Stress granules form in Brachionus manjavacas (Rotifera) in response to a variety of stressors

Comparative Biochemistry and Physiology - A Molecular and Integrative Physiology

Volumn 166, Issue 2, 2013, Pages 375-384

  Jones, Brande L ^a   VanLoozen, Josephine ^a   Kim, Min H ^a   Miles, Stacey J ^b   Dunham, Christine M ^b   Williams, Loren Dean ^a   Snell, Terry W ^a  

^a GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

EIF3B; EIF4E; RNA granules; SGs; TIA 1

Indexed keywords

INITIATION FACTOR; INITIATION FACTOR 2ALPHA; INITIATION FACTOR 3; INITIATION FACTOR 3B; INITIATION FACTOR 4A; INITIATION FACTOR 4B; INITIATION FACTOR 4E; INITIATION FACTOR 4G; T LYMPHOCYTE RESTRICTED INTRACELLULAR ANTIGEN 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ANTIGEN BINDING; ARTICLE; BRACHIONUS MANJAVACAS; CELL ORGANELLE; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENVIRONMENTAL STRESS; EPITOPE MAPPING; EUKARYOTIC CELL; HEAT STRESS; IMMUNOHISTOCHEMISTRY; LARGE RIBOSOMAL SUBUNIT; NEWBORN; NONHUMAN; OSMOTIC STRESS; PROTEIN AGGREGATION; PROTEIN LOCALIZATION; ROTIFERA; SMALL RIBOSOMAL SUBUNIT; STARVATION; STRESS GRANULE; SURVIVAL;

ANIMALIA; BRACHIONUS; EUKARYOTA; HEXAPODA; LOPHOTROCHOZOA; MAMMALIA; ROTIFERA; TRYPANOSOMATIDAE;

EIF3B; EIF4E; RNA GRANULES; SGS; TIA-1;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; CYCLOHEXIMIDE; CYTOPLASMIC GRANULES; EUKARYOTIC INITIATION FACTOR-3; EUKARYOTIC INITIATION FACTOR-4E; HELMINTH PROTEINS; POLY(A)-BINDING PROTEINS; PROTEIN SYNTHESIS INHIBITORS; PROTEIN TRANSPORT; PUROMYCIN; RIBOSOME SUBUNITS, LARGE; ROTIFERA; STRESS, PHYSIOLOGICAL;

EID: 84881510880     PISSN: 10956433     EISSN: 15314332     Source Type: Journal    
DOI: 10.1016/j.cbpa.2013.07.009     Document Type: Article

References (69)

1. Anderson P., Kedersha N. Stressful initiations. J. Cell Sci. 2002, 115:3227-3234.
2. Anderson P., Kedersha N. Visibly stressed: the role of eIF2, TIA-1, and stress granules in protein translation. Cell Stress Chaperones 2002, 7:213-221.
3. Anderson P., Kedersha N. RNA granules. J. Cell Biol. 2006, 172:803-808.
4. Anderson P., Kedersha N. Stress granules: the Tao of RNA triage. Trends Biochem. Sci. 2008, 33:141-150.
5. Anderson P., Kedersha N. RNA granules: post-transcriptional and epigenetic modulators of gene expression. Nat. Rev. Mol. Cell Biol. 2009, 10:430-436.
6. Anderson P., Kedersha N. Stress granules. Curr. Biol. 2009, 19:R397-R398.
7. Bashkirov V.I., Scherthan H., Solinger J.A., Buerstedde J.M., Heyer W.D. A mouse cytoplasmic exoribonuclease (mXRN1p) with preference for G4 tetraplex substrates. J. Cell Biol. 1997, 136:761-773.
8. Boschetti C., Pouchkina-Stantcheva N., Hoffmann P., Tunnacliffe A. Foreign genes and novel hydrophilic protein genes participate in the desiccation response of the bdelloid rotifer Adineta ricciae. J. Exp. Biol. 2011, 214:59-68.
9. Brengues M., Teixeira D., Parker R. Movement of eukaryotic mRNAs between polysomes and cytoplasmic processing bodies. Science 2005, 310:486-489.
10. Buchan J.R., Parker R. Eukaryotic stress granules: the ins and outs of translation. Mol. Cell 2009, 36:932-941.
11. Buchan J.R., Yoon J.H., Parker R. Stress-specific composition, assembly and kinetics of stress granules in Saccharomyces cerevisiae. J. Cell Sci. 2011, 124:228-239.
12. Cassola A. RNA granules living a post-transcriptional life: the trypanosomes' case. Curr. Chem. Biol. 2011, 5:108-117.
13. Cheng S., Gallie D.R. Wheat eukaryotic initiation factor 4B organizes assembly of RNA and eIFiso4G, eIF4A, and poly(A)-binding protein. J. Biol. Chem. 2006, 281:24351-24364.
14. Craig A.W., Haghighat A., Yu A.T., Sonenberg N. Interaction of polyadenylate-binding protein with the eIF4G homologue PAIP enhances translation. Nature 1998, 392:520-523.
15. Crowe J.H., Carpenter J.F., Crowe L.M. The role of vitrification in anhydrobiosis. Annu. Rev. Physiol. 1998, 60:73-103.
16. Dahms H.U., Hagiwara A., Lee J.S. Ecotoxicology, ecophysiology, and mechanistic studies with rotifers. Aquat. Toxicol. 2011, 101:1-12.
17. Denekamp N.Y., Thorne M.A., Clark M.S., Kube M., Reinhardt R., Lubzens E. Discovering genes associated with dormancy in the monogonont rotifer Brachionus plicatilis. BMC Genomics 2009, 10:108.
18. Denekamp N.Y., Reinhardt R., Kube M., Lubzens E. Late embryogenesis abundant (LEA) proteins in nondesiccated, encysted, and diapausing embryos of rotifers. Biol. Reprod. 2010, 82:714-724.
19. Eulalio A., Behm-Ansmant I., Izaurralde E. P bodies: at the crossroads of post-transcriptional pathways. Nat. Rev. Mol. Cell Biol. 2007, 8:9-22.
20. Farny N.G., Kedersha N.L., Silver P.A. Metazoan stress granule assembly is mediated by P-eIF2alpha-dependent and -independent mechanisms. RNA 2009, 15:1814-1821.
21. Fontaneto D., Giordani I., Melone G., Serra M. Disentangling the morphological stasis in two rotifer species of the Brachionus plicatilis species complex. Hydrobiologia 2007, 583:297-307.
22. Franks T.M., Lykke-Andersen J. TTP and BRF proteins nucleate processing body formation to silence mRNAs with AU-rich elements. Genes Dev. 2007, 21:719-735.
23. Franks T.M., Lykke-Andersen J. The control of mRNA decapping and P-body formation. Mol. Cell 2008, 32:605-615.
24. García-Roger E.M., Martínez A., Serra M. Starvation tolerance of rotifers produced from parthenogenetic eggs and from diapausing eggs: a life table approach. J. Plankton Res. 2006, 28:257-265.
25. Gilks N., Kedersha N., Ayodele M., Shen L., Stoecklin G., Dember L.M., Anderson P. Stress granule assembly is mediated by prion-like aggregation of TIA-1. Mol. Biol. Cell 2004, 15:5383-5398.
26. Gilly M., Pellegrini M. Puromycin photoaffinity labels small- and large-subunit proteins at the A site of the Drosophila ribosome. Biochemistry 1985, 24:5781-5786.
27. Grousl T., Ivanov P., Frydlova I., Vasicova P., Janda F., Vojtova J., Malinska K., Malcova I., Novakova L., Janoskova D., Valasek L., Hasek J. Robust heat shock induces eIF2alpha-phosphorylation-independent assembly of stress granules containing eIF3 and 40S ribosomal subunits in budding yeast, Saccharomyces cerevisiae. J. Cell Sci. 2009, 122:2078-2088.
28. Hand S.C., Menze M.A., Toner M., Boswell L., Moore D. LEA proteins during water stress: not just for plants anymore. Annu. Rev. Physiol. 2011, 73:115-134.
29. Hasenohrl D., Lombo T., Kaberdin V., Londei P., Blasi U. Translation initiation factor a/eIF2(-gamma) counteracts 5' to 3' mRNA decay in the archaeon Sulfolobus solfataricus. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:2146-2150.
30. Higgins D.G., BLeasby A.J., Fuchs R. Clustal V: improved software for multiple sequence alignment. Comput. Appl. Biosci. 1992, 8:189-191.
31. Hoekstra F.A., Golovina E.A., Buitink J. Mechanisms of plant desiccation tolerance. Trends Plant Sci. 2001, 6:431-438.
32. Ingelfinger D., Arndt-Jovin D.J., Luhrmann R., Achsel T. The human LSm1-7 proteins colocalize with the mRNA-degrading enzymes Dcp1/2 and Xrnl in distinct cytoplasmic foci. RNA 2002, 8:1489-1501.
33. Jones B.L., Schneider D.M., Snell T.W. Thermostable proteins in the diapausing eggs of Brachionus manjavacas (Rotifera). Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2012, 162:193-199.
34. Kedersha N., Anderson P. Stress granules: sites of mRNA triage that regulate mRNA stability and translatability. Biochem. Soc. Trans. 2002, 30:963-969.
35. Kedersha N., Anderson P. Mammalian stress granules and processing bodies. Methods Enzymol. 2007, 431:61-81.
36. Kedersha N.L., Gupta M., Li W., Miller I., Anderson P. RNA-binding proteins TIA-1 and TIAR link the phosphorylation of eIF-2 alpha to the assembly of mammalian stress granules. J. Cell Biol. 1999, 147:1431-1442.
37. Kedersha N., Cho M.R., Li W., Yacono P.W., Chen S., Gilks N., Golan D.E., Anderson P. Dynamic shuttling of TIA-1 accompanies the recruitment of mRNA to mammalian stress granules. J. Cell Biol. 2000, 151:1257-1268.
38. Kedersha N., Chen S., Gilks N., Li W., Miller I.J., Stahl J., Anderson P. Evidence that ternary complex (eIF2-GTP-tRNA(i)(Met))-deficient preinitiation complexes are core constituents of mammalian stress granules. Mol. Biol. Cell 2002, 13:195-210.
39. Kedersha N., Stoecklin G., Ayodele M., Yacono P., Lykke-Andersen J., Fritzler M.J., Scheuner D., Kaufman R.J., Golan D.E., Anderson P. Stress granules and processing bodies are dynamically linked sites of mRNP remodeling. J. Cell Biol. 2005, 169:871-884.
40. Kim B., Cooke H.J., Rhee K. DAZL is essential for stress granule formation implicated in germ cell survival upon heat stress. Development 2012, 139:568-578.
41. Kimball S.R., Horetsky R.L., Ron D., Jefferson L.S., Harding H.P. Mammalian stress granules represent sites of accumulation of stalled translation initiation complexes. Am. J. Physiol. Cell Physiol. 2003, 284:C273-C284.
42. Kramer S., Queiroz R., Ellis L., Webb H., Hoheisel J.D., Clayton C., Carrington M. Heat shock causes a decrease in polysomes and the appearance of stress granules in trypanosomes independently of eIF2(alpha) phosphorylation at Thr169. J. Cell Sci. 2008, 121:3002-3014.
43. Kwon S., Zhang Y., Matthias P. The deacetylase HDAC6 is a novel critical component of stress granules involved in the stress response. Genes Dev. 2007, 21:3381-3394.
44. Loschi M., Leishman C.C., Berardone N., Boccaccio G.L. Dynein and kinesin regulate stress-granule and P-body dynamics. J. Cell Sci. 2009, 122:3973-3982.
45. Luhrmann R., Bald R., Stoffler-Meilicke M., Stoffler G. Localization of the puromycin binding site on the large ribosomal subunit of Escherichia coli by immunoelectron microscopy. Proc. Natl. Acad. Sci. U. S. A. 1981, 78:7276-7280.
46. Manders' E.M., Stap J., Brakenhoff G.J., van Driel R., Aten J.A. Dynamics of three-dimensional replication patterns during the S-phase, analysed by double labelling of DNA and confocal microscopy. J. Cell Sci. 1992, 103(Pt 3):857-862.
47. Manders' E.M., Verbeek F.J., Aten J.A. Measurement of co-localization of objects in dual-colour confocal images. J. Microsc. 1993, 169:375-382.
48. McEwen E., Kedersha N., Song B., Scheuner D., Gilks N., Han A., Chen J.J., Anderson P., Kaufman R.J. Heme-regulated inhibitor kinase-mediated phosphorylation of eukaryotic translation initiation factor 2 inhibits translation, induces stress granule formation, and mediates survival upon arsenite exposure. J. Biol. Chem. 2005, 280:16925-16933.
49. Minkoff G., Lubzens E., Kahan D. Environmental factors affecting hatching of rotifer (Brachionus plicatilis) resting eggs. Hydrobiologia 1983, 104:61-69.
50. Navarro R.E., Blackwell T.K. Requirement for P granules and meiosis for accumulation of the germline RNA helicase CGH-1. Genesis 2005, 42:172-180.
51. Nilsson D., Sunnerhagen P. Cellular stress induces cytoplasmic RNA granules in fission yeast. RNA 2011, 17:120-133.
52. Nover L., Scharf K.D., Neumann D. Cytoplasmic heat shock granules are formed from precursor particles and are associated with a specific set of mRNAs. Mol. Cell. Biol. 1989, 9:1298-1308.
53. Ohn T., Kedersha N., Hickman T., Tisdale S., Anderson P. A functional RNAi screen links O-GlcNAc modification of ribosomal proteins to stress granule and processing body assembly. Nat. Cell Biol. 2008, 10:1224-1231.
54. Pérez-Legaspi I.A., Rico-martínez R. Effect of temperature and food concentration in two species of littoral rotifers. Hydrobiologia 1998, 387:341-348.
55. Rajesh K., Iyer A., Suragani R.N., Ramaiah K.V. Intersubunit and interprotein interactions of alpha- and beta-subunits of human eIF2: effect of phosphorylation. Biochem. Biophys. Res. Commun. 2008, 374:336-340.
56. Richter J.D. CPEB: a life in translation. Trends Biochem. Sci. 2007, 32:279-285.
57. Rico-Martínez R., Snell T.W. Comparative binding of antibody to a mate recognition pheromone on female Brachionus plicatilis and Brachionus rotundiformis (Rotifera). Hydrobiologia 1997, 358:71-76.
58. Schisa J.A., Pitt J.N., Priess J.R. Analysis of RNA associated with P granules in germ cells of C. elegans adults. Development 2001, 128:1287-1298.
59. Scriven D.R., Lynch R.M., Moore E.D. Image acquisition for colocalization using optical microscopy. Am. J. Physiol. Cell Physiol. 2008, 294:C1119-C1122.
60. Sheth U., Parker R. Decapping and decay of messenger RNA occur in cytoplasmic processing bodies. Science 2003, 300:805-808.
61. Smith H.A., Burns A.R., Shearer T.L., Snell T.W. Three heat shock proteins are essential for rotifer thermotolerance. J. Exp. Mar. Biol. Ecol. 2012, 413:1-6.
62. Snell T.W., Moffat B.D., Janssen C., Persoone G. Acute toxicity tests using rotifers: IV. Effects of cyst age, temperature, and salinity on the sensitivity of Brachionus calyciflorus. Ecotoxicol. Environ. Saf. 1991, 21:308-317.
63. Snell T.W., Kubanek J., Carter W., Payne A.B., Kim J., Hicks M.K., Stelzer C. A protein signal triggers sexual reproduction in Brachionus plicatilis (Rotifera). Mar. Biol. 2006, 149:763-773.
64. Starck S.R., Green H.M., Alberola-Ila J., Roberts R.W. A general approach to detect protein expression in vivo using fluorescent puromycin conjugates. Chem. Biol. 2004, 11:999-1008.
65. Stout E.P., La Clair J.J., Snell T.W., Shearer T.L., Kubanek J. Conservation of progesterone hormone function in invertebrate reproduction. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:11859-11864.
66. Teixeira D., Sheth U., Valencia-Sanchez M.A., Brengues M., Parker R. Processing bodies require RNA for assembly and contain nontranslating mRNAs. RNA 2005, 11:371-382.
67. Thomas M.G., Loschi M., Desbats M.A., Boccaccio G.L. RNA granules: the good, the bad and the ugly. Cell. Signal. 2011, 23:324-334.
68. Thompson J.D., Higgins D.G., Gibson T.J. Clustal W: improving sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994, 22:4673-4680.
69. van Dijk E., Cougot N., Meyer S., Babajko S., Wahle E., Seraphin B. Human Dcp2: a catalytically active mRNA decapping enzyme located in specific cytoplasmic structures. EMBO J. 2002, 21:6915-6924.