 9, 285-290
21. Laurenson, P., and Rine, J. (1992) Silencers, silencing, and heritable transcriptional states. Microbiol. Rev. 56, 543-560
22. Brunet, A., Sweeney, L. B., Sturgill, J. F., Chua, K. F., Greer, P. L., Lin, Y., Tran, H., Ross, S. E., Mostoslavsky, R., Cohen, H. Y., Hu, L. S., Cheng, H. L., Jedrychowski, M. P., Gygi, S. P., Sinclair, D. A., Alt, F. W., and Greenberg, M. E. (2004) Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science 303, 2011-2015 (Pubitemid 38393275)
23. Luo, J., Nikolaev, A. Y., Imai, S., Chen, D., Su, F., Shiloh, A., Guarente, L., and Gu, W. (2001) Negative control of p53 by Sir2α promotes cell survival under stress. Cell 107, 137-148 (Pubitemid 33035941)
24. Yeung, F., Hoberg, J. E., Ramsey, C. S., Keller, M. D., Jones, D. R., Frye, R. A., and Mayo, M. W. (2004) Modulation of NF-κB-dependent transcription and cell survival by the SIRT1 deacetylase. EMBO J. 23, 2369-2380 (Pubitemid 38954844)
25. Westerheide, S. D., Anckar, J., Stevens, S. M., Jr., Sistonen, L., and Morimoto, R. I. (2009) Stress-inducible regulation of heat shock factor 1 by the deacetylase SIRT1. Science 323, 1063-1066
26. Morley, J. F., and Morimoto, R. I. (2004) Regulation of longevity in Caenorhabditis elegans by heat shock factor and molecular chaperones. Mol. Biol. Cell 15, 657-664 (Pubitemid 38146482)
27. Morley, J. F., Brignull, H. R., Weyers, J. J., and Morimoto, R. I. (2002) The threshold for polyglutamine expansion protein aggregation and cellular toxicity is dynamic and influenced by aging in Caenorhabditis elegans. Proc. Natl. Acad. Sci. U.S.A. 99, 10417-10422
28. Brenner, S. (1974) The genetics of Caenorhabditis elegans. Genetics 77, 71-94
29. Wang, Y., and Tissenbaum, H. A. (2006) Overlapping and distinct functions for a Caenorhabditis elegans SIR2 and DAF-16/FOXO. Mech. Ageing Dev. 127, 48-56 (Pubitemid 41713513)
30. Lewis, J. A., and Fleming, J. T. (1995) Basic culture methods. Methods Cell Biol. 48, 3-29
31. Hansen, M., Chandra, A., Mitic, L. L., Onken, B., Driscoll, M., and Kenyon, C. (2008) A role for autophagy in the extension of lifespan by dietary restriction in C. elegans. PLoS Genet. 4, e24
32. Bookout, A. L., and Mangelsdorf, D. J. (2003) Quantitative real-time PCR protocol for analysis of nuclear receptor signaling pathways. Nucl. Recept. Signal. 1, e012
33. Ehrenfried, J. A., Evers, B. M., Chu, K. U., Townsend, C. M., Jr., and Thompson, J. C. (1996) Caloric restriction increases the expression of heat shock protein in the gut. Ann. Surg. 223, 592-597; discussion 597-599
34. Heydari, A. R., Wu, B., Takahashi, R., Strong, R., and Richardson, A. (1993) Expression of heat shock protein 70 is altered by age and diet at the level of transcription. Mol. Cell. Biol. 13, 2909-2918 (Pubitemid 23133962)
35. Westerheide, S. D., Bosman, J. D., Mbadugha, B. N., Kawahara, T. L., Matsumoto, G., Kim, S., Gu, W., Devlin, J. P., Silverman, R. B., and Morimoto, R. I. (2004) Celastrols as inducers of the heat shock response and cytoprotection. J. Biol. Chem. 279, 56053-56060 (Pubitemid 40066613)
36. Calamini, B., Silva, M. C., Madoux, F., Hutt, D. M., Khanna, S., Chalfant, M. A., Saldanha, S. A., Hodder, P., Tait, B. D., Garza, D., Balch, W. E., and Morimoto, R. I. (2012) Small-molecule proteostasis regulators for protein conformational diseases. Nat. Chem. Biol. 8, 185-196
37. Fujikake, N., Nagai, Y., Popiel, H. A., Okamoto, Y., Yamaguchi, M., and Toda, T. (2008) Heat shock transcription factor 1-activating compounds suppress polyglutamine-induced neurodegeneration through induction of multiple molecular chaperones. J. Biol. Chem. 283, 26188-26197
38. Waza, M., Adachi, H., Katsuno, M., Minamiyama, M., Sang, C., Tanaka, F., Inukai, A., Doyu, M., and Sobue, G. (2005) 17-AAG, an Hsp90 inhibitor, ameliorates polyglutamine-mediated motor neuron degeneration. Nat. Med. 11, 1088-1095 (Pubitemid 41486831)
39. Morimoto, R. I. (2008) Proteotoxic stress and inducible chaperone networks in neurodegenerative disease and aging. Genes Dev. 22, 1427-1438
40. Donmez, G., Arun, A., Chung, C. Y., McLean, P. J., Lindquist, S., and Guarente, L. (2012) SIRT1 protects against α-synuclein aggregation by activating molecular chaperones. J. Neurosci. 32, 124-132
41. Angelidis, C. E., Lazaridis, I., and Pagoulatos, G. N. (1991) Constitutive expression of heat shock protein 70 in mammalian cells confers thermoresistance. Eur. J. Biochem. 199, 35-39
42. Li, G. C., Li, L. G., Liu, Y. K., Mak, J. Y., Chen, L. L., and Lee, W. M. (1991) Thermal response of rat fibroblasts stably transfected with the human 70-kDa heat shock protein-encoding gene. Proc. Natl. Acad. Sci. U.S.A. 88, 1681-1685 (Pubitemid 21916289)
43. Riabowol, K. T., Mizzen, L. A., and Welch, W. J. (1988) Heat shock is lethal to fibroblasts microinjected with antibodies against Hsp70. Science 242, 433-436
44. Blake, M. J., Fargnoli, J., Gershon, D., and Holbrook, N. J. (1991) Concomitant decline in heat-induced hyperthermia and HSP70 mRNA expression in aged rats. Am. J. Physiol. 260, R663-R667
45. Campanini, C., Petronini, P. G., Alfieri, R., and Borghetti, A. F. (1992) Decreased expression of heat shock protein 70 mRNA and protein in WI-38 human fibroblasts aging in vitro. Ann. N.Y. Acad. Sci. 663, 442-443 (Pubitemid 23090570)
46. Deguchi, Y., Negoro, S., and Kishimoto, S. (1988) Age-related changes of heat shock protein gene transcription in human peripheral blood mononuclear cells. Biochem. Biophys. Res. Commun. 157, 580-584 (Pubitemid 19021219)
47. Faassen, A. E., O'Leary, J. J., Rodysill, K. J., Bergh, N., and Hallgren, H. M. (1989) Diminished heat shock protein synthesis following mitogen stimulation of lymphocytes from aged donors. Exp. Cell Res. 183, 326-334 (Pubitemid 19218491)
48. Fargnoli, J., Kunisada, T., Fornace, A. J., Jr., Schneider, E. L., and Holbrook, N. J. (1990) Decreased expression of heat shock protein 70 mRNA and protein after heat treatment in cells of aged rats. Proc. Natl. Acad. Sci. U.S.A. 87, 846-850 (Pubitemid 20051468)
49. Liu, A. Y., Lin, Z., Choi, H. S., Sorhage, F., and Li, B. (1989) Attenuated induction of heat shock gene expression in aging diploid fibroblasts. J. Biol. Chem. 264, 12037-12045 (Pubitemid 19185380)
50. Pahlavani, M. A., Harris, M. D., Moore, S. A., Weindruch, R., and Richardson, A. (1995) The expression of heat shock protein 70 decreases with age in lymphocytes from rats and rhesus monkeys. Exp. Cell Res. 218, 310-318
51. Heydari, A. R., You, S., Takahashi, R., Gutsmann, A., Sarge, K. D., and Richardson, A. (1996) Effect of caloric restriction on the expression of heat shock protein 70 and the activation of heat shock transcription factor 1. Dev. Genet. 18, 114-124
52. Lee, B. S., Chen, J., Angelidis, C., Jurivich, D. A., and Morimoto, R. I. (1995) Pharmacological modulation of heat shock factor 1 by anti-inflammatory drugs results in protection against stress-induced cellular damage. Proc. Natl. Acad. Sci. U.S.A. 92, 7207-7211
53. Jurivich, D. A., Sistonen, L., Sarge, K. D., and Morimoto, R. I. (1994) Arachidonate is a potent modulator of human heat shock gene transcription. Proc. Natl. Acad. Sci. U.S.A. 91, 2280-2284 (Pubitemid 24092087)
54. Török, Z., Tsvetkova, N. M., Balogh, G., Horváth, I., Nagy, E., Pénzes, Z., Hargitai, J., Bensaude, O., Csermely, P., Crowe, J. H., Maresca, B., and Vigh, L. (2003) Heat shock protein co-inducers with no effect on protein denaturation specifically modulate the membrane lipid phase. Proc. Natl. Acad. Sci. U.S.A. 100, 3131-3136