Systemic stress signalling: Understanding the cell non-autonomous control of proteostasis

Nature Reviews Molecular Cell Biology

Volumn 15, Issue 3, 2014, Pages 211-217

  Taylor, Rebecca C ^a   Berendzen, Kristen M ^a   Dillin, Andrew ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL AGING; CELL SURVIVAL; HUMANS; MODELS, BIOLOGICAL; PROTEOME; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL;

EID: 84894539428     PISSN: 14710072     EISSN: 14710080     Source Type: Journal    
DOI: 10.1038/nrm3752     Document Type: Review

References (73)

1. Balch, W. E., Morimoto, R. I., Dillin, A. & Kelly, J. W. Adapting proteostasis for disease intervention. Science 319, 916-919 (2008).
2. David, D. C. et al. Widespread protein aggregation as an inherent part of aging in C. elegans. PLoS Biol. 8, e1000450 (2010).
3. Poon, H. F., Vaishnav, R. A., Getchell, T. V., Getchell, M. L. & Butterfield, D. A. Quantitative proteomics analysis of differential protein expression and oxidative modification of specific proteins in the brains of old mice. Neurobiol. Aging 27, 1010-1019 (2006).
4. Ben-Zvi, A., Miller, E. A. & Morimoto, R. I. Collapse of proteostasis represents an early molecular event in Caenorhabditis elegans aging. Proc. Natl Acad. Sci. USA 106, 14914-14919 (2009).
5. Cotto, J. J. & Morimoto, R. I. Stress-induced activation of the heat-shock response: cell and molecular biology of heat-shock factors. Biochem. Soc. Symp. 64, 105-118 (1999).
6. Ron, D. & Walter, P. Signal integration in the endoplasmic reticulum unfolded protein response. Nature Rev. Mol. Cell Biol. 8, 519-529 (2007).
7. Spradling, A., Penman, S. & Pardue, M. L. Analysis of drosophila mRNA by in situ hybridization: sequences transcribed in normal and heat shocked cultured cells. Cell 4, 395-404 (1975).
8. McKenzie, S. L., Henikoff, S. & Meselson, M. Localization of RNA from heat-induced polysomes at puff sites in Drosophila melanogaster. Proc. Natl Acad. Sci. USA 72, 1117-1121 (1975).
9. Ilieva, H., Polymenidou, M. & Cleveland, D. W. Non-cell autonomous toxicity in neurodegenerative disorders: ALS and beyond. J. Cell Biol. 187, 761-772 (2009).
10. Herndon, L. A. et al. Stochastic and genetic factors influence tissue-specific decline in ageing C. elegans. Nature 419, 808-814 (2002).
11. Apfeld, J. & Kenyon, C. Cell nonautonomy of C. elegans daf-2 function in the regulation of diapause and life span. Cell 95, 199-210 (1998).
12. Wolkow, C. A., Kimura, K. D., Lee, M. S. & Ruvkun, G. Regulation of C. elegans life-span by insulinlike signaling in the nervous system. Science 290, 147-150 (2000).
13. Durieux, J., Wolff, S. & Dillin, A. The cell-non-autonomous nature of electron transport chain-mediated longevity. Cell 144, 79-91 (2011).
14. Bishop, N. A. & Guarente, L. Two neurons mediate diet-restriction- induced longevity in C. elegans. Nature 447, 545-549 (2007).
15. Hsin, H. & Kenyon, C. Signals from the reproductive system regulate the lifespan of C. elegans. Nature 399, 362-366 (1999).
16. Arantes-Oliveira, N., Apfeld, J., Dillin, A. & Kenyon, C. Regulation of life-span by germ-line stem cells in Caenorhabditis elegans. Science 295, 502-505 (2002).
17. Kenyon, C., Chang, J., Gensch, E., Rudner, A. & Tabtiang, R. A. C. elegans mutant that lives twice as long as wild type. Nature 366, 461-464 (1993).
18. Hwangbo, D. S., Gershman, B., Tu, M. P., Palmer, M. & Tatar, M. Drosophila dFOXO controls lifespan and regulates insulin signalling in brain and fat body. Nature 429, 562-566 (2004).
19. Giannakou, M. E. et al. Long-lived Drosophila with overexpressed dFOXO in adult fat body. Science 305, 361 (2004).
20. Holzenberger, M. et al. IGF-1 receptor regulates lifespan and resistance to oxidative stress in mice. Nature 421, 182-187 (2003).
21. Antebi, A. Regulation of longevity by the reproductive system. Exp. Gerontol. 48, 596-602 (2013).
22. Taylor, R. C. & Dillin, A. Aging as an event of proteostasis collapse. Cold Spring Harb. Perspect. Biol. 3, a004440 (2011).
23. Powers, E. T. & Balch, W. E. Diversity in the origins of proteostasis networks-a driver for protein function in evolution. Nature Rev. Mol. Cell Biol. 14, 237-248 (2013).
24. Akerfelt, M., Morimoto, R. I. & Sistonen, L. Heat shock factors: integrators of cell stress, development and lifespan. Nature Rev. Mol. Cell Biol. 11, 545-555 (2010).
25. Haynes, C. M. & Ron, D. The mitochondrial UPR-protecting organelle protein homeostasis. J. Cell Sci. 123, 3849-3855 (2010).
26. Mori, I. & Ohshima, Y. Neural regulation of thermotaxis in Caenorhabditis elegans. Nature 376, 344-348 (1995).
27. Prahlad, V., Cornelius, T. & Morimoto, R. I. Regulation of the cellular heat shock response in Caenorhabditis elegans by thermosensory neurons. Science 320, 811-814 (2008).
28. Lee, S. J. & Kenyon, C. Regulation of the longevity response to temperature by thermosensory neurons in Caenorhabditis elegans. Curr. Biol. 19, 715-722 (2009).
29. Prahlad, V. & Morimoto, R. I. Neuronal circuitry regulates the response of Caenorhabditis elegans to misfolded proteins. Proc. Natl Acad. Sci. USA 108, 14204-14209 (2011).
30. Maman, M. et al. A neuronal GPCR is critical for the induction of the heat shock response in the nematode C. elegans. J. Neurosci. 33, 6102-6111 (2013).
31. Beverly, M., Anbil, S. & Sengupta, P. Degeneracy and neuromodulation among thermosensory neurons contribute to robust thermosensory behaviors in Caenorhabditis elegans. J. Neurosci. 31, 11718-11727 (2011).
32. Hobert, O., D'Alberti, T., Liu, Y. & Ruvkun, G. Control of neural development and function in a thermoregulatory network by the LIM homeobox gene lin-11. J. Neurosci. 18, 2084-2096 (1998).
33. Garcia, S. M., Casanueva, M. O., Silva, M. C., Amaral, M. D. & Morimoto, R. I. Neuronal signaling modulates protein homeostasis in Caenorhabditis elegans post-synaptic muscle cells. Genes Dev. 21, 3006-3016 (2007).
34. van Oosten-Hawle, P., Porter, R. S. & Morimoto, R. I. Regulation of organismal proteostasis by transcellular chaperone signaling. Cell 153, 1366-1378 (2013).
35. Fawcett, T. W., Sylvester, S. L., Sarge, K. D., Morimoto, R. I. & Holbrook, N. J. Effects of neurohormonal stress and aging on the activation of mammalian heat shock factor 1. J. Biol. Chem. 269, 32272-32278 (1994).
36. Speese, S. et al. UNC-31 (CAPS) is required for dense-core vesicle but not synaptic vesicle exocytosis in Caenorhabditis elegans. J. Neurosci. 27, 6150-6162 (2007).
37. Martinus, R. D. et al. Selective induction of mitochondrial chaperones in response to loss of the mitochondrial genome. Eur. J. Biochem. 240, 98-103 (1996).
38. Zhao, Q. et al. A mitochondrial specific stress response in mammalian cells. EMBO J. 21, 4411-4419 (2002).
39. Yoneda, T. et al. Compartment-specific perturbation of protein handling activates genes encoding mitochondrial chaperones. J. Cell Sci. 117, 4055-4066 (2004).
40. Haynes, C. M., Petrova, K., Benedetti, C., Yang, Y. & Ron, D. ClpP mediates activation of a mitochondrial unfolded protein response in C. elegans. Dev. Cell 13, 467-480 (2007).
41. Dillin, A. et al. Rates of behavior and aging specified by mitochondrial function during development. Science 298, 2398-2401 (2002).
42. Kim, K. H. et al. Autophagy deficiency leads to protection from obesity and insulin resistance by inducing Fgf21 as a mitokine. Nature Med. 19, 83-92 (2013).
43. Suomalainen, A. et al. FGF-21 as a biomarker for muscle-manifesting mitochondrial respiratory chain deficiencies: a diagnostic study. Lancet Neurol. 10, 806-818 (2011).
44. Houtkooper, R. H. et al. Mitonuclear protein imbalance as a conserved longevity mechanism. Nature 497, 451-457 (2013).
45. Mouchiroud, L. et al. The NAD+/Sirtuin pathway modulates longevity through activation of mitochondrial UPR and FOXO signaling. Cell 154, 430-441 (2013).
46. Lee, C., Yen, K. & Cohen, P. Humanin: a harbinger of mitochondrial-derived peptides? Trends Endocrinol. Metab. 24, 222-228 (2013).
47. Yen, K., Lee, C., Mehta, H. & Cohen, P. The emerging role of the mitochondrial-derived peptide humanin in stress resistance. J. Mol. Endocrinol. 50, R11-R19 (2013).
48. Richardson, C. E., Kooistra, T. & Kim, D. H. An essential role for XBP-1 in host protection against immune activation in C. elegans. Nature 463, 1092-1095 (2010).
49. Richardson, C. E., Kinkel, S. & Kim, D. H. Physiological IRE-1-XBP-1 and PEK-1 signaling in Caenorhabditis elegans larval development and immunity. PLoS Genet. 7, e1002391 (2011).
50. Sun, J., Singh, V., Kajino-Sakamoto, R. & Aballay, A. Neuronal GPCR controls innate immunity by regulating noncanonical unfolded protein response genes. Science 332, 729-732 (2011).
51. Urano, F. et al. A survival pathway for Caenorhabditis elegans with a blocked unfolded protein response. J. Cell Biol. 158, 639-646 (2002).
52. Sun, J., Liu, Y. & Aballay, A. Organismal regulation of XBP-1-mediated unfolded protein response during development and immune activation. EMBO Rep. 13, 855-860 (2012).
53. Taylor, R. C. & Dillin, A. XBP-1 is a cellnonautonomous regulator of stress resistance and longevity. Cell 153, 1435-1447 (2013).
54. Mahadevan, N. R. et al. Transmission of endoplasmic reticulum stress and pro-inflammation from tumor cells to myeloid cells. Proc. Natl Acad. Sci. USA 108, 6561-6566 (2011).
55. Mahadevan, N. R. et al. Cell-extrinsic effects of tumor ER stress imprint myeloid dendritic cells and impair CD8+ T cell priming. PLoS ONE 7, e51845 (2012).
56. Madison, J. M., Nurrish, S. & Kaplan, J. M. UNC-13 interaction with syntaxin is required for synaptic transmission. Curr. Biol. 15, 2236-2242 (2005).
57. Shiu, R. P., Pouyssegur, J. & Pastan, I. Glucose depletion accounts for the induction of two transformation-sensitive membrane proteinsin Rous sarcoma virus-transformed chick embryo fibroblasts. Proc. Natl Acad. Sci. USA 74, 3840-3844 (1977).
58. Bi, M. et al. ER stress-regulated translation increases tolerance to extreme hypoxia and promotes tumor growth. EMBO J. 24, 3470-3481 (2005).
59. Libina, N., Berman, J. R. & Kenyon, C. Tissue-specific activities of C. elegans DAF-16 in the regulation of lifespan. Cell 115, 489-502 (2003).
60. Bluher, M., Kahn, B. B. & Kahn, C. R. Extended longevity in mice lacking the insulin receptor in adipose tissue. Science 299, 572-574 (2003).
61. Murphy, C. T. et al. Genes that act downstream of DAF-16 to influence the lifespan of Caenorhabditis elegans. Nature 424, 277-283 (2003).
62. Morley, J. F., Brignull, H. R., Weyers, J. J. & Morimoto, R. I. The threshold for polyglutamineexpansion protein aggregation and cellular toxicity is dynamic and influenced by aging in Caenorhabditis elegans. Proc. Natl Acad. Sci. USA 99, 10417-10422 (2002).
63. Cohen, E., Bieschke, J., Perciavalle, R. M., Kelly, J. W. & Dillin, A. Opposing activities protect against ageonset proteotoxicity. Science 313, 1604-1610 (2006).
64. Cohen, E. et al. Reduced IGF-1 signaling delays ageassociated proteotoxicity in mice. Cell 139, 1157-1169 (2009).
65. Demontis, F. & Perrimon, N. FOXO/4E-BP signaling in Drosophila muscles regulates organism-wide proteostasis during aging. Cell 143, 813-825 (2010).
66. Bai, H., Kang, P., Hernandez, A. M. & Tatar, M. Activin signaling targeted by tnsulin/dFOXO regulates aging and muscle proteostasis in Drosophila. PLoS Genet. 9, e1003941 (2013).
67. Owusu-Ansah, E., Song, W. & Perrimon, N. Muscle mitohormesis promotes longevity via systemic repression of insulin signaling. Cell 155, 699-712 (2013).
68. Zhang, P., Judy, M., Lee, S. J. & Kenyon, C. Direct and indirect gene regulation by a life-extending FOXO protein in C. elegans: roles for GATA factors and lipid gene regulators. Cell. Metab. 17, 85-100 (2013).
69. Shemesh, N., Shai, N. & Ben-Zvi, A. Germline stem cell arrest inhibits the collapse of somatic proteostasis early in Caenorhabditis elegans adulthood. Aging Cell 12, 814-822 (2013).
70. Vilchez, D. et al. RPN-6 determines C. elegans longevity under proteotoxic stress conditions. Nature 489, 263-268 (2012).
71. Hult, S. et al. Mutant huntingtin causes metabolic imbalance by disruption of hypothalamic neurocircuits. Cell Metab. 13, 428-439 (2011).
72. Jenkins, B. G., Koroshetz, W. J., Beal, M. F. & Rosen, B. R. Evidence for impairment of energy metabolism in vivo in Huntington's disease using localized 1H NMR spectroscopy. Neurology 43, 2689-2695 (1993).
73. Seong, I. S. et al. HD CAG repeat implicates a dominant property of huntingtin in mitochondrial energy metabolism. Hum. Mol. Genet. 14, 2871-2880 (2005).