Drosophila CrebB is a Substrate of the Nonsense-Mediated mRNA Decay Pathway that Sustains Circadian Behaviors |
Ri, Hwajung
(Department of Biological Sciences, Korea Advanced Institute of Science and Technology (KAIST))
Lee, Jongbin (Department of Biological Sciences, Korea Advanced Institute of Science and Technology (KAIST)) Sonn, Jun Young (Department of Biological Sciences, Korea Advanced Institute of Science and Technology (KAIST)) Yoo, Eunseok (School of Life Sciences, Ulsan National Institute of Science and Technology (UNIST)) Lim, Chunghun (School of Life Sciences, Ulsan National Institute of Science and Technology (UNIST)) Choe, Joonho (Department of Biological Sciences, Korea Advanced Institute of Science and Technology (KAIST)) |
1 | Agostino, P.V., Golombek, D.A., and Meck, W.H. (2011). Unwinding the molecular basis of interval and circadian timing. Front. Integr. Neurosci., 5, 64. DOI |
2 | Allada, R., White, N.E., So, W.V., Hall, J.C., and Rosbash, M. (1998). A mutant Drosophila homolog of mammalian clock disrupts circadian rhythms and transcription of period and timeless. Cell 93, 791-804. DOI |
3 | Alonso, C.R. (2005). Nonsense-mediated RNA decay: a molecular system micromanaging individual gene activities and suppressing genomic noise. Bioessays 27, 463-466. DOI |
4 | Aronson, B.D., Johnson, K.A., Loros, J.J., and Dunlap, J.C. (1994). Negative feedback defining a circadian clock: autoregulation of the clock gene frequency. Science 263, 1578-1584. DOI |
5 | Avery, P., Vicente-Crespo, M., Francis, D., Nashchekina, O., Alonso, C. R., and Palacios, I.M. (2011). Drosophila Upf1 and Upf2 loss of function inhibits cell growth and causes animal death in a Upf3-independent manner. RNA 17, 624-638. DOI |
6 | Barberan-Soler, S., and Zahler, A.M. (2008). Alternative splicing regulation during C. elegans development: splicing factors as regulated targets. PLoS Genet. 4, e1000001. DOI |
7 | Lim, C., and Allada, R. (2013). Emerging roles for post-transcriptional regulation in circadian clocks. Nat. Neurosci. 16, 1544-1550. DOI |
8 | Lim, C., Chung, B.Y., Pitman, J.L., McGill, J.J., Pradhan, S., Lee, J., Allada, R. (2007). Clockwork orange encodes a transcriptional repressor important for circadian-clock amplitude in Drosophila. Curr. Biol. 17, 1082-1089. DOI |
9 | Lim, C., Lee, J., Choi, C., Kilman, V.L., Kim, J., Park, S.M., Jang S.K., Allada R. and Choe, J. (2011). The novel gene twenty-four defines a critical translational step in the Drosophila clock. Nature 470, 399-403. DOI |
10 | Lim, C., Lee, J., Choi, C., Kim, J., Doh, E., and Choe, J. (2007). Functional role of CREB-binding protein in the circadian clock system of Drosophila melanogaster. Mol. Cell. Biol. 27, 4876-4890. DOI |
11 | Lin, Y., Stormo, G.D., and Taghert, P.H. (2004). The neuropeptide pigment-dispersing factor coordinates pacemaker interactions in the Drosophila circadian system. J. Neurosci. 24, 7951-7957. DOI |
12 | Sun, X., Dang, F., Zhang, D., Yuan, Y., Zhang, C., Wu, Y., Wang, Y. and Liu, Y. (2015). Glucagon-CREB/CRTC2 signaling cascade regulates hepatic BMAL1 protein. J. Biol. Chem. 290, 2189-2197. DOI |
13 | Shimizu, F., and Fukada, Y. (2007). Circadian phosphorylation of ATF-2, a potential activator of Period2 gene transcription in the chick pineal gland. J. Neurochem. 103, 1834-1842. DOI |
14 | Stanewsky, R., Kaneko, M., Emery, P., Beretta, B., Wager-Smith, K., Kay, S.A., Rosbash, M., and Hall, J.C. (1998). The cry(b) mutation identifies cryptochrome as a circadian photoreceptor in Drosophila. Cell 95, 681-692. DOI |
15 | Stoleru, D., Peng, Y., Agosto, J., and Rosbash, M. (2004). Coupled oscillators control morning and evening locomotor behaviour of Drosophila. Nature 431, 862-868. DOI |
16 | Suri, V., Lanjuin, A., and Rosbash, M. (1999). TIMELESS-dependent positive and negative autoregulation in the Drosophila circadian clock. Embo J. 18, 675-686. DOI |
17 | Tabrez, S.S., Sharma, R.D., Jain, V., Siddiqui, A.A., and Mukhopadhyay, A. (2017). Differential alternative splicing coupled to nonsense-mediated decay of mRNA ensures dietary restriction-induced longevity. Nat. Commun. 8, 306. DOI |
18 | Matsumoto, A., Ukai-Tadenuma, M., Yamada, R.G., Houl, J., Uno, K.D., Kasukawa, T., Dauwalder, B., Itoh, T.Q., Takahashi, K., Ueda, R., et al. (2007). A functional genomics strategy reveals clockwork orange as a transcriptional regulator in the Drosophila circadian clock. Genes Dev. 21, 1687-1700. DOI |
19 | Beckwith, E.J., and Ceriani, M.F. (2015). Experimental assessment of the network properties of the Drosophila circadian clock. J. Comp. Neurol. 523, 982-996. DOI |
20 | Livak, K.J., and Schmittgen, T.D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25, 402-408. DOI |
21 | Maurer, C., Winter, T., Chen, S.W., Hung, H.C., and Weber, F. (2016). The CREB-binding protein affects the circadian regulation of behaviour. FEBS Lett. 590, 3213-3220. DOI |
22 | Behm-Ansmant, I., Kashima, I., Rehwinkel, J., Sauliere, J., Wittkopp, N., and Izaurralde, E. (2007). mRNA quality control: an ancient machinery recognizes and degrades mRNAs with nonsense codons. FEBS Lett. 581, 2845-2853. DOI |
23 | Belvin, M.P., Zhou, H., and Yin, J.C. (1999). The Drosophila dCREB2 gene affects the circadian clock. Neuron 22, 777-787. DOI |
24 | Blau, J., and Young, M.W. (1999). Cycling vrille expression is required for a functional Drosophila clock. Cell 99, 661-671. DOI |
25 | Brunner, M., and Schafmeier, T. (2006). Transcriptional and post-transcriptional regulation of the circadian clock of cyanobacteria and Neurospora. Genes Dev. 20, 1061-1074. DOI |
26 | Chan, W.K., Huang, L., Gudikote, J.P., Chang, Y.F., Imam, J.S., MacLean, J.A. 2nd, and Wilkinson, M.F. (2007). An alternative branch of the nonsense-mediated decay pathway. Embo. J. 26, 1820-1830. DOI |
27 | Chang, Y.F., Imam, J.S., and Wilkinson, M.F. (2007). The nonsense-mediated decay RNA surveillance pathway. Annu. Rev. Biochem. 76, 51-74. DOI |
28 | Chapin, A., Hu, H., Rynearson, S.G., Hollien, J., Yandell, M., and Metzstein, M.M. (2014). In vivo determination of direct targets of the nonsense-mediated decay pathway in Drosophila. G3 (Bethesda) 4, 485-496. DOI |
29 | Cheng, P., Yang, Y.H., and Liu, Y. (2001). Interlocked feedback loops contribute to the robustness of the Neurospora circadian clock. Proc. Natl. Acad. Sci. USA 98, 7408-7413. DOI |
30 | Mendell, J.T., Sharifi, N.A., Meyers, J.L., Martinez-Murillo, F.M., and Dietz, H.C. (2004). Nonsense surveillance regulates expression of diverse classes of mammalian transcripts and mutes genomic noise. Nat. Genet. 36, 1073-1078. DOI |
31 | Merrow, M., Franchi, L., Dragovic, Z., Gorl, M., Johnson, J., Brunner, M., Macino, G., and Roenneberg, T. (2001). Circadian regulation of the light input pathway in Neurospora crassa. Embo J., 20, 307-315. DOI |
32 | Metzstein, M.M., and Krasnow, M.A. (2006). Functions of the nonsense-mediated mRNA decay pathway in Drosophila development. PLoS Genet 2, e180. DOI |
33 | Micale, L., Muscarella, L.A., Marzulli, M., Augello, B., Tritto, P., D'Agruma, L., Zelante, L., Palumbo, G., and Merla, G. (2009). VHL frameshift mutation as target of nonsense-mediated mRNA decay in Drosophila melanogaster and human HEK293 cell line. J. Biomed. Biotechnol. 2009, 860761. |
34 | Morgan, L.W., and Feldman, J.F. (1997). Isolation and characterization of a temperature-sensitive circadian clock mutant of Neurospora crassa. Genetics 146, 525-530. DOI |
35 | Muhlemann, O. (2008). Recognition of nonsense mRNA: towards a unified model. Biochem. Soc. Trans 36, 497-501. DOI |
36 | Vosshall, L.B., Price, J.L., Sehgal, A., Saez, L., and Young, M.W. (1994). Block in nuclear localization of period protein by a second clock mutation, timeless. Science 263, 1606-1609. DOI |
37 | O'Neill, J.S., Maywood, E.S., Chesham, J.E., Takahashi, J.S., and Hastings, M.H. (2008). cAMP-dependent signaling as a core component of the mammalian circadian pacemaker. Science 320, 949-953. DOI |
38 | Traunmuller, L., Bornmann, C., and Scheiffele, P. (2014). Alternative splicing coupled nonsense-mediated decay generates neuronal cell type-specific expression of SLM proteins. J. Neurosci. 34, 16755-16761. DOI |
39 | Travnickova-Bendova, Z., Cermakian, N., Reppert, S.M., and Sassone-Corsi, P. (2002). Bimodal regulation of mPeriod promoters by CREB-dependent signaling and CLOCK/BMAL1 activity. Proc. Natl. Acad. Sci. USA 99, 7728-7733. DOI |
40 | Tubon, T.C., Jr., Zhang, J., Friedman, E.L., Jin, H., Gonzales, E.D., Zhou, H., Drier, D., Gerstner, J.R., Paulson, E.A., Fropf, R., et al. (2013). dCREB2-mediated enhancement of memory formation. J. Neurosci. 33, 7475-7487. DOI |
41 | Williams, J.A., Su, H.S., Bernards, A., Field, J., and Sehgal, A. (2001). A circadian output in Drosophila mediated by neurofibromatosis-1 and Ras/MAPK. Science 293, 2251-2256. DOI |
42 | Wu, Y., Zhang, Y., Sun, Y., Yu, J., Wang, P., Ma, H., Chen, S., Ma, L., Zhang, D., He, Q., et al. (2017). Up-frameshift protein UPF1 regulates neurospora crassa circadian and diurnal growth rhythms. Genetics 206, 1881-1893 DOI |
43 | Yepiskoposyan, H., Aeschimann, F., Nilsson, D., Okoniewski, M., and Muhlemann, O. (2011). Autoregulation of the nonsense-mediated mRNA decay pathway in human cells. RNA 17, 2108-2118. DOI |
44 | Depetris-Chauvin, A., Berni, J., Aranovich, E.J., Muraro, N.I., Beckwith, E.J., and Ceriani, M.F. (2011). Adult-specific electrical silencing of pacemaker neurons uncouples molecular clock from circadian outputs. Curr. Biol. 21, 1783-1793. DOI |
45 | Cyran, S.A., Buchsbaum, A.M., Reddy, K.L., Lin, M.C., Glossop, N.R., Hardin, P.E., Young M.W., Storti R.V., and Blau, J. (2003). vrille, Pdp1, and dClock form a second feedback loop in the Drosophila circadian clock. Cell 112, 329-341. DOI |
46 | Davis, G.W., Schuster, C.M., and Goodman, C.S. (1996). Genetic dissection of structural and functional components of synaptic plasticity. III. CREB is necessary for presynaptic functional plasticity. Neuron 17, 669-679. DOI |
47 | Decker, C.J., and Parker, R. (2012). P-bodies and stress granules: possible roles in the control of translation and mRNA degradation. Cold Spring Harb. Perspect. Biol. 4, a012286. DOI |
48 | Eckel-Mahan, K.L., Phan, T., Han, S., Wang, H., Chan, G.C., Scheiner, Z.S., and Storm, D.R. (2008). Circadian oscillation of hippocampal MAPK activity and cAmp: implications for memory persistence. Nat. Neurosci. 11, 1074-1082. DOI |
49 | Emery, P., So, W.V., Kaneko, M., Hall, J.C., and Rosbash, M. (1998). CRY, a Drosophila clock and light-regulated cryptochrome, is a major contributor to circadian rhythm resetting and photosensitivity. Cell 95, 669-679. DOI |
50 | Eulalio, A., Behm-Ansmant, I., and Izaurralde, E. (2007). P bodies: at the crossroads of post-transcriptional pathways. Nat. Rev. Mol. Cell Biol. 8, 9-22. DOI |
51 | Filichkin, S.A., Cumbie, J.S., Dharmawadhana, J.P., Jaiswal, P., Chang, J.H., Palusa, S.G., Reddy A.S., Megraw, M., and Mockler, T.C., (2015). Environmental stresses modulate abundance and timing of alternatively spliced circadian transcripts in Arabidopsis. Mol. Plant 8, 207-227. DOI |
52 | Peng, Y., Stoleru, D., Levine, J.D., Hall, J.C., and Rosbash, M. (2003). Drosophila free-running rhythms require intercellular communication. PLoS Biol. 1, E13. DOI |
53 | Obrietan, K., Impey, S., Smith, D., Athos, J., and Storm, D.R. (1999). Circadian regulation of cAMP response element-mediated gene expression in the suprachiasmatic nuclei. J. Biol. Chem. 274, 17748-17756. DOI |
54 | Palacios-Munoz, A., and Ewer, J. (2018). Calcium and cAMP directly modulate the speed of the Drosophila circadian clock. PLoS Genet. 14, e1007433. DOI |
55 | Park, S., Sonn, J.Y., Oh, Y., Lim, C., and Choe, J. (2014). SIFamide and SIFamide receptor defines a novel neuropeptide signaling to promote sleep in Drosophila. Mol. Cells 37, 295-301. DOI |
56 | Perazzona, B., Isabel, G., Preat, T., and Davis, R.L. (2004). The role of cAMP response element-binding protein in Drosophila long-term memory. J. Neurosci. 24, 8823-8828. DOI |
57 | Peschel, N., and Helfrich-Forster, C. (2011). Setting the clock-by nature: circadian rhythm in the fruitfly Drosophila melanogaster. FEBS Lett. 585, 1435-1442. DOI |
58 | Pfeiffenberger, C., Lear, B.C., Keegan, K.P., and Allada, R. (2010). Processing circadian data collected from the Drosophila activity monitoring (DAM) system. Cold Spring Harb. Protoc. 2010, pdb prot5519. |
59 | Nickless, A., Bailis, J.M., and You, Z. (2017). Control of gene expression through the nonsense-mediated RNA decay pathway. Cell Biosci. 7, 26. DOI |
60 | Yin, J.C., Del Vecchio, M., Zhou, H., and Tully, T. (1995). CREB as a memory modulator: induced expression of a dCREB2 activator isoform enhances long-term memory in Drosophila. Cell 81, 107-115. DOI |
61 | Ginty, D.D., Kornhauser, J.M., Thompson, M.A., Bading, H., Mayo, K. E., Takahashi, J.S., and Greenberg, M.E. (1993). Regulation of CREB phosphorylation in the suprachiasmatic nucleus by light and a circadian clock. Science 260, 238-241. DOI |
62 | Frizzell, K.A., Rynearson, S.G., and Metzstein, M.M. (2012). Drosophila mutants show NMD pathway activity is reduced, but not eliminated, in the absence of Smg6. RNA 18, 1475-1486. DOI |
63 | Fropf, R., Tubon, T.C., Jr., and Yin, J.C. (2013). Nuclear gating of a Drosophila dCREB2 activator is involved in memory formation. Neurobiol. Learn Mem. 106, 258-267. DOI |
64 | Fukuhara, C., Liu, C., Ivanova, T.N., Chan, G.C., Storm, D.R., Iuvone, P.M., and Tosini, G. (2004). Gating of the cAMP signaling cascade and melatonin synthesis by the circadian clock in mammalian retina. J. Neurosci. 24, 1803-1811. DOI |
65 | Grima, B., Chelot, E., Xia, R.H., and Rouyer, F. (2004). Morning and evening peaks of activity rely on different clock neurons of the Drosophila brain. Nature 431, 869-873. DOI |
66 | Hatano, M., Umemura, M., Kimura, N., Yamazaki, T., Takeda, H., Nakano, H., Takahashi, S., Takahashi, Y. (2013). The 5'-untranslated region regulates ATF5 mRNA stability via nonsense-mediated mRNA decay in response to environmental stress. FEBS J. 280, 4693-4707. DOI |
67 | Hendricks, J.C., Williams, J.A., Panckeri, K., Kirk, D., Tello, M., Yin, J.C., and Sehgal, A. (2001). A non-circadian role for cAMP signaling and CREB activity in Drosophila rest homeostasis. Nat. Neurosci. 4, 1108-1115. DOI |
68 | Hosoda, H., Kato, K., Asano, H., Ito, M., Kato, H., Iwamoto, Suzuki, A., Masushige, S., and Kida, S. (2009). CBP/p300 is a cell type-specific modulator of CLOCK/BMAL1-mediated transcription. Mol. Brain 2, 34. DOI |
69 | Hug, N., Longman, D., and Caceres, J.F. (2016). Mechanism and regulation of the nonsense-mediated decay pathway. Nucleic Acids Res. 44, 1483-1495. DOI |
70 | Price, J.L., Dembinska, M.E., Young, M.W., and Rosbash, M. (1995). Suppression of PERIOD protein abundance and circadian cycling by the Drosophila clock mutation timeless. Embo J. 14, 4044-4049. DOI |
71 | Popp, M.W., and Maquat, L.E. (2014). The dharma of nonsense-mediated mRNA decay in mammalian cells. Mol. Cells 37, 1-8. DOI |
72 | Richier, B., Michard-Vanhee, C., Lamouroux, A., Papin, C., and Rouyer, F. (2008). The clockwork orange Drosophila protein functions as both an activator and a repressor of clock gene expression. J. Biol. Rhythms. 23, 103-116. DOI |
73 | Rutila, J.E., Suri, V., Le, M., So, W.V., Rosbash, M., and Hall, J.C. (1998). CYCLE is a second bHLH-PAS clock protein essential for circadian rhythmicity and transcription of Drosophila period and timeless. Cell 93, 805-814. DOI |
74 | Sakamoto, K., Norona, F.E., Alzate-Correa, D., Scarberry, D., Hoyt, K. R., and Obrietan, K. (2013). Clock and light regulation of the CREB coactivator CRTC1 in the suprachiasmatic circadian clock. J. Neurosci. 33, 9021-9027. DOI |
75 | Zheng, D., Chen, C.Y., and Shyu, A.B. (2011). Unraveling regulation and new components of human P-bodies through a protein interaction framework and experimental validation. RNA 17, 1619-1634. DOI |
76 | Yin, J.C., Wallach, J.S., Del Vecchio, M., Wilder, E.L., Zhou, H., Quinn, W.G., and Tully, T. (1994). Induction of a dominant negative CREB transgene specifically blocks long-term memory in Drosophila. Cell 79, 49-58. DOI |
77 | Yin, J.C., Wallach, J.S., Wilder, E.L., Klingensmith, J., Dang, D., Perrimon, N., Zhou, H., Tully, T., and. Quinn, W.G. (1995). A Drosophila CREB/CREM homolog encodes multiple isoforms, including a cyclic AMP-dependent protein kinase-responsive transcriptional activator and antagonist. Mol. Cell. Biol. 15, 5123-5130. DOI |
78 | Yu, D., Akalal, D.B., and Davis, R.L. (2006). Drosophila alpha/beta mushroom body neurons form a branch-specific, long-term cellular memory trace after spaced olfactory conditioning. Neuron 52, 845-855. DOI |
79 | Zhou, J., Yu, W., and Hardin, P.E. (2016). Clockwork orange enhances period mediated rhythms in transcriptional repression by antagonizing E-box binding by clock-cycle. PLoS Genet 12, e1006430. DOI |
80 | Scheving, L.A., and Gardner, W. (1998). Circadian regulation of CREB transcription factor in mouse esophagus. Am. J. Physiol. 274, C1011-1016. DOI |
81 | Schoning, J.C., Streitner, C., Meyer, I.M., Gao, Y., and Staiger, D. (2008). Reciprocal regulation of glycine-rich RNA-binding proteins via an interlocked feedback loop coupling alternative splicing to nonsense-mediated decay in Arabidopsis. Nucleic Acids Res. 36, 6977-6987. DOI |
82 | Schoning, J.C., Streitner, C., Page, D.R., Hennig, S., Uchida, K., Wolf, E., Furuya, M. and Staiger, D. (2007). Auto-regulation of the circadian slave oscillator component AtGRP7 and regulation of its targets is impaired by a single RNA recognition motif point mutation. Plant J. 52(6), 1119-1130. DOI |
83 | Kako, K., Wakamatsu, H., and Ishida, N. (1996). c-fos CRE-binding activity of CREB/ATF family in the SCN is regulated by light but not a circadian clock. Neurosci. Lett. 216, 159-162. DOI |
84 | Hung, H.C., Maurer, C., Kay, S.A., and Weber, F. (2007). Circadian transcription depends on limiting amounts of the transcription co-activator nejire/CBP. J. Biol. Chem. 282, 31349-31357. DOI |
85 | Johansson, M.J., He, F., Spatrick, P., Li, C., and Jacobson, A. (2007). Association of yeast Upf1p with direct substrates of the NMD pathway. Proc. Natl. Acad. Sci. USA 104, 20872-20877. DOI |
86 | Kadener, S., Stoleru, D., McDonald, M., Nawathean, P., and Rosbash, M. (2007). Clockwork orange is a transcriptional repressor and a new Drosophila circadian pacemaker component. Genes Dev. 21, 1675-1686. DOI |
87 | Kim, M., Lee, H., Hur, J.H., Choe, J., and Lim, C. (2016). CRTC Potentiates light-independent timeless transcription to sustain circadian rhythms in Drosophila. Sci. Rep. 6, 32113. DOI |
88 | Kojima, S., Shingle, D.L., and Green, C.B. (2011). Post-transcriptional control of circadian rhythms. J. Cell Sci. 124, 311-320. DOI |
89 | Konopka, R.J., and Benzer, S. (1971). Clock mutants of Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 68, 2112-2116. DOI |
90 | Koyanagi, S., Hamdan, A.M., Horiguchi, M., Kusunose, N., Okamoto, A., Matsunaga, N., and Ohdo, S. (2011). cAMP-response element (CRE)-mediated transcription by activating transcription factor-4 (ATF4) is essential for circadian expression of the Period2 gene. J. Biol. Chem. 286, 32416-32423. DOI |
91 | Kwon, Y.J., Park, M.J., Kim, S.G., Baldwin, I.T., and Park, C.M. (2014). Alternative splicing and nonsense-mediated decay of circadian clock genes under environmental stress conditions in Arabidopsis. BMC Plant. Biol. 14, 136. DOI |
92 | Lewis, B.P., Green, R.E., and Brenner, S.E. (2003). Evidence for the widespread coupling of alternative splicing and nonsense-mediated mRNA decay in humans. Proc. Natl. Acad. Sci. USA 100, 189-192. DOI |
93 | Lee, B., Li, A., Hansen, K.F., Cao, R., Yoon, J.H., and Obrietan, K. (2010). CREB influences timing and entrainment of the SCN circadian clock. J. Biol. Rhythms. 25, 410-420. DOI |
94 | Lee, Y., Lee, J., Kwon, I., Nakajima, Y., Ohmiya, Y., Son, G.H., Lee, K.H., and Kim, K. (2010). Coactivation of the CLOCK-BMAL1 complex by CBP mediates resetting of the circadian clock. J. Cell Sci. 123, 3547-3557. DOI |
95 | Lemos, D.R., Goodspeed, L., Tonelli, L., Antoch, M.P., Ojeda, S.R., and Urbanski, H.F. (2007). Evidence for circadian regulation of activating transcription factor 5 but not tyrosine hydroxylase by the chromaffin cell clock. Endocrinology 148, 5811-5821. DOI |
96 | Shen, Y., Wu, X., Liu, D., Song, S., Liu, D., and Wang, H. (2016). Cold-dependent alternative splicing of a Jumonji C domain-containing gene MtJMJC5 in Medicago truncatula. Biochem. Biophys. Res. Commun. 474, 271-276. DOI |
97 | Sehgal, A., Price, J.L., Man, B., and Young, M.W. (1994). Loss of circadian behavioral rhythms and per RNA oscillations in the Drosophila mutant timeless. Science 263, 1603-1606. DOI |
98 | Shaul, O. (2015). Unique aspects of plant nonsense-mediated mRNA decay. Trends Plant Sci. 20, 767-779. DOI |
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