Hypertonic stress induces rapid and widespread protein damage in C. elegans

American Journal of Physiology - Cell Physiology

Volumn 301, Issue 3, 2011, Pages

  Burkewitz, Kris ^a   Choe, Keith ^b   Strange, Kevin ^a  

^a MOUNT DESERT ISLAND BIOLOGICAL LABORATORY   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

Author keywords

Caenorhabditis elegans; Cell volume; Kidney; Macromolecular crowding; Organic osmolytes; Polyglutamine; Protein aggregation; Proteostasis

Indexed keywords

CELL PROTEIN; CYTOPLASM PROTEIN; DETERGENT; INSULIN; POLYGLUTAMINE; SODIUM CHLORIDE; YELLOW FLUORESCENT PROTEIN;

ACCLIMATIZATION; ARTICLE; CAENORHABDITIS ELEGANS; CELL TYPE; CONTROLLED STUDY; HYPEROSMOTIC STRESS; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DEFECT; PROTEIN HOMEOSTASIS; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION; WATER LOSS;

ACCLIMATIZATION; ALPHA-SYNUCLEIN; ANIMALS; ANIMALS, GENETICALLY MODIFIED; BACTERIAL PROTEINS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL NUCLEUS; GENES, REPORTER; INCLUSION BODIES; INSULIN; LUMINESCENT PROTEINS; MEMBRANE PROTEINS; MOVEMENT; MUSCLE CELLS; MYOFIBRILS; PARTICLE SIZE; PEPTIDES; PHARYNX; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN KINASES; PROTEOGLYCANS; RAS PROTEINS; RECEPTOR, INSULIN; RECOMBINANT FUSION PROTEINS; RNA, DOUBLE-STRANDED; SALINE SOLUTION, HYPERTONIC; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; TEMPERATURE; TRANSCRIPTION FACTORS; TROPOMYOSIN;

CAENORHABDITIS ELEGANS;

EID: 80052220796     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00030.2011     Document Type: Article

References (56)

1. Balch WE, Morimoto RI, Dillin A, Kelly JW. Adapting proteostasis for disease intervention. Science 319: 916-919, 2008.
2. Beranger F, Crozet C, Goldsborough A, Lehmann S. Trehalose impairs aggregation of PrPSc molecules and protects prion-infected cells against oxidative damage. Biochem Biophys Res Commun 374: 44-48, 2008.
3. Bjork JK, Sistonen L. Regulation of the members of the mammalian heat shock factor family. FEBS J 277: 4126-4139, 2010.
4. Borkan SC, Gullans SR. Molecular chaperones in the kidney. Annu Rev Physiol 64: 503-527, 2002.
5. Brenner S. The genetics of Caenorhabditis elegans. Genetics 77: 71-94, 1974.
6. Brignull H, Morley JF, Morimoto RI. The stress of misfolded proteins: C. elegans models for neurodegenerative disease and aging. Adv Exp Med Biol 594: 167-189, 2007.
7. Brown CR, Hong-Brown LQ, Welch WJ. Correcting temperaturesensitive protein folding defects. J Clin Invest 99: 1432-1444, 1997.
8. Burg MB, Ferraris JD, Dmitrieva NI. Cellular response to hyperosmotic stresses. Physiol Rev 87: 1441-1474, 2007.
9. Campioni S, Mannini B, Zampagni M, Pensalfini A, Parrini C, Evangelisti E, Relini A, Stefani M, Dobson CM, Cecchi C, Chiti F. A causative link between the structure of aberrant protein oligomers and their toxicity. Nat Chem Biol 6: 140-147, 2010.
10. Choe KP, Strange K. Genome-wide RNAi screen and in vivo protein aggregation reporters identify degradation of damaged proteins as an essential hypertonic stress response. Am J Physiol Cell Physiol 295: C1488-C1498, 2008.
11. Christoph K, Beck FX, Neuhofer W. Osmoadaptation of mammalian cells - an orchestrated network of protective genes. Curr Genomics 8: 209-218, 2007.
12. Chun W, Lesort M, Lee M, Johnson GV. Transient osmotic stress facilitates mutant huntingtin aggregation. Neuroreport 13: 2543-2546, 2002.
13. Cohen E, Dillin A. The insulin paradox: aging, proteotoxicity and neurodegeneration. Nat Rev Neurosci 9: 759-767, 2008.
14. David DC, Ollikainen N, Trinidad JC, Cary MP, Burlingame AL, Kenyon C. Widespread protein aggregation as an inherent part of aging in C. elegans. PLoS Biol 8: e1000450, 2010.
15. Diaz-Hernandez M, Moreno-Herrero F, Gomez-Ramos P, Moran MA, Ferrer I, Baro AM, Avila J, Hernandez F, Lucas JJ. Biochemical, ultrastructural, and reversibility studies on huntingtin filaments isolated from mouse and human brain. J Neurosci 24: 9361-9371, 2004.
16. Drummond DA, Wilke CO. The evolutionary consequences of erroneous protein synthesis. Nat Rev Genet 10: 715-724, 2009.
17. Dubus JC, Ravilly S. Inhaled therapies in cystic fibrosis. Rev Mal Respir 25: 989-998, 2008.
18. Ellis RJ, Minton AP. Protein aggregation in crowded environments. Biol Chem 387: 485-497, 2006.
19. Epstein HF, Casey DL, Ortiz I. Myosin and paramyosin of Caenorhabditis elegans embryos assemble into nascent structures distinct from thick filaments and multi-filament assemblages. J Cell Biol 122: 845-858, 1993.
20. Fontana L, Partridge L, Longo VD. Extending healthy life span-from yeast to humans. Science 328: 321-326, 2010.
21. Ghosh K, Dill K. Cellular proteomes have broad distributions of protein stability. Biophys J 99: 3996-4002, 2010.
22. Gidalevitz T, Ben Zvi A, Ho KH, Brignull H, Morimoto RI. Progressive disruption of cellular protein folding in models of polyglutamine diseases. Science 311: 1471-1474, 2006.
23. Goldschmidt L, Teng PK, Riek R, Eisenberg D. Identifying the amylome, proteins capable of forming amyloid-like fibrils. Proc Natl Acad Sci USA 107: 3487-3492, 2010.
24. Haslbeck M, Franzmann T, Weinfurtner D, Buchner J. Some like it hot: the structure and function of small heat-shock proteins. Nat Struct Mol Biol 12: 842-846, 2005.
25. Hoppe T. Too salty for worms: "hypertonic stress challenges proteostasis networks. Focus on "Hypertonic stress induces rapid and widespread protein damage in C. elegans."Am J Physiol Cell Physiol (June 29, 2011). doi:10.1152/ajpcell.00206.2011.
26. Jantzen JP. Prevention and treatment of intracranial hypertension. Best Pract Res Clin Anaesthesiol 21: 517-538, 2007.
27. Jarosz DF, Taipale M, Lindquist S. Protein homeostasis and the phenotypic manifestation of genetic diversity: principles and mechanisms. Annu Rev Genet 44: 189-216, 2010.
28. Katsuno M, Banno H, Suzuki K, Takeuchi Y, Kawashima M, Tanaka F, Adachi H, Sobue G. Molecular genetics and biomarkers of polyglutamine diseases. Curr Mol Med 8: 221-234, 2008.
29. Kayed R, Head E, Thompson JL, McIntire TM, Milton SC, Cotman CW, Glabe CG. Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 300: 486-489, 2003.
30. Kikis EA, Gidalevitz T, Morimoto RI. Protein homeostasis in models of aging and age-related conformational disease. Adv Exp Med Biol 694: 138-159, 2010.
31. Koga H, Kaushik S, Cuervo AM. Protein homeostasis and aging: the importance of exquisite quality control. Ageing Res Rev 10: 205-215, 2011.
32. Kraemer BC, Zhang B, Leverenz JB, Thomas JH, Trojanowski JQ, Schellenberg GD. Neurodegeneration and defective neurotransmission in a Caenorhabditis elegans model of tauopathy. Proc Natl Acad Sci USA 100: 9980-9985, 2003.
33. Kuzik BA, Al Qadhi SA, Kent S, Flavin MP, Hopman W, Hotte S, Gander S. Nebulized hypertonic saline in the treatment of viral bronchiolitis in infants. J Pediatr 151: 266-270, 2007.
34. Lamitina ST, Morrison R, Moeckel GW, Strange K. Adaptation of the nematode Caenorhabditis elegans to extreme osmotic stress. Am J Physiol Cell Physiol 286: C785-C791, 2004.
35. Lamitina ST, Strange K. Transcriptional targets of the DAF-16 insulin signaling pathway protect C. elegans from extreme hypertonic stress. Am J Physiol Cell Physiol 288: C467-C474, 2005.
36. Menzies FM, Huebener J, Renna M, Bonin M, Riess O, Rubinsztein DC. Autophagy induction reduces mutant ataxin-3 levels and toxicity in a mouse model of spinocerebellar ataxia type 3. Brain 133: 93-104, 2010.
37. Morley JF, Brignull H, Weyers JJ, Morimoto RI. 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, 2002.
38. Munishkina LA, Ahmad A, Fink AL, Uversky VN. Guiding protein aggregation with macromolecular crowding. Biochemistry 47: 8993-9006, 2008.
39. Neuhofer W, Beck FX. Survival in hostile environments: strategies of renal medullary cells. Physiology 21: 171-180, 2006.
40. Papia G, Burrows LL, Sinnadurai S, Marshall JC, Tawadros PS, Kapus A, Rotstein OD. Hypertonic saline resuscitation from hemorrhagic shock does not impair the neutrophil response to intraabdominal infection. Surgery 144: 814-821, 2008.
41. Richter K, Haslbeck M, Buchner J. The heat shock response: life on the verge of death. Mol Cell 40: 253-266, 2010.
42. Rutherford SL. Between genotype and phenotype: protein chaperones and evolvability. Nat Rev Genet 4: 263-274, 2003.
43. Ryu J, Kanapathipillai M, Lentzen G, Park CB. Inhibition of betaamyloid peptide aggregation and neurotoxicity by alpha-D-mannosylglycerate, a natural extremolyte. Peptides 29: 578-584, 2008.
44. Satyal SH, Schmidt E, Kitagawa K, Sondheimer N, Lindquist S, Kramer JM, Morimoto RI. Polyglutamine aggregates alter protein folding homeostasis in Caenorhabditis elegans. Proc Natl Acad Sci USA 97: 5750-5755, 2000.
45. Seki T, Abe-Seki N, Kikawada T, Takahashi H, Yamamoto K, Adachi N, Tanaka S, Hide I, Saito N, Sakai N. Effect of trehalose on the properties of mutant gammaPKC, which causes spinocerebellar ataxia type 14, in neuronal cell lines and cultured Purkinje cells. J Biol Chem 285: 33252-33264, 2010.
46. Silveira JR, Raymond GJ, Hughson AG, Race RE, Sim VL, Hayes SF, Caughey B. The most infectious prion protein particles. Nature 257-261, 2005.
47. Singer MA, Lindquist S. Multiple effects of trehalose on protein folding in vitro and in vivo. Mol Cell 1: 639-648, 1998.
48. Somero GN. Protons, osmolytes, and fitness of internal milieu for protein function. Am J Physiol Regul Integr Comp Physiol 251: R197-R213, 1986.
49. Tanaka M, Machida Y, Niu S, Ikeda T, Jana NR, Doi H, Kurosawa M, Nekooki M, Nukina N. Trehalose alleviates polyglutamine-mediated pathology in a mouse model of Huntington disease. Nat Med 10: 148-154, 2004.
50. Uversky VN. Neuropathology, biochemistry, and biophysics of α-synuclein aggregation. J Neurochem 103: 17-37, 2007.
51. Van Dyk TK, Gatenby AA, LaRossa RA. Demonstration by genetic suppression of interaction of GroE products with many proteins. Nature 342: 451-453, 1989.
52. van Ham TJ, Thijssen KL, Breitling R, Hofstra RM, Plasterk RH, Nollen EA. C. elegans model identifies genetic modifiers of α-synuclein inclusion formation during aging. PLoS Genet 4: e1000027, 2008.
53. Yamamoto A, Cremona ML, Rothman JE. Autophagy-mediated clearance of huntingtin aggregates triggered by the insulin-signaling pathway. J Cell Biol 172: 719-731, 2006.
54. Yang DS, Yip CM, Huang TH, Chakrabartty A, Fraser PE. Manipulating the amyloid-beta aggregation pathway with chemical chaperones. J Biol Chem 274: 32970-32974, 1999.
55. Yochem J, Sundaram M, Han M. Ras is required for a limited number of cell fates and not for general proliferation in Caenorhabditis elegans. Mol Cell Biol 17: 2716-2722, 1997.
56. Zhou HX, Rivas G, Minton AP. Macromolecular crowding and confinement: biochemical, biophysical, and potential physiological consequences. Annu Rev Biophys 37: 375-397, 2008.