Functional characterization of thioredoxin 3 (TRX-3), a Caenorhabditis elegans intestine-specific thioredoxin

Free Radical Biology and Medicine

Volumn 68, Issue , 2014, Pages 205-219

  Jiménez Hidalgo, María ^a   Cyril Léopold, Kurz ^b,i   José Rafael, Pedrajas ^c   Francisco José, Naranjo Galindo ^a   González Barrios, María ^a   Cabello, Juan ^d   Sáez, Alberto G ^e   Lozano, Encarnación ^e   Button, Emma L ^f   Veal, Elizabeth A ^f   Fierro González, Juan Carlos ^g   Swoboda, Peter ^g   Miranda Vizuete, Antonio ^a,h  

^a UNIVERSIDAD PABLO DE OLAVIDE   (Spain)

^b CENTRE D IMMUNOLOGIE DE MARSEILLE LUMINY   (France)

^c UNIVERSITY OF JAÉN   (Spain)

^d CENTER FOR BIOMEDICAL RESEARCH OF LA RIOJA CIBIR   (Spain)

^e Unidad Funcional de Investigación en Enfermedades Crónicas   (Spain)

^f NEWCASTLE UNIVERSITY   (United Kingdom)

^g KAROLINSKA INSTITUTE   (Sweden)

^h HOSPITAL UNIVERSITARIO VIRGEN DEL ROCÍO   (Spain)

ⁱ AIX MARSEILLE UNIVERSITÉ   (France)

Author keywords

Caenorhabditis elegans; Candida albicans; Intestine; Pathogen infection; Photorhabdus luminescens; Stress; Thioredoxin

Indexed keywords

GREEN FLUORESCENT PROTEIN; THIOREDOXIN; THIOREDOXIN 3; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; APICAL MEMBRANE; ARTICLE; BACTERIAL INFECTION; CAENORHABDITIS ELEGANS; CANDIDA ALBICANS; CONTROLLED STUDY; CYTOPLASM; DEFECATION; ENZYME ACTIVITY; GENE OVEREXPRESSION; INTESTINE CELL; INTESTINE FUNCTION; LONGEVITY; LOSS OF FUNCTION MUTATION; MYCOSIS; NONHUMAN; OXIDATION REDUCTION REACTION; PHOTORHABDUS LUMINESCENS; PRIORITY JOURNAL; REDUCTION; STOMACH PROTECTION; STRESS; WILD TYPE;

CAENORHABDITIS ELEGANS; CANDIDA ALBICANS; INTESTINE; PATHOGEN INFECTION; PHOTORHABDUS LUMINESCENS; STRESS; THIOREDOXIN;

AMINO ACID SEQUENCE; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; INTESTINES; LONGEVITY; ORGAN SPECIFICITY; OXIDATION-REDUCTION; THIOREDOXINS;

EID: 84892157593     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2013.11.023     Document Type: Article

References (56)

1. C.H. Lillig, and A. Holmgren Thioredoxin and related molecules - from biology to health and disease Antioxid. Redox Signaling 9 2007 25 47 (Pubitemid 44901873)
2. A. Holmgren, and J. Lu Thioredoxin and thioredoxin reductase: current research with special reference to human disease Biochem. Biophys. Res. Commun. 396 2010 120 124
3. A. Miranda-Vizuete, J.C. Fierro Gonzalez, G. Gahmon, J. Burghoorn, P. Navas, and P. Swoboda Lifespan decrease in a Caenorhabditis elegans mutant lacking TRX-1, a thioredoxin expressed in ASJ sensory neurons FEBS Lett. 580 2006 484 490 (Pubitemid 43089676)
4. J.C. Fierro-Gonzalez, A. Cornils, J. Alcedo, A. Miranda-Vizuete, and P. Swoboda The thioredoxin TRX-1 modulates the function of the insulin-like neuropeptide DAF-28 during dauer formation in Caenorhabditis elegans PLoS One 6 2011 e16561
5. J.C. Fierro-Gonzalez, M. Gonzalez-Barrios, A. Miranda-Vizuete, and P. Swoboda The thioredoxin TRX-1 regulates adult lifespan extension induced by dietary restriction in Caenorhabditis elegans Biochem. Biophys. Res. Commun. 406 2011 478 482
6. B. Cacho-Valadez, F. Munoz-Lobato, J.R. Pedrajas, J. Cabello, J.C. Fierro-Gonzalez, P. Navas, P. Swoboda, C.D. Link, and A. Miranda-Vizuete The characterization of the Caenorhabditis elegans mitochondrial thioredoxin system uncovers an unexpected protective role of TRXR-2 in beta-amyloid peptide toxicity Antioxid. Redox Signaling 16 2012 1384 1400
7. A. Schlotterer, A. Hamann, G. Kukudov, Y. Ibrahim, B. Heckmann, F. Bozorgmehr, M. Pfeiffer, H. Hutter, D. Stern, X. Du, M. Brownlee, A. Bierhaus, P. Nawroth, and M. Morcos Apurinic/apyrimidinic endonuclease 1, p53, and thioredoxin are linked in control of aging in C. elegans Aging Cell 9 2010 420 432
8. T. Suzuki, K. Tanabe, I. Hara, N. Taniguchi, and A. Colavita Dual enzymatic properties of the cytoplasmic peptide: N-glycanase in C. elegans Biochem. Biophys. Res. Commun. 358 2007 837 841 (Pubitemid 46802465)
9. N. Habibi-Babadi, A. Su, C.E. de Carvalho, and A. Colavita The N-glycanase png-1 acts to limit axon branching during organ formation in Caenorhabditis elegans J. Neurosci 30 2010 1766 1776
10. F. Munoz-Lobato, M.J. Rodriguez-Palero, F.J. Naranjo-Galindo, F. Shepard, C.J. Gaffney, N.J. Szewczyk, S. Hamamichi, K.A. Caldwell, G.A. Caldwell, C.D. Link, and A. Miranda-Vizuete Protective role of DNJ-27/ERdj5 in Caenorhabditis elegans models of human neurodegenerative diseases Antioxid. Redox Signaling 20 2014 217 235
11. McGhee, J. D. The C. elegans intestine. The C. elegans Research Community, WormBook, 27 March 2007; doi/10.1895/wormbook.1.133.1; 〈http://www.wormbook.org〉.
12. N. Libina, J.R. Berman, and C. Kenyon Tissue-specific activities of C. elegans DAF-16 in the regulation of lifespan Cell 115 2003 489 502 (Pubitemid 37456810)
13. B. Spanier, I. Rubio-Aliaga, H. Hu, and H. Daniel Altered signalling from germline to intestine pushes daf-2;pept-1 Caenorhabditis elegans into extreme longevity Aging Cell 9 2010 636 646
14. Darby, C. Interactions with microbial pathogens. The C. elegans Research Community, WormBook, 6 September 2005; doi/10.1895/wormbook.1.21.1; 〈http://www.wormbook.org〉.
15. J Sulston, and H.J. Methods. The Nematode Caenorhabditis elegans 1998 Cold Spring Harbor Laboratory Press Cold Spring Harbor, NY
16. A. Holmgren, and M. Bjornstedt Thioredoxin and thioredoxin reductase Methods Enzymol. 252 1995 199 208
17. C. Nieto, J. Almendinger, S. Gysi, E. Gomez-Orte, A. Kaech, M.O. Hengartner, R. Schnabel, S. Moreno, and J. Cabello ccz-1 mediates the digestion of apoptotic corpses in C. elegans J. Cell Sci. 123 2010 2001 2007
18. R. Schnabel, H. Hutter, D. Moerman, and H. Schnabel Assessing normal embryogenesis in Caenorhabditis elegans using a 4D microscope: variability of development and regional specification Dev. Biol. 184 1997 234 265 (Pubitemid 27224348)
19. B. Grant, Y. Zhang, M.C. Paupard, S.X. Lin, D.H. Hall, and D. Hirsh Evidence that RME-1, a conserved C. elegans EH-domain protein, functions in endocytic recycling Nat. Cell Biol. 3 2001 573 579 (Pubitemid 32536854)
20. E.J. O'Rourke, A.A. Soukas, C.E. Carr, and G.C. Ruvkun elegans major fats are stored in vesicles distinct from lysosome-related organelles Cell Metab. 10 2009 430 435
21. K. Hasegawa, S. Miwa, K. Isomura, K. Tsutsumiuchi, H. Taniguchi, and J. Miwa Acrylamide-responsive genes in the nematode Caenorhabditis elegans Toxicol. Sci. 101 2008 215 225
22. P.L. Larsen, P.S. Albert, and D.L. Riddle Genes that regulate both development and longevity in Caenorhabditis elegans Genetics 139 1995 1567 1583
23. V.L. Jensen, K.T. Simonsen, Y.H. Lee, D. Park, and D.L. Riddle RNAi screen of DAF-16/FOXO target genes in C. elegans links pathogenesis and dauer formation PLoS One 5 2010 e15902
24. J.R. Powell, and F.M. Ausubel Models of Caenorhabditis elegans infection by bacterial and fungal pathogens J.J. Ewbank, E. Vivier, Methods in Molecular Biology, Vol. 415, Innate Immunity 2008 Springer Totowa, NJ 403 427
25. I. Engelmann, A. Griffon, L. Tichit, F. Montanana-Sanchis, G. Wang, V. Reinke, R.H. Waterston, L.W. Hillier, and J.J. Ewbank A comprehensive analysis of gene expression changes provoked by bacterial and fungal infection in C. elegans PLoS One 6 2011 e19055
26. Y. Suzuki, M.D. Yandell, P.J. Roy, S. Krishna, C. Savage-Dunn, R.M. Ross, R.W. Padgett, and W.B. Wood A BMP homolog acts as a dose-dependent regulator of body size and male tail patterning in Caenorhabditis elegans Development 126 1999 241 250 (Pubitemid 29083962)
27. G.V. Mallo, C.L. Kurz, C. Couillault, N. Pujol, S. Granjeaud, Y. Kohara, and J.J. Ewbank Inducible antibacterial defense system in C. elegans Curr. Biol. 12 2002 1209 1214 (Pubitemid 34801168)
28. E. Allman, D. Johnson, and K. Nehrke Loss of the apical V-ATPase a-subunit VHA-6 prevents acidification of the intestinal lumen during a rhythmic behavior in C. elegans Am. J. Physiol. Cell Physiol 297 2009 C1071 1081
29. S. Parker, D.S. Walker, S. Ly, and H.A. Baylis Caveolin-2 is required for apical lipid trafficking and suppresses basolateral recycling defects in the intestine of Caenorhabditis elegans Mol. Biol. Cell 20 2009 1763 1771
30. D. Volonte, and F. Galbiati Inhibition of thioredoxin reductase 1 by caveolin 1 promotes stress-induced premature senescence EMBO Rep 10 2009 1334 1340
31. A. Holmgren Antioxidant function of thioredoxin and glutaredoxin systems Antioxid. Redox Signaling 2 2000 811 820 (Pubitemid 32062330)
32. C.T. Murphy The search for DAF-16/FOXO transcriptional targets: approaches and discoveries Exp. Gerontol. 41 2006 910 921 (Pubitemid 44821691)
33. K. Hartwig, T. Heidler, J. Moch, H. Daniel, and U. Wenzel Feeding a ROS-generator to Caenorhabditis elegans leads to increased expression of small heat shock protein HSP-16.2 and hormesis Genes Nutr 4 2009 59 67
34. K.J. Helmcke, and M. Aschner Hormetic effect of methylmercury on Caenorhabditis elegans Toxicol. Appl. Pharmacol. 248 2010 156 164
35. M. Olahova, S.R. Taylor, S. Khazaipoul, J. Wang, B.A. Morgan, K. Matsumoto, T.K. Blackwell, and E.A. Veal A redox-sensitive peroxiredoxin that is important for longevity has tissue- and stress-specific roles in stress resistance Proc. Natl. Acad. Sci. USA 105 2008 19839 19844
36. D. Knoefler, M. Thamsen, M. Koniczek, N.J. Niemuth, A.K. Diederich, and U. Jakob Quantitative in vivo redox sensors uncover oxidative stress as an early event in life Mol. Cell 47 2012 767 776
37. P. Back, W.H. De Vos, G.G. Depuydt, F. Matthijssens, J.R. Vanfleteren, and B.P. Braeckman Exploring real-time in vivo redox biology of developing and aging Caenorhabditis elegans Free Radic. Biol. Med. 52 2012 850 859
38. B. Lakowski, and S. Hekimi The genetics of caloric restriction in Caenorhabditis elegans Proc. Natl. Acad. Sci. USA 95 1998 13091 13096 (Pubitemid 28509529)
39. + exchanger NHX-2 increases life span J. Biol. Chem 278 2003 44657 44666 (Pubitemid 37377222)
40. E.A. Evans, W.C. Chen, and M.W. Tan The DAF-2 insulin-like signaling pathway independently regulates aging and immunity in C. elegans Aging Cell 7 2008 879 893 (Pubitemid 352749441)
41. K.D. Kimura, H.A. Tissenbaum, Y. Liu, and G. Ruvkun daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans Science 277 1997 942 946 (Pubitemid 27366677)
42. R. Pukkila-Worley, F.M. Ausubel, and E. Mylonakis Candida albicans infection of Caenorhabditis elegans induces antifungal immune defenses PLoS Pathog. 7 2011 e1002074
43. C. Boehnisch, D. Wong, M. Habig, K. Isermann, N.K. Michiels, T. Roeder, R.C. May, and H. Schulenburg Protist-type lysozymes of the nematode Caenorhabditis elegans contribute to resistance against pathogenic Bacillus thuringiensis PLoS One 6 2011 e24619
44. A. Miranda-Vizuete, C.M. Sadek, A. Jimenez, W.J. Krause, P. Sutovsky, and R. Oko The mammalian testis-specific thioredoxin system Antioxid. Redox Signaling 6 2004 25 40 (Pubitemid 38067243)
45. M.J. Svensson, P. Stenberg, and J. Larsson Organization and regulation of sex-specific thioredoxin encoding genes in the genus Drosophila Dev. Genes Evol. 217 2007 639 650 (Pubitemid 47377597)
46. E.R. Troemel, S.W. Chu, V. Reinke, S.S. Lee, F.M. Ausubel, and D.H. Kim p38 MAPK regulates expression of immune response genes and contributes to longevity in C. elegans PLoS Genet. 2 2006 e183
47. J.E. Irazoqui, E.R. Troemel, R.L. Feinbaum, L.G. Luhachack, B.O. Cezairliyan, and F.M. Ausubel Distinct pathogenesis and host responses during infection of C. elegans by P. aeruginosa and S. aureus PLoS Pathog. 6 2010 e1000982
48. S. Akira, S. Uematsu, and O. Takeuchi Pathogen recognition and innate immunity Cell 124 2006 783 801 (Pubitemid 43261452)
49. A.D. Johnston, and P.R. Ebert The redox system in C. elegans, a phylogenetic approach J. Toxicol 2012 2012 546915
50. V. Chavez, A. Mohri-Shiomi, and D.A. Garsin Ce-Duox1/BLI-3 generates reactive oxygen species as a protective innate immune mechanism in Caenorhabditis elegans Infect. Immun 77 2009 4983 4989
51. X. Sem, and M. Rhen Pathogenicity of Salmonella enterica in Caenorhabditis elegans relies on disseminated oxidative stress in the infected host PLoS One 7 2012 e45417
52. R. Hoeven, K.C. McCallum, M.R. Cruz, and D.A. Garsin 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 2011 e1002453
53. D. Papp, P. Csermely, and C. Soti A role for SKN-1/Nrf in pathogen resistance and immunosenescence in Caenorhabditis elegans PLoS Pathog 8 2012 e1002673
54. H. Schulenburg, M.P. Hoeppner, and J. Weiner 3rd; Bornberg-Bauer, E. Specificity of the innate immune system and diversity of C-type lectin domain (CTLD) proteins in the nematode Caenorhabditis elegans Immunobiology 213 2008 237 250
55. D. Wong, D. Bazopoulou, N. Pujol, N. Tavernarakis, and J.J. Ewbank Genome-wide investigation reveals pathogen-specific and shared signatures in the response of Caenorhabditis elegans to infection Genome Biol. 8 2007 R194
56. T.J. Fabian, and T.E. Johnson Production of age-synchronous mass cultures of Caenorhabditis elegans J. Gerontol. 49 1994 B145 156