The sirtuin SIRT6 regulates stress granule formation in C. elegans and mammals

Journal of Cell Science

Volumn 126, Issue 22, 2013, Pages 5166-5177

  Jedrusik Bode, Monika ^a   Studencka, Maja ^a   Smolka, Christian ^b   Baumann, Tobias ^c   Schmidt, Henning ^d   Kampf, Jan ^a   Paap, Franziska ^a   Martin, Sophie ^e   Tazi, Jamal ^e   Mü ller, Kristian M ^f   Krü ger, Marcus ^b   Braun, Thomas ^b   Bober, Eva ^b  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^b MAX PLANCK INSTITUTE FOR HEART AND LUNG RESEARCH   (Germany)

^c UNIVERSITY OF POTSDAM   (Germany)

^d TECHNICAL UNIVERSITY OF BRAUNSCHWEIG   (Germany)

^e INSTITUT DE GÉNÉTIQUE MOLÉCULAIRE DE MONTPELLIER   (France)

^f BIELEFELD UNIVERSITY   (Germany)

Author keywords

C. elegans; G3BP; SIRT6; Sirtuins; Stress; Stress granules

Indexed keywords

SIRTUIN; SIRTUIN 2.4; SIRTUIN 6; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CAENORHABDITIS ELEGANS; CATALYSIS; CELL PROLIFERATION; CELL STRESS; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; CYTOPLASM; ENZYME INHIBITION; FIBROBLAST; GENETIC CONSERVATION; GRANULE CELL; HEAT STRESS; HUMAN; HUMAN CELL; MAMMAL; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; STRESS GRANULE;

C. ELEGANS; G3BP; SIRT6; SIRTUINS; STRESS; STRESS GRANULES;

ANIMALS; CAENORHABDITIS ELEGANS; CELL NUCLEUS; CHROMATIN; CYTOPLASMIC GRANULES; GENE EXPRESSION REGULATION; GENOMIC INSTABILITY; MAMMALS; MICE; SIRTUINS; STRESS, PHYSIOLOGICAL;

EID: 84888177631     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.130708     Document Type: Article

References (50)

1. Allen, D. L. and Pielak, G. J. (1998). Baseline length and automated fitting of denaturation data. Protein Sci. 7, 1262-1263.
2. Anderson, P. and Kedersha, N. (2006). RNA granules. J. Cell Biol. 172, 803-808.
3. Anderson, P. and Kedersha, N. (2009). Stress granules. Curr. Biol. 19, R397-R398.
4. Buchan, J. R. and Parker, R. (2009). Eukaryotic stress granules: the ins and outs of translation. Mol. Cell 36, 932-941.
5. Chiang, W.-C., Tishkoff, D. X., Yang, B., Wilson-Grady, J., Yu, X., Mazer, T., Eckersdorff, M., Gygi, S. P., Lombard, D. B. and Hsu, A.-L. (2012). C. elegans SIRT6/7 homolog SIR-2.4 promotes DAF-16 relocalization and function during stress. PLoS Genet. 8, e1002948.
6. Choudhary, C., Kumar, C., Gnad, F., Nielsen, M. L., Rehman, M., Walther, T. C., Olsen, J. V. and Mann, M. (2009). Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 325, 834-840.
7. Cox, J. and Mann, M. (2008). MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26, 1367-1372.
8. Dignam, J. D., Lebovitz, R. M. and Roeder, R. G. (1983). Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11, 1475-1489.
9. Dolzhanskaya, N., Xie, W., Merz, G. and Denman, R. B. (2011). EGFP-FMRP forms proto-stress granules: A poor surrogate for endogenous FMRP. J. Biophys. Struct. Biol. 3, 1-23.
10. Drexler, H. C., Ruhs, A., Konzer, A., Mendler, L., Bruckskotten, M., Looso, M., Günther, S., Boettger, T., Krüger, M. and Braun, T. (2012). On marathons and Sprints: an integrated quantitative proteomics and transcriptomics analysis of differences between slow and fast muscle fibers. Mol. Cell. Proteomics 11, M111.010801.
11. Gallouzi, I. E. (2009). Could stress granules be involved in age-related diseases?. Aging 1, 753-757.
12. Gallouzi, I. E., Parker, F., Chebli, K., Maurier, F., Labourier, E., Barlat, I., Capony, J. P., Tocque, B. and Tazi, J. (1998). A novel phosphorylation-dependent RNase activity of GAP-SH3 binding protein: a potential link between signal transduction and RNA stability. Mol. Cell. Biol. 18, 3956-3965.
13. Ganesh, C., Shah, A. N., Swaminathan, C. P., Surolia, A. and Varadarajan, R. (1997). Thermodynamic characterization of the reversible, two-state unfolding of maltose binding protein, a large two-domain protein. Biochemistry 36, 5020-5028.
14. Ghosh, H. S., Reizis, B. and Robbins, P. D. (2011). SIRT1 associates with eIF2-alpha and regulates the cellular stress response. Sci. Rep. 1, 150.
15. Haigis, M. C. and Guarente, L. P. (2006). Mammalian sirtuins-emerging roles in physiology, aging, and calorie restriction. Genes Dev. 20, 2913-2921.
16. Irvine, K., Stirling, R., Hume, D. and Kennedy, D. (2004). Rasputin, more promiscuous than ever: a review of G3BP. Int. J. Dev. Biol. 48, 1065-1077.
17. Jedrusik, M. A. and Schulze, E. (2003). Telomeric position effect variegation in Saccharomyces cerevisiae by Caenorhabditis elegans linker histones suggests a mechanistic connection between germ line and telomeric silencing. Mol. Cell. Biol. 23, 3681-3691.
18. Jedrusik, M. A. and Schulze, E. (2007). Linker histone HIS-24 (H1.1) cytoplasmic retention promotes germ line development and influences histone H3 methylation in Caenorhabditis elegans. Mol. Cell. Biol. 27, 2229-2239.
19. Jiang, H., Khan, S., Wang, Y., Charron, G., He, B., Sebastian, C., Du, J., Kim, R., Ge, E., Mostoslavsky, R. et al. (2013). SIRT6 regulates TNF-a secretion through hydrolysis of long-chain fatty acyl lysine. Nature 496, 110-113.
20. Jud, M. C., Czerwinski, M. J., Wood, M. P., Young, R. A., Gallo, C. M., Bickel, J. S., Petty, E. L., Mason, J. M., Little, B. A., Padilla, P. A. et al. (2008). Large P bodylike RNPs form in C elegans oocytes in response to arrested ovulation, heat shock, osmotic stress, and anoxia and are regulated by the major sperm protein pathway. Dev. Biol. 318, 38-51.
21. Kaidi, A., Weinert, B. T., Choudhary, C. and Jackson, S. P. (2010). Human SIRT6 promotes DNA end resection through CtIP deacetylation. Science 329, 1348-1353.
22. Kanfi, Y., Naiman, S., Amir, G., Peshti, V., Zinman, G., Nahum, L., Bar-Joseph, Z. and Cohen, H. Y. (2012). The sirtuin SIRT6 regulates lifespan in male mice. Nature 483, 218-221.
23. Kawaguchi, Y., Kovacs, J. J., McLaurin, A., Vance, J. M., Ito, A. and Yao, T. P. (2003). The deacetylase HDAC6 regulates aggresome formation and cell viability in response to misfolded protein stress. Cell 115, 727-738.
24. Kawahara, T. L., Michishita, E., Adler, A. S., Damian, M., Berber, E., Lin, M., McCord, R. A., Ongaigui, K. C., Boxer, L. D., Chang, H. Y. et al. (2009). SIRT6 links histone H3 lysine 9 deacetylation to NF-kappaB-dependent gene expression and organismal life span. Cell 136, 62-74.
25. Kedersha, N., Cho, M. R., Li, W., Yacono, P. W., Chen, S., Gilks, N., Golan, D. E. and Anderson, P. (2000). Dynamic shuttling of TIA-1 accompanies the recruitment of mRNA to mammalian stress granules. J. Cell Biol. 151, 1257-1268.
26. Kourtis, N. and Tavernarakis, N. (2011). Cellular stress response pathways and ageing: intricate molecular relationships. EMBO J. 30, 2520-2531.
27. Kwon, S. H., Zhang, Y. andMatthias, P. (2007). The deacetylase HDAC6 is a novel critical component of stress granules involved in the stress response. Genes Dev. 21, 3381-3394.
28. Lavinder, J. J., Hari, S. B., Sullivan, B. J. and Magliery, T. J. (2009). Highthroughput thermal scanning: a general, rapid dye-binding thermal shift screen for protein engineering. J. Am. Chem. Soc. 131, 3794-3795.
29. Lavut, A. and Raveh, D. (2012). Sequestration of highly expressed mRNAs in cytoplasmic granules, P-bodies, and stress granules enhances cell viability. PLoS Genet. 8, e1002527.
30. Mao, Z., Hine, C., Tian, X., Van Meter, M., Au, M., Vaidya, A., Seluanov, A. and Gorbunova, V. (2011). SIRT6 promotes DNA repair under stress by activating PARP1. Science 332, 1443-1446.
31. McCord, R. A., Michishita, E., Hong, T., Berber, E., Boxer, L. D., Kusumoto, R., Guan, S., Shi, X., Gozani, O., Burlingame, A. L. et al. (2009). SIRT6 stabilizes DNA-dependent protein kinase at chromatin for DNA double-strand break repair. Aging 1, 109-121.
32. Mello, C. C., Kramer, J. M., Stinchcomb, D. and Ambros, V. (1991). Efficient gene transfer in C.elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J. 10, 3959-3970.
33. Michishita, E., McCord, R. A., Berber, E., Kioi, M., Padilla-Nash, H., Damian, M., Cheung, P., Kusumoto, R., Kawahara, T. L., Barrett, J. C. et al. (2008). SIRT6 is a histone H3 lysine 9 deacetylase that modulates telomeric chromatin. Nature 452, 492-496.
34. Michishita, E., McCord, R. A., Boxer, L. D., Barber, M. F., Hong, T., Gozani, O. and Chua, K. F. (2009). Cell cycle-dependent deacetylation of telomeric histone H3 lysine K56 by human SIRT6. Cell Cycle 8, 2664-2666.
35. Mostoslavsky, R., Chua, K. F., Lombard, D. B., Pang, W. W., Fischer, M. R., Gellon, L., Liu, P., Mostoslavsky, G., Franco, S., Murphy, M. M. et al. (2006). Genomic instability and aging-like phenotype in the absence of mammalian SIRT6. Cell 124, 315-329.
36. Ohn, T. and Anderson, P. (2010). The role of posttranslational modifications in the assembly of stress granules. WIREs RNA 1, 486-493.
37. Parker, F., Maurier, F., Delumeau, I., Duchesne, M., Faucher, D., Debussche, L., Dugue, A., Schweighoffer, F. and Tocque, B. (1996). A Ras-GTPase-activating protein SH3-domain-binding protein. Mol. Cell. Biol. 16, 2561-2569.
38. Phillips, K. and de la Peña, A. H. (2011). The combined use of the Thermofluor assay and ThermoQ analytical software for the determination of protein stability and buffer optimization as an aid in protein crystallization. Curr. Protoc. Mol. Biol. 10, 1-15.
39. Pitt, J. N., Schisa, J. A. and Priess, J. R. (2000). P granules in the germ cells of Caenorhabditis elegans adults are associated with clusters of nuclear pores and contain RNA. Dev. Biol. 219, 315-333.
40. Rappsilber, J., Mann, M. and Ishihama, Y. (2007). Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips. Nat. Protoc. 2, 1896-1906.
41. Rogina, B. and Helfand, S. L. (2004). Sir2 mediates longevity in the fly through a pathway related to calorie restriction. Proc. Natl. Acad. Sci. USA 101, 15998-16003.
42. Sanchez-Ruiz, J. M. (2010). Protein kinetic stability. Biophys. Chem. 148, 1-15.
43. Shevchenko, A., Tomas, H., Havlis, J., Olsen, J. V. and Mann, M. (2006). In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat. Protoc. 1, 2856-2860.
44. Sijen, T., Fleenor, J., Simmer, F., Thijssen, K. L., Parrish, S., Timmons, L., Plasterk, R. H. and Fire, A. (2001). On the role of RNA amplification in dsRNAtriggered gene silencing. Cell 107, 465-476.
45. Tennen, R. I., Berber, E. and Chua, K. F. (2010). Functional dissection of SIRT6: identification of domains that regulate histone deacetylase activity and chromatin localization. Mech. Ageing Dev. 131, 185-192.
46. Tissenbaum, H. A. and Guarente, L. (2001). Increased dosage of a sir-2 gene extends lifespan in Caenorhabditis elegans. Nature 410, 227-230.
47. Tourrière, H., Gallouzi, I. E., Chebli, K., Capony, J. P., Mouaikel, J., van der Geer, P. and Tazi, J. (2001). RasGAP-associated endoribonuclease G3Bp: selective RNA degradation and phosphorylation-dependent localization. Mol. Cell. Biol. 21, 7747-7760.
48. Tourrière, H., Chebli, K., Zekri, L., Courselaud, B., Blanchard, J. M., Bertrand, E. and Tazi, J. (2003). The RasGAP-associated endoribonuclease G3BP assembles stress granules. J. Cell Biol. 160, 823-831.
49. Uniewicz,K. A.,Ori,A., Xu, R.,Ahmed,Y.,Wilkinson,M. C.,Fernig, D. G. andYates, E.A. (2010). Differential scanning fluorimetry measurement of protein stability changes upon binding to glycosaminoglycans: a screening test for binding specificity. Anal. Chem. 82, 3796-3802.
50. Werner, E. D., Brodsky, J. L. and McCracken, A. A. (1996). Proteasome-dependent endoplasmic reticulum-associated protein degradation: an unconventional route to a familiar fate. Proc. Natl. Acad. Sci. USA 93, 13797-13801.