Identification of a Tissue-Selective Heat Shock Response Regulatory Network

PLoS Genetics

Volumn 9, Issue 4, 2013, Pages

  Guisbert, Eric ^a   Czyz, Daniel M ^a   Richter, Klaus ^a,c   McMullen, Patrick D ^b   Morimoto, Richard I ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b Northwestern University   (United States)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEASOME; HEAT SHOCK PROTEIN; PROTEIN;

ANIMAL TISSUE; ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; GENE EXPRESSION; GENE IDENTIFICATION; GENE REGULATORY NETWORK; GENOME ANALYSIS; HEAT SHOCK RESPONSE; INTESTINE; MUSCLE CELL; NONHUMAN; PROTEIN FOLDING; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; REGULATORY MECHANISM; RNA INTERFERENCE; SPERMATHECA; ANIMAL; GENETICS; METABOLISM;

ANIMALIA; CAENORHABDITIS ELEGANS; METAZOA;

ANIMALS; CAENORHABDITIS ELEGANS; HEAT-SHOCK PROTEINS; HEAT-SHOCK RESPONSE; PROTEIN FOLDING; PROTEINS; RNA INTERFERENCE;

EID: 84876869300     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003466     Document Type: Article

References (65)

1. Akerfelt M, Morimoto RI, Sistonen L, (2010) Heat shock factors: integrators of cell stress, development and lifespan. Nat Rev Mol Cell Biol 8: 545-555.
2. Craig EA, Gross CA, (1991) Is hsp70 the cellular thermometer? Trends Biochem Sci 16: 135-140.
3. Abravaya K, Myers MP, Murphy SP, Morimoto RI, (1992) The human heat shock protein hsp70 interacts with HSF, the transcription factor that regulates heat shock gene expression. Genes Dev 6: 1153-1164.
4. Baler R, Welch WJ, Voellmy R, (1992) Heat shock gene regulation by nascent polypeptides and denatured proteins: hsp70 as a potential autoregulatory factor. J Cell Biol 117: 1151-1159.
5. Mosser DD, Duchaine J, Massie B, (1993) The DNA-binding activity of the human heat shock transcription factor is regulated in vivo by hsp70. Mol Cell Biol 13: 5427-5438.
6. Shi Y, Mosser DD, Morimoto RI, (1998) Molecular chaperones as HSF1-specific transcriptional repressors. Genes Dev 12: 654-666.
7. Zou J, Guo Y, Guettouche T, Smith DF, Voellmy R, (1998) Repression of heat shock transcription factor HSF1 activation by HSP90 (HSP90 complex) that forms a stress-sensitive complex with HSF1. Cell 94: 471-480.
8. Elefant F, Palter KB, (1999) Tissue-specific expression of dominant negative mutant Drosophila HSC70 causes developmental defects and lethality. Mol Biol Cell 10: 2101-2117.
9. Mathur SK, Sistonen L, Brown IR, Murphy SP, Sarge KD, et al. (1994) Deficient induction of human hsp70 heat shock gene transcription in Y79 retinoblastoma cells despite activation of heat shock factor 1. Proc Natl Acad Sci U S A 91: 8695-8699.
10. 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.
11. Batulan Z, Shinder GA, Minotti S, He BP, Doroudchi MM, et al. (2003) High threshold for induction of the stress response in motor neurons is associated with failure to activate HSF1. J Neurosci 23: 5789-5798.
12. Blake MJ, Gershon D, Fargnoli J, Holbrook NJ, (1990) Discordant expression of heat shock protein mRNAs in tissues of heat-stressed rats. J Biol Chem 265: 15275-15279.
13. Morley JF, Morimoto RI, (2004) Regulation of longevity in Caenorhabditis elegans by heat shock factor and molecular chaperones. Mol Biol Cell 15: 657-664.
14. Wu BJ, Williams GT, Morimoto RI, (1987) Detection of three protein binding sites in the serum-regulated promoter of the human gene encoding the 70-kDa heat shock protein. Proc Natl Acad Sci U S A 84: 2203-2207.
15. Williams GT, McClanahan TK, Morimoto RI, (1989) E1a transactivation of the human HSP70 promoter is mediated through the basal transcriptional complex. Mol Cell Biol 9: 2574-2587.
16. Morgan WD, Williams GT, Morimoto RI, Greene J, Kingston RE, et al. (1987) Two transcriptional activators, CCAAT-box-binding transcription factor and heat shock transcription factor, interact with a human hsp70 gene promoter. Mol Cell Biol 7: 1129-1138.
17. Greene JM, Larin Z, Taylor IC, Prentice H, Gwinn KA, et al. (1987) Multiple basal elements of a human hsp70 promoter function differently in human and rodent cell lines. Mol Cell Biol 7: 3646-3655.
18. Abravaya K, Phillips B, Morimoto RI, (1991) Heat shock-induced interactions of heat shock transcription factor and the human hsp70 promoter examined by in vivo footprinting. Mol Cell Biol 11: 586-592.
19. Morimoto RI, (2008) Proteotoxic stress and inducible chaperone networks in neurodegenerative disease and aging. Genes Dev 22: 1427-1438.
20. Prahlad V, Cornelius T, Morimoto RI, (2008) Regulation of the cellular heat shock response in Caenorhabditis elegans by thermosensory neurons. Science 320: 811-814.
21. Ben-Zvi A, Miller EA, Morimoto RI, (2009) Collapse of proteostasis represents an early molecular event in Caenorhabditis elegans aging. Proc Natl Acad Sci U S A 106: 14914-14919.
22. 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.
23. Xiao X, Zuo X, Davis AA, McMillan DR, Curry BB, et al. (1999) HSF1 is required for extra-embryonic development, postnatal growth and protection during inflammatory responses in mice. EMBO J 18: 5943-5952.
24. Jedlicka P, Mortin MA, Wu C, (1997) Multiple functions of Drosophila heat shock transcription factor in vivo. EMBO J 16: 2452-2462.
25. Parker-Thornburg J, Bonner JJ, (1987) Mutations that induce the heat shock response of Drosophila. Cell 51: 763-772.
26. Bonner JJ, Parks C, Parker-Thornburg J, Mortin MA, Pelham HR, (1984) The use of promoter fusions in Drosophila genetics: isolation of mutations affecting the heat shock response. Cell 37: 979-991.
27. Silva MC, Fox S, Beam M, Thakkar H, Amaral MD, et al. (2011) A genetic screening strategy identifies novel regulators of the proteostasis network. PLoS Genet 7: e1002438 doi:10.1371/journal.pgen.1002438.
28. Nollen EA, Garcia SM, van Haaften G, Kim S, Chavez A, et al. (2004) Genome-wide RNA interference screen identifies previously undescribed regulators of polyglutamine aggregation. Proc Natl Acad Sci U S A 101: 6403-6408.
29. Shore DE, Carr CE, Ruvkun G, (2012) Induction of cytoprotective pathways is central to the extension of lifespan conferred by multiple longevity pathways. PLoS Genet 8: e1002792 doi:10.1371/journal.pgen.1002792.
30. Melo JA, Ruvkun G, (2012) Inactivation of conserved C. elegans genes engages pathogen- and xenobiotic-associated defenses. Cell 149: 452-466.
31. Wang MC, Min W, Freudiger CW, Ruvkun G, Xie XS, (2011) RNAi screening for fat regulatory genes with SRS microscopy. Nat Methods 8: 135-138.
32. Curran SP, Ruvkun G, (2007) Lifespan regulation by evolutionarily conserved genes essential for viability. PLoS Genet 3: e56 doi:10.1371/journal.pgen.0030056.
33. Hansen M, Hsu AL, Dillin A, Kenyon C, (2005) New genes tied to endocrine, metabolic, and dietary regulation of lifespan from a Caenorhabditis elegans genomic RNAi screen. PLoS Genet 1: e17 doi:10.1371/journal.pgen.0010017.
34. Wang J, Robida-Stubbs S, Tullet JM, Rual JF, Vidal M, et al. (2010) RNAi screening implicates a SKN-1-dependent transcriptional response in stress resistance and longevity deriving from translation inhibition. PLoS Genet 6: e1001048 doi:10.1371/journal.pgen.1001048.
35. Kamath RS, Fraser AG, Dong Y, Poulin G, Durbin R, et al. (2003) Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421: 231-237.
36. Kapulkin WJ, Hiester BG, Link CD, (2005) Compensatory regulation among ER chaperones in C. elegans. FEBS Lett 579: 3063-3068.
37. Calfon M, Zeng H, Urano F, Till JH, Hubbard SR, et al. (2002) IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 415: 92-96.
38. Khaleque MA, Bharti A, Gong J, Gray PJ, Sachdev V, et al. (2008) Heat shock factor 1 represses estrogen-dependent transcription through association with MTA1. Oncogene 27: 1886-1893.
39. Murawska M, Hassler M, Renkawitz-Pohl R, Ladurner A, Brehm A, (2011) Stress-induced PARP activation mediates recruitment of Drosophila Mi-2 to promote heat shock gene expression. PLoS Genet 7: e1002206 doi:10.1371/journal.pgen.1002206.
40. Hajdu-Cronin YM, Chen WJ, Sternberg PW, (2004) The L-type cyclin CYL-1 and the heat-shock-factor HSF-1 are required for heat-shock-induced protein expression in Caenorhabditis elegans. Genetics 168: 1937-1949.
41. Neef DW, Turski ML, Thiele DJ, Modulation of heat shock transcription factor 1 as a therapeutic target for small molecule intervention in neurodegenerative disease. PLoS Biol 8: e1000291 doi:10.1371/journal.pbio.1000291.
42. Guisbert E, Herman C, Lu CZ, Gross CA, (2004) A chaperone network controls the heat shock response in E. coli. Genes Dev 18: 2812-2821.
43. Poritz MA, Bernstein HD, Strub K, Zopf D, Wilhelm H, et al. (1990) An E. coli ribonucleoprotein containing 4.5S RNA resembles mammalian signal recognition particle. Science 250: 1111-1117.
44. Arnold CE, Wittrup KD, (1994) The stress response to loss of signal recognition particle function in Saccharomyces cerevisiae. J Biol Chem 269: 30412-30418.
45. Zhou M, Wu X, Ginsberg HN, (1996) Evidence that a rapidly turning over protein, normally degraded by proteasomes, regulates hsp72 gene transcription in HepG2 cells. J Biol Chem 271: 24769-24775.
46. Mathew A, Mathur SK, Morimoto RI, (1998) Heat shock response and protein degradation: regulation of HSF2 by the ubiquitin-proteasome pathway. Mol Cell Biol 18: 5091-5098.
47. Taubert S, Hansen M, Van Gilst MR, Cooper SB, Yamamoto KR, (2008) The Mediator subunit MDT-15 confers metabolic adaptation to ingested material. PLoS Genet 4: e1000021 doi:10.1371/journal.pgen.1000021.
48. Badenhorst P, Voas M, Rebay I, Wu C, (2002) Biological functions of the ISWI chromatin remodeling complex NURF. Genes Dev 16: 3186-3198.
49. Kipreos ET, (2005) Ubiquitin-mediated pathways in C. elegans. WormBook pp. 1-24.
50. Anderson LL, Mao X, Scott BA, Crowder CM, (2009) Survival from hypoxia in C. elegans by inactivation of aminoacyl-tRNA synthetases. Science 323: 630-633.
51. Segref A, Torres S, Hoppe T, (2011) A screenable in vivo assay to study proteostasis networks in Caenorhabditis elegans. Genetics 187: 1235-1240.
52. Link CD, Cypser JR, Johnson CJ, Johnson TE, (1999) Direct observation of stress response in Caenorhabditis elegans using a reporter transgene. Cell Stress Chaperones 4: 235-242.
53. Murphy CT, McCarroll SA, Bargmann CI, Fraser A, Kamath RS, et al. (2003) Genes that act downstream of DAF-16 to influence the lifespan of Caenorhabditis elegans. Nature 424: 277-283.
54. Caruso ME, Jenna S, Bouchecareilh M, Baillie DL, Boismenu D, et al. (2008) GTPase-mediated regulation of the unfolded protein response in Caenorhabditis elegans is dependent on the AAA+ ATPase CDC-48. Mol Cell Biol 28: 4261-4274.
55. Zhong W, Sternberg PW, (2006) Genome-wide prediction of C. elegans genetic interactions. Science 311: 1481-1484.
56. Newman ME, Girvan M, (2004) Finding and evaluating community structure in networks. Phys Rev E Stat Nonlin Soft Matter Phys 69: 026113.
57. Guimera R, Amaral LA, (2005) Cartography of complex networks: modules and universal roles. J Stat Mech 2005: nihpa35573.
58. Yoneda T, Benedetti C, Urano F, Clark SG, Harding HP, et al. (2004) Compartment-specific perturbation of protein handling activates genes encoding mitochondrial chaperones. J Cell Sci 117: 4055-4066.
59. Ron D, Walter P, (2007) Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 8: 519-529.
60. Reddy PS, Corley RB, (1999) The contribution of ER quality control to the biologic functions of secretory IgM. Immunol Today 20: 582-588.
61. Dunn AY, Melville MW, Frydman J, (2001) Review: cellular substrates of the eukaryotic chaperonin TRiC/CCT. J Struct Biol 135: 176-184.
62. Brenner S, (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71-94.
63. McKay SJ, Johnsen R, Khattra J, Asano J, Baillie DL, et al. (2003) Gene expression profiling of cells, tissues, and developmental stages of the nematode C. elegans. Cold Spring Harb Symp Quant Biol 68: 159-169.
64. Harris TW, Antoshechkin I, Bieri T, Blasiar D, Chan J, et al. WormBase: a comprehensive resource for nematode research. Nucleic Acids Res 38: D463-467.
65. Hall DH, Altun ZF (2008) C. elegans atlas. Cold Spring Harbor, N.Y.: Cold Spring Harbor Laboratory Press. x, 348 p. p.