Neuronal circuitry regulates the response of Caenorhabditis elegans to misfolded proteins

Proceedings of the National Academy of Sciences of the United States of America

Volumn 108, Issue 34, 2011, Pages 14204-14209

  Prahlad, Veena ^a   Morimoto, Richard I ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Hsp70; Neuronal control; Proteostasis; Small heat shock proteins; Stress response

Indexed keywords

CALPAIN; CHAPERONE; HEAT SHOCK PROTEIN 70; MUTANT PROTEIN; POLYGLUTAMINE; SUPEROXIDE DISMUTASE;

ACUTE STRESS; ANIMAL CELL; ARTICLE; CAENORHABDITIS ELEGANS; CELL FUNCTION; CELLULAR STRESS RESPONSE; CHRONIC STRESS; CONTROLLED STUDY; CYTOTOXICITY; HEAT SHOCK; INTESTINE CELL; MOUSE; MUSCLE CELL; NERVE CELL; NERVE CELL MEMBRANE POTENTIAL; NEUROSECRETION; NEUROTOXICITY; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN HOMEOSTASIS; PROTEIN SECRETION; SIGNAL TRANSDUCTION; SYNAPSE VESICLE; TEMPERATURE SENSE; TEMPERATURE STRESS; UPREGULATION;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; DNA-BINDING PROTEINS; GENES, REPORTER; HEAT-SHOCK RESPONSE; INTESTINES; MUTATION; NERVE NET; NEURONS; NEUROSECRETION; PEPTIDES; PROTEIN FOLDING; PROTEIN STRUCTURE, QUATERNARY; SECRETORY VESICLES; TEMPERATURE; TRANSCRIPTION FACTORS; TRINUCLEOTIDE REPEAT EXPANSION; TROPOMYOSIN; UP-REGULATION;

ANIMALIA; CAENORHABDITIS ELEGANS;

EID: 80052137410     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1106557108     Document Type: Article

References (49)

1. Soto C, Estrada LD (2008) Protein misfolding and neurodegeneration. Arch Neurol 65:184-189. (Pubitemid 351240778)
2. Carrell RW (2005) Cell toxicity and conformational disease. Trends Cell Biol 15:574-580.
3. Balch WE, Morimoto RI, Dillin A, Kelly JW (2008) Adapting proteostasis for disease intervention. Science 319:916-919. (Pubitemid 351263754)
4. Sherman MY, Goldberg AL (2001) Cellular defenses against unfolded proteins: A cell biologist thinks about neurodegenerative diseases. Neuron 29:15-32. (Pubitemid 32108719)
5. Hartl FU, Hayer-Hartl M (2009) Converging concepts of protein folding in vitro and in vivo. Nat Struct Mol Biol 16:574-581.
6. Jonikas MC, et al. (2009) Comprehensive characterization of genes required for protein folding in the endoplasmic reticulum. Science 323:1693-1697.
7. Lindquist S, Craig EA (1988) The heat-shock proteins. Annu Rev Genet 22:631-677. (Pubitemid 19156675)
8. 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.
9. Voellmy R, Boellmann F (2007) Chaperone regulation of the heat shock protein response. Adv Exp Med Biol 594:89-99.
10. Morimoto RI (1998) Regulation of the heat shock transcriptional response: Cross talk between a family of heat shock factors, molecular chaperones, and negative regulators. Genes Dev 12:3788-3796.
11. Zourlidou A, et al. (2007) Hsp27 overexpression in the R6/2 mouse model of Huntington's disease: Chronic neurodegeneration does not induce Hsp27 activation. Hum Mol Genet 16:1078-1090. (Pubitemid 47062728)
12. Hay DG, et al. (2004) Progressive decrease in chaperone protein levels in a mouse model of Huntington's disease and induction of stress proteins as a therapeutic approach. Hum Mol Genet 13:1389-1405. (Pubitemid 38961645)
13. Muchowski PJ (2002) Protein misfolding, amyloid formation, and neurodegeneration: A critical role for molecular chaperones? Neuron 35:9-12.
14. Satyal SH, et al. (2000) Polyglutamine aggregates alter protein folding homeostasis in Caenorhabditis elegans. Proc Natl Acad Sci USA 97:5750-5755. (Pubitemid 30367470)
15. Vleminckx V, et al. (2002) Upregulation of HSP27 in a transgenic model of ALS. J Neuropathol Exp Neurol 61:968-974. (Pubitemid 35278718)
16. Ferraiuolo L, et al. (2007) Microarray analysis of the cellular pathways involved in the adaptation to and progression of motor neuron injury in the SOD1 G93A mouse model of familial ALS. J Neurosci 27:9201-9219. (Pubitemid 47312070)
17. Bence NF, Sampat RM, Kopito RR (2001) Impairment of the ubiquitin-proteasome system by protein aggregation. Science 292:1552-1555. (Pubitemid 32493425)
18. Stenoien DL, et al. (1999) Polyglutamine-expanded androgen receptors form aggregates that sequester heat shock proteins, proteasome components and SRC-1, and are suppressed by the HDJ-2 chaperone. Hum Mol Genet 8:731-741. (Pubitemid 29189040)
19. Kim S, Nollen EA, Kitagawa K, Bindokas VP, Morimoto RI (2002) Polyglutamine protein aggregates are dynamic. Nat Cell Biol 4:826-831.
20. Olzscha H, et al. (2011) Amyloid-like aggregates sequester numerous metastable proteins with essential cellular functions. Cell 144:67-78.
21. Tatzelt J, Voellmy R, Welch WJ (1998) Abnormalities in stress proteins in prion diseases. Cell Mol Neurobiol 18:721-729. (Pubitemid 29012949)
22. Bush KT, Goldberg AL, Nigam SK (1997) Proteasome inhibition leads to a heat-shock response, induction of endoplasmic reticulum chaperones, and thermotolerance. J Biol Chem 272:9086-9092. (Pubitemid 27154911)
23. Fujimoto M, et al. (2005) Active HSF1 significantly suppresses polyglutamine aggregate formation in cellular and mouse models. J Biol Chem 280:34908-34916. (Pubitemid 41504625)
24. Auluck PK, Chan HY, Trojanowski JQ, Lee VM, Bonini NM (2002) Chaperone suppression of alpha-synuclein toxicity in a Drosophila model for Parkinson's disease. Science 295:865-868. (Pubitemid 34118369)
25. Warrick JM, et al. (1999) Suppression of polyglutamine-mediated neurodegeneration in Drosophila by the molecular chaperone HSP70. Nat Genet 23:425-428.
26. Cummings CJ, et al. (2001) Over-expression of inducible HSP70 chaperone suppresses neuropathology and improves motor function in SCA1 mice. Hum Mol Genet 10:1511-1518. (Pubitemid 32684893)
27. Fernandez-Funez P, et al. (2000) Identification of genes that modify ataxin-1-induced neurodegeneration. Nature 408:101-106.
28. Muchowski PJ, et al. (2000) Hsp70 and hsp40 chaperones can inhibit self-assembly of polyglutamine proteins into amyloid-like fibrils. Proc Natl Acad Sci USA 97:7841-7846. (Pubitemid 30460735)
29. Prahlad V, Cornelius T, Morimoto RI (2008) Regulation of the cellular heat shock response in Caenorhabditis elegans by thermosensory neurons. Science 320:811-814. (Pubitemid 351929633)
30. Inada H, et al. (2006) Identification of guanylyl cyclases that function in thermosensory neurons of Caenorhabditis elegans. Genetics 172:2239-2252.
31. Hobert O, et al. (1997) Regulation of interneuron function in the C. elegans thermoregulatory pathway by the ttx-3 LIM homeobox gene. Neuron 19:345-357. (Pubitemid 27374233)
32. Mohri-Shiomi A, Garsin DA (2008) Insulin signaling and the heat shock response modulate protein homeostasis in the Caenorhabditis elegans intestine during infection. J Biol Chem 283:194-201.
33. Kahn-Kirby AH, Bargmann CI (2006) TRP channels in C. elegans. Annu Rev Physiol 68:719-736.
34. Morley JF, Brignull HR, Weyers JJ, Morimoto RI (2002) The threshold for polyglutamine-expansion protein aggregation and cellular toxicity is dynamic and influenced by aging in Caenorhabditis elegans. Proc Natl Acad Sci USA 99:10417-10422.
35. Gidalevitz T, Krupinski T, Garcia S, Morimoto RI (2009) Destabilizing protein polymorphisms in the genetic background direct phenotypic expression of mutant SOD1 toxicity. PLoS Genet 5:e1000399.
36. Gidalevitz T, Ben-Zvi A, Ho KH, Brignull HR, Morimoto RI (2006) Progressive disruption of cellular protein folding in models of polyglutamine diseases. Science 311:1471-1474. (Pubitemid 43376703)
37. Gengyo-Ando K, Kagawa H (1991) Single charge change on the helical surface of the paramyosin rod dramatically disrupts thick filament assembly in Caenorhabditis elegans. J Mol Biol 219:429-441.
38. Hammarlund M, Watanabe S, Schuske K, Jorgensen EM (2008) CAPS and syntaxin dock dense core vesicles to the plasma membrane in neurons. J Cell Biol 180:483-491. (Pubitemid 351240698)
39. Speese S, et al. (2007) UNC-31 (CAPS) is required for dense-core vesicle but not synaptic vesicle exocytosis in Caenorhabditis elegans. J Neurosci 27:6150-6162. (Pubitemid 46890013)
40. Morley JF, Morimoto RI (2004) Regulation of longevity in Caenorhabditis elegans by heat shock factor and molecular chaperones. Mol Biol Cell 15:657-664. (Pubitemid 38146482)
41. Feder JH, Rossi JM, Solomon J, Solomon N, Lindquist S (1992) The consequences of expressing hsp70 in Drosophila cells at normal temperatures. Genes Dev 6:1402-1413.
42. 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.
43. Dai C, Whitesell L, Rogers AB, Lindquist S (2007) Heat shock factor 1 is a powerful multifaceted modifier of carcinogenesis. Cell 130:1005-1018. (Pubitemid 47410269)
44. Sugi T, Nishida Y, Mori I (2011) Regulation of behavioral plasticity by systemic temperature signaling in Caenorhabditis elegans. Nat Neurosci, 10.1038/nn.2854.
45. Sternberg EM (2006) Neural regulation of innate immunity: A coordinated nonspecific host response to pathogens. Nat Rev Immunol 6:318-328.
46. Tracey KJ (2002) The inflammatory reflex. Nature 420:853-859.
47. Spampanato J, Gu X, Yang XW, Mody I (2008) Progressive synaptic pathology of motor cortical neurons in a BAC transgenic mouse model of Huntington's disease. Neuroscience 157:606-620.
48. Mentis GZ, et al. (2011) Early functional impairment of sensory-motor connectivity in a mouse model of spinal muscular atrophy. Neuron 69:453-467.
49. Ilieva HS, et al. (2008) Mutant dynein (Loa) triggers proprioceptive axon loss that extends survival only in the SOD1 ALS model with highest motor neuron death. Proc Natl Acad Sci USA 105:12599-12604.