mRNA cycles through hypoxia-induced stress granules in live Drosophila embryonic muscles

International Journal of Developmental Biology

Volumn 56, Issue 9, 2012, Pages 701-709

  Van Der Laan, Annelies M A ^a   Van Gemert, Alice M C ^a   Dirks, Roeland W ^a   Noordermeer, Jasprina N ^a   Fradkin, Lee G ^a   Tanke, Hans J ^a   Jost, Carolina R ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Drosophila; FRAP; Hypoxia; mRNA; Stress granules

Indexed keywords

BIOLOGICAL MARKER; INSECT PROTEIN; MESSENGER RNA; PROTEIN DFMRI; PROTEIN RIN; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BLEACHING; CELL CULTURE; CELL GRANULE; CELL STRESS; CONTROLLED STUDY; DROSOPHILA; EMBRYO; HYPOXIA; IN VIVO STUDY; MOLECULAR DYNAMICS; MUSCLE CELL; MUSCLE TISSUE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN RNA BINDING; REPORTER GENE; RNA ANALYSIS; RNA CAPPING; RNA DEGRADATION; RNA STRUCTURE; RNA TRANSPORT; SARCOPLASMIC RETICULUM; TRANSLATION REGULATION;

ANIMALS; ANOXIA; CYTOPLASMIC GRANULES; DROSOPHILA; EMBRYO, NONMAMMALIAN; MUSCLE, SKELETAL; RNA, MESSENGER;

EID: 84869841854     PISSN: 02146282     EISSN: None     Source Type: Journal    
DOI: 10.1387/ijdb.103172al     Document Type: Article

References (40)

1. AIZER A, BRODY Y, LER LW, SONENBERG N, SINGER RH, SHAV-TAL Y (2008). The dynamics of mammalian P body transport, assembly, and disassembly in vivo. Mol Biol Cell 19: 4154-4166.
2. ALLEN DL, ROY RR, EDGERTON VR (1999). Myonuclear domains in muscle adaptation and disease. Muscle Nerve 22: 1350-1360.
3. ANDERSON P, KEDERSHA N (2009). Stress granules. Curr Biol 19: R397-R398.
4. ARIMOTO K, FUKUDA H, IMAJOH-OHMI S, SAITO H, TAKEKAWA M (2008). Formation of stress granules inhibits apoptosis by suppressing stress-responsive MAPK pathways. Nat Cell Biol 10: 1324-1332.
5. AZAD P, ZHOU D, RUSSO E, HADDAD GG (2009). Distinct mechanisms underlying tolerance to intermittent and constant hypoxia in Drosophila Melanogaster. PLoS One 4: e5371.
6. BARBEE SA, ESTES PS, CZIKO AM, HILLEBRAND J, LUEDEMAN RA, COLLER JM, et al., (2006). Staufen-and FMRP-containing neuronal RNPs are structurally and functionally related to somatic P bodies. Neuron 52: 997-1009.
7. BERTRAND E, CHARTRAND P, SCHAEFER M, SHENOY SM, SINGER RH, LONG RM (1998). Localization of ASH1 mRNA particles in living yeast. Mol Cell 2: 437-445.
8. BHATTACHARYYA SN, HABERMACHER R, MARTINE U, CLOSS EI, FILIPOWICZ W (2006). Stress-induced reversal of microRNA repression and mRNA P-body localization in human cells. Cold Spring Harb Symp Quant Biol 71: 513-521.
9. BRAND AH, PERRIMON N (1993). Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401-415.
10. BRENGUES M, TEIXEIRA D, PARKER R (2005). Movement of eukaryotic mRNAs between polysomes and cytoplasmic processing bodies. Science 310: 486-489.
11. COSSU G, SAMPAOLESI M (2007). New therapies for Duchenne muscular dystrophy: challenges, prospects and clinical trials. Trends Mol Med 13: 520-526.
12. DIGREGORIO PJ, UBERSAX JA, O'FARRELL PH (2001). Hypoxia and nitric oxide induce a rapid, reversible cell cycle arrest of the Drosophila syncytial divisions. J Biol Chem 276: 1930-1937.
13. DOUGLAS RM, XU T, HADDAD GG (2001). Cell cycle progression and cell division are sensitive to hypoxia in Drosophila Melanogaster embryos. Am J Physiol Regul Integr Comp Physiol 280: R1555-R1563.
14. INGELFINGER D, RNDT-JOVIN DJ, LUHRMANN R, ACHSEL T (2002). The human LSm1-7 proteins colocalize with the mRNA-degrading enzymes Dcp1/2 and Xrnl in distinct cytoplasmic foci. RNA 8: 1489-1501.
15. IRVINE K, STIRLING R, HUME D, KENNEDY D (2004). Rasputin, more promiscuous than ever: a review of G3BP. Int J Dev Biol 48: 1065-1077.
16. KEDERSHA N, ANDERSON P (2007). Mammalian stress granules and processing bodies. Methods Enzymol 431: 61-81.
17. KEDERSHA N, CHO MR, LI W, YACONO PW, CHEN S, GILKS N, et al., (2000). Dynamic shuttling of TIA-1 accompanies the recruitment of mRNA to mammalian stress granules. J Cell Biol 151: 1257-1268.
18. KEDERSHA N, STOECKLIN G, AYODELE M, YACONO P, LYKKE-ANDERSEN J, FRITZLER MJ, et al., (2005). Stress granules and processing bodies are dynamically linked sites of mRNP remodeling. J Cell Biol 169: 871-884.
19. KIM SH, DONG WK, WEILER IJ, GREENOUGH WT (2006). Fragile X mental retardation protein shifts between polyribosomes and stress granules after neuronal injury by arsenite stress or in vivo hippocampal electrode insertion. J Neurosci 26: 2413-2418.
20. KIM YK, FURIC L, PARISIEN M, MAJOR F, DESGROSEILLERS L, MAQUAT LE (2007). Staufen1 regulates diverse classes of mammalian transcripts. EMBO J 26: 2670-2681.
21. KINDLER S, WANG H, RICHTER D, TIEDGE H (2005). RNA transport and local control of translation. Annu Rev Cell Dev Biol 21: 223-245.
22. KROUWELS IM, WIESMEIJER K, ABRAHAM TE, MOLENAAR C, VERWOERD NP, TANKE HJ, et al., (2005). A glue for heterochromatin maintenance: stable SUV39H1 binding to heterochromatin is reinforced by the SET domain. J. Cell Biol. 170: 537-549.
23. LAGGERBAUER B, OSTARECK D, KEIDEL EM, OSTARECK-LEDERER A, FISCHER U (2001). Evidence that fragile X mental retardation protein is a negative regulator of translation. Hum Mol Genet 10: 329-338.
24. MAZROUI R, HUOT ME, TREMBLAY S, FILION C, LABELLE Y, KHANDJIAN EW (2002). Trapping of messenger RNA by Fragile X Mental Retardation protein into cytoplasmic granules induces translation repression. Hum Mol Genet 11: 3007-3017.
25. MOLLET S, COUGOT N, WILCZYNSKA A, DAUTRY F, KRESS M, BERTRAND E, et al., (2008). Translationally repressed mRNA transiently cycles through stress granules during stress. Mol Biol Cell 19: 4469-4479.
26. MOSQUEIRA M, WILLMANN G, RUOHOLA-BAKER H, KHURANA TS (2010). Chronic hypoxia impairs muscle function in the Drosophila model of Duchenne's muscular dystrophy (DMD). PLoS One 5: e13450.
27. NOVER L, SCHARF KD, NEUMANN D (1989). Cytoplasmic Heat-Shock Granules Are Formed from Precursor Particles and Are Associated with A Specific Set of Messenger-Rnas. Molec. Cell Biol. 9: 1298-1308.
28. PATEL NH (1994). Imaging neuronal subsets and other cell types in whole-mount Drosophila embryos and larvae using antibody probes. Methods Cell Biol 44: 445-487.
29. PAZMAN C, MAYES CA, FANTO M, HAYNES SR, MLODZIK M (2000). Rasputin, the Drosophila homologue of the RasGAP SH3 binding protein, functions in ras-and Rho-mediated signaling. Development 127: 1715-1725.
30. PILGRAM GS, POTIKANOND S, BAINES RA, FRADKIN LG, NOORDERMEER JN (2010). The roles of the dystrophin-associated glycoprotein complex at the synapse. Mol Neurobiol 41: 1-21.
31. REITS EA, NEEFJES JJ (2001). From fixed to FRAP: measuring protein mobility and activity in living cells. Nat Cell Biol 3: E145-E147.
32. SAKUNO T, ARAKI Y, OHYA Y, KOFUJI S, TAKAHASHI S, HOSHINO S, et al., (2004). Decapping reaction of mRNA requires Dcp1 in fission yeast: its characterization in different species from yeast to human. J Biochem 136: 805-812.
33. SCHENCK A, VAN DB, V, BARDONI B, GIANGRANDE A (2002). Novel features of dFMR1, the Drosophila orthologue of the fragile X mental retardation protein. Neurobiol Dis 11: 53-63.
34. SHCHERBATA HR, YATSENKO AS, PATTERSON L, SOOD VD, NUDEL U, YAFFE D, et al., (2007). Dissecting muscle and neuronal disorders in a Drosophila model of muscular dystrophy. EMBO J 26: 481-493.
35. SHE M, DECKER CJ, SVERGUN DI, ROUND A, CHEN N, MUHLRAD D, et al., (2008). Structural basis of dcp2 recognition and activation by dcp1. Mol Cell 29: 337-349.
36. SOUQUERE S, MOLLET S, KRESS M, DAUTRY F, PIERRON G, WEIL D (2009). Unravelling the ultrastructure of stress granules and associated P-bodies in human cells. J Cell Sci 122: 3619-3626.
37. STAVREVA DA, MCNALLY JG (2004). Fluorescence recovery after photobleaching (FRAP) methods for visualizing protein dynamics in living mammalian cell nuclei. Methods Enzymol 375: 443-455.
38. TOURRIERE H, CHEBLI K, ZEKRI L, COURSELAUD B, BLANCHARD JM, BERTRAND E, et al., (2003). The RasGAP-associated endoribonuclease G3BP assembles stress granules. J Cell Biol 160: 823-831.
39. VAN DER PLAS MC, PILGRAM GS, DE JONG AW, BANSRAJ MR, FRADKIN LG, NOORDERMEER JN (2007). Drosophila Dystrophin is required for integrity of the musculature. Mech Dev 124: 617-630.
40. VAN GEMERT AM, VAN DER LAAN AM, PILGRAM GS, FRADKIN LG, NOORDERMEER JN, TANKE HJ, et al., (2009). In vivo monitoring of mRNA movement in Drosophila body wall muscle cells reveals the presence of myofiber domains. PLoS One 4: e6663.