Transcellular chaperone signaling: An organismal strategy for integrated cell stress responses

Journal of Experimental Biology

Volumn 217, Issue 1, 2014, Pages 129-136

  Van Oosten Hawle, Patricija ^a   Morimoto, Richard I ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Caenorhabditis elegans; Cell non Autonomous; Chaperones; Metazoans; Proteostasis; Stress response

Indexed keywords

CAENORHABDITIS ELEGANS PROTEIN; HEAT SHOCK FACTOR 1, C ELEGANS; HEAT SHOCK FACTOR-1, C ELEGANS; HEAT SHOCK PROTEIN; TRANSCRIPTION FACTOR;

AGING; ANIMAL; CAENORHABDITIS ELEGANS; CELL COMMUNICATION; CELL NON-AUTONOMOUS; CHAPERONES; ENDOPLASMIC RETICULUM; HEAT SHOCK RESPONSE; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PROTEIN FOLDING; PROTEIN HOMEOSTASIS; REVIEW; SENSORY RECEPTOR; SIGNAL TRANSDUCTION; STRESS; UNFOLDED PROTEIN RESPONSE;

CAENORHABDITIS ELEGANS; CELL NON-AUTONOMOUS; CHAPERONES; METAZOANS; PROTEOSTASIS; STRESS RESPONSE;

AGING; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL COMMUNICATION; ENDOPLASMIC RETICULUM; HEAT-SHOCK PROTEINS; HEAT-SHOCK RESPONSE; PROTEIN FOLDING; SENSORY RECEPTOR CELLS; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; TRANSCRIPTION FACTORS; UNFOLDED PROTEIN RESPONSE;

EID: 84896516202     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.091249     Document Type: Review

References (105)

1. Abravaya, K., Phillips, B. and Morimoto, R. I. (1991). Attenuation of the heat shock response in HeLa cells is mediated by the release of bound heat shock transcription factor and is modulated by changes in growth and in heat shock temperatures. Genes Dev. 5, 2117-2127
2. Abravaya, K., Myers, M. P., Murphy, S. P. and Morimoto, R. I. (1992). The human heat shock protein hsp70 interacts with HSF, the transcription factor that regulates heat shock gene expression. Genes Dev. 6, 1153-1164
3. Åkerfelt, 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
4. Alcedo, J. and Kenyon, C. (2004). Regulation of C. Elegans longevity by specific gustatory and olfactory neurons. Neuron 41, 45-55
5. Ali, A., Bharadwaj, S., O'Carroll, R. and Ovsenek, N. (1998). HSP90 interacts with and regulates the activity of heat shock factor 1 in Xenopus oocytes. Mol. Cell. Biol. 18, 4949-4960
6. Altun, Z. F., Chen, B., Wang, Z. W. and Hall, D. H. (2009). High resolution map of Caenorhabditis elegans gap junction proteins. Dev. Dyn. 238, 1936-1950
7. Anckar, J. and Sistonen, L. (2007). SUMO: getting it on. Biochem. Soc. Trans. 35, 1409-1413
8. Anfinsen, C. B. (1973). Principles that govern the folding of protein chains. Science 181, 223-230
9. Arantes-Oliveira, N., Apfeld, J., Dillin, A. and Kenyon, C. (2002). Regulation of lifespan by germ-line stem cells in Caenorhabditis elegans. Science 295, 502-505
10. Azzam, E. I. and Little, J. B. (2004). The radiation-induced bystander effect: evidence and significance. Hum. Exp. Toxicol. 23, 61-65
11. Azzam, E. I., de Toledo, S. M. and Little, J. B. (2004). Stress signaling from irradiated to non-irradiated cells. Curr. Cancer Drug Targets 4, 53-64
12. Balch, W. E., Morimoto, R. I., Dillin, A. and Kelly, J. W. (2008). Adapting proteostasis for disease intervention. Science 319, 916-919
13. Baler, R., Dahl, G. and Voellmy, R. (1993). Activation of human heat shock genes is accompanied by oligomerization, modification, and rapid translocation of heat shock transcription factor HSF1. Mol. Cell. Biol. 13, 2486-2496
14. Baulcombe, D. (2004). RNA silencing in plants. Nature 431, 356-363
15. Baumeister, R., Schaffitzel, E. and Hertweck, M. (2006). Endocrine signaling in Caenorhabditis elegans controls stress response and longevity. J. Endocrinol. 190, 191-202
16. Ben-Zvi, A., Miller, E. A. and Morimoto, R. I. (2009). Collapse of proteostasis represents an early molecular event in Caenorhabditis elegans aging. Proc. Natl. Acad. Sci. USA 106, 14914-14919
17. Blüher, M., Kahn, B. B. and Kahn, C. R. (2003). Extended longevity in mice lacking the insulin receptor in adipose tissue. Science 299, 572-574
18. Brignull, H. R., Morley, J. F., Garcia, S. M. and Morimoto, R. I. (2006a). Modeling polyglutamine pathogenesis in C. Elegans. Methods Enzymol. 412, 256-282
19. Brignull, H. R., Moore, F. E., Tang, S. J. and Morimoto, R. I. (2006b). Polyglutamine proteins at the pathogenic threshold display neuron-specific aggregation in a panneuronal Caenorhabditis elegans model. J. Neurosci. 26, 7597-7606
20. Carrington, J. C. and Ambros, V. (2003). Role of microRNAs in plant and animal development. Science 301, 336-338
21. Caterina, M. J., Schumacher, M. A., Tominaga, M., Rosen, T. A., Levine, J. D. and Julius, D. (1997). The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389, 816-824
22. Chen, X., Liang, H., Zhang, J., Zen, K. and Zhang, C. Y. (2012). Secreted microRNAs: a new form of intercellular communication. Trends Cell Biol. 22, 125- 132
23. 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
24. Chim, S. S., Shing, T. K., Hung, E. C., Leung, T. Y., Lau, T. K., Chiu, R. W. and Lo, Y. M. (2008). Detection and characterization of placental microRNAs in maternal plasma. Clin. Chem. 54, 482-490
25. Clapham, D. E. (2003). TRP channels as cellular sensors. Nature 426, 517-524
26. Cohen, E., Bieschke, J., Perciavalle, R. M., Kelly, J. W. and Dillin, A. (2006). Opposing activities protect against age-onset proteotoxicity. Science 313, 1604- 1610
27. Cohen, E., Paulsson, J. F., Blinder, P., Burstyn-Cohen, T., Du, D., Estepa, G., Adame, A., Pham, H. M., Holzenberger, M., Kelly, J. W. et al. (2009). Reduced IGF-1 signaling delays age-associated proteotoxicity in mice. Cell 139, 1157-1169
28. Cypser, J. and Johnson, T. E. (2001). Hormesis extends the correlation between stress resistance and life span in long-lived mutants of Caenorhabditis elegans. Hum. Exp. Toxicol. 20, 295-296, discussion 319-320
29. de Bono, M. and Maricq, A. V. (2005). Neuronal substrates of complex behaviors in C. Elegans. Annu. Rev. Neurosci. 28, 451-501
30. Demontis, F. and Perrimon, N. (2010). FOXO/4E-BP signaling in Drosophila muscles regulates organism-wide proteostasis during aging. Cell 143, 813-825
31. Denef, C. (2008). Paracrinicity: the story of 30 years of cellular pituitary crosstalk. J. Neuroendocrinol. 20, 1-70
32. Drummond, D. A. and Wilke, C. O. (2008). Mistranslation-induced protein misfolding as a dominant constraint on coding-sequence evolution. Cell 134, 341-352
33. Durieux, J., Wolff, S. and Dillin, A. (2011). The cell-non-autonomous nature of electron transport chain-mediated longevity. Cell 144, 79-91
34. Ellis, R. J. and Minton, A. P. (2006). Protein aggregation in crowded environments. Biol. Chem. 387, 485-497
35. Feinberg, E. H. and Hunter, C. P. (2003). Transport of dsRNA into cells by the transmembrane protein SID-1. Science 301, 1545-1547
36. Gallio, M., Ofstad, T. A., Macpherson, L. J., Wang, J. W. and Zuker, C. S. (2011). The coding of temperature in the Drosophila brain. Cell 144, 614-624
37. Garcia, S. M., Casanueva, M. O., Silva, M. C., Amaral, M. D. and Morimoto, R. I. (2007). Neuronal signaling modulates protein homeostasis in Caenorhabditis elegans post-synaptic muscle cells. Genes Dev. 21, 3006-3016
38. Gidalevitz, T., Ben-Zvi, A., Ho, K. H., Brignull, H. R. and Morimoto, R. I. (2006). Progressive disruption of cellular protein folding in models of polyglutamine diseases. Science 311, 1471-1474
39. Grant, B. and Hirsh, D. (1999). Receptor-mediated endocytosis in the Caenorhabditis elegans oocyte. Mol. Biol. Cell 10, 4311-4326
40. Guettouche, T., Boellmann, F., Lane, W. S. and Voellmy, R. (2005). Analysis of phosphorylation of human heat shock factor 1 in cells experiencing a stress. BMC Biochem. 6, 4
41. Hamada, N., Kodama, S., Suzuki, K. and Watanabe, M. (2003). Gap junctional intercellular communication and cellular response to heat stress. Carcinogenesis 24, 1723-1728
42. Haynes, C. M. and Ron, D. (2010). The mitochondrial UPR - protecting organelle protein homeostasis. J. Cell Sci. 123, 3849-3855
43. Hietakangas, V., Ahlskog, J. K., Jakobsson, A. M., Hellesuo, M., Sahlberg, N. M., Holmberg, C. I., Mikhailov, A., Palvimo, J. J., Pirkkala, L. and Sistonen, L. (2003). Phosphorylation of serine 303 is a prerequisite for the stress-inducible SUMO modification of heat shock factor 1. Mol. Cell. Biol. 23, 2953-2968
44. Holmberg, C. I., Hietakangas, V., Mikhailov, A., Rantanen, J. O., Kallio, M., Meinander, A., Hellman, J., Morrice, N., MacKintosh, C., Morimoto, R. I. et al. (2001). Phosphorylation of serine 230 promotes inducible transcriptional activity of heat shock factor 1. EMBO J. 20, 3800-3810
45. Hsu, A. L., Murphy, C. T. and Kenyon, C. (2003). Regulation of aging and age-related disease by DAF-16 and heat-shock factor. Science 300, 1142-1145
46. Hwangbo, D. S., Gershman, B., Tu, M. P., Palmer, M. and Tatar, M. (2004). Drosophila dFOXO controls lifespan and regulates insulin signalling in brain and fat body. Nature 429, 562-566
47. Inada, H., Ito, H., Satterlee, J., Sengupta, P., Matsumoto, K. and Mori, I. (2006). Identification of guanylyl cyclases that function in thermosensory neurons of Caenorhabditis elegans. Genetics 172, 2239-2252
48. Jones-Rhoades, M. W., Bartel, D. P. and Bartel, B. (2006). MicroRNAS and their regulatory roles in plants. Annu. Rev. Plant Biol. 57, 19-53
49. Jose, A. M., Smith, J. J. and Hunter, C. P. (2009). Export of RNA silencing from C. Elegans tissues does not require the RNA channel SID-1. Proc. Natl. Acad. Sci. USA 106, 2283-2288
50. Kjenseth, A., Fykerud, T., Rivedal, E. and Leithe, E. (2010). Regulation of gap junction intercellular communication by the ubiquitin system. Cell. Signal. 22, 1267- 1273
51. Kline, M. P. and Morimoto, R. I. (1997). Repression of the heat shock factor 1 transcriptional activation domain is modulated by constitutive phosphorylation. Mol. Cell. Biol. 17, 2107-2115
52. Kurosu, H., Yamamoto, M., Clark, J. D., Pastor, J. V., Nandi, A., Gurnani, P., McGuinness, O. P., Chikuda, H., Yamaguchi, M., Kawaguchi, H. et al. (2005). Suppression of aging in mice by the hormone Klotho. Science 309, 1829-1833
53. Lage, K., Hansen, N. T., Karlberg, E. O., Eklund, A. C., Roque, F. S., Donahoe, P. K., Szallasi, Z., Jensen, T. S. and Brunak, S. (2008). A large-scale analysis of tissue-specific pathology and gene expression of human disease genes and complexes. Proc. Natl. Acad. Sci. USA 105, 20870-20875
54. Lawrie, C. H., Gal, S., Dunlop, H. M., Pushkaran, B., Liggins, A. P., Pulford, K., Banham, A. H., Pezzella, F., Boultwood, J., Wainscoat, J. S. et al. (2008). Detection of elevated levels of tumour-associated microRNAs in serum of patients with diffuse large B-cell lymphoma. Br. J. Haematol. 141, 672-675
55. Lee, S. J. and Kenyon, C. (2009). Regulation of the longevity response to temperature by thermosensory neurons in Caenorhabditis elegans. Curr. Biol. 19, 715-722
56. Lee, R. C., Feinbaum, R. L. and Ambros, V. (1993). The C. Elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75, 843-854
57. Lee, J. W., Beebe, K., Nangle, L. A., Jang, J., Longo-Guess, C. M., Cook, S. A., Davisson, M. T., Sundberg, J. P., Schimmel, P. and Ackerman, S. L. (2006). Editing-defective tRNA synthetase causes protein misfolding and neurodegeneration. Nature 443, 50-55
58. Lindquist, S. L. and Kelly, J. W. (2011). Chemical and biological approaches for adapting proteostasis to ameliorate protein misfolding and aggregation diseases: progress and prognosis. Cold Spring Harb. Perspect. Biol. 3, a004507
59. Liu, Y. and Chang, A. (2008). Heat shock response relieves ER stress. EMBO J. 27, 1049-1059
60. Liu, Q., Chen, B., Gaier, E., Joshi, J. and Wang, Z. W. (2006). Low conductance gap junctions mediate specific electrical coupling in body-wall muscle cells of Caenorhabditis elegans. J. Biol. Chem. 281, 7881-7889
61. Lu, R., Maduro, M., Li, F., Li, H. W., Broitman-Maduro, G., Li, W. X. and Ding, S. W. (2005). Animal virus replication and RNAi-mediated antiviral silencing in Caenorhabditis elegans. Nature 436, 1040-1043
62. McMullen, P. D., Aprison, E. Z., Winter, P. B., Amaral, L. A., Morimoto, R. I. and Ruvinsky, I. (2012). Macro-level modeling of the response of C. Elegans reproduction to chronic heat stress. PLOS Comput. Biol. 8, e1002338
63. Mitchell, S. A., Randers-Pehrson, G., Brenner, D. J. and Hall, E. J. (2004a). The bystander response in C3H 10T1/2 cells: the influence of cell-to-cell contact. Radiat. Res. 161, 397-401
64. Mitchell, S. A., Marino, S. A., Brenner, D. J. and Hall, E. J. (2004b). Bystander effect and adaptive response in C3H 10T(1/2) cells. Int. J. Radiat. Biol. 80, 465-472
65. Mori, I. (1999). Genetics of chemotaxis and thermotaxis in the nematode Caenorhabditis elegans. Annu. Rev. Genet. 33, 399-422
66. Mori, I., Sasakura, H. and Kuhara, A. (2007). Worm thermotaxis: a model system for analyzing thermosensation and neural plasticity. Curr. Opin. Neurobiol. 17, 712- 719
67. 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
68. 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. USA 99, 10417-10422
69. Nargund, A. M., Pellegrino, M. W., Fiorese, C. J., Baker, B. M. and Haynes, C. M. (2012). Mitochondrial import efficiency of ATFS-1 regulates mitochondrial UPR activation. Science 337, 587-590
70. Nussbaum-Krammer, C. I., Park, K. W., Li, L., Melki, R. and Morimoto, R. I. (2013). Spreading of a prion domain from cell-to-cell by vesicular transport in Caenorhabditis elegans. PLoS Genet. 9, e1003351
71. Orr, H. T. and Zoghbi, H. Y. (2007). Trinucleotide repeat disorders. Annu. Rev. Neurosci. 30, 575-621
72. Powers, E. T., Morimoto, R. I., Dillin, A., Kelly, J. W. and Balch, W. E. (2009). Biological and chemical approaches to diseases of proteostasis deficiency. Annu. Rev. Biochem. 78, 959-991
73. Prahlad, V. and Morimoto, R. I. (2009). Integrating the stress response: lessons for neurodegenerative diseases from C. Elegans. Trends Cell Biol. 19, 52-61
74. Prahlad, V. and Morimoto, R. I. (2011). Neuronal circuitry regulates the response of Caenorhabditis elegans to misfolded proteins. Proc. Natl. Acad. Sci. USA 108, 14204-14209
75. Prahlad, V., Cornelius, T. and Morimoto, R. I. (2008). Regulation of the cellular heat shock response in Caenorhabditis elegans by thermosensory neurons. Science 320, 811-814
76. Provost, N., Moreau, M., Leturque, A. and Nizard, C. (2003). Ultraviolet A radiation transiently disrupts gap junctional communication in human keratinocytes. Am. J. Physiol. 284, C51-C59
77. Qi, W., Huang, X., Neumann-Haefelin, E., Schulze, E. and Baumeister, R. (2012). Cell-nonautonomous signaling of FOXO/DAF-16 to the stem cells of Caenorhabditis elegans. PLoS Genet. 8, e1002836
78. Ron, D. and Walter, P. (2007). Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Rev. Mol. Cell Biol. 8, 519-529
79. Saleh, M. C., van Rij, R. P., Hekele, A., Gillis, A., Foley, E., O'Farrell, P. H. and Andino, R. (2006). The endocytic pathway mediates cell entry of dsRNA to induce RNAi silencing. Nat. Cell Biol. 8, 793-802
80. Samuelson, A. V., Carr, C. E. and Ruvkun, G. (2007). Gene activities that mediate increased life span of C. Elegans insulin-like signaling mutants. Genes Dev. 21, 2976-2994
81. 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 DNAbinding activity, and nuclear localization and can occur in the absence of stress. Mol. Cell. Biol. 13, 1392-1407
82. Satyal, S. H., Schmidt, E., Kitagawa, K., Sondheimer, N., Lindquist, S., Kramer, J. M. and Morimoto, R. I. (2000). Polyglutamine aggregates alter protein folding homeostasis in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 97, 5750-5755
83. Saumet, A. and Lecellier, C. H. (2006). Anti-viral RNA silencing: do we look like plants? Retrovirology 3, 3
84. Schröder, M. and Kaufman, R. J. (2005). The mammalian unfolded protein response. Annu. Rev. Biochem. 74, 739-789
85. Shapiro, J. A. (1998). Thinking about bacterial populations as multicellular organisms. Annu. Rev. Microbiol. 52, 81-104
86. Sherer, N. M. and Mothes, W. (2008). Cytonemes and tunneling nanotubules in cellcell communication and viral pathogenesis. Trends Cell Biol. 18, 414-420
87. Shi, Y., Mosser, D. D. and Morimoto, R. I. (1998). Molecular chaperones as HSF1- specific transcriptional repressors. Genes Dev. 12, 654-666
88. Sieburth, D., Madison, J. M. and Kaplan, J. M. (2007). PKC-1 regulates secretion of neuropeptides. Nat. Neurosci. 10, 49-57
89. Singer, S. J. (1992). Intercellular communication and cell-cell adhesion. Science 255, 1671-1677
90. Styer, K. L., Singh, V., Macosko, E., Steele, S. E., Bargmann, C. I. and Aballay, A. (2008). Innate immunity in Caenorhabditis elegans is regulated by neurons expressing NPR-1/GPCR. Science 322, 460-464
91. Sugi, T., Nishida, Y. and Mori, I. (2011). Regulation of behavioral plasticity by systemic temperature signaling in Caenorhabditis elegans. Nat. Neurosci. 14, 984-992
92. Sun, J., Singh, V., Kajino-Sakamoto, R. and Aballay, A. (2011). Neuronal GPCR controls innate immunity by regulating noncanonical unfolded protein response genes. Science 332, 729-732
93. Sun, J., Liu, Y. and Aballay, A. (2012). Organismal regulation of XBP-1-mediated unfolded protein response during development and immune activation. EMBO Rep. 13, 855-860
94. Taylor, R. C. and Dillin, A. (2013). XBP-1 is a cell-nonautonomous regulator of stress resistance and longevity. Cell 153, 1435-1447
95. Upham, B. L., Deocampo, N. D., Wurl, B. and Trosko, J. E. (1998). Inhibition of gap junctional intercellular communication by perfluorinated fatty acids is dependent on the chain length of the fluorinated tail. Int. J. Cancer 78, 491-495
96. Valadi, H., Ekström, K., Bossios, A., Sjöstrand, M., Lee, J. J. and Lötvall, J. O. (2007). Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat. Cell Biol. 9, 654-659
97. van Oosten-Hawle, P., Porter, R. S. and Morimoto, R. I. (2013). Regulation of organismal proteostasis by transcellular chaperone signaling. Cell 153, 1366-1378
98. Voets, T., Droogmans, G., Wissenbach, U., Janssens, A., Flockerzi, V. and Nilius, B. (2004). The principle of temperature-dependent gating in cold- and heat-sensitive TRP channels. Nature 430, 748-754
99. Voinnet, O. (2001). RNA silencing as a plant immune system against viruses. Trends Genet. 17, 449-459
100. 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
101. Wilkins, C., Dishongh, R., Moore, S. C., Whitt, M. A., Chow, M. and Machaca, K. (2005). RNA interference is an antiviral defence mechanism in Caenorhabditis elegans. Nature 436, 1044-1047
102. Xiao, R. and Shawn Xu, X. Z. (2011). Studying TRP channels in Caenorhabditis elegans. In TRP Channels (ed. M. X. Zhu). Boca Raton, FL: CRC Press
103. Xiao, R., Zhang, B., Dong, Y., Gong, J., Xu, T., Liu, J. and Xu, X. Z. (2013). A genetic program promotes C. Elegans longevity at cold temperatures via a thermosensitive TRP channel. Cell 152, 806-817
104. Zhang, P., Judy, M., Lee, S. J. and Kenyon, C. (2013). 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
105. Zou, J., Guo, Y., Guettouche, T., Smith, D. F. and 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