TRX-1 regulates SKN-1 nuclear localization cell non-autonomously in caenorhabditis elegans

Genetics

Volumn 203, Issue 1, 2016, Pages 387-402

  McCallum, Katie C ^a,b   Liu, Bin ^c   Fierro González, Juan Carlos ^d   Swoboda, Peter ^d   Arur, Swathi ^b,c   Miranda Vizuete, Antonio ^e   Garsin, Danielle A ^a,b  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF TEXAS   (United States)

^c UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^d KAROLINSKA INSTITUTE   (Sweden)

^e HOSPITAL UNIVERSITARIO VIRGEN DEL ROCÍO   (Spain)

Author keywords

ASJ neurons; Caenorhabditis elegans; Cell non autonomous signaling; Oxidative stress response; Thioredoxin

Indexed keywords

CAENORHABDITIS ELEGANS PROTEIN; COLLAGEN; LIPID; MITOGEN ACTIVATED PROTEIN KINASE P38; RNA; THIOREDOXIN; THIOREDOXIN 1; THIOREDOXIN 2; THIOREDOXIN 3; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SKN 1; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; SKN-1 PROTEIN, C ELEGANS; TRX-1 PROTEIN, C ELEGANS;

ADULT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CAENORHABDITIS ELEGANS; CELL NUCLEUS; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; DOWN REGULATION; GENETIC TRANSCRIPTION; LIPID TRANSPORT; NERVE CELL; NONHUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REGULATORY MECHANISM; RNA SEQUENCE; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; YOUNG ADULT; ANIMAL; CYTOLOGY; GENETICS; INTESTINE; METABOLISM; NUCLEOCYTOPLASMIC TRANSPORT; OXIDATIVE STRESS;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL NUCLEUS; DNA-BINDING PROTEINS; INTESTINES; NEURONS; OXIDATIVE STRESS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; SIGNAL TRANSDUCTION; THIOREDOXINS; TRANSCRIPTION FACTORS;

EID: 84979903024     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.115.185272     Document Type: Article

References (69)

1. An, J. H., and T. K. Blackwell, 2003 SKN-1 links C. elegans mesendodermal specification to a conserved oxidative stress response. Genes Dev. 17: 1882–1893.
2. An, J. H., K. Vranas, M. Lucke, H. Inoue, N. Hisamoto et al., 2005 Regulation of the Caenorhabditis elegans oxidative stress defense protein SKN-1 by glycogen synthase kinase-3. Proc. Natl. Acad. Sci. USA 102: 16275–16280.
3. Anderson, M. E., 1998 Glutathione: an overview of biosynthesis and modulation. Chem. Biol. Interact. 111–112: 1–14.
4. Arnér, E. S., and A. Holmgren, 2000 Physiological functions of thioredoxin and thioredoxin reductase. Eur. J. Biochem. 267: 6102–6109.
5. Berndt, C., C. H. Lillig, and A. Holmgren, 2008 Thioredoxins and glutaredoxins as facilitators of protein folding. Biochim. Biophys. Acta 1783: 641–650.
6. Bowerman, B., B. W. Draper, C. C. Mello, and J. R. Priess, 1993 The maternal gene skn-1 encodes a protein that is distributed unequally in early C. elegans embryos. Cell 74: 443–452.
7. Buchanan, B. B., A. Holmgren, J. P. Jacquot, and R. Scheibe, 2012 Fifty years in the thioredoxin field and a bountiful harvest. Biochim. Biophys. Acta 1820: 1822–1829.
8. Cacho-Valadez, B., F. Muñoz-Lobato, J. R. Pedrajas, J. Cabello, J. C. Fierro-González et al., 2012 The characterization of the Caenorhabditis elegans mitochondrial thioredoxin system uncovers an unexpected protective role of thioredoxin reductase 2 in b-amyloid peptide toxicity. Antioxid. Redox Signal. 16: 1384–1400.
9. Carroll, B. T., G. R. Dubyak, M. M. Sedensky, and P. G. Morgan, 2006 Sulfated signal from ASJ sensory neurons modulates stomatin-dependent coordination in Caenorhabditis elegans. J. Biol. Chem. 281: 35989–35996.
10. Chávez, V., A. Mohri-Shiomi, and D. A. Garsin, 2009 Ce-Duox1/ BLI-3 generates reactive oxygen species as a protective innate immune mechanism in Caenorhabditis elegans. Infect. Immun. 77: 4983–4989.
11. Choe, K. P., A. J. Przybysz, and K. Strange, 2009 The WD40 repeat protein WDR-23 functions with the CUL4/DDB1 ubiquitin ligase to regulate nuclear abundance and activity of SKN-1 in Caenorhabditis elegans. Mol. Cell. Biol. 29: 2704–2715.
12. Du, H., S. Kim, Y. S. Hur, M. S. Lee, S. H. Lee et al., 2015 A cytosolic thioredoxin acts as a molecular chaperone for peroxisome matrix proteins as well as antioxidant in peroxisome. Mol. Cells 38: 187–194.
13. Edgar, L. G., and J. D. McGhee, 1986 Embryonic expression of a gut-specific esterase in Caenorhabditis elegans. Dev. Biol. 114: 109–118.
14. Ewald, C. Y., J. N. Landis, J. P. Abate, C. T. Murphy, and T. K. Blackwell, 2014 Dauer-independent insulin/IGF-1-signalling implicates collagen remodelling in longevity. Nature 519: 97–101.
15. Fierro-González, J. C., A. Cornils, J. Alcedo, A. Miranda-Vizuete, and P. Swoboda, 2011a The thioredoxin TRX-1 modulates the function of the insulin-like neuropeptide DAF-28 during dauer formation in Caenorhabditis elegans. PLoS One 6: e16561.
16. Fierro-González, J. C., M. González-Barrios, A. Miranda-Vizuete, and P. Swoboda, 2011b The thioredoxin TRX-1 regulates adult lifespan extension induced by dietary restriction in Caenorhabditis elegans. Biochem. Biophys. Res. Commun. 406: 478–482.
17. Folick, A., H. D. Oakley, Y. Yu, E. H. Armstrong, M. Kumari et al., 2015 Aging. Lysosomal signaling molecules regulate longevity in Caenorhabditis elegans. Science 347: 83–86.
18. Fujino, G., T. Noguchi, K. Takeda, and H. Ichijo, 2006 Thioredoxin and protein kinases in redox signaling. Semin. Cancer Biol. 16: 427–435.
19. Fujino, G., T. Noguchi, A. Matsuzawa, S. Yamauchi, M. Saitoh et al., 2007 Thioredoxin and TRAF family proteins regulate reactive oxygen species-dependent activation of ASK1 through reciprocal modulation of the N-terminal homophilic interaction of ASK1. Mol. Cell. Biol. 27: 8152–8163.
20. Garsin, D. A., C. D. Sifri, E. Mylonakis, X. Qin, K. V. Singh et al., 2001 A simple model host for identifying Gram-positive virulence factors. Proc. Natl. Acad. Sci. USA 98: 10892–10897.
21. Glover-Cutter, K. M., S. Lin, and T. K. Blackwell, 2013 Integration of the unfolded protein and oxidative stress responses through SKN-1/Nrf. PLoS Genet. 9: e1003701.
22. González-Barrios, M., J. C. Fierro-González, E. Krpelanova, J. A. Mora-Lorca, J. R. Pedrajas et al., 2015 Cis- and trans-regulatory mechanisms of gene expression in the ASJ sensory neuron of Caenorhbditis elegans. Genetics 200: 123–134.
23. Grant, B., and D. Hirsh, 1999 Receptor-mediated endocytosis in the Caenorhabditis elegans oocyte. Mol. Biol. Cell 10: 4311–4326.
24. Hoeven, Rv., K. C. McCallum, M. R. Cruz, and D. A. Garsin, 2011 Ce-Duox1/BLI-3 generated reactive oxygen species trigger protective SKN-1 activity via p38 MAPK signaling during infection in C. elegans. PLoS Pathog. 7: e1002453.
25. Holmgren, A., 1985 Thioredoxin. Annu. Rev. Biochem. 54: 237–271.
26. Holmgren, A., and J. Lu, 2010 Thioredoxin and thioredoxin reductase: current research with special reference to human disease. Biochem. Biophys. Res. Commun. 396: 120–124.
27. Hope, I. A., 1999 C. elegans: A Practical Approach. The Practical Approach Series, Oxford University Press, Oxford.
28. Huang da, W., B. T. Sherman, and R. A. Lempicki, 2009a Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 37: 1–13.
29. Huang da, W., B. T. Sherman, and R. A. Lempicki, 2009b Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4: 44–57.
30. Hybertson, B. M., B. Gao, S. K. Bose, and J. M. McCord, 2011 Oxidative stress in health and disease: the therapeutic potential of Nrf2 activation. Mol. Aspects Med. 32: 234–246.
31. Inoue, H., N. Hisamoto, J. H. An, R. P. Oliveira, E. Nishida et al., 2005 The C. elegans p38 MAPK pathway regulates nuclear localization of the transcription factor SKN-1 in oxidative stress response. Genes Dev. 19: 2278–2283.
32. Jee, C., L. Vanoaica, J. Lee, B. J. Park, and J. Ahnn, 2005 Thioredoxin is related to life span regulation and oxidative stress response in Caenorhabditis elegans. Genes Cells 10: 1203–1210.
33. Jiménez-Hidalgo, M., C. L. Kurz, J. R. Pedrajas, F. J. Naranjo-Galindo, M. González-Barrios et al., 2014 Functional characterization of thioredoxin 3 (TRX-3), a Caenorhabditis elegans intestine-specific thioredoxin. Free Radic. Biol. Med. 68: 205–219.
34. Kahn, N. W., S. L. Rea, S. Moyle, A. Kell, and T. E. Johnson, 2008 Proteasomal dysfunction activates the transcription factor SKN-1 and produces a selective oxidative-stress response in Caenorhabditis elegans. Biochem. J. 409: 205–213.
35. Langmead, B., C. Trapnell, M. Pop, and S. L. Salzberg, 2009 Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10: R25.
36. Leung, C. K., K. Hasegawa, Y. Wang, A. Deonarine, L. Tang et al., 2014 Direct interaction between the WD40 repeat protein WDR-23 and SKN-1/Nrf inhibits binding to target DNA. Mol. Cell. Biol. 34: 3156–3167.
37. Liu, Y., and W. Min, 2002 Thioredoxin promotes ASK1 ubiquitination and degradation to inhibit ASK1-mediated apoptosis in a redox activity-independent manner. Circ. Res. 90: 1259–1266.
38. Loria, P. M., J. Hodgkin, and O. Hobert, 2004 A conserved postsynaptic transmembrane protein affecting neuromuscular signaling in Caenorhabditis elegans. J. Neurosci. 24: 2191–2201.
39. Lushchak, V. I., 2011 Adaptive response to oxidative stress: bacteria, fungi, plants and animals. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 153: 175–190.
40. Lynn, D. A., H. M. Dalton, J. N. Sowa, M. C. Wang, A. A. Soukas et al., 2015 Omega-3 and -6 fatty acids allocate somatic and germline lipids to ensure fitness during nutrient and oxidative stress in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 112: 15378–15383.
41. Mahajan-Miklos, S., M. W. Tan, L. G. Rahme, and F. M. Ausubel, 1999 Molecular mechanisms of bacterial virulence elucidated using a Pseudomonas aeruginosa-Caenorhabditis elegans path-ogenesis model. Cell 96: 47–56.
42. Marinho, H. S., C. Real, L. Cyrne, H. Soares, and F. Antunes, 2014 Hydrogen peroxide sensing, signaling and regulation of transcription factors. Redox Biol. 2: 535–562.
43. Maruyama, T., T. Araki, Y. Kawarazaki, I. Naguro, S. Heynen et al., 2014 Roquin-2 promotes ubiquitin-mediated degradation of ASK1 to regulate stress responses. Sci. Signal. 7: ra8.
44. McCord, J. M., and I. Fridovich, 1969 Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein). J. Biol. Chem. 244: 6049–6055.
45. Miranda-Vizuete, A., J. C. Fierro González, G. Gahmon, J. Burghoorn, P. Navas et al., 2006 Lifespan decrease in a Caenorhabditis elegans mutant lacking TRX-1, a thioredoxin expressed in ASJ sensory neurons. FEBS Lett. 580: 484–490.
46. Oliveira, R. P., J. Porter Abate, K. Dilks, J. Landis, J. Ashraf et al., 2009 Condition-adapted stress and longevity gene regulation by Caenorhabditis elegans SKN-1/Nrf. Aging Cell 8: 524–541.
47. Page, A. P., and I. L. Johnstone, 2007 The cuticle. (March 19, 2007), WormBook, ed. The C. elegans Research Community, WormBook, doi/10.1895/wormbook.1.138.1, http://www.wormbook.org.
48. Park, S. K., P. M. Tedesco, and T. E. Johnson, 2009 Oxidative stress and longevity in Caenorhabditis elegans as mediated by SKN-1. Aging Cell 8: 258–269.
49. Powis, G., and W. R. Montfort, 2001 Properties and biological activities of thioredoxins. Annu. Rev. Biophys. Biomol. Struct. 30: 421–455.
50. Prahlad, V., T. Cornelius, and R. I. Morimoto, 2008 Regulation of the cellular heat shock response in Caenorhabditis elegans by thermosensory neurons. Science 320: 811–814.
51. Ray, P. D., B. W. Huang, and Y. Tsuji, 2012 Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cell. Signal. 24: 981–990.
52. Robida-Stubbs, S., K. Glover-Cutter, D. W. Lamming, M. Mizunuma, S. D. Narasimhan et al., 2012 TOR signaling and rapamycin influence longevity by regulating SKN-1/Nrf and DAF-16/FoxO. Cell Metab. 15: 713–724.
53. Salazar, M., A. I. Rojo, D. Velasco, R. M. de Sagarra, and A. Cuadrado, 2006 Glycogen synthase kinase-3beta inhibits the xenobiotic and antioxidant cell response by direct phosphorylation and nuclear exclusion of the transcription factor Nrf2. J. Biol. Chem. 281: 14841–14851.
54. Schackwitz, W. S., T. Inoue, and J. H. Thomas, 1996 Chemosensory neurons function in parallel to mediate a pheromone response in C. elegans. Neuron 17: 719–728.
55. Schmeisser, S., S. Priebe, M. Groth, S. Monajembashi, P. Hemmerich et al., 2013 Neuronal ROS signaling rather than AMPK/sirtuin-mediated energy sensing links dietary restriction to lifespan extension. Mol. Metab. 2: 92–102.
56. Steinbaugh, M. J., S. D. Narasimhan, S. Robida-Stubbs, L. E. Moronetti Mazzeo, J. M. Dreyfuss et al., 2015 Lipid-mediated regulation of SKN-1/Nrf in response to germ cell absence. eLife 4: 4.
57. Sun, J., V. Singh, R. Kajino-Sakamoto, and A. Aballay, 2011 Neuronal GPCR controls innate immunity by regulating noncanonical unfolded protein response genes. Science 332: 729–732.
58. Taylor, R. C., and A. Dillin, 2013 XBP-1 is a cell-nonautonomous regulator of stress resistance and longevity. Cell 153: 1435–1447.
59. Thanan, R., S. Oikawa, Y. Hiraku, S. Ohnishi, N. Ma et al., 2014 Oxidative stress and its significant roles in neurodegenerative diseases and cancer. Int. J. Mol. Sci. 16: 193–217.
60. Tobiume, K., M. Saitoh, and H. Ichijo, 2002 Activation of apoptosis signal-regulating kinase 1 by the stress-induced activating phosphorylation of pre-formed oligomer. J. Cell. Physiol. 191: 95–104.
61. Trapnell, C., A. Roberts, L. Goff, G. Pertea, D. Kim et al., 2012 Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protoc. 7: 562–578.
62. Trapnell, C., D. G. Hendrickson, M. Sauvageau, L. Goff, J. L. Rinn et al., 2013 Differential analysis of gene regulation at transcript resolution with RNA-seq. Nat. Biotechnol. 31: 46–53.
63. Tullet, J. M., M. Hertweck, J. H. An, J. Baker, J. Y. Hwang et al., 2008 Direct inhibition of the longevity-promoting factor SKN-1 by insulin-like signaling in C. elegans. Cell 132: 1025–1038.
64. van Oosten-Hawle, P., and R. I. Morimoto, 2014a Organismal proteostasis: role of cell-nonautonomous regulation and transcellular chaperone signaling. Genes Dev. 28: 1533–1543.
65. van Oosten-Hawle, P., and R. I. Morimoto, 2014b Transcellular chaperone signaling: an organismal strategy for integrated cell stress responses. J. Exp. Biol. 217: 129–136.
66. Walker, A. K., R. See, C. Batchelder, T. Kophengnavong, J. T. Gronniger et al., 2000 A conserved transcription motif suggesting functional parallels between Caenorhabditis elegans SKN-1 and Cap’n’Collar-related basic leucine zipper proteins. J. Biol. Chem. 275: 22166–22171.
67. Wang, T. S., C. F. Kuo, K. Y. Jan, and H. Huang, 1996 Arsenite induces apoptosis in Chinese hamster ovary cells by generation of reactive oxygen species. J. Cell. Physiol. 169: 256–268.
68. Yoshioka, J., E. R. Schreiter, and R. T. Lee, 2006 Role of thioredoxin in cell growth through interactions with signaling molecules. Antioxid. Redox Signal. 8: 2143–2151.
69. Zhang, P., M. Judy, S. J. Lee, and C. Kenyon, 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.