Multifunctional roles of the mammalian CCR4-NOT complex in physiological phenomena

Frontiers in Genetics

Volumn 5, Issue AUG, 2014, Pages

  Shirai, Yo Taro ^a   Suzuki, Toru ^a   Morita, Masahiro ^b,c   Takahashi, Akinori ^a   Yamamoto, Tadashi ^a  

^a OKINAWA INSTITUTE OF SCIENCE AND TECHNOLOGY GRADUATE UNIVERSITY   (Japan)

^b MCGILL UNIVERSITY   (Canada)

^c MCGILL UNIVERSITY   (Canada)

Author keywords

Ccr4 not; Deadenylation; Knockout mice; mRNA decay; Posttranscriptional regulation

Indexed keywords

CARBON CATABOLITE REPRESSION 4 NOT COMPLEX; CARBON CATABOLITE REPRESSION 4 PROTEIN; CNOT1 PROTEIN; CNOT10 PROTEIN; CNOT11 PROTEIN; CNOT2 PROTEIN; CNOT3 PROTEIN; CNOT6 PROTEIN; CNOT6L PROTEIN; CNOT7 PROTEIN; CNOT8 PROTEIN; CNOT9 PROTEIN; NEGATIVE ON TATA LESS PROTEIN; PROTEASOME; PROTEIN; RNA BINDING PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CHEMICAL MODIFICATION; DEADENYLATION; GENE; HOMEOSTASIS; HUMAN; INTRACELLULAR SIGNALING; MAMMAL; NONHUMAN; ORTHOLOGY; PHYSIOLOGICAL PROCESS; PROTEIN FUNCTION; SINGLE NUCLEOTIDE POLYMORPHISM; TRANSCRIPTION REGULATION;

EID: 84906215359     PISSN: None     EISSN: 16648021     Source Type: Journal    
DOI: 10.3389/fgene.2014.00286     Document Type: Article

References (116)

1. Ajiro, M., Katagiri, T. Ueda, K., Nakagawa, H., Fukukawa, C., Lin, M. L. et al., (2009). Involvement of RQCD1 overexpression, a novel cancer-testis antigen, in the Akt pathway in breast cancer cells. Int. J. Oncol. 35, 673-681. doi: 10.3892/ijo_00000379
2. Ajiro, M., Nishidate, T., Katagiri, T., and Nakamura, Y. (2010). Critical involvement of RQCD1 in the EGFR-Akt pathway in mammary carcinogenesis. Int. J. Oncol. 37, 1085-1093. doi: 10.3892/ijo_00000760
3. Aslam, A., Mittal, S., Koch, F., Andrau, J. C., and Winkler, G. S. (2009). The Ccr4-NOT deadenylase subunits CNOT7 and CNOT8 have overlapping roles and modulate cell proliferation. Mol. Biol. Cell 20, 3840-3850. doi: 10.1091/mbc.E09-02-0146
4. Bai,Y., Salvadore, C., Chiang, Y. C., Collart, M. A., Liu, H. Y., and Denis, C. L. (1999). The CCR4 and CAF1 proteins of the CCR4-NOT complex are physically and functionally separated from NOT2, NOT4, and NOT5. Mol. Cell. Biol. 19, 6642-6651.
5. Bartlam, M., and Yamamoto, M. (2010). The structural basis for deadenylation by the CCR4-NOT complex. Protein Cell 25, 443-452. doi: 10.1007/s13238-010-0060-8
6. Basquin, J., Roudko, V. V., Rode, M., Basquin, C., Séraphin, B., and Conti, E. (2012). Architecture of the nuclease module of the yeast Ccr4-not complex: the Not1-Caf1-Ccr4 interaction. Mol. Cell 48, 207-218. doi: 10.1016/j.molcel.2012.08.014.
7. Bawankar, P., Loh, B., Wohlbold, L., Schmidt, S., and Izaurralde, E. (2013). NOT10 and C2orf29/NOT11 form a conserved module of the CCR4-NOT complex that docks onto the NOT1 N-terminal domain. RNA Biol. 10, 228-244. doi: 10.4161/rna.23018
8. Behm-Ansmant, I., Rehwinkel, J., Doerks, T., Stark, A., Bork, P., and Izaurralde, E. (2006). mRNA degradation by miRNAs and GW182 requires both CCR4:NOT deadenylase and DCP1:DCP2 decapping complexes. Genes Dev. 20, 1885-1898. doi:10.1101/gad.1424106
9. Berthet, C., Morera, A. M., Asensio, M. J., Chauvin, M. A., Morel, A. P., Dijoud, F., et al. (2004). CCR4-associated factor CAF1 is an essential factor for spermatogenesis. Mol. Cell. Biol. 24, 5808-5820. doi: 10.1128/MCB.24.13.5808-5820.2004
10. Bhandari, D., Raisch, T., Weichenrieder, O., Jonas, S., and Izaurralde, E. (2014). Structural basis for the Nanos-mediated recruitment of the CCR4-NOT complex and translational repression. Genes Dev. 28, 888-901. doi: 10.1101/gad.237289.113
11. Bianchin, C., Mauxion, F., Sentis, S., Séraphin, B., and Corbo, L. (2005). Conservation of the deadenylase activity of proteins of the Caf1 family in human. RNA 11, 487-494. doi: 10.1261/rna.7135305
12. Boland, A., Chen, Y., Raisch, T., Jonas, S., Kuzuoǧlu-Öztürk, D., Wohlbold, L. et al. (2013). Structure and assembly of the NOT module of the human CCR4-NOT complex. Nat. Struct. Mol. Biol. 20, 1289-1297. doi: 10.1038/nsmb.2681
13. Braun, J. E., Huntzinger, E., Fauser, M., and Izaurralde, E. (2011). GW182 proteins directly recruit cytoplasmic deadenylase complexes to miRNA targets. Mol. Cell 44, 120-133. doi: 10.1016/j.molcel.2011.09.007
14. Chapat, C., Kolytcheff, C., Le Romancer, M., Auboeuf, D., De La Grange, P., Chettab, K., et al. (2013). hCAF1/CNOT7 regulates interferon signalling by targeting STAT1. EMBO J. 32, 688-700. doi: 10.1038/emboj.2013.11
15. Chekulaeva, M., Mathys, H., Zipprich, J. T., Attig, J., Colic, M., Parker, R., et al. (2011). miRNA repression involves GW182-mediated recruitment of CCR4-NOT through conserved W-containing motifs. Nat. Struct. Mol. Biol. 18, 1218-1226. doi: 10.1038/nsmb.2166
16. Chen, C., Ito, K., Takahashi, A., Wang, G., Suzuki, T., Nakazawa, T., et al., (2011) Distinct expression patterns of the subunits of the CCR4-NOT deadenylase complexduring neural development. Biochem. Biophys. Res. Commun. 411, 360-364. doi: 10.1016/j.bbrc.2011.06.148
17. Chen, J., Rappsilber, J., Chiang, Y. C., Russell, P., Mann, M., and Denis, C. L. (2001). Purification and characterization of the 1.0 MDa CCR4-NOT complex identifies two novel components of the complex. J. Mol. Biol. 314, 683-694. doi:10.1006/jmbi.2001.5162
18. Chen, Y., Boland, A., Kuzuoǧlu-Öztürk, D., Bawankar, P., Loh, B., Chang, C. T. et al., (2014). A DDX6-CNOT1 Complex and W-Binding Pockets in CNOT9 Reveal Direct Links between miRNA Target Recognition and Silencing. Mol. Cell 54, 737-750. doi: 10.1016/j.molcel.2014.03.034
19. Chicoine, J., Benoit, P., Gamberi, C., Paliouras, M., Simonelig, M., and Lasko, P. (2007). Bicaudal-C recruits CCR4-NOT deadenylase to target mRNAs and regulates oogenesis, cytoskeletal organization, and its own expression. Dev. Cell 13, 691-704 doi: 10.1016/j.devcel.2007.10.002
20. Collart, M. A., and Struhl, K. (1993). CDC39, an essential nuclear protein that negatively regulates transcription and differentially affects the constitutive and inducible HIS3 promoters. EMBO J. 12, 177-186.
21. Collart, M. A., and Struhl, K. (1994). NOT1(CDC39), NOT2(CDC36), NOT3, and NOT4 encode a global-negative regulator of transcription that differentially affects TATA-element utilization. Genes Dev. 8, 525-537. doi: 10.1101/gad.8.5.525
22. Collart, M. A. (2003). Global control of gene expression in yeast by the Ccr4-Not complex. Gene. 313, 1-16. doi: 10.1016/S0378-1119(03)00672-3
23. Collart, M. A., and Timmers, H. T. (2004). The eukaryotic Ccr4-not complex: a regulatory platform integrating mRNA metabolism with cellular signaling pathways? Prog. Nucleic Acid Res. Mol. Biol. 77, 289-322. doi: 10.1016/S0079-6603(04)77008-7
24. Collart, M. A., and Panasenko, O. O. (2012). The Ccr4-Not complex. Gene 492, 42-53. doi: 10.1016/j.gene.2011.09.033
25. Cooke, A., Prigge, A., and Wickens, M. (2010). Translational repression by deadenylases. J. Biol. Chem. 285, 28506-28513. doi: 10.1074/jbc.M110.150763
26. De Keersmaecker, K., Atak, Z. K., Li, N., Vicente, C., Patchett, S., Girardi, T., et al. (2013). Exome sequencing identifies mutation in CNOT3 and ribosomal genes RPL5 and RPL10 in T-cell acute lymphoblastic leukemia. Nat. Genet. 45, 186-190. doi: 10.1038/ng.2508
27. Denis, C. L. (1984). Identification of new genes involved in the regulation of yeast alcohol dehydrogenase II. Genetics 108, 833-844.
28. Díaz-Peña, R., Aransay, A. M., Suárez-Álvarez, B., Bruges-Armas, J., Rodríguez-Ezpeleta, N., Regueiro, M., et al. (2012). A high density SNP genotyping approach within the 19q13 chromosome region identifies an association of a CNOT3 polymorphism with ankylosing spondylitis. Ann. Rheum. Dis. 71, 714-717. doi: 10.1136/annrheumdis-2011-20066
29. Doidge, R., Mittal, S., Aslam, A., and Winkler, G.S. (2012a). Deadenylation of cytoplasmic mRNA by the mammalian Ccr4-Not complex. Biochem. Soc. Trans. 40, 896-901. doi: 10.1042/BST20120074
30. Doidge, R., Mittal, S., Aslam, A., and Winkler, G.S. (2012b). The anti-proliferative activity of BTG/TOB proteins is mediated via the Caf1a (CNOT7) and Caf1b (CNOT8) deadenylase subunits of the Ccr4-not complex. PLoS One 7:e51331. doi: 10.1371/journal.pone.0051331
31. Dupressoir, A., Morel, A. P., Barbot, W., Loireau, M. P., Corbo, L., and Heidmann, T. (2001). Identification of four families of yCCR4- and Mg2+-dependent endonuclease-related proteins in higher eukaryotes, and characterization of orthologs of yCCR4 with a conserved leucine-rich repeat essential for hCAF1/hPOP2 binding.BMC Genomics 2:9
32. Eulalio, A., Behm-Ansmant, I., Schweizer, D., and Izaurralde, E. (2007). P-body formation is a consequence, not the cause, of RNA-mediated gene silencing. Mol. Cell. Biol. 27, 3970-3981. doi: 10.1128/MCB.00128-07
33. Ezzeddine, N., Chang, T. C., Zhu, W., Yamashita, A., Chen, C. Y., Zhong, Z., et al., (2007). Human TOB, an antiproliferative transcription factor, is a poly(A)-binding protein-dependent positive regulator of cytoplasmic mRNA deadenylation. Mol. Cell. Biol. 27, 7791-7801.
34. Ezzeddine, N., Chen, C. Y., and Shyu, A. B. (2012). Evidence providing new insights into TOB-promoted deadenylation and supporting a link between TOB's deadenylation-enhancing and antiproliferative activities. Mol. Cell. Biol. 32, 1089-1098. doi: 10.1128/MCB.06370-11
35. Fabian, M. R., Cieplak, M. K., Frank, F., Morita, M., Green, J., Srikumar, T., et al. (2011). miRNA-mediated deadenylation is orchestrated by GW182 through two conserved motifs that interact with CCR4-NOT. Nat. Struct. Mol. Biol. 18, 1211-1217. doi: 10.1038/nsmb.2149
36. Fabian, M. R., and Sonenberg, N. (2012). The mechanics of miRNA-mediated gene silencing: a look under the hood of miRISC. Nat. Struct. Mol. Biol. 19, 586-593. doi: 10.1038/nsmb.2296
37. Fabian, M. R., Frank, F., Rouya, C., Siddiqui, N., Lai, W. S., Karetnikov, A., et al. (2013). Structural basis for the recruitment of the human CCR4-NOT deadenylase complex by tristetraprolin. Nat. Struct. Mol. Biol. 20, 735-739. doi: 10.1038/nsmb.2572
38. Faraji, F., Hu, Y., Wu, G., Goldberger, N. E., Walker, R. C., Zhang, J., et al. (2014). An integrated systems genetics screen reveals the transcriptional structure of inherited predisposition to metastatic disease. Genome Res. 24, 227-240. doi:10.1101/gr.166223.113
39. Färber, V., Erben, E., Sharma, S., Stoecklin, G., and Clayton, C. (2013). Trypanosome CNOT10 is essential for the integrity of the NOT deadenylase complex and for degradation of many mRNAs. Nucleic Acids Res. 41, 1211-1222. doi: 10.1093/nar/gks1133
40. Funakoshi, Y., Doi, Y., Hosoda, N., Uchida, N., Osawa, M., Shimada, I., et al., (2007). Mechanism of mRNA deadenylation: evidence for a molecular interplay between translation termination factor eRF3 and mRNA deadenylases. Genes Dev. 21, 3135-48. doi: 10.1101/gad.1597707
41. Garapaty, S., Mahajan, M. A., and Samuels, H. H. (2008). Components of the CCR4-NOT complex function as nuclear hormone receptor coactivators via association with the NRC-interacting Factor NIF-1. J. Biol. Chem. 283, 6806-6816. doi: 10.1074/jbc.M706986200
42. Garces, R. G., Gillon, W., and Pai, E. F. (2007). Atomic model of human Rcd-1 reveals an armadillo-like-repeat protein with in vitro nucleic acid binding properties. Protein Sci. 16, 176-188. doi: 10.1110/ps.062600507
43. Godwin, A. R., Kojima, S., Green, C. B., and Wilusz, J. (2013). Kiss your tail goodbye: the role of PARN, Nocturnin, and Angel deadenylases in mRNA biology. Biochim. Biophys. Acta 1829, 571-579. doi: 10.1016/j.bbagrm
44. Goldstrohm, A. C., Hook, B. A., Seay, D. J., and Wickens, M. (2006). PUF proteins bind Pop2p to regulate messenger RNAs. Nat. Struct. Mol. Biol. 13, 533-539. doi:10.1038/nsmb1100
45. Goldstrohm, A. C., Seay, D. J., Hook, B. A., and Wickens, M. (2007). PUF protein-mediated deadenylation is catalyzed by Ccr4p. J. Biol. Chem. 282, 109-114. doi: 10.1074/jbc.M609413200
46. Goldstrohm, A. C., and Wickens, M. (2008). Multifunctional deadenylase complexes diversify mRNA control. Nat. Rev. Mol. Cell. Biol. 9, 337-344. doi: 10.1038/nrm2370
47. Gregory, R. C., Lord, K. A., Panek, L. B., Gaines, P., Dillon, S. B., and Wojchowski, D. M. (2000). Subtraction cloning and initial characterization of novel epo-immediate response genes. Cytokine 12, 845-857. doi: 10.1006/cyto.2000.0686
48. Gutierrez-Camino, A., Lopez-Lopez, E, Martin-Guerrero, I., Piñan, M. A., Garcia-Miguel, P, Sanchez-Toledo, J., et al. (2014). Noncoding RNA-related polymorphisms in pediatric acute lymphoblastic leukemia susceptibility. Pediatr. Res. 75, 767-773. doi: 10.1038/pr.2014.43
49. Haas, M., Siegert, M., Schürmann, A., Sodeik, B., and Wolfes, H. (2004). c-Myb protein interacts with Rcd-1, a component of the CCR4 transcription mediator complex. Biochemistry 43, 8152-8159. doi: 10.1021/bi035857y
50. Halter, D., Collart, M. A., and Panasenko, O. O. (2014). The Not4 E3 Ligase and CCR4 Deadenylase Play Distinct Roles in Protein Quality Control. PLoS One 9:e86218. doi: 10.1371/journal.pone.0086218
51. Hämmerle, M., Gutschner, T., Uckelmann, H., Ozgur, S., Fiskin, E., Gross, M., et al. (2013). Posttranscriptional destabilization of the liver-specific long noncoding RNA HULC by the IGF2 mRNA-binding protein 1 (IGF2BP1). Hepatology 58, 1703-1712. doi: 10.1002/hep.26537
52. Hiroi, N., Ito, T., Yamamoto, H., Ochiya, T., Jinno, S., and Okayama, H. (2002). Mammalian Rcd1 is a novel transcriptional cofactor that mediates retinoic acid-induced cell differentiation. EMBO J. 21, 5235-5244. doi: 10.1093/emboj/cdf521
53. Horiuchi, M., Takeuchi, K., Noda, N., Muroya, N., Suzuki, T., Nakamura, T., et al., (2009). J. Biol. Chem. 284, 13244-13255. doi: 10.1074/jbc.M809250200
54. Hosoda, N., Funakoshi, Y., Hirasawa, M., Yamagishi, R., Asano, Y., Miyagawa, R., et al.(2011). Anti-proliferative protein Tob negatively regulates CPEB3 target by recruiting Caf1 deadenylase. EMBO J. 30, 1311-1323. doi: 10.1038/emboj.2011.37
55. Hu, G., Kim, J., Xu, Q., Leng, Y., Orkin, S. H., and Elledge, S. J. (2009). A genome-wide RNAi screen identifies a new transcriptional module required for self-renewal. Genes Dev. 23, 837-848. doi: 10.1101/gad.1769609
56. Ito, K., Takahashi, A., Morita, M., Suzuki, T., and Yamamoto, T. (2011a). The role of the CNOT1 subunit of the CCR4-NOT complex in mRNA deadenylation and cell viability. Protein Cell 2, 755-763. doi: 10.1007/s13238-011-1092-4
57. Ito, K., Inoue, T., Yokoyama, K., Morita, M., Suzuki, T., and Yamamoto, T. (2011b). CNOT2 depletion disrupts and inhibits the CCR4-NOT deadenylase complex and induces apoptotic cell death. Genes Cells 16, 368-379. doi: 10.1111/j.1365-2443.2011.01492.x
58. Jayne, S., Zwartjes, C. G., van Schaik, F. M., and Timmers, H. T. (2006). Involvement of the SMRT/NCoR-HDAC3 complex in transcriptional repression by the CNOT2 subunit of the human Ccr4-Not complex. Biochem. J. 398, 461-467. doi: 10.1042/BJ20060406
59. Joly, W., Chartier, A., Rojas-Rios, P., Busseau, I., and Simonelig, M. (2013). The CCR4 Deadenylase Acts with Nanos and Pumilio in the Fine-Tuning of Mei-P26 Expression to Promote Germline Stem Cell Self-Renewal. Stem Cell Reports 1, 411-424. doi: 10.1016/j.stemcr.2013.09.007
60. Kerr, S. C., Azzouz, N., Fuchs, S. M., Collart, M. A., Strahl, B. D., Corbett, A. H., et al. (2011). The Ccr4-Not complex interacts with the mRNA export machinery. PLoS One 6:e18302. doi: 10.1371/journal.pone.0018302
61. Kim, I., Kwak, H., Lee, H. K., Hyun, S., and Jeong, S. (2012). β-Catenin recognizes a specific RNA motif in the cyclooxygenase-2 mRNA 3'-UTR and interacts with HuR in colon cancer cells. Nucleic Acids Res. 40, 6863-6872. doi: 10.1093/nar/gks331
62. Lau, N. C., Kolkman, A., van Schaik, F. M., Mulder, K.W., Pijnappel, W. W., Heck, A. J., et al. (2009). Human Ccr4-Not complexes contain variable deadenylase subunits. Biochem. J. 422, 443-453. doi: 10.1042/BJ20090500
63. Lee, T. I., Wyrick, J. J., Koh, S. S., Jennings, E. G., Gadbois, E. L., and Young, R. A. (1998). Interplay of positive and negative regulators in transcription initiation by RNA polymerase II holoenzyme. Mol. Cell. Biol. 18, 4455-4462.
64. Mahajan, M. A., Murray, A., and Samuels, H. H. (2002). NRC-interacting factor 1 is a novel cotransducer that interacts with and regulates the activity of the nuclear hormone receptor coactivator NRC. Mol. Cell. Biol. 22, 6883-6894. doi: 10.1128/MCB.22.19.6883-6894.2002
65. Maillet, L., Tu, C., Hong, Y. K., Shuster, E. O., and Collart, M. A. (2000). The essential function of Not1 lies within the Ccr4-Not complex. J. Mol. Biol. 303, 131-143. doi: 10.1006/jmbi.2000.4131
66. Maragozidis, P., Karangeli, M., Labrou, M., Dimoulou, G., Papaspyrou, K., Salataj, E., et al. (2012). Alterations of deadenylase expression in acute leukemias: evidence for poly(a)-specific ribonuclease as a potential biomarker. Acta Haematol. 128, 39-46. doi: 10.1159/000337418
67. Mathys, H., Basquin, J., Ozgur, S., Czarnocki-Cieciura, M., Bonneau, F., Aartse, A., et al. (2014). Structural and Biochemical Insights to the Role of the CCR4-NOT Complex and DDX6 ATPase in MicroRNA Repression. Mol. Cell 54, 751-765. doi: 10.1016/j.molcel.2014.03.036
68. Mauxion, F., Faux, C., and Séraphin, B. (2008). The BTG2 protein is a general activator of mRNA deadenylation. EMBO J. 27, 1039-1048. doi: 10.1038/emboj.2008.43
69. Mauxion, F., Prève, B., and Séraphin, B. (2013). C2ORF29/CNOT11 and CNOT10 form a new module of the CCR4-NOT complex. RNA Biol. 10, 267-276. doi:10.4161/rna.23065
70. Mittal, S., Aslam, A., Doidge, R., Medica, R., and Winkler, G. S. (2011). The Ccr4a (CNOT6) and Ccr4b (CNOT6L) deadenylase subunits of the human Ccr4-Not complex contribute to the prevention of cell death and senescence. Mol. Biol. Cell 22, 748-758. doi: 10.1091/mbc.E10-11-0898
71. Morita, M., Suzuki, T., Nakamura, T., Yokoyama, K., Miyasaka, T., and Yamamoto, T. (2007). Depletion of mammalian CCR4b deadenylase triggers elevation of the p27Kip1 mRNA level and impairs cell growth. Mol. Cell. Biol. 27, 4980-4990. doi: 10.1128/MCB.02304-06
72. Morita, M., Oike, Y., Nagashima, T., Kadomatsu, T., Tabata, M., Suzuki, T., et al. (2011). Obesity resistance and increased hepatic expression of catabolism-related mRNAs in Cnot3+/- mice. EMBO J. 30, 4678-4691. doi: 10.1038/emboj.2011.320
73. Morris, J. Z., Hong, A., Lilly, M. A., and Lehmann, R. (2005). twin, a CCR4 homolog, regulates cyclin poly(A) tail length to permit Drosophila oogenesis. Development 132, 1165-1174. doi: 10.1242/dev.01672
74. Moura, R., Pontillo, A., D'Adamo, P., Pirastu, N., Campos Coelho, A., and Crovella, S. (2014) Exome analysis of HIV patients submitted to dendritic cells therapeutic vaccine reveals an association of CNOT1 gene with response to the treatment. J. Int. AIDS Soc. 17:18938. doi: 10.7448/IAS.17.1.18938
75. Mulder, K. W., Winkler, G. S., and Timmers, H. T. (2005). DNA damage and replication stress induced transcription of RNR genes is dependent on the Ccr4-Not complex. Nucleic Acids Res. 33, 6384-6392. doi: 10.1093/nar/gki938
76. Mulder, K. W., Brenkman, A. B., Inagaki, A., van den Broek, N. J, and Timmers, H. T. (2007). Regulation of histone H3K4 tri-methylation and PAF complex recruitment by the Ccr4-Not complex. Nucleic Acids Res. 35, 2428-2439. doi: 10.1093/nar/gkm175
77. Nakamura, T., Yao, R., Ogawa, T., Suzuki, T., Ito, C., Tsunekawa, N., et al., (2004). Oligo-astheno-teratozoospermia in mice lacking Cnot7, a regulator of retinoid X receptor beta. Nat. Genet. 36, 528-533. doi: 10.1038/ng1344
78. Neely, G. G., Kuba, K., Cammarato, A., Isobe, K., Amann, S., Zhang, L., et al. (2010). A global in vivo Drosophila RNAi screen identifies NOT3 as a conserved regulator of heart function. Cell 141, 142-153. doi: 10.1016/j.cell.2010.02.023
79. Newton-Cheh, C., Eijgelsheim, M., Rice, K. M., de Bakker, P. I., Yin, X., Estrada, K. et al. (2009). Common variants at ten loci influence QT interval duration in the QTGEN Study. Nat. Genet. 41, 399-406. doi: 10.1038/ng.364
80. Nousch, M., Techritz, N., Hampel, D., Millonigg, S., and Eckmann, C. R. (2013). The Ccr4-Not deadenylase complex constitutes the main poly(A) removal activity in C. elegans. J. Cell Sci. 126, 4274-4285. doi: 10.1242/jcs.132936
81. Ogami, K., Hosoda, N., Funakoshi, Y., Hoshino, S. (2014). Antiproliferative protein Tob directly regulates c-myc proto-oncogene expression through cytoplasmic polyadenylation element-binding protein CPEB. Oncogene 33, 55-64. doi: 10.1038/onc.2012.548
82. Okazaki, N., Okazaki, K., Watanabe, Y., Kato-Hayashi, M., Yamamoto, M., and Okayama, H. (1998). Novel factor highly conserved among eukaryotes controls sexual development in fission yeast. Mol. Cell. Biol. 18, 887-895.
83. Panepinto, J. C., Heinz, E., and Traven, A. (2013). The cellular roles of Ccr4-NOT in model and pathogenic fungi-implications for fungal virulence. Front. Genet. 4:302. doi: 10.3389/fgene.2013.00302
84. Parker, R., and Sheth, U. (2007). P bodies and the control of mRNA translation and degradation. Mol. Cell 25, 635-646. doi: 10.1016/j.molcel.2007.02.011
85. Paul, P., van den Hoorn, T., Jongsma, M. L., Bakker, M. J., Hengeveld, R., and Janssen,L., et al. (2011). A Genome-wide multidimensional RNAi screen reveals pathways controlling MHC class II antigen presentation. Cell 145, 268-283. doi: 10.1016/j.cell.2011.03.023 Nucleic Acids Res. 40, 11058-11072. doi: 10.1093/nar/gks883
86. Petit, A. P., Wohlbold, L., Bawankar, P., Huntzinger, E., Schmidt, S., Izaurralde, E., et al., (2012). The structural basis for the interaction between the CAF1 nuclease and the NOT1 scaffold of the human CCR4-NOT deadenylase complex. Nucleic Acids Res. 40, 11058-11072. doi: 10.1093/nar/gks883
87. Pfeufer, A., Sanna, S., Arking, D. E., Müller, M., Gateva, V., Fuchsberger, C., et al. (2009). Common variants at ten loci modulate the QT interval duration in the QTSCD Study. Nat. Genet. 41, 407-414. doi: 10.1038/ng.362
88. Poulsen, J. B., Andersen, K. R., Kjær, K. H., Durand, F., Faou, P., Vestergaard, A. L., et al. (2011). Human 2'-phosphodiesterase localizes to the mitochondrial matrix with a putative function in mitochondrial RNA turnover. Nucleic Acids Res. 39, 3754-3770. doi: 10.1093/nar/gkq1282
89. Sakai, A., Chibazakura, T., Shimizu, Y., and Hishinuma, F. (1992). Molecular analysis of POP2 gene, a gene required for glucose-derepression of gene expression in Saccharomyces cerevisiae. Nucleic Acids Res. 20, 6227-6233. doi: 10.1093/nar/20.23.6227
90. Sandler, H., Kreth, J., Timmers, H. T., and Stoecklin, G. (2011). Not1 mediates recruitment of the deadenylase Caf1 to mRNAs targeted for degradation by tristetraprolin. Nucleic Acids Res. 39, 4373-4386. doi: 10.1093/nar/gkr011
91. Schwede, A., Ellis, L., Luther, J., Carrington, M., Stoecklin, G., and Clayton, C. (2008). A role for Caf1 in mRNA deadenylation and decay in trypanosomes and human cells. Nucleic Acids Res. 36, 3374-3388. doi: 10.1093/nar/gkn108
92. Seiden-Long, I. M., Brown, K. R., Shih, W., Wigle, D, A., Radulovich, N., Jurisica, I., et al. (2006). Transcriptional targets of hepatocyte growth factor signaling and Ki-ras oncogene activation in colorectal cancer. Oncogene 25, 91-102. doi: 10.1038/sj.onc.1209005
93. Semotok, J. L., Cooperstock, R. L., Pinder, B. D., Vari, H. K., Lipshitz, H. D., and Smibert, C. A. (2005). Smaug recruits the CCR4/POP2/NOT deadenylase complex to trigger maternal transcript localization in the early Drosophila embryo. Curr. Biol. 15, 284-294. doi: 10.1016/j.cub.2005.01.048
94. Solana, J., Gamberi, C., Mihaylova, Y., Grosswendt, S., Chen, C., Lasko, P., et al. (2013). The CCR4-NOT complex mediates deadenylation and degradation of stem cell mRNAs and promotes planarian stem cell differentiation. PLoS Genet. 9:e1004003. doi: 10.1371/journal.pgen.1004003
95. Suzuki, A., Igarashi, K., Aisaki, K., Kanno, J., and Saga, Y. (2010). NANOS2 interacts with the CCR4-NOT deadenylation complex and leads to suppression of specific RNAs. Proc. Natl. Acad. Sci. U. S. A. 107, 3594-3599. doi: 10.1073/pnas.0908664107
96. Suzuki, A., Saba, R., Miyoshi, K., Morita, Y., and Saga, Y. (2012). Interaction between NANOS2 and the CCR4-NOT deadenylation complex is essential for male germ cell development in mouse. PLoS One 7:e33558. doi: 10.1371/journal.pone.0033558
97. Takahashi, A., Kikuguchi, C., Morita, M., Shimodaira, T., Tokai-Nishizumi, N., Yokoyama, K., et al. (2012). Involvement of CNOT3 in mitotic progression through inhibition of MAD1 expression. Biochem. Biophys. Res. Commun. 419, 268-273. doi: 10.1016/j.bbrc.2012.02.007
98. Tay, Y., Kats, L., Salmena, L., Weiss, D., Tan, S. M., Ala, U., et al. (2011). Coding-independent regulation of the tumor suppressor PTEN by competing endogenous mRNAs. Cell 147, 344-357. doi: 10.1016/j.cell.2011.09.029
99. Temme, C., Zaessinger, S., Meyer, S., Simonelig, M., and Wahle, E. (2004). A complex containing the CCR4 and CAF1 proteins is involved in mRNA deadenylation inDrosophila. EMBO J. 23, 2862-2871. doi: 10.1038/sj.emboj.7600273
100. Temme, C., Zhang, L., Kremmer, E., Ihling, C., Chartier, A., Sinz, A., et al., (2010). Subunits of the Drosophila CCR4-NOT complex and their roles in mRNA deadenylation. RNA 16, 1356-1370. doi: 10.1261/rna.2145110
101. Tucker, M., Valencia-Sanchez, M. A., Staples, R. R., Chen, J., Denis, C. L., and Parker, R. (2001). The transcription factor associated Ccr4 and Caf1 proteins are components of the major cytoplasmic mRNA deadenylase in Saccharomyces cerevisiae. Cell 104, 377-386. doi: 10.1016/S0092-8674(01)00225-2
102. Tucker, M., Staples, R. R., Valencia-Sanchez, M. A., Muhlrad, D., and Parker, R. (2002). Ccr4p is the catalytic subunit of a Ccr4p/Pop2p/Notp mRNA deadenylase complex in Saccharomyces cerevisiae. EMBO J. 21, 1427-1436. doi: 10.1093/emboj/21.6.1427
103. Van Etten, J., Schagat, T. L., Hrit, J., Weidmann, C. A., Brumbaugh, J., Coon, J. J., et al. (2012). Human Pumilio proteins recruit multiple deadenylases to efficiently repress messenger RNAs. J. Biol. Chem. 287, 36370-36383. doi: 10.1074/jbc.M112.373522
104. Venturini, G., Rose, A. M., Shah, A. Z., Bhattacharya, S. S., and Rivolta, C. (2012). CNOT3 is a modifier of PRPF31 mutations in retinitis pigmentosa with incomplete penetrance. PLoS Genet. 8:e1003040. doi: 10.1371/journal.pgen.1003040
105. Wang, H., Morita, M., Yang, X., Suzuki, T., Yang, W., Wang, J., et al. (2010). Crystal structure of the human CNOT6L nuclease domain reveals strict poly(A) substrate specificity. EMBO J. 29, 2566-2576. doi: 10.1038/emboj.2010.152
106. Washio-Oikawa, K., Nakamura, T., Usui, M., Yoneda, M., Ezura, Y., Ishikawa, I., et al. (2007). Cnot7-null mice exhibit high bone mass phenotype and modulation of BMP actions. J. Bone Miner. Res. 22, 1217-1223. doi: 10.1359/JBMR.070411
107. Watanabe, C., Morita, M., Hayata, T., Nakamoto, T., Kikuguchi, C., Li, X. et al. (2014). Stability of mRNA influences osteoporotic bone mass via CNOT3. Proc. Natl. Acad.Sci. U. S. A. 111, 2692-2697. doi: 10.1073/pnas.1316932111
108. Wiederhold, K. and Passmore, L. A. (2010). Cytoplasmic deadenylation: regulation of mRNA fate. Biochem. Soc. Trans. 38, 1531-1536. doi: 10.1042/BST0381531
109. Winkler, G. S., Mulder, K. W., Bardwell, V. J., Kalkhoven, E., and Timmers, H. T. (2006). Human Ccr4-Not complex is a ligand-dependent repressor of nuclear receptor-mediated transcription. EMBO J. 25, 3089-3099. doi: 10.1038/sj.emboj.7601194
110. Winkler, G. S. (2010). The mammalian anti-proliferative BTG/Tob protein family. J. Cell. Physiol. 222, 66-72. doi: 10.1002/jcp.21919
111. Winkler, G. S. and Balacco, D. L. (2013). Heterogeneity and complexity within the nuclease module of the Ccr4-Not complex. Front. Genet. 4:296.
112. Yamashita, A., Chang, T. C., Yamashita, Y., Zhu, W., Zhong, Z., Chen, C. Y. et al. (2005). Concerted action of poly(A) nucleases and decapping enzyme in mammalian mRNA turnover. Nat. Struct. Mol. Biol. 12, 1054-1063. doi: 10.1038/nsmb1016
113. Yang, X., Morita, M., Wang, H., Suzuki, T., Yang, W., Luo, Y., et al., (2008). Crystal structures of human BTG2 and mouse TIS21 involved in suppression of CAF1 deadenylase activity. Nucleic Acids Res. 36, 6872-6881. doi: 10.1093/nar/gkn825
114. Zaessinger, S., Busseau, I., and Simonelig, M. (2006). Oskar allows nanos mRNA translation in Drosophila embryos by preventing its deadenylation by Smaug/CCR4. Development 133, 4573-4583. doi: 10.1242/dev.02649
115. Zheng, X., Dumitru, R., Lackford, B. L., Freudenberg, J. M., Singh, A. P., Archer, T. K., et al. (2012). Cnot1, Cnot2, and Cnot3 maintain mouse and human ESC identity and inhibit extraembryonic differentiation. Stem Cells 30, 910-22. doi: 10.1002/stem.1070
116. Zwartjes, C. G., Jayne, S., van den Berg, D. L., and Timmers, H. T. (2004). Repression of promoter activity by CNOT2, a subunit of the transcription regulatory Ccr4-not complex. J. Biol. Chem. 279, 10848-10854. doi: 10.1074/jbc.M311747200